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PMID: 11046154 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

The matrix protein of vesicular stomatitis virus inhibits nucleocytoplasmic transport when it is in the nucleus and associated with nuclear pore complexes.

Molecular and cellular biology ·Vol. 20 ·No. 22 ·2000-11-00 ·Pages 8590-601

Petersen JM, Her LS, Varvel V, Lund E, Dahlberg JE

Abstract

The matrix (M) protein of vesicular stomatitis virus (VSV) is a potent inhibitor of bidirectional nuclear transport. Here we demonstrate that inhibition occurs when M protein is in the nucleus of Xenopus laevis oocytes and that M activity is readily reversed by a monoclonal antibody (alphaM). We identify a region of M protein, amino acids 51 to 59, that is required both for inhibition of transport and for efficient recognition by alphaM. When expressed in transfected HeLa cells, M protein colocalizes with nuclear pore complexes (NPCs) at the nuclear rim. Moreover, mutation of a single amino acid, methionine 51, eliminates both transport inhibition and targeting to NPCs. We propose that M protein inhibits bidirectional transport by interacting with a component of the NPC or an NPC-associated factor that participates in nucleocytoplasmic transport.

MeSH Terms
Active Transport, Cell Nucleus Amino Acid Sequence Animals Antibodies, Monoclonal/metabolism Base Sequence Cell Nucleus Structures/metabolism Cytoplasm/metabolism Female Humans Molecular Sequence Data Oocytes/metabolism Point Mutation Viral Matrix Proteins/genetics,immunology,metabolism Xenopus laevis
Chemicals
Antibodies, Monoclonal M protein, Vesicular stomatitis virus Viral Matrix Proteins
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Petersen J M
Department of Biomolecular Chemistry, University of Wisconsin-Madison, Madison, Wisconsin 53706-1532, USA.
Her L S
Varvel V
Lund E
Dahlberg J E
References (59)
59 references, click to expand
  1. A novel receptor-mediated nuclear protein import pathway.
    Cell. 1996 Sep 20;86(6):985-94 PMID: 8808633
  2. Getting across the nuclear pore complex.
    Trends Cell Biol. 1999 Aug;9(8):312-8 PMID: 10407410
  3. Heat shock disassembles the nucleolus and inhibits nuclear protein import and poly(A)+ RNA export.
    EMBO J. 1996 Dec 2;15(23):6750-7 PMID: 8978700
  4. The C-terminal domain of TAP interacts with the nuclear pore complex and promotes export of specific CTE-bearing RNA substrates.
    RNA. 2000 Jan;6(1):136-58 PMID: 10668806
  5. Virus replication in enucleate cells: vesicular stomatitis virus and influenza virus.
    J Virol. 1974 Feb;13(2):394-9 PMID: 4359299
  6. Analysis of VSV mutant with attenuated cytopathogenicity: mutation in viral function, P, for inhibition of protein synthesis.
    Cell. 1977 Jun;11(2):273-81 PMID: 196757
  7. The use of Xenopus oocytes for the expression of cloned genes.
    Methods Enzymol. 1983;101:370-86 PMID: 6193395
  8. Identification and characterization of a nuclear pore complex protein.
    Cell. 1986 Jun 6;45(5):699-709 PMID: 3518946
  9. Rapid inhibition of processing and assembly of small nuclear ribonucleoproteins after infection with vesicular stomatitis virus.
    Mol Cell Biol. 1987 Mar;7(3):1148-55 PMID: 3031484
  10. Vesicular stomatitis virus M protein in the nuclei of infected cells.
    J Virol. 1988 Nov;62(11):4387-92 PMID: 2845149
  11. Regulation of human immunodeficiency virus env expression by the rev gene product.
    J Virol. 1989 May;63(5):1959-66 PMID: 2704072
  12. Genetic evidence for multiple functions of the matrix protein of vesicular stomatitis virus.
    J Gen Virol. 1990 Apr;71 ( Pt 4):991-6 PMID: 2157808
