Nup153 is an M9-containing mobile nucleoporin with a novel Ran-binding domain

EMBO Journal

Volumn 18, Issue 7, 1999, Pages 1982-1995

  Nakielny, Sara ^a   Shaikh, Sarah ^b   Burke, Brian ^b   Dreyfuss, Gideon ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF CALGARY   (Canada)

Author keywords

Nucleocytoplasmic transport; Nup153; Phage display; Ran GTPase; Transportin

Indexed keywords

CARRIER PROTEIN; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN; NUCLEOPORIN; ZINC FINGER PROTEIN;

ARTICLE; BINDING SITE; CYTOPLASM; HUMAN; HUMAN CELL; NONHUMAN; PHAGE DISPLAY; PRIORITY JOURNAL; PROTEIN TRANSPORT;

EID: 0033118942     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/18.7.1982     Document Type: Article

References (101)

1. Adam, S.A., Marr, R.S. and Gerace, L. (1990) Nuclear protein import in permeabilized mammalian cells requires soluble cytoplasmic factors. J. Cell Biol., 111, 807-816.
2. Aitchison, J.D., Blobel, G. and Rout, M.P. (1996) Kap104p: a karyopherin involved in the nuclear transport of messenger RNA binding proteins. Science, 274, 624-627.
3. Arts, G.-J., Fornerod, M. and Mattaj, I.W. (1998) Identification of a nuclear export receptor for tRNA. Curr. Biol., 8, 305-314.
4. Bastos, R., Lin, A., Enarson, M. and Burke, B. (1996) Targeting and function in mRNA export of nuclear pore complex protein Nup153. J. Cell Biol., 134, 1141-1156.
5. Bastos, R., de Pouplana, L.R., Enarson, M., Bodoor, K. and Burke, B. (1997) Nup84, a novel nucleoporin that is associated with CAN/Nup214 on the cytoplasmic face of the nuclear pore complex. J. Cell Biol., 137, 989-1000.
6. Beddow, A.L., Richards, S.A., Orem, N.R. and Macara, I.G. (1995) The Ran/TC4 GTPase-binding domain: identification by expression cloning and characterization of a conserved sequence motif. Proc. Natl. Acad. Sci. USA, 92, 3328-3332.
7. 1168, a novel RNA/ssDNA-binding protein with homology to the pro-oncoproteins TLS/FUS and EWS, is associated with both TFIID and RNA polymerase II. EMBO J., 15, 5022-5031.
8. Bischoff, F.R. and Görlich, D. (1997) RanBP1 is crucial for the release of RanGTP from importin β-related nuclear transport factors. FEBS Lett., 419, 249-254.
9. Bischoff, F.R., Krebber, H., Smirnova, E., Dong, W. and Ponstingl, H. (1995) Co-activation of RanGTPase and inhibition of GTP dissociation by Ran-GTP binding protein RanBP1. EMBO J., 14, 705-715.
10. Boche, I. and Fanning, E. (1997) Nucleocytoplasmic recycling of the nuclear localization signal receptor alpha subunit in vivo is dependent on a nuclear export signal, energy and RCC1. J. Cell Biol., 139, 313-325.
11. Bonifaci, N., Moroianu, J., Radu, A. and Blobel, G. (1997) Karyopherin β2 mediates nuclear import of a mRNA binding protein. Proc. Natl Acad. Sci. USA, 94, 5055-5060.
12. Chi, N.C. and Adam, S.A. (1997) Functional domains in nuclear import factor p97 for binding the nuclear localization sequence receptor and the nuclear pore. Mol. Biol. Cell, 8, 945-956.
13. Cole, C.N. and Saavedra, C. (1997) Regulation of the export of RNA from the nucleus. Semin. Cell Dev. Biol., 8, 71-78.
