Species-specific contribution of the four C-terminal amino acids of influenza a virus NS1 protein to virulence

Journal of Virology

Volumn 84, Issue 13, 2010, Pages 6733-6747

  Soubies, Sébastien M ^a   Volmer, Christelle ^a   Croville, Guillaume ^a   Loupias, Josianne ^a   Peralta, Brigitte ^a   Costes, Pierrette ^a   Lacroux, Caroline ^a   Guérin, Jean Luc ^a   Volmer, Romain ^a  

^a UNIVERSITÉ DE TOULOUSE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

INTERFERON; NONSTRUCTURAL PROTEIN 1;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL GROWTH; CONTROLLED STUDY; DUCK; FEMALE; HUMAN; HUMAN CELL; INFLUENZA VIRUS A; MOUSE; NONHUMAN; PHENOTYPE; PNEUMONIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN MOTIF; SPECIES DIFFERENCE; VIROGENESIS; VIRUS REPLICATION; VIRUS VIRULENCE;

AMINO ACIDS; ANIMALS; CELL LINE; DUCKS; GENETIC ENGINEERING; HUMANS; INFLUENZA A VIRUS; INFLUENZA IN BIRDS; LUNG; MICE; MUTANT PROTEINS; ORTHOMYXOVIRIDAE INFECTIONS; PROTEIN STRUCTURE, TERTIARY; RECOMBINATION, GENETIC; VIRAL NONSTRUCTURAL PROTEINS; VIRULENCE; VIRULENCE FACTORS; VIRUS REPLICATION;

ANAS; AVES; AVIAN INFLUENZA VIRUS; HUMAN INFLUENZA VIRUS; INFLUENZA A VIRUS; MUS; ORTHOMYXOVIRIDAE;

EID: 77953303859     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.02427-09     Document Type: Article

References (52)

