97
Views
3
CrossRef citations to date
0
Altmetric
Review

Generating humoral immune memory following infection or vaccination

Pages 1083-1093 | Published online: 09 Jan 2014

References

  • Ahmed R, Rouse BT. Immunological memory. Immunol. Rev.211(1), 5–7 (2006).
  • Yu X, Tsibane T, McGraw PA et al. Neutralizing antibodies derived from the B cells of 1918 influenza pandemic survivors. Nature455(7212), 532–536 (2008).
  • Amanna IJ, Slifka MK, Crotty S. Immunity and immunological memory following smallpox vaccination. Immunol. Rev.211, 320–337 (2006).
  • McHeyzer-Williams LJ, McHeyzer-Williams MG. Antigen-specific memory B cell development. Annu. Rev. Immunol.23, 487–513 (2005).
  • Tarlinton D. B-cell memory: are subsets necessary? Nat. Rev. Immunol.6(10), 785–790 (2006).
  • de Vinuesa CG, Cook MC, Ball J et al. Germinal centers without T cells. J. Exp. Med.191(3), 485–494 (2000).
  • Allen CDC, Okada T, Cyster JG. Germinal-center organization and cellular dynamics. Immunity27(2), 190–202 (2007).
  • Tarlinton DM. Evolution in miniature: selection, survival and distribution of antigen reactive cells in the germinal centre. Immunol. Cell Biol.86(2), 133–138 (2008).
  • Brodeur SR, Angelini F, Bacharier LB et al. C4b-binding protein (C4BP) activates B cells through the CD40 receptor. Immunity18(6), 837–848 (2003).
  • Obukhanych TV, Nussenzweig MC. T-independent type II immune responses generate memory B cells. J. Exp. Med.203(2), 305–310 (2006).
  • Inamine A, Takahashi Y, Baba N et al. Two waves of memory B-cell generation in the primary immune response. Int. Immunol.17(5), 581–589 (2005).
  • Chan TD, Gatto D, Wood K, Camidge T, Basten A, Brink R. Antigen affinity controls rapid T-dependent antibody production by driving the expansion rather than the differentiation or extrafollicular migration of early plasmablasts. J. Immunol.183(5), 3139–3149 (2009).
  • Weller S, Braun MC, Tan BK et al. Human blood IgM “memory” B cells are circulating splenic marginal zone B cells harboring a prediversified immunoglobulin repertoire. Blood104(12), 3647–3654 (2004).
  • Phan TG, Paus D, Chan TD et al. High affinity germinal center B cells are actively selected into the plasma cell compartment. J. Exp. Med.203(11), 2419–2424 (2006).
  • Shih T-AY, Meffre E, Roederer M, Nussenzweig MC. Role of BCR affinity in T cell dependent antibody responses in vivo. Nat. Immunol.3(6), 570–575 (2002).
  • Anderson SM, Khalil A, Uduman M et al. Taking advantage: high-affinity B cells in the germinal center have lower death rates, but similar rates of division, compared to low-affinity cells. J. Immunol.183(11), 7314–7325 (2009).
  • Cunningham AF, Gaspal F, Serre K et al. Salmonella induces a switched antibody response without germinal centers that impedes the extracellular spread of infection. J. Immunol.178(10), 6200–6207 (2007).
  • Gatto D, Paus D, Basten A, Mackay CR, Brink R. Guidance of B cells by the orphan G protein-coupled receptor EBI2 shapes humoral immune responses. Immunity31(2), 259–269 (2009).
  • Pereira JP, Kelly LM, Xu Y, Cyster JG. EBI2 mediates B cell segregation between the outer and centre follicle. Nature460(7259), 1122–1126 (2009).
  • Paul E, Nelde A, Verschoor A, Carrol MC. Follicular exclusion of autoreactive B cells requires FcγRIIb. Int. Immunol.19(4), 365–373 (2007).
  • Nieuwenhuis P, Opstelten D. Functional anatomy of germinal centers. Am. J. Anatomy170(3), 421–435 (1984).
  • Allen CDC, Ansel KM, Low C et al. Germinal center dark and light zone organization is mediated by CXCR4 and CXCR5. Nat. Immunol.5(9), 943–952 (2004).
  • Heidelberger M, Kendall FE. A quantitative theory of the precipitin reaction. III. The reaction between crystalline egg albumin and its homologous antibody. J. Exp. Med.62(5), 697–720 (1935).
  • Eisen HN, Siskind GW. Variations in affinities of antibodies during the immune response. Biochemistry3, 996–1008 (1964).
