Structural basis of the matrix metalloproteinases and their physiological inhibitors, the tissue inhibitors of metalloproteinases

Biological Chemistry

Volumn 384, Issue 6, 2003, Pages 863-872

  Bode, Wolfram ^a   Maskos, Klaus ^a  

^a MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

Author keywords

Crystal Structures; Matrix metalloproteinases (MMPs); Substrate specificity; Tissue inhibitors of metalloproteinases (TIMPs)

Indexed keywords

MATRIX METALLOPROTEINASE; PROTEINASE; TISSUE INHIBITOR OF METALLOPROTEINASE;

ARTHRITIS; COMPLEX FORMATION; ENZYME ACTIVE SITE; ENZYME SPECIFICITY; EXTRACELLULAR MATRIX; HUMAN; METASTASIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN STRUCTURE; REVIEW; STRUCTURE ACTIVITY RELATION; TUMOR GROWTH;

CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; HUMANS; MATRIX METALLOPROTEINASES; MODELS, MOLECULAR; TISSUE INHIBITOR OF METALLOPROTEINASES;

EID: 0037810391     PISSN: 14316730     EISSN: None     Source Type: Journal    
DOI: 10.1515/BC.2003.097     Document Type: Review

References (75)

1. Barrett, A.J., Rawlings, N.D. and Woessner Jr., J.F. (1998). Handbook of Proteolytic Enzymes (London, UK: Academic Press).
2. Becker, J.W., Marcy, A.I., Rokosz, L.L., Axel, M.G., Burbaum, J.J., Fitzgerald, P.M.D., Cameron, P.M., Esser, C.K., Hagmann, W.K., Hermes, J.D. and Springer, J.P. (1995). Stromelysin-1: three-dimensional structure of the inhibited catalytic domain and of the C-truncated proenzyme. Protein Sci. 4, 1966-1976.
3. Bode, W., Maskos, K. (2000). Structural studies on MMPs and TIMPs. In: Methods in Molecular Biology, Matrix Metalloproteinase Protocols 151, 45-77.
4. 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'. FEES Lett. 331, 134-140.
5. Bode, W., Reinemer P., Huber, R., Kleine, T., Schnierer, S. and Tschesche, H. (1994). The X-ray crystal structure of the catalytic domain of human neutrophil collagenase inhibited by a substrate analogue reveals the essentials for catalysis and specificity. EMBO J. 13, 1263-1269.
6. Bode W, Fernandez-Catalan C, Tschesche H, Grams F, Nagase H, and Maskos K. (1999). Structural properties of matrix metalloproteinases. Cell Mol. Life Sci. 55, 639-652.
7. Borkakoti, N., Winkler, F.K., Williams, D.H., D'Arcy, A., Broadhurst, M.J., Brown, P.A., Johnson, W.H. and Murray, E.J. (1994). Structure of the catalytic domain of human fibroblast collagenase complexed with an inhibitor. Nature Struct. Biol. 1, 106-110
8. Brandstetter, H., Grams, F., Glitz, D., Lang, A., Huber, R., Bode, W., Krell, H.-W., Engh, and R.A. (2001) The 1.8-Å crystal structure of a matrix metalloproteinase 8-barbiturate inhibitor complex reveals a previously unobserved mechanism for collagenase substrate recognition. J. Biol. Chem. 276, 17405-17412.
9. Brew, K., Dinakarpandian, D., and Nagase, H. (2000). Tissue inhibitors of metalloproteinases: evolution, structure and function. Biochim. Biophys. Acta 1477, 267-283.
10. Brinckerhoff, C.E. and Matrisian, L.M. (2002). Matrix metalloproteinases: a tail of a frog that became a prince. Nature Rev. Mol. Biol. 3, 207-214.
11. Browner, M.F., Smith, W.W. and Castelhano, A.L. (1995). Matrilysin-inhibitor complexes: common themes among metalloproteases. Biochemistry 34, 6602-6610.
12. Butler, G.S., Will, H., Atkinson, S.J. and Murphy, G. (1997). Membrane-type-2 matrix metalloproteinase can initiate the processing of progelatinase A and is regulated by the tissue inhibitors of metalloproteinases. Eur. J. Biochem. 244, 653-657.
