Leukocyte Adhesion to Endothelium

  • Martin H. Thornhill
  • Dorian O. Haskard
Part of the Blood Cell Biochemistry book series (BLBI, volume 5)

Abstract

The recruitment of leukocytes from the blood is a prerequisite for their participation in inflammatory responses within the tissues. In the case of monocytes, a low level of emigration takes place under physiological conditions, but this is greatly increased in the inflammatory setting. An analysis of mechanisms of monocyte—endothelial cell (EC) adhesion is therefore of great relevance to understanding the pathophysiology of diverse acute and chronic inflammatory conditions as well as that of wound healing and tissue repair.

Keywords

Human Endothelial Cell Leukocyte Adhesion Monocyte Migration Leukocyte Adhesion Molecule Leukocyte Adhesion Deficiency 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Albelda, S. M., and Buck, C. A., 1990, Integrins and other cell adhesion molecules, FASEB J. 4: 2868–2880.PubMedGoogle Scholar
  2. Alderson, L. M., Endemann, G., Lindsey, S., Pronczuk, A., Hoover, R. L., and Hayes, K. C., 1986, LDL enhances monocyte adhesion to endothelial cells, Am. J. Pathol. 123: 334–342.PubMedGoogle Scholar
  3. Anderson, D. C., Schmalstieg, F., Finegold, M. J., Hughes, B. J., Rothlein, R., Miller, L. J., Kohl, S., Tosi, M. F., Jacobs, R. L., Waldrop, T. C., Goldman, A. S., Shearer, W. T., and Springer, T. A., 1985, The severe and moderate phenotypes of heritable Mac-1, LFA-1 deficiency: Their quantitative definition and relation to leukocyte dysfunction and clinical features, J. Infect. Dis. 152: 668–689.PubMedCrossRefGoogle Scholar
  4. Arfors, K. E., Lundberg, C., Lindbom, L., Lundberg, K., Beatty, P. G., and Harlan, J. M., 1987, A monoclonal antibody to the membrane glycoprotein complex CD18 inhibits polymorphonuclear leukocyte accumulation and plasma leakage in vivo, Blood 69: 338–340.PubMedGoogle Scholar
  5. Amaout, M. A., Lanier, L. L., and Faller, D. V., 1988. Relative contribution of the leukocyte molecules Mo 1, LFA-1, and p150,95 (LeuM5) in adhesion of granulocytes and monocytes to vascular endothelium is tissue-and stimulus-specific, J. Cell. Physiol. 137: 305–309.CrossRefGoogle Scholar
  6. Atherton, A., and Born, G. V. R., 1972, Quantitative investigations of the adhesiveness of circulating polymorphonuclear leukocytes to blood vessel walls, J. Physiol. 222: 447–474.PubMedGoogle Scholar
  7. Beekhuizen, H., Corsèl-van Tilburg, A. J., and van Furth, R., 1990, Characterization of monocyte adher- ence to human macrovascular and microvascular endothelial cells, J. Immunol. 145: 510–518.PubMedGoogle Scholar
  8. Beekhuizen, H., Blokland, I., Corsèl-van Tilburg, A. J., Koning, F., and van Furth, R., 1991, CD14 contributes to the adherence of human monocytes to cytokine-stimulated endothelial cells, J. Immunol. 147: 3761–3767.PubMedGoogle Scholar
  9. Berliner, J. A., Territo, M. C., Sevanian, A., Ramin, S., Kim, J. A., Bamshad, B., Esterson. M., and Fogelman, A. M., 1990, Minimally modified low density lipoprotein stimulates monocyte endothelial interactions, J. Clin. Invest. 85: 1260–1266.Google Scholar
  10. Berman, C. L., Yeo, E. L., Wencel-Drake, J. D., Furie, B. C., Ginsberg, M. H., and Furie, B. 1986, A platelet alpha granule membrane protein that is associated with the plasma membrane after activation, J. Clin. Invest. 78: 130–137.PubMedCrossRefGoogle Scholar
  11. Bevilacqua, M. P., Pober, J. S., Wheeler, M. E., Cotran, R. S., and Gimbrone, M. A., 1985, Interleukin I acts on cultured human vascular endothelium to increase the adhesion of polymorphonuclear leukocytes, monocytes, and related cell lines, J. Clin. Invest. 76: 2003–2011.PubMedCrossRefGoogle Scholar
  12. Bevilacqua, M. P., Pober, J. S., Mendrick, D. L., Cotran, R. S., and Gimbrone, M. A., 1987, Identification of an inducible endothelial-leukocyte adhesion molecule, Proc. Natl. Acad. Sci. USA 84: 9238–9242.PubMedCrossRefGoogle Scholar
  13. Bevilacqua, M. P., Stengelin, S., Gimbrone, M. A., and Seed, B., 1989, Endothelial leukocyte adhesion molecule L: An inducible receptor for neutrophils related to complement regulatory proteins and lectins, Science 243: 1160–1 164.Google Scholar
  14. Bevilacqua, M., Butcher, E., Furie, B., Gallatin, M., Gimbrone, M., Harlan, J., Kishimoto, K., Lasky, L., McEver, R., Paulson, J., Rosen, S., Seed, B., Siegelman, M., Springer, T., Stoolman, L., Tedder, T., Varki, A., Wagner, D., Weissman, I., and Zimmerman, G., 1991, Selectins: A family of adhesion receptors, Cell 67: 233.PubMedCrossRefGoogle Scholar
  15. Bochner, B. S., Peachell, P. T., Brown, K. E., and Schleimer, R. P., 1988, Adherence of basophils to cultured umbilical vein endothelial cells, J. Clin. Invest. 81: 1355–1364.PubMedCrossRefGoogle Scholar
  16. Bochner, B. S., Luskinskas, F. W., Gimbrone, M. A. J., Newman, W., Sterbinsky, S. A., Derse-Anthony, C. P., Klunk, D., and Schleimer, R. P., 1991, Adhesion of human basophils, eosinophils, and neutrophils to IL-1-activated human vascular endothelial cells: Contributions of endothelial cell adhesion molecules, J. Exp. Med. 173: 1553–1556.PubMedCrossRefGoogle Scholar
