1. Neuroscience

Magnesium efflux from Drosophila Kenyon Cells is critical for normal and diet-enhanced long-term memory

  1. Yanying Wu
  2. Yosuke Funato
  3. Eleonora Meschi
  4. Kristijan Jovanoski
  5. Hiroaki Miki
  6. Scott Waddell  Is a corresponding author
  1. University of Oxford, United Kingdom
  2. Osaka University, Japan
https://doi.org/10.7554/eLife.61339
Share this article
Cite this article
  1. Yanying Wu
  2. Yosuke Funato
  3. Eleonora Meschi
  4. Kristijan Jovanoski
  5. Hiroaki Miki
  6. Scott Waddell
(2020)
Magnesium efflux from Drosophila Kenyon Cells is critical for normal and diet-enhanced long-term memory
eLife 9:e61339.
https://doi.org/10.7554/eLife.61339
  2. Download BibTeX
  3. Download .RIS

Abstract

Dietary magnesium (Mg2+) supplementation can enhance memory in young and aged rats. Memory-enhancing capacity was largely ascribed to increases in hippocampal synaptic density and elevated expression of the NR2B subunit of the NMDA-type glutamate receptor. Here we show that Mg2+ feeding also enhances long-term memory in Drosophila. Normal and Mg2+ enhanced fly memory appears independent of NMDA receptors in the mushroom body and instead requires expression of a conserved CNNM-type Mg2+-efflux transporter encoded by the unextended (uex) gene. UEX contains a putative cyclic nucleotide-binding homology domain and its mutation separates a vital role for uex from a function in memory. Moreover, UEX localization in mushroom body Kenyon Cells is altered in memory defective flies harboring mutations in cAMP-related genes. Functional imaging suggests that UEX-dependent efflux is required for slow rhythmic maintenance of Kenyon Cell Mg2+. We propose that regulated neuronal Mg2+ efflux is critical for normal and Mg2+ enhanced memory.

Data availability

Behaviour data from T-maza assays deposited in Dryad Digital Repository (doi:10.5061/dryad.q2bvq83hs). All other data generated or analysed during this study are included in the manuscript and supporting files.

The following data sets were generated

Article and author information

Author details

  1. Yanying Wu

    Centre for Neural Circuits & Behaviour, University of Oxford, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.

  2. Yosuke Funato

    Department of Cellular Regulation, Osaka University, Osaka, Japan
    Competing interests
    The authors declare that no competing interests exist.

  3. Eleonora Meschi

    Centre for Neural Circuits & Behaviour, University of Oxford, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2401-7969

  4. Kristijan Jovanoski

    Centre for Neural Circuits & Behaviour, University of Oxford, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.

  5. Hiroaki Miki

    Department of Cellular Regulation, Osaka University, Osaka, Japan
    Competing interests
    The authors declare that no competing interests exist.

  6. Scott Waddell

    Centre for Neural Circuits & Behaviour, University of Oxford, Oxford, United Kingdom
    For correspondence
    scott.waddell@cncb.ox.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4503-6229

Funding

Wellcome (200846/Z/16/Z)

  • Scott Waddell

European Commission (789274)

  • Scott Waddell

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. K VijayRaghavan, National Centre for Biological Sciences, Tata Institute of Fundamental Research, India

Version history

  1. Received: July 22, 2020
  2. Accepted: November 25, 2020
  3. Accepted Manuscript published: November 26, 2020 (version 1)
  4. Version of Record published: January 28, 2021 (version 2)

Copyright

© 2020, Wu et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 3,441
    views
  • 441
    downloads
  • 7
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Yanying Wu
  2. Yosuke Funato
  3. Eleonora Meschi
  4. Kristijan Jovanoski
  5. Hiroaki Miki
  6. Scott Waddell
(2020)
Magnesium efflux from Drosophila Kenyon Cells is critical for normal and diet-enhanced long-term memory
eLife 9:e61339.
https://doi.org/10.7554/eLife.61339

Share this article

https://doi.org/10.7554/eLife.61339

Categories and tags

Research organism

Further reading

    1. Neuroscience

    Memory: A divalent boost from magnesium

    Willem J Laursen, Paul A Garrity
    Insight

    Enhanced levels of dietary magnesium improve long-term memory in fruit flies.

  2. Listen to Scott Waddell explain how we could improve our memory.

    Podcast

    Magnesium supplements help boost long-term memory in flies

    1. Medicine
    2. Neuroscience

    Txnip deletions and missense alleles prolong the survival of cones in a retinitis pigmentosa mouse model

    Yunlu Xue, Yimin Zhou, Constance L Cepko
    Research Advance

    Retinitis pigmentosa (RP) is an inherited retinal disease in which there is a loss of cone-mediated daylight vision. As there are >100 disease genes, our goal is to preserve cone vision in a disease gene-agnostic manner. Previously we showed that overexpressing TXNIP, an α-arrestin protein, prolonged cone vision in RP mouse models, using an AAV to express it only in cones. Here, we expressed different alleles of Txnip in the retinal pigmented epithelium (RPE), a support layer for cones. Our goal was to learn more of TXNIP’s structure-function relationships for cone survival, as well as determine the optimal cell type expression pattern for cone survival. The C-terminal half of TXNIP was found to be sufficient to remove GLUT1 from the cell surface, and improved RP cone survival, when expressed in the RPE, but not in cones. Knock-down of HSP90AB1, a TXNIP-interactor which regulates metabolism, improved the survival of cones alone and was additive for cone survival when combined with TXNIP. From these and other results, it is likely that TXNIP interacts with several proteins in the RPE to indirectly support cone survival, with some of these interactions different from those that lead to cone survival when expressed only in cones.