Regulation of matrix metalloproteinase activity in health and disease

FEBS Journal

Volumn 278, Issue 1, 2011, Pages 28-45

  Hadler Olsen, Elin ^a   Fadnes, Bodil ^a   Sylte, Ingebrigt ^a   Uhlin Hansen, Lars ^a   Winberg, Jan Olof ^a  

^a UNIVERSITY OF TROMSØ   (Norway)

Author keywords

activation; compartmentalization; complexes; exosite; heteromers; inhibition; matrix metalloproteinases

Indexed keywords

ALPHA AMINO 3 HYDROXY 5 METHYL 4 ISOXAZOLEPROPIONIC ACID; BONE SIALOPROTEIN; CALCIUM ION; CHYMASE; COLLAGEN; COLLAGENASE 3; ELASTIN; GELATIN; GELATINASE A; GELATINASE B; GLUTATHIONE; GLYCOPROTEIN; HAPTOGLOBIN; HEPARIN; HETERODIMER; MATRILYSIN; MATRIX METALLOPROTEINASE; MATRIX METALLOPROTEINASE 26; MATRIX METALLOPROTEINASE INHIBITOR; MERCURY CHLORIDE; NEUTROPHIL GELATINASE ASSOCIATED LIPOCALIN; PEROXYNITRITE; SMALL INTEGRIN BINDING LIGAND N LINKED GLYCOPROTEIN; TISSUE INHIBITOR OF METALLOPROTEINASE 1; TISSUE INHIBITOR OF METALLOPROTEINASE 2; TRYPSIN; UNCLASSIFIED DRUG; VITRONECTIN RECEPTOR;

ALLOSTERISM; AMINO TERMINAL SEQUENCE; CARCINOGENESIS; CELL SURVIVAL; CLINICAL TRIAL; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; DRUG EFFICACY; DRUG PROTEIN BINDING; DRUG TARGETING; ENZYMATIC DEGRADATION; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INDUCTION; ENZYME INHIBITION; ENZYME REGULATION; ENZYME RELEASE; ENZYME SPECIFICITY; ENZYME SUBSTRATE COMPLEX; EXTRACELLULAR SPACE; HUMAN; MELANOMA; MOUTH CARCINOMA; NEOPLASM; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; OVARY CARCINOMA; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; REVIEW; UNSPECIFIED SIDE EFFECT;

DISEASE; ENZYME ACTIVATION; HEALTH; HUMANS; MATRIX METALLOPROTEINASES; PROTEIN PROCESSING, POST-TRANSLATIONAL;

EID: 78650437352     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2010.07920.x     Document Type: Review

References (149)

1. Bode W, Gomis-Ruth FX, &, Stockler 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.
2. Mattu TS, Royle L, Langridge J, Wormald MR, Van den Steen PE, Van Damme J, Opdenakker G, Harvey DJ, Dwek RA, &, Rudd PM, (2000) O-glycan analysis of natural human neutrophil gelatinase B using a combination of normal phase-HPLC and online tandem mass spectrometry: implications for the domain organization of the enzyme. Biochemistry 39, 15695-15704.
3. Piccard H, Van den Steen PE, &, Opdenakker G, (2007) Hemopexin domains as multifunctional liganding modules in matrix metalloproteinases and other proteins. J Leukoc Biol 81, 870-892.
4. Van Wart HE, &, 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 U S A 87, 5578-5582.
5. Nagase H, (1997) Activation mechanisms of matrix metalloproteinases. Biol Chem 378, 151-160.
6. Woessner JF Jr, &, Nagase H, (2000) Matrix Metalloproteinases and TIMPs. Oxford Univeristy Press, Oxford.
7. Butler GS, &, Overall CM, (2009) Updated biological roles for matrix metalloproteinases and new "intracellular" substrates revealed by degradomics. Biochemistry 48, 10830-10845.
8. Sela-Passwell N, Rosenblum G, Shoham T, &, Sagi I, (2010) Structural and functional bases for allosteric control of MMP activities: can it pave the path for selective inhibition? Biochim Biophys Acta 1803, 29-38.
9. Overall CM, (2002) Molecular determinants of metalloproteinase substrate specificity: matrix metalloproteinase substrate binding domains, modules, and exosites. Mol Biotechnol 22, 51-86.
10. Overall CM, McQuibban GA, &, Clark-Lewis I, (2002) Discovery of chemokine substrates for matrix metalloproteinases by exosite scanning: a new tool for degradomics. Biol Chem 383, 1059-1066.
11. Wang W, Schulze CJ, Suarez-Pinzon WL, Dyck JR, Sawicki G, &, Schulz R, (2002) Intracellular action of matrix metalloproteinase-2 accounts for acute myocardial ischemia and reperfusion injury. Circulation 106, 1543-1549.
12. Starckx S, Van den Steen PE, Verbeek R, Van Noort JM, &, Opdenakker G, (2003) A novel rationale for inhibition of gelatinase B in multiple sclerosis: MMP-9 destroys alpha B-crystallin and generates a promiscuous T cell epitope. J Neuroimmunol 141, 47-57.
13. Descamps FJ, Martens E, Proost P, Starckx S, Van den Steen PE, Van Damme J, &, Opdenakker G, (2005) Gelatinase B/matrix metalloproteinase-9 provokes cataract by cleaving lens betaB 1 crystallin. FASEB J 19, 29-35.
