A simple flow-cytometric method measuring B cell surface immunoglobulin avidity enables characterization of affinity maturation to influenza a virus

mBio

Volumn 6, Issue 4, 2015, Pages

  Frank, Gregory M ^a   Angeletti, Davide ^a   Ince, William L ^a   Gibbs, James S ^a   Khurana, Surender ^b   Wheatley, Adam K ^a   Max, Edward E ^b   McDermott, Adrian B ^a   Golding, Hana ^b   Stevens, James ^c   Bennink, Jack R ^a   Yewdell, Jonathan W ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

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

Author keywords

[No Author keywords available]

Indexed keywords

ADJUVANT; IMMUNOGLOBULIN G; INFLUENZA VACCINE; INFLUENZA VIRUS HEMAGGLUTININ; LYMPHOCYTE MEMBRANE IMMUNOGLOBULIN; LYMPHOCYTE ANTIGEN RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY AFFINITY; ANTIBODY RESPONSE; ARTICLE; B LYMPHOCYTE; CONTROLLED STUDY; CORRELATION ANALYSIS; DRUG DESIGN; FLOW CYTOMETRY; GERMINAL CENTER; IMMUNE RESPONSE; INFLUENZA A VIRUS; LYMPHOCYTE COUNT; MOUSE; NONHUMAN; PRIORITY JOURNAL; VIRUS IMMUNITY; ANIMAL; CELL DIFFERENTIATION; CHEMISTRY; IMMUNOLOGY; INTRAMUSCULAR DRUG ADMINISTRATION; PHYSIOLOGY; PROCEDURES;

ANIMALS; ANTIBODY AFFINITY; B-LYMPHOCYTES; CELL DIFFERENTIATION; FLOW CYTOMETRY; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; INFLUENZA A VIRUS; INJECTIONS, INTRAMUSCULAR; MICE; RECEPTORS, ANTIGEN, B-CELL;

EID: 84940888109     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.01156-15     Document Type: Article

References (49)

