The apoptotic function analysis of p53, Apaf1, Caspase3 and Caspase7 during the spermatogenesis of the Chinese fire-bellied nNewt Cynops orientalis

PLoS ONE

Volumn 7, Issue 6, 2012, Pages

  Wang, Da Hui ^a   Hu, Jian Rao ^b   Wang, Li Ya ^c   Hu, Yan Jun ^c   Tan, Fu Qing ^d   Zhou, Hong ^a   Shao, Jian Zhong ^a   Yang, Wan Xi ^a  

^a ZHEJIANG UNIVERSITY   (China)

^b HANGZHOU NORMAL UNIVERSITY   (China)

^c Zhejiang University School of Medicine   (China)

^d ZHEJIANG UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

APOPTOTIC PROTEASE ACTIVATING FACTOR 1; CADMIUM; CASPASE 3; CASPASE 7; CASPASE 8; CASPASE 9; PROTEIN P53;

ANIMAL TISSUE; APAF1 GENE; APOPTOSIS; ARTICLE; CASPASE3 GENE; CASPASE7 GENE; COLD EXPOSURE; CONTROLLED STUDY; CYNOPS ORIENTALIS; ENZYME ACTIVITY; GENE; GENE EXPRESSION; GERM CELL; HEAT SHOCK; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN FUNCTION; SALAMANDRIDAE; SPERM; SPERMATID; SPERMATOGENESIS; STARVATION; TESTIS; TUMOR SUPPRESSOR GENE;

AMINO ACID SEQUENCE; ANIMALS; APOPTOSIS; APOPTOTIC PROTEASE-ACTIVATING FACTOR 1; BASE SEQUENCE; CADMIUM; CASPASE 3; CASPASE 7; CHINA; DNA, COMPLEMENTARY; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; IN SITU NICK-END LABELING; MALE; MODELS, BIOLOGICAL; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; SALAMANDRIDAE; SEQUENCE ALIGNMENT; SPERMATOGENESIS; SPERMATOZOA; STRESS, PHYSIOLOGICAL; TESTIS; TUMOR SUPPRESSOR PROTEIN P53;

AMPHIBIA; CYNOPS ORIENTALIS; MAMMALIA; SALAMANDRIDAE;

EID: 84863092396     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0039920     Document Type: Article

References (148)

1. Lockshin RA, Williams CM, (1964) Programmed cell death II. Endocrine potentiation of the breakdown of the intersegmental muscles of silkmoths. J Insect Physiol 10: 643.
2. Sinha Hikim AP, Swerdloff RS, (1999) Hormonal and genetic control of germ cell apoptosis in the testis. Rev Reprod 4: 38-47.
3. Sinha Hikim AP, Wang C, Lue Y, Johnson L, Wang XH, et al. (1998) Spontaneous germ cell apoptosis in humans: evidence for ethnic differences in the susceptibility of germ cells to programmed cell death. J Clin Endocrinol Metab 83: 152-156.
4. Sinha Hikim AP, Wang C, Leung A, Swerdloff RS, (1995) Involvement of apoptosis in the induction of germ cell degeneration in adult rats after gonadotropin-releasing hormone antagonist treatment. Endocrinology 136: 2770-2775.
5. Brinkworth MH, Weinbauer GF, Schlatt S, Nieschlag E, (1995) Identification of male germ cells undergoing apoptosis in adult rats. J Reprod Fertil 105: 25-33.
6. Henriksen K, Hakovirta H, Parvinen M, (1995) Testosterone inhibits and induces apoptosis in rat seminiferous tubules in a stage-specific manner: in situ quantification in squash preparations after administration of ethane dimethane sulfonate. Endocrinology 136: 3285-3291.
7. Sinha Hikim AP, Rajavashisth TB, Sinha Hikim I, Lue Y, Bonavera JJ, et al. (1997) Significance of apoptosis in the temporal and stage-specific loss of germ cells in the adult rat after gonadotropin deprivation. Biol Reprod 57: 1193-1201.
8. Lue Y, Hikim AP, Wang C, Bonavera JJ, Baravarian S, et al. (1997) Early effects of vasectomy on testicular structure and on germ cell and macrophage apoptosis in the hamster. J Androl 18: 166-173.
