Abstract
Membrane-type matrix metalloproteinase 1 (MT1-MMP) has been recently described as an activator of proMMP-2 (MMP-2) which is involved in tumor invasion. We have shown by in situ hybridization that MT1-MMP is produced by stromal cells in close contact to preinvasive and invasive tumor cells of breast carcinomas. Of particular interest was the observation that some fibroblasts express this enzyme in focal areas in preinvasive lesions, suggesting that particular tumor cells may stimulate fibroblasts to produce MT1-MMP. We have therefore compared the ability of two different breast cancer cell lines, one non-invasive (MCF7) and one invasive (MDA-MB-231) to stimulate MT1-MMP production in human fibroblasts with consequent proMMP-2-activation. The MDA-MB-231 conditioned medium induced MT1-MMP mRNAs in human fibroblasts and a parallel activation of proMMP-2 whereas MCF7 conditioned medium did not have any effect. These results suggest the existence of soluble factor(s) secreted by invasive or some preinvasive breast tumor cells which stimulate fibroblasts to produce and activate MMPs, and emphasize the cooperation between cancer and stromal cells in tumor invasion.
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References
Azzam H, Arrand GA, Lippman ME and Thompson EW, 1993, MMP-2 activation potential associates with metastatic progression in human breast cancer cell lines, and is independent of MMP-2 production. JNCI, 85, 1758–64.
Gilles C, Polette M, Piette J, Birembaut P and Foidart JM, 1994, Epithelial to mesenchymal transition in HPV-33-transfected cervical keratinocytes is associated with increased invasiveness and expression of gelatinase A. Int J Cancer, 59, 661–6.
Brown PD, Levy AT, Margulies IM, Liotta LA and Stetler-Stevenson WG, 1990, Independent expression and cellular processing of Mr 72,000 type IV collagenase and interstitial collagenase in human tumorigenic cell lines. Cancer Res, 50, 6184–91.
Ward RV, Atkinon SJ, Slocombe PM et al.1991, Tissue inhibitor of metalloproteinases-2 inhibits the activation of 72 kDa progelatinase by fibroblast membrane. Biochem Biophys Acta, 1079, 242–6.
Murphy G, Willenbrock F, Ward RV et al.1992, The C-terminal domain of the 72 kDa gelatinase A is not required for catalysis but is essential for membrane activation and modulates interactions with tissue inhibitor of metalloproteinases. Biochem J, 283, 637–41.
Overall CM and Sodek J, 1990, Concanavalin A produces a matrix-degradive phenotype in human fibroblasts. J Biol Chem, 265, 21141–51.
Sato H, Takino T, Okada, et al.1994, A matrix metalloproteinase expressed on the surface of invasive tumor cells. Nature, 370, 61–5.
Gilles C, Polette M, Piette J, et al.1996, High level of MT-MMP expression is associated with invasiveness of cervical cancer cells. Int J Cancer, 65, 209–13.
Yu M, Sato H, Seiki M and Thompson EW, 1995, Complex regulation of membrane-type matrix metalloproteinase expression and matrix metalloproteinase-2 activation by concanavalin in MDA-MB-231 human breast cancer cells. Cancer Res, 55, 3272–7.
Yamamoto M, Mahanam S, Sawaya R, et al. 1996, Differential expression of membrane-type matrix metalloproteinase and its correlation with gelatinase A activation in human malignant brain tumors in vivoand in vitro. Cancer Res, 56, 384–92.
MacDougall JR and Matrisian LM, 1995, Contributions of tumor stromal matrix metalloproteinases to tumor progression, invasion and metastasis. Cancer Metastasis Rev, 14, 351–62.
Polette M and Birembaut P, 1996,Metalloproteinases and breast carcinomas. Breast J, 2, 1–13.
Birkedal-Hansen H, Moore WGI, Bodden MK, et al.1993, Matrix metalloproteinases: A review. Crit Rev Oral Biol Med, 4, 197–250.
Ellis SM, Nabeshima K and Biswas C, 1989, Monoclonal antibody preparation and purification of a tumor cell collagenase-stimulatory factor. Cancer Res, 49, 3385–91.
