Critical Role of Transient Activity of MT1-MMP for ECM Degradation in Invadopodia

PLoS Computational Biology

Volumn 9, Issue 5, 2013, Pages

  Watanabe, Ayako ^a   Hosino, Daisuke ^a   Koshikawa, Naohiko ^a   Seiki, Motoharu ^a,b   Suzuki, Takashi ^b,c   Ichikawa, Kazuhisa ^a,b  

^a THE UNIVERSITY OF TOKYO   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^c OSAKA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CELLS; DISEASES;

CANCER CELLS; COMPUTATIONAL MODELLING; DEGRADING ACTIVITIES; EXTRACELLULAR MATRICES; EXTRACELLULAR MATRIX DEGRADATION; HIGH FREQUENCY HF; LOW CONCENTRATIONS; LOWER FREQUENCIES; PULSATILES; STEADY STATE;

CANCER CELLS;

MATRIX METALLOPROTEINASE 14; TISSUE INHIBITOR OF METALLOPROTEINASE 2;

ARTICLE; CANCER CELL CULTURE; CELL MEMBRANE; CELL TRANSPORT; COMPUTER SIMULATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME INHIBITION; ENZYME KINETICS; ENZYME METABOLISM; EXTRACELLULAR MATRIX; EXTRACELLULAR MATRIX DEGRADATION; HEAD AND NECK SQUAMOUS CELL CARCINOMA; INVADOPODIUM; STEADY STATE;

EID: 84878503116     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1003086     Document Type: Article

References (34)

