Transcriptional regulation of IL-10 and its cell-specific role in vivo

Critical Reviews in Immunology

Volumn 34, Issue 4, 2014, Pages 315-345

  Mackenzie, Kirsty F ^a   Pattison, Michael J ^a   Arthur, J Simon C ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

B10; CREB; Interleukin 10; Macrophage; STAT3; Tr1

Indexed keywords

INTERLEUKIN 10; TOLL LIKE RECEPTOR;

ADOPTIVE TRANSFER; ARTICLE; B LYMPHOCYTE; BONE MARROW CELL; CELL FUNCTION; CELL SPECIFICITY; CYTOKINE PRODUCTION; CYTOTOXIC T LYMPHOCYTE; DENDRITIC CELL; IMMUNOCOMPETENT CELL; IN VIVO STUDY; INFLAMMATORY BOWEL DISEASE; INTESTINE FLORA; KNOCKOUT MOUSE; MACROPHAGE; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; TH1 CELL; TH17 CELL; TH2 CELL; ANIMAL; ANTIBODY SPECIFICITY; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; HUMAN; IMMUNOLOGY; INTRACELLULAR SPACE; METABOLISM; SIGNAL TRANSDUCTION; T LYMPHOCYTE SUBPOPULATION;

ANIMALS; DENDRITIC CELLS; GENE EXPRESSION REGULATION; HUMANS; INTERLEUKIN-10; INTRACELLULAR SPACE; MACROPHAGES; ORGAN SPECIFICITY; SIGNAL TRANSDUCTION; T-LYMPHOCYTE SUBSETS; TRANSCRIPTION, GENETIC;

EID: 84902505212     PISSN: 10408401     EISSN: None     Source Type: Journal    
DOI: 10.1615/CritRevImmunol.2014010694     Document Type: Article

References (204)

1. Saraiva M, O'Garra A. The regulation of IL-10 production by immune cells. Nat Rev Immunol. 2010 Mar;10(3):170-81.
2. Ouyang W, Rutz S, Crellin NK, Valdez PA, Hymowitz SG. Regulation and functions of the IL-10 family of cytokines in inflammation and disease. Annu Rev Immunol. 2011;29:71-109.
3. Defrance T, Vanbervliet B, Brière F, Durand I, Rousset F, Banchereau J. Interleukin 10 and transforming growth factor beta cooperate to induce anti-CD40-activated naive human B cells to secrete immunoglobulin A. J Exp Med. 1992;175(3):671-82.
4. Rousset F, Garcia E, Defrance T, Péronne C, Vezzio N, Hsu DH, Kastelein R, Moore KW, Banchereau J. Interleukin 10 is a potent growth and differentiation factor for activated human B lymphocytes. Proc Natl Acad Sci U S A. 1992;89(5):1890-3.
5. Go NF, Castle BE, Barrett R, Kastelein R, Dang W, Mosmann TR, Moore KW, Howard M. Interleukin 10, a novel B cell stimulatory factor: unresponsiveness of X chromosome-linked immunodeficiency B cells. J Exp Med. 1990;172(6):1625-31.
6. Llorente L, Zou W, Levy Y, Richaud-Patin Y, Wijdenes J, Alcocer-Varela J, Morel-Fourrier B, Brouet JC, Alarcon-Segovia D, Galanaud P, Emilie D. Role of interleukin 10 in the B lymphocyte hyperactivity and autoantibody production of human systemic lupus erythematosus. J Exp Med. 1995;181(3):839-44.
7. Kotenko SV, Krause CD, Izotova LS, Pollack BP, Wu W, Pestka S. Identification and functional characterization of a second chain of the interleukin-10 receptor complex. EMBO J. 1997;16(19):5894-903.
8. Tan JC, Indelicato SR, Narula SK, Zavodny PJ, Chou CC. Characterization of interleukin-10 receptors on human and mouse cells. J Biol Chem. 2001;268(28):21053-9.
9. Yoon S-I, Jones BC, Logsdon NJ, Harris BD, Deshpande A, Radaeva S, Halloran BA, Gao B, Walter MR. Structure and mechanism of receptor sharing by the IL-10R2 common chain. Structure. 2010;18(5):638-48.
10. Pils MC, Pisano F, Fasnacht N, Heinrich J-M, Groebe L, Schippers A, Rozell B, Jack RS, Müller W. Monocytes/macrophages and/or neutrophils are the target of IL-10 in the LPS endotoxemia model. Eur J Immunol. 2010;40(2):443-8.
11. Spencer SD, Di Marco F, Hooley J, Pitts-Meek S, Bauer M, Ryan AM, Sordat B, Gibbs VC, Aguet M. The orphan receptor CRF2-4 is an essential subunit of the interleukin 10 receptor. J Exp Med. 1998;187(4):571-8.
12. Finbloom DS, Winestock KD. IL-10 induces the tyrosine phosphorylation of tyk2 and Jak1 and the differential assembly of STAT1 alpha and STAT3 complexes in human T cells and monocytes. J Immunol. 1995;155(3):1079-90.
13. Ho AS, Wei SH, Mui AL, Miyajima A, Moore KW. Functional regions of the mouse interleukin-10 receptor cytoplasmic domain. Mol Cell Biol. 1995;15(9):5043-53.
14. Rodig SJ, Meraz MA, White JM, Lampe PA, Riley JK, Arthur CD, King KL, Sheehan KC, Yin L, Pennica D, Johnson EM, Schreiber RD. Disruption of the Jak1 gene demonstrates obligatory and nonredundant roles of the Jaks in cytokine-induced biologic responses. Cell. 1998;93(3):373-83.
15. Shimoda K, Kato K, Aoki K, Matsuda T, Miyamoto A, Shibamori M, Yamashita M, Numata A, Takase K, Kobayashi S, Shibata S, Asano Y, Gondo H, Sekiguchi K, Nakayama K, Nakayama T, Okamura T, Okamura S, Niho Y, Nakayama K. Tyk2 plays a restricted role in IFN alpha signaling, although it is required for IL-12-mediated T cell function. Immunity. 2000;13(4):561-71.
16. Karaghiosoff M, Neubauer H, Lassnig C, Kovarik P, Schindler H, Pircher H, McCoy B, Bogdan C, Decker T, Brem G, Pfeffer K, Müller M. Partial impairment of cytokine responses in Tyk2-deficient mice. Immunity. 2000;13(4):549-60.
17. Shaw MH, Freeman GJ, Scott MF, Fox BA, Bzik DJ, Belkaid Y, Yap GS. Tyk2 negatively regulates adaptive Th1 immunity by mediating IL-10 signaling and promoting IFN-gamma-dependent IL-10 reactivation. J Immunol. 2006;176(12):7263-71.
18. Sohn SJ, Barrett K, Van Abbema A, Chang C, Kohli PB, Kanda H, Smith J, Lai Y, Zhou A, Zhang B, Yang W, Williams K, Macleod C, Hurley CA, Kulagowski JJ, Lewin-Koh N, Dengler HS, Johnson AR, Ghilardi N, Zak M, Liang J, Blair WS, Magnuson S, Wu LC. A Restricted Role for TYK2 Catalytic Activity in Human Cytokine Responses Revealed by Novel TYK2-Selective Inhibitors. J Immunol. 2013;191(5):2205-16.
