The roles and functional mechanisms of interleukin-17 family cytokines in mucosal immunity

Cellular and Molecular Immunology

Volumn 13, Issue 4, 2016, Pages 418-431

  Song, Xinyang ^a,b   He, Xiao ^a   Li, Xiaoxia ^c   Qian, Youcun ^a,b  

^a SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b SHANGHAI JIAO TONG UNIVERSITY   (China)

^c LERNER RESEARCH INSTITUTE   (United States)

Author keywords

IL 17 family cytokines; mucosal immunity; signal transduction

Indexed keywords

INTERLEUKIN 17; PATTERN RECOGNITION RECEPTOR;

COMMENSAL; CYTOKINE RELEASE; EPITHELIUM CELL; HUMAN; IMMUNOCOMPETENT CELL; IMMUNOLOGICAL TOLERANCE; MUCOSAL IMMUNITY; NONHUMAN; REVIEW; SIGNAL TRANSDUCTION; ANIMAL; BIOLOGICAL MODEL; IMMUNOLOGY; METABOLISM;

ANIMALS; HUMANS; IMMUNITY, MUCOSAL; INTERLEUKIN-17; MODELS, BIOLOGICAL; SIGNAL TRANSDUCTION;

EID: 84977530108     PISSN: 16727681     EISSN: None     Source Type: Journal    
DOI: 10.1038/cmi.2015.105     Document Type: Review

References (172)

1. Iwasaki A, Medzhitov R. Control of adaptive immunity by the innate immune system. Nat Immunol 2015; 16: 343-353.
2. Kawai T, Akira S. The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat Immunol 2010; 11: 373-384.
3. Wu J, Chen ZJ. Innate immune sensing and signaling of cytosolic nucleic acids. Annu Rev Immunol 2014; 32: 461-488.
4. Rathinam VA, Vanaja SK, Fitzgerald KA. Regulation of inflammasome signaling. Nat Immunol 2012; 13: 333-342.
5. Peterson LW, Artis D. Intestinal epithelial cells: regulators of barrier function and immune homeostasis. Nat Rev Immunol 2014; 14: 141-153.
6. Rescigno M. Functional specialization of antigen presenting cells in the gastrointestinal tract. Curr Opin Immunol 2010; 22: 131-136.
7. Sonnenberg GF, Artis D. Innate lymphoid cells in the initiation, regulation and resolution of inflammation. Nat Med 2015; 21: 698-708.
8. Eberl G, Colonna M, Di Santo JP, McKenzie AN. Innate lymphoid cells. Innate lymphoid cells: a new paradigm in immunology. Science 2015; 348: aaa6566.
9. Song X, Qian Y. IL-17 family cytokines mediated signaling in the pathogenesis of inflammatory diseases. Cell Signal 2013; 25: 2335-2347.
10. Pappu R, Rutz S, Ouyang W. Regulation of epithelial immunity by IL-17 family cytokines. Trends Immunol 2012; 33: 343-349.
11. Rouvier E, Luciani MF, Mattei MG, Denizot F, CTLA-8 Golstein P. cloned from an activated T cell, bearing AU-rich messenger RNA instability sequences, and homologous to a herpesvirus saimiri gene. J Immunol 1993; 150: 5445-5456.
12. Song X, Qian Y. The activation and regulation of IL-17 receptor mediated signaling. Cytokine 2013; 62: 175-182.
13. Korn T, Bettelli E, Oukka M, Kuchroo VK. IL-17 and Th17 Cells. Annu Rev Immunol 2009; 27: 485-517.
14. Cua DJ, Tato CM. Innate IL-17-producing cells: the sentinels of the immune system. Nat Rev Immunol 2010; 10: 479-489.
15. Gaffen SL. Structure and signalling in the IL-17 receptor family. Nat Rev Immunol 2009; 9: 556-567.
16. Iwakura Y, Ishigame H, Saijo S, Nakae S. Functional specialization of interleukin-17 family members. Immunity 2011; 34: 149-162.
17. Gerhardt S, Abbott WM, Hargreaves D, Pauptit RA, Davies RA, Needham MR et al. Structure of IL-17A in complex with a potent, fully human neutralizing antibody. J Mol Biol 2009; 394: 905-921.
18. Hymowitz SG, Filvaroff EH, Yin JP, Lee J, Cai L, Risser P 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 2001; 20: 5332-5341.
19. Johnston A, Fritz Y, Dawes SM, Diaconu D, Al-Attar PM, Guzman AM et al. Keratinocyte overexpression of IL-17C promotes psoriasiform skin inflammation. J Immunol 2013; 190: 2252-2262.
20. Yu HS, Angkasekwinai P, Chang SH, Chung Y, Dong C. Protease allergens induce the expression of IL-25 via Erk and p38 MAPK pathway. J Korean Med Sci 2010; 25: 829-834.
21. Wright JF, Bennett F, Li B, Brooks J, Luxenberg DP, Whitters MJ et al. The human IL-17F/IL-17AA heterodimeric cytokine signals through the IL-17RA/IL-17RC receptor complex. J Immunol 2008; 181: 2799-2805.
22. Toy D, Kugler D, Wolfson M, Vanden Bos T, Gurgel J, Derry J et al. Cutting edge: interleukin 17 signals through a heteromeric receptor complex. J Immunol 2006; 177: 36-39.
