Nucleocytoplasmic recycling of the nuclear localization signal receptor α subunit in vivo is dependent on a nuclear export signal, energy, and RCC1

Journal of Cell Biology

Volumn 139, Issue 2, 1997, Pages 313-325

  Boche, Irene ^a   Fanning, Ellen ^a  

^a VANDERBILT UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GUANOSINE DIPHOSPHATE; GUANOSINE TRIPHOSPHATE; NUCLEAR PROTEIN; RECEPTOR SUBUNIT;

ANIMAL CELL; ARTICLE; CELL ENERGY; CELL NUCLEUS; CELL STRAIN BHK; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOPLASM; INTRACELLULAR TRANSPORT; MICROINJECTION; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TEMPERATURE DEPENDENCE; VERO CELL;

ALPHA KARYOPHERINS; ANIMALS; CARRIER PROTEINS; CELL CYCLE PROTEINS; CELL LINE; CELL NUCLEUS; CERCOPITHECUS AETHIOPS; CLONING, MOLECULAR; CRICETINAE; CYTOPLASM; DNA-BINDING PROTEINS; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HUMANS; KINETICS; MICROINJECTIONS; NUCLEAR LOCALIZATION SIGNALS; NUCLEAR PROTEINS; RECOMBINANT FUSION PROTEINS; SIGNAL TRANSDUCTION; VERO CELLS;

EID: 0030665816     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.139.2.313     Document Type: Article

References (69)

