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MMPs and TIMPs—An historical perspective

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Abstract

There are currently 25 known vertebrate matrix metalloproteinases (MMPs) and 4 tissue inhibitors of metalloproteinases (TIMPs). This article reviews these proteases from an historical perspective in terms of who discovered each protein, when the sequence was established, when action on protein substrates was demonstrated, and what names have been used. A similar approach is taken for the TIMPS, and their multiple functions in addition to protease inhibition are emphasized. MMPs from invertebrates, plants, and bacteria are also discussed. This review is an outgrowth and update of a chapter by the same name originally published in Matrix Metalloproteinase Protocols, pp. 1–23, edited by I. M. Clark and published by Humana Press in 2001.

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References

  1. Gross, J. and Lapière, C. M. (1962) Collagenolytic activity in amphibian tissues: a tissue culture assay. Proc. Natl. Acad. Sci. USA 48, 1014–1022.

    Article  PubMed  CAS  Google Scholar 

  2. Bauer, E. A., Stricklin, G. P., Jeffrey, J. J., and Eisen, A. Z. (1975) Collagenase production by human skin fibroblasts. Biochem. Biophys. Res. Commun. 64, 232–240.

    Article  PubMed  CAS  Google Scholar 

  3. Woolley, D. E., Roberts, D. R., and Evanson, J. M. (1975) Inhibition of human collagenase activity by a small molecular weight serum protein. Biochem. Biophys. Res. Commun. 66, 747–754.

    Article  PubMed  CAS  Google Scholar 

  4. Woessner, J. F., Jr. (1998) The matrix metalloproteinase family. Matrix Metalloproteinases (Parks, W. C. and Mecham, R. P., eds) Academic Press, San Diego, pp. 1–14.

    Google Scholar 

  5. Massova, I., Kotra, L. P., Fridman, R., and Mobashery, S. (1998) Matrix metalloproteinases-structures, evolution, and diversification. FASEB J. 12, 1075–1095.

    PubMed  CAS  Google Scholar 

  6. Nagase, H. and Woessner, J. F. (1999) Matrix metalloproteinases. J. Biol. Chem. 274, 21491–21494.

    Article  PubMed  CAS  Google Scholar 

  7. Parks, W. C. and Mecham, R. P. (1998) Matrix Metalloproteinases Academic Press, San Diego.

    Google Scholar 

  8. Woessner, J. F. and Nagase, H. (2000) Matrix Metalloproteinases and TIMPs: Protein Profile Oxford Univ. Press, Oxford.

    Book  Google Scholar 

  9. Clark, I. M. (2001) Matrix Metalloproteinase Protocols Humana Press, Totowa, NJ

    Google Scholar 

  10. Barrett, A. J., Rawlings, N. D., and Woessner, J. F. (1998) Handbook of Proteolytic Enzymes Academic Press, London.

    Google Scholar 

  11. Barrett, A. J. (1995) Methods in Enzymology. Vol. 248. Proteolytic Enzymes: Aspartic and Metallo Peptidases Academic Press, San Diego.

    Google Scholar 

  12. Bode, W., Gomis-Rüth, F. X., and Stöcker, W. (1993) Astacins, serralysins, snake venom and matrix metalloproteinases exhibit identical zinc-binding environments (HEXXHXXGXXH and Met-turn) and topologies and should be grouped into a common family, the ‘metzincins’. FEBS Lett. 331, 134–140.

    Article  PubMed  CAS  Google Scholar 

  13. Gross, J. and Nagai, Y. (1965) Specific degradation of the collagen molecule by tadpole collagenolytic enzyme. Proc. Natl. Acad. Sci. USA 54, 1197–1204.

    Article  PubMed  CAS  Google Scholar 

  14. Bauer, E. A., Eisen, A. Z., and Jeffrey, J. J. (1970) Immunologic relationship of a purified human skin collagenase to other human and animal collagenases. Biochem. Biophys. Acta 206, 152–160.

    PubMed  CAS  Google Scholar 

  15. Harper, E., Bloch, K. J., and Gross, J. (1971) The zymogen of tadpole collagenase. Biochemistry 10, 3035–3041.

    Article  PubMed  CAS  Google Scholar 

  16. Birkedal-Hansen, H., Cobb, C. M., Taylor, R. E., and Fullmer, H. M. (1975) Activation of latent bovine gingival collagenase. in: Arch. Oral Biol. 20, 681–685.

    Article  PubMed  CAS  Google Scholar 

  17. Werb, Z. and Burleigh, M. C. (1974) A specific collagenase from rabbit fibroblasts in monolayer culture. Biochem. J. 137, 373–385.

    PubMed  CAS  Google Scholar 

  18. Goldberg, G. I., Wilhelm, S. M., Kronberger, A., Bauer, E. A., Grant, G. A., and Eisen, A. Z. (1986) Human fibroblast collagenase. Complete primary structure and homology to an oncogene transformation-induced rat protein. J. Biol. Chem. 261, 6600–6605.

    PubMed  CAS  Google Scholar 

  19. Dioszegi, M., Cannon, P., and Van Wart, H. E. (1995) Vertebrate collagenases. Methods Enzymol. 248, 413–431.

    PubMed  CAS  Google Scholar 

  20. Cawston, T. E. (1998) Interstitial collagenase. Handbook of Proteolytic Enzymes (Barrett, A. J., Rawlings, N. D., and Woessner, J. F., eds) Academic Press, London, pp. 1155–1162.

    Google Scholar 

  21. Jeffrey, J. J. (1998) Interstitial collagenases. Matrix Metalloproteinases (Parks, W. C. and Mecham, R. P., eds) Academic Press, San Diego, pp. 15–42.

    Google Scholar 

  22. Sellers, A., Reynolds, J. J., and Meikle, M. C. (1978) Neutral metallo-proteinases of rabbit bone. Separation in latent forms of distinct enzymes that when activated degrade collagen, gelatin and proteoglycans. Biochem. J. 171, 493–496.

    PubMed  CAS  Google Scholar 

  23. Liotta, L. A., Abe, S., Robey, P. G., and Martin, G. R. (1979) Preferential digestion of basement membrane collagen by an enzyme derived from a metastatic murine tumor. Proc. Natl. Acad. Sci. USA 76, 2268–2272.

    Article  PubMed  CAS  Google Scholar 

  24. Seltzer, J. L., Eschbach, M. L., and Eisen, A. Z. (1985) Purification of gelatin-specific neutral protease from human skin by conventional and high-performance liquid chromatography. J. Chromatogr. 326, 147–155.

    Article  PubMed  CAS  Google Scholar 

  25. Salo, T., Liotta, L. A., and Tryggvason, K. (1983) Purification and characterization of a murine basement membrane collagen-degrading enzyme secreted by metastatic tumor cells. J. Biol. Chem. 258, 3058–3063.

    PubMed  CAS  Google Scholar 

  26. Murphy, G., McAlpine, C. G., Poll, C. T., and Reynolds, J. J. (1985) Purification and characterization of a bone metalloproteinase that degrades gelatin and types IV and V collagen. Biochim. Biophys. Acta 831, 49–58.

    PubMed  CAS  Google Scholar 

  27. Nakano, T., and Scott, P. G. (1986) Purification and characterization of a gelatinase produced by fibroblasts from human gingiva. Biochem. Cell. Biol. 64, 387–393.

    PubMed  CAS  Google Scholar 

  28. Collier, I. E., Wilhelm, S. M., Eisen, A. Z., et al. (1988) H-ras oncogene-transformed human bronchial epithelial cells (TBE-1) secrete a single metalloprotease capable of degrading basement membrane collagen. J. Biol. Chem. 263, 6579–6587.

