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http://dx.doi.org/10.4062/biomolther.2012.20.2.133

Matrix Metalloproteinases, New Insights into the Understanding of Neurodegenerative Disorders  

Kim, Yoon-Seong (Burnett School of Biomedical Sciences, College of Medicine, University of Central Florida)
Joh, Tong-H. (Department of Neurology and Neuroscience, Weill Cornell Medical College)
Publication Information
Biomolecules & Therapeutics / v.20, no.2, 2012 , pp. 133-143 More about this Journal
Abstract
Matrix metalloproteinases (MMPs) are a subfamily of zinc-dependent proteases that are re-sponsible for degradation and remodeling of extracellular matrix proteins. The activity of MMPs is tightly regulated at several levels including cleavage of prodomain, allosteric activation, com-partmentalization and complex formation with tissue inhibitor of metalloproteinases (TIMPs). In the central nervous system (CNS), MMPs play a wide variety of roles ranging from brain devel-opment, synaptic plasticity and repair after injury to the pathogenesis of various brain disorders. Following general discussion on the domain structure and the regulation of activity of MMPs, we emphasize their implication in various brain disorder conditions such as Alzheimer's disease, multiple sclerosis, ischemia/reperfusion and Parkinson's disease. We further highlight accumu-lating evidence that MMPs might be the culprit in Parkinson's disease (PD). Among them, MMP-3 appears to be involved in a range of pathogenesis processes in PD including neuroinflamma-tion, apoptosis and degradation of ${\alpha}$-synuclein and DJ-1. MMP inhibitors could represent poten-tial novel therapeutic strategies for treatments of neurodegenerative diseases.
Keywords
Matrix metalloproteinases; MMP-3; Parkinson's disease; Microglia; Neurodegenerative disorders;
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1 Eguchi, T., Kubota, S., Kawata, K., Mukudai, Y., Uehara, J., Ohgawara, T., Ibaragi, S., Sasaki, A., Kuboki, T. and Takigawa, M. (2008) Novel transcription-factor-like function of human matrix metalloproteinase 3 regulating the CTGF/CCN2 gene. Mol. Cell Biol. 28, 2391-2413.   DOI   ScienceOn
2 Fainardi, E., Castellazzi, M., Tamborino, C., Trentini, A., Manfrinato, M. C., Baldi, E., Tola, M. R., Dallocchio, F., Granieri, E. and Bellini, T. (2009) Potential relevance of cerebrospinal fl uid and serum levels and intrathecal synthesis of active matrix metalloproteinase-2 (MMP-2) as markers of disease remission in patients with multiple sclerosis. Mult. Scler. 15, 547-554.   DOI   ScienceOn
3 Forsyth, P. A., Wong, H., Laing, T. D., Rewcastle, N. B., Morris, D. G., Muzik, H., Leco, K. J., Johnston, R. N., Brasher, P. M., Sutherland, G. and Edwards, D. R. (1999) Gelatinase-A (MMP-2), gelatinase-B (MMP-9) and membrane type matrix metalloproteinase-1 (MT1- MMP) are involved in different aspects of the pathophysiology of malignant gliomas. Br. J. Cancer. 79, 1828-1835.   DOI
4 Freise, C., Erben, U., Muche, M., Farndale, R., Zeitz, M., Somasundaram, R. and 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.   DOI   ScienceOn
5 Gasche, Y., Copin, J. C., Sugawara, T., Fujimura, M. and Chan, P. H. (2001) Matrix metalloproteinase inhibition prevents oxidative stress-associated blood-brain barrier disruption after transient focal cerebral ischemia. J. Cereb. Blood Flow Metab. 21, 1393-1400.
6 Gearing, A. J., Beckett, P., Christodoulou, M., Churchill, M., Clements, J., Davidson, A. H., Drummond, A. H., Galloway, W. A., Gilbert, R., Gordon, J. L., Gordon, J. L., Leber, T. M., Mangan, M., Miller, K., Nayee, P., Owen, K., Patel, S., Thomas, W., Wells, G., Wood, L. M. and Woolley, K. (1994) Processing of tumour necrosis factor-alpha precursor by metalloproteinases. Nature. 370, 555-557.   DOI
7 Giuliani, F., Fu, S. A., Metz, L. M. and Yong, V. W. (2005) Effective combination of minocycline and interferon-beta in a model of multiple sclerosis. J. Neuroimmunol. 165, 83-91.   DOI
8 Gross, J. and Lapiere, C, M. (1962) Collagenolytic activity in amphibian tissues: a tissue culture assay. Proc. Natl. Acad. Sci. USA. 48, 1014-1022.   DOI   ScienceOn
9 Gu, Z., Cui, J., Brown, S., Fridman, R., Mobashery, S., Strongin, A. Y. and Lipton, S. A. (2005) A highly specifi c inhibitor of matrix metalloproteinase- 9 rescues laminin from proteolysis and neurons from apoptosis in transient focal cerebral ischemia. J. Neurosci. 25, 6401-6408.   DOI   ScienceOn
10 Gu, Z., Kaul, M., Yan, B., Kridel, S. J., Cui, J., Strongin, A., Smith, J. W., Liddington, R. C. and Lipton, S. A. (2002) S-nitrosylation of matrix metalloproteinases: signaling pathway to neuronal cell death. Science. 297, 1186-1190.   DOI   ScienceOn
11 Hewson, A. K., Smith, T., Leonard, J. P. and Cuzner, M. L. (1995) Suppression of experimental allergic encephalomyelitis in the Lewis rat by the matrix metalloproteinase inhibitor Ro31-9790. Infl amm. Res. 44, 345-349.   DOI   ScienceOn
12 Horstmann, S., Budig, L., Gardner, H., Koziol, J., Deuschle, M., Schilling, C. and Wagner, S. (2010) Matrix metalloproteinases in peripheral blood and cerebrospinal fl uid in patients with Alzheimer's disease. International psychogeriatrics / IPA 22: 966-972   DOI   ScienceOn
13 Hu, J., Van den Steen, P. E., Sang, Q. X. and Opdenakker, G. (2007) Matrix metalloproteinase inhibitors as therapy for infl ammatory and vascular diseases. Nat. Rev. Drug Discov. 6, 480-498.   DOI   ScienceOn
14 Ip, Y. C., Cheung, S. T. and Fan, S. T. (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.   DOI   ScienceOn
15 Ishiguro, N., Ito, T., Obata, K., Fujimoto, N. and Iwata, H. (1996) Determination of stromelysin-1, 72 and 92 kDa type IV collagenase, tissue inhibitor of metalloproteinase-1 (TIMP-1), and TIMP-2 in synovial fl uid and serum from patients with rheumatoid arthritis. J. Rheumatol. 23, 1599-1604.