14. Cordes, V.C., Reidenbach, S., Rackwitz, H.-R. and Franke, W.W. (1997) Identification of protein p270/Tpr as a constitutive component of the nuclear pore complex-attached intranuclear filaments. J. Cell Biol., 136, 515-529.
15. Coutavas, E., Ren, M., Oppenheim, J.D., D'Eustachio, P. and Rush, M.G. (1993) Characterization of proteins that interact with the cell-cycle regulatory protein Ran/TC4. Nature, 366, 585-587.
16. Dahlberg, J.E. and Lund, E. (1998) Functions of the GTPase Ran in RNA export from the nucleus. Curr. Opin. Cell Biol. 10, 400-408.
17. Davis, L.I. (1995) The nuclear pore complex. Annu. Rev. Biochem., 64, 865-896.
18. Delphin, C., Guan, T., Melchior, F. and Gerace, L. (1997) RanGTP targets p97 to RanBP2, a filamentous protein localized at the cytoplasmic periphery of the nuclear pore complex. Mol. Biol. Cell, 8, 2379-2390.
19. Dingwall, C. Kandels-Lewis, S. and Séraphin, B. (1995) A family of Ran binding proteins that includes nucleoporins. Proc. Natl Acad. Sci. USA, 92, 7525-7529.
20. Dove, V. and Hurt, E. (1997) From nucleoporins to nuclear pore complexes. Curr. Opin. Cell Biol., 9, 401-411.
21. Enarson, P., Enarson.M., Bastos, R. and Burke, B. (1998) Amino-terminal sequences that direct nucleoporin Nup153 to the inner surface of the nuclear envelope. Chromosoma, 107, 228-236.
22. Floer, M. and Blobel, G. (1996) The nuclear transport factor karyopherin β binds stoichiometrically to Ran-GTP and inhibits the Ran GTPase activating protein. J. Biol. Chem., 271, 5313-5316.
23. Fornerod, M., Ohno, M., Yoshida, M. and Mattaj, I.W. (1997a) CRM1 is an export receptor for leucine-rich nuclear export signals. Cell, 90, 1051-1060.
24. Fornerod, M., van Deursen, J., van Baal, S., Reynolds, A., Davis, D., Murti, K.G., Fransen, J. and Grosveld, G. (1997b) The human homologue of yeast CRM1 is in a dynamic subcomplex with CAN/ Nup214 and a novel nuclear pore component Nup88. EMBO J., 16, 807-816.
25. Fridell, R.A., Truant, R., Thorne, L., Benson, R.E. and Cullen, B.R. (1997) Nuclear import of hnRNP A1 is mediated by a novel cellular cofactor related to karyopherin-β. J. Cell Sci., 110, 1325-1331.
26. Fukuda, M., Asano, S., Nakamura, T., Adachi, M., Yoshida, M., Yanagida, M. and Nishida, E. (1997) CRM1 is responsible for intracellular transport mediated by the nuclear export signal. Nature, 390, 308-311.
27. Görlich, D. (1998) Transport into and out of the cell nucleus. EMBO J., 17, 2721-2727.
28. Görlich, D., Henklein, P., Laskey, R.A. and Hartmann, E. (1996a) A 41 amino acid motif in importin-α confers binding to importin-β and hence transit into the nucleus. EMBO J., 15, 1810-1817.
29. Görlich, D., Panté, N., Kutay, U., Aebi, U. and Bischoff, F.R. (1996b) Identification of different roles for RanGDP and RanGTP in nuclear protein import. EMBO J., 15, 5584-5594.
30. Görlich, D., Dabrowski, M., Bischoff, F.R., Kutay, U., Bork, P., Hartmann, E., Prehn, S. and Izaurralde, E. (1997) A novel class of RanGTP binding proteins. J. Cell Biol., 138, 65-80.
31. Grandi, P., Dang, T., Pané, N., Shevchenko, A., Mann, M., Forbes, D. and Hurt, E. (1997) Nup93, a vertebrate homologue of yeast Nic96p. forms a complex with a novel 205-kDa protein and is required for correct nuclear pore assembly. Mol. Biol. Cell, 8, 2017-2038.
