Pathogenesis of spondyloarthritis: Insights from synovial membrane studies

Current Rheumatology Reports

Volumn 8, Issue 4, 2006, Pages 275-282

  De Rycke, Leen ^b   Kruithof, Elli ^b   Vandooren, Bernard ^b   Tak, Paul P ^b   Baeten, Dominique ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b NONE

Author keywords

[No Author keywords available]

Indexed keywords

CALGRANULIN; CD163 ANTIGEN; GAMMA INTERFERON; INFLIXIMAB; INTERLEUKIN 1BETA; INTERLEUKIN 6; STROMELYSIN; TOLL LIKE RECEPTOR; TUMOR NECROSIS FACTOR ALPHA INHIBITOR;

ANKYLOSING SPONDYLITIS; B LYMPHOCYTE; CELL ACTIVATION; CELL ADHESION; CYTOKINE PRODUCTION; DISEASE ACTIVITY; ENDOTHELIUM CELL; GENETIC SUSCEPTIBILITY; HISTOPATHOLOGY; HUMAN; INNATE IMMUNITY; MACROPHAGE; PATHOGENESIS; POLYMORPHONUCLEAR CELL; PROTEIN EXPRESSION; REVIEW; SYNOVITIS; SYNOVIUM; T LYMPHOCYTE;

HUMANS; LYMPHOCYTES; MACROPHAGES; NEUTROPHILS; SPONDYLARTHRITIS; SYNOVIAL MEMBRANE; TOLL-LIKE RECEPTORS;

EID: 33750326944     PISSN: 15233774     EISSN: 15346307     Source Type: Journal    
DOI: 10.1007/s11926-006-0008-4     Document Type: Review

References (72)

