Retinoid X receptor regulates Nur77/thyroid hormone receptor 3-dependent apoptosis by modulating its nuclear export and mitochondrial targeting

Molecular and Cellular Biology

Volumn 24, Issue 22, 2004, Pages 9705-9725

  Cao, Xihua ^a   Liu, Wen ^a   Lin, Feng ^a   Li, Hui ^a   Kolluri, Siva Kumar ^a   Lin, Bingzhen ^a   Han, Young Hoon ^a   Dawson, Marcia I ^a   Zhang, Xiao Kun ^a  

^a BURNHAM INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL NUCLEUS RECEPTOR; LIGAND; PROTEIN BCL 2; RETINOIC ACID RECEPTOR; RETINOID X RECEPTOR ALPHA; THYROID HORMONE RECEPTOR; THYROID HORMONE RECEPTOR 3; UNCLASSIFIED DRUG; VITAMIN D RECEPTOR;

ANIMAL CELL; APOPTOSIS; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL NUCLEUS; CONTROLLED STUDY; DIMERIZATION; DNA BINDING; HUMAN; HUMAN CELL; INTRACELLULAR TRANSPORT; LIGAND BINDING; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN TARGETING;

ACTIVE TRANSPORT, CELL NUCLEUS; AMINO ACID SEQUENCE; ANIMALS; APOPTOSIS; BASE SEQUENCE; CELL LINE; DIMERIZATION; DNA; DNA-BINDING PROTEINS; HUMANS; MITOCHONDRIA; MOLECULAR SEQUENCE DATA; MUTATION; PROTO-ONCOGENE PROTEINS C-BCL-2; RECEPTORS, CYTOPLASMIC AND NUCLEAR; RECEPTORS, STEROID; RECEPTORS, THYROID HORMONE; RECOMBINANT FUSION PROTEINS; RETINOID X RECEPTOR ALPHA; RNA, SMALL INTERFERING; TETRADECANOYLPHORBOL ACETATE; TRANSCRIPTION FACTORS;

ANIMALIA; NES;

EID: 7644221712     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.24.22.9705-9725.2004     Document Type: Article

References (92)

1. Aarnisalo, P., C. H. Kim, J. W. Lee, and T. Perlmann. 2002. Defining requirements for heterodimerization between the retinoid X receptor and the orphan nuclear receptor Nurr1. J. Biol. Chem. 277:35118-35123.
2. Baumann, C. T., P. Maruvada, G. L. Hager, and P. M. Yen. 2001. Nuclear cytoplasmic shuttling by thyroid hormone receptors, multiple protein interactions are required for nuclear retention. J. Biol. Chem. 276:11237-11245.
3. Bissonnette, R. P., T. Brunner, S. B. Lazarchik, N. J. Yoo, M. F. Boehm, D. R. Green, and R. A. Heyman. 1995. 9-cis retinoic acid inhibition of activation-induced apoptosis is mediated via regulation of fas ligand and requires retinoic acid receptor and retinoid X receptor activation. Mol. Cell. Biol. 15:5576-5585.
4. Bourguet, W., M. Ruff, P. Chambon, H. Gronemeyer, and D. Moras. 1995. Crystal structure of the ligand-binding domain of the human nuclear receptor RXR-α. Nature 375:377-382.
5. Bourguet, W., V. Vivat, J. M. Wurtz, P. Chambon, H. Gronemeyer, and D. Moras. 2000. Crystal structure of a heterodimeric complex of RAR and RXR ligand-binding domains. Mol. Cell 5:289-298.
6. Bunn, C. F., J. A. Neidig, K. E. Freidinger, T. A. Stankiewicz, B. S. Weaver, J. McGrew, and L. A. Allison. 2001. Nucleocytoplasmic shuttling of the thyroid hormone receptor alpha. Mol. Endocrinol. 15:512-533.
7. Chang, C., J. Kokontis, S. S. Liao, and Y. Chang. 1989. Isolation and characterization of human TR3 receptor: a member of steroid receptor superfamily. J. Steroid Biochem. 34:391-395.
8. Chen, G. Q., B. Lin, M. I. Dawson, and X. K. Zhang. 2002. Nicotine modulates the effects of retinoids on growth inhibition and RAR beta expression in lung cancer cells. Int. J. Cancer 99:171-178.
