The receptor-DNA complex determines the retinoid response: A mechanism for the diversification of the ligand signal

Molecular and Cellular Biology

Volumn 16, Issue 8, 1996, Pages 4137-4146

  La Vista Picard, Nathalie ^a,b   Hobbs, Peter D ^c   Pfahl, Michaela ^a   Dawson, Marcia I ^c   Pfahl, Magnus ^a,b  

^a SIDNEY KIMMEL CANCER CENTER   (United States)

^b BURNHAM INSTITUTE   (United States)

^c SRI INTERNATIONAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL NUCLEUS RECEPTOR; DNA; LIGAND; RECEPTOR SUBTYPE; RETINOIC ACID RECEPTOR; RETINOID; RETINOID X RECEPTOR;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; DNA BINDING; LIGAND BINDING; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; RECEPTOR BINDING; RECEPTOR GENE; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION;

EID: 0029954388     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.16.8.4137     Document Type: Article

References (79)

1. Allenby, G., M. T. Bocquel, M. Saunders, S. Kazmer, J. Speck, M. Rosenberger, A. Lovey, P. Kastner, J. F. Grippo, P. Chambon, and A. A. Levin. 1993. Retinoic acid receptors and retinoid X receptors: interactions with endogenous retinoic acids. Proc. Natl. Acad. Sci. USA 90:30-34.
2. Apfel, R., D. Benbrook, E. Lernhardt, M. A. Ortiz, G. Salbert, and M. Pfahl. 1994. A novel orphan receptor specific for a subset of thyroid hormone-responsive elements and its interaction with the retinoid/thyroid hormone receptor subfamily. Mol. Cell. Biol. 14:7025-7035.
3. Baes, M., T. Gulick, H.-S. Choi, M. G. Martinoli, D. Simha, and D. D. Moore. 1994. A new orphan member of the nuclear hormone receptor superfamily that interacts with a subset of retinoic acid response elements. Mol. Cell. Biol. 14:1544-1552.
4. Beato, M. 1989. Gene regulation by steroid hormones. Cell 56:335-344.
5. Benbrook, D., W. Lernhardt, and M. Pfahl. 1988. A new retinoic acid receptor identified from a hepatocellular carcinoma. Nature (London) 333: 659-672.
6. Bernard, B. A., J.-M. Bernardon, C. Delescluse, B. Martin, M.-C. Lenoir, J. Maignan, B. Charpentier, W. R. Pilgrim, U. Reicher, and B. Shroot. 1992. Identification of synthetic retinoids with selectivity for human nuclear retinoic acid receptor γ. Biochem. Biophys. Res. Commun. 186:977-983.
7. Boehm, M. F., L. Zhang, B. A. Badea, S. K. White, D. E. Mais, E. Berger, C. M. Suto, M. E. Goldman, and R. A. Heyman. 1994. Synthesis and structure-activity relationships of novel retinoid X receptor-selective retinoids. J. Med. Chem. 37:2930-2941.
8. Bollag, W. 1983. Vitamin A and retinoids: from nutrition to pharmacotherapy in dermatology and oncology. Lancet i:860-863.
9. Bollag, W., and E. E. Holdener. 1992. Retinoids in cancer prevention and therapy. Ann. Oncol. 3:513-526.
10. Brand, N., M. Petkovich, A. Krust, H. de Thé, A. Marchio, P. Tiollais, and D. Dejean. 1988. Identification of a second human retinoic acid receptor. Nature (London) 332:850-853.
11. 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.
12. Castaigne, S., C. Chomienne, M. T. Daniel, P. Ballerini, R. Berger, P. Fenaux, and L. Degos. 1990. All-trans-retinoic acid as a differentiation therapy for acute promyelocytic leukemia. Blood 76:1704-1709.
