A distinct and parallel pathway for the nuclear import of an mRNA- binding protein

Journal of Cell Biology

Volumn 139, Issue 7, 1997, Pages 1645-1653

  Pemberton, Lucy F ^a   Rosenblum, Jonathan S ^a   Blobel, Günter ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; NUCLEOPORIN; RNA BINDING PROTEIN;

ARTICLE; CELL FRACTIONATION; CELL NUCLEUS; CYTOSOL; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PURIFICATION; PROTEIN TRANSPORT;

EID: 0031425954     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.139.7.1645     Document Type: Article

References (62)

1. Adam, E.J.H., and S. Adam. 1994. Identification of cytosolic factors required for nuclear location sequence-mediated binding to the nuclear envelope. J. Cell Biol. 125:547-555.
2. Aitchison, J.D., M.P. Rout, M. Marelli, G. Blobel, and R.W. Wozniak. 1995. Two novel related yeast nucleoporins Nup170p and Nup157p: complementation with the vertebrate homologue Nup155p and functional interactions with the yeast nuclear pore-membrane protein Pom152p. J. Cell Biol. 131: 1133-1148.
3. Aitchison, J.D., G. Blobel, and M.P. Rout. 1996. Kap104p: a karyopherin involved in the nuclear transport of messenger RNA binding proteins. Science. 274:624-627.
4. Anderson, J.T., S.M. Wilson, K.V. Datar, and M.S. Swanson. 1993. NAB2: a yeast nuclear polyadenylated RNA-binding protein essential for cell viability. Mol. Cell Biol. 13:2730-2741.
5. Birney, E., S. Kumar, and A.R. Krainer. 1993. Analysis of the RNA-recognition motif and RS and RGG domains: conservation in metazoan pre-mRNA splicing factors. Nucleic Acids Res. 21:5803-5816.
6. Bonifaci, N., J. Moroianu, A. Radu, and G. Blobel. 1997. Karyopherin β2 mediates nuclear import of a mRNA binding protein. Proc. Natl. Acad. Sci. USA. 94:5055-5060.
7. Bossie, M.A., C. DeHoratius, G. Barcelo, and P. Silver. 1992. A mutant nuclear protein with similarity to RNA binding proteins interferes with nuclear import in yeast. Mol. Biol. Cell. 3:875-893.
8. Chi, N.C., E.J.H. Adam, and S.A. Adam. 1995. Sequence and characterization of cytoplasmic nuclear import factor p 97. J. Cell Biol. 130:265-274.
9. Corbett, A.H., and P.A. Silver. 1997. Nucleocytoplasmic transport of macromolecules. Microbiol. Mol. Biol. Rev. 61:193-211.
10. Corbett, A.M., D.M. Koepp, G. Schlenstedt, M.S. Lee, A.K. Hopper, and P.A. Silver. 1995. Rna1p, a Ran/TC4 GTPase activating protein, is required for nuclear import. J. Cell Biol. 130:1017-1026.
11. 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.
12. Enenkel, C., G. Blobel, and M. Rexach. 1995. Identification of a yeast karyopherin heterodimer that targets import substrate to mammalian nuclear pore complexes. J. Biol. Chem. 270:16499-16502.
13. Finley, D., E. Ozkaynak, and A. Varshavsky. 1987. The yeast polyubiquitin gene is essential for resistance to high temperatures, starvation, and other stresses. Cell. 48:1035-1046.
14. Flach, J., M. Bossie, J. Vogel, A. Corbett, T. Jinks, D.A. Willins, and P.A. Silver. 1994. A yeast RNA-binding protein shuttles between the nucleus and the cytoplasm. Mol. Cell Biol. 14:8399-8407.
15. Floer, M., and G. Blobel. 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.
16. Fornerod, M., J. van Deursen, S. van Baal, A. Reynolds, D. Davis, K.G. Murti, J. Fransen, and G. Grosveld. 1997a. The human homologue of yeast CRM1 is in a dynamic subcomplex with CAN/Nup214 and a novel nuclear pore component Nup88. EMBO (Eur. Mol. Biol. Organ.) J. 16:807-816.
17. Fornerod, M., M. Ohno, M. Yoshida, and I.W. Mattaj. 1997b. CRM1 is an export receptor for leucine-rich nuclear export signals. Cell. 90:1051-1060.
