Thus, not only do the spermatozoa produced by such patients exhibit high levels of ROS in association with cytoplasmic retention but also surgical correction of this condition both prevents cytoplasmic retention and suppresses ROS generation. The induction of hyperthyroidism in rats is associated with oxidative stress in the testes as reflected by increased lipid peroxidation, elevated GSH levels and induction of antioxidant enzymes.
The oxidative stress appears to be associated with a thyroxine dependent increase in mitochondrial activity and concomitant leakage of electrons from the mitochondrial electron transport chain. Experimental induction of diabetes in animal models has been shown to impair testicular function and decrease male fertility.
Thus, diabetogens such as streptozotocin, enhance ROS generation and induce both lipid peroxidation and protein carbonyl expression in the testes. Moreover the oxidative stress associated with the diabetic condition is associated with DNA damage in the male germ line and high rates of embryonic loss in mated females dominant lethal effect.
These effects could be attenuated by the administration of antioxidants such as ascorbic acid, melatonin, taurine or an herbal mixture containing extracts from Musa paradisiaca, Tamarindus indica, Eugenia jambolana and Coccinia indica.
Another factor that may cause oxidative stress in the testes is infection. Experimental models of infection, involving the intraperitoneal injection of bacterial lipopolysaccharide LPS , induced lipid peroxidation in the testes and rapidly depleted this tissue of antioxidant enzyme activity in the form of SOD, catalase and the glutathione peroxidase-reductase couple.
Moreover, these effects were associated with the disruption of Leydig cell mitochondrial function and, specifically, the inhibition of StAR-mediated cholesterol transfer activity. Physical exercise has been shown to up-regulate antioxidant activities in the testes of aging rats and may represent a practical way in which the detrimental effects of age on testicular function can be ameliorated. The immediate endocrine environment of the testes has a major impact on the antioxidant status of this organ.
Treatments including exposure to cyclophosphamide or dimethane sulfonate that diminish the intratesticular concentration of testosterone, inhibit the testicular expression of antioxidant enzymes such as GPx, SOD and catalase.
Testicular SOD activities that are largely confined to the seminiferous tubules did not change dramatically under these circumstances.
These free radicals then attack the germ cells within the seminiferous tubules leading to extensive apoptosis and the disruption of spermatogenesis. The fact that aminoglutethimide, an inhibitor of the P cholesterol side-chain cleavage, induces extensive lipid peroxidation in the testis supports this contention. While fluctuations in Leydig cell steroidogenesis may be one source of free radical generation in the testes, another is the Sertoli cell population. The latter has been shown to generate ROS following stimulation with all trans-retinoic acid RA , a vital cofactor for spermatogenesis.
Exposure of rat Sertoli cells to RA led to activation of ROS generation, lipid peroxidation and, ultimately, a loss of cell viability. A wide variety of different xenobiotics have also been shown to induce oxidative stress in the testes in concert with the suppression of antioxidant mechanisms.
A summary of these testicular toxicants is provided in Table 1. In addition to smoking, excessive alcohol consumption also has a negative effect of testicular function through the induction of oxidative stress and the concomitant disruption of testicular antioxidant status. Table 1 also highlights a number of metals that are known to induce oxidative stress in the testes and compromise male infertility.
Chromium, for example, is a testicular toxicant that stimulates lipid peroxidation and suppresses antioxidant enzyme activities as well as ascorbate levels in the testes.
In this situation, the oxidative stress induced in the testes by acute iron overload must have so damaged the DNA in the spermatozoa that the resulting embryos were non-viable. Heavy metals such as lead, cadmium and uranium have a similar effect on the testes disrupting spermatogenesis via mechanisms that involved the induction of lipid peroxidation, depletion of ROS scavengers and disruption of testicular antioxidant enzyme activity.
The importance of oxidative stress in the testicular toxicity associated with arsenic was emphasised by the ability of ascorbate to reverse these changes. In addition to the above, Table 1 lists a wide variety of different industrial and environmental toxicants that are all capable of compromising male fertility by inducing a state of oxidative stress in the testes. These compounds include phthalate esters, , sulfur dioxide, sodium fluoride, a range of environmental estrogens e.
Given the variety and prevalence of chemical and physical factors that can generate oxidative stress in the male gonad, there is an urgent need to identify antioxidants that can supplement the tissue's own antioxidant strategies to rescue the testes from the consequences of ROS attack.
In order to determine the relative potential of different antioxidants to address oxidative stress in the testes, the testicular torsion-detorsion model has been repeatedly used.