13. Chambon, P. 1994. The retinoid signaling pathway: molecular and genetic analyses. Semin. Cell Biol. 5:115-125.
14. Dawson, M. I., L. Jong, P. D. Hobbs, J. F. Cameron, W.-R. Chao, M. Pfahl, M.-O. Lee, B. Shroot, and M. Pfahl. Conformation effects on retinoid receptor selectivity. Submitted for publication.
15. Delescluse, C., M. T. Cavey, B. Martin, B. A. Bernard, U. Reichert, J. Maignan, M. Darmon, and B. Shroot. 1991. Selective high affinity retinoic acid receptor α or β-γ ligands. Mol. Pharmacol. 40:556-562.
16. de Thé, H., M. M. Vivanco-Ruiz, P. Tiollais, H. Stunnenberg, and A. Dejean. 1990. Identification of a retinoic acid response element in the retinoic acid receptor gene. Nature (London) 343:177-180.
17. Edwards, M. K. S., and M. W. McBurney. 1983. The concentration of retinoic acid determines the differentiated cell types formed by a teratocarcinoma cell line. Dev. Biol. 98:187-191.
18. Ellis, L., E. Clausen, D. O. Nagan, M. Edery, R. A. Roth, and W. J. Rutten. 1986. Replacement of insulin receptor tyrosine residues 1162 and 1163 compromises insulin-stimulated kinase activity and uptake of 2-deoxyglucose. Cell 45:721-732.
19. Fanjul, A., M. I. Dawson, P. D. Hobbs, L. Jong, J. F. Cameron, E. Harlev, G. Graupner, X.-P. Lu, and M. Pfahl. 1994. A novel class of retinoids with selective anti-AP-1 activity exhibit anti-proliferative activity. Nature (London) 372:107-111.
20. Giguere, V., E. S. Ong, P. Seigi, and R. M. Evans. 1987. Identification of a receptor for the morphogen retinoic acid. Nature (London) 330:624-629.
21. Glass, C. K., J. DiRenzo, R. Kurokawa, and Z. Han. 1991 Regulation of gene expression by retinoic acid receptors. DNA Cell Biol. 10:623-638.
22. Goodman, D. S. 1984. Vitamin A and retinoids in health and disease. N. Engl. J. Med. 310:1023-1031.
23. Graupner, G., G. Malle, J. Maignan, G. Lang, M. Prunieras, and M. Pfahl. 1991. 6′-Substituted naphthalene-2-carboxylic acid analogs, a new class of retinoic acid receptor subtype-specific ligand. Biochem. Biophys. Res. Commun. 179:1554-1561.
24. Hermann, T., B. Hoffmann, X. K. Zhang, P. Tran, and M. Pfahl. 1992. Heterodimeric receptor complexes determine 3,5,3′-triiodothyronine and retinoid signaling specificities. Mol. Endocrinol. 6:1153-1162.
25. Heyman, R. A., D. J. Mangelsdorf, J. A. Cyck, R. B. Stein, G. Eichele, R. M. Evans, and C. Thaller. 1992. 9-cis-Retinoic acid is a high affinity ligand for the retinoid X receptor. Cell 68:397-406.
26. Hill, D. L., and C. J. Grubbs. 1992. Retinoids and cancer prevention. Annu. Rev. Nutr. 12:161-181.
27. Hoffmann, B., J. M. Lehmann, X.-K. Zhang, T. Hermann, G. Graupner, and M. Pfahl. 1990. A retinoic acid receptor specific clement controls the retinoic acid receptor-β promoter. J. Mol. Endocrinol. 4:1734-1743.
28. Hong, W. K., S. M. Lippman, L. M. Itri, D. Karp, J. S. Lee, R. Byers, S. P. Schantz, A. M. Kramer, R. Lotan, L. J. Peters, I. W. Dimery, W. B. Brown, and H. Goepfert. 1990. Prevention of second primary tumors with isotretinoin in squamous-cell carcinoma of the head and neck. N. Engl. J. Med. 323:795-801.
