Roles of matrix metalloproteinases and their targets in epileptogenesis and seizures

Clinical Psychopharmacology and Neuroscience

Volumn 11, Issue 2, 2013, Pages 45-52

  Mizoguchi, Hiroyuki ^a   Yamada, Kiyofumi ^b  

^a NAGOYA UNIVERSITY   (Japan)

^b NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Epilepsy; Matrix metalloproteinase; Nerve growth factors; Seizure; Tissue inhibitor of metalloproteinase

Indexed keywords

CELL SURFACE PROTEIN; GROWTH FACTOR; MATRIX METALLOPROTEINASE; MATRIX PROTEIN; NEUROTRANSMITTER RECEPTOR; NEUROTROPHIN; SCLEROPROTEIN; TISSUE INHIBITOR OF METALLOPROTEINASE;

CELL ADHESION; CELL SURFACE; ENZYME ACTIVITY; ENZYME BLOOD LEVEL; EPILEPTOGENESIS; EXTRACELLULAR MATRIX; HUMAN; LONG TERM POTENTIATION; MACROMOLECULE; MICROENVIRONMENT; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; NERVOUS TISSUE; NONHUMAN; PATHOGENESIS; PROTEIN EXPRESSION; REGULATORY MECHANISM; REVIEW; SEIZURE; SYNAPTOGENESIS;

EID: 84883610359     PISSN: 17381088     EISSN: 20934327     Source Type: Journal    
DOI: 10.9758/cpn.2013.11.2.45     Document Type: Review

References (65)

