Therapeutic targeting of gut-originating regulatory B cells in neuroinflammatory diseases.
IL-10
microbiome
multiple sclerosis
neuroinflammation
regulatory B cells (Bregs)
Journal
European journal of immunology
ISSN: 1521-4141
Titre abrégé: Eur J Immunol
Pays: Germany
ID NLM: 1273201
Informations de publication
Date de publication:
11 2023
11 2023
Historique:
revised:
29
05
2023
received:
06
02
2023
accepted:
23
08
2023
medline:
2
11
2023
pubmed:
25
8
2023
entrez:
25
8
2023
Statut:
ppublish
Résumé
Regulatory B cells (Bregs) are immunosuppressive cells that support immunological tolerance by the production of IL-10, IL-35, and TGF-β. Bregs arise from different developmental stages in response to inflammatory stimuli. In that regard, mounting evidence points towards a direct influence of gut microbiota on mucosal B cell development, activation, and regulation in health and disease. While an increasing number of diseases are associated with alterations in gut microbiome (dysbiosis), little is known about the role of microbiota on Breg development and induction in neuroinflammatory disorders. Notably, gut-originating, IL-10- and IgA-producing regulatory plasma cells have recently been demonstrated to egress from the gut to suppress inflammation in the CNS raising fundamental questions about the triggers and functions of mucosal-originating Bregs in systemic inflammation. Advancing our understanding of Bregs in neuroinflammatory diseases could lead to novel therapeutic approaches. Here, we summarize the main aspects of Breg differentiation and functions and evidence about their involvement in neuroinflammatory diseases. Further, we highlight current data of gut-originating Bregs and their microbial interactions and discuss future microbiota-regulatory B cell-targeted therapies in immune-mediated diseases.
Identifiants
pubmed: 37624875
doi: 10.1002/eji.202250033
doi:
Substances chimiques
Interleukin-10
130068-27-8
Types de publication
Journal Article
Review
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e2250033Informations de copyright
© 2023 The Authors. European Journal of Immunology published by Wiley-VCH GmbH.
Références
Li, R., Patterson, K. R. and Bar-Or, A., Reassessing B cell contributions in multiple sclerosis. Nat. Immunol. 2018. 19: 696-707.
Sabatino, J. J., Pröbstel, A.-K. and Zamvil, S. S., B cells in autoimmune and neurodegenerative central nervous system diseases. Nat. Rev. Neurosci. 2019. 18: 123-745.
Pröbstel, A.-K. and Hauser, S. L., Multiple sclerosis: B cells take center stage. J. Neuroophthalmol. 2018. 38: 251-258.
Jelcic, I., Al Nimer, F., Wang, J., Lentsch, V., Planas, R., Jelcic, I., Madjovski, A. et al., Memory B cells activate brain-homing, autoreactive CD4+ T cells in multiple sclerosis. Cell 2018. 175: 85-100.e23.
Li, R., Rezk, A., Miyazaki, Y., Hilgenberg, E., Touil, H., Shen, P., Moore, C. S. et al., Proinflammatory GM-CSF-producing B cells in multiple sclerosis and B cell depletion therapy. Sci. Transl. Med. 2015. 7: 310ra166.
Pröbstel, A.-K., Zhou, X., Baumann, R., Wischnewski, S., Kutza, M., Rojas, O. L., Sellrie, K. et al., Gut microbiota-specific IgA(+) B cells traffic to the CNS in active multiple sclerosis. Sci. Immunol. 2020. 5: eabc7191.
Ramesh, A., Schubert, R. D., Greenfield, A. L., Dandekar, R., Loudermilk, R., Sabatino, J. J., Koelzer, M. T. et al., A pathogenic and clonally expanded B cell transcriptome in active multiple sclerosis. Proc. Natl. Acad. Sci. USA. 2020. 117: 22932-22943.
Rojas, O. L., Pröbstel, A.-K., Porfilio, E. A., Wang, A. A., Charabati, M., Sun, T., Lee, D. S. W. et al., Recirculating intestinal IgA-producing cells regulate neuroinflammation via IL-10. Cell 2019. 176: 610-624.e18.
Bar-Or, A. and Li, R., Cellular immunology of relapsing multiple sclerosis: interactions, checks and balances. Lancet Neurol. 2021. 20: 470-483.
Comi, G., Bar-Or, A., Lassmann, H., Uccelli, A., Hartung, H.-P., Montalban, X., Sørensen, P. S. et al., Role of B cells in multiple sclerosis and related disorders. Ann. Neurol. 2021. 89: 13-23.
Nashi, E., Wang, Y. and Diamond, B., The role of B cells in lupus pathogenesis. Int. J. Biochem. Cell Biol. 2010. 42: 543-550.
Katz, S. I., Parker, D. and Turk, J. L., B-cell suppression of delayed hypersensitivity reactions. Nature 1974. 251: 550-551.
Wolf, S. D., Dittel, B. N., Hardardottir, F. and Janeway, C. A., Experimental autoimmune encephalomyelitis induction in genetically B cell-deficient mice. J. Exp. Med. 1996. 184: 2271-2278.
Fillatreau, S., Sweenie, C. H., Mcgeachy, M. J., Gray, D. and Anderton, S. M., B cells regulate autoimmunity by provision of IL-10. Nat. Immunol. 2002. 3: 944-950.
Mizoguchi, A., Mizoguchi, E., Takedatsu, H., Blumberg, R. S. and Bhan, A. K., Chronic intestinal inflammatory condition generates IL-10-producing regulatory B cell subset characterized by CD1d upregulation. Immunity 2002. 16: 219-230.
Mauri, C., Gray, D., Mushtaq, N. and Londei, M., Prevention of arthritis by interleukin 10-producing B cells. J. Exp. Med. 2003. 197: 489-501.
Pröbstel, A.-K. and Baranzini, S. E., The role of the gut microbiome in multiple sclerosis risk and progression: Towards characterization of the “MS Microbiome.” Neurotherapeutics 2018. 15: 126-134.
Shalapour, S., Lin, X.-J., Bastian, I. N., Brain, J., Burt, A. D., Aksenov, A. A., Vrbanac, A. et al., Inflammation-induced IgA+ cells dismantle anti-liver cancer immunity. Nature 2017. 551: 340-345.
Shen, P., Roch, T., Lampropoulou, V., O'connor, R. A., Stervbo, U., Hilgenberg, E., Ries, S. et al., IL-35-producing B cells are critical regulators of immunity during autoimmune and infectious diseases. Nature 2014. 507: 366-370.
Parekh, V. V., Prasad, D. V. R., Banerjee, P. P., Joshi, B. N., Kumar, A. and Mishra, G. C., B cells activated by lipopolysaccharide, but not by anti-Ig and anti-CD40 antibody, induce anergy in CD8+ T cells: Role of TGF-beta 1. J. Immunol. 2003. 170: 5897-5911.
