Factors from damaged sperm affect its DNA integrity and its ability to promote embryo implantation in mice

Journal of Andrology

Volumn 29, Issue 1, 2008, Pages 47-54

  Perez Crespo M ^a   Moreira, P ^a   Pintado, B ^a   Gutiérrez Adán, Alfonso ^a  

^a INIA   (Spain)

Author keywords

DNA integrity; Embryo quality; ICSI; Sperm endonucleases

Indexed keywords

ENDONUCLEASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLASTOCYST; CELL STRUCTURE; CONTROLLED STUDY; CRYOPROTECTION; DNA INTEGRATION; EMBRYO DEVELOPMENT; FEMALE; INTRACYTOPLASMIC SPERM INJECTION; MALE; MOUSE; NICK END LABELING; NIDATION; NONHUMAN; PRIORITY JOURNAL; SEMEN ABNORMALITY; SPERMATOZOON;

ANIMALS; CELL MEMBRANE; CRYOPRESERVATION; CULTURE MEDIA, CONDITIONED; DNA DAMAGE; EMBRYO IMPLANTATION; EPIDIDYMIS; FEMALE; MALE; MICE; MICE, INBRED STRAINS; PREGNANCY; PREGNANCY OUTCOME; SPERM INJECTIONS, INTRACYTOPLASMIC; SPERMATOZOA;

EID: 38049129379     PISSN: 01963635     EISSN: None     Source Type: Journal    
DOI: 10.2164/jandrol.107.003194     Document Type: Article

References (64)

