Role of matrix metalloproteinase-3 in neurodegeneration

Journal of Neurochemistry

Volumn 116, Issue 1, 2011, Pages 22-32

  Kim, Eun Mee ^a   Hwang, Onyou ^a  

^a University of Ulsan College of Medicine   (South Korea)

Author keywords

apoptosis; matrix metalloproteinase 3; neurodegeneration; neuroinflammation; Parkinson's disease; TIMP 1

Indexed keywords

CASPASE 3; CHYMOTRYPSIN A; DOXYCYCLINE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; LEUKOCYTE ELASTASE; MINOCYCLINE; MITOGEN ACTIVATED PROTEIN KINASE 1; STRESS ACTIVATED PROTEIN KINASE; STROMELYSIN; STROMELYSIN INHIBITOR; TISSUE INHIBITOR OF METALLOPROTEINASE 1; TRANSCRIPTION FACTOR PEA3; TUMOR NECROSIS FACTOR ALPHA; UROKINASE;

ALZHEIMER DISEASE; BINDING SITE; BLOOD BRAIN BARRIER; CELL STRESS; DIMERIZATION; DOPAMINE METABOLISM; DRUG ACTIVITY; ENZYME ACTIVITY; ENZYME SPECIFICITY; EXTRACELLULAR MATRIX; GENE OVEREXPRESSION; HUMAN; MICROGLIA; MULTIPLE SCLEROSIS; NERVE CELL PLASTICITY; NERVE DEGENERATION; NEUTROPHIL CHEMOTAXIS; NONHUMAN; OLIGOMERIZATION; OXIDATIVE STRESS; PARKINSON DISEASE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; PROTEIN TARGETING; PROTEIN TRANSPORT; REVIEW; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; UNSPECIFIED SIDE EFFECT;

ANIMALS; APOPTOSIS; HUMANS; MATRIX METALLOPROTEINASE 3; MATRIX METALLOPROTEINASE INHIBITORS; NERVE DEGENERATION; PROTEASE INHIBITORS;

EID: 78650099684     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2010.07082.x     Document Type: Review

References (108)