23. Kuestner RE, Taft DW, Haran A, Brandt CS, Brender T, Lum K et al. Identification of the IL-17 receptor related molecule IL-17RC as the receptor for IL-17F. J Immunol 2007; 179: 5462-5473.
24. Rickel EA, Siegel LA, Yoon BR, Rottman JB, Kugler DG, Swart DA et al. Identification of functional roles for both IL-17RB and IL-17RA in mediating IL-25-induced activities. J Immunol 2008; 181: 4299-4310.
25. Song X, Zhu S, Shi P, Liu Y, Shi Y, Levin SD et al. IL-17RE is the functional receptor for IL-17C and mediates mucosal immunity to infection with intestinal pathogens. Nat Immunol 2011; 12: 1151-1158.
26. Ramirez-Carrozzi V, Sambandam A, Luis E, Lin Z, Jeet S, Lesch J et al. IL-17C regulates the innate immune function of epithelial cells in an autocrine manner. Nat Immunol 2011; 12: 1159-1166.
27. Chang SH, Reynolds JM, Pappu BP, Chen G, Martinez GJ, Dong C. Interleukin-17C promotes Th17 cell responses and autoimmune disease via interleukin-17 receptor E. Immunity 2011; 35: 611-621.
28. Lee J, Ho WH, Maruoka M, Corpuz RT, Baldwin DT, Foster JS et al. IL-17E, a novel proinflammatory ligand for the IL-17 receptor homolog IL-17Rh1. J Biol Chem 2001; 276: 1660-1664.
29. Shi Y, Ullrich SJ, Zhang J, Connolly K, Grzegorzewski KJ, Barber MC et al. A novel cytokine receptor-ligand pair. Identification, molecular characterization, and in vivo immunomodulatory activity. J Biol Chem 2000; 275: 19167-19176.
30. Ron D, Fuchs Y, Chorev DS. Know thy Sef: a novel class of feedback antagonists of receptor tyrosine kinase signaling. Int J Biochem Cell Biol 2008; 40: 2040-2052.
31. Rong Z, Wang A, Li Z, Ren Y, Cheng L, Li Y et al. IL-17RD (Sef or IL-17RLM) interacts with IL-17 receptor and mediates IL-17 signaling. Cell Res 2009; 19: 208-215.
32. Mellett M, Atzei P, Horgan A, Hams E, Floss T, Wurst W et al. Orphan receptor IL-17RD tunes IL-17A signalling and is required for neutrophilia. Nat Commun 2012; 3: 1119.
33. Mellett M, Atzei P, Bergin R, Horgan A, Floss T, Wurst W et al. Orphan receptor IL-17RD regulates Toll-like receptor signalling via SEFIR/TIR interactions. Nat Commun 2015; 6: 6669.
34. Hartupee J, Liu C, Novotny M, Li X, Hamilton T. IL-17 enhances chemokine gene expression through mRNA stabilization. J Immunol 2007; 179: 4135-4141.
35. Qian Y, Liu C, Hartupee J, Altuntas CZ, Gulen MF, Jane-Wit D et al. The adaptor Act1 is required for interleukin 17-dependent signaling associated with autoimmune and inflammatory disease. Nat Immunol 2007; 8: 247-256.
36. Chang SH, Park H, Dong C. Act1 adaptor protein is an immediate and essential signaling component of interleukin-17 receptor. J Biol Chem 2006; 281: 35603-35607.
37. Liu C, Qian W, Qian Y, Giltiay NV, Lu Y, Swaidani S et al. Act1, a U-box E3 ubiquitin ligase for IL-17 signaling. Sci Signal 2009; 2: ra63.
38. Hartupee J, Liu C, Novotny M, Sun D, Li X, Hamilton TA. IL-17 signaling for mRNA stabilization does not require TNF receptorassociated factor 6. J Immunol 2009; 182: 1660-1666.
39. Sun D, Novotny M, Bulek K, Liu C, Li X, Hamilton T. Treatment with IL-17 prolongs the half-life of chemokine CXCL1 mRNA via the adaptor TRAF5 and the splicing-regulatory factor SF2 (ASF). Nat Immunol 2011; 12: 853-860.
40. Bulek K, Liu C, Swaidani S, Wang L, Page RC, Gulen MF et al. The inducible kinase IKKi is required for IL-17-dependent signaling associated with neutrophilia and pulmonary inflammation. Nat Immunol 2011; 12: 844-852.
41. Herjan T, Yao P, Qian W, Li X, Liu C, Bulek K et al. HuR Is Required for IL-17-Induced Act1-Mediated CXCL1 and CXCL5 mRNA Stabilization. J Immunol 2013; 191: 640-649.
42. Wu L, Chen X, Zhao J, Martin B, Zepp JA, Ko JS et al. A novel IL-17 signaling pathway controlling keratinocyte proliferation and tumorigenesis via the TRAF4-ERK5 axis. J Exp Med 2015; 212: 1571-1587.
43. Wang C, Wu L, Bulek K, Martin BN, Zepp JA, Kang Z et al. The psoriasis-associated D10N variant of the adaptor Act1 with impaired regulation by the molecular chaperone hsp90. Nat Immunol 2013; 14: 72-81.
44. Zhu S, Pan W, Song X, Liu Y, Shao X, Tang Y et al. The microRNA miR-23b suppresses IL-17-associated autoimmune inflammation by targeting TAB2, TAB3 and IKK-alpha. Nat Med 2012; 18: 1077-1086.
