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Biomechanical interactions of cancer cells with the microvasculature during metastasis

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Abstract

Metastasis is a major, life-threatening complication of cancer. The bloodstream is the most important disseminative route for cancer cells liberated from their parent tumors. Single circulating cancer cells are arrested in the microvasculature, where the vast majority are killed by rapid or slow processes, and the relatively few survivors grow into micrometastases.

We review the underlying causes of one type of rapid cancer cell death in the microcirculation, namely, that caused by biomechanical interactions of cancer cells with microvessel walls, which may result in cell surface membrane expansion and lethal rupture. These lethal interactions appear to be important rate-regulators in hematogenous metastasis, and to dictate some aspects of metastatic patterns. Although these are not the only interactions involving cancer cells, in contrast to others involving cellular and humoral defense mechanisms, they have received comparatively little attention.

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References

  1. Weiss, L. (1985a),Principles of Metastasis, Academic, Orlando, FL.

    Google Scholar 

  2. Weiss, L. (1971),Fed. Proc. 30, 1649.

    PubMed  CAS  Google Scholar 

  3. Weiss, L. and Harlos, J. P. (1971),Progr. Surface Sci. 1, 355.

    Article  Google Scholar 

  4. Hogg, R., Healy, T. W., and Furstenau, D. W. (1966),Trans. Faraday Soc. 62, 1638.

    Article  CAS  Google Scholar 

  5. Nir, S. (1976),Progr. Surface Sci. 8, 1.

    Article  Google Scholar 

  6. Israelachvili, J. N. and Pashley, R. M. (1983),Biophysics of Water, Franks, F., ed., Wiley, London.

    Google Scholar 

  7. Dolowy, K. (1984),Progr. Surface Sci. 15, 245.

    Article  CAS  Google Scholar 

  8. Parsegian, V. A. and Rand, P. P. (1983),Ann. NY Acad. Sci. 416, 1.

    Article  PubMed  CAS  Google Scholar 

  9. Weiss, L., Jung, O. S., and Zeigel, R. (1972),Int. J. Cancer 9, 48.

    PubMed  CAS  Google Scholar 

  10. Weiss, L. (1968a),Expl. Cell Res. 51, 609.

    Article  CAS  Google Scholar 

  11. Weiss, L. (1968b),Expl. Cell Res. 53, 603.

    Article  Google Scholar 

  12. Weiss, L. (1974),Expl. Cell Res. 83, 311.

    Article  CAS  Google Scholar 

  13. Weiss, L., Nir, S., Harlos, J. P., and Subjeck, J. R. (1975),J. Theor. Biol. 51, 439.

    Article  PubMed  CAS  Google Scholar 

  14. Weiss, L. and Harlos, J. P. (1972),J. Theor. Biol. 37, 169.

    Article  PubMed  CAS  Google Scholar 

  15. McCarthy, J. B., Basara, M. L., Palm, S. L., Sas, D. F., and Furcht, L. T. (1985),Cancer Metastasis Revs. 4, 125.

    Article  CAS  Google Scholar 

  16. Dimitrov, D. S. (1983),Progr. Surface Sci. 14, 295.

    Article  CAS  Google Scholar 

  17. Sorensen, T. S., ed. (1979),Dynamics and instability of fluid interfaces, Springer Verlag, Berlin.

    Google Scholar 

  18. Tozeren, H. and Skalak, R. (1979),Int. J. Multiphase Flow 5, 395.

    Article  Google Scholar 

