Avian influenza A viruses: From zoonosis to pandemic

Future Virology

Volumn 9, Issue 5, 2014, Pages 513-524

  Richard, Mathilde ^a   De Graaf, Miranda ^a   Herfst, Sander ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

airborne transmission; avian influenza A virus; HA stability; mammalian adaptation; pandemic; receptor specificity; zoonosis

Indexed keywords

HA PROTEIN; RNA POLYMERASE; UNCLASSIFIED DRUG; VIRUS ENZYME; VIRUS PROTEIN; VIRUS RNA;

AIRBORNE VIRUS; AVIAN INFLUENZA; AVIAN INFLUENZA VIRUS; BIRD; GENOTYPE; HUMAN; INFLUENZA VIRUS A H1N1; INFLUENZA VIRUS A H2N2; INFLUENZA VIRUS A H3N2; INFLUENZA VIRUS A H5N1; INFLUENZA VIRUS A H7N9; INFLUENZA VIRUS A H9N2; NONHUMAN; PANDEMIC; PHENOTYPE; PRIORITY JOURNAL; PROTEIN STABILITY; RECEPTOR BINDING; REVIEW; SEASONAL INFLUENZA; UPPER RESPIRATORY TRACT; VIRUS ATTACHMENT; VIRUS REPLICATION; VIRUS TRANSMISSION; ZOONOSIS;

EID: 84902472781     PISSN: 17460794     EISSN: 17460808     Source Type: Journal    
DOI: 10.2217/fvl.14.30     Document Type: Review

References (107)

