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Immunological Investigations
A Journal of Molecular and Cellular Immunology
Volume 50, 2021 - Issue 7
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Review

B Cell Response to Vaccination

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References

  • Abbott RK, Crotty S. 2020. Factors in B cell competition and immunodominance. Immunol Rev. 296(1):120–31.
  • Abbott RK, Lee JH, Menis S, Skog P, Rossi M, Ota T, Kulp DW, Bhullar D, Kalyuzhniy O, Havenar-Daughton C, et al. 2018. Precursor frequency and affinity determine B cell competitive fitness in germinal centers, tested with germline-targeting HIV vaccine immunogens. Immunity. 48(133–146):e136.
  • Ahuja A, Anderson SM, Khalil A, Shlomchik MJ. 2008. Maintenance of the plasma cell pool is independent of memory B cells. Proc Natl Acad Sci U S A. 105(12):4802–07.
  • Akira S, Takeda K, Kaisho T. 2001. Toll-like receptors: critical proteins linking innate and acquired immunity. Nat Immunol. 2(8):675–80.
  • Akram A, Inman RD. 2012. Immunodominance: a pivotal principle in host response to viral infections. Clin Immunol. 143(2):99–115.
  • Allen CD, Cyster JG. 2008. Follicular dendritic cell networks of primary follicles and germinal centers: phenotype and function. Semin Immunol. 20(1):14–25.
  • Allen CD, Okada T, Tang HL, Cyster JG. 2007. Imaging of germinal center selection events during affinity maturation. Science. 315(5811):528–31.
  • Altman MO, Angeletti D, Yewdell JW. 2018. Antibody immunodominance: the key to understanding influenza virus antigenic drift. Viral Immunol. 31(2):142–49.
  • Anderson SM, Khalil A, Uduman M, Hershberg U, Louzoun Y, Haberman AM, Kleinstein SH, Shlomchik MJ. 2009. 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):7314–25.
  • Angeletti D, Gibbs JS, Angel M, Kosik I, Hickman HD, Frank GM, Das SR, Wheatley AK, Prabhakaran M, Leggat DJ, et al. 2017. Defining B cell immunodominance to viruses. Nat Immunol. 18(4):456–63.
  • Arunachalam PS, Charles TP, Joag V, Bollimpelli VS, Scott MKD, Wimmers F, Burton SL, Labranche CC, Petitdemange C, Gangadhara S, et al. 2020. T cell-inducing vaccine durably prevents mucosal SHIV infection even with lower neutralizing antibody titers. Nat Med. 26(6):932–40.
  • Baden LR, El Sahly HM, Essink B, Kotloff K, Frey S, Novak R, Diemert D, Spector SA, Rouphael N, Creech CB, et al. 2021. Efficacy and safety of the mRNA-1273 SARS-CoV-2 vaccine. N Engl J Med. 384(5):403–16.
  • Baumjohann D, Okada T, Ansel KM. 2011. Cutting edge: distinct waves of BCL6 expression during T follicular helper cell development. J Immunol. 187(5):2089–92.
  • Baumjohann D, Preite S, Reboldi A, Ronchi F, Ansel KM, Lanzavecchia A, Sallusto F. 2013. Persistent antigen and germinal center B cells sustain T follicular helper cell responses and phenotype. Immunity. 38(3):596–605.
  • Benson MJ, Dillon SR, Castigli E, Geha RS, Xu S, Lam KP, Noelle RJ. 2008. Cutting edge: the dependence of plasma cells and independence of memory B cells on BAFF and APRIL. J Immunol. 180(6):3655–59.
  • Bergstrom JJ, Xu H, Heyman B. 2017. Epitope-specific suppression of IgG responses by passively administered specific IgG: evidence of epitope masking. Front Immunol. 8:238.
  • Bouteau A, Kervevan J, Su Q, Zurawski SM, Contreras V, Dereuddre-Bosquet N, Le Grand R, Zurawski G, Cardinaud S, Levy Y, et al. 2019. DC subsets regulate humoral immune responses by supporting the differentiation of distinct Tfh cells. Front Immunol. 10:1134.
  • Brynjolfsson SF, Persson Berg L, Olsen Ekerhult T, Rimkute I, Wick MJ, Martensson IL, Grimsholm O. 2018. Long-lived plasma cells in mice and men. Front Immunol. 9:2673.
  • Burnett DL, Langley DB, Schofield P, Hermes JR, Chan TD, Jackson J, Bourne K, Reed JH, Patterson K, Porebski BT, et al. 2018. Germinal center antibody mutation trajectories are determined by rapid self/foreign discrimination. Science. 360(6385):223–26.
  • Cabrita R, Lauss M, Sanna A, Donia M, Skaarup Larsen M, Mitra S, Johansson I, Phung B, Harbst K, Vallon-Christersson J, et al. 2020. Tertiary lymphoid structures improve immunotherapy and survival in melanoma. Nature. 577(7791):561–65.
  • Calado DP, Sasaki Y, Godinho SA, Pellerin A, Kochert K, Sleckman BP, De Alboran IM, Janz M, Rodig S, Rajewsky K. 2012. The cell-cycle regulator c-Myc is essential for the formation and maintenance of germinal centers. Nat Immunol. 13(11):1092–100.
