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Interactions between cancer cells and the microvasculature: a rate-regulator for metastasis

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Abstract

Hematogenous metastasis is a major consideration in the staging, treatment and prognosis of patients with cancer. Key events affecting hematogeneous metastasis occur in the microvasculature. This is a brief, selective review of some interactions involving cancer cells and the microvasculature in pathologic sequence, specifically: (1) intravasation of cancer cells; (2) the arrest of circulating cancer cells in the microvasculature; (3) cancer cell trauma associated with arrest; (4) microvascular trauma; (5) the inflammatory; and (6) the hemostatic coagulative responses associated with arrest, and finally (7) angiogenesis, leading to tumor vascularization. The evidence shows that through a series of complex interactions with cancer cells, the microvasculature acts as a rate-regulator for the metastatic process, in addition to providing routes for cancer cell dissemination and arrest sites for cancer cell emboli.

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References

  1. Abraham, J. A., Mergia, A., Whang, J. L., Tumolo, A., Friedman, J., Hjerrild, K. A., Gospodarowicz, D., andFiddes, J. C., 1986, Nucleotide sequence of a bovine clone encoding the angiogenic protein, basic fibroblast growth factor.Science,233, 545–548.

    PubMed  Google Scholar 

  2. Adams, S. L., Boettiger, D., Foct, R. J., Holtzer, H., andPacifici, M., 1982, Regulation of the synthesis of extracellular matrix components in chondroblasts transformed by a temperature-sensitive mutant of Rous sarcoma virus.Cell,30, 373–384.

    PubMed  Google Scholar 

  3. Adamson, I. Y. R., Orr, F. W., andYoung, L., 1986, Effects of injury and repair of the pulmonary endothelium on lung metastasis after bleomycin.J. Pathol.,150, 279–287.

    PubMed  Google Scholar 

  4. Adamson, I. Y. R., Young, L., andOrr, F. W., 1987, Tumor metastasis after hyperoxic injury and repair of the pulmonary enothelium.Lab. Invest.,57, 71–77.

    PubMed  Google Scholar 

  5. Albrechtsen, R., Nielsen, M., Wewer, U., Engvall, E., andRuoslahti, E., 1981, Basement membrane changes in breast cancer detected by immunohistochemical staining for laminin.Cancer Res.,41, 5076–5081.

    PubMed  Google Scholar 

  6. Alitalo, K., Keski-Oja, J., Hedman, K., andVaheri, A., 1982, Loss of different pericellular matrix components of rat cells transformed by a T-class ts mutant of Rouse sarcoma virus.Virology,119, 347–357.

    PubMed  Google Scholar 

  7. Armour, J. A., andRandall, W. C., 1971, Canine left ventricular intramyocardial pressures.Am. J. Physiol.,220, 1833–1839.

    PubMed  Google Scholar 

  8. Auerbach, R., Wei Cheng Lu, Pardon, E., Gumkowski, F., Kaminska, G., andKaminski, M., 1987, Specificity of adhesion between tumor cells and capillary endothelium: anin vitro correlate of preferential metastasisin vivo.Cancer Res.,47, 1492–1496.

    PubMed  Google Scholar 

  9. Aumailley, M., andTimpl, R., 1986, Attachment of cells to basement membrane collagen Type IV.J. Cell Biol.,103, 1569–1575.

    PubMed  Google Scholar 

  10. Ausprunk, D. H., andFolkman, J., 1977, Migration and proliferation of endothelial cells in preformed and newly formed blood vessels during tumor angiogenesis.Microvasc. Res.,14, 53–65.

    PubMed  Google Scholar 

  11. Barsky, S. M., Siegal, G. P., Jannotta, F., andLiotta, L. A., 1983, Loss of basement membrane components by invasive tumors but not by their benign counterparts.Lab Invest.,49, 140–147.

    PubMed  Google Scholar 

  12. Bastida, E., Almiral, L., Jamiesin, G. A., andOrdinas, A., 1987, Cell surface sialylation of two human tumor cell lines and its correlation with their platelet-activating activity.Cancer Res.,47, 1767–1770.

    PubMed  Google Scholar 

  13. Bastida, E.,Hass, T. A.,Almirall, L.,Lauri, D.,Orr, F. W., andBuchanan, M. R., 1988, Lipoxygenase-derived fatty acid metabolites influence tumor cell adhesion to endothelial cells and their extracellular matrix.J. Clin. Invest. (in the press).

  14. Batchev, A. C., Riser, B. L., Hellner, E. G., Fligiel, S. E. G., andVarani, J., 1986, Phorbol ester binding and phorbol ester-induced arachidonic acid metabolism in a highly responsive murine fibrosarcoma cell line and in a less-responsive variant.Clin. Expl. Metastasis,4, 51–61.

    Google Scholar 

  15. Ben-Ze'ev, A., andRaz, A., 1985, Relationship between the organization and synthesis of vimentin and the metastatic capability of B16 melanoma cells.Cancer Res.,45, 2232–2641.

    Google Scholar 

  16. Bettelheim, R., Mitchell, D., andGusterson, B. A., 1984, Immunocytochemistry in the identification of vascular invasion in breast cancer.J. Clin. Pathol.,37, 364–000.

    PubMed  Google Scholar 

  17. Bevilacqua, M. P., Pober, J. S., Wheeler, M. E., Cotran, R. S., andGimbrone, M. A., Jr, 1985, Interleukin-1 acts on cultured human vascular endothelium to increase the adhesion of polymorphonuclear leukocytes, monocytes, and related leukocyte cell lines.J. Clin. Invest.,76, 2003–2011.

    PubMed  Google Scholar 

  18. Blasi, F., Vassalli, J. D., andDano, K., 1987, Urokinase-type plasminogen activator: proenzyme, receptor, and inhibitors.J. Cell Biol.,104, 801–804.

    PubMed  Google Scholar 

  19. Borgeat, P., andSamuelsson, B., 1979, Transformation of arachidonic acid by rabbit polymorphonuclear leukocytes: formation of a novel dihydroxyeicosatetranenoic acid.J. Biol. Chem.,254, 2643–2646.

    PubMed  Google Scholar 

  20. Brown, P. J., andJuliano, R. L., 1986, Expression and function of a putative cell surface receptor for fibronectin in hamster and human cell lines.J. Cell Biol.,1103, 1595–1603.

    Google Scholar 

  21. Buchanan, M. R., Hass, T. A., Lagarde, M., andGuichardant, M., 1985, 13-hydroxy-octadecadienoic acid is the vessel wall chemorepellent factor, LOX.J. Biol. Chem.,260, 16056–16059.

    PubMed  Google Scholar 

  22. Buchanan, M. R., Butt, R. W., Hirsh, J., Markham, B. A., andNazir, D. J., 1986, Role of lipoxygenase metabolism in platelet function: effect of aspirin and salicylate.Prost. Leuk. Med.,21, 157–168.

    Google Scholar 

  23. Carlsson, J., Stalnacke, G. G., Acker, H. et al., 1979, The influence of oxygen on viability and proliferation in cellular spheroids.Int. J. Rad. Oncol. Bio. Phys.,5, 2011–2020.

    Google Scholar 

  24. Carmel, R. J., andBrown, J. M., 1977, The effect of cyclophosphamide and other drugs on the incidence of pulmonary metastasis in mice.Cancer Res.,37, 145–151.

    PubMed  Google Scholar 

  25. Carrell, N., Fitzgerald, L. A., Steiner, B., Erickson, H. P., andPhillips, D. R., 1985, Structure of human platlet membrane glycoproteins IIb and IIIa as determined by electron microscopy.J. Biol. Chem.,260, 1743.

    PubMed  Google Scholar 

  26. Cavender, D., Saegusa, Y., andZiff, M., 1987, Stimulation of endothelial cell binding of lymphocytes by tumor necrosis factor.J. Immunol.,139, 1885–1860.

    PubMed  Google Scholar 

  27. Chang, Y. S., Fitzgerald, L. A., Grossi, I. M., Sundram, U., Murray, J. A., andHonn, K. V., 1988, Tumor cell expression of MRNA's coding for the integrin receptors.FASEB J.,2, A1406.

    Google Scholar 

  28. Charo, I. F., Bekeart, L. S., andPhillips, D. R., 1987, Platelet glycoprotein IIb–IIIa-like proteins mediate endothelial cell attachment to adhesive proteins and the extracellular matrix.J. Biol. Chem.,262, 9935–9938.

    PubMed  Google Scholar 

  29. Chopra, H., Hatfield, J. S., Chang, Y. S., Grossi, I. M., Fitzgerald, L. A., O'Gara, C. Y., Marnett, L. J., Diglio, G. A., Taylor, J. D., andHonn, K. V., 1988, Role of tumor cell cytoskeleton and membrane glycoprotein IRGIIb/IIIa in platelet adhesion to tumor cell membrane and tumor cell induced platelet aggregation.Cancer Res.,48, 3787–3800.

