Role of the Vascular Endothelium in Cancer Metastasis

  • Paula N. Belloni
  • Garth L. Nicolson

Abstract

The overwhelming majority of patients who die from cancer do so because of metastatic disease. The prevention of cancer deaths is therefore dependent on understanding the mechanism of malignant tumor cell spread from primary tumor sites to distant organ sites. Cancer metastases form by way of a complex series of sequential steps involving a variety of tumor cell and host properties. These steps typically involve growth and invasion of malignant cells at primary sties, followed by their penetration of the lymphatics, the circulatory system, and body cavities. Once in this compartments, the malignant cells can detach and be transported to distant sites. There they can implant and invade surrounding tissues and establish suitable microenvironments for survival and growth.

Keywords

Endothelial Cell Microvascular Endothelial Cell Endothelial Cell Surface Tumor Cell Adhesion Endothelial Cell Monolayer 
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.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Sugarbaker, E. V., 1981, Patterns of metastasis, Cancer Biol. Rev. 2: 235–278.Google Scholar
  2. 2.
    Nicolson, G. L., 1982, Cancer metastasis: Organ colonization and the cell-surface properties of malignant cells, Biochim. Biophys. Acta 695: 113–176.PubMedGoogle Scholar
  3. 3.
    Naito, S., von Eschenbach, A. C., and Fidler, I. J., 1987, 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.PubMedGoogle Scholar
  4. 4.
    Murphy, P., Alexander, P., Senior, P. V., Flemming, J., Kirkham, N., and Taylor, I., 1988, Mechanisms of organ selective tumour growth by blood-borne cancer cells, Br. J. Cancer 57: 19–31.PubMedCrossRefGoogle Scholar
  5. 5.
    Nicolson, G. L., 1988, Organ specificity of tumor metastasis: Role of preferential adhesion, invasion and growth of malignant cells at specific secondary sites, Cancer Metastasis Rev. 7: 143–188.PubMedCrossRefGoogle Scholar
  6. 6.
    Auerbach, R., Lu, W., Pardon, E., Gukowski, F., Kaminska, G., and Kaminska, M., 1987, Specificity of adhesion between murine tumor cells and capillary endothelium: An in vitro correlate of preferential metastasis in vivo, Cancer Res. 47: 1492–1496.Google Scholar
  7. 7.
    Ewing, J., 1928, A treatise on tumors, in: Neoplastic Diseases, 3rd ed., Saunders, Philadelphia.Google Scholar
  8. 8.
    Paget, S., 1889, The distribution of secondary growths in cancer of the breast, Lancet 1: 571–573.CrossRefGoogle Scholar
  9. 9.
    Weiss, L., 1983, Random and nonrandom processes in metastasis, and metastatic efficiency, Invasion Metastasis 3: 193–208.PubMedGoogle Scholar
  10. 10.
    Irimura, T., and Nicolson, G. L., 1984, Carbohydrate chain analysis by lectin binding to mixtures of glycoproteins separated by Polyacrylamide slab-gel electrophoresis with in situ chemical modification, Carhohydr. Res. 115: 209–220.CrossRefGoogle Scholar
  11. 11.
    Hart, I. R., 1982, The role of animal models in the study of experimental metastasis, in: Tumor Invasion and Metastasis (L. Liotta and I. R. Hart, eds.), Nijhoff, The Hague, pp. 1–14.CrossRefGoogle Scholar
  12. 12.
    Hart, I. R., and Fidler, I. J., 1980, The role of organ selectivity in the determination of metastatic patterns of B16 melanoma, Cancer Res. 40: 2281–2287.PubMedGoogle Scholar
  13. 13.
    Roos, E., Middlekoop, O. P., and Van de Pavert, I. V., 1984, Adhesion of tumor cells to hepatocytes: Different mechanisms for mammary carcinoma compared with lymphosarcoma cells, J. Natl. Cancer Inst. 73: 963–969.PubMedGoogle Scholar
  14. 14.
    Belloni, P. N., and Tressler, R.J., 1990, Microvascular heterogeneity: Interactions with leukocytes and tumor cells, Cancer Metastasis Rev. 8: 353–389.PubMedCrossRefGoogle Scholar
  15. 15.
    Ford, W. L., 1973, The cellular basis for immune responses, in: Defense and Recognition (R. Porter, ed.), Butterworths, London, pp. 65–102.Google Scholar
  16. 16.
    Ford, W. D., Sedgely, M., and Smith, M. E., 1976, The migration of lymphocytes across specialized endothelium, Cell Tissue Kinet. 9: 351–361.PubMedGoogle Scholar
  17. 17.
    Gowans, J. L., and Knight, E. J., 1964, The route of recirculation of lymphocytes in the rat, Proc. R. Soc. London 159: 275–282.CrossRefGoogle Scholar
  18. 18.
    Stamper, H. B., and Woodruff, J. J., 1976, Lymphocyte homing into lymph nodes: In vitro demonstration of the selective affinity of recirculating lymphocytes for HEV, J. Exp. Med. 144: 828–841.PubMedCrossRefGoogle Scholar
  19. 19.
    Dujvestijn, A. M., Kerkhove, M., Bargatze, R. F., and Butcher, E. C., 1987, Lymphoid tissue and inflammation specific endothelial cell differentiation defined by monoclonal antibodies, J. Immunol. 138: 713–719.Google Scholar
  20. 20.
    Gallatin, W. M., Weissman, I. L., and Butcher, E. C., 1983, A cell surface molecule involved in organ-specific homing of lymphocytes, Nature 304: 30–34.PubMedCrossRefGoogle Scholar
  21. 21.
    Streeter, P. R. Lakey-Berg, E., Rouse, B., Bargatze, R., and Butcher, E. C., 1988, A tissue specific endothelial cell molecule involved in lymphocyte homing, Nature 331: 41–46.PubMedCrossRefGoogle Scholar
  22. 22.
    Streeter, P. R., Rouse, B. T., and Butcher, E. C., 1988, Immunohistologic and functional characterization of vascular addressin involved in lymphocyte homing into peripheral lymph nodes, J. Cell Biol. 107: 1853–1862.PubMedCrossRefGoogle Scholar
  23. 23.
    deBono, D., 1977, Lymphocytes and the microcirculation, Adv. Microcirc. 7: 68–95.Google Scholar
  24. 24.
    Weiss, L., Orr, F. W., and Honn, K. V., 1988, Interaction of cancer cells with the microvasculature during metastasis, FASEB J. 2: 12–21.PubMedGoogle Scholar
  25. 25.
