Proliferation and Apoptosis in Aged and Photoregressed Mammalian Seminiferous Epithelium, with Particular Attention to Rodents and Humans

Reproduction in Domestic Animals

Volumn 46, Issue 1, 2011, Pages 155-164

  Pastor, Luis Miguel ^a   Zuasti, A ^a   Ferrer, C ^a   Bernal Manas C M ^a   Morales, E ^a   Beltran Frutos E ^a   Seco Rovira, V ^a  

^a UNIVERSITY OF MURCIA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

MAMMALIA; RODENTIA;

EID: 78751492533     PISSN: 09366768     EISSN: 14390531     Source Type: Journal    
DOI: 10.1111/j.1439-0531.2009.01573.x     Document Type: Review

References (78)

1. Bakalska M, Atanassova N, Koeva Y, Nikolov B, Davidoff M, 2004: Induction of male germ cell apoptosis by testosterone withdrawal after ethane dimethanesulfonate treatment in adult rats. Endocr Regul 38, 103-110.
2. Barnes CJ, Covington BW 4th, Cameron IL, Lee M, 1998: Effect of aging on spontaneous and induced mouse testicular germ cell apoptosis. Aging (Milano) 10, 497-501.
3. Barnes CJ, Covington BW 4th, Lee M, 1999: Effect of aging and dietary restriction on rat testicular germ cell apoptosis. J Gerontol A Biol Sci Med Sci 54, B199-B204.
4. Bernal-Mañas CM, Morales E, Ferrer C, Zuasti A, Canteras M, Pastor LM, 2005: Effect of aging on proliferation of the seminiferous epithelium of hamster (Mesocricetus auratus). Histol Histopathol Sp1, S97.
5. Bernal-Mañas CM, Morales E, Ferrer C, Zuasti A, Beltrán E, Canteras M, Pastor LM, 2006: Relation of apoptosis with seminiferous tubular degeneration in hamster aging (Mesocricetus auratus). Reprod Domest Anim 41, 111.
6. Beumer TL, Roepers-Gajadien HL, Gademan IS, Van Buul PP, Gil-Gomez G, Rutgers DH, De Rooij DG, 1998: The role of the tumor suppressor p53 in spermatogenesis. Cell Death Differ 5, 669-677.
7. Beumer TL, Roepers-Gajadien HL, Gademan IS, Lock TM, Kal HB, De Rooij DG, 2000: Apoptosis regulation in the testis: involvement of Bcl-2 family members. Mol Reprod Dev 56, 353-359.
8. Blanco Rodríguez J, Martínez García C, 1997: Apoptosis pattern elicited by oestradiol treatment of the seminiferous epithelium of the adult rat. J Reprod Fertil 110, 61-70.
9. Blanco-Rodríguez J, Martínez-García C, 1996: Induction of apoptotic cell death in the seminiferous tubule of the adult rat testis: assessment of the germ cell types that exhibit the ability to enter apoptosis after hormone suppression by oestrodiol treatment. Int J Androl 19, 237-247.
10. Blottner S, Roelants H, Wagener A, Wenzel UD, 1999: Testicular mitosis, meiosis and apoptosis in mink (Mustela vison) during breeding and non-breeding seasons. Anim Reprod Sci 57, 237-249.
11. Blottner S, Schön J, Roelants H, 2007: Apoptosis is not the cause of seasonal testicular involution in roe deer. Cell Tissue Res 327, 615-624.
12. Boekelheide K, 2005: Mechanisms of toxic damage to spermatogenesis. J Natl Cancer Inst Monogr 34, 6-8.
13. Brinkworth MH, Weinbauer GF, Bergmann M, Nieschlag E, 1997: Apoptosis as a mechanism of germ cell loss in elderly men. Int J Androl 20, 222-228.
14. Cai L, Hales BF, Robaire B, 1997: Induction of apoptosis in the germ cells of adult male rats after exposure to cyclophosphamide. Biol Reprod 56, 1490-1497.
15. Calvo A, Bustos-Obregon E, Pastor LM, 1997: Morphological and histochemical changes in the epididymis of hamsters (Mesocricetus auratus) subjected to short photoperiod. J Anat 191, 77-88.
16. Calvo A, Pastor LM, Martínez E, Vázquez JM, Roca J, 1999: Age-related changes in the hamster epididymis. Anat Rec 256, 335-346.
17. Chaki SP, Misro MM, Gautam DK, Kaushik M, Ghosh D, Chainy GB, 2006: Estradiol treatment induces testicular oxidative stress and germ cell apoptosis in rats. Apoptosis 11, 1427-1437.
18. De Kretser DM, Kerr JB, 1994: The Cytology of the Testis. The Physiology of Reproduction. Raven Press, New York, 1177-1290 Vol. 1.
