Regulation of interleukin-10 and interleukin-22 expression in T helper cells

Current Opinion in Immunology

Volumn 23, Issue 5, 2011, Pages 605-612

  Rutz, Sascha ^a   Ouyang, Wenjun ^a  

^a GENENTECH INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 10; INTERLEUKIN 22; INTERLEUKIN 27; NOTCH RECEPTOR; TRANSFORMING GROWTH FACTOR BETA;

EPITHELIUM; HELPER CELL; HUMAN; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; IMMUNOREGULATION; INFLAMMATION; INNATE IMMUNITY; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; WOUND HEALING;

ANIMALS; CELL DIFFERENTIATION; GENE EXPRESSION REGULATION; HUMANS; IMMUNITY, INNATE; INFLAMMATION; INTERFERON-GAMMA; INTERLEUKIN-10; INTERLEUKIN-2; INTERLEUKINS; LYMPHOCYTE ACTIVATION; MICE; ORGAN SPECIFICITY; RECEPTORS, NOTCH; STAT TRANSCRIPTION FACTORS; TH1 CELLS; TH17 CELLS; TH2 CELLS; WOUND HEALING;

EID: 80053614883     PISSN: 09527915     EISSN: 18790372     Source Type: Journal    
DOI: 10.1016/j.coi.2011.07.018     Document Type: Review

References (59)