1. Stoop JW, Zegers BJ, Sander PC, Ballieux RE. 1969. Serum immunoglobulin levels in healthy children and adults. Clin Exp Immunol 4:101–112.
2. Eisen HN, Siskind GW. 1964. Variations in affinities of antibodies during the immune response. Biochemistry 3:996–1008. http://dx.doi.org/10.1021/bi00895a027.
3. Victora GD, Nussenzweig MC. 2012. Germinal centers. Annu Rev Immunol 30:429–457. http://dx.doi.org/10.1146/annurev-immunol-020711-075032.
4. McHeyzer-Williams LJ, McHeyzer-Williams MG. 2005. Antigen-specific memory B cell development. Annu Rev Immunol 23:487–513. http://dx.doi.org/10.1146/annurev.immunol.23.021704.115732.
5. Blink EJ, Light A, Kallies A, Nutt SL, Hodgkin PD, Tarlinton DM. 2005. Early appearance of germinal center-derived memory B cells and plasma cells in blood after primary immunization. J Exp Med 201:545–554. http://dx.doi.org/10.1084/jem.20042060.
6. Chan TD, Wood K, Hermes JR, Butt D, Jolly CJ, Basten A, Brink R. 2012. Elimination of germinal-center-derived self-reactive B cells is governed by the location and concentration of self-antigen. Immunity 37: 893–904. http://dx.doi.org/10.1016/j.immuni.2012.07.017.
7. Pape KA, Taylor JJ, Maul RW, Gearhart PJ, Jenkins MK. 2011. Different B cell populations mediate early and late memory during an endogenous immune response. Science 331:1203–1207. http://dx.doi.org/10.1126/science.1201730.
8. Wrammert J, Koutsonanos D, Li GM, Edupuganti S, Sui J, Morrissey M, McCausland M, Skountzou I, Hornig M, Lipkin WI, Mehta A, Razavi B, Del Rio C, Zheng NY, Lee JH, Huang M, Ali Z, Kaur K, Andrews S, Amara RR, Wang Y, Das SR, O’Donnell CD, Yewdell JW, Subbarao K, Marasco WA, Mulligan MJ, Compans R, Ahmed R, Wilson PC. 2011. Broadly cross-reactive antibodies dominate the human B cell response against 2009 pandemic H1N1 influenza virus infection. J Exp Med 208:181–193. http://dx.doi.org/10.1084/jem.20101352.
9. Purtha WE, Tedder TF, Johnson S, Bhattacharya D, Diamond MS. 2011. Memory B cells, but not long-lived plasma cells, possess antigen specificities for viral escape mutants. J Exp Med 208:2599–2606. http://dx.doi.org/10.1084/jem.20110740.
10. Wrammert J, Smith K, Miller J, Langley WA, Kokko K, Larsen C, Zheng NY, Mays I, Garman L, Helms C, James J, Air GM, Capra JD, Ahmed R, Wilson PC. 2008. Rapid cloning of high-affinity human monoclonal antibodies against influenza virus. Nature 453:667–671. http://dx.doi.org/10.1038/nature06890.
11. Gerhard W, Mozdzanowska K, Furchner M, Washko G, Maiese K. 1997. Role of the B-cell response in recovery of mice from primary influenza virus infection. Immunol Rev 159:95–103. http://dx.doi.org/10.1111/j.1600-065X.1997.tb01009.x.
12. Puck JM, Glezen WP, Frank AL, Six HR. 1980. Protection of infants from infection with influenza A virus by transplacentally acquired antibody. J Infect Dis 142:844–849. http://dx.doi.org/10.1093/infdis/142.6.844.
13. Molinari NA, Ortega-Sanchez IR, Messonnier ML, Thompson WW, Wortley PM, Weintraub E, Bridges CB. 2007. The annual impact of seasonal influenza in the US: measuring disease burden and costs. Vaccine 25:5086–5096. http://dx.doi.org/10.1016/j.vaccine.2007.03.046.
14. Beigel JH. 2008. Influenza. Crit Care Med 36:2660–2666. http://dx.doi.org/10.1097/CCM.0b013e318180b039.
15. Gerhard W. 2001. The role of the antibody response in influenza virus infection. Curr Top Microbiol Immunol 260:171–190. http://dx.doi.org/10.1007/978-3-662-05783-4_9.
16. Doucett VP, Gerhard W, Owler K, Curry D, Brown L, Baumgarth N. 2005. Enumeration and characterization of virus-specific B cells by multicolor flow cytometry. J Immunol Methods 303:40–52. http://dx.doi.org/10.1016/j.jim.2005.05.014.
