Surface plasmon resonance measurements of plasma antibody avidity during primary and secondary responses to anthrax protective antigen

Journal of Immunological Methods

Volumn 404, Issue 1, 2014, Pages 1-12

  Lynch, Heather E ^a   Stewart, Shelley M ^a   Kepler, Thomas B ^b   Sempowski, Gregory D ^a   Alam, S Munir ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Antibody avidity; Germinal centers; Protective antigen (PA); Surface plasmon resonance (SPR)

Indexed keywords

ALUMINUM POTASSIUM SULFATE; ANTIBODY; CD45 ANTIGEN; RECOMBINANT ANTHRAX PROTECTIVE ANTIGEN; RECOMBINANT ANTIGEN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANTHRAX; ANTIBODY BLOOD LEVEL; ANTIBODY PRODUCTION; ANTIBODY RESPONSE; ANTIGEN BINDING; ANTIGEN SPECIFICITY; ARTICLE; B LYMPHOCYTE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; FEMALE; GERMINAL CENTER; HISTOLOGY; HUMORAL IMMUNITY; IMMUNE RESPONSE; IMMUNIZATION; LYMPH NODE; MOUSE; NONHUMAN; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; SURFACE PLASMON RESONANCE; TREATMENT RESPONSE;

MUS;

ANTIBODY AVIDITY; GERMINAL CENTERS; PROTECTIVE ANTIGEN (PA); SURFACE PLASMON RESONANCE (SPR);

ADJUVANTS, IMMUNOLOGIC; ALUM COMPOUNDS; ANIMALS; ANTHRAX; ANTHRAX VACCINES; ANTIBODIES, BACTERIAL; ANTIBODIES, NEUTRALIZING; ANTIBODY AFFINITY; ANTIBODY SPECIFICITY; ANTIGENS, BACTERIAL; BACILLUS ANTHRACIS; BACTERIAL TOXINS; FEMALE; GERMINAL CENTER; IMMUNITY, HUMORAL; IMMUNIZATION, SECONDARY; MICE; MICE, INBRED C57BL; SURFACE PLASMON RESONANCE;

EID: 84896734531     PISSN: 00221759     EISSN: 18727905     Source Type: Journal    
DOI: 10.1016/j.jim.2013.11.026     Document Type: Article

References (47)