32. Guan, T., Müller, S., Klier, G., Panté, N., Blevitt, J.M., Haner, M., Paschal, B., Aebi, U. and Gerace, L. (1995) Structural analysis of the p62 complex, an assembly of O-linked glycoproteins that localizes near the central gated channel of the nuclear pore complex. Mol. Biol. Cell, 6, 1591-1603.
33. Hartmann, E. and Görlich, D. (1995) A Ran-binding motif in nuclear pore proteins. Trends Cell Biol., 5, 192-193.
34. Herold, A., Truant, R., Wiegand, H. and Cullen, B.R. (1998) Determination of the functional domain organization of the importin a nuclear import factor. J. Cell Biol., 143, 309-318.
35. Hu, T., Guan, T. and Gerace, L. (1996) Molecular and functional characterization of the p62 complex, an assembly of nuclear pore complex glycoproteins. J. Cell Biol., 134, 589-601.
36. Inoue, A., Takahashi, K.P., Kimura, M., Watanabe, T. and Morisawa, S. (1996) Molecular cloning of an RNA binding protein, S1-1. Nucleic Acids Res., 24, 2990-2997.
37. Iovine, M.K., Watkins, J.L. and Wente, S.R. (1995) The GLFG repetitive region of the nucleoporin Nup116p interacts with Kap95p, an essential yeast nuclear import factor. J. Cell Biol., 131, 1699-1713.
38. Izaurralde, E. and Adam, S. (1998) Transport of macromolecules between the nucleus and the cytoplasm. RNA, 4, 351-364.
39. Izaurralde, E., Jarmolowski, A., Beisel, C., Mattaj, I.W., Dreyfuss, G. and Fischer, U. (1997a) A role for the M9 transport signal of hnRNP A1 in mRNA nuclear export. J. Cell Biol., 137, 27-35.
40. Izaurralde, E., Kutay, U., von Kobbe, C., Mattaj, I.W. and Görlich, D. (1997b) The asymmetric distribution of the constituents of the Ran system is essential for transport into and out of the nucleus. EMBO J., 16, 6535-6547.
41. Jäkel, S. and Görlich, D. (1998) Importin β, transportin, RanBP5 and RanBP7 mediate nuclear import of ribosomal proteins in mammalian cells. EMBO J., 17, 4491-4502.
42. Kaffman, A., Miller Rank, N., O'Neill, E.M., Huang, L.S. and O'Shea, E.K. (1998) The receptor Msn5 exports the phosphorylated transcription factor Pho4 out of the nucleus. Nature, 396, 482-486.
43. Kamei, M., Webb, G.C., Young, I.G. and Campbell, H.D. (1998) SOLH, a human homologue of the Drosophila melanogaster small optic lobes gene is a member of the calpain and zinc-finger gene families and maps to human chromosome 16p13.3 near CATM (cataract with microphthalmia). Genomics, 51, 197-206.
44. Klebe, C., Bischoff, F.R., Ponsting I.H. and Wittinghofer, A. (1995) Interaction of the nuclear GTP-binding protein Ran with its regulatory proteins RCC1 and RanGAP1. Biochemistry, 34, 639-647.
45. Kose, S., Imamoto, N., Tachibana, T., Shimamoto, T. and Yoneda, Y. (1997) Ran-unassisted nuclear migration of a 97-kD component of nuclear pore-targeting complex. J. Cell Biol., 139, 841-849.
46. Kraemer, D., Wozniak, R.W., Blobel, G. and Radu, A. (1994) The human CAN protein, a putative oncogene product associated with myeloid leukemogenesis, is a nuclear pore complex protein that faces the cytoplasm. Proc. Natl Acad. Sci. USA, 91, 1519-1523.
