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Biomechanical interactions of cancer cells with the microvasculature during hematogenous metastasis

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Abstract

Different aspects of hematogenous metastasis are discussed from the viewpoint of biomechanics. The processes considered include the role of primary tumor pressure, cell locomotor forces and degradation, in invasion of tissues and intravasation by cancer cells. Consideration of the fluid dynamics of cancer cell movement along capillaries lead to the view thatin vivo, arrest is primarily due to mechanical trapping of cancer cells, and that the pathobiologic role of so-called adhesion molecules is not mainly in the arrest and adhesion of cancer cells, but rather in stimulating their proliferation by signal induction. As a consequence of deformation from spherical-to-cylindrical shape in the microvasculature, demands for increased surface membrane area leads to increases in surface membrane tension above critical levels for rupture, and the cancer cells are rapidly and lethally damaged. The possibility is briefly discussed of increasing the susceptibility of circulating cancer cells to mechanical trauma, as a form of anti-metastatic therapy.

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References

  1. WeissL, OrrFW, HonnKV: Interactions between cancer cells and the microvasculature: A rate-regulator for metastasis. Clin exp Metastasis 7: 127–167, 1980

    Google Scholar 

  2. OrrFW, BuchananMR, WeissL (eds): Microcirculation in Cancer Metastasis. CRC Press, Boca Raton, FL, 1991

    Google Scholar 

  3. YoungJS, LumsdenCE, StalkerAL: The significance of the ‘Tissue pressure’ of normal testicular and of neoplastic (Brown-Pearce carcinoma) tissue in the rabbit. J Path Bact 62: 313–333, 1950

    PubMed  Google Scholar 

  4. HoriK, SuzukiM, AbeI, SaitoS, SatoH: A micro-occlusion technique for the measurement of the microvascular pressure in tumor and subcutis. Gann 74: 122–127, 1983

    PubMed  Google Scholar 

  5. TrinkausJP: Cells into organs. The forces that shape the embryo. 2nd ed. Prentice-Hall Inc, Englewood Cliffs, NJ, pp 370–414, 1984

    Google Scholar 

  6. WeissL: Studies on cellular adhesion in tissue culture. IV. The alteration of substrata by cell surfaces. Exp Cell Res 25: 504–517, 1961

    PubMed  Google Scholar 

  7. WeissL, CoombsRRA: The demonstration of rupture of cell surfaces by an immunological technique. Exp Cell Res 30: 331–338, 1963

    PubMed  Google Scholar 

  8. WeissL, LachmannPJ: The origin of an antigenic zone surrounding HeLa cells cultured on glass. Exp Cell Res 36: 86–91, 1964

    PubMed  Google Scholar 

  9. MaslowDE: Collagenase effects on cancer cell invasiveness and motility. Invasion Metastasis 7: 297–310, 1987

    PubMed  Google Scholar 

  10. FolgerR, WeissL, GlavesD, SubjeckJR, HarlosJP: Translational movements of macrophages through media of different viscosities. J Cell Sci 31: 245–257, 1978

    PubMed  Google Scholar 

  11. WeissL: Studies on cellular adhesion in tissue culture. V Some effects of enzymes on cell detachment. Exp Cell Res 30: 5409–5420, 1963

    Google Scholar 

  12. WeissL: GlavesD: Effects on migration inhibiting factor(s) on thein vitro detachment of macrophages J Immunol 115: 1362–1365, 1975

    PubMed  Google Scholar 

  13. WeissL: Cellular locomotive pressure in relation to initial cell contacts. J Theor Biol 6: 275–281, 1964

    PubMed  Google Scholar 

  14. WeissL, HarlosJP, ElkinG: Measurements of compression of Ehrlich acites tumor cells and their relevance to hematogenous metastasis. Biorheology 28: 185–193, 1991

    PubMed  Google Scholar 

  15. RosenEM, GoldbergID: Protein factors which regulate cell motilityin vitro. Cell Devel. Biol. 25: 1079–1087, 1989

    Google Scholar 

  16. SuhO, WeissL: The development of a technique for the morphometric analysis of invasion in cancer. J Theor Biol 108: 547–562, 1984

    Google Scholar 

  17. ZeidmanI, BussJM: Transpulmonary passage of tumor cell emboli. Cancer Res 12: 731–733, 1952

    PubMed  Google Scholar 

  18. PrinzmetalM, OrnitzEM, SinkinB, BergmanHC: Arteriovenous anastomoses in liver, spleen and lungs. Am J Physiol 152: 48–52, 1948

    Google Scholar 

  19. WillisRA: The spread of tumours in the human body. Butterworth, London, 1973

    Google Scholar 

  20. DelRegatoJ: Physiopathology of metastasis. In: WeissL, GilbertHA (eds) Pulmonary Metastasis. GK Hall, Boston, pp 104–113, 1978

    Google Scholar 

  21. BrossIDJ, ViadanaE, PickrenJW: Does generalized metastasis occur directly from the primary? J chronic Dis 28: 149–159, 1975

    PubMed  Google Scholar 

  22. WeissL, GrundmannE, TorhorstJ, HartveitF, MobergI, EderM, Fenoglio-PreiserCM, NapierJ, HorneCHW, LopezMJ, Shaw-DunnRI, SugarJ, DaviesJD, DayDW, HarlosJP: Hematogenous metastatic patterns in colonic carcinoma: An analysis of 1541 necropsies. J Pathol 150: 195–203, 1986

    PubMed  Google Scholar 

  23. WeissL: Metastatic inefficiency and regional therapy for liver metastases from colorectal carcinoma. Reg Cancer Treatment 2: 77–81, 1989

