[en] Interactions between tumor cells and basement membranes represent a critical step in the progression of neoplasia and in the metastatic process. Reconstituted basement membrane matrix, matrigel, has been recently used with the aim of developing an in vitro assay of tumor cell invasiveness. We have extended these studies by comparing the invasiveness of a large series of normal and malignant epithelial and mesenchymal cells of human and animal origin cultured on matrigel. Normal cells (fibroblasts, glomerular mesangial cells, keratinocytes), human fibrosarcoma cells (HT1080), and reticular sarcoma cells (M5076) clearly established invasive capabilities in the matrix. However, all the other tested cell lines, malignant or virally transformed cells invasive in vivo (MCF7, T47D, SA52, SW613, MO4, A431, BeWo), as well as normal nontransformed cells (MOH22) were incapable of penetration. The morphological features of matrigel invasion by normal fibroblasts and HT1080 cells are described at the light and electron microscope levels. The extent of degradation of a radiolabeled matrigel is minimal and similar in several cell lines reported to be noninvasive or invasive in vivo. Our data suggest that matrigel does not provide a universal model to correlate the invasiveness of cells in vivo and in vitro.
Noël, Agnès ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biologie cellulaire et moléculaire appliquée à l'homme
Calle, A.
Emonard, H.
Nusgens, Betty ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Département des sciences biomédicales et précliniques
Simar, L.
Lapiere, C. M.
Foidart, Jean-Michel ; Université de Liège - ULiège > Département des sciences cliniques > Gynécologie - Obstétrique
Language :
English
Title :
Invasion of Reconstituted Basement Membrane Matrix Is Not Correlated to the Malignant Metastatic Cell Phenotype
Publication date :
01 January 1991
Journal title :
Cancer Research
ISSN :
0008-5472
eISSN :
1538-7445
Publisher :
American Association for Cancer Research, Inc. (AACR), Baltimore, United States - Maryland
Kleinman, H. K., Cannon, F. B., Laurie, G. W., Hassell, J. R., Aumailley, M., Terranova, V. P., Martin, G. R., and Dubois-Dalcq, M. Biological activities of laminin. J. Cell Biochem., 27:317-325, 1985.
Liotta, L. A., Abe, S., Gehron-Robey, P., and Martin, G. R. Preferential digestion of basement membrane collagen by an enzyme derived from a metastatic murine tumor. Proc. Natl. Acad. Sci. USA, 76:2268-2272, 1979.
Terranova, V. P., Williams, J. E., and Liotta, L. A. Modulation of the metastatic activity of melanoma cells by laminin and fibronectin. Science (Washington DC), 226:982-984, 1984.
Terranova, V. P., Liotta, L. A., Russo, R. G., and Martin, G. R. Role of laminin in the attachment and metastasis of murine tumor cells. Cancer Res., 42:2265-2269, 1982.
Poste, G., Doll, J., Hart, I. R., and Fidler, I. J. In vitro selection of murine B16 melanoma variants with enhanced tissue-invasive properties. Cancer Res., 40:1636-1644, 1980.
Liotta, L. A., Lee, W. C., and Morakis, D. J. New methods for preparing large surfaces of intact human basement membrane for tumor invasion studies. Cancer Lett., 11:141-147, 1980.
Kramer, R. H., Bensch, K. G., and Wong, J. Invasion of reconstituted basement membrane matrix by metastatic human tumor cells. Cancer Res., 46:1980-1989, 1986.
Albini, A., Iwamoto, Y., Kleinman, H. K., Martin, G. R., Aaronson, S. A., Kozlowski, J. M., and McEwan, R. N. A rapid in vitro assay for quantitating the invasive potential of tumor cells. Cancer Res., 47: 3239-3245, 1987.
Terranova, V. P., Hujanen, E. S., Loeb, D. M., Martin, G. R., Thornburg L., and Glushko, V. Use of a reconstituted basement membrane to measure cell invasiveness and select for highly invasive tumor cells. Proc. Natl. Acad. Sci. USA, 83:465-469, 1986.
Kleinman, H. K., Me Garvey, M. L., and Hassel, J. R. Basement membrane complexes with biological activity. Biochemistry, 25: 312-318, 1986.
Kleinman, H. K., Me Garvey, M. L., Liotta, L. A., Gehron Robey, P., Tryggvason, K., and Martin, G. R. Isolation and characterization of type IV procollagen, laminin and heparan sulfate proteoglycan from the EHS sarcoma. Biochemistry, 24:6188-6193, 1982.
