Potential Risk of Senescence on Male fertility and Sperm DNA damage on Progeny
Main Article Content
Abstract
There is a growing concern of the potential risk of producing genetically defective sperm and transmitting germ-line mutations to progeny by fathers who prefer their children at old age. Men with male factor infertility do not readily make themselves available for evaluation until very late when they seek assisted reproduction technique. The objective of this review is to highlight the impact of senescence on oxidative DNA damage on spermatozoa and possible effects on the progeny. Relevant literatures on oxidative sperm damage were reviewed in addition to the experience and publications we have made over the years on male factor infertility. Older men produce more spermatozoa with oxidative DNA damage probably due to enhance generation of reactive oxygen species, aberrant DNA repair mechanism leading to production of spermatozoa with abnormal genetic materials that could have adverse consequences on the progeny. It is suggested that men should have their children early and those with male factor infertility should seek medical attention early before old age. Adequate precaution should be taken when selecting spermatozoa for use during assisted reproduction technique.
Downloads
Article Details
This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.
How to Cite
References
Schmid TE, Eskenazi B, Baumgartner A, Marchetti F, Young S, Welblon R, Anderson D, Wyrobek AJ. The effects of male age on sperm DNA damage in healthy non-smokers. Human Reprod 2007; 22(1):180-187.
Kidd SA, Eskenazi B and Wyrobek AJ. Effects of male age on semen quality and fertility: a review of the literature. Fertil Steril 2001; 75(2):237–248.
Sloter E, Nath J, Eskenazi B and Wyrobek A. Effects of male age on the frequencies of germinal and heritable chromosomal abnormalities in humans and rodents. Fertil Steril 2004; 81(4):925–943.
Maher ER, Brueton LA, Bowdin SC, Luharia A, Cooper W, Cole TR, Macdonald F, Sampson JT. Beckwith–Wiedemann syndrome and assisted reproduction technology (ART). J Med Genet 2003; 40(1): 62–64.
Baccetti B, Afzelius BA. The biology of sperm cell. Monographs Development Biol 1976; 10:1-14.
Lian ZH, Zack MM and Erickson JD. Paternal age and the occurrence of birth defects. Am J Hum Genet 1989; 39(5):648–660.
Crow JF. The origins, patterns and implications of human spontaneous mutation. Nat Rev Genet 2000;1(1):40–47.
Risch N, Reich EW, Wishnick MM and McCarthy JG. Spontaneous mutation and parental age in humans. Am J Hum Genet 1987; 41(2):218–248.
Zhang Y, Kreger BE, Dorgan JF, Cupples LA, Myers RH, Splansky GL, Schatzkin A, Ellison RC. Parental age at child’s birth and son’s risk of prostate cancer. The Framingham Study. Am J Epidemiol 1999; 150(11):1208–1212.
Aitken RJ, Baker MA and Sawyer D. Oxidative stress in the male germ line and its role in the aetiology of male infertility and genetic disease. Reprod Biomed Online 2003;7(1):65–70.
Shi Q and Martin RH. Aneuploidy in human sperm: a review of the frequency and distribution of aneuploidy, effects of donor age and lifestyle factors. Cytogenet Cell Genet 2000; 90(3–4):219–226.
Tiemann-Boege I, Navidi W, Grewal R, Cohn D, Eskenazi B, Wyrobek AJ and Arnheim N. The observed human sperm mutation frequency cannot explain the achondroplasia paternal age effect. Proc Natl Acad Sci USA 2002; 99(23):14952–14957.
Bosch M, Rajmil O, Egozcue J and Templado C. Linear increase of structural and numerical chromosome 9 abnormalities in human sperm regarding age. Eur J Hum Genet 2003;11(10):754–759.
Glaser RL, Broman KW, Schulman RL, Eskenazi B, Wyrobek AJ and Jabs EW. The paternal-age effect in Apert syndrome is due, in part, to the increased frequency of mutations in sperm. Am J Hum Genet 2003; 73(4):939-947.
Wyrobek AJ, Evenson D, Arnheim N, Jabs EW, Young S, Pearson F, Evenson D. Advancing male age increase the frequencies of sperm with DNA fragmentation and certain gene mutations, but not aneuploidies or diploidies. Proc Natl Acad Sci USA 2006; 103(25):9601–9606.