45. Yang XO, Chang SH, Park H, Nurieva R, Shah B, Acero L et al. Regulation of inflammatory responses by IL-17F. J Exp Med 2008; 205: 1063-1075.
46. Shen F, Li N, Gade P, Kalvakolanu DV, Weibley T, Doble B et al. IL-17 receptor signaling inhibits C/EBPbeta by sequential phosphorylation of the regulatory 2 domain. Sci Signal 2009; 2: ra8.
47. Zhu S, Pan W, Shi P, Gao H, Zhao F, Song X et al. Modulation of experimental autoimmune encephalomyelitis through TRAF3-mediated suppression of interleukin 17 receptor signaling. J Exp Med 2010; 207: 2647-2662.
48. Zepp JA, Liu C, Qian W, Wu L, Gulen MF, Kang Z et al. Cutting edge: TNF receptor-associated factor 4 restricts IL-17-mediated pathology and signaling processes. J Immunol 2012; 189: 33-37.
49. Shi P, Zhu S, Lin Y, Liu Y, Liu Y, Chen Z et al. Persistent stimulation with interleukin-17 desensitizes cells through SCFbeta-TrCPmediated degradation of Act1. Sci Signal 2011; 4: ra73.
50. Qu F, Gao H, Zhu S, Shi P, Zhang Y, Liu Y et al. TRAF6 dependent Act1 phosphorylation by the IKK-related kinases suppresses IL-17-induced NF-kappaB activation.Mol Cell Biol 2012; 32: 3925-3937.
51. Zhong B, Liu X, Wang X, Chang SH, Liu X, Wang A et al. Negative regulation of IL-17-mediated signaling and inflammation by the ubiquitin-specific protease USP25. Nat Immunol 2012; 13: 1110-1117.
52. Garg AV, Ahmed M, Vallejo AN, Ma A, Gaffen SL. The deubiquitinase A20 mediates feedback inhibition of interleukin-17 receptor signaling. Sci Signal 2013; 6: 44.
53. Garg AV, Amatya N, Chen K, Cruz JA, Grover P, Whibley N et al. MCPIP1 endoribonuclease activity negatively regulates interleukin-17-mediated signaling and inflammation. Immunity 2015; 43: 475-487.
54. Claudio E, Sonder SU, Saret S, Carvalho G, Ramalingam TR, Wynn TA et al. The adaptor protein CIKS/Act1 is essential for IL-25-mediated allergic airway inflammation. J Immunol 2009; 182: 1617-1630.
55. Swaidani S, Bulek K, Kang Z, Gulen MF, Liu C, Yin W et al. T cell-derived Act1 is necessary for IL-25-mediated Th2 responses and allergic airway inflammation. J Immunol 2011; 187: 3155-3164.
56. Swaidani S, Bulek K, Kang Z, Liu C, Lu Y, Yin W et al. The critical role of epithelial-derived Act1 in IL-17-and IL-25-mediated pulmonary inflammation. J Immunol 2009; 182: 1631-1640.
57. Kang Z, Swaidani S, Yin W, Wang C, Barlow JL, Gulen MF et al. Epithelial cell-specific Act1 adaptor mediates interleukin-25-dependent helminth expulsion through expansion of Lin(-)c-Kit(+) innate cell population. Immunity 2012; 36: 821-833.
58. Maezawa Y, Nakajima H, Suzuki K, Tamachi T, Ikeda K, Inoue J et al. Involvement of TNF receptor-associated factor 6 in IL-25 receptor signaling. J Immunol 2006; 176: 1013-1018.
59. Zepp JA, Wu L, Qian W, Ouyang W, Aronica M, Erzurum S et al. TRAF4-SMURF2-mediated DAZAP2 degradation is critical for IL-25 signaling and allergic airway inflammation. J Immunol 2015; 194: 2826-2837.
60. Wu L, Zepp JA, Qian W, Martin BN, Ouyang W, Yin W et al. A novel IL-25 signaling pathway through STAT5. J Immunol 2015; 194: 4528-4534.
61. Yamaguchi Y, Fujio K, Shoda H, Okamoto A, Tsuno NH, Takahashi K et al. IL-17B and IL-17C are associated with TNF-alpha production and contribute to the exacerbation of inflammatory arthritis. J Immunol 2007; 179: 7128-7136.
62. Wu HH, Hwang-Verslues WW, Lee WH, Huang CK, Wei PC, Chen CL et al. Targeting IL-17B-IL-17RB signaling with an anti-IL-17RB antibody blocks pancreatic cancer metastasis by silencing multiple chemokines. J Exp Med 2015; 212: 333-349.
63. Huang CK, Yang CY, Jeng YM, Chen CL, Wu HH, Chang YC et al. Autocrine/paracrine mechanism of interleukin-17B receptor promotes breast tumorigenesis through NF-kappaB-mediated antiapoptotic pathway. Oncogene 2014; 33: 2968-2977.
64. Furuta S, Jeng YM, Zhou L, Huang L, Kuhn I, Bissell MJ et al. IL-25 causes apoptosis of IL-25R-expressing breast cancer cells without toxicity to nonmalignant cells. Sci Transl Med 2011; 3: 78-31.
65. Reynolds JM, Lee YH, Shi Y, Wang X, Angkasekwinai P, Nallaparaju KC et al. Interleukin-17B antagonizes interleukin-25-mediated mucosal inflammation. Immunity 2015; 42: 692-703.
