The molecular determinants of antibody recognition and antigenic drift in the H3 hemagglutinin of swine influenza A virus

Journal of Virology

Volumn 90, Issue 18, 2016, Pages 8266-8280

  Abente, Eugenio J ^a   Santos, Jefferson ^b   Lewis, Nicola S ^c   Gauger, Phillip C ^d   Stratton, Jered ^a   Skepner, Eugene ^c   Anderson, Tavis K ^a   Rajao, Daniela S ^a   Perez, Daniel R ^b   Vincent, Amy L ^a  

^a NATIONAL ANIMAL DISEASE CENTER   (United States)

^b UNIVERSITY OF GEORGIA   (United States)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^d IOWA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INFLUENZA VIRUS HEMAGGLUTININ; UNCLASSIFIED DRUG; VIRUS HEMAGGLUTININ H3; MUTANT PROTEIN; VIRUS ANTIBODY; VIRUS ANTIGEN;

AMINO ACID SUBSTITUTION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN RECOGNITION; ANTIGENIC DRIFT; ANTIGENICITY; ARTICLE; CONTROLLED STUDY; HEMAGGLUTINATION INHIBITION; LUNG LESION; NONHUMAN; PHENOTYPE; PIG; PRIORITY JOURNAL; SWINE INFLUENZA VIRUS; VIRUS MUTANT; VIRUS PATHOGENESIS; VIRUS SHEDDING; VIRUS TITRATION; VIRUS TRANSMISSION; ANIMAL; GENETIC DRIFT; GENETICS; HEMAGGLUTINATION INHIBITION TEST; IMMUNOLOGY; INFLUENZA A VIRUS; LUNG; ORTHOMYXOVIRUS INFECTION; PATHOLOGY; REVERSE GENETICS; SITE DIRECTED MUTAGENESIS; SWINE DISEASE; TRANSMISSION; VETERINARY; VIROLOGY; VIRULENCE;

AMINO ACID SUBSTITUTION; ANIMALS; ANTIBODIES, VIRAL; ANTIGENS, VIRAL; GENETIC DRIFT; HEMAGGLUTINATION INHIBITION TESTS; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; INFLUENZA A VIRUS; LUNG; MUTAGENESIS, SITE-DIRECTED; MUTANT PROTEINS; ORTHOMYXOVIRIDAE INFECTIONS; REVERSE GENETICS; SWINE; SWINE DISEASES; VIRULENCE; VIRUS SHEDDING;

EID: 84984660071     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01002-16     Document Type: Article

References (56)