1. Hammer RE, Maika SD, Richardson JA, et al.: Spontaneous inflammatory disease in transgenic rats expressing HLA-B27 and human beta 2m: an animal model of HLA-B27-associated human disorders. Cell 1990, 63:1099-1112.
2. Taurog JD, Richardson JA, Croft JT, et al.: The germfree state prevents development of gut and joint inflammatory disease in HLA-B27 transgenic rats. J Exp Med 1994, 180:2359-2364.
3. Hermann E, Yu DT, Meyer zum Buschenfelde KH, et al.: HLA-B27-restricted CD8 T cells derived from synovial fluids of patients with reactive arthritis and ankylosing spondylitis. Lancet 1993, 342:646-650.
4. Dulphy N, Peyrat MA, Tieng V, et al.: Common intra-articular T cell expansions in patients with reactive arthritis: identical beta-chain functional sequences and cytotoxicity toward HLA-B27. J Immunol 1999, 162:3830-3839.
5. Popov I, Dela Cruz CS, Barber BH, et al.: The effect of an anti-HLA-B27 immune response on CTL recognition of Chlamydia. J Immunol 2001, 167:3375-3382.
6. Ugrinovic S, Mertz A, Wu P, et al.: A single nonamer from the Yersinia 60-kDa heat shock protein is the target of HLA-B27-restricted CTL response in Yersinia-induced reactive arthritis. J Immunol 1997, 159:5715-5723.
7. Kuon W, Kuhne M, Busch DH, et al.: Identification of novel human aggrecan T cell epitopes in HLA-B27 transgenic mice associated with spondyloarthropathy. J Immunol 2004, 173:4859-4866.
8. Atagunduz P, Appel H, Kuon W, et al.: HLA-B27-restricted CD8+ T cell response to cartilage-derived self peptides in ankylosing spondylitis. Arthritis Rheum 2005, 52:892-901.
9. Zou J, Appel H, Rudwaleit M, et al.: Analysis of the CD8+ T cell response to the G1 domain of aggrecan in ankylosing spondylitis. Ann Rheum Dis 2005, 64:722-729.
10. + T cells, which have been thought to play a HLA-B27 restricted role in the pathogenesis of spondylarthritis, are not crucial for the pathology in HLA-B27 transgenic animals.
11. Mear JP, Schreiber KL, Munz C, et al.: Misfolding of HLA-B27 as a result of its B pocket suggests a novel mechanism for its role in susceptibility to spondyloarthropathies. J Immunol 1999, 163:6665-6670.
12. Allen RL, O'Callaghan CA, McMichael AJ, Bowness P: Cutting edge: HLA-B27 can form a novel beta 2-microglobulin-free heavy chain homodimer structure. J Immunol 1999, 162:5045-5048.
13. 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.
14. Chan AT, Kollnberger SD, Wedderburn LR, 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.
15. Baeuerle PA, Henkel T: Function and activation of NF-kappa B in the immune system. Annu Rev Immunol 1994, 12:141-179.
16. Tran TM, Satumtira N, Dorris ML, et al.: HLA-B27 in transgenic rats forms disulfide-linked heavy chain oligomers and multimers that bind to the chaperone BiP. J Immunol 2004, 172:5110-5119.
17. Ikawa T, Ikeda M, Yamaguchi A, et al.: Expression of arthritis-causing HLA-B27 on Hela cells promotes induction of c-fos in response to in vitro invasion by Salmonella typhimurium. J Clin Invest 1998, 101:263-272.
18. Penttinen MA, Holmberg CI, Sistonen L, Granfors K: HLA-B27 modulates nuclear factor kappaB activation in human monocytic cells exposed to lipopolysaccharide. Arthritis Rheum 2002, 46:2172-2180.
19. Smeets TJ, Dolhain RJ, Breedveld FC, Tak PP: Analysis of the cellular infiltrates and expression of cytokines in synovial tissue from patients with rheumatoid arthritis and reactive arthritis. J Pathol 1998, 186:75-81.
20. Baeten D, Demetter P, Cuvelier C, et al.: Comparative study of synovial histology in rheumatoid arthritis, spondyloarthropathy and osteoarthritis: influence of disease duration and activity. Ann Rheum Dis 2000, 59:945-953.
21. Baeten D, Kruithof E, De Rycke L, et al.: Diagnostic classification of spondylarthropathy and rheumatoid arthritis by synovial histopathology: a prospective study in 154 consecutive patients. Arthritis Rheum 2004, 50:2931-2941.
22. Baeten D, Møller HJ, Delanghe J, et al.: Association of CD163+ macrophages and local production of soluble CD163 with decreased lymphocyte activation in spondylarthropathy synovitis. Arthritis Rheum 2004, 50:1611-1623.
23. Canete JD, Martinez SE, Farres J, et al.: Differential Th1/Th2 cytokine patterns in chronic arthritis: Interferon gamma is highly expressed in synovium of rheumatoid arthritis compared with seronegative spondyloarthropathies. Ann Rheum Dis 2000, 59:263-268.
24. Rudwaleit M, Siegert S, Yin Z, et al.: Low T cell production of TNFalpha and IFNgamma in ankylosing spondylitis: its relation to HLA-B27 and influence of the TNF-308 gene polymorphism. Ann Rheum Dis 2001, 60:36-42.
25. Baeten D, Van Damme N, Van den Bosch F, et al.: Impaired Th1 cytokine production in spondyloarthropathy is restored by anti-TNFalpha. Ann Rheum Dis 2001, 60:750-755.
26. Baeten D, Vandooren B, De Rycke L, et al.: Effect of infliximab treatment on T cell cytokine responses in spondylarthropathy: comment on the article by Zou et al. Arthritis Rheum 2004, 50:1015-1016.
