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Microvascular endothelial cell heterogeneity: Interactions with leukocytes and tumor cells

Cancer and Metastasis Reviews volume 8, pages 353–389 (1990)Cite this article

Abstract

Endothelium constitutes a highly specialized organ that lines the vascular system and lymphatic channels. This organ is a complex network of arteries, veins, and microvessels that differ in size, structure, and function. The unique and strategic location imposes functional demands on the endothelium that are far greater than just being a passive barrier. Endothelial cells have the ability to differentiate both in structure and function in response to the needs of diverse tissue environments, making this organ extremely heterogeneous. Although vascular endothelial cells share certain common properties, they differ in regard to structure, antigenic and cell surface determinants, adhesion molecules, and metabolic function. The unique cell surface profiles expressed by endothelial cells in different tissue locations can be recognized by specific populations of circulating leukocytes or tumor cells, which contribute to their arrest and invasion patterns. This article attempts to review our current understanding of endothelial cell heterogeneity and its significance to patterns of leukocyte and tumor cell trafficking.

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References

  1. Sugerbaker EV: Patterns of metastasis. Cancer Biol Rev 2: 235–278, 1981

    Google Scholar 

  2. Nicolson GL: Cancer metastasis: Organ colonization and the cell-surface properties of malignant cells. Biochim Biophys Acta 695: 113–176, 1982a

    Google Scholar 

  3. Naito S, von Eschenbach AC, Fidler IJ: Different growth pattern and biologic behavior of human renal cell carcinoma implanted into different organs of nude mice. J Natl Cancer Inst 78: 377–385, 1987

    Google Scholar 

  4. Murphy P, Alexander P, Senior PV, Flemming J, Kirkham N, Taylor I: Mechanisms of organ selective tumour growth by blood-borne cancer cells. Br J Cancer 57: 19–31, 1988

    Google Scholar 

  5. Nicolson GL: Organ specificity of tumor metastasis: Role of preferential adhesion invasion and growth of malignant cells at specific secondary sites. Cancer Met Rev 7: 143–188, 1988

    Google Scholar 

  6. Aucrbach R, Lu W, Pardon E, Gumkowski F, Kaminski G, Kaminski M: Specificity of adhesion between murine tumor cells and capillary endothelium: An in vitro correlate of preferential metastasis in vivo. Cancer Res 47: 1492–1496, 1987

    Google Scholar 

  7. Ewing J: A treatise on tumors. In: Neoplastic Disease, 3rd edition, Saunders, Philadelphia, 1928

    Google Scholar 

  8. Paget S: The distribution of secondary growths in cancer of the breast. Lancet 1: 571–573, 1889

    Google Scholar 

  9. Weiss L: Random and nonrandom processes in metastasis, and metastatic efficiency. Invasion Metastasis 3: 193–208, 1983

    Google Scholar 

  10. Irimura T, Nicolson GL: Carbohydrate chain analysis by lectin binding to mixtures of glycoproteins separated by polyacrylamide slab-gel electrophoresis with in situ chemical modification. Carbohydrate Res 115: 209–220, 1984

    Google Scholar 

  11. Hart IR: The role of animal models in the study of experimental metastasis. In: Liotta L, Hart IR (eds) Tumor Invasion and Metastasis. Martinus Nijhoff, The Hague, 1982, pp 1–14

    Google Scholar 

  12. Hart IR, Fidler IJ: The role of organ selectivity in the determination of metastatic patterns of B16 melanoma. Cancer Res 40: 2281–2287, 1980

    Google Scholar 

  13. Roos E, Middlekoop OP, Van de Pavert IV: Adhesion of tumor cells to hepatocytes: Different mechanisms for mammary carcinoma compared with lymphosarcoma cells. J Natl Cancer Inst 73: 963–969, 1984

    Google Scholar 

  14. Schirrmacher V: Cancer metastasis: experimental approaches, theoretical concepts, and impacts for treatment strategics. Adv Cancer Res 831–873, 1985

  15. Ford WL: The cellular basis for immune responses. In: Porter T (ed) Defense and Recognition. Butterworth, London, 1973, pp 65–102

    Google Scholar 

  16. Ford WD, Sedgely M, Smith ME: The migration of lymphocytes across specialized endothelium. Cell Tissue Kinet 9: 351–361, 1976

    Google Scholar 

  17. Gowans JL, Knight EJ: The route of recirculation of lymphocytes in the rat. Proc R Soc Lond 159: 275–282, 1964

    Google Scholar 

  18. Stamper HB, Woodruff JJ: Lymphocyte homing into lymph nodes: In vitro demonstration of the selective affinity of recirculating lymphocytes for HEV. J Exp Med 144: 828–841, 1976

    Google Scholar 

  19. Dujvestijn AM, Kerkhove M, Bargatze RF, Butcher EC: Lymphoid tissue and inflammation specific endothelial cell differentiation defined by monoclonal antibodies. J Immunol 138: 713–719, 1987

    Google Scholar 

  20. Gallatin WM, Weissman IL, Butcher EC: A cell surface molecule involved in organ-specific homing of lymphocytes. Nature (Lond) 304: 30–34, 1983

    Google Scholar 

  21. Streeter PR, Lakey-Berg E, Rouse B, Bargatz R, Butcher EC: A tissue specific endothelial cell molecule involved in lymphocyte homing. Nature (Lond) 331: 41–46, 1988

    Google Scholar 

  22. Streeter PR, Rouse BT, Butcher EC: Immunohistologic and functional characterization of vascular addressin involved in lymphocyte homing into peripheral lymph nodes. J Cell Biol 107: 1853–1862, 1988

    Google Scholar 

  23. deBono D: Lymphocytes and the microcirculation Adv Microcirc 7: 68–95, 1977

    Google Scholar 

  24. Weiss L, Orr FW, Honn KV: Interaction of cancer cells with the microvasculature during metastasis. FASEB J 2: 12–21, 1988

    Google Scholar 

  25. Tressler RJ, Belloni PN, Nicolson GL: Correlation of inhibition of tumor cell-endothelial cell adhesion by RGD-containing peptide polymers and metastatic potential: Role of integrin-dependent and-independent adhesion mechanisms. Cancer Commun 1: 55–63, 1989

    Google Scholar 

  26. Greene HS, Harvey EK: The relationship between the dissemination of tumor cells and the distribution of metastases. Cancer Res 24: 799–811, 1964

    Google Scholar 

  27. Nicolson GL, Winkelhake JL: Organ specificity of bloodborne tumour metastasis determined by cell adhesion? Nature 255: 230–234, 1975

    Google Scholar 

  28. Nicolson GL: Metastatic tumor cell attachment and invasion assay utilizing vascular endothelial cell monolayers. J Histochem Cytochem 30: 214–220, 1982b

    Google Scholar 

  29. Belloni PN, Tressler RJ, Nicolson GL: Adhesion of metastatic tumor cells to organ-derived microvascular endothelial cells: Identification of nonintegrin endothelial cell adhesion molecules. (Submitted), 1989

  30. Abell RG: Quantitative studies on the rate of passage of nitrogenous substances through the walls of growing and differentiating mammalian capillaries. Collecting Net 14: 213–214, 1939

    Google Scholar 

  31. Shepro D, D'Amore PA: Endothelial cell metabolism. Adv Microcirc 9: 161–205, 1980

    Google Scholar 

  32. Thorgeirrson G, Robertson AL: The vascular endothelium: Pathobiologic significance. Am J Pathol 93: 802–848, 1978

    Google Scholar 

  33. Rhoden L: Structure and metabolism of connective tissue proteoglycans. In: Lennarz WJ (ed) The Biochemistry of Proteoglycans. Plenum, NY, 1980, pp 180–221

    Google Scholar 

  34. Majno G: Ultrastructure of the vascular membrane. In: Handbook of Physiology. Circulation Vol. III., 1965, pp 2293–2375

  35. Bennett HS: Morphological classification of vertebrate capillaries. Am J Physiol 196: 381–390, 1959

    Google Scholar 

  36. Stemmerman MB: General properties of blood vessels: Vascular endothelia. In: Abramson D, Dobrin P (eds) Blood Vessels and Lymphatics in Organ Systems. Academic Press, N. Y., 1980, pp 25–31

