Hostname: page-component-586b7cd67f-dlnhk Total loading time: 0 Render date: 2024-11-24T04:23:16.346Z Has data issue: false hasContentIssue false

Extracellular matrix in plasticity and epileptogenesis

Published online by Cambridge University Press:  05 June 2009

Alexander Dityatev*
Affiliation:
Department of Neuroscience and Brain Technologies, Italian Institute of Technology, via Morego 30, 16163 Genova, Italy
Tommaso Fellin
Affiliation:
Department of Neuroscience and Brain Technologies, Italian Institute of Technology, via Morego 30, 16163 Genova, Italy
*
Correspondence should be addressed to: Alexander Dityatev, Department of Neuroscience and Brain Technologies, The Italian Institute of Technology, 16163 Genova, Italy phone: +39 010 71781515 fax: +39 010 720321 email: [email protected]

Abstract

Extracellular matrix (ECM) in the brain is composed of molecules synthesized and secreted by neurons and glial cells in a cell-type-specific and activity-dependent manner. During development, ECM plays crucial roles in proliferation, migration and differentiation of neural cells. In the mature brain, ECM undergoes a slow turnover and supports multiple physiological processes, while restraining structural plasticity. In the first part of this review, we discuss the contribution of ECM molecules to different forms of plasticity, including developmental plasticity in the cortex, long-term potentiation and depression in the hippocampus, homeostatic scaling of synaptic transmission and metaplasticity. In the second part, we focus on pathological changes associated with epileptogenic mutations in ECM-related molecules or caused by seizure-induced remodeling of ECM. The available data suggest that ECM components regulating physiological plasticity are also engaged in different aspects of epileptogenesis, such as dysregulation of excitatory and inhibitory neurotransmission, sprouting of mossy fibers, granule cell dispersion and gliosis. At the end, we discuss combinatorial approaches that might be used to counteract seizure-induced dysregulation of both ECM molecules and extracellular proteases. By restraining ECM modification and preserving the status quo in the brain, these treatments might prove to be valid therapeutic interventions to antagonize the progression of epileptogenesis.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2009

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Al Sawaf, S., Mayatepek, E. and Hoffmann, B. (2008) Neurological findings in Hunter disease: pathology and possible therapeutic effects reviewed. Journal of Inherited Metabolic Disease 31, 473480.CrossRefGoogle ScholarPubMed
Alpar, A., Gartner, U., Hartig, W. and Bruckner, G. (2006) Distribution of pyramidal cells associated with perineuronal nets in the neocortex of rat. Brain Research 1120, 1322.CrossRefGoogle ScholarPubMed
Ballabh, P., Braun, A. and Nedergaard, M. (2004) The blood-brain barrier: an overview: structure, regulation, and clinical implications. Neurobiology of Disease 16, 113.CrossRefGoogle ScholarPubMed
Barger, S.W. and Van Eldik, L.J. (1992) S100 beta stimulates calcium fluxes in glial and neuronal cells. Journal of Biological Chemistry 267, 96899694.CrossRefGoogle ScholarPubMed
Beattie, E.C., Stellwagen, D., Morishita, W., Bresnahan, J.C., Ha, B.K., Von Zastrow, M. et al. (2002) Control of synaptic strength by glial TNFalpha. Science 295, 22822285.CrossRefGoogle ScholarPubMed