    Tressler, R. J., Belloni, P. N., and Nicolson, G. L., 1989, 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.PubMedGoogle Scholar
  26. 26.
    Greene, H. S., and Harvey, E. K., 1964, The relationship between the dissemination of tumor cells and the distribution of metastases, Cancer Res. 24: 799–811.PubMedGoogle Scholar
  27. 27.
    Nicolson, G. L., and Winkelhake, J. L., 1975, Organ specificity of blood-borne tumour metastasis determined by cell adhesion? Nature 255: 230–234.PubMedCrossRefGoogle Scholar
  28. 28.
    Nicolson, G. L., 1982, Metastatic tumor cell attachment and invasion assay utilizing vascular endothelial cell monolayers, J. Histochem. Cytochem. 30: 214–220.PubMedCrossRefGoogle Scholar
  29. 29.
    Tressler, R. J., and Nicolson, G. L., 1991, Butanol-extractable and detergent-solubilized cell surface components from murine large cell lymphoma cells associated with adhesion to organ microvessel endothelial cells, J. Cell. Biochem. in press.Google Scholar
  30. 30.
    Rhoden, L., 1980, Structure and metabolism of connective tissue proteoglycans, in: The Biochemistry of Proteoglycans (W. J. Lennarz, ed.), Plenum Press, New York, pp. 180–221.Google Scholar
  31. 31.
    Majno, G., 1965, Ultrastructure of the vascular membrane, in: Handbook of Physiology: Circulation, Vol. III, pp. 2293–2375.Google Scholar
  32. 32.
    Stemmerman, M. B., 1980, General properties of blood vessels: Vascular endothelia, in: Blood Vessels and Lymphatics in Organ Systems (D. Abramson and P. Dobrin, eds.), Academic Press, New York, pp. 25–31.Google Scholar
  33. 33.
    Timpl, R., and Martin, G. R., 1982, Components of basement membranes, in Immunochemistry of the Extracellular Matrix (H. Furthmayer, ed.), CRC Press, Boca Raton, pp. 119–150.Google Scholar
  34. 34.
    Carley, W. W., Milici, A. J., and Madri, J. A., 1988, Extracellular matrix specificity for the differentiation of capillary endothelial cells, Exp. Cell Res. 178: 426–434.PubMedCrossRefGoogle Scholar
  35. 35.
    Kefalides, N. A., 1975, Basement membranes: Structural and biosynthetic considerations, J. Invest. Dermatol. 65: 85–92.PubMedCrossRefGoogle Scholar
  36. 36.
    Madri, J. A., and Pratt, B. M., 1986, Endothelial cell-matrix interactions: In vitro models of angiogenesis, J. Histochem. Cytochem. 34: 85–91.PubMedCrossRefGoogle Scholar
  37. 37.
    Wang, Z. W., Irimura, T., Nakajima, M., Belloni, P. N., and Nicolson, G. L., 1985, Characterization of the ECM associated GAG produced by untransformed and transformed bovine corneal endothelial cells in culture, Eur. J. Biochem. 153: 125–130.PubMedCrossRefGoogle Scholar
  38. 38.
    Gospodarowicz, D., Gonzalez, R., and Fujii, D., 1983, 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.PubMedCrossRefGoogle Scholar
  39. 39.
    Vlodavsky, I., Folkman, J., and Klagsburn, M., 1987, Heparin-binding endothelial cell growth factors are sequestered by the extracellular matrix, in: Angiogenesis: Mechanisms and Pathology (D. B. Rifkin and M. Klagsburn, eds.), Cold Spring Harbor Laboratories, Cold Spring Harbor, N.Y., pp. 58–64.Google Scholar
  40. 40.
    Liotta, L. A., Rao, C. N., and Barsky, S. H., 1983, Tumor invasion and the extracellular matrix, Lab. Invest. 49: 636–649.PubMedGoogle Scholar
  41. 41.
    Nakajima, M., Irimura, T., and Nicolson, G. L., 1987, Basement membranes degradative enzymes and tumor metastasis, Cancer Bull. 39: 142–149.Google Scholar
  42. 42.
    Simionescu, M., Simionescu, N., and Palade, G., 1981, Differentiated microdomains on the luminal surfaces of capillary endothelium, J. Cell Biol. 90: 605–613.PubMedCrossRefGoogle Scholar
  43. 43.
    Simionescu, M., Simionescu, N., Silbert, E., and Palade, G., 1981, Differential microdomains on the luminal surfaces of capillary endothelium. II. Partial characterization of their anionic sites, J. Cell Biol. 90: 614–621.PubMedCrossRefGoogle Scholar
  44. 44.
    Simionescu, M., and Simionescu, N., 1980, Hydrophobic pathways of capillary endothelium, a dynamic system, in: Alfred Benson Symposium15 (H. H. Ussing, N. B. Bindilev, and O. Sten-Knudsen, eds.), Munksgaard, Copenhagen, pp. 1–21.Google Scholar
  45. 45.
    Simionescu, M., Simionescu, N., and Palade, G., 1982, Differential microdomains on the luminal surface of capillary endothelium: Distribution of lectin receptors, J. Cell Biol. 94: 406–413.PubMedCrossRefGoogle Scholar
  46. 46.
    Simionescu, M., Simionescu, N., and Palade, G., 1982, Preferential distribution of anionic sites on the basement membrane and abluminal aspect in fenestrated endothelium, J. Cell Biol. 95: 425–434.PubMedCrossRefGoogle Scholar
  47. 47.
    Simionescu, M., Simionescu, N., Santoro, F., and Palade, G., 1985, Differentiated microdomains of the luminal plasmalemma of murine muscle capillaries: Segmental variations in young and old, J. Cell Biol. 100: 1296–1307.CrossRefGoogle Scholar
  48. 48.
    Bankston, P. W., and Milici, A. J., 1983, 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.PubMedCrossRefGoogle Scholar
  49. 49.
    Born, G. V. R., and Palinski, D., 1985, Unusually high concentrations of sialic acid on the surface of vascular endothelia, Br. J. Exp. Pathol. 66: 543–549.PubMedGoogle Scholar
  50. 50.
    Soda, R., and Tavassolli, M., 1983, Mapping of the bone marrow sinus endothelium with lectins and glycosylated ferritins: Identification of different microdomains and their functional significance, J. Ultra-struct. Res. 84: 299–310.CrossRefGoogle Scholar
  51. 51.
    Pino, R. M., 1984, Ultrastructural localization of lectin receptors on the bone marrow sinusoidal endothelium of the rat, Am. J. Anat. 169: 259–272.PubMedCrossRefGoogle Scholar
  52. 52.
