Delayed skeletal muscle mitochondrial ADP recovery in youth with type 1 diabetes relates to muscle insulin resistance

Diabetes

Volumn 64, Issue 2, 2015, Pages 383-392

  Cree Green, Melanie ^a,b   Newcomer, Bradley R ^c   Brown, Mark S ^d   Baumgartner, Amy D ^a   Bergman, Bryan ^b,d   Drew, Brendan ^a   Regensteiner, Judith G ^b,d   Pyle, Laura ^a   Reusch, Jane E B ^b,d,e   Nadeau, Kristen J ^a,b  

^a Children's Hospital Colorado   (United States)

^b UNIVERSITY OF COLORADO   (United States)

^c UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^d UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^e VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE; GLUCOSE; INSULIN;

ADOLESCENT; ADULT; ARTICLE; BODY MASS; CHILD; CLINICAL ARTICLE; CONTROLLED STUDY; CROSS-SECTIONAL STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; FEMALE; GLUCOSE BLOOD LEVEL; GLUCOSE INFUSION; HUMAN; HYPERINSULINEMIA; INSULIN DEPENDENT DIABETES MELLITUS; INSULIN RESISTANCE; INSULIN SENSITIVITY; MALE; MITOCHONDRION; OXIDATIVE PHOSPHORYLATION; PHOSPHORUS NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROSPECTIVE STUDY; SKELETAL MUSCLE; TIME; METABOLISM; MUSCLE MITOCHONDRION; PHYSIOLOGY;

ADOLESCENT; CHILD; DIABETES MELLITUS, TYPE 1; FEMALE; HUMANS; INSULIN RESISTANCE; MALE; MITOCHONDRIA, MUSCLE; MUSCLE, SKELETAL;

EID: 84921931752     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db14-0765     Document Type: Article

References (36)

