Best Practice & Research Clinical Rheumatology
Volume 25, Issue 6 , Pages 767-777 , December 2011

The synovium as a privileged site in rheumatoid arthritis: Cadherin-11 as a dominant player in synovial pathology

References 

  1. Firestein GS. Evolving concepts of rheumatoid arthritis. Nature. 2003;423:356–361
  2. Mor A, Abramson SB, Pillinger MH. The fibroblast-like synovial cell in rheumatoid arthritis: a key player in inflammation and joint destruction. Clinical Immunology. 2005;115:118–128
  3. Pitsillides AA, Wilkinson LS, Mehdizadeh S, Bayliss MT, Edwards JC. Uridine diphosphoglucose dehydrogenase activity in normal and rheumatoid synovium: the description of a specialized synovial lining cell. International Journal of Experimental Pathology. 1993;74:27–34
  4. Chang HY, Chi JT, Dudoit S, Bondre C, van de Rijn M, Botstein D, et al. Diversity, topographic differentiation, and positional memory in human fibroblasts. Proceedings of the National Academy of Sciences USA. 2002;99:12877–12882
  5. Allard SA, Bayliss MT, Maini RN. The synovium-cartilage junction of the normal human knee. Implications for joint destruction and repair. Arthritis and Rheumatism. 1990;33:1170–1179
  6. Hamerman D, Barland P. Structure and function of the synovial membrane. British Journal of Rheumatology. 1966;16:396–399
  7. Barland P, Novikoff AB, Hamerman D. Electron microscopy of the human synovial membrane. Journal of Cell Biology. 1962;14:207–220
  8. De Bari C, Dell’Accio F, Tylzanowski P, Luyten FP. Multipotent mesenchymal stem cells from adult human synovial membrane. Arthritis and Rheumatism. 2001;44:1928–1942
  9. Hermida-Gomez T, Fuentes-Boquete I, Gimeno-Longas MJ, Muinos-Lopez E, Diaz-Prado S, de Toro FJ, et al. Quantification of cells expressing mesenchymal stem cell markers in healthy and osteoarthritic synovial membranes. Journal of Rheumatology. 2011;38:339–349
  10. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, et al. Multilineage potential of adult human mesenchymal stem cells. Science. 1999;284:143–147
  11. Athanasou NA. Synovial macrophages. Annals of the Rheumatic Diseases. 1995;54:392–394
  12. Koch AE, Burrows JC, Skoutelis A, Marder R, Domer PH, Anderson B, et al. Monoclonal antibodies detect monocyte/macrophage activation and differentiation antigens and identify functionally distinct subpopulations of human rheumatoid synovial tissue macrophages. American Journal of Pathology. 1991;138:165–173
  13. Morales-Ducret J, Wayner E, Elices MJ, Alvaro-Gracia JM, Zvaifler NJ, Firestein GS. Alpha 4/beta 1 integrin (VLA-4) ligands in arthritis. Vascular cell adhesion molecule-1 expression in synovium and on fibroblast-like synoviocytes. Journal of Immunology. 1992;149:1424–1431
  14. Stevens CR, Mapp PI, Revell PA. A monoclonal antibody (Mab 67) marks type B synoviocytes. Rheumatology International. 1990;10:103–106
  15. Rhee DK, Marcelino J, Baker M, Gong Y, Smits P, Lefebvre V, et al. The secreted glycoprotein lubricin protects cartilage surfaces and inhibits synovial cell overgrowth. Journal of Clinical Investigation. 2005;115:622–631
  16. Hamann J, Wishaupt JO, van Lier RA, Smeets TJ, Breedveld FC, Tak PP. Expression of the activation antigen CD97 and its ligand CD55 in rheumatoid synovial tissue. Arthritis and Rheumatism. 1999;42:650–658
  17. Jay GD, Britt DE, Cha CJ. Lubricin is a product of megakaryocyte stimulating factor gene expression by human synovial fibroblasts. Journal of Rheumatology. 2000;27:594–600
  18. Swann DA, Silver FH, Slayter HS, Stafford W, Shore E. The molecular structure and lubricating activity of lubricin isolated from bovine and human synovial fluids. Biochemical Journal. 1985;225:195–201
  19. Marcelino J, Carpten JD, Suwairi WM, Gutierrez OM, Schwartz S, Robbins C, et al. CACP, encoding a secreted proteoglycan, is mutated in camptodactyly-arthropathy-coxa vara-pericarditis syndrome. Nature Genetics. 1999;23:319–322
