383
Views
8
CrossRef citations to date
0
Altmetric
Review

Memory Generation and Re-Activation in Food Allergy

ORCID Icon, , , , ORCID Icon &
Pages 171-184 | Published online: 09 Jun 2021

References

  • Tritle LA. A New History of the Peloponnesian War. Wiley Online Library; 2010.
  • Bruton K, Koenig JFE, Phelps A, Jordana M. Perturbations to homeostasis in experimental models revealed innate pathways driving food allergy. Front Immunol. 2020;11:603272. doi:10.3389/fimmu.2020.603272
  • Florsheim EB, Sullivan ZA, Khoury-Hanold W, Medzhitov R. Food allergy as a biological food quality control system. Cell. 2021;184(6):1440–1454. doi:10.1016/j.cell.2020.12.007
  • Savage J, Sicherer S, Wood R. The natural history of food allergy. J Allergy Clin Immunol Pract. 2016;4(2):196–203; quiz 204. doi:10.1016/j.jaip.2015.11.024
  • Jiménez-Saiz R, Chu DK, Waserman S, Jordana M. Initiation, persistence and exacerbation of food allergy. In: Schmidt-Weber CB, editor. Allergy Prevention and Exacerbation. Cham: Springer International Publishing; 2017:121–144.
  • Amanna IJ, Carlson NE, Slifka MK. Duration of humoral immunity to common viral and vaccine antigens. N Engl J Med. 2007;357(19):1903–1915. doi:10.1056/NEJMoa066092
  • Winter O, Dame C, Jundt F, Hiepe F. Pathogenic long-lived plasma cells and their survival niches in autoimmunity, malignancy, and allergy. J Immunol. 2012;189(11):5105–5111. doi:10.4049/jimmunol.1202317
  • Luger EO, Wegmann M, Achatz G, Worm M, Renz H, Radbruch A. Allergy for a lifetime? Allergol Int. 2010;59(1):1–8. doi:10.2332/allergolint.10-RAI-0175
  • Jimenez-Saiz R, Bruton K, Koenig JFE, Waserman S, Jordana M. The IgE memory reservoir in food allergy. J Allergy Clin Immunol. 2018;142(5):1441–1443. doi:10.1016/j.jaci.2018.08.029
  • Carballeda-Sangiao N, Rodriguez-Mahillo AI, Careche M, Navas A, Moneo I, Gonzalez-Munoz M. Changes over time in IgE sensitization to allergens of the fish parasite Anisakis spp. PLoS Negl Trop Dis. 2016;10(7):e0004864. doi:10.1371/journal.pntd.0004864
  • Kim MS, Straesser MD, Keshavarz B, et al. IgE to galactose-alpha-1,3-galactose wanes over time in patients who avoid tick bites. J Allergy Clin Immunol Pract. 2020;8(1):364–367 e362. doi:10.1016/j.jaip.2019.08.045
  • Jimenez-Saiz R, Chu DK, Mandur TS, et al. Lifelong memory responses perpetuate humoral TH2 immunity and anaphylaxis in food allergy. J Allergy Clin Immunol. 2017;140(6):1604–1615 e1605. doi:10.1016/j.jaci.2017.01.018
  • Bernasconi NL, Traggiai E, Lanzavecchia A. Maintenance of serological memory by polyclonal activation of human memory B cells. Science. 2002;298(5601):2199–2202. doi:10.1126/science.1076071
  • Jimenez-Saiz R, Ellenbogen Y, Koenig JFE, et al. IgG1(+) B-cell immunity predates IgE responses in epicutaneous sensitization to foods. Allergy. 2019;74(1):165–175. doi:10.1111/all.13481
  • Asrat S, Kaur N, Liu X, et al. Chronic allergen exposure drives accumulation of long-lived IgE plasma cells in the bone marrow, giving rise to serological memory. Sci Immunol. 2020;5(43):eaav8402. doi:10.1126/sciimmunol.aav8402
  • Jimenez-Saiz R, Ellenbogen Y, Bruton K, et al. Human BCR analysis of single-sorted, putative IgE(+) memory B cells in food allergy. J Allergy Clin Immunol. 2019;144(1):336–339 e336. doi:10.1016/j.jaci.2019.04.001