1. Fouchier RA Munster V Wallensten A et al. Characterization of a novel influenza A virus hemagglutinin subtype (H16) obtained from black-headed gulls. J. Virol. 79(5) 2814-2822 (2005
2. Tong S Zhu X Li Y et al. New World bats harbor diverse influenza a viruses. PLoS Pathog. 9(10) e1003657 (2013
3. De Jong JC Claas EC Osterhaus AD Webster RG Lim WL. A pandemic warning? Nature 389(6651) 554 (1997
4. Taubenberger JK Morens DM. 1918 Influenza: the mother of all pandemics. Emerg. Infect. Dis. 12(1) 15-22 (2006
5. Scholtissek C Rohde W Von Hoyningen V Rott R. On the origin of the human influenza virus subtypes H2N2 and H3N2. Virology 87(1) 13-20 (1978
6. Neumann G Noda T Kawaoka Y. Emergence and pandemic potential of swine-origin H1N1 influenza virus. Nature 459(7249) 931-939 (2009
7. WHO. Cumulative number of confirmed human cases for avian influenza A (H5N1) reported to WHO 2003-2014. www.who.int/influenza/human-animal- interface/EN-GIP-20140124CumulativeNum berH5N1cases.pdfua=1
8. WHO. WHO risk assessment. Human infections with avian influenza A(H7N9) virus. www.who.int/influenza/human-animal- interface/influenza-h7n9/140225- H7N9RA- for-web-20140306FM.pdfua=1
9. Lam TT Wang J Shen Y et al. The genesis and source of the H7N9 influenza viruses causing human infections in China. Nature 502(7470) 241-244 (2013
10. Qi X Qian YH Bao CJ et al. Probable person to person transmission of novel avian influenza A (H7N9) virus in eastern China 2013: epidemiological investigation. BMJ 347 f4752 (2013
11. Guan Y Vijaykrishna D Bahl J Zhu H Wang J Smith GJ. The emergence of pandemic influenza viruses. Protein Cell 1(1) 9-13 (2010
12. Ma W Lager KM Vincent AL Janke BH Gramer MR Richt JA. The role of swine in the generation of novel influenza viruses. Zoonoses Public Health 56(6-7) 326-337 (2009
13. Herfst S Schrauwen EJ Linster M et al. Airborne transmission of influenza A/H5N1 virus between ferrets. Science 336(6088) 1534-1541 (2012
14. Alexander DJ. An overview of the epidemiology of avian influenza. Vaccine 25(30) 5637-5644 (2007
15. Arzey GG Kirkland PD Arzey KE et al. Influenza virus A (H10N7) in chickens and poultry abattoir workers Australia. Emerg. Infect. Dis. 18(5) 814-816 (2012
16. Russell CA Fonville JM Brown AE et al. The potential for respiratory droplet-transmissible A/H5N1 influenza virus to evolve in a mammalian host. Science 336(6088) 1541-1547 (2012
17. Shi W Shi Y Wu Y Liu D Gao GF. Origin and molecular characterization of the human-infecting H6N1 influenza virus in Taiwan. Protein Cell 4(11) 846-853 (2013
18. Ostrowsky B Huang A Terry W et al. Low pathogenic avian influenza A (H7N2) virus infection in immunocompromised adult New York USA 2003. Emerg. Infect. Dis. 18(7) 1128-1131 (2012
19. Avian influenza A/(H7N2) outbreak in the United Kingdom. Euro Surveill 12(5) E070531.2 (2007
20. Tweed SA Skowronski DM David ST et al. Human illness from avian influenza H7N3 British Columbia. Emerg. Infect. Dis. 10(12) 2196-2199 (2004
21. Nguyen-Van-Tam JS Nair P Acheson P et al. Outbreak of low pathogenicity H7N3 avian influenza in UK including associated case of human conjunctivitis. Eur. Surveill. 11(5) E060504.2 (2006
22. CDC. Notes from the field: highly pathogenic avian influenza A (H7N3) virus infection in two poultry workers-Jalisco Mexico July 2012. Morb. Mortal Wkly Rep. 61(36) 726-727 (2012
23. Kurtz J Manvell RJ Banks J. Avian influenza virus isolated from a woman with conjunctivitis. Lancet 348(9031) 901-902 (1996
24. Fouchier RA Schneeberger PM Rozendaal FW et al. Avian influenza A virus (H7N7) associated with human conjunctivitis and a fatal case of acute respiratory distress syndrome. Proc. Natl Acad. Sci. USA 101(5) 1356-1361 (2004
25. WHO. Influenza at the human-animal interface. WHO Press Geneva Switzerland (2013
26. Peiris M Yuen KY Leung CW et al. Human infection with influenza H9N2. Lancet 354(9182) 916-917 (1999
27. Butt KM Smith GJ Chen H et al. Human infection with an avian H9N2 influenza A virus in Hong Kong in 2003. J. Clin. Microbiol. 43(11) 5760-5767 (2005
28. Cheng VC Chan JF Wen X et al. Infection of immunocompromised patients by avian H9N2 influenza A virus. J. Infect. 62(5) 394-399 (2011
29. Promed: AVIAN INFLUENZA HUMAN (02): CHINA (HONG KONG) H9N2 ex (HUNAN) (2014). www.promedmail.org/direct. phpid=20140102.2148327
30. Promed: Avian influenza A (H1N7) humans avians-Egypt: correction (2004). www.promedmail.org/direct. phpid=20040524.1393
31. Promed: Human fatal case of avian influenza A(H10N8) in Jiangxi province (2014). www.promedmail.org/direct. phpid=20140214.2277024
