Diversity of A(H5N1) clade 2.3.2.1c avian influenza viruses with evidence of reassortment in Cambodia, 2014-2016


Autoři: Annika Suttie aff001;  Songha Tok aff001;  Sokhoun Yann aff001;  Ponnarath Keo aff001;  Srey Viseth Horm aff001;  Merryn Roe aff003;  Matthew Kaye aff003;  San Sorn aff004;  Davun Holl aff004;  Sothyra Tum aff004;  Philippe Buchy aff001;  Ian Barr aff003;  Aeron Hurt aff003;  Andrew R. Greenhill aff002;  Erik A. Karlsson aff001;  Dhanasekaran Vijaykrishna aff006;  Yi-Mo Deng aff003;  Philippe Dussart aff001;  Paul F. Horwood aff001
Působiště autorů: Virology Unit, Institut Pasteur du Cambodge, Institut Pasteur International Network, Phnom Penh, Cambodia aff001;  School of Health and Life Sciences, Federation University, Churchill, Australia aff002;  WHO Collaborating Centre for Reference and Research on Influenza, Victorian Infectious Diseases Reference Laboratory, at the Peter Doherty Institute for Infection and Immunity, Melbourne, Victoria, Australia aff003;  National Animal Health and Production Research Institute, General Directorate of Animal Health and Production, Cambodian Ministry of Agriculture, Forestry and Fisheries, Phnom Penh, Cambodia aff004;  GlaxoSmithKline Vaccines R&D Intercontinental, Singapore, Singapore aff005;  Department of Microbiology, Biomedicine Discovery Institute, Monash University, Melbourne, Victoria, Australia aff006;  College of Public Health, Medical and Veterinary Sciences, James Cook University, Townsville, Queensland, Australia aff007
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: 10.1371/journal.pone.0226108

Souhrn

In Cambodia, highly pathogenic avian influenza A(H5N1) subtype viruses circulate endemically causing poultry outbreaks and zoonotic human cases. To investigate the genomic diversity and development of endemicity of the predominantly circulating clade 2.3.2.1c A(H5N1) viruses, we characterised 68 AIVs detected in poultry, the environment and from a single human A(H5N1) case from January 2014 to December 2016. Full genomes were generated for 42 A(H5N1) viruses. Phylogenetic analysis shows that five clade 2.3.2.1c genotypes, designated KH1 to KH5, were circulating in Cambodia during this period. The genotypes arose through multiple reassortment events with the neuraminidase (NA) and internal genes belonging to H5N1 clade 2.3.2.1a, clade 2.3.2.1b or A(H9N2) lineages. Phylogenies suggest that the Cambodian AIVs were derived from viruses circulating between Cambodian and Vietnamese poultry. Molecular analyses show that these viruses contained the hemagglutinin (HA) gene substitutions D94N, S133A, S155N, T156A, T188I and K189R known to increase binding to the human-type α2,6-linked sialic acid receptors. Two A(H5N1) viruses displayed the M2 gene S31N or A30T substitutions indicative of adamantane resistance, however, susceptibility testing towards neuraminidase inhibitors (oseltamivir, zanamivir, lananmivir and peramivir) of a subset of thirty clade 2.3.2.1c viruses showed susceptibility to all four drugs. This study shows that A(H5N1) viruses continue to reassort with other A(H5N1) and A(H9N2) viruses that are endemic in the region, highlighting the risk of introduction and emergence of novel A(H5N1) genotypes in Cambodia.

Klíčová slova:

Cambodia – Infectious disease surveillance – Microbial mutation – Phylogenetic analysis – Population genetics – Poultry – Viral genomics


Zdroje

1. Webster RG, Bean WJ, Gorman OT, Chambers TM, Kawaoka Y. Evolution and ecology of influenza A viruses. Microbiol Rev 1992;56:152–179. 1579108

2. Kuiken T. Is low pathogenic avian influenza virus virulent for wild waterbirds? Proc R Soc B Biol Sci 2013;280:20130990–20130990. https://doi.org/10.1098/rspb.2013.0990.

