Abstract
A predominant characteristic of metastatic cells is the ability to invade host tissues and establish distant metastatic foci. Release of metastatic cells from a primary tumor results from disruption of tissue architecture and requires reversible modulation of cell-matrix and cell-cell contacts, cytoskeletal rearrangement, and acquisition of enhanced proteolytic potential. Malignant cells produce a spectrum of extracellular proteinases including matrix metalloproteinases (MMPs) that process extracellular matrix components, cell surface proteins, and immune modulators. Dysregulated proteolysis has been implicated in tumor invasion and metastasis in multiple model systems. This review will focus on data that highlight the influence of cell-matrix and cell-cell interactions and their associated signal transduction pathways on proteinase regulation. These data highlight cell adhesion signaling as a mechanism for a versatile cellular proteolytic response to changing microenvironmental cues.
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Lynch CC, Matrisian LM: Matrix metalloproteinases in tumor-host cell communication. Differentiation 70: 561–573, 2002
DeClerck YA, Mercurio AM, Stack MS, Chapman HA, Zutter MM, Muschel RJ, Raz A, Matrisian LM, Sloane BF, Noel A, Hendrix MJ, Coussens L, Padarathsingh M: Proteases, extracellular matrix, and cancer: A workshop of the path B study section. Am J Pathol 164: 1131–1139, 2004
Sternlicht MD, Werb Z: How matrix metalloproteinases regulate cell behavior. Annu Rev Cell Dev Biol 17: 463–516, 2001
Overall CM, Lopez-Otin C: Strategies for MMP inhibition in cancer: Innovations for the post-trial era. Nat Rev Cancer 2: 657–672, 2002
Wolf, K, Mazo, I, Leung, H, Engelke, K, von Andrian UH, Deryugina EI, Strongin AY, Brocker EB, Friedl P: Compensation mechanism in tumor cell migration: mesenchymal-amoeboid transition after blocking of pericellular proteolysis. J Cell Biol 160: 267–277, 2003
Hotary KB, Allen ED, Brooks PC, Datta NS, Long MW, Weiss SJ: Membrane type I matrix metalloproteinase usurps tumor growth control imposed by the three-dimensional extracellular matrix. Cell 114: 33–45, 2003
Westermarck J, Kahari VM: Regulation of matrix metalloproteinase expression in tumor invasion. Faseb J 13: 781–792, 1999
Vincenti MP, Brinckerhoff CE: Transcriptional regulation of collagenase (MMP-1, MMP-13) genes in arthritis: Integration of complex signaling pathways for the recruitment of gene-specific transcription factors. Arthritis Res 4: 157–164, 2002
Yamada KM, Miyamoto S: Integrin transmembrane signaling and cytoskeletal control. Curr Opin Cell Biol 7: 681–689, 1995
Schwartz MA, Ingber DE: Integrating with integrins. Mol Biol Cell 5: 389–393, 1994
Martin, KH, Slack JK, Boerner SA, Martin CC, Parsons JT: Integrin connections map: To infinity and beyond. Science 296: 1652–1653, 2002
Moro L, Venturino M, Bozzo C, Silengo L, Altruda F, Beguinot L, Tarone G, Defilippi P: Integrins induce activation of EGF receptor: Role in MAP kinase induction and adhesion-dependent cell survival. Embo J 17: 6622–6632, 1998
Mariotti A, Kedeshian PA, Dans M, Curatola AM, Gagnoux-Palacios L, Giancotti FG: EGF-R signaling through Fyn kinase disrupts the function of integrin alpha6beta4 at hemidesmosomes: role in epithelial cell migration and carcinoma invasion. J Cell Biol 155: 447–458, 2001