Ding, Q., Yeung, M., Camirand, G., Zeng, Q., Akiba, H., Yagita, H. and Chalasani, G., Regulatory B cells are identified by expression of TIM-1 and can be induced through TIM-1 ligation to promote tolerance in mice. J. Clin. Invest. 2011. 121: 3645-3656.
Xiao, S., Brooks, C. R., Sobel, R. A. and Kuchroo, V. K., Tim-1 is essential for induction and maintenance of IL-10 in regulatory B cells and their regulation of tissue inflammation. J. Immunol. 2015. 194: 1602-1608.
Aravena, O., Ferrier, A., Menon, M., Mauri, C., Aguillón, J. C., Soto, L. and Catalán, D., TIM-1 defines a human regulatory B cell population that is altered in frequency and function in systemic sclerosis patients. Arthritis Res. Ther. 2017. 19: 8.
Blair, P. A., Noreña, L. Y., Flores-Borja, F., Rawlings, D. J., Isenberg, D. A., Ehrenstein, M. R. and Mauri, C., CD19(+)CD24(hi)CD38(hi) B cells exhibit regulatory capacity in healthy individuals but are functionally impaired in systemic lupus erythematosus patients. Immunity 2010. 32: 129-140.
Iwata, Y., Matsushita, T., Horikawa, M., Dilillo, D. J., Yanaba, K., Venturi, G. M., Szabolcs, P. M. et al., Characterization of a rare IL-10-competent B-cell subset in humans that parallels mouse regulatory B10 cells. Blood 2011. 117: 530-541.
Lindner, S., Dahlke, K., Sontheimer, K., Hagn, M., Kaltenmeier, C., Barth, T. F. E., Beyer, T. et al., Interleukin 21-induced granzyme B-expressing B cells infiltrate tumors and regulate T cells. Cancer Res. 2013. 73: 2468-2479.
Mauri, C. and Menon, M., Human regulatory B cells in health and disease: Therapeutic potential. J. Clin. Invest. 2017. 127: 772-779.
Fillatreau, S., Regulatory functions of B cells and regulatory plasma cells. Biomed J 2019. 42: 233-242.
Matsumura, Y., Watanabe, R. and Fujimoto, M., Suppressive mechanisms of regulatory B cells in mice and humans. Int. Immunol. 2023. 35: 55-65.
Yoshizaki, A., Miyagaki, T., Dilillo, D. J., Matsushita, T., Horikawa, M., Kountikov, E. I., Spolski, R. et al., Regulatory B cells control T-cell autoimmunity through IL-21-dependent cognate interactions. Nature 2012. 491: 264-268.
Yanaba, K., Bouaziz, J.-D., Haas, K. M., Poe, J. C., Fujimoto, M. and Tedder, T. F., A regulatory B cell subset with a unique CD1dhiCD5+ phenotype controls T cell-dependent inflammatory responses. Immunity 2008. 28: 639-650.
Gray, M., Miles, K., Salter, D., Gray, D. and Savill, J., Apoptotic cells protect mice from autoimmune inflammation by the induction of regulatory B cells. Proc. Natl. Acad. Sci. USA. 2007. 104: 14080-14085.
Rosser, E. C., Oleinika, K., Tonon, S., Doyle, R., Bosma, A., Carter, N. A., Harris, K. A. et al., Regulatory B cells are induced by gut microbiota-driven interleukin-1β and interleukin-6 production. Nat. Med. 2014. 20: 1334-1339.
Matsumoto, M., Baba, A., Yokota, T., Nishikawa, H., Ohkawa, Y., Kayama, H., Kallies, A. et al., Interleukin-10-producing plasmablasts exert regulatory function in autoimmune inflammation. Immunity 2014. 41: 1040-1051.
Kalampokis, I., Yoshizaki, A. and Tedder, T. F., IL-10-producing regulatory B cells (B10 cells) in autoimmune disease. Arthritis Res. Ther. 2013. 15(Suppl): S1.
Shalapour, S., Font-Burgada, J., Di Caro, G., Zhong, Z., Sanchez-Lopez, E., Dhar, D., Willimsky, G. et al., Immunosuppressive plasma cells impede T-cell-dependent immunogenic chemotherapy. Nature 2015. 521: 94-98.
Rosser, E. C. and Mauri, C., Regulatory B cells: Origin, phenotype and function. Immunity 2015. 42: 607-612.
Yanaba, K., Bouaziz, J.-D., Matsushita, T., Tsubata, T. and Tedder, T. F., The development and function of regulatory B cells expressing IL-10 (B10 cells) requires antigen receptor diversity and TLR signals. J. Immunol. 2009. 182: 7459-7472.
Matsushita, T., Horikawa, M., Iwata, Y. and Tedder, T. F., Regulatory B cells (B10 cells) and regulatory T cells have independent roles in controlling experimental autoimmune encephalomyelitis initiation and late-phase immunopathogenesis. J. Immunol. 2010. 185: 2240-2252.
Lampropoulou, V., Hoehlig, K., Roch, T., Neves, P., Gómez, E. C., Sweenie, C. H., Hao, Y. et al., TLR-activated B cells suppress T cell-mediated autoimmunity. J. Immunol. 2008. 180: 4763-4773.
Radomir, L., Kramer, M. P., Perpinial, M., Schottlender, N., Rabani, S., David, K., Wiener, A. et al., The survival and function of IL-10-producing regulatory B cells are negatively controlled by SLAMF5. Nat. Commun. 2021. 12: 1893.
Menon, M., Blair, P. A., Isenberg, D. A. and Mauri, C., A regulatory feedback between plasmacytoid dendritic cells and regulatory B cells is aberrant in systemic lupus erythematosus. Immunity 2016. 44: 683-697.
Yang, M., Sun, L., Wang, S., Ko, K.-H., Xu, H., Zheng, B.-J, Cao, X. et al., Novel function of B cell-activating factor in the induction of IL-10-producing regulatory B cells. J. Immunol. 2010. 184: 3321-3325.
Burrows, N., Bashford-Rogers, R. J. M., Bhute, V. J., Peñalver, A., Ferdinand, J. R., Stewart, B. J., Smith, J. E. G. et al., Dynamic regulation of hypoxia-inducible factor-1α activity is essential for normal B cell development. Nat. Immunol. 2020. 21: 1408-1420.
Meng, X., Grötsch, B., Luo, Y., Knaup, K. X., Wiesener, M. S., Chen, X.-X., Jantsch, J. et al., Hypoxia-inducible factor-1α is a critical transcription factor for IL-10-producing B cells in autoimmune disease. Nat. Commun. 2018. 9: 251.
