The vertebrate GLFG nucleoporin, Nup98, is an essential component of multiple RNA export pathways

Journal of Cell Biology

Volumn 136, Issue 2, 1997, Pages 241-250

  Powers, Maureen A ^a   Forbes, Douglass J ^a   Dahlberg, James E ^b   Lund, Elsebet ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NUCLEOPORIN; POLYCLONAL ANTIBODY;

ANIMAL CELL; ARTICLE; CELL COMPOSITION; CELL NUCLEUS MEMBRANE; CELL VIABILITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN TARGETING; PROTEIN TRANSPORT; RNA SYNTHESIS; VERTEBRATE; XENOPUS LAEVIS;

ANIMALS; ANTIBODIES; BIOLOGICAL TRANSPORT; CELL NUCLEUS; MEMBRANE PROTEINS; NUCLEAR PORE COMPLEX PROTEINS; NUCLEAR PROTEINS; OOCYTES; PRECIPITIN TESTS; RNA; RNA CAPS; RNA, MESSENGER; RNA, RIBOSOMAL, 18S; RNA, RIBOSOMAL, 28S; RNA, RIBOSOMAL, 5S; RNA, SMALL NUCLEAR; RNA, TRANSFER; XENOPUS LAEVIS;

ANIMALIA; VERTEBRATA; XENOPUS LAEVIS;

EID: 0031046477     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.136.2.241     Document Type: Article

References (79)

