Subnuclear trafficking of glucocorticoid receptors in vitro: Chromatin recycling and nuclear export

Journal of Cell Biology

Volumn 137, Issue 3, 1997, Pages 523-538

  Yang, Jun ^a   Liu, Jimin ^a   DeFranco, Donald B ^a  

^a UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; CELL NUCLEUS RECEPTOR; GENISTEIN; GLUCOCORTICOID; GLUCOCORTICOID RECEPTOR; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 90; MOLYBDIC ACID; NUCLEAR PROTEIN; PHOSPHOTYROSINE; TYROSINE DERIVATIVE;

ANIMAL CELL; CELL NUCLEUS; CHROMATIN; CHROMATIN STRUCTURE; IMMUNOBLOTTING; LIGAND BINDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PHOSPHORYLATION; PROTEIN TRANSPORT; RAT; REVIEW;

ADENOSINE TRIPHOSPHATE; ANIMALS; BIOLOGICAL TRANSPORT; CELL COMPARTMENTATION; CELL MEMBRANE PERMEABILITY; CELL NUCLEUS; CHROMATIN; CORTICOSTERONE; DIGITONIN; ENZYME INHIBITORS; GENISTEIN; HEPARIN; HSP90 HEAT-SHOCK PROTEINS; ISOFLAVONES; LIVER; LIVER NEOPLASMS, EXPERIMENTAL; MICROCYSTINS; MOLYBDENUM; PEPTIDES, CYCLIC; PHOSPHOTYROSINE; PROTEIN-TYROSINE KINASES; PROTEIN-TYROSINE-PHOSPHATASE; RATS; RECEPTORS, GLUCOCORTICOID; TUMOR CELLS, CULTURED; TUNGSTEN COMPOUNDS; VANADATES;

EID: 0030907634     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.137.3.523     Document Type: Review

References (83)

