Biomolecules & Therapeutics

The Korean Society of Applied Pharmacology (한국응용약물학회)
권호 표지
DOI QR코드

DOI QR Code

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)
  • Received : 2012.03.06
  • Accepted : 2012.03.15
  • Published : 2012.03.31
Download PDF
⟨ Previous Next ⟩

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

References

  1. 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. https://doi.org/10.1084/jem.20051342
  2. 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. https://doi.org/10.1016/j.semcdb.2007.06.003
  3. 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. https://doi.org/10.1080/01902140802406059
  4. 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.
  5. 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.
  6. 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. https://doi.org/10.1097/00001756-200109170-00050
  7. 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. https://doi.org/10.1021/bi00232a039
  8. 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. https://doi.org/10.1016/S0165-5728(03)00006-7
  9. 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.
  10. 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. https://doi.org/10.1111/j.1471-4159.1992.tb09352.x
  11. 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. https://doi.org/10.1074/jbc.M110931200
  12. 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. https://doi.org/10.1002/pro.5560041002
  13. 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. https://doi.org/10.1177/1352458508099482
  14. Bode, W. (1995) A helping hand for collagenases: the haemopexin-like domain. Structure. 3, 527-530. https://doi.org/10.1016/S0969-2126(01)00185-X
  15. 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. https://doi.org/10.1016/0014-5793(93)80312-I
  16. 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. https://doi.org/10.1126/science.1077209
  17. 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. https://doi.org/10.1152/jn.00202.2007
  18. 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.
  19. 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. https://doi.org/10.1016/j.neuroscience.2008.06.025
  20. 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. https://doi.org/10.1016/0165-3806(95)00079-S
  21. 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. https://doi.org/10.1093/rheumatology/41.5.484
  22. 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. https://doi.org/10.1016/S0165-5728(96)00179-8
  23. 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.
  24. 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.
  25. 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. https://doi.org/10.1002/jnr.20727
  26. 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. https://doi.org/10.1089/ars.2009.3059
  27. 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. https://doi.org/10.1074/jbc.M111.222430
  28. 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. https://doi.org/10.1111/j.1471-4159.2008.05399.x
  29. 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. https://doi.org/10.1111/j.1471-4159.2008.05399.x
  30. 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. https://doi.org/10.1007/s004010050754
  31. 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. https://doi.org/10.1038/jcbfm.2008.130
  32. 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. https://doi.org/10.1097/00005072-199612000-00002
  33. 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.
  34. 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. https://doi.org/10.1128/MCB.01288-07
  35. 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. https://doi.org/10.1177/1352458509102372
  36. 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. https://doi.org/10.1038/sj.bjc.6990291
  37. 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. https://doi.org/10.1016/j.matbio.2009.08.001
  38. 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.
  39. 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. https://doi.org/10.1038/370555a0
  40. 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. https://doi.org/10.1016/j.jneuroim.2005.04.020
  41. Gross, J. and Lapiere, C, M. (1962) Collagenolytic activity in amphibian tissues: a tissue culture assay. Proc. Natl. Acad. Sci. USA. 48, 1014-1022. https://doi.org/10.1073/pnas.48.6.1014
  42. 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. https://doi.org/10.1523/JNEUROSCI.1563-05.2005
  43. 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. https://doi.org/10.1126/science.1073634
  44. 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. https://doi.org/10.1007/BF01796266
  45. 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 https://doi.org/10.1017/S1041610210000827
  46. 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. https://doi.org/10.1038/nrd2308
  47. 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. https://doi.org/10.1002/mc.20270
  48. 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.
  49. 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. https://doi.org/10.1016/j.exger.2006.11.012
  50. 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. https://doi.org/10.1016/j.neulet.2009.12.026
  51. 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. https://doi.org/10.1126/science.280.5365.898
  52. Kim, E. M. and Hwang, O. (2011) Role of matrix metalloproteinase-3 in neurodegeneration. J. Neurochem. 116, 22-32. https://doi.org/10.1111/j.1471-4159.2010.07082.x
  53. 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. https://doi.org/10.1042/BJ20071207
  54. 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.
  55. 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. https://doi.org/10.1523/JNEUROSCI.4346-04.2005
  56. 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. https://doi.org/10.1074/jbc.272.2.1188
  57. 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.
  58. 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. https://doi.org/10.1523/JNEUROSCI.1880-05.2006
  59. 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.
  60. 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. https://doi.org/10.1073/pnas.132197599
  61. Lee, R., Kermani, P., Teng, K. K. and Hempstead, B. L. (2001) Regulation of cell survival by secreted proneurotrophins. Science. 294, 1945-1948. https://doi.org/10.1126/science.1065057
  62. 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. https://doi.org/10.1523/JNEUROSCI.4085-05.2006
  63. 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. https://doi.org/10.1007/s11596-011-0262-1
  64. 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. https://doi.org/10.1073/pnas.0406976102
  65. 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. https://doi.org/10.1016/S0002-9440(10)62371-1
  66. 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. https://doi.org/10.1074/jbc.M501508200
  67. 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. https://doi.org/10.1016/j.bbrc.2010.04.067
