Inflammatory pathways in spondyloarthritis

Molecular Immunology

Volumn 57, Issue 1, 2014, Pages 28-37

  Hreggvidsdottir, Hulda S ^a   Noordenbos, Troy ^a   Baeten, Dominique L ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

Ankylosing spondylitis; Cytokines; IL 23; Spondyloarthritis; TNF

Indexed keywords

INTERLEUKIN 1; INTERLEUKIN 17; INTERLEUKIN 22; INTERLEUKIN 23; INTERLEUKIN 6; TUMOR NECROSIS FACTOR;

ARTICLE; CYTOKINE PRODUCTION; DISEASE ACTIVITY; GENE EXPRESSION; GENETIC ASSOCIATION; HUMAN; IN VIVO STUDY; INFLAMMATION; NONHUMAN; OSSIFICATION; PATHOPHYSIOLOGY; PHENOTYPE; PRIORITY JOURNAL; SPONDYLARTHRITIS;

ANKYLOSING SPONDYLITIS; CYTOKINES; IL-23; SPONDYLOARTHRITIS; TNF;

ANIMALS; GENETIC PREDISPOSITION TO DISEASE; HLA-B27 ANTIGEN; HUMANS; INFLAMMATION; INTERLEUKIN-1; INTERLEUKIN-17; INTERLEUKIN-23; INTERLEUKIN-6; MICE; POLYMORPHISM, SINGLE NUCLEOTIDE; SPONDYLITIS, ANKYLOSING; TUMOR NECROSIS FACTORS;

ANIMALIA; MUS;

EID: 84884415267     PISSN: 01615890     EISSN: 18729142     Source Type: Journal    
DOI: 10.1016/j.molimm.2013.07.016     Document Type: Article

References (122)

1. Adamopoulos I.E., Tessmer M., Chao C.-C., Adda S., Gorman Dan Petro M., Chou C.-C., Pierce R.H., Yao W., Lane N.E., Laface D., Bowman E.P. IL-23 is critical for induction of arthritis, osteoclast formation, and maintenance of bone mass. Journal of Immunology (Baltimore, MD) 2011, 187:951-959. 1950.
2. Alexopoulou L., Pasparakis M., Kollias G. A murine transmembrane tumor necrosis factor (TNF) transgene induces arthritis by cooperative p55/p75 TNF receptor signaling. European Journal of Immunology 1997, 27:2588-2592.
3. Ambarus C., Yeremenko N., Tak P.P., Baeten D. Pathogenesis of spondyloarthritis: autoimmune or autoinflammatory?. Current Opinion in Rheumatology 2012, 24.
4. Appel H., Maier R., Bleil J., Hempfing A., Loddenkemper C., Schlichting U., Syrbe U., Sieper J. In situ analysis of interleukin-23- and interleukin-12-positive cells in the spine of patients with ankylosing spondylitis. Arthritis & Rheumatism 2013, 65:1522-1529.
5. Appel H., Maier R., Wu P., Scheer R., Hempfing A., Kayser R., Thiel A., Radbruch A., Loddenkemper C., Sieper J. 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 Research & Therapy 2011, 13:R95.
6. Appel H., Ruiz-Heiland G., Listing J., Zwerina J., Herrmann M., Mueller R., Haibel H., Baraliakos X., Hempfing A., Rudwaleit M., Sieper J., Schett G. Altered skeletal expression of sclerostin and its link to radiographic progression in ankylosing spondylitis. Arthritis & Rheumatism 2009, 60:3257-3262.
7. Armaka M., Apostolaki M., Jacques P., Kontoyiannis D.L., Elewaut D., Kollias G. Mesenchymal cell targeting by TNF as a common pathogenic principle in chronic inflammatory joint and intestinal diseases. Journal of Experimental Medicine 2008, 205:331-337.
8. Atsumi T., Ishihara K., Kamimura D., Ikushima H., Ohtani T., Hirota S., Kobayashi H., Park S.-J., Saeki Y., Kitamura Y., Hirano T. A point mutation of Tyr-759 in interleukin 6 family cytokine receptor subunit gp130 causes autoimmune arthritis. Journal of Experimental Medicine 2002, 196:979-990.
9. Baeten D., Van Damme N., Van den Bosch F., Kruithof E., De Vos M., Mielants H., Veys E.M., De Keyser F. Impaired Th1 cytokine production in spondyloarthropathy is restored by anti-TNFα. Annals of the Rheumatic Diseases 2001, 60:750-755.
10. Baeten D., Breban M., Lories R., Schett G., Sieper J. Are spondylarthritides related but distinct conditions or a single disease with a heterogeneous phenotype?. Arthritis & Rheumatism 2013, 65:12-20.
11. Baeten D., Kruithof E., Van den Bosch F., Demetter P., Van Damme N., Cuvelier C., De Vos M., Mielants H., Veys E.M., De Keyser F. Immunomodulatory effects of anti-tumor necrosis factor α therapy on synovium in spondylarthropathy: histologic findings in eight patients from an open-label pilot study. Arthritis & Rheumatism 2001, 44:186-195.
