Spermiogenic Germ Cell Phase-Specific DNA Damage Following Cyclophosphamide Exposure

Journal of Andrology

Volumn 25, Issue 3, 2004, Pages 354-362

  Coddington, Alexis M ^a   Hales, Barbara F ^a   Robaire, Bernard ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

Chromatin remodeling; Comet assay; Sperm; Susceptibility; Toxicology

Indexed keywords

CAS 6055 19 2; CYCLOPHOSPHAMIDE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; COMET ASSAY; CONTROLLED STUDY; DNA DAMAGE; DNA STRAND BREAKAGE; DOSE RESPONSE; DRUG MEGADOSE; EPIDIDYMIS TAIL; GENETIC SUSCEPTIBILITY; GERM CELL; LOW DRUG DOSE; MALE; NONHUMAN; PRIORITY JOURNAL; SPERMATID; SPERMATOGENESIS; SPERMATOZOON;

EID: 1942469899     PISSN: 01963635     EISSN: None     Source Type: Journal    
DOI: 10.1002/j.1939-4640.2004.tb02800.x     Document Type: Article

References (67)

1. Aguilar-Mahecha A, Hales BF, Robaire B. Acute cyclophosphamide exposure has germ cell specific effects on the expression of stress response genes during rat spermatogenesis. Mol Reprod Dev. 2001;60:302-311.
2. Ahmadi A, Ng SC. Fertilizing ability of DNA-damaged spermatozoa. J Exp Zool. 1999;284:696-704.
3. Anderson D, Dhawan A, Yu TW, Plewa MJ. An investigation of bone marrow and testicular cells in vivo using the comet assay. Mutat Res. 1996;370:159-174.
4. Angelis KJ, Dusinska M, Collins AR. Single cell gel electrophoresis: detection of DNA damage at different levels of sensitivity. Electrophoresis. 1999;20:2133-2138.
5. Balhom R. A model for the structure of chromatin in mammalian sperm. J Cell Biol. 1982;93:298-305.
6. Bishop JB, Witt KL, Sloane RA. Genetic toxicities of human teratogens. Mutat Res. 1997;396:9-43.
7. Brinkworth MH. Paternal transmission of genetic damage: findings in animals and humans. Int J Androl. 2000;23:123-135.
8. Brinkworth MH, Nieschlag E. Association of cyclophosphamide-induced male-mediated, foetal abnormalities with reduced paternal germ-cell apoptosis. Mutat Res. 2000;447:149-154.
9. Cai L, Hales BF, Robaire B. Induction of apoptosis in the germ cells of adult male rats after exposure to cyclophosphamide. Biol Reprod. 1997;56:1490-1497.
10. Caron N, Veilleux S, Boissonneault G. Stimulation of DNA repair by the spermatidal TP1 protein. Mol Reprod Dev. 2001;58:437-443.
11. Chatterjee R, Haines GA, Perera DM, Goldstone A, Morris ID. Testicular and sperm DNA damage after treatment with fludarabine for chronic lymphocytic leukaemia. Hum Reprod. 2000;15:762-766.
12. Clermont Y. Kinetics of spermatogenesis in mammals: seminiferous epithelium cycle and spermatogonial renewal. Physiol Rev. 1972;52:198-236.
13. Ehling UH. Induction of gene mutations in germ cells of the mouse. Arch Toxicol. 1980;46:123-138.
14. Ehling UH, Cumming RB, Malling HV. Induction of dominant lethal mutations by alkylating agents in male mice. Mutat Res. 1968;5:417-428.
15. Generoso WM, Cain KT, Krishna M, Sheu CW, Gryder RM. Heritable translocation and dominant-lethal mutation induction with ethylene oxide in mice. Mutat Res. 1980;73:133-142.
16. Gorczyca W, Traganos F, Jesionowska H, Darzynkiewicz Z. Presence of DNA strand breaks and increased sensitivity of DNA in situ to denaturation in abnormal human sperm cells: analogy to apoptosis of somatic cells. Exp Cell Res. 1993;207:202-205.
17. Gross DS, Garrard WT. Nuclease hypersensitive sites in chromatin. Annu Rev Biochem. 1988;57:159-197.
18. Haines GA, Hendry JH, Daniel CP, Morris ID. Increased levels of comet-detected spermatozoa DNA damage following in vivo isotopic- or X-irradiation of spermatogonia. Mutat Res. 2001;495:21-32.
19. Haines GA, Hendry JH, Daniel CP, Morris ID. Germ cell and dose-dependent DNA damage measured by the comet assay in murine spermatozoa after testicular X-irradiation. Biol Reprod. 2002;67:854-861.
