Hostname: page-component-8448b6f56d-jr42d Total loading time: 0 Render date: 2024-04-24T01:45:08.306Z Has data issue: false hasContentIssue false

Oxidative stress and fertility: incorrect assumptions and ineffective solutions?

Published online by Cambridge University Press:  12 July 2012

Yves Ménézo*
Affiliation:
UNILABS, Laboratoire Dynabio, Polyclinique du Cotentin, 50120 Equeurdreville, France. UNILABS, Laboratoire d'Eylau, 55 Rue St Didier, Paris, France. PROCRELYS, 28 Avenue Rockefeller, 69008 Lyon, France. YM, MC are members of the Oxidative Stress College, Paris, France.
Frida Entezami
Affiliation:
UNILABS, Laboratoire Dynabio, Polyclinique du Cotentin, 50120 Equeurdreville, France.
Isabelle Lichtblau
Affiliation:
UNILABS, Laboratoire d'Eylau, 55 Rue St Didier, Paris, France.
Stephanie Belloc
Affiliation:
UNILABS, Laboratoire d'Eylau, 55 Rue St Didier, Paris, France.
Marc Cohen
Affiliation:
PROCRELYS, 28 Avenue Rockefeller, 69008 Lyon, France. YM, MC are members of the Oxidative Stress College, Paris, France.
Brian Dale
Affiliation:
Centre for Assisted Fertilization, Naples, 80123, Italy.
*
All correspondence to: Yves Ménézo. UNILABS, Laboratoire Dynabio, Polyclinique du Cotentin, 50120 Equeurdreville, France. e-mail: yves.menezo@club-internet.fr

Summary

One of the most important concerns in assisted reproduction (ART), and in particular ICSI, is the quality of sperm DNA. Oxidative stress is one of the major causes of damage to DNA and attempting to reduce generation of DNA damage related to reactive oxygen species (ROS) through consumption of antioxidants is often tempting. However, current antioxidant treatments, given irrespectively of clinically quantified deficiencies, are poorly efficient, potentially detrimental and over-exposure is risky. Here we discuss new treatments in relation to present day concepts on oxidative stress. This discussion includes stimulation of endogenous anti-ROS defense i.e. glutathione synthesis and recycling of homocysteine, the epicentre of multiple ROS-linked pathologies.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2012 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Aitken, R.J., Baker, M.A. & Sawyer, D. (2003). Oxidative stress in the male germ line and its role in the aetiology of male infertility and genetic disease. Reprod. Biomed. Online 7, 65–7.CrossRefGoogle ScholarPubMed
Aitken, R.J., Wingate, J.K., De Iuliis, G.N., Koppers, A.J. & McLaughlin, E.A. (2006). Cis-unsaturated fatty acids stimulate reactive oxygen species generation and lipid peroxidation in human spermatozoa. J. Clin. Endocrinol. Metab. 91, 4154–63.CrossRefGoogle ScholarPubMed
Almbro, M., Dowling, D.K. & Simmons, L.W. (2011). Effects of vitamin E and beta-carotene on sperm competitiveness. Ecol. Lett. 14, 891–5.CrossRefGoogle ScholarPubMed
Badouard, C., Ménézo, Y., Panteix, G.et al. (2008). Determination of new types of DNA lesions in human sperm. Zygote 16, 913.CrossRefGoogle ScholarPubMed
Belloc, S., Benkhalifa, M., Junca, A.M., Dumont, M., Bacrie, P.C. & Ménézo, Y. (2009). Paternal age and sperm DNA decay: discrepancy between chromomycin and aniline blue staining. Reprod. Biomed. Online 19, 264–9.CrossRefGoogle ScholarPubMed
