MT1-MMP and integrins: Hand-to-hand in cell communication

BioFactors

Volumn 36, Issue 4, 2010, Pages 248-254

  Gonzalo, Pilar ^a   Moreno, Vanessa ^a   Gálvez, Beatriz G ^a   Arroyo, Alicia G ^a  

^a CENTRO NACIONAL DE INVESTIGACIONES CARDIOVASCULARES CNIC   (Spain)

Author keywords

Integrins; Microdomains; Migration; MT1 MMP; Signaling

Indexed keywords

BETA1 INTEGRIN; INTEGRIN; MATRIX METALLOPROTEINASE 14; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; VITRONECTIN RECEPTOR;

ANGIOGENESIS; ARTICLE; CELL COMMUNICATION; CELL FRACTIONATION; CELL MIGRATION; CELLULAR DISTRIBUTION; ENDOCYTOSIS; ENDOTHELIUM CELL; EXTRACELLULAR MATRIX; FLUORESCENCE MICROSCOPY; GENETIC MODEL; MOLECULAR INTERACTION; MULTIPHOTON MICROSCOPY; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ANIMALS; CELL ADHESION; CELL COMMUNICATION; EXTRACELLULAR MATRIX; HUMANS; INTEGRINS; MATRIX METALLOPROTEINASE 14; MODELS, BIOLOGICAL; SIGNAL TRANSDUCTION;

EID: 78149473194     PISSN: 09516433     EISSN: 18728081     Source Type: Journal    
DOI: 10.1002/biof.99     Document Type: Article

References (66)

