Interleukin-23 and T helper 17-type responses in intestinal inflammation: From cytokines to T-cell plasticity

Immunology

Volumn 133, Issue 4, 2011, Pages 397-408

  Morrison, Peter J ^a   Ballantyne, Sarah J ^a   Kullberg, Marika C ^a  

^a UNIVERSITY OF YORK   (United Kingdom)

Author keywords

Colitis; Inflammation; Interferon ; Interleukin 17A; Interleukin 23; T helper 17 cells

Indexed keywords

CYTOKINE; GAMMA INTERFERON; INTERLEUKIN 17; INTERLEUKIN 17F; INTERLEUKIN 21; INTERLEUKIN 22; INTERLEUKIN 23;

COLITIS; CYTOKINE PRODUCTION; ENTERITIS; HUMAN; NONHUMAN; PATHOGENICITY; PHENOTYPE; PLASTICITY; PRIORITY JOURNAL; REVIEW; T LYMPHOCYTE; TH1 CELL; TH17 CELL;

ANIMALS; HUMANS; INFLAMMATION; INTERLEUKIN-23; INTESTINES; TH17 CELLS;

EID: 79959875101     PISSN: 00192805     EISSN: 13652567     Source Type: Journal    
DOI: 10.1111/j.1365-2567.2011.03454.x     Document Type: Review

References (151)

