New concepts in the generation and functions of IgA (original) (raw)
Brandtzaeg, P. Mucosal immunity: induction, dissemination, and effector functions. Scand. J. Immunol.70, 505–515 (2009). ArticleCASPubMed Google Scholar
Lycke, N., Erlandsson, L., Ekman, L., Schon, K. & Leanderson, T. Lack of J chain inhibits the transport of gut IgA and abrogates the development of intestinal antitoxic protection. J. Immunol.163, 913–919 (1999). CASPubMed Google Scholar
Forbes, S. J., Eschmann, M. & Mantis, N. J. Inhibition of Salmonella enterica serovar Typhimurium motility and entry into epithelial cells by a protective antilipopolysaccharide monoclonal immunoglobulin A antibody. Infect. Immun.76, 4137–4144 (2008). ArticleCASPubMedPubMed Central Google Scholar
Forbes, S. J., Bumpus, T., McCarthy, E. A., Corthesy, B. & Mantis, N. J. Transient suppression of Shigella flexneri type 3 secretion by a protective O-antigen-specific monoclonal IgA. MBio2, e00042-11 (2011). ArticleCASPubMedPubMed Central Google Scholar
Kadaoui, K. A. & Corthesy, B. Secretory IgA mediates bacterial translocation to dendritic cells in mouse Peyer's patches with restriction to mucosal compartment. J. Immunol.179, 7751–7757 (2007). ArticleCASPubMed Google Scholar
Mantis, N. J., Rol, N. & Corthesy, B. Secretory IgA's complex roles in immunity and mucosal homeostasis in the gut. Mucosal Immunol.4, 603–611 (2011). ArticleCASPubMedPubMed Central Google Scholar
Bakema, J. E. & van Egmond, M. The human immunoglobulin A Fc receptor FcαRI: a multifaceted regulator of mucosal immunity. Mucosal Immunol.4, 612–624 (2012). ArticleCAS Google Scholar
Robinson, J. K., Blanchard, T. G., Levine, A. D., Emancipator, S. N. & Lamm, M. E. A mucosal IgA-mediated excretory immune system in vivo. J. Immunol.166, 3688–3692 (2001). ArticleCASPubMed Google Scholar
Spencer, J., Klavinskis, L. S. & Fraser, L. D. The human intestinal IgA response; burning questions. Front. Immunol.3, 108 (2012). ArticlePubMedPubMed Central Google Scholar
Agace, W. W. & Persson, E. K. How vitamin A metabolizing dendritic cells are generated in the gut mucosa. Trends Immunol.33, 42–48 (2011). ArticleCASPubMed Google Scholar
Corthesy, B. Role of secretory immunoglobulin A and secretory component in the protection of mucosal surfaces. Future Microbiol.5, 817–829 (2011). Article Google Scholar
Macpherson, A. J., McCoy, K. D., Johansen, F. E. & Brandtzaeg, P. The immune geography of IgA induction and function. Mucosal Immunol.1, 11–22 (2008). ArticleCASPubMed Google Scholar
Gowans, J. L. & Knight, E. J. The route of re-circulation of lymphocytes in the rat. Proc. R. Soc. Lond. B159, 257–282 (1964). ArticleCASPubMed Google Scholar
Mei, H. E. et al. Blood-borne human plasma cells in steady state are derived from mucosal immune responses. Blood113, 2461–2469 (2009). ArticleCASPubMed Google Scholar
Mesin, L., Di Niro, R., Thompson, K. M., Lundin, K. E. & Sollid, L. M. Long-lived plasma cells from human small intestine biopsies secrete immunoglobulins for many weeks in vitro. J. Immunol.187, 2867–2874 (2012). ArticleCAS Google Scholar
Di Niro, R. et al. High abundance of plasma cells secreting transglutaminase 2-specific IgA autoantibodies with limited somatic hypermutation in celiac disease intestinal lesions. Nature Med.18, 441–445 (2012). ArticleCASPubMed Google Scholar
