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Gabapentin Receptor α2δ-1 Is a Neuronal Thrombospondin Receptor Responsible for Excitatory CNS Synaptogenesis

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Eroglu, Çagla, Allen, Nicola J., Susman, Michael W., O'Rourke, Nancy A., Park, Chan Young, Özkan, Engin, Chakraborty, Chandrani, Mulinyawe, Sara B., Annis, Douglas S., Huberman, Andrew D., Green, Eric M., Lawler, Jack, Dolmetsch, Ricardo, Garcia, K. Christopher, Smith, Stephen J., Luo, Z. David, Rosenthal, Arnon, Mosher, Deane F., Barres, Ben A.·2009·Cell

DOI 10.1016/j.cell.2009.09.025PMC PMC2791798

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Abstract

Synapses are asymmetric cellular adhesions that are critical for nervous system development and function, but the mechanisms that induce their formation are not well understood. We have previously identified thrombospondin as an astrocyte-secreted protein that promotes central nervous system (CNS) synaptogenesis. Here, we identify the neuronal thrombospondin receptor involved in CNS synapse formation as alpha2delta-1, the receptor for the anti-epileptic and analgesic drug gabapentin. We show that the VWF-A domain of alpha2delta-1 interacts with the epidermal growth factor-like repeats common to all thrombospondins. alpha2delta-1 overexpression increases synaptogenesis in vitro and in vivo and is required postsynaptically for thrombospondin- and astrocyte-induced synapse formation in vitro. Gabapentin antagonizes thrombospondin binding to alpha2delta-1 and powerfully inhibits excitatory synapse formation in vitro and in vivo. These findings identify alpha2delta-1 as a receptor involved in excitatory synapse formation and suggest that gabapentin may function therapeutically by blocking new synapse formation.

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Self-citation

Authors: Eroglu, Ç., Allen, N. J., Susman, M. W., O'Rourke, N. A., Park, C. Y., Özkan, E., Chakraborty, C., Mulinyawe, S. B., Annis, D. S., Huberman, A. D., Green, E. M., Lawler, J., Dolmetsch, R., Garcia, K. C., Smith, S. J., Luo, Z. D., Rosenthal, A., Mosher, D. F., & Barres, B. A.
Affiliations: Stanford Medicine (US)
Howard Hughes Medical Institute (US)
University of Wisconsin–Madison (US)
Beth Israel Deaconess Medical Center (US)
University of California, Irvine Medical Center (US)
ORCID: Allen, Nicola J.
Susman, Michael W.
Park, Chan Young
Özkan, Engin
Annis, Douglas S.
Huberman, Andrew D.
Green, Eric M.
Lawler, Jack
Dolmetsch, Ricardo
Smith, Stephen J.
Luo, Z. David
Rosenthal, Arnon
Mosher, Deane F.
Barres, Ben A.
Venue: Cell
Publisher: Elsevier BV
Published: 2009-10
Volume: 139
Issue: 2
Pages: 380-392
ISSN: 0092-8674 (ISSN-L)
DOI: 10.1016/j.cell.2009.09.025
PMC: PMC2791798
OpenAlex: W1988452935
Cited by: 893
References: 49
Citations by year: 2026: 30 · 2025: 47 · 2024: 62 · 2023: 57 · 2022: 52 · 2021: 59 · 2020: 68 · 2019: 41 · 2018: 54 · 2017: 53 · 2016: 50 · 2015: 41 · 2014: 54 · 2013: 66 · 2012: 56
FWCI: 21.76
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 1421 d)
doi.org/10.15223/policy-017 (stm-asf)
doi.org/10.15223/policy-037 (stm-asf)
doi.org/10.15223/policy-012 (stm-asf)
doi.org/10.15223/policy-029 (stm-asf)
doi.org/10.15223/policy-004 (stm-asf)
Locations: Cell (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Scholarworks@UNIST (Ulsan National Institute of Science and Technology) (submittedVersion)
Funders: National Heart, Lung, and Blood Institute (R01HL049081, HL49081)
National Institute on Drug Abuse (R01DA015043, R37DA015043, DA15043)
National Institute of Neurological Disorders and Stroke (NS-40135, R01NS040135)
National Institute of Dental and Craniofacial Research (R21DE014545, DE14545)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
Keywords: thrombospondin, synaptogenesis, excitatory synapses, astrocytes, epidermal growth factor-like repeats, synaptic adhesion, postsynaptic receptors, gabapentin, central nervous system development, synaptic plasticity
MeSH terms: Gabapentin, Amines, Animals, Cyclohexanecarboxylic Acids, gamma-Aminobutyric Acid, Neuronal Plasticity, Neurons, Synapses, Calcium Channels, Rats, Sprague-Dawley, CD36 Antigens, Calcium Channels, L-Type, Mice, Rats, Neurogenesis

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Gabapentin Receptor α2δ-1 Is a Neuronal Thrombospondin Receptor Responsible for Excitatory CNS Synaptogenesis

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