1. Hynes, R. O. (2002) Integrins: bidirectional, allosteric signaling machines. Cell 110, 673-687.
2. Hynes, R. O. (2009) The extracellular matrix: not just pretty fibrils. Science 326, 1216-1219.
3. Arroyo, A. G. and Iruela-Arispe, M. L. (2010) Extracellular matrix, inflammation, and the angiogenic response. Cardiovasc. Res. 86, 226-235.
4. Page-McCaw, A., Ewald, A. J., and Werb, Z. (2007) Matrix metalloproteinases and the regulation of tissue remodelling. Nat. Rev. Mol. Cell Biol. 8, 221-233.
5. Seiki, M., Mori, H., Kajita, M., Uekita, T., and Itoh, Y. (2003) Membrane-type 1 matrix metalloproteinase and cell migration. Biochem. Soc. Symp. 70, 253-262.
6. Holmbeck, K., Bianco, P., Caterina, J., Yamada, S., Kromer, M., Kuznetsov, S. A., Mankani, M., Robey, P. G., Poole, A. R., Pidoux, I., Ward, J. M., and Birkedal-Hansen, H. (1999) MT1-MMP-deficient mice develop dwarfism, osteopenia, arthritis, and connective tissue disease due to inadequate collagen turnover. Cell 99, 81-92.
7. Zhou, Z., Apte, S. S., Soininen, R., Cao, R., Baaklini, G. Y., Rauser, R. W., Wang, J., Cao, Y., and Tryggvason, K. (2000) Impaired endochondral ossification and angiogenesis in mice deficient in membrane-type matrix metalloproteinase I. Proc. Natl. Acad. Sci. USA 97, 4052-4057.
8. Lehti, K., Allen, E., Birkedal-Hansen, H., Holmbeck, K., Miyake, Y., Chun, T. H., and Weiss, S. J. (2005) An MT1-MMP-PDGF receptor-beta axis regulates mural cell investment of the microvasculature. Genes. Dev. 19, 979-991.
9. Oblander, S. A., Zhou, Z., Galvez, B. G., Starcher, B., Shannon, J. M., Durbeej, M., Arroyo, A. G., Tryggvason, K., and Apte, S. S. (2005) Distinctive functions of membrane type 1 matrix-metalloprotease (MT1-MMP or MMP-14) in lung and submandibular gland development are independent of its role in pro-MMP-2 activation. Dev. Biol. 277, 255-269.
10. Gonzalo, P., Guadamillas, M. C., Hernandez-Riquer, M. V., Pollan, A., Grande-Garcia, A., Bartolome, R. A., Vasanji, A., Ambrogio, C., Chiarle, R., Teixido, J., Risteli, J., Apte, S. S., Del Pozo, M. A., and Arroyo, A. G. (2010). MT1-MMP Is Required for Myeloid Cell Fusion via Regulation of Rac1 Signaling. Dev. Cell 18, 77-89.
11. Puyraimond, A., Fridman, R., Lemesle, M., Arbeille, B., and Menashi, S. (2001) MMP-2 colocalizes with caveolae on the surface of endothelial cells. Exp. Cell Res. 262, 28-36.
12. Hayer, A., Stoeber, M., Bissig, C., and Helenius, A. (2010) Biogenesis of caveolae: stepwise assembly of large caveolin and cavin complexes. Traffic. 11, 361-382.
13. Galvez, B. G., Matias-Roman, S., Yanez-Mo, M., Sanchez-Madrid, F., and Arroyo, A. G. (2002) 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.
14. Galvez, B. G., Matias-Roman, S., Yanez-Mo, M., Vicente-Manzanares, M., Sanchez-Madrid, F., and Arroyo, A. G. (2004) Caveolae are a novel pathway for membrane-type 1 matrix metalloproteinase traffic in human endothelial cells. Mol. Biol. Cell 15, 678-687.
15. Yanez-Mo, M., Barreiro, O., Gordon-Alonso, M., Sala-Valdes, M., and Sanchez-Madrid, F. (2009) Tetraspanin-enriched microdomains: a functional unit in cell plasma membranes. Trends Cell Biol. 19, 434-446.
16. Yanez-Mo, M., Barreiro, O., Gonzalo, P., Batista, A., Megias, D., Genis, L., Sachs, N., Sala-Valdes, M., Alonso, M. A., Montoya, M. C., Sonnenberg, A., Arroyo, A. G., and Sanchez-Madrid, F. (2008) MT1-MMP collagenolytic activity is regulated through association with tetraspanin CD151 in primary endothelial cells. Blood 112, 3217-3226.
17. Rozanov, D. V., Deryugina, E. I., Monosov, E. Z., Marchenko, N. D., and Strongin, A. Y. (2004) 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.
