RAE1 is a shuttling mRNA export factor that binds to a GLEBS-like NUP98 motif at the nuclear pore complex through multiple domains

Journal of Cell Biology

Volumn 145, Issue 2, 2000, Pages 237-253

  Pritchard, Colin E J ^a   Fornerod, Maarten ^b   Kasper, Lawryn H ^a   Van Deursen, Jan M A ^a,c  

^a ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^b EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^c MAYO CLINIC   (United States)

Author keywords

mRNA export; Nuclear pore complex; NUP98; RAE1; RNA polymerase II

Indexed keywords

MESSENGER RNA; RNA POLYMERASE II;

ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; ENZYME ACTIVATION; ENZYME ACTIVITY; GENE OVEREXPRESSION; GENETIC ANALYSIS; MESSENGER RNA SYNTHESIS; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; PROTEIN DOMAIN; RNA TRANSPORT; TANDEM REPEAT; XENOPUS LAEVIS;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; CELL LINE; CRICETINAE; CROSS-LINKING REAGENTS; DACTINOMYCIN; FEMALE; FUNGAL PROTEINS; HUMANS; MEMBRANE PROTEINS; MICE; MOLECULAR SEQUENCE DATA; NUCLEAR ENVELOPE; NUCLEAR MATRIX-ASSOCIATED PROTEINS; NUCLEAR PORE COMPLEX PROTEINS; NUCLEAR PROTEINS; NUCLEOCYTOPLASMIC TRANSPORT PROTEINS; OOCYTES; RECOMBINANT PROTEINS; REPETITIVE SEQUENCES, AMINO ACID; RNA POLYMERASE II; RNA, MESSENGER; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SCHIZOSACCHAROMYCES POMBE PROTEINS; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID; TRANSFECTION; XENOPUS LAEVIS;

ANIMALIA; MAMMALIA; SACCHAROMYCES CEREVISIAE; XENOPUS LAEVIS;

EID: 0344171991     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.145.2.237     Document Type: Article

References (59)