20. Haines G, Marples B, Daniel P, Morris I. DNA damage in human and mouse spermatozoa after in vitro-irradiation assessed by the comet assay. Adv Exp Med Biol. 1998;444:79-91.
21. Harrouk W, Codrington A, Vinson R, Robaire B, Hales BF. Paternal exposure to cyclophosphamide induces DNA damage and alters the expression of DNA repair genes in the rat preimplantation embryo. Mutat Res. 2000a;461:229-241.
22. Harrouk W, Khatabaksh S, Robaire B, Hales BF. Paternal exposure to cyclophosphamide dysregulates the gene activation program in rat preimplantation embryos. Mol Reprod Dev. 2000b;57:214-223.
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. Jackson H. The effects of alkylating agents on fertility. Br Med Bull. 1964;20:107-114.
25. Jenkinson PC, Anderson D. Malformed foetuses and karyotype abnormalities in the offspring of cyclophosphamide and allyl alcohol-treated male rats. Mutat Res. 1990;229:173-184.
26. Kierszenbaum AL. Transition nuclear proteins during spermiogenesis: unrepaired DNA breaks not allowed. Mol Reprod Dev. 2001;58:357-358.
27. Koppen G, Angelis KJ. Repair of X-ray induced DNA damage measured by the comet assay in roots of Vicia faba. Environ Mol Mutagen. 1998;32:281-285.
28. Kusakabe H, Szczygiel MA, Whittingham DG, Yanagimachi R. Maintenance of genetic integrity in frozen and freeze-dried mouse spermatozoa. Proc Natl Acad Sci U S A. 2001;98:13501-13506.
29. Larson KL, DeJonge CJ, Barnes AM, Jost LK, Evenson DP. Sperm chromatin structure assay parameters as predictors of failed pregnancy following assisted reproductive techniques. Hum Reprod. 2000;15:1717-1722.
30. Lopes S, Jurisicova A, Casper RF. Gamete-specific DNA fragmentation in unfertilized human oocytes after intracytoplasmic sperm injection. Hum Reprod. 1998a;13:703-708.
31. 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. 1998b;69:528-532.
32. Manicardi GC, Bianchi PG, Pantano S, Azzoni P, Bizzaro D, Bianchi U, Sakkas D. Presence of endogenous nicks in DNA of ejaculated human spermatozoa and its relationship to chromomycin A3 accessibility. Biol Reprod. 1995;52:864-867.
33. Manicardi GC, Tombacco A, Bizzaro D, Bianchi U, Bianchi PG, Sakkas D. DNA strand breaks in ejaculated human spermatozoa: comparison of susceptibility to the nick translation and terminal transferase assays. Histochem J. 1998;30:33-39.
34. McPherson SM, Longo FJ. Localization of DNase I-hypersensitive regions during rat spermatogenesis: stage-dependent patterns and unique sensitivity of elongating spermatids. Mol Reprod Dev. 1992;31:268-279.
35. McPherson SM, Longo FJ. Chromatin structure-function alterations during mammalian spermatogenesis: DNA nicking and repair in elongating spermatids. Eur J Histochem. 1993a;37:109-128.
36. McPherson SM, Longo FJ. Nicking of rat spermatid and spermatozoa DNA: possible involvement of DNA topoisomerase II. Dev Biol. 1993b;158:122-130.
37. Morris ID, Ilott S, Dixon L, Brison DR. 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. 2002;17:990-998.
38. Muenchen HJ, Pienta KJ. The role of the nuclear matrix in cancer chemotherapy. Crit Rev Eukaryot Gene Expr. 1999;9:337-343.
39. Olshan AF, Mattison DR, eds. Male Mediated Developmental Toxicity. New York, NY: Plenum Press; 1994.
40. Poccia D. Remodeling of nucleoproteins during gametogenesis, fertilization, and early development. Int Rev Cytol. 1986;105:1-65.
41. Pont J, Albrecht W. Fertility after chemotherapy for testicular germ cell cancer. Fertil Steril. 1997;68:1-5.
42. Qiu J, Hales BF, Robaire B. Effects of chronic low-dose cyclophosphamide exposure on the nuclei of rat spermatozoa. Biol Reprod. 1995a; 52:33-40.
43. Qiu J, Hales BF, Robaire B. Damage to rat spermatozoal DNA after chronic cyclophosphamide exposure. Biol Reprod. 1995b;53:1465-1473.
44. Robaire B, Hales BF, eds. Advances in Male-Mediated Developmental Toxicity. New York, NY: Kluwer Academic/Plenum Press; 2003.