1. Akey, C.W., and M. Radermacher. 1993. Architecture of the Xenopus nuclear pore complex revealed by three-dimensional cryo-electron microscopy. J. Cell Biol. 122:1-19.
2. Barsony, J., and W. McKoy. 1992. Molybdate increases intracellular 3′, 5′-guanosine cyclic monophosphate and stabilizes vitamin D receptor association with tubulin-containing filaments. J. Biol. Chem. 267:24457-24465.
3. Bodwell, J.E., E. Orti, J.M. Coull, D.J.C. Pappin, D.B. Mendel, L.I. Smith, and F. Swift. 1991. Identification of phosphorylated sites in the mouse glucocorticoid receptor. J. Biol. Chem. 266:7549-7555.
4. Bohen, S.P., and K.R. Yamamoto. 1993. Isolation of hsp90 mutants by screening for decreased steroid receptor function. Proc. Natl. Acad. Sci. USA. 90: 11424-11428.
5. Borer, R.A., C.F. Lehner, H.M. Eppenberger, and E.A. Nigg. 1989. Major nucleolar proteins shuttle between nucleus and cytoplasm. Cell. 56:379-390.
6. Bresnick, E.H., F.C. Dalman, E.R. Sanchez, and W.B. Pratt. 1989. Evidence that the 90-kDa heat shock protein is necessary for the steroid binding conformation of the L cell glucocorticoid receptor. J. Biol. Chem. 264:4992-4997.
7. Chandran, U.R., and D.B. DeFranco. 1992. Internuclear migration of chicken progesterone receptor, but not simian virus-40 large tumor antigen, in transient heterokaryons. Mol. Endocrinol. 6:837-844.
8. Cidlowski, J.A., D.L. Bellingham, F.E. Powell-Oliver, D.B. Lubahn, and M. Sar. 1990. Novel antipeptide antibodies to the human glucocorticoid receptor: recognition of multiple distinct receptor forms in vitro and distinct localization of cytoplasmic and nuclear receptors. Mol. Endocrinol. 4:1427-1437.
9. Corbett, A.H., D.M. Koepp, G. Schlenstedt, M.S. Lee, A.K. Hopper, and P.A. Silver. 1995. Rnalp, a Ran/TC4 GTPase activating protein, is required for nuclear import. J. Cell Biol. 130:1017-1026.
10. Csermely, P., T. Schnaider, and I. Szanto. 1995. Signalling and transport through the nuclear membrane. Biochim. Biophys. Acta. 1241:425-452.
11. Czar, M.J., R.H. Lyons, M.J. Welsh, J. Renoir, and W.B. Pratt. 1995. Evidence that the FK506-binding immunophilin heat shock protein 56 is required for the trafficking of the glucocorticoid receptor from the cytoplasm to the nucleus. Mol. Endocrinol. 9:1549-1560.
12. Dahmer, M.K., P.R. Housley, and W.B. Pratt. 1984. Effects of molybdate and endogenous inhibitors on steroid-receptor inactivation, transformation, and translocation. Annu. Rev. Physiol. 46:67-81.
13. Dauvois, S., R. White, and M.G. Parker. 1993. The antiestrogen ICI 182780 disrupts estrogen receptor nucleocytoplasmic shuttling. J. Cell Sci. 106:1377-1388.
14. DeFranco, D.B., M. Qi, K.C. Borror, M.J. Garabedian, and D.L. Brautigan. 1991. Protein phosphatase types 1 and/or 2A regulate nucleocytoplasmic shuttling of glucocorticoid receptors. Mol. Endocrinol. 5:1215-1228.
15. DeFranco, D.B., A.P. Madan, Y. Tang, U.R. Chandran, N. Xiao, and J. Yang. 1995. Nucleocytoplasmic shuttling of steroid receptors. In Vitamins and Hormones. Vol. 51. G. Litwack, editor. Academic Press, New York. 315-338.
16. Denner, L.A., N.L. Weigel, B.L. Maxwell, W.T. Schrader, and B.W. O'Malley. 1990. Regulation of progesterone receptor-mediated transcription by phosphorylation. Science (Wash. DC). 250:1740-1743.
17. Doye, V., and E.C. Hurt. 1995. Genetic approaches to nuclear pore structure and function. Trends Genet. 11:235-241.
18. Dreyfuss, G., M.J. Matunis, S. Pinol-Roma, and C.G. Burd. 1993. hnRNP proteins and the biogenesis of mRNA. Annu. Rev. Biochem. 62:289-321.
19. Evans, R.M. 1988. The steroid and thyroid hormone receptor superfamily. Science (Wash. DC). 240:889-895.