    Google Scholar 

  37. Timpl R, Martin GR: Components of basement membranes: Immunochemistry of the extracellular matrix. In: Furthmayer H (ed) CRC Press, FL, 1982, pp 119–150

    Google Scholar 

  38. Carley WW, Milici AJ, Madri JA: Extracellular matrix specificity for the differentiation of capillary endothelial cells. Exp Cell Res 178: 426–434, 1988

    Google Scholar 

  39. Kefalides NA: Basement membranes: structural and biosynthetic considerations. J Invest Dermatol 65: 85–92, 1975

    Google Scholar 

  40. Madri JA, Pratt BM: Endothelial cell-matrix interactions: In vitro models of angiogenesis. J Histochem Cytochem 34: 85–91, 1986

    Google Scholar 

  41. Wang ZW, Irimura T, Nakajima M, Belloni PN, Nicolson GL: Characterization of the ECM associated GAG produced by untransformed and transformed bovine corncal endothelial cells in culture. Eur J Biochem 153: 125–130, 1985

    Google Scholar 

  42. Godpodarowicz D, Gonzalez R, Fujii D: Are factors originating from serum, plasma, or cultured cells involved in the growth promoting effect of the ECM produced by cultured bovine corneal endothelial cells? J Cell Physiol 114: 191–199, 1983

    Google Scholar 

  43. Vlodavsky, I, Folkman, J, Klagsburn, M: Heparin-binding endothelial cell growth factors are sequestered by the extracellular matrix. In: Rifkin, DB, Klagsburn, M (eds) Angiogenesis: Mechanisms and Pathology. Cold Spring Harbor, New York, 1987, pp. 58–64

  44. Liotta LA, Rao CN, Barsky SH: Tumor invasion and the extracellular matrix. Lab Invest 49: 636–649, 1983

    Google Scholar 

  45. Nakajima M, Irimura T, Nicolson GL: Basement membranes degradative enzymes and tumor metastasis. Cancer Bull 39: 142–149, 1987

    Google Scholar 

  46. Wisse E, Knook DL: The investigation of sinusoidal cells: a new approach to the study of liver function. In: Popper H., Schaeffer F (ed) Progress in Liver Diseases Vol VI. Grune & Stratton, N. Y., 1979, pp 153–179

    Google Scholar 

  47. Weibel ER, Palade G: New cytoplasmic components in arterial endothelia. J Cell Biol 23: 101–112, 1964

    Google Scholar 

  48. Wagner RC: The isolation and culture of capillary endothelium from epidymal fat. Microvasc Res 10: 286–297, 1975

    Google Scholar 

  49. Wagner DD, Marder YJ: Biosynthesis of von Willebrand protein by human endothelial cells. J Biol Chem 268: 2005–2007, 1983

    Google Scholar 

  50. Simionescue M, Simionescue N, Palade G: Differentiated microdomains on the luminal surfaces of capillary endothelium. J Cell Biol 90: 605–613, 1981

    Google Scholar 

  51. Simionescue M, Simionescue N, Silbert E, Palade G: Differential microdomains on the luminal surfaces of capillary endothelium. II. Partial characterization of their anionic sites. J Cell Biol 90: 614–621, 1981

    Google Scholar 

  52. Simionescue M, Simionescue N: Hydrophobic pathways of capillary endothelium, a dynamic system. In: Ussing HH, Bindilev NB, Sten-Knudsen O (eds) Alfred Benson Symposium 15, on Water Transport Across Epithelia. Munksgaard, Copenhagen, 1980, pp 1–21

    Google Scholar 

  53. Simionescue M, Simionescue N, Palade G: Differential microdomains on the luminal surface of capillary endothelium: Distribution of lectin receptors. J Cell Biol 94: 406–413, 1982a

    Google Scholar 

  54. Simionescue M, Simionescue N, Palade G: Prefential distribution of anionic sites on the basement membrane and abluminal aspect in fenestrated endothelium. J Cell Biol 95: 425–434, 1982b

    Google Scholar 

  55. Simionescue M, Smionescue N, Santoro F, Palade G: Differentiated microdomains of the luminal plasmalemma of murine muscle capillaries: Segmental variations in young and old. J Cell Biol 100: 1296–1407, 1985

    Google Scholar 

  56. Bankston PW, Milici AJ: A survey of the binding of polycationic ferritin in several fenestrated capillary beds. Indication of heterogeneity in the luminal glycocalyx of fenestrated diaphragms. Microvasc Res 26: 36–48, 1983

    Google Scholar 

  57. Born GVR, Palinski D: Unusually high concentrations of sialic acid on the surface of vascular endothelia. Br J Exp Pathol 66: 543–549, 1985

    Google Scholar 

  58. Soda R, Tavassolli M: Mapping of the bone marrow sinus endothelium with lectins and glycosylated ferritins: Identification of different microdomains and their functional significance. J Ultrastruct Res 84: 299–310, 1983

    Google Scholar 

  59. Pino RM: Ultrastructural localization of lectin receptors on the bone marrow sinusoidal endothelium of the rat. Am J Anat 169: 259–272, 1984

    Google Scholar 

  60. Partridge WM: Recent advances in blood-brain barrier transport. Ann Rev Pharmacol Toxicol 28: 25–39, 1988

    Google Scholar 

  61. Vorbrodt AW, Dobrogowska DH, Lossinsky AS, Wisniewski HM: Ultrastructural localization of lectin receptors on the luminal and abluminal aspects of brain micro¢ blood vessels. J Histochem Cytochem 34: 251–261, 1986

    Google Scholar 

  62. Vorbrodt AW: Changes in the distribution of endothelial surface glycoconjugates associated with altered permeability of brain blood vessels. Acta Neuropathol 70: 103–111, 1986

    Google Scholar 

  63. Ponder BA, Wilkinson MM: Organ related differences of dolichos biflorus agglutinin to vascular endothelium. Dev Biol 96: 535–544, 1983

    Google Scholar 

  64. Belloni PN, Nicolson GL: Differential expression of cell surface glycoproteins on various organ-derived microvascular endothelia and endothelial cell cultures. J Cell Physiol 136: 398–410, 1988

    Google Scholar 

  65. Fatchi MI, Gerhurt DZ, Myers TG, Drews LR: Characterization of the blood-brain barrier: glycoconjugate receptors of 14 lectins in canine brain, cultured endothelial cells and blotted membrane proteins. Brain Res 415: 30–39, 1987

    Google Scholar 

  66. Belloni PN, Nicolson GL: Biochemical and immunological detection of organ specific glycoproteins associated with the blood brain barrier. Biology of the Vascular Endothelial Cell Fifth Symp (Abstract) VI-3, 1988

  67. Holthoffer H, Virtanen I, Kariniemi AL, Hormonia M, Linder E, Miettinen A: Ulex europeus I lectin as a marker for vascular endothelium in human tissue. Lab Invest 47: 60–66, 1982

    Google Scholar 

  68. Alroy J, Goyal V, Skutelsky E: Lectin histochemistry of mammalian endothelium. Histochemistry 86: 603–607, 1987

    Google Scholar 

  69. Walker RA: Ulex europeus I-peroxidase as a marker of vascular endothelium in routine histopathology. J Pathol 146: 123–127, 1985

    Google Scholar 

  70. Little D, Said JW, Siegel RJ, Fealy M, Fishbein MC: Endothelial cell markers in vascular neoplasms. J Pathol 149: 89–95, 1986

    Google Scholar 

  71. Laitinen L: Griffonia simplicifolia lectins bind specificially to endothelial cells and some epithelial cells in mouse tissues. Histochem J 19: 225, 234, 1987

    Google Scholar 

  72. Vorbrodt AW, Dobrogowska DH, Kim YS, Lossinsky AS, Wisniewski HM: Ultrastructural studies of glycoconjugates in brain microblood vessels and amyloid plaques of scrapie-infected mice. Acta Neuropathol 75: 277–287, 1988

    Google Scholar 

  73. Szumanska G, Vorbrodt AW, Mandybur TI, Wisnieski HM: Lectin histochemistry of plaques and tangles in Alzheimers disease. Acta Neuropathol 73: 1–11, 1987

    Google Scholar 

  74. Schnitzer JE, Carlet WW, Palade GE: Albumin interacts specifically with a 60-KDa microvascular endothelial glycoprotein. Proc Natl Acad Sci USA 85: 6773–6777, 1988