Hapfelmeier, S. et al. Reversible microbial colonization of germ-free mice reveals the dynamics of IgA immune responses. Science328, 1705–1709 (2010). ArticleCASPubMedPubMed Central Google Scholar
Tokoyoda, K., Hauser, A. E., Nakayama, T. & Radbruch, A. Organization of immunological memory by bone marrow stroma. Nature Rev. Immunol.10, 193–200 (2010). ArticleCAS Google Scholar
Chu, V. T. et al. Eosinophils are required for the maintenance of plasma cells in the bone marrow. Nature Immunol.12, 151–159 (2011). ArticleCAS Google Scholar
Winter, O. et al. Megakaryocytes constitute a functional component of a plasma cell niche in the bone marrow. Blood116, 1867–1875 (2010). ArticleCASPubMed Google Scholar
Ng, E. K. et al. Human intestinal epithelial and smooth muscle cells are potent producers of IL-6. Mediators Inflamm.12, 3–8 (2003). ArticlePubMedPubMed Central Google Scholar
Agace, W. W. et al. Constitutive expression of stromal derived factor-1 by mucosal epithelia and its role in HIV transmission and propagation. Curr. Biol.10, 325–328 (2000). ArticleCASPubMed Google Scholar
Avery, D. T. et al. BAFF selectively enhances the survival of plasmablasts generated from human memory B cells. J. Clin. Invest.112, 286–297 (2003). ArticleCASPubMedPubMed Central Google Scholar
Belnoue, E. et al. APRIL is critical for plasmablast survival in the bone marrow and poorly expressed by early-life bone marrow stromal cells. Blood111, 2755–2764 (2008). ArticleCASPubMed Google Scholar
Huard, B. et al. APRIL secreted by neutrophils binds to heparan sulfate proteoglycans to create plasma cell niches in human mucosa. J. Clin. Invest.118, 2887–2895 (2008). CASPubMedPubMed Central Google Scholar
Tezuka, H. et al. Prominent role for plasmacytoid dendritic cells in mucosal T cell-independent IgA induction. Immunity34, 247–257 (2011). ArticleCASPubMed Google Scholar
Xu, W. et al. Epithelial cells trigger frontline immunoglobulin class switching through a pathway regulated by the inhibitor SLPI. Nature Immunol.8, 294–303 (2007). ArticleCAS Google Scholar
He, B. et al. Intestinal bacteria trigger T cell-independent immunoglobulin A2 class switching by inducing epithelial-cell secretion of the cytokine APRIL. Immunity26, 812–826 (2007). ArticleCASPubMed Google Scholar
Macpherson, A. J. et al. A primitive T cell-independent mechanism of intestinal mucosal IgA responses to commensal bacteria. Science288, 2222–2226 (2000). CASPubMed Google Scholar
Bergqvist, P., Gardby, E., Stensson, A., Bemark, M. & Lycke, N. Y. Gut IgA class switch recombination in the absence of CD40 does not occur in the lamina propria and is independent of germinal centers. J. Immunol.177, 7772–7783 (2006). ArticleCASPubMed Google Scholar
Cong, Y., Feng, T., Fujihashi, K., Schoeb, T. R. & Elson, C. O. A dominant, coordinated T regulatory cell-IgA response to the intestinal microbiota. Proc. Natl Acad. Sci. USA106, 19256–19261 (2009). ArticleCASPubMedPubMed Central Google Scholar
Zoetendal, E. G., Akkermans, A. D. & De Vos, W. M. Temperature gradient gel electrophoresis analysis of 16S rRNA from human fecal samples reveals stable and host-specific communities of active bacteria. Appl. Environ. Microbiol.64, 3854–3859 (1998). CASPubMedPubMed Central Google Scholar
Lindner, C. et al. Age, microbiota, and T cells shape diverse individual IgA repertoires in the intestine. J. Exp. Med.209, 365–377 (2012). ArticleCASPubMedPubMed Central Google Scholar