1. Huber VC. 2014. Influenza vaccines: from whole virus preparations to recombinant protein technology. Expert Rev Vaccines 13:31-42. http: //dx.doi.org/10.1586/14760584.2014.852476.
2. U.S. Department of Agriculture. 2007. Swine 2006. Part II: reference of swine health and health management practices in the United States, 2006. U.S. Department of Agriculture, Fort Collins, CO.
3. Ma W, Richt JA. 2010. Swine influenza vaccines: current status and future perspectives. Anim Health Res Rev 11:81-96. http://dx.doi.org/10.1017 /S146625231000006X.
4. Krammer F, Palese P. 2015. Advances in the development of influenza virus vaccines. Nat Rev Drug Discov 14:167-182. http://dx.doi.org/10.1038/nrd4529.
5. Wiley DC, Wilson IA, Skehel JJ. 1981. Structural identification of the antibody-binding sites of Hong Kong influenza haemagglutinin and their involvement in antigenic variation. Nature 289:373-378. http://dx.doi.org/10.1038/289373a0.
6. Bush RM, Bender CA, Subbarao K, Cox NJ, Fitch WM. 1999. Predicting the evolution of human influenza A. Science 286:1921-1925. http://dx.doi.org/10.1126/science.286.5446.1921.
7. Lapedes A, Farber R. 2001. The geometry of shape space: application to influenza. J Theor Biol 212:57-69. http://dx.doi.org/10.1006/jtbi.2001.2347.
8. Lewis NS, Anderson TK, Kitikoon P, Skepner E, Burke DF, Vincent AL. 2014. Substitutions near the hemagglutinin receptor-binding site determine the antigenic evolution of influenza A H3N2 viruses in U.S. swine. J Virol 88:4752-4763. http://dx.doi.org/10.1128/JVI.03805-13.
9. Smith DJ, Lapedes AS, de Jong JC, Bestebroer TM, Rimmelzwaan GF, Osterhaus AD, Fouchier RA. 2004. Mapping the antigenic and genetic evolution of influenza virus. Science 305:371-376. http://dx.doi.org/10.1126/science.1097211.
10. Lewis NS, Daly JM, Russell CA, Horton DL, Skepner E, Bryant NA, Burke DF, Rash AS, Wood JL, Chambers TM, Fouchier RA, Mumford JA, Elton DM, Smith DJ. 2011. Antigenic and genetic evolution of equine influenza A (H3N8) virus from 1968 to 2007. J Virol 85:12742-12749. http://dx.doi.org/10.1128/JVI.05319-11.
11. Ampofo WK, Azziz-Baumgartner E, Bashir U, Cox NJ, Fasce R, Giovanni M, Grohmann G, Huang S, Katz J, Mironenko A, Mokhtari-Azad T, Sasono PM, Rahman M, Sawanpanyalert P, Siqueira M, Waddell AL, Waiboci L, Wood J, Zhang W, Ziegler T, WHO Writing Group. 2015. Strengthening the influenza vaccine virus selection and development process: report of the 3rd WHO Informal Consultation for Improving Influenza Vaccine Virus Selection held at WHO headquarters, Geneva, Switzerland, 1-3 April 2014. Vaccine 33:4368-4382. http://dx.doi.org/10.1016/j.vaccine.2015.06.090.
12. Barr IG, Russell C, Besselaar TG, Cox NJ, Daniels RS, Donis R, Engelhardt OG, Grohmann G, Itamura S, Kelso A, McCauley J, Odagiri T, Schultz-Cherry S, Shu Y, Smith D, Tashiro M, Wang D, Webby R, Xu X, Ye Z, Zhang W, Writing Committee of the World Health Organization Consultation on Northern Hemisphere Influenza Vaccine Composition for 2013-2014. 2014. WHO recommendations for the viruses used in the 2013-2014 Northern Hemisphere influenza vaccine: epidemiology, antigenic and genetic characteristics of influenza A(H1N1)pdm09, A(H3N2) and B influenza viruses collected from October 2012 to January 2013. Vaccine 32:4713-4725. http://dx.doi.org/10.1016/j.vaccine.2014.02.014.
13. Russell CA, Jones TC, Barr IG, Cox NJ, Garten RJ, Gregory V, Gust ID, Hampson AW, Hay AJ, Hurt AC, de Jong JC, Kelso A, Klimov AI, Kageyama T, Komadina N, Lapedes AS, Lin YP, Mosterin A, Obuchi M, Odagiri T, Osterhaus AD, Rimmelzwaan GF, Shaw MW, Skepner E, Stohr K, Tashiro M, Fouchier RA, Smith DJ. 2008. Influenza vaccine strain selection and recent studies on the global migration of seasonal influenza viruses. Vaccine 26(Suppl 4):D31-D34. http://dx.doi.org/10.1016/j.vaccine.2008.07.078.