Wang, R.-X., Yu, C.-R., Dambuza, I. M., Mahdi, R. M., Dolinska, M. B., Sergeev, Y. V., Wingfield, P. T. et al., Interleukin-35 induces regulatory B cells that suppress autoimmune disease. Nat. Med. 2014. 20: 633-641.
Carter, N. A., Vasconcellos, R., Rosser, E. C., Tulone, C., Muñoz-Suano, A., Kamanaka, M., Ehrenstein, M. R. et al., Mice lacking endogenous IL-10-producing regulatory B cells develop exacerbated disease and present with an increased frequency of Th1/Th17 but a decrease in regulatory T cells. J. Immunol. 2011. 186: 5569-5579.
Tadmor, T., Zhang, Y., Cho, H.-M., Podack, E. R. and Rosenblatt, J. D., The absence of B lymphocytes reduces the number and function of T-regulatory cells and enhances the anti-tumor response in a murine tumor model. Cancer Immunol. Immunother. 2011. 60: 609-619.
Mann, M. K., Maresz, K., Shriver, L. P., Tan, Y. and Dittel, B. N., B cell regulation of CD4+CD25+ T regulatory cells and IL-10 via B7 is essential for recovery from experimental autoimmune encephalomyelitis. J. Immunol. 2007. 178: 3447-3456.
Flores-Borja, F., Bosma, A., Ng, D., Reddy, V., Ehrenstein, M. R., Isenberg, D. A. and Mauri, C., CD19+CD24hiCD38hi B cells maintain regulatory T cells while limiting TH1 and TH17 differentiation. Sci. Transl. Med. 2013. 5: 173ra23.
Chen, X. and Jensen, P. E., Cutting edge: Primary B lymphocytes preferentially expand allogeneic FoxP3+ CD4 T cells. J. Immunol. 2007. 179: 2046-2050.
Bosma, A., Abdel-Gadir, A., Isenberg, D. A., Jury, E. C. and Mauri, C., Lipid-antigen presentation by CD1d(+) B cells is essential for the maintenance of invariant natural killer T cells. Immunity 2012. 36: 477-490.
Pennati, A., Nylen, E. A., Duncan, I. D. and Galipeau, J., Regulatory B cells normalize CNS myeloid cell content in a mouse model of multiple sclerosis and promote oligodendrogenesis and remyelination. J. Neurosci. 2020. 40: 5105-5115.
Lassmann, H. and Bradl, M., Multiple sclerosis: Experimental models and reality. Acta Neuropathol. 2017. 133: 223-244.
Steinman, L., Patarca, R. and Haseltine, W., Experimental encephalomyelitis at age 90, still relevant and elucidating how viruses trigger disease. J. Exp. Med. 2023. 220: e20221322.
Hauser, S. L., Bar-Or, A., Comi, G., Giovannoni, G., Hartung, H.-P., Hemmer, B., Lublin, F. et al., Ocrelizumab versus interferon beta-1a in relapsing multiple sclerosis. N. Engl. J. Med. 2017. 376: 221-234.
Montalban, X., Hauser, S. L., Kappos, L., Arnold, D. L., Bar-Or, A., Comi, G., De Seze, J. et al., Ocrelizumab versus placebo in primary progressive multiple sclerosis. N. Engl. J. Med. 2017. 376: 209-220.
Kappos, L., Hartung, H.-P., Freedman, M. S., Boyko, A., Radü, E. W., Mikol, D. D., Lamarine, M. et al., Atacicept in multiple sclerosis (ATAMS): A randomised, placebo-controlled, double-blind, phase 2 trial. Lancet Neurol. 2014. 13: 353-363.
Matsushita, T., Yanaba, K., Bouaziz, J.-D., Fujimoto, M. and Tedder, T. F., Regulatory B cells inhibit EAE initiation in mice while other B cells promote disease progression. J. Clin. Invest. 2008. 118: 3420-3430.
Weber, M. S., Prod'homme, T., Patarroyo, J. C., Molnarfi, N., Karnezis, T., Lehmann-Horn, K., Danilenko, D. M. et al., B-cell activation influences T-cell polarization and outcome of anti-CD20 B-cell depletion in central nervous system autoimmunity. Ann. Neurol. 2010. 68: 369-383.
Molnarfi, N., Schulze-Topphoff, U., Weber, M. S., Patarroyo, J. C., Prod'homme, T., Varrin-Doyer, M., Shetty, A. et al., MHC class II-dependent B cell APC function is required for induction of CNS autoimmunity independent of myelin-specific antibodies. J. Exp. Med. 2013. 210: 2921-2937.
Correale, J., Farez, M. and Razzitte, G., Helminth infections associated with multiple sclerosis induce regulatory B cells. Ann. Neurol. 2008. 64: 187-199.
Staun-Ram, E. and Miller, A., Effector and regulatory B cells in multiple sclerosis. Clin. Immunol. 2017. 184: 11-25.
Knippenberg, S., Peelen, E., Smolders, J., Thewissen, M., Menheere, P., Cohen Tervaert, J. W., Hupperts, R. et al., Reduction in IL-10 producing B cells (Breg) in multiple sclerosis is accompanied by a reduced naïve/memory Breg ratio during a relapse but not in remission. J. Neuroimmunol. 2011. 239: 80-86.
Duddy, M., Niino, M., Adatia, F., Hebert, S., Freedman, M., Atkins, H., Kim, H. J et al., Distinct effector cytokine profiles of memory and naive human B cell subsets and implication in multiple sclerosis. J. Immunol. 2007. 178: 6092-6099.
Michel, L., Chesneau, M., Manceau, P., Genty, A., Garcia, A., Salou, M., Elong Ngono, A. et al., Unaltered regulatory B-cell frequency and function in patients with multiple sclerosis. Clin. Immunol. 2014. 155: 198-208.
De Andrés, C., Tejera-Alhambra, M., Alonso, B., Valor, L., Teijeiro, R., Ramos-Medina, R., Mateos, D. et al., New regulatory CD19(+)CD25(+) B-cell subset in clinically isolated syndrome and multiple sclerosis relapse. Changes after glucocorticoids. J. Neuroimmunol. 2014. 270: 37-44.
Machado-Santos, J., Saji, E., Tröscher, A. R., Paunovic, M., Liblau, R., Gabriely, G., Bien, C. G. et al., The compartmentalized inflammatory response in the multiple sclerosis brain is composed of tissue-resident CD8+ T lymphocytes and B cells. Brain 2018. 141: 2066-2082.
Schubert, R. D., Hu, Y., Kumar, G., Szeto, S., Abraham, P., Winderl, J., Guthridge, J. M. et al., IFN-β treatment requires B cells for efficacy in neuroautoimmunity. J. Immunol. 2015. 194: 2110-2116.
