Abstract
Tissue remodeling is a key process involved in normal development, wound healing, bone remodeling, and embryonic implantation, as well as pathological conditions such as tumor invasion and metastasis, and angiogenesis. The degradation of the extracellular matrix that is associated with those processes is mediated by a number of families of extracellular proteinases. These families include the serine proteinases, such as the plasminogen-urokinase plasminogen activator system and leukocyte elastases, the cysteine proteinases, like cathepsin D and L, and the zinc-dependent matrix metalloproteinases (MMPs) [1]. Accumulating evidence has highlighted the central role of MMP-driven extracellular matrix remodeling in mammary gland development and breast cancer.
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References
Alexander CM, Werb Z: Extracellular matrix degradation. In: Hay ED (ed.) Cell Biology of Extracellular Matrix. Plenum Press, New York, 1991, pp 255–301
Aimes RT, Quigley JP: Matrix metalloproteinase-2 is an interstitial collagenase. Inhibitor-free enzyme catalyzes the cleavage of collagen fibrils and soluble native type I collagen generating the specific 3/4-and 1/4-length fragments. J Biol Chem 270: 5872–5876, 1995
Freije JM, Diez-Itza I, Balbin M, Sanchez LM, Blasco R, Tolivia J, Lopez-Otin C: Molecular cloning and expression of collagenase-3, a novel human matrix metalloproteinase produced by breast carcinomas. J Biol Chem 269: 16766–16773, 1994
Stolow MA, Bauzon DD, Li J, Sedgwick T, Liang VC, Sang QA, Shi YB: Identification and characterization of a novel collagenase in Xenopus laevis: possible roles during frog development. Mol Biol Cell 7: 1471–1483, 1996
Cossins J, Dudgeon TJ, Catlin G, Gearing AJ, Clements JM: Identification of MMP-18, a putative novel human matrix metalloproteinase. Biochem Biophys Res Commun 228: 494–498, 1996
Pei D, Majmudar G, Weiss SJ: Hydrolytic inactivation of a breast carcinoma cell-derived serpin by human stromely-sin-3. J Biol Chem 269: 25849–25855, 1994
Ochieng J, Fridman R, Nangia-Makker P, Kleiner DE, Liotta LA, Stetler-Stevenson WG, Raz A: Galectin-3 is a novel substrate for human matrix metalloproteinase-2 and-9. Biochemistry 33: 14109–14114, 1994
Ito A, Mukaiyama A, Itoh Y, Nagase H, Thogersen IB, Enghild JJ, Sasaguri Y, Mori Y: Degradation of interleukin 1beta by matrix metalloproteinases. J. Biol Chem 271: 14657–14660, 1996
Fowles JL, Enghild JJ, Suzuki K, Nagase H: Matrix metalloproteinases degrade insulin-like growth factor-binding protein-3 in dermal fibroblast cultures. J Biol Chem 269: 25742–25746, 1994
Birkedal-Hansen H, Moore WG, Bodden MK, Windsor LJ, Birkedal-Hansen B, De Carlo A, Engler JA: Matrix metalloproteinases: a review. Crit Rev Oral Biol Med 4: 197–250, 1993
Gomis-Ruth FX, Gohlke U, Betz M, Knauper V, Murphy G, Lopez-Otin C, Bode W: The helping hand of collagenase-3 (MMP-13): 2.7 A crystal structure of its C-terminal haemopexin-like domain. J Mol Biol 264: 556–566, 1996
Bode W, Reinemer P, Huber R, Kleine T, Schnierer S, Tschesche H: The X-ray crystal structure of the catalytic domain of human neutrophil collagenase inhibited by a substrate analogue reveals the essentials for catalysis and specificity. EMBO J 13: 1263–1269, 1994
Matrisian LM, Hogan BL: Growth factor-regulated proteases and extracellular matrix remodeling during mammalian development. Curr Top Dev Biol 24: 219–259, 1990
Brenner DA, O'Hara M, Angel P, Chojkier M, Karin M: Prolonged activation of jun and collagenase genes by tumour necrosis factor-alpha. Nature 337: 661–663, 1989
West-Mays JA, Strissel KJ, Sadow PM, Fini ME: Competence for collagenase gene expression by tissue fibroblasts requires activation of an interleukin 1 alpha autocrine loop. Proc Natl Acad Sci USA 92: 6768–6772, 1995
Corcoran ML, Hewitt RE, Kleiner Jr DE, Stetler-Stevenson WG: MMP-2: expression, activation and inhibition. Enzyme Protein 49: 7–19, 1996