  • Steiner LA, Eisen HN. Sequential changes in the relative affinity of antibodies synthesized during the immune response. J. Exp. Med.126(6), 1161–1183 (1967).
  • Siskind GW, Benacerraf B. Cell selection by antigen in the immune response. Adv. Immunol.10, 1–50 (1969).
  • Liu YJ, Joshua DE, Williams GT, Smith CA, Gordon J, MacLennan IC. Mechanism of antigen-driven selection in germinal centres. Nature342(6252), 929–931 (1989).
  • Wagner SD, Neuberger MS. Somatic hypermutation of immunoglobulin genes. Annu. Rev. Immunol.14, 441–457 (1996).
  • Jacob J, Kelsoe G, Rajewsky K, Weiss U. Intraclonal generation of antibody mutants in germinal centres. Nature354(6352), 389–392 (1991).
  • Berek C, Berger A, Apel M. Maturation of the immune response in germinal centers. Cell67(6), 1121–1129 (1991).
  • Matsumoto M, Lo SF, Carruthers CJ et al. Affinity maturation without germinal centres in lymphotoxin-α-deficient mice. Nature382(6590), 462–466 (1996).
  • Tarlinton DM, Smith KG. Dissecting affinity maturation: a model explaining selection of antibody-forming cells and memory B cells in the germinal centre. Immunol. Today21(9), 436–441 (2000).
  • MacLennan IC. Germinal centers. Annu. Rev. Immunol.12, 117–139 (1994).
  • Allen CDC, Okada T, Tang HL, Cyster JG. Imaging of germinal center selection events during affinity maturation. Science315(5811), 528–531 (2007).
  • Hauser AE, Junt T, Mempel TR et al. Definition of germinal-center B cell migration in vivo reveals predominant intrazonal circulation patterns. Immunity26(5), 655–667 (2007).
  • Schwickert TA, Lindquist RL, Shakhar G et al. In vivo imaging of germinal centres reveals a dynamic open structure. Nature446(7131), 83–87 (2007).
  • Allen CDC, Cyster JG. Follicular dendritic cell networks of primary follicles and germinal centers: phenotype and function. Semin. Immunol.20(1), 14–25 (2008).
  • Ye BH, Cattoretti G, Shen Q et al. The Bcl-6 proto-oncogene controls germinal-centre formation and Th2-type inflammation. Nat. Genet.16(2), 161–170 (1997).
  • Tew JG, Wu J, Fakher M, Szakal AK, Qin D. Follicular dendritic cells: beyond the necessity of T-cell help. Trends Immunol.22(7), 361–367 (2001).
  • Franzoso G, Carlson L, Poljak L et al. Mice deficient in nuclear factor (NF)-κB/p52 present with defects in humoral responses, germinal center reactions, and splenic microarchitecture. J. Exp. Med.187(2), 147–159 (1998).
  • Poljak L, Carlson L, Cunningham K, Kosco-Vilbois MH, Siebenlist U. Distinct activities of p52/NF-κB required for proper secondary lymphoid organ microarchitecture: functions enhanced by Bcl-3. J. Immunol.163(12), 6581–6588 (1999).
  • Matsumoto M, Fu YX, Molina H et al. Distinct roles of lymphotoxin α and the type I tumor necrosis factor (TNF) receptor in the establishment of follicular dendritic cells from non-bone marrow-derived cells. J. Exp. Med.186(12), 1997–2004 (1997).
  • Endres R, Alimzhanov MB, Plitz T et al. Mature follicular dendritic cell networks depend on expression of lymphotoxin β receptor by radioresistant stromal cells and of lymphotoxin β and tumor necrosis factor by B cells. J. Exp. Med.189(1), 159–168 (1999).
  • Ansel KM, Ngo VN, Hyman PL et al. A chemokine-driven positive feedback loop organizes lymphoid follicles. Nature406(6793), 309–314 (2000).
  • Hannum LG, Haberman AM, Anderson SM, Shlomchik MJ. Germinal center initiation, variable gene region hypermutation, and mutant B cell selection without detectable immune complexes on follicular dendritic cells. J. Exp. Med.192(7), 931–942 (2000).
  • Rahman ZSM, Rao SP, Kalled SL, Manser T. Normal induction but attenuated progression of germinal center responses in BAFF and BAFF-R signaling-deficient mice. J. Exp. Med.198(8), 1157–1169 (2003).
  • Phan TG, Green JA, Gray EE, Xu Y, Cyster JG. Immune complex relay by subcapsular sinus macrophages and noncognate B cells drives antibody affinity maturation. Nat. Immunol.10(7), 786–793 (2009).
