Cytogenetic analysis of in vivo and in vitro matured oocytes derived from naturally cycling and stimulated mice

Systems Biology in Reproductive Medicine

Volumn 54, Issue 3, 2008, Pages 155-162

  Xu, Lan ^a   Wang, Yue ^b   Zhou, Ping ^c   Cao, Yun Xia ^c   Huang, Tian Hua ^d   Chian, Ri Cheng ^b  

^a THE FIRST AFFILIATED HOSPITAL OF SHANTOU UNIVERSITY MEDICAL COLLEGE   (China)

^b MCGILL UNIVERSITY   (Canada)

^c ANHUI MEDICAL UNIVERSITY   (China)

^d SHANTOU UNIVERSITY MEDICAL COLLEGE   (China)

Author keywords

aneuploidy; chromosomal alignment; meiotic spindle; mouse; oocytes

Indexed keywords

CHORIONIC GONADOTROPIN; FERTILITY PROMOTING AGENT; FOLLITROPIN; RECOMBINANT PROTEIN;

ANEUPLOIDY; ANIMAL; ARTICLE; CELL CULTURE; CHROMOSOME ANALYSIS; CHROMOSOME SEGREGATION; DRUG EFFECT; FEMALE; GENETICS; HUMAN; IMMUNOHISTOCHEMISTRY; MEIOSIS; MOUSE; OOCYTE; OOCYTE DEVELOPMENT; OVULATION INDUCTION; TIME;

ANEUPLOIDY; ANIMALS; CELLS, CULTURED; CHORIONIC GONADOTROPIN; CHROMOSOME SEGREGATION; CYTOGENETIC ANALYSIS; FEMALE; FERTILITY AGENTS, FEMALE; FOLLICLE STIMULATING HORMONE; HUMANS; IMMUNOHISTOCHEMISTRY; MEIOSIS; MICE; OOCYTES; OOGENESIS; OVULATION INDUCTION; RECOMBINANT PROTEINS; TIME FACTORS;

EID: 51449116560     PISSN: 19396368     EISSN: 19396368     Source Type: Journal    
DOI: 10.1080/19396360802102012     Document Type: Review

References (129)

