Home Chondroitin sulfate proteoglycans: key modulators of neuronal plasticity, long-term memory, neurodegenerative, and psychiatric disorders
Article
Licensed
Unlicensed Requires Authentication

Chondroitin sulfate proteoglycans: key modulators of neuronal plasticity, long-term memory, neurodegenerative, and psychiatric disorders

  • Xin Yang ORCID logo EMAIL logo
Published/Copyright: March 3, 2020
Become an author with De Gruyter Brill

Abstract

The chondroitin sulfate proteoglycans (CSPGs) are large groups of heterogenous proteoglycans that are mainly expressed by reactive astrocytes in the central nervous system (CNS). They share similar core proteins and are post-transcriptionally modified by chondroitin sulfate glycosaminoglycans. CSPGs are the major components of the perineuronal nets (PNN) that regulate the opening and closure of the critical period. Mounting reports have documented the crucial roles of CSPGs in restricting neuronal plasticity, axonal growth, and pathfinding during development as well as axonal regeneration after CNS injury. Moreover, CSPGs and PNNs modulate long-term memory, which impairments frequently happened in several neurodegenerative and psychiatric disorders. This review will shortly introduce the expression patterns of CSPGs during development and after injury, the PNNs constitutions, the roles of CSPGs and PNNs in axonal regrowth, discuss the most recently identified roles of CSPGs and PNNs in mediating long-term memory and their correlation with brain disorders, and finally, propose a short perspective of future investigations. Hopefully, further explorations may validate the therapeutic potentials of PNNs and CSPGs.

  1. Conflict of interest statement: There is no conflict of interest.

References

Albiñana, E., Gutierrez-Luengo, J., Hernández-Juarez, N., Baraibar, A.M., Montell, E., Vergés, J., García, A.G., and Hernández-Guijo, J.M. (2015). Chondroitin sulfate induces depression of synaptic transmission and modulation of neuronal plasticity in rat hippocampal slices. Neural Plasticity 2015, 1–12.10.1155/2015/463854Search in Google Scholar

Anderson, M.A., Burda, J.E., Ren, Y., Ao, Y., O’Shea, T.M., Kawaguchi, R., Coppola, G., Khakh, B.S., Deming, T.J., and Sofroniew, M.V., 2016. Astrocyte scar formation aids central nervous system axon regeneration. Nature 532, 195–200.10.1038/nature17623Search in Google Scholar

Andrews, E.M., Richards, R.J., Yin, F.Q., Viapiano, M.S., and Jakeman, L.B. (2012). Alterations in chondroitin sulfate proteoglycan expression occur both at and far from the site of spinal contusion injury. Exp. Neurol. 235, 174–187.10.1016/j.expneurol.2011.09.008Search in Google Scholar

Banerjee, S.B., Gutzeit, V.A., Baman, J., Aoued, H.S., Doshi, N.K., Liu, R.C., and Ressler, K.J. (2017). Perineuronal nets in the adult sensory cortex are necessary for fear learning. Neuron 95, 169–179.e3.10.1016/j.neuron.2017.06.007Search in Google Scholar

Beurdeley, M., Spatazza, J., Lee, H.H.C., Sugiyama, S., Bernard, C., Di Nardo, A.A., Hensch, T.K., and Prochiantz, A. (2012). Otx2 binding to perineuronal nets persistently regulates plasticity in the mature visual cortex. J. Neurosci. 32, 9429–9437.10.1523/JNEUROSCI.0394-12.2012Search in Google Scholar

Bradbury, E.J., Moon, L.D.F., Popat, R.J., King, V.R., Bennett, G.S., Patel, P.N., Fawcett, J.W., and McMahon, S.B. (2002). Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature 416, 636–640.10.1038/416636aSearch in Google Scholar

Brakebusch, C., Seidenbecher, C.I., Asztely, F., Rauch, U., Matthies, H., Meyer, H., Krug, M., Bockers, T.M., Zhou, X., Kreutz, M.R., et al. (2002). Brevican-deficient mice display impaired hippocampal CA1 long-term potentiation but show no obvious deficits in learning and memory. Mol. Cell. Biol. 22, 7417–7427.10.1128/MCB.22.21.7417-7427.2002Search in Google Scholar

Brown, J.M., Xia, J., Zhuang, B., Cho, K.-S., Rogers, C.J., Gama, C.I., Rawat, M., Tully, S.E., Uetani, N., Mason, D.E., et al. (2012). A sulfated carbohydrate epitope inhibits axon regeneration after injury. Proc. Natl Acad. Sci. USA 109, 4768–4773.10.1073/pnas.1121318109Search in Google Scholar

Brückner, G., Brauer, K., Härtig, W., Wolff, J.R., Rickmann, M.J., Derouiche, A., Delpech, B., Girard, N., Oertel, W.H., and Reichenbach, A. (1993). Perineuronal nets provide a polyanionic, glia-associated form of microenvironment around certain neurons in many parts of the rat brain: polyanionic perineuronal nets and glia. Glia 8, 183–200.10.1002/glia.440080306Search in Google Scholar

Brückner, G., Bringmann, A., Köppe, G., Härtig, W., and Brauer, K. (1996). In vivo and in vitro labelling of perineuronal nets in rat brain. Brain Res. 720, 84–92.10.1016/0006-8993(96)00152-7Search in Google Scholar

Brückner, G., Hausen, D., Härtig, W., Drlicek, M., Arendt, T., and Brauer, K. (1999). Cortical areas abundant in extracellular matrix chondroitin sulphate proteoglycans are less affected by cytoskeletal changes in Alzheimer’s disease. Neuroscience 92, 791–805.10.1016/S0306-4522(99)00071-8Search in Google Scholar

Busch, S.A., Horn, K.P., Cuascut, F.X., Hawthorne, A.L., Bai, L., Miller, R.H., and Silver, J. (2010). Adult NG2+ cells are permissive to neurite outgrowth and stabilize sensory axons during macrophage-induced axonal dieback after spinal cord injury. J. Neurosci. 30, 255–265.10.1523/JNEUROSCI.3705-09.2010Search in Google Scholar

Cabungcal, J.-H., Steullet, P., Morishita, H., Kraftsik, R., Cuenod, M., Hensch, T.K., and Do, K.Q. (2013). Perineuronal nets protect fast-spiking interneurons against oxidative stress. Proc. Natl Acad. Sci. USA 110, 9130–9135.10.1073/pnas.1300454110Search in Google Scholar

Carstens, K.E., Phillips, M.L., Pozzo-Miller, L., Weinberg, R.J., and Dudek, S.M. (2016). Perineuronal nets suppress plasticity of excitatory synapses on CA2 pyramidal neurons. J. Neurosci. 36,6312–6320.10.1523/JNEUROSCI.0245-16.2016Search in Google Scholar

