Human sperm chromatin undergoes physiological remodeling during in vitro capacitation and acrosome reaction

Journal of Andrology

Volumn 33, Issue 5, 2012, Pages 1025-1035

  De Lamirande, E ^a   San Gabriel, M C ^a   Zini, A ^a  

^a ROYAL VICTORIA HOSPITAL   (Canada)

Author keywords

Aniline blue; DNA fragmentation index; Induced decondensation; Iodoacetamide fluorescein; Sperm physiology; Toluidine blue

Indexed keywords

CHROMOMYCIN A3; DITHIOTHREITOL; DNA; DODECYL SULFATE SODIUM; LYSOPHOSPHATIDYLCHOLINE; TOLUIDINE DERIVATIVE; HISTONE; PROTAMINE;

ACROSOME REACTION; ARTICLE; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; CONTROLLED STUDY; DNA DAMAGE; DNA FRAGMENTATION; HUMAN; HUMAN CELL; IN VITRO STUDY; MALE; NORMAL HUMAN; PRIORITY JOURNAL; SPERM; SPERMATOZOON; SPERMATOZOON CAPACITATION; SPERMATOZOON HEAD; DRUG EFFECT; METABOLISM; METHODOLOGY; PATHOLOGY; STAINING;

ACROSOME REACTION; CHROMATIN ASSEMBLY AND DISASSEMBLY; DITHIOTHREITOL; DNA DAMAGE; HISTONES; HUMANS; LYSOPHOSPHATIDYLCHOLINES; MALE; PROTAMINES; SODIUM DODECYL SULFATE; SPERM CAPACITATION; SPERM HEAD; STAINING AND LABELING;

EID: 84870724980     PISSN: 01963635     EISSN: 19394640     Source Type: Journal    
DOI: 10.2164/jandrol.111.015982     Document Type: Article

References (58)

