Intra- and interdomain flexibility in matrix metalloproteinases: Functional aspects and drug design

Current Pharmaceutical Design

Volumn 15, Issue 31, 2009, Pages 3592-3605

  Bertini, Ivano ^a   Fragai, Marco ^a   Luchinat, Claudio ^a  

^a UNIVERSITY OF FLORENCE   (Italy)

Author keywords

Matrix metalloproteinases; NMR; Protease inhibitors; Protein dynamics; Protein flexibility; SAXS; Structure based drug design

Indexed keywords

COLLAGENASE; GELATINASE; GLUTAMINE; HEMOPEXIN; MATRILYSIN; MATRIX METALLOPROTEINASE; MATRIX METALLOPROTEINASE 14; MATRIX METALLOPROTEINASE 15; MATRIX METALLOPROTEINASE 16; MATRIX METALLOPROTEINASE 19; MATRIX METALLOPROTEINASE 21; MATRIX METALLOPROTEINASE 23; MATRIX METALLOPROTEINASE 24; MATRIX METALLOPROTEINASE 26; MATRIX METALLOPROTEINASE 27; MATRIX METALLOPROTEINASE INHIBITOR; STROMELYSIN; UNCLASSIFIED DRUG; ZINC ION;

AMINO TERMINAL SEQUENCE; BINDING AFFINITY; BINDING SITE; BIOINFORMATICS; CATALYSIS; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; DRUG DESIGN; ENZYME ACTIVITY; ENZYME SPECIFICITY; ENZYME STABILITY; ENZYME STRUCTURE; ENZYME SUBSTRATE; HUMAN; HYDROPHOBICITY; MOLECULAR DYNAMICS; MOLECULAR RECOGNITION; PHYLOGENY; PRIORITY JOURNAL; PROTEIN DEGRADATION; REVIEW; SOLUBILITY; STRUCTURE ANALYSIS;

CATALYSIS; CATALYTIC DOMAIN; DRUG DESIGN; HUMANS; MATRIX METALLOPROTEINASES; PROTEASE INHIBITORS; PROTEIN CONFORMATION;

EID: 70449584752     PISSN: 13816128     EISSN: None     Source Type: Journal    
DOI: 10.2174/138161209789271852     Document Type: Review

References (137)

1. Shapiro SD. Matrix metalloproteinase degradation of extracellular matrix: biological consequences. Curr Opin Cell Biol 1998; 10: 602-608 (Pubitemid 28477018)
2. Woessner JF, Nagase H. Matrix metalloproteinases. J Biol Chem 1999; 274: 21491-21494
3. Page-McCaw A, Ewald AJ, Werb Z. Matrix metalloproteinases and the regulation of tissue remodelling. Nat Rev Mol Cell Biol 2007; 8: 221-233 (Pubitemid 46310551)
4. Overall CM. Molecular determinants of metalloproteinase substrate specificity. Mol Biotechnol 2002; 22: 51-86.
5. Visse R, Nagase H. Matrix metalloproteinases and tissue inhibitors of metalloproteinases: structure, function, and biochemistry. Circ Res 2003; 92: 827-839 (Pubitemid 36542523)
6. Aumailley M, Gayraud B. Structure and biological activity of the extracellular matrix. J Mol Med 1998; 76: 253-265 (Pubitemid 28098711)
7. Bosman FT, Stamenkovic I. Functional structure and composition of the extracellular matrix. J Pathol 2003; 200: 423-428 (Pubitemid 36818243)
8. Tanzer ML. Current concepts of extracellular matrix. J Orthop Sci 2006; 11: 326-331
9. Eble JA. The extracellular matrix in health and disease. Curr Pharm Des 2009; 15: 1275-1276
10. Sternlicht MD, Werb Z. How matrix metalloproteinases regulate cell behavior. Ann Rev Cell Dev Biol 2001; 17: 463-516. (Pubitemid 33096184)
11. Berrier AL, Yamada KM. Cell-matrix adhesion. J Cell Physiol 2007; 213: 565-573
12. Stamenkovic I. Extracellular matrix remodelling: the role of matrix metalloproteinases. J Pathol 2003; 200: 448-464 (Pubitemid 36818245)
13. Boire A, Covic L, Agarwal A, Jacques S, Sherifl S, Kuliopulos A. PAR1 is a matrix metalloprotease-1 receptor that promotes invasion and tumorigenesis of breast cancer cells. Cell 2005; 120: 303-313 (Pubitemid 40222426)
14. Nagase H, Visse R, Murphy G. Structure and function of matrix metalloproteinases and TIMPs. Cardiovasc Res 2006; 69: 562-573 (Pubitemid 43139720)
15. Parks WC, Wilson CL, Lopez-Boado YS. Matrix metalloproteinases as modulators of inflammation and innate immunity. Nat Rev Immunol 2004; 4: 617-629 (Pubitemid 39025047)
16. D'Alessio S, Fibbi G, Cinelli M, Guiducci S, Del Rosso A, Margheri F, et al. Matrix metalloproteinase 12-dependent cleavage of urokinase receptor in systemic sclerosis microvascular endothelial cells results in impaired angiogenesis. Arthritis Rheum 2004; 50: 3275-3285 (Pubitemid 39372005)