Carulli, D., Rhodes, K.E., Brown, D.J., Bonnert, T.P., Pollack, S.J., Oliver, K., Strata, P., and Fawcett, J.W. (2006). Composition of perineuronal nets in the adult rat cerebellum and the cellular origin of their components. J. Comp. Neurol. 494, 559–577.10.1002/cne.20822Search in Google Scholar

Carulli, D., Pizzorusso, T., Kwok, J.C.F., Putignano, E., Poli, A., Forostyak, S., Andrews, M.R., Deepa, S.S., Glant, T.T., and Fawcett, J.W. (2010). Animals lacking link protein have attenuated perineuronal nets and persistent plasticity. Brain 133, 2331–2347.10.1093/brain/awq145Search in Google Scholar

Celio, M.R., Spreafico, R., De Biasi, S., and Vitellaro-Zuccarello, L. (1998). Perineuronal nets: past and present. Trends Neurosci. 21, 510–515.10.1016/S0166-2236(98)01298-3Search in Google Scholar

Chelini, G., Pantazopoulos, H., Durning, P., and Berretta, S. (2018). The tetrapartite synapse: a key concept in the pathophysiology of schizophrenia. Eur. Psychiatry 50, 60–69.10.1016/j.eurpsy.2018.02.003Search in Google Scholar PubMed PubMed Central

Cisneros-Franco, J.M., Ouellet, L., Kamal, B., and de Villers-Sidani, E. (2018). A brain without brakes: reduced inhibition is associated with enhanced but dysregulated plasticity in the aged rat auditory cortex. Eneuro 5, ENEURO.0051–18.2018.10.1523/ENEURO.0051-18.2018Search in Google Scholar PubMed PubMed Central

Coles, C.H., Shen, Y., Tenney, A.P., Siebold, C., Sutton, G.C., Lu, W., Gallagher, J.T., Jones, E.Y., Flanagan, J.G., and Aricescu, A.R. (2011). Proteoglycan-specific molecular switch for RPTPσ clustering and neuronal extension. Science 332, 484–488.10.1126/science.1200840Search in Google Scholar PubMed PubMed Central

de Castro, R., Tajrishi, R., Claros, J., and Stallcup, W.B. (2005). Differential responses of spinal axons to transection: influence of the NG2 proteoglycan. Exp. Neurol. 192, 299–309.10.1016/j.expneurol.2004.11.027Search in Google Scholar PubMed

Deepa, S.S., Carulli, D., Galtrey, C., Rhodes, K., Fukuda, J., Mikami, T., Sugahara, K., and Fawcett, J.W. (2006). Composition of perineuronal net extracellular matrix in rat brain: a different disaccharide composition for the net-associated proteoglycans. J. Biol. Chem. 281, 17789–17800.10.1074/jbc.M600544200Search in Google Scholar PubMed

de Vivo, L., Landi, S., Panniello, M., Baroncelli, L., Chierzi, S., Mariotti, L., Spolidoro, M., Pizzorusso, T., Maffei, L., and Ratto, G.M. (2013). Extracellular matrix inhibits structural and functional plasticity of dendritic spines in the adult visual cortex. Nat. Commun. 4, 1484.10.1038/ncomms2491Search in Google Scholar PubMed

Dias, D.O., Kim, H., Holl, D., Werne Solnestam, B., Lundeberg, J., Carlén, M., Göritz, C., and Frisén, J. (2018). Reducing pericyte-derived scarring promotes recovery after spinal cord injury. Cell 173, 153–165.e22.10.1016/j.cell.2018.02.004Search in Google Scholar PubMed PubMed Central

Dickendesher, T.L., Baldwin, K.T., Mironova, Y.A., Koriyama, Y., Raiker, S.J., Askew, K.L., Wood, A., Geoffroy, C.G., Zheng, B., Liepmann, C.D., et al. (2012). NgR1 and NgR3 are receptors for chondroitin sulfate proteoglycans. Nat. Neurosci. 15, 703–712.10.1038/nn.3070Search in Google Scholar PubMed PubMed Central

Dimou, L. and Gallo, V. (2015). NG2-glia and their functions in the central nervous system: NG2-Glia in the CNS. Glia 63, 1429–1451.10.1002/glia.22859Search in Google Scholar PubMed PubMed Central

Du, K., Zheng, S., Zhang, Q., Li, S., Gao, X., Wang, J., Jiangs, L., and Liu, K. (2015). Pten deletion promotes regrowth of corticospinal tract axons 1 year after spinal cord injury. J. Neurosci. 35, 9754–9763.10.1523/JNEUROSCI.3637-14.2015Search in Google Scholar PubMed PubMed Central

Dunah, A.W., Hueske, E., Wyszynski, M., Hoogenraad, C.C., Jaworski, J., Pak, D.T., Simonetta, A., Liu, G., and Sheng, M. (2005). LAR receptor protein tyrosine phosphatases in the development and maintenance of excitatory synapses. Nat. Neurosci. 8, 458–467.10.1038/nn1416Search in Google Scholar PubMed

Dyck, S.M. and Karimi-Abdolrezaee, S. (2015). Chondroitin sulfate proteoglycans: key modulators in the developing and pathologic central nervous system. Exp. Neurol. 269, 169–187.10.1016/j.expneurol.2015.04.006Search in Google Scholar PubMed

Enwright, J.F., Sanapala, S., Foglio, A., Berry, R., Fish, K.N., and Lewis, D.A. (2016). Reduced labeling of parvalbumin neurons and perineuronal nets in the dorsolateral prefrontal cortex of subjects with schizophrenia. Neuropsychopharmacology 41, 2206–2214.10.1038/npp.2016.24Search in Google Scholar PubMed PubMed Central

Favuzzi, E., Marques-Smith, A., Deogracias, R., Winterflood, C.M., Sánchez-Aguilera, A., Mantoan, L., Maeso, P., Fernandes, C., Ewers, H., and Rico, B. (2017). Activity-dependent gating of parvalbumin interneuron function by the perineuronal net protein brevican. Neuron 95, 639–655.e10.10.1016/j.neuron.2017.06.028Search in Google Scholar

Fawcett, J. (2009). Molecular Control of Brain Plasticity and Repair. Progress in Brain Research. (Amsterdam: Elsevier), pp. 501–509.10.1016/S0079-6123(09)17534-9Search in Google Scholar