    Google Scholar 

  75. Pressman D: Tissue localizing antibodies. Ann. N.Y. Acad Sci 59: 376–379, 1955

    Google Scholar 

  76. Pressman D: Certain aspects of tissue specific antigens. Canadian Cancer Conf 5: 363–376, 1964

    Google Scholar 

  77. Auerbach R, Alby L, Morissey L, Tu M, Joseph J: Expression of organ-specific antigens on capillary endothelial cells. Microvasc Res 29: 401–406, 1985

    Google Scholar 

  78. Ghandour MS, Langley OK, Gombos G, Hirn M, Hirsch MR, Goridis GA: A surface marker for murinc vascular endothelial cells defined by monoclonal antibody. J Histochem Cytochem 30: 165–170, 1982

    Google Scholar 

  79. Zanetta JP, Dontenwill M, Meyer A, Roussel G: Isolation and immuno-histochemical localization of a lectin-like molecule from rat cerebellum. Dev Brain Res 17: 233–243, 1985

    Google Scholar 

  80. Michalak T, White FP, Gard AL, Dutton GR: A monoclonal antibody to the endothelium of rat brain microvessel. Brain Res 379: 320–328, 1986

    Google Scholar 

  81. Partridge WM, Yang J, Eisenberg J, Mietus LJ: Antibodies to blood-brain barrier bind selectively to brain capillary endothelial lateral membranes and to a 46 K protein. J Cereb Blood Flow Metab 6: 203–211, 1986

    Google Scholar 

  82. Risau W, Hallman R, Albrecht U, Henke-Fahle S: Brain induces the expression of an early cell surface marker for blood-brain barrier-specific endothelium. EMBO 5: 3179–3183, 1986

    Google Scholar 

  83. Hogg N, MacDonald S, Slusarenky M, Beverly PC: Monoclonal antibody specific for human monocytes, granulocytes and endothelium. Immunology 53: 753–767, 1984

    Google Scholar 

  84. Flotte TJ, Springer TA, Thorbecke GJ: Dendritic cell and macrophage staining by monoclonal antibodies in tissue sections and epidermal sheets. Am J Pathol 111: 112–119, 1983

    Google Scholar 

  85. Paul LC, Baldwin WM, van Es LS: Vascular endothelial alloantigens in renal transplantation. Transplantation 40: 117–123, 1985

    Google Scholar 

  86. Blankert JJ, Paul LC, van ES LA: Immunogenicity of various organs and genetic control of the response to a non-MHC endothelial antigen in rat. Transplant Proc 17: 785–791, 1985

    Google Scholar 

  87. Kennel SJ: Rat monoclonal antibodies to mouse lung components for analysis of fibrosis. Exp Mol Pathol 47: 110–124, 1987

    Google Scholar 

  88. Kennel SJ, Lankford TK, Ullrich RL, Jamashbi RJ: Enhancement of lung tumor colony formation by treatment of mice with monoclonal antibodies to pulmonary capillary endothelial cells. Cancer Res 48: 4964–4968, 1988

    Google Scholar 

  89. Moore MG, Chrzanowski RR, McCormick JR, Schwink A: Production of monoclonal antibodies to rat lung angiotensin-converting enzyme. Clin Immunol Immunopathol 33: 301–305, 1984

    Google Scholar 

  90. Irving MG, Roll FJ, Huang S, Montgomery-Bissel D: Characterization and culture of sinusoidal endothelium from normal rat liver; lipoprotein uptake and collagen phenotype. Gastroenterology 82: 1233–1217, 1984

    Google Scholar 

  91. Mukai K, Rosai J, Burgdorf WHC: Localizing of factor VIII related antigen in vascular endothelial cells using immunoperoxidase method. Am J Surg Pathol 4: 273–280, 1980

    Google Scholar 

  92. Harrach HR, Jasani B, Williams ED: Factor VIII as a marker of endothelial cells in follicular carcinoma of the thyroid. J Clin Pathol 36: 1050–1058, 1983

    Google Scholar 

  93. Dustin ML, Rothlein R, Bhan AK, Dinarello CA, Springer TA: Induction by IL-1 and interferon-L tissue distribution, biochemistry, and function of a natural adherence molecule (ICAM-1). J Immunol 37: 245–254, 1986

    Google Scholar 

  94. Bevilacqua MP, Pober JS, Mendrick DL, Cotran RS, Gimbrone MA: Identification of an inducible endothelialeukocyte adhesion molecule. Proc Natl Acad Sci USA 84: 9238–9242, 1987

    Google Scholar 

  95. Shepro D, Dunham B: Endothelial cell metabolism of biogenic amines. Ann Rev Physiol 48: 335–368, 1986

    Google Scholar 

  96. Zetter BR: Endothelial heterogeneity: influence of vessel size, organ location, and species specificity. In: Ryan U (ed) Biology of Vascular Endothelial Cells. CRC Press, Boca Raton, Florida, 1988, pp 63–80

    Google Scholar 

  97. Majno G: Ultrastructure of the vascular membrane. In: Handbook of Physiology. Circulation, Vol III, 1969, pp 2293–2375

  98. Svensjo E, Grega G: Evidence for endo cell-mediated regulation of macromolecular permeability by postcapillary venules. Fed Proc 45: 89–95, 1986

    Google Scholar 

  99. Grega GJ, Svensjo E, Haddy F: Macromolecular permeability of the microvasc membrane: physiological and pharmacological regulation. Microcirculation 1: 325–341, 1981

    Google Scholar 

  100. Schneeberger EE: Circulating proteins and macromolecular transport across continuous nonfenestrated endothelium. Ann N.Y. Acad Sci 401: 25–37, 1982

    Google Scholar 

  101. Svensjo E, Roempke K: Microvascular aspects of edema formation and its inhibition by b-receptor stimulants and some other anti-inflammatory drugs. In: Courtice FC, Garlick DG, Perry MA (eds) Progress in Microcirculation II. University of New South Wales, 1984, pp 447–463

  102. Robertson AL, Rosen LA: The arterial endothelium: Characteristics and function of the endothelial lining of large arteries. In: G Kaley, BM Altura (eds) Microcirculation. University Park Press, Baltimore, 1977, pp 145–165

    Google Scholar 

  103. Huttner I, Boufet M, More RH: Studies on protein passage through arterial endothelium. II. Regional differences in permeability to fine structural protein tracers in arterial endothelium of normotensive rats. Lab Invest 28: 678–685, 1973

    Google Scholar 

  104. Thorgeirsson G, Robertson AL: The vascular endothelium: Pathobiologic significance. Am J Pathol 93: 802–848, 1978

    Google Scholar 

  105. Albelda SM, Sampson PM, Hastelton FR, McNiff JM, Mueller SN, Williams SK, Fishman AP, Levine EM: Permeability characteristics of cultured endothelial cell monolayers. J Appl Physiol 64: 308–322, 1988

    Google Scholar 

  106. DelVecchio PJ, Siflinger-Birnboim A, Shepard JM, Bizios R, Cooper JA, Malik AB: Endothelial monolayer permeability to macromolecules. Federation Proc 46: 2511–1515, 1987

    Google Scholar 

  107. Brett J, Gerlach H, Nawroth P, Steinberg S, Godman G, Stern D: Tumor necrosis factor-cachectin increases permeability of endothelial cell monolayers by mechanism involving regulatory G proteins. J Exp Med 169: 1977–1991, 1989

    Google Scholar 

  108. DelVecchio PJ, Belloni PN, Holleran LA, Lum H, Malik AB: Culture characterization, and permeability of pulmonary microvessel endothelial cells. Proc Natl Acad Sci (in press), 1989

  109. Klatzo I: Neuropathological aspects of brain edema. J Neuropathol Exp Neurol 26: 1–14, 1967

    Google Scholar 

  110. Groothuis DR, Vick NA: Brain tumors and the blood-brain barrier. Trends Neurosci 5: 232–235, 1982

    Google Scholar 

  111. Long DM: Capillary ultrastructure and the blood-brain barrier in human malignant tumors. J Neurosurg 51: 53–58, 1979

    Google Scholar 

  112. Roy S, Chitra S: Ultrastructural study of microblood vessels in human brain tumors and peritumora tissue. J Neuro Oncol 7: 283–294, 1989