Grützke, B., Hucke, S., Gross, C. C., Herold, M. V. B., Posevitz-Fejfar, A., Wildemann, B. T., Kieseier, B. C. et al., Fingolimod treatment promotes regulatory phenotype and function of B cells. Ann. Clin. Transl. Neurol. 2015. 2: 119-130.
Heidt, S., Hester, J., Shankar, S., Friend, P. J. and Wood, K. J., B cell repopulation after alemtuzumab induction-transient increase in transitional B cells and long-term dominance of naïve B cells. Am. J. Transplant. 2012. 12: 1784-1792.
Guerrier, T., Labalette, M., Launay, D., Lee-Chang, C., Outteryck, O., Lefèvre, G., Vermersch, P. et al., Proinflammatory B-cell profile in the early phases of MS predicts an active disease. Neurol. Neuroimmunol. Neuroinflamm. 2018. 5: e431.
Kim, Y., Kim, G., Shin, H.-J., Hyun, J.-W., Kim, S.-H, Lee, E. and Kim, H. J., Restoration of regulatory B cell deficiency following alemtuzumab therapy in patients with relapsing multiple sclerosis. J. Neuroinflamm. 2018. 15: 300.
Wingerchuk, D. M., Banwell, B., Bennett, J. L., Cabre, P., Carroll, W., Chitnis, T., De Seze, J. et al., International consensus diagnostic criteria for neuromyelitis optica spectrum disorders. Neurology 2015. 85: 177-189.
Lennon, V. A., Wingerchuk, D. M., Kryzer, T. J., Pittock, S. J., Lucchinetti, C. F., Fujihara, K., Nakashima, I. et al., A serum autoantibody marker of neuromyelitis optica: distinction from multiple sclerosis. Lancet 2004. 364: 2106-2112.
Pröbstel, A.-K., Rudolf, G., Dornmair, K., Collongues, N., Chanson, J.-B., Sanderson, N. S., Lindberg, R. L. et al., Anti-MOG antibodies are present in a subgroup of patients with a neuromyelitis optica phenotype. J. Neuroinflamm. 2015. 12: 46.
Borisow, N., Mori, M., Kuwabara, S., Scheel, M. and Paul, F., Diagnosis and treatment of NMO spectrum disorder and MOG-encephalomyelitis. Front. Neurol. 2018. 9: 888.
Weber, M. S., Derfuss, T., Metz, I. and Brück, W., Defining distinct features of anti-MOG antibody associated central nervous system demyelination. Ther. Adv. Neurol. Disord. 2018. 11: 175628641876208.
Banwell, B., Bennett, J. L., Marignier, R., Kim, H. J., Brilot, F., Flanagan, E. P., Ramanathan, S. et al., Diagnosis of myelin oligodendrocyte glycoprotein antibody-associated disease: International MOGAD Panel proposed criteria. Lancet Neurol. 2023. 22: 268-282.
Marignier, R., Hacohen, Y., Cobo-Calvo, A., Pröbstel, A.-K., Aktas, O., Alexopoulos, H., Amato, M.-P. et al., Myelin-oligodendrocyte glycoprotein antibody-associated disease. Lancet Neurol. 2021. 20: 762-772.
Cho, E. B., Cho, H.-J., Seok, J. M., Min, J.-H., Kang, E.-S. and Kim, B. J., The IL-10-producing regulatory B cells (B10 cells) and regulatory T cell subsets in neuromyelitis optica spectrum disorder. Neurol. Sci. 2018. 39: 543-549.
Kim, Y., Kim, S. Y, Han, S.-M., Payumo, R. M., Park, K., Kim, H. E, Kim, S.-H et al., Functional impairment of CD19(+)CD24(hi)CD38(hi) B cells in neuromyelitis optica spectrum disorder is restored by B cell depletion therapy. Sci. Transl. Med. 2021. 13: eabk2132.
Quan, C., Yu, H., Qiao, J., Xiao, B., Zhao, G., Wu, Z., Li, Z. et al., Impaired regulatory function and enhanced intrathecal activation of B cells in neuromyelitis optica: distinct from multiple sclerosis. Mult. Scler. 2013. 19: 289-298.
Tedder, T. F., B10 cells: A functionally defined regulatory B cell subset. J. Immunol. 2015. 194: 1395-1401.
Teichmann, L. L., Kashgarian, M., Weaver, C. T., Roers, A., Müller, W. and Shlomchik, M. J., B cell-derived IL-10 does not regulate spontaneous systemic autoimmunity in MRL.Fas(lpr) mice. J. Immunol. 2012. 188: 678-685.
Mao, H., Pan, F., Wu, Z., Wang, Z., Zhou, Y., Zhang, P., Gou, M. et al., Colorectal tumors are enriched with regulatory plasmablasts with capacity in suppressing T cell inflammation. Int. Immunopharmacol. 2017. 49: 95-101.
Millet, N., Solis, N. V. and Swidergall, M., Mucosal IgA prevents commensal Candida albicans dysbiosis in the oral cavity. Front. Immunol. 2020. 11: 555363.
Fitzpatrick, Z., Frazer, G., Ferro, A., Clare, S., Bouladoux, N., Ferdinand, J., Tuong, Z. K. et al., Gut-educated IgA plasma cells defend the meningeal venous sinuses. Nature 2020. 587: 472-476.
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.
Hansen, I. S., Baeten, D. L. P. and Den Dunnen, J., The inflammatory function of human IgA. Cell. Mol. Life Sci. 2019. 76: 1041-1055.
Moor, K., Diard, M., Sellin, M. E., Felmy, B., Wotzka, S. Y., Toska, A., Bakkeren, E. et al., High-avidity IgA protects the intestine by enchaining growing bacteria. Nature 2017. 544: 498-502.
Gutzeit, C., Magri, G. and Cerutti, A., Intestinal IgA production and its role in host-microbe interaction. Immunol. Rev. 2014. 260: 76-85.
Pabst, O. and Slack, E., IgA and the intestinal microbiota: the importance of being specific. Mucosal Immunol. 2020. 13: 12-21.
Russell, M. W., Reinholdt, J. and Kilian, M., Anti-inflammatory activity of human IgA antibodies and their Fab alpha fragments: inhibition of IgG-mediated complement activation. Eur. J. Immunol. 1989. 19: 2243-2249.
Pilette, C., Detry, B., Guisset, A., Gabriels, J. and Sibille, Y., Induction of interleukin-10 expression through Fcalpha receptor in human monocytes and monocyte-derived dendritic cells: Role of p38 MAPKinase. Immunol. Cell Biol. 2010. 88: 486-493.
Lecocq, M., Detry, B., Guisset, A. and Pilette, C., FcαRI-mediated inhibition of IL-12 production and priming by IFN-γ of human monocytes and dendritic cells. J. Immunol. 2013. 190: 2362-2371.