1. Xavier RJ, Podolsky DK. Unravelling the pathogenesis of inflammatory bowel disease. Nature 2007; 448:427-34.
2. Bouma G, Strober W. The immunological and genetic basis of inflammatory bowel disease. Nat Rev Immunol 2003; 3:521-33.
3. Oppmann B, Lesley R, Blom B 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 2000; 13:715-25.
4. Yen D, Cheung J, Scheerens H et al. IL-23 is essential for T cell-mediated colitis and promotes inflammation via IL-17 and IL-6. J Clin Invest 2006; 116:1310-6.
5. Uhlig HH, McKenzie BS, Hue S et al. Differential activity of IL-12 and IL-23 in mucosal and systemic innate immune pathology. Immunity 2006; 25:309-18.
6. Hue S, Ahern P, Buonocore S, Kullberg MC, Cua DJ, McKenzie BS, Powrie F, Maloy KJ. Interleukin-23 drives innate and T cell-mediated intestinal inflammation. J Exp Med 2006; 203:2473-83.
7. Kullberg MC, Jankovic D, Feng CG et al. IL-23 plays a key role in Helicobacter hepaticus-induced T cell-dependent colitis. J Exp Med 2006; 203:2485-94.
8. Elson CO, Cong Y, Weaver CT, Schoeb TR, McClanahan TK, Fick RB, Kastelein RA. Monoclonal anti-interleukin 23 reverses active colitis in a T cell-mediated model in mice. Gastroenterology 2007; 132:2359-70.
9. Duerr RH, Taylor KD, Brant SR et al. A genome-wide association study identifies IL23R as an inflammatory bowel disease gene. Science 2006; 314:1461-3.
10. The Wellcome Trust Case Control Consortium. Genome-wide association study of 14, 000 cases of seven common diseases and 3, 000 shared controls. Nature 2007; 447:661-78.
11. Mancini G, Kan SH, Gallagher G. A novel insertion variant of the human IL-23 receptor-a chain transcript. Genes Immun 2008; 9:566-9.
12. Kan SH, Mancini G, Gallagher G. Identification and characterization of multiple splice forms of the human interleukin-23 receptor a chain in mitogen-activated leukocytes. Genes Immun 2008; 9:631-9.
13. Langrish CL, McKenzie BS, Wilson NJ, de Waal Malefyt R, Kastelein RA, Cua DJ. IL-12 and IL-23: Master regulators of innate and adaptive immunity. Immunol Rev 2004; 202:96-105.
14. Aggarwal S, Ghilardi N, Xie MH, de Sauvage FJ, Gurney AL. Interleukin-23 promotes a distinct CD4 T cell activation state characterized by the production of interleukin-17. J Biol Chem 2003; 278:1910-4.
15. 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.
16. Weaver CT, Hatton RD, Mangan PR, Harrington LE. IL-17 family cytokines and the expanding diversity of effector T cell lineages. Annu Rev Immunol 2007; 25:821-52.
17. McGeachy MJ, Cua DJ. Th17 cell differentiation: the long and winding road. Immunity 2008; 28:445-53.
18. Korn T, Oukka M, Kuchroo V, Bettelli E. Th17 cells: effector T cells with inflammatory properties. Semin Immunol 2007; 19:362-71.
19. Tesmer LA, Lundy SK, Sarkar S, Fox DA. Th17 cells in human disease. Immunol Rev 2008; 223:87-113.
20. Fujino S, Andoh A, Bamba S, Ogawa A, Hata K, Araki Y, Bamba T, Fujiyama Y. Increased expression of interleukin 17 in inflammatory bowel disease. Gut 2003; 52:65-70.
21. Nielsen OH, Kirman I, Rudiger N, Hendel J, Vainer B. Upregulation of interleukin-12 and -17 in active inflammatory bowel disease. Scand J Gastroenterol 2003; 38:180-5.
22. Seiderer J, Elben I, Diegelmann J et al. Role of the novel Th17 cytokine IL-17F in inflammatory bowel disease (IBD): upregulated colonic IL-17F expression in active Crohn's disease and analysis of the IL17F p.His161Arg polymorphism in IBD. Inflamm Bowel Dis 2008; 14:437-45.
23. Monteleone G, Monteleone I, Fina D et al. Interleukin-21 enhances T-helper cell type I signaling and interferon-g production in Crohn's disease. Gastroenterology 2005; 128:687-94.
24. Brand S, Beigel F, Olszak T et al. IL-22 is increased in active Crohn's disease and promotes proinflammatory gene expression and intestinal epithelial cell migration. Am J Physiol Gastrointest Liver Physiol 2006; 290:G827-38.
25. Wolk K, Witte E, Hoffmann U et al. IL-22 induces lipopolysaccharide-binding protein in hepatocytes: a potential systemic role of IL-22 in Crohn's disease. J Immunol 2007; 178:5973-81.
26. + T helper cells. Cell 2006; 126:1121-33.
