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Basement membrane proteins in synovial membrane: Distribution in rheumatoid arthritis and synthesis by fibroblast-like cells

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Summary

Rheumatoid arthritis is a complex disease of unknown origin. In consequence of some immunological reactions, proliferative invading synovial tissue leads to destruction of normal joint architecture. The aim of this study was to investigate qualitative changes in extracellular matrix distribution of proliferating rheumatoid synovium and their cellular origin. Synovial tissues from 57 clinically indicated arthrotomies were investigated with immunofluorescence, using specific antibodies against extracellular matrix proteins in tissue slides and cultured cells, which were also studied for collagen biosynthesis. Results indicated that synovial fibroblast-like cells synthesize and secrete basement membrane proteins laminin and collagen type IV as e.g. endothelial cells or organogenic fibroblasts. Laminin and collagen type IV were specifically demonstrated pericellularly in the hyperplastic lining layer of active rheumatoid synovitis. These findings are discussed with respect to the possible implication of altered cell-matrix interactions in rheumatoid synovial proliferation.

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References

  1. Harris, E.D. Pathogenesis of rheumatoid arthritis. In: Textbook of Rheumatology, 3rd ed. Eds.: Kelley et al. Saunders Company, Philadelphia, 1989, 905–942.

    Google Scholar 

  2. Zvaifler, N. New perspectives on the pathogenesis of rheumatoid arthritis. Am J Med 1988, 85 (SA4); 12–17.

    Google Scholar 

  3. Fassbender, H.G. Histomorphological basis of articular cartilage destruction in rheumatoid arthritis. Collagen Rel Res 1983, 3, 141–155.

    Google Scholar 

  4. Dreher, R. Origin of synovial type A cells during inflammation: an experimental approach. Immunobiol 1982, 161, 232–245.

    Google Scholar 

  5. Arend, W.P., Dayer, J-M. Cytokines and cytokine inhibitors or antagonists in rheumatoid arthritis. Arthritis Rheum 1990, 33, 305–313.

    PubMed  Google Scholar 

  6. Firestein, G.S., Zvaifler, N.J. How important are T cells in chronic rheumatoid synovitis? Arthritis Rheum 1990, 33, 768–773.

    PubMed  Google Scholar 

  7. Lipsky, P.E., Davis, L.S., Cush, J.J., Oppenheimer-Marks, N. The role of cytokines in the pathogenesis of rheumatoid arthritis. Springer Semin Immunopathol 1989, 11, 123–162.

    PubMed  Google Scholar 

  8. Henderson, B., Pettipher, E.R. The synovial lining cell: biology and pathobiology. Semin Arthritis Rheumatism 1985, 15, 1–32.

    Google Scholar 

  9. Chin, J.E., Winterrowd, G.E., Krzesicki, R.F., Sanders, M.E. Role of cytokines in inflammatory synovitis. The coordinate regulation of intercellular adhesions molecule 1 and HLA class I and II antigens in rheumatoid synovial fibroblasts. Arthritis Rheum 1990, 33, 1776–1786.

    PubMed  Google Scholar 

  10. Dayer, J.-M., Demczuk, S. Cytokines and other mediators in rheumatoid arthritis. Springer Semin Immunopathol 1984, 7, 387–413.

    PubMed  Google Scholar 

  11. Lipsky, P.E. The control of antibody production by immunomodulatory molecules. Arthritis Rheum 1989, 32, 1345–1353.

    PubMed  Google Scholar 

  12. McCachren, S.S., Greer, P., Niedel, J.E. Regulation of synovial fibroblast collagenase messenger RNA by interleukin-1. Arthritis Rheum 1989, 32, 1539–1545.

    PubMed  Google Scholar 

  13. Yaron, I., Meyer, F., Dayer, J.-M., Bleiberg, I., Yaron, M. Some recombinant human cytokines stimulate glycosaminoglycan synthesis in human synovial fibroblast cultures and inhibit it in human articular cartilage cultures. Arthritis Rheum 1989, 32, 173–180.

    PubMed  Google Scholar 

  14. Bucala, R., Richlin, Ch., Winchester, R., Cerami, A. Constitutive production of inflammatory and mitogenic cytokines by rheumatoid synovial fibroblasts. J Exp Med 1991, 173, 569–574.