1. 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 (review).
2. Andres-Mateos E., Perier C., Zhang L., et al. (2007) DJ-1 gene deletion reveals that DJ-1 is an atypical peroxiredoxin-like peroxidase. Proc. Natl Acad. Sci. USA 104, 14807-14812.
3. Becker J. W., Marcy A. I., and, Rokosz L. L., et al. (1995) Stromelysin-1: three-dimensional structure of the inhibited catalytic domain and of the C-truncated proenzyme. Protein Sci. 4, 1966-1976.
4. Block M.L., Zecca L., and, Hong J.S., (2007) Microglia-mediated neurotoxicity: uncovering the molecular mechanisms. Nat. Rev. Neurosci. 8, 57-69.Review.
5. Bonneh-Barkay D., and, Wiley C. A., (2009) Brain extracellular matrix in neurodegeneration. Brain Pathol. 19, 573-585 (review).
6. Borghaei R. C., Sullivan C., and, Mochan E., (1999) Identification of a cytokine-induced repressor of interleukin-1 stimulated expression of stromelysin 1 (MMP-3). J. Biol. Chem. 274, 2126-2131.
7. Candelario-Jalil E., Taheri S., and, Yang Y., et al. (2007) Cyclooxygenase inhibition limits blood-brain barrier disruption following intracerebral injection of tumor necrosis factor-alpha in the rat. J. Pharmacol. Exp. Ther. 323, 488-498.
8. Cao J., Rehemtulla A., Pavlaki M., Kozarekar P., and, Chiarelli C., (2005) Furin directly cleaves proMMP-2 in the trans-Golgi network resulting in a nonfunctioning proteinase. J. Biol. Chem. 280, 10974-10980.
9. Carvey P. M., Zhao C. H., Hendey B., Lum H., Trachtenberg J., Desai B. S., Snyder J., Zhu Y. G., and, Ling Z. D., (2005) 6-Hydroxydopamine-induced alterations in blood-brain barrier permeability. Eur. J. Neurosci. 22, 1158-1168.
10. Cauwe B., Van den Steen P. E., and, Opdenakker G., (2007) The biochemical, biological, and pathological kaleidoscope of cell surface substrates processed by matrix metalloproteinases. Crit. Rev. Biochem. Mol. Biol. 42, 113-185 (review).
11. Cho Y., Son H. J., Kim E. M., Choi J. H., Kim S. T., Ji I. J., Choi D. H., Joh T. H., Kim Y. S., and, Hwang O., (2009) Doxycycline is neuroprotective against nigral dopaminergic degeneration by a dual mechanism involving MMP-3. Neurotox. Res. 16, 361-371.
12. Choi H. J., Jang Y. J., Kim H. J., and, Hwang O., (2000) Tetrahydrobiopterin is released from and causes preferential death of catecholaminergic cells by oxidative stress. Mol. Pharmacol. 58, 633-640.
13. Choi D. H., Kim E. M., Son H. J., Joh T. H., Kim Y. S., Kim D., Beal M. F., and, Hwang O., (2008) A novel intracellular role of matrix metalloproteinase-3 during apoptosis of dopaminergic cells. J. Neurochem. 106, 405-415.
14. Choi D. H., Hwang O., Lee K. H., Lee J., Beal F., and, Kim Y. S, (2010) DJ-1 cleavage by matrix metalloproteinase 3 mediates oxidative stress induced dopaminergic cell death. Antioxid Redox Signal. in press.
15. Clayton D. F., and, George J. M., (1999) Synucleins in synaptic plasticity and neurodegenerative disorders. J. Neurosci. Res. 58, 120-129 (review).
16. Corbitt C. A., Lin J., and, Lindsey M. L., (2007) Mechanisms to inhibit matrix metalloproteinase activity: where are we in the development of clinically relevant inhibitors? Recent Pat. Anticancer Drug Discov. 2, 135-142 (review).
17. Crocker S. J., Milner R., Pham-Mitchell N., and, Campbell I. L., (2006) Cell and agonist-specific regulation of genes for matrix metalloproteinases and their tissue inhibitors by primary glial cells. J. Neurochem. 98, 812-823.
18. Deb S., and, Gottschall P. E., (1996) Increased production of matrix metalloproteinases in enriched astrocyte and mixed hippocampal cultures treated with beta-amyloid peptides. J. Neurochem. 66, 1641-1647.