9. Sinha Hikim AP, Lue Y, Diaz-Romero M, Yen PH, Wang C, et al. (2003) Deciphering the pathways of germ cell apoptosis in the testis. J Steroid Biochem Mol Biol 85: 175-182.
10. Lue Y, Sinha Hikim AP, Wang C, Im M, Leung A, et al. (2000) Testicular heat exposure enhances the suppression of spermatogenesis by testosterone in rats: the "two-hit" approach to male contraceptive development. Endocrinology 141: 1414-1424.
11. Lue YH, Hikim AP, Swerdloff RS, Im P, Taing KS, et al. (1999) Single exposure to heat induces stage-specific germ cell apoptosis in rats: role of intratesticular testosterone on stage specificity. Endocrinology 140: 1709-1717.
12. Beumer TL, Roepers-Gajadien HL, Gademan LS, Rutgers DH, de Rooij DG, (1997) P21 (Cip1/WAF1) expression in the mouse testis before and after X irradiation. Mol Reprod Dev 47: 240-247.
13. Knudson CM, Tung KSK, Tourtellotte WG, Brown GAJ, Korsmeyer SJ, (1995) Bax-deficient mice with lymphoid hyperplasia and male germ cell death. Science 270: 96-99.
14. 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.
15. Packer AI, Besmer P, Bachvarova RF, (1995) Kit ligand mediates survival of type A spermatogonia and dividing spermatocytes in postnatal mouse testes. Mol Reprod Dev 42: 303-310.
16. Nowicki A, Szenajch J, Ostrowska G, Wojtowicz A, Wojtowicz K, et al. (1996) Impaired tumor growth in colony-stimulating factor 1 (CSF-1)-deficient, macrophage-deficient op/op mouse: evidence for a role of CSF-1-dependent macrophages in formation of tumor stroma. Int J Cancer 65: 112-119.
17. Richburg JH, (2000) The relevance of spontaneous- and chemically-induced alterations in testicular germ cell apoptosis to toxicology. Toxicol Lett 112-113: 79-86.
18. Gosden R, Spears N, (1997) Programmed cell death in the reproductive system. Br Med Bull 53: 644-661.
19. de Rooij DG, Grootegoed JA, (1998) Spermatogonial stem cells. Curr Opin Cell Biol 10: 694-701.
20. Matsui Y, (1998) Regulation of germ cell death in mammalian gonads. APMIS 106: 142-147.
21. Xu G, Vogel KS, McMahan CA, Herbert DC, Walter CA, (2010) BAX and tumor suppressor TRP53 are important in regulating mutagenesis in spermatogenic cells in mice. Biol Reprod 83: 979-987.
22. Ohta H, Aizawa S, Nishimune Y, (2003) Functional analysis of the p53 gene in apoptosis induced by heat stress or loss of stem cell factor signaling in mouse male germ cells. Biol Reprod 68: 2249-2254.
23. Coureuil M, Fouchet P, Prat M, Letallec B, Barroca V, et al. (2006) Caspase-independent death of meiotic and postmeiotic cells overexpressing p53: calpain involvement. Cell Death Differ 13: 1927-1937.
24. Zou H, Henzel WJ, Liu X, Lutschg A, Wang X, (1997) Apaf-1, a human protein homologous to C. elegans CED-4, participates in cytochrome c-dependent activation of caspase-3. Cell 90: 405-413.
25. Fadeel B, Ottosson A, Pervaiz S, (2008) Big wheel keeps on turning: apoptosome regulation and its role in chemoresistance. Cell Death Differ 15: 443-452.
26. Park HH, Lo YC, Lin SC, Wang L, Yang JK, et al. (2007) The death domain superfamily in intracellular signaling of apoptosis and inflammation. Annu Rev Immunol 25: 561-586.
27. Print CG, Loveland KL, (2000) Germ cell suicide: new insights into apoptosis during spermatogenesis. Bioessays 22: 423-430.
28. Rodriguez I, Ody C, Araki K, Garcia I, Vassalli P, (1997) An early and massive wave of germinal cell apoptosis is required for the development of functional spermatogenesis. EMBO J 16: 2262-2270.
29. Krajewski S, Krajewska M, Shabaik A, Miyashita T, Wang HG, et al. (1994) Immunohistochemical determination of in vivo distribution of Bax, a dominant inhibitor of Bcl-2. Am J Pathol 145: 1323-1336.
