Functional overlap between two classes of matrix-degrading proteases in wound healing

EMBO Journal

Volumn 18, Issue 17, 1999, Pages 4645-4656

  Lund, Leif R ^a   Rømer, John ^a,c   Bugge, Thomas H ^b,d   Nielsen, Boye S ^a   Frandsen, Thomas L ^a   Degen, Jay L ^b   Stephens, Ross W ^a   Danø, Keld ^a  

^a FINSEN LABORATORY   (Denmark)

^b CINCINNATI CHILDREN S HOSPITAL RESEARCH FOUNDATION   (United States)

^c NOVO NORDISK A S   (Denmark)

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

Author keywords

Keratinocytes; Metalloprotease; Plasminogen; Serine protease; Wound healing

Indexed keywords

COLLAGENASE; FIBRIN; GELATINASE A; GELATINASE B; ILOMASTAT; MATRIX METALLOPROTEINASE; METALLOPROTEINASE INHIBITOR; PLASMINOGEN; PROTEINASE; STROMELYSIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CANCER INVASION; CELL MIGRATION; CONTROLLED STUDY; ENZYME ACTIVITY; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; KERATINOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN DEGRADATION; PROTEIN EXPRESSION; WOUND HEALING;

ANIMALS; CELL MOVEMENT; DIPEPTIDES; GENE EXPRESSION REGULATION, ENZYMOLOGIC; IMMUNOHISTOCHEMISTRY; KERATINOCYTES; METALLOENDOPEPTIDASES; MICE; MICE, INBRED C57BL; PLASMINOGEN; PROTEASE INHIBITORS; SKIN; TIME FACTORS; WOUND HEALING;

EID: 0033199235     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/18.17.4645     Document Type: Article

References (64)