19. Minegishi Y, Saito M, Morio T, Watanabe K, Agematsu K, Tsuchiya S, Takada H, Hara T, Kawamura N, Ariga T, Kaneko H, Kondo N, Tsuge I, Yachie A, Sakiyama Y, Iwata T, Bessho F, Ohishi T, Joh K, Imai K, Kogawa K, Shinohara M, Fujieda M, Wakiguchi H, Pasic S, Abinun M, Ochs HD, Renner ED, Jansson A, Belohradsky BH, Metin A, Shimizu N, Mizutani S, Miyawaki T, Nonoyama S, Karasuyama H. Human tyrosine kinase 2 deficiency reveals its requisite roles in multiple cytokine signals involved in innate and acquired immunity. Immunity. 2006;25(5):745-55.
20. Riley JK, Takeda K, Akira S, Schreiber RD. Interleukin-10 receptor signaling through the JAK-STAT pathway. Requirement for two distinct receptor-derived signals for anti-inflammatory action. J Biol Chem. 1999;274(23):16513-21.
21. Meraz MA, White JM, Sheehan KC, Bach EA, Rodig SJ, Dighe AS, Kaplan DH, Riley JK, Greenlund AC, Campbell D, Carver-Moore K, DuBois RN, Clark R, Aguet M, Schreiber RD. Targeted disruption of the Stat1 gene in mice reveals unexpected physiologic specificity in the JAK-STAT signaling pathway. Cell. 1996;84(3):431-42.
22. Takeda K, Clausen BE, Kaisho T, Tsujimura T. Enhanced Th1 activity and development of chronic enterocolitis in mice devoid of Stat3 in macrophages and neutrophils. Immunity. 1999.
23. Bazzoni F, Tamassia N, Rossato M, Cassatella MA. Understanding the molecular mechanisms of the multifaceted IL-10-mediated anti-inflammatory response: lessons from neutrophils. Eur J Immunol. 2010;40(9):2360-8.
24. Hutchins AP, Diez D, Miranda-Saavedra D. The IL-10/STAT3-mediated anti-inflammatory response: recent developments and future challenges. Briefings Funct Genomics. 2013;12(6): 489-98.
25. Murray PJ. The primary mechanism of the IL-10-regulated antiinflammatory response is to selectively inhibit transcription. Proc Natl Acad Sci U S A. 2005;102(24):8686-91.
26. Ishizuka T, Okayama Y, Kobayashi H, Mori M. Interleukin-10 is localized to and released by human lung mast cells. Clin Exp Allergy. 1999;29(10):1424-32.
27. Grimbaldeston MA, Nakae S, Kalesnikoff J, Tsai M, Galli SJ. Mast cell-derived interleukin 10 limits skin pathology in contact dermatitis and chronic irradiation with ultraviolet B. Nat Immunol. 2007;8(10):1095-104.
28. Zhang X, Majlessi L, Deriaud E, Leclerc C, LoMan R. Coactivation of Syk kinase and MyD88 adaptor protein pathways by bacteria promotes regulatory properties of neutrophils. Immunity. 2009;31(5):761-71.
29. Medzhitov R. TLR-mediated innate immune recognition. Semin Immunol. 2007;19(1):1-2.
30. Kawai T, Akira S. The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat Immunol. 2010 May;11(5):373-84.
31. Iwasaki A, Medzhitov R. Regulation of adaptive immunity by the innate immune system. Science. 2010;327(5963):291-5.
32. Takeuchi O, Akira S. Pattern recognition receptors and inflammation. Cell. 2010;140(6):805-20.
33. Akira S, Takeda K. Functions of toll-like receptors: lessons from KO mice. C R Biol. 2004;327(6):581-9.
34. Akira S, Takeda K. Toll-like receptor signalling. Nat Rev Immunol. 2004;4(7):499-511.
35. Clark K, Nanda S, Cohen P. Molecular control of the NEMO family of ubiquitin-binding proteins. Nat Rev Mol Cell Biol. 2013;14(10):673-85.
36. Boonstra A, Rajsbaum R, Holman M, Marques R, Asselin-Paturel C, Pereira JP, Bates EEM, Akira S, Vieira P, Liu Y-J, Trinchieri G, O'Garra A. Macrophages and myeloid dendritic cells, but not plasmacytoid dendritic cells, produce IL-10 in response to MyD88- and TRIF-dependent TLR signals, and TLR-independent signals. J Immunol. 2006;177(11):7551-8.
37. Yamamoto M, Sato S, Hemmi H, Hoshino K, Kaisho T, Sanjo H, Takeuchi O, Sugiyama M, Okabe M, Takeda K, Akira S. Role of adaptor TRIF in the MyD88-independent Toll-like receptor signaling pathway. Science. 2003;301(5633):640-3.
38. Häcker H, Redecke V, Blagoev B, Kratchmarova I, Hsu L-C, Wang GG, Kamps MP, Raz E, Wagner H, Häcker G, Mann M, Karin M. Specificity in Toll-like receptor signalling through distinct effector functions of TRAF3 and TRAF6. Nature. 2006 Jan 12;439(7073):204-7.
39. Pattison MJ, MacKenzie KF, Arthur JSC. Inhibition of JAKs in macrophages increases lipopolysaccharide-induced cytokine production by blocking IL-10-mediated feedback. J Immunol. 2012 Sep 15;189(6):2784-92.
40. Chang EY, Guo B, Doyle SE, Cheng G. Cutting edge: involvement of the type I IFN production and signaling pathway in lipopolysaccharide-induced IL-10 production. J Immunol. 2007;178(11):6705-9.
41. Liu Y-W, Chen C-C, Tseng H-P, Chang W-C. Lipopolysaccharide-induced transcriptional activation of interleukin-10 is mediated by MAPK- and NF-κB-induced CCAAT/ enhancer-binding protein delta in mouse macrophages. Cell Signal. 2006;18(9): 1492-500.
42. Banerjee A, Gugasyan R, McMahon M, Gerondakis S. Diverse Toll-like receptors utilize Tpl2 to activate extracellular signal-regulated kinase (ERK) in hemopoietic cells. Proc Natl Acad Sci U S A. 2006;103(9):3274-9.
43. Cao S, Zhang X, Edwards JP, Mosser DM. NF-kappaB1 (p50) homodimers differentially regulate pro- and anti-inflammatory cytokines in macrophages. J Biol Chem. 2006;281(36): 26041-50.
44. Saraiva M, Christensen JR, Tsytsykova AV, Goldfeld AE, Ley SC, Kioussis D, O'Garra A. Identification of a macrophage-specific chromatin signature in the IL-10 locus. J Immunol. 2005;175(2):1041-6.
45. Strickson S, Campbell DG, Emmerich CH, Knebel A, Plater L, Ritorto MS, Shpiro N, Cohen P. The anti-inflammatory drug BAY 11-7082 suppresses the MyD88-dependent signalling network by targeting the ubiquitin system. Biochem J. 2013 May 1;451(3):427-37.
