Biological significance of interstitial collagenase in DMBA-induced mammary tumors of the rat
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Summary
In this review the production of interstitial collagenase in DMBA-induced mammary tumors of the rat has been examined. Cell sorting and cell cultures have given us the opportunity to relate the release of collagenase to a specific cell type. By means of FITC-fluorescence and monospecific antibodies (S. Sakamoto, Harvard University, Boston) it was further possible to localize collagenase in vitro and in vivo. The most outstanding characteristic is that collagenase is produced both by cuboidal, epithelial cell and by macrophages in vitro but not by myoepithelial-like cells. On the other hand, synthesis of collagenase in vivo was detected in some stromal cells, possibly macrophages, but not in neoplastic cuboidal cells. This observation has been related to the inability of cuboidal cells to interact with stromal, fibrillar collagen in vivo since tumor cells are arranged in glandular-like structures bordered by myoepithelial cells and a basement membrane.
In vitro, fibrillar rat tail tendon collagen was found to be a potent stimulator of collagenase production by cuboidal cells. Collagenase stimulation by interstitial collagen therefore suggests a plausible mechanism for the degradation of collagen fibrils during local invasion by mammary tumor cells.
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collagen collagenase mammary tumorsPreview
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- 1.Gross J, Highberger JH, Johnson-Wint B, Biswas C: Mode of action and regulation of tissue collagenases. In: Woolley DE, Evanson JM (eds) Collagenase in normal and pathological connective tissues. John Wiley & Sons, New York, 1980, pp 11–35.Google Scholar
- 2.Woolley DE, Glanville RW, Roberts DR, Evanson JM: Purification, characterization and inhibition of human skin collagenase. Biochem J 169: 265–276, 1978.Google Scholar
- 3.Valle KJ, Bauer EA: Biosynthesis of collagenase by human skin fibroblasts in monolayer culture. J Biol Chem 254: 10115–10122, 1979.Google Scholar
- 4.Schuppan D, Timpl R, Glanville RW: Discontinuities in the triple helical sequence gly-x-y of basement membrane (type IV) collagen. FEBS Lett 115: 297–305, 1980.Google Scholar
- 5.Miller EJ, Gay S, Haralson MA, Martinez-Hernandez A, Rhodes RK: Chemistry and biology of the type V collagen system. In: Kuehn K, Schoene HH, Timpl R (eds) New trends in basement membrane research. Raven Press, New York, 1982, pp 99–105.Google Scholar
- 6.Liotta LA, Abe S, Gehron Robey P, Martin GR: Preferential digestion of basement membrane collagen by an enzyme derived from a metastatic murine tumor. Proc Natl Acad Sci 76: 2268–2272, 1979.Google Scholar
- 7.Salo T, Liotta LA, 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.Google Scholar
- 8.Birbeck MSC, Wheatley DN: An electron microscopic study of the invasion of ascites tumor cells into the abdominal wall. Cancer Res 25: 490–497, 1965.Google Scholar
- 9.Tarin D: Sequential electron microscopical study of experimental mouse skin carcinogenesis. Int J Cancer 2: 195–211, 1967.Google Scholar
- 10.Tarin D: Fine structure of murine mammary tumors: The relationship between epithelium and connective tissue in neoplasms induced by various agents. Br J Cancer 23: 417–425, 1969.Google Scholar
- 11.Dresden MH, Heilman SA, Schmidt JD: Collagenolytic enzymes is human neoplasms. Cancer Res 32: 993–996, 1972.Google Scholar
- 12.McCroskery PA, Richards JF, Harris EDJr.: Purification and characterization of a collagenase extracted from rabbit tumours. Biochem J 152: 131–142, 1975.Google Scholar
- 13.Wirl G, Frick J: Collagenase-A marker enzyme in human bladder cancer? Urol Res 7: 103–108, 1979.Google Scholar
- 14.Tane N, Hashimoto K, Kanzaki T, Ohyama H: Collagenolytic activities of cultured human malignant melanoma cells. J Biochem 84: 1171–1176, 1978.Google Scholar
- 15.Wolf W, Wirl G: Collagenase in the Walker 256 carcinoma. A study of the latent and active enzyme in vivo and in vitro. Eur J Biochem 121: 623–629, 1982.Google Scholar
- 16.Bauer EA, Gordon JH, Reddick ME, Eisen AZ: Quantitation and immunocytochemical localization of human skin collagenase in basal cell carcinoma. J Invest Dermatol 69: 363–367, 1977.Google Scholar