27. Sieper J: Mechanisms of action of biologicals in AS. Ann Rheum Dis 2005, 64: S111.
28. Zou J, Rudwaleit M, Brandt J, et al.: Up regulation of the production of tumour necrosis factor alpha and interferon gamma by T cells in ankylosing spondylitis during treatment with etanercept. Ann Rheum Dis 2003, 62:561-564.
29. Kraan MC, van Kuijk AW, Dinant HJ, et al.: Alefacept treatment in psoriatic arthritis: Reduction of the effector T cell population in peripheral blood and synovial tissue is associated with improvement of clinical signs of arthritis. Arthritis Rheum 2002, 46:2776-2784.
30. Baeten D, Kruithof E, Van den Bosch F, et al.: 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.
31. Kruithof E, Baeten D, Van den Bosch F, et al.: Histological evidence that infliximab treatment leads to downregulation of inflammation and tissue remodelling of the synovial membrane in spondyloarthropathy. Ann Rheum Dis 2005, 64:529-536.
32. Kruithof E, De Rycke L, Roth J, et al.: Immunomodulatory effects of etanercept on peripheral joint synovitis in the spondylarthropathies. Arthritis Rheum 2005, 52:3898-3909.
33. De Rycke L, Baeten D, Kruithof E, et al.: Infliximab, but not etanercept, induces IgM anti-double-stranded DNA autoantibodies as main antinuclear reactivity: biologic and clinical implications in autoimmune arthritis. Arthritis Rheum 2005, 52:2192-2201.
34. Shi S, Ciurli C, Cartman A, et al.: Experimental immunity to the G1 domain of the proteoglycan versican induces spondylitis and sacroiliitis, of a kind seen in human spondylarthropathies. Arthritis Rheum 2003, 48:2903-2915. Here, Shi et al. introduce a new animal model for spondylarthritis in which humoral immunity appears to play an important role.
35. Baeten D, Demetter P, Cuvelier CA, et al.: Macrophages expressing the scavenger receptor CD163: a link between immune alterations of the gut and synovial inflammation in spondyloarthropathy. J Pathol 2002, 196:343-350. This article first describes the selective increase of a specific macrophage subset characterized by the expression of the scavenger receptor CD163 in spondylarthritis.
36. Kruithof E, Baeten D, De Rycke L, et al.: Synovial histopathology of psoriatic arthritis, both oligo- and polyarticular, resembles spondyloarthropathy more than it does rheumatoid arthritis. Arthritis Res Ther 2005, 7:R569-R580.
37. Demetter P, De Vos M, Van Huysse JA, et al.: Colon mucosa of patients both with spondylarthritis and Crohn's disease is enriched with macrophages expressing the scavenger receptor CD163. Ann Rheum Dis 2005, 64:321-324.
38. De Rycke L, Baeten D, Foell D, et al.: Differential expression and response to anti-TNFalpha treatment of infiltrating versus resident tissue macrophage subsets in autoimmune arthritis. J Pathol 2005, 206:17-27.
39. Sack U, Stiehl P, Geiler G: Distribution of macrophages in rheumatoid synovial membrane and its association with basic activity. Rheumatol Int 1994, 13:181-186.
40. Tak PP, Smeets TJ, Daha MR, et al.: Analysis of the synovial cell infiltrate in early rheumatoid synovial tissue in relation to local disease activity. Arthritis Rheum 1997, 40:217-225.
41. Kraan MC, Versendaal H, Jonker M, et al.: Asymptomatic synovitis precedes clinically manifest arthritis. Arthritis Rheum 1998, 41:1481-1488.
42. Smeets TJ, Barg EC, Kraan MC, et al.: Analysis of the cell infiltrate and expression of proinflammatory cytokines and matrix metalloproteinases in arthroscopic synovial biopsies: comparison with synovial samples from patients with end stage, destructive rheumatoid arthritis. Ann Rheum Dis 2003, 62:635-638.
43. Gerlag DM, Haringman JJ, Smeets TJ, et al.: Effects of oral prednisolone on biomarkers in synovial tissue and clinical improvement in rheumatoid arthritis. Arthritis Rheum 2004, 50:3783-3791. This work demonstrates that synovial sublining macrophages are good biomarkers of response to treatment in rheumatoid arthritis.
44. Haringman JJ, Gerlag DM, Zwinderman AH, et al.: Synovial tissue macrophages: a sensitive biomarker for response to treatment in patients with rheumatoid arthritis. Ann Rheum Dis 2005, 64:834-838.
45. + macrophages and polymorphonuclear cells, correlate directly with global disease activity and inflammation in spondylarthritis.
46. Paleolog E: The therapeutic potential of TNF-alpha blockade in rheumatoid arthritis. Expert Opin Investig Drugs 2003, 12:1087-1095.
47. Smeets TJ, Kraan MC, van Loon ME, Tak PP: Tumor necrosis factor alpha blockade reduces the synovial cell infiltrate early after initiation of treatment, but apparently not by induction of apoptosis in synovial tissue. Arthritis Rheum 2003, 48:2155-2162.
48. Goedkoop AY, Kraan MC, Teunissen MB, et al.: Early effects of tumour necrosis factor alpha blockade on skin and synovial tissue in patients with active psoriasis and psoriatic arthritis. Ann Rheum Dis 2004, 63:769-773.
49. Kane D, Gogarty M, O'leary J, et al.: Reduction of synovial sublining layer inflammation and proinflammatory cytokine expression in psoriatic arthritis treated with methotrexate. Arthritis Rheum 2004, 50:3286-3295.
