The multibasic cleavage site of the hemagglutinin of highly pathogenic a/vietnam/1203/2004 (H5N1) avian influenza virus acts as a virulence factor in a host-specific manner in mammals

Journal of Virology

Volumn 86, Issue 5, 2012, Pages 2706-2714

  Suguitan, Orsolo L ^a,b   Matsuoka, Yumiko ^a   Lau, Yuk Fai ^a,c   Santos, Celia P ^a   Vogel, Leatrice ^a   Cheng, Lily I ^a,b   Orandle, Marlene ^a   Subbarao, Kanta ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b MEDIMMUNE   (United States)

^c DSO NATIONAL LABORATORIES   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

INFLUENZA VIRUS HEMAGGLUTININ; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; KERATINOCYTE DERIVED CHEMOKINE; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; MONOCYTE CHEMOTACTIC PROTEIN 1; RANTES; VIRULENCE FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHLOROCEBUS; CONTROLLED STUDY; CYTOKINE RESPONSE; FERRET; INFLUENZA A (H5N1); INFLUENZA VIRUS A H5N1; LYMPHOCYTOPENIA; MORTALITY; MOUSE; MULTIBASIC CLEAVAGE SITE; NONHUMAN; PNEUMONIA; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN STRUCTURE; RESPIRATORY SYSTEM; VIRAL CLEARANCE; VIRUS RECOMBINANT; VIRUS REPLICATION; VIRUS VIRULENCE;

AVIAN INFLUENZA VIRUS; CERCOPITHECUS AETHIOPS; MAMMALIA; MUS; MUSTELA; PRIMATES;

EID: 84857863488     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.05546-11     Document Type: Article

References (55)