Benkhalifa, M., Cohen, M., Tosti, E., Cohen-Bacrie, P., Ballashova, E. & Ménézo, Y. (2008). New Concept for Antioxidant Treatments for Sperm DNA Structure Alteration. International Congress of Andrology, ICA, Barcelona Spain.Google Scholar
Benkhalifa, M., Montjean, D., Cohen-Bacrie, P. & Ménézo, Y. (2010). Imprinting: RNA expression for homocysteine recycling in the human oocyte. Fertil. Steril. 93, 1585–90.CrossRefGoogle ScholarPubMed
Berker, B., Kaya, C., Aytac, R. & Satiroglu, H. (2009). Homocysteine concentrations in follicular fluid are associated with poor oocyte and embryo qualities in polycystic ovary syndrome patients undergoing assisted reproduction. Hum. Reprod. 24, 2293–302.CrossRefGoogle ScholarPubMed
Bjelakovic, G., Nikolova, D., Gluud, L.L., Simonetti, R.G. & Gluud, C. (2008). Antioxidant supplements for prevention of mortality in healthy participants and patients with various diseases. Cochrane Database Syst. Rev. 16, CD007176.Google Scholar
Bleau, G., Lemarbre, J., Faucher, G., Roberts, K.D. & Chapdelaine, A. (1984). Semen selenium and human fertility. Fertil. Steril. 42, 890–4.CrossRefGoogle ScholarPubMed
Bøhn, S.K., Myhrstad, M.C., Thoresen, M., Holden, M., Karlsen, A., Tunheim, S.H., Erlund, I., Svendsen, M., Seljeflot, I., Moskaug, J.O., Duttaroy, A.K., Laake, P., Arnesen, H., Tonstad, S., Collins, A., Drevon, C.A. & Blomhoff, R. (2010). Blood cell gene expression associated with cellular stress defense is modulated by antioxidant-rich food in a randomised controlled clinical trial of male smokers. BMC Med. 8, 5469.CrossRefGoogle Scholar
Boxmeer, J.C., Smit, M., Weber, R.F., Lindemans, J., Romijn, J.C., Eijkemans, M.J., Macklon, N.S. & Steegers-Theunissen, R.P. (2007). Seminal plasma cobalamin significantly correlates with sperm concentration in men undergoing IVF or ICSI procedures. J. Androl. 28, 521–7.CrossRefGoogle ScholarPubMed
Boxmeer, J.C., Smit, M., Utomo, E., Romijn, J.C., Eijkemans, M.J., Lindemans, J., Laven, J.S., Macklon, N.S., Steegers, E.A. & Steegers-Theunissen, R.P. (2009). Low folate in seminal plasma is associated with increased sperm DNA damage. Fertil. Steril. 92, 548–56.CrossRefGoogle ScholarPubMed
Brack, M., Brack, O., Bonnefont-Rousselot, D., Dreyfus, G., Chapman, J. & Kontush, A. (2012). Distinct profiles of systemic biomarkers of oxidative stress in chronic human pathologies: cardiovascular, psychiatric, neurovegetative, rheumatic, infectious, neoplastic and endocrinological diseases. In press.Google Scholar
Bungum, M., Bungum, L. & Giwercman, A. (2011). Sperm chromatin structure assay (SCSA): a tool in diagnosis and treatment of infertility. Asian J. Androl. 13, 6975.CrossRefGoogle ScholarPubMed
Centers for Disease Control and Prevention (CDC), National Center for Health Statistics (NCHS), National Health and Nutrition Examination Survey Questionnaire. Hyattsville, MD. (2001–2002). Available from: http://www.cdc.gov/nchs/about/major/nhanes/nhanes01–02.htm (cited 1 May 2007).Google Scholar
Combs, G.F. Jr, Watts, J.C., Jackson, M.I., Johnson, L.K., Zeng, H., Scheett, A.J., Uthus, E.O., Schomburg, L., Hoeg, A., Hoefig, C.S., Davis, C.D. & Milner, J.A. (2011). Determinants of selenium status in healthy adults. Nutr. J. 10, 75.CrossRefGoogle ScholarPubMed
