The IL-23/T17 pathogenic axis in psoriasis is amplified by keratinocyte responses

Trends in Immunology

Volumn 34, Issue 4, 2013, Pages 174-181

  Lowes, Michelle A ^a   Russell, Chris B ^b   Martin, David A ^b   Towne, Jennifer E ^b   Krueger, James G ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

^b AMGEN INC   (United States)

Author keywords

Anticytokine treatments; IL 23; Psoriasis; T cells; T17

Indexed keywords

ADALIMUMAB; APILIMOD; BETA DEFENSIN; BRIAKINUMAB; BRODALUMAB; CNTO 1959; CXCL2 CHEMOKINE; CYCLOSPORIN; CYTOKINE; ETANERCEPT; GAMMA INTERFERON; INFLIXIMAB; INTERLEUKIN 1; INTERLEUKIN 17; INTERLEUKIN 19; INTERLEUKIN 20; INTERLEUKIN 22; INTERLEUKIN 23; INTERLEUKIN 8; IXEKIZUMAB; LY 2525623; MACROPHAGE INFLAMMATORY PROTEIN 3ALPHA; MATRIX METALLOPROTEINASE; PROTEIN S 100; SCH 900222; SECUKINUMAB; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; UNINDEXED DRUG; USTEKINUMAB; VASCULOTROPIN;

CELL PROLIFERATION; CYTOKINE PRODUCTION; EPIDERMIS HYPERPLASIA; GENE MUTATION; HUMAN; KERATINOCYTE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PATHOGENESIS; PSORIASIS; REVIEW; ULTRAVIOLET B RADIATION;

ANIMALS; CARD SIGNALING ADAPTOR PROTEINS; EPIDERMIS; GENE-ENVIRONMENT INTERACTION; GUANYLATE CYCLASE; HUMANS; IMMUNITY, CELLULAR; INFLAMMATION MEDIATORS; INTERLEUKIN-17; INTERLEUKIN-23; KERATINOCYTES; MEMBRANE PROTEINS; MUTATION; PSORIASIS; RECEPTORS, INTERLEUKIN; TH17 CELLS;

EID: 84875864504     PISSN: 14714906     EISSN: 14714981     Source Type: Journal    
DOI: 10.1016/j.it.2012.11.005     Document Type: Review

References (99)

