The host-dependent interaction of α-importins with influenza PB2 polymerase subunit is required for virus RNA replication

PLoS ONE

Volumn 3, Issue 12, 2008, Pages

  Resa Infante, Patricia ^a,b   Jorba, Núria ^a,b   Zamarreño, Noelia ^a,b   Fernández, Yolanda ^a,b   Juárez, Silvia ^a,b   Ortín, Juan ^a,b  

^a CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

^b INSTITUTO DE SALUD CARLOS III   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

KARYOPHERIN ALPHA; MUTANT PROTEIN; RIBONUCLEOPROTEIN; RNA POLYMERASE; RNA POLYMERASE PA SUBUNIT; RNA POLYMERASE PB1 SUBUNIT; RNA POLYMERASE PB2 SUBUNIT; UNCLASSIFIED DRUG; VIRUS ENZYME; VIRUS RNA; ISOPROTEIN; PB2 PROTEIN, INFLUENZA VIRUS; PROTEIN SUBUNIT; RECOMBINANT PROTEIN; VIRUS PROTEIN;

ARTICLE; CELL NUCLEUS; CELL STRAIN HEK293; COMPLEX FORMATION; CONTROLLED STUDY; HELA CELL; HUMAN; HUMAN CELL; INFLUENZA VIRUS A H5N1; INFLUENZA VIRUS A H5N2; NONHUMAN; PHENOTYPE; PROTEIN AGGREGATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; REPLICON; RNA REPLICATION; VIRUS CELL INTERACTION; VIRUS REPLICATION; VIRUS STRAIN; VIRUS VIRULENCE; AMINO ACID SEQUENCE; BIOSYNTHESIS; CELL LINE; CHEMISTRY; ENZYMOLOGY; GENETICS; INTRACELLULAR SPACE; METABOLISM; MOLECULAR GENETICS; MUTATION; NUCLEAR LOCALIZATION SIGNAL; ORTHOMYXOVIRUS; PHYSIOLOGY; PROTEIN BINDING; PROTEIN TRANSPORT; SPECIES DIFFERENCE;

AVES; ORTHOMYXOVIRIDAE;

ALPHA KARYOPHERINS; AMINO ACID SEQUENCE; CELL LINE; HUMANS; INTRACELLULAR SPACE; MOLECULAR SEQUENCE DATA; MUTANT PROTEINS; MUTATION; NUCLEAR LOCALIZATION SIGNALS; ORTHOMYXOVIRIDAE; PROTEIN BINDING; PROTEIN ISOFORMS; PROTEIN SUBUNITS; PROTEIN TRANSPORT; RECOMBINANT PROTEINS; RIBONUCLEOPROTEINS; RNA, VIRAL; SPECIES SPECIFICITY; VIRAL PROTEINS; VIRUS REPLICATION;

EID: 57549086823     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0003904     Document Type: Article

References (42)

