{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,22]],"date-time":"2026-06-22T22:49:25Z","timestamp":1782168565912,"version":"3.54.5"},"reference-count":40,"publisher":"The Endocrine Society","issue":"9","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2012,9,1]]},"DOI":"10.1210\/jc.2011-3454","type":"journal-article","created":{"date-parts":[[2012,7,17]],"date-time":"2012-07-17T13:28:35Z","timestamp":1342531715000},"page":"3261-3269","source":"Crossref","is-referenced-by-count":95,"title":["Physical Activity Is the Key Determinant of Skeletal Muscle Mitochondrial Function in Type 2 Diabetes"],"prefix":"10.1210","volume":"97","author":[{"given":"F. H. J.","family":"van Tienen","sequence":"first","affiliation":[{"name":"Departments of Genetics and Cell Biology (F.H.J.v.T., P.J.L., H.J.M.S.), 6200 MD Maastricht, The Netherlands"},{"name":"Human Movement Sciences (L.J.C.v.L.), 6200 MD Maastricht, The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"S. F. E.","family":"Praet","sequence":"additional","affiliation":[{"name":"Departments of Rehabilitation Medicine (S.F.E.P.), 3000 CA Rotterdam, The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"H. M.","family":"de Feyter","sequence":"additional","affiliation":[{"name":"Department of Diagnostic Radiology (H.M.d.F.), Magnetic Resonance Research Center, Yale University School of Medicine, New Haven, Connecticut 06510"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"N. M.","family":"van den Broek","sequence":"additional","affiliation":[{"name":"Biomedical NMR (N.M.v.d.B., J.J.P., K.N.), Department of Biomedical Engineering, Eindhoven University of Technology, 5600 MB Eindhoven, The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"P. J.","family":"Lindsey","sequence":"additional","affiliation":[{"name":"Departments of Genetics and Cell Biology (F.H.J.v.T., P.J.L., H.J.M.S.), 6200 MD Maastricht, The Netherlands"},{"name":"NUTRIM School for Nutrition, Toxicology, and Metabolism (F.H.J.v.T., P.J.L., H.J.M.S., L.J.C.v.L.), 6200 MD Maastricht, The Netherlands"},{"name":"Cardiovascular Research Institute Maastricht (P.J.L., H.J.M.S.), 6200 MD Maastricht, The Netherlands"},{"name":"GROW-School of Oncology and Developmental Biology (P.J.L., H.J.M.S.), Maastricht University Medical Centre, 6200 MD Maastricht, The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"K. G. C.","family":"Schoonderwoerd","sequence":"additional","affiliation":[{"name":"Clinical Genetics (K.G.C.S.), 3000 CA Rotterdam, The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"I. F. M.","family":"de Coo","sequence":"additional","affiliation":[{"name":"Neurology (I.F.M.d.C.), Erasmus University Medical Center, 3000 CA Rotterdam, The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"K.","family":"Nicolay","sequence":"additional","affiliation":[{"name":"Biomedical NMR (N.M.v.d.B., J.J.P., K.N.), Department of Biomedical Engineering, Eindhoven University of Technology, 5600 MB Eindhoven, The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"J. J.","family":"Prompers","sequence":"additional","affiliation":[{"name":"Biomedical NMR (N.M.v.d.B., J.J.P., K.N.), Department of Biomedical Engineering, Eindhoven University of Technology, 5600 MB Eindhoven, The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"H. J. M.","family":"Smeets","sequence":"additional","affiliation":[{"name":"Departments of Genetics and Cell Biology (F.H.J.v.T., P.J.L., H.J.M.S.), 6200 MD Maastricht, The Netherlands"},{"name":"NUTRIM School for Nutrition, Toxicology, and Metabolism (F.H.J.v.T., P.J.L., H.J.M.S., L.J.C.v.L.), 6200 MD Maastricht, The Netherlands"},{"name":"Cardiovascular Research