1. Bateman, J.B., Pettit, T.H., Isenberg, S.J. and Simons, K.B. (1986) Ligneous conjunctivitis: an autosomal recessive disorder. J. Pediatr. Ophthalmol. Strabismus, 23, 137-140.
2. Bini, A., Itoh, Y, Kudryk, B.J. and Nagase, H. (1996) Degradation of cross-linked fibrin by matrix metalloproteinase 3 (stromelysin 1): hydrolysis of the gamma Gly404-Ala405 peptide bond. Biochemistry, 35, 13056-13063.
3. Blasi, F. (1993) Urokinase and urokinase receptor: a paracrine/autocrine system regulating cell migration and invasiveness. BioEssays, 15, 105-111.
4. Bouisson, M. (1847) Ophthalmic sur-aigue avec formation de pseudomembranes à la surface de la conjonctive. Ann. Oculist., 17, 100-104.
5. Brown, P.D. (1999) Clinical studies with matrix metalloproteinase inhibitors. Acta Pathol. Microbiol. Scand., 107, 174-180.
6. Bugge, T.H., Flick, M.J., Daugherty, C.C. and Degen, J.L. (1995a) Plasminogen deficiency causes severe thrombosis but is compatible with development and reproduction. Genes Dev., 9, 794-807.
7. Bugge, T.H., Suh, T.T., Flick, M.J., Daugherty, C.C., Rømer, J., Solberg, H., Ellis, V., Danø, K. and Degen, J.L. (1995b) The receptor for urokinase-type plasminogen activator is not essential for mouse development or fertility. J. Biol. Chem., 270, 16886-16894.
8. Bugge, T.H., Kombrinck, K.W., Flick, M.J., Daugherty, C.C., Danton, M.J. and Degen, J.L. (1996) Loss of fibrinogen rescues mice from the pleiotropic effects of plasminogen deficiency. Cell, 87, 709-719.
9. Bugge, T.H., Kombrinck, K.W., Xiao, Q., Holmback, K., Daugherty, C.C., Witte, D.P. and Degen, J.L. (1997) Growth and dissemination of Lewis lung carcinoma in plasminogen-deficient mice. Blood, 90, 4522-4531.
10. Bugge, T.H. et al. (1998) Reduced metastasis of polyoma virus middle T antigen-induced mammary cancer in plasminogen-deficient mice. Oncogene, 16, 3097-3104.
11. Chen, Z.L. and Strickland, S. (1998) Neuronal death in the hippocampus is promoted by plasmin-catalyzed degradation of laminin. Cell, 91, 917-925.
12. Danø, K., Andreasen, P.A., Grøndahl Hansen, J., Kristensen, P., Nielsen, L.S. and Skriver, L. (1985) Plasminogen activators, tissue degradation and cancer. Adv. Cancer Res., 44, 139-266.
13. Danø, K., Behrendt, N., Brünner, N., Ellis, V., Ploug, M. and Pyke, C. (1994) The urokinase receptor: protein structure and role in plasminogen activation and cancer invasion. Fibrinolysis, 8, 189-203.
14. Drew, A.F, Kaufman, A.H., Kombrinck, K.W., Danton, M.J., Daugherty, C.C., Degen, J.L. and Bugge, T.H. (1998) Ligneous conjunctivitis in plasminogen-deficient mice. Blood, 91, 1616-1624.
15. Dvorak, H.F. (1986) Tumors: wounds that do not heal. Similarities between tumor stroma generation and wound healing. N. Engl. J. Med., 315, 1650-1659.
16. Edwards, D.R. and Murphy, C. (1998) Proteases-invasion and more. Nature, 394, 527-528.
17. Galardy, R.E., Grobelny, D., Foellmer, H.G. and Fernandez, L.A. (1994) Inhibition of angiogenesis by the matrix metalloprotease inhibitor N-L-tryptophan methylamide. Cancer Res., 54, 4715-4718.
18. Gijbels, K., Galardy, R.E. and Steinman, L. (1994) Reversal of experimental autoimmune encephalomyelitis with a hydroxamate inhibitor of matrix metalloproteases. J. Clin. Invest., 94, 2177-2182.
19. Grobelny, D., Poncz, L. and Galardy, R.E. (1992) Inhibition of human skin fibroblast collagenase, thermolysin and Pseudomonas aeruginosa elastase by peptide hydroxamic acids. Biochemistry, 31, 7152-7154.
20. Grøndahl-Hansen, J., Lund, L.R., Ralfkiær, E., Ottevanger, V. and Danø, K. (1988) Urokinase- and tissue-type plasminogen activators in keratinocytes during wound reepithelialization in vivo. J. Invest. Dermatol., 90, 790-795.
21. Guo, L., Degenstein, L. and Fuchs, E. (1996) Keratinocyte growth factor is required for hair development but not for wound healing. Genes Dev., 10, 165-175.
22. Hammani, K., Henriet, P. and Eeckhout, Y. (1992) Cloning and sequencing of a cDNA encoding mouse stromelysin I. Gene, 120, 321-322.
