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

Journal article

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 and Dibner, Charna. (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 USA. 114(41), pp. 8565-8574. https://doi.org/10.1073/pnas.1705821114
AuthorsLoizides-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 and 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.

Keywordslipid metabolism; circadian clock; human skeletal muscle; human primary myotubes; lipidomics
Year2017
JournalProceedings of the National Academy of Sciences of USA
Journal citation114 (41), pp. 8565-8574
PublisherNational Academy of Sciences
ISSN0027-8424
Digital Object Identifier (DOI)https://doi.org/10.1073/pnas.1705821114
PubMed ID28973848
Scopus EID2-s2.0-85030779910
PubMed Central IDPMC5642690
Open accessOpen access
Page range8565-8574
FunderSwiss National Science Foundation (SNSF)
National Centre of Competence in Research Chemical Biology
Fondation Romande pour la Recherche sur le Diabète
Fondation Ernst et Lucie Schmidheiny
Société Académique de Genève
Biotechnology and Biological Sciences Research Council
Publisher's version
License
All rights reserved
File Access Level
Controlled
Publication process dates
Deposited16 Apr 2025
Grant IDCRSII3-154405
31003A-166700
310030B_166686
BB/I008470/1
Additional information

Bronze open access.

© 2017 National Academy of Sciences.

Freely available online through the PNAS open access option.

Permalink -

https://acuresearchbank.acu.edu.au/item/91q1y/lipidomics-reveals-diurnal-lipid-oscillations-in-human-skeletal-muscle-persisting-in-cellular-myotubes-cultured-in-vitro

Log in to edit

Restricted files

Publisher's version

  • 3
    total views
  • 0
    total downloads
  • 3
    views this month
  • 0
    downloads this month
These values are for the period from 19th October 2020, when this repository was created.