30. Russell LD, Chiarini-Garcia H, Korsmeyer SJ, Knudson CM, (2002) Bax-dependent spermatogonia apoptosis is required for testicular development and spermatogenesis. Biol Reprod 66: 950-958.
31. Yin Y, Stahl BC, DeWolf WC, Morgentaler A, (2002) P53 and Fas are sequential mechanisms of testicular germ cell apoptosis. J Androl 23: 64-70.
32. 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.
33. McClure RF, Heppelmann CJ, Paya CV, (1999) Constitutive Fas ligand gene transcription in Sertoli cells is regulated by Sp1. J Biol Chem 274: 7756-7762.
34. Young KA, Zirkin BR, Nelson RJ, (1999) Short photoperiods evoke testicular apoptosis in white-footed mice (Peromyscus leucopus). Endocrinology 140: 3133-3139.
35. 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.
36. Lee J, Richburg JH, Shipp EB, Meistrich ML, Boekelheide K, (1999) The Fas system, a regulator of testicular germ cell apoptosis, is differentially up-regulated in Sertoli cell versus germ cell injury of the testis. Endocrinology 140: 852-858.
37. Polager S, Ginsberg D, (2009) p53 and E2f partners in life and death. Nat Rev Cancer 9: 738-748.
38. Hamroun D, Kato S, Ishioka C, Claustres M, Béroud C, et al. (2006) The UMD TP53 database and website: update and revisions. Hum Mutat 27: 14-20.
39. Beumer TL, Roepers-Gajadien HL, Gademan IS, van Buul PP, Gil-Gomez G, et al. (1998) The role of the tumor suppressor p53 in spermatogenesis. Cell Death Differ 5: 669-677.
40. Hasegawa M, Zhang Y, Niibe H, Terry N, Meistrich M, (1998) Resistance of differentiating spermatogonia to radiation-induced apoptosis and loss in p53-deficient mice. Radiat Res 149: 263-270.
41. Allemand I, Anglo A, Jeantet AY, Cerutti I, May E, (1999) Testicular wild-type p53 expression in transgenic mice induces spermiogenesis alterations ranging from differentiation defects to apoptosis. Oncogene 18: 6521-6530.
42. Vousden KH, Prives C, (2009) Blinded by the light: the growing complexity of p53. Cell 137: 413-431.
43. Laptenko O, Prives C, (2006) Transcriptional regulation by p53: one protein, many possibilities. Cell Death Differ 13: 951-961.
44. Speidel D, (2009) Transcription-independent p53 apoptosis: an alternative route to death. Trends Cell Biol 20: 14-24.
45. Yin Y, DeWolf WC, Morgentaler A, (1998) Experimental cryptorchidism induces testicular germ cell apoptosis by p53-dependent and -independent pathways in mice. Biol Reprod 58: 492-496.
46. Yin Y, Stahl BC, DeWolf WC, Morgentaler A, (1998) p53-mediated germ cell quality control in spermatogenesis. Dev Biol 204: 165-171.
47. Ricote M, Alfaro JM, García-Tuñón I, Arenas MI, Fraile B, et al. (2002) Control of the annual testicular cycle of the marbled-newt by p53, p21, and Rb gene products. Mol Reprod Dev 63: 202-209.
48. Yazawa T, Nakayama Y, Fujimoto K, Matsuda Y, Abe K, et al. (2003) Abnormal spermatogenesis at low temperatures in the Japanese red-bellied newt, Cynops pyrrhogaster: possible biological significance of the cessation of spermatocytogenesis. Mol Reprod Dev 66: 60-66.
49. Yazawa T, Fujimoto K, Yamamoto T, Abé SI, (2001) Caspase activity in newt spermatogonial apoptosis induced by prolactin and cycloheximide. Mol Reprod Dev 59: 209-214.
50. Yazawa T, Yamamoto K, Kikuyama S, Abé SI, (1999) Elevation of plasma prolactin concentrations by low temperature is the cause of spermatogonial cell death in the newt, Cynops pyrrhogaster. Gen Comp Endocrinol 103: 302-311.
51. Yazawa T, Yamamoto T, Abé SI, (2000) Prolactin induces apoptosis in the penultimate spermatogonial stage of the testes in Japanese red-bellied newt (Cynops pyrrhogaster). Endocrinology 141: 2027-2032.