19. De Rooij DG, Lok D, Weenk D, 1985: Feedback regulation of the proliferation of the undifferentiated spermatogonia in the Chinese hamster by the differentiating spermatogonia. Cell Tissue Kinet 18, 71-81.
20. Desjardins C, Ewing LL, Johnson BH, 1971: Effect of light deprivation upon the apermatogenic and steroidogenic elements of hamster testes. Endocrinology 89, 791-800.
21. Francavilla S, D'Abrizio P, Cordeschi G, Pelliccione F, Necozione S, Ulisse S, Properzi G, Francavilla F, 2002: Fas expression correlates with human germ cell degeneration in meiotic and post-meiotic arrest of spermatogenesis. Mol Hum Reprod 8, 213-220.
22. Furuchi T, Masuko K, Nishimune Y, Obinata M, Matsui Y, 1996: Inhibition of testicular germ cell apoptosis and differentiation in mice misexpressing Bcl-2 in spermatogonia. Development 122, 1703-1709.
23. Furuta I, Porkka-Heiskanen T, Scarbrough K, Tapanainen J, Turek FW, Hsueh AJ, 1994: Photoperiod regulates testis cell apoptosis in Djungarian hamsters. Biol Reprod 51, 1315-1321.
24. Gündüz B, Karakas A, Terzi H, Oner J, Serin E, Kükner A, 2009: The effect of pinealectomy and leptin hormone on the proliferation and apoptosis activation in Syrian hamster testis in different photoperiods. Int J Androl 32, 343-352.
25. Hikim AP, Vera Y, Vernet D, Castanares M, Díaz-Romero M, Ferrini M, Swerdloff RS, González-Cadavid NF, Wang C, 2005: Involvement of nitric oxide-mediated intrínsic pathway signaling in age-related increase in germ cell apoptosis in male Brown-Norway rats. J Gerontol A Biol Sci Med Sci 60, 702-708.
26. Horn R, Pastor LM, Moreno E, Calvo A, Canteras M, Pallares J, 1996: Morphological and morphometric study of early changes in the ageing golden hamster testis. J Anat 188, 109-117.
27. Huckins C, 1978: The morphology and kinetics of spermatogonial degeneration in normal adult rats: an analysis using a simplified classification of the germinal epithelium. Anat Rec 190, 905-926.
28. L protein characterise testicular regression in American crows (Corvus brachyrhynchos). Reprod Fertil Dev 19, 461-469.
29. Johnson L, Nguyen HB, Petty CS, Neaves WB, 1987: Quantification of human spermatogenesis: germ cell degeneration during spermatocytogenesis and meiosis in testes from younger and older adult men. Biol Reprod 37, 739-747.
30. Kimura M, Itoh N, Takagi S, Sasao T, Takahashi A, Masumori N, Tsukamoto T, 2003: Balance of apoptosis and proliferation of germ cells related to spermatogenesis in aged men. J Androl 24, 185-191.
31. Lee J, Richburg JH, Younkin SC, Boekelheide K, 1997: The Fas system is a key regulator of germ cell apoptosis in the testis. Endocrinology 138, 2081-2088.
32. Lincoln GA, Almeida OF, Arendt J, 1981: Role of melatonin and circadian rhythms in seasonal reproduction in rams. J Reprod Fertil Suppl 30, 23-31.
33. Liu G, Gong P, Bernstein LR, Bi Y, Gong S, Cai L, 2007: Apoptotic cell death induced by low-dose radiation in male germ cells: hormesis and adaptation. Crit Rev Toxicol 37, 587-605.
34. Loveland KL, Schlatt S, 1997: Stem cell factor and c-kit in the mammalian testis: lessons originating from Mother Nature's gene knockouts. J Endocrinol 153, 337-344.
35. Meistrich ML, 1993: Effects of chemotherapy and radiotherapy on spermatogenesis. Eur J Urol 23, 136-141.
36. Meistrich ML, Shetty G, 2003: Inhibition of spermatogonial differentiation by testosterone. J Androl 24, 135-148.
37. Mizuno K, Hayashi Y, Kojima Y, Nakane A, Tozawa K, Kohri K, 2009: Activation of NF-kappaB associated with germ cell apoptosis in testes of experimentally induced cryptorchid rat model. Urology 73, 389-393.
38. Morales E, 2004: Efecto del envejecimiento y de la exposición a fotoperiodo corto en el epitelio seminífero del hámster (Mesocricetus auratus): Proliferación y apoptosis. Vías moleculares de la apoptosis. Doctoral Thesis. University of Murcia, Murcia.
39. Morales E, Pastor LM, Ferrer C, Zuasti A, Pallares J, Horn R, Calvo A, Santamaría L, Canteras M, 2002: Proliferation and apoptosis in the seminiferous epithelium of photoinhibited Syrian hamsters (Mesocricetus auratus). Int J Androl 25, 281-287.