    PubMed  Google Scholar 

  30. Chopra, H.,Onoda, J. M.,Hatfield, J. S.,Fligiel, S. E. G.,Taylor, J. D., andHonn, K. V., 1988, Effect of calcium channel blockers of the phenylalkylamine, benzothiazepine, and dihydropyridine classes on integrity or tumor cell cytoskeleton, mobility of the IRGIIb/IIIa receptor and tumor cell induced platelet aggregation (Submitted).

  31. Chung, D. C., Zetter, B. R., andBrodt, D., 1988, Lewis lung carcinoma variants with differing metastatic specificities adhere preferentially to different defined extracellular matrix molecules.Invasion Metastasis,8, 103–117.

    PubMed  Google Scholar 

  32. Cheresh, D. A., 1987, Human endothelial cells synthesize and express an Arg-Gly-Asp-directed adhesion receptor involved in attachment to fibrinogen and von Willebrand factor.Proc. Natl. Acad. Sci., USA,84, 6471–6475.

    Google Scholar 

  33. Clark, R. A., Stone, P. J., El Hag, A., Calore, J. D., andFranzblau, C., 1981, Myeloperoxidase-catalyzed inactivation of alpha 1-protease inhibitor by human neutrophils.J. Biol. Chem.,256, 3348–3353.

    PubMed  Google Scholar 

  34. Collins, T., Lapierre, L. A., Fiers, W., Strominger, J. L., andPober, J. S., 1986, Recombinant human tumor necrosis factor increase mRNA levels and surface expression of HLA-A, B antigens in vascular endothelial cells and dermal fibroblastsin vitro.Proc. Natl. Acad. Sci., USA,83, 446–450.

    Google Scholar 

  35. Cotran, R. S., 1987, New roles for the endothelium in inflammation and immunity.Am. J. Pathol.,129, 407–413.

    PubMed  Google Scholar 

  36. Cotran, R. S., Gimbrone, M. A. Jr, Bevilacqua, M. P., Mendrick, D. L., andPober, J. S., 1986, Induction and detection of a human endothelial activation antigenin vivo.J. Exp. Med.,164, 661–666.

    PubMed  Google Scholar 

  37. Crissman, J., Hatfield, J. S., Menter, D. G., Sloane, B. F., andHonn, K. V., 1988, Morphological study of interaction of intravascular tumor cells with endothelial cells and subendothelial matrix.Cancer Res.,48, 4065–4072.

    PubMed  Google Scholar 

  38. Crissman, J., Hatfield, J., Schaldenbrand, M., Sloane, B., andHonn, K. V., 1985, Arrest and extravasation of B16 amelanotic melanoma in murine lungs. A light and electron microscopic study.Lab. Invest.,53, 470–478.

    PubMed  Google Scholar 

  39. D'Amore, P. A., andThompson, R. W., 1987, Mechanisms of angiogenesis.Ann. Rev. Physiol.,49, 453–464.

    Google Scholar 

  40. D'Amore, P.A., 1988, Antiangiogenesis as a strategy for antimetastasis.Sem. Thromb. Hemostasis,14, 73–78.

    Google Scholar 

  41. Dao, T. L., andYogo, H., 1967, Enhancement of pulmonary metastases by X-irradiation in rats bearing mammary cancer.Cancer,20, 2020–2025.

    PubMed  Google Scholar 

  42. Dano, K., Andreason, P. A., Grondahl-Hansen, J., Kristensen, P., Nielsen, L. S., andSkriver, L., 1985, Plasminogen activators, tissue degradation, and cancer.Adv. Cancer Res.,44, 139–266.

    PubMed  Google Scholar 

  43. Davis, W. B., Rennard, S. J., Bitterman, P. B., andCrystal, R., 1983, Pulmonary oxygen toxicity.N. Engl. J. Med.,309, 878–883.

    PubMed  Google Scholar 

  44. Dedhar, S., Ruoslahti, E., andPierschbacher, M. D., 1987, A cell surface receptor complex for collagen type I recognizes the Arg-Gly-Asp sequence.J. Cell Biol.,104, 585–593.

    PubMed  Google Scholar 

  45. Dedhar, S., Argraves, W. S., Suzuki, S., Ruoslahti, E., andPierschbacher, M. D., 1987, Human osteosarcoma cells resistant to detachment by an Arg-Gly-Asp-containing peptide overproduces the fibronectin receptor.J. Cell Biol.,105, 1175–1182.

    PubMed  Google Scholar 

  46. Dennis, J. W., Laferte, S., Waghorne, C., Breitman, J. L., andKerbel, R. S., 1987, Beta 1–6 branching of ASN-linked oligosaccharides is directly associated with metastasis.Science,236, 582–585.

    PubMed  Google Scholar 

  47. Dimitrov, D. S., 1983, Dynamic interactions between approaching surfaces of biological interest.Progr. Surface Sci.,14, 295–423.

    Google Scholar 

  48. Duffy, M. J., 1987, Do proteases play a role in cancer invasion and metastasis?Eur. J. Cancer Clin. Oncol.,23, 583–589.

    PubMed  Google Scholar 

  49. Duszyk, M., andDoroszewski, J., 1984, Hydrodynamics of interaction of particles (including cells) with surfaces.Progr. Surface Sci.,15, 369–399.

    Google Scholar 

  50. Estrada, J., andNicolson, F. L., 1984, Tumor cell-platelet aggregation does not correlate with metastatic potential of rat 13762 NF mammary adenocarcinoma tumor cell clones.Int. J. Cancer,34, 101–105.

    PubMed  Google Scholar 

  51. Evans, E. A., andParsegian, V. A., 1983, Energetics of membrane deformation and adhesion in cell and vesicle aggregation.Ann. NY Acad. Sci.,416, 13–33.

    PubMed  Google Scholar 

  52. Evans, E. A., Waugh, R., andMelnik, L., 1976, Elastic area compressibility modulus of red cell membrane.Biophys. J.,16, 585–592.

    PubMed  Google Scholar 

  53. Fitzgerald, L. A., Charo, I. F., andPhillips, 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.

    PubMed  Google Scholar 

  54. Fitzgerald, L. A., andPhillips, D. R., 1985, Calcium requirements of the platelet membrane glycoprotein IIb/IIIa complex.J. Biol. Chem.,260, 11366–11374.

    PubMed  Google Scholar 

  55. Fitzgerald, L. A., andPhillips, D. R., 1988, Structure of platelet membrane glycoproteins.Platelet Immunology, edited by T. J. Kumicki and J. George (Philadelphia, J. B. Lippincott).

    Google Scholar 

  56. Fitzgerald, L. A., Stiener, B., Rall, S. C. Jr, Lo, S.-S., andPhillips, D. R., 1987, Protein sequence of endothelial glycoprotein IIIa derived from a cDNA clone.Biol. Chem.,262, 3936–3939.

    Google Scholar 

  57. Fligiel, S. E. G., Perone, P., andVarani, J., 1985, Arachidonic acid metabolism in murine fibrosarcoma cells with differentin vivo andin vitro characteristics.Int. J. Cancer,36, 383–388.

    PubMed  Google Scholar 

  58. Folkman, J., 1985, Toward an understanding of angiogenesis: Search and discovery.Perspect. Biol. Med.,29, 10–36.

    PubMed  Google Scholar 

  59. Folkman, J., andIngber, D.E., 1987, Angiostatic steroids.Ann. Surg.,206, 374–383.

    PubMed  Google Scholar 

  60. Folkman, J., andKlagsbrun, M., 1987, Angiogenic factors.Science,235, 442–447.

    PubMed  Google Scholar 

  61. Fox, E. B., 1985, Linkage of a membrane skeleton to integral membrane glycoproteins in human platelets.J. Clin. Invest.,76, 1673–1683.

    PubMed  Google Scholar 

  62. Fujiwara, S., Wiedmann, H., Timpl, R., Lustig, A., andEngel, J., 1984, Structure and interactions of heparan sulfate proteoglycans from a mouse tumor basement membrane.Eur. J. Biochem.,143, 145–157.

    PubMed  Google Scholar 

  63. Fung, Y. C., 1984,Biomechanics. Mechanical Properties of Living Tissues (New York: Springer), p. 226.

    Google Scholar 

  64. Furcht, L. T., 1986, Critical factors controlling angiogenesis: cell products, cell matrix and growth factors.Lab. Invest.,55, 505–509.

    PubMed  Google Scholar 

  65. Gabbert, H., Gerharz, C. D., Ramp, U., andBohl, J., 1987, The nature of host tissue destruction in tumor invasion.Virch. Arch. (Cell Pathol.),52, 513–517.

    Google Scholar 

  66. Gabor, H., andWeiss, L., 1985, Mechanically induced trauma suffered by cancer cells in passing through pores in polycarbonate membranes.Invasion Metastasis,5, 71–83.

