Inhibition of ran guanosine triphosphatase-dependent nuclear transport by the matrix protein of vesicular stomatitis virus

Science

Volumn 276, Issue 5320, 1997, Pages 1845-1848

  Her, Lu Shiun ^a   Lund, Elsebet ^a   Dahlberg, James E ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

GUANOSINE TRIPHOSPHATASE; MATRIX PROTEIN;

ANIMAL CELL; ARTICLE; CELL NUCLEUS; CONTROLLED STUDY; INTRACELLULAR TRANSPORT; NONHUMAN; OOCYTE; PRIORITY JOURNAL; PROTEIN TRANSPORT; RNA TRANSPORT; VESICULAR STOMATITIS VIRUS; XENOPUS LAEVIS;

ALPHA KARYOPHERINS; ANIMALS; BIOLOGICAL TRANSPORT, ACTIVE; CELL NUCLEUS; CYTOPLASM; GTP PHOSPHOHYDROLASES; NUCLEAR ENVELOPE; NUCLEAR PROTEINS; OOCYTES; PROTEINS; RAN GTP-BINDING PROTEIN; RNA; RNA CAPS; RNA PRECURSORS; RNA, MESSENGER; RNA, RIBOSOMAL; RNA, SMALL NUCLEAR; RNA, TRANSFER, AMINO ACID-SPECIFIC; VESICULAR STOMATITIS-INDIANA VIRUS; VIRAL MATRIX PROTEINS; WHEAT GERM AGGLUTININS; XENOPUS LAEVIS;

EID: 0030810744     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.276.5320.1845     Document Type: Article

