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Genetics, Receptor Binding Property, and Transmissibility in Mammals of Naturally Isolated H9N2 Avian Influenza Viruses


Avian influenza viruses continue to present challenges to human health. Recently the H7N9 and H10N8 viruses that are of low pathogenicity for poultry have caused human infections and deaths in China. H9N2 influenza virus have been isolated worldwide from wild and domestic avian species for several decades, and their low pathogenic nature to poultry made them a low priority for animal disease control, which has allowed them to continue to evolve and spread. Here, we investigated a series of H9N2 influenza viruses that were detected in live poultry markets in southern China. We found that these viruses are able to preferentially bind to the human-type receptor, and some of them can cause disease and transmit between ferrets by respiratory droplet. All the transmissible H9N2 viruses have a similar internal gene constellation, which was also present in the H7N9 and H10N8 viruses. Our study indicates that the widespread dissemination of H9N2 viruses poses a threat to human health not only because of the potential of these viruses to cause an influenza pandemic, but also because they can function as “vehicles” to deliver different subtypes of influenza viruses from avian species to humans.


Vyšlo v časopise: Genetics, Receptor Binding Property, and Transmissibility in Mammals of Naturally Isolated H9N2 Avian Influenza Viruses. PLoS Pathog 10(11): e32767. doi:10.1371/journal.ppat.1004508
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1004508

Souhrn

Avian influenza viruses continue to present challenges to human health. Recently the H7N9 and H10N8 viruses that are of low pathogenicity for poultry have caused human infections and deaths in China. H9N2 influenza virus have been isolated worldwide from wild and domestic avian species for several decades, and their low pathogenic nature to poultry made them a low priority for animal disease control, which has allowed them to continue to evolve and spread. Here, we investigated a series of H9N2 influenza viruses that were detected in live poultry markets in southern China. We found that these viruses are able to preferentially bind to the human-type receptor, and some of them can cause disease and transmit between ferrets by respiratory droplet. All the transmissible H9N2 viruses have a similar internal gene constellation, which was also present in the H7N9 and H10N8 viruses. Our study indicates that the widespread dissemination of H9N2 viruses poses a threat to human health not only because of the potential of these viruses to cause an influenza pandemic, but also because they can function as “vehicles” to deliver different subtypes of influenza viruses from avian species to humans.


Zdroje

1. WHO (2014) Cumulative number of confirmed human cases for avian influenza A (H5N1) reported to WHO, 2003–2014. Available: http://www.who.int/influenza/human_animal_interface/EN_GIP_20140124CumulativeNumberH5N1cases.pdf. Accessed 24 January 2014.

2. ZhangY, ZhangQ, KongH, JiangY, GaoY, et al. (2013) H5N1 hybrid viruses bearing 2009/H1N1 virus genes transmit in guinea pigs by respiratory droplet. Science 340: 1459–1463.

3. HerfstS, SchrauwenEJ, LinsterM, ChutinimitkulS, de WitE, et al. (2012) Airborne transmission of influenza A/H5N1 virus between ferrets. Science 336: 1534–1541.

4. ImaiM, WatanabeT, HattaM, DasSC, OzawaM, et al. (2012) Experimental adaptation of an influenza H5 HA confers respiratory droplet transmission to a reassortant H5 HA/H1N1 virus in ferrets. Nature 486: 420–428.

5. FouchierRA, SchneebergerPM, RozendaalFW, BroekmanJM, KeminkSA, et al. (2004) Avian influenza A virus (H7N7) associated with human conjunctivitis and a fatal case of acute respiratory distress syndrome. Proc Natl Acad Sci U S A 101: 1356–1361.

6. KoopmansM, WilbrinkB, ConynM, NatropG, van der NatH, et al. (2004) Transmission of H7N7 avian influenza A virus to human beings during a large outbreak in commercial poultry farms in the Netherlands. Lancet 363: 587–593.

7. WangG, DengG, ShiJ, LuoW, ZhangG, et al. (2014) H6 influenza viruses pose a potential threat to human health. J Virol 88: 3953–3964.

8. NamJH, KimEH, SongD, ChoiYK, KimJK, et al. (2011) Emergence of Mammalian Species-Infectious and -Pathogenic Avian Influenza H6N5 Virus with No Evidence of Adaptation. Journal of Virology 85: 13271–13277.

