Specific microbiota enhances intestinal IgA levels by inducing TGF-β in T follicular helper cells of Peyer's patches in mice.
Anaeroplasma
Peyer's patches
T follicular helper cells
TGF-β
mucosal IgA
Journal
European journal of immunology
ISSN: 1521-4141
Titre abrégé: Eur J Immunol
Pays: Germany
ID NLM: 1273201
Informations de publication
Date de publication:
06 2020
06 2020
Historique:
received:
15
11
2019
revised:
15
11
2019
accepted:
14
02
2020
pubmed:
18
2
2020
medline:
15
12
2020
entrez:
18
2
2020
Statut:
ppublish
Résumé
In humans and mice, mucosal immune responses are dominated by IgA antibodies and the cytokine TGF-β, suppressing unwanted immune reactions but also targeting Ig class switching to IgA. It had been suggested that eosinophils promote the generation and maintenance of mucosal IgA-expressing plasma cells. Here, we demonstrate that not eosinophils, but specific bacteria determine mucosal IgA production. Co-housing of eosinophil-deficient mice with mice having high intestinal IgA levels, as well as the intentional microbiota transfer induces TGF-β expression in intestinal T follicular helper cells, thereby promoting IgA class switching in Peyer's patches, enhancing IgA
Identifiants
pubmed: 32065660
doi: 10.1002/eji.201948474
doi:
Substances chimiques
Immunoglobulin A
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
783-794Subventions
Organisme : Dr. Rolf M. Schwiete Stiftung
Pays : International
Organisme : ERC advanced grant IMMEMO
ID : ERC-2010-AdG_20100317 Grant 268987
Pays : International
Organisme : Russian Science Foundation
ID : 17-74-20059
Pays : International
Organisme : Ministry of Science and Higher Education of the Russian Federation
ID : 075-15-2019-1660
Pays : International
Organisme : Deutsche Forschungsgemeinschaft
ID : SFB TRR130
Pays : International
Organisme : Deutsche Forschungsgemeinschaft
ID : SPP1656
Pays : International
Organisme : Deutsche Forschungsgemeinschaft
ID : TRR241
Pays : International
Organisme : Leibniz Association
Pays : International
Organisme : H2020 Marie Skłodowska-Curie Actions
Pays : International
Informations de copyright
© 2020 The Authors. European Journal of Immunology published by WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim.
Références
Brandtzaeg, P., Halstensen, T. S., Huitfeldt, H. S., Krajci, P., Kvale, D., Scott, H. and Thrane, P. S., Epithelial expression of HLA, secretory component (poly-Ig receptor), and adhesion molecules in the human alimentary tract. Ann. N. Y. Acad. Sci. 1992. 664: 157-179.
Craig, S. W. and Cebra, J. J., Peyer's patches: an enriched source of precursors for IgA-producing immunocytes in the rabbit. J. Exp. Med. 1971. 134: 188-200.
Fagarasan, S., Kinoshita, K., Muramatsu, M., Ikuta, K. and Honjo, T., In situ class switching and differentiation to IgA-producing cells in the gut lamina propria. Nature 2001. 413: 639-643.
Kruglov, A. A., Grivennikov, S. I., Kuprash, D. V., Winsauer, C., Prepens, S., Seleznik, G. M., Eberl, G. et al., Nonredundant function of soluble LTalpha3 produced by innate lymphoid cells in intestinal homeostasis. Science 2013. 342: 1243-1246.
Tsuji, M., Suzuki, K., Kinoshita, K. and Fagarasan, S., Dynamic interactions between bacteria and immune cells leading to intestinal IgA synthesis. Semin. Immunol. 2008. 20: 59-66.
Cazac, B. B. and Roes, J., TGF-beta receptor controls B cell responsiveness and induction of IgA in vivo. Immunity 2000. 13: 443-451.
Sonoda, E., Matsumoto, R., Hitoshi, Y., Ishii, T., Sugimoto, M., Araki, S., Tominaga, A. et al., Transforming growth factor beta induces IgA production and acts additively with interleukin 5 for IgA production. J. Exp. Med. 1989. 170: 1415-1420.
Islam, K. B., Nilsson, L., Sideras, P., Hammarstrom, L. and Smith, C. I., TGF-beta 1 induces germ-line transcripts of both IgA subclasses in human B lymphocytes. Int. Immunol. 1991. 3: 1099-1106.
Shockett, P. and Stavnezer, J., Effect of cytokines on switching to IgA and alpha germline transcripts in the B lymphoma I.29 mu. Transforming growth factor-beta activates transcription of the unrearranged C alpha gene. J. Immunol. 1991. 147: 4374-4383.
