The Nonconserved Hinge Region and Distinct Amino-Terminal Domains of the RORα Orphan Nuclear Receptor Isoforms are Required for Proper DNA Bending and RORα-DNA Interactions

REFERENCES

• Baur, C.-P., and R. Knippers. 1988. Protein-induced bending of the simian virus 40 origin of replication. J. Mol. Biol. 203:1009–1019.
   PubMedGoogle Scholar
• Bracco, L., D. Kotlarz, A. Kolb, S. Diekmann, and H. Buc. 1989. Synthetic curved DNA sequences can act as transcriptional activators in Escherichia coli. EMBO J. 8:4289–4296.
   PubMed Web of Science ®Google Scholar
• Bradshaw, M. S., S. Y. Tsai, X. Leng, A. D. W. Dobson, O. M. Conneely, B. W. O'Malley, and M.-J. Tsai. 1991. Studies on the mechanism of functional cooperativity between progesterone and estrogen receptors. J. Biol. Chem. 266:16684–16690.
   PubMed Web of Science ®Google Scholar
• Bugge, T. H., J. Pohl, O. Lonnoy, and H. G. Stunnenberg. 1992. RXRα, a promiscuous partner of retinoic acid and thyroid hormone receptors. EMBO J. 11:1409–1418.
   PubMed Web of Science ®Google Scholar
• Drouin, J., Y. L. Sun, S. Tremblay, P. Lavender, T. J. Schmidt, A. de Léan, and M. Nemer. 1992. Homodimer formation is rate-limiting for high affinity DNA binding by glucocorticoid receptor. Mol. Endocrinol. 6:1299–1309.
   PubMed Web of Science ®Google Scholar
• Espinás, M. L., J. Roux, J. Ghysdael, R. Pictet, and T. Grange. 1994. Participation of Ets transcription factors in the glucocorticoid response of the rat tyrosine aminotransferase gene. Mol. Cell. Biol. 14:4116–4126.
   PubMedGoogle Scholar
• Evans, R. M. 1988. The steroid and thyroid hormone receptor superfamily. Science 240:889–895.
   PubMed Web of Science ®Google Scholar
• Freedman, L. P. 1992. Anatomy of the steroid receptor zinc finger region. Endocr. Rev. 13:129–145.
   PubMed Web of Science ®Google Scholar
• Giese, K., J. Cox, and R. Grosschedl. 1992. The HMG domain of lymphoid enhancer factor 1 bends DNA and facilitates assembly of functional nucleoprotein structures. Cell 69:185–195.
   PubMed Web of Science ®Google Scholar
• Giese, K., and R. Grosschedl. 1993. LEF-1 contains an activation domain that stimulates transcription only in a specific context of factor-binding sites. EMBO J. 12:4667–4676.
   PubMedGoogle Scholar
• Giguère, V., S. H. Hollenberg, M. G. Rosenfeld, and R. M. Evans. 1986. Functional domains of the human glucocorticoid receptor. Cell 46:645–652.
   PubMed Web of Science ®Google Scholar
• Giguère, V., L. McBroom, and G. Flock. 1994. Unpublished data.
   Google Scholar
• Giguère, V., S. E. Ong, P. Segui, and R. M. Evans. 1987. Identification of a receptor for the morphogen retinoic acid. Nature (London) 330:624–629.
   PubMed Web of Science ®Google Scholar
• Giguère, V., M. Tini, G. Flock, E. S. Ong, R. M. Evans, and G. Otulakowski. 1994. Isoform-specific amino-terminal domains dictate DNA-binding properties of RORα, a novel family of orphan nuclear receptors. Genes Dev. 8:538–553.
   PubMed Web of Science ®Google Scholar
• Gilson, E., M. Roberge, R. Giraldo, D. Rhodes, and S. M. Gasser. 1993. Distortion of the DNA double helix by RAP1 at silencers and multiple telomeric binding sites. J. Mol. Biol. 231:293–310.
   PubMed Web of Science ®Google Scholar
• Gober, J. W., and L. Shapiro. 1990. Integration host factor is required for the activation of developmentally regulated genes in Caulobacter. Genes Dev. 4:1494–1504.
   PubMed Web of Science ®Google Scholar
• Goodman, S. D., and H. A. Nash. 1989. Functional replacement of a protein-induced bend in a DNA recombination site. Nature (London) 341:251–254.
   PubMed Web of Science ®Google Scholar
• Harding, H. P., and M. A. Lazar. 1993. The orphan receptor Rev-ErbAα activates transcription via a novel response element. Mol. Cell. Biol. 13: 3113–3121.
