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Year : 2014  |  Volume : 16  |  Issue : 1  |  Page : 31-38

Oxidative stress and male reproductive health

Priority Research Centre in Reproductive Science, Discipline of Biological Sciences, Faculty of Science and IT, University of Newcastle, Callaghan, NSW 2308, Australia

Date of Submission09-Aug-2013
Date of Decision12-Sep-2013
Date of Acceptance22-Sep-2013
Date of Web Publication16-Dec-2013

Correspondence Address:
Robert J Aitken
Priority Research Centre in Reproductive Science, Discipline of Biological Sciences, Faculty of Science and IT, University of Newcastle, Callaghan, NSW 2308
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/1008-682X.122203

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One of the major causes of defective sperm function is oxidative stress, which not only disrupts the integrity of sperm DNA but also limits the fertilizing potential of these cells as a result of collateral damage to proteins and lipids in the sperm plasma membrane. The origins of such oxidative stress appear to involve the sperm mitochondria, which have a tendency to generate high levels of superoxide anion as a prelude to entering the intrinsic apoptotic cascade. Unfortunately, these cells have very little capacity to respond to such an attack because they only possess the first enzyme in the base excision repair (BER) pathway, 8-oxoguanine glycosylase 1 (OGG1). The latter successfully creates an abasic site, but the spermatozoa cannot process the oxidative lesion further because they lack the downstream proteins (APE1, XRCC1) needed to complete the repair process. It is the responsibility of the oocyte to continue the BER pathway prior to initiation of S-phase of the first mitotic division. If a mistake is made by the oocyte at this stage of development, a mutation will be created that will be represented in every cell in the body. Such mechanisms may explain the increase in childhood cancers and other diseases observed in the offspring of males who have suffered oxidative stress in their germ line as a consequence of age, environmental or lifestyle factors. The high prevalence of oxidative DNA damage in the spermatozoa of male infertility patients may have implications for the health of children conceivedin vitro and serves as a driver for current research into the origins of free radical generation in the germ line.

Keywords: DNA damage; oxidative stress; oxoguanine glycosylase 1; oocyte; spermatozoa

How to cite this article:
Aitken RJ, Smith TB, Jobling MS, Baker MA, De Iuliis GN. Oxidative stress and male reproductive health. Asian J Androl 2014;16:31-8

How to cite this URL:
Aitken RJ, Smith TB, Jobling MS, Baker MA, De Iuliis GN. Oxidative stress and male reproductive health. Asian J Androl [serial online] 2014 [cited 2022 Nov 26];16:31-8. Available from:

  Introduction Top

Male infertility is a relatively common condition affecting approximately 1 in 20 of the male population. In a vast majority of infertile subjects sufficient numbers of spermatozoa are generated to initiate a pregnancy; however, the functionality of the spermatozoa has been compromised. As a result, defective sperm function is held to be the largest, single and defined cause of human infertility. [1] The primary causes of defective sperm function are undoubtedly multifactorial, involving a range of primary genetic, lifestyle and environmental factors, acting alone or, more frequently, in combination. However at the level of the gamete, the integration of these various forces frequently culminates in a state of oxidative stress that impairs the functional and structural integrity of these highly differentiated cells. The first suggestion that oxidative stress might play a role in the etiology of defective sperm function came from one of the pioneers of modern andrology, Dr John MacLeod. [2] He published an important paper in 1943 which demonstrated that in oxygenated medium human spermatozoa rapidly lost motility via mechanisms that could be rescued by the concomitant presence of catalase, a specific scavenger of hydrogen peroxide. The fundamental notion that spermatozoa could generate reactive oxygen species (ROS), specifically hydrogen peroxide, was confirmed by Tosic and Walton in a paper published in Nature in 1946. [3] In this, and a follow-up paper published in 1950, [4] these authors presented impressive biochemical evidence that bovine spermatozoa could not only generate hydrogen peroxide but also that this reactive oxygen metabolite was damaging to sperm function. In this specific case, the authors demonstrated the involvement of an L-amino acid oxidase with a particular affinity for aromatic amino acids such as phenylalanine. Many years later Shannon and Curson [5] confirmed the presence of such an oxidase in bovine spermatozoa and demonstrated that it was the dead cells in any given ejaculate that were particularly active in generating hydrogen peroxide in response to phenylalanine and that the oxidative stress generated in this manner could have an impact on the live cells present in the immediate vicinity. The cytotoxic effect of ROS generated on exposure to the phenylalanine in cryostorage medium could be rescued by the concomitant presence of catalase, confirming hydrogen peroxide as the cytotoxic principle.

The notion that oxidative stress might also be a factor in the etiology of defective sperm function in our species was advanced independently by Aitken and Clarkson [6] and Alvarez et al. [7] in 1987. An important but often overlooked catalyst for this discovery was the development of a technique for objectively measuring sperm function, in the form of the zona-free hamster oocyte penetration assay introduced by another pioneer of modern andrology, Ryuzo Yanagimachi. [8] Up until this point, the field had lacked objective methods for the measurement of human sperm function aside from motility. The hamster oocyte penetration assay provided an objective means of determining the competence of human spermatozoa to capacitate, undergo the acrosome reaction and generate a fusogenic equatorial segment capable of initiating fusion with the vitelline membrane of the oocyte. In the age of intracytoplasmic sperm injection (ICSI), the hamster oocyte model can also provide critical information on the ability of spermatozoa to form a pronucleus. [9],[10],[11] When combined with objective methods for assessing sperm motility, this assay has been shown to give a very accurate assessment of the fertilizing potential of human ejaculates. [12],[13] One of the interesting results secured with this assay was to demonstrate that defective sperm function was evident in infertile men, even when their spermatozoa had been treated with the divalent cation ionophore, A23187 in order to induce an acrosome reaction. [14] This result indicated that whatever the lesions are in defective spermatozoa, they lay downstream of the calcium influx normally triggered when the spermatozoa make contact with the cumulus-oocyte complex.

Such results suggested that there must be some defect in the plasma membrane of functionally compromised human spermatozoa that prevents them from fusing with the vitelline membrane of the oocyte. It was this quest for an explanation of failed membrane fusion in the hamster oocyte assay that led us to the concept that lipid peroxidation was a key factor in the etiology of defective sperm function. Spermatozoa are particularly vulnerable to lipid peroxidation because they contain high concentrations of unsaturated fatty acids, particularly docosahexaenoic acid with six double bonds per molecule. [15] The latter are vulnerable to free radical attack because the carbon hydrogen dissociation energies are lowest at the bisallylic methylene position. As a consequence, the hydrogen abstraction event that initiates lipid peroxidation is promoted, generating a carbon-centered lipid radical that then combines with oxygen to generate peroxyl (ROO•) and alkoxyl (RO•) radicals that, in order to stabilize, abstract hydrogen atoms from adjacent carbons. These chemical reactions create additional lipid radicals that then perpetuate the lipid peroxidation chain reaction, culminating in the generation of small molecular mass electrophilic lipid aldehydes such as 4-hydroxynonenal (4HNE), acrolein and malondialdehyde. Added to this vulnerability, we have shown that sperm mitochondria respond to the presence of free unsaturated fatty acids with a dramatic increase in ROS generation; the greater the level of unsaturation, the greater the level of the stimulatory effect. Esterification of the fatty acid counters this pro-oxidant effect suggesting that it is the amphiphilic properties of these molecules that are central to their ROS-inducing activity, possibly by defining the orientation of the fatty acids in relation to the mitochondrial electron transport chain. In this context, it is significant that defective human spermatozoa possess abnormally high cellular contents of free polyunsaturated fatty acids, the levels of which are positively correlated with mitochondrial superoxide generation. [17]

Thus, defective human spermatozoa are particularly vulnerable to oxidative stress because they contain a superabundance of free unsaturated fatty acids that trigger ROS generation by the sperm mitochondria and induce high levels of lipid peroxidation. To make matters worse, the products of lipid peroxidation in the form of small molecular mass electrophilic aldehydes such as 4HNE or acrolein, are also capable of triggering ROS generation by the sperm mitochondria. [18] This ability of lipid aldehydes generated as a consequence of lipid peroxidation to trigger mitochondrial ROS generation appears to be a function of their capacity to adduct onto proteins in the mitochondrial electron transport chain, such as succinic acid dehydrogenase. [18] As a consequence of these interactions, it is evident that oxidative stress in human spermatozoa is a self-propagating cycle that, once initiated, will inevitably lead to oxidative damage, a loss of functionality and ultimately, cell death [Figure 1].
Figure 1: Proposed cycle of cause and effect by which oxidative stress in the male germ line impacts upon the health and well-being of future generations. (1) A variety of primary factors can initiate oxidative stress in the male germ line including infection, age, obesity and exposure to a variety of adverse environmental influences. (2) This initial oxidative stress induces lipid peroxidation culminating in the production of lipid aldehydes such as 4HNE, which bind to proteins in the mitochondrial electron transport chain, stimulating the generation of reactive oxygen species (ROS). The latter stimulate yet more lipid peroxidation in a self-propagating cycle that culminates in apoptosis. (3) One of the most sensitive targets of oxidative stress is the DNA in the sperm nucleus, generating 8-hydroxy, 2'deoxyguanosine (8OHdG) base adducts. (4) The fi rst enzyme in the base excision repair pathway, 8-oxoguanine glycosylase 1 (OGG1), is present in spermatozoa and its activity creates abasic sites. The remainder of the DNA repair pathway is present in the oocyte. The oocyte has to repair the DNA damage brought into the zygote by the fertilizing spermatozoon before the initiation of S-phase for the fi rst mitotic division. (5) If the oocyte makes a mistake at this stage of DNA repair, it has the potential to create a mutation that will be represented in every cell in the body and could account for the range of pathologies seen in the offspring of fathers exhibiting high levels of oxidative DNA damage in their spermatozoa. Abbreviations: IVF, in vitro fertilization; ROS, reactive oxygen species.

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  Oxidative Stress Sperm Function, DNA Integrity and Cell Death Top

One of the first functions affected by oxidative stress and lipid peroxidation is sperm motility. Correlations between lipid peroxide formation and sperm movement have been repeatedly observed in a variety of different species. [15],[19],[20] Experiments involving exposure of mammalian spermatozoa to a variety of ROS using the xanthine oxidase ROS-generating system have also clearly demonstrated the susceptibility of sperm motility to oxidative attack and identified hydrogen peroxide as the most cytotoxic oxygen metabolite in this context; catalase, but not superoxide dismutase, preventing sperm motility loss under such circumstances. [21],[22],[23],[24] The mechanisms by which motility is lost when spermatozoa are under oxidative stress is not known with certainty, but both oxidative damage to the axoneme and depletion of intracellular adenosine triphosphate (ATP) appear to be involved. [25],[26],[27]

Notwithstanding the dramatic effects that high levels of exposure to ROS have on sperm motility, it is also evident that oxidative stress can compromise the fertilizing capacity of spermatozoa under conditions where motility is normal. [28],[29] Under these circumstances, it is the capacity of the spermatozoa to fuse with the vitelline membrane of the oocyte which is impaired. A careful dose-dependent analysis of the impact of oxidative stress on sperm-oocyte fusion demonstrated a biphasic response which beautifully encapsulates the complex relationship between ROS and sperm function. [30] Thus, at low levels of oxidative stress, sperm-oocyte fusion rates were enhanced, presumably as a consequence of: (i) the positive role that ROS are known to play in driving the tyrosine phosphorylation events associated with sperm capacitation, [31] and (ii) the importance of sterol oxidation in facilitating the efflux of cholesterol from the sperm plasma membrane. [32] However, at higher levels of oxidative stress the induction of lipid peroxidation in the plasma membrane is associated with a decline in the competence for sperm-oocyte fusion, possibly due to the direct induction of oxidative damage to proteins involved in the fusion process, rather than any change in the fluidity of the sperm plasma membrane. [33]

  Oxidative Stress and DNA Damage Top

When human spermatozoa were exposed to increasing levels of hydrogen peroxide it was not just the fertilizing potential of the cells that followed a biphasic pattern of change, the DNA in the sperm nucleus behaved similarly. At low levels of oxidative stress DNA damage was diminished, possibly because of the powerful role played by glutathione peroxidase in effecting the cross linking of sperm chromatin. However, at higher levels of oxidative stress, the sperm chromatin started to fragment. [30] Importantly, the losses of fertilizing potential and DNA integrity occurred at different rates, with the latter being the more sensitive. As a result, spermatozoa that had been driven to a high state of readiness for fertilization by low levels of oxidative stress were also found to exhibit significantly elevated levels of DNA damage. [30] This is an extremely significant observation, since it suggests a mechanism by which environmental influences on the paternal germ line could have a major impact on the health trajectory of any progeny.

