Directed selection of influenza virus produces antigenic variants that match circulating human virus isolates and escape from vaccine-mediated immune protection

Immunology

Volumn 148, Issue 2, 2016, Pages 160-173

  Dediego, Marta L ^a   Anderson, Christopher S ^a   Yang, Hongmei ^a   Holden Wiltse, Jeanne ^a   Fitzgerald, Theresa ^a   Treanor, John J ^a   Topham, David J ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

Antigenic drift; Circulating strains; Haemagglutinin; Human influenza virus; Influenza virus vaccination; Influenza specific antibodies; Vaccine strain

Indexed keywords

AMINO ACID; INFLUENZA VACCINE; INFLUENZA VIRUS HEMAGGLUTININ; VIRUS ANTIBODY;

ANIMAL CELL; ANTIBODY BLOOD LEVEL; ANTIBODY TITER; ANTIGENIC VARIATION; ARTICLE; GENE MUTATION; IMMUNITY; IN VITRO STUDY; INFECTION RISK; INFLUENZA A VIRUS (H3N2); INFLUENZA VACCINATION; MDCK CELL LINE; NONHUMAN; PRIORITY JOURNAL; SEASONAL INFLUENZA; VACCINE FAILURE; VIRUS ISOLATION; ANIMAL; BLOOD; CELL LINE; COHORT ANALYSIS; GENETICS; HUMAN; HUMORAL IMMUNITY; IMMUNOLOGY; INFANT; INFLUENZA; INFLUENZA A VIRUS (H1N1); MUSTELA PUTORIUS FURO; PRESCHOOL CHILD; PROSPECTIVE STUDY; SEASON; SITE DIRECTED MUTAGENESIS; TREATMENT OUTCOME; VACCINATION;

ANIMALS; ANTIBODIES, VIRAL; ANTIGENIC VARIATION; CELL LINE; CHILD, PRESCHOOL; COHORT STUDIES; FERRETS; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; HUMANS; IMMUNITY, HUMORAL; INFANT; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA A VIRUS, H3N2 SUBTYPE; INFLUENZA VACCINES; INFLUENZA, HUMAN; MUTAGENESIS, SITE-DIRECTED; PROSPECTIVE STUDIES; SEASONS; TREATMENT OUTCOME; VACCINATION;

EID: 84962745221     PISSN: 00192805     EISSN: 13652567     Source Type: Journal    
DOI: 10.1111/imm.12594     Document Type: Article

References (48)