    PubMed  CAS  Google Scholar 

  29. Collier, I. E., Krasnov, P. A., Strongin, A. Y., Birkedal-Hansen, H., and Goldberg, G. I. (1992) Alanine scanning mutagenesis and functional analysis of the fibronectin-like collagen-binding domain from human 92-kDa type IV collagenase. J. Biol. Chem. 267, 6776–6781.

    PubMed  CAS  Google Scholar 

  30. Murphy, G. and Crabbe, T. (1995) Gelatinases A and B. Methods Enzymol. 248, 470–484.

    PubMed  CAS  Google Scholar 

  31. Murphy, G. (1998) Gelatinase A. Handbook of Proteolytic Enzymes (Barrett, A. J., Rawlings, N. D., and Woessner, J. F., eds) Academic Press, London, pp. 1199–1205.

    Google Scholar 

  32. Yu, A. E., Murphy, A. N., and Stetler-Stevenson, W. G. (1998) 72-kDa gelatinase (gelatinase A): structure, activation, regulation and substrate specificity. Matrix Metalloproteinases (Parks, W. C. and Mecham, R. P., eds) Academic Press, San Diego, pp. 85–113.

    Google Scholar 

  33. Sapolsky, A. I., Howell, D. S., and Woessner, J. F., Jr. (1974) Neutral proteases and cathepsin D in human articular cartilage. J. Clin. Invest. 53, 1044–1053.

    PubMed  CAS  Google Scholar 

  34. Werb, Z. and Reynolds, J. J. (1974) Stimulation by endocytosis of the secretion of collagenase and neutral proteinase from rabbit synovial fibroblasts. J. Exp. Med. 140, 1482–1497.

    Article  PubMed  CAS  Google Scholar 

  35. Galloway, W. A., Murphy, G., Sandy, J. D., Gavrilovic, J., Cawston, T. E., and Reynolds, J. J. (1983) Purification and characterization of a rabbit bone metalloproteinase that degrades proteoglycan and other connective-tissue components. Biochem. J. 209, 741–752.

    PubMed  CAS  Google Scholar 

  36. Chin, J. R., Murphy, G., and Werb, Z. (1985) Stromelysin, a connective tissue-degrading metalloendopeptidase secreted by stimulated rabbit synovial fibroblasts in parallel with collagenase. Biosynthesis, isolation, characterization, and substrates. J. Biol. Chem. 260, 12,367–12,376.

    CAS  Google Scholar 

  37. Matrisian, L. M., Glaichenhaus, N., Gesnel, M.-C., and Breathnach, R. (1985) Epidermal growth factor and oncogenes induce transcription of the same cellular mRNA in rat fibroblasts. EMBO J. 4, 1435–1440.

    PubMed  CAS  Google Scholar 

  38. Treadwell, B. V., Neidel, J., Pavia, M., Towle, C. A., Trice, M. E., and Mankin, H. J. (1986) Purification and characterization of collagenase activator protein synthesized by articular cartilage. Arch. Biochem. Biophys. 251, 715–723.

    Article  PubMed  CAS  Google Scholar 

  39. Nagase, H. (1995) Human stromelysins 1 and 2. Methods Enzymol. 248, 449–470.

    PubMed  CAS  Google Scholar 

  40. Nagase, H. (1998) Stromelysin 1. Handbook of Proteolytic Enzymes (Barrett, A. J., Rawlings, N. D., and Woessner, J. F., eds) Academic Press, London, pp. 1172–1178.

    Google Scholar 

  41. Nagase, H. (1998) Stromelysins 1 and 2. Matrix Metalloproteinases (Parks, W. C. and Mecham, R. P., eds) Academic Press, San Diego, pp. 43–84.

    Google Scholar 

  42. Scott, P. G. and Goldberg, H. A. (1983) Cleavage of the carboxy-terminal cross-linking region of type I collagen by proteolytic activity from cultured porcine gingival explants. Coll. Relat. Res. 3, 295–304.

    PubMed  CAS  Google Scholar 

  43. Nakano, T. and Scott, P. G. (1987) Partial purification and characterization of a neutral proteinase with collagen telopeptidase activity produced by human gingival fibroblasts. Biochem. Cell Biol. 65, 286–292.

    Article  PubMed  CAS  Google Scholar 

  44. Wu, J. J., Lark, M. W., Chun, L. E., and Eyre, D. R. (1991) Sites of stromelysin cleavage in collagen types II, IX, X, and XI of cartilage. J. Biol. Chem. 266, 5625–5628.

    PubMed  CAS  Google Scholar 

  45. Overall, C. M. and Sodek, J. (1987) Initial characterization of a neutral metalloproteinase, active on native 3/4-collagen fragments, synthesized by ROS 17/2.8 osteoblastic cells, periodontal fibroblasts, and identified in gingival crevicular fluid. J. Dent. Res. 66, 1271–1282.

    PubMed  CAS  Google Scholar 

  46. Nagase, H., Barrett, A. J., and Woessner, J. F., Jr. (1992) Nomenclature and glossary of the matrix metalloproteinases. Matrix Suppl. 1, 421–424.

    PubMed  CAS  Google Scholar 

  47. Sapolsky, A. I., Keiser, H., Howell, D. S., and Woessner, J. F., Jr. (1976) Metalloproteases of human articular cartilage that digest cartilage proteoglycan at neutral and acid pH. J. Clin. Invest. 58, 1030–1041.

    PubMed  CAS  Google Scholar 

  48. Azzo, W. and Woessner, J. F., Jr. (1986) Purification and characterization of an acid metalloproteinase from human articular cartilage. J. Biol. Chem. 261, 5434–5441.

    PubMed  CAS  Google Scholar 

  49. Dean, D. D., Martel-Pelletier, J., Pelletier, J.-P., Howell, D. S., and Woessner, J. F., Jr. (1989) Evidence for metalloproteinase and metalloproteinase inhibitor imbalance in human osteoarthritic cartilage. J. Clin. Invest. 84, 678–685.

    PubMed  CAS  Google Scholar 

  50. Gunja-Smith, Z., Nagase, H., and Woessner, J. F., Jr. (1989) Purification of the neutral proteoglycan-degrading metalloproteinase from human articular cartilage tissue and its identification as stromelysin matrix metalloproteinase-3. Biochem. J. 258, 115–119.

    PubMed  CAS  Google Scholar 

  51. Sellers, A. and Woessner, J. F., Jr. (1980) The extraction of a neutral metalloproteinase from the involuting rat uterus, and its action on cartilage proteoglycan. Biochem. J. 189, 521–531.

    PubMed  CAS  Google Scholar 

  52. Woessner, J. F., Jr. and Taplin, C. J. (1988) Purification and properties of a small latent matrix metalloproteinase of the rat uterus. J. Biol. Chem. 263, 16,918–16,925.

    CAS  Google Scholar 

  53. Muller, D., Quantin, B., Gesnel, M. C., Millon-Collard, R., Abecassis, J., and Breathnach, R. (1988) The collagenase gene family in humans consists of at least four members. Biochem. J. 253, 187–192.

    PubMed  CAS  Google Scholar 

  54. Quantin, B., Murphy, G., and Breathnach, R. (1989) Pump-1 cDNA codes for a protein with characteristics similar to those of classical collagenase family members. Biochemistry 28, 5327–5334.