1. Yong VW, Power C, Forsyth P, Edwards DR. Metalloproteinases in biology and pathology of the nervous system. Nat Rev Neurosci 2001;2:502-511. (Pubitemid 33676585)
2. Ethell IM, Ethell DW. Matrix metalloproteinases in brain development and remodeling: synaptic functions and targets. J Neurosci Res 2007;85:2813-2823. (Pubitemid 47523564)
3. Sternlicht MD, Werb Z. How matrix metalloproteinases regulate cell behavior. Annu Rev Cell Dev Biol 2001;17:463-516. (Pubitemid 33096184)
4. Mannello F, Gazzanelli G. Tissue inhibitors of metalloproteinases and programmed cell death: conundrums, controversies and potential implications. Apoptosis 2001;6:479-482. (Pubitemid 33078759)
5. Vaillant C, Didier-Bazès M, Hutter A, Belin MF, Thomasset N. Spatiotemporal expression patterns of metalloproteinases and their inhibitors in the postnatal developing rat cerebellum. J Neurosci 1999;19:4994-5004. (Pubitemid 29270134)
6. Dzwonek J, Rylski M, Kaczmarek L. Matrix metalloproteinases and their endogenous inhibitors in neuronal physiology of the adult brain. FEBS Lett 2004;567:129-135. (Pubitemid 38686435)
7. Clark IM, Swingler TE, Sampieri CL, Edwards DR. The regulation of matrix metalloproteinases and their inhibitors. Int J Biochem Cell Biol 2008;40:1362-1378.
8. Rivera S, Tremblay E, Timsit S, Canals O, Ben-Ari Y, Khrestchatisky M. Tissue inhibitor of metalloproteinases-1 (TIMP-1) is differentially induced in neurons and astrocytes after seizures: evidence for developmental, immediate early gene, and lesion response. J Neurosci 1997;17:4223-4235. (Pubitemid 27220613)
9. Nedivi E, Hevroni D, Naot D, Israeli D, Citri Y. Numerous candidate plasticity-related genes revealed by differential cDNA cloning. Nature 1993;363:718-722. (Pubitemid 23227648)
10. Szklarczyk A, Lapinska J, Rylski M, McKay RD, Kaczmarek L. Matrix metalloproteinase-9 undergoes expression and activation during dendritic remodeling in adult hippocampus. J Neurosci 2002;22:920-930. (Pubitemid 34141772)
11. Nagy V, Bozdagi O, Matynia A, Balcerzyk M, Okulski P, Dzwonek J, et al. Matrix metalloproteinase-9 is required for hippocampal late-phase long-term potentiation and memory. J Neurosci 2006;26:1923-1934.
12. Meighan SE, Meighan PC, Choudhury P, Davis CJ, Olson ML, Zornes PA, et al. Effects of extracellular matrix-degrading proteases matrix metalloproteinases 3 and 9 on spatial learning and synaptic plasticity. J Neurochem 2006;96:1227-1241.
13. Mizoguchi H, Ibi D, Takuma K, Toth E, Sato J, Itohara S, et al. Alterations of emotional and cognitive behaviors in matrix metalloproteinase-2 and -9-deficient mice. Open Behav Sci J 2010;4:19-25.
14. Mizoguchi H, Yamada K, Nabeshima T. Matrix metalloproteinases contribute to neuronal dysfunction in animal models of drug dependence, Alzheimer's disease, and epilepsy. Biochem Res Int 2011;681385.
15. Morimoto K, Fahnestock M, Racine RJ. Kindling and status epilepticus models of epilepsy: rewiring the brain. Prog Neurobiol 2004;73:1-60. (Pubitemid 38749090)
16. Wilczynski GM, Konopacki FA, Wilczek E, Lasiecka Z, Gorlewicz A, Michaluk P, et al. Important role of matrix metalloproteinase 9 in epileptogenesis. J Cell Biol 2008;180:1021-1035. (Pubitemid 351398426)
17. Zeng LH, Xu L, Rensing NR, Sinatra PM, Rothman SM, Wong M. Kainate seizures cause acute dendritic injury and actin depolymerization in vivo. J Neurosci 2007;27:11604-11613. (Pubitemid 350006913)
18. Suenaga N, Ichiyama T, Kubota M, Isumi H, Tohyama J, Furukawa S. Roles of matrix metalloproteinase-9 and tissue inhibitors of metalloproteinases 1 in acute encephalopathy following prolonged febrile seizures. J Neurol Sci 2008; 266:126-130. (Pubitemid 351186532)
19. Li S, Yu S, Zhang C, Shu H, Liu S, An N, et al. Increased expression of matrix metalloproteinase 9 in cortical lesions from patients with focal cortical dysplasia type IIb and tuberous sclerosis complex. Brain Res 2012;1453:46-55.
20. Leppert D, Leib SL, Grygar C, Miller KM, Schaad UB, Holländer GA. Matrix metalloproteinase (MMP)-8 and MMP-9 in cerebrospinal fluid during bacterial meningitis: association with blood-brain barrier damage and neurological sequelae. Clin Infect Dis 2000;31:80-84. (Pubitemid 32268943)
21. Heuser K, Hoddevik EH, Taubøll E, Gjerstad L, Indahl U, Kaczmarek L, et al. Temporal lobe epilepsy and matrix metalloproteinase 9: a tempting relation but negative genetic association. Seizure 2010;19:335-338.
22. Rylski M, Amborska R, Zybura K, Michaluk P, Bielinska B, Konopacki FA, et al. JunB is a repressor of MMP-9 transcription in depolarized rat brain neurons. Mol Cell Neurosci 2009;40:98-110.
