Expression of neural proteoglycans correlates with the acquisition of mature neuronal properties in the mammalian brain
Abstract
The neurons in the mature mammalian central nervous system (CNS) are an enormously diverse group of cells. The acquisition of mature, differentiated neuronal properties takes place over an extended developmental period, through a number of different mechanisms. Some of the very last events in neuronal development occur late in the postnatal period, when the mature set of synapses between neurons and their targets is selected and the adult anatomical and physiological properties of neurons are acquired. Experiments in many different systems have shown that the mature set of synapses is selected from an initial set by selective stabilization of some synapses and elimination of others (for review, see Purves and Lichtman 1985). The process of synapse selection is governed, at least in part, by neuronal activity. Temporal matching of pre-and postsynaptic activity is thought to be critical in determining whether a synapse will be retained or lost. Environmental stimuli (such...
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Animal studies show PNNs are widely distributed in the brain.
“A large number of animal studies have shown that PNNs are widely distributed in the brain”
From Perineuronal nets and schizophrenia: The importance of neuronal coatings (2014) · cites this paper as Hockfield et al., 1990
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Animals lacking link protein have attenuated perineuronal nets and persistent plasticity
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“…CSPGs that were previously diffusely distributed are incorporated into specialized structures of condensed and stable matrix around the somata and dendrites of neurons, known as perineuronal nets (PNNs) (Hockfield et al.,1990; Schweizer et al., 1993; Pizzorusso et al., 2002; Galtrey et al., 2008).”
BackgroundExtracellular matrix of the central nervous system: from neglect to challenge
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“In addition, the establishment of perineuronal nets seems to stabilize the neuronal circuitry by suppressing the formation of new synaptic contacts (Galtrey and Fawcett 2007; HockWeld et al. 1990; Rauch 2004; Yamaguchi 2000).”
BackgroundExtracellular matrix and perineuronal nets in CNS repair
Kwok, J. C. F., Dick, G., Wang, D., & Fawcett, J. W. (2011) · Developmental Neurobiology · doi:10.1002/dneu.20974 · Cited by 395 · see citing works
“Dark rearing in newborn cats prolongs the critical period in the visual cortex with a concomitant decrease in aggrecan immunostaining (Hockfield et al., 1990; Lander et al., 1997; Pizzurusso et al., 2002), but in developing chicks light deprivation did not prevent PNN formation (Gati et al.”
BackgroundInfluentialThe perineuronal net and the control of CNS plasticity
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Perineuronal nets — a specialized form of extracellular matrix in the adult nervous system
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“, 2002), it is likely that aggrecan is the proteoglycan that contributes most to the structure of PNs (Hockfield et al., 1990; Lander et al., 1997; Matthews et al., 2002).”
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“CSPG up-regulation within the PNN is extremely important because it serves to limit potential functional plasticity, which could occur via compensatory sprouting from surviving inputs (Hockfield et al. 1990; Yamada et al. 1997; Berardi et al. 2004; Massey et al. 2006; Pizzorusso et al. 2006; Gogolla et al. 2009; Garcı…”
BackgroundReducing Intracortical Inhibition in the Adult Visual Cortex Promotes Ocular Dominance Plasticity
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“CP closure in OD plasticity has been attributed to developmental changes in several cellular and molecular factors (Hockfield et al., 1990; Schoop et al., 1997; Hensch et al., 1998; Huang et al., 1999; Pizzorusso et al., 2002, 2006; Berardi et al., 2003; Hensch, 2005; McGee et al., 2005) and in…”
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“This coincides with the assembly of stable extracellular matrix structures, the perineuronal nets (PNNs), which are formed mainly around the PV neurons (Hockfield et al., 1990; Pizzorusso et al., 2002; Balmer et al., 2009; Carulli et al., 2010).”
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“…inhibition (Saghatelyan et al., 2001), reopening of the critical period (Pizzorusso et al., 2002, 2006), and that dark rearing, which delays the close of the critical period, inhibits expression of aggrecan-positive PNs identified with Cat-301 (Guimaraes et al., 1990; Hockfield et al., 1990).”
BackgroundPerineuronal nets potentially protect against oxidative stress
Morawski, M., Brückner, M. K., Riederer, P., Brückner, G., & Arendt, T. (2004) · Experimental Neurology · doi:10.1016/j.expneurol.2004.04.017 · Cited by 246 · see citing works
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“The samples were thawed, and then centrifuged, the supernatant was discarded, and the pellet was dried and then dissolved in SDS-PAGE gel loading buffer and analyzed by Western blotting.”