    Article  PubMed  CAS  Google Scholar 

  55. Marcotte, P. A., Dudlak, D., Leski, M. L., Ryan, J., and Henkin, J. (1992) Characterization of a metalloprotease which cleaves with high site-specificity the Glu(143)-Leu(144) bond of urokinase. Fibrinolysis 6 (Suppl. 1), 57–62.

    Article  CAS  Google Scholar 

  56. Woessner, J. F., Jr. (1995) Matrilysin. Methods Enzymol. 248, 485–495.

    PubMed  CAS  Google Scholar 

  57. Wilson, C. L. and Matrisian, L. M. (1996) Matrilysin: an epithelial matrix metalloproteinase with potentially novel functions. Int. J. Biochem. Cell Biol. 28, 123–136.

    Article  PubMed  CAS  Google Scholar 

  58. Woessner, J. F. (1998) Matrilysin. Handbook of Proteolytic Enzymes (Barrett, A. J., Rawlings, N. D., and Woessner, J. F., eds) Academic Press, London, pp. 1183–1187.

    Google Scholar 

  59. Lazarus, G. S., Brown, R. S., Daniels, J. R., and Fullmer, H. M. (1968) Human granulocyte collagenase. Science 159, 1483–1485.

    Article  CAS  Google Scholar 

  60. Lazarus, G. S., Daniels, J. R., Brown, R. S., Bladen, H. A., and Fullmer, H. M. (1968) Degradation of collagen by a human granulocyte collagenolytic system. J. Clin. Invest. 47, 2622–2629.

    PubMed  CAS  Google Scholar 

  61. Kruze, D. and Wojtecka, E. (1972) Activation of leucocyte collagenase proenzyme by rheumatoid synovial fluid. Biochim. Biophys. Acta 285, 436–446.

    PubMed  CAS  Google Scholar 

  62. Murphy, G., Reynolds, J. J., Bretz, U., and Baggiolini, M. (1977) Collagenase is a component of the specific granules of human neutrophil leucocytes. Biochem. J. 162, 195–197.

    PubMed  CAS  Google Scholar 

  63. Oronsky, A. L., Perper, R. J., and Schroder, H. C. (1973) Phagocytic release and activation of human leukocyte procollagenase. Nature 246, 417–419.

    Article  PubMed  CAS  Google Scholar 

  64. Macartney, H. W. and Tschesche, H. (1983) Latent and active human polymorphonuclear leukocyte collagenases. Isolation, purification and characterisation. Eur. J. Biochem. 130, 71–78.

    Article  PubMed  CAS  Google Scholar 

  65. Hasty, K. A., Hibbs, M. S., Kang, A. H., and Mainardi, C. L. (1984) Heterogeneity among human collagenases demonstrated by monoclonal antibody that selectively recognizes and inhibits human neutrophil collagenase. J. Exp. Med. 159, 1455–1463.

    Article  PubMed  CAS  Google Scholar 

  66. Hasty, K. A., Pourmotabbed, T. F., Goldberg, G. I., et al. (1990) Human neutrophil collagenase. A distinct gene product with homology to other matrix metalloproteinases. J. Biol. Chem. 265, 11,421–11,424.

    CAS  Google Scholar 

  67. Tschesche, H. (1995) Human neutrophil collagenase. Methods Enzymol. 248, 431–449.

    PubMed  CAS  Google Scholar 

  68. Tschesche, H. and Pieper, M. (1998) Neutrophil collagenase, In: Handbook of Proteolytic Enzymes (Barrett, A. J., Rawlings, N. D., and Woessner, J. F., eds.), Academic Press, London, pp. 1162–1167.

    Google Scholar 

  69. Ohlsson, K. (1980) Polymorphonuclear leukocyte collagenase. Collagenase in Normal and Pathological Connective Tissues (Woolley, D. E. and Evanson, J. M., eds) Wiley, Chichester, England, pp. 209–222.

    Google Scholar 

  70. Harris, E. D., Jr. and Krane, S. M. (1972) An endopeptidase from rheumatoid synovial tissue culture. Biochim. Biophys. Acta 258, 566–576.

    PubMed  CAS  Google Scholar 

  71. Sopata, I. and Dancewicz, A. M. (1974) Presence of a gelatin-specific proteinase and its latent form in human leucocytes. Biochim. Biophys. Acta 370, 510–523.

    PubMed  CAS  Google Scholar 

  72. Sopata, I. and Wize, J. (1979) A latent gelatin specific proteinase of human leucocytes and its activation. Biochim. Biophys. Acta 571, 305–312.

    PubMed  CAS  Google Scholar 

  73. Mainardi, C. L., Seyer, J. M., and Kang, A. H. (1980) Type-specific collagenolysis: a type V collagen-degrading enzyme from macrophages. Biochem. Biophys. Res. Commun. 97, 1108–1115.

    PubMed  CAS  Google Scholar 

  74. Murphy, G., Bretz, U., Baggiolini, M., and Reynolds, J. J. (1980) The latent collagenase and gelatinase of human polymorphonuclear neutrophil leucocytes. Biochem. J. 192, 517–525.

    PubMed  CAS  Google Scholar 

  75. Rantala-Ryhänen, S., Ryhänen, L., Nowak, F. V., and Uitto, J. (1983) Proteinases in human polymorphonuclear leukocytes. Purification and characterization of an enzyme which cleaves denatured collagen and a synthetic peptide with a Gly-Ile sequence. Eur. J. Biochem. 134, 129–137.

    Article  PubMed  Google Scholar 

  76. Wilhelm, S. M., Collier, I. E., Marmer, B. L., Eisen, A. Z., Grant, G. A., and Goldberg, G. I. (1989) SV40-transformed human lung fibroblasts secrete a 92-kDa type IV collagenase which is identical to that secreted by normal human macrophages. J. Biol. Chem. 264, 17,213–17,221.

    CAS  Google Scholar 

  77. Goldberg, G. I., Strongin, A., Collier, I. E., Genrich, L. T., and Marmer, B. L. (1992) Interaction of 92-kDa type IV collagenase with the tissue inhibitor of metalloproteinases prevents dimerization, complex formation with interstitial collagenase, and activation of the proenzyme with stromelysin. J. Biol. Chem. 267, 4583–4591.

    PubMed  CAS  Google Scholar 

  78. Kjeldsen, L., Johnsen, A. H., Sengelov, H., and Borregaard, N. (1993) Isolation and primary structure of NGAL, a novel protein associated with human neutrophil gelatinase. J. Biol. Chem. 268, 10,425–10,432.

    CAS  Google Scholar 

  79. Vartio, T. (1985) The 95000-Mr gelatin-binding protein in human serum and plasma. Biochem. J. 228, 605–608.

    PubMed  CAS  Google Scholar 

  80. Vu, T. H. and Werb, Z. (1998) Gelatinase B: structure, regulation and function. Matrix Metalloproteinases (Parks, W. C. and Mecham, R. P., eds) Academic Press, San Diego, pp. 115–148.

    Google Scholar 

  81. Collier, I. E. and Goldberg, G. I. (1998) Gelatinase B. Handbook of Proteolytic Enzymes (Barrett, A. J., Rawlings, N. D., and Woessner, J. F., eds) Academic Press, London, pp. 1205–1210.

    Google Scholar 

  82. Breathnach, R., Matrisian, L. M., Gesnel, M.-C., Staub, A., and Leroy, P. (1987) Sequences coding for part of oncogene-induced transin are highly conserved in a related rat gene. Nucleic Acids Res. 15, 1139–1151.

    Article  PubMed  CAS  Google Scholar 

  83. Nicholson, R., Murphy, G., and Breathnach, R. (1989) Human and rat malignant-tumor-associated mRNAs encode stromelysin-like metalloproteinases. Biochemistry 28, 5195–5203.