  17. Cai, J.-P., Falanga, V., and Chin, Y.-H., 1991, Transforming growth factor-a regulates the adhesive interactions between mononuclear cells and microvascular endothelium, J. Invest. Dermatol. 97: 169–174.PubMedCrossRefGoogle Scholar
  18. Carlos, T. M., and Harlan, J. M., 1990, Membrane proteins involved in phagocyte adherence to endothelium, Immunol. Rev. 114: 5–29.PubMedCrossRefGoogle Scholar
  19. Carlos, T. M., Dobrina, A., Ross, R., and Harlan, J. M., 1988, Multiple receptors on monocytes are involved in adhesion to human endothelial cells in culture, Blood 72 (Sl): 483.Google Scholar
  20. Carlos, T., Kovach, N., Schwartz, B., Rosa, M., Newman, B., Wayner, E., Benjamin, C., Osborn, L., Lobb, R., and Harlan, J., 1991, Human monocytes bind to two cytokine-induced adhesive ligands on cultured human endothelial cells: Endothelial-leukocyte adhesion molecule-I and vascular cell adhesion molecule-1, Blood 77: 2266–2271.PubMedGoogle Scholar
  21. Cathcart, M. K., Morel, D. W., and Chisolm, G. M. I., 1985, Monocytes and neutrophils oxidise low density lipoprotein making it cytotoxic, J. Leukocyte Biol. 38: 341–350.PubMedGoogle Scholar
  22. Cavender, D. E., Haskard, D. O., Joseph, B., and Ziff, M., 1986, Interleukin-1 increases the binding of human B and T lymphocytes to endothelial cell monolayers, J. Immunol. 136: 203–207.PubMedGoogle Scholar
  23. Cavender, D. E., Saegusa, Y., and Ziff, M., 1987, Stimulation of endothelial cell binding of lymphocytes by tumor necrosis factor, J. Immunol. 139: 1855–1860.PubMedGoogle Scholar
  24. Clauss, M., Gerlach, M., Gerlach, H., Brett, J., Wang, F., Familletti, P. C., Pan, Y.-C. E., Olander, J. V., Connolly, D. T., and Stern, D., 1990, Vascular permeability factor: A tumor-derived polypeptide that induces endothelial cell and monocyte procoagulant activity, and promotes monocyte migration, J. Exp. Med. 172: 1535–1545.PubMedCrossRefGoogle Scholar
  25. Cohnheim, J., 1889, in Lectures in General Pathology (J. Cohnheim, ed.), pp. 242–382, New Sydenham Society, London.Google Scholar
  26. Colvin, R. B., and Dvorak, H. F., 1975, Role of the clotting system in cell-mediated hypersensitivity: II. Kinetics of fibrinogen/fibrin accumulation and vascular permeability changes in tuberculin and cutaneous basophil hypersensitivity reactions, J. Immunol. 114: 377–387.PubMedGoogle Scholar
  27. Corkill, M. M., Kirkham, B. W., Haskard, D. O., Barbatis, C., Gibson, T., and Panayi, G. S., 1991, Gold treatment of rheumatoid arthritis decreases synovial expression of the endothelial leukocyte adhesion receptor ELAM-1, J. Rheumatol. 18: 1453–1460.PubMedGoogle Scholar
  28. Cotran, R. S., Gimbrone, M. A., Bevilacqua, M. P., Mendrick, D. L., and Pober, J. S., 1986, Induction and detection of a human endothelial activation antigen in vivo, J. Exp. Med. 164: 661–666.PubMedCrossRefGoogle Scholar
  29. Cushing, S. D., Berliner, J. A., Valente, A. J., Territo, M. C., Navab, M., Parhami, F., Gerrity, R., Schwartz, C. J., and Fogelman, A. M., 1990, Minimally modified low density lipoprotein induces monocyte chemotactic protein 1 in human endothelial cells and smooth muscle cells, Proc. Natl. Acad. Sci. USA 87: 5134–5138.PubMedCrossRefGoogle Scholar
  30. Cybulsky, M. I., and Gimbrone, M. A., 1991, Endothelial expression of a mononuclear leukocyte adhesion molecule during atherogenesis, Science 251: 788–791.PubMedCrossRefGoogle Scholar
  31. Cybulsky, M. I., Fries, J. W. U., Williams, A. J., Sultan, P., Davis, V. M., Gimbrone, M. A., Jr., and Collins, T., 1991, Alternative splicing of human VCAM-1 in activated vascular endothelium, Am. J. Pathol. 138: 815–820.PubMedGoogle Scholar
  32. De Bono, D. P., and Green, C., 1984, The adhesion of different cell types to cultured vascular endothelium: Effects of culture density and age, Br. J. Exp. Pathol. 65: 145–154.PubMedGoogle Scholar
  33. de Fougerolles, A. R., Stacker, S. A., Schwarting, R., and Springer, T. A., 1991, Characterization of ICAM-2 and evidence for a third counter-receptor for LFA-1, J. Exp. Med. 174: 253–267.PubMedCrossRefGoogle Scholar
  34. Diamond, M. S., Staunton, D. E., de Fougerolles, A. R., Stacker, S. A., Garcia-Aguilar, J., Hibbs, M. L., and Springer, T. A., 1990, ICAM-1 (CD54): A counter-receptor for Mac-1 (CD 1 1 b/CD18), J. Cell Biol. 111: 3129–3139.PubMedCrossRefGoogle Scholar
  35. Diamond, M. S., Staunton, D. E., Marlin, S. D., and Springer, T. A., 1991, Binding of the integrin Mac-1 (CD 11b/CD18) to the third immunoglobulin-like domain of ICAM-1 (CD54) and its regulation by glycosylation, Cell 65: 961–971.PubMedCrossRefGoogle Scholar
  36. DiCorleto, P. E., and de la Motte, C. A., 1985, Characterization of the adhesion of the human monocytic cell line U937 to cultured endothelial cells, J. Clin. Invest. 75: 1153–1161.PubMedCrossRefGoogle Scholar
  37. DiCorleto, P. E., and de la Motte, C. A., 1989, Thrombin causes increased monocytic-cell adhesion to endothelial cells through a protein-kinase C-dependent pathway, Biochem. J. 15: 71–77.Google Scholar
  38. Doherty, D. E., Haslett, C., Tonnesar, M. G., and Henson, P. M., 1987, Human monocyte adherence: A primary effect of chemotactic factors on the monocyte to stimulate adherence to human endothelium, J. Immunol. 138: 1762–1771.PubMedGoogle Scholar
