A decade of molecular biology of retinoic acid receptors

FASEB Journal

Volumn 10, Issue 9, 1996, Pages 940-954

  Chambon, Pierre ^a  

^a l'alimentation et l'Environnement   (France)

Author keywords

AP1; coactivator; corepressor; cross modulation; ligand binding domain structure; ligand dependent transconformation; ligand dependent transcriptional activation; RA response elements; RAR , , and ; RXR RAR heterodimers; RXR , , and ; transactivation

Indexed keywords

CELL SURFACE RECEPTOR; RECEPTOR SUBTYPE; RETINOIC ACID DERIVATIVE; RETINOIC ACID RECEPTOR; RETINOID; RETINOL;

CELL DIFFERENTIATION; CHROMOSOME MAP; EMBRYO DEVELOPMENT; GENE EXPRESSION REGULATION; GENETIC VARIABILITY; HOMEOSTASIS; PRIORITY JOURNAL; PROTEIN FAMILY; RETINOL DEFICIENCY; REVIEW; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION;

EID: 0029794132     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fasebj.10.9.8801176     Document Type: Review

References (120)

1. Blomhoff, R. (1994) Vitamin A in Health and Disease (Blomhoff, R, ed) Marcel Dekker, New York
2. Sporn, M. B., Roberts, A. B., and Goodmun, D. S. (1994) The Retinoids: Biology, Chemistry, and Medicine, Raven Press, New York
3. De Luca, L. M. (1991) Retinoids and their receptors in differentiation, embryogenesis, and neoplasia. FASEB. J. 5, 2924-2933
4. Lohnes, D., Mark, M., Mendelsohn, G., Dollé, P., Dierich, A., Gorry, P., Gansmuller, A., and Chambon, P. (1994) Function of the retinoic acid receptors (RARs) during development.(I) Cranofacial and skeletal abnormalities in RAR double mutants. Development 120, 2723-2748
5. Mendelsolin, C., Lohnes, D., Décimo, U., Lufkin, T., LeMeur, M., Chambon, P., and Mark, M. (1994) Function of the retinoic acid receptors (RARs) during development (II). Multiple abnormalities at various stage of organogenesis in RAR double mutants. Development 120, 2749-2771
6. Kastner, P., Leid, M., and Chambon, P. (1994) The role of nuclear retinoic acid receptors in the regulation of gene expression. In Vitamin A in Health and Disease (Blomhoff, R., ed) pp. 189-238, Marcel Dekker, New York
7. Petkovich, M., Brand, N. J., Krust, A., and Chambon, P. (1987) A human retinoic acid receptor which belongs to the family of nuclear receptors. Nature (London) 330, 444-450
8. Giguère, V., Ong, E. S., Segui, P., and Evans, R. M. (1987) Identification of a receptor for the morphogen retinoic acid. Nature (London) 330, 624-629
9. Green, S., and Chambon, P. (1986) A superfamily of potentially oncogenic hormone receptors. Nature (London) 324, 615-617
10. Green, S., and Chambon, P. (1988) Nuclear receptors enhance our understanding of transcription regulation. Trends. Genet. 4, 309-314
11. Evans, R. M. (1980) The steroid and thyroid hormone receptor superfamily. Science 240, 889-895
12. Keaveny, M., and Stunnenberg, H.C. (1995) Retinoic acid receptors. In Inducible Gene Expression, Vol. 2 (Buuerle, P. A., eds) pp. 187-242, Birkhäeuscr, Boston
13. Leid, M., Kastner, P., and Chambon, P. (1992) Multiplicity generates diversity in the retinoic acid signalling pathways. Trends. Biochem. Sci. 17, 427-433
14. Napoli, J. L. (1996) Regulation of the biosynthesis and catabolism of retinoids. FASEB J. 10, 993-1001
15. Giguère, V. (1994) Retinoic acid receptors and cellular retinoid binding proteins: complex interplay in retinoid signaling. Endocr. Rev. 15, 61-79
16. Lumpron, C., Rochette-Egly, C., Gorry, P., Dollé, P., Mark, M., Lufkin, T., LeMeur, M., and Chambon, P. (1995) Mice deficient in cellular retinoic acid binding protein II (CRABPII) or in both CRABPI and CRABPII are essentially normal. Development 121, 539-548
17. Kastner, P., Mark, M., and Chambon, P. (1995) Nonsteroid nuclear receptors: what are genetic studies telling us about their role in real life? Cell 83, 859-869