9. Gillim-RossL, SantosC, ChenZ, AspelundA, YangCF, et al. (2008) Avian influenza h6 viruses productively infect and cause illness in mice and ferrets. J Virol 82: 10854–10863.

10. YuanJ, ZhangL, KanX, JiangL, YangJ, et al. (2013) Origin and molecular characteristics of a novel 2013 avian influenza A (H6N1) virus causing human infection in Taiwan. Clin Infect Dis 57: 1367–1368.

11. WHO (2014) Confirmed human cases of avian influenza A(H7N9) reported to WHO. Available: http://www.who.int/influenza/human_animal_interface/influenza_h7n9/16_ReportWebH7N9Number_20140325.pdf?ua=1. Accessed 25 March 2014.

12. ChenH, YuanH, GaoR, ZhangJ, WangD, et al. (2014) Clinical and epidemiological characteristics of a fatal case of avian influenza A H10N8 virus infection: a descriptive study. Lancet 383: 714–721.

13. HommePJ, EasterdayBC, AndersonDP (1970) Avian influenza virus infections. II. Experimental epizootiology of influenza A-turkey-Wisconsin-1966 virus in turkeys. Avian Dis 14: 240–247.

14. KawaokaY, ChambersTM, SladenWL, WebsterRG (1988) Is the gene pool of influenza viruses in shorebirds and gulls different from that in wild ducks? Virology 163: 247–250.

15. PeirisJS, GuanY, MarkwellD, GhoseP, WebsterRG, et al. (2001) Cocirculation of avian H9N2 and contemporary "human" H3N2 influenza A viruses in pigs in southeastern China: potential for genetic reassortment? J Virol 75: 9679–9686.

16. XuC, FanW, WeiR, ZhaoH (2004) Isolation and identification of swine influenza recombinant A/Swine/Shandong/1/2003(H9N2) virus. Microbes Infect 6: 919–925.

17. YuH, HuaRH, WeiTC, ZhouYJ, TianZJ, et al. (2008) Isolation and genetic characterization of avian origin H9N2 influenza viruses from pigs in China. Vet Microbiol 131: 82–92.

18. LiC, YuK, TianG, YuD, LiuL, et al. (2005) Evolution of H9N2 influenza viruses from domestic poultry in Mainland China. Virology 340: 70–83.

19. Lin Z, Xu C, Liu B, Ji Y, Fu Y, et al.. (2014) Analysis of the phylogeny of Chinese H9N2 avian influenza viruses and their pathogenicity in mice. Arch Virol. 2575–86.

20. LuX, RenshawM, TumpeyTM, KellyGD, Hu-PrimmerJ, et al. (2001) Immunity to influenza A H9N2 viruses induced by infection and vaccination. J Virol 75: 4896–4901.

21. GovorkovaEA, LenevaIA, GoloubevaOG, BushK, WebsterRG (2001) Comparison of efficacies of RWJ-270201, zanamivir, and oseltamivir against H5N1, H9N2, and other avian influenza viruses. Antimicrob Agents Chemother 45: 2723–2732.

22. MatrosovichMN, KraussS, WebsterRG (2001) H9N2 influenza A viruses from poultry in Asia have human virus-like receptor specificity. Virology 281: 156–162.

23. SorrellEM, WanH, ArayaY, SongH, PerezDR (2009) Minimal molecular constraints for respiratory droplet transmission of an avian-human H9N2 influenza A virus. Proc Natl Acad Sci U S A 106: 7565–7570.

24. SunY, QinK, WangJ, PuJ, TangQ, et al. (2011) High genetic compatibility and increased pathogenicity of reassortants derived from avian H9N2 and pandemic H1N1/2009 influenza viruses. Proc Natl Acad Sci U S A 108: 4164–4169.

25. KimbleJB, SorrellE, ShaoH, MartinPL, PerezDR (2011) Compatibility of H9N2 avian influenza surface genes and 2009 pandemic H1N1 internal genes for transmission in the ferret model. Proc Natl Acad Sci U S A 108: 12084–12088.

