The interleukin-23/interleukin-17 immune axis as a promising new target in the treatment of spondyloarthritis

Current Opinion in Rheumatology

Volumn 26, Issue 4, 2014, Pages 361-370

  Yeremenko, Nataliya ^a   Paramarta, Jacqueline E ^a   Baeten, Dominique ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

interleukin 17; interleukin 23; spondyloarthritis; treatment

Indexed keywords

APILIMOD; BRODALUMAB; FEZAKINUMAB; GUSELKUMAB; HLA B27 ANTIGEN; INTERLEUKIN 10; INTERLEUKIN 17; INTERLEUKIN 17F; INTERLEUKIN 21; INTERLEUKIN 22; INTERLEUKIN 23; INTERLEUKIN 25; INTERLEUKIN 4; IXEKIZUMAB; SECUKINUMAB; TILDRAKIZUMAB; USTEKINUMAB;

ANKYLOSING SPONDYLITIS; CYTOKINE PRODUCTION; GAMMA DELTA T LYMPHOCYTE; HUMAN; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; PSORIATIC ARTHRITIS; REVIEW; SIGNAL TRANSDUCTION; SPONDYLARTHRITIS;

EID: 84901824681     PISSN: 10408711     EISSN: 15316963     Source Type: Journal    
DOI: 10.1097/BOR.0000000000000069     Document Type: Review

References (67)

