Structural and Antigenic Variation among Diverse Clade 2 H5N1 Viruses

PLoS ONE

Volumn 8, Issue 9, 2013, Pages

  Shore, David A ^a   Yang, Hua ^a   Balish, Amanda L ^a   Shepard, Samuel S ^a   Carney, Paul J ^a   Chang, Jessie C ^a   Davis, Charles T ^a   Donis, Ruben O ^a   Villanueva, Julie M ^a   Klimov, Alexander I ^a   Stevens, James ^a  

^a CENTERS FOR DISEASE CONTROL AND PREVENTION   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INFLUENZA VIRUS HEMAGGLUTININ; SIALIC ACID;

AMINO ACID SUBSTITUTION; ANTIGENIC VARIATION; ANTIGENICITY; ARTICLE; BINDING SITE; CLADISTICS; COMPARATIVE STUDY; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENVIRONMENTAL FACTOR; HOST RANGE; INFLUENZA VIRUS A H5N1; NONHUMAN; PHYLOGENY; PROTEIN CONFORMATION; RECEPTOR BINDING; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; SPECIES DIVERSITY; STRUCTURAL BIOINFORMATICS; STRUCTURE ACTIVITY RELATION; VIRUS CELL INTERACTION; VIRUS ISOLATION; VIRUS PATHOGENESIS; VIRUS STRAIN; VIRUS TRANSMISSION;

ANTIGENIC VARIATION; BASE SEQUENCE; CLONING, MOLECULAR; COMPUTATIONAL BIOLOGY; CRYSTALLIZATION; EPITOPES; HEMAGGLUTININS, VIRAL; HUMANS; INFLUENZA A VIRUS, H5N1 SUBTYPE; INFLUENZA VACCINES; MODELS, MOLECULAR; PHYLOGENY; PROTEIN CONFORMATION; SEQUENCE ALIGNMENT;

EID: 84884697289     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0075209     Document Type: Article

References (84)