1. Amberg, D.C., A.L. Goldstein, and C.N. Cole. 1992. Isolation and characterization of RAT1: an essential gene of Saccharomyces cerevisiae required for the efficient nucleocytoplasmic trafficking of mRNA. Genes Dev. 6:1173-1189.
2. Arts, G.J., M. Fornerod, and I.W. Mattaj. 1998. Identification of a nuclear export receptor for tRNA. Curr. Biol. 8:305-314.
3. Audigier, Y. 1994. Assays for studying functional properties of in vitro translated Gs alpha subunit. Methods Enzymol. 237:239-254.
4. Bailer, S.M., S. Siniossoglou, A. Podtelejnikov, A. Hellwig, M. Mann, and E. Hurt. 1998. Nup116p and nup100p are interchangeable through a conserved motif which constitutes a docking site for the mRNA transport factor gle2p. EMBO (Eur. Mol. Biol. Organ.) J. 17:1107-1119.
5. Bastos, R., A. Lin, M. Enarson, and B. Burke. 1996. Targeting and function in mRNA export of nuclear pore complex protein Nup153. J. Cell Biol. 134: 1141-1156.
6. Bharathi, A., A. Ghosh, W.A. Whalen, J.H. Yoon, R. Pu, M. Dasso, and R. Dhar. 1997. The human RAE1 gene is a functional homologue of Schizosaccharomyces pombe rae1 gene involved in nuclear export of Poly(A)+ RNA. Gene. 198:251-258.
7. + RNA export and in the cytoskeleton. J. Biol. Chem. 270: 7411-7419.
8. Clapham, D.E., and E.J. Neer. 1997. G protein beta gamma subunits. Annu. Rev. Pharmacol. Toxicol. 37:167-203.
9. Cole, C.N., and C.M. Hammell. 1998. Nucleocytoplasmic transport: driving and directing transport. Curr. Biol. 8:R368-R372.
10. Doye, V., and E. Hurt. 1997. From nucleoporins to nuclear pore complexes. Curr. Opin. Cell Biol. 9:401-411.
11. Dreyfuss, G., M.J. Matunis, S. Piñol-Roma, and C.G. Burd. 1993. hnRNP proteins and the biogenesis of mRNA. Annu. Rev. Biochem. 62:289-321.
12. 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.
13. Fornerod, M., M. Ohno, M. Yoshida, and I.W. Mattaj. 1997a. CRM1 is an export receptor for leucine-rich nuclear export signals. Cell. 90:1051-1060.
14. Fornerod, M., J. van Deursen, S. van Baal, A. Reynolds, D. Davis, K.G. Murti, J. Fransen, and G. Grosveld. 1997b. 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.
15. Fukuda, M., S. Asano, T. Nakamura, M. Adachi, M. Yoshida, M. Yanagida, and E. Nishida. 1997. CRM1 is responsible for intracellular transport mediated by the nuclear export signal. Nature. 390:308-311.
16. Garcia-Higuera, I., J. Fenoglio, Y. Li, C. Lewis, M.P. Panchenko, O. Reiner, T.F. Smith, and E.J. Neer. 1996a. Folding of proteins with WD-repeats: comparison of six members of the WD-repeat superfamily to the G protein beta subunit. Biochemistry. 35:13985-13994.
17. Garcia-Higuera, I., C. Gaitatzes, T.F. Smith, and E.J. Neer. 1998. Folding a WD repeat propeller. Role of highly conserved aspartic acid residues in the G protein beta subunit and Sec 13. J. Biol. Chem. 273:9041-9049.
18. Garcia-Higuera, I., T.C. Thomas, F. Yi, and E.J. Neer. 1996b. Intersubunit surfaces in G protein alpha beta gamma heterotrimers. Analysis by cross-linking and mutagenesis of beta gamma. J. Biol. Chem. 271:528-535.
19. Görlich, D. 1997. Nuclear protein import. Curr. Opin. Cell Biol. 9:412-419.
20. Gruter, P., C. Tabernero, C. von Kobbe, C. Schmitt, C. Saavedra, A. Bachi, M. Wilm, B. Felber, and E. Izaurralde. 1998. TAP, the human homolog of Mex67p, mediates CTE-dependent RNA export from the nucleus. Mol. Cell. 1:649-659.
21. + RNA. J. Cell Biol. 126: 877-899.
22. Izaurralde, E., A. Jarmolowski, C. Beisel, I.W. Mattaj, G. Dreyfuss, and U. Fischer. 1997a. A role for the M9 transport signal of hnRNP A1 in mRNA nuclear export. J. Cell Biol. 137:27-35.
23. Izaurralde, E., U. Kutay, C. von Kobbe, I.W. Mattaj, and D. Görlich. 1997b. The asymmetric distribution of the constituents of the Ran system is essential for transport into and out of the nucleus. EMBO (Eur. Mol. Biol. Organ.) J. 16:6535-6547.
24. Izaurralde, E., J. Lewis, C. Gamberi, A. Jarmolowski, C. McGuigan, and I.W. Mattaj. 1995a. A cap-binding protein complex mediating U snRNA export. Nature. 376:709-712.
25. Izaurralde, E., and I.W. Mattaj. 1995. RNA export. Cell. 81:153-159.
26. Izaurralde, E., C. McGuigan, and I.W. Mattaj. 1995b. Nuclear localization of a cap-binding protein complex. Cold Spring Harbor Symp. Quant. Biol. 60: 669-675.
27. Jarmolowski, A., W.C. Boelens, E. Izaurralde, and I.W. Mattaj. 1994. Nuclear export of different classes of RNA is mediated by specific factors. J. Cell Biol. 124:627-635.
28. Kasper, L.H., P.K. Brindle, C.A. Schnabel, C.E.J. Pritchard, M.L. Cleary, and J.M.A. van Deursen. 1999. CREB binding protein interacts with nucleoporin-specific FG repeats that activate transcription and mediate NUP98-HOXA9 oncogenicity. Mol. Cell. Biol. 19:764-776.