18. Fridell, R.A., R. Truant, L. Thorne, R.E. Benson, and B.R. Cullen. 1997. Nuclear import of hnRNP A1 is mediated by a novel cellular cofactor related to karyopherin-β. J. Cell Sci. 110:1325-1331.
19. Gharahdaghi, F., M. Kirchner, J. Fernandez, and S.M. Mische. 1996. Peptide-mass profiles of polyvinylidene difluoride-bound proteins by matrix-assisted laser desorption/ionization time-of-flight mass spectrometry in the presence of nonionic detergents. Anal. Biochem. 233:94-99.
20. 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.
21. Görlich, D., F. Vogel, A. Mills, E. Hartmann, and R.A. Laskey. 1995. Distinct functions for the two importin subunits is nuclear protein import. Nature. 377:246-248.
22. Görlich, D., N. Pante, U. Kutay, U. Aebi, and F.R. Bischoff. 1996. Identification of different roles for RanGDP and RanGTP in nuclear protein import. EMBO (Eur. Mol. Biol. Organ.) J. 15:5584-5594.
23. Görlich, D., M. Dabrowski, F.R. Bischoff, U. Kutay, P. Bork, E. Hartmann, S. Prehn, and E. Izaurralde. 1997. A novel class of RanGTP binding proteins. J. Cell Biol. 138:65-80.
24. Henry, M., C.Z. Borland, M. Bossie, and P.A. Silver. 1996. Potential RNA binding proteins in Saccharomyces cerevisiae identified as suppressors of temperature-sensitive mutations in NPL3. Genetics. 142:103-115.
25. Imamoto, N., T. Shimamoto, T. Takao, T. Tachibana, S. Kose, M. Matsubae, T. Sekimoto, Y. Shimonishi, and Y. Yoneda. 1995b. In vivo evidence for involvement of a 58 kDa component of nuclear pore-tageting complex in nuclear protein import. EMBO (Eur. Mol. Biol. Organ.) J. 14:3617-3626.
26. Kadowaki, T., S. Chen, M. Hitomi, E. Jacobs, C. Kumagai, S. Liang, R. Schneller, D. Singleton, J. Wisniewska, and A.M. Tartakoff. 1994. Isolation and characterization of Saccharomyces cerevisiae mRNA transport-defective (mtr) mutants. J. Cell Biol. 126:649-659.
27. 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.
28. Kraemer, D.M., and G. Blobel. 1997. mRNA binding protein mrnp 41 localizes to both nucleus and cytoplasm. Proc. Natl. Acad. Sci. USA. 94:9119-9124.
29. Kraemer, D.M., C. Strambio-de-Castillia, G. Blobel, and M.P. Rout. 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.
30. Kutay, U., E. Izaurralde, F.R. Bischoff, I.W. Mattaj, and D. Görlich. 1997a. Dominant-negative mutants of importin-β block multiple pathways of import and export through the nuclear pore complex. EMBO (Eur. Mol. Biol. Organ.) J. 16:1153-1163.
31. Kutay, U., F.R. Bischoff, S. Kostka, R. Kraft, and D. Görlich. 1997b. Export of importin α from the nucleus is mediated by a specific nuclear transport factor. Cell. 90:1061-1071.
32. Lee, M.S., M. Henry, and P.A. Silver. 1996. A protein that shuttles between the nucleus and the cytoplasm is an important mediator of RNA export. Genes Dev. 10:1233-1246.
33. Loeb, J.D., G. Schlenstedt, D. Pellman, D. Kornitzer, P.A. Silver, and G.R. Fink. 1995. The yeast nuclear import receptor is required for mitosis. Proc. Natl. Acad. Sci. USA. 92:7647-7651.
34. 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 transport factor. J. Cell Biol. 123: 1649-1659.
35. Michael, W.M., P.S. Eder, and G. Dreyfuss. 1997. The K nuclear shuttling domain: a novel signal for nuclear import and nuclear export in the hnRNP K protein. EMBO (Eur. Mol. Biol. Organ.) J. 16:3587-3598.
36. Moore, M.S., and G. Blobel. 1993. The GTP-binding protein Ran/TC4 is required for protein import into the nucleus. Nature. 365:661-663.
37. 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.
38. Moroianu, J., G. Blobel, and A. Radu. 1995a. Previously identified protein of uncertain function is karyopherin α and together with karyopherin β docks import substrate at the nuclear pore complex. Proc. Natl. Acad. Sci. USA. 92: 2008-2011.