  • Looney TJ, Lee JY, Roskin KM, et al. Human B-cell isotype switching origins of IgE. J Allergy Clin Immunol. 2016;137(2):579–586 e577. doi:10.1016/j.jaci.2015.07.014
  • He JS, Subramaniam S, Narang V, et al. IgG1 memory B cells keep the memory of IgE responses. Nat Commun. 2017;8(1):641. doi:10.1038/s41467-017-00723-0
  • Turqueti-Neves A, Otte M, Schwartz C, et al. The extracellular domains of IgG1 and T cell-derived IL-4/IL-13 are critical for the polyclonal memory IgE response in vivo. PLoS Biol. 2015;13(11):e1002290. doi:10.1371/journal.pbio.1002290
  • Bruton K, Spill P, Vohra S, et al. Interrupting reactivation of immunologic memory diverts the allergic response and prevents anaphylaxis. J Allergy Clin Immunol. 2020. doi:10.1016/j.jaci.2020.11.042
  • Prussin C, Lee J, Foster B. Eosinophilic gastrointestinal disease and peanut allergy are alternatively associated with IL-5+ and IL-5(-) T(H)2 responses. J Allergy Clin Immunol. 2009;124(6):1326–1332 e1326. doi:10.1016/j.jaci.2009.09.048
  • DeLong JH, Simpson KH, Wambre E, James EA, Robinson D, Kwok WW. Ara h 1-reactive T cells in individuals with peanut allergy. J Allergy Clin Immunol. 2011;127(5):1211–1218 e1213. doi:10.1016/j.jaci.2011.02.028
  • Patil SU, Ogunniyi AO, Calatroni A, et al. Peanut oral immunotherapy transiently expands circulating Ara h 2-specific B cells with a homologous repertoire in unrelated subjects. J Allergy Clin Immunol. 2015;136(1):125–134 e112. doi:10.1016/j.jaci.2015.03.026
  • Hoh RA, Joshi SA, Lee JY, et al. Origins and clonal convergence of gastrointestinal IgE(+) B cells in human peanut allergy. Sci Immunol. 2020;5(45):eaay4209. doi:10.1126/sciimmunol.aay4209
  • Soleto-Fernandez I, Jimenez-Saiz R, Carrasco YR. Enlightening human B-cell diversity. Allergy. 2020. doi:10.1111/all.14685
  • Glass DR, Tsai AG, Oliveria JP, et al. An Integrated Multi-omic Single-Cell Atlas of Human B Cell Identity. Immunity. 2020;53(1):217–232 e215. doi:10.1016/j.immuni.2020.06.013
  • Jimenez-Saiz R, Molina E, Lopez-Exposito I. Peanut allergy: allergens and etiology. In: Lopez-Exposito I, Blazquez AB, editors. Peanuts: Bioactivities and Allergies. NOVA; 2013:137–152.
  • Hemmings O, Du Toit G, Radulovic S, Lack G, Santos AF. Ara h 2 is the dominant peanut allergen despite similarities with Ara h 6. J Allergy Clin Immunol. 2020;146(3):621–630 e625. doi:10.1016/j.jaci.2020.03.026
  • Hoh RA, Joshi SA, Liu Y, et al. Single B-cell deconvolution of peanut-specific antibody responses in allergic patients. J Allergy Clin Immunol. 2016;137(1):157–167. doi:10.1016/j.jaci.2015.05.029
  • Croote D, Darmanis S, Nadeau KC, Quake SR. High-affinity allergen-specific human antibodies cloned from single IgE B cell transcriptomes. Science. 2018;362(6420):1306–1309. doi:10.1126/science.aau2599
  • Levin M, King JJ, Glanville J, et al. Persistence and evolution of allergen-specific IgE repertoires during subcutaneous specific immunotherapy. J Allergy Clin Immunol. 2016;137(5):1535–1544. doi:10.1016/j.jaci.2015.09.027
  • Ehlers A, den Hartog Jager C, Knulst A, Otten H. Distinction between peanut allergy and tolerance by characterization of B-cell receptor repertoires. Authorea Preprints. 2020.