14. Murphy G, &, Nagase H, (2010) Localising MMP activities in the pericellular environment. FEBS J 278, 2-15.
15. Gialeli C, Theocharis AD, &, Karamanos NK, (2010) Metalloproteinases in health and disease: roles of matrix metalloproteinases in cancer progression and their pharmacological targeting. FEBS J 278, 16-27.
16. Tchougounova E, Lundequist A, Fajardo I, Winberg JO, Abrink M, &, Pejler G, (2005) A key role for mast cell chymase in the activation of pro-matrix metalloprotease-9 and pro-matrix metalloprotease-2. J Biol Chem 280, 9291-9296.
17. Descamps FJ, Martens E, Ballaux F, Geboes K, &, Opdenakker G, (2004) In vivo activation of gelatinase B/MMP-9 by trypsin in acute pancreatitis is a permissive factor in streptozotocin-induced diabetes. J Pathol 204, 555-561.
18. Paju A, Sorsa T, Tervahartiala T, Koivunen E, Haglund C, Leminen A, Wahlstrom T, Salo T, &, Stenman UH, (2001) The levels of trypsinogen isoenzymes in ovarian tumour cyst fluids are associated with promatrix metalloproteinase-9 but not promatrix metalloproteinase-2 activation. Br J Cancer 84, 1363-1371.
19. Okada Y, Morodomi T, Enghild JJ, Suzuki K, Yasui A, Nakanishi I, Salvesen G, &, Nagase H, (1990) Matrix metalloproteinase 2 from human rheumatoid synovial fibroblasts. Purification and activation of the precursor and enzymic properties. Eur J Biochem 194, 721-730.
20. Das S, Mandal M, Mandal A, Chakraborti T, &, Chakraborti S, (2004) Identification, purification and characterization of matrix metalloproteinase-2 in bovine pulmonary artery smooth muscle plasma membrane. Mol Cell Biochem 258, 73-89.
21. Lefebvre V, Peeters-Joris C, &, Vaes G, (1991) Production of gelatin-degrading matrix metalloproteinases ('type IV collagenases') and inhibitors by articular chondrocytes during their dedifferentiation by serial subcultures and under stimulation by interleukin-1 and tumor necrosis factor alpha. Biochim Biophys Acta 1094, 8-18.
22. Lindstad RI, Sylte I, Mikalsen SO, Seglen PO, Berg E, &, Winberg JO, (2005) Pancreatic trypsin activates human promatrix metalloproteinase-2. J Mol Biol 350, 682-698.
23. Sorsa T, Salo T, Koivunen E, Tyynela J, Konttinen YT, Bergmann U, Tuuttila A, Niemi E, Teronen O, Heikkila P, et al. (1997) Activation of type IV procollagenases by human tumor-associated trypsin-2. J Biol Chem 272, 21067-21074.
24. Bannikov GA, Karelina TV, Collier IE, Marmer BL, &, Goldberg GI, (2002) Substrate binding of gelatinase B induces its enzymatic activity in the presence of intact propeptide. J Biol Chem 277, 16022-16027.
25. Freise C, Erben U, Muche M, Farndale R, Zeitz M, Somasundaram R, &, Ruehl M, (2009) The alpha 2 chain of collagen type VI sequesters latent proforms of matrix-metalloproteinases and modulates their activation and activity. Matrix Biol 28, 480-489.
26. Fedarko NS, Jain A, Karadag A, &, Fisher LW, (2004) Three small integrin binding ligand N-linked glycoproteins (SIBLINGs) bind and activate specific matrix metalloproteinases. FASEB J 18, 734-736.
27. Ogbureke KU, &, Fisher LW, (2004) Expression of SIBLINGs and their partner MMPs in salivary glands. J Dent Res 83, 664-670.
28. Jain A, Karadag A, Fisher LW, &, Fedarko NS, (2008) Structural requirements for bone sialoprotein binding and modulation of matrix metalloproteinase-2. Biochemistry 47, 10162-10170.
29. Jain A, Fisher LW, &, Fedarko NS, (2008) Bone sialoprotein binding to matrix metalloproteinase-2 alters enzyme inhibition kinetics. Biochemistry 47, 5986-5995.
30. Hwang Q, Cheifetz S, Overall CM, McCulloch CA, &, Sodek J, (2009) Bone sialoprotein does not interact with pro-gelatinase A (MMP-2) or mediate MMP-2 activation. BMC Cancer 9, 121.
31. Kjeldsen L, Johnsen AH, Sengelov H, &, Borregaard N, (1993) Isolation and primary structure of NGAL, a novel protein associated with human neutrophil gelatinase. J Biol Chem 268, 10425-10432.
32. Triebel S, Blaser J, Reinke H, &, Tschesche H, (1992) A 25 kDa alpha 2-microglobulin-related protein is a component of the 125 kDa form of human gelatinase. FEBS Lett 314, 386-388.
33. Tschesche H, Zolzer V, Triebel S, &, Bartsch S, (2001) The human neutrophil lipocalin supports the allosteric activation of matrix metalloproteinases. Eur J Biochem 268, 1918-1928.
