Summary
Matrix metalloproteinase-2 (MMP-2), a zymogen requiring proteolytic activation for catalytic activity, has been implicated broadly in the invasion and metastasis of many cancer model systems, including human breast cancer (HBC). MMP-2 has been immunolocalized to carcinomatous human breast, where the degree of activation of MMP-2 correlates well with tumor grade and patient prognosis. Using Matrigel assays, we have stratified HBC cell lines for invasivenessin vitro, and compared this to their potential for metastatic spread in nude mice. HBC cell lines expressing the mesenchymal marker protein vimentin were found to be highly invasivein vitro, and tended to form metastases in nude mice. We have further discovered that culture on collagen-I gels (VitrogenTM; Vg) induces MMP-2-activator in highly invasive but not poorly invasive HBC cell lines. As seen for other MMP-2-activator inducing regimens, this induction requires protein synthesis and an intact MMP-2 hemopexin-like domain, appears to be mediated by a cell surface activity, and can be inhibited by metalloproteinase inhibitors. The induction is highly specific to collagen I, and is not seen with thin coatings of collagen I, collagen IV, laminin, or fibronectin, or with 3-dimensional gels of laminin, Matrigel, or gelatin. This review focuses on collagen I and MMP-2, their localization and source in HBC, and their relationship(s) to MMP-2 activation and HBC metastasis. The relevance of collagen I in activation of MMP-2in vivo is discussed in terms of stromal cell: tumor cell interaction for collagen I deposition, MMP-2 production, and MMP-2-activation. Such cooperativity may existin vivo for MMP-2 participation in HBC dissemination. A more complete understanding of the regulation of MMP-2-activator by type I collagen may provide new avenues for improved diagnosis and prognosis of human breast cancer.
Similar content being viewed by others
References
Schirrmacher V: Cancer metastasis: Experimental approaches, theoretical concepts and impacts for treatment strategies. Advances in Cancer Research 43: 1–73, 1985
Terranova VP, Hujanen ES, Martin GR: Basement membrane and the invasive activity of metastatic tumor cells. J Natl Cancer Inst 77: 311–316, 1986
Barsky SH, Siegal GP, Jannotta F, Liotta LA: Loss of basement membrane components by invasive tumors but not by their benign counterparts. Lab Invest 49: 140–147, 1983
Liotta LA, Rao CN, Barsky SH: Tumor invasion and the extracellular matrix. Lab Invest 49: 636–649, 1983
Barsky SH, Togo S, Garbisa S, Liotta LA: Type IV collagenase immunoreactivity in invasive breast carcinoma. Lancet 1: 296–297, 1983
Bae S-G, Arand G, Pavasant P, Azzam H, Thompson EW: Molecular and cellular analysis of basement membrane invasion by human breast cancer cells in matrigel-basedin vitro assays. Breast Cancer Research and Treatment 24: 241–255, 1993
Kleinman HK, McGarvey ML, Hassell JR, Star VL, Cannon FB, Laurie GW, Martin GR: Basement membrane complexes with biological activity. Biochem 25: 312–318, 1986
Albini A, Iwamoto Y, Kleinman HK, Martin GR, Aaronson SA, Kozlowski JM, McEwan RN: A rapidin vitro assay for quantitating the invasive potential of tumor cells. Cancer Res 47: 3239–3245, 1987
Fransden TL, Boysen BE, Jirus S, Spang-Thomsen M, Dano K, Thompson EW, Brunner N: Experimental models for the study of human cancer cell invasion and metastasis. Fibrinolysis Vol 6 Suppl 4: 71–76, 1992
Djakiew D, Pflug BR, Delsite R, Lynch JH, Arand G, Thompson EW: Chemotaxis and chemokinesis of human prostate tumor cell lines in response to human prostate stromal cell secretory proteins containing a specific nerve growth factor-like protein. Cancer Res 53: 1416–1420, 1993
Lippman ME, Dickson RB: Mechanisms of growth control in normal and malignant breast epithelium. Rec Prog Horm Res 45: 383–439, 1989
Allegra JC, Barlock A, Huff KK, Lippman ME: Changes in multiple or sequential estrogen receptor determinations in human breast cancer. Cancer 45: 792–794, 1980