40. Morales E, Pastor LM, Horn R, Zuasti A, Ferrer C, Calvo A, Santamaria L, Canteras M, 2003: Effect of ageing on the proliferation and apoptosis of testicular germ cells in the Syrian hamster (Mesocricetus auratus). Reprod Fertil Dev 15, 89-98.
41. Morales E, Horn R, Pastor LM, Santamaria L, Pallares J, Zuasti A, Ferrer C, Canteras M, 2004: Involution of seminiferous tubules in aged hamsters: an ultrastructural, immunohistochemical and quantitative morphological study. Histol Histopathol 19, 445-455.
42. Morales E, Ferrer C, Zuasti A, García-Borrón JC, Canteras M, Pastor LM, 2007: Apoptosis and molecular pathways in the seminiferous epithelium of aged and photoinhibited Syrian Hamsters (Mesocricetus auratus). J Androl 28, 123-135.
43. Nandi S, Banerjee PP, Zirkin BR, 1999: Germ cell apoptosis in the testes of Sprague Dawley rats following testosterone withdrawal by ethane 1, 2-dimethanesulfonate administration: relationship to Fas? Biol Reprod 61, 70-75.
44. Nascimento HF, Drumond AL, Franca LR, Chiarini-García H, 2009: Spermatogonial morphology, kinetics and niches in hamsters exposed to short- and long-photoperiod. Int J Androl 32, 486-497.
45. Nipken C, Wrobel KH, 1997: A quantitative morphological study of age-related changes in the donkey testis in the period between puberty and senium. Andrología 29, 149-161.
46. Nistal M, Codesal J, Paniagua R, Santamaría L, 1987: Decrease in the number of human Ap and Ad spermatogonia and in the Ap/Ad ratio with advancing age. New data on the spermatogonial stem cell. J Androl 8, 64-68.
47. Obregon EB, Ramírez O, 1997: Ageing and testicular function in Octodon degus. Andrología 29, 319-326.
48. Ohta Y, Nishikawa A, Fukazawa Y, Urushitani H, Matsuzawa A, Nishina Y, Iguchi I, 1996: Apoptosis in adult mouse testis induced by experimental cryptorchidism. Acta Anat (Basel) 157, 195-204.
49. Oldereid NB, Angelis PD, Wiger R, Clausen OP, 2001: Expression of Bcl-2 family proteins and spontaneous apoptosis in normal human testis. Mol Hum Reprod 7, 403-408.
50. Pastor LM, Morales E, Zuasti A, Ferrer C, Pallarés J, Cos M, Calvo A, 2001: Cellular proliferation and apoptosis in the seminiferous epithelium of hamster (Mesocricetus auratus) subjected to short photoperiod. In: Universitat de Barcelona (ed), Microscopy. Universitat de Barcelona, Barcelona, pp. 186-187.
51. Paul C, Teng S, Saunders PT, 2009: A single, mild, transient scrotal heat stress causes hypoxia and oxidative stress in mouse testes, which induces germ cell death. Biol Reprod 80, 913-919.
52. Riou L, Bastos H, Lassalle B, Coureuil M, Testart J, Boussin FD, Allemand I, Fouchet P, 2005: The telomerase activity of adult mouse testis resides in the spermatogonial alpha6-integrin-positive side population enriched in germinal stem cells. Endocrinology 146, 3926-3932.
53. Roelants H, Schneider F, Göritz F, Streich J, Blottner S, 2002: Seasonal changes of spermatogonial proliferation in roe deer, demonstrated by flow cytometric analysis of c-kit receptor, in relation to follicle-stimulating hormone, luteinizing hormone and testosterone. Biol Reprod 66, 305-312.
54. Ryu BY, Orwig KE, Oatley JM, Avarbock MR, Brinster RL, 2006: Effects of aging and niche microenvironment on spermatogonial stem cell self-renewal. Stem Cells 24, 1505-1511.
55. Salama M, Tsuji M, Tamura M, Kagawa S, 1998: Impact of aging and diabetes mellitus on the expresión of the proliferating cell nuclear antigen in rat testicular tissue. Arch Androl 40, 95-107.
56. Sasso-Cerri E, Cerri PS, Freymüller E, Miraglia SM, 2006: Apoptosis during the seasonal spermatogenic cycle of Rana catesbeiana. J Anat 209, 21-29.
57. Sato T, Tachiwana T, Takata K, Tay TW, Ishii M, Nakamura R, Kimura S, Kanai Y, Kurohmaru M, Hayashi Y, 2005: Testicular dynamics in Syrian hamsters exposed to both short photoperiod and low ambient temperature. Anat Histol Embryol 34, 220-224.
