Fertility and Sterility
Volume 91, Issue 4 , Pages 1110-1118 , April 2009

Association of sperm apoptosis and DNA ploidy with sperm chromatin quality in human spermatozoa

  • Reda Z. Mahfouz, M.D.

      Affiliations

    • Reproductive Research Center, Glickman Urological and Kidney Institute and Department of Obstetrics and Gynecology, Cleveland Clinic, Cleveland, Ohio
  • ,
  • Rakesh K. Sharma, Ph.D.

      Affiliations

    • Reproductive Research Center, Glickman Urological and Kidney Institute and Department of Obstetrics and Gynecology, Cleveland Clinic, Cleveland, Ohio
  • ,
  • Tamer M. Said, M.D.

      Affiliations

    • Toronto Institute for Reproductive Medicine, Toronto, Ontario, Canada
  • ,
  • Juris Erenpreiss, M.D.

      Affiliations

    • Andrology Laboratory, Riga Stradins University, Riga, Latvia
  • ,
  • Ashok Agarwal, Ph.D., H.C.L.D.

      Affiliations

    • Reproductive Research Center, Glickman Urological and Kidney Institute and Department of Obstetrics and Gynecology, Cleveland Clinic, Cleveland, Ohio
    • Corresponding Author InformationReprint requests: Ashok Agarwal, Ph.D., H.C.L.D., Professor and Director, Reproductive Research Center, 9500 Euclid Avenue, Desk A19.1, Cleveland Clinic, Cleveland OH 44195 (FAX: 216-445-6049).

Received 14 November 2007 ,Revised 11 January 2008 ,Accepted 11 January 2008.