20. Fantozzi, D.A., A.T. Harootunian, W. Wen, S.S. Taylor, J.R. Feramisco, R.Y. Tsien, and J.L. Menikoth. 1994. Thermostable inhibitor of cAMP-dependent protein kinase enhances the rate of export of the kinase catalytic subunit from the nucleus. J. Biol. Chem. 269:2676-2686.
21. Fischer, U., J. Huber, W.C. Boelens, I.W. Mattaj, and R. Luhrmann. 1995. The HIV-1 Rev activation domain is a nuclear export signal that accesses an export pathway used by specific cellular RNAs. Cell. 82:475-483.
22. Fu, X.-Y. 1992. A transcription factor with SH2 and SH3 domains is directly activated by an interferon α-induced cytoplasmic protein tyrosine kinase. Cell. 70:323-335.
23. Gametchu, B., and R.W. Harrison. 1984. Characterization of a monoclonal antibody to the rat liver glucocorticoid receptor. Endocrinology. 114:274-288.
24. Gasc, J.-M., J.-M. Renoir, F. Delahaye, and E.-E. Baulieu. 1990. Nuclear localization of two steroid receptor-associated proteins, hsp90 and hsp59. Exp. Cell Res. 186:362-367.
25. Gerace, L. 1992. Molecular trafficking across the nuclear pore complex. Curr. Opin. Cell Biol. 4:637-645.
26. Görlich, D., F. Vogel, A.D. Mills, E. Hartmann, and R.A. Laskey. 1995. Distinct functions for the two importin subunits in nuclear protein import. Nature (Lond.). 377:246-248.
27. Guiochon-Mantel, A., H. Loosfelt, P. Lescop, S. Sar, M. Atger, M. Perrot-Applanat, and E. Milgrom. 1989. Mechanisms of nuclear localization of the progesterone receptor: evidence for interactions between monomers. Cell. 57:1147-1154.
28. Guiochon-Mantel, A., P. Lescop, S. Christin-Maitre, H. Loosefelt, M. Perrot-Applanat, and E. Milgrom. 1991. Nucleocytoplasmic shuttling of the progesterone receptor. EMBO (Eur. Mol. Biol. Organ.) J. 10:3851-3859.
29. Guiochon-Mantel, A., K. Delabre, P. Lescop, and E. Milgrom. 1994. Nuclear localization signals also mediate the outward movement of proteins from the nucleus. Proc. Natl. Acad. Sci. USA. 91:7179-7183.
30. Howard, K.J., S.J. Holley, K.R. Yamamoto, and C.W. Distelhorst. 1990. Mapping the HSP90 binding region of the glucocorticoid receptor. J. Biol. Chem. 265:11928-11935.
31. Hurt, E.C. 1996. Importins/karyopherins meet nucleoporins. Cell. 84:509-515.
32. Kadowaki, T., D. Goldfarb, L.M. Spitz, A.M. Tartakoff, and M. Ohno. 1993. Regulation of RNA processing and transport by a nuclear guanine nucleotide release protein and members of the Ras superfamily. EMBO (Eur. Mol. Biol. Organ.) J. 12:2929-2937.
33. Lyderson, B., and D. Pettijohn. 1980. Human-specific nuclear protein that associates with the polar region of the mitotic apparatus: distribution in a human / hamster hybrid cell. Cell. 22:489-499.
34. Madan, A.P., and D.B. DeFranco. 1993. Bidirectional transport of glucocorticoid receptors across the nuclear envelope. Proc. Natl. Acad. Sci. USA. 90: 3588-3592.
35. Mandell, R.B., and C.M. Feldherr. 1990. Identification of two HSP70-related Xenopus oocyte proteins that are capable of recycling across the nuclear envelope. J. Cell Biol. 111:1775-1783.
36. Mangelsdorf, D.J., C. Thummel, M. Beato, P. Herrlich, G. Schütz, K. Umesono, B. Blumberg, P. Kastner, M. Mark, P. Chambon, and R.M. Evans. 1995. The nuclear receptor superfamily: the second decade. Cell. 83:835-840.
37. Mani, S.K., J.M. Allen, J.H. Clark, J.D. Blaustein, and B.W. O'Malley. 1994. Convergent pathways for steroid hormone- and neurotransmitter-induced rat sexual behavior. Science (Wash. DC). 265:1246-1249.
38. Melchior, F., B. Paschal, J. Evans, and L. Gerace. 1993. Inhibition of nuclear protein import by nonhydrolyzable analogues of GTP and identification of the small GTPase Ran/TC4 as an essential nuclear factor. J. Cell Biol. 123: 1649-1659.
39. Meyer, B.E., and M.H. Malim. 1994. The HIV-1 Rev trans-activator shuttles between the nucleus and the cytoplasm. Genes & Dev. 8:1538-1547.
