IgM, IgG, and IgA antibody responses to influenza A(H1N1)pdm09 hemagglutinin in infected persons during the first wave of the 2009 pandemic in the United States

Clinical and Vaccine Immunology

Volumn 21, Issue 8, 2014, Pages 1054-1060

  Li, Zhu Nan ^a   Lin, Seh Ching ^b   Carney, Paul J ^a   Li, Ji ^a   Liu, Feng ^a   Lu, Xiuhua ^a   Liu, Merry ^b   Stevens, James ^a   Levine, Min ^a   Katz, Jacqueline M ^a   Hancock, Kathy ^a  

^a NATIONAL CENTER FOR IMMUNIZATION AND RESPIRATORY DISEASES   (United States)

^b NATIONAL CENTER FOR EMERGING AND ZOONOTIC INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HEMAGGLUTININ H1; HEMAGGLUTININ H13; HEMAGGLUTININ H3; HEMAGGLUTININ H5; IMMUNOGLOBULIN A ANTIBODY; IMMUNOGLOBULIN G ANTIBODY; IMMUNOGLOBULIN M ANTIBODY; INFLUENZA VIRUS HEMAGGLUTININ; UNCLASSIFIED DRUG; VIRUS HEMAGGLUTININ; H1N1 VIRUS HEMAGGLUTININ; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; VIRUS ANTIBODY;

2009 H1N1 INFLUENZA; AGE DISTRIBUTION; ANTIBODY DETECTION; ANTIBODY RESPONSE; ARTICLE; BLOOD LEVEL; BLOOD SAMPLING; CONTROLLED STUDY; CROSS REACTION; DISEASE ASSOCIATION; ENZYME LINKED IMMUNOSORBENT ASSAY; INFLUENZA A (H1N1); INFLUENZA VIRUS A H1N1; NONHUMAN; NUCLEOTIDE SEQUENCE; OUTCOME ASSESSMENT; PRIORITY JOURNAL; RNA SEQUENCE; SEASONAL INFLUENZA; SENSITIVITY ANALYSIS; SENSITIVITY AND SPECIFICITY; SEQUENCE ANALYSIS; UNITED STATES; VIRUS IDENTIFICATION; VIRUS TITRATION; ADOLESCENT; ADULT; AGED; BLOOD; CHILD; FEMALE; HEMAGGLUTINATION INHIBITION TEST; HUMAN; IMMUNOLOGY; INFLUENZA; INFLUENZA A VIRUS (H1N1); LABORATORY DIAGNOSIS; MALE; MIDDLE AGED; PANDEMIC; PRESCHOOL CHILD; VERY ELDERLY; VIROLOGY; YOUNG ADULT;

ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; ANTIBODIES, VIRAL; CHILD; CHILD, PRESCHOOL; CROSS REACTIONS; ENZYME-LINKED IMMUNOSORBENT ASSAY; FALSE POSITIVE REACTIONS; FEMALE; HEMAGGLUTINATION INHIBITION TESTS; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; HUMANS; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA, HUMAN; MALE; MIDDLE AGED; PANDEMICS; UNITED STATES; YOUNG ADULT;

EID: 84906687898     PISSN: 15566811     EISSN: 1556679X     Source Type: Journal    
DOI: 10.1128/CVI.00129-14     Document Type: Article

References (44)