Cattoretti G, Andreola S, Clemente C, D'Amato l, Rilke F: Vimentin and p53 expression on epidermal growth factor receptor-positive, oestrogen receptor-negative breast carcinomas. British Journal of Cancer 57: 353–357, 1988
Raymond WA, Leong AS-Y: Co-expression of cytokeratin and vimentin intermediate filament proteins in benign and neoplastic breast epithelium. Journal of Pathology 157: 299–306, 1989
Raymond WA, Leong AS-Y: Vimentin- A new prognostic parameter in breast carcinoma? Journal of Pathology 158: 107–114, 1989
Domagala W, Lasota J, Bartowiak J, Weber K, Osborne M: Vimentin is preferentially expressed in human breast carcinomas with low estrogen receptor and high Ki67 growth fraction. American Journal of Pathology 136: 219–227, 1990
Domagala W, Leszek W, Lasota J, Weber K, Osborne M: Vimentin is preferentially expressed in high grade ductal and medullary, but not in lobular breast carcinomas. American Journal of Pathology 137: 1059–1064, 1990
Thompson EW, Paik S, Brünner N, Sommers CL, Shima TB, Torri J, Donahue S, Lippman ME, Martin GR, Dickson RB: 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: 534–544, 1992
Sommers SL, Byers SW, Thompson EW, Torri JA, Gelmann EP: Differentiation state and invasiveness of human breast cancer cell lines. Breast Cancer Research and Treatment, 1994 (this issue) 31: 325–335
Thompson EW, Torri J, Sabol M, Sommers CL, Byers SW, Martin GR, Lippman ME, Valverius ME, Stampfer MR, Dickson RB: Oncogene-induced basement membrane invasiveness in human mammary epithelial cells. Clin Exptl Metast, in press, 1994
Sommers CL, Heckford SE, Skerker JM, Worland P, Thompson EW, Byers SW, Gelman EG: Loss of epithelial markers and acquisition of vimentin expression in adriamycin-and vinblastine resistant human breast cancer cells. Cancer Research 52: 5190–5197, 1992
Clarke R, Skaar T, Baumann K, Leonessa F, James M, Lippman J, Thompson EW, Freter C, Brunner N: Hormonal carcinogenesis in breast cancer: Cellular and molecular studies of malignant progression. Breast Cancer Research and Treatment, in press, 1994 (this issue) 31: 237–248
Oka H, Shiozaki H, Kobayashi K, Inoue M, Tahara H, Kobayashi T, Takatsuka Y, Matsuyoshi N, Hirano S, Takeichi M, Mori T: Expression of E-cadherin cell adhesion molecule in human breast cancer tissues and its relationship to metastases. Cancer Res 53: 1696–1701, 1993
Gamallo C, Palacios J, Suarez A, Pizarro A, Navarro P, Quintanilla M, Cano A: Correlation of E-cadherin expression with differentiation grade and histological type in breast carcinoma. Am J Pathol 142: 987–993, 1993
Rasbridge SA, Gillett CE, Sampson SA, Walsh FS, Millis RR: Epithelial (E-) and placental (P-) cadherin cell adhesion molecule expression in breast carcinoma. J Pathol 169: 245–250, 1993
Liotta LA, Thorgeirsson UP, Garbisa S: Role of collagenases in tumor cell invasion. Cancer Met Rev 1: 277–288, 1982
Turpeenniemi-Hujanen T, Thorgeirsson UP, Hart IR, Grant SS, Liotta LA: Expression of collagenase IV (basement membrane collagenase) activity in murine tumor cell hybrids that differ in metastatic potential. J Natl Cancer Inst 75: 99–103, 1985
Liotta LA: Tumor invasion and metastases: Role of the basement membrane. Cancer Res 46: 1–7, 1986
Nakajima M, Welch DR, Belloni PN, Nicolson GL: Degradation of basement membrane type IV collagen and lung subendothelial matrix by rat mammary adenocarcinoma cell clones of differing metastatic potentials. Cancer Res 47: 4869–4876, 1987
Garbisa S, Pozzatti R, Muschel RJ, Saffioti U, Ballin M, Goldfarb RH, Khoury G, Liotta LA: Secretion of type IV collagenolytic protease and metastatic phenotype: Induction by transfection with c-Ha-ras but not c-Ha-ras plus Ad2-E1a. Cancer Res 47: 1523–1528, 1987
Liotta LA, Steeg PS, Stetler-Stevensen WG: Cancer metastasis and angiogenesis: An imbalance of positive and negative regulation. Cell 64: 327–336, 1991
