LTP Induction Boosts Glutamate Spillover by Driving Withdrawal of Perisynaptic Astroglia.


Journal

Neuron
ISSN: 1097-4199
Titre abrégé: Neuron
Pays: United States
ID NLM: 8809320

Informations de publication

Date de publication:
09 12 2020
Historique:
received: 30 10 2019
revised: 14 06 2020
accepted: 28 08 2020
pubmed: 26 9 2020
medline: 28 1 2021
entrez: 25 9 2020
Statut: ppublish

Résumé

Extrasynaptic actions of glutamate are limited by high-affinity transporters expressed by perisynaptic astroglial processes (PAPs): this helps maintain point-to-point transmission in excitatory circuits. Memory formation in the brain is associated with synaptic remodeling, but how this affects PAPs and therefore extrasynaptic glutamate actions is poorly understood. Here, we used advanced imaging methods, in situ and in vivo, to find that a classical synaptic memory mechanism, long-term potentiation (LTP), triggers withdrawal of PAPs from potentiated synapses. Optical glutamate sensors combined with patch-clamp and 3D molecular localization reveal that LTP induction thus prompts spatial retreat of astroglial glutamate transporters, boosting glutamate spillover and NMDA-receptor-mediated inter-synaptic cross-talk. The LTP-triggered PAP withdrawal involves NKCC1 transporters and the actin-controlling protein cofilin but does not depend on major Ca

Identifiants

pubmed: 32976770
pii: S0896-6273(20)30661-9
doi: 10.1016/j.neuron.2020.08.030
pmc: PMC7736499
pii:
doi:

Substances chimiques

Glutamic Acid 3KX376GY7L

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

919-936.e11

Subventions

Organisme : Wellcome Trust
ID : 101896
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 212251
Pays : United Kingdom

Informations de copyright

Copyright © 2020 The Authors. Published by Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of Interests The authors declare no competing interests.

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Auteurs

Christian Henneberger (C)

UCL Queen Square Institute of Neurology, University College London, London WC1N 3BG, UK; Institute of Cellular Neurosciences, Medical Faculty, University of Bonn, 53127 Bonn, Germany; German Center for Neurodegenerative Diseases (DZNE), 53175 Bonn, Germany. Electronic address: christian.henneberger@uni-bonn.de.

Lucie Bard (L)

UCL Queen Square Institute of Neurology, University College London, London WC1N 3BG, UK.

Aude Panatier (A)

INSERM U1215, Neurocentre Magendie, 33000 Bordeaux, France; Université de Bordeaux, 33000 Bordeaux, France; Interdisciplinary Institute for Neuroscience, CNRS UMR 5297, 33000 Bordeaux, France.

James P Reynolds (JP)

UCL Queen Square Institute of Neurology, University College London, London WC1N 3BG, UK.

Olga Kopach (O)

UCL Queen Square Institute of Neurology, University College London, London WC1N 3BG, UK.

Nikolay I Medvedev (NI)

Life Sciences, The Open University, Milton Keynes MK7 6AA, UK.

Daniel Minge (D)

Institute of Cellular Neurosciences, Medical Faculty, University of Bonn, 53127 Bonn, Germany.

Michel K Herde (MK)

Institute of Cellular Neurosciences, Medical Faculty, University of Bonn, 53127 Bonn, Germany.

Stefanie Anders (S)

Institute of Cellular Neurosciences, Medical Faculty, University of Bonn, 53127 Bonn, Germany.

Igor Kraev (I)

Life Sciences, The Open University, Milton Keynes MK7 6AA, UK.

Janosch P Heller (JP)

UCL Queen Square Institute of Neurology, University College London, London WC1N 3BG, UK.

Sylvain Rama (S)

UCL Queen Square Institute of Neurology, University College London, London WC1N 3BG, UK.

Kaiyu Zheng (K)

UCL Queen Square Institute of Neurology, University College London, London WC1N 3BG, UK.

Thomas P Jensen (TP)

UCL Queen Square Institute of Neurology, University College London, London WC1N 3BG, UK.

Inmaculada Sanchez-Romero (I)

Institute of Science and Technology Austria, 3400 Klosterneuburg, Austria.

Colin J Jackson (CJ)

Research School of Chemistry, Australian National University, Acton, ACT 2601, Australia.

Harald Janovjak (H)

Institute of Science and Technology Austria, 3400 Klosterneuburg, Austria; EMBL Australia, Australian Regenerative Medicine Institute, Faculty of Medicine, Nursing and Health Science, Monash University, Melbourne, VIC 3800, Australia.

Ole Petter Ottersen (OP)

Institute of Basic Medical Sciences, University of Oslo, 0317 Oslo, Norway; Karolinska Institutet, 171 77 Stockholm, Sweden.

Erlend Arnulf Nagelhus (EA)

Institute of Basic Medical Sciences, University of Oslo, 0317 Oslo, Norway.

Stephane H R Oliet (SHR)

INSERM U1215, Neurocentre Magendie, 33000 Bordeaux, France; Université de Bordeaux, 33000 Bordeaux, France.

Michael G Stewart (MG)

Life Sciences, The Open University, Milton Keynes MK7 6AA, UK. Electronic address: m.g.stewart@open.ac.uk.

U Valentin Nägerl (UV)

Université de Bordeaux, 33000 Bordeaux, France; Interdisciplinary Institute for Neuroscience, CNRS UMR 5297, 33000 Bordeaux, France. Electronic address: valentin.nagerl@u-bordeaux.fr.

Dmitri A Rusakov (DA)

UCL Queen Square Institute of Neurology, University College London, London WC1N 3BG, UK. Electronic address: d.rusakov@ucl.ac.uk.

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