    Google Scholar 

  113. Criscuolo GR, Merrill MJ, Oldfield EH: Further characterization of malignant glioma-derived vascular permeability factor. J Neurosurg 69: 254–262, 1988

    Google Scholar 

  114. Belloni PN, Ohigashi H, Nicolson GL: Human melanoma-derived factors increase brain microvascular permeability. (In preparation)

  115. Gerritsen ME: Functional heterogeneity of vascular endothelial cells. Biochem Pharmacol 36: 2710–2721, 1987

    Google Scholar 

  116. Todd AS: The histological localization of fibrinolysis activator. J Path Bact 78: 281–286, 1959

    Google Scholar 

  117. Luskotoff DJ, Edgington TS: Synthesis of fibrinolytic activator and inhibitor by endothelial cells. Proc Natl Acad Sci USA 74: 3903–3907, 1977

    Google Scholar 

  118. McNichol GP, Douglas AS: The fibrinolytic enzyme system. In: Biggs W (ed) Human Blood Coagulation, Hemostasis and Thrombosis. Blackwell, Oxford, 1970, pp 361–381

    Google Scholar 

  119. Levine E, Luskotoff DJ: Regulation of PA production by cultured endothelial cells. Ann NY Acad Sci 401: 184–194, 1982

    Google Scholar 

  120. Highsmoth R: Isolation and properties of a plasminogen activator derived from canine vascular tissue. J Biol Chem 256: 121. 1981

    Google Scholar 

  121. Esnard F, Dupuy E, Sosne AM, Bodevin E: Partial characterization of fibrinolytic inhibitor from human umbilical vein endothelial cells. Thromb Hemostasis 47: 128–131, 1981

    Google Scholar 

  122. Luskotoff DJ: Effect of thrombin on the fibrinolytic activity of cultured bovine endothelial cells. J Clin Invest 64: 329–332, 1979

    Google Scholar 

  123. Luskotoff D, Levin E: Properties of plasminogen activators produced by endothelial cells. In: Jaffe E (ed) The Biology of Endothelial Cells. Martinus Nijhoff, MA, 1984, pp 200–208

    Google Scholar 

  124. Rosenberg RD, Rosenberg JS: Natural anticoagulant mechanisms. J Clin Invest 74: 18–26, 1984

    Google Scholar 

  125. Esmon CT: The regulation of natural anticoagulant pathways. Science 235: 1348–1352, 1987

    Google Scholar 

  126. Isshi H, Salemm HH, Bell CE, Majerus PW: Thrombomodulin and endothelial anticoagulant protein is absent from human brain. Blood 67: 2757–2764, 1986

    Google Scholar 

  127. Murphy-Ullrich JE, Hook M: Thrombospondin modulates focal adhesion in endothelial cells. J Cell Biol 109: 1309–1319, 1989

    Google Scholar 

  128. Nemerson Y: The reaction between brain tissue factor and factor VII and X. Biochem 5: 601–606, 1966

    Google Scholar 

  129. Gonmori H, Takeda Y: Properties of human tissue thromboplastin from brain, lung and placenta. Thrombos Haemostas 36: 90–103, 1976

    Google Scholar 

  130. Colucci M, Balconi R, Lorenzel A, Pietra D, Semarara N: Cultured endothelial cells generate tissue factor in response to endotoxin. J Clin Invest 71: 1893–1901, 1983

    Google Scholar 

  131. Bevilacqua MP, Pober JS, Wheeler ME, Cotran RS, Gimbrone MA: Interleukin-I activation of vascular endothelium. Effects on procoagulant activity. Am J Pathol 121: 393–403, 1985

    Google Scholar 

  132. Bevilacqua MP, Pober JS, Majeua GR, Fiers W, Cotran RS, Gimbrone MA: Recombinant TNF induce procoagulant activity in cultured human endothelia: Characterization and comparison with the actions of IL-1. Proc Natl Acad Sci USA 83: 4533–4541, 1986

    Google Scholar 

  133. Hoyer LW, Santos R, Hoyer JR: Antihemophilic factor antigen. Localization in endothelial cells by immunofluorescent microscopy. J Clin Invest 52: 2737–2744, 1973

    Google Scholar 

  134. Jaffe E: Synthesis of factor VIII by endothelial cells. In: Biology of Endothelial Cells. Martinus Nijhoff, MA, 1984, pp 209–214

    Google Scholar 

  135. Kwast TH, Stel HV, Cristen E, Bertina RM, Veerman EC: Localization of FVIII-procoagulant antigen. Blood 67: 222–227, 1986

    Google Scholar 

  136. Ruggeri ZM, DeMarco L, Gatti L, Bader R, Montgomery RR: Platelets have more than one binding site for VonWillebrand factor. J Clin Invest 72: 1–12, 1983

    Google Scholar 

  137. Plow EF, Piersbacher MD, Rouslahti E, Marguerie GA, Ginsberg MH: The effect of Arg-Gly-Asp-containing peptides on fibrinogen and VonWillebrand factor binding to platelets. Proc Natl Acad Sci USA 82: 8057–8062, 1985

    Google Scholar 

  138. Hoyer LW: The factor VIII complex: Structure and function. Blood 58: 1–13, 1981

    Google Scholar 

  139. Hormonia M, Lehto VP, Virtanen I: Intracellular localization of factor VIII-RAg and fibronectin in cultured human endothelial cells. Eur J Cell Biol 33: 217–228, 1984

    Google Scholar 

  140. Zetter BR: The endothelial cells of large and small blood vessels. Diabetes 30: 244–228, 1981

    Google Scholar 

  141. Hormonia M: Expression of factor VIII-related antigen and UEA lectin binding sites in endothelial cells during long-term culture. Cell Biol Int Reports 6: 1123–1134, 1982

    Google Scholar 

  142. Dejana E, Lampugnani MG, Giorgio M, Gaboli M, DFederici AB, Ruggeri ZM, Marchisio PC: VonWillebrand factor promotes endothelial cell adhesion via an Arg-Gly-Asp-dependent mechanism. J Cell Biol 109: 367–375, 1989

    Google Scholar 

  143. Levin RI, Weksler BB, Marcus AF, Jaffe EA: Prostacyclin production by endothelial cells. In: Jaffe EA (ed) Biology of Endothelial Cells. Martinus Nijhoff, MA, 1984, pp 228–247

    Google Scholar 

  144. Ryan US, Ryan JW: Vasoactive substances of the lungs: Cellular mechanisms. In: Saldeen T (ed) The Microembolism Syndrome. Almqvlistt & Wiksell, Stockholm, 1979, pp 213–221

    Google Scholar 

  145. Weksler BB, Ley CW, Jaffe EA: Stimulation of endothelial prostacyclin production by thrombin, trypsin and A23187. J Clin Invest 62: 923–932, 1978

    Google Scholar 

  146. Ali AE, Barrett JC, Eling TE: Prostaglandin and thromboxane production by fibroblasts and vascular endothelial cells. Prostaglandin 20: 667–675, 1980

    Google Scholar 

  147. Hong SL: Effect of bradykinin and thrombin on PGI synthesis in endothelial cells from calf and pig aorta and human umbilical cord vein. Thrombosis Res 18: 787–795, 1980

    Google Scholar 

  148. Goldsmith JC, Kisker CT: Thrombin-endothelial cell interactions: Critical importance of vessel origin. Thrombosis Res 25: 131–136, 1982

    Google Scholar 

  149. Sun FF, Taylor BM: Metabolism of prostacyclin in rat. Biochemistry 17: 4096–5000, 1978

    Google Scholar 

  150. Dusting GJ, Moncada S, Vane JR: Recirculation of prostacyclin (PGI2) in the lung. Br J Pharmacol 64: 315–319, 1978

    Google Scholar 

  151. Johnson AR: Human pulmonary endothelial cells in culture: Activities of cells from arteries and veins. J Clin Invest 65: 841–849, 1980

    Google Scholar 

  152. Mosher DF, Doyle MJ, Jaffe EA: Synthesis and secretion of thrombospondin by cultured human endothelial cells. J Cell Biol 93: 343–348, 1982

    Google Scholar 

  153. Kefalides NA: Chemistry of basement membranes: Structure and biosynthesis. In: Alttura BM, Davis E, Harder H (ed) Vascular Endothelium and Basement Membranes. Karger Press, Switzerland, 1980, pp 295–322