18. Petkovich, M. (1992) Regulation of gene expression by vitamin A: the role of nuclear retinoic acid receptors. Annu. Rev. Nutr. 12, 443-471
19. Parker, M. C. (1993) Steroid und related receptors. Curr. Opin. Cell Biol. 5, 499-504
20. Chambon, P. (1994) The retinoid signaling pathway: molecular and genetic analyses. Semin. Cell Biol. 5, 115-125
21. Mangelsdorf, D. J., Umesono, K., and Evans, R. M. (1994) The retinoid receptors. In The Retinoids: Biology, Chemistry and Medicine (Sporn, M. B., Roberts, A. B., Goodman, D. S., eds) pp. 319-349, Raven Press, New York
22. Glass, C.K. (1994) Differential recognition of target genes by nuclear receptor monomers, dimers, and heterodimers. Endocr. Rev. 15, 391-407
23. Tsai, M. J., and O'Malley, B. W. (1994) Molecular mechanisms of action of steroid/thyroid receptor superfamily members. Annu. Rev. Biochem. 63, 451-486
24. Mangelsdorf, D. J., and Evans, R. M. (1995) The RXR heterodimers and orphan receptors. Cell 83, 841-850
25. Mangelsdorf, D. J., Thummel, C., Beato, M., Herrlich, P., Schütz, G., Umesono, K., Blumberg, B., Kastner, P., Mark, M., Chambon, P., and Evans, R. M. (1995) The nuclear receptor superfamily: the second decade. Cell 83, 835-839
26. Gronemeyer, H., and Laudet, V. (1996) Transcription factors 3: Nuclear receptors. Protein Profile, Vol. 2, Academic Press, New York
27. Dalman, F. C., Sturzenberker, L. J., Levin, A. A., Lucas, D. A., Perdew, G. H., Petkovich, M., Chambon, P., Grippo, J. F., and Pratt, W. B. (1991) Hetinoic acid receptor belongs to a subclass of nuclear receptors that do not form "docking" complexes with hsp90. Biochemistry 30, 5605-5608
28. Thummel, G. S. (1995) From embryogenesis to metamorphosis: the regulation ami function of Drosophila nuclear receptor superfamily members. Cell 83, 871-877
29. Nagpal, S., Saunders, M., Kastner, P., Durand, B., Nakshatri, H., and Chambon, P. (1992) Promoter context- and response element-dependent specificity of the transcriptional activation and modulating functions of retinoic acid receptors. Cell 70, 1007-1019
30. Nagpal, S., Friant, S., Nukshatri, H., and Chambon, P. (1993) RARs and RXRs: evidence for two autonomous transactivation functions (AF-1 and AF-2) and heterodimerization in vivo. EMBO J. 12, 2349-2360
31. Nagata, T., Kanno, Y., Ozato, K., and Taketo, M. (1994) The mouse Rxrb gene encoding RXR beta: genomic organization and two mRNA isoforms generated by alternative splicing of transcripts initiated from CpC island promoters. Gene 142, 183-189
32. Liu, Q., and Linnèy, E. (1993) The mouse retinoid-X receptor-gamma gene: genomic organization and evidence for functional isoforms. Mol. Endocrinol. 7, 651-658
33. Morriss-Kay, G. M., and Sokolova, N. (1996) Embryonic development and pattern formation. FASEB J. 10, 961-968
34. Kato, S., Sasaki, H., Susawa, M., Tora, L., Chambon, P., and Gronemeyer, H. (1995) Widely spaced, directly repeated PuGGTCA elements act as promiscuous enhancers for different classes of nuclear receptors. Mol. Cell Biol. 15, 5858-5867
35. Nakshatri, H., and Chambon, P. (1994) The directly repeated RG(G/T)TCA motifs of the rat and mouse cellular retinol-binding protein II genes are promiscuous binding sites for RAR, RXR, HNF-4 and ARP-1 homo- and heterodimers. J. Biol. Chem. 269, 890-902
36. Yu, V. C., Delsert, C., Andersen, B., Holloway, J. M., Devary, O. V., Naar, A. M., Kim, S. Y., Boutin, J. M., Class, C. K., and Rosenfeld, M. C. (1991) RXR beta: a coregulator that enhances binding of retinoic acid, thyroid hormone, and vitamin D receptors to their cognate response elements. Cell 67, 1251-1266
37. Leid, M., Kastner, P., Lyons, R., Nakshatri, H., Saunders, M., Zacharewski, T., Chen, J. Y., Staub, A., Gamier, J. M., Mader, S., et al. (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