Spano M, Kolstad AH, Larsen SB, Cordelli E, Leter G, Giwercman A and Bonde JP. The applicability of the flow cytometric sperm chromatinstructure assay in epidemiological studies. Hum Reprod 1998; 13(9):2495-2505.
Morris ID. Sperm DNA damage and cancer treatment. Int J Androl 2002; 25(5):255–261.
Singh A and Agarwal A. The role of sperm chromatin integrity and DNA damage on male infertility. The Open Reprod Sci J 2011; 3:65-71.
World Health Organization. WHO laboratory manual for the examination and processing of human semen. 5th ed. 2010.
Marchettini P, Solaro C. To become a pain specialist one has tounderstand the nervous system, yet the specialists of the nervoussystem still have a long way to go before understanding pain. Neurol Sci 2007; 28: 161-162.
Fuentes-Mascorro G, Serrano H, Rosado A. Sperm chromatin. Arch Androl 2000; 45:215-225.
Ward WS. Function of sperm chromatin structural elements infertilization and development. Mol Hum Reprod 2010; 16:30-36.
Sotolongo B, Lino E, Ward WS. Ability of hamster spermatozoa to digest their own DNA. Biol Reprod 2003; 69:2029-2035.
Martins RP, Ostermeier GC, Krawetz SA. Nuclear matrix interactions at the human protamine domain: a working model of potentiation. J Biol Chem 2004; 279:51862-51868.
Ajduk A, Yamauchi Y, Ward MA. Sperm chromatin remodeling after intracytoplasmic sperm injection differs from that of in vitro
fertilization. Biol Reprod 2006; 75:442-451.
Ogura A, Matsuda J, Yanagimachi R. Birth of normal young after electrofusion of mouse ocytes with round spermatids. Proc Natl
Acad Sci USA 1994; 91:7460-7462.
Hammoud SS, Nix DA, Zhang H, Purwar J, Carrell DT, Cairns BR. Distinctive chromatin in human sperm packages genes for
embryo development. Nature 2009; 460:473-478.
Ostermeier GC, Goodrich RJ, Diamond MP, Dix DJ, Krawetz SA. Toward using stable spermatozoal RNAs for prognostic assessment of male factor fertility. Fertil Steril 2005; 83: 1687-1694.
Arpanahi A, Brinkworth M, Iles D, Krawetz SA, Paradowska A, Platts AE, Saida M, Steger K, Tedder P. Endonuclease-sensitive regions of human spermatozoal chromatin are highly enriched in promoter and CTCF binding sequences. Genome Res 2009; 19:1338-1349.
Van der Heijden GW, Ramos L, Baart EB. Sperm-derived histones contribute to zygotic chromatin in humans. BMC Dev Biol 2008; 8: 34.
Shaman JA, Yamauchi Y, Ward WS. The sperm nuclear matrix is required for paternal DNA replication. J Cell Biochem 2007; 102:680-688.
Spano M, Seli E, Bizzaro D, Manicardi GC, Sakkas D. The significance of sperm nuclear DNA strand breaks on reproductive outcome. Curr Opin Obstet Gynecol 2005; 17: 255-260.
Singh NP, Muller CH, Berger RE. Effects of age on DNA double strand breaks and apoptosis in human sperm. Fertil Steril 2003; 80:1420-1430.
Menezo Y, Dale B, Cohen M. DNA damage and repair in human oocytes and embryos: a review. Zygote 2010; 4: 357-365.
Erenpreiss J, Spano M, Erenpreisa J, Bungum M, Giwercman A. Sperm chromatin structure and male fertility: biological and clinical aspects. Asian J Androl 2006; 8:11-29.
Twigg J, Fulton N, Gomez E, Irvine DS, Aitken RJ. Analysis of the impact of intracellular reactive oxygen species generation on the structural and functional integrity of human spermatozoa: lipid peroxidation, DNA fragmentation and effectiveness of antioxidants. Hum Reprod 1998; 13: 1429-36.