19. Dhanaraj V., Ye Q. Z., Johnson L. L., Hupe D. J., Ortwine D. F., Dunbar J. B., Jr, Rubin J. R., Pavlovsky A., Humblet C., and, Blundell T. L., (1996) X-ray structure of a hydroxamate inhibitor complex of stromelysin catalytic domain and its comparison with members of the zinc metalloproteinase superfamily. Structure 4, 375-386.
20. Docherty A. J., Lyons A., Smith B. J., Wright E. M., Stephens P. E., Harris T. J., Murphy G., and, Reynolds J. J., (1985) Sequence of human tissue inhibitor of metalloproteinases and its identity to erythroid-potentiating activity. Nature 318, 66-69.
21. D'Souza C. A., Mak B., and, Moscarello M. A., (2002) The up-regulation of stromelysin-1 (MMP-3) in a spontaneously demyelinating transgenic mouse precedes onset of disease. J. Biol. Chem. 277, 13589-13596.
22. Du Y., Ma Z., Lin S., et al. (2001) Minocycline prevents nigrostriatal dopaminergic neurodegeneration in the MPTP model of Parkinson's disease. Proc. Natl Acad. Sci. USA 98, 14669-14674.
23. Fosang A. J., Neame P. J., Hardingham T. E., Murphy G., and, Hamilton J. A., (1991) Cleavage of cartilage proteoglycan between G1 and G2 domains by stromelysins. J. Biol. Chem. 266, 15579-15582.
24. 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.
25. Gomis-Rüth F. X., Gohlke U., Betz M., Knäuper V., Murphy G., López-Otín C., and, Bode W., (1996) The helping hand of collagenase-3 (MMP-13): 2.7 A crystal structure of its C-terminal haemopexin-like domain. J. Mol. Biol. 264, 556-566.
26. Gomis-Rüth F. X., Maskos K., Betz M., et al. (1997) Mechanism of inhibition of the human matrix metalloproteinase stromelysin-1 by TIMP-1. Nature 389, 77-81.
27. Goñi-Allo B., Ramos M., Jordán J., and, Aguirre N., (2005) In vivo studies on the protective role of minocycline against excitotoxicity caused by malonate or N-methyl-d-aspartate. Exp. Neurol. 191, 326-330.
28. Grossetete M., Phelps J., Arko L., Yonas H., and, Rosenberg G. A., (2009) Elevation of matrix metalloproteinases 3 and 9 in cerebrospinal fluid and blood in patients with severe traumatic brain injury. Neurosurgery 65, 702-708.
29. Gurney K. J., Estrada E. Y., and, Rosenberg G. A., (2006) Blood-brain barrier disruption by stromelysin-1 facilitates neutrophil infiltration in neuroinflammation. Neurobiol. Dis. 23, 87-96.
30. Hammani K., Henriet P., and, Eeckhout Y., (1992) Cloning and sequencing of a cDNA encoding mouse stromelysin 1. Gene 120, 321-322.
31. Helbecque N., Cottel D., Hermant X., and, Amouyel P., (2007) Impact of the matrix metalloproteinase MMP-3 on dementia. Neurobiol. Aging 28, 1215-1220.
32. Herron G. S., Werb Z., Dwyer K., and, Banda M. J., (1986) Secretion of metalloproteinases by stimulated capillary endothelial cells. I. Production of procollagenase and prostromelysin exceeds expression of proteolytic activity. J. Biol. Chem. 261, 2810-2813.
33. Hornebeck W., Lambert E., Petitfrere E., and, Bernard P., (2005) Beneficial and detrimental influences of tissue inhibitor of metalloproteinase-1 (TIMP-1) in tumor progression. Biochimie 87, 377-383.
34. Horstmann S., Budig L., Gardner H., Koziol J., Deuschle M., Schilling C., and, Wagner S., (2010) Matrix metalloproteinases in peripheral blood and cerebrospinal fluid in patients with Alzheimer's disease. Int. Psychogeriatr. 22, 966-972.
35. Ito A., Mukaiyama A., Itoh Y., Nagase H., Thogersen I. B., Enghild J. J., Sasaguri Y., and, Mori Y., (1996) Degradation of interleukin 1beta by matrix metalloproteinases. J. Biol. Chem. 271, 14657-14660.
36. 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.
