Diverse functions of perineuronal nets

• Autorzy: Karetko M. , Skangiel-Kramska J.
• Języki publikacji: EN

Abstrakty

EN

Perineuronal nets represent well-organised components of the extracellular matrix, which are surrounding cell bodies, dendrites, and axon segments of a particular class of neurones as well as forming lattice-like structures. The role of perineuronal nets is not fully elucidated yet. Perineuronal nets may play a beneficial role by stabilizing the extracellular milieu assuring the characteristic features of enveloped neurons and protecting them from the influence of harmful agents. On the other hand, perineuronal nets create a barrier which limits neuronal plasticity and counteracts regeneration. This review examines recent evidence concerning the significance of the occurrence of perineuronal nets.

• Wydawca: -
• Czasopismo: Acta Neurobiologiae Experimentalis
• Rocznik: 2009
• Tom: 69
• Numer: 4
• Opis fizyczny: p.564–577,fig.,ref.

Twórcy

autor

Karetko M.

• Department of Molecular and Cellular Neurobiology, Nencki Institute of Experimental Biology, Polish Academy of Sciences, Warsaw, Poland

autor

Skangiel-Kramska J.

• Department of Molecular and Cellular Neurobiology, Nencki Institute of Experimental Biology, Polish Academy of Sciences, Warsaw, Poland