Kerr LD, Magun BE, Matrisian LM: The role of c-Fos in growth factor regulation of stromelysin/transin gene expression. Matrix Suppl 1: 176–183, 1992
Gaire M, Magbanua Z, McDonnell S, McNeil L, Lovett DH, Matrisian LM: Structure and expression of the human gene for the matrix metalloproteinase matrilysin. J Biol Chem 269: 2032–2040, 1994
Wasylyk C, Gutman A, Nicholson R, Wasylyk B: The c-Ets oncoprotein activates the stromelysin promoter through the same elements as several non-nuclear oncoproteins. EMBO J 10: 1127–1134, 1991
Gum R, Lengyel E, Juarez J, Chen JH, Sato H, Seiki M, Boyd D: Stimulation of 92-kDa gelatinase B promoter activity by ras is mitogen-activated protein kinase kinase 1-independent and requires multiple transcription factor binding sites including closely spaced PEA3/ets and AP-1 sequences. J Biol Chem 271: 10672–10680, 1996
Mauviel A, Chung KY, Agarwal A, Tamai K, Uitto J: Cell-specific induction of distinct oncogenes of the Jun family is responsible for differential regulation of collagenase gene expression by transforming growth factor-beta in fibroblasts and keratinocytes. J Biol Chem 271: 10917–10923, 1996
Braunhut SJ, Moses MA: Retinoids modulate endothelial cell production of matrix-degrading proteases and tissue inhibitors of metalloproteinases (TIMP). J Biol Chem 269: 13472–13479, 1994
Anglard P, Melot T, Guerin E, Thomas G, Basset P: Structure and promoter characterization of the human stromelysin-3 gene. J Biol Chem 270: 20337–20344, 1995
Jonat C, Rahmsdorf HJ, Park KK, Cato AC, Gebel S, Ponta H, Herrlich P: Antitumor promotion and antiinflammation: down-modulation of AP-1 (Fos/Jun) activity by glucocorticoid hormone. Cell 62: 1189–1204, 1990
Werb Z, Tremble PM, Behrendtsen O, Crowley E, Damsky CH: Signal transduction through the fibronectin receptor induces collagenase and stromelysin gene expression. J Cell Biol 109: 877–889, 1989
Tremble P, Chiquet-Ehrismann R, Werb Z: The extracellular matrix ligands fibronectin and tenascin collaborate in regulating collagenase gene expression in fibroblasts. Mol Biol Cell 5: 439–453, 1994
Huhtala P, Humphries MJ, McCarthy JB, Tremble PM, Werb Z, Damsky CH: Cooperative signaling by alpha 5 beta 1 and alpha 4 beta 1 integrins regulates metalloproteinase gene expression in fibroblasts adhering to fibronectin. J Cell Biol 129: 867–879, 1995
Langholz O, Rockel D, Mauch C, Kozlowska E, Bank I, Krieg T, Eckes B: Collagen and collagenase gene expression in three-dimensional collagen lattices are differentially regulated by alpha 1 beta 1 and alpha 2 beta 1 integrins. J Cell Biol 131: 1903–1915, 1995
Tremble P, Damsky CH, Werb Z: Components of the nuclear signaling cascade that regulate collagenase gene expression in response to integrin-derived signals. J Cell Biol 129: 1707–1720, 1995
Petersen MJ, Woodley DT, Stricklin GP, O'Keefe EJ: Enhanced synthesis of collagenase by human keratinocytes cultured on type I or type IV collagen. J Invest Dermatol 94: 341–346, 1990
Petersen MJ, Woodley DT, Stricklin GP, O'Keefe EJ: Synthesis and regulation of keratinocyte collagenase. Matrix Suppl 1: 192–197, 1992
Turpeenniemi-Hujanen T, Thorgeirsson UP, Rao CN, Liotta LA: Laminin increases the release of type IV collage nase from malignant cells. J Biol Chem 261: 1883–1889, 1986
Kanemoto T, Reich R, Royce L, Greatorex D, Adler SH, Shiraishi N, Martin GR, Yamada Y, Kleinman HK: Identification of an amino acid sequence from the laminin A chain that stimulates metastasis and collagenase IV production. Proc Natl Acad Sci USA 87: 2279–2283, 1990
Corcoran ML, Kibbey MC, Kleinman HK, Wahl LM: Laminin SIKVAV peptide induction of monocyte/macrophage prostaglandin E2 and matrix metalloproteinases. J Biol Chem 270: 10365–10368, 1995
Springman EB, Angleton EL, Birkedal-Hansen H, Van Wart HE: Multiple modes of activation of latent human fibroblast collagenase: evidence for the role of a Cys73 active-site zine complex in latency and a ‘cysteine switch’ mechanism for activation. Proc Natl Acad Sci USA 87: 364–368, 1990
