Regulation of apoptotic signaling pathways by 5α-dihydrotestosterone and 17β-estradiol in immature rat Sertoli cells

Journal of Steroid Biochemistry and Molecular Biology

Volumn 135, Issue 1, 2013, Pages 15-23

  Simoes V L ^a   Alves, M G ^a   Martins, A D ^a   Dias, T R ^a   Rato, L ^a   Socorro, S ^a   Oliveira, P F ^a  

^a UNIVERSITY OF BEIRA INTERIOR   (Portugal)

Author keywords

Androgens; Apoptosis; Caspases; Estrogens; Sertoli cells

Indexed keywords

ANDROSTANOLONE; APOPTOSIS INDUCING FACTOR; CASPASE 3; CASPASE 9; ESTRADIOL; MESSENGER RNA; PROTEIN BAX; PROTEIN BCL 2; PROTEIN P53;

ANIMAL CELL; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DNA FRAGMENTATION; ENZYME ACTIVITY; MALE; MITOCHONDRION; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; RAT; REGULATORY MECHANISM; SERTOLI CELL; SIGNAL TRANSDUCTION;

ANIMALS; APOPTOSIS; APOPTOSIS INDUCING FACTOR; APOPTOSIS REGULATORY PROTEINS; BCL-2-ASSOCIATED X PROTEIN; BCL-ASSOCIATED DEATH PROTEIN; CASPASE 3; CASPASE 9; CELLS, CULTURED; DIHYDROTESTOSTERONE; DNA FRAGMENTATION; DOWN-REGULATION; ESTRADIOL; MALE; MITOCHONDRIA; RATS; RATS, WISTAR; RNA, MESSENGER; SERTOLI CELLS; SIGNAL TRANSDUCTION; SPERMATOGENESIS; SPERMATOZOA; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84874408605     PISSN: 09600760     EISSN: 18791220     Source Type: Journal    
DOI: 10.1016/j.jsbmb.2012.11.019     Document Type: Article

References (63)

