Influenza Virus Virulence and Its Molecular Determinants

Advances in Virus Research

Volumn 65, Issue , 2005, Pages 121-145

  Noah, Diana L ^a   Krug, Robert M ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

VIRULENCE FACTOR; VIRUS PROTEIN;

ANIMAL; ARTICLE; GENETICS; HUMAN; IMMUNOLOGY; INFLUENZA; INFLUENZA VIRUS A; METABOLISM; PATHOGENICITY; VIRULENCE;

ANIMALS; HUMANS; INFLUENZA A VIRUS; INFLUENZA, HUMAN; VIRAL NONSTRUCTURAL PROTEINS; VIRULENCE; VIRULENCE FACTORS;

EID: 33644841402     PISSN: 00653527     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S0065-3527(05)65004-X     Document Type: Review

References (88)

1. Bender C., Hall H., Huang J., Klimov A., Cox N., Hay A., Gregory V., Cameron K., Lim W., and Subbarao K. Characterization of the surface proteins of influenza A (H5N1) viruses isolated from humans in 1997-1998. Virology 254 (1999) 115-123
2. Bright R.A., Cho D.S., Rowe T., and Katz J.M. Mechanisms of pathogenicity of influenza A (H5N1) viruses in mice. Avian Dis. 47 (2003) 1131-1134
3. Chen W., Calvo P.A., Malide D., Gibbs J., Schubert U., Bacik I., Basta S., O'Neill R., Schickli J., Palese P., Henklein P., Bennink J.R., and Yewdell J.W. A novel influenza A virus mitochondrial protein that induces cell death. Nat. Med. 7 (2001) 1306-1312
4. Chen Z., Li Y., and Krug R.M. Influenza A virus NS1 protein targets poly(A)-binding protein II of the cellular 3′-end processing machinery. EMBO J. 18 (1999) 2273-2283
5. Cheung C.Y., Poon L.L., Lau A.S., Luk W., Lau Y.L., Shortridge K.F., Gordon S., Guan Y., and Peiris J.S. Induction of proinflammatory cytokines in human macrophages by influenza A (H5N1) viruses: A mechanism for the unusual severity of human disease?. Lancet 360 (2002) 1831-1837
6. Chizhmakov I.V., Geraghty F.M., Ogden D.C., Hayhurst A., Antoniou M., and Hay A.J. Selective proton permeability and pH regulation of the influenza virus M2 channel expressed in mouse erythroleukaemia cells. J. Physiol. 494 (1996) 329-336
7. Claas E.C., Osterhaus A.D., van Beek R., De Jong J.C., Rimmelzwaan G.F., Senne D.A., Krauss S., Shortridge K.F., and Webster R.G. Human influenza A H5N1 virus related to a highly pathogenic avian influenza virus. Lancet 351 (1998) 472-477
8. Colman P.M., Varghese J.N., and Laver W.G. Structure of the catalytic and antigenic sites in influenza virus neuraminidase. Nature 303 (1983) 41-44
9. Cox N.J., and Subbarao K. Influenza. Lancet 354 (1999) 1277-1282
10. Crescenzo-Chaigne B., van der Werf S., and Naffakh N. Differential effect of nucleotide substitutions in the 3′ arm of the influenza A virus vRNA promoter on transcription/replication by avian and human polymerase complexes is related to the nature of PB2 amino acid 627. Virology 303 (2002) 240-252
11. Cros J.F., and Palese P. Trafficking of viral genomic RNA into and out of the nucleus: Influenza, Thogoto and Borna disease viruses. Virus Res. 95 (2003) 3-12
12. Falcon A.M., Marion R.M., Zurcher T., Gomez P., Portela A., Nieto A., and Ortin J. Defective RNA replication and late gene expression in temperature-sensitive influenza viruses expressing deleted forms of the NS1 protein. J Virol. 78 (2004) 3880-3888
13. Fechter P., Mingay L., Sharps J., Chambers A., Fodor E., and Brownlee G.G. Two aromatic residues in the PB2 subunit of influenza A RNA polymerase are crucial for cap binding. J. Biol. Chem. 278 (2003) 20381-20388