17. Fragai M, Nesi A. Substrate specificities of matrix metalloproteinase 1 in PAR-1 exodomain proteolysis. ChemBioChem 2007; 8: 1367-1369 (Pubitemid 47300327)
18. Doucet A, Overall CM. Protease proteomics: revealing protease in vivo functions using systems biology approaches. Mol Aspects Med 2008; 29: 339-358
19. Limb GA, Matter K, Murphy G, Cambrey AD, Bishop PN, Morris GE, Khaw PT. Matrix metalloproteinase-1 associates with intracellular organelles and confers resistance to lamin A/C degradation during apoptosis. Am J Pathol 2005; 166: 1555-1563 (Pubitemid 40586523)
20. Wang W, Schulze CJ, Suarez-Pinzon WL, Dyck JR, Sawicki G, Schulz R. Intracellular action of matrix metalloproteinase-2 accounts for acute myocardial ischemia and reperfusion injury. Circulation 2002; 106: 1543-1549 (Pubitemid 35050883)
21. Sawicki G, Leon H, Sawicka J, Sariahmetoglu M, Schulze CJ, Scott PG, et al. Degradation of myosin light chain in isolated rat hearts subjected to ischemia-reperfusion injury: a new intracellular target for matrix metalloproteinase-2. Circulation 2005; 112: 544-552 (Pubitemid 41060795)
22. Kwan JA, Schulze CJ, Wang W, Leon H, Sariahmetoglu M, Sung M, et al. Matrix metalloproteinase-2 (MMP-2) is present in the nucleus of cardiac myocytes and is capable of cleaving poly (ADP-ribose) polymerase (PARP) in vitro. FASEB J 2004; 18: 690-692
23. Luo D, Mari B, Stoll I, Anglard P. Alternative splicing and promoter usage generates an intracellular stromelysin 3 isoform directly translated as an active matrix metalloproteinase. J Biol Chem 2002; 277: 25527-25536 (Pubitemid 34951868)
24. Ra HJ, Parks WC. Control of matrix metalloproteinase catalytic activity. Matrix Biol 2007; 26: 587-596
25. Barmina OY, Walling HW, Fiacco GJ, Freije JM, Lopez-Otin C, Jeffrey JJ, et al. Collagenase-3 binds to a specific receptor and requires the low density lipoprotein receptor-related protein for internalization. J Biol Chem 1999; 274: 30087-30093 (Pubitemid 29483392)
26. Drouin L, Overall CM, Sodek J. Identification of matrix metalloendoproteinase inhibitor (TIMP) in human parotid and submandibular saliva: partial purification and characterization. J Periodontal Res 1988; 23: 370-377
27. Overall CM, Sodek J. Reciprocal regulation of collagenase, 72 kDa-gelatinase, and TIMP gene expression and protein synthesis in human fibroblasts induced by concanavalin A. Matrix Suppl 1992; 1: 209-211
28. Strongin AY, Marmer BL, Grant GA, Goldberg GI. Plasma membrane-dependent activation of the 72-kDa type IV collagenase is prevented by complex formation with TIMP-2. J Biol Chem 1993; 268: 14033-14039 (Pubitemid 23195520)
29. Uria JA, Ferrando AA, Velasco G, Freije JM, Lopez-Otin C. Structure and expression in breast tumors of human TIMP-3, a new member of the metalloproteinase inhibitor family. Cancer Res 1994; 54: 2091-2094 (Pubitemid 24138677)
30. Arumugam S, Hemme CL, Yoshida N, Suzuki K, Nagase H, Berjanskii M, et al. TIMP-1 contact sites and perturbations of stromelysin 1 mapped by NMR and a paramagnetic surface probe. Biochemistry 1998; 37: 9650-9657 (Pubitemid 28319609)
31. Wolf K, Wu YI, Liu Y, Geiger J, Tam E, Overall C, et al. Multi-step pericellular proteolysis controls the transition from individual to collective cancer cell invasion. Nat Cell Biol 2007; 9: 893-904. (Pubitemid 47190444)
32. Whittaker M, Floyd CD, Brown P, Gearing AJ. Design and therapeutic application of matrix metalloproteinase inhibitors. Chem Rev 1999; 99: 2735-2776 (Pubitemid 29133538)
33. Skiles JW, Gonnella NC, Jeng AY. The design, structure, and clinical update of small molecular weight matrix metalloproteinase inhibitors. Curr Med Chem 2004; 11: 2911-2977
34. Rao BG. Recent developments in the design of specific Matrix Metalloproteinase inhibitors aided by structural and computational studies. Curr Pharm Des 2005; 11: 295-322.
