Modulation of neuronal activity in the Drosophila mushroom body by DopEcR, a unique dual receptor for ecdysone and dopamine

Arianna Lark; Toshihiro Kitamoto; Jean-René Martin

doi:10.1016/j.bbamcr.2017.05.015

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Modulation of neuronal activity in the Drosophila mushroom body by DopEcR, a unique dual receptor for ecdysone and dopamine

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Modulation of neuronal activity in the Drosophila mushroom body by DopEcR, a unique dual receptor for ecdysone and dopamine

Arianna Lark, Toshihiro Kitamoto and Jean-René Martin

Biochimica et biophysica acta. Molecular cell research, Vol.1864(10), pp.1578-1588

10/2017

DOI: 10.1016/j.bbamcr.2017.05.015

PMID: 28554773

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Abstract

G-protein-coupled receptors (GPCRs) for steroid hormones mediate unconventional steroid signaling and play a significant role in the rapid actions of steroids in a variety of biological processes, including those in the nervous system. However, the effects of these GPCRs on overall neuronal activity remain largely elusive. Drosophila DopEcR is a GPCR that responds to both ecdysone (the major steroid hormone in insects) and dopamine, regulating multiple second messenger systems. Recent studies have revealed that DopEcR is preferentially expressed in the nervous system and involved in behavioral regulation. Here we utilized the bioluminescent Ca -indicator GFP-aequorin to monitor the nicotine-induced Ca -response within the mushroom bodies (MB), a higher-order brain center in flies, and examined how DopEcR modulates these Ca -dynamics. Our results show that in DopEcR knockdown flies, the nicotine-induced Ca -response in the MB was significantly enhanced selectively in the medial lobes. We then reveal that application of DopEcR's ligands, ecdysone and dopamine, had different effects on nicotine-induced Ca -responses in the MB: ecdysone enhanced activity in the calyx and cell body region in a DopEcR-dependent manner, whereas dopamine reduced activity in the medial lobes independently of DopEcR. Finally, we show that flies with reduced DopEcR function in the MB display decreased locomotor activity. This behavioral phenotype of DopEcR-deficient flies may be partly due to their enhanced MB activity, since the MB have been implicated in the suppression of locomotor activity. Overall, these data suggest that DopEcR is involved in region-specific modulation of Ca dynamics within the MB, which may play a role in behavioral modulation.

Drosophila melanogaster - physiology

Mushroom Bodies - physiology

Receptors, Steroid - metabolism

Signal Transduction

Receptors, Dopamine - metabolism

Receptors, G-Protein-Coupled

Drosophila melanogaster - genetics

Mushroom Bodies - drug effects

Nicotine - pharmacology

Animals

Receptors, Steroid - genetics

Neurons - physiology

Neurons - metabolism

Ecdysone - metabolism

Neurons - drug effects

Receptors, Dopamine - genetics

Dopamine - metabolism

Mushroom Bodies - metabolism

Details

Title: Subtitle: Modulation of neuronal activity in the Drosophila mushroom body by DopEcR, a unique dual receptor for ecdysone and dopamine
Creators: Arianna Lark - Interdisciplinary Program in Neuroscience, Graduate College, University of Iowa, Iowa City, IA 52242, USA
Toshihiro Kitamoto - Interdisciplinary Program in Neuroscience, Graduate College, University of Iowa, Iowa City, IA 52242, USA; Department of Anesthesia, Carver College of Medicine, University of Iowa, Iowa City, IA 52242, USA
Jean-René Martin - CNRS, NeuroPSI, UMR-9197, Imagerie Cérébrale Fonctionnelle et Comportements, 1 Avenue de la Terrasse (Bat. 32), 91198, Gif-sur-Yvette, France. Electronic address: jean-rene.martin@inaf.cnrs-gif.fr
Resource Type: Journal article
Publication Details: Biochimica et biophysica acta. Molecular cell research, Vol.1864(10), pp.1578-1588
DOI: 10.1016/j.bbamcr.2017.05.015
PMID: 28554773
NLM abbreviation: Biochim Biophys Acta Mol Cell Res
ISSN: 0167-4889
eISSN: 1879-2596
Publisher: Netherlands
Grant note: DOI: 10.13039/100000001, name: National Science Foundation, award: IOS-1352882; name: ANR FlyBrainImaging, award: ANR-11-BSV04-003-01; DOI: 10.13039/501100003990, name: Conseil Régional Île-de-France, award: OTP332581; name: CNRS
Language: English
Date published: 10/2017
Academic Unit: Iowa Neuroscience Institute; Anesthesia; Neuroscience and Pharmacology
Record Identifier: 9984007285702771

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