Tumor Invasion and Metastases—Role of the Extracellular Matrix: Rhoads Memorial Award Lecture

Cancer Research

Volumn 46, Issue 1, 1986, Pages 1-7

  Liotta, Lance A ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BASEMENT MEMBRANE; CANCER INVASION; ETIOLOGY; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; METASTASIS; PRIORITY JOURNAL;

ANIMAL; ANTIBODIES, MONOCLONAL; BASEMENT MEMBRANE; CELL ADHESION; CELL MOVEMENT; COLLAGEN; EXTRACELLULAR MATRIX; HUMAN; LAMININ; MICROBIAL COLLAGENASE; NEOPLASM METASTASIS; NEOPLASMS; RECEPTORS, IMMUNOLOGIC; RECEPTORS, LAMININ;

EID: 0022656975     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: None     Document Type: Article

References (83)

1. Sugarbaker, E. V., Weingard, D. N., and Roseman, J. M. Observations on cancer metastases. In: L. A. Liotta and I. R. Hart (eds.), Cancer Invasion and Metastases, pp. 427–465. The Hague: Martinus Nijhoff, 1982.
2. Fidler, I. J., Gersten, D. M., and Hart, I. R. The biology of cancer invasion and metastasis. Adv. Cancer Res., 28: 149-160, 1978.
3. Nicolson, G. L. Cancer metastasis: organ colonization and the cell surface properties of malignant cells. Biochim. Biophys. Acta, 695; 113-120, 1982.
4. Liotta, L. A. Mechanisms of cancer invasion and metastases. In: V. T. DeVita, A. Hellman, and S. Rosenberg (eds.), Progress in Oncology, Vol. 1, pp. 28–41. New York: J. B. Lippincott, in press, 1985.
5. Poste, G., and Fidler, I. The pathogenesis of cancer metastases. Nature (Lond.), 283: 139-146, 1980.
6. Hay, E. D. Cell Biology of Extracellular Matrix. New York: Plenum Publishing Corp., 1982.
7. Kleinman, H. K., Klebe, R. J., and Martin, G. R. Role of collagenous matrices in the adhesion and growth of cells. J. Cell Biol., 88: 473-482, 1981.
8. Bemfield, M. R., Banerjee, S. D., and Cohn, R. H. Dependence of salivary epithelial morphology and branching morphogenesis upon acid mucopolysaccharide-protein (proteoglycan) at the epithelial surface. J. Cell Biol., 52: 674-680, 1972.
9. Wicha, M. S., Liotta, L. A., Garbisa, S., and Kidwell, W. R. Basement membrane collagen requirements for attachment and growth of mammary epithelium. Exp. Cell Res., 124: 181-190, 1980.
10. Liotta, L. A., Rao, C. N., and Barsky, S. H. Tumor invasion and the extracellular matrix. Lab. Invest., 49: 636-649, 1983.
11. Vracko, R. Basal lamina scaffold—anatomy and significance for maintenance of orderly tissue structures. Am. J. Pathol., 77; 313-346, 1974.
12. Martinez-Hemandez, A., and Amenta, P. S. The basement membranes In pathology. Lab. Invest., 48: 656-680, 1983.
13. Kefalides, N. A., Alper, R., and Clark, C. C. Biochemistry and metabolism of basement membranes. Int. Rev. Cytol., 61: 167-180, 1979.
14. 2 collagen from lung parenchyma. Am. J. Pathol., 94: 322-332, 1979.
15. Timpl, R., Wiedmann, H., VanDelden, V., Furthmayer, H., and Kuhn, K. A network for the organization of type IV collagen molecules in basement membrane. Eur. J. Biochem., 120: 203-212, 1981.
16. Hogan, B. L. M. High molecular weight extracellular proteins synthesized by endoderm cells derived from mouse teratocarcinoma cells and normal extraembryonic membranes. Dev. Biol., 76; 275-281, 1980.
