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Thein vitro invasiveness and interactions with laminin of K-1735 melanoma cells. Evidence for different laminin-binding affinities in high and low metastatic variants

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Abstract

The invasive and metastatic characteristics of cloned cells derived from the K-1735 murine melanoma were investigated. Cell lines which are highly metastatic in mice were found to be invasivein vitro, and to show an enhanced attachment to, spreading on and migration toward laminin. As attachment, spreading and directional migration are thought to be receptor-mediated events, the binding of laminin to these cells was studied. Biotinylated laminin was used to evaluate receptor binding by fluorescence activated cell sorting (FACS) and this method was compared with that in which the binding of radioactive laminin is measured. Both studies revealed that metastatic K-1735 cells (a) have more receptors for laminin compared with non-metastatic cells and (b) exhibit a second population of low-affinity binding sites not present on the non-metastatic cells. The differences in receptor number and type may account for the greater interaction of metastatic cells with laminin and their invasive phenotype.

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References

  1. Albini, A., Iwamoto, Y., Kleinman, H. K., Martin, G. R., Aaronson, S. A., Kozlowsky, J. M., andMcEwan, R. N., 1987, A rapidin vitro assay for quantitating the invasive potential of tumor cells.Cancer Research,47, 3239–3245.

    Google Scholar 

  2. Aumailley, M., Nurcombe, V., Edgar, D., Paulsson, M., andTimpl, R., 1987, The cellular interaction of laminin fragments. Cell adhesion correlates with two fragmentspecific high affinity binding sites.Journal of Biological Chemistry,262, 11532–11538.

    Google Scholar 

  3. Cheresh, D. A., Pierschbacher, M. D., Herzig, M. A., andMujoo, K., 1986, Disialogangliosides GD2 and GD3 are involved in the attachment of human melanoma and neuroblastoma cells to extracellular matrix proteins.Journal of Cell Biology,102, 688–696.

    Google Scholar 

  4. Codogna, P., Doyennette-Moyne, M. A., andAubery, M., 1987, Evidence for a dual mechanism of chick embryo fibroblast adhesion on fibronectin and laminin substrate.Experimental Cell Research,169, 478–489.

    Google Scholar 

  5. Del Rosso, M., Cappelletti, R., Viti, M., Vannucchi, S., andChiarugi, V., 1981, Binding of the basement membrane glycoprotein laminin to glycosaminoglycans.Biochemical Journal,199, 699–704.

    Google Scholar 

  6. Fidler, I. J., Gruys, E., Cifone, M. A., Barnes, Z., andBucana, C., 1981, Demonstration of multiple phenotypic diversity in a murine melanoma of recent origin.Journal of the National Cancer Institute,67, 947–956.

    Google Scholar 

  7. Fidler, I. J., andBalch, C. M., 1978, Tumor heterogeneity and the biology of cancer invasion and metastasis.Cancer Research,38, 2651–2660.

    Google Scholar 

  8. Goodman, S. L., Deutzmann, R., andVon der Mark, K., 1987, Two distinct cell-binding domains in laminin can independently promote non-neuronal cell adhesion and spreading.Journal of Cell Biology,105, 589–598.

    Google Scholar 

  9. Hujanen, E. S., andTerranova, V. P., 1985, Migration of tumor cells to organ-derived chemoattractants.Cancer Research,45, 3517–3521.

    Google Scholar 

  10. Jones, P. A., andDeclerck, Y. A., 1980, Destruction of extracellular matrices containing glycoproteins, elastin and collagen by metastatic human tumor cells.Cancer Research,40, 3222–3227.

    Google Scholar 

  11. Kennedy, D. W., Rohrbach, D. H., Martin, G. R., Momoi, T., andYamada, K. M., 1983, The adhesive glycoprotein laminin is an agglutinin.Journal of Cellular Physiology,114, 257–262.

    Google Scholar 

  12. Kleinman, H. K., McGarvey, M. L., Liotta, L. A., Gehron Robey, P., andMartin, G. R., 1982, Isolation and characterization of native type IV collagen from the EHS sarcoma.Biochemistry,21, 6188–6193.

    Google Scholar 

  13. Kleinman, H. K., McGarvey, M. L., Hassel, J. R., Star, V. L., Cannon, F., Laurie, G. W., andMartin, G. R., 1986, Basement membrane complexes with biological activity.Biochemistry,25, 312–318.