Beck, H., Goussakov, I.V., Lie, A., Helmstaedter, C. and Elger, C.E. (2000) Synaptic plasticity in the human dentate gyrus. Journal of Neuroscience 20, 70807086.CrossRefGoogle ScholarPubMed
Berardi, N., Pizzorusso, T. and Maffei, L. (2004) Extracellular matrix and visual cortical plasticity: freeing the synapse. Neuron 44, 905908.Google ScholarPubMed
Berardi, N., Pizzorusso, T., Ratto, G.M. and Maffei, L. (2003) Molecular basis of plasticity in the visual cortex. Trends in Neurosciences 26, 369378.Google Scholar
Bienenstock, E.L., Cooper, L.N. and Munro, P.W. (1982) Theory for the development of neuron selectivity: orientation specificity and binocular interaction in visual cortex. Journal of Neuroscience 2, 3248.CrossRefGoogle ScholarPubMed
Bornstein, P. and Sage, E.H. (2002) Matricellular proteins: extracellular modulators of cell function. Current Opinion in Cell Biology 14, 608616.CrossRefGoogle ScholarPubMed
Bouilleret, V., Ridoux, V., Depaulis, A., Marescaux, C., Nehlig, A. and Le Gal La Salle, G. (1999) Recurrent seizures and hippocampal sclerosis following intrahippocampal kainate injection in adult mice: electroencephalography, histopathology and synaptic reorganization similar to mesial temporal lobe epilepsy. Neuroscience 89, 717729.CrossRefGoogle ScholarPubMed
Brakebusch, C., Seidenbecher, C.I., Asztely, F., Rauch, U., Matthies, H., Meyer, H. et al. (2002) Brevican-deficient mice display impaired hippocampal CA1 long-term potentiation but show no obvious deficits in learning and memory. Molecular and Cellular Biology 22, 74177427.Google Scholar
Brenneke, F., Bukalo, O., Dityatev, A. and Lie, A.A. (2004a) Mice deficient for the extracellular matrix glycoprotein tenascin-r show physiological and structural hallmarks of increased hippocampal excitability, but no increased susceptibility to seizures in the pilocarpine model of epilepsy. Neuroscience 124, 841855.CrossRefGoogle ScholarPubMed
Brenneke, F., Schachner, M., Elger, C.E. and Lie, A.A. (2004b) Up-regulation of the extracellular matrix glycoprotein tenascin-R during axonal reorganization and astrogliosis in the adult rat hippocampus. Epilepsy Research 58, 133143.CrossRefGoogle ScholarPubMed
Bruckner, G., Bringmann, A., Hartig, W., Koppe, G., Delpech, B. and Brauer, K. (1998) Acute and long-lasting changes in extracellular-matrix chondroitin-sulphate proteoglycans induced by injection of chondroitinase ABC in the adult rat brain. Experimental Brain Research 121, 300310.Google ScholarPubMed
Bruckner, G., Szeoke, S., Pavlica, S., Grosche, J. and Kacza, J. (2006) Axon initial segment ensheathed by extracellular matrix in perineuronal nets. Neuroscience 138, 365375.Google Scholar
Bukalo, O., Schachner, M. and Dityatev, A. (2001) Modification of extracellular matrix by enzymatic removal of chondroitin sulfate and by lack of tenascin-R differentially affects several forms of synaptic plasticity in the hippocampus. Neuroscience 104, 359369.CrossRefGoogle ScholarPubMed
Bukalo, O., Schachner, M. and Dityatev, A. (2007) Hippocampal metaplasticity induced by deficiency in the extracellular matrix glycoprotein tenascin-R. Journal of Neuroscience 27, 60196028.CrossRefGoogle ScholarPubMed
Burrage, P.S., Mix, K.S. and Brinckerhoff, C.E. (2006) Matrix metalloproteinases: role in arthritis. Frontiers in Bioscience 11, 529543.CrossRefGoogle ScholarPubMed
