IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-54778-x.html
   My bibliography  Save this article

Diverting glial glycolytic flux towards neurons is a memory-relevant role of Drosophila CRH-like signalling

Author

Listed:
  • Raquel Francés

    (Energy & Memory, Brain Plasticity (UMR 8249), CNRS, ESPCI Paris, PSL Research University)

  • Yasmine Rabah

    (Energy & Memory, Brain Plasticity (UMR 8249), CNRS, ESPCI Paris, PSL Research University)

  • Thomas Preat

    (Energy & Memory, Brain Plasticity (UMR 8249), CNRS, ESPCI Paris, PSL Research University)

  • Pierre-Yves Plaçais

    (Energy & Memory, Brain Plasticity (UMR 8249), CNRS, ESPCI Paris, PSL Research University)

Abstract

An essential role of glial cells is to comply with the large and fluctuating energy needs of neurons. Metabolic adaptation is integral to the acute stress response, suggesting that glial cells could be major, yet overlooked, targets of stress hormones. Here we show that Dh44 neuropeptide, Drosophila homologue of mammalian corticotropin-releasing hormone (CRH), acts as an experience-dependent metabolic switch for glycolytic output in glia. Dh44 released by dopamine neurons limits glial fatty acid synthesis and build-up of lipid stores. Although basally active, this hormonal axis is acutely stimulated following learning of a danger-predictive cue. This results in transient suppression of glial anabolic use of pyruvate, sparing it for memory-relevant energy supply to neurons. Diverting pyruvate destination may dampen the need to upregulate glial glycolysis in response to increased neuronal demand. Although beneficial for the energy efficiency of memory formation, this mechanism reveals an ongoing competition between neuronal fuelling and glial anabolism.