Export as

Related outputs

Defining the traditional mediterranean lifestyle : joint international consensus statement
Sidossis, Labros S, Lawson, Rob, Aprilakis, Emmanuel, Barata, Bernardo C., Baska, Alicja, Beneka, Anastasia, Bird, Robert, Birrell, Fraser, Chatzinikola, Charistoula, Chondronikola, Maria, Chrousos, George P, Conduit, Russell, Constantinou, Constantina, Karagounis, Leonidas, de Courten, Barbora, Cvejic, Jelena Helene, Davis, Andrew M, Demetriou, Christiana A., Errington, Linda, ... Itsiopoulos, Catherine. (2024). Defining the traditional mediterranean lifestyle : joint international consensus statement. Lifestyle Medicine. 5(4), pp. 1-13. https://doi.org/10.1002/lim2.115
Mapping of dietary interventions beneficial in the prevention of secondary health conditions in spinal cord injured population : A systematic review
Stojic, S., Eriks-Hoogland, I., Gamba, M., Valido, E., Minder, B., Chatelan, A., Karagounis, L. G., Ballesteros, M., Díaz, C., Brach, M., Stoyanov, J., Diviani, N., Rubinelli, S., Perret, C. and Glisic, Marija. (2023). Mapping of dietary interventions beneficial in the prevention of secondary health conditions in spinal cord injured population : A systematic review. Journal of Nutrition, Health and Aging. 27(7), pp. 524-541. https://doi.org/10.1007/s12603-023-1937-6
Skeletal muscle myostatin mRNA expression is upregulated in aged human adults with excess adiposity but is not associated with insulin resistance and ageing
Wilhelmsen, Andrew, Stephens, F, Bennett, Andrew J., Karagounis, Leonidas, Jones, Simon W. and Tsintzas, Kostas. (2023). Skeletal muscle myostatin mRNA expression is upregulated in aged human adults with excess adiposity but is not associated with insulin resistance and ageing. GeroScience. 46(2), pp. 2033-2049. https://doi.org/10.1007/s11357-023-00956-6
A meta-analysis comparing the effectiveness of alternate day fasting, the 5:2 diet, and time-restricted eating for weight loss
Elortegui Pascual, Paloma, Rolands, Maryann R., Eldridge, Alison L., Kassis, Amira, Mainardi, Fabio, Lê, Kim-Anne, Karagounis, Leonidas G., Gut, Philipp and Varady, Krista A.. (2023). A meta-analysis comparing the effectiveness of alternate day fasting, the 5:2 diet, and time-restricted eating for weight loss. Obesity. 31(Supp. 1), pp. 9-21. https://doi.org/10.1002/oby.23568
A randomized controlled clinical trial in healthy older adults to determine efficacy of glycine and n-acetylcysteine supplementation on glutathione redox status and oxidative damage
Lizzo, Giulia, Migliavacca, Eugenia, Lamers, Daniela, Frézal, Adrien, Corthesy, John, Vinyes-Parès, Gerard, Bosco, Nabil, Karagounis, Leonidas, Hövelmann, Ulrike, Heise, Tim, Von Eynatten, Maximilian and Gut, Philipp. (2022). A randomized controlled clinical trial in healthy older adults to determine efficacy of glycine and n-acetylcysteine supplementation on glutathione redox status and oxidative damage. Frontiers in Aging. 3, p. Article 852569. https://doi.org/10.3389/fragi.2022.852569
Impact of moderate dietary protein restriction on glucose homeostasis in a model of estrogen deficiency
Fournier, Carole, Karagounis, Leonidas G., Sacco, Sandra M., Horcajada, Marie-Noelle, Decaens, Thomas, Offord, Elizabeth A., Bouzakri, Karim and Ammann, Patrick. (2022). Impact of moderate dietary protein restriction on glucose homeostasis in a model of estrogen deficiency. Journal of Nutritional Biochemistry. 102, p. Article 108952. https://doi.org/10.1016/j.jnutbio.2022.108952
A randomized controlled trial to isolate the effects of fasting and energy restriction on weight loss and metabolic health in lean adults
Templeman, Iain, Smith, Harry Alex, Chowdhury, Enhad, Chen, Yung-Chih, Carroll, Harriet, Johnson-Bonson, Drusus, Hengist, Aaron, Smith, Rowan, Creighton, Jade, Clayton, David, Varley, Ian, Karagounis, Leonidas Georgios, Wilhelmsen, Andrew, Tsintzas, Kostas, Reeves, Sue, Walhin, Jean-Philippe, Gonzalez, Javier T., Thompson, Dylan and Betts, James A.. (2021). A randomized controlled trial to isolate the effects of fasting and energy restriction on weight loss and metabolic health in lean adults. Science Translational Medicine. 13(598), pp. 1-12. https://doi.org/10.1126/scitranslmed.abd8034
Low-grade systemic inflammation interferes with anabolic and catabolic characteristics of the aged human skeletal muscle
Draganidis, Dimitrios, Jamurtas, Athanasios Z., Chondrogianni, Niki, Mastorakos, Georgios, Jung, Tobias, Grune, Tilman, Papadopoulos, Constantinos, Papanikolaou, Konstantinos, Papassotiriou, Ioannis, Papaevgeniou, Nikoletta, Poulios, Athanasios, Batrakoulis, Alexios, Deli, Chariklia K., Georgakouli, Kalliopi, Chatzinikolaou, Athanasios, Karagounis, Leonidas G. and Fatouros, Ioannis G.. (2021). Low-grade systemic inflammation interferes with anabolic and catabolic characteristics of the aged human skeletal muscle. Oxidative Medicine and Cellular Longevity. 2021, p. Article 8376915. https://doi.org/10.1155/2021/8376915
