Cited by 764Neuroscience and Neuropharmacology ResearchProteoglycans and glycosaminoglycans researchNeurogenesis and neuroplasticity mechanisms

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Astrocyte glypicans 4 and 6 promote formation of excitatory synapses via GluA1 AMPA receptors

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Allen, Nicola J., Bennett, Mariko L., Foo, Lynette C., Wang, Gordon X., Chakraborty, Chandrani, Smith, Stephen J., Barres, Ben A.·2012·Nature

DOI 10.1038/nature11059PMC PMC3383085

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Abstract

In the developing central nervous system (CNS), the control of synapse number and function is critical to the formation of neural circuits. We previously demonstrated that astrocyte-secreted factors powerfully induce the formation of functional excitatory synapses between CNS neurons. Astrocyte-secreted thrombospondins induce the formation of structural synapses, but these synapses are postsynaptically silent. Here we use biochemical fractionation of astrocyte-conditioned medium to identify glypican 4 (Gpc4) and glypican 6 (Gpc6) as astrocyte-secreted signals sufficient to induce functional synapses between purified retinal ganglion cell neurons, and show that depletion of these molecules from astrocyte-conditioned medium significantly reduces its ability to induce postsynaptic activity. Application of Gpc4 to purified neurons is sufficient to increase the frequency and amplitude of glutamatergic synaptic events. This is achieved by increasing the surface level and clustering, but not overall cellular protein level, of the GluA1 subunit of the AMPA (α-amino-3-hydroxy-5-methyl-4-isoxazole propionic acid) glutamate receptor (AMPAR). Gpc4 and Gpc6 are expressed by astrocytes in vivo in the developing CNS, with Gpc4 expression enriched in the hippocampus and Gpc6 enriched in the cerebellum. Finally, we demonstrate that Gpc4-deficient mice have defective synapse formation, with decreased amplitude of excitatory synaptic currents in the developing hippocampus and reduced recruitment of AMPARs to synapses. These data identify glypicans as a family of novel astrocyte-derived molecules that are necessary and sufficient to promote glutamate receptor clustering and receptivity and to induce the formation of postsynaptically functioning CNS synapses.

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Authors: Allen, N. J., Bennett, M. L., Foo, L. C., Wang, G. X., Chakraborty, C., Smith, S. J., & Barres, B. A.
Affiliations: Stanford Medicine (US)
Corresponding author: Allen, Nicola J.
ORCID: Allen, Nicola J.
Bennett, Mariko L.
Foo, Lynette C.
Wang, Gordon X.
Smith, Stephen J.
Barres, Ben A.
Venue: Nature
Publisher: Springer Science and Business Media LLC
Published: 2012-05-27
Volume: 486
Issue: 7403
Pages: 410-414
ISSN: 0028-0836 (ISSN-L)
1476-4687
DOI: 10.1038/nature11059
PMC: PMC3383085
OpenAlex: W2012935976
Cited by: 764
References: 32
Citations by year: 2026: 49 · 2025: 58 · 2024: 61 · 2023: 72 · 2022: 61 · 2021: 72 · 2020: 64 · 2019: 47 · 2018: 43 · 2017: 56 · 2016: 39 · 2015: 48 · 2014: 46 · 2013: 36 · 2012: 11
FWCI: 18.58
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
Locations: Nature (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
RePEc: Research Papers in Economics (submittedVersion)
Funders: National Institute on Drug Abuse (R01DA015043)
National Institute of Neurological Disorders and Stroke (R01NS0725252, R01NS075252, R01NS077601)
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: GPC4, astrocytes, excitatory synapse formation, retinal ganglion cells, glutamatergic neurotransmission, synaptic plasticity, synaptic dysfunction, astrocyte-neuron interaction, hippocampus
MeSH terms: Animals, Astrocytes, Cerebellum, Female, Hippocampus, Humans, Male, Mice, Inbred C57BL, Retinal Ganglion Cells, Synapses, Culture Media, Conditioned, Rats, Sprague-Dawley, Receptors, AMPA, Excitatory Postsynaptic Potentials, Mice, Rats, Glypicans

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Astrocyte glypicans 4 and 6 promote formation of excitatory synapses via GluA1 AMPA receptors

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