Santavicca M, Noel A, Angliker H, Stoll I, Segain JP, Anglard P, Chretien M, Seidah N, Basset P: Characterization of structural determinants and molecular mechanisms involved in pro-stromelysin-3 activation by 4-aminophenylmercuric acetate and furin-type convertases. Biochem J 315: 953–958, 1996
Pei D, Weiss SJ: Transmembrane-deletion mutants of the membrane-type matrix metalloproteinase-1 process progelatinase A and express intrinsic matrix-degrading activity. J Biol Chem 271: 9135–9140, 1996
Cao J, Rehemtulla A, Bahou W, Zucker S: Membrane type matrix metalloproteinase 1 activates progelatinase A without furin cleavage of the N-terminal domain. J Biol Chem 271: 9135–9140, 1997
He CS, Wilhelm SM, Pentland AP, Marmer BL, Grant GA, Eisen AZ, Goldberg GI: Tissue cooperation in a proteoltyic cascade activating human interstitial collagenase. Proc Natl Acad Sci USA 86: 2632–2636, 1989
Knauper V, Will H, Lopez-Otin C, Smith B, Atkinson SJ, Stanton H, Hembry RM, Murphy G: Cellular mechanisms for human procollagenase-3 (MMP-13) activation. Evidence that MT1-MMP (MMP-14) and gelatinase a (MMP-2) are able to generate active enzyme. J Biol Chem 271: 17124–17131, 1996
Will H, Atkinson SJ, Butler GS, Smith B, Murphy G: The soluble catalytic domain of membrane type 1 matrix metalloproteinase cleaves the propeptide of progelatinase A and initiates autoproteolytic activation. Regulation by TIMP-2 and TIMP-3. J Biol Chem 271: 17119–17123, 1996
Greene J, Wang M, Liu YE, Raymond LA, Rosen C, Shi YE: Molecular cloning and characterization of human tissue inhibitor of metalloproteinase 4. J Biol Chem 271: 30375–30380, 1996
Logan SK, Garabedian MJ, Campbell CE, Werb Z: Synergistic transcriptional activation of the tissue inhibitor of metalloproteinases-1 promoter via functional interaction of AP-1 and Ets-1 transcription factors. J Biol Chem 271: 774–782, 1996
Ogata Y, Itoh Y, Nagase H: Steps involved in activation of the pro-matrix metalloproteinase 9 (progelatinase B)-tissue inhibitor of metalloproteinases-1 complex by 4-amino-phenylmercuric acetate and proteinases. J Biol Chem 270: 18506–18511, 1995
Imai K, Ohuchi E, Aoki T, Nomura H, Fujii Y, Sato H, Seiki M, Okada Y: Membrane-type matrix metalloproteinase 1 is a gelatinolytic enzyme and is secreted in a complex with tissue inhibitor of metalloproteinases 2. Cancer Res 56: 2707–2710, 1996
Strongin AY, Collier I, Bannikov G, Marmer BL, Grant GA, Goldberg GI: Mechanism of cell surface activation of 72-kDa type IV collagenase. Isolation of the activated form of the membrane metalloprotease. J Biol Chem 270: 5331–5338, 1995
Sympson CJ, Talhouk RS, Alexander CM, Chin JR, Clift SM, Bissell MJ, Werb Z: Targeted expression of stromelysin-1 in mammary gland provides evidence for a role of proteinases in branching morphogenesis and the requirement for an intact basement membrane for tissue-specific gene expression. J Cell Biol 125: 681–693, 1994
Witty JP, Wright JH, Matrisian LM: Matrix metalloproteinases are expressed during ductal and alveolar mammary morphogenesis, and misregulation of stromelysin-1 in transgenic mice induces unscheduled alveolar development. Mol Biol Cell 6: 1287–1303, 1995
Streuli CH, Schmidhauser C, Bailey N, Yurchenco P, Skubitz AP, Roskelley C, Bissell MJ: Laminin mediates tissue-specific gene expression in mammary epithelia. J Cell Biol 129: 591–603, 1995
Boudreau N, Sympson CJ, Werb Z, Bissell MJ: Suppression of ICE and apoptosis in mammary epithelial cells by extracellular matrix. Science 267: 891–893, 1995
Lefebvre O, Wolf C, Limacher JM, Hutin P, Wending C, Le Meur M, Basset P, Rio MC: The breast cancer-associated stromelysin-3 gene is expressed during mouse mammary gland apoptosis. J Cell Biol 119: 997–1002, 1992