14. Florent G., Lobmann M., Beare A.S., and Zygraich N. RNAs of influenza virus recombinants derived from parents of known virulence for man. Arch. Virol. 54 (1977) 19-28
15. Garcia-Sastre A. Inhibition of interferon-mediated antiviral responses by influenza A viruses and other negative-strand RNA viruses. Virology 279 (2001) 375-384
16. Geiss G.K., Salvatore M., Tumpey T.M., Carter V.S., Wang X., Basler C.F., Taubenberger J.K., Bumgarner R.E., Palese P., Katze M.G., and Garcia-Sastre A. Cellular transcriptional profiling in influenza A virus-infected lung epithelial cells: The role of the nonstructural NS1 protein in the evasion of the host innate defense and its potential contribution to pandemic influenza. Proc. Natl. Acad. Sci. USA 99 (2002) 10736-10741
17. Goto H., and Kawaoka Y. A novel mechanism for the acquisition of virulence by a human influenza A virus. Proc. Natl. Acad. Sci. USA 95 (1998) 10224-10228
18. Goto H., Wells K., Takada A., and Kawaoka Y. Plasminogen-binding activity of neuraminidase determines the pathogenicity of influenza A virus. J. Virol. 75 (2001) 9297-9301
19. Govorkova E.A., Rehg J.E., Krauss S., Yen H.L., Guan Y., Peiris M., Nguyen T.D., Hanh T.H., Puthavathana P., Long H.T., Buranathai C., Lim W., Webster R.G., and Hoffmann E. Lethality to ferrets of H5N1 influenza viruses isolated from humans and poultry in 2004. J. Virol. 79 (2005) 2191-2198
20. Green D.R. Apoptotic pathways: Paper wraps stone blunts scissors. Cell 102 1 (2000) 1-4
21. Guan Y., Poon L.L., Cheung C.Y., Ellis T.M., Lim W., Lipatov A.S., Chan K.H., Sturm-Ramirez K.M., Cheung C.L., Leung Y.H.C., Yuen K.Y., Webster R.G., and Peiris J.S.M. H5N1 influenza: A protean pandemic threat. Proc. Natl. Acad. Sci. USA 101 (2004) 8156-8161
22. Gubareva L.V., Penn C.R., and Webster R.G. Inhibition of replication of avian influenza viruses by the neuraminidase inhibitor 4-guanidino-2,4-dideoxy-2,3-dehydro-N-acetylneuraminic acid. Virology 212 (1995) 323-330
23. Harvey R., Martin A.C., Zambon M., and Barclay W.S. Restrictions to the adaptation of influenza a virus H5 hemagglutinin to the human host. J. Virol. 78 (2004) 502-507
24. Hatta M., Gao P., Halfmann P., and Kawaoka Y. Molecular basis for high virulence of Hong Kong H5N1 influenza A viruses. Science 293 (2001) 1840-1842
25. Hayden F.G., Osterhaus A.D., Treanor J.J., Fleming D.M., Aoki F.Y., Nicholson K.G., Bohnen A.M., Hirst H.M., Keene O., and Wightman K. Efficacy and safety of the neuraminidase inhibitor zanamivir in the treatment of influenzavirus infections. GG167 Influenza Study Group. N. Engl. J. Med. 337 (1997) 874-880
26. Hayden F.G., Treanor J.J., Betts R.F., Lobo M., Esinhart J.D., and Hussey E.K. Safety and efficacy of the neuraminidase inhibitor GG167 in experimental human influenza. JAMA 275 (1996) 295-299
27. Hinshaw V.S., Olsen C.W., Dybdahl-Sissoko N., and Evans D. Apoptosis: A mechanism of cell killing by influenza A and B viruses. J. Virol. 68 (1994) 3667-3673
28. Hulse D.J., Webster R.G., Russell R.J., and Perez D.R. Molecular determinants within the surface proteins involved in the pathogenicity of H5N1 influenza viruses in chickens. J. Virol. 78 (2004) 9954-9964
29. Kawaoka Y., and Webster R.G. Interplay between carbohydrate in the stalk and the length of the connecting peptide determines the cleavability of influenza virus hemagglutinin. J. Virol. 63 (1989) 3296-3300