Liotta LA, Kleinerman J, Catanzara P, Rynbrandt D: Degradation of basement membrane collagen by murine tumor cells. J Natl Cancer Inst 58: 1427–1431, 1977
Collier IE, Wilhelm SM, Eisen AZ, Marmer BL, Grant GA, Seltzer JL, Kronberger A, He C, Bauer E, 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
Stetler-Stevensen WG: Type IV collagenases in tumor invasion and metastasis. Cancer Metast Rev 9: 289–303, 1990
Murphy G, Reynolds JJ, Hembry RM: Metalloproteinases and cancer invasion and metastasis. Int J Cancer 44: 757–760, 1989
Ura H, Bonfil RD, Reich R, Reddel R, Pfeifer A, Harris CC: Expression of type IV collagenase and procollagen genes and its correlation with the tumorigenic, invasive, and metastatic abilities of oncogene-transformed human bronchial epithelial cells. Cancer Res 49: 4615–4621, 1989
Greenhalgh DA, Yuspa SH: Malignant conversion of murine squamous papilloma cell lines by transfection with the fos oncogene. Molec Carcinogen 1: 134–143, 1988
Hendrix MJC, Wood WR, Seftor EA, Lotan D, Nakajima M, Misiorowski RL, Seftor REB, Stetler-Stevensen WG, Bevacqua SJ, Liotta LA, Sobel ME, Raz A, Lotan R: Retinoic acid inhibition of human melanoma cell invasion through a reconstituted basement membrane and its relation to decreases in the expression of proteolytic enzymes and motility factor receptor. Cancer Res 50: 4121–4130, 1990
Wang M, Stearns ME: Blocking of collagenase secretion by estramustine duringin vitro tumor cell invasion. Cancer Res 48: 6262–6271, 1988
Albini A, Melchiori A, Santi L, Liotta LA, Brown PD, Stetler-Stevensen WG: Tumor cell invasion inhibited by TIMP-2. J Natl Cancer Inst 83: 775–779, 1991
Hoyhtya M, Hujanen E, Turpeenniemi-Hujanen T, Thorgiersson UP, Liotta LA, Tryggvason K: Modulation of type-IV collagenase activity and invasive behavior of metastatic human melanoma (A2058) cellsin vitro by monoclonal antibodies to type IV collagenase. Int J Cancer 46: 282–286, 1990
Vartio T, Baumann M: Human gelatinase/type IV procollagenase is a regular plasma component. FEBS Letters 255: 285–289, 1989
Fernandez P, Merino M, Nogales F, Charonis AS, Stetler-Stevenson W, Liotta L: Immunohistochemical profile of basement membrane proteins and 72 kilodalton type IV collagenase in the implantation placental site. Lab Inv 66: 572–579, 1992
Monteagudo C, Merino M, San-Juan J, Liotta L, Stetler-Stevenson W: Immunohistochemical distrubiton of type IV collagenase in normal, benign, and malignant breast tissue. Am J Path 136: 585–592, 1990
Daidone MG, Silvestrini R, D'Errico A, Di Fronzo G, Benini E, Mancini AM, Garbisa S, Liotta LA, Grigioni WF: Laminin receptors, collagenase IV and prognosis in nodenegative breast cancers. Int J Cancer 48: 529–532, 1991
D'Errico A, Garbisa S, Liotta LA, Castronovo V, Stetler-Stevenson WG, Grigioni WF: Augmentation of type IV collagenase, laminin receptor, and Ki67 proliferation antigen associated with human colon, gastric, and breast carcinoma progression. Modern Pathology 4: 239–246, 1991
Höyhtya M, Fridman R, Komarek D, Porter-Jordan K, Stetler-Stevenson WG, Liotta LA, Liang C-M: Immunohistochemical localization of matrix metalloproteinase-2 and its specific inhibitor TIMD-2 in neoplastic tissues with monoclonal antibodies. Int J Cancer 56: 500–505, 1994
Tryggvason K: Type IV collagenase in invasive tumors. Breast Cancer Research and Treatment 24: 209–218, 1993
Clavel C, Polette M, Doco M, Binninger I, Birembaut P: Immunolocalization of matrix metallo-proteinases and their tissue inhibitor in human mammary pathology. Bull Cancer (Paris) 79: 261–270, 1992
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
Brown PD, Bloxidge RE, Anderson E, Howell A: Expression of activated gelatinase in human invasive breast carcinoma. Clin Exptl Metast 11: 183–189, 1993
Davies B, Miles DW, Hepperfield LC, Naylor MS, Bobrow LG, Rubens RD, Balkwill FR: Activity of type IV collagenases in benign and malignant breast disease. Br J Cancer 67: 1126–1131, 1993