    Article  PubMed  CAS  Google Scholar 

  84. Matrisian, L. M. (1998) Stromelysin 2. Handbook of Proteolytic Enzymes (Barrett, A. J., Rawlings, N. D., and Woessner, J. F., eds) Academic Press, London, pp. 1178–1180.

    Google Scholar 

  85. Basset, P., Bellocq, J. P., Wolf, C., et al. (1990) A novel metalloproteinase gene specifically expressed in stromal cells of breast carcinomas. Nature 348, 699–704.

    Article  PubMed  CAS  Google Scholar 

  86. Murphy, G., Segain, J. P., O’Shea, M., et al. (1993) The 28-kDa N-terminal domain of mouse stromelysin-3 has the general properties of a weak metalloproteinase. J. Biol. Chem. 268, 15,435–15,441.

    CAS  Google Scholar 

  87. Pei, D., Majmudar, G., and Weiss, S. J. (1994) Hydrolytic inactivation of a breast carcinoma cell-derived serpin by human stromelysin-3. J. Biol. Chem. 269, 25,849–25,855.

    CAS  Google Scholar 

  88. Pei, D. and Weiss, S. J. (1995) Furin-dependent intracellular activation of the human stromelysin-3 zymogen. Nature 375, 244–247.

    Article  PubMed  CAS  Google Scholar 

  89. Basset, P., Bellocq, J. P., Lefebvre, O., et al. (1997) Stromelysin-3: a paradigm for stroma-derived factors implicated in carcinoma progression. Crit. Rev. Oncol. Hematol. 26, 43–53.

    Article  PubMed  CAS  Google Scholar 

  90. Werb, Z. and Gordon, S. (1975) Elastase secretion by stimulated macrophages. Characterization and regulation. J. Exp. Med. 142, 361–377.

    Article  PubMed  CAS  Google Scholar 

  91. Banda, M. J., Clark, E. J., and Werb, Z. (1980) Limited proteolysis by macrophage elastase inactivates human a1-proteinase inhibitor. J. Exp. Med. 152, 1563–1570.

    Article  PubMed  CAS  Google Scholar 

  92. Banda, M. J. and Werb, Z. (1981) Mouse macrophage elastase. Purification and characterization as a metalloproteinase. Biochem. J. 193, 589–605.

    PubMed  CAS  Google Scholar 

  93. Kettner, C., Shaw, E., White, R., and Janoff, A. (1981) The specificity of macrophage elastase on the insulin B-chain. Biochem. J. 195, 369–372.

    PubMed  CAS  Google Scholar 

  94. Shapiro, S. D., Griffin, G. L., Gilbert, D. J., et al. (1992) Molecular cloning, chromosomal localization, and bacterial expression of a murine macrophage metalloelastase. J. Biol. Chem. 267, 4664–4671.

    PubMed  CAS  Google Scholar 

  95. Belaaouaj, A., Shipley, J. M., Kobayashi, D. K., et al. (1995) Human macrophage metalloelastase. Genomic organization, chromosomal location, gene linkage, and tissue-specific expression. J. Biol. Chem. 270, 14,568–14,575.

    CAS  Google Scholar 

  96. Shapiro, S. D. and Senior, R. M. (1998) Macrophage elastase (MMP-12). Matrix Metalloproteinases (Parks, W. C. and Mecham, R. P., eds) Academic Press, San Diego, pp. 185–197.

    Google Scholar 

  97. Senior, R. M. and Shapiro, S. D. (1998) Macrophage elastase. Handbook of Proteolytic Enzymes (Barrett, A. J., Rawlings, N. D., and Woessner, J. F., eds) Academic Press, London, pp. 1180–1183.

    Google Scholar 

  98. Quinn, C. O., Scott, D. K., Brinckerhoff, C. E., Matrisian, L. M., Jeffrey, J. J., and Partridge, N. C. (1990) Rat collagenase. Cloning, amino acid sequence comparison, and parathyroid hormone regulation in osteoblastic cells. J. Biol. Chem. 265, 22,342–22,347.

    CAS  Google Scholar 

  99. Freije, J. M., Díez-Itza, I., Balbín, M., et al. (1994) Molecular cloning and expression of collagenase-3, a novel human matrix metalloproteinase produced by breast carcinomas. J. Biol. Chem. 269, 16,766–16,773.

    CAS  Google Scholar 

  100. Aer, J. (1971) Purification of rat bone collagenolytic enzymes. Ann. Med. Exp. Biol. Fenn. 49, 1–8.

    PubMed  CAS  Google Scholar 

  101. Jeffrey, J. J. and Gross, J. (1970) Collagenase from rat uterus. Isolation and partial characterization. Biochemistry 9, 268–273.

    Article  PubMed  CAS  Google Scholar 

  102. Roswit, W. T., Halme, J., and Jeffrey, J. J. (1983) Purification and properties of rat uterine procollagenase. Arch. Biochem. Biophys. 225, 285–295.

    Article  PubMed  CAS  Google Scholar 

  103. Weeks, J. G., Halme, J., and Woessner, J. F., Jr. (1976) Extraction of collagenase from the involuting rat uterus. Biochim. Biophys. Acta 445, 205–214.

    PubMed  CAS  Google Scholar 

  104. Jeffrey, J. J. (1998) Collagenase 3. Handbook of Proteolytic Enzymes (Barrett, A. J., Rawlings, N. D., and Woessner, J. F., eds) Academic Press, London, pp. 1167–1170.

    Google Scholar 

  105. Balbín, M., Fueyo, A., Knäuper, V., et al. (2001) Identification and enzymatic characterization of two diverging murine counterparts of human interstitial collagenase (MMP-1) expressed at sites of embryo implantation. J. Biol. Chem. 276, 10,253–10,262.

    Google Scholar 

  106. Sato, H., Takino, T., Okada, Y., et al. (1994) A matrix metalloproteinase expressed on the surface of invasive tumour cells. Nature 370, 61–65.

    Article  PubMed  CAS  Google Scholar 

  107. Okada, A., Bellocq, J. P., Rouyer, N., Chenard, M. P., Rio, M. C., Chambon, P., and Basset, P. (1995) Membrane-type matrix metalloproteinase (MT-MMP) gene is expressed in stromal cells of human colon, breast, and head and neck carcinomas. Proc. Natl. Acad. Sci. USA 92, 2730–2734.

    Article  PubMed  CAS  Google Scholar 

  108. Strongin, A. Y., Collier, I., Bannikov, G., Marmer, B. L., Grant, G. A., and Goldberg, G. I. (1995) Mechanism of cell surface activation of 72-kDa type IV collagenase. Isolation of the activated form of the membrane metalloprotease. J. Biol. Chem. 270, 5331–5338.

    Article  PubMed  CAS  Google Scholar 

  109. Takino, T., Sato, H., Yamamoto, E., and Seiki, M. (1995) Cloning of a human gene potentially encoding a novel matrix metalloproteinase having a C-terminal transmembrane domain. Gene 155, 293–298.

    Article  PubMed  CAS  Google Scholar 

  110. Seiki, M. (1998) Membrane-type matrix metalloproteinase 1. Handbook of Proteolytic Enzymes (Barrett, A. J., Rawlings, N. D., and Woessner, J. F., eds) Academic Press, London, pp. 1192–1195.

    Google Scholar 

  111. Knäuper, V. and Murphy, G. (1998) Membrane-type matrix metalloproteinases and cell surface-associated activation cascades for matrix metalloproteinases. Matrix Metalloproteinases (Parks, W. C. and Mecham, R. P., eds) Academic Press, San Diego, pp. 199–218.