12. Bal A., Unlu E., Bahar G., Aydog E., Eksioglu E., Yorgancioglu R. Comparison of serum IL-1 beta, sIL-2R, IL-6, and TNF-alpha levels with disease activity parameters in ankylosing spondylitis. Clinical Rheumatology 2007, 26:211-215.
13. Baraliakos X., Haibel H., Listing J., Sieper J., Braun J. Continuous long-term anti-TNF therapy does not lead to an increase in the rate of new bone formation over 8 years in patients with ankylosing spondylitis. Annals of the Rheumatic Diseases 2013.
14. Baraliakos X., Listing J., Rudwaleit M., Sieper J., Braun J. The relationship between inflammation and new bone formation in patients with ankylosing spondylitis. Arthritis Research & Therapy 2008, 10:R104.
15. Bowes J., Orozco G., Flynn E., Ho P., Brier R., Marzo-Ortega H., Coates L., McManus R., Ryan A.W., Kane D., Korendowych E., McHugh N., FitzGerald O., Packham J., Morgan A.W., Bruce I.N., Barton A. Confirmation of TNIP1 and IL23A as susceptibility loci for psoriatic arthritis. Annals of the Rheumatic Diseases 2011, 70:1641-1644.
16. Bowness P., Ridley A., Shaw J., Chan A.T., Wong-Baeza I., Fleming M., Cummings F., McMichael A., Kollnberger S. Th17 cells expressing KIR3DL2+ and responsive to HLA-B27 homodimers are increased in ankylosing spondylitis. Journal of Immunology (Baltimore, MD) 2011, 186:2672-2680.
17. Braun J., Brandt J., Listing J., Zink A., Alten R., Golder W., Gromnica-lhle E., Kellner H., Krause A., Schneider M., Sörensen H., Zeidler H., Thriene W., Sieper J. Treatment of active ankylosing spondylitis with infliximab: a randomised controlled multicentre trial. Lancet 2002, 359:1187-1193.
18. Burton P.R., Clayton D.G., Cardon L.R., Craddock N., Deloukas P., et al. Association scan of 14,500 nonsynonymous SNPs in four diseases identifies autoimmunity variants. Nature Genetics 2007, 39:1329-1337.
19. Chen C., Zhang X., Wang Y. Analysis of JAK2 and STAT3 polymorphisms in patients with ankylosing spondylitis in Chinese Han population. Clinical Immunology (Orlando, FL) 2010, 136:442-446.
20. Ciccia F., Accardo-Palumbo A., Alessandro R., Rizzo A., Principe S., Peralta S., Raiata F., Giardina A., De Leo G., Triolo G. Interleukin-22 and interleukin-22-producing NKp44+ natural killer cells in subclinical gut inflammation in ankylosing spondylitis. Arthritis & Rheumatism 2012, 64:1869-1878.
21. Ciccia F., Bombardieri M., Principato A., Giardina A., Tripodo C., Porcasi R., Peralta S., Franco V., Giardina E., Craxi A., Pitzalis C., Triolo G. Overexpression of interleukin-23, but not interleukin-17, as an immunologic signature of subclinical intestinal inflammation in ankylosing spondylitis. Arthritis & Rheumatism 2009, 60:955-965.
22. Coffre M., Roumier M., Rybczynska M., Sechet E., Law H.K.W., Gossec L., Dougados M., Bianchi E., Rogge L. Combinatorial control of Th17 and Th1 cell function by genetic variation at genes associated with the IL-23 signaling pathway in spondyloarthritis. Arthritis & Rheumatism 2013.
23. Cohen J.-D., Ferreira R., Jorgensen C. Ankylosing spondylitis refractory to tumor necrosis factor blockade responds to tocilizumab. Journal of Rheumatology 2011, 38:1527.
24. Corona-Sanchez E.G., Muñoz-Valle J.F., Gonzalez-Lopez L., Sanchez-Hernandez J.D., Vazquez-Del Mercado M., Ontiveros-Mercado H., Huerta M., Trujillo X., Rocha-Muñoz A.D., Celis A., Ortega-Flores R., Gamez-Nava J.I. -383 A/C tumor necrosis factor receptor 1 polymorphism and ankylosing spondylitis in Mexicans: a preliminary study. Rheumatology International 2012, 32:2565-2568.
25. Danoy P., Pryce K., Hadler J., Bradbury L.A., Farrar Claire Pointon J., Ward M., Weisman M., Reveille J.D., Wordsworth B., Paul Stone M.A., Maksymowych W.P., Rahman P., Gladman D., Inman Robert D., Brown Matthew A. Association of variants at 1q32 and STAT3 with ankylosing spondylitis suggests genetic overlap with Crohn's disease. PLoS Genetics 2010, 6:e1001195.
26. Davidson S.I., Liu Y., Danoy P.A., Wu X., Thomas G.P., Jiang L., Sun L., Wang N., Han J., Han H., Visscher P.M., Brown M.A., Xu H. Association of STAT3 and TNFRSF1A with ankylosing spondylitis in Han Chinese. Annals of the Rheumatic Diseases 2011, 70:289-292.
27. Di Meglio P., Di Cesare A., Laggner U., Chu C.-C., Napolitano L., Villanova F., Tosi I., Capon F., Trembath R.C., Peris K., Nestle F.O. 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.