1. Elton D, Digard P, Tiley L, Ortín J (2005) Structure and function of the influenza virus RNP. In: Kawaoka Y, ed. Current Topics in Influenza Virology. Norfolk: Horizon Scientific Press. pp 1-92.
2. Neumann G, Brownlee GG, Fodor E, Kawaoka Y (2004) Orthomyxovirus replication, transcription, and polyadenylation. Curr Top Microbiol Immunol 283: 121-143.
3. Palese P, Shaw M (2006) Orthomyxoviridae: the viruses and their replication. In: Knipe DM, Howley PM, eds. Fields Virology 5th edition. Philadelphia: Lippincott Williams & Wilkins. pp 1647-1689.
4. Martín-Benito J, Area E, Ortega J, Llorca O, Valpuesta JM, et al. (2001) Three dimensional reconstruction of a recombinant influenza virus ribonucleoprotein particle. EMBO Reports 2: 313-317.
5. Area E, Martín-Benito J, Gastaminza P, Torreira E, Valpuesta JM, et al. (2004) Three-dimensional structure of the influenza virus RNA polymerase: localization of subunit domains. Proc Natl Acad Sci USA 101: 308-313.
6. Torreira E, Schoehn G, Fernández Y, Jorba N, Ruigrok RW, et al. (2007) Three-dimensional model for the isolated influenza virus polymerase heterotrimer. Nucleic Acids Res 35: 3774-3783.
7. Mukaigawa J, Nayak DP (1991) Two signals mediate nuclear localization of influenza virus (A/WSN/33) polymerase basic protein 2. J Virol 65: 245-253.
8. Nath ST, Nayak DP (1990) Function of two discrete regions is required for nuclear localization of polymerase basic protein 1 of A/WSN/33 influenza virus (H1N1). Mol Cell Biol 10: 4139-4145.
9. Nieto A, de la Luna S, Bárcena J, Portela A, Ortín J (1994) Complex structure of the nuclear translocation signal of the influenza virus polymerase PA subunit. J Gen Virol 75: 29-36.
10. Tarendeau F, Boudet J, Guilligay D, Mas PJ, Bougault CM, et al. (2007) Structure and nuclear import function of the C-terminal domain of influenza virus polymerase PB2 subunit. Nat Struct Mol Biol 14: 229-233.
11. Fodor E, Smith M (2004) The PA subunit is required for efficient nuclear accumulation of the PB1 subunit of the influenza A virus RNA polymerase complex. J Virol 78: 9144-9153.
12. Deng T, Engelhardt OG, Thomas B, Akoulitchev AV, Brownlee GG, et al. (2006) The role of Ran Binding Protein 5 (RanBP5) in the nuclear import and assembly of the influenza virus RNA polymerase complex. J Virol 80: 11911-11919.
13. Deng T, Sharps J, Fodor E, Brownlee GG (2005) In vitro assembly of PB2 with a PB1-PA dimer supports a new model of assembly of influenza A virus polymerase subunits into a functional trimeric complex. J Virol 79: 8669-8674.
14. Momose F, Naito T, Yano K, Sugimoto S, Morikawa Y, et al. (2002) Identification of Hsp90 as a stimulatory host factor involved in influenza virus RNA synthesis. J Biol Chem 277: 45306-45314.
15. Naito T, Momose F, Kawaguchi A, Nagata K (2007) Involvement of Hsp90 in assembly and nuclear import of influenza virus RNA polymerase subunits. J Virol 81: 1339-1349.
16. Jorba N, Juarez S, Torreira E, Gastaminza P, Zamarrenño N, et al. (2008) Analysis of the interaction of influenza virus polymerase complex with human cell factors. Proteomics 8: 2077-2088.
17. Gabriel G, Herwig A, Klenk HD (2008) Interaction of Polymerase Subunit PB2 and NP with Importin alpha1 Is a Determinant of Host Range of Influenza A Virus. PLoS Pathog 4: e11.
18. Ortega J, Martín-Benito J, Zürcher T, Valpuesta JM, Carrascosa JL, et al. (2000) Ultrastructural and functional analyses of of recombinant influenza virus ribonucleoproteins suggest dimerization of nucleoprotein during virus amplification. J Virol 74: 156-163.
19. Mena I, de la Luna S, Albo C, Martín J, Nieto A, et al. (1994) Synthesis of biologically active influenza virus core proteins using a vaccinia-T7 RNA polymerase expression system. J Gen Virol 75: 2109-2114.
20. Perales B, Ortín J (1997) The influenza A virus PB2 polymerase subunit is required for the replication of viral RNA. J Virol 71: 1381-1385.
21. Almond JW (1977) A single gene determines the host range of influenza virus. Nature 270: 617-618.