38. 3 signalling. Nature (London) 355, 446-449
39. Zhang, X. K., Hoffmann, B., Tran, P. B., Graupner, G., and Pfahl, M. (1992) Retinoid X receptor is an auxiliary protein for thyroid hormone and retinoic acid receptors. Nature (London) 355, 441-446
40. Marks, M. S., Hallenbeck, P. L., Nagata, T., Segars, J. H., Appella, E., Nikodem, V. M., and Ozato, K. (1992) H-2RIIBP (RXR beta), heterodimerization provides a mechanism for combinatorial diversity in the regulation of retinoic acid and thyroid hormone responsive genes. EMBO J. 11, 1419-1435
41. Bugge, T. H., Pohl, J., Lonnoy, O., and Stunnenberg, H. G. (1992) RXR alpha, a promiscuous partner of retinoic acid and thyroid hormone receptors. EMBO J. 11, 1409-1418
42. Durand, B., Saunders, M., Leroy, P., Leid, M., and Chambon, P. (1992) All-trans and 9-cis retinoic acid induction of CRABPII transcription is mediated by RAR-RXR heterodimers hound to DR1 and DR2 repeated motifs. Cell 71, 73-85
43. Kliewer, S. A., Umesono, K., Nonnan, D. J., Heyman, R.A., and Evans, R. M. (1992) Convergence of 9-cis retinoic acid and peroxisome proliferator signalling pathways through heterodimer formation of their receptors. Nature (London) 358, 771-774
44. Bardot, O., Aldridge, T. C., Latruffe, N., and Green, S. (1993) PPAR-RXR heterodimer activates a peroxisome proliferator response element upstream of the bifunctional enzyme gene. Biochem. Biophys. Res. Commun. 192, 37-45
45. Mader, S., Chen, J. Y., Chen, Z., White, J., Chambon, P., and Gronemeyer, H. (1993) The patterns of binding of RAR, RXR and TR homo- and heterodimers to direct repeats are dictated by the binding specificites of the DNA binding domains. EMBO J. 12, 5029-5041
46. Mader, S., Leroy, P., Chen, J. Y., and Chambon, P. (1993) Multiple parameters control the selectivity of nuclear receptors for their response elements. J. Biol. Chem. 268, 591-600
47. Kurokawa, R., Yu, V. C., Naar, A., Kyakumoto, S., Han, Z., Silverman, S., Rosenfeld, M. G., and Glass, C. K. (1993) Differential orientations of the DNA-binding domain and carboxy-lerminal dimerization interface regulate binding site selection by nuclear receptor heterodimers. Genes & Dev. 7, 1423-1435
48. Luisi, B. F., Xu, W. X., Otwinowski, Z., Freedman, Z., P., Yamamoto, K. R., and Sigler, P. B. (1991) Cristallographic analysis of the interaction of the glucocorticoid receptor with DNA. Nature (London) 352, 497-505
49. Schwabe, J. W., Chapman, L., Finch, J. T., Rhodes, D., and Neuhaus, D. (1993) DNA recognition by the oestrogen receptor: from solution to crystal. Structure 1, 187-204
50. Forman, B. M., Umesone, K., Chen, J., and Evans, R. M. (1995) Unique response pathways are established by allosteric interactions among nuclear hormone receptors. Cell 81, 541-550
51. Kurokawa, R., DiRenzo, J., Boehm, M., Sugarman, J., Gloss, B., Rosenfeld, M. C., Heyman, R. A., and Glass, C. K. (1994) Regulation of retinoid signalling by receptor polarity and allosteric control of ligand binding. Nature (London) 371, 528-531
52. Perlmann, T., Rangarajan, P. N., Umesono, K., and Evans, R. M. (1993) Determinants for selective RAR and TR recognition of direct repent HREs. Genes & Dev. 7, 1411-1422
53. Zechel, C., Shen, X. Q., Chen, J. Y., Chen, Z. P., Chambon, P., and Gronemeyer, H. (1994) The dimerization interfaces formed between the DNA binding domains of RXR, RAR and TR determine the binding specificity and polarity of the full-length receptors to direct repeats. EMBO J. 13, 1425-1433
54. 3-thyroid hormone receptor heterodimer polarity directs ligand sensitivity of transactivation. Nature (London) 370, 382-386