28. Diarra D., Stolina M., Polzer K., Zwerina J., Ominsky M.S., Dwyer D., Korb A., Smolen J., Hoffmann M., Scheinecker C., van der Heide D., Landewe R., Lacey D., Richards W.G., Schett G. Georg Dickkopf-1 is a master regulator of joint remodeling. Nature Medicine 2007, 13:156-163.
29. Di Meglio P., Villanova F., Napolitano L., Tosi I., Barberio M.T., Mak R.K., Nutland S., Smith C.H., Barker J.N., Todd J.A., Nestle F.O. 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 2013, [Epub ahead of print]. 10.1038/jid.2013.170.
30. Dougados M., Gueguen A., Nakache J.P., Velicitat P., Zeidler H., Veys E., Calin A. Clinical relevance of C-reactive protein in axial involvement of ankylosing spondylitis. Journal of Rheumatology 1999, 26:971-974.
31. Dougados M., Baeten D. Spondyloarthritis. Lancet 2011, 377:2127-2137.
32. Edwards C.K., Bendele A.M., Reznikov L.I., Fantuzzi G., Chlipala E.S., Li L., Moldawer L.L., Mountz J.D., Li Y.-Y.Y., Dinarello C.A. Soluble human p55 and p75 tumor necrosis factor receptors reverse spontaneous arthritis in transgenic mice expressing transmembrane tumor necrosis factor alpha. Arthritis & Rheumatism 2006, 54:2872-2885.
33. Ernst M., Inglese M., Waring P., Campbell I.K., Bao S., Clay F.J., Alexander W.S., Wicks I.P., Tarlinton D.M., Novak U., Heath J.K., Dunn A.R. Defective gp130-mediated signal transducer and activator of transcription (STAT) signaling results in degenerative joint disease, gastrointestinal ulceration, and failure of uterine implantation. Journal of Experimental Medicine 2001, 194:189-203.
34. Evans D.M., Spencer C.C., Pointon J.J., Su Z., Harvey D., et al. Interaction between ERAP1 and HLA-B27 in ankylosing spondylitis implicates peptide handling in the mechanism for HLA-B27 in disease susceptibility. Nature Genetics 2011, 43:761-767.
35. Falkenbach A., Herold M., Wigand R. Interleukin-6 serum concentration in ankylosing spondylitis: a reliable predictor of disease progression in the subsequent year?. Rheumatology International 2000, 19:149-151.
36. Filer C., Ho P., Smith R.L., Griffiths C., Young H.S., Worthington J., Bruce I.N., Barton A. Investigation of association of the IL12B and IL23R genes with psoriatic arthritis. Arthritis & Rheumatism 2008, 58:3705-3709.
37. Finzel S., Kraus S., Schmidt S., Hueber A., Rech J., Engelke K., Englbrecht M., Schett G. Bone anabolic changes progress in psoriatic arthritis patients despite treatment with methotrexate or tumour necrosis factor inhibitors. Annals of the Rheumatic Diseases 2012.
38. François R.J., Neure L., Sieper J., Braun J. Immunohistological examination of open sacroiliac biopsies of patients with ankylosing spondylitis: detection of tumour necrosis factor alpha in two patients with early disease and transforming growth factor beta in three more advanced cases. Annals of the Rheumatic Diseases 2006, 65:713-720.
39. Gottlieb A., Menter A., Mendelsohn A., Shen Y.K., Guzzo C., Fretzin S., Kunynetz R., Kavanaugh A. Ustekinumab, a human interleukin 12/23 monoclonal antibody, for psoriatic arthritis: randomised, double-blind, placebo-controlled, crossover trial. Lancet 2009, 373:633-640.
40. Graham S., Gamie Z., Polyzois I., Narvani A.A., Tzafetta K., Tsiridis E., Helioti M., Mantalaris A., Tsiridis E. Prostaglandin EP2 and EP4 receptor agonists in bone formation and bone healing: in vivo and in vitro evidence. Expert Opinion on Investigational Drugs 2009, 18:746-766.
41. Gratacós J., Collado A., Filella X., Sanmartí R., Cañete J., Llena J., Molina R., Ballesta A., Muñoz-Gómez J. Serum cytokines (IL-6, TNF-alpha, IL-1 beta and IFN-gamma) in ankylosing spondylitis: a close correlation between serum IL-6 and disease activity and severity. British Journal of Rheumatology 1994, 33:927-931.
42. Haibel H., Rudwaleit M., Listing J., Sieper J. Open label trial of anakinra in active ankylosing spondylitis over 24 weeks. Annals of the Rheumatic Diseases 2005, 64:296-298.
43. Heiland G.R., Appel H., Poddubnyy D., Zwerina J., Hueber A., Haibel H., Baraliakos X., Listing J., Rudwaleit M., Schett G., Sieper J. High level of functional dickkopf-1 predicts protection from syndesmophyte formation in patients with ankylosing spondylitis. Annals of the Rheumatic Diseases 2012, 71:572-574.
44. Henes J.C., Horger M., Guenaydin I., Kanz L., Koetter I. Mixed response to tocilizumab for ankylosing spondylitis. Annals of the Rheumatic Diseases 2010, 69:2217-2218.