3. Sturm-Ramirez KM, Ellis T, Bousfield B, Bissett L, Dyrting K, Rehg JE, et al. Reemerging H5N1 Influenza Viruses in Hong Kong in 2002 Are Highly Pathogenic to Ducks. J Virol 2004;78:4892–901. https://doi.org/10.1128/JVI.78.9.4892-4901.2004 15078970

4. Swayne DE. Understanding the Complex Pathobiology of High Pathogenicity Avian Influenza Viruses in Birds. Avian Dis 2007;51:242–9. https://doi.org/10.1637/7763-110706-REGR.1 17494560

5. Xu X, Subbarao K, Cox NJ, Guo Y. Genetic characterization of the pathogenic influenza A/Goose/Guangdong/1/96 (H5N1) virus: similarity of its hemagglutinin gene to those of H5N1 viruses from the 1997 outbreaks in Hong Kong. Virology 1999;261:15–19. doi: 10.1006/viro.1999.9820 10484749

6. World Health Organization, Food and Agriculture Organization of the United Nations. H5N1 highly pathogenic avian influenza: Timeline of major events. 2014.

7. World Organization for Animal Health. Avian Influenza Portal: Update on avian influenza in animals (types H5 and H7) 2019. http://www.oie.int/en/animal-health-in-the-world/update-on-avian-influenza/2019/ (accessed August 28, 2019).

8. World Health Organisation. Cumulative number of confirmed human cases for avian influenza A(H5N1) reported to WHO, 2003–2019. 2019.

9. Claas EC, Osterhaus AD, Van Beek R, De Jong JC, Rimmelzwaan GF, Senne DA, et al. Human influenza A H5N1 virus related to a highly pathogenic avian influenza virus. The Lancet 1998;351:472–7.

10. Mounts AW, Kwong H, Izurieta HS, Ho Y, Au T, Lee M, et al. Case-control study of risk factors for avian influenza A (H5N1) disease, Hong Kong, 1997. J Infect Dis 1999;180:505–508. doi: 10.1086/314903 10395870

11. Herfst S, Schrauwen EJA, Linster M, Chutinimitkul S, de Wit E, Munster VJ, et al. Airborne Transmission of Influenza A/H5N1 Virus Between Ferrets. Science 2012;336:1534–41. https://doi.org/10.1126/science.1213362 22723413

12. Imai M, Watanabe T, Hatta M, Das SC, Ozawa M, Shinya K, et al. Experimental adaptation of an influenza H5 HA confers respiratory droplet transmission to a reassortant H5 HA/H1N1 virus in ferrets. Nature 2012. https://doi.org/10.1038/nature10831.

13. Ungchusak K, Auewarakul P, Dowell SF, Kitphati R, Auwanit W, Puthavathana P, et al. Probable person-to-person transmission of avian influenza A (H5N1). N Engl J Med 2005;352:333–340. doi: 10.1056/NEJMoa044021 15668219

14. Wang H, Feng Z, Shu Y, Yu H, Zhou L, Zu R, et al. Probable limited person-to-person transmission of highly pathogenic avian influenza A (H5N1) virus in China 2008:8.

15. Costa T, Chaves AJ, Valle R, Darji A, van Riel D, Kuiken T, et al. Distribution patterns of influenza virus receptors and viral attachment patterns in the respiratory and intestinal tracts of seven avian species. Vet Res 2012;43:28. https://doi.org/10.1186/1297-9716-43-28 22489675

16. Matrosovich M, Gambaryan A, Teneberg S, Piskarev V, Yamnikova S, Lvov D, et al. Avian influenza A viruses differ from human viruses by recognition of sialyloligosaccharides and gangliosides and by a higher conservation of the HA receptor-binding site. Virology 1997;233:224–234. doi: 10.1006/viro.1997.8580 9201232

17. National Institute of Statistics, Ministry of Planning. Cambodia Socio-Economic Survey 2017 2018. https://www.nis.gov.kh/index.php/en/14-cses/12-cambodia-socio-economic-survey-reports (accessed November 9, 2019).

18. World Health Organization. Cumulative number of confirmed human cases of avian influenza A(H5N1) reported to WHO 2019. https://www.who.int/influenza/human_animal_interface/H5N1_cumulative_table_archives/en/ (accessed September 28, 2019).

