MT1-MMP regulates the turnover and endocytosis of extracellular matrix fibronectin

Journal of Cell Science

Volumn 124, Issue 23, 2011, Pages 4039-4050

  Shi, Feng ^a   Sottile, Jane ^a  

^a UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

Author keywords

Endocytosis; Extracellular matrix; Fibronectin; Integrin; MMP14; MT1 MMP; Trafficking

Indexed keywords

ALPHA5 INTEGRIN; BETA1 INTEGRIN; COLLAGEN; FIBRINOGEN; FIBRONECTIN; MATRIX METALLOPROTEINASE 14; TISSUE INHIBITOR OF METALLOPROTEINASE 1; TISSUE INHIBITOR OF METALLOPROTEINASE 2;

ANIMAL CELL; ARTICLE; CELL MIGRATION; CONJUGATION; CONTROLLED STUDY; ENDOCYTOSIS; EXTRACELLULAR MATRIX; FIBER; FLUORESCENCE ANALYSIS; HUMAN; HUMAN CELL; INHIBITION KINETICS; INTRACELLULAR SPACE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN POLYMERIZATION; PROTEIN STABILITY; PROTEIN STRUCTURE; RAT; TURNOVER TIME;

ADENOVIRIDAE; ANIMALS; CLONING, MOLECULAR; CULTURE MEDIA; ENDOCYTOSIS; EXTRACELLULAR MATRIX; EXTRACELLULAR MATRIX PROTEINS; FIBRONECTINS; FLOW CYTOMETRY; HEK293 CELLS; HUMANS; INTEGRIN ALPHA5BETA1; MATRIX METALLOPROTEINASE 14; MYOCYTES, SMOOTH MUSCLE; MYOFIBROBLASTS; POLYMERIZATION; PROTEIN STABILITY; PROTEIN TRANSPORT; PROTEOLYSIS; RATS; TRANSFECTION; WOUND HEALING;

EID: 84856840530     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.087858     Document Type: Article

References (84)