52. Abé SI, Ji ZS, (1994) Initiation and stimulation of spermatogenesis in vitro by mammalian follicle-stimulating hormone in the Japanese newt, Cynops pyrrhogaster. Int J Dev Biol 38: 201-208.
53. Yazawa T, Yamamoto T, Kubokawa K, Nakayama Y, Fujimoto K, et al. (2001) Cold suppression of follicle-stimulating hormone activity on proliferation and survival of newt spermatogonia. Gen Comp Endocrinol. 122: 296-303.
54. Kim MS, Kim BJ, Woo HN, Kim KW, Kim KB, et al. (2000) Cadmium induces caspase-mediated cell death: suppression by Bcl-2. Toxicology 145: 27-37.
55. Roy A, Kucukural A, Zhang Y, (2010) I-TASSER: a unified platform for automated protein structure and function prediction. Nat Protoc 5: 725-738.
56. Roy A, Xu D, Poisson J, Zhang Y, (2011) A protocol for computer-based protein structure and function prediction. J Vis Exp 3: e3259.
57. Zhang Y, (2008) I-TASSER server for protein 3D structure prediction. BMC Bioinformatics 9: 40.
58. Ho WC, Fitzgerald MX, Marmorstein R, (2006) Structure of the p53 core domain dimer bound to DNA. J Biol Chem 281: 20494-20502.
59. Gordo S, Martos V, Santos E, Menéndez M, Bo C, et al. (2008) Stability and structural recovery of the tetramerization domain of p53-R337H mutant induced by a designed templating ligand. Proc Natl Acad Sci U S A 105: 16426-16431.
60. Qin H, Srinivasula SM, Wu G, Fernandes-Alnemri T, Alnemri ES, et al. (1999) Structural basis of procaspase-9 recruitment by the apoptotic protease-activating factor 1. Nature 399: 549-557.
61. Yu X, Acehan D, Ménétret JF, Booth CR, Ludtke SJ, et al. (2005) A structure of the human apoptosome at 12.8 A resolution provides insights into this cell death platform. Structure 13: 1725-1735.
62. Riedl SJ, Salvesen GS, (2007) The apoptosome: signaling platform of cell death. Nat Rev Mol Cell Biol 8: 405-413.
63. Yuan S, Yu X, Topf M, Ludtke SJ, Wang X, et al. (2010) Structure of an apoptosome-procaspase-9 CARD complex. Structure 18: 571-583.
64. Reubold TF, Wohlgemuth S, Eschenburg S, (2011) Crystal structure of full-length Apaf-1: how the death signal is relayed in the mitochondrial pathway of apoptosis. Structure 19: 1074-1083.
65. Li M, Ding Y, Mu Y, Ao J, Chen X, (2011) Molecular cloning and characterization of caspase-3 in large yellow croaker (Pseudosciaena crocea). Fish Shellfish Immunol 30: 910-916.
66. Yan N, Shi Y, (2005) Mechanisms of apoptosis through structural biology. Annu Rev Cell Dev Biol 21: 35-56.
67. Riedl SJ, Renatus M, Schwarzenbacher R, Zhou Q, Sun C, et al. (2001) Structural basis for the inhibition of caspase-3 by XIAP Cell 104: 791-800.
68. Ekert PG, Vaux DL, (2005) The mitochondrial death squad: hardened killers or innocent bystanders? Curr Opin Cell Biol 17: 626-30.
69. Honarpour N, Du C, Richardson JA, Hammer RE, Wang X, et al. (2000) Adult Apaf-1-deficient mice exhibit male infertility. Dev Biol 218: 248-58.
70. Honarpour N, Du C, Richardson JA, Hammer RE, Wang X, et al. (2000) Adult Apaf-1-deficient mice exhibit male infertility. Dev Biol 218: 248-58.
71. Salazar G, Joshi A, Liu D, Wei H, Persson JL, et al. (2005) Induction of apoptosis involving multiple pathways is a primary response to cyclin A1-deficiency in male meiosis. Dev Dyn 234: 114-123.
72. Wolgemuth DJ, (2003) Insights into regulation of the mammalian cell cycle from studies on spermatogenesis using genetic approaches in animal models. Cytogenet Genome Res 103: 256-266.
