The impact of bed rest on human skeletal muscle metabolism

Insulin sensitivity and metabolic flexibility decrease in response to bed rest, but the temporal and causal adaptations in human skeletal muscle metabolism are not fully defined. Here, we use an integrative approach to assess human skeletal muscle metabolism during bed rest and provide a multi-syste...

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Published inCell reports. Medicine Vol. 5; no. 1; p. 101372
Main Authors Eggelbusch, Moritz, Charlton, Braeden T., Bosutti, Alessandra, Ganse, Bergita, Giakoumaki, Ifigenia, Grootemaat, Anita E., Hendrickse, Paul W., Jaspers, Yorrick, Kemp, Stephan, Kerkhoff, Tom J., Noort, Wendy, van Weeghel, Michel, van der Wel, Nicole N., Wesseling, Julia R., Frings-Meuthen, Petra, Rittweger, Jörn, Mulder, Edwin R., Jaspers, Richard T., Degens, Hans, Wüst, Rob C.I.
Format Journal Article
LanguageEnglish
Published United States Elsevier Inc 16.01.2024
Elsevier
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Online AccessGet full text
ISSN2666-3791
2666-3791
DOI10.1016/j.xcrm.2023.101372

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Abstract Insulin sensitivity and metabolic flexibility decrease in response to bed rest, but the temporal and causal adaptations in human skeletal muscle metabolism are not fully defined. Here, we use an integrative approach to assess human skeletal muscle metabolism during bed rest and provide a multi-system analysis of how skeletal muscle and the circulatory system adapt to short- and long-term bed rest (German Clinical Trials: DRKS00015677). We uncover that intracellular glycogen accumulation after short-term bed rest accompanies a rapid reduction in systemic insulin sensitivity and less GLUT4 localization at the muscle cell membrane, preventing further intracellular glycogen deposition after long-term bed rest. We provide evidence of a temporal link between the accumulation of intracellular triglycerides, lipotoxic ceramides, and sphingomyelins and an altered skeletal muscle mitochondrial structure and function after long-term bed rest. An intracellular nutrient overload therefore represents a crucial determinant for rapid skeletal muscle insulin insensitivity and mitochondrial alterations after prolonged bed rest. [Display omitted] •Muscle glycogen build-up in bed rest reduces insulin sensitivity and further storage•Muscle lipid overload, lipotoxicity, and inflammation develop during bed rest•Bed rest shifts muscle metabolism from fatty acid to glucose oxidation•Intrinsic mitochondrial alterations occur after long-term bed rest Eggelbusch et al. show that a bed rest-induced nutrient overload contributes to insulin insensitivity, lipotoxicity, and mitochondrial alterations in human skeletal muscle. During prolonged bed rest, rapid insulin insensitivity and a metabolic shift toward glucose oxidation minimize additional glycogen storage, while inherent mitochondrial alterations are linked to progressive lipid accumulation.
AbstractList Insulin sensitivity and metabolic flexibility decrease in response to bed rest, but the temporal and causal adaptations in human skeletal muscle metabolism are not fully defined. Here, we use an integrative approach to assess human skeletal muscle metabolism during bed rest and provide a multi-system analysis of how skeletal muscle and the circulatory system adapt to short- and long-term bed rest (German Clinical Trials: DRKS00015677). We uncover that intracellular glycogen accumulation after short-term bed rest accompanies a rapid reduction in systemic insulin sensitivity and less GLUT4 localization at the muscle cell membrane, preventing further intracellular glycogen deposition after long-term bed rest. We provide evidence of a temporal link between the accumulation of intracellular triglycerides, lipotoxic ceramides, and sphingomyelins and an altered skeletal muscle mitochondrial structure and function after long-term bed rest. An intracellular nutrient overload therefore represents a crucial determinant for rapid skeletal muscle insulin insensitivity and mitochondrial alterations after prolonged bed rest.Insulin sensitivity and metabolic flexibility decrease in response to bed rest, but the temporal and causal adaptations in human skeletal muscle metabolism are not fully defined. Here, we use an integrative approach to assess human skeletal muscle metabolism during bed rest and provide a multi-system analysis of how skeletal muscle and the circulatory system adapt to short- and long-term bed rest (German Clinical Trials: DRKS00015677). We uncover that intracellular glycogen accumulation after short-term bed rest accompanies a rapid reduction in systemic insulin sensitivity and less GLUT4 localization at the muscle cell membrane, preventing further intracellular glycogen deposition after long-term bed rest. We provide evidence of a temporal link between the accumulation of intracellular triglycerides, lipotoxic ceramides, and sphingomyelins and an altered skeletal muscle mitochondrial structure and function after long-term bed rest. An intracellular nutrient overload therefore represents a crucial determinant for rapid skeletal muscle insulin insensitivity and mitochondrial alterations after prolonged bed rest.