35. Overall CM, Kleifeld O. Towards third generation matrix metalloproteinase inhibitors for cancer therapy. Br J Cancer 2006; 94: 941-946
36. Aureli L, Gioia M, Cerbara I, Monaco S, Fasciglione GF, Marini S, et al. Structural bases for substrate and inhibitor recognition by matrix metalloproteinases. Curr Med Chem 2008; 15: 2192-2222
37. Vincenti MP, Brinckerhoff CE. Signal transduction and cell-type specific regulation of matrix metalloproteinase gene expression: can MMPs be good for you? J Cell Physiol 2007; 213: 355-364
38. Martin MD, Matrisian LM. The other side of MMPs: Protective roles in tumor progression. Cancer Metastasis Rev 2007; 26: 717-724
39. Coussens LM, Fingleton B, Matrisian LM. Matrix metalloproteinase inhibitors and cancer: trials and tribulations. Science 2002; 295: 2387-2392 (Pubitemid 34270240)
40. Lopez-Otin C, Matrisian LM. Emerging roles of proteases in tumour suppression. Nat Rev Cancer 2007; 7: 800-808 (Pubitemid 47463671)
41. Overall CM. Molecular determinants of metalloproteinase substrate specificity - matrix metalloproteinase substrate binding domains, modules, and exosites. Mol Biotechnol 2002; 22: 51-86.
42. Gioia M, Fasciglione GF, Marini S, D'Alessio S, De Sanctis G, Diekmann O, et al. Modulation of the catalytic activity of neutrophil collagenase MMP-8 on bovine collagen I. Role of the activation cleavage and of the hemopexin-like domain. J Biol Chem 2002; 277: 23123-23130 (Pubitemid 34952136)
43. Piccard H, Van den Steen PE, Opdenakker G. Hemopexin domains as multifunctional liganding modules in matrix metalloproteinases and other proteins. J Leukoc Biol 2007; 81: 870-892 (Pubitemid 46495636)
44. Ohuchi E, Imai K, Fujii Y, Sato H, Seiki M, Okada Y. Membrane type 1 matrix metalloproteinase digests interstitial collagens and other extracellular matrix macromolecules. J Biol Chem 1997; 272: 2446-2451 (Pubitemid 27058534)
45. Allan JA, Docherty AJ, Barker PJ, Huskisson NS, Reynolds JJ, Murphy G. Binding of gelatinases A and B to type-I collagen and other matrix components. Biochem J 1995; 309 (Pt 1): 299-306.
