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Research Article

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

Ursula Loizides-Mangold, Laurent Perrin, Bart Vandereycken, James A. Betts, Jean-Philippe Walhin, Iain Templeman, Stéphanie Chanon, Benjamin D. Weger, Christine Durand, Maud Robert, Jonathan Paz Montoya, Marc Moniatte, Leonidas G. Karagounis, Jonathan D. Johnston, View ORCID ProfileFrédéric Gachon, Etienne Lefai, Howard Riezman, and Charna Dibner
PNAS October 10, 2017 114 (41) E8565-E8574; first published September 25, 2017; https://doi.org/10.1073/pnas.1705821114
Ursula Loizides-Mangold
aDivision of Endocrinology, Diabetology, Hypertension and Nutrition, Department of Internal Medicine Specialties, University of Geneva, CH-1211 Geneva, Switzerland;
bDepartment of Cell Physiology and Metabolism, University of Geneva, CH-1211 Geneva, Switzerland;
cFaculty Diabetes Centre, Faculty of Medicine, University of Geneva, CH-1211 Geneva, Switzerland;
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Laurent Perrin
aDivision of Endocrinology, Diabetology, Hypertension and Nutrition, Department of Internal Medicine Specialties, University of Geneva, CH-1211 Geneva, Switzerland;
bDepartment of Cell Physiology and Metabolism, University of Geneva, CH-1211 Geneva, Switzerland;
cFaculty Diabetes Centre, Faculty of Medicine, University of Geneva, CH-1211 Geneva, Switzerland;
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Bart Vandereycken
dSection of Mathematics, University of Geneva, CH-1211 Geneva, Switzerland;
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James A. Betts
eDepartment for Health, University of Bath, Bath BA2 7AY, United Kingdom;
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Jean-Philippe Walhin
eDepartment for Health, University of Bath, Bath BA2 7AY, United Kingdom;
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Iain Templeman
eDepartment for Health, University of Bath, Bath BA2 7AY, United Kingdom;
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Stéphanie Chanon
fCarMeN Laboratory, INSERM U1060, INRA 1397, University Lyon 1, 69600 Oullins, France;
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Benjamin D. Weger
gDepartment of Diabetes and Circadian Rhythms, Nestlé Institute of Health Sciences, CH-1015 Lausanne, Switzerland;
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Christine Durand
fCarMeN Laboratory, INSERM U1060, INRA 1397, University Lyon 1, 69600 Oullins, France;
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Maud Robert
hDepartment of Digestive Surgery, Center of Bariatric Surgery, Edouard Herriot Hospital, 69003 Lyon, France;
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Jonathan Paz Montoya
iProteomics Core Facility, École Polytechnique Fédérale de Lausanne, CH-1015 Lausanne, Switzerland;
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Marc Moniatte
iProteomics Core Facility, École Polytechnique Fédérale de Lausanne, CH-1015 Lausanne, Switzerland;
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Leonidas G. Karagounis
jExperimental Myology and Integrative Biology Research Cluster, Faculty of Sport and Health Sciences, Plymouth Marjon University, Plymouth PL6 8BH, United Kingdom;
kInstitute of Nutritional Science, Nestlé Research Centre, CH-1015 Lausanne, Switzerland;
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Jonathan D. Johnston
lFaculty of Health and Medical Sciences, University of Surrey, Guildford, Surrey GU2 7XH, United Kingdom;
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Frédéric Gachon
gDepartment of Diabetes and Circadian Rhythms, Nestlé Institute of Health Sciences, CH-1015 Lausanne, Switzerland;
mSchool of Life Sciences, École Polytechnique Fédérale de Lausanne, CH-1015 Lausanne, Switzerland;
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  • ORCID record for Frédéric Gachon
Etienne Lefai
fCarMeN Laboratory, INSERM U1060, INRA 1397, University Lyon 1, 69600 Oullins, France;
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Howard Riezman
nDepartment of Biochemistry, University of Geneva, CH-1211 Geneva, Switzerland;
oNational Centre of Competence in Research Chemical Biology, University of Geneva, CH-1211 Geneva, Switzerland
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  • For correspondence: Howard.Riezman@unige.ch charna.dibner@hcuge.ch
Charna Dibner
aDivision of Endocrinology, Diabetology, Hypertension and Nutrition, Department of Internal Medicine Specialties, University of Geneva, CH-1211 Geneva, Switzerland;
bDepartment of Cell Physiology and Metabolism, University of Geneva, CH-1211 Geneva, Switzerland;
cFaculty Diabetes Centre, Faculty of Medicine, University of Geneva, CH-1211 Geneva, Switzerland;
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  • For correspondence: Howard.Riezman@unige.ch charna.dibner@hcuge.ch
  1. Edited by Joseph S. Takahashi, Howard Hughes Medical Institute, University of Texas Southwestern Medical Center, Dallas, TX, and approved August 31, 2017 (received for review April 10, 2017)