1. Adolph, K.W., S.M. Cheng, and U.K. Laemmli. 1977. Role of nonhistone proteins in metaphase chomosome structure. Cell. 12:805-816.
2. 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.
3. Bataillé. N., T. Heiser, and H.M. Fried. 1990. Cytoplasmic transport of ribosomal subunits microinjected into the Xenopus laevis oocyte nucleus: a generalized, facilitated process. J. Cell Biol. 111:1571-1582.
4. Boelens, W.C., I. Palacios, and I.W. Mattaj. 1995. Nuclear retention of RNA as a mechanism for localization. RNA. 1:273-283.
5. Cheng, Y., J.E. Dahlberg, and E. Lund. 1995. Diverse effects of the guanine nucleotide exchange factor RCC1 on RNA transport. Science (Wash. DC). 267:1807-1810.
6. Cordes, V.C., S. Reidenbach, A. Kohler, N. Stuurman, R. van Driel, and W.W. Franke. 1993. Intranuclear filaments containing a nuclear pore complex protein. J. Cell Biol. 123(6):1333-1344.
7. Dabauvalle, M.C., and W.W. Franke. 1982. Karyophilic proteins: polypeptides synthesized in vitro accumulate in the nucleus on microinjection into the cytoplasm of amphibian oocytes. Proc. Natl. Acad. Sci. USA. 79:5302-5306.
8. Dahauvalle, M.C., R. Benavente, and N. Chaly. 1988. Monoclonal antibodies to a Mr 68,000 pore complex glycoprotein interfere with nuclear protein uptake in Xenopus oocytes. Chromosoma (Berl.). 97:193-197.
9. Dabauvalle, M.C., B. Schulz, U. Scheer, and R. Peters. 1988. Inhibition of nuclear accumulation of karyophilic proteins in living cells by microinjection of the lectin wheat germ agglutinin. Exp. Cell Res. 174:291-296.
10. Dahauvalle, M.C., K. Loos, and U. Scheer. 1990. Identification of a soluble precursor complex essential for nuclear pore assembly in vitro. Chromosoma (Berl.). 100:56-66.
11. Davis, L. 1995. The nuclear pore complex. Annu. Rev. Biochem. 64:865-896.
12. Doye, V., and E.G. Hurt. 1995. Genetic approaches to nuclear pore structure and function. Trends Genet. 11:235-241.
13. Fahre, E., and E.G. Hurt. 1994. Nuclear transport. Curr. Opin. Cell Biol. 6:335-342.
14. Fabre, E., W.C. Boelens, C. Wimmer, I. Mattaj, and E.C. Hurt. 1994. Nup145p is required for nuclear export of mRNA and binds homopolymeric RNA in vitro via a novel conserved motif. Cell. 78:275-289.
15. Featherstone, C., M.K. Darby, and L. Gerace. 1988. A monoclonal antibody against the nuclear pore complex inhibits nucleocytoplasmic transport of protein and RNA in vivo. J. Cell Biol. 107:1289-1297.
16. Finlay, D.R., and D.J. Forbes. 1990. Reconstitution of biochemically altered nuclear pores: transport can be eliminated and restored. Cell. 60:17-29.
17. Finlay, D.R., D.D. Newmeyer, T.M. Price, and D.J. Forbes. 1987. Inhibition of in vitro nuclear transport by a lectin that binds to nuclear pores. J. Cell Biol. 104:189-200.
18. Finlay, D.R., E. Meier, P. Bradley, J. Horecka, and D.J. Forbes. 1991. A complex of nuclear pore proteins required for pore function. J. Cell Biol. 114:169-183.
19. Fischer, U., E. Darzynkiewicz, S.M. Tahara, N.A. Dathan, R. Lührmann, and I.W. Mattaj. 1991. Diversity in the signals required for nuclear accumulation of U snRNPs and variety in the pathways of nuclear transport. J. Cell Biol. 113:705-714.
20. 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 ex- port pathway used by specific cellular RNAs. Cell. 82:475-483.
21. Forbes, D.J. 1992. Structure and function of the nuclear pore complex. Annu. Rev. Cell Biol. 8:495-527.
22. FridelJ. R.A., U. Fischer, R. Luhrmann, B.E. Meyer, J.L. Meinkoth, M.H. Malim, and B.R. Cullen. 1996. Amphibian transcription factor IIIA proteins contain a sequence element functionally equivalent to the nuclear export signal of human immunodeficiency virus type 1 Rev. Proc. Natl. Acad. Sci. USA. 93:2936-2940.
23. Görlich. D., and I.W. Mattaj. 1996. Protein kinesis: Nucleocytoplasmic transport. Science (Wash. DC). 271:1513-1518.
24. Görlich, D., F. Vogel, A.D. Mills, E. Hartmann, and R.A. Laskey. 1995. Distinct functions for the two importin subunits in nuclear protein import. Nature (Lond.). 377:246-248.
25. Gouilloud, E., and S.G. Clarkson. 1986. A dispersed tyrosine tRNA gene from Xenopus laevis with high transcriptional activity in vitro. J. Biol. Chem. 261:486-494.