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57. R. R. Wagner, J. R. Thomas, J. J. McGowan, Compr. Virol. 19, 223 (1984); P. K. Weck and R. R. Wagner, J. Virol. 30, 410 (1979); F.-S. Wu and J. M. Lucas-Lenard, Biochemistry 19, 804 (1980); D. Thomas, J. Virol. 54, 598 (1985).
58. R. R. Wagner, J. R. Thomas, J. J. McGowan, Compr. Virol. 19, 223 (1984); P. K. Weck and R. R. Wagner, J. Virol. 30, 410 (1979); F.-S. Wu and J. M. Lucas-Lenard, Biochemistry 19, 804 (1980); D. Thomas, J. Virol. 54, 598 (1985).
59. R. R. Wagner, J. R. Thomas, J. J. McGowan, Compr. Virol. 19, 223 (1984); P. K. Weck and R. R. Wagner, J. Virol. 30, 410 (1979); F.-S. Wu and J. M. Lucas-Lenard, Biochemistry 19, 804 (1980); D. Thomas, J. Virol. 54, 598 (1985).
60. L. D. Fresco, M. G. Kurilla, J. D. Keene, Mol. Cell. Biol. 7, 1148 (1987); D. E. Crone and J. D. Keene, J. Virol. 63, 4172 (1989).
61. L. D. Fresco, M. G. Kurilla, J. D. Keene, Mol. Cell. Biol. 7, 1148 (1987); D. E. Crone and J. D. Keene, J. Virol. 63, 4172 (1989).
62. I. W. Mattaj, Cell 46, 905 (1986).
63. B. L. Black and D. S. Lyles, J. Virol. 66, 4058 (1992).
64. It has been suggested that the short (47-nucleotide) leader RNA that is made early in VSV infection plays a role in host cell shutoff (77), but evidence that it directly affects nuclear gene expression is lacking.
65. 35S-labeled nuclear proteins for import assays have been described (23). The immunoblot analysis was done by standard techniques with monoclonal antibodies to M protein [L. Lefrancois and D. S. Lyles, J. Virol. 121, 157 (1982)] and monospecific antibodies to transport proteins as noted in the legend to Fig. 5; bound antibodies were detected by ECL (Kirkegaard & Perry Laboratories, Inc., Gaithersberg, MD).
66. M. P. Terns and J. E. Dahlberg, Science 264, 959 (1994).
67. M. A. Powers, D. J. Forbes, J. E. Dahlberg, E. Lund, J. Cell Biol. 136, 241 (1997).
68. C. Grimm, E. Lund, J. E. Dahlberg, EMBOJ. 16, 793 (1997).
69. L.-S. Her, E. Lund, J. E. Dahlberg, unpublished results.
70. In the presence of inhibitors of export pre-snRNAs are unstable in the nucleus (9, 23), thereby accounting for the lower amounts of these RNAs in the presence of M protein.
71. A. A. Hadjilov, The Nucleolus and Ribosome Biogenesis (Springer-Verlag, New York, 1985).
72. Unlike protein import, snRNP import is quite insensitive to other general inhibitors of NPC function such as WGA [U. Fisher et al., J. Cell Biol. 113, 705 (1991); N. Michaud and D. S. Goldfarb, ibid. 112, 215 (1991)] and monoclonal antibody mAb414 (9).
73. Unlike protein import, snRNP import is quite insensitive to other general inhibitors of NPC function such as WGA [U. Fisher et al., J. Cell Biol. 113, 705 (1991); N. Michaud and D. S. Goldfarb, ibid. 112, 215 (1991)] and monoclonal antibody mAb414 (9).
74. Ratios, rather than absolute amounts, of the proteins in the nuclear and cytoplasmic fractions are significant. Both the quantitative and qualitative changes in the distribution of importin-α in the treated oocytes were highly reproducible (25) and minor variations in amounts of Ran and importin-β between control and treated cells were not observed with other batches of oocytes. The persistance of multiple forms of importin-α even after phosphatase treatment (Fig. 5C) indicates that inaccessible phosphates or additional modifications may be involved. By co-immunoprecipitation we were unable to detect any interaction between M protein and Ran, or importins-α or -β (25).
75. Y. Azuma, M. M. Tabb, L. Vu, M. Nomura, Proc. Natl. Acad. Sci. U.S.A. 92, 5159 (1995); I. Török et al., J. Cell Biol. 129, 1473 (1995).
76. Y. Azuma, M. M. Tabb, L. Vu, M. Nomura, Proc. Natl. Acad. Sci. U.S.A. 92, 5159 (1995); I. Török et al., J. Cell Biol. 129, 1473 (1995).
77. In Saccharomyces cerevisiae, importin-α accumulates in the nucleus under conditions when the GDP form of Ran is expected to predominate; D. M. Koepp, D. H. Wong, A. H. Corbett, P. A. Silver, J. Cell Biol. 133, 1163 (1996).
78. N. Panté and U. Aebi, Science 273, 1729 (1996).
79. M protein does not affect passive diffusion of small RNAs or nucleotides across the nuclear envelope; C. Grimm, A. E. Pasquinelli, E. Lund, J. E. Dahlberg, unpublished results.
80. V. Varvel, E. Lund, J. E. Dahlberg, unpublished results.
81. Although M protein alone is sufficient to inhibit RNA export, a role for the VSV leader RNA in shut-off of nuclear gene expression of virus infected cells cannot be excluded (see 19).
82. B. L. Black, G. Brewer, D. S. Lyles, J. Virol. 68, 555 (1994); D. S. Lyles, M. O. McKenzie, M. Ahmed, S. C. Woolwine, Wrotogy 225, 172 (1996).
83. B. L. Black, G. Brewer, D. S. Lyles, J. Virol. 68, 555 (1994); D. S. Lyles, M. O. McKenzie, M. Ahmed, S. C. Woolwine, Wrotogy 225, 172 (1996).
84. Inhibition of protein import by M protein may secondarily inhibit intranuclear functions such as transcription (for example, through depletion of transcription factors), but these effects are unlikely to be as immediate as a direct block of RNA export.
85. 7G-caps; and A. Grandjean and M. Barr for technical assistance. Supported by NIH grant GM30220.