Mitochondrial respiratory capacity and coupling control decline with age in human skeletal muscle
Mitochondrial health is critical to physiological function, particularly in tissues with high ATP turnover, such as striated muscle. It has been postulated that derangements in skeletal muscle mitochondrial function contribute to impaired physical function in older adults. Here, we determined mitoch...
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| Published in | American journal of physiology: endocrinology and metabolism Vol. 309; no. 3; pp. E224 - E232 |
|---|---|
| Main Authors | , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
American Physiological Society
01.08.2015
|
| Series | Endocrine and Metabolic Dysfunction during Aging and Senescence |
| Subjects | |
| Online Access | Get full text |
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| Abstract | Mitochondrial health is critical to physiological function, particularly in tissues with high ATP turnover, such as striated muscle. It has been postulated that derangements in skeletal muscle mitochondrial function contribute to impaired physical function in older adults. Here, we determined mitochondrial respiratory capacity and coupling control in skeletal muscle biopsies obtained from young and older adults. Twenty-four young (28 ± 7 yr) and thirty-one older (62 ± 8 yr) adults were studied. Mitochondrial respiration was determined in permeabilized myofibers from the vastus lateralis after the addition of substrates oligomycin and CCCP. Thereafter, mitochondrial coupling control was calculated. Maximal coupled respiration (respiration linked to ATP production) was lower in muscle from older vs. young subjects ( P < 0.01), as was maximal uncoupled respiration ( P = 0.06). Coupling control in response to the ATP synthase inhibitor oligomycin was lower in older adults ( P < 0.05), as was the mitochondria flux control ratio, coupled respiration normalized to maximal uncoupled respiration ( P < 0.05). Calculation of respiratory function revealed lower respiration linked to ATP production ( P < 0.001) and greater reserve respiration ( P < 0.01); i.e., respiratory capacity not used for phosphorylation in muscle from older adults. We conclude that skeletal muscle mitochondrial respiratory capacity and coupling control decline with age. Lower respiratory capacity and coupling efficiency result in a reduced capacity for ATP production in skeletal muscle of older adults. |
|---|---|
| AbstractList | Mitochondrial health is critical to physiological function, particularly in tissues with high ATP turnover, such as striated muscle. It has been postulated that derangements in skeletal muscle mitochondrial function contribute to impaired physical function in older adults. Here, we determined mitochondrial respiratory capacity and coupling control in skeletal muscle biopsies obtained from young and older adults. Twenty-four young (28 ± 7 yr) and thirty-one older (62 ± 8 yr) adults were studied. Mitochondrial respiration was determined in permeabilized myofibers from the vastus lateralis after the addition of substrates oligomycin and CCCP. Thereafter, mitochondrial coupling control was calculated. Maximal coupled respiration (respiration linked to ATP production) was lower in muscle from older vs. young subjects (
P
< 0.01), as was maximal uncoupled respiration (
P
= 0.06). Coupling control in response to the ATP synthase inhibitor oligomycin was lower in older adults (
P
< 0.05), as was the mitochondria flux control ratio, coupled respiration normalized to maximal uncoupled respiration (
P
< 0.05). Calculation of respiratory function revealed lower respiration linked to ATP production (
P
< 0.001) and greater reserve respiration (
P
< 0.01); i.e., respiratory capacity not used for phosphorylation in muscle from older adults. We conclude that skeletal muscle mitochondrial respiratory capacity and coupling control decline with age. Lower respiratory capacity and coupling efficiency result in a reduced capacity for ATP production in skeletal muscle of older adults. Mitochondrial health is critical to physiological function, particularly in tissues with high ATP turnover, such as striated muscle. It has been postulated that derangements in skeletal muscle mitochondrial function contribute to impaired physical function in older adults. Here, we determined mitochondrial respiratory capacity and coupling control in skeletal muscle biopsies obtained from young and older adults. Twenty-four young (28 ± 7 yr) and thirty-one older (62 ± 8 yr) adults were studied. Mitochondrial respiration was determined in permeabilized myofibers from the vastus lateralis after the addition of substrates oligomycin and CCCP. Thereafter, mitochondrial coupling control was calculated. Maximal coupled respiration (respiration linked to ATP production) was lower in muscle from older vs. young subjects (P < 0.01), as was maximal uncoupled respiration (P = 0.06). Coupling control in response to the