Top

Published in:

01-01-2017 | Original Article

The extracellular matrix glycoprotein tenascin-C and matrix metalloproteinases modify cerebellar structural plasticity by exposure to an enriched environment

Authors: Vera Stamenkovic, Stefan Stamenkovic, Tomasz Jaworski, Maciej Gawlak, Milos Jovanovic, Igor Jakovcevski, Grzegorz M. Wilczynski, Leszek Kaczmarek, Melitta Schachner, Lidija Radenovic, Pavle R. Andjus

Published in: Brain Structure and Function | Issue 1/2017

Abstract

The importance of the extracellular matrix (ECM) glycoprotein tenascin-C (TnC) and the ECM degrading enzymes, matrix metalloproteinases (MMPs) -2 and -9, in cerebellar histogenesis is well established. This study aimed to examine whether there is a functional relationship between these molecules in regulating structural plasticity of the lateral deep cerebellar nucleus. To this end, starting from postnatal day 21, TnC- or MMP-9-deficient mice were exposed to an enriched environment (EE). We show that 8 weeks of exposure to EE leads to reduced lectin-based staining of perineuronal nets (PNNs), reduction in the size of GABAergic and increase in the number and size of glutamatergic synaptic terminals in wild-type mice. Conversely, TnC-deficient mice showed reduced staining of PNNs compared to wild-type mice maintained under standard conditions, and exposure to EE did not further reduce, but even slightly increased PNN staining. EE did not affect the densities of the two types of synaptic terminals in TnC-deficient mice, while the size of inhibitory, but not excitatory synaptic terminals was increased. In the time frame of 4–8 weeks, MMP-9, but not MMP-2, was observed to influence PNN remodeling and cerebellar synaptic plasticity as revealed by measurement of MMP-9 activity and colocalization with PNNs and synaptic markers. These findings were supported by observations on MMP-9-deficient mice. The present study suggests that TnC contributes to the regulation of structural plasticity in the cerebellum and that interactions between TnC and MMP-9 are likely to be important for these processes to occur.

Available only for authorised users

Andjus PR, Bajic A, Zhu L, Schachner M, Strata P (2005) Short-term facilitation and depression in the cerebellum: some observations on wild-type and mutant rodents deficient in the extracellular matrix molecule tenascin C. Ann N Y Acad Sci 1048:185–197PubMedCrossRef

Andrews MR, Czvitkovich S, Dassie E, Vogelaar CF, Faissner A, Blits B, Gage FH, ffrench-Constant C, Fawcett JW (2009) Alpha9 integrin promotes neurite outgrowth on tenascin-C and enhances sensory axon regeneration. J Neurosci 29:5546–5557PubMedCrossRef

Ayoub AE, Cai TQ, Kaplan RA, Luo J (2005) Developmental expression of matrix metalloproteinases 2 and 9 and their potential role in the histogenesis of the cerebellar cortex. J Comp Neurol 481:403–415PubMedCrossRef

Baroncelli L, Braschi C, Spolidoro M, Begenisic T, Sale A, Maffei L (2010) Nurturing brain plasticity: impact of environmental enrichment. Cell Death Differ 17:1092–1103PubMedCrossRef

Bartsch S, Bartsch U, Dorries U, Faissner A, Weller A, Ekblom P, Schachner M (1992) Expression of tenascin in the developing and adult cerebellar cortex. J Neurosci 12:736–749PubMed

Bauer DJ, Kerr AL, Swain RA (2011) Cerebellar dentate nuclei lesions reduce motivation in appetitive operant conditioning and open field exploration. Neurobiol Learn Mem 95:166–175PubMedCrossRef

Begenisic T, Spolidoro M, Braschi C, Baroncelli L, Milanese M, Pietra G, Fabbri ME, Bonanno G, Cioni G, Maffei L, Sale A (2011) Environmental enrichment decreases GABAergic inhibition and improves cognitive abilities, synaptic plasticity, and visual functions in a mouse model of Down syndrome. Front Cell Neurosci 5:29PubMedPubMedCentralCrossRef

