Skip to main content
Log in

The role of tumor cell adhesion as an important factor in formation of distant colorectal metastasis

  • Current Status
  • Published:
Diseases of the Colon & Rectum

Abstract

PURPOSE: The interactions of blood-borne colorectal carcinoma cells with vascular endothelium are important during hematogenous formation of distant metastases. To adhere to the vessel wall, circulating carcinoma cells that come into contact with the microvasculature must resist the tractive forces of the flow of plasma and other circulating cells that tend to detach them from the wall. METHODS: Hydrodynamic adhesion assays have been introduced to mimic the microcirculation and investigate cell adhesion under flow conditions. Different aspects of colorectal cancer cell adhesion during hematogenous formation of distant metastases are summarized and discussed in this review. RESULTS: Adhesion of colorectal carcinoma cells to endothelial cells and extracellular matrix is influenced by the presence of fluid flow. Shear forces alone are able to induce signal transduction events in these cells that result in cell activation and modification of adhesive behavior. CONCLUSIONS: Consideration of fluid dynamics of circulating colorectal cancer cell movement in the microcirculation leads to new knowledge ofin vivo processes that are involved in tumor cell adhesion to the vessel wall in host organs. Shear forces have been found to influence adhesive properties of colorectal carcinoma cells to endothelial cells and underlying subendothelial extracellular matrix. Understanding the complex processes involved in tumor cell adhesion may result in the development of novel therapeutic strategies.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Haier J. Indication and strategy of surgical treatment in metastatic colorectal cancer. In: Buhr HJ, Runkel N, eds. Operation course: colorectal carcinomas [in German]. Leipzig: Ambrosius Barth Verlag, 1997: 138–45.

    Google Scholar 

  2. Hermanek P Jr, Wiebelt H, Riedl S, Staimmer D, Hermanek P. Long-term results of surgical therapy of colon cancer. Results of the Colorectal Cancer Study Group [in German]. Chirurg 1994;65:287–97.

    PubMed  Google Scholar 

  3. Parkin DM, Pisani P, Ferlay J. Global cancer statistics. CA Cancer J Clin 1999;49:33–64.

    PubMed  Google Scholar 

  4. Haier J, Nasralla M, Nicolson GL. Cell surface molecules and their prognostic values in assessing colorectal carcinomas. Ann Surg 2000;231:11–24.

    Article  PubMed  Google Scholar 

  5. Nicolson GL. Cancer metastasis: tumor cell and host organ properties important in metastasis to specific secondary sites. Biochim Biophys Acta 1988;948:175–224.

    PubMed  Google Scholar 

  6. Feldman M, Eisenbach L. What makes a tumor cell metastatic? Sci Am 1988;259: 40–7.

    Google Scholar 

  7. De Both NJ, Vermey M, Groen N, Dinjens WN, Bosman FT. Clonal growth of colorectal-carcinoma cell lines transplanted to nude mice. Int J Cancer 1997;72:1137–41.

    Article  PubMed  Google Scholar 

  8. Nicolson GL. Organ specificity of tumor metastasis: role of preferential adhesion, invasion and growth of malignant cells at specific secondary sites. Cancer Metastasis Rev 1988;7:143–88.

    Article  PubMed  Google Scholar 

  9. Ewing J. A treatise on tumors, neoplastic diseases. 3rd ed. Philadelphia: WB Saunders, 1928.

    Google Scholar 

  10. Paget S. The distribution of secondary growth in cancer of the breast. Lancet 1889;1:571–3.

    Article  Google Scholar 

  11. Weiss L. Metastatic inefficiency. Adv Cancer Res 1990;54:159–211.

    PubMed  Google Scholar 

  12. Weiss L. Biomechanical interactions of cancer cells with the microvasculature during hematogenous metastasis. Cancer Metastasis Rev 1992;11:227–35.

    Article  PubMed  Google Scholar 

  13. Lawrence MB, McIntire LV, Eskin SG. Effect of flow on polymorphonuclear leukocyte/endothelial cell adhesion. Blood 1987;70:1284–90.