Dickson SR, Warburton MJ: Enhanced synthesis of gelatinase and stromelysin by myoepithelial cells during involution of the rat mammary gland. J Histochem Cytochem 40: 697–703, 1992
Li F, Strange R, Friis RR, Dionov V, Altermatt HJ, Saurer S, Niemann H, Andres AC: Expression of stromelysin-1 and TIMP-1 in the involuting mammary gland and in early invasive tumors of the mouse. Int J Cancer 59: 560–568, 1994
Fukuda Y, Masuda Y, Kishi J, Hashimoto Y, Hayakawa T, Nogawa H, Nakanishi Y: The role of interstitial collagens in cleft formation of mouse embryonic submandibular gland during initial branching. Development 103: 259–267, 1988
Hayakawa T, Kishi J, Nakanishi Y: Salivary gland morphogenesis: possible involvement of collagenase. Matrix Suppl 1: 344–351, 1992
Ganser GL, Stricklin GP, Matrisian LM: EGF and TGF alpha influence in vitro lung development by the induction of matrix-degrading metalloproteinases. Int J Dev Biol 35: 453–461, 1991
Ferguson JE, Schor AM, Howell A, Ferguson MW: Changes in the extracellular matrix of the normal human breast during the menstrual cycle. Cell Tissue Res 268: 167–177, 1992
Streuli CH, Bailey N, Bissell MJ: Control of mammary epithelial differentiation: basement membrane induces tissue-specific gene expression in the absence of cell-cell interaction and morphological polarity. J Cell Biol 115: 1383–1395, 1991
Roskelley CD, Desprez PY, Bissell MJ: Extracellular matrix-dependent tissue-specific gene expression in mammary epithelial cells requires both physical and biochemical signal transduction. Proc Natl Acad Sci USA 91: 12378–12382, 1994
Feng Z, Marti A, Jehn B, Altermatt HJ, Chicaiza G, Jaggi R: Glucocorticoid and progesterone inhibit involution and programmed cell death in the mouse mammary gland. J Cell Biol 131: 1095–1103, 1995
Strange R, Li F, Saurer S, Burkhardt A, Friis RR: Apoptotic cell death and tissue remodelling during mouse mammary gland involution. Development 115: 49–58, 1992
Lund LR, Romer J, Thomasset N, Solberg H, Pyke C, Bissell MJ, Dano K, Werb Z: Two distinct phases of apoptosis in mammary gland involution: proteinase-independent and-dependent pathways. Development 122: 181–193, 1996
Talhouk RS, Bissell MJ, Werb Z: Coordinated expression of extracellular matrix-degrading proteinases and their inhibitors regulates mammary epithelial function during involution. J Cell Biol 118: 1271–1282, 1992
Alexander CM, Howard EW, Bissell MJ, Werb Z: Rescue of mammary epithelial cell apoptosis and entactin degradation by a tissue inhibitor of metalloproteinases-1 transgene. J Cell Biol 135: 1669–1677, 1996
Stetler-Stevenson WG: Dynamics of matrix turnover during pathologic remodeling of the extracellular matrix. Am J Pathol 148: 1345–1350, 1996
Sreenath T, Matrisian LM, Stetler-Stevenson W, Gattoni-Celli S, Pozzatti RO: Expression of matrix metalloproteinase genes in transformed rat cell lines of high and low metastatic potential. Cancer Res 52: 4942–4947, 1992
Hewitt R, Dano K: Stromal cell expression of components of matrix-degrading protease systems in human cancer. Enzyme Protein 49: 163–173, 1996
Heppner KJ, Matrisian LM, Jensen RA, Rodgers WH: Expression of most matrix metalloproteinase family members in breast cancer represents a tumor-induced host response. Am J Pathol 149: 273–282, 1996
Polette M, Clavel C, Cockett M, Girod de Bentzmann S, Murphy G, Birembaut P: Detection and localization of mRNAs encoding matrix metalloproteinases and their tissue inhibitor in human breast pathology. Invasion Metastasis 13: 31–37, 1993
Iwata H, Kobayashi S, Iwase H, Masaoka A, Fujimoto N, Okada Y: Production of matrix metalloproteinases and tissue inhibitors of metalloproteinases in human breast carcinomas. Jpn J Cancer Res 87: 602–611, 1996
Wolf C, Rouyer N, Lutz Y, Adida C, Loriot M, Bellocq JP, Chambon P, Basset P: Stromclysin 3 belongs to a subgroup of proteinases expressed in breast carcinoma fibroblastic cells and possibly implicated in tumor progression. Proc Natl Acad Sci USA 90: 1843–1847, 1993
