The effect of MMP inhibitor GM6001 on early fibroblast-mediated collagen matrix contraction is correlated to a decrease in cell protrusive activity

European Journal of Cell Biology

Volumn 90, Issue 1, 2011, Pages 26-36

  Martin Martin, Belen ^a   Tovell, Victoria ^a   Dahlmann Noor, Annegret ^b   Khaw, Peng ^b   Bailly, Maryse ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b MOORFIELDS EYE HOSPITAL   (United Kingdom)

Author keywords

Cell dynamics; Matrix contraction; MMP inhibitor

Indexed keywords

COLLAGEN FIBER; ILOMASTAT;

ARTICLE; CELL ACTIVITY; CELL MIGRATION; CELL NUCLEUS MATRIX; CELL PROLIFERATION; CELL STRUCTURE; CELL VIABILITY; CONTROLLED STUDY; FIBROBLAST; HUMAN; HUMAN CELL; MUSCLE FIBER CONTRACTION; PRIORITY JOURNAL;

ANIMALS; CELL LINE; CELL MOVEMENT; CELL SHAPE; COLLAGEN; DIPEPTIDES; EXTRACELLULAR MATRIX; FIBROBLASTS; HUMANS; MATRIX METALLOPROTEINASES; MICE; MICROSCOPY, CONFOCAL; STAINING AND LABELING; WOUND HEALING;

EID: 78649460225     PISSN: 01719335     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ejcb.2010.09.008     Document Type: Article

References (42)