Emonard, H., Calle, A., Grimaud, J. A., Peyrol, S., Castronovo, V., Noel, A., Lapiere, C. M., and Foidart, J. M. Interactions between fibroblasts and a reconstituted basement membrane matrix. J. Invest. Dermatol., 89: 156-163, 1987.
Bergman, I., and Loxley, R. Two improved and simplified methods for the spectrophotometric determination of hydroxyproline. Anal. Chem., 35: 1961-1965, 1963.
Bitter, T., and Muir, H. M. A modified uronic acid carbazol reaction. Anal. Biochem., 4: 330-334, 1962.
Delvoye, P., Nusgens, B., and Lapiere, C. M. The capacity of retracting a collagen matrix is lost by dermatosparactic skin fibroblasts. J. Invest. Dermatol., 81: 267-270, 1983.
Green, H., Kehinde, O., and Thomas, J. Growth of cultured human epidermal cells into multiple epithelia suitable for grafting. Proc. Natl. Acad. Sci. USA, 76: 5665-5668, 1979.
Foidart, J. M., Foidart, J. B., Van Cauwenberghe, D., Decoux, M., Stul, M., Lenaers, A., Niebes, P., and Mahieu, P. R. Synthesis of types I, II, IV and V (A, B) collagens by glomerular mesangial cells and aortic smooth muscle cells in culture. In: F. Morel (ed.), Biochemistry of Kidney Functions. INSERM Symposium, Vol. 21, pp. 23-34. Amsterdam: Elsevier Biomedical Press, 1982.
Rasheed, S., Nelson-Rees, W. A., Toth, E. M., Amstein, P., and Gardner, M. B. Characterization of a newly derived human sarcoma cell line (HT1080). Cancer (Phila.), 33: 1027-1033, 1974.
Manoury, R. Etablissement et caracterisation de trois lignees cellulaires humaines derivees de tumeurs metastatiques cerebrates. CR Acad. Sci. (Paris), 284: 991-994, 1977.
Engel, L. W., and Young, N. A. Human breast carcinoma cells in continuous culture. A review. Cancer Res., 38:4327-4339, 1978.
Keydar, I., Chen, L., Karby, S., Weiss, F. R., Delarea, J., Radu, M., Chaitcik, S., and Brenner, H. J. Establishment and characterization of a cell line of human breast carcinoma origin. Eur. J. Cancer, 15:659-670, 1979.
Soule, H. D., Vazquez, J., Long, A., Albert, S., and Brennan, M. T. Human cell line from pleural effusion derived from breast carcinoma. J. Natl. Cancer Inst., 51: 1409-1413, 1973.
Soule, H. D., and McGrath, C. M. Estrogen responsive proliferation of clonal human breast carcinoma cells in athymic mice. Cancer Lett., 10: 177-189, 1980.
Kasid, A., Lippman, M. E., Papageorge, A. G., Lowy, D. R., and Gelmann, E. P. Transfection of V-ros DNA into MCF7 human breast cancer cells bypasses dependence in estrogen for tumorigenicity. Science (Washington DC), 228: 725-728, 1985.
Pattillo, R. A., and Gey, G. O. The establishment of a cell line of human hormone-synthesizing trophoblastic cells in vitro. Cancer Res., 28: 1231-1236, 1969.
Sekiya, S., Oosaki, T., Suzuki, N., and Takamizawa, H. Invasion potential of human choriocarcinoma cell lines and the role of lytic enzymes. Gynecol. Oncol., 22:324-333, 1985.
Santon, J. B., Cronin, M. T., Macleod, C. L., Mendelsohn, J., Masui, H., and Gill, G. N. Effect of epidermal growth factor receptor concentration on tumorigenicity of 4431 cells in nude mice. Cancer Res., 46: 4701-4705, 1986.
Giavazzi, R., Liotta, L., and Hart, I. Laminin inhibits the adhesion of a murine tumor of macrophage origin. Exp. Cell Res., 140: 315-322, 1982.
Mareel, M., De Ridder, L., De Brabander, M., and Vakaet, L. Characterization of spontaneous chemical and viral transformants of a C3H/3T3 type mouse cell line by transplantation into young chick blastoderms. J. Natl. Cancer Inst., 54:923-929, 1975.