References 

  1. Allamaneni SS, Agarwal A, Rama S, Ranganathan P, Sharma RK. Comparative study on density gradients and swim-up preparation techniques utilizing neat and cryopreserved spermatozoa. Asian J Androl. 2005;7:86–92
  2. Morrell JM. Update on semen technologies for animal breeding. Reprod Domest Anim. 2006;41:63–67
  3. Canto CL, Segurado AC, Pannuti C, Cedenho A, Srougi M, Spaine D, et al. Detection of HIV and HCV RNA in semen from Brazilian coinfected men using multiplex PCR before and after semen washing. Rev Inst Med Trop Sao Paulo. 2006;48:201–206
  4. Mousset-Simeon N, Rives N, Masse L, Chevallier F, Mace B. Comparison of six density gradient media for selection of cryopreserved donor spermatozoa. J Androl. 2004;25:881–884
  5. Henkel RR, Schill WB. Sperm preparation for ART. Reprod Biol Endocrinol. 2003;1:108
  6. Marchesi DE, Feng HL. Sperm DNA integrity from sperm to egg. J Androl. 2007;28:481–489
  7. Dias GM, Retamal CA, Tobella L, Arnholdt AC, Lopez ML. Nuclear status of immature and mature stallion spermatozoa. Theriogenology. 2006;66:354–365
  8. Perdichizzi A, Nicoletti F, La Vignera S, Barone N, D'Agata R, Vicari E, et al. Effects of tumour necrosis factor-alpha on human sperm motility and apoptosis. J Clin Immunol. 2007;27:152–162
  9. Bungum M, Humaidan P, Axmon A, Spano M, Bungum L, Erenpreiss J, et al. Sperm DNA integrity assessment in prediction of assisted reproduction technology outcome. Hum Reprod. 2007;22:174–179
  10. Agarwal A, Said TM. Role of sperm chromatin abnormalities and DNA damage in male infertility. Hum Reprod Update. 2003;9:331–345
  11. Evenson D, Wixon R. Meta-analysis of sperm DNA fragmentation using the sperm chromatin structure assay. Reprod Biomed Online. 2006;12:466–472
  12. Erenpreiss J, Jepson K, Giwercman A, Tsarev I, Erenpreisa J, Spano M. Toluidine blue cytometry test for sperm DNA conformation: comparison with the flow cytometric sperm chromatin structure and TUNEL assays. Hum Reprod. 2004;19:2277–2282
  13. Sakkas D, Moffatt O, Manicardi GC, Mariethoz E, Tarozzi N, Bizzaro D. Nature of DNA damage in ejaculated human spermatozoa and the possible involvement of apoptosis. Biol Reprod. 2002;66:1061–1067
  14. Sakkas D, Leppens-Luisier G, Lucas H, Chardonnens D, Campana A, Franken DR, et al. Localization of tyrosine phosphorylated proteins in human sperm and relation to capacitation and zona pellucida binding. Biol Reprod. 2003;68:1463–1469
  15. Angelopoulou R, Plastira K, Msaouel P. Spermatozoal sensitive biomarkers to defective protaminosis and fragmented DNA. Reprod Biol Endocrinol. 2007;5:36
  16. Aziz N, Said T, Paasch U, Agarwal A. The relationship between human sperm apoptosis, morphology and the sperm deformity index. Hum Reprod. 2007;22:1413–1419
  17. Grunewald S, Baumann T, Paasch U, Glander HJ. Capacitation and acrosome reaction in nonapoptotic human spermatozoa. Ann NY Acad Sci. 2006;1090:138–146
  18. Grunewald S, Paasch U, Said TM, Sharma RK, Glander HJ, Agarwal A. Caspase activation in human spermatozoa in response to physiological and pathological stimuli. Fertil Steril. 2005;83(Suppl 1):1106–1112
  19. Grunewald S, Said TM, Paasch U, Glander HJ, Agarwal A. Relationship between sperm apoptosis signalling and oocyte penetration capacity. Int J Androl. Published online 15 June 2007 [Epub ahead of print].
  20. Paasch U, Agarwal A, Gupta AK, Sharma RK, Grunewald S, Thomas AJ, et al. Apoptosis signal transduction and the maturity status of human spermatozoa. Ann NY Acad Sci. 2003;1010:486–488
  21. Paasch U, Grunewald S, Agarwal A, Glandera HJ. Activation pattern of caspases in human spermatozoa. Fertil Steril. 2004;81(Suppl 1):802–809
  22. Said TM, Agarwal A, Grunewald S, Rasch M, Glander HJ, Paasch U. Evaluation of sperm recovery following annexin V magnetic-activated cell sorting separation. Reprod Biomed Online. 2006;13:336–339
  23. Paasch U, Grunewald S, Glander HJ. Sperm selection in assisted reproductive techniques. Soc Reprod Fertil Supp. 2007;65:515–525
