Induction of interleukin-10 in the T helper type 17 effector population by the G protein coupled estrogen receptor (GPER) agonist G-1

Immunology

Volumn 134, Issue 1, 2011, Pages 93-106

  Brunsing, Ryan L ^a   Prossnitz, Eric R ^a,b  

^a UNIVERSITY OF NEW MEXICO HEALTH SCIENCES CENTER   (United States)

^b UNIVERSITY OF NEW MEXICO   (United States)

Author keywords

Estrogen receptor; G protein coupled estrogen receptor 1; GPR30; Hybrid T cell; Interleukin 10; Regulatory T cells; T helper type 17

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; CHEMOKINE RECEPTOR AGONIST; G PROTEIN COUPLED ESTROGEN RECEPTOR AGONIST G 1; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 17; RETINOID RELATED ORPHAN RECEPTOR GAMMA; T LYMPHOCYTE RECEPTOR; TRANSCRIPTION FACTOR FOXP3; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CD4+ T LYMPHOCYTE; CELL COMPARTMENTALIZATION; CELL POPULATION; CELL PROLIFERATION; CONTROLLED STUDY; CROSS LINKING; CYTOKINE PRODUCTION; CYTOKINE RELEASE; CYTOKINE RESPONSE; EX VIVO STUDY; FLOW CYTOMETRY; HYBRID CELL; IN VIVO STUDY; INTRACELLULAR SIGNALING; LYMPHOCYTE DIFFERENTIATION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SPLEEN CELL; SUPPRESSOR CELL; TH17 CELL;

ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; CELL PROLIFERATION; CYCLOPENTANES; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FORKHEAD TRANSCRIPTION FACTORS; GREEN FLUORESCENT PROTEINS; INTERFERON-GAMMA; INTERLEUKIN-10; INTERLEUKIN-17; INTERLEUKIN-23; INTERLEUKIN-6; LYMPHOCYTE ACTIVATION; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NUCLEAR RECEPTOR SUBFAMILY 1, GROUP F, MEMBER 3; QUINOLINES; RECEPTORS, G-PROTEIN-COUPLED; SIGNAL TRANSDUCTION; SPLEEN; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES; TH17 CELLS; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR-ALPHA;

EID: 79961208152     PISSN: 00192805     EISSN: 13652567     Source Type: Journal    
DOI: 10.1111/j.1365-2567.2011.03471.x     Document Type: Article

References (60)