1. Ahmadi A, Ng SC. Developmental capacity of damaged spermatozoa. Hum Reprod. 1999a;14:2279-2285.
2. Ahmadi A, Ng SC. Fertilizing ability of DNA-damaged spermatozoa. J Exp Zool. 1999b;284:696-704.
3. Aitken RJ. Founders' Lecture. Human spermatozoa: fruits of creation, seeds of doubt. Reprod Fertil Dev. 2004;16:655-664.
4. Aitken RJ, Baker MA. Oxidative stress, sperm survival and fertility control. Mol Cell Endocrinol. 2006;250:66-69.
5. Aitken RJ, Baker MA, 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;7:65-70.
6. Arnon J, Meirow D, Lewis-Roness H, Ornoy A. Genetic and teratogenic effects of cancer treatments on gametes and embryos. Hum Reprod Update. 2001;7:394-403.
7. Arny M, Nachtigall L, Quagliarello J. The effect of preimplantation culture conditions on murine embryo implantation and fetal development. Fertil Steril. 1987;48:861-865.
8. Baker MA, Aitken RJ. Reactive oxygen species in spermatozoa: methods for monitoring and significance for the origins of genetic disease and infertility. Reprod Biol Endocrinol. 2005;3:67.
9. Borini A, Tarozzi N, Bizzaro D, Bonu MA, Fava L, Flamigni C, Coticchio G. Sperm DNA fragmentation: paternal effect on early post-implantation embryo development in ART. Hum Reprod. 2006;21:2876-2881.
10. Braude P, Bolton V, Moore S. Human gene expression first occurs between the four- and eight-cell stages of preimplantation development. Nature. 1988;332:459-461.
11. Bungum M, Humaidan P, Spano M, Jepson K, Bungum L, Giwercman A. The predictive value of sperm chromatin structure assay (SCSA) parameters for the outcome of intrauterine insemination, IVF and ICSI. Hum Reprod. 2004;19:1401-1408.
12. Carrell DT, Liu L, Peterson CM, Jones KP, Hatasaka HH, Erickson L, Campbell B. Sperm DNA fragmentation is increased in couples with unexplained recurrent pregnancy loss. Arch Androl. 2003a;49: 49-55.
13. Carrell DT, Wilcox AL, Lowy L, Peterson CM, Jones KP, Erickson L, Campbell B, Branch DW, Hatasaka HH. Elevated sperm chromosome aneuploidy and apoptosis in patients with unexplained recurrent pregnancy loss. Obstet Gynecol. 2003b;101: 1229-1235.
14. Chan PJ, Corselli JU, Patton WC, Jacobson JD, Chan SR, King A. A simple comet assay for archived sperm correlates DNA fragmentation to reduced hyperactivation and penetration of zona-free hamster oocytes. Fertil Steril. 2001;75:186-192.
15. Estop AM, Munne S, Jost LK, Evenson DP. Studies on sperm chromatin structure alterations and cytogenetic damage of mouse sperm following in vitro incubation. Studies on in vitro-incubated mouse sperm. J Androl. 1993;14:282-288.
16. Fatehi AN, Bevers MM, Schoevers E, Roelen BA, Colenbrander B, Gadella BM. DNA damage in bovine sperm does not block fertilization and early embryonic development but induces apoptosis after the first cleavages. J Androl. 2006;27:176-188.
17. Fernández-Gonzalez R, Moreira P, Bilbao A, Jiménez A, Pérez-Crespo M, Ramirez MA, Rodriguez De Fonseca F, Pintado B, Gutiérrez-Adán A. Long-term effect of in vitro culture of mouse embryos with serum on mRNA expression of imprinting genes, development, and behavior. Proc Natl Acad Sci U S A. 2004;101: 5880-5885.
18. Filatov MV, Semenova EV, Vorob'eva OA, Leont'eva OA, Drobchenko EA. Relationship between abnormal sperm chromatin packing and IVF results. Mol Hum Reprod. 1999;5:825-830.
19. Garner DL, Johnson LA. Viability assessment of mammalian sperm using SYBR-14 and propidium iodide. Biol Reprod. 1995;53: 276-284.
20. Genesca A, Caballin MR, Miro R, Benet J, Germa JR, Egozcue J. Repair of human sperm chromosome aberrations in the hamster egg. Hum Genet. 1992;89:181-186.
21. Gutiérrez-Adán A, Granados J, Pintado B, De La Fuente J. Influence of glucose on the sex ratio of bovine IVM/IVF embryos cultured in vitro. Reprod Fertil Dev. 2001;13:361-365.
22. Hales BF, Aguilar-Mahecha A, Robaire B. The stress response in gametes and embryos after paternal chemical exposures. Toxical Appl Pharmacol. 2005;207:514-520.