46. Gioia M, Monaco S, Fasciglione GF, Coletti A, Modesti A, Marini S, et al. Characterization of the mechanisms by which gelatinase A, neutrophil collagenase, and membrane-type metalloproteinase MMP-14 recognize collagen I and enzymatically process the two alpha-chains. J Mol Biol 2007; 368: 1101-1113 (Pubitemid 46574666)
47. Matrisian LM, Bowden GT. Stromelysin/transin and tumor progression. Semin Cancer Biol 1990; 1: 107-115
48. Mecham RP, Broekelmann TJ, Fliszar CJ, Shapiro SD, Welgus HG, Senior RM. Elastin degradation by matrix metalloproteinases. Cleavage site specificity and mechanisms of elastolysis. J Biol Chem 1997; 272: 18071-18076
49. Taddese S, Weiss AS, Neubert RH, Schmelzer CE. Mapping of macrophage elastase cleavage sites in insoluble human skin elastin. Matrix Biol 2008; 27: 420-428
50. Mithieux SM, Weiss AS. Elastin. Adv Protein Chem 2005; 70: 437-461
51. Taddese S, Weiss AS, Jahreis G, Neubert RH, Schmelzer CE. In vitro degradation of human tropoelastin by MMP-12 and the generation of matrikines from domain 24. Matrix Biol 2009; 28: 84-91.
52. Massova I, Kotra LP, Fridman R, Mobashery S. Matrix metalloproteinases: structures, evolution, and diversification. FASEB J 1998; 12: 1075-1095 (Pubitemid 28418938)
53. Overall CM, Blobel CP. In search of partners: linking extracellular proteases to substrates. Nat Rev Mol Cell Biol 2007; 8: 245-257
54. Andreini C, Banci L, Bertini I, Luchinat C, Rosato A. A bioinformatic comparison of structures and homology-models of matrix metalloproteinases. J Proteome Res 2004; 3: 21-31. (Pubitemid 38233446)
55. Das S, Mandal M, Chakraborti T, Mandal A, Chakraborti S. Structure and evolutionary aspects of matrix metalloproteinases: a brief overview. Mol Cell Biochem 2003; 253: 31-40. (Pubitemid 37321709)
56. Puente XS, Sanchez LM, Overall CM, Lopez-Otin C. Human and mouse proteases: a comparative genomic approach. Nat Rev Genet 2003; 4: 544-558 (Pubitemid 36781345)
57. Lovejoy B, Hassell AM, Luther MA, Weigl D, Jordan SR. Crystal structures of recombinant 19-kDa human fibroblast collagenase complexed to itself. Biochemistry 1994; 33: 8207-8217 (Pubitemid 24241053)
58. Cha J, Auld DS. Site-directed mutagenesis of the active site glutamate in human matrilysin: investigation of its role in catalysis. Biochemistry 1997; 36: 16019-16024 (Pubitemid 28027407)
59. Lang R, Kocourek A, Braun M, Tschesche H, Huber R, Bode W, et al. Substrate specificity determinants of human macrophage elastase (MMP-12) based on the 1.1 angstrom crystal structure. J Mol Biol 2001; 312: 731-742 (Pubitemid 33116737)
60. Bertini I, Calderone V, Fragai M, Luchinat C, Mangani S, Terni B. X-ray structures of ternary enzyme-product-inhibitor complexes of MMP. Angew Chem Int Ed 2003; 42: 2673-2676
61. Bertini I, Calderone V, Fragai M, Luchinat C, Maletta M. Snapshots of the reaction mechanism of Matrix metalloproteinases. Angew Chem Int Ed 2006; 45: 7952-7955 (Pubitemid 44912749)
62. Park HI, Ni J, Gerkema FE, Liu D, Belozerov VE, Sang QX. Identification and characterization of human endometase (Matrix metalloproteinase-26) from endometrial tumor. J Biol Chem 2000; 275: 20540-20544 (Pubitemid 30457636)
63. Van Wart HE, Birkedal-Hansen H. 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 1990; 87: 5578-5582 (Pubitemid 20260224)
