Serum IgG titres, but not avidity, correlates with neutralizing antibody response after H5N1 vaccination

Vaccine

Volumn 32, Issue 35, 2014, Pages 4550-4557

  Pedersen, Gabriel Kristian ^a   Höschler, Katja ^b   Øie Solbak, Sara Marie ^a   Bredholt, Geir ^a   Pathirana, Rishi Delan ^a   Afsar, Aram ^b   Breakwell, Lucy ^b   Nøstbakken, Jane Kristin ^a   Raae, Arnt Johan ^a   Brokstad, Karl Albert ^a   Sjursen, Haakon ^a,c   Zambon, Maria ^b   Cox, Rebecca Jane ^a,c  

^a UNIVERSITY OF BERGEN   (Norway)

^b PUBLIC HEALTH ENGLAND   (United Kingdom)

^c HAUKELAND UNIVERSITY HOSPITAL   (Norway)

Author keywords

Antibody avidity; Influenza H5N1; ISCOM; Matrix M ; Pandemic influenza; Virosomal vaccine; Virus neutralization

Indexed keywords

IMMUNOGLOBULIN G ANTIBODY; IMMUNOGLOBULIN G1 ANTIBODY; IMMUNOGLOBULIN G3 ANTIBODY; INFLUENZA VACCINE; INFLUENZA VIRUS HEMAGGLUTININ; ISCOM; NEUTRALIZING ANTIBODY; IMMUNOGLOBULIN G; IMMUNOLOGICAL ADJUVANT; VIRUS ANTIBODY;

ADULT; ANTIBODY BLOOD LEVEL; ANTIBODY SPECIFICITY; ANTIBODY TITER; ANTIGEN BINDING; ARTICLE; CONTROLLED STUDY; ELUTION; ENZYME LINKED IMMUNOSORBENT ASSAY; HUMAN; HUMAN CELL; IMMUNE RESPONSE; INFLUENZA A (H5N1); INFLUENZA VACCINATION; INFLUENZA VIRUS A H5N1; LONG TERM MEMORY; MAJOR CLINICAL STUDY; MEMORY CELL; PERIPHERAL BLOOD MONONUCLEAR CELL; PHASE 1 CLINICAL TRIAL; PRIORITY JOURNAL; SERUM; SURFACE PLASMON RESONANCE; VIRUS NEUTRALIZATION; VIRUS STRAIN; ANTIBODY AFFINITY; BLOOD; CLINICAL TRIAL; IMMUNOLOGY; INTRAMUSCULAR DRUG ADMINISTRATION; MIDDLE AGED; PROCEDURES; SERODIAGNOSIS; VACCINATION; YOUNG ADULT;

ADJUVANTS, IMMUNOLOGIC; ADULT; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; ANTIBODY AFFINITY; ENZYME-LINKED IMMUNOSORBENT ASSAY; HUMANS; IMMUNOGLOBULIN G; INFLUENZA A VIRUS, H5N1 SUBTYPE; INFLUENZA VACCINES; INJECTIONS, INTRAMUSCULAR; MIDDLE AGED; NEUTRALIZATION TESTS; SERUM; SURFACE PLASMON RESONANCE; VACCINATION; YOUNG ADULT;

EID: 84904395075     PISSN: 0264410X     EISSN: 18732518     Source Type: Journal    
DOI: 10.1016/j.vaccine.2014.06.009     Document Type: Article

References (47)