  39. Doherty, D. E., Zagarella, L., Henson, P. M., and Worthen, G. S., 1989, Lipopolysaccharide stimulates monocyte adherence by effects on both the monocyte and the endothelial cell, J. Immunol. 143: 3673–3679.PubMedGoogle Scholar
  40. Doukas, J., and Pober, J. S., 1990, IFNy enhances endothelial activation induced by tumor necrosis factor but not IL-1, J. Immunol. 145: 1727–1733.PubMedGoogle Scholar
  41. Downs, E. C., Cornwell, D. G., Proctor, V. K., and Whisler, R. L., 1987, IL 1 and bacterial lipopolysaccharide increase the ability of human endothelial cells to bind peripheral blood monocytes, Lymphokine Res. 6: 351–355.PubMedGoogle Scholar
  42. Dransfield, I., Corcoran, D., Partridge, L. J., Hogg, N., and Burton, D. R., 1988, Comparison of human monocytes isolated by elutriation and adherence suggests that heterogeneity may reflect a continuum of maturation/activation states, Immunology 63: 491–498.PubMedGoogle Scholar
  43. Dransfield, I., Buckle, A.-M., and Hogg, N., 1990, Early events of the immune response mediated by leukocyte integrins, Immunol. Rev. 114: 29–44.PubMedCrossRefGoogle Scholar
  44. Dustin, M. L., and Springer, T. A., 1989, T-cell receptor cross-linking transiently stimulates adhesiveness through LFA-1, Nature (London) 341: 619–624.Google Scholar
  45. Dustin, M. L., Rothlein, R., Bhan, A. K., Dinarello, C. A., and Springer, T. A., 1986, Induction by IL-1 and interferon gamma: Tissue distribution, biochemistry, and function of a natural adherence molecule (ICAM-1), J. Immunol. 137: 245–254.PubMedGoogle Scholar
  46. Edwards, R. L., and Rickles, F. R., 1978, Delayed hypersensitivity in man: Effects of systemic anticoagulation, Science 200: 541–543.PubMedCrossRefGoogle Scholar
  47. Elices, M. J., Osborn, L., Takada, Y., Crouse, C., Luhowsky, S., Hemler, M. E., and Lobb, R. R., 1990, VCAM-1 on activated endothelium interacts with the leukocyte integrin VLA-4 at a site distinct from the VLA-4/fibronectin binding site, Cell 60: 577–584.PubMedCrossRefGoogle Scholar
  48. Elliott, M. J., Vadas, M. A., Cleland, L. G., Gamble, J. R., and Lopez, A. F., 1990, Igranulocyte-macrophage colony-stimulating factor stimulate two distinct phases of adhesion in human monocytes, J. Immunol. 145: 167–176.PubMedGoogle Scholar
  49. Endemann, G., Pronzcuk, A., Friedman, G., Lindsey, S., Alderson, L., and Hayes, K. C., 1987, Monocyte adherence to endothelial cells in vitro is increased by ß-VLDL, Am. J. Pathol. 126: 1–6.PubMedGoogle Scholar
  50. Florey, H. W., and Grant, L. H., 1961, Leucocyte migration from small blood vessels stimulated with ultra-violet light: An electron microscope study, J. Pathol. Bacteriol. 82: 13–17.PubMedCrossRefGoogle Scholar
  51. Freyer, D. R., Morganroth, M. L., Rogers, C. E., Arnaout, M. A., and Todd, R. F., 1988, Modulation of surface CD 11 /CD 18 glycoproteins (Mo 1, LFA-1, p 150,95) by human mononuclear phagocytes, Clin. Immunol. Immunopathol. 46: 272–283.PubMedCrossRefGoogle Scholar
  52. Gallatin, W. M., Weissman, I. L., and Butcher, E. C., 1983, A cell-surface molecule involved in organ-specific homing of lymphocytes, Nature (London) 304: 30–34.Google Scholar
  53. Gamble, J. R., and Vadas, M. A., 1988, Endothelial adhesiveness for blood neutrophils is inhibited by transforming growth factor beta, Science 242: 97–99.PubMedCrossRefGoogle Scholar
  54. Gamble, J. R., and Vadas, M. A., 1991, Endothelial cell adhesiveness for human T lymphocytes is inhibited by transforming growth factor-ß’, J. Immunol. 146: 1149–1154.PubMedGoogle Scholar
  55. Gamble, J. R., Harlan, J. M., Klebanoff, S. J., and Vadas, M. A., 1985, Stimulation of the adherence of neutrophils to umbilical vein endothelium by human recombinant tumour necrosis factor, Proc. Natl. Acad. Sci. USA 82: 8667–8671.PubMedCrossRefGoogle Scholar
  56. Gamble, J. R., Elliott, M. J., Jaipargas, E., Lopez, A. F., and Vadas, M. A., 1989, Regulation of human monocyte adherence by granulocyte-macrophage colony-stimulating factor, Proc. Natl. Acad. Sci. USA 86: 7169–7173.PubMedCrossRefGoogle Scholar
  57. Geng, J.-G., Bevilacqua, M. P., Moore, K. L., McIntyre, T. M., Prescott, S. M., Kim, J. M., Bliss, G. A., Zimmerman, G. A., and McEver, R. P., 1990, Rapid neutrophil adhesion to activated endothelium mediated by GMP-140, Nature (London) 343: 757–760.Google Scholar
  58. Goelz, S. E., Hession, C., Goff, D., Griffiths, B., Tizard, R., Newman, B., Chi-Rosso, G., and Lobb, R., 1990, ELFT: A gene that directs the expression of an ELAM-1 ligand, Cell 61: 1303–1313.CrossRefGoogle Scholar
  59. Goerdt, S., Zwadlo, G., Schlegel, R., Hagemeier, H.-H., and Sorg, C., 1987, Characterization and expression kinetics of an endothelial cell activation antigen in vivo present only in acute inflammatory diseases, Exp. Cell. Biol. 55: 117–126.PubMedGoogle Scholar
  60. Graber, N., Gopal, T. V., Wilson, D., Beall, L. D., Polte, T., and Newman, W., 1990, T cells bind to cytokine-activated endothelial cells via a novel, inducible sialoglycoprotein and endothelial leukocyte adhesion molecule-1, J. Immunol. 145: 819–830.PubMedGoogle Scholar
  61. Griffin, F. M., Griffin, J. A., and Silverstein, S. C., 1976, Studies on the mechanism of phagocytosis: II. The interaction of macrophages with immunoglobulin IgG-coated bone marrow-derived lymphocytes, J. Exp. Med. 144: 788–809.PubMedCrossRefGoogle Scholar