1. World Health Organization. 2009. World now at the start of 2009 influenza pandemic: statement to the press by WHO Director-General Dr Margaret Chan. World Health Organization, Geneva, Switzerland. http://www.who.int/mediacentre/ news/statements/2009/h1n1-pandemic-phase6-20090611/en/index.html.
2. World Health Organization. 2010. Global alert and response (GAR). Pandemic (H1N1) 2009 - update 2012. World Health Organization, Geneva, Switzerland. http://www.who.int/csr/don/2010-08-06/en/.
3. Garten RJ, Davis CT, Russell CA, Shu B, Lindstrom S, Balish A, Sessions WM, Xu X, Skepner E, Deyde V, Okomo-Adhiambo M, Gubareva L, Barnes J, Smith CB, Emery SL, Hillman MJ, Rivailler P, Smagala J, de Graaf M, Burke DF, Fouchier RA, Pappas C, Alpuche-Aranda CM, Lopez-Gatell H, Olivera H, Lopez I, Myers CA, Faix D, Blair PJ, Yu C, Keene KM, Dotson PD, Jr, Boxrud D, Sambol AR, Abid SH, St George K, Bannerman T, Moore AL, Stringer DJ, Blevins P, Demmler-Harrison GJ, Ginsberg M, Kriner P, Waterman S, Smole S, Guevara HF, Belongia EA, Clark PA, Beatrice ST, Donis R, Katz J, Finelli L, Bridges CB, Shaw M, Jernigan DB, Uyeki TM, Smith DJ, Klimov AI, Cox NJ. 2009. Antigenic and genetic characteristics of swineorigin 2009 A(H1N1) influenza viruses circulating in humans. Science 325:197-201. http://dx.doi.org/10.1126/science.1176225.
4. Burlington DB, Clements ML, Meiklejohn G, Phelan M, Murphy BR. 1983. Hemagglutinin-specific antibody responses in immunoglobulin G, A, and M isotypes as measured by enzyme-linked immunosorbent assay after primary or secondary infection of humans with influenza A virus. Infect. Immun. 41:540-545. (Pubitemid 13075234)
5. Karron RA, Talaat K, Luke C, Callahan K, Thumar B, Dilorenzo S, McAuliffe J, Schappell E, Suguitan A, Mills K, Chen G, Lamirande E, Coelingh K, Jin H, Murphy BR, Kemble G, Subbarao K. 2009. Evaluation of two live attenuated cold-adapted H5N1 influenza virus vaccines in healthy adults. Vaccine 27:4953-4960. http://dx.doi.org/10.1016/j.vaccine.2009.05.099.
6. Talaat KR, Karron RA, Callahan KA, Luke CJ, DiLorenzo SC, Chen GL, Lamirande EW, Jin H, Coelingh KL, Murphy BR, Kemble G, Subbarao K. 2009. A live attenuated H7N3 influenza virus vaccine is well tolerated and immunogenic in a phase I trial in healthy adults. Vaccine 27:3744-3753. http://dx.doi.org/10. 1016/j.vaccine.2009.03.082.
7. Alvarez MM, Lopez-Pacheco F, Aguilar-Yanez JM, Portillo-Lara R, Mendoza-Ochoa GI, Garcia-Echauri S, Freiden P, Schultz-Cherry S, Zertuche-Guerra MI, Bulnes-Abundis D, Salgado-Gallegos J, Elizondo-Montemayor L, Hernandez-Torre M. 2010. Specific recognition of influenza A/H1N1/2009 antibodies in human serum: a simple virus-free ELISA method. PLoS One 5:e10176. http://dx.doi.org/10.1371/journal.pone.0010176.
8. Arankalle VA, Virkar RG, Tandale BV, Ingle NB. 2010. Utility of pandemic H1N1 2009 influenza virus recombinant hemagglutinin protein-based enzyme- linked immunosorbent assay for serosurveillance. Clin. Vaccine Immunol. 17:1481-1483. http://dx.doi.org/10.1128/CVI.00223-10.
9. Murphy BR, Phelan MA, Nelson DL, Yarchoan R, Tierney EL, Alling DW, Chanock RM. 1981. Hemagglutinin-specific enzyme-linked immunosorbent assay for antibodies to influenza A and B viruses. J. Clin. Microbiol. 13:554-560. (Pubitemid 11153770)
10. Murphy BR, Nelson DL, Wright PF, Tierney EL, Phelan MA, Chanock RM. 1982. Secretory and systemic immunological response in children infected with live attenuated influenza A virus vaccines. Infect. Immun. 36:1102-1108. (Pubitemid 12124828)
11. Stevens J, Corper AL, Basler CF, Taubenberger JK, Palese P, Wilson IA. 2004. Structure of the uncleaved human H1 hemagglutinin from the extinct 1918 influenza virus. Science 303:1866-1870. http://dx.doi.org/10.1126/science. 1093373. (Pubitemid 38374878)
12. Yang H, Carney P, Stevens J. 2010. Structure and receptor binding properties of a pandemic H1N1 virus hemagglutinin. PLoS Curr. 2:RRN1152.