    PubMed  Google Scholar 

  67. Ganguly, P., andGould, M. L., 1979, Thrombin receptor of human platelets: thrombin binding and antithrombin properties of glycoprotein I.Br. J. Haematol.,42, 137.

    PubMed  Google Scholar 

  68. Garbisa, S., Pozzatti, R., Muschel, R. J., Sattiotti, U., Ballin, M., Goldfarb, G. H., Khoury, G., andLiotta, L. A., 1987, Secretion of type IV collagenolytic protease and metastatic phenotype: induction by transfection with c-Ha-ras but not c-Ha-ras plus AD2-E1a.Cancer Res.,47, 1523–1528.

    Google Scholar 

  69. Gasic, G. J., Gasic, T. B., andStewart, C. C., 1968, Antimetastatic effect associated with platelet reduction.Proc. Natl. Acad. Sci., USA,61, 46–52.

    Google Scholar 

  70. Gehlsen, K. R.,Argraves, W. S.,Piersbacher, M. D., andRuoslahti, E., 1988, Inhibition ofin vitro tumor cell invasion by Arg-Gly-Asp-containing synthetic peptides (Manuscript submitted).

  71. Geiger, B., Tokuyasu, K. T., Dutton, A. H., andSinger, S. J., 1981, Vinculin and intracellular protein localized at specialized sites where microfilaments terminate at cell membranes.Proc. Natl. Acad. Sci., USA,77, 4127–4131.

    Google Scholar 

  72. Gimbrone, M. A., Leapman, S. B., Cotran, R. S., andFolkman, J., 1972, Tumor dormancyin vivo be prevention of neovascularization.J. Exp. Med.,136, 261–276.

    PubMed  Google Scholar 

  73. Ginsberg, M. H., Loftus, J., Ryckwaert, J. J., Peirschbacher, M., Pytela, R., Rouslahti, E., andPlow, E. F., 1987, Immunochemical and amino-terminal sequence comparison of two cytoadhesins indicates they contain similar or identical beta subunits and distinct alpha subunits.J. Biol. Chem.,262, 5437–5440.

    PubMed  Google Scholar 

  74. Glaves, D., 1980, Metastasis: reticuloendothelial system and organ retention of disseminated malignant cells.Int. J. Cancer,26, 115–122.

    PubMed  Google Scholar 

  75. Glaves, D., 1983, Correlation between circulating cancer cells and incidence of metastasis.Br. J. Cancer,48, 665–673.

    PubMed  Google Scholar 

  76. Glaves, D., 1983, Role of polymorphonuclear leukocytes in the pulmonary clearance of arrested cancer cells.Invasion Metastasis,3, 160–173.

    PubMed  Google Scholar 

  77. Glaves, D., 1986, Intravascular death of disseminated cancer cells mediated by Superoxide anion.Invasion Metastasis,6, 101–111.

    PubMed  Google Scholar 

  78. Glaves, D., Huben, R. P., andWeiss, L., 1988, Hematogeneous dissemination of cells from human renal adenocarcinomas.Br. J. Cancer,57, 32–35.

    PubMed  Google Scholar 

  79. Gopalakrishna, R., andBarsky, S. H., 1988, Tumor promoter-induced membranebound protein kinase C regulates hematogenous metastasis.Proc. Natl. Acad. Sci., USA,85, 612–616.

    Google Scholar 

  80. Gorelik, E., 1987, Augmentation of the antimetastatic effect of anticoagulant drugs by immunostimulation in mice.Cancer Res.,47, 809–815.

    PubMed  Google Scholar 

  81. Gorelik, E., Bere, W., andHerberman, R., 1984, Role of NK cells in the antimetastatic effect of anticoagulant drugs.Int. J. Cancer,33, 87–94.

    PubMed  Google Scholar 

  82. Gross, J. L., Moscatelli, D., Jaffe, E. A., andRefkin, D. B., 1982, Plasminogen activator and collagenase production by cultured capillary endothelial cells.J. Cell Biol.,95, 974–981.

    PubMed  Google Scholar 

  83. Gross, J. L., Moscatelli, D., andRifkin, D. B., 1983, Increased capillary endothelial cell protease activity in response to angiogenic stimuliin vitro.Proc. Natl. Acad. Sci. USA,80, 2623–2627.

    PubMed  Google Scholar 

  84. Grossi, I. M.,Fitzgerald, J. A.,Umbarger, L. A.,Nelson, K. K.,Diglio, C. A.,Taylor, J. D., andHonn, K. V., 1988, Bidirectional control of membrane expression and/or activation of the tumor cell IRGIIb/IIIa receptor and tumor cell adhesion by lipoxygenase products or arachidonic acid and linoleic acid.Cancer Res. (In press).

  85. Grossi, I. M., Hatfield, J. S., Fitzgerald, L. H., Newcombe, M., Taylor, J. D., andHonn, K. V., 1988, Role of tumor cell glycoproteins immunologically related to glycoproteins Ib and IIb/IIIa in tumor cell-platlet and tumor cell-matrix interactions.FASEB J.,2, 2385–2395.

    PubMed  Google Scholar 

  86. Hagmar, B., andRyd, W., 1977, Tumor cell locomotion: a factor in metastasis formation? Influence of cytochalasin B on a tumor dissemination pattern.Int. J. Cancer,19, 576–580.

    PubMed  Google Scholar 

  87. Hajjar, K. A., Hamel, N. M., Harpel, P. C., andNachman, R. L., 1987, Binding of tissue plasminogen activator to cultured human endothelial cells.J. Clin. Invest.,80, 1712–1719.

    PubMed  Google Scholar 

  88. Hart, I. R., Raz, A., andFidler, I. J., 1980, Effect of cytoskeleton disrupting agents on the metastatic behavior of melanoma cells.J. Natl. Cancer Inst.,64, 891–899.

    PubMed  Google Scholar 

  89. Hayman, E. G., Pierschbacher, M. D., andRuoslahti, E., 1985, Detachment of cells from culture substrate by soluble fibronectin peptides.J. Cell Biol.,100, 1948–1954.

    PubMed  Google Scholar 

  90. Hirata, H., andTanaka, K., 1984, Artificial metastases and decrease of fibrinolysis in the nude mouse lung after hemithrocic irradiation.Clio. Exp. Metastasis,2, 311–319.

    Google Scholar 

  91. Honn, K. V., Grossi, I. M., Chopra, H., Steinert, B. W., Onoda, J. M., Nelson, K. K., andTaylor, J. D., 1988, Role of tumor cell eicosanoids and membrane glycoproteins IRGpIb and IRGpIIb/IIIa in metastasis.Eicosanoid, Lipid Peroxidation and Cancer, edited by S. Nigam, D. L. H. McBrien and T. G. Slater (Berlin: Springer Verlag) (In press).

    Google Scholar 

  92. Honn, K. V., Grossi, I. M., Fitzgerald, L. A., Umbarger, L. A., Diglio, C. A., andTaylor, J. D., 1988, Lipoxygenase products regulate IRGpIIb/IIIa receptor mediated adhesion of tumor cells to endothelial cells, subendothelial matrix and fibronectin.Proc. Soc. exp. Biol. Med.,189, 130–135.

    PubMed  Google Scholar 

  93. Honn, K. V.,Grossi, I. M.,Nelson, K. K.,Umbarger, L. A.,Fitzgerald, L. A.,Hatfield, J. S.,Fligiel, S. E. G.,Steinert, B. W.,Taylor, J. D., andOnoda, J. M., 1988, Correlation among expression of glycoprotein IRGpIIb/IIIa, tumor cell induced platelet aggregation, tumor cell adhesion and lung colonization in elutriated subpopulations of the B16 amelanotic melanoma and Lewis lung carcinomaCancer Res. (In press).

  94. Honn, K. V., Grossi, I. M., Steinert, B. W., Chopra, H., Onoda. J. M., Nelson, K. K., andTaylor, J. D., 1988, Lipoxygenase regulation of membrane expression of tumor cell glycoproteins and subsequent metastasis. In:Advances in Prostaglandins, Thromboxane, and Leukotriene Research, Vol. 18, edited by P. Wong, B. Samuelsson and F. Sun (New York: Raven Press) (In press).

    Google Scholar 

  95. Honn, K. V., Onoda, J. M., Pampalona, K., Battaglia, M., Neagos, G., Taylor, J. D., Diglio, C. A., andSloane, B. F., 1985, Inhibition by dihydropyridine class calcium channel blockers of tumor cell-platelet-endothelial cell interactionsin vitro metastasisin vivo.Biochem. Pharmacol.,34, 235–141.

    PubMed  Google Scholar 

  96. Honn, K. V., Powers, W. E., andSloane, B. F. (eds), 1986,Mechanisms of Cancer Metastasis. Potential Therapeutic Implications (Boston, MA: Martinus Nijhoff).