Kossakowska AE, Huchcroft SA, Urbanski SJ, Edwards DR: Comparative analysis of the expression patterns of metalloproteinases and their inhibitors in breast neoplasia, sporadic colorectal neoplasia, pulmonary carcinomas and malignant non-Hodgkin's lymphomas in humans. Br J Cancer 73: 1401–1408, 1996
Chenard MP, O'Siorain L, Shering S, Rouyer N, Lutz Y, Wolf C, Basset P, Bellocq JP, Duffy MJ: High levels of stromelysin-3 correlate with poor prognosis in patients with breast carcinoma. Int J Cancer 69: 448–451, 1996
Poulsom R, Hanby AM, Pignatelli M, Jeffery RE, Longcroft JM, Rogers L, Stamp GW: Expression of gelatinase A and TIMP-2 mRNAs in desmoplastic fibroblasts in both mammary carcinomas and basal cell carcinomas of the skin. J Clin Pathol 46: 429–436, 1993
Polette M, Gilbert N, Stas I, Nawrocki B, Noel A, Remacle A, Stetler-Stevenson WG, Birembaut P, Foidart M: Gelatinase A expression and localization in human breast cancer. An in situ hybridization study and immunohistochemical detection using confocal microscopy. Virchows Arch 424: 641–645, 1994
Okada A, Bellocq JP, Rouyer N, Chenard MP, Rio MC, Chambon P, Basset P: 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: 2730–2734, 1995
Hoyhtya M, Fridman R, Komarek D, Porter-Jordan K, Stetler-Stevenson WG, Liotta LA, Liang CM: Immunohistochemical localization of matrix metalloproteinase 2 and its specific inhibitor TIMP-2 in neoplastic tissues with monoclonal antibodies. Int J Cancer 56: 500–505, 1994
Visscher DW, Hoyhtya M, Ottosen SK, Liang CM, Sarkar FH, Crissman JD, Fridman R: Enhanced expression of tissue inhibitor of metalloproteinase-2 (TIMP-2) in the stroma of breast carcinomas correlates with tumor recurrence. Int J Cancer 59: 339–344, 1994
Sato H, Takino T, Okada Y, Cao J, Shinagawa A, Yamamoto E, Seiki M: A matrix metalloproteinase expressed on the surface of invasive tumour cells. Nature 370: 61–65, 1994
Polette M, Nawrocki B, Gilles C, Sato H, Seiki M, Tournier JM, Birembaut P: MT-MMP expression and localisation in human lung and breast cancer. Virchows Arch 428: 29–35, 1996
Emonard HP, Remacle AG, Noel AC, Grimaud JA, Stetler-Stevenson WG, Foidart JM: Tumor cell surface-associated binding site for the Mr 72,000 type IV collagenase. Can Res 52: 5845–5848, 1992
Brooks PC, Stomblad S, Sanders LC, von Schalscha TL, Aimes RT, Stetler-Stevenson WG, Quigley JP, Cheresh DA: Localization of matrix metalloproteinase MMP-2 to the surface of invasive cells by interaction with integrin alpha V beta 3. Cell 85: 683–693, 1996
Yoshiji H, Gomez DE, Thorgeirsson UP, Enhanced RNA expression of tissue inhibitor of metalloproteinase-1 (TIMP-1) in human breast cancer. Int J Cancer 69: 131–134, 1996
Uria JA, Ferrando AA, Velasco G, Freije JM, Lopez-Otin C: Structure and expression in breast tumors of human TIMP-3, a new member of the metalloproteinase inhibitor family. Cancer Res 54: 2091–2094, 1994
Byrne JA, Tomasetto C, Rouyer N, Bellocq JP, Rio MC, Basset P: The tissue inhibitor of metalloproteinase-3 gene in breast carcinoma: identification of multiple polyadenylation sites and a stromal pattern of expression. Mol Med 1: 418–427, 1995
Hayakawa T, Yamashita K, Tanzawa K, Uchijima E, Iwata K: Growth-promoting activity of tissue inhibitor of metalloproteinases-1 (TIMP-1) for a wide range of cells. A possible new growth factor in serum. FEBS Lett 298: 29–32, 1992
Davies B, Miles DW, Happerfield LC, Naylor MS, Bobrow LG, Rubens RD, Balkwill FR: Activity of type UV collagenases in benign and malignant breast disease. Br J Cancer 67: 1126–1131, 1993
Azzam HS, Arand G, Lippman ME, Thompson EW: Associatino of MMP-2 activation potential with metastatic progression in human breast cancer cell lines independent of MMP-2 production. J Natl Cancer Inst 85: 1758–1764, 1993
Lee KS, Rha SY, Kim SJ, Kim JH, Roh JK, Kim BS, Chung HC: Sequential activation and production of matrix metalloproteinase-2 during breast cancer progression. Clin Exp Metastasis 14: 512–519, 1996