1. Alam S.M., McAdams M., Boren D., Rak M., Scearce R.M., Gao F., Camacho Z.T., Gewirth D., Kelsoe G., Chen P., Haynes B.F. The role of antibody polyspecificity and lipid reactivity in binding of broadly neutralizing anti-HIV-1 envelope human monoclonal antibodies 2F5 and 4E10 to glycoprotein 41 membrane proximal envelope epitopes. J. Immunol. 2007, 178:4424.
2. Alam S.M., Morelli M., Dennison S.M., Liao H.X., Zhang R., Xia S.M., Rits-Volloch S., Sun L., Harrison S.C., Haynes B.F., Chen B. Role of HIV membrane in neutralization by two broadly neutralizing antibodies. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:20234.
3. Alam S.M., Liao H.X., Tomaras G.D., Bonsignori M., Tsao C.Y., Hwang K.K., Chen H., Lloyd K.E., Bowman C., Sutherland L., Jeffries T.L., Kozink D.M., Stewart S., Anasti K., Jaeger F.H., Parks R., Yates N.L., Overman R.G., Sinangil F., Berman P.W., Pitisuttithum P., Kaewkungwal J., Nitayaphan S., Karasavva N., Rerks-Ngarm S., Kim J.H., Michael N.L., Zolla-Pazner S., Santra S., Letvin N.L., Harrison S.C., Haynes B.F. Antigenicity and immunogenicity of RV144 vaccine AIDSVAX clade E envelope immunogen is enhanced by a gp120 N-terminal deletion. J. Virol. 2013, 87:1554.
4. Allen C.D., Okada T., Cyster J.G. Germinal-center organization and cellular dynamics. Immunity 2007, 27:190.
5. Allen C.D., Okada T., Tang H.L., Cyster J.G. Imaging of germinal center selection events during affinity maturation. Science 2007, 315:528.
6. Almanzar G., Ottensmeier B., Liese J., Prelog M. Assessment of IgG avidity against pertussis toxin and filamentous hemagglutinin via an adapted enzyme-linked immunosorbent assay (ELISA) using ammonium thiocyanate. J. Immunol. Methods 2013, 387:36.
7. Barkoff A.M., Grondahl-Yli-Hannuksela K., Vuononvirta J., Mertsola J., Kallonen T., He Q. Differences in avidity of IgG antibodies to pertussis toxin after acellular pertussis booster vaccination and natural infection. Vaccine 2012, 30:6897.
8. Bonsignori M., Alam S.M., Liao H.X., Verkoczy L., Tomaras G.D., Haynes B.F., Moody M.A. HIV-1 antibodies from infection and vaccination: insights for guiding vaccine design. Trends Microbiol. 2012, 20:532.
9. Canziani G.A., Klakamp S., Myszka D.G. Kinetic screening of antibodies from crude hybridoma samples using Biacore. Anal. Biochem. 2004, 325:301.
10. Cyster J.G., Schwab S.R. Sphingosine-1-phosphate and lymphocyte egress from lymphoid organs. Annu. Rev. Immunol. 2012, 30:69.
11. Dal Porto J.M., Haberman A.M., Kelsoe G., Shlomchik M.J. Very low affinity B cells form germinal centers, become memory B cells, and participate in secondary immune responses when higher affinity competition is reduced. J. Exp. Med. 2002, 195:1215.
12. Eisen H.N., Siskind G.W. Variations in affinities of antibodies during the immune response. Biochemistry 1964, 3:996.
13. Flynn B.J., Kastenmuller K., Willie-Reece U., Tomaras G.D., Alam S.M., Lindsay R.W., Salazar A.M., Perdiguero B., Gomez C.E., Wagner R., Esteban M., Park C.G., Trumpfheller C., Keler T., Panteleo G., Steinman R.M., Seder R. Immunization with HIV Gag targeted to dendritic cells followed by recombinant New York Vaccinia virus induces ribust T-cell immunity in nonhuman primates. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:7131.
14. Fried A.J., Altrich M.L., Liu H., Halsey J.F., Bonilla F.A. Correlation of pneumococcal antibody concentration and avidity with patient clinical and immunologic characteristics. J. Clin. Immunol. 2013, 33(4):847-856.
15. Friedlander A.M., Welkos S.L., Ivins B.E. Anthrax vaccines. Curr. Top. Microbiol. Immunol. 2002, 271:33.
16. Han S., Zheng B., Schatz D.G., Spanopoulou E., Kelsoe G. Neoteny in lymphocytes: Rag1 and Rag2 expression in germinal center B cells. Science 1996, 274:2094.
17. Haynes B.F., Gilbert P.B., McElrath M.J., Zolla-Pazner S., Tomaras G.D., Alam S.M., Evans D.T., Montefiori D.C., Karnasuta C., Sutthent R., Liao H.X., DeVico A.L., Lewis G.K., Williams C., Pinter A., Fong Y., Janes H., DeCamp A., Huang Y., Rao M., Billings E., Karasavvas N., Robb M.L., Ngauy V., de Souza M.S., Paris R., Ferrari G., Bailer R.T., Soderberg K.A., Andrews C., Berman P.W., Frahm N., De Rosa S.C., Alpert M.D., Yates N.L., Shen X., Koup R.A., Pitisuttithum P., Kaewkungwal J., Nitayaphan S., Rerks-Ngarm S., Michael N.L., Kim J.H. Immune-correlates analysis of an HIV-1 vaccine efficacy trial. N. Engl. J. Med. 2012, 366:1275.
18. Jacob J., Kelsoe G. In situ studies of the primary immune response to (4-hydroxy-3-nitrophenyl)acetyl. II. A common clonal origin for periarteriolar lymphoid sheath-associated foci and germinal centers. J. Exp. Med. 1992, 176:679.
19. Karlsson R., Michaelsson A., Mattsson L. Kinetic analysis of monoclonal antibody-antigen interactions with a new biosensor based analytical system. J. Immunol. Methods 1991, 145:229.
20. Kasturi S.P., Skountzou I., Albrecht R.A., Koutsonanos D., Hua T., Nakaya H.I., Ravindran R., Stewart S., Alam M., Kwissa M., Villinger F., Murthy N., Steel J., Jacob J., Hogan R.J., Garcia-Sastre A., Compans R., Pulendran B. Programming the magnitude and persistence of antibody responses with innate immunity. Nature 2011, 470:543.
21. Kelsoe G. Life and death in germinal centers (redux). Immunity 1996, 4:107.
