The IL23R A/Gln381 allele promotes IL-23 unresponsiveness in human memory T-helper 17 cells and impairs Th17 responses in psoriasis patients

Journal of Investigative Dermatology

Volumn 133, Issue 10, 2013, Pages 2381-2389

  Di Meglio, Paola ^a,c   Villanova, Federica ^a   Napolitano, Luca ^a   Tosi, Isabella ^a   Terranova Barberio, Manuela ^a   Mak, Rose K ^a   Nutland, Sarah ^b   Smith, Catherine H ^a   Barker, Jonathan N W N ^a   Todd, John A ^b   Nestle, Frank O ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^c NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 17; INTERLEUKIN 17F; INTERLEUKIN 22; INTERLEUKIN 23; INTERLEUKIN 23 RECEPTOR; INTERLEUKIN 23P19; IL23R PROTEIN, HUMAN; INTERLEUKIN RECEPTOR;

ADULT; AGED; ALLELE; ARTICLE; CD4+ T LYMPHOCYTE; CELL EXPANSION; CYTOKINE RELEASE; DIFFERENTIATION; DISEASE SEVERITY; FEMALE; GENETIC ASSOCIATION; GENOTYPE; HUMAN; MAJOR CLINICAL STUDY; MALE; MEMORY T LYMPHOCYTE; PATHOGENICITY; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PSORIASIS; PSORIASIS AREA AND SEVERITY INDEX; SURVIVAL; TH17 CELL; GENETICS; HETEROZYGOTE; HOMOZYGOTE; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; METABOLISM; MIDDLE AGED; SINGLE NUCLEOTIDE POLYMORPHISM; YOUNG ADULT;

ADULT; AGED; ALLELES; FEMALE; HETEROZYGOTE; HOMOZYGOTE; HUMANS; IMMUNOLOGIC MEMORY; INTERLEUKIN-23; MALE; MIDDLE AGED; POLYMORPHISM, SINGLE NUCLEOTIDE; PSORIASIS; RECEPTORS, INTERLEUKIN; TH17 CELLS; YOUNG ADULT;

EID: 84884287706     PISSN: 0022202X     EISSN: 15231747     Source Type: Journal    
DOI: 10.1038/jid.2013.170     Document Type: Article

References (40)