18. Lafleur, M. A., Xu, D., and Hemler, M. E. (2009) Tetraspanin proteins regulate membrane type-1 matrix metalloproteinase-dependent pericellular proteolysis. Mol. Biol. Cell 20, 2030-2040.
19. Tomari, T., Koshikawa, N., Uematsu, T., Shinkawa, T., Hoshino, D., Egawa, N., Isobe, T., and Seiki, M. (2009) High throughput analysis of proteins associating with a proinvasive MT1-MMP in human malignant melanoma A375 cells. Cancer Sci. 100, 1284-1290.
20. Niiya, D., Egawa, N., Sakamoto, T., Kikkawa, Y., Shinkawa, T., Isobe, T., Koshikawa, N., and Seiki, M. (2009) Identification and characterization of Lutheran blood group glycoprotein as a new substrate of membrane-type 1 matrix metalloproteinase 1 (MT1-MMP): a systemic whole cell analysis of MT1-MMP-associating proteins in A431 cells. J. Biol. Chem. 284, 27360-27369.
21. Geiger, B., Spatz, J. P., and Bershadsky, A. D. (2009) Environmental sensing through focal adhesions. Nat. Rev. Mol. Cell Biol. 10, 21-33.
22. Bravo-Cordero, J. J., Marrero-Diaz, R., Megias, D., Genis, L., Garcia-Grande, A., Garcia, M. A., Arroyo, A. G., and Montoya, M. C. (2007) MT1-MMP proinvasive activity is regulated by a novel Rab8-dependent exocytic pathway. EMBO J. 26, 1499-1510.
23. Gingras, D., Michaud, M., Di Tomasso, G., Beliveau, E., Nyalendo, C., and Beliveau, R. (2008) Sphingosine-1-phosphate induces the association of membrane-type 1 matrix metalloproteinase with p130Cas in endothelial cells. FEBS Lett. 582, 399-404.
24. Labrecque, L., Nyalendo, C., Langlois, S., Durocher, Y., Roghi, C., Murphy, G., Gingras, D., and Beliveau, R. (2004) Src-mediated tyrosine phosphorylation of caveolin-1 induces its association with membrane type 1 matrix metalloproteinase. J. Biol. Chem. 279, 52132-52140.
25. Nyalendo, C., Michaud, M., Beaulieu, E., Roghi, C., Murphy, G., Gingras, D., and Beliveau, R. (2007) Src-dependent phosphorylation of membrane type I matrix metalloproteinase on cytoplasmic tyrosine 573: role in endothelial and tumor cell migration. J. Biol. Chem. 282, 15690-15699.
26. Beardsley, A., Fang, K., Mertz, H., Castranova, V., Friend, S., and Liu, J. (2005) Loss of caveolin-1 polarity impedes endothelial cell polarization and directional movement. J. Biol. Chem. 280, 3541-3547.
27. Koshikawa, N., Giannelli, G., Cirulli, V., Miyazaki, K., and Quaranta, V. (2000) Role of cell surface metalloprotease MT1-MMP in epithelial cell migration over laminin-5. J. Cell Biol. 148, 615-624.
28. Takino, T., Watanabe, Y., Matsui, M., Miyamori, H., Kudo, T., Seiki, M., and Sato, H. (2006) Membrane-type 1 matrix metalloproteinase modulates focal adhesion stability and cell migration. Exp. Cell Res. 312, 1381-1389.
29. Caswell, P. T., Vadrevu, S., and Norman, J. C. (2009) Integrins: masters and slaves of endocytic transport. Nat. Rev. Mol. Cell Biol. 10, 843-853.
30. Uekita, T., Itoh, Y., Yana, I., Ohno, H., and Seiki, M. (2001) Cytoplasmic tail-dependent internalization of membrane-type 1 matrix metalloproteinase is important for its invasion-promoting activity. J. Cell Biol. 155, 1345-1356.
31. Jiang, A., Lehti, K., Wang, X., Weiss, S. J., Keski-Oja, J., and Pei, D. (2001) Regulation of membrane-type matrix metalloproteinase 1 activity by dynamin-mediated endocytosis. Proc. Natl. Acad. Sci. USA 98, 13693-13698.
32. Wu, X., Gan, B., Yoo, Y., and Guan, J. L. (2005) FAK-mediated src phosphorylation of endophilin A2 inhibits endocytosis of MT1-MMP and promotes ECM degradation. Dev. Cell 9, 185-196.
33. Remacle, A., Murphy, G., and Roghi, C. (2003) 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.
34. Wang, X., Ma, D., Keski-Oja, J., and Pei, D. (2004) Co-recycling of MT1-MMP and MT3-MMP through the trans-Golgi network. Identification of DKV582 as a recycling signal. J. Biol. Chem. 279, 9331-9336.
