Table of Contents Author Guidelines Submit a Manuscript
Biochemistry Research International
Volume 2011, Article ID 681385, 10 pages
http://dx.doi.org/10.1155/2011/681385
Review Article

Matrix Metalloproteinases Contribute to Neuronal Dysfunction in Animal Models of Drug Dependence, Alzheimer's Disease, and Epilepsy

1Futuristic Environmental Simulation Center, Research Institute of Environmental Medicine, Nagoya University, Nagoya 464-8601, Japan
2Department of Neuropsychopharmacology and Hospital Pharmacy, Nagoya University Graduate School of Medicine, Nagoya 466-8560, Japan
3Department of Chemical Pharmacology, Meijo University Graduate School of Pharmaceutical Sciences, Nagoya 468-8503, Japan
4Comparative Cognitive Science Institutes, Meijo University, Nagoya 468-8503, Japan

Received 25 August 2011; Accepted 17 November 2011

Academic Editor: Fengyu Song

Copyright © 2011 Hiroyuki Mizoguchi et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. V. W. Yong, C. Power, P. Forsyth, and D. R. Edwards, “Metalloproteinases in biology and pathology of the nervous system,” Nature Reviews Neuroscience, vol. 2, no. 7, pp. 502–511, 2001. View at Publisher · View at Google Scholar · View at Scopus
  2. I. M. Ethell and D. W. Ethell, “Matrix metalloproteinases in brain development and remodeling: synaptic functions and targets,” Journal of Neuroscience Research, vol. 85, no. 13, pp. 2813–2823, 2007. View at Publisher · View at Google Scholar · View at Scopus
  3. M. D. Sternlicht and Z. Werb, “How matrix metalloproteinases regulate cell behavior,” Annual Review of Cell and Developmental Biology, vol. 17, pp. 463–516, 2001. View at Publisher · View at Google Scholar · View at Scopus
  4. F. Mannello and G. Gazzanelli, “Tissue inhibitors of metalloproteinases and programmed cell death: conundrums, controversies and potential implications,” Apoptosis, vol. 6, no. 6, pp. 479–482, 2001. View at Publisher · View at Google Scholar · View at Scopus
  5. C. Vaillant, M. Didier-Bazès, A. Hutter, M. F. Belin, and N. Thomasset, “Spatiotemporal expression patterns of metalloproteinases and their inhibitors in the postnatal developing rat cerebellum,” Journal of Neuroscience, vol. 19, no. 12, pp. 4994–5004, 1999. View at Google Scholar · View at Scopus
  6. J. Dzwonek, M. Rylski, and L. Kaczmarek, “Matrix metalloproteinases and their endogenous inhibitors in neuronal physiology of the adult brain,” FEBS Letters, vol. 567, no. 1, pp. 129–135, 2004. View at Publisher · View at Google Scholar · View at Scopus
  7. J. W. Wright, J. R. Reichert, C. J. Davis, and J. W. Harding, “Neural plasticity and the brain renin-angiotensin system,” Neuroscience and Biobehavioral Reviews, vol. 26, no. 5, pp. 529–552, 2002. View at Publisher · View at Google Scholar · View at Scopus
  8. S. Rivera, E. Tremblay, S. Timsit, O. Canals, Y. Ben-Ari, and M. Khrestchatisky, “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,” Journal of Neuroscience, vol. 17, no. 11, pp. 4223–4235, 1997. View at Google Scholar · View at Scopus
  9. E. Nedivi, D. Hevroni, D. Naot, D. Israell, and Y. Citri, “Numerous candidate plasticity-related genes revealed by differential cDNA cloning,” Nature, vol. 363, no. 6431, pp. 718–722, 1993. View at Publisher · View at Google Scholar · View at Scopus