Ponton A, Coulombe B, Skup D: Decreased expression of tissue inhibitor of metalloproteinases in metatatic tumor cells leading to increased levels of collagenase activity. Cancer Res 51: 2138–2143, 1991
Ito A, Nakajima S, Sadaguri Y, Nagase H, Mori Y: 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: 1039–1045, 1995
Noel AC, Polette M, Lewalle JM, Munaut C, Emonard HP, Birembaut P, Foidart JM: Coordinate enhancement of gelatinase A mRNA and activity levels in human fibroblasts in response to breast-adenocarcinoma cells. Int J Cancer 56: 331–336, 1994
Polette M, Gilles C, Marchand V, Seiki M, Tournier JM, Birembaut P: Induction of membrane-type matrix metalloproteinase 1 (Mt1-Mmp) expression in human fibroblasts by breast adenocarcinoma cells. Clin Exp M 15(2): 157–163, 1997
Kataoka H, De Castro R, Zucker S, Biswas C: Tumor cell-derived collagenase-stimulatory factor increases expression of interstitial collagenase, stromelysin, and 72-kDa gelatinase. Cancer Res 53: 3154–3158, 1993
Biswas C, Zhang Y, De Castro R, Guo H, Nakamura T, Kataoka H, Nabeshima K: The human tumor cell-derived collagenase stimulatory factor (renamed LMMPRIN) is a member of the immunoglobulin superfamily. Cancer Res 55: 434–439, 1995
Biswas C: Matrix influence on the tumor cell stimulation of fibroblast collagenase production. J Cell Biochem 28: 39–45, 1985
Himelstein BP, Muschel RJ: Induction of matrix metalloproteinase 9 expression in breast carcinoma cells by a soluble factor from fibroblasts. Clin Exp Metastasis 14: 197–208, 1996
Crawford HC, Matrisian LM: Mechanisms controlling the transcription of matrix metalloproteinase genes in normal and neoplastic cells. Enzyme Protein 49: 20–37, 1996
Kaya M, Yoshida K, Higashino F, Mitaka T, Ishii S, Fujinaga K: A single ets-related transcription factor, E1AF, confers invasive phenotype on human cancer cells. Oncogene 12: 221–227, 1996
Giunciuglio D, Culty M, Fassina G, Masiello L, Melchiori A, Paglialunga G, Arand G, Ciardiello F, Basolo F, Thompson EW et al.: Invasive phenotype of MCF10A cells overexpressing c-Ha-ras and c-erbB-2 oncogenes. Int J Cancer 63: 815–822, 1995
Thompson EW, Paik S, Brunner N, Sommers CL, Zugmaier G, Clarke R, Shima TB, Torri J, Donahue S, Lippman ME, Dickson RB: Association of increased basement membrane invasiveness with absence of estrogen receptor and expression of vimentin in human breast cancer lines. J Cell Physiol 150(3): 534–544, 1992
Gilles C, Polette M, Seiki M, Birembaut P, Thompson EW: Implication of collagen type1-induced membrane-type1-matrix metalloproteinase expression and matrix metalloproteinase-2 activation in the metastatic progression of breast carcinoma. Lab Invest 76(5): 651–660, 1997
Gilles C, Polette M, Birembaut P, Brunner N, Thompson EW: Expression of c-ets-1 mRNA is associated with an invasive, EMT-derived phenotype in breast carcinoma cell lines. Clin Exp Metastasis 15: 519–526, 1997
Pulyaeva H, Bueno J, Polette M, Birembaut P, Sato H, Seiki M, Thompson EW: Mt1-Mmp correlates with Mmp-2 activation potential seen after epithelial to mesenchymal transition in human breast carcinoma cells. Clin Exp Metastasis 15(2): 111–120, 1997
Maemura M, Akiyama SK, Woods VL, Dickson RB: Expression and ligand binding of alpha 2 beta 1 integrin on breast carcinoma cells. Clin Exp Metastasis 13(4): 223–235, 1995
Dabbous MK, North SM, Haney L, Tipton DA, Nicolson GL: Effects of mast cell-macrophage interactions on the production of collagenolytic enzymes by metastatic tumor cells and tumor-derived and stromal fibroblasts. Clin Exp Metastasis 13: 33–41, 1995
Liotta LA, Steeg PS, Stetler-Stevenson WG: Cancer metastasis and angiogenesis: An imbalance of positive and negative regulation. Cell 64(2): 327–336, 1991
Wiesen JF, Werb Z: The role of stromelysin-1 in stromalepithelial interactions and cancer. Enzyme Protein 49: 174–181, 1996
