Cell surface collagenolysis requires homodimerization of the membrane-bound collagenase MT1-MMP

Molecular Biology of the Cell

Volumn 17, Issue 12, 2006, Pages 5390-5399

  Itoh, Yoshifumi ^a   Ito, Noriko ^a   Nagase, Hideaki ^a   Evans, Richard D ^a   Bird, Sarah A ^a   Seiki, Motoharu ^b  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN FIBER; COLLAGEN TYPE 1; COLLAGENASE 3; HEMOPEXIN; HOMODIMER; INTERSTITIAL COLLAGENASE; MATRIX METALLOPROTEINASE 14; MEMBRANE ENZYME; MONOMER;

ANIMAL CELL; ARTICLE; CELL MIGRATION; CELL SURFACE; COLLAGEN DEGRADATION; COMPLEX FORMATION; CONTROLLED STUDY; DIMERIZATION; ENZYMATIC DEGRADATION; ENZYME ACTIVITY; ENZYME MECHANISM; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION;

ANIMALS; CELL MEMBRANE; CERCOPITHECUS AETHIOPS; COLLAGEN TYPE I; COLLAGENASES; COS CELLS; DIMERIZATION; DOGS; GELS; HUMANS; MATRIX METALLOPROTEINASE 13; MATRIX METALLOPROTEINASE 14; MEMBRANE PROTEINS; MUTANT PROTEINS; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS;

EID: 33845396458     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E06-08-0740     Document Type: Article

References (47)