    Google Scholar 

  97. Honn, K. V., Steinert, B. W., Onoda, J. M., andSloane, B. F., 1987, The role of platelets in metastasis.Biorheology,24, 127–137.

    PubMed  Google Scholar 

  98. Hopkins, N. K., Ogglesby, T. D., Bundy, F. L., andGorman, R. R., 1984, Biosynthesis and metabolism of 15-hydroxy-5,8,11,13-eicosatetranenoic acid by human umbilical vein endothelial cells.J. Bio. Chem.,259, 14048–14053.

    Google Scholar 

  99. Humphries, M. J., Matsumoto, K., White, S. L., andOlden, K., 1986, Oligosac-charide modifications by swainsonine treatment inhibits pulmonary colonization by B16-F10 murine melanoma cells.Proc. Natl. Acad. Sci., USA,83, 1752–1756.

    Google Scholar 

  100. Humphries, M. J., Olden, K., andYamada, K. M., 1986, A synthetic peptide from fibronectin inhibits experimental metastasis of murine melanoma cells.Science,233, 467–470.

    Google Scholar 

  101. Humphries, M.J., Matsumoto, K., White, S. L., andOlden, K., 1986, Inhibition of experimental metastasis by castanospermine in mice: blockage of two distinct stages of tumor colonization by liogosaccharide processing inhibitors.Cancer Res.,46, 5215–5222.

    PubMed  Google Scholar 

  102. Humphries, M. J., Yamada, K. M., andOlden, 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.

    PubMed  Google Scholar 

  103. Hynes, R. O., 1986, Integrins: a family of cell surface receptors.Cell,48, 549–554.

    Google Scholar 

  104. Ishikawa, M., Koga, Y., Hosokawa, M., andKobayashi, H., 1986, Augmentation of B16 melanoma lung colony formation in C57BL/6 mice having marked granulocytosis.Int. J. Cancer,37, 919–924.

    PubMed  Google Scholar 

  105. Jones, C. L., Nelson, K. K., Hatfield, J., Honn, K. V., andOnoda, J. M., 1988, Regulation of metastasis by polymorphonuclear neutrophils.Proc. Am. Assoc. Cancer Res.,27, 62.

    Google Scholar 

  106. Jones, P. A., andDe Clerk, Y. A., 1982, Extracellular matrix destruction by invasive tumor cells.Cancer Metastasis Rev.,1, 289–318.

    PubMed  Google Scholar 

  107. Kanclerz, A., andShapman, J. D., 1987, The effectiveness ofcis-platinum, cyclophosphamide and melphalan in treating disseminated tumor cells in mice.Clin. Expl. Metastasis,5, 199–212.

    Google Scholar 

  108. Kerbel, R. S., Dennis, J. W., Lagarde, A. E., andFrost, P., 1982, Tumor progression in metastasis: an experimental approach using lectin resistant tumor variants.Metastasis Rev.,1, 99–140.

    Google Scholar 

  109. Khato, J., Sati, H., andSuzuki, M., 1979, Filterability and flow characteristics of leukemic and non-leukemic tumor cell suspensions through polycarbonate filters in relation to hematogeneous spread of cancer.Tohoku J. Exp. Med.,128, 273–284.

    PubMed  Google Scholar 

  110. Kieffer, N., Najet, D., Wicki, A., Titeux, M., Heuri, A., Mishal, Z., Breton-Gorius, J., Vainchenker, W., andClemetson, K. J., 1986, Expression of platlet glycoprotein Ibα in HEL cells.J. Biol. Chem.,261, 15854–15862.

    PubMed  Google Scholar 

  111. Kimura, A. K., Mehta, P., Xiang, J., Lawson, D., Dugger, D., Kao, K. J., andAmbrose, L. L., 1987, The lack of correlation between experimental metastatic potential and platelet aggregating activity of B16 melanoma clones viewed in relation to tumor cell heterogeneity.Clin Expl. Metastasis,5, 125–133.

    Google Scholar 

  112. Kinjo, M., 1978, Lodgement and extravasation of tumor cells in blood-borne metastases: an electron microscopic observation.Br. J. Cancer,38, 293–301.

    PubMed  Google Scholar 

  113. Kramer, R. H., Gonzales, R., andNicolson, G. L., 1980, Metastatic tumor cells adhere preferentially to the extracellular matrix underlying vascular endothelial cells.Int. J. Cancer,26, 639–645.

    PubMed  Google Scholar 

  114. Kramer, R. H., Vogel, K. G., andNicolson, G. L., 1982, Solubilization and degradation of subendothelial matrix glycoproteins and proteoglycans by metastatic tumor cells.J. Biol. Chem.,257, 2678–2686.

    PubMed  Google Scholar 

  115. Kramer, R. H., Vogel, K. G., andNicolson, G. L., 1982, Tumor cell interactions with vascular endothelial cells and their extracellular matrix.Prog. Clin. Biol. Res.,89, 333–351.

    PubMed  Google Scholar 

  116. Konstantinov, A. A., Peskin, A. V., Popova, E. Y., Khomutou, G. B., andRuuge, E. K., 1987, Superoxide generation by the respiratory chain of tumor mitochondria.Biochem. Biophys. Acta,894, 1–10.

    PubMed  Google Scholar 

  117. Lapis, K., Paku, S., andLiotta, L. A., 1988, Endothelialization of embolized tumor cells during metastasis formation.Clin. Exp. Metastasis,6, 73–89.

    PubMed  Google Scholar 

  118. Lauri, D.,Orr, F. W.,Bastida, E.,Sauder, D., andBuchanan, M. R., 1988, Differential effects of interleukin-1 and fMLP on chemotaxis and human endothelium adhesivity for A549 tumor cells (Manuscript submitted).

  119. Leroyer, V., Werner, L., Shaughnessy, S., Goddard, G. J., andOrr, F. W., 1987, Chemiluminescence and oxygen radical generation by Walker carcinosarcoma cells following chemotactic stimulation.Cancer Res.,47, 4771–4775.

    PubMed  Google Scholar 

  120. Lichtenstein, A., 1987, Stimulation of respiratory burst of muriperitoneal inflammatory neutrophils by conjugation with tumor cells.Cancer Res.,47, 2211–2217.

    PubMed  Google Scholar 

  121. Lichtenstein, A. K., Kahle, J., Berek, J., andZighelboim, J., 1984, Successful immunotherapy with intraperitoneal Corynebacterium parvum in a murine ovarian cancer model is associated with recruitment of tumor-lytic neutrophils into the peritoneal cavity.J. Immunol.,133, 519–526.

    PubMed  Google Scholar 

  122. Lichtner, R. B., andNicolson, G. L., 1987, Effects of the pyrimido-pyrimidine derivative RX-RA 85 on metastatic tumor cell-vascular endothelial cell interactions.Clin. Expl. Metastasis,5 (3), 219–231.

    Google Scholar 

  123. Liotta, L. A., 1986, Tumor invasion and membranes. Role of the extracellular matrix.Cancer Res.,46, 1–7.

    PubMed  Google Scholar 

  124. Liotta, L. A., Thorgeirsson, U. P., andGarbisa, S., 1982, Role of collagenases in tumor cell invasion.Cancer Metastasis Rev.,1, 277–288.

    PubMed  Google Scholar 

  125. Liotta, L. A., Horan Hand, P., Rao, C. N., Bryant, G., Barsky, S. H., andSchlom, J., 1985, Monoclonal antibodies to the human laminin receptor recognize structurally distinct sites.Expl. Cell Res.,156, 117–126.

    Google Scholar 

  126. Mayhew, E., andGlaves, D., 1984, Quantitation of tumorigenic disseminating and arrested cancer cells.Br. J. Cancer,50, 159–166.

    PubMed  Google Scholar 

  127. McCarthy, J., Palmard, S., andFurcht, L., 1983, Migration by hapotaxis of a Schwann cell tumor line to the basement membrane glycoprotein laminin.J. Cell Bio.,97, 772–779.

    Google Scholar 

  128. McCarthy, J. B., Basara, M. L., Palm, S. L., Sas, D. F., andFurcht, 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.

    PubMed  Google Scholar 

  129. McCarthy, J., Hagen, S. T., andFurcht, L. T., 1986, Fibronectin contains distinct adhesion and motility-promoting domains for metastatic melanoma cells.J. Cell Biol.,102, 179–188.

    PubMed  Google Scholar 

  130. McKever, R. P., Bennett, E. M., andMartin, M. N., 1983, Identification of two structurally and functionally distinct sites on human platelet membrane glycoprotein IIb-IIIa using monoclonal antibodies.J. Biol. Chem.,258, 5269.

    PubMed  Google Scholar 

  131. McMillan, T. J., Rao, J., andHart, I. R., 1986, Enhancement of experimental metastasis by pretreatment of tumor cells with hydroxyusea.Int. J. Cancer,38, 61–65.