The oxidized base adduct, 8-hydroxy, 2′deoxyguanosine (8OHdG), has been used in studies to demonstrate that oxidative DNA damage is significantly elevated in the spermatozoa of patients attending infertility clinics. [34],[35] Furthermore, the levels of 8OHdG expression have been shown to correlate highly with the measurement of DNA damage in spermatozoa, as measured by the TUNEL or sperm chromatin dispersion assays. [34],[36] Indeed, the correlation between 8OHdG formation and DNA damage is so high that we have been forced to conclude that most DNA damage in spermatozoa is oxidatively induced. In order to understand why this would be the case we need to appreciate the particular architecture of human spermatozoa and the major points of difference with somatic cells in terms of the mechanisms regulating apoptosis.

Apoptosis is the default condition for spermatozoa. In the absence of fertilization, most spermatozoa will become senescent and default to an apoptotic state. In somatic cells, apoptosis is associated with extensive nuclear fragmentation as a consequence of nucleases released from the mitochondria (e.g., endonuclease G) or activated in the cytosol (e.g., caspase-activated DNase). However, spermatozoa are distinguished from every other cell type in biology in having a nucleus that is physically separated from the mitochondria and most of the cytoplasm. As a consequence, even when apoptosis is activated in these cells using inhibitors of PI3 kinase such as wortmannin, [37] the nucleases associated with this process remain resolutely locked within the midpiece of the cell and do not penetrate the nuclear compartment [Figure 2]. Thus, even when apoptosis is induced in suspensions of human spermatozoa, the DNA does not become cleaved by nucleases, at least in the short-term. [37] The only products of apoptosis that can damage sperm DNA are the ROS generated by the mitochondria. Mitochondria are potent generators of ROS in spermatozoa and this activity becomes enhanced as soon as the spermatozoa default to an apoptotic state. Indeed mitochondrial ROS generation is one of the first signs that these cells have engaged the intrinsic apoptotic cascade. [37],[38] It is for this reason that most of the DNA damage observed in spermatozoa is oxidative in nature.
Figure 2: The unique architecture of spermatozoa infl uences the impact of apoptosis on DNA integrity. (a) Conventional somatic cells feature a centrally placed nucleus surrounded by mitochondria embedded in the cytoplasm. Under these circumstances, endonucleases activated in the cytoplasm or released from the mitochondria during apoptosis are able to move into the nucleus (arrows) and cleave the DNA. (b) Spermatozoa are completely different from such somatic cells because their mitochondria (stained black) and most of their cytoplasm are located in the midpiece of the cell, physically separated from the nucleus. (c) As a consequence of this compartmentalization key effectors of apoptosis such as apoptosis inducing factor (AIF) or Endonuclease G (Endo G) remain resolutely locked in the sperm midpiece even when apoptosis is induced by the powerful PI3 kinase inhibitor, wortmannin and cannot move into the sperm nucleus. Because of this physical limitation, most DNA damage in mature spermatozoa is induced by membrane permeant reactive oxygen species emanating from the mitochondria, rather than nucleases.

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If nucleases are ever involved, it would be at the very beginning or the very end of sperm existence. During late spermatogenesis, spermatid DNA becomes enzymatically cleaved in order to relieve the torsional stress associated with sperm chromatin compaction. Such endogenous nicks are thought to be resolved by topoisomerase before spermiation, however in pathological cases, such repair mechanisms may be deficient leading to the persistence of nicked DNA into the mature gamete. [39],[40] The possibility that DNA damage in spermatozoa has its origins during spermiation is supported by the profound correlation, which has been observed between DNA fragmentation and chromatin compaction in spermatozoa as detected by chromomycin A3 fluorescence. [34],[41] Viewed in this light, both DNA fragmentation and poor chromatin compaction may be regarded as independent signs of errors in spermiogenesis. An alternative explanation is that these two events are causally related. According to this 'two-step' model, errors in spermiogenesis initially lead to poor chromatin protamination and create a state of vulnerability in the spermatozoa. In the second step, spermatozoa are exposed to oxidative stress from a variety of sources including exposure to exogenous ROS as a consequence of leukocyte infiltration, or endogenous ROS triggered by entry into the intrinsic apoptotic cascade, ultimately resulting in enhanced oxidative DNA damage. Of course, this two-step hypothesis [42],[43] to explain the origins of oxidative DNA damage is not necessarily exclusive of the concept that nuclease-mediated DNA nicks might persist in spermatozoa from late spermatogenesis. Nevertheless, the high correlation that has been observed between oxidative DNA damage and DNA fragmentation suggests that most of the DNA damage is occurring following spermiation as a result of enhanced vulnerability to oxidative stress. [42] The only other time that nucleases may contribute to DNA damage in the male germ line would be at the end of a spermatozoon's life when intracellular nucleases released during the perimortem as the internal structure of these cells starts to break down, or extracellular nucleases released from the male reproductive tract, may aid in the final disposal of these cells by the phagocytic armies of the immune system. [44],[45]

  DNA Repair in Spermatozoa Top

The importance of oxidative stress in the mechanisms by which sperm DNA becomes damaged is also indicated by a consideration of the DNA repair strategies these cells are capable of employing. Incorporated into the subcellular structure of the sperm nucleus and mitochondria is an 8-oxoguanine glycosylase, known as 8-oxoguanine glycosylase 1 (OGG1). [46] When sperm DNA experiences an oxidative attack OGG1 immediately clips the 8OHdG residues out of the DNA generating an abasic site, releasing the oxidized base into the extracellular space. The next enzyme in the base excision repair (BER) pathway, APE1, then incises DNA at the phosphate groups 3' and 5' to the baseless site leaving 3'-OH and 5'- phosphate termini ready for the insertion of a new base. Spermatozoa do not possess this enzyme. [46] As a result, they carry their abasic sites into the oocyte for continuation of the repair process [Figure 1]. For its part, the oocyte engages in a round of DNA repair immediately after fertilization and puts S-phase on hold until this activity has been completed. [47],[48] If the oocyte should make a mistake during the completion of this post-fertilization repair process, it creates the potential for de novo mutations in the offspring which could have a profound impact on the health and well-being of the latter [Figure 1].

  Lifestyle, Age and Oxidative Stress Top

Given this propensity for oxidative damage to sperm DNA and a heavy reliance on OGG1 to cleave out damaged base adducts prior to fertilization, it would not be surprising if factors that impeded OGG1 activity had a profound impact on fertility and the health of progeny. The classic inhibitor of OGG1 activity is cadmium and the latter has a long history of being associated with the etiology of male infertility. [49],[50] Importantly, cadmium exposure has been shown to increase levels of DNA damage in spermatozoa [51] and positive correlations have been observed between 8OHdG levels in spermatozoa and the cadmium concentration in seminal plasma. [52] Since one of the classical sources of cadmium is cigarette smoke, it is also no surprise to learn that men who smoke heavily exhibit significantly elevated levels of oxidative DNA damage in their spermatozoa. [53] Furthermore, the impact of smoking on 8OHdG levels in human spermatozoa is significantly impacted by the presence of Ser326Cys polymorphism in the OGG1 gene. [54] Those individuals with variant Cys/Cys homozygosity for OGG1 showing higher levels of sperm 8OHdG than wildtype homozygote carriers (Ser/Ser). [53] The fact that paternal (not maternal) smoking is associated with a significant increase in the risk of childhood cancer in the offspring [55] is further testimony to the lasting clinical consequences of cigarette smoking and the power of the relationship between oxidative DNA damage in the paternal germ line and the long-term health trajectory of the offspring [Table 1].
Table 1: Summary of factors that are capable of causing oxidative DNA damage in the male germ line and their consequences for the offspring

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If the oxidative DNA damage induced in the germ line as a consequence of smoking can impact on the incidence of cancer in the progeny, then surely any factor capable of inducing oxidative damage in spermatozoa is potentially capable of profoundly influencing the health of children. Furthermore, because there is no particular proposed order to the nature of the DNA damage or aberrant DNA repair in the oocyte, we might anticipate that the range of pathologies generated as a consequence of oxidative stress in the male germ line might be considerable. A case in point is paternal aging. It is well-recognized that as men get older they do not stop producing spermatozoa; however, the quality of their gametes exhibits a progressive age-related decline as indicated by a highly significant, age-dependent increase in sperm DNA damage. [56],[57] Studies on the brown Norway rat indicate that this age-dependent increase in DNA damage in spermatozoa is associated with a concomitant down regulation of genes associated with the BER pathway and a corresponding increase in the levels of oxidative DNA damage in the spermatozoa. [58]

This relationship between paternal age and oxidative DNA damage in spermatozoa has also been indicated by recent studies on the senescence-accelerated mouse prone 8 (SAMP8). This mouse strain contains a suite of naturally occurring mutations resulting in an accelerated senescence phenotype largely mediated by oxidative stress, which is further enhanced by a mutation in the Ogg1 gene, greatly reducing the ability of the enzyme to excise 8OHdG adducts. An analysis of the reproductive phenotype of the SAMP8 males revealed a high level of DNA damage in caudal epididymal spermatozoa as detected by the alkaline Comet assay. Furthermore, these lesions were confirmed to be oxidative in nature, as demonstrated by significant increases in 8OHdG adduct formation in the SAMP8 testicular tissue and mature spermatozoa, relative to a control strain.