Filous, A.R., Tran, A., Howell, C.J., Busch, S.A., Evans, T.A., Stallcup, W.B., Kang, S.H., Bergles, D.E., Lee, S., Levine, J.M., et al. (2014). Entrapment via synaptic-like connections between NG2 proteoglycan+ cells and dystrophic axons in the lesion plays a role in regeneration failure after spinal cord injury. J. Neurosci. 34, 16369–16384.10.1523/JNEUROSCI.1309-14.2014Search in Google Scholar PubMed PubMed Central

Fisher, D., Xing, B., Dill, J., Li, H., Hoang, H.H., Zhao, Z., Yang, X.-L., Bachoo, R., Cannon, S., Longo, F.M., et al. (2011). Leukocyte common antigen-related phosphatase is a functional receptor for chondroitin sulfate proteoglycan axon growth inhibitors. J. Neurosci. 31, 14051–14066.10.1523/JNEUROSCI.1737-11.2011Search in Google Scholar PubMed PubMed Central

Foscarin, S., Raha-Chowdhury, R., Fawcett, J.W., and Kwok, J.C.F. (2017). Brain ageing changes proteoglycan sulfation, rendering perineuronal nets more inhibitory. Ageing 9, 1607–1622.10.18632/aging.101256Search in Google Scholar PubMed PubMed Central

Frischknecht, R., Heine, M., Perrais, D., Seidenbecher, C.I., Choquet, D., and Gundelfinger, E.D. (2009). Brain extracellular matrix affects AMPA receptor lateral mobility and short-term synaptic plasticity. Nat. Neurosci. 12, 897–904.10.1038/nn.2338Search in Google Scholar PubMed

Geissler, M., Gottschling, C., Aguado, A., Rauch, U., Wetzel, C.H., Hatt, H., and Faissner, A. (2013). Primary hippocampal neurons, which lack four crucial extracellular matrix molecules, display abnormalities of synaptic structure and function and severe deficits in perineuronal net formation. J. Neurosci. 33, 7742–7755.10.1523/JNEUROSCI.3275-12.2013Search in Google Scholar PubMed PubMed Central

Giamanco, K.A. and Matthews, R.T. (2012). Deconstructing the perineuronal net: cellular contributions and molecular composition of the neuronal extracellular matrix. Neuroscience 218, 367–384.10.1016/j.neuroscience.2012.05.055Search in Google Scholar PubMed PubMed Central

Gogolla, N., Caroni, P., Luthi, A., and Herry, C. (2009). Perineuronal nets protect fear memories from erasure. Science 325, 1258–1261.10.1126/science.1174146Search in Google Scholar PubMed

Han, S.M., Baig, H.S., and Hammarlund, M. (2016). Mitochondria localize to injured axons to support regeneration. Neuron 92, 1308–1323.10.1016/j.neuron.2016.11.025Search in Google Scholar PubMed PubMed Central

Happel, M.F.K., Niekisch, H., Castiblanco Rivera, L.L., Ohl, F.W., Deliano, M., and Frischknecht, R. (2014). Enhanced cognitive flexibility in reversal learning induced by removal of the extracellular matrix in the auditory cortex. Proc. Natl Acad. Sci. USA 111, 2800–2805.10.1073/pnas.1310272111Search in Google Scholar

Härtig, W., Brauer, K., Bigl, V., and Brückner, G. (1994). Chondroitin sulfate proteoglycan-immunoreactivity of lectin-labelled perineuronal nets around parvalbumin-containing neurons. Brain Res. 635, 307–311.10.1016/0006-8993(94)91452-4Search in Google Scholar

Härtig, W., Klein, C., Brauer, K., Schüppel, K.F., Arendt, T., Bigl, V., and Brückner, G. (2001). Hyperphosphorylated protein tau is restricted to neurons devoid of perineuronal nets in the cortex of aged bison. Neurobiol. Aging 22, 25–33.10.1016/S0197-4580(00)00179-2Search in Google Scholar

Hasenöhrl, R.U., Frisch, C., Junghans, U., Müller, H.W., and Huston, J.P. (1995). Facilitation of learning following injection of the chondroitin sulfate proteoglycan biglycan into the vicinity of the nucleus basalis magnocellularis. Behav. Brain Res. 70, 59–67.10.1016/0166-4328(94)00183-GSearch in Google Scholar

Hennig, A., Krueger, R., Mangoura, D., and Schwartz, N.B. (1992). Chondroitin sulfate proteoglycan expression during neuronal development. Cell. Mol. Biol. (Noisy-le-grand) 585–593.Search in Google Scholar

Hirono, M., Watanabe, S., Karube, F., Fujiyama, F., Kawahara, S., Nagao, S., Yanagawa, Y., and Misonou, H. (2018). Perineuronal nets in the deep cerebellar nuclei regulate GABAergic transmission and delay eyeblink conditioning. J. Neurosci. 38, 6130–6144.10.1523/JNEUROSCI.3238-17.2018Search in Google Scholar

Hockfield, S. and McKay, R.D. (1983). A surface antigen expressed by a subset of neurons in the vertebrate central nervous system. Proc. Natl Acad. Sci. USA 80, 5758–5761.10.1073/pnas.80.18.5758Search in Google Scholar

Horn, K.E., Xu, B., Gobert, D., Hamam, B.N., Thompson, K.M., Wu, C.-L., Bouchard, J.-F., Uetani, N., Racine, R.J., Tremblay, M.L., et al. (2012). Receptor protein tyrosine phosphatase sigma regulates synapse structure, function and plasticity: RPTPσ regulates synaptogenesis and plasticity. J. Neurochem. 122, 147–161.10.1111/j.1471-4159.2012.07762.xSearch in Google Scholar

Hossain-Ibrahim, M.K., Rezajooi, K., Stallcup, W.B., Lieberman, A.R., and Anderson, P.N. (2007). Analysis of axonal regeneration in the central and peripheral nervous systems of the NG2-deficient mouse. BMC Neurosci. 8, 80.10.1186/1471-2202-8-80Search in Google Scholar

Huston, J.P., Weth, K., De Souza Silva, A., Junghans, U., Müller, H.W., and Hasenöhrl, R.U. (2000). Facilitation of learning and long-term ventral pallidal–cortical cholinergic activation by proteoglycan biglycan and chondroitin sulfate C. Neuroscience 100, 355–361.10.1016/S0306-4522(00)00270-0Search in Google Scholar

Hylin, M.J., Orsi, S.A., Moore, A.N., and Dash, P.K. (2013). Disruption of the perineuronal net in the hippocampus or medial prefrontal cortex impairs fear conditioning. Learn. Mem. 20, 267–273.10.1101/lm.030197.112Search in Google Scholar PubMed PubMed Central