30. Kim C.U., Lew W., Williams M.A., Liu H., Zhang L., Swaminathan S., Bischofberger N., Chen M.S., Mendel D.B., Tai C.Y., Laver W.G., and Stevens R.C. Influenza neuraminidase inhibitors possessing a novel hydrophobic interaction in the enzyme active site: Design, synthesis and structural analysis of carbocyclic sialiac acid analogues with potent anti-influenza activity. J. Amer. Chem. Soc. 119 (1997) 681-690
31. Kim M.J., Latham A.G., and Krug R.M. Human influenza viruses activate an interferon-independent transcription of cellular antiviral genes: Outcome with influenza A virus is unique. Proc. Natl. Acad. Sci. USA 99 (2002) 10096-10101
32. Kiso M., Mitamura K., Sakai-Tagawa Y., Shiraishi K., Kawakami C., Kimura K., Hayden F.G., Sugaya N., and Kawaoka Y. Resistant influenza A viruses in children treated with oseltamivir: Descriptive study. Lancet 364 (2004) 759-765
33. Kobasa D., Takada A., Shinya K., Hatta M., Halfmann P., Theriault S., Suzuki H., Nishimura H., Mitamura K., Sugaya N., Usui T., Murata T., Maeda Y., Watanabe S., Suresh M., Suzuki T., Suzuki Y., Feldmann H., and Kawaoka Y. Enhanced virulence of influenza A viruses with the haemagglutinin of the 1918 pandemic virus. Nature 431 (2004) 703-707
34. Krug R.M., Alonso-Caplen F.V., Julkunen I., and Katze M.G. Expression and replication of the influenza virus genome. In: Krug R.M. (Ed). "The Influenza Viruses" (1989), Plenum Press, New York 89-152
35. Krug R.M., Shaw M., Broni B., Shapiro G., and Haller O. Inhibition of influenza viral mRNA synthesis in cells expressing the interferon-induced Mx gene product. J. Virol. 56 (1985) 201-206
36. Krug R.M., Yuan W., Noah D.L., and Latham A.G. Intracellular warfare between human influenza viruses and human cells: The roles of the viral NS1 protein. Virology 309 (2003) 181-189
37. Lamb, and Krug R. Orthomyxoviridae: The viruses and their replication. In: Knipe D.M., and Howley P.M. (Eds). "Fields Virology" (2001), Lippincott, Williams, and Wilkins, Philadelphia 1487-1531
38. Lamb R.A., Holsinger L.J., and Pinto L.H. The influenza A virus M2 ion channel protein and its role in the influenza virus life cycle. In: Wimmer E. (Ed). "Receptor-Mediated Virus Entry into Cells" (1994), Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY 303-312
39. Li M.L., Rao P., and Krug R.M. The active sites of the influenza cap-dependent endonuclease are on different polymerase subunits. EMBO J. 20 (2001) 2078-2086
40. Li Y., Chen Z.Y., Wang W., Baker C.C., and Krug R.M. The 3′-end-processing factor CPSF is required for the splicing of single-intron pre-mRNAs in vivo. RNA 7 (2001) 920-931
41. Linnemann Jr. C.C., Shea L., Partin J.C., Schubert W.K., and Schiff G.M. Reye's syndrome: Epidemiologic and viral studies, 1963-1974. Am. J. Epidemiol. 101 (1975) 517-526
42. Lipatov A.S., Andreansky S., Webby R.J., Hulse D.J., Rehg J.E., Krauss S., Perez D.R., Doherty P.C., Webster R.G., and Sangster M.Y. Pathogenesis of Hong Kong H5N1 influenza virus NS gene reassortants in mice: The role of cytokines and B- and T-cell responses. J. Gen. Virol. 86 (2005) 1121-1130
43. Loo Y.-M., Fredericksen B., and Gale M.J. Requirement of RIG-I in signaling the host response to virus infection (2005) Submitted for publication.