Davies B, Waxman J, Wasan H, Abel P, Williams G, Krausz T, Neal D, Thomas D, Hanby A, Balkwill F: Levels of matrix metalloproteases in bladder cancer correlate with tumor grade and invasion. Cancer Res 53: 5365–5369, 1993
Campo E, Merino M, Tavassoli F, Charonis A, Stetler-Stevenson WG, Liotta LA: Evaluation of basement membrane components and the 72 kDa type IV collagenase in serous tumors of the ovary. Am J Surg Path 16: 500–507, 1992
Stearns ME, Wang M: Type IV collagenase (Mr 72,000) expression in human prostate: Benign and malignant tissue. Cancer Res 53: 878–883, 1993
Levy A, Cioce V, Sobel M, Garbisa S, Grigioni WF, Liotta LA: Increased expression of the Mr 72,000 type IV collagenase in human colonic adenocarcinoma. Cancer Res 51: 439–444, 1991
Garbisa S, Scagliotti G, Masiero L, Di Francesco C, Caenasso C, Onisto M, Micela M, Stetler-Stevenson WG, Liotta LA: Correlation of serum metalloproteinase levels with lung cancer metastasis and response to therapy. Cancer Res 52: 4548–4549, 1992
Pyke S, Ralfkiaer E, Huhtala P, Hurskainen T, Dano K, Tryggvason K: Localization of messenger RNA for Mr 72,000 and 92,000 type IV collagenases in human skin cancers byin situ hybridization. Cancer Res 52: 1336–1341, 1993
Polette M, Clavel Ch, Cockett M, Girod de Bentzmann S, Murphy G, Birembaut Ph: Detection and localization of mRNA's encoding matrix metalloproteinases and their tissue inhibitor in human breast pathology. Invasion Metastasis 13: 31–37, 1993
Emonard HP, Remacle AG, Noel AC, Grimaud J-A, Stetler-Stevenson WG, Foidart J-M: Tumor cell surface-associated binding site for the Mr 72,000 type IV collagenase. Cancer Res 52: 5845–5848, 1992
Monsky WL, Kelly T, Lin C-Y, Yeh Y, Stetler-Stevenson WG, Mueller SC, Chen W-T: Binding and localization of Mr 72,000 matrix metalloproteinase at cell surface invadopodia. Cancer Res 53: 3159–3164, 1993
Springman EB, Angleton EL, Birkedahl-Hansen H, Van Wart HE: Multiple modes of activation of latent human fibroblast collagenase. Evidence for the role of a cys-73 active site zinc complex in latency and a cysteine switch mechanism for activation. Proc Natl Acad Sci 87: 364–368, 1990
Stetler-Stevenson W, Krutzsch HC, Wacher M, Margulies IMK, Liotta LA: The activation of human type IV collagenase proenzyme: Sequence identification of the major conversion product following organomercurial activation. J Biol Chem 264: 1353–1356, 1989
Brown PD, Levy AT, Margulies IM, Liotta LA, Stetler-Stevensen WG: Independent expression and cellular processing of Mr 72,000 type IV collagenase and interstitial collagenase in human tumorigenic cell lines. Cancer Res 50: 6184–6191, 1990
Overall CM, Sodek J: Concanavalin A produces a matrixdegradative phenotype in human fibroblasts. J Biol Chem 265: 21141–21151, 1990
Ward RV, Atkinson SJ, Slocombe PM, Docherty AJP, Reynolds JJ, Murphy G: Tissue inhibitor of metalloproteinases-2 inhibits the activation of 72 kDa progelatinase by fibroblast membranes. Biochim Biophys Acta 1079: 242–246, 1991
Azzam HS, Thompson EW: Collagen-induced activation of the 72 kDa type IV collagenase in human fibroblasts and a carcinosarcoma-derived human breast cancer cell line. Cancer Res 52: 4540–4544, 1992
Azzam HS, Arand GA, Lippman ME, Thompson EW: MMP-2 activation potential associates with metastatic progression in human breast cancer cell lines, and is independent of MMP-2 production. J Natl Cancer Inst 85: 1758–1764, 1993
Brown PD, Kleiner DE, Unsworth EJ, Stetler-Stevenson WG: Cellular activation of the 72 kDa type IV procollagenase / TIMP-2 complex. Kidney Int 43: 163–170, 1993
Murphy G, Willenbrock F, Ward RV, Cockett MI, Eaton D, Docherty AJ: 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. Bioch J 283: 637–641, 1992
Strongin AY, Marmer BL, Grant GA, Goldberg GI: Plasma membrane dependent activation of the 72 kDa type IV collagenase is prevented by complex formation with TIMP-2. J Biol Chem 268: 14033–14039, 1993