17. Carlin, B., Jaffe, R., Bender, B., and Chung, A. E. Entactin, a novel basal lamina-associated sulfated glycoprotein. J. Biol. Chem., 256; 5209–5218, 1981.
18. Ozzello, L. The behavior of basement membranes in intraductal carcinoma of the breast. Am. J. Pathol., 35: 887-891, 1959.
19. Siegal, G. P., Barsky, S. H., Terranova, V. P., and Liotta, L. A. Stages of neoplastic transformation of human breast tissue as monitored by dissolution of basement membrane components. Invasion Metastasis, 1: 54-65, 1981.
20. Barsky, S. H., Siegal, G., Jannotta, F., and Liotta, L. A. Loss of basement membrane components by invasive tumors but not by their benign counterparts. Lab. Invest., 49: 140-148, 1983.
21. Burtin, P., Chavanel, G., Foidart, J. M., and Martin, E. Antigens of basement membrane in the peritumoral stroma in human colon adenocarcinomas: an immunofluorescence study. Int. J. Cancer, 30: 13-18, 1982.
22. Babai, F. Etude ultrastructural sur la pathogenie de l’invasion du muscle strie par des tumeurs transplantables. J. Ultrastruct. Res., 56; 287-297, 1976.
23. Liotta, L. A., Kleinerman, J., Catanzara, P., and Rynbrandt, D. Degradation of basement membrane by murine tumor cells. J. Natl. Cancer Inst., 58: 1427-1439, 1977.
24. Kramer, R. H., Gonzalez, R., and Nicolson, G. L. Metastatic tumor cells adhere preferentially to the extracellular matrix underlying vascular endothelial cells. Int. J. Cancer, 26; 639-642, 1980.
25. Terranova, V. P., Rohrbach, D. H., and Martin, G. R. Role of laminin in the attachment of PAM 212 (epithelial) cells to basement membrane collagen. Cell, 22: 719-726, 1980.
26. Timpl, R., Rhode, H., Robey, P. G., Rennard, S. I., Foidart, J.-M., and Martin, G. R. Laminin: a glycoprotein from basement membranes. J. Biol. Chem., 254: 9933-9941, 1979.
27. Terranova, V. P., Rao, C. N., Kalebic, T., Margulies, I. M. K., and Liotta, L. A. Laminin receptor on human breast carcinoma cells. Proc. Natl. Acad. Sci. USA, 80: 444-451, 1983.
28. Rao, C. N., Barsky, S. H., Terranova, V. P., and Liotta, L. A. Isolation of a tumor cell laminin receptor. Biochem. Biophys. Res. Commun., 111: 804-808, 1983.
29. Malinoff, H., and Wicha, M. S. Isolation of a cell surface receptor protein for laminin from murine fibrosarcoma cells. J. Cell Biol., 96: 1475-1480, 1983.
30. Lesot, H., Kuhl, U., and Vondermark, K. Isolation of a laminin-binding protein from muscle cell membranes. EMBO J., 2; 861-870, 1983.
31. Barsky, S. H., Rao, C. N., Hyams, D., and Liotta, L. A. Characterization of a laminin receptor from human breast carcinoma tissue. Breast Cancer Res. and Treat., in press, 1986.
32. Liotta, L. A., Horan Hand, P., Rao, C. N., Bryant, G., Barsky, S. H., and Schlom, J. Monoclonal antibodies to the human laminin receptor recognize distinct structural domains. Exp. Cell Res., 156: 117-126, 1985.
33. Horan Hand, P., Thor, A., Schlom, J., Rao, C. N., and Liotta, L. Expression of laminin receptor in normal and carcinomatous human tissues as defined by a monoclonal antibody. Cancer Res., 45: 2713-2719, 1985.
34. Roberts. D. D., Rao, C. N., Magnani, J. L., Spitalnik, S. L., Liotta, L. A., and Ginsburg, V. Laminin binds specifically to sulfated glycolipids. Proc. Natl. Acad. Sci. USA, 82: 1306-1310, 1985.