14. Koel BF, Burke DF, Bestebroer TM, van der Vliet S, Zondag GC, Vervaet G, Skepner E, Lewis NS, Spronken MI, Russell CA, Eropkin MY, Hurt AC, Barr IG, de Jong JC, Rimmelzwaan GF, Osterhaus AD, Fouchier RA, Smith DJ. 2013. Substitutions near the receptor binding site determine major antigenic change during influenza virus evolution. Science 342:976-979. http://dx.doi.org/10.1126/science.1244730.
15. Feng Z, Gomez J, Bowman AS, Ye J, Long LP, Nelson SW, Yang J, Martin B, Jia K, Nolting JM, Cunningham F, Cardona C, Zhang J, Yoon KJ, Slemons RD, Wan XF. 2013. Antigenic characterization of H3N2 influenza A viruses from Ohio agricultural fairs. J Virol 87:7655-7667. http://dx.doi.org/10.1128/JVI.00804-13.
16. Anderson TK, Nelson MI, Kitikoon P, Swenson SL, Korslund JA, Vincent AL. 2013. Population dynamics of cocirculating swine influenza A viruses in the United States from 2009 to 2012. Influenza Other Respir Viruses 7(Suppl 4):S42-S51.
17. Tang Y, Lee CW, Zhang Y, Senne DA, Dearth R, Byrum B, Perez DR, Suarez DL, Saif YM. 2005. Isolation and characterization of H3N2 influenza A virus from turkeys. Avian Dis 49:207-213. http://dx.doi.org/10.1637/7288-101304R.
18. Pena L, Vincent AL, Ye J, Ciacci-Zanella JR, Angel M, Lorusso A, Gauger PC, Janke BH, Loving CL, Perez DR. 2011. Modifications in the polymerase genes of a swine-like triple-reassortant influenza virus to generate live attenuated vaccines against 2009 pandemic H1N1 viruses. J Virol 85:456-469. http://dx.doi.org/10.1128/JVI.01503-10.
19. Chen H, Ye J, Xu K, Angel M, Shao H, Ferrero A, Sutton T, Perez DR. 2012. Partial and full PCR-based reverse genetics strategy for influenza viruses. PLoS One 7:e46378. http://dx.doi.org/10.1371/journal.pone.0046378.
20. de Jong JC, Smith DJ, Lapedes AS, Donatelli I, Campitelli L, Barigazzi G, Van Reeth K, Jones TC, Rimmelzwaan GF, Osterhaus AD, Fouchier RA. 2007. Antigenic and genetic evolution of swine influenza A (H3N2) viruses in Europe. J Virol 81:4315-4322. http://dx.doi.org/10.1128/JVI.02458-06.
21. Lorusso A, Vincent AL, Harland ML, Alt D, Bayles DO, Swenson SL, Gramer MR, Russell CA, Smith DJ, Lager KM, Lewis NS. 2011. Genetic and antigenic characterization of H1 influenza viruses from United States swine from 2008. J Gen Virol 92:919-930. http://dx.doi.org/10.1099/vir.0.027557-0.
22. Nfon CK, Berhane Y, Hisanaga T, Zhang S, Handel K, Kehler H, Labrecque O, Lewis NS, Vincent AL, Copps J, Alexandersen S, Pasick J. 2011. Characterization of H1N1 swine influenza viruses circulating in Canadian pigs in 2009. J Virol 85:8667-8679. http://dx.doi.org/10.1128 /JVI.00801-11.
23. Kitikoon P, Nilubol D, Erickson BJ, Janke BH, Hoover TC, Sornsen SA, Thacker EL. 2006. The immune response and maternal antibody interference to a heterologous H1N1 swine influenza virus infection following vaccination. Vet Immunol Immunopathol 112:117-128. http://dx.doi.org /10.1016/j.vetimm.2006.02.008.
24. Gauger PC, Vincent AL, Loving CL, Henningson JN, Lager KM, Janke BH, Kehrli ME, Jr, Roth JA. 2012. Kinetics of lung lesion development and pro-inflammatory cytokine response in pigs with vaccine-associated enhanced respiratory disease induced by challenge with pandemic (2009) A/H1N1 influenza virus. Vet Pathol 49:900-912. http://dx.doi.org/10.1177/0300985812439724.