66. Li H, Chen J, Huang A, Stinson J, Heldens S, Foster J et al. Cloning and characterization of IL-17B and IL-17C, two new members of the IL-17 cytokine family. Proc Natl Acad Sci USA 2000; 97: 773-778.
67. Hurst SD, Muchamuel T, Gorman DM, Gilbert JM, Clifford T, Kwan S et al. New IL-17 family members promote Th1 or Th2 responses in the lung: in vivo function of the novel cytokine IL-25. J Immunol 2002; 169: 443-453.
68. O'Sullivan T, Saddawi-Konefka R, Gross E, Tran M, Mayfield SP, Ikeda H et al. Interleukin-17D mediates tumor rejection through recruitment of natural killer cells. Cell Rep 2014; 7: 989-998.
69. Saddawi-Konefka R, O'Sullivan T, Gross ET, Washington Jr A, Bui JD. Tumor-expressed IL-17D recruits NK cells to reject tumors. Oncoimmunology 2014; 3: e954853.
70. Ye P, Rodriguez FH, Kanaly S, Stocking KL, Schurr J, Schwarzenberger P 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 2001; 194: 519-527.
71. Kudva A, Scheller EV, Robinson KM, Crowe CR, Choi SM, Slight SR et al. Influenza A inhibits Th17-mediated host defense against bacterial pneumonia in mice. J Immunol 2011; 186: 1666-1674.
72. Ishigame H, Kakuta S, Nagai T, Kadoki M, Nambu A, Komiyama Y et al. Differential roles of interleukin-17A and-17F in host defense against mucoepithelial bacterial infection and allergic responses. Immunity 2009; 30: 108-119.
73. Aujla SJ, Chan YR, Zheng M, Fei M, Askew DJ, Pociask DA et al. IL-22 mediates mucosal host defense against Gram-negative bacterial pneumonia. Nat Med 2008; 14: 275-281.
74. Ivanov II, Atarashi K, Manel N, Brodie EL, Shima T, Karaoz U et al. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell 2009; 139: 485-498.
75. Atarashi K, Tanoue T, Ando M, Kamada N, Nagano Y, Narushima S et al. Th17 cell induction by adhesion of microbes to intestinal epithelial cells. Cell 2015; 63: 367-380.
76. Trautwein-Weidner K, Gladiator A, Nur S, Diethelm P, LeibundGut-Landmann S. IL-17-mediated antifungal defense in the oral mucosa is independent of neutrophils. Mucosal Immunol 2015; 8: 221-231.
77. Saijo S, Ikeda S, Yamabe K, Kakuta S, Ishigame H, Akitsu A et al. Dectin-2 recognition of alpha-mannans and induction of Th17 cell differentiation is essential for host defense against Candida albicans. Immunity 2010; 32: 681-691.
78. Conti HR, Shen F, Nayyar N, Stocum E, Sun JN, Lindemann MJ et al. Th17 cells and IL-17 receptor signaling are essential for mucosal host defense against oral candidiasis. J Exp Med 2009; 206: 299-311.
79. Huang W, Na L, Fidel PL, Schwarzenberger P. Requirement of interleukin-17A for systemic anti-Candida albicans host defense in mice. J Infect Dis 2004; 190: 624-631.
80. Bar E, Whitney PG, Moor K, Reis e Sousa C, LeibundGut-Landmann S. IL-17 regulates systemic fungal immunity by controlling the functional competence of NK cells. Immunity 2014; 40: 117-127.
81. Taylor PR, Roy S, Leal Jr SM, Sun Y, Howell SJ, Cobb BA et al. Activation of neutrophils by autocrine IL-17A-IL-17RC interactions during fungal infection is regulated by IL-6, IL-23, RORgammat and dectin-2. Nat Immunol 2014; 15: 143-151.
82. Lin Y, Ritchea S, Logar A, Slight S, Messmer M, Rangel-Moreno J et al. Interleukin-17 is required for T helper 1 cell immunity and host resistance to the intracellular pathogen Francisella tularensis. Immunity 2009; 31: 799-810.
83. Khader SA, Pearl JE, Sakamoto K, Gilmartin L, Bell GK, Jelley-Gibbs DM 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-gamma responses if IL-12p70 is available. J Immunol 2005; 175: 788-795.
84. Umemura M, Yahagi A, Hamada S, Begum MD, Watanabe H, Kawakami K et al. IL-17-mediated regulation of innate and acquired immune response against pulmonary Mycobacterium bovis bacille Calmette-Guerin infection. J Immunol 2007; 178: 3786-3796.
85. Khader SA, Bell GK, Pearl JE, Fountain JJ, Rangel-Moreno J, Cilley GE et al. IL-23 and IL-17 in the establishment of protective pulmonary CD4+ T cell responses after vaccination and during Mycobacterium tuberculosis challenge. Nat Immunol 2007; 8: 369-377.
86. Fujino S, Andoh A, Bamba S, Ogawa A, Hata K, Araki Y et al. Increased expression of interleukin 17 in inflammatory bowel disease. Gut 2003; 52: 65-70.
87. Sugihara T, Kobori A, Imaeda H, Tsujikawa T, Amagase K, Takeuchi K et al. The increased mucosal mRNA expressions of complement C3 and interleukin-17 in inflammatory bowel disease. Clin Exp Immunol 2010; 160: 386-393.