Hansen, I. S., Hoepel, W., Zaat, S. A. J., Baeten, D. L. P. and Den Dunnen, J., Serum IgA immune complexes promote proinflammatory cytokine production by human macrophages, monocytes, and kupffer cells through FcαRI-TLR cross-talk. J. Immunol. 2017. 199: 4124-4131.
Keler, T., Wallace, P. K., Vitale, L. A., Russoniello, C., Sundarapandiyan, K., Graziano, R. F. and Deo, Y. M., Differential effect of cytokine treatment on Fc alpha receptor I- and Fc gamma receptor I-mediated tumor cytotoxicity by monocyte-derived macrophages. J. Immunol. 2000. 164: 5746-5752.
Monteiro, R. C. and Van De Winkel, J. G. J., IgA Fc receptors. Annu. Rev. Immunol. 2003. 21: 177-204.
Steffen, U., Koeleman, C. A., Sokolova, M. V., Bang, H., Kleyer, A., Rech, J., Unterweger, H. et al., IgA subclasses have different effector functions associated with distinct glycosylation profiles. Nat. Commun. 2020. 11: 120.
Lycke, N. Y. and Bemark, M., The regulation of gut mucosal IgA B-cell responses: Recent developments. Mucosal Immunol. 2017. 10: 1361-1374.
Lee, C. M. and Oh, J. E., Resident memory B cells in barrier tissues. Front. Immunol. 2022. 13: 953088.
Bunker, J. J. and Bendelac, A., IgA responses to microbiota. Immunity 2018. 49: 211-224.
Cong, Y., Feng, T., Fujihashi, K., Schoeb, T. R. and Elson, C. O., A dominant, coordinated T regulatory cell-IgA response to the intestinal microbiota. Proc. Natl. Acad. Sci. USA. 2009. 106: 19256-19261.
Tyler, C. J., Guzman, M., Lundborg, L. R., Yeasmin, S., Zgajnar, N., Jedlicka, P., Bamias, G. et al., Antibody secreting cells are critically dependent on integrin α4β7/MAdCAM-1 for intestinal recruitment and control of the microbiota during chronic colitis. Mucosal Immunol 2022. 15: 109-119.
Cazac, B. B. and Roes, J., TGF-beta receptor controls B cell responsiveness and induction of IgA in vivo. Immunity 2000. 13: 443-451.
Marie, J. C., Liggitt, D. and Rudensky, A. Y., Cellular mechanisms of fatal early-onset autoimmunity in mice with the T cell-specific targeting of transforming growth factor-β receptor. Immunity 2006. 25: 441-454.
Shull, M. M., Ormsby, I., Kier, A. B., Pawlowski, S., Diebold, R. J., Yin, M., Allen, R. et al., Targeted disruption of the mouse transforming growth factor-beta 1 gene results in multifocal inflammatory disease. Nature 1992. 359: 693-699.
Tezuka, H., Abe, Y., Iwata, M., Takeuchi, H., Ishikawa, H., Matsushita, M., Shiohara, T. et al., Regulation of IgA production by naturally occurring TNF/iNOS-producing dendritic cells. Nature 2007. 448: 929-933.
Castigli, E., Wilson, S. A., Scott, S., Dedeoglu, F., Xu, S., Lam, K.-P., Bram, R. J. et al., TACI and BAFF-R mediate isotype switching in B cells. J. Exp. Med. 2005. 201: 35-39.
Pantazi, E., Marks, E., Stolarczyk, E., Lycke, N., Noelle, R. J. and Elgueta, R., Cutting edge: Retinoic acid signaling in B cells is essential for oral immunization and microflora composition. J. Immunol. 2015. 195: 1368-1371.
Seo, G.-Y., Jang, Y.-S., Kim, H.-A., Lee, M.-R., Park, M.-H., Park, S.-R., Lee, J.-M. et al., Retinoic acid, acting as a highly specific IgA isotype switch factor, cooperates with TGF-β1 to enhance the overall IgA response. J. Leukoc. Biol. 2013. 94: 325-335.
Kim, M., Qie, Y., Park, J. and Kim, C. H., Gut microbial metabolites fuel host antibody responses. Cell Host Microbe 2016. 20: 202-214.
Zhou, X., Baumann, R., Gao, X., Mendoza, M., Singh, S., Katz Sand, I., Xia, Z. et al., Gut microbiome of multiple sclerosis patients and paired household healthy controls reveal associations with disease risk and course. Cell 2022. 185: 3467-3486.e16.
Zundler, S., Günther, C., Kremer, A. E., Zaiss, M. M., Rothhammer, V. and Neurath, M. F., Gut immune cell trafficking: Inter-organ communication and immune-mediated inflammation. Nat. Rev. Gastroenterol. Hepatol. 2023. 20:50-64.
Antonini, M., Lo Conte, M., Sorini, C. and Falcone, M., How the interplay between the commensal microbiota, gut barrier integrity and mucosal immunity regulates brain autoimmunity. Front. Immunol. 2019. 10: 1937.
Berer, K., Mues, M., Koutrolos, M., Rasbi, Z. A., Boziki, M., Johner, C., Wekerle, H. et al., Commensal microbiota and myelin autoantigen cooperate to trigger autoimmune demyelination. Nature 2011. 479: 538-541.
Berer, K., Gerdes, L. A., Cekanaviciute, E., Jia, X., Xiao, L., Xia, Z., Liu, C. et al., Gut microbiota from multiple sclerosis patients enables spontaneous autoimmune encephalomyelitis in mice. Proc. Natl. Acad. Sci. USA. 2017. 114: 10719-10724.
Cekanaviciute, E., Yoo, B. B., Runia, T. F., Debelius, J. W., Singh, S., Nelson, C. A., Kanner, R. et al., Gut bacteria from multiple sclerosis patients modulate human T cells and exacerbate symptoms in mouse models. Proc. Natl. Acad. Sci. USA. 2017. 114: 10713-10718.
Diebold, M., Meola, M., Purushothaman, S., Siewert, L. K., Pössnecker, E., Roloff, T., Lindberg, R. L. et al., Gut microbiota composition as a candidate risk factor for dimethyl fumarate-induced lymphopenia in multiple sclerosis. Gut Microbes 2022. 14: 2147055.
Jangi, S., Gandhi, R., Cox, L. M., Li, N., Von Glehn, F., Yan, R., Patel, B. et al., Alterations of the human gut microbiome in multiple sclerosis. Nat. Commun. 2016. 7: 12015.
Round, J. L. and Mazmanian, S. K., Inducible Foxp3+ regulatory T-cell development by a commensal bacterium of the intestinal microbiota. Proc. Natl. Acad. Sci. USA. 2010. 107: 12204-12209.
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.