1. Lew W., et al. Psoriasis vulgaris: cutaneous lymphoid tissue supports T-cell activation and 'Type 1' inflammatory gene expression. Trends Immunol. 2004, 25:295-305.
2. Swindell W.R., et al. Heterogeneity of inflammatory and cytokine networks in chronic plaque psoriasis. PLoS ONE 2012, 7:e34594.
3. Suarez-Farinas M., et al. Expanding the psoriasis disease profile: interrogation of the skin and serum of patients with moderate-to-severe psoriasis. J. Invest. Dermatol. 2012, 132:2552-2564.
4. Tian S., et al. Meta-analysis derived (MAD) transcriptome of psoriasis defines the "core" pathogenesis of disease. PLoS ONE 2012, 7:e44274.
5. Johnson-Huang L.M., et al. Cytokine-producing dendritic cells in the pathogenesis of inflammatory skin diseases. J. Clin. Immunol. 2009, 29:247-256.
6. Zaba L.C., et al. Psoriasis is characterized by accumulation of immunostimulatory and Th1/Th17 cell-polarizing myeloid dendritic cells. J. Invest. Dermatol. 2009, 129:79-88.
7. Kennedy-Crispin M., et al. Human keratinocytes' response to injury upregulates CCL20 and other genes linking innate and adaptive immunity. J. Invest. Dermatol. 2012, 132:105-113.
8. Bromley S.K., et al. Orchestrating the orchestrators: chemokines in control of T cell traffic. Nat. Immunol. 2008, 9:970-980.
9. Charo I.F., Ransohoff R.M. The many roles of chemokines and chemokine receptors in inflammation. N. Engl. J. Med. 2006, 354:610-621.
10. Johnson-Huang L.M., et al. A single intradermal injection of IFN-gamma induces an inflammatory state in both non-lesional psoriatic and healthy skin. J. Invest. Dermatol. 2012, 132:1177-1187.
11. Johansen C., et al. 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.
12. Lowes M.A., et al. Increase in TNF-alpha and inducible nitric oxide synthase-expressing dendritic cells in psoriasis and reduction with efalizumab (anti-CD11a). Proc. Natl. Acad. Sci. U.S.A. 2005, 102:19057-19062.
13. Zaba L.C., et al. Resident and "inflammatory" dendritic cells in human skin. J. Invest. Dermatol. 2009, 129:302-308.
14. Summers deLuca L., Gommerman J.L. Fine-tuning of dendritic cell biology by the TNF superfamily. Nat. Rev. Immunol. 2012, 12:339-351.
15. Zaba L.C., et al. Amelioration of epidermal hyperplasia by TNF inhibition is associated with reduced Th17 responses. J. Exp. Med. 2007, 204:3183-3194.
16. Gray E.E., et al. Cutting edge: identification of a motile IL-17-producing gammadelta T cell population in the dermis. J. Immunol. 2011, 186:6091-6095.
17. Girardi M. Immunosurveillance and immunoregulation by gammadelta T cells. J. Invest. Dermatol. 2006, 126:25-31.
18. Korn T., Petermann F. Development and function of interleukin 17-producing gammadelta T cells. Ann. N. Y. Acad. Sci. 2012, 1247:34-45.
19. Cai Y., et al. Pivotal role of dermal IL-17-producing gammadelta T cells in skin inflammation. Immunity 2011, 35:596-610.
20. Laggner U., et al. Identification of a novel proinflammatory human skin-homing Vgamma9Vdelta2 T cell subset with a potential role in psoriasis. J. Immunol. 2011, 187:2783-2793.
21. Cai Y., et al. New insights of T cells in the pathogenesis of psoriasis. Cell. Mol. Immunol. 2012, 9:302-309.
22. van der Fits L., 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.
23. Van Belle A.B., et al. IL-22 is required for imiquimod-induced psoriasiform skin inflammation in mice. J. Immunol. 2012, 188:462-469.
24. Pantelyushin S., et al. Rorgammat+ innate lymphocytes and gammadelta T cells initiate psoriasiform plaque formation in mice. J. Clin. Invest. 2012, 122:2252-2256.
25. El Malki K., et al. An alternative pathway of imiquimod-induced psoriasis-like skin inflammation in the absence of interleukin-17 receptor A signaling. J. Invest. Dermatol. 2012, Epub 6 Sept.
26. Cherrier M., et al. Development and function of intestinal innate lymphoid cells. Curr. Opin. Immunol. 2012, 24:277-283.
27. Lin A.M., et al. Mast cells and neutrophils release IL-17 through extracellular trap formation in psoriasis. J. Immunol. 2011, 187:490-500.
28. Nograles K.E., et al. Th17 cytokines interleukin (IL)-17 and IL-22 modulate distinct inflammatory and keratinocyte-response pathways. Br. J. Dermatol. 2008, 159:1086-1091.