  • Cannons JL, Qi H, Lu KT, Dutta M, Gomez-Rodriguez J, Cheng J, Wakeland EK, Germain RN, Schwartzberg PL. 2010. Optimal germinal center responses require a multistage T cell: B cell adhesion process involving integrins, SLAM-associated protein, and CD84. Immunity. 32(2):253–65.
  • Carroll MC, Isenman DE. 2012. Regulation of humoral immunity by complement. Immunity. 37(2):199–207.
  • Chan TD, Gatto D, Wood K, Camidge T, Basten A, Brink R. 2009. 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):3139–49.
  • Chen M, Hong MJ, Sun H, Wang L, Shi X, Gilbert BE, Corry DB, Kheradmand F, Wang J. 2014. Essential role for autophagy in the maintenance of immunological memory against influenza infection. Nat Med. 20(5):503–10.
  • Chen M, Kodali S, Jang A, Kuai L, Wang J. 2015. Requirement for autophagy in the long-term persistence but not initial formation of memory B cells. J Immunol. 194(6):2607–15.
  • Cirelli KM, Carnathan DG, Nogal B, Martin JT, Rodriguez OL, Upadhyay AA, Enemuo CA, Gebru EH, Choe Y, Viviano F, et al. 2019. Slow delivery immunization enhances HIV neutralizing antibody and germinal center responses via modulation of immunodominance. Cell. 177(5):1153–1171 e1128.
  • Cirelli KM, Crotty S. 2017. Germinal center enhancement by extended antigen availability. Curr Opin Immunol. 47:64–69.
  • Clybouw C, Fischer S, Auffredou MT, Hugues P, Alexia C, Bouillet P, Raphael M, Leca G, Strasser A, Tarlinton DM, et al. 2011. Regulation of memory B-cell survival by the BH3-only protein Puma. Blood. 118(15):4120–28.
  • Coffey F, Alabyev B, Manser T. 2009. Initial clonal expansion of germinal center B cells takes place at the perimeter of follicles. Immunity. 30(4):599–609.
  • Crotty S. 2019. T follicular helper cell biology: a decade of discovery and diseases. Immunity. 50(5):1132–48.
  • Crotty S, Aubert RD, Glidewell J, Ahmed R. 2004. Tracking human antigen-specific memory B cells: a sensitive and generalized ELISPOT system. J Immunol Methods. 286(1–2):111–22.
  • Crotty S, Felgner P, Davies H, Glidewell J, Villarreal L, Ahmed R. 2003. Cutting edge: long-term B cell memory in humans after smallpox vaccination. J Immunol. 171(10):4969–73.
  • D’Souza L, Gupta SL, Bal V, Rath S, George A. 2017. CD73 expression identifies a subset of IgM(+) antigen-experienced cells with memory attributes that is T cell and CD40 signalling dependent. Immunology. 152:602–12.
  • Davis CW, Jackson KJL, McCausland MM, Darce J, Chang C, Linderman SL, Chennareddy C, Gerkin R, Brown SJ, Wrammert J, et al. 2020. Influenza vaccine-induced human bone marrow plasma cells decline within a year after vaccination. Science. 370(6513):237–41.
  • De Silva NS, Simonetti G, Heise N, Klein U. 2012. The diverse roles of IRF4 in late germinal center B-cell differentiation. Immunol Rev. 247(1):73–92.
  • DeFranco AL, Rookhuizen DC, Hou B. 2012. Contribution of Toll-like receptor signaling to germinal center antibody responses. Immunol Rev. 247(1):64–72.
  • Dempsey PW, Allison ME, Akkaraju S, Goodnow CC, Fearon DT. 1996. C3d of complement as a molecular adjuvant: bridging innate and acquired immunity. Science. 271(5247):348–50.
  • Di Niro R, Lee SJ, Vander Heiden JA, Elsner RA, Trivedi N, Bannock JM, Gupta NT, Kleinstein SH, Vigneault F, Gilbert TJ, et al. 2015. Salmonella infection drives promiscuous B cell activation followed by extrafollicular affinity maturation. Immunity. 43(1):120–31.
  • DiLillo DJ, Hamaguchi Y, Ueda Y, Yang K, Uchida J, Haas KM, Kelsoe G, Tedder TF. 2008. Maintenance of long-lived plasma cells and serological memory despite mature and memory B cell depletion during CD20 immunotherapy in mice. J Immunol. 180(1):361–71.
  • Dogan I, Bertocci B, Vilmont V, Delbos F, Megret J, Storck S, Reynaud CA, Weill JC. 2009. Multiple layers of B cell memory with different effector functions. Nat Immunol. 10(12):1292–99.
  • Dominguez-Sola D, Kung J, Holmes AB, Wells VA, Mo T, Basso K, Dalla-Favera R. 2015. The FOXO1 transcription factor instructs the germinal center dark zone program. Immunity. 43(6):1064–74.
  • Dominguez-Sola D, Victora GD, Ying CY, Phan RT, Saito M, Nussenzweig MC, Dalla-Favera R. 2012. The proto-oncogene MYC is required for selection in the germinal center and cyclic reentry. Nat Immunol. 13(11):1083–91.