32. Imai M Kawaoka Y. The role of receptor binding specificity in interspecies transmission of influenza viruses. Curr. Opin. Virol. 2(2) 160-167 (2012
33. Hirst GK. The agglutination of red cells by allantoic fluid of chick embryos infected with influenza virus. Science 94(2427) 22-23 (1941
34. Gottschalk A. Neuraminidase: the specific enzyme of influenza virus and Vibrio cholerae. Biochim. Biophys. Acta 23(3) 645-646 (1957
35. Rogers GN Paulson JC. Receptor determinants of human and animal influenza virus isolates: differences in receptor specificity of the H3 hemagglutinin based on species of origin. Virology 127(2) 361-373 (1983
36. Costa T Chaves AJ Valle R et al. Distribution patterns of influenza virus receptors and viral attachment patterns in the respiratory and intestinal tracts of seven avian species. Vet. Res. 43,28 (2012
37. Stevens J Blixt O Chen LM Donis RO Paulson JC Wilson IA. Recent avian H5N1 viruses exhibit increased propensity for acquiring human receptor specificity. J. Mol. Biol. 381(5) 1382-1394 (2008
38. Shinya K Ebina M Yamada S Ono M Kasai N Kawaoka Y. Avian flu: influenza virus receptors in the human airway. Nature 440(7083) 435-436 (2006
39. Van Riel D Munster VJ De Wit E et al. H5N1 virus attachment to lower respiratory tract. Science 312(5772) 399 (2006
40. Matrosovich MN Krauss S Webster RG. H9N2 influenza A viruses from poultry in Asia have human virus-like receptor specificity. Virology 281(2) 156-162 (2001
41. Belser JA Blixt O Chen LM et al. Contemporary North American influenza H7 viruses possess human receptor specificity: Implications for virus transmissibility. Proc. Natl Acad. Sci. USA 105(21) 7558-7563 (2008
42. Watanabe Y Ibrahim MS Ellakany HF et al. Acquisition of human-type receptor binding specificity by new H5N1 influenza virus sublineages during their emergence in birds in Egypt. PLoS Pathog. 7(5) e1002068 (2011
43. Xu R De Vries RP Zhu X et al. Preferential recognition of avian-like receptors in human influenza A H7N9 viruses. Science 342(6163) 1230-1235 (2013
44. Zhou J Wang D Gao R et al. Biological features of novel avian influenza A (H7N9) virus. Nature 499(7459) 500-503 (2013
45. Guo CT Takahashi N Yagi H et al. The quail and chicken intestine have sialylgalactose sugar chains responsible for the binding of influenza A viruses to human type receptors. Glycobiology 17(7) 713-724 (2007
46. Gambaryan A Tuzikov A Pazynina G Bovin N Balish A Klimov A. Evolution of the receptor binding phenotype of influenza A (H5) viruses. Virology 344(2) 432-438 (2006
47. Matrosovich M Tuzikov A Bovin N et al. Early alterations of the receptor-binding properties of H1 H2 and H3 avian influenza virus hemagglutinins after their introduction into mammals. J. Virol. 74(18) 8502-8512 (2000
48. Gambaryan A Yamnikova S Lvov D et al. Receptor specificity of influenza viruses from birds and mammals: new data on involvement of the inner fragments of the carbohydrate chain. Virology 334(2) 276-283 (2005
49. Stevens J Blixt O Glaser L et al. Glycan microarray analysis of the hemagglutinins from modern and pandemic influenza viruses reveals different receptor specificities. J. Mol. Biol. 355(5) 1143-1155 (2006
50. Chandrasekaran A Srinivasan A Raman R et al. Glycan topology determines human adaptation of avian H5N1 virus hemagglutinin. Nat. Biotechnol. 26(1) 107-113 (2008
51. Stevens J Blixt O Tumpey TM Taubenberger JK Paulson JC Wilson IA. Structure and receptor specificity of the hemagglutinin from an H5N1 influenza virus. Science 312(5772) 404-410 (2006
52. Maines TR Chen LM Van Hoeven N et al. Effect of receptor binding domain mutations on receptor binding and transmissibility of avian influenza H5N1 viruses. Virology 413(1) 139-147 (2011
53. Chutinimitkul S Van Riel D Munster VJ et al. In vitro assessment of attachment pattern and replication efficiency of H5N1 influenza A viruses with altered receptor specificity. J. Virol. 84(13) 6825-6833 (2010
54. Yamada S Suzuki Y Suzuki T et al. Haemagglutinin mutations responsible for the binding of H5N1 influenza A viruses to human-type receptors. Nature 444(7117) 378-382 (2006
55. Steel J Lowen AC Mubareka S Palese P. Transmission of influenza virus in a mammalian host is increased by PB2 amino acids 627K or 627E/701N. PLoS Pathog. 5(1) e1000252 (2009
56. Hatta M Hatta Y Kim JH et al. Growth of H5N1 influenza A viruses in the upper respiratory tracts of mice. PLoS Pathog. 3(10) 1374-1379 (2007
57. Mehle A Doudna JA. An inhibitory activity in human cells restricts the function of an avian-like influenza virus polymerase. Cell Host Microbe 4(2) 111-122 (2008
