The influenza virus NEP (NS2 protein) mediates the nuclear export of viral ribonucleoproteins

EMBO Journal

Volumn 17, Issue 1, 1998, Pages 288-296

  O'Neill, Robert E ^a   Talon, Julie ^a   Palese, Peter ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

HIV; Influenza virus NEP(NS2); Nucleocytoplasmic transport; Ribonucleoprotein; RNA export

Indexed keywords

NUCLEOPORIN; REV PROTEIN; RIBONUCLEOPROTEIN; VIRUS ANTIBODY; VIRUS PROTEIN;

ARTICLE; CELL NUCLEUS; CONTROLLED STUDY; HUMAN IMMUNODEFICIENCY VIRUS 1; INFLUENZA VIRUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN CROSS LINKING; PROTEIN DOMAIN; PROTEIN TRANSPORT; VIRION; VIRUS REPLICATION;

AMINO ACID SEQUENCE; BIOLOGICAL TRANSPORT; CELL NUCLEUS; MICROINJECTIONS; MOLECULAR SEQUENCE DATA; ORTHOMYXOVIRIDAE; PORINS; RECOMBINANT PROTEINS; RIBONUCLEOPROTEINS; SACCHAROMYCES CEREVISIAE; VIRAL NONSTRUCTURAL PROTEINS;

EID: 0032472328     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/17.1.288     Document Type: Article

References (50)