29. Ambrosi A., et al. IL-17: a new actor in IFN-driven systemic autoimmune diseases. Eur. J. Immunol. 2012, 42:2274-2284.
30. Onishi R.M., Gaffen S.L. Interleukin-17 and its target genes: mechanisms of interleukin-17 function in disease. Immunology 2010, 129:311-321.
31. Haider A.S., et al. Identification of cellular pathways of "type 1," Th17 T cells, and TNF- and inducible nitric oxide synthase-producing dendritic cells in autoimmune inflammation through pharmacogenomic study of cyclosporine A in psoriasis. J. Immunol. 2008, 180:1913-1920.
32. Johnson-Huang L.M., et al. Effective narrow-band UVB radiation therapy suppresses the IL-23/IL-17 axis in normalized psoriasis plaques. J. Invest. Dermatol. 2010, 130:2654-2663.
33. Zaba L.C., et al. Effective treatment of psoriasis with etanercept is linked to suppression of IL-17 signaling, not immediate response TNF genes. J. Allergy Clin. Immunol. 2009, 124. 1022-1030.e395.
34. Hueber W., et al. Effects of AIN457, a fully human antibody to interleukin-17A, on psoriasis, rheumatoid arthritis, and uveitis. Sci. Transl. Med. 2010, 2:52ra72.
35. Gaffen S.L. Structure and signalling in the IL-17 receptor family. Nat. Rev. Immunol. 2009, 9:556-567.
36. Genovese M.C., et al. LY2439821, a humanized anti-interleukin-17 monoclonal antibody, in the treatment of patients with rheumatoid arthritis: a phase I randomized, double-blind, placebo-controlled, proof-of-concept study. Arthritis Rheum. 2010, 62:929-939.
37. Leonardi C., et al. Anti-interleukin-17 monoclonal antibody ixekizumab in chronic plaque psoriasis. N. Engl. J. Med. 2012, 366:1190-1199.
38. Krueger J.G., et al. IL-17A is essential for cell activation and inflammatory gene circuits in subjects with psoriasis. J. Allergy Clin. Immunol. 2012, 130. 145-154.e9.
39. Papp K.A., et al. Brodalumab, an anti-interleukin-17-receptor antibody for psoriasis. N. Engl. J. Med. 2012, 366:1181-1189.
40. Papp K.A., et al. Anti-IL-17 receptor antibody AMG 827 leads to rapid clinical response in subjects with moderate to severe psoriasis: results from a phase I, randomized, placebo-controlled trial. J. Invest. Dermatol. 2012, 132:2466-2469.
41. Chiricozzi A., et al. Integrative responses to IL-17 and TNF-α in human keratinocytes account for key inflammatory pathogenic circuits in psoriasis. J. Invest. Dermatol. 2011, 131:677-687.
42. Wolk K., et al. The Th17 cytokine IL-22 induces IL-20 production in keratinocytes: a novel immunological cascade with potential relevance in psoriasis. Eur. J. Immunol. 2009, 39:3570-3581.
43. Zaba L.C., et al. Identification of TNF-related apoptosis-inducing ligand and other molecules that distinguish inflammatory from resident dendritic cells in patients with psoriasis. J. Allergy Clin. Immunol. 2010, 125. 1261-1268.e9.
44. Fuentes-Duculan J., et al. A subpopulation of CD163-positive macrophages is classically activated in psoriasis. J. Invest. Dermatol. 2010, 130:2412-2422.
45. Lee E., et al. Increased expression of interleukin 23 p19 and p40 in lesional skin of patients with psoriasis vulgaris. J. Exp. Med. 2004, 199:125-130.
46. Roberson E.D., Bowcock A.M. Psoriasis genetics: breaking the barrier. Trends Genet. 2010, 26:415-423.
47. Capon F., et al. Sequence variants in the genes for the interleukin-23 receptor (IL23R) and its ligand (IL12B) confer protection against psoriasis. Hum. Genet. 2007, 122:201-206.
48. Cargill M., 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.
49. Nair R.P., et al. Genome-wide scan reveals association of psoriasis with IL-23 and NF-kappaB pathways. Nat. Genet. 2009, 41:199-204.
50. Di Meglio P., et al. The IL23R R381Q gene variant protects against immune-mediated diseases by impairing IL-23-induced Th17 effector response in humans. PLoS ONE 2011, 6:e17160.
51. Leonardi C.L., et al. Efficacy and safety of ustekinumab, a human interleukin-12/23 monoclonal antibody, in patients with psoriasis: 76-week results from a randomised, double-blind, placebo-controlled trial (PHOENIX 1). Lancet 2008, 371:1665-1674.
52. Papp K.A., et al. Efficacy and safety of ustekinumab, a human interleukin-12/23 monoclonal antibody, in patients with psoriasis: 52-week results from a randomised, double-blind, placebo-controlled trial (PHOENIX 2). Lancet 2008, 371:1675-1684.
