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Dopamine Signalling in Mushroom Bodies Regulates Temperature-Preference Behaviour in Drosophila

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      Abstract

      The ability to respond to environmental temperature variation is essential for survival in animals. Flies show robust temperature-preference behaviour (TPB) to find optimal temperatures. Recently, we have shown that Drosophila mushroom body (MB) functions as a center controlling TPB. However, neuromodulators that control the TPB in MB remain unknown. To identify the functions of dopamine in TPB, we have conducted various genetic studies in Drosophila. Inhibition of dopamine biosynthesis by genetic mutations or treatment with chemical inhibitors caused flies to prefer temperatures colder than normal. We also found that dopaminergic neurons are involved in TPB regulation, as the targeted inactivation of dopaminergic neurons by expression of a potassium channel (Kir2.1) induced flies with the loss of cold avoidance. Consistently, the mutant flies for dopamine receptor gene (DopR) also showed a cold temperature preference, which was rescued by MB–specific expression of DopR. Based on these results, we concluded that dopamine in MB is a key component in the homeostatic temperature control of Drosophila. The current findings will provide important bases to understand the logic of thermosensation and temperature preference decision in Drosophila.

      Author Summary

      Temperature affects almost all aspects of animal development and physiological processes. The dependence of the body temperature of small insects on ambient temperature and other heat sources makes it plausible that neuronal mechanisms for sensing temperature and behavioral responses for maintaining body temperature in a permissive range must exist. By using the fruit fly model system and previously settled paradigms of temperature-preference test, we find that dopamine regulates temperature-preference behaviours. Wild-type flies show a strong temperature preference for 25°C, but inhibition of dopamine biosynthesis by genetic mutations or treatment with chemical inhibitors causes animals to prefer temperatures colder than normal. We also show that dopaminergic neurons are involved in the regulation of temperature-preference behaviours and that dopamine signalling in mushroom body neurons plays a critical role in regulating the behaviours. These results suggest that dopamine is a key component in the homeostatic temperature control of fruit flies.

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      Most cited references 59

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      A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila.

      Forward genetic screens in model organisms have provided important insights into numerous aspects of development, physiology and pathology. With the availability of complete genome sequences and the introduction of RNA-mediated gene interference (RNAi), systematic reverse genetic screens are now also possible. Until now, such genome-wide RNAi screens have mostly been restricted to cultured cells and ubiquitous gene inactivation in Caenorhabditis elegans. This powerful approach has not yet been applied in a tissue-specific manner. Here we report the generation and validation of a genome-wide library of Drosophila melanogaster RNAi transgenes, enabling the conditional inactivation of gene function in specific tissues of the intact organism. Our RNAi transgenes consist of short gene fragments cloned as inverted repeats and expressed using the binary GAL4/UAS system. We generated 22,270 transgenic lines, covering 88% of the predicted protein-coding genes in the Drosophila genome. Molecular and phenotypic assays indicate that the majority of these transgenes are functional. Our transgenic RNAi library thus opens up the prospect of systematically analysing gene functions in any tissue and at any stage of the Drosophila lifespan.
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        Spatiotemporal rescue of memory dysfunction in Drosophila.

        We have developed a method for temporal and regional gene expression targeting (TARGET) in Drosophila and show the simultaneous spatial and temporal rescue of a memory defect. The transient expression of the rutabaga-encoded adenylyl cyclase in the mushroom bodies of the adult brain was necessary and sufficient to rescue the rutabaga memory deficit, which rules out a developmental brain defect in the etiology of this deficit and demonstrates an acute role for rutabaga in memory formation in these neurons. The TARGET system offers general utility in simultaneously addressing issues of when and where gene products are required.
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          Dopamine receptors: from structure to function.

          The diverse physiological actions of dopamine are mediated by at least five distinct G protein-coupled receptor subtypes. Two D1-like receptor subtypes (D1 and D5) couple to the G protein Gs and activate adenylyl cyclase. The other receptor subtypes belong to the D2-like subfamily (D2, D3, and D4) and are prototypic of G protein-coupled receptors that inhibit adenylyl cyclase and activate K+ channels. The genes for the D1 and D5 receptors are intronless, but pseudogenes of the D5 exist. The D2 and D3 receptors vary in certain tissues and species as a result of alternative splicing, and the human D4 receptor gene exhibits extensive polymorphic variation. In the central nervous system, dopamine receptors are widely expressed because they are involved in the control of locomotion, cognition, emotion, and affect as well as neuroendocrine secretion. In the periphery, dopamine receptors are present more prominently in kidney, vasculature, and pituitary, where they affect mainly sodium homeostasis, vascular tone, and hormone secretion. Numerous genetic linkage analysis studies have failed so far to reveal unequivocal evidence for the involvement of one of these receptors in the etiology of various central nervous system disorders. However, targeted deletion of several of these dopamine receptor genes in mice should provide valuable information about their physiological functions.
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            Author and article information

            Affiliations
            [1 ]Department of Biological Sciences, Korea Advanced Institute of Science and Technology, Taejon, Korea
            [2 ]School of Biological Sciences, Chung-Ang University, Seoul, Korea
            [3 ]Department of Physiology, College of Medicine, Korea University, Seoul, Korea
            [4 ]National Creative Research Initiatives Center for Energy Homeostasis Regulation, Seoul National University, Seoul, Korea
            [5 ]Institute of Molecular Biology and Genetics, Seoul National University, Seoul, Korea
            [6 ]School of Biological Sciences, Seoul National University, Seoul, Korea
            University of California San Francisco, United States of America
            Author notes
            * E-mail: jkc@ 123456snu.ac.kr (J. Chung); jchoe@ 123456kaist.ac.kr (J. Choe)

            Conceived and designed the experiments: J Chung, J Choe. Performed the experiments: S Bang, S Hyun, S-T Hong, J Kang, K Jeong, J-J Park. Analyzed the data: S Bang, S Hyun, S-T Hong, J Kang, K Jeong, J-J Park. Wrote the paper: J Chung, S Bang.

            Contributors
            Role: Editor
            Journal
            PLoS Genet
            plos
            plosgen
            PLoS Genetics
            Public Library of Science (San Francisco, USA )
            1553-7390
            1553-7404
            March 2011
            March 2011
            24 March 2011
            : 7
            : 3
            3063753
            21455291
            10-PLGE-RA-2926R3
            10.1371/journal.pgen.1001346
            (Editor)
            Bang et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
            Counts
            Pages: 12
            Categories
            Research Article
            Neuroscience/Behavioral Neuroscience
            Neuroscience/Neural Homeostasis

            Genetics

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