1. Agarwal, A. and Said, T. M. (2004) Sperm Chromatin Assessment. Textbook of ART, PLC, London, UK. 7:93-106.
2. Agarwal, A., Said, T. M., Bedaiwy, M. A., Banerjee, J. and Alvarez, J. G. (2006) Oxidative stress in an assisted reproductive techniques setting. Fertil Steril 86:503-512.
3. Agbaje, I. M., McVicar, C. M., Schock, B. C., McClure, N., Atkinson, A. B., Rogers, D. A. and Lewis, S. E. M. (2007) Increased levels of the Oxidative DNA adduct 7, 8-dihydro-8-oxo-20-deoxoguanosine in the germ-line of men with type-1 diabetes. Reprod Biomed 16:401-409.
4. Ahmadi, A. and Ng, S. C. (1999a) Developmental capacity of damaged spermatozoa. Hum Reprod 14:2279-2285.
5. Ahmadi, A. and Ng, S. C. (1999b) Fertilizing ability of DNA-damaged spermatozoa. Journal of Experimental Zoology 284:696-704.
6. Aitken, J. and Fisher, H. (1994) Reactive oxygen species generation and human spermatozoa: the balance of benefit and risk. Bioessays 16:259-267.
7. Aitken, R. J. (2004) Founders' Lecture. Human spermatozoa: fruits of creation, seeds of doubt. Reprod Fertil Dev 16:655-664.
8. Aitken, R. J. (2006) Sperm function tests and fertility. Int J Androl 29: 69-75; discussion 105-108.
9. Aitken, R. J., Baker, M. A. and Sawyer, D. (2003a) Oxidative stress in the male germ line and its role in the aetiology of male infertility and genetic disease. Reprod Biomed Online 7:65-70.
10. Aitken, R. J., Ryan, A. L., Curry, B. J. and Baker, M. A. (2003b) Multiple forms of redox activity in populations of human spermatozoa. Mol Hum Reprod 9:645-661.
11. Aitken, R. J. and De Luliis, G. N. (2007) Value of DNA integrity assays for fertility evaluation. Soc Reprod Fertil Suppl 65:81-92.
12. Aitken, R. J., Gordon, E., Harkiss, D., Twigg, J. P., Milne, P., Jennings, Z. and Irvine, D. S. (1998) Relative impact of oxidative stress on the functional competence and genomic integrity of human spermatozoa. Biol Reprod 59:1037-1046.
13. Aitken, R. J. and Krausz, C. (2001) Oxidative stress, DNA damage and the Y chromosome. Reproduction 122:497-506.
14. Aitken, R. J. and Sawyer, D. (2003) The human spermatozoon-not waving but drowning. Adv Exp Med Biol 518:85-98.
15. Alvarez, J. G. (2005a) 'Efficient treatment of infertility due to sperm DNA damage by ICSI with testicular sperm'. Hum Reprod 20:2031-2032; author reply 2032-2033.
16. Alvarez, J. G. (2005b) The predictive value of sperm chromatin structure assay. Hum Reprod 20:2365-2367.
17. Andersen, A. N. and Erb, K. (2006) Register data on assisted reproductive technology (ART) in Europe. Including a detailed description of ART in Denmark. International Journal of Andrology 29:12-16.
18. Arabi, M. and Moshtaghi, H. (2005) Influence of cigarette smoking on spermatozoa via seminal plasma. Andrologia 37:119-124.
19. Aravindan, G. R., Bjordahl, J., Jost, L. K. and Evenson, D. P. (1997) Susceptibility of human sperm to in situ DNA denaturation is strongly correlated with DNA strand breaks identified by single-cell electrophoresis. Exp Cell Res 236:231-237.
20. ASRM (2006) The clinical utility of sperm DNA integrity testing. Fertil Steril 86:S35-S37.
21. Aust, A. E. and Eveleigh, J. F. (1999) Mechanisms of DNA oxidation. Proc Soc Exp Biol Med 222:246-252.
22. Baker, M. A. and Aitken, R. J. (2005) Reactive oxygen species in spermatozoa: methods for monitoring and significance for the origins of genetic disease and infertility. Reprod Biol Endocrinol 3:67.
23. Bar-Hava, I., Ashkenazi, J., Shelef, M., Schwartz, A., Brengauz, M., Feldberg, D., Orvieto, R. and Ben-Rafael, Z. (1997) Morphology and clinical outcomes of embryos after in vitro fertilization are superior to those after intracytoplasmic sperm injection. Fertil Steril 68:653-657.