16 Kim, E. M. and Hwang, O. (2011) Role of matrix metalloproteinase-3 in neurodegeneration. J. Neurochem. 116, 22-32.   DOI   ScienceOn
17 Ito, S., Kimura, K., Haneda, M., Ishida, Y., Sawada, M. and Isobe, K. (2007) Induction of matrix metalloproteinases (MMP3, MMP12 and MMP13) expression in the microglia by amyloid-beta stimulation via the PI3K/Akt pathway. Exp. Gerontol. 42, 532-537.   DOI   ScienceOn
18 Joo, S. H., Kwon, K. J., Kim, J. W., Kim, J. W., Hasan, M. R., Lee, H. J., Han, S. H. and Shin, C. Y. (2010) Regulation of matrix metalloproteinase- 9 and tissue plasminogen activator activity by alphasynuclein in rat primary glial cells. Neurosci. Lett. 469, 352-356.   DOI   ScienceOn
19 Kheradmand, F., Werner, E., Tremble, P., Symons, M. and Werb, Z. (1998) Role of Rac1 and oxygen radicals in collagenase-1 expression induced by cell shape change. Science. 280, 898-902.   DOI
20 Kim, K. S., Kim, H. Y., Joe, E. H. and Jou, I. (2008) Matrix metalloproteinase- 3 induction in rat brain astrocytes: focus on the role of two AP-1 elements. Biochem. J. 410, 605-611.   DOI   ScienceOn
21 Kim, Y. S., Choi, D. H., Block, M. L., Lorenzl, S., Yang, L., Kim, Y. J., Sugama, S., Cho, B. P., Hwang, O., Browne, S. E., Kim, S. Y., Hong, J. S., Beal, M. F. and Joh, T. H. (2007) A pivotal role of matrix metalloproteinase-3 activity in dopaminergic neuronal degeneration via microglial activation. FASEB J. 21, 179-187.
22 Kim, Y. S., Kim, S. S., Cho, J. J., Choi, D. H., Hwang, O., Shin, D. H., Chun, H. S., Beal, M. F. and Joh, T. H. (2005) Matrix metalloproteinase- 3: a novel signaling proteinase from apoptotic neuronal cells that activates microglia. J. Neurosci. 25, 3701-3711.   DOI   ScienceOn
23 Korzus, E., Nagase, H., Rydell, R. and Travis, J. (1997) The mitogenactivated protein kinase and JAK-STAT signaling pathways are required for an oncostatin M-responsive element-mediated activation of matrix metalloproteinase 1 gene expression. J. Biol. Chem. 272, 1188-1196.   DOI
24 Lee, M. K., Stirling, W., Xu, Y., Xu, X., Qui, D., Mandir, A. S., Dawson, T. M., Copeland, N. G., Jenkins, N. A. and Price, D. L. (2002) Human alpha-synuclein-harboring familial Parkinson's disease-linked Ala-53 --> Thr mutation causes neurodegenerative disease with alpha-synuclein aggregation in transgenic mice. Proc. Natl. Acad. Sci. USA. 99, 8968-8973.   DOI   ScienceOn
25 Kwan, J. A., Schulze, C. J., Wang, W., Leon, H., Sariahmetoglu, M., Sung, M., Sawicka, J., Sims, D. E., Sawicki, G. and Schulz, R. (2004) Matrix metalloproteinase-2 (MMP-2) is present in the nucleus of cardiac myocytes and is capable of cleaving poly (ADPribose) polymerase (PARP) in vitro. FASEB J. 18, 690-692.
26 Larsen, P. H., DaSilva, A. G., Conant, K. and Yong, V. W. (2006) Myelin formation during development of the CNS is delayed in matrix metalloproteinase-9 and -12 null mice. J. Neurosci. 26, 2207-2214.   DOI   ScienceOn
27 Larsen, P. H., Wells, J. E., Stallcup, W. B., Opdenakker, G. and Yong, V. W. (2003) Matrix metalloproteinase-9 facilitates remyelination in part by processing the inhibitory NG2 proteoglycan. J. Neurosci. 23, 11127-11135.