Fazekas de St, G. & Webster, R. G. Disquisitions of original antigenic sin. I. Evidence in man. J. Exp. Med.124, 331–345 (1966). Article Google Scholar
Ferrari, S. et al. Mutations of CD40 gene cause an autosomal recessive form of immunodeficiency with hyper IgM. Proc. Natl Acad. Sci. USA98, 12614–12619 (2001). ArticleCASPubMedPubMed Central Google Scholar
Craig, S. W. & Cebra, J. J. Peyer's patches: an enriched source of precursors for IgA-producing immunocytes in the rabbit. J. Exp. Med.134, 188–200 (1971). ArticleCASPubMedPubMed Central Google Scholar
Neutra, M. R., Mantis, N. J. & Kraehenbuhl, J. P. Collaboration of epithelial cells with organized mucosal lymphoid tissues. Nature Immunol.2, 1004–1009 (2001). ArticleCAS Google Scholar
Owen, R. L. Uptake and transport of intestinal macromolecules and microorganisms by M cells in Peyer's patches — a personal and historical perspective. Semin. Immunol.11, 157–163 (1999). ArticleCASPubMed Google Scholar
Lelouard, H., Fallet, M., de Bovis, B., Meresse, S. & Gorvel, J. P. Peyer's patch dendritic cells sample antigens by extending dendrites through M cell-specific transcellular pores. Gastroenterology142, 592–601 (2012). ArticleCASPubMed Google Scholar
Hase, K. et al. Uptake through glycoprotein 2 of FimH+ bacteria by M cells initiates mucosal immune response. Nature462, 226–230 (2009). ArticleCASPubMed Google Scholar
Mantis, N. J. et al. Selective adherence of IgA to murine Peyer's patch M cells: evidence for a novel IgA receptor. J. Immunol.169, 1844–1851 (2002). ArticleCASPubMed Google Scholar
Bergtold, A., Desai, D. D., Gavhane, A. & Clynes, R. Cell surface recycling of internalized antigen permits dendritic cell priming of B cells. Immunity23, 503–514 (2005). ArticleCASPubMed Google Scholar
Suzuki, K. et al. The sensing of environmental stimuli by follicular dendritic cells promotes immunoglobulin A generation in the gut. Immunity33, 71–83 (2010). ArticleCASPubMed Google Scholar
Borsutzky, S., Cazac, B. B., Roes, J. & Guzman, C. A. TGF-β receptor signaling is critical for mucosal IgA responses. J. Immunol.173, 3305–3309 (2004). ArticleCASPubMed Google Scholar
Tezuka, H. et al. Regulation of IgA production by naturally occurring TNF/iNOS-producing dendritic cells. Nature448, 929–933 (2007). ArticleCASPubMed Google Scholar
Austin, A. S. et al. Identification and characterization of a novel regulatory factor: IgA-inducing protein. J. Immunol.171, 1336–1342 (2003). ArticleCASPubMed Google Scholar
Endsley, M. A. et al. Human IgA-inducing protein from dendritic cells induces IgA production by naive IgD+ B cells. J. Immunol.182, 1854–1859 (2009). ArticleCASPubMed Google Scholar
Mora, J. R. et al. Generation of gut-homing IgA-secreting B cells by intestinal dendritic cells. Science314, 1157–1160 (2006). ArticleCASPubMed Google Scholar
Pabst, O. et al. Adaptation of solitary intestinal lymphoid tissue in response to microbiota and chemokine receptor CCR7 signaling. J. Immunol.177, 6824–6832 (2006). ArticleCASPubMed Google Scholar
Bouskra, D. et al. Lymphoid tissue genesis induced by commensals through NOD1 regulates intestinal homeostasis. Nature456, 507–510 (2008). ArticleCASPubMed Google Scholar
Pabst, O. et al. Cryptopatches and isolated lymphoid follicles: dynamic lymphoid tissues dispensable for the generation of intraepithelial lymphocytes. Eur. J. Immunol.35, 98–107 (2005). ArticleCASPubMed Google Scholar
