Transmission of H7N9 influenza viruses with a polymorphism at PB2 residue 627 in chickens and ferrets

Journal of Virology

Volumn 89, Issue 19, 2015, Pages 9939-9951

  Luk, Geraldine S M ^a   Leung, Connie Y H ^b   Sia, Sin Fun ^b   Choy, Ka Tim ^b   Zhou, Jie ^b   Ho, Candy C K ^b   Cheung, Peter P H ^b   Lee, Elaine F ^a   Wai, Chris K L ^a   Li, Pamela C H ^a   Ip, Sin Ming ^a   Poon, Leo L M ^b   Lindsley, William G ^c   Peiris, Malik ^b   Yen, Hui Ling ^b  

^a DEPARTMENT OF HEALTH   (Hong Kong)

^b UNIVERSITY OF HONG KONG   (Hong Kong)

^c NATIONAL INSTITUTE FOR OCCUPATIONAL SAFETY AND HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

VIRUS RNA; PB2 PROTEIN, INFLUENZAVIRUS A; RNA DIRECTED RNA POLYMERASE; VIRUS PROTEIN;

AIRBORNE VIRUS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CHICKEN; CONTROLLED STUDY; FERRET; INFLUENZA A VIRUS (H7N9); NONHUMAN; PRIORITY JOURNAL; SINGLE NUCLEOTIDE POLYMORPHISM; VIRUS GENOME; VIRUS INFECTIVITY; VIRUS REPLICATION; VIRUS SHEDDING; VIRUS TRANSMISSION; ANIMAL; AVIAN INFLUENZA; BIRD DISEASE; GENETIC POLYMORPHISM; GENETICS; HOST PATHOGEN INTERACTION; HUMAN; INFLUENZA; ISOLATION AND PURIFICATION; MICROBIOLOGY; ORTHOMYXOVIRUS INFECTION; PATHOGENICITY; SPECIES DIFFERENCE; TRANSMISSION; VETERINARY; VIROLOGY; ZOONOSIS;

AIR MICROBIOLOGY; ANIMALS; CHICKENS; FERRETS; GENOME, VIRAL; HOST-PATHOGEN INTERACTIONS; HUMANS; INFLUENZA A VIRUS, H7N9 SUBTYPE; INFLUENZA IN BIRDS; INFLUENZA, HUMAN; ORTHOMYXOVIRIDAE INFECTIONS; POLYMORPHISM, GENETIC; POULTRY DISEASES; RNA REPLICASE; RNA, VIRAL; SPECIES SPECIFICITY; VIRAL PROTEINS; ZOONOSES;

EID: 84940978422     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01444-15     Document Type: Article

References (53)