  • Dolton G, Tungatt K, Lloyd A, et al. More tricks with tetramers: a practical guide to staining T cells with peptide-MHC multimers. Immunology. 2015;146(1):11–22. doi:10.1111/imm.12499
  • Pascal M, Konstantinou GN, Masilamani M, Lieberman J, Sampson HA. In silico prediction of Ara h 2 T cell epitopes in peanut-allergic children. Clin Exp Allergy. 2013;43(1):116–127. doi:10.1111/cea.12014
  • Novak EJ, Liu AW, Gebe JA, et al. Tetramer-guided epitope mapping: rapid identification and characterization of immunodominant CD4+ T cell epitopes from complex antigens. J Immunol. 2001;166(11):6665–6670. doi:10.4049/jimmunol.166.11.6665
  • Chattopadhyay PK, Yu J, Roederer M. Live-cell assay to detect antigen-specific CD4+ T-cell responses by CD154 expression. Nat Protoc. 2006;1(1):1–6. doi:10.1038/nprot.2006.1
  • Ruiter B, Smith NP, Monian B, et al. Expansion of the CD4(+) effector T-cell repertoire characterizes peanut-allergic patients with heightened clinical sensitivity. J Allergy Clin Immunol. 2020;145(1):270–282. doi:10.1016/j.jaci.2019.09.033
  • Van Hemelen D, Mahler V, Fischer G, et al. HLA class II peptide tetramers vs allergen-induced proliferation for identification of allergen-specific CD4 T cells. Allergy. 2015;70(1):49–58. doi:10.1111/all.12524
  • Begin P, Nadeau KC. Changes in peanut-specific T-cell clonotype with oral immunotherapy. J Allergy Clin Immunol. 2015;135(6):1636–1638. doi:10.1016/j.jaci.2015.03.010
  • Tu AA, Gierahn TM, Monian B, et al. TCR sequencing paired with massively parallel 3ʹ RNA-seq reveals clonotypic T cell signatures. Nat Immunol. 2019;20(12):1692–1699. doi:10.1038/s41590-019-0544-5
  • Hintzen RQ, de Jong R, Lens SM, Brouwer M, Baars P, van Lier RA. Regulation of CD27 expression on subsets of mature T-lymphocytes. J Immunol. 1993;151(5):2426–2435.