    Vorbrodt, A. W., Dobrogowska, D. H., Lossinsky, A. S., and Wisniewski, H. M., 1986, Ultrastructural localization of lectin receptors on the luminal and abluminal aspects of brain micro-blood vessels, J. Histochem. Cytochem. 34: 251–261.PubMedCrossRefGoogle Scholar
  53. 53.
    Vorbrodt, A. W., 1986, Changes in the distribution of endothelial surface glycoconjugates associated with altered permeability of brain blood vessels, Acta Neuropathol. 70: 103–111.PubMedCrossRefGoogle Scholar
  54. 54.
    Ponder, B. A., and Wilkinson, M. M., 1983, Organ related differences of Dolichos biflorus agglutinin to vascular endothelium, Dev. Biol. 96: 535–544.PubMedCrossRefGoogle Scholar
  55. 55.
    Belloni, P. N., and Nicolson, G. L., 1988, Differential expression of cell surface glycoproteins on various organ-derived microvascular endothelia and endothelial cell cultures, J. Cell. Physiol. 136: 398–410.PubMedCrossRefGoogle Scholar
  56. 56.
    Fatehi, M. I., Gerhurt, D. Z., Myers, T. G., and Drews, L. R., 1987, 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.PubMedCrossRefGoogle Scholar
  57. 57.
    Belloni, P.N., and Nicolson, G. L., 1988, Biochemical and immunological detection of organ specific glycoproteins associated with the blood brain barrier, Biology of the Vascular Endothelial Cell Vth Symp. (Abstract) VI–3.Google Scholar
  58. 58.
    Holthoffer, H., Virtanen, I., Kariniemi, A. L., Hormonia, M., Linder, E., and Miettinen, A., 1982, Ulex europeus I lectin as a marker for vascular endothelium in human tissue, Lab. Invest. 47: 60–66.Google Scholar
  59. 59.
    Alroy, J., Goyal, V., and Skutelsky, E., 1987, Lectin histochemistry of mammalian endothelium, Histochemistry 86: 603–607.PubMedCrossRefGoogle Scholar
  60. 60.
    Laitinen, L., 1987, Griffonia simplicifolia lectins bind specifically to endothelial cells and some epithelial cells in mouse tissues, Histochem. J. 19: 225–234.PubMedCrossRefGoogle Scholar
  61. 61.
    Pressman, D., 1955, Tissue localizing antibodies, Ann. N.Y. Acad. Sci. 59: 376–379.PubMedCrossRefGoogle Scholar
  62. 62.
    Pressman, D., 1964, Certain aspects of tissue specific antigens, Can. Cancer Conf. 5: 363–376.Google Scholar
  63. 63.
    Auerbach, R., Alby, L., Morissey, L., Tu, M., and Joseph, J., 1985, Expression of organ-specific antigens on capillary endothelial cells, Microvasc. Res. 29: 401–406.PubMedCrossRefGoogle Scholar
  64. 64.
    Ghandour, M. S., Langley, O. K., Gombos, G., Hirn, M., Hirsch, M. R., and Goridis, C. A., 1982, A surface marker for murine vascular endothelial cells defined by monoclonal antibody, J. Histochem. Cytochem. 30: 165–170.PubMedCrossRefGoogle Scholar
  65. 65.
    Zanetta, J. P., Dontenwill, M., Meyer, A., and Roussel, G., 1985, Isolation and immunohistochemical localization of a lectin-like molecule from rat cerebellum, Dev. Brain Res. 17: 233–243.CrossRefGoogle Scholar
  66. 66.
    Michalak, T., White, F. P., Gard, A. L., and Dutton, G. R., 1986, A monoclonal antibody to the endothelium of rat brain microvessel, Brain Res. 379: 320–328.PubMedCrossRefGoogle Scholar
  67. 67.
    Partridge, W. M., Yang, J., Eisenberg, J., and Mietus, L. J., 1986, Antibodies to blood-brain barrier bind selectively to brain capillary endothelial lateral membranes and to a 46K protein, J. Cereb. Blood Flow Metab. 6: 203–211.CrossRefGoogle Scholar
  68. 68.
    Risau, W., Hallman, R. Albrecht, U., and Henke-Fahle, S., 1986, Brain induces the expression of an early cell surface marker for blood-brain barrier-specific endothelium, EMBO J. 5: 3179–3183.PubMedGoogle Scholar
  69. 69.
    Hogg, N., MacDonald, S., Slusarenky, M., and Beverly, P. C., 1984, Monoclonal antibody specific for human monocytes, granulocytes and endothelium, Immunology 53: 753–767.PubMedGoogle Scholar
  70. 70.
    Flotte, T. J., Springer, T. A., and Thorbecke, G. J., 1983, Dendritic cell and macrophage staining by monoclonal antibodies in tissue sections and epidermal sheets, Am. J. Pathol. 111: 112–119.PubMedGoogle Scholar
  71. 71.
    Paul, L.C., Baldwin, W. M., and van Es, L. S., 1985, Vascular endothelial alloantigens in renal transplantation, Transplantation 40: 117–123.PubMedCrossRefGoogle Scholar
  72. 72.
    Blankert, J. J., Paul, L. C., and van Es, L. A., 1985, Immunogenicity of various organs and genetic control of the response to a non-MHC endothelial antigen in rat, Transplant. Proc. 17: 785–791.Google Scholar
  73. 73.
    Kennel, S. J., 1987, Rat monoclonal antibodies to mouse lung components for analysis of fibrosis, Exp. Mol. Pathol. 47: 110–124.PubMedCrossRefGoogle Scholar
  74. 74.
    Kennel, S. J., Lankford, T. K., Ullrich, R. L., and Jamashbi, R. J., 1988, Enhancement of lung tumor colony formation by treatment of mice with monoclonal antibodies to pulmonary capillary endothelial cells, Cancer Res. 48: 4964–4968.PubMedGoogle Scholar
  75. 75.
    Moore, M. G., Chrzanowski, R. R., McCormick, J. R., and Schwink, A., 1984, Production of monoclonal antibodies to rat lung angiotensin-converting enzyme, Clin. Immunol. Immunopathol. 33: 301–305.PubMedCrossRefGoogle Scholar
  76. 76.
    Irving, M. G., Roll, F. J., Huang, S., and Montgomery-Bissel, D., 1984, Characterization and culture of sinusoidal endothelium from normal rat liver; lipoprotein uptake and collagen phenotype, Gastroenterology 82: 1203–1217.Google Scholar
  77. 77.