Tsuji, M. et al. Requirement for lymphoid tissue-inducer cells in isolated follicle formation and T cell-independent immunoglobulin A generation in the gut. Immunity29, 261–271 (2008). ArticleCASPubMed Google Scholar
Lorenz, R. G. & Newberry, R. D. Isolated lymphoid follicles can function as sites for induction of mucosal immune responses. Ann. NY Acad. Sci.1029, 44–57 (2004). ArticleCASPubMed Google Scholar
Kang, H. S. et al. Signaling via LTβR on the lamina propria stromal cells of the gut is required for IgA production. Nature Immunol.3, 576–582 (2002). ArticleCAS Google Scholar
McDonald, K. G., Leach, M. R., Huang, C., Wang, C. & Newberry, R. D. Aging impacts isolated lymphoid follicle development and function. Immun. Ageing8, 1 (2011). ArticleCASPubMedPubMed Central Google Scholar
Lane, P. J. et al. Lymphoid tissue inducer cells: innate cells critical for CD4+ T cell memory responses? Ann. NY Acad. Sci.1247, 1–15 (2012). ArticleCASPubMed Google Scholar
Quinti, I. et al. Long-term follow-up and outcome of a large cohort of patients with common variable immunodeficiency. J. Clin. Immunol.27, 308–316 (2007). ArticlePubMed Google Scholar
Fagarasan, S. et al. Critical roles of activation-induced cytidine deaminase in the homeostasis of gut flora. Science298, 1424–1427 (2002). CASPubMed Google Scholar
Hu, S., Yang, K., Yang, J., Li, M. & Xiong, N. Critical roles of chemokine receptor CCR10 in regulating memory IgA responses in intestines. Proc. Natl Acad. Sci. USA108, e1035–e1044 (2011). ArticlePubMedPubMed Central Google Scholar
Knoop, K. A. & Newberry, R. D. Isolated lymphoid follicles are dynamic reservoirs for the induction of intestinal IgA. Front. Immunol.3, 84 (2012). ArticlePubMedPubMed Central Google Scholar
Fagarasan, S., Kinoshita, K., Muramatsu, M., Ikuta, K. & Honjo, T. In situ class switching and differentiation to IgA-producing cells in the gut lamina propria. Nature413, 639–643 (2001). ArticleCASPubMed Google Scholar
Bergqvist, P., Stensson, A., Lycke, N. Y. & Bemark, M. T cell-independent IgA class switch recombination is restricted to the GALT and occurs prior to manifest germinal center formation. J. Immunol.184, 3545–3553 (2010). ArticleCASPubMed Google Scholar
Shikina, T. et al. IgA class switch occurs in the organized nasopharynx- and gut-associated lymphoid tissue, but not in the diffuse lamina propria of airways and gut. J. Immunol.172, 6259–6264 (2004). ArticleCASPubMed Google Scholar
Boursier, L., Gordon, J. N., Thiagamoorthy, S., Edgeworth, J. D. & Spencer, J. Human intestinal IgA response is generated in the organized gut-associated lymphoid tissue but not in the lamina propria. Gastroenterology128, 1879–1889 (2005). ArticleCASPubMed Google Scholar
Fritz, J. H. et al. Acquisition of a multifunctional IgA+ plasma cell phenotype in the gut. Nature481, 199–203 (2012). ArticleCAS Google Scholar
Macpherson, A. J. & Uhr, T. Induction of protective IgA by intestinal dendritic cells carrying commensal bacteria. Science303, 1662–1665 (2004). ArticleCASPubMed Google Scholar
Berberich, S., Forster, R. & Pabst, O. The peritoneal micromilieu commits B cells to home to body cavities and the small intestine. Blood109, 4627–4634 (2007). ArticleCASPubMed Google Scholar