If aging is associated with oxidative DNA damage to spermatozoa then we might expect to see these lesions reflected in the incidence of morbidity in the offspring of ageing fathers. In fact, we see three major kinds of paternal age-mediated pathology in the offspring; miscarriage, dominant genetic mutations and complex neurological conditions, as set out in [Table 1]. One of the first paternally-mediated pathologies to be detected was an increase in the incidence of dominant genetic diseases in children as an exponential function of their fathers' age. [59] These diseases classically include achondroplasia, Apert syndrome and multiple endocrine neoplasias. [60] The traditional explanation given for the appearance of these conditions is that they represent the consequences of replication error in the germ line. As men age, their germ cells experience multiple rounds of pre-meiotic replication, and with each cellular iteration, the risk of a mutation occurring as a consequence of replication error correspondingly increases. In certain cases, such as the FGFR2 (fibroblast growth factor receptor 2) mutation associated with Apert syndrome, there does indeed appear to be a correspondence between the incidence of this mutation in spermatozoa and the appearance of the condition in children. [60] However, the underlying cause is not just replication error. [61] The mutations that cause this condition are thought to become over-represented in the sperm population as a consequence of age-dependent clonal expansion; mutant spermatogonial stem cells having a proliferative advantage over non-mutated cells. Recent studies suggest that such mutations occur in clusters within the seminiferous tubules possibly as a consequence of failures of asymmetrical division within the germ line. [60] This germ line selection model may also explain the origins of achondroplasia, [62] although in this case there does appear to be a discrepancy between the incidence of the mutation in spermatozoa and the appearance of the disease in the progeny. [63]

An alternative explanation for paternal age effects may be aberrant repair of oxidative DNA damage in the fertilized oocyte, as suggested above in the context of smoking. [64] Such a mechanism could account for the increase in miscarriage rates observed as a function of paternal age [65] and could also contribute to the etiology of a range of other complex polygenic conditions that correlate with the age of the father at the moment of conception. Thus, paternal age is also associated with an increase in the incidence of complex polygenic neurological conditions in the offspring including epilepsy, spontaneous schizophrenia, bipolar disease and autism, as well as an increased rate of death in the F1 generation associated with congenital malformations, injury and poisoning. [19] An analysis of birth defects has also revealed significant associations between paternal age with the etiology of cleft palate, diaphragmatic hernia, right ventricular outflow tract obstruction and pulmonary valve stenosis. [66] As a result of recent studies conducted on the Icelandic population, there is now powerful incontrovertible evidence that the mutational load carried by children is correlated with the age of their fathers at the moment of conception and that once this load exceeds a certain critical level, overt pathologies such as autism appear in the offspring. [67] The link between this age-dependent increase in mutational load in children and the aberrant repair of oxidative sperm DNA damage in the zygote has yet to be definitively established, however such a relationship appears probable. Furthermore, given the range of environmental and lifestyle factors that can influence oxidative stress in the germ line from pesticides to electromagnetic radiation, [68] the potential contribution of such mechanisms to the integrity of the human genome is significant [Table 1].

Pertinent to this debate is the global increase in the use of assisted reproductive technology (ART) to solve human infertility. In advanced western countries such as Australia, nearly 4% of newborn children are the product of assisted conception therapy. [69] Since many of these conceptions will have been triggered by male factor infertility and the latter involves a high incidence of oxidative DNA damage in the germ line, it is inevitable that conceptions are being achieved in vitro with severely DNA damaged spermatozoa, that could never have occurred in vivo. [70] One of the consequences of this trend is that we might anticipate an increase in disease incidence in children conceived using ART. The emerging data on this point is suggestive but unsubstantiated. Thus, the incidence of birth defects following ART is approximately double the background rate and there is also evidence that imprinting disorders are more frequent in children conceived in vitro. [71],[72] Infants produced by ART are also significantly more likely to be admitted to a neonatal intensive care unit, to be hospitalized and to stay in hospital longer than their naturally conceived counterparts. [19] Recent studies have also shown an increase in the hospitalization of ART offspring in infancy and early childhood compared with spontaneously conceived children, as well as abnormal patterns of retinal vascularization and an increase in the incidence of undescended testicles in boys conceived by ICSI. [73],[74],[75],[76],[77]

Similarly, there are many environmental toxicants (herbicides, pesticides and so on) that will induce oxidative DNA damage in the male germ line and are therefore potential contributors to disease in the offspring. [68] Notwithstanding their possible impact, such transgenerational relationships still remain largely unexplored [Table 1].

  DNA Repair in The Germ Line During Spermatogenesis Top

Most of the above discussion has focused on the impact of oxidative stress at the level of gamete. However, if the oxidative insult is earlier in spermatogenesis, what are the likely consequences for fertility and the health and well-being of the offspring? Under these circumstances, severe oxidative DNA damage in germ cells entering meiosis will simply precipitate an increase in apoptosis. [78] However, milder levels of oxidative stress might induce compensatory mechanisms on the part of the germ line that will favor survival of the offspring. An example of such an effect might be the impact of paternal ageing on telomere length. As discussed above, ageing is associated with oxidative stress in the germ line. One of the ways in which the germ line responds to the stresses associated with ageing is to upregulate telomerase activity and increase the length of telomeres in spermatozoa. [79] Importantly telomere length is a paternally inherited trait and so the offspring of ageing fathers also have longer telomeres. [80] Because telomere length is associated with longevity, [81] one of few positive consequences of having an older father is that he may confer upon his children the molecular basis for a long life. By contrast, if the paternal germ line has experienced an oxidative stress post-meiotically, when telomerase can no longer increase (as is typically the case in infertile patients) then telomere length in the spermatozoa will be abnormally short and the implications for the health of ART offspring, potentially serious. [82]

  Questions from The Panel Top

Q1: Which lifestyle factors may cause oxidative stress?

A1: The factors that we know can cause oxidative stress in the male germ line are age, subfertility and smoking. However, because mitochondrial free radical generation is an early feature of apoptosis in spermatozoa, it is probable that any factor capable of compromising the vitality of male germ cells will initiate a state of oxidative stress. A list of potential factors has been compiled [68] and includes exposure to industrial pollutants such as bisphenol A, insecticides, pesticides, nonionizing electromagnetic radiation, heavy metals and a variety of small molecular mass toxicants, all of which are potentially influenced by interindividual differences in occupation and lifestyle.

Q2: What is known about oxidative stress in the mitochondria of male germ cells including spermatozoa, in response to different types of environmental chemicals (e.g., phthalates, dioxins and so on)? Is there any specificity in such responses?

A2: Any factor that causes oxidative stress in the germ line will automatically trigger mitochondrial ROS generation. It is a central feature of the intrinsic apoptotic cascade. In addition, exposure to free unsaturated fatty acids will trigger this activity by impeding the flow of electrons along the mitochondrial electron transport chain. The physiological significance of this association is indicated by the correlation observed between the spontaneous levels of mitochondrial ROS generation by human spermatozoa and their cellular content of free arachidonic and decosahexaenoic acids. [16],[17] A variety of synthetic and natural electrophiles are also capable of triggering superoxide release from the sperm mitochondria. In this context, the ability of electrophilic aldehydes (e.g., 4HNE, acrolein and malondialdehyde) generated as a consequence of lipid peroxidation to trigger mitochondrial ROS generation is particularly significant. [18] As a consequence of this pathway, any environmental factor that triggers oxidative stress in the germ line will potentiate the generation of further oxidative stress as a direct result of lipid peroxidation. Environmental factors such as dioxins are certainly capable of eliciting ROS generation from sperm mitochondria in an experimental situation. [84],[85] However, whether such toxicants contribute significantly towards the oxidative stress observed in association with male infertility and sperm DNA damage is not currently understood.

Q3: Are earlier stages of spermatogenesis sensitive to ROS, and if so, does oxidative stress during fetal development play a role in the decline in sperm quality?

A3: Whether maternal exposure to reproductive toxicants during pregnancy can cause permanent changes in the germ line that might subsequently impact the fertility of the F1 generation, and the health trajectory of their offspring, is another fascinating question to which we do not yet have a definitive answer. Much will depend on the nature and intensity of the oxidative stress. In general, DNA proof reading and DNA repair in the spermatogonial stem cell population is excellent as indicated by the low risk of birth defects in the children of men with a history of cancer treatment. [86] However, the stability of the sperm epigenome may be less certain. Studies involving the maternal administration of the antiandrogenic endocrine disruptor vinclozolin, have revealed a transgenerational impact on male fertility that is mediated by a long-lasting epigenetic change in the male germ line. [87] That epigenetic changes in the germ line might be associated with impaired semen quality is therefore feasible. Furthermore, oxidative distress is known to alter the pattern of DNA methylation in spermatozoa. [88] However, whether the creation of oxidative stress in the male germ line during fetal life can subsequently influence the fertility of the male offspring, remains an interesting but unresolved possibility.

  Conclusions Top

Oxidative stress is a major pathological mechanism responsible for both male infertility and DNA damage in the germ line. When the oxidative stress occurs in the mature gamete then 8OHdG adducts are created that are excised by OGG1; however, the remainder of the BER pathway is completed in the female germ line. Aberrant or inefficient repair on the part of the oocyte has the potential to create mutations in the offspring that will impact upon the latter's health trajectory. There is strong circumstantial evidence to support such a mechanism in that high levels of oxidative stress in spermatozoa, due to age or smoking, are known to increase the burden-of-disease subsequently carried by the offspring. Mutations in the OGG1 gene are also important contributors in this respect. Direct evidence for this causative mechanism whereby the male and female germ lines collude to increase the mutational load carried by the offspring (oxidative DNA lesions being acquired in the spermatozoa being followed by imperfect or incomplete repair in the oocyte) is currently lacking. Furthermore, we do not yet know whether the range of environmental and lifestyle factors capable of increasing oxidative DNA damage in human spermatozoa (e.g., infertility, obesity, exposure to electromagnetic radiation or environmental toxicants) have the same degree of impact on the mutation rates in the progeny. The role played by the assisted conception industry in facilitating the transfer of damaged DNA to the oocyte as a consequence of the widespread use of ICSI is also worthy of detailed scrutiny.

Finally, we do not know whether oxidative insults during fetal or prepubertal life can have a lasting impact on the genetic integrity of the germ line with implications for the health trajectory of any offspring. Studies addressing the impact of ageing on telomere length in the germ line suggest that early in spermatogenesis, germ cells are capable of exhibiting adaptive responses that may have a positive impact on offspring health. As ever, the impact of oxidative stress on reproduction is a balance of benefit and risk; quantifying the two sides of this delicate equation will be an important task for the future.

  Competing Interests Top

The authors declare that they have no competing interests.

  Acknowledgments Top

We are grateful to the Australian Research Council, National Health and Medical Research Council, the University of Newcastle and the Hunter Medical Research Council for financial support.

