Future challenges facing the development of specific active-site-directed synthetic inhibitors of MMPs

Biochimie

Volumn 87, Issue 3-4 SPEC. ISS., 2005, Pages 393-402

  Cuniasse, P ^a   Devel, L ^a   Makaritis, A ^b   Beau, F ^a   Georgiadis, D ^b   Matziari, M ^b   Yiotakis, A ^b   Dive, V ^a  

^a CEA SACLAY   (France)

^b UNIVERSITY OF ATHENS   (Greece)

Author keywords

Conformational variability; Inhibitor selectivity; Inhibitors; MMPs; Zinc protease

Indexed keywords

MATRIX METALLOPROTEINASE;

ARTICLE; CONFORMATIONAL TRANSITION; ENZYME ACTIVE SITE; ENZYME INHIBITION; ENZYME SPECIFICITY; ENZYME STRUCTURE; ENZYME SYNTHESIS; PROTEIN DOMAIN; PROTEIN FAMILY; STRUCTURE ANALYSIS;

EID: 15244350894     PISSN: 03009084     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biochi.2004.09.025     Document Type: Short Survey

References (69)

1. M. Whittaker, C.D. Floyd, P. Brown, and A.J. Gearing Design and therapeutic application of matrix metalloproteinase inhibitors Chem. Rev. 99 1999 2735 2776
2. K.R. Acharya, E.D. Sturrock, J.F. Riordan, and M.R. Ehlers Ace revisited: a new target for structure-based drug design Nat. Rev. Drug Discov. 2 2003 891 902
3. L.M. Coussens, B. Fingleton, and L.M. Matrisian Matrix metalloproteinase inhibitors and cancer: trials and tribulations Science 295 2002 2387 2392
4. M. Egeblad, and Z. Werb New functions for the matrix metalloproteinases in cancer progression Nat. Rev. Cancer 2 2002 161 174
5. C. Lopez-Otin, and C.M. Overall Protease degradomics: a new challenge for proteomics Nat. Rev. Mol. Cell Biol. 3 2002 509 519
6. A. Amour, P.M. Slocombe, A. Webster, M. Butler, C.G. Knight, and B.J. Smith TNF-alpha converting enzyme (TACE) is inhibited by TIMP-3 FEBS Lett. 435 1998 39 44
7. B.E. Turk, T.Y. Wong, R. Schwarzenbacher, E.T. Jarrell, S.H. Leppla, R.J. Collier, R.C. Liddington, and L.C. Cantley The structural basis for substrate and inhibitor selectivity of the anthrax lethal factor Nat. Struct. Mol. Biol. 11 2004 60 66
8. A. Saghatelian, N. Jessani, A. Joseph, M. Humphrey, and B.F. Cravatt Activity-based probes for the proteomic profiling of metalloproteases Proc. Natl. Acad. Sci. USA 101 2004 10000 10005
9. A. Makaritis, D. Georgiadis, V. Dive, and A. Yiotakis Diastereoselective solution and multipin-based combinatorial array synthesis of a novel class of potent phosphinic metalloprotease inhibitors Chemistry 9 2003 2079 2094
10. J. Jiracek, A. Yiotakis, B. Vincent, F. Checler, and V. Dive Development of the first potent and selective inhibitor of the zinc endopeptidase neurolysin using a systematic approach based on combinatorial chemistry of phosphinic peptides J. Biol. Chem. 271 1996 19606 19611
11. J. Jiracek, A. Yiotakis, B. Vincent, A. Lecoq, A. Nicolaou, and F. Checler Development of highly potent and selective phosphinic peptide inhibitors of zinc endopeptidase 24-15 using combinatorial chemistry J. Biol. Chem. 270 1995 21701 21706
12. V. Dive, J. Cotton, A. Yiotakis, A. Michaud, S. Vassiliou, and J. Jiracek RXP 407, a phosphinic peptide, is a potent inhibitor of angiotensin I converting enzyme able to differentiate between its two active sites Proc. Natl. Acad. Sci. USA 96 1999 4330 4335