23. Irvine DS, Twigg JP, Gordon EL, Fulton N, Milne PA, Aitken RJ. DNA integrity in human spermatozoa: relationships with semen quality. J Androl. 2000;21:33-44.
24. Ji BT, Shu XO, Linet MS, Zheng W, Wacholder S, Gao YT, Ying DM, Jin F. Paternal cigarette smoking and the risk of childhood cancer among offspring of nonsmoking mothers. J Natl Cancer Inst. 1997;89:238-244.
25. Khosla S, Dean W, Brown D, Reik W, Feil R. Culture of preimplantation mouse embryos affects fetal development and the expression of imprinted genes. Biol Reprod. 2001a;64:918-926.
26. Khosla S, Dean W, Reik W, Feil R. Culture of preimplantation embryos and its long-term effects on gene expression and phenotype. Hum Reprod Update. 2001b;7:419-427.
27. Kodama H, Yamaguchi R, Fukuda J, Kasai H, Tanaka T. Increased oxidative deoxyribonucleic acid damage in the spermatozoa of infertile male patients. Fertil Steril. 1997;68:519-524.
28. Kuretake S, Kimura Y, Hoshi K, Yanagimachi R. Fertilization and development of mouse oocytes injected with isolated sperm heads. Biol Reprod. 1996;55:789-795.
29. Madrid-Bury N, Pérez-Gutiérrez JF, Pérez-Garnelo S, Moreira P, Pintado Sanjuanbenito B, Gutiérrez-Adán A, de la Fuente Martinez J. Relationship between non-return rate and chromatin condensation of deep frozen bull spermatozoa. Theriogenology. 2005;64:232-241.
30. Maione B, Pittoggi C, Achene L, Lorenzini R, Spadafora C. Activation of endogenous nucleases in mature sperm cells upon interaction with exogenous DNA. DNA Cell Biol. 1997;16: 1087-1097.
31. Marchetti F, Wyrobek AJ. Mechanisms and consequences of paternally-transmitted chromosomal abnormalities. Birth Defects Res C Embryo Today. 2005;75:112-129.
32. Matsuda Y, Tobari I. Repair capacity of fertilized mouse eggs for x-ray damage induced in sperm and mature oocytes. Mutat Res. 1989;210:35-47.
33. McVicar CM, McClure N, Williamson K, Dalzell LH, Lewis SE. Incidence of Fas positivity and deoxyribonucleic acid double-stranded breaks in human ejaculated sperm. Fertil Steril. 2004;81(suppl 1):767-774.
34. Menezo YJ. Paternal and maternal factors in preimplantation embryogenesis: interaction with the biochemical environment. Reprod Biomed Online. 2006;12:616-621.
35. Moreira PN, Giraldo P, Cozar P, Pozueta J, Jiménez A, Montoliu L, Gutiérrez-Adán A. Efficient generation of transgenic mice with intact yeast artificial chromosomes by intracytoplasmic sperm injection. Biol Reprod. 2004;71:1943-1947.
36. Moreira PN, Pérez-Crespo M, Ramirez MA, Pozueta J, Montoliu L, Gutiérrez-Adán A. Effect of transgene concentration, flanking matrix attachment regions, and RecA-coating on the efficiency of mouse transgenesis mediated by intracytoplasmic sperm injection. Biol Reprod. 2007;76:336-343.
37. Morris ID. Sperm DNA damage and cancer treatment. Int J Androl. 2002;5:255-261.
38. Moskovtsev SI, Willis J, Azad A, Mullen JB. Sperm DNA integrity: correlation with sperm plasma membrane integrity in semen evaluated for male infertility. Arch Androl. 2005;51:33-40.
39. Muratori M, Maggi M, Spinelli S, Filimberti E, Forti G, Baldi E. Spontaneous DNA fragmentation in swim-up selected human spermatozoa during long term incubation. J Androl. 2003;24: 253-262.
40. Pérez-Crespo M, Pericuesta E, Rey R, Gutiérrez-Adán A. OC6 Scrotal heat stress in mice affects viability and DNA integrity of sperm, and sex ratio of the offspring. Reprod Domest Anim. 2006; 41(suppl 2):104.
41. Pérez-Crespo M, Ramirez MA, Fernández-González R, Rizos D, Lonergan P, Pintado B, Gutiérrez-Adán A. Differential sensitivity of male and female mouse embryos to oxidative induced heat-stress is mediated by glucose-6-phosphate dehydrogenase gene expression. Mol Reprod Dev. 2005;72:502-510.
42. Sakkas D. The use of blastocyst culture to avoid inheritance of an abnormal paternal genome after ICSI. Hum Reprod. 1999;14:4-5.
