Luteinizing hormone regulates inhibin-α subunit expression through multiple signaling pathways involving steroidogenic factor-1 and beta-catenin in the macaque corpus luteum

References

• Anttonen M, Parviainen H, Kyrönlahti A, Bielinska M, Wilson DB, Ritvos O, Heikinheimo M. 2006. GATA-4 is a granulosa cell factor employed in inhibin-alpha activation by the TGF-beta pathway. J Mol Endocrinol. 36:557–568.
   PubMed Web of Science ®Google Scholar
• Basseti SG, Winters SJ, Keeping HS, Zeleznik AJ. 1990. Serum immunoreactive inhibin levels before and after luteectomy in the cynomolgus monkey (Macaca fascicularis). J Clin Endocrinol Metab. 70:590–594.
   Google Scholar
• Boerboom D, Boerboom D, Paquet M, Hsieh M, Liu J, Jamin SP, Behringer RR, Sirois J, Taketo MM, Richards JS. 2005. Misregulated Wnt/beta-catenin signaling leads to ovarian granulosa cell tumor development. Cancer Res. 65:9206–9215.
   PubMed Web of Science ®Google Scholar
• Burkart AD, Mukherjee A, Mayo KE. 2006. Mechanism of repression of the inhibin alpha-subunit gene by inducible 3′,5′-cyclic adenosine monophosphate early repressor. Mol Endocrinol. 20:584–597.
   PubMedGoogle Scholar
• Burkart AD, Mukherjee A, Sterneck E, Johnson PF, Mayo KE. 2005. Repression of the inhibin alpha-subunit gene by the transcription factor CCAAT/enhancer-binding protein-beta. Endocrinology. 146:1909–1921.
   Google Scholar
• Desclozeaux M, Krylova IN, Horn F, Fletterick RJ, Ingraham HA. 2002. Phosphorylation and intramolecular stabilization of the ligand binding domain in the nuclear receptor steroidogenic factor 1. Mol Cell Biol.. 22:7193–7203.
   PubMed Web of Science ®Google Scholar
• Dewi DA, Abayasekara DR, Wheeler-Jones CP. 2002. Requirement for ERK1/2 activation in the regulation of progesterone production in human granulosa-lutein cells is stimulus specific. Endocrinology. 143:877–888.
   PubMed Web of Science ®Google Scholar
• Easwaran V, Pishvaian M, Salimuddin, Byers S. 1999. Cross-regulation of beta-catenin-LEF/TCF and retinoid signaling pathways. Curr Biol. 9:1415–1418.
   PubMed Web of Science ®Google Scholar
• Eramaa M, Heikinheimo K, Tuuri T, Hilden K, Ritvos O. 1993. Inhibin/activin subunit mRNA expression in human granulosa-luteal cells. Mol Cell Endocrinol. 92:R15–R20.
   PubMedGoogle Scholar
• Feng ZM, Wu AZ, Chen CL. 1998. Testicular GATA-1 factor up-regulates the promoter activity of rat inhibin alpha-subunit gene in MA-10 Leydig tumor cells. Mol Endocrinol. 12:378–390.
   PubMedGoogle Scholar
• Fowkes RC, Desclozeaux M, Patel MV, Aylwin SJ, King P, Ingraham HA, Burrin JM. 2003. Steroidogenic factor-1 and the gonadotrope-specific element enhance basal and pituitary adenylate cyclase-activating polypeptide-stimulated transcription of the human glycoprotein hormone alpha-subunit gene in gonadotropes. Mol Endocrinol. 17:2177–2188.
   PubMedGoogle Scholar
• Fraser HM, Lunn SF, Cowen GM, Saunders PT. 1993. Localization of inhibin/activin subunit mRNAs during the luteal phase in the primate ovary. J Mol Endocrinol. 10:245–257.
   Google Scholar
• Fraser HM, Robertson DM, De Kretser DM. 1989. Immunoreactive inhibin concentrations in serum throughout the menstrual cycle of the macaque: suppression of inhibin during the luteal phase after treatment with an LHRH antagonist. J Endocrinol. 121:R9–12.
   Google Scholar
• Gillio-Meina C, Hui YY, LaVoie HA. 2003. GATA-4 and GATA-6 transcription factors: Expression, immunohistochemical localization, and possible function in the porcine ovary. Biol Reprod. 68:412–422.
