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Physiological synaptic activity and recognition memory require astroglial glutamine

Author

Listed:
  • Giselle Cheung

    (Université PSL
    Institute of Science and Technology Austria)

  • Danijela Bataveljic

    (Université PSL
    University of Belgrade)

  • Josien Visser

    (Université PSL
    Pierre and Marie Curie University)

  • Naresh Kumar

    (Université Paris Saclay, ENS Paris-Saclay, CNRS, PPSM)

  • Julien Moulard

    (Université PSL
    Pierre and Marie Curie University)

  • Glenn Dallérac

    (Université PSL
    Université Paris-Saclay, CNRS, Institut des Neurosciences Paris-Saclay)

  • Daria Mozheiko

    (Université PSL
    Pierre and Marie Curie University)

  • Astrid Rollenhagen

    (Research Center Jülich
    Rheinisch-Westfaelische Technische Hochschule Aachen University)

  • Pascal Ezan

    (Université PSL)

  • Cédric Mongin

    (Université Paris Saclay, ENS Paris-Saclay, CNRS, PPSM)

  • Oana Chever

    (Université PSL
    Normandy University, UNIROUEN, INSERM, DC2N)

  • Alexis-Pierre Bemelmans

    (Université Paris-Sud, Neurodegenerative Diseases Laboratory)

  • Joachim Lübke

    (Research Center Jülich
    Rheinisch-Westfaelische Technische Hochschule Aachen University
    Jülich-Aachen Research Alliance Translational Brain Medicine)

  • Isabelle Leray

    (Université Paris Saclay, ENS Paris-Saclay, CNRS, PPSM)

  • Nathalie Rouach

    (Université PSL)

Abstract

Presynaptic glutamate replenishment is fundamental to brain function. In high activity regimes, such as epileptic episodes, this process is thought to rely on the glutamate-glutamine cycle between neurons and astrocytes. However the presence of an astroglial glutamine supply, as well as its functional relevance in vivo in the healthy brain remain controversial, partly due to a lack of tools that can directly examine glutamine transfer. Here, we generated a fluorescent probe that tracks glutamine in live cells, which provides direct visual evidence of an activity-dependent glutamine supply from astroglial networks to presynaptic structures under physiological conditions. This mobilization is mediated by connexin43, an astroglial protein with both gap-junction and hemichannel functions, and is essential for synaptic transmission and object recognition memory. Our findings uncover an indispensable recruitment of astroglial glutamine in physiological synaptic activity and memory via an unconventional pathway, thus providing an astrocyte basis for cognitive processes.

Suggested Citation

  • Giselle Cheung & Danijela Bataveljic & Josien Visser & Naresh Kumar & Julien Moulard & Glenn Dallérac & Daria Mozheiko & Astrid Rollenhagen & Pascal Ezan & Cédric Mongin & Oana Chever & Alexis-Pierre , 2022. "Physiological synaptic activity and recognition memory require astroglial glutamine," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-28331-7
    DOI: 10.1038/s41467-022-28331-7
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    Cited by:

    1. Woo-Hyun Cho & Kyungchul Noh & Byung Hun Lee & Ellane Barcelon & Sang Beom Jun & Hye Yoon Park & Sung Joong Lee, 2022. "Hippocampal astrocytes modulate anxiety-like behavior," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    2. Moises Freitas-Andrade & Cesar H. Comin & Peter Dyken & Julie Ouellette & Joanna Raman-Nair & Nicole Blakeley & Qing Yan Liu & Sonia Leclerc & Youlian Pan & Ziying Liu & Micaël Carrier & Karan Thakur , 2023. "Astroglial Hmgb1 regulates postnatal astrocyte morphogenesis and cerebrovascular maturation," Nature Communications, Nature, vol. 14(1), pages 1-20, December.

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