    Google Scholar 

  112. Murphy, G. and Knäuper, V. (1999) Membrane type matrix metalloproteinases: regulators of focal proteolysis. Metalloproteinases as Targets for Anti-Inflammatory Drugs (Bottomley, K.M.K., Bradshaw, D., and Nixon, J.S., eds) Birkhauser, Basel, pp. 99–116.

    Google Scholar 

  113. Seiki, M. (1999) Membrane-type matrix metalloproteinases. APMIS 107, 137–143.

    Article  PubMed  CAS  Google Scholar 

  114. Takino, T., Sato, H., Shinagawa, A., and Seiki, M. (1995) Identification of the second membrane-type matrix metalloproteinase (MT-MMP-2) gene from a human placenta cDNA library. MT-MMPs form a unique membrane-type subclass in the MMP family. J. Biol. Chem. 270, 23,013–23,020.

    CAS  Google Scholar 

  115. Will, H. and Hinzmann, B. (1995) cDNA sequence and mRNA tissue distribution of a novel human matrix metalloproteinase with a potential transmembrane segment. Eur. J. Biochem. 231, 602–608.

    Article  PubMed  CAS  Google Scholar 

  116. d’Ortho, M.-P., Will, H., Atkinson, S., et al. (1997) Membrane-type matrix metalloproteinases 1 and 2 exhibit broad-spectrum proteolytic capacities comparable to many matrix metalloproteinases. Eur. J. Biochem. 250, 751–757.

    Article  PubMed  CAS  Google Scholar 

  117. Matsumoto, S. I., Katoh, M., Saito, S., Watanabe, T., and Masuho, Y. (1997) Identification of soluble type of membrane-type matrix metalloproteinase-3 formed by alternatively spliced mRNA. Biochim. Biophys. Acta Gene Struct. Express. 1354, 159–170.

    Article  CAS  Google Scholar 

  118. Shimada, T., Nakamura, H., Ohuchi, E., et al. (1999) Characterization of a truncated recombinant form of human membrane type 3 matrix metalloproteinase. Eur. J. Biochem. 262, 907–914.

    Article  PubMed  CAS  Google Scholar 

  119. Puente, X. S., Pendás, A. M., Llano, E., Velasco, G., and López-Otín, C. (1996) Molecular cloning of a novel membrane-type matrix metalloproteinase from a human breast carcinoma. Cancer Res. 56, 944–949.

    PubMed  CAS  Google Scholar 

  120. Kajita, M., Kinoh, H., Ito, N., et al. (1999) Human membrane type-4 matrix metalloproteinase (MT4-MMP) is encoded by a novel major transcript: isolation of complementary DNA clones for human and mouse mt4-mmp transcripts. FEBS Lett. 457, 353–356.

    Article  PubMed  CAS  Google Scholar 

  121. Kolkenbrock, H., Essers, L., Ulbrich, N., and Will, H. (1999) Biochemical characterization of the catalytic domain of membrane-type 4 matrix metalloproteinase. Biol. Chem. 380, 1103–1108.

    Article  PubMed  CAS  Google Scholar 

  122. English, W. R., Puente, X. S., Freije, J. M. P., et al. (2000) Membrane type 4 matrix metalloproteinase (MMP17) has tumor necrosis factor-alpha convertase activity but does not activate pro-MMP2. J. Biol. Chem. 275, 14,046–14,055.

    Article  CAS  Google Scholar 

  123. 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, 34,260–34,266.

    CAS  Google Scholar 

  124. Stolow, M. A., Bauzon, D. D., Li, J., et al. (1996) Identification and characterization of a novel collagenase in Xenopus laevis: possible roles during frog development. Mol. Biol. Cell 7, 1471–1483.

    PubMed  CAS  Google Scholar 

  125. Shi, Y.-B. and Sang, Q.-X. A. (1998) Collagenase 4. Handbook of Proteolytic Enzymes (Barrett, A. J., Rawlings, N. D., and Woessner, J. F., eds) Academic Press, London, pp. 1170–1172.

    Google Scholar 

  126. Damjanovski, S., Puzianowska-Kuznicka, M., Ishuzuya-Oka, A., and Shi, Y. B. (2000) Differential regulation of three thyroid hormone-responsive matrix metalloproteinase genes implicates distinct functions during frog embryogenesis. FASEB J. 14, 503–510.

    PubMed  CAS  Google Scholar 

  127. Cossins, J., Dudgeon, T. J., Catlin, G., Gearing, A. J., and Clements, J. M. (1996) Identification of MMP-18, a putative novel human matrix metalloproteinase. Biochem. Biophys. Res. Commun. 228, 494–498.

    Article  PubMed  CAS  Google Scholar 

  128. Pendás, A. M., Knäuper, V., Puente, X. S., et al. (1997) Identification and characterization of a novel human matrix metalloproteinase with unique structural characteristics, chromosomal location, and tissue distribution. J. Biol. Chem. 272, 4281–4286.

    Article  PubMed  Google Scholar 

  129. Kolb, C., Mauch, S., Peter, H. H., Krawinkel, U., and Sedlacek, R. (1997) The matrix metalloproteinase RASI-1 is expressed in synovial blood vessels of a rheumatoid arthritis patient. Immunol. Lett. 57, 83–88.

    Article  PubMed  CAS  Google Scholar 

  130. Sedlacek, R., Mauch, S., Kolb, B., et al. (1998) Matrix metalloproteinase MMP-19 (RASI 1) is expressed on the surface of activated peripheral blood mononuclear cells and is detected as an autoantigen in rheumatoid arthritis. Immunobiology 198, 408–423.

    PubMed  CAS  Google Scholar 

  131. Stracke, J. O., Hutton, M., Stewart, M., et al. (2000) Biochemical characterization of the catalytic domain of human matrix metalloproteinase 19 — Evidence for a role as a potent basement membrane degrading enzyme. J. Biol. Chem. 275, 14,809–14,816.

    Article  CAS  Google Scholar 

  132. DenBesten, P. K. and Heffernan, L. M. (1989) Separation by polyacrylamide gel electrophoresis of multiple proteases in rat and bovine enamel. Arch. Oral Biol. 34, 399–404.

    Article  PubMed  CAS  Google Scholar 

  133. Moradian-Oldak, J., Simmer, J. P., Sarte, P. E., Zeichner-David, M., and Fincham, A. G. (1994) Specific cleavage of a recombinant murine amelogenin at the carboxy-terminal region by a proteinase fraction isolated from developing bovine tooth enamel. Arch. Oral Biol. 39, 647–656.

    Article  PubMed  CAS  Google Scholar 

  134. Bartlett, J. D., Simmer, J. P., Xue, J., Margolis, H. C., and Moreno, E. C. (1996) Molecular cloning and mRNA tissue distribution of a novel matrix metalloproteinase isolated from porcine enamel organ. Gene 183, 123–128.

    Article  PubMed  CAS  Google Scholar 

  135. Llano, E., Pendás, A. M., Knäuper, V., et al. (1997) Identification and structural and functional characterization of human enamelysin (MMP-20). Biochemistry 36, 15,101–15,108.

    Article  CAS  Google Scholar 

  136. Yang, M. Z., Murray, M. T., and Kurkinen, M. (1997) A novel matrix metalloproteinase gene (XMMP) encoding vitronectin-like motifs is transiently expressed in Xenopus laevis early embryo development. J. Biol. Chem. 272, 13,527–13,533

    CAS  Google Scholar 

  137. Marchenko, G. N., Ratnikov, B. I., Rozanov, D. V., Godzik, A., Deryugina, E. I., and Strongin, A. Y. (2001) Characterization of matrix metalloproteinase-26, a novel metalloproteinase widely expressed in cancer cells of epithelial origin. Biochem. J. 356, 705–718.

