The interleukin (IL)-23/IL-17 axis in ankylosing spondylitis: New advances and potentials for treatment

Clinical and Experimental Immunology

Volumn 183, Issue 1, 2016, Pages 30-36

  Jethwa, H ^a   Bowness, P ^a,b  

^a OXFORD UNIVERSITY HOSPITALS NHS FOUNDATION TRUST   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Ankylosing spondylitis; Th17; Treatment

Indexed keywords

ADALIMUMAB; BRIAKINUMAB; BRODALUMAB; ETANERCEPT; GOLIMUMAB; GUSELKUMAB; HLA B27 ANTIGEN; INFLIXIMAB; INTERLEUKIN 17; INTERLEUKIN 23; IXEKIZUMAB; NONSTEROID ANTIINFLAMMATORY AGENT; PERAKIZUMAB; SECUKINUMAB; TILDRAKIZUMAB; TUMOR NECROSIS FACTOR INHIBITOR; USTEKINUMAB;

ANKYLOSING SPONDYLITIS; ARTICLE; DRUG TARGETING; HUMAN; IMMUNE RESPONSE; INFLAMMATORY DISEASE; PATHOGENESIS; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL (TOPIC); TH17 CELL; ANIMAL; GENETICS; IMMUNOLOGY; IMMUNOTHERAPY; METABOLISM; MOLECULARLY TARGETED THERAPY; SIGNAL TRANSDUCTION; SPONDYLITIS, ANKYLOSING;

ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; HLA-B27 ANTIGEN; HUMANS; IMMUNOTHERAPY; INTERLEUKIN-17; INTERLEUKIN-23; MOLECULAR TARGETED THERAPY; SIGNAL TRANSDUCTION; SPONDYLITIS, ANKYLOSING;

EID: 84955372991     PISSN: 00099104     EISSN: 13652249     Source Type: Journal    
DOI: 10.1111/cei.12670     Document Type: Article

References (49)