Begenisic T, Baroncelli L, Sansevero G, Milanese M, Bonifacino T, Bonanno G, Cioni G, Maffei L, Sale A (2014) Fluoxetine in adulthood normalizes GABA release and rescues hippocampal synaptic plasticity and spatial memory in a mouse model of Down syndrome. Neurobiol Dis 63:12–19PubMedCrossRef

Bruckner G, Grosche J, Schmidt S, Hartig W, Margolis RU, Delpech B, Seidenbecher CI, Czaniera R, Schachner M (2000) Postnatal development of perineuronal nets in wild-type mice and in a mutant deficient in tenascin-R. J Comp Neurol 428:616–629PubMedCrossRef

Cancedda L, Putignano E, Sale A, Viegi A, Berardi N, Maffei L (2004) Acceleration of visual system development by environmental enrichment. J Neurosci 24:4840–4848PubMedCrossRef

Cao W, Duan J, Wang X, Zhong X, Hu Z, Huang F, Wang H, Zhang J, Li F, Zhang J, Luo X, Li CQ (2014) Early enriched environment induces an increased conversion of proBDNF to BDNF in the adult rat’s hippocampus. Behav Brain Res 265:76–83PubMedCrossRef

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 494:559–577PubMedCrossRef

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 501:83–94PubMedCrossRef

Carulli D, Foscarin S, Rossi F (2011) Activity-dependent plasticity and gene expression modifications in the adult CNS. Front Mol Neurosci 4:50PubMedPubMedCentralCrossRef

Carulli D, Foscarin S, Faralli A, Pajaj E, Rossi F (2013) Modulation of semaphorin3A in perineuronal nets during structural plasticity in the adult cerebellum. Mol Cell Neurosci 57:10–22PubMedCrossRef

Cauwe B, Opdenakker G (2010) Intracellular substrate cleavage: a novel dimension in the biochemistry, biology and pathology of matrix metalloproteinases. Crit Rev Biochem Mol Biol 45:351–423PubMedCrossRef

Chen J, Joon Lee H, Jakovcevski I, Shah R, Bhagat N, Loers G, Liu HY, Meiners S, Taschenberger G, Kugler S, Irintchev A, Schachner M (2010) The extracellular matrix glycoprotein tenascin-C is beneficial for spinal cord regeneration. Mol Ther 18:1769–1777PubMedPubMedCentralCrossRef

Costa DA, Cracchiolo JR, Bachstetter AD, Hughes TF, Bales KR, Paul SM, Mervis RF, Arendash GW, Potter H (2007) Enrichment improves cognition in AD mice by amyloid-related and unrelated mechanisms. Neurobiol Aging 28:831–844PubMedCrossRef

Dang D, Yang Y, Li X, Atakilit A, Regezi J, Eisele D, Ellis D, Ramos DM (2004) Matrix metalloproteinases and TGFbeta1 modulate oral tumor cell matrix. Biochem Biophys Res Commun 316:937–942PubMedCrossRef

Day JM, Olin AI, Murdoch AD, Canfield A, Sasaki T, Timpl R, Hardingham TE, Aspberg A (2004) Alternative splicing in the aggrecan G3 domain influences binding interactions with tenascin-C and other extracellular matrix proteins. J Biol Chem 279:12511–12518PubMedCrossRef

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 281:17789–17800PubMedCrossRef

Dityatev A, Schachner M (2003) Extracellular matrix molecules and synaptic plasticity. Nat Rev Neurosci 4:456–468PubMedCrossRef

Dityatev A, Schachner M (2006) The extracellular matrix and synapses. Cell Tissue Res 326:647–654PubMedCrossRef

Dityatev A, Bruckner 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 67:570–588PubMedCrossRef