Lorenz, M., Jung, S. and Radbruch, A., Switch transcripts in immunoglobulin class switching. Science 1995. 267: 1825-1828.
Crotty, S., Follicular helper CD4 T cells (TFH). Annu. Rev. Immunol. 2011. 29: 621-663.
Dullaers, M., Li, D., Xue, Y., Ni, L., Gayet, I., Morita, R., Ueno, H. et al., A T cell-dependent mechanism for the induction of human mucosal homing immunoglobulin A-secreting plasmablasts. Immunity 2009. 30: 120-129.
Reboldi, A., Arnon, T. I., Rodda, L. B., Atakilit, A., Sheppard, D. and Cyster, J. G., IgA production requires B cell interaction with subepithelial dendritic cells in Peyer's patches. Science 2016. 352: aaf4822.
Chu, V. T., Beller, A., Rausch, S., Strandmark, J., Zanker, M., Arbach, O., Kruglov, A. et al., Eosinophils promote generation and maintenance of immunoglobulin-A-expressing plasma cells and contribute to gut immune homeostasis. Immunity 2014. 40: 582-593.
Jung, Y., Wen, T., Mingler, M. K., Caldwell, J. M., Wang, Y. H., Chaplin, D. D., Lee, E. H. et al., IL-1beta in eosinophil-mediated small intestinal homeostasis and IgA production. Mucosal Immunol 2015. 8 (4), 930-42.
Yu, C., Cantor, A. B., Yang, H., Browne, C., Wells, R. A., Fujiwara, Y. and Orkin, S. H., Targeted deletion of a high-affinity GATA-binding site in the GATA-1 promoter leads to selective loss of the eosinophil lineage in vivo. J. Exp. Med. 2002. 195: 1387-1395.
Crabbe, P. A., Bazin, H., Eyssen, H. and Heremans, J. F., The normal microbial flora as a major stimulus for proliferation of plasma cells synthesizing IgA in the gut. The germ-free intestinal tract. Int. Arch. Allergy Appl. Immunol. 1968. 34: 362-375.
Hapfelmeier, S., Lawson, M. A., Slack, E., Kirundi, J. K., Stoel, M., Heikenwalder, M., Cahenzli, J. et al., Reversible microbial colonization of germ-free mice reveals the dynamics of IgA immune responses. Science 2010. 328: 1705-1709.
Levy, M., Kolodziejczyk, A. A., Thaiss, C. A. and Elinav, E., Dysbiosis and the immune system. Nat. Rev. Immunol. 2017. 17: 219-232.
ROBINSON, I. M., ALLISON, M. J. and HARTMAN, P. A., Anaeroplasma abactoclasticum gen.nov., sp.nov.: an Obligately Anaerobic Mycoplasma from the Rumen. Int. J. System. Evol. Microbiol. 1975. 25: 173-181.
Zimmermann, J., Hubschmann, T., Schattenberg, F., Schumann, J., Durek, P., Riedel, R., Friedrich, M. et al., High-resolution microbiota flow cytometry reveals dynamic colitis-associated changes in fecal bacterial composition. Eur. J. Immunol. 2016. 46: 1300-1303.
Palm, N. W., de Zoete, M. R., Cullen, T. W., Barry, N. A., Stefanowski, J., Hao, L., Degnan, P. H. et al., Immunoglobulin A coating identifies colitogenic bacteria in inflammatory bowel disease. Cell 2014. 158: 1000-1010.
Peterson, D. A., McNulty, N. P., Guruge, J. L. and Gordon, J. I., IgA response to symbiotic bacteria as a mediator of gut homeostasis. Cell Host Microbe 2007. 2: 328-339.
Becker, C., Fantini, M. C. and Neurath, M. F., TGF-beta as a T cell regulator in colitis and colon cancer. Cytokine Growth Factor Rev. 2006. 17: 97-106.
Borsutzky, S., Cazac, B. B., Roes, J. and Guzman, C. A., TGF-beta receptor signaling is critical for mucosal IgA responses. J. Immunol. 2004. 173: 3305-3309.
Irsch, J., Irlenbusch, S., Radl, J., Burrows, P. D., Cooper, M. D. and Radbruch, A. H., Switch recombination in normal IgA1+ B lymphocytes. Proc. Natl. Acad. Sci. U. S. A. 1994. 91: 1323-1327.
Hu, Y., Pan, Q., Pardali, E., Mills, F. C., Bernstein, R. M., Max, E. E., Sideras, P. et al., Regulation of germline promoters by the two human Ig heavy chain 3' alpha enhancers. J. Immunol. 2000. 164: 6380-6386.