24. Benchaib, M., Braun, V., Lornage, J., Hadj, S., Salle, B., Lejeune, H. and Guerin, J. F. (2003) Sperm DNA fragmentation decreases the pregnancy rate in an assisted reproductive technique. Hum Reprod 18:1023-1028.
25. Benchaib, M., Lornage, J., Mazoyer, C., Lejeune, H., Salle, B. and Francois Guerin, J. (2007) Sperm deoxyribonucleic acid fragmentation as a prognostic indicator of assisted reproductive technology outcome. Fertil Steril 87:93-100.
26. Braude, P., Bolton, V. and Moore, S. (1988) Human gene expression first occurs between the four- and eight-cell stages of preimplantation development. Nature 332:459-461.
27. Bungum, M., Humaidan, P., Axmon, A., Spano, M., Bungum, L., Erenpreiss, J. and Giwercman, A. (2007) Sperm DNA integrity assessment in prediction of assisted reproduction technology outcome. Hum Reprod 22:174-179.
28. Bungum, M., Humaidan, P., Spano, M., Jepson, K., Bungum, L. and Giwercman, A. (2004) The predictive value of sperm chromatin structure assay (SCSA) parameters for the outcome of intrauterine insemination, IVF and ICSI. Hum Reprod 19:1401-1408.
29. Bungum, M., Spanò , M., Humaidan, P., Eleuteri, P., Rescia, M. and Giwercman, A. (2008) Sperm chromatin structure assay parameters measured after density gradient centrifugation are not predictive for the outcome of ART. Hum Reprod 1:4-10.
30. Carrell, D. T., Liu, L., Peterson, C. M., Jones, K. P., Hatasaka, H. H., Erickson, L. and Campbell, B. (2003) Sperm DNA fragmentation is increased in couples with unexplained recurrent pregnancy loss. Arch Androl 49:49-55.
31. Cheng, K. C., Cahill, D. S., Kasai, H., Nishimura, S. and Loeb, L. A. (1992) 8-Hydroxyguanine, an abundant form of oxidative DNA damage, causes G-T and A-C substitutions. J Biol Chem 267:166-172.
32. Cooke, M. S., Evans, M. D., Dizdaroglu, M. and Lunec, J. (2003) Oxidative DNA damage: mechanisms, mutation, and disease. Faseb J 17:1195-1214.
33. Croteau, D. L. and Bohr, V. A. (1997) Repair of oxidative damage to nuclear and mitochondrial DNA in mammalian cells. J Biol Chem 272:25409-25412.
34. Crow, J. F. (2000) The origins, patterns and implications of human spontaneous mutation. Nat Rev Genet 1:40-47.
35. Cummins, J. M., Jequier, A. M. and Kan, R. (1994) Molecular biology of human male infertility: links with aging, mitochondrial genetics, and oxidative stress? Mol Reprod Dev 37:345-362.
36. De Iuliis, G. N., Wingate, J. K., Koppers, A. J., McLaughlin, E. A. and Aitken, R. J. (2006) Definitive evidence for the nonmitochondrial production of superoxide anion by human spermatozoa. J Clin Endocrinol Metab 91:1968-1975.
37. Donnelly, E. T., McClure, N. and 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 14:505-512.
38. Donnelly, E. T., O'Connell, M., McClure, N. and Lewis, S. E. (2000) Differences in nuclear DNA fragmentation and mitochondrial integrity of semen and prepared human spermatozoa. Hum Reprod 15:1552-1561.
39. Duran, E. H., Morshedi, M., Taylor, S. and Oehninger, S. (2002) Sperm DNA quality predicts intrauterine insemination outcome: a prospective cohort study. Hum Reprod 17:3122-3128.
40. Erenpreiss, J., Bungum, M., Spano, M., Elzanaty, S., Orbidans, J. and Giwercman, A. (2006) Intra-individual variation in sperm chromatin structure assay parameters in men from infertile couples: clinical implications. Hum Reprod 21:2061-2064.
41. Erenpreiss, J., Jepson, K., Giwercman, A., Tsarev, I., Erenpreisa, J. and Spano, M. (2004) Toluidine blue cytometry test for sperm DNA conformation: comparison with the flow cytometric sperm chromatin structure and TUNEL assays. Hum Reprod 19:2277-2282.