23. Henriet, P., Rousseau, G.G. and Eeckhout, Y. (1992) Cloning and sequencing of mouse collagenase cDNA. Divergence of mouse and rat collagenases from the other mammalian collagenases. FEBS Lett., 310, 175-178.
24. Hewitt, R. and Danø, K. (1996) Stromal cell expression of components of matrix-degrading protease systems in human cancer. Enzyme Protein, 49, 163-173.
25. 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.
26. Hydayat, A.A. and Riddle, P.J. (1987) Ligneous conjunctivitis. A clinicopathologic study of 17 cases. Ophthalmology, 94, 949-959.
27. Johnsen, M.J., Lund, L.R., Rømer, J., Almholt, K. and Danø, K. (1998) Cancer invasion and tissue remodeling. Common themes in proteolytic matrix degradation. Curr. Opin. Cell Biol., 1, 667-671.
28. Kim, J., Yu, W., Kovalski, K. and Ossowski, L. (1998) Requirement for specific proteases in cancer cell intravasation as revealed by a novel semiquantitative PCR-based assay. Cell, 94, 353-362.
29. Lefebvre, O., Wolf, C., Limacher, J.M., Hutin, P., Wendling, C., LeMeur, M., Basset, P. and Rio, M.C. (1992) The breast cancer-associated stromelysin-3 gene is expressed during mouse mammary gland apoptosis. J. Cell Biol., 119, 997-1002.
30. Levy, D.E. et al. (1998) Matrix metalloproteinase inhibitors: a structure-activity study. J. Med. Chem., 41, 199-223.
31. Liotta, L.A., Steeg, P.S. and Stetler-Slevenson, W.G. (1991) Cancer metastasis and angiogenesis: an imbalance of positive and negative regulation. Cell, 64, 327-336.
32. Lund, L.R., Rømer, J., Thomasset, N., Solberg, H., Pyke, C., Bissell, M.J., Danø, K. and Werb, Z. (1996) Two distinct phases of apoptosis in mammary gland involution: proteinase-independent and -dependent pathways. Development, 122, 181-193.
33. Mignatti, P. and Rifkin, D.B. (1996) Plasminogen activators and matrix metalloproteinases in angiogenesis. Enzyme Protein, 49, 117-137.
34. Mingers, A.M., Heimburger, N., Zeller, P., Kreth, H.W. and Schuster, V. (1997) Homozygous type I plasminogen deficiency. Semin. Thromb. Hemostasis, 23, 259-264.
35. Moss, M.L. et al. (1997) Cloning of a disintegrin metalloproteinase that processes precursor tumour-necrosis factor-α Nature, 385, 733-736.
36. Mazzieri, R., Masiero, L., Zanetta, L., Monea, S., Onisto, M., Garbisa, S. and Mignatti, P. (1997) Control of type IV collagenase activity by components of the urokinase-plasmin system: a regulatory mechanism with cell-bound reactants. EMBO J., 16, 2319-2332.
37. Murphy, G., Ward, R., Gavrilovic, J. and Atkinson, S. (1992) Physiological mechanisms for metalloproteinase activation. Matrix (Suppl.), 1, 224-230.
38. Pepper, M.S., Vassalli, J.D., Montesano, R. and Orci, L. (1987) Urokinase-type plasminogen activator is induced in migrating capillary endothelial cells. J. Cell Biol., 105, 2535-2541.
39. Peschon, J.J. et al. (1998) An essential role for extodomain shedding in mammalian development. Science, 282, 1281-1284.
40. Ploplis, V.A., Carmeliet, P., Vazirzadeh, S., Van, V.I., Moons, L., Plow, E.F. and Collen, D. (1995) Effects of disruption of the plasminogen gene on thrombosis, growth and health in mice. Circulation, 92, 2585-2593.
41. Reponen, P., Sahlberg, C., Huhtala, P., Hurskainen, T., Thesleff, I. and Tryggvason, K. (1992) Molecular cloning of murine 72-kDa type IV collagenase and its expression during mouse development. J. Biol. Chem., 267, 7856-7862.
42. Reponen, P., Sahlberg, C., Munaut, C., Thesleff, I. and Tryggvason, K. (1994) High expression of 92-kDa type IV collagenase (gelatinase) in the osteoclast lineage during mouse development. Ann. NY Acad. Sci., 732, 472-475.
43. Rinkenberger, J.L., Cross, J.C. and Werb, Z. (1997) Molecular genetics of implantation in the mouse. Dev. Genet., 2, 6-20.
44. Rømer, J., Lund, L.R., Eriksen, J., Ralfkiær, E., Zeheb, R., Gelehrter, T.D., Danø, K. and Kristensen, P. (1991) Differential expression of urokinase-type plasminogen activator and its type-1 inhibitor during healing of mouse skin wounds. J. Invest. Dermatol., 97, 803-811.