    Google Scholar 

  154. Sage H: Collagen synthesis by endothelial cells in culture. In: Jaffe E (ed) Biology of Endothelial Cells. Martinus Nijhoff, MA, 1984, pp 161–177

    Google Scholar 

  155. Madri JA, Dreyer B, Pitlick A, Furthmeyer H: The collagenous components of the subendothelium-correlation of structure and function. Lab Invest 43: 303–315, 1980

    Google Scholar 

  156. Wight TN: Vessel proteoglycans and thrombogenesis. In: Spaet T (ed) Progress in Hemostasis and Thrombosis, Vol. 5. Grune and Stratton, NY, 1980, pp 105–130

    Google Scholar 

  157. Gospodarowicz D, Gonzalex R, Fujii DK: Are factors originating from serum, plasma or cultured cells involved in the growth promoting effect of the extracellular matrix produced by cultured bovine corneal endothelial cells. J Cell Physiol 114: 191–202, 1983

    Google Scholar 

  158. Wang ZW, Irimura T, Nakajima M, Belloni PN, Nicolson GL: Characterization of the ECM associated GAG produced by untransformed and transformed bovine corneal endothelial cells in culture. Eur J Biochem 153: 125–130, 1985

    Google Scholar 

  159. Busch PC: Sulfated GAGs and vascular endothelial cells. In: Jaffe EA (ed) Biology of Endothelial Cells. Martinus Nijhoff, MA, 1984, pp 178–188

    Google Scholar 

  160. Merrilees MJ, Scott L: Culture of rat and pig aortic endothelial cell: Differences in their isolation, growth rate and glycosaminoglycan synthesis. Atherosclerosis 38: 19–25, 1986

    Google Scholar 

  161. Bar RS, Dake BL, Spanheimer RG: Sulfated GAGs in cultured endothelial cells from capillaries and large vessels of human and bovine origin. Atherosclerosis 56: 11–17, 1986

    Google Scholar 

  162. Buonassisi V, Colburn P: Biological significance of heparan sulfate proteoglycans. Ann N.Y. Acad Sci 401: 76–84, 1982

    Google Scholar 

  163. Soffer RL: Angiotensin converting enzyme and the regulation of vasoactive peptides. Ann Rev Biochem 45: 73–94, 1976

    Google Scholar 

  164. Mullane KM, Moncada S, Vane JR: Prostacyclin release induced by bradykinin may contribute to the antihypertensive action of angiotensin-converting enzyme inhibitors. Adv Prostaglandin Thromboxane Res 7: 1159–1161, 1980

    Google Scholar 

  165. Cushman DW, Ondetti MA: Inhibitors of ACE for treatment of hypertension. Biochem Pharmacol 29: 1871–1877, 1980

    Google Scholar 

  166. Caldwell PR, Seegal BC, Ksu KC, Das M, Soffer RC: Angiotensin converting enzyme: Vascular endothelial localization. Science 191: 1050–1052, 1976

    Google Scholar 

  167. Ng KK, Vane JR: Conversion of angiotensin I to angiotensin II. Nature (Lond) 216: 762–765, 1967

    Google Scholar 

  168. Ryan US, Ryan JW, Whitaker C, Chiu DA: Localization of angiotensin-converting enzyme. Immunocytochemistry and immunofluorescence. Tissue Cell 8: 125–131, 1976

    Google Scholar 

  169. DelVecchio PJ, Smith JR: Expression of ACE activity in cultured pulmonary artery endothelial cells. J Cell Physiol 108: 337–345, 1981

    Google Scholar 

  170. DelVecchio PJ, Lincoln DW: Phenotypes of cultured endothelium: Expression of ACE activity. In: Thilo-Korner GS, Freshney RI (eds) The Endothelial Cell: A Pluripotent Cell of the Vessel Wall. Karger Press, Switzerland, 1983, pp 67–83

    Google Scholar 

  171. Moore MG, Chrzanowski RR, McCormick JR, Schwink A: Production of monoclonal antibodies to rat lung angiotensin-converting enzyme. Clin Immunol Immunopathol 33: 301–305, 1984

    Google Scholar 

  172. DelVecchio PJ, Smith RJ: Aging of endothelial cell in culture: Decrease in ACE activity. Cell Biol Int Reports 6: 379–384, 1982

    Google Scholar 

  173. Lewis WH: Smooth muscle and endothelium in culture. Anat Rec 21: 72–80, 1921

    Google Scholar 

  174. Jaffe EA, Hoyer LW, Nachman RL: Synthesis of antihemolytic factor antigen by human endothelial cells. J Clin Invest 52: 2757–2764, 1973

    Google Scholar 

  175. Gimbrone MA: Culture of vascular endothelium. Progress Hemostasis Thrombosis 3: 1–10, 1976

    Google Scholar 

  176. Buonassisi V, Root M: Enzymatic degradation of heparin-related mucopolysaccharides from the surface of endothelial cell cultures. Biochim Biophys Acta 385: 1–10, 1975

    Google Scholar 

  177. Gospodarowicz D, Moran J, Braun D, Birdwell C: Clonal growth of bovine endothelial cells. Fibrolast growth factor as a survival agent. Proc Natl Acad Sci 73: 4120–4124, 1976

    Google Scholar 

  178. Gospodarowicz D, Ill C: Extracellular matrix and control of proliferation of vascular endothelial cells. J Clin Invest 65: 1351–1364, 1980

    Google Scholar 

  179. Poste G, Nicolson GL: In vitro systems for studying the interaction of metastatic tumour cells with endothelial cells and subendothelial cell basement membranes. In: Jaffe EA (ed) The Biology of Endothelial Cells. Martinus Nijhoff, The Hague, 1984, pp 438–449

    Google Scholar 

  180. Maciag T, Hoover GA, Stemmerman MB: Serial propagation of human endothelial cells in vitro. J Cell Biol 91: 420–426, 1981

    Google Scholar 

  181. McAuslan BR, Hannan GN, Reilly W: Signals causing change in morphological phenotype growth mode, and gene expression of vascular endothelial cells. J Cell Physiol 112: 96–106, 1982

    Google Scholar 

  182. Bowman PD, Betz AL, Ar D, Wolinsky JS, Penny JB, Shivers RR, Goldstein GW: Primary culture of capillary endothelium from rat brain. In Vitro 17: 353–362, 1981

    Google Scholar 

  183. Diglio C, Grammas P, Giaccamelli F, Wiener J: Primary culture of rat cerebral microvascular endothelial cells. Lab Invest 46: 554–563, 1982

    Google Scholar 

  184. Ager A: Isolation and culture of high endothelial cells from rat lymph nodes. J Cell Sci 87: 133–144, 1987

    Google Scholar 

  185. DeBault L, Henriquez E, Hart M, Cancilla P: Cerebral microvessels and derived cells in tissue culture. In Vitro 17: 480–494, 1981

    Google Scholar 

  186. Auerbach R, Alby J, Grieves J, Joseph J, Morrissey L, Sidky Y, Watt L: A monoclonal antibody against angiotensin converting enzyme: Its use as marker for murine, bovine; and human endothelial cells. Proc Natl Acad Sci USA 79: 7891–7895, 1982

    Google Scholar 

  187. Belloni PN, Carney DH, Nicolson GL: Organ-derived endothelial cells express differential responsiveness to thrombin and other growth factors. Microvasc Res (In press), 1989

  188. Ryan U, White L, Lopez M, Ryan J: Use of microcarriers to isolate and culture pulmonary microvascular endothelium. Tissue Cell 14: 597–606, 1982

    Google Scholar 

  189. Davison PM, Bensch K, Karasek MA: Growth and morphology of rabbit marginal vessel endothelium in cell culture. J Cell Biol 85: 187–195, 1980

    Google Scholar 

  190. Folkman J, Haudenchild C, Zetter BR: Long term culture of capillary endothelial cells. Proc Natl Acad Sci 76: 5217–5221, 1979

    Google Scholar 

  191. Gitlin J, D'Amore P: Culture of retinal capillary cells using selective growth media. Microvasc Res 26: 74–80, 1983

    Google Scholar 

  192. Davison PM, Karasck MA: Human dermal microvascular endothelial cells in vitro: Effect of cyclic AMP on cellular morphology and proliferation rate. J Cell Physiol 106: 253–258, 1980