1. Simmons C.P., Bernasconi N.L., Suguitan A.L., Mills K., Ward J.M., Chau N.V., et al. Prophylactic and therapeutic efficacy of human monoclonal antibodies against H5N1 influenza. PLoS Med 2007, 4:e178.
2. Gerhard W., Mozdzanowska K., Furchner M., Washko G., Maiese K. Role of the B-cell response in recovery of mice from primary influenza virus infection. Immunol Rev 1997, 159:95-103.
3. Roman E., Miller E., Harmsen A., Wiley J., Von Andrian U.H., Huston G., et al. CD4 effector T cell subsets in the response to influenza: heterogeneity, migration, and function. J Exp Med 2002, 196:957-968.
4. Graham M.B., Braciale V.L., Braciale T.J. Influenza virus-specific CD4+ T helper type 2 T lymphocytes do not promote recovery from experimental virus infection. J Exp Med 1994, 180:1273-1282.
5. WHO Tables on the Clinical Trials of Pandemic Influenza Prototype Vaccines 2014, WHO, Geneva.
6. Salk J.E., Menke W., Francis T. A clinical, epidemiological and immunological evaluation of vaccination against epidemic influenza. Am J Hyg 1945, 42:57-93.
7. Ohmit S.E., Petrie J.G., Cross R.T., Johnson E., Monto A.S. Influenza hemagglutination-inhibition antibody titer as a correlate of vaccine-induced protection. J Infect Dis 2011, 204:1879-1885.
8. Breukels M.A., Jol-van der Zijde E., van Tol M.J., Rijkers G.T. Concentration and avidity of anti-Haemophilus influenzae type b (Hib) antibodies in serum samples obtained from patients for whom Hib vaccination failed. Clin Infect Dis 2002, 34:191-197.
9. Usinger W.R., Lucas A.H. Avidity as a determinant of the protective efficacy of human antibodies to pneumococcal capsular polysaccharides. Infect Immun 1999, 67:2366-2370.
10. Junker A.K., Tilley P. Varicella-zoster virus antibody avidity and IgG-subclass patterns in children with recurrent chickenpox. J Med Virol 1994, 43:119-124.
11. Monsalvo A.C., Batalle J.P., Lopez M.F., Krause J.C., Klemenc J., Hernandez J.Z., et al. Severe pandemic 2009 H1N1 influenza disease due to pathogenic immune complexes. Nat Med 2011, 17:195-199.
12. Brokstad K.A., Cox R.J., Major D., Wood J.M., Haaheim L.R. Cross-reaction but no avidity change of the serum antibody response after influenza vaccination. Vaccine 1995, 13:1522-1528.
13. Khurana S., Verma N., Yewdell J.W., Hilbert A.K., Castellino F., Lattanzi M., et al. MF59 adjuvant enhances diversity and affinity of antibody-mediated immune response to pandemic influenza vaccines. Sci. Transl. Med. 2011, 3:85ra48.
14. Cox R.J., Pedersen G., Madhun A.S., Svindland S., Saevik M., Breakwell L., et al. Evaluation of a virosomal H5N1 vaccine formulated with Matrix M adjuvant in a phase I clinical trial. Vaccine 2011, 29:8049-8059.
15. Pullen G.R., Fitzgerald M.G., Hosking C.S. Antibody avidity determination by ELISA using thiocyanate elution. J Immunol Methods 1986, 86:83-87.
16. Crotty S., Aubert R.D., Glidewell J., Ahmed R. Tracking human antigen-specific memory B cells: a sensitive and generalized ELISPOT system. J. Immunol. Methods 2004, 286:111-122.
17. Rowe T., Abernathy R.A., Hu-Primmer J., Thompson W.W., Lu X., Lim W., et al. Detection of antibody to avian influenza A (H5N1) virus in human serum by using a combination of serologic assays. J. Clin. Microbiol. 1999, 37:937-943.
18. Khurana S., Verma N., Talaat K.R., Karron R.A., Golding H. Immune response following H1N1pdm09 vaccination: differences in antibody repertoire and avidity in young adults and elderly populations stratified by age and gender. J Infect Dis 2012, 205:610-620.
19. Edwards M.J., Dimmock N.J. A haemagglutinin (HA1)-specific FAb neutralizes influenza A virus by inhibiting fusion activity. J Gen Virol 2001, 82:1387-1395.
20. Cao Z., Meng J., Li X., Wu R., Huang Y., He Y. The epitope and neutralization mechanism of AVFluIgG01, a broad-reactive human monoclonal antibody against H5N1 influenza virus. PLoS ONE 2012, 7:e38126.
21. Katsamba P.S., Navratilova I., Calderon-Cacia M., Fan L., Thornton K., Zhu M., et al. Kinetic analysis of a high-affinity antibody/antigen interaction performed by multiple Biacore users. Anal Biochem 2006, 352:208-221.
22. Onell A., Andersson K. Kinetic determinations of molecular interactions using Biacore - minimum data requirements for efficient experimental design. J Mol Recognit 2005, 18:307-317.
23. de Jong M.D., Simmons C.P., Thanh T.T., Hien V.M., Smith G.J., Chau T.N., et al. Fatal outcome of human influenza A (H5N1) is associated with high viral load and hypercytokinemia. Nat Med 2006, 12:1203-1207.
24. Stephenson I., Wood J.M., Nicholson K.G., Zambon M.C. Sialic acid receptor specificity on erythrocytes affects detection of antibody to avian influenza haemagglutinin. J Med Virol 2003, 70:391-398.
25. CHMP Guideline on Dossier Structure and Content for Pandemic Influenza Vaccine Marketing Authorisation Application 2008, CHMP, London.