35. Grover, A., Andrews, G., and Adamson, E. D. Role of laminin in epithelium formation by F9 aggregates. J. Cell Biol., 97: 137-144, 1983.
36. Edgar, D., Timpl, R., and Thoenen, H. The heparin binding domain of laminin is responsible for its effects on neurite outgrowth and neuronal survival. EMBO J., 3: 1463-1468, 1984.
37. McCarthy, J., Palmard, S., and Furcht, L. Migration by hepatotaxis of a Schwann cell tumor line to the basement membrane glycoprotein laminin. J. Cell Biol., 97:772-779 1983.
38. Engel, J., Odermatt, E., Engel, A., Madri, J. A., Furthmayr, H., Rohde, H., and Timpl, R. Shapes, domain, organization, and flexibility of laminin and fibronectin, two multifunctional proteins of the extra cellular matrix. Mol. Biol., 150: 97-108, 1981.
39. Liotta, L. A., Goldfarb, R. H., Brundage, R., Siegal, G. P., Terranova, V., and Garbisa, S. Effect of plasminogen activator (urokinase), plasmin, and thrombin on glycoprotein and collagenous components of basement membrane. Cancer Res., 41: 4629-4635, 1981.
40. Rao, C. N., Goldstein, I. J., and Liotta, L. A. Lectin binding domains on laminin. Arch. Biochem. Biophys., 227: 118-124, 1983.
41. Rao. C. N., Margulies, I. M. K., Goldfarb, R. H., Madri, J. A., Woodley, D. T., and Liotta, L. A. Differential proteolytic susceptibility of laminin a and B subunits. Arch. Biochem. Biophys., 219: 65-72, 1982.
42. Rao, C. N., Margulies, I. M. K., Tralka, T. S., Terranova, V. P., Madri, J. A., and Liotta, L. A. Isolation of a submit of laminin and its role in molecular structure and tumor cell attachment. J. Biol. Chem., 257: 9740-9750, 1982.
43. Timpl, R., Johansson, S., VanDelden, V., Oberbaumer, I., and Hook, M. Characterization of protease-resistant fragments of laminin mediating attachment and spreading of rat hepatocytes. J. Biol. Chem., 258: 8922-8928, 1983.
44. Rao, C. N., Margulies, I. M. K., and Liotta, L. A. Binding domain for laminin on type IV collagen. Biochem. Biophys. Res. Commun., 128: 45-52, 1985.
45. Charanios, A. S., Tsilisbary, T. S., Yurchenko, P. D., and Furthmayr, H. Binding of laminin to type IV collagen: a morphological study. J. Cell Biol., 100: 1848-1853, 1985.
46. Barsky, S. H., Rao, C. N., Williams, J. E., and Liotta, L. A. Domains of laminin which alter metastases in a murine model. J. Clin. Invest., 74: 843-848, 1984.
47. 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: 2265-2273, 1982.
48. Varani, J., Lovett, E. J., McCoy, J. P., Shibata, S., Maddox, D., Goldstein, I., and Wicha, M. Differential expression of a laminin like substance by high and low metastatic tumor cells. Am. J. Pathol., 111: 27-34, 1983.
49. Thorgeirsson, U. P., Turpeenniemi-Hujanen, T., Neckers, L. M., Johnson, D. W., and Liotta, L. A. Protein synthesis but not DNA synthesis is required for tumor cell invasion in vitro. Invasion Metastasis, 4: 73-84, 1984.
50. Thorgeirsson, U. P., Liotta, L. A., Kalebic, T., Margulies, I. M. K., Thomas, K., Rios-Candelore, M., and Russo, R. G. Effect of natural protease inhibitors and a chemoattractant on tumor cell invasion in vitro. J. Natl. Cancer Inst., 69: 1049-1057, 1982.
