Higher Mitochondrial Respiration and Uncoupling with Reduced Electron Transport Chain Content in Vivo in Muscle of Sedentary Versus Active Subjects
Objective:This study investigated the disparity between muscle metabolic rate and mitochondrial metabolism in human muscle of sedentary vs. active individuals.Research Design and Methods:Chronic activity level was characterized by a physical activity questionnaire and a triaxial accelerometer as wel...
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| Published in | The journal of clinical endocrinology and metabolism Vol. 98; no. 1; pp. 129 - 136 |
|---|---|
| Main Authors | , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
Bethesda, MD
Oxford University Press
01.01.2013
Copyright by The Endocrine Society Endocrine Society |
| Subjects | |
| Online Access | Get full text |
| ISSN | 0021-972X 1945-7197 1945-7197 |
| DOI | 10.1210/jc.2012-2967 |
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| Abstract | Objective:This study investigated the disparity between muscle metabolic rate and mitochondrial metabolism in human muscle of sedentary vs. active individuals.Research Design and Methods:Chronic activity level was characterized by a physical activity questionnaire and a triaxial accelerometer as well as a maximal oxygen uptake test. The ATP and O2 fluxes and mitochondrial coupling (ATP/O2 or P/O) in resting muscle as well as mitochondrial capacity (ATPmax) were determined in vivo in human vastus lateralis muscle using magnetic resonance and optical spectroscopy on 24 sedentary and seven active subjects. Muscle biopsies were analyzed for electron transport chain content (using complex III as a representative marker) and mitochondrial proteins associated with antioxidant protection.Results:Sedentary muscle had lower electron transport chain complex content (65% of the active group) in proportion to the reduction in ATPmax (0.69 ± 0.07 vs. 1.07 ± 0.06 mm sec−1) as compared with active subjects. This lower ATPmax paired with an unchanged O2 flux in resting muscle between groups resulted in a doubling of O2 flux per ATPmax (3.3 ± 0.3 vs. 1.7 ± 0.2 μm O2 per mm ATP) that reflected mitochondrial uncoupling (P/O = 1.41 ± 0.1 vs. 2.1 ± 0.3) and greater UCP3/complex III (6.0 ± 0.7 vs. 3.8 ± 0.3) in sedentary vs. active subjects.Conclusion:A smaller mitochondrial pool serving the same O2 flux resulted in elevated mitochondrial respiration in sedentary muscle. In addition, uncoupling contributed to this higher mitochondrial respiration. This finding resolves the paradox of stable muscle metabolism but greater mitochondrial respiration in muscle of inactive vs. active subjects. |
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| AbstractList | OBJECTIVE:This study investigated the disparity between muscle metabolic rate and mitochondrial metabolism in human muscle of sedentary vs. active individuals.
RESEARCH DESIGN AND METHODS:Chronic activity level was characterized by a physical activity questionnaire and a triaxial accelerometer as well as a maximal oxygen uptake test. The ATP and O2 fluxes and mitochondrial coupling (ATP/O2 or P/O) in resting muscle as well as mitochondrial capacity (ATPmax) were determined in vivo in human vastus lateralis muscle using magnetic resonance and optical spectroscopy on 24 sedentary and seven active subjects. Muscle biopsies were analyzed for electron transport chain content (using complex III as a representative marker) and mitochondrial proteins associated with antioxidant protection.
RESULTS:Sedentary muscle had lower electron transport chain complex content (65% of the active group) in proportion to the reduction in ATPmax (0.69 ± 0.07 vs. 1.07 ± 0.06 mM sec) as compared with active subjects. This lower ATPmax paired with an unchanged O2 flux in resting muscle between groups resulted in a doubling of O2 flux per ATPmax (3.3 ± 0.3 vs. 1.7 ± 0.2 μM O2 per mM ATP) that reflected mitochondrial uncoupling (P/O = 1.41 ± 0.1 vs. 2.1 ± 0.3) and greater UCP3/complex III (6.0 ± 0.7 vs. 3.8 ± 0.3) in sedentary vs. active subjects.