    Google Scholar 

  14. Kleinman, H. K., Luckenbill-Edds, L., Cannon, F., andSephel, G., 1987, Use of extracellular matrix components for cell culture.Analytical Biochemistry,166, 1–13.

    Google Scholar 

  15. Kleinman, H. K., Ogle, R. C., Cannon, F. B., Little, C. D., Sweenly, T. M., andLuckenbill-Edds, L., 1988, Laminin receptors for neurite formation.Proceedings of the National Academy of Science of the U.S.A.,85, 1282–1286.

    Google Scholar 

  16. Kramer, R. H., Bensch, K. K., andWong, J., 1986, Invasion of reconstituted basement membrane matrix by metastatic tumor cells.Cancer Research,46, 1980–1989.

    Google Scholar 

  17. Kripke, M. L., 1979, Speculations on the role of ultraviolet radiation in the development of malignant melanoma.Journal of the National Cancer Institute,63, 541–548.

    Google Scholar 

  18. Lacovara, J., Cramer, E. B., andQuingley, J. B., 1984, Fibronectin enhancement of directed migration of B16 melanona cells.Cancer Research,44, 1657–1663.

    Google Scholar 

  19. Lesot, H., Kuhn, K., andVon der Mark, K., 1985, Isolation of a laminin binding protein from muscle cell membrane.EMBO Journal,2, 861–865.

    Google Scholar 

  20. Levine, E., Birk, D. E., andRaska, K., 1984, Attachment and degradation of collagen substrata by adenovirus-transformed cells of varying tumorigenicity.Collagen and Related Research,4, 49–62.

    Google Scholar 

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

    Google Scholar 

  22. Liotta, L., 1984, Tumor invasion and metastases: role of the basement membrane.American Journal of Pathology,117, 339–348.

    Google Scholar 

  23. Liotta, L. A., 1986, Tumor invasion and metastases. Role of the extracellular matrix. Rhoads Memorial Award Lecture.Cancer Research,46, 1–7.

    Google Scholar 

  24. Liotta, L. A., Mandler, R., Murano, G., Katz, D. A., Gordon, R. K., Chiang, P. K., andSchiffman, E., 1986, Tumor cell autocrine motility factor.Proceedings of the National Academy of Sciences of the U.S.A.,83, 3302–3306.

    Google Scholar 

  25. Lowry, O., Rosebrough, N., Farr, A., andRandall, R., 1951, Protein measurement with the folin phenol reagent.Journal of Biological Chemistry,193, 265–275.

    Google Scholar 

  26. Malinoff, H. K., andWicha, M. S., 1983, Isolation of a cell surface receptor protein from murine fibrosarcoma cells.Journal of Cell Biology,96, 1475–1479.

    Google Scholar 

  27. McCarthy, J. B., Palm, S. L., andFurcht, L. T., 1983, Migration by haptotaxis of a Schwann cell tumor line to the basement membrane glycoprotein laminin.Journal of Cell Biology,97, 772–779.

    Google Scholar 

  28. 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 Reviews,4, 125–152.

    Google Scholar 

  29. Mensing, H., Albini, A., Krieg, T., Pontz, B. F., andMüller, P. K., 1984, Enhanced chemotaxis of tumor-derived and virus-transformed cells to fibronectin and fibroblast-conditioned medium.International Journal of Cancer,33, 43–48.

    Google Scholar 

  30. Netland, P. A., andZetter, B. R., 1986, Melanoma cell adhesion to defined extracellular matrix components.Biochemical and Biophysical Research Communications,139, 515–522.

    Google Scholar 

  31. Nicolson, G. L., Irimura, T., Gonzales, R., andRuoslahti, E., 1981, The role of fibronectin in adhesion of metastatic melanoma cells to endothelial cells and their basal lamina.Experimental Cell Research,135, 461–465.

    Google Scholar 

  32. Nicolson, G. L., 1982, Cancer metastasis: organ colonization and the cell surface properties of malignant cells.Biochimica et Biophysica Acta,695, 113–176.

    Google Scholar 

  33. Rao, C. N., Barsky, S. H., Terranova, V. P., andLiotta, L. A., 1983, Isolation of a tumor cell laminin receptor.Biochemical and Biophysical Research Communications,111, 804–808.

    Google Scholar 

  34. Reich, R., Thompson, E., Iwamoto, Y., Martin, G. R., Deason, J. R., Fuller, G. C., andMiskin, R., 1988, Inhibition of plasminogen activator, serine proteases and collagenase IV prevents the invasion of basement membrane by metastatic cells.Cancer Research,48, 3307–3312.