  68. 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. https://doi.org/10.1006/exnr.2002.8019
  69. 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. https://doi.org/10.1016/S0197-0186(03)00004-4
  70. 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. https://doi.org/10.1097/00005072-199603000-00005
  71. 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. https://doi.org/10.1016/j.biocel.2003.12.007
  72. 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.
  73. 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.
  74. 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. https://doi.org/10.1021/bi702496v
  75. 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. https://doi.org/10.1016/j.neulet.2009.05.044
  76. 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. https://doi.org/10.1111/j.1471-4159.2005.03565.x
  77. 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. https://doi.org/10.1002/ana.20111
  78. 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. https://doi.org/10.1074/jbc.M304272200
  79. 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. https://doi.org/10.1111/j.1750-3639.2008.00132.x
  80. 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. https://doi.org/10.1007/BF00144019
  81. 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. https://doi.org/10.1002/glia.20349
  82. Ohnishi. S. and Takano, K. (2004) Amyloid fi brils from the viewpoint of protein folding. Cell Mol. Life Sci. 61, 511-524. https://doi.org/10.1007/s00018-003-3264-8
  83. 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. https://doi.org/10.1074/jbc.M102417200
  84. 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. https://doi.org/10.1016/j.bbagen.2005.12.014
  85. 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. https://doi.org/10.1055/s-2007-1016334
  86. 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. https://doi.org/10.1126/science.276.5321.2045
  87. 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.
  88. 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. https://doi.org/10.1074/jbc.273.9.5137
  89. 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.
  90. 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. https://doi.org/10.1006/bbrc.1994.2872
  91. 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. https://doi.org/10.1161/01.STR.29.5.1020
  92. 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. https://doi.org/10.1016/S0006-8993(00)03294-7
  93. 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. https://doi.org/10.2174/156802606776287045
  94. 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 https://doi.org/10.1172/JCI107641
  95. 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. https://doi.org/10.1016/S0361-9230(03)00097-2
  96. 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. https://doi.org/10.1016/j.neuint.2012.01.001
  97. 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. https://doi.org/10.1074/jbc.M110.106187
  98. 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. https://doi.org/10.2353/ajpath.2006.060005
  99. 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. https://doi.org/10.1038/42166
  100. 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. https://doi.org/10.1016/S0165-5728(03)00217-0
  101. 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. https://doi.org/10.1074/jbc.270.19.11555
  102. 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. https://doi.org/10.1016/j.neures.2007.09.009
  103. 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. https://doi.org/10.1074/jbc.M503341200
  104. 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. https://doi.org/10.1016/j.yjmcc.2007.07.055
  105. 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.
  106. 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. https://doi.org/10.1212/01.WNL.0000129697.01779.0A
  107. 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. https://doi.org/10.1016/0003-9861(86)90381-4
  108. 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. https://doi.org/10.1007/BF00128958
  109. 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. https://doi.org/10.1210/en.135.6.2479
  110. 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. https://doi.org/10.1016/S1044-7431(03)00196-9
  111. 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. https://doi.org/10.1074/jbc.M512308200
  112. 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. https://doi.org/10.1189/jlb.0607338
  113. 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. https://doi.org/10.1073/pnas.87.14.5578
  114. 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.
  115. 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. https://doi.org/10.1002/jcp.21208
  116. 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.
  117. Wang, W., Sawicki, G. and Schulz, R. (2002a) Peroxynitrite-induced myocardial injury is mediated through matrix metalloproteinase-2. Cardiovasc. Res. 53, 165-174. https://doi.org/10.1016/S0008-6363(01)00445-X
  118. 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. https://doi.org/10.1161/01.CIR.0000028818.33488.7B
  119. 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. https://doi.org/10.1212/WNL.53.7.1397
  120. Wenk, G. L. (2003) Neuropathologic changes in Alzheimer's disease. J. Clin. Psychiatry. 64(Suppl 9), 7-10.
  121. 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. https://doi.org/10.1084/jem.140.6.1482
  122. 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. https://doi.org/10.1111/j.1471-4159.2008.05430.x
  123. 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.
  124. 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.
  125. Yan, C. and Boyd, D. D. (2007) Regulation of matrix metalloproteinase gene expression. J. Cell Physiol. 211, 19-26. https://doi.org/10.1002/jcp.20948
  126. 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. https://doi.org/10.1074/jbc.M602440200
  127. 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.
  128. 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. https://doi.org/10.1111/j.1471-4159.2009.06433.x
  129. 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.
  130. 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. https://doi.org/10.1111/j.1524-475X.2011.00680.x
  131. Yong, V. W. (2005) Metalloproteinases: mediators of pathology and regeneration in the CNS. Nat. Rev. Neurosci. 6, 931-944. https://doi.org/10.1038/nrn1807
  132. 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. https://doi.org/10.1016/S0166-2236(97)01169-7
  133. 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. https://doi.org/10.1016/j.jns.2006.11.021
  134. 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. https://doi.org/10.1007/BF02478942
  135. 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. https://doi.org/10.1007/PL00007428
  136. 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. https://doi.org/10.1016/S0165-5728(00)00339-8
  137. 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.