29. Kraemer, D., and G. Blobel. 1997. mRNA binding protein mrnp 41 localizes to both nucleus and cytoplasm. Proc. Natl. Acad. Sci. USA. 94:9119-9124.
30. Kutay, U., G. Lipowsky, E. Izaurralde, F.R. Bischoff, P. Schwarzmaier, E. Hartmann, and D. Görlich. 1998. Identification of a tRNA specific nuclear export receptor. Mol. Cell. 1:359-369.
31. Li, Y., P.M. Sternweis, S. Charnecki, T.F. Smith, A.G. Gilman, E.J. Neer, and T. Kozasa. 1998. Sites for Galpha binding on the G protein beta subunit overlap with sites for regulation of phospholipase Cbeta and adenylyl cyclase. J. Biol. Chem. 273:16265-16272.
32. Mehlin, H., B. Daneholt, and U. Skoglund. 1995. Structural interaction between the nuclear pore complex and a specific translocating RNP particle. J. Cell Biol. 129: 1205-1216.
33. Michael, W.M., M. Choi, and G. Dreyfuss. 1995. A nuclear export signal in hnRNP A1: a signal-mediated, temperature-dependent nuclear protein export pathway. Cell. 83:415-422.
34. 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.
35. Misteli, T., and D.L. Spector. 1998. The cellular organization of gene expression. Curr. Opin. Cell Biol. 10:323-331.
36. Murphy, R., J.L. Walkins, and S.R. Wente. 1996. GLE2, a Saccharomyces cerevisiae homologue of the Schizosaccharomyces pombe export factor RAE1, is required for nuclear pore complex structure and function. Mol. Biol. Cell. 7:1921-1937.
37. Nakielny, S., and G. Dreyfuss. 1997. Nuclear export of proteins and RNAs. Curr. Opin. Cell Biol. 9:420-429.
38. Nakielny, S., U. Fischer, W.M. Michael, and G. Dreyfuss. 1997. RNA transport. Annu. Rev. Neurosci. 20:269-301.
39. Neer, E.J., B.M. Denker, T.C. Thomas, and C.J. Schmidt. 1994a. Analysis of G-protein alpha and beta gamma subunits by in vitro translation. Methods Enzymol. 237:226-239.
40. Neer, E.J., C.J. Schmidt, R. Nambudripad, and T.F. Smith. 1994b. The ancient regulatory-protein family of WD-repeat proteins. Nature. 371:297-300.
41. Neer, E.J., and T.F. Smith. 1996. G protein heterodimers: new structures propel new questions. Cell. 84:175-178.
42. Nigg, E.A. 1997. Nucleocytoplasmic transport: signals, mechanisms and regulation. Nature. 386:779-787.
43. Ohno, M., M. Fornerod, and I.W. Mattaj. 1998. Nucleocytoplasmic transport: the last 200 nanometers. Cell. 92:327-336.
44. Persons, D.A., J.A. Allay, E.R. Allay, R.J. Smeyne, R.A. Ashmun, B.P. Sorrentino, and A.W. Nienhuis. 1997. Retroviral-mediated transfer of the green fluorescent protein gene into murine hematopoietic cells facilitates scoring and selection of transduced progenitors in vitro and identification of genetically modified cells in vivo. Blood. 90:1777-1786.
45. Richards, S.A., K.L. Carey, and I.G. Macara. 1997. Requirement of guanosine triphosphate-bound ran for signal-mediated nuclear protein export. Science. 276:1842-1844.
46. Saavedra, C.A., C.M. Hammell, C.V. Heath, and C.N. Cole. 1997. Yeast heat shock mRNAs are exported through a distinct pathway defined by Rip1p. Genes Dev. 11:2845-2856.
47. + RNA and nuclear pores. EMBO (Eur. Mol. Biol. Organ.) J. 16: 3256-3271.
48. Snay-Hodge, C.A., H.V. Colot, A.L. Goldstein, and C.N. Cole. 1998. Dbp5p/ Rat8p is a yeast nuclear pore-associated DEAD-box protein essential for RNA export. EMBO (Eur. Mol. Biol. Organ.) J. 17:2663-2676.
49. Stade, K., C.S. Ford, C. Guthrie, and K. Weis. 1997. Exportin 1 (Crm1p) is an essential nuclear export factor. Cell. 90:1041-1050.
50. Stutz, F., J. Kantor, D. Zhang, T. McCarthy, M. Neville, and M. Rosbash. 1997. The yeast nucleoporin rip1p contributes to multiple export pathways with no essential role for its FG-repeat region. Genes Dev. 11:2857-2868.
51. Stutz, F., and M. Rosbash. 1998. Nuclear RNA export. Genes Dev. 12:3303-3319.
52. + RNA export. EMBO (Eur. Mol. Biol. Organ.) J. 17:2651-2662.
53. Ullman, K.S., M.A. Powers, and D.J. Forbes. 1997. Nuclear export receptors: from importin to exportin. Cell. 90:967-970.
54. van Deursen, J., J. Boer, L. Kasper, and G. Grosveld. 1996. G2 arrest and impaired nucleocytoplasmic transport in mouse embryos lacking the protooncogene CAN/Nup214. EMBO (Eur. Mol. Biol. Organ.) J. 15:5574-5583.
55. + RNA export. Proc. Natl. Acad. Sci. USA. 95:6779-6784.
56. Weis, K. 1998. Importins and exportins: how to get in and out of the nucleus. Trends Biochem. Sci. 23:185-189.
57. Wente, S.R., and G. Blobel. 1993. A temperature-sensitive NUP116 null mutant forms a nuclear envelope seal over the yeast nuclear pore complex thereby blocking nucleocytoplasmic traffic. J. Cell Biol. 123:275-284.
58. Whalen, W.A., A. Bharathi, D. Danielewicz, and R. Dhar. 1997. Advancement through mitosis requires rae1 gene function in fission yeast. Yeast. 13:1167-1179
59. Yi, F., B.M. Denker, and E.J. Neer. 1991. Structural and functional studies of cross-linked Go protein subunits. J. Biol. Chem. 266:3900-3906.