  20. Edwards JC, Wilkinson LS. Distribution in human tissues of the synovial lining-associated epitope recognised by monoclonal antibody 67. Journal of Anatomy. 1996;188(Pt 1):119–127
  21. Demaziere A, Athanasou NA. Adhesion receptors of intimal and subintimal cells of the normal synovial membrane. Journal of Pathology. 1992;168:209–215
  22. Kiener HP, Watts GF, Cui Y, Wright J, Thornhill TS, Skold M, et al. Synovial fibroblasts self-direct multicellular lining architecture and synthetic function in three-dimensional organ culture. Arthritis and Rheumatism. 2010;62:742–752
  23. Revell PA, al-Saffar N, Fish S, Osei D. Extracellular matrix of the synovial intimal cell layer. Annals of the Rheumatic Diseases. 1995;54:404–407
  24. Schneider M, Voss B, Rauterberg J, Menke M, Pauly T, Miehlke RK, et al. Basement membrane proteins in synovial membrane: distribution in rheumatoid arthritis and synthesis by fibroblast-like cells. Clinical Rheumatology. 1994;13:90–97
  25. Marsh JM, Wiebkin OW, Gale S, Muir H, Maini RN. Synthesis of sulphated proteoglycans by rheumatoid and normal synovial tissue in culture. Annals of the Rheumatic Diseases. 1979;38:166–170
  26. Pollock LE, Lalor P, Revell PA. Type IV collagen and laminin in the synovial intimal layer: an immunohistochemical study. Rheumatology International. 1990;9:277–280
  27. Mapp PI, Revell PA. Fibronectin production by synovial intimal cells. Rheumatology International. 1985;5:229–237
  28. McCachren SS, Lightner VA. Expression of human tenascin in synovitis and its regulation by interleukin-1. Arthritis and Rheumatism. 1992;35:1185–1196
  29. Yurchenco PD, O’Rear JJ. Basal lamina assembly. Current Opinion in Cell Biology. 1994;6:674–681
  30. Danen EH, Sonneveld P, Brakebusch C, Fassler R, Sonnenberg A. The fibronectin-binding integrins alpha5beta1 and alphavbeta3 differentially modulate RhoA-GTP loading, organization of cell matrix adhesions, and fibronectin fibrillogenesis. Journal of Cell Biology. 2002;159:1071–1086
  31. Ushiki T. Collagen fibers, reticular fibers and elastic fibers. A comprehensive understanding from a morphological viewpoint. Archives of Histology and Cytology. 2002;65:109–126
  32. Firestein GS, Paine MM. Stromelysin and tissue inhibitor of metalloproteinases gene expression in rheumatoid arthritis synovium. American Journal of Pathology. 1992;140:1309–1314
  33. Gravallese EM, Darling JM, Ladd AL, Katz JN, Glimcher LH. In situ hybridization studies of stromelysin and collagenase messenger RNA expression in rheumatoid synovium. Arthritis and Rheumatism. 1991;34:1076–1084
  34. Cunnane G, FitzGerald O, Hummel KM, Gay RE, Gay S, Bresnihan B. Collagenase, cathepsin B and cathepsin L gene expression in the synovial membrane of patients with early inflammatory arthritis. Rheumatology (Oxford). 1999;38:34–42
  35. Konttinen YT, Ainola M, Valleala H, Ma J, Ida H, Mandelin J, et al. Analysis of 16 different matrix metalloproteinases (MMP-1 to MMP-20) in the synovial membrane: different profiles in trauma and rheumatoid arthritis. Annals of the Rheumatic Diseases. 1999;58:691–697
  36. Close DR. Matrix metalloproteinase inhibitors in rheumatic diseases. Annals of the Rheumatic Diseases. 2001;60(Suppl. 3):iii62-7
  37. Valencia X, Higgins JM, Kiener HP, Lee DM, Podrebarac TA, Dascher CC, et al. Cadherin-11 provides specific cellular adhesion between fibroblast-like synoviocytes. Journal of Experimental Medicine. 2004;200:1673–1679
  38. Kiener HP, Lee DM, Agarwal SK, Brenner MB. Cadherin-11 induces rheumatoid arthritis fibroblast-like synoviocytes to form lining layers in vitro. American Journal of Pathology. 2006;168:1486–1499
  39. Lee DM, Kiener HP, Agarwal SK, Noss EH, Watts GF, Chisaka O, et al. Cadherin-11 in synovial lining formation and pathology in arthritis. Science. 2007;315:1006–1010
  40. Schumacher HR, Kitridou RC. Synovitis of recent onset. A clinicopathologic study during the first month of disease. Arthritis and Rheumatism. 1972;15:465–485
