Complex Antigens Drive Permissive Clonal Selection in Germinal Centers

Immunity

Volumn 44, Issue 3, 2016, Pages 542-552

  Kuraoka, Masayuki ^a   Schmidt, Aaron G ^b   Nojima, Takuya ^a   Feng, Feng ^c   Watanabe, Akiko ^a   Kitamura, Daisuke ^d   Harrison, Stephen C ^b,e   Kepler, Thomas B ^c,f   Kelsoe, Garnett ^a  

^a DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d TOKYO UNIVERSITY OF SCIENCE   (Japan)

^e HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^f Boston University   (United States)

Author keywords

B cell repertoire; Clonal selection; Germinal center; Influenza hemagglutinin; Protective antigen of B. anthracis

Indexed keywords

BACILLUS ANTHRACIS PROTECTIVE ANTIGEN; BACTERIAL ANTIGEN; EPITOPE; HAPTEN; INFLUENZA HEMAGGLUTININ; INFLUENZA VIRUS HEMAGGLUTININ; UNCLASSIFIED DRUG; ANTHRAX TOXIN; BACTERIAL TOXIN; LYMPHOCYTE ANTIGEN RECEPTOR; NANOBODY; VIRUS HEMAGGLUTININ;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIGEN BINDING; ANTIGEN BINDING CELL; ANTIGEN MEDIATED CLONAL SELECTION; ARTICLE; B CELL CULTURE; B LYMPHOCYTE; BACILLUS ANTHRACIS; CONTROLLED STUDY; FEMALE; GERMINAL CENTER; MOUSE; NONHUMAN; POPULATION DYNAMICS; PRIORITY JOURNAL; ANIMAL; ANTIBODY AFFINITY; ANTIBODY SPECIFICITY; BAGG ALBINO MOUSE; C57BL MOUSE; CELL CULTURE; GENETICS; HUMAN; HUMORAL IMMUNITY; IMMUNOLOGY; METABOLISM; ORTHOMYXOVIRIDAE; PHYSIOLOGY;

ANIMALS; ANTIBODY AFFINITY; ANTIBODY DIVERSITY; ANTIGENS, BACTERIAL; B-LYMPHOCYTES; BACTERIAL TOXINS; CELLS, CULTURED; CLONAL SELECTION, ANTIGEN-MEDIATED; FEMALE; GERMINAL CENTER; HEMAGGLUTININS, VIRAL; HUMANS; IMMUNITY, HUMORAL; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; ORTHOMYXOVIRIDAE; RECEPTORS, ANTIGEN, B-CELL; SINGLE-DOMAIN ANTIBODIES;

EID: 84960430333     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2016.02.010     Document Type: Article

References (41)

