Assembly and preferential localization of Nup116p on the cytoplasmic face of the nuclear pore complex by interaction with Nup82p

Molecular and Cellular Biology

Volumn 20, Issue 15, 2000, Pages 5736-5748

  Ho, Albert K ^a   Shen, Tian Xiang ^a   Ryan, Kathryn J ^a   Kiseleva, Elena ^b,c   Levy, Marilyn Aach ^a   Allen, Terence D ^b   Wente, Susan R ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b CHRISTIE HOSPITAL   (United Kingdom)

^c INSTITUTE OF CYTOLOGY AND GENETICS   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

NUCLEOPROTEIN;

ARTICLE; COMPLEX FORMATION; IMMUNOPRECIPITATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE;

CELL NUCLEUS; CYTOPLASM; FLUORESCENT ANTIBODY TECHNIQUE; FUNGAL PROTEINS; GREEN FLUORESCENT PROTEINS; LUMINESCENT PROTEINS; MEMBRANE PROTEINS; MUTATION; NUCLEAR PORE COMPLEX PROTEINS; NUCLEAR PROTEINS; RECOMBINANT PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TEMPERATURE; TWO-HYBRID SYSTEM TECHNIQUES;

SACCHAROMYCES CEREVISIAE;

EID: 0033942158     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.20.15.5736-5748.2000     Document Type: Article

References (70)