  10. A. Szklarczyk, J. Lapinska, M. Rylski, R. D. G. McKay, and L. Kaczmarek, “Matrix metalloproteinase-9 undergoes expression and activation during dendritic remodeling in adult hippocampus,” Journal of Neuroscience, vol. 22, no. 3, pp. 920–930, 2002. View at Google Scholar · View at Scopus
  11. V. Nagy, O. Bozdagi, A. Matynia et al., “Matrix metalloproteinase-9 is required for hippocampal late-phase long-term potentiation and memory,” Journal of Neuroscience, vol. 26, no. 7, pp. 1923–1934, 2006. View at Publisher · View at Google Scholar · View at Scopus
  12. P. Okulski, T. M. Jay, J. Jaworski et al., “TIMP-1 abolishes MMP-9-dependent long-lasting long-term potentiation in the prefrontal cortex,” Biological Psychiatry, vol. 62, no. 4, pp. 359–362, 2007. View at Publisher · View at Google Scholar · View at Scopus
  13. T. E. Brown, A. R. Wilson, D. L. Cocking, and B. A. Sorg, “Inhibition of matrix metalloproteinase activity disrupts reconsolidation but not consolidation of a fear memory,” Neurobiology of Learning and Memory, vol. 91, no. 1, pp. 66–72, 2009. View at Publisher · View at Google Scholar · View at Scopus
  14. J. W. Wright, T. E. Brown, and J. W. Harding, “Inhibition of hippocampal matrix metalloproteinase-3 and -9 disrupts spatial memory,” Neural Plasticity, vol. 2007, Article ID 73813, 2007. View at Publisher · View at Google Scholar · View at Scopus
  15. S. E. Meighan, P. C. Meighan, P. Choudhury et al., “Effects of extracellular matrix-degrading proteases matrix metalloproteinases 3 and 9 on spatial learning and synaptic plasticity,” Journal of Neurochemistry, vol. 96, no. 5, pp. 1227–1241, 2006. View at Publisher · View at Google Scholar · View at Scopus
  16. F. A. Chaillan, S. Rivera, E. Marchetti et al., “Involvement of tissue inhibition of metalloproteinases-1 in learning and memory in mice,” Behavioural Brain Research, vol. 173, no. 2, pp. 191–198, 2006. View at Publisher · View at Google Scholar · View at Scopus
  17. R. Pawlak, A. M. Magarinos, J. Melchor, B. McEwen, and S. Strickland, “Tissue plasminogen activator in the amygdala is critical for stress-induced anxiety-like behavior,” Nature Neuroscience, vol. 6, no. 2, pp. 168–174, 2003. View at Publisher · View at Google Scholar · View at Scopus
  18. T. Matys, R. Pawlak, E. Matys, C. Pavlides, B. S. McEwen, and S. Strickland, “Tissue plasminogen activator promotes the effects of corticotropin- releasing factor on the amygdala and anxiety-like behavior,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 46, pp. 16345–16350, 2004. View at Publisher · View at Google Scholar · View at Scopus
  19. P. Michaluk, L. Mikasova, L. Groc, R. Frischknecht, D. Choquet, and L. Kaczmarek, “Matrix metalloproteinase-9 controls NMDA receptor surface diffusion through integrin β1 signaling,” Journal of Neuroscience, vol. 29, no. 18, pp. 6007–6012, 2009. View at Publisher · View at Google Scholar · View at Scopus
  20. C. Barkus, S. B. McHugh, R. Sprengel, P. H. Seeburg, J. N. P. Rawlins, and D. M. Bannerman, “Hippocampal NMDA receptors and anxiety: at the interface between cognition and emotion,” European Journal of Pharmacology, vol. 626, no. 1, pp. 49–56, 2010. View at Publisher · View at Google Scholar · View at Scopus
  21. H. Mizoguchi, D. Ibi, K. Takuma et al., “Alterations of emotional and cognitive behaviors in matrix metalloproteinase-2 and -9-deficient mice,” Open Behavioral Science Journal, vol. 4, pp. 19–25, 2010. View at Google Scholar