1. M.D. Griswold Interactions between germ cells and sertoli cells in the testis Biology of Reproduction 52 1995 211 216
2. L. Johnson, D.L. Thompson Jr., and D.D. Varner Role of sertoli cell number and function on regulation of spermatogenesis Animal Reproduction Science 105 1-2 2008 23 51
3. L. Rato, S. Socorro, J.E.B. Cavaco, and P.F. Oliveira Tubular fluid secretion in the seminiferous epithelium: ion transporters and aquaporins in sertoli cells Journal of Membrane Biology 236 2 2010 215 224
4. J.M. Orth, G.L. Gunsalus, and A.A. Lamperti Evidence from sertoli cell-depleted rats indicates that spermatid number in adults depends on numbers of sertoli cells produced during perinatal development Endocrinology 122 3 1988 787 794
5. C.Y. Cheng, E.W. Wong, H.H. Yan, and D.D. Mruk Regulation of spermatogenesis in the microenvironment of the seminiferous epithelium: new insights and advances Molecular and Cellular Endocrinology 315 1-2 2010 49 56
6. K.K. Shukla, A.A. Mahdi, and S. Rajender Apoptosis, spermatogenesis and male infertility Frontiers in Bioscience 4 2012 746 754
7. N. Eid, Y. Ito, and Y. Otsuki Enhanced mitophagy in sertoli cells of ethanol-treated rats: morphological evidence and clinical relevance Journal of Molecular Histology 2012 1 10
8. A. Bozec, F. Chuzel, S. Chater, C. Paulin, R. Bars, M. Benahmed, and C. Mauduit The mitochondrial-dependent pathway is chronically affected in testicular germ cell death in adult rats exposed in utero to anti-androgens Journal of Endocrinology 183 1 2004 79 90
9. Y.J. Kim, J.Y. Chung, S.G. Lee, J.Y. Kim, J.E. Park, W.R. Kim, B.S. Joo, S.H. Han, K.S. Yoo, and Y.H. Yoo Arsenic trioxide-induced apoptosis in TM4 sertoli cells: The potential involvement of p21 expression and p53 phosphorylation Toxicology 285 3 2011 142 151
10. S.K. Kim, Y.D. Yoon, Y.S. Park, J.T. Seo, and J.H. Kim Involvement of the Fas-Fas ligand system and active caspase-3 in abnormal apoptosis in human testes with maturation arrest and sertoli cell-only syndrome Fertility and Sterility 87 3 2007 547 553
11. G. Dirami, N. Ravindranath, H. Kleinman, and M. Dym Evidence that basement membrane prevents apoptosis of sertoli cells in vitro in the absence of known regulators of sertoli cell function Endocrinology 136 10 1995 4439 4447
12. J. Tesarik, M. Guido, C. Mendoza, and E. Greco Human spermatogenesis in vitro: respective effects of follicle-stimulating hormone and testosterone on meiosis, spermiogenesis, and sertoli cell apoptosis Journal of Clinical Endocrinology and Metabolism 83 12 1998 4467 4473
13. V. Pentikäinen, K. Erkkilä, L. Suomalainen, M. Parvinen, L. Dunkel, and Estradiol Acts as a germ cell survival factor in the human testis in vitro Journal of Clinical Endocrinology and Metabolism 85 5 2000 2057 2067
14. S. Laurentino, J. Gonçalves, J.E. Cavaco, P.F. Oliveira, M.G. Alves, M. Sousa, A. Barros, and S. Socorro Apoptosis-inhibitor Aven is downregulated in defective spermatogenesis and a novel estrogen target gene in mammalian testis Fertility and Sterility 96 3 2011 745 750
15. J. Skommer, D. Wlodkowic, and A. Deptala Larger than life: mitochondria and the Bcl-2 family Leukemia Research 31 2006 277 286
16. S. Elmore Apoptosis: a review of programmed cell death Toxicologic Pathology 35 4 2007 495 516
17. P. Saikumar, Z. Dong, V. Mikhailov, M. Denton, J.M. Weimberg, and M.A. Venkatachalam Apoptosis: definition, mechanisms, and relevance to disease American Journal of Medicine 107 5 1999 489 506
18. B. Fadeel, and S. Orrenius Apoptosis: a basic biological phenomenon with wide-ranging implications in human disease Journal of Internal Medicine 258 6 2005 479 517
19. A. Jourdain, and J.C. Martinou Mitochondrial outer-membrane permeabilization and remodelling in apoptosis International Journal of Biochemistry and Cell Biology 41 10 2009 1884 1889
20. R. Zhang, Y. He, X. Zhang, B. Xing, Y. Sheng, H. Lu, and Z. Wei Estrogen receptor-regulated microRNAs contribute to the Bcl2/Bax imbalance in endometrial adenocarcinoma and precancerous lesions Cancer Letters 314 2 2011 155 165
21. M.H. Harris, and C.B. Thompson The role of the Bcl-2 family in the regulation of outer mitochondrial membrane permeability Cell Death and Differentiation 7 12 2000 1182 1191