Pardali, E., Xie, X. Q., Tsapogas, P., Itoh, S., Arvanitidis, K., Heldin, C. H., ten Dijke, P. et al., Smad and AML proteins synergistically confer transforming growth factor beta1 responsiveness to human germ-line IgA genes. J. Biol. Chem. 2000. 275: 3552-3560.
Park, S. R., Lee, J. H. and Kim, P. H., Smad3 and Smad4 mediate transforming growth factor-beta1-induced IgA expression in murine B lymphocytes. Eur. J. Immunol. 2001. 31: 1706-1715.
Fink, L. N. and Frokiaer, H., Dendritic cells from Peyer's patches and mesenteric lymph nodes differ from spleen dendritic cells in their response to commensal gut bacteria. Scand. J. Immunol. 2008. 68: 270-279.
Mora, J. R., Iwata, M., Eksteen, B., Song, S. Y., Junt, T., Senman, B., Otipoby, K. L. et al., Generation of gut-homing IgA-secreting B cells by intestinal dendritic cells. Science 2006. 314: 1157-1160.
Sato, A., Hashiguchi, M., Toda, E., Iwasaki, A., Hachimura, S. and Kaminogawa, S., CD11b+ Peyer's patch dendritic cells secrete IL-6 and induce IgA secretion from naive B cells. J. Immunol. 2003. 171: 3684-3690.
Atarashi, K., Tanoue, T., Oshima, K., Suda, W., Nagano, Y., Nishikawa, H., Fukuda, S. et al., Treg induction by a rationally selected mixture of Clostridia strains from the human microbiota. Nature 2013. 500: 232-236.
Suzuki, K., Maruya, M., Kawamoto, S., Sitnik, K., Kitamura, H., Agace, W. W. and Fagarasan, S., The sensing of environmental stimuli by follicular dendritic cells promotes immunoglobulin A generation in the gut. Immunity 2010. 33: 71-83.
Kubinak, J. L., Petersen, C., Stephens, W. Z., Soto, R., Bake, E., O'Connell, R. M. and Round, J. L., MyD88 signaling in T cells directs IgA-mediated control of the microbiota to promote health. Cell Host Microbe 2015. 17: 153-163.
Gutzeit, C., Magri, G. and Cerutti, A., Intestinal IgA production and its role in host-microbe interaction. Immunol. Rev. 2014. 260: 76-85.
Li, M. O. and Flavell, R. A., TGF-beta: a master of all T cell trades. Cell 2008. 134: 392-404.
Lecuyer, E., Rakotobe, S., Lengline-Garnier, H., Lebreton, C., Picard, M., Juste, C., Fritzen, R. et al., Segmented filamentous bacterium uses secondary and tertiary lymphoid tissues to induce gut IgA and specific T helper 17 cell responses. Immunity 2014. 40: 608-620.
Kim, M., Qie, Y., Park, J. and Kim, C. H., Gut microbial metabolites fuel host antibody responses. Cell Host Microbe 2016. 20: 202-214.
Moon, C., Baldridge, M. T., Wallace, M. A., Burnham, C. A., Virgin, H. W. and Stappenbeck, T. S., Vertically transmitted faecal IgA levels determine extra-chromosomal phenotypic variation. Nature 2015. 521: 90-93.
Caldwell, D. R. and Bryant, M. P., Medium without rumen fluid for nonselective enumeration and isolation of rumen bacteria. Appl. Microbiol. 1966. 14: 794-801.
Cossarizza, A., Chang, H. D., Radbruch, A., Acs, A., Adam, D., Adam-Klages, S., Agace, W. W. et al., Guidelines for the use of flow cytometry and cell sorting in immunological studies (second edition). Eur. J. Immunol. 2019. 49: 1457-1973.
Yang, Y. W., Chen, M. K., Yang, B. Y., Huang, X. J., Zhang, X. R., He, L. Q., Zhang, J. et al., Use of 16S rRNA gene-targeted group-specific primers for real-time PCR analysis of predominant bacteria in mouse feces. Appl. Environ. Microbiol. 2015. 81: 6749-6756.
Salzman, N. H., Hung, K., Haribhai, D., Chu, H., Karlsson-Sjoberg, J., Amir, E., Teggatz, P. et al., Enteric defensins are essential regulators of intestinal microbial ecology. Nat. Immunol. 2010. 11: 76-83.
Wang, Q., Garrity, G. M., Tiedje, J. M. and Cole, J. R., Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 2007. 73: 5261-5267.
McMurdie, P. J. and Holmes, S., phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One 2013. 8: e61217.