The Orphan Nuclear Receptor RORγt Directs the Differentiation Program of Proinflammatory IL-17+ T Helper Cells

Cell

Volumn 126, Issue 6, 2006, Pages 1121-1133

  Ivanov, Ivaylo I ^a   McKenzie, Brent S ^b   Zhou, Liang ^a   Tadokoro, Carlos E ^a   Lepelley, Alice ^a   Lafaille, Juan J ^a   Cua, Daniel J ^b   Littman, Dan R ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MERCK RESEARCH LABORATORIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 17; INTERLEUKIN 6; ORPHAN NUCLEAR RECEPTOR ROR GAMMA T; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; AUTOIMMUNE DISEASE; CD4+ T LYMPHOCYTE; CELL DIFFERENTIATION; CELL LINEAGE; EFFECTOR CELL; GENETIC TRANSCRIPTION; HELPER CELL; HOMEOSTASIS; INFLAMMATORY DISEASE; LAMINA PROPRIA; MOUSE; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE;

ANIMALS; ANTIGENS, CD4; AUTOIMMUNE DISEASES; CELL DIFFERENTIATION; DISEASE MODELS, ANIMAL; HEMATOPOIETIC STEM CELLS; HOMEOSTASIS; INTERLEUKIN-17; INTERLEUKIN-6; INTESTINAL MUCOSA; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; PROTEIN ISOFORMS; RECEPTORS, RETINOIC ACID; RECEPTORS, THYROID HORMONE; T-LYMPHOCYTES, HELPER-INDUCER;

EID: 33748588423     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2006.07.035     Document Type: Article

References (58)