Azzam HS, Bae S-N, Arand G, Yoon J, Kern FX, Stetler-Stevenson WG, Thompson EW: The hemopexin-like domain is required for collagen-induced activation of matrix metalloproteinase-2 by human breast cancer cell lines. Annual Meeting of the American Association for Cancer Research, 1994
Hay ED: Cell Biology of the Extracellular Matrix. 2nd Edition. New York: Plenum Press, 1991
Alberts B, Bray D, Lewis J, Raff M, Roberts K, Watson J: Molecular Biology of the Cell. 2nd ed. New York: Garland Pub, Inc: 802–815, 1989
Page D, Anderson T: Diagnostic Histopathology of the Breast. Edinburgh: Churchill Livingstone, pp 4–10, 89–103, 193–236, 1987
Martinez-Hernandez A, Francis D, Silverberg S: Elastosis and other stromal reactions in benign and malignant breast tissue. Cancer 40: 700–706, 1977
Barsky S, Green W, Grotendorst G, Liotta L: Desmoplastic breast carcinoma as a source of human myofibroblasts. Am J Pathol 115: 329–333, 1984
Barsky S, Gopalakrishna R: Increased invasion and the spontaneous metastasis of BL6 melanoma with inhibition of the desmoplastic response in C57 BL/6 mice. Cancer Res 47: 1663–1667, 1987
Mahfouz S, Chevallier M, Grimaud J: Distribution of the major connective matrix components of the stromal reaction in breast carcinoma. Cell Mol Biol 33: 453–467, 1987
Pages A, Foidart JM, Gordenne W: Localisation des collagenes de types I, III, IV et de la fibronectine dans les tumours benignes et les epitheliomas de la glande mammaire humanie. J Gynecol Obstet Biol Reprod 1: 34–50, 1984
Deak S, Galaug M, Pierce Ret al.: Desmoplasia in benign and malignant breast disease is characterized by alterations in level of mRNAs coding for type I and III procollagen. Matrix 11: 252–258, 1991
Gan YB. Expression of type I and type III procollagen genes in human scirrhous carcinoma of breast byin situ hybridization. Chung Hua Chung Liu Tsa Chih 14: 348–350, 1992
Clavel C, Doco M, Lallemand A, Laurent M, Birembaut P: Detection byin situ hybridization of messenger RNAs of collagen types I and IV in murine mammary cancer. Int J Cancer 44: 548–553, 1989
Vaage J, harlos JP: Collagen production by macrophages in tumour encapsulation and dormancy. Br J Cancer 63: 758–762, 1991
Kao R, Hal J, Stern R: Collagen and elastin synthesis in human stroma and breast carcinoma cell lines: modulation by the extracellular matrix. Connective Tissue Res 14: 245–255, 1986
Svoboda KK: Intracellular localization of types I and II collagen mRNA and endoplasmic reticulum in embryonic corneal epithelia. J Cell Sci 100: 23–33, 1991
Pucci Minafra I, Luparello C, Sciarrino S, Tomasino RM, Minafra S: Quantitative determination of collagen types present in the ductal infiltrating carcinoma of human mammary gland. Cell Biol Int Rep 9: 291–296, 1985
Minafra S, Minafra IP, Tomasino RM, Sciarrino S: Collagen composition in the ductal infiltrating carcinoma of human breast. Cell Biol Int Rep 8: 79–85, 1984
Minafra S, Luparello C, Rallo F, Pucci-Minafra I: Collagen biosynthesis by a breast carcinoma cell strain and biopsy fragments of the primary tumour. Cell Biol Int Rep 12: 895–905, 1988
Pucci-Minafra I, Luparello C, Andriolo M, Basirico L, Aquino A, Minafra S: A new form of tumor and fetal collagen that binds laminin. Biochem 32: 7421–7427, 1993
Luparello C, Sheterline P, Pucci-Minafra I, Minafra S: A comparison of spreading and motility behaviour of 8701-BC breast carcinoma cells on type I, I-trimer and type V collagen substrata. Evidence for a permissive effect of type I-trimer collagen on cell locomotion. J Cell Sci 100: 179–185, 1991
Jones W, Lee AE, Riddle P, Dils RR, Hallowes RC: Phenotypic responses of mouse mammary tumours and normal mammary epithelium cultured in collagen gels: Correlation with tumour type and progression. Tissue Cell 24: 879–894, 1992
Cullen KJ, Lippman ME: Stromal-epithelial interactions in breast cancer. In: Dickson RB, Lippman ME (eds) Genes, Oncogenes, and Hormones: Advances in Cellular and Molecular Biology of Breast Cancer. Kluwer Academic Publishers, Boston, 1991, pp 413–431