1. Jia N, de Vlas SJ, Liu YX, Zhang JS, Zhan L, et al. (2009) Serological reports of human infections of H7 and H9 avian influenza viruses in northern China. J Clin Virol 44: 225-229.
2. CDC (2012) Notes from the Field: Highly Pathogenic Avian Influenza A (H7N3) Virus Infection in Two Poultry Workers- Jalisco, Mexico, July 2012. MMWR Morb Mortal Wkly Rep 61: 726-727.
3. Watanabe Y, Ibrahim MS, Ellakany HF, Kawashita N, Mizuike R, 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.
4. WHO (2012) Cumulative number of confirmed human cases of avian influenza A(H5N1) reported to WHO. http://www.who.int/influenza/human_animal_interface/H5N1_cumulative_table_archives/en/index.html. Accessed 2013 Aug 16.
5. Ungchusak K, Auewarakul P, Dowell SF, Kitphati R, Auwanit W, et al. (2005) Probable person-to-person transmission of avian influenza A (H5N1). N Engl J Med 352: 333-340.
6. WHO (2006) Avian influenza situation in Indonesia- update 16. http://www.who.int/csr/don/2006_05_31/en/index.html. Accessed 2013 Aug 16.
7. Wang H, Feng Z, Shu Y, Yu H, Zhou L, et al. (2008) Probable limited person-to-person transmission of highly pathogenic avian influenza A (H5N1) virus in China. Lancet 371: 1427-1434.
8. WHO (2008) Human cases of avian influenza A (H5N1) in North-West Frontier Province, Pakistan, October-November 2007. Wkly Epidemiol Rec 83: 359-364.
9. Fauci AS, (2006) Seasonal and pandemic influenza preparedness: science and countermeasures. J Infect Dis 194Suppl 2: S73-76.
10. Fitch WM, Leiter JM, Li XQ, Palese P, (1991) Positive Darwinian evolution in human influenza A viruses. Proc Natl Acad Sci U S A 88: 4270-4274.
11. WHO_OIE_FAO_H5N1_Evolution_Working_Group (2008) Toward a unified nomenclature system for highly pathogenic avian influenza virus (H5N1). Emerg Infect Dis 14: e1.
12. WHO_OIE_FAO_H5N1_Evolution_Working_Group (2009) Continuing progress towards a unified nomenclature for the highly pathogenic H5N1 avian influenza viruses: divergence of clade 2.2 viruses. Influenza Other Respi Viruses 3: 59-62.
13. Yang JX, Ju LW, Jiang LF, Shi Q, Jiang QW, et al. (2009) [Type and subtype distribution of influenza virus and genetic evolution of hemagglutinin in Shanghai area in duration of 2004-2008]. Zhonghua Yu Fang Yi Xue Za Zhi 43: 305-308.
14. WHO (2010) Antigenic and genetic characteristics of influenza A(H5N1)and influenza A(H9N2) viruses and candidate vaccine viruses developed for potential use in human vaccines. Wkly Epidemiol Rec 85: 418-424.
15. WHO (2011) Antigenic and genetic characteristics of influenza A(H5N1) and influenza A(H9N2) viruses for development of candidate vaccines viruses for pandemic preparedness- February 2011. Wkly Epidemiol Rec 86: 93-100.
16. WHO (2012) Antigenic and genetic characteristics of zoonotic influenza viruses and development of candidate vaccine viruses for pandemic preparedness. Wkly Epidemiol Rec 87: 97-108.
17. Tang JW, Ngai KL, Chan PK, (2008) Lack of cross-immune reactivity against influenza H5N1 from seasonal influenza vaccine in humans. J Med Virol 80: 1992-1996.
18. Treanor JJ, Campbell JD, Zangwill KM, Rowe T, Wolff M, (2006) Safety and immunogenicity of an inactivated subvirion influenza A (H5N1) vaccine. N Engl J Med 354: 1343-1351.
19. Russell CA, Jones TC, Barr IG, Cox NJ, Garten RJ, et al. (2008) Influenza vaccine strain selection and recent studies on the global migration of seasonal influenza viruses. Vaccine 26Suppl 4: D31-34.
20. World Health Orgnization (2013) Candidate vaccine viruses and potency testing reagents for influenza A(H5N1). Geneva.
21. Peiris JS, Poon LL, Guan Y, (2012) Public health. Surveillance of animal influenza for pandemic preparedness. Science 335: 1173-1174.
22. Chandrasekaran A, Srinivasan A, Raman R, Viswanathan K, Raguram S, et al. (2008) Glycan topology determines human adaptation of avian H5N1 virus hemagglutinin. Nat Biotechnol 26: 107-113.
23. Ito T, Couceiro JN, Kelm S, Baum LG, Krauss S, et al. (1998) Molecular basis for the generation in pigs of influenza A viruses with pandemic potential. J Virol 72: 7367-7373.
24. Matrosovich MN, Matrosovich TY, Gray T, Roberts NA, Klenk H-D, (2004) Human and avian influenza viruses target different cell types in cultures of human airway epithelium. Proc Natl Acad Sci USA 101: 4620-4624.
25. Shinya K, Ebina M, Yamada S, Ono M, Kasai N, et al. (2006) Avian flu: influenza virus receptors in the human airway. Nature 440: 435-436.
26. Herfst S, Schrauwen EJ, Linster M, Chutinimitkul S, de Wit E, et al. (2012) Airborne transmission of influenza A/H5N1 virus between ferrets. Science 336: 1534-1541.
27. Imai M, Kawaoka Y, (2012) The role of receptor binding specificity in interspecies transmission of influenza viruses. Curr Opin Virol 2: 160-167.
28. Imai M, Watanabe T, Hatta M, Das SC, Ozawa M, 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.