35. Pellinen, T. and Ivaska, J. (2006) Integrin traffic. J. Cell Sci. 119, 3723-3731.
36. Remacle, A. G., Rozanov, D. V., Baciu, P. C., Chekanov, A. V., Golubkov, V. S., and Strongin, A. Y. (2005) The transmembrane domain is essential for the microtubular trafficking of membrane type-1 matrix metalloproteinase (MT1-MMP). J. Cell Sci. 118, 4975-4984.
37. Moss, N. M., Wu, Y. I., Liu, Y., Munshi, H. G., and Stack, M. S. (2009) Modulation of the membrane type 1 matrix metalloproteinase cytoplasmic tail enhances tumor cell invasion and proliferation in three-dimensional collagen matrices. J. Biol. Chem. 284, 19791-19799.
38. Moss, N. M., Liu, Y., Johnson, J. J., Debiase, P., Jones, J., Hudson, L. G., Munshi, H. G., and Stack, M. S. (2009) Epidermal growth factor receptor-mediated membrane type 1 matrix metalloproteinase endocytosis regulates the transition between invasive versus expansive growth of ovarian carcinoma cells in three-dimensional collagen. Mol. Cancer Res. 7, 809-820.
39. Steffen, A., Le Dez, G., Poincloux, R., Recchi, C., Nassoy, P., Rottner, K., Galli, T., and Chavrier, P. (2008) MT1-MMP-dependent invasion is regulated by TI-VAMP/VAMP7. Curr. Biol. 18, 926-931.
40. Luftman, K., Hasan, N., Day, P., Hardee, D., and Hu, C. (2009) Silencing of VAMP3 inhibits cell migration and integrin-mediated adhesion. Biochem. Biophys. Res. Commun. 380, 65-70.
41. Hasan, N. and Hu, C. (2010) Vesicle-associated membrane protein 2 mediates trafficking of alpha5beta1 integrin to the plasma membrane. Exp. Cell Res. 316, 12-23.
42. Gingras, D. and Beliveau, R. (2010) Emerging concepts in the regulation of membrane-type 1 matrix metalloproteinase activity. Biochim. Biophys. Acta. 1803, 142-150.
43. Sounni, N. E., Roghi, C., Chabottaux, V., Janssen, M., Munaut, C., Maquoi, E., Galvez, B. G., Gilles, C., Frankenne, F., Murphy, G., Foidart, J. M., and Noel, A. (2004) Up-regulation of vascular endothelial growth factor-A by active membrane-type 1 matrix metalloproteinase through activation of Src-tyrosine kinases. J. Biol. Chem. 279, 13564-13574.
44. D'Alessio, S., Ferrari, G., Cinnante, K., Scheerer, W., Galloway, A. C., Roses, D. F., Rozanov, D. V., Remacle, A. G., Oh, E. S., Shiryaev, S. A., Strongin, A. Y., Pintucci, G., and Mignatti, P. (2008) Tissue inhibitor of metalloproteinases-2 binding to membrane-type 1 matrix metalloproteinase induces MAPK activation and cell growth by a non-proteolytic mechanism. J. Biol. Chem. 283, 87-99.
45. Takino, T., Miyamori, H., Watanabe, Y., Yoshioka, K., Seiki, M., and Sato, H. (2004) Membrane type 1 matrix metalloproteinase regulates collagen-dependent mitogen-activated protein/extracellular signal-related kinase activation and cell migration. Cancer Res. 64, 1044-1049.
46. Deryugina, E. I., Ratnikov, B. I., Postnova, T. I., Rozanov, D. V., and Strongin, A. Y. (2002) 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.
47. Mu, D., Cambier, S., Fjellbirkeland, L., Baron, J. L., Munger, J. S., Kawakatsu, H., Sheppard, D., Broaddus, V. C., and Nishimura, S. L. (2002) The integrin alpha(v)beta8 mediates epithelial homeostasis through MT1-MMP-dependent activation of TGF-beta1. J. Cell Biol. 157, 493-507.
48. Alfranca, A., Lopez-Oliva, J. M., Genis, L., Lopez-Maderuelo, D., Mirones, I., Salvado, D., Quesada, A. J., Arroyo, A. G., and Redondo, J. M. (2008) PGE2 induces angiogenesis via MT1-MMP-mediated activation of the TGFbeta/Alk5 signaling pathway. Blood 112, 1120-1128.
49. Tatti, O., Vehvilainen, P., Lehti, K., and Keski-Oja, J. (2008) MT1-MMP releases latent TGF-beta1 from endothelial cell extracellular matrix via proteolytic processing of LTBP-1. Exp. Cell Res. 314, 2501-2514.
