A novel fluorescence-based genetic strategy identifies mutants of Saccharomyces cerevisiae defective for nuclear pore complex assembly

Molecular Biology of the Cell

Volumn 9, Issue 9, 1998, Pages 2439-2461

  Bucci, Mirella ^a   Wente, Susan R ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL PROTEIN; GREEN FLUORESCENT PROTEIN; MEMBRANE PROTEIN; MUTANT PROTEIN;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL NUCLEUS MEMBRANE; CONTROLLED STUDY; FLUORESCENCE ACTIVATED CELL SORTER; FUNGUS MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; SACCHAROMYCES CEREVISIAE; TEMPERATURE SENSITIVE MUTANT;

FUNGI; SACCHAROMYCES CEREVISIAE;

EID: 0031688617     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.9.9.2439     Document Type: Article

References (82)

1. Aitchison, J.D., Blobel, G., and Rout, M.P. (1995). Nup120p: a yeast nucleoporin required for NPC distribution and mRNA transport. J. Cell Biol. 131, 1659-1675.
2. Akey, C.W. (1995). Structural plasticity of the nuclear pore complex. J. Mol. Biol. 248, 273-293.
3. Akey, C.W., and Radermacher, M. (1993). Architecture of the Xenopus nuclear pore complex revealed by three-dimensional cryo-electron microscopy. J. Cell Biol. 122, 1-19.
4. Baudin, A., Ozier, K.O., Denouel, A., Lacroute, F., and Cullin, C. (1993). A simple and efficient method for direct gene deletion in Saccharomyces cerevisiae. Nucleic Acids Res. 21, 3329-3330.
5. Bogerd, A.M., Hoffman, J.A., Amberg, D.C., Fink, G.R., and Davis, L.I. (1994). nup1 mutants exhibit pleiotropic defects in nuclear pore complex function. J. Cell Biol. 127, 319-332.
6. Boman, A.L., Delannoy, M.R., and Wilson, K.L. (1992a). GTP hydrolysis is required for vesicle fusion during nuclear envelope assembly in vitro. J. Cell Biol. 116, 281-294.
7. Boman, A.L., Taylor, T.C., Melancon, P., and Wilson, K.L. (1992b). A role for ADP-ribosylation factor in nuclear vesicle dynamics. Nature 358, 512-514.
8. Bucci, M., and Wente, S.R. (1997). In vivo dynamics of nuclear pore complexes in yeast. J. Cell Biol. 136, 1185-1199.
9. Burke, B., and Gerace, L. (1986). A cell free system to study reassembly of the nuclear envelope at the end of mitosis. Cell 44, 639-652.
10. Christianson, T.W., Sikorski, R.S., Dante, M., Shero, J.H., and Hieter, P. (1992). Multifunctional yeast high-copy-number shuttle vectors. Gene 110, 119-122.
11. Corbett, A.H., and Silver, P.A. (1997). Nucleocytoplasmic transport of macromolecules. Microbiol. Mol. Biol. Rev. 61, 193-211.
12. Dabauvalle, M.C., Loos, K., and Scheer, U. (1990). Identification of a soluble precursor complex essential for nuclear pore assembly in vitro. Chromosoma 100, 56-66.
13. Davis, L.I. (1995). The nuclear pore complex. Annu. Rev. Biochem. 64, 865-896.
14. Doye, V., and Hurt, E. (1997). From nucleoporins to nuclear pore complexes. Curr. Opin. Cell Biol. 9, 401-411.
15. + RNA transport and nuclear pore distribution. EMBO J. 13, 6062-6075.
16. Emtage, J.L.T., Bucci, M., Watkins, J.L., and Wente, S.R. (1997). Defining the essential structural regions of the nucleoporin Nup145p. J. Cell Sci. 110, 911-925.
17. Fabre, E., Boelens, W.C., Wimmer, C., Mattaj, I.W., and Hurt, E.C. (1994). Nup145p is required for nuclear export of mRNA and binds homopolymeric RNA in vitro via a novel conserved motif. Cell 78, 275-289.
18. Finlay, D.R., and Forbes, D.J. (1990). Reconstitution of biochemically altered nuclear pores: transport can be eliminated and restored. Cell 60, 17-29.
19. Finlay, D.R., Meier, E., Bradley, P., Horecka, J., and Forbes, D.J. (1991). A complex of nuclear pore proteins required for pore function. J. Cell Biol. 114, 169-183.
