Intrinsic and extrinsic apoptotic pathways are involved in rat testis by cold water immersion-induced acute and chronic stress

References

• Agarwal, A., Saleh, R.A. and Bedaiwy, M.A. (2003) Role of reactive oxygen species in the pathophysiology of human reproduction. Fertil Steril 79:829–843
   PubMed Web of Science ®Google Scholar
• Agarwal, A., Virk, G., Ong, C. and du Plessis, S.S. (2014) Effect of Oxidative Stress on Male Reproduction. World J Mens Health 32:1–17
   PubMedGoogle Scholar
• Aitken, R.J. and Baker, R.A. (2013) Causes and consequences of apoptosis in spermatozoa; contributions to infertility and impacts on development. Int J Dev Biol 57:265–272
   PubMed Web of Science ®Google Scholar
• Allan, D.J., Harmon, B.V. and Kerr, J.F.R. (1987) Cell death in spermatogenesis. In: Perspectives on mammalian cell death. Potten CS, ed. Oxford University Press, UK, pp. 229–258
   Google Scholar
• Alvarez, J.G. and Storey, B.T. (1982) Spontaneous lipid peroxidation in rabbit epididymal spermatozoa: its effect on sperm motility. Biol Reprod 27:1102–1108
   PubMed Web of Science ®Google Scholar
• Banks, S., King, S.A., Irvine, D.S. and Saunders, P.T.K. (2005) Impact of a mild scrotal heat stress on DNA integrity in murine spermatozoa. Reproduction 129:505–514
   PubMed Web of Science ®Google Scholar
• Blanco-Rodríguez, J. (1998) A matter of death and life: the significance of germ cell death during spermatogenesis. Int J Androl 21:236–248
   PubMed Web of Science ®Google Scholar
• Blatt, N.B. and Glick, G.C. (2001) Signaling pathways and effector mechanisms pre-programmed cell death. Bio Org Med Chem 9:1371–1384
   PubMed Web of Science ®Google Scholar
• Braun, R.E. (1998) Early sperm is sacred or is it not? Nat Genet 18:202–204
   PubMed Web of Science ®Google Scholar
• Chen, Y., Wang, Q., Wang, F.-F., Gao, H.-B. and Zhang, P. (2012) Stress induces glucocorticoid-mediated apoptosis of rat Leydig cells in vivo. Stress 15:74–84
   PubMed Web of Science ®Google Scholar
• De Lamirande, E. and Gagnon, C. (1992a) Reactive oxygen species and human spermatozoa. l. Effects on the motility of intact spermatozoa and on sperm axonemes. J Androl 13:368–378
   PubMed Web of Science ®Google Scholar
• De Lamirande, E. and Gagnon, C. (1992b) Reactive oxygen species and human spermatozoa. ll. Depletion of adenosine triphosphate plays an important role in the inhibition of sperm motility. J Androl 13:379–386
   PubMed Web of Science ®Google Scholar
• Dhanabalan, S., Jubendradass, R., Latha, P. and Mathur, P.P. (2010) Effect of restraint stress on 2,3,7,8 tetrachlorodibenzo-p-dioxin induced testicular and epididymal toxicity in rats. Human Exp Tox 30:567–578
   PubMed Web of Science ®Google Scholar
• Dong, Q., Salva, A., Sottas, C.M., Niu, E., Holmes, M. and Hardy, M.M. (2004) Rapid glucocorticoid mediation of suppressed testosterone biosynthesis in male mice subjected to immobilization stress. J Androl 25:972–981
   Google Scholar
• Earnshaw, W.C., Martins, L.M. and Kaufman, S.H. (1999) Mammalian caspases: structure, activation, substrates, and functions during apoptosis. Annu Rev Biochem 68:383–424
   PubMed Web of Science ®Google Scholar
• Francavilla, S., D’Abrizio, P., Cordeschi, J., Pelliccione, F., Necozione, S., Ulisse, S., et al. (2002) Fas expression correlates with human germ cell degeneration in meiotic and post-meiotic arrest of spermatogenesis. Mol Hum Reprod 8:213–220
   PubMedGoogle Scholar
• Greenstein, S., Ghias, K., Krett, N.L. and Rosen, S.T. (2002) Mechanisms of glucocorticoid-mediated apoptosis in hematological malignancies. Clin Cancer Res 8:1681–1694