CONCLUSION:A smaller mitochondrial pool serving the same O2 flux resulted in elevated mitochondrial respiration in sedentary muscle. In addition, uncoupling contributed to this higher mitochondrial respiration. This finding resolves the paradox of stable muscle metabolism but greater mitochondrial respiration in muscle of inactive vs. active subjects. Objective:This study investigated the disparity between muscle metabolic rate and mitochondrial metabolism in human muscle of sedentary vs. active individuals.Research Design and Methods:Chronic activity level was characterized by a physical activity questionnaire and a triaxial accelerometer as well as a maximal oxygen uptake test. The ATP and O2 fluxes and mitochondrial coupling (ATP/O2 or P/O) in resting muscle as well as mitochondrial capacity (ATPmax) were determined in vivo in human vastus lateralis muscle using magnetic resonance and optical spectroscopy on 24 sedentary and seven active subjects. Muscle biopsies were analyzed for electron transport chain content (using complex III as a representative marker) and mitochondrial proteins associated with antioxidant protection.Results:Sedentary muscle had lower electron transport chain complex content (65% of the active group) in proportion to the reduction in ATPmax (0.69 ± 0.07 vs. 1.07 ± 0.06 mm sec−1) as compared with active subjects. This lower ATPmax paired with an unchanged O2 flux in resting muscle between groups resulted in a doubling of O2 flux per ATPmax (3.3 ± 0.3 vs. 1.7 ± 0.2 μm O2 per mm ATP) that reflected mitochondrial uncoupling (P/O = 1.41 ± 0.1 vs. 2.1 ± 0.3) and greater UCP3/complex III (6.0 ± 0.7 vs. 3.8 ± 0.3) in sedentary vs. active subjects.Conclusion:A smaller mitochondrial pool serving the same O2 flux resulted in elevated mitochondrial respiration in sedentary muscle. In addition, uncoupling contributed to this higher mitochondrial respiration. This finding resolves the paradox of stable muscle metabolism but greater mitochondrial respiration in muscle of inactive vs. active subjects. This study investigated the disparity between muscle metabolic rate and mitochondrial metabolism in human muscle of sedentary vs. active individuals. Chronic activity level was characterized by a physical activity questionnaire and a triaxial accelerometer as well as a maximal oxygen uptake test. The ATP and O(2) fluxes and mitochondrial coupling (ATP/O(2) or P/O) in resting muscle as well as mitochondrial capacity (ATP(max)) were determined in vivo in human vastus lateralis muscle using magnetic resonance and optical spectroscopy on 24 sedentary and seven active subjects. Muscle biopsies were analyzed for electron transport chain content (using complex III as a representative marker) and mitochondrial proteins associated with antioxidant protection. Sedentary muscle had lower electron transport chain complex content (65% of the active group) in proportion to the reduction in ATP(max) (0.69 ± 0.07 vs. 1.07 ± 0.06 mM sec(-1)) as compared with active subjects. This lower ATP(max) paired with an unchanged O(2) flux in resting muscle between groups resulted in a doubling of O(2) flux per ATP(max) (3.3 ± 0.3 vs. 1.7 ± 0.2 μM O(2) per mM ATP) that reflected mitochondrial uncoupling (P/O = 1.41 ± 0.1 vs. 2.1 ± 0.3) and greater UCP3/complex III (6.0 ± 0.7 vs. 3.8 ± 0.3) in sedentary vs. active subjects. A smaller mitochondrial pool serving the same O(2) flux resulted in elevated mitochondrial respiration in sedentary muscle. In addition, uncoupling contributed to this higher mitochondrial respiration. This finding resolves the paradox of stable muscle metabolism but greater mitochondrial respiration in muscle of inactive vs. active subjects. This study investigated the disparity between muscle metabolic rate and mitochondrial metabolism in human muscle of sedentary vs. active individuals.OBJECTIVEThis study investigated the disparity between muscle metabolic rate and mitochondrial metabolism in human muscle of sedentary vs. active individuals.Chronic activity level was