44. Marcus P.I., Rojek J.M., and Sekellick M.J. Interferon induction and/or production and its suppression by influenza A viruses. J. Virol. 79 (2005) 2880-2890
45. Martin K., and Helenius A. Nuclear transport of influenza virus ribonucleoproteins: The viral matrix protein (M1) promotes export and inhibits import. Cell 67 (1991) 117-130
46. Mase M., Tsukamoto K., Imada T., Imai K., Tanimura N., Nakamura K., Yamamoto Y., Hitomi T., Kira T., Nakai T., Kiso M., Horimoto T., Kawaoka Y., and Yamaguchi S. Characterization of H5N1 influenza A viruses isolated during the 2003-2004 influenza outbreaks in Japan. Virology 332 (2005) 167-176
47. Massin P., van der Werf S., and Naffakh N. Residue 627 of PB2 is a determinant of cold sensitivity in RNA replication of avian influenza viruses. J. Virol. 75 (2001) 5398-5404
48. Matrosovich M.N., Matrosovich T.Y., Gray T., Roberts N.A., and Klenk H.D. Human and avian influenza viruses target different cell types in cultures of human airway epithelium. Proc. Natl. Acad. Sci. USA 101 (2004) 4620-4624
49. McNicholl I.R., and McNicholl J.J. Neuraminidase inhibitors: Zanamivir and oseltamivir. Ann. Pharmacother. 35 (2001) 57-70
50. Mendel D.B., Tai C.Y., Escarpe P.A., Li W., Sidwell R.W., Huffman J.H., Sweet C., Jakeman K.J., Merson J., Lacy S.A., Lew W., Williams M.A., Zhang L., Chen M.S., Bischofberger N., and Kim C.U. Oral administration of a prodrug of the influenza virus neuraminidase inhibitor GS 4071 protects mice and ferrets against influenza infection. Antimicrob. Agents Chemother. 42 (1998) 640-646
51. Mould J.A., Drury J.E., Frings S.M., Kaupp U.B., Pekosz A., Lamb R.A., and Pinto L.H. Permeation and activation of the M2 ion channel of influenza A virus. J. Biol. Chem. 275 (2000) 31038-31050
52. Nemeroff M.E., Barabino S.M., Li Y., Keller W., and Krug R.M. Influenza virus NS1 protein interacts with the cellular 30 kDa subunit of CPSF and inhibits 3′ end formation of cellular pre-mRNAs. Mol. Cell 1 (1998) 991-1000
53. Noah D.L., Twu K.Y., and Krug R.M. Cellular antiviral responses against influenza A virus are countered at the posttranscriptional level by the viral NS1A protein via its binding to a cellular protein required for the 3′ end processing of cellular pre-mRNAS. Virology 307 (2003) 386-395
54. O'Neill R.E., Talon J., and Palese P. The influenza virus NEP (NS2 protein) mediates the nuclear export of viral ribonucleoproteins. EMBO J. 17 (1998) 288-296
55. Ohtsu Y., Honda Y., Sakata Y., Kato H., and Toyoda T. Fine mapping of the subunit binding sites of influenza virus RNA polymerase. Microbiol. Immunol. 46 (2002) 167-175
56. Oxford J.S., McGeoch D.J., Schild G.C., and Beare A.S. Analysis of virion RNA segments and polypeptides of influenza A virus recombinants of defined virulence. Nature 273 (1978) 778-779
57. Pinto L.H., Holsinger L.J., and Lamb R.A. Influenza virus M2 protein has ion channel activity. Cell 69 (1992) 517-528
58. Prevention. Background on Influenza (2005). http://www.cdc.gov/flu/background/professionals/background
59. Puthavathana P., Auewarakul P., Charoenying P.C., Sangsiriwut K., Pooruk P., Boonnak K., Khanyok R., Thawachsupa P., Kijphati R., and Sawanpanyalert P. Molecular characterization of the complete genome of human influenza H5N1 virus isolates from Thailand. J. Gen. Virol. 86 (2005) 423-433
