Late Developmental Plasticity in the T Helper 17 Lineage

Immunity

Volumn 30, Issue 1, 2009, Pages 92-107

  Lee, Yun Kyung ^a,b   Turner, Henrietta ^a   Maynard, Craig L ^a   Oliver, James R ^a   Chen, Dongquan ^c   Elson, Charles O ^c   Weaver, Casey T ^a  

^a University of Alabama at Birmingham   (United States)

^b University of Alabama at Birmingham   (United States)

^c University of Alabama at Birmingham   (United States)

Author keywords

MOLIMMUNO

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 12; INTERLEUKIN 12 RECEPTOR BETA2; INTERLEUKIN 17; INTERLEUKIN 17F; INTERLEUKIN 23; MESSENGER RNA; STAT4 PROTEIN; TRANSCRIPTION FACTOR T BET; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUTOIMMUNITY; BAGG ALBINO MOUSE; C57BL 6 MOUSE; CELL FATE; CELL LINEAGE; CELL MATURATION; CELLULAR IMMUNITY; COLITIS; CYTOKINE PRODUCTION; HOST RESISTANCE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; TH17 CELL;

ANIMALS; CELL LINEAGE; CELLS, CULTURED; FLOW CYTOMETRY; INTERFERON-GAMMA; INTERLEUKIN-17; INTERLEUKIN-23; MICE; MICE, KNOCKOUT; T-LYMPHOCYTE SUBSETS; TH1 CELLS; TH2 CELLS; TRANSFORMING GROWTH FACTOR BETA;

EID: 58149251898     PISSN: 10747613     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.immuni.2008.11.005     Document Type: Article

References (60)