    PubMed  Google Scholar 

  132. Menter, D. G., Harkins, C., Onoda, J. M., Riorden, W., Sloane, B. F., Taylor, J. D., andHonn, K. V., 1987, Inhibition of tumor cell induced platelet aggregation by prostacyclin and carbacyclin: an ultrastructural study.Invasion Metastasis,7, 109–128.

    PubMed  Google Scholar 

  133. Menter, D. G., Hatfield, J. S., Harkins, C. J., Sloane, B. F., Taylor, J. D., Crissman, J. D., andHonn, K. V., 1987, Tumor cell-platelet interactionsin vitro and their relationship toin vivo arrest of hematogenously circulating tumor cells.Clin. Expl. Metastasis,5, 65–78.

    Google Scholar 

  134. Menter, D. G., Sloane, B. F., Steinert, B. W., Onoda, J. M., Craig, R., Harkins, C., Taylor, J. D., andHonn, K. V., 1987, Platelet enhancement of tumor cell adhesion to subendothelial matrix. Role of platelet cytoskeleton and platelet membrane.J. Natl. Cancer Inst.,79, 1077–1098.

    PubMed  Google Scholar 

  135. Menter, D. G., Steinert, B. W., Sloane, B. F., Gundlach, N., O'Gara, C. Y., Marnett, L. J., Diglio, C., Walz, D., Taylor, J. D., andHonn, K. V., 1987, Role of platelet membrane in enhancement of tumor cell adhesion to endothelial cell extracellular matrix.Cancer Res.,47, 6751–6762.

    PubMed  Google Scholar 

  136. Meromsky, L., Lotan, R., andRaz, A., 1986, Implications of endogeneous tumor cell surface lectings as mediators of cellular interactions and lung colonization.Cancer Res.,46, 5270–5275.

    PubMed  Google Scholar 

  137. Milas, L., Malenica, B., andAllergetti, N., 1979, Enhancement of artificial lung metastases in mice caused by cyclophosphamide. I. Participation of impairment of host antitumor resistance.Cancer Immunol. Immunother'. 6, 191–196.

    Google Scholar 

  138. Moore, A., Ross, G. D., andMachman, E., 1978, Interaction of platelet membrane receptors with von Willebrand factor, ristocetin, and the Fc region of immunoglobulin G.J. Clin. Invest.,62, 1053.

    PubMed  Google Scholar 

  139. Moore, J. V., andDixon, B., 1977, Metastasis of a transplantable mammary tumour in rats treated with cyclophosphamide and/or irradiation.Br. J. Cancer,36, 221–226.

    PubMed  Google Scholar 

  140. Morganroth, M. L., Till, G. O., Kunkel, R. G., andWard, P. A., 1986, Complement and neutrophil-mediated injury of perfused rat lungs.Lab. Invest.,54, 507–514.

    PubMed  Google Scholar 

  141. Moscatelli, D., 1985, Collagenase and plasminogen activator production by bloodvessel associated cells in response to angiogenic preparations.Intracellular Protein Catabolism edited by E. A. Khairallah, J. S. Bond and J. W. C. Bird (New York: Liss), pp. 669–671.

    Google Scholar 

  142. Moscatelli, D., Presta, M., andRifkin, D. B., 1986, Purification of a factor from human placenta that stimulated capillary endothelial cell protease production, DNA synthesis and migration.Proc. Natl. Acad. Sci., USA,83, 2091–2095.

    Google Scholar 

  143. Muller, W. A., andGimbrone, M. A. Jr, 1986, Plasmalemmal proteins of cultured vascular endothelial cells exhibit apical-basal polarity: analysis by surface-selective iodination.J. Cell Biol.,103, 2389–2402.

    PubMed  Google Scholar 

  144. Mundy, G. R., DeMartino, S., andRowe, D. W., 1981, Collagen and collagen-derived fragments and chemotactic for tumor cells.J. Clin. Invest.,68, 1102–1105.

    PubMed  Google Scholar 

  145. Nakajima, M., Irimura, T., DiFerrante, D., DiFerrante, N., andNicolson, G. L., 1983, Heparan sulfate degradation: relation to tumor invasive and metastatic properties of mouse B16 melanoma sublines.Science,220, 611–613.

    PubMed  Google Scholar 

  146. Nakajima, M., Irimura, T., andNicolson, G. L., 1986, Tumor metastasis-associated heparanase (heparan sulfate endoglycosidase) activity in human melanoma cells.Cancer Lett.,31, 277–283.

    PubMed  Google Scholar 

  147. Nakajima, M., Welch, D. R., Belloni, P. N., andNicolson, G. L., 1987, Degradation of basement membrane type IV collagen and lung subendothelial matrix by rat mammary adenocarcinoma cell clones of differing metastatic potentials.Cancer Res.,47, 4869–4876.

    PubMed  Google Scholar 

  148. Nicolson, G. L., 1982, Metastatic tumor cell attachment and invasion assay utilizing vascular endothelial cell monolayers.J. Histochem. Cytochem.,30, 214–220.

    PubMed  Google Scholar 

  149. Nicolson, G. L., 1988, Cancer metastasis: Tumor cell and host organ properties important in metastasis to specific secondary sites.Biochim. Biophys. Acta (Cancer Rev.) (In press).

  150. Nicolson, G. L., andCustead, S. E., 1985, Effects of chemotherapeutic drugs on platelet and metastatic tumor cell-endothelial cell interactions as a model for assessing vascular endothelial integrity.Cancer Res.,45, 331–336.

    PubMed  Google Scholar 

  151. Nicolson, G. L., Irimura, T., Nakajima, M., Updyke, T. V., andPoste, G., 1984, The cellular interactions of metastatic tumor cells with special reference to endothelial cells and their basal lamina-like matrix.Hemostatic Mechanisms and Metastasis, edited by K. V. Honn and B. F. Sloane (Boston: Martinus Nijhoff), pp. 295–318.

    Google Scholar 

  152. Nicosia, R. F., andMadri, J. A., 1987, The microvascular extracellular matrix.Am. J. Pathol.,128, 78–90.

    PubMed  Google Scholar 

  153. Niedbala, M. J., Madiyalakan, R., Matta, K., Crickard, K., Sharma, M., andBernacki, R. J., 1987, Role of glycosidases in human ovarian carcinoma cell mediated degradation of subendothelial extracellular matrix.Cancer Res.,47, 4634–4641.

    PubMed  Google Scholar 

  154. Oberly, L. W., andBuettner, G. R., 1979, Role of Superoxide dismutase in cancer: a review.Cancer Res.,39, 1141–1149.

    PubMed  Google Scholar 

  155. Okito, J. R., Pidard, D., Newman, P. J., Montgomery, R. R., andKunicki, T. J., 1985, On the association of glycoprotein Ib and actin-binding protein in human platelets.J. Cell Biol.,100, 317.

    PubMed  Google Scholar 

  156. Olden, K., Humphries, M. J., andWhite, S. L., 1985, Biochemical effects and cancer therapeutic potential of tunicamycin.Monoclonal Antibodies and Cancer Therapy, edired by R. Riesfeld and S. Sell (New York: Alan R. Liss), pp. 443–472.

    Google Scholar 

  157. Onoda, J. M., Nelson, K. K., Grossi, I. M., Umbarger, L. A., Taylor, J. D., andHonn, K. V., 1988, Separation of high and low metastatic subpopulations from solid tumors by centrifugal elutriation.Proc. Soc. Exp. Biol. Med.,187, 250–255.

    PubMed  Google Scholar 

  158. Orr, F. W., Phan, S. H., Varani, J., Ward, P. A., Kreutzer, D. L., Webster, R. D., andHenson, P. M., 1979, Chemotactic factor for tumor cells derived from the C5a fragment of complement component C5.Proc. Natl. Acad. Sci., USA,76, 1986–1989.

    Google Scholar 

  159. Orr, F. W., Mokashi, S., andDelikatny, J., 1982, Generation of a complement-derived chemotactic factor for tumor cells in experimentally induced peritoneal exudates and its effect on the local metastasis of circulating tumor cells.Am. J. Pathol.,108, 112–118.

    PubMed  Google Scholar 

  160. Orr, F. W., andMokashi, S., 1985, Effect of leukocyte activation on the formation of heterotypic tumor-cell aggregatesin vitro.Int. J. Cancer,35, 101–106.

    PubMed  Google Scholar 

  161. Orr, F. W., Adamson, I. Y. R., andYoung, L., 1985, Pulmonary inflammation generates chemotactic activity for tumor cells and promotes lung metastasis.Am. Rev. Respir.Dis.,131, 607–611.

    PubMed  Google Scholar 

  162. Orr, F. W., Adamson, I. Y. R., andYoung, L., 1986, Promotion of pulmonary metastasis in mice by bleomycin-induced endothelial injury.Cancer Res.,46, 891–897.

