Tumor cell traffic through the extracellular matrix is controlled by the membrane-anchored collagenase MT1-MMP

Journal of Cell Biology

Volumn 167, Issue 4, 2004, Pages 769-781

  Sabeh, Farideh ^a   Ota, Ichiro ^a   Holmbeck, Kenn ^b   Birkedal Hansen, Henning ^b   Soloway, Paul ^c   Balbin, Milagros ^d   Lopez Otin, Carlos ^d   Shapiro, Steven ^e   Inada, Masaki ^e   Krane, Stephen ^e   Allen, Edward ^a   Chung, Duane ^a   Weiss, Stephen J ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b NATIONAL INSTITUTE OF DENTAL AND CRANIOFACIAL RESEARCH   (United States)

^c Cornell University ^*  (United States)

^d UNIVERSITY OF OVIEDO   (Spain)

^e MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGENASE; COLLAGENASE 2; COLLAGENASE 3; GELATINASE A; GELATINASE B; MATRIX METALLOPROTEINASE; MATRIX METALLOPROTEINASE 14; PLASMINOGEN; STROMELYSIN; TISSUE INHIBITOR OF METALLOPROTEINASE 2; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL ACTIVITY; CELL INVASION; CELL ISOLATION; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVITY; EXTRACELLULAR MATRIX; FIBROBLAST; GENE TARGETING; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; TUMOR CELL;

ANIMALS; CELL MEMBRANE; CELL MOVEMENT; CELLS, CULTURED; CHICK EMBRYO; COCULTURE TECHNIQUES; COLLAGEN; COLLAGENASES; EXTRACELLULAR MATRIX; FIBROBLASTS; GENE TARGETING; MATRIX METALLOPROTEINASE 13; MATRIX METALLOPROTEINASE 14; MATRIX METALLOPROTEINASE 2; MATRIX METALLOPROTEINASE 3; MATRIX METALLOPROTEINASE 9; MATRIX METALLOPROTEINASES, MEMBRANE-ASSOCIATED; METALLOENDOPEPTIDASES; MICE; MICE, KNOCKOUT; NEOPLASM INVASIVENESS; NEOPLASMS; PHENOTYPE;

ANIMALIA;

EID: 9444290419     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.200408028     Document Type: Article

References (59)

