Mechanisms of receptor-mediated nuclear import and nuclear export

Traffic

Volumn 6, Issue 3, 2005, Pages 187-198

  Pemberton, Lucy F ^a,b   Paschal, Bryce M ^a,b  

^a UNIVERSITY OF VIRGINIA   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

Author keywords

Exportin; Importin; Karyopherin; Nuclear export signal; Nuclear localization signal; Nucleoporin; RanGTP; Steroid hormone receptor

Indexed keywords

GUANOSINE TRIPHOSPHATASE; KARYOPHERIN; MESSENGER RNA; RAN PROTEIN; RAS PROTEIN; STEROID RECEPTOR;

EUKARYOTE; HUMAN; MOLECULAR RECOGNITION; NONHUMAN; NUCLEAR IMPORT; NUCLEAR LOCALIZATION SIGNAL; NUCLEAR PORE COMPLEX; NUCLEOCYTOPLASMIC TRANSPORT; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEIN TRANSPORT; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; CELL NUCLEUS; HUMANS; KARYOPHERINS; NEOPLASM PROTEINS; NUCLEAR LOCALIZATION SIGNALS; NUCLEAR PORE; NUCLEAR PORE COMPLEX PROTEINS; PROTEIN TRANSPORT; RAN GTP-BINDING PROTEIN; RECEPTORS, STEROID; RNA TRANSPORT; SIGNAL TRANSDUCTION;

EID: 14544299215     PISSN: 13989219     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1600-0854.2005.00270.x     Document Type: Review

References (124)