   PubMed Web of Science ®Google Scholar
• Hoover, T. R., E. Santero, S. Porter, and S. Kustu. 1990. The integration host factor stimulates interaction of RNA polymerase with NIFA, the transcriptional activator for nitrogen fixation operons. Cell 63:11–22.
   PubMed Web of Science ®Google Scholar
• Kerppola, T. K., and T. Curran. 1991. DNA bending by Fos and Jun: the flexible hinge model. Science 254:1210–1214.
   PubMedGoogle Scholar
• Kerppola, T. K., and T. Curran. 1991. Fos-Jun heterodimers and Jun homodimers bend DNA in opposite orientations: implications for transcription factor cooperativity. Cell 66:317–326.
   PubMedGoogle Scholar
• King, I. N., T. se Soyza, D. F. Catanzaro, and T. N. Lavin. 1993. Thyroid hormone receptor-induced bending of specific sequences is modified by an accessory factor. J. Biol. Chem. 268:495–501.
   PubMedGoogle Scholar
• Kliewer, S. A., K. Umesono, D. J. Mangelsdorf, and R. M. Evans. 1992. Retinoid X receptor interacts with nuclear receptors in retinoic acid, thyroid hormone and vitamin D3 signalling. Nature (London) 335:446–449.
   Google Scholar
• Klock, G., U. Strähle, and G. Schütz. 1987. Oestrogen and glucocorticoid response elements are closely related but distinct. Nature (London) 329: 734–736.
   PubMed Web of Science ®Google Scholar
• Knegtel, R. M. A., M. Katahira, J. G. Schilthuis, A. M. J. J. Bonvin, R. Boelens, D. Eib, P. T. van der Saag, and R. Kaptein. 1993. The solution structure of the human retinoic acid receptor-β DNA-binding domain. J. Biol. NMR 3:1–17.
   PubMedGoogle Scholar
• Krust, A., S. Green, P. Argos, V. Kumar, P. Walter, J.-M. Bornert, and P. Chambon. 1986. The chicken oestrogen receptor sequence: homology with verbA and the human oestrogen and glucocorticoid receptors. EMBO J. 5:891–897.
   PubMed Web of Science ®Google Scholar
• Kumar, V., and P. Chambon. 1988. The estrogen receptor binds tightly to its responsive element as a ligand-induced homodimer. Cell 55:145–156.
   PubMed Web of Science ®Google Scholar
• Laudet, V., C. Hänni, J. Coli, F. Catzeflis, and D. Stéhelin. 1992. Evolution of the nuclear receptor gene superfamily. EMBO J. 11:1003–1013.
   PubMed Web of Science ®Google Scholar
• Lavorgna, G., H. Ueda, J. Clos, and C. Wu. 1991. FTZ-F1, a steroid hormone receptor-like protein implicated in the activation of fushi tarazu. Science 252:848–851.
   PubMed Web of Science ®Google Scholar
• Lazar, M. A., R. A. Hodin, D. S. Darling, and W. W. Chin. 1989. A novel member of the thyroid/steroid hormone receptor family is encoded by the opposite strand of the rat c-erbAα transcriptional unit. Mol. Cell. Biol. 9:1128–1136.
   PubMedGoogle Scholar
• Lee, M. S., S. A. Kliewer, J. Provençal, P. E. Wright, and R. M. Evans. 1993. Solution structure of the RXR α DNA-binding domain: a helix required for homodimeric DNA binding. Science 260:1117–1121.
   PubMed Web of Science ®Google Scholar
• Leid, M., P. Kastner, R. Lyons, H. Nakshari, M. Saunders, T. Zacharewski, J.-Y. Chen, A. Staub, J.-M. Garnier, S. Mader, and P. Chambon. 1992. Purification, cloning, and RXR identity of the HeLa cell factor with which RAR or TR heterodimerizes to bind target sequences efficiently. Cell 68: 377–395.
   PubMed Web of Science ®Google Scholar
• Leidig, F., A. R. Shepard, W. Zhang, A. Stelter, P. A. Cattini, J. D. Baxter, and N. L. Eberhardt. 1992. Thyroid hormone responsiveness in human growth hormone-related genes. J. Biol. Chem. 267:913–921.
   PubMed Web of Science ®Google Scholar
• Lu, X. P., N. L. Eberhardt, and M. Pfahl. 1993. DNA bending by retinoid X receptor-containing retinoid and thyroid hormone receptor complexes. Mol. Cell. Biol. 13:6509–6519.
   PubMedGoogle Scholar
• Luisi, B. F., W. X. Xu, Z. Otwinowski, L. P. Freedman, K. R. Yamamoto, and P. Sigler. 1991. Crystallographic analysis of the interaction of the glucocor-ticoid receptor with DNA. Nature (London) 352:497–505.