    Google Scholar 

  24. DimitrovDS: Dynamic interactions between approaching surfaces of biological interest. Progr Surface Sci 14: 295–423, 1984

    Google Scholar 

  25. WeissL, Schmid-SchonbeinGW: Biomechanical interactions of cancer cells with the microvasculature during metastasis. Cell Biophys 14: 187–215, 1989

    PubMed  Google Scholar 

  26. WeissL, DimitrovDS, AngelovaM: The hemodynamic destruction of cancer cells in relation to myocardial metastasis. Proc nat Acad Sci USA 82: 5737–5741, 1985

    PubMed  Google Scholar 

  27. HammerDA, LauffenburgerDA: A dynamical model for receptor-mediated cell adhesion to surfaces in viscous shear flow. Cell Biophys 14: 139–173, 1989

    PubMed  Google Scholar 

  28. CrissmanJD, HatfieldJ, SchaldenbrandJ, SloaneBF, HonnKV: Arrest and extravasation of B16 amelanotic melanoma in murine lungs. Lab Invest 53: 470–478, 1985

    PubMed  Google Scholar 

  29. WeissL: Metastatic inefficiency. Adv Cancer Res 54: 159–211, 1990

    PubMed  Google Scholar 

  30. WeissL, NannmarkU, JohanssonBR, BaggeU: Lethal deformation of cancer cells in the microcirculation: a potential rate-regulator of hematogenous metastasis. Int J Cancer 51: 103–113, 1992

    Google Scholar 

  31. WeissL: The biomechanics of cancer cell traffic, arrest and intravascular destruction. In: OrrFW, BuchananMR, WeissL (eds) Microcirculation in cancer metastasis, CRC Press, Boca Raton, FL, pp 131–144, 1991

    Google Scholar 

  32. BlomqvistG, ScolnikG, BraideM, BjurstenLM, BlixtA, BaggeU: Differences in lodgement of tumour cells in muscle and liver. Clin exp Metastasis 6: 285–289, 1988

    PubMed  Google Scholar 

  33. SatoH, SuzukiM: Deformability and viability of tumor cells by transcapillary passage with reference to organ affinity in metastasis in cancer. In: WeissL (ed) Fundamental Aspects of Metastasis. North Holland, Amsterdam, pp 311–318, 1976

    Google Scholar 

  34. WeissL, AschBB, ElkinG: Effects of cytoskeletal perturbation on the sensitivity of ehrlich ascites tumor cell membranes to mechanical trauma. Invasion Metastasis 11: 93–101, 1991

    PubMed  Google Scholar 

  35. WeissL: Studies on cell deformability. II Effects of some proteolytic enzymes. J Cell Biol 30: 39–43, 1966

    PubMed  Google Scholar 

  36. WeissL, BernackiRJ, ElkinG, HillmanM: Effects of Doxorubicin on the sensitivity of L1210 leukemia cells to deformation-associated trauma. Cell Biophys 18: 57–67, 1991

    PubMed  Google Scholar 

  37. WeissL: Biomechanical destruction of cancer cells in the heart: a rate-regulator for hematogenous metastasis. Invasion Metastasis 8: 228–237, 1988

    PubMed  Google Scholar 

  38. WeissL: Biomechanical destruction of cancer cells in skeletal muscle: a rate-regulator for hematogenous metastasis. Clin Exp Metastasis 7: 483–491, 1989

    PubMed  Google Scholar 

  39. GaborH, WeissL: Mechanically induced trauma suffered by cancer cells in passing through pores in polycarbonate membranes. Invasion Metastasis 5: 71–83, 1985

    PubMed  Google Scholar 

  40. RazA, Ben-Ze'evA: Modulation of the metastatic capability in B16 melanoma by cell shape. Science 221: 1307–1310, 1983

    PubMed  Google Scholar 

  41. ElsonEL: Cellular mechanics as an indicator of cytoskeletal structure and function. Ann Rev Biophys Biophys Chem 17: 397–430, 1988

    Google Scholar 

  42. WurzingerLJ, OpitzR, WolfM, Schmid-SchonbeinH: ‘Shear induced platelet activation’—A critical review. Biorheology 22: 399–413, 1985

    PubMed  Google Scholar 

  43. FrangosJA, McIntyreLV, IveCL: Flow effects on prostacyclin production by cultured human endothelial cells. Science 227: 1477–1479, 1985

    PubMed  Google Scholar 

  44. FolkmanJ, MosconaA: Role of cell shape in growth control. Nature 273: 345–349, 1978

    PubMed  Google Scholar 

  45. IngberDE, FolkmanJ: Tension and compression as basic determinants of cell form and function: utilization of a cellular tensegrity mechanism. In: SteinWD, BronnerF (eds) Cell Shape: Determinants, Regulation, and Regulatory Role. Academic Press, New York, pp 3–31, 1989

    Google Scholar 

  46. IngberDE, FolkmanJ: Mechanochemical switching between growth and differentiation during fibroblast growth factor-stimulated angiogenesisin vitro: role of extracellular matrix. J Cell Biol 109: 317–330, 1989

    PubMed  Google Scholar 

  47. KuterI, Johnson-WintB, BeaupreN, GrossJ: Collagenase secretion accompanying changes in cell shape occur only in the presence of a biologically active cytokine. J Cell Sci 92: 473–485, 1989

    PubMed  Google Scholar 

  48. AndoJ, NomuraH, KamiyaA: The effect of fluid shear stres on the migration and proliferation of cultured endothelial cells. Microvascular Res 33: 62–70, 1987

    Google Scholar 

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Weiss, L. Biomechanical interactions of cancer cells with the microvasculature during hematogenous metastasis. Cancer Metast Rev 11, 227–235 (1992). https://doi.org/10.1007/BF01307179

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