Noel AC, Lefebvre O, Maquoi E, Van Hoorde L, Chenard MP, Mareel M, Foidart JM, Basset P, Rio MC: Stromelysin-3 expression promotes tumor take in nude mice. J Clin Invest 97: 1924–1930, 1996
Low JA, Johnson MD, Bone EA, Dickson RB: The matrix metalloproteinase inhibitor batimasat (BB-94) retards human breast cancer solid tumor growth but not ascites formation in nude mice. Clin Cancer Res 2: 1207–1214, 1997
Sledge Jr GW, Qulali M, Goulet R, Bone EA, Fife R: Effect of matrix metalloproteinase inhibitor batimastat on breast cancer regrowth and metastasis in athymic mice. J Natl Cancer Inst 87: 1546–1550, 1995
Eccles S, Box G, Court W, Bone E, Brown P: Control of lymphatic and hematogenous metastasis of rat mammary carcinoma by the matrix metalloproteinase inhibitor batimastat (BB-94). Cancer Res 56: 2815–2822, 1996
Taipale J, Keski-Oja J: Growth factors in the extracellular matrix. FASEB J 11: 51–59, 1997
Chandler S, Cossins J, Lury J, Wells G: Macrophage metalloelastase degrades matrix and myelin proteins and processes a tumour necrosis factor-alpha fusion protein. Biochem Biophys Res Commun 228: 421–429, 1996
Whitelock JM, Murdoch AD, Iozzo RV, Underwood PA: The degradation of human endothelial cell-derived perlecan and release of bound basic fibroblast growth factor by stromelysin, collagenase, plasmin and heparanases. J Biol Chem 271: 10079–10086, 1996
Mignatti P, Tsuboi R, Robbins E, Rifkin DB: In vitro angiogenesis on the human amniotic membrane: requirement for basic fibroblast growth factor-induced proteinases. J Cell Biol 108: 671–682, 1989
Mignatti P, Rifkin DB: Plasminogen activators and matrix metalloproteinases in angiogenesis. Enzyme Protein 49: 117–137, 1996
Benelli R, Adatia R, Ensoli B, Stetler-Stevenson WG, Santi L, Albini A: Inhibition of AIDS-Kaposi's sarcoma cell induced endothelial cell invasion by TIMP-2 and a synthetic peptide from the metalloproteinase propeptide: implications for an anti-angiogenic therapy. Oncol Res 6: 251–257, 1994
Taraboletti G, Garofalo A, Belotti D, Drudis T, Borsotti P, Scanziani E, Brown PD, Giavazzi R: Inhibition of angiogenesis and murine hemangioma growth by batimastat, a synthetic inhibitor of matrix metalloproteinases. J Natl Cancer Inst 87: 293–298, 1995
Hanemaaijer R, Koolwijk P, le Clercq L, de Vree WJ, van Hinsbergh VW: Regulation of matrix metalloproteinase expression in human vein and microvascular endothelial cells. Effects of tumour necrosis factor alpha, interleukin 1 and phorbol ester. Biochem J 296: 803–809, 1993
Monsky WL, Kelly T, Lin CY, Yeh Y, Stetler-Stevenson WG, Mueller SC, Chen WT: Binding and localization of M(r) 72,000 matrix metalloproteinase at cell surface invadopodia. Cancer Res 53: 3159–3164, 1993
Davies B, Brown PD, East N, Crimmin MJ, Balkwill FR: A synthetic matrix metalloproteinase inhibitor decreases tumor burden and prolongs survival of mice bearing human ovarian carcinoma xenografts. Cancer Res 53: 2087–2091, 1993
Chirivi RG, Garofalo A, Crimmin MJ, Bawden LJ, Stoppacciaro A, Brown PD, Giavazzi R: Inhibition of the metastatic spread and growth of B16-BL6 murine melanoma by a synthetic matrix metalloproteinase inhibitor. Int J Cancer 58: 460–464, 1994
Wang X, Fu X, Brown PD, Crimmin MJ, Hoffman RM: Matrix metalloproteinase inhibitor BB-94 (batimastat) inhibits human colon tumor growth and spread in a patient-like orthotopic model in nude mice. Cancer Res 54: 4726–4728, 1994
An Z, Wang X, Willmott N, Chander SK, Tickle S, Docherty AJ, Mountain A, Millican AT, Morphy JR, Porter JP, Epemolu O, Kubota T, Moossa AR, Hoffman RM: Conversion of highly malignant colon cancer from an aggressive to a controlled disease by oral administration of a metalloproteinase inhibitor. Clin Exp Metastasis 15: 184–195, 1997
Belloc C, Lu H, Soria C, Fridman R, Legrand Y, Menashi S: The effect of platelets on invasiveness and protease production of human mamary tumor cells. Int J Cancer 60: 413–417, 1995