45. Horai R., Saijo S., Tanioka H., Nakae S., Sudo K., Okahara A., Ikuse T., Asano M., Iwakura Y. Development of chronic inflammatory arthropathy resembling rheumatoid arthritis in interleukin 1 receptor antagonist-deficient mice. Journal of Experimental Medicine 2000, 191:313-320.
46. Hueber W., Patel D.D., Dryja T., Wright A.M., Koroleva I., Bruin G., Antoni C., Draelos Z., Gold M.H., Durez P., Tak Paul P., Gomez-Reino J.J., Foster C.S., Kim R.Y., Samson C.M., Falk N.S., Chu D.S., Callanan D., Nguyen Q.D., Rose K., Haider A., Di Padova F. Effects of AIN457, a fully human antibody to interleukin-17A, on psoriasis, rheumatoid arthritis, and uveitis. Science Translational Medicine 2010, 2:52ra72.
47. Karaderi T., Pointon J.J., Wordsworth T.W.H., Harvey D., Appleton L.H., Cohen C.J., Farrar C., Harin A., Brown M.A., Wordsworth B.P. Evidence of genetic association between TNFRSF1A encoding the p55 tumour necrosis factor receptor, and ankylosing spondylitis in UK Caucasians. Clinical and Experimental Rheumatology 2012, 30:110-113.
48. Keffer J., Probert L., Cazlaris H., Georgopoulos S., Kaslaris E., Kioussis D., Kollias G. Transgenic mice expressing human tumour necrosis factor: a predictive genetic model of arthritis. EMBO Journal 1991, 10:4025-4031.
49. Kenna T.J., Davidson S.I., Duan R., Bradbury L.A., McFarlane J., Smith M., Weedon H., Street S., Thomas R., Thomas G.P., Brown Matthew A. Enrichment of circulating interleukin-17-secreting interleukin-23 receptor-positive γ/δ T cells in patients with active ankylosing spondylitis. Arthritis & Rheumatism 2012, 64:1420-1429.
50. Koenders M.I., Devesa I., Marijnissen R.J., Abdollahi-Roodsaz S., Boots A.M.H., Walgreen B., Di Padova F.E., Nicklin M.J.H., Joosten L.A.B., Van den Berg W.B. Interleukin-1 drives pathogenic Th17 cells during spontaneous arthritis in interleukin-1 receptor antagonist-deficient mice. Arthritis & Rheumatism 2008, 58:3461-3470.
51. Kontoyiannis D., Pasparakis M., Pizarro T.T., Cominelli F., Kollias G. Impaired on/off regulation of TNF biosynthesis in mice lacking TNF AU-rich elements: implications for joint and gut-associated immunopathologies. Immunity 1999.
52. Koumakis E., Feydy A., Kahan A., Allanore Y. Interleukin 6 blockade in spondyloarthritis. Journal of Rheumatology 2012, 39:1097-1098. author reply 1098.
53. Kroon F., Landewé R., Dougados M., Van der Heijde D. Continuous NSAID use reverts the effects of inflammation on radiographic progression in patients with ankylosing spondylitis. Annals of the Rheumatic Diseases 2012, 71:1623-1629.
54. Kruithof E., Baeten D., De Rycke L., Vandooren B., Foell D., Roth J., Cañete J.D., Boots A.M., Veys E.M., De Keyser F. Synovial histopathology of psoriatic arthritis, both oligo- and polyarticular resembles spondyloarthropathy more than it does rheumatoid arthritis. Arthritis Research & Therapy 2005, 7:R569-R580.
55. Lea W., Lee Y.H. The associations between interleukin-1 polymorphisms and susceptibility to ankylosing spondylitis: a meta-analysis. Joint Bone Spine 2012, 79:370-374.
56. LeibundGut-Landmann S., Gross O., Robinson M.J., Osorio F., Slack E.C., Tsoni S.V., Schweighoffer E., Tybulewicz V., Brown G.D., Ruland J., Reis e Sousa C. Syk- and CARD9-dependent coupling of innate immunity to the induction of T helper cells that produce interleukin 17. Nature Immunology 2007, 8:630-638.
57. Leonardi C., Matheson R., Zachariae C., Cameron G., Li L., Edson-Heredia E., Braun D., Banerjee S. Anti-interleukin-17 monoclonal antibody ixekizumab in chronic plaque psoriasis. New England Journal of Medicine 2012, 366:1190-1199.
58. Leonardi C.L., Kimball A.B., Papp K.A., Yeilding N., Guzzo C., Wang Y., Li S., Dooley Lisa T., Gordon K.B. 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.
59. Limón-Camacho L., Vargas-Rojas M.I., Vázquez-Mellado J., Casasola-Vargas J., Moctezuma J.F., Burgos-Vargas R., Llorente L. In vivo peripheral blood proinflammatory T cells in patients with ankylosing spondylitis. Journal of Rheumatology 2012, 39:830-835.
60. Lin Z., Bei J.-X., Shen M., Li Q., Liao Z., et al. A genome-wide association study in Han Chinese identifies new susceptibility loci for ankylosing spondylitis. Nature Genetics 2012, 44:73-77.