1. Adam, E.J.H., and S.A. Adam. 1994. Identification of cytosolic factors required for nuclear location sequence-mediated binding to the nuclear envelope. J. Cell Biol. 125:547-555.
2. Adam, S.A., T.J. Lobl, M.A. Mitchell, and L. Gerace. 1990. Identification of specific binding proteins for a nuclear localization sequence. Nature (Lond.). 337:276-279.
3. Aitchinson, J.D., G. Blobel, and M.P. Rout. 1995. Nup 120p: a yeast nucleoporin required for NPC distribution and mRNA transport. J. Cell Biol. 131:1659-1675.
4. Bischoff, F.R., and H. Ponstingl. 1991a. Mitotic regulator protein RCC1 is complexed with a nuclear ras-related polypeptide. Proc. Natl. Acad. Sci. USA. 88:10830-10834.
5. Bischoff, F.R., and H. Ponstingl. 1991b. Catalysis of guanine nucleotide exchange on Ran by the mitotic regulator RCC1. Nature (Lond.). 354:80-82.
6. Bischoff, F.R., C. Klebe, J. Kretschmer, A. Wittinghofer, and H. Ponstingl. 1994. RanGAP1 induces GTPase activity of nuclear Ras-related Ran. Proc. Natl. Acad. Sci. USA. 91:2587-2591.
7. Bischoff, F.R., H. Krebber, T. Kempf, I. Hermes, and H. Ponstingl. 1995a. Human RanGTPase activating protein RanGAP1 is a homologue of yeast Rnalp involved in mRNA processing and transport. Proc. Natl. Acad. Sci. USA. 92:1794-1753.
8. Bischoff, F.R., H. Krebber, E. Smirnova, W. Dong, and H. Ponstingl. 1995b, Coactivation of RanGTPase and inhibition of GTP dissociation by RanGTP binding protein RanBP1. EMBO (Eur. Mol. Biol. Organ.) J. 14:705-715.
9. Chi, N.C., E.J.H. Adams, and S. Adams. 1995. Sequence and characterization of cytoplasmic nuclear protein import factor p97. J. Cell Biol. 130:265-274.
10. Chi, N.C., E.J.H. Adams, G.D. Visser, and S. Adams. 1996. RanBP1 stabilizes the interaction of Ran with p97 in nuclear protein import. J. Cell Biol. 135: 559-569.
11. Corbett, A.H., D.M. Koepp, G. Schlenstedt, M.S. Lee, A.K. Hopper, and P.A. Silver. 1995. Rna1p. a Ran/TC4GTPase activating protein, is required for nuclear import. J. Cell Biol. 130:1017-1026.
12. Cuomo, C.A., S.A. Kirch, J. Gyuris, R. Brent, and M.A. Oettinger. 1994. Rch1, a protein that specifically interacts with the RAG-1 recombination-activating protein. Proc. Nail. Acad. Sci. USA. 91:6156-6160.
13. Dasso, M. 1993. RCC1 in the cell cycle: the regulator of chromosome condensation takes on new roles. Trends Biochem. Sci. 18:96-101.
14. Dickmanns, A., R.F. Bischoff, C. Marshallsay, R. Lührmann, H. Ponstingl, and E. Fanning. 1996. The thermolability of nuclear protein import in tsBN2 cells is suppressed by microinjected Ran-GTP or -GDP, but not by RanQ69L or RanT24N. J. Cell Sci. 109:1449-1457.
15. Dingwall, C., and R.A. Laskey. 1991. Nuclear targeting sequences-a consensus? Trends Biol. Sci. 16:478-481.
16. Earley, E.M., and K.M. Johnson. 1988. The lineage of Vero, Vero 76 and its clone C1008 in the United States. In Vero Cells - Origin, Properties, and Biomedical Applications. B. Simizu and T. Terasima, editors. Soft Science Publications, Tokyo, Japan. 26-29.
17. Fischer, U., J. Huber, W.C. Boelens, I.W. Mattaj, and R. Lührmann. 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.
18. Forbes, C.J. 1992. Structure and function of the nuclear pore. Annu. Rev. Cell Biol. 8:495-527.
19. Gallay, P., S. Verna, C. Mundy, M. Oettinger, and D. Trono. 1996. Role of the karyopherin pathway in Human Immunodeficiency Virus Type 1 nuclear import. J. Virol. 70:1027-1032.
20. Garcia-Bustos, J.F., J. Heitman, and M. Hall. 1991. Nuclear protein localization. Biochim. Biophys. Acta. 1071:83-101.
21. Gerace, L. 1995. Nuclear export signals and the fast track to the cytoplasm. Cell. 82:341-344.
22. Goding, J.W. 1983. Monoclonal Antibodies: Principles and Practice. Academic Press, New York. 276 pp.
23. Görlich, D., and I.W. Mattaj. 1996. Nucleocytoplasmic transport. Science (Wash. DC). 271:1513-1518.
24. Görlich, D., S. Prehn, R.A. Laskey, and E. Hartmann. 1994. Isolation of a protein that is essential for the first step of nuclear protein import. Cell. 79:767-778.