  22. D. Sulzer, “How addictive drugs disrupt presynaptic dopamine neurotransmission,” Neuron, vol. 69, no. 4, pp. 628–649, 2011. View at Publisher · View at Google Scholar
  23. M. S. Bowers, B. T. Chen, and A. Bonci, “AMPA receptor synaptic plasticity induced by psychostimulants: the past, present, and therapeutic future,” Neuron, vol. 67, no. 1, pp. 11–24, 2010. View at Publisher · View at Google Scholar · View at Scopus
  24. K. M. Grant, T. D. LeVan, S. M. Wells et al., “Methamphetamine-associated psychosis,” Journal of Neuroimmune Pharmacology. In press. View at Publisher · View at Google Scholar
  25. H. Kamei, T. Nagai, H. Nakano et al., “Repeated methamphetamine treatment impairs recognition memory through a failure of novelty-induced ERK1/2 activation in the prefrontal cortex of mice,” Biological Psychiatry, vol. 59, no. 1, pp. 75–84, 2006. View at Publisher · View at Google Scholar · View at Scopus
  26. H. Mizoguchi, K. Takuma, A. Fukakusa et al., “Improvement by minocycline of methamphetamine-induced impairment of recognition memory in mice,” Psychopharmacology, vol. 196, no. 2, pp. 233–241, 2008. View at Publisher · View at Google Scholar · View at Scopus
  27. A. Nakajima, K. Yamada, T. Nagai et al., “Role of tumor necrosis factor-α in methamphetamine-induced drug dependence and neurotoxicity,” Journal of Neuroscience, vol. 24, no. 9, pp. 2212–2225, 2004. View at Publisher · View at Google Scholar · View at Scopus
  28. H. Mizoguchi, K. Yamada, M. Mizuno et al., “Regulations of methamphetamine reward by extracellular signal-regulated kinase 1/2/ets-like gene-1 signaling pathway via the activation of dopamine receptors,” Molecular Pharmacology, vol. 65, no. 5, pp. 1293–1301, 2004. View at Publisher · View at Google Scholar · View at Scopus
  29. T. E. Robinson and B. Kolb, “Persistent structural modifications in nucleus accumbens and prefrontal cortex neurons produced by previous experience with amphetamine,” Journal of Neuroscience, vol. 17, no. 21, pp. 8491–8497, 1997. View at Google Scholar · View at Scopus
  30. E. J. Nestler, “Molecular basis of long-term plasticity underlying addiction,” Nature Reviews Neuroscience, vol. 2, no. 2, pp. 119–128, 2001. View at Publisher · View at Google Scholar · View at Scopus
  31. K. Yamada and T. Nabeshima, “Endogenous modulators for drug dependence,” Biological and Pharmaceutical Bulletin, vol. 31, no. 9, pp. 1635–1638, 2008. View at Publisher · View at Google Scholar · View at Scopus
  32. H. Mizoguchi, K. Yamada, A. Mouri et al., “Role of matrix metalloproteinase and tissue inhibitor of MMP in methamphetamine-induced behavioral sensitization and reward: implications for dopamine receptor down-regulation and dopamine release,” Journal of Neurochemistry, vol. 102, no. 5, pp. 1548–1560, 2007. View at Publisher · View at Google Scholar · View at Scopus
  33. H. Mizoguchi, K. Yamada, M. Niwa et al., “Reduction of methamphetamine-induced sensitization and reward in matrix metalloproteinase-2 and -9-deficient mice,” Journal of Neurochemistry, vol. 100, no. 6, pp. 1579–1588, 2007. View at Publisher · View at Google Scholar · View at Scopus