  • Ellebedy AH, Krammer F, Li GM, Miller MS, Chiu C, Wrammert J, Chang CY, Davis CW, McCausland M, Elbein R, et al. 2014. Induction of broadly cross-reactive antibody responses to the influenza HA stem region following H5N1 vaccination in humans. Proc Natl Acad Sci U S A. 111(36):13133–38.
  • Engels N, Konig LM, Heemann C, Lutz J, Tsubata T, Griep S, Schrader V, Wienands J. 2009. Recruitment of the cytoplasmic adaptor Grb2 to surface IgG and IgE provides antigen receptor-intrinsic costimulation to class-switched B cells. Nat Immunol. 10(9):1018–25.
  • Engels N, Konig LM, Schulze W, Radtke D, Vanshylla K, Lutz J, Winkler TH, Nitschke L, Wienands J. 2014. The immunoglobulin tail tyrosine motif upgrades memory-type BCRs by incorporating a Grb2-Btk signalling module. Nat Commun. 5(1):5456.
  • Ersching J, Efeyan A, Mesin L, Jacobsen JT, Pasqual G, Grabiner BC, Dominguez-Sola D, Sabatini DM, Victora GD. 2017. Germinal center selection and affinity maturation require dynamic regulation of mTORC1 kinase. Immunity. 46(6):1045–1058 e1046.
  • Frank SA. 2002. In immunology and evolution of infectious disease. Princeton (NJ): Princeton University Press. SBN-10: 0-691-09595-7.
  • Gitlin AD, Von Boehmer L, Gazumyan A, Shulman Z, Oliveira TY, Nussenzweig MC. 2016. Independent roles of switching and hypermutation in the development and persistence of B lymphocyte memory. Immunity. 44(4):769–81.
  • Goenka R, Barnett LG, Silver JS, O’Neill PJ, Hunter CA, Cancro MP, Laufer TM. 2011. Cutting edge: dendritic cell-restricted antigen presentation initiates the follicular helper T cell program but cannot complete ultimate effector differentiation. J Immunol. 187(3):1091–95.
  • Hauser AE, Junt T, Mempel TR, Sneddon MW, Kleinstein SH, Henrickson SE, Von Andrian UH, Shlomchik MJ, Haberman AM. 2007. Definition of germinal-center B cell migration in vivo reveals predominant intrazonal circulation patterns. Immunity. 26:655–67.
  • Havenar-Daughton C, Sarkar A, Kulp DW, Toy L, Hu X, Deresa I, Kalyuzhniy O, Kaushik K, Upadhyay AA, Menis S, et al. 2018. The human naive B cell repertoire contains distinct subclasses for a germline-targeting HIV-1 vaccine immunogen. Sci Transl Med. 10:eaat0381.
  • He JS, Subramaniam S, Narang V, Srinivasan K, Saunders SP, Carbajo D, Wen-Shan T, Hidayah Hamadee N, Lum J, Lee A, et al. 2017. IgG1 memory B cells keep the memory of IgE responses. Nat Commun. 8(1):641.
  • Helmink BA, Reddy SM, Gao J, Zhang S, Basar R, Thakur R, Yizhak K, Sade-Feldman M, Blando J, Han G, et al. 2020. B cells and tertiary lymphoid structures promote immunotherapy response. Nature. 577(7791):549–55.
  • Henry C, Palm AE, Krammer F, Wilson PC. 2018. From original antigenic sin to the universal influenza virus vaccine. Trends Immunol. 39(1):70–79.
  • Hofer T, Muehlinghaus G, Moser K, Yoshida T, Hebel K, Hauser A, Hoyer B, Dorner T, O’ Luger E, Dörner T, et al. 2006. Adaptation of humoral memory. Immunol Rev. 211:295–302.
  • Hong S, Zhang Z, Liu H, Tian M, Zhu X, Zhang Z, Wang W, Zhou X, Zhang F, Ge Q, et al. 2018. B cells are the dominant antigen-presenting cells that activate naive CD4(+) T cells upon immunization with a virus-derived nanoparticle antigen. Immunity. 49(4):695–708 e694.
  • Hou B, Saudan P, Ott G, Wheeler ML, Ji M, Kuzmich L, Lee LM, Coffman RL, Bachmann MF, DeFranco AL. 2011. Selective utilization of toll-like receptor and MyD88 signaling in B cells for enhancement of the antiviral germinal center response. Immunity. 34(3):375–84.
  • Huang D, Abbott RK, Havenar-Daughton C, Skog PD, Al-Kolla R, Groschel B, Blane TR, Menis S, Tran JT, Thinnes TC, et al. 2020. B cells expressing authentic naive human VRC01-class BCRs can be recruited to germinal centers and affinity mature in multiple independent mouse models. Proc Natl Acad Sci U S A. 117(37):22920–31.
  • Ise W, Fujii K, Shiroguchi K, Ito A, Kometani K, Takeda K, Kawakami E, Yamashita K, Suzuki K, Okada T, et al. 2018. T follicular helper cell-germinal center B cell interaction strength regulates entry into plasma cell or recycling germinal center cell fate. Immunity. 48(4):702–715 e704.