1. Mosammaparast N, Pemberton LF. Karyopherins: from nuclear-transport mediators to nuclear-function regulators. Trends Cell Biol 2004;14:547-556.
2. Fried H, Kutay U. Nucleocytoplasmic transport: taking an inventory. Cell Mol Life Sci 2003;60:1659-1688.
3. Weis K. Regulating access to the genome: nucleocytoplasmic transport throughout the cell cycle. Cell 2003;112:441-451.
4. Goldfarb DS, Corbett AH, Mason DA, Harreman MT, Adam SA. Importin alpha: a multipurpose nuclear-transport receptor. Trends Cell Biol 2004;14:505-514.
5. Gorlich D, Kutay U. Transport between the cell nucleus and the cytoplasm. Annu Rev Cell Dev Biol 1999;15:607-660.
6. Kaffman A, O'Shea EK. Regulation of nuclear localization: a key to a door. Annu Rev Cell Dev Biol 1999;15:291-339.
7. Harreman MT, Kline TM, Milford HG, Harben MB, Hodel AE, Corbett AH. Regulation of nuclear import by phosphorylation adjacent to nuclear localization signals. J Biol Chem 2004;279:20613-20621.
8. Poon IKH, Jans DA. Regulation of nuclear transport: central role in development and transformation. Traffic 2005;6:173-186.
9. Conti E, Uy M, Leighton L, Blobel G, Kuriyan J. Crystallographic analysis of the recognition of a nuclear localization signal by the nuclear import factor karyopherin alpha. Cell 1998;94:193-204.
10. Kobe B. Autoinhibition by an internal nuclear localization signal revealed by the crystal structure of mammalian importin alpha. Nat Struct Biol 1999;6:388-397.
11. Peifer M, Berg S, Reynolds AB. A repeating amino acid motif shared by proteins with diverse cellular roles. Cell 1994;76:789-791.
12. Conti E, Kuriyan J. Crystallographic analysis of the specific yet versatile recognition of distinct nuclear localization signals by karyopherin alpha. Structure Fold Des 2000;8:329-338.
13. Fontes MR, Teh T, Kobe B. Structural basis of recognition of monopartite and bipartite nuclear localization sequences by mammalian importin-alpha. J Mol Biol 2000;297:1183-1194.
14. Fontes MR, Teh T, Jans D, Brinkworth RI, Kobe B. Structural basis for the specificity of bipartite nuclear localization sequence binding by importin-alpha. J Biol Chem 2003;278:27981-27987.
15. Mosammaparast N, Jackson KR, Guo Y, Brame CJ, Shabanowitz J, Hunt DF, Pemberton LF. Nuclear import of histone H2A and H2B is mediated by a network of karyopherins. J Cell Biol 2001;153:251-262.
16. Mosammaparast N, Ewart CS, Pemberton LF. A role for nucleosome assembly protein 1 in the nuclear transport of histones H2A and H2B. EMBO J 2002;21:6527-6538.
17. Muhlhausser P, Muller EC, Otto A, Kutay U. Multiple pathways contribute to nuclear import of core histones. EMBO Rep 2001;2:690-696.
18. Jakel S, Gorlich D. Importin beta, transportin, RanBP5 and RanBP7 mediate nuclear import of ribosomal proteins in mammalian cells. EMBO J 1998;17:4491-4502.
19. Senger B, Simos G, Bischoff FR, Podtelejnikov A, Mann M, Hurt E. Mtr10p functions as a nuclear import receptor for the mRNA-binding protein Npl3p. EMBO J 1998;17:2196-2207.
20. Leslie DM, Zhang W, Timney BL, Chait BT, Rout MP, Wozniak RW, Aitchison JD. Characterization of karyopherin cargoes reveals unique mechanisms of Kap121p-mediated nuclear import. Mol Cell Biol 2004;24:8487-8503.
21. Pollard VW, Michael WM, Nakielny S, Siomi MC, Wang F, Dreyfuss G. A novel receptor-mediated nuclear protein import pathway. Cell 1996;86:985-994.
22. Rosenblum JS, Pemberton LF, Bonifaci N, Blobel G. Nuclear import and the evolution of a multifunctional RNA-binding protein. J Cell Biol 1998;143:887-899.
23. Fischer U, Huber J, Boelens WC, Mattaj IW, Luhrmann R. The HIV-1 Rev activation domain is a nuclear export signal that accesses an export pathway used by specific cellular RNAs. Cell 1995;82: 475-483.
24. Fornerod M, Ohno M, Yoshida M, Mattaj IW. CRM1 is an export receptor for leucine-rich nuclear export signals. Cell 1997;90: 1051-1060.
25. Stade K, Ford CS, Guthrie C, Weis K. Exportin 1 (Crm1) is an essential nuclear export factor. Cell 1997;90:1041-1050.
26. la Cour T, Gupta R, Rapacki K, Skriver K, Poulsen FM, Brunak S. NESbase, version 1.0: a database of nuclear export signals. Nucleic Acids Res 2003;31:393-396.