1. McGonagle D. A proposed classification of the immunological diseases. PLOS Med 2006; 3:e297.
2. Brown MA, Kennedy LG, MacGregor AJ et al. Susceptibility to ankylosing spondylitis in twins: the role of genes, HLA and the environment. Arthritis Rheumatol 2007; 40:1823-8.
3. Evans DM, Spencer CCA, Pointon JJ et al. Interaction between ERAP1 and HLA-B27 in ankylosing spondylitis implicates peptide handling in the mechanism for HLA-B27 in disease susceptibility. Nat Genet 2011; 43:761-7.
4. Costello ME, Elewant D, Kenna JJ, Brown MA. Microbiomes, the gut and ankylosing spondylitis. Arthritis Res Ther 2013; 15:214.
5. Bettelli E, Korn T, Kuchroo VK. Th17: the third member of the effector T cell trilogy. Curr Opin Immunol 2007; 19:652-7.
6. Dong C. TH17 cells in development: an updated view of their molecular identity and genetic programming. Nat Rev Immunol 2008; 8:337-48.
7. 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.
8. 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.
9. Piper C, Pesenacker AM, Bending D et al. T cell expression of granulocyte-macrophage colony-stimulating factor in juvenile arthritis is contingent upon Th17 plasticity. Arthritis Rheumatol 2014; 66:1955-60.
10. 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.
11. 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.
12. - entheseal resident T cells. Nat Med 2012; 18:1069-76.
13. Hue S, Ahern P, Buonocore S et al. Interleukin-23 drives innate and T cell-mediated intestinal inflammation. J Exp Med 2006; 203:2473-83.
14. Di Meglio P, Nestle FO. The role of IL-23 in the immunopathogenesis of psoriasis. F1000 Biol Rep 2010; 2:40.
15. Cua DJ, Sherlock J, Chen Y et al. Interleukin-23 rather than interleukin-12 is the critical cytokine for autoimmune inflammation of the brain. Nature 2003; 421:744-8.
16. Veldhoen M, Hocking RJ, Atkins CJ, Locksley RM, Stockinger B. TGFbeta in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells. Immunity 2006; 24:179-89.
17. Ye P, Rodriguez FH, Kanaly S 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; 194:519-27.
18. Zielinski CE, Mele F, Aschenbrenner D et al. Pathogen-induced human Th17 cells produce IFN-γ or IL-10 are regulated by IL-1β. Nature 2012; 484:514-8.
19. Chen Y, Langrish CL, McKenzie B et al. Anti-IL-23 therapy inhibits multiple inflammatory pathways and ameliorates autoimmune encephalomyelitis. J Clin Invest 2006; 116:1317-26.
20. 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.
21. Iwakura Y, Ishigame H. The IL-23/IL-17 axis in inflammation. J Clin Invest 2006; 116:1218-22.
22. Blauvelt A. T-helper 17 cells in psoriatic plaques and additional genetic links between IL-23 and psoriasis. J Invest Dermatol 2008; 128:1064-7.
23. Chan JR, Blumenschein W, Murphy E et al. IL-23 stimulates epidermal hyperplasia via TNF and IL-20R2-dependent mechanisms with implications for psoriasis pathogenesis. J Exp Med 2006; 203:2557-87.
24. Kopp T, Lenz P, Bello-Fernandez C, Kastelein RA, Kupper TS, Stingl G. IL-23 production by cosecretion of endogenous p19 and transgenic p40 in keratin 14/p40 transgenic mice: evidence for enhanced cutaneous immunity. J Immunol 2003; 170:5438-44.
25. Lubberts E, Koenders MI, van den Berg WB. The role of T cell interleukin-17 in conducting destructive arthritis: lessons from animal models. Arthritis Res Ther 2005; 7: 29-37.
26. Nakae S, Nambu A, Sudo K, Iwakura Y. Suppression of immune induction of collagen-induced arthritis in IL-17-deficient mice. J Immunol 2003; 171:6173-7.
27. Murphy CA, Langrish CL, Chen Y et al. Divergent pro- and antiinflammatory roles for IL-23 and IL-12 in joint autoimmune inflammation. J Exp Med 2003; 198:1951-7.
28. Hueber AJ, Asquith DL, Miller AM et al. Cutting edge: mast cells express IL-17A in rheumatoid arthritis synovium. J Immunol 2010; 184:3336-40.
29. Noordenbos T, Yeremenko N, Gofita I et al. Interleukin-17-positive mast cells contribute to synovial inflammation in spondylarthritis. Arthritis Rheumatol 2001; 64:99-109.
30. Lubberts E, Koenders MI, Oppers-Walgreen B et al. Treatment with a neutralizing anti-murine interleukin-17 antibody after the onset of collagen-induced arthritis reduces joint inflammation, cartilage destruction, and bone erosion. Arthritis Rheumatol 2004; 50:650-9.
31. Davidson SI, Liu Y, Danoy PA et al. Association of STAT3 and TNFRSF1A with ankylosing spondylitis in Han Chinese. Ann Rheum Dis 2011; 70:289-92.
32. Brown MA, Pile KD, Kennedy LG et al. HLA class I associations of ankylosing spondylitis in the white population in the United Kingdom. Ann Rheum Dis 1996; 55:268-70.
33. Bowness P. Overview of Ankylosing Spondylitis Genetics and Pathogenesis. Available at: http://www.rheumatology.org.uk/includes/documents/cm_docs/2012/1/1400_overview_of_ankylosing_spondylitis_genetics_and_pathogenesis.pdf (accessed 1 January 2015).
34. Brown MA, Laval SH, Brophy S, Calin A. Recurrence risk modelling of the genetic susceptibility to ankylosing spondylitis. Ann Rheum Dis 2000; 59:883-6.
35. Chou CT, Timms AE, Wei JCC, Tsai WC, Wordsworth BP, Brown MA. Replication of association of IL1 gene complex members with ankylosing spondylitis in Taiwanese Chinese. Ann Rheum Dis 2006; 65:1106-9.
36. Cortes A, Hadler J, Pointon JP et al. Identification of multiple risk variants for ankylosing spondylitis through high-density genotyping of immune-related loci. Nat Genet 2013; 45:730-8.
37. Davidson SI, Wu X, Liu Y et al. Association of ERAP1, but not IL23R, with ankylosing spondylitis in a Han Chinese population. Arthritis Rheum 2009; 60:3263-8.
38. Jadon D, Tillett W, Wallis D et al. Exploring ankylosing spondylitis-associated ERAP1, IL23R and IL12B gene polymorphisms in subphenotypes of psoriatic arthritis. Rheumatology 2013; 52:261-6.
39. Di Meglio P, Di Cesare A, Laggner U 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.
40. Chan AT, Kollnberger SD, Wedderburn LR, Wordsworth BP. Expansion and enhanced survival of natural killer cells expressing the killer immunoglobulin-like receptor KIR3DL2 in spondyloarthritis. Arthritis Rheum 2005; 52:3586-95.
41. Appel H, Maier R, Wu P et al. Analysis of IL-17+ cells in facet joints of patients with spondyloarthritis suggests that the innate immune pathway might be of greater relevance than the Th17-mediated adaptive immune response. Arthritis Res Ther 2011; 13:95.
42. DeLay ML, Turner MJ, Klenk EI, Smith JA, Sowders DP, Colbert RA. HLA-B27 misfolding and the unfolded protein response augment IL-23 production and are associated with Th17 activation in transgenic rats. Arthritis Rheum 2009; 60:2633-43.
43. Payeli SK, Kollnberger S, Maroguin Belaunzaran O et al. Inhibiting HLA-B27 homodimer-driven immune cell inflammation in spondylarthritis. Arthritis Rheum 2012; 64:3139-49.
44. Baeten D, Baraliakos X, Braun J et al. Anti-interleukin-17A monoclonal antibody secukinumab in treatment of ankylosing spondylitis: a randomised, double-blind, placebo-controlled trial. Lancet 2013; 382:1705-13.
45. Braun J, Brandt J, Listing J et al. Treatment of active ankylosing spondylitis with infliximab: a randomised controlled multicentre trial. Lancet 2002; 359:1187-93.
46. Baeten DL, Braun J, Baraliakios et al. Secukinumab, a monoclonal antibody to interleukin-17A, significantly improves signs and symptoms of active ankylosing spondylitis: results of a 52-week phase 3 randomized placebo-controlled trial with intravenous loading and subcutaneous maintenance dosing. Arthritis Rheum 2014; 66 (Suppl. 1): ACR Abstract no. 819.
47. Deodhar AA, Baeten DL, Braun J et al. Secukinumab, a monoclonal antibody to interleukin-17A, significantly improves physical function and quality of life in subjects with active ankylosing spondylitis: results of a phase 3 randomized, placebo-controlled trial with intravenous loading and subcutaneous maintenance dosing. Arthritis Rheum 2014; 66 (Suppl. 1): ACR Abstract no. 538.
48. Poddubnyy D, Hermann KG, Calhoff J, Listing J, Sieper J. Ustekinumab for the treatment of patients with active ankylosing spondylitis: results of a 28-week, prospective, open-label, proof-of-concept study (TOPAS). Ann Rheum Dis 2014; 73:817-23.
49. Ivanov II, McKenzie BS, Zhou L et al. The orphan nuclear receptor RORγ directs the differentiation program of proinflammatory IL-17+ T helper cells. Cell 2006; 126:1121-33.