64. Rosenblum G, Meroueh S, Toth M, Fisher JF, Fridman R, Mobashery S, et al. Molecular structures and dynamics of the stepwise activation mechanism of a matrix metalloproteinase zymogen: challenging the cysteine switch dogma. J Am Chem Soc 2007; 129: 13566-13574 (Pubitemid 350071785)
65. Glasheen BM, Kabra AT, Page-McCaw A. Distinct functions for the catalytic and hemopexin domains of a Drosophila matrix metalloproteinase. Proc Natl Acad Sci USA 2009; 106: 2659-2664
66. Morgunova E, Tuuttila A, Bergmann U, Isupov M, Lindqvist Y, Schneider G, et al. Structure of human pro-matrix metalloproteinase-2: activation mechanism revealed. Science 1999; 284: 1667-1670 (Pubitemid 29291376)
67. Steffensen B, Wallon UM, Overall CM. Extracellular matrix binding properties of recombinant fibronectin type II-like modules of human 72-kDa gelatinase/type IV collagenase. High affinity binding to native type I collagen but not native type IV collagen. J Biol Chem 1995; 270: 11555-11566
68. Strongin AY, Collier IE, Krasnov PA, Genrich LT, Marmer BL, Goldberg GI. Human 92 kDa type IV collagenase: functional analysis of fibronectin and carboxyl-end domains. Kidney Int 1993; 43: 158-162
69. Elkins PA, Ho YS, Smith WW, Janson CA, D'Alessio KJ, McQueney MS, et al. Structure of the C-terminally truncated human ProMMP9, a gelatin-binding matrix metalloproteinase. Acta Crystallogr D Biol Crystallogr 2002; 58: 1182-1192
70. Maskos K, Bode W. Structural basis of matrix metalloproteinases and tissue inhibitors of metalloproteinases. Mol Biotechnol 2003; 25: 241-266 (Pubitemid 37410016)
71. Pirard B. Insight into the structural determinants for selective inhibition of matrix metalloproteinases. Drug Discov Today 2007; 12: 640-646 (Pubitemid 47243704)
72. Bode W, Reinemer P, Huber R, Kleine T, Schnierer S, Tschesche H. The X-ray crystal-structure of the catalytic domain of human neutrophil collagenase inhibited by a substrate-analog reveals the essentials for catalysis and specificity. EMBO J 1994; 13: 1263-1269 (Pubitemid 24090206)
73. Li J, Brick P, Ohare MC, Skarzynski T, Lloyd LF, Curry VA, et al. Structure of full-length porcine synovial collagenase reveals a C-terminal domain-containing a calcium-linked, 4-bladed beta-propeller. Structure 1995; 3: 541-549
74. Piccard H, Van den Steen PE, Opdenakker G. Hemopexin domains as multifunctional liganding modules in matrix metalloproteinases and other proteins. J Leukoc Biol 2007; 81: 870-892 (Pubitemid 46495636)
75. Van den Steen PE, Van Aelst I, Hvidberg V, Piccard H, Fiten P, Jacobsen C, et al. The hemopexin and O-glycosylated domains tune gelatinase B/MMP-9 bioavailability via inhibition and binding to cargo receptors. J Biol Chem 2006; 281: 18626-18637 (Pubitemid 44035522)
76. Pei D, Weiss SJ. Furin-dependent intracellular activation of the human stromelysin-3 zymogen. Nature 1995; 375: 244-247
77. Lovejoy B, Welch AR, Carr S, Luong C, Broka C, Hendricks RT, et al. Crystal structures of MMP-1 and -13 reveal the structural basis for selectivity of collagenase inhibitors. Nat Struct Biol 1999; 6: 217-221 (Pubitemid 29107223)
78. Bertini, I., Fragai, M., Luchinat, C., Melikian, M., and Venturi, C. Characterization of the MMP-12-elastin adduct. 2009; In press.