53. Gordon K.B., et al. A phase III, randomized, controlled trial of the fully human IL-12/23 mAb briakinumab in moderate-to-severe psoriasis. J. Invest. Dermatol. 2011, 132:304-314.
54. Gottlieb A.B., et al. Efficacy and safety of briakinumab vs. etanercept and placebo in patients with moderate to severe chronic plaque psoriasis. Br. J. Dermatol. 2011, 165:652-660.
55. Strober B.E., et al. Efficacy and safety results from a phase III, randomized controlled trial comparing the safety and efficacy of briakinumab with etanercept and placebo in patients with moderate to severe chronic plaque psoriasis. Br. J. Dermatol. 2011, 165:661-668.
56. Wada Y., et al. Apilimod inhibits the production of IL-12 and IL-23 and reduces dendritic cell infiltration in psoriasis. PLoS ONE 2012, 7:e35069.
57. Sofen H., et al. Results of a single ascending dose study to assess the safety and tolerability of CNTO 1959 following intravenous or subcutaneous administration in healthy subjects and in subjects with moderate to severe psoriasis. FC-21. Psoriasis: from Gene to Clinic 6th International Congress, 1-3 December 2011. Br. J. Dermatol. 2011, 165:e1-e46.
58. Austin L.M., et al. The majority of epidermal T cells in psoriasis vulgaris lesions can produce type 1 cytokines, interferon-gamma, interleukin-2, and tumor necrosis factor-alpha, defining TC1 (cytotoxic T lymphocyte) and TH1 effector populations: a type 1 differentiation bias is also measured in circulating blood T cells in psoriatic patients. J. Invest. Dermatol. 1999, 113:752-759.
59. Lew W., et al. Psoriasis genomics: analysis of proinflammatory (type 1) gene expression in large plaque (Western) and small plaque (Asian) psoriasis vulgaris. Br. J. Dermatol. 2004, 150:668-676.
60. Kryczek I., et al. Induction of IL-17+ T cell trafficking and development by IFN-gamma: mechanism and pathological relevance in psoriasis. J. Immunol. 2008, 181:4733-4741.
61. Yao Y., et al. Type I interferon: potential therapeutic target for psoriasis?. PLoS ONE 2008, 3:e2737.
62. Suárez-Fariñas M., et al. Evaluation of the psoriasis transcriptome across different studies by gene set enrichment analysis (GSEA). PLoS ONE 2010, 5:e10247.
63. Lowes M.A., et al. Pathogenesis and therapy of psoriasis. Nature 2007, 445:866-873.
64. Marrakchi S., et al. Interleukin-36-receptor antagonist deficiency and generalized pustular psoriasis. N. Engl. J. Med. 2011, 365:620-628.
65. Onoufriadis A., et al. Mutations in IL36RN/IL1F5 are associated with the severe episodic inflammatory skin disease known as generalized pustular psoriasis. Am. J. Hum. Genet. 2011, 89:432-437.
66. Sugiura K., et al. A novel IL36RN/IL1F5 homozygous nonsense mutation, p.Arg10X, in a Japanese patient with adult-onset generalized pustular psoriasis. Br. J. Dermatol. 2012, 167:699-701.
67. Johnston A., et al. IL-1F5, -F6 -F8, and -F9: a novel IL-1 family signaling system that is active in psoriasis and promotes keratinocyte antimicrobial peptide expression. J. Immunol. 2011, 186:2613-2622.
68. Muhr P., et al. Expression of interleukin (IL)-1 family members upon stimulation with IL-17 differs in keratinocytes derived from patients with psoriasis and healthy donors. Br. J. Dermatol. 2011, 165:189-193.
69. Blumberg H., et al. Opposing activities of two novel members of the IL-1 ligand family regulate skin inflammation. J. Exp. Med. 2007, 204:2603-2614.
70. Blumberg H., et al. IL-1RL2 and its ligands contribute to the cytokine network in psoriasis. J. Immunol. 2010, 185:4354-4362.
71. Towne J.E., et al. Interleukin-36 (IL-36) ligands require processing for full agonist (IL-36alpha, IL-36beta, and IL-36gamma) or antagonist (IL-36Ra) activity. J. Biol. Chem. 2011, 286:42594-42602.
72. Towne J., Sims J. IL-36 in psoriasis. Curr. Opin. Pharmacol. 2012, 12:486-490.
73. Jordan C.T., et al. Rare and common variants in CARD14, encoding an epidermal regulator of NF-kappaB, in psoriasis. Am. J. Hum. Genet. 2012, 90:796-808.
74. Jordan C.T., et al. PSORS2 is due to mutations in CARD14. Am. J. Hum. Genet. 2012, 90:784-795.