  • Jardine J, Julien JP, Menis S, Ota T, Kalyuzhniy O, McGuire A, Sok D, Huang PS, MacPherson S, Jones M, et al. 2013. Rational HIV immunogen design to target specific germline B cell receptors. Science. 340(6133):711–16.
  • Jardine JG, Kulp DW, Havenar-Daughton C, Sarkar A, Briney B, Sok D, Sesterhenn F, Ereno-Orbea J, Kalyuzhniy O, Deresa I, et al. 2016. HIV-1 broadly neutralizing antibody precursor B cells revealed by germline-targeting immunogen. Science. 351(6280):1458–63.
  • Jenks SA, Cashman KS, Woodruff MC, Lee FE, Sanz I. 2019. Extrafollicular responses in humans and SLE. Immunol Rev. 288:136–48.
  • Jones DD, Wilmore JR, Allman D. 2015. Cellular dynamics of memory B cell populations: igM+ and IgG+ memory B cells persist indefinitely as quiescent cells. J Immunol. 195(10):4753–59.
  • Kallies A, Hasbold J, Tarlinton DM, Dietrich W, Corcoran LM, Hodgkin PD, Nutt SL. 2004. Plasma cell ontogeny defined by quantitative changes in blimp-1 expression. J Exp Med. 200:967–77.
  • Kasturi SP, Rasheed MAU, Havenar-Daughton C, Pham M, Legere T, Sher ZJ, Kovalenkov Y, Gumber S, Huang JY, Gottardo R, et al. 2020. 3M-052, a synthetic TLR-7/8 agonist, induces durable HIV-1 envelope-specific plasma cells and humoral immunity in nonhuman primates. Sci Immunol. 5(48):eabb1025.
  • Kasturi SP, Skountzou I, Albrecht RA, Koutsonanos D, Hua T, Nakaya HI, Ravindran R, Stewart S, Alam M, Kwissa M, et al. 2011. Programming the magnitude and persistence of antibody responses with innate immunity. Nature. 470(7335):543–47.
  • Kato Y, Abbott RK, Freeman BL, Haupt S, Groschel B, Silva M, Menis S, Irvine DJ, Schief WR, Crotty S. 2020. Multifaceted effects of antigen valency on B cell response composition and differentiation in vivo. Immunity. 53(3):548–563 e548.
  • Khodadadi L, Cheng Q, Radbruch A, Hiepe F. 2019. The maintenance of memory plasma cells. Front Immunol. 10:721.
  • Kim YM, Pan JY, Korbel GA, Peperzak V, Boes M, Ploegh HL. 2006. Monovalent ligation of the B cell receptor induces receptor activation but fails to promote antigen presentation. Proc Natl Acad Sci U S A. 103(9):3327–32.
  • Klein U, Casola S, Cattoretti G, Shen Q, Lia M, Mo T, Ludwig T, Rajewsky K, Dalla-Favera R. 2006. Transcription factor IRF4 controls plasma cell differentiation and class-switch recombination. Nat Immunol. 7(7):773–82.
  • Koike T, Harada K, Horiuchi S, Kitamura D. 2019. The quantity of CD40 signaling determines the differentiation of B cells into functionally distinct memory cell subsets. Elife. 8:e44245.
  • Krammer F, Palese P. 2015. Advances in the development of influenza virus vaccines. Nat Rev Drug Discov. 14:167–82.
  • Krautler NJ, Suan D, Butt D, Bourne K, Hermes JR, Chan TD, Sundling C, Kaplan W, Schofield P, Jackson J, et al. 2017. Differentiation of germinal center B cells into plasma cells is initiated by high-affinity antigen and completed by Tfh cells. J Exp Med. 214(5):1259–67.
  • Krishnaswamy JK, Alsen S, Yrlid U, Eisenbarth SC, Williams A. 2018. Determination of T follicular helper cell fate by dendritic cells. Front Immunol. 9:2169.
  • Krishnaswamy JK, Gowthaman U, Zhang B, Mattsson J, Szeponik L, Liu D, Wu R, White T, Calabro S, Xu L, et al. 2017. Migratory CD11b(+) conventional dendritic cells induce T follicular helper cell-dependent antibody responses. Sci Immunol:2(18):eaam9169.
  • Kuraoka M, Schmidt AG, Nojima T, Feng F, Watanabe A, Kitamura D, Harrison SC, Kepler TB, Kelsoe G. 2016. Complex antigens drive permissive clonal selection in germinal centers. Immunity. 44(3):542–52.
  • Laidlaw BJ, Schmidt TH, Green JA, Allen CD, Okada T, Cyster JG. 2017. The Eph-related tyrosine kinase ligand Ephrin-B1 marks germinal center and memory precursor B cells. J Exp Med. 214(3):639–49.
  • Lam WY, Becker AM, Kennerly KM, Wong R, Curtis JD, Llufrio EM, McCommis KS, Fahrmann J, Pizzato HA, Nunley RM, et al. 2016. Mitochondrial pyruvate import promotes long-term survival of antibody-secreting plasma cells. Immunity. 45(1):60–73.