9. Davis, I. J., T. G. Hazel, R. H. Chen, J. Blenis, and L. F. Lau. 1993. Functional domains and phosphorylation of the orphan receptor Nur77. Mol. Endocrinol. 7:953-964.
10. Dawson, M. I., P. D. Hobbs, V. J. Peterson, M. Leid, C. W. Lange, K. C. Feng, G. Chen, J. Gu, H. Li, S. K. Kolluri, X. Zhang, Y. Zhang, and J. A. Fontana. 2001. Apoptosis induction in cancer cells by a novel analogue of 6-[3-(1-adamantyl)-4-hydroxyphenyl]-2-naphthalenecarboxylic acid lacking retinoid receptor transcriptional activation activity. Cancer Res. 61:4723-4730.
11. DeFranco, D. B. 1999. Regulation of steroid receptor subcellular trafficking. Cell Biochem. Biophys. 30:1-24.
12. Dufour, J. M., and K. H. Kim. 1999. Cellular and subcellular localization of six retinoid receptors in rat testis during postnatal development: identification of potential heterodimeric receptors. Biol. Reprod. 61:1300-1308.
13. 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.
14. Elbashir, S. M., J. Harborth, W. Lendeckel, A. Yalcin, K. Weber, and T. Tuschl. 2001. Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 411:494-498.
15. Fahrner, T. J., S. L. Carroll, and J. Milbrandt. 1990. The NGFI-B protein, an inducible member of the thyroid/steroid receptor family, is rapidly modified posttranslationally. Mol. Cell. Biol. 10:6454-6459.
16. 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.
17. Gampe, R. T., Jr., V. G. Montana, M. H. Lambert, A. B. Miller, R. K. Bledsoe, M. V. Milburn, S. A. Kliewer, T. M. Willson, and H. E. Xu. 2000. Asymmetry in the PPARγ/RXRα crystal structure reveals the molecular basis of heterodimerization among nuclear receptors. Mol. Cell 5:545-555.
18. Gampe, R. T., Jr., V. G. Montana, M. H. Lambert, G. B. Wisely, M. V. Milburn, and H. E. Xu. 2000. Structural basis for autorepression of retinoid X receptor by tetramer formation and the AF-2 helix. Genes Dev. 14:2229-2241.
19. Hazel, T. G., R. Misra, I. J. Davis, M. E. Greenberg, and L. F. Lau. 1991. Nur77 is differentially modified in PC12 cells upon membrane depolarization and growth factor treatment. Mol. Cell. Biol. 11:3239-3246.
20. Hazel, T. G., D. Nathans, and L. F. Lau. 1988. A gene inducible by serum growth factors encodes a member of the steroid and thyroid hormone receptor superfamily. Proc. Natl. Acad. Sci. USA 85:8444-8448.
21. Hedvat, C. V., and S. G. Irving. 1995. The isolation and characterization of MINOR, a novel mitogen-inducible nuclear orphan receptor. Mol. Endocrinol. 9:1692-1700.
22. Heyman, R. A., D. J. Mangelsdorf, J. A. Dyck, 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.
23. Hirata, Y., K. Kiuchi, H. C. Chen, J. Milbrandt, and G. Guroff. 1993. The phosphorylation and DNA binding of the DNA-binding domain of the orphan nuclear receptor NGFI-B. J. Biol. Chem. 268:24808-24812.
24. Holmes, W. F., D. R. Soprano, and K. J. Soprano. 2003. Comparison of the mechanism of induction of apoptosis in ovarian carcinoma cells by the conformationally restricted synthetic retinoids CD437 and 4-HPR. J. Cell Biochem. 89:262-278.
25. Holmes, W. F., D. R. Soprano, and K. J. Soprano. 2002. Elucidation of molecular events mediating induction of apoptosis by synthetic retinoids using a CD437-resistant ovarian carcinoma cell line. J. Biol. Chem. 277: 45408-45419.
26. Ijpenberg, A., N. S. Tan, L. Gelman, S. Kersten, J. Seydoux, J. Xu, D. Metzger, L. Canaple, P. Chambon, W. Wahli, and B. Desvergne. 2004. In vivo activation of PPAR target genes by RXR homodimers. EMBO J. 23: 2083-2091.
