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The Temporal Requirements for Insulin Signaling During Development in Drosophila

Recent studies have indicated that the insulin-signaling pathway controls body and organ size in Drosophila, and most metazoans, by signaling nutritional conditions to the growing organs. The temporal requirements for insulin signaling during development are, however, unknown. Using a temperature-se...

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Autores principales: Shingleton, Alexander W, Das, Jayatri, Vinicius, Lucio, Stern, David L
Formato: Texto
Lenguaje:English
Publicado: Public Library of Science 2005
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1184592/
https://www.ncbi.nlm.nih.gov/pubmed/16086608
http://dx.doi.org/10.1371/journal.pbio.0030289
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author Shingleton, Alexander W
Das, Jayatri
Vinicius, Lucio
Stern, David L
author_facet Shingleton, Alexander W
Das, Jayatri
Vinicius, Lucio
Stern, David L
author_sort Shingleton, Alexander W
collection PubMed
description Recent studies have indicated that the insulin-signaling pathway controls body and organ size in Drosophila, and most metazoans, by signaling nutritional conditions to the growing organs. The temporal requirements for insulin signaling during development are, however, unknown. Using a temperature-sensitive insulin receptor (Inr) mutation in Drosophila, we show that the developmental requirements for Inr activity are organ specific and vary in time. Early in development, before larvae reach the “critical size” (the size at which they commit to metamorphosis and can complete development without further feeding), Inr activity influences total development time but not final body and organ size. After critical size, Inr activity no longer affects total development time but does influence final body and organ size. Final body size is affected by Inr activity from critical size until pupariation, whereas final organ size is sensitive to Inr activity from critical size until early pupal development. In addition, different organs show different sensitivities to changes in Inr activity for different periods of development, implicating the insulin pathway in the control of organ allometry. The reduction in Inr activity is accompanied by a two-fold increase in free-sugar levels, similar to the effect of reduced insulin signaling in mammals. Finally, we find that varying the magnitude of Inr activity has different effects on cell size and cell number in the fly wing, providing a potential linkage between the mode of action of insulin signaling and the distinct downstream controls of cell size and number. We present a model that incorporates the effects of the insulin-signaling pathway into the Drosophila life cycle. We hypothesize that the insulin-signaling pathway controls such diverse effects as total developmental time, total body size and organ size through its effects on the rate of cell growth, and proliferation in different organs.
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spelling pubmed-11845922005-08-16 The Temporal Requirements for Insulin Signaling During Development in Drosophila Shingleton, Alexander W Das, Jayatri Vinicius, Lucio Stern, David L PLoS Biol Research Article Recent studies have indicated that the insulin-signaling pathway controls body and organ size in Drosophila, and most metazoans, by signaling nutritional conditions to the growing organs. The temporal requirements for insulin signaling during development are, however, unknown. Using a temperature-sensitive insulin receptor (Inr) mutation in Drosophila, we show that the developmental requirements for Inr activity are organ specific and vary in time. Early in development, before larvae reach the “critical size” (the size at which they commit to metamorphosis and can complete development without further feeding), Inr activity influences total development time but not final body and organ size. After critical size, Inr activity no longer affects total development time but does influence final body and organ size. Final body size is affected by Inr activity from critical size until pupariation, whereas final organ size is sensitive to Inr activity from critical size until early pupal development. In addition, different organs show different sensitivities to changes in Inr activity for different periods of development, implicating the insulin pathway in the control of organ allometry. The reduction in Inr activity is accompanied by a two-fold increase in free-sugar levels, similar to the effect of reduced insulin signaling in mammals. Finally, we find that varying the magnitude of Inr activity has different effects on cell size and cell number in the fly wing, providing a potential linkage between the mode of action of insulin signaling and the distinct downstream controls of cell size and number. We present a model that incorporates the effects of the insulin-signaling pathway into the Drosophila life cycle. We hypothesize that the insulin-signaling pathway controls such diverse effects as total developmental time, total body size and organ size through its effects on the rate of cell growth, and proliferation in different organs. Public Library of Science 2005-09 2005-08-16 /pmc/articles/PMC1184592/ /pubmed/16086608 http://dx.doi.org/10.1371/journal.pbio.0030289 Text en Copyright: © 2005 Shingleton et al. http://creativecommons.org/licenses/by/4.0/ 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 properly credited.
spellingShingle Research Article
Shingleton, Alexander W
Das, Jayatri
Vinicius, Lucio
Stern, David L
The Temporal Requirements for Insulin Signaling During Development in Drosophila
title The Temporal Requirements for Insulin Signaling During Development in Drosophila
title_full The Temporal Requirements for Insulin Signaling During Development in Drosophila
title_fullStr The Temporal Requirements for Insulin Signaling During Development in Drosophila
title_full_unstemmed The Temporal Requirements for Insulin Signaling During Development in Drosophila
title_short The Temporal Requirements for Insulin Signaling During Development in Drosophila
title_sort temporal requirements for insulin signaling during development in drosophila
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1184592/
https://www.ncbi.nlm.nih.gov/pubmed/16086608
http://dx.doi.org/10.1371/journal.pbio.0030289
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