    PubMed  Google Scholar 

  163. Orr, F. W., andWarner, D. J. A., 1987, Effects of neutrophil-mediated pulmonary endothelial injury on the localization and metastasis of circulating Walker carcinosarcoma cells.Invasion Metastasis,7, 183–196.

    PubMed  Google Scholar 

  164. Ossowski, L., 1988, Plasminogen-activator dependent pathways in the dissemination of human tumor cells in the chick embryo.Cell,52, 321–328.

    PubMed  Google Scholar 

  165. Ostrowski, L. E., Ahsan, A., Suther, B. P., Pagast, P., Bain, D. L., Wong, C., Patal, A., andSchultz, R. M., 1986, Selective inhibition of proteolytic enzymes in anin vivo mouse model for experimental metastasis.Cancer Res.,46, 4121–4128.

    PubMed  Google Scholar 

  166. Ozaki, T., Yoshida, K., Ushijima, K., andHayashi, H., 1971, Studies on the mechanisms of invasion in cancer. II.In vivo effects of a factor chemotactic for cancer cells.Int. J. Cancer,7, 93–100.

    PubMed  Google Scholar 

  167. Paget, S., 1889, The disttibution of secondary growths in cancer of the breast.Lancet,i, 571–573.

    Google Scholar 

  168. Painter, R. G., andGinsberg, M., 1982, Concanavalin A induces interactions between surface glycoproteins and the platelet cytoskeleton.J. Cell Biol.,92, 565.

    PubMed  Google Scholar 

  169. Palmblad, J., Malmsten, D., Uden, A. M., Radmark, O., Engsted, L., andSamuelsson, B., 1981, Leukotriene B4 is a potent and stereospecific stimulator of neutrophil chemotaxis and adherence.Blood,58, 658–661.

    PubMed  Google Scholar 

  170. Pepin, J. M., andLanger, R. O. 1985, Effects of dimethyl sulfoxide (DMSO) on bleomycin-induced pulmonary fibrosis.Biochem. Pharmacol.,34, 2386–2389.

    PubMed  Google Scholar 

  171. Peterson, D. M., Stathhopoulos, N. A., Georgio, D. D., Helums, J. D., andMoike, J. L., 1987, Shear-induced platelet aggregation requires von Willebrand factor and platelet membrane glycoproteins Ib and IIb–IIIa.Blood,69, 625.

    PubMed  Google Scholar 

  172. Phillips, D. R., andAgin, P. P., 1977, Platelet plasma membrane glycoproteins. Evidence for the presence of nonequivalent disulfide bonds using nonreduced-reduced two-dimensional gel electrophoresis.J. Biol. Chem.,252, 21.

    Google Scholar 

  173. Phillips, D. R., andShuman, M. A., 1986,Biochemistry of Platelets (New York: Academic Press).

    Google Scholar 

  174. Pidard, D., Montgomery, R. R., Bennett, J. S., andKunicki, T. J., 1983, Interaction of AP-2, a monoclonal antibody specific for the human platelet membrane glycoprotein IIb–IIIa complex, with intact platelets.J. Biol. Chem.,258, 12582–12586.

    PubMed  Google Scholar 

  175. Pober, J. S., Bevilacqua, M. P., Mendrick, D. L., Lapiere, L. A., Fiers, W., andGimbrone, M. A. Jr, 1986, Two distinct monocines, interleukin 1 and tumor necrosis factor, each independently induce biosynthesis and transient expression of the same antigen on the surface of cultured human vascular endothelial cells.J. Immunol.,136, 1680–1687.

    PubMed  Google Scholar 

  176. Pober, J. S., Gimbrone, M. A. Jr, Lapierre, L. A., Mendrick, D. L., Fiers, W., Rothlein, R., andSpringer, T. A., 1986, Overlapping patterns of activation of human endothelial cells by interleukin 1, tumor necrosis factor, and immune interferon.J. Immunol.,137, 1893–1896.

    PubMed  Google Scholar 

  177. Pober, J. S., Lapierre, L. A., Stolpen, A. H., Brock, T. A., Springer, T. A., Fiers, W., Bevilacqua, M. P., Mendrick, D. L., andGimbrone, M. A. Jr, 1987, Activation of cultured human endothelial cells by recombinant lymphotoxin: comparison with tumor necrosis factor and interleukin species.J. Immunol.,138, 3319–3324.

    PubMed  Google Scholar 

  178. Polverini, P. J., andLeibovich, S. J., 1984, Induction of neovasculaturizationin vivo and endothelial proliferationin vitro by tumor-associated macrophages.Lab. Invest.,51, 635–642.

    PubMed  Google Scholar 

  179. Poupon, M. F., Pauwels, C., Jasmin, C., Antoine, E., Lascaux, V., andRosa, B., 1984, Amplified pulmonary metastases of a rat rhabdomyosarcoma in response to nitrosourea treatment.Cancer Treat. Rep.,68, 749–758.

    PubMed  Google Scholar 

  180. Pytela, R., Pierschbacher, M. D., andRuoslahti, E., 1985, Identification and isolation of a 140-Kd cell surface glycoprotein with properties expected of a fibronectin receptor.Cell,40, 191–198.

    PubMed  Google Scholar 

  181. Pytela, R., Pierschbacher, M. D., andRuoslahti, E., 1985, A 125/115-kDa cell surface receptor specific for vitronectin interacts with the arginine-glycine-aspartic acid adhesion sequence derived from fibronectin.Proc. Natl. Acad. Sci., USA,82, 5766–5770.

    Google Scholar 

  182. Rao, C. N., Margulies, I. M. K., Tralka, T. S., Terranova, V. P., Madri, J. A., andLiotta, L., 1982, Isolation of a subunit og laminin and its role in molecular structure and tumor cell attachment.J. Biol. Chem.,257, 9740–9744.

    PubMed  Google Scholar 

  183. Rao, M. C., Barsky, S. H., Terranova, V. P., andLiotta, L., 1983, Isolation of a tumor cell laminin receptor.Biochem. Biophys. Res. Commun.,111, 804–808.

    PubMed  Google Scholar 

  184. Raz, A., andBen-Ze'ev, A., 1987, Cell-contact and architecture of malignant cells and their relationship to metastasis.Cancer Metastasis Rev.,6, 3–21.

    PubMed  Google Scholar 

  185. Rothlein, R., Dustin, M. L., Marlin, S. D., andSpringer, T. A., 1986, A human intercellular adhesion molecule (ICAM-1) distinct from LFA-1.J. Immunol.,137, 1270–1274.

    PubMed  Google Scholar 

  186. Rozhin, J., Robinson, D., Stevens, M. A., Lah, T. T., Honn, K. V., Ryan, R. E., andSloane, B. F., 1987, Properties of a plasma membrane-associated cathepsin B-like cysteine proteinase in metastatic B16 melanoma variants.Cancer Res.,47, 6620–6628.

    PubMed  Google Scholar 

  187. Ruoslahti, E., andPierschbacher, M. D., 1987, New perspectives in cell adhesion: RGD and intergrins.Science,238, 491–497.

    PubMed  Google Scholar 

  188. Santoso, S., Zimmermann, U., Neppert, J., andMueller-Eckhardt, C., 1986, Receptor patching and capping of platelet membranes induced by monoclonal antibodies.Blood,67, 343–349.

    PubMed  Google Scholar 

  189. Sato, H., andSuzuki, M., 1976, Deformability and viability of tumor cells by transcapillary passage with reference to organ affinity in metastasis in cancer.Fundamental Aspects of Metastasis, edited by L. Weiss (Amsterdam: North-Holland), pp. 311–317.

    Google Scholar 

  190. Schmid-Schonbein, G. W., 1986, Rheology of leukocytes.Handbook of Bioengineering, edited by R. Skalak and S. Chien (New York: Pergamon), chap. 13.

    Google Scholar 

  191. Schmid-Schonbein, G. W., 1987, Leukocyte kinetics in the microcirculation.Bioheology,24, 139–151.

    Google Scholar 

  192. Shah, S. V., Baricos, W. H., andBasci, A., 1987, Degradation of human glomerular basement by stimulated neutrophils. Activation of a metalloproteinase(s) by reactive oxygen metabolites.J. Clin. Invest.,79, 25–31.

    PubMed  Google Scholar 

  193. Shoenfeld, Y., Tal, A., Berliner, S., andPinkhas, J., 1986, Leukocytosis in nonhematological malignancies-a possible tumor-associated marker.J. Cancer Res. Clin. Oncol.,111, 54–58.

    PubMed  Google Scholar 

  194. Sindelar, W. F., Tralka, T. S., andKetcham, A. S., 1975, Electron microscopic observations on formation of pulmonary metastases.J. Surg. Res.,18, 137.