1. Armstrong, P.B., J.P. Quigley, and E. Sidebottom. 1982. Transepithelial invasion and intramesenchymal infiltration of the chick embryo chorioallantois by tumor cell lines. Cancer Res. 42:1826-1837.
2. Balbin, M., A. Fueyo, V. Knauper, J.M. Lopez, J. Alvarez, L.M. Sanchez, V. Quesada, J. Bordallo, G. Murphy, and V. Lopez-Otin. 2001. Identification and enzymatic characterization of two diverging murine counter-parts of human interstitial collagenase (MMP-1) expressed at sites of embryo implantation. J. Biol. Chem. 276:10253-10262.
3. Balbin, M., A. Fueyo, A.M. Tester, A.M. Pendas, A.S. Pitiot, A. Astudillo, C.M. Overall, S.D. Shapiro, and C. Lopez-Otin. 2003. Loss of collagen-2 confers increased skin tumor susceptibility to male mice. Nat. Genet. 35:252-257.
4. Benbow, U., M.P. Schoenermark, T.I. Mitchell, J.L. Rutter, K. Shimokawa, H. Nagase, and C.E. Brinckerhoff. 1999. A novel host/tumor cell interaction activates matrix metalloproteinase 1 and mediates invasion through type I collagen. J. Biol. Chem. 274:25371-25378.
5. Birkedal-Hansen, H. 1987. Catabolism and turnover of collagens: collagenases. Methods Enzymol. 144:140-171.
6. Brinckerhoff, C.E., and L.M. Matrisian. 2002. Matrix metalloproteinases: a tail of a frog that became a prince. Nat. Rev. Mol. Cell Biol. 3:207-214.
7. Bullard, K.M., L. Lund, J.S. Mudgett, T.N. Mellin, T.K. Hunt, B. Murphy, J. Ronan, Z. Werb, and M.J. Banda. 1999. Impaired wound contraction in stromelysin-1-deficient mice. Ann. Surg. 230:260-265.
8. Capaldi, M.J., and J.A. Chapman. 1982. The C-terminal extrahelical peptide of type I collagen and its role in fibrillogenesis in vitro. Biopolymers. 21:2291-2313.
9. Caulfield, J.B., and T.K. Borg. 1979. The collagen network of the heart. Lab. Invest. 40:364-372.
10. Chambers, A.F., A.C. Groom, and I.D. MacDonald. 2002. Dissemination and growth of cancer cells in metastatic sites. Nat. Rev. Cancer. 2:563-572.
11. Creemers, L.B., D.C. Jansen, A. van Veen-Reurings, T. van den Bos, and V. Everts. 1997. Microassay for the assessment of low levels of hydroxyproline. Biotechniques. 22:656-658.
12. Cukierman, E., R. Pankov, and K.M. Yamada. 2002. Cell interactions with three-dimensional matrices. Curr. Opin. Cell Biol. 14:633-639.
13. Dong, J., J. Grunstein, M. Tejada, F. Peale, G. Frantz, W.-C. Liang, W. Bai, L. Yu, J. Kowalski, X. Liang, et al. 2004. VEGF-null cells require PDG-FRα signaling-mediated stromal fibroblast recruitment for tumorigenesis. EMBO J. 23:2800-2810.
14. 1 integrin upon release from keratinocytes migrating on type I collagen. J. Biol. Chem. 276:29368-29374.
15. Egeblad, M., and Z. Werb. 2002. New functions for the matrix metalloproteinases in cancer progression. Nat. Rev. Cancer. 2:161-174.
16. Ellerbroek, S.M., Y.I. Wu, C.M. Overall, and M.S. Stack. 2001. Functional interplay between type I collagen and cell surface matrix metalloproteinase activity. J. Biol. Chem. 276:24833-24842.
17. Friedl, P., and K. Wolf. 2003. Tumour-cell invasion and migration: diversity and escape mechanisms. Nat. Rev. Cancer. 3:362-374.
18. Ghersi, G., H. Dong, L.A. Goldstein, Y. Yeh, L. Hakkinen, H.S. Larjava, and W.-T. Chen. 2002. Regulation of fibroblast migration on collagenous matrix by a cell surface peptidase complex. J. Biol. Chem. 277:29231-29241.
19. Grinnell, F. 2003. Fibroblast biology in three-dimensional collagen matrices. Trends Cell Biol. 13:264-269.
20. Hanahan, D., and R.A. Weinberg. 2000. The hallmarks of cancer. Cell. 100:57-70.
21. Havemose-Poulsen, A., P. Holmstrup, K. Stoltze, and H. Birkedal-Hansen. 1998. Dissolution of type I collagen fibrils by gingival fibroblasts isolated from patients of various peridontitis categories. J. Periodontal Res. 33:280-291.
22. Hay, E.D. 1991. Cell Biology of Extracellular Matrix. Plenum Press, New York. 417 pp.