   PubMed Web of Science ®Google Scholar
• Gummow BM, Winnay JN, Hammer GD. 2003. Convergence of Wnt signaling and steroidogenic factor-1 (SF-1) on transcription of the rat inhibin alpha gene. J Biol Chem. 278:26572–26579.
   Google Scholar
• Green N, Alexander H, Olson A, Alexander S, Shinnick TM, Sutcliffe JG, Lerner RA. 1982. Immunogenic structure of the influenza virus hemagglutinin. Cell. 28:477–487.
   PubMed Web of Science ®Google Scholar
• Hammer GD, Krylova I, Zhang Y, Darimont BD, Simpson K, Weigel NL, Ingraham HA. 1999. Phosphorylation of the nuclear receptor SF-1 modulates cofactor recruitment: Integration of hormone signaling in reproduction and stress. Mol Cell. 3:521–526.
   PubMed Web of Science ®Google Scholar
• Heikkila M, Peltoketo H, Leppaluoto J, Ilves M, Vuolteenaho O, Vainio S. 2002. Wnt-4 deficiency alters mouse adrenal cortex function, reducing aldosterone production. Endocrinology. 143:4358–4365.
   PubMed Web of Science ®Google Scholar
• Ito M, Park Y, Weck J, Mayo KE, Jameson JL. 2000. Synergistic activation of the inhibin alpha-promoter by steroidogenic factor-1 and cyclic adenosine 3′,5′-monophosphate. Mol Endocrinol. 14:66–81.
   PubMedGoogle Scholar
• Jeyasuria P, Ikeda Y, Jasmin SP, Zhao L, De Rooij DG, Themmen AP, Behringer RR, Parker KL. 2004. Cell-specific knockout steroidogenic factor 1 reveals its essential role in gonadal function. Mol Endocrinol. 18:1610–1619.
   PubMed Web of Science ®Google Scholar
• Jiang J, Luo G. 2009. Apolipoprotein E but not B is required for the formation of infectious Hepatitis C virus particles. J Virol. 83:12680–12691.
   PubMed Web of Science ®Google Scholar
• Little TH, Zhang Y, Matulis CK, Weck J, Zhang Z, Ramachandran A, Mayo KE, Radhakrishnan I. 2006. Sequence-specific deoxyribonucleic acid (DNA) recognition by steroidogenic factor 1: A helix at the carboxy terminus of the DNA binding domain is necessary for complex stability. Mol Endocrinol. 20:831–843.
   PubMedGoogle Scholar
• Lockwood G. 2004. The diagnostic value of inhibin in infertility evaluation. Semin Reprod Med. 22:195–208.
   Google Scholar
• Luo X, Kiss A, Makara G, Lolait SJ, Aguilera G. 1994. Stress-specific regulation of corticotropin releasing hormone receptor expression in the paraventricular and supraoptic nuclei of the hypothalamus in the rat. J Neuroendocrinol. 6:689–696.
   PubMed Web of Science ®Google Scholar
• Matzuk MM, Finegold MJ, Su JG, Hsueh AJ, Bradley A. 1992. Alpha-inhibin is a tumour-suppressor gene with gonadal specificity in mice. Nature. 360:313–319.
   PubMed Web of Science ®Google Scholar
• Matzuk MM, Kumar TR, Shou W, Coerver KA, Lau AL, Behringer RR, Finegold MJ. 1996. Transgenic models to study the roles of inhibins and activins in reproduction, oncogenesis, and development. Recent Prog Horm Res. 51:123–154.
   PubMedGoogle Scholar
• Maizels ET, Mukherjee A, Sithanandam G, Peters CA, Cottom J, Mayo KE, Hunzicker-Dunn M. 2001. Developmental regulation of mitogen-activated protein kinase-activated kinases-2 and -3 (MAPKAPK-2/-3) in vivo during corpus luteum formation in the rat. Mol Endocrinol. 15:716–733.
   PubMedGoogle Scholar
• Miyagishi M, Fujii R, Hatta M, Yoshida E, Araya N, Nagafuchi A, Ishihara S, Nakajima T, Fukamizu A. 2000. Regulation of Lef-mediated transcription and p53-dependent pathway by associating beta-catenin with CBP/p300. J Biol Chem. 275:35170–35175.