45. Rømer, J., Lund, L.R., Eriksen, J., Pyke, C., Kristensen, P. and Danø, K. (1994) The receptor for urokinase-type plasminogen activator is expressed by keratinocytes at the leading edge during reepithelialization of mouse skin wounds. J. Invest. Dermatol., 102, 519-522.
46. Rømer, J., Bugge, T.H., Pyke, C., Lund, L.R., Flick, M.J., Degen, J.L. and Danø, K. (1996) Impaired wound healing in mice with a disrupted plasminogen gene. Nature Med., 2, 287-292.
47. Sappino, A.P., Huarte, J., Belin, D. and Vassalli, J.D. (1989) Plasminogen activators in tissue remodeling and invasion: mRNA localization in mouse ovaries and implanting embryos. J. Cell Biol., 109, 2471-2479.
48. Schott, D. et al. (1998) Successful replacement therapy with a purified plasminogen concentrate in an infant with ligneous conjunctivitis and homozygous plasminogen deficiency. N. Engl. J. Med., 339, 1679-1686.
49. Schuster, V., Mingers, A.M., Seidenspinner, S., Nussgens, Z., Pukrop, T. and Kreth, H.W. (1997) Homozygous mutations in the plasminogen gene of two unrelated girls with ligneous conjunctivitis. Blood, 90, 958-966.
50. Schuster, V. et al. (1999) Compound-heterozygous mutations in the plasminogen gene predispose to the development of ligneous conjunctivitis. Blood, 93, 3457-3466.
51. Shapiro, S.D., Griffin, G.L., Gilbert, D.J., Jenkins, N.A., Copeland, N.G., Welgus, H.G., Senior, R.M. and Ley, T.J. (1992) Molecular cloning, chromosomal localization and bacterial expression of a murine macrophage metalloelastase. J. Biol. Chem., 267, 4664-4671.
52. Shrivastava, A. et al. (1997) An orphan receptor tyrosine kinase family whose members serve as nonintegrin collagen receptors. Mol. Cell, 1, 25-34.
53. Solorzano, C.C. et al. (1997) A matrix metalloproteinase inhibitor prevents processing of tumor necrosis factor alpha (TNF α) and abrogates endotoxin-induced lethality. Shock, 7, 427-431.
54. Sternlicht, M.D. and Werb, Z. (1999) Extracellular matrix proteinases. In Kreis, T. and Vale, R. (eds), Guidebook to the Extracellular Matrix and Adhesion Proteins. Oxford University Press, New York, in press.
55. Strauss, B.H. et al. (1996) In vivo collagen turnover following experimental balloon angioplasty injury and the role of matrix metalloproteinases. Circ. Res., 79, 541-550.
56. Talhouk, R.S., Bissell, M.J. and Werb, Z. (1992) Coordinated expression of extracellular matrix-degrading proteinases and their inhibitors regulates mammary epithelial function during involution. J. Cell. Biol., 118, 1271-1282.
57. Teesalu, J., Blasi, F. and Talarico, D. (1998) Expression and function of the urokinase type plasminogen activator during mouse hemochorial placental development. Dev. Dynam., 213, 27-38.
58. Tsirka, S.E., Bugge, T.H., Degen, J.L. and Strickland, S. (1997) Neuronal death in the central nervous system demonstrates a non-fibrin substrate for plasmin. Proc. Natl Acad. Sci. USA, 94, 9779-9781.
59. Vogel, W., Gish, G.D., Alves, F. and Pawson, T. (1997) The discoidin domain receptor tyrosine kinases are activated by collagen. Mol. Cell, 1, 13-23.
60. Waltz, D.A., Natkin, L.R, Fujita, R.M., Wei, Y. and Chapman, H.A. (1997) Plasmin and plasminogen-activator inhibitor type-1 promote cellular motility by regulating the interaction between the urokinase receptor and vitronectin. J. Clin. Invest., 100, 58-67.
61. Werb, Z. (1997) ECM and cell surface proteolysis: regulating cellular ecology. Cell, 91, 439-442.
62. Whitelock, J.M., Murdoch, A.D., Iozzo, R.V. and Underwood, P.A. (1996) The degradation of human endothelial cell-derived perlecan and release of bound basic fibroblast growth-factor by stromelysin, collagenase, plasmin and heparanases. J. Biol. Chem., 271, 10079-10086.
63. Witte, M.B., Thornton, F.J., Kiyama, T., Efron, D.T., Schulz, G.S., Moldawer, L.L. and Barbul, A. (1998) Metalloproteinase inhibitors and wound healing: a novel enhancer of wound strength. Surgery, 124, 464-470.
64. Wolfsberg, T.G., Primakoff, P., Myles, D.G. and White, J.M. (1995) ADAM, a novel family of membrane proteins containing a disintegrin and metalloprotease domain: multipotential functions in cell-cell and cell-matrix interactions. J. Cell Biol., 131, 275-278.