Insulin sensitivity and metabolic flexibility decrease in response to bed rest, but the temporal and causal adaptations in human skeletal muscle metabolism are not fully defined. Here, we use an integrative approach to assess human skeletal muscle metabolism during bed rest and provide a multi-system analysis of how skeletal muscle and the circulatory system adapt to short- and long-term bed rest (German Clinical Trials: DRKS00015677). We uncover that intracellular glycogen accumulation after short-term bed rest accompanies a rapid reduction in systemic insulin sensitivity and less GLUT4 localization at the muscle cell membrane, preventing further intracellular glycogen deposition after long-term bed rest. We provide evidence of a temporal link between the accumulation of intracellular triglycerides, lipotoxic ceramides, and sphingomyelins and an altered skeletal muscle mitochondrial structure and function after long-term bed rest. An intracellular nutrient overload therefore represents a crucial determinant for rapid skeletal muscle insulin insensitivity and mitochondrial alterations after prolonged bed rest.
Insulin sensitivity and metabolic flexibility decrease in response to bed rest, but the temporal and causal adaptations in human skeletal muscle metabolism are not fully defined. Here, we use an integrative approach to assess human skeletal muscle metabolism during bed rest and provide a multi-system analysis of how skeletal muscle and the circulatory system adapt to short- and long-term bed rest (German Clinical Trials: DRKS00015677). We uncover that intracellular glycogen accumulation after short-term bed rest accompanies a rapid reduction in systemic insulin sensitivity and less GLUT4 localization at the muscle cell membrane, preventing further intracellular glycogen deposition after long-term bed rest. We provide evidence of a temporal link between the accumulation of intracellular triglycerides, lipotoxic ceramides, and sphingomyelins and an altered skeletal muscle mitochondrial structure and function after long-term bed rest. An intracellular nutrient overload therefore represents a crucial determinant for rapid skeletal muscle insulin insensitivity and mitochondrial alterations after prolonged bed rest. •Muscle glycogen build-up in bed rest reduces insulin sensitivity and further storage•Muscle lipid overload, lipotoxicity, and inflammation develop during bed rest•Bed rest shifts muscle metabolism from fatty acid to glucose oxidation•Intrinsic mitochondrial alterations occur after long-term bed rest Eggelbusch et al. show that a bed rest-induced nutrient overload contributes to insulin insensitivity, lipotoxicity, and mitochondrial alterations in human skeletal muscle. During prolonged bed rest, rapid insulin insensitivity and a metabolic shift toward glucose oxidation minimize additional glycogen storage, while inherent mitochondrial alterations are linked to progressive lipid accumulation.
