Skip to main content
SpringerLink
Log in

Organ Specificity of Metastasis: Adhesive, Invasive and Growth Properties of Organ-Specific Metastatic Cells

  • Chapter
New Concepts in Cancer

  • 11 Accesses

Abstract

Tumor metastases form by way of a complex series of sequential steps involving the growth and invasion of malignant cells at primary sites, their penetration into lymphatics, blood circulation and body cavities, transport to distant sites, implantation at these sites, and invasion and growth. Often metastasis can occur to selective secondary sites that would be unexpected on the basis of mechanical considerations or circulatory or lymphatic patterns (Table 3.1) (Sugarbaker, 1981; Nicolson, 1982a, 1988a, b).

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

Access this chapter

Log in via an institution

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Ahlering, T.E., Dubeau, L. and Jones, P.A. (1987). A new in vivo model to study invasion and metastasis of human bladder carcinoma. Cancer Res., 47, 6660–5.

    CAS  PubMed  Google Scholar 

  • Alsslen, L.A., Hove, L.M. and Hartviet, F. (1987). Metastatic distribution in malignant melanoma. A 30 year autopsy study. Invasion Metastasis, 7, 253–63.

    Google Scholar 

  • Atnip, K.D., Carter, L.M., Nicolson, G.L. and Dabbous, M.K. (1987). Chemotactic response of rat mammary adenocarcinoma cell clones to tumor-derived cytokines. Biophys. Biochem. Res. Comm., 146, 996–1002.

    Article  CAS  Google Scholar 

  • Auerbach, R., Lu, W. C, Pardon, E., Gumkowski, F., Kaminska, G. and Kaminska, M. (1987). Specificity of adhesion between murine tumor cells and capillary endothelium: An in vitro correlate of preferential metastasis in vivo. Cancer Res., 47, 1492–6.

    CAS  PubMed  Google Scholar 

  • Belloni, P.N. and Nicolson, G.L. (1988). Differential expression of cell surface glycoproteins on organ-derived murine endothelia and endothelial cells. J. Cell. Physiol, 136, 398–410.

    Article  CAS  PubMed  Google Scholar 

  • Bresalier, R.S., Hujanen, E.S., Raper, S.E., Roll, F.J., Itzkowitz, S.H., Martin, G.R. and Kim, Y.S. (1987). An animal model for colon cancer metastasis: establishment and characterization of murine cell lines with enhanced liver-metastasizing ability. Cancer Res., 47, 1398–406.

    CAS  PubMed  Google Scholar 

  • Brunson, K.W. and Nicolson, G.L. (1979). Selection of malignant melanoma variant cell lines for ovary colonization. J. Supramol. Struct., 11, 517–28.

    Article  CAS  PubMed  Google Scholar 

  • Brunson, K.W., Beattie, G. and Nicolson, G.L. (1978). Selection and altered tumor cell properties of brain-colonising metastatic melanoma. Nature (Lond.), 272, 543–5.

    Article  CAS  Google Scholar 

  • Cavanaugh, P.P.G. and Nicolson, G.L. (1989). Purification and some properties of a lung-derived growth factor (LDGF-1) that differentially stimulates the growth of tumor cells metastatic to the lung. Cancer Res., 49, 3928–33.

    CAS  PubMed  Google Scholar 

  • Fidler, I.J. (1973). Selection of successive tumor lines for metastasis. Nature New Biol. (Lond.), 242, 148–9.

    Article  CAS  Google Scholar 

  • Fidler, I.J. (1986). Rationale and methods for the use of nude mice to study the biology and therapy of human cancer metastasis. Cancer Metastasis Rev., 5, 29–49.

    Article  CAS  PubMed  Google Scholar 

  • Fidler, I.J. and Nicolson, G.L. (1976). Organ selectivity for implantation survival and growth of B16 melanoma variant tumor lines. J. Natl Cancer Inst., 57, 199–1202.

    Google Scholar 

  • Foidart, J.M., Bere, E.W., Yaar, M., Rennard, S.I., Gullino, M., Martin, G.R. and Katz, S.I. (1980). Distribution and immunoelectron microscopic localization of laminin. A noncollagenous basement membrane glycoprotein. Lab. Invest., 42, 336–42.