1. Abbas A.K., Murphy K.M., and Sher A. Functional diversity of helper T lymphocytes. Nature 383 (1996) 787-793
2. Aggarwal S., Ghilardi N., Xie M.H., de Sauvage F.J., and Gurney A.L. Interleukin-23 promotes a distinct CD4 T cell activation state characterized by the production of interleukin-17. J. Biol. Chem. 278 (2003) 1910-1914
3. Barczyk A., Pierzchala W., and Sozanska E. Interleukin-17 in sputum correlates with airway hyperresponsiveness to methacholine. Respir. Med. 97 (2003) 726-733
4. Bettelli E., Carrier Y., Gao W., Korn T., Strom T.B., Oukka M., Weiner H.L., and Kuchroo V.K. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 441 (2006) 235-238
5. Chen W., Jin W., Hardegen N., Lei K.J., Li L., Marinos N., McGrady G., and Wahl S.M. Conversion of peripheral CD4+CD25- naive T cells to CD4+CD25+ regulatory T cells by TGF-beta induction of transcription factor Foxp3. J. Exp. Med. 198 (2003) 1875-1886
6. Chen Y., Langrish C.L., McKenzie B., Joyce-Shaikh B., Stumhofer J.S., McClanahan T., Blumenschein W., Churakovsa T., Low J., Presta L., et al. Anti-IL-23 therapy inhibits multiple inflammatory pathways and ameliorates autoimmune encephalomyelitis. J. Clin. Invest. 116 (2006) 1317-1326
7. Christen U., and von Herrath M.G. Manipulating the type 1 vs type 2 balance in type 1 diabetes. Immunol. Res. 30 (2004) 309-325
8. Cua D.J., Sherlock J., Chen Y., Murphy C.A., Joyce B., Seymour B., Lucian L., To W., Kwan S., Churakova T., et al. Interleukin-23 rather than interleukin-12 is the critical cytokine for autoimmune inflammation of the brain. Nature 421 (2003) 744-748
9. Dong C. Diversification of T-helper-cell lineages: finding the family root of IL-17-producing cells. Nat. Rev. Immunol. 6 (2006) 329-333
10. Eberl G., and Littman D.R. The role of the nuclear hormone receptor RORgammat in the development of lymph nodes and Peyer's patches. Immunol. Rev. 195 (2003) 81-90
11. Eberl G., and Littman D.R. Thymic origin of intestinal alphabeta T cells revealed by fate mapping of RORgammat+ cells. Science 305 (2004) 248-251
12. Eberl G., Marmon S., Sunshine M.J., Rennert P.D., Choi Y., and Littman D.R. An essential function for the nuclear receptor RORgamma(t) in the generation of fetal lymphoid tissue inducer cells. Nat. Immunol. 5 (2004) 64-73
13. Eugster H.P., Frei K., Kopf M., Lassmann H., and Fontana A. IL-6-deficient mice resist myelin oligodendrocyte glycoprotein-induced autoimmune encephalomyelitis. Eur. J. Immunol. 28 (1998) 2178-2187
14. Fantini M.C., Becker C., Monteleone G., Pallone F., Galle P.R., and Neurath M.F. Cutting edge: TGF-beta induces a regulatory phenotype in CD4+CD25- T cells through Foxp3 induction and down-regulation of Smad7. J. Immunol. 172 (2004) 5149-5153
15. Fujino S., Andoh A., Bamba S., Ogawa A., Hata K., Araki Y., Bamba T., and Fujiyama Y. Increased expression of interleukin 17 in inflammatory bowel disease. Gut 52 (2003) 65-70
16. Gately M.K., Renzetti L.M., Magram J., Stern A.S., Adorini L., Gubler U., and Presky D.H. The interleukin-12/interleukin-12-receptor system: role in normal and pathologic immune responses. Annu. Rev. Immunol. 16 (1998) 495-521
17. Glimcher L.H., and Murphy K.M. Lineage commitment in the immune system: the T helper lymphocyte grows up. Genes Dev. 14 (2000) 1693-1711
18. Hamada H., Hiroi T., Nishiyama Y., Takahashi H., Masunaga Y., Hachimura S., Kaminogawa S., Takahashi-Iwanaga H., Iwanaga T., Kiyono H., et al. Identification of multiple isolated lymphoid follicles on the antimesenteric wall of the mouse small intestine. J. Immunol. 168 (2002) 57-64
19. Happel K.I., Dubin P.J., Zheng M., Ghilardi N., Lockhart C., Quinton L.J., Odden A.R., Shellito J.E., Bagby G.J., Nelson S., and Kolls J.K. Divergent roles of IL-23 and IL-12 in host defense against Klebsiella pneumoniae. J. Exp. Med. 202 (2005) 761-769
20. Harrington L.E., Hatton R.D., Mangan P.R., Turner H., Murphy T.L., Murphy K.M., and Weaver C.T. Interleukin 17-producing CD4+ effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat. Immunol. 6 (2005) 1123-1132
21. Infante-Duarte C., Horton H.F., Byrne M.C., and Kamradt T. Microbial lipopeptides induce the production of IL-17 in Th cells. J. Immunol. 165 (2000) 6107-6115
22. Ivanov I.I., Diehl G.E., and Littman D.R. Lymphoid tissue inducer cells in intestinal immunity. Curr. Top. Microbiol. Immunol. 308 (2006) 59-82
23. Iwakura Y., and Ishigame H. The IL-23/IL-17 axis in inflammation. J. Clin. Invest. 116 (2006) 1218-1222
24. Jetten A.M. Recent advances in the mechanisms of action and physiological functions of the retinoid-related orphan receptors (RORs). Curr. Drug Targets Inflamm. Allergy 3 (2004) 395-412
25. Jetten A.M., Kurebayashi S., and Ueda E. The ROR nuclear orphan receptor subfamily: critical regulators of multiple biological processes. Prog. Nucleic Acid Res. Mol. Biol. 69 (2001) 205-247
26. Kanamori Y., Ishimaru K., Nanno M., Maki K., Ikuta K., Nariuchi H., and Ishikawa H. Identification of novel lymphoid tissues in murine intestinal mucosa where clusters of c-kit+ IL-7R+ Thy1+ lympho-hemopoietic progenitors develop. J. Exp. Med. 184 (1996) 1449-1459
27. Kinugasa T., Sakaguchi T., Gu X., and Reinecker H.C. Claudins regulate the intestinal barrier in response to immune mediators. Gastroenterology 118 (2000) 1001-1011
28. Kolls J.K., and Linden A. Interleukin-17 family members and inflammation. Immunity 21 (2004) 467-476
29. Kopf M., Baumann H., Freer G., Freudenberg M., Lamers M., Kishimoto T., Zinkernagel R., Bluethmann H., and Kohler G. Impaired immune and acute-phase responses in interleukin-6-deficient mice. Nature 368 (1994) 339-342