1. CHP. Avian influenza report, vol 11, week 15.2015. CHP, Hong Kong. http://www.chp.gov.hk/files/pdf/2015_avian_influenza_report_vol11_wk15.pdf.
2. Yu H, Cowling BJ, Feng L, Lau EH, Liao Q, Tsang TK, Peng Z, Wu P, Liu F, Fang VJ, Zhang H, Li M, Zeng L, Xu Z, Li Z, Luo H, Li Q, Feng Z, Cao B, Yang W, Wu JT, Wang Y, Leung GM. 2013. Human infection with avian influenza A H7N9 virus: an assessment of clinical severity. Lancet 382:138-145. http://dx.doi.org/10.1016/S0140-6736(13)61207-6.
3. Gao R, Cao B, Hu Y, Feng Z, Wang D, Hu W, Chen J, Jie Z, Qiu H, Xu K, Xu X, Lu H, Zhu W, Gao Z, Xiang N, Shen Y, He Z, Gu Y, Zhang Z, Yang Y, Zhao X, Zhou L, Li X, Zou S, Zhang Y, Li X, Yang L, Guo J, Dong J, Li Q, Dong L, Zhu Y, Bai T, Wang S, Hao P, Yang W, Zhang Y, Han J, Yu H, Li D, Gao GF, Wu G, Wang Y, Yuan Z, Shu Y. 2013. Human infection with a novel avian-origin influenza A (H7N9) virus. N Engl J Med 368:1888-1897. http://dx.doi.org/10.1056/NEJMoa1304459.
4. Kageyama T, Fujisaki S, Takashita E, Xu H, Yamada S, Uchida Y, Neumann G, Saito T, Kawaoka Y, Tashiro M. 2013. Genetic analysis of novel avian A(H7N9) influenza viruses isolated from patients in China, February to April 2013. Euro Surveill 18(15):20453.
5. Lam TT, Wang J, Shen Y, Zhou B, Duan L, Cheung CL, Ma C, Lycett SJ, Leung CY, Chen X, Li L, Hong W, Chai Y, Zhou L, Liang H, Ou Z, Liu Y, Farooqui A, Kelvin DJ, Poon LL, Smith DK, Pybus OG, Leung GM, Shu Y, Webster RG, Webby RJ, Peiris JS, Rambaut A, Zhu H, Guan Y. 2013. The genesis and source of the H7N9 influenza viruses causing human infections in China. Nature 502:241-244. http://dx.doi.org/10.1038/nature12515.
6. Shi JZ, Deng GH, Liu PH, Zhou JP, Guan LZ, Li WH, Li XY, Guo J, Wang GJ, Fan J, Wang JL, Li YY, Jiang YP, Liu LL, Tian GB, Li CJ, Chen HL. 2013. Isolation and characterization of H7N9 viruses from live poultry markets-implication of the source of current H7N9 infection in humans. Chin Sci Bull 58:1857-1863. http://dx.doi.org/10.1007/s11434-013-5873-4.
7. Lu J, Wu J, Zeng X, Guan D, Zou L, Yi L, Liang L, Ni H, Kang M, Zhang X, Zhong H, He X, Monagin C, Lin J, Ke C. 2014. Continuing reassortment leads to the genetic diversity of influenza virus H7N9 in Guangdong, China. J Virol 88:8297-8306. http://dx.doi.org/10.1128/JVI.00630-14.
8. Lam TT, Zhou B, Wang J, Chai Y, Shen Y, Chen X, Ma C, Hong W, Chen Y, Zhang Y, Duan L, Chen P, Jiang J, Zhang Y, Li L, Poon LL, Webby RJ, Smith DK, Leung GM, Peiris JS, Holmes EC, Guan Y, Zhu H. 11 March 2015. Dissemination, divergence and establishment of H7N9 influenza viruses in China. Nature http://dx.doi.org/10.1038/nature14348.
9. Meng Z, Han R, Hu Y, Yuan Z, Jiang S, Zhang X, Xu J. 2014. Possible pandemic threat from new reassortment of influenza A(H7N9) virus in China. Euro Surveill 19(6):20699.
10. Pasricha G, Mukherjee S, Chakrabarti AK. 2014. Comprehensive sequence analysis of HA protein of H7 subtype avian influenza viruses: an emphasis on mutations in novel H7N9 viruses. Future Virol 9:251-273. http://dx.doi.org/10.2217/fvl.13.132.