73. Lee S, Elenbaas B, Levine A, Griffith J, (1995) p53 and its 14 kDa C-terminal domain recognize primary DNA damage in the form of insertion/deletion mismatches. Cell 81: 1013-1020.
74. Oberosler P, Hloch P, Ramsperger U, Stahl H, (1993) p53-catalyzed annealing of complementary single-stranded nucleic acids. EMBO J 12: 2389-2396.
75. Bakalkin G, Yakovleva T, Selivanova G, Magnusson KP, Szekely L, et al. (1994) p53 binds single-stranded DNA ends and catalyzes DNA renaturation and strand transfer. Proc Natl Acad Sci USA 91: 413-417.
76. Said TM, Paasch U, Glander HJ, Agarwal A, (2004) Role of caspases in male infertility. Hum Reprod Update. 10: 39-51.
77. Wang Q, Zhao XF, Ji YL, Wang H, Liu P, et al. (2010) Mitochondrial signaling pathway is also involved in bisphenol A induced germ cell apoptosis in testes. Toxicol Lett. 199: 129-135.
78. Bartke A, (1995) Apoptosis of male germ cells, a generalized or a cell type-specific phenomenon? Endocrinology 36: 3-4.
79. Billig H, Furuka I, Rivier C, Tapanainea J, Parvinen M, et al. (1995) Apoptosis in testis germ cells: developmental changes in gonadotropin dependence and localization to selective tubule stages. Endocrinology 136: 5-12.
80. Sen Gupta R, Kim J, Gomes C, Oh S, Park J, et al. (2004) Effect of ascorbic acid supplementation on testicular steroidogenesis and germ cell death in cadmium-treated male rats. Mol Cell Endocrinol 221: 57-66.
81. Vera Y, Erkkilä K, Wang C, Nunez C, Kyttänen S, et al. (2006) Involvement of p38 mitogen-activated protein kinase and inducible nitric oxide synthase in apoptotic signaling of murine and human male germ cells after hormone deprivation. Mol Endocrinol 20: 1597-1609.
82. Embree-Ku M, Venturini D, Boekelheide K, (2002) Fas is involved in the p53-dependent apoptotic response to ionizing radiation in mouse testis. Biol Reprod 66: 1456-1461.
83. Chai J, Shiozaki E, Srinivasula SM, Wu Q, Datta P, et al. (2001) Structural basis of caspase-7 inhibition by XIAP. Cell 104: 769-780.
84. Hueber AO, Zornig M, Lyon D, Suda T, Nagata S, et al. (1997) Requirement for the CD95 receptor-ligand pathway in c-Myc-induced apoptosis. Science 278: 1305-1309.
85. Schamberger CJ, Gerner C, Cerni C, (2005) Caspase-9 plays a marginal role in serum starvation-induced apoptosis. Exp Cell Res 302: 115-28.
86. Rathmell JC, Fox CJ, Plas DR, Hammerman PS, Cinalli RM, et al. (2003) Akt-directed glucose metabolism can prevent Bax conformation change and promote growth factor-independent survival. Mol Cell Biol 23: 7315-7328.
87. Zhao Y, Altman BJ, Coloff JL, Herman CE, Jacobs SR, et al. (2007) Glycogen synthase kinase 3alpha and 3beta mediate a glucose-sensitive antiapoptotic signaling pathway to stabilize Mcl-1. Mol Cell Biol 27: 4328-4339.
88. Zhao Y, Coloff JL, Ferguson EC, Jacobs SR, Cui K, et al. (2008) Glucose metabolism attenuates p53 and Puma-dependent cell death upon growth factor deprivation. J Biol Chem 283: 36344-36353.
89. Lomb DJ, Desouza LA, Franklin JL, Freeman RS, (2009) Prolyl hydroxylase inhibitors depend on extracellular glucose and hypoxia-inducible factor (HIF)-2alpha to inhibit cell death caused by nerve growth factor (NGF) deprivation: evidence that HIF-2alpha has a role in NGF-promoted survival of sympathetic neurons. Mol Pharmacol 75: 1198-1209.
90. Morissette MR, Howes AL, Zhang T, Heller Brown J, (2003) Upregulation of GLUT1 expression is necessary for hypertrophy and survival of neonatal rat cardiomyocytes. J Mol Cell Cardiol 35: 1217-1227.