20. Gerace, L., Ottaviano, Y., and Kondor-Koch, C. (1982). Identification of a major polypeptide of the nuclear pore complex. J. Cell Biol. 95, 826-837.
21. Goldberg, M.W., and Allen, T.D. (1995). Structural and functional organization of the nuclear envelope. Curr. Opin. Cell Biol. 7, 301-309.
22. Goldberg, M.W., Wiese, C., Allen, T.D., and Wilson, K.L. (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.
23. Goldstein, A.L., Snay, C.A., Heath, C.V., and Cole, C.N. (1996). Pleiotropic nuclear defects associated with a conditional allele of the novel nucleoporin Rat9p/Nup85p. Mol. Biol. Cell 7, 917-934.
24. Gorsch, L.C., Dockendorff, T.C., and Cole, C.N. (1995). A conditional allele of the novel repeat-containing yeast nucleoporin RAT7/NUP159 causes both rapid cessation of mRNA export and reversible clustering of nuclear pore complexes. J. Cell Biol. 129, 939-955.
25. Grandi, P., Dang, T., Pane, N., Shevchenko, A., Mann, M., Forbes, D., and Hurt, E. (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.
26. Grandi, P., Emig, S., Weise, C., Hucho, F., Pohl, T., and Hurt, E.C. (1995a). A novel nuclear pore protein Nup82p which specifically binds to a fraction of Nsp1p. J. Cell Biol. 130, 1263-1273.
27. Grandi, P., Schlaich, N., Tekotte, H., and Hurt, E.C. (1995b). Functional interaction of Nic96p with a core nucleoporin complex consisting of Nsp1p, Nup49p and a novel protein Nup57p. EMBO J. 14, 76-87.
28. Greber, U.F., Senior, A., and Gerace, L. (1990). A major glycoprotein of the nuclear pore complex is a membrane-spanning polypeptide with a large lumenal domain and a small cytoplasmic tail. EMBO J. 9, 1495-502.
29. Guarente, L. (1983). Yeast promoters and lacZ fusions designed to study expression of cloned genes in yeast. Methods Enzymol. 101, 181-191.
30. Guldener, U., Heck, S., Fielder, T., Beinhauer, J., and Hegemann, J.H. (1996). A new efficient gene disruption cassette for repeated use in budding yeast. Nucleic Acids Res. 24, 2519-2524.
31. Hallberg, E., Wozniak, R.W., and Blobel, G. (1993). An integral membrane protein of the pore membrane domain of the nuclear envelope contains a nucleoporin-like region. J. Cell Biol. 122, 513-21.
32. Hardy, C.F.J. (1996). OAF1, and essential ORC2 associated factor, plays a role in DNA replication. Mol. Cell. Biol. 16, 1832-1841.
33. + RNA associated with mutation of the Saccharomyces cerevisiae rat2/nup120 gene. J. Cell Biol. 131, 1677-1697.
34. Heim, R., and Tsien, R.Y. (1996). Engineering green fluorescent protein for improved brightness, longer wavelengths and fluorescence resonance energy transfer. Curr. Biol. 6, 178-182.
35. Hinshaw, J.E., Carragher, B.O., and Milligan, R.A. (1992). Architecture and design of the nuclear pore complex. Cell 69, 1133-1141.
36. Ho, A.K., Raczniak, G.A., Ives, E.B., and Wente, S.R. (1998). The integral membrane protein Snl1p is genetically linked to yeast nuclear pore complex function. Mol. Biol. Cell 9, 355-373.
37. Iovine, M.K., Watkins, J.L., and Wente, S.R. (1995). The GLFG repetitive region of the nucleoporin Nup116p interacts with Kap95p, an essential yeast nuclear import factor. J. Cell Biol. 131, 1699-1713.
38. Ito, H., Fukuda, Y., Murata, K., and Kimura, A. (1983). Transformation of intact yeast cells treated with alkali cations. J. Bacteriol. 153, 163-168.
39. Kenna, M.A., Petranka, J.G., Reilly, J.L., and Davis, L.I. (1996). Yeast Nle3/Nup170p is required for normal stoichiometry of FG nucleoporins within the nuclear pore complex. Mol. Cell. Biol. 16, 2025-2036.
40. Kraemer, D.M., Strambio-de-Castillia, C., Blobel, G., and Rout, M.P. (1995). The essential yeast nucleoporin NUP159 is located on the cytoplasmic side of the nuclear pore complex and serves in karyo-pherin-mediated binding of transport substrate. J. Biol. Chem. 270, 19017-19021.