11. Zhang Q, Shi J, Deng G, Guo J, Zeng X, He X, Kong H, Gu C, Li X, Liu J, Wang G, Chen Y, Liu L, Liang L, Li Y, Fan J, Wang J, Li W, Guan L, Li Q, Yang H, Chen P, Jiang L, Guan Y, Xin X, Jiang Y, Tian G, Wang X, Qiao C, Li C, Bu Z, Chen H. 2013. H7N9 influenza viruses are transmissible in ferrets by respiratory droplet. Science 341:410-414. http://dx.doi.org/10.1126/science.1240532.
12. Hatta M, Hatta Y, Kim JH, Watanabe S, Shinya K, Nguyen T, Lien PS, Le QM, Kawaoka Y. 2007. Growth of H5N1 influenza A viruses in the upper respiratory tracts of mice. PLoS Pathog 3:1374-1379.
13. Herfst S, Schrauwen EJ, Linster M, Chutinimitkul S, de Wit E, Munster VJ, Sorrell EM, Bestebroer TM, Burke DF, Smith DJ, Rimmelzwaan GF, Osterhaus AD, Fouchier RA. 2012. Airborne transmission of influenza A/H5N1 virus between ferrets. Science 336:1534-1541. http://dx.doi.org/10.1126/science.1213362.
14. Imai M, Herfst S, Sorrell EM, Schrauwen EJ, Linster M, De Graaf M, Fouchier RA, Kawaoka Y. 2013. Transmission of influenza A/H5N1 viruses in mammals. Virus Res 178:15-20. http://dx.doi.org/10.1016/j.virusres.2013.07.017.
15. Mok CK, Lee HH, Lestra M, Nicholls JM, Chan MC, Sia SF, Zhu H, Poon LL, Guan Y, Peiris JS. 2014. Amino acid substitutions in polymerase basic protein 2 gene contribute to the pathogenicity of the novel A/H7N9 influenza virus in mammalian hosts. J Virol 88:3568-3576. http://dx.doi.org/10.1128/JVI.02740-13.
16. 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. http://dx.doi.org/10.1371/journal.ppat.1000252.
17. Zhang H, Li X, Guo J, Li L, Chang C, Li Y, Bian C, Xu K, Chen H, Sun B. 2014. The PB2 E627K mutation contributes to the high polymerase activity and enhanced replication of H7N9 influenza virus. J Gen Virol 95:779-786. http://dx.doi.org/10.1099/vir.0.061721-0.
18. Van Hoeven N, Pappas C, Belser JA, Maines TR, Zeng H, García-Sastre A, Sasisekharan R, Katz JM, Tumpey TM. 2009. Human HA and polymerase subunit PB2 proteins confer transmission of an avian influenza virus through the air. Proc Natl Acad Sci U S A 106:3366-3371. http://dx.doi.org/10.1073/pnas.0813172106.
19. de Wit E, Munster VJ, van Riel D, Beyer WE, Rimmelzwaan GF, Kuiken T, Osterhaus AD, Fouchier RA. 2010. Molecular determinants of adaptation of highly pathogenic avian influenza H7N7 viruses to efficient replication in the human host. J Virol 84:1597-1606. http://dx.doi.org/10.1128/JVI.01783-09.
20. Jonges M, Welkers MR, Jeeninga RE, Meijer A, Schneeberger P, Fouchier RA, de Jong MD, Koopmans M. 2014. Emergence of the virulence-associated PB2 E627K substitution in a fatal human case of highly pathogenic avian influenza virus A(H7N7) infection as determined by Illumina Ultra-Deep sequencing. J Virol 88:1694-1702. http://dx.doi.org/10.1128/JVI.02044-13.
21. Golender N, Panshin A, Banet-Noach C, Nagar S, Pokamunski S, Pirak M, Tendler Y, Davidson I, Garcia M, Perk S. 2008. Genetic characterization of avian influenza viruses isolated in Israel during 2000-2006. Virus Genes 37:289-297. http://dx.doi.org/10.1007/s11262-008-0272-7.
22. Abdel-Moneim AS, AfifiMA, El-Kady MF. 2012. Isolation and mutation trend analysis of influenza A virus subtype H9N2 in Egypt. Virol J 9:173. http://dx.doi.org/10.1186/1743-422X-9-173.
