DNA damage in bovine sperm does not block fertilization and early embryonic development but induces apoptosis after the first cleavages

Journal of Andrology

Volumn 27, Issue 2, 2006, Pages 176-188

  Fatehi, A N ^a   Bevers, M M ^a   Schoevers, E ^a   Roelen, B A J ^a   Colenbrander, B ^a   Gadella, B M ^b  

^a UTRECHT UNIVERSITY   (Netherlands)

^b UTRECHT UNIVERSITY   (Netherlands)

Author keywords

Blastocyst; ICSI; Mitotic spindles

Indexed keywords

ACRIDINE ORANGE; DNA;

ACROSOME REACTION; ANIMAL CELL; APOPTOSIS; ARTICLE; BLASTOCYST; CELL DIVISION; CELL MEMBRANE; CONTROLLED STUDY; DNA DAMAGE; EMBRYO; EMBRYO DEVELOPMENT; EMBRYO TRANSFER; FERTILIZATION; FERTILIZATION IN VITRO; GAMMA IRRADIATION; GENE EXPRESSION; INTRACYTOPLASMIC SPERM INJECTION; MALE INFERTILITY; MEMBRANE DEPOLARIZATION; MITOCHONDRIAL MEMBRANE; MITOSIS SPINDLE; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; RADIATION DOSE; REPRODUCTION; SPERM; SPERMATOZOON MOTILITY; SUBFERTILITY; X IRRADIATION;

ACROSOME; ANIMALS; APOPTOSIS; CATTLE; CELL MEMBRANE; DNA DAMAGE; EMBRYONIC DEVELOPMENT; FEMALE; FERTILIZATION; GAMMA RAYS; MALE; MITOCHONDRIAL MEMBRANES; MODELS, ANIMAL; OOCYTES; PREGNANCY; SPERM MOTILITY; SPERMATOZOA; X-RAYS;

EID: 33644519981     PISSN: 01963635     EISSN: None     Source Type: Journal    
DOI: 10.2164/jandrol.04152     Document Type: Article

References (84)

