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Axonal RNA localization is essential for long-term memory

Author

Listed:
  • Bruna R. Queiroz

    (Université Côte d’Azur, CNRS, Inserm)

  • Hiba Laghrissi

    (Université Côte d’Azur, CNRS, Inserm)

  • Seetha Rajeev

    (Université Côte d’Azur, CNRS, Inserm)

  • Lauren Blot

    (Université Côte d’Azur, CNRS, Inserm)

  • Fabienne Graeve

    (Université Côte d’Azur, CNRS, Inserm)

  • Marine Dehecq

    (Université Côte d’Azur, CNRS, Inserm)

  • Martina Hallegger

    (The Francis Crick Institute
    UK Dementia Research Institute at King’s College London
    University of Oxford)

  • Ugur Dag

    (Howard Hughes Medical Institute, Janelia Research Campus)

  • Marion Dunoyer de Segonzac

    (Université Côte d’Azur, CNRS, Inserm)

  • Mirana Ramialison

    (University of Melbourne
    Australian Regenerative Medicine Institute
    University of Melbourne)

  • Chantal Cazevieille

    (INM, Université de Montpellier, Inserm)

  • Krystyna Keleman

    (Howard Hughes Medical Institute, Janelia Research Campus)

  • Jernej Ule

    (The Francis Crick Institute
    UK Dementia Research Institute at King’s College London
    King’s College London)

  • Arnaud Hubstenberger

    (Université Côte d’Azur, CNRS, Inserm)

  • Florence Besse

    (Université Côte d’Azur, CNRS, Inserm)

Abstract

Localization of mRNAs to neuronal terminals, coupled to local translation, has emerged as a prevalent mechanism controlling the synaptic proteome. However, the physiological regulation and function of this process in the context of mature in vivo memory circuits has remained unclear. Here, we combined synaptosome RNA profiling with whole brain high-resolution imaging to uncover mRNAs with different localization patterns in the axons of Drosophila Mushroom Body memory neurons, some exhibiting regionalized, input-dependent, recruitment along axons. By integrating transcriptome-wide binding approaches and functional assays, we show that the conserved Imp RNA binding protein controls the transport of mRNAs to Mushroom Body axons and characterize a mutant in which this transport is selectively impaired. Using this unique mutant, we demonstrate that axonal mRNA localization is required for long-term, but not short-term, behavioral memory. This work uncovers circuit-dependent mRNA targeting in vivo and demonstrates the importance of local RNA regulation in memory consolidation.

Suggested Citation

  • Bruna R. Queiroz & Hiba Laghrissi & Seetha Rajeev & Lauren Blot & Fabienne Graeve & Marine Dehecq & Martina Hallegger & Ugur Dag & Marion Dunoyer de Segonzac & Mirana Ramialison & Chantal Cazevieille , 2025. "Axonal RNA localization is essential for long-term memory," Nature Communications, Nature, vol. 16(1), pages 1-17, December.
    • Handle: RePEc:nat:natcom:v:16:y:2025:i:1:d:10.1038_s41467-025-57651-7
    DOI: 10.1038/s41467-025-57651-7
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    References listed on IDEAS

    as
    1. Jeshlee Vijayakumar & Charlène Perrois & Marjorie Heim & Luc Bousset & Simon Alberti & Florence Besse, 2019. "The prion-like domain of Drosophila Imp promotes axonal transport of RNP granules in vivo," Nature Communications, Nature, vol. 10(1), pages 1-14, December.
    2. Karl E. Bauer & Inmaculada Segura & Imre Gaspar & Volker Scheuss & Christin Illig & Georg Ammer & Saskia Hutten & Eugénia Basyuk & Sandra M. Fernández-Moya & Janina Ehses & Edouard Bertrand & Michael , 2019. "Live cell imaging reveals 3′-UTR dependent mRNA sorting to synapses," Nature Communications, Nature, vol. 10(1), pages 1-13, December.
    3. Zhengchang Lei & Kristin Henderson & Krystyna Keleman, 2022. "A neural circuit linking learning and sleep in Drosophila long-term memory," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    4. Kavya Vinayan Pushpalatha & Mathilde Solyga & Akira Nakamura & Florence Besse, 2022. "RNP components condense into repressive RNP granules in the aging brain," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
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