Threonine 157 of influenza virus PA polymerase subunit modulates RNA replication in infectious viruses

Journal of Virology

Volumn 77, Issue 10, 2003, Pages 6007-6013

  Huarte, Maite ^a   Falcón, Ana ^a   Nakaya, Yuri ^b   Ortín, Juan ^a   García Sastre, Adolfo ^b   Nietol, Amelia ^a  

^a CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY RNA; MUTANT PROTEIN; PROTEIN PA; PROTEIN PAT157A; PROTEIN SUBUNIT; PROTEINASE; RIBONUCLEOPROTEIN; RNA POLYMERASE; THREONINE; UNCLASSIFIED DRUG; VIRUS ENZYME; VIRUS PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CELL STRAIN; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVITY; ENZYME ASSAY; HUMAN; HUMAN CELL; INFLUENZA VIRUS A; LUNG; MOUSE; NONHUMAN; NUCLEAR IMPORT; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS; REGULATORY MECHANISM; RNA REPLICATION; RNA SYNTHESIS; VIROGENESIS; VIRUS CELL INTERACTION; VIRUS INFECTIVITY; VIRUS MUTANT; VIRUS MUTATION; VIRUS PATHOGENESIS; VIRUS RECOMBINANT; VIRUS REPLICATION; VIRUS TITRATION; VIRUS TRANSCRIPTION; WEIGHT REDUCTION; WILD TYPE;

ANIMALS; CELL LINE; DNA-DIRECTED RNA POLYMERASES; DOGS; GENE EXPRESSION REGULATION, VIRAL; HUMANS; INFLUENZA A VIRUS; INFLUENZA, HUMAN; MICE; MUTATION; PLAQUE ASSAY; RECOMBINATION, GENETIC; RIBONUCLEOPROTEINS; RNA REPLICASE; RNA, VIRAL; THREONINE; VIRAL PROTEINS; VIRUS REPLICATION;

EID: 0038371106     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.77.10.6007-6013.2003     Document Type: Article

References (45)