19. Horm SV, Mardy S, Rith S, Ly S, Heng S, Vong S, et al. Epidemiological and Virological Characteristics of Influenza Viruses Circulating in Cambodia from 2009 to 2011. PLoS ONE 2014;9:e110713. https://doi.org/10.1371/journal.pone.0110713 25340711

20. Horwood PF, Karlsson EA, Horm SV, Ly S, Heng S, Chin S, et al. Circulation and characterization of seasonal influenza viruses in Cambodia. Influenza Other Respir Viruses 2019;13:465–76. https://doi.org/10.1111/irv.12647 31251478

21. Smith GJD, Donis RO, World Health Organization/World Organisation for Animal Health/Food and Agriculture Organization (WHO/OIE/FAO) H5 Evolution Working Group. Nomenclature updates resulting from the evolution of avian influenza A(H5) virus clades 2.1.3.2a, 2.2.1, and 2.3.4 during 2013–2014. Influenza Other Respir Viruses 2015;9:271–6. https://doi.org/10.1111/irv.12324 25966311

22. Horm SV, Tarantola A, Rith S, Ly S, Gambaretti J, Duong V, et al. Intense circulation of A/H5N1 and other avian influenza viruses in Cambodian live-bird markets with serological evidence of sub-clinical human infections. Emerg Microbes Infect 2016;5:e70. https://doi.org/10.1038/emi.2016.69 27436362

23. Rith S, Davis CT, Duong V, Sar B, Horm SV, Chin S, et al. Identification of Molecular Markers Associated with Alteration of Receptor-Binding Specificity in a Novel Genotype of Highly Pathogenic Avian Influenza A(H5N1) Viruses Detected in Cambodia in 2013. J Virol 2014;88:13897–909. https://doi.org/10.1128/JVI.01887-14 25210193

24. Ly S, Horwood P, Chan M, Rith S, Sorn S, Oeung K, et al. Seroprevalence and Transmission of Human Influenza A(H5N1) Virus before and after Virus Reassortment, Cambodia, 2006–2014. Emerg Infect Dis 2017;23:300–3. https://doi.org/10.3201/eid2302.161232 28098551

25. Horwood PF, Horm SV, Suttie A, Thet S, Y P, Rith S, et al. Co-circulation of Influenza A H5, H7, and H9 Viruses and Co-infected Poultry in Live Bird Markets, Cambodia. Emerg Infect Dis 2018;24:352–5. https://doi.org/10.3201/eid2402.171360 29350140

26. QGIS Development Team. QGIS Geographic Information System. Open Source Geospatial Foundation 2018.

27. Zhou B, Donnelly ME, Scholes DT, St. George K, Hatta M, Kawaoka Y, et al. Single-Reaction Genomic Amplification Accelerates Sequencing and Vaccine Production for Classical and Swine Origin Human Influenza A Viruses. J Virol 2009;83:10309–13. https://doi.org/10.1128/JVI.01109-09 19605485

28. Shu Y, McCauley J. GISAID: Global initiative on sharing all influenza data–from vision to reality. Eurosurveillance 2017;22.

29. Katoh K, Standley DM. MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability. Mol Biol Evol 2013;30:772–80. https://doi.org/10.1093/molbev/mst010 23329690

30. Kosakovsky Pond SL, Posada D, Gravenor MB, Woelk CH, Frost SDW. Automated Phylogenetic Detection of Recombination Using a Genetic Algorithm. Mol Biol Evol 2006;23:1891–901. https://doi.org/10.1093/molbev/msl051 16818476

31. Weaver S, Shank SD, Spielman SJ, Li M, Muse SV, Kosakovsky Pond SL. Datamonkey 2.0: a modern web application for characterizing selective and other evolutionary processes. Mol Biol Evol 2018;35:773–777. doi: 10.1093/molbev/msx335 29301006

32. Nguyen L-T, Schmidt HA, von Haeseler A, Minh BQ. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 2015;32:268–274. https://doi.org/10.1093/molbev/msu300 25371430

33. Minh BQ, Nguyen MAT, von Haeseler A. Ultrafast Approximation for Phylogenetic Bootstrap. Mol Biol Evol 2013;30:1188–95. https://doi.org/10.1093/molbev/mst024 23418397

34. Tavaré S. Some probabilistic and statistical problems in the analysis of DNA sequences. Lect Math Life Sci 1986;17:57–86.

35. Andrew Rambaut. Molecular evolution, phylogenetics and epidemiology: FigTree 2016. http://tree.bio.ed.ac.uk/software/figtree/.

36. Drummond AJ, Suchard MA, Xie D, Rambaut A. Bayesian Phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 2012;29:1969–73. https://doi.org/10.1093/molbev/mss075 22367748

37. Miller MA, Pfeiffer W, Schwartz T. Creating the CIPRES Science Gateway for inference of large phylogenetic trees. 2010 Gatew. Comput. Environ. Workshop GCE, Ieee; 2010, p. 1–8.