Cekanaviciute, E., Pröbstel, A.-K., Thomann, A., Runia, T. F., Casaccia, P., Katz Sand, I., Crabtree, E. et al., Multiple sclerosis-associated changes in the composition and immune functions of spore-forming bacteria. mSystems 2018. 3: 18-e00083.
Rothhammer, V., Borucki, D. M., Tjon, E. C., Takenaka, M. C., Chao, C.-C., Ardura-Fabregat, A., De Lima, K. A. et al., Microglial control of astrocytes in response to microbial metabolites. Nature 2018. 557: 724-728.
Haghikia, A., Jörg, S., Duscha, A., Berg, J., Manzel, A., Waschbisch, A., Hammer, A. et al., Dietary fatty acids directly impact central nervous system autoimmunity via the small intestine. Immunity 2015. 43: 817-829.
Buscarinu, M. C., Cerasoli, B., Annibali, V., Policano, C., Lionetto, L., Capi, M., Mechelli, R. et al., Altered intestinal permeability in patients with relapsing-remitting multiple sclerosis: A pilot study. Mult. Scler. 2017. 23: 442-446.
Manfredo Vieira, S., Hiltensperger, M., Kumar, V., Zegarra-Ruiz, D., Dehner, C., Khan, N., Costa, F. R. C. et al., Translocation of a gut pathobiont drives autoimmunity in mice and humans. Science 2018. 359: 1156-1161.
Nouri, M., Bredberg, A., Weström, B. and Lavasani, S., Intestinal barrier dysfunction develops at the onset of experimental autoimmune encephalomyelitis and can be induced by adoptive transfer of auto-reactive T cells. PLoS One 2014. 9: e106335.
Camara-Lemarroy, C. R., Silva, C., Greenfield, J., Liu, W.-Q., Metz, L. M. and Yong, V. W., Biomarkers of intestinal barrier function in multiple sclerosis are associated with disease activity. Mult. Scler. 2020. 26: 1340-1350.
Cree, B. A. C., Spencer, C. M., Varrin-Doyer, M., Baranzini, S. E. and Zamvil, S. S., Gut microbiome analysis in neuromyelitis optica reveals overabundance of Clostridium perfringens. Ann. Neurol. 2016. 80: 443-447.
Zamvil, S. S., Spencer, C. M., Baranzini, S. E. and Cree, B. A. C., The gut microbiome in neuromyelitis optica. Neurotherapeutics 2018. 15: 92-101.
Varrin-Doyer, M., Spencer, C. M., Schulze-Topphoff, U., Nelson, P. A., Stroud, R. M., C Cree, B. A. and Zamvil, S. S., Aquaporin 4-specific T cells in neuromyelitis optica exhibit a Th17 bias and recognize Clostridium ABC transporter. Ann. Neurol. 2012. 72: 53-64.
Breithaupt, C., Schubart, A., Zander, H., Skerra, A., Huber, R., Linington, C. and Jacob, U., Structural insights into the antigenicity of myelin oligodendrocyte glycoprotein. Proc. Natl. Acad. Sci. USA. 2003. 100: 9446-9451.
Miyauchi, E., Kim, S.-W., Suda, W., Kawasumi, M., Onawa, S., Taguchi-Atarashi, N., Morita, H. et al., Gut microorganisms act together to exacerbate inflammation in spinal cords. Nature 2020. 585: 102-106.
Hughes, L., Cross-reactivity between related sequences found in Acinetobacter sp., Pseudomonas aeruginosa, myelin basic protein and myelin oligodendrocyte glycoprotein in multiple sclerosis. J. Neuroimmunol. 2003. 144: 105-115.
Kim, M. and Kim, C. H., Regulation of humoral immunity by gut microbial products. Gut Microbes 2017. 8: 392-399.
Maerz, J. K., Trostel, C., Lange, A., Parusel, R., Michaelis, L., Schäfer, A., Yao, H. et al., Bacterial immunogenicity is critical for the induction of regulatory B cells in suppressing inflammatory immune responses. Front. Immunol. 2019. 10: 3093.
Piper, C. J. M., Rosser, E. C., Oleinika, K., Nistala, K., Krausgruber, T., Rendeiro, A. F., Banos, A. et al., Aryl hydrocarbon receptor contributes to the transcriptional program of IL-10-producing regulatory B cells. Cell Rep. 2019. 29: 1878-1892.e7.
Rosser, E. C., Piper, C. J. M., Matei, D. E., Blair, P. A., Rendeiro, A. F., Orford, M., Alber, D. G. et al., Microbiota-derived metabolites suppress arthritis by amplifying aryl-hydrocarbon receptor activation in regulatory B cells. Cell Metab. 2020. 31: 837-851.e10.
Sterlin, D., Fadlallah, J., Slack, E. and Gorochov, G., The antibody/microbiota interface in health and disease. Mucosal Immunol. 2020. 13: 3-11.
Mei, H. E., Yoshida, T., Sime, W., Hiepe, F., Thiele, K., Manz, R. A., Radbruch, A. et al., Blood-borne human plasma cells in steady state are derived from mucosal immune responses. Blood 2009. 113: 2461-2469.
Mei, H. E., Hahne, S., Redlin, A., Hoyer, B. F., Wu, K., Baganz, L., Lisney, A. R. et al., Plasmablasts with a mucosal phenotype contribute to plasmacytosis in systemic lupus erythematosus. Arthritis Rheumatol 2017. 69: 2018-2028.
Bashford-Rogers, R. J. M., Bergamaschi, L., Mckinney, E. F., Pombal, D. C., Mescia, F., Lee, J. C., Thomas, D. C. et al., Analysis of the B cell receptor repertoire in six immune-mediated diseases. Nature 2019. 574: 122-126.
Quintana, J. F., Chandrasegaran, P., Sinton, M. C., Briggs, E. M., Otto, T. D., Heslop, R., Bentley-Abbot, C. et al., Single cell and spatial transcriptomic analyses reveal microglia-plasma cell crosstalk in the brain during Trypanosoma brucei infection. Nat. Commun. 2022. 13: 5752.
Wang, Y., Chen, D., Xu, D., Huang, C., Xing, R., He, D. and Xu, H., Early developing B cells undergo negative selection by central nervous system-specific antigens in the meninges. Immunity 2021. 54: 2784-2794.e6.
Brioschi, S., Wang, W.-L., Peng, V., Wang, M., Shchukina, I., Greenberg, Z. J., Bando, J. K. et al., Heterogeneity of meningeal B cells reveals a lymphopoietic niche at the CNS borders. Science 2021. 373: eabf9277.
Muñoz, Ú., Sebal, C., Escudero, E., García Sánchez, M. I., Urcelay, E., Jayo, A., Arroyo, R. et al., High prevalence of intrathecal IgA synthesis in multiple sclerosis patients. Sci. Rep. 2022. 12: 4247.