91. Hall JL, Chatham JC, Eldar-Finkelman H, Gibbons GH, (2001) Upregulation of glucose metabolism during intimal lesion formation is coupled to the inhibition of vascular smooth muscle cell apoptosis. Role of GSK3beta. Diabetes 50: 1171-1179.
92. Vander Heiden MG, Plas DR, Rathmell JC, Fox CJ, Harris MH, et al. (2001) Growth factors can influence cell growth and survival through effects on glucose metabolism. Mol Cell Biol 21: 5899-5912.
93. Mason EF, Rathmell JC, (2011) Cell metabolism: an essential link between cell growth and apoptosis. Biochim Biophys Acta 1813: 645-654.
94. Kaufmann SH, Hengartner MO, (2001) Programmed cell death: alive and well in the new millennium. Trends Cell Biol 11: 526-534.
95. Allsopp TE, McLuckie J, Kerr LE, Macleod M, Sharkey J, et al. (2000) Caspase 6 activity initiates caspase 3 activation in cerebellar granule cell apoptosis. Cell Death Differ 7: 984-993.
96. Kilic M, Schafer R, Hoppe J, Kagerhuber U, (2002) Formation of noncanonical high molecular weight caspase-3 and-6 complexes and activation of caspase-12 during serum starvation induced apoptosis in AKR-2B mouse fibroblasts. Cell Death Differ 9: 125-137.
97. Chipuk JE, Green DR, (2008) How do BCL-2 proteins induce mitochondrial outer membrane permeabilization? Trends Cell Biol 18: 157-164.
98. Ekert PG, Read SH, Silke J, Marsden VS, Kaufmann H, et al. (2004) Apaf-1 and caspase-9 accelerate apoptosis, but do not determine whether factor-deprived or drug-treated cells die. J Cell Biol 165: 835-842.
99. Canman CE, Gilmer TM, Coutts SB, Kastan MB, (1995) Growth factor modulation of p53-mediated growth arrest versus apoptosis. Genes Dev 9: 600-11.
100. Thangaraju M, Kaufmann SH, Couch FJ, (2000) BRCA1 facilitates stress-induced apoptosis in breast and ovarian cancer cell lines. J Biol Chem 275: 33487-33496.
101. Zhou T, Zhou G, Song W, Eguchi N, Lu W, et al. (1999) Cadmium-induced apoptosis and changes in expression of p53, c-jun and MT-I genes in testes and ventral prostate of rats. Toxicology 142: 1-13.
102. Siu ER, Mruk DD, Porto CS, Cheng CY, (2009) Cadmium-induced testicular injury. Toxicol Appl Pharmacol 238: 240-249.
103. Ozawa N, Goda N, Makino N, Yamaguchi T, Yoshimura Y, et al. (2002) Leydig cell-derived heme oxygenase-1 regulates apoptosis of premeiotic germ cells in response to stress. J Clin Invest 109: 457-467.
104. Pant N, Upadhyay G, Pandey S, Mathur N, Saxena DK, et al. (2003) Lead and cadmium concentration in the seminal plasma of men in the general population: correlation with sperm quality. Reprod Toxicol 17: 447-450.
105. Kim J, Soh J, (2009) Cadmium-induced apoptosis is mediated by the translocation of AIF to the nucleus in rat testes. Toxicol Lett 188: 45-51.
106. Xu C, Johnson JE, Singh PK, Jones MM, Yan H, et al. (1996) In vivo studies of cadmium-induced apoptosis in testicular tissue of the rat and its modulation by a chelating agent. Toxicology 107: 1-8.
107. Ji YL, Wang H, Liu P, Wang Q, Zhao XF, et al. (2010) Pubertal cadmium exposure impairs testicular development and spermatogenesis via disrupting testicular testosterone synthesis in adult mice. Reprod Toxicol 29: 176-183.
108. Lafuente A, Cano P, Esquifino A, (2003) Are cadmium effects on plasma gonadotropins, prolactin, ACTH, GH and TSH levels, dose-dependent? Biometals 16: 243-250.
109. Lafuente A, González-Carracedo A, Romero A, Cano P, Esquifino AI, (2004) Cadmium exposure differentially modifies the circadian patterns of norepinephrine at the median eminence and plasma LH, FSH and testosterone levels. Toxicol Lett 146: 175-182.
