Gelatinase A (MMP-2) and cysteine proteinases are essential for the degradation of collagen in soft connective tissue

Matrix Biology

Volumn 17, Issue 1, 1998, Pages 35-46

  Creemers, Laura B ^a,b   Jansen, Ineke D C ^a   Docherty, Andrew J P ^c   Reynolds, John J ^d   Beertsen, Wouter ^a   Everts, Vincent ^a,b  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b ACADEMIC MEDICAL CENTER   (Netherlands)

^c UCB PHARMA   (Belgium)

^d GUY S HOSPITAL   (United Kingdom)

Author keywords

Collagen degradation; Cysteine proteinases; Gelatinase; Matrix metalloproteinases

Indexed keywords

4 AMINOPHENYLMERCURIC ACETATE; COLLAGEN; CYSTEINE PROTEINASE; GELATINASE A; GELATINASE INHIBITOR; LEUPEPTIN; MATRIX METALLOPROTEINASE INHIBITOR; N [N (3 CARBOXYOXIRANE 2 CARBONYL)LEUCYL]AGMATINE;

ANIMAL TISSUE; ARTICLE; COLLAGEN DEGRADATION; CONNECTIVE TISSUE; CONTROLLED STUDY; GINGIVA; NONHUMAN; PERIODONTAL LIGAMENT; PRIORITY JOURNAL; SKIN; TOOTH PULP;

EID: 0031965487     PISSN: 0945053X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0945-053X(98)90123-8     Document Type: Article

References (64)

