Estrogenic regulation of testicular expression of stem cell factor and c-kit: Implications in germ cell survival and male fertility

Fertility and Sterility

Volumn 102, Issue 1, 2014, Pages 299-306

  Correia, Sara ^a   Alves, Mário R ^a   Cavaco, José E ^a   Oliveira, Pedro F ^a   Socorro, Sílvia ^a  

^a UNIVERSITY OF BEIRA INTERIOR   (Portugal)

Author keywords

Apoptosis; c kit; estrogens; male infertility; SCF

Indexed keywords

EFFECTOR CASPASE; ESTRADIOL; FAS LIGAND; KI 67 ANTIGEN; PROTEIN BAX; PROTEIN BCL 2; RNA; STEM CELL FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL PROLIFERATION; CELL SURVIVAL; COLORIMETRY; CONTROLLED STUDY; ENZYME ACTIVITY; GERM CELL; HORMONAL REGULATION; IMMUNOHISTOCHEMISTRY; MALE; MALE FERTILITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEMINIFEROUS TUBULE; TESTIS; UPREGULATION; WESTERN BLOTTING;

APOPTOSIS; C-KIT; ESTROGENS; MALE INFERTILITY; SCF;

ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; CELL PROLIFERATION; CELL SURVIVAL; ESTRADIOL; FERTILITY; MALE; PROTO-ONCOGENE PROTEINS C-KIT; RATS; RATS, WISTAR; SEMINIFEROUS TUBULES; SIGNAL TRANSDUCTION; STEM CELL FACTOR; TIME FACTORS; TISSUE CULTURE TECHNIQUES;

EID: 84903381688     PISSN: 00150282     EISSN: 15565653     Source Type: Journal    
DOI: 10.1016/j.fertnstert.2014.04.009     Document Type: Article

References (54)

