Dehydroepiandrosterone sulfate mediates activation of transcription factors CREB and ATF-1 via a Gα11-coupled receptor in the spermatogenic cell line GC-2

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1833, Issue 12, 2013, Pages 3064-3075

  Shihan, Mazen ^a   Kirch, Ulrike ^a   Scheiner Bobis, Georgios ^a  

^a JUSTUS LIEBIG UNIVERSITY   (Germany)

Author keywords

Androgen receptor; ATF 1; CREB; DHEAS; Erk1 2; Gn 11; Signaling; Spermatogenic cells

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 1; ADENOSINE PHOSPHATE; ANDROGEN RECEPTOR; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; G PROTEIN COUPLED RECEPTOR; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT 11 PROTEIN; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PRASTERONE SULFATE; PROTEIN KINASE P60; SMALL INTERFERING RNA; STERYL SULFATASE; TESTOSTERONE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL LINE; CONTROLLED STUDY; CYTOSOL; ENZYME ACTIVATION; GENE SILENCING; INTRACELLULAR SIGNALING; MALE; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SPERMATOCYTE;

EID: 84884321113     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2013.08.015     Document Type: Article

References (47)

1. Burger H.G. Androgen production in women. Fertil. Steril. 2002, 77(Suppl. 4):S3-S5.
2. Chen F., Knecht K., Birzin E., Fisher J., Wilkinson H., Mojena M., Moreno C.T., Schmidt A., Harada S., Freedman L.P., Reszka A.A. Direct agonist/antagonist functions of dehydroepiandrosterone. Endocrinology 2005, 146:4568-4576.
3. Ebeling P., Koivisto V.A. Physiological importance of dehydroepiandrosterone. Lancet 1994, 343:1479-1481.
4. Mensah-Nyagan A.G., Do-Rego J.L., Beaujean D., Luu-The V., Pelletier G., Vaudry H. Neurosteroids: expression of steroidogenic enzymes and regulation of steroid biosynthesis in the central nervous system. Pharmacol. Rev. 1999, 51:63-81.
5. Maninger N., Wolkowitz O.M., Reus V.I., Epel E.S., Mellon S.H. Neurobiological and neuropsychiatric effects of dehydroepiandrosterone (DHEA) and DHEA sulfate (DHEAS). Front. Neuroendocrinol. 2009, 30:65-91.
6. Krug A.W., Langbein H., Ziegler C.G., Bornstein S.R., Eisenhofer G., Ehrhart-Bornstein M. Dehydroepiandrosterone-sulphate (DHEA-S) promotes neuroendocrine differentiation of chromaffin pheochromocytoma PC12 cells. Mol. Cell. Endocrinol. 2009, 300:126-131.
7. Ziegler C.G., Langbein H., Krug A.W., Ludwig B., Eisenhofer G., Ehrhart-Bornstein M., Bornstein S.R. Direct effect of dehydroepiandrosterone sulfate (DHEAS) on PC-12 cell differentiation processes. Mol. Cell. Endocrinol. 2011, 336:149-155.
8. Sicard F., Ehrhart-Bornstein M., Corbeil D., Sperber S., Krug A.W., Ziegler C.G., Rettori V., McCann S.M., Bornstein S.R. Age-dependent regulation of chromaffin cell proliferation by growth factors, dehydroepiandrosterone (DHEA), and DHEA sulfate. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:2007-2012.
9. Kurata K., Takebayashi M., Morinobu S., Yamawaki S. Beta-estradiol, dehydroepiandrosterone, and dehydroepiandrosterone sulfate protect against N-methyl-d-aspartate-induced neurotoxicity in rat hippocampal neurons by different mechanisms. J. Pharmacol. Exp. Ther. 2004, 311:237-245.
10. Nieschlag E., Loriaux D.L., Ruder H.J., Zucker I.R., Kirschner M.A., Lipsett M.B. The secretion of dehydroepiandrosterone and dehydroepiandrosterone sulphate in man. J. Endocrinol. 1973, 57:123-134.
11. Vermeulen A. Sex hormone status of the postmenopausal woman. Maturitas 1980, 2:81-89.
12. Webb S.J., Geoghegan T.E., Prough R.A., Michael Miller K.K. The biological actions of dehydroepiandrosterone involves multiple receptors. Drug Metab. Rev. 2006, 38:89-116.