Kroth, J., Ciolac, D., Fleischer, V., Koirala, N., Krämer, J., Muthuraman, M., Luessi, F. et al., Increased cerebrospinal fluid albumin and immunoglobulin A fractions forecast cortical atrophy and longitudinal functional deterioration in relapsing-remitting multiple sclerosis. Mult. Scler. 2019. 25: 338-343.
Abdelhak, A., Hottenrott, T., Mayer, C., Hintereder, G., Zettl, U. K., Stich, O. and Tumani, H., CSF profile in primary progressive multiple sclerosis: Re-exploring the basics. PLoS One 2017. 12: e0182647.
Cross, A. H., Stark, J. L., Lauber, J., Ramsbottom, M. J. and Lyons, J.-A., Rituximab reduces B cells and T cells in cerebrospinal fluid of multiple sclerosis patients. J. Neuroimmunol. 2006. 180: 63-70.
Mdel, M. P., Cravens, P. D., Winger, R., Kieseier, B. C., Cepok, S., Eagar, T. N., Zamvil, S. S. et al., Depletion of B lymphocytes from cerebral perivascular spaces by rituximab. Arch. Neurol. 2009. 66: 1016-1020.
Hofmann, K., Clauder, A.-K. and Manz, R. A., Targeting B cells and plasma cells in autoimmune diseases. Front. Immunol. 2018. 9: 835.
Pellkofer, H. L., Krumbholz, M., Berthele, A., Hemmer, B., Gerdes, L. A., Havla, J., Bittner, R. et al., Long-term follow-up of patients with neuromyelitis optica after repeated therapy with rituximab. Neurology 2011. 76: 1310-1315.
Tahara, M., Oeda, T., Okada, K., Kiriyama, T., Ochi, K., Maruyama, H., Fukaura, H. et al., Safety and efficacy of rituximab in neuromyelitis optica spectrum disorders (RIN-1 study): A multicentre, randomised, double-blind, placebo-controlled trial. Lancet Neurol. 2020. 19: 298-306.
Krumbholz, M., Faber, H., Steinmeyer, F., Hoffmann, L.-A., Kümpfel, T., Pellkofer, H., Derfuss, T. et al., Interferon-beta increases BAFF levels in multiple sclerosis: implications for B cell autoimmunity. Brain 2008. 131(Pt): 1455-1463.
Barr, T. A., Shen, P., Brown, S., Lampropoulou, V., Roch, T., Lawrie, S., Fan, B. et al., B cell depletion therapy ameliorates autoimmune disease through ablation of IL-6-producing B cells. J. Exp. Med. 2012. 209: 1001-1010.
Shinoda, K., Li, R., Rezk, A., Mexhitaj, I., Patterson, K. R., Kakara, M., Zuroff, L. et al., Differential effects of anti-CD20 therapy on CD4 and CD8 T cells and implication of CD20-expressing CD8 T cells in MS disease activity. Proc. Natl. Acad. Sci. USA. 2023. 120: e2207291120.
Ho, S., Oswald, E., Wong, H. K., Vural, A., Yilmaz, V., Tüzün, E., Türkoğlu, R. et al., Ocrelizumab treatment modulates B-cell regulating factors in multiple sclerosis. Neurol. Neuroimmunol. Neuroinflamm. 2023. 10: e200083.
Lavie, F., Miceli-Richard, C., Ittah, M., Sellam, J., Gottenberg, J.-E. and Mariette, X., Increase of B cell-activating factor of the TNF family (BAFF) after rituximab treatment: insights into a new regulating system of BAFF production. Ann. Rheum. Dis. 2007. 66: 700-702.
Petereit, H. and Rubbert-Roth, A., Rituximab levels in cerebrospinal fluid of patients with neurological autoimmune disorders. Mult. Scler. 2009. 15: 189-192.
Michel, L., Touil, H., Pikor, N. B., Gommerman, J. L., Prat, A. and Bar-Or, A., B cells in the multiple sclerosis central nervous system: Trafficking and contribution to CNS-compartmentalized inflammation. Front. Immunol. 2015. 6: 636-636.
Serafini, B., Rosicarelli, B., Magliozzi, R., Stigliano, E. and Aloisi, F., Detection of ectopic B-cell follicles with germinal centers in the meninges of patients with secondary progressive multiple sclerosis. Brain Pathol. 2004. 14: 164-174.
Magliozzi, R., Howell, O., Vora, A., Serafini, B., Nicholas, R., Puopolo, M., Reynolds, R. et al., Meningeal B-cell follicles in secondary progressive multiple sclerosis associate with early onset of disease and severe cortical pathology. Brain 2007. 130(Pt): 1089-1104.
Lehmann-Horn, K., Kinzel, S., Feldmann, L., Radelfahr, F., Hemmer, B., Traffehn, S., Bernard, C. C. A. et al., Intrathecal anti-CD20 efficiently depletes meningeal B cells in CNS autoimmunity. Ann. Clin. Transl. Neurol. 2014. 1: 490-496.
Komori, M., Lin, Y. C., Cortese, I., Blake, A., Ohayon, J., Cherup, J., Maric, D. et al., Insufficient disease inhibition by intrathecal rituximab in progressive multiple sclerosis. Ann. Clin. Transl. Neurol. 2016. 3: 166-179.
Steinmaurer, A., Wimmer, I., Berger, T., Rommer, P. S. and Sellner, J., Bruton's tyrosine kinase inhibition in the treatment of preclinical models and multiple sclerosis. Curr. Pharm. Des. 2022. 28: 437-444.
Torke, S., Pretzsch, R., Häusler, D., Haselmayer, P., Grenningloh, R., Boschert, U., Brück, W. et al., Inhibition of Bruton's tyrosine kinase interferes with pathogenic B-cell development in inflammatory CNS demyelinating disease. Acta Neuropathol. 2020. 140: 535-548.
Von Büdingen, H.-C, Kuo, T. C., Sirota, M., Van Belle, C. J., Apeltsin, L., Glanville, J., Cree, B. A. et al., B cell exchange across the blood-brain barrier in multiple sclerosis. J. Clin. Invest. 2012. 122: 4533-4543.
Blauth, K., Owens, G. P. and Bennett, J. L., The ins and outs of B cells in multiple sclerosis. Front. Immunol. 2015. 6: 565.
Takeshita, Y. and Ransohoff, R. M., Inflammatory cell trafficking across the blood-brain barrier: Chemokine regulation and in vitro models. Immunol. Rev. 2012. 248: 228-239.
Pollok, K., Mothes, R., Ulbricht, C., Liebheit, A., Gerken, J. D., Uhlmann, S., Paul, F. et al., The chronically inflamed central nervous system provides niches for long-lived plasma cells. Acta Neuropatholog. Communic. 2017. 5: 88.