  • Wambre E, Bajzik V, DeLong JH, et al. A phenotypically and functionally distinct human TH2 cell subpopulation is associated with allergic disorders. Sci Transl Med. 2017;9(401). doi:10.1126/scitranslmed.aam9171
  • Wambre E, James EA, Kwok WW. Characterization of CD4+ T cell subsets in allergy. Curr Opin Immunol. 2012;24(6):700–706. doi:10.1016/j.coi.2012.07.009
  • Wambre E, DeLong JH, James EA, LaFond RE, Robinson D, Kwok WW. Differentiation stage determines pathologic and protective allergen-specific CD4+ T-cell outcomes during specific immunotherapy. J Allergy Clin Immunol. 2012;129(2):544–551, 551 e541–547. doi:10.1016/j.jaci.2011.08.034
  • Chiang D, Chen X, Jones SM, et al. Single-cell profiling of peanut-responsive T cells in patients with peanut allergy reveals heterogeneous effector TH2 subsets. J Allergy Clin Immunol. 2018;141(6):2107–2120. doi:10.1016/j.jaci.2017.11.060
  • Blom LH, Martel BC, Larsen LF, et al. The immunoglobulin superfamily member CD200R identifies cells involved in type 2 immune responses. Allergy. 2017;72(7):1081–1090. doi:10.1111/all.13129
  • Bangert C, Rindler K, Krausgruber T, et al. Persistence of mature dendritic cells, TH2A, and Tc2 cells characterize clinically resolved atopic dermatitis under IL-4Ralpha blockade. Sci Immunol. 2021;6(55):eabe2749. doi:10.1126/sciimmunol.abe2749
  • Noval Rivas M, Burton OT, Wise P, et al. Regulatory T cell reprogramming toward a Th2-cell-like lineage impairs oral tolerance and promotes food allergy. Immunity. 2015;42(3):512–523. doi:10.1016/j.immuni.2015.02.004
  • Cosmi L, Maggi L, Santarlasci V, et al. Identification of a novel subset of human circulating memory CD4(+) T cells that produce both IL-17A and IL-4. J Allergy Clin Immunol. 2010;125(1):222–230 e221–224. doi:10.1016/j.jaci.2009.10.012
  • Spergel J, Aceves SS. Allergic components of eosinophilic esophagitis. J Allergy Clin Immunol. 2018;142(1):1–8. doi:10.1016/j.jaci.2018.05.001
  • Kobayashi T, Iijima K, Dent AL, Kita H. Follicular helper T cells mediate IgE antibody response to airborne allergens. J Allergy Clin Immunol. 2017;139(1):300–313 e307. doi:10.1016/j.jaci.2016.04.021
  • Meli AP, Fontes G, Leung Soo C, King IL. T follicular helper cell-derived IL-4 is required for IgE production during intestinal helminth infection. J Immunol. 2017;199(1):244–252. doi:10.4049/jimmunol.1700141
  • Gowthaman U, Chen JS, Zhang B, et al. Identification of a T follicular helper cell subset that drives anaphylactic IgE. Science. 2019;365(6456):eaaw6433. doi:10.1126/science.aaw6433
  • Jimenez-Saiz R, Bruton K, Jordana M. Follicular T cells: from stability to failure. Allergy. 2020;75(4):1006–1007. doi:10.1111/all.14167
  • Chu DK, Mohammed-Ali Z, Jimenez-Saiz R, et al. T helper cell IL-4 drives intestinal Th2 priming to oral peanut antigen, under the control of OX40L and independent of innate-like lymphocytes. Mucosal Immunol. 2014;7(6):1395–1404. doi:10.1038/mi.2014.29
  • Chu DK, Jimenez-Saiz R, Verschoor CP, et al. Indigenous enteric eosinophils control DCs to initiate a primary Th2 immune response in vivo. J Exp Med. 2014;211(8):1657–1672. doi:10.1084/jem.20131800
  • Ellenbogen Y, Jimenez-Saiz R, Spill P, Chu DK, Waserman S, Jordana M. The Initiation of Th2 immunity towards food allergens. Int J Mol Sci. 2018;19(5):1447. doi:10.3390/ijms19051447