Dityatev A, Schachner M, Sonderegger P (2010) The dual role of the extracellular matrix in synaptic plasticity and homeostasis. Nat Rev Neurosci 11:735–746PubMedCrossRef

Dobbertin A, Czvitkovich S, Theocharidis U, Garwood J, Andrews MR, Properzi F, Lin R, Fawcett JW, Faissner A (2010) Analysis of combinatorial variability reveals selective accumulation of the fibronectin type III domains B and D of tenascin-C in injured brain. Exp Neurol 225:60–73PubMedCrossRef

Dziembowska M, Milek J, Janusz A, Rejmak E, Romanowska E, Gorkiewicz T, Tiron A, Bramham CR, Kaczmarek L (2012) Activity-dependent local translation of matrix metalloproteinase-9. J Neurosci 32:14538–14547PubMedCrossRef

Evers MR, Salmen B, Bukalo O, Rollenhagen A, Bosl MR, Morellini F, Bartsch U, Dityatev A, Schachner M (2002) Impairment of L-type Ca²⁺ channel-dependent forms of hippocampal synaptic plasticity in mice deficient in the extracellular matrix glycoprotein tenascin-C. J Neurosci 22:7177–7194PubMed

Faherty CJ, Raviie Shepherd K, Herasimtschuk A, Smeyne RJ (2005) Environmental enrichment in adulthood eliminates neuronal death in experimental Parkinsonism. Brain Res Mol Brain Res 134:170–179PubMedCrossRef

Ferhat L, au Chevassus N, Jorquera I, Niquet J, Khrestchatisky M, Ben Y, Represa A (1996) Transient increase of tenascin-C in immature hippocampus: astroglial and neuronal expression. J Neurocytol 25:53–66PubMedCrossRef

Foscarin S, Ponchione D, Pajaj E, Leto K, Gawlak M, Wilczynski GM, Rossi F, Carulli D (2011) Experience-dependent plasticity and modulation of growth regulatory molecules at central synapses. PLoS One 6:e16666PubMedPubMedCentralCrossRef

Foti F, Laricchiuta D, Cutuli D, De Bartolo P, Gelfo F, Angelucci F, Petrosini L (2011) Exposure to an enriched environment accelerates recovery from cerebellar lesion. Cerebellum 10:104–119PubMedCrossRef

Franz M, Berndt A, Neri D, Galler K, Grun K, Porrmann C, Reinbothe F, Mall G, Schlattmann P, Renner A, Figulla HR, Jung C, Kuthe F (2013) Matrix metalloproteinase-9, tissue inhibitor of metalloproteinase-1, B(+) tenascin-C and ED-A(+) fibronectin in dilated cardiomyopathy: potential impact on disease progression and patients’ prognosis. Int J Cardiol 168:5344–5351PubMedCrossRef

Gall CM, Pinkstaff JK, Lauterborn JC, Xie Y, Lynch G (2003) Integrins regulate neuronal neurotrophin gene expression through effects on voltage-sensitive calcium channels. Neuroscience 118:925–940PubMedCrossRef

Galtrey CM, Kwok JC, Carulli D, Rhodes KE, Fawcett JW (2008) Distribution and synthesis of extracellular matrix proteoglycans, hyaluronan, link proteins and tenascin-R in the rat spinal cord. Eur J Neurosci 27:1373–1390PubMedCrossRef

Gawlak M, Gorkiewicz T, Gorlewicz A, Konopacki FA, Kaczmarek L, Wilczynski GM (2009) High resolution in situ zymography reveals matrix metalloproteinase activity at glutamatergic synapses. Neuroscience 158:167–176PubMedCrossRef

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 67:888–899PubMedCrossRef

Grumet M, Milev P, Sakurai T, Karthikeyan L, Bourdon M, Margolis RK, Margolis RU (1994) Interactions with tenascin and differential effects on cell adhesion of neurocan and phosphacan, two major chondroitin sulfate proteoglycans of nervous tissue. J Biol Chem 269:12142–12146PubMed

