The critical role of interleukin-23 in spondyloarthropathy

Molecular Immunology

Volumn 57, Issue 1, 2014, Pages 38-43

  Sherlock, Jonathan P ^a,b   Buckley, Christopher D ^a   Cua, Daniel J ^c  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c MERCK RESEARCH LABORATORIES   (United States)

Author keywords

Enthesitis; Interleukin 23; Spondyloarthropathy; T lymphocytes

Indexed keywords

HLA B27 ANTIGEN; INTERLEUKIN 23; INTERLEUKIN 23 RECEPTOR; OSTEOGENIC PROTEIN 1;

ANTIGEN RECOGNITION; CD8+ T LYMPHOCYTE; CELL PROLIFERATION; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; ENTHESITIS; GEL ELECTROPHORESIS; GENETIC VARIABILITY; HEREDITY; HISTOPATHOLOGY; HUMAN; NONHUMAN; OSTEOCLAST; PHYSICAL STRESS; PRIORITY JOURNAL; PROTEIN FOLDING; REVIEW; SPONDYLOARTHROPATHY; UNFOLDED PROTEIN RESPONSE;

ENTHESITIS; INTERLEUKIN-23; SPONDYLOARTHROPATHY; T LYMPHOCYTES;

ANIMALS; BONE AND BONES; GENETIC PREDISPOSITION TO DISEASE; HLA-B27 ANTIGEN; HUMANS; INTERLEUKIN-23; JOINTS; SPINE; SPONDYLITIS, ANKYLOSING;

EID: 84884411123     PISSN: 01615890     EISSN: 18729142     Source Type: Journal    
DOI: 10.1016/j.molimm.2013.06.010     Document Type: Review

References (59)