61. Lories R.J.U., Derese I., Luyten F.P. Inhibition of osteoclasts does not prevent joint ankylosis in a mouse model of spondyloarthritis. Rheumatology (Oxford, England) 2008, 47:605-608.
62. Lories R.J.U., Derese I., De Bari C., Luyten F.P. Evidence for uncoupling of inflammation and joint remodeling in a mouse model of spondylarthritis. Arthritis & Rheumatism 2007, 56:489-497.
63. Lories R.J.U., Derese I., Luyten F.P. Modulation of bone morphogenetic protein signaling inhibits the onset and progression of ankylosing enthesitis. Journal of Clinical Investigation 2005, 115:1571-1579.
64. Lories R.J.U., Luyten F.P., De Vlam K. Progress in spondylarthritis. Mechanisms of new bone formation in spondyloarthritis. Arthritis Research & Therapy 2009, 11:221.
65. Matsuki T., Isoda K., Horai R., Nakajima A., Aizawa Y., Suzuki K., Ohsuzu F., Iwakura Y. Involvement of tumor necrosis factor-alpha in the development of T cell-dependent aortitis in interleukin-1 receptor antagonist-deficient mice. Circulation 2005, 112:1323-1331.
66. McInnes I.B., Sieper J., Braun J., Emery P., Van der Heijde D., Isaacs J.D., Dahmen G., Wollenhaupt J., Schulze-Koops H., Kogan J., Ma S., Schumacher M.M., Bertolino A.P., Hueber W., Tak P.P. Efficacy and safety of secukinumab, a fully human anti-interleukin-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. Annals of the Rheumatic Diseases 2013.
67. Melis L., Vandooren B., Kruithof E., Jacques P., De Vos M., Mielants H., Verbruggen G., De Keyser F., Elewaut D. Systemic levels of IL-23 are strongly associated with disease activity in rheumatoid arthritis but not spondyloarthritis. Annals of the Rheumatic Diseases 2010, 69:618-623.
68. Monnet D., Kadi A., Izac B., Lebrun N., Letourneur F., Zinovieva E., Said-Nahal R., Chiocchia G., Breban M. Association between the IL-1 family gene cluster and spondyloarthritis. Annals of the Rheumatic Diseases 2012, 71:885-890.
69. Nakae S., Saijo S., Horai R., Sudo K., Mori S., Iwakura Y. IL-17 production from activated T cells is required for the spontaneous development of destructive arthritis in mice deficient in IL-1 receptor antagonist. Proceedings of the National Academy of Sciences of the United States of America 2003, 100:5986-5990.
70. Nakajima K., Kanda T., Takaishi M., Shiga T., Miyoshi K., Nakajima H., Kamijima R., Tarutani M., Benson J.M., Elloso M.M., Gutshall L.L., Naso M.F., Iwakura Y., DiGiovanni J., Sano S. Distinct roles of IL-23 and IL-17 in the development of psoriasis-like lesions in a mouse model. Journal of Immunology 2011, 186(7):4481-4489. Erratum in: Journal of Immunology 2011;187(11):6157-6158. 10.4049/jimmunol.1000148.
71. Noordenbos T., Yeremenko N., Gofita I., Van de Sande M., Tak P.P., Caňete J.D., Baeten D. Interleukin-17-positive mast cells contribute to synovial inflammation in spondylarthritis. Arthritis & Rheumatism 2012, 64:99-109.
72. Ozgocmen S., Godekmerdan A., Ozkurt-Zengin F. Acute-phase response, clinical measures and disease activity in ankylosing spondylitis. Joint, Bone, Spine: Revue du Rhumatisme 2007, 74:249-253.
73. Papp K.A., Langley R.G., Sigurgeirsson B., Abe M., Baker D.R., Konno P., Haemmerle S., Thurston H.J., Papavassilis C., Richards H.B. Efficacy and safety of secukinumab in the treatment of moderate-to-severe plaque psoriasis: a randomized, double-blind, placebo-controlled phase II dose-ranging study. British Journal of Dermatology 2013, 168:412-421.
74. Papp K.A., Langley R.G., Lebwohl M., Krueger G.G., Szapary P., Yeilding N., Guzzo C., Hsu M.-C., Wang Y., Li S., Dooley Lisa T., Reich K. 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.
75. Papp K.A., Leonardi C., Menter A., Ortonne J.-P., Krueger J.G., Kricorian G., Aras G., Li J., Russell C.B., Thompson E.H.Z., Baumgartner S. Brodalumab, an anti-interleukin-17-receptor antibody for psoriasis. New England Journal of Medicine 2012, 366:1181-1189.
76. Pappu B.P., Borodovsky A., Zheng T.S., Yang X., Wu P., Dong X., Weng S., Browning B., Scott M.L., Ma L., Su L., Tian Q., Schneider P., Flavell R.A., Dong C., Burkly L.C. TL1A-DR3 interaction regulates Th17 cell function and Th17-mediated autoimmune disease. Journal of Experimental Medicine 2008, 205:1049-1062.