Guntinas-Lichius O, Angelov DN, Morellini F, Lenzen M, Skouras E, Schachner M, Irintchev A (2005) Opposite impacts of tenascin-C and tenascin-R deficiency in mice on the functional outcome of facial nerve repair. Eur J Neurosci 22:2171–2179PubMedCrossRef

Harauzov A, Spolidoro M, DiCristo G, De Pasquale R, Cancedda L, Pizzorusso T, Viegi A, Berardi N, Maffei L (2010) Reducing intracortical inhibition in the adult visual cortex promotes ocular dominance plasticity. J Neurosci 30:361–371PubMedCrossRef

Haunso A, Ibrahim M, Bartsch U, Letiembre M, Celio MR, Menoud P (2000) Morphology of perineuronal nets in tenascin-R and parvalbumin single and double knockout mice. Brain Res 864:142–145PubMedCrossRef

Horii-Hayashi N, Sasagawa T, Matsunaga W, Nishi M (2015) Development and structural variety of the chondroitin sulfate proteoglycans-contained extracellular matrix in the mouse brain. Neural Plast 2015:256389PubMedPubMedCentral

Husmann K, Faissner A, Schachner M (1992) Tenascin promotes cerebellar granule cell migration and neurite outgrowth by different domains in the fibronectin type III repeats. J Cell Biol 116:1475–1486PubMedCrossRef

Imai K, Kusakabe M, Sakakura T, Nakanishi I, Okada Y (1994) Susceptibility of tenascin to degradation by matrix metalloproteinases and serine proteinases. FEBS Lett 352:216–218PubMedCrossRef

Irintchev A, Rollenhagen A, Troncoso E, Kiss JZ, Schachner M (2005) Structural and functional aberrations in the cerebral cortex of tenascin-C deficient mice. Cereb Cortex 15:950–962PubMedCrossRef

Jasinska M, Milek J, Cymerman IA, Leski S, Kaczmarek L, Dziembowska M (2015) miR-132 regulates dendritic spine structure by direct targeting of matrix metalloproteinase 9 mRNA. Mol Neurobiol. doi:10.1007/s12035-015-9383-z PubMedPubMedCentral

Joyal CC, Strazielle C, Lalonde R (2001) Effects of dentate nucleus lesions on spatial and postural sensorimotor learning in rats. Behav Brain Res 122:131–137PubMedCrossRef

Kalembeyi I, Inada H, Nishiura R, Imanaka-Yoshida K, Sakakura T, Yoshida T (2003) Tenascin-C upregulates matrix metalloproteinase-9 in breast cancer cells: direct and synergistic effects with transforming growth factor beta1. Int J Cancer 105:53–60PubMedCrossRef

Keyvani K, Sachser N, Witte OW, Paulus W (2004) Gene expression profiling in the intact and injured brain following environmental enrichment. J Neuropathol Exp Neurol 63:598–609PubMedCrossRef

Kuriyama N, Duarte S, Hamada T, Busuttil RW, Coito AJ (2011) Tenascin-C: a novel mediator of hepatic ischemia and reperfusion injury. Hepatology 54:2125–2136PubMedPubMedCentralCrossRef

Kwok JC, Dick G, Wang D, Fawcett JW (2011) Extracellular matrix and perineuronal nets in CNS repair. Dev Neurobiol 71:1073–1089PubMedCrossRef

Leggio MG, Mandolesi L, Federico F, Spirito F, Ricci B, Gelfo F, Petrosini L (2005) Environmental enrichment promotes improved spatial abilities and enhanced dendritic growth in the rat. Behav Brain Res 163:78–90PubMedCrossRef

Li S, Tian X, Hartley DM, Feig LA (2006) The environment versus genetics in controlling the contribution of MAP kinases to synaptic plasticity. Curr Biol 16:2303–2313PubMedCrossRef