1. Alcalde M., Acebes J.C., Cruz M., González-Hombrado L., Herrero-Beaumont G., Sánchez-Pernaute O. A sonographic enthesitic index of lower limbs is a valuable tool in the assessment of ankylosing spondylitis. Ann. Rheum. Dis. 2007, 66:1015-1019.
2. Allen R.L., Raine T., Haude A., Trowsdale J., Wilson M.J. Leukocyte receptor complex-encoded immunomodulatory receptors show differing specificity for alternative HLA-B27 structures. J. Immunol. 2001, 167:5543-5547.
3. Antoniou A.N., Ford S., Taurog J.D., Butcher G.W., Powis S.J. Formation of HLA-B27 homodimers and their relationship to assembly kinetics. J. Biol. Chem. 2004, 279:8895-8902.
4. Appel H., Kuhne M., Spiekermann S., Ebhardt H., Grozdanovic Z., Köhler D., Dreimann M., Hempfing A., Rudwaleit M., Stein H., et al. Immunohistologic analysis of zygapophyseal joints in patients with ankylosing spondylitis. Arthritis Rheum. 2006, 54:2845-2851.
5. Appel H., Kuhne M., Spiekermann S., Köhler D., Zacher J., Stein H., Sieper J., Loddenkemper C. Immunohistochemical analysis of hip arthritis in ankylosing spondylitis: evaluation of the bone-cartilage interface and subchondral bone marrow. Arthritis Rheum. 2006, 54:1805-1813.
6. 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 alpha therapy on synovium in spondylarthropathy: histologic findings in eight patients from an open-label pilot study. Arthritis Rheum. 2001, 44:186-195.
7. Ball J. Enthesopathy of rheumatoid and ankylosing spondylitis. Ann. Rheum. Dis. 1971, 30:213-223.
8. Benjamin M., McGonagle D. The anatomical basis for disease localisation in seronegative spondyloarthropathy at entheses and related sites. J. Anat. 2001, 199:503-526.
9. Benjamin M., Kaiser E., Milz S. Structure-function relationships in tendons: a review. J. Anat. 2008, 212:211-228.
10. Benjamin M., McGonagle D. Histopathologic changes at synovio-entheseal complexes suggesting a novel mechanism for synovitis in osteoarthritis and spondylarthritis. Arthritis Rheum. 2007, 56:3601-3609.
11. Benjamin R., Parham P. Guilt by association: HLA-B27 and ankylosing spondylitis. Immunol. Today 1990, 11:137-142.
12. Bird L.A., Peh C.A., Kollnberger S., Elliott T., McMichael A.J., Bowness P. Lymphoblastoid cells express HLA-B27 homodimers both intracellularly and at the cell surface following endosomal recycling. Eur. J. Immunol. 2003, 33:748-759.
13. Bollow M., Fischer T., Reisshauer H., Backhaus M., Sieper J., Hamm B., Braun J. Quantitative analyses of sacroiliac biopsies in spondyloarthropathies: T cells and macrophages predominate in early and active sacroiliitis-cellularity correlates with the degree of enhancement detected by magnetic resonance imaging. Ann. Rheum. Dis. 2000, 59:135-140.
14. Borman P., Koparal S., Babaoǧlu S., Bodur H. Ultrasound detection of entheseal insertions in the foot of patients with spondyloarthropathy. Clin. Rheumatol. 2006, 25:373-377.
15. 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. J. Immunol. 2011, 186:2672-2680.
16. Breban M., Fernández-Sueiro J.L., Richardson J.A., Hadavand R.R., Maika S.D., Hammer R.E., Taurog J.D. T cells, but not thymic exposure to HLA-B27, are required for the inflammatory disease of HLA-B27 transgenic rats. J. Immunol. 1996, 156:794-803.
17. Canoso J.J. The premiere enthesis. J. Rheumatol. 1998, 25:1254-1256.
18. Cauli A., Dessole G., Fiorillo M.T., Vacca A., Mameli A., Bitti P., Passiu G., Sorrentino R., Mathieu A. Increased level of HLA-B27 expression in ankylosing spondylitis patients compared with healthy HLA-B27-positive subjects: a possible further susceptibility factor for the development of disease. Rheumatology (Oxford) 2002, 41:1375-1379.
19. Chan A.T., Kollnberger S.D., Wedderburn L.R., Bowness P. Expansion and enhanced survival of natural killer cells expressing the killer immunoglobulin-like receptor KIR3DL2 in spondylarthritis. Arthritis Rheum. 2005, 52:3586-3595.
20. Ciccia F., Bombardieri M., Principato A., Giardina A., Tripodo C., Porcasi R., Peralta S., Franco V., Giardina E., Craxi 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.
21. Cua D.J., Sherlock J.P. Autoimmunity's collateral damage: gut microbiota strikes 'back'. Nat. Med. 2011, 17:1055-1056.