  62. Griffin, J. D., Spertini, O., Ernst, T. J., Belvin, M. P., Levine, H. B., Kananura, Y., and Tedder, T. F., 1990, Granulocyte-macrophage colony-stimulating factor and other cytokines regulate surface expression of the leukocyte adhesion molecule-1 on human neutrophils, monocytes, and their precursors, J. Immunol. 145: 576–584.PubMedGoogle Scholar
  63. Haberland, M. E., Fong, D., and Cheng, L., 1988, Malondialdehyde altered protein occurs in atheroma of WHHL rabbits, Science 241: 215–218.PubMedCrossRefGoogle Scholar
  64. Hakkert, B. C., Rentenaar, J. M., van Aken, W. G., Roos, D., and van Mourik, J. A., 1990, A three-dimensional model system to study the interactions between human leukocytes and endothelial cells, Eur. J. Immunol. 20: 2775–2781.PubMedCrossRefGoogle Scholar
  65. Hakkert, B. C., Kuijpers, T. W., Leeuwenberg, J. F. M., van Mourik, J. A., and Roos, D., 1991, Neutrophil and monocyte adherence to and migration across monolayers of cytokine-activated endothelial cells: The contribution of CD18, ELAM-1, and VLA-4, Blood 78: 2721–2726.PubMedGoogle Scholar
  66. Hale, L. P., Martin, M. E., McCollum, D. E., Nunley, J. A., Springer, T. A., Singer, K. H., and Haynes, B. F., 1989, Immunohistologic analysis of the distribution of cell adhesion molecules within the inflammatory synovial microenvironment, Arthritis Rheum. 32: 22–30.Google Scholar
  67. Hallmann, R., Jutila, M. A., Smith, C. W., Anderson, D. C., Kishimoto, T. K., and Butcher, E. C’., 1991, The peripheral lymph node homing receptor, LECAM-1, is involved in CD18-independent adhesion of human neutrophils to endothelium, Biochem. Biophys. Res. Commun. 174: 236–243.Google Scholar
  68. Haskard, D. O., Cavender, D. E., Beatty, P., Springer, T. A., and Ziff, M., 1986, T cell adhesion to endothelial cells: Mechanisms demonstrated by anti-LFA-1 monoclonal antibodies, J. Immunol. 137: 2901–2906.PubMedGoogle Scholar
  69. Haskard, D. 0., Cavender, D. E., Fleck, R. M., Sontheimer, R., and Ziff, M., 1987, Human dermal microvascular endothelial cells behave like umbilical vein endothelial cells in T cell adhesion studies, J. Invest. Dermatol. 88: 340–344.Google Scholar
  70. Haskard, D. O., Strobel, S., Thornhill, M., Pitzalis, C., and Levinsky, R. J., 1989, Mechanisms of lympho- cyte adhesion to endothelial cells: Studies using a LFA- I deficient cell line, Immunology 66: 111–116.PubMedGoogle Scholar
  71. Hattori, R., Hamilton, K. K., Fugate, R. D., McEver, R. D., and Sims, P. J., 1989a, Stimulated secretion of endothelial von Willebrand factor is accompanied by rapid redistribution to the cell surface of the intracellular granule membrane protein GMP-140, J. Biol. Chem. 264: 7768–7771.PubMedGoogle Scholar
  72. Hattori, R., Hamilton, K. K., McEver, R. P., and Sims, P. J., 1989b, Complement proteins C5b-9 induce secretion of high molecular weight multimers of endothelial von Willebrand factor and translocation of granule membrane protein GMP-140 to the cell surface, J. Biol. Chem. 264: 9053–9060.PubMedGoogle Scholar
  73. Heineck, J. W., Rosen, H., and Chait, A., 1984, Iron and copper promote modification of low density lipoprotein by human arterial smooth muscle cells in culture, J. Clin. Invest. 74: 1890–1894.CrossRefGoogle Scholar
  74. Hession, C., Tizard, R., Vassallo, C., Schiffer, S. B., Goff, D., Moy, P., Chi-Rosso, G., Luhowskyj, S., Lobb, R., and Osborn, L., 1991, Cloning of an alternate form of vascular cell adhesion molecule-1 (VCAM1), J. Biol. Chem. 266: 6682–6685.PubMedGoogle Scholar
  75. Imai, Y., Singer, M. S., Fennie, C., Lasky, L. A., and Rosen, S. D., 1991, Identification of a carbohydrate-based endothelial ligand for a lymphocyte homing receptor, J. Cell Biol. 113: 1213–1222.PubMedCrossRefGoogle Scholar
  76. Issekutz, A. C., and Movat, H. Z., 1980, The in vivo quantification and kinetics of rabbit neutrophil leukocyte accumulation in the skin in response to chemotactic agents and Escherichia coli, Lab. Invest. 42: 310–318.PubMedGoogle Scholar
  77. Issekutz, T. B., Issekutz, A. C., and Movat, H. Z., 1981, The in vivo quantification and kinetics of monocyte migration into acute inflammatory tissue, Am. J. Pathol. 103: 47–55.PubMedGoogle Scholar
  78. Johnston, G. I., Cook, R. G., and McEver, R. P., 1989, Cloning ofGMP-140, a granule membrane protein of platelets and endothelium: Sequence similarity to proteins involved in cell adhesion and inflammation, Cell 56: 1033–1044.PubMedCrossRefGoogle Scholar
  79. Keizer, G. D., to Velde, A., Schwarting, R., Figdor, C. G., and De Vries, J. E., 1987, Role ofp150,95 in adhesion, migration, chemotaxis, and phagocytosis of human monocytes, Eur. J. Immunol. 17: 1317–1322.PubMedCrossRefGoogle Scholar
  80. Kishimoto, T. K., Warnock, R. A., Jutila, M. A., Butcher, E. C., Lane, C., Anderson, D. C., and Smith, C. W., 1991, Antibodies against human neutrophil LECAM-1 (LAM-1/Leu-8/DREG-56 antigen) and endothelial cell ELAM-1 inhibit a common CD I 8-independent adhesion pathway in vitro, Blood 78: 805–811.PubMedGoogle Scholar
