LXXLL-Related Motifs in Dax-1 Have Target Specificity for the Orphan Nuclear Receptors Ad4BP/SF-1 and LRH-1

REFERENCES

• Altincicek, B., S. P. Tenbaum, U. Dressel, D. Thormeyer, R. Renkawitz, and A. Baniahmad. 2000. Interaction of the corepressor Alien with DAX-1 is abrogated by mutations of DAX-1 involved in adrenal hypoplasia congenita. J. Biol. Chem. 275: 7662–7667.
   PubMedGoogle Scholar
• Boerboom, D., N. Pilon, R. Behdjani, D. W. Silversides, and J. Sirois. 2000. Expression and regulation of transcripts encoding two members of the NR5A nuclear receptor subfamily of orphan nuclear receptors, steroidogenic factor-1 and NR5A2, in equine ovarian cells during the ovulatory process. Endocrinology 141: 4647–4656.
   PubMedGoogle Scholar
• Bourguet, W., M. Ruff, P. Chambon, H. Gronemeyer, and D. Moras. 1995. Crystal structure of the ligand-binding domain of the human nuclear receptor RXRα. Nature 375: 377–382.
   PubMed Web of Science ®Google Scholar
• Brzozowski, A. M., A. C. Pike, Z. Dauter, R. E. Hubbard, T. Bonn, O. Engstrom, L. Ohman, G. L. Greene, J. A. Gustafsson, and M. Carlquist. 1997. Molecular basis of agonism and antagonism in the oestrogen receptor. Nature 389: 753–758.
   PubMed Web of Science ®Google Scholar
• Chang, C., J. D. Norris, H. Gron, L. A. Paige, P. T. Hamilton, D. J. Kenan, D. Fowlkes, and D. P. McDonnell. 1999. Dissection of the LXXLL nuclear receptor-coactivator interaction motif using combinatorial peptide libraries: discovery of peptide antagonists of estrogen receptors α and β. Mol. Cell. Biol. 19: 8226–8239.
   PubMed Web of Science ®Google Scholar
• Crawford, P. A., C. Dorn, Y. Sadovsky, and J. Milbrandt. 1998. Nuclear receptor DAX-1 recruits nuclear receptor corepressor N-CoR to steroidogenic factor 1. Mol. Cell. Biol. 18: 2949–2956.
   PubMed Web of Science ®Google Scholar
• Crawford, P. A., J. A. Polish, G. Ganpule, and Y. Sadovsky. 1997. The activation function-2 hexamer of steroidogenic factor-1 is required, but not sufficient for potentiation by SRC-1. Mol. Endocrinol. 11: 1626–1635.
   PubMedGoogle Scholar
• Darimont, B. D., R. L. Wagner, J. W. Apriletti, M. R. Stallcup, P. J. Kushner, J. D. Baxter, R. J. Fletterick, and K. R. Yamamoto. 1998. Structure and specificity of nuclear receptor-coactivator interactions. Genes Dev. 12: 3343–3356.
   PubMed Web of Science ®Google Scholar
• Egea, P. F., A. Mitschler, N. Rochel, M. Ruff, P. Chambon, and D. Moras. 2000. Crystal structure of the human RXRα ligand-binding domain bound to its natural ligand: 9-cis retinoic acid. EMBO J. 19: 2592–2601.
   PubMed Web of Science ®Google Scholar
• Feng, W., R. C. Ribeiro, R. L. Wagner, H. Nguyen, J. W. Apriletti, R. J. Fletterick, J. D. Baxter, P. J. Kushner, and B. L. West. 1998. Hormone-dependent coactivator binding to a hydrophobic cleft on nuclear receptors. Science 280: 1747–1749.
   PubMed Web of Science ®Google Scholar
• Fijan, N., D. Sulimanovic, M. Bearzotti, D. Muzinc, L. O. Zwillenberg, S. Chilmonczyk, J. F. Vautherot, and P. de Kinkelin. 1983. Some properties of the Epithelioma papulosum cyprini (EPC) cell line from carp Cyprinus carpio. Ann. Virol. (Inst. Pasteur) 134E: 207–220.
   Google Scholar
• Forman, B. M., K. Umesono, J. Chen, and R. M. Evans. 1995. Unique response pathways are established by allosteric interactions among nuclear hormone receptors. Cell 81: 541–550.
   PubMed Web of Science ®Google Scholar
• Galarneau, L., J. F. Pare, D. Allard, D. Hamel, L. Levesque, J. D. Tugwood, S. Green, and L. Belanger. 1996. The α1-fetoprotein locus is activated by a nuclear receptor of the Drosophila FTZ-F1 family. Mol. Cell. Biol. 16: 3853–3865.