1. Baskin, C. R., H. Bielefeldt-Ohmann, T. M. Tumpey, P. J. Sabourin, J. P. Long, A. Garcia-Sastre, A. E. Tolnay, R. Albrecht, J. A. Pyles, P. H. Olson, L. D. Aicher, E. R. Rosenzweig, K. Murali-Krishna, E. A. Clark, M. S. Kotur, J. L. Fornek, S. Proll, R. E. Palermo, C. L. Sabourin, and M. G. Katze. 2009. Early and sustained innate immune response defines pathology and death in nonhuman primates infected by highly pathogenic influenza virus. Proc. Natl. Acad. Sci. U. S. A. 106:3455-3460.
2. Chen, G. W., S. C. Chang, C. K. Mok, Y. L. Lo, Y. N. Kung, J. H. Huang, Y. H. Shih, J. Y. Wang, C. Chiang, C. J. Chen, and S. R. Shih. 2006. Genomic signatures of human versus avian influenza A viruses. Emerg. Infect. Dis. 12:1353-1360.
3. Chen, R., and E. C. Holmes. 2006. Avian influenza virus exhibits rapid evolutionary dynamics. Mol. Biol. Evol. 23:2336-2341.
4. Dittmann, J., S. Stertz, D. Grimm, J. Steel, A. Garcia-Sastre, O. Haller, and G. Kochs. 2008. Influenza A virus strains differ in sensitivity to the antiviral action of Mx-GTPase. J. Virol. 82:3624-3631.
5. Dugan, V. G., R. Chen, D. J. Spiro, N. Sengamalay, J. Zaborsky, E. Ghedin, J. Nolting, D. E. Swayne, J. A. Runstadler, G. M. Happ, D. A. Senne, R. Wang, R. D. Slemons, E. C. Holmes, and J. K. Taubenberger. 2008. The evolutionary genetics and emergence of avian influenza viruses in wild birds. PLoS Pathog. 4:e1000076.
6. Dundon, W., and I. Capua. 2009. A closer look at the NS1 of influenza virus. Viruses 1:1057-1072.
7. Dundon, W. G., A. Milani, G. Cattoli, and I. Capua. 2006. Progressive truncation of the non-structural 1 gene of H7N1 avian influenza viruses following extensive circulation in poultry. Virus Res. 119:171-176.
8. Dunn, G. P., A. T. Bruce, K. C. Sheehan, V. Shankaran, R. Uppaluri, J. D. Bui, M. S. Diamond, C. M. Koebel, C. Arthur, J. M. White, and R. D. Schreiber. 2005. A critical function for type I interferons in cancer immunoediting. Nat. Immunol. 6:722-729.
9. Falcón, A. M., R. M. Marion, T. Zurcher, P. Gomez, A. Portela, A. Nieto, and J. Ortin. 2004. Defective RNA replication and late gene expression in temperature-sensitive influenza viruses expressing deleted forms of the NS1 protein. J. Virol. 78:3880-3888.
10. Garten, R. J., C. T. Davis, C. A. Russell, B. Shu, S. Lindstrom, A. Balish, W. M. Sessions, X. Xu, E. Skepner, V. Deyde, M. Okomo-Adhiambo, L. Gubareva, J. Barnes, C. B. Smith, S. L. Emery, M. J. Hillman, P. Rivailler, J. Smagala, M. de Graaf, D. F. Burke, R. A. Fouchier, C. Pappas, C. M. Alpuche-Aranda, H. Lopez-Gatell, H. Olivera, I. Lopez, C. A. Myers, D. Faix, P. J. Blair, C. Yu, K. M. Keene, P. D. Dotson, Jr., D. Boxrud, A. R. Sambol, S. H. Abid, K. St. George, T. Bannerman, A. L. Moore, D. J. Stringer, P. Blevins, G. J. Demmler-Harrison, M. Ginsberg, P. Kriner, S. Waterman, S. Smole, H. F. Guevara, E. A. Belongia, P. A. Clark, S. T. Beatrice, R. Donis, J. Katz, L. Finelli, C. B. Bridges, M. Shaw, D. B. Jernigan, T. M. Uyeki, D. J. Smith, A. I. Klimov, and N. J. Cox. 2009. Antigenic and genetic characteristics of swine-origin 2009 A (H1N1) influenza viruses circulating in humans. Science 325:197-201.
11. Grimm, D., P. Staeheli, M. Hufbauer, I. Koerner, L. Martinez-Sobrido, A. Solorzano, A. Garcia-Sastre, O. Haller, and G. Kochs. 2007. Replication fitness determines high virulence of influenza A virus in mice carrying functional Mx1 resistance gene. Proc. Natl. Acad. Sci. U. S. A. 104:6806-6811.
12. Hale, B. G., R. E. Randall, J. Ortin, and D. Jackson. 2008. The multifunctional NS1 protein of influenza A viruses. J. Gen. Virol. 89:2359-2376.
13. Hale, B. G., J. Steel, B. Manicassamy, R. A. Medina, J. Ye, D. Hickman, A. C. Lowen, D. R. Perez, and A. Garcia-Sastre. Mutations in the NS1 C-terminal tail do not enhance replication or virulence of the 2009 pandemic H1N1 influenza A virus. J. Gen. Virol., in press.
14. Haller, O., H. Arnheiter, I. Gresser, and J. Lindenmann. 1981. Virus-specific interferon action. Protection of newborn Mx carriers against lethal infection with influenza virus. J. Exp. Med. 154:199-203.
15. Hatta, M., Y. Hatta, J. H. Kim, S. Watanabe, K. Shinya, T. Nguyen, P. S. Lien, Q. M. Le, and Y. Kawaoka. 2007. Growth of H5N1 influenza A viruses in the upper respiratory tracts of mice. PLoS Pathog. 3:1374-1379.