  81. Koch, A. E., Burrows, J. C., Haines, G. K., Carlos, T. M., Harlan, J. M., and Leibovich, S. J., 1991, Immunolocalization of endothelial and leukocyte adhesion molecules in human rheumatoid and osteoarthritic synovial tissues, Lab. Invest. 64: 313–320.PubMedGoogle Scholar
  82. Kuijpers, T. W., Hakkert, B. C., van Mourik, J. A., and Roos, D., 1990, Distinct adhesive properties of granulocytes and monocytes to endothelial cells under static and stirred conditions, J. Immunol. 145: 2588–2594.PubMedGoogle Scholar
  83. Kuijpers, T. W., Hakkert, B. C., Hoogerwerf, M., Leeuwenberg, J. F. M., and Roos, D., 1991, Role of endothelial leukocyte adhesion molecule-1 and platelet-activating factor in neutrophil adherence to IL-1-prestimulated endothelial cells: Endothelial leukocyte adhesion molecule-1-mediated CD18 activation, J. Immunol. 147: 1369–1376.PubMedGoogle Scholar
  84. Kyan-Aung, U., Haskard, D. O., Poston, R. N., Thornhill, M. H., and Lee, T. H., 1991, Endothelial leukocyte adhesion molecule- I and intercellular adhesion molecule-1 mediate the adhesion of eosinophils to endothelial cells in vitro and are expressed by endothelium in allergic cutaneous inflammation in vivo, J. Immunol. 146: 521–528.PubMedGoogle Scholar
  85. Lamas, A. M., Mulroney, C. M., and Schleimer, R. P., 1988, Studies on the adhesive interaction between purified human eosinophils and cultured vascular endothelial cells, J. Immunol. 140: 1500–1505.PubMedGoogle Scholar
  86. Larsen, E., Celi, A., Gilbert, G. E., Furie, B. C., Erban, J. K., Bonfanti, R., Wagner, D. D., and Furie, B., 1989, PADGEM protein: A receptor that mediates the interaction of activated platelets with neutrophils and monocytes, Cell 59: 305–312.PubMedCrossRefGoogle Scholar
  87. Larsen, E., Palabrica, T., Sajer, S., Gilbert, G. E., Wagner, D. D., Furie, B. C., and Furie, B., 1990, PADGEM-dependent adhesion of platelets to monocytes and neutrophils is mediated by a lineage-specific carbohydrate, LNF III (CD15), Cell 63: 467–474.PubMedCrossRefGoogle Scholar
  88. Lasky, L. A., Singer, M. S., Yednock, T. A., Dowbenko, D., Fennie, C., Rodriguez, H., Nguyen, T., Stachel, S., and Rosen, S. D., 1989, Cloning of a lymphocyte homing receptor reveals a lectin domain, Cell 56: 1045–1055.PubMedCrossRefGoogle Scholar
  89. Lawrence, M. B., and Springer, T. A., 1991, Leukocytes roll on a selectin at physiologic flow rates: Distinction from and prerequisite for adhesion through integrins, Cell 65: 859–873.PubMedCrossRefGoogle Scholar
  90. Lawrence, M. B., Smith, C. W., Eskin, S. G., and McIntyre, L. V., 1990, Effect of venous shear stress on CD18-mediated neutrophil adhesion to cultured endothelium, Blood 75: 227–237.PubMedGoogle Scholar
  91. Leber, P. D., Milgrom, M., and Cohen, S., 1973, Eosinophils in delayed hypersensitivity skin reaction sites, Immunol. Commun. 2: 615–620.PubMedGoogle Scholar
  92. Leeuwenberg, J. F. M., von Asmuth, E. J. U., Jeunhomme, T. M. A. A., and Buurman, W. A., 1990, Interferon-gamma regulates the expression of an adhesion molecule ELAM-1 and IL-6 by human endothelial cells in vitro, J. Immunol. 145: 2110–2114.PubMedGoogle Scholar
  93. Lewinsohn, D. M., Bargatze, R. F., and Butcher, E. C., 1987, Leukocyte-endothelial cell recognition: Evidence of a common molecular mechanism shared by neutrophils, lymphocytes, and other leukocytes, J. Immunol. 138: 4313–4321.PubMedGoogle Scholar
  94. Lo, S. K., Lee, S., Ramos, R. A., Lobb, R., Rosa, M., Chi-Rosso, G., and Wright, S. D., 1991, Endothelial-leukocyte adhesion molecule 1 stimulates the adhesive activity of leukocyte integrin CR3 (CD1 lb/ CD18, Mac-1, am/32) on human neutrophils, J. Exp. Med. 173: 1493–1500.PubMedCrossRefGoogle Scholar
  95. Lowe, J. B., Stoolman, L. M., Nair, R. P., Larsen, R. D., Berhend, T. L., and Marks, R. M., 1990, ELAM-1 dependent cell adhesion to vascular endothelium determined by a transfected human fucosyltransferase cDNA, Cell 63: 475–484.PubMedCrossRefGoogle Scholar
  96. Marchesi, V. T., 1961, The site of leucocyte emigration during inflammation, Q. J. Exp. Physiol. 46: 115–118.PubMedGoogle Scholar
  97. Marchesi, V. T., and Florey, H. W., 1960, Electron micrographic observations on the emigration of leukocytes, Q. J. Exp. Physiol. 45: 343–348.PubMedGoogle Scholar
  98. Masinovsky, B., Urdal, D., and Gallatin, W. M., 1990, Iacts synergistically with IL-lß to promote lymphocyte adhesion to microvascular endothelium by induction of vascular cell adhesion molecule-1, J. Immunol. 145: 2886–2895.PubMedGoogle Scholar
  99. Matsushima, K., and Oppenheim, J. J., 1989, Interleukin 8 and MCAF: Novel inflammatory cytokines inducible by IL 1 and TNF, Cytokine 1: 2–13.PubMedCrossRefGoogle Scholar
  100. McEver, R. P., and Martin, M. N., 1984, A monoclonal antibody to a membrane glycoprotein binds only to activated platelets, J. Biol. Chem. 259: 9799–9804.PubMedGoogle Scholar
  101. McEver, R. P., Beckstead, J. H., Moore, K. L., Marshall-Carlson, L., and Bainton, D. F., 1989, GMP-140, a platelet a-granule membrane protein, is also synthesized by vascular endothelial cells and is localized in Weibel-Palade bodies, J. Clin. Invest. 84: 92–99.PubMedCrossRefGoogle Scholar