77. Paramarta J.E., De Rycke L., Heijda T.F., Ambarus Carmen A., Vos K., Dinant H.J., Tak P.P., Baeten D.L. Efficacy and safety of adalimumab for the treatment of peripheral arthritis in spondyloarthritis patients without ankylosing spondylitis or psoriatic arthritis. Annals of the Rheumatic Diseases 2012.
78. Parham C., Chirica M., Timans J., Vaisberg E., Travis M., Cheung J., Pflanz S., Zhang R., Singh K.P., Vega F., To W., Wagner J., O'Farrell A.-M., McClanahan T., Zurawski S., Hannum C., Gorman D., Rennick D.M., Kastelein R.A., De Waal M.R., Moore K.W. A receptor for the heterodimeric cytokine IL-23 is composed of IL-12R{beta}1 and a novel cytokine receptor subunit, IL-23R. Journal of Immunology 2002, 168:5699-5708.
79. Park H., Bourla A.B., Kastner D.L., Colbert R.A., Siegel R.M. Lighting the fires within: the cell biology of autoinflammatory diseases. Nature Reviews. Immunology 2012, 12:570-580.
80. Pedersen S.J., Sørensen I.J., Garnero P., Johansen J.S., Madsen O.R., Tvede N., Hansen M.S., Thamsborg G., Andersen L.S., Majgaard O., Loft A.G., Erlendsson J., Asmussen K., Jurik A.G., Møller J., Hasselquist M., Mikkelsen D., Skjødt T., Lambert R., Hansen A., Østergaard M. ASDAS, BASDAI and different treatment responses and their relation to biomarkers of inflammation, cartilage and bone turnover in patients with axial spondyloarthritis treated with TNFα inhibitors. Annals of the Rheumatic Diseases 2011, 70:1375-1381.
81. Phillips K.L.E., Jordan-Mahy N., Nicklin M.J.H., Le Maitre C.L. Interleukin-1 receptor antagonist deficient mice provide insights into pathogenesis of human intervertebral disc degeneration. Annals of the Rheumatic Diseases 2013.
82. Pidasheva S., Trifari S., Phillips A., Hackney J.A., Ma Y., Smith A., Sohn S.J., Spits H., Little R.D., Behrens T.W., Honigberg L., Ghilardi N., Clark H.F. Functional studies on the IBD susceptibility gene IL23R implicate reduced receptor function in the protective genetic variant R381Q. PLoS ONE 2011, 6:e25038.
83. Pobezinskaya Y.L., Liu Z. The role of TRADD in death receptor signaling. Cell Cycle (Georgetown, TX) 2012, 11:871-876.
84. Poddubnyy D., Brandt H., Vahldiek J., Spiller I., Song I.-H., Rudwaleit M., Sieper J. The frequency of non-radiographic axial spondyloarthritis in relation to symptom duration in patients referred because of chronic back pain: results from the Berlin early spondyloarthritis clinic. Annals of the Rheumatic Diseases 2012, 71:1998-2001.
85. Poddubnyy D., Haibel H., Listing J., Märker-Hermann E., Zeidler H., Braun J., Sieper J., Rudwaleit M. Baseline radiographic damage elevated acute-phase reactant levels, and cigarette smoking status predict spinal radiographic progression in early axial spondylarthritis. Arthritis & Rheumatism 2012, 64:1388-1398.
86. Poddubnyy D., Rudwaleit M., Haibel H., Listing J., Märker-Hermann E., Zeidler H., Braun J., Sieper J. Rates and predictors of radiographic sacroiliitis progression over 2 years in patients with axial spondyloarthritis. Annals of the Rheumatic Diseases 2011, 70:1369-1374.
87. Pointon J.J., Harvey D., Karaderi T., Appleton L.H., Farrar C., Stone M.A., Sturrock R.D., Reveille J.D., Weisman M.H., Ward M.M., Brown A., Matthew, Wordsworth B.P. The chromosome 16q region associated with ankylosing spondylitis includes the candidate gene tumour necrosis factor receptor type 1-associated death domain (TRADD). Annals of the Rheumatic Diseases 2010, 69:1243-1246.
88. Reveille J.D., Sims A.M., Danoy P., Evans D.M., Leo P., Pointon J.J., Jin R., Zhou X., Bradbury L.A., Appleton L.H., Davis J.C., Diekman L., Doan T., Dowling A., Duan R., Duncan E.L., Farrar C., Hadler J., Harvey D., Karaderi T., Mogg R., Pomeroy E., Pryce K., Taylor J., Savage L., Deloukas P., Kumanduri V., Peltonen L., Ring S.M., Whittaker P., Glazov E., Thomas G.P., Maksymowych W.P., Inman R.D., Ward M.M., Stone M.A., Weisman M.H., Wordsworth B.P., Brown M.A. Genome-wide association study of ankylosing spondylitis identifies non-MHC susceptibility loci. Nature Genetics 2010, 42:123-127.
89. Romero-Sánchez C., Robinson W.H., Tomooka B.H., Londoño J., Valle-Oñate R., Huang F., Deng X., Zhang L., Yang C., Yu D.T. Identification of acute phase reactants and cytokines useful for monitoring infliximab therapy in ankylosing spondylitis. Clinical Rheumatology 2008, 27:1429-1435.
