Glial glucose fuels the neuronal pentose phosphate pathway for long-term memory

Summary: Brain function relies almost solely on glucose as an energy substrate. The main model of brain metabolism proposes that glucose is taken up and converted into lactate by astrocytes to fuel the energy-demanding neuronal activity underlying plasticity and memory. Whether direct neuronal gluco...

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Main Authors: Eloïse de Tredern, Yasmine Rabah, Laure Pasquer, Julia Minatchy, Pierre-Yves Plaçais, Thomas Preat
Format: Article
Language:English
Published: Elsevier 2021-08-01
Series:Cell Reports
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2211124721010585
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author Eloïse de Tredern
Yasmine Rabah
Laure Pasquer
Julia Minatchy
Pierre-Yves Plaçais
Thomas Preat
author_facet Eloïse de Tredern
Yasmine Rabah
Laure Pasquer
Julia Minatchy
Pierre-Yves Plaçais
Thomas Preat
author_sort Eloïse de Tredern
collection DOAJ
description Summary: Brain function relies almost solely on glucose as an energy substrate. The main model of brain metabolism proposes that glucose is taken up and converted into lactate by astrocytes to fuel the energy-demanding neuronal activity underlying plasticity and memory. Whether direct neuronal glucose uptake is required for memory formation remains elusive. We uncover, in Drosophila, a mechanism of glucose shuttling to neurons from cortex glia, an exclusively perisomatic glial subtype, upon formation of olfactory long-term memory (LTM). In vivo imaging reveals that, downstream of cholinergic activation of cortex glia, autocrine insulin signaling increases glucose concentration in glia. Glucose is then transferred from glia to the neuronal somata in the olfactory memory center to fuel the pentose phosphate pathway and allow LTM formation. In contrast, our results indicate that the increase in neuronal glucose metabolism, although crucial for LTM formation, is not routed to glycolysis.
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spelling doaj.art-1e86f296eb18470b84240d7d1290bf722022-12-21T18:29:29ZengElsevierCell Reports2211-12472021-08-01368109620Glial glucose fuels the neuronal pentose phosphate pathway for long-term memoryEloïse de Tredern0Yasmine Rabah1Laure Pasquer2Julia Minatchy3Pierre-Yves Plaçais4Thomas Preat5Energy & Memory, Brain Plasticity Unit, CNRS, ESPCI Paris, PSL Research University, 10 rue Vauquelin, 75005 Paris, FranceEnergy & Memory, Brain Plasticity Unit, CNRS, ESPCI Paris, PSL Research University, 10 rue Vauquelin, 75005 Paris, FranceEnergy & Memory, Brain Plasticity Unit, CNRS, ESPCI Paris, PSL Research University, 10 rue Vauquelin, 75005 Paris, FranceEnergy & Memory, Brain Plasticity Unit, CNRS, ESPCI Paris, PSL Research University, 10 rue Vauquelin, 75005 Paris, FranceEnergy & Memory, Brain Plasticity Unit, CNRS, ESPCI Paris, PSL Research University, 10 rue Vauquelin, 75005 Paris, France; Corresponding authorEnergy & Memory, Brain Plasticity Unit, CNRS, ESPCI Paris, PSL Research University, 10 rue Vauquelin, 75005 Paris, France; Corresponding authorSummary: Brain function relies almost solely on glucose as an energy substrate. The main model of brain metabolism proposes that glucose is taken up and converted into lactate by astrocytes to fuel the energy-demanding neuronal activity underlying plasticity and memory. Whether direct neuronal glucose uptake is required for memory formation remains elusive. We uncover, in Drosophila, a mechanism of glucose shuttling to neurons from cortex glia, an exclusively perisomatic glial subtype, upon formation of olfactory long-term memory (LTM). In vivo imaging reveals that, downstream of cholinergic activation of cortex glia, autocrine insulin signaling increases glucose concentration in glia. Glucose is then transferred from glia to the neuronal somata in the olfactory memory center to fuel the pentose phosphate pathway and allow LTM formation. In contrast, our results indicate that the increase in neuronal glucose metabolism, although crucial for LTM formation, is not routed to glycolysis.http://www.sciencedirect.com/science/article/pii/S2211124721010585glialong-term memoryglucoseenergy metabolismpentose phosphate pathwayinsulin
spellingShingle Eloïse de Tredern
Yasmine Rabah
Laure Pasquer
Julia Minatchy
Pierre-Yves Plaçais
Thomas Preat
Glial glucose fuels the neuronal pentose phosphate pathway for long-term memory
Cell Reports
glia
long-term memory
glucose
energy metabolism
pentose phosphate pathway
insulin
title Glial glucose fuels the neuronal pentose phosphate pathway for long-term memory
title_full Glial glucose fuels the neuronal pentose phosphate pathway for long-term memory
title_fullStr Glial glucose fuels the neuronal pentose phosphate pathway for long-term memory
title_full_unstemmed Glial glucose fuels the neuronal pentose phosphate pathway for long-term memory
title_short Glial glucose fuels the neuronal pentose phosphate pathway for long-term memory
title_sort glial glucose fuels the neuronal pentose phosphate pathway for long term memory
topic glia
long-term memory
glucose
energy metabolism
pentose phosphate pathway
insulin
url http://www.sciencedirect.com/science/article/pii/S2211124721010585
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AT juliaminatchy glialglucosefuelstheneuronalpentosephosphatepathwayforlongtermmemory
AT pierreyvesplacais glialglucosefuelstheneuronalpentosephosphatepathwayforlongtermmemory
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