SummaryInsulin sensitivity and metabolic flexibility decrease in response to bed rest, but the temporal and causal adaptations in human skeletal muscle metabolism are not fully defined. Here, we use an integrative approach to assess human skeletal muscle metabolism during bed rest and provide a multi-system analysis of how skeletal muscle and the circulatory system adapt to short- and long-term bed rest (German Clinical Trials: DRKS00015677). We uncover that intracellular glycogen accumulation after short-term bed rest accompanies a rapid reduction in systemic insulin sensitivity and less GLUT4 localization at the muscle cell membrane, preventing further intracellular glycogen deposition after long-term bed rest. We provide evidence of a temporal link between the accumulation of intracellular triglycerides, lipotoxic ceramides, and sphingomyelins and an altered skeletal muscle mitochondrial structure and function after long-term bed rest. An intracellular nutrient overload therefore represents a crucial determinant for rapid skeletal muscle insulin insensitivity and mitochondrial alterations after prolonged bed rest.
Insulin sensitivity and metabolic flexibility decrease in response to bed rest, but the temporal and causal adaptations in human skeletal muscle metabolism are not fully defined. Here, we use an integrative approach to assess human skeletal muscle metabolism during bed rest and provide a multi-system analysis of how skeletal muscle and the circulatory system adapt to short- and long-term bed rest (German Clinical Trials: DRKS00015677). We uncover that intracellular glycogen accumulation after short-term bed rest accompanies a rapid reduction in systemic insulin sensitivity and less GLUT4 localization at the muscle cell membrane, preventing further intracellular glycogen deposition after long-term bed rest. We provide evidence of a temporal link between the accumulation of intracellular triglycerides, lipotoxic ceramides, and sphingomyelins and an altered skeletal muscle mitochondrial structure and function after long-term bed rest. An intracellular nutrient overload therefore represents a crucial determinant for rapid skeletal muscle insulin insensitivity and mitochondrial alterations after prolonged bed rest. [Display omitted] •Muscle glycogen build-up in bed rest reduces insulin sensitivity and further storage•Muscle lipid overload, lipotoxicity, and inflammation develop during bed rest•Bed rest shifts muscle metabolism from fatty acid to glucose oxidation•Intrinsic mitochondrial alterations occur after long-term bed rest Eggelbusch et al. show that a bed rest-induced nutrient overload contributes to insulin insensitivity, lipotoxicity, and mitochondrial alterations in human skeletal muscle. During prolonged bed rest, rapid insulin insensitivity and a metabolic shift toward glucose oxidation minimize additional glycogen storage, while inherent mitochondrial alterations are linked to progressive lipid accumulation.
ArticleNumber 101372
Author van der Wel, Nicole N.
Rittweger, Jörn
Ganse, Bergita
van Weeghel, Michel
Wüst, Rob C.I.
Bosutti, Alessandra
Wesseling, Julia R.
Kemp, Stephan
Degens, Hans
Frings-Meuthen, Petra
Grootemaat, Anita E.
Mulder, Edwin R.
Jaspers, Richard T.
Giakoumaki, Ifigenia
Kerkhoff, Tom J.
Charlton, Braeden T.
Jaspers, Yorrick
Hendrickse, Paul W.
Eggelbusch, Moritz
Noort, Wendy
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Issue 1
Keywords insulin sensitivity
bed rest
mitochondria
lipotoxicity
nutrient overload
metabolism
skeletal muscle
GLUT4
physical inactivity
Language English
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Snippet Insulin sensitivity and metabolic flexibility decrease in response to bed rest, but the temporal and causal adaptations in human skeletal muscle metabolism are...
SummaryInsulin sensitivity and metabolic flexibility decrease in response to bed rest, but the temporal and causal adaptations in human skeletal muscle...
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SubjectTerms Advanced Basic Science
bed rest
Bed Rest - adverse effects
Energy Metabolism - physiology
GLUT4
Glycogen - metabolism
Humans
Insulin Resistance - physiology
insulin sensitivity
lipotoxicity
metabolism
mitochondria
Muscle, Skeletal - metabolism
nutrient overload
physical inactivity
skeletal muscle
Title The impact of bed rest on human skeletal muscle metabolism
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https://www.proquest.com/docview/2916406953
https://pubmed.ncbi.nlm.nih.gov/PMC10829795
http://www.cell.com/article/S2666379123006018/pdf
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