  • Victoratos P, Lagnel J, Tzima S et al. FDC-specific functions of p55TNFR and IKK2 in the development of FDC networks and of antibody responses. Immunity24(1), 65–77 (2006).
  • Randall KL, Lambe T, Johnson A et al. Dock8 mutations cripple B cell immunological synapses, germinal centers and long-lived antibody production. Nat. Immunol.10(12), 1283–1291 (2009).
  • Phan TG, Grigorova I, Okada T, Cyster JG. Subcapsular encounter and complement-dependent transport of immune complexes by lymph node B cells. Nat. Immunol.8(9), 992–1000 (2007).
  • Al-Qahtani A, Xu Z, Zan H, Walsh CM, Casali P. A role for DRAK2 in the germinal center reaction and the antibody response. Autoimmunity41(5), 341–352 (2008).
  • Koopman G, Keehnen RM, Lindhout E, Zhou DF, de Groot C, Pals ST. Germinal center B cells rescued from apoptosis by CD40 ligation or attachment to follicular dendritic cells, but not by engagement of surface immunoglobulin or adhesion receptors, become resistant to CD95-induced apoptosis. Eur J. Immunol.27(1), 1–7 (1997).
  • Vinuesa CG, Tangye SG, Moser B, Mackay CR. Follicular B helper T cells in antibody responses and autoimmunity. Nat. Rev. Immunol.5(11), 853–865 (2005).
  • Nurieva RI, Chung Y, Martinez GJ et al. Bcl6 mediates the development of T follicular helper cells. Science325(5943), 1001–1005 (2009).
  • Johnston RJ, Poholek AC, DiToro D et al. Bcl6 and Blimp-1 are reciprocal and antagonistic regulators of T follicular helper cell differentiation. Science325(5943), 1006–1010 (2009).
  • Yu D, Rao S, Tsai LM et al. The transcriptional repressor Bcl-6 directs T follicular helper cell lineage commitment. Immunity31(3), 457–468 (2009).
  • Zotos D, Coquet JM, Zhang Y et al. IL-21 regulates germinal center B cell differentiation and proliferation through a B cell-intrinsic mechanism. J. Exp. Med.207(2), 365–378 (2010).
  • Linterman MA, Beaton L, Yu D et al. IL-21 acts directly on B cells to regulate Bcl-6 expression and germinal center responses. J. Exp. Med.207(2), 353–363 (2010).
  • Smith KG, Light A, O’Reilly LA, Ang SM, Strasser A, Tarlinton D. Bcl-2 transgene expression inhibits apoptosis in the germinal center and reveals differences in the selection of memory B cells and bone marrow antibody-forming cells. J. Exp. Med.191(3), 475–484 (2000).
  • Klein U, Casola S, Cattoretti G et al. Transcription factor IRF4 controls plasma cell differentiation and class-switch recombination. Nat. Immunol.7(7), 773–782 (2006).
  • Shapiro-Shelef M, Lin K-I, McHeyzer-Williams LJ, Liao J, McHeyzer-Williams MG, Calame K. Blimp-1 is required for the formation of immunoglobulin secreting plasma cells and pre-plasma memory B cells. Immunity19(4), 607–620 (2003).
  • Shaffer AL, Shapiro-Shelef M, Iwakoshi NN et al. XBP1, downstream of Blimp-1, expands the secretory apparatus and other organelles, and increases protein synthesis in plasma cell differentiation. Immunity21(1), 81–93 (2004).
  • Allen RC, Armitage RJ, Conley ME et al. CD40 ligand gene defects responsible for X-linked hyper-IgM syndrome. Science259(5097), 990–993 (1993).
  • Aruffo A, Farrington M, Hollenbaugh D et al. The CD40 ligand, gp39, is defective in activated T cells from patients with X-linked hyper-IgM syndrome. Cell72(2), 291–300 (1993).
  • DiSanto JP, Bonnefoy JY, Gauchat JF, Fischer A, de Saint Basile G. CD40 ligand mutations in x-linked immunodeficiency with hyper-IgM. Nature361(6412), 541–543 (1993).
  • Fuleihan R, Ramesh N, Loh R et al. Defective expression of the CD40 ligand in X chromosome-linked immunoglobulin deficiency with normal or elevated IgM. Proc. Natl Acad. Sci. USA90(6), 2170–2173 (1993).
  • Ferrari S, Giliani S, Insalaco A et al. Mutations of CD40 gene cause an autosomal recessive form of immunodeficiency with hyper IgM. Proc. Natl Acad. Sci. USA98(22), 12614–12619 (2001).