1. Dougados M, Baeten D. Spondyloarthritis. Lancet 2011; 377:2127-2137.
2. Brandt J, Haibel H, Cornely D, et al. Successful treatment of active ankylosing spondylitis with the antitumor necrosis factor alpha monoclonal antibody infliximab. Arthritis Rheum 2000; 43:1346-1352. (Pubitemid 30416320)
3. Van den Bosch F, Kruithof E, Baeten D, et al. Effects of a loading dose regimen of three infusions of chimeric monoclonal antibody to tumour necrosis factor alpha (infliximab) in spondyloarthropathy: an open pilot study. Ann Rheum Dis 2000; 59:428-433. (Pubitemid 30395599)
4. Baraliakos X, Listing J, Brandt J, et al. Clinical response to discontinuation of anti-TNF therapy in patients with ankylosing spondylitis after 3 years of continuous treatment with infliximab. Arthritis Res Ther 2005; 7:R439-R444.
5. Paramarta JE, Heijda TF, Baeten DL. Fast relapse upon discontinuation of tumour necrosis factor blocking therapy in patients with peripheral spondy-loarthritis. Ann Rheum Dis 2013; 72:1581-1582.
6. Song IH, Althoff CE, Haibel H, et al. Frequency and duration of drug-free remission after 1 year of treatment with etanercept versus sulfasalazine in early axial spondyloarthritis: 2 year data of the ESTHER trial. Ann Rheum Dis 2012; 71:1212-1215.
7. 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; 421:744-748. (Pubitemid 36227625)
8. Baeten DL, Kuchroo VK. How Cytokine networks fuel inflammation: Inter-leukin-17 and a tale of two autoimmune diseases. Nat Med 2013; 19:824-825.
9. 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; 198:1951-1957. (Pubitemid 38032126)
10. Aggarwal S, Ghilardi N, Xie MH, et al. Interleukin-23 promotes a distinct CD4 T cell activation state characterized by the production of interleukin-17. J Biol Chem 2003; 278:1910-1914. (Pubitemid 36801431)
11. Wright JF, Guo Y, Quazi A, et al. Identification of an interleukin 17F/17A heterodimerinactivatedhuman CD4+Tcells.JBiol Chem2007; 282:13447-13455. (Pubitemid 47100510)
12. Shen F, Gaffen SL. Structure-function relationships in the IL-17 receptor: implications for signal transduction and therapy. Cytokine 2008; 41:92-104.
13. Lee YK, Turner H, Maynard CL, et al. Late developmental plasticity in the T helper 17 lineage. Immunity 2009; 30:92-107.
14. Zielinski CE, Mele F, Aschenbrenner D, et al. Pathogen-induced human TH17 cells produce IFN-gamma or IL-10 and are regulated by IL-1beta. Nature 2012; 484:514-518.
15. Evans HG, Roostalu U, Walter GJ, et al. TNF-alpha blockade induces IL-10 expression in human CD4+ T cells. Nat Commun 2014; 5:3199. doi:10.1038/ ncomms4199.
16. Awasthi A, Riol-Blanco L, Jager A, et al. Cutting edge: IL-23 receptor gfp reporter mice reveal distinct populations of IL-17-producing cells. J Immunol 2009; 182:5904-5908.
17. Burton PR, Clayton DG, Cardon LR, et al. Association scan of 14, 500 nonsynonymous SNPs in four diseases identifies autoimmunity variants. Nat Genet 2007; 39:1329-1337. (Pubitemid 350041542)
18. Danoy P, Pryce K, Hadler J, et al. Association of variants at 1q32 and STAT3 with ankylosing spondylitis suggests genetic overlap with Crohn's disease. PLoS Genet 2010; 6:e1001195.
19. Evans DM, Spencer CC, 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; 43:761-767.
20. 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; 45:730-738.
21. Pointon JJ, Harvey D, Karaderi T, et al. Elucidating the chromosome 9 association with AS: CARD9 is a candidate gene. Genes Immun 2010; 11:490-496.
22. Chen Q, Muramoto K, Masaaki N, et al. A novel antagonist of the prosta-glandin E(2) EP(4) receptor inhibits Th1 differentiation and Th17 expansion and is orally active in arthritis models. Br J Pharmacol 2010; 160:292-310.
23. Gu J, Rihl M, Marker-Hermann E, et al. Clues to pathogenesis of spondyloar-thropathy derived from synovial fluid mononuclear cell gene expression profiles. J Rheumatol 2002; 29:2159-2164.
24. Dong W, Zhang Y, Yan M, et al. Upregulation of 78-kDa glucose-regulated protein in macrophages in peripheral joints of active ankylosing spondylitis. Scand J Rheumatol 2008; 37:427-434.