1. Mosmann TR, Coffman RL. TH1 and TH2 cells: different patterns of lymphokine secretion lead to different functional properties. Annu Rev Immunol 1989; 7:145-73.
2. + effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat Immunol 2005; 6:1123-32.
3. + T helper cells. Cell 2006; 126:1121-33.
4. Wei L, Laurence A, Elias KM, O'Shea JJ. IL-21 is produced by Th17 cells and drives IL-17 production in a STAT3-dependent manner. J Biol Chem 2007; 282:34605-10.
5. Torchinsky MB, Blander JM. T helper 17 cells: discovery, function, and physiological trigger. Cell Mol Life Sci 2010; 67:1407-21.
6. McGeachy MJ, Chen Y, Tato CM et al. The interleukin 23 receptor is essential for the terminal differentiation of interleukin 17-producing effector T helper cells in vivo. Nat Immunol 2009; 10:314-24.
7. Vignali DA, Collison LW, Workman CJ. How regulatory T cells work. Nat Rev 2008; 8:523-32.
8. Patey-Mariaud de Serre N, Canioni D, Ganousse S, Rieux-Laucat F, Goulet O, Ruemmele F, Brousse N. Digestive histopathological presentation of IPEX syndrome. Mod Pathol 2009; 22:95-102.
9. Clark LB, Appleby MW, Brunkow ME, Wilkinson JE, Ziegler SF, Ramsdell F. Cellular and molecular characterization of the scurfy mouse mutant. J Immunol 1999; 162:2546-54.
10. Kuhn R, Lohler J, Rennick D, Rajewsky K, Muller W. Interleukin-10-deficient mice develop chronic enterocolitis. Cell 1993; 75:263-74.
11. Glocker EO, Kotlarz D, Boztug K et al. Inflammatory bowel disease and mutations affecting the interleukin-10 receptor. N Eng J Med 2009; 361:2033-45.
12. Saraiva M, O'Garra A. The regulation of IL-10 production by immune cells. Nat Rev 2010; 10:170-81.
13. 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; 31:209-19.
14. Del Prete G, De Carli M, Almerigogna F, Giudizi MG, Biagiotti R, Romagnani S. 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; 150:353-60.
15. 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; 156:2776-82.
16. - Th1 cells are the major source of host-protective regulatory IL-10 during intracellular protozoan infection. J Exp Med 2007; 204:273-83.
17. 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; 170:2081-95.
18. Fitzgerald DC, Zhang GX, El-Behi M et al. Suppression of autoimmune inflammation of the central nervous system by interleukin 10 secreted by interleukin 27-stimulated T cells. Nat Immunol 2007; 8:1372-9.
19. H-17 cell-mediated pathology. Nat Immunol 2007; 8:1390-7.
20. Stumhofer JS, Silver JS, Laurence A et al. Interleukins 27 and 6 induce STAT3-mediated T cell production of interleukin 10. Nat Immunol 2007; 8:1363-71.
21. Maynard CL, Weaver CT. Diversity in the contribution of interleukin-10 to T-cell-mediated immune regulation. Immunol Rev 2008; 226:219-33.
22. Battaglia M, Gregori S, Bacchetta R, Roncarolo MG. Tr1 cells: from discovery to their clinical application. Semin Immunol 2006; 18:120-7.
23. Roncarolo MG, Gregori S, Battaglia M, Bacchetta R, Fleischhauer K, Levings MK. Interleukin-10-secreting type 1 regulatory T cells in rodents and humans. Immunol Rev 2006; 212:28-50.
24. - precursor cells in the absence of interleukin 10. Nat Immunol 2007; 8:931-41.
25. 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.
26. Bettelli E, Carrier Y, Gao W, Korn T, Strom TB, Oukka M, Weiner HL, Kuchroo VK. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 2006; 441:235-8.
27. Bluestone JA, Mackay CR, O'Shea JJ, Stockinger B. The functional plasticity of T cell subsets. Nat Rev 2009; 9:811-6.
28. Lee YK, Mukasa R, Hatton RD, Weaver CT. Developmental plasticity of Th17 and Treg cells. Curr Opin Immunol 2009; 21:274-80.
29. Barnes MJ, Powrie F. Hybrid Treg cells: steel frames and plastic exteriors. Nat Immunol 2009; 10:563-4.
30. H17 cell differentiation. Nature 2008; 455:808-12.
31. Liao JJ, Huang MC, Goetzl EJ. Cutting edge: alternative signaling of Th17 cell development by sphingosine 1-phosphate. J Immunol 2007; 178:5425-8.
32. 3 modulates Th17 polarization and interleukin-22 expression by memory T cells from patients with early rheumatoid arthritis. Arthritis Rheum 2010; 62:132-42.
33. + Tregs to TH17-like cells in tumor-draining lymph nodes. Blood 2009; 113:6102-11.
34. Mucida D, Park Y, Kim G, Turovskaya O, Scott I, Kronenberg M, Cheroutre H. Reciprocal TH17 and regulatory T cell differentiation mediated by retinoic acid. Science 2007; 317:256-60.