  • Coffey AJ, Brooksbank RA, Brandau O et al. Host response to EBV infection in X-linked lymphoproliferative disease results from mutations in an SH2-domain encoding gene. Nat. Genet.20(2), 129–135 (1998).
  • Nichols KE, Harkin DP, Levitz S et al. Inactivating mutations in an SH2 domain-encoding gene in X-linked lymphoproliferative syndrome. Proc. Natl Acad. Sci. USA95(23), 13765–13770 (1998).
  • Sayos J, Wu C, Morra M et al. The X-linked lymphoproliferative-disease gene product SAP regulates signals induced through the co-receptor SLAM. Nature395(6701), 462–469 (1998).
  • Crotty S, Kersh EN, Cannons J, Schwartzberg PL, Ahmed R. SAP is required for generating long-term humoral immunity. Nature421(6920), 282–287 (2003).
  • Qi H, Cannons JL, Klauschen F, Schwartzberg PL, Germain RN. SAP-controlled T–B cell interactions underlie germinal centre formation. Nature455(7214), 764–769 (2008).
  • Nichols KE, Ma CS, Cannons JL, Schwartzberg PL, Tangye SG. Molecular and cellular pathogenesis of X-linked lymphoproliferative disease. Immunol. Rev.203, 180–199 (2005).
  • Ma CS, Nichols KE, Tangye SG. Regulation of cellular and humoral immune responses by the SLAM and SAP families of molecules. Annu. Rev. Immunol.25, 337–379 (2007).
  • Bacchelli C, Buckridge S, Thrasher AJ, Gaspar HB. Translational mini-review series on immunodeficiency: molecular defects in common variable immunodeficiency. Clin. Exp. Immunol.149(3), 401–409 (2007).
  • Grimbacher B, Hutloff A, Schlesier M et al. Homozygous loss of ICOS is associated with adult-onset common variable immunodeficiency. Nat. Immunol.4(3), 261–268 (2003).
  • Warnatz K, Bossaller L, Salzer U et al. Human ICOS deficiency abrogates the germinal center reaction and provides a monogenic model for common variable immunodeficiency. Blood107(8), 3045–3052 (2006).
  • Wong S-C, Oh E, Ng C-H, Lam K-P. Impaired germinal center formation and recall T-cell-dependent immune responses in mice lacking the costimulatory ligand B7-H2. Blood102(4), 1381–1388 (2003).
  • van Zelm MC, Reisli I, van der Burg M et al. An antibody-deficiency syndrome due to mutations in the CD19 gene. N. Engl. J. Med354(18), 1901–1912 (2006).
  • Wang Y, Brooks SR, Li X, Anzelon AN, Rickert RC, Carter RH. The physiologic role of CD19 cytoplasmic tyrosines. Immunity17(4), 501–514 (2002).
  • van Zelm MC, Smet J, Adams B et al. CD81 gene defect in humans disrupts CD19 complex formation and leads to antibody deficiency. J. Clin. Invest.120(4), 1265–1274 (2010).
  • Mackay F, Schneider P, Rennert P, Browning J. Baff and April: a tutorial on B cell survival. Annu. Rev. Immunol.21, 231–264 (2003).
  • Salzer U, Chapel HM, Webster ADB et al. Mutations in TNFRSF13B encoding TACI are associated with common variable immunodeficiency in humans. Nat. Genet.37(8), 820–828 (2005).
  • Castigli E, Wilson SA, Garibyan L et al. TACI is mutant in common variable immunodeficiency and IgA deficiency. Nat. Genet.37(8), 829–834 (2005).
  • Pan-Hammarstrom Q, Salzer U, Du L et al. Reexamining the role of TACI coding variants in common variable immunodeficiency and selective IgA deficiency. Nat. Genet.39(4), 429–430 (2007).
  • Yan M, Wang H, Chan B et al. Activation and accumulation of B cells in TACI-deficient mice. Nat. Immunol.2(7), 638–643 (2001).
  • Warnatz K, Salzer U, Rizzi M et al. B-cell activating factor receptor deficiency is associated with an adult-onset antibody deficiency syndrome in humans. Proc. Natl Acad. Sci. USA106(33), 13945–13950 (2009).
  • Zheng B, Switzer K, Marinova E, Wansley D, Han S. Correction of age-associated deficiency in germinal center response by immunization with immune complexes. Clin. Immunol.124(2), 131–137 (2007).