34. Okamoto T, Akaike T, Sawa T, Miyamoto Y, Van DerVliet A, &, Maeda H, (2001) Activation of matrix metalloproteinases by peroxynitrite-induced protein S-glutathiolation via disulfide S-oxide formation. J Biol Chem 276, 29596-29602.
35. Viappiani S, Nicolescu AC, Holt A, Sawicki G, Crawford BD, Leon H, Van Mulligen T, &, Schulz R, (2009) Activation and modulation of 72kDa matrix metalloproteinase-2 by peroxynitrite and glutathione. Biochem Pharmacol 77, 826-834.
36. Migita K, Maeda Y, Abiru S, Komori A, Yokoyama T, Takii Y, Nakamura M, Yatsuhashi H, Eguchi K, &, Ishibashi H, (2005) Peroxynitrite-mediated matrix metalloproteinase-2 activation in human hepatic stellate cells. FEBS Lett 579, 3119-3125.
37. Rajagopalan S, Meng XP, Ramasamy S, Harrison DG, &, Galis ZS, (1996) Reactive oxygen species produced by macrophage-derived foam cells regulate the activity of vascular matrix metalloproteinases in vitro. Implications for atherosclerotic plaque stability. J Clin Invest 98, 2572-2579.
38. Frears ER, Zhang Z, Blake DR, O'Connell JP, &, Winyard PG, (1996) Inactivation of tissue inhibitor of metalloproteinase-1 by peroxynitrite. FEBS Lett 381, 21-24.
39. McCarthy SM, Bove PF, Matthews DE, Akaike T, &, Van DerVliet A, (2008) Nitric oxide regulation of MMP-9 activation and its relationship to modifications of the cysteine switch. Biochemistry 47, 5832-5840.
40. Itoh Y, &, Seiki M, (2006) MT1-MMP: a potent modifier of pericellular microenvironment. J Cell Physiol 206, 1-8.
41. Visse R, &, Nagase H, (2003) Matrix metalloproteinases and tissue inhibitors of metalloproteinases: structure, function, and biochemistry. Circ Res 92, 827-839.
42. Bigg HF, Morrison CJ, Butler GS, Bogoyevitch MA, Wang Z, Soloway PD, &, Overall CM, (2001) Tissue inhibitor of metalloproteinases-4 inhibits but does not support the activation of gelatinase A via efficient inhibition of membrane type 1-matrix metalloproteinase. Cancer Res 61, 3610-3618.
43. English JL, Kassiri Z, Koskivirta I, Atkinson SJ, Di Grappa M, Soloway PD, Nagase H, Vuorio E, Murphy G, &, Khokha R, (2006) Individual Timp deficiencies differentially impact pro-MMP-2 activation. J Biol Chem 281, 10337-10346.
44. Lafleur MA, Tester AM, &, Thompson EW, (2003) Selective involvement of TIMP-2 in the second activational cleavage of pro-MMP-2: refinement of the pro-MMP-2 activation mechanism. FEBS Lett 553, 457-463.
45. Elenjord R, Allen JB, Johansen HT, Kildalsen H, Svineng G, Maelandsmo GM, Loennechen T, &, Winberg JO, (2009) Collagen I regulates matrix metalloproteinase-2 activation in osteosarcoma cells independent of S100A4. FEBS J 276, 5275-5286.
46. Iida J, Wilhelmson KL, Ng J, Lee P, Morrison C, Tam E, Overall CM, &, McCarthy JB, (2007) Cell surface chondroitin sulfate glycosaminoglycan in melanoma: role in the activation of pro-MMP-2 (pro-gelatinase A). Biochem J 403, 553-563.
47. Morrison CJ, Butler GS, Bigg HF, Roberts CR, Soloway PD, &, Overall CM, (2001) Cellular activation of MMP-2 (gelatinase A) by MT2-MMP occurs via a TIMP-2-independent pathway. J Biol Chem 276, 47402-47410.
48. Miyamori H, Takino T, Kobayashi Y, Tokai H, Itoh Y, Seiki M, &, Sato H, (2001) Claudin promotes activation of pro-matrix metalloproteinase-2 mediated by membrane-type matrix metalloproteinases. J Biol Chem 276, 28204-28211.
49. Brooks PC, Silletti S, Von Schalscha TL, Friedlander M, &, Cheresh DA, (1998) Disruption of angiogenesis by PEX, a noncatalytic metalloproteinase fragment with integrin binding activity. Cell 92, 391-400.
50. Brooks PC, Stromblad S, Sanders LC, Von Schalscha TL, Aimes RT, Stetler-Stevenson WG, Quigley JP, &, Cheresh DA, (1996) Localization of matrix metalloproteinase MMP-2 to the surface of invasive cells by interaction with integrin alpha v beta 3. Cell 85, 683-693.
51. Deryugina EI, Bourdon MA, Jungwirth K, Smith JW, &, Strongin AY, (2000) Functional activation of integrin alpha V beta 3 in tumor cells expressing membrane-type 1 matrix metalloproteinase. Int J Cancer 86, 15-23.
52. Deryugina EI, Ratnikov B, Monosov E, Postnova TI, DiScipio R, Smith JW, &, Strongin AY, (2001) MT1-MMP initiates activation of pro-MMP-2 and integrin alphavbeta3 promotes maturation of MMP-2 in breast carcinoma cells. Exp Cell Res 263, 209-223.
