Axonal RNA localization is essential for long-term memory

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, Krystyna Keleman, Jernej Ule, Arnaud Hubstenberger and Florence Besse ()
Additional contact information
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
Ugur Dag: Howard Hughes Medical Institute, Janelia Research Campus
Marion Dunoyer de Segonzac: Université Côte d’Azur, CNRS, Inserm
Mirana Ramialison: 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
Arnaud Hubstenberger: Université Côte d’Azur, CNRS, Inserm
Florence Besse: Université Côte d’Azur, CNRS, Inserm

Nature Communications, 2025, vol. 16, issue 1, 1-17

Abstract: 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.

Date: 2025
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DOI: 10.1038/s41467-025-57651-7

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