22. C. Artus, H. Boujrad, A. Bouharrour, M.N. Brunelle, S. Hoos, V.J. Yuste, P. Lenormand, J.C. Rousselle, A. Namane, and P. England AIF promotes chromatinolysis and caspase-independent programmed necrosis by interacting with histone H2AX EMBO Journal 29 9 2010 1585 1599
23. S.S. Du Plessis, S. Cabler, D.A. McAlister, E. Sabanegh, and A. Agarwal The effect of obesity on sperm disorders and male infertility Nature Reviews Urology 7 3 2010 153 161
24. D.A. Paduch, A. Bolyakov, P. Cohen, and A. Travis Reproduction in men with Klinefelter syndrome: the past, the present, and the future Seminars in Reproductive Medicine 27 2 2009 137 148
25. P.F. Oliveira, M.G. Alves, L. Rato, J. Silva, R. Sa, A. Barros, M. Sousa, R.A. Carvalho, J.E. Cavaco, and S. Socorro Influence of 5alpha- dihydrotestosterone and 17beta-estradiol on human sertoli cells metabolism International Journal of Andrology 34 6 Pt 2 2011 e612 e620
26. L. Rato, M.G. Alves, S. Socorro, R.A. Carvalho, J.E. Cavaco, and P.F. Oliveira Metabolic modulation induced by oestradiol and DHT in immature rat sertoli cells cultured in vitro Bioscience Reports 32 1 2012 61 69
27. B.S. Majors, M.J. Betenbaugh, and G.G. Chiang Links between metabolism and apoptosis in mammalian cells: applications for anti-apoptosis engineering Metabolic Engineering 9 4 2007 317 326
28. S. Meroni, M. Riera, E. Pellizzari, and S. Cigorraga Regulation of rat sertoli cell function by FSH: possible role of phosphatidylinositol 3-kinase/protein kinase B pathway Journal of Endocrinology 174 2 2002 195 204
29. P.F. Oliveira, M.G. Alves, L. Rato, S. Laurentino, J. Silva, R. Sa, A. Barros, M. Sousa, R.A. Carvalho, J.E. Cavaco, and S. Socorro Effect of insulin deprivation on metabolism and metabolism-associated gene transcript levels of in vitro cultured human sertoli cells Biochimica et Biophysica Acta 1820 2 2012 84 89
30. K. Steger, R. Rey, S. Kliesch, F. Louis, G. Schleicher, and M. Bergmann Immunohistochemical detection of immature sertoli cell markers in testicular tissue of infertile adult men: a preliminary study International Journal of Andrology 19 2 1996 122 128
31. V.B. Mahesh, T.G. Muldoon, J.C. Eldridge, and K.S. Korach The role of steroid hormones in the regulation of gonadotropin secretion Journal of Steroid Biochemistry 6 6 1975 1025 1036
32. T.T. Turner, C.E. Jones, S.S. Howards, L.L. Ewing, B. Zegeye, and G.L. Gunsalus On the androgen microenvironment of maturing spermatozoa Endocrinology 115 5 1984 1925 1932
33. B.P. Setchell Hormones: what the testis really sees Reproduction, Fertility, and Development 16 5 2004 535 545
34. W. Strober Appendix 3B Trypan Blue Exclusion Test of cell viability Current Protocols in Immunology 2001
35. M.G. Alves, N.G. Machado, V.A. Sardao, R.A. Carvalho, and P.J. Oliveira Anti-apoptotic protection afforded by cardioplegic celsior and histidine buffer solutions to hearts subjected to ischemia and ischemia/reperfusion Journal of Cellular Biochemistry 112 12 2011 3872 3881
36. D. Speidel Transcription-independent p53 apoptosis: an alternative route to death Trends in Cell Biology 20 1 2010 14 24
37. H. Zou, R. Yang, J. Hao, J. Wang, C. Sun, S.W. Fesik, J.C. Wu, K.J. Tomaselli, and R.C. Armstrong Regulation of the Apaf-1/caspase-9 apoptosome by caspase-3 and XIAP Journal of Biological Chemistry 278 10 2003 8091 8098
38. D. Twiddy, and K. Cain Caspase-9 cleavage, do you need it? Biochemical Journal 405 1 2007 e1 e2
39. C. Cande, N. Vahsen, D. Metivier, H. Tourriere, K. Chebli, C. Garrido, J. Tazi, and G. Kroemer Regulation of cytoplasmic stress granules by apoptosis-inducing factor Journal of Cell Science 117 Pt 19 2004 4461 4468
40. P.R. Walker, and M. Sikorska New aspects of the mechanism of DNA fragmentation in apoptosis Biochemistry and Cell Biology Biochimie et Biologie Cellulaire 75 4 1997 287 299
41. N. Sofikitis, N. Giotitsas, P. Tsounapi, D. Baltogiannis, D. Giannakis, and N. Pardalidis Hormonal regulation of spermatogenesis and spermiogenesis Journal of Steroid Biochemistry and Molecular Biology 109 3 2008 323 330
42. M.D. Griswold The central role of sertoli cells in spermatogenesis Seminars in Cell and Developmental Biology 9 4 1998 411 416