46. Arthur JSC, Ley SC. Mitogen-activated protein kinases in innate immunity. Nat Rev Immunol. 2013 Sep;13(9):679-92.
47. Kim C, Sano Y, Todorova K, Carlson BA, Arpa L, Celada A, Lawrence T, Otsu K, Brissette JL, Arthur JSC, Park JM. The kinase p38 alpha serves cell type-specific inflammatory functions in skin injury and coordinates pro- and anti-inflammatory gene expression. Nat Immunol. 2008 Sep;9(9):1019-27.
48. Salojin KV, Owusu IB, Millerchip KA, Potter M, Platt KA, Oravecz T. Essential role of MAPK phosphatase-1 in the negative control of innate immune responses. J Immunol. 2006;176(3):1899-907.
49. Risco A, del Fresno C, Mambol A, Alsina-Beauchamp D, MacKenzie KF, Yang H-T, Barber DF, Morcelle C, Arthur JSC, Ley SC, Ardavin C, Cuenda A. p38γ and p38δ kinases regulate the Toll-like receptor 4 (TLR4)-induced cytokine production by controlling ERK1/2 protein kinase pathway activation. Proc Natl Acad Sci U S A. 2012 Jul 10;109(28):11200-5.
50. Naqvi S, Macdonald A, McCoy CE, Darragh J, Reith AD, Arthur JSC. Characterization of the cellular action of the MSK inhibitor SB-747651A. Biochem J. 2012 Jan 1;441(1):347-57.
51. Ananieva O, Darragh J, Johansen C, Carr JM, McIlrath J, Park JM, Wingate A, Monk CE, Toth R, Santos SG, Iversen L, Arthur JSC. The kinases MSK1 and MSK2 act as negative regulators of Toll-like receptor signaling. Nat Immunol. 2008 Sep;9(9):1028-36.
52. Dyson MH, Thomson S, Inagaki M, Goto H, Arthur SJ, Nightingale K, Iborra FJ, Mahadevan LC. MAP kinase-mediated phosphorylation of distinct pools of histone H3 at S10 or S28 via mitogen- and stress-activated kinase 1/2. J Cell Sci. 2005;118(Pt 10):2247-59.
53. Soloaga A, Thomson S, Wiggin GR, Rampersaud N, Dyson MH, Hazzalin CA, Mahadevan LC, Arthur JSC. MSK2 and MSK1 mediate the mitogen- and stress-induced phosphorylation of histone H3 and HMG-14. EMBO J. 2003 Jun 2;22(11):2788-97.
54. Bettelli E, Das MP, Howard ED, Weiner HL, Sobel RA, Kuchroo VK. 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(7):3299-306.
55. Zhang X, Edwards JP, Mosser DM. Dynamic and transient remodeling of the macrophage IL-10 promoter during transcription. J Immunol. 2006;177(2):1282-8.
56. Wiggin GR, Soloaga A, Foster JM, Murray-Tait V, Cohen P, Arthur JSC. MSK1 and MSK2 are required for the mitogen- and stress-induced phosphorylation of CREB and ATF1 in fibroblasts. Mol Cell Biol. 2002 Apr;22(8):2871-81.
57. Gee K, Angel JB, Ma W, Mishra S, Gajanayaka N, Parato K, Kumar A. Intracellular HIV-Tat expression induces IL-10 synthesis by the CREB-1 transcription factor through Ser133 phosphorylation and its regulation by the ERK1/2 MAPK in human monocytic cells. J Biol Chem. 2006 Oct 20;281(42):31647-58.
58. Elcombe SE, Naqvi S, Van Den Bosch MWM, MacKenzie KF, Cianfanelli F, Brown GD, Arthur JSC. Dectin-1 regulates IL-10 production via a MSK1/2 and CREB dependent pathway and promotes the induction of regulatory macrophage markers. PLoS ONE. 2013;8(3):e60086.
59. Naqvi S, Martin KJ, Arthur JSC. CREB phosphorylation at Ser133 regulates transcription via distinct mechanisms downstream of cAMP and MAPK signaling. Biochem J. Mar 15 2014;458(3):469-79.
60. Johannessen M, Delghandi MP, Moens U. What turns CREB on? Cell Signal. 2004 Nov;16(11):1211-27.
61. Tyson DR, Swarthout JT, Jefcoat SC, Partridge NC. PTH induction of transcriptional activity of the cAMP response element-binding protein requires the serine 129 site and glycogen synthase kinase-3 activity, but not casein kinase II sites. Endocrinology. 2002 Feb;143(2):674-82.
62. Tullai JW, Chen J, Schaffer ME, Kamenetsky E, Kasif S, Cooper GM. Glycogen synthase kinase-3 represses cyclic AMP response element-binding protein (CREB)-targeted immediate early genes in quiescent cells. J Biol Chem. 2007 Mar 30;282(13):9482-91.
63. Hu X, Paik PK, Chen J, Yarilina A, Kockeritz L, Lu T T, Woodgett JR, Ivashkiv LB. IFN-gamma suppresses IL-10 production and synergizes with TLR2 by regulating GSK3 and CREB/ AP-1 proteins. Immunity. 2006 May;24(5): 563-74.
64. Martin M, Rehani K, Jope RS, Michalek SM. Toll-like receptor-mediated cytokine production is differentially regulated by glycogen synthase kinase 3. Nat Immunol. 2005;6(8):777-84.
65. Wang H, Brown J, Garcia CA, Tang Y, Benakanakere MR, Greenway T, Alard P, Kinane DF, Martin M. The role of glycogen synthase kinase 3 in regulating IFN-β-mediated IL-10 production. J Immunol. 2011 Jan 15;186(2): 675-84.
66. Ehlting C, Ronkina N, Böhmer O, Albrecht U, Bode KA, Lang KS, Kotlyarov A, Radzioch D, Gaestel M, Häussinger D, Bode JG. Distinct functions of the mitogen-activated protein kinase-activated protein (MAPKAP) kinases MK2 and MK3: MK2 mediates lipopolysaccharide-induced signal transducers and activators of transcription 3 (STAT3) activation by preventing negative regulatory effects of MK3. J Biol Chem. 2011;286(27):24113-24.
67. Mellett M, Atzei P, Jackson R, O'Neill LA, Moynagh PN. Mal mediates TLR-induced activation of CREB and expression of IL-10. J Immunol. 2011;186(8):4925-35.
68. Ronkina N, Menon MB, Schwermann J, Tiedje C, Hitti E, Kotlyarov A, Gaestel M. MAPKAP kinases MK2 and MK3 in inflammation: complex regulation of TNF biosynthesis via expression and phosphorylation of tristetraprolin. Biochem Pharm. 2010;80(12):1915-20.
69. Stoecklin G, Tenenbaum SA, Mayo T, Chittur SV, George AD, Baroni TE, Blackshear PJ, Anderson P. Genome-wide analysis identifies interleukin-10 mRNA as target of tristetraprolin. J Biol Chem. 2008;283(17): 11689-99.
70. Ronkina N, Kotlyarov A, Dittrich-Breiholz O, Kracht M, Hitti E, Milarski K, Askew R, Marusic S, Lin L-L, Gaestel M, Telliez J-B. The mitogen-activated protein kinase (MAPK)-activated protein kinases MK2 and MK3 cooperate in stimulation of tumor necrosis factor biosynthesis and stabilization of p38 MAPK. Mol Cell Biol. 2007;27(1):170-81.