25. Görlich, D., S. Kostka, R. Kraft, C. Dingwall, R.A. Laskey, E. Hartmann, and S. Prehn. 1995a. Two different subunits of importin cooperate to recognize nuclear location signals and bind them to the nuclear envelope. Curr. Biol. 5: 383-392.
26. Görlich, D., F. Vogel, A.D. Mills, E. Hartmann, and R.A. Laskey. 1995b. Distinct functions for the two importin subunits in nuclear protein import. Nature (Lond.). 377:246-248.
27. Görlich, D., P. Henklein, R.A. Laskey, and E. Hartmann. 1996a. A 41 amino acid motif in importin-α confers binding to importin-β and hence transit into the nucleus. EMBO (Eur. Mol. Biol. Organ.) J. 15:1810-1817.
28. Görlich, D., N. Pante, U. Kutay, U. Aebi, and F.R. Bischoff. 1996b. Identification of different roles for RanGDP and RanGTP in nuclear protein import. EMBO (Eur. Mol. Biol. Organ.) J. 15: 5584-5594.
29. Grundmann, U., C. Nerlich, T. Rein, F. Lottspeich, and H.A. Kuepper. 1988. Isolation of cDNA coding for the placental protein 15 (ppl5). Nucleic Acids Res. 16:4721.
30. Gurney, E.G., R.O. Harrison, and F. Fenno. 1980. Monoclonal antibodies against SV40 T antigens: evidence for distinct subclasses of large T antigen and for similarities among nonviral T antigens. J. Virol. 34:752-763.
31. Imamoto, M., T. Shimamoto, T. Takao, T. Tachibana, S. Kose, M. Matsubae, T. Sekimoto, Y. Shimonshi, and Y. Yoneda. 1995a. In vivo evidence for involvement of a 58 kD component of nuclear pore targeting complex in nuclear protein import. EMBO (Eur. Mol. Biol. Organ.) J. 14:3617-3626.
32. Imamoto, M., T. Tachibana, M. Matsubae, and Y. Yoneda. 1995b. A karyophilic protein forms a stable complex with cytoplasmic components before nuclear pore binding. J. Biol. Chem. 270:8559-8565.
33. Johnson, D.G., and G.M. de C. Nogueira Araujo. 1981. A simple method of reducing the fading of immunofluorescence during microscopy. J. Immunol. Methods. 43:349-350.
34. Koepp, D.M., D.H. Wong, A.H. Corbett, and P.A. Silver. 1996. Dynamic localization of the nuclear import receptor and its interactions with transport factors. J. Cell Biol. 133:1163-1176.
35. Mahajan, R.C., C. Delphin, T. Guan, L. Gerace, and F. Melchior. 1997. A small ubiquitin-related polypeptide involved in targeting RanGAP1 to nuclear pore complex protein RanBP2. Cell. 88:97-107.
36. Matunis, M.J., E. Coutavas, and G. Blobel. 1996. A novel ubiquitin-like modification modulates the partitioning of the Ran-GTPase-activation protein RanGAP1 between the cytosol and the nuclear pore complex. J. Cell Biol. 135:1457-1470.
37. Melchior, F., B. Pascal, 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 transport factor. J. Cell Biol. 123: 1649-1659.
38. Melchior, F., and L. Gerace. 1995. Mechanisms of nuclear protein import. Curr. Opin. Cell Biol. 7:310-318.
39. Melchior, F., T. Guan, N. Yokoyama, T. Nishimoto, and L. Gerace. 1995. GTP hydrolysis by Ran occurs at the nuclear pore complex in an early step of protein import. J. Cell Biol. 131:571-582.
40. Moore, M.S., and G. Blobel. 1992. The two steps of nuclear import, targeting to the nuclear envelope and translocation through the nuclear pore, require different cellular cytosolic factors. Cell. 69:939-950.
41. 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.
42. 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.
43. Moroianu, J., G. Blobel, and A. Radu. 1995a. Previously identified protein of uncertain function is karyopherin a and together with karyopherin β docks import substrates at nuclear pore complexes. Proc. Natl. Acad. Sci. USA. 92: 2008-2011.
44. Moroianu, J., M. Hijikata, G. Blobel, and A. Radu. 1995b. Mammalian karyopherin α1β and α2β: α1 or α2 subunit binds nuclear localization signal and β subunit interacts with peptide repeat-containing nucleoporins. Proc. Natl. Acad. Sci. USA. 92:6532-6536.
45. Moroianu, J., G. Blobel, and A. Radu. 1996a. The binding site of karyopherin α for karyopherin β overlaps with a nuclear localization sequence. Proc. Natl. Acad. Sci. USA. 93:6572-6576.