1. Agren, M.S.: Gelatinase activity during wound healing. Brit. J. Dermatol. 131: 634-640, 1994.
2. Aimes, R.T. and Quigley, J.P.: Matrix metalloproteinase-2 is an interstitial collagenase. J. Biol. Chem. 270: 5872-5876, 1995.
3. Beertsen, W. and Everts, V.: The site of remodelling of collagen in the periodontal ligament of the mouse incisor. Anat. Rec. 189: 479-498, 1977.
4. Birkedal-Hansen, H., Moore, W.G.I., Bodden, M.K., Windsor, L. J., Birkedal-Hansen, B., DeCarlo, A. and Engler, J.A.: Matrix metalloproteinases: a review. Critic. Rev. Oral Biol. Med. 4: 197-250, 1993.
5. Birkedal-Hansen, H.: Collagenase in periodontal disease. In: Collagenase in Normal and Pathological Connective Tissues, ed. by Woolley, D.E. and Evanson, J.M., John Wiley and Sons, Chichester, 1981, pp. 127-140.
6. Brown, C.C., Hembry, R.M. and Reynolds, J.J.: Immunolocalization of metalloproteinases and their inhibitor in the rabbit growth plate. J. Bone Joint Surg. 71: 580-593, 1989.
7. Crabbe, T., Willenbrock, F., Eaton, D., Hynds, P., Carne, A.F., Murphy, G. and Docherty, A.J.P.: Biochemical characterization of matrilysin. Activation conforms to the stepwise mechanisms proposed for other metalloproteinases. Biochemistry 31: 8500-8507, 1992.
8. Crabbe, T., Zucker, S., Cockett, M.I., Willenbrock, F., Tickle, S.P., O'Conell, J.P., Scothern, J.M., Murphy, G. and Docherty, A.J.P.: Mutation of the active site glutamic acid of human gelatinase-A: effects on latency, catalysis and the binding of tissue inhibitor of metalloproteinases-1 (TIMP-1). Biochemistry 33: 6684-6694, 1994.
9. Creemers, L.B., Jansen, D.C., van Veen-Reurings, A., van den Bos, T. and Everts, V.: Microassay for the assessment of low levels of hydoxyproline. Biotechniques 22: 656-658, 1997.
10. Dean, D.D., Muniz, O.K. and Howell, D.S.: Association of collagenase and tissue inhibitor of metalloproteinases (TIMP) with hypertrophic cell enlargement in the growth plate. Matrix 9: 366-375, 1989.
11. Eeckhout, Y., Delaissé, J.M. and Vaes, G.: Direct extraction and assay of bone tissue collagenase and its relation to parathyroid-hormone-induced bone resorption. Biochem. J. 279; 793-796, 1986.
12. Everts, V., Beertsen, W. and Tigchelaar-Gutter W.: The digestion of phagocytosed collagen is inhibited by the proteinase inhibitors leupeptin and E-64. Collagen Rel. Res. 5: 315-336, 1985.
13. Everts V., Hembry, R.M., Reynolds, J.J. and Beertsen, W.: Metalloproteinases are not involved in the phagocytosis of collagen fibrils by fibroblasts. Matrix 9: 266-276, 1989.
14. Everts, V., Hoeben, K. and Beertsen, W.: The release of tissue inhibitor of metalloproteinases by calvarial bone explants and its immunolocalization. Bone Miner. 22: 43-55, 1993.
15. Everts, V., Van der Zee, E., Creemers, L. and Beertsen, W.: Phagocytosis and intracellular digestion of collagen, its role in turnover and remodeling. Histochem. J. 28: 229-245, 1996.
16. Everts, V., Wolvius, E., Saklatvala, J. and Beertsen, W.: Interleukin-1 increases the production of collagenase but does not influence the phagocytosis of collagen fibrils. Matrix 10: 388-393, 1990.
17. Fukae, M., Kaneko, I., Tanabe, T. and Shimizu, M.: Metalloproteinases in the mineralized compartments of porcine dentine as detected by substrate-gel electrophoresis. Arch. Oral Biol. 36: 567-573, 1991.
18. Geiger, S. and Harper, E.: Human gingival collagenase in periodontal disease: The release of collagenase and the breakdown of endogenous collagen in gingival explants. J. Dent. Res. 59: 11-16, 1980.
19. Heussen, C. and Dowdle, E.B.: Electrophoretic analysis of plasminogen activators in polyacrylamide gels containing sodium dodecyl sulfate and copolymerized substrates. Anal. Biochem. 102: 196-202, 1980.
20. Hill, P.A., Docherty, A.J., Bottomley, K.M., O'Connell, J.P., Morphy, J.R., Reynolds, J.J. and Meikle, M.C.: Inhibition of bone resorption in vitro by selective inhibitors of gelatinase and collagenase. Biochem. J. 308: 167-175, 1995.
21. Hill, P.A., Murphy, G., Docherty, A.J.P., Hembry, R.M., Millican, T.A., Reynolds, J.J. and Meikle, M.C.: The effects of selective inhibitors of matrix metalloproteinases (MMPs) on bone resorption and the identification of MMPs and TIMP-1 in isolated osteoclasts. J. Cell Sci. 107: 3055-3064, 1994.