    PubMed  Google Scholar 

  15. Dalton, B.J., Connor, J.R., Johnson, W.J. Interleukin-1 induces interleukin -1α and and interleukin-1β gene expression in synovial fibroblasts and peripheral blood monocytes. Arthritis Rheum 1989, 32, 279–287.

    PubMed  Google Scholar 

  16. Tan, P.L.J., Farmiloe, S., Yeoman, S., Watson, J.D. Expression of interleukin 6 gene in rheumatoid synovial fibroblasts. J Rheumatol 1990, 17, 1608–1612.

    PubMed  Google Scholar 

  17. Daireaux, M., Penfornis, H., Langris, M. et al. Effect of a mononuclear cell culture medium on collagen and glycosaminoglycan production by synovial cells in culture. FEBS Lett 1981, 132, 93–97.

    PubMed  Google Scholar 

  18. Gay, S., Gay, R.E. Cellular basis and oncogene expression of rheumatoid joint destruction. Rheumatol Int 1989, 9, 105–113.

    PubMed  Google Scholar 

  19. Krane, S.M., Dayer, J.-M., Simon, L.S., Byrne, M.S. Mononuclear cell-conditioned medium containing mononuclear cell factor, homologous with interleukin-1, stimulates collagen and fibronectin synthesis by adherent rheumatoid synovial cells: effects of prostaglandin E2 and indometacin. Collagen Rel Res 1985, 5, 99–117.

    Google Scholar 

  20. Parrott, D.P., Goldberg, R.L., Kaplan, S.R., Fuller, G.C. The effect of lymphokines on proliferation and collagen synthesis of cultured synovial cells. Eur J Clin Invest 1982, 12, 407–415.

    PubMed  Google Scholar 

  21. Wolf, J., Carsons, S.E. Distribution of type VI collagen expression in synovial tissue and cultured synoviocytes: relation to fibronectin expression. Ann Rheum Dis 1991, 50, 493–496.

    PubMed  Google Scholar 

  22. Miller, E.J., Epstein, E.H., Piez, K.A. Identification of three genetically distinct collagens by cyanogen bromide cleavage of insoluble human skin and cartilage collagen. Biochem Biophys Res Commun 1971, 42, 1029–1049.

    Google Scholar 

  23. Dixit, S.N. Isolation and characterization of two collagenous components from anterior lens capsule. FEBS Lett 1978, 85, 153–157.

    PubMed  Google Scholar 

  24. Rhode, R.K.P., Miller, E.J. Physiochemical characterization and molecular organization of the collagen A and B chains. Biochemistry 1978, 17, 3442–3448.

    PubMed  Google Scholar 

  25. Engvall, E., Ruoslahti, E., Miller, E.J. Affinity of fibronectin to collagens of different genetic types and to fibrinogen. J Exp Med 1978, 147, 1584–1595.

    PubMed  Google Scholar 

  26. Voss, B., Rauterberg, J., Allam, S., et al. Distribution of collagen type I and III and of two collagenous components of basement membranes in human liver. Pathol Res Pract 1980, 170, 50–60.

    Google Scholar 

  27. Voss, B., Rauterberg, J., Pott, G. et al. Nonparenchymal cells cultivated from explants of fibrotic liver resemble endothelial and smooth muscle cells from blood vessel walls. Hepatol 1982, 2, 19–28.

    Google Scholar 

  28. Rauterberg, J., Allam, S., Brehmer, U., Wirth, W., Hauss, W. Characterization of the collagen synthesized by cultured human smooth muscle cells from fetal and adult aorta. Hoppe Seylers Z Physiol Chem 1977, 358, 401–407.

    PubMed  Google Scholar 

  29. Cutolo, M., Picasso, M., Ponassi, M., Sun, M.Z., Balza, E. Tenascin and fibronectin distribution in human normal and pathological synovium. J Rheumatol 1992, 19, 1439–1447.

    PubMed  Google Scholar 

  30. Levick, J.R., McDonald, J.N. Microfibrillar meshwork of the synovial lining and associated broad banded collagen: a clue to identity. Ann Rheum Dis 1990, 49, 31–36.

