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Neurotransmitters Affect Larval Development by Regulating the Activity of Prothoracicotropic Hormone-Releasing Neurons in Drosophila melanogaster

Ecdysone, an essential insect steroid hormone, promotes larval metamorphosis by coordinating growth and maturation. In Drosophila melanogaster, prothoracicotropic hormone (PTTH)-releasing neurons are considered to be the primary promoting factor in ecdysone biosynthesis. Recently, studies have repor...

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Autores principales: Hao, Shun, Gestrich, Julia Yvonne, Zhang, Xin, Xu, Mengbo, Wang, Xinwei, Liu, Li, Wei, Hongying
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8718639/
https://www.ncbi.nlm.nih.gov/pubmed/34975366
http://dx.doi.org/10.3389/fnins.2021.653858
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author Hao, Shun
Gestrich, Julia Yvonne
Zhang, Xin
Xu, Mengbo
Wang, Xinwei
Liu, Li
Wei, Hongying
author_facet Hao, Shun
Gestrich, Julia Yvonne
Zhang, Xin
Xu, Mengbo
Wang, Xinwei
Liu, Li
Wei, Hongying
author_sort Hao, Shun
collection PubMed
description Ecdysone, an essential insect steroid hormone, promotes larval metamorphosis by coordinating growth and maturation. In Drosophila melanogaster, prothoracicotropic hormone (PTTH)-releasing neurons are considered to be the primary promoting factor in ecdysone biosynthesis. Recently, studies have reported that the regulatory mechanisms of PTTH release in Drosophila larvae are controlled by different neuropeptides, including allatostatin A and corazonin. However, it remains unclear whether neurotransmitters provide input to PTTH neurons and control the metamorphosis in Drosophila larvae. Here, we report that the neurotransmitters acetylcholine (ACh) affect larval development by modulating the activity of PTTH neurons. By downregulating the expression of different subunits of nicotinic ACh receptors in PTTH neurons, pupal volume was significantly increased, whereas pupariation timing was relatively unchanged. We also identified that PTTH neurons were excited by ACh application ex vivo in a dose-dependent manner via ionotropic nicotinic ACh receptors. Moreover, in our Ca(2+) imaging experiments, relatively low doses of OA caused increased Ca(2+) levels in PTTH neurons, whereas higher doses led to decreased Ca(2+) levels. We also demonstrated that a low dose of OA was conveyed through OA β-type receptors. Additionally, our electrophysiological experiments revealed that PTTH neurons produced spontaneous activity in vivo, which provides the possibility of the bidirectional regulation, coming from neurons upstream of PTTH cells in Drosophila larvae. In summary, our findings indicate that several different neurotransmitters are involved in the regulation of larval metamorphosis by altering the activity of PTTH neurons in Drosophila.
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spelling pubmed-87186392022-01-01 Neurotransmitters Affect Larval Development by Regulating the Activity of Prothoracicotropic Hormone-Releasing Neurons in Drosophila melanogaster Hao, Shun Gestrich, Julia Yvonne Zhang, Xin Xu, Mengbo Wang, Xinwei Liu, Li Wei, Hongying Front Neurosci Neuroscience Ecdysone, an essential insect steroid hormone, promotes larval metamorphosis by coordinating growth and maturation. In Drosophila melanogaster, prothoracicotropic hormone (PTTH)-releasing neurons are considered to be the primary promoting factor in ecdysone biosynthesis. Recently, studies have reported that the regulatory mechanisms of PTTH release in Drosophila larvae are controlled by different neuropeptides, including allatostatin A and corazonin. However, it remains unclear whether neurotransmitters provide input to PTTH neurons and control the metamorphosis in Drosophila larvae. Here, we report that the neurotransmitters acetylcholine (ACh) affect larval development by modulating the activity of PTTH neurons. By downregulating the expression of different subunits of nicotinic ACh receptors in PTTH neurons, pupal volume was significantly increased, whereas pupariation timing was relatively unchanged. We also identified that PTTH neurons were excited by ACh application ex vivo in a dose-dependent manner via ionotropic nicotinic ACh receptors. Moreover, in our Ca(2+) imaging experiments, relatively low doses of OA caused increased Ca(2+) levels in PTTH neurons, whereas higher doses led to decreased Ca(2+) levels. We also demonstrated that a low dose of OA was conveyed through OA β-type receptors. Additionally, our electrophysiological experiments revealed that PTTH neurons produced spontaneous activity in vivo, which provides the possibility of the bidirectional regulation, coming from neurons upstream of PTTH cells in Drosophila larvae. In summary, our findings indicate that several different neurotransmitters are involved in the regulation of larval metamorphosis by altering the activity of PTTH neurons in Drosophila. Frontiers Media S.A. 2021-12-17 /pmc/articles/PMC8718639/ /pubmed/34975366 http://dx.doi.org/10.3389/fnins.2021.653858 Text en Copyright © 2021 Hao, Gestrich, Zhang, Xu, Wang, Liu and Wei. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Neuroscience
Hao, Shun
Gestrich, Julia Yvonne
Zhang, Xin
Xu, Mengbo
Wang, Xinwei
Liu, Li
Wei, Hongying
Neurotransmitters Affect Larval Development by Regulating the Activity of Prothoracicotropic Hormone-Releasing Neurons in Drosophila melanogaster
title Neurotransmitters Affect Larval Development by Regulating the Activity of Prothoracicotropic Hormone-Releasing Neurons in Drosophila melanogaster
title_full Neurotransmitters Affect Larval Development by Regulating the Activity of Prothoracicotropic Hormone-Releasing Neurons in Drosophila melanogaster
title_fullStr Neurotransmitters Affect Larval Development by Regulating the Activity of Prothoracicotropic Hormone-Releasing Neurons in Drosophila melanogaster
title_full_unstemmed Neurotransmitters Affect Larval Development by Regulating the Activity of Prothoracicotropic Hormone-Releasing Neurons in Drosophila melanogaster
title_short Neurotransmitters Affect Larval Development by Regulating the Activity of Prothoracicotropic Hormone-Releasing Neurons in Drosophila melanogaster
title_sort neurotransmitters affect larval development by regulating the activity of prothoracicotropic hormone-releasing neurons in drosophila melanogaster
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8718639/
https://www.ncbi.nlm.nih.gov/pubmed/34975366
http://dx.doi.org/10.3389/fnins.2021.653858
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