27. Becker C, Wirtz S, Blessing M et al. Constitutive p40 promoter activation and IL-23 production in the terminal ileum mediated by dendritic cells. J Clin Invest 2003; 112:693-706.
28. Ivanov II, Frutos Rde L, Manel N, Yoshinaga K, Rifkin DB, Sartor RB, Finlay BB, Littman DR. Specific microbiota direct the differentiation of IL-17-producing T-helper cells in the mucosa of the small intestine. Cell Host Microbe 2008; 4:337-49.
29. Niess JH, Leithauser F, Adler G, Reimann J. Commensal gut flora drives the expansion of proinflammatory CD4 T cells in the colonic lamina propria under normal and inflammatory conditions. J Immunol 2008; 180:559-68.
30. Ivanov II, Atarashi K, Manel N et al. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell 2009; 139:485-98.
31. Barnes MJ, Powrie F. Regulatory T cells reinforce intestinal homeostasis. Immunity 2009; 31:401-11.
32. Izcue A, Hue S, Buonocore S, Arancibia-Carcamo CV, Ahern PP, Iwakura Y, Maloy KJ, Powrie F. Interleukin-23 restrains regulatory T cell activity to drive T cell-dependent colitis. Immunity 2008; 28:559-70.
33. Ahern PP, Schiering C, Buonocore S, McGeachy MJ, Cua DJ, Maloy KJ, Powrie F. Interleukin-23 drives intestinal inflammation through direct activity on T cells. Immunity 2010; 33:279-88.
34. Buonocore S, Ahern PP, Uhlig HH, Ivanov II, Littman DR, Maloy KJ, Powrie F. Innate lymphoid cells drive interleukin-23-dependent innate intestinal pathology. Nature 2010; 464:1371-5.
35. Umemura M, Yahagi A, Hamada S et al. IL-17-mediated regulation of innate and acquired immune response against pulmonary Mycobacterium bovis bacille Calmette-Guerin infection. J Immunol 2007; 178:3786-96.
36. Ouyang W, Kolls JK, Zheng Y. The biological functions of T helper 17 cell effector cytokines in inflammation. Immunity 2008; 28:454-67.
37. Ishigame H, Kakuta S, Nagai T et al. Differential roles of interleukin-17A and -17F in host defense against mucoepithelial bacterial infection and allergic responses. Immunity 2009; 30:108-19.
38. Zheng Y, Valdez PA, Danilenko DM et al. Interleukin-22 mediates early host defense against attaching and effacing bacterial pathogens. Nat Med 2008; 14:282-9.
39. Kao CY, Chen Y, Thai P, Wachi S, Huang F, Kim C, Harper RW, Wu R. IL-17 markedly up-regulates b-defensin-2 expression in human airway epithelium via JAK and NF-kB signaling pathways. J Immunol 2004; 173:3482-91.
40. Liang SC, Tan XY, Luxenberg DP, Karim R, Dunussi-Joannopoulos K, Collins M, Fouser LA. Interleukin (IL)-22 and IL-17 are coexpressed by Th17 cells and cooperatively enhance expression of antimicrobial peptides. J Exp Med 2006; 203:2271-9.
41. Ogawa A, Andoh A, Araki Y, Bamba T, Fujiyama Y. Neutralization of interleukin-17 aggravates dextran sulfate sodium-induced colitis in mice. Clin Immunol 2004; 110:55-62.
42. Yang XO, Chang SH, Park H et al. Regulation of inflammatory responses by IL-17F. J Exp Med 2008; 205:1063-75.
43. Strober W, Fuss IJ, Blumberg RS. The immunology of mucosal models of inflammation. Annu Rev Immunol 2002; 20:495-549.
44. Kinugasa T, Sakaguchi T, Gu X, Reinecker HC. Claudins regulate the intestinal barrier in response to immune mediators. Gastroenterology 2000; 118:1001-11.
45. Chen Y, Thai P, Zhao YH, Ho YS, DeSouza MM, Wu R. Stimulation of airway mucin gene expression by interleukin (IL)-17 through IL-6 paracrine/autocrine loop. J Biol Chem 2003; 278:17036-43.
46. Zenewicz LA, Yancopoulos GD, Valenzuela DM, Murphy AJ, Stevens S, Flavell RA. Innate and adaptive interleukin-22 protects mice from inflammatory bowel disease. Immunity 2008; 29:947-57.
47. Sugimoto K, Ogawa A, Mizoguchi E et al. IL-22 ameliorates intestinal inflammation in a mouse model of ulcerative colitis. J Clin Invest 2008; 118:534-44.
48. Kolls JK, Linden A. Interleukin-17 family members and inflammation. Immunity 2004; 21:467-76.
49. Iwakura Y, Ishigame H, Saijo S, Nakae S. Functional specialization of interleukin-17 family members. Immunity 2011; 34:149-62.
50. Gaffen SL. Structure and signalling in the IL-17 receptor family. Nat Rev Immunol 2009; 9:556-67.