28 Lee, R., Kermani, P., Teng, K. K. and Hempstead, B. L. (2001) Regulation of cell survival by secreted proneurotrophins. Science. 294, 1945-1948.   DOI   ScienceOn
29 Lee, S. R., Kim, H. Y., Rogowska, J., Zhao, B. Q., Bhide, P., Parent, J. M. and Lo, E. H. (2006) Involvement of matrix metalloproteinase in neuroblast cell migration from the subventricular zone after stroke. J. Neurosci. 26, 3491-3495.   DOI   ScienceOn
30 Li, W., Chang, L., Rong, Z. and Liu, W. (2011) Retinoic aacid diminished the expression of MMP-2 in hyperoxia-exposed premature rat lung fi broblasts through regulating mitogen-activated protein kinases. J. Huazhong. Univ. Sci. Technolog. Med. Sci. 31, 251-257.   DOI   ScienceOn
31 Liu, X., Manzano, G., Lovett, D. H. and Kim, H. T. (2010) Role of AP-1 and RE-1 binding sites in matrix metalloproteinase-2 transcriptional regulation in skeletal muscle atrophy. Biochem. Biophys. Res. Commun. 396, 219-223.   DOI   ScienceOn
32 Li, W., West, N., Colla, E., Pletnikova, O., Troncoso, J. C., Marsh, L., Dawson, T. M., Jäkälä, P., Hartmann, T., Price, D. L. and Lee, M. K. (2005) Aggregation promoting C-terminal truncation of alphasynuclein is a normal cellular process and is enhanced by the familial Parkinson's disease-linked mutations. Proc. Natl. Acad. Sci. USA. 102, 2162-2167.   DOI   ScienceOn
33 Limb, G. A., Matter, K., Murphy, G., Cambrey, A. D., Bishop, P. N., Morris, G. E. and Khaw, P. T. (2005) Matrix metalloproteinase-1 associates with intracellular organelles and confers resistance to lamin A/C degradation during apoptosis. Am. J. Pathol. 166, 1555-1563.   DOI   ScienceOn
34 Liu, C. W., Giasson, B. I., Lewis, K. A., Lee, V. M., Demartino, G. N. and Thomas, P. J. (2005) A precipitating role for truncated alphasynuclein and the proteasome in alpha-synuclein aggregation: implications for pathogenesis of Parkinson disease. J. Biol. Chem. 280, 22670-22678.   DOI
35 Lorenzl, S., Albers, D. S., Narr, S., Chirichigno, J. and Beal, M. F. (2002) Expression of MMP-2, MMP-9, and MMP-1 and their endogenous counterregulators TIMP-1 and TIMP-2 in postmortem brain tissue of Parkinson's disease. Exp. Neurol. 178, 13-20.   DOI   ScienceOn
36 Lorenzl, S., Albers, D. S., Relkin, N., Ngyuen, T., Hilgenberg, S. L., Chirichigno, J., Cudkowicz, M. E. and Beal, M. F. (2003) Increased plasma levels of matrix metalloproteinase-9 in patients with Alzheimer's disease. Neurochem. Int. 43, 191-196.   DOI   ScienceOn
37 Maeda, A. and Sobel, R. A. (1996) Matrix metalloproteinases in the normal human central nervous system, microglial nodules, and multiple sclerosis lesions. J. Neuropathol. Exp. Neurol. 55, 300- 309.   DOI
38 Matsuno, H., Yudoh, K., Watanabe, Y., Nakazawa, F., Aono, H. and Kimura, T. (2001) Stromelysin-1 (MMP-3) in synovial fl uid of patients with rheumatoid arthritis has potential to cleave membrane bound Fas ligand. J. Rheumatol. 28, 22-28.
39 Marchenko, N. D., Marchenko, G. N., Weinreb, R. N., Lindsey, J. D., Kyshtoobayeva, A., Crawford, H. C. and Strongin, A. Y. (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.   DOI   ScienceOn
40 Matrisian, L. M., Glaichenhaus, N., Gesnel, M. C. and Breathnach, R. (1985) Epidermal growth factor and oncogenes induce transcription of the same cellular mRNA in rat fi broblasts. EMBO J. 4, 1435- 1440.
41 McCarthy, S. M., Bove, P. F., Matthews, D. E., Akaike, T. and van der Vliet, A. (2008) Nitric oxide regulation of MMP-9 activation and its relationship to modifi cations of the cysteine switch. Biochemistry. 47, 5832-5840.   DOI   ScienceOn
42 McClain, J. A., Phillips, L. L. and Fillmore, H. L. (2009) Increased MMP-3 and CTGF expression during lipopolysaccharide-induced dopaminergic neurodegeneration. Neurosci. Lett. 460, 27-31.   DOI   ScienceOn
43 Meighan, S. E., Meighan, P. C., Choudhury, P., Davis, C. J., Olson, M. L., Zornes, P. A., Wright, J. W. and Harding, J. W. (2006) Effects of extracellular matrix-degrading proteases matrix metalloproteinases 3 and 9 on spatial learning and synaptic plasticity. J. Neurochem. 96, 1227-1241.   DOI   ScienceOn
44 Metz, L. M., Zhang, Y., Yeung, M., Patry, D. G., Bell, R. B., Stoian, C. A., Yong, V. W., Patten, S. B., Duquette, P., Antel, J. P. and Mitchell, J. R. (2004) Minocycline reduces gadolinium-enhancing magnetic resonance imaging lesions in multiple sclerosis. Ann. Neurol. 55, 756.   DOI   ScienceOn
45 Ogier, C., Bernard, A., Chollet, A. M., LE Diguardher, T., Hanessian, S., Charton, G., Khrestchatisky, M. and Rivera, S. (2006) Matrix metalloproteinase- 2 (MMP-2) regulates astrocyte motility in connection with the actin cytoskeleton and integrins. Glia. 54, 272-284.   DOI   ScienceOn