58. Schlatt S, Weinbauer GF, 1994: Immunohistochemical localization of proliferating cell nuclear antigen as a tool to study cell proliferation in rodent and primate testes. Int J Androl 17, 214-222.
59. Schoenfeld HA, Hall SJ, Boekelheide K, 2001: Continuously proliferative stem germ cells partially repopulate the aged, atrophic rat testis after gonadotropin-releasing hormone agonist therapy. Biol Reprod 64, 1273-1282.
60. Sihna Hikim AP, Bartke A, Russell LD, 1988: The seasonal breeding hamster as a model to study structure-function relationships in the testis. Tissue Cell 20, 63-78.
61. Stephan H, Polzar B, Rauch F, Zanotti S, Ulke C, Mannherz HG, 1996: Distribution of deoxyribonuclease I (DNase I) and p53 in rat testis and their correlation with apoptosis. Histochem Cell Biol 106, 383-393.
62. Strbenc M, Fazarinc G, Bavdek SV, Pogacnik A, 2003: Apoptosis and proliferation during seasonal testis regression in the brown hare (Lepus europaeus L). Anat Histol Embryol 32, 48-53.
63. Tanemura K, Kanai Y, Kanai-Azuma M, Kurohmaru M, Kuramoto K, Yazaki K, Hayashi Y, 1996: Reinitiation of spermatogonial mitotic differentiation in inactive old BDF1 mouse seminiferous tubules transplanted to W/Wv mouse testis. Biol Reprod 55, 1237-1242.
64. Tiba T, Takahashi M, Igura M, Kita I, 1992: Enhanced proliferation of undifferentiated spermatogonia after treatment of short photoperiod exposure in the Syrian hamster (Mesocricetus auratus). Anat Histol Embryol 21, 9-22.
65. Turner TT, Tung KS, Tomomosa H, Wilson LW, 1997: Acute testicular ischemia results in germ cell-specific apoptosis in the rat. Biol Reprod 57, 1267-1274.
66. Turner TT, Bang HJ, Lysiak JL, 2004: The molecular pathology of experimental testicular torsion suggests adjunct therapy to surgical repair. J Urol 172, 2574-2578.
67. Vigodner M, Lewin LM, Shochat L, Golan R, 2001: Spermatogenesis in the golden hamster: the role of c-kit. Mol Reprod Dev 60, 562-568.
68. Wang C, Sinha Hikim AP, Lue Y, Leung A, Baravarian S, Swerdloff RS, 1999: Reproductive aging in the Brown Norway rat is characterized by accelerated germ cell apoptosis and is not altered by luteinizing hormone replacement. J Androl 20, 509-518.
69. Wine RN, Ku WW, Li LH, Chapin RE, 1997: Cyclophilin A is present in rat germ cells and is associated with spermatocyte apoptosis Reproductive Toxicology Group. Biol Reprod 56, 439-446.
70. Woolveridge I, De Boer-Brouwer M, Taylor MF, Teerds KJ, Wu FC, Morris ID, 1999: Apoptosis in the rat spermatogenic epithelium following androgen withdrawal: changes in apoptosis-related genes. Biol Reprod 60, 461-470.
71. Wright WW, Fiore C, Zirkin BR, 1993: The effect of aging on the seminiferous epithelium of the brown Norway rat. J Androl 14, 110-117.
72. Yin Y, Hawkins KL, De Wolf WC, Morgentaler AJ, 1997: Heat stress causes testicular germ cell apoptosis in adult mice. J Androl 18, 159-165.
73. Young KA, Nelson RJ, 2001: Mediation of seasonal testicular regression by apoptosis. Reproduction 122, 677-685.
74. Young KA, Zirkin BR, Nelson RJ, 1999: Short photoperiods evoke testicular apoptosis in white-footed mice (Peromyscus leucopus). Endocrinology 140, 3133-3139.
75. Young KA, Zirkin BR, Nelson RJ, 2000: Testicular regression in response to food restriction and short photoperiod in white-footed mice (Peromyscus leucopus) is mediated by apoptosis. Biol Reprod 62, 347-354.
76. Young KA, Ball GF, Nelson RJ, 2001: Photoperiod-induced testicular apoptosis in European starlings (Sturnus vulgaris). Biol Reprod 64, 706-713.
77. Zhang X, Ebata KT, Robaire B, Nagano MC, 2006: Aging of male germ line stem cells in mice. Biol Reprod 74, 119-124.
78. Zhang L, Han XK, QI YY, Liu Y, Chen QS, 2008: Seasonal effects on apoptosis and proliferation of germ cells in the testes of the Chinese soft-shelled turtle Pelodiscus sinensis. Theriogenology 69, 1148-1158.