  • Ruiter B, Shreffler WG. Innate immunostimulatory properties of allergens and their relevance to food allergy. Semin Immunopathol. 2012;34(5):617–632. doi:10.1007/s00281-012-0334-8
  • McKinstry KK, Strutt TM, Bautista B, et al. Effector CD4 T-cell transition to memory requires late cognate interactions that induce autocrine IL-2. Nat Commun. 2014;5:5377. doi:10.1038/ncomms6377
  • Surh CD, Sprent J. Homeostasis of naive and memory T cells. Immunity. 2008;29(6):848–862. doi:10.1016/j.immuni.2008.11.002
  • Fazilleau N, Eisenbraun MD, Malherbe L, et al. Lymphoid reservoirs of antigen-specific memory T helper cells. Nat Immunol. 2007;8(7):753–761. doi:10.1038/ni1472
  • Gasper DJ, Tejera MM, Suresh M. CD4 T-cell memory generation and maintenance. Crit Rev Immunol. 2014;34(2):121–146. doi:10.1615/CritRevImmunol.2014010373
  • Gramaglia I, Jember A, Pippig SD, Weinberg AD, Killeen N, Croft M. The OX40 costimulatory receptor determines the development of CD4 memory by regulating primary clonal expansion. J Immunol. 2000;165(6):3043–3050. doi:10.4049/jimmunol.165.6.3043
  • Schiott A, Lindstedt M, Johansson-Lindbom B, Roggen E, Borrebaeck CA. CD27- CD4+ memory T cells define a differentiated memory population at both the functional and transcriptional levels. Immunology. 2004;113(3):363–370. doi:10.1111/j.1365-2567.2004.01974.x
  • Crotty S. T follicular helper cell biology: a decade of discovery and diseases. Immunity. 2019;50(5):1132–1148. doi:10.1016/j.immuni.2019.04.011
  • Zhang B, Liu E, Gertie JA, et al. Divergent T follicular helper cell requirement for IgA and IgE production to peanut during allergic sensitization. Sci Immunol. 2020;5(47). doi:10.1126/sciimmunol.aay2754
  • Noble A, Zhao J. Follicular helper T cells are responsible for IgE responses to Der p 1 following house dust mite sensitization in mice. Clin Exp Allergy. 2016;46(8):1075–1082. doi:10.1111/cea.12750
  • Dolence JJ, Kobayashi T, Iijima K, et al. Airway exposure initiates peanut allergy by involving the IL-1 pathway and T follicular helper cells in mice. J Allergy Clin Immunol. 2018;142(4):1144–1158.
  • Lu KT, Kanno Y, Cannons JL, et al. Functional and epigenetic studies reveal multistep differentiation and plasticity of in vitro-generated and in vivo-derived follicular T helper cells. Immunity. 2011;35(4):622–632. doi:10.1016/j.immuni.2011.07.015
  • Vogelzang A, McGuire HM, Yu D, Sprent J, Mackay CR, King C. A fundamental role for interleukin-21 in the generation of T follicular helper cells. Immunity. 2008;29(1):127–137. doi:10.1016/j.immuni.2008.06.001
  • Weber JP, Fuhrmann F, Feist RK, et al. ICOS maintains the T follicular helper cell phenotype by down-regulating Kruppel-like factor 2. J Exp Med. 2015;212(2):217–233. doi:10.1084/jem.20141432
  • Mahajan S, Cervera A, MacLeod M, et al. The role of ICOS in the development of CD4 T cell help and the reactivation of memory T cells. Eur J Immunol. 2007;37(7):1796–1808. doi:10.1002/eji.200636661
  • Merkenschlager J, Finkin S, Ramos V, et al. Dynamic regulation of TFH selection during the germinal centre reaction. Nature. 2021;591(7850):458–463. doi:10.1038/s41586-021-03187-x
  • Kunzli M, Schreiner D, Pereboom TC, et al. Long-lived T follicular helper cells retain plasticity and help sustain humoral immunity. Sci Immunol. 2020;5(45):eaay5552. doi:10.1126/sciimmunol.aay5552