71. Tan NY, Khachigian LM. Sp1 phosphorylation and its regulation of gene transcription. Mol Cell Biol. 2009;29(10):2483-8.
72. D'Addario M, Arora PD, McCulloch CA. Role of p38 in stress activation of Sp1. Gene. 2006;379:51-61.
73. Ma W, Lim W, Gee K, Aucoin S, Nandan D, Kozlowski M, Diaz-Mitoma F, Kumar A. The p38 mitogen-activated kinase pathway regulates the human interleukin-10 promoter via the activation of Sp1 transcription factor in lipopolysaccharide-stimulated human macrophages. J Biol Chem. 2001;276(17): 13664-74.
74. Brightbill HD, Plevy SE, Modlin RL, Smale ST. A prominent role for Sp1 during lipopolysaccharide-mediated induction of the IL-10 promoter in macrophages. J Immunol. 2000;164(4):1940-51.
75. Tone M, Powell MJ, Tone Y, Thompson SA, Waldmann H. IL-10 gene expression is controlled by the transcription factors Sp1 and Sp3. J Immunol. 2000;165(1):286-91.
76. Cao S, Liu J, Song L, Ma X. The protooncogene c-Maf is an essential transcription factor for IL-10 gene expression in macrophages. J Immunol. 2005;174(6):3484-92.
77. Sii-Felice K, Pouponnot C, Gillet S, Lecoin L, Girault J-A, Eychène A, Felder-Schmittbuhl M-P. MafA transcription factor is phosphorylated by p38 MAP kinase. FEBS Lett. 2005;579(17):3547-54.
78. Kim S-H, Serezani CH, Okunishi K, Zaslona Z, Aronoff DM, Peters-Golden M. Distinct protein kinase A anchoring proteins direct prostaglandin E2 modulation of Toll-like receptor signaling in alveolar macrophages. J Biol Chem. 2011;286(11):8875-83.
79. MacKenzie KF, Clark K, Naqvi S, McGuire VA, Nöehren G, Kristariyanto Y, van den Bosch M, Mudaliar M, McCarthy PC, Pattison MJ, Pedrioli PGA, Barton GJ, Toth R, Prescott A, Arthur JSC. PGE(2) induces macrophage IL-10 production and a regulatory-like phenotype via a protein kinase A-SIK-CRTC3 pathway. J Immunol. 2013 Jan 15;190(2):565-77.
80. Feng W, Wang Y, Zhang J, Wang X, Li C, Chang Z. Effects of CTx and 8-bromo-cAMP on LPS-induced gene expression of cytokines in murine peritoneal macrophages. Biochem Biophys Res Commun. 2000;269(2):570-3.
81. Eigler A, Siegmund B, Emmerich U, Baumann KH, Hartmann G, Endres S. Anti-inflammatory activities of cAMP-elevating agents: enhancement of IL-10 synthesis and concurrent suppression of TNF production. J Leukoc Biol. 1998;63(1): 101-7.
82. Clark K, MacKenzie KF, Petkevicius K, Kristariyanto Y, Zhang J, Choi HG, Peggie M, Plater L, Pedrioli PGA, McIver E, Gray NS, Arthur JSC, Cohen P. Phosphorylation of CRTC3 by the salt-inducible kinases controls the interconversion of classically activated and regulatory macrophages. Proc Natl Acad Sci U S A. 2012 Oct 16;109(42):16986-91.
83. Kang Y-J, Wingerd BA, Arakawa T, Smith WL. Cyclooxygenase-2 gene transcription in a macrophage model of inflammation. J Immunol. 2006;177(11):8111-22.
84. Haselow K, Bode JG, Wammers M, Ehlting C, Keitel V, Kleinebrecht L, Schupp A-K, Häussinger D, Graf D. Bile acids PKA-dependently induce a switch of the IL-10/IL-12 ratio and reduce proinflammatory capability of human macrophages. J Leukoc Biol. 2013.
85. Haskó G, Pacher P, Deitch EA, Vizi ES. Shaping of monocyte and macrophage function by adenosine receptors. Pharmacol Ther. 2007 Feb;113(2):264-75.
86. Csóka B, Németh ZH, Virág L, Gergely P, Leibovich SJ, Pacher P, Sun C-X, Blackburn MR, Vizi ES, Deitch EA, Haskó G. A2A adenosine receptors and C/EBPbeta are crucially required for IL-10 production by macrophages exposed to Escherichia coli. Blood. 2007;110(7): 2685-95.
87. Liu Y-W, Tseng H-P, Chen L-C, Chen B-K, Chang W-C. Functional cooperation of simian virus 40 promoter factor 1 and CCAAT/ enhancer-binding protein beta and delta in lipopolysaccharide-induced gene activation of IL-10 in mouse macrophages. J Immunol. 2003;171(2):821-8.
88. Kerrigan AM, Brown GD. Syk-coupled C-type lectins in immunity. Trends Immunol. 2011 Apr;32(4):151-6.
89. Kelly EK, Wang L, Ivashkiv LB. Calcium-activated pathways and oxidative burst mediate zymosan-induced signaling and IL-10 production in human macrophages. J Immunol. 2010;184(10):5545-52.
90. Slack EC, Robinson MJ, Hernanz-Falcón P, Brown GD, Williams DL, Schweighoffer E, Tybulewicz VL, Reis e Sousa C. Syk-dependent ERK activation regulates IL-2 and IL-10 production by DC stimulated with zymosan. Eur J Immunol. 2007;37(6):1600-12.
91. Alvarez Y, Municio C, Alonso S, Sánchez Crespo M, Fernández N. The induction of IL-10 by zymosan in dendritic cells depends on CREB activation by the coactivators CREB-binding protein and TORC2 and autocrine PGE2. J Immunol. 2009;183(2):1471-9.
92. van Vliet SJ, Bay S, Vuist IM, Kalay H, García-Vallejo JJ, Leclerc C, van Kooyk Y. MGL signaling augments TLR2-mediated responses for enhanced IL-10 and TNF-α secretion. J Leukoc Biol. 2013;94(2):315-23.
93. Gringhuis SI, Dunnen den J, Litjens M, van Het Hof B, van Kooyk Y, Geijtenbeek TBH. C-type lectin DC-SIGN modulates Toll-like receptor signaling via Raf-1 kinase-dependent acetylation of transcription factor NF-kappaB. Immunity. 2007;26(5):605-16.
94. Stuart LM, Ezekowitz RAB. Phagocytosis: elegant complexity. Immunity. 2005;22(5): 539-50.
95. Voll RE, Herrmann M, Roth EA, Stach C, Kalden JR, Girkontaite I. Immunosuppressive effects of apoptotic cells. Nature. 1997;390(6658):350-1.
96. Herrmann M, Voll RE, Zoller OM, Hagenhofer M, Ponner BB, Kalden JR. Impaired phagocytosis of apoptotic cell material by monocyte-derived macrophages from patients with systemic lupus erythematosus. Arthritis Rheum. 1998;41(7):1241-50.
97. Gal A, Li Y, Thompson DA, Weir J, Orth U, Jacobson SG, Apfelstedt-Sylla E, Vollrath D. Mutations in MERTK, the human orthologue of the RCS rat retinal dystrophy gene, cause retinitis pigmentosa. Nat Genet. 2000;26(3):270-1.