110. Laskey JW, Phelps PV, (1991) Effect of cadmium and other metal cations on in vitro Leydig cell testosterone production. Toxicol Appl Pharmacol 108: 296-306.
111. Ragan HA, Mast TJ, (1990) Cadmium inhalation and male reproductive toxicology. Rev Environ Contam Toxicol 114: 1-22.
112. Hew KW, Ericson WA, Welsh MJ, (1993) A single low cadmium dose causes failure of spermiation in the rat. Toxicol Appl Pharmacol 121: 15-21.
113. Yang JM, Arnush M, Chen QY, Wu XD, Pang B, et al. (2003) Cadmium-induced damage to primary cultures of rat Leydig cells. Reprod Toxicol 142: 553-560.
114. Roberts KP, Zirkin BR, (1991) Androgen regulation of spermatogenesis in the rat. Ann N Y Acad Sci 637: 90-106.
115. O'Donnell L, McLachlan RI, Wreford NG, de Kretser DM, Robertson DM, (1996) Testosterone withdrawal promotes stage-specific detachment of round spermatids from the rat seminiferous epithelium. Biol Reprod 55: 895-901.
116. Pareek TK, Joshi AR, Sanyal A, Dighe RR, (2007) Insights into male germ cell apoptosis due to depletion of gonadotropins caused by GnRH antagonists. Apoptosis 12: 1085-1100.
117. Woolveridge I, Boer-Brouwer M, Taylor MF, Teerds KJ, Wu FCW, et al. (1999) Apoptosis in the rat spermatogenic epithelium following androgen withdrawal: changes in apoptosis-related genes. Biol Reprod 60: 461-470.
118. Stocco DM, Wells J, Clark BJ, (1993) The effects of hydrogen peroxide on steroidogenesis in mouse Leydig tumor cells. Endocrinology 133: 2827-2832.
119. Ciesielska AS, Stachura A, Slotwinska M, Kaminska T, Sniezko R, et al. (2000) The inhibitory effect of zinc on cadmium-induced cell apoptosis and reactive oxygen species production in cell culture. Toxicology 145: 171-183.
120. Stohs SJ, Bagchi D, Hassoun E, Bagchi M, (2001) Oxidative mechanism in toxicity of chromium and cadmium ions. J Environ Pathol Oncol 20: 77-88.
121. Jimi S, Uchiyama M, Takaki A, Suzumiya J, Hara S, (2004) Mechanisms of cell death induced by cadmium and arsenic. Ann N Y Acad Sci 1011: 325-331.
122. Liu J, Shen HM, Ong CN, (2001) Role of intracellular thio depletion, mitochondrial dysfunction and reactive oxygen species in Salvia miltiorrhiza-induced apoptosis in human hepatoma HepG2 cells. Life Sci 69: 1833-1850.
123. Hassoum EA, Stohs SJ, (1996) Cadmium-induced production of superoxide and nitric oxide. DNA single strand breaks and lactate dehydrogenase leakage in J774A. 1 cell cultures. Toxicology 112: 219-226.
124. Wu X, Faqi AS, Yang J, Pang B, Ding X, et al. (2002) 2-Bromopropane induces DNA damage, impairs functional antioxidant cellular defenses, and enhances the lipid peroxidation process in primary cultures of rat Leydig cells. Reprod Toxicol 16: 379-384.
125. Bonini P, Cicconi S, Cardinale A, Vitale C, Serafino AL, et al. (2004) Oxidative stress induces p53-mediated apoptosis in glia: p53 transcription-independent way to die. J Neurosci Res 75: 83-95.
126. Kasahara E, Sato EF, Miyoshi M, Konaka R, Hiramoto K, et al. (2002) Role of oxidative stress in germ cell apoptosis induced by di (2-ethylhexyl) phthalate. Biochem J 365: 849-856.
127. Kondoh M, Araragi S, Sato K, Higashimoto M, Takiguchi M, et al. (2002) Cadmium induces apoptosis partly via caspase-9 activation in HL-60 cells. Toxicology 170: 111-117.