38. Drummond AJ, Ho SY, Phillips MJ, Rambaut A. Relaxed phylogenetics and dating with confidence. PLoS Biol 2006;4:e88. doi: 10.1371/journal.pbio.0040088 16683862

39. Shapiro B, Rambaut A, Drummond AJ. Choosing Appropriate Substitution Models for the Phylogenetic Analysis of Protein-Coding Sequences. Mol Biol Evol 2006;23:7–9. https://doi.org/10.1093/molbev/msj021 16177232

40. Minin VN, Bloomquist EW, Suchard MA. Smooth Skyride through a Rough Skyline: Bayesian Coalescent-Based Inference of Population Dynamics. Mol Biol Evol 2008;25:1459–71. https://doi.org/10.1093/molbev/msn090 18408232

41. Creanga A, Thi Nguyen D, Gerloff N, Thi Do H, Balish A, Dang Nguyen H, et al. Emergence of multiple clade 2.3.2.1 influenza A (H5N1) virus subgroups in Vietnam and detection of novel reassortants. Virology 2013;444:12–20. https://doi.org/10.1016/j.virol.2013.06.005 23849789

42. Nguyen DT, Jang Y, Nguyen TD, Jones J, Shepard SS, Yang H, et al. Shifting Clade Distribution, Reassortment, and Emergence of New Subtypes of Highly Pathogenic Avian Influenza A(H5) Viruses Collected from Vietnamese Poultry from 2012 to 2015. J Virol 2017;91:e01708–16. https://doi.org/10.1128/JVI.01708-16.

43. Nguyen T, Rivailler P, Davis CT, Thi Hoa D, Balish A, Hoang Dang N, et al. Evolution of highly pathogenic avian influenza (H5N1) virus populations in Vietnam between 2007 and 2010. Virology 2012;432:405–16. https://doi.org/10.1016/j.virol.2012.06.021 22818871

44. Centers for Disease Control and Prevention. H5N1 Genetic Changes Inventory: A Tool for Influenza Surveillance and Preparedness. 2012.

45. Suttie A, Deng Y-M, Greenhill AR, Dussart P, Horwood PF, Karlsson EA. Inventory of molecular markers affecting biological characteristics of avian influenza A viruses. Virus Genes 2019. https://doi.org/10.1007/s11262-019-01700-z.

46. Gupta R, Jung E, Brunak S. Prediction of N-glycosylation sites in human proteins. 2004. Ref Type Unpubl Work 2016.

47. Burke DF, Smith DJ. A Recommended Numbering Scheme for Influenza A HA Subtypes. PLoS ONE 2014;9:e112302. https://doi.org/10.1371/journal.pone.0112302 25391151

48. Pond SLK, Muse SV. HyPhy: hypothesis testing using phylogenies. Stat. Methods Mol. Evol., Springer; 2005, p. 125–181.

49. Murrell B, Moola S, Mabona A, Weighill T, Sheward D, Kosakovsky Pond SL, et al. FUBAR: a fast, unconstrained bayesian approximation for inferring selection. Mol Biol Evol 2013;30:1196–1205. doi: 10.1093/molbev/mst030 23420840

50. Murrell B, Wertheim JO, Moola S, Weighill T, Scheffler K, Pond SLK. Detecting individual sites subject to episodic diversifying selection. PLoS Genet 2012;8:e1002764. doi: 10.1371/journal.pgen.1002764 22807683

51. Kosakovsky Pond SL, Frost SD. Not so different after all: a comparison of methods for detecting amino acid sites under selection. Mol Biol Evol 2005;22:1208–1222. doi: 10.1093/molbev/msi105 15703242

52. Hurt AC, Barr IG, Hartel G, Hampson AW. Susceptibility of human influenza viruses from Australasia and South East Asia to the neuraminidase inhibitors zanamivir and oseltamivir. Antiviral Res 2004;62:37–45. https://doi.org/10.1016/j.antiviral.2003.11.008 15026200

53. World Health Organisation and others. Meetings of the WHO working group on surveillance of influenza antiviral susceptibility—Geneva, November 2011 and June 2012. Wkly Epidemiol Rec 2012;87:369–374. 23061103

54. Horwood PF, Horm SV, Suttie A, Thet S, Phalla Y, Rith S, et al. Co-circulation of Influenza A H5, H7, and H9 Viruses and Co-infected Poultry in Live Bird Markets, Cambodia. Emerg Infect Dis 2018;24. https://doi.org/10.3201/eid2402.171360.