Barnes CJ, Hardman WE, Maze GL, Lee M and Cameron IL. Age dependent sensitization to oxidative stress by dietary fatty acids. Aging (Milano)1998; 10(6):455–462.
Barroso G, Morshedi M and Oehninger S.Analysis of DNA fragmentation, plasma membrane translocation of phosphatidylserine and oxidative stress in human spermatozoa. Hum Reprod 2000;15(6),1338–1344.
Garrido N, Meseguer M, Simon C, Pellicer A, Remohi J. Prooxidative and anti-oxidative imbalance in human semen and its relation with male fertility. Asian J Androl 2004; 6:59-65.
Emokpae MA, Uadia PO, Mohammed AZ, Omale-ItodoA. Hormonal abnormalities in azoospermic men in Kano, Northern Nigeria. Indian J Med Res 2006; 124:299-303.
Emokpae MA, Uadia PO, Omole-Ohonsi A. Pattern of hormonal abnormalities and Association with sperm parameters among
oligospermic male partners of infertile couples. Nig Endoc Pract 2014; 8(1):13-19.
Emokpae MA,Uadia PO, Omale- Itodo A, Orok TN. Male infertility and Endocrinopathies in Kano, North Western Nigeria. Ann Afri Med 20076(2):64- 67.
Uadia PO, Emokpae MA. Male infertility in Nigeria: A neglected Reproductive Health issue requiring attention. J Basic Clin Reprod Scis 2015;4(2):45-53.
Uadia PO, Emokpae MA Implications of Oxidative Stress on Male Infertility.Trans Nig Soc Biochem Mole Biol 2015;1(1):19-29.
Esteves SC, Agarwal A. Novel Concepts in male infertility. Int Braz J Urol. 2011; 37(1):5-15.
Gonzalez-Flecha B. Oxidant mechanisms in response to ambient air particles. Mol Aspects Med 2004; 25:169-182.
Agarwal A, Makker K, Sharma R. Clinical relevance of oxidative stress in male factor infertility: an update. Am J Reprod Immunol
; 59:2-11.
Oremosu AA, Akang EN. Impact of alcohol on male reproductive hormones, oxidative stress and semen parameters in Sprague-Dawley rats. Middle East Fertil Soc J 2015; 20:114-118.
Emokpae MA, Chima HN, Ahmed M. Seminal plasma caspase 3, cytochrome c and total antioxidant capacity in oligospermic males and association with sperm indices.J Experiment integrat Med 2016; 6(4):1-4.
Almeida C, Sousa M, Barros A. Phosphatidylserine translocation in human spermatozoa from impaired spermatogenesis. Reprod Biomed Online. 2009; 19:770-777.
Gandini L, Lombardo F, Paoli D, Caponecchia L, Familiari G, Verlengia C, et al. Study of apoptotic DNA fragmentation in
human spermatozoa. Hum Reprod. 2000;15(4):830-839.
Marchetti C, Gallego MA, Deffosez A, Formstecher P, Marchetti P. Staining of human sperm with fluorochrome-labeled inhibitor of caspases to detect activated caspases: correlation with apoptosis and sperm parameters. Hum Reprod. 2004;19(5):1127-
Oosterhuis GJ, Mulder AB, Kalsbeek-Batenburg E, Lambalk CB, Schoemaker J,Vermes I. Measuring apoptosis in human spermatozoa: a biological assay for semen quality? Fertil Steril. 2000; 74:245-250.
Zhang H, Chen Z, Ma C, Lu S, Wang L, Li X. Early apoptotic changes in human spermatozoa and their relationships with conventional semen parameters and sperm DNA fragmentation. Asian J Androl. 2008; 10:227-235.
Johnson L, Thompson Jr DL, Varner DD. Role of Sertoli cell number and function on regulation of spermatogenesis. Anim Reprod Sci. 2008;105(1-2):23-51.
Pentikainen V, Erkkila K, Dunkel L. Fas regulates germ cell apoptosis in the human testis in vitro. Am J Physiol. 1999;276(2
Pt 1):E310–306.
Eguchi J, Koji T, Nomata K, Yoshii A, Shin M, Kanetake H. FasFas ligand as a possible mediator of spermatogenic cell apoptosis
in human maturation-arrested testes. Hum Cell. 2002;15(1):61-68.