    Article  PubMed  CAS  Google Scholar 

  138. Marchenko, G. N. and Strongin, A. Y. (2001) MMP-28, a new human matrix metalloproteinase with an unusual cysteine-switch sequence is widely expressed in tumors. Gene 265, 87–93.

    Article  PubMed  CAS  Google Scholar 

  139. Yang, M. Z. and Kurkinen, M. (1998) Cloning and characterization of a novel matrix metalloproteinase (MMP), CMMP, from chicken embryo fibroblasts — CMMP, Xenopus XMMP, and human MMP-19 have a conserved unique cysteine in the catalytic domain. J. Biol. Chem. 273, 17,893–17,900.

    CAS  Google Scholar 

  140. Gururajan, R., Lahti, J. M., Grenet, J., et al. (1998) Duplication of a genomic region containing the Cdc211-2 and MMP21-22 genes on human chromosome 1p36.3 and their linkage to d1z2. Genome Res. 8, 929–939.

    PubMed  CAS  Google Scholar 

  141. Gururajan R., Grenet, J., Lahti, J. M., and Kidd, V. J. (1998) Isolation and characterization of two novel metalloproteinase genes linked to the Cdc21 locus on human chromosome lp36.3. Genomics 52, 101–106.

    Article  PubMed  CAS  Google Scholar 

  142. Velasco, G., Pendás, A. M., Fueyo, A., Knäuper, V., Murphy, G., and López-Otín, C. (1999) Cloning and characterization of human MMP-23, a new matrix metalloproteinase predominantly expressed in reproductive tissues and lacking conserved domains in other family members. J. Biol. Chem. 274, 4570–4576.

    Article  PubMed  CAS  Google Scholar 

  143. Ohnishi, J., Ohnishi, E., Jin, M., et al. (2001) Cloning and characterization of a rat ortholog of MMP-23 (matrix metalloproteinase-23), a unique type of membraneanchored matrix metalloproteinase and conditioned switching of its expression during the ovarian follicular development. Mol. Endocrinol. 15, 747–764.

    Article  PubMed  CAS  Google Scholar 

  144. Pei, D. Q. (1999) CA-MMP: a matrix metalloproteinase with a novel cysteine array, but without the classic cysteine switch. FEBS Lett. 457, 262–270.

    Article  PubMed  CAS  Google Scholar 

  145. Pei, D. Q., Kang, T. B., and Qi, H. X. (2000) Cysteine array matrix metalloproteinase (CA-MMP)/MMP-23 is a type II transmembrane matrix metalloproteinase regulated by a single cleavage for both secretion and activation. J. Biol. Chem. 275, 33,988–33,997.

    CAS  Google Scholar 

  146. Pei, D. Q. (1999) Identification and characterization of the fifth membrane-type matrix metalloproteinase MT5-MMP. J. Biol. Chem. 274, 8925–8932.

    Article  PubMed  CAS  Google Scholar 

  147. Kinoh, H., Hayashita, H., Kajita, M., Okada, A., and Seiki, M. (1999) Assignment of the genes for membrane-type-4 matrix metalloproteinase (Mmp17, MMP17) to mouse chromosome 5, human chromosome band 12q24.3 and membrane-type-5 matrix metalloproteinase (Mmp24, MMP24) to mouse chromosome 2 and human chromosome band 20q11.2-Δ q12, respectively, by radiation hybrid and in situ hybridization. Cytogenet. Cell. Genet. 87, 97–98.

    Article  PubMed  CAS  Google Scholar 

  148. Llano, E., Pendás, A. M., Freije, J. P., et al. (1999) Identification and characterization of human MT5-MMP, a new membrane-bound activator of progelatinase a overexpressed in brain tumors. Cancer Res. 59, 2570–2576.

    PubMed  CAS  Google Scholar 

  149. Wang, X., Yi, J., Lei, J. X., and Pei, D. Q. (1999) Expression, purification and characterization of recombinant mouse MT5-MMP protein products. FEBS Lett. 462, 261–266.

    Article  PubMed  CAS  Google Scholar 

  150. Pei, D. (1999) Leukolysin/MMP25/MT6-MMP: a novel matrix metalloproteinase specifically expressed in the leukocyte lineage. Cell Res. 9, 291–303.

    Article  PubMed  CAS  Google Scholar 

  151. Velasco, G., Cal, S., Merlos-Suarez, A., et al. (2000) Human MT6-matrix metalloproteinase: Identification, progelatinase A activation, and expression in brain tumors. Cancer Res. 60, 877–882.

    PubMed  CAS  Google Scholar 

  152. English, W. R., Velasco, G., Stracke, J. O., Knäuper, V., and Murphy, G. (2001) Catalytic activities of membrane-type 6 matrix metalloproteinase (MMP25). FEBS Lett. 491, 137–142.

    Article  PubMed  CAS  Google Scholar 

  153. de Coignac, A. B., Elson, G., Delneste, Y., et al. (2000) Cloning of MMP-26 — A novel matrilysin-like proteinase. Eur. J. Biochem. 267, 3323–3329.

    Article  PubMed  Google Scholar 

  154. Park, H. I., Ni, J., Gerkema, F. E., Liu, D., Belozerov, V. E., and Sang, Q. X. A. (2000) Identification and characterization of human endometase (matrix metalloproteinase-26) from endometrial tumor. J. Biol. Chem. 275, 20,540–20,544.

    CAS  Google Scholar 

  155. Wang, H., Liu, C. Y., Song, Y. L., Gordon, D., Alavi, M. Z., and Moore, S. (2001) Expression of metallo-proteinases and its inhibitor in later stage of rabbit neointima development. Int. J. Mol. Med. 7, 105–112.

    PubMed  Google Scholar 

  156. Lohi, J., Wilson, C. L., Roby, J. D., and Parks, W. C. (2001) Epilysin, a novel human matrix metalloproteinase (MMP-28) expressed in testis and keratinocytes and in response to injury. J. Biol. Chem. 276, 10,134–10,144.

    Article  CAS  Google Scholar 

  157. Lepage, T. and Gache, C. (1989) Purification and characterization of the sea urchin embryo hatching enzyme. J. Biol. Chem. 264, 4787–4793.

    PubMed  CAS  Google Scholar 

  158. Lepage, T. and Gache, C. (1990) Early expression of a collagenase-like hatching enzyme gene in the sea urchin embryo. EMBO J. 9, 3003–3012.

    PubMed  CAS  Google Scholar 

  159. Nomura, K., Shimizu, T., Kinoh, H., Sendai, Y., Inomata, M., and Suzuki, N. (1997) Sea urchin hatching enzyme (envelysin) - cDNA cloning and deprivation of protein substrate specificity by autolytic degradation. Biochemistry 36, 7225–7238.

    Article  PubMed  CAS  Google Scholar 

  160. Gache, C., Lepage, T., Ghiglione, C., Emily-Fenouil, F., and Lhomond, G. (1998) Envelysin. Handbook of Proteolytic Enzymes (Barrett, A. J., Rawlings, N. D., and Woessner, J. F., eds) Academic Press, London, pp. 1195–1199.