42. ESHRE Andrology Special Interest Group. (1996) Andrology: Consensus workshop on advanced diagnostic andrology techniques. Hum Reprod 11(7):1463-1479.
43. Esterhuizen, A. D., Franken, D. R., Lourens, J. G., Prinsloo, E. and van Rooyen, L. H. (2000) Sperm chromatin packaging as an indicator of in-vitro fertilization rates. Hum Reprod 15:657-661.
44. Evenson, D. (1980) Relation of mamalian sperm chromatin heterogeneity to fertility. Science 210:1131-1133.
45. Evenson, D. and Jost, L. (2000) Sperm chromatin structure assay is useful for fertility assessment. Methods Cell Sci 22:169-189.
46. Evenson, D. and Kasperson, K. and Wixon, R. (2007) Analysis of sperm DNA fragmentation using flow cytometry and other techniques. Nottingham University Press.
47. Evenson, D. P., Jost, L. K., Marshall, D., Zinaman, M. J., Clegg, E., Purvis, K., de Angelis, P. and Claussen, O. P. (1999) Utility of the sperm chromatin structure assay as a diagnostic and prognostic tool in the human fertility clinic. Hum Reprod 14:1039-1049.
48. Evenson, D. P., Larson, K. L. and 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 23:25-43.
49. Fraga, C. G., Motchnik, P. A., Shigenaga, M. K., Helbock, H. J., Jacob, R. A. and Ames, B. N. (1991) Ascorbic acid protects against endogenous oxidative DNA damage in human sperm. Proc Natl Acad Sci USA 88:11003-11006.
50. Fraga, C. G., Motchnik, P. A., Wyrobek, A. J., Rempel, D. M. and Ames, B. N. (1996) Smoking and low antioxidant levels increase oxidative damage to sperm DNA. Mutat Res 351:199-203.
51. Gandini, L., Lombardo, F., Paoli, D., Caruso, F., Eleuteri, P., Leter, G., Ciriminna, R., Culasso, F., Dondero, F., Lenzi, A., et al. (2004) Full-term pregnancies achieved with ICSI despite high levels of sperm chromatin damage. Hum Reprod 19:1409-1417.
52. Genesca, A., Caballin, M. R., Miro, R., Benet, J., Germa, J. R. and Egozcue, J. (1992) Repair of human sperm chromosome aberrations in the hamster egg. Hum Genet 89:181-186.
53. Gorczyca, W., Gong, J. and Darzynkiewicz, Z. (1993) Detection of DNA strand breaks in individual apoptotic cells by the in situ terminal deoxynucleotidyl transferase and nick translation assays. Cancer Res 53:1945-1951.
54. Greco, E., Romano, S., Iacobelli, M., Ferrero, S., Baroni, E., Minasi, M. G., Ubaldi, F., Rienzi, L. and Tesarik, J. (2005a) ICSI in cases of sperm DNA damage: beneficial effect of oral antioxidant treatment. Hum Reprod 20:2590-2594.
55. Greco, E., Scarselli, F., Iacobelli, M., Rienzi, L., Ubaldi, F., Ferrero, S., Franco, G., Anniballo, N., Mendoza, C. and Tesarik, J. (2005b) Efficient treatment of infertility due to sperm DNA damage by ICSI with testicular spermatozoa. Hum Reprod 20:226-230.
56. Guzick, D. S., Overstreet, J. W., Factor-Litvak, P., Brazil, C. K., Nakajima, S. T., Coutifaris, C., Carson, S. A., Cisneros, P., Steinkampf, M. P., Hill, J. A., et al. (2001) Sperm morphology, motility, and concentration in fertile and infertile men. N Engl J Med 345: 1388-1393.
57. Hales, B. F. and Robaire, B. (2001) Paternal exposure to drugs and environmental chemicals: effects on progeny outcome. J Androl 22:927-936.
58. Halliwell, B. (2000) Why and how should we measure oxidative DNA damage in nutritional studies? How far have we come? Am J Clin Nutr 72:1082-1087.
59. Hammadeh, M. E., Stieber, M., Haidl, G. and Schmidt, W. (1998) Association between sperm cell chromatin condensation, morphology based on strict criteria, and fertilization, cleavage and pregnancy rates in an IVF program. Andrologia 30:29-35.