1. Alonso-Caplen, F.V. and Krug, R.M. (1991) Regulation of the extent of splicing of influenza virus NS1 mRNA: roles of the rates of splicing and of nucleocytoplasmic transport of NS1 mRNA. Mol. Cell. Biol. 11, 1092-1098.
2. Alonso-Caplen, F.V. and Krug, R.M. (1992) Nucleocytoplasmic transport: the influenza virus NS1 protein regulates the transport of spliced NS2 mRNA and its precursor NS1 mRNA. Genes. Dev., 6, 255-267.
3. Bogerd, H.P., Fridell, R.A., Madore, S. and Cullen, B.R. (1995) Identification of a novel cellular cofactor for the Rev/Rex class of retroviral regulatory proteins. Cell, 82, 485-494.
4. Davis, L.I. (1995) The nuclear pore complex. Annu. Rev. Biochem., 64, 865-896.
5. Diaz, J.-J., Dodon, M.D., Schaerer-Uthurralt, N., Simonin, D., Kindbeiter, K., Gazzolo, L. and Madjar, J.J. (1996) Post-transcriptional transactivation of human retroviral envelope glycoprotein expression by herpes simplex virus Us11 protein. Nature, 379, 273-277.
6. Dobbelstein, M., Roth, J., Kimberly, W.T., Levine, A.J. and Shenk, T. (1997) Nuclear export of the E1B 55-kDa and E4 34-kDa adenoviral oncoproteins mediated by a Rev-like signal sequence. EMBO J., 16, 4276-4284.
7. Felber, B.K., Hadzopoulou-Cladaras, M., Cladaras, C., Copeland, T. and Pavlakis, G.N. (1989) Rev protein of human immunodeficiency virus type 1 affects the stability and transport of the viral mRNA. Proc. Natl Acad. Sci. USA, 86, 1495-1499.
8. Fischer, U., Meyer, S., Teufel, M., Heckel, C., Luhrmann, R. and Rautmann, G. (1994) Evidence that HIV-1 Rev directly promotes the nuclear export of unspliced RNA. EMBO J., 13, 4105-4112.
9. Fischer, U., Huber, J., Boelens, W.C., Mattaj, I.W. and Luhrmann, R. (1995) The HIV-1 Rev activation domain is a nuclear export signal that accesses an export pathway used by specific cellular RNAs. Cell, 82, 475-483.
10. Fortes, P., Beloso, A. and Ortin, J. (1994) Influenza virus NS1 protein inhibits pre-mRNA splicing and blocks mRNA nucleocytoplasmic transport. EMBO J., 13, 704-712.
11. Fridell, R.A., Bogerd, H.P. and Cullen, B.R. (1996a) Nuclear export of late HIV-1 mRNAs occurs via a cellular protein export pathway. Proc. Natl Acad. Sci. USA, 93, 4421-4424.
12. Fridell, R.A., Fischer, U., Luhrmann, R., Meyer, B.E., Meinkoth, J.L., Malim, M.H. and Cullen, B.R. (1996b) 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.
13. Fritz, C.C., Zapp, M.L. and Green, M.R. (1995) A human nucleoporin-like protein that specifically interacts with HIV Rev. Nature, 376, 530-533.
14. Greenspan, D., Krysta, M., Nakada, S., Arnheiter, H., Lyles, D.S. and Palese, P. (1985) Expression of influenza virus NS2 nonstructural protein in bacteria and localization of NS2 in infected eucaryotic cells. J. Virol. 54, 833-843.
15. Guddat, U., Bakken, A.H. and Pieler, T. (1990) Protein-mediated nuclear export of RNA: 5S rRNA containing small RNPs in Xenopus oocytes. Cell, 60, 619-628.
16. Guiochon-Mantel, A., Lescop, P., Christin-Maitre, S., Loosfelt, H., Perrot-Applanat, M. and Milgrom, W. (1991) Nucleocytoplasmic shuttling of the progesterone receptor. EMBO J., 10, 3851-3859.
17. Gyuris, J., Golemis, E., Chertkov, H. and Brent, R. (1993) Cdil, a human G1 and S phase protein phosphatase that associates with cdk2. Cell, 75, 791-803.
18. Harlow, E. and Lane, D. (1988) Antibodies: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
19. Hope, T.J., Huang, X., McDonald, D. and Parslow, T.G. (1990) Steroid-receptor fusion of the human immunodeficiency virus type 1 Rev transactivator: mapping cryptic functions of the arginine-rich motif. Proc. Natl Acad. Sci. USA, 87, 7787-7791.
20. Izaurralde, E. and Mattaj, I.W. (1995) RNA export. Cell, 81, 153-158.
21. Lamb, R.A., Etkind, P.R. and Choppin, P.W. (1978) Evidence for a ninth influenza viral polypeptide. Virology, 91, 60-78.
22. Malim, M.H., Böhnlein, S., Hauber, J. and Cullen, B.R. (1989a) Functional dissection of the HIV-1 Rev trans-activator: derivation of a transdominant repressor of Rev function. Cell, 58, 205-214.
23. Malim, M.H., Hauber, J., Le, S.-Y., Maizel, J.V. and Cullen, B.R. (1989b) The HIV-1 rev trans-activator acts through a structured target sequence to activate nuclear export of unspliced viral mRNA. Nature, 338, 254-257.
24. Malim, M.H., McCarn, D.F., Tiley, L.S. and Cullen, B.R. (1991) Mutational definition of the human immunodeficiency virus type 1 Rev activation domain. J. Virol., 65, 4248-4254.
25. Martin, K. and Helenius, A. (1991) Nuclear transport of influenza virus ribonucleoproteins: the viral matrix protein (M1) promotes export and inhibits import. Cell, 67, 117-130.