characterized by a physical activity questionnaire and a triaxial accelerometer as well as a maximal oxygen uptake test. The ATP and O(2) fluxes and mitochondrial coupling (ATP/O(2) or P/O) in resting muscle as well as mitochondrial capacity (ATP(max)) were determined in vivo in human vastus lateralis muscle using magnetic resonance and optical spectroscopy on 24 sedentary and seven active subjects. Muscle biopsies were analyzed for electron transport chain content (using complex III as a representative marker) and mitochondrial proteins associated with antioxidant protection.RESEARCH DESIGN AND METHODSChronic activity level was characterized by a physical activity questionnaire and a triaxial accelerometer as well as a maximal oxygen uptake test. The ATP and O(2) fluxes and mitochondrial coupling (ATP/O(2) or P/O) in resting muscle as well as mitochondrial capacity (ATP(max)) were determined in vivo in human vastus lateralis muscle using magnetic resonance and optical spectroscopy on 24 sedentary and seven active subjects. Muscle biopsies were analyzed for electron transport chain content (using complex III as a representative marker) and mitochondrial proteins associated with antioxidant protection.Sedentary muscle had lower electron transport chain complex content (65% of the active group) in proportion to the reduction in ATP(max) (0.69 ± 0.07 vs. 1.07 ± 0.06 mM sec(-1)) as compared with active subjects. This lower ATP(max) paired with an unchanged O(2) flux in resting muscle between groups resulted in a doubling of O(2) flux per ATP(max) (3.3 ± 0.3 vs. 1.7 ± 0.2 μM O(2) per mM ATP) that reflected mitochondrial uncoupling (P/O = 1.41 ± 0.1 vs. 2.1 ± 0.3) and greater UCP3/complex III (6.0 ± 0.7 vs. 3.8 ± 0.3) in sedentary vs. active subjects.RESULTSSedentary muscle had lower electron transport chain complex content (65% of the active group) in proportion to the reduction in ATP(max) (0.69 ± 0.07 vs. 1.07 ± 0.06 mM sec(-1)) as compared with active subjects. This lower ATP(max) paired with an unchanged O(2) flux in resting muscle between groups resulted in a doubling of O(2) flux per ATP(max) (3.3 ± 0.3 vs. 1.7 ± 0.2 μM O(2) per mM ATP) that reflected mitochondrial uncoupling (P/O = 1.41 ± 0.1 vs. 2.1 ± 0.3) and greater UCP3/complex III (6.0 ± 0.7 vs. 3.8 ± 0.3) in sedentary vs. active subjects.A smaller mitochondrial pool serving the same O(2) flux resulted in elevated mitochondrial respiration in sedentary muscle. In addition, uncoupling contributed to this higher mitochondrial respiration. This finding resolves the paradox of stable muscle metabolism but greater mitochondrial respiration in muscle of inactive vs. active subjects.CONCLUSIONA smaller mitochondrial pool serving the same O(2) flux resulted in elevated mitochondrial respiration in sedentary muscle. In addition, uncoupling contributed to this higher mitochondrial respiration. This finding resolves the paradox of stable muscle metabolism but greater mitochondrial respiration in muscle of inactive vs. active subjects. |
| Author | Arakaki, Lori Amara, Catherine E. Bajpeyi, Sudip Conley, Kevin E. Costford, Sheila R. Jubrias, Sharon A. Smith, Steven R. Murray, Kori Marcinek, David J. |
| AuthorAffiliation | Department of Molecular Endocrinology (S.B., S.R.C., K.M., S.R.S.), Pennington Biomedical Research Center, Louisiana State University System, Baton Rouge, Louisiana 70808; and Departments of Radiology (K.E.C., C.E.A., S.A.J., D.J.M.), Physiology and Biophysics (K.E.C.), Bioengineering (K.E.C., D.J.M.), and Pediatrics (L.A.), University of Washington Medical Center, Seattle, Washington 98195 |
| AuthorAffiliation_xml | – name: Department of Molecular Endocrinology (S.B., S.R.C., K.M., S.R.S.), Pennington Biomedical Research Center, Louisiana State University System, Baton Rouge, Louisiana 70808; and Departments of Radiology (K.E.C., C.E.A., S.A.J., D.J.M.), Physiology and Biophysics (K.E.C.), Bioengineering (K.E.C., D.J.M.), and Pediatrics (L.A.), University of Washington Medical Center, Seattle, Washington 98195 |
