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

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 (KCs) 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 KC Mg²⁺. We propose that regulated neuronal Mg²⁺ efflux is critical for normal and Mg²⁺-enhanced memory.

SUBMITTER: Wu Y

PROVIDER: S-EPMC7843133 | biostudies-literature | 2020 Nov

REPOSITORIES: biostudies-literature

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

Wu Yanying Y Funato Yosuke Y Meschi Eleonora E Jovanoski Kristijan D KD Miki Hiroaki H Waddell Scott S

eLife 20201126

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 ...[more]

PMID: 33242000

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Project description:Purpose: The formation and recall of long term memory (LTM) requires neuron activity induced gene expression. Transcriptome analysis has been used to identify genes that have altered expression after memory acquisition, however, we still have an incomplete picture of the transcriptional changes that are required for LTM formation. The complex spatial and temporal dynamics of memory formation creates significant challenges in defining memory-relevant gene expression changes. The mushroom body (MB) is a signaling hub in the insect brain that integrates sensory information to form memories. Our study looks to further elucidate the transcriptional mechanisms underlying LTM by profiling gene expression changes in nuclei of the MB during a time course of LTM formation. Methods: We isolated and sequenced fly RNA from biologically paired whole head (WH) and mushroom body (MB) nuclei. MB nuclei were isolated using INTACT (isolation of nuclei tagged in a specific cell type). LTM was induced using a seven-hour courtship conditioning protocol. Fly heads were collected one hour and 24-hours after this period of sexual rejection. Samples of naive, socially isolated males were also collected at the same age and time-of-day for comparison. Results and conclusions: We identified more transcriptional changes 1 hour after memory acquisition (WH = 322, MB = 305) than at 24 hours (WH = 20, MB = 24). WH samples showed downregulation of developmental genes and upregulation of sensory response genes. In contrast, MB samples showed vastly different gene expression changes affecting biological processes that are specifically related to LTM. MB-downregulated genes were highly enriched for metabolic function, consistent with the MB-specific energy influx that occurs during LTM formation. MB-upregulated genes were highly enriched for known learning and memory processes, including calcium mediated neurotransmitter release and cAMP signalling. The neuron activity inducible genes hr38 and sr were also specifically induced in the MB. These results highlight the importance of sampling time and cell type in capturing biologically relevant transcriptional changes involved in learning and memory. Our data suggests that MB cells transiently upregulate known memory related pathways after memory acquisition, and provides a critical frame of reference for further investigation into the role MB-specific gene regulation in memory.

Dataset Information

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

Publications

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

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