1. Abdel-Ghafar AN, et al. 2008. Update on avian influenza A (H5N1) virus infection in humans. N. Engl. J. Med. 358:261-273.
2. Baskin CR, et al. 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.
3. Bhatia M, Moochhala S. 2004. Role of inflammatory mediators in the pathophysiology of acute respiratory distress syndrome. J. Pathol. 202: 145-156.
4. Boon AC, et al. 2009. Host genetic variation affects resistance to infection with a highly pathogenic H5N1 influenza A virus in mice. J. Virol. 83: 10417-10426.
5. Bosch FX, Garten W, Klenk HD, Rott R. 1981. Proteolytic cleavage of influenza virus hemagglutinins: primary structure of the connecting peptide between HA1 and HA2 determines proteolytic cleavability and pathogenicity of avian influenza viruses. Virology 113:725-735.
6. Bosch FX, Orlich M, Klenk HD, Rott R. 1979. The structure of the hemagglutinin, a determinant for the pathogenicity of influenza viruses. Virology 95:197-207.
7. Cameron CM, et al. 2008. Gene expression analysis of host innate immune responses during lethal H5N1 infection in ferrets. J. Virol. 82: 11308-11317.
8. Chen H, et al. 2007. Polygenic virulence factors involved in pathogenesis of 1997 Hong Kong H5N1 influenza viruses in mice. Virus Res. 128:159-163.
9. Chen H, et al. 2006. Establishment of multiple sublineages of H5N1 influenza virus in Asia: implications for pandemic control. Proc. Natl. Acad. Sci. U. S. A. 103:2845-2850.
10. Conenello GM, Zamarin D, Perrone LA, Tumpey T, Palese P. 2007. A single mutation in the PB1-F2 of H5N1 (HK/97) and 1918 influenza A viruses contributes to increased virulence. PLoS Pathog. 3:1414-1421.
11. de Jong MD, et al. 2006. Fatal outcome of human influenza A (H5N1) is associated with high viral load and hypercytokinemia. Nat. Med. 12:1203-1207.
12. Fornek JL, et al. 2009. A single-amino-acid substitution in a polymerase protein of an H5N1 influenza virus is associated with systemic infection and impaired T-cell activation in mice. J. Virol. 83:11102-11115.
13. Gao Y, et al. 2009. Identification of amino acids in HA and PB2 critical for the transmission of H5N1 avian influenza viruses in a mammalian host. PLoS Pathog. 5:e1000709.
14. Govorkova EA, et al. 2005. Lethality to ferrets of H5N1 influenza viruses isolated from humans and poultry in 2004. J. Virol. 79:2191-2198.
15. Hatta M, Gao P, Halfmann P, Kawaoka Y. 2001. Molecular basis for high virulence of Hong Kong H5N1 influenza A viruses. Science 293:1840-1842.
16. Horimoto T, Kawaoka Y. 1997. Biologic effects of introducing additional basic amino acid residues into the hemagglutinin cleavage site of a virulent avian influenza virus. Virus Res. 50:35-40.
17. Horimoto T, Kawaoka Y. 1994. Reverse genetics provides direct evidence for a correlation of hemagglutinin cleavability and virulence of an avian influenza A virus. J. Virol. 68:3120-3128.
18. Horimoto T, Nakayama K, Smeekens SP, Kawaoka Y. 1994. Proproteinprocessing endoproteases PC6 and furin both activate hemagglutinin of virulent avian influenza viruses. J. Virol. 68:6074-6078.
19. Jackson D, Hossain MJ, Hickman D, Perez DR, Lamb RA. 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.
20. Kandun IN, et al. 2006. Three Indonesian clusters of H5N1 virus infection in 2005. N. Engl. J. Med. 355:2186-2194.
21. Karlas A, et al. 2010. Genome-wide RNAi screen identifies human host factors crucial for influenza virus replication. Nature 463:818-822.
22. Kawaoka Y. 1991. Structural features influencing hemagglutinin cleavability in a human influenza A virus. J. Virol. 65:1195-1201.
23. Kawaoka Y, Webster RG. 1989. Interplay between carbohydrate in the stalk and the length of the connecting peptide determines the cleavability of influenza virus hemagglutinin. J. Virol. 63:3296-3300.
24. Kawaoka Y, Webster RG. 1988. Sequence requirements for cleavage activation of influenza virus hemagglutinin expressed in mammalian cells. Proc. Natl. Acad. Sci. U. S. A. 85:324-328.
25. Klenk HD, Rott R, Orlich M, Blodorn J. 1975. Activation of influenza A viruses by trypsin treatment. Virology 68:426-439.
26. Konig R, et al. 2010. Human host factors required for influenza virus replication. Nature 463:813-817.
27. Maeda T, Ohnishi S. 1980. Activation of influenza virus by acidic media causes hemolysis and fusion of erythrocytes. FEBS Lett. 122:283-287.