Jezek, K., Schulz, D., De Souza Silva, M.A., Müller, H.-W., Huston, J.P., and Hasenöhrl, R.U. (2003). Effects of chronic intraventricular infusion of heparin glycosaminoglycan on learning and brain acetylcholine parameters in aged rats. Behav. Brain Res. 147, 115–123.10.1016/S0166-4328(03)00138-4Search in Google Scholar

Jitsuki, S., Nakajima, W., Takemoto, K., Sano, A., Tada, H., Takahashi-Jitsuki, A., and Takahashi, T. (2016). Nogo receptor signaling restricts adult neural plasticity by limiting synaptic AMPA receptor delivery. Cerebral Cortex 26, 427–439.10.1093/cercor/bhv232Search in Google Scholar PubMed PubMed Central

Jones, L.L., Yamaguchi, Y., Stallcup, W.B., and Tuszynski, M.H. (2002). NG2 is a major chondroitin sulfate proteogly can produced after spinal cord injury and is expressed by macrophages and oligodendrocyte progenitors. J. Neurosci. 22,2792–2803.10.1523/JNEUROSCI.22-07-02792.2002Search in Google Scholar

Khoo, G.H., Lin, Y.-T., Tsai, T.-C., and Hsu, K.-S. (2019). Perineuronal nets restrict the induction of long-term depression in the mouse hippocampal CA1 region. Mol. Neurobiol. 56, 6436–6450.10.1007/s12035-019-1526-1Search in Google Scholar PubMed

Kjellén, L. and Lindahl, U. (1991). Proteoglycans: structures and interactions. Annu. Rev. Biochem. 60, 443–475.10.1146/annurev.bi.60.070191.002303Search in Google Scholar PubMed

Ko, J.S., Pramanik, G., Um, J.W., Shim, J.S., Lee, D., Kim, K.H., Chung, G.-Y., Condomitti, G., Kim, H.M., Kim, H., et al. (2015). PTPσ functions as a presynaptic receptor for the glypican-4/LRRTM4 complex and is essential for excitatory synaptic transmission. Proc. Natl Acad. Sci. USA 112, 1874–1879.10.1073/pnas.1410138112Search in Google Scholar PubMed PubMed Central

Kochlamazashvili, G., Henneberger, C., Bukalo, O., Dvoretskova, E., Senkov, O., Lievens, P.M.-J., Westenbroek, R., Engel, A.K., Catterall, W.A., Rusakov, D.A., et al. (2010). The extracellular matrix molecule hyaluronic acid regulates hippocampal synaptic plasticity by modulating postsynaptic L-type Ca2+ channels. Neuron 67, 116–128.10.1016/j.neuron.2010.05.030Search in Google Scholar PubMed PubMed Central

Köppe, G., Brückner, G., Brauer, K., Härtig, W., and Bigl, V. (1997). Developmental patterns of proteoglycan-containing extracellular matrix in perineuronal nets and neuropil of the postnatal rat brain. Cell Tissue Res. 288, 33–41.10.1007/s004410050790Search in Google Scholar PubMed

Krishnan, K., Wang, B.-S., Lu, J., Wang, L., Maffei, A., Cang, J., and Huang, Z.J. (2015). MeCP2 regulates the timing of critical period plasticity that shapes functional connectivity in primary visual cortex. Proc. Natl Acad. Sci. USA 112, E4782–E4791.10.1073/pnas.1506499112Search in Google Scholar PubMed PubMed Central

Kurihara, D. and Yamashita, T. (2012). Chondroitin sulfate proteoglycans down-regulate spine formation in cortical neurons by targeting tropomyosin-related kinase B (TrkB) protein. J. Biol. Chem. 287, 13822–13828.10.1074/jbc.M111.314070Search in Google Scholar PubMed PubMed Central

Kwok, J.C.F., Warren, P., and Fawcett, J.W. (2012). Chondroitin sulfate: a key molecule in the brain matrix. Int. J. Biochem. Cell Biol. 44, 582–586.10.1016/j.biocel.2012.01.004Search in Google Scholar PubMed

Lang, B.T., Cregg, J.M., DePaul, M.A., Tran, A.P., Xu, K., Dyck, S.M., Madalena, K.M., Brown, B.P., Weng, Y.-L., Li, S., et al. (2015). Modulation of the proteoglycan receptor PTPσ promotes recovery after spinal cord injury. Nature 518, 404–408.10.1038/nature13974Search in Google Scholar PubMed PubMed Central

Lee, H., Raiker, S.J., Venkatesh, K., Geary, R., Robak, L.A., Zhang, Y., Yeh, H.H., Shrager, P., and Giger, R.J. (2008). Synaptic function for the nogo-66 receptor NgR1: regulation of dendritic spine morphology and activity-dependent synaptic strength. J. Neurosci. 28, 2753–2765.10.1523/JNEUROSCI.5586-07.2008Search in Google Scholar PubMed PubMed Central

Lensjø, K.K., Christensen, A.C., Tennøe, S., Fyhn, M., and Hafting, T. (2017). Differential expression and cell-type specificity of perineuronal nets in hippocampus, medial entorhinal cortex, and visual cortex examined in the rat and mouse. eNeuro 4, ENEURO.0379–16.2017.10.1523/ENEURO.0379-16.2017Search in Google Scholar PubMed PubMed Central

Levine, J. (1994). Increased expression of the NG2 chondroitin-sulfate proteoglycan after brain injury. J. Neurosci. 14, 4716–4730.10.1523/JNEUROSCI.14-08-04716.1994Search in Google Scholar

Levine, J. (2016). The reactions and role of NG2 glia in spinal cord injury. Brain Res. 1638, 199–208.10.1016/j.brainres.2015.07.026Search in Google Scholar PubMed PubMed Central

Li, Y., Zhang, P., Choi, T.-Y., Park, S.K., Park, H., Lee, E.-J., Lee, D., Roh, J.D., Mah, W., Kim, R., et al. (2015). Splicing-dependent trans-synaptic SALM3–LAR-RPTP interactions regulate excitatory synapse development and locomotion. Cell Rep. 12, 1618–1630.10.1016/j.celrep.2015.08.002Search in Google Scholar PubMed PubMed Central

Li, Y., Li, Z.-X., Jin, T., Wang, Z.-Y., and Zhao, P. (2017). Tau pathology promotes the reorganization of the extracellular matrix and inhibits the formation of perineuronal nets by regulating the expression and the distribution of hyaluronic acid synthases. J. Alzheimer’s Dis. 57, 395–409.10.3233/JAD-160804Search in Google Scholar PubMed PubMed Central