- 17.Woolley DE, Tetlow LC, Mooney CJ, Evanson JM: Human collagenase and its extracellular inhibitors in relation to tumor invasiveness. In: Sträuli P, Barrett AJ, Baici A (eds) Proteinases and tumor invasion. Raven Press, New York, 1980, pp 97–115.Google Scholar
- 18.Barsky SH, Siegal GP, Jannota F, Liotta LA: Loss of basement membrane components by invasive tumors but not by their benign counterparts. Lab Invest 49: 140–147, 1983.Google Scholar
- 19.Strauch L: The role of collagenases in tumour invasion. In: Tarin D (ed) Tissue interactions in carcinogenesis. Academic Press, New York, 1972, pp 399–435.Google Scholar
- 20.Recklies AD, Tiltman KJ, Stoker AM, Poole AR: Secretion of proteinases from malignant and nonmalignant human breast tissue. Cancer Res 40: 550–556, 1980.Google Scholar
- 21.Kuettner KE, Soble L, Croxen RL, Marczynska B, Hiti J, Harper E: Tumor cell collagenase and its inhibition by a cartilagederived protease inhibitor. Science 196: 653–654, 1977.Google Scholar
- 22.O'Grady RL, Upfold L, Stephens RW: Rat mammary carcinoma cells secrete active collagenase and activate latent enzyme in the stroma via plasminogen activator. Int J Cancer 28: 509–515, 1981.Google Scholar
- 23.Tarin D, Hoyt BJ, Evans DJ: Correlation of collagenase secretion with metastatic-colonization potential in naturally occuring murine mammary tumours. Br J Cancer 46: 266–277, 1982.Google Scholar
- 24.Shafie SM, Liotta LA: Formation of metastasis by human breast carcinoma cells (MCF-7) in nude mice. Cancer Letters 11: 81–87, 1980.Google Scholar
- 25.Barsky SH, Togo S, Garbisa S, Liotta LA: Type IV collagenase immunoreactivity in invasive breast carcinoma. The Lancet 1: 296, 1983.Google Scholar
- 26.Liotta LA, Kleinerman J, Catanzaro P, Rynbrandt D: Degradation of basement membrane by murine tumor cells. J Natl Cancer Inst 58: 1427–1431, 1977.Google Scholar
- 27.Siegal GF, Barsky SH, Terranova VP, Liotta LA: Stages of neoplastic transformation of human breast tissue as monitored by dissolution of basement membrane components. An immunoperoxydase study. Invasion Metastasis 1: 54–71, 1981.Google Scholar
- 28.Haslam SZ, Bern HA: Histopathogenesis of 7,12-dimethylbenz(a)-anthracene-induced rat mammary tumors. Proc Natl Acad Sci USA 74: 4020–4024, 1977.Google Scholar
- 29.Russo J, Tait L, Russo IH: Susceptibility of the mammary gland to carcinogenesis III. The cell of origin of rat mammary carcinoma. Am J Pathol 113: 50–65, 1983.Google Scholar
- 30.Huggins C, Briziarelli G, Sutton H: Rapid induction of mammary carcinoma in the rat and the influence of hormones on the tumors. J Exp Med 109: 25–54, 1959.Google Scholar
- 31.Wirl G: Extractable collagenase and carcinogenesis of the mouse skin. Connect Tissue Res 5: 171–178, 1977.Google Scholar
- 32.Yang J, Richards J, Guzman R, Imagawa W, Nandi S: Sustained growth in primary culture of normal mammary epithelial cells embedded in collagen gels. Proc Natl Acad Sci USA 77: 2088–2092, 1980.Google Scholar
- 33.Wicha MS, Lowrie G, Kohn E, Bagavandoss, Mahn T: Extracellular matrix promotes mammary epithelial growth and differentiation in vitro. Proc Natl Acad Sci USA 79: 3213–3217, 1982.Google Scholar
- 34.Haeuptle MT, Suard YLM, Bogenmann E, Reggio H, Racine L, Kraehenbuhl JP: Effect of cell shape change on the function and differentiation of rabbit mammary cells in culture. J Cell Biol 96: 1425–1434, 1983.Google Scholar
- 35.Emerman JT, Pitelka DR: Maintenance and induction of morphological differentiation in dissociated mammary epithelium on floating collagen membranes. In Vitro 23: 316–328, 1977.Google Scholar
- 36.Ossowski L, Biegel D, Reich E: Mammary plasminogen activator: Correlation with involution, hormonal modulation and comparison between normal and neoplastic tissue. Cell 16: 929–940, 1979.Google Scholar
- 37.Evers JL, Patel J, Madeja JM, Schneider SL, Hobika GH, Camiolo SM, Markus G: Plasminogen activator activity and composition in human breast cancer. Cancer Res 42: 219–226, 1982.Google Scholar
- 38.Ceriani RL, Taylor-Papadimitriou J, Peterson JA, Brown P: Characterization of cells cultured from early lactation milks. In Vitro 15: 356–362, 1979.Google Scholar
- 39.Werb Z, Bainton DF, Jones PA: Degradation of connective tissue matrices by macrophages. J Exp Med 152: 1537–1553, 1980.Google Scholar