40. Michael, W.M., M. Choi, and G. Dreyfuss. 1995. A nuclear export signal in hnRNP A1: a signal-mediated, temperature-dependent nuclear protein export pathway. Cell. 83:415-422.
41. Mishra, K., and V.K. Parnaik. 1995. Essential role of protein phosphorylation in nuclear transport. Exp. Cell Res. 216:124-134.
42. Modarress, K.J., A.H. Cavanaugh, P.K. Chakraborti, and S.S.J. Simons. 1994. Metal oxyanion stabilization of the rat glucocorticoid receptor is independent of thiols. J. Biol. Chem. 269:25621-25628.
43. Moore, M.S., and G. Blobel. 1993. The GTP-binding protein Ran/TC4 is required for protein import into the nucleus. Nature (Lond.). 365:661-663.
44. Moore, M.S., and G. Blobel. 1994. Purification of a Ran-interacting protein that is required for protein import into the nucleus. Proc. Natl. Acad. Sci. USA. 91:10212-10216.
45. Moroianu, J., and G. Blobel. 1995. Protein export from the nucleus requires the GTPase Ran and GTP hydrolysis. Proc. Natl. Acad. Sci. USA. 92:4318-4322.
46. 2 subunit binds nuclear localization signal and β subunit interacts with peptide repeat-containing nucleoporins. Proc. Natl. Acad. Sci. USA. 92:6532-6536.
47. Munck, A., and T. Brinck-Johnsen. 1968. Specific and nonspecific physicochemical interactions of glucocorticoids and related steroids with rat thymus cells in vitro. J. Biol. Chem. 243:5556-5565.
48. Munck, A., and R. Foley. 1976. Kinetics of glucocorticoid-receptor complexes in rat thymus cells. J. Steroid Biochem. 7:1117-1122.
49. Mymryk, J.S., and T.K. Archer. 1995. Influence of hormone antagonists on chromatin remodeling and transcription factor binding to the mouse mammary tumor virus promoter in vivo. Mol. Endocrinol. 9:1825-1834.
50. Nehrbass, U., and G. Blobel. 1996. Role of the nuclear transport factor p10 in nuclear import. Science (Wash. DC). 272:120-122.
51. Newmeyer, D.D. 1993. The nuclear pore complex and nucleocytoplasmic transport. Curr. Opin. Cell Biol. 5:395-407.
52. Nigg, E.A., P.A. Baeuerle, and R. Lührmann. 1991. Nuclear import-export: in search of signals and mechanisms. Cell. 66:15-22.
53. Orti, E., D.B. Mendel, L.I. Smith, J.E. Bodwell, and A. Munck. 1989. A dynamic model of glucocorticoid receptor phosphorylation and recycling in intact cells. J. Steroid Biochem. 34:85-96.
54. Picard, D., and K.R. Yamamoto. 1987. Two signals mediate hormone-dependent nuclear localization of the glucocorticoid receptor. EMBO (Eur. Mol. Biol. Organ.) J. 6:3333-3340.
55. Picard, D., B. Khursheed, M.J. Garabedian, M.G. Fortin, S. Lindquist, and K.R. Yamamoto. 1990a. Reduced levels of hsp90 compromise steroid action in vivo. Nature (Lond.). 348:166-168.
56. Picard, D., V. Kumar, P. Chambon, and K.R. Yamamoto. 1990b. Signal transduction by steroid hormones: nuclear localization is differentially regulated in estrogen and progesterone receptors. Cell Regul. 1:291-299.
57. Pinol-Roma, S., and G. Dreyfuss. 1992. Shuttling of pre-mRNA binding proteins between nucleus and cytoplasm. Nature (Lond.). 355:730-732.
58. Power, R.F., C.K. Mani, J. Codina, O.M. Connelly, and B.W. O'Malley. 1991. Dopaminergic and ligand-independent activation of steroid hormone receptors. Science (Wash. DC). 254:1636-1639.
59. Pratt, W.B. 1987. Transformation of glucocorticoid and progesterone receptors to the DNA-binding state. J. Cell. Biochem. 35:51-68.
60. Pratt, W.B. 1993. The role of heat shock proteins in regulating the function, folding, and trafficking of the glucocorticoid receptor. J. Biol. Chem. 268: 21455-21458.
61. Qi, M., B.J. Hamilton, and D. DeFranco. 1989. v-mos oncoproteins affect the nuclear retention and reutilization of glucocorticoid receptors. Mol. Endocrinol. 3:1279-1288.