45. Russell LB, Hunsicker PR, Cacheiro NL, Bangham JW, Russell WL, Shelby MD. Chlorambucil effectively induces deletion mutations in mouse germ cells. Proc Natl Acad Sci U S A. 1989;86:3704-3708.
46. Russell LB, Hunsicker PR, Shelby MD. Melphalan, a second chemical for which specific-locus mutation induction in the mouse is maximum in early spermatids. Mutat Res. 1992;282:151-158.
47. Russell WL, Kelly EM, Hunsicker PR, Bangham JW, Maddux SC, Phipps EL. Specific-locus test shows ethylnitrosourea to be the most potent mutagen in the mouse. Proc Natl Acad Sci U S A. 1979;76:5818-5819.
48. 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 assay. J Androl. 1995;16:80-87.
49. Sakkas D, Manicardi G, Bianchi PG, Bizzaro D, Bianchi U. Relationship between the presence of endogenous nicks and sperm chromatin packaging in maturing and fertilizing mouse spermatozoa. Biol Reprod. 1995;52:1149-1155.
50. Sakkas D, Urner F, Bianchi PG, Bizzaro D, Wagner I, Jaquenoud N, Manicardi G, Campana A. Sperm chromatin anomalies can influence decondensation after intracytoplasmic sperm injection. Hum Reprod. 1996;11:837-843.
51. Schilsky RL, Lewis BJ, Sherins RJ, Young RC. Gonadal dysfunction in patients receiving chemotherapy for cancer. Ann Intern Med. 1980;93:109-114.
52. Sega GA. Molecular dosimetry of chemical mutagens. Measurement of molecular dose and DNA repair in mammalian germ cells. Mutat Res. 1976;38:317-326.
53. Sega GA, Owens JG. Methylation of DNA and protamine by methyl methanesulfonate in the germ cells of male mice. Mutat Res. 1983;111:227-244.
54. Sega GA, Wolfe KW, Owens JG. A comparison of the molecular action of an SN1-type methylating agent, methyl nitrosourea and an SN2-type methylating agent, methyl methanesulfonate, in the germ cells of male mice. Chem Biol Interact. 1981;33:253-269.
55. Singh NP, Danner DB, Tice RR, McCoy MT, Collins GD, Schneider EL. Abundant alkali-sensitive sites in DNA of human and mouse sperm. Exp Cell Res. 1989;184:461-470.
56. Singh NP, McCoy MT, Tice RR, Schneider EL. A simple technique for quantitation of low levels of DNA damage in individual cells. Exp Cell Res. 1988;175:184-191.
57. Sinha Hikim AP, Swerdloff RS. Hormonal and genetic control of germ cell apoptosis in the testis. Rev Reprod. 1999;4:38-47.
58. Sotomayor RE, Cumming RB. Induction of translocations by cyclophosphamide in different germ cell stages of male mice: cytological characterization and transmission. Mutat Res. 1975;27:375-388.
59. Sotomayor RE, Sega GA, Cumming RB. Unscheduled DNA synthesis in spermatogenic cells of mice treated in vivo with the indirect alkylating agents cyclophosphamide and mitomen. Mutat Res. 1978;50:229-240.
60. 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.
61. Tice RR, Agurell E, Anderson D, et al. Single cell gel/comet assay: guidelines for in vitro and in vivo genetic toxicology testing. Environ Mol Mutagen. 2000;35:206-221.
62. Trasler JM, Hales BF, Robaire B. Paternal cyclophosphamide treatment of rats causes fetal loss and malformations without affecting male fertility. Nature. 1985;316:144-146.
63. Trasler JM, Hales BF, Robaire B. Chronic low dose cyclophosphamide treatment of adult male rats: effect on fertility, pregnancy outcome and progeny. Biol Reprod. 1986;34:275-283.
64. Trasler JM, Hales BF, Robaire B. A time-course study of chronic paternal cyclophosphamide treatment in rats: effects on pregnancy outcome and the male reproductive and hematologic systems. Biol Reprod. 1987;37:317-326.
65. Ward WS. Deoxyribonucleic acid loop domain tertiary structure in mammalian spermatozoa. Biol Reprod. 1993;48:1193-1201.
66. Ward WS, Coffey DS. DNA packaging and organization in mammalian spermatozoa: comparison with somatic cells. Biol Reprod. 1991;44:569-574.
67. Wouters-Tyrou D, Martinage A, Chevaillier P, Sautiere P. Nuclear basic proteins in spermiogenesis. Biochimie. 1998;80:117-128.