IL-10-Producing Lymphocytes in Inflammatory Disease

REFERENCES

• Fiorentino DF, Bond MW, Mosmann TR. Two types of mouse T helper cell. IV. Th2 clones secrete a factor that inhibits cytokine production by Th1 clones. J Exp Med 1989;170(6):2081–2095.
   PubMed Web of Science ®Google Scholar
• Moore KW, Vieira P, Fiorentino DF, Homology of cytokine synthesis inhibitory factor (IL-10) to the Epstein-Barr virus gene BCRFI. Science 1990;248(4960):1230–1234.
   PubMedGoogle Scholar
• Hawrylowicz CM, O'Garra A. Potential role of interleukin-10-secreting regulatory T cells in allergy and asthma. Nat Rev Immunol 2005;5(4):271–283.
   PubMed Web of Science ®Google Scholar
• O'Garra A, Barrat FJ, Castro AG, Strategies for use of IL-10 or its antagonists in human disease. Immunol Rev 2008;223:114–131.
   PubMed Web of Science ®Google Scholar
• Moore KW, de Waal Malefyt R, Coffman RL, O'Garra A. Interleukin-10 and the interleukin-10 receptor. Annu Rev Immunol 2001;19:683–765.
   PubMed Web of Science ®Google Scholar
• O'Garra A, Vieira P. Regulatory T cells and mechanisms of immune system control. Nat Med 2004;10(8):801–805.
   PubMed Web of Science ®Google Scholar
• Roncarolo MG, Gregori S, Battaglia M, Interleukin-10-secreting type 1 regulatory T cells in rodents and humans. Immunol Rev 2006;212:28–250.
   PubMed Web of Science ®Google Scholar
• O'Garra A, Vieira P. T(H)1 cells control themselves by producing interleukin-10. Nat Rev Immunol 2007;7(6):425–428.
   PubMed Web of Science ®Google Scholar
• Trinchieri G. Interleukin-10 production by effector T cells: Th1 cells show self control. J Exp Med 2007;204(2):239–243.
   PubMed Web of Science ®Google Scholar
• Maynard CL, Weaver CT. Diversity in the contribution of interleukin-10 to T-cell-mediated immune regulation. Immunol Rev 2008;226:219–233.
   PubMed Web of Science ®Google Scholar
• Maloy KJ, Powrie F. Regulatory T cells in the control of immune pathology. Nat Immunol 2001;2(9):816–822.
   PubMed Web of Science ®Google Scholar
• Ryan JJ, Kashyap M, Bailey D, Mast cell homeostasis: a fundamental aspect of allergic disease. Crit Rev Immunol 2007;27(1):15–32.
   PubMed Web of Science ®Google Scholar
• Fillatreau S, Gray D, Anderton SM. Not always the bad guys: B cells as regulators of autoimmune pathology. Nat Rev Immunol 2008;8(5):391–397.
   PubMed Web of Science ®Google Scholar
• Williams LM, Ricchetti G, Sarma U, Interleukin-10 suppression of myeloid cell activation–a continuing puzzle. Immunology 2004;113(3):281–292.
   PubMedGoogle Scholar
• Emami CN, Chokshi N, Wang J, Role of interleukin-10 in the pathogenesis of necrotizing enterocolitis. Am J Surg 2012;203(4):428–435.
   PubMed Web of Science ®Google Scholar
• Fedorak RN, Gangl A, Elson CO, Recombinant human interleukin 10 in the treatment of patients with mild to moderately active Crohn's disease. The interleukin 10 inflammatory bowel disease cooperative study group. Gastroenterology 2000;119(6):1473–1482.
   PubMed Web of Science ®Google Scholar
• Docke WD, Asadullah K, Belbe G, Comprehensive biomarker monitoring in cytokine therapy: heterogeneous, time-dependent, and persisting immune effects of interleukin-10 application in psoriasis. J Leukoc Biol 2009;85(3):582–593.