   PubMed Web of Science ®Google Scholar
• Giguere, V. 1999. Orphan nuclear receptors: from gene to function. Endocr. Rev. 20: 689–725.
   PubMed Web of Science ®Google Scholar
• Goodwin, B., S. A. Jones, R. R. Price, M. A. Watson, D. D. McKee, L. B. Moore, C. Galardi, J. G. Wilson, M. C. Lewis, M. E. Roth, P. R. Maloney, T. M. Willson, and S. A. Kliewer. 2000. A regulatory cascade of the nuclear receptors FXR, SHP-1, and LRH-1 represses bile acid biosynthesis. Mol. Cell 6: 517–526.
   PubMed Web of Science ®Google Scholar
• Harish, S., T. Khanam, S. Mani, and P. Rangarajan. 2001. Transcriptional activation by hepatocyte nuclear factor-4 in a cell- free system derived from rat liver nuclei. Nucleic Acids Res. 29: 1047–1053.
   PubMedGoogle Scholar
• Heery, D. M., S. Hoare, S. Hussain, M. G. Parker, and H. Sheppard. 2001. Core LXXLL motif sequences in CREB-binding protein, SRC1, and RIP140 define affinity and selectivity for steroid and retinoid receptors. J. Biol. Chem. 276: 6695–6702.
   PubMed Web of Science ®Google Scholar
• Heery, D. M., E. Kalkhoven, S. Hoare, and M. G. Parker. 1997. A signature motif in transcriptional co-activators mediates binding to nuclear receptors. Nature 387: 733–736.
   PubMed Web of Science ®Google Scholar
• Hu, X., and M. A. Lazar. 1999. The CoRNR motif controls the recruitment of corepressors by nuclear hormone receptors. Nature 402: 93–96.
   PubMed Web of Science ®Google Scholar
• Ikeda, Y., A. Swain, T. J. Weber, K. E. Hentges, E. Zanaria, E. Lalli, K. T. Tamai, P. Sassone-Corsi, R. Lovell-Badge, G. Camerino, and K. L. Parker. 1996. Steroidogenic factor 1 and Dax-1 colocalize in multiple cell lineages: potential links in endocrine development. Mol. Endocrinol. 10: 1261–1272.
   PubMedGoogle Scholar
• Ikeda, Y., Y. Takeda, T. Shikayama, T. Mukai, S. Hisano, and K. I. Morohashi. 2001. Comparative localization of Dax-1 and Ad4BP/SF-1 during development of the hypothalamic-pituitary-gonadal axis suggests their closely related and distinct functions. Dev. Dyn. 220: 363–376.
   PubMedGoogle Scholar
• Ito, M., R. Yu, and J. L. Jameson. 1997. DAX-1 inhibits SF-1 mediated transactivation via a carboxy-terminal domain that is deleted in adrenal hypoplasia congenita. Mol. Cell. Biol. 17: 1476–1483.
   PubMed Web of Science ®Google Scholar
• Ito, M., R. N. Yu, and J. L. Jameson. 1998. Steroidogenic factor-1 contains a carboxy-terminal transcriptional activation domain that interacts with steroid receptor coactivator-1. Mol. Endocrinol. 12: 290–301.
   PubMedGoogle Scholar
• James, P., J. Halladay, and E. A. Craig. 1996. Genomic libraries and a host strain designed for highly efficient two-hybrid selection in yeast. Genetics 144: 1425–1436.
   PubMed Web of Science ®Google Scholar
• Johansson, L., A. Bavner, J. S. Thomsen, M. Farnegardh, J. A. Gustafsson, and E. Treuter. 2000. The orphan nuclear receptor SHP utilizes conserved LXXLL-related motifs for interactions with ligand-activated estrogen receptors. Mol. Cell. Biol. 20: 1124–1133.
   PubMed Web of Science ®Google Scholar
• Johansson, L., J. S. Thomsen, A. E. Damdimopoulos, G. Spyrou, J. A. Gustafsson, and E. Treuter. 1999. The orphan nuclear receptor SHP inhibits agonist-dependent transcriptional activity of estrogen receptors ERα and ERβ. J. Biol. Chem. 274: 345–353.
   PubMedGoogle Scholar
• Kane, C. D., and A. R. Means. 2000. Activation of orphan receptor-mediated transcription by Ca2+/calmodulin-dependent protein kinase IV. EMBO J. 19: 691–701.