22. Klein U., Dalla-Favera R. Germinal centres: role in B-cell physiology and malignancy. Nat. Rev. Immunol. 2008, 8:22.
23. Kneitz R.H., Schubert J., Tollmann F., Zens W., Hedman K., Weissbrich B. A new method for determination of varicella-zoster virus immunoglobulin G avidity in serum and cerebrospinal fluid. BMC Infect. Dis. 2004, 4:33.
24. Kraal G., Hardy R.R., Gallatin W.M., Weissman I.L., Butcher E.C. Antigen-induced changes in B cell subsets in lymph nodes: analysis by dual fluorescence flow cytofluorometry. Eur. J. Immunol. 1986, 16:829.
25. Kuppers R., Zhao M., Hansmann M.L., Rajewsky K. Tracing B cell development in human germinal centres by molecular analysis of single cells picked from histological sections. EMBO J. 1993, 12:4955.
26. Leonard P., Safsten P., Hearty S., McDonnell B., Finlay W., O'Kennedy R. High throughput ranking of recombinant avian scFv antibody fragments from crude lysates using the Biacore A100. J. Immunol. Methods 2007, 323:172.
27. Liu Y.J., Cairns J.A., Holder M.J., Abbot S.D., Jansen K.U., Bonnefoy J.Y., Gordon J., MacLennan I.C. Recombinant 25-kDa CD23 and interleukin 1 alpha promote the survival of germinal center B cells: evidence for bifurcation in the development of centrocytes rescued from apoptosis. Eur. J. Immunol. 1991, 21:1107.
28. Lullau E., Heyse S., Vogel H., Marison I., vonStockar U., Kraehenbuhl J.P., Corthesy B. Antigen binding properties of purified immunoglobulin A and reconstituted secretory immunoglobulin A antibodies. J. Biol. Chem. 1996, 271:16300.
29. MacLennan I.C. Germinal centers. Annu. Rev. Immunol. 1994, 12:117.
30. Marrack P., McKee A.S., Munks M.W. Towards an understanding of the adjuvant action of aluminium. Nat. Rev. Immunol. 2009, 9:287.
31. McHeyzer-Williams L.J., McHeyzer-Williams M.G. Antigen-specific memory B cell development. Annu. Rev. Immunol. 2005, 23:487.
32. Mouquet H., Warncke M., Scheid J.F., Seaman M.S., Nussenzweig M.C. Enhanced HIV-1 neutralization by antibody heteroligation. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:875.
33. Naito Y., Takematsu H., Koyama S., Miyake S., Yamamoto H., Fujinawa R., Sugai M., Okuno Y., Tsujimoto G., Yamaji T., Hashimoto Y., Itohara S., Kawasaki T., Suzuki A., Kozutsumi Y. Germinal center marker GL7 probes activation-dependent repression of N-glycolylneuraminic acid, a sialic acid species involved in the negative modulation of B-cell activation. Mol. Cell. Biol. 2007, 27:3008.
34. Nieuwenhuis P., Opstelten D. Functional anatomy of germinal centers. Am. J. Anat. 1984, 170:421.
35. Pasare C., Medzhitov R. Control of B-cell responses by Toll-like receptors. Nature 2005, 438:364.
36. Pittman P.R., Gibbs P.H., Cannon T.L., Friedlander A.M. Anthrax vaccine: short-term safety experience in humans. Vaccine 2001, 20:972.
37. Prelog M., Almanzar G., Rieber N., Ottensmeier B., Zlamy M., Liese J. Differences of IgG antibody avidity after an acellular pertussis (aP) booster in adolescents after a whole cell (wcP) or aP primary vaccination. Vaccine 2013, 31:387.
38. Pulendran B. Modulating vaccine responses with dendritic cells and Toll-like receptors. Immunol. Rev. 2004, 199:227.
39. Quinn C.P., Sabourin C.L., Niemuth N.A., Li H., Semenova V.A., Rudge T.L., Mayfield H.J., Schiffer J., Mittler R.S., Ibegbu C.C., Wrammert J., Ahmed R., Brys A.M., Hunt R.E., Levesque D., Estep J.E., Barnewall R.E., Robinson D.M., Plikaytis B.D., Marano N., Group A.L.W. A three-dose intramuscular injection schedule of anthrax vaccine adsorbed generates sustained humoral and cellular immune responses to protective antigen and provides long-term protection against inhalation anthrax in rhesus macaques. Clin. Vaccine Immunol. 2012, CVI 19:1730.
40. Safsten P., Klakamp S.L., Drake A.W., Karlsson R., Myszka D.G. Screening antibody-antigen interactions in parallel using Biacore A100. Anal. Biochem. 2006, 353:181.
41. Sever J.L., Brenner A.I., Gale A.D., Lyle J.M., Moulton L.H., Ward B.J., West D.J. Safety of anthrax vaccine: an expanded review and evaluation of adverse events reported to the Vaccine Adverse Event Reporting System (VAERS). Pharmacoepidemiol. Drug Saf. 2004, 13:825.
42. Shih T.A., Roederer M., Nussenzweig M.C. Role of antigen receptor affinity in T cell-independent antibody responses in vivo. Nat. Immunol. 2002, 3:399.
43. Siskind G.W., Benacerraf B. Cell selection by antigen in the immune response. Adv. Immunol. 1969, 10:1.
44. Staats H.F., Alam S.M., Scearce R.M., Kirwan S.M., Zhang J.X., Gwinn W.M., Haynes B.F. In vitro and in vivo characterization of anthrax anti-protective antigen and anti-lethal factor monoclonal antibodies after passive transfer in a mouse lethal toxin challenge model to define correlates of immunity. Infect. Immun. 2007, 75:5443.
45. Verkoczy L., Kelsoe G., Moody M.A., Haynes B.F. Role of immune mechanisms in induction of HIV-1 broadly neutralizing antibodies. Curr. Opin. Immunol. 2011, 23:383.
46. Victora G.D., Nussenzweig M.C. Germinal centers. Annu. Rev. Immunol. 2012, 30:429.
47. Wasserman G.M., Grabenstein J.D., Pittman P.R., Rubertone M.V., Gibbs P.P., Wang L.Z., Golder L.G. Analysis of adverse events after anthrax immunization in US Army medical personnel. J. Occup. Environ. Med. 2003, 45:222.