Deugnier MA, Faraldo MM, Rousselle P, Thiery JP, Glukhova MA: Cell-extracellular matrix interactions and EGF are important regulators of the basal mammary epithelial cell phenotype. J Cell Sci 112(Pt 7): 1035–1044, 1999
Moro L, Dolce L, Cabodi S, Bergatto E, Erba EB, Smeriglio M, Turco E, Retta SF, Giuffrida MG, Venturino M, Godovac-Zimmermann J, Conti A, Schaefer E, Beguinot L, Tacchetti C, Gaggini P, Silengo L, Tarone G, Defilippi P: Integrin-induced epidermal growth factor (EGF) receptor activation requires c-Src and p130Cas and leads to phosphorylation of specific EGF receptor tyrosines. J Biol Chem 277: 9405–9414, 2002
Miyamoto S, Teramoto H, Coso OA, Gutkind JS, Burbelo PD, Akiyama SK, Yamada KM: Integrin function: Molecular hierarchies of cytoskeletal and signaling molecules. J Cell Biol 131: 791–805, 1995
Miyamoto S, Akiyama SK, Yamada KM: Synergistic roles for receptor occupancy and aggregation in integrin transmembrane function. Science 267: 883–885, 1995
Ingber DE: Cancer as a disease of epithelial-mesenchymal interactions and extracellular matrix regulation. Differentiation 70: 547–560, 2002
Ingber DE: Tensegrity II. How structural networks influence cellular information processing networks. J Cell Sci 116: 1397–1408, 2003
Bershadsky, AD, Balaban, NQ, Geiger, B: Adhesion-dependent cell mechanosensitivity. Annu Rev Cell Dev Biol 19: 677–695, 2003
Katsumi, A, Orr, AW, Tzima, E, Schwartz MA: Integrins in mechanotransduction. J Biol Chem 279: 12001–12004, 2004
Pollanen, J, Hedman, K, Nielsen, LS, Dano, K, Vaheri A: Ultrastructural localization of plasma membrane-associated urokinase-type plasminogen activator at focal contacts. J Cell Biol 106: 87–5, 1988
Aggeler J, Frisch SM, Werb Z: Changes in cell shape correlate with collagenase gene expression in rabbit synovial fibroblasts. J Cell Biol 98: 1662–1671, 1984
Werb Z, Hembry RM, Murphy G, Aggeler J: Commitment to expression of the metalloendopeptidases, collagenase and stromelysin: Relationship of inducing events to changes in cytoskeletal architecture. J Cell Biol 102: 697–702, 1986
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
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
Terranova VP, Williams JE, Liotta LA, Martin GR: Modulation of the metastatic activity of melanoma cells by laminin and fibronectin. Science 226: 982–985, 1984
Turpeenniemi-Hujanen T, Thorgeirsson UP, Rao CN, Liotta LA: Laminin increases the release of type IV collagenase 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
Stack S, Gray RD, Pizzo SV: Modulation of plasminogen activation and type IV collagenase activity by a synthetic peptide derived from the laminin A chain. Biochemistry 30: 2073–2077, 1991
Jia Y, Zeng ZZ, Markwart SM, Rockwood KF, Ignatoski KM, Ethier SP, Livant DL: Integrin fibronectin receptors in matrix metalloproteinase-1-dependent invasion by breast cancer and mammary epithelial cells. Cancer Res 64: 8674–8681, 2004
Iyer V, Pumiglia K, DiPersio CM: Alpha3beta1 integrin regulates MMP-9 mRNA stability in immortalized keratinocytes: A novel mechanism of integrin-mediated MMP gene expression. J Cell Sci 118: 1185–1195, 2005
Lauer JL, Gendron CM, Fields GB: Effect of ligand conformation on melanoma cell alpha3beta1 integrin-mediated signal transduction events: Implications for a collagen structural modulation mechanism of tumor cell invasion. Biochemistry 37: 5279–5287, 1998