Celio, M.R., Spreafico, R., De Biasi, S. and Vitellaro-Zuccarello, L. (1998) Perineuronal nets: past and present. Trends in Neurosciences 21, 510515.CrossRefGoogle ScholarPubMed
Chung, K.F. (2006) Cytokines as targets in chronic obstructive pulmonary disease. Current Drug Targets 7, 675681.CrossRefGoogle ScholarPubMed
Cingolani, L.A., Thalhammer, A., Yu, L.M., Catalano, M., Ramos, T., Colicos, M.A. et al. (2008) Activity-dependent regulation of synaptic AMPA receptor composition and abundance by beta3 integrins. Neuron 58, 749762.CrossRefGoogle ScholarPubMed
Dityatev, A., Bruckner, G., Dityateva, G., Grosche, J., Kleene, R. and Schachner, M. (2007) Activity-dependent formation and functions of chondroitin sulfate-rich extracellular matrix of perineuronal nets. Developmental Neurobiology 67, 570588.CrossRefGoogle ScholarPubMed
Dityatev, A., Frischknecht, R. and Seidenbecher, C.I. (2006) Extracellular matrix and synaptic functions. Results and Problems in Cell Differentiation 43, 6997.CrossRefGoogle ScholarPubMed
Dityatev, A., Irintchev, A., Morellini, F. and Schachner, M. (2008) Extracellular matrix molecules: synaptic plasticity and learning. In Squire, L.R. (ed.) Encyclopedia of Neuroscience. Elsevier, pp. 149156.Google Scholar
Dityatev, A. and Schachner, M. (2003) Extracellular matrix molecules and synaptic plasticity. Nature Reviews Neuroscience 4, 456468.CrossRefGoogle ScholarPubMed
Dyck, R.H., Bogoch, I.I., Marks, A., Melvin, N.R. and Teskey, G.C. (2002) Enhanced epileptogenesis in S100B knockout mice. Brain Research Molecular Brain Research 106, 2229.CrossRefGoogle ScholarPubMed
Etienne-Manneville, S. and Hall, A. (2001) Integrin-mediated activation of Cdc42 controls cell polarity in migrating astrocytes through PKCzeta. Cell 106, 489498.CrossRefGoogle ScholarPubMed
Fagiolini, M., Fritschy, J.M., Low, K., Mohler, H., Rudolph, U. and Hensch, T.K. (2004) Specific GABAA circuits for visual cortical plasticity. Science 303, 16811683.CrossRefGoogle ScholarPubMed
Fasen, K., Elger, C.E. and Lie, A.A. (2003) Distribution of alpha and beta integrin subunits in the adult rat hippocampus after pilocarpine-induced neuronal cell loss, axonal reorganization and reactive astrogliosis. Acta Neuropathologica 106, 319322.CrossRefGoogle ScholarPubMed
Fellin, T. (2009) Communication between neurons and astrocytes: relevance to the modulation of synaptic and network activity. Journal of Neurochemistry 108, 533544.CrossRefGoogle Scholar
Fukata, Y., Adesnik, H., Iwanaga, T., Bredt, D.S., Nicoll, R.A. and Fukata, M. (2006) Epilepsy-related ligand/receptor complex LGI1 and ADAM22 regulate synaptic transmission. Science 313, 17921795.CrossRefGoogle ScholarPubMed
Galtrey, C.M. and Fawcett, J.W. (2007) The role of chondroitin sulfate proteoglycans in regeneration and plasticity in the central nervous system. Brain Research Reviews 54, 118.CrossRefGoogle ScholarPubMed
Gong, C., Wang, T.W., Huang, H.S. and Parent, J.M. (2007) Reelin regulates neuronal progenitor migration in intact and epileptic hippocampus. Journal of Neuroscience 27, 18031811.CrossRefGoogle ScholarPubMed
Goussakov, I.V., Fink, K., Elger, C.E. and Beck, H. (2000) Metaplasticity of mossy fiber synaptic transmission involves altered release probability. Journal of Neuroscience 20, 34343441.CrossRefGoogle ScholarPubMed
Gu, W., Sander, T., Becker, T. and Steinlein, O.K. (2004) Genotypic association of exonic LGI4 polymorphisms and childhood absence epilepsy. Neurogenetics 5, 4144.CrossRefGoogle ScholarPubMed