1. Akkina, R. K., T. M. Chambers, D. R. Londo, and D. P. Nayak. 1987. Intracellular localization of the viral polymerase proteins in cells infected with influenza virus and cells expressing PB1 protein from cloned cDNA. J. Virol. 61:2217-2224.
2. Almond, J. W., and V. Felsenreich. 1982. Phosphorylation of the nucleoprotein of an avian influenza virus. J. Gen. Virol. 60:295-305.
3. Arrese, M., and A. Portela. 1996. Serine 3 is critical for phosphorylation at the N-terminal end of the nucleoprotein of influenza virus A/Victoria/3/75. J. Virol. 70:3385-3391.
4. Bárcena, J., M. Ochoa, S. de la Luna, J. A. Melero, A. Nieto, J. Ortin, and A. Portela. 1994. Monoclonal antibodies against influenza virus PB2 and NP polypeptides interfere with the initiation step of viral mRNA synthesis in vitro. J. Virol. 68:6900-6909.
5. Biswas, S. K., and D. P. Nayak. 1994. Mutational analysis of the conserved motifs of influenza A virus polymerase basic protein 1. J. Virol. 68:1819-1826.
6. Blaas, D., E. Patzelt, and E. Keuchler. 1982. Identification of the cap binding protein of influenza virus. Nucleic Acids Res. 10:4803-4812.
7. Blok, V., C. Clancl, K. W. Tibbles, S. C. Inglis, M. Krystal, and P. Digard. 1996. Inhibition of the influenza virus RNA-dependent RNA polymerase by antisera directed against the carboxy-terminal region of the PB2 subunit. J. Gen. Virol. 77:1025-1033.
8. Fodor, E., M. Crow, L. Mingay, T. Deng, J. Sharps, P. Fechter, and G. Brownlee. 2002. A single amino acid mutation in the the PA subunit of the influenza virus RNA polymerase inhibits endonucleolytic cleavage of capped RNAs. J. Virol. 76:8989-9001.
9. Fodor, E., D. C. Pritlove, and G. G. Brownlee. 1994. The influenza virus panhandle is involved in the initiation of transcription. J. Virol. 68:4092-4096.
10. Gastaminza, P., B. Perales, A. M. Falcón, and J. Ortín. 2003. Mutations in the N-terminal region of influenza virus. PB2 protein affect virus RNA replication but not transcription. J. Virol. 77:5098-5108.
11. Gonzalez, S., and J. Ortín. 1998. Characterization of influenza virus PB1 protein binding to viral RNA: two separate regions of the protein contribute to the interaction domain. J. Virol. 73:631-637.
12. Gonzalez, S., and J. Ortfn. 1999. Distinct regions of influenza virus PB1 subunit recognize vRNA and cRNA templates. EMBO J. 18:3767-3775.
13. González, S., T. Zürcher, and J. Ortín. 1996. Identification of two separate domains in the influenza virus PB1 protein involved in the interaction with the PB2 and the PA subunits: a model for the viral RNA polymerase structure. Nucleic Acids Res. 24:4456-4463.
14. Gregoriades, A., T. Christie, and K. Markarian. 1984. The membrane (M1) protein of influenza virus occurs in two forms and is a phosphoprotein. J. Virol. 49:229-235.
15. Hara, K., M. Shiota, H. Kido, Y. Ohtsu, T. Kashiwagi, J. Iwahashi, N. Hamada, K. Mizoue, N. Tsumura, H. Kato, and T. Toyoda. 2001. Influenza virus RNA polymerase PA subunit is a novel serine protease with Ser624 at the active site. Genes Cells 6:87-97.
16. Honda, A., K. Mizumoto, and A. Ishihama. 1999. Two separate sequences of PB2 subunit constitute the RNA cap-binding site of influenza virus RNA polymerase. Genes Cells 8:475-485.
17. Huarte, M., J. J. Sanz-Ezquerro, F. Roncal, J. Ortín, and A. Nieto. 2001. the PA subunit from influenza virus polymerase complex interacts with a cellular protein with homology to a family of transcriptional activators. J. Virol. 75:8597-8604.
18. Jones, I. M., P. A. Reay, and K. L. Philpott. 1986. Nuclear location of all three influenza polymerase proteins and a nuclear signal in polymerase PB2. EMBO J. 9:2371-2376.
19. Kistner, O., H. Müller, H. Becht, and C. Scholtissek. 1985. Phosphopeptide fingerprints of nucleoproteins of various influenza A virus strains grown in different host cells. J. Gen. Virol. 66:465-472.
20. Krug, R. M. 1989. The influenza viruses. Plenum Press, New York, N.Y.
21. Lee, M. T., K. Bishop, L. Medcalf, D. Elton, P. Digard, and L. Tiley. 2002. Definition of the minimal viral components required for the initiation of umprimed RNA synthesis by influenza virus RNA polymerase. Nucleic Acids Res. 30:429-438.
22. Li, M.-L., P. Rao, and R. M. Krug. 2001. The active sites of the influenza cap-dependent endonuclease are on different polymerase subunits. EMBO J. 20:2078-2100.