  References Top

1.Hull MG, Glazener CM, Kelly NJ, Conway DI, Foster PA, et al. Population study of causes, treatment and outcome of infertility. Br Med J (Clin Res Ed) 1985; 291: 1693-7.  Back to cited text no. 1
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29 Aqueous extract of Pedalium murex D. Royen ex L. leafy stem protects against lead induced testicular toxicity in Wistar rats
Gerard Bessan Dossou-Agoin, Adam Gbankoto, Simon Azonbakin, Razack Osseni, Achille Yemoa, Anatole Lalèyè
Journal of Complementary and Integrative Medicine. 2022; 0(0)
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30 Oxidative stress and iron metabolism in human sperm
Brufman Adriana, Brunori Magali, Raspo Esteban, Grillo Juliana
Pharmacy & Pharmacology International Journal. 2022; 10(5): 185
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31 Biological Activities, Pharmacokinetics and Toxicity of Nootkatone: A Review
Ankush Kumar Jha, Shobhit Gairola, Sourav Kundu, Pakpi Doye, Abu Mohammad Syed, Chetan Ram, Uttam Kulhari, Naresh Kumar, Upadhyayula Suryanarayana Murty, Bidya Dhar Sahu
Mini-Reviews in Medicinal Chemistry. 2022; 22(17): 2244
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32 Seminal Microbiota of Idiopathic Infertile Patients and Its Relationship With Sperm DNA Integrity
Sergio Garcia-Segura, Javier del Rey, Laia Closa, Iris Garcia-Martínez, Carlos Hobeich, Ana Belén Castel, Francisco Vidal, Jordi Benet, Jordi Ribas-Maynou, Maria Oliver-Bonet
Frontiers in Cell and Developmental Biology. 2022; 10
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33 Is oxidative stress evaluated in viable human spermatozoa a marker of good semen quality?
Giulia Traini, Lara Tamburrino, Linda Vignozzi, Elisabetta Baldi, Sara Marchiani
Frontiers in Endocrinology. 2022; 13
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34 The Impact of Oxidative Stress in Male Infertility
Amanda Mannucci, Flavia Rita Argento, Eleonora Fini, Maria Elisabetta Coccia, Niccolò Taddei, Matteo Becatti, Claudia Fiorillo
Frontiers in Molecular Biosciences. 2022; 8
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35 Heavy metals and metalloids exposure and in vitro fertilization: Critical concerns in human reproductive medicine
Cecilia Nwadiuto Obasi, Chiara Frazzoli, Orish Ebere Orisakwe
Frontiers in Reproductive Health. 2022; 4
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36 Potential Use of Tannin Extracts as Additives in Semen Destined for Cryopreservation: A Review
Mohammed S. Liman, Abubeker Hassen, Lyndy J. McGaw, Peter Sutovsky, Dietmar E. Holm
Animals. 2022; 12(9): 1130
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37 Frequency of Semen Collection Affects Ram Sperm Cryoresistance
Cristina Palacin-Martinez, Mercedes Alvarez, Rafael Montes-Garrido, Marta Neila-Montero, Luis Anel-Lopez, Paulino de Paz, Luis Anel, Marta F. Riesco
Animals. 2022; 12(12): 1492
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38 Enzymatic Antioxidant Defense and Polymorphic Changes in Male Infertility
Jedrzej Baszynski, Piotr Kaminski, Maria Bogdzinska, Slawomir Mroczkowski, Marek Szymanski, Karolina Wasilow, Emilia Stanek, Karolina Holderna-Bona, Sylwia Brodzka, Rafal Bilski, Halyna Tkachenko, Natalia Kurhaluk, Tomasz Stuczynski, Malgorzata Lorek, Alina Wozniak
Antioxidants. 2022; 11(5): 817
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39 Association between Seminal Oxidation-Reduction Potential and Sperm DNA Fragmentation—A Meta-Analysis
Manesh Kumar Panner Selvam, Saradha Baskaran, Samantha O’Connell, Wael Almajed, Wayne J. G. Hellstrom, Suresh C. Sikka
Antioxidants. 2022; 11(8): 1563
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40 Vitamin E Lipid-Based Nanodevices as a Tool for Ovine Sperm Protection against Oxidative Stress: Impact on Sperm Motility
Alejandro Jurado-Campos, Pedro Javier Soria-Meneses, María Arenas-Moreira, Carlos Alonso-Moreno, Iván Bravo, Virginia Rodríguez-Robledo, Irene Sánchez-Ajofrín, Ana Josefa Soler, José Julián Garde, María del Rocío Fernández-Santos
Antioxidants. 2022; 11(10): 1988
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41 Fertility Impairment after Trekking at High Altitude: A Proof of Mechanisms on Redox and Metabolic Seminal Changes
Vittore Verratti, Simona Mrakic-Sposta, Jonathan Fusi, Iva Sabovic, Ferdinando Franzoni, Tiziana Pietrangelo, Danilo Bondi, Stefano Dall’Acqua, Simona Daniele, Giorgia Scarfò, Camillo Di Giulio, Andrea Garolla
International Journal of Molecular Sciences. 2022; 23(16): 9066
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42 The relationship between reactive oxygen species, DNA fragmentation, and sperm parameters in human sperm using simplified sucrose vitrification with or without triple antioxidant supplementation
Theesit Juanpanich, Tayita Suttirojpattana, Rangsun Parnpai, Teraporn Vutyavanich
Clinical and Experimental Reproductive Medicine. 2022; 49(2): 117
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43 Cysteine improves boar sperm quality via glutathione biosynthesis during the liquid storage
Zhendong Zhu, Yao Zeng, Wenxian Zeng
Animal Bioscience. 2022; 35(2): 166
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44 Hydrogen peroxide has adverse effects on human sperm quality parameters, induces apoptosis, and reduces survival
DwiAri Pujianto,Mona Oktarina,IdaAyu Sharma Sharaswati,Yulhasri Yulhasri
Journal of Human Reproductive Sciences. 2021; 14(2): 121
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45 Male Infertility: Pathogenetic Significance of Oxidative Stress and Antioxidant Defence (Review)
Vsevolod Koshevoy, Svitlana Naumenko, Pavlo Skliarov, Serhiy Fedorenko, Lidia Kostyshyn
Scientific Horizons. 2021; 24(6): 107
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46 Histopathological and Hormonal Evaluation of Interaction effects of Ethidium Bromide, Nigella sativa, and Silver Nanoparticle on Male Rat Fertility
Ali M. Ethaeb,Sattar J.J. Al-Shaeli,Tamarah H. Ahmed
Research Journal of Pharmacy and Technology. 2021; : 3184
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47 The “Hitchhiker’s Guide to the Galaxy” of Endothelial Dysfunction Markers in Human Fertility
Daniele Santi,Giorgia Spaggiari,Carla Greco,Clara Lazzaretti,Elia Paradiso,Livio Casarini,Francesco Potì,Giulia Brigante,Manuela Simoni
International Journal of Molecular Sciences. 2021; 22(5): 2584
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48 Molecular Consequences of Depression Treatment: A Potential In Vitro Mechanism for Antidepressants-Induced Reprotoxic Side Effects
Przemyslaw Solek, Jennifer Mytych, Anna Tabecka-Lonczynska, Marek Koziorowski
International Journal of Molecular Sciences. 2021; 22(21): 11855
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49 DNA Repair in Haploid Context
Loïs Mourrain, Guylain Boissonneault
International Journal of Molecular Sciences. 2021; 22(22): 12418
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50 Mitochondrial Reactive Oxygen Species (ROS) Production Alters Sperm Quality
Rosanna Chianese,Riccardo Pierantoni
Antioxidants. 2021; 10(1): 92
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51 Hidrox® Counteracts Cyclophosphamide-Induced Male Infertility through NRF2 Pathways in a Mouse Model
Roberta Fusco,Angela Trovato Salinaro,Rosalba Siracusa,Ramona D’Amico,Daniela Impellizzeri,Maria Scuto,Maria Laura Ontario,Roberto Crea,Marika Cordaro,Salvatore Cuzzocrea,Rosanna Di Paola,Vittorio Calabrese
Antioxidants. 2021; 10(5): 778
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52 Vitamin E Delivery Systems Increase Resistance to Oxidative Stress in Red Deer Sperm Cells: Hydrogel and Nanoemulsion Carriers
Alejandro Jurado-Campos, Pedro Javier Soria-Meneses, Francisca Sánchez-Rubio, Enrique Niza, Iván Bravo, Carlos Alonso-Moreno, María Arenas-Moreira, Olga García-Álvarez, Ana Josefa Soler, José Julián Garde, María del Rocío Fernández-Santos
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53 Effects of Sub-Chronic Exposure to Imidacloprid on Reproductive Organs of Adult Male Rats: Antioxidant State, DNA Damage, and Levels of Essential Elements
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54 Multiparametric Study of Antioxidant Effect on Ram Sperm Cryopreservation—From Field Trials to Research Bench
Marta F. Riesco,Mercedes Alvarez,Luis Anel-Lopez,Marta Neila-Montero,Cristina Palacin-Martinez,Rafael Montes-Garrido,Juan Carlos Boixo,Paulino de Paz,Luis Anel
Animals. 2021; 11(2): 283
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55 Effects of Double Layer Centrifugation on the Improvement of Sperm Quality in Dogs: A Comparative Note among Different Breeds
Annals of Veterinary Science. 2021; : 1
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56 Changes in Expressions of Spermatogenic Marker Genes and Spermatogenic Cell Population Caused by Stress
Pengxiang Tian,Zhiming Zhao,Yanli Fan,Na Cui,Baojun Shi,Guimin Hao
Frontiers in Endocrinology. 2021; 12
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57 Sperm a cell in distress: Yoga to the rescue
Vidhu Dhawan,Rajeev Kumar,Neena Malhotra,Vatsla Dadhwal,Dibakar Borthakur,Rima Dada
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58 Oxidative origin of sperm DNA fragmentation in the adult varicocele
Jessica Timóteo Jeremias,Larissa Berloffa Belardin,Fatima Kazue Okada,Mariana P. Antoniassi,Renato Fraietta,Ricardo Pimenta Bertolla,Paula Intasqui
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59 Ameliorative effect of hesperidin on streptozotocin-diabetes mellitus-induced testicular DNA damage and sperm quality degradation in Sprague–Dawley rats
Emrah Hicazi Aksu,Fatih Mehmet Kandemir,Sefa Küçükler
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60 Antioxidant Potential of Parsley Leaf (Petroselinum crispum) Essential Oil on Hypothyroidism and Testicular Injury in Mice Intoxicated by Carbon Tetrachloride
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BioMed Research International. 2021; 2021: 1
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61 The current perspective on genetic and epigenetic factors in sperm maturation in the epididymis
Suheyla Esra Ozkocer,Ece Konac
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62 Supplementation of ram’s semen extender with Mito-TEMPO II: Quality evaluation and flow cytometry study of post-thawed spermatozoa
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63 Developmental programming and ageing of male reproductive function
Elena Zambrano,Peter W. Nathanielsz,Guadalupe L. Rodríguez-González
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64 Sperm donation: an alternative to improve post-ICSI live birth rates in advanced maternal age patients
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65 Mitochondria: their role in spermatozoa and in male infertility
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66 Seminal Plasma Does Not Influence Canine Semen Stored at 5°C for Long-Term Conservation
Michelle Silva Araujo,Otávio Luís de Oliveira Henriques Paulo,Fernanda Paulini,Daniel de Souza Ramos Angrimani,Miriam Harumi Tsunemi,Camila de Paula Freitas DellæAqua,Frederico Ozanam Papa,Fabiana Ferreira de Souza
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67 Aging and oxidative stress alter DNA repair mechanisms in male germ cells of superoxide dismutase-1 null mice
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68 Paternal periconception metabolic health and offspring programming
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69 Effect of varicoceles on spermatogenesis
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70 A review on the Potential Mechanism of Lead Poisoning to the growth and development of ovarian follicle
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71 Age-related changes in human conventional semen parameters and SCSA defined sperm DNA/chromatin integrity
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72 Myristic acid defends against testicular oxidative stress, inflammation, apoptosis: Restoration of spermatogenesis, steroidogenesis in diabetic rats
Ajlaa Sofya Mohd Khalil,Nelli Giribabu,Suseela Yelumalai,Huma Shahzad,Eswar Kumar Kilari,Naguib Salleh
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73 High-fat diet-induced obesity amplifies HSP70-2a and HSP90 expression in testicular tissue; correlation with proliferating cell nuclear antigen (PCNA)
Masoumeh Moradi-Ozarlou,Sana Moshari,Hamed Rezaei Agdam,Amir Nomanzadeh,Simineh Shahmohamadlou,Mazdak Razi
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74 Correlation between the DNA fragmentation index (DFI) and sperm morphology of infertile patients
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Journal of Assisted Reproduction and Genetics. 2021;
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75 The Potential Relationship Between Different Human Female Reproductive Disorders and Sperm Quality in Female Genital Tract
Forough Mahdavinezhad,Roghaye Gharaei,Ahmad Reza Farmani,Farideh Hashemi,Mahsa Kouhestani,Fardin Amidi
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76 Astaxanthin Relieves Busulfan-Induced Oxidative Apoptosis in Cultured Human Spermatogonial Stem Cells by Activating the Nrf-2/HO-1 pathway