1. Aitchison, J. D., G. Blobel, and M. P. Rout. 1996. Kap104p: a karyopherin involved in nuclear transport of messenger RNA binding proteins. Science 274:624-627.
2. Akey, C. W. 1995. Structural plasticity of the nuclear pore complex. J. Mol. Biol. 248:273-293.
3. Akey, C. W., and M. Radermacher. 1993. Architecture of the Xenopus nuclear pore complex revealed by three-dimensional cryo-electron microscopy. J. Cell Biol. 122:1-19.
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 export factor Gle2p. EMBO J. 17:1107-1119.
5. Bartel, P. L., and S. Fields. 1995. Analyzing protein-protein interactions using two-hybrid system. Methods Enzymol. 254:241-263.
6. Belgareh, N., C. Snay-Hodge, F. Pasteau, S. Dagher, C. N. Cole, and V. Doye. 1998. Functional characterization of a Nup159p-containing nuclear pore subcomplex. Mol. Biol. Cell 9:3475-3492.
7. Breeden, L., and K. Nasmyth. 1985. Regulation of the yeast HO gene. Cold Spring Harbor Symp. Quant. Biol. 50:643-650.
8. Bucci, M., and S. R. Wente. 1998. A novel fluorescence-based genetic strategy identifies mutants of Saccharomyces cerevisiae defective for nuclear pore complex assembly. Mol. Biol. Cell 9:2439-2461.
9. Dabauvalle, M. C., K. Loos, and U. Scheer. 1990. Identification of a soluble precursor complex essential for nuclear pore assembly in vitro. Chromosoma 100:56-66.
10. Doye, V., and E. Hurt. 1997. From nucleoporins to nuclear pore complexes. Curr. Opin. Cell Biol. 9:401-411.
11. Emtage, J. L. T., M. Bucci, J. L. Watkins, and S. R. Wente. 1997. Defining the essential structural regions of the nucleoporin Nup145p. J. Cell Sci. 110: 911-925.
12. Fabre, E., W. C. Boelens, C. Wimmer, I. W. 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.
13. Fahrenkrog, B., E. C. Hurt, U. Aebi, and N. Pante. 1998 Molecular architecture of the yeast nuclear pore complex: localization of Nsp1p complexes. J. Cell Biol. 143:577-588.
14. 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.
15. Fontoura, B. M. A., G. Blobel, and M. J. Matunis. 1999. A conserved biogenesis pathway for nucleoporins: proteolytic processing of a 186-kilodalton precursor generates Nup98 and the novel nucleoporin, Nup96. J. Cell Biol. 144:1097-1112.
16. Goldberg, M. W., and T. D. Allen. 1992. High resolution scanning electron microscopy of the nuclear envelope: demonstration of a new, regular, fibrous lattice attached to the baskets of the nucleoplasmic face of the nuclear pores. J. Cell Biol. 119:1429-1440.
17. Goldberg, M. W., and T. D. Allen. 1996. The nuclear pore complex and lamina: three-dimensional structures and interactions determined by field emission in-lens scanning electron microscopy. J. Mol. Biol. 257:848-865.
18. Goldberg, M. W., J. J. Blow, and T. D. Allen. 1992. The use of field emission in-lens scanning electron microscopy to study the steps of assembly of the nuclear envelope in vitro. J. Struct. Biol. 108:257-268.
19. Goldberg, M. W., C. Wiese, T. D. Allen, and K. L. Wilson. 1997. Dimples, pores, star-rings, and thin rings on growing nuclear envelopes: evidence for structural intermediates in nuclear pore complex assembly. J. Cell Sci. 110:409-420.
20. Gorsch, L. C., T. C. Dockendorff, and C. N. Cole. 1995. A conditional allele of the novel repeat-containing yeast nucleoporin R4T7/NUP159 causes both rapid cessation of mRNA export and reversible clustering of nuclear pore complexes. J. Cell Biol. 129:939-955.
21. Grandi, P., T. Dang, N. Pane, A. Shevchenko, M. Mann, D. Forbes, and E. Hurt. 1997. Nup93, a vertebrate homologue of yeast Nic96p, forms a complex with a novel 205-kDa protein and is required for correct nuclear pore assembly. Mol. Biol. Cell 8:2017-2038.
22. Grandi, P., V. Doye, and E. C. Hurt. 1993. Purification of NSP1 reveals complex formation with 'GLFG' nucleoporins and a novel nuclear pore protein NIC96. EMBO J. 12:3061-3071.
23. Grandi, P., S. Emig, C. Weise, F. Hucho, T. Pohl, and E. C. Hurt. 1995. A novel nuclear pore protein Nup82p which specifically binds to a fraction of Nsp1p. J. Cell Biol. 130:1263-1273.
24. 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 J. 14:76-87.
25. Guan, T. L., S. Muller, G. Klier, N. Pante, J. M. Blevitt, M. Haner, B. Paschal, U. Aebi, and L. Gerace. 1995. Structural analysis of the p62 complex, an assembly of α-linked glycoproteins that localizes near the central gated channel of the nuclear pore complex. Mol. Biol. Cell 6:1591-1603.
26. Haney, P. M., M. A. Levy, M. S. Strube, and M. Mueckler. 1995. Insulin-sensitive targeting of the GLUT4 glucose transporter in L6 myoblasts is conferred by its COOH-terminal cytoplasmic tail. J. Cell Biol. 129:641-658.
27. Hinshaw, J. E., B. O. Carragher, and R. A. Milligan. 1992. Architecture and design of the nuclear pore complex. Cell 69:1133-1141.
28. Ho, A. K., G. A. Raczniak, E. B. Ives, and S. R. Wente. 1998. The integral membrane protein Snl1p is genetically linked to yeast nuclear pore complex function. Mol. Biol. Cell 9:355-373.
29. Hodge, C. A., H. V. Colot, P. Stafford, and C. N. Cole. 1999. Rat8p/Dbp5p is a shuttling transport factor that interacts with Rat7p/Nup159p and Gle1p and suppresses the mRNA export defect of xpol-1 cells. EMBO J. 18:5778-5788.
30. Hu, T., T. Guan, and L. Gerace. 1996. Molecular and functional characterization of the p62 complex, an assembly of nuclear pore complex glycoproteins. J. Cell Biol. 134:589-601.
31. + RNA export. J. Cell Biol. 130:1275-1281.
32. Hurwitz, M. E., C. Strambio-de-Castillia, and G. Blobel. 1998. Two yeast nuclear pore complex proteins involved in mRNA export form a cytoplasmically oriented subcomplex. Proc. Natl. Acad. Sci. USA 95:11241-11245.
33. Iovine, M. K., J. L. Watkins, and S. R. Wente. 1995. The GLFG repetitive region of the nucleoporin Nup116p interacts with Kap95p, an essential yeast nuclear import factor. J. Cell Biol. 131:1699-1713.
34. Iovine, M. K., and S. R. Wente. 1997. A nuclear export signal in Kap95p is required for both recycling the import factor and interaction with the nucleoporin GLFG repeat regions of Nup116p and Nup100p. J. Cell Biol. 137:797-811.