Cited by

  1. Herpes Simplex Virus Type 1 and Other Pathogens are Key Causative Factors in Sporadic Alzheimer’s Disease vol.48, pp.2, 2015, https://doi.org/10.3233/JAD-142853
  2. Leukocyte Gene Expression and Plasma Concentration in Multiple Sclerosis: Alteration of Transforming Growth Factor-βs, Claudin-11, and Matrix Metalloproteinase-2 vol.36, pp.6, 2016, https://doi.org/10.1007/s10571-015-0270-y
  3. Cerebrospinal Fluid Peptides as Potential Parkinson Disease Biomarkers: A Staged Pipeline for Discovery and Validation vol.14, pp.3, 2015, https://doi.org/10.1074/mcp.M114.040576
  4. The involvement of anterior gradient 2 in the stromal cell-derived factor 1-induced epithelial-mesenchymal transition of glioblastoma vol.37, pp.5, 2016, https://doi.org/10.1007/s13277-015-4481-0
  5. Anti-inflammatory activities and mechanisms of Artemisia asiatica ethanol extract vol.152, pp.3, 2014, https://doi.org/10.1016/j.jep.2014.01.030
  6. Post-translational modifications in neurodegeneration vol.3, pp.1, 2015, https://doi.org/10.3934/biophy.2016.1.27
  7. Altered Serum Levels of Matrix Metalloproteinase-2, -9 in Response to Electroconvulsive Therapy for Mood Disorders vol.19, pp.9, 2016, https://doi.org/10.1093/ijnp/pyw019
  8. Protopanaxatriol ginsenoside Rh1 inhibits the expression of matrix metalloproteinases and the in vitro invasion/migration of human astroglioma cells vol.63, pp.2, 2013, https://doi.org/10.1016/j.neuint.2013.05.002
  9. Whole Brain Radiation-Induced Cognitive Impairment: Pathophysiological Mechanisms and Therapeutic Targets vol.20, pp.4, 2012, https://doi.org/10.4062/biomolther.2012.20.4.357
  10. Differential effects of duration and age on the consequences of neuroinflammation in the hippocampus vol.34, pp.10, 2013, https://doi.org/10.1016/j.neurobiolaging.2013.03.034
  11. Differential temporal expression of matrix metalloproteinases following sciatic nerve crush vol.11, pp.7, 2016, https://doi.org/10.4103/1673-5374.187059
  12. MMPs: a novel drug target for schizophrenia vol.19, pp.1, 2015, https://doi.org/10.1517/14728222.2014.957672
  13. Marine pharmacology: therapeutic targeting of matrix metalloproteinases in neuroinflammation vol.22, pp.2, 2017, https://doi.org/10.1016/j.drudis.2016.09.023
  14. PEITC inhibits human brain glioblastoma GBM 8401 cell migration and invasion through the inhibition of uPA, Rho A, and Ras with inhibition of MMP-2, -7 and -9 gene expression vol.34, pp.5, 2015, https://doi.org/10.3892/or.2015.4260
  15. Transcriptomic Analyses Reveal Differential Gene Expression of Immune and Cell Death Pathways in the Brains of Mice Infected with West Nile Virus and Chikungunya Virus vol.8, 2017, https://doi.org/10.3389/fmicb.2017.01556
  16. The Use of Agmatine Provides the New Insight in an Experimental Model of Multiple Sclerosis vol.40, pp.8, 2015, https://doi.org/10.1007/s11064-015-1655-5
  17. Microglial Polarization and Inflammatory Mediators After Intracerebral Hemorrhage vol.54, pp.3, 2017, https://doi.org/10.1007/s12035-016-9785-6
  18. Potent selective inhibition of MMP-14 by chloroauric acid and its inhibitory effect on cancer cell invasion vol.5, pp.23, 2015, https://doi.org/10.1039/C4RA16532B
  19. A close look at brain dynamics: Cells and vessels seen by in vivo two-photon microscopy vol.121, 2014, https://doi.org/10.1016/j.pneurobio.2014.06.005
  20. Age and duration of inflammatory environment differentially affect the neuroimmune response and catecholaminergic neurons in the midbrain and brainstem vol.35, pp.5, 2014, https://doi.org/10.1016/j.neurobiolaging.2013.11.006