Guadagno, E. and Moukhles, H. (2004) Laminin-induced aggregation of the inwardly rectifying potassium channel, Kir4.1, and the water-permeable channel, AQP4, via a dystroglycan-containing complex in astrocytes. Glia 47, 138149.CrossRefGoogle Scholar
Guerrini, R. and Filippi, T. (2005) Neuronal migration disorders, genetics, and epileptogenesis. Journal of Child Neurology 20, 287299.Google Scholar
Guntinas-Lichius, O., Angelov, D.N., Morellini, F., Lenzen, M., Skouras, E., Schachner, M. et al. (2005) Opposite impacts of tenascin-C and tenascin-R deficiency in mice on the functional outcome of facial nerve repair. European Journal of Neuroscience 22, 21712179.CrossRefGoogle ScholarPubMed
Gurevicius, K., Gureviciene, I., Valjakka, A., Schachner, M. and Tanila, H. (2004) Enhanced cortical and hippocampal neuronal excitability in mice deficient in the extracellular matrix glycoprotein tenascin-R. Molecular and Cellular Neuroscience 25, 515523.CrossRefGoogle ScholarPubMed
Gurevicius, K., Kuang, F., Stoenica, L., Irintchev, A., Gureviciene, I., Dityatev, A. et al. (2009) Genetic ablation of tenascin-C expression leads to abnormal hippocampal CA1 structure and electrical activity in vivo. Hippocampus DOI 10.1002/hipo.20585.CrossRefGoogle ScholarPubMed
Haber, M., Zhou, L. and Murai, K.K. (2006) Cooperative astrocyte and dendritic spine dynamics at hippocampal excitatory synapses. Journal of Neuroscience 26, 88818891.CrossRefGoogle ScholarPubMed
Hargus, G., Cui, Y., Schmid, J.S., Xu, J., Glatzel, M., Schachner, M. et al. (2008) Tenascin-R promotes neuronal differentiation of embryonic stem cells and recruitment of host-derived neural precursor cells after excitotoxic lesion of the mouse striatum. Stem Cells 26, 19731984.CrossRefGoogle ScholarPubMed
Heinrich, C., Nitta, N., Flubacher, A., Muller, M., Fahrner, A., Kirsch, M. et al. (2006) Reelin deficiency and displacement of mature neurons, but not neurogenesis, underlie the formation of granule cell dispersion in the epileptic hippocampus. Journal of Neuroscience 26, 47014713.Google Scholar
Hoffmann, K., Sivukhina, E., Potschka, H., Schachner, M., Löscher, W. and Dityatev, A. (2009) Retarded kindling progression in mice deficient in the extracellular matrix glycoprotein tenascin-R. Epilepsia 50, 859869.CrossRefGoogle ScholarPubMed
Holley, J.E., Gveric, D., Whatmore, J.L. and Gutowski, N.J. (2005) Tenascin C induces a quiescent phenotype in cultured adult human astrocytes. Glia 52, 5358.CrossRefGoogle ScholarPubMed
Houser, C.R. (1990) Granule cell dispersion in the dentate gyrus of humans with temporal lobe epilepsy. Brain Research 535, 195204.CrossRefGoogle ScholarPubMed
Huang, Y.Y., Bach, M.E., Lipp, H.P., Zhuo, M., Wolfer, D.P., Hawkins, R.D. et al. (1996) Mice lacking the gene encoding tissue-type plasminogen activator show a selective interference with late-phase long-term potentiation in both Schaffer collateral and mossy fiber pathways. Proceedings of the National Academy of Sciences of the U.S.A. 93, 86998704.CrossRefGoogle ScholarPubMed
Iadecola, C. and Nedergaard, M. (2007) Glial regulation of the cerebral microvasculature. Nature Neuroscience 10, 13691376.CrossRefGoogle ScholarPubMed
Ikeshima-Kataoka, H., Shen, J.S., Eto, Y., Saito, S. and Yuasa, S. (2008) Alteration of inflammatory cytokine production in the injured central nervous system of tenascin-deficient mice. In Vivo 22, 409413.Google Scholar