58. Gabriel G Klingel K Otte A et al. Differential use of importin-alpha isoforms governs cell tropism and host adaptation of influenza virus. Nat. Commun. 2 156 (2011
59. Jonges M Bataille A Enserink R et al. Comparative analysis of avian influenza virus diversity in poultry and humans during a highly pathogenic avian influenza A (H7N7) virus outbreak. J. Virol. 85(20) 10598-10604 (2011
60. De Wit E Munster VJ Van Riel D et al. Molecular determinants of adaptation of highly pathogenic avian influenza H7N7 viruses to efficient replication in the human host. J. Virol. 84(3) 1597-1606 (2010
61. Manz B Schwemmle M Brunotte L. Adaptation of avian influenza A virus polymerase in mammals to overcome the host species barrier. J. Virol. 87(13) 7200-7209 (2013
62. Tellier R. Aerosol transmission of influenza A virus: a review of new studies. J. R Soc. Interface 6(Suppl. 6) S783-S790 (2009
63. Brankston G Gitterman L Hirji Z Lemieux C Gardam M. Transmission of influenza A in human beings. Lancet Infect. Dis. 7(4) 257-265 (2007
64. Alford RH Kasel JA Gerone PJ Knight V. Human influenza resulting from aerosol inhalation. Proc. Soc. Exp. Biol. Med. 122(3) 800-804 (1966
65. Fabian P McDevitt JJ Dehaan WH et al. Influenza virus in human exhaled breath: an observational study. PLoS ONE 3(7) e2691 (2008
66. Lindsley WG Blachere FM Thewlis RE et al. Measurements of airborne influenza virus in aerosol particles from human coughs. PLoS ONE 5(11) e15100 (2010
67. Smith W Andrewes CH Laidlaw PP. A virus obtained from influenza patients. Lancet 222(5732) 66-68 (1933
68. Kirkeby S Martel CJ Aasted B. Infection with human H1N1 influenza virus affects the expression of sialic acids of metaplastic mucous cells in the ferret airways. Virus Res. 144(1-2) 225-232 (2009
69. Van Riel D Munster VJ De Wit E et al. Human and avian influenza viruses target different cells in the lower respiratory tract of humans and other mammals. Am. J. Pathol. 171(4) 1215-1223 (2007
70. Almond JW. A single gene determines the host range of influenza virus. Nature 270(5638) 617-618 (1977
71. Lowen AC Mubareka S Tumpey TM Garcia-Sastre A Palese P. The guinea pig as a transmission model for human influenza viruses. Proc. Natl Acad. Sci. USA 103(26) 9988-9992 (2006
72. Maines TR Chen LM Matsuoka Y et al. Lack of transmission of H5N1 avian-human reassortant influenza viruses in a ferret model. Proc. Natl Acad. Sci. USA 103(32) 12121-12126 (2006
73. Belser JA Maines TR Katz JM Tumpey TM. Considerations regarding appropriate sample size for conducting ferret transmission experiments. Future Microbiol. 8(8) 961-965 (2013
74. Van Riel D Den Bakker MA Leijten LM et al. Seasonal and pandemic human influenza viruses attach better to human upper respiratory tract epithelium than avian influenza viruses. Am. J. Pathol. 176(4) 1614-1618 (2010
75. Tumpey TM Maines TR Van Hoeven N et al. A two-amino acid change in the hemagglutinin of the 1918 influenza virus abolishes transmission. Science 315(5812) 655-659 (2007
76. Pappas C Viswanathan K Chandrasekaran A et al. Receptor specificity and transmission of H2N2 subtype viruses isolated from the pandemic of 1957. PLoS ONE 5(6) e11158 (2010
77. Roberts KL Shelton H Scull M Pickles R Barclay WS. Lack of transmission of a human influenza virus with avian receptor specificity between ferrets is not due to decreased virus shedding but rather a lower infectivity in vivo. J. Gen. Virol. 92(Pt 8) 1822-1831 (2011
78. Connor RJ Kawaoka Y Webster RG Paulson JC. Receptor specificity in human avian and equine H2 and H3 influenza virus isolates. Virology 205(1) 17-23 (1994
79. Rogers GN D'Souza BL. Receptor binding properties of human and animal H1 influenza virus isolates. Virology 173(1) 317-322 (1989
80. Glaser L Stevens J Zamarin D et al. A single amino acid substitution in 1918 influenza virus hemagglutinin changes receptor binding specificity. J. Virol. 79(17) 11533-11536 (2005
81. Kilander A Rykkvin R Dudman SG Hungnes O. Observed association between the HA1 mutation D222G in the 2009 pandemic influenza A(H1N1) virus and severe clinical outcome Norway 2009-2010. Euro Surveill 15(9) (2010
82. Chutinimitkul S Herfst S Steel J et al. Virulence-associated substitution D222G in the hemagglutinin of 2009 pandemic influenza A(H1N1) virus affects receptor binding. J. Virol. 84(22) 11802-11813 (2010
83. Imai M Watanabe T Hatta M et al. Experimental adaptation of an influenza H5 HA confers respiratory droplet transmission to a reassortant H5 HA/H1N1 virus in ferrets. Nature 486(7403) 420-428 (2012
