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 in | Cell reports. Medicine Vol. 5; no. 1; p. 101372 |
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Main Authors | , , , , , , , , , , , , , , , , , , , |
Format | Journal Article |
Language | English |
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United States
Elsevier Inc
16.01.2024
Elsevier |
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Online Access | Get full text |
ISSN | 2666-3791 2666-3791 |
DOI | 10.1016/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. |
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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 |
Author_xml | – sequence: 1 givenname: Moritz surname: Eggelbusch fullname: Eggelbusch, Moritz organization: Department of Human Movement Sciences, Faculty of Behavioural and Movement Sciences, Vrije Universiteit Amsterdam, Amsterdam Movement Sciences, Amsterdam, the Netherlands – sequence: 2 givenname: Braeden T. surname: Charlton fullname: Charlton, Braeden T. organization: Department of Human Movement Sciences, Faculty of Behavioural and Movement Sciences, Vrije Universiteit Amsterdam, Amsterdam Movement Sciences, Amsterdam, the Netherlands – sequence: 3 givenname: Alessandra surname: Bosutti fullname: Bosutti, Alessandra organization: Department of Life Sciences, University of Trieste, Trieste, Italy – sequence: 4 givenname: Bergita surname: Ganse fullname: Ganse, Bergita organization: Research Centre for Musculoskeletal Science and Sports Medicine, Faculty of Science and Engineering, Manchester Metropolitan University, Manchester, UK – sequence: 5 givenname: Ifigenia surname: Giakoumaki fullname: Giakoumaki, Ifigenia organization: Research Centre for Musculoskeletal Science and Sports Medicine, Faculty of Science and Engineering, Manchester Metropolitan University, Manchester, UK – sequence: 6 givenname: Anita E. surname: Grootemaat fullname: Grootemaat, Anita E. organization: Electron Microscopy Center Amsterdam, Department of Medical Biology, Amsterdam University Medical Centers, Amsterdam, the Netherlands – sequence: 7 givenname: Paul W. surname: Hendrickse fullname: Hendrickse, Paul W. organization: Research Centre for Musculoskeletal Science and Sports Medicine, Faculty of Science and Engineering, Manchester Metropolitan University, Manchester, UK – sequence: 8 givenname: Yorrick surname: Jaspers fullname: Jaspers, Yorrick organization: Laboratory Genetic Metabolic Diseases, Amsterdam University Medical Centers, Amsterdam, the Netherlands – sequence: 9 givenname: Stephan surname: Kemp fullname: Kemp, Stephan organization: Laboratory Genetic Metabolic Diseases, Amsterdam University Medical Centers, Amsterdam, the Netherlands – sequence: 10 givenname: Tom J. surname: Kerkhoff fullname: Kerkhoff, Tom J. organization: Department of Human Movement Sciences, Faculty of Behavioural and Movement Sciences, Vrije Universiteit Amsterdam, Amsterdam Movement Sciences, Amsterdam, the Netherlands – sequence: 11 givenname: Wendy surname: Noort fullname: Noort, Wendy organization: Department of Human Movement Sciences, Faculty of Behavioural and Movement Sciences, Vrije Universiteit Amsterdam, Amsterdam Movement Sciences, Amsterdam, the Netherlands – sequence: 12 givenname: Michel surname: van Weeghel fullname: van Weeghel, Michel organization: Laboratory Genetic Metabolic Diseases, Amsterdam University Medical Centers, Amsterdam, the Netherlands – sequence: 13 givenname: Nicole N. surname: van der Wel fullname: van der Wel, Nicole N. organization: Electron Microscopy Center Amsterdam, Department of Medical Biology, Amsterdam University Medical Centers, Amsterdam, the Netherlands – sequence: 14 givenname: Julia R. surname: Wesseling fullname: Wesseling, Julia R. organization: Department of Human Movement Sciences, Faculty of Behavioural and Movement Sciences, Vrije Universiteit Amsterdam, Amsterdam Movement Sciences, Amsterdam, the Netherlands – sequence: 15 givenname: Petra surname: Frings-Meuthen fullname: Frings-Meuthen, Petra organization: Institute of Aerospace Medicine, German Aerospace Center (DLR), Cologne, Germany – sequence: 16 givenname: Jörn surname: Rittweger fullname: Rittweger, Jörn organization: Institute of Aerospace Medicine, German Aerospace Center (DLR), Cologne, Germany – sequence: 17 givenname: Edwin R. surname: Mulder fullname: Mulder, Edwin R. organization: Institute of Aerospace Medicine, German Aerospace Center (DLR), Cologne, Germany – sequence: 18 givenname: Richard T. surname: Jaspers fullname: Jaspers, Richard T. organization: Department of Human Movement Sciences, Faculty of Behavioural and Movement Sciences, Vrije Universiteit Amsterdam, Amsterdam Movement Sciences, Amsterdam, the Netherlands – sequence: 19 givenname: Hans surname: Degens fullname: Degens, Hans organization: Research Centre for Musculoskeletal Science and Sports Medicine, Faculty of Science and Engineering, Manchester Metropolitan University, Manchester, UK – sequence: 20 givenname: Rob C.I. orcidid: 0000-0003-3781-5177 surname: Wüst fullname: Wüst, Rob C.I. email: r.wust@vu.nl organization: Department of Human Movement Sciences, Faculty of Behavioural and Movement Sciences, Vrije Universiteit Amsterdam, Amsterdam Movement Sciences, Amsterdam, the Netherlands |
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Keywords | insulin sensitivity bed rest mitochondria lipotoxicity nutrient overload metabolism skeletal muscle GLUT4 physical inactivity |
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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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