22. D'Agostino M.A., Said-Nahal R., Hacquard-Bouder C., Brasseur J.-L., Dougados M., Breban M. Assessment of peripheral enthesitis in the spondylarthropathies by ultrasonography combined with power Doppler: a cross-sectional study. Arthritis Rheum. 2003, 48:523-533.
23. Dangoria N.S., DeLay M.L., Kingsbury D.J., Mear J.P., Uchanska-Ziegler B., Ziegler A., Colbert R.A. HLA-B27 misfolding is associated with aberrant intermolecular disulfide bond formation dimerization in the endoplasmic reticulum. J. Biol. Chem. 2002, 277:23459-23468.
24. de Miguel E., Cobo T., Muñoz-Fernández S., Naredo E., Usón J., Acebes J.C., Andréu J.L., Martín-Mola E. Validity of enthesis ultrasound assessment in spondyloarthropathy. Ann. Rheum. Dis. 2009, 68:169-174.
25. DeLay M.L., Turner M.J., Klenk E.I., Smith J.A., Sowders D.P., Colbert R.A. 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.
26. Emad Y., Ragab Y., Bassyouni I., Moawayh O., Fawzy M., Saad A., Abou-Zeid A., Rasker J.J. Enthesitis and related changes in the knees in seronegative spondyloarthropathies and skin psoriasis: magnetic resonance imaging case-control study. J. Rheumatol. 2010, 37:1709-1717.
27. Emad Y., Ragab Y., Shaarawy A., Abou-Zeid A., Saad A., Fawzy M., Jokhdar H., Rasker J.J. Can magnetic resonance imaging differentiate undifferentiated arthritis based on knee imaging. J. Rheumatol. 2009, 36:1963-1970.
28. François R.J., Gardner D.L., Degrave E.J., Bywaters E.G. Histopathologic evidence that sacroiliitis in ankylosing spondylitis is not merely enthesitis. Arthritis Rheum. 2000, 43:2011-2024.
29. Goodall J.C., Wu C., Zhang Y., McNeill L., Ellis L., Saudek V., Gaston J.S.H. Endoplasmic reticulum stress-induced transcription factor, CHOP, is crucial for dendritic cell IL-23 expression. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:17698-17703.
30. Hansasuta P., Dong T., Thananchai H., Weekes M., Willberg C., Aldemir H., Rowland-Jones S., Braud V.M. Recognition of HLA-A3 and HLA-A11 by KIR3DL2 is peptide-specific. Eur. J. Immunol. 2004, 34:1673-1679.
31. Jevtic V., Watt I., Rozman B., Kos-Golja M., Demsar F., Jarh O. Distinctive radiological features of small hand joints in rheumatoid arthritis and seronegative spondyloarthritis demonstrated by contrast-enhanced Gd-DTPA magnetic resonance imaging. Skeletal Radiol. 1995, 24:351-355.
32. Karmakar S., Kay J., Gravallese E.M. Bone damage in rheumatoid arthritis: mechanistic insights and approaches to prevention. Rheum. Dis. Clin. North Am. 2010, 36:385-404.
33. Khare S.D., Luthra H.S., David C.S. Spontaneous inflammatory arthritis in HLA-B27 transgenic mice lacking beta 2-microglobulin: a model of human spondyloarthropathies. J. Exp. Med. 1995, 182:1153-1158.
34. Kidd B.L., Moore K., Walters M.T., Smith J.L., Cawley M.I. Immunohistological features of synovitis in ankylosing spondylitis: a comparison with rheumatoid arthritis. Ann. Rheum. Dis. 1989, 48:92-98.
35. Kollnberger S., Bird L.A., Roddis M., Hacquard-Bouder C., Kubagawa H., Bodmer H.C., Breban M., McMichael A.J., Bowness P. HLA-B27 heavy chain homodimers are expressed in HLA-B27 transgenic rodent models of spondyloarthritis and are ligands for paired Ig-like receptors. J. Immunol. 2004, 173:1699-1710.
36. Kollnberger S., Bird L., Sun M.-Y., Retiere C., Braud V.M., McMichael A., Bowness P. Cell-surface expression and immune receptor recognition of HLA-B27 homodimers. Arthritis Rheum. 2002, 46:2972-2982.
37. Kollnberger S., Chan A., Sun M.-Y., Chen L.Y., Wright C., Di Gleria K., McMichael A., Bowness P. Interaction of HLA-B27 homodimers with KIR3DL1 and KIR3DL2, unlike HLA-B27 heterotrimers, is independent of the sequence of bound peptide. Eur. J. Immunol. 2007, 37:1313-1322.
38. Lanier L.L. NK cell recognition. Annu. Rev. Immunol. 2005, 23:225-274.
39. Lee E., Trepicchio W.L., Oestreicher J.L., Pittman D., Wang F., Chamian F., Dhodapkar M., Krueger J.G. Increased expression of interleukin 23 p19 and p40 in lesional skin of patients with psoriasis vulgaris. J. Exp. Med. 2004, 199:125-130.
40. Lehtinen A., Taavitsainen M., Leirisalo-Repo M. Sonographic analysis of enthesopathy in the lower extremities of patients with spondylarthropathy. Clin. Exp. Rheumatol. 1994, 12:143-148.
41. Lories R.J.U., Luyten F.P., de Vlam K. Progress in spondylarthritis. Mechanisms of new bone formation in spondyloarthritis. Arthritis Res. Ther. 2009, 11:221.
