Apoptosis, spermatogenesis and male infertility

Frontiers in Bioscience - Elite

Volumn 4 E, Issue 2, 2012, Pages 746-754

  Shukla, Kamla Kant ^a,b   Mahdi, Abbas Ali ^b   Singh, Rajender ^a  

^a CENTRAL DRUG RESEARCH INSTITUTE   (India)

^b KING GEORGE'S MEDICAL UNIVERSITY   (India)

Author keywords

Apoptosis; Male infertility; Review; Sperm

Indexed keywords

APOPTOSIS INDUCING FACTOR; CYTOCHROME C; FAS ANTIGEN; FAS LIGAND; FOLLITROPIN; LUTEINIZING HORMONE; REACTIVE OXYGEN METABOLITE;

ADENOHYPOPHYSIS; APOPTOSIS; AZOOSPERMIA; BLOOD TESTIS BARRIER; CELL DIFFERENTIATION; CELL DIVISION; CELL PROLIFERATION; CELL RENEWAL; CRYPTORCHISM; DNA FRAGMENTATION; DOUBLE STRANDED DNA BREAK; HIGH TEMPERATURE; HUMAN; MALE FERTILITY; MALE INFERTILITY; NONHUMAN; OCCUPATIONAL EXPOSURE; OLIGOSPERMIA; OXIDATIVE STRESS; QUALITY CONTROL; REPRODUCTION; REVIEW; SERTOLI CELL; SIGNAL TRANSDUCTION; SPERMATID; SPERMATOCYTE; SPERMATOGENESIS; SPERMATOGONIUM; SPERMATOZOON; TESTIS; THERMOREGULATION; AGING; ANIMAL; MALE; PATHOLOGY; PHYSIOLOGY; SPERM;

AGING; ANIMALS; APOPTOSIS; CRYPTORCHIDISM; HUMANS; INFERTILITY, MALE; MALE; OXIDATIVE STRESS; SEMEN; SPERMATOGENESIS; TESTIS;

EID: 84860871091     PISSN: 19450494     EISSN: 19450508     Source Type: Journal    
DOI: None     Document Type: Review

References (91)