   PubMed Web of Science ®Google Scholar
• Hales, D.B. and Payne, A.H. (1989) Glucocorticoid-mediated repression of P450scc mRNA and de novo synthesis in cultured Leydig cells. Endocrinol 124:2099–2104
   PubMed Web of Science ®Google Scholar
• Hardy, M.P., Hui-Bao, G., Qiang, D., Renshan, G., Qian, W., Wei, R.C., et al. (2005) Stress hormone and male reproductive function. Cell Tissue Res 322:147–153
   PubMed Web of Science ®Google Scholar
• Jin, P., Wang, X., Chang, F., Bai, Y., Li, Y., Zhou, R., et al. (2013) Low dose bisphenol A impairs spermatogenesis by suppressing reproductive hormone production and promoting germ cell apoptosis in adult rats. J Biomed Res 27:135–144
   PubMedGoogle Scholar
• Kaufmann, T., Strasser, A. and Jost, P.J. (2012) Fas death receptor signaling: roles of Bid and XIAP. Cell Death Differ 19:42–50
   PubMed Web of Science ®Google Scholar
• Kim, J-M., Ghosh, S.R., Weill, A.C.P. and Zirkin, B.R. (2001) Caspase-3 and Caspase-Activated Deoxyribonuclease are associated with testicular germ cell apoptosis resulting from reduced intratesticular testosterone. Endocrinol 142:3809–3816
   PubMed Web of Science ®Google Scholar
• Knudson, C.M., Tung, K.S.K., Toutellotte, W.G., Brown, G.A.J. and Korsmeyer, S.J. (1995) Bax-deficient mice with lymphoid hyperplasia and male germ cell death. Science 270:96–99
   PubMed Web of Science ®Google Scholar
• Koji, T. (2001) Male germ cell death in mouse testes: possible involvement of Fas and Fas ligand. Med Electron Microsc 34:213–222
   PubMedGoogle Scholar
• Lee, J., Richburg, J.H., Younkin, S.C. and Boekelheide, K. (1997) The Fas system is a key regulator of germ cell apoptosis in the testis. Endocrinol 138:2081–2088
   PubMed Web of Science ®Google Scholar
• Lee, J., Richburg, J.H., Shipp, E.B., Meistrich, M.L. and 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. Endocrinol 140:852–858
   PubMed Web of Science ®Google Scholar
• Lucio, R.A., Tlachi, J.L., López, A.A., Zempoalteca, R. and Velázquez-Moctezuma, J. (2009) Análisis de los parámetros del eyaculado en la rata Wistar de laboratorio: descripción de la técnica. Vet Méx 40:405–415
   Google Scholar
• Lue, Y.H., Amiya, P., Sinha-Hikim, R.S., Swerdloff, P.I., Khay, S.T., Tan, B., et al. (1999) Single exposure to heat induces stage-specific germ cell apoptosis in rats: role of intratesticular testosterone on stage specificity. Endocrinol 140:1709–1717
   PubMed Web of Science ®Google Scholar
• Maheshwari, A., Misro, M.M., Aggarwal, A., Sharma, R.K. and Nandan, D. (2009) Pathways involved in testicular germ cell apoptosis induced by H2O2 in vitro. FEBS J 276:870–881
   PubMed Web of Science ®Google Scholar
• Mahmoud, H., Mahmoud, O., Layasadat, K. and Naeim, A. (2009) Dexamethasone effects on Bax expression in the mouse testicular germ cells. Fol Histochem Cytobiol 47:237–241
   PubMed Web of Science ®Google Scholar
• Nagata, S. and Golstein, P. (1995) The Fas death factor. Science 267:1449–1456
   PubMed Web of Science ®Google Scholar
• Nakanishi, Y. and Shiratsuchi, A. (2004) Phagocytic removal of apoptotic spermatogenic cells by Sertoli cells: mechanisms and consequences. Biol Pharm Bull 27:13–16
   PubMed Web of Science ®Google Scholar
• Nirupama, M., Devaki, M., Nirupama, R. and Yajurvedi, H.N. (2012) Chronic intermittent stress-induced alterations in the spermatogenesis and antioxidant status of the testis are irreversible in albino rat. J Physiol Biochem 69:59–68
   PubMed Web of Science ®Google Scholar