27. Janssen, J. J., E. D. Kuhlmann, A. H. van Vugt, H. J. Winkens, B. P. Janssen, A. F. Deutman, and C. A. Driessen. 1999. Retinoic acid receptors and retinoid X receptors in the mature retina: subtype determination and cellular distribution. Curr. Eye Res. 19:338-347.
28. Jeong, J. H., J. S. Park, B. Moon, M. C. Kim, J. K. Kim, S. Lee, H. Suh, N. D. Kim, J. M. Kim, Y. C. Park, and Y. H. Yoo. 2003. Orphan nuclear receptor Nur77 translocates to mitochondria in the early phase of apoptosis induced by synthetic chenodeoxycholic acid derivatives in human stomach cancer cell line SNU-1. Ann. N. Y. Acad. Sci. 1010:171-177.
29. Kastner, P., M. Mark, and P. Chambon. 1995. Nonsteroid nuclear receptors: what are genetic studies telling us about their role in real life? Cell 83:859-869.
30. Katagiri, Y., K. Takeda, Z. X. Yu, V. J. Ferrans, K. Ozato, and G. Guroff. 2000. Modulation of retinoid signalling through NGF-induced nuclear export of NGFI-B. Nat. Cell Biol. 2:435-440.
31. Kolluri, S. K., X. Cao, N. Bruey-Sedano, B. Lin, F. Lin, Y. Han, M. I. Dawson, and X. Zhang. 2003. Mitogenic effect of orphan receptor TR3 and its regulation by MEKK1 in lung cancer cells. Mol. Cell. Biol. 23:8651-8667.
32. Kousteni, S., T. Bellido, L. I. Plotkin, C. A. O'Brien, D. L. Bodenner, L. Han, K. Han, G. B. DiGregorio, J. A. Katzenellenbogen, B. S. Katzenellenbogen, P. K. Roberson, R. S. Weinstein, R. L. Jilka, and S. C. Manolagas. 2001. Nongenotropic, sex-nonspecific signaling through the estrogen or androgen receptors: dissociation from transcriptional activity. Cell 104:719-730.
33. Kudo, N., N. Matsumori, H. Taoka, D. Fujiwara, E. P. Schreiner, B. Wolff, M. Yoshida, and S. Horinouchi. 1999. Leptomycin B inactivates CRM1/ exportin 1 by covalent modification at a cysteine residue in the central conserved region. Proc. Natl. Acad. Sci. USA 96:9112-9117.
34. Labelle, Y., J. Bussieres, F. Courjal, and M. B. Goldring. 1999. The EWS/ TEC fusion protein encoded by the t(9;22) chromosomal translocation in human chondrosarcomas is a highly potent transcriptional activator. Oncogene 18:3303-3308.
35. Labelle, Y., J. Zucman, G. Stenman, L. G. Kindblom, J. Knight, C. Turc-Carel, B. Dockhorn-Dworniczak, N. Mandahl, C. Desmaze, M. Peter, et al. 1995. Oncogenic conversion of a novel orphan nuclear receptor by chromosome translocation. Hum. Mol. Genet. 4:2219-2226.
36. Law, S. W., O. M. Conneely, F. J. DeMayo, and B. W. O'Malley. 1992. Identification of a new brain-specific transcription factor, NURR1. Mol. Endocrinol. 6:2129-2135.
37. Lee, J. M., K. H. Lee, M. Weidner, B. A. Osborne, and S. D. Hayward. 2002. Epstein-Barr virus EBNA2 blocks Nur77-mediated apoptosis. Proc. Natl. Acad. Sci. USA 99:11878-11883.
38. Lee, M. S., S. A. Kliewer, J. Provencal, P. E. Wright, and R. M. Evans. 1993. Structure of the retinoid X receptor alpha DNA binding domain: a helix required for homodimeric DNA binding. Science 260:1117-1121.
39. Levin, A. A., L. J. Sturzenbecker, S. Kazmer, T. Bosakowski, C. Huselton, G. Allenby, J. Speck, C. Kratzeisen, M. Rosenberger, A. Lovey, et al. 1992. 9-cis retinoic acid stereoisomer binds and activates the nuclear receptor RXR alpha. Nature 355:359-361.
40. Li, H., S. K. Kolluri, J. Gu, M. I. Dawson, X. Cao, P. D. Hobbs, B. Lin, G. Chen, J. Lu, F. Lin, Z. Xie, J. A. Fontana, J. C. Reed, and X. Zhang. 2000. Cytochrome c release and apoptosis induced by mitochondrial targeting of nuclear orphan receptor TR3. Science 289:1159-1164.