Baronas-Lowell D, Lauer-Fields JL, Borgia JA, Sferrazza GF, Al-Ghoul M, Minond D, Fields GB: Differential modulation of human melanoma cell metalloproteinase expression by alpha2beta1 integrin and CD44 triple-helical ligands derived from type IV collagen. J Biol Chem 279: 43503–43513, 2004
Azzam HS, Thompson EW: Collagen-induced activation of the M(r) 72,000 type IV collagenase in normal and malignant human fibroblastoid cells. Cancer Res 52: 4540–4544, 1992
Gilles C, Polette M, Seiki M, Birembaut P, Thompson EW: Implication of collagen type I-induced membrane-type 1-matrix metalloproteinase expression and matrix metalloproteinase-2 activation in the metastatic progression of breast carcinoma. Lab Invest 76: 651–660, 1997
Ellerbroek SM, Wu YI, Overall CM, Stack MS: Functional interplay between type I collagen and cell surface matrix metalloproteinase activity. J Biol Chem 276: 24833–24842, 2001
Ellerbroek SM, Fishman DA, Kearns AS, Bafetti LM, Stack MS: Ovarian carcinoma regulation of matrix metalloproteinase-2 and membrane type 1 matrix metalloproteinase through beta1 integrin. Cancer Res 59: 1635–1641, 1999
Galvez BG, Matias-Roman S, Yanez-Mo M, Sanchez-Madrid F, Arroyo AG: ECM regulates MT1-MMP localization with beta1 or alphavbeta3 integrins at distinct cell compartments modulating its internalization and activity on human endothelial cells. J Cell Biol 159: 509–521, 2002
Deryugina EI, Ratnikov BI, Postnova TI, Rozanov DV, Strongin AY: Processing of integrin alpha(v) subunit by membrane type 1 matrix metalloproteinase stimulates migration of breast carcinoma cells on vitronectin and enhances tyrosine phosphorylation of focal adhesion kinase. J Biol Chem 277: 9749–9756, 2002
Baciu PC, Suleiman EA, Deryugina EI, Strongin AY: Membrane type-1 matrix metalloproteinase (MT1-MMP) processing of pro-alphav integrin regulates cross-talk between alphavbeta3 and alpha2beta1 integrins in breast carcinoma cells. Exp Cell Res 291: 167–175, 2003
Dumin JA, Dickeson SK, Stricker TP, Bhattacharyya-Pakrasi M, Roby JD, Santoro SA, Parks WC: Pro-collagenase-1 (matrix metalloproteinase-1) binds the alpha(2)beta(1) integrin upon release from keratinocytes migrating on type I collagen. J Biol Chem 276: 29368–29374, 2001
Bafetti LM, Young TN, Itoh Y, Stack MS: Intact vitronectin induces matrix metalloproteinase-2 and tissue inhibitor of metalloproteinases-2 expression and enhanced cellular invasion by melanoma cells. J Biol Chem 273: 143–149, 1998
Nisato RE, Hosseini G, Sirrenberg C, Butler GS, Crabbe T, Docherty AJ, Wiesner M, Murphy G, Overall CM, Goodman SL, Pepper MS: Dissecting the role of matrix metalloproteinases (MMP) and integrin alpha(v)beta3 in angiogenesis in vitro: Absence of hemopexin C domain bioactivity, but membrane-Type 1-MMP and alpha(v)beta3 are critical. Cancer Res 65: 9377–9387, 2005
Steffensen B, Bigg HF, Overall CM: The involvement of the fibronectin type II-like modules of human gelatinase A in cell surface localization and activation. J Biol Chem 273: 20622–20628, 1998
Tam EM, Wu YI, Butler GS, Stack MS, Overall CM: Collagen binding properties of the membrane type-1 matrix metalloproteinase (MT1-MMP) hemopexin C domain. The ectodomain of the 44-kDa autocatalytic product of MT1-MMP inhibits cell invasion by disrupting native type I collagen cleavage. J Biol Chem 277: 39005–39014, 2002