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Significance

Our experiments provide the analysis of lipid metabolite circadian oscillations in a cellular system synchronized in vitro, suggesting cell-autonomous diurnal changes in lipid profiles independent of feeding. Moreover, our work represents a comprehensive comparison between the lipid composition of human skeletal muscle derived from sedentary healthy adults, receiving hourly isocaloric solutions, and human primary skeletal myotubes cultured in vitro. A substantial number of lipid metabolites, in particular membrane lipids, exhibited oscillatory patterns in muscle tissue and in myotube cells, where they were blunted upon cell-autonomous clock disruption. As lipid oscillations in skeletal muscle membrane lipids may impact on insulin signaling and on the development of insulin resistance, studying the temporal lipid composition of human muscle is therefore of utmost importance.

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.

  • lipid metabolism
  • circadian clock
  • human skeletal muscle
  • human primary myotubes
  • lipidomics

Footnotes

  • ↵1To whom correspondence may be addressed. Email: Howard.Riezman{at}unige.ch or charna.dibner{at}hcuge.ch.
  • Author contributions: U.L.-M., J.A.B., J.D.J., F.G., E.L., H.R., and C. Dibner designed research; U.L.-M., L.P., J.-P.W., I.T., S.C., B.D.W., C. Durand, M.R., and J.P.M. performed research; J.P.M., M.M., and L.G.K. contributed new reagents/analytic tools; U.L.-M. and B.V. analyzed data; and U.L.-M. wrote the paper.

  • Conflict of interest statement: B.D.W. and F.G. are employees of Nestlé Institute of Health Sciences SA; L.G.K. is an employee of Nestec Ltd. J.A.B. has been a consultant for PepsiCo (Quaker) and Kellogg’s. The other authors have no conflict of interest to declare.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1705821114/-/DCSupplemental.

Freely available online through the PNAS open access option.

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Circadian lipidomics in human skeletal muscle
Ursula Loizides-Mangold, Laurent Perrin, Bart Vandereycken, James A. Betts, Jean-Philippe Walhin, Iain Templeman, Stéphanie Chanon, Benjamin D. Weger, Christine Durand, Maud Robert, Jonathan Paz Montoya, Marc Moniatte, Leonidas G. Karagounis, Jonathan D. Johnston, Frédéric Gachon, Etienne Lefai, Howard Riezman, Charna Dibner
Proceedings of the National Academy of Sciences Oct 2017, 114 (41) E8565-E8574; DOI: 10.1073/pnas.1705821114

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Circadian lipidomics in human skeletal muscle
Ursula Loizides-Mangold, Laurent Perrin, Bart Vandereycken, James A. Betts, Jean-Philippe Walhin, Iain Templeman, Stéphanie Chanon, Benjamin D. Weger, Christine Durand, Maud Robert, Jonathan Paz Montoya, Marc Moniatte, Leonidas G. Karagounis, Jonathan D. Johnston, Frédéric Gachon, Etienne Lefai, Howard Riezman, Charna Dibner
Proceedings of the National Academy of Sciences Oct 2017, 114 (41) E8565-E8574; DOI: 10.1073/pnas.1705821114
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