Bibliografia

• Angelov DN, Walther M, Streppel M, Guntinas-Lichius O, Neiss WF, Probstmeier R, Pesheva P (1998) Tenascin-R is antiadhesive for activated microglia that induce down- regulation of the protein after peripheral nerve injury: a new role in neuronal protection. J Neurosci 18: 6218­6229.
• Bahia CP, Houzel JC, Picanço-Diniz CW, Pereira A Jr (2008) Spatiotemporal distribution of proteoglycans in the developing rat's barrel field and the effects of early deafferentation. J Comp Neurol 510: 145-157.
• Balmer TS, Carels VM, Frisch JL, Nick TA (2009) Modulation of perineuronal nets and parvalbumin with developmental song learning. J Neurosci 29: 12878­12885.
• Baig S, Wilcock GK, Love S (2005) Loss of perineuronal net N-acetylgalactosamine in Alzheimer's disease. Acta Neuropathol 110: 393-401.
• Barritt AW, Davies M, Marchand F, Hartley R, Grist J, Yip P, McMahon SB, Bradbury EJ (2006) Chondroitinase ABC promotes sprouting of intact and injured spinal sys­tems after spinal cord injury. J Neurosci 26: 10856­10867.
• Beck H, Semisch M, Culmsee C, Plesnila N, Hatzopoulos AK (2008) Egr-1 regulates expression of the glial scar component phosphacan in astrocytes after experimental stroke. Am J Pathol 173: 77-92.
• Bertolotto A, Manzardo E, Guglielmone R (1996) Immunohistochemical mapping of perineuronal nets con­taining chondroitin unsulfated proteoglycan in the rat central nervous system. Cell Tissue Res 283: 283-295.
• Bidmon HJ, Jancsik V, Schleicher A, Hagemann G, Witte OW, Woodhams P, Zilles K (1998) Structural alterations and changes in cytoskeletal proteins and proteoglycans after focal cortical ischemia. Neuroscience 82: 397-420.
• Bradbury EJ, Moon LD, Popat RJ, King VR, Bennett GS, Patel PN, Fawcett JW, McMahon SB (2002) Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature 416: 636-640.
• Brakebusch C, Seidenbecher CI, Asztely F, Rauch U, Matthies H, Meyer H, Krug M, Böckers TM, Zhou X, Kreutz MR, Montag D, Gundelfinger ED, Fässler R (2002) Brevican- deficient mice display impaired hippocampal CA1 long- term potentiation but show no obvious deficits in learning and memory. Mol Cell Biol 22: 7417-7427.
• Brückner G, Brauer K, Hartig W, Wolff JR, Rickmann MJ, Derouiche A, Delpech B, Girard N, Oertel WH, Reichenbach A (1993) Perineuronal nets provide a polyanionic, glia-as- sociated form of microenvironment around certain neurons in many parts of the rat brain. Glia 8: 183-200.
• Brückner G, Seeger G, Brauer K, Härtig W, Kacza J, Bigl V (1994) Cortical areas are revealed by distribution patterns of proteoglycan components and parvalbumin in the Mongolian gerbil and rat. Brain Res 658: 67-86.
• Brückner G, Härtig W, Seeger J, Rübsamen R, Reimer K, Brauer K (1998) Cortical perineuronal nets in the gray short-tailed opossum (Monodelphis domestica): a distri­bution pattern contrasting with that shown in placental mammals. Anat Embryol (Berl) 197: 249-262.
• Brückner G, Hausen D, Härtig W, Drlicek M, Arendt T, Brauer K (1999) Cortical areas abundant in extracellular matrix chondroitin sulphate proteoglycans are less affect­ed by cytoskeletal changes in Alzheimer's disease. Neuroscience 92: 791-805.
• Brückner G, Grosche J, Hartlage-Rübsamen M, Schmidt S, Schachner M (2003) Region and lamina-specific distribu­tion of extracellular matrix proteoglycans, hyaluronan and tenascin-R in the mouse hippocampal formation. J Chem Neuroanat 26: 37-50.
• Brückner G, Szeöke S, Pavlica S, Grosche J, Kacza J (2006) Axon initial segment ensheathed by extracellular matrix in perineuronal nets. Neuroscience 138: 365-375.
• Bukalo O, Schachner M, 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: 359-369.
• Cafferty WB, Yang SH, Duffy PJ, Li S, Strittmatter SM (2007) Functional axonal regeneration through astrocytic scar genetically modified to digest chondroitin sulfate proteoglycans. J Neurosci 27: 2176-2185.
• Cafferty WB, Bradbury EJ, Lidierth M, Jones M, Duffy PJ, Pezet S, McMahon SB (2008) Chondroitinase ABC­mediated plasticity of spinal sensory function. J Neurosci 28: 11998-112009.