    Mukai, K., Rosai, J., and Burgdorf, W. H. C., 1980, Localizing of factor VIII related antigen in vascular endothelial cells using immunoperoxidase method, Am. J. Surg. Pathol. 4: 273–280.PubMedCrossRefGoogle Scholar
  78. 78.
    Harrach, H. R., Jasani, B., and Williams, E. D., 1983, Factor VIII as a marker of endothelial cells in follicular carcinoma of the thyroid, J. Clin. Pathol. 36: 1050–1058.CrossRefGoogle Scholar
  79. 79.
    Dustin, M. L., Rothlein, R., Bhan, A. K., Dinarello, C. A., and Springer, T. A., 1986, Induction by IL-1 and interferon-7 tissue distribution, biochemistry, and function of a natural adherence molecule (ICAM-1), J. Immunol. 37: 245–254.Google Scholar
  80. 80.
    Bevilacqua, M. P., Pober, J. S., Mendrick, D. L., Cotran, R. S., and Gimbrone, M. A., 1987, Identification of an inducible endothelia-leukocyte adhesion molecule, Proc. Natl. Acad. Sci. USA 84: 9238–9242.PubMedCrossRefGoogle Scholar
  81. 81.
    Shepro, D., and Dunham, B., 1986, Endothelial cell metabolism of biogenic amines, Annu. Rev. Physiol. 48: 335–368.PubMedCrossRefGoogle Scholar
  82. 82.
    Zetter, B. R., 1988, Endothelial heterogeneity: Influence of vessel size, organ location, and species specificity, in: Biology of Vascular Endothelial Cells (U. Ryan, ed.), CRC Press, Boca Raton, pp. 63–80.Google Scholar
  83. 83.
    Grega, G. J., Svensjo, E., and Haddy, F., 1981, Macromolecular permeability of the microvascular membrane: Physiological and pharmacological regulation, Microcirculation 1: 325–341.Google Scholar
  84. 84.
    Schneeberger, E. E., 1982, Circulating proteins and macromolecular transport across continuous nonfenestrated endothelium, Ann. N.Y. Acad. Sci. 401: 25–37.PubMedCrossRefGoogle Scholar
  85. 85.
    Svensjo, E., and Roempke, K., 1984, Microvascular aspects of edema formation and its inhibition by β-receptor stimulants and some other anti-inflammatory drugs, in: Progress in Microcirculation II (E C. Courtice, D. G., Garlick, and M. A. Perry, eds.), University of New South Wales, pp. 447–463.Google Scholar
  86. 86.
    Robertson, A. L., and Rosen, L. A., 1977, The arterial endothelium: Characteristics and function of the endothelial lining of large arteries, in: Microcirculation (G. Kaley and B. M. Altura, eds.), University Park Press, Baltimore, pp. 145–165.Google Scholar
  87. 87.
    Huttner, I., Boufet, M., and More, R. H., 1973, Studies on protein passage through arterial endothelium. H. Regional differences in permeability to fine structural protein tracers in arterial endothelium of normo-tensive rats, Lab. Invest. 28: 678–685.PubMedGoogle Scholar
  88. 88.
    Thorgeirsson, G., and Robertson, A. L., 1978, The vascular endothelium: Pathobiologic significance, Am. J. Pathol. 93: 802–848.Google Scholar
  89. 89.
    Albelda, S. M., Sampson, P. M., Hastelton, F. R., McNiff, J. M., Mueller, S. N., Williams, S. K., Fishman, A. P., and Levine, E.M., 1988, Permeability characteristics of cultured endothelial cell monolayers, J. Appl. Physiol. 64: 308–322.PubMedGoogle Scholar
  90. 90.
    DelVecchio, P. J., Siflinger-Birnboim, A., Shepard, J. M., Bizios, R., Cooper, J. A., and Malik, A. B., 1987, Endothelial monolayer permeability to macromolecules, Fed. Proc. 46: 2511–2515.Google Scholar
  91. 91.
    Klatzo, I., 1967, Neuropathological aspects of brain edema, J. Neuropathol. Exp. Neurol. 26: 1–14.PubMedCrossRefGoogle Scholar
  92. 92.
    Groothuis, D. R., and Vick, N. A., 1982, Brain tumors and the blood-brain barrier, Trends Neurosci. 5: 232–235.CrossRefGoogle Scholar
  93. 93.
    Long, D. M., 1979, Capillary ultrastructure and the blood-brain barrier in human malignant tumors, J. Neurosurg. 51: 53–58.PubMedCrossRefGoogle Scholar
  94. 94.
    Roy, S., and Chitra, S., 1989, Ultrastructural study of microblood vessels in human brain tumors and peritumora tissue, J. NeuroOncol. 7: 283–294.PubMedCrossRefGoogle Scholar
  95. 95.
    Criscuolo, G. R., Merrill, M. J., and Oldfield, E. H., 1988, Further characterization of malignant gliomaderived vascular permeability factor, J. Neurosurg. 69: 254–262.PubMedCrossRefGoogle Scholar
  96. 96.
    Belloni, P.N., Ohigashi, H., and Nicolson, G. L., 1990, Human melanoma-derived factors increase brain microvascular permeability, in preparation.Google Scholar
  97. 97.
    Nemerson, Y., 1966, The reaction between brain tissue factor and factor VII and J., Biochemistry 5: 601–606.PubMedCrossRefGoogle Scholar
  98. 98.
    Gonmori, H., and Takeda, Y., 1976, Properties of human tissue thromboplastin from brain, lung and placenta, Thromb. Haemostas. 36: 90–103.Google Scholar
  99. 99.
    Colucci, M., Balconi, R., Lorenzel, A., Pietra, D., and Semarara, N., 1983, Cultured endothelial cells generate tissue factor in response to endotoxin, J. Clin. Invest. 71: 1893–1901.PubMedCrossRefGoogle Scholar
  100. 100.
    Bevilacqua, M. P., Pober, J. S., Wheeler, M. E., Cotran, R. S., and Gimbrone, M. A., 1985, Interleukin-1 activation of vascular endothelium. Effects on procoagulant activity, Am. J. Pathol. 121: 393–403.Google Scholar
  101. 101.
    Bevilacqua, M. P., Pober, J. S., Majeua, G. R., Fiers, W., Cotran, R. S., and Gimbrone, M. A., 1986, 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.PubMedCrossRefGoogle Scholar
  102. 102.
    Hoyer, L. W., Santos, R., and Hoyer, J. R., 1973, Antihemophilic factor antigen. Localization in endothelial cells by immunofluorescent microscopy, J. Clin. Invest. 52: 2737–2744.PubMedCrossRefGoogle Scholar
  103. 103.