46 Miller, D. W., Ahmad, R., Hague, S., Baptista, M. J., Canet-Aviles, R., McLendon, C., Carter, D. M., Zhu, P. P., Stadler, J., Chandran, J., Klinefelter, G. R. Blackstone, C. and Cookson, M. R. (2003) L166P mutant DJ-1, causative for recessive Parkinson's disease, is degraded through the ubiquitin-proteasome system. J. Biol. Chem. 278, 36588-36595.   DOI   ScienceOn
47 Miners, J. S., Baig, S., Palmer, J., Palmer, L. E., Kehoe, P. G. and Love, S. (2008) Abeta-degrading enzymes in Alzheimer's disease. Brain Pathol. 18, 240-252.   DOI   ScienceOn
48 Mohanam, S., Wang, S. W., Rayford, A., Yamamoto, M., Sawaya, R., Nakajima, M., Liotta, L. A., Nicolson, G. L., Stetler-Stevenson, W. G. and Rao, J. S. (1995) Expression of tissue inhibitors of metalloproteinases: negative regulators of human glioblastoma invasion in vivo. Clin. Exp. Metastasis. 13, 57-62.   DOI   ScienceOn
49 Ohnishi. S. and Takano, K. (2004) Amyloid fi brils from the viewpoint of protein folding. Cell Mol. Life Sci. 61, 511-524.   DOI   ScienceOn
50 Okamoto, T., Akaike, T., Sawa, T., Miyamoto, Y., van der Vliet, A. and Maeda, H. (2001) Activation of matrix metalloproteinases by peroxynitrite-induced protein S-glutathiolation via disulfi de S-oxide formation. J. Biol. Chem. 276, 29596-29602.   DOI   ScienceOn
51 Opdenakker, G., Dillen, C., Fiten, P., Martens, E., Van Aelst, I., Van den Steen, P. E., Nelissen, I., Starckx, S., Descamps, F. J., Hu, J., Piccard, H., Van Damme, J., Wormald, M. R., Rudd, P. M. and Dwek, R. A. (2006) Remnant epitopes, autoimmunity and glycosylation. Biochim. Biophys. Acta. 1760, 610-615.   DOI   ScienceOn
52 Osteen, K. G., Bruner, K. L. and Sharpe-Timms, K. L. (1996) Steroid and growth factor regulation of matrix metalloproteinase expression and endometriosis. Semin. Reprod. Endocrinol. 14, 247-255.   DOI
53 Ries, C. and Petrides, P. E. (1995) Cytokine regulation of matrix metalloproteinase activity and its regulatory dysfunction in disease. Biol. Chem. Hoppe. Seyler. 376, 345-355.
54 Polymeropoulos, M. H., Lavedan, C., Leroy, E., Ide, S. E., Dehejia, A., Dutra, A., Pike, B., Root, H., Rubenstein, J., Boyer, R., Stenroos, E. S., Chandrasekharappa, S., Athanassiadou, A., Papapetropoulos, T., Johnson, W. G., Lazzarini, A. M., Duvoisin, R. C., Di Iorio, G., Golbe, L. I. and Nussbaum, R. L. (1997) Mutation in the alphasynuclein gene identifi ed in families with Parkinson's disease. Science. 276, 2045-2047.   DOI
55 Rao, J. S., Yamamoto, M., Mohaman, S., Gokaslan, Z. L., Fuller, G. N., Stetler-Stevenson, W. G., Rao, V. H., Liotta, L. A., Nicolson, G. L. and Sawaya, R. E. (1996) Expression and localization of 92 kDa type IV collagenase/gelatinase B (MMP-9) in human gliomas. Clin. Exp. Metastasis. 14, 12-18.
56 Reunanen, N., Westermarck, J., Hakkinen, L., Holmstrom, T. H., Elo, I., Eriksson, J. E. and Kahari, V. M. (1998) Enhancement of fi broblast collagenase (matrix metalloproteinase-1) gene expression by ceramide is mediated by extracellular signal-regulated and stressactivated protein kinase pathways. J. Biol. Chem. 273, 5137-5145.   DOI
57 Roher, A. E., Kasunic, T. C., Woods, A. S., Cotter, R. J., Ball, M. J. and Fridman, R. (1994) Proteolysis of A beta peptide from Alzheimer disease brain by gelatinase A. Biochem Biophys Res Commun. 205, 1755-1761.   DOI   ScienceOn
58 Romanic, A. M., White, R. F., Arleth, A. J., Ohlstein, E. H. and Barone, F. C. (1998) Matrix metalloproteinase expression increases after cerebral focal ischemia in rats: inhibition of matrix metalloproteinase- 9 reduces infarct size. Stroke. 29, 1020-1030.   DOI   ScienceOn
59 Rosenberg, G. A., Cunningham, L. A., Wallace, J., Alexander, S., Estrada, E. Y., Grossetete, M., Razhagi, A., Miller, K. and Gearing, A. (2001) Immunohistochemistry of matrix metalloproteinases in reperfusion injury to rat brain: activation of MMP-9 linked to stromelysin- 1 and microglia in cell cultures. Brain Res. 893, 104-112.   DOI
60 Sang, Q. X., Jin, Y., Newcomer, R. G., Monroe, S. C., Fang, X., Hurst, D. R., Lee, S., Cao, Q. and Schwartz, M. A. (2006) Matrix metalloproteinase inhibitors as prospective agents for the prevention and treatment of cardiovascular and neoplastic diseases. Curr. Top. Med. Chem. 6, 289-316.   DOI   ScienceOn
61 Sapolsky, A. I., Howell, D. S. and Woessner JF, Jr. (1974) Neutral proteases and cathepsin D in human articular cartilage. The Journal of clinical investigation 53, 1044-1053   DOI
62 Sellebjerg, F. and Sorensen, T. L. (2003) Chemokines and matrix metalloproteinase- 9 in leukocyte recruitment to the central nervous system. Brain Res. Bull. 61, 347-355.   DOI   ScienceOn