41. Lenz-Bohme, B., Wismar, J., Fuchs, S., Reifegerste, R., Buchner, E., Betz, H., and Schmitt, B. (1997). Insertional mutation of the Drosophilia nuclear lamin Dmo gene results in defective nuclear envelopes, clustering of nuclear pore complexes, and accumulation of annulate lamellae. J. Cell Biol. 137, 1001-1016.
42. + RNA and constitutive clustering of nuclear pore complexes. Mol. Biol. Cell 6, 401-417.
43. Lohka, M.J., and Masui, Y. (1983). Formation in vitro of sperm pronuclei and mitotic chromosomes induced by amphibian ooplasmic components. Science 220, 719-721.
44. Macaulay, C., and Forbes, D.J. (1996). Assembly of the nuclear pore - biochemically distinct steps revealed with nem, gtp-gamma-s, and bapta. J. Cell Biol. 132, 5-20.
45. Miake-Lye, R., and Kirschner, M.W. (1985). Induction of early mitotic events in a cell-free system. Cell 41, 165-175.
46. Murphy, R., Watkins, J.L., and Wente, S.R. (1996). GLE2, a S. cerevisiae homologue of the S. pombe export factor RAE1, is required for nuclear pore complex structure and function. Mol. Biol. Cell 7, 1921-1937.
47. Murphy, R., and Wente, S. (1996). An RNA export mediator with an essential nuclear export signal. Nature 383, 357-360.
48. Mutvei, A., Dihlmann, S., Herth, W., and Hurt, E.C. (1992). NSP1 depletion in yeast affects nuclear pore formation and nuclear accumulation. Eur. J. Cell Biol. 59, 280-295.
49. Nehrbass, U., Fabre, E., Dihlmann, S., Herth, W., and Hurt, E.C. (1993). Analysis of nucleo-cytoplasmic transport in a thermosensitive mutant of nuclear pore protein NSP1. Eur. J. Cell Biol. 62, 1-12.
50. Nehrbass, U., Kern, H., Mutvei, A., Horstmann, H., Marshallsay, B., and Hurt, E.C. (1990). NSP1: a yeast nuclear envelope protein localized at the nuclear pores exerts its essential function by its carboxy-terminal domain. Cell 61, 979-89.
51. Newmeyer, D.D., and Forbes, D.J. (1990). A N-ethylmaleimide-sensitive cytosolic factor necessary for nuclear protein import: requirement in signal-mediated binding to the nuclear pore. J. Cell Biol. 110, 547-557.
52. Newport, J. (1987). Nuclear reconstitution in vitro: stages of assembly around protein-free DNA. Cell 48, 205-217.
53. Newport, J.W., and Dunphy, W. (1992). Characterization of the membrane binding and fusion events during nuclear envelope assembly using purified components. J. Cell Biol. 116, 295-306.
54. Pante, N., and Aebi, U. (1996). Molecular dissection of the nuclear pore complex. Crit. Rev. Biochem. Mol. Biol. 31, 153-199.
55. Pemberton, L.F., Rout, M.P., and Blobel, G. (1995). Disruption of the nucleoporin gene NUP133 results in clustering of nuclear pore complexes. Proc. Natl. Acad. Sci. USA 92, 1187-1191.
56. Pfaller, R., Smythe, C., and Newport, J.W. (1991). Assembly/disassembly of the nuclear envelope membrane: cell cycle-dependent binding of nuclear membrane vesicles to chromatin in vitro. Cell 65, 209-217.
57. 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.
58. Rout, M.P., and Blobel, G. (1993). Isolation of the yeast nuclear pore complex. J. Cell Biol. 123, 771-783.
59. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual, Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
60. Sanger, F., Nicklen, S., and Coulson, A.R. (1977). DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. USA 74, 5463-5467.
61. Schlaich, N.L., Haner, M., Lustig, A., Aebi, U., and Hurt, E.C. (1997). In vitro reconstitution of a heterotrimeric nucleoporin complex consisting of recombinant Nsp1p, Nup49p, and Nup57p. Mol. Biol. Cell 8, 33-46.