55. Peng W, Bouwman KM, McBride R, Grant OC, Woods RJ, Verheije MH, et al. Enhanced Human-Type Receptor Binding by Ferret-Transmissible H5N1 with a K193T Mutation. J Virol 2018;92. https://doi.org/10.1128/JVI.02016-17.

56. Chutinimitkul S, van Riel D, Munster VJ, van den Brand JMA, Rimmelzwaan GF, Kuiken T, et al. In Vitro Assessment of Attachment Pattern and Replication Efficiency of H5N1 Influenza A Viruses with Altered Receptor Specificity. J Virol 2010;84:6825–33. https://doi.org/10.1128/JVI.02737-0920392847

57. Li J, Li Y, Hu Y, Chang G, Sun W, Yang Y, et al. PB1-mediated virulence attenuation of H5N1 influenza virus in mice is associated with PB2. J Gen Virol 2011;92:1435–44. https://doi.org/10.1099/vir.0.030718-0 21367983

58. Taft AS, Ozawa M, Fitch A, Depasse JV, Halfmann PJ, Hill-Batorski L, et al. Identification of mammalian-adapting mutations in the polymerase complex of an avian H5N1 influenza virus. Nat Commun 2015;6. https://doi.org/10.1038/ncomms8491.

59. Feng X, Wang Z, Shi J, Deng G, Kong H, Tao S, et al. Glycine at Position 622 in PB1 Contributes to the Virulence of H5N1 Avian Influenza Virus in Mice. J Virol 2016;90:1872–9. https://doi.org/10.1128/JVI.02387-15 26656683

60. Schmolke M, Manicassamy B, Pena L, Sutton T, Hai R, Varga ZT, et al. Differential Contribution of PB1-F2 to the Virulence of Highly Pathogenic H5N1 Influenza A Virus in Mammalian and Avian Species. PLoS Pathog 2011;7:e1002186. https://doi.org/10.1371/journal.ppat.1002186 21852950

61. Kamal RP, Kumar A, Davis CT, Tzeng W-P, Nguyen T, Donis RO, et al. Emergence of Highly Pathogenic Avian Influenza A(H5N1) Virus PB1-F2 Variants and Their Virulence in BALB/c Mice. J Virol 2015;89:5835–46. https://doi.org/10.1128/JVI.03137-14 25787281

62. Hu J, Mo Y, Wang X, Gu M, Hu Z, Zhong L, et al. PA-X Decreases the Pathogenicity of Highly Pathogenic H5N1 Influenza A Virus in Avian Species by Inhibiting Virus Replication and Host Response. J Virol 2015;89:4126–42. https://doi.org/10.1128/JVI.02132-14 25631083

63. Gao H, Sun Y, Hu J, Qi L, Wang J, Xiong X, et al. The contribution of PA-X to the virulence of pandemic 2009 H1N1 and highly pathogenic H5N1 avian influenza viruses. Sci Rep 2015;5. https://doi.org/10.1038/srep08262.

64. Gao H, Sun Y, Liu X, Sun H, Hu J, Wang J, et al. Twenty amino acids at the C-terminus of PA-X are associated with increased influenza A virus replication and pathogenicity. J Gen Virol 2015;96:2036–49. https://doi.org/10.1099/vir.0.000143 25877935

65. OFFLU. Influenza A Cleavage Sites 2019.

66. Su Y, Yang H-Y, Zhang B-J, Jia H-L, Tien P. Analysis of a point mutation in H5N1 avian influenza virus hemagglutinin in relation to virus entry into live mammalian cells. Arch Virol 2008;153:2253–61. https://doi.org/10.1007/s00705-008-0255-y 19020946

67. Yang Z-Y, Wei C-J, Kong W-P, Wu L, Xu L, Smith DF, et al. Immunization by Avian H5 Influenza Hemagglutinin Mutants with Altered Receptor Binding Specificity. Science 2007;317:825–8. https://doi.org/10.1126/science.1135165 17690300

68. Wang W, Lu B, Zhou H, Suguitan AL, Cheng X, Subbarao K, 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 2010;84:6570–7. https://doi.org/10.1128/JVI.00221-10 20427525

