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. 1994 Mar;68(3):1432–1437. doi: 10.1128/jvi.68.3.1432-1437.1994

Influenza virus NS1 protein stimulates translation of the M1 protein.

K Enami 1, T A Sato 1, S Nakada 1, M Enami 1
PMCID: PMC236597  PMID: 7508995

Abstract

The influenza virus NS1 protein was shown to stimulate translation of the M1 protein. M-CAT RNA, which contains the chloramphenicol acetyltransferase (CAT) reporter gene and the terminal noncoding sequence of segment 7 (coding for the M1 and M2 proteins), was ribonucleoprotein transfected into clone 76 cells expressing the influenza virus RNA polymerase and NP proteins required for the transcription and replication of influenza virus ribonucleoproteins. When the cells were superinfected with a recombinant vaccinia virus which expresses the NS1 protein, CAT expression from the M-CAT RNA was significantly stimulated but transcription was not altered. The expression of NS-CAT RNA, which contains noncoding sequences of segment 8 (coding for the NS1 and NS2 proteins), was not altered by the NS1 protein. Site-directed mutagenesis showed that the sequence GGUAGAUA upstream of the initiation codon on segment 7 was required for stimulation.

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Selected References

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  1. Briedis D. J., Conti G., Munn E. A., Mahy B. W. Migration of influenza virus-specific polypeptides from cytoplasm to nucleus of infected cells. Virology. 1981 May;111(1):154–164. doi: 10.1016/0042-6822(81)90661-9. [DOI] [PubMed] [Google Scholar]
  2. Compans R. W. Influenza virus proteins. II. Association with components of the cytoplasm. Virology. 1973 Jan;51(1):56–70. doi: 10.1016/0042-6822(73)90365-6. [DOI] [PubMed] [Google Scholar]
  3. Cooper J. A., Moss B. In vitro translation of immediate early, early, and late classes of RNA from vaccinia virus-infected cells. Virology. 1979 Jul 30;96(2):368–380. doi: 10.1016/0042-6822(79)90095-3. [DOI] [PubMed] [Google Scholar]
  4. Enami K., Qiao Y., Fukuda R., Enami M. An influenza virus temperature-sensitive mutant defective in the nuclear-cytoplasmic transport of the negative-sense viral RNAs. Virology. 1993 Jun;194(2):822–827. doi: 10.1006/viro.1993.1324. [DOI] [PubMed] [Google Scholar]
  5. Enami M., Fukuda R., Ishihama A. Transcription and replication of eight RNA segments of influenza virus. Virology. 1985 Apr 15;142(1):68–77. doi: 10.1016/0042-6822(85)90423-4. [DOI] [PubMed] [Google Scholar]
  6. Enami M., Luytjes W., Krystal M., Palese P. Introduction of site-specific mutations into the genome of influenza virus. Proc Natl Acad Sci U S A. 1990 May;87(10):3802–3805. doi: 10.1073/pnas.87.10.3802. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Enami M., Palese P. High-efficiency formation of influenza virus transfectants. J Virol. 1991 May;65(5):2711–2713. doi: 10.1128/jvi.65.5.2711-2713.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Garfinkel M. S., Katze M. G. How does influenza virus regulate gene expression at the level of mRNA translation? Let us count the ways. Gene Expr. 1993;3(2):109–118. [PMC free article] [PubMed] [Google Scholar]
  9. Hatada E., Hasegawa M., Shimizu K., Hatanaka M., Fukuda R. Analysis of influenza A virus temperature-sensitive mutants with mutations in RNA segment 8. J Gen Virol. 1990 Jun;71(Pt 6):1283–1292. doi: 10.1099/0022-1317-71-6-1283. [DOI] [PubMed] [Google Scholar]
  10. Hershey J. W. Translational control in mammalian cells. Annu Rev Biochem. 1991;60:717–755. doi: 10.1146/annurev.bi.60.070191.003441. [DOI] [PubMed] [Google Scholar]
  11. Honda A., Uéda K., Nagata K., Ishihama A. RNA polymerase of influenza virus: role of NP in RNA chain elongation. J Biochem. 1988 Dec;104(6):1021–1026. doi: 10.1093/oxfordjournals.jbchem.a122569. [DOI] [PubMed] [Google Scholar]