25. Halbur PG, Paul PS, Frey ML, Landgraf J, Eernisse K, Meng XJ, Lum MA, Andrews JJ, Rathje JA. 1995. Comparison of the pathogenicity of two US porcine reproductive and respiratory syndrome virus isolates with that of the Lelystad virus. Vet Pathol 32:648-660. http://dx.doi.org/10.1177/030098589503200606.
26. Khurana S, Loving CL, Manischewitz J, King LR, Gauger PC, Henningson J, Vincent AL, Golding H. 2013. Vaccine-induced anti-HA2 antibodies promote virus fusion and enhance influenza virus respiratory disease. Sci Transl Med 5:200ra114. http://dx.doi.org/10.1126/scitranslmed.3006366.
27. Edgar RC. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792-1797. http://dx.doi.org/10.1093/nar/gkh340.
28. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Meintjes P, Drummond A. 2012. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647-1649. http://dx.doi.org/10.1093 /bioinformatics/bts199.
29. Stamatakis A. 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312-1313. http: //dx.doi.org/10.1093/bioinformatics/btu033.
30. Miller M, Wayne Pfeiffer, and Terri Schwartz. 2010. Creating the CIPRES Science Gateway for inference of large phylogenetic trees, p 1-8. In Proceedings of the Gateway Computing Environments Workshop, New Orleans, LA, 14 November 2010.
31. Pattengale ND, Alipour M, Bininda-Emonds OR, Moret BM, Stamatakis A. 2010. How many bootstrap replicates are necessary? J Comput Biol 17:337-354. http://dx.doi.org/10.1089/cmb.2009.0179.
32. Kitikoon P, Nelson MI, Killian ML, Anderson TK, Koster L, Culhane MR, Vincent AL. 2013. Genotype patterns of contemporary reassorted H3N2 virus in U.S. swine. J Gen Virol 94:1236-1241. http://dx.doi.org/10.1099/vir.0.051839-0.
33. Yassine HM, Al-Natour MQ, Lee CW, Saif YM. 2007. Interspecies and intraspecies transmission of triple reassortant H3N2 influenza A viruses. Virol J 4:129. http://dx.doi.org/10.1186/1743-422X-4-129.
34. Monto AS, Petrie JG, Cross RT, Johnson E, Liu M, Zhong W, Levine M, Katz JM, Ohmit SE. 2015. Antibody to influenza virus neuraminidase: an independent correlate of protection. J Infect Dis 212:1191-1199. http://dx.doi.org/10.1093/infdis/jiv195.
35. Veguilla V, Hancock K, Schiffer J, Gargiullo P, Lu X, Aranio D, Branch A, Dong L, Holiday C, Liu F, Steward-Clark E, Sun H, Tsang B, Wang D, Whaley M, Bai Y, Cronin L, Browning P, Dababneh H, Noland H, Thomas L, Foster L, Quinn CP, Soroka SD, Katz JM. 2011. Sensitivity and specificity of serologic assays for detection of human infection with 2009 pandemic H1N1 virus in U.S. populations. J Clin Microbiol 49: 2210-2215. http://dx.doi.org/10.1128/JCM.00229-11.
36. Luksza M, Lassig M. 2014. A predictive fitness model for influenza. Nature 507:57-61. http://dx.doi.org/10.1038/nature13087.
37. Neher RA, Russell CA, Shraiman BI. 11 November 2014. Predicting evolution from the shape of genealogical trees. eLife 3. http://dx.doi.org /10.7554/eLife.03568.
38. Anonymous. 2015. Recommended composition of influenza virus vaccines for use in the 2015-2016 northern hemisphere influenza season. Wkly Epidemiol Rec 90:97-108.
39. Chambers BS, Parkhouse K, Ross TM, Alby K, Hensley SE. 2015. Identification of hemagglutinin residues responsible for H3N2 antigenic drift during the 2014-2015 influenza season. Cell Rep 12:1-6. http://dx.doi.org/10.1016/j.celrep.2015.06.005.
40. Volz EM, Koelle K, Bedford T. 2013. Viral phylodynamics. PLoS Comput Biol 9:e1002947. http://dx.doi.org/10.1371/journal.pcbi.1002947.
41. Koelle K, Cobey S, Grenfell B, Pascual M. 2006. Epochal evolution shapes the phylodynamics of interpandemic influenzaA(H3N2) in humans. Science 314:1898-1903. http://dx.doi.org/10.1126/science.1132745.