   PubMedGoogle Scholar
• Kawabe, K., T. Shikayama, H. Tsuboi, S. Oka, K. Oba, T. Yanase, H. Nawata, and K. Morohashi. 1999. Dax-1 as one of the target genes of Ad4BP/SF-1. Mol. Endocrinol. 13: 1267–1284.
   PubMedGoogle Scholar
• Ko, L., G. R. Cardona, T. Iwasaki, K. S. Bramlett, T. P. Burris, and W. W. Chin. 2002. Ser-884 adjacent to the LXXLL motif of coactivator TRBP defines selectivity for ERs and TRs. Mol. Endocrinol. 16: 128–140.
   PubMedGoogle Scholar
• Lala, D. S., P. M. Syka, S. B. Lazarchik, D. J. Mangelsdorf, K. L. Parker, and R. A. Heyman. 1997. Activation of the orphan nuclear receptor steroidogenic factor 1 by oxysterols. Proc. Natl. Acad. Sci. USA 94: 4895–4900.
   PubMed Web of Science ®Google Scholar
• Le Douarin, B., A. L. Nielsen, J. M. Garnier, H. Ichinose, F. Jeanmougin, R. Losson, and P. Chambon. 1996. A possible involvement of TIF1α and TIF1β in the epigenetic control of transcription by nuclear receptors. EMBO J. 15: 6701–6715.
   PubMed Web of Science ®Google Scholar
• Lee, Y. K., H. Dell, D. H. Dowhan, M. Hadzopoulou-Cladaras, and D. D. Moore. 2000. The orphan nuclear receptor SHP inhibits hepatocyte nuclear factor 4 and retinoid X receptor transactivation: two mechanisms for repression. Mol. Cell. Biol. 20: 187–195.
   PubMed Web of Science ®Google Scholar
• Li, L. A., E. F. Chiang, J. C. Chen, N. C. Hsu, Y. J. Chen, and B. C. Chung. 1999. Function of steroidogenic factor 1 domains in nuclear localization, transactivation, and interaction with transcription factor TFIIB and c-Jun. Mol. Endocrinol. 13: 1588–1598.
   PubMedGoogle Scholar
• Lopez, D., W. Shea-Eaton, M. D. Sanchez, and M. P. McLean. 2001. DAX-1 represses the high-density lipoprotein receptor through interaction with positive regulators sterol regulatory element-binding protein-1a and steroidogenic factor-1. Endocrinology 142: 5097–5106.
   PubMedGoogle Scholar
• Luo, X., Y. Ikeda, and K. L. Parker. 1994. A cell-specific nuclear receptor is essential for adrenal and gonadal development and sexual differentiation. Cell 77: 481–490.
   PubMed Web of Science ®Google Scholar
• Mak, H. Y., S. Hoare, P. M. Henttu, and M. G. Parker. 1999. Molecular determinants of the estrogen receptor-coactivator interface. Mol. Cell. Biol. 19: 3895–3903.
   PubMedGoogle Scholar
• Mangelsdorf, D. J., and R. M. Evans. 1995. The RXR heterodimers and orphan receptors. Cell 83: 841–850.
   PubMed Web of Science ®Google Scholar
• Mangelsdorf, D. J., C. Thummel, M. Beato, P. Herrlich, G. Schutz, K. Umesono, B. Blumberg, P. Kastner, M. Mark, P. Chambon, and R. M. Evans. 1995. The nuclear receptor superfamily: the second decade. Cell 83: 835–839.
   PubMed Web of Science ®Google Scholar
• McInerney, E. M., D. W. Rose, S. E. Flynn, S. Westin, T. M. Mullen, A. Krones, J. Inostroza, J. Torchia, R. T. Nolte, N. Assa-Munt, M. V. Milburn, C. K. Glass, and M. G. Rosenfeld. 1998. Determinants of coactivator LXXLL motif specificity in nuclear receptor transcriptional activation. Genes Dev. 12: 3357–3368.
   PubMed Web of Science ®Google Scholar
• Mellon, P. L., C. H. Clegg, L. A. Correll, and G. S. McKnight. 1989. Regulation of transcription by cyclic AMP-dependent protein kinase. Proc. Natl. Acad. Sci. USA 86: 4887–4891.
   PubMed Web of Science ®Google Scholar
• Mellon, S. H., and S. R. Bair. 1998. 25-Hydroxycholesterol is not a ligand for the orphan nuclear receptor steroidogenic factor-1 (SF-1). Endocrinology 139: 3026–3029.
   PubMed Web of Science ®Google Scholar
• Monte, D., F. DeWitte, and D. W. Hum. 1998. Regulation of the human P450scc gene by steroidogenic factor 1 is mediated by CBP/p300. J. Biol. Chem. 273: 4585–4591.