98. Camenisch TD, Koller BH, Earp HS, Matsushima GK. A novel receptor tyrosine kinase, Mer, inhibits TNF-alpha production and lipopolysaccharide-induced endotoxic shock. J Immunol. 1999;162(6):3498-503.
99. Byrne A, Reen DJ. Lipopolysaccharide induces rapid production of IL-10 by monocytes in the presence of apoptotic neutrophils. J Immunol. 2002;168(4):1968-77.
100. Chung EY, Liu J, Homma Y, Zhang Y, Brendolan A, Saggese M, Han J, Silverstein R, Selleri L, Ma X. Interleukin-10 expression in macrophages during phagocytosis of apoptotic cells is mediated by homeodomain proteins Pbx1 and Prep-1. Immunity. 2007;27(6):952-64.
101. Staples KJ, Smallie T, Williams LM, Foey A, Burke B, Foxwell BMJ, Ziegler-Heitbrock L. IL-10 induces IL-10 in primary human monocyte-derived macrophages via the transcription factor Stat3. J Immunol. 2007;178(8):4779-85.
102. Cheng F, Wang H-W, Cuenca A, Huang M, Ghansah T, Brayer J, Kerr WG, Takeda K, Akira S, Schoenberger SP, Yu H, Jove R, Sotomayor EM. A critical role for Stat3 signaling in immune tolerance. Immunity. 2003;19(3):425-36.
103. Skok J, Poudrier J, Gray D. Dendritic cell-derived IL-12 promotes B cell induction of Th2 differentiation: a feedback regulation of Th1 development. J Immunol. 1999;163(8): 4284-91.
104. Sayi A, Kohler E, Toller IM, Flavell RA, Müller W, Roers A, Müller A. TLR-2-activated B cells suppress Helicobacter-induced preneoplastic gastric immunopathology by inducing T regulatory-1 cells. J Immunol. 2011;186(2): 878-90.
105. Wagner M, Poeck H, Jahrsdoerfer B, Rothenfusser S, Prell D, Bohle B, Tuma E, Giese T, Ellwart JW, Endres S, Hartmann G. IL-12p70-dependent Th1 induction by human B cells re-quires combined activation with CD40 ligand and CpG DNA. J Immunol. 2004;172(2):954-63.
106. Agrawal S, Gupta S. TLR1/2, TLR7, and TLR9 signals directly activate human peripheral blood naive and memory B cell subsets to produce cytokines, chemokines, and hematopoietic growth factors. J Clin Immunol. 2011;31(1):89-98.
107. Sun C-M, Deriaud E, Leclerc C, Lo-Man R. Upon TLR9 signaling, CD5+ B cells control the IL-12-dependent Th1-priming capacity of neonatal DCs. Immunity. 2005;22(4):467-77.
108. Lee K-G, Xu S, Wong E-T, Tergaonkar V, Lam K-P. Bruton's tyrosine kinase separately regulates NFkappaB p65RelA activation and cytokine interleukin (IL)-10/IL-12 production in TLR9-stimulated B Cells. J Biol Chem. 2008;283(17):11189-98.
109. Schmidt NW, Thieu VT, Mann BA, Ahyi A-NN, Kaplan MH. Bruton's tyrosine kinase is required for TLR-induced IL-10 production. J Immunol. 2006;177(10):7203-10.
110. Zhang X, Deriaud E, Jiao X, Braun D, Leclerc C, Lo-Man R. Type I interferons protect neonates from acute inflammation through interleukin 10-producing B cells. J Exp Med. 2007;204(5):1107-18.
111. Giordani L, Sanchez M, Libri I, Quaranta MG, Mattioli B, Viora M. IFN-alpha amplifies human naive B cell TLR-9-mediated activation and Ig production. J Leukoc Biol. 2009;86(2):261-71.
112. Matsumoto M, Fujii Y, Baba A, Hikida M, Kurosaki T, Baba Y. The calcium sensors STIM1 and STIM2 control B cell regulatory function through interleukin-10 production. Immunity. 2011;34(5):703-14.
113. Vasanthakumar A, Kallies A. IL-27 paves different roads to Tr1. Eur J Immunol. 2013;43(4):882-5.
114. Glimcher LH, Murphy KM. Lineage commitment in the immune system: the T helper lymphocyte grows up. Genes Dev. 2000;14(14):1693-711.
115. Hirahara K, Poholek A, Vahedi G, Laurence A, Kanno Y, Milner JD, O'Shea JJ. Mechanisms underlying helper T-cell plasticity: implications for immune-mediated disease. J Allergy Clin Immunol. 2013;131(5):1276-87.
116. Lee C-G, Kang K-H, So J-S, Kwon H-K, Son J-S, Song M-K, Sahoo A, Yi H-J, Hwang K-C, Matsuyama T, Yui K, Im S-H. A distal cis-regulatory element, CNS-9, controls NFAT1 and IRF4-mediated IL-10 gene activation in T helper cells. Mol Immunol. 2009;46(4):613-21.
117. Jones EA, Flavell RA. Distal enhancer elements transcribe intergenic RNA in the IL-10 family gene cluster. J Immunol. 2005;175(11):7437-46.
118. Stumhofer JS, Silver JS, Laurence A, Porrett PM, Harris TH, Turka LA, Ernst M, Saris CJM, O'Shea JJ, Hunter CA. Interleukins 27 and 6 induce STAT3-mediated T cell production of interleukin 10. Nat Immunol. 2007;8(12): 1363-71.
119. Mosmann TR, Cherwinski H, Bond MW, Giedlin MA, Coffman RL. Two types of murine helper T cell clone. I. Definition according to profiles of lymphokine activities and secreted proteins. J Immunol. 1986;136(7):2348-57.
120. 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):2081-95.
121. Shoemaker J, Saraiva M, O'Garra A. GATA-3 directly remodels the IL-10 locus independently of IL-4 in CD4+ T cells. J Immunol. 2006; 176(6):3470-9.
122. Chang H-D, Helbig C, Tykocinski L, Kreher S, Koeck J, Niesner U, Radbruch A. Expression of IL-10 in Th memory lymphocytes is conditional on IL-12 or IL-4, unless the IL-10 gene is imprinted by GATA-3. Eur J Immunol. 2007;37(3):807-17.
123. Scheinman EJ, Avni O. Transcriptional regulation of GATA3 in T helper cells by the integrated activities of transcription factors downstream of the interleukin-4 receptor and T cell receptor. J Biol Chem. 2009;284(5):3037-48.
124. Kim JI, Ho IC, Grusby MJ, Glimcher LH. The transcription factor c-Maf controls the production of interleukin-4 but not other Th2 cytokines. Immunity. 1999;10(6):745-51.
125. Ouyang W, Löhning M, Gao Z, Assenmacher M, Ranganath S, Radbruch A, Murphy KM. Stat6-independent GATA-3 autoactivation directs IL-4-independent Th2 development and commitment. Immunity. 2000;12(1):27-37.