    CAS  PubMed  Google Scholar 

  • Gallatin, M., St John, T.P., Siegelman, M., Reichert, R., Butcher, E.C. and Weissman, I.L. (1986). Lymphocyte homing receptors. Cell, 44, 673–80.

    Article  CAS  PubMed  Google Scholar 

  • Graff, J., Iwamoto, Y., Sasaki, M., Martin, G.M., Kleinman, H.K., Robey, F.A. and Yamada, Y. (1987). Identification of an amino acid sequence in laminin mediating cell attachment, chemotaxis, and receptor binding. Cell, 48, 989–96.

    Article  Google Scholar 

  • Hart, I.R. (1981). Mechanisms of tumor cell invasion. Cancer Biol. Rev., 2,29–58.

    Google Scholar 

  • Hart, I.R. (1982). Seed and soil revisited. Mechanisms of site specific metastasis. Cancer Metastasis Rev., 1, 5–16.

    Article  CAS  PubMed  Google Scholar 

  • Hart, I.R. and Fidler, I.J. (1980). The role of organ selectivity in the determination of metastatic patterns of B16 melanoma. Cancer Res., 40, 2281–7.

    CAS  PubMed  Google Scholar 

  • Horak, E., Darling, D.L. and Tarin, D. (1986). Analysis of organ-specific effects on metastatic tumor formation by studies in vitro. J. Natl Cancer Inst., 75, 913–22.

    Google Scholar 

  • Hujanen, E.S. and Terranova, V.P. (1985). Migration of tumor cells to organ-derived chemoattractants. Cancer Res., 45, 3517–21.

    CAS  PubMed  Google Scholar 

  • Humphreys, M.J., Olden, K. and Yamada, K.M. (1986). A synthetic peptide from fibronectin inhibits experimental metastasis of melanoma cells. Science, 233, 467–9.

    Article  Google Scholar 

  • Iwamoto, Y., Robey, F.A., Graf, J., Sasaki, M., Kleinman, H.K., Yamada, Y. and Martin, G.R. (1987). YIGSR, a synthetic laminin pentapeptide, inhibits experimental metastasis formation. Science, 238, 1132–4.

    Article  CAS  PubMed  Google Scholar 

  • Kahan, B. (1987). Experimental metastasis of mouse embryonal carcinoma cell lines to specific locations. Cancer Res., 47, 6315–23.

    CAS  PubMed  Google Scholar 

  • Kamenov, B. and Longenecker, B.M. (1985). Further evidence for the existence of homing receptors on murine leukemia cells which mediate adherence to normal bone marrow stromal cells. Leukemia Res., 9, 1529–37.

    Article  CAS  Google Scholar 

  • Kawaguchi, T., Kawaguchi, M., Miner, K.M., Lembo, T.M. and Nicolson, G.L. (1983). Brain meninges tumor formation by in vivo-selected metastatic B16 melanoma variants in mice. Clin. Exp. Metastasis, 3, 247–59.

    Article  Google Scholar 

  • Kiernan, M.W. and Longenecker, B.M. (1983). Organ specific metastasis with special reference to avian systems. Cancer Metastasis Rev., 2,165–82.

    Article  Google Scholar 

  • Kleinman, H.K., McGarvey, M.L., Hassell, J.R., Star, V.L., Cannon, F.B., Laurie, G.W. and Martin, G.R. (1986). Biochemistry, 25, 312–18.

    Google Scholar 

  • Korach, S., Poupon, M.-F., Du Villard, J.-A. and Becker, M. (1986). Differential adhesiveness of rhabdomyosarcoma-derived cloned metastatic cell lines to vascular endothelial monolayers. Cancer Res., 46, 3624–9.

    CAS  PubMed  Google Scholar 

  • Kramer, R.H., Gonzalez, R. and Nicolson, G.L. (1980). Metastatic tumor cells adhere preferentially to the extracellular matrix underlying vascular endothelial cells. Int. J. Cancer, 26, 639–45.

    Article  CAS  PubMed  Google Scholar 

  • Kraus, M.H., Popescu, N. C, Amsbaugh, S.C. and King, C.R. (1987). Over-expression of the EGF receptor-related proto-oncogene erb-2 in human mammary tumor cell lines by different molecular mechanisms. EMBO J., 6, 605–10.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lacovara, J., Cramer, E.B. and Quigley, J.P. (1984). Fibronectin enhancement of directed migration of B16 melanoma cells. Cancer Res., 44, 1657–63.