Institute Maastricht (P.J.L., H.J.M.S.), 6200 MD Maastricht, The Netherlands"},{"name":"GROW-School of Oncology and Developmental Biology (P.J.L., H.J.M.S.), Maastricht University Medical Centre, 6200 MD Maastricht, The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"L. J. C.","family":"van Loon","sequence":"additional","affiliation":[{"name":"Human Movement Sciences (L.J.C.v.L.), 6200 MD Maastricht, The Netherlands"},{"name":"NUTRIM School for Nutrition, Toxicology, and Metabolism (F.H.J.v.T., P.J.L., H.J.M.S., L.J.C.v.L.), 6200 MD Maastricht, The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"80","reference":[{"key":"key\n\t\t\t\t2019041113343569500_B1","doi-asserted-by":"crossref","first-page":"389","DOI":"10.1080\/07853890600888413","article-title":"The metabolic syndrome: role of skeletal muscle metabolism.","volume":"38","author":"Stump","year":"2006","journal-title":"Ann Med"},{"key":"key\n\t\t\t\t2019041113343569500_B2","doi-asserted-by":"crossref","first-page":"206","DOI":"10.1016\/j.bbadis.2005.04.001","article-title":"Reduced insulin-mediated citrate synthase activity in cultured skeletal muscle cells from patients with type 2 diabetes: evidence for an intrinsic oxidative enzyme defect.","volume":"1741","author":"Ortenblad","year":"2005","journal-title":"Biochim Biophys Acta"},{"key":"key\n\t\t\t\t2019041113343569500_B3","doi-asserted-by":"crossref","first-page":"2944","DOI":"10.2337\/diabetes.51.10.2944","article-title":"Dysfunction of mitochondria in human skeletal muscle in type 2 diabetes.","volume":"51","author":"Kelley","year":"2002","journal-title":"Diabetes"},{"key":"key\n\t\t\t\t2019041113343569500_B4","doi-asserted-by":"crossref","first-page":"790","DOI":"10.1007\/s00125-007-0594-3","article-title":"Patients with type 2 diabetes have normal mitochondrial function in skeletal muscle.","volume":"50","author":"Boushel","year":"2007","journal-title":"Diabetologia"},{"key":"key\n\t\t\t\t2019041113343569500_B5","doi-asserted-by":"crossref","first-page":"3309","DOI":"10.2337\/db05-1230","article-title":"Skeletal muscle mitochondrial functions, mitochondrial DNA copy numbers, and gene transcript profiles in type 2 diabetic and nondiabetic subjects at equal levels of low or high insulin and euglycemia.","volume":"55","author":"Asmann","year":"2006","journal-title":"Diabetes"},{"key":"key\n\t\t\t\t2019041113343569500_B6","doi-asserted-by":"crossref","first-page":"2943","DOI":"10.2337\/db08-0391","article-title":"Lower intrinsic ADP-stimulated mitochondrial respiration underlies in vivo mitochondrial dysfunction in muscle of male type 2 diabetic patients.","volume":"57","author":"Phielix","year":"2008","journal-title":"Diabetes"},{"key":"key\n\t\t\t\t2019041113343569500_B7","doi-asserted-by":"crossref","first-page":"8","DOI":"10.2337\/diabetes.54.1.8","article-title":"Deficiency of subsarcolemmal mitochondria in obesity and type 2 diabetes.","volume":"54","author":"Ritov","year":"2005","journal-title":"Diabetes"},{"key":"key\n\t\t\t\t2019041113343569500_B8","doi-asserted-by":"crossref","first-page":"643","DOI":"10.1530\/EJE-07-0756","article-title":"Early or advanced stage type 2 diabetes is not accompanied by in vivo skeletal muscle mitochondrial dysfunction.","volume":"158","author":"De Feyter","year":"2008","journal-title":"Eur J Endocrinol"},{"key":"key\n\t\t\t\t2019041113343569500_B9","doi-asserted-by":"crossref","first-page":"2541","DOI":"10.2337\/diacare.28.10.2541","article-title":"Type 2 diabetes, muscle strength, and impaired physical function: the tip of the iceberg?","volume":"28","author":"Sayer","year":"2005","journal-title":"Diabetes