Typically this model involves the application of antioxidant therapy prior to the creation of a brief period of oxidative stress and subsequent comparison of various testicular attributes lipid peroxidation, histopathology, DNA damage or antioxidant enzyme status with sham operated controls Table 2. Such analyses have recorded significant protection against oxidative stress for factors as garlic extract, 57 caffeic acid phenethyl ester CAPE , 60 N-acetyl cysteine, pentoxifylline, erdostein, resveratrol, 58 dexpathenol, L-carnitine 59 and propofol anaesthetic.
A variety of antioxidants have also been assessed for their ability to counteract oxidative stress in the testes created by alternative mechanisms. One of the most effective antioxidants for the protection of testicular function is melatonin. This evolutionarily conserved compound has been shown to reduce oxidative stress in the testes induced by ethanol, indomethacin, X-irradiation, streptozotocin-induced diabetes, 86 and cisplatin.
The administration of antioxidants such as resveratrol, ascorbate or cocoa rich in flavanols to normal animals, not suffering from induced oxidative stress, also appears to improve testicular function, suggesting that oxidative stress is a consistent feature of testicular physiology.
Very few properly controlled double blind crossover trials have been conducted in this context. However where these conditions have been met, the results have been extremely promising.
Oxidative stress is a major factor in the aetiology of male infertility. At the level of the isolated spermatozoon, ROS attack can induce lipid peroxidation and DNA fragmentation disrupting both the motility of these cells and their ability to support normal embryonic development. However these two lines of evidence have not yet come together. Although oxidative stress is clearly a dominant feature in the aetiology of male infertility, the underlying causative mechanisms remain unresolved.
The plethora of physical, chemical, and pathological factors that can apparently contribute to the induction of oxidative stress in the testes is impressive and suggests that the clinical picture will be extremely complex, with each individual being subject to a unique range of causative factors as a result of differences in occupational and environmental exposures, the presence of other pathological factors such as infection or diabetes, and genetic factors that could influence everything from the way in which specific xenobiotics are metabolised to the endocrine environment in which the testes have to function.
That there are so many factors capable of inducing oxidative stress in the testes strongly suggests that this is a vulnerable tissue that is both highly dependent on oxygen to drive spermatogenesis and yet highly susceptible to the toxic effects of reactive oxygen metabolites; in this context, the testis is very like the brain.
While the testes clearly do possess highly specialized antioxidant defence enzymes such as extracellular SOD, PHGPx etc, there are clear benefits to be gained by treating susceptible individuals with exogenous antioxidants. Despite the evident clinical market for an antioxidant preparation specifically designed to support male reproductive health, it is remarkable how little effort has gone into the development of such a preparation and how poor most of the clinical trials in this area have been.
In animal models an impressive range of antioxidant preparations has been examined and compounds identified that are clearly capable of crossing the blood testes barrier and protecting the germinal epithelium and Leydig cells from oxidative stress. The future imperatives for this area are to go beyond the superficial phenomenology that characterizes most of the clinical research in this area in an attempt to i gain insights into the underlying causes of oxidative stress in the male reproductive tract and ii develop optimized antioxidant preparations to treat pathologies arising from an imbalance in the redox status of these tissues.
The journey will be long and difficult but ultimately more rewarding than the empirical approach that characterizes the current approach to treating the infertile male. Reprinted from: Molecular Mechanisms in Spermatogenesis , edited by C. National Center for Biotechnology Information , U. Oxid Med Cell Longev. Author information Article notes Copyright and License information Disclaimer. Corresponding author. Correspondence to: R. Key words: spermatogenesis, oxidative stress, antioxidant enzymes, reactive oxygen species, testes.
This article has been cited by other articles in PMC. Introduction Spermatogenesis is an extremely active replicative process capable of generating approximately 1, sperm a second. Antioxidant Enzymes Despite the low oxygen tensions that characterize the testicular micro-environment, this tissue remains vulnerable to oxidative stress due to the abundance of highly unsaturated fatty acids particularly and and the presence of potential reactive oxygen species ROS -generating systems.
Open in a separate window. Figure 1. Small Molecular Mass Antioxidants In addition to the major ROS processing enzymes, the testes rely heavily on small molecular weight antioxidant factors for protection against oxidative damage.
Vitamins C and E. Melatonin and cytochrome C. Disruption of the Antioxidant Status of the Testes Notwithstanding the antioxidant protection afforded to the testes in order to support its dual functions of steroidogenesis and sperm production, a wide variety of endogenous and exogenous factors are known to perturb these defences and generate a state of oxidative stress.
Testicular torsion. Physical exertion. Reproductive hormone imbalance. Impact of xenobiotics. Compound Ref. Antioxidant Therapy In order to determine the relative potential of different antioxidants to address oxidative stress in the testes, the testicular torsion-detorsion model has been repeatedly used. Antioxidant Outcome Ref. Conclusions Oxidative stress is a major factor in the aetiology of male infertility. References 1. Respiratory gas tensions in tissues and fluids of the male rat reproductive tract.
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