  • Alterauge D, Bagnoli JW, Dahlstrom F, et al. Continued Bcl6 expression prevents the transdifferentiation of established Tfh cells into Th1 cells during acute viral infection. Cell Rep. 2020;33(1):108232. doi:10.1016/j.celrep.2020.108232
  • Alvarez D, Arkinson JL, Sun J, Fattouh R, Walker T, Jordana M. Th2 differentiation in distinct lymph nodes influences the site of mucosal Th2 immune-inflammatory responses. J Immunol. 2007;179(5):3287–3296. doi:10.4049/jimmunol.179.5.3287
  • Ugur M, Schulz O, Menon MB, Krueger A, Pabst O. Resident CD4+ T cells accumulate in lymphoid organs after prolonged antigen exposure. Nat Commun. 2014;5:4821. doi:10.1038/ncomms5821
  • Islam SA, Luster AD. T cell homing to epithelial barriers in allergic disease. Nat Med. 2012;18(5):705–715. doi:10.1038/nm.2760
  • Masopust D, Choo D, Vezys V, et al. Dynamic T cell migration program provides resident memory within intestinal epithelium. J Exp Med. 2010;207(3):553–564. doi:10.1084/jem.20090858
  • Hondowicz BD, An D, Schenkel JM, et al. Interleukin-2-dependent allergen-specific tissue-resident memory cells drive asthma. Immunity. 2016;44(1):155–166. doi:10.1016/j.immuni.2015.11.004
  • Bosnjak B, Kazemi S, Altenburger LM, Mokrovic G, Epstein MM. Th2-TRMs maintain life-long allergic memory in experimental asthma in mice. Front Immunol. 2019;10:840. doi:10.3389/fimmu.2019.00840
  • Steinbach K, Vincenti I, Merkler D. Resident-memory T cells in tissue-restricted immune responses: for better or worse? Front Immunol. 2018;9:2827. doi:10.3389/fimmu.2018.02827
  • Carrasco YR, Batista FD. B cells acquire particulate antigen in a macrophage-rich area at the boundary between the follicle and the subcapsular sinus of the lymph node. Immunity. 2007;27(1):160–171.
  • Cyster JG, Allen CDC. B cell responses: cell interaction dynamics and decisions. Cell. 2019;177(3):524–540. doi:10.1016/j.cell.2019.03.016
  • Yao Y, Chen CL, Yu D, Liu Z. Roles of follicular helper and regulatory T cells in allergic diseases and allergen immunotherapy. Allergy. 2021;76(2):456–470. doi:10.1111/all.14639
  • Taylor JJ, Pape KA, Jenkins MK. A germinal center-independent pathway generates unswitched memory B cells early in the primary response. J Exp Med. 2012;209(3):597–606. doi:10.1084/jem.20111696
  • Roco JA, Mesin L, Binder SC, et al. Class-switch recombination occurs infrequently in germinal centers. Immunity. 2019;51(2):337–350 e337. doi:10.1016/j.immuni.2019.07.001
  • Allie SR, Bradley JE, Mudunuru U, et al. The establishment of resident memory B cells in the lung requires local antigen encounter. Nat Immunol. 2019;20(1):97–108. doi:10.1038/s41590-018-0260-6
  • Yang Z, Robinson MJ, Allen CD. Regulatory constraints in the generation and differentiation of IgE-expressing B cells. Curr Opin Immunol. 2014;28:64–70. doi:10.1016/j.coi.2014.02.001
  • Finney J, Yeh C-H, Kelsoe G, Kuraoka M. Germinal center responses to complex antigens. Immunol Rev. 2018;284(1):42–50. doi:10.1111/imr.12661
  • Zuccarino-Catania GV, Sadanand S, Weisel FJ, et al. CD80 and PD-L2 define functionally distinct memory B cell subsets that are independent of antibody isotype. Nat Immunol. 2014;15(7):631–637. doi:10.1038/ni.2914
  • Di Niro R, Lee SJ, Vander Heiden JA, et al. Salmonella infection drives promiscuous b cell activation followed by extrafollicular affinity maturation. Immunity. 2015;43(1):120–131. doi:10.1016/j.immuni.2015.06.013
