Cargando…

Sex Differences in Intestinal Carbohydrate Metabolism Promote Food Intake and Sperm Maturation

Physiology and metabolism are often sexually dimorphic, but the underlying mechanisms remain incompletely understood. Here, we use the intestine of Drosophila melanogaster to investigate how gut-derived signals contribute to sex differences in whole-body physiology. We find that carbohydrate handlin...

Descripción completa

Detalles Bibliográficos
Autores principales: Hudry, Bruno, de Goeij, Eva, Mineo, Alessandro, Gaspar, Pedro, Hadjieconomou, Dafni, Studd, Chris, Mokochinski, Joao B., Kramer, Holger B., Plaçais, Pierre-Yves, Preat, Thomas, Miguel-Aliaga, Irene
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cell Press 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6700282/
https://www.ncbi.nlm.nih.gov/pubmed/31398343
http://dx.doi.org/10.1016/j.cell.2019.07.029
_version_ 1783444839448182784
author Hudry, Bruno
de Goeij, Eva
Mineo, Alessandro
Gaspar, Pedro
Hadjieconomou, Dafni
Studd, Chris
Mokochinski, Joao B.
Kramer, Holger B.
Plaçais, Pierre-Yves
Preat, Thomas
Miguel-Aliaga, Irene
author_facet Hudry, Bruno
de Goeij, Eva
Mineo, Alessandro
Gaspar, Pedro
Hadjieconomou, Dafni
Studd, Chris
Mokochinski, Joao B.
Kramer, Holger B.
Plaçais, Pierre-Yves
Preat, Thomas
Miguel-Aliaga, Irene
author_sort Hudry, Bruno
collection PubMed
description Physiology and metabolism are often sexually dimorphic, but the underlying mechanisms remain incompletely understood. Here, we use the intestine of Drosophila melanogaster to investigate how gut-derived signals contribute to sex differences in whole-body physiology. We find that carbohydrate handling is male-biased in a specific portion of the intestine. In contrast to known sexual dimorphisms in invertebrates, the sex differences in intestinal carbohydrate metabolism are extrinsically controlled by the adjacent male gonad, which activates JAK-STAT signaling in enterocytes within this intestinal portion. Sex reversal experiments establish roles for this male-biased intestinal metabolic state in controlling food intake and sperm production through gut-derived citrate. Our work uncovers a male gonad-gut axis coupling diet and sperm production, revealing that metabolic communication across organs is physiologically important. The instructive role of citrate in inter-organ communication might be significant in more biological contexts than previously recognized.
format Online
Article
Text
id pubmed-6700282
institution National Center for Biotechnology Information
language English
publishDate 2019
publisher Cell Press
record_format MEDLINE/PubMed
spelling pubmed-67002822019-08-22 Sex Differences in Intestinal Carbohydrate Metabolism Promote Food Intake and Sperm Maturation Hudry, Bruno de Goeij, Eva Mineo, Alessandro Gaspar, Pedro Hadjieconomou, Dafni Studd, Chris Mokochinski, Joao B. Kramer, Holger B. Plaçais, Pierre-Yves Preat, Thomas Miguel-Aliaga, Irene Cell Article Physiology and metabolism are often sexually dimorphic, but the underlying mechanisms remain incompletely understood. Here, we use the intestine of Drosophila melanogaster to investigate how gut-derived signals contribute to sex differences in whole-body physiology. We find that carbohydrate handling is male-biased in a specific portion of the intestine. In contrast to known sexual dimorphisms in invertebrates, the sex differences in intestinal carbohydrate metabolism are extrinsically controlled by the adjacent male gonad, which activates JAK-STAT signaling in enterocytes within this intestinal portion. Sex reversal experiments establish roles for this male-biased intestinal metabolic state in controlling food intake and sperm production through gut-derived citrate. Our work uncovers a male gonad-gut axis coupling diet and sperm production, revealing that metabolic communication across organs is physiologically important. The instructive role of citrate in inter-organ communication might be significant in more biological contexts than previously recognized. Cell Press 2019-08-08 /pmc/articles/PMC6700282/ /pubmed/31398343 http://dx.doi.org/10.1016/j.cell.2019.07.029 Text en © 2019 Medical Research Council on behalf of UKRI and Imperial College London http://creativecommons.org/licenses/by/4.0/ This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Hudry, Bruno
de Goeij, Eva
Mineo, Alessandro
Gaspar, Pedro
Hadjieconomou, Dafni
Studd, Chris
Mokochinski, Joao B.
Kramer, Holger B.
Plaçais, Pierre-Yves
Preat, Thomas
Miguel-Aliaga, Irene
Sex Differences in Intestinal Carbohydrate Metabolism Promote Food Intake and Sperm Maturation
title Sex Differences in Intestinal Carbohydrate Metabolism Promote Food Intake and Sperm Maturation
title_full Sex Differences in Intestinal Carbohydrate Metabolism Promote Food Intake and Sperm Maturation
title_fullStr Sex Differences in Intestinal Carbohydrate Metabolism Promote Food Intake and Sperm Maturation
title_full_unstemmed Sex Differences in Intestinal Carbohydrate Metabolism Promote Food Intake and Sperm Maturation
title_short Sex Differences in Intestinal Carbohydrate Metabolism Promote Food Intake and Sperm Maturation
title_sort sex differences in intestinal carbohydrate metabolism promote food intake and sperm maturation
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6700282/
https://www.ncbi.nlm.nih.gov/pubmed/31398343
http://dx.doi.org/10.1016/j.cell.2019.07.029
work_keys_str_mv AT hudrybruno sexdifferencesinintestinalcarbohydratemetabolismpromotefoodintakeandspermmaturation
AT degoeijeva sexdifferencesinintestinalcarbohydratemetabolismpromotefoodintakeandspermmaturation
AT mineoalessandro sexdifferencesinintestinalcarbohydratemetabolismpromotefoodintakeandspermmaturation
AT gasparpedro sexdifferencesinintestinalcarbohydratemetabolismpromotefoodintakeandspermmaturation
AT hadjieconomoudafni sexdifferencesinintestinalcarbohydratemetabolismpromotefoodintakeandspermmaturation
AT studdchris sexdifferencesinintestinalcarbohydratemetabolismpromotefoodintakeandspermmaturation
AT mokochinskijoaob sexdifferencesinintestinalcarbohydratemetabolismpromotefoodintakeandspermmaturation
AT kramerholgerb sexdifferencesinintestinalcarbohydratemetabolismpromotefoodintakeandspermmaturation
AT placaispierreyves sexdifferencesinintestinalcarbohydratemetabolismpromotefoodintakeandspermmaturation
AT preatthomas sexdifferencesinintestinalcarbohydratemetabolismpromotefoodintakeandspermmaturation
AT miguelaliagairene sexdifferencesinintestinalcarbohydratemetabolismpromotefoodintakeandspermmaturation