Liu HY, Nur EKA, Schachner M, Meiners S (2005) Neurite guidance by the FnC repeat of human tenascin-C: neurite attraction vs. neurite retention. Eur J Neurosci 22:1863–1872PubMedCrossRef

Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275PubMed

Lu P, Takai K, Weaver VM, Werb Z (2011) Extracellular matrix degradation and remodeling in development and disease. Cold Spring Harb Perspect Biol 3:a005058PubMedPubMedCentralCrossRef

Luo J (2005) The role of matrix metalloproteinases in the morphogenesis of the cerebellar cortex. Cerebellum 4:239–245PubMedCrossRef

Mandolesi L, De Bartolo P, Foti F, Gelfo F, Federico F, Leggio MG, Petrosini L (2008) Environmental enrichment provides a cognitive reserve to be spent in the case of brain lesion. J Alzheimers Dis 15:11–28PubMed

Mataga N, Mizuguchi Y, Hensch TK (2004) Experience-dependent pruning of dendritic spines in visual cortex by tissue plasminogen activator. Neuron 44:1031–1041PubMedCrossRef

Michaluk P, Kolodziej L, Mioduszewska B, Wilczynski GM, Dzwonek J, Jaworski J, Gorecki DC, Ottersen OP, Kaczmarek L (2007) Beta-dystroglycan as a target for MMP-9, in response to enhanced neuronal activity. J Biol Chem 282:16036–16041PubMedCrossRef

Michaluk P, Mikasova L, Groc L, Frischknecht R, Choquet D, Kaczmarek L (2009) Matrix metalloproteinase-9 controls NMDA receptor surface diffusion through integrin beta1 signaling. J Neurosci 29:6007–6012PubMedCrossRef

Michaluk P, Wawrzyniak M, Alot P, Szczot M, Wyrembek P, Mercik K, Medvedev N, Wilczek E, De Roo M, Zuschratter W, Muller D, Wilczynski GM, Mozrzymas JW, Stewart MG, Kaczmarek L, Wlodarczyk J (2011) Influence of matrix metalloproteinase MMP-9 on dendritic spine morphology. J Cell Sci 124:3369–3380PubMedCrossRef

Milev P, Fischer D, Haring M, Schulthess T, Margolis RK, Chiquet-Ehrismann R, Margolis RU (1997) The fibrinogen-like globe of tenascin-C mediates its interactions with neurocan and phosphacan/protein-tyrosine phosphatase-zeta/beta. J Biol Chem 272:15501–15509PubMedCrossRef

Mizoguchi H, Nakade J, Tachibana M, Ibi D, Someya E, Koike H, Kamei H, Nabeshima T, Itohara S, Takuma K, Sawada M, Sato J, Yamada K (2011) Matrix metalloproteinase-9 contributes to kindled seizure development in pentylenetetrazole-treated mice by converting pro-BDNF to mature BDNF in the hippocampus. J Neurosci 31:12963–12971PubMedCrossRef

Monferran S, Paupert J, Dauvillier S, Salles B, Muller C (2004) The membrane form of the DNA repair protein Ku interacts at the cell surface with metalloproteinase 9. EMBO J 23:3758–3768PubMedPubMedCentralCrossRef

Morawski M, Dityatev A, Hartlage-Rubsamen M, Blosa M, Holzer M, Flach K, Pavlica S, Dityateva G, Grosche J, Bruckner G, Schachner M (2014) Tenascin-R promotes assembly of the extracellular matrix of perineuronal nets via clustering of aggrecan. Philos Trans R Soc Lond B Biol Sci 369:20140046PubMedPubMedCentralCrossRef

Nagase H, Visse R, Murphy G (2006) Structure and function of matrix metalloproteinases and TIMPs. Cardiovasc Res 69:562–573PubMedCrossRef