26. Grandi, P., N. Schlaich, H. Tekotte, and E.C. Hurt. 1995. Functional interaction of Nic96p with a core nucleoporin complex consisting of Nsp1p, Nup49p, and a novel protein Nup57p. EMBO (Eur. Mol. Biol. Organ.) J. 14:76-87.
27. Grimm, C., E. Lund, and J.E. Dahlberg. 1997. EMBO (Eur. Mol. Biol. Organ.) J. In Press.
28. Guddat, U., A.H. Bakken, and T. Pieler. 1990. Protein-mediated nuclear export of RNA: 5S rRNA containing small RNPs in Xenopus oocytes. Cell. 60:619-628.
29. Gurdon, J.B. and M.P. Wickens. 1983. The use of Xenopus oocytes for the expression of cloned genes. Methods Enzymol. 101:370-386.
30. Hadjiolov, A.A. 1985. The Nucleolus and Ribosome Biogenesis. In Cell Biology Monographs. Springer-Verlag Inc., New York. 125:133-165.
31. Hamm, J., and I.W. Mattaj. 1990. Monomethylated cap structures facilitate RNA export from the nucleus. Celt. 63:109-118.
32. Hope, T., and R.J. Pomerantz. 1995. The human immunodeficiency virus type 1 Rev protein: a pivotal protein in the viral life cycle. Curr. Top. Microbiol. Immunol. 193:91-105.
33. Iovine, M.K., J.L. Watkins, and S.R. Wente. 1995. The GLFG repetitive region of the nucleoporin Nup1106 interacts with Kap95p, an essential yeast nuclear import factor. J. Cell Biol. 131:1699-1713.
34. Izaurralde, E., and I.W. Mattaj. 1992. Transport of RNA between nucleus and cytoplasm. Semin. Cell Biol. 3:279-288.
35. Izaurralde, E., and I.W. Mattaj. 1995. RNA export. Cell. 81:153-159.
36. Izaurralde, E., J. Stepinski, E. Darzynkiewicz, and I.W. Mattaj. 1992. A cap binding protein that may mediate nuclear export of RNA polymerase II-transcribed RNAs. J. Cell Biol. 118:1287-1295.
37. Izaurralde, E., J. Lewis, C. Gamberi, A. Jarmolowski, C. McGuigan, and I.W. Mattaj. 1995. A cap-binding protein complex mediating U snRNA export. Nature (Lond.). 376:709-712.
38. 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.
39. Kisleva, E., M.W. Goldberg, B. Daneholt, and T.D. Allen. 1996. RNP export is mediated by structural reorganization of the nuclear pore basket. J. Mol. Biol. 260:304-311.
40. Konarska, M.M., and P.A. Sharp. 1987. Interactions between small nuclear ribonucleoprotein particles in formation of spliceosomes. Cell. 49:763-774.
41. Kraemer, D., R.W. Wozniak, G. Blobel, and A. Radu. 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.
42. Lund, E., and J.E. Dahlberg. 1989. In vitro synthesis of vertebrate U1 snRNA. EMBO (Eur. Mol Biol. Organ.) J. 8:287-292.
43. Lund, E., and P.L. Paine. 1990. Nonaqueous isolation of transcriptionally active nuclei from Xenopus oocytes. Methods Enzymol. 181:36-43.
44. Macaulay, C., E. Meier, and D.J. Forbes. 1995. Differential mitotic phosphorylation of proteins of the nuclear pore complex. J. Biol. Chem. 207:254-262.
45. Mattaj, I.W. 1986. Cap trimethylation of U snRNA is cytoplasmic and dependent on U snRNP protein binding. Cell. 46:905-911.
46. Meier, E., B. Miller, and D.J. Forbes. 1995. Nuclear pore complex assembly studied with a biochemical assay for annulate lamellae formation. J. Cell Biol. 129:1459-1472.
47. Melchior, F., and L. Gerace. 1995. Mechanisms of nuclear protein import. Curr. Opin. Cell Biol. 7:310-318.
48. Melton, D.A., P.A. Krieg, M.R. Rebagliati, T. Maniatis, K. Zinn, and M.R. Green. 1984. Efficient in vitro synthesis of biologically active RNA and RNA hybridization probes from plasmids containing a bacteriophage SP6 promoter. Nucleic Adas Res. 12:7035-7056.
49. Michael, M.W., 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.
50. Michaud, N., and D.S. Goldfarb. 1991. Multiple pathways in nuclear transport: the import of U2 snRNP occurs by a novel kinetic pathway. J. Cell Biol. 112:215-223.
51. Miller, M.W., and J.A. Hanover. 1994. Functional nuclear pores reconstituted with β1-4 galactose-modified O-linked N-acetylglucosamine modified glycoproteins. J. Biol. Chem. 269:9289-9297.
52. Moore, M.S., and G. Blobel. 1994. A G protein involved in nucleocytoplasmic transport: the role of Ran. Trends Biochem. Sci. 19:211-216.