88. Seiderer J, Elben I, Diegelmann J, Glas J, Stallhofer J, Tillack C 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.His161 Arg polymorphism in IBD. Inflamm Bowel Dis 2008; 14: 437-445.
89. Duerr RH, Taylor KD, Brant SR, Rioux JD, Silverberg MS, Daly MJ et al. A genome-wide association study identifies IL23R as an inflammatory bowel disease gene. Science 2006; 314: 1461-1463.
90. Barrett JC, Hansoul S, Nicolae DL, Cho JH, Duerr RH, Rioux JD et al. Genome-wide association defines more than 30 distinct susceptibility loci for Crohn's disease. Nat Genet 2008; 40: 955-962.
91. Wang K, Zhang H, Kugathasan S, Annese V, Bradfield JP, Russell RK et al. Diverse genome-wide association studies associate the IL12/IL23 pathway with Crohn Disease. Am J Hum Genet 2009; 84: 399-405.
92. Ciccacci C, Biancone L, Di Fusco D, Ranieri M, Condino G, Giardina E et al. TRAF3IP2 gene is associated with cutaneous extraintestinal manifestations in inflammatory bowel disease. J Crohns Colitis 2013; 7: 44-52.
93. 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.
94. Ito R, Kita M, Shin-Ya M, Kishida T, Urano A, Takada R et al. Involvement of IL-17A in the pathogenesis of DSS-induced colitis in mice. Biochem Biophys Res Commun 2008; 377: 12-16.
95. Song X, Dai D, He X, Zhu S, Yao Y, Gao H et al. Growth Factor FGF2 Cooperates with Interleukin-17 to Repair Intestinal Epithelial Damage. Immunity 2015; 43: 488-501.
96. Johansen C, Usher PA, Kjellerup RB, Lundsgaard D, Iversen L, Kragballe K. Characterization of the interleukin-17 isoforms and receptors in lesional psoriatic skin. The British journal of dermatology 2009; 160: 319-324.
97. Wilson NJ, Boniface K, Chan JR, McKenzie BS, Blumenschein WM, Mattson JD et al. Development, cytokine profile and function of human interleukin 17-producing helper T cells. Nat Immunol 2007; 8: 950-957.
98. Genetic Analysis of Psoriasis Cthe Wellcome Trust Case Control C, Strange A, Capon F, Spencer CC, Knight J et al. A genome-wide association study identifies new psoriasis susceptibility loci and an interaction between HLA-C and ERAP1. Nat Genet 2010; 42: 985-990.
99. Ellinghaus E, Ellinghaus D, Stuart PE, Nair RP, Debrus S, Raelson JV et al. Genome-wide association study identifies a psoriasis susceptibility locus at TRAF3IP2. Nat Genet 2010; 42: 991-995.
100. Cargill M, Schrodi SJ, Chang M, Garcia VE, Brandon R, Callis KP et al. A large-scale genetic association study confirms IL12B and leads to the identification of IL23R as psoriasis-risk genes. Am J Hum Genet 2007; 80: 273-290.
101. Rizzo HL, Kagami S, Phillips KG, Kurtz SE, Jacques SL, Blauvelt A. IL-23-mediated psoriasis-like epidermal hyperplasia is dependent on IL-17A. J Immunol 2011; 186: 1495-1502.
102. Cai Y, Shen X, Ding C, Qi C, Li K, Li X et al. Pivotal role of dermal IL-17-producing gammadelta T cells in skin inflammation. Immunity 2011; 35: 596-610.
103. van der Fits L, Mourits S, Voerman JS, Kant M, Boon L, Laman JD et al. Imiquimod-induced psoriasis-like skin inflammation in mice is mediated via the IL-23/IL-17 axis. J Immunol 2009; 182: 5836-5845.
104. El Malki K, Karbach SH, Huppert J, Zayoud M, Reissig S, Schuler R et al. An alternative pathway of imiquimod-induced psoriasis-like skin inflammation in the absence of interleukin-17 receptor a signaling. J Invest Dermatol 2013; 133: 441-451.
105. Ha HL, Wang H, Pisitkun P, Kim JC, Tassi I, Tang W et al. IL-17 drives psoriatic inflammation via distinct, target cell-specific mechanisms. Proc Natl Acad Sci USA 2014; 111: E3422-E3431.
106. Nakajima K, Kanda T, Takaishi M, Shiga T, Miyoshi K, Nakajima H et al. Distinct roles of IL-23 and IL-17 in the development of psoriasis-like lesions in a mouse model. J Immunol 2011; 186: 4481-4489.
107. Liang SC, Tan XY, Luxenberg DP, Karim R, Dunussi-Joannopoulos K, Collins M et al. Interleukin (IL)-22 and IL-17 are coexpressed by Th17 cells and cooperatively enhance expression of antimicrobial peptides. J Exp Med 2006; 203: 2271-2279.
108. Teunissen MB, Koomen CW, de Waal Malefyt R, Wierenga EA, Bos JD. Interleukin-17 and interferon-gamma synergize in the enhancement of proinflammatory cytokine production by human keratinocytes. J Invest Dermatol 1998; 111: 645-649.
109. Chiricozzi A, Guttman-Yassky E, Suarez-Farinas M, Nograles KE, Tian S, Cardinale I et al. Integrative responses to IL-17 and TNF-alpha in human keratinocytes account for key inflammatory pathogenic circuits in psoriasis. J Invest Dermatol 2011; 131: 677-687.