62. Sheehan, M.A., Mills, A.D., Sleeman, A.M., Laskey, R.A., and Blow, J.J. (1988). Steps in the assembly of replication-competent nuclei in a cell-free system from Xenopus eggs. J. Cell Biol. 106, 1-12.
63. Sherman, F., Fink, G.R., and Hicks, J.B. (1986). Methods in Yeast Genetics, Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
64. Sikorski, R.S., and Hieter, P. (1989). A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122, 19-27.
65. Siniossoglou, S., Wimmer, C., Rieger, M., Doye, V., Tekotte, H., Weise, C., Emig, S., Segref, A., and Hurt, E.C. (1996). A novel complex of nucleoporins, which includes Sec13p and a Sec13p homolog, is essential for normal nuclear pores. Cell 84, 265-275.
66. Strambio-de-Castillia, C., Blobel, G., and Rout, M.P. (1995). Isolation and characterization of nuclear envelopes from the yeast Saccharomyces. J. Cell Biol. 131, 19-31.
67. Sullivan, K.M., Busa, W.B., and Wilson, K.L. (1993). Calcium mobilization is required for nuclear vesicle fusion in vitro: implications for membrane traffic and IP3 receptor function. Cell 73, 1411-1422.
68. Suprynowicz, F.A., and Gerace, L. (1986). A fractionated cell-free system for analysis of prophase nuclear disassembly. J. Cell Biol. 103, 2073-2081.
69. Underwood, M.R., and Fried, H.M. (1990). Characterization of nuclear localizing sequences derived from yeast ribosomal protein L29. EMBO J. 9, 91-99.
70. Vigers, G.P., and Lohka, M.J. (1991). A distinct vesicle population targets membranes and pore complexes to the nuclear envelope in Xenopus eggs. J. Cell Biol. 112, 545-556.
71. Vigers, G.P., and Lohka, M.J. (1992). Regulation of nuclear envelope precursor functions during cell division. J. Cell Sci. 102, 273-284.
72. Wendland, B., McCaffery, J.M, Xiao, Q., and Emr, S.D. (1996). A novel fluorescence-activated cell sorter-based screen for yeast endocytosis mutants identifies a yeast homologue of mammalian eps15. J. Cell Biol. 135, 1485-1500.
73. Wente, S.R., and Blobel, G. (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.
74. Wente, S.R., and Blobel, G. (1994). NUP145 encodes a novel yeast glycine-leucine-phenylalanine-glycine (GLFG) nucleoporin required for nuclear envelope structure. J. Cell Biol. 125, 955-969.
75. Wente, S.R., Gasser, S.M., and Caplan, A.J. (1997). The nucleus and nucleocytoplasmic transport in Saccharomyces cerevisiae. In: The Molecular and Cellular Biology of the Yeast Saccharomyces, ed. J. Pringle, J. Broach, and E. Jones, Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press, 471-546.
76. Wente, S.R., Rout, M.P., and Blobel, G. (1992). A new family of yeast nuclear pore complex proteins. J. Cell Biol. 119, 705-723.
77. Wimmer, C., Doye, V., Grandi, P., Nehrbass, U., and Hurt, E.C. (1992). A new subclass of nucleoporins that functionally interact with nuclear pore protein NSP1. EMBO J. 11, 5051-5061.
78. Wozniak, R.W., Bartnik, E., and Blobel, G. (1989). Primary structure analysis of an integral membrane glycoprotein of the nuclear pore. J. Cell Biol. 108, 2083-2092.
79. Wozniak, R.W., Blobel, G., and Rout, M.P. (1994). POM152 is an integral protein of the pore membrane domain of the yeast nuclear envelope. J. Cell Biol. 125, 31-42.
80. Yan, C., Leibowitz, N., and Melese, T. (1997). A role for the divergent actin gene, ACT2, in nuclear pore complex structure and function. EMBO J. 16, 3572-3586.
81. Yang, X., Hubbard, E.J., and Carlson, M. (1992). A protein kinase substrate identified by the two-hybrid system. Science 257, 680-682.
82. Zabel, U., Doye, V., Tekotte, H., Wepf, R., Grandi, P., and Hurt, E.C. (1996). Nic96p is required for nuclear pore formation and functionally interacts with a novel nucleoporin, Nup188p. J. Cell Biol. 133, 1141-1152.