35. Ito, H., Y. Fukuda, K. Murata, and A. Kimura. 1983. Transformation of intact yeast cells treated with alkali cations. J. Bacteriol. 153:163-168.
36. James, P., J. Halladay, and E. A. Craig. 1996. Genomic libraries and a host strain designed for highly efficient two-hybrid selection in yeast. Genetics 144:1425-1436.
37. Kenna, M. A., J. G. Petranka, J. L. Reilly, and L. I. Davis. 1996. Yeast Nle3p/Nup170p is required for normal stoichiometry of FG nucleoporins within the nuclear pore complex. Mol. Cell. Biol. 16:2025-2036.
38. Kiseleva, 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.
39. 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.
40. Macaulay, C., E. Meier, and D. J. Forbes. 1995. Differential mitotic phosphorylation of proteins of the nuclear pore complex. J. Biol. Chem. 270:254-262.
41. Marelli, M., J. D. Aitchison, and R. W. Wozniak. 1998. Specific binding of the karyopherin Kap121p to a subunit of the nuclear pore complex containing Nup53p, Nup59p, and Nup170p. J. Cell Biol. 143:1813-1830.
42. Ohno, M., M. Fornerod, and I. W. Mattaj. 1998. Nucleocytoplasmic transport: the last 200 nanometers. Cell 92:327-336.
43. Powers, M. A., C. Macaulay, F. R. 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.
44. Pritchard, C. E. J., M. Fornerod, L. H. Kasper, and J. M. A. van Deursen. 1999. RAE1 is a shuttling mRNA export factor that binds to a GLEBS-like NUP98 motif at the nuclear pore complex through multiple domains. J. Cell Biol. 145:237-253.
45. Radu, A., M. S. Moore, and G. Blobel. 1995. The peptide repeat domain of nucleoporin Nup98 functions as a docking site in transport across the nuclear pore complex. Cell 81:215-222.
46. Reichelt, R., A. Holzenburg, E. J. Buhle, M. Jarnik, A. Engel, and U. Aebi. 1990. Correlation between structure and mass distribution of the nuclear pore complex and of distinct pore complex components. J. Cell Biol. 110:883-894.
47. Ris, H. 1991. The three dimensional structure of the nuclear pore complex as seen by high voltage electron microscopy and high resolution low voltage scanning electron microscopy. EMSA Bull. 21:54-56.
48. Rout, M. P., J. D. Aitchison, A. Suprapto, K. Hjertaas, Y. Zhao, and B. T. Chait. 2000. The yeast nuclear pore complex: composition, architecture, and transport mechanism. J. Cell Biol. 148:635-651.
49. Rout, M. P., and G. Blobel. 1993. Isolation of the yeast nuclear pore complex. J. Cell Biol. 123:771-783.
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. Rozijn, T. H., and G. J. M. Tonino. 1964. Studies on the yeast nucleus. I. The isolation of nuclei. Biochim. Biophys. Acta 91:105-112.
52. Ryan, K. J., and S. R. Wente. 2000. The nuclear pore complex: a protein machine bridging the nucleus and cytoplasm. Curr. Opin. Cell Biol. 12:361-371.
53. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
54. Schlaich, N. L., M. Haner, A. Lustig, U. Aebi, and E. C. Hurt. 1997. In vitro reconstitution of a heterotrimeric nucleoporin complex consisting of recombinant Nsp1p, Nup49p, and Nup57p. Mol. Biol. Cell 8:33-46.
55. Schmitt, C., C. Von Kobbe, A. Bachi, N. Pante, J. P. Rodrigues, C. Boscheron, G. Rigaut, M. Wilm, B. Seraphin, M. Carmo-Fonseca, and E. Izaurralde. 1999. Dbp5, a DEAD-hox protein required for mRNA export, is recruited to the cytoplasmic fibrils of nuclear pore complex via a conserved interaction with CAN/Nup159p. EMBO J. 18:4332-4347.
56. Seedorf, M., M. Damelin, J. Kahana, T. Taura, and P. A. Silver. 1999. Interactions between a nuclear transporter and a subset of nuclear pore complex proteins depend on Ran GTPase. Mol. Cell. Biol. 19:1547-1557.
57. Sherman, F., G. R. Fink, and J. B. Hicks. 1986. Methods in yeast genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
58. Siniossoglou, S., C. Wimmer, M. Rieger, V. Doye, H. Tekotte, C. Weise, S. Emig, A. Segref, and E. C. Hurt. 1996. A novel complex of nucleoporins, which includes Sec13p and a Sec13p homolog, is essential for normal nuclear pores. Cell 84:265-275.
59. 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 J. 17:2663-2676.
60. Stoffler, D., B. Fahrenkrog, and U. Aebi. 1999. The nuclear pore complex: from molecular architecture to functional dynamics. Curr. Opin. Cell Biol. 11:391-401.
61. Strambio de Castillia, C., G. Blobel, and M. P. Rout. 1995. Isolation and characterization of nuclear envelopes from the yeast Saccharomyces. J. Cell Biol. 131:19-31.
62. Tseng, S. S.-I., P. L. Weaver, M. Hitomi, A. M. Tartakoff, and T.-H. Chang. 1998. Dbp5p, a cytosolic RNA helicase, is required for poly(A)+ RNA export. EMBO J. 17:2652-2662.
63. Wente, S. R., and G. Blobel. 1994. NUP145 encodes a novel yeast glycine-leucine-phenylalanine-glycine (GLFG) nucleoporin required for nuclear envelope structure. J. Cell Biol. 125:955-969.
64. 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.
65. Wente, S. R., S. M. Gasser, and A. J. Caplan. 1997. The nucleus and nucleocytoplasmic transport in Saccharomyces cerevisiae, p. 471-546. In J. R. Broach, E. Jones, and J. Pringle (ed.). The molecular and cellular biology of the yeast Saccharomyces, vol. 3. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
66. 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.
67. Wimmer, C., V. Doye, P. Grandi, U. Nehrbass, and E. C. Hurt. 1992. A new subclass of nucleoporins that functionally interact with nuclear pore protein NSP1. EMBO J. 11:5051-5061.
68. Wozniak, R. W., M. P. Rout, and J. D. Aitchison. 1998. Karyopherins and kissing cousins. Trend. Cell Biol. 8:184-188.
69. Yang, Q., M. P. Rout, and C. W. Akey. 1998. Three-dimensional architecture of the isolated yeast nuclear pore complex: functional and evolutionary implications. Mol. Cell 1:223-234.
70. Zolotukhin, A. S., and B. K. Felber. 1999. Nucleoporins Nup98 and Nup214 participate in nuclear export of human immunodeficiency virus type 1 Rev. J. Virol. 73:120-127.