51. + T cells. J Biol Chem 2007; 282:13447-55.
52. Liang SC, Long AJ, Bennett F et al. An IL-17F/A heterodimer protein is produced by mouse Th17 cells and induces airway neutrophil recruitment. J Immunol 2007; 179:7791-9.
53. Zhang Z, Zheng M, Bindas J, Schwarzenberger P, Kolls JK. Critical role of IL-17 receptor signaling in acute TNBS-induced colitis. Inflamm Bowel Dis 2006; 12:382-8.
54. Qian Y, Liu C, Hartupee J et al. The adaptor Act1 is required for interleukin 17-dependent signaling associated with autoimmune and inflammatory disease. Nat Immunol 2007; 8:247-56.
55. Fina D, Sarra M, Fantini MC et al. Regulation of gut inflammation and Th17 cell response by interleukin-21. Gastroenterology 2008; 134:1038-48.
56. Monteleone G, Caruso R, Fina D et al. Control of matrix metalloproteinase production in human intestinal fibroblasts by interleukin 21. Gut 2006; 55:1774-80.
57. Caruso R, Fina D, Peluso I et al. A functional role for interleukin-21 in promoting the synthesis of the T-cell chemoattractant, MIP-3a, by gut epithelial cells. Gastroenterology 2007; 132:166-75.
58. Fantini MC, Rizzo A, Fina D et al. IL-21 regulates experimental colitis by modulating the balance between Treg and Th17 cells. Eur J Immunol 2007; 37:3155-63.
59. + T lymphocytes. J Immunol 2007; 178:732-9.
60. Strengell M, Sareneva T, Foster D, Julkunen I, Matikainen S. IL-21 up-regulates the expression of genes associated with innate immunity and Th1 response. J Immunol 2002; 169:3600-5.
61. Strengell M, Matikainen S, Siren J, Lehtonen A, Foster D, Julkunen I, Sareneva T. IL-21 in synergy with IL-15 or IL-18 enhances IFN-g production in human NK and T cells. J Immunol 2003; 170:5464-9.
62. Zhou L, Ivanov II, Spolski R et al. IL-6 programs TH-17 cell differentiation by promoting sequential engagement of the IL-21 and IL-23 pathways. Nat Immunol 2007; 8:967-74.
63. Korn T, Bettelli E, Gao W, Awasthi A, Jager A, Strom TB, Oukka M, Kuchroo VK. IL-21 initiates an alternative pathway to induce proinflammatory TH17 cells. Nature 2007; 448:484-7.
64. Nurieva R, Yang XO, Martinez G et al. Essential autocrine regulation by IL-21 in the generation of inflammatory T cells. Nature 2007; 448:480-3.
65. + T cell-mediated colitis in a Th17-independent manner. Int Immunol 2007; 19:1431-40.
66. Leppkes M, Becker C, Ivanov II et al. RORg-expressing Th17 cells induce murine chronic intestinal inflammation via redundant effects of IL-17A and IL-17F. Gastroenterology 2009; 136:257-67.
67. 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.
68. Boniface K, Blumenschein WM, Brovont-Porth K et al. Human Th17 cells comprise heterogeneous subsets including IFN-g-producing cells with distinct properties from the Th1 lineage. J Immunol 2010; 185:679-87.
69. Veldhoen M, Hocking RJ, Atkins CJ, Locksley RM, Stockinger B. TGFb in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells. Immunity 2006; 24:179-89.
70. Mangan PR, Harrington LE, O'Quinn DB et al. Transforming growth factor-b induces development of the TH17 lineage. Nature 2006; 441:231-4.
71. 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.
72. Acosta-Rodriguez EV, Napolitani G, Lanzavecchia A, Sallusto F. Interleukins 1b and 6 but not transforming growth factor-b are essential for the differentiation of interleukin 17-producing human T helper cells. Nat Immunol 2007; 8:942-9.
73. Wilson NJ, Boniface K, Chan JR et al. Development, cytokine profile and function of human interleukin 17-producing helper T cells. Nat Immunol 2007; 8:950-7.
74. Zheng Y, Danilenko DM, 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; 445:648-51.
75. McGeachy MJ, Bak-Jensen KS, Chen Y, Tato CM, Blumenschein W, McClanahan T, Cua DJ. TGF-b and IL-6 drive the production of IL-17 and IL-10 by T cells and restrain TH-17 cell-mediated pathology. Nat Immunol 2007; 8:1390-7.
76. Suryani S, Sutton I. An interferon-g-producing Th1 subset is the major source of IL-17 in experimental autoimmune encephalitis. J Neuroimmunol 2007; 183:96-103.