53. Wu Y, Dai J, Schmuckler NG, Bakdash N, Yoder MC, Overall CM, &, Colman RW, (2010) Cleaved high molecular weight kininogen inhibits tube formation of endothelial progenitor cells via suppression of matrix metalloproteinase 2. J Thromb Haemost 8, 185-193.
54. Nisato RE, Hosseini G, Sirrenberg C, Butler GS, Crabbe T, Docherty AJ, Wiesner M, Murphy G, Overall CM, Goodman SL, et al. (2005) Dissecting the role of matrix metalloproteinases (MMP) and integrin alpha(v)beta3 in angiogenesis in vitro: absence of hemopexin C domain bioactivity, but membrane-Type 1-MMP and alpha(v)beta3 are critical. Cancer Res 65, 9377-9387.
55. Banyai L, Tordai H, &, Patthty L, (1996) Structure and domain-domain interactions of the gelatin binding site of human 72-kilodalton type IV collagenase (gelatinase A, matrix metalloproteinase 2). J Biol Chem 271, 12003-12008.
56. Emonard H, &, Hornebeck W, (1997) Binding of 92 kDa and 72 kDa progelatinases to insoluble elastin modulates their proteolytic activation. Biol Chem 378, 265-271.
57. Crabbe T, Ioannou C, &, Docherty AJ, (1993) Human progelatinase A can be activated by autolysis at a rate that is concentration-dependent and enhanced by heparin bound to the C-terminal domain. Eur J Biochem 218, 431-438.
58. Shiomi T, Inoki I, Kataoka F, Ohtsuka T, Hashimoto G, Nemori R, &, Okada Y, (2005) Pericellular activation of proMMP-7 (promatrilysin-1) through interaction with CD151. Lab Invest 85, 1489-1506.
59. Goldberg GI, Strongin A, Collier IE, Genrich LT, &, Marmer BL, (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.
60. Hibbs MS, Hasty KA, Seyer JM, Kang AH, &, Mainardi CL, (1985) Biochemical and immunological characterization of the secreted forms of human neutrophil gelatinase. J Biol Chem 260, 2493-2500.
61. Olson MW, Bernardo MM, Pietila M, Gervasi DC, Toth M, Kotra LP, Massova I, Mobashery S, &, Fridman R, (2000) Characterization of the Monomeric and Dimeric Forms of Latent and Active Matrix Metalloproteinase-9. Differential rates for activation by stromelysin 1. J Biol Chem 275, 2661-2668.
62. Triebel S, Blaser J, Reinke H, Knauper V, &, Tschesche H, (1992) Mercurial activation of human PMN leucocyte type IV procollagenase (gelatinase). FEBS Lett 298, 280-284.
63. Winberg JO, Kolset SO, Berg E, &, Uhlin-Hansen L, (2000) Macrophages secrete matrix metalloproteinase 9 covalently linked to the core protein of chondroitin sulphate proteoglycans. J Mol Biol 304, 669-680.
64. Winberg JO, Berg E, Kolset SO, &, Uhlin-Hansen L, (2003) Calcium-induced activation and truncation of promatrix metalloproteinase-9 linked to the core protein of chondroitin sulfate proteoglycans. Eur J Biochem 270, 3996-4007.
65. Bu CH, &, Pourmotabbed T, (1995) Mechanism of activation of human neutrophil gelatinase B. Discriminating between the role of Ca2+ in activation and catalysis. J Biol Chem 270, 18563-18569.
66. Bu CH, &, Pourmotabbed T, (1996) Mechanism of Ca2+-dependent activity of human neutrophil gelatinase B. J Biol Chem 271, 14308-14315.
67. Okada Y, Gonoji Y, Naka K, Tomita K, Nakanishi I, Iwata K, Yamashita K, &, Hayakawa T, (1992) Matrix metalloproteinase 9 (92-kDa gelatinase/type IV collagenase) from HT 1080 human fibrosarcoma cells. Purification and activation of the precursor and enzymic properties. J Biol Chem 267, 21712-21719.
68. Geurts N, Martens E, Van Aelst I, Proost P, Opdenakker G, &, Van Den Steen PE, (2008) Beta-hematin interaction with the hemopexin domain of gelatinase B/MMP-9 provokes autocatalytic processing of the propeptide, thereby priming activation by MMP-3. Biochemistry 47, 2689-2699.
69. Van denSteen PE, Dubois B, Nelissen I, Rudd PM, Dwek RA, &, Opdenakker G, (2002) Biochemistry and molecular biology of gelatinase B or matrix metalloproteinase-9 (MMP-9). Crit Rev Biochem Mol Biol 37, 375-536.
70. Strongin AY, Collier IE, Krasnov PA, Genrich LT, Marmer BL, &, Goldberg GI, (1993) Human 92 kDa type IV collagenase: functional analysis of fibronectin and carboxyl-end domains. Kidney Int 43, 158-162.
71. 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.
72. Kolkenbrock H, Hecker-Kia A, Orgel D, Kinawi A, &, Ulbrich N, (1996) Progelatinase B forms from human neutrophils. complex formation of monomer/lipocalin with TIMP-1. Biol Chem 377, 529-533.