Cooney, C.A., Dave, A.A. & Wolff, G.L. (2002). Maternal methyl supplements in mice affect epigenetic variation and DNA methylation of offspring. J. Nutr. 132, 2393S2400S.CrossRefGoogle ScholarPubMed
Davis, C.D. & Uthus, E.O. (2003). Dietary folate and selenium affect dimethylhydrazine-induced aberrant crypt formation, global DNA methylation and one-carbon metabolism in rats. J. Nutr. 133, 2907–14.CrossRefGoogle ScholarPubMed
Davis, C.D., Uthus, E.O. & Finley, J.W. (2000). Dietary selenium and arsenic affect DNA methylation in vitro in Caco-2 cells and in vivo in rat liver and colon. J. Nutr. 130, 2903–9.CrossRefGoogle ScholarPubMed
de la Villehuchet, A.M., Brack, M., Dreyfus, G., Oussar, Y., Bonnefont-Rousselot, D. & Chapman, M.J. & Kontush, A. (2009). A machine-learning approach to the prediction of oxidative stress in chronic inflammatory disease. Redox Rep. 14, 2333.CrossRefGoogle Scholar
Derijck, A., van der Heijden, G., Giele, M., Philippens, M. & de Boer, P. (2008). DNA double-strand break repair in parental chromatin of mouse zygotes, the first cell cycle as an origin of de novo mutation. Hum. Mol. Genet. 17, 1922–37.CrossRefGoogle ScholarPubMed
Donnelly, E.T., McClure, N. & Lewis, S.E. (1999). The effect of ascorbate and alpha-tocopherol supplementation in vitro on DNA integrity and hydrogen peroxide-induced DNA damage in human spermatozoa. Mutagenesis 14, 505–12.CrossRefGoogle ScholarPubMed
Ebisch, I.M., Peters, W.H., Thomas, C.M., Wetzels, A.M., Peer, P.G. & Steegers-Theunissen, R.P. (2006). Homocysteine, glutathione and related thiols affect fertility parameters in the (sub) fertile couple. Hum. Reprod. 21, 1725–33.CrossRefGoogle ScholarPubMed
Ebisch, I.M., Thomas, C.M., Peters, W.H., Braat, D.D. & Steegers-Theunissen, R.P. (2007). The importance of folate, zinc and antioxidants in the pathogenesis and prevention of subfertility. Hum. Reprod. Update 13, 163–74.CrossRefGoogle ScholarPubMed
Evenson, D.P., Darzynkiewicz, Z. & Melamed, M.R. (1980). Relation of mammalian sperm chromatin heterogeneity to fertility. Science 210, 1131–3.CrossRefGoogle ScholarPubMed
Evenson, D.P., Larson, K.L. & Jost, L.K. (2002). Sperm chromatin structure assay: its clinical use for detecting sperm DNA fragmentation in male infertility and comparisons with other techniques. J. Androl. 23, 2543.CrossRefGoogle ScholarPubMed
Fernández-Gonzalez, R., Moreira, P.N., Pérez-Crespo, M., Sánchez-Martín, M., Ramirez, M.A., Pericuesta, E., Bilbao, A., Bermejo-Alvarez, P., de Dios Hourcade, J., de Fonseca, F.R. & Gutiérrez-Adán, A. (2008). Long-term effects of mouse intracytoplasmic sperm injection with DNA-fragmented sperm on health and behavior of adult offspring. Biol. Reprod. 78, 761–72.CrossRefGoogle ScholarPubMed
Fraga, C.G., Motchnik, P.A., Shigenaga, M.K., Helbock, H.J., Jacob, R.A., & Ames, B.N. (1991). Ascorbic acid protects against endogenous oxidative DNA damage in human sperm. Proc. Natl. Acad. Sci. USA 88, 11003–6.CrossRefGoogle ScholarPubMed
Frydman, N., Prisant, N., Hesters, L., Frydman, R., Tachdjian, G., Cohen-Bacrie, P. & Fanchin, R. (2008). Adequate ovarian follicular status does not prevent the decrease in pregnancy rates associated with high sperm DNA fragmentation. Fertil. Steril. 89, 92–7.CrossRefGoogle Scholar