69. Tada T, Suzuki K, Sakurai Y, Kubo M, Okada H, Itoh T, et al. NP body domain and PB2 contribute to increased virulence of H5N1 highly pathogenic avian influenza viruses in chickens. J Virol 2011;85:1834–46. https://doi.org/10.1128/JVI.01648-10 21123376

70. Wasilenko JL, Sarmento L, Pantin-Jackwood MJ. A single substitution in amino acid 184 of the NP protein alters the replication and pathogenicity of H5N1 avian influenza viruses in chickens. Arch Virol 2009;154:969–79. https://doi.org/10.1007/s00705-009-0399-4 19475480

71. Matsuoka Y, Swayne DE, Thomas C, Rameix-Welti M-A, Naffakh N, Warnes C, et al. Neuraminidase Stalk Length and Additional Glycosylation of the Hemagglutinin Influence the Virulence of Influenza H5N1 Viruses for Mice. J Virol 2009;83:4704–8. https://doi.org/10.1128/JVI.01987-08 19225004

72. Fan S, Deng G, Song J, Tian G, Suo Y, Jiang Y, et al. Two amino acid residues in the matrix protein M1 contribute to the virulence difference of H5N1 avian influenza viruses in mice. Virology 2009;384:28–32. https://doi.org/10.1016/j.virol.2008.11.044 19117585

73. Nao N, Kajihara M, Manzoor R, Maruyama J, Yoshida R, Muramatsu M, et al. A Single Amino Acid in the M1 Protein Responsible for the Different Pathogenic Potentials of H5N1 Highly Pathogenic Avian Influenza Virus Strains. PloS One 2015;10:e0137989. https://doi.org/10.1371/journal.pone.0137989 26368015

74. Cheung C-L, Rayner JM, Smith GJ, Wang P, Naipospos TSP, Zhang J, et al. Distribution of amantadine-resistant H5N1 avian influenza variants in Asia. J Infect Dis 2006;193:1626–1629. doi: 10.1086/504723 16703504

75. Bean WJ, Threlkeld SC, Webster RG. Biologic potential of amantadine-resistant influenza A virus in an avian model. J Infect Dis 1989;159:1050–6. doi: 10.1093/infdis/159.6.1050 2723453

76. Long J-X, Peng D-X, Liu Y-L, Wu Y-T, Liu X-F. Virulence of H5N1 avian influenza virus enhanced by a 15-nucleotide deletion in the viral nonstructural gene. Virus Genes 2008;36:471–8. https://doi.org/10.1007/s11262-007-0187-8 18317917

77. Jiao P, Tian G, Li Y, Deng G, Jiang Y, Liu C, et al. A Single-Amino-Acid Substitution in the NS1 Protein Changes the Pathogenicity of H5N1 Avian Influenza Viruses in Mice. J Virol 2008;82:1146–54. https://doi.org/10.1128/JVI.01698-07 18032512

78. Kuo R-L, Krug RM. Influenza A Virus Polymerase Is an Integral Component of the CPSF30-NS1A Protein Complex in Infected Cells. J Virol 2009;83:1611–6. https://doi.org/10.1128/JVI.01491-08 19052083

79. Heui Seo S, Hoffmann E, Webster RG. Lethal H5N1 influenza viruses escape host anti-viral cytokine responses. Nat Med 2002;8:950–4. https://doi.org/10.1038/nm757 12195436

80. Spesock A, Malur M, Hossain MJ, Chen L-M, Njaa BL, Davis CT, et al. The Virulence of 1997 H5N1 Influenza Viruses in the Mouse Model Is Increased by Correcting a Defect in Their NS1 Proteins. J Virol 2011;85:7048–58. https://doi.org/10.1128/JVI.00417-11 21593152

81. Obayashi E, Yoshida H, Kawai F, Shibayama N, Kawaguchi A, Nagata K, et al. The structural basis for an essential subunit interaction in influenza virus RNA polymerase. Nature 2008;454:1127–31. https://doi.org/10.1038/nature07225 18660801

82. Sugiyama K, Obayashi E, Kawaguchi A, Suzuki Y, Tame JRH, Nagata K, et al. Structural insight into the essential PB1-PB2 subunit contact of the influenza virus RNA polymerase. EMBO J 2009;28:1803–11. https://doi.org/10.1038/emboj.2009.138 19461581

83. Guilligay D, Tarendeau F, Resa-Infante P, Coloma R, Crepin T, Sehr P, et al. The structural basis for cap binding by influenza virus polymerase subunit PB2. Nat Struct Mol Biol 2008;15:500–6. https://doi.org/10.1038/nsmb.1421 18454157

84. Fan S, Hatta M, Kim JH, Halfmann P, Imai M, Macken CA, et al. Novel residues in avian influenza virus PB2 protein affect virulence in mammalian hosts. Nat Commun 2014;5. https://doi.org/10.1038/ncomms6021.