126. Maneechotesuwan K, Xin Y, Ito K, Jazrawi E, Lee K-Y, Usmani OS, Barnes PJ, Adcock IM. Regulation of Th2 cytokine genes by p38 MAPK-mediated phosphorylation of GATA-3. J Immunol. 2007;178(4):2491-8.
127. Saraiva M, Christensen JR, Veldhoen M, Murphy TL, Murphy KM, O'Garra A. 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):209-19.
128. Ho IC, Hodge MR, Rooney JW, Glimcher LH. The proto-oncogene c-maf is responsible for tissue-specific expression of interleukin-4. Cell. 1996;85(7):973-83.
129. Ahyi A-NN, Chang H-C, Dent AL, Nutt SL, Kaplan MH. IFN regulatory factor 4 regulates the expression of a subset of Th2 cytokines. J Immunol. 2009;183(3):1598-606.
130. Kashiwada M, Cassel SL, Colgan JD, Rothman PB. NFIL3/E4BP4 controls type 2 T helper cell cytokine expression. EMBO J. 2011;30(10): 2071-82.
131. Motomura Y, Kitamura H, Hijikata A, Matsunaga Y, Matsumoto K, Inoue H, Atarashi K, Hori S, Watarai H, Zhu J, Taniguchi M, Kubo M. The transcription factor E4BP4 regulates the production of IL-10 and IL-13 in CD4+ T cells. Nat Immunol. 2011;12(5):450-9.
132. O'Garra A, Vieira P. T(H)1 cells control themselves by producing interleukin-10. Nat Rev Immunol. 2007;7(6):425-8.
133. Jankovic D, Kullberg MC, Feng CG, Goldszmid RS, Collazo CM, Wilson M, Wynn TA, Kamanaka M, Flavell RA, Sher A. 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):273-83.
134. Freitas do Rosário AP, Lamb T, Spence P, Stephens R, Lang A, Roers A, Müller W, O'Garra A, Langhorne J. IL-27 promotes IL-10 production by effector Th1 CD4+ T cells: a critical mechanism for protection from severe immunopathology during malaria infection. J Immunol. 2012;188(3):1178-90.
135. 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):285-97.
136. Kitani A, Fuss I, Nakamura K, Kumaki F, Usui T, Strober W. Transforming growth factor (TGF)-beta1-producing regulatory T cells induce Smad-mediated interleukin 10 secretion that facilitates coordinated immunoregulatory activity and amelioration of TGF-beta1-mediated fibrosis. J Exp Med. 2003;198(8):1179-88.
137. Huss DJ, Winger RC, Cox GM, Guerau-de-Arellano M, Yang Y, Racke MK, Lovett-Racke AE. TGF-β signaling via Smad4 drives IL-10 production in effector Th1 cells and reduces T-cell trafficking in EAE. Eur J Immunol. 2011;41(10):2987-96.
138. Brunkow ME, Jeffery EW, Hjerrild KA, Paeper B, Clark LB, Yasayko SA, Wilkinson JE, Galas D, Ziegler SF, Ramsdell F. Disruption of a new forkhead/winged-helix protein, scurfin, results in the fatal lymphoproliferative disorder of the scurfy mouse. Nat Genet. 2001;27(1):68-73.
139. Groux H, O'Garra A, Bigler M, Rouleau M, Antonenko S, de Vries JE, Roncarolo MG. A CD4+ T-cell subset inhibits antigen-specific T-cell responses and prevents colitis. Nature. 1997;389(6652):737-42.
140. Vieira PL, Christensen JR, Minaee S, O'Neill EJ, Barrat FJ, Boonstra A, Barthlott T, Stockinger B, Wraith DC, O'Garra A. IL-10-secreting regulatory T cells do not express Foxp3 but have comparable regulatory function to naturally occurring CD4+CD25+ regulatory T cells. J Immunol. 2004;172(10):5986-93.
141. Maynard CL, Harrington LE, Janowski KM, Oliver JR, Zindl CL, Rudensky AY, Weaver C T. Regulatory T cells expressing interleukin 10 develop from Foxp3+ and Foxp3- precursor cells in the absence of interleukin 10. Nat Immunol. 2007;8(9):931-41.
142. Cretney E, Xin A, Shi W, Minnich M, Masson F, Miasari M, Belz GT, Smyth GK, Busslinger M, Nutt SL, Kallies A. The transcription factors Blimp-1 and IRF4 jointly control the differentiation and function of effector regulatory T cells. Nat Immunol. 2011;12(4): 304-11.
143. Sun J, Dodd H, Moser EK, Sharma R, Braciale TJ. CD4+ T cell help and innate-derived IL-27 induce Blimp-1-dependent IL-10 production by antiviral CTLs. Nat Immunol. 2011;12(4):327-34.
144. Iwasaki Y, Fujio K, Okamura T, Yanai A, Sumitomo S, Shoda H, Tamura T, Yoshida H, Charnay P, Yamamoto K. Egr-2 transcription factor is required for Blimp-1-mediated IL-10 production in IL-27-stimulated CD4+ T cells. Eur J Immunol. 2013;43(4):1063-73.
145. Kallies A, Hawkins ED, Belz GT, Metcalf D, Hommel M, Corcoran LM, Hodgkin PD, Nutt SL. Transcriptional repressor Blimp-1 is essential for T cell homeostasis and self-tolerance. Nat Immunol. 2006;7(5):466-74.
146. Awasthi A, Carrier Y, Peron JPS, Bettelli E, Kamanaka M, Flavell RA, Kuchroo VK, Oukka M, Weiner HL. A dominant function for interleukin 27 in generating interleukin 10-producing anti-inflammatory T cells. Nat Immunol. 2007;8(12):1380-9.
147. Murugaiyan G, Mittal A, Lopez-Diego R, Maier LM, Anderson DE, Weiner HL. IL-27 is a key regulator of IL-10 and IL-17 production by human CD4+ T cells. J Immunol. 2009;183(4):2435-43.
148. Apetoh L, Quintana FJ, Pot C, Joller N, Xiao S, Kumar D, Burns EJ, Sherr DH, Weiner HL, Kuchroo VK. The aryl hydrocarbon receptor interacts with c-Maf to promote the differentiation of type 1 regulatory T cells induced by IL-27. Nat Immunol. 2010;11(9):854-61.
149. Gandhi R, Kumar D, Burns EJ, Nadeau M, Dake B, Laroni A, Kozoriz D, Weiner HL, Quintana FJ. Activation of the aryl hydrocarbon receptor induces human type 1 regulatory T cell-like and Foxp3(+) regulatory T cells. Nat Immunol. 2010;11(9):846-53.
150. Pot C, Jin H, Awasthi A, Liu SM, Lai C-Y, Madan R, Sharpe AH, Karp CL, Miaw S-C, Ho I-C, Kuchroo VK. Cutting edge: IL-27 induces the transcription factor c-Maf, cytokine IL-21, and the costimulatory receptor ICOS that coordinately act together to promote differentiation of IL-10-producing Tr1 cells. J Immunol. 2009;183(2):797-801.
151. Spolski R, Kim H-P, Zhu W, Levy DE, Leonard WJ. IL-21 mediates suppressive effects via its induction of IL-10. J Immunol. 2009;182(5):2859-67.
