Lipidomics reveals diurnal lipid oscillations in human skeletal muscle persisting in cellular myotubes cultured in vitro

Ursula Lozides-Mangold, Laurent Perrin, Bart Vandereycken, James Betts, Jean-Philippe Walhin, Iain Templeman, Stephanie Chanon, Benjamin Weger, Christine Durand, Maud Robert, Jonathan Paz, Marc Moniatte, Leonidas Karagounis, Howard Riezman, Charna Dibner

Research output: Contribution to journalArticle

17 Citations (Scopus)

Abstract

Circadian clocks play an important role in lipid homeostasis, with impact on various metabolic diseases. Due to the central role of skeletal muscle in whole-body metabolism, we aimed at studying muscle lipid profiles in a temporal manner. Moreover, it has not been shown whether lipid oscillations in peripheral tissues are driven by diurnal cycles of rest–activity and food intake or are able to persist in vitro in a cell-autonomous manner. To address this, we investigated lipid profiles over 24 h in human skeletal muscle in vivo and in primary human myotubes cultured in vitro. Glycerolipids, glycerophospholipids, and sphingolipids exhibited diurnal oscillations, suggesting a widespread circadian impact on muscle lipid metabolism. Notably, peak levels of lipid accumulation were in phase coherence with core clock gene expression in vivo and in vitro. The percentage of oscillating lipid metabolites was comparable between muscle tissue and cultured myotubes, and temporal lipid profiles correlated with transcript profiles of genes implicated in their biosynthesis. Lipids enriched in the outer leaflet of the plasma membrane oscillated in a highly coordinated manner in vivo and in vitro. Lipid metabolite oscillations were strongly attenuated upon siRNA-mediated clock disruption in human primary myotubes. Taken together, our data suggest an essential role for endogenous cell-autonomous human skeletal muscle oscillators in regulating lipid metabolism independent of external synchronizers, such as physical activity or food intake.

LanguageEnglish
PagesE8565-E8574
JournalProceedings of the National Academy of Sciences of the United States of America
Volume114
Issue number41
Early online date25 Sep 2017
DOIs
StatusPublished - 10 Oct 2017

Fingerprint

Skeletal Muscle Fibers
Skeletal Muscle
Lipids
Lipid Metabolism
Muscles
Eating
Glycerophospholipids
Activity Cycles
In Vitro Techniques
Circadian Clocks
Sphingolipids
Metabolic Diseases
Small Interfering RNA
Homeostasis
Cell Membrane
Gene Expression

Cite this

Lipidomics reveals diurnal lipid oscillations in human skeletal muscle persisting in cellular myotubes cultured in vitro. / Lozides-Mangold, Ursula; Perrin, Laurent; Vandereycken, Bart; Betts, James; Walhin, Jean-Philippe; Templeman, Iain; Chanon, Stephanie; Weger, Benjamin; Durand, Christine; Robert, Maud; Paz, Jonathan; Moniatte, Marc; Karagounis, Leonidas; Riezman, Howard; Dibner, Charna.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 114, No. 41, 10.10.2017, p. E8565-E8574.

Research output: Contribution to journalArticle

Lozides-Mangold, U, Perrin, L, Vandereycken, B, Betts, J, Walhin, J-P, Templeman, I, Chanon, S, Weger, B, Durand, C, Robert, M, Paz, J, Moniatte, M, Karagounis, L, Riezman, H & Dibner, C 2017, 'Lipidomics reveals diurnal lipid oscillations in human skeletal muscle persisting in cellular myotubes cultured in vitro', Proceedings of the National Academy of Sciences of the United States of America, vol. 114, no. 41, pp. E8565-E8574. https://doi.org/10.1073/pnas.1705821114
Lozides-Mangold, Ursula ; Perrin, Laurent ; Vandereycken, Bart ; Betts, James ; Walhin, Jean-Philippe ; Templeman, Iain ; Chanon, Stephanie ; Weger, Benjamin ; Durand, Christine ; Robert, Maud ; Paz, Jonathan ; Moniatte, Marc ; Karagounis, Leonidas ; Riezman, Howard ; Dibner, Charna. / Lipidomics reveals diurnal lipid oscillations in human skeletal muscle persisting in cellular myotubes cultured in vitro. In: Proceedings of the National Academy of Sciences of the United States of America. 2017 ; Vol. 114, No. 41. pp. E8565-E8574.
@article{abc3561607734471b824ee208b261d4f,
title = "Lipidomics reveals diurnal lipid oscillations in human skeletal muscle persisting in cellular myotubes cultured in vitro",
abstract = "Circadian clocks play an important role in lipid homeostasis, with impact on various metabolic diseases. Due to the central role of skeletal muscle in whole-body metabolism, we aimed at studying muscle lipid profiles in a temporal manner. Moreover, it has not been shown whether lipid oscillations in peripheral tissues are driven by diurnal cycles of rest–activity and food intake or are able to persist in vitro in a cell-autonomous manner. To address this, we investigated lipid profiles over 24 h in human skeletal muscle in vivo and in primary human myotubes cultured in vitro. Glycerolipids, glycerophospholipids, and sphingolipids exhibited diurnal oscillations, suggesting a widespread circadian impact on muscle lipid metabolism. Notably, peak levels of lipid accumulation were in phase coherence with core clock gene expression in vivo and in vitro. The percentage of oscillating lipid metabolites was comparable between muscle tissue and cultured myotubes, and temporal lipid profiles correlated with transcript profiles of genes implicated in their biosynthesis. Lipids enriched in the outer leaflet of the plasma membrane oscillated in a highly coordinated manner in vivo and in vitro. Lipid metabolite oscillations were strongly attenuated upon siRNA-mediated clock disruption in human primary myotubes. Taken together, our data suggest an essential role for endogenous cell-autonomous human skeletal muscle oscillators in regulating lipid metabolism independent of external synchronizers, such as physical activity or food intake.",
author = "Ursula Lozides-Mangold and Laurent Perrin and Bart Vandereycken and James Betts and Jean-Philippe Walhin and Iain Templeman and Stephanie Chanon and Benjamin Weger and Christine Durand and Maud Robert and Jonathan Paz and Marc Moniatte and Leonidas Karagounis and Howard Riezman and Charna Dibner",
year = "2017",
month = "10",
day = "10",
doi = "10.1073/pnas.1705821114",
language = "English",
volume = "114",
pages = "E8565--E8574",
journal = "Proceedings of the National Academy of Sciences of the United States of America",
issn = "0027-8424",
publisher = "National Academy of Sciences",
number = "41",