110. Gaffen SL, Jain R, Garg AV, Cua DJ. The IL-23-IL-17 immune axis: from mechanisms to therapeutic testing. Nat Rev Immunol 2014; 14: 585-600.
111. Molet S, Hamid Q, Davoine F, Nutku E, Taha R, Page N et al. IL-17 is increased in asthmatic airways and induces human bronchial fibroblasts to produce cytokines. The Journal of allergy and Clin Immunol 2001; 108: 430-438.
112. Doe C, Bafadhel M, Siddiqui S, Desai D, Mistry V, Rugman P et al. Expression of the T helper 17-associated cytokines IL-17A and IL-17F in asthma and COPD. Chest 2010; 138: 1140-1147.
113. Al-Ramli W, Prefontaine D, Chouiali F, Martin JG, Olivenstein R, Lemiere C et al. T(H)17-associated cytokines (IL-17A and IL-17F) in severe asthma. The Journal of allergy and Clin Immunol 2009; 123: 1185-1187.
114. McKinley L, Alcorn JF, Peterson A, Dupont RB, Kapadia S, Logar A et al. TH17 cells mediate steroid-resistant airway inflammation and airway hyperresponsiveness in mice. J Immunol 2008; 181: 4089-4097.
115. Nakae S, Komiyama Y, Nambu A, Sudo K, Iwase M, Homma I et al. Antigen-specific T cell sensitization is impaired in IL-17-deficient mice, causing suppression of allergic cellular and humoral responses. Immunity 2002; 17: 375-387.
116. Lajoie S, Lewkowich IP, Suzuki Y, Clark JR, Sproles AA, Dienger K et al. Complement-mediated regulation of the IL-17A axis is a central genetic determinant of the severity of experimental allergic asthma. Nat Immunol 2010; 11: 928-935.
117. Guo C, Chen G, Ge R. IL-23, rather than IL-17, is crucial for the development of ovalbumin-induced allergic rhinitis. Molecular immunology. 201567(2 Pt B)436-443.
118. Huang F, Kao CY, Wachi S, Thai P, Ryu J, Wu R. Requirement for both JAK-mediated PI3K signaling and ACT1/TRAF6/TAK1-dependent NF-kappaB activation by IL-17A in enhancing cytokine expression in human airway epithelial cells. J Immunol 2007; 179: 6504-6513.
119. Kao CY, Huang F, Chen Y, Thai P, Wachi S, Kim C et al. Up-regulation of CC chemokine ligand 20 expression in human airway epithelium by IL-17 through a JAK-independent but MEK/NF-kappaB-dependent signaling pathway. J Immunol 2005; 175: 6676-6685.
120. Kao CY, Chen Y, Thai P, Wachi S, Huang F, Kim C et al. IL-17 markedly up-regulates beta-defensin-2 expression in human airway epithelium via JAK and NF-kappaB signaling pathways. J Immunol 2004; 173: 3482-3491.
121. Wiehler S, Proud D. Interleukin-17A modulates human airway epithelial responses to human rhinovirus infection. American journal of physiology Lung cellular and molecular physiology 2007; 293: L505-L515.
122. Mori K, Fujisawa T, Kusagaya H, Yamanaka K, Hashimoto D, Enomoto N et al. Synergistic Proinflammatory Responses by IL-17A and Toll-Like Receptor 3 in Human Airway Epithelial Cells. PLoS ONE 2015; 10: e0139491.
123. Zijlstra GJ, Ten Hacken NH, Hoffmann RF, van Oosterhout AJ, Heijink IH. Interleukin-17A induces glucocorticoid insensitivity in human bronchial epithelial cells. The European respiratory journal 2012; 39: 439-445.
124. Kudo M, Melton AC, Chen C, Engler MB, Huang KE, Ren X et al. IL-17A produced by alphabeta T cells drives airway hyper-responsiveness in mice and enhances mouse and human airway smooth muscle contraction. Nat Med 2012; 18: 547-554.
125. Fujisawa T, Velichko S, Thai P, Hung LY, Huang F, Wu R. Regulation of airway MUC5AC expression by IL-1beta and IL-17A; the NF-kappaB paradigm. J Immunol 2009; 183: 6236-6243.
126. Fujisawa T, Chang MM, Velichko S, Thai P, Hung LY, Huang F et al. NF-kappaB mediates IL-1beta-and IL-17A-induced MUC5B expression in airway epithelial cells. Am J Respir Cell Mol Biol 2011; 45: 246-252.
127. Chae WJ, Gibson TF, Zelterman D, Hao L, Henegariu O, Bothwell AL. Ablation of IL-17A abrogates progression of spontaneous intestinal tumorigenesis. Proc Natl Acad Sci USA 2010; 107: 5540-5544.
128. Hyun YS, Han DS, Lee AR, Eun CS, Youn J, Kim HY. Role of IL-17A in the development of colitis-associated cancer. Carcinogenesis 2012; 33: 931-936.
129. Grivennikov SI, Wang K, Mucida D, Stewart CA, Schnabl B, Jauch D et al. Adenoma-linked barrier defects and microbial products drive IL-23/IL-17-mediated tumour growth. Nature 2012; 491: 254-258.
130. Wu S, Rhee KJ, Albesiano E, Rabizadeh S, Wu X, Yen HR et al. A human colonic commensal promotes colon tumorigenesis via activation of T helper type 17T cell responses. Nat Med 2009; 15: 1016-1022.
