Export of importin α from the nucleus is mediated by a specific nuclear transport factor

Cell

Volumn 90, Issue 6, 1997, Pages 1061-1071

  Kutay, Ulrike ^a   Ralf Bischoff, F ^b   Kostka, Susanne ^c   Kraft, Regine ^c   Görlich, Dirk ^a  

^a Im Neuenheimer Feld 282   (Germany)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^c MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

KARYOPHERIN; NUCLEAR PROTEIN;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; CELL NUCLEUS; CELL NUCLEUS MEMBRANE; INTRACELLULAR TRANSPORT; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; XENOPUS;

ANIMALIA;

EID: 0342276108     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0092-8674(00)80372-4     Document Type: Article

References (72)

1. Adam, S.A., and Gerace, L. (1991). Cytosolic proteins that specifically bind nuclear location signals are receptors for nuclear import. Cell 66, 837-847.
2. Aitchison, J.D., Blobel, G., and Rout, M.P. (1996). Kap 104: a karyopherin involved in the nuclear transport of messenger RNA binding proteins. Science 274, 624-627.
3. Becker, J., Melchior, F., Gerke, V., Bischoff, F.R., Ponstingl, H., and Wittinghofer, A. (1995). RNA1 encodes a GTPase-activating protein specific for Gsp1p, the Ran/TC4 homologue of Saccharomyces cerevisiae. J. Biol. Chem. 270, 11860-11865.
4. Bischoff, F.R., Klebe, C., Kretschmer, J., Wittinghofer, A., and Ponstingl, H. (1994). RanGAP1 induces GTPase activity of nuclear ras-related Ran. Proc. Natl. Acad. Sci. USA 91, 2587-2591.
5. Bischoff, F.R., Krebber, H., Kempf, T., Hermes, I., and Ponstingl, H. (1995a). Human RanGTPase activating protein RanGAP1 is a homolog of yeast RNA1p involved in messenger RNA processing and transport. Proc. Natl. Acad. Sci. USA 92, 1749-1753.
6. Bischoff, F.R., Krebber, H., Smirnova, E., Dong, W.H., and Ponstingl, H. (1995b). Coactivation of RanGTPase and inhibition of GTP dissociation by Ran GTP binding protein RanBP1. EMBO J. 14, 705-715.
7. Bischoff, F.R., and Ponstingl, H. (1991b). Catalysis of guanine nucleotide exchange on Ran by the mitotic regulator RCC1. Nature 354, 80-82.
8. Bischoff, F.R., and Ponstingl, H. (1991a). Mitotic regulator protein RCC1 is complexed with a nuclear ras-related polypeptide. Proc. Natl. Acad. Sci. USA 88, 10830-10834.
9. Brinkmann, U., Brinkmann, E., Gallo, M., and Pastan, I. (1995). Cloning and characterization of a cellular apoptosis susceptibility gene, the human homologue to the yeast chromosome segregation gene CSE1. Proc. Natl. Acad. Sci. USA 92, 10427-10431.
10. Brinkmann, U., Brinkmann, E., Gallo, M., Scherf, U., and Pastan, I. (1996). Role of CAS, a human homologue to the yeast chromosome segregation gene CSE1, in toxin and tumor necrosis factor mediated apoptosis. Biochemistry 35, 6891-6899.
11. Chi, N.C., Adam, E.J.H., Visser, G.D., and Adam, S.A. (1996). RanBP1 stabilises the interaction of Ran with p97 in nuclear protein import. J. Cell Biol. 135, 559-569.
12. Corbett, A.H., Koepp, D.M., Schlenstedt, G., Lee, M.S., Hopper, A.K., and Silver, P.A. (1995). Rna1p, a Ran/TC4 GTPase activating protein, is required for nuclear import. J. Cell Biol. 130, 1017-1026.
13. Corbett, A.H., and Silver, P.A. (1997). Nucleocytoplasmic transport of macromolecules. Microbiol. Mol. Biol. Rev. 61, 193-211.
14. 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.
15. Deane, R., Schäfer, W., Zimmermann, H.-P., Mueller, L., Görlich, D., Prehn, S., Ponstingl, H., and Bischoff, F.R. (1997). Ran-binding protein 5 (RanBP5) is related to the nuclear transport factor importin β but interacts differently with RanBP1. Mol. Cell. Biol., in press.
16. Dingwall, C., and Laskey, R.A. (1991). Nuclear targeting sequences - a consensus? Trends Biochem. Sci. 16, 478-481.
17. Drivas, G.T., Shih, A., Coutavas, E., Rush, M.G., and D'Eustachio, P. (1990). Characterization of four novel ras-like genes expressed in a human teratocarcinoma cell line. Mol. Cell. Biol. 10, 1793-1798.
18. Fischer, U., Huber, J., Boelens, W.C., Mattaj, I.W., and Lührmann, R. (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.
19. 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.
20. Fornerod, M., van Deursen, J., van Baal, S., Reynolds, A., Davis, D., Gopal, M., Fransen, J., and Grosveld, G. (1997a). The human homologue of yeast Crm1 is in a dynamic subcomplex with Can/Nup214 and a novel nuclear pore component. EMBO J. 16, 807-816.