  • Lam WY, Jash A, Yao CH, D’Souza L, Wong R, Nunley RM, Meares GP, Patti GJ, Bhattacharya D. 2018. Metabolic and transcriptional modules independently diversify plasma cell lifespan and function. Cell Rep. 24(9):2479–2492 e2476.
  • Lederer K, Castano D, Gomez Atria D, Oguin TH 3rd, Wang S, Manzoni TB, Muramatsu H, Hogan MJ, Amanat F, Cherubin P, et al. 2020. SARS-CoV-2 mRNA vaccines foster potent antigen-specific germinal center responses associated with neutralizing antibody generation. Immunity. 53(6):1281–1295 e1285.
  • Lee SK, Rigby RJ, Zotos D, Tsai LM, Kawamoto S, Marshall JL, Ramiscal RR, Chan TD, Gatto D, Brink R, et al. 2011. B cell priming for extrafollicular antibody responses requires Bcl-6 expression by T cells. J Exp Med. 208(7):1377–88.
  • Li GM, Chiu C, Wrammert J, McCausland M, Andrews SF, Zheng NY, Lee JH, Huang M, Qu X, Edupuganti S, et al. 2012. Pandemic H1N1 influenza vaccine induces a recall response in humans that favors broadly cross-reactive memory B cells. Proc Natl Acad Sci U S A. 109(23):9047–52.
  • Lingwood D, McTamney PM, Yassine HM, Whittle JR, Guo X, Boyington JC, Wei CJ, Nabel GJ. 2012. Structural and genetic basis for development of broadly neutralizing influenza antibodies. Nature. 489(7417):566–70.
  • Liu D, Xu H, Shih C, Wan Z, Ma X, Ma W, Luo D, Qi H. 2015. T-B-cell entanglement and ICOSL-driven feed-forward regulation of germinal centre reaction. Nature. 517(7533):214–18.
  • Liu YJ, Mason DY, Johnson GD, Abbot S, Gregory CD, Hardie DL, Gordon J, MacLennan IC. 1991. Germinal center cells express bcl-2 protein after activation by signals which prevent their entry into apoptosis. Eur J Immunol. 21(8):1905–10.
  • Luo W, Hawse W, Conter L, Trivedi N, Weisel F, Wikenheiser D, Cattley RT, Shlomchik MJ. 2019. The AKT kinase signaling network is rewired by PTEN to control proximal BCR signaling in germinal center B cells. Nat Immunol. 20(6):736–46.
  • Luo W, Weisel F, Shlomchik MJ. 2018. B cell receptor and CD40 signaling are rewired for synergistic induction of the c-Myc transcription factor in germinal center B cells. Immunity. 48(2):313–326 e315.
  • Lutz J, Dittmann K, Bosl MR, Winkler TH, Wienands J, Engels N. 2015. Reactivation of IgG-switched memory B cells by BCR-intrinsic signal amplification promotes IgG antibody production. Nat Commun. 6(1):8575.
  • Martin JT, Cottrell CA, Antanasijevic A, Carnathan DG, Cossette BJ, Enemuo CA, Gebru EH, Choe Y, Viviano F, Fischinger S, et al. 2020. Targeting HIV Env immunogens to B cell follicles in nonhuman primates through immune complex or protein nanoparticle formulations. NPJ Vaccines. 5(1):72.
  • Martin SW, Goodnow CC. 2002. Burst-enhancing role of the IgG membrane tail as a molecular determinant of memory. Nat Immunol. 3(2):182–88.
  • Maruyama M, Lam KP, Rajewsky K. 2000. Memory B-cell persistence is independent of persisting immunizing antigen. Nature. 407(6804):636–42.
  • Mayer CT, Gazumyan A, Kara EE, Gitlin AD, Golijanin J, Viant C, Pai J, Oliveira TY, Wang Q, Escolano A, et al. 2017. The microanatomic segregation of selection by apoptosis in the germinal center. Science. 358(6360):eaao2602.
  • Mesin L, Schiepers A, Ersching J, Barbulescu A, Cavazzoni CB, Angelini A, Okada T, Kurosaki T, Victora GD. 2020. Restricted clonality and limited germinal center reentry characterize memory B cell reactivation by boosting. Cell. 180(1):92–106 e111.
  • Mikell I, Sather DN, Kalams SA, Altfeld M, Alter G, Stamatatos L. 2011. Characteristics of the earliest cross-neutralizing antibody response to HIV-1. PLoS Pathog. 7(1):e1001251.
  • Mishra AK, Mariuzza RA. 2018. Insights into the structural basis of antibody affinity maturation from next-generation sequencing. Front Immunol. 9:117.
  • Nachbagauer R, Choi A, Izikson R, Cox MM, Palese P, Krammer F. 2016. Age dependence and Isotype specificity of influenza virus hemagglutinin stalk-reactive antibodies in humans. mBio. 7(1):e01996–01915.
  • Ochiai K, Maienschein-Cline M, Simonetti G, Chen J, Rosenthal R, Brink R, Chong AS, Klein U, Dinner AR, Singh H, et al. 2013. Transcriptional regulation of germinal center B and plasma cell fates by dynamical control of IRF4. Immunity. 38(5):918–29.