Itoh Y, Takamura A, Ito N, Maru Y, Sato H, Suenaga N, Aoki T, Seiki M: Homophilic complex formation of MT1-MMP facilitates proMMP-2 activation on the cell surface and promotes tumor cell invasion. Embo J 20: 4782–4793, 2001
Lehti K, Lohi J, Juntunen MM, Pei D, Keski-Oja J: Oligomerization through hemopexin and cytoplasmic domains regulates the activity and turnover of membrane-type 1 matrix metalloproteinase. J Biol Chem 277: 8440–8448, 2002
Nonaka T, Nishibashi K, Itoh Y, Yana I, Seiki M: Competitive disruption of the tumor-promoting function of membrane type 1 matrix metalloproteinase/matrix metalloproteinase-14 in vivo. Mol Cancer Ther 4: 1157–1166, 2005
Jiang A, Lehti K, Wang X, Weiss SJ, Keski-Oja J, Pei D: Regulation of membrane-type matrix metalloproteinase 1 activity by dynamin-mediated endocytosis. Proc Natl Acad Sci USA 98: 13693–13698, 2001
Rozanov DV, Deryugina EI, Monosov EZ, Marchenko ND, Strongin AY: Aberrant, persistent inclusion into lipid rafts limits the tumorigenic function of membrane type-1 matrix metalloproteinase in malignant cells. Exp Cell Res 293: 81–95, 2004
Uekita T, Itoh Y, Yana I, Ohno H, Seiki M: Cytoplasmic tail-dependent internalization of membrane-type 1 matrix metalloproteinase is important for its invasion-promoting activity. J Cell Biol 155: 1345-1356, 2001
Remacle, A, Murphy G, Roghi C: Membrane type I-matrix metalloproteinase (MT1-MMP) is internalised by two different pathways and is recycled to the cell surface. J Cell Sci 116: 3905–3916, 2003
Annabi B, Lachambre M, Bousquet-Gagnon N, Page M, Gingras D, Beliveau R: Localization of membrane-type 1 matrix metalloproteinase in caveolae membrane domains. Biochem J 353: 547–553, 2001
Wu, X, Gan B, Yoo Y, Guan JL: FAK-mediated src phosphorylation of endophilin A2 inhibits endocytosis of MT1-MMP and promotes ECM degradation. Dev Cell 9: 185–196, 2005
Wu YI, Munshi HG, Sen R, Snipas SJ, Salvesen GS, Fridman R, Stack MS: Glycosylation broadens the substrate profile of membrane type 1 matrix metalloproteinase. J Biol Chem 279: 8278–8289, 2004
Munshi HG, Wu YI, Ariztia EV, Stack MS: Calcium regulation of matrix metalloproteinase-mediated migration in oral squamous cell carcinoma cells. J Biol Chem 277: 41480–41488, 2002
Munshi HG, Wu YI, Mukhopadhyay S, Ottaviano AJ, Sassano A, Koblinski JE, Platanias LC, Stack MS: Differential regulation of membrane type 1-matrix metalloproteinase activity by ERK 1/2- and p38 MAPK-modulated tissue inhibitor of metalloproteinases 2 expression controls transforming growth factor-beta1-induced pericellular collagenolysis. J Biol Chem 279: 39042–39050, 2004
Golubkov VS, Boyd S, Savinov AY, Chekanov AV, Osterman AL, Remacle A, Rozanov DV, Doxsey SJ, Strongin AY: Membrane type-1 matrix metalloproteinase (MT1-MMP) exhibits an important intracellular cleavage function and causes chromosome instability. J Biol Chem 280: 25079–25086, 2005
Fujiwara T, Bandi M, Nitta M, Ivanova EV, Bronson RT, Pellman D: Cytokinesis failure generating tetraploids promotes tumorigenesis in p53-null cells. Nature 437: 1043–1047, 2005
Wijnhoven BP, Dinjens WN, Pignatelli M: E-cadherin-catenin cell-cell adhesion complex and human cancer. Br J Surg 87: 992–1005, 2000
Conacci-Sorrell M, Zhurinsky J, Ben-Ze'ev A: The cadherin-catenin adhesion system in signaling and cancer. J Clin Invest 109: 987–991, 2002
Kantak SS and Kramer RH: E-cadherin regulates anchorage-independent growth and survival in oral squamous cell carcinoma cells. J Biol Chem 273: 16953–16961, 1998