Azita Afzali,Fardin Amidi,Morteza Koruji,Hassan Nazari,Mohammad Ali Sadighi Gilani,Aligholi Sobhani Sanjbad
Reproductive Sciences. 2021;
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77 Antioxidant and antiapoptotic paracrine effects of mesenchymal stem cells on spermatogenic arrest in oligospermia rat model
Maha Baligh Zickri,Mohamed Hafez Moustafa,Alaa Essam-Eldin Fasseh,Samaa Samir Kamar
Annals of Anatomy - Anatomischer Anzeiger. 2021; 237: 151750
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78 The mutagenic effect of tobacco smoke on male fertility
Temidayo S. Omolaoye,Omar El Shahawy,Bongekile T. Skosana,Thomas Boillat,Tom Loney,Stefan S du Plessis
Environmental Science and Pollution Research. 2021;
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79 Lycopene protects sperm from oxidative stress in the experimental varicocele model
Atefeh Babaei, Reza Asadpour, Kamran Mansouri, Adel Sabrivand, Siamak Kazemi-Darabadi
Food Science & Nutrition. 2021;
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80 Antioxidant enzymes and association of CAT SNP-21 A/T (rs7943316) with male infertility
Khulah Sadia,Sikandar Sultan,Kifayatullah Khan,Leonel M. Javeres,Baseerat Rumman,Syed T. A. Shah,Sajida Batool,Syed M. Nurulain
Molecular Reproduction and Development. 2021;
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81 Epimedium promotes steroidogenesis by CREB activation-mediated mitochondrial fusion in endosulfan treated leydig cells
Ho-Lin Chuang,V. Bharath Kumar,Cecilia Hsuan Day,Chih-Chu Ho,Tsung-Jung Ho,Ray-Jade Chen,Viswanadha Vijaya Padma,Wei-Wen Kuo,Chih-Yang Huang
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82 Fertility and flow cytometry evaluations of ram frozen semen in plant-based extender supplemented with Mito-TEMPO
Nader Asadzadeh,Zahra Abdollahi,Saeid Esmaeilkhanian,Reza Masoudi
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83 Sperm quality assessment in Ficopomatus enigmaticus (Fauvel, 1923): Effects of selected organic and inorganic chemicals across salinity levels
Alessia Cuccaro,Lucia De Marchi,Matteo Oliva,Matilde Vieira Sanches,Rosa Freitas,Valentina Casu,Gianfranca Monni,Vincenzo Miragliotta,Carlo Pretti
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84 Associations between depression, oxidative stress, and semen quality among 1,000 healthy men screened as potential sperm donors
Yi-Xiang Ye,Heng-Gui Chen,Bin Sun,Ying-Jun Chen,Peng Duan,Tian-Qing Meng,Cheng-Liang Xiong,Yi-Xin Wang,An Pan
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85 Scientific landscape of oxidative stress in male reproductive research: A scientometric study
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Free Radical Biology and Medicine. 2020;
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86 Associations of blood trihalomethanes with semen quality among 1199 healthy Chinese men screened as potential sperm donors
Ying-Jun Chen,Peng Duan,Tian-Qing Meng,Heng-Gui Chen,Jorge E. Chavarro,Cheng-Liang Xiong,An Pan,Yi-Xin Wang,Wen-Qing Lu,Carmen Messerlian
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87 Melatonin improves the motility and DNA integrity of frozen-thawed ram spermatozoa likely via suppression of mitochondrial superoxide production
K.R. Pool,J.P. Rickard,S.P. de Graaf
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88 Toxic effects of arsenic trioxide on spermatogonia are associated with oxidative stress, mitochondrial dysfunction, autophagy and metabolomic alterations
Hanming Chen,Gaoyang Liu,Na Qiao,Zhenlong Kang,Lianmei Hu,Jianzhao Liao,Fan Yang,Congying Pang,Bingxian Liu,Qiwen Zeng,Yao Li,Ying Li
Ecotoxicology and Environmental Safety. 2020; 190: 110063
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89 The Role of Oxidative Stress in Association between Disinfection By-Products Exposure and Semen Quality: A Mediation Analysis among Men from an Infertility Clinic
Min Zhang,Chong Liu,Fei-Peng Cui,Pan-Pan Chen,Yan-Ling Deng,Qiong Luo,Yu Miao,Sheng-Zhi Sun,Yu-Feng Li,Wen-Qing Lu,Qiang Zeng
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90 Effects of freezing extender supplementation with mitochondria-targeted antioxidant Mito-TEMPO on frozen-thawed rooster semen quality and reproductive performance
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Animal Reproduction Science. 2020; : 106671
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91 Quercetin supplemented casein-based extender improves the post-thaw quality of rooster semen
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92 Supplementation of ramæs semen extender with Mito-TEMPO I: Improvement in quality parameters and reproductive performance of cooled-stored semen
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93 Obesity-related genes are expressed in human Sertoli cells and modulated by energy homeostasis regulating hormones
Sara C. Pereira,Ana C. Martins,Bruno P. Moreira,Raquel L. Bernardino,Alberto Barros,Mariana P. Monteiro,Pedro F. Oliveira,Marco G. Alves
Journal of Cellular Physiology. 2020;
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94 Covariation in superoxide, sperm telomere length and sperm velocity in a polymorphic reptile
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Behavioral Ecology and Sociobiology. 2020; 74(6)
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95 Effect of Folic Acid and Zinc Supplementation in Men on Semen Quality and Live Birth Among Couples Undergoing Infertility Treatment
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96 Multiparameter Flow Cytometry Assay for Analysis of Nitrosative Stress Status in Human Spermatozoa
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97 Flow Cytometry of Male Reproductive Potential
Kewal Asosingh
Cytometry Part A. 2020;
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98 Increased Sperm DNA Fragmentation in Infertile Men with Varicocele: Relationship with Apoptosis, Seminal Oxidative Stress, and Spermatic Parameters
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99 Downregulation of gene expression and the outcome of ICSI in severe oligozoospermic patients: A preliminary study
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100 Relevance of seminal F2-dihomo-IsoPs, F2-IsoPs and F4-NeuroPs in idiopathic infertility and varicocele
Mariangela Longini,Elena Moretti,Cinzia Signorini,Daria Noto,Francesca Iacoponi,Giulia Collodel
Prostaglandins & Other Lipid Mediators. 2020; : 106448
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101 Could leptin be responsible for the reproductive dysfunction in obese men?
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Reproductive Biology. 2020;
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102 Dietary flaxseed oil improve boar semen quality, antioxidant status and in-vivo fertility in humid sub-tropical region of North East India
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103 Association of the serum metabolomic profile by nuclear magnetic resonance spectroscopy with sperm parameters: a cross-sectional study of 325 men
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104 Effects and mechanisms of pyrethroids on male reproductive system
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105 Successful sperm cryopreservation in Egyptian spiny mice Acomys cahirinus
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106 Transcriptional alterations of genes related to fertility decline in male rats induced by chronic sleep restriction
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Systems Biology in Reproductive Medicine. 2020; : 1
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107 Effect of epigallocatechin-3-gallate (EGCG) on embryos inseminated with oxidative stress-induced DNA damage sperm
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108 Metabolic diseases affect male reproduction and induce signatures in gametes that may compromise the offspring health
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109 Advanced sperm testing
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110 Antioxidant effects of penicillamine against in vitro-induced oxidative stress in human spermatozoa
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111 The role of infections and leukocytes in male infertility
Ralf Henkel,Ugochukwu Offor,David Fisher
Andrologia. 2020;
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112 Teratozoospermia: Its association with sperm DNA defects, apoptotic alterations, and oxidative stress
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113 The effects of functionalization of carbon nanotubes on toxicological parameters in mice
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114 Are specialized sperm function tests clinically useful in planning assisted reproductive technology?
Sandro C. Esteves
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115 Laboratory assessment of sperm apoptosis ability in men with different fertility
M.V. Ploskonos,D.F. Zulbalaeva,N.R. Kurbangalieva,S.V. Ripp
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116 Sperm DNA fragmentation is a necessity for modern clinical practice
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117 The effect of pre- and postnatal exposure to a mixture of daidzein and genistein on the reproductive system of male rats
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118 Ambient sulfur dioxide could have an impact on testicular volume from a observational study on a population of infertile male
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BMC Urology. 2020; 20(1)
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119 Effects of Qilin pills on spermatogenesis, reproductive hormones, oxidative stress, and the TSSK2 gene in a rat model of oligoasthenospermia
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120 Reactive Oxygen Species Secreted by Leukocytes in Semen Induce Self-Expression of Interleukin-6 and Affect Sperm Quality
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American Journal of Men's Health. 2020; 14(5): 1557988320
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121 Low Dose of Genistein Alleviates Mono-(2-Ethylhexyl) Phthalate-Induced Fetal Testis Disorder Based on Organ Culture Model
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Oxidative Medicine and Cellular Longevity. 2020; 2020: 1
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122 FTIR Spectroscopy to Reveal Lipid and Protein Changes Induced on Sperm by Capacitation: Bases for an Improvement of Sample Selection in ART
Maria Pachetti,Luisa Zupin,Irene Venturin,Elisa Mitri,Rita Boscolo,Francesco D’Amico,Lisa Vaccari,Sergio Crovella,Giuseppe Ricci,Lorella Pascolo
International Journal of Molecular Sciences. 2020; 21(22): 8659
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123 Catalase as a Molecular Target for Male Infertility Diagnosis and Monitoring: An Overview
Nuria Rubio-Riquelme,Natalia Huerta-Retamal,María José Gómez-Torres,Rosa María Martínez-Espinosa
Antioxidants. 2020; 9(1): 78
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124 Molecular Changes Induced by Oxidative Stress that Impair Human Sperm Motility
Karolina Nowicka-Bauer,Brett Nixon
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125 Oxidative Stress in Male Infertility: Causes, Effects in Assisted Reproductive Techniques, and Protective Support of Antioxidants
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Biology. 2020; 9(4): 77
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126 Oxidative Stress and Reproductive Function in the Aging Male
Paulina Nguyen-Powanda,Bernard Robaire
Biology. 2020; 9(9): 282
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127 Cichorium intybus L. extract ameliorates testicular oxidative stress induced by lead acetate in male rats
Mehran Dorostghoal,Seyyed Mansour Seyyednejad,Marzieh Noroozi Tabrizi Nejad
Clinical and Experimental Reproductive Medicine. 2020; 47(3): 161
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128 Rutin ameliorates carbon tetrachloride (CCl4)-induced hepatorenal toxicity and hypogonadism in male rats
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129 Telomere Dynamics Throughout Spermatogenesis
Heather Fice,Bernard Robaire
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130 Cancer Chemotherapy and Chemiluminescence Detection of Reactive Oxygen Species in Human Semen
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Antioxidants. 2019; 8(10): 449
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131 Soy Isoflavones Improve the Spermatogenic Defects in Diet-Induced Obesity Rats Through Nrf2/HO-1 Pathway
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132 Antibiotics Versus Natural Biomolecules: The Case of In Vitro Induced Bacteriospermia by Enterococcus Faecalis in Rabbit Semen
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133 DNA methylation patterns vary in boar sperm cells with different levels of DNA fragmentation