Rosado, M. M. et al. From the fetal liver to spleen and gut: the highway to natural antibody. Mucosal Immunol.2, 351–361 (2009). ArticleCASPubMed Google Scholar
Roy, B. et al. Somatic hypermutation in peritoneal B1b cells. Mol. Immunol.46, 1613–1619 (2009). ArticleCASPubMed Google Scholar
Jiang, N. et al. Determinism and stochasticity during maturation of the zebrafish antibody repertoire. Proc. Natl Acad. Sci. USA108, 5348–5353 (2011). ArticleCASPubMedPubMed Central Google Scholar
Weinstein, J. A., Jiang, N., White, R. A., Fisher, D. S. & Quake, S. R. High-throughput sequencing of the zebrafish antibody repertoire. Science324, 807–810 (2009). ArticleCASPubMedPubMed Central Google Scholar
Ippolito, G. C. et al. Antibody repertoires in humanized NOD-_scid_-IL2Rγnull mice and human B cells reveals human-like diversification and tolerance checkpoints in the mouse. PLoS ONE7, e35497 (2012). ArticleCASPubMedPubMed Central Google Scholar
Boursier, L., Dunn-Walters, D. K. & Spencer, J. Sequence analysis of light chain genes from human intestinal plasma cells demonstrates that λ genes are almost all in-frame and highly mutated and most κ genes are highly mutated when in-frame and minimally mutated when out-of-frame. Eur. J. Immunol.30, 2908–2917 (2000). ArticleCASPubMed Google Scholar
Yuvaraj, S. et al. Evidence for local expansion of IgA plasma cell precursors in human ileum. J. Immunol.183, 4871–4878 (2009). ArticleCASPubMed Google Scholar
Stoel, M. et al. Restricted IgA repertoire in both B-1 and B-2 cell-derived gut plasmablasts. J. Immunol.174, 1046–1054 (2005). ArticleCASPubMed Google Scholar
Holtmeier, W., Hennemann, A. & Caspary, W. F. IgA and IgM VH repertoires in human colon: evidence for clonally expanded B cells that are widely disseminated. Gastroenterology119, 1253–1266 (2000). ArticleCASPubMed Google Scholar
Barone, F. et al. IgA-producing plasma cells originate from germinal centers that are induced by B-cell receptor engagement in humans. Gastroenterology140, 947–956 (2011). ArticleCASPubMed Google Scholar
Benckert, J. et al. The majority of intestinal IgA+ and IgG+ plasmablasts in the human gut are antigen-specific. J. Clin. Invest.121, 1946–1955 (2011). ArticleCASPubMedPubMed Central Google Scholar
Bos, N. A. et al. Monoclonal immunoglobulin A derived from peritoneal B cells is encoded by both germ line and somatically mutated VH genes and is reactive with commensal bacteria. Infect. Immun.64, 616–623 (1996). CASPubMedPubMed Central Google Scholar
Kepler, T. B. & Perelson, A. S. Cyclic re-entry of germinal center B cells and the efficiency of affinity maturation. Immunol. Today14, 412–415 (1993). ArticleCASPubMed Google Scholar
Bergqvist, P. et al. Re-utilization of germinal centers in multiple Peyer's patches results in highly synchronized, oligoclonal, and affinity-matured gut IgA responses. Mucosal Immunol. 11 Jul 2012 (doi:10.1038/mi.2012.56). ArticleCASPubMed Google Scholar
Slack, E., Balmer, M. L., Fritz, J. H. & Hapfelmeier, S. Functional flexibility of intestinal IgA — broadening the fine line. Front. Immunol.3, 100 (2012). ArticlePubMedPubMed Central Google Scholar
van der Waaij, L. A., Limburg, P. C., Mesander, G. & van der Waaij, D. In vivo IgA coating of anaerobic bacteria in human faeces. Gut38, 348–354 (1996). ArticleCASPubMedPubMed Central Google Scholar
De Palma, G. et al. Intestinal dysbiosis and reduced immunoglobulin-coated bacteria associated with coeliac disease in children. BMC Microbiol.10, 63 (2010). ArticleCASPubMedPubMed Central Google Scholar