• Canas N, Valero T, Villarroya M, Montell E, Verges J, Garcia AG, Lopez MG (2007) Chondroitin sulfate protects SH-SY5Y cells from oxidative stress by inducing heme oxygenase-1 via phosphatidylinositol 3-kinase/Akt. J Pharmacol Exp Ther 323: 946-953.
• Carmichael ST, Wei L, Rovainen CM, Woolsey TA (2001) New patterns of intracortical projections after focal corti­cal stroke. Neurobiol Dis 8: 910-922.
• Carmichael ST, Archibeque I, Luke L, Nolan T, Momiy J, Li S (2005) Growth-associated gene expression after stroke: evidence for a growth-promoting region in peri-infarct cortex. Exp Neurol 193: 291-311.
• Carrell RW, Pemberton PA, Boswell DR (1987) The serpins: evolution and adaptation in a family of protease inhibi­tors. Cold Spring Harb Symp Quant Biol 52: 527-535.
• Carulli D, Rhodes KE, Brown DJ, Bonnert TP, Pollack SJ, Oliver K, Strata P, Fawcett JW (2006) Composition of perineuronal nets in the adult rat cerebellum and the cellular origin of their components. J Comp Neurol 494: 559-577.
• Carulli D, Rhodes KE, Fawcett JW (2007) Upregulation of aggrecan, link protein 1, and hyaluronan synthases during formation of perineuronal nets in the rat cerebellum. J Comp Neurol 501: 83-94.
• Caughey B, Raymond GJ (1993) Sulfated polyanion inhibi­tion of scrapie-associated PrP accumulation in cultured cells. J Virol 67: 643-650.
• Celio MR, Blumcke I (1994) Perineuronal nets - a special­ized form of extracellular matrix in the adult nervous system. Brain Res Brain Res Rev 19: 128-145.
• Costa C, Tortosa R, Domenech A, Vidal E, Pumarola M, Bassols A (2007) Mapping of aggrecan, hyaluronic acid, heparan sulphate proteoglycans and aquaporin 4 in the central ner­vous system of the mouse. J Chem Neuroanat 33: 111-123.
• Crespo D, Asher RA, Lin R, Rhodes KE, Fawcett JW (2007) How does chondroitinase promote functional recovery in the damaged CNS? Exp Neurol 206: 159-171.
• Cybulska-Klosowicz A, Zakrzewska R, Pyza E, Kossut M, Schachner M (2004) Reduced plasticity of cortical whis­ker representation in adult tenascin-C-deficient mice after vibrissectomy. Eur J Neurosci 20: 1538-1544.
• Deepa SS, Carulli D, Galtrey C, Rhodes K, Fukuda J, Mikami T, Sugahara K, Fawcett JW (2006) Composition of perineuronal net extracellular matrix in rat brain: a dif­ferent disaccharide composition for the net-associated proteoglycans. J Biol Chem 281: 17789-17800.
• Derouiche A, Härtig W, Brauer K, Brückner G (1996) Spatial relationship of lectin-labelled extracellular matrix and glutamine synthetase-immunoreactive astro- cytes in rat cortical forebrain regions. J Anat 189: 363­372.
• Dino MR, Harroch S, Hockfield S, Matthews RT (2006) Monoclonal antibody Cat-315 detects a glycoform of receptor protein tyrosine phosphatase beta/phosphacan early in CNS development that localizes to extrasynaptic sites prior to synapse formation. Neuroscience 142: 1055-1069.
• Dityatev A, Schachner M (2003) Extracellular matrix mol­ecules and synaptic plasticity. Review Nat Rev Neurosci 4: 456-468.
• Dityatev A, Brückner G, Dityateva G, Grosche J, Kleene R, Schachner M (2007) Activity-dependent formation and functions of chondroitin sulfate-rich extracellular matrix of perineuronal nets. Dev Neurobiol 67: 570-588.
• Engel M, Maurel P, Margolis RU, Margolis RK (1996) Chondroitin sulfate proteoglycans in the developing cen­tral nervous system. I. Cellular sites of synthesis of neu- rocan and phosphacan. J Comp Neurol 366: 34-43.
• Flaumenhaft R, Rifkin DB (1991) Extracellular matrix regu­lation of growth factor and protease activity. Curr Opin Cell Biol 3: 817-823.
• Freitag S, Schachner M, Morellini F (2003) Behavioral alterations in mice deficient for the extracellular matrix glycoprotein tenascin-R. Behav Brain Res 145: 189-207.
• Frischknecht R, Heine M, Perrais D, Seidenbecher CI, Choquet D, Gundelfinger ED (2009) Brain extracellular matrix affects AMPA receptor lateral mobility and short- term synaptic plasticity.Nat Neurosci 12: 897-904.
• Galtrey CM, Fawcett JW (2007) Characterization of tests of functional recovery after median and ulnar nerve injury and repair in the rat forelimb. J Peripher Nerv Syst 12: 11-27.