  19. Fenton, B. M., Wilson, D. W., and Cohelet, G. R. (1985),Pflugers Arch. 403, 396.

    Article  PubMed  CAS  Google Scholar 

  20. Gaehtgen, P., Ley, K., Pries, A. R., and Muller, R. (1985),Prog. Appl. Microcirc. 7, 15.

    Google Scholar 

  21. Bagge, U., Skolnik, G., and Ericson, L. E. (1983),J. Cancer Res. Clin. Oncol. 105, 134.

    Article  PubMed  CAS  Google Scholar 

  22. Weiss, L. (1967),The Cell Periphery, Metastasis and Other Contact Phenomena, N. Holland, Amsterdam, pp. 192–213.

    Google Scholar 

  23. Tillmanns, H., Ikeda, S., Hansen, H., Sorma, J. S., Fauvel, J. M., and Bing, R. J. (1974),Circ. Res. 34, 561.

    PubMed  CAS  Google Scholar 

  24. Baage, U. and Branemark, P. I. (1977),Adv. Microcirc. 7, 1.

    Google Scholar 

  25. Schmid-Schönbein, G. W., Usani, S., Skalak, R., and Chien, S. (1980),Microvasc. Res. 19, 45.

    Article  PubMed  Google Scholar 

  26. Weiss, L., Dimitrov, D. S., and Angelova, M. (1985),Proc. Natl. Acad. Sci. USA 82, 5737.

    Article  PubMed  CAS  Google Scholar 

  27. Weiss, L. and Dimitrov, D. S. (1986),J. Theor. Biol. 121, 307.

    Article  PubMed  CAS  Google Scholar 

  28. Weiss, L., and Dimitrov, D. S. (1984),Cell Biophys. 6, 9.

    PubMed  CAS  Google Scholar 

  29. Dimitrov, D. S. and Jain, R. K. (1984),Biochim. Biophys. Acta 779, 437.

    PubMed  CAS  Google Scholar 

  30. Weiss, L. (1985b),Principles of Metastasis, Academic, Orlando, FL, pp. 82–95.

    Google Scholar 

  31. Aumailley, M. and Timpl, R. (1986),J. Cell Biol. 103, 1569.

    Article  PubMed  CAS  Google Scholar 

  32. Auerbach, R., Lu, W-C., Pardon, E., Gumkowski, F., Kaminska, G., and Kaminski, M. (1987),Cancer Res. 47, 1492.

    PubMed  CAS  Google Scholar 

  33. Hynes, R. O. (1987),Cell 48, 549.

    Article  PubMed  CAS  Google Scholar 

  34. Juliano, R. L. (1987),Biochim. Biophys. Acta 907, 261.

    PubMed  CAS  Google Scholar 

  35. Mayrovitz, H. N. (1982),White blood cells: Morphology and Rheology as Related to Induction, Bagge, U., Boru, G. V. R., Gaehtgens, P., eds. Martinus Nijhoff, The Hague, pp. 82–88.

    Google Scholar 

  36. Bagge, U., Blixt, A., and Strid, K.-G. (1983),Int. J. Microcirc. Clin. Exp. 2, 215.

    PubMed  CAS  Google Scholar 

  37. Bagge, U., Amundson, B., and Lauritzen, C. (1980),Acta Physiol. Scand. 108, 159.

    Article  PubMed  CAS  Google Scholar 

  38. Barosso-Arranda, F., Schmid-Schönbein, G. W., Fuerfach, B. W., and Engler, R. L. (1988),Circ. Res., in press.

  39. Yamakawa, T., Yamaguchi, S., Niimi, H., and Sugiyama, I. (1987),Circ. Shock 22, 232.

    Google Scholar 

  40. Horse, S. D. and Lipowsky, H. H. (1987),Microvasc. Res. 34, 363.

    Article  Google Scholar 

  41. Schmid-Schönbein, G. W. (1987),Prog. Appl. Microcirc. 12, 223.

    Google Scholar 

  42. Valerius, N. H., Stendahl, O., Hartwig, J. H., and Stossel, T. P. (1981),Cell 24, 195.

    Article  PubMed  CAS  Google Scholar 

  43. Schmid-Schönbein, G. W., Skalak, R., Sung, K. L. P., and Chien, S. (1982)White Blood Cell Morphology and Rheology as Related to Function, Bagge, U., Boru, G. V. R., Gaehtgen, P., eds., Martinus Nijhoff, The Hague, pp. 21–31.