27. Wen W, Meinkoth JL, Tsien RY, Taylor SS. Identification of a signal for rapid export of proteins from the nucleus. Cell 1995;82:463-473.
28. Paraskeva E, Izaurralde E, Bischoff FR, Huber J, Kutay U, Hartmann E, Luhrmann R, Gorlich D. CRM1-mediated recycling of snurportin 1 to the cytoplasm. J Cell Biol 1999;145:255-264.
29. Ohno M, Segref A, Bachi A, Wilm M, Mattaj IW. PHAX, a mediator of U snRNA nuclear export whose activity is regulated by phosphorylation. Cell 2000;101:187-198.
30. Johnson AW, Lund E, Dahlberg J. Nuclear export of ribosomal subunits. Trends Biochem Sci 2002;27:580-585.
31. Kaffman A, Rank NM, O'Neill EM, Huang LS, O'Shea EK. The receptor Msn5 exports the phosphorylated transcription factor Pho4 out of the nucleus. Nature 1998;396:482-486.
32. Yoshida K, Blobel G. The karyopherin Kap142p/Msn5p mediates nuclear import and nuclear export of different cargo proteins. J Cell Biol 2001;152:729-740.
33. Kutay U, Bischoff FR, Kostka S, Kraft R, Görlich D. Export of importin α from the nucleus is mediated by a specific nuclear transport factor. Cell 1997;90:1061-1071.
34. Lei EP, Silver PA. Protein and RNA export from the nucleus. Dev Cell 2002;2:261-272.
35. Kutay U, Lipowsky G, Izaurralde E, Bischoff FR, Schwarzmaier P, Hartmann E, Gorlich D. Identification of a tRNA-specific nuclear export receptor. Mol Cell 1998;1:359-369.
36. Arts GJ, Kuersten S, Romby P, Ehresmann B, Mattaj IW. The role of exportin-t in selective nuclear export of mature tRNAs. EMBO J 1998;17:7430-7441.
37. Kim VN. MicroRNA precursors in motion: exportin-5 mediates their nuclear export. Trends Cell Biol 2004;14:156-159.
38. Zeng Y, Cullen BR. Structural requirements for pre-microRNA binding and nuclear export by exportin 5. Nucleic Acids Res 2004;32: 4776-4785.
39. Chook YM, Blobel G. Karyopherins and nuclear import. Curr Opin Struct Biol 2001;11:703-715.
40. Conti E. Structures of importins. Results Probl Cell Differ 2002;35: 93-113.
41. Petosa C, Schoehn G, Askjaer P, Bauer U, Moulin M, Steuerwald U, Soler-Lopez M, Baudin F, Mattaj IW, Muller CW. Architecture of CRM1/Exportin1 suggests how cooperativity is achieved during formation of a nuclear export complex. Mol Cell 2004;16:761-775.
42. Matsuura Y, Stewart M. Structural basis for the assembly of a nuclear export complex. Nature 2004;432:872-877.
43. Cingolani G, Petosa C, Weis K, Muller CW. Structure of importin-beta bound to the IBB domain of importin-alpha. Nature 1999;399:221-229.
44. Cingolani G, Bednenko J, Gillespie MT, Gerace L. Molecular basis for the recognition of a nonclassical nuclear localization signal by importin beta. Mol Cell 2002;10:1345-1353.
45. Lee SJ, Sekimoto T, Yamashita E, Nagoshi E, Nakagawa A, Imamoto N, Yoshimura M, Sakai H, Chong KT, Tsukihara T, Yoneda Y. The structure of importin-beta bound to SREBP-2: nuclear import of a transcription factor. Science 2003;302:1571-1575.
46. Bayliss R, Littlewood T, Stewart M. Structural basis for the interaction between FxFG nucleoporin repeats and importin-beta in nuclear trafficking. Cell 2000;102:99-108.
47. Vetter IR, Arndt A, Kutay U, Gorlich D, Wittinghofer A. Structural view of the Ran-importin beta interaction at 2.3A resolution. Cell 1999;97:635-646.
48. Chook YM, Blobel G. Structure of the nuclear transport complex karyopherin-beta2-Ran x GppNHp. Nature 1999;399:230-237.
49. Andrade MA, Bork P. HEAT repeats in the Huntington's disease protein. Nat Genet 1995;11:115-116.
50. Fukuhara N, Fernandez E, Ebert J, Conti E, Svergun D. Conformational variability of nucleo-cytoplasmic transport factors. J Biol Chem 2004;279:2176-2181.
51. Chook YM, Jung A, Rosen MK, Blobel G. Uncoupling Kapbeta2 substrate dissociation and ran binding. Biochemistry 2002;41: 6955-6966.
52. Suntharalingam M, Wente SR. Peering through the pore: nuclear pore complex structure, assembly, and function. Dev Cell 2003;4: 775-789.
53. Rout MP, Aitchison JD, Suprapto A, Hjertaas K, Zhao Y, Chait BT. The yeast nuclear pore complex: composition, architecture, and transport mechanism. J Cell Biol 2000;148:635-651.
54. Cronshaw JM, Krutchinsky AN, Zhang W, Chait BT, Matunis MJ. Proteomic analysis of the mammalian nuclear pore complex. J Cell Biol 2002;158:915-927.
