Insulin resistance in type 2 diabetes youth relates to serum free fatty acids and muscle mitochondrial dysfunction

Journal of Diabetes and its Complications

Volumn 31, Issue 1, 2017, Pages 141-148

  Cree Green, Melanie ^a   Gupta, Abhinav ^a   Coe, Gregory V ^a   Baumgartner, Amy D ^a   Pyle, Laura ^b,f   Reusch, Jane E B ^a,c   Brown, Mark S ^d   Newcomer, Bradley R ^e   Nadeau, Kristen J ^a  

^a UNIVERSITY OF COLORADO   (United States)

^b University of Colorado Denver and Children s Hospital Colorado   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

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

^e JAMES MADISON UNIVERSITY   (United States)

^f Food Science and Human Nutrition   (United States)

Author keywords

Adolescents; Free fatty acids; Insulin resistance; Mitochondrial function; Type 2 diabetes

Indexed keywords

CREATINE KINASE; FATTY ACID; GLUCOSE; HEMOGLOBIN A1C; INSULIN; INTRAMYOCELLULAR LIPID; LIPID; LONG ACTING INSULIN; UNCLASSIFIED DRUG;

ADOLESCENT; ARTICLE; BODY MASS; CONTROLLED STUDY; CREATINE KINASE BLOOD LEVEL; DISORDERS OF MITOCHONDRIAL FUNCTIONS; FATTY ACID BLOOD LEVEL; FEMALE; GASTROCNEMIUS MUSCLE; GLUCOSE BLOOD LEVEL; HUMAN; HYPERINSULINEMIA; INSULIN INFUSION; INSULIN RESISTANCE; JUVENILE; LIPID BLOOD LEVEL; MAJOR CLINICAL STUDY; MALE; MITOCHONDRIAL RESPIRATION; NON INSULIN DEPENDENT DIABETES MELLITUS; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL; PUBERTY; BLOOD; BLOOD FLOW; COMPLICATION; EXERCISE; GLUCOSE CLAMP TECHNIQUE; LIPID METABOLISM; METABOLISM; MUSCLE MITOCHONDRION; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; OBESITY; OXYGEN CONSUMPTION; PATHOPHYSIOLOGY; PHYSIOLOGY; SKELETAL MUSCLE;

ADOLESCENT; DIABETES MELLITUS, TYPE 2; EXERCISE; FATTY ACIDS, NONESTERIFIED; FEMALE; GLUCOSE CLAMP TECHNIQUE; HUMANS; INSULIN RESISTANCE; LIPID METABOLISM; MAGNETIC RESONANCE SPECTROSCOPY; MALE; MITOCHONDRIA, MUSCLE; MUSCLE, SKELETAL; OBESITY; OXYGEN CONSUMPTION; REGIONAL BLOOD FLOW;

EID: 85006324003     PISSN: 10568727     EISSN: 1873460X     Source Type: Journal    
DOI: 10.1016/j.jdiacomp.2016.10.014     Document Type: Article

References (40)