    Google Scholar 

  44. McDonough, P. F., Rauzzino, M. J., and Weidow, M. J. (1988),FASEB J. 2, A1873.

    Google Scholar 

  45. Hammerschmidt, D. E., Harris, P. D., Wayland, J. H., Craddock, P. R., and Jacob, H. S. (1981),Am. J. Pathol. 102, 146.

    PubMed  CAS  Google Scholar 

  46. Barosso-Aranda, J., and Schmid-Schönbein, G. W. (1988),Circ. Res., submitted.

  47. Weiss, L., Orr, F. W., and Honn, K. V. (1988),FASEB J. 2, 12.

    PubMed  CAS  Google Scholar 

  48. Weiss, L. (1982),Liver Metastasis, Weiss, L. and Gilbert, H. A., eds. G. K. Hall, Boston, MA, pp. 126–149.

    Google Scholar 

  49. Glaves, D., Huben, R. P., and Weiss, L. (1988),Brit. J. Cancer 57, 32.

    PubMed  CAS  Google Scholar 

  50. Weiss, L., Mayhew, E., Rapp, D. G., and Holmes, J. C. (1982),Brit. J. Cancer 45, 44.

    PubMed  CAS  Google Scholar 

  51. Liotta, L. A., Kleinerman, J., and Saidel, G. M. (1974),Cancer Res. 34, 997.

    PubMed  CAS  Google Scholar 

  52. Butler, T. P. and Gullino, P. M. (1975)Cancer Res. 35, 512.

    PubMed  CAS  Google Scholar 

  53. Fidler, I. J. and Kripke, M. L. (1977),Science 197, 893.

    Article  PubMed  CAS  Google Scholar 

  54. Weiss, L., Ward, P. M., and Holmes, J. C. (1983),Int. J. Cancer 32, 79.

    Article  PubMed  CAS  Google Scholar 

  55. Sindelar, W. R., Tralka, T. S., and Ketcham, A. S. (1975),J. Surg. Res. 18, 137.

    Article  PubMed  CAS  Google Scholar 

  56. Wallace, A. C., Chew, E-C., and Jones, D. S. (1978),Pulmonary Metastasis, Weiss, L. and Gilbert, H. A. eds., G. K. Hall, Boston, MA, pp. 26–42.

    Google Scholar 

  57. Kinjo, M. (1978),Br. J. Cancer 38, 293.

    PubMed  CAS  Google Scholar 

  58. Machado, E. A., Gerard, D. A., Mitchell, J. R., Lozzio, B. B., and Lozzio, C. B. (1982),Virch. Arch A 396, 73.

    Article  CAS  Google Scholar 

  59. Crissman, J., Hatfield, J., Schaldenbrand, M., Sloane, B. F., and Honn, K. V. (1985),Lab Invest. 53, 470.

    PubMed  CAS  Google Scholar 

  60. Mayhew, E. and Glaves, D. (1984),Brit. J. Cancer 50, 159.

    PubMed  CAS  Google Scholar 

  61. Vaage, J. (1985),Basic Mechanisms and Clinical Treatment of Tumor Metastasis, Torisu, M., and Yoshida, T., eds., Academic, Orlando, FL, pp. 163–187.