1. Dabelea D, Bell RA, D'Agostino RB Jr, et al.; Writing Group for the SEARCH for Diabetes in Youth Study Group. Incidence of diabetes in youth in the United States. JAMA 2007;297:2716-2724
2. Nadeau KJ, Regensteiner JG, Bauer TA, et al. Insulin resistance in adolescents with type 1 diabetes and its relationship to cardiovascular function. J Clin Endocrinol Metab 2010;95:513-521
3. Orchard TJ, Olson JC, Erbey JR, et al. Insulin resistance-related factors, but not glycemia, predict coronary artery disease in type 1 diabetes: 10-year followup data from the Pittsburgh Epidemiology of Diabetes Complications Study. Diabetes Care 2003;26:1374-1379
4. Bergman BC, Howard D, Schauer IE, et al. Features of hepatic and skeletal muscle insulin resistance unique to type 1 diabetes. J Clin Endocrinol Metab 2012;97:1663-1672
5. Maahs DM, Nadeau K, Snell-Bergeon JK, et al. Association of insulin sensitivity to lipids across the lifespan in people with Type 1 diabetes. Diabet Med 2011;28:148-155
6. Schauer IE, Snell-Bergeon JK, Bergman BC, et al. Insulin resistance, defective insulin-mediated fatty acid suppression, and coronary artery calcification in subjects with and without type 1 diabetes: The CACTI study. Diabetes 2011;60:306-314
7. Olson JC, Erbey JR, Williams KV, et al. Subclinical atherosclerosis and estimated glucose disposal rate as predictors of mortality in type 1 diabetes. Ann Epidemiol 2002;12:331-337
8. Petersen KF, Shulman GI. Etiology of insulin resistance. Am J Med 2006;119(Suppl. 1):S10-S16
9. Petersen KF, Befroy D, Dufour S, et al. Mitochondrial dysfunction in the elderly: possible role in insulin resistance. Science 2003;300:1140-1142
10. Cree MG, Fram RY, Herndon DN, et al. Human mitochondrial oxidative capacity is acutely impaired after burn trauma. Am J Surg 2008;196:234-239
11. Cree MG, Newcomer BR, Herndon DN, et al. PPAR-alpha agonism improves whole body and muscle mitochondrial fat oxidation, but does not alter intracellular fat concentrations in burn trauma children in a randomized controlled trial. Nutr Metab (Lond) 2007;4:9
12. Rickels MR, Naji A, Teff KL. Insulin sensitivity, glucose effectiveness, and free fatty acid dynamics after human islet transplantation for type 1 diabetes. J Clin Endocrinol Metab 2006;91:2138-2144
13. Perseghin G, Lattuada G, Danna M, et al. Insulin resistance, intramyocellular lipid content, and plasma adiponectin in patients with type 1 diabetes. Am J Physiol Endocrinol Metab 2003;285:E1174-E1181
14. Snell-Bergeon JK, Nadeau K. Cardiovascular disease risk in young people with type 1 diabetes. J Cardiovasc Transl Res 2012;5:446-462
15. Antonetti DA, Reynet C, Kahn CR. Increased expression of mitochondrialencoded genes in skeletal muscle of humans with diabetes mellitus. J Clin Invest 1995;95:1383-1388
16. Karakelides H, Asmann YW, Bigelow ML, et al. Effect of insulin deprivation on muscle mitochondrial ATP production and gene transcript levels in type 1 diabetic subjects. Diabetes 2007;56:2683-2689
17. Kacerovsky M, Brehm A, Chmelik M, et al. Impaired insulin stimulation of muscular ATP production in patients with type 1 diabetes. J Intern Med 2011;269:189-199
18. Item F, Heinzer-Schweizer S, Wyss M, et al. Mitochondrial capacity is affected by glycemic status in young untrained women with type 1 diabetes but is not impaired relative to healthy untrained women. Am J Physiol Regul Integr Comp Physiol 2011;301:R60-R66
19. Crowther GJ, Milstein JM, Jubrias SA, Kushmerick MJ, Gronka RK, Conley KE. Altered energetic properties in skeletal muscle of men with well-controlled insulin-dependent (type 1) diabetes. Am J Physiol Endocrinol Metab 2003;284:E655-E662
20. Lanza IR, Bhagra S, Nair KS, Port JD. Measurement of human skeletal muscle oxidative capacity by 31P-MR spectroscopy: a cross-validation with in vitro measurements. J Magn Reson Imaging 2011;34:1143-1150
21. Cree-Green M, Newcomer BR, Brown M, et al. Method for controlled mitochondrial perturbation during phosphorus MRS in children. Med Sci Sports Exerc. 26 February 2014 [Epub ahead of print]
22. Larson-Meyer DE, Newcomer BR, Hunter GR, Hetherington HP, Weinsier RL. 31P MRS measurement of mitochondrial function in skeletal muscle: reliability, force-level sensitivity and relation to whole body maximal oxygen uptake. NMR Biomed 2000;13:14-27
23. Bamman MM, Caruso JF. Resistance exercise countermeasures for space flight: implications of training specificity. J Strength Cond Res 2000;14:45-9
24. Sirikul B, Hunter GR, Larson-Meyer DE, Desmond R, Newcomer BR. Relationship between metabolic function and skeletal muscle fatigue during a 90 s maximal isometric contraction. Appl Physiol Nutr Metab 2007;32:394-399
25. Van Den Boogaart A. MRUI MANUAL V. 96.3. A User's Guide to the Magnetic Resonance User Interface Software Package. Delft, Netherlands, Delft Technical University Press, 1997
26. Klose U. In vivo proton spectroscopy in presence of eddy currents. Magn Reson Med 1990;14:26-30
27. Rico-Sanz J, Thomas EL, Jenkinson G, Mierisová S, Iles R, Bell JD. Diversity in levels of intracellular total creatine and triglycerides in human skeletal muscles observed by 1H-MRS. J Appl Physiol (1985) 1999;87:2068-2072
28. Newcomer BR, Boska MD. Adenosine triphosphate production rates, metabolic economy calculations, pH, phosphomonoesters, phosphodiesters, and force output during short-duration maximal isometric plantar flexion exercises and repeated maximal isometric plantar flexion exercises. Muscle Nerve 1997;20:336-346
29. Spriet LL. Anaerobic metabolism in human skeletal muscle during shortterm, intense activity. Can J Physiol Pharmacol 1992;70:157-165
30. Yki-Järvinen H, Helve E, Koivisto VA. Hyperglycemia decreases glucose uptake in type I diabetes. Diabetes 1987;36:892-896
31. Vuorinen-Markkola H, Koivisto VA, Yki-Jarvinen H. Mechanisms of hyperglycemia-induced insulin resistance in whole body and skeletal muscle of type I diabetic patients. Diabetes 1992;41:571-580
32. Liu H-Y, Cao SY, Hong T, Han J, Liu Z, Cao W. Insulin is a stronger inducer of insulin resistance than hyperglycemia in mice with type 1 diabetes mellitus (T1DM). J Biol Chem 2009;284:27090-27100
33. Shulman GI. Cellular mechanisms of insulin resistance. J Clin Invest 2000;106:171-176
34. Rabøl R, Højberg PM, Almdal T, et al. Effect of hyperglycemia on mitochondrial respiration in type 2 diabetes. J Clin Endocrinol Metab 2009;94:1372-1378
35. Thankamony A, Tossavainen PH, Sleigh A, et al. Short-term administration of pegvisomant improves hepatic insulin sensitivity and reduces soleus muscle intramyocellular lipid content in young adults with type 1 diabetes. J Clin Endocrinol Metab 2014;99:639-647
36. Goodpaster BH, He J, Watkins S, Kelley DE. Skeletal muscle lipid content and insulin resistance: evidence for a paradox in endurance-trained athletes. J Clin Endocrinol Metab 2001;86:5755-5761