63 Shin, E. J., Kim, E. M., Lee, J. A., Rhim, H. and Hwang, O. (2012) Matrix metalloproteinase-3 is activated by HtrA2/Omi in dopaminergic cells: Relevance to Parkinson's disease. Neurochem. Int. 60, 249-256.   DOI   ScienceOn
64 Singh, N. K., Quyen, D. V., Kundumani-Sridharan, V., Brooks, P. C. and Rao, G. N. (2010) AP-1 (Fra-1/c-Jun)-mediated induction of expression of matrix metalloproteinase-2 is required for 15S-hydroxyeicosatetraenoic acid-induced angiogenesis. J. Biol. Chem. 285, 16830-16843.   DOI
65 Si-Tayeb, K., Monvoisin, A., Mazzocco, C., Lepreux, S., Decossas, M., Cubel, G., Taras, D., Blanc, J. F., Robinson, D. R. and Rosenbaum, J. (2006) Matrix metalloproteinase 3 is present in the cell nucleus and is involved in apoptosis. Am. J. Pathol. 169, 1390-1401.   DOI   ScienceOn
66 Spillantini, M. G., Schmidt, M. L., Lee, V. M., Trojanowski, J. Q., Jakes, R. and Goedert, M. (1997) Alpha-synuclein in Lewy bodies. Nature. 388, 839-840.   DOI
67 Starckx, S., Van den Steen, P. E., Verbeek, R., van Noort, J. M. and 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.   DOI
68 Sung, J. Y., Park, S. M., Lee, C. H., Um, J. W., Lee, H. J., Kim, J., Oh, Y. J., Lee, S. T., Paik, S. R. and Chung, K. C. (2005) Proteolytic cleavage of extracellular secreted {alpha}-synuclein via matrix metalloproteinases. J. Biol. Chem. 280, 25216-25224.   DOI   ScienceOn
69 Steffensen, B., Wallon, U. M. and Overall, C. M. (1995) Extracellular matrix binding properties of recombinant fi bronectin type II-like modules of human 72-kDa gelatinase/type IV collagenase. High affi nity binding to native type I collagen but not native type IV collagen. J. Biol. Chem. 270, 11555-11566.   DOI   ScienceOn
70 Stojic, J., Hagemann, C., Haas, S., Herbold, C., Kühnel, S., Gerngras, S., Roggendorf, W., Roosen, K. and Vince, G. H. (2008) Expression of matrix metalloproteinases MMP-1, MMP-11 and MMP-19 is correlated with the WHO-grading of human malignant gliomas. Neurosci. Res. 60, 40-49.   DOI   ScienceOn
71 Sung, M. M., Schulz, C. G., Wang, W., Sawicki, G., Bautista-López, N. L. and Schulz, R. (2007) Matrix metalloproteinase-2 degrades the cytoskeletal protein alpha-actinin in peroxynitrite mediated myocardial injury. J. Mol. Cell Cardiol. 43, 429-436.   DOI   ScienceOn
72 Szklarczyk, A., Lapinska, J., Rylski, M., McKay, R. D. and Kaczmarek, L. (2002) Matrix metalloproteinase-9 undergoes expression and activation during dendritic remodeling in adult hippocampus. J. Neurosci. 22, 920-930.
73 Tiraboschi, P., Hansen, L. A., Thal, L. J. and Corey-Bloom, J. (2004) The importance of neuritic plaques and tangles to the development and evolution of AD. Neurology. 62, 1984-1989.   DOI   ScienceOn
74 Treadwell, B. V., Neidel, J., Pavia, M., Towle, C. A., Trice, M. E. and Mankin, H. J. (1986) Purifi cation and characterization of collagenase activator protein synthesized by articular cartilage. Arch. Biochem. Biophys. 251, 715-723.   DOI   ScienceOn
75 Uhm, J. H., Dooley, N. P., Villemure, J. G. and Yong, V. W. (1996) Glioma invasion in vitro: regulation by matrix metalloprotease-2 and protein kinase C. Clin. Exp. Metastasis. 14, 421-433.   DOI   ScienceOn
76 Van Lint, P. and Libert, C. (2007) Chemokine and cytokine processing by matrix metalloproteinases and its effect on leukocyte migration and infl ammation. J. Leukoc. Biol. 82, 1375-1381.   DOI   ScienceOn
77 Ulisse, S., Farina, A. R., Piersanti, D., Tiberio, A., Cappabianca, L., D'Orazi, G., Jannini, E. A., Malykh, O., Stetler-Stevenson, W. G. and D'Armiento, M. (1994) Follicle-stimulating hormone increases the expression of tissue inhibitors of metalloproteinases TIMP-1 and TIMP-2 and induces TIMP-1 AP-1 site binding complex(es) in prepubertal rat Sertoli cells. Endocrinology. 135, 2479-2487.   DOI   ScienceOn
78 Vaillant, C., Meissirel, C., Mutin, M., Belin, M. F., Lund, L. R. and Thomasset, N. (2003) MMP-9 defi ciency affects axonal outgrowth, migration, and apoptosis in the developing cerebellum. Mol. Cell Neurosci. 24, 395-408.   DOI   ScienceOn
79 Van den Steen, P. E., Van Aelst, I., Hvidberg, V., Piccard, H., Fiten, P., Jacobsen, C., Moestrup, S. K., Fry, S., Royle, L., Wormald, M. R., Wallis, R., Rudd, P. M., Dwek, R. A. and Opdenakker, G. (2006) The hemopexin and O-glycosylated domains tune gelatinase B/ MMP-9 bioavailability via inhibition and binding to cargo receptors. J. Biol. Chem. 281, 18626-18637.   DOI
80 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.   DOI   ScienceOn
81 Vincenti, M. P. (2001) The matrix metalloproteinase (MMP) and tissue inhibitor of metalloproteinase (TIMP) genes. (2001) Transcriptional and posttranscriptional regulation, signal transduction and celltype- specifi c expression. Methods Mol. Biol. 151, 121-148.