Care"},{"key":"key\n\t\t\t\t2019041113343569500_B10","doi-asserted-by":"crossref","first-page":"699","DOI":"10.1007\/s00125-007-0595-2","article-title":"Mitochondrial function: use it or lose it.","volume":"50","author":"Hawley","year":"2007","journal-title":"Diabetologia"},{"key":"key\n\t\t\t\t2019041113343569500_B11","doi-asserted-by":"crossref","first-page":"165","DOI":"10.1016\/j.ygeno.2005.09.007","article-title":"Expression profiling following local muscle inactivity in humans provides new perspective on diabetes-related genes.","volume":"87","author":"Timmons","year":"2006","journal-title":"Genomics"},{"key":"key\n\t\t\t\t2019041113343569500_B12","doi-asserted-by":"crossref","first-page":"170","DOI":"10.1016\/j.metabol.2007.08.021","article-title":"Effect of aerobic exercise training on oxidative stress in patients with type 2 diabetes mellitus.","volume":"57","author":"Nojima","year":"2008","journal-title":"Metabolism"},{"key":"key\n\t\t\t\t2019041113343569500_B13","doi-asserted-by":"crossref","first-page":"1543","DOI":"10.2337\/diabetes.53.6.1543","article-title":"Muscle strength in type 2 diabetes.","volume":"53","author":"Andersen","year":"2004","journal-title":"Diabetes"},{"key":"key\n\t\t\t\t2019041113343569500_B14","doi-asserted-by":"crossref","first-page":"605","DOI":"10.7326\/0003-4819-132-8-200004180-00002","article-title":"Low cardiorespiratory fitness and physical inactivity as predictors of mortality in men with type 2 diabetes.","volume":"132","author":"Wei","year":"2000","journal-title":"Ann Intern Med"},{"key":"key\n\t\t\t\t2019041113343569500_B15","doi-asserted-by":"crossref","first-page":"163","DOI":"10.1530\/EJE-07-0169","article-title":"Longstanding, insulin-treated type 2 diabetes patients with complications respond well to short-term resistance and interval exercise training.","volume":"158","author":"Praet","year":"2008","journal-title":"Eur J Endocrinol"},{"key":"key\n\t\t\t\t2019041113343569500_B16","article-title":"Definition and diagnosis of diabetes mellitus and intermediate hyperglycaemia: report of a WHO\/IDF consultation","author":"World Health Organization and International Diabetes Federation","year":"2006"},{"key":"key\n\t\t\t\t2019041113343569500_B17","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1016\/0925-4439(95)00013-T","article-title":"Riboflavin-responsive complex I deficiency.","volume":"1271","author":"Scholte","year":"1995","journal-title":"Biochim Biophys Acta"},{"key":"key\n\t\t\t\t2019041113343569500_B18","doi-asserted-by":"crossref","first-page":"e92","DOI":"10.1161\/01.RES.0000172081.30327.28","article-title":"Downregulation of apoptosis-inducing factor in harlequin mutant mice sensitizes the myocardium to oxidative stress-related cell death and pressure overload-induced decompensation.","volume":"96","author":"van Empel","year":"2005","journal-title":"Circ Res"},{"key":"key\n\t\t\t\t2019041113343569500_B19","doi-asserted-by":"crossref","first-page":"207","DOI":"10.1016\/j.bbrc.2009.07.004","article-title":"Wnt5b stimulates adipogenesis by activating PPAR\u03b3, and inhibiting the \u03b2-catenin dependent Wnt signaling pathway together with Wnt5a.","volume":"387","author":"van Tienen","year":"2009","journal-title":"Biochem Biophys Res Commun"},{"key":"key\n\t\t\t\t2019041113343569500_B20","doi-asserted-by":"crossref","first-page":"R61","DOI":"10.1186\/gb-2003-4-10-r61","article-title":"Time- and exercise-dependent gene regulation in human skeletal muscle.","volume":"4","author":"Zambon","year":"2003","journal-title":"Genome Biol"},{"key":"key\n\t\t\t\t2019041113343569500_B21","doi-asserted-by":"crossref","first-page":"467S","DOI":"10.3945\/ajcn.2008.26717D","article-title":"Muscle