85. Liu Y, Qin K, Meng G, Zhang J, Zhou J, Zhao G, et al. Structural and functional characterization of K339T substitution identified in the PB2 subunit cap-binding pocket of influenza A virus. J Biol Chem 2013;288:11013–23. https://doi.org/10.1074/jbc.M112.392878 23436652

86. Yamaji R, Yamada S, Le MQ, Li C, Chen H, Qurnianingsih E, et al. Identification of PB2 mutations responsible for the efficient replication of H5N1 influenza viruses in human lung epithelial cells. J Virol 2015;89:3947–56. https://doi.org/10.1128/JVI.03328-14 25609813

87. Chen W, Zhong Y, Qin Y, Sun S, Li Z. The Evolutionary Pattern of Glycosylation Sites in Influenza Virus (H5N1) Hemagglutinin and Neuraminidase. PLoS ONE 2012;7:e49224. https://doi.org/10.1371/journal.pone.0049224 23133677

88. Suttie A, Karlsson EA, Deng Y-M, Horm SV, Yann S, Tok S, et al. Influenza A(H5N1) viruses with A(H9N2) single gene (matrix or PB1) reassortment isolated from Cambodian live bird markets. Virology 2018;523:22–6. https://doi.org/10.1016/j.virol.2018.07.028 30075357

89. Naughtin M, Dyason JC, Mardy S, Sorn S, von Itzstein M, Buchy P. Neuraminidase Inhibitor Sensitivity and Receptor-Binding Specificity of Cambodian Clade 1 Highly Pathogenic H5N1 Influenza Virus. Antimicrob Agents Chemother 2011;55:2004–10. https://doi.org/10.1128/AAC.01773-10 21343450

90. FAO. Investigation of duck production and hatcheries and duckling supply in Cambodia. AHBL—Promoting strategies for prevention and control of HPAI. Rome: 2009.

91. Horm SV, Sorn S, Allal L, Buchy P. Influenza A(H5N1) Virus Surveillance at Live Poultry Markets, Cambodia, 2011. Emerg Infect Dis 2013;19:305–8. https://doi.org/10.3201/eid1902.121201 23347451

92. World Health Organization (WHO/OIE/FAO) H5N1 Evolution Working Group. Revised and updated nomenclature for highly pathogenic avian influenza A (H5N1) viruses. Influenza Other Respir Viruses 2014;8:384–8. https://doi.org/10.1111/irv.12230 24483237

93. Naguib MM, Kinne J, Chen H, Chan K-H, Joseph S, Wong P-C, et al. Outbreaks of highly pathogenic avian influenza H5N1 clade 2.3. 2.1 c in hunting falcons and kept wild birds in Dubai implicate intercontinental virus spread. J Gen Virol 2015;96:3212–3222. doi: 10.1099/jgv.0.000274 26350163

94. Marchenko VY, Susloparov IM, Kolosova NP, Goncharova NI, Shipovalov AV, Ilyicheva TN, et al. Highly pathogenic influenza H5N1 virus of clade 2.3.2.1c in Western Siberia. Arch Virol 2016;161:1645–9. https://doi.org/10.1007/s00705-016-2800-4 26935914

95. Monamele CG, Y P, Karlsson EA, Vernet M-A, Wade A, Okomo M-CA, et al. Evidence of exposure and human seroconversion during an outbreak of avian influenza A(H5N1) among poultry in Cameroon. Emerg Microbes Infect 2019;8:186–96. https://doi.org/10.1080/22221751.2018.1564631 30866772

96. Bi Y, Chen J, Zhang Z, Li M, Cai T, Sharshov K, et al. Highly pathogenic avian influenza H5N1 Clade 2.3.2.1c virus in migratory birds, 2014–2015. Virol Sin 2016;31:300–5. https://doi.org/10.1007/s12250-016-3750-4 27405930

97. He S, Shi J, Qi X, Huang G, Chen H, Lu C. Lethal infection by a novel reassortant H5N1 avian influenza A virus in a zoo-housed tiger. Microbes Infect 2015;17:54–61. https://doi.org/10.1016/j.micinf.2014.10.004 25461468