Hassan MA, Killick SR. Effect of male age on fertility: Evidence for the decline in male fertility with increasing age. Fertil Steril 2003;79 Suppl 3:1520‑1527.
Gennart JP, Buchet JP, Roels H,Ghyselen P, Cuelemans E, Lauerys R. Fertility of male workers exposed to cadmium, lead or manganese. Am J Epidemiol 1992; 135:1208-1219.
Kasahara E, Sato EF, Miyoshi M, Konaka R, Hiramoto K, SasakiJ, Tokuda M, Nakano Y, Inoue M. Role of oxidative stress in germ cell apoptosis induced by di-(2-ethylhexyl) phthalate. Biochem J 2002; 365:849-856.
Gonzalez-Flecha B. Oxidant mechanisms in response to ambient air particles. Mol Aspects Med. 2004; 25:169-182.
Aitken RJ, Curry BJ. Redox regulation of human sperm function: from the physiological control of sperm capacitation to the etiology of infertility and DNA damage in the germ line. Antioxid Redox Signal 2011; 14: 367–381.
Aitken RJ, Gibb Z, Mitchell LA, Lambourne SR, Connaughton HS, De luliis GN. Sperm motility is lost in vitro as a consequence of mitochondrial free radical production and the generation of electrophilic aldehydes but can be significantly rescued by the presence of nucleophilic thiols. Biol Reprod 2012; 87:110.
Aitken RJ, Smith TB, Jobling MS, Baker MA, De Luliis GN. Oxidative stress and male reproductive health. Asian J Androl
; 16:31-38.
Baumber J, Ball BA, Gravance CG, Medina V, Davies-Morel MC. The effect of reactive oxygen species on equine sperm motility, viability, acrosomal integrity,mitochondrial membrane potential, and membrane lipid peroxidation. J Androl 2000; 21: 895–902.
Aitken RJ, Buckingham D, Harkiss D. Use of a xanthine oxidase free radical generating system to investigate the cytotoxic effects of reactive oxygen species on human spermatozoa. J Reprod Fertil 1993; 97:441–450.
Awda BJ, Mackenzie‑Bell M, Buhr MM. Reactive oxygen species and boar sperm function. Biol Reprod 2009; 81:553–561.
Martinez‑Pastor F, Aisen E, Fernandez‑Santos MR, Esteso MC, Maroto-Morales A,et al. Reactive oxygen species generators affect quality parameters and apoptosis markers differently in red deer spermatozoa. Reproduction 2009; 137: 225–235.
de Lamirande E, Gagnon C. Reactive oxygen species and human spermatozoa. II. Depletion of adenosine triphosphate plays an important role in the inhibition of sperm motility. J Androl 1992; 13: 379–386.
Tsunoda S, Kawano N, Miyado K, Kimura N, Fujii J. Impaired fertilizing ability of superoxide dismutase 1-deficient mouse sperm during in vitro fertilization. Biol Reprod 2012; 87: 121.
Wishart GJ. Effects of lipid peroxide formation in fowl semen on sperm motility, ATP content and fertilizing ability. J Reprod Fertil 1984; 71: 113–118.
Gomez E, Irvine DS, Aitken RJ. Evaluation of a spectrophotometric assay for the measurement of malondialdehyde and 4-hydroxyalkenals in human spermatozoa:relationships with semen quality and sperm function. Int J Androl 1998; 21:81–94.
Aitken RJ, Gordon E, Harkiss D, Twigg JP, Milne P, Jennings Z, Irvine DS. Relative impact of oxidative stress on the functional competence and genomic integrity of human spermatozoa. Biol Reprod 1998; 59: 1037–1046.
Aitken RJ, Harkiss D, Knox W, Paterson M, Irvine DS. A novel signal transduction cascade in capacitating human spermatozoa characterised by a redox-regulated, cAMP-mediated induction of tyrosine phosphorylation. J Cell Sci 1998; 111:645–656.