1. Cox NJ, Subbarao K. Global epidemiology of influenza: past and present. Annu Rev Med 2000; 51:407-21.
2. Hensley SE. Challenges of selecting seasonal influenza vaccine strains for humans with diverse pre-exposure histories. Curr Opin Virol 2014; 8:85-9.
3. Nicholls JM, Chan RW, Russell RJ, Air GM, Peiris JS. Evolving complexities of influenza virus and its receptors. Trends Microbiol 2008; 16:149-57.
4. Virelizier JL. Host defenses against influenza virus: the role of anti-hemagglutinin antibody. J Immunol 1975; 115:434-9.
5. Eichelberger MC, Wan H. Influenza neuraminidase as a vaccine antigen. Curr Top Microbiol Immunol 2015; 386:275-99.
6. Wohlbold TJ, Krammer F. In the shadow of hemagglutinin: a growing interest in influenza viral neuraminidase and its role as a vaccine antigen. Viruses 2014; 6:2465-94.
7. Corti D, Voss J, Gamblin SJ, Codoni G, Macagno A, Jarrossay D et al. A neutralizing antibody selected from plasma cells that binds to group 1 and group 2 influenza A hemagglutinins. Science 2011; 333:850-6.
8. Ekiert DC, Bhabha G, Elsliger MA, Friesen RH, Jongeneelen M, Throsby M et al. Antibody recognition of a highly conserved influenza virus epitope. Science 2009; 324:246-51.
9. Sui J, Hwang WC, Perez S, Wei G, Aird D, Chen LM et al. Structural and functional bases for broad-spectrum neutralization of avian and human influenza A viruses. Nat Struct Mol Biol 2009; 16:265-73.
10. Xu R, Ekiert DC, Krause JC, Hai R, Crowe JE Jr, Wilson IA. Structural basis of preexisting immunity to the 2009 H1N1 pandemic influenza virus. Science 2010; 328:357-60.
11. Steel J, Lowen AC, Wang TT, Yondola M, Gao Q, Haye K et al. Influenza virus vaccine based on the conserved hemagglutinin stalk domain. MBio 2010; 1:e00018-10.
12. Margine I, Krammer F, Hai R, Heaton NS, Tan GS, Andrews SA et al. Hemagglutinin stalk-based universal vaccine constructs protect against group 2 influenza A viruses. J Virol 2013; 87:10435-46.
13. Smith DJ, Lapedes AS, de Jong JC, Bestebroer TM, Rimmelzwaan GF, Osterhaus AD et al. Mapping the antigenic and genetic evolution of influenza virus. Science 2004; 305:371-6.
14. Laver WG, Air GM, Webster RG, Markoff LJ. Amino acid sequence changes in antigenic variants of type A influenza virus N2 neuraminidase. Virology 1982; 122:450-60.
15. Kilbourne ED, Johansson BE, Grajower B. Independent and disparate evolution in nature of influenza A virus hemagglutinin and neuraminidase glycoproteins. Proc Natl Acad Sci USA 1990; 87:786-90.
16. Shih AC, Hsiao TC, Ho MS, Li WH. Simultaneous amino acid substitutions at antigenic sites drive influenza A hemagglutinin evolution. Proc Natl Acad Sci USA 2007; 104:6283-8.
17. Wilson IA, Cox NJ. Structural basis of immune recognition of influenza virus hemagglutinin. Annu Rev Immunol 1990; 8:737-71.
18. Blackburne BP, Hay AJ, Goldstein RA. Changing selective pressure during antigenic changes in human influenza H3. PLoS Pathog 2008; 4:e1000058.
19. Matsuzaki Y, Sugawara K, Nakauchi M, Takahashi Y, Onodera T, Tsunetsugu-Yokota Y et al. Epitope mapping of the hemagglutinin molecule of A/(H1N1)pdm09 influenza virus by using monoclonal antibody escape mutants. J Virol 2014; 88:12364-73.
20. Lambkin R, McLain L, Jones SE, Aldridge SL, Dimmock NJ. Neutralization escape mutants of type A influenza virus are readily selected by antisera from mice immunized with whole virus: a possible mechanism for antigenic drift. J Gen Virol 1994; 75(Pt 12):3493-502.
21. Sitaras I, Kalthoff D, Beer M, Peeters B, de Jong MC. Immune escape mutants of highly pathogenic avian influenza H5N1 selected using polyclonal sera: identification of key amino acids in the HA protein. PLoS ONE 2014; 9:e84628.
22. Haaheim LR, Tomasov CC, Barr IG, Hampson AW, Komadina N. Identification of genetic diversity by cultivating influenza A(H3N2) virus in vitro in the presence of post-infection sera from small children. Vaccine 2006; 24:6708-11.
23. Flannery B, Clippard J, Zimmerman RK, Nowalk MP, Jackson ML, Jackson LA et al. Early estimates of seasonal influenza vaccine effectiveness - United States, January 2015. MMWR Morb Mortal Wkly Rep 2015; 64:10-15.
24. Appiah GD, Blanton L, D'Mello T, Kniss K, Smith S, Mustaquim D et al. Influenza activity - United States, 2014-15 season and composition of the 2015-16 influenza vaccine. MMWR Morb Mortal Wkly Rep 2015; 64:583-90.
25. Chambers BS, Parkhouse K, Ross TM, Alby K, Hensley SE. Identification of hemagglutinin residues responsible for H3N2 antigenic drift during the 2014-2015 influenza season. Cell Rep 2015; 12:1-6.