Mareel M, Boterberg T, Noe V, Van Hoorde L, Vermeulen S, Bruyneel E, Bracke M: E-cadherin/catenin/cytoskeleton complex: A regulator of cancer invasion. J Cell Physiol 173: 271–274, 1997
Angst BD, Marcozzi C, Magee AI: The cadherin superfamily. J Cell Sci 114: 625–626, 2001
Pece S, Chiariello M, Murga C, Gutkind JS: Activation of the protein kinase Akt/PKB by the formation of E-cadherin-mediated cell-cell junctions. Evidence for the association of phosphatidylinositol 3-kinase with the E-cadherin adhesion complex. J Biol Chem 274: 19347–19351, 1999
Pece S, Gutkind JS: Signaling from E-cadherins to the MAPK pathway by the recruitment and activation of epidermal growth factor receptors upon cell-cell contact formation. J Biol Chem 275: 41227–41233, 2000
Luo J, Lubaroff DM, Hendrix MJ: Suppression of prostate cancer invasive potential and matrix metalloproteinase activity by E-cadherin transfection. Cancer Res 59: 3552–3556, 1999
Chunthapong J, Seftor EA, Khalkhali-Ellis Z, Seftor RE, Amir S, Lubaroff DM, Heidger PM, Jr, Hendrix MJ: Dual roles of E-cadherin in prostate cancer invasion. J Cell Biochem 91: 649–661, 2004
Nawrocki-Raby B, Gilles C, Polette M, Martinella-Catusse C, Bonnet N, Puchelle E, Foidart JM, Van Roy F, Birembaut P: E-Cadherin mediates MMP down-regulation in highly invasive bronchial tumor cells. Am J Pathol 163: 653–661, 2003
Llorens A, Rodrigo I, Lopez-Barcons L, Gonzalez-Garrigues M, Lozano E, Vinyals A, Quintanilla M, Cano A, Fabra A: Down-regulation of E-cadherin in mouse skin carcinoma cells enhances a migratory and invasive phenotype linked to matrix metalloproteinase-9 gelatinase expression. Lab Invest 78: 1131–1142, 1998
Munshi, HG, Ghosh S, Mukhopadhyay S, Wu YI, Sen R, Green KJ, Stack MS: Proteinase suppression by E-cadherin-mediated cell-cell attachment in premalignant oral keratinocytes. J Biol Chem 277: 38159–38167, 2002
Margulis A, Zhang W, Alt-Holland A, Crawford HC, Fusenig NE, Garlick JA: E-cadherin suppression accelerates squamous cell carcinoma progression in three-dimensional, human tissue constructs. Cancer Res 65: 1783–1791, 2005
Nawrocki-Raby B, Gilles C, Polette M, Bruyneel E, Laronze JY, Bonnet N, Foidart JM, Mareel M, Birembaut P: Upregulation of MMPs by soluble E-cadherin in human lung tumor cells. Int J Cancer 105: 790–795, 2003
Marchenko GN, Marchenko ND, Leng J, Strongin AY: Promoter characterization of the novel human matrix metalloproteinase-26 gene: regulation by the T-cell factor-4 implies specific expression of the gene in cancer cells of epithelial origin. Biochem J 363: 253–262, 2002
Brabletz, T, Jung, A, Dag, S, Hlubek F, Kirchner T: beta-catenin regulates the expression of the matrix metalloproteinase-7 in human colorectal cancer. Am J Pathol 155: 1033–1038, 1999
Crawford HC, Fingleton BM, Rudolph-Owen LA, Goss KJ, Rubinfeld B, Polakis P, Matrisian LM: The metalloproteinase matrilysin is a target of beta-catenin transactivation in intestinal tumors. Oncogene 18: 2883–2891, 1999
Gustavson MD, Crawford HC, Fingleton B, Matrisian LM: Tcf binding sequence and position determines beta-catenin and Lef-1 responsiveness of MMP-7 promoters. Mol Carcinog 41: 125–139, 2004
Cheon, S, Poon, R, Yu, C, Khoury, M, Shenker R, Fish J, Alman BA: Prolonged beta-catenin stabilization and tcf-dependent transcriptional activation in hyperplastic cutaneous wounds. Lab Invest 85: 416–425, 2005
