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Serotonergic neuron ribosomal proteins regulate the neuroendocrine control of Drosophila development

The regulation of ribosome function is a conserved mechanism of growth control. While studies in single cell systems have defined how ribosomes contribute to cell growth, the mechanisms that link ribosome function to organismal growth are less clear. Here we explore this issue using Drosophila Minut...

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Autores principales: Deliu, Lisa Patricia, Turingan, Michael, Jadir, Deeshpaul, Lee, Byoungchun, Ghosh, Abhishek, Grewal, Savraj Singh
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9473637/
https://www.ncbi.nlm.nih.gov/pubmed/36048889
http://dx.doi.org/10.1371/journal.pgen.1010371
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author Deliu, Lisa Patricia
Turingan, Michael
Jadir, Deeshpaul
Lee, Byoungchun
Ghosh, Abhishek
Grewal, Savraj Singh
author_facet Deliu, Lisa Patricia
Turingan, Michael
Jadir, Deeshpaul
Lee, Byoungchun
Ghosh, Abhishek
Grewal, Savraj Singh
author_sort Deliu, Lisa Patricia
collection PubMed
description The regulation of ribosome function is a conserved mechanism of growth control. While studies in single cell systems have defined how ribosomes contribute to cell growth, the mechanisms that link ribosome function to organismal growth are less clear. Here we explore this issue using Drosophila Minutes, a class of heterozygous mutants for ribosomal proteins. These animals exhibit a delay in larval development caused by decreased production of the steroid hormone ecdysone, the main regulator of larval maturation. We found that this developmental delay is not caused by decreases in either global ribosome numbers or translation rates. Instead, we show that they are due in part to loss of Rp function specifically in a subset of serotonin (5-HT) neurons that innervate the prothoracic gland to control ecdysone production. We find that these effects do not occur due to altered protein synthesis or proteostasis, but that Minute animals have reduced expression of synaptotagmin, a synaptic vesicle protein, and that the Minute developmental delay can be partially reversed by overexpression of synaptic vesicle proteins in 5-HTergic cells. These results identify a 5-HT cell-specific role for ribosomal function in the neuroendocrine control of animal growth and development.
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spelling pubmed-94736372022-09-15 Serotonergic neuron ribosomal proteins regulate the neuroendocrine control of Drosophila development Deliu, Lisa Patricia Turingan, Michael Jadir, Deeshpaul Lee, Byoungchun Ghosh, Abhishek Grewal, Savraj Singh PLoS Genet Research Article The regulation of ribosome function is a conserved mechanism of growth control. While studies in single cell systems have defined how ribosomes contribute to cell growth, the mechanisms that link ribosome function to organismal growth are less clear. Here we explore this issue using Drosophila Minutes, a class of heterozygous mutants for ribosomal proteins. These animals exhibit a delay in larval development caused by decreased production of the steroid hormone ecdysone, the main regulator of larval maturation. We found that this developmental delay is not caused by decreases in either global ribosome numbers or translation rates. Instead, we show that they are due in part to loss of Rp function specifically in a subset of serotonin (5-HT) neurons that innervate the prothoracic gland to control ecdysone production. We find that these effects do not occur due to altered protein synthesis or proteostasis, but that Minute animals have reduced expression of synaptotagmin, a synaptic vesicle protein, and that the Minute developmental delay can be partially reversed by overexpression of synaptic vesicle proteins in 5-HTergic cells. These results identify a 5-HT cell-specific role for ribosomal function in the neuroendocrine control of animal growth and development. Public Library of Science 2022-09-01 /pmc/articles/PMC9473637/ /pubmed/36048889 http://dx.doi.org/10.1371/journal.pgen.1010371 Text en © 2022 Deliu et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Deliu, Lisa Patricia
Turingan, Michael
Jadir, Deeshpaul
Lee, Byoungchun
Ghosh, Abhishek
Grewal, Savraj Singh
Serotonergic neuron ribosomal proteins regulate the neuroendocrine control of Drosophila development
title Serotonergic neuron ribosomal proteins regulate the neuroendocrine control of Drosophila development
title_full Serotonergic neuron ribosomal proteins regulate the neuroendocrine control of Drosophila development
title_fullStr Serotonergic neuron ribosomal proteins regulate the neuroendocrine control of Drosophila development
title_full_unstemmed Serotonergic neuron ribosomal proteins regulate the neuroendocrine control of Drosophila development
title_short Serotonergic neuron ribosomal proteins regulate the neuroendocrine control of Drosophila development
title_sort serotonergic neuron ribosomal proteins regulate the neuroendocrine control of drosophila development
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9473637/
https://www.ncbi.nlm.nih.gov/pubmed/36048889
http://dx.doi.org/10.1371/journal.pgen.1010371
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