23. Chin AW, Li OT, Mok CK, Ng MK, Peiris M, Poon LL. 2014. Influenza A viruses with different amino acid residues at PB2-627 display distinct replication properties in vitro and in vivo: revealing the sequence plasticity of PB2-627 position. Virology 468-470:545-555.
24. Cowling BJ, Jin L, Lau EH, Liao Q, Wu P, Jiang H, Tsang TK, Zheng J, Fang VJ, Chang Z, Ni MY, Zhang Q, Ip DK, Yu J, Li Y, Wang L, Tu W, Meng L, Wu JT, Luo H, Li Q, Shu Y, Li Z, Feng Z, Yang W, Wang Y, Leung GM, Yu H. 2013. Comparative epidemiology of human infections with avian influenza A H7N9 and H5N1 viruses in China: a populationbased study of laboratory-confirmed cases. Lancet 382:129-137. http://dx.doi.org/10.1016/S0140-6736(13)61171-X.
25. Liu B, Havers F, Chen E, Yuan Z, Yuan H, Ou J, Shang M, Kang K, Liao K, Liu F, Li D, Ding H, Zhou L, Zhu W, Ding F, Zhang P, Wang X, Yao J, Xiang N, Zhou S, Liu X, Song Y, Su H, Wang R, Cai J, Cao Y, Wang X, Bai T, Wang J, Feng Z, Zhang Y, Widdowson MA, Li Q. 2014. Risk factors for influenza A(H7N9) disease-China, 2013. Clin Infect Dis 59: 787-794. http://dx.doi.org/10.1093/cid/ciu423.
26. OIE. 2013. World Organisation for Animal Health (OIE) visit to the People's Republic of China to investigate influenza A (H7N9) infections in poultry 25 April-1 May 2013. OIE, Paris, France. http://www.oie.int/fileadmin/Home/eng/Media_Center/docs/pdf/RD_China_H7N9_June2013.pdf.
27. WHO. 2015. WHO risk assessment of human infections with avian influenza A(H7N9) virus. WHO, Geneva, Switzerland. http://www.who.int/influenza/human_animal_interface/influenza_h7n9/RiskAssessment_H7N9_23Feb20115.pdf?ua=1.
28. Tellier R. 2009. Aerosol transmission of influenza A virus: a review of new studies. J the Royal Society, Interface/the Royal Society 6 Suppl 6:S783-790. http://dx.doi.org/10.1098/rsif.2009.0302.focus.
29. He Y, Liu P, Tang S, Chen Y, Pei E, Zhao B, Ren H, Li J, Zhu Y, Zhao H, Pan Q, Gu B, Yuan Z, Wu F. 2014. Live poultry market closure and control of avian influenza A(H7N9), Shanghai, China Emerg Infect Dis 20:1565-1566.
30. Wu P, Jiang H, Wu JT, Chen E, He J, Zhou H, Wei L, Yang J, Yang B, Qin Y, Fang VJ, Li M, Tsang TK, Zheng J, Lau EH, Cao Y, Chai C, Zhong H, Li Z, Leung GM, Feng L, Gao GF, Cowling BJ, Yu H. 2014. Poultry market closures and human infection with influenza A(H7N9) virus, China, 2013-14. Emerg Infect Dis 20:1891-1894. http://dx.doi.org/10.3201/eid2011.140556.
31. Yu H, Wu JT, Cowling BJ, Liao Q, Fang VJ, Zhou S, Wu P, Zhou H, Lau EH, Guo D, Ni MY, Peng Z, Feng L, Jiang H, Luo H, Li Q, Feng Z, Wang Y, Yang W, Leung GM. 2014. Effect of closure of live poultry markets on poultry-to-person transmission of avian influenza A H7N9 virus: an ecological study. Lancet 383:541-548. http://dx.doi.org/10.1016/S0140-6736(13)61904-2.
32. FAO. 2014. Addressing avian influenza A(H7N9) qualitative risk assessment update. FAO, Rome, Italy. http://www.fao.org/3/a-i3813e.pdf.