98. Chen Q, Wang H, Zhao L, Ma L, Wang R, Lei Y, et al. First documented case of avian influenza (H5N1) virus infection in a lion. Emerg Microbes Infect 2016;5:e125–e125. https://doi.org/10.1038/emi.2016.127 27999425

99. Buchy P, Fourment M, Mardy S, Sorn S, Holl D, Ly S, et al. Molecular Epidemiology of Clade 1 Influenza A Viruses (H5N1), Southern Indochina Peninsula, 2004–2007. Emerg Infect Dis 2009;15:1641–4. https://doi.org/10.3201/eid1510.090115 19861062

100. Van Kerkhove MD, Vong S, Guitian J, Holl D, Mangtani P, San S, et al. Poultry movement networks in Cambodia: Implications for surveillance and control of highly pathogenic avian influenza (HPAI/H5N1). Vaccine 2009;27:6345–52. https://doi.org/10.1016/j.vaccine.2009.05.004 19840671

101. Chen H, Yuan H, Gao R, Zhang J, Wang D, Xiong Y, et al. Clinical and epidemiological characteristics of a fatal case of avian influenza A H10N8 virus infection: a descriptive study. The Lancet 2014;383:714–721.

102. Pu J, Wang S, Yin Y, Zhang G, Carter RA, Wang J, et al. Evolution of the H9N2 influenza genotype that facilitated the genesis of the novel H7N9 virus. Proc Natl Acad Sci 2015;112:548–53. https://doi.org/10.1073/pnas.1422456112 25548189

103. Hatta M. Molecular Basis for High Virulence of Hong Kong H5N1 Influenza A Viruses. Science 2001;293:1840–2. https://doi.org/10.1126/science.1062882 11546875

104. Li Z, Chen H, Jiao P, Deng G, Tian G, Li Y, et al. Molecular Basis of Replication of Duck H5N1 Influenza Viruses in a Mammalian Mouse Model. J Virol 2005;79:12058–64. https://doi.org/10.1128/JVI.79.18.12058-12064.2005 16140781

105. Skehel JJ, Stevens DJ, Daniels RS, Douglas AR, Knossow M, Wilson IA, et al. A carbohydrate side chain on hemagglutinins of Hong Kong influenza viruses inhibits recognition by a monoclonal antibody. Proc Natl Acad Sci 1984;81:1779–83. https://doi.org/10.1073/pnas.81.6.1779 6584912

106. Wang C-C, Chen J-R, Tseng Y-C, Hsu C-H, Hung Y-F, Chen S-W, et al. Glycans on influenza hemagglutinin affect receptor binding and immune response. Proc Natl Acad Sci 2009;106:18137–18142. doi: 10.1073/pnas.0909696106 19822741

107. Hervé P-L, Lorin V, Jouvion G, Da Costa B, Escriou N. Addition of N-glycosylation sites on the globular head of the H5 hemagglutinin induces the escape of highly pathogenic avian influenza A H5N1 viruses from vaccine-induced immunity. Virology 2015;486:134–45. https://doi.org/10.1016/j.virol.2015.08.033 26433051

108. Deshpande KL, Fried VA, Ando M, Webster RG. Glycosylation affects cleavage of an H5N2 influenza virus hemagglutinin and regulates virulence. Proc Natl Acad Sci 1987;84:36–40. https://doi.org/10.1073/pnas.84.1.36 3467357

109. Kawaoka Y, Webster RG. Interplay between Carbohydrate in the Stalk and the Length of the Connecting Peptide Determines the Cleavability of Influenza Virus Hemagglutinin n.d.:5.

110. Gao Y, Zhang Y, Shinya K, Deng G, Jiang Y, Li Z, 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 2009;5:e1000709. https://doi.org/10.1371/journal.ppat.100070920041223

111. Demicheli V, Jefferson T, Ferroni E, Rivetti A, Di Pietrantonj C. Vaccines for preventing influenza in healthy adults. Cochrane Database Syst Rev 2018.

112. Bright RA, Medina M, Xu X, Perez-Oronoz G, Wallis TR, Davis XM, et al. Incidence of adamantane resistance among influenza A (H3N2) viruses isolated worldwide from 1994 to 2005: a cause for concern. The Lancet 2005;366:1175–1181.


Článek vyšel v časopise

PLOS One


2019 Číslo 12