13. Butler, G.S., Butler, M.J., Atkinson, S.J., Will, H., Tamura, T., van Westrum, S.S., Crabbe, T., Clements, J., d'Ortho, M.P. and Murphy, G. (1998). The TIMP2 membrane type 1 metalloproteinase 'receptor' regulates the concentration and efficient activation of progelatinase A. J. Biol. Chem. 273, 871-880.
14. Butler, G.S., Apte, S.S., Willenbrock, F., and Murphy, G. (1999). Human tissue inhibitor of metalloproteinases 3 interacts with both the N- and C-terminal domains of gelatinases A and B. Regulation by polyanions. J. Biol. Chem. 274, 10846-10851.
15. Cao, J., Shinagawa, A., Yamamoto, E. and Seiki, M. (1994). A matrix metalloproteinase expressed on the surface of invasive tumour cells. Nature 370, 61-65.
16. Cao, J., Sato, H., Takino, T., and Seiki, M. (1995). The C-terminal region of membrane type matrix metalloproteinase is a functional transmembrane domain required for progelatinase A activation. J. Biol. Chem. 270, 801-805.
17. Cha, H., Kopetzki, E., Huber, R., Lanzendorfer, M., Brandstetter, H. (2002). Structural basis of the adaptive molecular recognition by MMP9. J. Mol. Biol. 320, 1065-1079.
18. Chung, L., Shimokawa, K., Dinakarpandian, D., Grams, F., Fields, G.B., and Nagase, H. (2000). Identification of the (183)RWTNNFREY(191) region as a critical segment of matrix metalloproteinase 1 for the expression of collagenolytic activity. J. Biol. Chem. 275, 29610-29617.
19. Dhanaraj, V., Williams, M.G., Ye, Q.-Z., Molina, F., Johnson, L.L., Ortwine, D.F., Pavlovshy, A., Rubin, R., Skeean, R.W., White, A.D. et al. (1999). X-ray structure of gelatinase A catalytic domain complexed with a hydroxamate inhibitor. Croat. Chem. Acta 72, 575-591.
20. Deryugina, E.I., Ratnikov, B., Monosov, E., Postnova, T.I., DiScipio R., Smith J.W., and Strongin A.Y. (2001). MT1-MMP initiates activation of pro-MMP-2 and integrin αvβ3 promotes maturation of MMP-2 in breast carcinoma cells. Exp. Cell Res. 263, 209-223.
21. Dove, A. (2002). MMP inhibitors: glimmers of hope amidst clinical failures. Nature Med. 8, 95.
22. Elkins, P.A., Ho, Y.S., Smith, W.W., Janson, C.A., D'Alessio, K.J., McQueney, M.S., Cummings, M.D., and Romanic, A.M. (2002). Structure of the C-terminally truncated human ProMMP9, a gelatin-binding matrix metalloproteinase. Acta Crystallogr. D Biol. Crystallogr. 58, 1182-1192.
23. Fernandez-Catalan, C., Bode, W., Huber, R., Turk, D., Calvete, J.J., Lichte, A., Tschesche, H. and Maskos, K. (1998). Crystal structure of the complex formed by the membrane type 1-matrix metalloproteinase with the tissue inhibitor of metalloproteinases-2, the soluble progelatinase A receptor. EMBO J. 17, 5238-5248.
24. Gall, A.L., Ruff, M., Kannan, R., Cuniasse, P., Yiotakis, A., Dive, V., Rio, M.C., Basset, P., and Moras, D. (2001). Crystal structure of the stromelysin-3 (MMP-11) catalytic domain complexed with a phosphinic inhibitor mimicking the transition-state. J. Mol. Biol. 307, 577-586.
25. Giavazzi, R., and Taraboletti, G. (2001). Preclinical development of metalloproteasis inhibitors in cancer therapy. Crit. Rev. Oncol./Hematol. 37, 53-60.
26. 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.
27. Gomis-Rüth, F.X., Maskos, K., Betz, M., Bergner, A., Huber, R., Suzuki, K., Yoshida, N., Nagase, H., Brew, K., Bourenkov, G.P., Bartunik, H. and Bode, W. (1997). Mechanism of inhibition of the human matrix metalloproteinase stromelysin-1 by TIMP-1. Nature 389, 77-81.