33. Zhu H, Wang D, Kelvin DJ, Li L, Zheng Z, Yoon SW, Wong SS, Farooqui A, Wang J, Banner D, Chen R, Zheng R, Zhou J, Zhang Y, Hong W, Dong W, Cai Q, Roehrl MH, Huang SS, Kelvin AA, Yao T, Zhou B, Chen X, Leung GM, Poon LL, Webster RG, Webby RJ, Peiris JS, Guan Y, Shu Y. 2013. Infectivity, transmission, and pathology of human-isolated H7N9 influenza virus in ferrets and pigs. Science 341: 183-186. http://dx.doi.org/10.1126/science.1239844.
34. Jones JC, Sonnberg S, Webby RJ, Webster RG. 2015. Influenza A(H7N9) virus transmission between finches and poultry. Emerg Infect Dis 21:619-628. http://dx.doi.org/10.3201/eid2104.141703.
35. Yen HL, Zhou J, Choy KT, Sia SF, Teng O, Ng IH, Fang VJ, Hu Y, Wang W, Cowling BJ, Nicholls JM, Guan Y, Peiris JS. 2014. The R292K mutation that confers resistance to neuraminidase inhibitors leads to competitive fitness loss of A/Shanghai/1/2013 (H7N9) influenza virus in ferrets. J Infect Dis 210:1900-1908. http://dx.doi.org/10.1093/infdis/jiu353.
36. Slomka MJ, Pavlidis T, Coward VJ, Voermans J, Koch G, Hanna A, Banks J, Brown IH. 2009. Validated RealTime reverse transcriptase PCR methods for the diagnosis and pathotyping of Eurasian H7 avian influenza viruses. Influenza Other Respir Viruses 3:151-164. http://dx.doi.org/10.1111/j.1750-2659.2009.00083.x.
37. Wong CK, Zhu H, Li OT, Leung YH, Chan MC, Guan Y, Peiris JS, Poon LL. 2013. Molecular detection of human H7N9 influenza A virus causing outbreaks in China. Clin Chem 59:1062-1067. http://dx.doi.org/10.1373/clinchem.2013.208975.
38. Hoffmann E, Stech J, Guan Y, Webster RG, Perez DR. 2001. Universal primer set for the full-length amplification of all influenza A viruses. Arch Virol 146:2275-2289. http://dx.doi.org/10.1007/s007050170002.
39. Xu R, de Vries RP, Zhu X, Nycholat CM, McBride R, Yu W, Paulson JC, Wilson IA. 2013. Preferential recognition of avian-like receptors in human influenza A H7N9 viruses. Science 342:1230-1235. http://dx.doi.org/10.1126/science.1243761.
40. Blachere FM, Lindsley WG, Pearce TA, Anderson SE, Fisher M, Khakoo R, Meade BJ, Lander O, Davis S, Thewlis RE, Celik I, Chen BT, Beezhold DH. 2009. Measurement of airborne influenza virus in a hospital emergency department. Clin Infect Dis 48:438-440. http://dx.doi.org/10.1086/596478.
41. Ku KB, Park EH, Yum J, Kim HM, Kang YM, Kim JC, Kim JA, Kim HS, Seo SH. 2014. Transmissibility of novel H7N9 and H9N2 avian influenza viruses between chickens and ferrets. Virology 450-451:316-323.
42. Chen Y, Liang W, Yang S, Wu N, Gao H, Sheng J, Yao H, Wo J, Fang Q, Cui D, Li Y, Yao X, Zhang Y, Wu H, Zheng S, Diao H, Xia S, Zhang Y, Chan KH, Tsoi HW, Teng JL, Song W, Wang P, Lau SY, Zheng M, Chan JF, To KK, Chen H, Li L, Yuen KY. 2013. Human infections with the emerging avian influenza A H7N9 virus from wet market poultry: clinical analysis and characterisation of viral genome. Lancet 381:1916-1925. http://dx.doi.org/10.1016/S0140-6736(13)60903-4.
43. Rabadan R, Levine AJ, Robins H. 2006. Comparison of avian and human influenza A viruses reveals a mutational bias on the viral genomes. J Virol 80:11887-11891. http://dx.doi.org/10.1128/JVI.01414-06.