1. IM Cruz, Colmenares, CL Berrueta, PR Gomez, H Montes, L Berrueta, H Montes, S Salmen, JA Osuna. Evaluation of the quality of the human spermatozoon: comparison between spermatic DNA integrity and semen variables. Invest Clin 51, 87-99 (2010)
2. CA Fernandez. Free fatty acids block growth hormone (GH) releasing hormone-stimulated GH secretion in man directly at the pituitary. J Clin Endocrinol Metab 65, 634-642 (1987)
3. K Makker, A Agarwal and R Sharma. Oxidative stress & male infertility. Indian J Med Res 129, 357- 367 (2009)
4. World Health Organization. Laboratory manual for the examination of human semen and sperm cervical mucus interaction. 4th ed. New York: Cambridge University Press (1999)
5. S Lambard, DI Galeraud, G Martin, R Levy, A Chocat and S Carreau. Analysis and significance of mRNA in human ejaculated sperm from normozoospermic donors: relationship to sperm motility and capacitation. Mol Hum Reprod 10, 535-541 (2004)
6. R Angelopoulou, K Plastira and P Msaouel. Spermatozoal sensitive biomarkers to defective protaminosis and fragmented DNA. Reprod Biol Endocrinol 5, 36 (2007)
7. JF Kerr. History of the events leading to the formulation of the apoptosis concept. Toxicology 181, 471-474 (2002)
8. JJ Cohen. Apoptosis: the physiologic pathway of cell death. Hosp Pract 28, 35-43 (1993)
9. S Afford, S Randhawa. Apoptosis. Mol Pathol 53, 55-63 (2000)
10. F Simone, M Adrienne, Gorman, H Osamu and S Afshin. Cellular Stress Responses: Cell Survival and Cell Death. International Journal of Cell Biol, Article ID 214074, 23 (2010)
11. AT Vaughan, CJ Betti, MJ Villalobos. Surviving apoptosis. Apoptosis 7, 173-177. (2002)
12. S Rajender, P Rahul, AA Mahdi. Mitochondria, spermatogenesis and male infertility. Mitochondrion 10, 419-428 (2010)
13. I Bourges, C Ramus, DCB Mousson, R Beugnot, C Remacle, P Cardol, G Hofhaus and JP Issartel. Structural organization of mitochondrial human complex I: role of the ND4 and ND5 mitochondria-encoded subunits and interaction with prohibitin. Biochem J 383, 491-499 (2004)
14. MB Shamsi, S Venkatesh, M Tanwar, P Talwar, RK Sharma, A Dhawan, R Kumar, NP Gupta, N Malhota, N Singh, S Mittal, R Dada. DNA integrity and semen quality in men with low seminal antioxidant levels. Mutat Res 665, 29-36 (2009)
15. D Sakkas, O Moffatt, GC Manicardi, E Mariethoz, N Tarozzi, D Bizzaro. Nature of DNA damage in ejaculated human spermatozoa and the possible involvement of apoptosis. Biol Reprod 66, 1061-1067 (2002)
16. MD Stiblar. Morphometrical evaluation of germ cell apoptosis in infertile men. Folia Biol (Praha) 55, 233-237 (2009)
17. A Hassan, EM el-Nashar, T Mostafa. Programmed cell death in varicocele- bearing testes. Andrologia 41, 39-45 (2009)
18. RJ Aitken, AJ Koppers. Apoptosis and DNA damage in human spermatozoa. Asian J Androl 13, 36-42 (2011)
19. DP Evenson. Loss of livestock breeding efficiency due to uncompensable sperm nuclear defects. Reprod Fertil Dev 11, 1-15 (1999)
20. U Paasch, S Grunewald, A Agarwal, HJ Glandera. Activation pattern of caspases in human spermatozoa. Fertil Steril 81, 802-809 (2004)
21. M Cavalcanti, C Steilmann, K Failing, M Bergmann, S Kliesch, W Weidner, K Steger. Apoptotic gene expression in potentially fertile and subfertile men. Mol Hum Reprod (in press)
22. TM Said, U Paasch, HJ Glander, A Agarwal. Role of caspases in male infertility. Hum Reprod Update 10, 39-51(2004)
23. SL Taylor, SL Weng, P Fox, EH Duran, MS Morshedi, S Oehninger and SJ Beebe. Somatic cell apoptosis markers and pathways in human ejaculated sperm: potential utility as indicators of sperm quality. Mol Hum Reprod 10, 825-834 (2004)
24. ED Kim, AZ Barqawi, JT Seo, RB Meacham. Apoptosis: its importance in spermatogenic dysfunction. Urol Clin North Am 29, 755-765 (2002)
