Acquisition of Human-Type Receptor Binding Specificity by New H5N1 Influenza Virus Sublineages during Their Emergence in Birds in Egypt

English version České info

Highly pathogenic avian influenza A virus subtype H5N1 is currently widespread in Asia, Europe, and Africa, with 60% mortality in humans. In particular, since 2009 Egypt has unexpectedly had the highest number of human cases of H5N1 virus infection, with more than 50% of the cases worldwide, but the basis for this high incidence has not been elucidated. A change in receptor binding affinity of the viral hemagglutinin (HA) from α2,3- to α2,6-linked sialic acid (SA) is thought to be necessary for H5N1 virus to become pandemic. In this study, we conducted a phylogenetic analysis of H5N1 viruses isolated between 2006 and 2009 in Egypt. The phylogenetic results showed that recent human isolates clustered disproportionally into several new H5 sublineages suggesting that their HAs have changed their receptor specificity. Using reverse genetics, we found that these H5 sublineages have acquired an enhanced binding affinity for α2,6 SA in combination with residual affinity for α2,3 SA, and identified the amino acid mutations that produced this new receptor specificity. Recombinant H5N1 viruses with a single mutation at HA residue 192 or a double mutation at HA residues 129 and 151 had increased attachment to and infectivity in the human lower respiratory tract but not in the larynx. These findings correlated with enhanced virulence of the mutant viruses in mice. Interestingly, these H5 viruses, with increased affinity to α2,6 SA, emerged during viral diversification in bird populations and subsequently spread to humans. Our findings suggested that emergence of new H5 sublineages with α2,6 SA specificity caused a subsequent increase in human H5N1 influenza virus infections in Egypt, and provided data for understanding the virus's pandemic potential.

Vyšlo v časopise: Acquisition of Human-Type Receptor Binding Specificity by New H5N1 Influenza Virus Sublineages during Their Emergence in Birds in Egypt. PLoS Pathog 7(5): e32767. doi:10.1371/journal.ppat.1002068
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1002068

Souhrn

Zdroje

1. World Health Organization H5N1 avian influenza: timeline of major exents reported to WHO. Available: http://www.who.int/csr/disease/avian_influenza/2010_10_20_h5n1_avian_influenza_timeline_updates.pdf. Accessed 4 November 2010

2. World Health Organization/World Organisation for Animal Health/Food and Agriculture Organization H5N1 Evolution Working Group 2008 Toward a unified nomenclature system for highly pathogenic avian influenza virus (H5N1). Emerg Infect Dis 14 e1

3. ChenHLiYLiZShiJShinyaK 2006 Properties and dissemination of H5N1 viruses isolated during an influenza outbreak in migratory waterfowl in western China. J Virol 80 5976 5983

4. ChenHSmithGJZhangSYQinKWangJ 2005 Avian flu: H5N1 virus outbreak in migratory waterfowl. Nature 436 191 192

5. SalzbergSLKingsfordCCattoliGSpiroDJJaniesDA 2007 Genome analysis linking recent European and African influenza (H5N1) viruses. Emerg Infect Dis 13 713 718

6. WangGZhanDLiLLeiFLiuB 2008 H5N1 avian influenza re-emergence of Lake Qinghai: phylogenetic and antigenic analyses of the newly isolated viruses and roles of migratory birds in virus circulation. J Gen Virol 89 697 702

7. CattoliGMonneIFusaroAJoannisTMLombinLH 2009 Highly pathogenic avian influenza virus subtype H5N1 in Africa: a comprehensive phylogenetic analysis and molecular characterization of isolates. PLoS One 4 e4842

8. FusaroANelsonMIJoannisTBertolottiLMonneI 2010 Evolutionary dynamics of multiple sublineages of H5N1 influenza viruses in Nigeria from 2006 to 2008. J Virol 84 3239 3247

9. DawoodFSJainSFinelliLShawMWLindstromS 2009 Emergence of a novel swine-origin influenza A (H1N1) virus in humans. N Engl J Med 360 2605 2615

10. World Health Organization Cumulative number of confirmed human cases of avian influenza A/(H5N1) reported to WHO. Available: http://www.who.int/csr/disease/avian_influenza/country/en/index.html. Accessed 4 November 2010

11. World Organisation for Animal Health Update for highly pathogenic avian influenza in animals (Type H5 and H7). Available: http://www.oie.int/downld/AVIAN%20INFLUENZA/A_AI-Asia.htm. Accessed 4 November 2010

12. ConnorRJKawaokaYWebsterRGPaulsonJC 1994 Receptor specificity in human, avian, and equine H2 and H3 influenza virus isolates. Virology 205 17 23

13. MatrosovichMNGambaryanASTenebergSPiskarevVEYamnikovaSS 1997 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 233 224 234

14. RogersGNPaulsonJC 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

15. AngataTVarkiA 2002 Chemical diversity in the sialic acids and related alpha-keto acids: an evolutionary perspective. Chem Rev 102 439 469