1. 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.
2. Barilla, M. L. and Carsons, S. E. (2000). Fibronectin fragments and their role in inflammatory arthritis. Semin. Arthritis Rheum. 29, 252-265.
3. Berk, B. C., Fujiwara, K. and Lehoux, S. (2007). ECM remodeling in hypertensive heart disease. J. Clin. Invest 117, 568-575.
4. Bourdoulous, S., Orend, G., MacKenna, D. A., Pasqualini, R. and Ruoslahti, E. (1998). Fibronectin matrix regulates activation of RHO and CDC42 GTPases and cell cycle progression. J. Cell Biol. 143, 267-276.
5. Bretscher, M. S. (1989). Endocytosis and recycling of the fibronectin receptor in CHO cells [published erratum appears in EMBO J. (1989). 8, 2122]. EMBO. J. 8, 1341-1348.
6. Caswell, P. T., Spence, H. J., Parsons, M., White, D. P., Clark, K., Cheng, K. W., Mills, G. B., Humphries, M. J., Messent, A. J., Anderson, K. I. et al. (2007). Rab25 associates with alpha5beta1 integrin to promote invasive migration in 3D microenvironments. Dev. Cell 13, 496-510.
7. Caswell, P. T., Chan, M., Lindsay, A. J., McCaffrey, M. W., Boettiger, D. and Norman, J. C. (2008). Rab-coupling protein coordinates recycling of alpha5beta1 integrin and EGFR1 to promote cell migration in 3D microenvironments. J. Cell Biol. 183, 143-155.
8. 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.
9. Chiang, H. Y., Korshunov, V. A., Serour, A., Shi, F. and Sottile, J. (2009). Fibronectin is an important regulator of flow-induced vascular remodeling. Arterioscler. Thromb. Vasc. Biol. 29, 1074-1079.
10. 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.
11. Clark, R. A. F. (1996). Wound repair: Overview and general considerations. In The Molecular and Cellular Biology of Wound Repair (ed. R. A. F. Clark), pp. 3-50. New York: Plenum Press.
12. Clark, R. A., Wikner, N. E., Doherty, D. E. and Norris, D. A. (1988). Cryptic chemotactic activity of fibronectin for human monocytes resides in the 120-kDa fibroblastic cell-binding fragment. J. Biol Chem. 263, 12115-12123.
13. Czekay, R. P., Aertgeerts, K., Curriden, S. A. and Loskutoff, D. J. (2003). Plasminogen activator inhibitor-1 detaches cells from extracellular matrices by inactivating integrins. J. Cell Biol. 160, 781-791.
14. Dai, R., Iwama, A., Wang, S. and Kapila, Y. L. (2005). Disease-associated fibronectin matrix fragments trigger anoikis of human primary ligament cells: p53 and c-myc are suppressed. Apoptosis 10, 503-512.
15. East, L., McCarthy, A., Wienke, D., Sturge, J., Ashworth, A. and Isacke, C. M. (2003). A targeted deletion in the endocytic receptor gene Endo180 results in a defect in collagen uptake. EMBO Rep. 4, 710-716.
16. Filippov, S., Koenig, G. C., Chun, T. H., Hotary, K. B., Ota, I., Bugge, T. H., Roberts, J. D., Fay, W. P., Birkedal-Hansen, H., Holmbeck, K. et al. (2005). MT1-matrix metalloproteinase directs arterial wall invasion and neointima formation by vascular smooth muscle cells. J. Exp. Med. 202, 663-671.
17. Frisch, S. M. and Ruoslahti, E. (1997). Integrins and anoikis. Curr. Opin. Cell Biol. 9, 701-706.
18. Galis, Z. S., Johnson, C., Godin, D., Magid, R., Shipley, J. M., Senior, R. M. and Ivan, E. (2002). Targeted disruption of the matrix metalloproteinase-9 gene impairs smooth muscle cell migration and geometrical arterial remodeling. Circ. Res. 91, 852-859.
19. 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.
20. 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.
21. Genis, L., Gonzalo, P., Tutor, A. S., Galvez, B. G., Martinez-Ruiz, A., Zaragoza, C., Lamas, S., Tryggvason, K., Apte, S. S. and Arroyo, A. G. (2007). Functional interplay between endothelial nitric oxide synthase and membrane type 1 matrix metalloproteinase in migrating endothelial cells. Blood 110, 2916-2923.
22. Giannelli, G., Falk-Marzillier, J., Schiraldi, O., Stetler-Stevenson, W. G. and Quaranta, V. (1997). Induction of cell migration by matrix metalloprotease-2 cleavage of laminin-5. Science 277, 225-227.
23. Gildner, C. D., Lerner, A. L. and Hocking, D. C. (2004). Fibronectin matrix polymerization increases the tensile strength of a model tissue. Am. J. Physiol. Heart Circ. Physiol. 287, H46-H53.