25. AP Sinha Hikim, Y Lue, M Diaz-Romero, PH Yen, C Wang, RS Swerdloff. Deciphering the pathways of germ cell apoptosis in the testis. J Steroid Biochem Mol Biol 85, 175-182 (2003)
26. TK Pareek, AR Joshi, A Sanyal, RR Dighe. Insights into male germ cell apoptosis due to depletion of gonadotropins C aused by GnRH antagonists. Apoptosis 12, 1085-1100 (2007)
27. CG Print, KL Loveland. Germ cell suicide: new insights into apoptosis during spermatogenesis. Bioassays 22, 423-430 (2000)
28. DS Martincic, I Virant Klun, B Zorn, HM Vrtovec. Germ cell apoptosis in the human testis. Pflugers Arch 442, 59-60 (2001)
29. F Porcelli, D Meggiolaro, A Carnevali, B Ferrandi. Fas ligand in bull ejaculated spermatozoa: A quantitative immunocytochemical study. Acta Histochem 108, 287-292 (2006)
30. D Sakkas, E Mariethoz and JC St John. Abnormal sperm parameters in humans are indicative of an abortive apoptotic mechanism linked to the Fasmediated pathway. Exp Cell Res 251, 350-355 (1999)
31. AE Calogero, S La Vignera, R Condorelli, A Perdichizzi, D Valenti, P Asero, U Corbone, B Boggia, N De Rossa, G Lombardi R D'Agata, E Vicari, M De Rossa. Environmental car exhaust pollution damages human sperm chromatin and DNA. J Endocrinol Invest, online Oct 15 (2010)
32. Q Wang, XF Zhao, YL Ji, H Wang, P Liu, C Zhang, Y Zhang, DX Xu. Mitochondrial signalling pathway is also involved in bisphenol a induced germ cell apoptosis in testes. Toxicol Lett 199, 129-135 (2010)
33. M Orazizadeh, LS Khorsandi, M Hashemitabar. Toxic effects of dexamethasone on mouse testicular germ cells. Andrologia 42, 247-253 (2010)
34. E Nieschlag, E Leifke. Empirical therapies for idiopathic infertility. In: Nieschlag E, Behre HM, eds. Andrology: male reproductive health and dysfunction. Heidelberg: Springer 12, 313-319 (1997)
35. FF Casanueva, L Villanueva, C Dieguez, Y Diaz, JA Cabranes, B Szoke, MF Scanlon, AV Schally, A Fernandez-Cruz. Free fatty acids block growth hormone (GH) releasing hormone-stimulated GH secretion in man directly at the pituitary. J Clin Endocrinol Metab 65, 634-642 (1987)
36. JJ Wirth, RS Mijal. Adverse effects of low level heavy metal exposure on male reproductive function. Syst Biol Reprod Med 56, 147-167 (2010)
37. A Ferlin, E Speltra, C Patassini, MA Pati, A Garolla, N Caretta, C Foresta.Heat shock protein and heat shock factor expression in sperm: relation to oligozoospermia and varicocele. J Urol 183, 1248-1252 (2010)
38. N Falzone, C Huyser, DR Franken, D Leszczynski. Mobile phone radiation does not induced pro-apoptosis effects in human spermatozoa. Radiat Res 174, 169-176 (2010)
39. R Rendtorff, C Hohmann, S Reinmuth, A Müller, R Dittrich, M Beyer, L Wickmann, T Keil, G Henze, Borgmann A Staudt. Hormone and Sperm Analyses after Chemo- and Radiotherapy in Childhood and Adolescence. Klin Padiatr 222, 145-149 (2010)
40. CM McVicar, N McClure, K Williamson, LH Dalzell, SE Lewis. Incidence of Fas positivity and deoxyribonucleic a acid double-standard breaks in human ejaculated sperm. Fertil Steril 81, 767-774 (2004)
41. M Anzar, L He, MM Buhr, TG Kroetsch, KP Pauls. Sperm apoptosis in fresh and cryopreserved bull semen detected by flow cytometry and its relationship with fertility. Biol Reprod 66, 354-360 (2002)
42. C Lachaud, J Tesarik, ML Cañadas, C Mendoza. Apoptosis and necrosis in human ejaculated spermatozoa. Hum Reprod 19, 607-610 (2004)
43. DC Martin. Malignancy in the cryptorchid testis. Urol Clin North Am 9, 371-376 (1982)
44. BA Kogan, R Gupta, KP Juenemann. Fertility in cryptorchidism: further development of an experimental model. J Urol 137, 128-131 (1987)
45. AM Schinder, P Diaz, A Cueddent, PC Sizonenko. Cryptorchidism: a morphological study of 670 biopsies. Helv Paediatr Acta 42, 145-158 (1987)
46. DS Huff, F Hadziselimovic, HM Snyder 3rd, JW Duckett, MA Keating. Postnantal testicular maldevelopment in unilateral cryptochidism. J Urol 142, 546-548 (1989)