47. Kraemer, D.M., Strambio-de-Castillia, C., Blobel, G. and Rout, M.P. (1995) The essential yeast nucleoporin NUP159 is located on the cytoplasmic side of the nuclear pore complex and serves in karyopherin-mediated binding of transport substrate. J. Biol. Chem., 270, 19017-19021.
48. Kutay, U., Bischoff, F.R., Kostka, S., Kraft, R. and Görlich, D. (1997a) Export of importin a from the nucleus is mediated by a specific nuclear transport factor. Cell, 90, 1061-1071.
49. Kutay, U., Izaurralde, E., Bischoff, F.R., Mattaj, I.W. and Görlich, D. (1997b) Dominant-negative mutants of importin-β block multiple pathways of import and export through the nuclear pore complex. EMBO J., 16, 1153-1163.
50. Kutay, U., Lipowsky, G., Izaurralde, E., Bischoff, F.R., Schwarzmaier, P., Hartmann, E. and Görlich, D. (1998) Identification of a tRNA-specific nuclear export receptor. Mol. Cell, 1, 359-369.
51. Lee, M.S., Henry, M. and Silver, P.A. (1996) A protein that shuttles between the nucleus and the cytoplasm is an important mediator of RNA export. Genes Dev., 10, 1233-1246.
52. Lounsbury, K.M., Beddow, A.L. and Macara, I.G. (1994) A family of proteins that stabilize the Ran/TC4 GTPase in its GTP-bound conformation. J. Biol. Chem., 269, 11285-11290.
53. Mackay, J. and Crossley, M. (1998) Zinc fingers are sticking together. Trends Biochem. Sci., 23, 1-4.
54. Mahajan, R., Delphin, C., Guan, T., Gerace, L. and Melchoir, F. (1997) A small ubiquitin-related polypeptide involved in targeting RanGAP1 to nuclear pore complex protein RanBP2. Cell, 88, 97-107.
55. Mattaj, I.W. and Englmeier, L. (1998) Nucleocytoplasmic transport: the soluble phase. Annu. Rev. Biochem., 67, 265-306.
56. Matunis, M.J., Coutavas, E. and Blobel, G. (1996) 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., 135, 1457-1470.
57. McMorrow, I., Bastos, R., Horton, H. and Burke, B. (1994) Sequence analysis of a cDNA encoding a human nuclear pore complex protein, hnup153. Biochim. Biophys. Acta, 1217, 219-223.
58. Melchior, F. and Gerace, L. (1998) Two-way trafficking with Ran. Trends Cell Biol., 8, 175-179.
59. Michael, W.M., Choi, M. and Dreyfuss, G. (1995) A nuclear export signal in hnRNP A1: a signal-mediated, temperature-dependent nuclear protein export pathway. Cell, 83, 415-422.
60. Michael, W.M., Eder, P.S. and Dreyfuss, G. (1997) The K nuclear shuttling domain: a novel signal for nuclear import and nuclear export in the hnRNP K protein. EMBO J., 16, 3587-3598.
61. Morohoshi, F., Arai, K., Takahashi, E.-i., Tanigami, A. and Ohki, M. (1996) Cloning and mapping of a human RBP56 gene encoding a putative RNA binding protein similar to FUS/TLS and EWS proteins. Genomics, 38, 51-57.
62. Nakielny, S. and Dreyfuss, G. (1996) The hnRNP C proteins contain a nuclear retention sequence that can override nuclear export signals. J. Cell Biol., 134, 1365-1373.
63. Nakielny, S. and Dreyfuss, G. (1997) Import and export of the nuclear protein import receptor transportin by a mechanism independent of GTP hydrolysis. Curr. Biol., 8, 89-95.
64. Nakielny, S., Siomi, M.C., Siomi, H., Michael, W.M., Pollard, V. and Dreyfuss, G. (1996) Transportin: nuclear transport receptor of a novel nuclear protein import pathway. Exp. Cell Res., 229, 261-266.