28. Gooley, P.R., O'Connell, J.F., Marcy, A.I., Cuca, G.C., Salowe, S.P., Bush, B.L., Hermes, J.D., Esser, C.K., Hagmann, W.K., Springer, J.P. and Johnson, B.A. (1994). NMR structure of inhibited catalytic domain of human stromelysin-1. Nature Struct. Biol. 1, 111-118.
29. Grams, F., Reinemer, P., Powers, J.C., Kleine, T., Pieper, M., Tschesche, H., Huber, R. and Bode, W. (1995). X-ray structures of human neutrophil collagenase complexed with peptide hydroxamate and peptide thiol inhibitors. Implications for substrate binding and rational drug design. Eur. J. Biochem. 228, 830-841.
30. Hidalgo, M. and Eckhardt, S.G. (2001). Development of matrix metalloproteinase inhibitors in cancer therapy. J. Natl. Cancer Inst. 93, 178-193.
31. 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, 34260-34266
32. Itoh, Y., Takamura, A., Ito, N., Maru, Y., Sato, H., Suenaga, N., Aoki, T., Seiki, M. (2001). Homophilic complex formation of MT1-MMP facilitates proMMP-2 activation on the cell surface and promotes tumor cell invasion. EMBO J. 20, 4782-4793.
33. Kang, T., Nagase, H., and Pei, D. (2002). Activation of membrane-type matrix metalloproteinase 3 zymogen by the proprotein convertase furin in the trans-Golgi network. Cancer Res. 62, 675-681.
34. Kinoshita, T., Sato, H., Takino, T., Itoh, M., Akizawa, T. and Seiki, M. (1996). Processing of a precursor of 72-kilodalton type IV collagenase/gelatinase A by a recombinant membrane-type 1 matrix metalloproteinase. Cancer Res. 56, 2535-2538.
35. Kraulis, P.J. (1991). MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr. 24, 946-950.
36. Lang, R., Kocourek, A., Braun, M., Tschesche, H., Huber, R., Bode, W., and Maskos, K. (2001). Substrate specificity determinants of human macrophage elastase (Mmp-12) based on the 1.1 Å crystal structure. J. Mol. Biol. 312, 731-742.
37. Lehti, K., Lohi, J., Juntunen, M.M., Pei, D., and Keski-Oja, J. (2002). Oligomerization through hemopexin and cytoplasmic domains regulates the activity and turnover of membrane-type 1 matrix metalloproteinase. J. Biol. Chem. 277, 8440-8448.
38. Li, J.-Y., Brick, P., O'Hare, M.C., Skarzynski, T., Lloyd, L.F., Curry, V.A., Clark, I.M., Bigg, H.F., Hazleman, B.L., Cawston, T.E. and Blow, D.M. (1995). Structure of full-length porcine synovial collagenase reveals a C-terminal domain containing a calcium-linked, four-bladed β-propeller. Structure 3, 541-549.
39. Lovejoy, B., Cleasby, A., Hassell, A.M., Longley, K., Luther, M.A., Weigl, D., McGeehan, G., McElroy, A.B., Drewry, D., Lambert, M.H. and Jordan, S.R. (1994). Structure of the catalytic domain of fibroblast collagenase complexed with an inhibitor. Science 263, 375-377.
40. Lovejoy, B., Welch, A.R., Carr, S., Luong, C., Broka, C., Hendricks, R.T., Campbell, J.A., Walker, K.A.M., Martin, R., Van Wart, H. and Browner, M.F. (1999). Crystal structures of MMP-1 and -13 reveal the structural basis for selectivity of collagenase inhibitors. Nature Struct. Biol. 6, 217-221.
41. Massova, I., Kotra, L.P, Fridman, R. and Mobashery, S. (1998). Matrix metalloproteinases: structures, evolution, and diversification. FASEB J. 12, 1075-1095.
42. Matthews, B.W. (1988). Structural basis of the action of thermolysin and related zinc peptidases. Acc. Chem. Res. 21, 333-340.
43. Merritt, E.A. and Bacon, D.J. (1997). Raster3D photorealistic molecular graphics. Methods Enzymol. 277, 505-527.
44. Morgunova, E., Tuuttila, A., Bergmann, U., Isupov, M., Lindqvist, Y., Schneider, G., and Tryggvason, K. (1999). Structure of human pro-matrix metalloproteinase-2: activation mechanism revealed. Science 284, 1667-1670.