   PubMedGoogle Scholar
• Mizusaki H, Kawabe K, Mukai T, Ariyoshi E, Kasahara M, Yoshioka H, Swain A, Morohashi K. 2003. Dax-1 (dosage-sensitive sex reversal-adrenal hypoplasia congenita critical region on the X chromosome, gene 1) gene transcription is regulated by wnt4 in the female developing gonad. Mol Endocrinol. 17:507–519.
   PubMedGoogle Scholar
• Mukherjee A, Urban J, Sassone-Corsi P, Mayo KE. 1998. Gonadotropins regulate inducible cyclic adenosine 3′,5′-monophosphate early repressor in the rat ovary: Implications for inhibin alpha subunit gene expression. Mol Endocrinol. 12:785–800.
   PubMedGoogle Scholar
• Mulholland DJ, Cheng H, Reid K, Rennie PS, Nelson CC. 2002. The androgen receptor can promote beta-catenin nuclear translocation independently of adenomatous polyposis coli. J Biol Chem. 277:17933–17943.
   PubMed Web of Science ®Google Scholar
• Muttukrishna S, Fowler PA, George L, Groome NP, Knight PG. 1996. Changes in peripheral serum levels of total activin A during the human menstrual cycle and pregnancy. J Clin Endocrinol Metab. 81:3328–3334.
   PubMedGoogle Scholar
• Myers M, Gay E, McNeilly AS, Fraser HM, Duncan WC. 2007. In vitro evidence suggests activin-A may promote tissue remodeling associated with human luteolysis. Endocrinology. 148:3730–3739.
   Google Scholar
• Parakh TN, Hernandez JA, Grammer JC, Weck J, Hunzicker-Dunn M, Zeleznik AJ, Nilson JH. 2006. Follicle-stimulating hormone/cAMP regulation of aromatase gene expression requires beta-catenin. Proc Natl Acad Sci USA. 103:12435–12440.
   Google Scholar
• Pawlowski JE, Ertel JR, Allen MP, Xu M, Butler C, Wilson EM, Wierman ME. 2002. Liganded androgen receptor interaction with beta-catenin: Nuclear co-localization and modulation of transcriptional activity in neuronal cells. J Biol Chem. 277:20702–20710.
   PubMed Web of Science ®Google Scholar
• Pei L, Dodson R, Schoderbek WE, Maurer RA, Mayo KE. 1991. Regulation of the alpha inhibin gene by cyclic adenosine 3′,5′-monophosphate after transfection into rat granulosa cells. Mol Endocrinol. 5:521–534.
   PubMedGoogle Scholar
• Peng N, Kim JW, Rainey WE, Carr BR, Attia GR. 2003. The role of the orphan nuclear receptor, liver receptor homologue-1, in the regulation of human corpus luteum 3beta-hydroxysteroid dehydrogenase type II. J Clin Endocrinol Metab.. 88:6020–6028.
   PubMedGoogle Scholar
• Priyanka S, Medhamurthy R. 2007. Characterization of cAMP/PKA/CREB signaling cascade in the bonnet monkey corpus luteum: expressions of inhibin-alpha and StAR during different functional status. Mol Hum Reprod. 13:381–390.
   Google Scholar
• Priyanka S, Jayaram P, Sridaran R, Medhamurthy R. 2009. Genome-wide gene expression analysis reveals a dynamic interplay between luteotropic and luteolytic factors in the regulation of corpus luteum function in the bonnet monkey (Macaca radiata). Endocrinology. 150:1473–1484.
   PubMed Web of Science ®Google Scholar
• Richards JS, Russell DL, Ochsner S, Hsieh M, Doyle KH, Falender AE, Lo YK, Sharma SC. 2002. Novel signaling pathways that control ovarian follicular development, ovulation, and luteinization. Recent Prog Horm Res. 57:195–220.
   PubMedGoogle Scholar
• Robert NM, Miyamoto Y, Taniguchi H, Viger RS. 2006. LRH-1/NR5A2 cooperates with GATA factors to regulate inhibin alpha-subunit promoter activity. Mol Cell Endocrinol. 257-258:65–74.
   Google Scholar
• Roy L, McDonald CA, Jiang C, Maroni D, Zeleznik AJ, Wyatt TA, Hou X, Davis JS. 2009. Convergence of 3′,5′-cyclic adenosine 5′-monophosphate/protein kinase A and glycogen synthase kinase-3beta/beta-catenin signaling in corpus luteum progesterone synthesis. Endocrinology. 150:5036–5045.