  12. Huang T. S., Palese P., Krystal M. Determination of influenza virus proteins required for genome replication. J Virol. 1990 Nov;64(11):5669–5673. doi: 10.1128/jvi.64.11.5669-5673.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Kimura N., Fukushima A., Oda K., Nakada S. An in vivo study of the replication origin in the influenza virus complementary RNA. J Biochem. 1993 Jan;113(1):88–92. doi: 10.1093/oxfordjournals.jbchem.a124009. [DOI] [PubMed] [Google Scholar]
  14. Kimura N., Nishida M., Nagata K., Ishihama A., Oda K., Nakada S. Transcription of a recombinant influenza virus RNA in cells that can express the influenza virus RNA polymerase and nucleoprotein genes. J Gen Virol. 1992 Jun;73(Pt 6):1321–1328. doi: 10.1099/0022-1317-73-6-1321. [DOI] [PubMed] [Google Scholar]
  15. Koennecke I., Boschek C. B., Scholtissek C. Isolation and properties of a temperature-sensitive mutant (ts 412) of an influenza A virus recombinant with a ts lesion in the gene coding for the nonstructural protein. Virology. 1981 Apr 15;110(1):16–25. doi: 10.1016/0042-6822(81)90003-9. [DOI] [PubMed] [Google Scholar]
  16. Krug R. M., Etkind P. R. Cytoplasmic and nuclear virus-specific proteins in influenza virus-infected MDCK cells. Virology. 1973 Nov;56(1):334–348. doi: 10.1016/0042-6822(73)90310-3. [DOI] [PubMed] [Google Scholar]
  17. Krug R. M., Soeiro R. Studies on the intranuclear localization of influenza virus-specific proteins. Virology. 1975 Apr;64(2):378–387. doi: 10.1016/0042-6822(75)90114-2. [DOI] [PubMed] [Google Scholar]
  18. Lazarowitz S. G., Compans R. W., Choppin P. W. Influenza virus structural and nonstructural proteins in infected cells and their plasma membranes. Virology. 1971 Dec;46(3):830–843. doi: 10.1016/0042-6822(71)90084-5. [DOI] [PubMed] [Google Scholar]
  19. Li X., Palese P. Mutational analysis of the promoter required for influenza virus virion RNA synthesis. J Virol. 1992 Jul;66(7):4331–4338. doi: 10.1128/jvi.66.7.4331-4338.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Luo G., Palese P. Genetic analysis of influenza virus. Curr Opin Genet Dev. 1992 Feb;2(1):77–81. doi: 10.1016/s0959-437x(05)80326-0. [DOI] [PubMed] [Google Scholar]
  21. Luytjes W., Krystal M., Enami M., Parvin J. D., Palese P. Amplification, expression, and packaging of foreign gene by influenza virus. Cell. 1989 Dec 22;59(6):1107–1113. doi: 10.1016/0092-8674(89)90766-6. [DOI] [PubMed] [Google Scholar]
  22. Martin K., Helenius A. Nuclear transport of influenza virus ribonucleoproteins: the viral matrix protein (M1) promotes export and inhibits import. Cell. 1991 Oct 4;67(1):117–130. doi: 10.1016/0092-8674(91)90576-k. [DOI] [PubMed] [Google Scholar]
  23. Nakamura Y., Oda K., Nakada S. Growth complementation of influenza virus temperature-sensitive mutants in mouse cells which express the RNA polymerase and nucleoprotein genes. J Biochem. 1991 Sep;110(3):395–401. doi: 10.1093/oxfordjournals.jbchem.a123592. [DOI] [PubMed] [Google Scholar]
  24. Parvin J. D., Palese P., Honda A., Ishihama A., Krystal M. Promoter analysis of influenza virus RNA polymerase. J Virol. 1989 Dec;63(12):5142–5152. doi: 10.1128/jvi.63.12.5142-5152.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Piccone M. E., Fernandez-Sesma A., Palese P. Mutational analysis of the influenza virus vRNA promoter. Virus Res. 1993 May;28(2):99–112. doi: 10.1016/0168-1702(93)90129-b. [DOI] [PubMed] [Google Scholar]