22. Himelstein, B.P., Canete-Soler, R., Bernhard, E.J. and Muschel, RJ.: Induction of fibroblast 92 kDa gelatinase/type IV collagenase expression by direct contact with metastatic tumor cells. J. Cell Sci. 107: 477-486, 1994.
23. Imai, K., Ohuchi, E., Takanori, A., Nomura, H., Fujii, Y., Sato, H., Seiki, M., Okada, Y.: Membrane-type matrix metalloproteinase-1 is a gelatinolytic enzyme and is secreted in a complex with tissue inhibitor of metalloproteinases. Cancer Res. 56: 2707-2710, 1996.
24. Imberman, M., Ramamurthy, N., Golub, L. and Schneir, M.: A reassessment of collagen half-life in rat periodontal tissues: Application of the pool-expansion approach. J. Periodont. Res. 21: 396-402, 1986.
25. Katanuma, N. Current trends in the study of intracellular protein degradation. J. Biol. Chem. 20: 36-61, 1989.
26. Kirschke, H. and Barrett, A.J.: Cathepsin L-A lysosomal cysteine proteinase. Progr. Clin. Biol. Res. 180: 61-69, 1986.
27. Kirschke, H., Kembhavi, A.A., Bohley, P. and Barrett, A.J.: Action of rat liver cathepsin L on collagen and other substrates. Biochem. J. 201: 367-372, 1982.
28. Kirschke, H., Langner, J., Riemann, S., Wiederanders, B., Ansorge, A. and Bohley, P.: Lysosomal cysteine proteinases. In: Protein Degradation in Health and Disease, Excerpta Medica, Amsterdam, 1980, pp. 15-35.
29. Koita, H., Nabeshima, K., Inoue, T. and Koono, M.: Sequential degradation of interstitial collagen by metalloproteinases extracted from tumors of murine ascites hepatomas. Clin. Exp. Metastasis 9: 441-456, 1991.
30. Krane, S.M.: Is collagenase (matrix metalloproteinase-1) necessary for bone and other connective tissue remodeling? Clin. Orthop. Rel. Res. 313: 47-53, 1995.
31. Liu, M.L., Wu, H., Byrne, M., Jeffrey, J., Krane, S. and Jaenisch, R.: A targeted mutation at the known collagenase cleavage site in mouse type I collagen impairs tissue remodeling. J. Cell Biol. 130: 227-237, 1995.
32. Matsubara, M., Girard, M.T., Kublin, C.L., Cintron, C. and Fini, M.E.: Differential roles for two gelatinolytic enzymes of the matrix metalloproteinase family in the remodelling cornea. Develop. Biol. 147: 425-439, 1991.
33. r 72,000 matrix metalloproteinase at the cell surface invadopodia. Cancer Res. 53: 3159-3164, 1993.
34. Murphy, G., Atkinson, S., Ward, R., Gavrilovic, J. and Reynolds, J.J.: The role of plasminogen activators in the regulation of connective tissue metalloproteinases. Ann. N.Y. Acad. Sci. 667: 1-13, 1992.
35. Murphy, G., Hembry, R.M., McGarrity, A.M., Reynolds, J.J. and Henderson, B.: Gelatinase (type IV collagenase) immunolocalization in cells and tissue: use of an antiserum to rabbit bone gelatinase that identifies high and low Mw forms. J. Cell Sci. 92: 487-495, 1989.
36. Murphy, G. and Reynolds, J.J.: Extracellular matrix degradation. In: Connective Tissue and its Heritable Disorders, ed. by Royce, P.M. and Steinmann, B., John Wiley and Sons, Chichester, 1993, pp. 287-316.
37. Nagase, H., Ogata, Y., Suzuki, K., Enghild, J.J. and Salvesen, G.: Substrate specificities and activation mechanisms of matrix metalloproteinases. Biochem. Soc. Trans. 19: 715-718, 1991.
38. Okada, Y., Morodomi, T., Enghild, J.J., Suzuki, K., Yasui, A., Nakanishi, L., Salvesen, G. and Nagase, H.: Matrix metalloproteinase 2 from human rheumatoid synovial fibroblasts. Eur. J. Biochem. 194: 721-730, 1990.
39. Orlowski, W.A.: The turnover of collagen in the dental pulp of rat incisors. J. Dent. Res. 56: 437-440, 1977.
40. Orlowski, W.A.: Biochemical study of collagen turnover in rat incisor periodontal ligament. Arch. Oral Biol. 23: 1163-1165, 1978.
41. Pelletier, J.P., Martel-Pelletier, J., Howell, D.S., Ghandur-Mnaymneh, L., Enis, J.E. and Woessner, J.F.: Collagenase and collagenolytic activity in human osteoarthritic cartilage. Arthr. Rheum. 26: 63-68, 1983.
42. Reich, R., Thompson, E.W., Iwanoto, Y., Martin, G.R., Deason, J.R., Fuller, G.G. and Miskin, R.: Effects of inhibitors of plasminogen activator, serine proteinases, and collagenase IV on the invasion of basement membranes by metastatic cells. Cancer Res. 48: 3307-3312, 1985.
43. Robins, E., Hirsch, H.E. and Emmons, S.S.: Glycosidases in the nervous system. J. Biol. Chem. 243: 4246-4252, 1968.