• Goedert M, Jakes R, Spillantini MG, Hasegawa M, Smith MJ, Crowther RA (1996) Assembly of microtubule-asso- ciated protein tau into Alzheimer-like filaments induced by sulphated glycosaminoglycans. Nature 383: 550-553.
• Gogolla N, Caroni P, Lüthi A, Herry C (2009) Perineuronal nets protect fear memories from erasure. Science 325: 1258-1261.
• Golgi C (1873) On the structure of the brain grey matter (in Italian). Gazzetta Medica Italiana. Lombardia 33: 244-246.
• Gray E, Thomas TL, Betmouni S, Scolding N, Love S (2008) Elevated matrix metalloproteinase-9 and degrada­tion of perineuronal nets in cerebrocortical multiple scle­rosis plaques. J Neuropathol Exp Neurol 67: 888-899.
• Grumet M, Hoffman S, Crossin KL, Edelman GM (1985) Cytotactin, an extracellular matrix protein of neural and non-neural tissues that mediates glia-neuron interaction. Proc Natl Acad Sci U S A 82: 8075-8079.
• Guerrero-Tarrago M, Yuste VJ, Iglesias M, Pérez J, Comella JX (1999) Binding patterns of lectins with GalNAc specificity in the mouse dorsal root ganglia and spinal cord. J Neurocytol 28: 75-84.
• Gurevicius K, Gureviciene I, Valjakka A, Schachner M, Tanila H (2005) Enhanced cortical and hippocampal neu­ronal excitability in mice deficient in the extracellular matrix glycoprotein tenascin-R. Mol Cell Neurosci 25: 515-523.
• Hartig W, Derouiche A, Welt K, Brauer K, Grosche J, Mader M, Reichenbach A, Brückner G (1999) Cortical neurons immunoreactive for the potassium channel Kv3.1b sub­unit are predominantly surrounded by perineuronal nets presumed as a buffering system for cations. Brain Res 842: 15-29.
• Härtig W, Klein C, Brauer K, Schüppel KF, Arendt T, Bigl V, Brückner G (2001) Hyperphosphorylated protein tau is restricted to neurons devoid of perineuronal nets in the cortex of aged bison. Neurobiol Aging 22: 25-33.
• Haunso A, Ibrahim M, Bartsch U, Letiembre M, Celio MR, Menoud PA ( 2000) Morphology of perineuronal nets in tenascin-R and parvalbumin single and double knockout mice. Brain Res 864: 142-145.
• Hayashi N, Miyata S, Yamada M, Kamei K, Oohira A (2005) Neuronal expression of the chondroitin sulfate proteogly- cans receptor-type protein-tyrosine phosphatase beta and phosphacan. Neuroscience 131: 331-348.
• Hensch TK (2005) Critical period plasticity in local cortical circuits. Nat Rev Neurosci 6: 877-888.
• Hilbich C, Kisters-Woike B, Reed J, Masters CL, Beyreuther K (1991) Aggregation and secondary structure of syn­thetic amyloid beta A4 peptides of Alzheimer's disease. J Mol Biol 218: 149-163.
• Hobohm C, Günther A, Grosche J, Rossner S, Schneider D, Brückner G (2005) Decomposition and long-lasting downregulation of extracellular matrix in perineuronal nets induced by focal cerebral ischemia in rats. J Neurosci Res 80: 539-548.
• Hockfield S, Kalb RG, Zaremba S, Fryer H (1990) Expression of neural proteoglycans correlates with the acquisition of mature neuronal properties in the mammalian brain. Cold Spring Harb Symp Quant Biol 55: 505-514.
• Horii-Hayashi N, Okuda H, Tatsumi K, Ishizaka S, Yoshikawa M, Wanaka A (2008) Localization of chondroitin sulfate proteoglycan versican in adult brain with special refer­ence to large projection neurons. Cell Tissue Res 334: 163-177.
• Ishii M, Maeda N (2008) Spatiotemporal expression of chon- droitin sulfate sulfotransferases in the postnatal develop­ing mouse cerebellum. Glycobiology 18: 602-614.
• John N, Krügel H, Frischknecht R, Smalla KH, Schultz C, Kreutz MR, Gundelfinger ED, Seidenbecher CI (2006) Brevican-containing perineuronal nets of extracellular matrix in dissociated hippocampal primary cultures. Mol Cell Neurosci 31: 774-784.
• Jones LL, Sajed D, Tuszynski MH (2003) Axonal regenera­tion through regions of chondroitin sulfate proteoglycan deposition after spinal cord injury: a balance of permis­siveness and inhibition. J Neurosci 23: 9276-9288.
• Kaas JH, Qi HX, Burish MJ, Gharbawie OA, Onifer SM, Massey JM (2008) Cortical and subcortical plasticity in the brains of humans, primates, and rats after damage to sensory afferents in the dorsal columns of the spinal cord. Exp Neurol 209: 407-416.