  • Rush CM, Mitchell TJ, Burke B, Garside P. Dissecting the components of the humoral immune response elicited by DNA vaccines. Vaccine24(6), 776–784 (2006).
  • Ma Y, Ross AC. Toll-like receptor 3 ligand and retinoic acid enhance germinal center formation and increase the tetanus toxoid vaccine response. Clin. Vaccine Immunol.16(10), 1476–1484 (2009).
  • Lee CH, Melchers M, Wang H et al. Regulation of the germinal center gene program by interferon (IFN) regulatory factor 8/IFN consensus sequence-binding protein. J. Exp. Med.203(1), 63–72 (2006). (Erratum appears in J. Exp. Med.203(2), 475 [2006]).
  • Schubart K, Massa S, Schubart D, Corcoran LM, Rolink AG, Matthias P. B cell development and immunoglobulin gene transcription in the absence of Oct-2 and OBF-1. Nat. Immunol.2(1), 69–74 (2001) (Erratum appears in Nat. Immunol.7(9), 1004 [2006]).
  • Huntington ND, Xu Y, Puthalakath H et al. CD45 links the B cell receptor with cell survival and is required for the persistence of germinal centers. Nat. Immunol.7(2), 190–198 (2006).
  • Clayton E, Bardi G, Bell SE et al. A Crucial role for the p110{δ} subunit of phosphatidylinositol 3-kinase in B cell development and activation. J. Exp. Med.196, 753–763 (2002).
  • Otero DC, Rickert RC. CD19 function in early and late B cell development. II. CD19 facilitates the pro-B/pre-B transition. J. Immunol.171(11), 5921–5930 (2003).
  • Quemeneur L, Angeli V, Chopin M, Jessberger R. SWAP-70 deficiency causes high-affinity plasma cell generation despite impaired germinal center formation. Blood111(5), 2714–2724 (2008).
  • Su GH, Chen HM, Muthusamy N et al. Defective B cell receptor-mediated responses in mice lacking the Ets protein, Spi-B. EMBO J.16(23), 7118–7129 (1997).
  • Delgado P, Cubelos B, Calleja E et al. Essential function for the GTPase TC21 in homeostatic antigen receptor signaling. Nat. Immunol.10(8), 880–888 (2009).
  • Ferguson SE, Han S, Kelsoe G, Thompson CB. CD28 is required for germinal center formation. J. Immunol.156(12), 4576–4581 (1996).
  • Borriello F, Sethna MP, Boyd SD et al. B7–1 and B7–2 have overlapping, critical roles in immunoglobulin class switching and germinal center formation. Immunity6(3), 303–313 (1997).
  • Cunningham AF, Serre K, Mohr E, Khan M, Toellner K-M. Loss of CD154 impairs the Th2 extrafollicular plasma cell response but not early T cell proliferation and interleukin-4 induction. Immunology113(2), 187–193 (2004).
  • Kawabe T, Naka T, Yoshida K et al. The immune responses in CD40-deficient mice: impaired immunoglobulin class switching and germinal center formation. Immunity1(3), 167–178 (1994).
  • Cannons JL, Qi H, Lu KT et al. Optimal germinal center responses require a multistage T cell:B cell adhesion process involving integrins, SLAM-associated protein, and CD84. Immunity32(2), 253–265 (2010).
  • Caamano JH, Rizzo CA, Durham SK et al. Nuclear factor (NF)-κ B2 (p100/p52) is required for normal splenic microarchitecture and B cell-mediated immune responses. J. Exp. Med.187(2), 185–196 (1998).
  • Weih DS, Yilmaz ZB, Weih F. Essential role of RelB in germinal center and marginal zone formation and proper expression of homing chemokines. J. Immunol.167(4), 1909–1919 (2001).
  • Vora KA, Tumas-Brundage KM, Lentz VM, Cranston A, Fishel R, Manser T. Severe attenuation of the B cell immune response in Msh2-deficient mice. J. Exp. Med.189(3), 471–482 (1999).
  • Kuwahara K, Fujimura S, Takahashi Y et al. Germinal center-associated nuclear protein contributes to affinity maturation of B cell antigen receptor in T cell-dependent responses. Proc. Natl Acad. Sci. USA101(4), 1010–1015 (2004).
  • Thai T-H, Calado DP, Casola S et al. Regulation of the germinal center response by microRNA-155. Science316(5824), 604–608 (2007).

Website

  • Panum PL. Observations made during the epidemic of measles on the Faroe Islands in the year 1846 (translated from Danish). (Delta Omega Honorary Society in Public Health, 1847) www.deltaomega.org/Classics.cfm

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.