1. Abbasi M, Alizadeh R, Abolhassani F, Amidi F, Ragerdi KI, Fazelipour S, Hoshino Y, Sato E, Dehpour AR. Effect of aminoguanidine in sperm DNA fragmentation in varicocelized rats: role of nitric oxide. Reprod Sci. 2011;18:545-550.
2. 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.
3. Agarwal A, Juris E, Rakesh S. Sperm chromatin assessment. In: Gardner DK, Weissman A, Howles CM, Shoham Z, eds. Textbook of Assisted Reproductive Technologies, Laboratory and Clinical Perspectives. 3rd ed. London, United Kingdom: Informa Healthcare; 2008:67-84.
4. Baker HW, Liu DY, Garrett C, Martic M. The human acrosome reaction. Asian J Androl. 2000;2:172-178.
5. Balhorn R. Sperm chromatin: an overview. In: Zini, A, Agarwal, A, eds. Sperm Chromatin: Biological and Clinical Applications in Male Infertility and Assisted Reproduction. New York, NY: Springer; 2011:3-18.
6. Barratt CLR, Aitken RJ, Bjorndahl L, Carrell DT, de Boer P, Kvist U, Lewis SE, Perreault SD, Perry MJ, Ramos L, Robaire B, Ward S, Zini A. Sperm DNA: organization, protection and vulnerability: from basic science to clinical applications-a position report. Hum Reprod. 2010;25:824-838.
7. Bianchi PG, Manicardi GC, Bizzaro D, Bianchi U, Sakkas D. Effect of deoxyribonucleic acid protamination on fluorochrome staining and in situ nick-translation of murine and human mature spermatozoa. Biol Reprod. 1993;49:1083-1088.
8. Björndahl L, Kvist U. Human sperm chromatin stabilization: a proposed model including zinc bridges. Mol Hum Reprod. 2010; 16:23-29.
9. Blaise G. Heparin and protamine interaction. Can J Anaesth. 1998;45:1144-1147.
10. Chatterjee S, de Lamirande E, Gagnon C. Cryopreservation alters membrane sulfhydryl status of bull spermatozoa: protection by oxidized glutathione. Mol Reprod Dev. 2001;60:498-506.
11. Codrington AM, Hales BF, Robaire B. Exposure of male rats to cyclophosphamide alters the chromatin structure and basic proteome in spermatozoa. Hum Reprod. 2007;22:1431-1442.
12. Dadoune JP, Mayaux MJ, Guihard-Moscato ML. Correlation between defects in chromatin condensation of human spermatozoa stained by aniline blue and semen characteristics. Andrologia. 1988;20:211-217.
13. De Jonge C. Biological basis for human capacitation. Hum Reprod Update. 2005;11:205-214.
14. de Lamirande E, Gagnon C. Reactive oxygen species and human spermatozoa: I. Effects on the motility of intact spermatozoa and on sperm axonemes. J Androl. 1992;13:368-378.
15. de Lamirande E, Gagnon C. Capacitation-associated production of superoxide anion by human spermatozoa. Free Radic Biol Med. 1995;18:487-495.
16. de Lamirande E, Gagnon C. Paradoxical effect of reagents for sulfhydryl and disulfide groups on human sperm capacitation and superoxide production. Free Radic Biol Med. 1998;25:803-817.
17. de Lamirande E, Lamothe G. Levels of semenogelin in human spermatozoa decrease during capacitation: involvement of reactive oxygen species and zinc. Hum Reprod. 2010;25:1619-1630.
18. de Lamirande E, Lamothe G, Villemure M. Control of superoxide and nitric oxide formation during human sperm capacitation. Free Radic Biol Med. 2009;46:1420-1427.
19. de Lamirande E, Leclerc P, Gagnon C. Capacitation as a regulatory event that primes spermatozoa for the acrosome reaction and fertilization. Mol Hum Reprod. 1997;3:175-194.
20. de Lamirande E, O'Flaherty C. Sperm activation: role of reactive oxygen species and kinases. Biochim Biophys Acta. 2008;1784: 106-115.
21. de Lamirande E, Tsai C, Harakat A, Gagnon C. Involvement of reactive oxygen species in human sperm arcosome reaction induced by A23187, lysophosphatidylcholine, and biological fluid ultrafiltrates. J Androl. 1998;19:585-594.
22. Engh E, Clausen OP, Scholberg A, Tollefsrud A, Purvis K. Relationship between sperm quality and chromatin condensation measured by sperm DNA fluorescence using flow cytometry. Int J Androl. 1992;15:407-415.
23. Erenpreisa J, Erenpreiss J, Freivalds T, Slaidina M, Krampe R, Butikova J, Ivanov A, Pjanova D. Toluidine blue test for sperm DNA integrity and elaboration of image cytometry algorithm. Cytometry A. 2003;52:19-27.
24. Erenpreiss J, Bars J, Lipatnikova V, Erenpreisa J, Zalkalns J. Comparative study of cytochemical tests for sperm chromatin integrity. J Androl. 2001;22:45-53.
25. Evenson DP. Sperm chromatin structure assay (SCSAH): 30 years of experience with the SCSAH. In: Zini A, Agarwal A, eds. Sperm Chromatin: Biological and Clinical Applications in Male Infertility and Assisted Reproduction. New York, NY: Springer; 2011:125-149.
26. Evenson DP, Jost LK, Marshall D, Zinaman MJ, Clegg E, Purvis K, de Angelis P, Claussen OP. Utility of the sperm chromatin structure assay as a diagnostic and prognostic tool in the human fertility clinic. Hum Reprod. 1999;14:1039-1049.
27. Giles NM, Watts AB, Giles GI, Fry FH, Littlechild JA, Jacob C. Metal and redox modulation of cysteine protein function. Chem Biol. 2003;10:677-693.
28. Hales BF, Grenier L, Lalancette C, Robaire B. Epigenetic programming: from gametes to blastocyst. Birth Defects Res Part A: Clin Mol Teratol. 2011;91:652-665.
29. 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.
30. Huret JL, Courtot AM. Effect of migration and capacitation on the nuclear stability of human sperm. Arch Androl. 1984;13:147-152.