Liu, K., Lu, Y., Lee, J.K., Samara, R., Willenberg, R., Sears-Kraxberger, I., Tedeschi, A., Park, K.K., Jin, D., Cai, B., et al. (2010). PTEN deletion enhances the regenerative ability of adult corticospinal neurons. Nat. Neurosci. 13, 1075–1081.10.1038/nn.2603Search in Google Scholar PubMed PubMed Central

Matthews, R.T., Kelly, G.M., Zerillo, C.A., Gray, G., Tiemeyer, M., and Hockfield, S. (2002). Aggrecan glycoforms contribute to the molecular heterogeneity of perineuronal nets. J. Neurosci. 22, 7536–7547.10.1523/JNEUROSCI.22-17-07536.2002Search in Google Scholar

Mauney, S.A., Athanas, K.M., Pantazopoulos, H., Shaskan, N.,Passeri, E., Berretta, S., and Woo, T.-U.W. (2013). Developmental pattern of perineuronal nets in the human prefrontal cortex and their deficit in schizophrenia. Biol. Psychiatry 74, 427–435.10.1016/j.biopsych.2013.05.007Search in Google Scholar PubMed PubMed Central

McKeon, R., Schreiber, R., Rudge, J., and 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. 11, 3398–3411.10.1523/JNEUROSCI.11-11-03398.1991Search in Google Scholar

McKeon, R.J., Jurynec, M.J., and Buck, C.R. (1999). The chondroitin sulfate proteoglycans neurocan and phosphacan are expressed by reactive astrocytes in the chronic CNS glial scar. J. Neurosci. 19, 10778–10788.10.1523/JNEUROSCI.19-24-10778.1999Search in Google Scholar

McRae, P.A., Rocco, M.M., Kelly, G., Brumberg, J.C., and Matthews, R.T. (2007). Sensory deprivation alters aggrecan and perineuronal net expression in the mouse barrel cortex. J. Neurosci. 27, 5405–5413.10.1523/JNEUROSCI.5425-06.2007Search in Google Scholar PubMed PubMed Central

McRae, P.A., Baranov, E., Sarode, S., Brooks-Kayal, A.R., and Porter, B.E. (2010). Aggrecan expression, a component of the inhibitory interneuron perineuronal net, is altered following an early-life seizure. Neurobiol. Dis. 39, 439–448.10.1016/j.nbd.2010.05.015Search in Google Scholar PubMed PubMed Central

McTigue, D.M., Wei, P., and Stokes, B.T. (2001). Proliferation of NG2-positive cells and altered oligodendrocyte numbers in the contused rat spinal cord. J. Neurosci. 21, 3392–3400.10.1523/JNEUROSCI.21-10-03392.2001Search in Google Scholar

Mikami, T. and Kitagawa, H. (2013). Biosynthesis and function of chondroitin sulfate. Biochim. Biophys. Acta 1830, 4719–4733.10.1016/j.bbagen.2013.06.006Search in Google Scholar PubMed

Miller, G.M. and Hsieh-Wilson, L.C. (2015). Sugar-dependent modulation of neuronal development, regeneration, and plasticity by chondroitin sulfate proteoglycans. Exp. Neurol. 274, 115–125.10.1016/j.expneurol.2015.08.015Search in Google Scholar PubMed PubMed Central

Miyata, S., Nishimura, Y., and Nakashima, T. (2007). Perineuronal nets protect against amyloid β-protein neurotoxicity in cultured cortical neurons. Brain Res. 1150, 200–206.10.1016/j.brainres.2007.02.066Search in Google Scholar PubMed

Miyata, S., Komatsu, Y., Yoshimura, Y., Taya, C., and Kitagawa, H. (2012). Persistent cortical plasticity by upregulation of chondroitin 6-sulfation. Nat. Neurosci. 15, 414–422.10.1038/nn.3023Search in Google Scholar PubMed

Mizuno, H., Warita, H., Aoki, M., and Itoyama, Y. (2008). Accumulation of chondroitin sulfate proteoglycans in the microenvironment of spinal motor neurons in amyotrophic lateral sclerosis transgenic rats. J. Neurosci. Res. 86, 2512–2523.10.1002/jnr.21702Search in Google Scholar

Mohan, V., Wyatt, E.V., Gotthard, I., Phend, K.D., Diestel, S., Duncan, B.W., Weinberg, R.J., Tripathy, A., and Maness, P.F. (2018). Neurocan inhibits semaphorin 3F induced dendritic spine remodeling through NrCAM in cortical neurons. Front. Cell. Neurosci. 12, 346.10.3389/fncel.2018.00346Search in Google Scholar

Moon, L.D.F., Asher, R.A., Rhodes, K.E., and Fawcett, J.W. (2001). Regeneration of CNS axons back to their target following treatment of adult rat brain with chondroitinase ABC. Nat. Neurosci. 4, 465–466.10.1038/87415Search in Google Scholar

Morawski, M., Brückner, M.K., Riederer, P., Brückner, G., and Arendt, T. (2004). Perineuronal nets potentially protect against oxidative stress. Exp. Neurol. 188, 309–315.10.1016/j.expneurol.2004.04.017Search in Google Scholar

Morawski, M., Brückner, G., Jäger, C., Seeger, G., and Arendt, T. (2010). Neurons associated with aggrecan-based perineuronal nets are protected against tau pathology in subcortical regions in Alzheimer’s disease. Neuroscience 169, 1347–1363.10.1016/j.neuroscience.2010.05.022Search in Google Scholar

Morawski, M., Brückner, G., Jäger, C., Seeger, G., Matthews, R.T., and Arendt, T. (2012). Involvement of perineuronal and pe risynaptic extracellular matrix in Alzheimer’s disease neuropathology: perineuronal and perisynaptic matrix in AD. Brain Pathol. 22, 547–561.10.1111/j.1750-3639.2011.00557.xSearch in Google Scholar

Okamoto, M., Sakiyama, J., Mori, S., Kurazono, S., Usui, S., Hasegawa, M., and Oohira, A. (2003). Kainic acid-induced convulsions cause prolonged changes in the chondroitin sulfate proteoglycans neurocan and phosphacan in the limbic structures. Exp. Neurol. 184, 179–195.10.1016/S0014-4886(03)00251-6Search in Google Scholar

Orlando, C., Ster, J., Gerber, U., Fawcett, J.W., and Raineteau, O. (2012). Perisynaptic chondroitin sulfate proteoglycans restrict structural plasticity in an integrin-dependent manner. J. Neurosci. 32, 18009–18017.10.1523/JNEUROSCI.2406-12.2012Search in Google Scholar PubMed PubMed Central