Alter, A., Duddy, M., Hebert, S., Biernacki, K., Prat, A., Antel, J. P., Yong, V. W. et al., Determinants of human B cell migration across brain endothelial cells. J. Immunol. 2003. 170: 4497-4505.
Lehmann-Horn, K., Sagan, S. A., Bernard, C. C. A., Sobel, R. A. and Zamvil, S. S., B-cell very late antigen-4 deficiency reduces leukocyte recruitment and susceptibility to central nervous system autoimmunity. Ann. Neurol. 2015. 77: 902-908.
Mancuso, R., Franciotta, D., Rovaris, M., Caputo, D., Sala, A., Hernis, A., Agostini, S. et al., Effects of natalizumab on oligoclonal bands in the cerebrospinal fluid of multiple sclerosis patients: A longitudinal study. Mult. Scler. 2014. 20: 1900-1903.
Cayrol, R., Wosik, K., Berard, J. L., Dodelet-Devillers, A., Ifergan, I., Kebir, H., Haqqani, A. S. et al., Activated leukocyte cell adhesion molecule promotes leukocyte trafficking into the central nervous system. Nat. Immunol. 2008. 9: 137-145.
Michel, L., Grasmuck, C., Charabati, M., Lécuyer, M.-A., Zandee, S., Dhaeze, T., Alvarez, J. I. et al., Activated leukocyte cell adhesion molecule regulates B lymphocyte migration across central nervous system barriers. Sci. Transl. Med. 2019. 11:eaaw0475.
Okai, S., Usui, F., Yokota, S., Hori-I, Y., Hasegawa, M., Nakamura, T., Kurosawa, M. et al., High-affinity monoclonal IgA regulates gut microbiota and prevents colitis in mice. Nat. Microbiol. 2016. 1: 16103.
Shinkura, R., Therapeutic immunoglobulin A antibody for dysbiosis-related diseases. Int. Immunol. 2021. 33: 787-790.
Moor, K., Wotzka, S. Y., Toska, A., Diard, M., Hapfelmeier, S. and Slack, E., Peracetic acid treatment generates potent inactivated oral vaccines from a broad range of culturable bacterial species. Front. Immunol. 2016. 7: 34.
Diard, M., Bakkeren, E., Lentsch, V., Rocker, A., Bekele, N. A., Hoces, D., Aslani, S. et al., A rationally designed oral vaccine induces immunoglobulin A in the murine gut that directs the evolution of attenuated Salmonella variants. Nat. Microbiol. 2021. 6: 830-841.
Federici, S., Kredo-Russo, S., Valdés-Mas, R., Kviatcovsky, D., Weinstock, E., Matiuhin, Y., Silberberg, Y. et al., Targeted suppression of human IBD-associated gut microbiota commensals by phage consortia for treatment of intestinal inflammation. Cell 2022. 185: 2879-2898.e24.
Harimoto, T., Hahn, J., Chen, Y.-Y., Im, J., Zhang, J., Hou, N., Li, F. et al., A programmable encapsulation system improves delivery of therapeutic bacteria in mice. Nat. Biotechnol. 2022. 40: 1259-1269.
Turnbaugh, P. J., Ridaura, V. K., Faith, J. J., Rey, F. E., Knight, R. and Gordon, J. I., The effect of diet on the human gut microbiome: A metagenomic analysis in humanized gnotobiotic mice. Sci. Transl. Med. 2009. 1: 6ra14.
Bressa, C., Bailén-Andrino, M., Pérez-Santiago, J., González-Soltero, R., Pérez, M., Montalvo-Lominchar, M. G., Maté-Muñoz, J. L. et al., Differences in gut microbiota profile between women with active lifestyle and sedentary women. PLoS One 2017. 12: e0171352.
Gupta, V. K., Paul, S. and Dutta, C., Geography, ethnicity or subsistence-specific variations in human microbiome composition and diversity. Front. Microbiol. 2017. 8: 1162.
Krienke, C., Kolb, L., Diken, E., Streuber, M., Kirchhoff, S., Bukur, T., Akilli-Öztürk, Ö. et al., A noninflammatory mRNA vaccine for treatment of experimental autoimmune encephalomyelitis. Science 2021. 371: 145-153.
Horikawa, M., Weimer, E. T., Dilillo, D. J., Venturi, G. M., Spolski, R., Leonard, W. J., Heise, M. T. et al., Regulatory B cell (B10 Cell) expansion during Listeria infection governs innate and cellular immune responses in mice. J. Immunol. 2013. 190: 1158-1168.
Sun, J., Wang, J., Pefanis, E., Chao, J., Rothschild, G., Tachibana, I., Chen, J. K. et al., Transcriptomics identify CD9 as a marker of murine IL-10-competent regulatory B cells. Cell Rep. 2015. 13: 1110-1117.
Watanabe, R., Fujimoto, M., Ishiura, N., Kuwano, Y., Nakashima, H., Yazawa, N., Okochi, H. et al., CD19 expression in B cells is important for suppression of contact hypersensitivity. Am. J. Pathol. 2007. 171: 560-570.
Miles, K., Heaney, J., Sibinska, Z., Salter, D., Savill, J., Gray, D. and Gray, M., A tolerogenic role for Toll-like receptor 9 is revealed by B-cell interaction with DNA complexes expressed on apoptotic cells. Proc. Natl. Acad. Sci. USA. 2012. 109: 887-892.
Evans, J. G., Chavez-Rueda, K. A., Eddaoudi, A., Meyer-Bahlburg, A., Rawlings, D. J., Ehrenstein, M. R. and Mauri, C., Novel suppressive function of transitional 2 B cells in experimental arthritis. J. Immunol. 2007. 178: 7868-7878.
Blair, P. A., Chavez-Rueda, K. A., Evans, J. G., Shlomchik, M. J., Eddaoudi, A., Isenberg, D. A., Ehrenstein, M. R. et al., Selective targeting of B cells with agonistic anti-CD40 is an efficacious strategy for the generation of induced regulatory T2-like B cells and for the suppression of lupus in MRL/lpr mice. J. Immunol. 2009. 182: 3492-3502.
Zhang, X., Deriaud, E., Jiao, X., Braun, D., Leclerc, C. and Lo-Man, R., Type I interferons protect neonates from acute inflammation through interleukin 10-producing B cells. J. Exp. Med. 2007. 204: 1107-1118.
Van De Veen, W., Stanic, B., Wirz, O. F., Jansen, K., Globinska, A. and Akdis, M., Role of regulatory B cells in immune tolerance to allergens and beyond. J. Allergy Clin. Immunol. 2016. 138: 654-665.
Hasan, M. M., Nair, S. S., O'leary, J. G., Thompson-Snipes, L., Nyarige, V., Wang, J., Park, W. et al., Implication of TIGIT(+) human memory B cells in immune regulation. Nat. Commun. 2021. 12: 1534.