23. Hiraoka, N., E. Allen, I. Apel, M.R. Gyetko, and S.J. Weiss. 1998. Matrix metalloproteinases regulate neovascularization by acting as pericellular fibrinolysins. Cell. 95:365-377.
24. Hlubek, F., S. Spaderna, A. Jung, T. Kirchner, and T. Brabletz. 2004. β-Catenin activates a coordinated expression of the proinvasive factors laminin-5 γ2 chain and MT1-MMP in colorectal carcinomas. Int. J. Cancer. 108:321-326.
25. Hollander, A.P., I. Pidoux, A. Reiner, C. Rorabeck, R. Bourne, and A.R. Poole. 1995. Damage to type II collagen in aging and osteoarthritis starts at the articular surface, originates around chondrocytes, and extends into the artilage with progressive degeneration. J. Clin. Invest. 96:2859-2869.
26. Holmbeck, K., P. Bianco, J. Caterina, S. Yamada, M. Kromer, S.A. Kuznetsov, M. Mankani, P.G. Robey, A.R. Poole, I. Pidoux, et al. 1999. MT1-MMP-deficient mice develop dwarfism, osteopenia, arthritis, and connective tissue disease due to inadequate collagen turnover. Cell. 99:81-92.
27. Holopainen, J.M., J.A.O. Moilanen, T. Sorsa, M. Kivela-Rajamaki, T. Tervahartiala, M.H. Vesaluoma, and T.M.T. Tervo. 2003. Activation of matrix metalloproteinase-8 by membrane type 1-MMP and their expression in human tears after photorefractive keratectomy. Invest. Ophthalmol. Vis. Sci. 44:2550-2556.
28. Hotary, K., E. Allen, A. Punturieri, I. Yana, and S.J. Weiss. 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.
29. Hotary, K.B., I. Yana, F. Sabeh, X.-Y. Li, K. Holmbeck, H. Birkedal-Hansen, E.D. Allen, N. Hiraoka, and S.J. Weiss. 2002. Matrix metalloproteinases (MMPs) regulate fibrin-invasive activity via MT1-MMP-dependent and -independent processes. J. Exp. Med. 195:295-308.
30. Hotary, K.B., E.D. Allen, P.C. Brooks, N.S. Datta, M.W. Long, and S.J. Weiss. 2003. Membrane type-1 matrix metalloproteinase usurps tumor growth control imposed by the three-dimensional extracellular matrix. Cell. 114:33-45.
31. Huber, A.R., and S.J. Weiss. 1989. Disruption of the subendothelial basement membrane during neutrophil diapedesis in an in vitro construct of the vessel wall. J. Clin. Invest. 83:1122-1136.
32. Iida, J., K.L. Wilhelmson, M.A. Price, C.M. Wilson, D. Pei, L.T. Furcht, and J.B. McCarthy. 2004. Membrane type-1 matrix metalloproteinase promotes human melanoma invasion and growth. J. Invest. Dermatol. 122:167-176.
33. Itoh, T., M. Tanioka, H. Yoshida, T. Yoshioka, H. Nishimoto, and S. Itohara. 1998. Reduced angiogenesis and tumor progression in gelatinase A-deficientmice. Cancer Res. 58:1048-1051.
34. Kim, J., W. Yu, K. Kovalski, and L. Ossowski. 1998. Requirement for specific proteases in cancer cell intravasation as revealed by a novel semiquantitative PCR-based assay. Cell. 94:353-362.
35. Kleinman, H.K., M.L. McGarvey, L.A. Liotta, P.G. Robey, K. Tryggvason, and G.R. Martin. 1982. Isolation and characterization of type IV procollagen, laminin, and heparin sulfate proteoglycan from the EHS sarcoma. Biochemistry. 21:6188-6193.
36. Liu, Z., J.M. Shipley, T. Vu, X. Zhou, Z. Diaz, Z. Werb, and R.M. Senior. 1998. Gelatinase B-deficient mice are resistant to experimental bullous pemphigoid. J. Exp. Med. 188:475-482.
37. Matrisian, L.M., G.W. Sledge Jr., and S. Mohla. 2003. Extracellular proteolysis and cancer: meeting summary and future directions. Cancer Res. 63:6105-6109.
38. Mays, P.K., J.E. Bishop, and G.J. Laurent. 1988. Age-related changes in the proportion of types I and III collagen. Mech. Ageing Dev. 45:203-212.
39. Mudgett, J.S., N.I. Hutchinson, N.M.A. Chartrain, A.J. Forsyth, J. McDonnel, I.I. Singel, E.K. Bayne, J. Flanagan, D. Kawaka, C.F. Shen, et al. 1998. Susceptibility of stromelysin I-deficient mice to collagen-induced arthritis and cartilage destruction. Arthritis Rheum. 41:110-121.
40. Murphy, G., and J. Gavrilovic. 1999. Proteolysis and cell migration: creating a path? Curr. Opin. Cell Biol. 11:614-621.