  • Yang Z, Robinson MJ, Chen X, et al. Regulation of B cell fate by chronic activity of the IgE B cell receptor. Elife. 2016;5. doi:10.7554/eLife.21238
  • Haniuda K, Fukao S, Kodama T, Hasegawa H, Kitamura D. Autonomous membrane IgE signaling prevents IgE-memory formation. Nat Immunol. 2016;17(9):1109–1117. doi:10.1038/ni.3508
  • Laffleur B, Debeaupuis O, Dalloul Z, Cogne M. B cell intrinsic mechanisms constraining IgE memory. Front Immunol. 2017;8(1277):1277. doi:10.3389/fimmu.2017.01277
  • Blazquez AB, Berin MC. Gastrointestinal dendritic cells promote Th2 skewing via OX40L. J Immunol. 2008;180(7):4441–4450. doi:10.4049/jimmunol.180.7.4441
  • Adler LN, Jiang W, Bhamidipati K, et al. The other function: class II-restricted antigen presentation by B cells. Front Immunol. 2017;8:319. doi:10.3389/fimmu.2017.00319
  • Moutsoglou DM, Dreskin SC. B cells establish, but do not maintain, long-lived murine anti-peanut IgE(a). Clin Exp Allergy. 2016;46(4):640–653. doi:10.1111/cea.12715
  • Harris DP, Goodrich S, Mohrs K, Mohrs M, Lund FE. Cutting edge: the development of IL-4-producing B cells (B effector 2 cells) is controlled by IL-4, IL-4 receptor alpha, and Th2 cells. J Immunol. 2005;175(11):7103–7107. doi:10.4049/jimmunol.175.11.7103
  • Katona IM, Urban JF Jr, Kang SS, Paul WE, Finkelman FD. IL-4 requirements for the generation of secondary in vivo IgE responses. J Immunol. 1991;146(12):4215–4221.
  • Finkelman FD, Katona IM, Urban JF Jr, et al. IL-4 is required to generate and sustain in vivo IgE responses. J Immunol. 1988;141(7):2335–2341.
  • King IL, Mohrs M. IL-4-producing CD4+ T cells in reactive lymph nodes during helminth infection are T follicular helper cells. J Exp Med. 2009;206(5):1001–1007. doi:10.1084/jem.20090313
  • Liang HE, Reinhardt RL, Bando JK, Sullivan BM, Ho IC, Locksley RM. Divergent expression patterns of IL-4 and IL-13 define unique functions in allergic immunity. Nat Immunol. 2011;13(1):58–66. doi:10.1038/ni.2182
  • McHeyzer-Williams M, Okitsu S, Wang N, McHeyzer-Williams L. Molecular programming of B cell memory. Nat Rev Immunol. 2011;12(1):24–34. doi:10.1038/nri3128
  • Etzioni A, Ochs HD. The hyper IgM syndrome–an evolving story. Pediatr Res. 2004;56(4):519–525. doi:10.1203/01.PDR.0000139318.65842.4A
  • Dong C, Juedes AE, Temann UA, et al. ICOS co-stimulatory receptor is essential for T-cell activation and function. Nature. 2001;409(6816):97–101. doi:10.1038/35051100
  • Latham LE, Wikenheiser DJ, Stumhofer JS. ICOS signaling promotes a secondary humoral response after re-challenge with Plasmodium chabaudi chabaudi AS. PLoS Pathog. 2020;16(4):e1008527. doi:10.1371/journal.ppat.1008527
  • Salek-Ardakani S, Song J, Halteman BS, et al. OX40 (CD134) controls memory T helper 2 cells that drive lung inflammation. J Exp Med. 2003;198(2):315–324. doi:10.1084/jem.20021937
  • Takatsuka S, Yamada H, Haniuda K, et al. IL-9 receptor signaling in memory B cells regulates humoral recall responses. Nat Immunol. 2018;19(9):1025–1034. doi:10.1038/s41590-018-0177-0
  • Blazquez AB, Knight AK, Getachew H, et al. A functional role for CCR6 on proallergic T cells in the gastrointestinal tract. Gastroenterology. 2010;138(1):275–284 e271–274. doi:10.1053/j.gastro.2009.09.016