Irintchev, A., Rollenhagen, A., Troncoso, E., Kiss, J.Z. and Schachner, M. (2005) Structural and functional aberrations in the cerebral cortex of tenascin-C deficient mice. Cerebral Cortex 15, 950962.CrossRefGoogle ScholarPubMed
Kalachikov, S., Evgrafov, O., Ross, B., Winawer, M., Barker-Cummings, C., Martinelli Boneschi, F. et al. (2002) Mutations in LGI1 cause autosomal-dominant partial epilepsy with auditory features. Nature Genetics 30, 335341.CrossRefGoogle ScholarPubMed
Kaneko, M., Stellwagen, D., Malenka, R.C. and Stryker, M.P. (2008) Tumor necrosis factor-alpha mediates one component of competitive, experience-dependent plasticity in developing visual cortex. Neuron 58, 673680.CrossRefGoogle ScholarPubMed
Katagiri, H., Fagiolini, M. and Hensch, T.K. (2007) Optimization of somatic inhibition at critical period onset in mouse visual cortex. Neuron 53, 805812.CrossRefGoogle ScholarPubMed
Kerever, A., Schnack, J., Vellinga, D., Ichikawa, N., Moon, C., Arikawa-Hirasawa, E. et al. (2007) Novel extracellular matrix structures in the neural stem cell niche capture the neurogenic factor fibroblast growth factor 2 from the extracellular milieu. Stem Cells 25, 21462157.CrossRefGoogle ScholarPubMed
Lander, C., Kind, P., Maleski, M. and Hockfield, S. (1997) A family of activity-dependent neuronal cell-surface chondroitin sulfate proteoglycans in cat visual cortex. Journal of Neuroscience 17, 19281939.CrossRefGoogle ScholarPubMed
Letts, V.A., Felix, R., Biddlecome, G.H., Arikkath, J., Mahaffey, C.L., Valenzuela, A. et al. (1998) The mouse stargazer gene encodes a neuronal Ca2+-channel gamma subunit. Nature Genetics 19, 340347.CrossRefGoogle ScholarPubMed
Li, S.Y., Xu, D.S. and Jia, H.T. (2003) AGS-induced expression of Narp is concomitant with expression of AMPA receptor subunits GluR1 and GluR2 in hippocampus but not inferior colliculus of P77PMC rats. Neurobiology of Disease 14, 328335.Google Scholar
Lively, S. and Brown, I.R. (2008) The extracellular matrix protein SC1/hevin localizes to excitatory synapses following status epilepticus in the rat lithium-pilocarpine seizure model. Journal of Neuroscience Research 86, 28952905.CrossRefGoogle ScholarPubMed
Lundell, A., Olin, A.I., Morgelin, M., al-Karadaghi, S., Aspberg, A. and Logan, D.T. (2004) Structural basis for interactions between tenascins and lectican C-type lectin domains: evidence for a crosslinking role for tenascins. Structure 12, 14951506.CrossRefGoogle ScholarPubMed
Mataga, N., Mizuguchi, Y. and Hensch, T.K. (2004) Experience-dependent pruning of dendritic spines in visual cortex by tissue plasminogen activator. Neuron 44, 10311041.Google Scholar
Mataga, N., Nagai, N. and Hensch, T.K. (2002) Permissive proteolytic activity for visual cortical plasticity. Proceedings of the National Academy of Sciences of the U.S.A. 99, 77177721.CrossRefGoogle ScholarPubMed
Meighan, S.E., Meighan, P.C., Choudhury, P., Davis, C.J., Olson, M.L., Zornes, P.A. et al. (2006) Effects of extracellular matrix-degrading proteases matrix metalloproteinases 3 and 9 on spatial learning and synaptic plasticity. Journal of Neurochemistry 96, 12271241.CrossRefGoogle ScholarPubMed
Miyata, S., Akagi, A., Hayashi, N., Watanabe, K. and Oohira, A. (2004) Activity-dependent regulation of a chondroitin sulfate proteoglycan 6B4 phosphacan/RPTPbeta in the hypothalamic supraoptic nucleus. Brain Research 1017, 163171.CrossRefGoogle ScholarPubMed