29. Russell RJ, Stevens DJ, Haire LF, Gamblin SJ, Skehel JJ, (2006) Avian and human receptor binding by hemagglutinins of influenza A viruses. Glycoconj J 23: 85-92.
30. Yamada S, Suzuki Y, Suzuki T, Le MQ, Nidom CA, et al. (2006) Haemagglutinin mutations responsible for the binding of H5N1 influenza A viruses to human-type receptors. Nature 444: 378-382.
31. Wan XF, Dong L, Lan Y, Long LP, Xu C, et al. (2011) Indications that live poultry markets are a major source of human H5N1 influenza virus infection in China. J Virol 85: 13432-13438.
32. Younan M, Poh MK, Elassal E, Davis T, Rivailler P, et al. (2013) Microevolution of highly pathogenic avian influenza A(H5N1) viruses isolated from humans, Egypt, 2007-2011. Emerg Infect Dis 19: 43-50.
33. WHO OIE FAO H5N1 Evolution Working Group (2012) Continued evolution of highly pathogenic avian influenza A (H5N1): Updated nomenclature. Influenza Other Respi Viruses 6: 1-5.
34. Lee MS, Yang CF, (2003) Cross-reactive H1N1 antibody responses to a live attenuated influenza vaccine in children: implication for selection of vaccine strains. J Infect Dis 188: 1362-1366.
35. Subbarao K, Chen H, Swayne D, Mingay L, Fodor E, et al. (2003) Evaluation of a genetically modified reassortant H5N1 influenza A virus vaccine candidate generated by plasmid-based reverse genetics. Virology 305: 192-200.
36. Stevens J, Blixt O, Tumpey TM, Taubenberger JK, Paulson JC, et al. (2006) Structure and receptor specificity of the hemagglutinin from an H5N1 influenza virus. Science 312: 404-410.
37. Liu J, Stevens DJ, Haire LF, Walker PA, Coombs PJ, et al. (2009) Structures of receptor complexes formed by hemagglutinins from the Asian Influenza pandemic of 1957. Proc Natl Acad Sci U S A 106: 17175-17180.
38. Skehel JJ, Wiley DC, (2000) Receptor binding and membrane fusion in virus entry: the influenza hemagglutinin. Annu Rev Biochem 69: 531-569.
39. Caton AJ, Brownlee GG, Yewdell JW, Gerhard W, (1982) The antigenic structure of the influenza virus A/PR/8/34 hemagglutinin (H1 subtype). Cell 31: 417-427.
40. Kaverin NV, Rudneva IA, Govorkova EA, Timofeeva TA, Shilov AA, et al. (2007) Epitope mapping of the hemagglutinin molecule of a highly pathogenic H5N1 influenza virus by using monoclonal antibodies. J Virol 81: 12911-12917.
41. Cai Z, Ducatez MF, Yang J, Zhang T, Long LP, et al. (2012) Identifying Antigenicity-Associated Sites in Highly Pathogenic H5N1 Influenza Virus Hemagglutinin by Using Sparse Learning. J Mol Biol 422: 145-155.
42. Auewarakul P, Suptawiwat O, Kongchanagul A, Sangma C, Suzuki Y, et al. (2007) An avian influenza H5N1 virus that binds to a human-type receptor. J Virol 81: 9950-9955.
43. Gao Y, Zhang Y, Shinya K, Deng G, Jiang Y, 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.
44. Ilyushina NA, Govorkova EA, Gray TE, Bovin NV, Webster RG, (2008) Human-like receptor specificity does not affect the neuraminidase-inhibitor susceptibility of H5N1 influenza viruses. PLoS Pathog 4: e1000043.
45. Kongchanagul A, Suptawiwat O, Kanrai P, Uiprasertkul M, Puthavathana P, et al. (2008) Positive selection at the receptor-binding site of haemagglutinin H5 in viral sequences derived from human tissues. J Gen Virol 89: 1805-1810.
46. Maines TR, Chen LM, Van Hoeven N, Tumpey TM, Blixt O, et al. (2011) Effect of receptor binding domain mutations on receptor binding and transmissibility of avian influenza H5N1 viruses. Virology 413: 139-147.
47. Naughtin M, Dyason JC, Mardy S, Sorn S, von Itzstein M, et al. (2011) Neuraminidase inhibitor sensitivity and receptor-binding specificity of Cambodian clade 1 highly pathogenic H5N1 influenza virus. Antimicrob Agents Chemother 55: 2004-2010.
48. Stevens J, Blixt O, Chen LM, Donis RO, Paulson JC, et al. (2008) Recent avian H5N1 viruses exhibit increased propensity for acquiring human receptor specificity. J Mol Biol 381: 1382-1394.
49. Wang W, Lu B, Zhou H, Suguitan AL Jr, Cheng X, et al. (2010) 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: 6570-6577.
50. Yang ZY, Wei CJ, Kong WP, Wu L, Xu L, et al. (2007) Immunization by avian H5 influenza hemagglutinin mutants with altered receptor binding specificity. Science 317: 825-828.
51. Yen H-L, Aldridge JR, Boon ACM, Ilyushina NA, Salomon R, et al. (2009) Changes in H5N1 influenza virus hemagglutinin receptor binding domain affect systemic spread. Proc Natl Acad Sci USA 106: 286-291.
52. CDC (2012) H5N1 Genetic Changes Inventory: A Tool for Influenza Surveillance and Preparedness. http://wwwcdcgov/flu/avianflu/h5n1-genetic-changeshtm.
53. Stevens J, Blixt O, Glaser L, Taubenberger JK, Palese P, et al. (2006) Glycan microarray analysis of the hemagglutinins from modern and pandemic influenza viruses reveals different receptor specificities. J Mol Biol 355: 1143-1155.
54. Blixt O, Hoffmann J, Svenson S, Norberg T, (2008) Pathogen specific carbohydrate antigen microarrays: a chip for detection of Salmonella O-antigen specific antibodies. Glycoconj J 25: 27-36.