    Google Scholar 

  161. Llano, E., Pendás, A. M., Aza-Blanc, P., Kornberg, T. B., and López-Otín, C. (2000) Dm1-MMP, a matrix metalloproteinase from Drosophila with a potential role in extracellular matrix remodeling during neural development. J. Biol. Chem. 275, 35,978–35,985.

    Article  CAS  Google Scholar 

  162. Wada, K., Sato, H., Kinoh, H., Kajita, M., Yamamoto, H., and Seiki, M. (1998) Cloning of three Caenorhabditis elegans genes potentially encoding novel matrix metalloproteinases. Gene 211, 57–62.

    Article  PubMed  CAS  Google Scholar 

  163. Leontovich, A. A., Zhang, J. S., Shimokawa, K., Nagase, H., and Sarras, M. P. (2000) A novel hydra matrix metalloproteinase (HMMP) functions in extracellular matrix degradation, morphogenesis and the maintenance of differentiated cells in the foot process. Development 127, 907–920.

    PubMed  CAS  Google Scholar 

  164. Ragster, L. and Chrispeels, M. J. (1979) Azocoll-digesting proteinases in soybean leaves: characteristics and changes during leaf maturation. Plant Physiol. 64, 857–862.

    PubMed  CAS  Google Scholar 

  165. Graham, J. S., Xiong, J., and Gillikin, J. W. (1991) Purification and developmental analysis of a metalloendoproteinase from the leaves of Glycine max. Plant Physiol. 97, 786–792.

    PubMed  CAS  Google Scholar 

  166. McGeehan, G., Burkhart, W., Anderegg, R., Becherer, J. D., Gillikin, J. W., and Graham, J. S. (1992) Sequencing and characterization of the soybean leaf metallo-proteinase. Structural and functional similarity to the matrix metalloproteinase family. Plant Physiol. 99, 1179–1183.

    PubMed  CAS  Google Scholar 

  167. McGeehan, G. and Graham, J. S. (1998) Soybean metalloproteinase 1. Handbook of Proteolytic Enzymes (Barrett, A. J., Rawlings, N. D., and Woessner, J. F., eds) Academic Press, London, pp. 1190–1192.

    Google Scholar 

  168. Maidment, J. M., Moore, D., Murphy, G. P., Murphy, G., and Clark, I. M. (1999) Matrix metalloproteinase homologues from Arabidopsis thaliana—Expression and activity. J. Biol. Chem. 274, 34,706–34,710.

    Article  CAS  Google Scholar 

  169. van Tassell, R. L., Lyerly, D. M., and Wilkins, T. D. (1992) Purification and characterization of an enterotoxin from Bacteroides fragilis. Infect. Immun. 60, 1343–1350.

    PubMed  Google Scholar 

  170. Moncrief, J. S., Obiso, R., Jr., Barroso, L. A., et al. (1995) The enterotoxin of Bacteroides fragilis is a metalloprotease. Infect. Immun. 63, 175–181.

    PubMed  CAS  Google Scholar 

  171. Obiso, R. J., Lyerly, D. M., van Tassell, R. L., and Wilkins, T. D. (1995) Proteolytic activity of the Bacteroides fragilis enterotoxin causes fluid secretion and intestinal damage in vivo. Infect. Immun. 63, 3820–3826.

    PubMed  CAS  Google Scholar 

  172. Obiso, R. J., Jr. and Wilkins, T. D. (1998) Fragilysin. Handbook of Proteolytic Enzymes (Barrett, A. J., Rawlings, N. D., and Woessner, J. F., eds) Academic Press, London, pp. 1211–1213.

    Google Scholar 

  173. Kuettner, K. E., Hiti, J., Eisenstein, R., and Harper, E. (1976) Collagenase inhibition by cationic proteins derived from cartilage and aorta. Biochem. Biophys. Res. Commun. 72, 40–46.

    Article  PubMed  CAS  Google Scholar 

  174. Welgus, H. G., Stricklin, G. P., Eisen, A. Z., Bauer, E. A., Cooney, R. V., and Jeffrey, J. J. (1979) A specific inhibitor of vertebrate collagenase produced by human skin fibroblasts. J. Biol. Chem. 254, 1938–1943.

    PubMed  CAS  Google Scholar 

  175. Cawston, T. E., Galloway, W. A., Mercer, E., Murphy, G., and Reynolds, J. J. (1981) Purification of rabbit bone inhibitor of collagenase. Biochem. J. 195, 159–165.

    PubMed  CAS  Google Scholar 

  176. Nolan, J. C., Ridge, S. C., Oronsky, A. L., and Kerwar, S. S. (1980) Purification and properties of a collagenase inhibitor from cultures of bovine aorta. Atherosclerosis 35, 93–102.

    Article  PubMed  CAS  Google Scholar 

  177. Docherty, A. J. P., Lyons, A., Smith, B. J., et al. (1985) Sequence of human tissue inhibitor of metallo-proteinases and its identity to erythroid-potentiating activity. Nature 318, 66–69.

    Article  PubMed  CAS  Google Scholar 

  178. Gauwerky, C. E., Lusis, A. J., and Golde, D. W. (1980) Erythroid-potentiating activity: characterization and target cells. Exp. Hematol. 8, 117–127.

    PubMed  CAS  Google Scholar 

  179. Gasson, J.C., Golde, D.W., Kaufman, S.E., et al. (1985) Molecular characterization and expression of the gene encoding human erythroid-potentiating activity. Nature 315, 768–771.

    Article  PubMed  CAS  Google Scholar 

  180. Edwards, D. R., Parfett, C. L., and Denhardt, D. T. (1985) Transcriptional regulation of two serum-induced RNAs in mouse fibroblasts: equivalence of one species to B2 repetitive elements. Mol. Cell. Biol. 5, 3280–3288.

    PubMed  CAS  Google Scholar 

  181. Johnson, M. D., Housey, G. M., Kirschmeier, P. T., and Weinstein, I. B. (1987) Molecular cloning of gene sequences regulated by tumor promoters and mitogens through protein kinase C. Mol. Cell. Biol. 7, 2821–2829.

    PubMed  CAS  Google Scholar 

  182. Gewert, D. R., Coulombe, B., Castelino, M., Skup, D., and Williams, B. R. G. (1987) Characterization and expression of a murine gene homologous to human EPA/TIMP: a virus-induced gene in the mouse. EMBO J. 6, 651–657.

    PubMed  CAS  Google Scholar 

  183. Satoh, T., Kobayashi, K., Yamashita, S., Kikuchi, M., Sendai, Y., and Hoshi, H. (1994) Tissue inhibitor of metalloproteinases (TIMP-1) produced by granulosa and oviduct cells enhances in vitro development of bovine embryo. Biol. Reprod. 50, 835–844.

    Article  PubMed  CAS  Google Scholar 

  184. Boujrad, N., Ogwuegbu, S. O., Garnier, M., Lee, C. H., Martin, B. M., and Papadopoulos, V. (1995) Identification of a stimulator of steroid hormone synthesis isolated from testis. Science 268, 1609–1612.

    Article  PubMed  CAS  Google Scholar 

  185. Hayakawa, T. (1994) Tissue inhibitors of metalloproteinases and their cell growth-promoting activity. Cell Struct. Funct. 19, 109–114.

    Article  PubMed  CAS  Google Scholar 

  186. Gomez, D. E., Alonso, D. F., Yoshiji, H., and Thorgeirsson, U. P. (1997) Tissue inhibitors of metalloproteinases-structure, regulation and biological functions. Eur. J. Cell Biol. 74, 111–122.