26. Mehlin, H., Daneholt, B. and Skoglund, U. (1992) Translocation of a specific premessenger ribonucleoprotein particle through the nuclear pore studied with electron microscope tomography. Cell, 69, 605-613.
27. Meyer, B.E., Mienkoth, J.L. and Michael, M.H. (1996) Nuclear transport of human immunodeficiency virus type 1, visna virus and equine infectious anemia virus rev proteins: identification of a family of transferable nuclear export signals. J. Virol., 70, 2350-2359.
28. Michael, W.M., Choi, M. and Dreyfuss, G. (1995) A nuclear export signal in hnRNP A1: a signal-mediated, temperature-dependent nuclear protein export pathway. Cell, 83, 415-422.
29. Murphy, R. and Wente, S.R. (1996) An RNA-export mediator with an essential nuclear export signal. Nature, 383, 357-360.
30. Nigg, E.A. (1997) Nucleocytoplasmic transport: signals, mechanisms and regulation. Nature, 386, 779-787.
31. O'Neill, R.E. and Palese, P. (1995) NPI-1, the human homologue of SRP1, interacts with influenza virus nucleoprotein. Virology, 206, 116-125.
32. O'Neill, R.E., Moroianu, J., Jaskunas, R., Blobel, G. and Palese, P. (1995) Nuclear import of influenza virus RNA can be mediated by the viral NP and transport factors required for protein import. J. Biol. Chem., 270, 22701-22704.
33. Palmieri, D. and Malim, M.H. (1996) The human T-cell leukemia virus type 1 posttranscriptional trans-activator Rex contains a nuclear export signal. J. Virol., 70, 6442-6445.
34. Piñol-Roma, S. and Dreyfuss, G. (1992) Shuttling of pre-mRNA binding proteins between nucleus and cytoplasm. Nature, 355, 730-732.
35. Qiu, Y. and Krug, R.M. (1994) The influenza virus NS1 protein is a poly(A)-binding protein that inhibits nuclear export of mRNAs containing poly(A). J. Virol., 68, 2425-2432.
36. Rey, O. and Nayak, D.P. (1992) Nuclear retention of M1 protein in a temperature-sensitive mutant of influenza (A/WSN/33) virus does not affect nuclear export of viral ribonucleoproteins. J. Virol., 66, 5815-5824.
37. Richardson, J.C. and Akkina, R.K. (1991) NS2 protein of influenza virus is found in purified virus and phosphorylated in infected cells. Arch. Virol., 116, 69-80.
38. Stutz, R. and Rosbash, M. (1994) A functional interaction between Rev and yeast pre-mRNA is related to splicing complex formation. EMBO J., 13, 4096-4104.
39. Stutz, F., Neville, M. and Rosbash, M. (1995) Identification of a novel nuclear pore-associated protein as a functional target of the HIV-1 Rev protein in yeast. Cell, 82, 495-506.
40. Stutz, F., Izaurralde, E., Mattaj, I.W. and Rosbash, M. (1996) A role for nucleoporin FG repeat domains in export of human immunodeficiency virus type 1 Rev protein and RNA from the nucleus. Mol. Cell. Biol., 16, 7144-7150.
41. Visa, N., Alzhanova-Ericsson, A.T., Sun, X., Kiseleva, E., Björkroth, B., Wurtz, T. and Daneholt, B. (1996) A pre-mRNA-binding protein accompanies the RNA from the gene through the nuclear pores and into the polysomes. Cell, 84, 253-264.
42. Ward, A.C., Castelli, L.A., Lucantoni, A.C., White, J.F., Azad, A.A. and Macreadie, I.G. (1995) Expression and analysis of the NS2 protein of influenza A virus. Arch. Virol., 140, 2067-2073.
43. Wen, W.A., Harootunian, S.R., Adams, S.R., Feramisco, J., Tsien, R.Y., Meinkoth, J.L. and Taylor, S.S. (1994) Heat-stable inhibitors of cAMP-dependent protein kinase carry a nuclear export signal. J. Biol. Chem., 269, 32214-32220.
44. Wen, W., Meinkoth, J.L., Tsien, R.Y. and Taylor, S.S. (1995) Identification of a signal for rapid export of proteins from the nucleus. Cell, 82, 463-473.
45. Whittaker, G., Bui, M. and Helenius, A. (1996a) Nuclear trafficking of influenza virus ribonucleoproteins in heterokaryons. J. Virol., 70, 2743-2756.
46. Whittaker, G., Bui, M. and Helenius, A. (1996b) The role of nuclear import and export in influenza virus infection. Trends Cell Biol., 6, 67-71.
47. Wolff, T., O'Neill, R.E. and Palese, P. (1996) Interaction of NSI-1, a human protein that binds to the non-structural NS1 proteins of influenza A and B viruses. J. Virol., 70, 5363-5372.
48. Yasuda, J., Nakada, S., Kato, A., Toyoda, T. and Ishihama, A. (1993) Molecular assembly of influenza virus: association of the NS2 protein with virion matrix. Virology, 196, 249-255.
49. Youg, J.F., Desselberger, U., Graves, P., Palese, P., Shatzman, A. and Rosenberg, M. (1982) Cloning and expression of influenza virus genes. In Laver, W.G. (ed.) The Origin of Pandemic Viruses. Elsevier Science, New York, USA, pp. 129-138.
50. Zervos, A.S., Gyuris, J. and Brent, R. (1993) Mxil, a protein that specifically interacts with Max to bind Myc-Max recognition sites. Cell, 72, 222-232.