47. F Hadziselimovic, B Herzog, M Buser. Development of cryptorchid testes. Eur J Pediatr 146, 8-12 (1987)
48. F Absalan, M Ronaghi. Molecular inversion probe assay. Methods Mol Biol 396, 315-330 (2007)
49. Setchell BP. The Parkes Lecture. Heat and the testis. J Reprod Fertil 114, 179-194 (1998)
50. L Lund and KT Nielsen. Varicocele testis and testicular temperature. Br J Urol 78, 113-135 (1996)
51. JF Griveau, P Renard, D Le Lannou. Superoxide anion production by human spermatozoa as a part of the ionophore induced acrosome reaction process. Int J Androl 18, 67-74 (1995)
52. KK Shukla, V Mishra, AA Mahdi, MK Ahmad, R Singh and SN Sankhwar. Mucuna pruriens Reduces DNA Damage and Improve Male Fertility. Biol Reprod 81, 470 (2009)
53. A Agarwal, K Makker, R Sharma. Clinical relevance of oxidative stress in male factor infertility. Am J Reprod Immunol 59, 2-11 (2008)
54. L Söderquist, H Rodriguez-Martinez, L Janson. Postthaw motility, ATP content and cytochrome C oxidase activity of A.I. bull spermatozoa in relation to fertility. Zentralbl Veterinarmed A 38, 165-174 (1991)
55. RD Leandri, E Dulious, P Jouannet, M De Almeida. Deficit in cytochrome c oxidase activity induced in rat sperm mitochondria by in vivo exposure to zidovidine. Int J Androl 26, 305-309 (2003)
56. RJ Aitken, JK Findlay, KJ Hutt and JB Kerr. Apoptosis in the germ line. Reproduction 141, 139-150 (2011)
57. Kimura M, Itoh N, Takagi S, Sasao T, Takahashi A, Masumori N, Tsukamoto T. Balance of apoptosis and proliferation of germ cells related to spermatogenesis in aged men. J Androl 24, 185-191 (2003)
58. I Sasagawa, S Matsuki, Y Suzuki, Y Iuchi, K Tohya, M Kimura, T Nakada, J Fujii. Possible involvement of the membrane-bound form of peroxiredoxin 4 in acrosome formation during spermiogenesis of rats. Eur J Biochem 268, 3053-3061 (2001)
59. M Fujisawa, C Hiramine, H Tanaka, H Okada, S Arakawa, S Kamidono. Decrease in apoptosis of germ cells in the testes of infertile men with varicocele. World J Urol 17, 296-300 (1999)
60. J Tesarik, F Martinez, L Rienzi, M Iacobelli, F Ubaldi, C Mendoza, E Greco. In-vitro effects of FSH and testosterone withdrawal on caspase activation and DNA fragmentation in different cell types of human seminiferous epithelium. Hum Reprod 17, 1811-1819 (2002)
61. J Lee, JH Richburg, SC Younkin, K Boekelheide. The Fas system is a key regulator of germ cells apoptosis in the testis. Endocrinology 138, 2081-2088 (1997)
62. CH Lee, YH Cho. Aspects of mammalian spermatogenesis: electrophoretical analysis of protamines in mammalian species. Mol Cells 31, 556-559 (1999)
63. V Pentikäinen, K Erkkilä, L Dunkel. Fas regulates germ cell apoptosis in human testis in vitro. Am J Physiol 276, 310-316 (1999)
64. JH Richburg. The relevance of spontaneous and chemically-induced alterations in testicular germ cell apoptosis to toxicology. Toxicol Lett 112, 79-86 (2000)
65. Aziz N, Said T, Paasch U, Agarwal A. The relationship between human sperm apoptosis, morphology and the sperm deformity index. Hum Reprod 22, 1413-1419 (2007)
66. JM Bedford. The status and the state of the human epididymis. Hum Reprod 9, 2187-2199 (1994)
67. G Huszar, P Patrizio, L Vigue, M Willets, C Wilker, D Adhoot, L Johnson. Cytoplasmic extrusion and the switch from creatine kinase B to M isoform are completed by the commencement of epididymal transport in human and stallion spermatozoa. J Androl 19, 11-20 (1998)
68. GJ Oosterhuis, I Vermes. Apoptosis in human ejaculated spermatozoa. J Biol Regul Homeost Agents 18, 115-119 (2004)
69. J Majar, M Thomas, L Bezrukov, A Chanturia, G Pekkurnaz, S Yin, SA Kuznetsov, PG Robey, J Zmmerberg. Cytotoxicity mediated by the Fas ligand (FasL)-activated apoptotic pathway in stem cells. J Biol chem 284, 22022-22028 (2009)