    PubMed  CAS  Google Scholar 

  187. Goldberg, G. I., Marmer, B. L., Grant, G. A., Eisen, A. Z., Wilhelm, S., and He, C. S. (1989) Human 72-kilodalton type IV collagenase forms a complex with a tissue inhibitor of metalloproteases designated TIMP-2. Proc. Natl. Acad. Sci. USA 86, 8207–8211.

    Article  PubMed  CAS  Google Scholar 

  188. Herron, G. S., Banda, M. J., Clark, E. J., Gavrilovic, J., and Werb, Z. (1986) Secretion of metalloproteinases by stimulated capillary endothelial cells. II. Expression of collagenase and stromelysin activities is regulated by endogenous inhibitors. J. Biol. Chem. 261, 2814–2818.

    PubMed  CAS  Google Scholar 

  189. Raynes, J. G., Clarke, F. A., Anderson, J. C., Fitzpatrick, R. J., and Dobson, H. (1988) Collagenase inhibitor concentration in cultured cervical tissue of sheep is increased in late pregnancy. J. Reprod. Fertil. 83, 893–900.

    Article  PubMed  CAS  Google Scholar 

  190. De Clerck, Y. A., Yean, T.-D., Ratzkin, B. J., Lu, H. S., and Langley, K. E. (1989) Purification and characterization of two related but distinct metalloproteinase inhibitors secreted by bovine aortic endothelial cells. J. Biol. Chem. 264, 17,445–17,453.

    Google Scholar 

  191. Stetler-Stevenson, W. G., Krutzsch, H. C., and Liotta, L. A. (1989) Tissue inhibitor of metalloproteinase (TIMP-2). A new member of the metalloproteinase inhibitor family. J. Biol. Chem. 264, 17,374–17,378.

    CAS  Google Scholar 

  192. Stetler-Stevenson, W. G., Brown, P. D., Onisto, M., Levy, A. T., and Liotta, L. A. (1990) Tissue inhibitor of metalloproteinases-2 (TIMP-2) mRNA expression in tumor cell lines and human tumor tissues. J. Biol. Chem. 265, 13,933–13,938.

    CAS  Google Scholar 

  193. Matsumoto, H., Ishibashi, Y., Ohtaki, T., Hasegawa, Y., Koyama, C., and Inoue, K. (1993) Newly established murine pituitary folliculo-stellate-like cell line (TtT/GF) secretes potent pituitary glandular cell survival factors, one of which corresponds to metalloproteinase inhibitor. Biochem. Biophys. Res. Commun. 194, 909–915.

    Article  PubMed  CAS  Google Scholar 

  194. Nemeth, J. A., and Goolsby, C. L. (1993) TIMP-2, a growth-stimulatory protein from SV40-transformed human fibroblasts. Exp. Cell. Res. 207, 376–382.

    Article  PubMed  CAS  Google Scholar 

  195. Osawa, K., Shirai, T., Yanagawa, M., Yamada, K., Nishikawa, K., and Tanaka, H. (1994) Purification and characterization of growth and differentiation factors from human osteosarcoma cell line, OST-1-PF, in Animal Cell Technology: Basic and Applied Aspects (Kobayashi, T., Kitagawa, Y., and Okumura, K., eds), Kluwer, Dordrecht, pp. 589–593.

    Google Scholar 

  196. Murphy, G. and Willenbrock, F. (1995) Tissue inhibitors of matrix metalloendopeptidases. Methods Enzymol. 248, 496–510.

    Article  PubMed  CAS  Google Scholar 

  197. Blenis, J. and Hawkes, S. P. (1983) Transformation-sensitive protein associated with the cell substratum of chicken embryo fibroblasts. Proc. Natl. Acad. Sci. USA 80, 770–774.

    Article  PubMed  CAS  Google Scholar 

  198. Blenis, J. and Hawkes, S. P. (1984) Characterization of a transformation-sensitive protein in the extracellular matrix of chicken embryo fibroblasts. J. Biol. Chem. 259, 11,563–11,570.

    CAS  Google Scholar 

  199. Staskus, P. W., Masiarz, F. R., Pallanck, L. J., and Hawkes, S. P. (1991) The 21-kDa protein is a transformation-sensitive metalloproteinase inhibitor of chicken fibroblasts. J. Biol. Chem. 266, 449–454.

    PubMed  CAS  Google Scholar 

  200. Pavloff, N., Staskus, P. W., Kishnani, N. S., and Hawkes, S. P. (1992) A new inhibitor of metalloproteinases from chicken: ChIMP-3. A third member of the TIMP family. J. Biol. Chem. 267, 17,321–17,326.

    CAS  Google Scholar 

  201. Apte, S. S., Hayashi, K., Seldin, M. F., Mattei, M. G., Hayashi, M., and Olsen, B.R. (1994) Gene encoding a novel murine tissue inhibitor of metalloproteinases (TIMP), TIMP-3, is expressed in developing mouse epithelia, cartilage, and muscle, and is located on mouse chromosome 10. Dev. Dyn. 200, 177–197.

    PubMed  CAS  Google Scholar 

  202. Weber, B. H. F., Vogt, G., Pruett, R. C., Stohr, H., and Felbor, U. (1994) Mutations in the tissue inhibitor of metalloproteinases-3 (TIMP3) in patients with Sorsby’s fundus dystrophy. Nature Genet. 8, 352–356.

    Article  PubMed  CAS  Google Scholar 

  203. Yu, W. H., Yu, S. S. C., Meng, Q., Brew, K., and Woessner, J. F. (2000) TIMP-3 binds to sulfated glycosaminoglycans of the extracellular matrix. J. Biol. Chem. 275, 31,226–31,232.

    CAS  Google Scholar 

  204. Greene, J., Wang, M., Liu, Y. E., Raymond, L. A., Rosen, C., and Shi, Y. E. (1996) Molecular cloning and characterization of human tissue inhibitor of metalloproteinase 4. J. Biol. Chem. 271, 30,375–30,380.

    CAS  Google Scholar 

  205. Bigg, H. F., Shi, Y. E., Liu, Y. L. E., Steffensen, B., and Overall, C. M. (1997) Specific, high affinity binding of tissue inhibitor of metalloproteinases-4 (TIMP4) to the COOH-terminal hemopexin-like domain of human gelatinase A - TIMP-4 binds progelatinase A and the COOH-terminal domain in a similar manner to TIMP-2. J. Biol. Chem. 272, 15,496–15,500.

    Article  CAS  Google Scholar 

  206. Leco, K. J., Apte, S. S., Taniguchi, G. T., et al. (1997) Murine tissue inhibitor of metalloproteinases-4 (TIMP-4): cDNA isolation and expression in adult mouse tissues. FEBS Lett. 401, 213–217.

    Article  PubMed  CAS  Google Scholar 

  207. Douglas, D. A., Shi, Y. E., and Sang, Q. X. A. (1997) Computational sequence analysis of the tissue inhibitor of metalloproteinase family. J. Protein Chem. 16, 237–255.

    Article  PubMed  CAS  Google Scholar 

  208. Mott, J. D., Takahara, K., Rosenbach, M. T., et al. (1998) A novel matrix metalloproteinase inhibitor in human brain tumors. FASEB J. 11, A1255.

    Google Scholar 

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  1. Dept. Biochem. Mol. Biol. R-127, Univ. Miami School of Med., P.O. Box 016960, 33101, Miami, FL

    J. Frederick Woessner

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  1. J. Frederick Woessner
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Correspondence to J. Frederick Woessner.

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Woessner, J.F. MMPs and TIMPs—An historical perspective. Mol Biotechnol 22, 33–49 (2002). https://doi.org/10.1385/MB:22:1:033

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