• Karetko M, Soulsby S, Nowicka D, Skangiel-Kramska J, Glazewski S (2008) Comparison of developmental distribu­tion of parvalbumin containing and PNN- enwrapped neu­rones in the barrel and visual cortices. FENS Abstr 4: 179.5.
• Karetko M, Nowicka D, Skangiel-Kramska J (2009) Loss and restoration of perineuronal nets after cortical photo- thrombotic stroke in rats [Polish Neuroscience Society 9th International Congress Abstract no. TIII.10]. Acta Neurobiol Exp (Wars) 69: 310.
• Kokaia Z, Lindvall O (2003) Neurogenesis after ischaemic brain insults. Curr Opin Neurobiol 13: 127-132.
• Koppe G, Brückner G, Hartig W, Delpech B, Bigl V (1997) Characterization of proteoglycan-containing perineuronal nets by enzymatic treatments of rat brain sections. Histochem J 29: 11-20.
• Kwok JC, Afshari F, Garcia-Alias G, Fawcett JW (2008) Proteoglycans in the central nervous system: plasticity, regeneration and their stimulation with chondroitinase ABC. Restor Neurol Neurosci 26: 131-145.
• Lander C, Kind P, Maleski M, Hockfield S (1997) A family of activity-dependent neuronal cell-surface chondroitin sulfate proteoglycans in cat visual cortex. J Neurosci 17: 1928-1939.
• Lander C, Zhang H, Hockfield S (1998) Neurons produce a neuronal cell surface-associated chondroitin sulfate proteoglycan. J Neurosci 18: 174-183.
• Mabuchi M, Murakami S, Taguchi T, Ohtsuka A, Murakami T (2001) Purkinje cells in the adult cat cerebellar cortex possess a perineuronal net of proteoglycans. Arch Histol Cytol 64: 203-209.
• Margolis RK, Rauch U, Maurel P, Margolis RU (1996) Neurocan and phosphacan: two major nervous tissue- specific chondroitin sulfate proteoglycans. Perspect Dev Neurobiol 3: 273-290.
• Massey JM, Amps J, Viapiano MS, Matthews RT, Wagoner MR, Whitaker CM, Alilain W, Yonkof AL, Khalyfa A, Cooper NG, Silver J, Onifer SM (2007) Increased chon- droitin sulfate proteoglycan expression in denervated brainstem targets following spinal cord injury creates a barrier to axonal regeneration overcome by chondroitinase ABC and neurotrophin-3. Exp Neurol 209: 426-445.
• Matsui F, Kawashima S, Shuo T, Yamauchi S, Tokita Y, Aono S, Keino H, Oohira A (2002) Transient expression of juvenile-type neurocan by reactive astrocytes in adult rat brains injured by kainate-induced seizures as well as surgical incision. Neuroscience 112: 773-781.
• Matthews RT, Kelly GM, Zerillo CA, Gray G, Tiemeyer M, Hockfield S (2002) Aggrecan glycoforms contribute to the molecular heterogeneity of perineuronal nets. J Neurosci 22: 7536-7547.
• McGee AW, Yang Y, Fischer QS, Daw NW, Strittmatter SM (2005) Experience- driven plasticity of visual cortex lim­ited by myelin and Nogo receptor. Science 309: 2222­2226.
• McKeon RJ, Schreiber RC, Rudge JS, Silver J (1991) Reduction of neurite outgrowth in a model of glial scar­ring following CNS injury is correlated with the expres­sion of inhibitory molecules on reactive astrocytes. J Neurosci 1: 3398-3411.
• McRae PA, Rocco MM, Kelly G, Brumberg JC, Matthews RT (2007) Sensory deprivation alters aggrecan and perineuronal net expression in the mouse barrel cortex. J Neurosci 27: 5405-5413.
• Meyer-Puttlitz B, Milev P, Junker E, Zimmer I, Margolis RU, Margolis RK (1995) Chondroitin sulfate and chon- droitin/keratan sulfate proteoglycans of nervous tissue: developmental changes of neurocan and phosphacan. J Neurochem 65: 2327-2337.
• Milev P, Maurel P, Chiba A, Mevissen M, Popp S, Yamaguchi Y, Margolis RK, Margolis RU (1998) Differential regula­tion of expression of hyaluronan-binding proteoglycans in developing brain: aggrecan, versican, neurocan, and brevican. Biochem Biophys Res Commun 247: 207-212.
• Miyata S, Nishimura Y, Hayashi N, Oohira A (2005) Construction of perineuronal net-like structure by cortical neurons in culture. Neuroscience 136: 95-104.
• Miyata S, Nishimura Y, Nakashima T (2007) Perineuronal nets protect against amyloid beta-protein neurotoxicity in cultured cortical neurons. Brain Res 1150: 200-206.
• Montag-Sallaz M, Montag D (2003) Severe cognitive and motor coordination deficits in tenascin-R-deficient mice. Genes Brain Behav 2: 20-31.