65. Nakielny, S., Fischer, U., Michael, W.M. and Dreyfuss, G. (1997) RNA transport. Annu. Rev. Neurosci., 20, 269-301.
66. Neville, M., Stutz, F., Lee, L., Davis, L.I. and Rosbash, M. (1997) The importin-β family member Crm1p bridges the interaction between Rev and the nuclear pore complex during nuclear export. Curr. Biol., 7, 767-775.
67. Nigg, E.A. (1997) Nucleocytoplasmic transport: signals, mechanisms and regulation. Nature, 386, 779-787.
68. Oliner, J.D., Kinzler, K.W., Meltzer, P.S., George, D.L. and Vogelstein, B. (1992) Amplification of a gene encoding a p53-associated protein in human sarcomas. Nature, 358, 80-83.
69. Ossareh-Nazari, B., Bachelerie, F. and Dargemont, C. (1997) Evidence for a role of CRM1 in signal-mediated nuclear protein export. Science, 278, 141-144.
70. Pante, N., Bastos, R., McMorrow, I., Burke, B. and Aebi, U. (1994) Interactions and three-dimensional localization of a group of nuclear pore complex proteins. J. Cell Biol., 126, 603-617.
71. Percipalle, P., Clarkson, W.D., Kent, H.M., Rhodes, D. and Stewart, M. (1997) Molecular interactions between the importin α/β heterodimer and proteins involved in vertebrate nuclear protein import. J. Mol. Biol., 226, 722-732.
72. Piñol-Roma, S. (1997) HnRNP proteins and the nuclear export of mRNA. Semin. Cell Dev. Biol., 8, 57-63.
73. Piñol-Roma, S. and Dreyfuss, G. (1992) Shuttling of pre-mRNA binding proteins between nucleus and cytoplasm. Nature, 355, 730-732.
74. Pollard, V.W., Michael, W.M., Nakielny, S., Siomi, M.C., Wang, F. and Dreyfuss, G. (1996) A novel receptor-mediated nuclear protein import pathway. Cell, 86, 985-994.
75. Powell, L. and Burke, B. (1990) Internuclear exchange of an inner nuclear membrane protein (p55) in heterokaryons: in vivo evidence for the association of p55 with the nuclear lamina. J. Cell Biol., 111, 2225-2234.
76. Radu, A., Moore, M.S. and Blobel, G. (1995) The peptide repeat domain of nucleoporin Nup98 functions as a docking site in transport across the nuclear pore complex. Cell, 81, 215-222.
77. Rexach, M. and Blobel, G. (1995) Protein import into nuclei: association and dissociation reactions involving transport substrate, transport factors and nucleoporins. Cell, 83, 683-692.
78. Richards, S.A., Carey, K.L. and Macara, J.G. (1997) Requirement of guanosine triphosphate-bound Ran for signal-mediated nuclear protein export. Science, 276, 1842-1844.
79. Ribbeck, K., Lipowsky, G., Kent, H.M., Stewart, M. and Görlich, D. (1998) NTF2 mediates nuclear import of Ran. EMBO J., 17, 6587-6598.
80. Rout, M.P. and Wente, S.R. (1994) Pores for thought: nuclear pore complex proteins. Trends Cell Biol., 4, 357-365.
81. Rush, M.G., Drivas, G. and D'Eustachio, P. (1996) The small nuclear GTPase Ran: how much does it run? BioEssays, 18, 103-112.
82. Shah, S., Tugendreich, S. and Forbes, D. (1998) Major binding sites for the nuclear import receptor are the internal nucleoporin Nup153 and the adjacent nuclear filament protein Tpr. J. Cell Biol., 141, 31-49.
83. Siomi, H. and Dreyfuss, G. (1995) A nuclear localization domain in the hnRNP A1 protein. J. Cell Biol., 129, 551-560.