1. E.F. Oakberg A description of spermiogenesis in the mouse and its use in analysis of the cycle of the seminiferous epithelium and germ cell renewal Am J Anat 99 1956 391 413
2. C.G. Print, and K.L. Loveland Germ cell suicide: new insights into apoptosis during spermatogenesis Bioessays 22 2000 423 430
3. W.W. Lin, D.J. Lamb, T.M. Wheeler, J. Abrams, L.I. Lipshultz, and E.D. Kim Apoptotic frequency is increased in spermatogenic maturation arrest and hypospermatogenic states J Urol 158 1997 1791 1793
4. S. Takagi, N. Itoh, M. Kimura, T. Sasao, and T. Tsukamoto Spermatogonial proliferation and apoptosis in hypospermatogenesis associated with nonobstructive azoospermia Fertil Steril 76 2001 901 907
5. H.L. Feng, J.I. Sandlow, A.E. Sparks, A. Sandra, and L.J. Zheng Decreased expression of the c-kit receptor is associated with increased apoptosis in subfertile human testes Fertil Steril 71 1999 85 89
6. S. Laurentino, J. Gonçalves, J.E. Cavaco, P.F. Oliveira, M.G. Alves, and M. de Sousa et al. Apoptosis-inhibitor Aven is downregulated in defective spermatogenesis and a novel estrogen target gene in mammalian testis Fertil Steril 96 2011 745 750
7. S.S. Laurentino, S. Correia, J.E. Cavaco, P.F. Oliveira, M. de Sousa, and A. Barros et al. Regucalcin, a calcium-binding protein with a role in male reproduction? Mol Hum Reprod 18 2012 161 170
8. 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 Fertil Steril 87 2007 547 553
9. S. Weikert, M. Schrader, M. Müller, H. Krause, and K. Miller Expression of the apoptosis inhibitor survivin in testicular tissue of infertile patients Int J Androl 27 2004 161 165
10. S. Chaki, M. Misro, D.K. Gautam, M. Kaushik, D. Ghosh, and G. Chainy Estradiol treatment induces testicular oxidative stress and germ cell apoptosis in rats Apoptosis 11 2006 1427 1437
11. D.P. Mishra, and C. Shaha Estrogen-induced Spermatogenic Cell Apoptosis Occurs via the Mitochondrial Pathway role of superoxide and nitric oxide J Biol Chem 280 2005 6181 6196
12. V. Simões, M. Alves, A. Martins, T. Dias, L. Rato, and S. Socorro et al. Regulation of apoptotic signaling pathways by 5α- dihydrotestosterone and 17β-estradiol in immature rat Sertoli cells J Steroid Biochem Mol Biol 135C 2012 15 23
13. R. D'Souza, M.K. Gill-Sharma, S. Pathak, N. Kedia, R. Kumar, and N. Balasinor Effect of high intratesticular estrogen on the seminiferous epithelium in adult male rats Mol Cell Endocrinol 241 2005 41 48
14. J. Toppari Environmental endocrine disrupters and disorders of sexual differentiation Semin Reprod Med 20 2002 305 312
15. O.A. Levalle, C. Zylbersztein, S. Aszpis, V. Mariani, R. Ponzio, and C. Aranda et al. Serum luteinizing hormone pulsatility and intratesticular testosterone and oestradiol concentrations in idiopathic infertile men with high and normal follicle stimulating hormone serum concentrations Hum Reprod 9 1994 781 787
16. M. Lardone, P. Castillo, R. Valdevenito, M. Ebensperger, A. Ronco, and R. Pommer et al. P450-Aromatase activity and expression in human testicular tissues with severe spermatogenic failure Int J Androl 33 2010 650 660
17. P. Rossi, C. Albanesi, P. Grimaldi, and R. Geremia Expression of the mRNA for the ligand of c-kit in mouse Sertoli cells Biochem Biophys Res Commun 176 1991 910 914
18. V. Sorrentino, M. Giorgi, R. Geremia, P. Besmer, and P. Rossi Expression of the c-kit proto-oncogene in the murine male germ cells Oncogene 6 1991 149 151
19. K. Yoshinaga, S. Nishikawa, M. Ogawa, S.I. Hayashi, T. Kunisada, and T. Fujimoto et al. Role of c-kit in mouse spermatogenesis - identification of spermatogonia as a specific site of c-kit expression and function Development 113 1991 689 699
20. F. Guerif, V. Cadoret, V. Rahal-Perola, J. Lansac, F. Bernex, and J.J. Panthier et al. Apoptosis, onset and maintenance of spermatogenesis: evidence for the involvement of Kit in Kit-haplodeficient mice Biol Reprod 67 2002 70 79
21. H. Ohta, K. Yomogida, K. Dohmae, and Y. Nishimune Regulation of proliferation and differentiation in spermatogonial stem cells: The role of c-kit and its ligand SCF Development 127 2000 2125 2131
22. W. Yan, J. Suominen, and J. Toppari Stem cell factor protects germ cells from apoptosis in vitro J Cell Sci 113 2000 161 168
23. M. Tanikawa, T. Harada, M. Mitsunari, Y. Onohara, T. Iwabe, and N. Terakawa Expression of c-kit messenger ribonucleic acid in human oocyte and presence of soluble c-kit in follicular fluid J Clin Endocrinol Metab 83 1998 1239 1242
24. D. Huansheng, P. Qingjie, Z. Hanqiong, Z. Lianjun, C. Bo, and Y. Wenbin Estrogen inhibits the early development of mouse follicles through regulating the expression of Kit ligand Biochem Biophys Res Commun 410 2011 659 664
25. R.X.-D. Song, G. Mor, F. Naftolin, R.A. McPherson, J. Song, and Z. Zhang et al. Effect of long-term estrogen deprivation on apoptotic responses of breast cancer cells to 17β-estradiol J Natl Cancer Inst 93 2001 1714 1723
26. G. Jaita, M. Candolfi, V. Zaldivar, S. Zárate, L. Ferrari, and D. Pisera et al. Estrogens up-regulate the Fas/FasL apoptotic pathway in lactotropes Endocrinology 146 2005 4737 4744
27. S.S. Laurentino, S. Correia, J.E. Cavaco, P.F. Oliveira, L. Rato, and M. Sousa et al. Regucalcin is broadly expressed in male reproductive tissues and is a new androgen-target gene in mammalian testis Reproduction 142 2011 447 456