37. Ji K. A., Eu M. Y., Kang S. H., Gwag B. J., Jou I., and, Joe E. H., (2008) Differential neutrophil infiltration contributes to regional differences in brain inflammation in the substantia nigra pars compacta and cortex. Glia 56, 1039-1047.
38. Jian Liu K., and, Rosenberg G. A., (2005) Matrix metalloproteinases and free radicals in cerebral ischemia. Free Radic. Biol. Med. 39, 71-80 (review).
39. Johnson L. L., Pavlovsky A. G., Johnson A. R., Janowicz J. A., Man C. F., Ortwine D. F., Purchase C. F., II, White A. D., and, Hupe D. J., (2000) A rationalization of the acidic pH dependence for stromelysin-1 (matrix metalloproteinase-3) catalysis and inhibition. J. Biol. Chem. 275, 11026-11033.
40. Kayed R., Head E., Thompson J. L., McIntire T. M., Milton S. C., Cotman C. W., and, Glabe C. G., (2003) Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science 300, 486-489.
41. Kim Y. S., and, Joh T. H., (2006) Microglia, major player in the brain inflammation: their roles in the pathogenesis of Parkinson's disease. Exp. Mol. Med. 38, 333-347 (review).
42. Kim W. G., Mohney R. P., Wilson B., Jeohn G. H., Liu B., and, Hong J. S., (2000) Regional difference in susceptibility to lipopolysaccharide-induced neurotoxicity in the rat brain: role of microglia. J. Neurosci. 20, 6309-6316.
43. Kim H. J., Fillmore H. L., Reeves T. M., and, Phillips L. L., (2005a) Elevation of hippocampal MMP-3 expression and activity during trauma-induced synaptogenesis. Exp. Neurol. 192, 60-72.
44. Kim Y. S., Kim S. S., Cho J. J., Cho J. J., Choi D. H., Hwang O., Shin D. H., Chun H. S., Beal M. F., and, Joh T. H., (2005b) Matrix metalloproteinase-3: a novel signaling proteinase from apoptotic neuronal cells that activates microglia. J. Neurosci. 25, 3701-3711.
45. Kim Y. S., Choi D. H., Block M. L., et al. (2007) A pivotal role of matrix metalloproteinase-3 activity in dopaminergic neuronal degeneration via microglial activation. FASEB J. 21, 179-187.
46. Kim S., Moon M., and, Park S., (2009) Exendin-4 protects dopaminergic neurons by inhibition of microglial activation and matrix metalloproteinase-3 expression in an animal model of Parkinson's disease. J. Endocrinol. 202, 431-439.
47. Kim E. M., Shin E. J., Choi J. H., Son H. J., Park I. S., Joh T. H., and, Hwang O., (2010) Matrix metalloproteinase-3 is increased and participates in neuronal apoptotic signaling downstream of caspase-12 during endoplasmic reticulum stress. J. Biol. Chem. 285, 16444-16452.
48. Kirstein M., Sanz L., Quinones S., Moscat J., Az-Meco M. T., and, Saus J., (1996) Cross-talk between different enhancer elements during mitogenic induction of the human stromelysin-1 gene. J. Biol. Chem. 271, 18231-18236.
49. Kortekaas R., Leenders K. L., Van Oostrom J. C., Vaalburg W., Bart J., Willemsen A. R., and, Hendrikse N. H., (2005) Blood-brain barrier dysfunction in parkinsonia midbrain in vivo. Ann. Neurol. 57, 176-179. (Pubitemid 40179854)
50. Kouwenhoven M., Ozenci V., Tjernlund A., Pashenkov M., Homman M., Press R., and, Link H., (2002) Monocyte-derived dendritic cells express and secrete matrix-degrading metalloproteinases and their inhibitors and are imbalanced in multiple sclerosis. J. Neuroimmunol. 126, 161-171.
51. Koyama Y., and, Tanaka K., (2008) Endothelins stimulate the production of stromelysin-1 in cultured rat astrocytes. Biochem. Biophys. Res. Commun. 371, 659-663.
52. LaFerla F. M., Green K. N., and, Oddo S., (2007) Intracellular amyloid-beta in Alzheimer's disease. Nat. Rev. Neurosci. 8, 499-509 (review).
53. Lee E. J., Kim S. Y., Hyun J. W., Min S. W., Kim D. H., and, Kim H. S., (2010a) Glycitein inhibits glioma cell invasion through down-regulation of MMP-3 and MMP-9 gene expression. Chem. Biol. Interact. 185, 18-24.
