Hormone-sensitive lipase couples intergenerational sterol metabolism to reproductive success

Triacylglycerol (TG) and steryl ester (SE) lipid storage is a universal strategy to maintain organismal energy and membrane homeostasis. Cycles of building and mobilizing storage fat are fundamental in (re)distributing lipid substrates between tissues or to progress ontogenetic transitions. In this...

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Main Authors: Christoph Heier, Oskar Knittelfelder, Harald F Hofbauer, Wolfgang Mende, Ingrid Pörnbacher, Laura Schiller, Gabriele Schoiswohl, Hao Xie, Sebastian Grönke, Andrej Shevchenko, Ronald P Kühnlein
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2021-02-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/63252
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author Christoph Heier
Oskar Knittelfelder
Harald F Hofbauer
Wolfgang Mende
Ingrid Pörnbacher
Laura Schiller
Gabriele Schoiswohl
Hao Xie
Sebastian Grönke
Andrej Shevchenko
Ronald P Kühnlein
author_facet Christoph Heier
Oskar Knittelfelder
Harald F Hofbauer
Wolfgang Mende
Ingrid Pörnbacher
Laura Schiller
Gabriele Schoiswohl
Hao Xie
Sebastian Grönke
Andrej Shevchenko
Ronald P Kühnlein
author_sort Christoph Heier
collection DOAJ
description Triacylglycerol (TG) and steryl ester (SE) lipid storage is a universal strategy to maintain organismal energy and membrane homeostasis. Cycles of building and mobilizing storage fat are fundamental in (re)distributing lipid substrates between tissues or to progress ontogenetic transitions. In this study, we show that Hormone-sensitive lipase (Hsl) specifically controls SE mobilization to initiate intergenerational sterol transfer in Drosophila melanogaster. Tissue-autonomous Hsl functions in the maternal fat body and germline coordinately prevent adult SE overstorage and maximize sterol allocation to embryos. While Hsl-deficiency is largely dispensable for normal development on sterol-rich diets, animals depend on adipocyte Hsl for optimal fecundity when dietary sterol becomes limiting. Notably, accumulation of SE but not of TG is a characteristic of Hsl-deficient cells across phyla including murine white adipocytes. In summary, we identified Hsl as an ancestral regulator of SE degradation, which improves intergenerational sterol transfer and reproductive success in flies.
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spelling doaj.art-f44cb629f0a14f5886e00d24a7b6c7ad2022-12-22T03:33:51ZengeLife Sciences Publications LtdeLife2050-084X2021-02-011010.7554/eLife.63252Hormone-sensitive lipase couples intergenerational sterol metabolism to reproductive successChristoph Heier0https://orcid.org/0000-0001-6858-408XOskar Knittelfelder1https://orcid.org/0000-0002-1565-7238Harald F Hofbauer2https://orcid.org/0000-0003-2617-5901Wolfgang Mende3Ingrid Pörnbacher4Laura Schiller5Gabriele Schoiswohl6Hao Xie7Sebastian Grönke8https://orcid.org/0000-0002-1539-5346Andrej Shevchenko9https://orcid.org/0000-0002-5079-1109Ronald P Kühnlein10Institute of Molecular Biosciences, University of Graz, Graz, Austria; BioTechMed-Graz, Graz, AustriaMax Planck Institute of Molecular Cell Biology and Genetics, Dresden, GermanyInstitute of Molecular Biosciences, University of Graz, Graz, Austria; BioTechMed-Graz, Graz, AustriaInstitute of Molecular Biosciences, University of Graz, Graz, AustriaInstitute of Molecular Biosciences, University of Graz, Graz, AustriaInstitute of Molecular Biosciences, University of Graz, Graz, AustriaInstitute of Molecular Biosciences, University of Graz, Graz, Austria; Field of Excellence BioHealth - University of Graz, Graz, AustriaInstitute of Molecular Biosciences, University of Graz, Graz, AustriaMax Planck Institute for Biophysical Chemistry, Göttingen, GermanyMax Planck Institute of Molecular Cell Biology and Genetics, Dresden, GermanyInstitute of Molecular Biosciences, University of Graz, Graz, Austria; BioTechMed-Graz, Graz, Austria; Field of Excellence BioHealth - University of Graz, Graz, Austria; Max Planck Institute for Biophysical Chemistry, Göttingen, GermanyTriacylglycerol (TG) and steryl ester (SE) lipid storage is a universal strategy to maintain organismal energy and membrane homeostasis. Cycles of building and mobilizing storage fat are fundamental in (re)distributing lipid substrates between tissues or to progress ontogenetic transitions. In this study, we show that Hormone-sensitive lipase (Hsl) specifically controls SE mobilization to initiate intergenerational sterol transfer in Drosophila melanogaster. Tissue-autonomous Hsl functions in the maternal fat body and germline coordinately prevent adult SE overstorage and maximize sterol allocation to embryos. While Hsl-deficiency is largely dispensable for normal development on sterol-rich diets, animals depend on adipocyte Hsl for optimal fecundity when dietary sterol becomes limiting. Notably, accumulation of SE but not of TG is a characteristic of Hsl-deficient cells across phyla including murine white adipocytes. In summary, we identified Hsl as an ancestral regulator of SE degradation, which improves intergenerational sterol transfer and reproductive success in flies.https://elifesciences.org/articles/63252lipid metabolismsterolhormone-sensitive lipaseDrosophilafecundityadipocyte
spellingShingle Christoph Heier
Oskar Knittelfelder
Harald F Hofbauer
Wolfgang Mende
Ingrid Pörnbacher
Laura Schiller
Gabriele Schoiswohl
Hao Xie
Sebastian Grönke
Andrej Shevchenko
Ronald P Kühnlein
Hormone-sensitive lipase couples intergenerational sterol metabolism to reproductive success
eLife
lipid metabolism
sterol
hormone-sensitive lipase
Drosophila
fecundity
adipocyte
title Hormone-sensitive lipase couples intergenerational sterol metabolism to reproductive success
title_full Hormone-sensitive lipase couples intergenerational sterol metabolism to reproductive success
title_fullStr Hormone-sensitive lipase couples intergenerational sterol metabolism to reproductive success
title_full_unstemmed Hormone-sensitive lipase couples intergenerational sterol metabolism to reproductive success
title_short Hormone-sensitive lipase couples intergenerational sterol metabolism to reproductive success
title_sort hormone sensitive lipase couples intergenerational sterol metabolism to reproductive success
topic lipid metabolism
sterol
hormone-sensitive lipase
Drosophila
fecundity
adipocyte
url https://elifesciences.org/articles/63252
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