128. Li M, Kondo T, Zhao QL, Li FJ, Tanabe K, et al. (2000) Apoptosis induced by cadmium in human lymphoma U937 cells through Ca2+-calpain and caspase-mitochondria-dependent pathways. J Biol Chem 275: 39702-39709.
129. Vousden KH, (2006) Outcomes of p53 activation-spoilt for choice. J Cell Sci 19: 5015-20.
130. Zheng H, Liu J, Choo KHA, Michalska AE, Klaassen CD, (1996) Metallothionein-I and-II knock-out mice are sensitive to cadmium-induced liver mRNA expression of c-jun and p53. Toxicol Appl Pharmacol 136: 229-235.
131. Mieusset R, Bujan L, (1995) Testicular heating and its possible contributions to male fertility: a review. Int J Androl 18: 169-184.
132. Chowdhury AK, Steinberger E, (1964) A quantitative study of the effect of heat on germinal epithelium of rat testes. J Anat 115: 509-524.
133. Vera Y, Diaz-Romero M, Rodriguez S, Lue Y, Wang C, et al. (2004) Mitochondria-dependent pathway is involved in heat induced male germ cell death: lessons from mutant mice. Biol Reprod 70: 1534-1540.
134. Bernal-Mañas CM, Morales E, Pastor LM, Pinart E, Bonet S, et al. (2005) Proliferation and apoptosis of spermatogonia in postpuberal boar (Sus domesticus) testes with spontaneous unilateral and bilateral abdominal cryptorchidism. Acta Histochem 107: 365-372.
135. Xu J, Xu Z, Jiang Y, Qian X, Huang Y, (2000) Cryptorchidism induces mouse testicular germ cell apoptosis and changes in bcl-2 and bax protein expression. J Environ Pathol Toxicol Oncol 19: 25-33.
136. Zhang ZH, Jin X, Zhang XS, Hu ZY, Zou RJ, et al. (2003) Bcl-2 and Bax are involved in experimental cryptorchidism-induced testicular germ cell apoptosis in rhesus monkeys. Contraception 68: 297-301.
137. Heckert L, Griswold MD, (1993) Expression of the FSH receptor in the testis. Recent Prog Horm Res 48: 61-77.
138. Ji ZS, Abé S, (1994) Mammalian follicle-stimulating hormone stimulates DNA synthesis in secondary spermatogonia and Sertoli cells in organ culture of testes fragments from the newt, Cynops pyrrhogaster. Zygote 2: 53-61.
139. Huang Y, Jin H, Liu Y, Zhou J, Ding J, et al. (2010) FSH inhibits ovarian cancer cell apoptosis by up-regulating Survivin and down-regulating PDCD6 and DR5. Endocr Relat Cancer 18: 13-26.
140. Blanco-Rodriguez J, Martinez-Garcia C, Porras A, (2003) Correlation between DNA synthesis in the second, third and fourth generations of spermatogonia and the occurrence of apoptosis in both spermatogonia and spermatocytes. Reproduction 126: 661-668.
141. Li LH, Wine RN, Chapin RE, (1996) 2-Methoxyacetic acid (MAA)-induced spermatocyte apoptosis in human and rat testes: an in vitro comparison. J Androl 17: 538-548.
142. 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.
143. Allan DJ, Harmon BV, Roberts SA, (1992) Spermatogonia apoptosis has three morphologically recognizable phases and shows no circadian rhythm during normal spermatogenesis in the rat. Cell Prolif 25: 241-250.
144. Paasch U, Grunewald S, Fitzl G, Glander H, (2003) Deterioration of plasma membrane is associated with activated caspases in human spermatozoa. J Androl 24: 246-252.
145. Thornberry N, Lazebnik Y, (1998) Caspases: enemies within. Science 281: 1312-1316.
146. Paasch U, Grunewald S, Glander HJ, (2002) Presence of up- and downstream caspases in relation to impairment of human spermatogenesis. Andrologia 34: 279.
147. Weng S, Taylor S, Morshedi M, Schuffner A, Duran E, et al. (2002) Caspase activity and apoptotic markers in ejaculated human sperm. Mol Hum Reprod 8: 984-991.
148. Wang X, Sharma R, Sikka S, Thomas AJ Jr, Falcone T, et al. (2003) Oxidative stress is associated with increased apoptosis leading to spermatozoa DNA damage in patients with male factor infertility. Fertil Steril 80: 531-535.