31. Kirkman-Brown JC, Punt EL, Barratt CL, Publicover SJ. Zona pellucida and progesterone-induced Ca2+ signaling and acrosome reaction in human spermatozoa. J Androl. 2002;23:306-315.
32. Kosower NS, Katayose H, Yanagimachi R. Thiol-disulfide status and acridine orange fluorescence of mammalian sperm nuclei. J Androl. 1992;13:342-348.
33. Krzanowska H. Toluidine blue staining reveals changes in chromatin stabilization of mouse spermatozoa during epididymal maturation and penetration of ova. J Reprod Fertil. 1982;64:97-101.
34. Liguori L, de Lamirande E, Minelli A, Gagnon C. Various protein kinases regulate human sperm acrosome reaction and the associated phosphorylation of Tyr residues and of the Thr-Glu-Tyr motif. Mol Hum Reprod. 2005;11:211-221.
35. Liu DY, Baker HW. Sperm nuclear chromatin normality: relationship with sperm morphology, sperm-zona pellucida binding, and fertilization rates in vitro. Fertil Steril. 1992;58:1178-1184.
36. Marchesi DE, Biederman H, Ferrara S, Hershlag A, Feng HL. The effect of semen processing on sperm DNA integrity: comparison of two techniques using the novel toluidine blue assay. Eur J Obstet Gynecol Reprod Biol. 2010;151:176-180.
37. Maret W. Zinc coordination environments in proteins determine zinc functions. J Trace Elem Med Biol. 2005;19:7-12.
38. Molina J, Castilla JA, Gil T, Hortas ML, Vergara F, Herruzo A. Influence of incubation on the chromatin condensation and nuclear stability of human spermatozoa by flow cytometry. Hum Reprod. 1995;10:1280-1286.
39. O'Flaherty C, de Lamirande E, Gagnon C. Positive role of reactive oxygen species in mammalian sperm capacitation: triggering and modulation of phosphorylation events. Free Radic Biol Med. 2006a;41:528-540.
40. O'Flaherty C, de Lamirande E, Gagnon C. Reactive oxygen species modulate independent protein phosphorylation pathways during human sperm capacitation. Free Radic BiolMed. 2006b;40:1045-1055.
41. O'Flaherty C, Vaisheva F, Hales BF, Chan P, Robaire B. Characterization of sperm chromatin quality in testicular cancer and Hodgkin's lymphoma patients prior to chemotherapy. Hum Reprod. 2008;23:1044-1052.
42. Olds-Clarke P. Unresolved issues in mammalian fertilization. Int Rev Cytol. 2003;232:129-184.
43. Oliva A, Porstmann E, Caille A, Bartolomeo C. Effect of different culture techniques used to induce capacitation on the chromatin stability of human sperm. Int J Androl. 1992;15:293-298.
44. Oliva R, Castillo J. Sperm nucleoproteins. In: Zini A, Agarwal A, eds. Sperm Chromatin: Biological and Clinical Applications in Male Infertility and Assisted Reproduction. New York, NY: Springer; 2011:45-60.
45. Rodriguez H, Ohanian C, Bustos-Obregon E. Nuclear chromatin decondensation of spermatozoa in vitro: a method for evaluating the fertilizing ability of ovine semen. Int J Androl. 1985;8:147-158.
46. Romanato M, Julianelli V, Zappi M, Calvo L, Calvo JC. The presence of heparan sulfate in the mammalian oocyte provides a clue to human sperm nuclear decondensation in vivo. Hum Reprod. 2008;23:1145-1150.
47. Rosenborg L, Rao KM, Bjorndahl L, Kvist U, Pousette A, Akerlof E, Fredricsson B. Changes in human sperm chromatin stability during preparation for in-vitro fertilization. Int J Androl. 1990;13:287-296.
48. Rufas O, Fisch B, Seligman J, Tadir Y, Ovadia J, Shalgi R. Thiol status in human sperm. Mol Reprod Dev. 1991;29:282-288.
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. Singleton S, Mudrak O, Morshedi M, Oehninger S, Zalenskaya I, Zalensky A. Characterisation of a human sperm cell subpopulation marked by the presence of the TSH2B histone. Reprod Fertil Dev. 2007;19:392-397.
51. Talebi AR, Moein MR, Tabibnejad N, Ghasemzadeh J. Effect of varicocele on chromatin condensation and DNA integrity of ejaculated spermatozoa using cytochemical tests. Andrologia. 2008;40:245-251.
52. Tsarev I, Erenpreiss J. Cytochemical tests for sperm chromatin maturity. In: Zini A, Agarwal A, eds. Sperm Chromatin: Biological and Clinical Applications in Male Infertility and Assisted Reproduction. New York, NY: Springer; 2011:181-188.
53. Ward WS. Function of sperm chromatin structural elements in fertilization and development. Mol Hum Reprod. 2010;16:30-36.
54. World Health Organization (WHO). Laboratory Manual for the Examination of Human Semen and Semen-cervical Mucus Interaction. 4th ed. Cambridge, United Kingdom: Cambridge University Press; 1999.
55. Zalewski PD, Jian X, Soon LL, Breed WG, Seamark RF, Lincoln SF, Ward AD, Sun FZ. Changes in distribution of labile zinc in mouse spermatozoa during maturation in the epididymis assessed by the fluorophore Zinquin. Reprod Fertil Dev. 1996; 8:1097-1105.
56. Zini A, Azhar R, Baazeem A, Gabriel MS. Effect of microsurgical varicocelectomy on human sperm chromatin and DNA integrity: a prospective trial. Int J Androl. 2011;34:14-19.
57. Zini A, Bielecki R, Phang D, Zenzes MT. Correlations between two markers of sperm DNA integrity, DNA denaturation and DNA fragmentation, in fertile and infertile men. Fertil Steril. 2001; 75:674-677.
58. Zini A, Fischer MA, Sharir S, Shayegan B, Phang D, Jarvi K. Prevalence of abnormal sperm DNA denaturation in fertile and infertile men. Urology. 2002;60:1069-1072.