84. Zhu H Wang D Kelvin DJ et al. Infectivity transmission and pathology of human H7N9 influenza in ferrets and pigs. Science 341(6142) 183-186 (2013
85. Belser JA Gustin KM Pearce MB et al. Pathogenesis and transmission of avian influenza A (H7N9) virus in ferrets and mice. Nature 501(7468) 556-559 (2013
86. Watanabe T Kiso M Fukuyama S et al. Characterization of H7N9 influenza A viruses isolated from humans. Nature 501(7468) 551-555 (2013
87. Richard M Schrauwen EJ De Graaf M et al. Limited airborne transmission of H7N9 influenza A virus between ferrets. Nature 501(7468) 560-563 (2013
88. Zhang Q Shi J Deng G et al. H7N9 influenza viruses are transmissible in ferrets by respiratory droplet. Science 341(6144) 410-414 (2013
89. Gao Y Zhang Y Shinya K et al. Identification of amino acids in HA and PB2 critical for the transmission of H5N1 avian influenza viruses in a mammalian host. PLoS Pathog. 5(12) e1000709 (2009
90. Wang W Lu B Zhou H et al. Glycosylation at 158N of the hemagglutinin protein and receptor binding specificity synergistically affect the antigenicity and immunogenicity of a live attenuated H5N1 A/Vietnam/1203/2004 vaccine virus in ferrets. J. Virol. 84(13) 6570-6577 (2010
91. Van Hoeven N Pappas C Belser JA et al. Human HA and polymerase subunit PB2 proteins confer transmission of an avian influenza virus through the air. Proc. Natl Acad. Sci. USA 106(9) 3366-3371 (2009
92. Galloway SE Reed ML Russell CJ Steinhauer DA. Influenza HA subtypes demonstrate divergent phenotypes for cleavage activation and pH of fusion: implications for host range and adaptation. PLoS Pathog. 9(2) e1003151 (2013
93. Shelton H Roberts KL Molesti E Temperton N Barclay WS. Mutations in haemagglutinin that affect receptor binding and pH stability increase replication of a PR8 influenza virus with H5 HA in the upper respiratory tract of ferrets and may contribute to transmissibility. J. Gen. Virol. 94(Pt 6) 1220-1229 (2013
94. Zaraket H Bridges OA Duan S et al. Increased acid stability of the hemagglutinin protein enhances H5N1 influenza virus growth in the upper respiratory tract but is insufficient for transmission in ferrets. J. Virol. 87(17) 9911-9922 (2013
95. Zaraket H Bridges OA Russell CJ. The pH of activation of the hemagglutinin protein regulates H5N1 influenza virus replication and pathogenesis in mice. J. Virol. 87(9) 4826-4834 (2013
96. Xiong X Coombs PJ Martin SR et al. Receptor binding by a ferret-transmissible H5 avian influenza virus. Nature 497(7449) 392-396 (2013
97. Zhang W Shi Y Lu X Shu Y Qi J Gao GF. An airborne transmissible avian influenza H5 hemagglutinin seen at the atomic level. Science 340(6139) 1463-1467 (2013
98. Richard M Schrauwen EJ De Graaf M et al. Limited airborne transmission of H7N9 influenza A virus between ferrets. Nature 501(7468) 560-563 (2013
99. Wagner R Matrosovich M Klenk HD. Functional balance between haemagglutinin and neuraminidase in influenza virus infections. Rev. Med. Virol. 12(3) 159-166 (2002
100. Sorrell EM Schrauwen EJ Linster M De Graaf M Herfst S Fouchier RA. Predicting ?airborne' influenza viruses: (trans-) mission impossible? Curr. Opin. Virol. 1(6) 635-642 (2011
101. Kobasa D Kodihalli S Luo M et al. Amino acid residues contributing to the substrate specificity of the influenza A virus neuraminidase. J. Virol. 73(8) 6743-6751 (1999
102. Matrosovich M Zhou N Kawaoka Y Webster R. The surface glycoproteins of H5 influenza viruses isolated from humans chickens and wild aquatic birds have distinguishable properties. J. Virol. 73(2) 1146-1155 (1999
103. Chen LM Blixt O Stevens J et al. In vitro evolution of H5N1 avian influenza virus toward human-type receptor specificity. Virology 422(1) 105-113 (2012
104. Zhang Y Zhang Q Kong H et al. H5N1 hybrid viruses bearing 2009/H1N1 virus genes transmit in guinea pigs by respiratory droplet. Science 340(6139) 1459-1463 (2013
105. Baum LG Paulson JC. The N2 neuraminidase of human influenza virus has acquired a substrate specificity complementary to the hemagglutinin receptor specificity. Virology 180(1) 10-15 (1991
106. Sorrell EM Wan H Araya Y Song H Perez DR. Minimal molecular constraints for respiratory droplet transmission of an avian-human H9N2 influenza A virus. Proc. Natl Acad. Sci. USA 106(18) 7565-7570 (2009
107. Kimble JB Sorrell E Shao H Martin PL Perez DR. Compatibility of H9N2 avian influenza surface genes and 2009 pandemic H1N1 internal genes for transmission in the ferret model. Proc. Natl Acad. Sci. USA 108(29) 12084-12088 (2011).