    PubMed  Google Scholar 

  195. Sloane, B. F., andHonn, K. V., 1984, Cysteine proteinases and metastasis.Cancer Metastasis Rev.,3, 249–263.

    PubMed  Google Scholar 

  196. Sloane, B. F., Rozhin, J., Hatfield, J. S., Crissman, J. D., andHonn, K. V., 1987, Plasma membrane-associated cysteine proteinases in human and animal tumors.Exp. Cell Biol.,55, 209–224.

    PubMed  Google Scholar 

  197. Sobel, M. E., Yamamoto, T., DeCrombrughe, B., andPastan, I., 1981, Regulation of procollagen messenger ribonculeic acid levels in Rous sarcoma virus transformed chick embryo fibroblasts.Biochemistry,20, 2678–2684.

    PubMed  Google Scholar 

  198. Soberman, R. J., Harper, T. W., Betteridge, D., Lewis, R. A., andAusten, K. F., 1985, Characterization and separation of the arachidonic acid 5-lipoxygenase and linoleic acid W-6 lipoxgenase (arachidonic acid 15-lipoxygenase) of human polymor-phonuclear leukocytes.J. Biol. Chem.,260, 4508–4515.

    PubMed  Google Scholar 

  199. Solum, N. A., andOlsen, T. M., 1984, Glycoprotein Ib in the Triton-insoluble (cytoskeletal) fraction of blood platelets.Biochem. Biophys. Acta,799, 209.

    PubMed  Google Scholar 

  200. Sommer, A.,Brewer, M. T.,Thompson, R. C.,Moscatelli, D.,Presta, M., andRifkin, D. B., 1987/8, Primary structure of a human placental angiogenesis factor and cDNA sequence of a clone coding for a homologous protein from a human hepatoma cell line.Biochem. Biophys. Res. Commun.

  201. Starkey, J. R., Liggitt, H. D., Jones, W., andHosick, H. L., 1984, Influence of migratory blood cells on the attachment of tumor cells to vascular endothelium.Int. J. Cancer,34, 535–543.

    PubMed  Google Scholar 

  202. Steel, G. G., andAdams, K., 1977, Enhancement by cytotoxic agents of artificial pulmonary metastasis.Br. J. Cancer,36, 653–658.

    PubMed  Google Scholar 

  203. Stewart, R. A. N., andHacker, M. P., 1984, Enhancement of B16 melanoma pulmonary colonization in mice following bleomycin in hyperoxia.Proc. Am. Assoc. Cancer Res.,25, 60.

    Google Scholar 

  204. Strauli, P., andWeiss, L., 1977, Cell locomotion and tumor penetration.Eur. J. Cancer,13, 1–12.

    PubMed  Google Scholar 

  205. Suzuki, S., Argraves, W. S., Pytela, R., Arai, H., Krusius, T., Pierschbacher, M. D., andRouslahti, E., 1986, cDNA and amino acid sequences of the cell adhesion protein receptor recognizing vitronectin reveal a transmembrane domain and homologies with other adhesion protein receptors.Proc. Natl. Acad. Sci., USA,83, 8614–8618.

    Google Scholar 

  206. Tabilio, A., Rosa, J. P., Testa, U., Kieffer, N., Nurden, A. T., DelCanizo, M. C. J., Breton-Gorius, J., andVainchenken, W., 1984, Expression of platelet membrane glycoproteins and alpha-granule proteins by a human erythroleukemia cellline (HEL).Embo J.,3, 453–459.

    PubMed  Google Scholar 

  207. Takahashi, M., Fujiwara, M., Kishi, K., Sakai, C., Sanada, C., Sanada, M., Moriyama, Y., andShibata, A., 1985, CSF producing all bladder cancer: case report and characteristics of the CSF produced by tumor cells.Int. J. Cell Cloning,3, 294–303.

    PubMed  Google Scholar 

  208. Tanaka, N. G., Tohgo, A., andOgawa, H., 1986, Platelet-aggregation activities of metastasizing tumor cells. V.In situ roles of platelets in hematogeneous metastasis.Invasion Metastasis,6, 209–224.

    PubMed  Google Scholar 

  209. Tao, T.-W., andJohnson, L. K., 1982, Altered adhesiveness of tumor cells surface variants with reduced metastasizing capacity-reduced adhesiveness to vascular wall components in culture.Int. J. Cancer,30, 763–766.

    PubMed  Google Scholar 

  210. Terranova, V. P., Williams, J. E., andLiotta, L. A., 1984, Modulation of the metastatic activity of melanoma cells by laminin and fibronectin.Science,226, 982–985.

    PubMed  Google Scholar 

  211. Thiagarajan, P., Shapiro, S., Swererlitsch, L., andMcCord, S., 1987, A human erythroleukemic cell line synthesizes a functionally active glycoprotein IIb/IIIa complex capable of binding fibrinogen.Biochem. Biophys. Acta,924, 127–134.

    PubMed  Google Scholar 

  212. Thompson, W. D., Shiach, K. J., Fraser, R. A., McIntosh, L. C., andSimpson, J. G., 1987, Tumours acquire their vasculature by vessel incorporation, not vessel in growth.J. Pathol.,151, 323–332.

    PubMed  Google Scholar 

  213. Thorgeirsson, U. P., Liotta, L. A., Kalebic, T., Margulies, I. M., Thomas, K., Rios-Candelore, M., andRusso, R. G., 1982, Effect of natural protease inhibitors and a chemoattractant on tumor cell invasionin vitro.J. Natl. Cancer Inst.,69, 1049–1054.

    PubMed  Google Scholar 

  214. Till, G. O., Johnson, K. J., Kunkel, R., andWard, P. A., 1982, Intravascular activation of complement and acute lung injury.J. Clin. Invest.,69, 1126–1135.

    PubMed  Google Scholar 

  215. Tohgo, A., Tanaka, N. G., andOgawa, H., 1986, Platelet aggregating activities of metastasizing tumor cells. IV. Effects of cell surface modification on thrombin generation, platelet aggregation and subsequent lung colonization.Invasion Metastasis,6, 58–68.

    PubMed  Google Scholar 

  216. Turpeenniemi-Hujanen, T., Thorgeirsson, U. P., Hart, I. R., Grant, S. S., andLiotta, L. A., 1985, Expression of collagenase IV (basement membrane collagenase) activity in murine tumor cell hybrids that differ in metastatic potential.J. Natl. Cancer Inst.,75, 99–103.

    PubMed  Google Scholar 

  217. Tuszynski, G. P., Tatiana, B. G., Rothman, V. L., Knudsen, K. A., andGasic, G. J., 1987, Thrombospondin. A potentiator of tumor cell metastasis.Cancer Res.,47, 4130–4133.

    PubMed  Google Scholar 

  218. Tyagi, J. S., Hirano, H., Merlino, G. T., andPastan, I., 1983, Transcriptional control of the fibronectin gene in chick embryo fibroblasts transformed by Rous sarcoma virus.J. Biol. Chem.,258, 5787–5793.

    PubMed  Google Scholar 

  219. Van den Brenk, H. A. S., Stone, M., Kelly, H., Orton, C., andSharpington, C., 1984, Promotion of growth of tumour cells in acutely inflammed tissues.Br. J. Cancer,30, 246–260.

    Google Scholar 

  220. Vaupel, P., andMuller-Klieser, W., 1983, Interstitieller Raum and Mikromilieu in malignen tumoren.Mikrozirk Forsch Klin, Vol. 2 (Basel: Karger).

    Google Scholar 

  221. VanPutten, L. M., Kram, K. L. J., Van Dierendonck, H. H. C., Smink, T., andFuzy, M., 1975, Enhancement by drugs of metastatic lung nodule formation after intravenous tumour cell injection.Int. J. Cancer,15, 588–595.

    PubMed  Google Scholar 

  222. Varani, J., andFantone, J. C., 1982, Phorbol myristae acetate-induced adherence of Walker 256 carcinosarcoma cells.Cancer Res.,42, 190–197.

    PubMed  Google Scholar 

  223. Varani, J., Dixit, V. M., Fligiel, S. E. G., McKeever, P. E., andCarey, T. E., 1986, Thrombospondin-induced attachment and spreading of human squamous carcinoma cells.Expl. Cell Res.,167, 376–390.

    Google Scholar 

  224. Vlodavsky, I., Atzmon, A. R., andFuks, Z., 1982, Tumor cell attachment to the vascular endothelium and subsequent degradation of the subendothelial extracellular matrix.Expl. Cell Res.,140, 149–159.

    Google Scholar 

  225. Vlodavsky, I., Fuks, Z., Bar-Ner, M., Ariav, Y., andSchirrmacher, V., 1983, Lymphoma cell-mediated degradation of sulfated proteoglycans in the subendothelial extracellular matrix: relationship to tumor cell metastasis.Cancer Res.,43, 2704–2711.