    CAS  PubMed  Google Scholar 

  • Lapis, K., Paku, S. and Liotta, L.A. (1988). Endothelization of embolized tumor cells during metastasis formation. Clin. Exp. Metastasis, 6, 73–89.

    Article  CAS  PubMed  Google Scholar 

  • Lichtner, R., Belloni, P. and Nicolson, G.L. (1989). Differential adhesion of metastatic rat mammary carcinoma cells to organ-derived microvessel endothe-lial cells and subendothelial matrix. Exp. Cell Biol., 57,146–52.

    CAS  PubMed  Google Scholar 

  • Liotta, L.A., Mandler, R., Murano, G., Katz, D.A., Gordon, R.K., Chang, P.K. and Sciffman, E. (1986). Tumor autocrine motility factor. Proc. NatlAcad. Sci. USA, 83, 3302–6.

    Article  CAS  Google Scholar 

  • Mareel, M.M.K. (1983). Invasion in vitro: Methods of analysis. Cancer Metastasis Rev, 2, 201–18.

    Article  CAS  PubMed  Google Scholar 

  • McGuire, E.J., Mascali, J.J., Grady, S.R. and Nicolson, G.L. (1984). Involvement of cell-cell adhesion molecules in liver colonization by metastatic murine lymphoma/lymphosarcoma variants. Clin. Exp. Metastasis, 2, 213–22.

    Article  CAS  PubMed  Google Scholar 

  • Mentzer, T., Burrakoff, S. and Faller, D. (1986). Adhesion of T-lymphocytes to human endothelial cells is regulated by the LFA-1 membrane molecule. J. Cell. Physiol., 126, 283–90.

    Article  Google Scholar 

  • Meromsky, L., Lotan, R. and Raz, A. (1986). Implications of endogenous tumor cell surface lectins as mediators of cellular interactions and lung colonization. Cancer Res., 46, 5270–5.

    CAS  PubMed  Google Scholar 

  • Middlekoop, O.P., van Bavel, P., Calafat, J. and Roos, E. (1985). Hepatocyte surface molecule involved in the adhesion of TA3 mammary carcinoma cells to rat hepatocyte cultures. Cancer Res., 45, 3825–35.

    Google Scholar 

  • Middlekoop, O.P., Roos, E. and Van de Pavert, I.V. (1982). Infiltration of lymphosarcoma cells into hepatocyte cultures: inhibition of univalent antibodies against liver plasma membranes and lymphosarcoma cells. J. Cell Sci., 56, 461–70.

    Google Scholar 

  • Miner, K.M., Kawaguchi, T., Uba, G.W. and Nicolson, G.L. (1982). Clonal drift of cell surface, melanogenic and experimental metastatic properties of in vivo-selected, brain meninges-colonizing murine B16 melanoma. Cancer Res., 42, 4631–8.

    CAS  PubMed  Google Scholar 

  • Naito, S., Giavazzi, R. and Fidler, I.J. (1987). Correlation between the in vitro interactions of tumor cells with an organ environment and metastatic in vivo. Invasion Metastasis, 7,126–9.

    Google Scholar 

  • Neri, A., Welch, D., Kawaguchi, T. and Nicolson, G.L. (1982). Development and biologic properties of malignant cell sublines and clones of a spontaneously metastatizing rat mammary adenocarcinoma. J. Natl Cancer Inst., 68, 507–17.

    CAS  PubMed  Google Scholar 

  • Nicolson, G.L. (1982a). Cancer metastasis: organ colonization and the cell surface properties of malignant cells. Biochim. Biophys. Acta, 695,113–76.

    CAS  PubMed  Google Scholar 

  • Nicolson, G.L. (1982b). Metastatic tumor cell attachment and invasion assay utilizing vascular endothelial cell monolayers. J. Histochem. Cytochem., 30, 214–20.

    Article  CAS  PubMed  Google Scholar 

  • Nicolson, G.L. (1987). Differential growth properties of metastatic large cell lymphoma cells in target organ-conditioned medium. Exp. Cell Res., 168,572–7.

    Article  CAS  PubMed  Google Scholar 

  • Nicolson, G.L. (1988a). Organ specificity of tumor metastasis: role of preferential adhesion invasion and growth of unique malignant cells at specific organ sites. Cancer Metastasis Rev., 7,143–88.

