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Lipidomics reveals diurnal lipid oscillations in human skeletal muscle persisting in cellular myotubes cultured in vitro.
Proc Natl Acad Sci U S A. 2017 10 10; 114(41):E8565-E8574.PN

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.

Authors+Show Affiliations

Division of Endocrinology, Diabetology, Hypertension and Nutrition, Department of Internal Medicine Specialties, University of Geneva, CH-1211 Geneva, Switzerland. Department of Cell Physiology and Metabolism, University of Geneva, CH-1211 Geneva, Switzerland. Faculty Diabetes Centre, Faculty of Medicine, University of Geneva, CH-1211 Geneva, Switzerland.Division of Endocrinology, Diabetology, Hypertension and Nutrition, Department of Internal Medicine Specialties, University of Geneva, CH-1211 Geneva, Switzerland. Department of Cell Physiology and Metabolism, University of Geneva, CH-1211 Geneva, Switzerland. Faculty Diabetes Centre, Faculty of Medicine, University of Geneva, CH-1211 Geneva, Switzerland.Section of Mathematics, University of Geneva, CH-1211 Geneva, Switzerland.Department for Health, University of Bath, Bath BA2 7AY, United Kingdom.Department for Health, University of Bath, Bath BA2 7AY, United Kingdom.Department for Health, University of Bath, Bath BA2 7AY, United Kingdom.CarMeN Laboratory, INSERM U1060, INRA 1397, University Lyon 1, 69600 Oullins, France.Department of Diabetes and Circadian Rhythms, Nestlé Institute of Health Sciences, CH-1015 Lausanne, Switzerland.CarMeN Laboratory, INSERM U1060, INRA 1397, University Lyon 1, 69600 Oullins, France.Department of Digestive Surgery, Center of Bariatric Surgery, Edouard Herriot Hospital, 69003 Lyon, France.Proteomics Core Facility, École Polytechnique Fédérale de Lausanne, CH-1015 Lausanne, Switzerland.Proteomics Core Facility, École Polytechnique Fédérale de Lausanne, CH-1015 Lausanne, Switzerland.Experimental Myology and Integrative Biology Research Cluster, Faculty of Sport and Health Sciences, Plymouth Marjon University, Plymouth PL6 8BH, United Kingdom. Institute of Nutritional Science, Nestlé Research Centre, CH-1015 Lausanne, Switzerland.Faculty of Health and Medical Sciences, University of Surrey, Guildford, Surrey GU2 7XH, United Kingdom.Department of Diabetes and Circadian Rhythms, Nestlé Institute of Health Sciences, CH-1015 Lausanne, Switzerland. School of Life Sciences, École Polytechnique Fédérale de Lausanne, CH-1015 Lausanne, Switzerland.CarMeN Laboratory, INSERM U1060, INRA 1397, University Lyon 1, 69600 Oullins, France.Department of Biochemistry, University of Geneva, CH-1211 Geneva, Switzerland; Howard.Riezman@unige.ch charna.dibner@hcuge.ch. National Centre of Competence in Research Chemical Biology, University of Geneva, CH-1211 Geneva, Switzerland.Division of Endocrinology, Diabetology, Hypertension and Nutrition, Department of Internal Medicine Specialties, University of Geneva, CH-1211 Geneva, Switzerland; Howard.Riezman@unige.ch charna.dibner@hcuge.ch. Department of Cell Physiology and Metabolism, University of Geneva, CH-1211 Geneva, Switzerland. Faculty Diabetes Centre, Faculty of Medicine, University of Geneva, CH-1211 Geneva, Switzerland.

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't

Language

eng

PubMed ID

28973848

Citation

Loizides-Mangold, Ursula, et al. "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, 2017, pp. E8565-E8574.
Loizides-Mangold U, Perrin L, Vandereycken B, et al. Lipidomics reveals diurnal lipid oscillations in human skeletal muscle persisting in cellular myotubes cultured in vitro. Proc Natl Acad Sci USA. 2017;114(41):E8565-E8574.
Loizides-Mangold, U., Perrin, L., Vandereycken, B., Betts, J. A., Walhin, J. P., Templeman, I., Chanon, S., Weger, B. D., Durand, C., Robert, M., Paz Montoya, J., Moniatte, M., Karagounis, L. G., Johnston, J. D., Gachon, F., Lefai, E., 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
Loizides-Mangold U, et al. Lipidomics Reveals Diurnal Lipid Oscillations in Human Skeletal Muscle Persisting in Cellular Myotubes Cultured in Vitro. Proc Natl Acad Sci USA. 2017 10 10;114(41):E8565-E8574. PubMed PMID: 28973848.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Lipidomics reveals diurnal lipid oscillations in human skeletal muscle persisting in cellular myotubes cultured in vitro. AU - Loizides-Mangold,Ursula, AU - Perrin,Laurent, AU - Vandereycken,Bart, AU - Betts,James A, AU - Walhin,Jean-Philippe, AU - Templeman,Iain, AU - Chanon,Stéphanie, AU - Weger,Benjamin D, AU - Durand,Christine, AU - Robert,Maud, AU - Paz Montoya,Jonathan, AU - Moniatte,Marc, AU - Karagounis,Leonidas G, AU - Johnston,Jonathan D, AU - Gachon,Frédéric, AU - Lefai,Etienne, AU - Riezman,Howard, AU - Dibner,Charna, Y1 - 2017/09/25/ PY - 2017/10/5/pubmed PY - 2018/6/27/medline PY - 2017/10/5/entrez KW - circadian clock KW - human primary myotubes KW - human skeletal muscle KW - lipid metabolism KW - lipidomics SP - E8565 EP - E8574 JF - Proceedings of the National Academy of Sciences of the United States of America JO - Proc. Natl. Acad. Sci. U.S.A. VL - 114 IS - 41 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. SN - 1091-6490 UR - https://www.unboundmedicine.com/medline/citation/28973848/Lipidomics_reveals_diurnal_lipid_oscillations_in_human_skeletal_muscle_persisting_in_cellular_myotubes_cultured_in_vitro_ L2 - http://www.pnas.org/cgi/pmidlookup?view=long&pmid=28973848 DB - PRIME DP - Unbound Medicine ER -