Pantazopoulos, H., Woo, T.-U.W., Lim, M.P., Lange, N., andBerretta, S. (2010). Extracellular matrix-glial abnormalities in the amygdala and entorhinal cortex of subjects diagnosed with schizophrenia. Arch. Gen. Psychiatry 67, 155.10.1001/archgenpsychiatry.2009.196Search in Google Scholar PubMed PubMed Central

Pantazopoulos, H., Markota, M., Jaquet, F., Ghosh, D., Wallin, A., Santos, A., Caterson, B., and Berretta, S. (2015). Aggrecan and chondroitin-6-sulfate abnormalities in schizophrenia and bipolar disorder: a postmortem study on the amygdala. Transl. Psychiatry 5, e496.10.1038/tp.2014.128Search in Google Scholar PubMed PubMed Central

Park, J.H., Widi, G.A., Gimbel, D.A., Harel, N.Y., Lee, D.H.S., and Strittmatter, S.M. (2006). Subcutaneous nogo receptor removes brain amyloid- and improves spatial memory in Alzheimer’s transgenic mice. J. Neurosci. 26, 13279–13286.10.1523/JNEUROSCI.4504-06.2006Search in Google Scholar PubMed PubMed Central

Paylor, J.W., Wendlandt, E., Freeman, T.S., Greba, Q., Marks, W.N., Howland, J.G., and Winship, I.R. (2018). Impaired cognitive function after perineuronal net degradation in the medial prefrontal cortex. eNeuro 5, ENEURO.0253–18.2018.10.1523/ENEURO.0253-18.2018Search in Google Scholar PubMed PubMed Central

Pearson, C.S., Mencio, C.P., Barber, A.C., Martin, K.R., and Geller, H.M. (2018). Identification of a critical sulfation in chondroitin that inhibits axonal regeneration. eLife 7, e37139.10.7554/eLife.37139Search in Google Scholar PubMed PubMed Central

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, 1248–1251.10.1126/science.1072699Search in Google Scholar PubMed

Pizzorusso, T., Medini, P., Landi, S., Baldini, S., Berardi, N., and Maffei, L. (2006). Structural and functional recovery from early monocular deprivation in adult rats. Proc. Natl Acad. Sci. USA 103, 8517–8522.10.1073/pnas.0602657103Search in Google Scholar PubMed PubMed Central

Rankin-Gee, E.K., McRae, P.A., Baranov, E., Rogers, S., Wandrey, L., and Porter, B.E. (2015). Perineuronal net degradation in epilepsy. Epilepsia 56, 1124–1133.10.1111/epi.13026Search in Google Scholar PubMed

Riga, D., Kramvis, I., Koskinen, M.K., van Bokhoven, P., van der Harst, J.E., Heistek, T.S., Jaap Timmerman, A., van Nierop, P., van der Schors, R.C., Pieneman, A.W., et al. (2017). Hippocampal extracellular matrix alterations contribute to cognitive impairment associated with a chronic depressive-like state in rats. Sci. Transl. Med. 9, eaai8753.10.1126/scitranslmed.aai8753Search in Google Scholar PubMed

Romberg, C., Yang, S., Melani, R., Andrews, M.R., Horner, A.E., Spillantini, M.G., Bussey, T.J., Fawcett, J.W., Pizzorusso, T., and Saksida, L.M. (2013). Depletion of perineuronal nets enhances recognition memory and long-term depression in the perirhinal cortex. J. Neurosci. 33, 7057–7065.10.1523/JNEUROSCI.6267-11.2013Search in Google Scholar PubMed PubMed Central

Rowlands, D., Lensjø, K.K., Dinh, T., Yang, S., Andrews, M.R., Hafting, T., Fyhn, M., Fawcett, J.W., and Dick, G. (2018). Aggrecan directs extracellular matrix-mediated neuronal plasticity. J. Neurosci. 38, 10102–10113.10.1523/JNEUROSCI.1122-18.2018Search in Google Scholar PubMed PubMed Central

Sainath, R., Ketschek, A., Grandi, L., and Gallo, G. (2017). CSPGs inhibit axon branching by impairing mitochondria-dependent regulation of actin dynamics and axonal translation: CSPGs impact mitochondria. Develop. Neurobiol. 77, 454–473.10.1002/dneu.22420Search in Google Scholar PubMed PubMed Central

Sakamoto, K., Ozaki, T., Ko, Y.-C., Tsai, C.-F., Gong, Y., Morozumi, M., Ishikawa, Y., Uchimura, K., Nadanaka, S., Kitagawa, H., et al. (2019). Glycan sulfation patterns define autophagy flux at axon tip via PTPRσ-cortactin axis. Nat. Chem. Biol. 15, 699–709.10.1038/s41589-019-0274-xSearch in Google Scholar PubMed

Sanz, R.L., Ferraro, G.B., Kacervosky, J., Salesse, C., Gowing, E., Hua, L., Rambaldi, I., Beaubien, F., Holmbeck, K., Cloutier, J.F., et al. (2018). MT3-MMP promotes excitatory synapse formation by promoting nogo-66 receptor ectodomain shedding. J. Neurosci. 38, 518–529.10.1523/JNEUROSCI.0962-17.2017Search in Google Scholar PubMed PubMed Central

Sethi, M.K. and Zaia, J. (2017). Extracellular matrix proteomics in schizophrenia and Alzheimer’s disease. Anal. Bioanal. Chem. 409, 379–394.10.1007/s00216-016-9900-6Search in Google Scholar PubMed PubMed Central

Shah, A. and Lodge, D.J. (2013). A loss of hippocampal perineuronal nets produces deficits in dopamine system function: relevance to the positive symptoms of schizophrenia. Transl. Psychiatry 3, e215.10.1038/tp.2012.145Search in Google Scholar PubMed PubMed Central

Sharma, K., Selzer, M.E., and Li, S. (2012). Scar-mediated inhibition and CSPG receptors in the CNS. Exp. Neurol. 237, 370–378.10.1016/j.expneurol.2012.07.009Search in Google Scholar PubMed PubMed Central

Shen, Y., Tenney, A.P., Busch, S.A., Horn, K.P., Cuascut, F.X., Liu, K., He, Z., Silver, J., and Flanagan, J.G. (2009). PTP is a receptor for chondroitin sulfate proteoglycan, an inhibitor of neural regeneration. Science 326, 592–596.10.1126/science.1178310Search in Google Scholar PubMed PubMed Central

Sigal, Y.M., Bae, H., Bogart, L.J., Hensch, T.K., and Zhuang, X. (2019). Structural maturation of cortical perineuronal nets and their perforating synapses revealed by superresolution imaging. Proc. Natl Acad. Sci. USA 116, 7071–7076.10.1073/pnas.1817222116Search in Google Scholar PubMed PubMed Central