Kataoka H, Decastro R, Zucker S and Biswas C, 1993, Tumor cell-derived collagenase-stimulatory factor increases expression of interstitial collagenase, stromelysin and 72-kDa gelatinase. Cancer Res, 53, 3154–8.
Thompson EW, Paik S, Brünner N, et al.1992, Association of increased basement membrane invasiveness with absence of estrogen receptor and expression of vimentin in human breast cancer cell lines. J Cell Physiol, 150, 534–44.
Seog-Nyeon B, Arand G, Azzam H, et al. 1993, Molecular and cellular analysis of basement membrane invasion by human breast cancer cells in Matrigelbased in vitroassays. Breast Cancer Res Treat, 24, 214–55.
Okada A, Bellocq JP, Rouyer N, et al.1995, Membrane-type matrix metalloproteinase (MT-MMP) gene is expressed in stromal cells of human colon, breast, and head and neck carcinomas. Proc Natl Acad Sci USA, 92, 2730–4.
Polette M, Nawrocki B, Gilles C, et al.1996, MT-MMP expression and localisation in human breast and lung cancers. Virchows Arch, 428, 29–35.
Himelstein BP, Canete-Soler R, Bernhard E and Muschel RJ, 1992, Induction of fibroblast 92 kDa gelatinase/type IV collagenase expression by direct contact with metastatic tumor cells. J Cell Sci, 107, 477–86.
Noël AC, Munaut C, Nusgens B, Lapiere CM and Foidart JM, 1993, Different mechanisms of extracellular matrix remodelling by fibroblasts in reponse to human mammary neoplastic cells. Inv Metastasis, 13, 72–81.
Noël AC, Polette M, Lewalle JM, et al.1994, Coordinate enhancement of gelatinase A mRNA and activity levels in human fibroblasts in response to breast-adenocarcinoma cell. Int J Cancer, 56, 331–6.
Gilles C and Thompson EW, 1996, The epithelial to mesenchymal transition and metastatic progression in carcinoma. Breast J, 2, 83–96.
Ito A, Nakajima S, Sasaguri Y, Nagase H and Mori Y, 1995, Co-culture of human breast adenocarcinoma MCF-7 cells and human dermal fibroblasts enhances the production of matrix metalloproteinases 1, 2 and 3 in fibroblasts. Br J Cancer, 71, 1039–45.
Miyagi E, Yasumitsu H, Hirahara F, et al.1995, Marked induction of gelatinases, especially type B, in host fibroblasts by human ovarian cancer cells in athymic mice. Clin Exp Metastasis, 13, 89–96.
Bates SE, Davidson NE, Valverius EM, et al.1988, Expression of transforming growth factor a and its messenger ribonucleic acid in human breast cancer: its regulation by oestrogen and its possible functional significance. Mol Endocrinol, 2, 543–55.
Luparello C, Ginty AF, Gallagher JA, Pucci-Minafra I and Minafra S, 1993, Transforming growth factorβ1, β2, and β3, urokinase and parathyroid hormonerelated peptide expression in 8701-BC breast cancer cells and clones. Different, 55, 73–80.
Unemori EN, Hibbs MS and Amento EP, 1991, Constitutive expression of 92-kDa gelatinase (type IV) collagenase by rheumatoid synovial fibroblasts and its induction in normal human fibroblasts by inflammatory cytokines. J Clin Invest, 88, 1656–62.
Pei D and Weiss SJ, 1996, Transmembrane-deletion mutants of the membrane-type matrix metalloproteinase-1 process proMMP-2 and express intrinsic matrix-degrading activity. J Biol Chem, 271, 9135–40.
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Polette, M., Gilles, C., Marchand, V. et al. Induction of membrane-type matrix metalloproteinase 1 (MT1-MMP) expression in human fibroblasts by breast adenocarcinoma cells. Clin Exp Metastasis 15, 157–163 (1997). https://doi.org/10.1023/A:1018404927753
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DOI: https://doi.org/10.1023/A:1018404927753