  21. Exogenous C2 Ceramide Suppresses Matrix Metalloproteinase Gene Expression by Inhibiting ROS Production and MAPK Signaling Pathways in PMA-Stimulated Human Astroglioma Cells vol.17, pp.4, 2016, https://doi.org/10.3390/ijms17040477
  22. Gamma-decanolactone inhibits iNOS and TNF-alpha production by lipopolysaccharide-activated microglia in N9 cells vol.780, 2016, https://doi.org/10.1016/j.ejphar.2016.03.029
  23. Matrix-metalloproteinases as targets for controlled delivery in cancer: An analysis of upregulation and expression vol.259, 2017, https://doi.org/10.1016/j.jconrel.2017.01.034
  24. Priming Wharton's Jelly-Derived Mesenchymal Stromal/Stem Cells With ROCK Inhibitor Improves Recovery in an Intracerebral Hemorrhage Model vol.116, pp.2, 2015, https://doi.org/10.1002/jcb.24969
  25. The anti-inflammatory role of tissue inhibitor of metalloproteinase-2 in lipopolysaccharide-stimulated microglia vol.11, pp.1, 2014, https://doi.org/10.1186/1742-2094-11-116
  26. Possible Association between Serum Matrix Metalloproteinase-9 (MMP-9) Levels and Relapse in Depressed Patients following Electroconvulsive Therapy (ECT) vol.21, pp.3, 2018, https://doi.org/10.1093/ijnp/pyx086
  27. Excitotoxicity in the pathogenesis of neurological and psychiatric disorders: Therapeutic implications vol.32, pp.3, 2018, https://doi.org/10.1177/0269881118754680
  28. Microglial interactions with the neurovascular system in physiology and pathology vol.78, pp.6, 2018, https://doi.org/10.1002/dneu.22576
  29. Potent and selective inhibition of matrix metalloproteinases by lanthanide trichloride vol.8, pp.26, 2018, https://doi.org/10.1039/C8RA00871J
  30. A new triazine bearing a pyrazolone group capable of copper, nickel, and zinc chelation vol.8, pp.6, 2018, https://doi.org/10.1039/C7RA09459K
  31. Perspectives and New Aspects of Metalloproteinases’ Inhibitors in the Therapy of CNS Disorders: From Chemistry to Medicine vol.26, pp.18, 2012, https://doi.org/10.2174/0929867325666180514111500
  32. Metalloproteinases and their tissue inhibitors in Alzheimer’s disease and other neurodegenerative disorders vol.76, pp.16, 2012, https://doi.org/10.1007/s00018-019-03178-2
  33. Matrix Metalloproteinase-9 Gene Polymorphisms in South-West Iranian Multiple Sclerosis (MS) Patients vol.55, pp.10, 2012, https://doi.org/10.1134/s1022795419100107
  34. Association between abdominal hernia and the risk of subsequent dementia vol.9, pp.11, 2012, https://doi.org/10.1002/brb3.1434
  35. A Review on Emerging Drug Targets in Treatment of Schizophrenia vol.21, pp.None, 2012, https://doi.org/10.2174/1389450121666200615150429
  36. Increased prolidase activity in Alzheimer’s dementia: A case-control study vol.53, pp.None, 2012, https://doi.org/10.1016/j.ajp.2020.102242
  37. Hold on or Cut? Integrin- and MMP-Mediated Cell–Matrix Interactions in the Tumor Microenvironment vol.22, pp.1, 2021, https://doi.org/10.3390/ijms22010238
  38. Proteolytic α-Synuclein Cleavage in Health and Disease vol.22, pp.11, 2012, https://doi.org/10.3390/ijms22115450
  39. Investigation of the role of matrix metalloproteinases in the genetic etiology of Alzheimer's disease vol.104, pp.None, 2021, https://doi.org/10.1016/j.neurobiolaging.2021.03.011
  40. Matrix Metalloproteinases Shape the Tumor Microenvironment in Cancer Progression vol.23, pp.1, 2022, https://doi.org/10.3390/ijms23010146