35. Polanczyk MJ, Hopke C, Huan J, Vandenbark AA, Offner H. Enhanced FoxP3 expression and Treg cell function in pregnant and estrogen-treated mice. J Neuroimmunol 2005; 170:85-92.
36. Yates MA, Li Y, Chlebeck PJ, Offner H. GPR30, but not estrogen receptor-alpha, is crucial in the treatment of experimental autoimmune encephalomyelitis by oral ethinyl estradiol. BMC Immunol 2010; 11:20.
37. Confavreux C, Hutchinson M, Hours MM, Cortinovis-Tourniaire P, Moreau T. Rate of pregnancy-related relapse in multiple sclerosis. Pregnancy in Multiple Sclerosis Group. N Eng J Med 1998; 339:285-91.
38. Wang C, Dehghani B, Li Y, Kaler LJ, Proctor T, Vandenbark AA, Offner H. Membrane estrogen receptor regulates experimental autoimmune encephalomyelitis through up-regulation of programmed death 1. J Immunol 2009; 182:3294-303.
39. Blasko E, Haskell CA, Leung S et al. Beneficial role of the GPR30 agonist G-1 in an animal model of multiple sclerosis. J Neuroimmunol 2009; 214:67-77.
40. Dennis MK, Burai R, Ramesh C et al. In vivo effects of a GPR30 antagonist. Nat Chem Biol 2009; 5:421-7.
41. Haribhai D, Lin W, Relland LM, Truong N, Williams CB, Chatila TA. Regulatory T cells dynamically control the primary immune response to foreign antigen. J Immunol 2007; 178:2961-72.
42. Filardo EJ, Quinn JA, Bland KI, Frackelton AR Jr. Estrogen-induced activation of Erk-1 and Erk-2 requires the G protein-coupled receptor homolog, GPR30, and occurs via trans-activation of the epidermal growth factor receptor through release of HB-EGF. Mol Endocrinol 2000; 14:1649-60.
43. Ait-Oufella H, Herbin O, Bouaziz JD et al. B cell depletion reduces the development of atherosclerosis in mice. J Exp Med 2010; 207:1579-87.
44. Taleb S, Romain M, Ramkhelawon B et al. Loss of SOCS3 expression in T cells reveals a regulatory role for interleukin-17 in atherosclerosis. J Exp Med 2009; 206:2067-77.
45. Taleb S, Tedgui A, Mallat Z. Interleukin-17: friend or foe in atherosclerosis? Curr Opin Lipidol 2010; 21:404-8.
46. O'Connor W Jr, Kamanaka M, Booth CJ, Town T, Nakae S, Iwakura Y, Kolls JK, Flavell RA. A protective function for interleukin 17A in T cell-mediated intestinal inflammation. Nat Immunol 2009; 10:603-9.
47. Cua DJ, Sherlock J, Chen Y et al. Interleukin-23 rather than interleukin-12 is the critical cytokine for autoimmune inflammation of the brain. Nature 2003; 421:744-8.
48. Langrish CL, Chen Y, Blumenschein WM et al. IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J Exp Med 2005; 201:233-40.
49. Hofstetter HH, Ibrahim SM, Koczan D, Kruse N, Weishaupt A, Toyka KV, Gold R. Therapeutic efficacy of IL-17 neutralization in murine experimental autoimmune encephalomyelitis. Cell Immunol 2005; 237:123-30.
50. Muranski P, Boni A, Antony PA et al. Tumor-specific Th17-polarized cells eradicate large established melanoma. Blood 2008; 112:362-73.
51. + regulatory T cells implicates compensatory pathways including regulatory B cells. Immunology 2011; 132:340-7.
52. Polanczyk MJ, Hopke C, Vandenbark AA, Offner H. Treg suppressive activity involves estrogen-dependent expression of programmed death-1 (PD-1). Int Immunol 2007; 19:337-43.
53. Bologa CG, Revankar CM, Young SM et al. Virtual and biomolecular screening converge on a selective agonist for GPR30. Nat Chem Biol 2006; 2:207-12.
54. Prossnitz ER, Arterburn JB, Smith HO, Oprea TI, Sklar LA, Hathaway HJ. Estrogen signaling through the transmembrane G protein-coupled receptor GPR30. Annu Rev Physiol 2008; 70:165-90.
55. Wang C, Dehghani B, Magrisso IJ et al. GPR30 contributes to estrogen-induced thymic atrophy. Mol Endocrinol 2008; 22:636-48.
56. Das J, Ren G, Zhang L et al. Transforming growth factor beta is dispensable for the molecular orchestration of Th17 cell differentiation. J Exp Med 2009; 206:2407-16.
57. H17 cell differentiation by antagonizing RORγt function. Nature 2008; 453:236-40.
58. Beriou G, Costantino CM, Ashley CW, Yang L, Kuchroo VK, Baecher-Allan C, Hafler DA. IL-17-producing human peripheral regulatory T cells retain suppressive function. Blood 2009; 113:4240-9.
59. Koch MA, Tucker-Heard G, Perdue NR, Killebrew JR, Urdahl KB, Campbell DJ. The transcription factor T-bet controls regulatory T cell homeostasis and function during type 1 inflammation. Nat Immunol 2009; 10:595-602.
60. Spolski R, Kim HP, Zhu W, Levy DE, Leonard WJ. IL-21 mediates suppressive effects via its induction of IL-10. J Immunol 2009; 182:2859-67.