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Identification and characterization of mushroom body neurons that regulate fat storage in Drosophila

BACKGROUND: In an earlier study, we identified two neuronal populations, c673a and Fru-GAL4, that regulate fat storage in fruit flies. Both populations partially overlap with a structure in the insect brain known as the mushroom body (MB), which plays a critical role in memory formation. This overla...

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Autores principales: Al-Anzi, Bader, Zinn, Kai
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6090720/
https://www.ncbi.nlm.nih.gov/pubmed/30103787
http://dx.doi.org/10.1186/s13064-018-0116-7
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author Al-Anzi, Bader
Zinn, Kai
author_facet Al-Anzi, Bader
Zinn, Kai
author_sort Al-Anzi, Bader
collection PubMed
description BACKGROUND: In an earlier study, we identified two neuronal populations, c673a and Fru-GAL4, that regulate fat storage in fruit flies. Both populations partially overlap with a structure in the insect brain known as the mushroom body (MB), which plays a critical role in memory formation. This overlap prompted us to examine whether the MB is also involved in fat storage homeostasis. METHODS: Using a variety of transgenic agents, we selectively manipulated the neural activity of different portions of the MB and associated neurons to decipher their roles in fat storage regulation. RESULTS: Our data show that silencing of MB neurons that project into the α’β’ lobes decreases de novo fatty acid synthesis and causes leanness, while sustained hyperactivation of the same neurons causes overfeeding and produces obesity. The α’β’ neurons oppose and dominate the fat regulating functions of the c673a and Fru-GAL4 neurons. We also show that MB neurons that project into the γ lobe also regulate fat storage, probably because they are a subset of the Fru neurons. We were able to identify input and output neurons whose activity affects fat storage, feeding, and metabolism. The activity of cholinergic output neurons that innervating the β’2 compartment (MBON-β’2mp and MBON-γ5β’2a) regulates food consumption, while glutamatergic output neurons innervating α’ compartments (MBON-γ2α’1 and MBON-α’2) control fat metabolism. CONCLUSIONS: We identified a new fat storage regulating center, the α’β’ lobes of the MB. We also delineated the neuronal circuits involved in the actions of the α’β’ lobes, and showed that food intake and fat metabolism are controlled by separate sets of postsynaptic neurons that are segregated into different output pathways. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s13064-018-0116-7) contains supplementary material, which is available to authorized users.
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spelling pubmed-60907202018-08-17 Identification and characterization of mushroom body neurons that regulate fat storage in Drosophila Al-Anzi, Bader Zinn, Kai Neural Dev Research Article BACKGROUND: In an earlier study, we identified two neuronal populations, c673a and Fru-GAL4, that regulate fat storage in fruit flies. Both populations partially overlap with a structure in the insect brain known as the mushroom body (MB), which plays a critical role in memory formation. This overlap prompted us to examine whether the MB is also involved in fat storage homeostasis. METHODS: Using a variety of transgenic agents, we selectively manipulated the neural activity of different portions of the MB and associated neurons to decipher their roles in fat storage regulation. RESULTS: Our data show that silencing of MB neurons that project into the α’β’ lobes decreases de novo fatty acid synthesis and causes leanness, while sustained hyperactivation of the same neurons causes overfeeding and produces obesity. The α’β’ neurons oppose and dominate the fat regulating functions of the c673a and Fru-GAL4 neurons. We also show that MB neurons that project into the γ lobe also regulate fat storage, probably because they are a subset of the Fru neurons. We were able to identify input and output neurons whose activity affects fat storage, feeding, and metabolism. The activity of cholinergic output neurons that innervating the β’2 compartment (MBON-β’2mp and MBON-γ5β’2a) regulates food consumption, while glutamatergic output neurons innervating α’ compartments (MBON-γ2α’1 and MBON-α’2) control fat metabolism. CONCLUSIONS: We identified a new fat storage regulating center, the α’β’ lobes of the MB. We also delineated the neuronal circuits involved in the actions of the α’β’ lobes, and showed that food intake and fat metabolism are controlled by separate sets of postsynaptic neurons that are segregated into different output pathways. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s13064-018-0116-7) contains supplementary material, which is available to authorized users. BioMed Central 2018-08-13 /pmc/articles/PMC6090720/ /pubmed/30103787 http://dx.doi.org/10.1186/s13064-018-0116-7 Text en © The Author(s). 2018 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Al-Anzi, Bader
Zinn, Kai
Identification and characterization of mushroom body neurons that regulate fat storage in Drosophila
title Identification and characterization of mushroom body neurons that regulate fat storage in Drosophila
title_full Identification and characterization of mushroom body neurons that regulate fat storage in Drosophila
title_fullStr Identification and characterization of mushroom body neurons that regulate fat storage in Drosophila
title_full_unstemmed Identification and characterization of mushroom body neurons that regulate fat storage in Drosophila
title_short Identification and characterization of mushroom body neurons that regulate fat storage in Drosophila
title_sort identification and characterization of mushroom body neurons that regulate fat storage in drosophila
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6090720/
https://www.ncbi.nlm.nih.gov/pubmed/30103787
http://dx.doi.org/10.1186/s13064-018-0116-7
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