Li YJ, Wei ZM, Meng YX, Ji XR: Beta-catenin up-regulates the expression of cyclinD1, c-myc and MMP-7 in human pancreatic cancer: Relationships with carcinogenesis and metastasis. World J Gastroenterol 11: 2117–2123, 2005
Takahashi M, Tsunoda T, Seiki M, Nakamura Y, Furukawa Y: Identification of membrane-type matrix metalloproteinase-1 as a target of the beta-catenin/Tcf4 complex in human colorectal cancers. Oncogene 21: 5861–5867, 2002
Marchenko ND, Marchenko GN, Weinreb RN, Lindsey JD, Kyshtoobayeva A, Crawford H C, Strongin AY: Beta-catenin regulates the gene of MMP-26, a novel metalloproteinase expressed both in carcinomas and normal epithelial cells. Int J Biochem Cell Biol 36: 942–956, 2004
Qian X, Karpova T, Sheppard AM, McNally J, Lowy DR: E-cadherin-mediated adhesion inhibits ligand-dependent activation of diverse receptor tyrosine kinases. Embo J 23: 1739–1748, 2004
Suyama, K, Shapiro, I, Guttman, M, Hazan RB: A signaling pathway leading to metastasis is controlled by N-cadherin and the FGF receptor. Cancer Cell 2: 301–314, 2002
Behrens, J, Birchmeier, W, Goodman, SL, Imhof BA: Dissociation of Madin-Darby canine kidney epithelial cells by the monoclonal antibody anti-arc-1: Mechanistic aspects and identification of the antigen as a component related to uvomorulin. J Cell Biol 101: 1307–1315, 1985
Shibamoto, S, Hayakawa, M, Takeuchi K, Hori T, Oku N, Miyazawa, K, Kitamura, N, Takeichi M, Ito F: Tyrosine phosphorylation of beta-catenin and plakoglobin enhanced by hepatocyte growth factor and epidermal growth factor in human carcinoma cells. Cell Adhes Commun 1: 295–305, 1994
Frixen UH, Behrens J, Sachs M, Eberle G, Voss B, Warda A, Lochner D, Birchmeier W: E-cadherin-mediated cell-cell adhesion prevents invasiveness of human carcinoma cells. J Cell Biol 113: 173–185, 1991
Hoschuetzky H, Aberle H, Kemler R: Beta-catenin mediates the interaction of the cadherin-catenin complex with epidermal growth factor receptor. J Cell Biol 127: 1375–1380, 1994
Peinado H, Marin F, Cubillo E, Stark HJ, Fusenig N, Nieto MA, Cano A: Snail and E47 repressors of E-cadherin induce distinct invasive and angiogenic properties in vivo. J Cell Sci 117: 2827–2839, 2004
Huber MA, Kraut N, Beug H: Molecular requirements for epithelial-mesenchymal transition during tumor progression. Curr Opin Cell Biol 17: 548–558, 2005
De Craene B, Gilbert B, Stove C, Bruyneel E, van Roy F, Berx G: The transcription factor snail induces tumor cell invasion through modulation of the epithelial cell differentiation program. Cancer Res 65: 6237–6244, 2005
Comijn J, Berx G, Vermassen P, Verschueren K, van Grunsven L, Bruyneel E, Mareel M, Huylebroeck D, van Roy F: The two-handed E box binding zinc finger protein SIP1 downregulates E-cadherin and induces invasion. Mol Cell 7: 1267–1278, 2001
Hajra KM, Fearon ER: Cadherin and catenin alterations in human cancer. Genes Chromosomes Cancer 34: 255–268, 2002
Sugimachi K, Tanaka S, Kameyama T, Taguchi K, Aishima S, Shimada M, Tsuneyoshi M: Transcriptional repressor snail and progression of human hepatocellular carcinoma. Clin Cancer Res 9: 2657–2664, 2003
Rosivatz E, Becker I, Specht K, Fricke E, Luber B, Busch R, Hofler H, Becker KF: Differential expression of the epithelial-mesenchymal transition regulators snail, SIP1, twist in gastric cancer. Am J Pathol 161: 1881–1891, 2002