77. Acosta-Rodriguez EV, Rivino L, Geginat J, Jarrossay D, Gattorno M, Lanzavecchia A, Sallusto F, Napolitani G. Surface phenotype and antigenic specificity of human interleukin 17-producing T helper memory cells. Nat Immunol 2007; 8:639-46.
78. Annunziato F, Cosmi L, Santarlasci V et al. Phenotypic and functional features of human Th17 cells. J Exp Med 2007; 204:1849-61.
79. + T cell precursor. J Exp Med 2008; 205:1903-16.
80. Luger D, Silver PB, Tang J et al. Either a Th17 or a Th1 effector response can drive autoimmunity: conditions of disease induction affect dominant effector category. J Exp Med 2008; 205:799-810.
81. + T cells. Science 2010; 327:1098-102.
82. Murphy KM, Stockinger B. Effector T cell plasticity: flexibility in the face of changing circumstances. Nat Immunol 2010; 11:674-80.
83. Shi G, Cox CA, Vistica BP, Tan C, Wawrousek EF, Gery I. Phenotype switching by inflammation-inducing polarized Th17 cells, but not by Th1 cells. J Immunol 2008; 181:7205-13.
84. Lee YK, Turner H, Maynard CL, Oliver JR, Chen D, Elson CO, Weaver CT. Late developmental plasticity in the T helper 17 lineage. Immunity 2009; 30:92-107.
85. Bending D, De La Pena H, Veldhoen M, Phillips JM, Uyttenhove C, Stockinger B, Cooke A. Highly purified Th17 cells from BDC2.5NOD mice convert into Th1-like cells in NOD/SCID recipient mice. J Clin Invest 2009; 119:565-72.
86. Martin-Orozco N, Chung Y, Chang SH, Wang YH, Dong C. Th17 cells promote pancreatic inflammation but only induce diabetes efficiently in lymphopenic hosts after conversion into Th1 cells. Eur J Immunol 2009; 39:216-24.
87. Lexberg MH, Taubner A, Forster A, Albrecht I, Richter A, Kamradt T, Radbruch A, Chang HD. Th memory for interleukin-17 expression is stable in vivo. Eur J Immunol 2008; 38:2654-64.
88. Lexberg MH, Taubner A, Albrecht I, Lepenies I, Richter A, Kamradt T, Radbruch A, Chang HD. IFN-g and IL-12 synergize to convert in vivo generated Th17 into Th1/Th17 cells. Eur J Immunol 2010; 40:3017-27.
89. Nurieva R, Yang XO, Chung Y, Dong C. Cutting edge: in vitro generated Th17 cells maintain their cytokine expression program in normal but not lymphopenic hosts. J Immunol 2009; 182:2565-8.
90. Kurschus FC, Croxford AL, Heinen AP, Wortge S, Ielo D, Waisman A. Genetic proof for the transient nature of the Th17 phenotype. Eur J Immunol 2010; 40:3336-46.
91. Hirota K, Duarte JH, Veldhoen M et al. Fate mapping of IL-17-producing T cells in inflammatory responses. Nat Immunol 2011; 12:255-63.
92. Bending D, Newland S, Krejci A, Phillips JM, Bray S, Cooke A. Epigenetic changes at il12rb2 and tbx21 in relation to plasticity behavior of Th17 cells. J Immunol 2011; 186:3373-82.
93. + T cells are important for the balance between protective and pathogenic cell-mediated immunity. J Exp Med 1994; 179:589-600.
94. + T cells. Immunity 1994; 1:553-62.
95. + TH1-like responses. J Clin Invest 1996; 98:1010-20.
96. 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; 66:5157-66.
97. Cooper AM, Kipnis A, Turner J, Magram J, Ferrante J, Orme IM. Mice lacking bioactive IL-12 can generate protective, antigen-specific cellular responses to mycobacterial infection only if the IL-12 p40 subunit is present. J Immunol 2002; 168:1322-7.
98. Khader SA, Pearl JE, Sakamoto K et al. IL-23 compensates for the absence of IL-12p70 and is essential for the IL-17 response during tuberculosis but is dispensable for protection and antigen-specific IFN-g responses if IL-12p70 is available. J Immunol 2005; 175:788-95.
99. Simpson SJ, Shah S, Comiskey M, de Jong YP, Wang B, Mizoguchi E, Bhan AK, Terhorst C. T cell-mediated pathology in two models of experimental colitis depends predominantly on the interleukin 12/Signal transducer and activator of transcription (Stat)-4 pathway, but is not conditional on interferon g expression by T cells. J Exp Med 1998; 187:1225-34.
100. + T cells from interferon-gamma (IFN-g)-deficient mice induce intestinal inflammation in immunodeficient hosts. Clin Exp Immunol 1999; 118:228-34.
101. Neurath MF, Weigmann B, Finotto S et al. The transcription factor T-bet regulates mucosal T cell activation in experimental colitis and Crohn's disease. J Exp Med 2002; 195:1129-43.