    PubMed  Google Scholar 

  14. Takahashi M, Ishida T, Traub O, Corson MA, Berk BC. Mechanotransduction in endothelial cells: temporal signaling events in response to shear stress. J Vasc Res 1997;34:212–9.

    PubMed  Google Scholar 

  15. Belloni PN, Nicolson GL. The role of the vascular endothelium in cancer metastasis. In: Simionescu N, Simionescu M, eds. Endothelial cell dysfunctions. New York: Plenum Press, 1992:395–425.

    Google Scholar 

  16. Schnitzer JE, Siflinger-Birnboim A, Del Vecchio PJ, Malik AB. Segmental differentiation of permeability, protein glycosylation, and morphology of cultured bovine lung vascular endothelium. Biochem Biophys Res Commun 1994;199:11–9.

    Article  PubMed  Google Scholar 

  17. Carley WW, Milici AJ, Madri JA. Extracellular matrix specificity for the differentiation of capillary endothelial cells. Exp Cell Res 178;1988:426–34.

    Article  PubMed  Google Scholar 

  18. Menger MD, Vollmer B. Adhesion molecules as determinants of disease: from molecular biology to surgical research. Br J Surg 1996;83:588–601.

    PubMed  Google Scholar 

  19. Irimura T, Nakamori S, Matsushita Y,et al. Colorectal cancer metastasis determined by carbohydrate-mediated cell adhesion: role of sialyl-LeX antigens. Semin Cancer Biol 1993;4:319–24.

    PubMed  Google Scholar 

  20. Irimura T, Tressler RJ, Nicolson GL. Sialoglycoproteins of murine RAW117 large cell lymphoma/lymphosarcoma sublines of various metastatic colonization properties. Exp Cell Res 1986;165:403–16.

    Article  PubMed  Google Scholar 

  21. Yun Z, Smith TW, Menter DG, McIntire LV, Nicolson GL. Differential adhesion of metastatic RAW117 large-cell lymphoma under static conditions: role of theαvβ3 integrin. Clin Exp Metastasis 1997;15:3–11.

    Article  PubMed  Google Scholar 

  22. Giavazzi R, Foppolo M, Dossi R, Remuzzi A. Rolling and adhesion of human tumor cells on vascular endothelium under physiological flow conditions. J Clin Invest 1993;92:3038–44.

    PubMed  Google Scholar 

  23. Tözeren A, Kleinman HK, Grant DS, Morales D, Mercurio AM, Byers SW. E-selectin-mediated dynamic interactions of breast- and colon-cancer cells with endothelial-cell monolayers. Int J Cancer 1995;60:426–31.

    PubMed  Google Scholar 

  24. Hamada J, Cavanaugh PG, Lotan O, Nicolson GL. Separable growth and migration factors for large-cell lymphoma cells secreted by microvascular endothelial cells derived from target organs for metastasis. Br J Cancer 1992;66:349–54.

    PubMed  Google Scholar 

  25. Sawada H, Wakabayashi H, Nawa A, Mora E, Cavanaugh PG, Nicolson GL. Differential motility stimulation but not growth stimulation or adhesion of metastatic human colorectal carcinoma cells by target organ-derived liver sinusoidal endothelial cells. Clin Exp Metastasis 1996;14:308–14.

    PubMed  Google Scholar 

  26. Nicolson GL. Organ specificity of tumor metastasis: role of preferential adhesion, invasion and growth of malignant cells at specific secondary sites. Cancer Metastasis Rev 1988;7:143–88.

    Article  PubMed  Google Scholar 

  27. Nicolson GL. Metastatic tumor cell interactions with endothelium, basement membrane and tissue. Curr Opin Cell Biol 1989;1:1009–19.

    Article  PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  29. Haier J, Nasralla M, Nicolson GL. Different adhesion properties of highly and poorly metastatic HT-29 colon carcinoma cells with extracellular matrix components: role of integrin expression and cytoskeletal components. Br J Cancer 1999;80:1867–74.

    Article  PubMed  Google Scholar 

  30. Haier J, Nasralla M, Nicolson GL.β1-integrin mediated dynamic adhesion of colon carcinoma cells to extracellular matrix under laminar flow. Clin Exp Metastasis 1999;17:377–88.