13. Yang H, Carney PJ, Chang JC, Villanueva JM, Stevens J. 2013. Structural analysis of the hemagglutinin from the recent 2013 H7N9 influenza virus. J. Virol. 87:12433-12446. http://dx.doi.org/10.1128/JVI.01854-13.
14. Yang H, Chang JC, Guo Z, Carney PJ, Shore DA, Donis RO, Cox NJ, Villanueva JM, Klimov AI, Stevens J. 2014. Structural stability of influenza A(H1N1)pdm09 virus hemagglutinins. J. Virol. 88:4828-4838. http://dx.doi.org/10. 1128/JVI.02278-13.
15. Centers for Disease Control and Prevention. 2014. National health and nutrition examination survey. Centers for Disease Control and Prevention, Atlanta, GA. http://wwwn.cdc.gov/nchs/nhanes/search/nhanes07-08.aspx.
16. 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.
17. Wood JM, Major D, Heath A, Newman RW, Hoschler K, Stephenson I, Clark T, Katz JM, Zambon MC. 2012. Reproducibility of serology assays for pandemic influenza H1N1: collaborative study to evaluate a candidate WHO International Standard. Vaccine 30:210-217. http://dx.doi.org/10.1016/j.vaccine.2011.11.019.
18. Kendal AP, Pereira MS, Skehel JJ. 1982. Concepts and procedures for laboratory-based influenza surveillance. Centers for Disease Control and Prevention, Atlanta, GA.
19. WHO Global Influenza Surveillance Network. 2011. Manual for the laboratory diagnosis and virological surveillance of influenza.WHO Press, Geneva, Switzerland.
20. Laurie KL, Huston P, Riley S, Katz JM, Willison DJ, Tam JS, Mounts AW, Hoschler K, Miller E, Vandemaele K, Broberg E, Van Kerkhove MD, Nicoll A. 2013. Influenza serological studies to inform public health action: best practices to optimise timing, quality and reporting. Influenza Other Respir. Viruses 7:211-224. http://dx.doi.org/10.1111/j.1750-2659.2012.0370a.x.
21. Erdman DD, Anderson LJ, Adams DR, Stewart JA, Markowitz LE, Bellini WJ. 1991. Evaluation of monoclonal antibody-based capture enzyme immunoassays for detection of specific antibodies to measles virus. J. Clin. Microbiol. 29:1466-1471.
22. Zambon M. 1998. Laboratory diagnosis of influenza. Blackwell Science, Oxford, United Kingdom.
23. Qiu C, Tian D, Wan Y, Zhang W, Zhu Z, Ye R, Song Z, Zhou M, Yuan S, Shi B, Wu M, Liu Y, Gu S, Wei J, Zhou Z, Zhang X, Zhang Z, Hu Y, Yuan Z, Xu J. 2011. Early adaptive humoral immune responses and virus clearance in humans recently infected with pandemic 2009 H1N1 influenza virus. PLoS One 6:e22603. http://dx.doi.org/10.1371/journal.pone.0022603.
24. Salonen EM, Vaheri A, Suni J, Wager O. 1980. Rheumatoid factor in acute viral infections: interference with determination of IgM, IgG, and IgA antibodies in an enzyme immunoassay. J. Infect. Dis. 142:250-255. http://dx.doi.org/10.1093/infdis/142.2.250. (Pubitemid 10004079)
25. Xu R, Ekiert DC, Krause JC, Hai R, Crowe JE, Jr, Wilson IA. 2010. Structural basis of preexisting immunity to the 2009 H1N1 pandemic influenza virus. Science 328:357-360. http://dx.doi.org/10.1126/science.1186430.
26. Hancock K, Veguilla V, Lu X, Zhong W, Butler EN, Sun H, Liu F, Dong L, DeVos JR, Gargiullo PM, Brammer TL, Cox NJ, Tumpey TM, Katz JM. 2009. Cross-reactive antibody responses to the 2009 pandemic H1N1 influenza virus. N. Engl. J. Med. 361:1945-1952. http://dx.doi.org/10.1056/NEJMoa0906453.
27. Reed C, Katz JM, Hancock K, Balish A, Fry AM, H1N1 Serosurvey Working Group. 2012. Prevalence of seropositivity to pandemic influenza A/H1N1 virus in the United States following the 2009 pandemic. PLoS One 7:e48187. http://dx.doi.org/10.1371/journal.pone.0048187.
28. Zhao R, Cui S, Guo L, Wu C, Gonzalez R, Paranhos-Baccala G, Vernet G, Wang J, Hung T. 2011. Identification of a highly conserved H1 sub-type- specific epitope with diagnostic potential in the hemagglutinin protein of influenza a virus. PLoS One 6:e23374. http://dx.doi.org/10.1371/journal.pone.0023374.
29. Khurana S, Chearwae W, Castellino F, Manischewitz J, King LR, Honorkiewicz A, Rock MT, Edwards KM, Del Giudice G, Rappuoli R, Golding H. 2010. Vaccines with MF59 adjuvant expand the antibody repertoire to target protective sites of pandemic avian H5N1 influenza virus. Sci. Transl. Med. 2:15ra15. http://dx.doi.org/10.1126/scitranslmed.3000624.