   PubMed Web of Science ®Google Scholar
• Morohashi, K. I., and T. Omura. 1996. Ad4BP/SF-1, a transcription factor essential for the transcription of steroidogenic cytochrome P450 genes and for the establishment of the reproductive function. FASEB J. 10: 1569–1577.
   PubMedGoogle Scholar
• Nachtigal, M. W., Y. Hirokawa, D. L. Enyeart-VanHouten, J. N. Flanagan, G. D. Hammer, and H. A. Ingraham. 1998. Wilms' tumor 1 and Dax-1 modulate the orphan nuclear receptor SF-1 in sex-specific gene expression. Cell 93: 445–454.
   PubMed Web of Science ®Google Scholar
• Nagy, L., H. Y. Kao, J. D. Love, C. Li, E. Banayo, J. T. Gooch, V. Krishna, K. Chatterjee, R. M. Evans, and J. W. Schwabe. 1999. Mechanism of corepressor binding and release from nuclear hormone receptors. Genes Dev. 13: 3209–3216.
   PubMed Web of Science ®Google Scholar
• Nolte, R. T., G. B. Wisely, S. Westin, J. E. Cobb, M. H. Lambert, R. Kurokawa, M. G. Rosenfeld, T. M. Willson, C. K. Glass, and M. V. Milburn. 1998. Ligand binding and co-activator assembly of the peroxisome proliferator- activated receptor-γ. Nature 395: 137–143.
   PubMed Web of Science ®Google Scholar
• Nuclear Receptors Nomenclature Committee. 1999. A unified nomenclature system for the nuclear receptor superfamily. Cell 97: 161–163.
   PubMed Web of Science ®Google Scholar
• Ogawa, H., and K. Umesono. 1998. Intracellular localization and transcriptional activation by the human glucocorticoid receptor-green fluorescent protein (GFP) fusion proteins. Acta Histochem. Cytochem. 31: 303–308.
   Google Scholar
• Ohno, C. K., H. Ueda, and M. Petkovich. 1994. The Drosophila nuclear receptors FTZ-F1α and FTZ-F1β compete as monomers for binding to a site in the fushi tarazu gene. Mol. Cell. Biol. 14: 3166–3175.
   PubMedGoogle Scholar
• Parker, K. L., and B. P. Schimmer. 1997. Steroidogenic factor 1: a key determinant of endocrine development and function. Endocr. Rev. 18: 361–377.
   PubMed Web of Science ®Google Scholar
• Perissi, V., L. M. Staszewski, E. M. McInerney, R. Kurokawa, A. Krones, D. W. Rose, M. H. Lambert, M. V. Milburn, C. K. Glass, and M. G. Rosenfeld. 1999. Molecular determinants of nuclear receptor-corepressor interaction. Genes Dev. 13: 3198–3208.
   PubMed Web of Science ®Google Scholar
• Perlmann, T., and L. Jansson. 1995. A novel pathway for vitamin A signaling mediated by RXR heterodimerization with NGFI-B and NURR1. Genes Dev. 9: 769–782.
   PubMed Web of Science ®Google Scholar
• Perlmann, T., P. N. Rangarajan, K. Umesono, and R. M. Evans. 1993. Determinants for selective RAR and TR recognition of direct repeat HREs. Genes Dev. 7: 1411–1422.
   PubMed Web of Science ®Google Scholar
• Sadovsky, Y., P. A. Crawford, K. G. Woodson, J. A. Polish, M. A. Clements, L. M. Tourtellotte, K. Simburger, and J. Milbrandt. 1995. Mice deficient in the orphan receptor steroidogenic factor 1 lack adrenal glands and gonads but express P450 side-chain-cleavage enzyme in the placenta and have normal embryonic serum levels of corticosteroids. Proc. Natl. Acad. Sci. USA 92: 10939–10943.
   PubMed Web of Science ®Google Scholar
• Schwartz, C. J., H. M. Sampson, D. Hlousek, A. Percival-Smith, J. W. Copeland, A. J. Simmonds, and H. M. Krause. 2001. FTZ-Factor1 and Fushi tarazu interact via conserved nuclear receptor and coactivator motifs. EMBO J. 20: 510–519.
   PubMedGoogle Scholar
• Seol, W., H. S. Choi, and D. D. Moore. 1996. An orphan nuclear hormone receptor that lacks a DNA binding domain and heterodimerizes with other receptors. Science 272: 1336–1339.