Ohishi K, Fujita N, Morinaga Y, Tsuruo T: H-31 human breast cancer cells stimulate type I collagenase production in osteoblast-like cells and induce bone resorption. Clin Exp Metastasis 13: 287–295, 1995
Goldberg GI, Wilhelm SM, Kronberger A, Bauer EA, Grant GA, Eisen AZ: Human fibroblast collagenase. Complete primary structure and homology to an oncogene transformation-induced rat protein. J Biol Chem 261: 6600–6605, 1986
Knauper V, Kramer S, Reinke H, Tschesche H: Characterization and activation of procollagenase from human polymorphonuclear leucocytes. N-terminal sequence determination of the proenzyme and various proteolytically activated forms. Eur J Biochem 189: 295–300, 1990
Hasty KA, Pourmotabbed TF, Goldberg GI, Thompson JP, Spinella DG, Stevens RM, Mainardi CL: Human neutrophil collagenase. A distinct gene product with homology to other matrix metalloproteinases. J Biol Chem 265: 11421–11424, 1990
Collier IE, Wilhelm SM, Eisen AZ, Marmer BL, Grant GA, Seltzer JL, Kronberger A, He CS, Bauer EA, Goldberg GI: H-ras oncogene-transformed human bronchial epithelial cells (TBE-1) secrete a single metalloprotease capable of degrading basement membrane collagen. J Biol Chem 263: 6579–6587, 1988
Wilhelm SM, Collier IE, Marmer BL, Eisen AZ, Grant GA, Goldberg GI: SV40-transformed human lung fibroblasts secrete a 92-kDa type IV collagenase which is identical to that secreted by normal human macrophages. J Biol Chem 264: 17213–17221, 1989
Whitham SE, Murphy G, Angel P, Rahmsdorf HJ, Smith BJ, Lyons A, Harris TJ, Reynolds JJ, Herrlich P, Docherty AJ: Comparison of human stromelysin and collagenase by cloning and sequence analysis. Biochem J 240: 913–916, 1986
Muller D, Quantin B, Gesnel MC, Millon-Collard R, Abecassis J, Breathnach R: The collagenase gene family in humans consists of at least four members. Biochem J 253: 187–192, 1988
Basset P, Bellocq JP, Wolf C, Stoll I, Hutin P, Limacher JM, Podhajcer OL, Chenard MP, Rio MC, Chambon P: A novel metalloproteinase gene specifically expressed in stromal cells of breast carcinomas. Nature 348: 699–704, 1990
Shapiro SD, Kobayashi DK, Ley TJ: Cloning and characterization of a unique elastolytic metalloproteinase produced by human alveolar macrophages. J Biol Chem 268: 23824–23829, 1993
Takino T, Sato H, Yamamoto E, Seiki M: Cloning of a human gene potentially encoding a novel matrix metalloproteinase having a C-terminal transmembrane domain. Gene 155: 293–298, 1995
Takino T, Sato H, Shinagawa A, Seiki M: Identification of the second membrane-type matrix metalloproteinase (MT-MMP-2) gene from a human placenta cDNA library. MT-MMPs form a unique membrane-type subclass in the MMP family. J Biol Chem 270: 23013–23020, 1995
Will H, Hinzmann B: eDNA sequence and mRNA tissue distribution of a novel human matrix metalloproteinase with a potential transmembrane segment. Eur J Biochem 231: 602–608, 1995
Puente XS, Pendas AM, Llano E, Velasco G, Lopez-Otin C: Molecular cloning of a novel membrane-type matrix metalloproteinase from a human breast carcinoma. Cancer Res 56: 944–949, 1996
Pendas AM, Knauper V, Puente XS, Llano E, Mattei MG, Apte S, Murphy G, Lopez-Otin C: Identification and characterization of a novel human matrix metalloproteinase with unique structural characteristics, chromosomal location, and tissue distribution. J Biol Chem 272: 4281–4286, 1997
Bartlett JD, Simmer JP, Xue J, Margolis HC, Moreno EC: Molecular cloning and mRNA tissue distribution of a novel matrix metalloproteinase isolated from porcine enamel organ. Gene 183: 123–128, 1996
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Benaud, C., Dickson, R.B. & Thompson, E.W. Roles of the matrix metalloproteinases in mammary gland development and cancer. Breast Cancer Res Treat 50, 97–116 (1998). https://doi.org/10.1023/A:1006061115909
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DOI: https://doi.org/10.1023/A:1006061115909