79. Chung LD, Dinakarpandian D, Yoshida N, Lauer-Fields JL, Fields GB, Visse R, et al. Collagenase unwinds triple-helical collagen prior to peptide bond hydrolysis. EMBO J 2004; 23: 3020-3030 (Pubitemid 39093596)
80. Bhaskaran R, Palmier MO, Lauer-Fields JL, Fields GB, Van Doren SR. MMP-12 catalytic domain recognizes triple-helical peptide models of collagen V with exosites and high activity. J Biol Chem 2008; 283: 21779-21788
81. Stetler-Stevenson WG, Hewitt R. Matrix metalloproteinases and tumor invasion: from correlation and causuality to the clinic. Sem Cancer Biol 1996; 7: 147-154 (Pubitemid 26179261)
82. McCawley LJ, Matrisian LM. Matrix metalloproteinases: multifunctional contributors to tumor progression. Mol Med Today 2000; 6: 149-156 (Pubitemid 30171365)
83. Liotta LA, Tryggvason K, Garbisa S, Hart I, Foltz CM, Shafie S. Metastatic potential correlates with enzymatic degradation of basement membrane collagen. Nature 1980; 284: 67-68 (Pubitemid 10098769)
84. Ossowski L, Reich E. Antibodies to plasminogen activator inhibit human tumor metastasis. Cell 1983; 35: 611-619 (Pubitemid 14168365)
85. Moore WM, Spilburg CA. Peptide hydroxamic acids inhibit skin collagenase. Biochem Biophys Res Commun 1986; 136: 390-395
86. Brown PD. Ongoing trials with matrix metalloproteinase inhibitors. Expert Opin Investig Drugs 2000; 9: 2167-2177 (Pubitemid 30682201)
87. Steward WP, Thomas AL. Marimastat: the clinical development of a matrix metalloproteinase inhibitor. Expert Opin Investig Drugs 2000; 9: 2913-2922
88. Pavlaki M, Zucker S. Matrix metalloproteinase inhibitors (MMPIs): the beginning of phase I or the termination of phase III clinical trials. Cancer Metastasis Rev 2003; 22: 177-203. (Pubitemid 36561057)
89. Grams F, Reinemer P, Powers JC, Kleine T, Pieper M, Tschesche H, et al. 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 1995; 228: 830-841
90. Floyd CD, Lewis CN, Patel SR, Whittaker M. A method for the synthesis of hydroxamic acids on solid phase. Tetrahedron Lett 1996; 37: 8045-8048 (Pubitemid 26358225)
91. MacPherson LJ, Bayburt EK, Capparelli MP, Carroll BJ, Goldstein R, Justice MR, et al. Discovery of CGS 27023A, a non-peptidic, potent, and orally active stromelysin inhibitor that blocks cartilage degradation in rabbits. J Med Chem 1997; 40: 2525-2532 (Pubitemid 27347016)
92. Moy FJ, Chanda PK, Chen JM, Cosmi S, Edris W, Skotnicki JS, et al. NMR solution structure of the catalytic fragment of human fibroblast collagenase complexed with a sulfonamide derivative of a hydroxamic acid compound. Biochemistry 1999; 38: 7085-7096 (Pubitemid 129515010)
93. Bertini I, Calderone V, Fragai M, Luchinat C, Mangani S, Terni B. Crystal structure of the catalytic domain of human matrix metyalloproteinase 10. J Mol Biol 2004; 336: 707-716 (Pubitemid 38183023)
94. Castelhano AL, Billedeau R, Dewdney N, Donnelly S, Horne S, Kurz LJ, et al. Novel indolactam-based inhibitors of matrix metalloproteinases. Bioorg Med Chem Lett 1995; 5: 1415-1420
95. Wang XQ, Choe YC, Craik CS, Ellman JA. Design and synthesis of novel inhibitors of gelatinase B. Bioorg Med Chem Lett 2002; 12: 2201-2204 (Pubitemid 34804399)
96. Agrawal A, Romero-Perez D, Jacobsen JA, Villarreal FJ, Cohen SM. Zinc-binding groups modulate selective inhibition of MMPs. ChemMedChem 2008; 3: 812-820
97. Pikul S, Ohler NE, Ciszewski G, Laufersweiler MC, Almstead NG, De B, et al. Potent and selective carboxylic acid-based inhibitors of matrix metalloproteinases. J Med Chem 2001; 44: 2499-2502 (Pubitemid 32852138)
98. Auge F, Hornebeck W, Decarme M, Laronze JY. Improved gelatinase A selectivity by novel zinc binding groups containing galardin derivatives. Bioorg Med Chem Lett 2003; 13: 1783-1786 (Pubitemid 36561164)