41. Netzel-Arnett, S., D.J. Mitola, S.S. Yamada, K. Chrysovergis, K. Holmbeck, H. Birkedal-Hansen, and T.H. Bugge. 2002. Collagen dissolution by keratinocytes requires cell surface plasminogen activation and matrix metalloproteinase activity. J. Biol. Chem. 277:45154-45161.
42. Niedermeyer, J., M. Kirz, F. Hilberg, P. Garin-Chesa, U. Bamberger, M.C. Lenter, J.B. Park, H. Puschner, M. Mauz, W.J. Rettig, and A. Schnapp. 2000. Targeted disruption of mouse fibroblast activation protein. Mol. Cell. Biol. 20:1089-1094.
43. Okada, A., C. Tomasetto, Y. Lutz, J.-P. Bellocq, M.-C. Rio, and P. Basset. 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.
44. Ploplis, V., P. Carmeliet, S. Vazirzadeh, I. Van Vlaenderen, L. Moons, E. Plow, and D. Collen. 1995. Effects of disruption of the plasminogen gene on thrombosis, growth, and health in mice. Circulation. 92:2585-2593.
45. Ramaswamy, S., K.N. Ross, E.S. Lander, and T.R. Golub. 2003. A molecular signature of metastasis in primary solid tumors. Nat. Genet. 33:49-54.
46. Ramos-DeSimone, N., E. Hahn-Dantona, J. Sipley, H. Nagase, D.L. Franch, and J.P. Quigley. 1999. Activation of matrix metalloproteinase-9 (MMP-9) via a converging plasmin/stromelysin-1 cascade enhances tumor cell invasion. J. Biol. Chem. 274:13066-13076.
47. Sahai, E., and C.J. Marshall. 2003. Differing modes of tumour cell invasion have distinct requirements for Rho/ROCK signaling and extracellular proteolysis. Nat. Cell Biol. 5:711-719.
48. Sawhney, R.K., and J. Howard. 2002. Slow local movements of collagen fibers by fibroblasts drive the rapid global self-organization of collagen gels. J. Cell Biol. 157:1083-1091.
49. Scacheri, P.C., O. Rozenblatt-Rosen, N.J. Caplen, T.G. Wolfsberg, L. Umayam, J.C. Lee, C.M. Hughes, K.S. Shanmugam, A. Bhattacharjee, M. Meyerson, and F.S. Collins. 2004. Short interfering RNAs can induce unexpected and divergent changes in the levels of untargeted proteins in mammalian cells. Proc. Natl. Acad. Sci. USA. 101:1892-1897.
50. Seiki, M., N. Koshikawa, and I. Yana. 2003. Role of pericellular proteolysis by membrane-type I matrix metalloproteinase in cancer invasion and angiogenesis. Cancer Metastasis Rev. 22:129-143.
51. Snowden, J.M., and D.A. Swann. 1979. The formation and thermal stability of in vitro assembled fibrils from acid-soluble and pepsin-treated collagens. Biochim. Biophys. Acta. 580:372-381.
52. Tam, E.M., Y.I. Wu, G.S. Butler, M.S. Stack, and C.M. Overall. 2002. Collagen binding properties of the membrane type-1 matrix metalloproteinase (MT1-MMP) hemopexin C domain. J. Biol. Chem. 277:39005-39014.
53. Thiery, J.P. 2002. Epithelial-mesenchymal transitions in tumour progression. Nat. Rev. Cancer. 2:442-454.
54. Turk, V., J. Kos, and B. Turk. 2004. Cysteine cathepsins (proteases)-on the main stage of cancer? Cancer Cell. 5:409-410.
55. Ueda, J., M. Kajita, N. Suenaga, K. Fujii, and M. Seiki. 2003. Sequence-specific silencing of MT1-MMP expression suppresses tumor cell migration and invasion: importance of MT1-MMP as a therapeutic target for invasion tumors. Oncogene. 22:8716-8722.
56. Wang, Z., R. Juttermann, and P.D. Soloway. 2000. TIMP-2 is required for efficient activation of proMMP-2 in vivo. J. Biol. Chem. 275:26411-26415.
57. Weiss, S.J. 1989. Tissue destruction by human neutrophils. N. Engl. J. Med. 320:365-376.
58. Wolf, K., I. Mazo, H. Leung, K. Engelke, U.H. von Andrian, E.I. Deryugina, A.Y. Strongin, E.-B. Brocker, and P. Friedl. 2003. Compensation mechanism in tumor cell migration: mesenchymal-amoeboid transition after blocking of pericellular proteolysis. J. Cell Biol. 160:267-277.
59. Wu, N., S. Opalenik, J. Liu, E.D. Jansen, M.G. Giro, and J.M. Davidson. 2002. Real-time visualization of MMP-13 promoter activity in transgenic mice. Matrix Biol. 21:149-161.