45. Morgunova, E., Tuuttila, A., Bergmann, U., and Tryggvason, K. (2002). Structural insight into the complex formation of latent matrix metalloproteinase 2 with tissue inhibitor of metalloproteinase 2. Proc. Nat. Acad. Sci. USA 99, 7414-7419.
46. Morrison, C.J., Butler, G.S., Bigg, H.F., Roberts, C.R., Soloway, P.D., and Overall, C.M. (2001). Cellular activation of MMP-2 (gelatinase A) by MT2-MMP occurs via a TIMP-2-independent pathway. J. Biol. Chem. 276, 47402-47410.
47. Murphy, G. and Willenbrock, F. (1995). Tissue inhibitors of matrix metalloendopeptidases. Methods Enzymol. 248, 496-510.
48. Murphy, G. and Knäuper, V. (1997). Relating matrix metalloproteinase structure to function: why the 'hemopexin' domain? Matrix Biol. 15, 511-518.
49. Murphy, G., Houbrechts, A., Cockett, M.I., Williamson, R.A., O'Shea, M. and Docherty, A.J.R (1991). The N-terminal domain of human tissue inhibitor of metalloproteinases retains metalloproteinase inhibitory activity. Biochemistry 30, 8097-8102.
50. Muskett, F.W., Frenkiel, T.A., Feeney, J., Freedman, R.B., Carr, M.D. and Williamson, R. (1998). High resolution structure of the N-terminal domain of tissue inhibitor of metalloproteinases-2 and characterization of its interaction site with matrix metalloproteinase-3. J. Biol. Chem. 273, 21736-21743.
51. Nagase, H. (1997). Activation mechanisms of matrix metalloproteinases. Biol. Chem. 378, 151-160.
52. Nar, H., Werle, K., Bauer, M.M., Dollinger, H., and Jung, B. (2001). Crystal structure of human macrophage elastase (MMP-12) in complex with a hydroxamic acid inhibitor. J. Mol. Biol. 312, 743-751.
53. Opdenakker, G., Van den Steen, P.E., and Van Damme, J. (2001). Gelatinase B: a tuner and amplifier of immune functions. Trends Immunol. 22, 571-579.
54. Ottl, J., Gabriel, D., Murphy, G., Knäuper, V., Tominaga, Y., Nagase, H., Kroger, M., Tschesche, H., Bode, W., and Moroder, L. (2000). Recognition and catabolism of synthetic heterotrimeric collagen peptides by matrix metalloproteinases. Chem Biol. 7, 119-132.
55. Overall, C.M. (2002). Molecular determinants of metalloproteinase substrate specificity: matrix metalloproteinase substrate binding domains, modules, and exosites. Mol. Biotechnol. 22, 51-86.
56. Overall, C.M., King, A.E., Bigg, H.F., McQuibban, A., Atherstone, J., Sam, D.K., Ong, A.D., Lau, T.T., Wallon, U.M., DeClerck, Y.A., and Tam, E. (1999). Identification of the TIMP-2 binding site on the gelatinase A hemopexin C-domain by site-directed mutagenesis and the yeast two-hybrid system. Ann. NY Acad. Sci. 878, 747-753.
57. Pei, D. (1999). A-MMP: a matrix metalloproteinase with a novel cysteine array, but without the classic cysteine switch. FEBS Lett. 457, 262-270.
58. Pei, D., and Weiss, S.J. (1995). Furin-dependent intracellular activation of the human stromelysin-3 zymogen. Nature 375, 244-247.
59. Pei, D., Kang, T., Qi, H. (2000). Cysteine array matrix metalloproteinase (CA-MMP)/MMP-23 is atype II transmembrane matrix metalloproteinase regulated by a single cleavage for both secretion and activation. J. Biol. Chem. 275, 33988-33997.
60. Reinemer, P., Grams, F., Huber, R., Kleine, T., Schnierer, S., Pieper, M., Tschesche, H. and Bode, W. (1994). Structural implications for the role of the N-terminus in the 'superactivation' of collagenases - a crystallographic study. FEBS Lett. 338, 227-233.