51. Strauli, P. Proteinases and tumor invasion. In: P. Strauli, A. J. Barrett, and A. Baici (eds.), Proteinases and Tumor Invasion, Vol. 6, p. 215. New York: Raven Press, 1980.
52. Liotta, L. A., Thorgeirsson, U. P., and Garbisa, S. Role of collagenases in tumor cell invasion. Cancer Metastasis Rev., 1:277:297, 1982.
53. Wirl, G., and Frick, J. Collagenase: a marker enzyme in human bladder cancer. Urol. Res., 7:103, 1979.
54. Woolley, D. E., Tetlow, L. C., Mooney, C. J., and Evanson, J. M. Human collagenase and its extracellular inhibitors in relation to tumor invasiveness. In: P. Strand, A. J. Barrett, and A. Baiei (eds.), Proteinases and Tumor Invasion, pp. 97–134. New York: Raven Press, 1980.
55. Gross, J., and Nagai, Y. Specific degradation of the collagen molecule by tadpole collagenolytic enzyme. Proc. Natl. Acad. Sci. USA, 54: 1197–1210, 1965.
56. Wallace, A. C., Chew, E., and Jones, D. S. The arrest and extravasation of cancer cells in the lung. In: L. Weiss and H. A. Gilbert, Pulmonary Metastasis, Vol. 3. pp. 26–32. Boston: G. K. Hall, 1978.
57. 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: 67-68, 1980.
58. Liotta, L. A., Tryggvason, K., Garbisa, S., Rohey, P. G., and Abe, S. Partial purification and characterization of a neutral protease which cleaves type IV collagen. Biochemistry, 20: 100-108, 1981.
59. Salo, T., Liotta, L. A., Keski-Oja, J., Turpeenniemi-Hujanen, T., and Tryggvason, K. Secretion of basement membrane collagen degrading enzyme and plasminogen activator by transformed cells: role in metastases. Int. J. Cancer, 30: 669-674, 1982.
60. Salo, T., Liotta, L. A., and Tryggvason, K. Purification and characterization of murine basement membrane collagen-degrading enzyme secreted by metastatic tumor cells. J. Biol. Chem., 258: 2058-2062, 1983.
61. Henry, N., Eeckhout, Y., van Lamsweerde, A.-L., and Vaes, G. Co-operation between metastatic tumor cells and macrophages in the degradation of basement membrane (type IV) collagen. FEBS Letters, 161: 243-250, 1983.
62. Nakajima, M., Custead, S. E., Welch, D. R., and Nicolson, G. L. Type IV collagenolysis: relation to metastatic properties of rat 13762 mammary adenocarcinoma metastatic cell clones. Proc. Am. Assoc. Cancer Res., 25: 62, 1984.
63. Starkey, J. R., Hosick, H. L., Stanfard, D. R., and Liggitt, H. D. The interaction of metastatic tumor cells with bovine lens capsule basement membrane. Cancer Res. 44: 1585-1594, 1984.
64. Liotta, L. A., Abe, S., Gehron, 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: 2268-2276, 1979.
65. Welgus, H. G., Jeffrey, J. J., and Eisen, A. E. The collagen substrate specificity of human skin fibroblast collagenase. J. Biol. Chem., 256: 9511-9525, 1981.
66. Mainardi, C. L., Seyer, J. M., and Kang, A. H. Type-specific collagenolysis: a type V-degrading enzyme from macrophages. Biochem. Biophys. Res. Commun., 97: 1108-1112, 1980.
67. Kalebic, T., Garbisa, S., Glaser, B., and Liotta, L. A. Basement membrane collagen: Degradation by migrating endothelial cells. Science (Wash. DC), 221: 281-283, 1983.
68. Murphy, G., Cawston, T. E., Galloway, W. A., Barnes, M. J., Bunning, R. A. D., Mercer, E., Reynolds, J. J., and Burgeson, R. E. Metaloproteinases from rabbit bone culture medium degrade types IV and V collagens, laminin and fibronectin. Biochem. J., 199: 807-817, 1981.