28. V. Pentikäinen, K. Erkkilä, L. Suomalainen, M. Parvinen, and L. Dunkel Estradiol acts as a germ cell survival factor in the human testis in vitro J Clin Endocrinol Metab 85 2000 2057 2067
29. M. Zhao, S.D. Baker, X. Yan, Y. Zhao, W.W. Wright, and B.R. Zirkin et al. Simultaneous determination of steroid composition of human testicular fluid using liquid chromatography tandem mass spectrometry Steroids 69 2004 721 726
30. M. Roth, K. Lin, J. Amory, A. Matsumoto, B. Anawalt, and C. Snyder et al. Serum LH correlates highly with intratesticular steroid levels in normal men J Androl 31 2010 138 145
31. J. Hellemans, G. Mortier, A. De Paepe, F. Speleman, and J. Vandesompele qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data Genome Biol 8 2007 R19
32. 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 J Cell Biochem 112 2011 3872 3881
33. J. Lee, J.H. Richburg, S.C. Younkin, and K. Boekelheide The Fas system is a key regulator of germ cell apoptosis in the testis Endocrinology 138 1997 2081 2088
34. A. Lawen Apoptosis -An introduction Bioessays 25 2003 888 896
35. M. Harris, and C. Thompson The role of the Bcl-2 family in the regulation of outer mitochondrial membrane permeability Cell Death Differ 7 2000 1182 1191
36. T.J. Mackey, A. Borkowski, P. Amin, S.C. Jacobs, and N. Kyprianou bcl-2/bax ratio as a predictive marker for therapeutic response to radiotherapy in patients with prostate cancer Urology 52 1998 1085 1090
37. T. Strohmeyer, D. Reese, M. Press, R. Ackermann, M. Hartmann, and D. Slamon Expression of the c-kit proto-oncogene and its ligand stem cell factor (SCF) in normal and malignant human testicular tissue J Urol 153 1995 511 515
38. C. Bokemeyer, M.A. Kuczyk, T. Dunn, J. Serth, K. Hartmann, and J. Jonasson et al. Expression of stem-cell factor and its receptor c-kit protein in normal testicular tissue and malignant germ-cell tumours J Cancer Res Clin Oncol 122 1996 301 306
39. S.K. Unni, D.N. Modi, S.G. Pathak, J.V. Dhabalia, and D. Bhartiya Stage-specific localization and expression of c-kit in the adult human testis J Histochem Cytochem 57 2009 861 869
40. J. Gerdes, H. Lemke, H. Baisch, H.-H. Wacker, U. Schwab, and H. Stein Cell cycle analysis of a cell proliferation-Associated human nuclear antigen defined by the monoclonal antibody Ki-67 J Immunol 133 1984 1710 1715
41. Y. Tajima, H. Onoue, Y. Kitamura, and Y. Nishimune Biologically active kit ligand growth factor is produced by mouse Sertoli cells and is defective in SId mutant mice Development 113 1991 1031 1035
42. K. Manova, E.J. Huang, M. Angeles, V. De Leon, S. Sanchez, and S.M. Pronovost et al. The expression pattern of the c-kit ligand in gonads of mice supports a role for the c-kit receptor in oocyte growth and in proliferation of spermatogonia Dev Biol 157 1993 85 99
43. A. Chimento, R. Sirianni, C. Delalande, D. Silandre, C. Bois, and S. Andò et al. 17β-estradiol activates rapid signaling pathways involved in rat pachytene spermatocytes apoptosis through GPR30 and ERα Mol Cell Endocrinol 320 2010 136 144
44. J.M. Blechman, S. Lev, J. Barg, M. Eisenstein, B. Vaks, and Z. Vogel et al. The fourth immunoglobulin domain of the stem cell factor receptor couples ligand binding to signal transduction Cell 80 1995 103 113
45. H. Morimoto, M. Kanatsu-Shinohara, S. Takashima, S. Chuma, N. Nakatsuji, and M. Takehashi et al. Phenotypic plasticity of mouse spermatogonial stem cells PLoS One 4 2009 e7909
46. P. Blume-Jensen, G. Jiang, R. Hyman, K.-F. Lee, S. O'Gorman, and T. Hunter Kit/stem cell factor receptor-induced activation of phosphatidylinositol 3′-kinase is essential for male fertility Nat Genet 24 2000 157 162
47. L.-X. Feng, N. Ravindranath, and M. Dym Stem cell factor/c-kit up-regulates cyclin D3 and promotes cell cycle progression via the phosphoinositide 3-kinase/p70 S6 kinase pathway in spermatogonia J Biol Chem 275 2000 25572 25576
48. C. Lizama, D. Rojas-Benítez, M. Antonelli, A. Ludwig, X. Bustamante-Marín, and J. Brouwer-Visser et al. TACE/ADAM17 is involved in germ cell apoptosis during rat spermatogenesis Reproduction 140 2010 305 317
49. W. Yan, M. Samson, B. Jégou, and J. Toppari Bcl-w forms complexes with Bax and Bak, and elevated ratios of Bax/Bcl-w and Bak/Bcl-w correspond to spermatogonial and spermatocyte apoptosis in the testis Mol Endocrinol 14 2000 682 699
50. M.K. Dahmer Caspases-2, -3, and -7 are involved in thapsigargin-induced apoptosis of SH-SY5Y neuroblastoma cells J Neurosci Res 80 2005 576 583
51. A. Sugihara, S. Saiki, M. Tsuji, T. Tsujimura, Y. Nakata, and A. Kubota et al. Expression of Fas and Fas ligand in the testes and testicular germ cell tumors: An immunohistochemical study Anticancer Res 17 1997 3861 3865
52. D. Bellgrau, D. Gold, H. Selawry, J. Moore, A. Franzusoff, and R.C. Duke A role for CD95 ligand in preventing graft rejection Nature 377 1995 630 632
53. K.L. Porter, G. Shetty, G.A. Shuttlesworth, C.C. Weng, I. Huhtaniemi, and P. Pakarinen et al. Estrogen enhances recovery from radiation-induced spermatogonial arrest in rat testes J Androl 30 2009 440 451
54. O. Gregoriou, P. Bakas, C. Grigoriadis, M. Creatsa, D. Hassiakos, and G. Creatsas Changes in hormonal profile and seminal parameters with use of aromatase inhibitors in management of infertile men with low testosterone to estradiol ratios Fertil Steril 98 2012 48 51