1. 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
2. Annunziato F., Cosmi L., Santarlasci V., Maggi L., Liotta F., Mazzinghi B., Parente E., Fili L., Ferri S., Frosali F., et al. Phenotypic and functional features of human Th17 cells. J. Exp. Med. 204 (2007) 1849-1861
3. Batten M., Li J., Yi S., Kljavin N.M., Danilenko D.M., Lucas S., Lee J., de Sauvage F.J., and Ghilardi N. Interleukin 27 limits autoimmune encephalomyelitis by suppressing the development of interleukin 17-producing T cells. Nat. Immunol. 7 (2006) 929-936
4. Becher B., Durell B.G., and Noelle R.J. Experimental autoimmune encephalitis and inflammation in the absence of interleukin-12. J. Clin. Invest. 110 (2002) 493-497
5. 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
6. Bettelli E., and Kuchroo V.K. IL-12- and IL-23-induced T helper cell subsets: Birds of the same feather flock together. J. Exp. Med. 201 (2005) 169-171
7. Bettelli E., Sullivan B., Szabo S.J., Sobel R.A., Glimcher L.H., and Kuchroo V.K. Loss of T-bet, but not STAT1, prevents the development of experimental autoimmune encephalomyelitis. J. Exp. Med. 200 (2004) 79-87
8. Chang S.H., and Dong C. A novel heterodimeric cytokine consisting of IL-17 and IL-17F regulates inflammatory responses. Cell Res. 17 (2007) 435-440
9. 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
10. Chitnis T., Najafian N., Benou C., Salama A.D., Grusby M.J., Sayegh M.H., and Khoury S.J. Effect of targeted disruption of STAT4 and STAT6 on the induction of experimental autoimmune encephalomyelitis. J. Clin. Invest. 108 (2001) 739-747
11. 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
12. Dardalhon V., Korn T., Kuchroo V.K., and Anderson A.C. Role of Th1 and Th17 cells in organ-specific autoimmunity. J. Autoimmun. 31 (2008) 252-256
13. Elson C.O., Cong Y., Weaver C.T., Schoeb T.R., McClanahan T.K., Fick R.B., and Kastelein R.A. Monoclonal anti-interleukin 23 reverses active colitis in a T cell-mediated model in mice. Gastroenterology 132 (2007) 2359-2370
14. Ferber I.A., Brocke S., Taylor-Edwards C., Ridgway W., Dinisco C., Steinman L., Dalton D., and Fathman C.G. Mice with a disrupted IFN-gamma gene are susceptible to the induction of experimental autoimmune encephalomyelitis (EAE). J. Immunol. 156 (1996) 5-7
15. Gorelik L., Fields P.E., and Flavell R.A. Cutting edge: TGF-beta inhibits Th type 2 development through inhibition of GATA-3 expression. J. Immunol. 165 (2000) 4773-4777
16. Gorham J.D., Guler M.L., Fenoglio D., Gubler U., and Murphy K.M. Low dose TGF-beta attenuates IL-12 responsiveness in murine Th cells. J. Immunol. 161 (1998) 1664-1670
17. Gran B., Zhang G.X., Yu S., Li J., Chen X.H., Ventura E.S., Kamoun M., and Rostami A. IL-12p35-deficient mice are susceptible to experimental autoimmune encephalomyelitis: Evidence for redundancy in the IL-12 system in the induction of central nervous system autoimmune demyelination. J. Immunol. 169 (2002) 7104-7110
18. + effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat. Immunol. 6 (2005) 1123-1132
19. Harrington L.E., Janowski K.M., Oliver J.R., Zajac A.J., and Weaver C.T. Memory CD4 T cells emerge from effector T-cell progenitors. Nature 452 (2008) 356-360
20. Harris T.J., Grosso J.F., Yen H.R., Xin H., Kortylewski M., Albesiano E., Hipkiss E.L., Getnet D., Goldberg M.V., Maris C.H., et al. Cutting edge: An in vivo requirement for STAT3 signaling in TH17 development and TH17-dependent autoimmunity. J. Immunol. 179 (2007) 4313-4317
21. Hymowitz S.G., Filvaroff E.H., Yin J.P., Lee J., Cai L., Risser P., Maruoka M., Mao W., Foster J., Kelley R.F., et al. IL-17s adopt a cystine knot fold: Structure and activity of a novel cytokine, IL-17F, and implications for receptor binding. EMBO J. 20 (2001) 5332-5341
22. Iqbal N., Oliver J.R., Wagner F.H., Lazenby A.S., Elson C.O., and Weaver C.T. T helper 1 and T helper 2 cells are pathogenic in an antigen-specific model of colitis. J. Exp. Med. 195 (2002) 71-84
23. + T helper cells. Cell 126 (2006) 1121-1133
24. Izcue A., Hue S., Buonocore S., Arancibia-Carcamo C.V., Ahern P.P., Iwakura Y., Maloy K.J., and Powrie F. Interleukin-23 restrains regulatory T cell activity to drive T cell-dependent colitis. Immunity 28 (2008) 559-570
25. + T cell responses after vaccination and during Mycobacterium tuberculosis challenge. Nat. Immunol. 8 (2007) 369-377
26. Kolls J.K., and Linden A. Interleukin-17 family members and inflammation. Immunity 21 (2004) 467-476
27. Korn T., Bettelli E., Gao W., Awasthi A., Jager A., Strom T.B., Oukka M., and Kuchroo V.K. IL-21 initiates an alternative pathway to induce proinflammatory T(H)17 cells. Nature 448 (2007) 484-487
28. 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
29. Laurence A., Tato C.M., Davidson T.S., Kanno Y., Chen Z., Yao Z., Blank R.B., Meylan F., Siegel R., Hennighausen L., et al. Interleukin-2 signaling via STAT5 constrains T helper 17 cell generation. Immunity 26 (2007) 371-381
30. Letimier F.A., Passini N., Gasparian S., Bianchi E., and Rogge L. Chromatin remodeling by the SWI/SNF-like BAF complex and STAT4 activation synergistically induce IL-12Rbeta2 expression during human Th1 cell differentiation. EMBO J. 26 (2007) 1292-1302