99. Campbell DA, Xiao XY, Harris D, Ida S, Mortezaei R, Ngu K, et al. Malonyl alpha-mercaptoketones and alpha-mercaptoalcohols, a new class of matrix metalloproteinase inhibitors. Bioorg Med Chem Lett 1998; 8: 1157-1162 (Pubitemid 28231390)
100. Brown M, Bernardo MM, Li Z, Kotra LP, Tanaka Y, Mobashery S. Potent and selective mechanism-based inhibition of gelatinases. J Am Chem Soc 2000; 122: 6799-6800 (Pubitemid 30490016)
101. Bernardo MM, Brown S, Li ZH, Fridman R, Mobashery S. Design, synthesis, and characterization of potent, slow-binding inhibitors that are selective for gelatinases. J Biol Chem 2002; 277: 11201-11207 (Pubitemid 34952882)
102. Dunten P, Kammlott U, Crowther R, Levin W, Foley LH, Wang P, et al. X-ray structure of a novel matrix metalloproteinase inhibitor complexed to stromelysin. Protein Sci 2001; 10: 923-926 (Pubitemid 32367482)
103. Brandstetter H, Grams F, Glitz D, Lang A, Huber R, Bode W, et al. The 1.8-A crystal structure of a matrix metalloproteinase 8-barbiturate inhibitor complex reveals a previously unobserved mechanism for collagenase substrate recognition. J Biol Chem 2001; 276: 17405-17412 (Pubitemid 37411553)
104. Gall AL, Ruff M, Kannan R, Cuniasse P, Yiotakis A, Dive V, et al. Crystal structure of the Stromelysin-3 (MMP-11) catalytic domain complexed with a phosphinic inhibitor mimicking the transitionstate. J Mol 2001; 307: 577-586 (Pubitemid 33027678)
105. Gavuzzo E, Pochetti G, Mazza F, Gallina C, Gorini B, D'Alessio S, et al. 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 2000; 43: 3377-3385 (Pubitemid 30695974)
106. Devel L, Rogakos V, David A, Makaritis A, Beau F, Cuniasse P, et al. Development of selective inhibitors and substrate of matrix metalloproteinase- 12. J Biol Chem 2006; 281: 11152-11160 (Pubitemid 43855540)
107. Puerta DT, Lewis JA, Cohen SM. New beginnings for matrix metalloproteinase inhibitors: identification of high-affinity zinc-binding groups. J Am Chem Soc 2004; 126: 8388-8389
108. Mannino C, Nievo M, Machetti F, Papakyriakou A, Fragai M, Guarna A. Synthesis of byciclic molecular scaffolds (BTAa) for the development of new matrix metalloproteinases inhibitors. Bioorg Med Chem 2006; 14: 7392-7403 (Pubitemid 44488739)
109. Engel CK, Pirard B, Schimanski S, Kirsch R, Habermann J, Klingler O, et al. Structural basis for the highly selective inhibition of MMP-13. Chem Biol 2005; 12: 181-189 (Pubitemid 40281325)
110. Johnson AR, Pavlovsky AG, Ortwine DF, Prior F, Man CF, Bornemeier DA, et al. Discovery and characterization of a novel inhibitor of matrix metalloprotease-13 that reduces cartilage damage in vivo without joint fibroplasia side effects. J Biol Chem 2007; 282: 27781-27791
111. Li JJ, Nahra J, Johnson AR, Bunker A, O'Brien P, Yue WS, et al. Quinazolinones and pyrido[3,4-d]pyrimidin-4-ones as orally active and specific matrix metalloproteinase-13 inhibitors for the treatment of osteoarthritis. J Med Chem 2008; 51: 835-841
112. von Itzstein M, Wu WY, Kok GB, Pegg MS, Dyason JC, Jin B, et al. Rational design of potent sialidase-based inhibitors of influenza virus replication. Nature 1993; 363: 418-423 (Pubitemid 23179386)
113. Habeck M. FDA licences imatinib mesylate for CML. Lancet Oncol 2002; 3: 6. (Pubitemid 34121132)
114. Moy FJ, Chanda PK, Chen J, Cosmi S, Edris W, Levin JI, et al. Impact of mobility on structure-based drug design for the MMPs. J Am Chem Soc 2002; 124: 12658-12659 (Pubitemid 35215979)
115. Bhaskaran R, Palmier MO, Bagegni NA, Liang XY, Van Doren SR. Solution structure of inhibitor-free human metalloelastase (MMP-12) indicates an internal conformational adjustment. J Mol Biol 2007; 374: 1333-1344 (Pubitemid 350122548)
116. Ishima R, Torchia DA. Protein dynamics from NMR. Nat Struct Biol 2000; 7: 740-743
117. Kay LE. Protein dynamics from NMR. Nat Struct Biol 1998; 5: 513-517