22. Subbarao EK, London W, Murphy BR (1993) A single amino acid in the PB2 gene of influenza A virus is a determinant of host range. J Virol 67: 1761-1764.
23. Labadie K, Dos Santos Afonso E, Rameix-Welti MA, van der Werf S, Naffakh N (2007) Host-range determinants on the PB2 protein of influenza A viruses control the interaction between the viral polymerase and nucleoprotein in human cells. Virology 362: 271-282.
24. Gastaminza P, Perales B, Falcón AM, Ortín J (2003) Influenza virus mutants in the N-terminal region of PB2 protein are affected in virus RNA replication but not transcription. J Virol 76: 5098-5108.
25. Lee MT, Bishop K, Medcalf L, Elton D, Digard P, et al. (2002) Definition of the minimal viral components required for the initiation of unprimed RNA synthesis by influenza virus RNA polymerase. Nucleic Acids Res 30: 429-438.
26. Finkelstein DB, Mukatira S, Mehta PK, Obenauer JC, Su X, et al. (2007) Persistent host markers in pandemic and H5N1 influenza viruses. J Virol 81: 10292-10299.
27. Gabriel G, Dauber B, Wolff T, Planz O, Klenk HD, et al. (2005) The viral polymerase mediates adaptation of an avian influenza virus to a mammalian host. Proc Natl Acad Sci U S A 102: 18590-18595.
28. Li Z, Chen H, Jiao P, Deng G, Tian G, et al. (2005) Molecular basis of replication of duck H5N1 influenza viruses in a mammalian mouse model. J Virol 79: 12058-12064.
29. Rigaut G, Shevchenko A, Rutz B, Wilm M, Mann M, et al. (1999) A generic protein purification method for protein complex characterization and proteome exploration. Nat Biotechnol 17: 1030-1032.
30. Naffakh N, Tomoiu A, Rameix-Welti MA, van der Werf S (2008) Host restriction of avian influenza viruses at the level of the ribonucleoproteins. Ann Rev Microbiology 62: 403-424.
31. Ortín J, Nájera R, López C, Dávila M, Domingo E (1980) Genetic variability of Hong Kong (H3N2) influenza viruses: spontaneous mutations and their location in the viral genome. Gene 11: 319-331.
32. Fuerst TR, Earl PL, Moss B (1987) Use of a hybrid vaccinia virus-T7 RNA polymerase system for expression of target genes. Mol Cell Biol 7: 2538-2544.
33. Jorba N, Area E, Ortín J (2008) Oligomerisation of the influenza virus polymerase complex in vivo. J Gen Virol 89: 520-524.
34. Falcón AM, Marión RM, Zürcher T, Gómez P, Portela A, et al. (2004) Defective RNA replication and late gene expression in temperature-sensitive (A/Victoria/ 3/75) influenza viruses expressing deleted forms of NS1 protein. J Virol 78: 3880-3888.
35. Neumann G, Watanabe T, Ito H, Watanabe S, Goto H, et al. (1999) Generation of influenza A viruses entirely from cloned cDNAs. Proc Natl Acad Sci U S A 96: 9345-9350.
36. Bárcena J, Ochoa M, de la Luna S, Melero JA, Nieto A, et al. (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.
37. Ochoa M, Bárcena J, de la Luna S, Melero JA, Douglas AR, et al. (1995) Epitope mapping of cross-reactive monoclonal antibodies specific for the influenza A virus PA and PB2 polypeptides. Virus Res 37: 305-315.
38. Wigler M, Pellicer A, Silverstein S, Axel R, Urlaub G, et al. (1979) DNA-mediated transfer of the adenine phosphoribosyltransferase locus into mammalian cells. Proc Natl Acad Sci U S A 76: 1373-1376.
39. Marión RM, Zürcher T, de la Luna S, Ortín J (1997) Influenza virus NS1 protein interacts with viral transcription-replication complexes in vivo. J Gen Virol 78: 2447-2451.
40. Villacé P, Marión RM, Ortín J (2004) The composition of Staufen-containing RNA granules from human cells indicate a role in the regulated transport and translation of messenger RNAs. Nucleic Acids Res 32: 2411-2420.
41. Guilligay D, Tarendeau F, Resa-Infante P, Coloma R, Crepin T, et al. (2008) The structural basis for cap-binding by influenza virus polymerase subunit PB2. Nat Struct Mol Biol 15: 500-506.
42. Zhang J, Zenobi R (2004) Matrix-dependent cationization in MALDI mass spectrometry. J Mass Spectrom 39: 808-816.