Brouwers JF, Boerke A, Silva PF, Garcia-Gil N, van Gestel RA, Helms JB, va de Lest CH, Gadella BM. Mass spectrometric detection of cholesterol oxidation in bovine sperm. Biol Reprod 2011;85: 128–136.
Christova Y, James PS, Jones R. Lipid diffusion in sperm plasma membranes exposed to peroxidative injury from oxygen free radicals. Mol Reprod Dev 2004; 68:365–372.
Emokpae MA,Uadia PO. Acrosin Activity in Spermatozoa of Infertile Nigerian Males. Indian J Clin Biochem, 2006; 12(1): 199-201.
Zalata AA, Ahmed AH, Allamaneni SSR, Comhaire FH and Ashok A. Relationship between acrosin activity of human spermatozoa and oxidative stress.Asian J.Androl. 2003; 6:313-318.
Iannaccone PM. Conception,implantation and early development. In:Principles and practice of Endocrinology and metabolism. ed. Kenneth L. Becher, JB Lippincott company Philadelphia, Grand Rapids New York St. Louis San Francisco,London, Sydney, Tokyo: 1990:881-882.
Emokpae MA, Emokpae LA. Calcium concentration in semen Of Azoospermic Nigerians. J Med Lab Sci 1997; 6:43 – 44.
Singh NP, Muller CH and Berger RE. Effects of age on DNA double strand breaks and apoptosis in human sperm. Fertil Steril
; 80(6):1420–1430.
Paul C, Nagano M, Robaire B. Aging results in differential regulation of DNA repair pathways in pachytene spermatocytes in the Brown Norway rat. Biol Reprod 2011; 85: 1269–1278.
Crow JF. The origins, patterns and implications of human spontaneous mutation. Nat Rev Genet 2000; 1:40–47.
Crow JF. Upsetting the dogma: germline selection in human males. PLoS Genet 2012; 8: e1002535.
Goriely A, McVean GA, Rojmyr M, Ingemarsson B, Wilkie AO.Evidence for selective advantage of pathogenic FGFR2 mutations in the male germ line. Science 2003; 301:643–646.
Koppers AJ, Garg ML, Aitken RJ. Stimulation of mitochondrial reactive oxygen species production by unesterified, unsaturated fatty acids in defective human spermatozoa.Free Radic Biol Med 2010; 48: 112–119.
Kong A, Frigge ML, Masson G, Besenbacher S, Sulem P, Magnusson G, Gudjonsson SA, Sigurdsson A, Jonasdottir A, Jonasdottir A, Wong WSW, Helgason H, Thorleifsson G, Gudbjartsson DF, Helgason A, Magnusson OT, Thorsteinsdottir U, Stefansson K. Rate of de novo mutations and the importance of father’s age to disease risk.Nature 2012;488:471-475.
Aitken RJ, Roman SD. Antioxidant systems and oxidative stress in the testes. Adv Exp Med Biol 2008; 636: 154–171.
Gosden R, Trasler J, Lucifero D, Faddy M. Rare congenital disorders, imprinted genes, and assisted reproductive technology. Lancet 2003; 361: 1975-1977.
Hansen M, Kurinczuk JJ, Bower C, Webb S. The risk of major birth defects after intracytoplasmic sperm injection and in vitro
fertilization. N Engl J Med 2002; 346: 725-730.91. Ericson A, Nygren KG, Olausson PO, Kallen B. Hospital care utilization of infants born after IVF. Hum Reprod 2002; 17: 929-932.
Kallen B, Finnstrom O, Nygren KG, Olausson PO. In vitro fertilization in Sweden: child morbidity including cancer risk. Fertil Steril 2005; 84: 605–610.
Klemetti R, Sevon T, Gissler M, Hemminki E. Health of children born as a result of in vitro fertilization. Pediatrics 2006; 118:
–1827.
Aitken RJ, Findlay JK, Hutt KJ, Kerr JB. Apoptosis in the germ line. Reproduction 2011; 141: 139–150.
Unryn BM, Cook LS, Riabowol KT. Paternal age is positively linked to telomere length of children. Aging Cell 2005; 4: 97–101.
Shammas MA. Telomeres, lifestyle, cancer, and aging. Curr Opin Clin Nutr Metab Care 2011; 14: 28–34