    Jaffe, E., 1984, Synthesis of factor VIII by endothelial cells, in: Biology of Endothelial Cells, Nijhoff, The Hague, pp. 209–214.CrossRefGoogle Scholar
  104. 104.
    Kwast, T. H., Stel, H. V., Cristen, E., Bertina, R. M., and Veerman, E. C., 1986, Localization of FVIII-procoagulant antigen, Blood 67: 222–227.PubMedGoogle Scholar
  105. 105.
    Ruggeri, Z. M., DeMarco, L., Gatti, L., Bader, R., and Montgomery, R. R., 1983, Platelets have more than one binding site for VonWillebrand factor, J. Clin. Invest. 72: 1–12.PubMedCrossRefGoogle Scholar
  106. 106.
    Plow, E. F., Piersbacher, M. D., Ruoslahti, E., Marguerie, G. A., and Ginsberg, M. H., 1985, The effect of Arg-Gly-Asp-containing peptides on fibrinogen and Von Willebrand factor binding to platelets, Proc. Natl. Acad. Sci. USA 82: 8057–8062.PubMedCrossRefGoogle Scholar
  107. 107.
    Hoyer, L. W., 1981, The factor VIII complex: Structure and function, Blood 58: 1–13.PubMedGoogle Scholar
  108. 108.
    Hormonia, M., Lento, V. P., and Virtanen, I., 1984, Intracellular localization of factor VIII-RAg and fibronectin in cultured human endothelial cells, Eur. J. Cell Biol. 33: 217–228.Google Scholar
  109. 109.
    Zetter, B. R., 1981, The endothelial cells of large and small blood vessels, Diabetes 30: 244–248.Google Scholar
  110. 110.
    Hormonia, M., 1982, Expression of factor VIII-related antigen and UEA lectin binding sites in endothelial cells during long-term culture, Cell Biol. Int. Rep. 6: 1123–1134.CrossRefGoogle Scholar
  111. 111.
    Dejana, E., Lampugnani, M. G., Giorgio, M., Gaboli, M., Federici, A.B., Ruggeri, Z. M., and Marchisio, P. C., 1989, VonWillebrand factor promotes endothelial cell adhesion via an Arg-Gly-Asp-dependent mechanism, J. Cell Biol. 109: 367–375.PubMedCrossRefGoogle Scholar
  112. 112.
    Hong, S. L., 1980, Effect of bradykinin and thrombin on PGI synthesis in endothelial cells from calf and pig aorta and human umbilical cord vein, Thromb. Res. 18: 787–795.PubMedCrossRefGoogle Scholar
  113. 113.
    Goldsmith, J. C., and Kisker, C.T., 1982, Thrombin-endothelial cell interactions: Critical importance of vessel origin, Thromb. Res. 25: 131–136.PubMedCrossRefGoogle Scholar
  114. 114.
    Sun, F. F., and Taylor, B. M., 1978, Metabolism of prostacyclin in rat, Biochemistry 17: 4996–5000.CrossRefGoogle Scholar
  115. 115.
    Dusting, G. J., Moncada, S., and Vane, J. R., 1978, Recirculation of prostacyclin (PGI2) in the lung, Br. J. Pharmacol. 64: 315–319.PubMedCrossRefGoogle Scholar
  116. 116.
    Johnson, A. R., 1980, Human pulmonary endothelial cells in culture: Activities of cells from arteries and veins, J. Clin. Invest. 65: 841–849.PubMedCrossRefGoogle Scholar
  117. 117.
    Mosher, D. F., Doyle, M. J., and Jaffe, E. A., 1982, Synthesis and secretion of thrombospondin by cultured human endothelia cells, J. Cell Biol. 93: 343–348.PubMedCrossRefGoogle Scholar
  118. 118.
    Kefalides, N. A., 1980, Chemistry of basement membranes: Structure and biosynthesis, in: Vascular Endothelium and Basement Membranes (B. M. Alttura, E. Davis, and H. Harder, eds.), Karger, Basel, pp. 295–322.Google Scholar
  119. 119.
    Sage, H., 1984, Collagen synthesis by endothelial cells in culture, in: Biology of Endothelial Cells (E. Jaffe, ed.), Nijhoff, The Hague, pp. 161–177.CrossRefGoogle Scholar
  120. 120.
    Madri, J. A., Dreyer, B., Pitlick, A., and Furthmeyer, H., 1980, The collagenous components of the subendothelium—Correlation of structure and function, Lab. Invest. 43: 303–315.PubMedGoogle Scholar
  121. 121.
    Belloni, P. N., Carney, D. H., and Nicolson, G. L., 1991, Organ-derived endothelial cells express differential responsiveness to thrombin and other growth factors, Microvasc. Res. in press.Google Scholar
  122. 122.
    Maciag, T., Hoover, G. A., and Stemmerman, M. B., 1981, Serial propagation of human endothelial cells in vitro, J. Cell Biol. 91: 420–426.CrossRefGoogle Scholar
  123. 123.
    Hormonia, M., 1982, Expression of factor Vlll-related antigen and UEA lectin binding sites in endothelial cells during long-term culture, Cell Biol. Int. Rep. 6: 1123–1134.CrossRefGoogle Scholar
  124. 124.
    Pitas, R. E., Boyles, J., Mahley, R. W., and Montgomery-Bissell, D., 1985, Uptake of chemically modified low density lipoproteins in vivo is mediated by specific endothelial cells, J. Cell Biol. 100: 103–117.PubMedCrossRefGoogle Scholar
  125. 125.
    Rupnick, M. A., Carey, A., and Williams, S. K., 1988, Phenotypic diversity in cultured cerebral microvascular endothelial cells, In Vitro 24: 435–444.Google Scholar
  126. 126.
    Del Regato, D., 1977, Pathways of metastatic spread of malignant tumors, Semin. Oncol. 4: 33–38.PubMedGoogle Scholar
  127. 127.
    Fidler, I. J., and Nicolson, G. L., 1981, Immunobiology of experimental metastatic melanoma, Cancer Biol. Rev. 2: 171–234.Google Scholar
  128. 128.
    Viadana, E., Bross, I. D. J., and Pickren, J. E., 1973, An autopsy study of some routes of dissemination, Br. J. Cancer 27: 336–340.PubMedCrossRefGoogle Scholar
  129. 129.
    Hansen, H. H., and Muggia, F. M., 1972, Staging of inoperable patients with bronchogenic carcinoma with special reference to bone marrow examination, Cancer 30: 1395–1401.PubMedCrossRefGoogle Scholar
  130. 130.