  • Aguilera-Lizarraga J, Florens MV, Viola MF, et al. Local immune response to food antigens drives meal-induced abdominal pain. Nature. 2021;590(7844):151–156. doi:10.1038/s41586-020-03118-2
  • Moran I, Nguyen A, Khoo WH, et al. Memory B cells are reactivated in subcapsular proliferative foci of lymph nodes. Nat Commun. 2018;9(1):3372. doi:10.1038/s41467-018-05772-7
  • Palm AE, Henry C. Remembrance of things past: long-term B cell memory after infection and vaccination. Front Immunol. 2019;10(1787):1787. doi:10.3389/fimmu.2019.01787
  • Syed A, Garcia MA, Lyu SC, et al. Peanut oral immunotherapy results in increased antigen-induced regulatory T-cell function and hypomethylation of forkhead box protein 3 (FOXP3). J Allergy Clin Immunol. 2014;133(2):500–510. doi:10.1016/j.jaci.2013.12.1037
  • Karlsson MR, Rugtveit J, Brandtzaeg P. Allergen-responsive CD4+CD25+ regulatory T cells in children who have outgrown cow’s milk allergy. J Exp Med. 2004;199(12):1679–1688. doi:10.1084/jem.20032121
  • Sayin I, Radtke AJ, Vella LA, et al. Spatial distribution and function of T follicular regulatory cells in human lymph nodes. J Exp Med. 2018;215(6):1531–1542. doi:10.1084/jem.20171940
  • Clement RL, Daccache J, Mohammed MT, et al. Follicular regulatory T cells control humoral and allergic immunity by restraining early B cell responses. Nat Immunol. 2019;20(10):1360–1371. doi:10.1038/s41590-019-0472-4
  • Xie MM, Chen Q, Liu H, et al. T follicular regulatory cells and IL-10 promote food antigen-specific IgE. J Clin Invest. 2020;130(7):3820–3832. doi:10.1172/JCI132249
  • Canete PF, Sweet RA, Gonzalez-Figueroa P, et al. Regulatory roles of IL-10-producing human follicular T cells. J Exp Med. 2019;216(8):1843–1856. doi:10.1084/jem.20190493
  • Yang Z, Wu CM, Targ S, Allen CDC. IL-21 is a broad negative regulator of IgE class switch recombination in mouse and human B cells. J Exp Med. 2020;217(5). doi:10.1084/jem.20190472
  • Rosser EC, Mauri C. Regulatory B cells: origin, phenotype, and function. Immunity. 2015;42(4):607–612. doi:10.1016/j.immuni.2015.04.005
  • Ma S, Satitsuksanoa P, Jansen K, Cevhertas L, van de Veen W, Akdis M. B regulatory cells in allergy. Immunol Rev. 2020. doi:10.1111/imr.12937
  • Jansen K, Cevhertas L, Ma S, Satitsuksanoa P, Akdis M, van de Veen W. Regulatory B cells, A to Z. Allergy. 2021. doi:10.1111/all.14763
  • Jimenez-Saiz R, Patil SU. The multifaceted B cell response in allergen immunotherapy. Curr Allergy Asthma Rep. 2018;18(12):66. doi:10.1007/s11882-018-0819-1
  • Boonpiyathad T, Meyer N, Moniuszko M, et al. High-dose bee venom exposure induces similar tolerogenic B-cell responses in allergic patients and healthy beekeepers. Allergy. 2017;72(3):407–415. doi:10.1111/all.12966
  • Boonpiyathad T, Tantilipikorn P, Ruxrungtham K, et al. IL-10-producing innate lymphoid cells increased in patients with house dust mite allergic rhinitis following immunotherapy. J Allergy Clin Immunol. 2020.
  • Zissler UM, Jakwerth CA, Guerth FM, et al. Early IL-10 producing B-cells and coinciding Th/Tr17 shifts during three year grass-pollen AIT. EBioMedicine. 2018;36:475–488. doi:10.1016/j.ebiom.2018.09.016
  • Armingol E, Officer A, Harismendy O, Lewis NE. Deciphering cell-cell interactions and communication from gene expression. Nat Rev Genet. 2021;22(2):71–88. doi:10.1038/s41576-020-00292-x