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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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2015-07-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/06930 |
| _version_ | 1828167307282612224 |
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| author | Tobias Reiff Jake Jacobson Paola Cognigni Zeus Antonello Esther Ballesta Kah Junn Tan Joanne Y Yew Maria Dominguez Irene Miguel-Aliaga |
| author_facet | Tobias Reiff Jake Jacobson Paola Cognigni Zeus Antonello Esther Ballesta Kah Junn Tan Joanne Y Yew Maria Dominguez Irene Miguel-Aliaga |
| author_sort | Tobias Reiff |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-04-12T02:14:33Z |
| format | Article |
| id | doaj.art-6302a9c5427f4c098b2d1bf012cfe315 |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-12T02:14:33Z |
| publishDate | 2015-07-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-6302a9c5427f4c098b2d1bf012cfe3152022-12-22T03:52:17ZengeLife Sciences Publications LtdeLife2050-084X2015-07-01410.7554/eLife.06930Endocrine remodelling of the adult intestine sustains reproduction in DrosophilaTobias Reiff0Jake Jacobson1Paola Cognigni2Zeus Antonello3Esther Ballesta4Kah Junn Tan5Joanne Y Yew6Maria Dominguez7Irene Miguel-Aliaga8Instituto de Neurociencias, Consejo Superior de Investigaciones Cientificas, Universidad Miguel Hernández, Alicante, SpainMRC Clinical Sciences Centre, Imperial College London, London, United KingdomMRC Clinical Sciences Centre, Imperial College London, London, United KingdomInstituto de Neurociencias, Consejo Superior de Investigaciones Cientificas, Universidad Miguel Hernández, Alicante, SpainInstituto de Neurociencias, Consejo Superior de Investigaciones Cientificas, Universidad Miguel Hernández, Alicante, SpainTemasek Life Sciences Laboratory, Singapore, SingaporeTemasek Life Sciences Laboratory, Singapore, Singapore; Department of Biological Sciences, National University of Singapore, Singapore, SingaporeInstituto de Neurociencias, Consejo Superior de Investigaciones Cientificas, Universidad Miguel Hernández, Alicante, SpainMRC Clinical Sciences Centre, Imperial College London, London, United KingdomThe 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.https://elifesciences.org/articles/06930intestinestem cellorgan plasticity |
| spellingShingle | Tobias Reiff Jake Jacobson Paola Cognigni Zeus Antonello Esther Ballesta Kah Junn Tan Joanne Y Yew Maria Dominguez Irene Miguel-Aliaga Endocrine remodelling of the adult intestine sustains reproduction in Drosophila eLife intestine stem cell organ plasticity |
| 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 | intestine stem cell organ plasticity |
| url | https://elifesciences.org/articles/06930 |
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