Nagy, V., Bozdagi, O., Matynia, A., Balcerzyk, M., Okulski, P., Dzwonek, J. et al. (2006) Matrix metalloproteinase-9 is required for hippocampal late-phase long-term potentiation and memory. Journal of Neuroscience 26, 19231934.CrossRefGoogle ScholarPubMed
Nikonenko, A., Schmidt, S., Skibo, G., Bruckner, G. and Schachner, M. (2003) Tenascin-R-deficient mice show structural alterations of symmetric perisomatic synapses in the CA1 region of the hippocampus. The Journal of Comparative Neurology 456, 338349.CrossRefGoogle ScholarPubMed
Okamoto, M., Sakiyama, J., Mori, S., Kurazono, S., Usui, S., Hasegawa, M. et al. (2003) Kainic acid-induced convulsions cause prolonged changes in the chondroitin sulfate proteoglycans neurocan and phosphacan in the limbic structures. Experimental Neurology 184, 179195.Google Scholar
Okulski, P., Jay, T.M., Jaworski, J., Duniec, K., Dzwonek, J., Konopacki, F.A. et al. (2007) TIMP-1 abolishes MMP-9-dependent long-lasting long-term potentiation in the prefrontal cortex. Biological Psychiatry 62, 359362.CrossRefGoogle ScholarPubMed
Oray, S., Majewska, A. and Sur, M. (2004) Dendritic spine dynamics are regulated by monocular deprivation and extracellular matrix degradation. Neuron 44, 10211030.CrossRefGoogle ScholarPubMed
Peng, H., Shah, W., Holland, P. and Carbonetto, S. (2008) Integrins and dystroglycan regulate astrocyte wound healing: the integrin beta1 subunit is necessary for process extension and orienting the microtubular network. Developmental Neurobiology 68, 559574.CrossRefGoogle ScholarPubMed
Perosa, S.R., Porcionatto, M.A., Cukiert, A., Martins, J.R., Amado, D., Nader, H.B. et al. (2002) Extracellular matrix components are altered in the hippocampus, cortex, and cerebrospinal fluid of patients with mesial temporal lobe epilepsy. Epilepsia 43 (Suppl. 5), 159161.CrossRefGoogle ScholarPubMed
Pizzorusso, T., Medini, P., Berardi, N., Chierzi, S., Fawcett, J.W. and Maffei, L. (2002) Reactivation of ocular dominance plasticity in the adult visual cortex. Science 298, 12481251.CrossRefGoogle ScholarPubMed
Ponta, H., Sherman, L. and Herrlich, P.A. (2003) CD44: from adhesion molecules to signalling regulators. Nature Reviews Molecular and Cellular Biology 4, 3345.Google Scholar
Powell, E.M., Campbell, D.B., Stanwood, G.D., Davis, C., Noebels, J.L. and Levitt, P. (2003) Genetic disruption of cortical interneuron development causes region- and GABA cell type-specific deficits, epilepsy, and behavioral dysfunction. Journal of Neuroscience 23, 622631.Google Scholar
Rauch, U. (2004) Extracellular matrix components associated with remodeling processes in brain. Cellular and Molecular Life Sciences 61, 20312045.CrossRefGoogle ScholarPubMed
Rich, M.M. and Wenner, P. (2007) Sensing and expressing homeostatic synaptic plasticity. Trends in Neurosciences 30, 119125.Google Scholar
Rigato, F., Garwood, J., Calco, V., Heck, N., Faivre-Sarrailh, C. and Faissner, A. (2002) Tenascin-C promotes neurite outgrowth of embryonic hippocampal neurons through the alternatively spliced fibronectin type III BD domains via activation of the cell adhesion molecule F3/contactin. Journal of Neuroscience 22, 65966609.CrossRefGoogle ScholarPubMed
Royer-Zemmour, B., Ponsole-Lenfant, M., Gara, H., Roll, P., Leveque, C., Massacrier, A. et al. (2008) Epileptic and developmental disorders of the speech cortex: ligand/receptor interaction of wild-type and mutant SRPX2 with the plasminogen activator receptor uPAR. Human Molecular Genetics 17, 36173630.CrossRefGoogle ScholarPubMed