70. G Ji, A Gu, F Hu, S Wang, J Liang, Y Xia, C Lu, L Song, G Fu, Wang X. Polymorphisms in cell death pathway genes are associated with altered sperm apoptosis and poor semen quality. Hum Reprod 24, 2439-2446 (2009)
71. KK Shukla, V Mishra, AA Mahdi, SN Shankhwar, R Singh, D Patel, M Das. Withania somnifera improves semen quality combating oxidative stress, cell death and improving essential metal levels. Reprod Bio Med Online 5th feb, (2011)
72. EC Roosen- Runge. Germinal-cell loss in normal metazoan spermatogenesis. J Reprod Fertil 35, 339-348 (1973)
73. X Wang, RK Sharma, SC Sikka AJ Thomas, T Jr Falcone, A Agarwal. "Oxidative stress is associated with increased apoptosis leading to spermatozoa DNA damage in patients with male factor infertility". Fertil Steril 80, 531-535 (2003)
74. Q Xu, HY Lin, SD Yeh, IC Yu, RS Wang, YT Chen, C Zhang, S Altuwaijri, LM Chen, KH Chuang, HS Chiang, S Yeh, C Chang. Infertility with defective spermatogenesis and steroidogensis in male lacking androgen receptor in Leydig cells. Endocrine 32, 96-106 (2007)
75. L Samanta, A Sahoo, GB Chainy. Age related changes in rat testicular oxidative stress parameters by hexachlorocyclohexane. Arch Toxicol 73, 96-107 (1999)
76. V Serre, B Robaire. Segment-specific morphological changes in aging brown Norway rat epididymis. Biol Reprod 58, 497-513 (1998)
77. S Levy, B Robaire.Segment- specific changes with age in the expression of junctional proteins and the permeability of the blood-epididymis barrier in rats. Biol Reprod 60, 1392-1401 (1999)
78. KM Jervis, B Robaire. Changes in gene expression during in the Brown Norway rat epididymis. Exp Gerontol 37, 897-906 (2002)
79. RS Viger, B Robaire. Gene expression in the aging brown Norway rat epididymis. J Androl 16, 108-117 (1995)
80. A Colin, G Barroso, N Gómez-López, EH Duran, S Oehninger. The effect of age on the expression of apoptosis biomarkers human spermatozoa. Fertil Steril 94, 2609-2614 (2010)
81. RJ Aitken, JK Findlay, KJ Hutt and JB Kerr. Apoptosis in the germ line. Reproduction 141, 139-150 (2011)
82. J Tesarik, E Greco, P Cohen-Bacrie, C Mendoza. Germ cell apoptosis in men with complete and incomplete spermiogenesis failure. Mol Hum Reprod 4, 757-762 (1998)
83. C Zuying, H Russ, MT Alexander, LS Jain, JD David, GB Linda and PS Narendra. The Relationship between Human Semen Characteristics and Sperm Apoptosis: A Pilot Study. J Androl 27, 112-120 (2006)
84. N Bissonnette, B Wasylyk, DJ Hunting. The apoptotic and transcriptional transactivation activities of p53 can be dissociated. Biochem Cell Biol 75, 351-358 (1997)
85. HM Shen, J Dai, SE Chia, A Lim, CN Ong. Detection of apoptotic alterations in sperm in sub fertile patients and their correlations with sperm quality. Hum Reprod 17, 1266-1273 (2002)
86. RA Saleh, A Agarwal. Oxidative stress and male infertility: from research bench to clinical practice. J Androl 23, 737-752 (2002)
87. RJ Aitken. The Amoroso Lecture. The human spermatozoon-a cell in crisis? J Reprod fertile 115, 1-7 (1999)
88. GC Manicardi, A Tombacco, D Bizzaro, U Bianchi, PG Bianchi, D Sakkas. DNA strand break in ejaculated human spermatozoa: comparison of suscepatibility to the nic translation and terminal tranferase assays. Histochem J 30, 33-39 (1998)
89. A Zini, K Kamal, D Phang, J Willis, K Jarvi. Biologic variability of sperm DNA denaturation in infertile men. Urology 58, 258-261 (2001)
90. G Barroso, M Morshedi, S Oehninger. Analysis of DNA fragmentation, plasma membrane translocation of phosphatidylserine and oxidative stress in human spermatozoa. Hum Reprod 15, 1338-1344 (2000)
91. S Han-Ming, HM Shen, SE Chia, A Lim and CN Ong. Detection of apoptotic alterations in sperm in sub-fertile patients and their correlations with sperm quality. Hum Reprod 17, 1266-1273 (2002)