   PubMed Web of Science ®Google Scholar
• Mangelsdorf, D. J., E. S. Ong, J. A. Dyck, and R. M. Evans. 1990. Nuclear receptor that identifies a novel retinoic acid response pathway. Nature (London) 345:224–229.
   PubMed Web of Science ®Google Scholar
• Marks, M. S., P. L. Hallenbeck, T. Nagata, J. H. Segars, E. Appella, V. M. Nikodem, and K. Ozato. 1992. H-2RIIBP (RXRβ) heterodimerization provides a mechanism for combinatorial diversity in the regulation of retinoic acid and thyroid hormone responsive genes. EMBO J. 11:1419–1435.
   PubMed Web of Science ®Google Scholar
• Martinez, E., F. Givel, and W. Wahli. 1987. The estrogen-responsive element as an inducible enhancer: DNA sequence requirements and conversion to a glucocorticoid-responsive element. EMBO J. 6:3719–3727.
   PubMed Web of Science ®Google Scholar
• McBroom, L. D. B., and P. D. Sadowski. 1994. DNA bending by Saccharomyces cerevisiae ABF1 and its proteolytic fragments. J. Biol. Chem. 269: 16461–16468.
   PubMedGoogle Scholar
• Näär, A. M., J. M. Boutin, S. M. Lipkin, V. C. Yu, J. M. Holloway, C. K. Glass, and M. G. Rosenfeld. 1991. The orientation and spacing of core DNA-binding motifs dictate selective transcriptional responses to three nu clear receptors. Cell 65:1267–1279.
   PubMed Web of Science ®Google Scholar
• Nardulli, A. M., and D. J. Shapiro. 1992. Binding of the estrogen receptor DNA-binding domain to the estrogen response element induces DNA bending. Mol. Cell. Biol. 12:2037–2042.
   PubMedGoogle Scholar
• Natesan, S., and M. Z. Gilman. 1993. DNA bending and orientation-dependent function of YY1 in the c-fos promoter. Genes Dev. 7:2497–2509.
   PubMed Web of Science ®Google Scholar
• Oñate, S. A., P. Prendergast, J. P. Wagner, M. Nissen, R. Reeves, D. E. Pettijohn, and D. P. Edwards. 1994. The DNA-bending protein HMG-1 enhances progesterone receptor binding to its target DNA sequences. Mol. Cell. Biol. 14:3376–3391.
   PubMedGoogle Scholar
• Pérez-Martín, J., and M. Espinosa. 1993. Protein-induced bending as a transcriptional switch. Science 260:805–807.
   PubMed Web of Science ®Google Scholar
• Retnakaran, R., G. Flock, and V. Giguère. 1994. Identification of RVR, a novel orphan nuclear receptor that acts as a negative transcriptional regulator. Mol. Endocrinol. 8:1234–1244.
   PubMedGoogle Scholar
• Rhodes, S. J., R. Chen, G. E. DiMatta, K. M. Scully, K. A. Kalla, S.-C. Lin, V. C. Yu, and M. G. Rosenfeld. 1994. A tissue-specific enhancer confers Pit-1-dependent morphogen inducibility and autoregulation on the pit-1 gene. Genes Dev. 7:913–932.
   Google Scholar
• Rojo, F., A. Zaballos, and M. Salas. 1990. Bend induced by the phage F29 transcriptional activator in the viral late promoter is required for activation. J. Mol. Biol. 211:713–725.
   PubMedGoogle Scholar
• Russo, F. D., and T. J. Silhavy. 1992. Alpha: the cinderella subunit of RNA polymerase. J. Biol. Chem. 267:14515–14518.
   PubMedGoogle Scholar
• Sabbah, M., S. Le Ricousse, G. Redeuilh, and E.-E. Baulieu. 1992. Estrogen receptor-induced bending of Xenopus vitellogenin A2 gene hormone response element. Biochem. Biophys. Res. Commun. 185:944–952.
   PubMed Web of Science ®Google Scholar
• Salvo, J. J., and N. D. F. Grindley. 1988. The γδ resolvase bends the res site into a recombinogenic complex. EMBO J. 7:3609–3616.
   PubMedGoogle Scholar
• Schüle, R., M. Muller, H. Otsuka-Murakami, and R. Renkawitz. 1988. Co-operativity of the glucocorticoid receptor and the CACCC-box binding factor. Nature (London) 332:8790.
   Google Scholar
• Schwabe, J. W. R., L. Chapman, J. T. Finch, and D. Rhodes. 1993. The crystal structure of the estrogen receptor DNA-binding domain bound to DNA: how receptors discriminate between their response elements. Cell 75:567–578.