    Elliott, R. H. E., and Frantz, V.K., 1960, Metastatic carcinoma masquerading as primary thyroid cancer: A report of authors’ 14 cases, Ann. Surg. 151: 551–561.PubMedCrossRefGoogle Scholar
  131. 131.
    Prout, G. R., 1973, Prostate gland, in: Cancer Medicine (J. F. Holland and E. Frei, eds.), Lea & Febiger, Philadelphia, pp. 1680–1694.Google Scholar
  132. 132.
    Fidler, I. J., and Nicholson, G. L., 1976, Organ selectivity for implantation, survival, and growth of B16 melanoma variant tumor lines, J. Natl. Cancer Inst. 57: 1199–1202.PubMedGoogle Scholar
  133. 133.
    Brunson, K. W., Beatty, G., and Nicolson, G. L., 1978, Selection and altered tumor cell properties of brain colonizing metastatic melanoma, Nature 272: 543–545.PubMedCrossRefGoogle Scholar
  134. 134.
    Nicolson, G. L., Miner, K. M., and Reading, C. L., 1981, Tumor cell heterogeneity and blood-borne metastasis, in: Fundamental Mechanisms in Human Cancer Immunology (J. Saunders, J. Daniels, B. Ser-rous, C. Rosenfeld, and C. Denny, eds.), Elsevier, Amsterdam, pp. 31–39.Google Scholar
  135. 135.
    Fidler, I. J., 1973, Selection of successive tumor lines for metastasis, Nature New Biol. 242: 148–149.PubMedGoogle Scholar
  136. 136.
    Nicolson, G. L., Museali, J. J., and McGuire, E. J., 1983, Metastatic RAW117 lymphosarcoma as a model for malignant-normal cell interaction. Possible roles for cell surface antigens in determining the quantity and localization of secondary tumors, Oncodev. BioMed. 4: 149–152.Google Scholar
  137. 137.
    Schirrmacher, V., Chiensong Popov, R., and Arnheiter, H., 1980, Hepatocyte tumor cell interactions in vitro, J. Exp. Med. 151: 984–989.CrossRefGoogle Scholar
  138. 138.
    Nicolson, G. L., Dulski, K. M., Basson, C., and Welch, D. R., 1985, Preferential organ attachment and invasion in vitro by B16 melanoma cells selected for different metastatic colonization and invasive properties, Invasion Metastasis 5: 144–158.PubMedGoogle Scholar
  139. 139.
    Nicolson, G. L., Belloni, P. N., Tressler, R. J., Dulski, K., Inoue, T., and Cavanaugh, P. G., 1989, Adhesive, invasive and growth properties of selected metastatic variants of murine large cell lymphoma, Invasion Metastasis 9: 102–116.PubMedGoogle Scholar
  140. 140.
    Kawaguchi, T., Kawaguchi, M., Miner, K. M., Lembo, T. M., and Nicolson, G. L., 1983, Brain meninges tumor formation by in vitro-selected metastatic B16 melanoma variants in mice, Clin. Exp. Metastasis 3: 247–259.CrossRefGoogle Scholar
  141. 141.
    Lapis, K., Pakus, S., and Liotta, L. A., 1988, Endothelialization of embolized tumor cells during metastasis formation, Clin. Exp. Metastasis 6: 73–89.PubMedCrossRefGoogle Scholar
  142. 142.
    Netland, P.A., and Zetter, B. R., 1985, Metastatic potential of B16 melanoma cells after in vitro selection for organ-specific adherence, J. Cell Biol. 101: 720–724.PubMedCrossRefGoogle Scholar
  143. 143.
    Menter, D. G., Hatfield, J. S., Harkins, C., Sloane, B. F., Taylor, J. D., Crissman, J. D., and Honn, K. V., 1987, Tumor cell-platelet interactions in vitro and their relationship to in vivo arrest of hematogenously circulating tumor cells, Clin. Exp. Metastasis 5: 65–78.PubMedCrossRefGoogle Scholar
  144. 144.
    Kramer, R. H., and Nicolson, G. L., 1981, Invasion of vascular endothelial cells and underlying extracellular matrix by metastatic human cancer cells, in: International Cell Biology (S. Schweiger, ed.), Springer-Verlag, Berlin, pp. 794–799.Google Scholar
  145. 145.
    Varani, J., Orr, W., and Ward, P. A., 1980, Adhesion characteristics of tumor cell variants of high and low tumorigenic potential, J. Natl. Cancer Inst. 64: 1173–1178.PubMedGoogle Scholar
  146. 146.
    Varani, J., Grimstad, I. A., Knibbs, R. N., Hovig, T., and McCoy, J. P., 1985, Attachment spreading, and growth in vitro of highly malignant and low malignant murine fibrosarcoma cells, Clin. Exp. Metastasis 3: 45–59.PubMedCrossRefGoogle Scholar
  147. 147.
    Roos, E., Tulp, A., Middlekoop, O. P., and Pavert, I. V., 1985, Interaction between lymphoid tumor cells and isolated liver endothelial cells, J. Natl. Cancer Inst. 72: 1173–1180.Google Scholar
  148. 148.
    Korach, S., Poupon, M. F., Du Villard, J. A., and Becker, M., 1986, Differential adhesiveness of rhabdomyosarcoma-derived cloned metastatic cell lines to vascular endothelial monolayers, Cancer Res. 46: 3624–3629.PubMedGoogle Scholar
  149. 149.
    Kramer, R. H., Gonzalez, R., and Nicolson, G. L., 1980, Metastatic tumor cells adhere preferentially to the extracellular matrix underlying vascular endothelial cells, Int. J. Cancer 26: 639–645.PubMedCrossRefGoogle Scholar
  150. 150.
    Vlodavsky, I., Schirrmacher, V., Ariav, Y., and Fuks, Z., 1983, Lymphoma cell interaction with cultured vascular endothelial cells and with the subendothelial basal lamina: Attachment, invasion and morphological appearance, Invasion Metastasis 3: 81–97.PubMedGoogle Scholar
  151. 151.
    Nicolson, G. L., Irimura, T., Gonzales, R., and Ruoslahti, E., 1981, The role of fibronectin in adhesion of metastatic melanoma cells to endothelial cells and their basal lamina, Exp. Cell Res. 135: 461–465.PubMedCrossRefGoogle Scholar
  152. 152.
    Lichtner, R. B., Belloni, P. N., and Nicolson, G. L., 1989, Differential adhesion of metastatic rat mammary carcinoma cells to organ derived microvascular endothelial cells and subendothelial matrix, Exp. Cell Biol. 57: 146–152.PubMedGoogle Scholar
  153. 153.