26. Jelley-Gibbs D.M., Brown D.M., Dibble J.P., Haynes L., Eaton S.M., Swain S.L. Unexpected prolonged presentation of influenza antigens promotes CD4 T cell memory generation. J Exp Med 2005, 202:697-706.
27. Zammit D.J., Turner D.L., Klonowski K.D., Lefrancois L., Cauley L.S. Residual antigen presentation after influenza virus infection affects CD8 T cell activation and migration. Immunity 2006, 24:439-449.
28. Bachmann M.F., Odermatt B., Hengartner H., Zinkernagel R.M. Induction of long-lived germinal centers associated with persisting antigen after viral infection. J Exp Med 1996, 183:2259-2269.
29. Pedersen G.K., Madhun A.S., Breakwell L., Hoschler K., Sjursen H., Pathirana R.D., et al. T-helper 1 cells elicited by H5N1 vaccination predict seroprotection. J Infect Dis 2012, 206:158-166.
30. Verma N., Dimitrova M., Carter D.M., Crevar C.J., Ross T.M., Golding H., et al. Influenza virus H1N1pdm09 infections in the young and old: evidence of greater antibody diversity and affinity for the hemagglutinin globular head domain (HA1 Domain) in the elderly than in young adults and children. J Virol 2012, 86:5515-5522.
31. Wu H., Pfarr D.S., Tang Y., An L.L., Patel N.K., Watkins J.D., et al. Ultra-potent antibodies against respiratory syncytial virus: effects of binding kinetics and binding valence on viral neutralization. J Mol Biol 2005, 350:126-144.
32. Zhu Z., Dimitrov A.S., Bossart K.N., Crameri G., Bishop K.A., Choudhry V., et al. Potent neutralization of Hendra and Nipah viruses by human monoclonal antibodies. J Virol 2006, 80:891-899.
33. Klein J.S., Gnanapragasam P.N., Galimidi R.P., Foglesong C.P., West A.P., Bjorkman P.J. Examination of the contributions of size and avidity to the neutralization mechanisms of the anti-HIV antibodies b12 and 4E10. Proc Natl Acad Sci U S A 2009, 106:7385-7390.
34. Brown L.E., Murray J.M., White D.O., Jackson D.C. An analysis of the properties of monoclonal antibodies directed to epitopes on influenza virus hemagglutinin. Arch Virol 1990, 114:1-26.
35. Schofield D.J., Stephenson J.R., Dimmock N.J. High and low efficiency neutralization epitopes on the haemagglutinin of type A influenza virus. J Gen Virol 1997, 78(Pt. 10):2441-2446.
36. Hartshorn K.L., Reid K.B., White M.R., Jensenius J.C., Morris S.M., Tauber A.I., et al. Neutrophil deactivation by influenza A viruses: mechanisms of protection after viral opsonization with collectins and hemagglutination-inhibiting antibodies. Blood 1996, 87:3450-3461.
37. Kopf M., Abel B., Gallimore A., Carroll M., Bachmann M.F. Complement component C3 promotes T-cell priming and lung migration to control acute influenza virus infection. Nat Med 2002, 8:373-378.
38. Powers D.C. Effect of age on serum immunoglobulin G subclass antibody responses to inactivated influenza virus vaccine. J Med Virol 1994, 43:57-61.
39. El-Madhun A.S., Cox R.J., Haaheim L.R. The effect of age and natural priming on the IgG and IgA subclass responses after parenteral influenza vaccination. J Infect Dis 1999, 180:1356-1360.
40. Hamilton R.G. Human IgG subclass measurements in the clinical laboratory. Clin Chem 1987, 33:1707-1725.
41. Mathiesen T., Persson M.A., Sundqvist V.A., Wahren B. Neutralization capacity and antibody dependent cell-mediated cytotoxicity of separated IgG subclasses 1, 3 and 4 against herpes simplex virus. Clin Exp Immunol 1988, 72:211-215.
42. Rodrigo W.W., Block O.K., Lane C., Sukupolvi-Petty S., Goncalvez A.P., Johnson S., et al. Dengue virus neutralization is modulated by IgG antibody subclass and Fcgamma receptor subtype. Virology 2009, 394:175-182.
43. Hofmeister Y., Planitzer C.B., Farcet M.R., Teschner W., Butterweck H.A., Weber A., et al. Human IgG subclasses: in vitro neutralization of and in vivo protection against West Nile virus. J Virol 2011, 85:1896-1899.
44. Frolich D., Giesecke C., Mei H.E., Reiter K., Daridon C., Lipsky P.E., et al. Secondary immunization generates clonally related antigen-specific plasma cells and memory B cells. J Immunol 2010, 185:3103-3110.
45. Purtha W.E., Tedder T.F., Johnson S., Bhattacharya D., Diamond M.S. Memory B cells, but not long-lived plasma cells, possess antigen specificities for viral escape mutants. J Exp Med 2011, 208:2599-2606.
46. Romero-Steiner S., Holder P.F., Gomez de Leon P., Spear W., Hennessy T.W., Carlone G.M. Avidity determinations for Haemophilus influenzae Type b anti-polyribosylribitol phosphate antibodies. Clin Diagn Lab Immunol 2005, 12:1029-1035.
47. Lofgren J.A., Dhandapani S., Pennucci J.J., Abbott C.M., Mytych D.T., Kaliyaperumal A., et al. Comparing ELISA and surface plasmon resonance for assessing clinical immunogenicity of panitumumab. J Immunol 2007, 178:7467-7472.