    Article  PubMed  Google Scholar 

  31. Tözeren A, Kleinman HK, Wu S, Mercurio AM, Byers SW. Integrinα6β4 mediates dynamic interactions with laminin. J Cell Sci 1994;107:3153–63.

    PubMed  Google Scholar 

  32. Patton JT, Menter DG, Benson DM, Nicolson GL, McIntire LV. Computerized analysis of tumor cells flowing in a parallel plate chamber to determine their adhesion stabilization lag time. Cell Motil Cytoskeleton 1993;26:88–98.

    Article  PubMed  Google Scholar 

  33. Menter DG, Patton JT, Updyke TV,et al. Transglutaminase stabilizes melanoma adhesion under laminar flow. Cell Biophys 1992;18:123–43.

    Google Scholar 

  34. Menter DG, Fitzgerald L, Patton J, McIntire LV, Nicolson GL. Human melanoma integrins contribute to arrest and stabilization potential while flowing over extracellular matrix. Immunol Cell Biol 1995;73:575–83.

    PubMed  Google Scholar 

  35. Haier J, Nicolson GL. Tumor cell adhesion of human colon carcinoma cells with different metastatic properties to extracellular matrix under dynamic conditions of laminar flow. J Cancer Res Clin Oncol 2000;126:699–706.

    Article  PubMed  Google Scholar 

  36. Haier J, Nicolson GL. Time-dependent dephosphorylation through Serine/Threonine phosphatases is required for stable adhesion of highly and poorly metastatic HT-29 colon carcinoma cell lines to collagen. Anticancer Res 2000;20:2265–71.

    PubMed  Google Scholar 

  37. Cartwright CA, Meisler AI, Echhart W. Activation of the pp60c-src protein kinase is an early event in colonic carcinogenesis. Proc Natl Acad Sci USA 1990;87:558–62.

    PubMed  Google Scholar 

  38. Han NM, Curley SA, Gallick GE. Differential activation of pp60c-src and pp62c-yes in human colorectal carcinoma liver metastases. Clin Cancer Res 1996;2:1397–1404.

    PubMed  Google Scholar 

  39. Li S, Kim M, Hu YI,et al. Fluid shear stress activation of focal adhesion kinase. Linking to mitogen-activated protein kinase. J Biol Chem 1997;272:30455–62.

    Article  PubMed  Google Scholar 

  40. Yano Y, Geibel J, Sumpio BE. Tyrosine phosphorylation of pp125FAK and paxillin in aortic endothelial cells induced by mechanical strain. Am J Physiol 1996;271:C635–49.

    PubMed  Google Scholar 

  41. Takahashi M, Berk BC. Mitogen-activated protein kinase (ERK1/2) activation by shear stress and adhesion in endothelial cells. Essential role for a herbimycin-sensitive kinase. J Clin Invest 1996;98:2623–31.

    PubMed  Google Scholar 

  42. Resnick N, Yahav H, Khachigian LM,et al. Endothelial gene regulation by laminar shear stress. Adv Exp Med Biol 1997;430:155–64.

    PubMed  Google Scholar 

  43. Banes AJ, Tsuzaki M, Yamamoto J,et al. Mechanoreception at the cellular level: the detection, interpretation, and diversity of responses to mechanical signals. Biochem Cell Biol 1995;73:349–65.

    PubMed  Google Scholar 

  44. Felsenfeld DP, Schwartzberg PL, Venegas A, Tse R, Sheetz MP. Selective regulation of integrin-cytoskeleton interactions by the tyrosine kinase Src. Nat Cell Biol 1999;1:200–6.

    Article  PubMed  Google Scholar 

  45. Haier J, Nicolson GL. Role of the cytoskeleton in adhesion stabilization of human colorectal carcinoma cells to extracellular matrix components under dynamic conditions of laminar flow. Clin Exp Metastasis 1999;17:713–21.

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

About this article

Cite this article

Haier, J., Nicolson, G.L. The role of tumor cell adhesion as an important factor in formation of distant colorectal metastasis. Dis Colon Rectum 44, 876–884 (2001). https://doi.org/10.1007/BF02234713

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02234713

Key words

Navigation