13. S.X. Peng, M.J. Strojnowski, J.K. Hu, B.J. Smith, T.H. Eichhold, and K.R. Wehmeyer Gas chromatographic-mass spectrometric analysis of hydroxylamine for monitoring the metabolic hydrolysis of metalloprotease inhibitors in rat and human liver microsomes J. Chromatogr. B Biomed. Sci. Appl. 724 1999 181 187
14. B. Lovejoy, A.R. Welch, S. Carr, C. Luong, C. Broka, and R.T. Hendricks Crystal structures of MMP-1 and -13 reveal the structural basis for selectivity of collagenase inhibitors Nat. Struct. Biol. 6 1999 217 221
15. B. Lovejoy, A. Cleasby, A.M. Hassell, K. Longley, M.A. Luther, and D. Weigl Structure of the catalytic domain of fibroblast collagenase complexed with an inhibitor Science 263 1994 375 377
16. I. Bertini, V. Calderone, M. Fragai, C. Luchinat, S. Mangani, and B. Terni X-ray structures of binary and ternary enzyme-product-inhibitor complexes of matrix metalloproteinases Angew. Chem. Int. Ed. Engl. 42 2003 2673 2676
17. R.E. Babine, and S.L. Bender Molecular recognition of protein-ligand complexes: applications to drug design Chem. Rev. 97 1997 1359 1472
18. A. Mucha, P. Cuniasse, R. Kannan, F. Beau, A. Yiotakis, and P. Basset Membrane type-1 matrix metalloprotease and stromelysin-3 cleave more efficiently synthetic substrates containing unusual amino acids in their P1′ positions J. Biol. Chem. 273 1998 2763 2768
19. S. Vassiliou, A. Mucha, P. Cuniasse, D. Georgiadis, K. Lucet-Levannier, and F. Beau Phosphinic pseudo-tripeptides as potent inhibitors of matrix metalloproteinases: a structure-activity study J. Med. Chem. 42 1999 2610 2620
20. A.L. Gall, M. Ruff, R. Kannan, P. Cuniasse, A. Yiotakis, V. Dive, M.C. Rio, P. Basset, and D. Moras Crystal structure of the stromelysin-3 (MMP-11) catalytic domain complexed with a phosphinic inhibitor mimicking the transition-state J. Mol. Biol. 307 2001 577 586
21. F.J. Moy, P.K. Chanda, J. Chen, S. Cosmi, W. Edris, J.I. Levin, T.S. Rush, J. Wilhelm, and R. Powers Impact of mobility on structure-based drug design for the MMPs J. Am. Chem. Soc. 124 2002 12658 12659
22. D.L. Steele, O. El-Kabbani, P. Dunten, L.J. Windsor, R.U. Kammlott, and R.L. Crowther Expression, characterization and structure determination of an active site mutant (Glu202-Gln) of mini-stromelysin-1 Protein Eng. 13 2000 397 405
23. A.G. Pavlovsky, M.G. Williams, Q.Z. Ye, D.F. Ortwine, C.F. Purchase 2nd, and A.D. White X-ray structure of human stromelysin catalytic domain complexed with nonpeptide inhibitors: implications for inhibitor selectivity Protein Sci. 8 1999 1455 1462
24. M.G. Natchus, R.G. Bookland, B. De, N.G. Almstead, S. Pikul, and M.J. Janusz Development of new hydroxamate matrix metalloproteinase inhibitors derived from functionalized 4-aminoprolines J. Med. Chem. 43 2000 4948 4963
25. H. Matter, W. Schwab, D. Barbier, G. Billen, B. Haase, and B. Neises Quantitative structure-activity relationship of human neutrophil collagenase (MMP-8) inhibitors using comparative molecular field analysis and X-ray structure analysis J. Med. Chem. 42 1999 1908 1920