    Google Scholar 

  193. Sherer G, Fitzharris T, Faulk W, LeRoy E: Cultivation of microvascular endothelial cells from human preputial skin. In Vitro 16: 675–684, 1980

    Google Scholar 

  194. Kern P, Knedler A, Eckel R: Isolation and culture of microvascular endothelium from human adipose tissue. J Clin Invest 71: 1822–1829, 1983

    Google Scholar 

  195. Striker G, Soderland C, Schmer G, Johnson A, Ross R, Striker L: Isolation, characterization, and propagation in vitro of human glomerular endothelial cells. J Exp Med 160: 323–328, 1984

    Google Scholar 

  196. Belloni PN, Nicolson GL: Differential expression of cell-surface glycoproteins associated with human brain microvessel endothelium. (In preparation)

  197. Gospodarowicz D, Brown KD, Birdwell CR, Zetter BR: Control of proliferation of human vascular endothelial cells. Characterization of the response of human umbilical vein endothelial cells to FGF, EGF, and thrombin. J Cell Biol 77: 774–788, 1978

    Google Scholar 

  198. Gospodarowicz D, Massoglia S, Cheng J, Fujii DK: Effect of fibroblast growth factor and lipoproteins on the proliferations of endothelial cells derived from bovine adrenal cortex, brain cortex, and corpus luteum capillaries. J Cell Physiol 127: 121–136, 1986

    Google Scholar 

  199. Zetter BR, Antoniades HN: Stimulation of human vascular endothelial cell growth by PDGF and thrombin. J Supramol Struct 11: 361–370, 1979

    Google Scholar 

  200. Knauer DJ, Cunningham DD: A re-evaluation of the response of human umbilical vein endothelial cells to certain growth factors. J Cell Physiol 117: 397–406, 1983

    Google Scholar 

  201. Hormonia M: Expression of factor VIII-related antigen and UEA lectin binding sites in endothelial cells during long-term culture. Cell Biol Int Reports 6: 1123–1134, 1982

    Google Scholar 

  202. Pitas RE, Boyles J, Mahley RW, Montgomery-Bissell D: Uptake of chemically modified low density lipoproteins in vivo is mediated by specific endothelial cells. J Cell Biol 100: 103–117, 1985

    Google Scholar 

  203. Rupnick MA, Carey A, Williams SK: Phenotypic diversity in cultured cerebral microvascular endothelial cells. In Vitro 24: 435–444, 1988

    Google Scholar 

  204. Weksler BB, Ley CW, Jaffe EA: Stimulation of endothelial prostacyclin production by thrombin, trypsin and A23187. J Clin Invest 62: 923–932, 1978

    Google Scholar 

  205. Stern DM, Bank I, Nawroth PP, Cassimiers J, Kisiel W, Fenton JW, Dinarello C, Chess L, Jaffe EA: Self regulation of procoagulant events on the endothelial cell-surface. J Exp Med 162: 1223–1233, 1985

    Google Scholar 

  206. Garcia JG, Birmboim A, Bizios R, DelVecchio PJ, Fenton JW, Malik AB: Thrombin induced increase in albumin permeability across the endothelium. J Cell Physiol 128: 96–104, 1986

    Google Scholar 

  207. Bizios R, Lai LC, Cooper JA, DelVecchio PJ, Malik AB: Thrombin induced adhesion of neutrophils to cultured endothelial monolayers: Increased endothelial cell adhesiveness. J Cell Physiol 34: 275–283, 1988

    Google Scholar 

  208. Saegusa Y, Cavender D, Ziff M: Stimulation of mononuclear cell binding to human endothelial cell monolayers by thrombin. J Immunol 141: 4140–4145, 1988

    Google Scholar 

  209. Malik AB, Lo SK, Bizios R: Thrombin induced alterations in endothelial permeability. Ann NY Acad Sci 434: 293–309, 1986

    Google Scholar 

  210. Wilkinson PC, Lackie JM: The adhesion, migration and chemotaxis of leukocytes in inflammation. In: Movat Z (ed) Current Topics in Pathology, Vol. 68. Springer-Verlag, NY, 1979, pp 48–84

    Google Scholar 

  211. Stoolman LM: Adhesion molecules controlling lymphocyte migration. Cell 56: 907–910, 1989

    Google Scholar 

  212. Yednock TA, Rosen SD: Lymphocyte homing. Adv Immunol 44: 313–378, 1989

    Google Scholar 

  213. deSousa MAB, Parrot DMV, Pantelouris EM: The lymphoid tissues in mice with congenital aplasia of the thymus. Clin Exp Immunol 4: 637–645, 1969

    Google Scholar 

  214. Hendricks HR, Estermans IL: Disappearance and reappearance of HEV and immigrating lymphocytes in lymph nodes deprived of afferent lymphatic vessels: A possible regulatory role of macrophages in lymphocyte migration. Eur J Immunol 13: 663–678, 1983

    Google Scholar 

  215. Nightingale D, Hurley JD: Relationship between lymphocyte immigration and vascular endothelium in chronic inflammation. Pathology 10: 27–35, 1978

    Google Scholar 

  216. Stamper HB, Woodruff JJ: Lymphocyte homing into lymph nodes: In vitro demonstration of the selective affinity of recirculating lymphocytes for HEV. J Exp Med 144: 828–841, 1976

    Google Scholar 

  217. Woodruff JJ, Katz IM, Lucas LE, Stamper HB: Membrane and cytoplasmic events involved in lymphocyte adherence to specialized HEV of lymph nodes. J Immunol 119: 1603–1610, 1977

    Google Scholar 

  218. Berg EL, Goldstein LA, Jutila MA, Nakache M, Picker LJ, Streeter PR, Wu NW, Zhou DFH, Butcher EC: Homing receptors and vascular addressins: Cell adhesion molecules that direct lymphocyte traffic. Immunol Rev 108: 1–18, 1989

    Google Scholar 

  219. Woodruff JJ, Clark LM, Chin YH: Specific cell adhesion mechanisms determining migration pathways of recirculating lymphocytes. Ann Rev Immunol 5: 201–222, 1987

    Google Scholar 

  220. Jalkanen ST, Bargatze RF, Herron LR, Butcher EC: A lymphoid cell surface glycoprotein involved in endothelial cell recognition and lymphocyte homing in man. Eur J Immunol 16: 1195–1202, 1986

    Google Scholar 

  221. Hammann A, Jablonzki-Westrich D, Duijvestijn A, Butcher EC, Baisch H, Harder R, Thiele HG: Alterations in homing receptors expression and organ-specific high endothelial venules binding of lymphocytes upon activation. J Immunol 140: 693–699, 1988

    Google Scholar 

  222. Dustin ML, Springer TA: Lymphocyte function associated antigen-1 (LFA-a) interaction with intercellular adhesion molecule-1 (ICAM-1) is one of at least three mechanisms for lymphocyte adhesion to cultured endothelial cells. J Cell Biol 107: 321–331.

  223. Yednock TA, Butcher EC, Stoolman LM, Rosen SD: Receptors involved in lymphocyte homing: Relationship between carbohydrate binding receptor and MEL-14 antigen. J Cell Biol 104: 725–731, 1987

    Google Scholar 

  224. Laskey LA, Singer MS, Yednock TA, Dowbenko D, Fennie C, Rodriguez H, Nguyen T, Stachel S, Rosen SD: Cloning of a lymphocyte homing-receptor reveals a lectin domain. Cell 56: 1045–1055, 1989

    Google Scholar 

  225. Siegelman MH, van de Rijn M, Weissman IL: Mouse lymph node homing receptor cDNA clone encodes a glycoprotein revealing tandem interaction domains. Science 243: 1165–1172.