24. 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. et al. (2010a). MT1-MMP is required for myeloid cell fusion via regulation of Rac1 signaling. Dev. Cell 18, 77-89.
25. Gonzalo, P., Moreno, V., Galvez, B. G. and Arroyo, A. G. (2010b). MT1-MMP and integrins: Hand-to-hand in cell communication. Biofactors 36, 248-254.
26. Graham, H. K., Horn, M. and Trafford, A. W. (2008). Extracellular matrix profiles in the progression to heart failure. European young physiologists symposium keynote lecture - Bratislava 2007. Acta. Physiol. 194, 3-21.
27. Gronski, T. J., Jr, Martin, R. L., Kobayashi, D. K., Walsh, B. C., Holman, M. C., Huber, M., Van Wart, H. E. and Shapiro, S. D. (1997). Hydrolysis of a broad spectrum of extracellular matrix proteins by human macrophage elastase. J. Biol. Chem. 272, 12189-12194.
28. Heeneman, S., Cleutjens, J. P., Faber, B. C., Creemers, E. E., van Suylen, R. J., Lutgens, E., Cleutjens, K. B. and Daemen, M. J. (2003). The dynamic extracellular matrix: intervention strategies during heart failure and atherosclerosis. J. Pathol. 200, 516-525.
29. Hemmann, S., Graf, J., Roderfeld, M. and Roeb, E. (2007). Expression of MMPs and TIMPs in liver fibrosis - a systematic review with special emphasis on anti-fibrotic strategies. J. Hepatol. 46, 955-975.
30. Hocking, D. C. and Chang, C. H. (2003). Fibronectin matrix polymerization regulates small airway epithelial cell migration. Am. J. Physiol. 285, L169-L179.
31. Hocking, D. C. and Kowalski, K. (2002). A cryptic fragment from fibronectin's III1 module localizes to lipid rafts and stimulates cell growth and contractility. J. Cell Biol. 158, 175-184.
32. Holmbeck, K., Bianco, P., Caterina, J., Yamada, S., Kromer, M., Kuznetsov, S. A., Mankani, M., Robey, P. G., Poole, A. R., Pidoux, I. et al. (1999). MT1-MMPdeficient mice develop dwarfism, osteopenia, arthritis, and connective tissue disease due to inadequate collagen turnover. Cell 99, 81-92.
33. Homandberg, G. A., Williams, J. E., Grant, D., Schumacher, B. and Eisenstein, R. (1985). Heparin-binding fragments of fibronectin are potent inhibitors of endothelial cell growth. Am. J. Pathol. 120, 327-332.
34. Hotary, K., Allen, E., Punturieri, A., Yana, I. and Weiss, S. J. (2000). Regulation of cell invasion and morphogenesis in a three-dimensional type I collagen matrix by membrane-type matrix metalloproteinases 1, 2, and 3. J. Cell Biol. 149, 1309-1323.
35. Hotary, K. B., Yana, I., Sabeh, F., Li, X. Y., Holmbeck, K., Birkedal-Hansen, H., Allen, E. D., Hiraoka, N. and Weiss, S. J. (2002). Matrix metalloproteinases (MMPs) regulate fibrin-invasive activity via MT1-MMP-dependent and -independent processes. J. Exp. Med. 195, 295-308.
36. Hotary, K. B., Allen, E. D., Brooks, P. C., Datta, N. S., Long, M. W. and Weiss, S. J. (2003). Membrane type I matrix metalloproteinase usurps tumor growth control imposed by the three-dimensional extracellular matrix. Cell 114, 33-45.
37. Intengan, H. D. and Schiffrin, E. L. (2001). Vascular remodeling in hypertension: roles of apoptosis, inflammation, and fibrosis. Hypertension 38, 581-587.
38. Ivaska, J., Whelan, R. D., Watson, R. and Parker, P. J. (2002). PKC epsilon controls the traffic of beta1 integrins in motile cells. EMBO J. 21, 3608-3619.
39. Kenny, H. A., Kaur, S., Coussens, L. M. and Lengyel, E. (2008). The initial steps of ovarian cancer cell metastasis are mediated by MMP-2 cleavage of vitronectin and fibronectin. J. Clin. Invest 118, 1367-1379.
40. Kjaer, M. (2004). Role of extracellular matrix in adaptation of tendon and skeletal muscle to mechanical loading. Physiol. Rev. 84, 649-698.
41. Klein, R. M., Zheng, M., Ambesi, A., Van De Water, L. and McKeown-Longo, P. J. (2003). Stimulation of extracellular matrix remodeling by the first type III repeat in fibronectin. J. Cell Sci. 116, 4663-4674.
42. LaFlamme, S. E., Shi, F. and Sottile, J. (2008). Integrin trafficking. In Cell Junctions (eds. S. E. LaFlamme and A. P. Kowalczyk), pp. 89-107. Weinheim: Wiley-VCH.
43. Li, Y. Y., McTiernan, C. F. and Feldman, A. M. (2000). Interplay of matrix metalloproteinases, tissue inhibitors of metalloproteinases and their regulators in cardiac matrix remodeling. Cardiovasc. Res. 46, 214-224.