  102. Mentzer, S. J., Crimmins, M. A., Burakoff, S. J., and Faller, D. V., 1987, Alpha and beta subunits of the LFA-1 membrane molecule are involved in human monocyte-endothelial cell adhesion, J. Cell. Physiol. 130: 410–420.PubMedCrossRefGoogle Scholar
  103. Migliorisi, G., Folkes, E., Pawlowski, N., and Cramer, E. B., 1987, In vitro studies of human monocyte migration across endothelium in response to leukotriene B4 and f-Met-Leu-Phe, Am. J. Pathol. 127: 157–167.PubMedGoogle Scholar
  104. Miller, L. J., Bainton, D. F., Borregaard, N., and Springer, T. A., 1987, Stimulated mobilization of monocyte Mac-1 and p150,95 adhesion proteins from an intracellular vesicular compartment to the cell surface, J. Clin. Invest. 80: 535–544.PubMedCrossRefGoogle Scholar
  105. Molenaar, R., Visser, W. J., Verkerk, A., Koster, J. F., and Jongkind, J. F., 1989, Peroxidase stress and in vitro aging of endothelial cells increases the monocyte-endothelial cell adherence in a human in vitro system, Atherosclerosis 76: 193–202.PubMedCrossRefGoogle Scholar
  106. Morel, D. W., DiCorleto, P. E., and Chisolm, G. M., 1984, Endothelial and smooth muscle cells alter low density lipoprotein in vitro by free radical oxidation, Arteriosclerosis 4: 357–364.PubMedCrossRefGoogle Scholar
  107. Munro, J. M., Pober, J. S., and Cotran, R. S., 1989, Tumor necrosis factor and interferon-y induce distinct patterns of endothelial activation and associated leukocyte accumulation in skin of Papio anubis, Am. J. Pathol. 135: 121–133.PubMedGoogle Scholar
  108. Navab, M., Hough, G. P., Stevenson, L. W., Drinkwater, D. C., Laks, H., and Fogelman, A. M., 1988, Monocyte migration into the subendothelial space of a coculture of adult human endothelial and smooth muscle cells, J. Clin. Invest. 82: 1853–1863.PubMedCrossRefGoogle Scholar
  109. Nelson, D. S., 1965, The effects of anticoagulants and other drugs on cellular and cutaneous reactions to antigen in guinea-pigs with delayed-type hypersensitivity, Immunology 9: 219–234.PubMedGoogle Scholar
  110. Norris, P., Poston, R. N., Thomas, D. S., Thornhill, M., Hawk, J., and Haskard, D. O., 1991, The expression of endothelial leukocyte adhesion molecule-I (ELAM-1), intercellular adhesion molecule-1 (ICAM-1) and vascular cell adhesion molecule-1 (VCAM-1) in experimental cutaneous inflammation: A comparison of ultraviolet B erythema and delayed hypersensitivity, J. Invest. Dermatol. 96: 763–770.PubMedCrossRefGoogle Scholar
  111. Nortamo, P., Li, R., Renkonen, R., Timonen, T., Prieto, J., Patarroyo, M., and Gahmberg, C. G., 1991, The expression of human intercellular adhesion molecule-2 is refractory to inflammatory cytokines, Eur. J. Immunol. 21: 2629–2632.PubMedCrossRefGoogle Scholar
  112. Oppenheimer-Marks, N., Davis, L. S., Bogue, D. T., Ramberg, J., and Lipsky, P. E., 1991, Differential utilization of ICAM-1 and VCAM-1 during the adhesion and transendothelial migration of human T lymphocytes, J. Immunol. 147: 2913–2921.PubMedGoogle Scholar
  113. Osborn, L., Hession, C., Tizard, R., Vassallo, C., Luhowskyj, S., Chi-Rosso, G., and Lobb, R., 1989, Direct expression cloning of vascular cell adhesion molecule 1 (VCAM1), a cytokine-induced endothelial protein that binds to lymphocytes, Cell 59: 1203–1211.PubMedCrossRefGoogle Scholar
  114. Patel, K. D., Zimmerman, G. A., Prescott, S. M., McEver, R. P., and McIntyre, T. M., 1991, Oxygen radicals induce human endothelial cells to express GMP- 140 and bind neutrophils, J. Cell Biol. 112: 749–759.PubMedCrossRefGoogle Scholar
  115. Pawlowski, N. A., Kaplan, G., Abraham, E., and Cohn, Z. A., 1988, The selective binding and transmigration of monocytes through the junctional complexes of human endothelium, J. Exp. Med. 168: 1865–1882.PubMedCrossRefGoogle Scholar
  116. Pawlowsky, N. A., Abraham, E. L., Poutier, S., Scott, W. A., and Cohn, Z. A., 1985, Human monocyte-endothelial cell interaction, Proc. Natl. Acad. Sci. USA 82: 8208–8212.CrossRefGoogle Scholar
  117. Philips, M., Buyon, J., Winchester, R., Weissman, G., and Abramson, S., 1988, Upregulation of iC3b receptors (CR3) is neither necessary nor sufficient to promote neutrophil aggregation, J. Clin. Invest. 82: 495–501.PubMedCrossRefGoogle Scholar
  118. Phillips, M. L., Nudelman, E., Gaeta, F. C. A., Perez, M., Singhal, A. K., Hakomori, S.-I., and Paulson, J. C., 1990, ELAM-1 mediates cell adhesion by recognition of a carbohydrate ligand, sialyl-lex, Science 250: 1130–1132.PubMedCrossRefGoogle Scholar
  119. Picker, L. J., Kishimoto, T. K., Smith, C. W., Warnock, R. A., and Butcher, E. C., 199la, ELAM-1 is an adhesion molecule for skin-homing T cells, Nature (London) 349: 796–799.Google Scholar
  120. Picker, L. J., Warnock, R. A., Burns, A. R., Doerschuk, C. M., Berg, E. L., and Butcher, E. C., 199lb, The neutrophil selectin LECAM-1 presents carbohydrate ligands to the vascular selectins ELAM-1 and GMP-140, Cell 66: 921–933.Google Scholar
  121. Pigott, R., Needham, L. A., Edwards, R. M., Walker, C., and Power, C., 1991, Structural and functional studies of the endothelial activation antigen endothelial leucocyte adhesion molecule-1 using a panel of monoclonal antibodies, J. Immunol. 147: 130–135.PubMedGoogle Scholar
  122. Pober, J. S., and Cotran, R. S., 1990, Cytokines and endothelial cell biology, Physiol. Rev. 70: 427–451.PubMedGoogle Scholar