53. Moroianu, J., M. Hijikata, G. Blobel, and A. Radu. 1995. Mammalian karyo- pherin a1b and a2b heterodimers: a1 or a2 suhunit hinds nuclear localization signal and b subunit interacts with peptide repeat-containing nucleoporins, Proc. Natl. Acad. Sci. USA. 92:6532-6536.
54. Munns, T.W., M.K. Liszewski, J.T. Tellam, H.F. Sims, and R.E. Rhoads. 1982. Antibody-nucleic acid complexes. Immunospecific retention of globin messenger ribonucleic acid with antibodies specific for 7-methylguanosine. Biochemistry. 21:2922-2928.
55. Nehrbass, U., and G. Blobel. 1996. Role of the nuclear transport factor p10 in nuclear import. Science (Wash. DC). 272:120-122.
56. Neuman de Vegvar, H.E., and E. Dahlberg. 1990. Nucleocytoplasmic transport and processing of small nuclear RNA precursors. Mol. Cell. Biol. 10:3365-3375.
57. Pante, N., and U. Aebi. 1993. The nuclear pore complex. J. Cell Biol. 122:977-984.
58. Pasquinelli, A.E., J.E. Dahlberg, and E. Lund. 1995. Reverse 5′ caps in RNAs made in vitro by phage RNA polymerases. RNA. 1:957-967.
59. Peculis, B.A., and J.A. Sleitz. 1993. Disruption of U8 nucleolar snRNA inhibits 5.8S and 28S rRNA processing in the Xenopus oocyte. Cell. 73:1233-1245.
60. Pokrywka, N.J., and D.S. Goldfarb. 1995. Nuclear export pathways of tRNA and 40 S ribosomes include both common and specific intermediates. J. Biol. Chem. 270:3619-3624.
61. Powers, M.A., and D.J. Forbes. 1994. Cytosolic factors in nuclear import: what's importin? Cell. 79:931-934.
62. Powers, M.A., C. Macaulay, F. Masiarz, and D.J. Forbes. 1995. Reconstituted nuclei depleted of a vertebrate GLFG nuclear pore protein. p97, import but are defective in nuclear growth and replication. J. Cell Biol. 128:721-736.
63. 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.
64. Radu, A., M.S. Moore, and G. Blobel. 1995e. The peptide repeat domain of nucleoporin Nup98 functions as a docking site in transport across the nuclear pore complex. Cell. 81:215-222.
65. 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.
66. Rout, M.P., and S.R. Wente. 1994. Pores for thought: nuclear pote complex proteins. Trends Cell Biol. 4:357-365.
67. Sazer, S. 1996. The search for the primary function of the Ran GTPase continues. Trends Cell Biol. 6:81-85.
68. Schlensiedt, G., E. Hurt, V. Doye, and P.A. Silver. 1993. Reconstitution of nuclear protein transport with semi-intact yeast cells. J. Cell Biol. 123:785-798.
69. Simons, F.H., S.A. Rutjes, W.J. van Venrooij, and G.J. Pruijn. 1996. The interactions with Ro60 and La differentially affect nuclear export of hY1 RNA. RNA. 2:264-273.
70. Terns, M.P., and J.E. Dahlberg. 1994. Retention and 57prime; cap trimethylation of U3 snRNA in the nucleus. Science (Wash. DC). 264:959-961.
71. Terns, M.P., J.E. Dahlberg, and E. Lund. 1993a. Multiple cis-acting signals for export of pre-U1 snRNA from the nucleus. Genes Dev. 7:1898-1908.
72. Terns, M.P., E. Lund, and J.E. Dahlberg. 1993b. A pre-export U1 snRNP in Xenopus laevis oocyte nuclei. Nucleic Acids Res. 21:4569-4573.
73. Vankan, P., C. McGuigan, and I.W. Mattaj. 1990. Domains of U4 and U6 snRNAs required for snRNP assembly and splicing complementation in Xenopus oocytes. EMBO (Eur. Mol. Biol. Organ.) J. 9:3397-3404.
74. Visa, N., E. Izaurralde, J. Ferreira, B. Daneholt, and I.W. Mattaj. 1996. A nu clear CAP-binding complex binds balbiani ring pre-mRNA cotranscriptionally and accompanies the ribonucleoprotein particle during nuclear export J. Cell Biol. 133:5-14.
75. Wente, S.R., and G. Blobel. 1994. NUP145 encodes a novel yeast glycine-teucine-phenylalanine-glycine (GLFG) nucleoporin required for nuclear envelope structure. J Cell Biol. 125:955-969.
76. 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.
77. Wimmer, C., V. Doye, P. Grandi, U. Nehrbass, and E.G. Hurt. 1992. A new subclass of nucleoporins that functionally interact with nuclear pore protein NSP1. EM BO (Eur. Mol. Biol. Organ.). J. 11:5051-5061.
78. Wolffe, A.P., E. Jordan, and D.D. Brown. 1986. A bacteriophage RNA polymerase transcribes through a Xenopus 5S RNA gene transcription complex without disrupting it. Cell. 44:381-389.
79. Zasloff, M. 1983. tRNA transport from the nucleus in a eukaryotic cell: carrier-mediated translocation process. Proc. Natl. Acad. Sci. USA. 80:6436-6440.