46. Moroianu, J., G. Blobel, and A. Radu. 1996b. Nuclear protein import: Ran-GTP dissociates the karyopherin αβ heterodimer by displacing α from an overlapping binding site on β. Proc. Natl. Acad. Sci. USA. 93:7059-7062.
47. Nehrbass, U., and G. Blobel. 1996. Role of the nuclear transport factor p10 in nuclear import. Science (Wash. DC). 272:120-122.
48. Newmeyer, D.D., and D.J. Forbes. 1990. An N-ethylmaleimide-sensitive cytosolic factor for nuclear protein import: requirement in signal-mediated binding to the nuclear pore. J. Cell Biol. 110:547-557.
49. Nigg, E.A. 1997. Nucleocytoplasmic transport: signals, mechanisms and regulation. Nature (Lond.). 386:779-787.
50. Nishimoto, T., and C. Basilico. 1978. Analysis of a method for selecting temperature-sensitive mutants of BHK cells. Somatic Cell Genet. 4:323-340.
51. Nishimoto, T., E. Eilen, and C. Basilico. 1978. Premature chromosome condensation in a ts DNA-mutant of BHK cells. Cell. 15:475-483.
52. Ohtsubo, M., R. Kai, N. Furuno, T. Sekiguchi, M. Hayashida, K. Kuma, T. Miyata, S. Funkushige, T. Murotsu, K. Matsubara, and T. Nishimoto. 1987. 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. 1:585-593.
53. Paschal, B.M., and L. Gerace. 1995. Identification of NTF2, a cytosolic factor for nuclear import that interacts with nuclear pore complex protein p62. J. Cell Biol. 129:925-937.
54. Paschal, B.M., C. Delphin, and L. Gerace. 1996. Nucleotide-specific interaction of Ran/TC4 with nuclear transport factors NTF2 and p97. Proc. Natl. Acad. Sci. USA. 93:7679-7683.
55. Podust, V.N., L.M. Podust, F. Goubin, B. Ducommun, and U. Hübscher. 1995. Mechanism of inhibition of proliferation cell nuclear antigen-dependent DNA synthesis by the cyclin-dependent kinase inhibitor p21. Biochemistry. 34:8869-8875.
56. Radu, A., G. Blobel, and M.S. Moore. 1995. Identification of a protein complex that is required for nuclear protein import and mediates docking of import substrate to distinct nucleoporins. Proc. Natl. Acad. Sci. USA. 92:1769-1773.
57. Ren, M., G. Drivas, P. D'Eustachio, and M.G. Rush. 1993. Ran/TC4: a small nuclear GTP-binding protein that regulates DNA synthesis. J. Cell Biol. 120: 313-323.
58. 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.
59. Richards, S.A., K.L. Carey, and I.G. Macara. 1997. Requirement of guanosine triphosphate-bound Ran for signal-mediated nuclear protein export. Science (Wash. DC). 276:1842-1844.
60. Rout, M., and S. Wente. 1994. Pores for the thought: nuclear pore complex proteins. Trends Cell Biol. 4:357-365.
61. Schlenstedt, G., S. Saavedra, J.D.J. Loeb, C.N. Cole, and P.A. Silver. 1995. The GTP-bound form of the yeast Ran/TC4 homologue blocks nuclear protein import and appearance of poly (A)+ RNA in the cytoplasm. Proc. Natl. Acad. Sci. USA. 92:225-229.
62. Schmidt-Zachmann, M.S., C. Dargemont, L.C, Kuehn, and E.A. Nigg. 1993. Nuclear export of proteins: the role of nuclear retention. Cell. 74:493-504.
63. Schneider, C., K. Weiβhart, L.A. Guarino, I. Dornreiter, and E. Fanning. 1994. Species specific functional interactions of DNA polymerase α-primase with SV40 T antigen require SV40 origin DNA. Mol. Cell. Biol. 14:3176-3185.
64. stoker, M.P.G., and I.A. MacPherson. 1964. Syrian hamster fibroblast cell line BHK21 and its derivatives. Nature (Lond.). 203:1355-1357.
65. 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.
66. Weis, K., I. Mattaj, and A. Lamond. 1995. Identification of hSRP1α as a functional receptor for nuclear localization sequences. Science (Wash. DC). 268: 1049-1053.
67. Weis, K., U. Ryder, and A.I. Lamond. 1996. The conserved amino-terminal domain of hSRP1α is essential for nuclear protein import. EMBO (Eur. Mol. Biol. Organ.) J. 15:1818-1825.
68. 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.
69. Yano, R., M. Oakes, M. Yamaghishi, J.A. Dodd, and M. Nomura. 1992. Cloning and characterization of SRP1p, a suppressor of temperature-sensitive RNA polymerase I mutations, in Saccharomyces cerevisiae. Mol. Cell. Biol. 12:5640-5651.