61. Rowsell, S., Hawtin, P., Minshull, C.A., Jepson, H., Brockbank, S.M., Barratt, D.G., Slater, A.M., McPheat, W.L., Waterson, D., Henney, A.M., and Pauptit, R.A. (2002). Crystal structure of human MMP9 in complex with a reverse hydroxamate inhibitor. J. Mol. Biol. 319, 173-181.
62. Rozanov, D.V., Deryugina, E.I., Ratnikov, B.I., Monosov, E.Z., Marchenko, G.N., Quigley, J.P., and Strongin, A.Y. (2001). Mutation analysis of membrane type-1 matrix metalloproteinase (MT1-MMP). The role of the cytoplasmic tail Cys(574), the active site Glu(240), and furin cleavage motifs in oligomerization, processing, and self-proteolysis of MT1-MMP expressed in breast carcinoma cells. J. Biol. Chem. 276, 25705-25714.
63. Sato, H., Takino, T., Okada, Y., Cao, J., Shinagawa, A., Yamamoto, E. and Seiki, M. (1994). A matrix metalloproteinase expressed on the surface of invasive tumour cells. Nature 370, 61-65.
64. Schechter, I. and Berger, A. (1967). On the size of the active site in proteases. I. Papain. Biochem. Biophys. Res. Commun. 27, 157-162.
65. Spurlino, J.C., Smallwood, A.M., Carlton, D.D., Banks, T.M., Vavra, K.J., Johnson, J.S., Cook, E.R., Falvo, J., Wahl, R.C., Pulvino, T.A., Wendoloski, J.J. and Smith, D.L. (1994). 1.56Å structure of mature truncated human fibroblast collagenase. Proteins: Struct. Funct. Genet. 19, 98-109.
66. Stams, T., Spurlino, J.C., Smith, D.L., Wahl, R.C., Ho, T.F., Qoronfleh, M.W., Banks, T.M. and Rubin, B. (1994). Structure of human neutrophil collagenase reveals large S1' specificity pocket. Nature Struct. Biol. 1, 119-123.
67. Sternlicht, M.D., and Werb, Z. (2001). How matrix metalloproteinases regulate cell behaviour. Annu. Rev. Cell Dev. Biol. 17, 463-516.
68. Stöcker, W., Grams, F., Baumann, U., Reinemer, P., Gomis-Rüth, F.X., McKay, D.B. and Bode, W. (1995). The metzincins-topological and sequential relations between the astacins, adamalysins, serralysins, and matrixins (collagenases) define a superfamily of zinc-peptidases. Protein Sci. 4, 823-840.
69. Strongin, A.Y., Collier, I.E., Bannikov, U., Marmer, B.L., Grant, G.A. and Goldberg, G.I. (1995). Mechanism of cell surface activation of 72-kDa type IV collagenase. J. Biol. Chem. 270, 5331-5338.
70. Tuuttila, A., Morgunova, E., Bergmann, U., Lindquist, Y., Maskos, K., Fernandez-Catalan, C., Bode, W., Tryggvason, K. and Schneider, G. (1998). Three-dimensional structure of human tissue inhibitor of metalloproteinases-2 at 2.1 Å resolution. J. Mol. Biol. 284, 1133-1140.
71. Van Wart, H.E. and Birkedal-Hansen, H. (1990). The cysteine switch: a principle of regulation of metalloproteinase activity with potential applicability to the entire matrix metalloproteinase gene family. Proc. Natl. Acad. Sci. USA 87, 5578-5582.
72. Velasco, G., Pendas, A.M., Fueyo, A., Knäuper, V., Murphy, G., and Lopez-Otin, 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.
73. Williamson, R.A., Martorell, G., Carr, M.D., Murphy, G., Docherty, A.J., Freedman, R.B. and Feeney, J. (11994). Solution structure of the active domain of tissue inhibitor of metalloproteinases-2. A new member of the OB fold protein family. Biochemistry 33, 11745-11759.
74. Woessner, J.F. and Nagase, H. (2000). Matrix metalloproteinases and TIMPs (New York, USA: Oxford University Press).
75. Wu B., Arumugam, S., Gao, G., Le, G., Semenchenko, V., Huang, W., Brew, K. and VanDoren, S.R. (2000). NMR structure of tissue inhibitor of metalloproteinases-1 implicates localized induced fit in recognition of matrix metalloproteinases. J. Mol. Biol. 295, 257-268.