BackgroundInfluentialSelf-citationBrain derived versican V2 is a potent inhibitor of axonal growth
Schmalfeldt, M., Bandtlow, C. E., Dours-Zimmermann, M. T., Winterhalter, K. H., & Zimmermann, D. R. (2000) · Journal of Cell Science · doi:10.1242/jcs.113.5.807 · Cited by 197 · see citing works
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“PNNs are believed to be important in stabilising synapses (Hockfield et al., 1990), controlling synaptic plasticity (Corvetti and Rossi, 2005) and neuroprotection (Br¨uckner et al., 1999; Hartig et al., 2001 and Morawski et al., 2004).”
Suttkus, A., Rohn, S., Weigel, S., Glöckner, P., Arendt, T., & Morawski, M. (2014) · Cell Death & Disease · doi:10.1038/cddis.2014.25 · Cited by 168 · see citing works
“plasticity.(9,17,18) In addition, the glycoprotein components of the PNs carry numerous glycosaminoglycan (GAG) side”
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“During postnatal development, these components accumulate in characteristic patterns, which persist throughout life (Hockfield et al. 1990; Fujita and Kudo 1992; Bignami et al. 1993; Schweizer et al. 1993; Köppe et al. 1997a; Lurie et al. 1997).”
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“Dark rearing, which prolongs critical pe- The released tPA increases extracellular proteolysis directly or by the activation of plasmin from the zymogenriod closure, also prolongs CSPG condensation (Hockfield et al., 1990).”
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“Experience-dependent expression of aggrecan provides correlative evidence to support the hypothesis that aggrecan is the key CSPGs that regulates the termination of the critical period (Sur et al., 1988; Hockfield et al., 1990).”
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“Once the mature sets of synapses are ensheathed by a PN, they are stabilized and subject to little reorganization in the adult (Sur et al., 1988; Kalb and Hockfield, 1990a; Hockfield et al., 1990; Pizzorusso et al., 2002; McRae et al., 2007).”
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“In the neocortex, the PV cells mature in parallel with the assembly of the PNNs late in postnatal development as the critical period comes to an end (Hockfield et al., 1990; Pizzorusso et al., 2002; Ye and Miao, 2013).”
BackgroundHow does chondroitinase promote functional recovery in the damaged CNS?
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BackgroundAggrecan: Beyond cartilage and into the brain
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Köppe, G., Brückner, G., Brauer, K., Härtig, W., & Bigl, V. (1997) · Cell and Tissue Research · doi:10.1007/s004410050790 · Cited by 129 · see citing works
“Since the main periods of synaptogenesis as described for some cortical areas (Aghajanian and Bloom 1967; Blue and Parnavelas 1983) roughly correspond with the time course of perineuronal accumulation of CSPGs, a role in the termination of synaptic plasticity related to synaptic stabilization, was suggested (Sur et al…”
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Advancing models of neural development with biomaterials
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Self-citationSigal, Y. M., Bae, H., Bogart, L. J., Hensch, T. K., & Zhuang, X. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1817222116 · Cited by 118 · see citing works
“The condensed PNN is thought to act as a molecular brake on synaptic plasticity as critical periods close (10, 11), and cleavage of PNN components can partially reopen plasticity in adulthood (12, 13).”
BackgroundAxon initial segment ensheathed by extracellular matrix in perineuronal nets
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Versican V2 Is a Major Extracellular Matrix Component of the Mature Bovine Brain
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Plasticity in the adult brain: lessons from the visual system
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“sation of extracellular matrix molecules into perineuronal nets (HockWeld et al. 1990; Pizzorusso et al. 2002) and the maturation of intracortical inhibition (Hensch et al.”
BackgroundEarly postmitotic neurons transiently express TOAD‐64, a neural specific protein
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Self-citationLoss of perineuronal net N-acetylgalactosamine in Alzheimer’s disease
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“The PN is also involved in the development, stabilisation and remodelling of synapses [8, 17, 28, 55].”
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“PNNs inhibit the outgrowth of neurites (Hockfield et al., 1990; Pizzorusso et al., 2002; Mcrae et al., 2007), which may lead to restricted synaptic plasticity and defective neurotransmission over the course of AD, aggravating the disease’s pathological damage.”
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Extracellular matrix organization in various regions of rat brain grey matter
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Protective Properties of Neural Extracellular Matrix
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Self-citationNeurons Produce a Neuronal Cell Surface-Associated Chondroitin Sulfate Proteoglycan
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“Although the molecular composition of the perineuronal nets is not yet known in great detail, it is clear from a number of studies that the constituents of these nets are highly heterogeneous and that different neuronal subsets can be distinguished by the complement of chondroitin sulfate proteoglycans (CSPGs) that th…”
BackgroundSelf-citationWegner, F., Härtig, W., Bringmann, A., Grosche, J., Wohlfarth, K., Zuschratter, W., & Brückner, G. (2003) · Experimental Neurology · doi:10.1016/s0014-4886(03)00313-3 · Cited by 107 · see citing works
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Perineuronal nets protect against amyloid β-protein neurotoxicity in cultured cortical neurons
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On the existence of a cartilage‐like proteoglycan and link proteins in the central nervous system
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“Changes in CSPG expression and composition occur at the end of periods of developmental plasticity (Galtrey et al., 2008; Hockfield et al., 1990; Matthews et al., 2002), implicating these molecules in an essential role in regulating activity dependent changes in synaptic function.”