    Article  CAS  PubMed  Google Scholar 

  • Nicolson, G.L. (1988b). Cancer metastasis: tumor cell and host organ properties important in colonization of specific secondary sites. Biochim. Biophys. Acta, 948,175–224.

    CAS  PubMed  Google Scholar 

  • Nicolson, G.L. (1989). Differential organ tissue adhesion, invasion and growth properties of metastatic rat mammary adenocarcinoma cells. Breast Cancer Res. Treat, 12, 167–76.

    Article  Google Scholar 

  • Nicolson, G.L. and Dulski, K.M. (1986). Organ specificity of metastatic tumor colonization is related to organ-selective growth properties of malignant cells. Int. J. Cancer, 38, 289–94.

    Article  CAS  PubMed  Google Scholar 

  • Nicolson, G.L., Belloni, P.N., Tressler, R.J., Inoue, T. and Cavanaugh, P. (1989). Adhesive, invasive, and growth properties of selected metastatic variants of a murine large cell lymphoma. Invasion Metastasis, 9, 102–16.

    CAS  PubMed  Google Scholar 

  • Nicolson, G.L., Dulski, K., Basson, C. and Welch, D.R. (1985). Preferential organ attachment and invasion in vitro by B16 melanoma cells selected for differing metastatic colonization and invasive properties. Invasion Metastasis, 5, 1144–58.

    Google Scholar 

  • Nicolson, G.L., Irimura, T., Gonzalez, R. and Rouslahti, E. (1981). The role of fibronectin in adhesion of metastatic melanoma cells to endothelial cells and their basal lamina. Exp. Cell Res., 135, 461–5.

    Article  CAS  PubMed  Google Scholar 

  • Nicolson, G.L. and Poste, G. (1983). Tumor implantation and invasion at metastatic sites. Int. Rev. Exp. Pathol., 25, 77–181.

    CAS  PubMed  Google Scholar 

  • Orr, F.W., Varani, J., Delkatny, J., Jain, N. and Ward, P.A. (1981). Comparison of the chemotactic response of tumor cells: a model for cancer metastasis. Am. J. Pathol., 102, 160–7.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Paget, S. (1889). The distribution of secondary growths in cancer of the breast. Lancet, 1, 571–3.

    Article  Google Scholar 

  • Pauli, B.U., Schwartz, D.E., Thomas, E.J.M. and Kuettner, K.E. (1983). Tumor invasion and host extracellular matrix. Cancer Metastasis Rev., 2,129–52.

    Article  CAS  PubMed  Google Scholar 

  • Pierschbacher, M.D. and Ruoslahti, E. (1984). Cell attachment activity of fibronectin can be duplicated by small synthetic fragments of the molecule. Nature (Lond.), 309, 30–3.

    Article  CAS  Google Scholar 

  • Roos, E. and Roossien, F.F. (1987). Involvement of leukocyte function-associated-1 (LFA-1) in the invasion of hepatocyte cultures by lymphoma and T-cell hybridoma cells. J. Cell Biol., 105, 553–9.

    Article  CAS  PubMed  Google Scholar 

  • Roos, E., Collard, J.G., Roossien, F.F. and Riviere, G.L. (1988). Interactions between tumor cells and liver cells during liver metastasis. In Nicolson, G.L. and Fidler, I.J. (eds.), Tumor Progression and Metastasis, Alan R. Liss, New York, 271–8.

    Google Scholar 

  • Schirrmacher, V. (1985). Cancer metastasis: Experimental approaches, theoretical concepts and treatment strategies. Adv. Cancer Res., 43, 1–73.

    Article  CAS  PubMed  Google Scholar 

  • Shearman, P.J., Gallatin, W.M. and Longenecker, B.M. (1980). Detection of a cell-surface antigen correlated with organ-specific metastasis. Nature (Lond.), 286, 267–9.

    Article  CAS  Google Scholar 

  • Sindelar, W.F., Tralka, T.S. and Ketcham, A.S. (1975). Electron microscopic observations on formation of pulmonary metastases. J. Surg. Res., 18, 137–67.