ATP synthase inhibitor oligomycin was lower in older adults (P < 0.05), as was the mitochondria flux control ratio, coupled respiration normalized to maximal uncoupled respiration (P < 0.05). Calculation of respiratory function revealed lower respiration linked to ATP production (P < 0.001) and greater reserve respiration (P < 0.01); i.e., respiratory capacity not used for phosphorylation in muscle from older adults. We conclude that skeletal muscle mitochondrial respiratory capacity and coupling control decline with age. Lower respiratory capacity and coupling efficiency result in a reduced capacity for ATP production in skeletal muscle of older adults. Mitochondrial health is critical to physiological function, particularly in tissues with high ATP turnover, such as striated muscle. It has been postulated that derangements in skeletal muscle mitochondrial function contribute to impaired physical function in older adults. Here, we determined mitochondrial respiratory capacity and coupling control in skeletal muscle biopsies obtained from young and older adults. Twenty-four young (28 ± 7 yr) and thirty-one older (62 ± 8 yr) adults were studied. Mitochondrial respiration was determined in permeabilized myofibers from the vastus lateralis after the addition of substrates oligomycin and CCCP. Thereafter, mitochondrial coupling control was calculated. Maximal coupled respiration (respiration linked to ATP production) was lower in muscle from older vs. young subjects (P < 0.01), as was maximal uncoupled respiration (P = 0.06). Coupling control in response to the ATP synthase inhibitor oligomycin was lower in older adults (P < 0.05), as was the mitochondria flux control ratio, coupled respiration normalized to maximal uncoupled respiration (P < 0.05). Calculation of respiratory function revealed lower respiration linked to ATP production (P < 0.001) and greater reserve respiration (P < 0.01); i.e., respiratory capacity not used for phosphorylation in muscle from older adults. We conclude that skeletal muscle mitochondrial respiratory capacity and coupling control decline with age. Lower respiratory capacity and coupling efficiency result in a reduced capacity for ATP production in skeletal muscle of older adults.Mitochondrial health is critical to physiological function, particularly in tissues with high ATP turnover, such as striated muscle. It has been postulated that derangements in skeletal muscle mitochondrial function contribute to impaired physical function in older adults. Here, we determined mitochondrial respiratory capacity and coupling control in skeletal muscle biopsies obtained from young and older adults. Twenty-four young (28 ± 7 yr) and thirty-one older (62 ± 8 yr) adults were studied. Mitochondrial respiration was determined in permeabilized myofibers from the vastus lateralis after the addition of substrates oligomycin and CCCP. Thereafter, mitochondrial coupling control was calculated. Maximal coupled respiration (respiration linked to ATP production) was lower in muscle from older vs. young subjects (P < 0.01), as was maximal uncoupled respiration (P = 0.06). Coupling control in response to the ATP synthase inhibitor oligomycin was lower in older adults (P < 0.05), as was the mitochondria flux control ratio, coupled respiration normalized to maximal uncoupled respiration (P < 0.05). Calculation of respiratory function revealed lower respiration linked to ATP production (P < 0.001) and greater reserve respiration (P < 0.01); i.e., respiratory capacity not used for phosphorylation in muscle from older adults. We conclude that skeletal muscle mitochondrial respiratory capacity and coupling control decline with age. Lower respiratory capacity and coupling efficiency result in a reduced capacity for ATP production in skeletal muscle of older adults. |
| Author | Durham, William J. Børsheim, Elisabet Sheffield-Moore, Melinda Cotter, Matthew V. Sidossis, Labros S. Hurren, Nicholas M. Tuvdendorj, Demidmaa Reidy, Paul T. Volpi, Elena Bhattarai, Nisha Rasmussen, Blake B. Dillon, Edgar L. Porter, Craig |
| Author_xml | – sequence: 1 givenname: Craig surname: Porter fullname: Porter, Craig organization: Department of Surgery, University of Texas Medical Branch, Galveston, Texas;, Shriners Hospitals for Children, Galveston, Texas – sequence: 2 givenname: Nicholas M. surname: Hurren fullname: Hurren, Nicholas M. organization: Department of Surgery, University of Texas Medical Branch, Galveston, Texas;, Shriners Hospitals for Children, Galveston, Texas;, Departments of Pediatrics and Geriatrics, University of Arkansas for Medical Sciences, Little Rock, Arkansas;, Arkansas Children's Hospital Research Institute, and Arkansas Children's Nutrition Center, Little Rock, Arkansas – sequence: 3 givenname: Matthew V. surname: Cotter fullname: Cotter, Matthew V. organization: Department of Surgery, University of Texas Medical Branch, Galveston, Texas;, Departments of Pediatrics and Geriatrics, University of Arkansas for Medical