90. Rudwaleit M., Listing J., Brandt J., Braun J., Sieper J. Prediction of a major clinical response (BASDAI 50) to tumour necrosis factor alpha blockers in ankylosing spondylitis. Annals of the Rheumatic Diseases 2004, 63:665-670.
91. Sandborn W.J., Feagan B.G., Fedorak R.N., Scherl E., Fleisher M.R., Katz S., Johanns J., Blank M., Rutgeerts P. A randomized trial of Ustekinumab, a human interleukin-12/23 monoclonal antibody, in patients with moderate-to-severe Crohn's disease. Gastroenterology 2008, 135:1130-1141.
92. Sandborn W.J., Gasink C., Gao L.-L., Blank M.A., Johanns J., Guzzo C., Sands B.E., Hanauer S.B., Targan S., Rutgeerts P., Ghosh S., De Villiers W.J.S., Panaccione R., Greenberg G., Schreiber S., Lichtiger S., Feagan B.G. Ustekinumab induction and maintenance therapy in refractory Crohn's disease. New England Journal of Medicine 2012, 367:1519-1528.
93. 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. Proceedings of the National Academy of Sciences of the United States of America 2011, 108:9560-9565.
94. Schett G., Stolina M., Dwyer D., Zack D., Uderhardt S., Krönke G., Kostenuik P., Feige U. Tumor necrosis factor α and RANKL blockade cannot halt bony spur formation in experimental inflammatory arthritis. Arthritis & Rheumatism 2009, 60:2644-2654.
95. Sheehan N.J., Slavin B.M., Donovan M.P., Mount J.N., Mathews J.A. Lack of correlation between clinical disease activity and erythrocyte sedimentation rate, acute phase proteins or protease inhibitors in ankylosing spondylitis. British Journal of Rheumatology 1986, 25:171-174.
96. Shen H., Goodall J.C., Hill Gaston J.S. Frequency and phenotype of peripheral blood Th17 cells in ankylosing spondylitis and rheumatoid arthritis. Arthritis & Rheumatism 2009, 60:1647-1656.
97. - entheseal resident T cells. Nature Medicine 2012, 18:1069-1076.
98. Shima Y., Tomita T., Ishii T., Morishima A., Maeda Y., Ogata A., Kishimoto T., Tanaka T. Tocilizumab a humanized anti-interleukin-6 receptor antibody, ameliorated clinical symptoms and MRI findings of a patient with ankylosing spondylitis. Modern Rheumatology/The Japan Rheumatism Association 2011, 21:436-439.
99. Sieper J., Inman R.D., Badalamenti S., Radin A., Braun J. Sarilumab for the treatment of ankylosing spondylitis: results of a phase 2, randomized. Double-blind, placebo-controlled, international study (align). Annals of the Rheumatic Diseases 2012, 71(Suppl. 3):111.
100. Sieper J., Porter-Brown B., Thompson L., Harari O., Dougados M. Tocilizumab (TCZ) is not effective for the treatment of ankylosing spondylitis (AS): results of a phase 2, international, multicentre, randomised, double-blind placebo-controlled trial. Annals of the Rheumatic Diseases 2012, 71(Suppl. 3):110.
101. Sieper J., Appel H., Braun J., Rudwaleit M. Critical appraisal of assessment of structural damage in ankylosing spondylitis: implications for treatment outcomes. Arthritis & Rheumatism 2008, 58:649-656.
102. Sieper J., Van der Heijde D., Dougados M., Mease P.J., Maksymowych W.P., Brown M.A., Arora V., Pangan A.L. Efficacy and safety of adalimumab in patients with non-radiographic axial spondyloarthritis: results of a randomised placebo-controlled trial (ABILITY-1). Annals of the Rheumatic Diseases 2012.
103. Sonomoto K., Yamaoka K., Oshita K., Fukuyo S., Zhang X., Nakano K., Okada Y., Tanaka Y. Interleukin-1β induces differentiation of human mesenchymal stem cells into osteoblasts via the Wnt-5a/receptor tyrosine kinase-like orphan receptor 2 pathway. Arthritis & Rheumatism 2012, 64:3355-3363.
104. Spoorenberg A., Van der Heijde D., De Klerk E., Dougados M., De Vlam K., Mielants H., Van der Tempel H., Van der Linden S. Relative value of erythrocyte sedimentation rate and C-reactive protein in assessment of disease activity in ankylosing spondylitis. Journal of Rheumatology 1999, 26:980-984.
105. Tan A.L., Marzo-Ortega H., O'Connor P., Fraser A., Emery P., McGonagle D. Efficacy of anakinra in active ankylosing spondylitis: a clinical and magnetic resonance imaging study. Annals of the Rheumatic Diseases 2004, 63:1041-1045.
106. Uderhardt S., Diarra D., Katzenbeisser J., David J.-P., Zwerina J., Richards W., Kronke G., Schett G. Blockade of Dickkopf (DKK)-1 induces fusion of sacroiliac joints. Annals of the Rheumatic Diseases 2010, 69:592-597.
