Alteration of interleukin-10-producing Type 1 regulatory cells in autoimmune diseases.


Journal

Current opinion in hematology
ISSN: 1531-7048
Titre abrégé: Curr Opin Hematol
Pays: United States
ID NLM: 9430802

Informations de publication

Date de publication:
01 07 2022
Historique:
entrez: 5 7 2022
pubmed: 6 7 2022
medline: 7 7 2022
Statut: ppublish

Résumé

This review highlights findings describing the role of interleukin (IL)-10-producing Type 1 regulatory T (Tr1) cells in controlling autoimmune diseases and possible approaches to restore their function and number. Reduced frequency and/or function of cell subsets playing a role in Tr1 cell induction (e.g., DC-10 and Bregs), was found in patients with autoimmunity and may impact on Tr1 cell frequency. IL-10 is a pleiotropic cytokine with fundamental anti-inflammatory functions acting as negative regulator of immune responses. IL-10 is critically involved in the induction and functions of Tr1 cells, a subset of memory CD4+ T cells induced in the periphery to suppress immune responses to a variety of antigens (Ags), including self-, allogeneic, and dietary Ags. Alterations in IL-10-related pathways and/or in the frequency and activities of Tr1 cells have been associated to several autoimmune diseases. We will give an overview of the alterations of IL-10 and IL-10-producing Tr1 cells in Multiple Sclerosis, Type 1 Diabetes, and Celiac Disease, in which similarities in the role of these tolerogenic mechanisms are present. Current and future approaches to overcome Tr1 cell defects and restore tolerance in these diseases will also be discussed.

Identifiants

pubmed: 35787550
doi: 10.1097/MOH.0000000000000720
pii: 00062752-202207000-00009
doi:

Substances chimiques

IL10 protein, human 0
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

218-224

Informations de copyright

Copyright © 2022 Wolters Kluwer Health, Inc. All rights reserved.