54. Lee E. J., Woo M. S., Moon P. G., Baek M. C., Choi I. Y., Kim W. K., Junn E., and, Kim H. S., (2010b) Alpha-Synuclein activates microglia by inducing the expressions of matrix metalloproteinases and the subsequent activation of protease-activated receptor-1. J. Immunol. 185, 615-623.
55. Lee J., Lim E., Kim Y., Li E., and, Park S., (2010c) Ghrelin attenuates kainic acid-induced neuronal cell death in the mouse hippocampus. J. Endocrinol. 205, 263-270.
56. Levin J., Giese A., Boetzel K., Israel L., Hogen T., Nubling G., Kretzschmar H., and, Lorenzl S., (2009) Increased α-synuclein aggregation following limited cleavage by certain matrix metalloproteinases. Exp. Neurol. 215, 201-208.
57. Li W., West N., Colla E., Pletnikova O., Troncoso J. C., Marsh L., Dawson T. M., Jakala P., Hartmann T., Price D. L., and, Lee M. K., (2005) Aggregation promoting C-terminal truncation of α-synuclein is a normal cellular process and is enhanced by the familial Parkinson's disease-linked mutations. Proc. Natl. Acad. Sci. USA 102, 2162-2167.
58. Lijnen H. R., (2002) Matrix metalloproteinases and cellular fibrinolytic activity. Biochemistry (Mosc) 67, 92-98.
59. Lijnen H. R., Ugwu F., Bini A., and, Collen D., (1998) Generation of an angiostatin-like fragment from plasminogen by stromelysin-1 (MMP-3). Biochemistry 37, 4699-4702.
60. Matsukawa N., Yasuhara T., Hara K., Xu L., Maki M., Yu G., Kaneko Y., Ojika K., Hess D. C., and, Borlongan C. V., (2009) Therapeutic targets and limits of minocycline neuroprotection in experimental ischemic stroke. BMC Neurosci. 10, 126.
61. 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.
62. Mlekusch R., and, Humpel C., (2009) Matrix metalloproteinases-2 and -3 are reduced in cerebrospinal fluid with low beta-amyloid1-42 levels. Neurosci. Lett. 466, 135-138.
63. Moon M., Kim H. G., Hwang L., et al. (2009) Neuroprotective effect of ghrelin in the 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine mouse model of Parkinson's disease by blocking microglial activation. Neurotox. Res. 15, 332-347.
64. Murphy G., (1995) Matrix metalloproteinases and their inhibitors. Acta Orthop. Scand. Suppl. 266, 55-60 (review).
65. Murphy G., Cockett M. I., Ward R. V., and, Docherty A. J., (1991) Matrix metalloproteinase degradation of elastin, type IV collagen and proteoglycan. A quantitative comparison of the activities of 95 kDa and 72 kDa gelatinases, stromelysins-1 and -2 and punctuated metalloproteinase (PUMP). Biochem. J. 277, 277-279.
66. Nagase H., and, Woessner J.F., Jr, (1999) Matrix metalloproteinases. J. Biol. Chem. 274, 21491-21494 (review).
67. NINDS NET-PD Investigators (2008) A pilot clinical trial of creatine and minocycline in early Parkinson disease: 18-month results. Clin. Neuropharmacol. 31, 141-150.
68. Okada Y., Nagase H., and, Harris E.D., Jr, (1987) Matrix metalloproteinases 1, 2, and 3 from rheumatoid synovial cells are sufficient to destroy joints. J. Rheumatol. 14 Spec No, 41-42.
69. Okada Y., Harris E.D., Jr, and, Nagase H., (1988a) The precursor of a metalloendopeptidase from human rheumatoid synovial fibroblasts. Purification and mechanisms of activation by endopeptidases and 4-aminophenylmercuric acetate. Biochem. J. 254, 731-741.
70. Okada Y., Watanabe S., Nakanishi I., Kishi J., Hayakawa T., Watorek W., Travis J., and, Nagase H., (1988b) Inactivation of tissue inhibitor of metalloproteinases by neutrophil elastase and other serine proteinases. FEBS Lett. 229, 157-160.