1. Allen D., Simon T., Sablitzky F., Rajewsky K., Cumano A. Antibody engineering for the analysis of affinity maturation of an anti-hapten response. EMBO J. 1988, 7:1995-2001.
2. Aoki-Ota M., Torkamani A., Ota T., Schork N., Nemazee D. Skewed primary Igκ repertoire and V-J joining in C57BL/6 mice: implications for recombination accessibility and receptor editing. J. Immunol. 2012, 188:2305-2315.
3. Baumgarth N. How specific is too specific? B-cell responses to viral infections reveal the importance of breadth over depth. Immunol. Rev. 2013, 255:82-94.
4. Benjamin D.C., Berzofsky J.A., East I.J., Gurd F.R., Hannum C., Leach S.J., Margoliash E., Michael J.G., Miller A., Prager E.M., et al. The antigenic structure of proteins: a reappraisal. Annu. Rev. Immunol. 1984, 2:67-101.
5. Berek C., Berger A., Apel M. Maturation of the immune response in germinal centers. Cell 1991, 67:1121-1129.
6. Bothwell A.L., Paskind M., Reth M., Imanishi-Kari T., Rajewsky K., Baltimore D. Heavy chain variable region contribution to the NPb family of antibodies: somatic mutation evident in a gamma 2a variable region. Cell 1981, 24:625-637.
7. Cain D.W., Sanders S.E., Cunningham M.M., Kelsoe G. Disparate adjuvant properties among three formulations of "alum". Vaccine 2013, 31:653-660.
8. Dal Porto J.M., Haberman A.M., Shlomchik M.J., Kelsoe G. Antigen drives very low affinity B cells to become plasmacytes and enter germinal centers. J. Immunol. 1998, 161:5373-5381.
9. 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, 195:1215-1221.
10. Di Niro R., Lee S.J., Vander Heiden J.A., Elsner R.A., Trivedi N., Bannock J.M., Gupta N.T., Kleinstein S.H., Vigneault F., Gilbert T.J., et al. Salmonella infection drives promiscuous B cell activation followed by extrafollicular affinity maturation. Immunity 2015, 43:120-131.
11. Felsenstein, J. (2005). PHYLIP (Phylogeny Inference Package). http://evolution.genetics.washington.edu/phylip.html.
12. George J., Claflin L. Selection of B cell clones and memory B cells. Semin. Immunol. 1992, 4:11-17.
13. Hangartner L., Zinkernagel R.M., Hengartner H. Antiviral antibody responses: the two extremes of a wide spectrum. Nat. Rev. Immunol. 2006, 6:231-243.
14. 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, 176:679-687.
15. Jacob J., Kelsoe G., Rajewsky K., Weiss U. Intraclonal generation of antibody mutants in germinal centres. Nature 1991, 354:389-392.
16. Jacob J., Przylepa J., Miller C., Kelsoe G. In situ studies of the primary immune response to (4-hydroxy-3-nitrophenyl)acetyl. III. The kinetics of V region mutation and selection in germinal center B cells. J. Exp. Med. 1993, 178:1293-1307.
17. Kantor A.B., Merrill C.E., Herzenberg L.A., Hillson J.L. An unbiased analysis of V(H)-D-J(H) sequences from B-1a, B-1b, and conventional B cells. J. Immunol. 1997, 158:1175-1186.
18. Kavaler J., Caton A.J., Staudt L.M., Gerhard W. A B cell population that dominates the primary response to influenza virus hemagglutinin does not participate in the memory response. Eur. J. Immunol. 1991, 21:2687-2695.
19. Kepler T.B. Reconstructing a B-cell clonal lineage. I. Statistical inference of unobserved ancestors. F1000Res. 2013, 2:103.
20. Kuraoka M., Liao D., Yang K., Allgood S.D., Levesque M.C., Kelsoe G., Ueda Y. Activation-induced cytidine deaminase expression and activity in the absence of germinal centers: insights into hyper-IgM syndrome. J. Immunol. 2009, 183:3237-3248.
21. Kuraoka M., Holl T.M., Liao D., Womble M., Cain D.W., Reynolds A.E., Kelsoe G. Activation-induced cytidine deaminase mediates central tolerance in B cells. Proc. Natl. Acad. Sci. USA 2011, 108:11560-11565.
22. Laver W.G., Air G.M., Webster R.G., Smith-Gill S.J. Epitopes on protein antigens: misconceptions and realities. Cell 1990, 61:553-556.
23. Loh D.Y., Bothwell A.L., White-Scharf M.E., Imanishi-Kari T., Baltimore D. Molecular basis of a mouse strain-specific anti-hapten response. Cell 1983, 33:85-93.