42. May E., Dorris M.L., Satumtira N., Iqbal I., Rehman M.I., Lightfoot E., Taurog J.D. CD8 alpha beta T cells are not essential to the pathogenesis of arthritis or colitis in HLA-B27 transgenic rats. J. Immunol. 2003, 170:1099-1105.
43. McGonagle D., Gibbon W., Emery P. Classification of inflammatory arthritis by enthesitis. Lancet 1998, 352:1137-1140.
44. McGonagle D., Gibbon W., O'Connor P., Green M., Pease C., Emery P. Characteristic magnetic resonance imaging entheseal changes of knee synovitis in spondylarthropathy. Arthritis Rheum. 1998, 41:694-700.
45. McGonagle D., Marzo-Ortega H., O'Connor P., Gibbon W., Hawkey P., Henshaw K., Emery P. Histological assessment of the early enthesitis lesion in spondyloarthropathy. Ann. Rheum. Dis. 2002, 61:534-537.
46. Mielants H., Veys E.M., Cuvelier C., de Vos M., Goemaere S., de Clercq L., Schatteman L., Elewaut D. The evolution of spondyloarthropathies in relation to gut histology. II. Histological aspects. J. Rheumatol. 1995, 22:2273-2278.
47. Muche B., Bollow M., François R.J., Sieper J., Hamm B., Braun J. Anatomic structures involved in early- and late-stage sacroiliitis in spondylarthritis: a detailed analysis by contrast-enhanced magnetic resonance imaging. Arthritis Rheum. 2003, 48:1374-1384.
48. Piskin G., Sylva-Steenland R.M.R., Bos J.D., Teunissen M.B.M. In vitro and in situ expression of IL-23 by keratinocytes in healthy skin and psoriasis lesions: enhanced expression in psoriatic skin. J. Immunol. 2006, 176:1908-1915.
49. Rudwaleit M., van der Heijde D., Landewé R., Akkoc N., Brandt J., Chou C.T., Dougados M., Huang F., Gu J., Kirazli Y., et al. The Assessment of SpondyloArthritis International Society classification criteria for peripheral spondyloarthritis and for spondyloarthritis in general. Ann. Rheum. Dis. 2011, 70:25-31.
50. Scott D.L., Wolfe F., Huizinga T.W.J. Rheumatoid arthritis. Lancet 2010, 376:1094-1108.
51. Shen H., Goodall J.C., Hill Gaston J.S. Frequency and phenotype of peripheral blood Th17 cells in ankylosing spondylitis and rheumatoid arthritis. Arthritis Rheum. 2009, 60:1647-1656.
52. Sherlock J.P., Joyce-Shaikh B., Turner S.P., Chao C.-C., Sathe M., Grein J., Gorman D.M., Bowman E.P., McClanahan T.K., Yearley J.H., et al. IL-23 induces spondyloarthropathy by acting on ROR-(t+CD3+CD4-CD8-entheseal resident T cells. Nat. Med. 2012, 18:1069-1076.
53. Tan A.L., Benjamin M., Toumi H., Grainger A.J., Tanner S.F., Emery P., McGonagle D. The relationship between the extensor tendon enthesis and the nail in distal interphalangeal joint disease in psoriatic arthritis - a high-resolution MRI and histological study. Rheumatology (Oxford) 2007, 46:253-256.
54. Taurog J.D., Maika S.D., Simmons W.A., Breban M., Hammer R.E. Susceptibility to inflammatory disease in HLA-B27 transgenic rat lines correlates with the level of B27 expression. J. Immunol. 1993, 150:4168-4178.
55. Taurog J., Dorris M., Satumtira N., Tran T., Sharma R., Dressel R., van den Brandt J., Reichardt H. Spondylarthritis in HLA-B27/human beta2-microglobulin-transgenic rats is not prevented by lack of CD8. Arthritis Rheum. 2009, 60:1977-1984.
56. Taurog J.D., Rival C., van Duivenvoorde L.M., Satumtira N., Dorris M.L., Sun M., Shelton J.M., Richardson J.A., Hamra F.K., Hammer R.E., et al. Autoimmune epididymoorchitis is essential to the pathogenesis of male-specific spondylarthritis in HLA-B27-transgenic rats. Arthritis Rheum. 2012, 64:2518-2528.
57. Turner M.J., Sowders D.P., DeLay M.L., Mohapatra R., Bai S., Smith J.A., Brandewie J.R., Taurog J.D., Colbert R.A. HLA-B27 misfolding in transgenic rats is associated with activation of the unfolded protein response. J. Immunol. 2005, 175:2438-2448.
58. van Echteld I., Cieza A., Boonen A., Stucki G., Zochling J., Braun J., van der Heijde D. Identification of the most common problems by patients with ankylosing spondylitis using the international classification of functioning, disability and health. J. Rheumatol. 2006, 33:2475-2483.
59. Wellcome Trust Case Control Consortium, Australo-Anglo-American Spondylitis Consortium (TASC), Burton P.R., Clayton D.G., Cardon L.R., Craddock N., Deloukas P., Duncanson A., Kwiatkowski D.P., McCarthy M.I., et al. Association scan of 14,500 nonsynonymous SNPs in four diseases identifies autoimmunity variants. Nat. Genet. 2007, 39:1329-1337.