44. Rodgers, W.H., Matrisian, L.M., Giudice, L.C., Dsupin, B., Cannon, P., Svitek, C., Gorstein, F. and Osteen, K.G.: Patterns of matrix metalloproteinase expression in cycling endometrium imply differential functions and regulation by steroid hormones. J. Clin. Invest. 94: 946-953, 1994.
45. 14C in collagen and in non-collagenous proteins. Anal. Biochem. 57: 1-7, 1974.
46. Sato, H., Takino, T., Okada, Y., Cao, J., Shinagawa, A., Yamamoto, E. and Seiki, M.: A matrix metalloproteinase expressed on the surface of invasive tumor cells. Nature 370: 61-65, 1994.
47. Shore, R.C. and Berkovitz, B.K.B.: An ultrastructural study of periodontal ligament fibroblasts in relation to their possible role in tooth eruption and intracellular degradation in the rat. Arch. Oral Biol. 24: 155-164, 1979.
48. Smith, L .T., Holbrook, K.A. and Madri, J.A.: Collagen types I, III, and V in human embryonic and fetal skin. Am. J. Anat. 175: 507-521, 1986.
49. Sodek, J.: A comparison of the rates of synthesis and turnover of collagen and non-collagen proteins in adult rat periodontal tissues and skin using a microassay. Arch. Oral Biol. 22: 655-665, 1977.
50. Sodek, J.: A comparison of collagen and the non-collagenous protein metabolism in rat molar and incisor periodontal ligament. Arch. Oral Biol. 23: 977-982, 1978.
51. Sodek, J. and Ferrier, J.M.: Collagen remodelling in rat periodontal tissues: compensation for precursor reutilization confirms rapid turnover of collagen. Collagen Rel. Res. 1: 11-21, 1988.
52. Sodek, J. and Overall, C.M.: Matrix degradation in hard and soft connective tissue. In: Biological Mechanisms of Tooth Eruption and Root Resorption, ed. by Davidovich, Z., EBSCO Media, Birmingham AL, 1988, pp. 303-311.
53. Soini, Y., Hurskainen, T., Höyhtyä, M., Oikarinen, A. and Autio-Harmainen, H.: 72 kD and 92 kD type IV collagenase, type IV collagen and laminin mRNAs in breast cancer: a study by in situ hybridization. J. Histochem. Cytochem. 42: 945-951, 1994.
54. Taverne, A.A.R., Lemmens, I.G. and Tonino, G.J.M.: Lathyrogens and the role of collagen in the eruption of rat incisors. Arch. Oral Biol. 31: 127-131, 1986.
55. Ten Cate, A.R., Deporter, D.A. and Freeman, E.: The degradative role of the fibroblast in the remodelling and turnover of collagen in soft connective tissue. Am. J. Orthod. 69: 155-168, 1976.
56. Tournier, J-M., Polette, M., Hinnrasky, J., Beck, J., Werb, Z. and Basbaum, C.: Expression of gelatinase A, a mediator of extracellular matrix remodeling, by tracheal gland serous cells in culture and in vivo. J. Biol. Chem. 269: 25454-25464, 1994.
57. Trancart, M.M., Chalmeigne, N., Girardot, C., Zarpanelian, C. and Prigent, D.: Gelatinase is the main matrix metalloproteinase involved in granuloma-induced cartilage degradation. Int. Tiss. Reac. XIV: 287-294, 1992.
58. Van der Zee, E., Everts, V., Hoeben, K. and Beertsen, W.: Cytokines modulate phagocytosis and intracellular digestion of collagen fibrils by fibroblasts in rabbit periosteal explants. J. Cell Sci. 107: 1047-1053, 1994.
59. Van der Zee, E., Everts, V., Hoeben, K. and Beertsen, W.: Cytokine-induced endogenous procollagenase stored in the extracellular matrix of soft connective tissue results in a burst of collagen breakdown following its activation. J. Periodont. Res. 31: 83-488, 1996.
60. Wang, H.M.: Detection of lysosomal enzymes derived from pig periodontal ligament fibroblasts and their ability to digest collagen fibrils and proteoglycan. Arch. Oral Biol. 27: 715-720, 1982.
61. Ward, R.V., Atkinson, S.J., Reynolds, J.J. and Murphy, G.: Cell surface-mediated activation of progelatinase A: demonstration of the involvement of the C-terminal domain of progelatinase A in cell surface binding and activation of progelatinase A by primary fibroblasts. Biochem. J. 304: 263-269, 1994.
62. Wilson, M.J., Garcia, B., Woodson, M. and Sinha, A.A.: Gelatinolytic and caseinolytic proteinase activities in the secretions of the ventral, lateral and dorsal lobes of the rat prostate. Biol. Reprod. 48: 1174-1184, 1993.
63. Woessner, J.E.: Collagenase in uterine resorption. In: Collagenase in Normal and Pathologic Connective Tissues, ed. by Woolley, D.E. and Evanson, J.M., John Wiley and Sons, Chichesterbridge, UK, 1980, pp. 223-239.
64. Woolley, D.E. and Davies, R.M: Immunolocalization of collagenase in periodontal disease. J. Periodont. Res. 16: 292-297 1981.