55. Weirich CS, Erzberger JP, Berger JM, Weis K. The N-terminal domain of Nup159 forms a beta-propeller that functions in mRNA export by tethering the helicase dbp5 to the nuclear pore. Mol Cell 2004;16:749-760.
56. Devos D, Dokudovskaya S, Alber F, Williams R, Chait BT, Sali A, Rout MP. Components of coated vesicles and nuclear pore complexes share a common molecular architecture. PLoS Biol 2004;2:e380.
57. Strawn LA, Shen T, Shulga N, Goldfarb DS, Wente SR. Minimal nuclear pore complexes define FG repeat domains essential for transport. Nat Cell Biol 2004;6:197-206.
58. Bednenko J, Cingolani G, Gerace L. Importin beta contains a COOH-terminal nucleoporin binding region important for nuclear transport. J Cell Biol 2003;162:391-401.
59. Makhnevych T, Lusk CP, Anderson AM, Aitchison JD, Wozniak RW. Cell cycle regulated transport controlled by alterations in the nuclear pore complex. Cell 2003;115:813-823.
60. Ben-Efraim I, Gerace L. Gradient of increasing affinity of importin beta for nucleoporins along the pathway of nuclear import. J Cell Biol 2001;152:411-417.
61. Pyhtila B, Rexach M. A gradient of affinity for the karyopherin Kap95p along the yeast nuclear pore complex. J Biol Chem 2003;278: 42699-42709.
62. Shah S, Tugendreich S, Forbes D. Major binding sites for the nuclear import receptor are the internal nucleoporin Nup153 and the adjacent nuclear filament protein Tpr. J Cell Biol 1998;141:31-49.
63. Zeitler B, Weis K. The FG-repeat asymmetry of the nuclear pore complex is dispensable for bulk nucleocytoplasmic transport in vivo. J Cell Biol 2004;167:583-590.
64. Smith AE, Slepchenko BM, Schaff JC, Loew LM, Macara IG. Systems analysis of Ran transport. Science 2002;295:488-491.
65. Gorlich D, Seewald MJ, Ribbeck K. Characterization of Ran-driven cargo transport and the RanGTPase system by kinetic measurements and computer simulation. EMBO J 2003;22:1088-1100.
66. Moore MS, Blobel G. Purification of a Ran-interacting protein that is required for protein import into the nucleus. Proc Natl Acad Sci USA 1994;91:10212-10216.
67. Paschal BM, Gerace L. Identification of NTF2, a cytosolic factor for nuclear import that interacts with nuclear pore complex protein p62. J Cell Biol 1995;129:925-937.
68. Smith A, Brownawell A, Macara IG. Nuclear import of Ran is mediated by the transport factor NTF2. Curr Biol 1998;8:1403-1406.
69. Ribbeck K, Lipowsky G, Kent HM, Stewart M, Gorlich D. NTF2 mediates nuclear import of Ran. EMBO J 1998;17:6587-6598.
70. Bayliss R, Leung SW, Baker RP, Quimby BB, Corbett AH, Stewart M. Structural basis for the interaction between NTF2 and nucleoporin FxFG repeats. EMBO J 2002;21:2843-2853.
71. Stewart M, Kent HM, McCoy AJ. Structural basis for molecular recognition between nuclear transport factor 2 (NTF2) and the GDP-bound form of the Ras-family GTPase Ran. J Mol Biol 1998;277:635-646.
72. Oki M, Nishimoto T. A protein required for nuclear-protein import, Mog1p, directly interacts with GTP-Gsp1p, the Saccharomyces cerevisiae Ran homologue. Proc Natl Acad Sci USA 1998;95:15388-15393.
73. Oki M, Nishimoto T. Yrb1p interaction with the gsp1p C terminus blocks Mog1p stimulation of GTP release from Gsp1p. J Biol Chem 2000;275:32894-32900.
74. Steggerda SM, Paschal BM. The mammalian Mog1 protein is a guanine nucleotide release factor for Ran. J Biol Chem 2000;275:23175-23180.
75. Ohtsubo M, Kai R, Furuno N, Sekiguchi T, Sekiguchi M, Hayashida M, Kuma K, Miyata T, Fuukushige S, Murotsu T, Matsubara K, Nishimoto T. Isolation and characterization of the active cDNA of the human cell cycle gene (RCC1) involved in the regulation of onset of chromosome condensation. Genes Dev 1987;1:585-593.
76. Bischoff FR, Ponstingl H. Catalysis of guanine nucleotide exchange on Ran by the mitotic regulator RCC1. Nature 1991;354:80-82.
77. Nemergut ME, Mizzen CA, Stukenberg T, Allis CD, Macara IG. Chromatin docking and exchange activity enhancement of RCC1 by histones H2A and H2B. Science 2001;292:1540-1543.
78. Renault L, Kuhlmann J, Henkel A, Wittinghofer A. Structural basis for guanine nucleotide exchange on Ran by the regulator of chromosome condensation (RCC1). Cell 2001;105:245-255.