102. Durant L, Watford WT, Ramos HL et al. Diverse targets of the transcription factor STAT3 contribute to T cell pathogenicity and homeostasis. Immunity 2010; 32:605-15.
103. Fossiez F, Djossou O, Chomarat P et al. T cell interleukin-17 induces stromal cells to produce proinflammatory and hematopoietic cytokines. J Exp Med 1996; 183:2593-603.
104. Infante-Duarte C, Horton HF, Byrne MC, Kamradt T. Microbial lipopeptides induce the production of IL-17 in Th cells. J Immunol 2000; 165:6107-15.
105. Murphy CA, Langrish CL, Chen Y, Blumenschein W, McClanahan T, Kastelein RA, Sedgwick JD, Cua DJ. Divergent pro- and antiinflammatory roles for IL-23 and IL-12 in joint autoimmune inflammation. J Exp Med 2003; 198:1951-7.
106. Park H, Li Z, Yang XO et al. A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat Immunol 2005; 6:1133-41.
107. Stark MA, Huo Y, Burcin TL, Morris MA, Olson TS, Ley K. Phagocytosis of apoptotic neutrophils regulates granulopoiesis via IL-23 and IL-17. Immunity 2005; 22:285-94.
108. Yao Z, Painter SL, Fanslow WC, Ulrich D, Macduff BM, Spriggs MK, Armitage RJ. Human IL-17: a novel cytokine derived from T cells. J Immunol 1995; 155:5483-6.
109. Happel KI, Zheng M, Young E et al. Cutting edge: roles of Toll-like receptor 4 and IL-23 in IL-17 expression in response to Klebsiella pneumoniae infection. J Immunol 2003; 170:4432-6.
110. + T cells. J Exp Med 2008; 205:1019-27.
111. Do JS, Fink PJ, Li L, Spolski R, Robinson J, Leonard WJ, Letterio JJ, Min B. Cutting edge: spontaneous development of IL-17-producing gd T cells in the thymus occurs via a TGF-b1-dependent mechanism. J Immunol 2010; 184:1675-9.
112. Hayday AC. δγ T cells and the lymphoid stress-surveillance response. Immunity 2009; 31:184-96.
113. + T cells. J Exp Med 2008; 205:1381-93.
114. Lockhart E, Green AM, Flynn JL. IL-17 production is dominated by gd T cells rather than CD4 T cells during Mycobacterium tuberculosis infection. J Immunol 2006; 177:4662-9.
115. Martin B, Hirota K, Cua DJ, Stockinger B, Veldhoen M. Interleukin-17-producing gd T cells selectively expand in response to pathogen products and environmental signals. Immunity 2009; 31:321-30.
116. Riol-Blanco L, Lazarevic V, Awasthi A et al. IL-23 receptor regulates unconventional IL-17-producing T cells that control bacterial infections. J Immunol 2010; 184:1710-20.
117. Sutton CE, Lalor SJ, Sweeney CM, Brereton CF, Lavelle EC, Mills KH. Interleukin-1 and IL-23 induce innate IL-17 production from gd T cells, amplifying Th17 responses and autoimmunity. Immunity 2009; 31:331-41.
118. Yang XO, Pappu BP, Nurieva R et al. T helper 17 lineage differentiation is programmed by orphan nuclear receptors RORa and RORg. Immunity 2008; 28:29-39.
119. Bauquet AT, Jin H, Paterson AM, Mitsdoerffer M, Ho IC, Sharpe AH, Kuchroo VK. 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; 10:167-75.
120. Doisne JM, Becourt C, Amniai L, Duarte N, Le Luduec JB, Eberl G, Benlagha K. Skin and peripheral lymph node invariant NKT cells are mainly retinoic acid receptor-related orphan receptor gt+ and respond preferentially under inflammatory conditions. J Immunol 2009; 183:2142-9.
121. Lee KA, Kang MH, Lee YS, Kim YJ, Kim DH, Ko HJ, Kang CY. A distinct subset of natural killer T cells produces IL-17, contributing to airway infiltration of neutrophils but not to airway hyperreactivity. Cell Immunol 2008; 251:50-5.
122. Michel ML, Mendes-da-Cruz D, Keller AC, Lochner M, Schneider E, Dy M, Eberl G, Leite-de-Moraes MC. Critical role of ROR-gt in a new thymic pathway leading to IL-17-producing invariant NKT cell differentiation. Proc Natl Acad Sci U S A 2008; 105:19845-50.
123. Pichavant M, Goya S, Meyer EH et al. Ozone exposure in a mouse model induces airway hyperreactivity that requires the presence of natural killer T cells and IL-17. J Exp Med 2008; 205:385-93.
124. Rachitskaya AV, Hansen AM, Horai R, Li Z, Villasmil R, Luger D, Nussenblatt RB, Caspi RR. Cutting edge: NKT cells constitutively express IL-23 receptor and RORgt and rapidly produce IL-17 upon receptor ligation in an IL-6-independent fashion. J Immunol 2008; 180:5167-71.