   PubMed Web of Science ®Google Scholar
• Schwartz, C. J. E., and P. D. Sadowski. 1989. FLP recombinase of the 2 mm circle plasmid of Saccharomyces cerevisiae bends its DNA target. Isolation of FLP mutants defective in DNA bending. J. Mol. Biol. 205:647–658.
   Google Scholar
• Siebenlist, U., and W. Gilbert. 1980. Contacts between Escherichia coli RNA polymerase and an early promoter of phage T7. Proc. Natl. Acad. Sci. USA 77:122–126.
   PubMed Web of Science ®Google Scholar
• Stenzel, T. T., T. MacAllister, and D. Bastia. 1991. Cooperativity at a distance promoted by the combined action of two replication initiator proteins and a DNA bending protein at the replication origin of pSC101. Genes Dev. 5:1453–1463.
   PubMedGoogle Scholar
• Thompson, J. F., and A. Landy. 1988. Empirical estimation of protein-induced DNA bending angles: applications to l site-specific recombination complexes. Nucleic Acids Res. 16:9687–9705.
   PubMed Web of Science ®Google Scholar
• Tini, M., G. Otulakowski, M. L. Breitman, L.-T. Tsui, and V. Giguère. 1993. An everted repeat mediates retinoic acid induction of the γF-crystallin gene: evidence of a direct role for retinoids in lens development. Genes Dev. 7:295–307.
   PubMed Web of Science ®Google Scholar
• Torchia, J., and V. Giguère. Unpublished observations.
   Google Scholar
• Truss, M., and M. Beato. 1993. Steroid hormone receptors: interaction with deoxyribonucleic acid and transcription factors. Endocr. Rev. 14:459–479.
   PubMed Web of Science ®Google Scholar
• Truss, M., G. Chalepakis, E. P. Slater, S. Mader, and M. Beato. 1991. Functional interaction of hybrid response elements with wild-type and mutant steroid hormone receptors. Mol. Cell. Biol. 11:3247–3258.
   PubMed Web of Science ®Google Scholar
• Tsukiyama, T., H. Ueda, S. Hirose, and O. Niwa. 1992. Embryonal long terminal repeat-binding protein is a murine homolog of FTZ-F1, a member of the steroid receptor superfamily. Mol. Cell. Biol. 12:1286–1291.
   PubMed Web of Science ®Google Scholar
• Ueda, H., G.-C. Sun, T. Murata, and S. Hirose. 1992. A novel DNA-binding motif abuts the zinc fingers domain of insect nuclear hormone receptor FTZ-F1 and mouse embryonal long terminal repeat-binding protein. Mol. Cell. Biol. 12:5667–5672.
   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
• Williams, J. S., T. T. Eckdahl, and J. N. Anderson. 1988. Bent DNA functions as a replication enhancer in Saccharomyces cerevisiae. Mol. Cell. Biol. 8:2763–2769.
   PubMedGoogle Scholar
• Wilson, T. E., T. J. Fahrner, M. Johnson, and J. Milbrandt. 1991. Identification of the DNA binding site for NGFI-B by genetic selection in yeast. Science 252:1296–1300.
   PubMed Web of Science ®Google Scholar
• Wilson, T. E., T. J. Fahrner, and J. Millbrandt. 1993. The orphan receptors NGFI-B and steroidogenic factor 1 establish monomer binding as a third paradigm of nuclear receptor-DNA interaction. Mol. Cell. Biol. 13:5794–5804.
   PubMedGoogle Scholar
• Wilson, T. E., R. E. Paulsen, K. A. Padgett, and J. Milbrandt. 1992. Participation of non-zinc finger residues in DNA binding by two nuclear orphan receptors. Science 256:107–110.
   PubMed Web of Science ®Google Scholar
• Wu, H.-M., and D. M. Crothers. 1984. The locus of sequence-directed and protein-induced DNA bending. Nature (London) 308:509–513.
   PubMed Web of Science ®Google Scholar
• Yu, V. C., C. Delsert, B. Andersen, J. M. Holloway, O. V. Devary, A. M. Näär, S. Y. Kim, J. M. Boutin, C. K. Glass, and M. G. Rosenfeld. 1991. RXRβ: a coregulator that enhances binding of retinoic acid, thyroid hormone, and vitamin D receptors to their cognate response elements. Cell 67:1251–1266.
   PubMed Web of Science ®Google Scholar
• Zhang, X.-K., B. Hoffmann, P. B.-V. Tran, G. Graupner, and M. Pfahl. 1992. Retinoid X receptor is an auxiliary protein for thyroid hormone and retinoic acid receptors. Nature (London) 335:441–446.
   Google Scholar
• Zinkel, S. S., and D. M. Crothers. 1987. DNA bend direction by phase sensitive detection. Nature (London) 328:178–181.
   PubMed Web of Science ®Google Scholar