39. 2 bind nuclear localization signal and β interacts with peptide repeat-containing nucleoporins. Proc. Natl. Acad. Sci. USA. 92:6532-6536.
40. Moroianu, J., G. Blobel, and A. Radu. 1996. Nuclear protein import: Ran-GTP dissociates the karyopherin α/β heterodimer by displacing α from an over-lapping binding site on β. Proc Natl. Acad. Sci. USA. 93:7059-7062.
41. Nakielny, S., U. Fischer, W.M. Michael, and G. Dreyfuss. 1997. RNA transport. Annu. Rev. Neurosci. 20:269-301.
42. Nehrbass, U., and G. Blobel. 1996. Role of the nuclear transport factor p10 in nuclear import. Science. 272:120-122.
43. Nigg, E.A. 1997. Nucleocytoplasmic transport: signals, mechanisms and regulation. Nature. 386:779-787.
44. 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.
45. Piñol-Roma, S., and G. Dreyfuss. 1992. Shuttling of pre-mRNA binding proteins between nucleus and cytoplasm. Nature. 355:730-732.
46. Pollard, V.W., W.M. Michael, S. Nakielny, M.C. Siomi, F. Wang, and G. Dreyfuss. 1996. A novel receptor-mediated nuclear protein import pathway. Cell. 86:985-994.
47. Radu, A., G. Blobel, and M.S. Moore. 1995a. 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.
48. Radu, A., M.S. Moore, and G. Blobel. 1995b. The peptide repeat domain of nucleoporin Nup98 functions as a docking site in transport across the nuclear pore complex. Cell. 81:215-222.
49. 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.
50. Rout, M.P., G. Blobel, and J.D. Aitchison. 1997. A distinct nuclear import pathway used by ribosomal proteins. Cell. 89:715-725.
51. Russell, I.D., and D. Tollervey. 1992. NOP3 is an essential yeast protein which is required for pre-rRNA processing. J. Cell Biol. 119:737-747.
52. Schneiter, R., T. Kadowaki, and A.M. Tartakoff. 1995. mRNA transport in yeast: time to reinvestigate the functions of the nucleolus. Mol. Biol. Cell. 6:357-370.
53. Schneiter, R.T., M. Hitomi, A.S. Ivessa, E.V. Fasch, S.D. Kohlwein, and A.M. Tartakoff. 1996. A yeast acetyl coenzyme A carboxylase mutant links very-long-chain fatty acid synthesis to the structure and function of the nuclear membrane-pore complex. Mol. Cell Biol. 16:7161-7172.
54. Sherman, F., G.R. Fink, and J.B. Hicks. 1986. Methods in Yeast Genetics. Cold Spring Harbor Press, Cold Spring Harbor, NY.
55. Shulga, N., P. Roberts, Z. Gu, L. Spitz, M.M. Tabb, M. Nomura, and D.S. Goldfarb. 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.
56. Singleton, D.R., S. Chen, M. Hitomi, C. Kumagai, and A.M. Tartakoff. 1995. A yeast protein that bidirectionally affects nucleocytoplasmic transport. J. Cell Sci. 108:265-272.
57. Stade, K., C.S. Ford, C. Guthrie, and K. Weis. 1997. Exporlin 1 (Crm1) is an essential nuclear export factor. Cell. 90:1041-1050.
58. Visa, N., A.T. Alzhanova-Ericsson, X. Sun, E. Kiseleva, B. Bjorkroth, T. Wurtz, and B. Daneholt. 1996. A pre-mRNA-binding protein accompanies the RNA from the gene through nuclear pores and into polysomes. Cell. 84: 253-264.
59. Wente, S.R., M.P. Rout, and G. Blobel. 1992. A new family of yeast nuclear pore complex proteins. J. Cell Biol. 119:705-723.
60. Wilson, S.M., K.V. Datar, M.R. Paddy, J.R. Swedlow, and M. Swanson. 1994. Characterization of nuclear polyadenylated RNA-binding proteins in Saccharomyces cerevisiae. J. Cell Biol. 127:1173-1184.
61. Wolff, B., J. Sanglier, and Y. Wang. 1997. Leptomycin B is an inhibitor of nuclear export: Inhibition of nucleo-cytoplasmic translocation of the human immunodeficiency virus type 1 (HIV-1) Rev protein and Rev-dependent mRNA. Chem. Biol. 4:139-147.
62. Wong, D.H., A.H. Corbett, H.M. Kent, M. Stewart, and P.A. Silver. 1997. Interaction between the small GTPase Ran/Gsp1p and Ntf2p is required for nuclear transport. Mol. Cell. Biol. 17:3755-3767.