44. Liotta, L. A. and Kohn, E. C. (2001). The microenvironment of the tumour-host interface. Nature 411, 375-379.
45. Lobert, V. H., Brech, A., Pedersen, N. M., Wesche, J., Oppelt, A., Malerod, L. and Stenmark, H. (2010). Ubiquitination of alpha 5 beta 1 integrin controls fibroblast migration through lysosomal degradation of fibronectin-integrin complexes. Dev. Cell 19, 148-159.
46. Madsen, D. H., Engelholm, L. H., Ingvarsen, S., Hillig, T., Wagenaar-Miller, R. A., Kjoller, L., Gardsvoll, H., Hoyer-Hansen, G., Holmbeck, K., Bugge, T. H. et al. (2007). Extracellular collagenases and the endocytic receptor, urokinase plasminogen activator receptor-associated protein/Endo180, cooperate in fibroblast-mediated collagen degradation. J. Biol. Chem. 282, 27037-27045.
47. Magnusson, M. K. and Mosher, D. F. (1998). Fibronectin: structure, assembly, and cardiovascular implications. Arteriosclerosis Thrombosis Vascular Biology 18, 1363-1370.
48. Marchina, E. and Barlati, S. (1996). Degradation of human plasma and extracellular matrix fibronectin by tissue type plasminogen activator and urokinase. Int. J. Biochem. Cell Biol. 28, 1141-1150.
49. Matias-Roman, S., Galvez, B. G., Genis, L., Yanez-Mo, M., de la Rosa, G., Sanchez-Mateos, P., Sanchez-Madrid, F. and Arroyo, A. G. (2005). Membrane type 1-matrix metalloproteinase is involved in migration of human monocytes and is regulated through their interaction with fibronectin or endothelium. Blood 105, 3956-3964.
50. Mercurius, K. W. and Morla, A. O. (1998). Inhibition of vascular smooth muscle cell growth by inhibition of fibronectin matrix assembly. Circ. Res. 82, 548-556.
51. Millis, A. J., Hoyle, M., Mann, D. M. and Brennan, M. J. (1985). Incorporation of cellular and plasma fibronectins into smooth muscle cell extracellular matrix in vitro. Proc. Natl. Acad. Sci. USA 82, 2746-2750.
52. Nagase, H., Visse, R. and Murphy, G. (2006). Structure and function of matrix metalloproteinases and TIMPs. Cardiovasc. Res. 69, 562-573.
53. Ng, T., Parsons, M., Hughes, W. E., Monypenny, J., Zicha, D., Gautreau, A., Arpin, M., Gschmeissner, S., Verveer, P. J., Bastiaens, P. I. et al. (2001). Ezrin is a downstream effector of trafficking PKC-integrin complexes involved in the control of cell motility. EMBO J. 20, 2723-2741.
54. Norris, D. A., Clark, R. A., Swigart, L. M., Huff, J. C., Weston, W. L. and Howell, S. E. (1982). Fibronectin fragment(s) are chemotactic for human peripheral blood monocytes. J. Immunol. 129, 1612-1618.
55. Odrljin, T. M., Haidaris, C. G., Lerner, N. B. and Simpson-Haidaris, P. J. (2001). Integrin alphavbeta3-mediated endocytosis of immobilized fibrinogen by A549 lung alveolar epithelial cells. Am. J. Respir. Cell Mol. Biol. 24, 12-21.
56. Ohuchi, E., Imai, K., Fujii, Y., Sato, H., Seiki, M. and Okada, Y. (1997). Membrane type 1 matrix metalloproteinase digests interstitial collagens and other extracellular matrix macromolecules. J. Biol. Chem. 272, 2446-2451.
57. Panetti, T. S., Wilcox, S. A., Horzempa, C. and McKeown-Longo, P. J. (1995). Alpha v beta 5 integrin receptor-mediated endocytosis of vitronectin is protein kinase Cdependent. J. Biol. Chem. 270, 18593-18597.
58. Paszek, M. J., Zahir, N., Johnson, K. R., Lakins, J. N., Rozenberg, G. I., Gefen, A., Reinhart-King, C. A., Margulies, S. S., Dembo, M., Boettiger, D. et al. (2005). Tensional homeostasis and the malignant phenotype. Cancer Cell 8, 241-254.
59. Pellinen, T., Arjonen, A., Vuoriluoto, K., Kallio, K., Fransen, J. A. and Ivaska, J. (2006). Small GTPase Rab21 regulates cell adhesion and controls endosomal traffic of beta1-integrins. J. Cell Biol. 173, 767-780.
60. Pereira, M., Rybarczyk, B. J., Odrljin, T. M., Hocking, D. C., Sottile, J. and Simpson-Haidaris, P. J. (2002). The incorporation of fibrinogen into extracellular matrix is dependent on active assembly of a fibronectin matrix. J. Cell Sci. 115, 609-617.
61. Peyton, S. R. and Putnam, A. J. (2005). Extracellular matrix rigidity governs smooth muscle cell motility in a biphasic fashion. J. Cell Physiol. 204, 198-209.
62. Roberts, M., Barry, S., Woods, A., van der Sluijs, P. and Norman, J. (2001). PDGFregulated rab4-dependent recycling of alphavbeta3 integrin from early endosomes is necessary for cell adhesion and spreading. Curr. Biol. 11, 1392-1402.