82 Vincenti, M. P. and Brinckerhoff, C. E. (2007) Signal transduction and cell-type specifi c regulation of matrix metalloproteinase gene expression: can MMPs be good for you? J. Cell Physiol. 213, 355- 364.   DOI   ScienceOn
83 Wang, W., Schulze, C. J., Suarez-Pinzon, W. L., Dyck, J. R., Sawicki, G. and Schulz, R. (2002b) Intracellular action of matrix metalloproteinase- 2 accounts for acute myocardial ischemia and reperfusion injury. Circulation. 106, 1543-1549.   DOI   ScienceOn
84 Agrawal, S., Anderson, P., Durbeej, M., van Rooijen, N., Ivars, F., Opdenakker, G. and Sorokin, L. M. (2006) Dystroglycan is selectively cleaved at the parenchymal basement membrane at sites of leukocyte extravasation in experimental autoimmune encephalomyelitis. J. Exp. Med. 203, 1007-1019.   DOI   ScienceOn
85 Agrawal, S. M., Lau, L. and Yong, V. W. (2008) MMPs in the central nervous system: where the good guys go bad. Semin. Cell Dev. Biol. 19, 42-51.   DOI   ScienceOn
86 Aldonyte, R., Brantly, M., Block, E., Patel, J. and Zhang, J. (2009) Nuclear localization of active matrix metalloproteinase-2 in cigarette smoke-exposed apoptotic endothelial cells. Exp. Lung Res. 35, 59-75.   DOI   ScienceOn
87 Walker, E. J. and Rosenberg, G. A. (2010) Divergent role for MMP-2 in myelin breakdown and oligodendrocyte death following transient global ischemia. J. Neurosci. Res. 88, 764-773.
88 Wang, W., Sawicki, G. and Schulz, R. (2002a) Peroxynitrite-induced myocardial injury is mediated through matrix metalloproteinase-2. Cardiovasc. Res. 53, 165-174.   DOI   ScienceOn
89 Waubant, E., Goodkin, D. E., Gee, L., Bacchetti, P., Sloan, R., Stewart, T., Andersson, P. B., Stabler, G. and Miller, K. (1999) Serum MMP-9 and TIMP-1 levels are related to MRI activity in relapsing multiple sclerosis. Neurology. 53, 1397-1401.   DOI   ScienceOn
90 Wenk, G. L. (2003) Neuropathologic changes in Alzheimer's disease. J. Clin. Psychiatry. 64(Suppl 9), 7-10.
91 Werb, Z. and Reynolds, J. J. (1974) Stimulation by endocytosis of the secretion of collagenase and neutral proteinase from rabbit synovial fi broblasts. J. Exp. Med. 140, 1482-1497.   DOI   ScienceOn
92 Woo, M. S., Park, J. S., Choi, I. Y., Kim, W. K. and Kim, H. S. (2008) Inhibition of MMP-3 or -9 suppresses lipopolysaccharide-induced expression of proinfl ammatory cytokines and iNOS in microglia. J. Neurochem. 106, 770-780.   DOI   ScienceOn
93 Yamamoto, M., Hirayama, R., Naruse, K., Yoshino, K., Shimada, A., Inoue, S., Kayagaki, N., Yagita, H., Okumura, K. and Ikeda, S. (1999) Structure-activity relationship of hydroxamate-based inhibitors on membrane-bound Fas ligand and TNF-alpha processing. Drug Des. Discov. 16, 119-130.
94 Auble, D. T. and Brinckerhoff, C. E. (1991) The AP-1 sequence is necessary but not suffi cient for phorbol induction of collagenase in fi - broblasts. Biochemistry. 30, 4629-4635.   DOI   ScienceOn
95 Allan, J. A., Docherty, A. J., Barker, P. J., Huskisson, N. S., Reynolds, J. J. and Murphy, G. (1995) Binding of gelatinases A and B to type-I collagen and other matrix components. Biochem. J. 309, 299-306.
96 Asahi, M., Asahi, K., Jung, J. C., del Zoppo, G. J., Fini, M. E. and Lo, E. H. (2000) Role for matrix metalloproteinase 9 after focal cerebral ischemia: effects of gene knockout and enzyme inhibition with BB- 94. J. Cereb. Blood Flow Metab. 20, 1681-1689.
97 Asahi, M., Sumii, T., Fini, M. E., Itohara, S. and Lo, E. H. (2001) Matrix metalloproteinase 2 gene knockout has no effect on acute brain injury after focal ischemia. Neuroreport. 12, 3003-3007.   DOI   ScienceOn
98 Avolio, C., Ruggieri, M., Giuliani, F., Liuzzi, G. M., Leante, R., Riccio, P., Livrea, P. and Trojano, M. (2003) Serum MMP-2 and MMP-9 are elevated in different multiple sclerosis subtypes. J. Neuroimmunol. 136, 46-53.   DOI
99 Baba, M., Nakajo, S., Tu, P. H., Tomita, T., Nakaya, K., Lee, V. M., Trojanowski, J. Q. and Iwatsubo, T. (1998) Aggregation of alphasynuclein in Lewy bodies of sporadic Parkinson's disease and dementia with Lewy bodies. Am. J. Pathol. 152, 879-884.
100 Backstrom, J. R., Miller, C. A. and Tokes, Z. A. (1992) Characterization of neutral proteinases from Alzheimer-affected and control brain specimens: identifi cation of calcium-dependent metalloproteinases from the hippocampus. J. Neurochem. 58, 983-992.   DOI
101 Bannikov, G. A., Karelina, T. V., Collier, I. E., Marmer, B. L. and Goldberg, G. I. (2002) Substrate binding of gelatinase B induces its enzymatic activity in the presence of intact propeptide. J. Biol. Chem. 277, 16022-16027.   DOI
102 Yan, W., Zhang, W., Sun, L., Liu, Y., You, G., Wang, Y., Kang, C., You, Y. and Jiang, T. (2011) Identifi cation of MMP-9 specifi c microRNA expression profi le as potential targets of anti-invasion therapy in glioblastoma multiforme. Brain Res. 1411, 108-115.