50. Kruithof E, De Rycke L, Vandooren B, et al.: Identification of synovial biomarkers of response to experimental treatment in early phase clinical trials in spondylarthropathy. Arthritis Rheum 2006, In press.
51. Hogger P, Dreier J, Droste A, et al.: Identification of the integral membrane protein RM3/1 on human monocytes as a glucocorticoid-inducible member of the scavenger receptor cysteine-rich family (CD163). J Immunol 1998, 161:1883-1890.
52. Mantovani A, Sica A, Sozzani S, et al.: The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol 2004, 25:677-686. Article clearly and comprehensively reviews different macrophage subsets.
53. Kristiansen M, Graversen JH, Jacobsen C, et al.: Identification of the haemoglobin scavenger receptor. Nature 2001, 409:198-201.
54. Langlois MR, Delanghe JR: Biological and clinical significance of haptoglobin polymorphism in humans. Clin Chem 1996, 42:1589-1600.
55. Droste A, Sorg C, Hogger P: Shedding of CD163, a novel regulatory mechanism for a member of the scavenger receptor cysteine-rich family. Biochem Biophys Res Commun 1999, 256:110-113.
56. Moller HJ, Peterslund NA, Graversen JH, Moestrup SK: Identification of the hemoglobin scavenger receptor/CD163 as a natural soluble protein in plasma. Blood 2002, 99:378-380.
57. Schebesch C, Kodelja V, Muller C, et al.: Alternatively activated macrophages actively inhibit proliferation of peripheral blood lymphocytes and CD4+ T cells in vitro. Immunology 1997, 92:478-486.
58. Hogger P, Sorg C: Soluble CD163 inhibits phorbol ester-induced lymphocyte proliferation. Biochem Biophys Res Commun 2001, 288:841-843.
59. Van den Heuvel MM, Tensen CP, van As JH, et al.: Regulation of CD 163 on human macrophages: cross-linking of CD163 induces signaling and activation. J Leukoc Biol 1999, 66:858-866.
60. Moestrup SK, Moller HJ: CD163: a regulated hemoglobin scavenger receptor with a role in the anti-inflammatory response. Ann Med 2004, 36:347-354.
61. Seibl R, Birchler T, Loeliger S, et al.: Expression and regulation of Toll-like receptor 2 in rheumatoid arthritis synovium. Am J Pathol 2003, 162:1221-1227.
62. Iwahashi M, Yamamura M, Aita T, et al.: Expression of Toll-like receptor 2 on CD16+ blood monocytes and synovial tissue macrophages in rheumatoid arthritis. Arthritis Rheum 2004, 50:1457-1467.
63. Radstake TR, Roelofs MF, Jenniskens YM, et al.: Expression of Toll-like receptors 2 and 4 in rheumatoid synovial tissue and regulation by proinflammatory cytokines interleukin-12 and interleukin-18 via interferon-gamma. Arthritis Rheum 2004, 50:3856-3865.
64. Choe JY, Crain B, Wu SR, Corr M: Interleukin 1 receptor dependence of serum transferred arthritis can be circumvented by toll-like receptor 4 signaling. J Exp Med 2003, 197:537-542.
65. Joosten LA, Koenders MI, Smeets RL, et al.: Toll-like receptor 2 pathway drives streptococcal cell wall-induced joint inflammation: critical role of myeloid differentiation factor 88. J Immunol 2003, 171:6145-6153.
66. De Rycke L, Vandooren B, Kruithof E, et al.: Tumor necrosis factor alpha blockade treatment down-modulates the increased systemic and local expression of Toll-like receptor 2 and Toll-like receptor 4 in spondylarthropathy. Arthritis Rheum 2005, 52:2146-2158. This study demonstrates the higher expression of TLR2 and TLR4 in spondylarthritis synovitis compared with rheumatoid arthritis and indicates that the expression and function of TLR is modulated by TNF-α blockade in vivo. This is the first study to identify TLR as central players in spondylarthritis.
67. Termeer C, Benedix F, Sleeman J, et al.: Oligosaccharides of Hyaluronan activate dendritic cells via toll-like receptor 4. J Exp Med 2002, 195:99-111.
68. Johnson GB, Brunn GJ, Kodaira Y, Platt JL: Receptor-mediated monitoring of tissue well-being via detection of soluble heparan sulfate by Toll-like receptor 4. J Immunol 2002, 168:5233-5239.
69. Baeten D, Kruithof E, Van den Bosch F, et al.: Systematic safety follow up in a cohort of 107 patients with spondyloarthropathy treated with infliximab: a new perspective on the role of host defence in the pathogenesis of the disease? Ann Rheum Dis 2003, 62:829-834.
70. Netea MG, Radstake T, Joosten LA, et al.: Salmonella septicemia in rheumatoid arthritis patients receiving antitumor necrosis factor therapy: association with decreased interferon-gamma production and Toll-like receptor 4 expression. Arthritis Rheum 2003, 48:1853-1857.
71. Vandooren B, Kruithof E, Yu DT, et al.: Involvement of matrix metalloproteinases and their inhibitors in peripheral synovitis and down-regulation by tumor necrosis factor alpha blockade in spondylarthropathy. Arthritis Rheum 2004, 50:2942-2953.
72. Ritchlin CT, Haas-Smith SA, Li P, et al.: Mechanisms of TNF-alpha- and RANKL-mediated osteoclastogenesis and bone resorption in psoriatic arthritis. J Clin Invest 2003, 111:821-831.