Wei, M. et al. Mice carrying a knock-in mutation of Aicda resulting in a defect in somatic hypermutation have impaired gut homeostasis and compromised mucosal defense. Nature Immunol.12, 264–270 (2011). ArticleCAS Google Scholar
Shimoda, M., Inoue, Y., Azuma, N. & Kanno, C. Natural polyreactive immunoglobulin A antibodies produced in mouse Peyer's patches. Immunology97, 9–17 (1999). ArticleCASPubMedPubMed Central Google Scholar
Quan, C. P., Berneman, A., Pires, R., Avrameas, S. & Bouvet, J. P. Natural polyreactive secretory immunoglobulin A autoantibodies as a possible barrier to infection in humans. Infect. Immun.65, 3997–4004 (1997). CASPubMedPubMed Central Google Scholar
Peterson, D. A., McNulty, N. P., Guruge, J. L. & Gordon, J. I. IgA response to symbiotic bacteria as a mediator of gut homeostasis. Cell Host Microbe2, 328–339 (2007). ArticleCASPubMed Google Scholar
Shroff, K. E., Meslin, K. & Cebra, J. J. Commensal enteric bacteria engender a self-limiting humoral mucosal immune response while permanently colonizing the gut. Infect. Immun.63, 3904–3913 (1995). CASPubMedPubMed Central Google Scholar
Perrier, C., Sprenger, N. & Corthesy, B. Glycans on secretory component participate in innate protection against mucosal pathogens. J. Biol. Chem.281, 14280–14287 (2006). ArticleCASPubMed Google Scholar
Mathias, A. & Corthesy, B. Recognition of Gram-positive intestinal bacteria by hybridoma- and colostrum-derived secretory immunoglobulin A is mediated by carbohydrates. J. Biol. Chem.286, 17239–17247 (2011). ArticleCASPubMedPubMed Central Google Scholar
Lycke, N., Eriksen, L. & Holmgren, J. Protection against cholera toxin after oral immunization is thymus-dependent and associated with intestinal production of neutralizing IgA antitoxin. Scand. J. Immunol.25, 413–419 (1987). ArticleCASPubMed Google Scholar
Kawamoto, S. et al. The inhibitory receptor PD-1 regulates IgA selection and bacterial composition in the gut. Science336, 485–489 (2012). ArticleCASPubMed Google Scholar
Wijburg, O. L. et al. Innate secretory antibodies protect against natural Salmonella typhimurium infection. J. Exp. Med.203, 21–26 (2006). ArticleCASPubMedPubMed Central Google Scholar
Burns, J. W., Siadat-Pajouh, M., Krishnaney, A. A. & Greenberg, H. B. Protective effect of rotavirus VP6-specific IgA monoclonal antibodies that lack neutralizing activity. Science272, 104–107 (1996). ArticleCASPubMed Google Scholar
Schaffer, F. M., Monteiro, R. C., Volanakis, J. E. & Cooper, M. D. IgA deficiency. Immunodefic. Rev.3, 15–44 (1991). CASPubMed Google Scholar
Brandtzaeg, P. Update on mucosal immunoglobulin A in gastrointestinal disease. Curr. Opin. Gastroenterol.26, 554–563 (2010). ArticleCASPubMed Google Scholar
Shulzhenko, N. et al. Crosstalk between B lymphocytes, microbiota and the intestinal epithelium governs immunity versus metabolism in the gut. Nature Med.17, 1585–1593 (2012). ArticleCAS Google Scholar
Reikvam, D. H. et al. Epithelial–microbial crosstalk in polymeric Ig receptor deficient mice. Eur. J. Immunol. 2 Aug 2012 (doi:10.1002/eji.201242543). ArticleCASPubMed Google Scholar
Di Niro, R. et al. Rapid generation of rotavirus-specific human monoclonal antibodies from small-intestinal mucosa. J. Immunol.185, 5377–5383 (2010). ArticleCASPubMed Google Scholar