  34. H. Mizoguchi, K. Yamada, and T. Nabeshima, “Neuropsychotoxicity of abused drugs: involvement of matrix metalloproteinase-2 and -9 and tissue inhibitor of matrix metalloproteinase-2 in methamphetamine-induced behavioral sensitization and reward in rodents,” Journal of Pharmacological Sciences, vol. 106, no. 1, pp. 9–14, 2008. View at Publisher · View at Google Scholar · View at Scopus
  35. C. Vaillant, M. Didier-Bazès, A. Hutter, M. F. Belin, and N. Thomasset, “Spatiotemporal expression patterns of metalloproteinases and their inhibitors in the postnatal developing rat cerebellum,” Journal of Neuroscience, vol. 19, no. 12, pp. 4994–5004, 1999. View at Google Scholar · View at Scopus
  36. T. M. Reeves, M. L. Prins, J. Zhu, J. T. Povlishock, and L. L. Phillips, “Matrix metalloproteinase inhibition alters functional and structural correlates of deafferentation-induced sprouting in the dentate gyrus,” Journal of Neuroscience, vol. 23, no. 32, pp. 10182–10189, 2003. View at Google Scholar · View at Scopus
  37. T. E. Brown, M. R. Forquer, D. L. Cocking, H. T. Jansen, J. W. Harding, and B. A. Sorg, “Role of matrix metalloproteinases in the acquisition and reconsolidation of cocaine-induced conditioned place preference,” Learning and Memory, vol. 14, no. 3, pp. 214–223, 2007. View at Publisher · View at Google Scholar · View at Scopus
  38. T. E. Brown, M. R. Forquer, J. W. Harding, J. W. Wright, and B. A. Sorg, “Increase in matrix metalloproteinase-9 levels in the rat medial prefrontal cortex after cocaine reinstatement of conditioned place preference,” Synapse, vol. 62, no. 12, pp. 886–889, 2008. View at Publisher · View at Google Scholar · View at Scopus
  39. P. Sillanaukee, A. Kalela, K. Seppä, M. Höyhtyä, and S. T. Nikkari, “Matrix metalloproteinase-9 is elevated in serum of alcohol abusers,” European Journal of Clinical Investigation, vol. 32, no. 4, pp. 225–229, 2002. View at Publisher · View at Google Scholar · View at Scopus
  40. J. Haorah, K. Schall, S. H. Ramirez, and Y. Persidsky, “Activation of protein tyrosine kinases and matrix metalloproteinases causes blood-brain barrier injury: novel mechanism for neurodegeneration associated with alcohol abuse,” GLIA, vol. 56, no. 1, pp. 78–88, 2008. View at Publisher · View at Google Scholar · View at Scopus
  41. A. W. Smith, K. A. Nealey, J. W. Wright, and B. M. Walker, “Plasticity associated with escalated operant ethanol self-administration during acute withdrawal in ethanol-dependent rats requires intact matrix metalloproteinase systems,” Neurobiology of Learning and Memory, vol. 96, no. 2, pp. 199–206, 2011. View at Publisher · View at Google Scholar
  42. Y. Liu, S. Brown, J. Shaikh, J. A. Fishback, and R. R. Matsumoto, “Relationship between methamphetamine exposure and matrix metalloproteinase 9 expression,” NeuroReport, vol. 19, no. 14, pp. 1407–1409, 2008. View at Publisher · View at Google Scholar · View at Scopus
  43. K. Conant, I. Lonskaya, A. Szklarczyk et al., “Methamphetamine-associated cleavage of the synaptic adhesion molecule intercellular adhesion molecule-5,” Journal of Neurochemistry, vol. 118, no. 4, pp. 521–532, 2011. View at Publisher · View at Google Scholar
  44. D. Sulzer, T. K. Chen, Y. Y. Lau, H. Kristensen, S. Rayport, and A. Ewing, “Amphetamine redistributes dopamine from synaptic vesicles to the cytosol and promotes reverse transport,” Journal of Neuroscience, vol. 15, no. 5, pp. 4102–4108, 1995. View at Google Scholar · View at Scopus