21. Fornerod, M., Ohno, M., Yoshida, M., and Mattaj, I.W. (1997). CRM1 is an export receptor for leucine-rich nuclear export signals. Cell, this issue, 90, 1051-1060.
22. Fridell, R.A., Fischer, U., Lührmann, R., Meyer, B.E., Meinkoth, J.L., Malim, M.H., and Cullen, B.R. (1996). Amphibian TFIIIA proteins contain a sequence element functionally equivalent to the nuclear export signal of HIV-1 Rev. Proc. Natl. Acad. Sci. USA 93, 2936-2940.
23. 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.
24. Görlich, D. (1997). Nuclear protein import. Curr. Opin. Cell Biol. 9, 412-419.
25. Görlich, D., Kostka, S., Kraft, R., Dingwall, C., Laskey, R.A., Hartmann, E., and Prehn, S. (1995a). Two different subunits of importin cooperate to recognize nuclear localization signals and bind them to the nuclear envelope. Curr. Biol. 5, 383-392.
26. Görlich, D., Vogel, F., Mills, A.D., Hartmann, E., and Laskey, R.A. (1995b). Distinct functions for the two importin subunits in nuclear protein import. Nature 377, 246-248.
27. Görlich, D., Henklein, P., Laskey, R.A., and Hartmann, E. (1996a). A 41 amino acid motif in importin alpha confers binding to importin beta and hence transit into the nucleus. EMBO J. 15, 1810-1817.
28. Görlich, D., Panteß, 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.
29. Görlich, D., Kraft, R., Kostka, S., Vogel, F., Hartmann, E., Laskey, R.A., Mattaj, I.W., and Izaurralde, E. (1996c). Importin provides a link between nuclear protein import and U snRNA export. Cell 87, 21-32.
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. Hopper, A.K., Traglia, H.M., and Dunst, R.W. (1990). The yeast RNA1 gene product necessary for RNA processing is located in the cytosol and apparently excluded from the nucleus. J. Cell Biol. 111, 309-321.
32. Irniger, S., Piatti, S., Michaelis, C., and Nasmyth, K. (1995). Genes involved in sister chromatid separation are needed for B-type cyclin proteolysis in budding yeast. Cell 81, 269-278.
33. Izaurralde, E., Kutay, U., Mattaj, I.W., and Görlich, D. (1997). The asymmetric distribution of the constituents of the Ran system is essential for transport into and out of the nucleus. EMBO J., in press.
34. Klebe, C., Bischoff, F.R., Ponstingl, H., and Wittinghofer, A. (1995). Interaction of the nuclear GTP-binding protein Ran with its regulatory proteins RCC1 and RanGAP1. Biochemistry 34, 639-647.
35. Koepp, D.M., and Silver, P.A. (1996). A GTPase controlling nuclear trafficking: running the right way or walking randomly? Cell 87, 1-4.
36. Koepp, D., Wong, D., Corbett, A., and Silver, P. (1996). Dynamic localisation of the nuclear import receptor and its interactions with transport factors. J. Cell Biol. 133, 1163-1176.
37. Kutay, U., Izaurralde, E., Bischoff, F.R., Mattaj, I.W., and Görlich, D. (1997). Dominant-negative mutants of importin β block multiple pathways of import and export through the nuclear pore complex. EMBO J. 16, 1153-1163.
38. Leno, G.H., and Laskey, R.A. (1991). DNA replication in cell-free extracts from Xenopus laevis. Meth. Cell Biol. 36, 561-579.
39. Loeb, J.D.J., Schlenstedt, G., Pellman, D., Kornitzer, D., Silver, P.A., and Fink, G.R. (1995). The yeast nuclear import receptor is required for mitosis. Proc. Natl. Acad. Sci. USA 92, 7647-7651.
40. Lounsbury, K.M., and Macara, I.G. (1997). Ran-binding protein 1 (RanBP1) forms a ternary complex with Ran and karyopherin b and reduces GTPase-activating protein (RanGAP) inhibition by karyopherin b. J. Biol Chem. 272, 551-555.
41. Mahajan, R., Delphin, C., Guan, T., Gerace, L., and Melchior, F. (1997). A small ubiquitin-related polypeptide involved in targeting RanGAP1 to nuclear pore complex protein RanBP2. Cell 88, 97-107.
42. Matunis, M.J., Coutavas, E., and Blobel, G. (1996). A novel ubiquitin-like modification modulates the partitioning of the Ran-GTPase-activating protein between cytosol and nuclear pore complex. J. Cell Biol. 135, 1457-1470.
43. Melchior, F., Paschal, B., Evans, E., and Gerace, L. (1993a). Inhibition of nuclear protein import by nonhydrolyzable analogs of GTP and identification of the small GTPase Ran/TC4 as an essential transport factor. J. Cell Biol. 123, 1649-1659.
44. Melchior, F., Weber, K., and Gerke, V. (1993b). A functional homologue of the RNA1 gene product in Schizosaccharomyces pombe: purification, biochemical characterization, and identification of a leucine-rich repeat motif. Mol. Biol. Cell 4, 569-581.