• Moon LD, Asher RA, Rhodes KE, Fawcett JW (2001) Regeneration of CNS axons back to their target following treatment of adult rat brain with chondroitinase ABC. Nat Neurosci 4: 465-466.
• Morawski M, Brückner MK, Riederer P, Brückner G, Arendt T (2004) Perineuronal nets potentially protect against oxidative stress. Exp Neurol 188: 309-315.
• Morawski M, Pavlica S, Seeger G, Grosche J, Kouznetsova E, Schliebs R, Brückner G, Arendt T (2008) Perineuronal nets are largely unaffected in Alzheimer model Tg2576 mice. Neurobiol Aging Oct 1. [Epub ahead of print].
• Murakami T, Ohtsuka A, Su WD, Taguchi T, Oohashi T, Murakami T, Abe K, Ninomiya Y (1999) The extracellu­lar matrix in the mouse brain: its reactions to endo-alpha- N-acetylgalactosaminidase and certain other enzymes. Arch Histol Cytol 62: 273-281.
• Murakami T, Ohtsuka A, Matsuoka H, Taguchi T, Murakami T, Abe K, Ninomiya Y (2001) Intensely positively charged perineuronal nets in the adult rat brain as detected by stain­ing with anionic iron colloid. Arch Histol Cytol 64: 45-50.
• Murakami T, Ohtsuka A (2003) Perisinapstic barrier of pro- teoglicans in the mature brain and spinal cord. Arch Histol Cytol 66: 195-207.
• Nakamura M, Nakano K, Morita S, Nakashima T, Oohira A, Miyata S (2009) Expression of chondroitin sulfate pro- teoglycans in barrel field of mouse and rat somatosensory cortex. Brain Res 1252: 117-129.
• Niederost BP, Zimmermann DR, Schwab ME, Bandtlow CE (1999) Bovine CNS myelin contains neurite growth-in­hibitory activity associated with chondroitin sulfate pro­teoglycans. J Neurosci 19: 8979-8989.
• Nikonenko A, Schmidt S, Skibo G, Brückner G, Schachner M (2003) Tenascin-R-deficient mice show structural altera­tions of symmetric perisomatic synapses in the CA1 region of the hippocampus. J Comp Neurol 456: 338-349.
• Nowicka D, Liguz-Lecznar M, Skangiel-Kramska J (2003) A surface antigen delineating a subset of neurons in the primary somatosensory cortex of the mouse. Acta Neurobiol Exp (Wars) 63: 185-195.
• Nowicka D, Soulsby S, Skangiel-Kramska J, Glazewski S (2009) Parvalbumin-containing neurones, perineuronal nets and experience-dependent plasticity in murine barrel cortex. Eur J Neurosci 30: 2053-2063.
• Ojima H, Sakai M, Ohyama J (1998) Molecular heterogene­ity of Vicia Villosa-recognized perineuronal nets sur­rounding pyramidal and nonpyramidal neurons in the guinea pig cerebral cortex. Brain Res 786: 274-280.
• Okamoto M, Mori S, Ichimura M, Endo H (1994) Chondroitin sulfate proteoglycans protect cultured rat's cortical and hippocampal neurons from delayed cell death induced by excitatory amino acids. Neurosci Lett 172: 51-54.
• Pesheva P, Gennarini G, Goridis C, Schachner M (1993) The F3/11 cell adhesion molecule mediates the repulsion of neurons by the extracellular matrix glycoprotein J1-160/180. Neuron 10: 69-82.
• Pizzorusso T, Medini P, Berardi N, Chierzi S, Fawcett JW, Maffei L (2002) Reactivation of ocular dominance plastic­ity in the adult visual cortex. Science 298: 1248-1251.
• Pizzorusso T, Medini P, Landi S, Baldini S, Berardi N, Maffei L (2006) Structural and functional recovery from early monocular deprivation in adult rats. Proc Natl Acad Sci U S A 103: 8517-8522.
• Popp S, Andersen JS, Maurel P, Margolis RU (2003) Localization of aggrecan and versican in the developing rat central nervous system. Dev Dyn 227: 143-149.
• Quaglia X, Beggah AT, Seidenbecher C, Zurn AD (2008) Delayed priming promotes CNS regeneration post-rhizo- tomy in Neurocan and Brevican-deficient mice. Brain 131: 240-249.
• Rauch U (2004) Extracellular matrix components associated with remodeling processes in brain. Cell Moll Life Sci 61: 2031-2045.
• Reimers S, Hartlage-Rübsamen M, Brückner G, Rossner S (2007) Formation of perineuronal nets in organo- typic mouse brain slice cultures is independent of neuronal glutamatergic activity. Eur J Neurosci 25: 2640-2648.
• Reinert T, Morawski M, Arendt T, Butz T (2003) Quantitative microanalysis of perineuronal nets in brain tissue. Nucl Instrum Methods Phys Res B 210: 395-400.
