Skeletal muscle in healthy humans exhibits a day-night rhythm in lipid metabolism

Held, Ntsiki M.; Wefers, Jakob; Weeghel, Michel van; Daemen, Sabine; Hansen, Janne Hedegaard; Vaz, Frédéric M.; Moorsel, Dirk van; Hesselink, Matthijs K. C.; Houtkooper, Riekelt H.; Schrauwen, Patrick

doi:10.1016/j.molmet.2020.100989

Cited by 35 publications

(45 citation statements)

References 36 publications

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“…Previously, an integrated omics method employing both LC-MS/MS and GC-MS using derivatizations was used on bacteria, urine, cell cultures, mouse tissue and plant leaves to detect 51 polar metabolites and 84 lipid species ( Nakayasu et al, 2016 ). Hence, we set out to develop a comprehensive omics protocol for C. elegans , combining our previously reported metabolomics and lipidomics methods into a unified extraction, a variation of the popular Folch or Bligh and Dyer liquid-liquid extraction (LLE) method ( Bligh and Dyer, 1959 ), and reliant exclusively on LC-MS for analysis ( Molenaars et al, 2020 ; Held et al, 2020 ).…”

Section: Introductionmentioning

confidence: 99%

Metabolomics and lipidomics in Caenorhabditis elegans using a single-sample preparation

Molenaars

Schomakers

Elfrink

et al. 2021

Disease Models &Amp; Mechanisms

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Comprehensive metabolomic and lipidomic mass spectrometry methods are in increasing demand, for instance in research related to nutrition and aging. The nematode C. elegans is a key model organism in these fields, due to the large repository of available C. elegans mutants and their convenient natural lifespan. Here, we describe a robust and sensitive analytical method for the semi-quantitative analysis of >100 polar (metabolomics) and >1000 apolar (lipidomics) metabolites in C. elegans, using a single sample preparation. Our method is capable of reliably detecting a wide variety of biologically relevant metabolic aberrations in, for instance, glycolysis and the TCA cycle, pyrimidine metabolism and complex lipid biosynthesis. In conclusion, we provide a powerful analytical tool that maximizes metabolic data yield from a single sample.

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Section: Introductionmentioning

confidence: 99%

Metabolomics and lipidomics in Caenorhabditis elegans using a single-sample preparation

Molenaars

Schomakers

Elfrink

et al. 2021

Disease Models &Amp; Mechanisms

Self Cite

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“…Many of these rhythmic genes are involved in metabolism, and therefore rhythmicity of metabolites might be a better readout to explore the effect of aging on circadian oscillations. Previously, we have shown that lipid metabolism in human muscle tissue exhibits day-night rhythmicity 16 . In the present study, we have compared the rhythmicity of the lipidome of WAT vs BAT.…”

Section: Introductionmentioning

confidence: 99%

Aging selectively dampens oscillation of lipid abundance in white and brown adipose tissue

Held

Buijink

Elfrink

et al. 2021

Sci Rep

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Lipid metabolism is under the control of the circadian system and circadian dysregulation has been linked to obesity and dyslipidemia. These factors and outcomes have also been associated to, or affected by, the process of aging. Here, we investigated whether murine white (WAT) and brown (BAT) adipose tissue lipids exhibit rhythmicity and if this is affected by aging. To this end, we have measured the 24 h lipid profiles of WAT and BAT using a global lipidomics analysis of > 1100 lipids. We observed rhythmicity in nearly all lipid classes including glycerolipids, glycerophospholipids, sterol lipids and sphingolipids. Overall, ~ 22% of the analyzed lipids were considered rhythmic in WAT and BAT. Despite a general accumulation of lipids upon aging the fraction of oscillating lipids decreased in both tissues to 14% and 18%, respectively. Diurnal profiles of lipids in BAT appeared to depend on the lipid acyl chain length and this specific regulation was lost in aged mice. Our study revealed how aging affects the rhythmicity of lipid metabolism and could contribute to the quest for targets that improve diurnal lipid homeostasis to maintain cardiometabolic health during aging.

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“…Concordantly, lipidomics analyses demonstrated that above 20% of the lipid species including phospholipids, sphingolipids, and diacylglycerols were circadian rhythmic [387,388]. Moreover, lipid droplet size and content showed diurnal rhythmicity in type 1 muscle fibers [388]. While highly informative and allowing to unravel important insights into the human rhythmic physiology, these approaches are also highly invasive for the participant due to serial tissue biopsies, have limited time resolution, and are not applicable to most human tissues.…”

Section: The Circadian Clock System and Human Diseasesmentioning

confidence: 99%

“…Similarly, transcriptomic studies of human skeletal muscle biopsies collected from healthy volunteers revealed that genes involved in glucose and lipid metabolism exhibited strongly rhythmic temporal profiles [386]. Concordantly, lipidomics analyses demonstrated that above 20% of the lipid species including phospholipids, sphingolipids, and diacylglycerols were circadian rhythmic [387,388]. Moreover, lipid droplet size and content showed diurnal rhythmicity in type 1 muscle fibers [388].…”

Section: The Circadian Clock System and Human Diseasesmentioning

confidence: 99%

Coupled network of the circadian clocks: a driving force of rhythmic physiology

2020

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The circadian system is composed of coupled endogenous oscillators that allow living beings, including humans, to anticipate and adapt to daily changes in their environment. In mammals, circadian clocks form a hierarchically organized network with a ‘master clock’ located in the suprachiasmatic nucleus of the hypothalamus, which ensures entrainment of subsidiary oscillators to environmental cycles. Robust rhythmicity of body clocks is indispensable for temporally coordinating organ functions, and the disruption or misalignment of circadian rhythms caused for instance by modern lifestyle is strongly associated with various widespread diseases. This review aims to provide a comprehensive overview of our current knowledge about the molecular architecture and system‐level organization of mammalian circadian oscillators. Furthermore, we discuss the regulatory roles of peripheral clocks for cell and organ physiology and their implication in the temporal coordination of metabolism in human health and disease. Finally, we summarize methods for assessing circadian rhythmicity in humans.

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Skeletal muscle in healthy humans exhibits a day-night rhythm in lipid metabolism

Cited by 35 publications

References 36 publications

Metabolomics and lipidomics in Caenorhabditis elegans using a single-sample preparation

Metabolomics and lipidomics in Caenorhabditis elegans using a single-sample preparation

Aging selectively dampens oscillation of lipid abundance in white and brown adipose tissue

Coupled network of the circadian clocks: a driving force of rhythmic physiology

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