44. Zaraket H, Baranovich T, Kaplan BS, Carter R, Song MS, Paulson JC, Rehg JE, Bahl J, Crumpton JC, Seiler J, Edmonson M, Wu G, Karlsson E, Fabrizio T, Zhu H, Guan Y, Husain M, Schultz-Cherry S, Krauss S, McBride R, Webster RG, Govorkova EA, Zhang J, Russell CJ, Webby RJ. 2015. Mammalian adaptation of influenza A(H7N9) virus is limited by a narrow genetic bottleneck. Nat Commun 6:6553. http://dx.doi.org/10.1038/ncomms7553.
45. Spackman E, Gelb J, Jr, Preskenis LA, Ladman BS, Pope CR, Pantin-Jackwood MJ, McKinley ET. 2010. The pathogenesis of low pathogenicity H7 avian influenza viruses in chickens, ducks and turkeys. Virol J 7:331. http://dx.doi.org/10.1186/1743-422X-7-331.
46. KalthoffD, Bogs J, Grund C, Tauscher K, Teifke JP, Starick E, Harder T, Beer M. 2014. Avian influenza H7N9/13 and H7N7/13: a comparative virulence study in chickens, pigeons, and ferrets. J Virol 88:9153-9165. http://dx.doi.org/10.1128/JVI.01241-14.
47. Pantin-Jackwood MJ, Miller PJ, Spackman E, Swayne DE, Susta L, Costa-Hurtado M, Suarez DL. 2014. Role of poultry in the spread of novel H7N9 influenza virus in China. J Virol 88:5381-5390. http://dx.doi.org/10.1128/JVI.03689-13.
48. Watanabe T, Kiso M, Fukuyama S, Nakajima N, Imai M, Yamada S, Murakami S, Yamayoshi S, Iwatsuki-Horimoto K, Sakoda Y, Takashita E, McBride R, Noda T, Hatta M, Imai H, Zhao D, Kishida N, Shirakura M, de Vries RP, Shichinohe S, Okamatsu M, Tamura T, Tomita Y, Fujimoto N, Goto K, Katsura H, Kawakami E, Ishikawa I, Watanabe S, Ito M, Sakai-Tagawa Y, Sugita Y, Uraki R, Yamaji R, Eisfeld AJ, Zhong G, Fan S, Ping J, Maher EA, Hanson A, Uchida Y, Saito T, Ozawa M, Neumann G, Kida H, Odagiri T, Paulson JC, Hasegawa H, Tashiro M, Kawaoka Y. 2013. Characterization of H7N9 influenza A viruses isolated from humans. Nature 501:551-555. http://dx.doi.org/10.1038/nature12392.
49. Spackman E, Pantin-Jackwood M, Swayne DE, Suarez DL, Kapczynski DR. 2015. Impact of route of exposure and challenge dose on the pathogenesis of H7N9 low pathogenicity avian influenza virus in chickens. Virology 477:72-81. http://dx.doi.org/10.1016/j.virol.2015.01.013.
50. Guan J, Fu Q, Chan M, Spencer JL. 2013. Aerosol transmission of an avian influenza H9N2 virus with a tropism for the respiratory tract of chickens. Avian Dis 57:645-649. http://dx.doi.org/10.1637/10486-010913-Reg.1.
51. Shi H, Ashraf S, Gao S, Lu J, Liu X. 2010. Evaluation of transmission route and replication efficiency of H9N2 avian influenza virus. Avian Dis 54:22-27. http://dx.doi.org/10.1637/8937-052809-Reg.1.
52. Yu X, Jin T, Cui Y, Pu X, Li J, Xu J, Liu G, Jia H, Liu D, Song S, Yu Y, Xie L, Huang R, Ding H, Kou Y, Zhou Y, Wang Y, Xu X, Yin Y, Wang J, Guo C, Yang X, Hu L, Wu X, Wang H, Liu J, Zhao G, Zhou J, Pan J, Gao GF, Yang R, Wang J. 2014. Influenza H7N9 and H9N2 viruses: coexistence in poultry linked to human H7N9 infection and genome characteristics. J Virol 88:3423-3431. http://dx.doi.org/10.1128/JVI.02059-13.
53. Lindsley WG, Blachere FM, Thewlis RE, Vishnu A, Davis KA, Cao G, Palmer JE, Clark KE, Fisher MA, Khakoo R, Beezhold DH. 2010. Measurements of airborne influenza virus in aerosol particles from human coughs. PLoS One 5:e15100. http://dx.doi.org/10.1371/journal.pone.0015100.