41. Li, Y., B. Lin, A. Agadir, R. Liu, M. I. Dawson, J. C. Reed, J. A. Fontana, F. Bost, P. D. Hobbs, Y. Zheng, G. Q. Chen, B. Shroot, D. Mercola, and X. K. Zhang. 1998. Molecular determinants of AHPN (CD437)-induced growth arrest and apoptosis in human lung cancer cell lines. Mol. Cell. Biol. 18: 4719-4731.
42. Lin, B., G. Q. Chen, D. Xiao, S. K. Kolluri, X. Cao, H. Su, and X. K. Zhang. 2000. Orphan receptor COUP-TF is required for induction of retinoic acid receptor beta, growth inhibition, and apoptosis by retinoic acid in cancer cells. Mol. Cell. Biol. 20:957-970.
43. Lin, B., S. Kolluri, F. Lin, W. Liu, Y. H. Han, X. Cao, M. I. Dawson, J. C. Reed, and X. K. Zhang. 2004. Conversion of Bcl-2 from protector to killer by interaction with nuclear orphan receptor Nur77/TR3. Cell 116:527-540.
44. Liu, Z. G., S. W. Smith, K. A. McLaughlin, L. M. Schwartz, and B. A. Osborne. 1994. Apoptotic signals delivered through the T-cell receptor of a T-cell hybrid require the immediate-early gene nur77. Nature 367:281-284.
45. Mages, H. W., O. Rilke, R. Bravo, G. Senger, and R. A. Kroczek. 1994. NOT, a human immediate-early response gene closely related to the steroid/thyroid hormone receptor NAK1/TR3. Mol. Endocrinol. 8:1583-1591.
46. Mangelsdorf, D. J., and R. M. Evans. 1995. The RXR heterodimers and orphan receptors. Cell 83:841-850.
47. Maruyama, K., T. Tsukada, S. Bandoh, K. Sasaki, N. Ohkura, and K. Yamaguchi. 1995. Expression of NOR-1 and its closely related members of the steroid/thyroid hormone receptor superfamily in human neuroblastoma cell lines. Cancer Lett. 96:117-122.
48. Maruyama, K., T. Tsukada, N. Ohkura, S. Bandoh, T. Hosono, and K. Yamaguchi. 1998. The NGFI-B subfamily of the nuclear receptor superfamily. Int. J. Oncol. 12:1237-1243.
49. Masuyama, N., K. Oishi, Y. Mori, T. Ueno, Y. Takahama, and Y. Gotoh. 2001. Akt inhibits the orphan nuclear receptor Nur77 and T-cell apoptosis. J. Biol. Chem. 276:32799-32805.
50. Migliaccio, A., G. Castoria, M. Di Domenico, A. de Falco, A. Bilancio, M. Lombardi, M. V. Barone, D. Ametrano, M. S. Zannini, C. Abbondanza, and F. Auricchio. 2000. Steroid-induced androgen receptor-oestradiol receptor beta-Src complex triggers prostate cancer cell proliferation. EMBO J. 19: 5406-5417.
51. Milbrandt, J. 1988. Nerve growth factor induces a gene homologous to the glucocorticoid receptor gene. Neuron 1:183-188.
52. Ohkura, N., M. Hijikuro, A. Yamamoto, and K. Miki. 1994. Molecular cloning of a novel thyroid/steroid receptor superfamily gene from cultured rat neuronal cells. Biochem. Biophys. Res. Commun. 205:1959-1965.
53. Pekarsky, Y., C. Hallas, A. Palamarchuk, A. Koval, F. Bullrich, Y. Hirata, R. Bichi, J. Letofsky, and C. M. Croce. 2001. Akt phosphorylates and regulates the orphan nuclear receptor Nur77. Proc. Natl. Acad. Sci. USA 98:3690-3694.
54. 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.
55. Perlmann, T., K. Umesono, P. N. Rangarajan, B. M. Forman, and R. M. Evans. 1996. Two distinct dimerization interfaces differentially modulate target gene specificity of nuclear hormone receptors. Mol. Endocrinol. 10: 958-966.