- 40.Werb Z, Gordon S: Secretion of a specific collagenase by stimulated macrophages. J Exp Med 142: 346–360, 1975.Google Scholar
- 41.Horwitz AL, Crystal RG: Collagenase from rabbit pulmonary alveolar macrophages. Biochem Biophys Res Commun 69: 296–303, 1976.Google Scholar
- 42.Sakamoto N, Alfant M, Sakamoto S: Isolation and immunochemical localization of collagenase in mouse peritoneal macrophages. J Biochem 90: 715–720, 1981.Google Scholar
- 43.Hallowes RC, Rudland PS, Hawkins RA, Lewis DJ, Bennet D, Durbin H: Comparison of the effects of hormones on DNA synthesis in cell cultures of nonneoplastic and neoplastic mammary epithelium from rats. Cancer Res 37 2492–2504, 1977.Google Scholar
- 44.Wahl LM, Blandau RJ, Page RC: Effect of hormones on collagen metabolism and collagenase activity in the public symphysis ligament of the guinea pig. Endocrinol 100: 571–579, 1977.Google Scholar
- 45.Koob TJ, Jeffrey JJ, Eisen AZ, Bauer EA: Hormonal interactions in mammalian collagenase regulation. Comparative studies in human skin and rat uterus. Biochim Biophys Acta 629: 13–23, 1980.Google Scholar
- 46.Biswas C, Moran WP, Bloch KJ, Gross J: Collagenolytic activity of rabbit V2-Carcinoma growing at multiple sites. Biochem Biophys Res Commun (80): 33–38, 1978.Google Scholar
- 47.Bussolati G, Botta G, Guriotta P: Actin-rich (Myoepithelial) cells in ductal carcinoma-in-situ of the breast. Virchows Arch B Cell Path (34): 251–259, 1980.Google Scholar
- 48.Gusterson BA, Warburton MJ, Mitchell D, Ellison M, Neville AM, Rudland PS: Distribution of myoepithelial cells and basement membrane proteins in the normal breast and in benign and malignant breast diseases. Cancer Res 42: 4763–4770, 1982.Google Scholar
- 49.Bennet DC, Peachy LA, Durbin H, Rudland PS: A possible mammary stem cell line. Cell 15: 283–298, 1978.Google Scholar
- 50.Warburton MJ, Mitchell D, Ormerod EA, Rudland PS: Distribution of myoepithelial cells and basement membrane proteins in the resting, pregnant, lactating and involuting rat mammary gland. J Histochem Cytochem 30: 667–676, 1982.Google Scholar
- 51.Ormerod EJ, Warburton MJ, Hughes C, Rudland PS: Synthesis of basement membrane proteins by rat mammary epithelial cells. Dev Biol 96: 269–275, 1983.Google Scholar
- 52.Dulbecco R, Henahan M, Armstrong B: Cell types and morphogenesis in the mammary gland. Proc Natl Acad Sci USA 79: 7346–7350, 1982.Google Scholar
- 53.Williams JM Daniel CW: Mammary ductal elongation: Differentiation of myoepithelium and basal lamina during branching morphogenesis. Dev Biol 97: 274–290, 1983.Google Scholar
- 54.David G, Bernfield MR: Collagen reduces glycosaminoglycan degradation by cultured mammary epithelial cells: Possible mechanism for basal lamina formation. Proc Natl Acad Sci USA 76: 786–790, 1979.Google Scholar
- 55.Shannon JM, Pitelka DR: Influence of cell shape on the induction of functional differentiation in mouse mammary cells in vitro. In Vitro 17: 1016–1028, 1981.Google Scholar
- 56.Rapraeger AC, Bernfield MR: Integral membrane proteoglycan is capable of binding components of the cytoskeleton and the extracellular matrix. In: Hawkes S, Wang JL (eds) Extracellular matrix. Academic Press, New York, 1982, pp 265–269.Google Scholar
- 57.Biswas C, Dayer JM: Stimulation of collagenase production by collagen in mammalian cell cultures. Cell 18: 1035–1041, 1979.Google Scholar
- 58.Goldberg B: Binding of soluble type I collagen molecules to the fibroblast plasma membrane. Cell 16: 265–275, 1979.Google Scholar
- 59.Chiang TM, Kang AH: Isolation and purification of collagen 1(I) receptor from human platelet membrane. J Biol Chem 257: 7581–7586, 1982.Google Scholar
- 60.Mollenhauer J, von der Mark K: Isolation and characterization of a collagen binding glycoprotein from chondrocyte membranes. EMBO J 2: 45–50, 1983.Google Scholar
- 61.Eccles SA, Alexander P: Macrophage content of tumors in relation to metastatic spread and host immune reaction. Nature 250: 667–669, 1974.Google Scholar
- 62.Svennevig JL, Svaar H: Content and distribution of macrophages and lymphocytes in solid malignant human tumors. Int J Cancer 24: 754–758, 1979.Google Scholar
- 63.Henry N, Eeckhout Y, van Lamsweerde AL, Vaes G: Co-operation between metastatic tumor cells and macrophages in the degradation of basement membrane (type IV) collagen. FEBS Letters 161: 243–247, 1983.Google Scholar