62. Reik, A., G. Schütz, and A.F. Stewart. 1991. Glucocorticoids are required for establishment and maintenance of an alteration in chromatin structure: induction leads to a reversible disruption of nucleosomes over an enhancer. EMBO (Eur. Mol. Biol. Organ.) J. 10:2569-2576.
63. Rexach, M., and G. Blobel. 1995. Protein import into nuclei: association and dissociation reactions involving transport substrate, transport factors, and nucleoporins. Cell. 83:683-692.
64. Rihs, H.-P., and R. Peters. 1989. Nuclear transport kinetics depend on phosphorylation-site-containing sequences flanking the karyophilic signal of the simian virus 40 T-antigen. EMBO (Eur. Mol. Biol. Organ.) J. 8:1479-1484.
65. Rihs, H.-P., D.A. Jans, H. Fan, and R. Peters. 1991. The rate of nuclear cytoplasmic protein transport is determined by the casein kinase II site flanking the nuclear localization sequence of the SV40 T-antigen. EMBO (Eur. Mol. Biol. Organ.) J. 10:633-639.
66. Rossini, G.P. 1987. Molybdate inhibits glucocorticoid-receptor complex binding to RNA. Mol. Cell. Endocrinol. 49:129-135.
67. Rush, M.G., G. Drivas, and P. D'Eustachio. 1996. The small nuclear GTPase Ran: how much does it run? Bioessays. 18:103-112.
68. Sackey, F.N.A., R.J.G. Hache, T. Reich, J. Kwast-Welfeld, and Y.A. Lefebvre. 1996. Determinants of subcellular distribution of the glucocorticoid receptor. Mol. Endocrinol. 10:1191-1205.
69. + RNA in the cytoplasm. Proc. Natl. Acad. Sci. USA. 92:225-229.
70. Schmidt-Zachmann, M.S., C. Dargemont, L.C. Kuhn, and E.A. Nigg. 1993. Nuclear export of proteins: the role of nuclear retention. Cell. 74:493-504.
71. Shuai, K., G.R. Stark, I.M. Kerr, and J.E.J. Darnell. 1993. A single phosphotyrosine residue of Stat91 required for gene activation by interferon-γ. Science (Wash. DC). 261:1744-1746.
72. Somers, J.P., and D.B. DeFranco. 1992. Effects of okadaic acid, a protein phosphatase inhibitor, on glucocorticoid receptor mediated enhancement. Mol. Endocrinol. 6:26-34.
73. Tachibana, T., N. Imamoto, H. Seino, T. Nishimoto, and Y. Yoneda. 1994. Loss of RCC1 leads to suppression of nuclear protein import in living cells. J. Biol. Chem. 269:24542-24545.
74. Tang, Y., and D.B. DeFranco. 1996. ATP-dependent release of glucocorticoid receptors from the nuclear matrix. Mol. Cell. Biol. 16:1989-2001.
75. Tsai, M.-J., and B.W. O'Malley. 1994. Molecular mechanisms of action of steroid/thyroid receptor superfamily members. Annu. Rev. Biochem. 63: 451-486.
76. Welshons, W., M.E. Lieberman, and J. Gorski. 1984. Nuclear localization of unoccupied estrogen receptors: cytochalasin enucleation of GH3 cells. Nature (Lond.). 307:747-749.
77. 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.
78. Wikström, A.-C., O. Bakke, S. Okret, M. Bronnegard, and J.-A. Gustafsson. 1987. Intracellular localization of the glucocorticoid receptor: evidence for cytoplasmic and nuclear localization. Endocrinology. 120:1232-1242.
79. Yamamoto, K.R. 1985. Steroid receptor regulated transcription of genes and gene networks. Annu. Rev. Genet. 19:209-252.
80. Yamamoto, K.R., and B.M. Alberts. 1976. Steroid receptors: elements for modulation of eukaryotic transcription. Annu. Rev. Biochem. 45:721-746.
81. Yang, J., and D.B. DeFranco. 1994. Differential roles of heat shock protein 70 the in vitro nuclear import of glucocorticoid receptor and simian virus 40 large tumor antigen. Mol. Cell. Biol. 14:5088-5098.
82. Yang, J., and D.B. DeFranco. 1996. Assessment of glucocorticoid receptor-heat shock protein 90 interactions in vivo during nucleocytoplasmic trafficking. Mol. Endocrinol. 10:3-13.
83. Zhang, Y., W. Bai, W.E. Allgood, and N.L. Weigel. 1994. Multiple signaling pathways activate the chicken progesterone receptor. Mol. Endocrinol. 8: 577-584.