The DOI matches its Crossref record; 59 of the 59 references it cites were found in a registry or an index.
Activity‐dependent formation and functions of chondroitin sulfate‐rich extracellular matrix of perineuronal nets
Abstract
Extracellular matrix molecules—including chondroitin sulfate proteoglycans, hyaluronan, and tenascin‐R—are enriched in perineuronal nets (PNs) associated with subsets of neurons in the brain and spinal cord. In the present study, we show that similar cell type‐dependent extracellular matrix aggregates are formed in dissociated cell cultures prepared from early postnatal mouse hippocampus. Starting from the 5th day in culture, accumulations of lattice‐like extracellular structures labeled with Wisteria floribunda agglutinin were detected at the cell surface of parvalbumin‐expressing interneurons, which developed after 2–3 weeks into conspicuous PNs localized around synaptic contacts at somata and proximal dendrites, as well as around axon initial segments. Physiological recording and intracellular labeling of PN‐expressing neurons revealed that these are large fast‐spiking interneurons with morphological characteristics of basket cells. To study mechanisms of activity‐dependent formation of PNs, we performed pharmacological analysis and found that blockade of action potentials, transmitter release, Ca 2+ permeable AMPA subtype of glutamate receptors or L‐type Ca 2+ voltage‐gated channels strongly decreased the extracellular accumulation of PN components in cultured neurons. Thus, we suggest that Ca 2+ influx via AMPA receptors and L‐type channels is necessary for activity‐dependent formation of PNs. To study functions of chondroitin sulfate‐rich PNs, we treated cultures with chondroitinase ABC that resulted in a prominent reduction of several major PN components. Removal of PNs did not affect the number and distribution of perisomatic GABAergic contacts but increased the excitability of interneurons in cultures, implicating the extracellular matrix of PNs in regulation of interneuronal activity. © 2007 Wiley Periodicals, Inc. Develop Neurobiol, 2007
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In the citing paper
“PNNs are found primarily around fast--spiking, parvalbumin (PV)--containing GABAergic interneurons in many brain regions (Hartig et al., 1992;Schuppel et al., 2002;Dityatev et al., 2007), but not all regions (e.g., cerebellum; see below).”
From Casting a Wide Net: Role of Perineuronal Nets in Neural Plasticity (2016) · cites this paper as Dityatev et al., 2007
In the citing paper
“PNNs are formed during development (Brückner et al., 2000) in an activity-dependent manner (Dityatev et al., 2007).”
From Perineuronal Nets Regulate the Inhibitory Perisomatic Input onto Parvalbumin Interneurons and γ Activity in the Prefrontal Cortex (2020) · cites this paper as Dityatev et al., 2007
In the citing paper
“Abnormal glutamatergic transmission, polymorphisms of genes encoding for some of their components and altered CSPG expression in glial cells may, independently or in conjunction, cause defective PNN maturation.3, 5, 6, 7, 59”
From Aggrecan and chondroitin-6-sulfate abnormalities in schizophrenia and bipolar disorder: a postmortem study on the amygdala (2015) · cites this paper as [59]
In the citing paper
“Their maturation occurs in an experience-dependent manner, requiring (i) neuronal activation through glutamatergic excitation,78 (ii) availability of key PNN components, such as specific CSPGs, link proteins and tenascin R, (iii) expression on neurons of ECM surface receptors79, 80 and (iv) transcription factors inducing neuronal maturation.25, 38”
From Aggrecan and chondroitin-6-sulfate abnormalities in schizophrenia and bipolar disorder: a postmortem study on the amygdala (2015) · cites this paper as [78]
In the citing paper
“Overall, these functions underlie the role of the adult ECM to neuronal excitability, receptor desensitization, long-term potentiation and long-term depression.59, 87, 88, 90, 91, 92, 93”
From Aggrecan and chondroitin-6-sulfate abnormalities in schizophrenia and bipolar disorder: a postmortem study on the amygdala (2015) · cites this paper as [59]
In the citing paper
“PNNs surround inhibitory fast spiking parvalbumin-positive GABAergic interneurons12–14, but are also associated with further subpopulations, for example excitatory pyramidal neurons in the cerebral cortex15,16.”