118. Lindorff-Larsen K, Best RB, DePristo MA, Dobson CM, Vendruscolo M. Simultaneous determination of protein structure and dynamics. Nature 2005; 433: 128-132
119. Fischer MWF, Zeng L, Majumdar A, Zuiderweg ERP. Characterizing semilocal motions in proteins by NMR relaxation studies. Proc Natl Acad Sci USA 1998; 95: 8016-8019 (Pubitemid 28326058)
120. Mittermaier A, Kay LE. New tools provide new insights in NMR studies of protein dynamics. Science 2006; 312: 224-228
121. Fragai M, Luchinat C, Parigi G. "Four-dimensional" protein structures: examples from metalloproteins. Acc Chem Res 2006; 39: 909-917
122. Bertini I, Calderone V, Cosenza M, Fragai M, Lee Y-M, Luchinat C, et al. Conformational variability of MMPs: beyond a single 3D structure. Proc Natl Acad Sci USA 2005; 102: 5334-5339
123. Bertini I, Calderone V, Fragai M, Giachetti A, Loconte M, Luchinat C, et al. Exploring the subtleties of drug-receptor interactions: the case of matrix metalloproteinases. J Am Chem Soc 2007; 129: 2466-2475 (Pubitemid 46364051)
124. Bertini I, Calderone V, Fragai M, Jaiswal R, Luchinat C, Melikian M, et al. Evidence of reciprocal reorientaion of the catalytic and hemopexin-like domains of full-length MMP-12. J Am Chem Soc 2008; 130: 7011-7021 (Pubitemid 351770143)
125. Bertini I, Fragai M, Luchinat C, Melikian M, Mylonas E, Sarti N, et al. Interdomain flexibility in full-lenght matrix metalloproteinase-1 (MMP-1). J Biol Chem 2009; 284: 12821-12828
126. Rosenblum G, Van den Steen PE, Cohen SR, Grossmann JG, Frenkel J, Sertchook R, et al. Insights into the structure and domain flexibility of full-length pro-matrix metalloproteinase-9/gelatinase B. Structure 2007; 15: 1227-1236 (Pubitemid 47539163)
127. Overall CM, Butler GS. Protease yoga: Extreme matrix metalloproteinase. Structure 2007; 15: 1159-1161
128. Diaz N, Suarez D, Valdes H. From the X-ray compact structure to the elongated form of the full-length MMP-2 enzyme in solution: a molecular dynamics study. J Am Chem Soc 2008; 130: 14070-14071
129. Saffarian S, Collier IE, Marmer BL, Elson EL, Goldberg G. Interstitial collagenase is a Brownian ratchet driven by proteolysis of collagen. Science 2004; 306: 108-111 (Pubitemid 39451949)
130. Iyer S, Visse R, Nagase H, Acharya KR. Crystal structure of an active form of human MMP-1. J Mol Biol 2006; 362: 78-88. (Pubitemid 44262357)
131. Jozic D, Bourenkov G, Lim NH, Visse R, Nagase H, Bode W, et al. X-ray structure of human proMMP-1 - New insights into procollagenase activation and collagen binding. J Biol Chem 2005; 280: 9578-9585 (Pubitemid 40409653)
132. Lauer-Fields JL, Minond D, Chase PS, Baillargeon PE, Saldanha SA, Stawikowska R, et al. High throughput screening of potentially selective MMP-13 exosite inhibitors utilizing a triple-helical FRET substrate. Bioorg Med Chem 2009; 17: 990-1005.
133. Lauer-Fields J, Brew K, Whitehead JK, Li S, Hammer RP, Fields GB. Triple-helical transition state analogues: a new class of selective matrix metalloproteinase inhibitors. J Am Chem Soc 2007; 129: 10408-10417 (Pubitemid 47330258)
134. Lauer-Fields JL, Whitehead JK, Li S, Hammer RP, Brew K, Fields GB. Selective modulation of matrix metalloproteinase 9 (MMP-9) functions via exosite inhibition. J Biol Chem 2008; 283: 20087-20095
135. Jiang Z. Computational analysis of the interaction between ligand-receptor pairs. Curr Pharm Des 2008; 14(6): 588-592
136. Porcellini E, Davis EJ, Chiappelli M, Ianni E, Di Stefano G, Forti P, Ravaglia G, Licastro F. Elevated plasma levels of alpha-1-antichymotrypsin in age-related cognitive decline and Alzheimer's disease: a potential therapeutic target. Curr Pharm Des 2008; 14(26): 2659-2664
137. Suhr F, Brixius K, Bloch W. Angiogenic and vascular modulation by extracellular matrix cleavage products. Curr Pharm Des 2009; 15(4): 389-410.