31. Liang S.C., Long A.J., Bennett F., Whitters M.J., Karim R., Collins M., Goldman S.J., Dunussi-Joannopoulos K., Williams C.M., Wright J.F., and Fouser L.A. An IL-17F/A heterodimer protein is produced by mouse Th17 cells and induces airway neutrophil recruitment. J. Immunol. 179 (2007) 7791-7799
32. + T cells at priming and at recall: Differential involvement of Stat4 and T-bet. J. Immunol. 174 (2005) 5950-5958
33. 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
34. Mathur A.N., Chang H.C., Zisoulis D.G., Kapur R., Belladonna M.L., Kansas G.S., and Kaplan M.H. T-bet is a critical determinant in the instability of the IL-17-secreting T-helper phenotype. Blood 108 (2006) 1595-1601
35. Mathur A.N., Chang H.C., Zisoulis D.G., Stritesky G.L., Yu Q., O'Malley J.T., Kapur R., Levy D.E., Kansas G.S., and Kaplan M.H. Stat3 and Stat4 direct development of IL-17-secreting Th cells. J. Immunol. 178 (2007) 4901-4907
36. + and Foxp3- precursor cells in the absence of interleukin 10. Nat. Immunol. 8 (2007) 931-941
37. McGeachy M.J., Bak-Jensen K.S., Chen Y., Tato C.M., Blumenschein W., McClanahan T., and Cua D.J. 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. 8 (2007) 1390-1397
38. McGeachy M.J., and Cua D.J. Th17 cell differentiation: The long and winding road. Immunity 28 (2008) 445-453
39. McKenzie B.S., Kastelein R.A., and Cua D.J. Understanding the IL-23-IL-17 immune pathway. Trends Immunol. 27 (2006) 17-23
40. 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
41. Neurath M.F., Weigmann B., Finotto S., Glickman J., Nieuwenhuis E., Iijima H., Mizoguchi A., Mizoguchi E., Mudter J., Galle P.R., et al. The transcription factor T-bet regulates mucosal T cell activation in experimental colitis and Crohn's disease. J. Exp. Med. 195 (2002) 1129-1143
42. Nurieva R., Yang X.O., Martinez G., Zhang Y., Panopoulos A.D., Ma L., Schluns K., Tian Q., Watowich S.S., Jetten A.M., and Dong C. Essential autocrine regulation by IL-21 in the generation of inflammatory T cells. Nature 448 (2007) 480-483
43. 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
44. Parham C., Chirica M., Timans J., Vaisberg E., Travis M., Cheung J., Pflanz S., Zhang R., Singh K.P., Vega F., et al. A receptor for the heterodimeric cytokine IL-23 is composed of IL-12Rbeta1 and a novel cytokine receptor subunit, IL-23R. J. Immunol. 168 (2002) 5699-5708
45. 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
46. + T cells. J. Exp. Med. 183 (1996) 2669-2674
47. + T cells are important for the balance between protective and pathogenic cell-mediated immunity. J. Exp. Med. 179 (1994) 589-600
48. + T cells induce or protect from chronic intestinal inflammation in C. B-17 scid mice. Int. Immunol. 5 (1993) 1461-1471
49. Stockinger B., and Veldhoen M. Differentiation and function of Th17 T cells. Curr. Opin. Immunol. 19 (2007) 281-286
50. 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
51. Villarino A., Hibbert L., Lieberman L., Wilson E., Mak T., Yoshida H., Kastelein R.A., Saris C., and Hunter C.A. The IL-27R (WSX-1) is required to suppress T cell hyperactivity during infection. Immunity 19 (2003) 645-655
52. Weaver C.T., Harrington L.E., Mangan P.R., Gavrieli M., and Murphy K.M. Th17: An effector CD4 T cell lineage with regulatory T cell ties. Immunity 24 (2006) 677-688
53. Weaver C.T., Hatton R.D., Mangan P.R., and Harrington L.E. IL-17 family cytokines and the expanding diversity of effector T cell lineages. Annu. Rev. Immunol. 25 (2007) 821-852
54. Willenborg D.O., Fordham S., Bernard C.C., Cowden W.B., and Ramshaw I.A. IFN-gamma plays a critical down-regulatory role in the induction and effector phase of myelin oligodendrocyte glycoprotein-induced autoimmune encephalomyelitis. J. Immunol. 157 (1996) 3223-3227
55. Yang X.O., Panopoulos A.D., Nurieva R., Chang S.H., Wang D., Watowich S.S., and Dong C. STAT3 regulates cytokine-mediated generation of inflammatory helper T cells. J. Biol. Chem. 282 (2007) 9358-9363
56. 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 28 (2008) 29-39
57. Zhang G.X., Gran B., Yu S., Li J., Siglienti I., Chen X., Kamoun M., and Rostami A. Induction of experimental autoimmune encephalomyelitis in IL-12 receptor-beta 2-deficient mice: IL-12 responsiveness is not required in the pathogenesis of inflammatory demyelination in the central nervous system. J. Immunol. 170 (2003) 2153-2160
58. Zheng Y., Danilenko D.M., Valdez P., Kasman I., Eastham-Anderson J., Wu J., and Ouyang W. Interleukin-22, a T(H)17 cytokine, mediates IL-23-induced dermal inflammation and acanthosis. Nature 445 (2007) 648-651
59. Zheng Y., Valdez P.A., Danilenko D.M., Hu Y., Sa S.M., Gong Q., Abbas A.R., Modrusan Z., Ghilardi N., de Sauvage F.J., and Ouyang W. Interleukin-22 mediates early host defense against attaching and effacing bacterial pathogens. Nat. Med. 14 (2008) 282-289
60. Zhou L., Ivanov I.I., Spolski R., Min R., Shenderov K., Egawa T., Levy D.E., Leonard W.J., and Littman D.R. IL-6 programs T(H)-17 cell differentiation by promoting sequential engagement of the IL-21 and IL-23 pathways. Nat. Immunol. 8 (2007) 967-974