Essential Role of the Homeodomain for Pituitary Homeobox 1 Activation of Mouse Gonadotropin-Releasing Hormone Receptor Gene Expression through Interactions with c-Jun and DNA

REFERENCES

• Albarracin, C. T., Kaiser U. B., and Chin W. W.. 1994. Isolation and characterization of the 5′-flanking region of the mouse gonadotropin-releasing hormone receptor gene. Endocrinology 135:2300–2306.
   PubMedGoogle Scholar
• Ando, H., Hew C. L., and Urano A.. 2001. Signal transduction pathways and transcription factors involved in the gonadotropin-releasing hormone-stimulated gonadotropin subunit gene expression. Comp. Biochem. Physiol. B 129:525–532.
   PubMedGoogle Scholar
• Bach, I., Carrière C., Ostendorff H. P., Andersen B., and Rosenfeld M. G.. 1997. A family of LIM domain-associated cofactors confer transcriptional synergism between LIM and Otx homeodomain proteins. Genes Dev. 11:1370–1380.
   PubMedGoogle Scholar
• Basuyaux, J. P., Ferreira E., Stéhelin D., and Butticè G.. 1997. The Ets transcription factors interact with each other and with the c-Fos/c-Jun complex via distinct protein domains in a DNA-dependent and -independent manner. J. Biol. Chem. 272:26188–26195.
   PubMed Web of Science ®Google Scholar
• Boyd, K. E., and Farnham P. J.. 1999. Coexamination of site-specific transcription factor binding and promoter activity in living cells. Mol. Cell. Biol. 19:8393–8399.
   PubMedGoogle Scholar
• Cesnjaj, M., Catt K. J., and Stojilkovic S. S.. 1994. Coordinate actions of calcium and protein kinase-C in the expression of primary response genes in pituitary gonadotrophs. Endocrinology 135:692–701.
   PubMedGoogle Scholar
• Chi, L., Zhou W., Prikhozhan A., Flanagan C., Davidson J. S., Golembo M., Illing N., Millar R. P., and Sealfon S. C.. 1993. Cloning and characterization of the human GnRH receptor. Mol. Cell. Endocrinol. 91:R1–R6.
   PubMed Web of Science ®Google Scholar
• Duval, D. L., Nelson S. E., and Clay C. M.. 1997. A binding site for steroidogenic factor-1 is part of a complex enhancer that mediates expression of the murine gonadotropin-releasing hormone receptor gene. Biol. Reprod. 56:160–168.
   PubMedGoogle Scholar
• Duval, D. L., Nelson S. E., and Clay C. M.. 1997. The tripartite basal enhancer of the gonadotropin-releasing hormone (GnRH) receptor gene promoter regulates cell-specific expression through a novel GnRH receptor activating sequence. Mol. Endocrinol. 11:1814–1821.
   PubMedGoogle Scholar
• Eidne, K. A., Sellar R. E., Couper G., Anderson L., and Taylor P. L.. 1992. Molecular cloning and characterisation of the rat pituitary gonadotropin-releasing hormone (GnRH) receptor. Mol. Cell. Endocrinol. 90:R5–R9.
   PubMedGoogle Scholar
• Ellsworth, B. S., White B. R., Burns A. T., Cherrington B. D., Otis A. M., and Clay C. M.. 2003. c-Jun N-terminal kinase activation of activator protein-1 underlies homologous regulation of the gonadotropin-releasing hormone receptor gene in αT3-1 cells. Endocrinology 144:839–849.
   PubMedGoogle Scholar
• Gharib, S. D., Wierman M. E., Shupnik M. A., and Chin W. W.. 1990. Molecular biology of the pituitary gonadotropins. Endocr. Rev. 11:177–199.
   PubMed Web of Science ®Google Scholar
• Halvorson, L. M., Kaiser U. B., and Chin W. W.. 1996. Stimulation of luteinizing hormone β gene promoter activity by the orphan nuclear receptor, steroidogenic factor-1. J. Biol. Chem. 271:6645–6650.