Références

Miller SD, Turley DM, Podojil JR. Antigen-specific tolerance strategies for the prevention and treatment of autoimmune disease. Nat Rev Immunol 2007; 7:665–677.
Cooper GS, Bynum ML, Somers EC. Recent insights in the epidemiology of autoimmune diseases: improved prevalence estimates and understanding of clustering of diseases. J Autoimmun 2009; 33:197–207.
Rosenblum MD, Remedios KA, Abbas AK. Mechanisms of human autoimmunity. J Clin Investig 2015; 125:2228–2233.
Cepika AM, Sato Y, Liu JM, et al. Tregopathies: Monogenic diseases resulting in regulatory T-cell deficiency. J Allergy Clin Immunol 2018; 142:1679–1695.
Barzaghi F, Passerini L. IPEX syndrome: improved knowledge of immune pathogenesis empowers diagnosis. Front Pediatr 2021; 9:1–10.
Atkinson TP. Immune deficiency and autoimmunity. Curr Opin Rheumatol 2012; 24:515–521.
Zhu L, Shi T, Zhong C, et al. IL-10 and IL-10 receptor mutations in very early onset inflammatory bowel disease. Gastroenterol Res 2017; 10:65–69.
Mowat AM, Agace WW. Regional specialization within the intestinal immune system. Nat Rev Immunol 2014; 14:667–685.
Ouyang W, O’Garra A. IL-10 family cytokines IL-10 and IL-22: from basic science to clinical translation. Immunity 2019; 50:871–891.
Battaglia M, Gianfrani C, Gregori S, Roncarolo MG. IL-10-producing T regulatory type 1 cells and oral tolerance. Ann N Y Acad Sci 2004; 1029:142–153.
Neumann C, Scheffold A, Rutz S. Functions and regulation of T cell-derived interleukin-10. Semin Immunol 2019; 44:1–14.
Passerini L, Di Nunzio S, Gregori S, et al. Functional type 1 regulatory T cells develop regardless of FOXP3 mutations in patients with IPEX syndrome. Eur J Immunol 2011; 41:1120–1131.
Gagliani N, Jofra T, Valle A, et al. Transplant tolerance to pancreatic islets is initiated in the graft and sustained in the spleen. Am J Transplant 2013; 13:1963–1975.
Maynard CL, Harrington LE, Janowski KM, et al. Regulatory T cells expressing interleukin 10 develop from Foxp3+ and Foxp3- precursor cells in the absence of interleukin 10. Nat Immunol 2007; 8:931–941.
Roncarolo MG, Gregori S, Bacchetta R, et al. The biology of t regulatory Type 1 cells and their therapeutic application in immune-mediated diseases. Immunity 2018; 49:1004–1019.
Magnani CF, Alberigo G, Bacchetta R, et al. Killing of myeloid APCs via HLA class I, CD2 and CD226 defines a novel mechanism of suppression by human Tr1 cells. Eur J Immunol 2011; 41:1652–1662.
Celebi Sozener Z, Mungan D, Cevhertas L, et al. Tolerance mechanisms in allergen immunotherapy. Curr Opin Allergy Clin Immunol 2020; 20:591–601.
Rojas JM, Avia M, Martin V, Sevilla N. IL-10: a multifunctional cytokine in viral infections. J Immunol Res 2017; 2017:1–14.
Bonnal RJP, Rossetti G, Lugli E, et al. Clonally expanded EOMES(+) Tr1-like cells in primary and metastatic tumors are associated with disease progression. Nat Immunol 2021; 22:735–745.
Groux H, Cottrez F, Rouleau M, et al. A transgenic model to analyze the immunoregulatory role of IL-10 secreted by antigen-presenting cells. J Immunol 1999; 162:1723–1729.
Wakkach A, Fournier N, Brun V, et al. Characterization of dendritic cells that induce tolerance and T regulatory 1 cell differentiation in vivo. Immunity 2003; 18:605–617.
Wakkach A, Cottrez F, Groux H. Differentiation of regulatory T cells 1 is induced by CD2 costimulation. J Immunol 2001; 167:3107–3113.
Kemper C, Chan AC, Green JM, et al. Activation of human CD4+ cells with CD3 and CD46 induces a T-regulatory cell 1 phenotype. Nature 2003; 421:388–392.
Ito T, Hanabuchi S, Wang YH, et al. Two functional subsets of FOXP3+ regulatory T cells in human thymus and periphery. Immunity 2008; 28:870–880.