55. Perlmann, T., and Jansson, L. (1995) A novel pathway for vitamin A signaling mediated by RXR heterodimerization with NGFI-B and NURRI. Genes & Dev. 9, 769-782
56. Zechel, C., Shen, X. Q., Chambon, P., and Gronemeyer, H. (1994) Dimerization interfaces formed between the DNA binding domains determine the cooperative binding of RXR/RAR and RXR/TR heterodimers to DR5 and DR4 elements. EMBO J. 13, 1414-1424
57. Rastinejad, F., Perlmann, T., Evans, R. M., and Sigler, P.B. (1995) Structural determinants of nuclear receptor assembly on DNA direct repeats. Nature (London) 375, 203-211
58. Zhang, X-K., Lehmann, J., Hoffmann, B., Dawson, M. I., Cameron, J., Graupner, C., Hermann, T., Tran, P., and Pfahl, M. (1992) Homodimer formation of retinoid X receptor induced by 9-cis retinoic acid. Nature (London) 358, 587-591
59. Chen, Z. P., Shemshedini, L., Durand, B., Noy, N., Chambon, P., and Gronemeyer, H. (1994) Pure and functionally homogeneous recombinant retinoid X receptor. J. Biol. Chem. 269, 25770-25776
60. Heery, D. M., Pierrat, B., Gronemeyer, H., Chambon, P., and Losson, R. (1994) Homo- and heterodimers of the retinoid X receptor (RXR) activated transcription in yeast. Nucleic Acids Res. 22, 726-731
61. Dey, A., Minucci, S., and Ozato., K. (1994) Ligand-dependent occupancy of the retinoic acid receptor beta 2 promoter in vivo. Mol. Cell Biol. 14, 8191-8201
62. Apfel, C. M., Kamber, M., Klaus, M., Mohr, P., Keidel, S., and LeMotte, P. K. (1995) Enhancement of HL-60 differentiation by a new class of retinoids with selective activity on retinoid X receptor. J. Biol. Chem. 270, 30765-30772
63. Leblanc, B. P., and Stunnenberg, H. G. (1995) 9Cis retinoic acid signalling: changing partners causes some excitement. Genes & Dev. 9, 1811-1816
64. Rosen, E. D., O'Donnell, A. L., and Koenig, R. J. (1992) Ligand-dependent synergy of thyroid hormone and retinoid X receptors. J. Biol. Chem. 267, 22010-22013
65. Carlberg, C., Bendik, I., Wyss, A., Meier, E., Sturzenbecker, L.J., Grippo, J.F., and Hunziker, W. (1993) Two nuclear signalling pathways for vitamin D. Nature (London) 361, 657-660
66. Durand, B., Saunders, M., Gaudon, C., Roy, B., Losson, R., and Chambon, F. (1994) Activation function 2 (AF-2) of retinoic acid receptor and 9-cis retinoic acid receptor: presence of a conserved autonomous constitutive activating domain and influence of the nature of the response element on AF-2 activity. EMBO J. 13, 5370-5382
67. Roy, B., Taneja, R., and Chambon, P. (1995) Synergistic activation of retinoic acid (RA)-responsive genes and induction of embryonal carcinoma cell differentiation by a RAR receptor a (RARα)-, RARβ or RARγ-selective ligand in combination with a retinoid X receptor-specific ligand. Mol. Cell. Biol. 15, 6181-6187
68. Taneja, R., Roy, B., Zusi, C.F., Ostrowski, J., Reczek, P. R., and Chambon, F. (1996) Cell-type and promoter-context dependent RAR redundancies for RARβ2 and Hoxa-1 activation in F9 and P19 cells can be artefactually generated by gene knockouts. Proc. Natl. Acad. Sci. In press
69. Taneja, R., Bouillet, P., Boylan, J., Gaub, M. P., Roy, B., Gudas, L., and Chambon; P. (1995) Reexpression of retinoic acid receptor (RAR)γ or overexpression of RARα or KARβ in RARγ-null F9 cells reveals a partial functional redundancy between the three RAR types. Proc. Natl. Acad. Sci. USA 92, 7854-7858
70. Clifford, J., Chiba, H., Sobieszczuk, D. Metzger, D., and Chambon, P. (1996) RXRα-null F9 embryonal carcinoma cells arc resistant to the differentiation, antiproliferative and apoptotic effects of retinoids. EMBO J. In press
71. Mangelsdorf, D. J., Umesono, K., Kliewer, S. A., Borgmeyer, U., Ong, E. S., and Evans, R. M. (1991) A direct repeat in the cellular retinol binding protein type II gene confers differential regulation by RXR and RAR. Cell 66, 555-561.