   PubMedGoogle Scholar
• Illing, N., Jacobs G. F., Becker I. I., Flanagan C. A., Davidson J. S., Eales A., Zhou W., Sealfon S. C., and Millar R. P.. 1993. Comparative sequence analysis and functional characterization of the cloned sheep gonadotropin-releasing hormone receptor reveal differences in primary structure and ligand specificity among mammalian receptors. Biochem. Biophys. Res. Commun. 196:745–751.
   PubMedGoogle Scholar
• Jakacka, M., Ito M., Weiss J., Chien P.-Y., Gehm B. D., and Jameson J. L.. 2001. Estrogen receptor binding to DNA is not required for its activity through the nonclassical AP1 pathway. J. Biol. Chem. 276:13615–13621.
   PubMed Web of Science ®Google Scholar
• Kaiser, U. B., Conn P. M., and Chin W. W.. 1997. Studies of gonadotropin-releasing hormone (GnRH) action using GnRH receptor-expressing pituitary cell lines. Endocr. Rev. 18:46–70.
   PubMed Web of Science ®Google Scholar
• Kaiser, U. B., Sabbagh E., Katzenellenbogen R. A., Conn P. M., and Chin W. W.. 1995. A mechanism for the differential regulation of gonadotropin subunit gene expression by gonadotropin-releasing hormone. Proc. Natl. Acad. Sci. USA 92:12280–12284.
   PubMedGoogle Scholar
• Kaiser, U. B., Zhao D., Cardona G. R., and Chin W. W.. 1992. Isolation and characterization of cDNAs encoding the rat pituitary gonadotropin-releasing hormone receptor. Biochem. Biophys. Res. Commun. 189:1645–1652.
   PubMedGoogle Scholar
• Kakar, S. S., Musgrove L. C., Devor D. C., Sellers J. C., and Neill J. D.. 1992. Cloning, sequencing, and expression of human gonadotropin-releasing hormone (GnRH) receptor. Biochem. Biophys. Res. Commun. 189:289–295.
   PubMed Web of Science ®Google Scholar
• Kakar, S. S., Rahe C. H., and Neill J. D.. 1993. Molecular cloning, sequencing, and characterizing the bovine receptor for gonadotropin releasing hormone (GnRH). Domest. Anim. Endocrinol. 10:335–342.
   PubMed Web of Science ®Google Scholar
• Ko, L., Cardona G. R., Henrion-Caude A., and Chin W. W.. 2002. Identification and characterization of a tissue-specific coactivator, GT198, that interacts with the DNA-binding domains of nuclear receptors. Mol. Cell. Biol. 22:357–369.
   PubMedGoogle Scholar
• Lamonerie, T., Tremblay J. J., Lanctôt C., Therrien M., Gauthier Y., and Drouin J.. 1996. Ptx1, a bicoid-related homeo box transcription factor involved in transcription of the pro-opiomelanocortin gene. Genes Dev. 10:1284–1295.
   PubMed Web of Science ®Google Scholar
• Lilie, H., Schwarz E., and Rudolph R.. 1998. Advances in refolding of proteins produced in E. coli. Curr. Opin. Biotechnol. 9:497–501.
   PubMed Web of Science ®Google Scholar
• Mathur, M., Tucker P. W., and Samuels H. H.. 2001. PSF is a novel corepressor that mediates its effect through Sin3A and the DNA binding domain of nuclear hormone receptors. Mol. Cell. Biol. 21:2298–2311.
   PubMedGoogle Scholar
• Melamed, P., Koh M., Preklathan P., Bei L., and Hew C.. 2002. Multiple mechanisms for Pitx-1 transactivation of a luteinizing hormone β subunit gene. J. Biol. Chem. 277:26200–26207.
   PubMedGoogle Scholar
• Mercer, J. E., and Chin W. W.. 1995. Regulation of pituitary gonadotrophin gene expression. Hum. Reprod. Update 1:363–384.
   PubMedGoogle Scholar
• Moilanen, A.-M., Poukka H., Karvonen U., Häkli M., Jänne O. A., and Palvimo J. J.. 1998. Identification of a novel RING finger protein as a coregulator in steroid receptor-mediated gene transcription. Mol. Cell. Biol. 18:5128–5139.