Sagane, K., Hayakawa, K., Kai, J., Hirohashi, T., Takahashi, E., Miyamoto, N. et al. (2005) Ataxia and peripheral nerve hypomyelination in ADAM22-deficient mice. BMC Neuroscience 6, 33.CrossRefGoogle ScholarPubMed
Sagane, K., Ishihama, Y. and Sugimoto, H. (2008) LGI1 and LGI4 bind to ADAM22, ADAM23 and ADAM11. International Journal of Biological Sciences 4, 387396.CrossRefGoogle ScholarPubMed
Saghatelyan, A.K., Dityatev, A., Schmidt, S., Schuster, T., Bartsch, U. and Schachner, M. (2001) Reduced perisomatic inhibition, increased excitatory transmission, and impaired long-term potentiation in mice deficient for the extracellular matrix glycoprotein tenascin-R. Molecular and Cellular Neuroscience 17, 226240.CrossRefGoogle ScholarPubMed
Saghatelyan, A.K., Gorissen, S., Albert, M., Hertlein, B., Schachner, M. and Dityatev, A. (2000) The extracellular matrix molecule tenascin-R and its HNK-1 carbohydrate modulate perisomatic inhibition and long-term potentiation in the CA1 region of the hippocampus. European Journal of Neuroscience 12, 33313342.CrossRefGoogle ScholarPubMed
Saghatelyan, A.K., Snapyan, M., Gorissen, S., Meigel, I., Mosbacher, J., Kaupmann, K. et al. (2003) Recognition molecule associated carbohydrate inhibits postsynaptic GABA(B) receptors: a mechanism for homeostatic regulation of GABA release in perisomatic synapses. Molecular and Cellular Neuroscience 24, 271282.CrossRefGoogle ScholarPubMed
Sakatani, S., Seto-Ohshima, A., Itohara, S. and Hirase, H. (2007) Impact of S100B on local field potential patterns in anesthetized and kainic acid-induced seizure conditions in vivo. European Journal of Neuroscience 25, 11441154.CrossRefGoogle ScholarPubMed
Sakatani, S., Seto-Ohshima, A., Shinohara, Y., Yamamoto, Y., Yamamoto, H., Itohara, S. et al. (2008) Neural-activity-dependent release of S100B from astrocytes enhances kainate-induced gamma oscillations in vivo. Journal of Neuroscience 28, 1092810936.CrossRefGoogle ScholarPubMed
Scharfman, H.E., Goodman, J.H. and Sollas, A.L. (2000) Granule-like neurons at the hilar/CA3 border after status epilepticus and their synchrony with area CA3 pyramidal cells: functional implications of seizure-induced neurogenesis. Journal of Neuroscience 20, 61446158.CrossRefGoogle ScholarPubMed
Schubert, M., Siegmund, H., Pape, H.C. and Albrecht, D. (2005) Kindling-induced changes in plasticity of the rat amygdala and hippocampus. Learning & Memory 12, 520526.CrossRefGoogle ScholarPubMed
Sirko, S., von Holst, A., Wizenmann, A., Gotz, M. and Faissner, A. (2007) Chondroitin sulfate glycosaminoglycans control proliferation, radial glia cell differentiation and neurogenesis in neural stem/progenitor cells. Development 134, 27272738.CrossRefGoogle ScholarPubMed
Staubli, U., Vanderklish, P. and Lynch, G. (1990) An inhibitor of integrin receptors blocks long-term potentiation. Behavioral and Neural Biology 53, 15.CrossRefGoogle ScholarPubMed
Stellwagen, D. and Malenka, R.C. (2006) Synaptic scaling mediated by glial TNF-alpha. Nature 440, 10541059.CrossRefGoogle ScholarPubMed
Struve, J., Maher, P.C., Li, Y.Q., Kinney, S., Fehlings, M.G., Kuntz, C.T. et al. (2005) Disruption of the hyaluronan-based extracellular matrix in spinal cord promotes astrocyte proliferation. Glia 52, 1624.CrossRefGoogle ScholarPubMed