1. Ouyang W., Rutz S., Crellin N.K., Valdez P.A., Hymowitz S.G. Regulation and functions of IL-10 family cytokines in inflammation and diseases. Annu Rev Immunol 2010.
2. Saraiva M., O'Garra A. The regulation of IL-10 production by immune cells. Nat Rev Immunol 2010.
3. Ouyang W. Distinct roles of IL-22 in human psoriasis and inflammatory bowel disease. Cytokine Growth Factor Rev 2010, 21(6):435-441.
4. Sonnenberg G.F., Fouser L.A., Artis D. Border patrol: regulation of immunity, inflammation and tissue homeostasis at barrier surfaces by IL-22. Nat Immunol 2011, 12(5):383-390.
5. Vivier E., Spits H., Cupedo T. Interleukin-22-producing innate immune cells: new players in mucosal immunity and tissue repair?. Nat Rev Immunol 2009, 9(4):229-234.
6. Zhu J., Yamane H., Paul W.E. Differentiation of effector CD4 T cell populations. Annu Rev Immunol 2010.
7. Roncarolo M.G., Gregori S., Battaglia M., Bacchetta R., Fleischhauer K., Levings M.K. Interleukin-10-secreting type 1 regulatory T cells in rodents and humans. Immunol Rev 2006, 212:28-50.
8. Maynard C.L., Harrington L.E., Janowski K.M., Oliver J.R., Zindl C.L., Rudensky A.Y., 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):931-941.
9. Gerosa F., Nisii C., Righetti S., Micciolo R., Marchesini M., Cazzadori A., Trinchieri G. 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.
10. Jankovic D., Kullberg M., Feng C., Goldszmid R., Collazo C., Wilson M., Wynn T., Kamanaka M., Flavell R., 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):273-283.
11. Volpe E., Touzot M., Servant N., Marloie-Provost M.-A., Hupé P., Barillot E., Soumelis V. Multiparametric analysis of cytokine-driven human Th17 differentiation reveals a differential regulation of IL-17 and IL-22 production. Blood 2009, 114(17):3610-3614.
12. Fiorentino D.F., Bond M.W., Mosmann T.R. 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.
13. Zheng Y., Danilenko D., Valdez P., Kasman I., Eastham-Anderson J., Wu J., Ouyang W. Interleukin-22, a T(h)17 cytokine, mediates IL-23-induced dermal inflammation and acanthosis. Nature 2007, 445(7128):648-651.
14. Liang S.C., Tan X.-Y., Luxenberg D.P., Karim R., Dunussi-Joannopoulos K., Collins M., Fouser L.A. Interleukin (IL)-22 and IL-17 are coexpressed by Th17 cells and cooperatively enhance expression of antimicrobial peptides. J Exp Med 2006, 203(10):2271-2279.
15. Veldhoen M., Hocking R.J., Atkins C.J., Locksley R.M., Stockinger B. Tgfbeta in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells. Immunity 2006, 24(2):179-189.
16. Bettelli E., Carrier Y., Gao W., Korn T., Strom T.B., Oukka M., Weiner H.L., Kuchroo V.K. Reciprocal developmental pathways for the generation of pathogenic effector Th17 and regulatory T cells. Nature 2006, 441(7090):235-238.
17. Mangan P.R., Harrington L.E., O'Quinn D.B., Helms W.S., Bullard D.C., Elson C.O., Hatton R.D., Wahl S.M., Schoeb T.R., Weaver C.T. Transforming growth factor-beta induces development of the T(h)17 lineage. Nature 2006, 441(7090):231-234.
18. Duhen T., Geiger R., Jarrossay D., Lanzavecchia A., Sallusto F. Production of interleukin 22 but not interleukin 17 by a subset of human skin-homing memory T cells. Nat Immunol 2009.
19. Xu J., Yang Y., Qiu G., Lal G., Wu Z., Levy D.E., Ochando J.C., Bromberg J.S., Ding Y. c-Maf regulates IL-10 expression during th17 polarization. J Immunol 2009, 182(10):6226-6236.
20. Ghoreschi K., Laurence A., Yang X.-P., Tato C.M., McGeachy M.J., Konkel J.E., Ramos H.L., Wei L., Davidson T.S., Bouladoux N., et al. Generation of pathogenic T(h)17 cells in the absence of TGF-β signalling. Nature 2010, 467(7318):967-971.
21. Veldhoen M., Uyttenhove C., van Snick J., Helmby H., Westendorf A., Buer J., Martin B., Wilhelm C., Stockinger B. Transforming growth factor-beta 'reprograms' the differentiation of T helper 2 cells and promotes an interleukin 9-producing subset. Nat Immunol 2008, 9(12):1341-1346.
22. Dardalhon V., Awasthi A., Kwon H., Galileos G., Gao W., Sobel R.A., Mitsdoerffer M., Strom T.B., Elyaman W., Ho I.-C., et al. IL-4 inhibits TGF-beta-induced foxp3+ T cells and, together with TGF-beta, generates IL-9+ IL-10+ foxp3(-) effector T cells. Nat Immunol 2008, 9(12):1347-1355.
23. Trifari S., Kaplan C., Tran E., Crellin N., Spits H. Identification of a human helper T cell population that has abundant production of interleukin 22 and is distinct from T(h)-17, T(h)1 and T(h)2 cells. Nat Immunol 2009.
24. Eyerich S., Eyerich K., Pennino D., Carbone T., Nasorri F., Pallotta S., Cianfarani F., Odorisio T., Traidl-Hoffmann C., Behrendt H., et al. Th22 cells represent a distinct human T cell subset involved in epidermal immunity and remodeling. J Clin Invest 2009, 119(12):3573-3585.
25. Saraiva M., Christensen J., Veldhoen M., Murphy T., Murphy K., 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.
26. 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):3484-3492.
27. Pot C., Jin H., Awasthi A., Liu S.M., Lai C.-Y., Madan R., Sharpe A.H., Karp C.L., Miaw S.-C., Ho I.-C., Kuchroo V.K. 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.
28. Apetoh L., Quintana F.J., Pot C., Joller N., Xiao S., Kumar D., Burns E.J., Sherr D.H., Weiner H.L., Kuchroo V.K. 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.
29. Yang Y., Ochando J., Yopp A., Bromberg J.S., Ding Y. IL-6 plays a unique role in initiating c-Maf expression during early stage of CD4 T cell activation. J Immunol 2005, 174(5):2720-2729.
30. Nurieva R., Yang X.O., Martinez G., Zhang Y., Panopoulos A.D., Ma L., Schluns K., Tian Q., Watowich S.S., Jetten A.M., Dong C. Essential autocrine regulation by IL-21 in the generation of inflammatory T cells. Nature 2007, 448(7152):480-483.
31. Yang X.O., Panopoulos A.D., Nurieva R., Chang S.H., Wang D., Watowich S.S., Dong C. Stat3 regulates cytokine-mediated generation of inflammatory helper T cells. J Biol Chem 2007, 282(13):9358-9363.