1. Ahmadi A, Ng SC. Fertilizing ability of DNA-damaged spermatozoa. J Exp Zool. 1999;284:696-704.
2. Aitken RJ. The Amoroso Lecture. The human spermatozoon-a cell in crisis? J Reprod Fertil. 1999;115:1-7.
3. 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.
4. Arney KL, Bao S, Bannister AJ, Kouzarides T, Surani MA. Histone methylation defines epigenetic asymmetry in the mouse zygote. Int J Dev Biol. 2002;46:317-320.
5. Baccetti B, Collodel G, Piomboni P. Apoptosis in human ejaculated sperm cells (notulae seminologicae 9). J Submicrosc Cytol Pathol. 1996;28:587-596.
6. Beker-van Woudenberg AR, van Tol HT, Roelen BA, Colenbrander B, Bevers MM. Estradiol and its membrane-impermeable conjugate (estradiol-bovine serum albumin) during in vitro maturation of bovine oocytes: effects on nuclear and cytoplasmic maturation, cytoskeleton, and embryo quality. Biol Reprod. 2004;70:1465-1474.
7. Bonduelle M, Liebaers I, Deketelaere V, Derde M-P, Camus M, Devroey P, van Steirteghem A. Neonatal data on a cohort of 2889 infants born after ICSI (1991-1999) and of 2995 infants born after IVF (1983-1999). Hum Reprod. 2002b;17671-17694.
8. Bonduelle M, Van Assche E, Joris H, Keymolen K, Devroey P, Van Steirteghem A, Liebaers I. Prenatal testing in ICSI pregnancies: incidence of chromosomal anomalies in 1586 karyotypes and relation to sperm parameters. Hum Reprod. 2002a;17:2600-2614.
9. Bonduelle M, Wilikens A, Buysse A, Van Assche E, Devroey P, Van Steirteghem AC, Liebaers I. A follow-up study of children born after intracytoplasmic sperm injection (ICSI) with epididymal and testicular spermatozoa and after replacement of cryopreserved embryos obtained after ICSI. Hum Reprod. 1998;13(suppl 1):196-207.
10. Bordignon V, Smith LC. Ultraviolet-irradiated spermatozoa activate oocytes but arrest preimplantation development after fertilization and nuclear transplantation in cattle. Biol Reprod. 1999;61:1513-1520.
11. Brandriff B, Pedersen RA. Repair of the ultraviolet-irradiated male genome in fertilized mouse eggs. Science. 1981;211:1431-1433.
12. Brinkworth MH. Paternal transmission of genetic damage: findings in animals and humans. Int J Androl. 2000;23:123-135.
13. Buitendijk SE. Children after in vitro fertilization. An overview of the literature. Int J Technol Assess Health Care. 1999;15:52-65.
14. Campbell AJ, Irvine DS. Male infertility and intracytoplasmic sperm injection (ICSI). Br Med Bull. 2000;56:616-629.
15. Carrano AV. Chromosomal alterations as markers of exposure and effect. J Occup Med. 1986;28:1112-1116.
16. Chandley AC, Kofman-Alfaro S. "Unscheduled" DNA synthesis in human germ cells following UV irradiation. Exp Cell Res. 1971;69:45-48.
17. Cleaver JE. Restriction enzyme cleavage of ultraviolet-damaged simian virus 40 and pBR322 DNA. J Mol Biol. 1983;170:305-317.
18. Collins JA, Burrows EA, Wilan AR. The prognosis for live birth among untreated infertile couples. Fertil Steril. 1995;64:22-28.
19. Cox GF, Burger J, Lip V, Mau UA, Sperling K, Wu BL, Horsthemke B. Intracytoplasmic sperm injection may increase the risk of imprinting defects. Am J Hum Genet. 2002;71:162-164.
20. De Sousa PA, Watson AJ, Schultz GA, Bilodeau-Goeseels S. Oogenetic and zygotic gene expression directing early bovine embryogenesis: a review. Mol Reprod Dev. 1998;51:112-121.
21. De Vries KJ, Wiedmer T, Sims PJ, Gadella BM. Caspase-independent exposure of aminophospholipids and tyrosine phosphorylation in bicarbonate responsive human sperm cells. Biol Reprod. 2003;6:2122-2134.
22. Devroey P, van Steirteghem A. A review of ten years experience of ICSI. Hum Reprod Update. 2004;10:19-28.
23. Doyle YG, McNeilly RH. The diffusion of new medical technologies in the private sector of the U.K. health care system. Int J Technol Assess Health Care. 1999;15:619-628.
24. Egozcue S, Vendrell JM, Garcia F, Veiga A, Aran B, Barri PN, Egozcue J. Increased incidence of meiotic anomalies in oligoasthenozoospermic males preselected for intracytoplasmic sperm injection. J Assist Reprod Genet. 2000;17:307-309.
25. Ericson A, Kallen B. Congenital malformations in infants born after IVF: a population-based study. Hum Reprod. 2001;16:504-509.
26. Evenson DP, Jost LK, Baer RK, Turner TW, Schrader SM. Individuality of DNA denaturation patterns in human sperm as measured by the sperm chromatin structure assay. Reprod Toxicol. 1991;5:115-125.
27. Evenson DP, Larson KL, Jost LK. Sperm chromatin structure assay: its clinical use for detecting sperm DNA fragmentation in male infertility and comparisons with other techniques. J Androl. 2002;23:25-43.
28. Fatehi AN, Zeinstra EC, Kooij RV, Colenbrander B, Bevers MM. Effect of cumulus cell removal of in vitro matured bovine oocytes prior to in vitro fertilization on subsequent cleavage rate. Theriogenology. 2002;57:1347-1355.