  226. Bevilacqua MP, Stengelin S, Gimbrone MA, Seed B: Endothelial lcukocyte adhesion molecule 1: Receptor for neutrophils related to complement regulatory proteins and lectins. Science 243: 1160–1165, 1989

    Google Scholar 

  227. Staunton DE, Dustin ML, Springer TA: Functional cloning of ICAM-2, a cell adhesion ligand for LFA-1 homologous to ICAM-1. Nature (Lond) 339: 61–64, 1989

    Google Scholar 

  228. Moraes JR, Stastny P: Human endothelial cell antigens: Molecular independence from HLA and expression in blood monocytes. Transplant Proc 9: 605–610, 1977

    Google Scholar 

  229. Hirschberg A, Evense S, Henmoksen T, Thorsby E: The human mixed lymphocyte endothelial culture interactions. Transplantation 75: 495–504, 1975

    Google Scholar 

  230. Ashida E, Johnson A, Lipsky P: Human endothelial cell-lymphocyte interaction: Endothelial cells function as accessory cells necessary for mitogen-induced human T lymphocyte activation in vitro. J Clin Invest 67: 1490–1499, 1981

    Google Scholar 

  231. Bevilacqua MP, Pober JS, Wheeler MZ, Mendrick D, Cotran RS, Gimbrone MA: Interlcukin-1 acts on cultured human vascular endothelial cells to increase the adhesion of PMN. monocytes and related leukocyte cell lines. J Clin Invest 76: 2003–2010, 1985

    Google Scholar 

  232. Haskard D, Cavender D, Beatty P, Springer T, Ziff M: T lymphocyte adhesion to endothelial cells: mechanisms demonstrated by anti LFA-1 monoclonal antibodies. J Immunol 137: 2901–2906, 1986

    Google Scholar 

  233. Bender JR, Pardi R, Karasck MA, Engelman EG: Phenotypic and functional characterization of lymphocytes that bind human microvascular endothelial cells in vitro. J Clin Invest 79: 1979–1988, 1987

    Google Scholar 

  234. Lotz MT, Matory YL, Rayner AA, Ettinghausen SE, Serpp C, Rosenberg S: Clinical effects and toxicity of IL-2 in patients with cancer. Cancer 58: 2764–2772, 1986

    Google Scholar 

  235. Damle NK, Doyle LV, Bender JR, Bradley EC: Interlcukin-2 activated human lymphocytes exhibit enhanced adhesion to normal vascular endothelial cells and cause their lysis. J Immunol 138: 1779–1785, 1987

    Google Scholar 

  236. Del Regato D: Pathways of metastatic spread of malignant tumors. Sem Oncol 4: 33–38, 1977

    Google Scholar 

  237. Fidler IJ, Nicolson GL: Immunobiology of experimental metastatic melanoma. Cancer Biol Rev 2: 171–234, 1981

    Google Scholar 

  238. Viadana E, Bross IDJ, Pickren JE: An autopsy study of some routes of dissemination. Br J Cancer 27: 336–340, 1973

    Google Scholar 

  239. Hansen HH, Muggia FM: Staging of inoperable patients with bronchogenic carcinoma with special reference to bone marrow examination. Cancer 30: 1395–1401, 1972

    Google Scholar 

  240. Prout GR: Prostate gland. In: Holland JF, Frei E (eds) Cancer Medicine. Lea and Febiger, PA, 1973, pp 1680–1694

    Google Scholar 

  241. Elliott RHE, Frantz VK: Metastatic carcinoma masquerading as primary thyroid cancer: A report of authors' 14 cases. Ann Surg 151: 551–561, 1960

    Google Scholar 

  242. Fidler IJ, Nicolson GL: Organ selectivity for implantation, survival, and growth of B16 melanoma variant tumor lines. J Natl Cancer Inst 57: 1100–1202, 1976

    Google Scholar 

  243. Brunson KW, Beatty G, Nicolson GL: Selection and altered tumor cell properties of brain colonizing metastatic melanoma. Nature 272: 543–545, 1978

    Google Scholar 

  244. Nicolson GL, Minor KM, Reading CL: Tumor cell heterogeneity and blood-borne metastasis. In: Saunders J, Daniels J, Serrous B, Rosenfeld C, Denny C (ed) Fundamental Mechanisms in Human Cancer Immunology. Elsevier Press, N. Y., 1981, pp 31–39

    Google Scholar 

  245. Fidler IJ: Selection of successive tumor line for metastasis. Nature (New Biol) 242: 148–149, 1973

    Google Scholar 

  246. Phondke GP, Madyastha KR, Madyastha PR, Barth RF: Relationship between conconavalin A-induced agglutinability of murine leukemia cells and their propensity to form heterotypic aggregates with syngeneic lymphoid cells. J Natl Cancer Inst 66: 643–647, 1981

    Google Scholar 

  247. Nicolson GL, Muscali JJ, McGuire EJ: Metastatic RAW 117 lymphosarcoma as a model for malignant-normal cell interaction. Possible roles for cell surface antigens in determining the quantity and localization of secondary tumors. Oncodevop Bio Med 4: 149–152, 1983

    Google Scholar 

  248. Schirrmacher V, Chiensong Popov R, Arnheiter H: Hepatocyte tumor cell interactions in vitro. J Exp Med 151: 984–989, 1980

    Google Scholar 

  249. Nicolson GL, Dulski KM, Basson C, Welch DR: Preferential organ attachment and invasion in vitro by B16 melanoma cells selected for different metastatic colonization and invasive properties. Invasion Metastasis 5: 144–158, 1985

    Google Scholar 

  250. Netland PA, Zetter BR: Metastatic potential of B16 melanoma cells after in vitro selection for organ-specific adherence. J Cell Biol 101: 720–724, 1985

    Google Scholar 

  251. Menter DG, Hatfield JS, Harkins C, Sloane BF, Taylor JD, Crissman JD, Honn KV: Tumor cell-platelet interactions in vitro and their relationship to in vivo arrest of hematogenously circulating tumor cells. Clin Exp Metastasis 5: 65–78, 1987

    Google Scholar 

  252. Kramer RH, Nicolson GL: Invasion of vascular endothelial cells and underlying extracellular matrix by metastatic human cancer cells. In: Schweiger S (ed) International Cell Biology. Springer-Verlag, N. Y., 1981, pp 794–799

    Google Scholar 

  253. Varani J, Orr W, Ward PA: Adhesion characteristics of tumor cell variants of high and low tumorigenic potential. J Natl Cancer Inst 64: 1173–1178, 1980

    Google Scholar 

  254. Varani J, Grimstad IA, Knibbs RN, Hovig T, McCoy JP: Attachment spreading, and growth in vitro of highly malignant and low malignant murine fibrosarcoma cells. Clin Exp Metastasis 3: 45–59, 1985

    Google Scholar 

  255. Roos E, Tulp A, Middlekoop OP, Van de Pavert IV: Interactions between lymphoid tumor cells and isolated liver endothelial cells. J Natl Cancer Inst 72: 1173–1180, 1985

    Google Scholar 

  256. Korach S, Poupon MF, DuVillard JA, Becker M: Differential adhesiveness of rhabdomyosarcoma-derived cloned metastatic cell lines to vascular endothelial monolayers. Cancer Res 46: 3624–3629, 1986

    Google Scholar 

  257. Kramer RH, Gonzalez R, Nicolson GL: Metastatic tumor cells adhere prefercntially to the extracellular matrix underlying vascular endothelial cells. Int J Cancer 26: 639–645, 1980

    Google Scholar 

  258. Vlodavsky I, Schirrmacher V, Ariav Y, Fuks Z: Lymphoma cell interaction with cultured vascular endothelial cells and with the subendothelial basal lamina: Attachment, invasion and morphological appearance. Invasion Metastasis 3: 81–97, 1983

    Google Scholar 

  259. Nicolson GL, Irimura T, Gonzales R, Rouslahti E: The role of fibronectin in adhesion of metastatic melanoma cells to endothelial cells and their basal lamina. Exp Cell Res 135: 461–465, 1981

    Google Scholar 

  260. Netland PA, Zetter BR: Melanoma cell adhesion to defined extracellular matrix components. Biophys Biochem Res Commun 139: 515–522, 1986

    Google Scholar 

  261. Murray CJ, Liotta LA, Rennard SI, Martin GR: Adhesion characteristics of murinc metastatic and nonmetastatic tumor cells in vitro. Cancer Res 40: 347–351, 1980

    Google Scholar 

  262. Terranova VP, Williams JE, Liotta LA, Martin GR: Modulation of metastatic activity of melanoma cells by laminin and fibronectin. Science 226: 982–985, 1984

    Google Scholar 

  263. Chung DC, Zetter BR, Brodt NP: Lewis lung carcinoma variants with different metastatic spccificities adhere preferentially to diffcrentially defined extracellular matrix molecules. Invasion Metastasis 8: 103–117, 1988

    Google Scholar 

  264. Irmura T, Hester JE, Yamori T, Belloni PN, Ota D, Nicolson GL: Preferential adhesion of metastatic human colon carcinoma cells and extracellular matrix. (Submitted), 1989