Garcıa-Herrero, S., Garrido, N., Martınez-Conejero, J.A., Remohı, J., Pellicer, A. & Meseguer, M. (2011). Differential transcriptomic profile in spermatozoa achieving pregnancy or not via ICSI. Reprod. Biomed. Online 22, 2536.CrossRefGoogle ScholarPubMed
Gharagozloo, P. & Aitken, R.J. (2011). The role of sperm oxidative stress in male infertility and the significance of oral antioxidant therapy. Hum. Reprod. 26, 1628–40.CrossRefGoogle ScholarPubMed
Giustarini, D., Dalle-Donne, I., Colombo, R., Milzani, A. & Rossi, R. (2008). Is ascorbate able to reduce disulfide bridges? A cautionary note. Nitric Oxide 19, 252–8.CrossRefGoogle Scholar
Hammadeh, M.E., Zeginiadov, T., Rosenbaum, P., Georg, T., Schmidt, W. & Strehler, E. (2001). Predictive value of sperm chromatin condensation (aniline blue staining) in the assessment of male fertility. Arch. Androl. 46, 99104.CrossRefGoogle ScholarPubMed
Hammerstedt, R.H., Volonté, C. & Racker, E. (1988). Motility, heat, and lactate production in ejaculated bovine sperm. Arch. Biochem. Biophys. 266, 111–23.CrossRefGoogle ScholarPubMed
Hartwig, A., Blessing, H., Schwerdtle, T. & Walter, I. (2003). Modulation of DNA repair processes by arsenic and selenium compounds. Toxicology 193, 161–9.CrossRefGoogle ScholarPubMed
Hawkes, W.C. & Turek, P.J. (2001). Effects of dietary selenium on sperm motility in healthy men. J. Androl. 22, 764–72.CrossRefGoogle ScholarPubMed
Hawkes, W.C., Alkan, Z. & Wong, K. (2009). Selenium supplementation does not affect testicular selenium status or semen quality in North American men. J. Androl. 30, 525–33.CrossRefGoogle ScholarPubMed
Ho, E. (2004). Zinc deficiency, DNA damage and cancer risk. J. Nutr. Biochem. 15, 572–8.CrossRefGoogle ScholarPubMed
Hoffman, M. (2011). Hypothesis: hyperhomocysteinemia is an indicator of oxidant stress. Med. Hypotheses 77, 1088–93.CrossRefGoogle ScholarPubMed
Izawa, H., Kohara, M., Aizawa, K., Suganuma, H., Inakuma, T., Watanabe, G., Taya, K. & Sagai, M. (2008). Alleviative effects of quercetin and onion on male reproductive toxicity induced by diesel exhaust particles. Biosci. Biotechnol. Biochem. 72, 1235–41.CrossRefGoogle ScholarPubMed
Jaroudi, S., Kakourou, G., Cawood, S., Doshi, A., Ranieri, D.M., Serhal, P., Harper, J.C. & Sengupta, S.B. (2009). Expression profiling of DNA repair genes in human oocytes and blastocysts using microarrays. Hum. Reprod. 24, 2649–55.CrossRefGoogle ScholarPubMed
Jenkins, T.G. & Carrell, D.T. (2012). The sperm epigenome and potential implications for the developing embryo. Reproduction 143, 727–34.CrossRefGoogle ScholarPubMed
Junca, A., Gonzalez Marti, B., Tosti, E., Cohen, M., De la Fontaine, D., Benkhalifa, M. & Ménézo, Y. (2012). Sperm nucleus decondensation, hyaluronic acid (HA) binding and oocyte activation capacity: different markers of sperm immaturity? Case reports. J. Assist. Reprod. Genet. 29, 353–5.CrossRefGoogle ScholarPubMed
Kand’ár, R., Drábková, P. & Hampl, R. (2011). The determination of ascorbic acid and uric acid in human seminal plasma using an HPLC with UV detection. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 879, 2834–9.CrossRefGoogle Scholar
Kao, S.H., Chao, H.T., Chen, H.W., Hwang, T.I., Liao, T.L. & Wei, Y.H. (2008). Increase of oxidative stress in human sperm with lower motility Fertil. Steril. 89, 1183–90.CrossRefGoogle Scholar