    Google Scholar 

  62. Glaves, D. (1983),Brit. J. Cancer 48, 665.

    PubMed  CAS  Google Scholar 

  63. Glaves, D. and Mayhew, E. (1984),Cancer Drug Delivery 1, 293.

    PubMed  CAS  Google Scholar 

  64. Weiss, L. (1980),Int. J. Cancer 25, 385.

    Article  PubMed  CAS  Google Scholar 

  65. Fidler, I. J. (1973),Eur. J. Cancer 9, 223.

    PubMed  CAS  Google Scholar 

  66. Liotta, L. A., Kleinerman, J., and Saidel, G. M. (1976),Cancer Res. 36, 889.

    PubMed  CAS  Google Scholar 

  67. Zeidman, I. and Buss, J. M. (1952),Cancer Res. 12, 731.

    PubMed  CAS  Google Scholar 

  68. Zeidman, I., Gamble, W. J., and Clovis, W. L. (1956),Cancer Res. 16, 814.

    PubMed  Google Scholar 

  69. Bierman, H. R., Byron, R. L., Kelly, K. H., and Cordes, F. (1951),Cancer Res. 11, 236.

    Google Scholar 

  70. Prinzmetal, M., Ornitz, E. M., Sinkin, B., and Bergman, H. C. (1948),Amer. J. Physiol. 152, 48.

    PubMed  CAS  Google Scholar 

  71. Tobin, C. E. and Zariquiey, M. O. (1950),Proc. Soc. Exp. Biol. Med. 75, 827.

    PubMed  CAS  Google Scholar 

  72. Schmid-Schönbein, G. W., Skalak, R., Usani, S., and Chien, S. (1980),Microvasc. Res. 19, 18.

    Article  PubMed  Google Scholar 

  73. Mayrovitz, H. N. and Rubin, R. (1985),Microvasc. Res. 29, 282.

    Article  PubMed  CAS  Google Scholar 

  74. Blixt, A., Braida, M., Myrhage, R., and Bagge, U. (1987),Int. J. Microcirc. Clin. Exp. 6, 273.

    PubMed  CAS  Google Scholar 

  75. Ley, K., Mayer, J.-U., Intaglietta, M., and Arfors, K.-E. (1988),FASEB J. 2, A1871.

    Google Scholar 

  76. Chien, S., Tvetenstraud, C. D., Farrell-Epstein, M., and Schmid-Schönbein, G. W. (1985),Am. J. Physiol. 248, H568.

    PubMed  CAS  Google Scholar 

  77. Goldsmith, H. L. (1976),Fundamental Aspects of Metastasis, Weiss, L., ed., N. Holland, Amsterdam, pp. 99–120.

    Google Scholar 

  78. Carter, S. B. (1965),Nature (London) 208, 1183.

    Article  CAS  Google Scholar 

  79. McCarthy, J. B. and Furcht, L. T. (1984),J. Cell Biol. 98, 1474.

    Article  PubMed  CAS  Google Scholar 

  80. McCarthy, J. B., Hagen, S. T., and Furcht, L. T. (1986),J. Cell Biol. 102, 179.

    Article  PubMed  CAS  Google Scholar 

  81. Skolnik, G., Ericson, L. E., and Bagge, U. (1983),J. Cancer Res. Clin. Oncol. 105, 30.

    Article  PubMed  CAS  Google Scholar 

  82. Nicolson, G. L. (1988),Cancer Metastasis Revs., in press.

  83. Zeidman, I. (1961),Cancer Res. 21, 38.

    PubMed  CAS  Google Scholar 

  84. Weiss,L. (1965),J. Cell Biol. 26, 735.

    Article  Google Scholar 

  85. Weiss, L. and Clement, K. (1969),Exp. Cell Res. 58, 379.

    Article  PubMed  CAS  Google Scholar 

  86. Schmid-Schönbein, G. W. (1981),Biophys. J. 36, 243.

    PubMed  Google Scholar 

  87. Dong, C., Skalak, R., Sung, K. L. P., Schmid-Schönbein, G. W., and Chien, S. (1988),J. Biomech. Eng. 110, 27.

    PubMed  CAS  Google Scholar 

  88. Evans, E. A. and Parsegian, V. A. (1983),Ann. NY Acad. Sci. 416, 13.

    Article  PubMed  CAS  Google Scholar 

  89. Sung, K. L. P., Schmid-Schönbein, G. W., Skalak, R., Schuessler, G. B., Usani, S., and Chien, S. (1982),Biophys. J. 39, 101.

    PubMed  CAS  Google Scholar 

  90. Skalak, R., Chien, S., and Schmid-Schönbein, G. W. (1984),White Cell Mechanics: Basic Science and Clinical Aspects, Meiselman, H. J., Lichtman, M. A., and LaCelle, P. L., eds., Liss, New York, pp. 3–18.