1. Bailly M., Yan L., Whitesides G.M., Condeelis J.S., Segall J.E. Regulation of protrusion shape and adhesion to the substratum during chemotactic responses of mammalian carcinoma cells. Exp Cell Res 1998, 241:285-299.
2. Bell E., Ivarsson B., Merrill C. Production of a tissue-like structure by contraction of collagen lattices by human fibroblasts of different proliferative potential in vitro. Proc Natl Acad Sci USA 1979, 76:1274-1278.
3. Brightman A.O., Rajwa B.P., Sturgis J.E., McCallister M.E., Robinson J.P., Voytik-Harbin S.L. Time-lapse confocal reflection microscopy of collagen fibrillogenesis and extracellular matrix assembly in vitro. Biopolymers 2000, 54:222-234.
4. Bullard K.M., Lund L., Mudgett J.S., Mellin T.N., Hunt T.K., Murphy B., Ronan J., Werb Z., Banda M.J. Impaired wound contraction in stromelysin-1-deficient mice. Ann Surg 1999, 230:260-265.
5. Cooke M.E., Sakai T., Mosher D.F. Contraction of collagen matrices mediated by alpha2beta1A and alpha(v)beta3 integrins. J Cell Sci 2000, 113(Pt 13):2375-2383.
6. Dahlmann-Noor A.H., Martin-Martin B., Eastwood M., Khaw P.T., Bailly M. Dynamic protrusive cell behaviour generates force and drives early matrix contraction by fibroblasts. Exp Cell Res 2007, 313:4158-4169.
7. Daniels J.T., Cambrey A.D., Occleston N.L., Garrett Q., Tarnuzzer R.W., Schultz G.S., Khaw P.T. Matrix metalloproteinase inhibition modulates fibroblast-mediated matrix contraction and collagen production in vitro. Invest Ophthalmol Vis Sci 2003, 44:1104-1110.
8. Daniels J.T., Khaw P.T. Temporal stimulation of corneal fibroblast wound healing activity by differentiating epithelium in vitro. Invest Ophthalmol Vis Sci 2000, 41:3754-3762.
9. DeMali K.A., Wennerberg K., Burridge K. Integrin signaling to the actin cytoskeleton. Curr Opin Cell Biol 2003, 15:572-582.
10. DesMarais V., Macaluso F., Condeelis J., Bailly M. Synergistic interaction between the Arp2/3 complex and cofilin drives stimulated lamellipod extension. J Cell Sci 2004, 117:3499-3510.
11. Finlay G.A., Thannickal V.J., Fanburg B.L., Paulson K.E. Transforming growth factor-beta 1-induced activation of the ERK pathway/activator protein-1 in human lung fibroblasts requires the autocrine induction of basic fibroblast growth factor. J Biol Chem 2000, 275:27650-27656.
12. Grinnell F. Fibroblasts, myofibroblasts, and wound contraction. J Cell Biol 1994, 124:401-404.
13. Grinnell F. Fibroblast biology in three-dimensional collagen matrices. Trends Cell Biol 2003, 13:264-269.
14. Hooper S., Marshall J.F., Sahai E. Tumor cell migration in three dimensions. Methods Enzymol 2006, 406:625-643.
15. Hotary K.B., Allen E.D., Brooks P.C., Datta N.S., Long M.W., Weiss S.J. Membrane type I matrix metalloproteinase usurps tumor growth control imposed by the three-dimensional extracellular matrix. Cell 2003, 114:33-45.
16. Ignotz R.A., Massague J. Transforming growth factor-beta stimulates the expression of fibronectin and collagen and their incorporation into the extracellular matrix. J Biol Chem 1986, 261:4337-4345.
17. Kato T., Saika S., Ohnishi Y. Effects of the matrix metalloproteinase inhibitor GM6001 on the destruction and alteration of epithelial basement membrane during the healing of post-alkali burn in rabbit cornea. Jpn J Ophthalmol 2006, 50:90-95.
18. Langholz O., Rockel D., Mauch C., Kozlowska E., Bank I., Krieg T., Eckes B. Collagen and collagenase gene expression in three-dimensional collagen lattices are differentially regulated by alpha 1 beta 1 and alpha 2 beta 1 integrins. J Cell Biol 1995, 131:1903-1915.
19. Lee M.A., Palace J., Stabler G., Ford J., Gearing A., Miller K. Serum gelatinase B, TIMP-1 and TIMP-2 levels in multiple sclerosis. A longitudinal clinical and MRI study. Brain 1999, 122(Pt 2):191-197.
20. Li X.Y., Ota I., Yana I., Sabeh F., Weiss S.J. Molecular dissection of the structural machinery underlying the tissue-invasive activity of membrane type-1 matrix metalloproteinase. Mol Biol Cell 2008, 19:3221-3233.
21. Mirastschijski U., Haaksma C.J., Tomasek J.J., Agren M.S. Matrix metalloproteinase inhibitor GM 6001 attenuates keratinocyte migration, contraction and myofibroblast formation in skin wounds. Exp Cell Res 2004, 299:465-475.
22. Page-McCaw A., Ewald A.J., Werb Z. Matrix metalloproteinases and the regulation of tissue remodelling. Nat Rev Mol Cell Biol 2007, 8:221-233.
23. Phillips J.A., Vacanti C.A., Bonassar L.J. Fibroblasts regulate contractile force independent of MMP activity in 3D-collagen. Biochem Biophys Res Commun 2003, 312:725-732.
24. Ravanti L., Kahari V.M. Matrix metalloproteinases in wound repair (review). Int J Mol Med 2000, 6:391-407.
25. Romer J., Bugge T.H., Pyke C., Lund L.R., Flick M.J., Degen J.L., Dano K. Impaired wound healing in mice with a disrupted plasminogen gene. Nat Med 1996, 2:287-292.
26. Ross R., Odland G. Human wound repair. II. Inflammatory cells, epithelial-mesenchymal interrelations, and fibrogenesis. J Cell Biol 1968, 39:152-168.
27. Sabeh F., Fox D., Weiss S.J. Membrane-type I matrix metalloproteinase-dependent regulation of rheumatoid arthritis synoviocyte function. J Immunol 2010, 184:6396-6406.
28. Sabeh F., Li X.Y., Saunders T.L., Rowe R.G., Weiss S.J. Secreted versus membrane-anchored collagenases: relative roles in fibroblast-dependent collagenolysis and invasion. J Biol Chem 2009, 284:23001-23011.
29. Sabeh F., Ota I., Holmbeck K., Birkedal-Hansen H., Soloway P., Balbin M., Lopez-Otin C., Shapiro S., Inada M., Krane S., et al. Tumor cell traffic through the extracellular matrix is controlled by the membrane-anchored collagenase MT1-MMP. J Cell Biol 2004, 167:769-781.
30. Sabeh F., Shimizu-Hirota R., Weiss S.J. Protease-dependent versus -independent cancer cell invasion programs: three-dimensional amoeboid movement revisited. J Cell Biol 2009, 185:11-19.
31. Sanz-Moreno V., Gadea G., Ahn J., Paterson H., Marra P., Pinner S., Sahai E., Marshall C.J. Rac activation and inactivation control plasticity of tumor cell movement. Cell 2008, 135:510-523.
32. Scott K.A., Wood E.J., Karran E.H. A matrix metalloproteinase inhibitor which prevents fibroblast-mediated collagen lattice contraction. FEBS Lett 1998, 441:137-140.
33. Shao D., Forge A., Munro P.M., Bailly M. Arp2/3 complex-mediated actin polymerisation occurs on specific pre-existing networks in cells and requires spatial restriction to sustain functional lamellipod extension. Cell Motil Cytoskeleton 2006, 63:395-414.
34. Sternlicht M.D., Werb Z. How matrix metalloproteinases regulate cell behavior. Annu Rev Cell Dev Biol 2001, 17:463-516.
35. Tomasek J.J., Gabbiani G., Hinz B., Chaponnier C., Brown R.A. Myofibroblasts and mechano-regulation of connective tissue remodelling. Nat Rev Mol Cell Biol 2002, 3:349-363.
36. Townley W.A., Cambrey A.D., Khaw P.T., Grobbelaar A.O. Matrix metalloproteinase inhibition reduces contraction by dupuytren fibroblasts. J Hand Surg Am 2008, 33:1608-1616.
37. Wolf K., Mazo I., Leung H., Engelke K., von Andrian U.H., Deryugina E.I., Strongin A.Y., Brocker E.B., Friedl P. Compensation mechanism in tumor cell migration: mesenchymal-amoeboid transition after blocking of pericellular proteolysis. J Cell Biol 2003, 160:267-277.
38. Wong T.T., Daniels J.T., Crowston J.G., Khaw P.T. MMP inhibition prevents human lens epithelial cell migration and contraction of the lens capsule. Br J Ophthalmol 2004, 88:868-872.
39. Wong T.T., Mead A.L., Khaw P.T. Prolonged antiscarring effects of ilomastat and MMC after experimental glaucoma filtration surgery. Invest Ophthalmol Vis Sci 2005, 46:2018-2022.
40. Wong T.T., Sethi C., Daniels J.T., Limb G.A., Murphy G., Khaw P.T. Matrix metalloproteinases in disease and repair processes in the anterior segment. Surv Ophthalmol 2002, 47:239-256.
41. Ylisirnio S., Hoyhtya M., Turpeenniemi-Hujanen T. Serum matrix metalloproteinases -2, -9 and tissue inhibitors of metalloproteinases -1,-2 in lung cancer--TIMP-1 as a prognostic marker. Anticancer Res 2000, 20:1311-1316.
42. Zhu Y.K., Umino T., Liu X.D., Wang H.J., Romberger D.J., Spurzem J.R., Rennard S.I. Contraction of fibroblast-containing collagen gels: initial collagen concentration regulates the degree of contraction and cell survival. In Vitro Cell Dev Biol Anim 2001, 37:10-16.