73. Yan L, Borregaard N, Kjeldsen L, &, Moses MA, (2001) The high molecular weight urinary matrix metalloproteinase (MMP) activity is a complex of gelatinase B/MMP-9 and neutrophil gelatinase-associated lipocalin (NGAL). Modulation of MMP-9 activity by NGAL. J Biol Chem 276, 37258-37265.
74. Ray S, Lukyanov P, &, Ochieng J, (2003) Members of the cystatin superfamily interact with MMP-9 and protect it from autolytic degradation without affecting its gelatinolytic activities. Biochim Biophys Acta 1652, 91-102.
75. Allan JA, Docherty AJ, Barker PJ, Huskisson NS, Reynolds JJ, &, Murphy G, (1995) Binding of gelatinases A and B to type-I collagen and other matrix components. Biochem J 309, 299-306.
76. Collier IE, Krasnov PA, Strongin AY, Birkedal-Hansen H, &, Goldberg GI, (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.
77. Hornebeck W, Bellon G, &, Emonard H, (2005) Fibronectin type II (FnII)-like modules regulate gelatinase A activity. Pathol Biol (Paris) 53, 405-410.
78. Murphy G, Nguyen Q, Cockett MI, Atkinson SJ, Allan JA, Knight CG, Willenbrock F, &, Docherty AJ, (1994) Assessment of the role of the fibronectin-like domain of gelatinase A by analysis of a deletion mutant. J Biol Chem 269, 6632-6636.
79. O'Farrell TJ, &, Pourmotabbed T, (1998) The fibronectin-like domain is required for the type V and XI collagenolytic activity of gelatinase B. Arch Biochem Biophys 354, 24-30.
80. Pourmotabbed T, (1994) Relation between substrate specificity and domain structure of 92-kDa type IV collagenase. Ann N Y Acad Sci 732, 372-374.
81. Shipley JM, Doyle GA, Fliszar CJ, Ye QZ, Johnson LL, Shapiro SD, Welgus HG, &, Senior RM, (1996) The structural basis for the elastolytic activity of the 92-kDa and 72- kDa gelatinases. Role of the fibronectin type II-like repeats. J Biol Chem 271, 4335-4341.
82. Steffensen B, Wallon UM, &, Overall CM, (1995) 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 270, 11555-11566.
83. Xu X, Chen Z, Wang Y, Yamada Y, &, Steffensen B, (2005) Functional basis for the overlap in ligand interactions and substrate specificities of matrix metalloproteinases-9 and -2. Biochem J 392, 127-134.
84. Xu X, Wang Y, Lauer-Fields JL, Fields GB, &, Steffensen B, (2004) Contributions of the MMP-2 collagen binding domain to gelatin cleavage. Substrate binding via the collagen binding domain is required for hydrolysis of gelatin but not short peptides. Matrix Biol 23, 171-181.
85. Malla N, Berg E, Uhlin-Hansen L, &, Winberg JO, (2008) Interaction of pro-matrix metalloproteinase-9/proteoglycan heteromer with gelatin and collagen. J Biol Chem 283, 13652-13665.
86. Rosenblum G, Van denSteen PE, Cohen SR, Grossmann JG, Frenkel J, Sertchook R, Slack N, Strange RW, Opdenakker G, &, Sagi I, (2007) Insights into the structure and domain flexibility of full-length pro-matrix metalloproteinase-9/gelatinase B. Structure 15, 1227-1236.
87. Polticelli F, Bocedi A, Minervini G, &, Ascenzi P, (2008) Human haptoglobin structure and function-a molecular modelling study. FEBS J 275, 5648-5656.
88. Bannikov GA, Mattoon JS, Abrahamsen EJ, Premanandan C, Green-Church KB, Marsh AE, &, Lakritz J, (2007) Biochemical and enzymatic characterization of purified covalent complexes of matrix metalloproteinase-9 and haptoglobin released by bovine granulocytes in vitro. Am J Vet Res 68, 995-1004.
89. Williams RJ, (2003) Restriction endonucleases: classification, properties, and applications. Mol Biotechnol 23, 225-243.
90. Clark IM, &, Cawston TE, (1989) Fragments of human fibroblast collagenase. Purification and characterization. Biochem J 263, 201-206.
91. Hurst DR, Schwartz MA, Ghaffari MA, Jin Y, Tschesche H, Fields GB, &, Sang QX, (2004) Catalytic- and ecto-domains of membrane type 1-matrix metalloproteinase have similar inhibition profiles but distinct endopeptidase activities. Biochem J 377, 775-779.
92. Knauper V, Cowell S, Smith B, Lopez-Otin C, O'Shea M, Morris H, Zardi L, &, Murphy G, (1997) The role of the C-terminal domain of human collagenase-3 (MMP-13) in the activation of procollagenase-3, substrate specificity, and tissue inhibitor of metalloproteinase interaction. J Biol Chem 272, 7608-7616.
93. Knauper V, Osthues A, DeClerck YA, Langley KE, Blaser J, &, Tschesche H, (1993) Fragmentation of human polymorphonuclear-leucocyte collagenase. Biochem J 291 (Pt 3), 847-854.
94. Murphy G, Allan JA, Willenbrock F, Cockett MI, O'Connell JP, &, Docherty AJ, (1992) The role of the C-terminal domain in collagenase and stromelysin specificity. J Biol Chem 267, 9612-9618.