23. Konopacki FA, Rylski M, Wilczek E, Amborska R, Detka D, Kaczmarek L, et al. Synaptic localization of seizure-induced matrix metalloproteinase-9 mRNA. Neuroscience 2007;150:31-39. (Pubitemid 350198686)
24. Le AP, Friedman WJ. Matrix metalloproteinase-7 regulates cleavage of pro-nerve growth factor and is neuroprotective following kainic acid-induced seizures. J Neurosci 2012;32:703-712.
25. Stein VM, Genini S, Puff C, Baumgärtner W, Tipold A. Seizure activity in dogs is associated with enhanced TIMP-2 expression of microglia. Vet Immunol Immunopathol 2012;146:101-105.
26. Wright JW, Harding JW. The brain angiotensin system and extracellular matrix molecules in neural plasticity, learning, and memory. Prog Neurobiol 2004;72:263-293. (Pubitemid 38609580)
27. Zhang JW, Deb S, Gottschall PE. Regional and differential expression of gelatinases in rat brain after systemic kainic acid or bicuculline administration. Eur J Neurosci 1998;10:3358-3368.
28. Kim GW, Kim HJ, Cho KJ, Kim HW, Cho YJ, Lee BI. The role of MMP-9 in integrin-mediated hippocampal cell death after pilocarpine-induced status epilepticus. Neurobiol Dis 2009;36:169-180.
29. Goddard GV, McIntyre DC, Leech CK. A permanent change in brain function resulting from daily electrical stimulation. Exp Neurol 1969;25:295-330.
30. Racine RJ. Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr Clin Neurophysiol 1972;32:281-294.
31. Pinel JP, Rovner LI. Electrode placement and kindling-induced experimental epilepsy. Exp Neurol 1978;58:335-346. (Pubitemid 8268486)
32. Sutula T, He XX, Cavazos J, Scott G. Synaptic reorganization in the hippocampus induced by abnormal functional activity. Science 1988;239:1147-1150. (Pubitemid 18084325)
33. Cavazos JE, Golarai G, Sutula TP. Mossy fiber synaptic reorganization induced by kindling: time course of development, progression, and permanence. J Neurosci 1991;11:2795-2803.
34. Cavazos JE, Das I, Sutula TP. Neuronal loss induced in limbic pathways by kindling: evidence for induction of hippocampal sclerosis by repeated brief seizures. J Neurosci 1994;14:3106-3121. (Pubitemid 24138997)
35. Mizoguchi H, Nakade J, Tachibana M, Ibi D, Someya E, Koike H, et al. Matrix metalloproteinase-9 contributes to kindled seizure development in pentylenetetrazole-treated mice by converting pro-BDNF to mature BDNF in the hippocampus. J Neurosci 2011;31:12963-12971.
36. Girgenti MJ, Collier E, Sathyanesan M, Su XW, Newton SS. Characterization of electroconvulsive seizure-induced TIMP-1 and MMP-9 in hippocampal vasculature. Int J Neuropsychopharmacol 2011;14:535-544.
37. Takács E, Nyilas R, Szepesi Z, Baracskay P, Karlsen B, Røsvold T, et al. Matrix metalloproteinase-9 activity increased by two different types of epileptic seizures that do not induce neuronal death: a possible role in homeostatic synaptic plasticity. Neurochem Int 2010;56:799-809.
38. Jourquin J, Tremblay E, Dé canis N, Charton G, Hanessian S, Chollet AM, et al. Neuronal activity-dependent increase of net matrix metalloproteinase activity is associated with MMP-9 neurotoxicity after kainate. Eur J Neurosci 2003;18:1507-1517. (Pubitemid 37215104)
39. Hoehna Y, Uckermann O, Luksch H, Stefovska V, Marzahn J, Theil M, et al. Matrix metalloproteinase 9 regulates cell death following pilocarpine-induced seizures in the developing brain. Neurobiol Dis 2012;48:339-347.
40. Ben-Ari Y, Tremblay E, Riche D, Ghilini G, Naquet R. Electrographic, clinical and pathological alterations following systemic administration of kainic acid, bicuculline or pentetrazole: metabolic mapping using the deoxyglucose method with special reference to the pathology of epilepsy. Neuroscience 1981;6:1361-1391. (Pubitemid 11074864)
41. Parent JM, Yu TW, Leibowitz RT, Geschwind DH, Sloviter RS, Lowenstein DH. Dentate granule cell neurogenesis is increased by seizures and contributes to aberrant network reorganization in the adult rat hippocampus. J Neurosci 1997;17:3727-3738. (Pubitemid 27200597)
42. Bengzon J, Kokaia Z, Elmér E, Nanobashvili A, Kokaia M, Lindvall O. Apoptosis and proliferation of dentate gyrus neurons after single and intermittent limbic seizures. Proc Natl Acad Sci USA 1997;94:10432-10437.
43. Buga AM, Vintilescu R, Balseanu AT, Pop OT, Streba C, Toescu E, et al. Repeated PTZ treatment at 25-day intervals leads to a highly efficient accumulation of doublecortin in the dorsal hippocampus of rats. PLoS One 2012;7:e39302.
44. Gray WP, Sundstrom LE. Kainic acid increases the proliferation of granule cell progenitors in the dentate gyrus of the adult rat. Brain Res 1998;790:52-59. (Pubitemid 28234487)