  13. Nonaqueous isolation of transcriptionally active nuclei from Xenopus oocytes.
    Methods Enzymol. 1990;181:36-43 PMID: 1696347
  14. Mutational definition of the human immunodeficiency virus type 1 Rev activation domain.
    J Virol. 1991 Aug;65(8):4248-54 PMID: 2072452
  15. Signal-mediated nuclear transport in proliferating and growth-arrested BALB/c 3T3 cells.
    J Cell Biol. 1991 Nov;115(4):933-9 PMID: 1955463
  16. Vesicular stomatitis virus matrix protein inhibits host cell-directed transcription of target genes in vivo.
    J Virol. 1992 Jul;66(7):4058-64 PMID: 1318397
  17. The role of vesicular stomatitis virus matrix protein in inhibition of host-directed gene expression is genetically separable from its function in virus assembly.
    J Virol. 1993 Aug;67(8):4814-21 PMID: 8392615
  18. Multiple cis-acting signals for export of pre-U1 snRNA from the nucleus.
    Genes Dev. 1993 Oct;7(10):1898-908 PMID: 8405997
  19. Identification of cytosolic factors required for nuclear location sequence-mediated binding to the nuclear envelope.
    J Cell Biol. 1994 May;125(3):547-55 PMID: 8175880
  20. Sequences of the vesicular stomatitis virus matrix protein involved in binding to nucleocapsids.
    J Virol. 1991 Mar;65(3):1057-65 PMID: 1847435
  21. Retention and 5' cap trimethylation of U3 snRNA in the nucleus.
    Science. 1994 May 13;264(5161):959-61 PMID: 8178154
  22. PHD--an automatic mail server for protein secondary structure prediction.
    Comput Appl Biosci. 1994 Feb;10(1):53-60 PMID: 8193956
  23. Inducible and conditional inhibition of human immunodeficiency virus proviral expression by vesicular stomatitis virus matrix protein.
    J Virol. 1995 Jun;69(6):3529-37 PMID: 7745700
  24. The HIV-1 Rev activation domain is a nuclear export signal that accesses an export pathway used by specific cellular RNAs.
    Cell. 1995 Aug 11;82(3):475-83 PMID: 7543368
  25. Reverse 5' caps in RNAs made in vitro by phage RNA polymerases.
    RNA. 1995 Nov;1(9):957-67 PMID: 8548660
  26. Regulation of mRNA export in response to stress in Saccharomyces cerevisiae.
    Genes Dev. 1996 Jul 1;10(13):1608-20 PMID: 8682292
  27. The vesicular stomatitis virus matrix protein inhibits transcription from the human beta interferon promoter.
    J Virol. 1997 Jan;71(1):371-7 PMID: 8985359
  28. The vertebrate GLFG nucleoporin, Nup98, is an essential component of multiple RNA export pathways.
    J Cell Biol. 1997 Jan 27;136(2):241-50 PMID: 9015297
  29. In vivo selection of RNAs that localize in the nucleus.
    EMBO J. 1997 Feb 17;16(4):793-806 PMID: 9049308
  30. The human homologue of yeast CRM1 is in a dynamic subcomplex with CAN/Nup214 and a novel nuclear pore component Nup88.
    EMBO J. 1997 Feb 17;16(4):807-16 PMID: 9049309
  31. Activity of vesicular stomatitis virus M protein mutants in cell rounding is correlated with the ability to inhibit host gene expression and is not correlated with virus assembly function.
    Virology. 1997 Mar 3;229(1):77-89 PMID: 9123880
  32. Seventy-five percent accuracy in protein secondary structure prediction.
    Proteins. 1997 Mar;27(3):329-35 PMID: 9094735
  33. Dominant-negative mutants of importin-beta block multiple pathways of import and export through the nuclear pore complex.
    EMBO J. 1997 Mar 17;16(6):1153-63 PMID: 9135132
  34. Inhibition of Ran guanosine triphosphatase-dependent nuclear transport by the matrix protein of vesicular stomatitis virus.
    Science. 1997 Jun 20;276(5320):1845-8 PMID: 9188527
  35. A novel class of RanGTP binding proteins.
    J Cell Biol. 1997 Jul 14;138(1):65-80 PMID: 9214382
  36. Nuclear export of the E1B 55-kDa and E4 34-kDa adenoviral oncoproteins mediated by a rev-like signal sequence.