29. Flesch FM, Voorhout WF, Colenbrander B, van Golde LM, Gadella BM. Use of lectins to characterize plasma membrane preparations from boar spermatozoa: a novel technique for monitoring membrane purity and quantity. Biol Reprod. 1998;59:1530-1539.
30. Gadella BM, Harrison RA. Capacitation induces cyclic adenosine 3',5'-monophosphate-dependent, but apoptosis-unrelated, exposure of aminophospholipids at the apical head plasma membrane of boar sperm cells. Biol Reprod. 2002;67:340-350.
31. Gamen S, Anel A, Perez-Galan P, Lasierra P, Johnson D, Pineiro A, Naval J. Doxorubicin treatment activates a Z-VAD-sensitive caspase, which causes deltapsim loss, caspase-9 activity, and apoptosis in Jurkat cells. Exp Cell Res. 2000;258:223-235.
32. Gandolfi TA, Gandolfi F. The maternal legacy to the embryo: cytoplasmic components and their effects on early development. Theriogenology. 2001;55:1255-1276.
33. Generoso WM, Cain KT, Krishna M, Huff SW. Genetic lesions induced by chemicals in spermatozoa and spermatids of mice are repaired in the egg. Proc Natl Acad Sci U S A. 1979;76:435-437.
34. Gledhill BL, Darzynkiewicz Z. Unscheduled synthesis of DNA during mammalian spermatogenesis in response to UV irradiation. J Exp Zool. 1973;183:375-382.
35. Gomez E, Aitken J. Impact of in vitro fertilization culture media on peroxidative damage to human spermatozoa. Fertil Steril 1996;65:880-882.
36. Gorczyca W, Gong J, Darzynkiewicz Z. Detection of DNA strand breaks in individual apoptotic cells by the in situ terminal deoxynucleotidyl transferase and nick translation assays. Cancer Res. 1993;53:1945-1951.
37. Gulbins E, Dreschers S, Bock J. Role of mitochondria in apoptosis. Exp Physiol. 2003;88:85-90.
38. Hales BF, Robaire B. Reversibility of the effects of chronic paternal exposure to cyclophosphamide on pregnancy outcome in rats. Mutat Res. 1990;229:129-134.
39. Hales BF, Robaire B. Paternal exposure to drugs and environmental chemicals: effects on progeny outcome. J Androl 2001;22:927-936.
40. Hansen M, Kurinczuk JJ, Bower C, Webb S. The risk of major birth defects after intracytoplasmatic sperm injection and in vitro fertilization. N Engl J Med. 2002;346:725-730.
41. Hargreave T. Genetically determined male infertility and assisted reproduction techniques. J Endocrinol Invest. 2000a;23:697-710.
42. Hargreave TB. Genetic basis of male fertility. Br Med Bull 2000b;56:650-671.
43. Hargreave TB. Genetics and male infertility. Curr Opin Obstet Gynecol. 2000c;12:207-219.
44. Hendriksen PJ, Gadella BM, Vos PL, Mullaart E, Kruip TA, Dieleman SJ. Follicular dynamics around the recruitment of the first follicular wave in the cow. Biol Reprod. 2003;69:2036-2044.
45. Izadyar F, Zeinstra E, Colenbrander B, Vanderstichele HM, Bevers MM. In vitro maturation of bovine oocytes in the presence of bovine activin A does not affect the number of embryos. Anim Reprod Sci. 1996;45:37-45.
46. Jarow JP. Detection of oxidative DNA damage in human sperm and the association with cigarette smoking. J Urol. 1998;159:1774-1775.
47. Kaina B. DNA damage-triggered apoptosis: critical role of DNA repair, double-strand breaks, cell proliferation and signaling. Biochem Pharmacol. 2003;66:1547-1554.
48. Karaki RZ, Samarraie SS, Younis NA, Lahloub TM, Ibrahim MH. Blastocyst culture and transfer: a step toward improved in vitro fertilization outcome. Fertil Steril. 2002;77:114-118.
49. Kellogg DR, Moritz M, Alberts BM. The centrosome and cellular organization. Annu Rev Biochem. 1994;63:639-674.
50. Kondro W. Proposed curbs on reproductive technology. Lancet. 1993;342:1477-1478.
51. Lopes S, Sun JG, Jurisicova A, Meriano J, Casper RF. Sperm deoxyribonucleic acid fragmentation is increased in poor-quality semen samples and correlates with failed fertilization in intracytoplasmic sperm injection. Fertil Steril. 1998;69:528-532.
52. Ludwig M, Katalinic A. Pregnancy course and health of children born after ICSI depending on parameters of male factor infertility. Hum Reprod. 2003;18:351-357.
53. Makrigiorgos GM, Adelstein SJ, Kassis AI. Cellular radiation dosimetry and its implications for estimation of radiation risks. Illustrative results with technetium 99m-labeled microspheres and macroaggregates. JAMA. 1990;264:592-595.
54. Masui Y, Pedersen RA. Ultraviolet light-induced unscheduled DNA synthesis in mouse oocytes during meiotic maturation. Nature. 1975;257:705-706.
55. Milki AA, Hinckley MD, Fisch JD, Dasig D, Behr B. Comparison of blastocyst transfer with day 3 embryo transfer in similar patient populations. Fertil Steril. 2000;73:126-129.
56. Mortimer D. The future of male infertility management and assisted reproduction technology. Hum Reprod. 2000;15(suppl 5):98-110.