    Google Scholar 

  35. Roberts, D. D., Rao, C. N., Magnani, J. L., Spitalnik, S. L., Liotta, L. A., andGinnsburg, V., 1985, Laminin binds specifically to sulphated glycolipids.Proceedings of the National Academy of Sciences of the U.S.A.,82, 1306–1310.

    Google Scholar 

  36. Ruoslahti, E., Hayman, E. G., Pierschbacher, M., andEngvall, E., 1982, Fibronectin: purification, immunochemical properties and biological activities. In L. W. Cunningham and P. W. Frederiksen, Eds.,Methods in Enzymology (Academic Press, New York, London, Paris), Volume 82, pp. 803–831.

    Google Scholar 

  37. Scatchard, G., 1949, The attractions of proteins for small molecules and ions.Annals of the New York Academy of Sciences,51, 660–672.

    Google Scholar 

  38. Talmadge, J. E., andFidler, I. J., 1982, Enhanced metastatic potential of tumor cells harvested from spontaneous metastases of heterogenous murine tumors.Journal of the National Cancer Institute,69, 975–980.

    Google Scholar 

  39. Terranova, V. P., Liotta, L. A., Russo, R. G., andMartin, G., 1982, Role of laminin in the attachment and metastasis of murine tumor cells.Cancer Research,42, 2265–2269.

    Google Scholar 

  40. Terranova, V. P., Rao, C. N., Kalebic, T., Margulies, T. M., andLiotta, L. A., 1983, Laminin receptors on human breast carcinoma cells.Proceedings of the National Academy of Sciences of the U.S.A.,80, 444–448.

    Google Scholar 

  41. Terranova, V. P., Hujanen, E. S., andMartin, G. M., 1986, Basement membranes and the invasive activity of metastatic tumor cells.Journal of the National Cancer Institute,77, 311–316.

    Google Scholar 

  42. Timpl, R., Rohde, H., Robey, P. G., Rennard, S. I., Foidart, J. M., andMartin, G. R., 1979, Laminin—a glycoprotein from basement membrane.Journal of Biological Chemistry,254, 9933–9937.

    Google Scholar 

  43. Timpl, R., 1982, Antibodies to collagens and procollagens.Methodsin Enzymology,82, 472–498.

    Google Scholar 

  44. Turpeeniniemi-Hujanen, T., Thorgeirsson, U. P., Rao, C. N., andLiotta, L. A., 1986, Laminin increases the release of type IV collagenase from malignant cells.Journal of Biological Chemistry,261, 1883–1889.

    Google Scholar 

  45. Varani, J., andWard, P. A., 1982, Tumor cell chemotaxis.The Biological Basis of Metastasis, edited by I. Hart and L. A. Liotta, (The Hague: Martinus Nijhoff), pp. 99–112.

    Google Scholar 

  46. Vlodavsky, I., andGospodarowicz, D., 1981, Respective roles of laminin and fibronectin in adhesion of human carcinoma and sarcoma cells.Nature (London),289, 304–306.

    Google Scholar 

  47. Volk, T., Geiger, B., andRaz, A., 1984, Motility and adhesive properties of high- and low-metastatic murine neoplastic cells.Cancer Research,44, 811–824.

    Google Scholar 

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Author notes

  1. Adriana Albini & Douglas M. Noonan

    Present address: National Institute for Research on Cancer, 16132, Genova, Italy

  2. Sharon Lea Aukerman

    Present address: Cetus Corporation, 94608, Emeryville, CA, USA

  3. Roy C. Ogle

    Present address: University of South Carolina, 29425, Charleston, SC, USA

Authors and Affiliations

  1. Laboratory for Developmental Biology and Anomalies, NIDR, NIH, 20892, Bethesda, MD, USA

    Adriana Albini, Roy C. Ogle, Douglas M. Noonan, Rafael Fridman & George R. Martin

  2. Department of Cell Biology, M.D. Anderson Hospital and Tumor Institute, 77030, Houston, TX, USA

    Sharon Lea Aukerman & Isaiah J. Fidler

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  1. Adriana Albini
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Albini, A., Aukerman, S.L., Ogle, R.C. et al. Thein vitro invasiveness and interactions with laminin of K-1735 melanoma cells. Evidence for different laminin-binding affinities in high and low metastatic variants. Clin Exp Metast 7, 437–451 (1989). https://doi.org/10.1007/BF01753664

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  • DOI: https://doi.org/10.1007/BF01753664

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