79. Li HY, Wirtz D, Zheng Y. A mechanism of coupling RCC1 mobility to RanGTP production on the chromatin in vivo. J Cell Biol 2003;160: 635-644.
80. Li HY, Zheng Y. Phosphorylation of RCC1 in mitosis is essential for producing a high RanGTP concentration on chromosomes and for spindle assembly in mammalian cells. Genes Dev 2004;18:512-527.
81. Kalab P, Weis K, Heald R. Visualization of a Ran-GTP gradient in interphase and mitotic Xenopus egg extracts. Science 2002;295: 2452-2456.
82. Harel A, Forbes DJ. Importin Beta; conducting a much larger cellular symphony. Mol Cell 2004;16:319-330.
83. Bischoff FR, Klebe C, Kretschmer J, Wittinghofer A, Ponstingl H. RanGAP1 induces GTPase activity of nuclear Ras-related Ran. Proc Natl Acad Sci USA 1994;91:2587-2591.
84. Bischoff FR, Krebber H, Smirnova E, Dong W, Ponstingl H. Co-activation of RanGTPase and inhibition of GTP dissociation by Ran-GTP binding protein RanBP1. EMBO J 1995;14:705-715.
85. Izaurralde E, Kutay U, von Kobbe C, Mattaj IW, Gorlich D. The asymmetric distribution of the constituents of the Ran system is essential for transport into and out of the nucleus. EMBO J 1997;16:6535-6547.
86. Nemergut ME, Macara IG. Nuclear import of the ran exchange factor, RCC1, is mediated by at least two distinct mechanisms. J Cell Biol 2000;149:835-850.
87. Talcott B, Moore MS. The nuclear import of RCC1 requires a specific nuclear localization sequence receptor, karyopherin alpha3/Qip. J Biol Chem 2000;275:10099-10104.
88. Matunis MJ, Coutavas E, Blobel G. A novel ubiquitin-like modification modulates the partitioning of the Ran-GTPase-activating protein RanGAP1 between the cytosol and the nuclear pore complex. J Cell Biol 1996;135:1457-1470.
89. Mahajan R, Delphin C, Guan T, Gerace L, Melchior F. A small ubiquitin-related polypeptide involved in targeting RanGAP1 to nuclear pore complex protein RanBP2. Cell 1997;88:97-107.
90. Wu J, Matunis MJ, Kraemer D, Blobel G, Coutavas E. Nup358, a cytoplasmically exposed nucleoporin with peptide repeats, Ran-GTP binding sites, zinc fingers, a cyclophilin A homologous domain, and a leucine-rich region. J Biol Chem 1995;270:14209-14213.
91. Yokoyama N, Hayashi N, Seki T, Pante N, Ohba T, Nishii K, Kuma K, Hayashida T, Miyata T, Aebi U et al. A giant nucleopore protein that binds Ran/TC4. Nature 1995;376:184-188.
92. Lindsay ME, Plafker K, Smith AE, Clurman BE, Macara IG. Npap60/Nup50 is a tri-stable switch that stimulates importin-alpha: beta-mediated nuclear protein import. Cell 2002;110:349-360.
93. Lindsay ME, Holaska JM, Welch K, Paschal BM, Macara IG. Ran-binding protein 3 is a cofactor for Crm1-mediated nuclear protein export. J Cell Biol 2001;153:1391-1402.
94. McKenna NJ, O'Malley BW. Combinatorial control of gene expression by nuclear receptors and coregulators. Cell 2002;108:465-474.
95. DeFranco DB. Navigating steroid hormone receptors through the nuclear compartment. Mol Endocrinol 2002;16:1449-1455.
96. Shank LC, Paschal BM. Nuclear transport of steroid hormone receptors. Crit Rev Eukaryot Gene Expr 2005; in press.
97. Picard D, Yamamoto KR. Two signals mediate hormone-dependent nuclear localization of the glucocorticoid receptor. EMBO J 1987;6:3333-3340.
98. Zhou ZX, Sar M, Simental JA, Lane MV, Wilson EM. A ligand-dependent bipartite nuclear targeting signal in the human androgen receptor. Requirement for the DNA-binding domain and modulation by NH2-terminal and carboxyl-terminal sequences. J Biol Chem 1994;269:13115-13123.
99. Simental JA, Sar M, Lane MV, French FS, Wilson EM. Transcriptional activation and nuclear targeting signals of the human androgen receptor. J Biol Chem 1991;266:510-518.
100. Ylikomi T, Bocquel MT, Berry M, Gronemeyer H, Chambon P. Cooperation of proto-signals for nuclear accumulation of estrogen and progesterone receptors. EMBO J 1992;11:3681-3694.
101. Picard D, Kumar V, Chambon P, Yamamoto KR. Signal transduction by steroid hormones: nuclear localization is differentially regulated in estrogen and glucocorticoid receptors. Cell Regul 1990;1:291-299.