   PubMed Web of Science ®Google Scholar
• Mulvaney, J. M., and Roberson M. S.. 2000. Divergent signaling pathways requiring discrete calcium signals mediate concurrent activation of two mitogen-activated protein kinases by gonadotropin-releasing hormone. J. Biol. Chem. 275:14182–14189.
   PubMedGoogle Scholar
• Nordeen, S. K. 1988. Luciferase reporter gene vectors for analysis of promoters and enhancers. BioTechniques 6:454–458.
   PubMed Web of Science ®Google Scholar
• Norwitz, E. R., Cardona G. R., Jeong K.-H., and Chin W. W.. 1999. Identification and characterization of the gonadotropin-releasing hormone response elements in the mouse gonadotropin-releasing hormone receptor gene. J. Biol. Chem. 274:867–880.
   PubMedGoogle Scholar
• Norwitz, E. R., Jeong K.-H., and Chin W. W.. 1999. Molecular mechanisms of gonadotropin-releasing hormone receptor gene regulation. J. Soc. Gynecol. Investig. 6:169–178.
   PubMedGoogle Scholar
• Norwitz, E. R., Xu S., Xu J., Spiryda L. B., Park J. S., Jeong K.-H., McGee E. A., and Kaiser U. B.. 2002. Direct binding of AP-1 (Fos/Jun) proteins to a SMAD binding element facilitates both gonadotropin-releasing hormone (GnRH)- and activin-mediated transcriptional activation of the mouse GnRH receptor gene. J. Biol. Chem. 277:37469–37478.
   PubMedGoogle Scholar
• Paech, K., Webb P., Kuiper G. G. J. M., Nilsson S., Gustafsson J.-A., Kushner P. J., and Scanlan T. S.. 1997. Differential ligand activation of estrogen receptors ERα and ERβ at AP1 sites. Science 277:1508–1510.
   PubMed Web of Science ®Google Scholar
• Poulin, G., Lebel M., Chamberland M., Paradis F. W., and Drouin J.. 2000. Specific protein-protein interaction between basic helix-loop-helix transcription factors and homeoproteins of the Pitx family. Mol. Cell. Biol. 20:4826–4837.
   PubMed Web of Science ®Google Scholar
• Quirk, C. C., Lozada K. L., Keri R. A., and Nilson J. H.. 2001. A single Pitx1 binding site is essential for activity of the LHβ promoter in transgenic mice. Mol. Endocrinol. 15:734–746.
   PubMedGoogle Scholar
• Reinhart, J., Mertz L. M., and Catt K. J.. 1992. Molecular cloning and expression of cDNA encoding the murine gonadotropin-releasing hormone receptor. J. Biol. Chem. 267:21281–21284.
   PubMed Web of Science ®Google Scholar
• Rosenberg, S. B., and Mellon P. L.. 2002. An Otx-related homeodomain protein binds an LHβ promoter element important for activation during gonadotrope maturation. Mol. Endocrinol. 16:1280–1298.
   PubMedGoogle Scholar
• Saadi, I., Kuburas A., Engle J. J., and Russo A. F.. 2003. Dominant negative dimerization of a mutant homeodomain protein in Axenfeld-Rieger syndrome. Mol. Cell. Biol. 23:1968–1982.
   PubMedGoogle Scholar
• Sanger, F., Nicklen S., and Coulson A. R.. 1977. DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. USA 74:5463–5467.
   PubMed Web of Science ®Google Scholar
• Shang, Y., Hu X., DiRenzo J., Lazar M. A., and Brown M.. 2000. Cofactor dynamics and sufficiency in estrogen receptor-regulated transcription. Cell 103:843–852.
   PubMed Web of Science ®Google Scholar
• Stanislaus, D., Ponder S., Ji T. H., and Conn P. M.. 1998. Gonadotropin-releasing hormone receptor couples to multiple G proteins in rat gonadotrophs and in GGH3 cells: evidence from palmitoylation and overexpression of G proteins. Biol. Reprod. 59:579–586.