26. T. Masuda, and Y. Nakayama Development of a water-soluble matrix metalloproteinase inhibitor as an intra-arterial infusion drug for prevention of restenosis after angioplasty J. Med. Chem. 46 2003 3497 3501
27. C.A. Hunter, and S. Tomas Cooperativity, partially bound states, and enthalpy-entropy compensation Chem. Biol. 10 2003 1023 1032
28. D.H. Williams, D.P. O'Brien, and B. Bardsley Enthalpy/entropy compensation as a competition between dynamics and bonding: the relevance to melting of crystals and biological aggregates J. Am. Chem. Soc. 123 2001 737 738
29. R. Tellez-Sanz, L. Garcia-Fuentes, and C. Baron Calorimetric analysis of lisinopril binding to angiotensin I-converting enzyme FEBS Lett. 423 1998 75 80
30. E. Ortiz-Salmeron, C. Baron, and L. Garcia-Fuentes Enthalpy of captopril-angiotensin I-converting enzyme binding FEBS Lett. 435 1998 219 224
31. F.J. Moy, P.K. Chanda, J.M. Chen, S. Cosmi, W. Edris, and J.S. Skotnicki NMR solution structure of the catalytic fragment of human fibroblast collagenase complexed with a sulfonamide derivative of a hydroxamic acid compound Biochemistry 38 1999 7085 7096
32. J.C. Spurlino, A.M. Smallwood, D.D. Carlton, T.M. Banks, K.J. Vavra, and J.S. Johnson 1.56 Å structure of mature truncated human fibroblast collagenase Proteins 19 1994 98 109
33. J. Li, P. Brick, M.C. O'Hare, T. Skarzynski, L.F. Lloyd, and V.A. Curry Structure of full-length porcine synovial collagenase reveals a C-terminal domain containing a calcium-linked, four-bladed beta-propeller Structure 3 1995 541 549
34. N. Borkakoti, F.K. Winkler, D.H. Williams, A. D'Arcy, M.J. Broadhurst, and P.A. Brown Structure of the catalytic domain of human fibroblast collagenase complexed with an inhibitor Nat. Struct. Biol. 1 1994 106 110
35. Y. Feng, J.J. Likos, L. Zhu, H. Woodward, G. Munie, J.J. McDonald, A.M. Stevens, C.P. Howard, G.A. De Crescenzo, D. Welsch, H.S. Shieh, and W.C. Stallings Solution structure and backbone dynamics of the catalytic domain of matrix metalloproteinase-2 complexed with a hydroxamic acid inhibitor Biochim. Biophys. Acta 1598 2002 10 23
36. S. Pikul, K.M. Dunham, N.G. Almstead, B. De, M.G. Natchus, Y.O. Taiwo, L.E. Williams, B.A. Hynd, L.C. Hsieh, M.J. Janusz, F. Gu, and G.E. Mieling Heterocycle-based MMP inhibitors with P2 substituents Bioorg. Med. Chem. Lett. 11 2001 1009 1013
37. P. Dunten, U. Kammlott, R. Crowther, W. Levin, L.H. Foley, P. Wang, and R. Palermo X-ray structure of a novel matrix metalloproteinase inhibitor complexed to stromelysin Protein Sci. 10 2001 923 926
38. N.G. Almstead, R.S. Bradley, S. Pikul, B. De, M.G. Natchus, and Y.O. Taiwo Design, synthesis, and biological evaluation of potent thiazine- and thiazepine-based matrix metalloproteinase inhibitors J. Med. Chem. 42 1999 4547 4562
39. L. Chen, T.J. Rydel, F. Gu, C.M. Dunaway, S. Pikul, and K.M. Dunham Crystal structure of the stromelysin catalytic domain at 2.0 Å resolution: inhibitor-induced conformational changes J. Mol. Biol. 293 1999 545 557
40. S. Pikul, K.L. McDow Dunham, N.G. Almstead, B. De, M.G. Natchus, and M.V. Anastasio Discovery of potent, achiral matrix metalloproteinase inhibitors J. Med. Chem. 41 1998 3568 3571