95. Patterson ML, Atkinson SJ, Knauper V, &, Murphy G, (2001) Specific collagenolysis by gelatinase A, MMP-2, is determined by the hemopexin domain and not the fibronectin-like domain. FEBS Lett 503, 158-162.
96. Chung L, Dinakarpandian D, Yoshida N, Lauer-Fields JL, Fields GB, Visse R, &, Nagase H, (2004) Collagenase unwinds triple-helical collagen prior to peptide bond hydrolysis. EMBO J 23, 3020-3030.
97. Overall CM, &, Kleifeld O, (2006) Towards third generation matrix metalloproteinase inhibitors for cancer therapy. Br J Cancer 94, 941-946.
98. Overall CM, &, Kleifeld O, (2006) Tumour microenvironment-opinion: validating matrix metalloproteinases as drug targets and anti-targets for cancer therapy. Nat Rev Cancer 6, 227-239.
99. Hu J, Van denSteen PE, Sang QX, &, Opdenakker G, (2007) Matrix metalloproteinase inhibitors as therapy for inflammatory and vascular diseases. Nat Rev Drug Discov 6, 480-498.
100. Minond D, Lauer-Fields JL, Cudic M, Overall CM, Pei D, Brew K, Visse R, Nagase H, &, Fields GB, (2006) The roles of substrate thermal stability and P2 and P1â' subsite identity on matrix metalloproteinase triple-helical peptidase activity and collagen specificity. J Biol Chem 281, 38302-38313.
101. Lauer-Fields JL, Minond D, Chase PS, Baillargeon PE, Saldanha SA, Stawikowska R, Hodder P, &, Fields GB, (2009) High throughput screening of potentially selective MMP-13 exosite inhibitors utilizing a triple-helical FRET substrate. Bioorg Med Chem 17, 990-1005.
102. Lauer-Fields J, Brew K, Whitehead JK, Li S, Hammer RP, &, Fields GB, (2007) Triple-helical transition state analogues: a new class of selective matrix metalloproteinase inhibitors. J Am Chem Soc 129, 10408-10417.
103. Lauer-Fields JL, Whitehead JK, Li S, Hammer RP, Brew K, &, Fields GB, (2008) Selective modulation of matrix metalloproteinase 9 (MMP-9) functions via exosite inhibition. J Biol Chem 283, 20087-20095.
104. Knauper V, Patterson ML, Gomis-Ruth FX, Smith B, Lyons A, Docherty AJ, &, Murphy G, (2001) The role of exon 5 in fibroblast collagenase (MMP-1) substrate specificity and inhibitor selectivity. Eur J Biochem 268, 1888-1896.
105. Chung L, Shimokawa K, Dinakarpandian D, Grams F, Fields GB, &, 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.
106. Brandstetter H, Grams F, Glitz D, Lang A, Huber R, Bode W, Krell HW, &, Engh RA, (2001) 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 276, 17405-17412.
107. Engel CK, Pirard B, Schimanski S, Kirsch R, Habermann J, Klingler O, Schlotte V, Weithmann KU, &, Wendt KU, (2005) Structural basis for the highly selective inhibition of MMP-13. Chem Biol 12, 181-189.
108. Gooljarsingh LT, Lakdawala A, Coppo F, Luo L, Fields GB, Tummino PJ, &, Gontarek RR, (2008) Characterization of an exosite binding inhibitor of matrix metalloproteinase 13. Protein Sci 17, 66-71.
109. Heim-Riether A, Taylor SJ, Liang S, Gao DA, Xiong Z, Michael August E, Collins BK, Farmer BT II, Haverty K, Hill-Drzewi M, et al. (2009) Improving potency and selectivity of a new class of non-Zn-chelating MMP-13 inhibitors. Bioorg Med Chem Lett 19, 5321-5324.
110. Butler GS, Butler MJ, Atkinson SJ, Will H, Tamura T, Van Westrum SS, Crabbe T, Clements J, D'Ortho MP, &, Murphy G, (1998) The TIMP2 membrane type 1 metalloproteinase "receptor" regulates the concentration and efficient activation of progelatinase A. A kinetic study. J Biol Chem 273, 871-880.
111. Cha J, Pedersen MV, &, Auld DS, (1996) Metal and pH dependence of heptapeptide catalysis by human matrilysin. Biochemistry 35, 15831-15838.
112. Crabbe T, O'Connell JP, Smith BJ, &, Docherty AJ, (1994) Reciprocated matrix metalloproteinase activation: a process performed by interstitial collagenase and progelatinase A. Biochemistry 33, 14419-14425.
113. Gadher SJ, Eyre DR, Wotton SF, Schmid TM, &, Woolley DE, (1990) Degradation of cartilage collagens type II, IX, X and XI by enzymes derived from human articular chondrocytes. Matrix 10, 154-163.
114. Kao WW, Ebert J, Kao CW, Covington H, &, Cintron C, (1986) Development of monoclonal antibodies recognizing collagenase from rabbit PMN; the presence of this enzyme in ulcerating corneas. Curr Eye Res 5, 801-815.
115. Sakamoto S, Sakamoto M, Goldhaber P, &, Glimcher MJ, (1975) Studies on the interaction between heparin and mouse bone collagenase. Biochim Biophys Acta 385, 41-50.