26. WanH, SorrellEM, SongH, HossainMJ, Ramirez-NietoG, et al. (2008) Replication and transmission of H9N2 influenza viruses in ferrets: evaluation of pandemic potential. PLoS One 3: e2923.

27. ZhangP, TangY, LiuX, LiuW, ZhangX, et al. (2009) A novel genotype H9N2 influenza virus possessing human H5N1 internal genomes has been circulating in poultry in eastern China since 1998. J Virol 83: 8428–8438.

28. PeirisM, YuenKY, LeungCW, ChanKH, IpPL, et al. (1999) Human infection with influenza H9N2. Lancet 354: 916–917.

29. ButtKM, SmithGJ, ChenH, ZhangLJ, LeungYH, et al. (2005) Human infection with an avian H9N2 influenza A virus in Hong Kong in 2003. J Clin Microbiol 43: 5760–5767.

30. WHO (2014) Influenza at the human-animal interface. Available: http://www.who.int/influenza/human_animal_interface/Influenza_Summary_IRA_HA_interface_24January14.pdf. Accessed 24 January 2014.

31. WangM, FuCX, ZhengBJ (2009) Antibodies against H5 and H9 avian influenza among poultry workers in China. N Engl J Med 360: 2583–2584.

32. PawarSD, TandaleBV, RautCG, ParkhiSS, BardeTD, et al. (2012) Avian influenza H9N2 seroprevalence among poultry workers in Pune, India, 2010. PLoS One 7: e36374.

33. BlairPJ, PutnamSD, KruegerWS, ChumC, WierzbaTF, et al. (2013) Evidence for avian H9N2 influenza virus infections among rural villagers in Cambodia. J Infect Public Health 6: 69–79.

34. ComanA, MafteiDN, KruegerWS, HeilGL, FriaryJA, et al. (2013) Serological evidence for avian H9N2 influenza virus infections among Romanian agriculture workers. J Infect Public Health 6: 438–447.

35. GrayGC, FergusonDD, LowtherPE, HeilGL, FriaryJA (2011) A national study of US bird banders for evidence of avian influenza virus infections. J Clin Virol 51: 132–135.

36. OkoyeJ, EzeD, KruegerWS, HeilGL, FriaryJA, et al. (2013) Serologic evidence of avian influenza virus infections among Nigerian agricultural workers. J Med Virol 85: 670–676.

37. UyekiTM, NguyenDC, RoweT, LuX, Hu-PrimmerJ, et al. (2012) Seroprevalence of antibodies to avian influenza A (H5) and A (H9) viruses among market poultry workers, Hanoi, Vietnam, 2001. PLoS One 7: e43948.

38. WangQ, JuL, LiuP, ZhouJ, LvX, et al. (2014) Serological and Virological Surveillance of Avian Influenza A Virus H9N2 Subtype in Humans and Poultry in Shanghai, China, Between 2008 and 2010. Zoonoses Public Health

39. GaoR, CaoB, HuY, FengZ, WangD, et al. (2013) Human infection with a novel avian-origin influenza A (H7N9) virus. N Engl J Med 368: 1888–1897.

40. ZhangQ, ShiJ, DengG, GuoJ, ZengX, et al. (2013) H7N9 influenza viruses are transmissible in ferrets by respiratory droplet. Science 341: 410–414.

41. CDC (2012) H5N1 Genetic Changes Inventory: A Tool for Influenza Surveillance and Preparedness. Available: http://www.cdc.gov/flu/pdf/avianflu/h5n1-inventory.pdf. Accessed 26 June 2012.

42. Hulse-PostDJ, FranksJ, BoydK, SalomonR, HoffmannE, et al. (2007) Molecular changes in the polymerase genes (PA and PB1) associated with high pathogenicity of H5N1 influenza virus in mallard ducks. J Virol 81: 8515–8524.

43. LiJ, LiY, HuY, ChangG, SunW, et al. (2011) PB1-mediated virulence attenuation of H5N1 influenza virus in mice is associated with PB2. J Gen Virol 92: 1435–1444.

44. FanS, DengG, SongJ, TianG, SuoY, et al. (2009) Two amino acid residues in the matrix protein M1 contribute to the virulence difference of H5N1 avian influenza viruses in mice. Virology 384: 28–32.