17. Onodera T, Takahashi Y, Yokoi Y, Ato M, Kodama Y, Hachimura S, Kurosaki T, Kobayashi K. 2012. Memory B cells in the lung participate in protective humoral immune responses to pulmonary influenza virus reinfection. Proc Natl Acad Sci U S A 109:2485–2490. http://dx.doi.org/10.1073/pnas.1115369109.
18. Bardelli M, Alleri L, Angiolini F, Buricchi F, Tavarini S, Sammicheli C, Nuti S, Degl’Innocenti E, Isnardi I, Fragapane E, Del Giudice G, Castellino F, Galli G. 2013. Ex vivo analysis of human memory B lymphocytes specific for a and B influenza hemagglutinin by polychromatic flowcytometry. PLoS One 8:e70620. http://dx.doi.org/10.1371/journal.pone.0070620.
19. Whittle JR, Wheatley AK, Wu L, Lingwood D, Kanekiyo M, Ma SS, Narpala SR, Yassine HM, Frank GM, Yewdell JW, Ledgerwood JE, Wei CJ, McDermott AB, Graham BS, Koup RA, Nabel GJ. 2014. Flow cytometry reveals that H5N1 vaccination elicits cross-reactive stemdirected antibodies from multiple Ig heavy-chain lineages. J Virol 88: 4047–4057. http://dx.doi.org/10.1128/JVI.03422-13.
20. Magadán JG, Khurana S, Das SR, Frank GM, Stevens J, Golding H, Bennink JR, Yewdell JW. 2013. Influenza A virus hemagglutinin trimerization completes monomer folding and antigenicity. J Virol 87: 9742–9753. http://dx.doi.org/10.1128/JVI.00471-13.
21. Price PW, McKinney EC, Wang Y, Sasser LE, Kandasamy MK, Matsuuchi L, Milcarek C, Deal RB, Culver DG, Meagher RB. 2009. Engineered cell surface expression of membrane immunoglobulin as a means to identify monoclonal antibody-secreting hybridomas. J Immunol Methods 343:28–41. http://dx.doi.org/10.1016/j.jim.2009.01.005.
22. Oracki SA, Walker JA, Hibbs ML, Corcoran LM, Tarlinton DM. 2010. Plasma cell development and survival. Immunol Rev 237:140–159. http://dx.doi.org/10.1111/j.1600-065X.2010.00940.x.
23. Shimizu T, Oda M, Azuma T. 2003. Estimation of the relative affinity of B cell receptor by flow cytometry. J Immunol Methods 276:33–44. http://dx.doi.org/10.1016/S0022-1759(03)00068-1.
24. Kavaler J, Caton AJ, Staudt LM, Schwartz D, Gerhard W. 1990. A set of closely related antibodies dominates the primary antibody response to the antigenic site CB of the A/PR/8/34 influenza virus hemagglutinin. J Immunol 145:2312–2321.
25. Muramatsu M, Kinoshita K, Fagarasan S, Yamada S, Shinkai Y, Honjo T. 2000. Class switch recombination and hypermutation require activation-induced cytidine deaminase (AID), a potential RNA editing enzyme. Cell 102:553–563. http://dx.doi.org/10.1016/S0092-8674(00)00078-7.
26. Zaheen A, Boulianne B, Parsa JY, Ramachandran S, Gommerman JL, Martin A. 2009. AID constrains germinal center size by rendering B cells susceptible to apoptosis. Blood 114:547–554. http://dx.doi.org/10.1182/blood-2009-03-211763.
27. Harris K, Ream R, Gao J, Eichelberger MC. 2011. Intramuscular immunization of mice with live influenza virus is more immunogenic and offers greater protection than immunization with inactivated virus. Virol J 8:251. http://dx.doi.org/10.1186/1743-422X-8-251.
28. Virelizier JL. 1975. Host defenses against influenza virus: the role of antihemagglutinin antibody. J Immunol 115:434–439.
29. Whittle JR, Zhang R, Khurana S, King LR, Manischewitz J, Golding H, Dormitzer PR, Haynes BF, Walter EB, Moody MA, Kepler TB, Liao HX, Harrison SC. 2011. Broadly neutralizing human antibody that recognizes the receptor-binding pocket of influenza virus hemagglutinin. Proc Natl Acad Sci U S A 108:14216–14221. http://dx.doi.org/10.1073/pnas.1111497108.
30. Roost HP, Bachmann MF, Haag A, Kalinke U, Pliska V, Hengartner H, Zinkernagel RM. 1995. Early high-affinity neutralizing anti-viral IgG responses without further overall improvements of affinity. Proc Natl Acad Sci U S A 92:1257–1261. http://dx.doi.org/10.1073/pnas.92.5.1257.
31. FazekasdeStGroth S. 1967. Cross recognition and cross reactivity. Cold Spring Harb Symp Quant Biol 32:525–536.
32. Jerne NK. 1985. The generative grammar of the immune system. Science 229:1057–1059. http://dx.doi.org/10.1126/science.4035345.