75. Morizane S., Gallo R.L. Antimicrobial peptides in the pathogenesis of psoriasis. J. Dermatol. 2012, 39:225-230.
76. Lande R., et al. Plasmacytoid dendritic cells sense self-DNA coupled with antimicrobial peptide. Nature 2007, 449:564-569.
77. Ganguly D., et al. Self-RNA-antimicrobial peptide complexes activate human dendritic cells through TLR7 and TLR8. J. Exp. Med. 2009, 206:1983-1994.
78. Dombrowski Y., et al. Cytosolic DNA triggers inflammasome activation in keratinocytes in psoriatic lesions. Sci. Transl. Med. 2011, 3:82ra38.
79. Dombrowski Y., Schauber J. Cathelicidin LL-37: a defense molecule with a potential role in psoriasis pathogenesis. Exp. Dermatol. 2012, 21:327-330.
80. Vogl T., et al. Mrp8 and Mrp14 are endogenous activators of Toll-like receptor 4, promoting lethal, endotoxin-induced shock. Nat. Med. 2007, 13:1042-1049.
81. Wolf R., et al. Chemotactic activity of S100A7 (Psoriasin) is mediated by the receptor for advanced glycation end products and potentiates inflammation with highly homologous but functionally distinct S100A15. J. Immunol. 2008, 181:1499-1506.
82. Yang D., et al. Beta-defensins: linking innate and adaptive immunity through dendritic and T cell CCR6. Science 1999, 286:525-528.
83. Gottlieb A.B., et al. Infliximab induction therapy for patients with severe plaque-type psoriasis: a randomized, double-blind, placebo-controlled trial. J. Am. Acad. Dermatol. 2004, 51:534-542.
84. Menter A., et al. A randomized comparison of continuous vs. intermittent infliximab maintenance regimens over 1 year in the treatment of moderate-to-severe plaque psoriasis. J. Am. Acad. Dermatol. 2007, 56. 31e31-15.
85. Reich K., et al. Infliximab induction and maintenance therapy for moderate-to-severe psoriasis: a phase III, multicentre, double-blind trial. Lancet 2005, 366:1367-1374.
86. Gordon K.B., et al. Clinical response to adalimumab treatment in patients with moderate to severe psoriasis: double-blind, randomized controlled trial and open-label extension study. J. Am. Acad. Dermatol. 2006, 55:598-606.
87. Menter A., et al. Adalimumab therapy for moderate to severe psoriasis: a randomized, controlled phase III trial. J. Am. Acad. Dermatol. 2008, 58:106-115.
88. Saurat J.H., et al. Efficacy and safety results from the randomized controlled comparative study of adalimumab vs. methotrexate vs. placebo in patients with psoriasis (CHAMPION). Br. J. Dermatol. 2008, 158:558-566.
89. Leonardi C.L., et al. Etanercept as monotherapy in patients with psoriasis. N. Engl. J. Med. 2003, 349:2014-2022.
90. Papp K.A., et al. A global phase III randomized controlled trial of etanercept in psoriasis: safety, efficacy, and effect of dose reduction. Br. J. Dermatol. 2005, 152:1304-1312.
91. Tyring S., et al. Etanercept and clinical outcomes, fatigue, and depression in psoriasis: double-blind placebo-controlled randomised phase III trial. Lancet 2006, 367:29-35.
92. Ribot J.C., et al. CD27 is a thymic determinant of the balance between interferon-gamma- and interleukin 17-producing gammadelta T cell subsets. Nat. Immunol. 2009, 10:427-436.
93. Azfar R.S., Gelfand J.M. Psoriasis and metabolic disease: epidemiology and pathophysiology. Curr. Opin. Rheumatol. 2008, 20:416-422.
94. Gelfand J.M., et al. Risk of myocardial infarction in patients with psoriasis. JAMA 2006, 296:1735-1741.
95. Mehta N.N., et al. Patients with severe psoriasis are at increased risk of cardiovascular mortality: cohort study using the General Practice Research Database. Eur. Heart J. 2010, 31:1000-1006.
96. Davidovici B.B., et al. Psoriasis and systemic inflammatory diseases: potential mechanistic links between skin disease and co-morbid conditions. J. Invest. Dermatol. 2010, 130:1785-1796.
97. Christophers E. Psoriasis - epidemiology and clinical spectrum. Clin. Exp. Dermatol. 2001, 26:314-320.
98. Cheng J., et al. Psoriasis increased the risk of diabetes: a meta-analysis. Arch. Dermatol. Res. 2012, 304:119-125.
99. Mehta N.N., et al. Systemic and vascular inflammation in patients with moderate to severe psoriasis as measured by [18F]-fluorodeoxyglucose positron emission tomography-computed tomography (FDG-PET/CT): a pilot study. Arch. Dermatol. 2011, 147:1031-1039.