103 Yamamoto, M., Mohanam, S., Sawaya, R., Fuller, G. N., Seiki, M., Sato, H., Gokaslan, Z. L., Liotta, L. A., Nicolson, G. L. and Rao, J. S. (1996) Differential expression of membrane-type matrix metalloproteinase and its correlation with gelatinase A activation in human malignant brain tumors in vivo and in vitro. Cancer Res. 56, 384-392.
104 Yan, C. and Boyd, D. D. (2007) Regulation of matrix metalloproteinase gene expression. J. Cell Physiol. 211, 19-26.   DOI   ScienceOn
105 Yan, P., Hu, X., Song, H., Yin, K., Bateman, R. J., Cirrito, J. R., Xiao, Q., Hsu, F. F., Turk, J. W., Xu, J., Hsu, C. Y., Holtzman, D. M. and Lee, J. M. (2006) Matrix metalloproteinase-9 degrades amyloidbeta fi brils in vitro and compact plaques in situ. J. Biol. Chem. 281, 24566-24574.   DOI
106 Yang, Y., Candelario-Jalil, E., Thompson, J. F., Cuadrado, E., Estrada, E. Y., Rosell, A., Montaner, J. and Rosenberg, G. A. (2010) Increased intranuclear matrix metalloproteinase activity in neurons interferes with oxidative DNA repair in focal cerebral ischemia. J. Neurochem. 112, 134-149.   DOI   ScienceOn
107 Yang, Y., Estrada, E. Y., Thompson, J. F., Liu, W. and Rosenberg, G. A. (2007) Matrix metalloproteinase-mediated disruption of tight junction proteins in cerebral vessels is reversed by synthetic matrix metalloproteinase inhibitor in focal ischemia in rat. J. Cereb. Blood Flow Metab. 27, 697-709.
108 Ye, H., Cai, P. C., Zhou, Q. and Ma, W. L. (2011) Transforming growth factor-${\beta}1$ suppresses the up-regulation of matrix metalloproteinase- 2 by lung fi broblasts in response to tumor necrosis factor-$\alpha$. Wound Repair Regen. 19, 392-399.   DOI   ScienceOn
109 Yong, V. W. (2005) Metalloproteinases: mediators of pathology and regeneration in the CNS. Nat. Rev. Neurosci. 6, 931-944.   DOI   ScienceOn
110 Becker, J. W., Marcy, A. I., Rokosz, L. L., Axel, M. G., Burbaum, J. J., Fitzgerald, P. M., Cameron, P. M., Esser, C. K., Hagmann, W. K., Hermes, J. D. and Springer, J. P. (1995) Stromelysin-1: threedimensional structure of the inhibited catalytic domain and of the C-truncated proenzyme. Protein Sci. 4, 1966-1976.   DOI   ScienceOn
111 Benesova, Y., Vasku, A., Novotna, H., Litzman, J., Stourac, P., Beranek, M., Kadanka, Z. and Bednarík, J. (2009) Matrix metalloproteinase- 9 and matrix metalloproteinase-2 as biomarkers of various courses in multiple sclerosis. Mult. Scler. 15, 316-322.   DOI   ScienceOn
112 Bode, W. (1995) A helping hand for collagenases: the haemopexin-like domain. Structure. 3, 527-530.   DOI   ScienceOn
113 Bode, W., Gomis-Rüth, F. X. and Stöckler, 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.   DOI
114 Bonifati, V., Rizzu, P., van Baren, M. J., Schaap, O., Breedveld, G. J., Krieger, E., Dekker, M. C., Squitieri, F., Ibanez, P., Joosse, M., van Dongen, J. W., Vanacore, N., van Swieten, J. C., Brice, A., Meco, G., van Duijn, C. M., Oostra, B. A. and Heutink, P. (2003) Mutations in the DJ-1 gene associated with autosomal recessive early-onset parkinsonism. Science. 299, 256-259.   DOI
115 Bozdagi, O., Nagy, V., Kwei, K. T. and Huntley, G. W. (2007) In vivo roles for matrix metalloproteinase-9 in mature hippocampal synaptic physiology and plasticity. J. Neurophysiol. 98, 334-344.   DOI   ScienceOn
116 Campbell, B. C., McLean, C. A., Culvenor, J. G., Gai, W. P., Blumbergs, P. C., Jakala, P., Beyreuther, K., Masters, C. L. and Li, Q. X. (2001) The solubility of alpha-synuclein in multiple system atrophy differs from that of dementia with Lewy bodies and Parkinson's disease. J. Neurochem. 76, 87-96.
117 Yoshiyama, Y., Asahina, M. and Hattori, T. (2000) Selective distribution of matrix metalloproteinase-3 (MMP-3) in Alzheimer's disease brain. Acta. Neuropathol. 99, 91-95.   DOI   ScienceOn
118 Yong, V. W., Krekoski, C. A., Forsyth, P. A., Bell, R. and Edwards, D. R. (1998) Matrix metalloproteinases and diseases of the CNS. Trends Neurosci. 21, 75-80.   DOI   ScienceOn
119 Yong, V. W., Zabad, R. K., Agrawal, S., Goncalves Dasilva, A. and Metz, L. M. (2007) Elevation of matrix metalloproteinases (MMPs) in multiple sclerosis and impact of immunomodulators. J. Neurol. Sci. 259, 79-84.   DOI
120 Yoshida, D., Watanabe, K., Takahashi, H., Sugisaki, Y. and Teramoto, A. (2003) Apoptotic induction by BE16627B on human malignant glioma cell lines by an anti-matrix metalloproteinase agent. Brain Tumor Pathol. 20, 13-19.   DOI   ScienceOn
121 Yushchenko, M., Weber, F., Mäder, M., Schöll, U., Maliszewska, M., Tumani, H., Felgenhauer, K. and Beuche, W. (2000) Matrix metalloproteinase- 9 (MMP-9) in human cerebrospinal fl uid (CSF): elevated levels are primarily related to CSF cell count. J. Neuroimmunol. 110, 244-251.   DOI
122 Zucker, S., Lysik, R. M., Zarrabi, M. H., Greenwald, R. A., Gruber, B., Tickle, S. P., Baker, T. S. and Docherty, A. J. (1994) Elevated plasma stromelysin levels in arthritis. J. Rheumatol. 21, 2329-2333.