Unacylated ghrelin, leptin, and appetite display diurnal rhythmicity in lean Adults
Templeman, Iain, Smith, Harry A., Walhin, Jean-Philippe, Middleton, Benita, Gonzalez, Javier T., Karagounis, Leonidas G., Johnston, Jonathan D. and Betts, James A.. (2021). Unacylated ghrelin, leptin, and appetite display diurnal rhythmicity in lean Adults. Journal of Applied Physiology. 130(5), pp. 1534-1543. https://doi.org/10.1152/japplphysiol.00920.2020
Systemic and metabolic signature of sarcopenia in community-dwelling older adults
Lu, Yanxia, Karagounis, Leonidas G., Ng, Tze Pin, Carre, Christophe, Narang, Vipin, Wong, Glenn, Tan, Crystal Tze Ying, Nyunt, Ma Shwe Zin, Gao, Qi, Abel, Brian, Poidinger, Michael, Fulop, Tamas, Bosco, Nabil and Larbi, Anis. (2020). Systemic and metabolic signature of sarcopenia in community-dwelling older adults. Journals of Gerontology: Series A Biological Sciences and Medical Sciences. 75(2), pp. 309-317. https://doi.org/10.1093/gerona/glz001
The importance of dietary protein at breakfast in childhood
Karagounis, Leonidas. (2019). The importance of dietary protein at breakfast in childhood. In In Nicklas, Theresa A., Nicklaus, Sophie and Henry, Christiani J. (Ed.). Nurturing a Healthy Generation of Children: Research Gaps and Opportunities : 91st Nestlé Nutrition Institute Workshop, Manila, March 2018 pp. 143 - 151 Karger. https://doi.org/10.1159/000493706
Chronotype : Implications for Epidemiologic Studies on Chrono-Nutrition and Cardiometabolic Health
Almoosawi, Suzana, Vingeliene, Snieguole, Gachon, Frédéric, Voortman, Trudy, Palla, Luigi, Johnston, Jonathan D., Van Dam, Rob, Darimont, Christian and Karagounis, Leonidas. (2019). Chronotype : Implications for Epidemiologic Studies on Chrono-Nutrition and Cardiometabolic Health. Advances in Nutrition. 10(1), pp. 30-42. https://doi.org/10.1093/advances/nmy070
Ingestion of a pre-bedtime protein containing beverage prevents overnight induced negative whole body protein balance in healthy middle-aged men : A randomized trial
Karagounis, Leonidas G., Beaumont, Maurice, Donato-Capel, Laurence, Godin, Jean-Philippe, Kapp, Anne-France, Draganidis, Dimitrios, Pinaud, Stéphane, Vuichoud, Jacques, Shevlyakova, Maya, Rade-Kukic, Koraljka and Breuillé, Denis. (2019). Ingestion of a pre-bedtime protein containing beverage prevents overnight induced negative whole body protein balance in healthy middle-aged men : A randomized trial. Frontiers in Nutrition. 6, p. Article 181. https://doi.org/10.3389/fnut.2019.00181
Longitudinal association of dietary protein intake in infancy and adiposity throughout childhood
Jen, Vincent, Braun, Kim V. E., Karagounis, Leonidas G., Nguyen, Anh N., Jaddoe, Vincent W. V., Schoufour, Josje D., Franco, Oscar H. and Voortman, Trudy. (2019). Longitudinal association of dietary protein intake in infancy and adiposity throughout childhood. Clinical Nutrition. 38(3), pp. 1296-1302. https://doi.org/10.1016/j.clnu.2018.05.013
Transcriptomic analyses reveal rhythmic and CLOCK-driven pathways in human skeletal muscle
Perrin, Laurent, Loizides-Mangold, Ursula, Chanon, Stéphanie, Gobet, Cédric, Hulo, Nicolas, Isenegger, Laura, Weger, Benjamin D., Migliavacca, Eugenia, Charpagne, Aline, Betts, James A., Walhin, Jean-Philippe, Templeman, Iain, Stokes, Keith A., Karagounis, Leonidas, Thompson, Dylan, Tsintzas, Kostas, Robert, Maud, Howald, Cedric, Riezman, Howard, ... Dibner, Charna. (2018). Transcriptomic analyses reveal rhythmic and CLOCK-driven pathways in human skeletal muscle. eLife. 7, pp. 1-30. https://doi.org/10.7554/eLife.34114
Intermittent fasting, energy balance and associated health outcomes in adults : Study protocol for a randomised controlled trial
Templeman, Iain, Thompson, Dylan, Gonzalez, Javier T., Walhin, Jean-Philippe, Reeves, Sue, Rogers, Phoebe, Brunstrom, Jeffrey M., Karagounis, Leonidas, Tsintzas, Kostas and Betts, James A.. (2018). Intermittent fasting, energy balance and associated health outcomes in adults : Study protocol for a randomised controlled trial. Trials. 19(1), pp. 1-11. https://doi.org/10.1186/s13063-018-2451-8
Post-game high protein intake may improve recovery of football-specific performance during a congested game fixture : Results from the PRO-FOOTBALL study