71. Okouchi M., Ekshyyan O., Maracine M., and, Aw T.Y., (2007) Neuronal apoptosis in neurodegeneration. Antioxid. Redox Signal. 9, 1059-1096 (review).
72. Overall C. M., and, López-Otín C., (2002) Strategies for MMP inhibition in cancer: innovations for the post-trial era. Nat. Rev. Cancer 2, 657-672 (review).
73. Ozenci V., Rinaldi L., Teleshova N., Matusevicius D., Kivisäkk P., Kouwenhoven M., and, Link H., (1999) Metalloproteinases and their tissue inhibitors in multiple sclerosis. J. Autoimmun. 12, 297-303.
74. Pei D., and, Weiss S. J., (1995) Furin-dependent intracellular activation of the human stromelysin-3 zymogen. Nature 375, 244-247.
75. Pei D., and, Weiss S. J., (1996) Transmembrane-deletion mutants of the membrane-type matrix metalloproteinase-1 process progelatinase A and express intrinsic matrix-degrading activity. J. Biol. Chem. 271, 9135-9140.
76. Polymeropoulos M. H., Lavedan C., Leroy E., et al. (1997) Mutation in the alpha-synuclein gene identified in families with Parkinson's disease. Science 276, 2045-2047.
77. Puerta D. T., Mongan J., Tran B. L., McCammon J. A., and, Cohen S. M., (2005) Potent, selective pyrone-based inhibitors of stromelysin-1. J. Am. Chem. Soc. 127, 14148-14149.
78. Ramsey C. P., and, Giasson B. I., (2008) The E163K DJ-1 mutant shows specific antioxidant deficiency. Brain Res. 1239, 1-11.
79. Reunanen N., Westermarck J., Häkkinen L., Holmström T. H, Elo I., Eriksson J. E., and, Kähäri V. M., (1998) Enhancement of fibroblast collagenase (matrix metalloproteinase-1) gene expression by ceramide is mediated by extracellular signal-regulated and stress-activated protein kinase pathways. J. Biol. Chem. 273, 5137-5145.
80. Rosenberg G. A., Cunningham L. A., and, Wallace J., et al. (2001a) 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.
81. Rosenberg G. A., Sullivan N., and, Esiri M. M., (2001b) White matter damage is associated with matrix metalloproteinases in vascular dementia. Stroke 32, 1162-1168.
82. Saarela M. S., Lehtimäki T., Rinne J. O., Hervonen A., Jylhä M., Röyttä M., Ahonen J. P., and, Mattila K. M., (2004) Interaction between matrix metalloproteinase 3 and the epsilon4 allele of apolipoprotein E increases the risk of Alzheimer's disease in Finns. Neurosci. Lett. 367, 336-339.
83. Saus J., Quinones S., Otani Y., Nagase H., Harris E. D., Jr, and, Kurkinin M., (1988) The complete primary structure of human matrix metalloproteinase-3. Identity with stromelysin. J. Biol. Chem. 263, 6742-6745.
84. Schonbeck U., Mach F., and, Libby P., (1998) Generation of biologically active IL-1 beta by matrix metalloproteinases: a novel caspase-1-independent pathway of IL-1 beta processing. J. Immunol. 161, 3340-3346.
85. Sharrocks A. D., Brown A. L., Ling Y., and, Yates P. R., (1997) The ETS-domain transcription factor family. Int. J. Biochem. Cell Biol. 29, 1371-1387.
86. Spillantini M. G., Crowther R. A., Jakes R., Hasegawa M., and, Goedert M., (1998) α-Synuclein in filamentous inclusions of Lewy bodies from Parkinson's disease and dementia with Lewy bodies. Proc. Natl Acad. Sci. USA 95, 6469-6473. (Pubitemid 28249037)
87. Stomrud E., Björkqvist M., Janciauskiene S., Minthon L., and, Hansson O., (2010) Alterations of matrix metalloproteinases in the healthy elderly with increased risk of prodromal Alzheimer's disease. Alzheimers Res. Ther. 2, 20.
88. 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.
89. Suo Z., Wu M., Ameenuddin S., Anderson H. E., Zoloty J. E., Citron B. A., Andrade-Gordon P., and, Festoff B. W., (2002) Participation of protease-activated receptor-1 in thrombin-induced microglial activation. J. Neurochem. 80, 655-666.