Silver, D.J. and Silver, J. (2014). Contributions of chondroitin sulfate proteoglycans to neurodevelopment, injury, and cancer. Curr. Opin. Neurobiol. 27, 171–178.10.1016/j.conb.2014.03.016Search in Google Scholar PubMed PubMed Central

Sorg, B.A., Berretta, S., Blacktop, J.M., Fawcett, J.W., Kitagawa, H., Kwok, J.C.F., and Miquel, M. (2016). Casting a wide net: role of perineuronal nets in neural plasticity. J. Neurosci. 36, 11459–11468.10.1523/JNEUROSCI.2351-16.2016Search in Google Scholar PubMed PubMed Central

Steullet, P., Cabungcal, J.-H., Coyle, J., Didriksen, M., Gill, K., Grace, A.A., Hensch, T.K., LaMantia, A.-S., Lindemann, L., Maynard, T.M., et al. (2017). Oxidative stress-driven parvalbumin interneuron impairment as a common mechanism in models of schizophrenia. Mol. Psychiatry 22, 936–943.10.1038/mp.2017.47Search in Google Scholar PubMed PubMed Central

Steullet, P., Cabungcal, J.-H., Bukhari, S.A., Ardelt, M.I., Pantazopoulos, H., Hamati, F., Salt, T.E., Cuenod, M., Do, K.Q., and Berretta, S. (2018). The thalamic reticular nucleus in schizophrenia and bipolar disorder: role of parvalbumin-expressing neuron networks and oxidative stress. Mol. Psychiatry 23, 2057–2065.10.1038/mp.2017.230Search in Google Scholar PubMed PubMed Central

Suttkus, A., Rohn, S., Weigel, S., Glöckner, P., Arendt, T., and Morawski, M. (2017). Aggrecan, link protein and tenascin-R are essential components of the perineuronal net to protect neurons against iron-induced oxidative stress. Cell Death Dis. 5, e1119.10.1038/cddis.2014.25Search in Google Scholar PubMed PubMed Central

Suzuki, T., Akimoto, M., Imai, H., Ueda, Y., Mandai, M., Yoshimura, N., Swaroop, A., and Takahashi, M. (2007). Chondroitinase ABC treatment enhances synaptogenesis between transplant and host neurons in model of retinal degeneration. Cell Transpl. 16, 493–503.10.3727/000000007783464966Search in Google Scholar PubMed

Takeuchi, K., Yoshioka, N., Higa Onaga, S., Watanabe, Y., Miyata, S., Wada, Y., Kudo, C., Okada, M., Ohko, K., Oda, K., et al. (2013). Chondroitin sulphate N-acetylgalactosaminyl-transferase-1 inhibits recovery from neural injury. Nat. Commun. 4, 2740.10.1038/ncomms3740Search in Google Scholar PubMed PubMed Central

Tan, A.M. (2006). Antibodies against the NG2 proteoglycan promote the regeneration of sensory axons within the dorsal columns of the spinal cord. J. Neurosci. 26, 4729–4739.10.1523/JNEUROSCI.3900-05.2006Search in Google Scholar PubMed PubMed Central

Tang, X., Davies, J.E., and Davies, S.J. (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, 427–444.10.1002/jnr.10523Search in Google Scholar PubMed

Thompson, E.H., Lensjø, K.K., Wigestrand, M.B., Malthe-Sørenssen, A., Hafting, T., and Fyhn, M. (2018). Removal of perineuronal nets disrupts recall of a remote fear memory. Proc. Natl Acad. Sci. USA 115, 607–612.10.1073/pnas.1713530115Search in Google Scholar PubMed PubMed Central

Townley, R.A. and Bülow, H.E. (2018). Deciphering functional glycosaminoglycan motifs in development. Curr. Opin. Struct. Biol. 50, 144–154.10.1016/j.sbi.2018.03.011Search in Google Scholar PubMed PubMed Central

Tsien, R.Y. (2013). Very long-term memories may be stored in the pattern of holes in the perineuronal net. Proc. Natl Acad. Sci. USA 110, 12456–12461.10.1073/pnas.1310158110Search in Google Scholar PubMed PubMed Central

Ughrin, Y.M., Chen, Z.J., and Levine, J.M. (2003). Multiple regions of the NG2 proteoglycan inhibit neurite growth and induce growth cone collapse. J. Neurosci. 23, 175–186.10.1523/JNEUROSCI.23-01-00175.2003Search in Google Scholar

Um, J.W., Kim, K.H., Park, B.S., Choi, Y., Kim, D., Kim, C.Y., Kim, S.J., Kim, M., Ko, J.S., and Lee, S.-G. (2014). Structural basis for LAR-RPTP/Slitrk complex-mediated synaptic adhesion. Nat. Commun. 5, 5423.10.1038/ncomms6423Search in Google Scholar PubMed

Vadivelu, S., Stewart, T.J., Qu, Y., Horn, K., Liu, S., Li, Q., Silver, J., and McDonald, J.W. (2015). NG2+ progenitors derived from embryonic stem cells penetrate glial scar and promote axonal outgrowth into white matter after spinal cord injury: NG2+ ES cells penetrate glial scar. Stem Cells Transl. Med. 4, 401–411.10.5966/sctm.2014-0107Search in Google Scholar PubMed PubMed Central

Valenzuela, J.C., Heise, C., Franken, G., Singh, J., Schweitzer, B., Seidenbecher, C.I., and Frischknecht, R. (2014). Hyaluronan-based extracellular matrix under conditions of homeostatic plasticity. Philos. Trans. R. Soc. B: Biol. Sci. 369, 20130606.10.1098/rstb.2013.0606Search in Google Scholar PubMed PubMed Central

van’t Spijker, H.M. and Kwok, J.C.F. (2017). A sweet talk: the molecular systems of perineuronal nets in controlling neuronal communication. Front. Integr. Neurosci. 11, 33.10.3389/fnint.2017.00033Search in Google Scholar PubMed PubMed Central

Viganò, F. and Dimou, L. (2016). The heterogeneous nature of NG2-glia. Brain Res. 1638, 129–137.10.1016/j.brainres.2015.09.012Search in Google Scholar PubMed

Wang, X., Chun, S.-J., Treloar, H., Vartanian, T., Greer, C.A., and Strittmatter, S.M. (2002). Localization of nogo-A and nogo-66 receptor proteins at sites of axon-myelin and synaptic contact. J. Neurosci. 22, 5505–5515.10.1523/JNEUROSCI.22-13-05505.2002Search in Google Scholar