23. Li, M. L., B. C. Ramirez, and R. M. Krug. 1998. RNA-dependent activation of primer RNA production by influenza virus polymerase: different regions of the same protein subunit constitute the two required RNA-binding sites. EMBO J. 17:5844-5852.
24. Licheng, S., D. F. Summers, Q. Peng, and J. Galarza. 1995. Influenza A virus polymerase subunit PB2 is the endonuclease which cleaves host cell mRNA and functions only as the trimeric enzyme. Virology 208:38-47.
25. Mahy, B. W. J. 1983. Mutants of influenza virus, p. 192-253. In P. Palese and D. W. Kingsbury (ed.), Genetics of influenza viruses. Springer-Verlag, Vienna, Austria.
26. Mukaigawa, J., and D. P. Nayak. 1991. Two signals mediate nuclear localization of influenza virus (A/WSN/33) polymerase basic protein 2. J. Virol. 65:245-253.
27. Naffakh, N., P. Massin, and S. van der Werf. 2001. The transcription/replication activity of the polymerase of influenza A viruses is not correlated with the level of proteolysis induced by the the PA subunit. Virology 285:244-252.
28. Nath, S. T., and D. P. Nayak. 1990. Function of two discrete regions is required for nuclear localization of polymerase basic protein 1 I of A/WSN/33 influenza virus (H1N1). Mol. Cell. Biol. 10:4139-4145.
29. Neumann, G., M. R. Castrucci, and Y. Kawaoka. 1997. Import and export of influenza virus nucleoprotein. J. Virol. 71:9690-9700.
30. Neumann, G., T. Watanabe, H. Ito, S. Watanabe, H. Goto, P. Gao, M. Hugues, D. R. Perea, R. Donis, E. Hoffmann, G. Hobom, and Y. Kawaoka. 1999. Generation of influenza A viruses entirely from cloned cDNAs. Proc. Natl. Acad. Sci. USA 96:9345-9350.
31. Nieto, A., S. de la Luna, J. Bárcena, A. Portela, and J. Ortín. 1994. Complex structure of the nuclear translocation signal of the influenza virus polymerase the PA subunit. J. Gen. Virol. 75:29-36.
32. Nieto, A., S. de la Luna, J. Bárcena, A. Portela, J. Valcárcel, J. A. Melero, and J. Ortín. 1992. Nuclear transport of influenza virus polymerase PA protein. Virus Res. 24:65-75.
33. Perales, B., J. J. Sanz-Ezquerro, P. Gastaminza, J. Ortega, J. Fernandez-Santarén, J. Ortín, and A. Nieto. 2000. The replication activity of influenza virus polymerase is linked to the capacity of the PA subunit to induce proteolysis. J. Virol. 74:1307-1312.
34. Perez, D. R., and R. O. Donis. 1995. A 48-amino-acid region of influenza A virus PB1 protein is sufficient for complex formation with PA. J. Virol. 69:6932-6939.
35. Poch, O., I. Sauvaget, M. Delarue, and N. Tordo. 1990. Identification of four conserved motifs among the RNA-dependent polymerase encoding elements. EMBO J. 8:3867-3874.
36. + mRNA in vitro. J. Virol. 73:109-114.
37. Privalsky, M. L., and E. E. Penhoet. 1977. Phosphorylated protein component present in influenza virions. J. Virol. 24:401-405.
38. Sanz-Ezquerro, J. J., S. de la Luna, J. Ortín, and A. Nieto. 1995. Individual expression of influenza virus PA protein induces degradation of coexpressed proteins. J. Virol. 69:2420-2426.
39. Sanz-Ezquerro, J. J., J. Férnandez-Santarén, T. Sierra, T. Aragón, J. Ortega, J. Ortin, G. L. Smith, and A. Nieto. 1998. The PA influenza virus polymerase subunit is a phosphorylated protein. J. Gen. Virol. 79:471-478.
40. Sanz-Ezquerro, J. J., T. Zürcher, S. de la Luna, J. Ortin, and A. Nieto. 1996. The amino-terminal one-third of the influenza virus PA protein is responsible for the induction of proteolysis. J. Virol. 70:1905-1911.
41. Smith, G. L., J. Z. Levin, P. Palese, and B. Moss. 1987. Synthesis and cellular location of the ten influenza polypeptides individually expressed by recombinant vaccinia viruses. Virology 160:336-345.
42. Tiley, L. S., M. Hagen, J. T. Matthews, and M. Krystal. 1994. Sequencespecific binding of the influenza virus RNA polymerase to sequences located at the 5′ ends of the viral RNAs. J. Virol. 68:5108-5116.
43. Toyoda, T., D. M. Adyshev, M. Kobayashi, A. Iwata, and A. Ishihama. 1996. Molecular assembly of the influenza virus RNA polymerase: determination of the subunit-subunit contact sites. J. Gen. Virol. 77:2149-2157.
44. Ulmanen, I., B. A. Broni, and R. M. Krug. 1981. Role of two of the influenza virus core P proteins in recognizing cap 1 structures (m7GpppNm) on RNAs and in initiating viral RNA transcription. Proc. Natl. Acad. Sci. USA 78:7355-7359.
45. Whittaker, G., I. Kemler, and A. Helenius. 1995. Hyperphosphorylation of mutant influenza virus matrix protein, M1, causes its retention in the nucleus. J. Virol. 69:439-445.