16. GagneuxPCheriyanMHurtado-ZiolaNvan der LindenECAndersonD 2003 Human-specific regulation of alpha 2–6-linked sialic acids. J Biol Chem 278 48245 48250

17. GuoCTTakahashiNYagiHKatoKTakahashiT 2007 The quail and chicken intestine have sialyl-galactose sugar chains responsible for the binding of influenza A viruses to human type receptors. Glycobiology 17 713 724

18. CouceiroJNPaulsonJCBaumLG 1993 Influenza virus strains selectively recognize sialyloligosaccharides on human respiratory epithelium; the role of the host cell in selection of hemagglutinin receptor specificity. Virus Res 29 155 165

19. ItoTCouceiroJNKelmSBaumLGKraussS 1998 Molecular basis for the generation in pigs of influenza A viruses with pandemic potential. J Virol 72 7367 7373

20. MatrosovichMTuzikovABovinNGambaryanAKlimovA 2000 Early alterations of the receptor-binding properties of H1, H2, and H3 avian influenza virus hemagglutinins after their introduction into mammals. J Virol 74 8502 8512

21. TumpeyTMMainesTRVan HoevenNGlaserLSolorzanoA 2007 A two-amino acid change in the hemagglutinin of the 1918 influenza virus abolishes transmission. Science 315 655 659

22. PeyreMSamahaHMakonnenYJSaadAAbd-ElnabiA 2009 Avian influenza vaccination in Egypt: Limitations of the current strategy. J Mol Genet Med 3 198 204

23. AuewarakulPSuptawiwatOKongchanagulASangmaCSuzukiY 2007 An avian influenza H5N1 virus that binds to a human-type receptor. J Virol 81 9950 9955

24. YamadaSSuzukiYSuzukiTLeMQNidomCA 2006 Haemagglutinin mutations responsible for the binding of H5N1 influenza A viruses to human-type receptors. Nature 444 378 382

25. Abdel-MoneimASShanySAFereidouniSREidBTel-KadyMF 2009 Sequence diversity of the haemagglutinin open reading frame of recent highly pathogenic avian influenza H5N1 isolates from Egypt. Arch Virol 154 1559 1562

26. van RielDMunsterVJde WitERimmelzwaanGFFouchierRA 2006 H5N1 Virus Attachment to Lower Respiratory Tract. Science 312 399

27. van RielDMunsterVJde WitERimmelzwaanGFFouchierRA 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

28. ChandrasekaranASrinivasanARamanRViswanathanKRaguramS 2008 Glycan topology determines human adaptation of avian H5N1 virus hemagglutinin. Nat Biotechnol 26 107 113

29. SrinivasanAViswanathanKRamanRChandrasekaranARaguramS 2008 Quantitative biochemical rationale for differences in transmissibility of 1918 pandemic influenza A viruses. Proc Natl Acad Sci U S A 105 2800 2805

30. HattaMGaoPHalfmannPKawaokaY 2001 Molecular basis for high virulence of Hong Kong H5N1 influenza A viruses. Science 293 1840 1842

31. KobasaDTakadaAShinyaKHattaMHalfmannP 2004 Enhanced virulence of influenza A viruses with the haemagglutinin of the 1918 pandemic virus. Nature 431 703 707

32. MunsterVJde WitEvan RielDBeyerWERimmelzwaanGF 2007 The molecular basis of the pathogenicity of the Dutch highly pathogenic human influenza A H7N7 viruses. J Infect Dis 196 258 265

33. DasPLiJRoyyuruAKZhouR 2009 Free energy simulations reveal a double mutant avian H5N1 virus hemagglutinin with altered receptor binding specificity. J Comput Chem 30 1654 1663

34. HaYStevensDJSkehelJJWileyDC 2001 X-ray structures of H5 avian and H9 swine influenza virus hemagglutinins bound to avian and human receptor analogs. Proc Natl Acad Sci U S A 98 11181 11186

35. VeljkovicVVeljkovicNMullerCPMullerSGlisicS 2009 Characterization of conserved properties of hemagglutinin of H5N1 and human influenza viruses: possible consequences for therapy and infection control. BMC Struct Biol 9 21

36. KongchanagulASuptawiwatOKanraiPUiprasertkulMPuthavathanaP 2008 Positive selection at the receptor-binding site of haemagglutinin H5 in viral sequences derived from human tissues. J Gen Virol 89 1805 1810

37. BelserJABlixtOChenLMPappasCMainesTR 2008 Contemporary North American influenza H7 viruses possess human receptor specificity: Implications for virus transmissibility. Proc Natl Acad Sci U S A 105 7558 7563

38. Van HoevenNPappasCBelserJAMainesTRZengH 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

39. ParrishCRKawaokaY 2005 The origins of new pandemic viruses: the acquisition of new host ranges by canine parvovirus and influenza A viruses. Annu Rev Microbiol 59 553 586

40. Ayora-TalaveraGSheltonHScullMARenJJonesIM 2009 Mutations in H5N1 influenza virus hemagglutinin that confer binding to human tracheal airway epithelium. PLoS One 4 e7836