    PubMed  Google Scholar 

  226. Walther, H. E., 1948,Krebsmetastasen (Basel: Schwabe), pp. 296–297.

    Google Scholar 

  227. Warburton, M. J., Ferns, S. A., Kimbell, R., Rudland, P. S., Monoghand, P., andGusterson, B. A., 1987, Loss of basement membrane deposits and development of invasive potential by virally-transformed rat mammary cells are independent of collagenase production.Int. J. Cancer,40, 270–277.

    PubMed  Google Scholar 

  228. Ward, P. M., andWeiss, L., 1985, Effects of single versus triple intravenous injections of B16 melanoma cells on the development of pulmonary tumors in mice.Int. J. Cancer,36, 519–521.

    PubMed  Google Scholar 

  229. Warren, B. A., 1979, Tumor angiogenesis.Tumor Blood Circulation, edited by H.-I. Peterson (Boca Raton, FL: CRC Press), pp. 49–75.

    Google Scholar 

  230. Weiss, L., 1965, Studies on cell deformability. I. Effect of surface charge.J. Cell Biol.,26, 735–739.

    Google Scholar 

  231. Weiss, L., 1979, Dynamic aspects of cancer cell populations in metastasis.Am. J. Pathol.,97, 601–608.

    PubMed  Google Scholar 

  232. Weiss, L., 1980, Cancer cell traffic from the lungs to the liver: an example of metastatic inefficiency.Int. J. Cancer,25, 385–392.

    PubMed  Google Scholar 

  233. Weiss, L., 1985,Principles of Metastasis (Orlando, FL: Academic Press), pp. 3–9.

    Google Scholar 

  234. Weiss, L., 1985,Principles of Metastasis, (Orlando: Academic Press), pp. 134–159.

    Google Scholar 

  235. Weiss, L., 1985,Principles of Metastasis, (Orlando, FL: Academic press), pp. 162.

    Google Scholar 

  236. Weiss, L., 1986, A critical overview of the metastatic porcess.Mechanisms of Cancer Metastasis: Potential Therapeutic Implications, edited by K. V. Honn, W. E. Powers and B. F. Sloane (Boston, MA: Martinus Nijhoff), pp. 23–40.

    Google Scholar 

  237. Weiss, L., 1986, Metastatic inefficiency: causes and consequences.Cancer Rev.,3, 1–24.

    Google Scholar 

  238. Weiss, L., 1987, The hemodynamic destruction of circulating cancer cells.Biorheology,24, 105–115.

    PubMed  Google Scholar 

  239. Weiss, L., 1988, Biomechanical destruction of cancer cells in the heart: a rateregulator for hematogenous metastasis.Invasion Metastasis,8, 228–237.

    PubMed  Google Scholar 

  240. Weiss, L., 1988, Biomechanical destruction of cancer cells in the skeletal muscle: a rate-regulator for hematogenous metastasis.Clin. Expl. Metastasis (In press).

  241. Weiss, L., andClement, K., 1969, Studies on cell deformability: some rheological considerations.Expl. Cell. Res.,58, 379–387.

    Google Scholar 

  242. Weiss, L., andDimitrov, D. S., 1984, A fluid mechanical analysis of the velocity, adhesion and destruction of cancer cells in capillaries during metastasis.Cell Biophys,6, 9–22.

    PubMed  Google Scholar 

  243. Weiss, L., andDimitrov, D. S., 1986, Mechanical aspects of the lungs as cancer cellkilling organs during hematogenous metastasis.J. Theor. Biol.,121, 307–321.

    PubMed  Google Scholar 

  244. Weiss. L., Dimitrov, D. S., andAngelova, M., 1985, The hemodynamic destruction of intravascular cancer cells in relation to myocardial metastasis.Proc. Natl. Acad. Sci., USA,82, 5737–5741.

    Google Scholar 

  245. Weiss, L., andGlaves, D., 1983, Cancer cell damage at the vascular endothelium.Ann. NY Acad. Sci.,416, 681–692.

    PubMed  Google Scholar 

  246. Weiss, L., Grundmann, E., Torhorst, J., Hartveit, F., Moberg, I., Eder, M., Fenoglio-Preiser, C. M., Napier, J., Horne, C. H. W., Lopez, M. J., Shaw-Dunn, R. I., Sugar, J., Davies, J. D., Day, D. W., andHarlos, J. P., 1986, Hematogenous metastatic patterns in colonic carcinoma: an analysis of 1541 necropsies.J. Pathol.,150, 195–203.

    PubMed  Google Scholar 

  247. Weiss, L., andHarlos, J. P., 1972, Some speculations on the rate of adhesion of cells to coverslips.J. Theor. Biol.,37, 169–179.

    PubMed  Google Scholar 

  248. Weiss, L., andHarlos, J. P., 1972, Short-term interactions between cell surfaces. Progr.Surface Sci.,1, 355–405.

    Google Scholar 

  249. Weiss, L., andHarlos, J. P., 1987, Unpublished data.

  250. Weiss, L., Orr, F. W., andHonn, K. V., 1988, Interactions of cancer cells with the microvasculature during metastasis.FASEB J.,2, 12–21.

    PubMed  Google Scholar 

  251. Weiss, L., andSuh, O. W., 1985, The quantitation of some aspects of invasionin vivo andin vitro.Basic Mechanisms and Clinical Tremtment of Tumor Metastasis, edited by M. Toriss and Y. Yoshida (New York: Academic Press), pp. 23–40.

    Google Scholar 

  252. Weiss, L., Ward, P. M., Harlos, J. P., andHolmes, J. C., 1984, Target organ patterns of tumors in mice following the arterial dissemination of B16 melanoma cells.Int. J. Cancer,33, 825–830.

    PubMed  Google Scholar 

  253. Weiss, L., Ward, P. M., andHolmes, J. C., 1983, Liver to lung traffic of cancer cells.Int. J. Cancer,32, 79–83.

    PubMed  Google Scholar 

  254. Weiss, L., Peppin, G., Ortiz, X., Ragsdale, C., andTest, S. T., 1985, Oxidative autoactivation of latent collagenase by human neutrophils.Science,227, 747–749.

    PubMed  Google Scholar 

  255. Wencel-Drake, J. D., Plow, E. F., Kunicki, T. J., Woods, V. L., Keller, D. M., andGinsberg, M. H., 1986, Localization of internal pools of membrane glycoproteins involved in platelet adhesive responses.Am. J. Pathol.,124, 324–334.

    PubMed  Google Scholar 

  256. Willis, R. A., 1952,The Spread of Tumours in the Human Body (London: Butterworth), pp. 284–285.

    Google Scholar 

  257. Wood, S., 1958, Pathogenesis of metastasis formation observedin vivo in the rabbit ear chamber.Arch. Pathol.,66, 550–568.

    Google Scholar 

  258. Woods, D. L. Jr, Wolff, L. E., andKeller, D. M., 1986, Restins platelets contain a substantial centrally located pool of glycoprotein IIb–IIIa complex which may be accessible to some but not other extracellular proteins.J. Biol Chem.,261, 15242.

    PubMed  Google Scholar 

  259. Woolley, D. E., 1984, Collagenolytic mechanisms in tumor cell invasion.Cancer Metastasis Rev.,3, 361–372.

    PubMed  Google Scholar 

  260. Woolley, D. E., 1984, Proteolytic enzymes of invasive cells.Invasion. Experimental and Clinical Implications, edited by M. M. Mareel and K. C. Calman (Oxford: Oxford University Press), pp. 228–251.

    Google Scholar 

  261. Yogeeswaran, G., 1983, Cell surface glycolipids and glycoproteins in malignant transformation.Adv. Cancer Res.,38, 289–350.

    PubMed  Google Scholar 

  262. Zeidman, I., 1961, The fate of circulating cancer cells. I. Passage of cells through capillaries.Cancer Res.,121, 38–39.

    Google Scholar 

  263. Zeidman, I., andBuss, J. M., 1952, Transpulmonary passage of tumor cell emboli.Cancer Res.,12, 731–733.

    PubMed  Google Scholar 

  264. Zucker, S., Lysik, R. M., Ramamurthy, N. S., Golub, L. M., Wieman, J. M., andWilkie, D. P., 1985, Diversity of melanoma plasma membrane proteinases: inhibition of collagenolytic and cytolytic activities by minocycline.J. Natl. Cancer Inst.,75, 517–525.

    Google Scholar 

  265. Zucker, S., Lysik, R. M., Wieman, J., Wilkie, D. P., andLane, B., 1985, Diversity of human pancreatic cancer cell proteinases: role of cell membrane metalloproteinases in collagenolysis and cytolysis.Cancer Res.,45, 6168–6178.

    PubMed  Google Scholar 

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Weiss, L., Orr, F.W. & Honn, K.V. Interactions between cancer cells and the microvasculature: a rate-regulator for metastasis. Clin Exp Metast 7, 127–167 (1989). https://doi.org/10.1007/BF01787020

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