Sakakura T: New aspects of stroma-parenchyma relations in mammary gland differentiation. Int Rev Cytol 125: 165–202, 1991
Vande Berg J, Rudolph R, Woodward M: Growth dynamics of cultured myofibroblasts from human breast cancer and non malignant contracting tissues. Plastic and Recon Surg 73: 605–616, 1984
Sappino AP, Schurch W, Gabbiani G: Differentiation repertoire of fibroblastic cells: Expression of cytoskeletal proteins as marker of phenotypic modulation. Lab Invest 63: 144–161, 1990
Rinnov-Jessen L, Van Deurs B, Celis JE, Peterson OW: Smooth muscle differentiation in cultured human breast gland stromal cells. Lab Invest 63: 532–543, 1990
Schor SL, Schor AM, Durning P, Rushton G: Skin fibroblasts obtained from cancer patients display foetal-like migratory behaviour on collagen gels. J Cell Sci 73: 235–244, 1985
Schor SL, Schor AM, Howell A, Crowther D: Hypothesis: Persistent expression of fetal phenotypic characteristics by fibroblasts is associated with an increased susceptibility to neoplastic disease. Exp Cell Biol 55: 11–17, 1987
Cullen KJ, Smith HS, Hill S, Rosen N, Lippman ME: Growth factor messenger RNA expression by human breast fibroblasts from benign and malignant tissues. Cancer Res 51: 4978–4985, 1991
Ohtani H, Sasano N: Stromal cell changes in human colorectal adenomas and carcinomas: an ultrastructural study of fibroblasts, myofibroblasts and smooth muscle cells Virchows Arch [A] 401: 209, 1983
Ohtani H, Kuroiw A, Obinata M, Ooshima A, Nagura H: Identification of type I collagen producing cells in human gastrointestinal carcinomas by non-radioactivein situ hybridization and immunoelectron microscopy. J Histochem Cytochem 40: 1139–1146, 1992
Noël A, Munaut C, Boulvain A, Calberg-Bacq CM, Lambert CA, Nusgens B, Lapiere CM, Foidart JM: Modulation of collagen and fibronectin synthese in fibroblasts by normal and malignant cells 48: 150–161, 1992
Noël A, Munaut C, Nusgens B, Foidart JM, Lapiere CM: The stimulation of fibroblasts collagen synthesis by neoplastic cell is modulated by the extracellular matrix. Matrix 12: 213–220, 1992
Noël A, Munaut C, Nusgens B, Lapière CM, Fordart JM: Different mechanisms of extracellular matrix remodeling by fibroblasts in response to human mammary neoplastic cells. Invasion and Metastasis 13: 72–81, 1993
Frey J, Rattner A, Chamson A: Synthese et organisation supramoleculaire de composants de la matrice extracellulaire par des fibroblastes cultivés dans une trame de collagene. Pathol Biol (Paris) 40: 859–864, 1992
Saito K, Shimizu F, Sato T, Oite T: Modulation of human mesangial cell behaviour by extracellular matrix components-the possible role of interstitial type III collagen. Clin Exp Immunol 91: 510–515, 1993
Galfi P, Gabel G, Martens H: Influences of extracellular matrix components on the growth and differentiation of ruminal epithelial cells in primary culture. Res Vet Sci 54: 102–109, 1993
Yamamoto K, Yamamoto M, Noumura N: Disassembly of F-actin filaments in human endothelial cells cultured on type V collagen. Exp Cell Res 20: 55–63, 1992
Davis GE: Affinity of integrins for damaged extracellular matrix: alpha v beta 3 binds to denatured collagen type I through RGD sites. Biochem Biophys Res Commun 182: 1025–1031, 1992
Sipes JM, Guo N, Negre E, Vogel T, Krutzsch HC, Roberts DD: Inhibition of fibronectin binding and fibronectin-mediated cell adhesion to collagen by a peptide from the second type I repeat of thrombospondin. J Cell Biol 121: 469–477, 1993
Ezoe K, Horikoshi T: Tumor necrosis factor-alpha increased the integrin alpha 2 beta 1 expression and cell attachment to type I collagen in human dermal fibroblasts. Biochem Biophys Res Commun 192: 281–287, 1993
Monboisse JC, Garnotel R, Randoux A, Dufer J, Borel JP: Adhesion of human neutrophils to and activation by type-I collagen involving a beta 2 integrin. J Leukoc Biol 50: 373–380, 1991