13. Hofmann M.C., Narisawa S., Hess R.A., Millan J.L. Immortalization of germ cells and somatic testicular cells using the SV40 large T antigen. Exp. Cell Res. 1992, 201:417-435.
14. Woo L.W., Ganeshapillai D., Thomas M.P., Sutcliffe O.B., Malini B., Mahon M.F., Purohit A., Potter B.V. Structure-activity relationship for the first-in-class clinical steroid sulfatase inhibitor Irosustat (STX64, BN83495). ChemMedChem 2011, 6:2019-2034.
15. Valverde M.A., Parker M.G. Classical and novel steroid actions: a unified but complex view. Trends Biochem. Sci. 2002, 27:172-173.
16. Walker W.H. Molecular mechanisms of testosterone action in spermatogenesis. Steroids 2009, 74:602-607.
17. Walker W.H. Nongenomic actions of androgen in Sertoli cells. Curr. Top. Dev. Biol. 2003, 56:25-53.
18. Konrad L., Dietze R., Kirch U., Kirch H., Eva A., Scheiner-Bobis G. Cardiotonic steroids trigger non-classical testosterone signaling in Sertoli cells via the alpha4 isoform of the sodium pump. Biochim. Biophys. Acta 2011, 1813:2118-2124.
19. Lucas T.F., Royer C., Siu E.R., Lazari M.F., Porto C.S. Expression and signaling of G protein-coupled estrogen receptor 1 (GPER) in rat Sertoli cells. Biol. Reprod. 2010, 83:307-317.
20. Pena D., Pontillo C., Garcia M.A., Cocca C., Alvarez L., Chiappini F., Bourguignon N., Frahm I., Bergoc R., Kleiman de Pisarev D., Randi A. Alterations in c-Src/HER1 and estrogen receptor alpha signaling pathways in mammary gland and tumors of hexachlorobenzene-treated rats. Toxicology 2012, 293:68-77.
21. Dietze R., Konrad L., Shihan M., Kirch U., Scheiner-Bobis G. Cardiac glycoside ouabain induces activation of ATF-1 and StAR expression by interacting with the alpha4 isoform of the sodium pump in Sertoli cells. Biochim. Biophys. Acta 2013, 1833:511-519.
22. Grazzini E., Guillon G., Mouillac B., Zingg H.H. Inhibition of oxytocin receptor function by direct binding of progesterone. Nature 1998, 392:509-512.
23. Evans S.J., Murray T.F., Moore F.L. Partial purification and biochemical characterization of a membrane glucocorticoid receptor from an amphibian brain. J. Steroid Biochem. Mol. Biol. 2000, 72:209-221.
24. Rojas-Garcia P.P., Recabarren M.P., Sarabia L., Schon J., Gabler C., Einspanier R., Maliqueo M., Sir-Petermann T., Rey R., Recabarren S.E. Prenatal testosterone excess alters Sertoli and germ cell number and testicular FSH receptor expression in rams. Am. J. Physiol. Endocrinol. Metab. 2010, 299:E998-E1005.
25. Romero D.G., Zhou M.Y., Yanes L.L., Plonczynski M.W., Washington T.R., Gomez-Sanchez C.E., Gomez-Sanchez E.P. Regulators of G-protein signaling 4 in adrenal gland: localization, regulation, and role in aldosterone secretion. J. Endocrinol. 2007, 194:429-440.
26. Mizota K., Yoshida A., Uchida H., Fujita R., Ueda H. Novel type of Gq/11 protein-coupled neurosteroid receptor sensitive to endocrine disrupting chemicals in mast cell line (RBL-2H3). Br. J. Pharmacol. 2005, 145:545-550.
27. Hu Y., Xing J., Chen L., Guo X., Du Y., Zhao C., Zhu Y., Lin M., Zhou Z., Sha J. RGS22, a novel testis-specific regulator of G-protein signaling involved in human and mouse spermiogenesis along with GNA12/13 subunits. Biol. Reprod. 2008, 79:1021-1029.
28. Freeman M.R., Cinar B., Lu M.L. Membrane rafts as potential sites of nongenomic hormonal signaling in prostate cancer. Trends Endocrinol. Metab. 2005, 16:273-279.
29. Kato S., Masuhiro Y., Watanabe M., Kobayashi Y., Takeyama K.I., Endoh H., Yanagisawa J. Molecular mechanism of a cross-talk between oestrogen and growth factor signalling pathways. Genes Cells 2000, 5:593-601.