Steinbrink K, Graulich E, Kubsch S, et al. CD4(+) and CD8(+) anergic T cells induced by interleukin-10-treated human dendritic cells display antigen-specific suppressor activity. Blood 2002; 99:2468–2476.
Steinbrink K, Wolfl M, Jonuleit H, et al. Induction of tolerance by IL-10-treated dendritic cells. J Immunol 1997; 159:4772–4780.
Kryczanowsky F, Raker V, Graulich E, et al. IL-10-modulated human dendritic cells for clinical use: identification of a stable and migratory subset with improved tolerogenic activity. J Immunol 2016; 197:3607–3617.
Gregori S, Tomasoni D, Pacciani V, et al. Differentiation of type 1 T regulatory cells (Tr1) by tolerogenic DC-10 requires the IL-10-dependent ILT4/HLA-G pathway. Blood 2010; 116:935–944.
Amodio G, Comi M, Tomasoni D, et al. Hla-g expression levels influence the tolerogenic activity of human DC-10. Haematologica 2015; 100:548–557.
Comi M, Avancini D, Santoni de Sio F, et al. Coexpression of CD163 and CD141 identifies human circulating IL-10-producing dendritic cells (DC-10). Cell Mol Immunol 2020; 95–107.
Amodio G, Mugione A, Sanchez AM, et al. HLA-G expressing DC-10 and CD4(+) T cells accumulate in human decidua during pregnancy. Hum Immunol 2013; 74:406–411.
Filippi M, Bar-Or A, Piehl F, et al. Multiple sclerosis. Nat Rev Dis Primers 2018; 4:43.
Dendrou CA, Fugger L, Friese MA. Immunopathology of multiple sclerosis. Nat Rev Immunol 2015; 15:545–558.
Bettelli E, Das MP, Howard ED, et al. IL-10 is critical in the regulation of autoimmune encephalomyelitis as demonstrated by studies of IL-10- and IL-4-deficient and transgenic mice. J Immunol 1998; 161:3299–3306.
Samoilova EB, Horton JL, Chen Y. Acceleration of experimental autoimmune encephalomyelitis in interleukin-10-deficient mice: roles of interleukin-10 in disease progression and recovery. Cell Immunol 1998; 188:118–124.
Maghrebi O, Hanachi M, Bahrini K, et al. Differential gene expression patterns in blood and cerebrospinal fluid of multiple sclerosis and neuro-behcet disease. Front Genet 2021; 12:1–11.
Sedeeq MS, El-Nahrery EMA, Shalaby N, et al. Micro-RNA-96 and interleukin-10 are independent biomarkers for multiple sclerosis activity. J Neurol Sci 2019; 403:92–96.
Romme Christensen J, Bornsen L, Hesse D, et al. Cellular sources of dysregulated cytokines in relapsing-remitting multiple sclerosis. J Neuroinflammation 2012; 9:215.
Correale J, Gilmore W, McMillan M, et al. Patterns of cytokine secretion by autoreactive proteolipid protein-specific T cell clones during the course of multiple sclerosis. J Immunol 1995; 154:2959–2968.
Pelfrey CM, Rudick RA, Cotleur AC, et al. Quantification of self-recognition in multiple sclerosis by single-cell analysis of cytokine production. J Immunol 2000; 165:1641–1651.
Kvarnstrom M, Ydrefors J, Ekerfelt C, et al. Longitudinal interferon-beta effects in multiple sclerosis: differential regulation of IL-10 and IL-17A, while no sustained effects on IFN-gamma, IL-4 or IL-13. J Neurol Sci 2013; 325:79–85.
Chiarini M, Serana F, Zanotti C, et al. Modulation of the central memory and Tr1-like regulatory T cells in multiple sclerosis patients responsive to interferon-beta therapy. Mult Scler 2012; 18:788–798.
Astier AL, Meiffren G, Freeman S, Hafler DA. Alterations in CD46-mediated Tr1 regulatory T cells in patients with multiple sclerosis. J Clin Investig 2006; 116:3252–3257.
Martinez-Forero I, Garcia-Munoz R, Martinez-Pasamar S, et al. IL-10 suppressor activity and ex vivo Tr1 cell function are impaired in multiple sclerosis. Eur J Immunol 2008; 38:576–586.
Cao Y, Goods BA, Raddassi K, et al. Functional inflammatory profiles distinguish myelin-reactive T cells from patients with multiple sclerosis. Sci Transl Med 2015; 7:1–10.