26. Skowronski DM, Janjua NZ, De Serres G, Sabaiduc S, Eshaghi A, Dickinson JA et al. Low 2012-13 influenza vaccine effectiveness associated with mutation in the egg-adapted H3N2 vaccine strain not antigenic drift in circulating viruses. PLoS ONE 2014; 9:e92153.
27. Osterholm MT, Kelley NS, Sommer A, Belongia EA. Efficacy and effectiveness of influenza vaccines: a systematic review and meta-analysis. Lancet Infect Dis 2012; 12:36-44.
28. Guindon S, Gascuel O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 2003; 52:696-704.
29. Gupta V, Earl DJ, Deem MW. Quantifying influenza vaccine efficacy and antigenic distance. Vaccine 2006; 24:3881-8.
30. Ndifon W, Wingreen NS, Levin SA. Differential neutralization efficiency of hemagglutinin epitopes, antibody interference, and the design of influenza vaccines. Proc Natl Acad Sci USA 2009; 106:8701-6.
31. Wiley DC, Wilson IA, Skehel JJ. Structural identification of the antibody-binding sites of Hong Kong influenza haemagglutinin and their involvement in antigenic variation. Nature 1981; 289:373-8.
32. Koel BF, Burke DF, Bestebroer TM, van der Vliet S, Zondag GC, Vervaet G et al. Substitutions near the receptor binding site determine major antigenic change during influenza virus evolution. Science 2013; 342:976-9.
33. Li Y, Myers JL, Bostick DL, Sullivan CB, Madara J, Linderman SL et al. Immune history shapes specificity of pandemic H1N1 influenza antibody responses. J Exp Med 2013; 210:1493-500.
34. Lin YP, Gregory V, Collins P, Kloess J, Wharton S, Cattle N et al. Neuraminidase receptor binding variants of human influenza A(H3N2) viruses resulting from substitution of aspartic acid 151 in the catalytic site: a role in virus attachment? J Virol 2010; 84:6769-81.
35. Chambers BS, Li Y, Hodinka RL, Hensley SE. Recent H3N2 influenza virus clinical isolates rapidly acquire hemagglutinin or neuraminidase mutations when propagated for antigenic analyses. J Virol 2014; 88:10986-9.
36. Collins PJ, Haire LF, Lin YP, Liu J, Russell RJ, Walker PA et al. Crystal structures of oseltamivir-resistant influenza virus neuraminidase mutants. Nature 2008; 453:1258-61.
37. Zhu X, McBride R, Nycholat CM, Yu W, Paulson JC, Wilson IA. Influenza virus neuraminidases with reduced enzymatic activity that avidly bind sialic acid receptors. J Virol 2012; 86:13371-83.
38. Hensley SE, Das SR, Bailey AL, Schmidt LM, Hickman HD, Jayaraman A et al. Hemagglutinin receptor binding avidity drives influenza A virus antigenic drift. Science 2009; 326:734-6.
39. Li Y, Bostick DL, Sullivan CB, Myers JL, Griesemer SB, Stgeorge K et al. Single hemagglutinin mutations that alter both antigenicity and receptor binding avidity influence influenza virus antigenic clustering. J Virol 2013; 87:9904-10.
40. Yewdell JW, Caton AJ, Gerhard W. Selection of influenza A virus adsorptive mutants by growth in the presence of a mixture of monoclonal antihemagglutinin antibodies. J Virol 1986; 57:623-8.
41. Nakajima S, Nobusawa E, Nakajima K. Variation in response among individuals to antigenic sites on the HA protein of human influenza virus may be responsible for the emergence of drift strains in the human population. Virology 2000; 274:220-31.
42. Eshaghi A, Duvvuri VR, Li A, Patel SN, Bastien N, Li Y et al. Genetic characterization of seasonal influenza A (H3N2) viruses in Ontario during 2010-2011 influenza season: high prevalence of mutations at antigenic sites. Influenza Other Respir Viruses 2014; 8:250-7.
43. Guihot A, Luyt CE, Parrot A, Rousset D, Cavaillon JM, Boutolleau D et al. Low titers of serum antibodies inhibiting hemagglutination predict fatal fulminant influenza A(H1N1) 2009 infection. Am J Respir Crit Care Med 2014; 189:1240-9.
44. Skountzou I, Koutsonanos DG, Kim JH, Powers R, Satyabhama L, Masseoud F et al. Immunity to pre-1950 H1N1 influenza viruses confers cross-protection against the pandemic swine-origin 2009 A (H1N1) influenza virus. J Immunol 2010; 185:1642-9.
45. Jacobs JH, Archer BN, Baker MG, Cowling BJ, Heffernan RT, Mercer G et al. Searching for sharp drops in the incidence of pandemic A/H1N1 influenza by single year of age. PLoS ONE 2012; 7:e42328.
46. Lin YP, Xiong X, Wharton SA, Martin SR, Coombs PJ, Vachieri SG et al. Evolution of the receptor binding properties of the influenza A(H3N2) hemagglutinin. Proc Natl Acad Sci USA 2012; 109:21474-9.
47. Gulati S, Smith DF, Cummings RD, Couch RB, Griesemer SB, St George K et al. Human H3N2 influenza viruses isolated from 1968 to 2012 show varying preference for receptor substructures with no apparent consequences for disease or spread. PLoS ONE 2013; 8:e66325.
48. Hooper KA, Bloom JD. A mutant influenza virus that uses an N1 neuraminidase as the receptor-binding protein. J Virol 2013; 87:12531-40.