Microbiota and immunoregulation: A focus on regulatory B lymphocytes and transplantation.
B cell biology
basic (laboratory) research/science
immune regulation
immunobiology
immunosuppression/immune modulation
microbiomics
organ transplantation in general
translational research/science
Journal
American journal of transplantation : official journal of the American Society of Transplantation and the American Society of Transplant Surgeons
ISSN: 1600-6143
Titre abrégé: Am J Transplant
Pays: United States
ID NLM: 100968638
Informations de publication
Date de publication:
07 2021
07 2021
Historique:
revised:
29
12
2020
received:
27
09
2020
pubmed:
10
2
2021
medline:
10
8
2021
entrez:
9
2
2021
Statut:
ppublish
Résumé
The microbiota plays a major role in the regulation of the host immune functions thus establishing a symbiotic relationship that maintains immune homeostasis. Among immune cells, regulatory B cells (Bregs), which can inhibit effector T cell responses, may be involved in the intestinal homeostasis. Recent works suggest that the interaction between the microbiota and Bregs appears to be important to limit autoimmune diseases and help to maintain tolerance in transplantation. Short-chain fatty acids (SCFAs), recognized as major metabolites of the microbiota, seem to be involved in the generation of a pro-tolerogenic environment in the gut, particularly through the regulation of B cell differentiation, limiting mature B cells and promoting the function of Bregs. In this review, we show that this B cells-microbiota interaction may open a path toward new potential therapeutic applications not only for patients with autoimmune diseases but also in transplantation.
Identifiants
pubmed: 33559282
doi: 10.1111/ajt.16522
pii: S1600-6135(22)08623-3
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
2341-2347Informations de copyright
© 2021 The American Society of Transplantation and the American Society of Transplant Surgeons.
Références
Bach J-F. The hygiene hypothesis in autoimmunity: the role of pathogens and commensals. Nat Rev Immunol. 2018;18(2):105-120.
Rooks MG, Garrett WS. Gut microbiota, metabolites and host immunity. Nat Rev Immunol. 2016;16(6):341-352.
Mauri C, Menon M. Human regulatory B cells in health and disease: therapeutic potential. J Clin Invest. 2017;127(3):772-779.
Rosser EC, Oleinika K, Tonon S, et al. Regulatory B cells are induced by gut microbiota-driven interleukin-1β and interleukin-6 production. Nat Med. 2014;20(11):1334-1339.
Rosser EC, Piper CJM, Matei DE, et al. Microbiota-derived metabolites suppress arthritis by amplifying aryl-hydrocarbon receptor activation in regulatory B cells. Cell Metab. 2020;31(4):837-851.e10.
Oleinika K, Mauri C, Salama AD. Effector and regulatory B cells in immune-mediated kidney disease. Nat Rev Nephrol. 2019;15(1):11-26.
Sanchez HN, Moroney JB, Gan H, et al. B cell-intrinsic epigenetic modulation of antibody responses by dietary fiber-derived short-chain fatty acids. Nat Commun. 2020;11(1):60.
Piper CJM, Rosser EC, Oleinika K, et al. Aryl hydrocarbon receptor contributes to the transcriptional program of IL-10-producing regulatory B cells. Cell Rep. 2019;29(7):1878-1892.e7.
Katz SI, Parker D, Turk JL. B-cell suppression of delayed hypersensitivity reactions. Nature. 1974;251(5475):550-551.
Fillatreau S, Sweenie CH, McGeachy MJ, Gray D, Anderton SM. B cells regulate autoimmunity by provision of IL-10. Nat Immunol. 2002;3(10):944-950.
Flores-Borja F, Bosma A, Ng D, et al. CD19+CD24hiCD38hi B cells maintain regulatory T cells while limiting TH1 and TH17 differentiation. Sci Transl Med. 2013;5(173):173ra23.
Iwata Y, Matsushita T, Horikawa M, et al. Characterization of a rare IL-10-competent B-cell subset in humans that parallels mouse regulatory B10 cells. Blood. 2011;117(2):530-541.
Matsumoto M, Baba A, Yokota T, et al. Interleukin-10-producing plasmablasts exert regulatory function in autoimmune inflammation. Immunity. 2014;41(6):1040-1051.
Menon M, Blair PA, Isenberg DA, Mauri C. A regulatory feedback between plasmacytoid dendritic cells and regulatory B cells Is aberrant in systemic lupus erythematosus. Immunity. 2016;44(3):683-697.
Clatworthy MR, Watson CJE, Plotnek G, et al. B-cell-depleting induction therapy and acute cellular rejection. N Engl J Med. 2009;360(25):2683-2685.