Abdolrahman Khezri,Birgitte Narud,Else-Berit Stenseth,Anders Johannisson,Frøydis Deinboll Myromslien,Ann Helen Gaustad,Robert C. Wilson,Robert Lyle,Jane M. Morrell,Elisabeth Kommisrud,Rafi Ahmad
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134 SRXN1 Is Necessary for Resolution of GnRH-Induced Oxidative Stress and Induction of Gonadotropin Gene Expression
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135 Improvement of sperm motility within one month under selenium and vitamin E supplementation in four infertile dogs with low selenium status
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136 Nigella sativa L. (Black Cumin): A Promising Natural Remedy for Wide Range of Illnesses
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137 Testicular Toxicity of Water Pipe Smoke Exposure in Mice and the Effect of Treatment with Nootkatone Thereon
Badreldin H. Ali,Suhail Al-Salam,Sirin A. Adham,Khalid Al Balushi,Mohammed Al Zaæabi,Sumaya Beegam,Priya Yuvaraju,Priyadarsini Manoj,Abderrahim Nemmar
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138 Evaluation of Male Fertility-Enhancing Activities of Water Seed Extract of Hunteria umbellata in Wistar Rats
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Evidence-Based Complementary and Alternative Medicine. 2019; 2019: 1
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139 Orchestrating the antioxidant defenses in the epididymis
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140 Dark side of the epididymis: tails of sperm maturation
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141 An update on clinical and surgical interventions to reduce sperm DNA fragmentation in infertile men
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142 Leptin and reproductive dysfunction in obese men
Fayez A. Almabhouh,Amir Hafidz Md Mokhtar,Ifrah Alam Malik,Noor Azean Anis Abdul Aziz,Damayanthi Durairajanayagam,Harbindar Jeet Singh
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143 Effect of aspirin on semen quality: A review
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144 Sperm cryopreservation reduces offspring growth
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145 Deficiency of X-ray repair cross-complementing group 1 in primordial germ cells contributes to male infertility
Cheng Xu,Jin Xu,Guixiang Ji,Qian Liu,Wentao Shao,Yaoyao Chen,Jie Gu,Zhenkun Weng,Xin Zhang,Yubang Wang,Aihua Gu
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146 Experimental manipulation of reproductive tactics in Seba’s short-tailed bats: consequences on sperm quality and oxidative status
Magali Meniri,Florence Gohon,Ophélie Gning,Gaétan Glauser,Armelle Vallat,Nicolas J Fasel,Fabrice Helfenstein,Zhi-Yun JIA
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147 Physical activity and sedentary time in relation to semen quality in healthy men screened as potential sperm donors
Bin Sun,Carmen Messerlian,Zhong-Han Sun,Peng Duan,Heng-Gui Chen,Ying-Jun Chen,Peng Wang,Liang Wang,Tian-Qing Meng,Qi Wang,Mariel Arvizu,Jorge E Chavarro,Yi-Xin Wang,Cheng-Liang Xiong,An Pan
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148 Should the current guidelines for the treatment of varicoceles in infertile men be re-evaluated?
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149 The relationship among sperm global DNA methylation, telomere length, and DNA fragmentation in varicocele: a cross-sectional study of 20 cases
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150 The relationship of body condition, superoxide dismutase, and superoxide with sperm performance
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151 The effects of silver nanoparticles exposure on the testicular antioxidant system during pre-pubertal rat stage
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152 Effects of clothianidin on antioxidant enzyme activities and malondialdehyde level in honey bee drone semen
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153 Potential effect of advanced glycation end products (AGEs) on spermatogenesis and sperm quality in rodents
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154 Whole-body exposures to radiofrequency-electromagnetic energy can cause DNA damage in mouse spermatozoa via an oxidative mechanism
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155 Experimental exposure to gasohol impairs sperm quality with recognition of the classification pattern of exposure groups by machine learning algorithms
Kátia Cristina de Melo Tavares Vieira,Andressa Ágata Fernandes,Karina Martins Silva,Viviane Ribas Pereira,Danillo Roberto Pereira,Ana Paula Alves Favareto
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156 The triple role of glutathione S-transferases in mammalian male fertility
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157 Bisphenol AF compromises blood-testis barrier integrity and sperm quality in mice
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158 Effects of CoQ10 on the quality of ram sperm during cryopreservation in plant and animal based extenders
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159 Herbal yeast product, Equi-Strath®, alters the antioxidant status of stallion semen
Anette van Dorland,Fredi Janett,Rupert Bruckmaier,Lucyna Wach-Gygax,Elise Jeannerat,Heiner Bollwein,Harald Sieme,Dominik Burger
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160 Mediation of the relationship between phthalate exposure and semen quality by oxidative stress among 1034 reproductive-aged Chinese men
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161 The genomic effects of cell phone exposure on the reproductive system
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162 The sperm mitochondrion: Organelle of many functions
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163 Cinnamtannin B-1, a novel antioxidant for sperm in red deer
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164 Supplementation of extender with coenzyme Q10 improves the function and fertility potential of rooster spermatozoa after cryopreservation
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165 In Utero and Postnatal Exposure to High Fat, High Sucrose Diet Suppressed Testis Apoptosis and Reduced Sperm Count
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166 Shedding light into the relevance of telomeres in human reproduction and male factor infertility†
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167 Association between expression of TNF-a, P53 and HIF1a with asthenozoospermia
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168 Vitamin E and vitamin C attenuate Di-(2-ethylhexyl) phthalate-induced blood-testis barrier disruption by p38 MAPK in immature SD rats
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169 Sperm mitochondrial DNA measures and semen parameters among men undergoing fertility treatment
Haotian Wu,Alexandra M. Huffman,Brian W. Whitcomb,Srinihaari Josyula,Suzanne Labrie,Ellen Tougias,Tayyab Rahil,Cynthia K. Sites,J Richard Pilsner
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170 Birth characteristics in men with infertility
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171 Reactive Oxygen Species in Seminal Plasma as a Cause of Male Infertility
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172 Soluble protein fraction of human seminal plasma
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173 Accuracy of human sperm DNA oxidation quantification and threshold determination using an 8-OHdG immuno-detection assay
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174 Evidence that fertility trades off with early offspring fitness as males age
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175 Association of polymorphisms in genes coding for antioxidant enzymes and human male infertility
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176 Effect of in vitro vitamin E (alpha-tocopherol) supplementation in human spermatozoon submitted to oxidative stress
L. N. G. Adami,L. B. Belardin,B. T. Lima,J. T. Jeremias,M. P. Antoniassi,F. K. Okada,R. P. Bertolla
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177 Proteomic analysis of sperm proteins in infertile men with high levels of reactive oxygen species
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178 Selenium and vitamin E supplementation enhances the antioxidant status of spermatozoa and improves semen quality in male dogs with lowered fertility
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179 Comparison of enhanced male mice sexual function among three medicinal materials
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180 Paternal factors and embryonic development: Role in recurrent pregnancy loss
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181 Effect of orchiectomy on sperm functional aspects and semen oxidative stress in men with testicular tumours
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182 Effects of ascorbic acid 2-glucoside and alpha-tocopherol on the characteristics of equine spermatozoa stored at 5°C
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183 Stallion semen quality depends on major histocompatibility complex matching to teaser mare
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184 Effects of the supplementation with an high-polyphenols extra-virgin olive oil on kinetic sperm features and seminal plasma oxidative status in healthy dogs
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185 Total antioxidant capacity and protein peroxidation intensity in seminal plasma of infertile and fertile dogs
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186 In vivo analysis of Bisphenol A induced dose-dependent adverse effects in cauda epididymis of mice
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187 Acrosome reaction and chromatin integrity as additional parameters of semen analysis to predict fertilization and blastocyst rates
Pamela Tello-Mora,Leticia Hernández-Cadena,Jeimy Pedraza,Esther López-Bayghen,Betzabet Quintanilla-Vega
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188 Incubation of human sperm with micelles made from glycerophospholipid mixtures increases sperm motility and resistance to oxidative stress
Gonzalo Ferreira,Carlos Costa,Verónica Bassaizteguy,Marcelo Santos,Romina Cardozo,José Montes,Robert Settineri,Garth L. Nicolson,Joël R Drevet
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189 Genistein attenuates di-(2-ethylhexyl) phthalate-induced testicular injuries via activation of Nrf2/HO-1 following prepubertal exposure
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190 Probing the Origins of 1,800 MHz Radio Frequency Electromagnetic Radiation Induced Damage in Mouse Immortalized Germ Cells and Spermatozoa in vitro
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191 DNA Damage and Repair in Human Reproductive Cells
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192 A Cellular Perspective on the Importance of Oxidative Stress Effects on Sperm
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194 Seminal reactive oxygen species and total antioxidant capacity: Correlations with sperm parameters and impact on male infertility
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195 Probiotic administration improves sperm quality in asthenozoospermic human donors
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196 Pleurotus tuber-regium mushrooms in the diet of rats ameliorates reproductive and testicular injury caused by carbon tetrachloride
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197 Clusterin in the mouse epididymis: possible roles in sperm maturation and capacitation
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198 Chrysin Administration Protects against Oxidative Damage in Varicocele-Induced Adult Rats
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199 DNA Repair Mechanism Gene, XRCC1A (Arg194Trp) but not XRCC3 (Thr241Met) Polymorphism Increased the Risk of Breast Cancer in Premenopausal Females: A Case–Control Study in Northeastern Region of India
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200 Could vitamin C and zinc chloride protect the germ cells against sodium arsenite?
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201 Study on testicular response to prolong artemisinin-based combination therapy treatments in guinea pigs
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202 A multicenter study to evaluate oxidative stress by oxidation-reduction potential, a reliable and reproducible method
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203 The diagnosis of male infertility: an analysis of the evidence to support the development of global WHO guidance—challenges and future research opportunities
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204 Comparative investigation of methionine and novel formulation Metovitan protective effects in Wistar rats with testicular and epididymal toxicity induced by anti-tuberculosis drugs co-administration
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205 Sperm DNA fragmentation in miscarriage – a promising diagnostic, or a test too far?
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206 Response: nitroblue tetrazolium (NBT) assay
