TY - JOUR
T1 - Circadian misalignment disturbs the skeletal muscle lipidome in healthy young men
AU - Harmsen, Jan-Frieder
AU - van Polanen, Nynke
AU - van Weeghel, Michel
AU - Wefers, Jakob
AU - Hoeks, Joris
AU - Vaz, Frédéric M.
AU - Pras-Raves, Mia L.
AU - van Kampen, Antoine H. C.
AU - Schaart, Gert
AU - van Moorsel, Dirk
AU - Hansen, Jan
AU - Hesselink, Matthijs K. C.
AU - Houtkooper, Riekelt H.
AU - Schrauwen, Patrick
N1 - Funding Information:
We acknowledge the support from the Netherlands Cardiovascular Research Initiative: an initiative with the support of the Dutch Heart Foundation (CVON2014‐02 ENERGISE); this work is partly financed by the Netherlands Organization for Scientific Research (TOP 40‐00812‐98‐14047 to PS); J. Hansen is supported by the School of Nutrition and Translational Research in Metabolism (NUTRIM) Netherlands Organization for Scientific Research (NWO) Graduate Programme, which is financially supported by Netherlands Organization for Scientific Research Grant 022.003.011; work in the Houtkooper group is financially supported by a VIDI grant from ZonMw (no. 91715305). The remaining authors declare no conflicts of interest.
Publisher Copyright:
© 2021 The Authors. The FASEB Journal published by Wiley Periodicals LLC on behalf of Federation of American Societies for Experimental Biology
Copyright:
Copyright 2021 Elsevier B.V., All rights reserved.
PY - 2021/6/1
Y1 - 2021/6/1
N2 - Circadian misalignment, as seen in shift work, is associated with an increased risk to develop type 2 diabetes. In an experimental setting, we recently showed that a rapid day-night shift for 3 consecutive nights leads to misalignment of the core molecular clock, induction of the PPAR pathway, and insulin resistance in skeletal muscle of young, healthy men. Here, we investigated if circadian misalignment affects the skeletal muscle lipidome and intramyocellular lipid droplet characteristics, explaining the misalignment-induced insulin resistance. Fourteen healthy men underwent one aligned and one circadian misalignment period, both consisting of ~3.5 days. In the misaligned condition, day and night were rapidly shifted by 12 hours leading to opposite eating, sleep, and activity times compared with the aligned condition. For each condition, two muscle biopsies were taken from the m. vastus lateralis in the morning and evening and subjected to semi-targeted lipidomics and confocal microscopy analysis. We found that only 2% of detected lipids were different between morning and evening in the aligned condition, whereas 12% displayed a morning-evening difference upon misalignment. Triacylglycerols, in particular species of a carbon length ≥55, were the most abundant lipid species changed upon misalignment. Cardiolipins were decreased upon misalignment, whereas phosphatidylcholines consistently followed the same morning-evening pattern, suggesting regulation by the circadian clock. Cholesteryl esters adjusted to the shifted behavior. Lipid droplet characteristics remained unaltered upon misalignment. Together, these findings show that simulated shift work disturbs the skeletal muscle lipidome, which may contribute to misalignment-induced insulin resistance.
AB - Circadian misalignment, as seen in shift work, is associated with an increased risk to develop type 2 diabetes. In an experimental setting, we recently showed that a rapid day-night shift for 3 consecutive nights leads to misalignment of the core molecular clock, induction of the PPAR pathway, and insulin resistance in skeletal muscle of young, healthy men. Here, we investigated if circadian misalignment affects the skeletal muscle lipidome and intramyocellular lipid droplet characteristics, explaining the misalignment-induced insulin resistance. Fourteen healthy men underwent one aligned and one circadian misalignment period, both consisting of ~3.5 days. In the misaligned condition, day and night were rapidly shifted by 12 hours leading to opposite eating, sleep, and activity times compared with the aligned condition. For each condition, two muscle biopsies were taken from the m. vastus lateralis in the morning and evening and subjected to semi-targeted lipidomics and confocal microscopy analysis. We found that only 2% of detected lipids were different between morning and evening in the aligned condition, whereas 12% displayed a morning-evening difference upon misalignment. Triacylglycerols, in particular species of a carbon length ≥55, were the most abundant lipid species changed upon misalignment. Cardiolipins were decreased upon misalignment, whereas phosphatidylcholines consistently followed the same morning-evening pattern, suggesting regulation by the circadian clock. Cholesteryl esters adjusted to the shifted behavior. Lipid droplet characteristics remained unaltered upon misalignment. Together, these findings show that simulated shift work disturbs the skeletal muscle lipidome, which may contribute to misalignment-induced insulin resistance.
KW - circadian clock
KW - human skeletal muscle
KW - insulin resistance
KW - lipid droplet
KW - lipidomics
KW - shift work
UR - https://www.scopus.com/pages/publications/85105768542
U2 - 10.1096/fj.202100143R
DO - 10.1096/fj.202100143R
M3 - Article
C2 - 33977623
SN - 0892-6638
VL - 35
SP - e21611
JO - FASEB journal
JF - FASEB journal
IS - 6
M1 - e21611
ER -