29. Huang, M.-E., Y.-C. Ye, S.-R. Chen, J.-R. Chai, J.-X. Lu, L. Zhoa, L.-J. Gu, and Z.-Y. Wang. 1988. Use of all-trans-retinoic acid in the treatment of acute promyelocytic leukemia. Blood 72:567-572.
30. Husmann, J., B. Hoffmann, D. G. Stump, F. Chytil, and M. Pfahl. 1992. A retinoic acid response element from the rat CRBPI promoter is activated by an RAR/RXR heterodimer. Biochem. Biophys. Res. Commun. 187:1558-1564.
31. Husmann, M., J. Lehmann, B. Hoffmann, T. Hermann, M. Tzukerman, and M. Pfahl. 1991. Antagonism between retinoic acid receptors. Mol. Cell. Biol. 11:4097-4103.
32. 3 signaling. Nature (London) 355:445-449.
33. Kliewer, S. A., K. Umesono, D. J. Noonan, R. A. Heyman, and R. M. Evans. 1992. Convergence of 9-cis-retinoic acid and peroxisome proliferator signalling pathways through heterodimer formation of their receptors. Nature (London) 358:771-774.
34. Kraemer, K. H., J. J. Di Giovanni, A. N. Moshell, R. E. Tarone, and G. L. Peck. 1988. Prevention of skin cancer in xeroderma pigmentosum with the use of oral isotretinoin. N. Engl. J. Med. 318:1633-1637.
35. Kraemer, K. H., J. J. Di Giovanni, and G. L. Peck. 1992. Chemoprevention of skin cancer in xeroderma pigmentosum. J. Dermatol. (Tokyo) 19:715-718.
36. Kurokawa, R., J. DiRenzo, M. Boehm, J. Sugarman, B. Gloss, M. Rosenfeld, R. A. Heyman, and C. K. Glass. 1994. Regulation of retinoid signalling by receptor polarity and allosteric control of ligand binding. Nature (London) 371:528-531.
37. Kurokawa, R., M. Soderstrom, A. Horlein, S. Halachmi, M. Brown, M. G. Rosenfeld, and C. K. Glass. 1995. Polarity-specific activities of retinoic acid receptors determined by a co-repressor. Nature (London) 377:451-454.
38. 37a. Kurokawa, R., V. C. Yu, A. Näär, S. Kyakumoto, Z. Han, S. Silverman, M. G. Rosenfeld, and C. K. Glass. 1993. Differential orientations of the DNA-binding domain and carboxy-terminal dimerization interface regulate binding site selection by nuclear receptor heterodimers. Genes Dev. 7:1423-1435.
39. Lee, M. O., P. D. Hobbs, X.-K. Zhang, M. I. Dawson, and M. Pfahl. 1994. A new retinoid antagonist inhibits the HIV-1 promoter. Proc. Natl. Acad. Sci. USA 91:5632-5636.
40. Lehmann, J. M., M. I. Dawson, P. D. Hobbs, M. Husmann, and M. Pfahl. 1991. Identification of retinoids with nuclear receptor subtype-selective activities. Cancer Res. 51:4804-4809.
41. Lehmann, J. M., L. Jong, A. Fanjul, J. F. Cameron, X.-P. Lu, P. Haefner, M. I. Dawson, and M. Pfahl. 1992. Retinoids selective for retinoid X receptor response pathways. Science 258:1944-1946.
42. 3 response: hormonal cross talk by ligand-induced squelching. Mol. Cell. Biol. 13:7698-7707.
43. Lehmann, J. M., X.-K. Zhang, and M. Pfahl. 1992. RARγ2 expression is regulated through a retinoic acid response element embedded in Sp1 sites. Mol. Cell. Biol. 12:2976-2985.
44. Leid, M., P. Kastner, and P. Chambon. 1992. Multiplicity generates diversity in the retinoic acid signalling pathways. Trends Biochem. Sci. 17:427-433.