  24. Grizard G, Ouchchane L, Roddier H, Artonne C, Sion B, Vasson MP, et al. In vitro alachlor effects on reactive oxygen species generation, motility patterns and apoptosis markers in human spermatozoa. Reprod Toxicol. 2007;23:55–62
  25. Oancea M, Mazumder S, Crosby ME, Almasan A. Apoptosis assays. Methods Mol Med. 2006;129:279–290
  26. Shen HM, Dai J, Chia SE, Lim A, Ong CN. Detection of apoptotic alterations in sperm in subfertile patients and their correlations with sperm quality. Hum Reprod. 2002;17:1266–1273
  27. Varum S, Bento C, Sousa AP, Gomes-Santos CS, Henriques P, Almeida-Santos T, et al. Characterization of human sperm populations using conventional parameters, surface ubiquitination, and apoptotic markers. Fertil Steril. 2007;87:572–583
  28. Kurz A, Viertel D, Herrmann A, Muller K. Localization of phosphatidylserine in boar sperm cell membranes during capacitation and acrosome reaction. Reproduction. 2005;130:615–626
  29. Paasch U, Sharma RK, Gupta AK, Grunewald S, Mascha EJ, Thomas AJ, et al. Cryopreservation and thawing is associated with varying extent of activation of apoptotic machinery in subsets of ejaculated human spermatozoa. Biol Reprod. 2004;71:1828–1837
  30. O'Neill DA, McVicar CM, McClure N, Maxwell P, Cooke I, Pogue KM, et al. Reduced sperm yield from testicular biopsies of vasectomized men is due to increased apoptosis. Fertil Steril. 2007;87:834–841
  31. Alvarez JG. DNA fragmentation in human spermatozoa: significance in the diagnosis and treatment of infertility. Minerva Ginecologica. 2003;55:233–239
  32. Fraser L, Strzezek J. Effect of different procedures of ejaculate collection, extenders and packages on DNA integrity of boar spermatozoa following freezing-thawing. Anim Reprod Sci. 2007;99:317–329
  33. World Health Organization WHO. WHO laboratory manual for the examination of human semen and sperm-cervical mucus interaction. 4th ed.. Cambridge: Cambridge University Press; 1999;
  34. Beletti ME, Mello ML. Comparison between the toluidine blue stain and the Feulgen reaction for evaluation of rabbit sperm chromatin condensation and their relationship with sperm morphology. Theriogenology. 2004;62:398–402
  35. Erenpreisa J, Erenpreiss J, Freivalds T, Slaidina M, Krampe R, Butikova J, et al. Toluidine blue test for sperm DNA integrity and elaboration of image cytometry algorithm. Cytometry A. 2003;52:19–27
  36. Boe-Hansen GB, Fedder J, Ersboll AK, Christensen P. The sperm chromatin structure assay as a diagnostic tool in the human fertility clinic. Hum Reprod. 2006;21:1576–1582
  37. Vermes I, Haanen C, Steffens-Nakken H, Reutelingsperger C. A novel assay for apoptosis. Flow cytometric detection of phosphatidylserine expression on early apoptotic cells using fluorescein labelled annexin V. J Immunol Methods. 1995;184:39–51
  38. Moreau MF, Guillet C, Massin P, Chevalier S, Gascan H, Basle MF, et al. Comparative effects of five bisphosphonates on apoptosis of macrophage cells in vitro. Biochem Pharmacol. 2007;73:718–723
  39. Chaveiro A, Santos P, da Silva F. Assessment of sperm apoptosis in cryopreserved bull semen after swim-up treatment: a flow cytometric study. Reprod Domest Anim. 2007;42:17–21
  40. Andre S, Pinto AE, Laranjeira C, Quaresma M, Soares J. Male and female breast cancer—differences in DNA ploidy, p21 and p53 expression reinforce the possibility of distinct pathways of oncogenesis. Pathobiology. 2007;74:323–327
  41. Graesslin O, Chantot-Bastaraud S, Lorenzato M, Birembaut P, Quereux C, Darai E. Fluorescence in situ hybridization and immunohistochemical analysis of p53 expression in endometrial cancer: prognostic value and relation to ploidy. Ann Surg Oncol. Published online 11 December 2007 [Epub ahead of print].
  42. Levek-Motola N, Soffer Y, Shochat L, Raziel A, Lewin LM, Golan R. Flow cytometry of human semen: a preliminary study of a non-invasive method for the detection of spermatogenetic defects. Hum Reprod. 2005;20:3469–3475