mitochondrial changes with aging and exercise.","volume":"89","author":"Lanza","year":"2009","journal-title":"Am J Clin Nutr"},{"key":"key\n\t\t\t\t2019041113343569500_B22","doi-asserted-by":"crossref","first-page":"1160","DOI":"10.1210\/jc.2010-1621","article-title":"Skeletal muscle mitochondrial capacity and insulin resistance in type 2 diabetes.","volume":"96","author":"Bajpeyi","year":"2011","journal-title":"J Clin Endocrinol Metab"},{"key":"key\n\t\t\t\t2019041113343569500_B23","doi-asserted-by":"crossref","first-page":"1427","DOI":"10.1007\/s00125-011-2098-4","article-title":"Increased mitochondrial substrate sensitivity in skeletal muscle of patients with type 2 diabetes.","volume":"54","author":"Larsen","year":"2011","journal-title":"Diabetologia"},{"key":"key\n\t\t\t\t2019041113343569500_B24","doi-asserted-by":"crossref","first-page":"1592","DOI":"10.2337\/db06-0981","article-title":"Mitochondrial respiration is decreased in skeletal muscle of patients with type 2 diabetes.","volume":"56","author":"Mogensen","year":"2007","journal-title":"Diabetes"},{"key":"key\n\t\t\t\t2019041113343569500_B25","doi-asserted-by":"crossref","first-page":"2004","DOI":"10.1152\/jappl.1992.73.5.2004","article-title":"Adaptation of mitochondrial ATP production in human skeletal muscle to endurance training and detraining.","volume":"73","author":"Wibom","year":"1992","journal-title":"J Appl Physiol"},{"key":"key\n\t\t\t\t2019041113343569500_B26","doi-asserted-by":"crossref","first-page":"1297","DOI":"10.1097\/00005768-200108000-00009","article-title":"Muscular characteristics of detraining in humans.","volume":"33","author":"Mujika","year":"2001","journal-title":"Medicine and science in sports and exercise"},{"key":"key\n\t\t\t\t2019041113343569500_B27","doi-asserted-by":"crossref","first-page":"664","DOI":"10.1056\/NEJMoa031314","article-title":"Impaired mitochondrial activity in the insulin-resistant offspring of patients with type 2 diabetes.","volume":"350","author":"Petersen","year":"2004","journal-title":"N Engl J Med"},{"key":"key\n\t\t\t\t2019041113343569500_B28","doi-asserted-by":"crossref","first-page":"1888","DOI":"10.2337\/diabetes.52.8.1888","article-title":"Impact of aerobic exercise training on age-related changes in insulin sensitivity and muscle oxidative capacity.","volume":"52","author":"Short","year":"2003","journal-title":"Diabetes"},{"key":"key\n\t\t\t\t2019041113343569500_B29","doi-asserted-by":"crossref","first-page":"e289","DOI":"10.1371\/journal.pmed.0020289","article-title":"Insulin resistance in the offspring of parents with type 2 diabetes.","volume":"2","author":"Wagenmakers","year":"2005","journal-title":"PLoS medicine"},{"key":"key\n\t\t\t\t2019041113343569500_B30","doi-asserted-by":"crossref","first-page":"7996","DOI":"10.1073\/pnas.1332551100","article-title":"Effect of insulin on human skeletal muscle mitochondrial ATP production, protein synthesis, and mRNA transcripts.","volume":"100","author":"Stump","year":"2003","journal-title":"Proc Natl Acad Sci USA"},{"key":"key\n\t\t\t\t2019041113343569500_B31","doi-asserted-by":"crossref","first-page":"463S","DOI":"10.3945\/ajcn.2008.26717C","article-title":"Skeletal muscle \u201cmitochondrial deficiency\u201d does not mediate insulin resistance.","volume":"89","author":"Holloszy","year":"2009","journal-title":"Am J Clin Nutr"},{"key":"key\n\t\t\t\t2019041113343569500_B32","doi-asserted-by":"crossref","first-page":"7815","DOI":"10.1073\/pnas.0802057105","article-title":"High-fat diets cause insulin resistance despite an increase in muscle mitochondria.","volume":"105","author":"Hancock","year":"2008","journal-title":"Proc