45. Leroy, P., A. Krust, P. Kastner, C. Mendelsohn, A. Zelent, and P. Chambon. 1992. Retinoic acid receptors, p. 2-25. Oxford University Press, New York.
46. Levin, A. A., L. M. Sturzenbecker, S. Kazmer, T. Busakowski, C. Huselton, G. Allenby, J. Speck, C. Kratzeisen, M. Rosenberger, A. Lovey, and J. F. Grippo. 1992. 9-cis-Retinoic acid steroisomer binds and activates the nuclear receptor RXRα. Nature (London) 355:359-361.
47. Lippmann, S. M., J. F. Kessler, and F. L. Meyskens, Jr. 1987. Retinoids as preventive and therapeutic anticancer agents. Cancer Treat. Rep. 71:493-515.
48. Lombardo, A., E. Costa, W.-R. Chao, L. Toll, P. Hobbs, L. Jong, M. Lee, M. Pfahl, K. Ely, and M. Dawson. 1994. Recombinant human retinoic acid receptor β: binding of synthetic retinoids and transcriptional activation. J. Biol. Chem. 269:7297-7303.
49. Lotan, R. 1981. Effects of vitamin A and its analogs (retinoids) on normal and neoplastic cells. Biochim. Biophys. Acta 605:33-91.
50. 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.
51. Mader, S., J.-Y. Chen, Z. Chen, J. White, P. Chambon, and H. Gronemeyer. 1993. The distinct binding site repertoires of RAR, RXR, and TR homo- and heterodimers are dictated by the binding specificities of their DNA binding domains. EMBO J. 12:5029-5041.
52. Mangelsdorf, D. J., U. Borgmeyer, R. A. Heyman, J.-Y. Zhan, E. S. Ong, A. E. Oro, A. Kakizuka, and R. M. Evans. 1992. Characterization of three RXR genes that mediate the action of 9-cis-RA retinoic acid. Genes Dev. 6:329-344.
53. Mangelsdorf, D. J., K. Umesono, and R. M. Evans. 1994. The retinoid receptors, p. 319-349. In M. B. Sporn, A. B. Roberts, and D. S. Goodman (ed.), The retinoids, 2nd ed. Academic Press, Orlando, Fla.
54. Mangelsdorf, D. J., K. Umesono, S. A. Kliewer, U. Borgmeyer, E. S. Ong, and R. M. Evans. 1991. A direct repeat in the cellular retinol-binding protein type II gene confers differential regulation by RXR and RAR. Cell 66:555-561.
55. 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 response genes. EMBO J. 11:1419-1435.
56. Nagpal, S., S. Friant, H. Nakshatri, and P. Chambon. 1993. Evidence for two autonomous transactivation functions (AF-1 and AF-2) and heterodimerization in vivo. EMBO J. 12:2349-2360.
57. Nagpal, S., M. Saunders, P. Kastner, B. Durand, H. Nakshatri, and P. Chambon. 1992. Promoter context- and response element-dependent specificity of the transcriptional activation and modulating functions of retinoic acid receptors. Cell 70:1007-1019.
58. Petkovich, M., N. J. Brand, A. Krust, and P. Chambon. 1987. Human retinoic acid receptor belongs to the family of nuclear receptors. Nature (London) 330:444-450.
59. Pfahl, M. 1993. Nuclear receptor/AP-1 interaction. Endocr. Rev. 14:651-658.
60. Pfahl, M., R. Apfel, I. Bendik, A. Fanjul, G. Graupner, M.-O. Lee, N. La Vista, X.-P. Lu, J. Piedrafita, M. A. Ortiz, G. Salbert, and X.-K. Zhang. 1994. Nuclear retinoid receptors and their mechanisms of action. Vitam. Horm. 49:327-382.