Nakamura H, Fujii Y, Inoki I, Sugimoto K, Tanzawa K, Matsuki H, Miura R, Yamaguchi Y, Okada Y (2000) Brevican is degraded by matrix metalloproteinases and aggrecanase-1 (ADAMTS4) at different sites. J Biol Chem 275:38885–38890PubMedCrossRef

Nithianantharajah J, Hannan AJ (2006) Enriched environments, experience-dependent plasticity and disorders of the nervous system. Nat Rev Neurosci 7:697–709PubMedCrossRef

Noblett KL, Swain RA (2003) Pretraining enhances recovery from visuospatial deficit following cerebellar dentate nucleus lesion. Behav Neurosci 117:785–798PubMedCrossRef

Orend G (2005) Potential oncogenic action of tenascin-C in tumorigenesis. Int J Biochem Cell Biol 37:1066–1083PubMedCrossRef

Orend G, Chiquet-Ehrismann R (2006) Tenascin-C induced signaling in cancer. Cancer Lett 244:143–163PubMedCrossRef

Pang PT, Teng HK, Zaitsev E, Woo NT, Sakata K, Zhen S, Teng KK, Yung WH, Hempstead BL, Lu B (2004) Cleavage of proBDNF by tPA/plasmin is essential for long-term hippocampal plasticity. Science 306:487–491PubMedCrossRef

Pesheva P, Probstmeier R (2000) The yin and yang of tenascin-R in CNS development and pathology. Prog Neurobiol 61:465–493PubMedCrossRef

Peter NR, Shah RT, Chen J, Irintchev A, Schachner M (2012) Adhesion molecules close homolog of L1 and tenascin-C affect blood-spinal cord barrier repair. Neuroreport 23:479–482PubMedCrossRef

Peterson TC, Villatoro L, Arneson T, Ahuja B, Voss S, Swain RA (2012) Behavior modification after inactivation of cerebellar dentate nuclei. Behav Neurosci 126:551–562PubMedCrossRef

Pizzorusso T, Medini P, Berardi N, Chierzi S, Fawcett JW, Maffei L (2002) Reactivation of ocular dominance plasticity in the adult visual cortex. Science 298:1248–1251PubMedCrossRef

Pollock E, Everest M, Brown A, Poulter MO (2014) Metalloproteinase inhibition prevents inhibitory synapse reorganization and seizure genesis. Neurobiol Dis 70:21–31PubMedCrossRef

Rampon C, Jiang CH, Dong H, Tang YP, Lockhart DJ, Schultz PG, Tsien JZ, Hu Y (2000) Effects of environmental enrichment on gene expression in the brain. Proc Natl Acad Sci USA 97:12880–12884PubMedPubMedCentralCrossRef

Rauch U, Clement A, Retzler C, Fröhlich L, Fässler R, Göhring W, Faissner A (1997) Mapping of a defined neurocan binding site to distinct domains of tenascin-C. J Biol Chem 272:26905–26912PubMedCrossRef

Reeves TM, Prins ML, Zhu J, Povlishock JT, Phillips LL (2003) Matrix metalloproteinase inhibition alters functional and structural correlates of deafferentation-induced sprouting in the dentate gyrus. J Neurosci 23:10182–10189PubMed

Reimers S, Hartlage-Rubsamen M, Bruckner G, Rossner S (2007) Formation of perineuronal nets in organotypic mouse brain slice cultures is independent of neuronal glutamatergic activity. Eur J Neurosci 25:2640–2648PubMedCrossRef

Sale A, Maya Vetencourt JF, Medini P, Cenni MC, Baroncelli L, De Pasquale R, Maffei L (2007) Environmental enrichment in adulthood promotes amblyopia recovery through a reduction of intracortical inhibition. Nat Neurosci 10:679–681PubMedCrossRef

Sale A, Berardi N, Maffei L (2009) Enrich the environment to empower the brain. Trends Neurosci 32:233–239PubMedCrossRef