  • Ols S, Yang L, Thompson EA, Pushparaj P, Tran K, Liang F, Lin A, Eriksson B, Karlsson Hedestam GB, Wyatt RT, et al. 2020. Route of vaccine administration alters antigen trafficking but not innate or adaptive immunity. Cell Rep. 30(12):3964–3971 e3967.
  • Palm AE, Henry C. 2019. Remembrance of things past: long-term B cell memory after infection and vaccination. Front Immunol. 10:1787.
  • 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(6021):1203–07.
  • Pardi N, Hogan MJ, Naradikian MS, Parkhouse K, Cain DW, Jones L, Moody MA, Verkerke HP, Myles A, Willis E, et al. 2018. Nucleoside-modified mRNA vaccines induce potent T follicular helper and germinal center B cell responses. J Exp Med. 215(6):1571–88.
  • Pardi N, Tuyishime S, Muramatsu H, Kariko K, Mui BL, Tam YK, Madden TD, Hope MJ, Weissman D. 2015. Expression kinetics of nucleoside-modified mRNA delivered in lipid nanoparticles to mice by various routes. J Control Release. 217:345–51.
  • Park JK, Xiao Y, Ramuta MD, Rosas LA, Fong S, Matthews AM, Freeman AD, Gouzoulis MA, Batchenkova NA, Yang X, et al. 2020. Pre-existing immunity to influenza virus hemagglutinin stalk might drive selection for antibody-escape mutant viruses in a human challenge model. Nat Med. 26(8):1240–46.
  • Pauli NT, Henry Dunand CJ, Wilson PC. 2011. Exploiting human memory B cell heterogeneity for improved vaccine efficacy. Front Immunol. 2:77.
  • Paus D, Phan TG, Chan TD, Gardam S, Basten A, Brink R. 2006. Antigen recognition strength regulates the choice between extrafollicular plasma cell and germinal center B cell differentiation. J Exp Med. 203(4):1081–91.
  • Pereira JP, Kelly LM, Cyster JG. 2010. Finding the right niche: B-cell migration in the early phases of T-dependent antibody responses. Int Immunol. 22(6):413–19.
  • Petitprez F, De Reynies A, Keung EZ, Chen TW, Sun CM, Calderaro J, Jeng YM, Hsiao LP, Lacroix L, Bougouin A, et al. 2020. B cells are associated with survival and immunotherapy response in sarcoma. Nature. 577(7791):556–60.
  • Phan TG, Paus D, Chan TD, Turner ML, Nutt SL, Basten A, Brink R. 2006. High affinity germinal center B cells are actively selected into the plasma cell compartment. J Exp Med. 203(11):2419–24.
  • Pinna D, Corti D, Jarrossay D, Sallusto F, Lanzavecchia A. 2009. Clonal dissection of the human memory B-cell repertoire following infection and vaccination. Eur J Immunol. 39(5):1260–70.
  • Poholek AC, Hansen K, Hernandez SG, Eto D, Chandele A, Weinstein JS, Dong X, Odegard JM, Kaech SM, Dent AL, et al. 2010. In vivo regulation of Bcl6 and T follicular helper cell development. J Immunol. 185(1):313–26.
  • Polack FP, Thomas SJ, Kitchin N, Absalon J, Gurtman A, Lockhart S, Perez JL, Perez Marc G, Moreira ED, Zerbini C, et al. 2020. Safety and efficacy of the BNT162b2 mRNA Covid-19 vaccine. N Engl J Med. 383:2603–15.
  • Pulendran B, Ahmed R. 2006. Translating innate immunity into immunological memory: implications for vaccine development. Cell. 124(4):849–63.
  • Reddy ST, Van der Vlies AJ, Simeoni E, Angeli V, Randolph GJ, O’Neil CP, Lee LK, Swartz MA, Hubbell JA. 2007. Exploiting lymphatic transport and complement activation in nanoparticle vaccines. Nat Biotechnol. 25(10):1159–64.
  • Reed JH, Jackson J, Christ D, Goodnow CC. 2016. Clonal redemption of autoantibodies by somatic hypermutation away from self-reactivity during human immunization. J Exp Med. 213(7):1255–65.
  • Roth GA, Gale EC, Alcantara-Hernandez M, Luo W, Axpe E, Verma R, Yin Q, Yu AC, Lopez Hernandez H, Maikawa CL, et al. 2020. Injectable hydrogels for sustained codelivery of subunit vaccines enhance humoral immunity. ACS Cent Sci. 6(10):1800–12.
  • Sander S, Chu VT, Yasuda T, Franklin A, Graf R, Calado DP, Li S, Imami K, Selbach M, Di Virgilio M, et al. 2015. PI3 kinase and FOXO1 transcription factor activity differentially control B cells in the germinal center light and dark zones. Immunity. 43(6):1075–86.
  • Sangster MY, Baer J, Santiago FW, Fitzgerald T, Ilyushina NA, Sundararajan A, Henn AD, Krammer F, Yang H, Luke CJ, et al. 2013. B cell response and hemagglutinin stalk-reactive antibody production in different age cohorts following 2009 H1N1 influenza virus vaccination. Clin Vaccine Immunol. 20(6):867–76.