57. Moustafa MH, Sharma RK, Thornton J, Mascha E, Abdel-Hafez MA, Thomas AJ Jr, Agarwal A. Relationship between ROS production, apoptosis and DNA denaturation in spermatozoa from patients examined for infertility. Hum Reprod. 2004;19:129-138.
58. Nagata S, Nagase H, Kawane K, Mukae N, Fukuyama H. Degradation of chromosomal DNA during apoptosis. Cell Death Differ. 2003;10:108-116.
59. Navara CS, Simerly C, Zoran S, Schatten G. The sperm centrosome during fertilization in mammals: implications for fertility and reproduction. Reprod Fertil Dev. 1995;7:747-754.
60. Nudell D, Castillo M, Turek PJ, Pera RR. Increased frequency of mutations in DNA from infertile men with meiotic arrest. Hum Reprod. 2000;15:1289-1294.
61. O'Brien DA, Welch JE, Fulcher KD, Eddy EM. Expression of mannose 6-phosphate receptor messenger ribonucleic acids in mouse spermatogenic and Sertoli cells. Biol Reprod. 1994;50:429-435.
62. Oliva R, Dixon GH. Vertebrate protamine genes and the histone-to-protamine replacement reaction. Prog Nucleic Acid Res Mol Biol. 1991;40:25-94.
63. Painter RB. Response of Chinese hamster ovary cells to DNA damage after a conditioning exposure to ultraviolet light. Biochim Biophys Acta. 1980;609:257-263.
64. Parrish JJ, Susko-Parrish J, Winer MA, First NL. Capacitation of bovine sperm by heparin. Biol Reprod. 1988;38:1171-1180.
65. Sailer BL, Jost LK, Evenson DP. Mammalian sperm DNA susceptibility to in situ denaturation associated with the presence of DNA strand breaks as measured by the terminal deoxynucleotidyl transferase as-say. J Androl. 1995;16:80-87.
66. Sakkas D, Manicardi G, Bizzaro D, Bianchi PG. Possible consequences of performing intracytoplasmic sperm injection (ICSI) with sperm possessing nuclear DNA damage. Hum Fertil. 2000;3:26-30.
67. Sakkas D, Mariethoz E, Manicardi G, Bizzaro D, Bianchi PG, Bianchi U. Origin of DNA damage in ejaculated human spermatozoa. Rev Reprod. 1999;4:31-37.
68. Sancar A, Sancar GB. DNA repair enzymes. Annu Rev Biochem. 1988;57:29-67.
69. Scovassi AI, Torriglia A. Activation of DNA-degrading enzymes during apoptosis. Eur J Histochem. 2003;47:185-194.
70. Shen H, Ong C. Detection of oxidative DNA damage in human sperm and its association with sperm function and male infertility. Free Radic Biol Med. 2000;28:529-536.
71. Shen HM, Chia SE, Ni ZY, New AL, Lee BL, Ong CN. Detection of oxidative DNA damage in human sperm and the association with cigarette smoking. Reprod Toxicol. 1997;11:675-680.
72. Shi Q, 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;90:219-226.
73. Simerly C, Schatten G. Techniques for localization of specific molecules in oocytes and embryos. Methods Enzymol. 1993;225:516-553.
74. Snick HK, Snick TS, Evers JL, Collins JA. The spontaneous pregnancy prognosis in untreated subfertile couples: the Walcheren primary care study. Hum Reprod. 1997;12:1582-1588.
75. Somfai T, Bodo S, Nagy S, Papp AB, Ivancsics J, Baranyai B, Gocza E, Kovacs A. Effect of swim up and Percoll treatment on viability and acrosome integrity of frozen-thawed bull spermatozoa. Reprod Domest Anim. 2002;37:285-290.
76. Spandidos DA, Koumantakis E, Sifakis S, Sourvinos G. Microsatellite mutations in spontaneously aborted embryos. Fertil Steril. 1998;70:892-895.
77. Spanos S, Rice S, Karagiannis P, Taylor D, Becker DL, Winston RM, Hardy K. Caspase activity and expression of cell death genes during development of human preimplantation embryos. Reproduction. 2002;124:353-363.
78. Sun JG, Jurisicova A, Casper RF. Detection of deoxyribonucleic acid fragmentation in human sperm: correlation with fertilization in vitro. Biol Reprod. 1997;56:602-607.
79. Tateno H, Kamiguchi Y, Shimada M, Mikamo K. Difference in types of radiation-induced structural chromosome aberrations and their incidences between Chinese and Syrian hamster spermatozoa. Mutat Res. 1996;350:339-348.
80. Van Landuyt L, de Vos A, Joris H, Verheyen G, Devroey P, van Steirteghem A. Blastocyst formation in in vitro fertilization versus intracytoplasmatic sperm injection cycles: influence of the fertilization procedure. Fertil Steril. 2005;83:1397-1403
81. Viuff D, Avery B, Greve T, King WA, Hyttel P. Transcriptional activity in in vitro produced bovine two- and four-cell embryos. Mol Reprod Dev. 1996;43:171-179.
82. Weil M, Jacobson MD, Coles HS, Davies TJ, Gardner RL, Raff KD, Raff MC. Constitutive expression of the machinery for programmed cell death. J Cell Biol. 1996;133:1053-1059.
83. Yamazaki Y, Tsuruga M, Zhou D, Fujita Y, Shang X, Dang Y, Kawasaki K, Oka S. Cytoskeletal disruption accelerates caspase-3 activation and alters the intracellular membrane reorganization in DNA damage-induced apoptosis. Exp Cell Res. 2000;259:64-78.
84. Zhang D, Nicklas RB. The impact of chromosomes and centrosomes on spindle assembly as observed in living cells. J Cell Biol. 1995;129:1287-1300.