Scali M, Begenisic T, Mainardi M, Milanese M, Bonifacino T, Bonanno G, Sale A, Maffei L (2013) Fluoxetine treatment promotes functional recovery in a rat model of cervical spinal cord injury. Sci Rep 3:2217PubMedPubMedCentralCrossRef

Sekeljic V, Andjus PR (2012) Tenascin-C and its functions in neuronal plasticity. Int J Biochem Cell Biol 44:825–829PubMedCrossRef

Siri A, Knauper V, Veirana N, Caocci F, Murphy G, Zardi L (1995) Different susceptibility of small and large human tenascin-C isoforms to degradation by matrix metalloproteinases. J Biol Chem 270:8650–8654PubMedCrossRef

Srinivasan J, Schachner M, Catterall WA (1998) Interaction of voltage-gated sodium channels with the extracellular matrix molecules tenascin-C and tenascin-R. Proc Natl Acad Sci USA 95:15753–15757PubMedPubMedCentralCrossRef

Stawarski M, Stefaniuk M, Wlodarczyk J (2014) Matrix metalloproteinase-9 involvement in the structural plasticity of dendritic spines. Front Neuroanat 8:68PubMedPubMedCentralCrossRef

Stegemann C, Didangelos A, Barallobre-Barreiro J, Langley SR, Mandal K, Jahangiri M, Mayr M (2013) Proteomic identification of matrix metalloproteinase substrates in the human vasculature. Circ Cardiovasc Genet 6:106–117PubMedCrossRef

Szklarczyk A, Lapinska J, Rylski M, McKay RD, Kaczmarek L (2002) Matrix metalloproteinase-9 undergoes expression and activation during dendritic remodeling in adult hippocampus. J Neurosci 22:920–930PubMed

Tsilibary E, Tzinia A, Radenovic L, Stamenkovic V, Lebitko T, Mucha M, Pawlak R, Frischknecht R, Kaczmarek L (2014) Neural ECM proteases in learning and synaptic plasticity. Prog Brain Res 214:135–157PubMedCrossRef

Turk BE, Huang LL, Piro ET, Cantley LC (2001) Determination of protease cleavage site motifs using mixture-based oriented peptide libraries. Nat Biotechnol 19:661–667PubMedCrossRef

Uusisaari M, Knopfel T (2011) Functional classification of neurons in the mouse lateral cerebellar nuclei. Cerebellum 10:637–646PubMedCrossRef

Vaillant C, Didier-Bazes M, Hutter A, Belin MF, Thomasset N (1999) Spatiotemporal expression patterns of metalloproteinases and their inhibitors in the postnatal developing rat cerebellum. J Neurosci 19:4994–5004PubMed

Vaillant C, Meissirel C, Mutin M, Belin MF, Lund LR, Thomasset N (2003) MMP-9 deficiency affects axonal outgrowth, migration, and apoptosis in the developing cerebellum. Mol Cell Neurosci 24:395–408PubMedCrossRef

van der Kooij MA, Fantin M, Rejmak E, Grosse J, Zanoletti O, Fournier C, Ganguly K, Kalita K, Kaczmarek L, Sandi C (2014) Role for MMP-9 in stress-induced downregulation of nectin-3 in hippocampal CA1 and associated behavioural alterations. Nat Commun 5:4995PubMedPubMedCentralCrossRef

Vu TH, Shipley JM, Bergers G, Berger JE, Helms JA, Hanahan D, Shapiro SD, Senior RM, Werb Z (1998) MMP-9/gelatinase B is a key regulator of growth plate angiogenesis and apoptosis of hypertrophic chondrocytes. Cell 93:411–422PubMedPubMedCentralCrossRef

Wang D, Fawcett J (2012) The perineuronal net and the control of CNS plasticity. Cell Tissue Res 349:147–160PubMedCrossRef