60. Hansen, M., Bower, C., Milne, E., de Klerk, N. and Kurinczuk, J. J. (2005) Assisted reproductive technologies and the risk of birth defects-a systematic review. Hum Reprod 20:328-338.
61. Harari, O., Bourne, H., McDonald, M., Richings, N., Speirs, A. L., Johnston, W. I. and Baker, H. W. (1995) Intracytoplasmic sperm injection: a major advance in the management of severe male subfertility. Fertil Steril 64:360-368.
62. Hazout, A., Dumont-Hassan, M., Junca, A. M., Cohen Bacrie, P. and Tesarik, J. (2006) High-magnification ICSI overcomes paternal effect resistant to conventional ICSI. Reprod Biomed Online 12: 19-25.
63. Henkel, R., Hajimohammad, M., Stalf, T., Hoogendijk, C., Mehnert, C., Menkveld, R., Gips, H., Schill, W. B. and Kruger, T. F. (2004) Influence of deoxyribonucleic acid damage on fertilization and pregnancy. Fertil Steril 81:965-972.
64. Henkel, R., Kierspel, E., Hajimohammad, M., Stalf, T., Hoogendijk, C., Mehnert, C., Menkveld, R., Schill, W. B. and Kruger, T. F. (2003) DNA fragmentation of spermatozoa and assisted reproduction technology. Reprod Biomed Online 7:477-484.
65. Hewitson, L., Dominko, T., Takahashi, D., Martinovich, C., Ramalho- Santos, J., Sutovsky, P., Fanton, J., Jacob, D., Monteith, D., Neuringer, M., et al. (1999) Unique checkpoints during the first cell cycle of fertilization after intracytoplasmic sperm injection in rhesus monkeys. Nat Med 5:431-433.
66. Holt, W. V. (2005) Is quality assurance in semen analysis still really necessary? A spermatologist's viewpoint. Hum Reprod 20: 2983-2986.
67. Host, E., Lindenberg, S. and Smidt-Jensen, S. (2000) The role of DNA strand breaks in human spermatozoa used for IVF and ICSI. Acta Obstet Gynecol Scand 79:559-563.
68. Huang, C. C., Lin, D. P., Tsao, H. M., Cheng, T. C., Liu, C. H. and Lee, M. S. (2005) Sperm DNA fragmentation negatively correlates with velocity and fertilization rates but might not affect pregnancy rates. Fertil Steril 84:130-140.
69. Irvine, D. S., Twigg, J. P., Gordon, E. L., Fulton, N., Milne, P. A. and Aitken, R. J. (2000) DNA integrity in human spermatozoa: relationships with semen quality. J Androl 21:33-44.
70. Jequier, A. M. (2005) Is quality assurance in semen analysis still really necessary? A clinician's viewpoint. Hum Reprod 20:2039-2042.
71. Ji, B. T., Shu, X. O., Linet, M. S., Zheng, W., Wacholder, S., Gao, Y. T., Ying, D. M. and Jin, F. (1997) Paternal cigarette smoking and the risk of childhood cancer among offspring of nonsmoking mothers. J Natl Cancer Inst 89:238-244.
72. Kodama, H., Yamaguchi, R., Fukuda, J., Kasai, H. and Tanaka, T. (1997) Increased oxidative deoxyribonucleic acid damage in the spermatozoa of infertile male patients. Fertil Steril 68:519-524.
73. Lewis, S. (2007) Is sperm evaluation useful in predicting human fertility? Reproduction 134:1-11.
74. Lewis, S. E. and Aitken, R. J. (2005) DNA damage to spermatozoa has impacts on fertilization and pregnancy. Cell Tissue Res 322:33-41.
75. Lewis, S. E., Boyle, P. M., McKinney, K. A., Young, I. S. and Thompson,W. (1995) Total antioxidant capacity of seminal plasma is different in fertile and infertile men. Fertil Steril 64:868-870.
76. Lewis, S. E., O'Connell, M., Stevenson, M., Thompson-Cree, L. and McClure, N. (2004) An algorithm to predict pregnancy in assisted reproduction. Hum Reprod 19:1385-1394.
77. Loft, S., Kold-Jensen, T., Hjollund, N. H., Giwercman, A., Gyllemborg, J., Ernst, E., Olsen, J., Scheike, T., Poulsen, H. E. and Bonde, J. P. (2003) Oxidative DNA damage in human sperm influences time to pregnancy. Hum Reprod 18:1265-1272.