72. 3. J. Biol. Chem. 270, 23906-23909
73. Davis, K. D., Berrodin, T. J., Stelmach, J. F., Winkler, J. D., and Lazar, M. A. (1994) Endogenous retinoid X receptors can function as hormone receptors in pituitary cells. Mol. Cell. Biol. 14, 7105-7110
74. Folkers, C. F., van der Leede, B. J., and van der Saag, P. T. (1993) The retinoic acid receptor-beta 2 contains two separate cell-specific transactivation domains, at the N-terminus and in the ligand-binding domain. Mol. Endocrinol. 7, 616-627
75. Heery, D. M., Zacharewski, T., Pierrat, B., Gronemeyer, H., Chambon, P., and Losson, R. (1993) Efficient transactivation by retinoic acid receptors in yeast requires retinoid X receptors, Proc. Natl. Acad. Sci. USA 90, 4281-4285
76. Tjian, R., and Maniatis, T. (1994) Transcriptional activation: a complex puzzle with few easy pieces. Cell 77, 5-8
77. Barettino, D., Vivaneo Ruiz, M. M., and Stunnenberg, H. C. (1994) Characturization of the ligand-dependent transactivation domain of thyroid hormone receptor. EMBO J. 13, 3039-3049
78. Leng, X., Blanco, J. Tsai, S. Y. Ozato, K., O'Malley, B. W., and Tsai, M. J. (1995) Mouse retinoid X receptor contains a separable ligand-binding and transactivation domain in its E region. Mol. Cell Biol. 15, 255-263
79. Saatcioglu, F., Bartunek, P., Deng, T., Zenke, M., and Karin, M. (1993) A conserved C-terminal sequence that is deleted in v-ErbA is essential for the biological activities of c-ErbA (the thyroid hormone receptor). Mol. Cell Biol. 13, 3675-3685
80. Danielian, P.S., White, R. Lees, J. A., and Parker, M. C. (1992) Identification of a conserved region required for hormone dependent transcriptional activation by steroid hormone receptors [published erratum appears in EMBO J. 1992 Jun; 11 (6), 2366]. EMBO J. 11, 1025-1033
81. Le Douarin, B., Zechel, C., Garnier, J.-M., Lutz, Y., Tora, L., Pierrat, B., Heery, D., Gronemeyer, H., Chambon, P., and Losson, R. (1995) TIF1, a potential mediator of the ligand-dependent activation function (AF-2) of nuclear receptors, is fused to B-raf in the oncogenic protein T18. EMBO J. 14, 2020-2033
82. vom Baur, K., Zechel, C., Heery, D., Heine, M., Garnier, J. M., Vivat, V., Le Douarin, B., Gronemeyer, H., Chambon, P., and Losson, R. (1995) Differential ligand-dependent interactions between the AF-2 activating domain of nuclear receptors and the putative transcriptional intermediary factors mSUG1 and TIF1. EMBO J. 15, 110-124
83. Bocquel, M.-T., Kumar, V., Stricker, C., Chambon, P., and Gronemeyer, H. (1989) The contribution of the N- and C-terminal regions of steroid receptors to activation of transcription is both receptor and cell-specific. Nucleic Acids Res. 17, 2581-2595
84. Meyer, M. K., Gronemeyer, H., Turcotte, B., Boequel, M. T., Tasset, D., and Chambon, P. (1989) Steroid hormone receptors compete for factors that mediate their enhancer function. Cell 57, 433-442
85. Tasset, D., Tora, L., Fromental, C., Scheer, E., and Chambon, P. (1990) Distinct classes of transcriptional activating domains function by different mechanisms. Cell 62, 1177-1187
86. Tora, L., White, J., Brou, C., Tasset, D., Webster, N., Scheer, E., and Chambon, P. (1989) The human estrogen receptor has two independent nonacidic transcriptional activation functions. Cell 59, 477-487
87. Berry, M., Metzger, D., and Chambon, P. (1990) Role of the two activating domains of the oestrogen receptor in the cell-type and promoter-context dependent agonistic activity of the anti-oestrogen 4-hydroxytamoxifen. EMBO J. 9, 2811-2818