Wang XB, Bozdagi O, Nikitczuk JS, Zhai ZW, Zhou Q, Huntley GW (2008) Extracellular proteolysis by matrix metalloproteinase-9 drives dendritic spine enlargement and long-term potentiation coordinately. Proc Natl Acad Sci USA 105:19520–19525PubMedPubMedCentralCrossRef

Wilczynski GM, Konopacki FA, Wilczek E, Lasiecka Z, Gorlewicz A, Michaluk P, Wawrzyniak M, Malinowska M, Okulski P, Kolodziej LR, Konopka W, Duniec K, Mioduszewska B, Nikolaev E, Walczak A, Owczarek D, Gorecki DC, Zuschratter W, Ottersen OP, Kaczmarek L (2008) Important role of matrix metalloproteinase 9 in epileptogenesis. J Cell Biol 180:1021–1035PubMedPubMedCentralCrossRef

Xu Y, Li Z, Jiang P, Wu G, Chen K, Zhang X, Li X (2015) The co-expression of MMP-9 and Tenascin-C is significantly associated with the progression and prognosis of pancreatic cancer. Diagn Pathol 10:211PubMedPubMedCentralCrossRef

Yamada J, Jinno S (2013) Spatio-temporal differences in perineuronal net expression in the mouse hippocampus, with reference to parvalbumin. Neuroscience 253:368–379PubMedCrossRef

Yang Y, Candelario-Jalil E, Thompson JF, Cuadrado E, Estrada EY, Rosell A, Montaner J, Rosenberg GA (2010) Increased intranuclear matrix metalloproteinase activity in neurons interferes with oxidative DNA repair in focal cerebral ischemia. J Neurochem 112:134–149PubMedCrossRef

Ye Q, Miao QL (2013) Experience-dependent development of perineuronal nets and chondroitin sulfate proteoglycan receptors in mouse visual cortex. Matrix Biol 32:352–363PubMedCrossRef

Yu YM, Cristofanilli M, Valiveti A, Ma L, Yoo M, Morellini F, Schachner M (2011) The extracellular matrix glycoprotein tenascin-C promotes locomotor recovery after spinal cord injury in adult zebrafish. Neuroscience 183:238–250PubMedCrossRef

Zhou X, Panizzutti R, de Villers-Sidani E, Madeira C, Merzenich MM (2011) Natural restoration of critical period plasticity in the juvenile and adult primary auditory cortex. J Neurosci 31:5625–5634PubMedPubMedCentralCrossRef

Zink D, Fischer AH, Nickerson JA (2004) Nuclear structure in cancer cells. Nat Rev Cancer 4:677–687PubMedCrossRef

Title: The extracellular matrix glycoprotein tenascin-C and matrix metalloproteinases modify cerebellar structural plasticity by exposure to an enriched environment
Authors: Vera Stamenkovic
Stefan Stamenkovic
Tomasz Jaworski
Maciej Gawlak
Milos Jovanovic
Igor Jakovcevski
Grzegorz M. Wilczynski
Leszek Kaczmarek
Melitta Schachner
Lidija Radenovic
Pavle R. Andjus
Publication date: 01-01-2017
Publisher: Springer Berlin Heidelberg
Published in: Brain Structure and Function / Issue 1/2017
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI: https://doi.org/10.1007/s00429-016-1224-y

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

The extracellular matrix glycoprotein tenascin-C and matrix metalloproteinases modify cerebellar structural plasticity by exposure to an enriched environment

Abstract

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 1/2017

Distribution of growth hormone-responsive cells in the mouse brain

Oxidative and nitrosative stress pathways in the brain of socially isolated adult male rats demonstrating depressive- and anxiety-like symptoms

Cerebellar sub-divisions differ in exercise-induced plasticity of noradrenergic axons and in their association with resilience to activity-based anorexia

Meta-analytic connectivity modeling of the human superior temporal sulcus

Forward masking in the superior paraolivary nucleus of the rat

Sex differences in impulsivity and brain morphometry in methamphetamine users