60. Rao P., Yuan W., and Krug R.M. Crucial role of CA cleavage sites in the cap-snatching mechanism for initiating viral mRNA synthesis. EMBO J. 22 (2003) 1188-1198
61. Reid A.H., Taubenberger J.K., and Fanning T.G. The 1918 Spanish influenza: Integrating history and biology. Microbes Infect. 3 (2001) 81-87
62. Rott R., Orlich M., and Scholtissek C. Correlation of pathogenicity and gene constellation of influenza A viruses. III. Nonpathogenic recombinants derived from highly pathogenic parent strains. J. Gen. Virol. 44 (1979) 471-477
63. Ryan D.M., Ticehurst J., Dempsey M.H., and Penn C.R. Inhibition of influenza virus replication in mice by GG167 (4-guanidino-2,4-dideoxy-2,3-dehydro-N-acetylneuraminic acid) is consistent with extracellular activity of viral neuraminidase (sialidase). Antimicrob. Agents Chemother. 38 (1994) 2270-2275
64. Schultz-Cherry S., and Hinshaw V.S. Influenza virus neuraminidase activates latent transforming growth factor beta. J. Virol. 70 (1996) 8624-8629
65. Seo S.H., Hoffmann E., and Webster R.G. Lethal H5N1 influenza viruses escape host antiviral cytokine responses. Nat. Med. 8 (2002) 950-954
66. Shih S.R., and Krug R.M. Novel exploitation of a nuclear function by influenza virus: The cellular SF2/ASF splicing factor controls the amount of the essential viral M2 ion channel protein in infected cells. EMBO J. 15 (1996) 5415-5427
67. Shih S.R., Nemeroff M.E., and Krug R.M. The choice of alternative 5′ splice sites in influenza virus M1 mRNA is regulated by the viral polymerase complex. Proc. Natl. Acad. Sci. USA 92 (1995) 6324-6328
68. Shimuzu K., Iguchi A., Gomyou R., and Onu Y. Influenza virus inhibits cleavage of the HSP70 pre-MRNAs at the polyadenylation site. Virology 254 (1999) 213-219
69. Shinya K., Hamm S., Hatta M., Ito H., Ito T., and Kawaoka Y. PB2 amino acid at position 627 affects replicative efficiency, but not cell tropism, of Hong Kong H5N1 influenza A viruses in mice. Virology 320 (2004) 258-266
70. Skehel J.J., Hay A.J., and Armstrong J.A. On the mechanism of inhibition of influenza virus replication by amantadine hydrochloride. J. Gen. Virol. 38 (1978) 97-110
71. Staeheli P., Horisberger M.A., and Haller O. Mx-dependent resistance to influenza viruses is induced by mouse interferons alpha and beta but not gamma. Virology 132 (1984) 456-461
72. Stieneke-Grober A., Vey M., Angliker H., Shaw E., Thomas G., Roberts C., Klenk H.D., and Garten W. Influenza virus hemagglutinin with multibasic cleavage site is activated by furin, a subtilisin-like endoprotease. EMBO J. 11 (1992) 2407-2414
73. Suarez D.L., Perdue M.L., Cox N., Rowe T., Bender C., Huang J., and Swayne D.E. Comparisons of highly virulent H5N1 influenza A viruses isolated from humans and chickens from Hong Kong. J. Virol. 72 (1998) 6678-6688
74. Subbarao K., Klimov A., Katz J., Regnery H., Lim W., Hall H., Perdue M., Swayne D., Bender C., Huang J., Hemphill M., Rowe T., Shaw M., Xu X., Fukuda K., and Cox N. Characterization of an avian influenza A (H5N1) virus isolated from a child with a fatal respiratory illness. Science 279 (1998) 393-396
75. Sumpter Jr. R., Loo Y.M., Foy E., Li K., Yoneyama M., Fujita T., Lemon S.M., and Gale Jr. M. Regulating intracellular antiviral defense and permissiveness to hepatitis C virus RNA replication through a cellular RNA helicase, RIG-I. J. Virol. 79 (2005) 2689-2699