   PubMedGoogle Scholar
• Lopez MN, Pesce B, Kurte M, A synthetic peptide homologous to IL-10 functional domain induces monocyte differentiation to TGF-beta+ tolerogenic dendritic cells. Immunobiology 2011;216(10):1117–1126.
   PubMedGoogle Scholar
• Li MO, Flavell RA. Contextual regulation of inflammation: a duet by transforming growth factor-beta and interleukin-10. Immunity 2008;28(4):468–476.
   PubMed Web of Science ®Google Scholar
• Jankovic D, Kullberg MC, Feng CG, Conventional T-bet(+)Foxp3(-) Th1 cells are the major source of host-protective regulatory IL-10 during intracellular protozoan infection. J Exp Med 2007;204(2):273–283.
   PubMedGoogle Scholar
• Anderson CF, Oukka M, Kuchroo VJ, Sacks D. CD4(+)CD25(-)Foxp3(-) Th1 cells are the source of IL-10-mediated immune suppression in chronic cutaneous leishmaniasis. J Exp Med 2007;204(2):285–297.
   PubMedGoogle Scholar
• Gabrysova L, Nicolson KS, Streeter HB, Negative feedback control of the autoimmune response through antigen-induced differentiation of IL-10-secreting Th1 cells. J Exp Med 2009;206(8):1755–1767.
   PubMedGoogle Scholar
• Saraiva M, Christensen JR, Veldhoen M, Interleukin-10 production by Th1 cells requires interleukin-12-induced STAT4 transcription factor and ERK MAP kinase activation by high antigen dose. Immunity 2009;31(2):209–219.
   PubMedGoogle Scholar
• Gerosa F, Nisii C, Righetti S, CD4(+) T cell clones producing both interferon-gamma and interleukin-10 predominate in bronchoalveolar lavages of active pulmonary tuberculosis patients. Clin Immunol 1999;92(3):224–234.
   PubMedGoogle Scholar
• Meyaard L, Hovenkamp E, Otto SA, Miedema F. IL-12-induced IL-10 production by human T cells as a negative feedback for IL-12-induced immune responses. J Immunol 1996;156(8):2776–2782.
   PubMed Web of Science ®Google Scholar
• Yssel H, De Waal Malefyt R, Roncarolo MG, IL-10 is produced by subsets of human CD4+ T cell clones and peripheral blood T cells. J Immunol 1992;149(7):2378–2384.
   PubMedGoogle Scholar
• Del Prete G, De Carli M, Almerigogna F, Human IL-10 is produced by both type 1 helper (Th1) and type 2 helper (Th2) T cell clones and inhibits their antigen-specific proliferation and cytokine production. J Immunol 1993;150(2):353–360.
   PubMed Web of Science ®Google Scholar
• McGeachy MJ, Bak-Jensen KS, Chen Y, TGF-beta and IL-6 drive the production of IL-17 and IL-10 by T cells and restrain T(H)-17 cell-mediated pathology. Nat Immunol 2007;8(12): 1390–1397.
   PubMed Web of Science ®Google Scholar
• Fitzgerald DC, Zhang GX, El-Behi M, Suppression of autoimmune inflammation of the central nervous system by interleukin 10 secreted by interleukin 27-stimulated T cells. Nat Immunol 2007;8(12):1372–1379.
   PubMed Web of Science ®Google Scholar
• Stumhofer JS, Silver JS, Laurence A, Interleukins 27 and 6 induce STAT3-mediated T cell production of interleukin 10. Nat Immunol 2007;8(12):1363–1371.
   PubMed Web of Science ®Google Scholar
• Saraiva M, O'Garra A. The regulation of IL-10 production by immune cells. Nat Rev Immunol 2010;10(3):170–181.
   PubMed Web of Science ®Google Scholar
• Belkaid Y, Tarbell K. Regulatory T cells in the control of host-microorganism interactions (*). Annu Rev Immunol 2009;27:551–589.
   Google Scholar
• Belkaid Y. Regulatory T cells and infection: a dangerous necessity. Nat Rev Immunol 2007;7(11):875–888.