Theodosis, D.T., Poulain, D.A. and Oliet, S.H. (2008) Activity-dependent structural and functional plasticity of astrocyte–neuron interactions. Physiological Reviews 88, 9831008.CrossRefGoogle ScholarPubMed
Thiagarajan, T.C., Lindskog, M. and Tsien, R.W. (2005) Adaptation to synaptic inactivity in hippocampal neurons. Neuron 47, 725737.Google Scholar
Turrigiano, G. (2007) Homeostatic signaling: the positive side of negative feedback. Current Opinion in Neurobiology 17, 318324.CrossRefGoogle ScholarPubMed
Turrigiano, G.G., Leslie, K.R., Desai, N.S., Rutherford, L.C. and Nelson, S.B. (1998) Activity-dependent scaling of quantal amplitude in neocortical neurons. Nature 391, 892896.CrossRefGoogle ScholarPubMed
Turrigiano, G.G. and Nelson, S.B. (2004) Homeostatic plasticity in the developing nervous system. Nature Reviews Neuroscience 5, 97107.CrossRefGoogle ScholarPubMed
Vezzani, A. and Granata, T. (2005) Brain inflammation in epilepsy: experimental and clinical evidence. Epilepsia 46, 17241743.CrossRefGoogle ScholarPubMed
Volterra, A. and Meldolesi, J. (2005) Astrocytes, from brain glue to communication elements: the revolution continues. Nature Reviews Neuroscience 6, 626640.CrossRefGoogle ScholarPubMed
Wang, X.B., Bozdagi, O., Nikitczuk, J.S., Zhai, Z.W., Zhou, Q. and Huntley, G.W. (2008) Extracellular proteolysis by matrix metalloproteinase-9 drives dendritic spine enlargement and long-term potentiation coordinately. Proceedings of the National Academy of Sciences of the U.S.A. 105, 1952019525.CrossRefGoogle ScholarPubMed
Wetherington, J., Serrano, G. and Dingledine, R. (2008) Astrocytes in the epileptic brain. Neuron 58, 168178.CrossRefGoogle ScholarPubMed
Wiesel, T.N. and Hubel, D.H. (1963) Single-cell responses in striate cortex of kittens deprived of vision in one eye. Journal of Neurophysiology 26, 10031017.CrossRefGoogle ScholarPubMed
Wilczynski, G.M., Konopacki, F.A., Wilczek, E., Lasiecka, Z., Gorlewicz, A., Michaluk, P. et al. (2008) Important role of matrix metalloproteinase 9 in epileptogenesis. The Journal of Cell Biology 180, 10211035.CrossRefGoogle ScholarPubMed
Wu, Y.P., Siao, C.J., Lu, W., Sung, T.C., Frohman, M.A., Milev, P. et al. (2000) The tissue plasminogen activator (tPA)/plasmin extracellular proteolytic system regulates seizure-induced hippocampal mossy fiber outgrowth through a proteoglycan substrate. The Journal of Cell Biology 148, 12951304.CrossRefGoogle ScholarPubMed
Yamaguchi, Y. (2000) Lecticans: organizers of the brain extracellular matrix. Cellular and Molecular Life Sciences 57, 276289.Google Scholar
Ye, Z.C. and Sontheimer, H. (2002) Modulation of glial glutamate transport through cell interactions with the extracellular matrix. International Journal of Developmental Neuroscience 20, 209217.CrossRefGoogle ScholarPubMed
Yepes, M., Sandkvist, M., Coleman, T.A., Moore, E., Wu, J.Y., Mitola, D. et al. (2002) Regulation of seizure spreading by neuroserpin and tissue-type plasminogen activator is plasminogen-independent. The Journal of Clinical Investigation 109, 15711578.CrossRefGoogle ScholarPubMed
Yuan, W., Matthews, R.T., Sandy, J.D. and Gottschall, P.E. (2002) Association between protease-specific proteolytic cleavage of brevican and synaptic loss in the dentate gyrus of kainate-treated rats. Neuroscience 114, 10911101.CrossRefGoogle ScholarPubMed
Zhou, X.H., Brakebusch, C., Matthies, H., Oohashi, T., Hirsch, E., Moser, M. et al. (2001) Neurocan is dispensable for brain development. Molecular and Cellular Biology 21, 59705978.Google Scholar