   PubMed Web of Science ®Google Scholar
• Shiau, A. K., D. Barstad, P. M. Loria, L. Cheng, P. J. Kushner, D. A. Agard, and G. L. Greene. 1998. The structural basis of estrogen receptor/coactivator recognition and the antagonism of this interaction by tamoxifen. Cell 95: 927–937.
   PubMed Web of Science ®Google Scholar
• Shinoda, K., H. Lei, H. Yoshii, M. Nomura, M. Nagano, H. Shiba, H. Sasaki, Y. Osawa, Y. Ninomiya, O. Niwa, K. Morohashi, and E. Li. 1995. Developmental defects of the ventromedial hypothalamic nucleus and pituitary gonadotroph in the Ftz-F1 disrupted mice. Dev. Dyn. 204: 22–29.
   PubMed Web of Science ®Google Scholar
• Suzuki, T., H. Kawasaki, R. T. Yu, H. Ueda, and K. Umesono. 2001. Segmentation gene product Fushi tarazu is an LXXLL motif-dependent coactivator for orphan receptor FTZ-F1. Proc. Natl. Acad. Sci. USA 98: 12403–12408.
   PubMedGoogle Scholar
• Torchia, J., D. W. Rose, J. Inostroza, Y. Kamei, S. Westin, C. K. Glass, and M. G. Rosenfeld. 1997. The transcriptional co-activator p/CIP binds CBP and mediates nuclear-receptor function. Nature 387: 677–684.
   PubMed Web of Science ®Google Scholar
• Tremblay, J. J., and R. S. Viger. 1999. Transcription factor GATA-4 enhances Mullerian inhibiting substance gene transcription through a direct interaction with the nuclear receptor SF-1. Mol. Endocrinol. 13: 1388–1401.
   PubMedGoogle Scholar
• Umesono, K., K. K. Murakami, C. C. Thompson, and R. M. Evans. 1991. Direct repeats as selective response elements for the thyroid hormone, retinoic acid, and vitamin D3 receptors. Cell 65: 1255–1266.
   PubMed Web of Science ®Google Scholar
• Voegel, J. J., M. J. Heine, C. Zechel, P. Chambon, and H. Gronemeyer. 1996. TIF2, a 160 kDa transcriptional mediator for the ligand-dependent activation function AF-2 of nuclear receptors. EMBO J. 15: 3667–3675.
   PubMed Web of Science ®Google Scholar
• Wang, Z. N., M. Bassett, and W. E. Rainey. 2001. Liver receptor homologue-1 is expressed in the adrenal and can regulate transcription of 11β-hydroxylase. J. Mol. Endocrinol. 27: 255–258.
   PubMed Web of Science ®Google Scholar
• Warnmark, A., T. Almlof, J. Leers, J. A. Gustafsson, and E. Treuter. 2001. Differential recruitment of the mammalian mediator subunit TRAP220 by estrogen receptors ERα and ERβ. J. Biol. Chem. 276: 23397–23404.
   PubMed Web of Science ®Google Scholar
• Xie, W., H. Hong, N. N. Yang, R. J. Lin, C. M. Simon, M. R. Stallcup, and R. M. Evans. 1999. Constitutive activation of transcription and binding of coactivator by estrogen-related receptors 1 and 2. Mol. Endocrinol. 13: 2151–2162.
   PubMedGoogle Scholar
• Xu, L., C. K. Glass, and M. G. Rosenfeld. 1999. Coactivator and corepressor complexes in nuclear receptor function. Curr. Opin. Genet. Dev. 9: 140–147.
   PubMed Web of Science ®Google Scholar
• Yussa, M., U. Lohr, K. Su, and L. Pick. 2001. The nuclear receptor Ftz-F1 and homeodomain protein Ftz interact through evolutionarily conserved protein domains. Mech. Dev. 107: 39–53.
   PubMedGoogle Scholar
• Zanaria, E., F. Muscatelli, B. Bardoni, T. M. Strom, S. Guioli, W. Guo, E. Lalli, C. Moser, A. P. Walker, E. R. McCabe, T. Meitinger, A. P. Monaco, P. Sassone-Corsi, and G. Camerino. 1994. An unusual member of the nuclear hormone receptor superfamily responsible for X-linked adrenal hypoplasia congenita. Nature 372: 635–641.
   PubMed Web of Science ®Google Scholar
• Zhang, H., J. S. Thomsen, L. Johansson, J. A. Gustafsson, and E. Treuter. 2000. DAX-1 functions as an LXXLL-containing corepressor for activated estrogen receptors. J. Biol. Chem. 275: 39855–39859.
   PubMed Web of Science ®Google Scholar