76. Suzuki H., Saito R., Masuda H., Oshitani H., Sato M., and Sato I. Emergence of amantadine-resistant influenza A viruses: Epidemiological study. J. Infect. Chemother. 9 (2003) 195-200
77. Talon J., Horvath C.M., Polley R., Basler C.F., Muster T., Palese P., and Garcia-Sastre A. Activation of interferon regulatory factor 3 is inhibited by the influenza A virus NS1 protein. J. Virol. 74 (2000) 7989-7996
78. To K.F., Chan P.K., Chan K.F., Lee W.K., Lam W.Y., Wong K.F., Tang N.L., Tsang D.N., Sung R.Y., Buckley T.A., Tam J.S., and Cheng A.F. Pathology of fatal human infection associated with avian influenza A H5N1 virus. J. Med. Virol. 63 (2001) 242-246
79. Tran T.H., Nguyen T.L., Nguyen T.D., Luong T.S., Pham P.M., Nguyen V.C., Pham T.S., Vo C.D., Le T.Q., Ngo T.T., Dao B.K., Le P.P., Nguyen T.T., Hoang T.L., Cao V.T., Le T.G., Nguyen D.T., Le H.N., Nguyen K.T., Le H.S., Le V.T., Christiane D., Tran T.T., Menno de J., Schultsz C., Cheng P., Lim W., Horby P., Farrar J., World Health, Organization International Avian, Influenza Investigative, and Team. Avian influenza A (H5N1) in 10 patients in Vietnam. New Engl. J. Med. 350 (2004) 1179-1188
80. Ungchusak K., Auewarakul P., Dowell S.F., Kitphati R., Auwanit W., Puthavathana P., Uiprasertkul M., Boonnak K., Pittayawonganon C., Cox N.J., Zaki S.R., Thawatsupha P., Chittaganpitch M., Khontong R., Simmerman J.M., and Chunsutthiwat S. Probable person-to-person transmission of avian influenza A (H5N1). N. Engl. J. Med. 352 (2005) 333-340
81. Varghese J.N., Laver W.G., and Colman P.M. Structure of the influenza virus glycoprotein antigen neuraminidase at 2.9 A resolution. Nature 303 (1983) 35-40
82. von Itzstein M., Wu W.Y., Kok G.B., Pegg M.S., Dyason J.C., Jin B., Van Phan T., Smythe M.L., White H.F., Oliver S.W., Colman P.M., Varghese J.N., Ryan D.M., Woods J.M., Bethell R.C., Hotham V.J., Cameron J.M., and Penn C.R. Rational design of potent sialidase-based inhibitors of influenza virus replication. Nature 363 (1993) 418-423
83. Woods J.M., Bethell R.C., Coates J.A., Healy N., Hiscox S.A., Pearson B.A., Ryan D.M., Ticehurst J., Tilling J., and Walcott S.M. 4-Guanidino-2,4-dideoxy-2,3-dehydro-N-acetylneuraminic acid is a highly effective inhibitor both of the sialidase (neuraminidase) and of growth of a wide range of influenza A and B viruses in vitro. Antimicrob. Agents Chemother. 37 (1993) 1473-1479
84. Wright P.F., and Webster R.G. Orthomyxoviruses. In: Knipe D.M., and Howley P.M. (Eds). "Fields Virology, 4th edition" (2001), Lippincott, Williams, and Wilkins, Philadelphia 1533-1579
85. Yoneyama M., Kikuchi M., Natsukawa T., Shinobu N., Imaizumi T., Miyagishi M., Taira K., Akira S., and Fujita T. The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat. Immunol. 5 (2004) 730-737
86. Yuan W., and Krug R.M. Influenza B virus NS1 protein inhibits conjugation of the interferon (IFN)-induced ubiquitin-like ISG15 protein. EMBO J. 20 (2001) 362-371
87. Zhirnov O.P., Konakova T.E., Wolff T., and Klenk H.D. NS1 protein of influenza A virus downregulates apoptosis. J. Virol. 76 (2002) 1617-1625
88. Zitzow L.A., Rowe T., Morken T., Shieh W.J., Zaki S., and Katz J.M. Pathogenesis of avian influenza A (H5N1) viruses in ferrets. J. Virol. 76 (2002) 4420-4429