152. Bi Y, Liu G, Yang R. Th17 cell induction and immune regulatory effects. J Cell Physiol. 2007;211(2):273-8.
153. Weaver CT, Harrington LE, Mangan PR, Gavrieli M, Murphy KM. Th17: an effector CD4 T cell lineage with regulatory T cell ties. Immunity. 2006;24(6):677-88.
154. Xu J, Yang Y, Qiu G, Lal G, Wu Z, Levy DE, Ochando JC, Bromberg JS, Ding Y. c-Maf regulates IL-10 expression during Th17 polarization. J Immunol. 2009;182(10):6226-36.
155. Miao T, Raymond M, Bhullar P, Ghaffari E, Symonds ALJ, Meier UC, Giovannoni G, Li S, Wang P. Early growth response gene-2 controls IL-17 expression and Th17 differentiation by negatively regulating Batf. J Immunol. 2013;190(1):58-65.
156. Murphy TL, Tussiwand R, Murphy KM. Specificity through cooperation: BATF-IRF interactions control immune-regulatory networks. Nat Rev Immunol. 2013;13(7):499-509.
157. Ciofani M, Madar A, Galan C, Sellars M, Mace K, Pauli F, Agarwal A, Huang W, Parkurst CN, Muratet M, Newberry KM, Meadows S, Greenfield A, Yang Y, Jain P, Kirigin FK, Birchmeier C, Wagner EF, Murphy KM, Myers RM, Bonneau R, Littman DR. A validated regulatory network for Th17 cell specification. Cell. 2012;151(2):289-303.
158. Schraml BU, Hildner K, Ise W, Lee W-L, Smith WA-E, Solomon B, Sahota G, Sim J, Mukasa R, Cemerski S, Hatton RD, Stormo GD, Weaver CT, Russell JH, Murphy TL, Murphy KM. The AP-1 transcription factor Batf controls T(H)17 differentiation. Nature. 2009;460(7253):405-9.
159. Li P, Spolski R, Liao W, Wang L, Murphy TL, Murphy KM, Leonard WJ. BATF-JUN is critical for IRF4-mediated transcription in T cells. Nature. 2012;490(7421):543-6.
160. Palmer EM, Holbrook BC, Arimilli S, Parks GD, Alexander-Miller MA. IFNgamma-producing, virus-specific CD8+ effector cells acquire the ability to produce IL-10 as a result of entry into the infected lung environment. Virology. 2010;404(2):225-30.
161. 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):277-84.
162. 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):3642-52.
163. Redford PS, Murray PJ, O'Garra A. The role of IL-10 in immune regulation during M. tuberculosis infection. Mucosal Immunol. 2011;4(3):261-70.
164. Wilson EB, Brooks DG. The role of IL-10 in regulating immunity to persistent viral infections. Current topics in microbiology and immunology. 2011;350:39-65.
165. O'Garra A, Barrat FJ, Castro AG, Vicari A, Hawrylowicz C. Strategies for use of IL-10 or its antagonists in human disease. Immunol Rev. 2008;223:114-31.
166. Kühn R, Löhler J, Rennick D, Rajewsky K, Müller W. Interleukin-10-deficient mice develop chronic enterocolitis. Cell. 1993 Oct 22;75(2):263-74.
167. Kullberg MC, Ward JM, Gorelick PL, Caspar P, Hieny S, Cheever A, Jankovic D, Sher A. Helicobacter hepaticus triggers colitis in specific-pathogen-free interleukin-10 (IL-10)-deficient mice through an IL-12- and gamma interferon-dependent mechanism. Infect Immun. 1998;66(11):5157-66.
168. Sellon RK, Tonkonogy S, Schultz M, Dieleman LA, Grenther W, Balish E, Rennick DM, Sartor RB. Resident enteric bacteria are necessary for development of spontaneous colitis and immune system activation in interleukin-10-deficient mice. Infect Immun. 1998;66(11):5224-31.
169. Glocker E-O, Kotlarz D, Boztug K, Gertz EM, Schäffer AA, Noyan F, Perro M, Diestelhorst J, Allroth A, Murugan D, Hätscher N, Pfeifer D, Sykora K-W, Sauer M, Kreipe H, Lacher M, Nustede R, Woellner C, Baumann U, Salzer U, Koletzko S, Shah N, Segal AW, Sauerbrey A, Buderus S, Snapper SB, Grimbacher B, Klein C. Inflammatory bowel disease and mutations affecting the interleukin-10 receptor. N Engl J Med. 2009;361(21):2033-45.
170. Glocker E-O, Frede N, Perro M, Sebire N, Elawad M, Shah N, Grimbacher B. Infant colitis-it's in the genes. Lancet. 2010;376(9748):1272.
171. Asseman C, Mauze S, Leach MW, Coffman RL, Powrie F. An essential role for interleukin 10 in the function of regulatory T cells that inhibit intestinal inflammation. J Exp Med. 1999;190(7):995-1004.
172. Maloy KJ, Salaun L, Cahill R, Dougan G, Saunders NJ, Powrie F. CD4+CD25+ T(R) cells suppress innate immune pathology through cytokine-dependent mechanisms. J Exp Med. 2003;197(1):111-9.
173. Madan R, Demircik F, Surianarayanan S, Allen JL, Divanovic S, Trompette A, Yogev N, Gu Y, Khodoun M, Hildeman D, Boespflug N, Fogolin MB, Gröbe L, Greweling M, Finkelman FD, Cardin R, Mohrs M, Müller W, Waisman A, Roers A, Karp CL. Nonredundant roles for B cell-derived IL-10 in immune counter-regulation. J Immunol. 2009;183(4):2312-20.
174. Roers A, Siewe L, Strittmatter E, Deckert M, Schlüter D, Stenzel W, Gruber AD, Krieg T, Rajewsky K, Müller W. T cell-specific inactivation of the interleukin 10 gene in mice results in enhanced T cell responses but normal innate responses to lipopolysaccharide or skin irritation. J Exp Med. 2004;200(10): 1289-97.
175. Rubtsov YP, Rasmussen JP, Chi EY, Fontenot J, Castelli L, Ye X, Treuting P, Siewe L, Roers A, Henderson WR, Müller W, Rudensky AY. Regulatory T cell-derived interleukin-10 limits inflammation at environmental interfaces. Immunity. 2008;28(4):546-58.
176. Murai M, Turovskaya O, Kim G, Madan R, Karp CL, Cheroutre H, Kronenberg M. Interleukin 10 acts on regulatory T cells to maintain expression of the transcription factor Foxp3 and suppressive function in mice with colitis. Nat Immunol. 2009;10(11):1178-84.
177. Chaudhry A, Samstein RM, Treuting P, Liang Y, Pils MC, Heinrich J-M, Jack RS, Wunderlich F T, Brüning JC, Müller W, Rudensky AY. Interleukin-10 signaling in regulatory T cells is required for suppression of Th17 cell-mediated inflammation. Immunity. 2011;34(4):566-78.
178. Huber S, Gagliani N, Esplugues E, O'Connor W, Huber FJ, Chaudhry A, Kamanaka M, Kobayashi Y, Booth CJ, Rudensky AY, Roncarolo MG, Battaglia M, Flavell RA. 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(4):554-65.