    PubMed  Google Scholar 

  31. Matsubara, T., Velvart, M., Odermatt, B.F., Spycher, M.A., Rüttner, J.R., Fehr, K. The thickening of basement membrane in synovial capillaries in rheumatoid arthritis. Rheumatol Int 1983, 3, 57–64.

    PubMed  Google Scholar 

  32. Scott, D.L., Salmon, M., Morris, C.J., Wainwright, A.C., Walton, K.W. Laminin and vascular proliferation in rheumatoid arthritis. Ann Rheum Dis 1984, 43, 551–555.

    PubMed  Google Scholar 

  33. Pollock, L.E., Lalor, P., Revell, P.A. Type IV collagen and laminin in the synovial mitimal layer: an immunohistochemical study. Rheumatol Int 1990, 9, 277–280.

    PubMed  Google Scholar 

  34. Kramer, R.H., Fuh, G.-M. Type IV collagen synthesis by cultured human microvascular endothelial cells and its deposition into the subendothelial basement membrane. Biochemistry 1985, 24, 7423–7430.

    PubMed  Google Scholar 

  35. Olsen, D.R., Uitto, J. Differential expression of type IV procollagen and laminin genes by fetal vs adult skin fibroblasts in culture. Determination of subunit mRNA steady-state levels. J Invest Dermatol 1988, 93, 127–131.

    Google Scholar 

  36. Woodley, D.T., Stanley, J.R., Reese, M.J., O'Keefe, E.J. Human dermal fibroblasts synthesize laminin. J Invest Dermatol 1989, 90, 679–683.

    Google Scholar 

  37. Okada, Y., Naka, K., Minamoto, T. et al. Localization of type VI collagen in the lining cell layer of normal and rheumatoid synovium. Lab Invest 1990, 63, 647–656.

    PubMed  Google Scholar 

  38. Howard, P.S., Myers, J.C., Gorfien, S.F., Macarak, E.J. Progressive modulation of endothelial phenotype during in vitro blood vessel formation. Dev Biol 1991, 146, 325–338.

    PubMed  Google Scholar 

  39. Hamilton, J.A., Picolli, D.S., Leizer, T., Butler, D.M., Croatto, M., Royston, A.K.M. Transforming growth factor β stimulates urokinase-type plasminogen activator and DNA synthesis, but not prostaglandin E2 production, in human synovial fibroblasts. Proc Natl Acad Sci USA 1991, 88, 7180–7184.

    PubMed  Google Scholar 

  40. Carlsson, R., Engvall, E., Freeman, A., Ruoslahti, E. Laminin and fibronectin in cell adhesion: enhanced adhesion of cells from regenerating liver to laminin. Proc Natl Acad Sci USA 1981, 78, 2403–2406.

    PubMed  Google Scholar 

  41. Toyota, B., Carbonetto, S., David, S. A dual laminin/collagen receptor acts in peripheral nerve regeneration. Proc Natl Acad Sci USA 1990, 87, 1319–1322.

    PubMed  Google Scholar 

  42. Hoyt, D.G., Lazo, J.S. Bleomycin and cyclophosphamide increase pulmonary type IV collagen mRNA in mice. Am J Physiol 1990, 259, L47-L52.

    PubMed  Google Scholar 

  43. Ingber, D.E., Folkman, J. How does extracellular matrix control capillary morphogenesis? Cell 1989, 58, 803–805.

    PubMed  Google Scholar 

  44. Ingber, D.E., Folkman, J. Mechanochemical switching between growth and differentiation during fibroblast growth factor-stimulated angiogenesis in vitro, role of extracellular matrix. J Cell Biol 1989, 109, 317–330.

    PubMed  Google Scholar 

  45. Nicosia, R.F., Ottinetti, A. Modulation of microvascular growth and morphogenesis by reconstituted basement membrane gel in three-dimensional cultures of rat aorta: a comparative study of angiogenesis in matrigel, collagen, fibrin, and plasma clot. In Virto Cell Dev Biol 1990, 26, 119–128.

    Google Scholar 

  46. Dinther-Janssen van, A.C.H.M., Pals, S.T., Scheper, R., Breedveld, F., Meijer, C.J.L.M. Dendritic cells and high endothelial venules in rheumatoid synovial membrane. J Rheumatol 1990, 17, 11–17.