43. W.H. Walker Non-classical actions of testosterone and spermatogenesis Philosophical Transactions of the Royal Society of London, Series B: Biological Sciences 365 1546 2010 1557 1569
44. S. Carreau, D. Silandre, C. Bois, H. Bouraima, I. Galeraud-Denis, and C. Delalande Estrogens: a new player in spermatogenesis Folia Histochemica et Cytobiologica 45 Suppl. 1 2007 4 5
45. J.E.B. Cavaco, S.S. Laurentino, A. Barros, M. Sousa, S. Socorro, and Estrogen Receptors alfa and beta in human testis: both isoforms are expressed Systems Biology in Reproductive Medicine 55 0 2009 137 144
46. G. Verhoeven, and J. Cailleau Follicle-stimulating hormone and androgens increase the concentration of the androgen receptor in sertoli cells Endocrinology 122 4 1988 1541 1550
47. L. Rato, M.G. Alves, S. Socorro, A.I. Duarte, J.E. Cavaco, and P.F. Oliveira Metabolic regulation is important for spermatogenesis Nature Reviews Urology 9 2012 330 338
48. M.G. Alves, L. Rato, R.A. Carvalho, P.I. Moreira, S. Socorro, and P.F. Oliveira Hormonal control of sertoli cell metabolism regulates spermatogenesis Cellular and Molecular Life Sciences 2012 10.1007/s00018-012-1079-1
49. M. Bialek, P. Zaremba, K.K. Borowicz, and S.J. Czuczwar Neuroprotective role of testosterone in the nervous system Polish Journal of Pharmacology 56 2004 509 518
50. K. Erkkilä, K. Henriksén, V. Hirvonen, S. Rannikko, J. Salo, M. Parvinen, and L. Dunkel Testosterone regulates apoptosis in adult human seminiferous tubules in vitro Journal of Clinical Endocrinology and Metabolism 82 7 1997 2314 2321
51. T. Pelzer, M. Schumann, M. Neumann, T. deJager, M. Stimpel, E. Serfling, and L. Neyses 17 [beta]-Estradiol prevents programmed cell death in cardiac myocytes Biochemical and Biophysical Research Communications 268 1 2000 192 200
52. M.G. Alves, S. Socorro, J. Silva, A. Barros, M. Sousa, J.E. Cavaco, and P.F. Oliveira In vitro cultured human sertoli cells secrete high amounts of acetate that is stimulated by 17β-estradiol and suppressed by insulin deprivation Biochimica et Biophysica Acta 1823 8 2012 1389 1394
53. K. Moley, and M. Mueckler Glucose transport and apoptosis Apoptosis 5 2 2000 99 105
54. D. Schwartz, and V. Rotter p53-Dependent cell cycle control: response to genotoxic stress Seminars in Cancer Biology 8 5 1998 325 336
55. O. Terrones, B. Antonsson, H. Yamaguchi, H.G. Wang, J. Liu, R.M. Lee, A. Herrmann, and G. Basanez Lipidic pore formation by the concerted action of proapoptotic Bax and tBID Journal of Biological Chemistry 279 29 2004 30081 30091
56. J. Tesarik, F. Martinez, L. Rienzi, M. Iacobelli, F. Ubaldi, C. Mendoza, and E. Greco In-vitro effects of FSH and testosterone withdrawal on caspase activation and DNA fragmentation in different cell types of human seminiferous epithelium Human Reproduction 17 7 2002 1811 1819
57. C. Royer, T.F. Lucas, M.F. Lazari, and C.S. Porto 17β-Estradiol signaling and regulation of proliferation and apoptosis of rat sertoli cells Biology of Reproduction 86 4 2012 1 13
58. I. Schmitz, S. Kirchhoff, and P.H. Krammer Regulation of death receptor-mediated apoptosis pathways International Journal of Biochemistry and Cell Biology 32 11-12 2000 1123 1136
59. K.M. Boatright, and G.S. Salvesen Mechanisms of caspase activation Current Opinion in Cell Biology 15 6 2003 725 731
60. D. Le Goff, C. Viville, and S. Carreau Apoptotic effects of 25-hydroxycholesterol in immature rat sertoli cells: prevention by 17beta-estradiol Reproductive Toxicology 21 3 2006 329 334
61. T.F.G. Lucas, C. Royer, E.R. Siu, M.F.M. Lazari, and C.S. Porto Expression and signaling of G protein-coupled estrogen receptor 1 (GPER) in rat sertoli cells Biology of Reproduction 83 2 2010 307 317
62. I. Petrache, T.R. Medler, A.T. Richter, K. Kamocki, U. Chukwueke, L. Zhen, Y. Gu, J. Adamowicz, K.S. Schweitzer, W.C. Hubbard, E.V. Berdyshev, G. Lungarella, and R.M. Tuder Superoxide dismutase protects against apoptosis and alveolar enlargement induced by ceramide American Journal of Physiology-Lung Cellular and Molecular Physiology 295 1 2008 L44 L53
63. C. Cande, I. Cohen, E. Daugas, L. Ravagnan, N. Larochette, N. Zamzami, and G. Kroemer Apoptosis-inducing factor (AIF): a novel caspase-independent death effector released from mitochondria Biochimie 84 2-3 2002 215 222