Suggested Citation

  • Raquel Francés & Yasmine Rabah & Thomas Preat & Pierre-Yves Plaçais, 2024. "Diverting glial glycolytic flux towards neurons is a memory-relevant role of Drosophila CRH-like signalling," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-54778-x
    DOI: 10.1038/s41467-024-54778-x
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-54778-x
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-024-54778-x?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Dafni Hadjieconomou & George King & Pedro Gaspar & Alessandro Mineo & Laura Blackie & Tomotsune Ameku & Chris Studd & Alex Mendoza & Fengqiu Diao & Benjamin H. White & André E. X. Brown & Pierre-Yves , 2020. "Enteric neurons increase maternal food intake during reproduction," Nature, Nature, vol. 587(7834), pages 455-459, November.
    2. Daniel Jimenez-Blasco & Arnau Busquets-Garcia & Etienne Hebert-Chatelain & Roman Serrat & Carlos Vicente-Gutierrez & Christina Ioannidou & Paula Gómez-Sotres & Irene Lopez-Fabuel & Monica Resch-Beushe, 2020. "Glucose metabolism links astroglial mitochondria to cannabinoid effects," Nature, Nature, vol. 583(7817), pages 603-608, July.
    3. Rubing Zhao-Shea & Steven R. DeGroot & Liwang Liu & Markus Vallaster & Xueyan Pang & Qin Su & Guangping Gao & Oliver J. Rando & Gilles E. Martin & Olivier George & Paul D. Gardner & Andrew R. Tapper, 2015. "Increased CRF signalling in a ventral tegmental area-interpeduncular nucleus-medial habenula circuit induces anxiety during nicotine withdrawal," Nature Communications, Nature, vol. 6(1), pages 1-14, November.
    4. Ellen McMullen & Helen Hertenstein & Katrin Strassburger & Leon Deharde & Marko Brankatschk & Stefanie Schirmeier, 2023. "Glycolytically impaired Drosophila glial cells fuel neural metabolism via β-oxidation," Nature Communications, Nature, vol. 14(1), pages 1-9, December.
    5. Sven Dorkenwald & Arie Matsliah & Amy R. Sterling & Philipp Schlegel & Szi-chieh Yu & Claire E. McKellar & Albert Lin & Marta Costa & Katharina Eichler & Yijie Yin & Will Silversmith & Casey Schneider, 2024. "Neuronal wiring diagram of an adult brain," Nature, Nature, vol. 634(8032), pages 124-138, October.
    6. Dafni Hadjieconomou & George King & Pedro Gaspar & Alessandro Mineo & Laura Blackie & Tomotsune Ameku & Chris Studd & Alex Mendoza & Fengqiu Diao & Benjamin H. White & André E. X. Brown & Pierre-Yves , 2020. "Author Correction: Enteric neurons increase maternal food intake during reproduction," Nature, Nature, vol. 588(7839), pages 36-36, December.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Junjun Gao & Song Zhang & Pan Deng & Zhigang Wu & Bruno Lemaitre & Zongzhao Zhai & Zheng Guo, 2024. "Dietary L-Glu sensing by enteroendocrine cells adjusts food intake via modulating gut PYY/NPF secretion," Nature Communications, Nature, vol. 15(1), pages 1-22, December.
    2. Christian F. Christensen & Quentin Laurichesse & Rihab Loudhaief & Julien Colombani & Ditte S. Andersen, 2024. "Drosophila activins adapt gut size to food intake and promote regenerative growth," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    3. Yunpo Zhao & Mohammed A. Khallaf & Emilia Johansson & Najat Dzaki & Shreelatha Bhat & Johannes Alfredsson & Jianli Duan & Bill S. Hansson & Markus Knaden & Mattias Alenius, 2022. "Hedgehog-mediated gut-taste neuron axis controls sweet perception in Drosophila," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    4. Nathan Fearby & Samantha Penman & Panayotis Thanos, 2022. "Effects of Δ9-Tetrahydrocannibinol (THC) on Obesity at Different Stages of Life: A Literature Review," IJERPH, MDPI, vol. 19(6), pages 1-28, March.
    5. Yuto Hasegawa & Juhyun Kim & Gianluca Ursini & Yan Jouroukhin & Xiaolei Zhu & Yu Miyahara & Feiyi Xiong & Samskruthi Madireddy & Mizuho Obayashi & Beat Lutz & Akira Sawa & Solange P. Brown & Mikhail V, 2023. "Microglial cannabinoid receptor type 1 mediates social memory deficits in mice produced by adolescent THC exposure and 16p11.2 duplication," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    6. Ignacio Fernández-Moncada & Gianluca Lavanco & Unai B. Fundazuri & Nasrin Bollmohr & Sarah Mountadem & Tommaso Dalla Tor & Pauline Hachaguer & Francisca Julio-Kalajzic & Doriane Gisquet & Roman Serrat, 2024. "A lactate-dependent shift of glycolysis mediates synaptic and cognitive processes in male mice," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    7. Albert Stuart Reece & Gary Kenneth Hulse, 2022. "Epigenomic and Other Evidence for Cannabis-Induced Aging Contextualized in a Synthetic Epidemiologic Overview of Cannabinoid-Related Teratogenesis and Cannabinoid-Related Carcinogenesis," IJERPH, MDPI, vol. 19(24), pages 1-57, December.
    8. Burak Gür & Luisa Ramirez & Jacqueline Cornean & Freya Thurn & Sebastian Molina-Obando & Giordano Ramos-Traslosheros & Marion Silies, 2024. "Neural pathways and computations that achieve stable contrast processing tuned to natural scenes," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    9. Weihua Ding & Liuyue Yang & Eleanor Shi & Bowon Kim & Sarah Low & Kun Hu & Lei Gao & Ping Chen & Wei Ding & David Borsook & Andrew Luo & Jee Hyun Choi & Changning Wang & Oluwaseun Akeju & Jun Yang & C, 2023. "The endocannabinoid N-arachidonoyl dopamine is critical for hyperalgesia induced by chronic sleep disruption," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    10. Paula Gómez-Sotres & Urszula Skupio & Tommaso Dalla Tor & Francisca Julio-Kalajzic & Astrid Cannich & Doriane Gisquet & Itziar Bonilla-Del Rio & Filippo Drago & Nagore Puente & Pedro Grandes & Luigi B, 2024. "Olfactory bulb astrocytes link social transmission of stress to cognitive adaptation in male mice," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    11. Kirsten Bohmbach & Nicola Masala & Eva M. Schönhense & Katharina Hill & André N. Haubrich & Andreas Zimmer & Thoralf Opitz & Heinz Beck & Christian Henneberger, 2022. "An astrocytic signaling loop for frequency-dependent control of dendritic integration and spatial learning," Nature Communications, Nature, vol. 13(1), pages 1-17, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-54778-x. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.