78. Lopes, S., Sun, J. G., Jurisicova, A., Meriano, J. and Casper, R. F. (1998) Sperm deoxyribonucleic acid fragmentation is increased in poor quality semen samples and correlates with failed fertilization in intracytoplasmic sperm injection. Fertil Steril 69:528-532.
79. Lysiak, J. J., Zheng, S., Woodson, R. and Turner, T. T. (2007) Caspase-9- dependent pathway to murine germ cell apoptosis: mediation by oxidative stress, BAX, and caspase 2. Cell Tissue Res 328:411-419.
80. Makhlouf, A. A. and Niederberger, C. (2006) DNA integrity tests in clinical practice: it is not a simple matter of black and white (or red and green). J Androl 27:316-323.
81. Matsuda, Y., Tobari, I., Maemori, M. and Seki, N. (1989) Mechanism of chromosome aberration induction in the mouse egg fertilized with sperm recovered from postmeiotic germ cells treated with methyl methanesulfonate. Mutat Res 214:165-180.
82. McVicar, C. M., McClure, N.,Williamson, K., Dalzell, L. H. and Lewis, S. E. (2004) Incidence of Fas positivity and deoxyribonucleic acid doublestranded breaks in human ejaculated sperm. Fertil Steril 81(Suppl 1): 767-774.
83. Moore, H. (1996) The influence of the epididymis on human and animal sperm maturation and storage. Hum Reprod 11(Suppl):103-110.
84. Morris, I. D., Ilott, S., Dixon, L. and Brison, D. R. (2002) The spectrum of DNA damage in human sperm assessed by single cell gel electrophoresis (Comet assay) and its relationship to fertilization and embryo development. Hum Reprod 17:990-998.
85. O'Connell, M., McClure, N. and Lewis, S. E. (2002) Mitochondrial DNA deletions and nuclear DNA fragmentation in testicular and epididymal human sperm. Hum Reprod 17:1565-1570.
86. Ollero, M., Gil-Guzman, E., Lopez, M. C., Sharma, R. K., Agarwal, A., Larson, K., Evenson, D., Thomas, A. J., Jr. and Alvarez, J. G. (2001) Characterization of subsets of human spermatozoa at different stages of maturation: implications in the diagnosis and treatment of male infertility. Hum Reprod 16:1912-1921.
87. Olshan, A. and Mattison, D. (1994) Male mediated developmental toxicity, New York: Plenum Press.
88. Ozmen, B., Koutlaki, N., Youssry, M., Diedrich, K. and Al-Hasani, S. (2007) DNA damage of human spermatozoa in assisted reproduction: origins, diagnosis, impacts and safety. Reprod Biomed Online 14: 384-395.
89. Payne, J. F., Raburn, D. J., Couchman, G. M., Price, T. M., Jamison, M. G. and Walmer, D. K. (2005) Redefining the relationship between sperm deoxyribonucleic acid fragmentation as measured by the sperm chromatin structure assay and outcomes of assisted reproductive techniques. Fertil Steril 84:356-364.
90. Perera, D., Pizzey, A., Campbell, A., Katz, M., Porter, J., Petrou, M., Irvine, D. S. and Chatterjee, R. (2002) Sperm DNA damage in potentially fertile homozygous beta-thalassaemia patients with iron overload. Hum Reprod 17:1820-1825.
91. Perreault, S. D., Aitken, R. J., Baker, H. W., Evenson, D. P., Huszar, G., Irvine, D. S.,Morris, I. D., Morris, R. A., Robbins, W. A., Sakkas, D., et al. (2003) Integrating new tests of sperm genetic integrity into semen analysis: breakout group discussion. Adv Exp Med Biol 518:253-268
92. Philipp, T. and Kalousek, D. K. (2002) Generalized abnormal embryonic development in missed abortion: embryoscopic and cytogenetic findings. Am J Med Genet 111:43-47.
93. Platts, A. E., Dix, D. J., Chemes, H. E., Thompson, K. E., Goodrich, R., Rockett, J. C., Rawe, V. Y., Quintana, S., Diamond, M. P., Strader, L. F. and Krawetz, S. A. (2007) Success and failure in human spermatogenesis as revealed by teratozoospermic RNAs. Hum Mol Genet 16:763-773.