32. Yang X.O., Pappu B.P., Nurieva R., Akimzhanov A., Kang H.S., Chung Y., Ma L., Shah B., Panopoulos A.D., Schluns K.S., et al. T helper 17 lineage differentiation is programmed by orphan nuclear receptors ror alpha and ror gamma. Immunity 2008, 28(1):29-39.
33. Schraml B., Hildner K., Ise W., Lee W., Smith W., Solomon B., Sahota G., Sim J., Mukasa R., Cemerski S., et al. The ap-1 transcription factor batf controls T(h)17 differentiation. Nature 2009.
34. Veldhoen M., Hirota K., Westendorf A.M., Buer J., Dumoutier L., Renauld J.-C., Stockinger B. The aryl hydrocarbon receptor links th17-cell-mediated autoimmunity to environmental toxins. Nature 2008, 453(7191):106-109.
35. Manel N., Unutmaz D., Littman D.R. The differentiation of human T(h)-17 cells requires transforming growth factor-beta and induction of the nuclear receptor rorgammat. Nat Immunol 2008, 9(6):641-649.
36. Veldhoen M., Hirota K., Christensen J., O'Garra A., Stockinger B. Natural agonists for aryl hydrocarbon receptor in culture medium are essential for optimal differentiation of th17 T cells. J Exp Med 2009, 206(1):43-49.
37. Stumhofer J., Silver J., Laurence A., Porrett P., Harris T., Turka L., Ernst M., Saris C., O'Shea J., Hunter C. Interleukins 27 and 6 induce stat3-mediated T cell production of interleukin 10. Nat Immunol 2007, 8(12):1363-1371.
38. Rutz S., Janke M., Kassner N., Hohnstein T., Krueger M., Scheffold A. Notch regulates IL-10 production by T helper 1 cells. Proc Natl Acad Sci U S A 2008, 105(9):3497-3502.
39. Kassner N., Krueger M., Yagita H., Dzionek A., Hutloff A., Kroczek R., Scheffold A., Rutz S. Cutting edge: plasmacytoid dendritic cells induce IL-10 production in T cells via the delta-like-4/notch axis. J Immunol 2010, 184(2):550-554.
40. Alam M.S., Maekawa Y., Kitamura A., Tanigaki K., Yoshimoto T., Kishihara K., Yasutomo K. Notch signaling drives IL-22 secretion in CD4+ T cells by stimulating the aryl hydrocarbon receptor. Proc Natl Acad Sci U S A 2010, 107(13):5943-5948.
41. Gandhi R., Kumar D., Burns E.J., Nadeau M., Dake B., Laroni A., Kozoriz D., Weiner H.L., Quintana F.J. Activation of the aryl hydrocarbon receptor induces human type 1 regulatory T cell-like and foxp3(+) regulatory T cells. Nat Immunol 2010.
42. McGeachy M., Bak-Jensen K., Chen Y., Tato C., Blumenschein W., McClanahan T., Cua D. 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.
43. Paulos C.M., Carpenito C., Plesa G., Suhoski M.M., Varela-Rohena A., Golovina T.N., Carroll R.G., Riley J.L., June C.H. The inducible costimulator (icos) is critical for the development of human th17 cells. Sci Transl Med 2010, 2(55):55ra78.
44. Liu H., Rohowsky-Kochan C. Interleukin-27-mediated suppression of human th17 cells is associated with activation of stat1 and suppressor of cytokine signaling protein 1. J Interferon Cytokine Res: Off J Int Soc Interferon Cytokine Res 2011.
45. Fitzgerald D., Zhang G., El-Behi M., Fonseca-Kelly Z., Li H., Yu S., Saris C., Gran B., Ciric B., Rostami A. 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.
46. Batten M., Kljavin N.M., Li J., Walter M.J., de Sauvage F.J., Ghilardi N. Cutting edge: IL-27 is a potent inducer of IL-10 but not foxp3 in murine T cells. J Immunol 2008, 180(5):2752-2756.
47. Gerosa F., Paganin C., Peritt D., Paiola F., Scupoli M., ste-Amezaga M., Frank I., Trinchieri G. Interleukin-12 primes human CD4 and CD8 T cell clones for high production of both interferon-gamma and interleukin-10. J Exp Med 1996, 183(6):2559-2569.
48. Chang H., 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):807-817.
49. 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):3470-3479.
50. Stockinger B., Hirota K., Duarte J., Veldhoen M. External influences on the immune system via activation of the aryl hydrocarbon receptor. Semin Immunol 2011.
51. Quintana F.J., Basso A.S., Iglesias A.H., Korn T., Farez M.F., Bettelli E., Caccamo M., Oukka M., Weiner H.L. Control of T(reg) and T(h)17 cell differentiation by the aryl hydrocarbon receptor. Nature 2008, 453(7191):65-71.
52. Kimura A., Naka T., Nohara K., Fujii-Kuriyama Y., Kishimoto T. Aryl hydrocarbon receptor regulates stat1 activation and participates in the development of th17 cells. Proc Natl Acad Sci U S A 2008, 105(28):9721-9726.
53. Martin B., Hirota K., Cua D.J., Stockinger B., Veldhoen M. Interleukin-17-producing gammadelta T cells selectively expand in response to pathogen products and environmental signals. Immunity 2009, 31(2):321-330.
54. Osborne B., Minter L. Notch signalling during peripheral T-cell activation and differentiation. Nat Rev Immunol 2007, 7(1):64-75.
55. Ito T., Yang M., Wang Y., Lande R., Gregorio J., Perng O., Qin X., Liu Y., Gilliet M. Plasmacytoid dendritic cells prime IL-10-producing T regulatory cells by inducible costimulator ligand. J Exp Med 2007, 204(1):105-115.
56. Mukherjee S., Schaller M.A., Neupane R., Kunkel S.L., Lukacs N.W. Regulation of T cell activation by notch ligand, dll4, promotes IL-17 production and rorc activation. J Immunol 2009, 182(12):7381-7388.
57. Kamakura S., Oishi K., Yoshimatsu T., Nakafuku M., Masuyama N., Gotoh Y. Hes binding to stat3 mediates crosstalk between notch and jak-stat signalling. Nat Cell Biol 2004, 6(6):547-554.
58. Awasthi A., Carrier Y., Peron J., Bettelli E., Kamanaka M., Flavell R., Kuchroo V., Oukka M., Weiner H. A dominant function for interleukin 27 in generating interleukin 10-producing anti-inflammatory T cells. Nat Immunol 2007, 8(12):1380-1389.
59. Bauquet A.T., Jin H., Paterson A.M., Mitsdoerffer M., Ho I.-C., Sharpe A.H., Kuchroo V.K. The costimulatory molecule icos regulates the expression of c-Maf and IL-21 in the development of follicular T helper cells and Th-17 cells. Nat Immunol 2009, 10(2):167-175.