    Article  CAS  PubMed  Google Scholar 

  • Slamon, D.J., Clark, G.M., Wong, S.G., Levin, W.J., Ullrich, A. and McGuire, W.L. (1987). Breast cancer: correlation of relapse and survival with amplification of the HER-2/neu oncogene. Science, 235, 177–82.

    Article  CAS  PubMed  Google Scholar 

  • Sugarbaker, E.V. (1981). Patterns of metastasis in human malignancies. Cancer Biol. Rev., 2, 235–78.

    Google Scholar 

  • Sugarbaker, E.V., Cohen, A.M. and Ketcham, A.S. (1971). Do metastases metastasize? Ann. Surg., 174, 161–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Szaniawska, B., Majewski, S., Maninski, M.J., Noremberg, K., Swierz, M. and Janik, P. (1985). Stimulatory and inhibitory activities of lung-conditioned medium on the growth of normal and neoplastic cells in vitro. J. Natl Cancer Inst., 75, 303–6.

    CAS  PubMed  Google Scholar 

  • Tao, T.-W., Matter, A., Vogel, K. and Burger, M.M. (1979). Int. J. Cancer, 23, 854–7.

    Google Scholar 

  • Tsuruo, T., Kawabata, H., Iida, H. and Yamori, T. (1986). Tumor-induced platelet aggregation and growth promoting factors as determinants for successful tumor metastasis. Clin. Exp. Metastasis, 4, 25–33.

    Article  CAS  PubMed  Google Scholar 

  • Varani, J. (1982). Chemotaxis of metastatic tumor cells. Cancer Metastasis Rev., 1, 17–8.

    Article  CAS  PubMed  Google Scholar 

  • Venter, D.J., Kumar, S., Tuzi, N.L. and Gullick, W.J. (1987). Overexpression of the c-erb-2 oncoprotein in human breast carcinomas immunohistological assessment correlates with gene amplification. Lancet, 1, 69–71.

    Article  Google Scholar 

  • Vollmers, H.P.and Birchmeier, W. (1983). Monoclonal antibodies inhibit the adhesion of mouse B16 melanoma cells in vitro and block lung metastasis in vivo. Proc. NatlAcad. Sci. USA, 80, 3729–33.

    Article  CAS  Google Scholar 

  • Vollmers, H.P., Imhof, B.A., Braun, S., Waller, C.A., Schirrmacher, V. and Birchmeier, W. (1984). Monoclonal antibodies which prevent experimental lung metastases. Interference with the adhesion of tumor cells to laminin. FEBS Lett., 172,17–20.

    Article  CAS  PubMed  Google Scholar 

  • Wewer, U.M., Taraboletti, G., Sobel, M.E., Albrechtsen, R. and Liotta, L.A. (1987). Role of laminin receptor in tumor cell migration. Cancer Res., 47, 5691–8.

    CAS  PubMed  Google Scholar 

  • Yamori, T., Iida, H., Tsukagoshi, S. and Tsuruo, T. (1988). Growth stimulating activity of lung extract on lung-colonizing colon 26 clones and its partial characterization. Clin. Exp. Metastasis, 6,131–9.

    Article  CAS  PubMed  Google Scholar 

  • Zeidman, I. and Buss, J.M. (1952). Transpulmonary passage of tumor cell emboli. Cancer Res., 12, 731–3.

    CAS  PubMed  Google Scholar 

Download references

Authors
  1. Garth L. Nicolson
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Pierre Fabre Médicament, Castres, France

    C. Etievant

  2. CNRS, Toulouse, France

    J. Cros

  3. Roswell Park Memorial Hospital, Buffalo, NY, USA

    Y. M. Rustum

Copyright information

© 1990 Macmillan Publishers Limited

About this chapter

Cite this chapter

Nicolson, G.L. (1990). Organ Specificity of Metastasis: Adhesive, Invasive and Growth Properties of Organ-Specific Metastatic Cells. In: Etievant, C., Cros, J., Rustum, Y.M. (eds) New Concepts in Cancer. Palgrave, London. https://doi.org/10.1007/978-1-349-10671-4_3

Download citation

  • DOI: https://doi.org/10.1007/978-1-349-10671-4_3

  • Publisher Name: Palgrave, London

  • Print ISBN: 978-1-349-10673-8

  • Online ISBN: 978-1-349-10671-4

  • eBook Packages: EngineeringEngineering (R0)

Publish with us

Policies and ethics

Search

Navigation