56. Philips, A., S. Lesage, R. Gingras, M. H. Maira, Y. Gauthier, P. Hugo, and J. Drouin. 1997. Novel dimeric Nur77 signaling mechanism in endocrine and lymphoid cells. Mol. Cell. Biol. 17:5946-5951.
57. Prufer, K., and J. Barsony. 2002. Retinoid X receptor dominates the nuclear import and export of the unliganded vitamin D receptor. Mol. Endocrinol. 16:1738-1751.
58. Prufer, K., A. Racz, G. C. Lin, and J. Barsony. 2000. Dimerization with retinoid X receptors promotes nuclear localization and subnuclear targeting of vitamin D receptors. J. Biol. Chem. 275:41114-41123.
59. Ramaswamy, S., K. N. Ross, E. S. Lander, and T. R. Golub. 2003. A molecular signature of metastasis in primary solid tumors. Nat. Genet. 33:49-54.
60. Rastinejad, F., T. Wagner, Q. Zhao, and S. Khorasanizadeh. 2000. Structure of the RXR-RAR DNA-binding complex on the retinoic acid response element DR1. EMBO J. 19:1045-1054.
61. Sacchetti, P., H. Dwornik, P. Formstecher, C. Rachez, and P. Lefebvre. 2002. Requirements for heterodimerization between the orphan nuclear receptor Nurr1 and retinoid X receptors. J. Biol. Chem. 277:35088-35096.
62. Sakaue, M., H. Adachi, M. Dawson, and A. M. Jetten. 2001. Induction of Egr-1 expression by the retinoid AHPN in human lung carcinoma cells is dependent on activated ERK1/2. Cell Death Differ. 8:411-424.
63. Shipp, M. A., K. N. Ross, P. Tamayo, A. P. Weng, J. L. Kutok, R. C. Aguiar, M. Gaasenbeek, M. Angelo, M. Reich, G. S. Pinkus, T. S. Ray, M. A. Koval, K. W. Last, A. Norton, T. A. Lister, J. Mesirov, D. S. Neuberg, E. S. Lander, J. C. Aster, and T. R. Golub. 2002. Diffuse large B-cell lymphoma outcome prediction by gene-expression profiling and supervised machine learning. Nat. Med. 8:68-74.
64. Simoncini, T., A. Hafezi-Moghadam, D. P. Brazil, K. Ley, W. W. Chin, and J. K. Liao. 2000. Interaction of estrogen receptor with the regulatory subunit of phosphatidylinositol-3-OH kinase. Nature 407:538-541.
65. Szondy, Z., U. Reichert, and L. Fesus. 1998. Retinoic acids regulate apoptosis of T lymphocytes through an interplay between RAR and RXR receptors. Cell Death Differ. 5:4-10.
66. Uemura, H., and C. Chang. 1998. Antisense TR3 orphan receptor can increase prostate cancer cell viability with etoposide treatment. Endocrinology 139:2329-2334.
67. Wang, H. G., U. R. Rapp, and J. C. Reed. 1996. Bcl-2 targets the protein kinase Raf-1 to mitochondria. Cell 87:629-638.
68. Wansa, K. D., J. M. Harris, and G. E. Muscat. 2002. The activation function-1 domain of Nur77/NR4A1 mediates transactivation, cell specificity, and coactivator recruitment. J. Biol. Chem. 277:33001-33011.
69. Weih, F., R. P. Ryseck, L. Chen, and R. Bravo. 1996. Apoptosis of nur77/ N10-transgenic thymocytes involves the Fas/Fas ligand pathway. Proc. Natl. Acad. Sci. USA 93:5533-5538.
70. Wen, W., J. L. Meinkoth, R. Y. Tsien, and S. S. Taylor. 1995. Identification of a signal for rapid export of proteins from the nucleus. Cell 82:463-473.
71. Wilson, A. J., D. Arango, J. M. Mariadason, B. G. Heerdt, and L. H. Augenlicht. 2003. TR3/Nur77 in colon cancer cell apoptosis. Cancer Res. 63:5401-5407.
72. Wilson, T. E., T. J. Fahrner, M. Johnston, and J. Milbrandt. 1991. Identification of the DNA binding site for NGFI-B by genetic selection in yeast. Science 252:1296-1300.
73. Winoto, A., and D. R. Littman. 2002. Nuclear hormone receptors in T lymphocytes. Cell 109(Suppl.):S57-S66.
74. Woronicz, J. D., B. Calnan, V. Ngo, and A. Winoto. 1994. Requirement for the orphan steroid receptor Nur77 in apoptosis of T-cell hybridomas. Nature 367:277-281.