30. Nobusawa E, Aoyama T, Kato H, Suzuki Y, Tateno Y, Nakajima K. 1991. Comparison of complete amino acid sequences and receptorbinding properties among 13 serotypes of hemagglutinins of influenza A viruses. Virology 182: 475-485. http://dx.doi.org/10.1016/0042-6822(91)90588-3.
31. Krystal M, Elliott RM, Benz EW, Jr, Young JF, Palese P. 1982. Evolution of influenza A and B viruses: conservation of structural features in the hemagglutinin genes. Proc. Natl. Acad. Sci. U. S. A. 79:4800-4804. http://dx.doi.org/10.1073/pnas.79.15.4800.
32. 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. http://dx.doi.org/10.1016/0092-8674(82)90135-0. (Pubitemid 13178866)
33. Wilson IA, Skehel JJ, Wiley DC. 1981. Structure of the haemagglutinin membrane glycoprotein of influenza virus at 3 A resolution. Nature 289:366-373. http://dx.doi.org/10.1038/289366a0.
34. Tsuchiya E, Sugawara K, Hongo S, Matsuzaki Y, Muraki Y, Li ZN, Nakamura K. 2001. Antigenic structure of the haemagglutinin of human influenza A/H2N2 virus. J. Gen. Virol. 82:2475-2484. (Pubitemid 32936780)
35. Wiley DC, Skehel JJ. 1987. The structure and function of the hemagglutinin membrane glycoprotein of influenza virus. Annu. Rev. Biochem. 56:365-394. http://dx.doi.org/10.1146/annurev.bi.56.070187.002053.
36. Sui J, Hwang WC, Perez S, Wei G, Aird D, Chen LM, Santelli E, Stec B, Cadwell G, Ali M, Wan H, Murakami A, Yammanuru A, Han T, Cox NJ, Bankston LA, Donis RO, Liddington RC, Marasco WA. 2009. Structural and functional bases for broad-spectrum neutralization of avian and human influenza A viruses. Nat. Struct. Mol. Biol. 16:265-273. http://dx.doi.org/10.1038/nsmb.1566.
37. Ekiert DC, Bhabha G, Elsliger MA, Friesen RH, Jongeneelen M, Throsby M, Goudsmit J, Wilson IA. 2009. Antibody recognition of a highly conserved influenza virus epitope. Science 324:246-251. http://dx.doi.org/10.1126/science. 1171491.
38. Ekiert DC, Friesen RH, Bhabha G, Kwaks T, Jongeneelen M, Yu W, Ophorst C, Cox F, Korse HJ, Brandenburg B, Vogels R, Brakenhoff JP, Kompier R, Koldijk MH, Cornelissen LA, Poon LL, Peiris M, Koudstaal W, Wilson IA, Goudsmit J. 2011. A highly conserved neutralizing epitope on group 2 influenza A viruses. Science 333:843-850. http://dx.doi.org/10.1126/science.1204839.
39. Corti D, Voss J, Gamblin SJ, Codoni G, Macagno A, Jarrossay D, Vachieri SG, Pinna D, Minola A, Vanzetta F, Silacci C, Fernandez-Rodriguez BM, Agatic G, Bianchi S, Giacchetto-Sasselli I, Calder L, Sallusto F, Collins P, Haire LF, Temperton N, Langedijk JP, Skehel JJ, Lanzavecchia A. 2011. A neutralizing antibody selected from plasma cells that binds to group 1 and group 2 influenza A hemagglutinins. Science 333:850-856. http://dx.doi.org/10.1126/science. 1205669.
40. Okuno Y, Isegawa Y, Sasao F, Ueda S. 1993. A common neutralizing epitope conserved between the hemagglutinins of influenza A virus H1 and H2 strains. J. Virol. 67:2552-2558. (Pubitemid 23118850)
41. Koopmans M, de Bruin E, Godeke GJ, Friesema I, van Gageldonk R, Schipper M, Meijer A, van Binnendijk R, Rimmelzwaan GF, de Jong MD, Buisman A, van Beek J, van de Vijver D, Reimerink J. 2012. Profiling of humoral immune responses to influenza viruses by using protein microarray. Clin. Microbiol. Infect. 18:797-807. http://dx.doi.org/10.1111/j.1469-0691.2011.03701.x.
42. Burlington DB, Wright PF, van Wyke KL, Phelan MA, Mayner RE, Murphy BR. 1985. Development of subtype-specific and heterosubtypic antibodies to the influenza A virus hemagglutinin after primary infection in children. J. Clin. Microbiol. 21:847-849. (Pubitemid 15093154)
43. Stelzer-Braid S, Wong B, Robertson P, Lynch GW, Laurie K, Shaw R, Barr I, Selleck PW, Baleriola C, Escott R, Katsoulotos G, Rawlinson WD. 2008. A commercial ELISA detects high levels of human H5 antibody but cross-reacts with influenza A antibodies. J. Clin. Virol. 43:241-243. http://dx.doi.org/10.1016/j. jcv.2008.06.012.
44. Francis T. 1960. On the doctrine of original antigenic sin. Proc. Am. Philos. Soc. 104:572-578.