55. Guan Y, Poon LL, Cheung CY, Ellis TM, Lim W, et al. (2004) H5N1 influenza: a protean pandemic threat. Proc Natl Acad Sci U S A 101: 8156-8161.
56. Wu WL, Chen Y, Wang P, Song W, Lau SY, et al. (2008) Antigenic profile of avian H5N1 viruses in Asia from 2002 to 2007. J Virol 82: 1798-1807.
57. Rogers GN, Paulson JC, Daniels RS, Skehel JJ, Wilson IA, et al. (1983) Single amino acid substitutions in influenza haemagglutinin change receptor binding specificity. Nature 304: 76-78.
58. Connor RJ, Kawaoka Y, Webster RG, Paulson JC, (1994) Receptor specificity in human, avian, and equine H2 and H3 influenza virus isolates. Virology 205: 17-23.
59. Tumpey TM, Maines TR, Van Hoeven N, Glaser L, Solorzano A, et al. (2007) A two-amino acid change in the hemagglutinin of the 1918 influenza virus abolishes transmission. Science 315: 655-659.
60. Su Y, Yang HY, Zhang BJ, Jia HL, Tien P, (2008) Analysis of a point mutation in H5N1 avian influenza virus hemagglutinin in relation to virus entry into live mammalian cells. Arch Virol 153: 2253-2261.
61. de Vries RP, de Vries E, Bosch BJ, de Groot RJ, Rottier PJ, et al. (2010) The influenza A virus hemagglutinin glycosylation state affects receptor-binding specificity. Virology 403: 17-25.
62. Wang CC, Chen JR, Tseng YC, Hsu CH, Hung YF, et al. (2009) Glycans on influenza hemagglutinin affect receptor binding and immune response. Proc Natl Acad Sci U S A 106: 18137-18142.
63. Chen LM, Blixt O, Stevens J, Lipatov AS, Davis CT, et al. (2012) In vitro evolution of H5N1 avian influenza virus toward human-type receptor specificity. Virology 422: 105-113.
64. O'Neill E, Donis RO, (2009) Generation and characterization of candidate vaccine viruses for prepandemic influenza vaccines. Curr Top Microbiol Immunol 333: 83-108.
65. Frank S, Kammerer RA, Mechling D, Schulthess T, Landwehr R, et al. (2001) Stabilization of short collagen-like triple helices by protein engineering. J Mol Biol 308: 1081-1089.
66. Stevens J, Corper AL, Basler CF, Taubenberger JK, Palese P, et al. (2004) Structure of the uncleaved human H1 hemagglutinin from the extinct 1918 influenza virus. Science 303: 1866-1870.
67. Yang H, Carney P, Stevens J (2010) Structure and Receptor binding properties of a pandemic H1N1 virus hemagglutinin. PLoS Curr: RRN1152.
68. Yang H, Chen LM, Carney PJ, Donis RO, Stevens J, (2010) Structures of receptor complexes of a North American H7N2 influenza hemagglutinin with a loop deletion in the receptor binding site. PLoS Pathog 6: e1001081.
69. Chayen NE, Shaw-Steward PD, Blow DM, (1992) Microbatch crystallization under oil - a new technique allowing many small volume crystallization experiments J Cryst Growth. 122: 176-180.
70. Otwinowski A, Minor W, (1997) Processing of X-ray diffraction data collected in oscillation mode. Meothds in Enzymology 276: 307-326.
71. Emsley P, Cowtan K, (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60: 2126-2132.
72. Adams PD, Afonine PV, Bunkoczi G, Chen VB, Davis IW, et al. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 66: 213-221.
73. CCP4 (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr D Biol Crystallogr 50: 760-763.
74. Winn MD, Isupov MN, Murshudov GN, (2001) Use of TLS parameters to model anisotropic displacements in macromolecular refinement. Acta Crystallogr D Biol Crystallogr 57: 122-133.
75. Davis IW, Leaver-Fay A, Chen VB, Block JN, Kapral GJ, et al. (2007) MolProbity: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res 35: W375-383.
76. McCoy AJ, Grosse-Kunstleve RW, Storoni LC, Read RJ, (2005) Likelihood-enhanced fast translation functions. Acta Crystallogr D Biol Crystallogr 61: 458-464.
77. Blixt O, Head S, Mondala T, Scanlan C, Huflejt ME, et al. (2004) Printed covalent glycan array for ligand profiling of diverse glycan binding proteins. Proc Natl Acad Sci U S A 101: 17033-17038.
78. WHO (2011) Manual for the laboratory diagnosis and virological surveillance of Influenza. WHO Global Influenza Surveillance Network: 48-57.
79. Klimov A, Balish A, Veguilla V, Sun H, Schiffer J, et al. (2012) Influenza virus titration, antigenic characterization, and serological methods for antibody detection. Methods Mol Biol 865: 25-51.
80. Shepard SS, Davis CT, Bahl J, Rivailler P, York IA, et al. (2013) LABEL: fast and accurate lineage assignment with assessment of H5N1 and H9N2 influenza A hemagglutinins. http://137.132.104.5/label/. Accessed 2013 Aug 16.
81. Waterhouse AM, Procter JB, Martin DM, Clamp M, Barton GJ, (2009) Jalview Version 2-a multiple sequence alignment editor and analysis workbench. Bioinformatics 25: 1189-1191.
82. Katoh K, Misawa K, Kuma K, Miyata T, (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 30: 3059-3066.
83. Edgar RC, (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792-1797.
84. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG, (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25: 4876-4882.