Natl Acad Sci USA"},{"key":"key\n\t\t\t\t2019041113343569500_B33","doi-asserted-by":"crossref","first-page":"E1298","DOI":"10.1210\/jc.2011-0278","article-title":"Intact primary mitochondrial function in myotubes established from women with PCOS.","volume":"96","author":"Eriksen","year":"2011","journal-title":"J Clin Endocrinol Metab"},{"key":"key\n\t\t\t\t2019041113343569500_B34","doi-asserted-by":"crossref","first-page":"1166","DOI":"10.2337\/db07-1556","article-title":"Asian Indians have enhanced skeletal muscle mitochondrial capacity to produce ATP in association with severe insulin resistance.","volume":"57","author":"Nair","year":"2008","journal-title":"Diabetes"},{"key":"key\n\t\t\t\t2019041113343569500_B35","doi-asserted-by":"crossref","first-page":"127","DOI":"10.1002\/jmri.21620","article-title":"Phosphorus-31 magnetic resonance spectroscopy of skeletal muscle in maternally inherited diabetes and deafness A3243G mitochondrial mutation carriers.","volume":"29","author":"van Elderen","year":"2009","journal-title":"J Magn Reson Imaging"},{"key":"key\n\t\t\t\t2019041113343569500_B36","doi-asserted-by":"crossref","first-page":"841","DOI":"10.2337\/diacare.27.3.841","article-title":"Is a long-term aerobic plus resistance training program feasible for and effective on metabolic profiles in type 2 diabetic patients?","volume":"27","author":"Balducci","year":"2004","journal-title":"Diabetes Care"},{"key":"key\n\t\t\t\t2019041113343569500_B37","doi-asserted-by":"crossref","first-page":"2511","DOI":"10.2337\/dc07-0183","article-title":"Exercise training improves glycemic control in longstanding insulin-treated type 2 diabetic patients.","volume":"30","author":"De Feyter","year":"2007","journal-title":"Diabetes Care"},{"key":"key\n\t\t\t\t2019041113343569500_B38","doi-asserted-by":"crossref","first-page":"752","DOI":"10.1016\/j.mehy.2008.06.024","article-title":"Exercise interval training: an improved stimulus for improving the physiology of pre-diabetes.","volume":"71","author":"Earnest","year":"2008","journal-title":"Med Hypotheses"},{"key":"key\n\t\t\t\t2019041113343569500_B39","doi-asserted-by":"crossref","first-page":"572","DOI":"10.2337\/db09-1322","article-title":"Restoration of muscle mitochondrial function and metabolic flexibility in type 2 diabetes by exercise training is paralleled by increased myocellular fat storage and improved insulin sensitivity.","volume":"59","author":"Meex","year":"2010","journal-title":"Diabetes"},{"key":"key\n\t\t\t\t2019041113343569500_B40","doi-asserted-by":"crossref","first-page":"1324","DOI":"10.2337\/diabetes.50.6.1324","article-title":"GLUT4 is reduced in slow muscle fibers of type 2 diabetic patients: is insulin resistance in type 2 diabetes a slow, type 1 fiber disease?","volume":"50","author":"Gaster","year":"2001","journal-title":"Diabetes"}],"container-title":["The Journal of Clinical Endocrinology & Metabolism"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/academic.oup.com\/jcem\/article-pdf\/97\/9\/3261\/9048423\/jcem3261.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2019,7,1]],"date-time":"2019-07-01T02:37:35Z","timestamp":1561948655000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/jcem\/article\/97\/9\/3261\/2537032"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2012,9,1]]},"references-count":40,"journal-issue":{"issue":"9","published-print":{"date-parts":[[2012,9,1]]}},"URL":"https:\/\/doi.org\/10.1210\/jc.2011-3454","relation":{},"ISSN":["0021-972X","1945-7197"],"issn-type":[{"value":"0021-972X","type":"print"},{"value":"1945-7197","type":"electronic"}],"subject":[],"published":{"date-parts":[[2012,9,1]]}}}