1. Bergboer JG, Oostveen AM, de Jager ME et al. (2012) Paediatric-onset psoriasis is associated with ERAP1 and IL23R loci, LCE3C-LCE3B deletion and HLA-C*06. Br J Dermatol 167: 922-5
2. Boniface K, Blumenschein WM, Brovont-Porth K et al. (2010) Human Th17 cells comprise heterogeneous subsets including IFN-gamma-producing cells with distinct properties from the Th1 lineage. J Immunol 185: 679-87
3. Capon F, Di Meglio P, Szaub J et al. (2007) Sequence variants in the genes for the interleukin-23 receptor (IL23R) and its ligand (IL12B) confer protection against psoriasis. Hum Genet 122: 201-6
4. Cargill M, Schrodi SJ, Chang M et al. (2007) A large-scale genetic association study confirms IL12B and leads to the identification of IL23R as psoriasisrisk genes. Am J Hum Genet 80: 273-90
5. Carvalho A, Cunha C, Di Ianni M et al. (2010) Prognostic significance of genetic variants in the IL-23/Th17 pathway for the outcome of T celldepleted allogeneic stem cell transplantation. Bone Marrow Transplant 45: 1645-52
6. Chan JR, Blumenschein W, Murphy E et al. (2006) IL-23 stimulates epidermal hyperplasia via TNF and IL-20R2-dependent mechanisms with implications for psoriasis pathogenesis. J Exp Med 203: 2577-87
7. Clark L, Lebwohl M (2008) The effect of weight on the efficacy of biologic therapy in patients with psoriasis. J Am Acad Dermatol 58: 443-6
8. de Beaucoudrey L, Puel A, Filipe-Santos O et al. (2008) Mutations in STAT3 and IL12RB1 impair the development of human IL-17-producing T cells. J Exp Med 205: 1543-50
9. Di Cesare A, Di Meglio P, Nestle FO (2009) The IL-23/Th17 axis in the immunopathogenesis of psoriasis. J Invest Dermatol 129: 1339-50
10. Di Meglio P, Di Cesare A, Laggner U et al. (2011) The IL23R R381Q gene variant protects against immune-mediated diseases by impairing IL-23-induced Th17 effector response in humans. PLoS ONE 6:e17160
11. Duerr RH, Taylor KD, Brant SR et al. (2006) A genome-wide association study identifies IL23R as an inflammatory bowel disease gene. Science 314: 1461-3
12. Elder JT, Bruce AT, Gudjonsson JE et al. (2010) Molecular dissection of psoriasis: integrating genetics and biology. J Invest Dermatol 130: 1213-26
13. Fitch E, Harper E, Skorcheva I et al. (2007) Pathophysiology of psoriasis: recent advances on IL-23 and Th17 cytokines. Curr Rheumatol Rep 9: 461-7
14. Gottlieb AB, Chamian F, Masud S et al. (2005) TNF inhibition rapidly downregulates multiple proinflammatory pathways in psoriasis plaques. J Immunol 175: 2721-9
15. Griffiths CE, Strober BE, van de Kerkhof P et al. (2010) Comparison of ustekinumab and etanercept for moderate-to-severe psoriasis. N Engl J Med 362: 118-28
16. Guttman-Yassky E, Nograles KE, Krueger JG (2011) Contrasting pathogenesis of atopic dermatitis and psoriasis-part II: immune cell subsets and therapeutic concepts. J Allergy Clin Immunol 127: 1420-32
17. Hernandez-Santos N, Gaffen SL (2012) Th17 cells in immunity to Candida albicans. Cell Host Microbe 11: 425-35
18. Hueber W, Patel DD, Dryja T et al. (2010) Effects of AIN457, a fully human antibody to interleukin-17A, on psoriasis, rheumatoid arthritis, and uveitis. Sci Transl Med 2:52ra72
19. Kagami S, Rizzo HL, Lee JJ et al. (2010) Circulating Th17, Th22, and Th1 cells are increased in psoriasis. J Invest Dermatol 130: 1373-83
20. Leonardi C, Matheson R, Zachariae C et al. (2012) Anti-interleukin-17 monoclonal antibody ixekizumab in chronic plaque psoriasis. N Engl J Med 366: 1190-9
21. Lowes MA, Kikuchi T, Fuentes-Duculan J et al. (2008) Psoriasis vulgaris lesions contain discrete populations of Th1 and Th17 T cells. J Invest Dermatol 128: 1207-1
22. McGeachy MJ, Chen Y, Tato CM et al. (2009) The interleukin 23 receptor is essential for the terminal differentiation of interleukin 17-producing effector T helper cells in vivo. Nat Immunol 10: 314-24
23. Miller LS, Cho JS (2011) Immunity against Staphylococcus aureus cutaneous infections. Nat Rev Immunol 11: 505-18
24. Miossec P, Korn T, Kuchroo VK (2009) Interleukin-17 and type 17 helper T cells. N Engl J Med 361: 888-98
25. Nair RP, Duffin KC, Helms C et al. (2009) Genome-wide scan reveals association of psoriasis with IL-23 and NF-kappaB pathways. Nat Genet 41: 199-204
26. Nestle FO, Kaplan DH, Barker J (2009) Psoriasis. N Engl J Med 361: 496-509
27. Papp KA, Griffiths CE, Gordon K et al. (2013) Long-term safety of ustekinumab in patients with moderate-to-severe psoriasis: final results from five years of follow-up. Br J Dermatol 168: 844-54
28. Papp KA, Leonardi C, Menter A et al. (2012) Brodalumab, an anti-interleukin- 17-receptor antibody for psoriasis. N Engl J Med 366: 1181-9
29. Perera GK, Di Meglio P, Nestle FO (2012) Psoriasis. Annu Rev Pathol 7: 385-422
30. Pidasheva S, Trifari S, Phillips A et al. (2011) Functional studies on the IBD susceptibility gene IL23R implicate reduced receptor function in the protective genetic variant R381Q. PLoS ONE 6:e25038
31. Puel A, Cypowyj S, Bustamante J et al. (2011) Chronic mucocutaneous candidiasis in humans with inborn errors of interleukin-17 immunity. Science 332: 65-8
32. Rizzo HL, Kagami S, Phillips KG et al. (2011) IL-23-mediated psoriasis-like epidermal hyperplasia is dependent on IL-17A. J Immunol 186: 1495-502
33. Rueda B, Orozco G, Raya E et al. (2008) The IL23R Arg381Gln non-synonymous polymorphism confers susceptibility to ankylosing spondylitis. Ann Rheum Dis 67: 1451-4
34. Sarin R,Wu X, Abraham C (2011) Inflammatory disease protective R381Q IL23 receptor polymorphism results in decreased primary CD4+ and CD8+ human T-cell functional responses. Proc Natl Acad Sci USA 108: 9560-5
35. Tonel G, Conrad C, Laggner U et al. (2010) Cutting edge: A critical functional role for IL-23 in psoriasis. J Immunol 185: 5688-91
36. Tsoi LC, Spain SL, Knight J et al. (2012) Identification of 15 new psoriasis susceptibility loci highlights the role of innate immunity. Nat Genet 44: 1341-8
37. van der Fits L, Mourits S, Voerman JS et al. (2009) Imiquimod-induced psoriasis-like skin inflammation in mice is mediated via the IL-23/IL-17 axis. J Immunol 182: 5836-45
38. Volpe E, Touzot M, Servant N et al. (2009) Multiparametric analysis of cytokine-driven human Th17 differentiation reveals a differential regulation of IL-17 and IL-22 production. Blood 114: 3610-4
39. Wilson NJ, Boniface K, Chan JR et al. (2007) Development, cytokine profile and function of human interleukin 17-producing helper T cells. Nat Immunol 8: 950-7
40. Zaba LC, Cardinale I, Gilleaudeau P et al. (2007) Amelioration of epidermal hyperplasia by TNF inhibition is associated with reduced Th17 responses. J Exp Med 204: 3183-94