    PubMed  Google Scholar 

  47. Harper, G.P. Leukocyte-endothelial interaction. Agents and Actions 1989, 28, 235–237.

    PubMed  Google Scholar 

  48. Osborn, L. Leukocyte adhesion to endothelium in inflammation. Cell 1990, 62, 3–6.

    PubMed  Google Scholar 

  49. Sheehan, N.J., Brown, K.A., Perry, J.D., Chasty, R.C., Yates, D.A.H., Dumonde, D.C. Adherence of rheumatoid polymorphonuclear cells to cultured endothelial cell monolayers. Ann Rheum Dis 1987, 46, 93–97.

    PubMed  Google Scholar 

  50. Ziff, M. Pathways of mononuclear cell infiltration in rheumatoid synovitis. Rheumatol Int 1989, 9, 97–103.

    PubMed  Google Scholar 

  51. Kleinman, H.K., McGarvey, M.L., Hassell, J.R. et al. Basement membrane complexes with biological activity. Biochemistry 1985, 25, 312–318.

    Google Scholar 

  52. Panayotou, G., End, P., Aumailley, M., Timpl, R., Engel, J. Domains of laminin with growth factor activity. Cell 1989, 56, 93–101.

    PubMed  Google Scholar 

  53. Paralkar, V.M., Vukicevic, S., Reddi, H. Transforming growth factor β type I binds to collagen IV of basement membrane matrix: implications for development. Dev Biol 1991, 143, 303–308.

    PubMed  Google Scholar 

  54. Humphries, M.J., Yamada, K.M. Non-collagenous glycoproteins. Rheumatology 1986, 10, 104–142.

    Google Scholar 

  55. Ekblom, P., Alitalo, K., Vaheri, A., Timpl, R., Saxen, L. Induction of a basement membrane glycoprotein in embryonic kidney: possible role of laminin in morphogenesis. Proc Natl Acad Sci USA 1990, 77, 485–489.

    Google Scholar 

  56. Gelly, J.L., Richoux, J.P., Leheup, B.P., Grignon, G. Immunolocalization of type IV collagen and laminin during rat gonadal morphogenesis and postnatal development of the testis and epididymis. Histochem 1989, 93, 31–37.

    Google Scholar 

  57. Schuger, L., O'Shea, S., Rheinheimer, J., Varani, J. Laminin in lung development: Effects of anti-laminin antibody in murine lung morphogenesis. Dev Biol 1990, 137, 26–32.

    PubMed  Google Scholar 

  58. Shah, K.D., Gerber, M.A. Development of intrahepatic bile ducts in humans. Arch Pathol Lab Med 1990, 114, 597–600.

    PubMed  Google Scholar 

  59. Emonard, H., Christiane, Y., Munaut, C., Foidart, J.M. Reconstituted basement membrane matrix stimulates interstitial procollagenase synthesis by human fibroblasts in culture. Matrix 1990, 10, 373–377.

    PubMed  Google Scholar 

  60. Bohnsack, J.F., Akiyama, S.K., Damsky, C.H., Knape, W.A., Zimmerman, G.A. Human neutrophil adherence to laminin in vitro. J Exp Med 1990, 171, 1221–1237.

    PubMed  Google Scholar 

  61. Campbell, J.H., Terranova, V.P. Laminin: Molecular organization and biological function. J Oral Pathol 1988, 17, 309–323.

    PubMed  Google Scholar 

  62. Stallmach, A., Schuppan, D., Dax, J., Hanski, C., Riecken, E.O. Identification of laminin binding proteins in cell membranes of a human colon adenocarcinoma cell line. Gut 1990, 31, 70–76.

    PubMed  Google Scholar 

  63. Terranova, V.P., Liotta, L.A., Russo, R.G., Martin, G.R. Role of laminin in the attachment and metastasis of murine tumor cells. Cancer Res 1982, 42, 2265–2269.

    PubMed  Google Scholar 

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Schneider, M., Voss, B., Rauterberg, J. et al. Basement membrane proteins in synovial membrane: Distribution in rheumatoid arthritis and synthesis by fibroblast-like cells. Clin Rheumatol 13, 90–97 (1994). https://doi.org/10.1007/BF02229873

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