Borel JP, Bellon G, Garnotel R, Monboisse JC: Adhesion and activation of human neutrophils on basement membrane molecules. Kidney Int 43: 26–29, 1993
Carri NG, Rubin K, Gullberg D, Ebendal T: Neuritogenesis on collagen substrates. Involvement of integrin-like matrix receptor in retinal fibre outgrowth on collagen. Int J Dev Neurosci 10: 393–405, 1992
Berdichevsky F, Gilbert C, Shearer M, Taylor-Papadimitriou J: Collagen-induced rapid morphogenesis of human mammary epithelial cells: the role of the alpha 2 beta 1 integrin. J Cell Sci 102: 437–446, 1992
Schiro JA, Chan BM, Roswit WT, Kassner PD, Pentland AP, Hemler ME, Eisen AZ, Kupper TS: Integrin alpha 2 beta 1 (VLA-2) mediated reorganization and contraction of collagen matrices by human cells. Cell 67: 403–410, 1991
Grzesiak JJ, Davis GE, Kirchhofer D, Pierschbacher MD: Regulation of alpha 2 beta 1-mediated fibroblast migration on type I collagen by shifts in the concentrations of extracellular Mg2+ and Ca2+. J Cell Biol 117: 1109–1117, 1992
Scharffetter-Kochanek K, Klein CE, Heinen G, Mauch C, Schaefer T, Adelmann-Grill BC, Goerz G, Fusenig NE, Krieg TM, Plewig G: Migration of a human keratinocyte cell line (HACAT) to interstitial collagen type I is mediated by the alpha 2 beta 1-integrin receptor. J Invest Dermatol 98: 3–11, 1992
Leavesley DI, Schwartz MA, Rosenfeld M, Cheresh DA: Integrin beta 1- and beta 3-mediated endothelial cell migration is triggered through distinct signaling mechanisms. J Cell Biol 121: 163–170, 1993
Myers JC: Differential expression of type I collagen and cellular fibronectin isoforms in endothelial cell variants. Kidney Int 43: 45–52, 1993
Hirai K, Shimada H, Ogawa T, Taji S: The spread of human lung cancer cells on collagens and its inhibition by type III collagen. Clin Exp Metastasis 9: 517–527, 1991
Jackson CJ, Jenkins K, Schrieber L: Possible mechanisms of type I collagen-induced vascular tube formation. EXS 61: 198–204, 1992
Monboisse JC, Garnotel R, Bellon G, Borel JP: Activation of polymorphonuclear neutrophils by contact with collagen I and degradation of collagen. C R Seances Soc Biol Fil 185: 164–170, 1991
Shapiro SD, Kobayashi DK, Pentland AP, Welgus HG: Induction of macrophage metalloproteinases by extracellular matrix. Evidence for enzyme- and substrate-specific responses involving prostaglandin-dependent mechanisms. J Biol Chem 268: 8170–8175, 1993
Seftor RE, Seftor EA, Stetler-Stevenson WG, Hendrix MJ: The 72 kDa type IV collagenase is modulated via differential expression of alpha v beta 3 and alpha 5 beta 1 integrins during human melanoma cell invasion. Cancer Res 53: 3411–3415, 1993
Sarret Y, Woodley DT, Goldberg GS, Kronberger A, Wynn KC: Constitutive synthesis of a 92-kDa keratinocyte-derived type IV collagenase is enhanced by type I collagen and decreased by type IV collagen matrices. J Invest Dermatol 99: 836–841, 1992
Seftor RE, Seftor EA, Gehlsen KR, Stetler-Stevenson WG, Brown PD, Ruoslahti E, Hendrix MJ: Role of the alpha v beta 3 integrin in human melanoma cell invasion. Proc Natl Acad Sci USA 89: 1557–1561, 1992
Gehlsen KR, Davis GE, Sriramarao P: Integrin expression in human melanoma cells with differing invasive and metastatic properties. Clin Exp Metastasis 10: 111–120, 1992
Albelda SM, Buck CA: Integrins and other cell adhesion molecules. FASEB J 4: 2868–2880, 1990
Gullberg D, Turner DC, Borg TK, Terracio L, Rubin K: Different beta 1-integrin collagen receptors on rat hepatocytes and cardiac fibroblasts. Exp Cell Res 190: 254–264, 1990
Gullberg D, Gehlsen KR, Turner DC, Ahlen K, Zijenah LS, Barnes MJ, Rubin K: Analysis of alpha 1 beta 1, alpha 2 beta 1 and alpha 3 beta 1 integrins in cell-collagen interactions: identification of conformation dependent alpha 1 beta 1 binding sites in collagen type I. EMBO J 11: 3865–3873, 1992
Elices MJ, Urry LA, Hemler ME: Receptor functions for the integrin VLA-3: fibronectin, collagen, and laminin binding are differentially influenced by Arg-Gly-Asp peptide and by divalent cations. J Cell Biol 112: 169–181, 1991