131. Wang K, Kim MK, Di Caro G, Wong J, Shalapour S, Wan J et al. Interleukin-17 receptor a signaling in transformed enterocytes promotes early colorectal tumorigenesis. Immunity 2014; 41: 1052-1063.
132. Wang L, Yi T, Zhang W, Pardoll DM, Yu H. IL-17 enhances tumor development in carcinogen-induced skin cancer. Cancer Res. 2010; 70: 10112-10120.
133. Langowski JL, Zhang X, Wu L, Mattson JD, Chen T, Smith K et al. IL-23 promotes tumour incidence and growth. Nature 2006; 442: 461-465.
134. He D, Li H, Yusuf N, Elmets CA, Athar M, Katiyar SK et al. IL-17 mediated inflammation promotes tumor growth and progression in the skin. PLoS ONE 2012; 7: e32126.
135. Chang SH, Mirabolfathinejad SG, Katta H, Cumpian AM, Gong L, Caetano MS et al. T helper 17 cells play a critical pathogenic role in lung cancer. Proc Natl Acad Sci USA 2014; 111: 5664-5669.
136. Chae WJ, Bothwell AL. IL-17F deficiency inhibits small intestinal tumorigenesis in ApcMin/+ mice. Biochem Biophys Res Commun 2011; 414: 31-36.
137. Tong Z, Yang XO, Yan H, Liu W, Niu X, Shi Y et al. A protective role by interleukin-17F in colon tumorigenesis. PLoS ONE 2012; 7: e34959.
138. Fallon PG, Ballantyne SJ, Mangan NE, Barlow JL, Dasvarma A, Hewett DR et al. Identification of an interleukin (IL)-25-dependent cell population that provides IL-4, IL-5, and IL-13 at the onset of helminth expulsion. J Exp Med 2006; 203: 1105-1116.
139. Zhao A, Urban Jr JF, Sun R, Stiltz J, Morimoto M, Notari L et al. Critical role of IL-25 in nematode infection-induced alterations in intestinal function. J Immunol 2010; 185: 6921-6929.
140. Owyang AM, Zaph C, Wilson EH, Guild KJ, McClanahan T, Miller HR et al. Interleukin 25 regulates type 2 cytokine-dependent immunity and limits chronic inflammation in the gastrointestinal tract. J Exp Med 2006; 203: 843-849.
141. Su J, Chen T, Ji XY, Liu C, Yadav PK, Wu R et al. IL-25 downregulates Th1/Th17 immune response in an IL-10-dependent manner in inflammatory bowel disease. Inflamm Bowel Dis. 2013 Mar-Apr 19: 720-728.
142. McHenga SS, Wang D, Janneh FM, Feng Y, Zhang P, Li Z et al. Differential dose effects of recombinant IL-25 on the development of dextran sulfate sodium-induced colitis. Inflamm Res 2010; 59: 879-887.
143. McHenga SS, Wang D, Li C, Shan F, Lu C. Inhibitory effect of recombinant IL-25 on the development of dextran sulfate sodiuminduced experimental colitis in mice. Cell Mol Immunol 2008; 5: 425-431.
144. Caruso R, Sarra M, Stolfi C, Rizzo A, Fina D, Fantini MC et al. Interleukin-25 inhibits interleukin-12 production and Th1 celldriven inflammation in the gut. Gastroenterology 2009; 136: 2270-2279.
145. Rizzo A, Monteleone I, Fina D, Stolfi C, Caruso R, Fantini MC et al. Inhibition of colitis by IL-25 associates with induction of alternatively activated macrophages. Inflamm Bowel Dis 2012; 18: 449-459.
146. Wang AJ, Smith A, Li Y, Urban Jr JF, Ramalingam TR, Wynn TA et al. Genetic deletion of IL-25 (IL-17E) confers resistance to dextran sulfate sodium-induced colitis in mice. Cell & bioscience 2014; 4: 72.
147. Camelo A, Barlow JL, Drynan LF, Neill DR, Ballantyne SJ, Wong SH et al. Blocking IL-25 signalling protects against gut inflammation in a type-2 model of colitis by suppressing nuocyte and NKT derived IL-13. Journal of gastroenterology 2012; 47: 1198-1211.
148. Xu G, Zhang L, Wang DY, Xu R, Liu Z, Han DM et al. Opposing roles of IL-17A and IL-25 in the regulation of TSLP production in human nasal epithelial cells. Allergy 2010; 65: 581-589.
149. Corrigan CJ, Wang W, Meng Q, Fang C, Eid G, Caballero MR et al. Allergen-induced expression of IL-25 and IL-25 receptor in atopic asthmatic airways and late-phase cutaneous responses. The Journal of allergy and Clin Immunol 2011; 128: 116-124.
150. Tamachi T, Maezawa Y, Ikeda K, Kagami S, Hatano M, Seto Y et al. IL-25 enhances allergic airway inflammation by amplifying a TH2 cell-dependent pathway in mice. The Journal of allergy and Clin Immunol 2006; 118: 606-614.
151. Angkasekwinai P, Park H, Wang YH, Wang YH, Chang SH, Corry DB et al. Interleukin 25 promotes the initiation of proallergic type 2 responses. J Exp Med 2007; 204: 1509-1517.
152. Ballantyne SJ, Barlow JL, Jolin HE, Nath P, Williams AS, Chung KF et al. Blocking IL-25 prevents airway hyperresponsiveness in allergic asthma. The Journal of allergy and Clin Immunol 2007; 120: 1324-1331.