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“HILE the presence of an extracellular matrix in nonneural tissues has been universally accepted, only recently has evidence been adduced for an organized extracellular matrix in the mammalian central nervous system (CNS) ~ (Reichardt and Tomaselli, 1991; Hocktield et al., 1990; Sanes, 1989).”
Self-citationPerineuronal nets and schizophrenia: The importance of neuronal coatings
Bitanihirwe, B. K. Y., & Woo, T.-U. W. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.03.018 · Cited by 95 · see citing works
Darkness Alters Maturation of Visual Cortex and Promotes Fast Recovery from Monocular Deprivation
Duffy, K. R., & Mitchell, D. E. (2013) · Current Biology · doi:10.1016/j.cub.2013.01.017 · Cited by 95 · see citing works
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“Chondroitin sulphate proteoglycans (CSPGs) are the major known extracellular constituents of perineuronal nets (Delpech et al., 1982, 1989; Hockfield et al., 1990; Bertolotto et al., 1991; Bignami et al., 1992a, 1993a; Fryer et al., 1992; Fujita & Kudo, 1992; Girard et al., 1992; Brückner et al.,…”
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“Although others have suggested that some PGs are localized to neurons that form functional or anatomical systems (Hockfield et al., 1990; Maeda et al., 1992), the types of neurons that express glypican mRNA do not correspond to any single functional or transmitter-specific subdivision of the brain.”
BackgroundDistribution of pyramidal cells associated with perineuronal nets in the neocortex of rat
Alpár, A., Gärtner, U., Härtig, W., & Brückner, G. (2006) · Brain Research · doi:10.1016/j.brainres.2006.08.069 · Cited by 93 · see citing works
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“(CSPGs) are inhibitory extracellular matrix molecules that play a role in synaptic stabilization and in limiting neuronal plasticity (Hockfield et al., 1990; Yamaguchi, 2000; Corvetti & Rossi, 2005).”
BackgroundPersistent decrease in multiple components of the perineuronal net following status epilepticus
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“…matrix (ECM) structure that forms a lattice-like configuration around the synapses on the somata and proximal dendrites of a subset of interneurons (Hockfield et al., 1990; Brückner et al., 1993), and is therefore uniquely positioned to influence synaptic integrity and stability (Frischknecht et…”
BackgroundExtracellular Matrix and Visual Cortical PlasticityFreeing the Synapse
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“…various sets of neurons that are either components of local circuits (cortical interneurons) or projection neurons of the brainstem and spinal cord (Hockfield and McKay 1983; Zaremba et al 1989; Fujita et al. 1989; Bertolotto et al. 1990, 1991; Hockfield et al. 1990a; Fujita and Kudo 1992).”
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The Role of Extracellular Matrix in Human Neurodegenerative Diseases
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- Authors
- Hockfield, S., Kalb, R. G., Zaremba, S., & Fryer, H.
- Affiliations
- Yale University (US)
- Venue
- Cold Spring Harbor Symposia on Quantitative Biology
- Publisher
- Cold Spring Harbor Laboratory
- Published
- 1990-01-01
- Volume
- 55
- Issue
- 0
- Pages
- 505-514
- ISSN
- 0091-7451 (ISSN-L)
- 1943-4456
- OpenAlex
- W2325060126
- Cited by
- 271
- References
- 0
- Citations by year
- 2026: 1 · 2025: 2 · 2024: 5 · 2023: 4 · 2022: 7 · 2021: 9 · 2020: 10 · 2019: 4 · 2018: 9 · 2017: 7 · 2016: 5 · 2015: 12 · 2014: 13 · 2013: 12 · 2012: 11
- Type
- posted content
- Language
- en
- Open access
- closed
- Locations
- Cold Spring Harbor Symposia on Quantitative Biology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (5k08ns001247-04, 5f32ey005855-02)
- National Eye Institute (EY05855, EY 06511)
- National Institute of Neurological Disorders and Stroke (NS-01247)
- Topics
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Proteoglycans and glycosaminoglycans research
- Keywords
- neuronal maturation, postnatal brain development, synaptic pruning, synaptic stabilization, central nervous system development
- MeSH terms
- Animals, Antibodies, Monoclonal, Brain, Cats, Cell Differentiation, Extracellular Matrix, Motor Neurons, Neurons, Chondroitin Sulfate Proteoglycans, Proteoglycans, Spinal Cord, Visual Cortex
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