33. Yewdell JW. 2003. He put the id in idiotype. EMBO Rep 4:931–1004. http://dx.doi.org/10.1038/sj.embor.embor951.
34. Ennis FA, Yi-Hua Q, Schild GC. 1982. Antibody and cytotoxic T lymphocyte responses of humans to live and inactivated influenza vaccines. J Gen Virol 58:273–281. http://dx.doi.org/10.1099/0022-1317-58-2-273.
35. Yewdell JW. 1981. The study of influenza virus antigens by means of monoclonal hybridoma antibodies. University of Pennsylvania, Philadelphia, PA.
36. Yang H, Chen LM, Carney PJ, Donis RO, Stevens J. 2010. Structures of receptor complexes of a North American H7N2 influenza hemagglutinin with a loop deletion in the receptor binding site. PLoS Pathog 6:e1001081. http://dx.doi.org/10.1371/journal.ppat.1001081.
37. Elsner RA, Ernst DN, Baumgarth N. 2012. Single and coexpression of CXCR4 and CXCR5 identifies CD4 T helper cells in distinct lymph node niches during influenza virus infection. J Virol 86:7146–7157. http://dx.doi.org/10.1128/JVI.06904-11.
38. Boyden AW, Legge KL, Waldschmidt TJ. 2012. Pulmonary infection with influenza A virus induces site-specific germinal center and T follicular helper cell responses. PLoS One 7:e40733. http://dx.doi.org/10.1371/journal.pone.0040733.
39. Bessa J, Zabel F, Link A, Jegerlehner A, Hinton HJ, Schmitz N, Bauer M, Kündig TM, Saudan P, Bachmann MF. 2012. Low-affinity B cells transport viral particles from the lung to the spleen to initiate antibody responses. Proc Natl Acad Sci U S A 109:20566–20571. http://dx.doi.org/10.1073/pnas.1206970109.
40. Zinkernagel RM. 2002. On differences between immunity and immunological memory. Curr Opin Immunol 14:523–536. http://dx.doi.org/10.1016/S0952-7915(02)00367-9.
41. Fazekas de Saint Groth S, Webster RG, Davenport FM. 1969. The antigenic subunits of influenza viruses. I. The homologous antibody response. J Immunol 103:1099–1106.
42. Khurana S, Verma N, Yewdell JW, Hilbert AK, Castellino F, Lattanzi M, Del Giudice G, Rappuoli R, Golding H. 2011. MF59 adjuvant enhances diversity and affinity of antibody-mediated immune response to pandemic influenza vaccines. Sci Transl Med 3:85ra48. http://dx.doi.org/10.1126/scitranslmed.3002336.
43. Hedman K, Hietala J, Tiilikainen A, Hartikainen-Sorri AL, Räihä K, Suni J, Väänänen P, Pietiläinen M. 1989. Maturation of immunoglobulin G avidity after rubella vaccination studied by an enzyme linked immunosorbent assay (avidity-ELISA) and by haemolysis typing. J Med Virol 27:293–298. http://dx.doi.org/10.1002/jmv.1890270407.
44. Wilson PC, Andrews SF. 2012. Tools to therapeutically harness the human antibody response. Nat Rev Immunol 12:709–719. http://dx.doi.org/10.1038/nri3285.
45. Burton DR, Poignard P, Stanfield RL, Wilson IA. 2012. Broadly neutralizing antibodies present new prospects to counter highly antigenically diverse viruses. Science 337:183–186. http://dx.doi.org/10.1126/science.1225416.
46. Finn JA, Crowe JE, Jr. 2013. Impact of new sequencing technologies on studies of the human B cell repertoire. Curr Opin Immunol 25:613–618. http://dx.doi.org/10.1016/j.coi.2013.09.010.
47. Osterholm MT, Kelley NS, Sommer A, Belongia EA. 2012. Efficacy and effectiveness of influenza vaccines: a systematic review and meta-analysis. Lancet Infect Dis 12:36–44. http://dx.doi.org/10.1016/S1473-3099(11)70295-X.
48. List T, Neri D. 2013. Immunocytokines: a review of molecules in clinical development for cancer therapy. Clin Pharmacol Adv Appl 5:29–45. http://dx.doi.org/10.2147/CPAA.S49231.
49. Caton AJ, Koprowski H. 1990. Influenza virus hemagglutinin-specific antibodies isolated from a combinatorial expression library are closely related to the immune response of the donor. Proc Natl Acad Sci U S A 87:6450–6454. http://dx.doi.org/10.1073/pnas.87.16.6450.