116. Wallon UM, &, Overall CM, (1997) The hemopexin-like domain (C domain) of human gelatinase A (matrix metalloproteinase-2) requires Ca2+ for fibronectin and heparin binding. Binding properties of recombinant gelatinase A C domain to extracellular matrix and basement membrane components. J Biol Chem 272, 7473-7481.
117. Yu WH, &, Woessner JF Jr, (2000) Heparan sulfate proteoglycans as extracellular docking molecules for matrilysin (matrix metalloproteinase 7). J Biol Chem 275, 4183-4191.
118. Hadler-Olsen E, Kanapathippillai P, Berg E, Svineng G, Winberg JO, &, Uhlin-Hansen L, (2010) Gelatin in situ zymography on fixed, paraffin-embedded tissue: zinc and ethanol fixation preserve enzyme activity. J Histochem Cytochem 58, 29-39.
119. D'Alessio S, Ferrari G, Cinnante K, Scheerer W, Galloway AC, Roses DF, Rozanov DV, Remacle AG, Oh ES, Shiryaev SA, et al. (2008) Tissue inhibitor of metalloproteinases-2 binding to membrane-type 1 matrix metalloproteinase induces MAPK activation and cell growth by a non-proteolytic mechanism. J Biol Chem 283, 87-99.
120. Koyama Y, Naruo H, Yoshitomi Y, Munesue S, Kiyono S, Kusano Y, Hashimoto K, Yokoi T, Nakanishi H, Shimizu S, et al. (2008) Matrix metalloproteinase-9 associated with heparan sulphate chains of GPI-anchored cell surface proteoglycans mediates motility of murine colon adenocarcinoma cells. J Biochem 143, 581-592.
121. Lambert E, Bridoux L, Devy J, Dasse E, Sowa ML, Duca L, Hornebeck W, Martiny L, &, Petitfrere-Charpentier E, (2009) TIMP-1 binding to proMMP-9/CD44 complex localized at the cell surface promotes erythroid cell survival. Int J Biochem Cell Biol 41, 1102-1115.
122. Mantuano E, Inoue G, Li X, Takahashi K, Gaultier A, Gonias SL, &, Campana WM, (2008) The hemopexin domain of matrix metalloproteinase-9 activates cell signaling and promotes migration of schwann cells by binding to low-density lipoprotein receptor-related protein. J Neurosci 28, 11571-11582.
123. Radjabi AR, Sawada K, Jagadeeswaran S, Eichbichler A, Kenny HA, Montag A, Bruno K, &, Lengyel E, (2008) Thrombin induces tumor invasion through the induction and association of matrix metalloproteinase-9 and beta1-integrin on the cell surface. J Biol Chem 283, 2822-2834.
124. Kwan JA, Schulze CJ, Wang W, Leon H, Sariahmetoglu M, Sung M, Sawicka J, Sims DE, Sawicki G, &, Schulz R, (2004) 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 18, 690-692.
125. Si-Tayeb K, Monvoisin A, Mazzocco C, Lepreux S, Decossas M, Cubel G, Taras D, Blanc JF, Robinson DR, &, Rosenbaum J, (2006) Matrix metalloproteinase 3 is present in the cell nucleus and is involved in apoptosis. Am J Pathol 169, 1390-1401.
126. Ip YC, Cheung ST, &, Fan ST, (2007) Atypical localization of membrane type 1-matrix metalloproteinase in the nucleus is associated with aggressive features of hepatocellular carcinoma. Mol Carcinog 46, 225-230.
127. Aldonyte R, Brantly M, Block E, Patel J, &, Zhang J, (2009) Nuclear localization of active matrix metalloproteinase-2 in cigarette smoke-exposed apoptotic endothelial cells. Exp Lung Res 35, 59-75.
128. Yang Y, Candelario-Jalil E, Thompson JF, Cuadrado E, Estrada EY, Rosell A, Montaner J, &, Rosenberg GA, (2010) Increased intranuclear matrix metalloproteinase activity in neurons interferes with oxidative DNA repair in focal cerebral ischemia. J Neurochem 112, 134-149.
129. Cuadrado E, Rosell A, Borrell-Pages M, Garcia-Bonilla L, Hernandez-Guillamon M, Ortega-Aznar A, &, Montaner J, (2009) Matrix metalloproteinase-13 is activated and is found in the nucleus of neural cells after cerebral ischemia. J Cereb Blood Flow Metab 29, 398-410.
130. Eguchi T, Kubota S, Kawata K, Mukudai Y, Uehara J, Ohgawara T, Ibaragi S, Sasaki A, Kuboki T, &, Takigawa M, (2008) Novel transcription-factor-like function of human matrix metalloproteinase 3 regulating the CTGF/CCN2 gene. Mol Cell Biol 28, 2391-2413.
131. Choi DH, Kim EM, Son HJ, Joh TH, Kim YS, Kim D, Flint Beal M, &, Hwang O, (2008) A novel intracellular role of matrix metalloproteinase-3 during apoptosis of dopaminergic cells. J Neurochem 106, 405-415.
132. Limb GA, Matter K, Murphy G, Cambrey AD, Bishop PN, Morris GE, &, Khaw PT, (2005) Matrix metalloproteinase-1 associates with intracellular organelles and confers resistance to lamin A/C degradation during apoptosis. Am J Pathol 166, 1555-1563.