Sautenet B, Blancho G, Büchler M, et al. One-year results of the effects of rituximab on acute antibody-mediated rejection in renal transplantation: RITUX ERAH, a multicenter double-blind randomized placebo-controlled trial. Transplantation. 2016;100(2):391-399.
Manna A, Kellett T, Aulakh S, et al. Targeting CD38 is lethal to Breg-like chronic lymphocytic leukemia cells and Tregs, but restores CD8+ T-cell responses. Blood Adv. 2020;4(10):2143-2157.
van de Veen W, Stanic B, Yaman G, et al. IgG4 production is confined to human IL-10-producing regulatory B cells that suppress antigen-specific immune responses. J Allergy Clin Immunol. 2013;131(4):1204-1212.
Ray A, Khalil MI, Pulakanti KL, et al. Mature IgDlow/- B cells maintain tolerance by promoting regulatory T cell homeostasis. Nat Commun. 2019;10(1):190.
Rosser EC, Mauri C. Regulatory B cells: origin, phenotype, and function. Immunity. 2015;42(4):607-612.
Gondek DC, Lu L-F, Quezada SA, Sakaguchi S, Noelle RJ. Cutting edge: contact-mediated suppression by CD4+CD25+ regulatory cells involves a granzyme B-dependent, perforin-independent mechanism. J Immunol. 2005;174(4):1783-1786.
Hagn M, Schwesinger E, Ebel V, et al. Human B cells secrete granzyme B when recognizing viral antigens in the context of the acute phase cytokine IL-21. J Immunol. 2009;183(3):1838-1845.
Chesneau M, Michel L, Dugast E, et al. Tolerant kidney transplant patients produce B cells with regulatory properties. J Am Soc Nephrol. 2015;26(10):2588-2598.
Chesneau M, Pallier A, Braza F, et al. Unique B cell differentiation profile in tolerant kidney transplant patients. Am J Transplant. 2014;14(1):144-155.
Chesneau M, Mai HL, Danger R, et al. Efficient expansion of human granzyme B-expressing B cells with potent regulatory properties. J Immunol. 2020;205(9):2391-2401.
Dubois F, Limou S, Chesneau M, Degauque N, Brouard S, Danger R. Transcriptional meta-analysis of regulatory B cells. Eur J Immunol. Published online June 11, 2020. 2020;50(11):1757-1769.
Hooper LV, Littman DR, Macpherson AJ. Interactions between the microbiota and the immune system. Science. 2012;336(6086):1268-1273.
Okai S, Usui F, Yokota S, et al. High-affinity monoclonal IgA regulates gut microbiota and prevents colitis in mice. Nat Microbiol. 2016;1(9):16103.
Alhabbab R, Blair P, Elgueta R, et al. Diversity of gut microflora is required for the generation of B cell with regulatory properties in a skin graft model. Sci Rep. 2015;5:11554.
Lozupone CA, Stombaugh JI, Gordon JI, Jansson JK, Knight R. Diversity, stability and resilience of the human gut microbiota. Nature. 2012;489(7415):220-230.
Bartman C, Chong AS, Alegre M-L. The influence of the microbiota on the immune response to transplantation. Curr Opin Organ Transplant. 2015;20(1):1-7.
Cummings JH, Pomare EW, Branch WJ, Naylor CP, Macfarlane GT. Short chain fatty acids in human large intestine, portal, hepatic and venous blood. Gut. 1987;28(10):1221-1227.
Smith PM, Howitt MR, Panikov N, et al. The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science. 2013;341(6145):569-573.
Wu W, Sun M, Chen F, et al. Microbiota metabolite short-chain fatty acid acetate promotes intestinal IgA response to microbiota which is mediated by GPR43. Mucosal Immunol. 2017;10(4):946-956.
Arpaia N, Campbell C, Fan X, et al. Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation. Nature. 2013;504(7480):451-455.
Tan J, McKenzie C, Vuillermin P, et al. Dietary fiber and bacterial SCFA enhance oral tolerance and protect against food allergy through diverse cellular pathways. Cell Rep. 2016;15(12):2809-2824.
Kim M, Qie Y, Park J, Kim CH. Gut microbial metabolites fuel host antibody responses. Cell Host Microbe. 2016;20(2):202-214.
Abbott KC, Swanson SJ, Richter ER, et al. Late urinary tract infection after renal transplantation in the United States. Am J Kidney Dis. 2004;44:353-362.
Reinke P, Lippert J, Ewert R, et al. Late-acute renal allograft rejection and symptomless cytomegalovirus infection. Lancet. 1994;344:1737-1738.