  • Sather DN, Armann J, Ching LK, Mavrantoni A, Sellhorn G, Caldwell Z, Yu X, Wood B, Self S, Kalams S, et al. 2009. Factors associated with the development of cross-reactive neutralizing antibodies during human immunodeficiency virus type 1 infection. J Virol. 83(2):757–69.
  • Schittek B, Rajewsky K. 1990. Maintenance of B-cell memory by long-lived cells generated from proliferating precursors. Nature. 346(6286):749–51.
  • Scholz JL, Crowley JE, Tomayko MM, Steinel N, O’Neill PJ, Quinn WJ 3rd, Goenka R, Miller JP, Cho YH, Long V, et al. 2008. BLyS inhibition eliminates primary B cells but leaves natural and acquired humoral immunity intact. Proc Natl Acad Sci U S A. 105(40):15517–22.
  • Schroeder KM, Agazio A, Torres RM. 2017. Immunological tolerance as a barrier to protective HIV humoral immunity. Curr Opin Immunol. 47:26–34.
  • Schwickert TA, Victora GD, Fooksman DR, Kamphorst AO, Mugnier MR, Gitlin AD, Dustin ML, Nussenzweig MC. 2011. A dynamic T cell-limited checkpoint regulates affinity-dependent B cell entry into the germinal center. J Exp Med. 208(6):1243–52.
  • Shi W, Liao Y, Willis SN, Taubenheim N, Inouye M, Tarlinton DM, Smyth GK, Hodgkin PD, Nutt SL, Corcoran LM. 2015. Transcriptional profiling of mouse B cell terminal differentiation defines a signature for antibody-secreting plasma cells. Nat Immunol. 16(6):663–73.
  • Shinnakasu R, Inoue T, Kometani K, Moriyama S, Adachi Y, Nakayama M, Takahashi Y, Fukuyama H, Okada T, Kurosaki T. 2016. Regulated selection of germinal-center cells into the memory B cell compartment. Nat Immunol. 17(7):861–69.
  • Shlomchik MJ, Luo W, Weisel F. 2019. Linking signaling and selection in the germinal center. Immunol Rev. 288(1):49–63.
  • Shlomchik MJ, Weisel F. 2012. Germinal center selection and the development of memory B and plasma cells. Immunol Rev. 247(1):52–63.
  • Smirnov D, Schmidt JJ, Capecchi JT, Wightman PD. 2011. Vaccine adjuvant activity of 3M-052: an imidazoquinoline designed for local activity without systemic cytokine induction. Vaccine. 29(33):5434–42.
  • Suan D, Krautler NJ, Maag JLV, Butt D, Bourne K, Hermes JR, Avery DT, Young C, Statham A, Elliott M, et al. 2017. CCR6 defines memory B cell precursors in mouse and human germinal centers, revealing light-zone location and predominant low antigen affinity. Immunity. 47(6):1142–1153 e1144.
  • Sweet RA, Ols ML, Cullen JL, Milam AV, Yagita H, Shlomchik MJ. 2011. Facultative role for T cells in extrafollicular toll-like receptor-dependent autoreactive B-cell responses in vivo. Proc Natl Acad Sci U S A. 108(19):7932–37.
  • Tam HH, Melo MB, Kang M, Pelet JM, Ruda VM, Foley MH, Hu JK, Kumari S, Crampton J, Baldeon AD, et al. 2016. Sustained antigen availability during germinal center initiation enhances antibody responses to vaccination. Proc Natl Acad Sci U S A. 113(43):E6639–E6648.
  • Tas JM, Mesin L, Pasqual G, Targ S, Jacobsen JT, Mano YM, Chen CS, Weill JC, Reynaud CA, Browne EP, et al. 2016. Visualizing antibody affinity maturation in germinal centers. Science. 351(6277):1048–54.
  • Taylor JJ, Pape KA, Jenkins MK. 2012. A germinal center-independent pathway generates unswitched memory B cells early in the primary response. J Exp Med. 209(3):597–606.
  • Tisoncik JR, Korth MJ, Simmons CP, Farrar J, Martin TR, Katze MG. 2012. Into the eye of the cytokine storm. Microbiol Mol Biol Rev. 76(1):16–32.
  • Tokatlian T, Read BJ, Jones CA, Kulp DW, Menis S, Chang JYH, Steichen JM, Kumari S, Allen JD, Dane EL, et al. 2019. Innate immune recognition of glycans targets HIV nanoparticle immunogens to germinal centers. Science. 363(6427):649–54.
  • Tomayko MM, Steinel NC, Anderson SM, Shlomchik MJ. 2010. Cutting edge: hierarchy of maturity of murine memory B cell subsets. J Immunol. 185(12):7146–50.
  • Turner JS, Zhou JQ, Han J, Schmitz AJ, Rizk AA, Alsoussi WB, Lei T, Amor M, McIntire KM, Meade P, et al. 2020. Human germinal centres engage memory and naive B cells after influenza vaccination. Nature. 586(7827):127–32.
  • Viant C, Weymar GHJ, Escolano A, Chen S, Hartweger H, Cipolla M, Gazumyan A, Nussenzweig MC. 2020. Antibody affinity shapes the choice between memory and germinal center B cell fates. Cell. 183(5):1298–311.