41. M. Cheng, B. De, N.G. Almstead, S. Pikul, M.E. Dowty, and C.R. Dietsch Design, synthesis, and biological evaluation of matrix metalloproteinase inhibitors derived from a modified proline scaffold J. Med. Chem. 42 1999 5426 5436
42. M. Cheng, B. De, S. Pikul, N.G. Almstead, M.G. Natchus, and M.V. Anastasio Design and synthesis of piperazine-based matrix metalloproteinase inhibitors J. Med. Chem. 43 2000 369 380
43. M.G. Natchus, M. Cheng, C.T. Wahl, S. Pikul, N.G. Almstead, and R.S. Bradley Design and synthesis of conformationally-constrained MMP inhibitors Bioorg. Med. Chem. Lett. 8 1998 2077 2080
44. Y.C. Li, X. Zhang, R. Melton, V. Ganu, and N.C. Gonnella Solution structure of the catalytic domain of human stromelysin-1 complexed to a potent, nonpeptidic inhibitor Biochemistry 37 1998 14048 14056
45. S.R. Van Doren, A.V. Kurochkin, W. Hu, Q.Z. Ye, L.L. Johnson, and D.J. Hupe Solution structure of the catalytic domain of human stromelysin complexed with a hydrophobic inhibitor Protein Sci. 4 1995 2487 2498
46. P.R. Gooley, J.F. O'Connell, A.I. Marcy, G.C. Cuca, S.P. Salowe, and B.L. Bush The NMR structure of the inhibited catalytic domain of human stromelysin-1 Nat. Struct. Biol. 1 1994 111 118
47. C.K. Esser, R.L. Bugianesi, C.G. Caldwell, K.T. Chapman, P.L. Durette, and N.N. Girotra Inhibition of stromelysin-1 (MMP-3) by P1′- biphenylylethyl carboxyalkyl dipeptides J. Med. Chem. 40 1997 1026 1040
48. M.G. Natchus, R.G. Bookland, M.J. Laufersweiler, S. Pikul, N.G. Almstead, B. De, M.J. Janusz, L.C. Hsieh, F. Gu, M.E. Pokross, V.S. Patel, S.M. Garver, S.X. Peng, T.M. Branch, S.L. King, T.R. Baker, D.J. Foltz, and G.E. Mieling Development of new carboxylic acid-based MMP inhibitors derived from functionalized propargylglycines J. Med. Chem. 44 2001 1060 1071
49. J.W. Becker, A.I. Marcy, L.L. Rokosz, M.G. Axel, J.J. Burbaum, and P.M. Fitzgerald Stromelysin-1: three-dimensional structure of the inhibited catalytic domain and of the C-truncated proenzyme Protein Sci. 4 1995 1966 1976
50. B.C. Finzel, E.T. Baldwin, G.L. Bryant Jr., G.F. Hess, J.W. Wilks, and C.M. Trepod Structural characterizations of nonpeptidic thiadiazole inhibitors of matrix metalloproteinases reveal the basis for stromelysin selectivity Protein Sci. 7 1998 2118 2126
51. B.J. Stockman, D.J. Waldon, J.A. Gates, T.A. Scahill, D.A. Kloosterman, and S.A. Mizsak Solution structures of stromelysin complexed to thiadiazole inhibitors Protein Sci. 7 1998 2281 2286
52. M.F. Browner, W.W. Smith, and A.L. Castelhano Matrilysin-inhibitor complexes: common themes among metalloproteases Biochemistry 34 1995 6602 6610
53. T. Stams, J.C. Spurlino, D.L. Smith, R.C. Wahl, T.F. Ho, and M.W. Qoronfleh Structure of human neutrophil collagenase reveals large S1′ specificity pocket Nat. Struct. Biol. 1 1994 119 123
54. F. Grams, P. Reinemer, J.C. Powers, T. Kleine, M. Pieper, and H. Tschesche 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 1995 830 841
55. P. Reinemer, F. Grams, R. Huber, T. Kleine, S. Schnierer, and M. Piper Structural implications for the role of the N terminus in the 'superactivation' of collagenases. A crystallographic study FEBS Lett. 338 1994 227 233