    Netland, P. A., and Zetter, B. R., 1986, Melanoma cell adhesion to defined extracellular matrix components, Biochem. Biophys. Res. Commun. 139: 515–522.PubMedCrossRefGoogle Scholar
  154. 154.
    Murray, C. J., Liotta, L. A., Rennard, S. I., and Martin, G. R., 1980, Adhesion characteristics of murine metastatic and nonmetastatic tumor cells in vitro, Cancer Res. 40: 347–351.Google Scholar
  155. 155.
    Terranova, V. P., Williams, J. E., Liotta, L. A., and Martin, G. R., 1984, Modulation of metastatic activity of melanoma cells by laminin and fibronectin, Science 226: 982–985.PubMedCrossRefGoogle Scholar
  156. 156.
    Chung, D. C., Zetter, B. R., and Brodt, N. P., 1988, Lewis lung carcinoma variants with different metastatic specificities adhere preferentially to differentially defined extracellular matrix molecules, Invasion Metastasis 8: 103–117.PubMedGoogle Scholar
  157. 157.
    Liotta, L. A., Rao, C. N., and Barsky, S. H., 1983, Tumor invasion and the extracellular matrix, Lab. Invest. 49: 636–649.PubMedGoogle Scholar
  158. 158.
    Irimura, T., Hester, J. E., Yamori, T., Belloni, P. N., Ota, D., and Nicolson, G. L., 1991, Preferential adhesion of metastatic human colon carcinoma cells and extracellular matrix, submitted for publication.Google Scholar
  159. 159.
    McCarthy, J. B., Basara, M. L., Palm, S. L., Sas, D. F., and Furcht, L. T., 1985, The role of cell adhesion proteins laminin and fibronectin in the movement of malignant and metastatic cells, Cancer Metastasis Rev. 4: 125–152.PubMedCrossRefGoogle Scholar
  160. 160.
    Alby, L., and Auerbach, R., 1984, Differential adhesion of tumor cells to capillary endothelial cells in vitro, Proc. Natl. Acad. Sci. USA 81: 5739–5743.CrossRefGoogle Scholar
  161. 161.
    Belloni, P. N., Tressler, R. J., and Nicolson, G. L., 1991, Adhesion of metastatic tumor cells to organ-derived microvascular endothelial cells: Identification of non-integrin endothelial cell adhesion molecules, submitted for publication.Google Scholar
  162. 162.
    Yednock, T. A., and Rosen, S. D., 1989, Lymphocyte homing, Adv. Immunol. 44: 313–378.PubMedCrossRefGoogle Scholar
  163. 163.
    Berg, E. L., Goldstein, L. A., Jutila, M. A., Nakache, M., Picker, L. J., Streeter, P. R., Wu, N. W., Zhou, D., and Butcher, E. C., 1989, Homing receptors and vascular addressins: Cell adhesion molecules that direct lymphocyte traffic, Immunol. Rev. 108: 5–18.PubMedCrossRefGoogle Scholar
  164. 164.
    Belloni, P.N., and Nicolson, G. L., 1989, 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.Google Scholar
  165. 165.
    Bevilacqua, M. P., Stengelin, S., Gimbrone, M. A., and Seed, B., 1989, Endothelial leukocyte adhesion molecule 1: Receptor for neutrophils related to complement regulatory proteins and lectins, Science 243: 1160–1165.PubMedCrossRefGoogle Scholar
  166. 166.
    Wood, N. L., Schook, L. B., Stoder, E. J., and Mohanakumar, T., 1988, Biochemical characterization of human vascular endothelial cell monolayer antigens defined by monoclonal antibodies, Transplantation 45: 787–792.PubMedCrossRefGoogle Scholar
  167. 167.
    Butcher, E. C., and Weissman, I., 1984, Lymphocytes, tissues and organs, in: Fundamental Immunology (W. E. Paul, ed.), Raven Press, New York, pp. 109–127.Google Scholar
  168. 168.
    Bargatze, R. F., Wu, N. W., Weissman, I. L., and Butcher, E. C., 1987, High endothelial venule binding as a predictor of the dissemination of passaged murine lymphomas, J. Exp. Med. 166: 1125–1131.PubMedCrossRefGoogle Scholar
  169. 169.
    Hatta, K. S., Takagi, S., Fujisawa, H., and Takeichi, M., 1987, Spatial and temporal expression pattern of N-cadherin cell adhesion molecules correlated with morphogenetic processes of chicken embryos, Dev. Biol. 120: 215–227.PubMedCrossRefGoogle Scholar
  170. 170.
    Crossin, K. L., Chuong, C.M., and Edelman, G.M., 1985, Expression sequences of cell adhesion molecules, Proc. Natl. Acad. Sci. USA 82: 6942–6946.PubMedCrossRefGoogle Scholar
  171. 171.
    Dustin, M. L., and Springer, T. A., 1988, Lymphocyte function associated antigen-1 (LFA-1) 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.PubMedCrossRefGoogle Scholar
  172. 172.
    Hynes, R. O., 1987, Integrins: A family of cell surface receptors, Cell 48: 549–554.PubMedCrossRefGoogle Scholar
  173. 173.
    Ruoslahti, E., and Pierschbacher, M. D., 1987, New perspectives in cell adhesion, Science 238: 491–497.PubMedCrossRefGoogle Scholar
  174. 174.
    Cheresh, D. A., Pytela, R., Pierschbacher, M. D., Klier, F. G., Ruoslahti, E., and Reisfeld, R. A., 1987, 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.PubMedCrossRefGoogle Scholar
  175. 175.
    Miller, L. J., Schwarting, R., and Springer, T. A., 1986, Regulated expression of the Mac-1, LFA-1, pl50,95 glycoprotein family during leucocyte differentiation, J. Immunol. 137: 2891–2900.PubMedGoogle Scholar
  176. 176.
    Springer, T. A., Dustin, M. L., Kishimoto, T. K., and Marlin, S. D., 1987, The lymphocyte function-associated LFA-1, CD2, and LFA-3 molecules: Cell adhesion receptors of the immune system, Annu. Rev. Immunol. 5: 223–252.PubMedCrossRefGoogle Scholar
  177. 177.
    Fitzgerald, L. A., Charo, I. F., and Phillips, D. R., 1985, Human and bovine endothelial cells synthesize membrane proteins similar to human platelet glycoproteins IIb and IIIa, J. Biol. Chem. 260: 10893–10896.PubMedGoogle Scholar
  178. 178.