1. Anilkumar, N., Uekita, T., Couchman, J. R., Nagase, H., Seiki, M., and Itoh, Y. (2005). Palmitoylation at Cys574 is essential for MT1-MMP to promote cell migration. FASEB J. 19, 1326-1328.
2. Bai, S., Thummel, R., Godwin, A. R., Nagase, H., Itoh, Y., Li, L., Evans, R., McDermott, J., Seiki, M., and Sarras, M. P., Jr. (2005). Matrix metalloproteinase expression and function during fin regeneration in zebrafish: analysis of MT1-MMP, MMP2 and T1MP2. Matrix Biol. 24, 247-260.
3. Belkin, A. M., Akimov, S. S., Zaritskaya, L. S., Ratnikov, B. I., Deryugina, E. I., and Strongin, A. Y. (2001). Matrix-dependent proteolysis of surface transglutaminase by membrane-type metalloproteinase regulates cancer cell adhesion and locomotion. J. Biol. Chem. 276, 18415-18422.
4. Bode, W., Reinemer, P., Huber, R., Kleine, T., Schnierer, S., and Tschesche, H. (1994). The X-ray crystal structure of the catalytic domain of human neutrophil collagenase inhibited by a substrate analogue reveals the essentials for catalysis and specificity. EMBO J. 13, 1263-1269.
5. Borkakoti, N., Winkler, F. K., Williams, D. H., D'Arcy, A., Broadhurst, M. J., Brown, P. A., Johnson, W. H., and Murray, E. J. (1994). Structure of the catalytic domain of human fibroblast collagenase complexed with an inhibitor. Nat. Struct. Biol. 1, 106-110.
6. Cawston, T. E. (1996). Metalloproteinase inhibitors and the prevention of connective tissue breakdown. Pharmacol. Ther. 70, 163-182.
7. 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.
8. Chung, L., Dinakarpandian, D., Yoshida, N., Lauer-Fields, J. L., Fields, G. B., Visse, R., and Nagase, H. (2004). Collagenase unwinds triple-helical collagen prior to peptide bond hydrolysis. EMBO J. 23, 3020-3030.
9. Clark, I. M., and Cawston, T. E. (1989). Fragments of human fibroblast collagenase. Purification and characterization. Biochem. J. 263, 201-206.
10. d'Ortho, M. P., Will, H., Atkinson, S., Butler, G., Messent, A., Gavrilovic, J., Smith, B., Timpl, R., Zardi, L., and Murphy, G. (1997). Membrane-type matrix metalloproteinases 1 and 2 exhibit broad-spectrum proteolytic capacities comparable to many matrix metalloproteinases. Eur. J. Biochem. 250, 751-757.
11. Ellerbroek, S. M., Wu, Y. I., Overall, C. M., and Stack, M. S. (2001). Functional interplay between type I collagen and cell surface matrix metalloproteinase activity. J. Biol. Chem. 276, 24833-24842.
12. Endo, K., Takino, T., Miyamori, H., Kinsen, H., Yoshizaki, T., Furukawa, M., and Sato, H. (2003). Cleavage of syndecan-1 by membrane type matrix metalloproteinase-1 stimulates cell migration. J. Biol. Chem. 278, 40764-40770.
13. Hiraoka, N., Allen, E., Apel, I. J., Gyetko, M. R., and Weiss, S. J. (1998). Matrix metalloproteinases regulate neovascularization by acting as pericellular fibrinolysins. Cell 95, 365-377.
14. Ho, S. N., Hunt, H. D., Horton, R. M., Pullen, J. K., and Pease, L. R. (1989). Site-directed mutagenesis by overlap extension using the polymerase chain reaction [see comments]. Gene 77, 51-59.
15. Holmbeck, K., et al. (1999). MT1-MMP-deficient mice develop dwarfism, osteopenia, arthritis, and connective tissue disease due to inadequate collagen turnover. Cell 99, 81-92.
16. Holmbeck, K., Bianco, P., Yamada, S., and Birkedal-Hansen, H. (2004). MT1-MMP: a tethered collagenase. J. Cell Physiol. 200, 11-19.
17. 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.
18. 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.
19. Huang, W., Suzuki, K., Nagase, H., Arumugam, S., Van Doren, S. R., and Brew, K. (1996). Folding and characterization of the amino-terminal domain of human tissue inhibitor of metalloproteinases-1 (TIMP-1) expressed at high yield in E. coli. FEBS Lett. 384, 155-161.
20. Itoh, Y., Ito, A., Iwata, K., Tanzawa, K., Mori, Y., and Nagase, H. (1998). Plasma Membrane-bound tissue inhibitor of metalloproteinases (TIMP)-2 specifically inhibits matrix metalloproteinase 2 (Gelatinase A) activated on the cell surface. J. Biol. Chem. 273, 24360-24367.
21. Itoh, Y., Kajita, M., Kinoh, H., Mori, H., Okada, A., and Seiki, M. (1999). Membrane Type 4 matrix metalloproteinase (MT4-MMP, MMP-17) is a glycosylphosphatidylinositol-anchored proteinase. J. Biol. Chem. 274, 34260-34266.
22. Itoh, Y., and Seiki, M. (2006). MT1-MMP: a potent modifier of pericellular microenvironment. J. Cell Physiol. 206, 1-8.