  45. T. Nagai, Y. Noda, K. Ishikawa et al., “The role of tissue plasminogen activator in methamphetamine-related reward and sensitization,” Journal of Neurochemistry, vol. 92, no. 3, pp. 660–667, 2005. View at Publisher · View at Google Scholar · View at Scopus
  46. H. Khoshbouei, N. Sen, B. Guptaroy et al., “N-terminal phosphorylation of the dopamine transporter is required for amphetamine-induced efflux,” PLoS Biology, vol. 2, no. 3, pp. 387–393, 2004. View at Publisher · View at Google Scholar · View at Scopus
  47. R. Z. Goldstein and N. D. Volkow, “Drug addiction and its underlying neurobiological basis: neuroimaging evidence for the involvement of the frontal cortex,” American Journal of Psychiatry, vol. 159, no. 10, pp. 1642–1652, 2002. View at Publisher · View at Google Scholar · View at Scopus
  48. M. S. Bowers, K. McFarland, R. W. Lake et al., “Activator of G protein signaling 3: a gatekeeper of cocaine sensitization and drug seeking,” Neuron, vol. 42, no. 2, pp. 269–281, 2004. View at Publisher · View at Google Scholar · View at Scopus
  49. J. F. Bowyer and N. Weiner, “Modulation of the Ca++-evoked release of [3H]dopamine from striatal synaptosomes by dopamine (D2) agonists and antagonists,” Journal of Pharmacology and Experimental Therapeutics, vol. 241, no. 1, pp. 27–33, 1987. View at Google Scholar · View at Scopus
  50. N. Lindgren, Z. Q. D. Xu, M. Herrera-Marschitz, J. Haycock, T. Hökfelt, and G. Fisone, “Dopamine D2 receptors regulate tyrosine hydroxylase activity and phosphorylation at Ser40 in rat striatum,” European Journal of Neuroscience, vol. 13, no. 4, pp. 773–780, 2001. View at Publisher · View at Google Scholar · View at Scopus
  51. A. M. Palmer, “Neuroprotective therapeutics for Alzheimers disease: progress and prospects,” Trends in Pharmacological Sciences, vol. 32, no. 3, pp. 141–147, 2011. View at Publisher · View at Google Scholar
  52. K. Yamada and T. Nabeshima, “Animal models of Alzheimer's disease and evaluation of anti-dementia drugs,” Pharmacology and Therapeutics, vol. 88, no. 2, pp. 93–113, 2000. View at Publisher · View at Google Scholar · View at Scopus
  53. K. Takuma, S. S. Yan, D. M. Stern, and K. Yamada, “Mitochondrial dysfunction, endoplasmic reticulum stress, and apoptosis in Alzheimer's disease,” Journal of Pharmacological Sciences, vol. 97, no. 3, pp. 312–316, 2005. View at Publisher · View at Google Scholar · View at Scopus
  54. K. Takuma, F. Fang, W. Zhang et al., “RAGE-mediated signaling contributes to intraneuronal transport of amyloid-β and neuronal dysfunction,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 47, pp. 20021–20026, 2009. View at Publisher · View at Google Scholar · View at Scopus
  55. K. Yamada, M. Takayanagi, H. Kamei et al., “Effects of memantine and donepezil on amyloid β-induced memory impairment in a delayed-matching to position task in rats,” Behavioural Brain Research, vol. 162, no. 2, pp. 191–199, 2005. View at Publisher · View at Google Scholar
  56. D. Wang, Y. Noda, Y. Zhou et al., “The allosteric potentiation of nicotinic acetylcholine receptors by galantamine ameliorates the cognitive dysfunction in beta amyloid 25–35 I.c.v.-injected mice: involvement of dopaminergic systems,” Neuropsychopharmacology, vol. 32, no. 6, pp. 1261–1271, 2007. View at Publisher · View at Google Scholar · View at Scopus