102. Savory JG, Hsu B, Laquian IR, Giffin W, Reich T, Hache RJ, Lefebvre YA. Discrimination between NL1- and NL2-mediated nuclear localization of the glucocorticoid receptor. Mol Cell Biol 1999;19:1025-1037.
103. Poukka H, Karvonen U, Yoshikawa N, Tanaka H, Palvimo JJ, Janne OA. The RING finger protein SNURF modulates nuclear trafficking of the androgen receptor. J Cell Sci 2000;113:2991-3001.
104. Freedman ND, Yamamoto KR. Importin 7 and importin {alpha}/importin {beta} are nuclear import receptors for the glucocorticoid receptor. Mol Biol Cell 2004;15:2276-2286.
105. Pratt WB, Toft DO. Steroid receptor interactions with heat shock protein and immunophilin chaperones. Endocr Rev 1997;18:306-360.
106. Davies TH, Ning YM, Sanchez ER. A new first step in activation of steroid receptors: hormone-induced switching of FKBP51 and FKBP52 immunophilins. J Biol Chem 2002;277:4597-4600.
107. Black BE, Holaska JM, Rastinejad F, Paschal BM. DNA binding domains in diverse nuclear receptors function as nuclear export signals. Curr Biol 2001;11:1749-1758.
108. Saporita AJ, Zhang Q, Navai N, Dincer Z, Hahn J, Cai X, Wang Z. Identification and characterization of a ligand-regulated nuclear export signal in androgen receptor. J Biol Chem 2003;278: 41998-42005.
109. Katagiri Y, Takeda K, Yu ZX, Ferrans VJ, Ozato K, Guroff G. Modulation of retinoid signalling through NGF-induced nuclear export of NGFI-B. Nat Cell Biol 2000;2:435-440.
110. Liu J, DeFranco DB. Protracted nuclear export of glucocorticoid receptor limits its turnover and does not require the exportin 1/CRM1-directed nuclear export pathway. Mol Endocrinol 2000;14:40-51.
111. Itoh M, Adachi M, Yasui H, Takekawa M, Tanaka H, Imai K. Nuclear export of glucocorticoid receptor is enhanced by c-Jun N-terminal kinase-mediated phosphorylation. Mol Endocrinol 2002;16:2382-2392.
112. Yang J, Liu J, DeFranco DB. Subnuclear trafficking of glucocorticoid receptors in vitro: chromatin recycling and nuclear export. J Cell Biol 1997;137:523-538.
113. Stade K, Ford CS, Guthrie C, Weis K. Exportin 1 (Crm1p) is an essential nuclear export factor. Cell 1997;90:1041-1050.
114. Kino T, Souvatzoglou E, De Martino MU, Tsopanomihalu M, Wan Y, Chrousos GP. Protein 14-3-3sigma interacts with and favors cytoplasmic subcellular localization of the glucocorticoid receptor, acting as a negative regulator of the glucocorticoid signaling pathway. J Biol Chem 2003;278:25651-25656.
115. Amazit L, Alj Y, Tyagi RK, Chauchereau A, Loosfelt H, Pichon C, Pantel J, Foulon-Guinchard E, Leclerc P, Milgrom E, Guiochon-Mantel A. Subcellular localization and mechanisms of nucleocytoplasmic trafficking of steroid receptor coactivator-1. J Biol Chem 2003;278:32195-32203.
116. Prufer K, Barsony J. Retinoid X receptor dominates the nuclear import and export of the unliganded vitamin D receptor. Mol Endocrinol 2002;16:1738-1751.
117. Holaska JM, Black BE, Love DC, Hanover JA, Leszyk J, Paschal BM. Calreticulin is a receptor for nuclear export. J Cell Biol 2001;152:127-140.
118. Walther RF, Lamprecht C, Ridsdale A, Groulx I, Lee S, Lefebvre YA, Hache RJ. Nuclear export of the glucocorticoid receptor is accelerated by cell fusion-dependent release of calreticulin. J Biol Chem 2003;278:37858-37864.
119. Ji JY, Jing H, Diamond SL. Shear stress causes nuclear localization of endothelial glucocorticoid receptor and expression from the GRE promoter. Circ Res 2003;92:279-285.
120. Qiu M, Olsen A, Faivre E, Horwitz KB, Lange CA. Mitogen-activated protein kinase regulates nuclear association of human progesterone receptors. Mol Endocrinol 2003;17:628-642.
121. Cronshaw JM, Matunis MJ. The nuclear pore complex: disease associations and functional correlations. Trends Endocrinol Metab 2004;15:34-39.
122. Black BE, Paschal BM. Intranuclear organization and function of the androgen receptor. Trends Endocrinol Metab 2004;15: 411-417.
123. Zhang L, Johnson M, Le KH, Sato M, Ilagan R, Iyer M, Gambhir SS, Wu L, Carey M. Interrogating androgen receptor function in recurrent prostate cancer. Cancer Res 2003;63:4552-4560.
124. Gioeli D, Mandell JW, Petroni GR, Frierson HF Jr, Weber MJ. Activation of mitogen-activated protein kinase associated with prostate cancer progression. Cancer Res 1999;59:279-284.