88. Halachmi, S., Marden, E., Martin, G., MacKay, H., Abbondanza, C., and Brown, M. (1994) Oestrogen receptor-associated proteins: possible mediators of hormone-induced transcription. Science 264, 1455-1458
89. Cavaillès, V., Dauvois, S., Danielian, P. S., and Parker, M. C. (1994) Interaction of proteins with transcriptionally active estrogen receptors. Proc. Natl. Acad. Sci. USA 91, 10009-10013
90. Kurokawa, R., Soderstrom, M., Horlein, A., Halachmi, S., Brown, M., Rosenfeld, M. C., and Glass, C. K. (1995) Polarity-specific activities of retinuic acid receptors determined by a co-repressor. Nature (London) 377, 451-454
91. Voegel, J. J., Heine, M. J. S., Zechel, C., Chambon, P., and Gronemeyer, H. (1996) A 160 kDa transcriptional mediator for the ligand-dependent activation function AF-2 of nurlear receptors. EMBO J. In press
92. Lee, J. W., Ryan, F., Swaffield, J. C., Johnston, S. A.,and Moore, D. A. (1995) Interaction of thyroid-hormone receptor with a conserved transcriptional mediator. Nature (London) 374, 91-94
93. Cavaillès, V., Dauvois, S., L'Horset, F., Lopez, C., Hoare, S., Kushner, P. J., and Parker, M. G. (1995) Nuclear factor RIPI40 modulates transcriptional activation by the estrogen receptor. EMBO J. 14, 3741-3751
94. Onate, S. A., Tsai, S. Y., Tsai, M. J., and O'Malley, B. (1995) Sequence and characterization of a coactivator for the steroid hormone receptor superfamily. Science 270, 1354-1357
95. Beato, M., Herrlich, P., and Schütz, G. (1995) Steroid hormone receptors: many actors in search of a plot. Cell 83, 851-857
96. Wreggett, K. A., Hill, F., James, P. S., Hutchings, A., Butcher, G. W., and Singh, P. B. (1994) A mammalian homologue of Drosophila heterochromatin protein 1 (HP1) is a component of constitutive heterochromatin. Cytogenet. Cell Genet. 66, 99-103
97. Schulman, I. G., Chakravarti, D., Juguilon, H., Romo, A., and Evans, R. M. (1995) Interactions between the retinoid X receptor and a conserved region of the TATA-binding protein mediate hormone-dependent transactivation. Proc. Natl. Acad. Sci. USA 92, 8288-8292
98. Martin, B., Renkawitz, R., and Muller, M. (1994) Two silencing sub-domains of v-erbA synergize with each other, but not with RXR. Nucleic Acids Res. 22, 4898-4905
99. Perlmann, T., and Vennström, B. (1995) The sound of silence. Nature (London) 377, 387-388
100. Horlein, A. J., Määr, A. M., Heinzel, T., Torehia, J., Gloss, B., Kurokawa, R., Ryan, A., Kamei, Y., Soderstrom, M., Glass, C. K., and Rosenfeld, M. G. (1995) Ligand-independent repression by the thyroid hormone receptor mediated by a nuclear receptor co-repressor. Nature (London) 377, 397-403
101. Chen, J. D., and Evans, R. M. (1995) A transcriptional co-repressor that interacts with nuclear hormone receptors. Nature (London) 377, 454-457
102. Bourguet, W., Ruff, M., Chambon, P. Gronemeyer, H., and Moras, D. (1995) Crystal structure of the ligand binding domain of the human nuclear receptor RXRα. Nature 375, 377-382
103. Renaud, J. P., Rochel, N., Ruff, M., Vivat, V., Chambon, P., Gronemeyer, H., and Moras, D. (1995) Crystal structure of the RARγ ligand-binding domain bound to all-trans retinoic acid. Nature (London) 378, 681-689
104. Forman, B. M., and Samuels, H. H. (1990) Interactions among a subfamily of nuclear hormone receptors: The regulatory zipper model. Mol. Endocrinol. 4, 1293-1301
105. Wagner, R. L., Apriletti, J. W., McGrath, M. E., West, B. L., Baxter, J. D., and Fletterick, R. J. (1995) A structural role for hormone in the thyroid hormone receptor. Nature (London) 378, 690-697