61. Pijnappel, W. W. M., H. F. J. Hendriks, G. E. Folkers, C. E. van den Brink, E. J. Dekker, C. Edelenbosch, P. T. van der Saag, and A. J. Durston. 1993. The retinoid ligand 4-oxo-retinoic acid is a highly active modulator of positional specification. Nature (London) 366:340-344.
62. Predki, P. F., D. Zamble, S. S. Bibuddhendra, and V. Giguere. 1994. Ordered binding of retinoic acid and retinoid-X receptors to asymmetric response elements involves determinants adjacent to the DNA-binding domain. Mol. Endocrinol. 8:31-39.
63. Rottman, J. N., R. L. Widom, B. Nadal-Ginard, V. Mahdavi, and S. K. Karathanasis. 1991. A retinoic acid-responsive element in the apolipoprotein AI gene distinguishes between two different retinoic acid response pathways. Mol. Cell. Biol. 11:3814-3820.
64. 1 promoter by antagonizing AP-1 activity. Mol. Endocrinol. 7:1347-1356.
65. Saurat, J. H. 1992. Side effects of systemic retinoids and their clinical management. J. Am. Acad. Dermatol. 27:23-28.
66. Schaefer, H., and U. Reichert. 1990. Retinoids and their perspectives in dermatology. Nouv. Dermatol. 9:3-6.
67. Schüle, R., P. Rangarajan, N. Yang, S. Kliewer, L. J. Ransone, J. Bolado, I. M. Verma, and R. M. Evans. 1991. Retinoic acid is a negative regulator of AP-1-responsive genes. Proc. Natl. Acad. Sci. USA 88:6092-6096.
68. Smith, M. A., D. R. Parkinson, B. D. Cheson, and M. A. Friedman. 1992. Retinoids in cancer therapy. J. Clin. Oncol. 10:839-864.
69. Sporn, M. B., A. B. Roberts, and D. S. Goodman (ed.). 1994. The retinoids, 2nd ed. Academic Press, Inc., Orlando, Fla.
70. Sucov, H. M., K. K. Murakami, and R. M. Evans. 1990. Characterization of an autoregulated response element in the mouse retinoic acid receptor type β gene. Proc. Natl. Acad. Sci. USA 87:5392-5396.
71. Thaller, C., and G. Eichele. 1990. Isolation of 3,4-didehydroretinoic acid, a novel morphogenetic signal in the chick wing bud. Nature (London) 345: 815-819.
72. Tini, M., G. Otulakowski, M. L. Breitman, L. C. Tsui, and V. Giguere. 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.
73. 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.
74. Yang-Yen, H.-F., X.-K. Zhang, G. Graupner, M. Tzukerman, B. Sakamoto, M. Karin, and M. Pfahl. 1991. Antagonism between retinoic acid receptors and AP-1: implication for tumor promotion and inflammation. New Biol. 3:1206-1219.
75. Yu, V. C., C. Delsert, B. Andersen, J. M. Holloway, O. V. Devary, A. M. Näär, S. Y. Kim, J.-M. Goutin, 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.
76. Zechel, C., X.-Q. Shen, J.-Y. Chen, Z.-P. Chen, P. Chambon, and H. Gronemeyer. 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.
77. Zhang, X. K., B. Hoffmann, P. Tran, G. Graupner, and M. Pfahl. 1992. Retinoid X receptor is an auxiliary protein for thyroid hormone and retinoic acid receptors. Nature (London) 355:441-446.
78. Zhang, X.-K., J. Lehmann, B. Hoffmann, M. I. Dawson, J. Cameron, G. Graupner, T. Hermann, P. Tran, and M. Pfahl. 1992. Homodimer formation of retinoid X receptor induced by 9-cis-retinoic acid. Nature (London) 358: 587-591.
79. Zhang, X.-K., and M. Pfahl. 1993. Regulation of retinoid and thyroid action through homo- and heterodimeric receptors. Trends Endocrinol. Metab. 4:156-162.