1. Hanahan D, Weinberg RA, (2000) The hallmarks of cancer. Cell 100: 57-70.
2. Taniwaki K, Fukamachi H, Komori K, Ohtake Y, Nonaka T, et al. (2007) Stroma-derived matrix metalloproteinase (MMP)-2 promotes membrane type 1-MMP-dependent tumor growth in mice. Cancer Res 67: 4311-4319.
3. Maquoi E, Assent D, Detilleux J, Peuwueux C, Goidart JM, et al. (2011) MT1-MMP protects breast carcinoma cells against type I collagen-induced apoptosis. Oncogene 31: 480-93.
4. Nonaka T, Nishibashi K, Itoh Y, Yana I, Seiki M, (2005) Competitive disruption of the tumor-Npromoting function of membrane type 1 matrix metalloproteinase/matrix metalloproteinase-14 in vivo. Mol Cancer Ther 4: 1157-1166.
5. Artym VV, Zhauq Y, Seiller-Moiseiwitsch F, Yamada KM, Mueller SC, (2006) Dynamic interactions of cortactin and membrane type 1 matrix metalloproteinase at invadopodia: defining the stages of invadopodia formation and function. Cancer Res 66: 3034-3043.
6. Nakahara H, Howard L, Thompson EW, Sato H, Seiki M, et al. (1997) Transmembrane/cytoplasmic domain-mediated membrane type 1-matrix metalloprotease docking to invadopodia is required for cell invasion. Proc Natl Acad Sci U S A 94: 7959-7964.
7. Chen WT, Wang JY, (1999) Specialized surface protrusions of invasive cells, invadopodia and lamellipodia, have differential MT1-MMP, MMP-2, and TIMP-2 localization. Ann N Y Acad Sci 878: 361-371.
8. Hoshino D, Tomari T, Nagano M, Koshikawa N, Seiki M, (2009) A novel protein associated with membrane-type 1 matrix metalloproteinase binds p27(kip1) and regulates RhoA activation, actin remodeling, and matrigel invasion. J Biol Chem 284: 27315-27326.
9. Imai K, Ohuchi E, Aoki T, Nomura H, Fujii Y, et al. (1996) 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.
10. Kinoshita T, Sato H, Okada A, Ohuchi E, Imai K, et al. (1998) TIMP-2 promotes activation of progelatinase A by membrane-type 1 matrix metalloproteinase immobilized on agarose beads. J Biol Chem 273: 16098-16103.
11. Seiki M, (2002) The cell surface: the stage for matrix metalloproteinase regulation of migration. Current Opinion in Cell Biology 14: 624-632.
12. Gioia M, Monaco S, Fasciqlione GF, Coletti A, Modesti A, et al. (2007) Characterization of the mechanisms by which gelatinase A, neutrophil collagenase, and membrane-type metalloproteinase MMP-14 recognize collagen I and enzymatically process the two alpha-chains. J Mol Biol 368: 1101-13.
13. Okada Y, Morodomi T, Enghild JJ, Suzuki K, Yasui A, et al. (1990) Matrix metalloproteinase 2 from human rheumatoid synovial fibroblasts. Purification and activation of the precursor and enzymic properties. Eur J Biochem 194: 721-730.
14. Aimes RT, Quigley JP, (1995) 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.
15. Nagase H, Visse R, Murphy G, (2006) Structure and function of matrix metalloproteinases and TIMPs. Cardiovasc Res 69: 562-73.
16. Ohuchi E, Imai K, Fujii Y, Sato H, Seiki M, et al. (1997) Membrane type 1 matrix metalloproteinase digests interstitial collagens and other extracellular matrix macromolecules. J Biol Chem 272: 2446-2451.
17. Seiki M, (2003) Membrane-type 1 matrix metalloproteinase: a key enzyme for tumor invasion. Cancer Lett 194: 1-11.
18. Butler GS, Butler MJ, Atkinson SJ, Will H, Tamura T, et al. (1998) The TIMP2 membrane type 1 metalloproteinase "receptor" regulates the concentration and efficient activation of progelatinase A. A kinetic study. J Biol Chem 273: 871-880.
19. Itoh Y, Takamura A, Ito N, Maru Y, Sato H, et al. (2001) Homophilic complex formation of MT1-MMP facilitates proMMP-2 activation on the cell surface and promotes tumor cell invasion. EMBO J 20: 4782-4793.
20. Itoh Y, Seiki M, (2006) MT1-MMP: a potent modifier of pericellular microenvironment. J Cell Physiol 206: 1-8.
21. Steffen A, Le Dez G, Poincloux R, Recchi C, Nassoy P, et al. (2008) MT1-MMP-dependent invasion is regulated by TI-VAMP/VAMP7. Curr Biol 18: 926-31.
22. Hashimoto S, Onodera Y, Hashimoto A, Tanaka M, Hamaguchi M, et al. (2004) Requirement for Arf6 in breast cancer invasive activities. Proc Natl Acad Sci U S A 101: 6647-6652.
23. Hoshino D, Koshikawa N, Suzuki T, Quaranta V, Weaver AM, et al. (2012) Establishment and validation of computational model for MT1-MMP dependent ECM degradation and intervention strategies. PLoS Comput Biol 8: e1002479.
24. Yu X, Zech T, McDnaod L, Gonzalez EG, Li A, et al. (2012) N-WASP coordinates the delivery and F-actin-mediated capture of MT1-MMP at invasive pseudopods. J Cell Biol 199: 527-44.
25. Baldassarre M, Pomepeo A, Beznoussenko G, Castaldi C, Cortellino S, et al. (2003) Dynamin participates in focal extracellular matrix degradation by invasive cells. Mol Biol Cell 14: 1074-1084.
26. Sakurai-Yageta M, Recchi C, Le Dez G, Sibarita JB, Davient L, et al. (2008) The interaction of IQGAP1 with the exocyst complex is required for tumor cell invasion downstream of Cdc42 and RhoA. J Cell Biol 181: 985-998.
27. Gimona M, Buccione R, Courtneidge SA, Linder S, (2008) Assembly and biological role of podosomes and invadopodia. Curr Opin Cell Biol 20: 235-241.
28. Yamaguchi H, Takeo Y, Yoshida S, Kouchi Z, Nakamura Y, et al. (2009) Lipid rafts and caveolin-1 are required for invadopodia formation and extracellular matrix degradation by human breast cancer cells. Cancer Res 69: 8594-602.
29. Bravo-Cordero JJ, Marrero-Diaz R, Meqias D, Genis L, Garcia-Grande A, et al. (2007) MT1-MMP proinvasive activity is regulated by a novel Rab8-dependent exocytic pathway. EMBO J 26: 1499-1510.
30. Chen WT, Wang JY, (1999) Specialized surface protrusions of invasive cells, invadopodia and lamellipodia, have differential MT1-MMP, MMP-2, and TIMP-2 localization. Ann N Y Acad Sci 878: 361-71.
31. Clark ES, Whigham AS, Yarbrough WG, Weaver AM, (2007) Cortactin is an essential regulator of matrix metalloproteinase secretion and extracellular matrix degradation in invadopodia. Cancer Res 67: 4227-35.
32. Ichikawa K, (2001) A-Cell: graphical user interface for the construction of biochemical reaction models. Bioinformatics 17: 483-4.
33. Ichikawa K, (2005) A modeling environment with three-dimensional morphology, A-Cell-3D, and Ca2+ dynamics in a spine. Neuroinformatics 3: 49-64.
34. Karagiannis ED, Popel AS, (2004) A theoretical model of type I collagen proteolysis by matrix metalloproteinase (MMP) 2 and membrane type 1 MMP in the presence of tissue inhibitor of metalloproteinase 2. J Biol Chem 279: 39105-39114.