43. Sakkas D, Urner F, Bizzaro D, Manicardi G, Bianchi PG, Shoukir Y, Campana A. Sperm nuclear DNA damage and altered chromatin structure: effect on fertilization and embryo development. Hum Reprod. 1998;13(suppl 4):11-19.
44. Saleh RA, Agarwal A, Nada EA, El-Tonsy MH, Sharma RK, Meyer A, Nelson DR, Thomas AJ. Negative effects of increased sperm DNA damage in relation to seminal oxidative stress in men with idiopathic and male factor infertility. Fertil Steril. 2003; 79(suppl 3):1597-1605.
45. Seli E, Gardner DK, Schoolcraft WB, Moffatt O, Sakkas D. Extent of nuclear DNA damage in ejaculated spermatozoa impacts on blastocyst development after in vitro fertilization. Fertil Steril. 2004;82:378-383.
46. Sergerie M, Laforest G, Bujan L, Bissonnette F, Bleau G. Sperm DNA fragmentation: threshold value in male fertility. Hum Reprod. 2005;20:3446-3451.
47. Shaman JA, Prisztoka R, Ward WS. Topoisomerase IIB and an extracellular nuclease interact to digest sperm DNA in an apoptotic-like manner. Biol Reprod. 2006;75:741-748.
48. Shimura T, Inoue M, Taga M, Shiraishi K, Uematsu N, Takei N, Yuan ZM, Shinohara T, Niwa O. p53-dependent S-phase damage checkpoint and pronuclear cross talk in mouse zygotes with X-irradiated sperm. Mol Cell Biol. 2002a;22:2220-2228.
49. Shimura T, Toyoshima M, Taga M, Shiraishi K, Uematsu N, Inoue M, Niwa O. The novel surveillance mechanism of the Trp53-dependent S-phase checkpoint ensures chromosome damage repair and preimplantation-stage development of mouse embryos fertilized with x-irradiated sperm. Radiat Res. 2002b;158:735-742.
50. Sotolongo B, Huang TT, Isenberger E, Ward WS. An endogenous nuclease in hamster, mouse, and human spermatozoa cleaves DNA into loop-sized fragments. J Androl. 2005;26:272-280.
51. 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.
52. Szczygiel MA, Ward WS. Combination of dithiothreitol and detergent treatment of spermatozoa causes paternal chromosomal damage. Biol Reprod. 2002;67:1532-1537.
53. Tateno H, Kimura Y, Yanagimachi R. Sonication per se is not as deleterious to sperm chromosomes as previously inferred. Biol Reprod. 2000;63:341-346.
54. Tesarik J, Greco E, Mendoza C. Late, but not early, paternal effect on human embryo development is related to sperm DNA fragmentation. Hum Reprod. 2004;19:611-615.
55. Tesarik J, Mendoza C, Greco E. Paternal effects acting during the first cell cycle of human preimplantation development after ICSI. Hum Reprod. 2002;17:184-189.
56. Tomlinson MJ, Moffatt O, Manicardi GC, Bizzaro D, Afnan M, Sakkas D. Interrelationships between seminal parameters and sperm nuclear DNA damage before and after density gradient centrifugation: implications for assisted conception. Hum Reprod. 2001;16:2160-2165.
57. Van der Auwera I, Pijnenborg R, Koninckx PR. The influence of in-vitro culture versus stimulated and untreated oviductal environment on mouse embryo development and implantation. Hum Reprod. 1999;14:2570-2574.
58. Virro MR, Larson-Cook KL, Evenson DP. 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. 2004;81:1289-1295.
59. Ward MA, Ward WS. A model for the function of sperm DNA degradation. Reprod Fertil Dev. 2004;16:547-554.
60. Yamauchi Y, Shaman JA, Ward WS. Topoisomerase II-mediated breaks in spermatozoa cause the specific degradation of paternal DNA in fertilized oocytes. Biol Reprod. 2007;76:666-672.
61. Zenzes MT. Smoking and reproduction: gene damage to human gametes and embryos. Hum Reprod Update. 2000;6:122-131.
62. Zheng P, Schramm RD, Latham KE. Developmental regulation and in vitro culture effects on expression of DNA repair and cell cycle checkpoint control genes in rhesus monkey oocytes and embryos. Biol Reprod. 2005;72:1359-1369.
63. Zhu BK, Setchell BP. Effects of paternal heat stress on the in vivo development of preimplantation embryos in the mouse. Reprod Nutr Dev. 2004;44:617-629.
64. Zini A, Meriano J, Kader K, Jarvi K, Laskin CA, Cadesky K. Potential adverse effect of sperm DNA damage on embryo quality after ICSI. Hum Reprod. 2005;20:3476-3480.