133. Boire A, Covic L, Agarwal A, Jacques S, Sherifi S, &, Kuliopulos A, (2005) PAR1 is a matrix metalloprotease-1 receptor that promotes invasion and tumorigenesis of breast cancer cells. Cell 120, 303-313.
134. Yang E, Boire A, Agarwal A, Nguyen N, O'Callaghan K, Tu P, Kuliopulos A, &, Covic L, (2009) Blockade of PAR1 signaling with cell-penetrating pepducins inhibits Akt survival pathways in breast cancer cells and suppresses tumor survival and metastasis. Cancer Res 69, 6223-6231.
135. Bolli R, &, Marban E, (1999) Molecular and cellular mechanisms of myocardial stunning. Physiol Rev 79, 609-634.
136. Sung MM, Schulz CG, Wang W, Sawicki G, Bautista-Lopez NL, &, Schulz R, (2007) Matrix metalloproteinase-2 degrades the cytoskeletal protein alpha-actinin in peroxynitrite mediated myocardial injury. J Mol Cell Cardiol 43, 429-436.
137. Sawicki G, Leon H, Sawicka J, Sariahmetoglu M, Schulze CJ, Scott PG, Szczesna-Cordary D, &, Schulz R, (2005) Degradation of myosin light chain in isolated rat hearts subjected to ischemia-reperfusion injury: a new intracellular target for matrix metalloproteinase-2. Circulation 112, 544-552.
138. Marchenko ND, Marchenko GN, Weinreb RN, Lindsey JD, Kyshtoobayeva A, Crawford HC, &, Strongin AY, (2004) Beta-catenin regulates the gene of MMP-26, a novel metalloproteinase expressed both in carcinomas and normal epithelial cells. Int J Biochem Cell Biol 36, 942-956.
139. Zhao YG, Xiao AZ, Newcomer RG, Park HI, Kang T, Chung LW, Swanson MG, Zhau HE, Kurhanewicz J, &, Sang QX, (2003) Activation of pro-gelatinase B by endometase/matrilysin-2 promotes invasion of human prostate cancer cells. J Biol Chem 278, 15056-15064.
140. Li W, Savinov AY, Rozanov DV, Golubkov VS, Hedayat H, Postnova TI, Golubkova NV, Linli Y, Krajewski S, &, Strongin AY, (2004) Matrix metalloproteinase-26 is associated with estrogen-dependent malignancies and targets alpha1-antitrypsin serpin. Cancer Res 64, 8657-8665.
141. Lee S, Park HI, &, Sang QX, (2007) Calcium regulates tertiary structure and enzymatic activity of human endometase/matrilysin-2 and its role in promoting human breast cancer cell invasion. Biochem J 403, 31-42.
142. Savinov AY, Remacle AG, Golubkov VS, Krajewska M, Kennedy S, Duffy MJ, Rozanov DV, Krajewski S, &, Strongin AY, (2006) Matrix metalloproteinase 26 proteolysis of the NH2-terminal domain of the estrogen receptor beta correlates with the survival of breast cancer patients. Cancer Res 66, 2716-2724.
143. Taraboletti G, D'Ascenzo S, Borsotti P, Giavazzi R, Pavan A, &, Dolo V, (2002) Shedding of the matrix metalloproteinases MMP-2, MMP-9, and MT1-MMP as membrane vesicle-associated components by endothelial cells. Am J Pathol 160, 673-680.
144. Dean DD, Schwartz Z, Schmitz J, Muniz OE, Lu Y, Calderon F, Howell DS, &, Boyan BD, (1996) Vitamin D regulation of metalloproteinase activity in matrix vesicles. Connect Tissue Res 35, 331-336.
145. Schmitz JP, Dean DD, Schwartz Z, Cochran DL, Grant GM, Klebe RJ, Nakaya H, &, Boyan BD, (1996) Chondrocyte cultures express matrix metalloproteinase mRNA and immunoreactive protein; stromelysin-1 and 72 kDa gelatinase are localized in extracellular matrix vesicles. J Cell Biochem 61, 375-391.
146. Graves LE, Ariztia EV, Navari JR, Matzel HJ, Stack MS, &, Fishman DA, (2004) Proinvasive properties of ovarian cancer ascites-derived membrane vesicles. Cancer Res 64, 7045-7049.
147. Ginestra A, Monea S, Seghezzi G, Dolo V, Nagase H, Mignatti P, &, Vittorelli ML, (1997) Urokinase plasminogen activator and gelatinases are associated with membrane vesicles shed by human HT1080 fibrosarcoma cells. J Biol Chem 272, 17216-17222.
148. Vilen ST, Nyberg P, Hukkanen M, Sutinen M, Ylipalosaari M, Bjartell A, Paju A, Haaparanta V, Stenman UH, Sorsa T, et al. (2008) Intracellular co-localization of trypsin-2 and matrix metalloprotease-9: possible proteolytic cascade of trypsin-2, MMP-9 and enterokinase in carcinoma. Exp Cell Res 314, 914-926.
149. Schnaeker EM, Ossig R, Ludwig T, Dreier R, Oberleithner H, Wilhelmi M, &, Schneider SW, (2004) Microtubule-dependent matrix metalloproteinase-2/ matrix metalloproteinase-9 exocytosis: prerequisite in human melanoma cell invasion. Cancer Res 64, 8924-8931.