    Google Scholar 

  91. Sato, H. and Suzuki, M. (1976),Fundamental Aspects of Metastasis, Weiss, L., ed., N. Holland, Amsterdam, pp. 311–317.

    Google Scholar 

  92. Weiss, L., Orr, F. W., and Honn, H. V. (1988),Clin. Exp. Metastasis, in press.

  93. Gabor, H. and Weiss, L. (1985),Invasion Metastasis 5, 71.

    PubMed  CAS  Google Scholar 

  94. Chien, S., Schmid-Schönbein, G. W., Sung, K. L. P., Schmalzer, E. A., and Skalak, R. (1984),White Cell Mechanics: Basic Science and Clinical Aspects, Meiselman, H. J., Lichtman, M. A., and LaCelle, P. L., eds., Liss, New York, pp. 19–51.

    Google Scholar 

  95. Evans, E. A., and Skalak, R. (1979),Crit. Rev. Bioeng. 304, 181.

    Google Scholar 

  96. Kwork, R. and Evans, E. (1981),Briophys. J. 35, 637.

    Google Scholar 

  97. Rosenberg, M. D. (1963),J. Cell Biol. 17, 289.

    Article  PubMed  CAS  Google Scholar 

  98. Weiss, L. (1968c),J. Theoret. Biol. 18, 9.

    Article  CAS  Google Scholar 

  99. Schmid-Schönbein, G. W., Shih, Y. Y., and Chien, S. (1980),Blood 56, 866.

    PubMed  Google Scholar 

  100. Weiss, L. (1988),Invasion Metastasis,8, 228.

    PubMed  CAS  Google Scholar 

  101. Klocke, F. J., Mates, R. E., Canty, J. M., and Ellis, A. K. (1985),Circ. Res.,56, 310.

    PubMed  CAS  Google Scholar 

  102. Baird, R. J., Goldbach, M. M., and del la Rocha, A. (1972),J. Thor. Cardiovasc. Surg. 64, 635.

    CAS  Google Scholar 

  103. Armour, J. A. and Randall, W. C. (1971),Amer. J. Physiol. 220, 1833.

    PubMed  CAS  Google Scholar 

  104. Weiss, L. (1985c),Principles of Metastasis, Academic, Orlando, FL, p. 162.

    Google Scholar 

  105. Weiss, L., Ward, P. M., Harlos, J. P., and Holmes, J. C. (1984),Int. J. Cancer 33, 825.

    Article  PubMed  CAS  Google Scholar 

  106. Weiss, L. (1988),Clin. Exp. Metastasis, in press.

  107. Weiss, L. and Gilbert, H. A., eds. (1982),Liver Metastasis, G. K. Hall, Boston, MA.

    Google Scholar 

  108. Weiss, L., Grundman, E., Torhorst, J., Harveit, F., Moberg, I., Eder, M., Fenoglio-Preiser, C. M., Napier, J., Horne, C. H. W., Lopez, M. J., Shaw-Dunn, R. I., Sugar, L. J., Davies, J. D., Day, D. W., and Harlos, J. P. (1986),J. Path. 150, 195.

    Article  PubMed  CAS  Google Scholar 

  109. Weiss, L. (1985),Principles of Metastasis, Academic, Orlando, FL, pp. 1–21.

    Google Scholar 

  110. Bross, I. D. J., Viadana, E., and Pickren, J. W. (1975),J. Chronic Dis. 28, 149.

    Article  PubMed  CAS  Google Scholar 

  111. Weiss, L. and Mayhew, E. (1985),Cancer Drug Delivery 2, 19.

    PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Experimental Pathology, Roswell Park Memorial Institute, 14263, Buffalo, NY

    Leonard Weiss

  2. Department of Applied Mechanics and Engineering Sciences, University of California, San Diego, 92093, La Jolla, CA

    Geert W. Schmid-Schönbein

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  1. Leonard Weiss
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Weiss, L., Schmid-Schönbein, G.W. Biomechanical interactions of cancer cells with the microvasculature during metastasis. Cell Biophysics 14, 187–215 (1989). https://doi.org/10.1007/BF02797133

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