125. Da Silva CA, Hartl D, Liu W, Lee CG, Elias JA. TLR-2 and IL-17A in chitin-induced macrophage activation and acute inflammation. J Immunol 2008; 181:4279-86.
126. Ferretti S, Bonneau O, Dubois GR, Jones CE, Trifilieff A. IL-17, produced by lymphocytes and neutrophils, is necessary for lipopolysaccharide-induced airway neutrophilia: IL-15 as a possible trigger. J Immunol 2003; 170:2106-12.
127. Li L, Huang L, Vergis AL et al. IL-17 produced by neutrophils regulates IFN-g-mediated neutrophil migration in mouse kidney ischemia-reperfusion injury. J Clin Invest 2010; 120:331-42.
128. Colonna M. Interleukin-22-producing natural killer cells and lymphoid tissue inducer-like cells in mucosal immunity. Immunity 2009; 31:15-23.
129. + lineage distinct from conventional natural killer cells. J Exp Med 2010; 207:281-90.
130. + natural killer-like cells. Nat Immunol 2009; 10:66-74.
131. Takatori H, Kanno Y, Watford WT, Tato CM, Weiss G, Ivanov II, Littman DR, O'Shea JJ. Lymphoid tissue inducer-like cells are an innate source of IL-17 and IL-22. J Exp Med 2009; 206:35-41.
132. Takahashi N, Vanlaere I, de Rycke R, Cauwels A, Joosten LA, Lubberts E, van den Berg WB, Libert C. IL-17 produced by Paneth cells drives TNF-induced shock. J Exp Med 2008; 205:1755-61.
133. Hueber AJ, Asquith DL, Miller AM, Reilly J, Kerr S, Leipe J, Melendez AJ, McInnes IB. Mast cells express IL-17A in rheumatoid arthritis synovium. J Immunol 2010; 184:3336-40.
134. + effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat Immunol 2005; 6:1123-32.
135. Veldhoen M, Hirota K, Westendorf AM, Buer J, Dumoutier L, Renauld JC, Stockinger B. The aryl hydrocarbon receptor links TH17-cell-mediated autoimmunity to environmental toxins. Nature 2008; 453:106-9.
136. Suzuki S, Kokubu F, Kawaguchi M et al. Expression of interleukin-17F in a mouse model of allergic asthma. Int Arch Allergy Immunol 2007; 143(Suppl. 1):89-94.
137. Chang SH, Dong C. A novel heterodimeric cytokine consisting of IL-17 and IL-17F regulates inflammatory responses. Cell Res 2007; 17:435-40.
138. Parrish-Novak J, Dillon SR, Nelson A et al. Interleukin 21 and its receptor are involved in NK cell expansion and regulation of lymphocyte function. Nature 2000; 408:57-63.
139. Wurster AL, Rodgers VL, Satoskar AR, Whitters MJ, Young DA, Collins M, Grusby MJ. Interleukin 21 is a T helper (Th) cell 2 cytokine that specifically inhibits the differentiation of naive Th cells into interferon g-producing Th1 cells. J Exp Med 2002; 196:969-77.
140. + T follicular helper cells. J Immunol 2007; 179:8180-90.
141. Chtanova T, Tangye SG, Newton R, Frank N, Hodge MR, Rolph MS, Mackay CR. T follicular helper cells express a distinctive transcriptional profile, reflecting their role as non-Th1/Th2 effector cells that provide help for B cells. J Immunol 2004; 173:68-78.
142. Coquet JM, Kyparissoudis K, Pellicci DG, Besra G, Berzins SP, Smyth MJ, Godfrey DI. IL-21 is produced by NKT cells and modulates NKT cell activation and cytokine production. J Immunol 2007; 178:2827-34.
143. Harada M, Magara-Koyanagi K, Watarai H et al. IL-21-induced Be cell apoptosis mediated by natural killer T cells suppresses IgE responses. J Exp Med 2006; 203:2929-37.
144. Andoh A, Zhang Z, Inatomi O et al. Interleukin-22, a member of the IL-10 subfamily, induces inflammatory responses in colonic subepithelial myofibroblasts. Gastroenterology 2005; 129:969-84.
145. + T lymphocytes. Cell Res 2006; 16:902-7.
146. Eyerich S, Eyerich K, Pennino D et al. Th22 cells represent a distinct human T cell subset involved in epidermal immunity and remodeling. J Clin Invest 2009; 119:3573-85.
147. + T cells lacking IL-17 production. Proc Natl Acad Sci U S A 2009; 106:21795-800.
148. Cella M, Fuchs A, Vermi W et al. A human natural killer cell subset provides an innate source of IL-22 for mucosal immunity. Nature 2009; 457:722-5.
149. + cell populations in gut and skin. Nat Immunol 2009; 10:75-82.
150. + cells that provide innate mucosal immune defense. Immunity 2008; 29:958-70.
151. + innate lymphoid cells. Immunology 2011; 132:453-65.