84. Siomi, M.C., Eder, P.S., Kataoka, N., Wan, L., Liu, Q. and Dreyfuss, G. (1997) Transportin-mediated nuclear import of heterogeneous nuclear RNP proteins. J. Cell Biol., 138, 1181-1192.
85. Siomi, M.C., Fromont, M., Rain, J.-C., Wan, L., Wang, F., Legrain, P. and Dreyfuss, G. (1998) Functional conservation of the transportin nuclear import pathway in divergent organisms. Mol. Cell. Biol., 18, 4141-4148.
86. Stade, K., Ford, C.S., Guthrie, C. and Weis, K. (1997) Exportin 1 (Crm1p) is an essential nuclear export factor. Cell, 90, 1041-1050.
87. Stahl, B., Chou, J.H., Li, C., Südhof, T.C. and Jahn, R. (1996) Rab3 reversibly recruits rabphilin to synaptic vesicles by a mechanism analogous to raf recruitment by ras. EMBO J., 15, 1799-1809.
88. Stolow, D.T. and Haynes, S.R. (1995) Cabeza, a Drosophila gene encoding a novel RNA binding protein, shares homology with EWS and TLS, two genes involved in human sarcoma formation. Nucleic Acids Res., 23, 835-843.
89. Südhof, T.C. (1997) Function of Rab3 GDP-GTP exchange. Neuron, 18, 519-522.
90. Sukegawa, J. and Blobel, G. (1993) A nuclear pore complex protein that contains zinc finger motifs, binds DNA and faces the nucleoplasm. Cell, 72, 29-38.
91. Takiguchi, S., Tokino, T., Imai, T., Tanigami, A., Koyama, K. and Nakamura, Y. (1993) Identification and characterization of a cDNA, which is highly homologous to the ribonucleoprotein gene, from a locus (D10S102) closely linked to MEN2 (multiple endocrine neoplasia type 2). Cytogenet. Cell Genet., 64, 128-130.
92. + RNA binding protein. Mol. Cell. Biol., 18, 1449-1458.
93. Visa, N., Alzhanova-Ericsson, A.T., Sun, X., Kiseleva, E., Björkroth, B., Wurtz, T. and Daneholt, B. (1996) A pre-mRNA-binding protein accompanies the RNA from the gene through the nuclear pores and into polysomes. Cell, 84, 253-264.
94. Wang, Y., Okamoto, M., Schmitz, F., Hofmann, K. and Südhof, T.C. (1997) Rim is a putative Rab3 effector in regulating synaptic-vesicle fusion. Nature, 388, 593-598.
95. Wehner, E.P., Rao, E. and Brendel, M. (1993) Molecular structure and genetic regulation of SFA, a gene responsible for resistance to formaldehyde in Saccharomyces cerevisiae and characterization of its protein product. Mol. Gen. Genet., 237, 351-358.
96. Weighardt, F., Biamonti, G. and Riva, S. (1995) Nucleo-cytoplasmic distribution of human hnRNP proteins: a search for the targeting domains in hnRNP A1. J. Cell Sci., 108, 545-555.
97. Weis, K., Ryder, U. and Lamond, A.I. (1996) The conserved amino-terminal domain of hSRP1α is essential for nuclear protein import. EMBO J., 15, 1818-1825.
98. Wilken, N., Senécal, J.-L., Scheer, U. and Dabauvalle, M.-C. (1995) Localization of the Ran-GTP binding protein RanBP2 at the cytoplasmic side of the nuclear pore complex. Eur. J. Cell Biol., 68, 211-219.
99. Wu, J., Matunis, M.J., Kraemer, D., Blobel, G. and Coutavas, E. (1995) 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., 270, 14209-14213.
100. Yang, Q., Rout, M.P. and Akey, C.W. (1998) Three-dimensional architecture of the isolated yeast nuclear pore complex: functional and evolutionary implications. Mol. Cell, 1, 223-234.
101. Yokoyama, N. et al. (1995) A giant nucleopore protein that binds Ran/ TC4. Nature, 376, 184-188.