Katari, S., Turan, N., Bibikova, M., Erinle, O., Chalian, R., Foster, M., Gaughan, J.P., Coutifaris, C. & Sapienza, C. (2009). DNA methylation and gene expression differences in children conceived in vitro or in vivo. Hum. Mol. Genet. 18, 3769–78.CrossRefGoogle ScholarPubMed
King, J.C., Shames, D.M. & Woodhouse, L.R (2000). Zinc homeostasis in humans. J. Nutr. 130, 1360S–6S.CrossRefGoogle ScholarPubMed
Klein, E.A., Thompson, I.M. Jr, Tangen, C.M., Crowley, J.J., Lucia, M.S., Goodman, P.J., Minasian, L.M., Ford, L.G., Parnes, H.L., Gaziano, J.M., Karp, D.D., Lieber, M.M., Walther, P.J., Klotz, L., Parsons, J.K., Chin, J.L., Darke, A.K., Lippman, S.M., Goodman, G.E., Meyskens, F.L. Jr & Baker, L.H. (2011). Vitamin E and the risk of prostate cancer: the Selenium and Vitamin E Cancer Prevention Trial (SELECT). JAMA 306, 1549–56.CrossRefGoogle Scholar
Koppers, A.J., De Iuliis, G.N., Finnie, J.M., McLaughlin, E.A. & Aitken, R.J. (2008). Significance of mitochondrial reactive oxygen species in the generation of oxidative stress in spermatozoa. J. Clin. Endocrinol. Metab. 93, 3199–207.CrossRefGoogle ScholarPubMed
Li, P., Zhong, Y., Jiang, X., Wang, C., Zuo, Z. & Sha, A. (2012). Seminal plasma metals concentration with respect to semen quality. Biol. Trace Elem. Res. [Epub ahead of print].CrossRefGoogle Scholar
Liu, Z.X. & Artmann, C. (2009). Relative bioavailability comparison of different co-enzyme Q10 formulations with a novel delivery system. Altern. Ther. Health Med. 15, 42–6.Google ScholarPubMed
Lopes, S., Jurisicova, A. & Casper, R.F. (1998). Gamete-specific DNA fragmentation in unfertilized human oocytes after intracytoplasmic sperm injection. Hum. Reprod. 13, 703–8.CrossRefGoogle ScholarPubMed
Mancini, A. & Balercia, G. (2011). Co-enzyme Q(10) in male infertility: physiopathology and therapy. Biofactors 37, 374–8.CrossRefGoogle Scholar
Marchetti, F., Essers, J., Kanaar, R. & Wyrobek, A.J. (2007). Disruption of maternal DNA repair increases sperm-derived chromosomal aberrations. Proc. Natl. Acad. Sci. USA. 104, 17725–9.CrossRefGoogle ScholarPubMed
Ménézo, Y., Khatchadourian, C., Gharib, A., Hamidi, J., Greenland, T. & Sarda, N. (1989). Regulation of S-adenosyl methionine synthesis in the mouse embryo. Life Sci. 44, 1601–9.CrossRefGoogle ScholarPubMed
Ménézo, Y Jr, Russo, G., Tosti, E., El Mouatassim, S. & Benkhalifa, M. (2007a). Expression profile of genes coding for DNA repair in human oocytes using pangenomic microarrays, with a special focus on ROS linked decays. J. Assist. Reprod. Genet. 24, 513–20.CrossRefGoogle ScholarPubMed
Ménézo, Y., Hazout, A., Panteix, G., Robert, F., Rollet, J., Cohen-Bacrie, P., Chapuis, F., Clément, P. & Benkhalifa, M. (2007b). Antioxidants to reduce sperm DNA fragmentation: an unexpected adverse effect. Reprod. Biomed. Online 14, 418–21.CrossRefGoogle ScholarPubMed
Ménézo, Y., Dale, B. & Cohen, M. (2010a). DNA damage and repair in human oocytes and embryos: a review. Zygote 18, 357–65.CrossRefGoogle ScholarPubMed
Ménézo, Y., Elder, K., Benkhalifa, M. & Dale, B. (2010b). DNA methylation and gene expression in IVF. Reprod. Biomed. Online 20, 709–10.CrossRefGoogle ScholarPubMed