153. Angkasekwinai P, Chang SH, Thapa M, Watarai H, Dong C. Regulation of IL-9 expression by IL-25 signaling. Nat Immunol 2010; 11: 250-256.
154. Petersen BC, Budelsky AL, Baptist AP, Schaller MA, Lukacs NW. Interleukin-25 induces type 2 cytokine production in a steroidresistant interleukin-17RB+ myeloid population that exacerbates asthmatic pathology. Nat Med 2012; 18: 751-758.
155. Sharkhuu T, Matthaei KI, Forbes E, Mahalingam S, Hogan SP, Hansbro PM et al. Mechanism of interleukin-25 (IL-17E)-induced pulmonary inflammation and airways hyper-reactivity. Clinical and experimental allergy: journal of the British Society for Allergy and Clin Immunol 2006; 36: 1575-1583.
156. Kawashima S, Hirose K, Takahashi K, Tamachi T, Ikeda K, Tokoyoda K et al. Interleukin-25 induces pulmonary arterial remodeling via natural killer T cell-dependent mechanisms. International archives of allergy and immunology 2013; 161 (Suppl 2): 118-124.
157. Corrigan CJ, Wang W, Meng Q, Fang C, Wu H, Reay V et al. T-helper cell type 2 (Th2) memory T cell-potentiating cytokine IL-25 has the potential to promote angiogenesis in asthma. Proc Natl Acad Sci USA 2011; 108: 1579-1584.
158. Gregory LG, Jones CP, Walker SA, Sawant D, Gowers KH, Campbell GA et al. IL-25 drives remodelling in allergic airways disease induced by house dust mite. Thorax 2013; 68: 82-90.
159. Van Maele L, Carnoy C, Cayet D, Songhet P, Dumoutier L, Ferrero I et al. TLR5 signaling stimulates the innate production of IL-17 and IL-22 by CD3(neg)CD127+ immune cells in spleen and mucosa. J Immunol 2010; 185: 1177-1185.
160. Wu Q, Martin RJ, Rino JG, Breed R, Torres RM, Chu HW. IL-23-dependent IL-17 production is essential in neutrophil recruitment and activity in mouse lung defense against respiratory Mycoplasma pneumoniae infection. Microbes and infection/Institut Pasteur 2007; 9: 78-86.
161. Huang J, Meng S, Hong S, Lin X, Jin W, Dong C. IL-17C is required for lethal inflammation during systemic fungal infection. Cell Mol Immunol; e-pub ahead of print 13 July 2015; doi:10.1038/cmi.2015.56.
162. Conti HR, Whibley N, Coleman BM, Garg AV, Jaycox JR, Gaffen SL. Signaling through IL-17C/IL-17RE is dispensable for immunity to systemic, oral and cutaneous candidiasis. PLoS ONE 2015; 10: e0122807.
163. Pfeifer P, Voss M, Wonnenberg B, Hellberg J, Seiler F, Lepper PM et al. IL-17C is a mediator of respiratory epithelial innate immune response. Am J Respir Cell Mol Biol 2013; 48: 415-421.
164. Holland DB, Bojar RA, Farrar MD, Holland KT. Differential innate immune responses of a living skin equivalent model colonized by Staphylococcus epidermidis or Staphylococcus aureus. FEMS Microbiol Lett 2009; 290: 149-155.
165. Song X, Gao H, Lin Y, Yao Y, Zhu S, Wang J et al. Alterations in the microbiota drive interleukin-17C production from intestinal epithelial cells to promote tumorigenesis. Immunity 2014; 40: 140-152.
166. Roth SA, Simanski M, Rademacher F, Schroder L, Harder J. The pattern recognition receptor NOD2 mediates Staphylococcus aureus-induced IL-17C expression in keratinocytes. J Invest Dermatol 2014; 134: 374-380.
167. Im E, Jung J, Rhee SH. Toll-like receptor 5 engagement induces interleukin-17C expression in intestinal epithelial cells. J Interferon Cytokine Res 2012; 32: 583-591.
168. Kusagaya H, Fujisawa T, Yamanaka K, Mori K, Hashimoto D, Enomoto N et al. Toll-like receptor-mediated airway IL-17C enhances epithelial host defense in an autocrine/paracrine manner. Am J Respir Cell Mol Biol 2014; 50: 30-39.
169. Johansen C, Riis JL, Gedebjerg A, Kragballe K, Iversen L. Tumor necrosis factor alpha-mediated induction of interleukin 17C in human keratinocytes is controlled by nuclear factor kappaB. J Biol Chem 2011; 286: 25487-25494.
170. Friedrich M, Diegelmann J, Schauber J, Auernhammer CJ, Brand S. Intestinal neuroendocrine cells and goblet cells are mediators of IL-17A-amplified epithelial IL-17C production in human inflammatory bowel disease. Mucosal Immunol 2015; 8: 943-958.
171. Zheng Y, Valdez PA, Danilenko DM, Hu Y, Sa SM, Gong Q et al. Interleukin-22 mediates early host defense against attaching and effacing bacterial pathogens. Nat Med 2008; 14: 282-289.
172. Reynolds JM, Martinez GJ, Nallaparaju KC, Chang SH, Wang YH, Dong C. Cutting edge: regulation of intestinal inflammation and barrier function by IL-17C. J Immunol 2012; 189: 4226-4230.