25. Zeng L, Lindstrom MJ, Smith JA. Ankylosing spondylitis macrophage production of higher levels of interleukin-23 in response to lipopolysaccharide without induction of a significant unfolded protein response. Arthritis Rheum 2011; 63:3807-3817.
26. Kollnberger S, Bird L, Sun MY, et al. Cell-surface expression and immune receptor recognition of HLA-B27 homodimers. Arthritis Rheum 2002; 46:2972-2982. (Pubitemid 35315891)
27. Bowness P, Ridley A, Shaw J, et al. Th17 cells expressing KIR3DL2+ and responsive to HLA-B27 homodimers are increased in ankylosing spondylitis. J Immunol 2011; 186:2672-2680.
28. Jandus C, Bioley G, Rivals JP, et al. Increased numbers of circulating polyfunctional Th17 memory cells in patients with seronegative spondylarthri-tides. Arthritis Rheum 2008; 58:2307-2317.
29. Shen H, Goodall JC, Hill Gaston JS. Frequency and phenotype of peripheral blood Th17 cells in ankylosing spondylitis and rheumatoid arthritis. Arthritis Rheum 2009; 60:1647-1656.
30. Zhang L, Li YG, Li YH, et al. Increased frequencies of Th22 cells as well as Th17 cells in the peripheral blood of patients with ankylosing spondylitis and rheumatoid arthritis. PLoS One 2012; 7:e31000.
31. Kenna TJ, Davidson SI, Duan R, et al. Enrichment of circulating interleukin-17-secreting interleukin-23 receptor-positive gamma/delta T cells in patients with active ankylosing spondylitis. Arthritis Rheum 2012; 64:1420-1429.
32. Prevosto C, Goodall JC, Hill Gaston JS. Cytokine secretion by pathogen recognition receptor-stimulated dendritic cells in rheumatoid arthritis and ankylosing spondylitis. J Rheumatol 2012; 39:1918-1928.
33. 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:R95.
34. Appel H, Maier R, Bleil J, et al. In situ analysis of interleukin-23-and interleukin-12-positive cells in the spine of patients with ankylosing spondylitis. Arthritis Rheum 2013; 65:1522-1529.
35. Noordenbos T, Yeremenko N, Gofita I, et al. Interleukin-17-positive mast cells contribute to synovial inflammation in spondylarthritis. Arthritis Rheum 2012; 64:99-109.
36. Ciccia F, Bombardieri M, Principato A, et al. Overexpression of interleukin-23, but not interleukin-17, as an immunologic signature of subclinical intestinal inflammation in ankylosing spondylitis. Arthritis Rheum 2009; 60:955-965.
37. DeLay ML, Turner MJ, Klenk EI, et al. HLA-B27 misfolding and the unfolded protein response augment interleukin-23 production and are associated with Th17 activation in transgenic rats. Arthritis Rheum 2009; 60:2633-2643.
38. Glatigny S, Fert I, Blaton MA, et al. Proinflammatory Th17 cells are expanded and induced by dendritic cells in spondylarthritis-prone HLA-B27-transgenic rats. Arthritis Rheum 2012; 64:110-120.
39. Abe Y, Ohtsuji M, Ohtsuji N, et al. Ankylosing enthesitis associated with up-regulated IFN-gamma and IL-17 production in (BXSB x NZB) F(1) male mice: a new mouse model. Mod Rheumatol 2009; 19:316-322.
40. Sherlock JP, Joyce-Shaikh B, Turner SP, et al. IL-23 induces spondyloarthropathy by acting on ROR-gammat+ CD3+CD4-CD8-entheseal resident T cells. Nat Med 2012; 18:1069-1076.
41. Duerr RH, Taylor KD, Brant SR, et al. A genome-wide association study identifies IL23R as an inflammatory bowel disease gene. Science 2006; 314:1461-1463. (Pubitemid 44871953)
42. Cargill M, Schrodi SJ, Chang 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. (Pubitemid 46175676)
43. Di MP, Di CA, 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.
44. Sarin R, Wu X, Abraham C. Inflammatory disease protective R381Q IL23 receptor polymorphism results in decreased primary CD4+ and CD8+ human T-cell functional responses. Proc Natl Acad Sci USA 2011; 108:9560-9565.
45. Utriainen L, Firmin D, Wright P, et al. Expression of HLA-B27 causes loss of migratory dendritic cells in a rat model of spondylarthritis. Arthritis Rheum 2012; 64:3199-3209.
46. Parkes M, Cortes A, van Heel DA, Brown MA. Genetic insights into common pathways and complex relationships among immune-mediated diseases. Nat Rev Genet 2013; 14:661-673.
47. Sieper J, Porter-Brown B, Thompson L, et al. Assessment of short-term symptomatic efficacy of tocilizumab in ankylosing spondylitis: results of randomised, placebo-controlled trials. Ann Rheum Dis 2014; 73:95-100.