69. Liotta, L. A., Lanzer, W. L., and Garbisa, S. Identification of a type V collagenolytic enzyme. Biochem. Biophys. Res. Commun., 98: 184-189, 1981.
70. Fessler, L. I., Duncan, K. G., Fessler, J. H., Salo, T., and Tryggvason, K. Characterization of the procollagen IV cleavage products produced by a specific tumor collagenase. J. Biol. Chem., 259: 9783-9789, 1984.
71. Thorgeirsson, U. P., Turpeenniemi-Huganen, T., Williams, J. E., Westin, E. H., Heilman, C. A., Talmadge, J. E., and Liotta, L. A. NIH-3T3 cells transfected with human tumor DNA containing activated ras oncogens express the metastatic phenotype in nude mide. Mol. Cell. Biol., 5: 259-262, 1985.
72. Turpeenniemi-Huganen, T., Thorgeirsson, U. P., Hart, I. R., Grant, S. S., and Liotta, L. A. Expression of collagenase IV (basement membrane collagenase) activity in murine tumor cell hybrids that differ in metastatic potential. J. Natl. Cancer Inst., 74; 99-103, 1985.
73. Muschel, R. J., Williams, J. E., Lowy, D. R., and Liotta, L. A. Harvey ras induction of metastatic potential depends upon oncogene activation and the type of recipient cell. Am. J. Pathol., 121: 1-8, 1985.
74. Bernstein, S. C., and Weinberg, R. A. Expression of the metastatic phenotype in cells transfected with human metastatic tumor DNA. Proc. Natl. Acad. Sci. USA,82; 1726-1730, 1985.
75. Greig, R. G., Koestler, T. P., Trainer, D. L., Corwin, S. P., Miles, L., Klein, T., Sweet, R., Yokoyama, S., and Poste, G. Tumorigenic and metastatic properties of “normal” and ras-transfected NIH/3T3 cells. Proc. Natl. Acad. Sci. USA, 82: 3698-3701, 1985.
76. Walich, R., Bulbuc, N., Hammerlin, G. J., Katzav, S., Segal, S., and Feldman, M. Abrogation of metastatic properties of tumor cells by de novo expression of H-2K antigens following H-2 gene transfection. Nature (Lond.), 315: 301-305, 1985.
77. Hart, I. R. Tumor cell hybridization and neoplastic progression. In: G. L. Nicolson and L. Milas (eds.), Cancer Invasion and Metastasis: Biologic and Therapeutic Aspects, pp. 133–143. New York: Raven Press, 1985.
78. Sidebottom, E., and Clark, S. R. Cell fusion segregates progressive growth from metastasis. Br. J. Cancer, 47: 399-406, 1983.
79. Ossowski, L., and Reich, E. Antibodies to plasminogen activator inhibit human tumor metastasis. Cell, 35: 611-619, 1983.
80. Poole, A. R., Recklies, A. D., and Mort, J. S. Secretion of proteinases from human breast tumors: excessive release from carcinomas of a thiol proteinase. In: P. Strauli, A. J. Barrett, and A. Baici (eds.), Proteases and Tumor Invasion, Vol. 6, pp. 215–217. New York: Raven Press, 1980.
81. Sloane, B. F., Dunn, J. R., and Horn, K. V. Lysosomal cathepsin B: correlation with metastatic potential. Science (Wash. DC), 212: 1151-1152, 1981.
82. Nakajima, M., Irimura, T., DiFerrante, N., and Nicolson, G. L. Metastatic melanoma cell heparanase. Characterization of heparan sulfate degradation fragments produced by B16 melanoma endoglucoronidase. J. Biol. Chem., 259: 2283-2290, 1984.
83. Liotta, L. A., et al. Tumor autocrine motility factor. Proc. Natl. Acad. Sci., in press, 1986.