Emonard, H., Christiane, Y., Smet, M., Grimaud, J. A., and Foidart, J. M. Type IV and interstitial collagenolytic activities in normal and human hormone-synthesizing trophoblastic cells in vitro. Invasion Metastasis, 10:170-177, 1990.
Reich, R., Thompson, E. W., Iwamoto, Y., Martin, G. R., Deason, J. R., Fuller, G. C., and Miskin, R. Effects of inhibitors of plasminogen activator, serine proteases and collagenase IV on the invasion of basement membranes by metastatic cells. Cancer Res., 48: 3307-3312, 1988.
Liotta, L. A. Invasion and metastasis: role of basement membrane. Am. J. Pathol., 117: 339-348, 1984.
Zucker, S., Wieman, J. M., Lysik, R. M., Wilkie, D., Ramamurthy, N. S., Golub, L. M., and Lane, B. Enrichment of collagen and gelatin degrading activities in the plasma membranes of human cancer cells. Cancer Res., 47: 1608-1614, 1987.
Kramer, R. H., and Vogel, K. G. Selective degradation of basement membrane macromolecules by metastatic melanoma cells. J. Natl. Cancer. Inst., 72: 889-899, 1984.
Salo, T., Liotta, L. A., and Tryggvason, K. Purification and characterization of a murine basement membrane collagen-degrading enzyme secreted by metastatic tumor cells. J. Biol. Chem., 258: 3058-3063, 1983.
Liotta, L. A., and Goldfarb, R. H. Interaction of tumor cells with the basement membrane of endothelium. In: K. V. Honn and B. F. Sloane (eds.), Hemostatic Mechanisms and Metastasis, pp. 319-374. Boston: Martinus Nijhoff Publishing, 1984.
Liotta, L. A., Tryggvason, K., Garbisa, S., Hart, I., Foltz, C. M., and Shafie, S. Metastatic potential correlates with enzymatic degradation of basement membrane collagen. Nature (Lond.), 284:65, 1980.
Bonfll, R. D., Reddel, R. R., Ura, H., Reich, R., Fridman, R., Harris, C. C., and Klein-Szanto, A. J. P. Invasive and metastatic potential of a V-Ha-raj-transformed human bronchial epithelial cell line. J. Natl. Cancer Inst., 81: 587-594, 1989.
Krystosek, A., and Seeds, N. W. Peripheral neurons and Schwan cells secrete plasminogen activator. J. Cell Biol., 98: 773-776, 1984.
Me Guire, P. G., and Seeds, N. W. The interaction of plasminogen activator with a reconstituted basement membrane matrix and extracellular macromolecules produced by cultured epithelial cells. J. Cell. Biochem., 40, 215-227, 1989.
Turpeenniemi-Hujanen, T., Thorgeirsson, U. P., Rao, C. N., and Liotta, L. A. Laminin increases the release of type IV collagenase from malignant cells. J. Cell. Biochem., 261: 1883-1889, 1986.
Jones, P. A., Heustein, H. B., Gonzales, F., and Bogenmanne, E. Invasion of an artificial blood vessel wall by human fibrosarcoma cells. Cancer Res., 41:4613-4620, 1981.
Noel, A., Calle, A., Emonard, H., Nusgens, B., Foidart, J. M., and Lapiere, Ch.M. Antagonistic effects of laminin and fibronectin on cell to cell and cell to matrix interactions in MCF7 cultures. In Vitro (Rockville), 24: 373-379, 1988.
Hadley, M. A., Byers, S. W., Suarez-Quian, C. A., Kleinman, H. K., and Dym, M. Extracellular matrix regulates Sertoli cell differentiation, testicular cord formation and germ cell development in vitro. J. Cell Biol., 101: 1511-1522, 1985.
Bendayan, M., Duhr, M. A., and Gingras, D. Studies of pancreatic acinar cells in tissue culture: basal lamina (basement membrane) matrix promotes 3-dimensional reorganization. Eur. J. Cell Biol., 42:60-67, 1986.
Li, M. L., Aggeler, J., Farson, D. A., Hatier, C., Hassell, J., and Bissell, J. Influence of reconstituted basement membrane and its component on casein gene expression and secretion in mouse mammary epithelial cells. Proc. Natl. Acad. Sci. USA, 84: 136-140, 1986.
Oliver, C., Waters, J. F., Tolbert, C. L., and Kleinman, H. K. Culture of parotid acinar cells on a reconstituted basement membrane substratum. J. Dent. Res., 66: 594-595, 1987.