50. Del Pozo, M. A., Kiosses, W. B., Alderson, N. B., Meller, N., Hahn, K. M., and Schwartz, M. A. (2002) Integrins regulate GTP-Rac localized effector interactions through dissociation of Rho-GDI. Nat. Cell Biol. 4, 232-239.
51. Fisher, K. E., Sacharidou, A., Stratman, A. N., Mayo, A. M., Fisher, S. B., Mahan, R. D., Davis, M. J., and Davis, G. E. (2009) MT1-MMP- and Cdc42-dependent signaling co-regulate cell invasion and tunnel formation in 3D collagen matrices. J. Cell Sci. 122, 4558-4569.
52. Hoshino, D., Tomari, T., Nagano, M., Koshikawa, N., and 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.
53. Chun, T. H., Sabeh, F., Ota, I., Murphy, H., McDonagh, K. T., Holmbeck, K., Birkedal-Hansen, H., Allen, E. D., and Weiss, S. J. (2004) MT1-MMP-dependent neovessel formation within the confines of the three-dimensional extracellular matrix. J. Cell Biol. 167, 757-767.
54. Galvez, B. G., Matias-Roman, S., Albar, J. P., Sanchez-Madrid, F., and Arroyo, A. G. (2001) Membrane type 1-matrix metalloproteinase is activated during migration of human endothelial cells and modulates endothelial motility and matrix remodeling. J. Biol. Chem. 276, 37491-37500.
55. Sakamoto, T. and Seiki, M. (2009) Cytoplasmic tail of MT1-MMP regulates macrophage motility independently from its protease activity. Genes Cells. 14, 617-626.
56. Wolf, K., Wu, Y. I., Liu, Y., Geiger, J., Tam, E., Overall, C., Stack, M. S., and Friedl, P. (2007) Multi-step pericellular proteolysis controls the transition from individual to collective cancer cell invasion. Nat. Cell Biol. 9, 893-904.
57. Friedl, P. and Wolf, K. Plasticity of cell migration: a multiscale tuning model. J. Cell Biol. 188, 11-19.
58. Deryugina, E. I., Ratnikov, B., Monosov, E., Postnova, T. I., DiScipio, R., Smith, J. W., and Strongin, A. Y. (2001) MT1-MMP initiates activation of pro-MMP-2 and integrin alphavbeta3 promotes maturation of MMP-2 in breast carcinoma cells. Exp. Cell Res. 263, 209-223.
59. Clark, R. A., Tonnesen, M. G., Gailit, J., and Cheresh, D. A. (1996) Transient functional expression of alphaVbeta 3 on vascular cells during wound repair. Am. J. Pathol. 148, 1407-1421.
60. Yana, I., Sagara, H., Takaki, S., Takatsu, K., Nakamura, K., Nakao, K., Katsuki, M., Taniguchi, S., Aoki, T., Sato, H., Weiss, S. J., and Seiki, M. (2007) Crosstalk between neovessels and mural cells directs the site-specific expression of MT1-MMP to endothelial tip cells. J. Cell Sci. 120, 1607-1614.
61. Galvez, B. G., Genis, L., Matias-Roman, S., Oblander, S. A., Tryggvason, K., Apte, S. S., and Arroyo, A. G. (2005) Membrane type 1-matrix metalloproteinase is regulated by chemokines monocyte-chemoattractant protein-1/ccl2 and interleukin-8/CXCL8 in endothelial cells during angiogenesis. J. Biol. Chem. 280, 1292-1298.
62. Sheppard, D. (2004) Roles of alphav integrins in vascular biology and pulmonary pathology. Curr. Opin. Cell Biol. 16, 552-557.
63. Ohtake, Y., Tojo, H., and Seiki, M. (2006) Multifunctional roles of MT1-MMP in myofiber formation and morphostatic maintenance of skeletal muscle. J. Cell Sci. 119, 3822-3832.
64. Shi, J., Son, M. Y., Yamada, S., Szabova, L., Kahan, S., Chrysovergis, K., Wolf, L., Surmak, A., and Holmbeck, K. (2008) Membrane-type MMPs enable extracellular matrix permissiveness and mesenchymal cell proliferation during embryogenesis. Dev. Biol. 313, 196-209.
65. Aszodi, A., Hunziker, E. B., Brakebusch, C., and Fassler, R. (2003) Beta1 integrins regulate chondrocyte rotation, G1 progression, and cytokinesis. Genes Dev. 17, 2465-2479.
66. Brakebusch, C. and Fassler, R. (2005) beta 1 integrin function in vivo: adhesion, migration and more. Cancer Metastasis Rev. 24, 403-411.