Vilchez RA, Dauber J, McCurry K, et al. Parainfluenza virus infection in adult lung transplant recipients: an emergent clinical syndrome with implications on allograft function. Am J Transplant. 2003;3(2):116-120.
Roussey-Kesler G, Giral M, Moreau A, et al. Clinical operational tolerance after kidney transplantation. Am J Transplant. 2006;6(4):736-746.
Massart A, Pallier A, Pascual J, et al. The DESCARTES-Nantes sur- vey of kidney transplant recipients displaying clinical operational tolerance identifies 35 new tolerant patients and 34 almost toler- ant patients. Nephrol Dial Transplant. 2016;31(6):1002-1013.
Brouard S, Pallier A, Renaudin K, et al. The natural history of clinical operational tolerance after kidney transplantation through twenty- seven cases. Am J Transplant. 2012;12(12):3296-3307.
Lee JR, Muthukumar T, Dadhania D, et al. Gut microbial community structure and complications after kidney transplantation: a pilot study. Transplantation. 2014;98(7):697-705.
Ahmed EB, Wang T, Daniels M, Alegre ML, Chong AS. IL-6 induced by Staphylococcus aureus infection prevents the induction of skin allograft acceptance in mice. Am J Transplant. 2011;11(5):936-946.
Lei YM, Sepulveda M, Chen L, et al. Skin-restricted commensal colonization accelerates skin graft rejection. JCI Insight. 2019;5(15):e127569.
Karczewski J, Karczewski M, Glyda M, Wiktorowicz K. Role of TH1/TH2 cytokines in kidney allograft rejection. Transplant Proc. 2008;40(10):3390-3392.
McIntosh CM, Chen L, Shaiber A, Eren AM, Alegre M-L. Gut microbes contribute to variation in solid organ transplant outcomes in mice. Microbiome. 2018;6(1):96.
Zhang Z, Liu L, Tang H, et al. Immunosuppressive effect of the gut microbiome altered by high-dose tacrolimus in mice. Am J Transplant. 2018;18(7):1646-1656.
Bromberg JS, Hittle L, Xiong Y, et al. Gut microbiota-dependent modulation of innate immunity and lymph node remodeling affects cardiac allograft outcomes. JCI Insight. 2018;3(19):e121045.
Colas L, Mongodin EF, Montassier E, et al. Unique and specific proteobacteria diversity in urinary microbiota of tolerant kidney transplanted recipients. Am J Transplant. 2020;20(1):145-158.
Pallier A, Hillion S, Danger R, et al. Patients with drug-free long-term graft function display increased numbers of peripheral B cells with a memory and inhibitory phenotype. Kidney Int. 2010;78(5):503-513.
Sagoo P, Perucha E, Sawitzki B, et al. Development of a cross-platform biomarker signature to detect renal transplant tolerance in humans. J Clin Invest. 2010;120(6):1848-1861.
Newell KA, Asare A, Sanz I, et al. Longitudinal studies of a B cell-derived signature of tolerance in renal transplant recipients. Am J Transplant. 2015;15(11):2908-2920.
Brouard S, Mansfield E, Braud C, et al. Identification of a peripheral blood transcriptional biomarker panel associated with operational renal allograft tolerance. Proc Natl Acad Sci USA. 2007;104(39):15448-15453.
Cherukuri A, Rothstein DM, Clark B, et al. Immunologic human renal allograft injury associates with an altered IL 10/TNF-alpha expression ratio in regulatory B cells. J Am Soc Nephrol. 2014;25(7):1575-1585.
Wu H, Singer J, Kwan TK, et al. Gut microbial metabolites induce donor-specific tolerance of kidney allografts through induction of T regulatory cells by short-chain fatty acids. J Am Soc Nephrol. 2020;31(7):1445-1461.
Luu M, Pautz S, Kohl V, et al. The short-chain fatty acid pentanoate suppresses autoimmunity by modulating the metabolic-epigenetic crosstalk in lymphocytes. Nat Commun. 2019;10(1):760.
Alegre ML. Can diet induce transplantation tolerance? J Am Soc Nephrol. 2020;31(7):1417-1418.
Loupy A, Lefaucheur C. Antibody-mediated rejection of solid-organ allografts. N Engl J Med. 2018;379(12):1150-1160.
Colas L, Brouard S. B cells and extracellular vesicles: new key players in solid organ transplantation? Am J Transplant. Published online August 10, 2020. 2020. https://doi.org/10.1111/ajt.16253.
Alhabbab RY, Nova-Lamperti E, Aravena O, et al. Regulatory B cells: development, phenotypes, functions, and role in transplantation. Immunol Rev. 2019;292(1):164-179.