  123. Pober, J. S., Gimbrone, M. A., Lapierre, L. A., Mendrick, D. L., Fiers, W., Rothlein, R., and Springer, T. A., 1986, Overlapping patterns of activation of human endothelial cells by interleukin 1, tumour necrosis factor, and immune interferon, J. Immunol. 137: 1893–1896.PubMedGoogle Scholar
  124. Polley, M. J., Phillips, M. L., Wayner, E., Nudelman, E., Singhal, A. K., Hakomori, S., and Paulson, J. C., 1991, CD62 and endothelial cell-leukocyte adhesion molecule 1 (ELAM-1) recognize the same carbohydrate ligand, sialyl-Lewis x, Proc. Natl. Acad. Sci. USA 88: 6224–6228.PubMedCrossRefGoogle Scholar
  125. Polte, T., Newman, W., Raghunathan, G., and Venkat Gopal, T., 1991, Structural and functional studies of full-length vascular cell adhesion molecule-1: Internal duplication and homology to several adhesion proteins, DNA Cell Biol. 10: 349–357.PubMedCrossRefGoogle Scholar
  126. Poston, R. N., Haskard, D. O., Coucher, J. R., Gall, N. P., and Tidey, R. R., 1992, Expression of the adhesion molecule ICAM-1 in atherosclerotic plaques: Implications for positive-feedback monocyte recruitment in the pathogenesis of the plaque, Am. J. Pathol. 140: 665–673.PubMedGoogle Scholar
  127. Prieto, J., Beatty, P. G., Clark, E. A., and Patarroyo, M., 1988, Molecules mediating adhesion of T and B cells, monocytes and granulocytes to vascular endothelial cells, Immunology 63: 631–637.PubMedGoogle Scholar
  128. Rice, G. E., and Bevilacqua, M. P., 1989, An inducible endothelial cell surface glycoprotein mediates melanoma adhesion, Science 246: 1303–1306.PubMedCrossRefGoogle Scholar
  129. Rice, G. E., Munro, J. M., and Bevilacqua, M. P., 1990, Inducible cell adhesion molecule 110 (INCAM110) is an inducible endothelial cell receptor for lymphocytes, J. Exp. Med. 171: 1369–1374.PubMedCrossRefGoogle Scholar
  130. Rollins, B. J., and Pober, J. S., 1991, Interleukin-4 induces the synthesis and secretion of MCP-1/JE by human endothelial cells, Am. J. Pathol. 138: 1315–1319.PubMedGoogle Scholar
  131. Rollins, B. J., Yoshimura, T., Leonard, E. J., and Pober, J. S., 1990, Cytokine-activated human endothelial cells synthesize and secrete a monocyte chemoattractant, MCP-1/JE, Am. J. Pathol. 136: 1229–1233.PubMedGoogle Scholar
  132. Rothlein, R., Dustin, M. L., Marlin, S. D., and Springer, T. A., 1986, A human intercellular adhesion molecule (ICAM-1) distinct from LFA-1, J. Immunol. 137: 1270–1274.PubMedGoogle Scholar
  133. Saegusa, Y., Cavender, D., and Ziff, M., 1988, Stimulation of mononuclear cell binding to human endothelial cell monolayers by thrombin, J Immunol. 141: 4140–4145.PubMedGoogle Scholar
  134. Schall, T. J., Bacon, K., Toy, K. J., and Goeddel, D. V., 1990, Selective attraction of monocytes and T lymphocytes of the memory phenotype by cytokine RANTES, Nature (London) 347: 669–671.Google Scholar
  135. Schleimer, R. P., and Rutledge, B. K., 1986, Cultured human endothelial cells acquire adhesiveness for neutrophils after stimulation with interleukin 1, endotoxin, and tumor-promoting phorbol esters, J. Immunol. 136: 649–654.PubMedGoogle Scholar
  136. Shimizu, Y., Shaw, S., Graber, N., Gopal, T. V., Horgan, K. J., Van Seventer, G. A., and Newman, W., 1991, Activation-independent binding of human memory T cells to adhesion molecule ELAM-1, Nature (London) 349: 799–802.Google Scholar
  137. Siegelman, M. H., and Weissman, I. L., 1989, Human homologue of mouse lymph node homing receptor: Evolutionary conservation at tandem cell interaction domains, Proc. Natl. Acad. Sci. USA 86: 5562–5566.PubMedCrossRefGoogle Scholar
  138. Siegelman, M. H., Cheng, I. C., Weissman, I. L., and Wakeland, E. K., 1990, The mouse lymph node homing receptor is identical with the lymphocyte cell surface marker Ly-22: Role of the EGF domain in endothelial binding, Cell 61: 611–622.PubMedCrossRefGoogle Scholar
  139. Spertini, O., Luscinskas, F. W., Kansas, G. S., Munro, J. M., Griffin, J. D., Gimbrone, M. A., Jr., and Tedder, T. F., 1991, Leukocyte adhesion molecule-1 (LAM-1, L-selectin) interacts with an inducible endothelial cell ligand to support leukocyte adhesion, J. Immunol. 147: 2565–2573.PubMedGoogle Scholar
  140. Sporn, M. B., Roberts, A. B., Wakefield, L. M., and Assoian, R. K., 1986, Transforming growth factor-0: Biological function and chemical structure, Science 233: 532–534.PubMedCrossRefGoogle Scholar
  141. Staunton, D. E., Marlin, S. D., Stratova, C., Dustin, M. L., and Springer, T. A., 1988, Primary structure of ICAM-1 demonstrates interaction between members of the immunoglobulin and integrin supergene families, Cell 52: 925–933.PubMedCrossRefGoogle Scholar
  142. Staunton, D. E., Dustin, M. L., and Springer, T. A., 1989, Functional cloning of ICAM-2, a cell adhesion ligand for LFA-1 homologous to ICAM-1, Nature (London) 339: 61–64.Google Scholar
  143. Swerlick, R. A., Garcia-Gonzalez, E., Kubota, Y., Xu, Y., and Lawley, T. J., 1991, Studies of the modulation of MHC antigen and cell adhesion molecule expression on human dermal microvascular endothelial cells, J. Invest. Dermatol. 97: 190–196.PubMedCrossRefGoogle Scholar
