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

Loizides-Mangold, Ursula
; 
Perrin, Laurent
; 
Vandereycken, Bart
; 
Betts, James A.
; 
Walhin, Jean-Philippe
; 
Templeman, Iain
; 
Chanon, Stéphanie
; 
Weger, Benjamin D.
; 
Durand, Christine
; 
Robert, Maud
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Author
Loizides-Mangold, Ursula
Perrin, Laurent
Vandereycken, Bart
Betts, James A.
Walhin, Jean-Philippe
Templeman, Iain
Chanon, Stéphanie
Weger, Benjamin D.
Durand, Christine
Robert, Maud
Montoya, Jonathan Paz
Moniatte, Marc
Karagounis, Leonidas G.
Johnston, Jonathan D.
Gachon, Frédéric
Lefai, Etienne
Riezman, Howard
Dibner, Charna
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.
Keywords
lipid metabolism, circadian clock, human skeletal muscle, human primary myotubes, lipidomics
Date
2017
Type
Journal article
Journal
Proceedings of the National Academy of Sciences of USA
Book
Volume
114
Issue
41
Page Range
8565-8574
Article Number
ACU Department
Mary MacKillop Institute for Health Research
Faculty of Health Sciences
Collections
Mary MacKillop Institute for Health Research
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URI
https://hdl.handle.net/20.500.14802/24095
Relation URI
DOI
10.1073/pnas.1705821114
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Open Access Status
Open access
License
All rights reserved
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Controlled
Notes
Bronze open access. © 2017 National Academy of Sciences. Freely available online through the PNAS open access option.