42. Gulati S, Smith DF, Cummings RD, Couch RB, Griesemer SB, St George K, Webster RG, Air GM. 2013. 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 8:e66325. http://dx.doi.org/10.1371/journal.pone.0066325.
43. Hensley SE, Das SR, Bailey AL, Schmidt LM, Hickman HD, Jayaraman A, Viswanathan K, Raman R, Sasisekharan R, Bennink JR, Yewdell JW. 2009. Hemagglutinin receptor binding avidity drives influenza A virus antigenic drift. Science 326:734-736. http://dx.doi.org/10.1126/science.1178258.
44. Li Y, Bostick DL, Sullivan CB, Myers JL, Griesemer SB, Stgeorge K, Plotkin JB, Hensley SE. 2013. Single hemagglutinin mutations that alter both antigenicity and receptor binding avidity influence influenza virus antigenic clustering. J Virol 87:9904-9910. http://dx.doi.org/10.1128/JVI.01023-13.
45. Das SR, Hensley SE, David A, Schmidt L, Gibbs JS, Puigbo P, Ince WL, Bennink JR, Yewdell JW. 2011. Fitness costs limit influenza A virus hemagglutinin glycosylation as an immune evasion strategy. Proc Natl Acad Sci U S A 108:E1417-E1422. http://dx.doi.org/10.1073/pnas.1108754108.
46. Das SR, Hensley SE, Ince WL, Brooke CB, Subba A, Delboy MG, Russ G, Gibbs JS, Bennink JR, Yewdell JW. 2013. Defining influenza A virus hemagglutinin antigenic drift by sequential monoclonal antibody selection. Cell Host Microbe 13:314-323. http://dx.doi.org/10.1016/j.chom.2013.02.008.
47. Kryazhimskiy S, Dushoff J, Bazykin GA, Plotkin JB. 2011. Prevalence of epistasis in the evolution of influenza A surface proteins. PLoS Genet 7:e1001301. http://dx.doi.org/10.1371/journal.pgen.1001301.
48. Corzo CA, Culhane M, Juleen K, Stigger-Rosser E, Ducatez MF, Webby RJ, Lowe JF. 2013. Active surveillance for influenza A virus among swine, midwestern United States, 2009-2011. Emerg Infect Dis 19:954-960. http: //dx.doi.org/10.3201/eid1906.121637.
49. Kitikoon P, Gauger PC, Anderson TK, Culhane MR, Swenson S, Loving CL, Perez DR, Vincent AL. 2013. Swine influenza virus vaccine serologic cross-reactivity to contemporary US swine H3N2 and efficacy in pigs in-fected with an H3N2 similar to 2011-2012 H3N2v. Influenza Other Respir Viruses 7(Suppl 4):S32-S41.
50. Loving CL, Lager KM, Vincent AL, Brockmeier SL, Gauger PC, Anderson TK, Kitikoon P, Perez DR, Kehrli ME, Jr. 2013. Efficacy in pigs of inactivated and live attenuated influenza virus vaccines against infection and transmission of an emerging H3N2 similar to the 2011-2012 H3N2v. J Virol 87:9895-9903. http://dx.doi.org/10.1128/JVI.01038-13.
51. Anonymous. 2007. Center for Veterinary Biologics notice no. 07-17: labeling of equine influenza and swine influenza vaccines. USDA Animal and Plant Health Inspection Service, Ames, IA.
52. Rajao DS, Anderson TK, Gauger PC, Vincent AL. 2014. Pathogenesis and vaccination of influenza A virus in swine. Curr Top Microbiol Immunol 385:307-326. http://dx.doi.org/10.1007/82_2014_391.
53. Sandbulte MR, Spickler AR, Zaabel PK, Roth JA. 2015. Optimal use of vaccines for control of influenza A virus in swine. Vaccines 3:22-73. http: //dx.doi.org/10.3390/vaccines3010022.
54. Myers JL, Wetzel KS, Linderman SL, Li Y, Sullivan CB, Hensley SE. 2013. Compensatory hemagglutinin mutations alter antigenic properties of influenza viruses. J Virol 87:11168-11172. http://dx.doi.org/10.1128 /JVI.01414-13.
55. Fonville JM. 24 June 2015. The expected effect of deleterious mutations on within-host adaptation of pathogens. J Virol http://dx.doi.org/10.1128 /JVI.00832-15.
56. Neher RA, Bedford T. 26 June 2015. nextflu: real-time tracking of seasonal influenza virus evolution in humans. Bioinformatics http://dx.doi.org/10.1093/bioinformatics/btv381.