   PubMed Web of Science ®Google Scholar
• Josefowicz SZ, Rudensky A. Control of regulatory T cell lineage commitment and maintenance. Immunity 2009;30(5):616–625.
   PubMed Web of Science ®Google Scholar
• Shevach EM. Mechanisms of foxp3+ T regulatory cell-mediated suppression. Immunity 2009;30(5):636–645.
   PubMed Web of Science ®Google Scholar
• Maynard CL, Harrington LE, Janowski KM, Regulatory T cells expressing interleukin 10 develop from Foxp3+ and Foxp3–precursor cells in the absence of interleukin 10. Nat Immunol 2007;8(9):931–941.
   PubMedGoogle Scholar
• Morrissey PJ, Charrier K, Braddy S, et al.. CD4+ T cells that express high levels of CD45RB induce wasting disease when transferred into congenic severe combined immunodeficient mice. Disease development is prevented by cotransfer of purified CD4+ T cells. J Exp Med 1993;178(1):237–244.
   PubMed Web of Science ®Google Scholar
• Powrie F, Leach MW, Mauze S, Phenotypically distinct subsets of CD4+ T cells induce or protect from chronic intestinal inflammation in C. B-17 scid mice. Int Immunol 1993;5(11):1461–1471.
   PubMed Web of Science ®Google Scholar
• Denning TL, Kim G, Kronenberg M. Cutting edge: CD4+CD25+ regulatory T cells impaired for intestinal homing can prevent colitis. J Immunol 2005;174(12):7487–7491.
   PubMed Web of Science ®Google Scholar
• Guichelaar T, ten Brink CB, van Kooten PJ, Autoantigen-specific IL-10-transduced T cells suppress chronic arthritis by promoting the endogenous regulatory IL-10 response. J Immunol 2008;180(3):1373–1381.
   PubMedGoogle Scholar
• Zhang L, Yuan S, Cheng G, Guo B. Type I IFN promotes IL-10 production from T cells to suppress Th17 cells and Th17-associated autoimmune inflammation. PLoS One 2011;6(12):e28432.
   Google Scholar
• Zhao J, Fett C, Trandem K, IFN-gamma- and IL-10-expressing virus epitope-specific Foxp3(+) T reg cells in the central nervous system during encephalomyelitis. J Exp Med 2011;208(8): 1571–1577.
   PubMed Web of Science ®Google Scholar
• Huss DJ, Winger RC, Cox GM, TGF-beta signaling via Smad4 drives IL-10 production in effector Th1 cells and reduces T-cell trafficking in EAE. Eur J Immunol 2011;41(10):2987–2996.
   PubMedGoogle Scholar
• Liu Y, Zhu T, Cai G, Elevated circulating CD4+ ICOS+ Foxp3+ T cells contribute to overproduction of IL-10 and are correlated with disease severity in patients with systemic lupus erythematosus. Lupus 2011;20(6):620–627.
   PubMedGoogle Scholar
• Trandem K, Zhao J, Fleming E, Perlman S. Highly activated cytotoxic CD8 T cells express protective IL-10 at the peak of coronavirus-induced encephalitis. J Immunol 2011;186(6):3642–3652.
   PubMed Web of Science ®Google Scholar
• Chaudhry A, Samstein RM, Treuting P, Interleukin-10 signaling in regulatory T cells is required for suppression of Th17 cell-mediated inflammation. Immunity 2011;34(4):566–578.
   PubMed Web of Science ®Google Scholar
• DiLillo DJ, Matsushita T, Tedder TF. B10 cells and regulatory B cells balance immune responses during inflammation, autoimmunity, and cancer. Ann NY Acad Sci 2010;1183:38–57.
   PubMed Web of Science ®Google Scholar
• Lampropoulou V, Calderon-Gomez E, Roch T, Suppressive functions of activated B cells in autoimmune diseases reveal the dual roles of toll-like receptors in immunity. Immunol Rev 2010;233(1):146–161.
   PubMedGoogle Scholar
• Mauri C, Blair PA. Regulatory B cells in autoimmunity: developments and controversies. Nat Rev Rheumatol 2010;6(11):636–643.