  41. Henderson B, Pettipher ER. The synovial lining cell: biology and pathobiology. Seminars in Arthritis and Rheumatism. 1985;15:1–32
  42. Hollywell C, Morris CJ, Farr M, Walton KW. Ultrastructure of synovial changes in rheumatoid disease and in seronegative inflammatory arthropathies. Virchows Archiv A Pathological Anatomy and Histopathology. 1983;400:345–355
  43. Takemura S, Braun A, Crowson C, Kurtin PJ, Cofield RH, O’Fallon WM, et al. Lymphoid neogenesis in rheumatoid synovitis. Journal of Immunology. 2001;167:1072–1080
  44. Koch AE. Review: angiogenesis: implications for rheumatoid arthritis. Arthritis and Rheumatism. 1998;41:951–962
  45. Gumbiner BM. Cell adhesion: the molecular basis of tissue architecture and morphogenesis. Cell. 1996;84:345–357
  46. Takeichi M, Nakagawa S, Aono S, Usui T, Uemura T. Patterning of cell assemblies regulated by adhesion receptors of the cadherin superfamily. Philosophical Transactions of the Royal Society B: Biological Sciences. 2000;355:885–890
  47. Tanihara H, Sano K, Heimark RL, St John T, Suzuki S. Cloning of five human cadherins clarifies characteristic features of cadherin extracellular domain and provides further evidence for two structurally different types of cadherin. Cell Communication and Adhesion. 1994;2:15–26
  48. Nelson WJ. Regulation of cell-cell adhesion by the cadherin-catenin complex. Biochemical Society Transactions. 2008;36:149–155
  49. Takeichi M. Cadherin cell adhesion receptors as a morphogenetic regulator. Science. 1991;251:1451–1455
  50. Chen CP, Posy S, Ben-Shaul A, Shapiro L, Honig BH. Specificity of cell-cell adhesion by classical cadherins: critical role for low-affinity dimerization through beta-strand swapping. Proceedings of the National Academy of Sciences USA. 2005;102:8531–8536
  51. Huber AH, Weis WI. The structure of the beta-catenin/E-cadherin complex and the molecular basis of diverse ligand recognition by beta-catenin. Cell. 2001;105:391–402
  52. Yamada S, Pokutta S, Drees F, Weis WI, Nelson WJ. Deconstructing the cadherin-catenin-actin complex. Cell. 2005;123:889–901
  53. Weis WI, Nelson WJ. Re-solving the cadherin-catenin-actin conundrum. Journal of Biological Chemistry. 2006;281:35593–35597
  54. Drees F, Pokutta S, Yamada S, Nelson WJ, Weis WI. Alpha-catenin is a molecular switch that binds E-cadherin-beta-catenin and regulates actin-filament assembly. Cell. 2005;123:903–915
  55. Vasioukhin V, Bauer C, Yin M, Fuchs E. Directed actin polymerization is the driving force for epithelial cell-cell adhesion. Cell. 2000;100:209–219
  56. Braga VM, Machesky LM, Hall A, Hotchin NA. The small GTPases Rho and Rac are required for the establishment of cadherin-dependent cell-cell contacts. Journal of Cell Biology. 1997;137:1421–1431
  57. Piedra J, Martinez D, Castano J, Miravet S, Dunach M, de Herreros AG. Regulation of beta-catenin structure and activity by tyrosine phosphorylation. Journal of Biological Chemistry. 2001;276:20436–20443
  58. Baki L, Marambaud P, Efthimiopoulos S, Georgakopoulos A, Wen P, Cui W, et al. Presenilin-1 binds cytoplasmic epithelial cadherin, inhibits cadherin/p120 association, and regulates stability and function of the cadherin/catenin adhesion complex. Proceedings of the National Academy of Sciences of the United States of America. 2001;98:2381–2386
  59. Ireton RC, Davis MA, van Hengel J, Mariner DJ, Barnes K, Thoreson MA, et al. A novel role for p120 catenin in E-cadherin function. Journal of Cell Biology. 2002;159:465–476
  60. Fujita Y, Krause G, Scheffner M, Zechner D, Leddy HE, Behrens J, et al. Hakai, a c-Cbl-like protein, ubiquitinates and induces endocytosis of the E-cadherin complex. Nature Cell Biology. 2002;4:222–231
  61. Kiener HP, Stipp CS, Allen PG, Higgins JM, Brenner MB. The cadherin-11 cytoplasmic juxtamembrane domain promotes alpha-catenin turnover at adherens junctions and intercellular motility. Molecular Biology of the Cell. 2006;17:2366–2376