24. MacLennan I.C. Germinal centers. Annu. Rev. Immunol. 1994, 12:117-139.
25. Manser T., Huang S.Y., Gefter M.L. Influence of clonal selection on the expression of immunoglobulin variable region genes. Science 1984, 226:1283-1288.
26. McWilliams L., Su K.Y., Liang X., Liao D., Floyd S., Amos J., Moody M.A., Kelsoe G., Kuraoka M. The human fetal lymphocyte lineage: identification by CD27 and LIN28B expression in B cell progenitors. J. Leukoc. Biol. 2013, 94:991-1001.
27. Nojima T., Haniuda K., Moutai T., Matsudaira M., Mizokawa S., Shiratori I., Azuma T., Kitamura D. In-vitro derived germinal centre B cells differentially generate memory B or plasma cells in vivo. Nat. Commun. 2011, 2:465.
28. Rohatgi S., Ganju P., Sehgal D. Systematic design and testing of nested (RT-)PCR primers for specific amplification of mouse rearranged/expressed immunoglobulin variable region genes from small number of B cells. J. Immunol. Methods 2008, 339:205-219.
29. Sabouri Z., Schofield P., Horikawa K., Spierings E., Kipling D., Randall K.L., Langley D., Roome B., Vazquez-Lombardi R., Rouet R., et al. Redemption of autoantibodies on anergic B cells by variable-region glycosylation and mutation away from self-reactivity. Proc. Natl. Acad. Sci. USA 2014, 111:E2567-E2575.
30. Schmidt A.G., Xu H., Khan A.R., O'Donnell T., Khurana S., King L.R., Manischewitz J., Golding H., Suphaphiphat P., Carfi A., et al. Preconfiguration of the antigen-binding site during affinity maturation of a broadly neutralizing influenza virus antibody. Proc. Natl. Acad. Sci. USA 2013, 110:264-269.
31. Schmidt A.G., Therkelsen M.D., Stewart S., Kepler T.B., Liao H.X., Moody M.A., Haynes B.F., Harrison S.C. Viral receptor-binding site antibodies with diverse germline origins. Cell 2015, 161:1026-1034.
32. Schwickert T.A., Victora G.D., Fooksman D.R., Kamphorst A.O., Mugnier M.R., Gitlin A.D., Dustin M.L., Nussenzweig M.C. A dynamic T cell-limited checkpoint regulates affinity-dependent B cell entry into the germinal center. J. Exp. Med. 2011, 208:1243-1252.
33. Shih T.A., Meffre E., Roederer M., Nussenzweig M.C. Role of BCR affinity in T cell dependent antibody responses in vivo. Nat. Immunol. 2002, 3:570-575.
34. Takahashi Y., Dutta P.R., Cerasoli D.M., Kelsoe G. In situ studies of the primary immune response to (4-hydroxy-3-nitrophenyl)acetyl. V. Affinity maturation develops in two stages of clonal selection. J. Exp. Med. 1998, 187:885-895.
35. Tiller T., Busse C.E., Wardemann H. Cloning and expression of murine Ig genes from single B cells. J. Immunol. Methods 2009, 350:183-193.
36. Wardemann H., Yurasov S., Schaefer A., Young J.W., Meffre E., Nussenzweig M.C. Predominant autoantibody production by early human B cell precursors. Science 2003, 301:1374-1377.
37. Weiss U., Rajewsky K. The repertoire of somatic antibody mutants accumulating in the memory compartment after primary immunization is restricted through affinity maturation and mirrors that expressed in the secondary response. J. Exp. Med. 1990, 172:1681-1689.
38. White-Scharf M.E., Imanishi-Kari T. Characterization of the NPa idiotype through the analysis of monoclonal BALB/c anti-(4-hydroxy-3-nitrophenyl)acetyl (NP) antibodies. Eur. J. Immunol. 1981, 11:897-904.
39. Whittle J.R., Zhang R., Khurana S., King L.R., Manischewitz J., Golding H., Dormitzer P.R., Haynes B.F., Walter E.B., Moody M.A., et al. Broadly neutralizing human antibody that recognizes the receptor-binding pocket of influenza virus hemagglutinin. Proc. Natl. Acad. Sci. USA 2011, 108:14216-14221.
40. Wrammert J., Smith K., Miller J., Langley W.A., Kokko K., Larsen C., Zheng N.Y., Mays I., Garman L., Helms C., et al. Rapid cloning of high-affinity human monoclonal antibodies against influenza virus. Nature 2008, 453:667-671.
41. Zhang Y., Meyer-Hermann M., George L.A., Figge M.T., Khan M., Goodall M., Young S.P., Reynolds A., Falciani F., Waisman A., et al. Germinal center B cells govern their own fate via antibody feedback. J. Exp. Med. 2013, 210:457-464.