63. Sabeh, F., Ota, I., Holmbeck, K., Birkedal-Hansen, H., Soloway, P., Balbin, M., Lopez-Otin, C., Shapiro, S., Inada, M., Krane, S. et al. (2004). Tumor cell traffic through the extracellular matrix is controlled by the membrane-anchored collagenase MT1-MMP. J. Cell Biol. 167, 769-781.
64. Sasaki, T., Larsson, H., Tisi, D., Claesson-Welsh, L., Hohenester, E. and Timpl, R. (2000). Endostatins derived from collagens XV and XVIII differ in structural and binding properties, tissue distribution and anti-angiogenic activity. J. Mol. Biol. 301, 1179-1190.
65. Schenk, S. and Quaranta, V. (2003). Tales from the crypt[ic] sites of the extracellular matrix. Trends Cell Biol. 13, 366-375.
66. Sechler, J. L. and Schwarzbauer, J. E. (1998). Control of cell cycle progression by fibronectin matrix architecture. J. Biol. Chem. 273, 25533-25536.
67. Shapiro, S. D. (1998). Matrix metalloproteinase degradation of extracellular matrix: biological consequences. Curr. Opin. Cell Biol. 10, 602-608.
68. Shi, F. and Sottile, J. (2008). Caveolin-1 dependent integrin trafficking is a critical regulator of fibronectin turnover. J. Cell Sci. 121, 2360-2371.
69. Shi, F., Harman, J., Fujiwara, K. and Sottile, J. (2010). Collagen I matrix turnover is regulated by fibronectin polymerization. Am. J. Physiol. Cell Physiol. 298, C1265-C1275.
70. Singh, P., Carraher, C. and Schwarzbauer, J. E. (2010). Assembly of fibronectin extracellular matrix. Annu. Rev. Cell Dev. Biol. 26, 397-419.
71. Sottile, J. (2004). Regulation of angiogenesis by extracellular matrix. Biochim. Biophys. Acta 1654, 13-22.
72. Sottile, J. and Chandler, J. (2005). Fibronectin matrix turnover occurs through a caveolin-1-dependent process. Mol. Biol. Cell 16, 757-768.
73. Sottile, J. and Hocking, D. C. (2002). Fibronectin polymerization regulates the composition and stability of extracellular matrix fibrils and cell-matrix adhesions. Mol. Biol. Cell 13, 3546-3559.
74. Sottile, J., Hocking, D. C. and Swiatek, P. (1998). Fibronectin matrix assembly enhances adhesion-dependent cell growth. J. Cell Sci. 111, 2933-2943.
75. Sottile, J., Shi, F., Rublyevska, I., Chiang, H. Y., Lust, J. and Chandler, J. (2007). Fibronectin-dependent collagen I deposition modulates the cell response to fibronectin. Am. J. Physiol. Cell Physiol. 293, C1934-C1946.
76. Spinale, F. G. (2007). Myocardial matrix remodeling and the matrix metalloproteinases: influence on cardiac form and function. Physiol. Rev. 87, 1285-1342.
77. Streuli, C. (1999). Extracellular matrix remodelling and cellular differentiation. Curr. Opin. Cell Biol. 11, 634-640.
78. Todaro, G. and Green, H. (1963). Quantitative studies of the growth of mouse embryo cells in culture and their development into established lines. J. Cell Biol. 17, 299-313.
79. Tomasini-Johansson, B. R., Kaugman, N. R., Ensenberger, M. G., Ozeri, V., Hanski, E. and Mosher, D. F. (2001). A 49-residue peptide from adhesin F1 of Streptococcus pyogenes inhibits fibronectin matrix assembly. J. Biol. Chem. 276, 23430-23439.
80. van der Rest, M. and Garrone, R. (1991). Collagen family of proteins. FASEB J. 5, 2814-2823.
81. Velling, T., Risteli, J., Wennerberg, K., Mosher, D. F. and Johansson, S. (2002). Polymerization of type I and III collagens is dependent on fibronectin and enhanced by integrins alpha 11beta 1 and alpha 2beta 1. J. Biol. Chem. 277, 37377-37381.
82. Visse, R. and Nagase, H. (2003). Matrix metalloproteinases and tissue inhibitors of metalloproteinases: structure, function, and biochemistry. Circ. Res. 92, 827-839.
83. Watanabe, K., Takahashi, H., Habu, Y., Kamiya-Kubushiro, N., Kamiya, S., Nakamura, H., Yajima, H., Ishii, T., Katayama, T., Miyazaki, K. et al. (2000). Interaction with heparin and matrix metalloproteinase 2 cleavage expose a cryptic anti-adhesive site of fibronectin. Biochemistry 39, 7138-7144.
84. Xu, J., Rodriguez, D., Petitclerc, E., Kim, J. J., Hangai, M., Yuen, S. M., Davis, G. E. and Brooks, P. C. (2001). Proteolytic exposure of a cryptic site within collagen type IV is required for angiogenesis and tumor growth in vivo. J. Cell Biol. 154, 1069-1079.