107. Van den Bosch F., Kruithof E., Baeten D., Herssens A., De Keyser F., Mielants H., Veys E.M. Randomized double-blind comparison of chimeric monoclonal antibody to tumor necrosis factor α (infliximab) versus placebo in active spondylarthropathy. Arthritis & Rheumatism 2002, 46:755-765.
108. Van der Heijde D., Kavanaugh A., Gladman D.D., Antoni C., Krueger G.G., Guzzo C., Zhou B., Dooley L.T., De Vlam K., Geusens P., Birbara C., Halter D., Beutler A. Infliximab inhibits progression of radiographic damage in patients with active psoriatic arthritis through one year of treatment: results from the induction and maintenance psoriatic arthritis clinical trial 2. Arthritis & Rheumatism 2007, 56:2698-2707.
109. Van der Heijde D., Landewé R., Baraliakos X., Houben H., Van Tubergen A., Williamson P., Xu W., Baker D., Goldstein N., Braun J. Radiographic findings following two years of infliximab therapy in patients with ankylosing spondylitis. Arthritis & Rheumatism 2008, 58:3063-3070.
110. Van der Heijde D., Landewé R., Einstein S., Ory P., Vosse D., Ni L., Lin S.-L., Tsuji W., Davis J.C. Radiographic progression of ankylosing spondylitis after up to two years of treatment with etanercept. Arthritis & Rheumatism 2008, 58:1324-1331.
111. Van der Heijde D., Salonen D., Weissman B.N., Landewé R., Maksymowych W.P., Kupper H., Ballal S., Gibson E., Wong R. Assessment of radiographic progression in the spines of patients with ankylosing spondylitis treated with adalimumab for up to 2 years. Arthritis Research & Therapy 2009, 11:R127.
112. Van Duivenvoorde L.M., Ambarus C.A., Masdar H., Tok M.N.v., Tak P.P., Yeremenko N.G., Baeten D.L. A2.15 relative overexpression of transmembrane versus soluble TNF in human and experimental spondyloarthritis. Annals of the Rheumatic Diseases 2013, 72:A9-A10.
113. Van Duivenvoorde L.M., Dorris M.L., Satumtira N., Van Tok M.N., Redlich K., Tak P.P., Taurog J.D., Baeten D.L. Relationship between inflammation bone destruction, and osteoproliferation in the HLA-B27/human β2-microglobulin-transgenic rat model of spondylarthritis. Arthritis & Rheumatism 2012, 64:3210-3219.
114. Vandooren B., Cantaert T., Noordenbos T., Tak P.P., Baeten D. The abundant synovial expression of the RANK/RANKL/osteoprotegerin system in peripheral spondylarthritis is partially disconnected from inflammation. Arthritis & Rheumatism 2008, 58:718-729.
115. Vandooren B., Kruithof E., Yu D.T., Rihl M., Gu J., De Rycke L., Van Den Bosch F., Veys E.M., De Keyser F., Baeten D. Involvement of matrix metalloproteinases and their inhibitors in peripheral synovitis and down-regulation by tumor necrosis factor α blockade in spondylarthropathy. Arthritis & Rheumatism 2004, 50:2942-2953.
116. Vandooren B., Yeremenko N., Noordenbos T., Bras J., Tak P.P., Baeten D. Mediators of structural remodeling in peripheral spondylarthritis. Arthritis & Rheumatism 2009, 60:3534-3545.
117. Visvanathan S., Wagner C., Marini J.C., Baker D., Gathany T., Han J., Van der Heijde D., Braun J. Inflammatory biomarkers, disease activity and spinal disease measures in patients with ankylosing spondylitis after treatment with infliximab. Annals of the Rheumatic Diseases 2008, 67:511-517.
118. Wanders A., van der Heijde D., Landewé R., Béhier J.-M., Calin A., Olivieri I., Zeidler H., Dougados M. Nonsteroidal antiinflammatory drugs reduce radiographic progression in patients with ankylosing spondylitis: a randomized clinical trial. Arthritis & Rheumatism 2005, 52:1756-1765.
119. Wendling D., Cedoz J.-P., Racadot E. Serum and synovial fluid levels of p40 IL12/23 in spondyloarthropathy patients. Clinical Rheumatology 2009, 28:187-190.
120. Zeng L., Lindstrom M.J., Smith J.A. Ankylosing spondylitis macrophage production of higher levels of interleukin-23 in response to lipopolysaccharide without induction of a significant unfolded protein response. Arthritis & Rheumatism 2011, 63:3807-3817.
121. Zinovieva E., Bourgain C., Kadi A., Letourneur F., Izac B., Said-Nahal R., Lebrun N., Cagnard N., Vigier A., Jacques S., Miceli-Richard C., Garchon H.J., Heath S., Charon C., Bacq D., Boland A., Zelenika D., Chiocchia G., Breban M. Comprehensive linkage and association analyses identify haplotype, near to the TNFSF15 gene, significantly associated with spondyloarthritis. PLoS Genetics 2009, 5:e1000528.
122. Zwerina J., Redlich K., Polzer K., Joosten L., Kronke G., Distler J., Hess A., Pundt N., Pap T., Hoffmann O., Gasser J., Scheinecker C., Smolen J.S., van den Berg W., Schett G. TNF-induced structural joint damage is mediated by IL-1. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:11742-11747.