   PubMed Web of Science ®Google Scholar
• Mauri C, Bosma A. Immune regulatory function of B cells. Annu Rev Immunol 2012;30:221–241.
   PubMed Web of Science ®Google Scholar
• Fillatreau S, Sweenie CH, McGeachy MJ, B cells regulate autoimmunity by provision of IL-10. Nat Immunol 2002;3(10):944–950.
   PubMed Web of Science ®Google Scholar
• Lampropoulou V, Hoehlig K, Roch T, TLR-activated B cells suppress T cell-mediated autoimmunity. J Immunol 2008;180(7):4763–4773.
   PubMed Web of Science ®Google Scholar
• Rieger A, Bar-Or A. B-cell-derived interleukin-10 in autoimmune disease: regulating the regulators. Nat Rev Immunol 2008;8(6):486–487.
   PubMed Web of Science ®Google Scholar
• Knippenberg S, Peelen E, Smolders J, Reduction in IL-10 producing B cells (Breg) in multiple sclerosis is accompanied by a reduced naive/memory Breg ratio during a relapse but not in remission. J Neuroimmunol 2011;239(1–2):80–86.
   PubMed Web of Science ®Google Scholar
• Carter NA, Rosser EC, Mauri C. IL-10 produced by B cells is crucial for the suppression of Th17/ Th1 responses, induction of Tr1 cells and reduction of collagen-induced arthritis. Arthritis Res Ther 2012;14(1):R32.
   Web of Science ®Google Scholar
• Fernandez L, Salinas GF, Rocha C, The TNF-ligand APRIL can control CIA by regulating antibody-production and stimulating anti-inflammatory IL-10 producing B cells. Ann Rheum Dis 2011;70:A58.
   Google Scholar
• Yanaba K, Yoshizaki A, Asano Y, IL-10-producing regulatory B10 cells inhibit intestinal injury in a mouse model. Am J Pathol 2011;178(2):735–743.
   PubMedGoogle Scholar
• Xiao Z, Mohamood AS, Uddin S, Inhibition of Fas ligand in NOD mice unmasks a protective role for IL-10 against insulitis development. Am J Pathol 2011;179(2):725–732.
   PubMedGoogle Scholar
• Trinchieri G. Biology of natural killer cells. Adv Immunol 1989;47:187–376.
   PubMed Web of Science ®Google Scholar
• Freud AG, Caligiuri MA. Human natural killer cell development. Immunol Rev 2006;214:56–72.
   PubMed Web of Science ®Google Scholar
• Moretta L, Ferlazzo G, Bottino C, Effector and regulatory events during natural killer-dendritic cell interactions. Immunol Rev 2006;214:219–228.
   PubMed Web of Science ®Google Scholar
• Perona-Wright G, Mohrs K, Szaba FM, Systemic but not local infections elicit immunosuppressive IL-10 production by natural killer cells. Cell Host Microbe 2009;6(6):503–512.
   PubMed Web of Science ®Google Scholar
• Peritt D, Robertson S, Gri G, Differentiation of human NK cells into NK1 and NK2 subsets. J Immunol 1998;161(11):5821–5824.
   PubMed Web of Science ®Google Scholar
• Deniz G, Erten G, Kucuksezer UC, Regulatory NK cells suppress antigen-specific T cell responses. J Immunol 2008;180(2):850–857.
   PubMed Web of Science ®Google Scholar
• Moore KW, O'Garra A, de Waal Malefyt R, Interleukin-10. Annu Rev Immunol 1993;11:165–190.
   PubMed Web of Science ®Google Scholar
• Qian C, An H, Yu Y, TLR agonists induce regulatory dendritic cells to recruit Th1 cells via preferential IP-10 secretion and inhibit Th1 proliferation. Blood 2007;109(8):3308–3315.
   PubMedGoogle Scholar
• Mocellin S, Panelli M, Wang E, IL-10 stimulatory effects on human NK cells explored by gene profile analysis. Genes Immun 2004;5(8):621–630.