• Rhodes KE, Fawcett JW (2004) Chondroitin sulphate pro­teoglycans: preventing plasticity or protecting the CNS? J Anat 204: 33-48.
• Schüppel K, Brauer K, Härtig W, Grosche J, Earley B, Leonard BE, Brückner G (2002) Perineuronal nets of extracellular matrix around hippocampal interneurons resist destruction by activated microglia in trimethyltin- treated rats. Brain Res 958: 448-453.
• Seeger G, Lüth HJ, Winkelmann E, Brauer K (1996) Distribution patterns of Wisteria floribunda agglutinin binding sites and parvalbumin-immunoreactive neurons in the human visual cortex: a double-labelling study. J Hirnforsch 37: 351-366.
• Seidenbecher CI, Smalla KH, Fischer N, Gundelfinger ED, Kreutz MR (2002) Brevican isoforms associate with neu­ral membranes. J Neurochem 83: 738-746.
• Shen LH, Li Y, Gao Q, Savant-Bhonsale S, Chopp M (2008) Down-regulation of neurocan expression in reactive astrocytes promotes axonal regeneration and facilitates the neurorestorative effects of bone marrow stromal cells in the ischemic rat brain. Glia 56: 1747-1754.
• Silver J, Miller JH (2004) Regeneration beyond the glial scar. Nat Rev Neurosci 5: 146-156.
• Sobel RA, Ahmed AS (2001) White matter extracellular matrix chondroitin sulfate/dermatan sulfate proteoglycans in mul­tiple sclerosis. J Neuropathol Exp Neurol 60: 1198-1207.
• Sugiyama S, Di Nardo AA, Aizawa S, Matsuo I, Volovitch M, Prochiantz A, Hensch TK (2008) Experience- dependent transfer of Otx2 homeoprotein into the visual cortex activates postnatal plasticity. Cell 134: 508-520.
• Sykova E, Vorisek I, Mazel T, Antonova T, Schachner M (2005) Reduced extracellular space in the brain of tenascin-Rand HNK-1-sulphotransferase deficient mice. Eur J Neurosci 22: 1873-1880.
• Tang X, Davies JE, Davies SJ (2003) Changes in distribu­tion, cell associations, and protein expression levels of NG2, neurocan, phosphacan, brevican, versican V2, and tenascin-C during acute to chronic maturation of spinal cord scar tissue. J Neurosci Res 71: 427-444.
• Tsubouchi Y, Tsubouchi M, Hitomi S, Ohtsuka A, Murakami T (1996) Perineuronal sulfated proteoglycans in the adult rat brain: histochemical and electron microscopic studies. Acta Med Okayama 50: 237-241.
• Vidal E, Bolea R, Tortosa R, Costa C, Domenech A, Monleon E, Vargas A, Badiola JJ, Pumarola M (2006) Assessment of calcium-binding proteins (Parvalbumin and Calbindin D-28K) and perineuronal nets in normal and scrapie-af- fected adult sheep brains. J Virol Methods 136: 137-146.
• Weber P, Bartsch U, Rasband MN, Czaniera R, Lang Y, Bluethmann H, Margolis RU, Levinson SR, Shrager P, Montag D, Schachner M (1999) Mice deficient for tenas- cin-R display alterations of the extracellular matrix and decreased axonal conduction velocities in the CNS. J Neurosci 19: 4245-4262.
• Wegner F, Härtig W, Bringmann A, Grosche J, Wohlfarth K, Zuschratter W, Brückner G (2003) Diffuse perineuronal nets and modified pyramidal cells immunoreactive for glutamate and the GABA(A) receptor alpha1 subunit form a unique entity in rat cerebral cortex. Exp Neurol 184: 705-714.
• Wintergerst ES, Vogt Weisenhorn DM, Rathjen FG, Riederer BM, Lambert S, Celio MR (1996) Temporal and spatial appearance of the membrane cytoskeleton and perineuronal nets in the rat neocortex. Neurosci Lett 209: 173-176.
• Wojcik L, Sawicka A, Rivera S, Zalewska T (2009) Neurogenesis in gerbil hippocampus following brain ischemia: focus on the involvement of metalloproteinas- es. Acta Neurobiol Exp (Wars) 69: 52-61.
• Yamaguchi Y (1996) Brevican: a major proteoglycan in adult brain. Perspect Dev Neurobiol 3: 307-317.
• Yamaguchi Y (2000) Lecticans: organizers of the brain extracellular matrix. Cell Mol Life Sci 57: 276-289.
• Zhou XH, Brakebusch C, Matthies H, Oohashi T, Hirsch E, Moser M, Krug M, Seidenbecher CI, Boeckers TM, Rauch U, Buettner R, Gundelfinger ED, Fässler R (2001) Neurocan is dispensable for brain development. Mol Cell Biol 21: 5970-5978.
• Zimmermann DR, Dours-Zimmermann MT (2008) Extracellular matrix of the central nervous system: from neglect to challenge. Histochem Cell Biol 130: 635-653.

Uwagi

PL

Rekord w opracowaniu