  57. T. Alkam, A. Nitta, H. Mizoguchi, A. Itoh, and T. Nabeshima, “A natural scavenger of peroxynitrites, rosmarinic acid, protects against impairment of memory induced by Aβ25–35,” Behavioural Brain Research, vol. 180, no. 2, pp. 139–145, 2007. View at Publisher · View at Google Scholar · View at Scopus
  58. M. H. Tran, K. Yamada, A. Olariu, M. Mizuno, X. H. Ren, and T. Nabeshima, “Amyloid beta-peptide induces nitric oxide production in rat hippocampus: association with cholinergic dysfunction and amelioration by inducible nitric oxide synthase inhibitors,” The FASEB Journal, vol. 15, no. 8, pp. 1407–1409, 2001. View at Google Scholar · View at Scopus
  59. K. Yamada, T. Tanaka, D. Han, K. Senzaki, T. Kameyama, and T. Nabeshima, “Protectiye effects of idebenone and α-tocopherol on β-amyloid-(1-42)-induced learning and memory deficits in rats: implication of oxidative stress in β-amyloid-induced neurotoxicity in vivo,” European Journal of Neuroscience, vol. 11, no. 1, pp. 83–90, 1999. View at Google Scholar
  60. C. Zussy, A. Brureau, B. Delair et al., “Time-course and regional analyses of the physiopathological changes induced after cerebral injection of an amyloid β fragment in rats,” American Journal of Pathology, vol. 179, no. 1, pp. 315–334, 2011. View at Publisher · View at Google Scholar
  61. T. Malm, M. Ort, L. Tähtivaara et al., “β-amyloid infusion results in delayed and age-dependent learning deficits without role of inflammation or β-amyloid deposits,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 23, pp. 8852–8857, 2006. View at Publisher · View at Google Scholar · View at Scopus
  62. J. R. Backstrom, G. P. Lim, M. J. Cullen, and Z. A. Tökés, “Matrix metalloproteinase-9 (MMP-9) is synthesized in neurons of the human hippocampus and is capable of degrading the amyloid-β peptide (1–40),” Journal of Neuroscience, vol. 16, no. 24, pp. 7910–7919, 1996. View at Google Scholar · View at Scopus
  63. J. R. Backstrom, C. A. Miller, and Z. A. Tokes, “Characterization of neutral proteinases from Alzheimer-affected and control brain specimens: identification of calcium-dependent metalloproteinases from the hippocampus,” Journal of Neurochemistry, vol. 58, no. 3, pp. 983–992, 1992. View at Google Scholar · View at Scopus
  64. S. Baig, P. G. Kehoe, and S. Love, “MMP-2, -3 and -9 levels and activity are not related to Aβ load in the frontal cortex in Alzheimer's disease,” Neuropathology and Applied Neurobiology, vol. 34, no. 2, pp. 205–215, 2008. View at Publisher · View at Google Scholar
  65. M. Asahina, Y. Yoshiyama, and T. Hattori, “Expression of matrix metalloproteinase-9 and urinary-type plasminogen activator in Alzheimer's disease brain,” Clinical Neuropathology, vol. 20, no. 2, pp. 60–63, 2001. View at Google Scholar · View at Scopus
  66. S. Deb and P. E. Gottschall, “Increased production of matrix metalloproteinases in enriched astrocyte and mixed hippocampal cultures treated with β-amyloid peptides,” Journal of Neurochemistry, vol. 66, no. 4, pp. 1641–1647, 1996. View at Google Scholar · View at Scopus
  67. P. Yan, X. Hu, H. Song et al., “Matrix metalloproteinase-9 degrades amyloid-β fibrils in vitro and compact plaques in situ,” Journal of Biological Chemistry, vol. 281, no. 34, pp. 24566–24574, 2006. View at Publisher · View at Google Scholar · View at Scopus