| Author_xml | – sequence: 1 givenname: Kevin E. surname: Conley fullname: Conley, Kevin E. email: kconley@uw.edu organization: 2 Departments of Radiology (K.E.C., C.E.A., S.A.J., D.J.M.), Seattle, Washington 98195 – sequence: 2 givenname: Catherine E. surname: Amara fullname: Amara, Catherine E. organization: 2 Departments of Radiology (K.E.C., C.E.A., S.A.J., D.J.M.), Seattle, Washington 98195 – sequence: 3 givenname: Sudip surname: Bajpeyi fullname: Bajpeyi, Sudip organization: 1Department of Molecular Endocrinology (S.B., S.R.C., K.M., S.R.S.), Pennington Biomedical Research Center, Louisiana State University System, Baton Rouge, Louisiana 70808 – sequence: 4 givenname: Sheila R. surname: Costford fullname: Costford, Sheila R. organization: 1Department of Molecular Endocrinology (S.B., S.R.C., K.M., S.R.S.), Pennington Biomedical Research Center, Louisiana State University System, Baton Rouge, Louisiana 70808 – sequence: 5 givenname: Kori surname: Murray fullname: Murray, Kori organization: 1Department of Molecular Endocrinology (S.B., S.R.C., K.M., S.R.S.), Pennington Biomedical Research Center, Louisiana State University System, Baton Rouge, Louisiana 70808 – sequence: 6 givenname: Sharon A. surname: Jubrias fullname: Jubrias, Sharon A. organization: 2 Departments of Radiology (K.E.C., C.E.A., S.A.J., D.J.M.), Seattle, Washington 98195 – sequence: 7 givenname: Lori surname: Arakaki fullname: Arakaki, Lori organization: 5Pediatrics (L.A.), University of Washington Medical Center, Seattle, Washington 98195 – sequence: 8 givenname: David J. surname: Marcinek fullname: Marcinek, David J. organization: 2 Departments of Radiology (K.E.C., C.E.A., S.A.J., D.J.M.), Seattle, Washington 98195 – sequence: 9 givenname: Steven R. surname: Smith fullname: Smith, Steven R. organization: 1Department of Molecular Endocrinology (S.B., S.R.C., K.M., S.R.S.), Pennington Biomedical Research Center, Louisiana State University System, Baton Rouge, Louisiana 70808 |
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| Keywords | Human Obesity Nutrition Nutrition disorder Metabolic diseases In vivo Mitochondria Reduction Content Muscle Respiration Sedentary Transport Endocrinology Nutritional status Comparative study |
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| Snippet | Objective:This study investigated the disparity between muscle metabolic rate and mitochondrial metabolism in human muscle of sedentary vs. active... OBJECTIVE:This study investigated the disparity between muscle metabolic rate and mitochondrial metabolism in human muscle of sedentary vs. active individuals.... This study investigated the disparity between muscle metabolic rate and mitochondrial metabolism in human muscle of sedentary vs. active individuals. Chronic... This study investigated the disparity between muscle metabolic rate and mitochondrial metabolism in human muscle of sedentary vs. active... |
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| SubjectTerms | Accelerometry - methods Adult Biological and medical sciences Biopsy Cell Respiration Electron Transport - physiology Electron transport chain Electron Transport Chain Complex Proteins - metabolism Electron Transport Chain Complex Proteins - physiology Endocrine Care Endocrinopathies Energy Metabolism - physiology Feeding. Feeding behavior Fundamental and applied biological sciences. Psychology Humans Male Medical sciences Metabolic rate Metabolism Mitochondria Mitochondria, Muscle - metabolism Motor Activity - physiology Muscle, Skeletal - metabolism Oxygen Consumption - physiology Physical activity Protein transport Respiration Rest Sedentary Lifestyle Spectroscopy Surveys and Questionnaires Up-Regulation Vertebrates: anatomy and physiology, studies on body, several organs or systems Vertebrates: endocrinology Young Adult |
| Title | Higher Mitochondrial Respiration and Uncoupling with Reduced Electron Transport Chain Content in Vivo in Muscle of Sedentary Versus Active Subjects |
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