van der Vlugt LE, Mlejnek E, Ozir-Fazalalikhan A, et al. CD24(hi)CD27(+) B cells from patients with allergic asthma have impaired regulatory activity in response to lipopolysaccharide. Clin Exp Allergy 2014; 44:517–528.
Mielle J, Audo R, Hahne M, et al. IL-10 Producing B cells ability to induce regulatory T cells is maintained in rheumatoid arthritis. Front Immunol 2018; 9:961.
Wang A, Rojas O, Lee D, Gommerman JL. Regulation of neuroinflammation by B cells and plasma cells. Immunol Rev 2021; 299:45–60.
Roep BO, Tree TI. Immune modulation in humans: implications for type 1 diabetes mellitus. Nat Rev Endocrinol 2014; 10:229–242.
Roncarolo MG, Levings MK. The role of different subsets of T regulatory cells in controlling autoimmunity. Curr Opin Immunol 2000; 12:676–683.
Petrich de Marquesini LG, Fu J, Connor KJ, et al. IFN-gamma and IL-10 islet-antigen-specific T cell responses in autoantibody-negative first-degree relatives of patients with type 1 diabetes. Diabetologia 2010; 53:1451–1460.
Arif S, Tree TI, Astill TP, et al. Autoreactive T cell responses show proinflammatory polarization in diabetes but a regulatory phenotype in health. J Clin Investig 2004; 113:451–463.
Chujo D, Nguyen TS, Foucat E, et al. Adult-onset type 1 diabetes patients display decreased IGRP-specific Tr1 cells in blood. Clin Immunol 2015; 161:270–277.
Sanda S, Roep BO, von Herrath M. Islet antigen specific IL-10+ immune responses but not CD4+CD25+FoxP3+ cells at diagnosis predict glycemic control in type 1 diabetes. Clin Immunol 2008; 127:138–143.
Tree TI, Lawson J, Edwards H, et al. Naturally arising human CD4 T-cells that recognize islet autoantigens and secrete interleukin-10 regulate proinflammatory T-cell responses via linked suppression. Diabetes 2010; 59:1451–1460.
Groux H, O’Garra A, Bigler M, et al. A CD4+ T-cell subset inhibits antigen-specific T-cell responses and prevents colitis. Nature 1997; 389:737–742.
Amodio G, Mandelli A, Curto R, et al. Altered frequency and phenotype of HLA-G-Expressing DC-10 in Type 1 diabetes patients at onset and in subjects at risk to develop the disease. Front Immunol 2021; 12:1–11.
Jia X, Zhai T, Wang B, et al. Decreased number and impaired function of type 1 regulatory T cells in autoimmune diseases. J Cell Physiol 2019; 234:12442–12450.
Huber S, Gagliani N, Esplugues E, et al. Th17 cells express interleukin-10 receptor and are controlled by Foxp3(-) and Foxp3+ regulatory CD4+ T cells in an interleukin-10-dependent manner. Immunity 2011; 34:554–565.
Gagliani N, Amezcua Vesely MC, Iseppon A, et al. Th17 cells transdifferentiate into regulatory T cells during resolution of inflammation. Nature 2015; 523:221–225.
Yu H, Gagliani N, Ishigame H, et al. Intestinal type 1 regulatory T cells migrate to periphery to suppress diabetogenic T cells and prevent diabetes development. Proc Natl Acad Sci USA 2017; 114:10443–10448.
Battaglia M, Stabilini A, Draghici E, et al. Induction of tolerance in type 1 diabetes via both CD4+CD25+ T regulatory cells and T regulatory type 1 cells. Diabetes 2006; 55:1571–1580.
Wang Y, Qin Y, Wang X, et al. Decrease in the proportion of CD24(hi) CD38(hi) B cells and impairment of their regulatory capacity in type 1 diabetes patients. Clin Exp Immunol 2020; 200:22–32.
El-Mokhtar MA, Elsherbiny NM, Sayed D, et al. Altered regulatory B cell subsets in children with Type 1 diabetes mellitus. J Immunol Res 2020; 2020:1–8.
Boldison J, Wong FS. Regulatory B cells: role in Type 1 diabetes. Front Immunol 2021; 12:1–9.
Stamnaes J, Sollid LM. Celiac disease: Autoimmunity in response to food antigen. Semin Immunol 2015; 27:343–352.
Izcue A, Coombes JL, Powrie F. Regulatory lymphocytes and intestinal inflammation. Annu Rev Immunol 2009; 27:313–338.