   Google Scholar
• Salvador LM, Maizels E, Hales DB, Miyamoto E, Yamamoto H, Hunzicker-Dunn M. 2002. Acute signaling by the LH receptor is independent of protein kinase C activation. Endocrinology. 143:2986–2994.
   Google Scholar
• Smith KB, Millar MR, McNeilly AS, Illingworth PJ, Fraser HM, Baird DT. 1991. Immunocytochemical localization of inhibin alpha-subunit in the human corpus luteum. J Endocrinol. 129:155–160.
   Google Scholar
• Stenvers Findlay. 2010. Inhibins: from reproductive hormones to tumour suppressors. Trends Endocrinol Metab. 21:174–180.
   Google Scholar
• Suresh PS, Jayachandra KC, Medhamurthy R. 2011. The effect of progesterone replacement on gene expression in the corpus luteum during induced regression and late luteal phase in the bonnet monkey (Macaca radiata). Reprod Biol Endocrinol 2011. 9:20.
   Google Scholar
• Suresh PS, Medhamurthy R. 2009. Dynamics of circulating concentrations of gonadotropins and ovarian hormones throughout the menstrual cycle in the bonnet monkey: Role of inhibin A in the regulation of follicle-stimulating hormone secretion. Am J Primatol. 71:817–824.
   PubMed Web of Science ®Google Scholar
• Taniguchi H, Komiyama J, Viger RS, Okuda K. 2009. The expression of the nuclear receptors NR5A1 and NR5A2 and transcription factor GATA6 correlates with steroidogenic gene expression in the bovine corpus luteum. Mol Reprod Dev. 76:873–880.
   Google Scholar
• Tremblay JJ, Viger RS. 2001. GATA factors differentially activate multiple gonadal promoters through conserved GATA regulatory elements. Endocrinology. 142:977–986.
   PubMed Web of Science ®Google Scholar
• Tremblay JJ, Viger RS. 2003. Transcription factor GATA-4 is activated by phosphorylation of serine 261 via the cAMP/protein kinase a signaling pathway in gonadal cells. J Biol Chem. 278:22128–22135.
   PubMed Web of Science ®Google Scholar
• Truica CI, Byers S, Gelmann EP. 2000. Beta-catenin affects androgen receptor transcriptional activity and ligand specificity. Cancer Res. 60:4709–4713.
   PubMed Web of Science ®Google Scholar
• Walter G, Scheidtmann KH, Carbone A, Laudano AP, Doolittle RF. 1980. Antibodies specific for the carboxy- and amino-terminal regions of simian virus 40 large tumor antigen. Proc Natl Acad Sci USA. 77:5197–5200.
   PubMed Web of Science ®Google Scholar
• Weck J, Mayo KE. 2006. Switching of NR5A proteins associated with the inhibin alpha-subunit gene promoter after activation of the gene in granulosa cells. Mol Endocrinol. 20:1090–1103.
   Google Scholar
• Yadav VK, Medhamurthy R. 2006. Dynamic changes in mitogen-activated protein kinase (MAPK) activities in the corpus luteum of the bonnet monkey (Macaca radiata) during development, induced luteolysis, and simulated early pregnancy: A role for p38 MAPK in the regulation of luteal function. Endocrinology. 147:2018–2027.
   PubMed Web of Science ®Google Scholar
• Yadav VK, Sudhagar RR, Medhamurthy R. 2002. Apoptosis during spontaneous and prostaglandinF(2alpha)-induced luteal regression in the buffalo cow (Bubalus bubalis): Involvement of mitogen-activated protein kinases. Biol Reprod. 67:752–759.
   PubMed Web of Science ®Google Scholar
• Yang F, Li X, Sharma M, Sasaki CY, Longo DL, Lim B, Sun Z. 2002. Linking beta-catenin to androgen-signaling pathway. J Biol Chem. 277:11336–11344.
   PubMed Web of Science ®Google Scholar
• Zhao C, Barner R, Vinh TN, McManus K, Dabbs D, Vang R. 2008. SF-1 is a diagnostically useful immunohistochemical marker and comparable to other sex cord-stromal tumor markers for the differential diagnosis of ovarian sertoli cells tumor. Int J Gynecol Pathol. 27:507–514.
   Google Scholar