Moody SE, Perez D, Pan TC, Sarkisian CJ, Portocarrero CP, Sterner CJ, Notorfrancesco KL, Cardiff RD, Chodosh LA: The transcriptional repressor Snail promotes mammary tumor recurrence. Cancer Cell 8: 197–209, 2005
Miyoshi A, Kitajima Y, Sumi K, Sato K, Hagiwara A, Koga Y, Miyazaki K: Snail and SIP1 increase cancer invasion by upregulating MMP family in hepatocellular carcinoma cells. Br J Cancer 90: 1265–1273, 2004
Miyoshi A, Kitajima Y, Kido S, Shimonishi T, Matsuyama S, Kitahara K, Miyazaki K: Snail accelerates cancer invasion by upregulating MMP expression and is associated with poor prognosis of hepatocellular carcinoma. Br J Cancer 92: 252–258, 2005
Yokoyama K, Kamata N, Fujimoto R, Tsutsumi S, Tomonari M, Taki M, Hosokawa H, Nagayama M: Increased invasion and matrix metalloproteinase-2 expression by Snail-induced mesenchymal transition in squamous cell carcinomas. Int J Oncol 22: 891–898, 2003
Kuphal S, Palm HG, Poser I, Bosserhoff AK: Snail-regulated genes in malignant melanoma. Melanoma Res 15: 305–313, 2005
Jorda M, Olmeda D, Vinyals A, Valero E, Cubillo E, Llorens A, Cano A, Fabra A: Upregulation of MMP-9 in MDCK epithelial cell line in response to expression of the Snail transcription factor. J Cell Sci 118: 3371–3385, 2005
Shih, JY, Tsai, MF, Chang, TH, Chang, YL, Yuan A, Yu, CJ, Lin, SB, Liou, GY, Lee, ML, Chen JJ, Hong TM, Yang SC, Su JL, Lee YC, Yang PC: Transcription repressor slug promotes carcinoma invasion and predicts outcome of patients with lung adenocarcinoma. Clin Cancer Res 11: 8070–8078, 2005
Xian, W, Schwertfeger, KL, Vargo-Gogola, T, Rosen JM: Pleiotropic effects of FGFR1 on cell proliferation, survival, migration in a 3D mammary epithelial cell model. J Cell Biol 171: 663–673, 2005
Noe V, Fingleton B, Jacobs K, Crawford HC, Vermeulen S, Steelant W, Bruyneel E, Matrisian LM, Mareel M: Release of an invasion promoter E-cadherin fragment by matrilysin and stromelysin-1. J Cell Sci 114: 111–118, 2001
McGuire JK, Li Q, Parks WC: Matrilysin (matrix metalloproteinase-7) mediates E-cadherin ectodomain shedding in injured lung epithelium. Am J Pathol 162: 1831–1843, 2003
Covington MD, Burghardt RC, Parrish AR: Ischemia-induced cleavage of cadherins in NRK cells requires MT1-MMP (MMP-14). Am J Physiol Renal Physiol 290: F43–51, 2006
Sanceau J, Truchet S, Bauvois B: Matrix metalloproteinase-9 silencing by RNA interference triggers the migratory-adhesive switch in Ewing's sarcoma cells. J Biol Chem 278: 36537–36546, 2003
Ho AT, Voura EB, Soloway PD, Watson KL, Khokha R: MMP inhibitors augment fibroblast adhesion through stabilization of focal adhesion contacts and up-regulation of cadherin function. J Biol Chem 276: 40215–40224, 2001
Radisky, DC, Levy, DD, Littlepage, LE, Liu, H, Nelson, CM, Fata, JE, Leake, D, Godden EL, Albertson DG, Nieto MA, Werb Z, Bissell MJ: Rac1b and reactive oxygen species mediate MMP-3-induced EMT and genomic instability. Nature 436: 123–127, 2005
Reya T, Clevers H: Wnt signalling in stem cells and cancer. Nature 434: 843–850, 2005
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Munshi, H.G., Stack, M.S. Reciprocal interactions between adhesion receptor signaling and MMP regulation. Cancer Metastasis Rev 25, 45–56 (2006). https://doi.org/10.1007/s10555-006-7888-7
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DOI: https://doi.org/10.1007/s10555-006-7888-7