94. Ponjaert-Kristoffersen, I., Tjus, T., Nekkebroek, J., et al. (2004) Psychological follow-up study of 5-year-old ICSI children. Hum Reprod 19:2791-2797.
95. Rimm, A. A., Katayama, A. C., Diaz, M. and Katayama, K. P. (2004) A meta-analysis of controlled studies comparing major malformation rates in IVF and ICSI infants with naturally conceived children. J Assist Reprod Genet 21:437-443.
96. Sakkas, D., Mariethoz, E. and St John, J. C. (1999) Abnormal sperm parameters in humans are indicative of an abortive apoptotic mechanism linked to the Fas-mediated pathway. Exp Cell Res 251:350-355.
97. Sakkas, D., Urner, F., Bizzaro, D., Manicardi, G., Bianchi, P. G., Shoukir, Y. and Campana, A. (1998) Sperm nuclear DNA damage and altered chromatin structure: effect on fertilization and embryo development. Hum Reprod 13(Suppl 4):11-19.
98. Saleh, R. A., Agarwal, A., Nada, E. A., El-Tonsy, M. H., Sharma, R. K., Meyer, A., Nelson, D. R. and Thomas, A. J. (2003) Negative effects of increased sperm DNA damage in relation to seminal oxidative stress in men with idiopathic and male factor infertility. Fertil Steril 79(Suppl 3):1597-1605.
99. Sergerie, M., Laforest, G., Bujan, L., Bissonnette, F. and Bleau, G. (2005) Sperm DNA fragmentation: threshold value in male fertility. Hum Reprod 20:3446-3451.
100. Shaman, J. A., Yamauchi, Y. and Ward, W. S. (2007) Sperm DNA fragmentation: awakening the sleeping genome. Biochem Soc Trans 35:626-628.
101. Shen, H. and Ong, C. (2000) Detection of oxidative DNA damage in human sperm and its association with sperm function and male infertility. Free Radic Biol Med 28:529-536.
102. Shen, H. M., Chia, S. E. and Ong, C. N. (1999) Evaluation of oxidative DNA damage in human sperm and its association with male infertility. J Androl 20:718-723.
103. Shi, W. and Haaf, T. (2002) Aberrant methylation patterns at the two-cell stage as an indicator of early developmental failure. Mol Reprod Dev 63:329-334.
104. Singh, N. P., Muller, C. H. and Berger, R. E. (2003) Effects of age on DNA double-strand breaks and apoptosis in human sperm. Fertil Steril 80:1420-1430.
105. Smith, C. J., Perfetti, T. A., Mullens, M. A., Rodgman, A. and Doolittle, D. J. (2000) ''IARC group 2B Carcinogens'' reported in cigarette mainstream smoke. Food Chem Toxicol 38:825-848.
106. Sorahan, T., Prior, P., Lancashire, R. J., Faux, S. P., Hulten, M. A., Peck, I. M. and Stewart, A. M. (1997) Childhood cancer and parental use of tobacco: deaths from 1971 to 1976. Br J Cancer 76:1525-1531.
107. Spano, M., Bonde, J. P., Hjollund, H. I., Kolstad, H. A., Cordelli, E. and Leter, G. (2000) Sperm chromatin damage impairs human fertility. The Danish First Pregnancy Planner Study Team. Fertil Steril 73:43-50.
108. Steele, E. K., McClure, N., Maxwell, R. J. and Lewis, S. E. (1999) A comparison of DNA damage in testicular and proximal epididymal spermatozoa in obstructive azoospermia. Mol Hum Reprod 5: 831-835.
109. Suganuma, R., Yanagimachi, R. and Meistrich, M. L. (2005) Decline in fertility of mouse sperm with abnormal chromatin during epididymal passage as revealed by ICSI. Hum Reprod 20:3101-3108.
110. Sun, J. G., Jurisicova, A. and Casper, R. F. (1997) Detection of deoxyribonucleic acid fragmentation in human sperm: correlation with fertilization in vitro. Biol Reprod 56:602-607.
111. Tarlatzis, B. C. and Bili, H. (1998) Survey on intracytoplasmic sperm injection: report from the ESHRE ICSI Task Force. European Society of Human Reproduction and Embryology. Hum Reprod 13(Suppl 1):165-177.
112. Tesarik, J., Greco, E. and Mendoza, C. (2004) Late, but not early, paternal effect on human embryo development is related to sperm DNA fragmentation. Hum Reprod 19:611-615.