From Elimination of the four extracellular matrix molecules tenascin-C, tenascin-R, brevican and neurocan alters the ratio of excitatory and inhibitory synapses (2019) · cites this paper as [14]
In the citing paper
“These data are in agreement with the report of Dityatev and colleagues who found a higher excitability of hippocampal neurons in culture after ChABC treatment14.”
From Elimination of the four extracellular matrix molecules tenascin-C, tenascin-R, brevican and neurocan alters the ratio of excitatory and inhibitory synapses (2019) · cites this paper as [14]
In the citing paper
“Several reports suggest that CSPGs like aggrecan or brevican are incorporated into perineuronal nets through their interaction with TnR and hyaluronic acid14,53,54.”
From Elimination of the four extracellular matrix molecules tenascin-C, tenascin-R, brevican and neurocan alters the ratio of excitatory and inhibitory synapses (2019) · cites this paper as [14]
In the citing paper
“Levels of PV (Kinney et al, 2006) and PNN labeling (Dityatev et al, 2007;Giamanco and Matthews, 2012) are regulated in an activity-dependent manner.”
From Reduced Labeling of Parvalbumin Neurons and Perineuronal Nets in the Dorsolateral Prefrontal Cortex of Subjects with Schizophrenia (2016) · cites this paper as Dityatev et al, 2007
In the citing paper
“PNNs regulate survival (Morawski et al. 2004(Morawski et al. , 2015;;Cabungcal et al. 2013) and excitability of PV interneurons (Dityatev et al. 2007;Carulli et al. 2010;Balmer 2016), and stabilization of sensory circuits (Pizzorusso et al. 2002;McRae et al. 2007).”
From 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 (2018) · cites this paper as Dityatev et al. 2007
In the citing paper
“Consistently, PNN enzymatic digestion results in increased excitability of interneurons (Dityatev et al., 2007).”
From Losing the sugar coating: Potential impact of perineuronal net abnormalities on interneurons in schizophrenia (2015) · cites this paper as Dityatev et al., 2007
In the citing paper
“PNN gradual maturation around somata and dendrites stabilizes successful synapses, restricting plasticity, regulating synaptogenesis and maintaining mature forms of learning (Bukalo et al., 2001; Carulli et al., 2013b; Dityatev et al., 2007; Faissner et al., 2010; Gundelfinger et al., 2010; McRae and Porter, 2012; Pyka et al., 2011).”
From Losing the sugar coating: Potential impact of perineuronal net abnormalities on interneurons in schizophrenia (2015) · cites this paper as Dityatev et al., 2007
In the citing paper
“blockage of glutamate receptors and presynaptic N- and P/Q-type calcium channels (both implicated in glutamate release) did not affect PNN growth, indicating that neuronal activity is required but that glutamatergic neurotransmission is not essential for PNN development (Dityatev et al., 2007)”
From Perineuronal nets and schizophrenia: The importance of neuronal coatings (2014) · cites this paper as Dityatev et al., 2007
In the citing paper
“blockage of sodium channels inhibits the formation of PNNs (Dityatev et al., 2007)”
From Perineuronal nets and schizophrenia: The importance of neuronal coatings (2014) · cites this paper as Dityatev et al., 2007
In the citing paper
“Formation of PNNs has been found to be activity-dependent.”