30. Langowski J.L., Zhang X., Wu L., Mattson J.D., Chen T., Smith K., Basham B., McClanahan T., Kastelein R.A., and Oft M. IL-23 promotes tumour incidence and growth. Nature 442 (2006) 461-465
31. Langrish C.L., Chen Y., Blumenschein W.M., Mattson J., Basham B., Sedgwick J.D., McClanahan T., Kastelein R.A., and Cua D.J. IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J. Exp. Med. 201 (2005) 233-240
32. Lock C., Hermans G., Pedotti R., Brendolan A., Schadt E., Garren H., Langer-Gould A., Strober S., Cannella B., Allard J., et al. Gene-microarray analysis of multiple sclerosis lesions yields new targets validated in autoimmune encephalomyelitis. Nat. Med. 8 (2002) 500-508
33. Lorenz R.G., Chaplin D.D., McDonald K.G., McDonough J.S., and Newberry R.D. Isolated lymphoid follicle formation is inducible and dependent upon lymphotoxin-sufficient B lymphocytes, lymphotoxin beta receptor, and TNF receptor I function. J. Immunol. 170 (2003) 5475-5482
34. 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., and Weaver C.T. Transforming growth factor-beta induces development of the T(H)17 lineage. Nature 441 (2006) 231-234
35. McKenzie B.S., Kastelein R.A., and Cua D.J. Understanding the IL-23-IL-17 immune pathway. Trends Immunol. 27 (2006) 17-23
36. Mowat A.M. Anatomical basis of tolerance and immunity to intestinal antigens. Nat. Rev. Immunol. 3 (2003) 331-341
37. Murphy C.A., Langrish C.L., Chen Y., Blumenschein W., McClanahan T., Kastelein R.A., Sedgwick J.D., and Cua D.J. Divergent pro- and antiinflammatory roles for IL-23 and IL-12 in joint autoimmune inflammation. J. Exp. Med. 198 (2003) 1951-1957
38. Nakae S., Nambu A., Sudo K., and Iwakura Y. Suppression of immune induction of collagen-induced arthritis in IL-17-deficient mice. J. Immunol. 171 (2003) 6173-6177
39. Newberry R.D., and Lorenz R.G. Organizing a mucosal defense. Immunol. Rev. 206 (2005) 6-21
40. Niess J.H., Brand S., Gu X., Landsman L., Jung S., McCormick B.A., Vyas J.M., Boes M., Ploegh H.L., Fox J.G., et al. CX3CR1-mediated dendritic cell access to the intestinal lumen and bacterial clearance. Science 307 (2005) 254-258
41. Ogawa A., Andoh A., Araki Y., Bamba T., and Fujiyama Y. Neutralization of interleukin-17 aggravates dextran sulfate sodium-induced colitis in mice. Clin. Immunol. 110 (2004) 55-62
42. Oppmann B., Lesley R., Blom B., Timans J.C., Xu Y., Hunte B., Vega F., Yu N., Wang J., Singh K., et al. Novel p19 protein engages IL-12p40 to form a cytokine, IL-23, with biological activities similar as well as distinct from IL-12. Immunity 13 (2000) 715-725
43. Pabst O., Herbrand H., Worbs T., Friedrichsen M., Yan S., Hoffmann M.W., Korner H., Bernhardt G., Pabst R., and Forster R. Cryptopatches and isolated lymphoid follicles: dynamic lymphoid tissues dispensable for the generation of intraepithelial lymphocytes. Eur. J. Immunol. 35 (2005) 98-107
44. Park H., Li Z., Yang X.O., Chang S.H., Nurieva R., Wang Y.H., Wang Y., Hood L., Zhu Z., Tian Q., and Dong C. A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat. Immunol. 6 (2005) 1133-1141
45. Rakoff-Nahoum S., Paglino J., Eslami-Varzaneh F., Edberg S., and Medzhitov R. Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell 118 (2004) 229-241
46. Rescigno M., Urbano M., Valzasina B., Francolini M., Rotta G., Bonasio R., Granucci F., Kraehenbuhl J.P., and Ricciardi-Castagnoli P. Dendritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria. Nat. Immunol. 2 (2001) 361-367
47. Seder R.A., and Paul W.E. Acquisition of lymphokine-producing phenotype by CD4+ T cells. Annu. Rev. Immunol. 12 (1994) 635-673
48. Stamp L.K., James M.J., and Cleland L.G. Interleukin-17: the missing link between T-cell accumulation and effector cell actions in rheumatoid arthritis?. Immunol. Cell Biol. 82 (2004) 1-9
49. Stark M.A., Huo Y., Burcin T.L., Morris M.A., Olson T.S., and Ley K. Phagocytosis of apoptotic neutrophils regulates granulopoiesis via IL-23 and IL-17. Immunity 22 (2005) 285-294
50. Sun Z., Unutmaz D., Zou Y.R., Sunshine M.J., Pierani A., Brenner-Morton S., Mebius R.E., and Littman D.R. Requirement for RORgamma in thymocyte survival and lymphoid organ development. Science 288 (2000) 2369-2373
51. Szabo S.J., Kim S.T., Costa G.L., Zhang X., Fathman C.G., and Glimcher L.H. A novel transcription factor, T-bet, directs Th1 lineage commitment. Cell 100 (2000) 655-669
52. Taylor R.T., and Williams I.R. Lymphoid organogenesis in the intestine. Immunol. Res. 33 (2005) 167-181
53. Trembleau S., Germann T., Gately M.K., and Adorini L. The role of IL-12 in the induction of organ-specific autoimmune diseases. Immunol. Today 16 (1995) 383-386
54. Veldhoen M., Hocking R.J., Atkins C.J., Locksley R.M., and Stockinger B. TGFbeta in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells. Immunity 24 (2006) 179-189
55. Witowski J., Ksiazek K., and Jorres A. Interleukin-17: a mediator of inflammatory responses. Cell. Mol. Life Sci. 61 (2004) 567-579
56. Ye P., Rodriguez F.H., Kanaly S., Stocking K.L., Schurr J., Schwarzenberger P., Oliver P., Huang W., Zhang P., Zhang J., et al. Requirement of interleukin 17 receptor signaling for lung CXC chemokine and granulocyte colony-stimulating factor expression, neutrophil recruitment, and host defense. J. Exp. Med. 194 (2001) 519-527
57. Yen D., Cheung J., Scheerens H., Poulet F., McClanahan T., McKenzie B., Kleinschek M.A., Owyang A., Mattson J., Blumenschein W., et al. IL-23 is essential for T cell-mediated colitis and promotes inflammation via IL-17 and IL-6. J. Clin. Invest. 116 (2006) 1310-1316
58. Zheng W., and Flavell R.A. The transcription factor GATA-3 is necessary and sufficient for Th2 cytokine gene expression in CD4 T cells. Cell 89 (1997) 587-596