Sciences, Little Rock, Arkansas;, Arkansas Children's Hospital Research Institute, and Arkansas Children's Nutrition Center, Little Rock, Arkansas – sequence: 4 givenname: Nisha surname: Bhattarai fullname: Bhattarai, Nisha organization: Department of Surgery, University of Texas Medical Branch, Galveston, Texas;, Shriners Hospitals for Children, Galveston, Texas – sequence: 5 givenname: Paul T. surname: Reidy fullname: Reidy, Paul T. organization: Department of Rehabilitation Sciences, University of Texas Medical Branch, Galveston, Texas; and – sequence: 6 givenname: Edgar L. surname: Dillon fullname: Dillon, Edgar L. organization: Department of Internal Medicine, University of Texas Medical Branch, Galveston, Texas – sequence: 7 givenname: William J. surname: Durham fullname: Durham, William J. organization: Department of Internal Medicine, University of Texas Medical Branch, Galveston, Texas – sequence: 8 givenname: Demidmaa surname: Tuvdendorj fullname: Tuvdendorj, Demidmaa organization: Department of Internal Medicine, University of Texas Medical Branch, Galveston, Texas – sequence: 9 givenname: Melinda surname: Sheffield-Moore fullname: Sheffield-Moore, Melinda organization: Department of Internal Medicine, University of Texas Medical Branch, Galveston, Texas – sequence: 10 givenname: Elena surname: Volpi fullname: Volpi, Elena organization: Department of Internal Medicine, University of Texas Medical Branch, Galveston, Texas – sequence: 11 givenname: Labros S. surname: Sidossis fullname: Sidossis, Labros S. organization: Shriners Hospitals for Children, Galveston, Texas;, Department of Internal Medicine, University of Texas Medical Branch, Galveston, Texas – sequence: 12 givenname: Blake B. surname: Rasmussen fullname: Rasmussen, Blake B. organization: Department of Rehabilitation Sciences, University of Texas Medical Branch, Galveston, Texas; and – sequence: 13 givenname: Elisabet surname: Børsheim fullname: Børsheim, Elisabet organization: Department of Surgery, University of Texas Medical Branch, Galveston, Texas;, Shriners Hospitals for Children, Galveston, Texas;, Departments of Pediatrics and Geriatrics, University of Arkansas for Medical Sciences, Little Rock, Arkansas;, Arkansas Children's Hospital Research Institute, and Arkansas Children's Nutrition Center, Little Rock, Arkansas |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/26037248$$D View this record in MEDLINE/PubMed |
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| Cites_doi | 10.1007/s00424-003-1044-9 10.1111/j.1469-7793.2000.00211.x 10.1073/pnas.0501559102 10.2337/db08-0349 10.1096/fj.03-1104fje 10.1016/S0140-6736(89)92143-0 10.1042/CS20140101 10.1016/j.exger.2014.08.013 10.1113/jphysiol.2012.230185 10.1111/j.1474-9726.2012.00844.x 10.1007/978-1-61779-382-0_3 10.1016/0925-4439(94)90061-2 10.1152/jappl.2000.89.3.1072 10.1146/annurev.genet.39.110304.095751 10.1371/journal.pone.0018317 10.3109/00365517509095787 10.1371/journal.pone.0010778 10.1023/A:1006834912257 10.1111/j.1474-9726.2007.00282.x 10.1152/jappl.1993.75.2.813 10.1111/j.1474-9726.2010.00628.x 10.1113/jphysiol.2011.212712 10.2337/db12-1219 10.1016/S0531-5565(03)00092-5 10.1111/j.1748-1716.2012.02408.x 10.1016/S0021-9258(18)96046-1 10.1016/0076-6879(69)13005-0 10.1093/gerona/63.4.350 10.1016/j.jss.2013.05.054 10.1210/jc.2009-1822 10.1016/0006-291X(70)90017-3 10.1073/pnas.93.26.15364 10.3945/ajcn.2010.28608A 10.1152/physrev.1997.77.3.731 10.1073/pnas.0610131104 10.1016/j.biocel.2009.03.013 10.1007/s00424-003-1022-2 |
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| SubjectTerms | Adenosine triphosphatase Adult Age differences Aged Aged, 80 and over Aging ATP Biopsy Call for Papers Carbonyl Cyanide m-Chlorophenyl Hydrazone - pharmacology Cohort Studies Down-Regulation - drug effects Electron Transport Complex I - antagonists & inhibitors Electron Transport Complex I - metabolism Electron Transport Complex II - antagonists & inhibitors Electron Transport Complex II - metabolism Female Humans Male Middle Aged Mitochondria Mitochondria, Muscle - drug effects Mitochondria, Muscle - enzymology Mitochondria, Muscle - metabolism Muscle, Skeletal - drug effects Muscle, Skeletal - growth & development Muscle, Skeletal - metabolism Musculoskeletal system Myofibrils - drug effects Myofibrils - enzymology Myofibrils - metabolism Older people Oligomycins - pharmacology Oxidative Phosphorylation - drug effects Phosphorylation Physiology Proton Ionophores - pharmacology Quadriceps Muscle - drug effects Quadriceps Muscle - growth & development Quadriceps Muscle - metabolism Respiration Respiratory function Uncoupling Agents - pharmacology Young Adult |
| Title | Mitochondrial respiratory capacity and coupling control decline with age in human skeletal muscle |
| URI | https://www.ncbi.nlm.nih.gov/pubmed/26037248 https://www.proquest.com/docview/1702113524 https://www.proquest.com/docview/1701346251 https://pubmed.ncbi.nlm.nih.gov/PMC4525111 |
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