90. Tan H. K., Heywood D., Ralph G. S., Bienemann A., Baker A. H., and, Uney J. B., (2003) Tissue inhibitor of metalloproteinase 1 inhibits excitotoxic cell death in neurons. Mol. Cell Neurosci. 22, 98-106.
91. Tansey M. G., McCoy M. K., and, Frank-Cannon T. C., (2007) Neuroinflammatory mechanisms in Parkinson's disease: potential environmental triggers, pathways, and targets for early therapeutic intervention. Exp. Neurol. 208, 1-25.
92. Tejima E., Guo S., Murata Y., Arai K., Lok J., Van Leyen K., Rosell A., Wang X., and, Lo E. H., (2009) Neuroprotective effects of overexpressing tissue inhibitor of metalloproteinase TIMP-1. J. Neurotrauma 26, 1935-1941.
93. Thorne M., Moore C. S., and, Robertson G. S., (2009) Lack of TIMP-1 increases severity of experimental autoimmune encephalomyelitis: Effects of darbepoetin alfa on TIMP-1 null and wild-type mice. J. Neuroimmunol. 211, 92-100.
94. Tikka T., Fiebich B. L., Goldsteins G., Keinanen R., and, Koistinaho J., (2001) Minocycline, a tetracycline derivative, is neuroprotective against excitotoxicity by inhibiting activation and proliferation of microglia. J. Neurosci. 21, 2580-2588.
95. Ugwu F., Van Hoef B., Bini A., Collen D., and, Lijnen H. R., (1998) Proteolytic cleavage of urokinase-type plasminogen activator by stromelysin-1 (MMP-3). Biochemistry 37, 7231-7236.
96. 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.
97. Vincenti M. P., and, Brinckerhoff C. E., (2002) Transcriptional regulation of collagenase (MMP-1, MMP-13) genes in arthritis: integration of complex signaling pathways for the recruitment of gene-specific transcription factors. Arthritis Res. 4, 157-164.
98. Vu T. K., Hung D. T., Wheaton V. I., and, Coughlin S. R., (1991) Molecular cloning of a functional thrombin receptor reveals a novel proteolytic mechanism of receptor activation. Cell 64, 1057-1068.
99. Walker E. J., and, Rosenberg G. A., (2009) TIMP-3 and MMP-3 contribute to delayed inflammation and hippocampal neuronal death following global ischemia. Exp. Neurol. 216, 122-131.
100. Westermarck J., and, Kahari V. M., (1999) Regulation of matrix metalloproteinase expression in tumor invasion. FASEB J. 13, 781-792 (review).
101. Wetzel M., Rosenberg G. A., and, Cunningham L. A., (2003) Tissue inhibitor of metalloproteinases-3 and matrix metalloproteinase-3 regulate neuronal sensitivity to doxorubicin-induced apoptosis. Eur. J. Neurosci. 18, 1050-1060.
102. White A. R., Du T., Laughton K. M., et al. (2006) Degradation of the Alzheimer disease amyloid beta-peptide by metal-dependent up-regulation of metalloprotease activity. J. Biol. Chem. 281, 17670-17680.
103. Witek-Zawada B., and, Koj A., (2003) Regulation of expression of stromyelysin-1 by proinflammatory cytokines in mouse brain astrocytes. J. Physiol. Pharmacol. 54, 489-496.
104. 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 proinflammatory cytokines and iNOS in microglia. J. Neurochem. 106, 770-780.
105. Wu D. C., Jackson-Lewis V., Vila M., Tieu K., Teismann P., Vadseth C., Choi D. K., Ischiropoulos H., and, Przedborski S., (2002) Blockade of microglial activation is neuroprotective in the 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine mouse model of Parkinson disease. J. Neurosci. 22, 1763-1771.
106. 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 (review).
107. 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.
108. Zhao C., Ling Z., Newman M. B., Bhatia A., and, Carvey P. M., (2007) TNF-alpha knockout and minocycline treatment attenuates blood-brain barrier leakage in MPTP-treated mice. Neurobiol. Dis. 26, 36-46.