56. W. Bode, P. Reinemer, R. Huber, T. Kleine, S. Schnierer, and H. Tschesche 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 1994 1263 1269
57. M. Betz, P. Huxley, S.J. Davies, Y. Mushtaq, M. Pieper, and H. Tschesche 1.8-Å crystal structure of the catalytic domain of human neutrophil collagenase (matrix metalloproteinase-8) complexed with a peptidomimetic hydroxamate primed-side inhibitor with a distinct selectivity profile Eur. J. Biochem. 247 1997 356 363
58. H. Brandstetter, R.A. Engh, E.G. Von Roedern, L. Moroder, R. Huber, and W. Bode Structure of malonic acid-based inhibitors bound to human neutrophil collagenase. A new binding mode explains apparently anomalous data Protein Sci. 7 1998 1303 1309
59. F. Grams, M. Crimmin, L. Hinnes, P. Huxley, M. Pieper, and H. Tschesche Structure determination and analysis of human neutrophil collagenase complexed with a hydroxamate inhibitor Biochemistry 34 1995 14012 14020
60. E. Gavuzzo, G. Pochetti, F. Mazza, C. Gallina, B. Gorini, and S. D'Alessio Two crystal structures of human neutrophil collagenase, one complexed with a primed- and the other with an unprimed-side inhibitor: implications for drug design J. Med. Chem. 43 2000 3377 3385
61. J. Schroder, A. Henke, H. Wenzel, H. Brandstetter, H.G. Stammler, A. Stammler, W.D. Pfeiffer, and H. Tschesche Structure-based design and synthesis of potent matrix metalloproteinase inhibitors derived from a 6H-1,3,4-thiadiazine scaffold J. Med. Chem. 44 2001 3231 3243
62. H. Brandstetter, F. Grams, D. Glitz, A. Lang, R. Huber, W. Bode, H.W. Krell, and R.A. Engh 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 2001 17405 17412
63. H. Nar, K. Werle, M.M. Bauer, H. Dollinger, and B. Jung Crystal structure of human macrophage elastase (MMP-12) in complex with a hydroxamic acid inhibitor J. Mol. Biol. 312 2001 743 751
64. R. Lang, A. Kocourek, M. Braun, H. Tschesche, R. Huber, W. Bode, and K. Maskos Substrate specificity determinants of human macrophage elastase (MMP-12) based on the 1.1 Å crystal structure J. Mol. Biol. 312 2001 731 742
65. I. Botos, E. Meyer, S.M. Swanson, V. Lemaitre, Y. Eeckhout, and E.F. Meyer Structure of recombinant mouse collagenase-3 (MMP-13) J. Mol. Biol. 292 1999 837 844
66. X. Zhang, N.C. Gonnella, J. Koehn, N. Pathak, V. Ganu, and R. Melton Solution structure of the catalytic domain of human collagenase-3 (MMP-13) complexed to a potent non-peptidic sulfonamide inhibitor: binding comparison with stromelysin-1 and collagenase-1 J. Mol. Biol. 301 2000 513 524
67. F.J. Moy, P.K. Chanda, J.M. Chen, S. Cosmi, W. Edris, and J.I. Levin High-resolution solution structure of the catalytic fragment of human collagenase-3 (MMP-13) complexed with a hydroxamic acid inhibitor J. Mol. Biol. 302 2000 671 689
68. R. Lang, M. Braun, N.E. Sounni, A. Noel, F. Frankenne, J.M. Foidart, W. Bode, and K. Maskos Crystal structure of the catalytic domain of MMP-16/MT3-MMP: characterization of MT-MMP specific features J. Mol. Biol. 336 2004 213 225
69. W.L. DeLano The PyMOL Molecular Graphics System 2002 DeLano Scientific San Carlos, CA, USA