75. Woronicz, J. D., A. Lina, B. J. Calnan, S. Szychowski, L. Cheng, and A. Winoto. 1995. Regulation of the Nur77 orphan steroid receptor in activation-induced apoptosis. Mol. Cell. Biol. 15:6364-6376.
76. Wu, Q., M. I. Dawson, Y. Zheng, P. D. Hobbs, A. Agadir, L. Jong, Y. Li, R. Liu, B. Lin, and X. K. Zhang. 1997. Inhibition of trans-retinoic acid-resistant human breast cancer cell growth by retinoid X receptor-selective retinoids. Mol. Cell. Biol. 17:6598-6608.
77. Wu, Q., Y. Li, R. Liu, A. Agadir, M. O. Lee, Y. Liu, and X. Zhang. 1997. Modulation of retinoic acid sensitivity in lung cancer cells through dynamic balance of orphan receptors nur77 and COUP-TF and their heterodimerization. EMBO J. 16:1656-1669.
78. Wu, Q., S. Liu, X. F. Ye, Z. W. Huang, and W. J. Su. 2002. Dual roles of Nur77 in selective regulation of apoptosis and cell cycle by TPA and ATRA in gastric cancer cells. Carcinogenesis 23:1583-1592.
79. Wu, W. S., Z. X. Xu, R. Ran, F. Meng, and K. S. Chang. 2002. Promyelocytic leukemia protein PML inhibits Nur77-mediated transcription through specific functional interactions. Oncogene 21:3925-3933.
80. 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.
81. Yang, Y., J. Bailey, M. S. Vacchio, R. Yarchoan, and J. D. Ashwell. 1995. Retinoic acid inhibition of ex vivo human immunodeficiency virus-associated apoptosis of peripheral blood cells. Proc. Natl. Acad. Sci. USA 92:3051-3055.
82. Yang, Y., S. Minucci, K. Ozato, R. A. Heyman, and J. D. Ashwell. 1995. Efficient inhibition of activation-induced Fas ligand up-regulation and T-cell apoptosis by retinoids requires occupancy of both retinoid X receptors and retinoic acid receptors. J. Biol. Chem. 270:18672-18677.
83. Yang, Y., M. S. Vacchio, and J. D. Ashwell. 1993. 9-cis-Retinoic acid inhibits activation-driven T-cell apoptosis: implications for retinoid X receptor involvement in thymocyte development. Proc. Natl. Acad. Sci. USA 90:6170-6174.
84. Zamzami, N., and G. Kroemer. 2001. The mitochondrion in apoptosis: how Pandora's box opens. Nat. Rev. Mol. Cell. Biol. 2:67-71.
85. 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.
86. Zhang, X. K. 2002. Vitamin A and apoptosis in prostate cancer. Endocrinol. Relat. Cancer 9:87-102.
87. Zhang, X. K., B. Hoffmann, P. B. Tran, G. Graupner, and M. Pfahl. 1992. Retinoid X receptor is an auxiliary protein for thyroid hormone and retinoic acid receptors. Nature 355:441-446.
88. 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 358:587-591.
89. Zhang, X. K., and M. Pfahl. 1993. Hetero- and homodimeric receptors in thyroid hormone and vitamin A action. Receptor 3:183-191.
90. Zhang, X. K., G. Salbert, M. O. Lee, and M. Pfahl. 1994. Mutations that alter ligand-induced switches and dimerization activities in the retinoid X receptor. Mol. Cell. Biol. 14:4311-4323.
91. Zhang, Y., M. I. Dawson, R. Mohammad, A. K. Rishi, L. Farhana, K. C. Feng, M. Leid, V. Peterson, X. K. Zhang, M. Edelstein, D. Eilander, S. Biggar, N. Wall, U. Reichert, and J. A. Fontana. 2002. Induction of apoptosis of human B-CLL and ALL cells by a novel retinoid and its nonretinoidal analog. Blood 100:2917-2925.
92. Zhu, X. G., J. A. Hanover, G. L. Hager, and S. Y. Cheng. 1998. Hormone-induced translocation of thyroid hormone receptors in living cells visualized using a receptor green fluorescent protein chimera. J. Biol. Chem. 273: 27058-27063.