    Fujimoto, T., and Singer, S. J., 1988, Immunocytochemical studies of endothelial cells in vivo. H. Chicken aortic and capillary endothelial cells exhibit different cell surface distributions of the integrin complex, J. Histochem. Cytochem. 36: 1309–1317.PubMedCrossRefGoogle Scholar
  179. 179.
    Knudsen, K. A., Smith, L., Smith, S., Karczewski, J., and Tuszynski, G. P., 1988, Role of IIb-IIIa-like glycoproteins in cell-substratum adhesion of human melanoma cells, J. Cell. Physiol. 136: 471–478.PubMedCrossRefGoogle Scholar
  180. 180.
    McCarthy, J. B., Chelberg, M. K., Mickelson, D. J., and Furcht, L. T., 1988, Localization and chemical synthesis of fibronectin peptides with melanoma adhesion and heparin binding activities, Biochemistry 27: 1380–1388.PubMedCrossRefGoogle Scholar
  181. 181.
    Humphries, M. J., Yamada, K. M., and Olden, K., 1988, 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.PubMedCrossRefGoogle Scholar
  182. 182.
    Welch, D. R., Lobl, T. J., Seftor, E. A., Wack, P. I. J., Aeed, P. A., Rohem, K. H., Seftor, R. E. B., and Hendrix, M. J. C., 1989, Use of the membrane invasion culture system (MICS) as a screen for anti-invasive agents, Int. J. Cancer 43: 449–457.PubMedCrossRefGoogle Scholar
  183. 183.
    Tressler, R. J., Belloni, P.N., and Nicolson, G. L., 1989, 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.PubMedGoogle Scholar
  184. 184.
    Pierschbacher, M. D., and Ruoslahti, E., 1987, Influence of stereochemistry of the sequence Arg-Gly-Asp-Xaa on binding specificity of cell adhesion, J. Biol. Chem. 262: 17294–17298.PubMedGoogle Scholar
  185. 185.
    Danilov, Y. N., and Juliano, R. L., 1989, (Arg-Gly-Asp)n-albumin conjugates as a model substratum for integrin-mediated cell adhesion, Exp. Cell Res. 182: 186–196.PubMedCrossRefGoogle Scholar
  186. 186.
    Levin, J. M., and Garnier, J., 1988, 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.PubMedCrossRefGoogle Scholar
  187. 187.
    Iwamoto, F. A., Robey, J., Graf, M., Sasaki, S., Kleinman, H. K., Yamada, Y., and Martin, G. R., 1987, YIGSR, a synthetic laminin pentapeptide, inhibits experimental metastasis formation, Science 238: 1132–1134.PubMedCrossRefGoogle Scholar
  188. 188.
    Horak, E., Darling, D. L., and Tarin, D., 1986, Analysis of organ-specific effects on metastatic tumor formation by studies in vitro, J. Natl. Cancer Inst. 75: 913–922.Google Scholar
  189. 189.
    Naito, S., Giavazzi, R., and Fidler, I. J., 1987, Correlation between the in vitro interaction of tumor cells with an organ environmental and metastatic properties in vivo, Invasion Metastasis 7: 126–129.Google Scholar
  190. 190.
    Tsuruo, T., Kawabata, H., Iida, H., and Yamori, T., 1986, Tumor-induced platelet aggregation and growth promoting factors as determinants for successful tumor metastasis, Clin. Exp. Metastasis 4: 25–33.PubMedCrossRefGoogle Scholar
  191. 191.
    Nicolson, G. L., and Dulski, K. M., 1986, Organ specificity of metastatic tumor colonization is related to organ-selective growth properties of malignant cells, Int. J. Cancer 38: 389–394.CrossRefGoogle Scholar
  192. 192.
    Nicolson, G. L., 1988, Differential organ tissue adhesion, invasion, and growth properties of metastatic rat mammary adenocarcinoma cells, Breast Cancer Res. Treat. 12: 167–176.PubMedCrossRefGoogle Scholar
  193. 193.
    Nicolson, G. L., 1987, Differential growth properties of metastatic large cell lymphoma cells in target organ conditioned medium, Exp. Cell Res. 168: 572–577.PubMedCrossRefGoogle Scholar
  194. 194.
    Holley, R. W., Bohlen, P., Fava, R., Baldwin, J. H., Kleeman, G., and Armour, R., 1980, Purification of kidney epithelial cell growth inhibitors, Proc. Natl. Acad. Sci. USA 77: 5989–5992.PubMedCrossRefGoogle Scholar
  195. 195.
    Lücker, R. F., Shipley, G. D., Moses, H. L., and Holley, R. W., 1984, Growth inhibitor from BSC-1 cells closely related to platelet type b transforming growth factor, Science 226: 705–707.CrossRefGoogle Scholar
  196. 196.
    McMahon, J.B., Farelly, J. G., and Iype, P. T., 1982, Purification and properties of rat liver protein that specifically inhibits the proliferation of non-malignant epithelial cells from rat liver, Proc. Natl. Acad. Sci. USA 79: 456–460.PubMedCrossRefGoogle Scholar
  197. 197.
    Szaniawska, B., Majewski, S., Kaminski, M. J., Noremberg, K., Swierz, M., and Janik, P., 1985, Stimulatory and inhibitory activities of lung-conditioned medium on the growth of normal and neoplastic cells in vitro, J. Natl. Cancer Inst. 75: 303–306.Google Scholar
  198. 198.
    Cavanaugh, P. G., and Nicolson, G. L., 1989, Purification and some properties of a lung-derived growth factor that differentially stimulates the growth of tumor cells metastatic to the lung, Cancer Res. 49: 3928–3933.PubMedGoogle Scholar
  199. 199.
    Cavanaugh, P. G., and Nicolson, G. L., 1991, Lung-derived growth factor that stimulates the growth of lung-metastasizing tumor cells: identification as transferrin. J. Cell. Biochem. in press.Google Scholar
  200. 200.
    Yamori, T., Iida, H., Tsukagoshi, S., and Tsuruo, T., 1988, Growth stimulatory activity of lung extract on lung colonizing colon 26 clones and its partial characterization, Clin. Exp. Metastasis 6: 131–139.PubMedCrossRefGoogle Scholar
  201. 201.
    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 339: 61–64.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1992

Authors and Affiliations

  • Paula N. Belloni
    • 1
  • Garth L. Nicolson
    • 1
  1. 1.Department of Tumor BiologyThe University of Texas M. D. Anderson Cancer CenterHoustonUSA

Personalised recommendations