• Nuñez, G., Benedict, M.A., Hu, Y. and Inohara, N. (1998) Caspases: the proteases of the apoptotic pathway. Oncogene 17:3237–3245
   PubMed Web of Science ®Google Scholar
• O'Donnell, L., McLachlan, R.I., Wreford, N.G., de Kretser, D.M. and Robertson, D.M. (1996) Testosterone withdrawal promotes stage-specific detachment of round spermatids from the rat seminiferous epithelium. Biol Reprod 55:895–901
   PubMed Web of Science ®Google Scholar
• Otala, M., Suomalainen, L., Pentikäinen, M.O., Kovanen, P., Tenhunen, M., Erkkilä, K., et al. (2005) Protection from radiation-induced male germ cell loss by sphingosine-1-phosphate. Biol Reprod 70:759–767
   Web of Science ®Google Scholar
• Orr, T.E., Taylor, M.F., Bhattacharyya, A.K., Collins, D.C. and Mann, D.R. (1994) Acute immobilization stress disrupts testicular steroidogenesis in adult male rats by inhibiting the activities of 17α-hydroxylase and 17,20-lyase without affecting the binding of LH/hCG receptors. J Androl 15:302–308
   PubMed Web of Science ®Google Scholar
• Ozawa, N., Goda, N., Makino, N., Yamaguchi, T., Yoshimura, Y. and Suematsu, M. (2002) Leydig cell-derived heme oxygenase-1 regulates apoptosis of premeiotic germ cells in response to stress. J Clin Invest 109:457–467
   PubMed Web of Science ®Google Scholar
• Pareek, T.K., Joshi, A.R., Sanyal, A. and Dighe, R.R. (2007) Insights into male germ cell apoptosis due to depletion of gonadotropins caused by GnRH antagonists. Apoptosis 12:1085–1100
   PubMed Web of Science ®Google Scholar
• Payne, A.H. and Sha, L.L. (1991) Multiple mechanism for regulation of 3β-hydroxysteroid dehydrogenase/Δ5-Δ4isomerase, 17α-hydroxylase/C17-20 lyase cytochrome P450, and cholesterol side-chain cleavage cytochrome P450 messenger ribonucleic acid levels in primary cultures of mouse Leydig cells. Endocrinol 129:1429–1435
   PubMed Web of Science ®Google Scholar
• Pentikainen, V., Erkkila, K. and Dunkel, L. (1999) Fas regulates germ cell apoptosis in the human testis in vitro. Am J Physiol 276:310–316
   Google Scholar
• Porcelli, F., Megiollaro, D., Carnevali, A. and Ferrandi, B. (2006) Fas ligand in bull ejaculated spermatozoa: A quantitative immunohistochemical study. Acta Histochem 13:287–292
   Web of Science ®Google Scholar
• Print, C.G. and Loveland, K.L. (2000) Germ cell suicide: new insights into apoptosis during spermatogenesis. Bioessays 22:423–430
   PubMed Web of Science ®Google Scholar
• Rao, B., Sourfir, J.C., Martin, M. and David, G. (1989) Lipid peroxidation in human spermatozoa as related to midpiece abnormalities and motility. Gamete Res 24:127–134
   PubMedGoogle Scholar
• Retana-Márquez, S., Domínguez-Salazar, E. and Velázquez-Moctezuma, J. (1996) Effect of acute and chronic stress on masculine sexual behavior in the rat. Psychoneuroendocrinology 21:39–50
   PubMed Web of Science ®Google Scholar
• Robaire, B., Hinton, B.T. and Orgebin-Crist, M.C. (2006) The epididymis In: Knobil and Neill's Physiology of Reproduction. Neill JD, Plant MT, Donald WP, Challis JGC, De Kretser DM, Richards JS, et al., eds. St. Louis (MO): Academic Press, pp. 1081–1092
   Google Scholar
• Rockett, J.C., Mapp, F.L., Garges, J.B., Luft, J.C. and Dix, D.J. (2001) Effects of hyperthermia on spermatogenesis, apoptosis, gene expression, and fertility in adult male mice. Biol Reprod 65:229–239
   PubMed Web of Science ®Google Scholar
• Said, T.M., Paasch, U., Glander, H.J. and Agarwal, A. (2004) Role of caspases in male infertility. Hum Reprod 10:39–51
   Web of Science ®Google Scholar