179. Kamanaka M, Huber S, Zenewicz LA, Gagliani N, Rathinam C, O'Connor W, Wan YY, Nakae S, Iwakura Y, Hao L, Flavell RA. Memory/effector (CD45RB(lo)) CD4 T cells are controlled directly by IL-10 and cause IL-22-dependent intestinal pathology. J Exp Med. 2011;208(5): 1027-40.
180. Abel S, Lückheide N, Westendorf AM, Geffers R, Roers A, Müller W, Sparwasser T, Matuschewski K, Buer J, Hansen W. Strong impact of CD4+ Foxp3+ regulatory T cells and limited effect of T cell-derived IL-10 on pathogen clearance during Plasmodium yoelii infection. J Immunol. 2012;188(11):5467-77.
181. Kalampokis I, Yoshizaki A, Tedder TF. IL-10-producing regulatory B cells (B10 cells) in autoimmune disease. Arthritis Res Ther. 2013;15 (Suppl 1):S1.
182. Vitale G, Mion F, Pucillo C. Regulatory B cells: evidence, developmental origin and population diversity. Mol Immunol. 2010;48(1-3):1-8.
183. Maseda D, Smith SH, DiLillo DJ, Bryant JM, Candando KM, Weaver CT, Tedder TF. Regulatory B10 cells differentiate into antibody-secreting cells after transient IL-10 production in vivo. J Immunol. 2012;188(3):1036-48.
184. Yanaba K, Bouaziz J-D, Matsushita T, Tsubata T, Tedder TF. The development and function of regulatory B cells expressing IL-10 (B10 cells) requires antigen receptor diversity and TLR signals. J Immunol. 2009;182(12):7459-72.
185. Fillatreau S, Sweenie CH, McGeachy MJ, Gray D, Anderton SM. B cells regulate autoimmunity by provision of IL-10. Nat Immunol. 2002;3(10):944-50.
186. Matsushita T, Yanaba K, Bouaziz J-D, Fujimoto M, Tedder TF. Regulatory B cells inhibit EAE initiation in mice while other B cells promote disease progression. J Clin Invest. 2008;118(10):3420-30.
187. Matsushita T, Horikawa M, Iwata Y, Tedder TF. Regulatory B cells (B10 cells) and regulatory T cells have independent roles in controlling experimental autoimmune encepha-lomyelitis initiation and late-phase immunopathogenesis. J Immunol. 2010;185(4):2240-52.
188. Yoshizaki A, Miyagaki T, DiLillo DJ, Matsushita T, Horikawa M, Kountikov EI, Spolski R, Poe JC, Leonard WJ, Tedder TF. Regulatory B cells control T-cell autoimmunity through IL-21-dependent cognate interactions. Nature. 2012;491(7423):264-8.
189. Mauri C, Gray D, Mushtaq N, Londei M. Prevention of arthritis by interleukin 10-producing B cells. J Exp Med. 2003;197(4): 489-501.
190. Evans JG, Chavez-Rueda KA, Eddaoudi A, Meyer-Bahlburg A, Rawlings DJ, Ehrenstein MR, Mauri C. Novel suppressive function of transitional 2 B cells in experimental arthritis. J Immunol. 2007;178(12):7868-78.
191. Carter NA, Rosser EC, Mauri C. Interleukin-10 produced by B cells is crucial for the suppression of Th17/Th1 responses, induction of T regulatory type 1 cells and reduction of collagen-induced arthritis. Arthritis Res Ther. 2012;14(1):R32.
192. Yang M, Deng J, Liu Y, Ko K-H, Wang X, Jiao Z, Wang S, Hua Z, Sun L, Srivastava G, Lau C-S, Cao X, Lu L. IL-10-producing regulatory B10 cells ameliorate collagen-induced arthritis via suppressing Th17 cell generation. Am J Pathol. 2012;180(6):2375-85.
193. Oakley OR, Garvy BA, Humphreys S, Qureshi MH, Pomeroy C. Increased weight loss with reduced viral replication in interleukin-10 knockout mice infected with murine cytomegalovirus. Clin Exp Immunol. 2008;151(1):155-64.
194. Siewe L, Bollati-Fogolín M, Wickenhauser C, Krieg T, Müller W, Roers A. Interleukin-10 derived from macrophages and/or neutrophils regulates the inflammatory response to LPS but not the response to CpG DNA. Eur J Immunol. 2006;36(12):3248-55.
195. Bosschaerts T, Morias Y, Stijlemans B, Hérin M, Porta C, Sica A, Mantovani A, De Baetselier P, Beschin A. IL-10 limits production of pathogenic TNF by M1 myeloid cells through induction of nuclear NF-κB p50 member in Trypanosoma congolense infection-resistant C57BL/6 mice. Eur J Immunol. 2011;41(11):3270-80.
196. Dudeck A, Dudeck J, Scholten J, Petzold A, Surianarayanan S, Köhler A, Peschke K, Vöhringer D, Waskow C, Krieg T, Müller W, Waisman A, Hartmann K, Gunzer M, Roers A. Mast cells are key promoters of contact allergy that mediate the adjuvant effects of haptens. Immunity. 2011;34(6):973-84.
197. Chan CY, St John AL, Abraham SN. Mast cell interleukin-10 drives localized tolerance in chronic bladder infection. Immunity. 2013;38(2):349-59.
198. Girard-Madoux MJH, Kel JM, Reizis B, Clausen BE. IL-10 controls dendritic cell-induced T-cell reactivation in the skin to limit contact hypersensitivity. J Allergy Clin Immunol. 2012;129(1):143.e1-10-150.e1-10.
199. Mäkelä MJ, Kanehiro A, Borish L, Dakhama A, Loader J, Joetham A, Xing Z, Jordana M, Larsen GL, Gelfand EW. IL-10 is necessary for the expression of airway hyperresponsiveness but not pulmonary inflammation after allergic sensitization. Proc Natl Acad Sci U S A. 2000;97(11):6007-12.
200. Liu X, Alli R, Steeves M, Nguyen P, Vogel P, Geiger TL. The T cell response to IL-10 alters cellular dynamics and paradoxically promotes central nervous system autoimmunity. J Immunol. 2012;189(2):669-78.
201. Yin Z, Bahtiyar G, Zhang N, Liu L, Zhu P, Robert ME, McNiff J, Madaio MP, Craft J. IL-10 regulates murine lupus. J Immunol. 2002;169(4):2148-55.
202. Teichmann LL, Kashgarian M, Weaver CT, Roers A, Müller W, Shlomchik MJ. B cell-derived IL-10 does not regulate spontaneous systemic autoimmunity in MRL.Fas(lpr) mice. J Immunol. 2012;188(2):678-85.
203. Li C, Corraliza I, Langhorne J. A defect in interleukin-10 leads to enhanced malarial disease in Plasmodium chabaudi chabaudi infection in mice. Infect Immun. 1999;67(9):4435-42.
204. Gazzinelli RT, Wysocka M, Hieny S, Scharton-Kersten T, Cheever A, Kühn R, Müller W, Trinchieri G, Sher A. In the absence of endogenous IL-10, mice acutely infected with Toxoplasma gondii succumb to a lethal immune response dependent on CD4+ T cells and accompanied by overproduction of IL-12, IFN-gamma and TNF-alpha. J Immunol. 1996;157(2):798-805.