45. 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.
46. 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. 12, 3587-3598.
47. Moore, M.S., and Blobel, G. (1993). The GTP-binding protein Ran/ TC4 is required for protein import into the nucleus. Nature 365, 661-663.
48. Moore, M.S., and Blobel, G. (1994). Purification of a Ran-interacting protein that is required for protein import into the nucleus. Proc. Natl. Acad. Sci. USA 91, 10212-10216.
49. Moroianu, J., Hijikata, M., Blobel, G., and Radu, A. (1995). Mammalian karyopherin a1b and a2b heterodimers: a1 or a2 subunit binds nuclear localization sequence and b subunit interacts with peptide repeat containing nucleoporins. Proc. Natl. Acad. Sci. USA 92, 6532-6536.
50. 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.
51. Nigg, E.A. (1997). Nucleocytoplasmic transport: signals, mechanism and regulation. Nature 386, 779-787.
52. Ohtsubo, M., Okazaki, H., and Nishimoto, T. (1989). The RCC1 protein, a regulator for the onset of chromosome condensation locates in the nucleus and binds to DNA. J. Cell Biol. 109, 1389-1397.
53. Palacios, I., Weis, K., Klebe, C., and Dingwall, C. (1996). Ran/TC4 mutants identify a common requirement for snRNP and protein import into the nucleus. J. Cell Biol. 133, 485-494.
54. 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 88, 985-994.
55. 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.
56. Richards, S.A., Carey, K.L., and Macara, I.G. (1997). Requirement of guanosine triphosphate-bound Ran for signal-mediated nuclear protein export. Science 276, 1842-1844.
57. Richards, S.A., Lounsbury, K.M., Carey, K.L., and Macara, I.G. (1996). A nuclear export signal is essential for the cytosolic localisation of the Ran binding protein, RanBP1. J. Cell Biol. 134, 1157-1168.
58. Richards, S.A., Lounsbury, K.M., and Macara, I.G. (1995). The C terminus of the nuclear Ran/TC4 GTPase stabilises the GDP bound state and mediates interactions with RCC1, Ran-GAP and HTF9A/RanBP1. J. Biol. Chem. 270, 14405-14411.
59. Schlenstedt, G. (1996). Protein import into the nucleus. FEBS Lett. 389, 75-79.
60. + RNA in the cytoplasm. Proc. Natl. Acad. Sci. USA 92, 225-229.
61. Shulga, N., Roberts, P., Spitz, L., Tabb, M.M., Nomura, M., and Goldfarb, D.S. (1996). In vivo nuclear transport kinetics in Saccharomyces cerevisiae: a role for heat shock protein 70 during targeting and translocation. J. Cell. Biol. 135, 329-339.
62. Siomi, H., and Dreyfuss, G. (1995). A nuclear localization domain in the hnRNP A1 protein. J. Cell Biol. 129, 551-560.
63. Stade, K., Ford, C.S., Guthrie, C., and Weis, K. Exportin 1 (Crm1p) is an essential nuclear export factor. Cell, this issue, 90, 1041-1050.
64. Weighardt, F., Biamonti, G., and Riva, S. (1995). Nucleo-cytoplasmic distribution of human hnRNP proteins: a search for the targeting domains of hnRNP A1. J. Cell Sci. 108, 545-555.
65. Weis, K., Mattaj, I.W., and Lamond, A.I. (1995). Identification of hSRP1α as a functional receptor for nuclear localization sequences. Science 268, 1049-1053.
66. Weis, K., Ryder, U., and Lamond, A.I. (1996a). The conserved aminoterminal domain of hSRP1α is essential for nuclear protein import. EMBO J. 15, 1818-1825.
67. Weis, K., Dingwall, C., and Lamond, A.I. (1996b). Characterization of the nuclear protein import mechanism using Ran mutants with altered nucleotide binding specificities. EMBO J. 15, 7120-7128.
68. Wen, W., Meinkoth, J.L., Tsien, R.Y., and Taylor, S.S. (1995). Identification of a signal for rapid export of proteins from the nucleus. Cell 82, 463-473.
69. Wu, J., Matunis, M.J., Kraemer, D., Blobel, G., and Coutavas, E. (1995). Nup358, acytoplasmically 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.
70. Xiao, Z., McGrew, J.T., Schroeder, A.J., and Fitzgerald-Hayes, M. (1993). CSE1 and CSE2, two new genes required for accurate mitotic chromosome segregation in Saccharomyces cerevisiae. Mol. Cell Biol. 13, 4691-4702.
71. Yano, R., Oakes, M., Yamaghishi, M., Dodd, J.A., and Nomura, M. (1992). Cloning and characterization of SRP1, a suppressor of temperature-sensitive RNA polymerase I mutations, in Saccharomyces cerevisiae. Mol. Cell. Biol. 12, 5640-5651.
72. Yokoyama, N., Hayashi, N., Seki, T., Panté, N., Ohba, T., Nishii, K., Kuma, K., Hayashida, T., Miyata, T., Aebi, U., et al. (1995). A giant nucleopore protein that binds Ran/TC4. Nature 376, 184-188.