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207 Specific activity of Korean red ginseng saponin and non-saponin fractions in ageing-induced rat testicular dysfunction
Spandana Rajendra Kopalli,Kyu-Min Cha,Ji-Hoon Ryu,Seock-Yeon Hwang,Si-Kwan Kim
Journal of Functional Foods. 2017; 29: 226
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208 Relationship between serum dioxin-like polychlorinated biphenyls and post-testicular maturation in human sperm
Raiza Paul,Julia Moltó,Nuria Ortuño,Alejandro Romero,Carlos Bezos,Jon Aizpurua,María José Gómez-Torres
Reproductive Toxicology. 2017;
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209 Effects of Treatment with Nauclea latifolia Root Decoction on Sexual Behavior and Reproductive Functions in Male Rabbits
Quadri Kunle Alabi,Olaoluwa Sesan Olukiran,Modinat Adebukola Adefisayo,Benson Akinloye Fadeyi
Journal of Dietary Supplements. 2017; : 1
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210 Oxidative stress and male infertility
Shilpa Bisht,Muneeb Faiq,Madhuri Tolahunase,Rima Dada
Nature Reviews Urology. 2017;
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211 SLY regulates genes involved in chromatin remodeling and interacts with TBL1XR1 during sperm differentiation
Charlotte Moretti,Maria-Elisabetta Serrentino,Côme Ialy-Radio,Marion Delessard,Tatiana A Soboleva,Frederic Tores,Marjorie Leduc,Patrick Nitschké,Joel R Drevet,David J Tremethick,Daniel Vaiman,Ayhan Kocer,Julie Cocquet
Cell Death and Differentiation. 2017; 24(6): 1029
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212 Inverse association between ambient sulfur dioxide exposure and semen quality in Wuhan, China
Yuewei Liu,Yun Zhou,Jixuan Ma,Wei Bao,Jingjing Li,Ting Zhou,Xiuqing Cui,Zhe Peng,Hai Zhang,Min Feng,Yuan Yuan,Yuanqi Chen,Xiji Huang,Yonggang Li,Yonggang Duan,Tingming Shi,Lei Jin,Li Wu
Environmental Science & Technology. 2017;
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213 Quality of seminal fluids varies with type of stimulus at ejaculation
E. Jeannerat,F. Janett,H. Sieme,C. Wedekind,D. Burger
Scientific Reports. 2017; 7: 44339
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214 Attenuation of perfluorooctanoic acid-induced testicular oxidative stress and apoptosis by quercetin in mice
Yangyang Yuan,Shuna Ge,Zehui Lv,Mei Wu,Haibin Kuang,Bei Yang,Jianhua Yang,Lei Wu,Weiying Zou,Dalei Zhang
RSC Adv.. 2017; 7(71): 45045
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215 Effect of reduced glutathione supplementation in semen extender on tyrosine phosphorylation and apoptosis like changes in frozen thawed Hariana bull spermatozoa
Nadeem Shah,Vijay Singh,Hanuman Prasad Yadav,Meena Verma,Dharmendra Singh Chauhan,Atul Saxena,Sarvajeet Yadav,Dilip Kumar Swain
Animal Reproduction Science. 2017; 182: 111
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216 Hyaluronic acid improves frozen-thawed sperm quality and fertility potential in rooster
Saied Lotfi,Morteza Mehri,Mohsen Sharafi,Reza Masoudi
Animal Reproduction Science. 2017; 184: 204
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217 Inter-and Intra-Laboratory Standardization of TUNEL Assay for Assessment of Sperm DNA Fragmentation
Sajal Gupta,Rakesh Sharma,Ashok Agarwal
Current Protocols in Toxicology. 2017; 74(1)
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218 Plasma membrane calcium ATPase 4 (PMCA4) co-ordinates calcium and nitric oxide signaling in regulating murine sperm functional activity
Kristine E. Olli,Kun Li,Deni S. Galileo,Patricia A. Martin-DeLeon
Journal of Cellular Physiology. 2017;
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219 The AhRR-c.565C>G transversion may increase total antioxidant capacity levels of the seminal plasma in infertile men
Gholam Ali Josarayi,Azadeh Mohammad-Hasani,Younes Aftabi,Emadodin Moudi,Abasalt Hosseinzadeh Colagar
Environmental Science and Pollution Research. 2017;
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220 Actions and mechanisms of reactive oxygen species and antioxidative system in semen
Shan Gao,Chunjin Li,Lu Chen,Xu Zhou
Molecular & Cellular Toxicology. 2017; 13(2): 143
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221 Effects of aging on the male reproductive system
Sezgin Gunes,Gulgez Neslihan Taskurt Hekim,Mehmet Alper Arslan,Ramazan Asci
Journal of Assisted Reproduction and Genetics. 2016;
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222 Condition-dependent ejaculate production affects male mating behavior in the common bedbugCimex lectularius
Bettina Kaldun,Oliver Otti
Ecology and Evolution. 2016; : n/a
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223 Dynamic changes in the sperm quality ofMytilus galloprovincialisunder continuous thermal stress
Raffaele Boni,Alessandra Gallo,Melania Montanino,Alberto Macina,Elisabetta Tosti
Molecular Reproduction and Development. 2016; 83(2): 162
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224 Paternal contribution to development: sperm genetic damage and repair in fish
María Paz Herráez,Juan Ausió,Alain Devaux,Silvia González-Rojo,Cristina Fernández-Díez,Sylvie Bony,Núria Saperas,Vanesa Robles
Aquaculture. 2016;
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225 Resveratrol prevents oxidative damage and loss of sperm motility induced by long-term treatment with valproic acid in Wistar rats
Giovana M. Ourique,Tanise S. Pês,Etiane M.H. Saccol,Isabela A. Finamor,Werner G. Glanzner,Bernardo Baldisserotto,Maria A. Pavanato,Paulo B.D. Gonçalves,Kátia P. Barreto
Experimental and Toxicologic Pathology. 2016;
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226 Causes and consequences of oxidative stress in spermatozoa
Robert John Aitken,Zamira Gibb,Mark A. Baker,Joel Drevet,Parviz Gharagozloo
Reproduction, Fertility and Development. 2016; 28(2): 1
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227 Argirein alleviates stress-induced and diabetic hypogonadism in rats via normalizing testis endothelin receptor A and connexin 43
Ming Xu,Chen Hu,Hussein-hamed Khan,Fang-hong Shi,Xiao-dong Cong,Qing Li,Yin Dai,De-zai Dai
Acta Pharmacologica Sinica. 2016; 37(2): 246
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228 Does murine spermatogenesis require WNT signalling? A lesson from Gpr177 conditional knockout mouse models
Su-Ren Chen,J-X Tang,J-M Cheng,X-X Hao,Y-Q Wang,X-X Wang,Y-X Liu
Cell Death and Disease. 2016; 7(6): e2281
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229 Epigenetics in male reproduction: effect of paternal diet on sperm quality and offspring health
Undraga Schagdarsurengin,Klaus Steger
Nature Reviews Urology. 2016;
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230 Follicular fluid lipid peroxidation levels in women with endometriosis during controlled ovarian hyperstimulation
Camila Bruna de Lima,Fernanda Bertuccez Cordeiro,Mariana Camargo,Daniel Suslik Zylbersztejn,Agnaldo Pereira Cedenho,Ricardo Pimenta Bertolla,Edson Guimarães Lo Turco
Human Fertility. 2016; : 1
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231 Pitfalls and promises in FTIR spectromicroscopy analyses to monitor iron-mediated DNA damage in sperm
Lorella Pascolo,Diana E. Bedolla,Lisa Vaccari,Irene Venturin,Francesca Cammisuli,Alessandra Gianoncelli,Elisa Mitri,Elena Giolo,Stefania Luppi,Monica Martinelli,Marina Zweyer,Giuseppe Ricci
Reproductive Toxicology. 2016; 61: 39
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232 New flow cytometry approaches in equine andrology
Fernando J. Peña,Cristina Ortega Ferrusola,Patricia Martín Muñoz
Theriogenology. 2016;
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233 Selección espermática in vitro: espermatozoides con mejores características funcionales
Paula Cristina Lalinde Acevedo,Walter Darío Cardona Maya
Urología Colombiana. 2016;
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234 La eyaculación frecuente mejora la morfología espermática: reporte de caso
Paula Cristina Lalinde Acevedo,Alejandro Carvajal,Walter Darío Cardona Maya
Urología Colombiana. 2016;
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235 Exposure to 2,4-dichlorophenoxyacetic acid induces oxidative stress and apoptosis in mouse testis
Dalei Zhang,Yaling Wu,Yangyang Yuan,Wenwen Liu,Haibin Kuang,Jianhua Yang,Bei Yang,Lei Wu,Weiying Zou,Changshui Xu
Pesticide Biochemistry and Physiology. 2016;
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236 Flow Cytometry Probes to Evaluate Stallion Spermatozoa
Fernando J. Peña,Patricia Martin Muñoz,Cristina Ortega Ferrusola
Journal of Equine Veterinary Science. 2016;
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237 A novel antioxidant formulation designed to treat male infertility associated with oxidative stress: promising preclinical evidence from animal models
P. Gharagozloo,A. Gutiérrez-Adán,A. Champroux,A. Noblanc,A. Kocer,A. Calle,S. Pérez-Cerezales,E. Pericuesta,A. Polhemus,A. Moazamian,J.R. Drevet,R.J. Aitken
Human Reproduction. 2016; 31(2): 252
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238 Effect of brain-derived neurotrophic factor on sperm function, oxidative stress and membrane integrity in human
A. Najafi,F. Amidi,M. A. Sedighi Gilani,A. R. Moawad,E. Asadi,N. Khanlarkhni,P. Fallah,Z. Rezaiian,A. Sobhani
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239 Are oxidative stress markers associated with unexplained male infertility?
B. J. M. Mayorga-Torres,M. Camargo,Á. P. Cadavid,S. S. du Plessis,W. D. Cardona Maya
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240 The intracellular concentration of homocysteine and related thiols is negatively correlated to sperm quality after highly effective method of sperm lysis
M. Kralikova,I. Crha,M. Huser,J. Melounova,J. Zakova,M. Matejovicova,P. Ventruba
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241 Effects of treatment with Hypoxis hemerocallidea extract on sexual behaviour and reproductive parameters in male rats
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242 Involvement of homocysteine, homocysteine thiolactone, and paraoxonase type 1 (PON-1) in the etiology of defective human sperm function
R. J. Aitken,H. M. Flanagan,H. Connaughton,S. Whiting,A. Hedges,M. A. Baker
Andrology. 2016; : n/a
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243 Determination of testicular function in adolescents with varicocoele - a proteomics approach
P. T. Del Giudice,L. B. Belardin,M. Camargo,D. S. Zylbersztejn,V. M. Carvalho,K. H. M. Cardozo,R. P. Bertolla,A. P. Cedenho
Andrology. 2016; 4(3): 447
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244 Semen leukocytes and oxidative-dependent DNA damage of spermatozoa in male partners of subfertile couples with no symptoms of genital tract infection
A. Micillo,M. R. C. Vassallo,G. Cordeschi,S. DæAndrea,S. Necozione,F. Francavilla,S. Francavilla,A. Barbonetti
Andrology. 2016;
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245 Analysis of the functional aspects and seminal plasma proteomic profile of sperm from smokers
Mariana Pereira Antoniassi,Paula Intasqui,Mariana Camargo,Daniel Suslik Zylbersztejn,Valdemir Melechco Carvalho,Karina H. M. Cardozo,Ricardo Pimenta Bertolla
BJU International. 2016; 118(5): 814
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246 Melatonin promotes development of haploid germ cells from early developing spermatogenic cells ofSuffolksheep under in vitro condition
Shou-Long Deng,Su-Ren Chen,Zhi-Peng Wang,Yan Zhang,Ji-Xin Tang,Jian Li,Xiu-Xia Wang,Jin-Mei Cheng,Cheng Jin,Xiao-Yu Li,Bao-Lu Zhang,Kun Yu,Zheng-Xing Lian,Guo-Shi Liu,Yi-Xun Liu
Journal of Pineal Research. 2016; 60(4): 435
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247 Resveratrol improves reproductive parameters of adult rats varicocelized in peripuberty
Talita Biude Mendes,Camila Cicconi Paccola,Flávia Macedo de Oliveira Neves,Joana Noguères Simas,André da Costa Vaz,Regina Elisabeth L Cabral,Vanessa Vendramini,Sandra Maria Miraglia
Reproduction. 2016; 152(1): 23
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248 Impact of sperm DNA damage and oocyte-repairing capacity on trout development
C Fernández-Díez,S González-Rojo,M Lombó,M P Herráez
Reproduction. 2016; 152(1): 57
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249 The effects of radiofrequency electromagnetic radiation on sperm function
B J Houston,B Nixon,B V King,G N De Iuliis,R J Aitken
Reproduction. 2016; 152(6): R263
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250 Understanding the dynamics of physiological impacts of environmental stressors on Australian marsupials, focus on the koala (Phascolarctos cinereus)
Edward J. Narayan,Michelle Williams
BMC Zoology. 2016; 1(1)
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251 CABYR is essential for fibrous sheath integrity and progressive motility in mouse spermatozoa
Samantha A. M. Young,Haruhiko Miyata,Yuhkoh Satouh,Robert John Aitken,Mark A. Baker,Masahito Ikawa
Journal of Cell Science. 2016; 129(23): 4379
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252 Role of melatonin in mitigating chemotherapy-induced testicular dysfunction in Wistar rats
P. Madhu,K. Pratap Reddy,P. Sreenivasula Reddy