45. Yang F, Wang JC, Han JL, Zhao G, Jiang W. Different effects of mild and severe seizures on hippocampal neurogenesis in adult rats. Hippocampus 2008;18:460-468. (Pubitemid 351671405)
46. Hung YW, Yang DI, Huang PY, Lee TS, Kuo TB, Yiu CH, et al. The duration of sustained convulsive seizures determines the pattern of hippocampal neurogenesis and the development of spontaneous epilepsy in rats. Epilepsy Res 2012;98:206-215.
47. Wang L, Zhang ZG, Zhang RL, Gregg SR, Hozeska-Solgot A, LeTourneau Y, et al. Matrix metalloproteinase 2 (MMP2) and MMP9 secreted by erythropoietin- activated endothelial cells promote neural progenitor cell migration. J Neurosci 2006;26:5996-6003. (Pubitemid 44318365)
48. Benekareddy M, Mehrotra P, Kulkarni VA, Ramakrishnan P, Dias BG, Vaidya VA. Antidepressant treatments regulate matrix metalloproteinases-2 and -9 (MMP-2/MMP-9) and tissue inhibitors of the metalloproteinases (TIMPS 1-4) in the adult rat hippocampus. Synapse 2008;62:590-600. (Pubitemid 351951297)
49. Cabelli RJ, Hohn A, Shatz CJ. Inhibition of ocular dominance column formation by infusion of NT-4/5 or BDNF. Science 1995;267:1662-1666.
50. Horch HW, Krü ttgen A, Portbury SD, Katz LC. Destabilization of cortical dendrites and spines by BDNF. Neuron 1999;23:353-364. (Pubitemid 29315729)
51. Nagappan G, Zaitsev E, Senatorov VV Jr, Yang J, Hempstead BL, Lu B. Control of extracellular cleavage of ProBDNF by high frequency neuronal activity. Proc Natl Acad Sci USA 2009;106:1267-1272.
52. Lee R, Kermani P, Teng KK, Hempstead BL. Regulation of cell survival by secreted proneurotrophins. Science 2001;294:1945-1948. (Pubitemid 33101595)
53. Hwang JJ, Park MH, Choi SY, Koh JY. Activation of the Trk signaling pathway by extracellular zinc. Role of metalloproteinases. J Biol Chem 2005;280:11995-12001.
54. Koyama R, Yamada MK, Fujisawa S, Katoh-Semba R, Matsuki N, Ikegaya Y. Brain-derived neurotrophic factor induces hyperexcitable reentrant circuits in the dentate gyrus. J Neurosci 2004;24:7215-7224. (Pubitemid 39100691)
55. Bilousova TV, Rusakov DA, Ethell DW, Ethell IM. Matrix metalloproteinase-7 disrupts dendritic spines in hippocampal neurons through NMDA receptor activation. J Neurochem 2006;97:44-56.
56. Gu Z, Cui J, Brown S, Fridman R, Mobashery S, Strongin AY, et al. A highly specific inhibitor of matrix metalloproteinase-9 rescues laminin from proteolysis and neurons from apoptosis in transient focal cerebral ischemia. J Neurosci 2005;25:6401-6408. (Pubitemid 40962536)
57. Michaluk P, Kolodziej L, Mioduszewska B, Wilczynski GM, Dzwonek J, Jaworski J, et al. Beta-dystroglycan as a target for MMP-9, in response to enhanced neuronal activity. J Biol Chem 2007;282:16036-16041. (Pubitemid 47100368)
58. Hübschmann MV, Skladchikova G, Bock E, Berezin V. Neural cell adhesion molecule function is regulated by metalloproteinase-mediated ectodomain release. J Neurosci Res 2005;80:826-837.
59. Oray S, Majewska A, Sur M. Dendritic spine dynamics are regulated by monocular deprivation and extracellular matrix degradation. Neuron 2004;44:1021-1030. (Pubitemid 39643097)
60. Wu YP, Siao CJ, Lu W, Sung TC, Frohman MA, Milev P, et al. The tissue plasminogen activator (tPA)/plasmin extracellular proteolytic system regulates seizure-induced hippocampal mossy fiber outgrowth through a proteoglycan substrate. J Cell Biol 2000;148:1295-1304.
61. Dziembowska M, Milek J, Janusz A, Rejmak E, Romanowska E, Gorkiewicz T, et al. Activity-dependent local translation of matrix metalloproteinase-9. J Neurosci 2012;32:14538-14547.
62. Bouchard V, Demers MJ, Thibodeau S, Laquerre V, Fujita N, Tsuruo T, et al. Fak/Src signaling in human intestinal epithelial cell survival and anoikis: differentiation state-specific uncoupling with the PI3-K/Akt-1 and MEK/Erk pathways. J Cell Physiol 2007;212:717-728. (Pubitemid 47271883)
63. Pankov R, Cukierman E, Clark K, Matsumoto K, Hahn C, Poulin B, et al. Specific beta1 integrin site selectively regulates Akt/protein kinase B signaling via local activation of protein phosphatase 2A. J Biol Chem 2003;278:18671-18681. (Pubitemid 36799495)
64. Lee SR, Lo EH. Induction of caspase-mediated cell death by matrix metalloproteinases in cerebral endothelial cells after hypoxia-reoxygenation. J Cereb Blood Flow Metab 2004;24:720-727. (Pubitemid 38880217)
65. Levkau B, Kenagy RD, Karsan A, Weitkamp B, Clowes AW, Ross R, et al. Activation of metalloproteinases and their association with integrins: an auxiliary apoptotic pathway in human endothelial cells. Cell Death Differ 2002;9:1360-1367. (Pubitemid 36097706)