23. Itoh, Y., Takamura, A., Ito, N., Maru, Y., Sato, H., Suenaga, N., Aoki, T., and Seiki, M. (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.
24. Jiang, A., Lehti, K., Wang, X., Weiss, S.J., KeskiOja, 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.
25. Kadono, Y., Shibahara, K., Namiki, M., Watanabe, Y., Seiki, M., and Sato, H. (1998). Membrane type 1-matrix metalloproteinase is involved in the formation of hepatocyte growth factor/scatter factor-induced branching tubules in madin-darby canine kidney epithelial cells. Biochem. Biophys. Res. Commun. 251, 681-687.
26. Kajita, M., Itoh, Y., Chiba, T., Mori, H., Okada, A., Kinoh, H., and Seiki, M. (2001). Membrane-type 1 matrix metalloproteinase cleaves CD44 and promotes cell migration. J. Cell Biol. 153, 893-904.
27. Knäuper, V., Osthues, A., DeClerck, Y. A., Langley, K. E., Blaser, J., and Tschesche, H. (1993). Fragmentation of human polymorphonuclear-leucocyte collagenase. Biochem. J. 291(Pt 3), 847-854.
28. Knäuper, V., Will, H., López-Otín, C., Smith, B., Atkinson, S. J., Stanton, H., Hembry, R. M., and Murphy, G. (1996). Cellular mechanisms for human procollagenase 3 (mmp 13) activation: evidence that mt1 mmp (mmp 14) and gelatinase a (mmp 2) are able to generate active enzyme. J. Biol. Chem. 273, 17124-17131.
29. 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.
30. Lehti, K., Lohi, J., Juntunen, M. M., Pei, D., and Keski-Oja, J. (2002). Oligomerization through hemopexin and cytoplasmic domains regulates the activity and turnover of membrane-type 1 matrix metalloproteinase. J. Biol. Chem. 277, 8440-8448.
31. Murphy, G., Allan, J. A., Willenbrock, F., Cockett, M. I., O'Connell, J. P., and Docherty, A.J.P. (1992). The role of the C-terminal domain in collagenase and stromelysin specificity. J. Biol. Chem. 267, 9612-9618.
32. Nonaka, T., Nishibashi, K., Itoh, Y., Yana, I., and Seiki, M. (2005). Competitive disruption of the tumor-promoting function of membrane type 1 matrix metalloproteinase/matrix metalloproteinase-14 in vivo. Mol. Cancer Ther. 4, 1157-1166.
33. 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.
34. Okada, A., Tomasetto, C., Lutz, Y., Bellocq, J. P., Rio, M. C., and Basset, P. (1997). Expression of matrix metalloproteinases during rat skin wound healing: evidence that membrane type-1 matrix metalloproteinase is a stromal activator of pro-gelatinase A. J. Cell Biol. 137, 67-77.
35. Patterson, M. L., Atkinson, S. J., Knauper, V., and Murphy, G. (2001). Specific collagenolysis by gelatinase A, MMP-2, is determined by the hemopexin domain and not the fibronectin-like domain. FEBS Lett. 503, 158-162.
36. Ramachandran, G. N., and Kartha, G. (1955). Structure of collagen. Nature 176, 593-595.
37. Ratnikov, B. I., Rozanov, D. V., Postnova, T. I., Baciu, P. G., Zhang, H., DiScipio, R. G., Chestukhina, G. G., Smith, J. W., Deryugina, E. I., and Strongin, A. Y. (2002). An alternative processing of integrin alpha, (v) subunit in tumor cells by membrane type-1 matrix metalloproteinase. J. Biol. Chem. 277, 7377-7385.
38. 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.
39. Sabeh, F., 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.
40. Sato, H., Takino, T., Okada, Y., Cao, J., Shinagawa, A., Yamamoto, E., and Seiki, M. (1994). A matrix metalloproteinase expressed on the surface of invasive tumour cells. Nature 370, 61-65.
41. Seiki, M. (1999). Membrane-type matrix metalloproteinases. Apmis 107, 137-143.
42. Sternlicht, M. D., and Werb, Z. (2001). How matrix metalloproteinases regulate cell behavior. Annu. Rev. Cell Dev. Biol. 17, 463-516.
43. Tam, E. M., Wu, Y. I., Butler, G. S., Stack, M. S., and Overall, C. M. (2002). 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.
44. 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.
45. Visse, R., and Nagase, H. (2003). Matrix metalloproteinases and tissue inhibitors of metalloproteinases: structure, function, and biochemistry. Circ. Res. 92, 827-839.
46. Wolf, K., Mazo, I., Leung, H., Engelke, K., von Andrian, U. H., Deryugina, E. I., Strongin, A. Y., Brocker, E. B., and Friedl, P. (2003). Compensation mechanism in tumor cell migration: mesenchymal-amoeboid transition after blocking of pericellular proteolysis. J. Cell Biol. 160, 267-277.
47. 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.