  43. Marchiani S, Tamburrino L, Maoggi A, Vannelli GB, Forti G, Baldi E, et al. Characterization of M540 bodies in human semen: evidence that they are apoptotic bodies. Mol Hum Reprod. 2007;13:621–631
  44. Srinivas M, Degaonkar M, Gupta DK, Raghunathan P, Das SN, Mitra DK. Evaluation of developing rat testis by phosporus 31P magnetic resonance spectroscopy and DNA flow cytometry. Pediatr Surg Int. 2001;17:316–320
  45. Oliveira H, Loureiro J, Filipe L, Santos C, Ramalho-Santos J, Sousa M, et al. Flow cytometry evaluation of lead and cadmium effects on mouse spermatogenesis. Reprod Toxicol. 2006;22:529–535
  46. Sarkar S, Jones OW, Shioura N. Constancy in human sperm DNA content. Proc Natl Acad Sci U S A. 1974;71:3512–3516
  47. He Y, Cao Y, Xu YJ, Huang J, Sun ZX, Zhou ZM, et al. [Experimental study on the effects of Jujingwan on oligospermia]. Zhonghua Nan Ke Xue. 2006;12:1135–1138
  48. Cui FJ, Li Y, Xu YY, Liu ZQ, Huang DM, Zhang ZC, et al. Induction of apoptosis in SGC-7901 cells by polysaccharide-peptide GFPS1b from the cultured mycelia of Grifola frondosa GF9801. Toxicol In Vitro. 2007;21:417–427
  49. Tarozzi N, Bizzaro D, Flamigni C, Borini A. Clinical relevance of sperm DNA damage in assisted reproduction. Reprod Biomed Online. 2007;14:746–757
  50. Aitken RJ, De Iuliis GN. Origins and consequences of DNA damage in male germ cells. Reprod Biomed Online. 2007;14:727–733
  51. Agarwal A, Gupta S, Sikka S. The role of free radicals and antioxidants in reproduction. Curr Opin Obstet Gynecol. 2006;18:325–332
  52. Samardzija M, Karadjole M, Matkovic M, Cergolj M, Getz I, Dobranic T, et al. A comparison of BoviPure and Percoll on bull sperm separation protocols for IVF. Anim Reprod Sci. 2006;91:237–247
  53. Morrell JM, Moffatt O, Sakkas D, Manicardi GC, Bizzaro D, Tomlinson M, et al. Reduced senescence and retained nuclear DNA integrity in human spermatozoa prepared by density gradient centrifugation. J Assist Reprod Genet. 2004;21:217–222
  54. Moskovtsev SI, Willis J, White J, Mullen JB. Sperm survival: relationship to age-related sperm DNA integrity in infertile men. Arch Androl. 2007;53:29–32
  55. Weng SL, Taylor SL, Morshedi M, Schuffner A, Duran EH, Beebe S, et al. Caspase activity and apoptotic markers in ejaculated human sperm. Mol Hum Reprod. 2002;8:984–991
  56. Chen Z, Hauser R, Trbovich AM, Shifren JL, Dorer DJ, Godfrey-Bailey L, et al. The relationship between human semen characteristics and sperm apoptosis: a pilot study. J Androl. 2006;27:112–120
  57. Stronati A, Manicardi GC, Cecati M, Bordicchia M, Ferrante L, Spano M, et al. Relationships between sperm DNA fragmentation, sperm apoptotic markers and serum levels of CB-153 and p,p'-DDE in European and Inuit populations. Reproduction. 2006;132:949–958
  58. Kajstura M, Halicka HD, Pryjma J, Darzynkiewicz Z. Discontinuous fragmentation of nuclear DNA during apoptosis revealed by discrete “sub-G1” peaks on DNA content histograms. Cytometry A. 2007;71:125–131
  59. Muriel L, Goyanes V, Segrelles E, Gosalvez J, Alvarez JG, Fernandez JL. Increased aneuploidy rate in sperm with fragmented DNA as determined by the sperm chromatin dispersion (SCD) test and FISH analysis. J Androl. 2007;28:38–49
  60. Sloter ED, Marchetti F, Eskenazi B, Weldon RH, Nath J, Cabreros D, et al. Frequency of human sperm carrying structural aberrations of chromosome 1 increases with advancing age. Fertil Steril. 2007;87:1077–1086
  61. Wyrobek AJ, Eskenazi B, Young S, Arnheim N, Tiemann-Boege I, Jabs EW, et al. Advancing age has differential effects on DNA damage, chromatin integrity, gene mutations, and aneuploidies in sperm. Proc Natl Acad Sci U S A. 2006;103:9601–9606
  62. Lachaud C, Tesarik J, Canadas ML, Mendoza C. Apoptosis and necrosis in human ejaculated spermatozoa. Hum Reprod. 2004;19:607–610

 R.Z.M. has nothing to disclose. R.K.S. has nothing to disclose. T.M.S. has nothing to disclose. J.E. has nothing to disclose. A.A. has nothing to disclose.

PII: S0015-0282(08)00142-8

doi: 10.1016/j.fertnstert.2008.01.047

Fertility and Sterility
Volume 91, Issue 4 , Pages 1110-1118 , April 2009