Ménézo, Y., Ménézo, Y., Pluntz, L., Chouteau, J., Gurgan, T., Demirol, A., Dalleac, A. & Benkhalifa, M. (2011a). Zinc concentrations in serum and follicular fluid during ovarian stimulation and expression of Zn2+ transporters in human oocytes and cumulus cells. Reprod. Biomed. Online 22, 647–52.CrossRefGoogle ScholarPubMed
Ménézo, Y., Mares, P., Cohen, M., Brack, M., Viville, S. & Elder, K. (2011b). Autism, imprinting and epigenetic disorders: a metabolic syndrome linked to anomalies in homocysteine recycling starting in early life? J. Assist. Reprod. Genet. 28, 1143–5.CrossRefGoogle ScholarPubMed
Montjean, D., Ménézo, Y., Benkhalifa, M., Cohen, M., Belloc, S., Cohen-Bacrie, P. & de Mouzon, J. (2010). Malonaldehyde formation and DNA fragmentation: two independent sperm decays linked to reactive oxygen species. Zygote 18, 265–8.CrossRefGoogle ScholarPubMed
Moskaug, J.Ø., Carlsen, H., Myhrstad, M.C. & Blomhoff, R. (2005). Polyphenols and glutathione synthesis regulation Am. J. Clin. Nutr. 81, 277S283S.CrossRefGoogle ScholarPubMed
Nadjarzadeh, A., Sadeghi, M.R., Amirjannati, N., Vafa, M.R., Motevalian, S.A., Gohari, M.R., Akhondi, M.A., Yavari, P. & Shidfar, F. (2011). Co-enzyme Q10 improves seminal oxidative defense but does not affect on semen parameters in idiopathic oligoasthenoteratozoospermia: a randomized double-blind, placebo controlled trial. J. Endocrinol. Invest. Epub ahead of print.Google Scholar
Rousseaux, S., Reynoird, N., Escoffier, E., Thevenon, J., Caron, C. & Khochbin, S. (2008). Epigenetic reprogramming of the male genome during gametogenesis and in the zygote. Reprod. Biomed. Online 16, 492503.CrossRefGoogle ScholarPubMed
Sreekanth, D., Arunasree, M.K., Roy, K.R., Chandramohan Reddy, T., Reddy, G.V. & Reddanna, P. (2007). Betanin a betacyanin pigment purified from fruits of Opuntia ficus-indica induces apoptosis in human chronic myeloid leukemia cell line-K562. Phytomedicine 14, 739–46.CrossRefGoogle ScholarPubMed
Tunc, O. & Tremellen, K. (2009). Oxidative DNA damage impairs global sperm DNA methylation in infertile men. J. Assist. Reprod. Genet. 26, 537–44.CrossRefGoogle ScholarPubMed
Ursini, F., Maiorino, M. & Roveri, A. (1997). Phospholipid hydroperoxide glutathione peroxidase (PHGPx): more than an antioxidant enzyme? Biomed. Environ. Sci. 10, 327–32.Google ScholarPubMed
Villalba, J.M., Parrado, C., Santos-Gonzalez, M. & Alcain, F.J. (2010). Therapeutic use of coenzyme Q10 and coenzyme Q10-related compounds and formulations. Expert Opin. Investig. Drugs 19, 535–54.CrossRefGoogle Scholar
Xiang, N., Zhao, R. & Zhong, W. (2009). Sodium selenite induces apoptosis by generation of superoxide via the mitochondrial-dependent pathway in human prostate cancer cells. Cancer Chemother. Pharmacol. 63, 351–62.CrossRefGoogle ScholarPubMed
Young, S.S., Eskenazi, B., Marchetti, F.M., Block, G. & Wyrobek, A.J. (2008). The association of folate, zinc and antioxidant intake with sperm aneuploidy in healthy non-smoking men. Hum. Reprod. 23, 1014–22.CrossRefGoogle ScholarPubMed
Zenzes, M.T. (2000). Smoking and reproduction: gene damage to human gametes and embryos. Hum. Reprod. Update 6, 122–3.CrossRefGoogle ScholarPubMed
Zenzes, M.T., Puy, L.A. & Bielecki, R. (1998). Immunodetection of benzo[a]pyrene adducts in ovarian cells of women 4, 159–65.CrossRefGoogle Scholar