   PubMed Web of Science ®Google Scholar
• Szeto, D. P., Rodriguez-Esteban C., Ryan A. K., O'Connell S. M., Liu F., Kioussi C., Gleiberman A. S., Izpisúa-Belmonte J. C., and Rosenfeld M. G.. 1999. Role of the bicoid-related homeodomain factor Pitx1 in specifying hindlimb morphogenesis and pituitary development. Genes Dev. 13:484–494.
   PubMed Web of Science ®Google Scholar
• Szeto, D. P., Ryan A. K., O'Connell S. M., and Rosenfeld M. G.. 1996. P-OTX: a PIT-1-interacting homeodomain factor expressed during anterior pituitary gland development. Proc. Natl. Acad. Sci. USA 93:7706–7710.
   PubMed Web of Science ®Google Scholar
• Therrien, M., and Drouin J.. 1993. Cell-specific helix-loop-helix factor required for pituitary expression of the pro-opiomelanocortin gene. Mol. Cell. Biol. 13:2342–2353.
   PubMedGoogle Scholar
• Tremblay, J. J., and Drouin J.. 1999. Egr-1 is a downstream effector of GnRH and synergizes by direct interaction with Ptx1 and SF-1 to enhance luteinizing hormone β gene transcription. Mol. Cell. Biol. 19:2567–2576.
   PubMed Web of Science ®Google Scholar
• Tremblay, J. J., Lanctôt C., and Drouin J.. 1998. The pan-pituitary activator of transcription, Ptx1 (pituitary homeobox 1), acts in synergy with SF-1 and Pit1 and is an upstream regulator of the Lim-homeodomain gene Lim3/Lhx3. Mol. Endocrinol. 12:428–441.
   PubMedGoogle Scholar
• Tremblay, J. J., Marcil A., Gauthier Y., and Drouin J.. 1999. Ptx1 regulates SF-1 activity by an interaction that mimics the role of the ligand-binding domain. EMBO J. 18:3431–3441.
   PubMed Web of Science ®Google Scholar
• Tsutsumi, M., Zhou W., Millar R. P., Mellon P. L., Roberts J. L., Flanagan C. A., Dong K., Gillo B., and Sealfon S. C.. 1992. Cloning and functional expression of a mouse gonadotropin-releasing hormone receptor. Mol. Endocrinol. 6:1163–1169.
   PubMed Web of Science ®Google Scholar
• Ubeda, M., Vallejo M., and Habener J. F.. 1999. CHOP enhancement of gene transcription by interactions with Jun/Fos AP-1 complex proteins. Mol. Cell. Biol. 19:7589–7599.
   PubMedGoogle Scholar
• Ulloa-Aguirre, A., Stanislaus D., Arora V., Väänänen J., Brothers S., Janovick J. A., and Conn P. M.. 1998. The third intracellular loop of the rat gonadotropin-releasing hormone receptor couples the receptor to Gs- and Gq/11-mediated signal transduction pathways: evidence from loop fragment transfection in GGH3 cells. Endocrinology 139:2472–2478.
   PubMedGoogle Scholar
• White, B. R., Duval D. L., Mulvaney J. M., Roberson M. S., and Clay C. M.. 1999. Homologous regulation of the gonadotropin-releasing hormone receptor gene is partially mediated by protein kinase C activation of an activator protein-1 element. Mol. Endocrinol. 13:566–577.
   PubMedGoogle Scholar
• Yen, P. M., Wilcox E. C., and Chin W. W.. 1995. Steroid hormone receptors selectively affect transcriptional activation but not basal repression by thyroid hormone receptors. Endocrinology 136:440–445.
   PubMedGoogle Scholar
• Zakaria, M. M., Jeong K.-H., Lacza C., and Kaiser U. B.. 2002. Pituitary homeobox 1 activates the rat FSHβ (rFSHβ) gene through both direct and indirect interactions with the rFSHβ gene promoter. Mol. Endocrinol. 16:1840–1852.
   PubMedGoogle Scholar
• Zhou, X.-F., Shen X.-Q., and Shemshedini L.. 1999. Ligand-activated retinoic acid receptor inhibits AP-1 transactivation by disrupting c-Jun/c-Fos dimerization. Mol. Endocrinol. 13:276–285.
   PubMed Web of Science ®Google Scholar