  26. Plucienniczak A., Schroeder E., Zettlmeissl G., Streeck R. E. Nucleotide sequence of a cluster of early and late genes in a conserved segment of the vaccinia virus genome. Nucleic Acids Res. 1985 Feb 11;13(3):985–998. doi: 10.1093/nar/13.3.985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Pons M. W. Studies on the replication of influenza virus RNA. Virology. 1972 Mar;47(3):823–832. doi: 10.1016/0042-6822(72)90574-0. [DOI] [PubMed] [Google Scholar]
  28. Ritchey M. B., Palese P., Kilbourne E. D. RNAs of influenza A, B, and C viruses. J Virol. 1976 May;18(2):738–744. doi: 10.1128/jvi.18.2.738-744.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Saiki R. K., Gelfand D. H., Stoffel S., Scharf S. J., Higuchi R., Horn G. T., Mullis K. B., Erlich H. A. Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science. 1988 Jan 29;239(4839):487–491. doi: 10.1126/science.2448875. [DOI] [PubMed] [Google Scholar]
  30. Seong B. L., Brownlee G. G. A new method for reconstituting influenza polymerase and RNA in vitro: a study of the promoter elements for cRNA and vRNA synthesis in vitro and viral rescue in vivo. Virology. 1992 Jan;186(1):247–260. doi: 10.1016/0042-6822(92)90079-5. [DOI] [PubMed] [Google Scholar]
  31. Shapiro G. I., Gurney T., Jr, Krug R. M. Influenza virus gene expression: control mechanisms at early and late times of infection and nuclear-cytoplasmic transport of virus-specific RNAs. J Virol. 1987 Mar;61(3):764–773. doi: 10.1128/jvi.61.3.764-773.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Shaw M. W., Compans R. W. Isolation and characterization of cytoplasmic inclusions from influenza A virus-infected cells. J Virol. 1978 Feb;25(2):608–615. doi: 10.1128/jvi.25.2.608-615.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Smith G. L., Levin J. Z., Palese P., Moss B. Synthesis and cellular location of the ten influenza polypeptides individually expressed by recombinant vaccinia viruses. Virology. 1987 Oct;160(2):336–345. doi: 10.1016/0042-6822(87)90004-3. [DOI] [PubMed] [Google Scholar]
  34. Taylor J. M., Hampson A. W., Layton J. E., White D. O. The polypeptides of influenza virus. IV. An analysis of nuclear accumulation. Virology. 1970 Nov;42(3):744–752. doi: 10.1016/0042-6822(70)90320-x. [DOI] [PubMed] [Google Scholar]
  35. Wolstenholme A. J., Barrett T., Nichol S. T., Mahy B. W. Influenza virus-specific RNA and protein syntheses in cells infected with temperature-sensitive mutants defective in the genome segment encoding nonstructural proteins. J Virol. 1980 Jul;35(1):1–7. doi: 10.1128/jvi.35.1.1-7.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Yamanaka K., Ishihama A., Nagata K. Translational regulation of influenza virus mRNAs. Virus Genes. 1988 Oct;2(1):19–30. doi: 10.1007/BF00569734. [DOI] [PubMed] [Google Scholar]
  37. Yamanaka K., Nagata K., Ishihama A. Temporal control for translation of influenza virus mRNAs. Arch Virol. 1991;120(1-2):33–42. doi: 10.1007/BF01310947. [DOI] [PubMed] [Google Scholar]
  38. Yamanaka K., Ogasawara N., Yoshikawa H., Ishihama A., Nagata K. In vivo analysis of the promoter structure of the influenza virus RNA genome using a transfection system with an engineered RNA. Proc Natl Acad Sci U S A. 1991 Jun 15;88(12):5369–5373. doi: 10.1073/pnas.88.12.5369. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Yoshida T., Shaw M. W., Young J. F., Compans R. W. Characterization of the RNA associated with influenza A cytoplasmic inclusions and the interaction of NS1 protein with RNA. Virology. 1981 Apr 15;110(1):87–97. doi: 10.1016/0042-6822(81)90010-6. [DOI] [PubMed] [Google Scholar]
  40. Young J. F., Desselberger U., Palese P., Ferguson B., Shatzman A. R., Rosenberg M. Efficient expression of influenza virus NS1 nonstructural proteins in Escherichia coli. Proc Natl Acad Sci U S A. 1983 Oct;80(19):6105–6109. doi: 10.1073/pnas.80.19.6105. [DOI] [PMC free article] [PubMed] [Google Scholar]

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