Chondroitin sulfate proteoglycans regulate astrocyte‐dependent synaptogenesis and modulate synaptic activity in primary embryonic hippocampal neurons

Pyka, Martin; Wetzel, Christian; Aguado, Ainhara; Geissler, Maren; Hatt, Hanns; Faissner, Andreas

doi:10.1111/j.1460-9568.2011.07690.x

Cited by 131Neuroscience and Neuropharmacology ResearchProteoglycans and glycosaminoglycans researchNeurogenesis and neuroplasticity mechanisms

Chondroitin sulfate proteoglycans regulate astrocyte‐dependent synaptogenesis and modulate synaptic activity in primary embryonic hippocampal neurons

Pyka, Martin, Wetzel, Christian, Aguado, Ainhara, Geissler, Maren, Hatt, Hanns, Faissner, Andreas·2011·European Journal of Neuroscience

DOI 10.1111/j.1460-9568.2011.07690.x

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Abstract

It has been shown that astrocyte‐derived extracellular matrix (ECM) is important for formation and maintenance of CNS synapses. In order to study the effects of glial‐derived ECM on synaptogenesis, E18 rat hippocampal neurons and primary astrocytes were co‐cultivated using a cell‐insert system. Under these conditions, neurons differentiated under low density conditions (3500 cells/cm 2) in defined, serum‐free medium and in the absence of direct, membrane‐mediated neuron–astrocyte interactions. Astrocytes promoted the formation of structurally intact synapses, as documented by the co‐localisation of bassoon‐ and ProSAP1/Shank2‐positive puncta, markers of the pre‐ and postsynapse, respectively. The development of synapses was paralleled by the emergence of perineuronal net (PNN)‐like structures that contained various ECM components such as hyaluronic acid, brevican and neurocan. In order to assess potential functions for synaptogenesis, the ECM was removed by treatment with hyaluronidase or chondroitinase ABC. Both enzymes significantly enhanced the number of synaptic puncta. Whole‐cell voltage‐clamp recordings of control and enzyme‐treated hippocampal neurons revealed that chondroitinase ABC treatment led to a significant decrease in amplitude and a reduced charge of miniature excitatory postsynaptic currents, whereas inhibitory postsynaptic currents were not affected. When the response to the application of glutamate was measured, a reduced sensitivity could be detected and resulted in decreased currents in response to the excitatory neurotransmitter. These findings are consistent with the interpretation that the ECM partakes in the regulation of the density of glutamate receptors in subsynaptic sites.

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When hippocampal neurons were treated with chondroitinase ABC (ChABC) in vitro, synapse formation was boosted.
“When hippocampal neurons were treated with ChABC in vitro, synapse formation was boosted6.”
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 [6]
It is unclear how these molecules are assembled to form PNN around neurons.
“It is unclear how these molecules are assembled to form PNN around neurons, but some studies suggest that both neurons and glial cells are involved in the process (Miyata et al., 2007; Pyka et al., 2011).”
From The Perineuronal ‘Safety’ Net? Perineuronal Net Abnormalities in Neurological Disorders (2018) · cites this paper as Pyka et al., 2011
Both neurons and glial cells are involved in the assembly of PNN around neurons.
“It is unclear how these molecules are assembled to form PNN around neurons, but some studies suggest that both neurons and glial cells are involved in the process (Miyata et al., 2007; Pyka et al., 2011).”
From The Perineuronal ‘Safety’ Net? Perineuronal Net Abnormalities in Neurological Disorders (2018) · cites this paper as Pyka et al., 2011
Disruption of perineuronal nets can alter the resting membrane potential of parvalbumin neurons and decrease the amplitudes of both inhibitory and excitatory postsynaptic currents.
“Fourth, disruption of PNNs can alter the resting membrane potential of PV neurons (Miyata et al, 2012) and decrease the amplitudes of both inhibitory (Liu et al, 2013) and excitatory (Pyka et al, 2011) postsynaptic currents.”
From Reduced Labeling of Parvalbumin Neurons and Perineuronal Nets in the Dorsolateral Prefrontal Cortex of Subjects with Schizophrenia (2016) · cites this paper as Pyka et al, 2011

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Authors: Pyka, M., Wetzel, C., Aguado, A., Geissler, M., Hatt, H., & Faissner, A.
Affiliations: Ruhr University Bochum (DE)
ORCID: Wetzel, Christian
Venue: European Journal of Neuroscience
Publisher: Wiley
Published: 2011-05-25
Volume: 33
Issue: 12
Pages: 2187-2202
ISSN: 0953-816X (ISSN-L)
1460-9568
DOI: 10.1111/j.1460-9568.2011.07690.x
OpenAlex: W1572938127
Cited by: 131
References: 84
Citations by year: 2026: 1 · 2025: 6 · 2024: 3 · 2023: 10 · 2022: 10 · 2021: 7 · 2020: 16 · 2019: 7 · 2018: 11 · 2017: 12 · 2016: 11 · 2015: 6 · 2014: 13 · 2013: 9 · 2012: 4
FWCI: 4.11
Type: journal article
Language: en
Open access: closed
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations: European Journal of Neuroscience (publishedVersion)
PubMed (publishedVersion)
Funders: Deutsche Forschungsgemeinschaft
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: chondroitin sulfate proteoglycans, synaptogenesis, astrocytes, extracellular matrix, hippocampal neurons, perineuronal nets, chondroitinase ABC, hyaluronidase, miniature excitatory postsynaptic currents, synaptic transmission, brevican, neurocan, hyaluronic acid, shank, bassoon
MeSH terms: Animals, Astrocytes, Embryo, Mammalian, Extracellular Matrix, Fibroblasts, Hippocampus, Hyaluronoglucosaminidase, Synaptic Transmission, Neurons, Chondroitin Sulfate Proteoglycans, Rats, Inbred Strains, Synapses, Patch-Clamp Techniques, Glutamic Acid, Coculture Techniques, Cell Culture Techniques, Chondroitin ABC Lyase, Rats, Miniature Postsynaptic Potentials

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Chondroitin sulfate proteoglycans regulate astrocyte‐dependent synaptogenesis and modulate synaptic activity in primary embryonic hippocampal neurons

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