106. Wurtz, J. M., Bourguet, W., Renaud, J. P., Vivat, V., Chambon, P., Moras, D., and Gronemeyer, H. (1996) A canonical structure for the ligand binding domain of nuclear receptors. Nature (London) Struct. Biol. 3, 87-94
107. Nicholson, R. C., Mader, S., Nagpal, S., Leid, M., Rochelle Egly, C., and Chambon, P. (1990) Negative regulation of the rat stromelysin gene promoter by retinoic acid is mediated by an AP1 binding site. EMBO J. 9, 4443-44, 54
108. Lafyatis, R., Kim, S. J., Angel, P., Roberts, A. B., Sporn, M. B., Karin, M., and Wilder, R. L. (1990) Interleukin-1 stimulates and all-trans-retinoic acid inhibits collagenase gene expression through its 5′ activator protein-1-binding site. Mol. Endocrinol. 4, 973-980
109. Yang-Yen, H. F., Zhang, X. K., Graupner, C., Tzukerman, M., Sakamoto, B., Karin, M., and Pfahl, M. (1991) Antagonism between retinoic acid receptors and AP-1: implications for tumor promotion and inflammation. New. Biol. 3, 1206-1219
110. Schule, R., Rangarajan, P., Yang, N., Kliewer, S., Ransone, L. J., Bolado, J., Verma, I. M., and Evans, R. M. (1991) Retinoic acid is a negative regulator of AP-1-responsive genes. Proc. Natl. Acad. Sci. USA 88, 6092-6096
111. Salbert, G., Fanjul, A., Piedrafita, F. J., Lu, X. P., Kim, S. J., Tran, P., and Pfahl, M. (1993) Retinoic acid receptors and retinoid X receptor-alpha down-regulate the transforming growth factor-beta 1 promoter by antagonizing AP-1 activity. Mol. Endocrinol. 7, 1347-1356
112. Saatcioglu, F., Claret, F. X., and Karin, M. (1994) Negative transcriptional regulation by nuclear receptors. Sem. Cancer Biol. 5, 347-359
113. Pfahl, M. (1993) Nuclear receptor/AP-1 interaction. Endocr. Rev. 14, 651-650
114. Herrlich, P., and Ponta, H. (1994) Mutual cross-modulalion of steroid/retinoic acid receptor and AP-1 transcription factor activities. A novel property with practical implications. Trends Endocrinol. Metab. 5, 341-346
115. Shemshedini, L., Knauthe, R., Sassone Corsi, P., Pornon, A., and Gronemeyer, H. (1991) Cell-specific inhibitory and stimulatory effects of Fos and Jun on transcription activation by nuclear receptors. EMBO J. 10, 3839-3849
116. Chen, J. Y., Penco, S., Ostrowski, J., Balaguer, P., Pons, M., Starrett, J. E., Reczek, P., Chambon, P., and Gronemeyer, H. (1995) RAR-specific agonist/antaagonists which dissociate transactivation and AP1 transrepression inhibit anchorage-independent cell proliferation. EMBO J. 14, 1187-1197
117. Fanjul, A., Dawson, M. I., Hubbs, P. D., Jong, L., Cameron, J. F., Harlev, E., Graupner, G., Lu, X.-P., and Pfahl, M. (1994) A new class of retinoids with selective inhibition of AP-1 inhibits proliferation. Nature (London) 372, 107-111
118. Nagpal, S., Athanika, J., and Chandraratna, R. A. S. (1995) Separation of transactivation and AP1 antagonism functions of retinoic acid receptor α. J. Biol. Chem. 270, 923-927
119. Kato, S., Endoh, H., Masuhiro, T., Kitamoto, T., Uchiyama, S., Sasaki, H., Masushige, S., Gotoh, Y., Nishida, E., Kawashima, H., Metzger, D., and Chambon, P. (1995) Activation of the estrogen receptor through phosphorylation by mitogen-activated protein kinase. Science 270, 1491-1494
120. Kamei, Y., Xu, L. Heinzel, T., Torchia, J., Kurokawa, R., Gloss, B., Lin, S-C., Heyman, R.A., Rose, D.W., Glass, C.K., and Rosenfield, M.C. (1996). A CBP integrator complex mediates transcriptional activation and AP-1 inhibition by nuclear receptors. Cell 85, 403-414