    EMBO J. 1997 Jul 16;16(14):4276-84 PMID: 9250671
  37. Selection and nuclear immobilization of exportable RNAs.
    Proc Natl Acad Sci U S A. 1997 Sep 16;94(19):10122-7 PMID: 9294173
  38. Nuclear export receptors: from importin to exportin.
    Cell. 1997 Sep 19;90(6):967-70 PMID: 9323123
  39. Exportin 1 (Crm1p) is an essential nuclear export factor.
    Cell. 1997 Sep 19;90(6):1041-50 PMID: 9323132
  40. CRM1 is an export receptor for leucine-rich nuclear export signals.
    Cell. 1997 Sep 19;90(6):1051-60 PMID: 9323133
  41. Nuclear import of U snRNPs requires importin beta.
    EMBO J. 1997 Nov 17;16(22):6783-92 PMID: 9362492
  42. The asymmetric distribution of the constituents of the Ran system is essential for transport into and out of the nucleus.
    EMBO J. 1997 Nov 3;16(21):6535-47 PMID: 9351834
  43. Identification of a nuclear export receptor for tRNA.
    Curr Biol. 1998 Mar 12;8(6):305-14 PMID: 9512417
  44. Importins and exportins: how to get in and out of the nucleus.
    Trends Biochem Sci. 1998 May;23(5):185-9 PMID: 9612083
  45. Functions of the GTPase Ran in RNA export from the nucleus.
    Curr Opin Cell Biol. 1998 Jun;10(3):400-8 PMID: 9640542
  46. Identification of a tRNA-specific nuclear export receptor.
    Mol Cell. 1998 Feb;1(3):359-69 PMID: 9660920
  47. Nuclear retention elements of U3 small nucleolar RNA.
    Mol Cell Biol. 1999 Dec;19(12):8412-21 PMID: 10567566
  48. Snurportin1, an m3G-cap-specific nuclear import receptor with a novel domain structure.
    EMBO J. 1998 Jul 15;17(14):4114-26 PMID: 9670026
  49. Importin beta, transportin, RanBP5 and RanBP7 mediate nuclear import of ribosomal proteins in mammalian cells.
    EMBO J. 1998 Aug 3;17(15):4491-502 PMID: 9687515
  50. Karyopherins and kissing cousins.
    Trends Cell Biol. 1998 May;8(5):184-8 PMID: 9695836
  51. Ran and nuclear transport.
    J Biol Chem. 1998 Sep 4;273(36):22857-60 PMID: 9722501
  52. Effect of vesicular stomatitis virus matrix protein on transcription directed by host RNA polymerases I, II, and III.
    J Virol. 1998 Oct;72(10):8413-9 PMID: 9733895
  53. Nucleocytoplasmic transport: the soluble phase.
    Annu Rev Biochem. 1998;67:265-306 PMID: 9759490
  54. Inhibition of host RNA polymerase II-dependent transcription by vesicular stomatitis virus results from inactivation of TFIID.
    Virology. 1998 Nov 25;251(2):383-92 PMID: 9837802
  55. Nuclear import of Cdk/cyclin complexes: identification of distinct mechanisms for import of Cdk2/cyclin E and Cdc2/cyclin B1.
    J Cell Biol. 1999 Jan 25;144(2):213-24 PMID: 9922449
  56. The nucleoporin nup153 plays a critical role in multiple types of nuclear export.
    Mol Biol Cell. 1999 Mar;10(3):649-64 PMID: 10069809
  57. Influenza A virus NS1 protein targets poly(A)-binding protein II of the cellular 3'-end processing machinery.
    EMBO J. 1999 Apr 15;18(8):2273-83 PMID: 10205180
  58. Ran-independent nuclear import of cyclin B1-Cdc2 by importin beta.
    Proc Natl Acad Sci U S A. 1999 Jul 6;96(14):7938-43 PMID: 10393926
  59. Incorporation of non-local interactions in protein secondary structure prediction from the amino acid sequence.
    Protein Eng. 1996 Feb;9(2):133-42 PMID: 9005434
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
0270-7306
Published
2000-11-00
Pages
8590-601
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC102164
Subset
IM
Grants
NIGMS NIH HHS · R37 GM030220 · United States
NIGMS NIH HHS · T32 GM008349 · United States
NIGMS NIH HHS · GM08349-08 · United States
NIGMS NIH HHS · GM30220 · United States
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