Lopez MS, Tiscornia MM, Dicarlos MB, Zapata PD. IL-10 gene promoter region polymorphisms and their association with celiac disease. Rev Esp Enferm Dig 2020; 112:915–920.
Aflatoonian M, Sivandzadeh G, Morovati-Sharifabad M, et al. Associations of Il-6-174g>C and Il-10-1082a>G polymorphisms with susceptibility to celiac disease: evidence from a meta-analysis and literature review. Arq Gastroenterol 2019; 56:323–328.
Barisani D, Ceroni S, Meneveri R, et al. IL-10 polymorphisms are associated with early-onset celiac disease and severe mucosal damage in patients of Caucasian origin. Genet Med 2006; 8:169–174.
Forsberg G, Hernell O, Hammarstrom S, Hammarstrom ML. Concomitant increase of IL-10 and pro-inflammatory cytokines in intraepithelial lymphocyte subsets in celiac disease. Int Immunol 2007; 19:993–1001.
Salvati VM, Mazzarella G, Gianfrani C, et al. Recombinant human interleukin 10 suppresses gliadin dependent T cell activation in ex vivo cultured coeliac intestinal mucosa. Gut 2005; 54:46–53.
Borrelli M, Salvati VM, Maglio M, et al. Immunoregulatory pathways are active in the small intestinal mucosa of patients with potential celiac disease. Am J Gastroenterol 2013; 108:1775–1784.
Camarca A, Auricchio R, Picascia S, et al. Gliadin-reactive T cells in Italian children from preventCD cohort at high risk of celiac disease. Pediatr Allergy Immunol 2017; 28:362–369.
Girard-Madoux MJ, Ober-Blobaum JL, Costes LM, et al. IL-10 control of CD11c+ myeloid cells is essential to maintain immune homeostasis in the small and large intestine. Oncotarget 2016; 7:32015–32030.
Costes LMM, Lindenbergh-Kortleve DJ, van Berkel LA, et al. IL-10 signaling prevents gluten-dependent intraepithelial CD4(+) cytotoxic T lymphocyte infiltration and epithelial damage in the small intestine. Mucosal Immunol 2019; 12:479–490.
Du Pre MF, Kozijn AE, van Berkel LA, et al. Tolerance to ingested deamidated gliadin in mice is maintained by splenic, type 1 regulatory T cells. Gastroenterology 2011; 141:610–620. 620 e611-612.
Gianfrani C, Levings MK, Sartirana C, et al. Gliadin-specific type 1 regulatory T cells from the intestinal mucosa of treated celiac patients inhibit pathogenic T cells. J Immunol 2006; 177:4178–4186.
Thrower SL, James L, Hall W, et al. Proinsulin peptide immunotherapy in type 1 diabetes: report of a first-in-man Phase I safety study. Clin Exp Immunol 2009; 155:156–165.
Jurynczyk M, Walczak A, Jurewicz A, et al. Immune regulation of multiple sclerosis by transdermally applied myelin peptides. Ann Neurol 2010; 68:593–601.
Clemente-Casares X, Blanco J, Ambalavanan P, et al. Expanding antigen-specific regulatory networks to treat autoimmunity. Nature 2016; 530:434–440.
Serra P, Santamaria P. Antigen-specific therapeutic approaches for autoimmunity. Nat Biotechnol 2019; 37:238–251.
Passerini L, Gregori S. Induction of antigen-specific tolerance in T cell mediated diseases. Front Immunol 2020; 11:1–14.
Desreumaux P, Foussat A, Allez M, et al. Safety and efficacy of antigen-specific regulatory T-cell therapy for patients with refractory Crohn's disease. Gastroenterology 2012; 143:1207–1217. e1201-1202.
Chen PP, Cepika AM, Agarwal-Hashmi R, et al. Alloantigen-specific type 1 regulatory T cells suppress through CTLA-4 and PD-1 pathways and persist long-term in patients. Sci Transl Med 2021; 13:eabf5264.
Pellerin L, Jenks JA, Chinthrajah S, et al. Peanut-specific type 1 regulatory T cells induced in vitro from allergic subjects are functionally impaired. J Allergy Clin Immunol 2017; 202–213.

Auteurs

Silvia Gregori (S)

Mechanisms of Peripheral Tolerance Unit, San Raffaele Telethon Institute for Gene Therapy (SR-Tiget), IRCCS San Raffaele Scientific Institute, Milan, Italy.

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