  68. S. Deb, J. W. Zhang, and P. E. Gottschall, “β-amyloid induces the production of active, matrix-degrading proteases in cultured rat astrocytes,” Brain Research, vol. 970, no. 1-2, pp. 205–213, 2003. View at Publisher · View at Google Scholar · View at Scopus
  69. E. M. Muir, K. H. Adcock, D. A. Morgenstern et al., “Matrix metalloproteases and their inhibitors are produced by overlapping populations of activated astrocytes,” Molecular Brain Research, vol. 100, no. 1-2, pp. 103–117, 2002. View at Publisher · View at Google Scholar · View at Scopus
  70. H. Mizoguchi, K. Takuma, E. Fukuzaki et al., “Matrix metalloprotease-9 inhibition improves amyloid β-mediated cognitive impairment and neurotoxicity in mice,” Journal of Pharmacology and Experimental Therapeutics, vol. 331, no. 1, pp. 14–22, 2009. View at Publisher · View at Google Scholar · View at Scopus
  71. J. Jourquin, E. Tremblay, N. Décanis et al., “Neuronal activity-dependent increase of net matrix metalloproteinase activity is associated with MMP-9 neurotoxicity after kainate,” European Journal of Neuroscience, vol. 18, no. 6, pp. 1507–1517, 2003. View at Publisher · View at Google Scholar · View at Scopus
  72. Y. Tamura, F. Watanabe, T. Nakatani et al., “Highly selective and orally active inhibitors of type IV collagenase (MMP-9 and MMP-2): N-sulfonylamino acid derivatives,” Journal of Medicinal Chemistry, vol. 41, no. 4, pp. 640–649, 1998. View at Publisher · View at Google Scholar · View at Scopus
  73. L. H. Zeng, L. Xu, N. R. Rensing, P. M. Sinatra, S. M. Rothman, and M. Wong, “Kainate seizures cause acute dendritic injury and actin depolymerization in vivo,” Journal of Neuroscience, vol. 27, no. 43, pp. 11604–11613, 2007. View at Publisher · View at Google Scholar · View at Scopus
  74. M. Kokaia, “Seizure-induced neurogenesis in the adult brain,” European Journal of Neuroscience, vol. 33, no. 6, pp. 1133–1138, 2011. View at Publisher · View at Google Scholar
  75. D. Han, K. Yamada, K. Senzaki, H. Xiong, H. Nawa, and T. Nabeshima, “Involvement of nitric oxide in pentylenetetrazole-induced kindling in rats,” Journal of Neurochemistry, vol. 74, no. 2, pp. 792–798, 2000. View at Publisher · View at Google Scholar · View at Scopus
  76. A. Wahab, K. Albus, S. Gabriel, and U. Heinemann, “In search of models of pharmacoresistant epilepsy,” Epilepsia, vol. 51, no. 3, pp. 154–159, 2010. View at Publisher · View at Google Scholar · View at Scopus
  77. W. Löscher and R. Köhling, “Functional, metabolic, and synaptic changes after seizures as potential targets for antiepileptic therapy,” Epilepsy and Behavior, vol. 19, no. 2, pp. 105–113, 2010. View at Publisher · View at Google Scholar · View at Scopus
  78. N. Suenaga, T. Ichiyama, M. Kubota, H. Isumi, J. Tohyama, and S. Furukawa, “Roles of matrix metalloproteinase-9 and tissue inhibitors of metalloproteinases 1 in acute encephalopathy following prolonged febrile seizures,” Journal of the Neurological Sciences, vol. 266, no. 1-2, pp. 126–130, 2008. View at Publisher · View at Google Scholar · View at Scopus
  79. M. Rylski, R. Amborska, K. Zybura et al., “JunB is a repressor of MMP-9 transcription in depolarized rat brain neurons,” Molecular and Cellular Neuroscience, vol. 40, no. 1, pp. 98–110, 2009. View at Publisher · View at Google Scholar · View at Scopus