45. JiaoP, TianG, LiY, DengG, JiangY, et al. (2008) A single-amino-acid substitution in the NS1 protein changes the pathogenicity of H5N1 avian influenza viruses in mice. J Virol 82: 1146–1154.

46. SmeenkCA, WrightKE, BurnsBF, ThakerAJ, BrownEG (1996) Mutations in the hemagglutinin and matrix genes of a virulent influenza virus variant, A/FM/1/47-MA, control different stages in pathogenesis. Virus Res 44: 79–95.

47. BeanWJ, ThrelkeldSC, WebsterRG (1989) Biologic potential of amantadine-resistant influenza A virus in an avian model. J Infect Dis 159: 1050–1056.

48. HattaM, GaoP, HalfmannP, KawaokaY (2001) Molecular basis for high virulence of Hong Kong H5N1 influenza A viruses. Science 293: 1840–1842.

49. LiZ, ChenH, JiaoP, DengG, TianG, et al. (2005) Molecular basis of replication of duck H5N1 influenza viruses in a mammalian mouse model. J Virol 79: 12058–12064.

50. GaoY, ZhangY, ShinyaK, DengG, JiangY, 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.

51. ChenY, LiangW, YangS, WuN, GaoH, et al. (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.

52. ZhangH, LiX, GuoJ, LiL, ChangC, et al. (2014) The PB2 E627K mutation contributes to the high polymerase activity and enhanced replication of H7N9 influenza virus. J Gen Virol 95: 779–786.

53. MokCK, LeeHH, LestraM, NichollsJM, ChanMC, et al. (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.

54. VinesA, WellsK, MatrosovichM, CastrucciMR, ItoT, et al. (1998) The role of influenza A virus hemagglutinin residues 226 and 228 in receptor specificity and host range restriction. J Virol 72: 7626–7631.

55. TumpeyTM, MainesTR, Van HoevenN, GlaserL, SolorzanoA, et al. (2007) A two-amino acid change in the hemagglutinin of the 1918 influenza virus abolishes transmission. Science 315: 655–659.

56. RogersGN, PaulsonJC (1983) Receptor determinants of human and animal influenza virus isolates: differences in receptor specificity of the H3 hemagglutinin based on species of origin. Virology 127: 361–373.

57. WatanabeT, KisoM, FukuyamaS, NakajimaN, ImaiM, et al. (2013) Characterization of H7N9 influenza A viruses isolated from humans. Nature 501: 551–555.

58. WatanabeY, IbrahimMS, EllakanyHF, KawashitaN, MizuikeR, et al. (2011) Acquisition of human-type receptor binding specificity by new H5N1 influenza virus sublineages during their emergence in birds in Egypt. PLoS Pathog 7: e1002068.

59. LinsterM, van BoheemenS, de GraafM, SchrauwenEJ, LexmondP, et al. (2014) Identification, characterization, and natural selection of mutations driving airborne transmission of A/H5N1 virus. Cell 157: 329–339.

60. SteelJ, LowenAC, MubarekaS, PaleseP (2009) Transmission of influenza virus in a mammalian host is increased by PB2 amino acids 627K or 627E/701N. PLoS Pathog 5: e1000252.

61. ChenH, DengG, LiZ, TianG, LiY, et al. (2004) The evolution of H5N1 influenza viruses in ducks in southern China. Proc Natl Acad Sci U S A 101: 10452–10457.

62. LiY, ShiJ, ZhongG, DengG, TianG, et al. (2010) Continued evolution of H5N1 influenza viruses in wild birds, domestic poultry, and humans in China from 2004 to 2009. J Virol 84: 8389–8397.

63. DengG, TanD, ShiJ, CuiP, JiangY, et al. (2013) Complex reassortment of multiple subtypes of avian influenza viruses in domestic ducks at the Dongting Lake Region of China. J Virol 87: 9452–9462.

64. ZhangY, ZhangQ, GaoY, HeX, KongH, et al. (2012) Key molecular factors in hemagglutinin and PB2 contribute to efficient transmission of the 2009 H1N1 pandemic influenza virus. J Virol 86: 9666–9674.

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Hygiena a epidemiológia Infekčné lekárstvo Laboratórium

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