123 Chandler, S., Miller, K. M., Clements, J. M., Lury, J., Corkill, D., Anthony, D. C., Adams, S. E. and Gearing, A. J. (1997) Matrix metalloproteinases, tumor necrosis factor and multiple sclerosis: an overview. J. Neuroimmunol. 72, 155-161.   DOI   ScienceOn
124 Candelario-Jalil, E., Yang, Y. and Rosenberg, G. A. (2009) Diverse roles of matrix metalloproteinases and tissue inhibitors of metalloproteinases in neuroinfl ammation and cerebral ischemia. Neuroscience. 158, 983-994.   DOI   ScienceOn
125 Canete Soler, R., Gui, Y. H., Linask, K. K. and Muschel, R. J. (1995) MMP-9 (gelatinase B) mRNA is expressed during mouse neurogenesis and may be associated with vascularization. Brain Res. Dev. Brain Res. 88, 37-52.   DOI   ScienceOn
126 Catrina, A. I., Lampa, J., Ernestam, S., af Klint, E., Bratt, J., Klareskog, L. and Ulfgren, A. K. (2002) Anti-tumour necrosis factor (TNF)-alpha therapy (etanercept) down-regulates serum matrix metalloproteinase (MMP)-3 and MMP-1 in rheumatoid arthritis. Rheumatology (Oxford). 41, 484-489.   DOI
127 Chang, D. I., Hosomi, N., Lucero, J., Heo, J. H., Abumiya, T., Mazar, A. P. and del Zoppo, G. J. (2003) Activation systems for latent matrix metalloproteinase-2 are upregulated immediately after focal cerebral ischemia. J. Cereb. Blood Flow Metab. 23, 1408-1419.
128 Chin, J. R., Murphy, G. and Werb, Z. (1985) Stromelysin, a connective tissue-degrading metalloendopeptidase secreted by stimulated rabbit synovial fi broblasts in parallel with collagenase. Biosynthesis, isolation, characterization, and substrates. J. Biol. Chem. 260, 12367-12376.
129 Cho, K. O., La, H. O., Cho, Y. J., Sung, K. W. and Kim, S. Y. (2006) Minocycline attenuates white matter damage in a rat model of chronic cerebral hypoperfusion. J. Neurosci. Res. 83, 285-291.   DOI   ScienceOn
130 Choi, D. H., Hwang, O., Lee, K. H., Lee, J., Beal, M. F. and Kim, Y. S. (2011a) DJ-1 cleavage by matrix metalloproteinase 3 mediates oxidative stress-induced dopaminergic cell death. Antioxid. Redox. Signal. 14, 2137-2150.   DOI   ScienceOn
131 Cossins, J. A., Clements, J. M., Ford, J., Miller, K. M., Pigott, R., Vos, W., Van der Valk, P. and De Groot, C. J. (1997) Enhanced expression of MMP-7 and MMP-9 in demyelinating multiple sclerosis lesions. Acta. Neuropathol. 94, 590-598.   DOI   ScienceOn
132 Choi, D. H., Kim, Y. J., Kim, Y. G., Joh, T. H., Beal, M. F. and Kim, Y. S. (2011b) Role of matrix metalloproteinase 3-mediated alphasynuclein cleavage in dopaminergic cell death. J. Biol. Chem. 286, 14168-14177.   DOI
133 Choi, D. H., Kim, E. M., Son, H. J., Joh, T. H., Kim, Y. S., Kim, D., Flint Beal, M. and Hwang, O. (2008) A novel intracellular role of matrix metalloproteinase-3 during apoptosis of dopaminergic cells. J. Neurochem. 106, 405-415.   DOI   ScienceOn
134 Choi, D. H., Kim, E. M., Son, H. J., Joh, T. H., Kim, Y. S., Kim, D., Flint Beal, M. and Hwang, O. (2008) A novel intracellular role of matrix metalloproteinase-3 during apoptosis of dopaminergic cells. J. Neurochem. 106, 405-415.   DOI   ScienceOn
135 Cuadrado, E., Rosell, A., Borrell-Pages, M., Garcia-Bonilla, L., Hernandez-Guillamon, M., Ortega-Aznar, A. and 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.   DOI   ScienceOn
136 Cuzner, M. L., Gveric, D., Strand, C., Loughlin, A. J., Paemen, L., Opdenakker, G. and Newcombe, J. (1996) The expression of tissuetype plasminogen activator, matrix metalloproteases and endogenous inhibitors in the central nervous system in multiple sclerosis: comparison of stages in lesion evolution. J. Neuropathol. Exp. Neurol. 55, 1194-1204.   DOI   ScienceOn
137 Edwards, D. R., Murphy, G., Reynolds, J. J., Whitham, S. E., Docherty, A. J., Angel, P. and Heath, J. K. (1987) Transforming growth factor beta modulates the expression of collagenase and metalloproteinase inhibitor. EMBO J. 6, 1899-1904.