16. Hayman, A., S. Comely, A. Lackenby, L. C. Hartgroves, S. Goodbourn, J. W. McCauley, and W. S. Barclay. 2007. NS1 proteins of avian influenza A viruses can act as antagonists of the human alpha/beta interferon response. J. Virol. 81:2318-2327.
17. Hayman, A., S. Comely, A. Lackenby, S. Murphy, J. McCauley, S. Good-bourn, and W. Barclay. 2006. Variation in the ability of human influenza A viruses to induce and inhibit the IFN-beta pathway. Virology 347:52-64.
18. Herlocher, M. L., S. Elias, R. Truscon, S. Harrison, D. Mindell, C. Simon, and A. S. Monto. 2001. Ferrets as a transmission model for influenza: sequence changes in HA1 of type A (H3N2) virus. J. Infect. Dis. 184:542-546.
19. Hoffmann, E., G. Neumann, Y. Kawaoka, G. Hobom, and R. G. Webster. 2000. A DNA transfection system for generation of influenza A virus from eight plasmids. Proc. Natl. Acad. Sci. U. S. A. 97:6108-6113.
20. Hoffmann, E., J. Stech, Y. Guan, R. G. Webster, and D. R. Perez. 2001. Universal primer set for the full-length amplification of all influenza A viruses. Arch. Virol. 146:2275-2289.
21. Holzinger, D., C. Jorns, S. Stertz, S. Boisson-Dupuis, R. Thimme, M. Weidmann, J. L. Casanova, O. Haller, and G. Kochs. 2007. Induction of MxA gene expression by influenza A virus requires type I or type III interferon signaling. J. Virol. 81:7776-7785.
22. Horimoto, T., and Y. Kawaoka. 2001. Pandemic threat posed by avian influenza A viruses. Clin. Microbiol. Rev. 14:129-149.
23. Ito, T., Y. Suzuki, T. Suzuki, A. Takada, T. Horimoto, K. Wells, H. Kida, K. Otsuki, M. Kiso, H. Ishida, and Y. Kawaoka. 2000. Recognition of Nglycolylneuraminic acid linked to galactose by the alpha2,3 linkage is associated with intestinal replication of influenza A virus in ducks. J. Virol. 74:9300-9305.
24. Jackson, D., M. J. Hossain, D. Hickman, D. R. Perez, and R. A. Lamb. 2008. A new influenza virus virulence determinant: the NS1 protein four C-terminal residues modulate pathogenicity. Proc. Natl. Acad. Sci. U. S. A. 105:4381-4386.
25. Kawaoka, Y., O. T. Gorman, T. Ito, K. Wells, R. O. Donis, M. R. Castrucci, I. Donatelli, and R. G. Webster. 1998. Influence of host species on the evolution of the nonstructural (NS) gene of influenza A viruses. Virus Res. 55:143-156.
26. Kida, H., R. Yanagawa, and Y. Matsuoka. 1980. Duck influenza lacking evidence of disease signs and immune response. Infect. Immun. 30:547-553.
27. Kobasa, D., S. M. Jones, K. Shinya, J. C. Kash, J. Copps, H. Ebihara, Y. Hatta, J. H. Kim, P. Halfmann, M. Hatta, F. Feldmann, J. B. Alimonti, L. Fernando, Y. Li, M. G. Katze, H. Feldmann, and Y. Kawaoka. 2007. Aberrant innate immune response in lethal infection of macaques with the 1918 influenza virus. Nature 445:319-323.
28. Min, J. Y., and R. M. Krug. 2006. The primary function of RNA binding by the influenza A virus NS1 protein in infected cells: inhibiting the 2′-5′ oligo(A) synthetase/RNase L pathway. Proc. Natl. Acad. Sci. U. S. A. 103:7100-7105.
29. Min, J. Y., S. Li, G. C. Sen, and R. M. Krug. 2007. A site on the influenza A virus NS1 protein mediates both inhibition of PKR activation and temporal regulation of viral RNA synthesis. Virology 363:236-243.
30. Munster, V. J., E. de Wit, D. van Riel, W. E. Beyer, G. F. Rimmelzwaan, A. D. Osterhaus, T. Kuiken, and R. A. Fouchier. 2007. The molecular basis of the pathogenicity of the Dutch highly pathogenic human influenza A H7N7 viruses. J. Infect. Dis. 196:258-265.
31. Neumann, G., T. Noda, and Y. Kawaoka. 2009. Emergence and pandemic potential of swine-origin H1N1 influenza virus. Nature 459:931-939.
32. Obenauer, J. C., J. Denson, P. K. Mehta, X. Su, S. Mukatira, D. B. Finkelstein, X. Xu, J. Wang, J. Ma, Y. Fan, K. M. Rakestraw, R. G. Webster, E. Hoffmann, S. Krauss, J. Zheng, Z. Zhang, and C. W. Naeve. 2006. Largescale sequence analysis of avian influenza isolates. Science 311:1576-1580.
33. Perrone, L. A., J. K. Plowden, A. Garcia-Sastre, J. M. Katz, and T. M. Tumpey. 2008. H5N1 and 1918 pandemic influenza virus infection results in early and excessive infiltration of macrophages and neutrophils in the lungs of mice. PLoS Pathog. 4:e1000115.
34. Petri, T., and N. J. Dimmock. 1981. Phosphorylation of influenza virus nucleoprotein in vivo. J. Gen. Virol. 57:185-190.