  144. Tedder, T. F., Isaacs, C. M., Ernst, T. J., Demetri, G. D., Adler, D. A., and Disteche, C. M., 1989, Isolation and chromosomal localization of cDNAs encoding a novel human lymphocyte cell surface molecule, LAM-1, J. Exp. Med. 170: 123–133.PubMedCrossRefGoogle Scholar
  145. Territo, M., Berliner, J. A., and Fogelman, A. M., 1984, Effect of monocyte migration on low density lipoprotein transport across aortic endothelial monolayers, J. Clin. Invest. 74: 2279–2284.PubMedCrossRefGoogle Scholar
  146. Territo, M. C., Berliner, J. A., Almada, L., Ramirez, R., and Fogelman, A. M., 1989, Very low density lipoprotein pretreatment of endothelial monolayers increases monocyte adhesion, Arteriosclerosis 9: 824–828.PubMedCrossRefGoogle Scholar
  147. to Velde, A., Keizer, G. D., and Figdor, C. G., 1987, Differential function of LFA-1 family molecules (CD 11 and CD 18) in adhesion of human monocytes to melanoma cells and endothelial cells, Immunology 61: 2617–2627.Google Scholar
  148. Thornhill, M. H., and Haskard, D. O., 1990, IL-4 regulates endothelial activation by IL-1, tumor necrosis factor or IFNy, J. Immunol. 145: 865–872.PubMedGoogle Scholar
  149. Thornhill, M., Kyan-Aung, U., Lee, T. L., and Haskard, D. O., 1990a, T cells and neutrophils exhibit differential adhesion to cytokine stimulated endothelial cells, Immunology 69: 287–292.PubMedGoogle Scholar
  150. Thornhill, M., Kyan-Aung, U., and Haskard, D. O., 1990b, Interleukin-4 increases human endothelial cell adhesiveness for T cells but not for neutrophils, J. Immunol. 144: 3060–3065.PubMedGoogle Scholar
  151. Thornhill, M., Wellicome, S. M., Mahiouz, D. L., Lanchbury, J. S. S., Kyan-Aung, U., and Haskard, D. O., 1991, Tumor necrosis factor combines with IL-4 or IFN-y to selectively enhance endothelial cell adhesiveness for T cells: The contribution of VCAM-1 dependent and independent binding mechanisms, J. Immunol. 146: 592–598.PubMedGoogle Scholar
  152. Vedder, N. B., and Harlan, J. M., 1988, Increased surface expression of CDI lb/CD18 (Mac-1) is not required for stimulated neutrophil adherence to cultured endothelium, J. Clin. Invest. 81: 676–682.PubMedCrossRefGoogle Scholar
  153. Von Andrian, U. H., Chambers, J. D., McEvoy, L. M., Bargatze, R. F., Arfors, K.-E., and Butcher, E. C., 1991, Two-step model of leukocyte-endothelial cell interaction in inflammation: Distinct roles for LECAM-1 and the leukocyte Rz integrins in vivo, Proc. Natl. Acad. Sci. USA 88: 7538–7542.CrossRefGoogle Scholar
  154. Wallis, W. J., Beatty, P. G., Ochs, H. D., and Harlan, J. M., 1985, Human monocyte adherence to cultured vascular endothelium: Monoclonal antibody-defined mechanisms, J. Immunol. 135: 2323–2330.PubMedGoogle Scholar
  155. Walz, G., Aruffo, A., Kolanus, W., Bevilacqua, M., and Seed, B., 1990, Recognition of ELAM-1 of the sialyl-le` determinant on myeloid and tumor cells, Science 250: 1132–1135.PubMedCrossRefGoogle Scholar
  156. Watson, M. L., Kingsmore, S. F., Johnston, G. I., Siegelman, M. H., Le Beau, M. M., Lemons, R. S., Bora, N. S., Howard, T. A., Weissman, I. L., McEver, R. P., and Seldin, M. F., 1990, Genomic organization of the selectin family of leukocyte adhesion molecules on human and mouse chromosome 1, 1 Exp. Med. 172: 263–272.CrossRefGoogle Scholar
  157. Watson, S. R., Fennie, C., and Lasky, L. A., 1991, Neutrophil influx into an inflammatory site inhibited by a soluble homing receptor-IgG chimaera, Nature (London) 349: 164–167.Google Scholar
  158. Wellicome, S. M., Thornhill, M. H., Pitzalis, C., Thomas, D. S., Lanchbury, J. S. S., Panayi, G. S., and Haskard, D. O., 1990, A monoclonal antibody that detects a novel antigen on endothelial cells that is induced by tumor necrosis factor, IL-1 or lipopolysaccharide, J Immunol. 144: 2558–2565.PubMedGoogle Scholar
  159. Wilkinson, L. S., Poston, R. N., Edwards, J., and Haskard, D. O., 1991, Expression of vascular cell adhesion molecule-1 (VCAM-1) on synovial lining and germinal center cells in human synovium, Lab. Invest.,in press.Google Scholar
  160. Yu, C.-L., Haskard, D. O., Cavender, D. E., Johnson, A. R., and Ziff, M., 1985, Human gamma interferon increases the binding of T lymphocytes to endothelial cells, Clin. Exp. Immunol. 62: 554–561.PubMedGoogle Scholar
  161. Yu, C.-L., Haskard, D. O., Cavender, D. E., and Ziff, M., 1986, Effects of bacterial lipopolysaccharide on the binding of lymphocytes to human endothelial cells, J. Immunol. 136: 569–573.PubMedGoogle Scholar
  162. Zimmerman, G. A., McIntyre, T. M., and Prescott, S. M., 1985, Thrombin stimulates the adherence of neutrophils to human endothelial cells in vitro, J. Clin. Invest. 76: 2235–2246.PubMedCrossRefGoogle Scholar
  163. Zimmerman, G. A., McIntyre, T. M., Mehra, M., and Prescott, S. M., 1990, Endothelial cell-associated platelet-activating factor: A novel mechanism for signaling intercellular adhesion, J. Cell Biol. 110: 529–540.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1993

Authors and Affiliations

  • Martin H. Thornhill
    • 1
  • Dorian O. Haskard
    • 2
  1. 1.Department of Oral Medicine and PeriodontologyThe London Hospital Medical CollegeLondonUK
  2. 2.Rheumatology Unit, Department of Medicine, Royal Postgraduate Medical SchoolHammersmith HospitalLondonUK

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