Drug and Chemical Toxicology. 2016; 39(2): 137
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253 Protective Effects of Pleurotus tuber-regium on Carbon- Tetrachloride Induced Testicular Injury in Sprague Dawley Rats
Kenneth O. Okolo,Iyeopu M. Siminialayi,Orish E. Orisakwe
Frontiers in Pharmacology. 2016; 7
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254 New insights in sperm biology: How benchside results in the search for molecular markers may help understand male infertility
Sara Marchiani,Lara Tamburrino,Monica Muratori,Elisabetta Baldi
World Journal of Translational Medicine. 2016; 5(1): 26
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255 Tobacco Use Increases Oxidative DNA Damage in Sperm - Possible Etiology of Childhood Cancer
Shiv Basant Kumar,Bhavna Chawla,Shilpa Bisht,Raj Kumar Yadav,Rima Dada
Asian Pacific Journal of Cancer Prevention. 2015; 16(16): 6967
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256 Cerium dioxide nanoparticles affectin vitrofertilization in mice
Lise Preaubert,Blandine Courbiere,Vincent Achard,Virginie Tassistro,Fanny Greco,Thierry Orsiere,Jean-Yves Bottero,Jérome Rose,Mélanie Auffan,Jeanne Perrin
Nanotoxicology. 2015; : 1
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257 Inhibition of Mitochondrial Complex I Leads to Decreased Motility and Membrane Integrity Related to Increased Hydrogen Peroxide and Reduced ATP Production, while the Inhibition of Glycolysis Has Less Impact on Sperm Motility
María Plaza Davila,Patricia Martin Muñoz,Jose A. Tapia,Cristina Ortega Ferrusola,Carolina Balao da Silva C,Fernando J. Peña,Joël R Drevet
PLOS ONE. 2015; 10(9): e0138777
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258 Effects of increased paternal age on sperm quality, reproductive outcome and associated epigenetic risks to offspring
Rakesh Sharma,Ashok Agarwal,Vikram K Rohra,Mourad Assidi,Muhammad Abu-Elmagd,Rola F Turki
Reproductive Biology and Endocrinology. 2015; 13(1)
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259 Advances in sperm proteomics: best-practise methodology and clinical potential
Montserrat Codina,Josep Maria Estanyol,María José Fidalgo,Josep Lluís Ballescà,Rafael Oliva
Expert Review of Proteomics. 2015; 12(3): 255
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260 Sertoli cells are the target of environmental toxicants in the testis – a mechanistic and therapeutic insight
Ying Gao,Dolores D Mruk,C Yan Cheng
Expert Opinion on Therapeutic Targets. 2015; 19(8): 1073
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261 Paternal obesity induces metabolic and sperm disturbances in male offspring that are exacerbated by their exposure to an “obesogenic” diet
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262 Investigation on the Origin of Sperm DNA Fragmentation: Role of Apoptosis, Immaturity and Oxidative Stress
Monica Muratori,Lara Tamburrino,Sara Marchiani,Marta Cambi,Biagio Olivito,Chiara Azzari,Gianni Forti,Elisabetta Baldi
Molecular Medicine. 2015; 21(1): 109
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263 An Ecology of Sperm: Sperm Diversification by Natural Selection
Klaus Reinhardt,Ralph Dobler,Jessica Abbott
Annual Review of Ecology, Evolution, and Systematics. 2015; 46(1): 435
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264 Coenzyme Q10,a-Tocopherol, and Oxidative Stress Could Be Important Metabolic Biomarkers of Male Infertility
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265 Involvement of seminal leukocytes, reactive oxygen species, and sperm mitochondrial membrane potential in the DNA damage of the human spermatozoa
A. M. Lobascio,M. De Felici,M. Anibaldi,P. Greco,M. G. Minasi,E. Greco
Andrology. 2015; : n/a
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266 Decreased activity of superoxide dismutase in the seminal plasma of infertile men correlates with increased sperm deoxyribonucleic acid fragmentation during the first hours after sperm donation
Artur Wdowiak,Szymon Bakalczuk,Grzegorz Bakalczuk
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267 Joint effect of glutathione S-transferase genotypes and cigarette smoking on idiopathic male infertility
S. L. Yarosh,E. V. Kokhtenko,M. I. Churnosov,M. A. Solodilova,A. V. Polonikov
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268 Oxidative stress and human spermatozoa: diagnostic and functional significance of aldehydes generated as a result of lipid peroxidation
R. Moazamian,A. Polhemus,H. Connaughton,B. Fraser,S. Whiting,P. Gharagozloo,R. J. Aitken
Molecular Human Reproduction. 2015; 21(6): 502
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269 Plasma membrane Ca2+-ATPase 4: interaction with constitutive nitric oxide synthases in human sperm and prostasomes which carry Ca2+/CaM-dependent serine kinase
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Molecular Human Reproduction. 2015; 21(11): 832
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270 Genotoxic effects of two-generational selenium deficiency in mouse somatic and testicular cells
A. Graupner,C. Instanes,J. M. Andersen,A. Brandt-Kjelsen,S. D. Dertinger,B. Salbu,G. Brunborg,A.-K. Olsen
Mutagenesis. 2015; 30(2): 217
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271 Defective Human Sperm Cells Are Associated with Mitochondrial Dysfunction and Oxidant Production1
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Biology of Reproduction. 2015; 93(5)
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272 Compartmentalization of membrane trafficking, glucose transport, glycolysis, actin, tubulin and the proteasome in the cytoplasmic droplet/Hermes body of epididymal sperm
Catherine E. Au,Louis Hermo,Elliot Byrne,Jeffrey Smirle,Ali Fazel,Robert E. Kearney,Charles E. Smith,Hojatollah Vali,Julia Fernandez-Rodriguez,Paul H. G. Simon,Craig Mandato,Tommy Nilsson,John J. M. Bergeron
Open Biology. 2015; 5(8): 150080
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273 Differences in the seminal plasma proteome are associated with oxidative stress levels in men with normal semen parameters
Paula Intasqui,Mariana Pereira Antoniassi,Mariana Camargo,Marcílio Nichi,Valdemir Melechco Carvalho,Karina Helena Morais Cardozo,Daniel Suslik Zylbersztejn,Ricardo Pimenta Bertolla
Fertility and Sterility. 2015; 104(2): 292
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274 Association between the seminal plasma proteome and sperm functional traits
Paula Intasqui,Mariana Camargo,Mariana Pereira Antoniassi,Agnaldo Pereira Cedenho,Valdemir Melechco Carvalho,Karina Helena Morais Cardozo,Daniel Suslik Zylbersztejn,Ricardo Pimenta Bertolla
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275 Functional deficit of sperm and fertility impairment in men with antisperm antibodies
V.A. Bozhedomov,M.A. Nikolaeva,I.V. Ushakova,N.A. Lipatova,G.E. Bozhedomova,G.T. Sukhikh
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276 Spermatogenesis, DNA damage and DNA repair mechanisms in male infertility
Sezgin Gunes,Maha Al-Sadaan,Ashok Agarwal
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277 Female transcriptomic response to male genetic and nongenetic ejaculate variation
O. Otti,P. R. Johnston,G. J. Horsburgh,J. Galindo,K. Reinhardt
Behavioral Ecology. 2015; 26(3): 681
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278 Reproductive toxicity of carbon nanomaterials: a review
I Vasyukova,A Gusev,A Tkachev
IOP Conference Series: Materials Science and Engineering. 2015; 98: 012001
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279 High total antioxidant capacity of the porcine seminal plasma (SP-TAC) relates to sperm survival and fertility
Isabel Barranco,Asta Tvarijonaviciute,Cristina Perez-Patiño,Inmaculada Parrilla,Jose J. Ceron,Emilio A. Martinez,Heriberto Rodriguez-Martinez,Jordi Roca
Scientific Reports. 2015; 5: 18538
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280 Effects of black seeds (Nigella sativa) on male infertility: A systematic review
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Journal of Herbal Medicine. 2015; 5(3): 133
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281 Effect of bajijiasu isolated from Morinda officinalis F. C. how on sexual function in male mice and its antioxidant protection of human sperm
Ze-Qing Wu,Di-Ling Chen,Fang-Hua Lin,Li Lin,Ou Shuai,Jin-Yu Wang,Long-Kai Qi,Peng Zhang
Journal of Ethnopharmacology. 2015; 164: 283
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282 Parental exposure to the herbicide diuron results in oxidative DNA damage to germinal cells of the Pacific oyster Crassostrea gigas
Audrey Barranger,Clothilde Heude-Berthelin,Julien Rouxel,Béatrice Adeline,Abdellah Benabdelmouna,Thierry Burgeot,Farida Akcha
Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology. 2015;
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283 Old male sex: large ejaculate, many sperm, but few offspring
Tobias Kehl,Michaël Beaulieu,Alexander Kehl,Klaus Fischer
Behavioral Ecology and Sociobiology. 2015; 69(9): 1543
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284 Reactive Oxygen Species (ROS) in human semen: determination of a reference range
Sheryl T. Homa,Wayne Vessey,Ana Perez-Miranda,Tripat Riyait,Ashok Agarwal
Journal of Assisted Reproduction and Genetics. 2015;
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285 A single-cell assay for telomere DNA content shows increasing telomere length heterogeneity, as well as increasing mean telomere length in human spermatozoa with advancing age
Danielle M. F. Antunes,Keri H. Kalmbach,Fang Wang,Roberta C. Dracxler,Michelle L. Seth-Smith,Yael Kramer,Julia Buldo-Licciardi,Fabiana B. Kohlrausch,David L. Keefe
Journal of Assisted Reproduction and Genetics. 2015; 32(11): 1685
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286 Biochemical composition and protein profile of alpaca (Vicugna pacos) oviductal fluid
S.A. Apichela,M.E. Argañaraz,R. Zampini,J. Vencato,D.C. Miceli,C. Stelletta
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287 Novel SNPs in heat shock protein 70 gene and their association with sperm quality traits of Boer goats and Boer crosses
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288 Protein modification as oxidative stress marker in follicular fluid from women with polycystic ovary syndrome: the effect of inositol and metformin
P. Piomboni,R. Focarelli,A. Capaldo,A. Stendardi,V. Cappelli,A. Cianci,A. La Marca,A. Luddi,V. De Leo
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289 Next day determination of ejaculatory sperm motility after overnight shipment of semen to remote locations
Leyla Sati,David Bennett,Michael Janes,Gabor Huszar
Journal of Assisted Reproduction and Genetics. 2014;
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290 Abnormalities in the male reproductive system after exposure to diesel and biodiesel blend
Elena R. Kisin,Naveena Yanamala,Mariana T. Farcas,Dmitriy W. Gutkin,Michael R. Shurin,Valerian E. Kagan,Aleksandar D. Bugarski,Anna A. Shvedova
Environmental and Molecular Mutagenesis. 2014; : n/a
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291 ROS, thiols and thiol-regulating systems in male gametogenesis
Marcus Conrad,Irina Ingold,Katalin Buday,Sho Kobayashi,Jose Pedro Friedmann Angeli
Biochimica et Biophysica Acta (BBA) - General Subjects. 2014;
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292 Reactive oxygen species in human semen: validation and qualification of a chemiluminescence assay
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293 Identification of Drosophila-based Endpoints for the Assessment and Understanding of Xenobiotic-Mediated Male Reproductive Adversities
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294 Impact of adrenalectomy and dexamethasone treatment on testicular morphology and sperm parameters in rats: insights into the adrenal control of male reproduction
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Andrology. 2014; : n/a
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295 Prepubertal Exposure to Genistein Alleviates Di-(2-ethylhexyl) Phthalate Induced Testicular Oxidative Stress in Adult Rats
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296 Parenting from before conception
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297 Chlorophytum borivilianum (Safed Musli) root extract prevents impairment in characteristics and elevation of oxidative stress in sperm of streptozotocin-induced adult male diabetic Wistar rats
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BMC Complementary and Alternative Medicine. 2014; 14(1)
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298 Recent knowledge concerning mammalian sperm chromatin organization and its potential weaknesses when facing oxidative challenge
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Basic and Clinical Andrology. 2014; 24(1): 6
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299 Roles of Reactive Oxygen Species in the Spermatogenesis Regulation
Giulia Guerriero,Samantha Trocchia,Fagr K. Abdel-Gawad,Gaetano Ciarcia
Frontiers in Endocrinology. 2014; 5
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