}

TY - JOUR

T1 - Lipidomics reveals diurnal lipid oscillations in human skeletal muscle persisting in cellular myotubes cultured in vitro

AU - Lozides-Mangold, Ursula

AU - Perrin, Laurent

AU - Vandereycken, Bart

AU - Betts, James

AU - Walhin, Jean-Philippe

AU - Templeman, Iain

AU - Chanon, Stephanie

AU - Weger, Benjamin

AU - Durand, Christine

AU - Robert, Maud

AU - Paz, Jonathan

AU - Moniatte, Marc

AU - Karagounis, Leonidas

AU - Riezman, Howard

AU - Dibner, Charna

PY - 2017/10/10

Y1 - 2017/10/10

N2 - Circadian clocks play an important role in lipid homeostasis, with impact on various metabolic diseases. Due to the central role of skeletal muscle in whole-body metabolism, we aimed at studying muscle lipid profiles in a temporal manner. Moreover, it has not been shown whether lipid oscillations in peripheral tissues are driven by diurnal cycles of rest–activity and food intake or are able to persist in vitro in a cell-autonomous manner. To address this, we investigated lipid profiles over 24 h in human skeletal muscle in vivo and in primary human myotubes cultured in vitro. Glycerolipids, glycerophospholipids, and sphingolipids exhibited diurnal oscillations, suggesting a widespread circadian impact on muscle lipid metabolism. Notably, peak levels of lipid accumulation were in phase coherence with core clock gene expression in vivo and in vitro. The percentage of oscillating lipid metabolites was comparable between muscle tissue and cultured myotubes, and temporal lipid profiles correlated with transcript profiles of genes implicated in their biosynthesis. Lipids enriched in the outer leaflet of the plasma membrane oscillated in a highly coordinated manner in vivo and in vitro. Lipid metabolite oscillations were strongly attenuated upon siRNA-mediated clock disruption in human primary myotubes. Taken together, our data suggest an essential role for endogenous cell-autonomous human skeletal muscle oscillators in regulating lipid metabolism independent of external synchronizers, such as physical activity or food intake.

AB - Circadian clocks play an important role in lipid homeostasis, with impact on various metabolic diseases. Due to the central role of skeletal muscle in whole-body metabolism, we aimed at studying muscle lipid profiles in a temporal manner. Moreover, it has not been shown whether lipid oscillations in peripheral tissues are driven by diurnal cycles of rest–activity and food intake or are able to persist in vitro in a cell-autonomous manner. To address this, we investigated lipid profiles over 24 h in human skeletal muscle in vivo and in primary human myotubes cultured in vitro. Glycerolipids, glycerophospholipids, and sphingolipids exhibited diurnal oscillations, suggesting a widespread circadian impact on muscle lipid metabolism. Notably, peak levels of lipid accumulation were in phase coherence with core clock gene expression in vivo and in vitro. The percentage of oscillating lipid metabolites was comparable between muscle tissue and cultured myotubes, and temporal lipid profiles correlated with transcript profiles of genes implicated in their biosynthesis. Lipids enriched in the outer leaflet of the plasma membrane oscillated in a highly coordinated manner in vivo and in vitro. Lipid metabolite oscillations were strongly attenuated upon siRNA-mediated clock disruption in human primary myotubes. Taken together, our data suggest an essential role for endogenous cell-autonomous human skeletal muscle oscillators in regulating lipid metabolism independent of external synchronizers, such as physical activity or food intake.

UR - http://doi.org/10.1073/pnas.1705821114

U2 - 10.1073/pnas.1705821114

DO - 10.1073/pnas.1705821114

M3 - Article

VL - 114

SP - E8565-E8574

JO - Proceedings of the National Academy of Sciences of the United States of America

T2 - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

SN - 0027-8424

IS - 41

ER -