  62. Kimura Y, Matsunami H, Inoue T, Shimamura K, Uchida N, Ueno T, et al. Cadherin-11 expressed in association with mesenchymal morphogenesis in the head, somite, and limb bud of early mouse embryos. Developmental Biology. 1995;169:347–358
  63. Locascio A, Nieto MA. Cell movements during vertebrate development: integrated tissue behaviour versus individual cell migration. Current Opinion in Genetics and Development. 2001;11:464–469
  64. Pishvaian MJ, Feltes CM, Thompson P, Bussemakers MJ, Schalken JA, Byers SW. Cadherin-11 is expressed in invasive breast cancer cell lines. Cancer Research. 1999;59:947–952
  65. Tomita K, van Bokhoven A, van Leenders GJ, Ruijter ET, Jansen CF, Bussemakers MJ, et al. Cadherin switching in human prostate cancer progression. Cancer Research. 2000;60:3650–3654
  66. Onder TT, Gupta PB, Mani SA, Yang J, Lander ES, Weinberg RA. Loss of E-cadherin promotes metastasis via multiple downstream transcriptional pathways. Cancer Research. 2008;68:3645–3654
  67. Seidensticker MJ, Behrens J. Biochemical interactions in the wnt pathway. Biochimica et Biophysica Acta. 2000;1495:168–182
  68. Gradl D, Kuhl M, Wedlich D. The Wnt/Wg signal transducer beta-catenin controls fibronectin expression. Molecular Cell Biology. 1999;19:5576–5587
  69. Pan FY, Zhang SZ, Xu N, Meng FL, Zhang HX, Xue B, et al. Beta-catenin signaling involves HGF-enhanced HepG2 scattering through activating MMP-7 transcription. Histochemistry and Cell Biology. 2010;134:285–295
  70. Noren NK, Liu BP, Burridge K, Kreft B. p120 catenin regulates the actin cytoskeleton via Rho family GTPases. Journal of Cell Biology. 2000;150:567–580
  71. Nobes CD, Hall A. Rho GTPases control polarity, protrusion, and adhesion during cell movement. Journal of Cell Biology. 1999;144:1235–1244
  72. Daniel JM, Reynolds AB. The catenin p120(ctn) interacts with Kaiso, a novel BTB/POZ domain zinc finger transcription factor. Molecular Cell Biology. 1999;19:3614–3623
  73. Wong AS, Gumbiner BM. Adhesion-independent mechanism for suppression of tumor cell invasion by E-cadherin. Journal of Cell Biology. 2003;161:1191–1203
  74. Kiener HP, Niederreiter B, Lee DM, Jimenez-Boj E, Smolen JS, Brenner MB. Cadherin 11 promotes invasive behavior of fibroblast-like synoviocytes. Arthritis and Rheumatism. 2009;60:1305–1310
  75. Hoffmann I, Balling R. Cloning and expression analysis of a novel mesodermally expressed cadherin. Developmental Biology. 1995;169:337–346
  76. Kawaguchi J, Takeshita S, Kashima T, Imai T, Machinami R, Kudo A. Expression and function of the splice variant of the human cadherin-11 gene in subordination to intact cadherin-11. Journal of Bone and Mineral Research. 1999;14:764–775
  77. Shibata T, Ochiai A, Gotoh M, Machinami R, Hirohashi S. Simultaneous expression of cadherin-11 in signet-ring cell carcinoma and stromal cells of diffuse-type gastric cancer. Cancer Letters. 1996;99:147–153
  78. Chen GT, Getsios S, MacCalman CD. Cadherin-11 is a hormonally regulated cellular marker of decidualization in human endometrial stromal cells. Molecular Reproduction and Development. 1999;52:158–165
  79. Nobes CD, Hall A. Rho, rac, and cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell. 1995;81:53–62
  80. Vandooren B, Cantaert T, ter Borg M, Noordenbos T, Kuhlman R, Gerlag D, et al. Tumor necrosis factor alpha drives cadherin 11 expression in rheumatoid inflammation. Arthritis and Rheumatism. 2008;58:3051–3062
  81. Noss EH, Brenner MB. The role and therapeutic implications of fibre oblast-like synoviocytes in inflammation and cartilage erosion in rheumatoid arthritis. Immunology Review. 2008;223:252–270
  82. Chang SK, Noss EH, Chen M, Gu Z, Townsend K, Grenha R, et al. Cadherin-11 regulates fibroblast inflammation. Proceedings of the National Academy of Sciences of the United States of America. 2011;108:8402–8407

PII: S1521-6942(11)00168-9

doi: 10.1016/j.berh.2011.11.012

Best Practice & Research Clinical Rheumatology
Volume 25, Issue 6 , Pages 767-777 , December 2011

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