  80. F. A. Konopacki, M. Rylski, E. Wilczek et al., “Synaptic localization of seizure-induced matrix metalloproteinase-9 mRNA,” Neuroscience, vol. 150, no. 1, pp. 31–39, 2007. View at Publisher · View at Google Scholar · View at Scopus
  81. J. W. Wright and J. W. Harding, “The brain angiotensin system and extracellular matrix molecules in neural plasticity, learning, and memory,” Progress in Neurobiology, vol. 72, no. 4, pp. 263–293, 2004. View at Publisher · View at Google Scholar · View at Scopus
  82. J. W. Zhang, S. Deb, and P. E. Gottschall, “Regional and differential expression of gelatinases in rat brain after systemic kainic acid or bicuculline administration,” European Journal of Neuroscience, vol. 10, no. 11, pp. 3358–3368, 1998. View at Publisher · View at Google Scholar · View at Scopus
  83. G. M. Wilczynski, F. A. Konopacki, E. Wilczek et al., “Important role of matrix metalloproteinase 9 in epileptogenesis,” Journal of Cell Biology, vol. 180, no. 5, pp. 1021–1035, 2008. View at Publisher · View at Google Scholar · View at Scopus
  84. G. W. Kim, H. J. Kim, K. J. Cho, H. W. Kim, Y. J. Cho, and B. I. Lee, “The role of MMP-9 in integrin-mediated hippocampal cell death after pilocarpine-induced status epilepticus,” Neurobiology of Disease, vol. 36, no. 1, pp. 169–180, 2009. View at Publisher · View at Google Scholar · View at Scopus
  85. E. Takács, R. Nyilas, Z. Szepesi 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,” Neurochemistry International, vol. 56, no. 6-7, pp. 799–809, 2010. View at Publisher · View at Google Scholar · View at Scopus
  86. H. Mizoguchi, J. Nakade, M. Tachibana et al., “Matrix metalloproteinase-9 contributes to kindled seizure development in pentylenetetrazole-treated mice by converting pro-BDNF to mature BDNF in the hippocampus,” Journal of Neuroscience, vol. 31, no. 36, pp. 12963–12971, 2011. View at Publisher · View at Google Scholar
  87. R. J. Cabelli, A. Hohn, and C. J. Shatz, “Inhibition of ocular dominance column formation by infusion of NT-4/5 or BDNF,” Science, vol. 267, no. 5204, pp. 1662–1666, 1995. View at Google Scholar · View at Scopus
  88. H. W. Horch, A. Krüttgen, S. D. Portbury, and L. C. Katz, “Destabilization of cortical dendrites and spines by BDNF,” Neuron, vol. 23, no. 2, pp. 353–364, 1999. View at Publisher · View at Google Scholar · View at Scopus
  89. G. Nagappan, E. Zaitsev, V. V. Senatorov Jr., J. Yang, B. L. Hempstead, and B. Lu, “Control of extracellular cleavage of ProBDNF by high frequency neuronal activity,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 4, pp. 1267–1272, 2009. View at Publisher · View at Google Scholar · View at Scopus
  90. R. Lee, P. Kermani, K. K. Teng, and B. L. Hempstead, “Regulation of cell survival by secreted proneurotrophins,” Science, vol. 294, no. 5548, pp. 1945–1948, 2001. View at Publisher · View at Google Scholar · View at Scopus
  91. J. H. Jung, M. H. Park, S. Y. Choi, and J. Y. Koh, “Activation of the Trk signaling pathway by extracellular zinc. Role of metalloproteinases,” Journal of Biological Chemistry, vol. 280, no. 12, pp. 11995–12001, 2005. View at Publisher · View at Google Scholar · View at Scopus
  92. R. Koyama, M. K. Yamada, S. Fujisawa, R. Katoh-Semba, N. Matsuki, and Y. Ikegaya, “Brain-derived neurotrophic factor induces hyperexcitable reentrant circuits in the dentate gyrus,” Journal of Neuroscience, vol. 24, no. 33, pp. 7215–7224, 2004. View at Publisher · View at Google Scholar