Poulios, Athanasios, Fatouros, Ioannis G., Mohr, Magni, Draganidis, Dimitrios, Deli, Chariklia K., Papanikolaou, Konstantinos, Sovatzidis, Apostolos, Nakopoulou, Theofano, Ermidis, Georgios, Tzatzakis, Theofanis, Laschou, Vasiliki C., Georgakouli, Kalliopi, Koulouris, Agisilaos, Tsimeas, Panagiotis, Chatzinikolaou, Athanasios, Karagounis, Leonidas G., Batsilas, Dimitrios, Krustrup, Peter and Jamurtas, Athanasios Z.. (2018). Post-game high protein intake may improve recovery of football-specific performance during a congested game fixture : Results from the PRO-FOOTBALL study. Nutrients. 10(4), p. Article 494. https://doi.org/10.3390/nu10040494
Dietary protein intake in school-age children and detailed measures of body composition : The Generation R Study
Jen, Vincent, Karagounis, Leonidas G., Jaddoe, Vincent W. V., Franco, Oscar H. and Voortman, Trudy. (2018). Dietary protein intake in school-age children and detailed measures of body composition : The Generation R Study. International Journal of Obesity. 42(10), pp. 1715-1723. https://doi.org/10.1038/s41366-018-0098-x
Disparate habitual physical activity and dietary intake profiles of elderly men with low and elevated systemic inflammation
Draganidis, Dimitrios, Jamurtas, A, Stampoulis, Theodoros, Laschou, Vasiliki C., Deli, Chariklia K., Georgakouli, Kalliopi, Papanikolaou, Konstantinos, Chatzinikolaou, A, Michalopoulou, Maria, Papadopoulos, Constantinos, Tsimeas, Panagiotis, Chondrogianni, Niki, Koutedakis, Yiannis, Karagounis, Leonidas and Fatouros, i. (2018). Disparate habitual physical activity and dietary intake profiles of elderly men with low and elevated systemic inflammation. Nutrients. 10(5), p. Article 566. https://doi.org/10.3390/nu10050566
Protein intake at breakfast promotes a positive whole-body protein balance in a dose-response manner in healthy children : A randomized trial
Karagounis, Leonidas G., Volterman, Kimberly A., Breuillé, Denis, Offord, Elizabeth A., Emady-Azar, Shahram and Moore, Daniel R.. (2018). Protein intake at breakfast promotes a positive whole-body protein balance in a dose-response manner in healthy children : A randomized trial. The Journal of Nutrition. 148(5), pp. 729-737. https://doi.org/10.1093/jn/nxy026
Protein and energy intakes are skewed toward the evening among children and adolescents in the United States : NHANES 2013-2014
Mathias, Kevin C., Almoosawi, Suzana and Karagounis, Leonidas G.. (2017). Protein and energy intakes are skewed toward the evening among children and adolescents in the United States : NHANES 2013-2014. The Journal of Nutrition. 147(6), pp. 1160-1166. https://doi.org/10.3945/jn.116.245621
Timing and pattern of postexercise protein ingestion affects whole-body protein balance in healthy children : A randomized trial
Volterman, Kimberly A., Moore, Daniel R., Breithaupt, Peter, Grathwohl, Dominik, Offord, Elizabeth A., Karagounis, Leonidas G. and Timmons, Brian W.. (2017). Timing and pattern of postexercise protein ingestion affects whole-body protein balance in healthy children : A randomized trial. Applied Physiology, Nutrition and Metabolism. 42(11), pp. 1142-1148. https://doi.org/10.1139/apnm-2017-0185
Protein ingestion preserves proteasome activity during intense aseptic inflammation and facilitates skeletal muscle recovery in humans
Draganidis, Dimitrios, Chondrogianni, Niki, Chatzinikolaou, Athanasios, Terzis, Gerasimos, Karagounis, Leonidas G., Sovatzidis, Apostolos, Avloniti, Alexandra, Lefaki, Maria, Protopapa, Maria, Deli, Chariklia K., Papanikolaou, Konstantinos, Jamurtas, Athanasios Z. and Fatouros, Ioannis G.. (2017). Protein ingestion preserves proteasome activity during intense aseptic inflammation and facilitates skeletal muscle recovery in humans. British Journal of Nutrition. 118(3), pp. 189-200. https://doi.org/10.1017/S0007114517001829
Screen-based sedentary behavior and associations with functional strength in 6–15 year-old children in the United States
Edelson, Lisa R., Mathias, Kevin C., Fulgoni, Victor L. and Karagounis, Leonidas G.. (2016). Screen-based sedentary behavior and associations with functional strength in 6–15 year-old children in the United States. BMC Public Health. 16(1), p. Article 116. https://doi.org/10.1186/s12889-016-2791-9
Amino acid composition of breast milk from urban Chinese mothers
Garcia-Rodenas, Clara L., Affolter, Michael, Vinyes-Parès, Gerard, De Castro, Carlos A., Karagounis, Leonidas G., Zhang, Yumei, Wang, Peiyu and Thakkar, Sagar K.. (2016). Amino acid composition of breast milk from urban Chinese mothers. Nutrients. 8(10), p. Article 606. https://doi.org/10.3390/nu8100606
Inflammaging and skeletal muscle : Can protein intake make a difference?
Draganidis, Dimitrios, Karagounis, Leonidas G., Athanailidis, Ioannis, Chatzinikolaou, Athanasios, Jamurtas, Athanasios Z. and Fatouros, Ioannis G.. (2016). Inflammaging and skeletal muscle : Can protein intake make a difference? The Journal of Nutrition. 146(10), pp. 1940-1952. https://doi.org/10.3945/jn.116.230912