• Saki, G., Fakher, R. and Alizadeh, K. (2010) Effect of forced swimming stress on count, motility and fertilization capacity of the sperm in adult rats. Hum Reprod Sci 2:72–75
   Google Scholar
• Schultz, R., Isola, J., Parvinen, M., Honkaniemi, J., Wikström, A.C., Gustafsson, J.A., et al. (1993) Localization of the glucocorticoid receptor in testis an accessory sexual organs of male rat. Mol Cell Endocrinol 95:115–120
   PubMed Web of Science ®Google Scholar
• Shaha, C. (2008) Germ cell apoptosis: relevance to infertility and contraception. Immunol Endocr Metab Agents Med Chem 8:66–78
   Google Scholar
• Shaha, C., Tripathi, R. and Mishra, D.P. (2010) Male germ cell apoptosis: regulation and biology. Phil Trans R Soc B 365:1501–1515
   PubMed Web of Science ®Google Scholar
• Silva, E.J., Queiróz, D.B.C., Honda, L. and Avellar, M.C.W. (2010) Glucocorticoid receptor in the rat epididymis: expression, cellular distribution and regulation by steroid hormones. Mol Cell Endocrinol 325:64–77
   PubMed Web of Science ®Google Scholar
• Sinha Hikim, A.P., Rajavashisth, T.B., Sinha Hikim, I., Lue, Y., Bonavera, J.J., Leung, A., 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
   PubMed Web of Science ®Google Scholar
• Sionov, R.V., Cohen, O., Kfir, S., Zilberman, Y. and Yefenof, E. (2006) Role of mitochondrial glucocorticoid-induced apoptosis. J Exp Med 203:189–201
   PubMed Web of Science ®Google Scholar
• Sofikitis, N., Ono, K., Yamamoto, Y., Papadopoulos, H. and Miyagawa, I. (1999) Influence of the male reproductive tract on the reproductive potential of round spermatids abnormally released from the seminiferous epithelium. Horm Reprod 14:1998–2006
   Web of Science ®Google Scholar
• Stiblar-Martinic, D. (2009) Morphometrical evaluation of germ cell apoptosis in infertile men. Folia Biol (Praha) 55:233–237
   PubMed Web of Science ®Google Scholar
• Wang, D.-H., Hu, J.-R., Wang, L.-Y., Hu, Y.-J., Tan, F.-Q., Zhou, H., et al. (2012) The Apoptotic Function Analysis of p53, Apaf1, Caspase3 and Caspase7 during the Spermatogenesis of the Chinese Fire-Bellied Newt Cynops orientalis. PLoS One 7:e39920
   PubMed Web of Science ®Google Scholar
• Woodward, C. and Emery, P.W. (1987) Determination of plasma corticosterone using high-performance liquid chromatography. J Chrom 419:280–284
   PubMed Web of Science ®Google Scholar
• Yan, W., Suominen, J., Samson, M., Jegou, B. and Toppari, J. (2000) Involvement of Bcl-2 family proteins in germ cell apoptosis during testicular development in the rat and pro-survival effect of stem cell factor on germ cell in vitro. Mol and Cell Endocrinol 165:115–129
   PubMed Web of Science ®Google Scholar
• Yamamoto, C.-M., Sinha, H.A.P., Huynh, P.N., Shapiro, B., Lue, Y., Salameh, W.A., et al. (2000) Redistribution of Bax is an early step in an apoptotic leading to germ cell death in rats, triggered by mild testicular hyperthermia. Biol Reprod 63:1683–1690
   PubMed Web of Science ®Google Scholar
• Yazawa, H., Sasagawa, I., Ishigooka, M. and Nakada, T. (1999) Effect of immobilization stress on testicular germ cell apoptosis in rats. Human Reprod 14:1917–1920
   Web of Science ®Google Scholar
• Yazawa, H., Sasagawa, I. and Nakada, T. (2000) Apoptosis of testicular germ cells induced by exogenous glucocorticoid in rats. Human Reprod 15:1917–1920
   PubMed Web of Science ®Google Scholar
• Zhang, F.P., Pakarainen, T., Poutanen, M., Toppari, J. and Huhtaniemi, I. (2004) The low gonadotropin-independent constitutive production of testicular testosterone is sufficient to maintain spermatogenesis. Proc Natl Acad Sci USA 100:13692–13697
   Web of Science ®Google Scholar