Adler S: Characterization of glomerular epithelial cell matrix receptors. Am J Pathol 141: 571–578, 1992
Pignatelli M, Liu D, Nasim MM, Stamp GW, Hirano S, Takeichi M: Morphoregulatory activities of E-cadherin and beta-1 integrins in colorectal tumour cells. Br J Cancer 66: 629–634, 1992
Dedhar S, Gray V: Isolation of a novel integrin receptor mediating Arg-Gly-Asp-directed cell adhesion to fibronectin and type I collagen from human neuroblastoma cells. Association of a novel beta 1-related subunit with alpha v. J Cell Biol 110: 2185–2193, 1990
Staatz WD, Fok KF, Zutter MM, Adams SP, Rodriguez BA, Santoro SA: Identification of a tetrapeptide recognition sequence for the alpha 2 beta 1 integrin in collagen. J Biol Chem 266: 7363–7367, 1991
Staatz WD, Walsh JJ, Pexton T, Santoro SA: The alpha 2 beta 1 integrin cell surface collagen receptor binds to the alpha 1 (I)-CB3 peptide of collagen. J Biol Chem 265: 4778–4781, 1990
Schwartz MA: Signalling by integrins: Implications for tumorigenesis. Cancer Res 53: 1503–1506, 1993
Juliano RL, Haskill S: Signal transduction from the extracellular matrix. J Cell Biol 120: 577–585, 1993
Cybulsky AV, Carbonetto S, Cyr MD, McTavish AJ, Huang Q: Extracellular matrix-stimulated phospholipase activation is mediated by beta 1-integrin. Am J Physiol 264: C323–332, 1993
Bauer J, Margolis M, Schreiner C, Edgell CJ, Azizkhan J, Lazarowski E, Juliano RL:In vitro model of angiogenesis using a human endothelium-derived permanent cell line: contributions of induced gene expression G-proteins, and integrins. J Cell Physiol 153: 437–449, 1992
Ikeda K, Michelangeli VP, Martin TJ, Findlay DM: Type I collagen substrate increases calcitonin and parathyroid hormone receptor-mediated signal transduction in UMR 106-06 osteoblast-like cells. J Cell Physiol 156: 130–137, 1993
Schwartz MA, Ingber DE, Lawrence M, Springer TA, Lechene C: Multiple integrins share the ability to induce elevation of intracellular pH. Exp Cell Res 195: 533–535, 1991
Lester BR, McCarthy JB, Sun ZQ, Smith RS, Furcht LT, Spiegel AM: G-protein involvement in matrix-mediated motility and invasion of high and low experimental metastatic B16 melanoma clones. Cancer Res 49: 5940–5948, 1989
Lester BR, McCarthy JB: Tumor cell adhesion to the extracellular matrix and signal transduction mechanisms implicated in tumor cell motility, invasion and metastasis. Cancer and Metastasis Reviews 11: 31–44, 1992
Yohem KH, Clothier JL, Montague SL, Geary RJ, Winters AL, Hendrix MJ, Welch DR: Inhibition of tumor cell invasion by verapamil. Pigment Cell Res (Denmark) 4: 225–233, 1991
Davies BR, Davies MP, Gibbs FE, Barraclough R, Rudland PS: Induction of the metastatic phenotype by transfection of a benign rat mammary epithelial cell line with the gene for p9Ka, a rat calcium-binding protein, but not with the oncogene EJ-ras-1. Oncogene 8: 999–1008, 1993
Chambers AF: Ras-responsive genes and tumor metastasis. Crit Rev Oncog 4: 95–114, 1993
Barbero MC, Garcia M, Almena A, Alino SF: Correlation between secretion pattern and metastatic potential from drug-treated 3LL tumor cell line. Cell Mol Biol 37: 501–508, 1991
Parker C, Sherbet GV: Modulators of intracellular Ca2+ and the calmodulin inhibitor W-7 alter the expression of metastasis-associated genes MTS1 and NM23 in metastatic variants of the B16 murine melanoma. Melanoma Res 2: 337–343, 1992
Korczak B, Whale C, Kerbel RS: Possible involvement of Ca2+ mobilization and protein kinase C activation in the induction of spontaneous metastasis by mouse adenocarcinoma cells. Cancer Research 49: 2597–2602, 1989
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Thompson, E.W., Yu, M., Bueno, J. et al. Collagen induced MMP-2 activation in human breast cancer. Breast Cancer Res Tr 31, 357–370 (1994). https://doi.org/10.1007/BF00666168
Issue Date:
DOI: https://doi.org/10.1007/BF00666168