48. Neerinckx B, Carter S, Lories RJ. No evidence for a critical role of the unfolded protein response in synovium and blood of patients with ankylosing spondy-litis. Ann Rheum Dis 2013; 73:629-630.
49. Melis L, Vandooren B, Kruithof E, et al. Systemic levels of IL-23 are strongly associated with disease activity in rheumatoid arthritis but not spondyloar-thritis. Ann Rheum Dis 2010; 69:618-623.
50. Wendling D, Cedoz JP, Racadot E. Serum and synovial fluid levels of p40 IL12/23 in spondyloarthropathy patients. Clin Rheumatol 2009; 28:187-190.
51. Adamopoulos IE, Tessmer M, Chao CC, et al. IL-23 is critical for induction of arthritis, osteoclast formation, and maintenance of bone mass. J Immunol 2011; 187:951-959.
52. Molle C, Zhang T, Ysebrant de Lendonck L, et al. Tristetraprolin regulation of interleukin 23 mRNA stability prevents a spontaneous inflammatory disease. J Exp Med 2013; 210:1675-1684.
53. Leonardi CL, Kimball AB, Papp KA, 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. (Pubitemid 351671883)
54. Papp KA, Langley RG, Sigurgeirsson B, et al. Efficacy and safety of secu-kinumab in the treatment of moderate-to-severe plaque psoriasis: a randomized, double-blind, placebo-controlled phase II dose-ranging study. Br J Dermatol 2013; 168:412-421.
55. Leonardi C, Matheson R, Zachariae C, et al. Antiinterleukin-17 monoclonal antibody ixekizumab in chronic plaque psoriasis. N Engl J Med 2012; 366:1190-1199.
56. Papp KA, Leonardi C, Menter A, et al. Brodalumab, an antiinterleukin-17- receptor antibody for psoriasis. N Engl J Med 2012; 366:1181-1189.
57. Sandborn WJ, Feagan BG, Fedorak RN, et al. A randomized trial of Usteki-numab, a human interleukin-12/23 monoclonal antibody, in patients with moderate-to-severe Crohn's disease. Gastroenterology 2008; 135:1130-1141.
58. Sandborn WJ, Gasink C, Gao LL, et al. Ustekinumab induction and maintenance therapy in refractory Crohn's disease. N Engl J Med 2012; 367:1519-1528.
59. Hueber W, Sands BE, Lewitzky S, et al. Secukinumab, a human anti-IL-17A monoclonal antibody, for moderate to severe Crohn's disease: unexpected results of a randomised, double-blind placebo-controlled trial. Gut 2012; 61:1693-1700.
60. Gottlieb A, Menter A, Mendelsohn A, et al. Ustekinumab, a human interleukin 12/23 monoclonal antibody, for psoriatic arthritis: randomised, double-blind, placebo-controlled, crossover trial. Lancet 2009; 373:633-640.
61. McInnes IB, Kavanaugh A, Gottlieb AB, et al. Efficacy and safety of usteki-numab in patients with active psoriatic arthritis: 1 year results of the phase 3, multicentre, double-blind, placebo-controlled PSUMMIT 1 trial. Lancet 2013; 382:780-789.
62. Ritchlin C, Rahman P, Kavanaugh A, et al. Efficacy and safety of the anti-IL-12/23 p40 monoclonal antibody, ustekinumab, in patients with active psoriatic arthritis despite conventional nonbiological and biological antitumour necrosis factor therapy: 6-month and 1-year results of the phase 3, multicentre, double-blind, placebo-controlled, randomised PSUMMIT 2 trial. Ann Rheum Dis 2014. doi: 10.1136/annrheumdis-2013-204655.
63. Poddubnyy D, Hermann KG, Callhoff J, et al. 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; 73:817-823.
64. McInnes IB, Sieper J, Braun J, et al. Efficacy and safety of secukinumab, a fully human antiinterleukin-17A monoclonal antibody, in patients with moderate-to-severe psoriatic arthritis: a 24-week, randomised, double-blind, placebo-controlled, phase II proof-of-concept trial. Ann Rheum Dis 2014; 73:349-56.
65. Baeten D, Baraliakos X, Braun J, et al. Antiinterleukin-17A mono-clonal antibody secukinumab in treatment of ankylosing spondylitis: a randomised, double-blind, placebo-controlled trial. Lancet 2013; 382:1705-1713.
66. Mease PJ, Genovese MC, Greenwald MW, et al. Efficacy of brodalumab, an anti-IL-17R antibody, in subjects with psoriatic arthritis [abstract]. Ann Rheum Dis 2013; 72 (Suppl3):85.
67. Ritchlin CT, Gottlieb AB, McInnes IB, et al. Ustekinumab in active psoriatic arthritis including patients previously treated with anti-TNF agents: results of a phase 3, multicenter, double-blind, placebo-controlled study [abstract]. Arthritis Rheum 2012; 64 (Suppl):S1080-S1081.