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

30 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.

Original languageEnglish
Pages (from-to)E8565-E8574
Number of pages10
JournalProceedings of the National Academy of Sciences of the United States of America
Volume114
Issue number41
Early online date25 Sep 2017
DOIs
Publication statusPublished - 10 Oct 2017

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    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, 114(41), E8565-E8574. https://doi.org/10.1073/pnas.1705821114