35. Pillai, S. P., D. L. Suarez, M. Pantin-Jackwood, and C. W. Lee. 2008. Pathogenicity and transmission studies of H5N2 parrot avian influenza virus of Mexican lineage in different poultry species. Vet. Microbiol. 129:48-57.
36. Rameix-Welti, M. A., A. Tomoiu, E. Dos Santos Afonso, S. van der Werf, and N. Naffakh. 2009. Avian influenza A virus polymerase association with nucleoprotein, but not polymerase assembly, is impaired in human cells during the course of infection. J. Virol. 83:1320-1331.
37. Salomon, R., P. Staeheli, G. Kochs, H. L. Yen, J. Franks, J. E. Rehg, R. G. Webster, and E. Hoffmann. 2007. Mx1 gene protects mice against the highly lethal human H5N1 influenza virus. Cell Cycle 6:2417-2421.
38. Schumacher, B., D. Bernasconi, U. Schultz, and P. Staeheli. 1994. The chicken Mx promoter contains an ISRE motif and confers interferon inducibility to a reporter gene in chick and monkey cells. Virology 203:144-148.
39. Seo, S. H., E. Hoffmann, and R. G. Webster. 2002. Lethal H5N1 influenza viruses escape host anti-viral cytokine responses. Nat. Med. 8:950-954.
40. Sommereyns, C., S. Paul, P. Staeheli, and T. Michiels. 2008. IFN-lambda (IFN-lambda) is expressed in a tissue-dependent fashion and primarily acts on epithelial cells in vivo. PLoS Pathog. 4:e1000017.
41. Sorrell, E. M., H. Wan, Y. Araya, H. Song, and D. R. Perez. 2009. Minimal molecular constraints for respiratory droplet transmission of an avian-human H9N2 influenza A virus. Proc. Natl. Acad. Sci. U. S. A. 106:7565-7570.
42. Soubies, S., C. Volmer, J. Guérin, and R. Volmer. 2010. Truncation of the NS1 protein converts a low pathogenic avian influenza virus into a strong interferon inducer in duck cells. Avian Dis. 54:527-531.
43. Spackman, E., D. E. Swayne, D. L. Suarez, D. A. Senne, J. C. Pedersen, M. L. Killian, J. Pasick, K. Handel, S. P. Pillai, C. W. Lee, D. Stallknecht, R. Slemons, H. S. Ip, and T. Deliberto. 2007. Characterization of low-pathogenicity H5N1 avian influenza viruses from North America. J. Virol. 81:11612-11619. (Pubitemid 47623793)
44. Steel, J., A. C. Lowen, S. Mubareka, and P. Palese. 2009. Transmission of influenza virus in a mammalian host is increased by PB2 amino acids 627K or 627E/701N. PLoS Pathog. 5:e1000252.
45. Subbarao, E. K., W. London, and B. R. Murphy. 1993. A single amino acid in the PB2 gene of influenza A virus is a determinant of host range. J. Virol. 67:1761-1764.
46. Szretter, K. J., S. Gangappa, J. A. Belser, H. Zeng, H. Chen, Y. Matsuoka, S. Sambhara, D. E. Swayne, T. M. Tumpey, and J. M. Katz. 2009. Early control of H5N1 influenza virus replication by the type I interferon response in mice. J. Virol. 83:5825-5834.
47. Tonikian, R., Y. Zhang, S. L. Sazinsky, B. Currell, J. H. Yeh, B. Reva, H. A. Held, B. A. Appleton, M. Evangelista, Y. Wu, X. Xin, A. C. Chan, S. Seshagiri, L. A. Lasky, C. Sander, C. Boone, G. D. Bader, and S. S. Sidhu. 2008. A specificity map for the PDZ domain family. PLoS Biol. 6:e239.
48. Tumpey, T. M., K. J. Szretter, N. Van Hoeven, J. M. Katz, G. Kochs, O. Haller, A. Garcia-Sastre, and P. Staeheli. 2007. The Mx1 gene protects mice against the pandemic 1918 and highly lethal human H5N1 influenza viruses. J. Virol. 81:10818-10821.
49. van der Goot, J. A., M. van Boven, A. Stegeman, S. G. van de Water, M. C. de Jong, and G. Koch. 2008. Transmission of highly pathogenic avian influenza H5N1 virus in Pekin ducks is significantly reduced by a genetically distant H5N2 vaccine. Virology 382:91-97.
50. Volmer, R., C. Monnet, and D. Gonzalez-Dunia. 2006. Borna disease virus blocks potentiation of presynaptic activity through inhibition of protein kinase C signaling. PLoS Pathog. 2:e19.
51. Webster, R. G., M. Yakhno, V. S. Hinshaw, W. J. Bean, and K. G. Murti. 1978. Intestinal influenza: replication and characterization of influenza viruses in ducks. Virology 84:268-278. (Pubitemid 8286072)
52. Yamada, S., Y. Suzuki, T. Suzuki, M. Q. Le, C. A. Nidom, Y. Sakai-Tagawa, Y. Muramoto, M. Ito, M. Kiso, T. Horimoto, K. Shinya, T. Sawada, M. Kiso, T. Usui, T. Murata, Y. Lin, A. Hay, L. F. Haire, D. J. Stevens, R. J. Russell, S. J. Gamblin, J. J. Skehel, and Y. Kawaoka. 2006. Haemagglutinin mutations responsible for the binding of H5N1 influenza A viruses to human-type receptors. Nature 444:378-382