30. Simoncini T., Mannella P., Fornari L., Varone G., Caruso A., Genazzani A.R. Dehydroepiandrosterone modulates endothelial nitric oxide synthesis via direct genomic and nongenomic mechanisms. Endocrinology 2003, 144:3449-3455.
31. Charalampopoulos I., Margioris A.N., Gravanis A. Neurosteroid dehydroepiandrosterone exerts anti-apoptotic effects by membrane-mediated, integrated genomic and non-genomic pro-survival signaling pathways. J. Neurochem. 2008, 107:1457-1469.
32. Payne A.H. Testicular steroid sulfotransferases: comparison to liver and adrenal steroid sulfotransferases of the mature rat. Endocrinology 1980, 106:1365-1370.
33. Dufort I., Tremblay Y., Belanger A., Labrie F., Luu-The V. Isolation and characterization of a stereospecific 3beta-hydroxysteriod sulfotransferase (pregnenolone sulfotransferase) cDNA. DNA Cell Biol. 1996, 15:481-487.
34. Almog T., Naor Z. Mitogen activated protein kinases (MAPKs) as regulators of spermatogenesis and spermatozoa functions. Mol. Cell. Endocrinol. 2008, 282:39-44.
35. Li M.W., Mruk D.D., Cheng C.Y. Mitogen-activated protein kinases in male reproductive function. Trends Mol. Med. 2009, 15:159-168.
36. Sette C., Barchi M., Bianchini A., Conti M., Rossi P., Geremia R. Activation of the mitogen-activated protein kinase ERK1 during meiotic progression of mouse pachytene spermatocytes. J. Biol. Chem. 1999, 274:33571-33579.
37. Di Agostino S., Botti F., Di Carlo A., Sette C., Geremia R. Meiotic progression of isolated mouse spermatocytes under simulated microgravity. Reproduction 2004, 128:25-32.
38. Faivre E.J., Lange C.A. Progesterone receptors upregulate Wnt-1 to induce epidermal growth factor receptor transactivation and c-Src-dependent sustained activation of Erk1/2 mitogen-activated protein kinase in breast cancer cells. Mol. Cell. Biol. 2007, 27:466-480.
39. Servillo G., Della Fazia M.A., Sassone-Corsi P. Coupling cAMP signaling to transcription in the liver: pivotal role of CREB and CREM. Exp. Cell Res. 2002, 275:143-154.
40. Shell S.A., Fix C., Olejniczak D., Gram-Humphrey N., Walker W.H. Regulation of cyclic adenosine 3',5'-monophosphate response element binding protein (CREB) expression by Sp1 in the mammalian testis. Biol. Reprod. 2002, 66:659-666.
41. El-Alfy M., Azzi L., Lessard J., Lavergne E., Pelletier M., Labrie C. Stage-specific expression of the Atce1/Tisp40alpha isoform of CREB3L4 in mouse spermatids. J. Androl. 2006, 27:686-694.
42. Kim J.S., Song M.S., Seo H.S., Yang M., Kim S.H., Kim J.C., Kim H., Saito T.R., Shin T., Moon C. Immunohistochemical analysis of cAMP response element-binding protein in mouse testis during postnatal development and spermatogenesis. Histochem. Cell Biol. 2009, 131:501-507.
43. Scobey M., Bertera S., Somers J., Watkins S., Zeleznik A., Walker W. Delivery of a cyclic adenosine 3',5'-monophosphate response element-binding protein (CREB) mutant to seminiferous tubules results in impaired spermatogenesis. Endocrinology 2001, 142:948-954.
44. Walker W.H. Non-classical actions of testosterone and spermatogenesis. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2010, 365:1557-1569.
45. Coso O.A., Chiariello M., Kalinec G., Kyriakis J.M., Woodgett J., Gutkind J.S. Transforming G protein-coupled receptors potently activate JNK (SAPK). Evidence for a divergence from the tyrosine kinase signaling pathway. J. Biol. Chem. 1995, 270:5620-5624.
46. Seo B., Choy E.W., Maudsley S., Miller W.E., Wilson B.A., Luttrell L.M. Pasteurella multocida toxin stimulates mitogen-activated protein kinase via G(q/11)-dependent transactivation of the epidermal growth factor receptor. J. Biol. Chem. 2000, 275:2239-2245.
47. Hubbard K.B., Hepler J.R. Cell signalling diversity of the Gqalpha family of heterotrimeric G proteins. Cell. Signal. 2006, 18:135-150.