From Perineuronal nets and schizophrenia: The importance of neuronal coatings (2014) · cites this paper as Dityatev et al., 2007
In the citing paper
“Accumulating evidence suggests that PNN formation is driven by neuronal activity (Dityatev et al., 2007)”
From Adult neurogenesis, glia, and the extracellular matrix (2019) · cites this paper as Dityatev et al., 2007
Citations
Cites
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Hyaluronan: from extracellular glue to pericellular cue
Toole, B. P. (2004) · Nature Reviews Cancer · doi:10.1038/nrc1391 · Cited by 2,125
Reactivation of Ocular Dominance Plasticity in the Adult Visual Cortex
Pizzorusso, T., Medini, P., Berardi, N., Chierzi, S., Fawcett, J. W., & Maffei, L. (2002) · Science · doi:10.1126/science.1072699 · Cited by 1,679
Defined types of cortical interneurone structure space and spike timing in the hippocampus
Somogyi, P., & Klausberger, T. (2005) · The Journal of Physiology · doi:10.1113/jphysiol.2004.078915 · Cited by 927
Kv3 channels: voltage-gated K+ channels designed for high-frequency repetitive firing
Rudy, B., & McBain, C. J. (2001) · Trends in Neurosciences · doi:10.1016/s0166-2236(00)01892-0 · Cited by 781
Jones, F. S., & Jones, P. L. (2000) · Developmental Dynamics · doi:10.1002/(sici)1097-0177(200006)218:2 · Cited by 699
Lecticans: organizers of the brain extracellular matrix
Yamaguchi, Y. (2000) · Cellular and Molecular Life Sciences · doi:10.1007/pl00000690 · Cited by 642
Interneuron Diversity series: Rhythm and mood in perisomatic inhibition
Freund, T. F. (2003) · Trends in Neurosciences · doi:10.1016/s0166-2236(03)00227-3 · Cited by 641
Extracellular matrix molecules and synaptic plasticity
Dityatev, A., & Schachner, M. (2003) · Nature Reviews Neuroscience · doi:10.1038/nrn1115 · Cited by 564
Self-citationNovel hyaluronidase from streptomyces
Takaichi, O. H. Y. A., & Kaneko, Y. (1970) · Biochimica et Biophysica Acta (BBA) - Enzymology · doi:10.1016/0005-2744(70)90139-7 · Cited by 518
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The dual role of the extracellular matrix in synaptic plasticity and homeostasis
Dityatev, A., Schachner, M., & Sonderegger, P. (2010) · Nature Reviews Neuroscience · doi:10.1038/nrn2898 · Cited by 559
Self-citationBrain extracellular matrix affects AMPA receptor lateral mobility and short-term synaptic plasticity
Frischknecht, R., Heine, M., Perrais, D., Seidenbecher, C. I., Choquet, D., & Gundelfinger, E. D. (2009) · Nature Neuroscience · doi:10.1038/nn.2338 · Cited by 554
Metadata
- Authors
- Dityatev, A., Brückner, G., Dityateva, G., Grosche, J., Kleene, R., & Schachner, M.
- Affiliations
- Leipzig University (DE)
- University Medical Center Hamburg-Eppendorf (DE)
- Corresponding author
- Schachner, Melitta
- Venue
- Developmental Neurobiology
- Publisher
- Wiley
- Published
- 2007-02-09
- Volume
- 67
- Issue
- 5
- Pages
- 570-588
- ISSN
- 1932-8451 (ISSN-L)
- 1932-846X
- OpenAlex
- W2106489369
- Cited by
- 365
- References
- 59
- Citations by year
- 2026: 13 · 2025: 27 · 2024: 21 · 2023: 20 · 2022: 24 · 2021: 24 · 2020: 25 · 2019: 29 · 2018: 27 · 2017: 24 · 2016: 19 · 2015: 19 · 2014: 18 · 2013: 13 · 2012: 13
- FWCI
- 4.89
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Developmental Neurobiology (publishedVersion)
- PubMed (publishedVersion)
- Rutgers University Community Repository (Rutgers University) (submittedVersion)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Proteoglycans and glycosaminoglycans research
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- perineuronal nets, chondroitin sulfate proteoglycans, extracellular matrix, parvalbumin interneurons, basket cells, fast-spiking interneurons, AMPA receptors, L-type calcium channels, chondroitinase ABC, GABAergic synapses, interneuron excitability, hippocampus, postnatal development
- MeSH terms
- Animals, Cell Count, Cells, Cultured, Chondroitin Sulfates, Electrophysiology, Extracellular Matrix, Hippocampus, Immunohistochemistry, Interneurons, Mice, Inbred C57BL, Proteoglycans, Synapses, Blotting, Western, Receptors, GABA, Chondroitin ABC Lyase, Satellite Cells, Perineuronal, Mice
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