41. IlyushinaNAGovorkovaEAGrayTEBovinNVWebsterRG 2008 Human-like receptor specificity does not affect the neuraminidase-inhibitor susceptibility of H5N1 influenza viruses. PLoS Pathog 4 e1000043

42. ChutinimitkulSvan RielDMunsterVJvan den BrandJMRimmelzwaanGF 2010 In vitro assessment of attachment pattern and replication efficiency of H5N1 influenza A viruses with altered receptor specificity. J Virol 84 6825 6833

43. NichollsJMChanMCChanWYWongHKCheungCY 2007 Tropism of avian influenza A (H5N1) in the upper and lower respiratory tract. Nat Med 13 147 149

44. Egypt State Information Service Bird Flu. Bird Flu in Egypt. Available: http://birdflu.sis.gov.eg/html/. Accessed 10 November 2010

45. GaoPWatanabeSItoTGotoHWellsK 1999 Biological heterogeneity, including systemic replication in mice, of H5N1 influenza A virus isolates from humans in Hong Kong. J Virol 73 3184 3189

46. HarfordCGHamlinA 1952 Effect of influenza virus on cilia and epithelial cells in the bronchi of mice. J Exp Med 95 173 190

47. HattaMHattaYKimJHWatanabeSShinyaK 2007 Growth of H5N1 influenza A viruses in the upper respiratory tracts of mice. PLoS Pathog 3 1374 1379

48. ImaiHShinyaKTakanoRKisoMMuramotoY 2010 The HA and NS genes of human H5N1 influenza A virus contribute to high virulence in ferrets. PLoS Pathog 6 e1001106

49. NingZYLuoMYQiWBYuBJiaoPR 2009 Detection of expression of influenza virus receptors in tissues of BALB/c mice by histochemistry. Vet Res Commun 33 895 903

50. CastranovaVRJRabovskyJTuckerJHMilesPR 1988 The alveolar type II epithelial cell: a multifunctional pneumocyte. Toxicol Appl Pharmacol 93 472 483

51. SalomonRFranksJGovorkovaEAIlyushinaNAYenHL 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

52. BoltzDADouangngeunBPhommachanhPSinthasakSMondryR 2010 Emergence of H5N1 avian influenza viruses with reduced sensitivity to neuraminidase inhibitors and novel reassortants in Lao People's Democratic Republic. J Gen Virol 91 949 959

53. KimbleBNietoGRPerezDR 2010 Characterization of influenza virus sialic acid receptors in minor poultry species. Virol J 7 365

54. AbdelwhabEMHafezHMAlyMMGrundCHarderTC 2010 Increasing prevalence of unique mutation patterns in H5N1 avian influenza virus HA and NA glycoproteins from human infections in Egypt. Sequencing 2010 1 4

55. FusaroAJoannisTMonneISalviatoAYakubuB 2009 Introduction into Nigeria of a distinct genotype of avian influenza virus (H5N1). Emerg Infect Dis 15 445 447

56. MonneIJoannisTMFusaroADe BenedictisPLombinLH 2008 Reassortant avian influenza virus (H5N1) in poultry, Nigeria, 2007. Emerg Infect Dis 14 637 640

57. OwoadeAAGerloffNADucatezMFTaiwoJOKremerJR 2008 Replacement of sublineages of avian influenza (H5N1) by reassortments, sub-Saharan Africa. Emerg Infect Dis 14 1731 1735

58. BahgatMMKutkatMANasraaMHMostafaAWebbyR 2009 Characterization of an avian influenza virus H5N1 Egyptian isolate. J Virol Methods 159 244 250

59. Di LonardoAButtinelliGAmatoCNovelloFRidolfiB 2002 Rapid methods for identification of poliovirus isolates and determination of polio neutralizing antibody titers in human sera. J Virol Methods 101 189 196

60. WatanabeYOhtakiNHayashiYIkutaKTomonagaK 2009 Autogenous translational regulation of the Borna disease virus negative control factor X from polycistronic mRNA using host RNA helicases. PLoS Pathog 5 e1000654

61. HoffmannEStechJGuanYWebsterRGPerezDR 2001 Universal primer set for the full-length amplification of all influenza A viruses. Arch Virol 146 2275 2289

62. WatanabeYIbrahimMSHagiwaraKOkamotoMKamitaniW 2007 Characterization of a Borna disease virus field isolate which shows efficient viral propagation and transmissibility. Microbes Infect 9 417 427

63. FodorEDevenishLEngelhardtOGPalesePBrownleeGG 1999 Rescue of influenza A virus from recombinant DNA. J Virol 73 9679 9682

64. TamuraKDudleyJNeiMKumarS 2007 MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24 1596 1599

65. KatohKMisawaKKumaKMiyataT 2002 MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 30 3059 3066

66. YamadaSHattaMStakerBLWatanabeSImaiH 2010 Biological and structural characterization of a host-adapting amino acid in influenza virus. PLoS Pathog 6 e1001034

67. GotoJKataokaRMutaHHirayamaN 2008 ASEDock-docking based on alpha spheres and excluded volumes. J Chem Inf Model 48 583 590