  • Victora GD, Schwickert TA, Fooksman DR, Kamphorst AO, Meyer-Hermann M, Dustin ML, Nussenzweig MC. 2010. Germinal center dynamics revealed by multiphoton microscopy with a photoactivatable fluorescent reporter. Cell. 143(4):592–605.
  • Weisel F, Shlomchik M. 2017. Memory B cells of mice and humans. Annu Rev Immunol. 35(1):255–84.
  • Weisel FJ, Mullett SJ, Elsner RA, Menk AV, Trivedi N, Luo W, Wikenheiser D, Hawse WF, Chikina M, Smita S, et al. 2020. Germinal center B cells selectively oxidize fatty acids for energy while conducting minimal glycolysis. Nat Immunol. 21(3):331–42.
  • Weisel FJ, Zuccarino-Catania GV, Chikina M, Shlomchik MJ. 2016. A temporal switch in the germinal center determines differential output of memory B and plasma cells. Immunity. 44(1):116–30.
  • Widge AT, Rouphael NG, Jackson LA, Anderson EJ, Roberts PC, Makhene M, Chappell JD, Denison MR, Stevens LJ, Pruijssers AJ. 2021. Durability of responses after SARS-CoV-2 mRNA-1273 vaccination. N Engl J Med. 384(1):80–82.
  • Willis SN, Good-Jacobson KL, Curtis J, Light A, Tellier J, Shi W, Smyth GK, Tarlinton DM, Belz GT, Corcoran LM, et al. 2014. Transcription factor IRF4 regulates germinal center cell formation through a B cell-intrinsic mechanism. J Immunol. 192(7):3200–06.
  • Woodruff MC, Ramonell RP, Nguyen DC, Cashman KS, Saini AS, Haddad NS, Ley AM, Kyu S, Howell JC, Ozturk T, et al. 2020. Extrafollicular B cell responses correlate with neutralizing antibodies and morbidity in COVID-19. Nat Immunol. 21(12):1506–16.
  • Wrammert J, Koutsonanos D, Li GM, Edupuganti S, Sui J, Morrissey M, McCausland M, Skountzou I, Hornig M, Lipkin WI, et al. 2011. Broadly cross-reactive antibodies dominate the human B cell response against 2009 pandemic H1N1 influenza virus infection. J Exp Med. 208:181–93.
  • Wu NC, Thompson AJ, Lee JM, Su W, Arlian BM, Xie J, Lerner RA, Yen HL, Bloom JD, Wilson IA. 2020. Different genetic barriers for resistance to HA stem antibodies in influenza H3 and H1 viruses. Science. 368(6497):1335–40.
  • Xu H, Chaudhri VK, Wu Z, Biliouris K, Dienger-Stambaugh K, Rochman Y, Singh H. 2015. Regulation of bifurcating B cell trajectories by mutual antagonism between transcription factors IRF4 and IRF8. Nat Immunol. 16(12):1274–81.
  • Xu H, Zhang L, Heyman B. 2018. IgG-mediated immune suppression in mice is epitope specific except during high epitope density conditions. Sci Rep. 8(1):15292.
  • Yu X, Tsibane T, McGraw PA, House FS, Keefer CJ, Hicar MD, Tumpey TM, Pappas C, Perrone LA, Martinez O, et al. 2008. Neutralizing antibodies derived from the B cells of 1918 influenza pandemic survivors. Nature. 455:532–36.
  • Zhang A, Stacey HD, Mullarkey CE, Miller MS. 2019. Original antigenic sin: how first exposure shapes lifelong anti-influenza virus immune responses. J Immunol. 202(2):335–40.
  • Zhang Y, Tech L, George LA, Acs A, Durrett RE, Hess H, Walker LSK, Tarlinton DM, Fletcher AL, Hauser AE, et al. 2018. Plasma cell output from germinal centers is regulated by signals from Tfh and stromal cells. J Exp Med. 215(4):1227–43.
  • Zhao Z, Hu Y, Harmon T, Pentel P, Ehrich M, Zhang C. 2019. Effect of adjuvant release rate on the immunogenicity of nanoparticle-based vaccines: a case study with a nanoparticle-based nicotine vaccine. Mol Pharm. 16(6):2766–75.
  • Zinkernagel RM, Hengartner H, Yu X, Tsibane T, McGraw PA, House FS, Keefer CJ, Hicar MD, Tumpey TM, Pappas C, et al. 2006. Protective ‘immunity’ by pre-existent neutralizing antibody titers and preactivated T cells but not by so-called ‘immunological memory’. Immunol Rev. 211(1):310–19.
  • Zost SJ, Wu NC, Hensley SE, Wilson IA. 2019. Immunodominance and antigenic variation of influenza virus hemagglutinin: implications for design of universal vaccine immunogens. J Infect Dis. 219(Supplement_1):S38–S45.
  • Zuccarino-Catania GV, Sadanand S, Weisel FJ, Tomayko MM, Meng H, Kleinstein SH, Good-Jacobson KL, Shlomchik MJ. 2014. CD80 and PD-L2 define functionally distinct memory B cell subsets that are independent of antibody isotype. Nat Immunol. 15:631–37.

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