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Endocrine remodelling of the adult intestine sustains reproduction in Drosophila

The production of offspring is energetically costly and relies on incompletely understood mechanisms that generate a positive energy balance. In mothers of many species, changes in key energy-associated internal organs are common yet poorly characterised functionally and mechanistically. In this stu...

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Autores principales: Reiff, Tobias, Jacobson, Jake, Cognigni, Paola, Antonello, Zeus, Ballesta, Esther, Tan, Kah Junn, Yew, Joanne Y, Dominguez, Maria, Miguel-Aliaga, Irene
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4515472/
https://www.ncbi.nlm.nih.gov/pubmed/26216039
http://dx.doi.org/10.7554/eLife.06930
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author Reiff, Tobias
Jacobson, Jake
Cognigni, Paola
Antonello, Zeus
Ballesta, Esther
Tan, Kah Junn
Yew, Joanne Y
Dominguez, Maria
Miguel-Aliaga, Irene
author_facet Reiff, Tobias
Jacobson, Jake
Cognigni, Paola
Antonello, Zeus
Ballesta, Esther
Tan, Kah Junn
Yew, Joanne Y
Dominguez, Maria
Miguel-Aliaga, Irene
author_sort Reiff, Tobias
collection PubMed
description The production of offspring is energetically costly and relies on incompletely understood mechanisms that generate a positive energy balance. In mothers of many species, changes in key energy-associated internal organs are common yet poorly characterised functionally and mechanistically. In this study, we show that, in adult Drosophila females, the midgut is dramatically remodelled to enhance reproductive output. In contrast to extant models, organ remodelling does not occur in response to increased nutrient intake and/or offspring demands, but rather precedes them. With spatially and temporally directed manipulations, we identify juvenile hormone (JH) as an anticipatory endocrine signal released after mating. Acting through intestinal bHLH-PAS domain proteins Methoprene-tolerant (Met) and Germ cell-expressed (Gce), JH signals directly to intestinal progenitors to yield a larger organ, and adjusts gene expression and sterol regulatory element-binding protein (SREBP) activity in enterocytes to support increased lipid metabolism. Our findings identify a metabolically significant paradigm of adult somatic organ remodelling linking hormonal signals, epithelial plasticity, and reproductive output. DOI: http://dx.doi.org/10.7554/eLife.06930.001
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spelling pubmed-45154722015-07-29 Endocrine remodelling of the adult intestine sustains reproduction in Drosophila Reiff, Tobias Jacobson, Jake Cognigni, Paola Antonello, Zeus Ballesta, Esther Tan, Kah Junn Yew, Joanne Y Dominguez, Maria Miguel-Aliaga, Irene eLife Developmental Biology and Stem Cells The production of offspring is energetically costly and relies on incompletely understood mechanisms that generate a positive energy balance. In mothers of many species, changes in key energy-associated internal organs are common yet poorly characterised functionally and mechanistically. In this study, we show that, in adult Drosophila females, the midgut is dramatically remodelled to enhance reproductive output. In contrast to extant models, organ remodelling does not occur in response to increased nutrient intake and/or offspring demands, but rather precedes them. With spatially and temporally directed manipulations, we identify juvenile hormone (JH) as an anticipatory endocrine signal released after mating. Acting through intestinal bHLH-PAS domain proteins Methoprene-tolerant (Met) and Germ cell-expressed (Gce), JH signals directly to intestinal progenitors to yield a larger organ, and adjusts gene expression and sterol regulatory element-binding protein (SREBP) activity in enterocytes to support increased lipid metabolism. Our findings identify a metabolically significant paradigm of adult somatic organ remodelling linking hormonal signals, epithelial plasticity, and reproductive output. DOI: http://dx.doi.org/10.7554/eLife.06930.001 eLife Sciences Publications, Ltd 2015-07-28 /pmc/articles/PMC4515472/ /pubmed/26216039 http://dx.doi.org/10.7554/eLife.06930 Text en © 2015, Reiff et al http://creativecommons.org/licenses/by/4.0/ This article is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Developmental Biology and Stem Cells
Reiff, Tobias
Jacobson, Jake
Cognigni, Paola
Antonello, Zeus
Ballesta, Esther
Tan, Kah Junn
Yew, Joanne Y
Dominguez, Maria
Miguel-Aliaga, Irene
Endocrine remodelling of the adult intestine sustains reproduction in Drosophila
title Endocrine remodelling of the adult intestine sustains reproduction in Drosophila
title_full Endocrine remodelling of the adult intestine sustains reproduction in Drosophila
title_fullStr Endocrine remodelling of the adult intestine sustains reproduction in Drosophila
title_full_unstemmed Endocrine remodelling of the adult intestine sustains reproduction in Drosophila
title_short Endocrine remodelling of the adult intestine sustains reproduction in Drosophila
title_sort endocrine remodelling of the adult intestine sustains reproduction in drosophila
topic Developmental Biology and Stem Cells
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4515472/
https://www.ncbi.nlm.nih.gov/pubmed/26216039
http://dx.doi.org/10.7554/eLife.06930
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