Wen, T.H., Afroz, S., Reinhard, S.M., Palacios, A.R., Tapia, K., Binder, D.K., Razak, K.A., and Ethell, I.M. (2018a). Genetic reduction of matrix metalloproteinase-9 promotes formation of perineuronal nets around parvalbumin-expressing interneurons and normalizes auditory cortex responses in developing Fmr1 knock-out mice. Cerebral Cortex 28, 3951–3964.10.1093/cercor/bhx258Search in Google Scholar PubMed PubMed Central

Wen, T.H., Binder, D.K., Ethell, I.M., and Razak, K.A. (2018b). The perineuronal ‘safety’ net? Perineuronal net abnormalities in neurological disorders. Front. Mol. Neurosci. 11, 270.10.3389/fnmol.2018.00270Search in Google Scholar PubMed PubMed Central

Wills, Z.P., Mandel-Brehm, C., Mardinly, A.R., McCord, A.E., Giger, R.J., and Greenberg, M.E. (2012). The nogo receptor family restricts synapse number in the developing hippocampus. Neuron 73, 466–481.10.1016/j.neuron.2011.11.029Search in Google Scholar PubMed PubMed Central

Won, S.Y., Kim, C.Y., Kim, D., Ko, J., Um, J.W., Lee, S.B., Buck, M., Kim, E., Heo, W.D., Lee, J.-O., et al. (2017). LAR-RPTP clustering is modulated by competitive binding between synaptic adhesion partners and heparan sulfate. Front. Mol. Neurosci. 10, 327.10.3389/fnmol.2017.00327Search in Google Scholar PubMed PubMed Central

Woo, J., Kwon, S.-K., Choi, S., Kim, S., Lee, J.-R., Dunah, A.W., Sheng, M., and Kim, E. (2009). Trans-synaptic adhesion between NGL-3 and LAR regulates the formation of excitatory synapses. Nat. Neurosci. 12, 428–437.10.1038/nn.2279Search in Google Scholar PubMed

Xu, B., Park, D., Ohtake, Y., Li, H., Hayat, U., Liu, J., Selzer, M.E., Longo, F.M., and Li, S. (2015). Role of CSPG receptor LAR phosphatase in restricting axon regeneration after CNS injury. Neurobiol. Dis. 73, 36–48.10.1016/j.nbd.2014.08.030Search in Google Scholar PubMed PubMed Central

Yamada, J., Ohgomori, T., and Jinno, S. (2015). Perineuronal nets affect parvalbumin expression in GABAergic neurons of the mouse hippocampus. Eur. J. Neurosci. 41, 368–378.10.1111/ejn.12792Search in Google Scholar PubMed

Yamada, J., Nadanaka, S., Kitagawa, H., Takeuchi, K., and Jinno, S. (2018). Increased synthesis of chondroitin sulfate proteoglycan promotes adult hippocampal neurogenesis in response to enriched environment. J. Neurosci. 38, 8496–8513.10.1523/JNEUROSCI.0632-18.2018Search in Google Scholar PubMed PubMed Central

Yang, W.-Z., Liu, T.-T., Cao, J.-W., Chen, X.-F., Liu, X., Wang, M., Su, X., Zhang, S.-Q., Qiu, B.-L., Hu, W.-X., et al. (2016). Fear erasure facilitated by immature inhibitory neuron transplantation. Neuron 92, 1352–1367.10.1016/j.neuron.2016.11.018Search in Google Scholar PubMed

Yang, S., Hilton, S., Alves, J.N., Saksida, L.M., Bussey, T., Matthews, R.T., Kitagawa, H., Spillantini, M.G., Kwok, J.C.F., and Fawcett, J.W. (2017). Antibody recognizing 4-sulfated chondroitin sulfate proteoglycans restores memory in tauopathy-induced neurodegeneration. Neurobiol. Aging 59, 197–209.10.1016/j.neurobiolaging.2017.08.002Search in Google Scholar PubMed

Yiu, G. and He, Z. (2006). Glial inhibition of CNS axon regeneration. Nat. Rev. Neurosci. 7, 617–627.10.1038/nrn1956Search in Google Scholar PubMed PubMed Central

Yutsudo, N. and Kitagawa, H. (2015). Involvement of chondroitin 6-sulfation in temporal lobe epilepsy. Exp. Neurol. 274, 126–133.10.1016/j.expneurol.2015.07.009Search in Google Scholar PubMed

Zhao, Y., Sivaji, S., Chiang, M.C., Ali, H., Zukowski, M., Ali, S., Kennedy, B., Sklyar, A., Cheng, A., Guo, Z., et al. (2017). Amyloid-beta peptides block new synapse assembly by nogo receptor-mediated inhibition of T-type calcium channels. Neuron 96, 355–372.e6.10.1016/j.neuron.2017.09.041Search in Google Scholar PubMed PubMed Central

Zhou, X.-H., Brakebusch, C., Matthies, H., Oohashi, T., Hirsch, E., Moser, M., Krug, M., Seidenbecher, C.I., Boeckers, T.M., Rauch, U., et al. (2001). Neurocan is dispensable for brain development. Mol. Cell. Biol. 21, 5970–5978.10.1128/MCB.21.17.5970-5978.2001Search in Google Scholar PubMed PubMed Central

Zhou, B., Yu, P., Lin, M.-Y., Sun, T., Chen, Y., and Sheng, Z.-H. (2016). Facilitation of axon regeneration by enhancing mitochondrial transport and rescuing energy deficits. J. Cell Biol. 214, 103–119.10.1083/jcb.201605101Search in Google Scholar PubMed PubMed Central

Zukor, K., Belin, S., Wang, C., Keelan, N., Wang, X., and He, Z. (2013). Short hairpin RNA against PTEN enhances regenerative growth of corticospinal tract axons after spinal cord injury. J. Neurosci. 33, 15350–15361.10.1523/JNEUROSCI.2510-13.2013Search in Google Scholar PubMed PubMed Central

Zuo, J., Ferguson, T.A., Hernandez, Y.J., Stetler-Stevenson, W.G., and Muir, D. (1998). Neuronal matrix metalloproteinase-2 degrades and inactivates a neurite-inhibiting chondroitin sulfate proteoglycan. J. Neurosci. 18, 5203–5211.10.1523/JNEUROSCI.18-14-05203.1998Search in Google Scholar

Received: 2019-12-11
Accepted: 2020-01-02
Published Online: 2020-03-03
Published in Print: 2020-07-28

©2020 Walter de Gruyter GmbH, Berlin/Boston

Downloaded on 31.10.2025 from https://www.degruyterbrill.com/document/doi/10.1515/revneuro-2019-0117/html
Scroll to top button