113. Tesarik, J., Mendoza-Tesarik, R. and Mendoza, C. (2006) Sperm nuclear DNA damage: update on the mechanism, diagnosis and treatment. Reprod Biomed Online 12:715-721.
114. Trasler, J. M. and Doerksen, T. (1999) Teratogen update: paternal exposures-reproductive risks. Teratology 60:161-172.
115. Trasler, J. M., Hales, B. F. and Robaire, B. (1986) Chronic low dose cyclophosphamide treatment of adult male rats: effect on fertility, pregnancy outcome and progeny. Biol Reprod 34:275-283.
116. Twigg, J. P., Irvine, D. S. and Aitken, R. J. (1998) Oxidative damage to DNA in human spermatozoa does not preclude pronucleus formation at intracytoplasmic sperm injection. Hum Reprod 13:1864-1871.
117. Van den Bergh, M., Hohl, M. K., De Geyter, C., Stalberg, A. M. and Limoni, C. (2005) Ten years of Swiss National IVF Register FIVNAT-CH. Are we making progress? Reprod Biomed Online 11:632-640.
118. Van Loon, A. A., Den Boer, P. J., Van der Schans, G. P., Mackenbach, P., Grootegoed, J. A., Baan, R. A. and Lohman, P. H. (1991) Immunochemical detection of DNA damage induction and repair at different cellular stages of spermatogenesis of the hamster after in vitro or in vivo exposure to ionizing radiation. Exp Cell Res 193:303-309.
119. Van Steirteghem, A. C., Liu, J., Joris, H., Nagy, Z., Janssenswillen, C., Tournaye, H., Derde, M. P., Van Assche, E. and Devroey, P. (1993) Higher success rate by intracytoplasmic sperm injection than by subzonal insemination. Report of a second series of 300 consecutive treatment cycles. Hum Reprod 8:1055-1060.
120. Virro, M. R., Larson-Cook, K. L. and Evenson, D. P. (2004) Sperm chromatin structure assay (SCSA) parameters are related to fertilization, blastocyst development, and ongoing pregnancy in in vitro fertilization and intracytoplasmic sperm injection cycles. Fertil Steril 81:1289-1295.
121. Vogel, F. and Rathenberg, R. (1975) Spontaneous mutation in man. Adv Hum Genet 5:223-318.
122. Wennerholm, U. B., Bergh, C., Hamberger, L., Lundin, K., Nilsson, L., Wikland, M. and Kallen, B. (2000) Incidence of congenital malformations in children born after ICSI. Hum Reprod 15:944-948.
123. World Health Organization (WHO) (1987) WHO Laboratory Manual for the examination of human semen and sperm-cervical mucus interaction. 2nd ed. Cambridge, UK: Cambridge Univeristy Press.
124. WHO (2006) WHO laboratory manual for the examination of human semen and sperm-cervical mucus interaction, Cambridge University Press.
125. Xu, D. X., Shen, H. M., Zhu, Q. X., Chua, L., Wang, Q. N., Chia, S. E. and Ong, C. N. (2003) The associations among semen quality, oxidative DNA damage in human spermatozoa and concentrations of cadmium, lead and selenium in seminal plasma. Mutat Res 534:155-163.
126. Yamauchi, Y., Shaman, J. A., Boaz, S. M. and Ward, W. S. (2007a) Paternal pronuclear DNA degradation is functionally linked to DNA replication in mouse oocytes. Biol Reprod 77:407-415.
127. Yamauchi, Y., Shaman, J. A. and Ward, W. S. (2007b) Topoisomerase II-mediated breaks in spermatozoa cause the specific degradation of paternal DNA in fertilized oocytes. Biol Reprod 76: 666-672.
128. Zini A., Bielecki, R., Phang, D. and Zenzes,M. T. (2001) Correlations between two markers of sperm DNA integrity, DNA denaturation and DNA fragmentation, in fertile and infertile men. Fertil Steril 75: 674-677.
129. Zini, A., Meriano, J., Kader, K., Jarvi, K., Laskin, C. A. and Cadesky, K. (2005) Potential adverse effect of sperm DNA damage on embryo quality after ICSI. Hum Reprod 20:3476-3480.