  265. Liotta LA, Rao CN, Barsky SH: Tumor invasion and the extracellular matrix. Lab Invest 49: 636–649, 1983

    Google Scholar 

  266. McCarthy JB, Basara ML, Palm SL, Sas DF, Furcht LT: The role of cell adhcsion proteins laminin and fibronectin in the movement of malignant and metastatic cells. Cancer Mctastasis Rev 4: 125–152, 1985

    Google Scholar 

  267. Alby L, Auerbach R: Differential adhesion of tumor cells to capillary endothelial cells in vitro. Proc Natl Acad Sci USA 81: 5739–5743, 1984

    Google Scholar 

  268. Belloni PN, Tressler RJ, Nicolson GL: Adhesion of metastatic tumor cells to organ-derived microvascular endothelial cells: Identification of non-integrin endothelial cell adhesion molecules. (Submitted), 1989

  269. Belloni PN, Nicolson GL: Identification and partial characterization of endothelial cell surface glycoproteins associated with adhesion of murine RAW117 large cell lymphoma cells and leukocytes. M.D. Anderson Symposium: Critical Determinants in Cancer Progression and Metastasis, 1989, p 50

  270. Wood NL, Schook LB, Stoder EJ, Mohanakumar T: Biochemical characterization of human vascular endothelial cell monolayer antigens defined by monoclonal antibodics. Transplantation 45: 787–792, 1988

    Google Scholar 

  271. Butcher EC, Weissman I: Lymphocytes, tissues and organs. In: Paul WE (ed) Fundamental Immunology. Raven Press, NY, 1984, pp 109–127

    Google Scholar 

  272. Bargatze RF, Wu NW, Weissman IL, Butcher EC: High endothelial venule binding as a predictor of the dissemination of passaged murine lymphomas, J Exp Med 166: 1125–1131, 1987

    Google Scholar 

  273. Masuyama J, Minato N, Kano S: Mechanisms of lymphocyte adhesion to human vascular endothelial cells in culture. J Clin Invest 77: 1596–1605, 1986

    Google Scholar 

  274. Hatta KS, Takagi S, Fujisawa H, Takeichi M: Spatial and temporal expression pattern of N-cadherin cell adhesion molecules correlated with morphogenetic processes of chicken embryos. Dev Biol 120: 215–227, 1987

    Google Scholar 

  275. Crossin KL, Chuong CM, Edelman GM: Expression sequences of cell adhesion molecules. Proc Natl Acad Sci USA 82: 6942–6946, 1985

    Google Scholar 

  276. Rouslahti E, Hayman EG, Pierschbacher MD: Extracellular matrices and cell adhesion. Arteriosclerosis 5: 581–594, 1985

    Google Scholar 

  277. Hynes RO: Integrins: A family of cell surface receptors. Cell 48: 549–554, 1987

    Google Scholar 

  278. Ruoslahti E, Pierschbacher MD: New perspectives in cell adhesion. Science 238: 491–497, 1987

    Google Scholar 

  279. Cheresh DA, Pytela R, Pierschbacher MD, Klier FG, Ruoslahti E, Reisfeld RA: An Arg-Gly-Asp-directed receptor on the surface of human melanoma cells exists in a divalent cation-dependent functional complex with the disialoganglioside GD2. J Cell Biol 105: 1163–1173, 1987

    Google Scholar 

  280. Miller LJ, Schwarting R, Springer TA: Regulated expression of the Mac-1, LFA-1, p150,95 glycoprotein family during leucocyte differentiation. J Immunol 137: 2891–2900, 1986

    Google Scholar 

  281. Springer TA, Dustin ML, Kishimoto TK, Marlin SD: The lymphocyte function-associated LFA-1, CD2, and LFA-3 molecules: Cell adhesion receptors of the immune system. Ann Rev Immunol 5: 223–252, 1987

    Google Scholar 

  282. Fitzgerald LA, Charo IF, Phillips DR: Human and bovine endothelial cells synthesize membrane proteins similar to human platelet glycoproteins IIb and IIla. J Biol Chem 260: 10893–10896, 1985

    Google Scholar 

  283. Fujimoto T, Singer SJ: Immunocytochemical studies of endothelial cells in vivo. II. Chicken aortic and capillary endothelial cells exhibit different cell surface distributions of the integrin complex. J Histochem Cytochem 36: 1309–1317, 1988

    Google Scholar 

  284. Knudsen KA, Smith L, Smith S, Karczewski J, Tuszynski GP: Role of IIb-IIIa-like glycoproteins in cell-substratum adhesion of human melanoma cells. J Cell Physiol 136: 471–478, 1988

    Google Scholar 

  285. McCarthy JB, Chelberg MK, Mickelson DJ, Furcht LT: Localization and chemical synthesis of fibronectin peptides with melanoma adhesion and heparin binding activities. Biochemistry 27: 1380–1388, 1988

    Google Scholar 

  286. Humphries MJ, Yamada KM, Olden K: Investigation of the biological effects of anti-cell adhesive synthetic peptides that inhibit experimental metastasis of B16-F10 murine melanoma cells. J Clin Invest 81: 782–790, 1988

    Google Scholar 

  287. Welch DR, Lobl TJ, Scftor EA, Wack PIJ, Aced PA, Yohem KH, Seftor REB, Hendrix MJC: Use of the membrane invasion culture system (MICS) as a screen for anti-invasive agents. Int J Cancer 43: 449–457, 1989

    Google Scholar 

  288. Tressler RJ, Belloni PN, Nicolson GL: Correlation of inhibition of adhesion of large cell lymphoma and hepatic sinusoidal endothelial cells by RGD-containing peptide polymers with metastatic potential: Role of integrin-dependent and-independent adhesion mechanisms. Cancer Commun 1: 55–63, 1989

    Google Scholar 

  289. Pierschbacher MD, Ruoslahti E: Influence of stereochemistry of the sequence Arg-Gly-Asp-Xaa on binding specificity of cell adhesion. J Biol Chem 262: 17294–17298, 1987

    Google Scholar 

  290. Danilov YN, Juliano RL: (Arg-Gly-Asp)n-Albumin conjugates as a model substratum for integrin-mediated cell adhesion. Exp Cell Res 182: 186–196, 1989

    Google Scholar 

  291. Knudsen KA, Tuszynski GP, Huang TF, Niewiarowski S: Trigramin: An RGD-containing peptide from snake venom, inhibits cell-substratum adhesion of human melanoma cells. Exp Cell Res 179: 42–49, 1988

    Google Scholar 

  292. Levin JM, Garnier J: Improvements in a secondary structure prediction method based on a search for local sequence homologies and its use as a model building tool. Biochim Biophys Acta 955: 283–295, 1988

    Google Scholar 

  293. Iwamoto FA, Robey J, Graf M, Sasaki S, Kleinman HK, Yamada Y, Martin GR: YIGSR, a synthetic laminin pentapeptide, inhibits experimental metastasis formation. Science 238: 1132–1134, 1987

    Google Scholar 

  294. Bretani RR, Ribeiro SF, Potocnjak P, Pasqualini R, Lopes JD, Nakaie CR: Characterization of the cellular receptor for fibronectin through a hydropathic complementarity approach. Proc Natl Acad Sci USA 85: 364–369, 1988

    Google Scholar 

  295. Picker LJ, de los Toyos J, Telen MJ, Haynes BF, Butcher EC: Monoclonal antibodies against the CD44 [In(Lu)-related p80] and Pgp-1 antigens in man recognize the Hermes class of lymphocyte homing receptors. J Immunol 142: 2046–2051, 1989

    Google Scholar 

  296. Roos E, Roosien FF: Involvement of leucocyte function antigen-1 (LFA-1) in the invasion of hepatocyte cultures by lymphoma and T-cell hybridoma cells. J Cell Biol 105: 553–559, 1987

    Google Scholar 

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Belloni, P.N., Tressler, R.J. Microvascular endothelial cell heterogeneity: Interactions with leukocytes and tumor cells. Cancer Metast Rev 8, 353–389 (1990). https://doi.org/10.1007/BF00052608

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  • DOI: https://doi.org/10.1007/BF00052608

Key words

  • microvascular
  • heterogeneity
  • organ specific
  • tumor cell adhesion