   PubMed Web of Science ®Google Scholar
• Cai G, Kastelein RA, Hunter CA. IL-10 enhances NK cell proliferation, cytotoxicity and production of IFN-gamma when combined with IL-18. Eur J Immunol 1999;29(9):2658–2665.
   PubMed Web of Science ®Google Scholar
• Carson WE, Lindemann MJ, Baiocchi R, The functional characterization of interleukin-10 receptor expression on human natural killer cells. Blood 1995;85(12):3577–3585.
   PubMed Web of Science ®Google Scholar
• Shibata Y, Foster LA, Kurimoto M, Immunoregulatory roles of IL-10 in innate immunity: IL-10 inhibits macrophage production of IFN-gamma-inducing factors but enhances NK cell production of IFN-gamma. J Immunol 1998;161(8):4283–4288.
   PubMedGoogle Scholar
• Chiu BC, Stolberg VR, Chensue SW. Mononuclear phagocyte-derived IL-10 suppresses the innate IL-12/IFN-gamma axis in lung-challenged aged mice. J Immunol 2008;181(5):3156–3166.
   PubMedGoogle Scholar
• Scott MJ, Hoth JJ, Turina M, Woods DR, Interleukin-10 suppresses natural killer cell but not natural killer T cell activation during bacterial infection. Cytokine 2006;33(2):79–86.
   PubMedGoogle Scholar
• Coudert JD, Zimmer J, Tomasello E, Altered NKG2D function in NK cells induced by chronic exposure to NKG2D ligand-expressing tumor cells. Blood 2005;106(5):1711–1717.
   PubMed Web of Science ®Google Scholar
• Oppenheim DE, Roberts SJ, Clarke SL, Sustained localized expression of ligand for the activating NKG2D receptor impairs natural cytotoxicity in vivo and reduces tumor immunosurveillance. Nat Immunol 2005;6(9):928–937.
   PubMed Web of Science ®Google Scholar
• Sun J, Madan R, Karp CL, Braciale TJ. Effector T cells control lung inflammation during acute influenza virus infection by producing IL-10. Nat Med 2009;15(3):277–284.
   PubMed Web of Science ®Google Scholar
• Peppa D, Micco L, Javaid A, Blockade of immunosuppressive cytokines restores NK cell antiviral function in chronic hepatitis B virus infection. PLoS Pathog 2010;6(12):e1001227.
   PubMed Web of Science ®Google Scholar
• Cheong JY, Cho SW, Hwang IL, Association between chronic hepatitis B virus infection and interleukin-10, tumor necrosis factor-alpha gene promoter polymorphisms. J Gastroenterol Hepatol 2006;21(7):1163–1169.
   PubMed Web of Science ®Google Scholar
• Miyazoe S, Hamasaki K, Nakata K, Influence of interleukin-10 gene promoter polymorphisms on disease progression in patients chronically infected with hepatitis B virus. Am J Gastroenterol 2002;97(8):2086–2092.
   PubMedGoogle Scholar
• Stacey MA, Marsden M, Wang EC, IL-10 restricts activation-induced death of NK cells during acute murine cytomegalovirus infection. J Immunol 2011;187(6):2944–2952.
   PubMed Web of Science ®Google Scholar
• Grant LR, Yao ZJ, Hedrich CM, Stat4-dependent, T-bet-independent regulation of IL-10 in NK cells. Genes Immun 2008;9(4):316–327.
   PubMedGoogle Scholar
• Gray M, Miles K, Salter D, Apoptotic cells protect mice from autoimmune inflammation by the induction of regulatory B cells. Proc Natl Acad Sci USA 2007;104(35):14080–14085.
   PubMed Web of Science ®Google Scholar
• Carter NA, Vasconcellos R, Rosser EC, 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(10):5569–5579.
   PubMed Web of Science ®Google Scholar
• Hao J, Liu R, Piao W, Central nervous system (CNS)-resident natural killer cells suppress Th17 responses and CNS autoimmune pathology. J Exp Med 2010;207(9):1907–1921.
   PubMed Web of Science ®Google Scholar