28. Maines TR, et al. 2005. Avian influenza (H5N1) viruses isolated from humans in Asia in 2004 exhibit increased virulence in mammals. J. Virol. 79:11788-11800.
29. Maines TR, et al. 2008. Pathogenesis of emerging avian influenza viruses in mammals and the host innate immune response. Immunol. Rev. 225: 68-84.
30. Nicholls JM, et al. 2007. Tropism of avian influenza A (H5N1) in the upper and lower respiratory tract. Nat. Med. 13:147-149.
31. Perrone LA, Plowden JK, Garcia-Sastre A, Katz JM, Tumpey TM. 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.
32. Rott R, Klenk HD, Nagai Y, Tashiro M. 1995. Influenza viruses, cell enzymes, and pathogenicity. Am. J. Respir. Crit. Care Med. 152:S16-S19.
33. Salomon R, et al. 2006. The polymerase complex genes contribute to the high virulence of the human H5N1 influenza virus isolate A/Vietnam/ 1203/04. J. Exp. Med. 203:689-697.
34. Shapira SD, et al. 2009. A physical and regulatory map of host-influenza interactions reveals pathways in H1N1 infection. Cell 139:1255-1267.
35. Song MS, et al. 2009. The polymerase acidic protein gene of influenza a virus contributes to pathogenicity in a mouse model. J. Virol. 83:12325-12335.
36. Srivastava B, et al. 2009. Host genetic background strongly influences the response to influenza A virus infections. PLoS One 4:e4857.
37. Stech O, et al. 2009. Acquisition of a polybasic hemagglutinin cleavage site by a low-pathogenic avian influenza virus is not sufficient for immediate transformation into a highly pathogenic strain. J. Virol. 83:5864-5868.
38. Steel J, Lowen AC, Mubareka S, Palese P. 2009. Transmission of influenza virus in a mammalian host is increased by PB2 amino acids 627K or 627E/701N. PLoS Pathog. 5:e1000252.
39. Steiner DF, Smeekens SP, Ohagi S, Chan SJ. 1992. The new enzymology of precursor processing endoproteases. J. Biol. Chem. 267:23435-23438.
40. Steinhauer DA. 1999. Role of hemagglutinin cleavage for the pathogenicity of influenza virus. Virology 258:1-20.
41. Stieneke-Grober A, et al. 1992. Influenza virus hemagglutinin with multibasic cleavage site is activated by furin, a subtilisin-like endoprotease. EMBO J. 11:2407-2414.
42. Subbarao K, et al. 1998. Characterization of an avian influenza A (H5N1) virus isolated from a child with a fatal respiratory illness. Science 279:393-396.
43. Suguitan AL, Jr, et al. 2009. The influence of the multi-basic cleavage site of the H5 hemagglutinin on the attenuation, immunogenicity and efficacy of a live attenuated influenza A H5N1 cold-adapted vaccine virus. Virology 395:280-288.
44. Suguitan AL, Jr, et al. 2006. Live, attenuated influenza A H5N1 candidate vaccines provide broad cross-protection in mice and ferrets. PLoS Med. 3:e360.
45. Suzuki Y, et al. 2000. Sialic acid species as a determinant of the host range of influenza A viruses. J. Virol. 74:11825-11831.
46. Svitek N, von Messling V. 2007. Early cytokine mRNA expression profiles predict morbillivirus disease outcome in ferrets. Virology 362:404-410.
47. Szretter KJ, et al. 2007. Role of host cytokine responses in the pathogenesis of avian H5N1 influenza viruses in mice. J. Virol. 81:2736-2744.
48. Tumpey TM, et al. 2005. Characterization of the reconstructed 1918 Spanish influenza pandemic virus. Science 310:77-80.
49. Tumpey TM, Lu X, Morken T, Zaki SR, Katz JM. 2000. Depletion of lymphocytes and diminished cytokine production in mice infected with a highly virulent influenza A (H5N1) virus isolated from humans. J. Virol. 74:6105-6116.
50. Ungchusak K, et al. 2005. Probable person-to-person transmission of avian influenza A (H5N1). N. Engl. J. Med. 352:333-340.
51. van Riel D, et al. 2007. Human and avian influenza viruses target different cells in the lower respiratory tract of humans and other mammals. Am. J. Pathol. 171:1215-1223.
52. Webster RG, Rott R. 1987. Influenza virus A pathogenicity: the pivotal role of hemagglutinin. Cell 50:665-666.
53. White J, Matlin K, Helenius A. 1981. Cell fusion by Semliki Forest, influenza, and vesicular stomatitis viruses. J. Cell Biol. 89:674-679.
54. World Health Organization. 20 November 2011, access date. Cumulative number of confirmed human cases of avian influenza A/(H5N1) reported to WHO. World Health Organization, Geneva, Switzerland. http://www.who.int/influenza/human_animal_interface/H5N1_cumulative_table_archives/en/.
55. Zitzow LA, et al. 2002. Pathogenesis of avian influenza A (H5N1) viruses in ferrets. J. Virol. 76:4420-4429.