1. Antonetti, D.A., Reynet, C., Kahn, C.R., Increased expression of mitochondrial-encoded genes in skeletal muscle of humans with diabetes mellitus. The Journal of Clinical Investigation 95 (1995), 1383–1388.
2. Argov, Z., De Stefano, N., Arnold, D.L., ADP recovery after a brief ischemic exercise in normal and diseased human muscle—a 31P MRS study. NMR in Biomedicine 9 (1996), 165–172.
3. Bajaj, M., Suraamornkul, S., Romanelli, A., Cline, G.W., Mandarino, L.J., Shulman, G.I., DeFronzo, R.A., Effect of a sustained reduction in plasma free fatty acid concentration on intramuscular long-chain fatty acyl-CoAs and insulin action in type 2 diabetic patients. Diabetes 54 (2005), 3148–3153.
4. Bajpeyi, S., Pasarica, M., Moro, C., Conley, K., Jubrias, S., Sereda, O., Smith, S.R., Skeletal muscle mitochondrial capacity and insulin resistance in type 2 diabetes. The Journal of Clinical Endocrinology and Metabolism 96 (2011), 1160–1168.
5. Befroy, D.E., Petersen, K.F., Dufour, S., Mason, G.F., de Graaf, R.A., Rothman, D.L., Shulman, G.I., Impaired mitochondrial substrate oxidation in muscle of insulin-resistant offspring of type 2 diabetic patients. Diabetes 56 (2007), 1376–1381.
6. Bjornstad, P., Maahs, D.M., Cherney, D.Z., Cree-Green, M., West, A., Pyle, L., Nadeau, K.J., Insulin sensitivity is an important determinant of renal health in adolescents with type 2 diabetes. Diabetes Care 37 (2014), 3033–3039.
7. Cree, M.G., Fram, R.Y., Herndon, D.N., Qian, T., Angel, C., Green, J.M., Wolfe, R.R., Human mitochondrial oxidative capacity is acutely impaired after burn trauma. American Journal of Surgery 196 (2008), 234–239.
8. Cree-Green, M., Newcomer, B.R., Brown, M.S., Baumgartner, A.D., Bergman, B., Drew, B., Nadeau, K.J., Delayed skeletal muscle mitochondrial ADP recovery in youth with type 1 diabetes relates to muscle insulin resistance. Diabetes 64 (2015), 383–392.
9. Cree-Green, M., Newcomer, B.R., Brown, M., Hull, A., West, A.D., Singel, D., Nadeau, K.J., Method for controlled mitochondrial perturbation during phosphorus MRS in children. Medicine and Science in Sports and Exercise, 2014.
10. Cree-Green, M., Newcomer, B.R., Coe, G., Newnes, L., Baumgartner, A., Brown, M.S., Nadeau, K.J., Peripheral insulin resistance in obese girls with hyperandrogenism is related to oxidative phosphorylation and elevated serum free fatty acids. American Journal of Physiology. Endocrinology and Metabolism 308 (2015), E726–E733.
11. Cree-Green, M., Triolo, T.M., Nadeau, K.J., Etiology of insulin resistance in youth with type 2 diabetes. Current Diabetes Reports 13 (2013), 81–88.
12. Dabelea, D., Bell, R.A., D'Agostino, R.B. Jr., Imperatore, G., Johansen, J.M., Linder, B., Waitzfelder, B., Incidence of diabetes in youth in the United States. JAMA 297 (2007), 2716–2724.
13. D'Adamo, E., Caprio, S., Type 2 diabetes in youth: Epidemiology and pathophysiology. Diabetes Care 34:Suppl. 2 (2011), S161–S165.
14. Daniele, G., Eldor, R., Merovci, A., Clarke, G.D., Xiong, J., Tripathy, D., Defronzo, R.A., Chronic reduction of plasma FFA improves mitochondrial function and whole body insulin sensitivity in obese and type 2 diabetic individuals. Diabetes 63:8 (2014), 2812–2820, 10.2337/db13-1130.
15. Daniele, G., Eldor, R., Merovci, A., Clarke, G.D., Xiong, J., Tripathy, D., DeFronzo, R.A., Chronic reduction of plasma free fatty acid improves mitochondrial function and whole-body insulin sensitivity in obese and type 2 diabetic individuals. Diabetes 63 (2014), 2812–2820.
16. De Feyter, H.M., Lenaers, E., Houten, S.M., Schrauwen, P., Hesselink, M.K., Wanders, R.J., Prompers, J.J., Increased intramyocellular lipid content but normal skeletal muscle mitochondrial oxidative capacity throughout the pathogenesis of type 2 diabetes. The FASEB Journal 22 (2008), 3947–3955.
17. DeLany, J.P., Dube, J.J., Standley, R.A., Distefano, G., Goodpaster, B.H., Stefanovic-Racic, M., Toledo, F.G., Racial differences in peripheral insulin sensitivity and mitochondrial capacity in the absence of obesity. The Journal of Clinical Endocrinology and Metabolism 99 (2014), 4307–4314.
18. Esterhammer, R., Schocke, M., Gorny, O., Posch, L., Messner, H., Jaschke, W., Greiner, A., Phosphocreatine kinetics in the calf muscle of patients with bilateral symptomatic peripheral arterial disease during exhaustive incremental exercise. Molecular Imaging and Biology: MIB: The Official Publication of the Academy of Molecular Imaging 10 (2008), 30–39.
19. Kelsey, M.M., Forster, J.E., Van Pelt, R.E., Reusch, J.E., Nadeau, K.J., Adipose tissue insulin resistance in adolescents with and without type 2 diabetes. Pediatric Obesity 9 (2014), 373–380.
20. Kelsey, M.M., Zaepfel, A., Bjornstad, P., Nadeau, K.J., Age-related consequences of childhood obesity. Gerontology 60 (2014), 222–228.
21. Klose, U., In vivo proton spectroscopy in presence of eddy currents. Magnetic Resonance in Medicine 14 (1990), 26–30.
22. Larson-Meyer, D.E., Newcomer, B.R., Hunter, G.R., Hetherington, H.P., Weinsier, R.L., 31P MRS measurement of mitochondrial function in skeletal muscle: Reliability, force-level sensitivity and relation to whole body maximal oxygen uptake. NMR in Biomedicine 13 (2000), 14–27.
23. Levitt Katz, L., Gidding, S.S., Bacha, F., Hirst, K., McKay, S., Pyle, L., Lima, J.A., Alterations in left ventricular, left atrial, and right ventricular structure and function to cardiovascular risk factors in adolescents with type 2 diabetes participating in the TODAY clinical trial. Pediatric Diabetes 16 (2015), 39–47.
24. Levy-Marchal, C., Arslanian, S., Cutfield, W., Sinaiko, A., Druet, C., Marcovecchio, M.L., Chiarelli, F., Insulin resistance in children: Consensus, perspective, and future directions. The Journal of Clinical Endocrinology and Metabolism 95 (2010), 5189–5198.
25. Martin, S.D., Morrison, S., Konstantopoulos, N., McGee, S.L., Mitochondrial dysfunction has divergent, cell type-dependent effects on insulin action. Molecular Metabolism 3 (2014), 408–418.
26. Nadeau, K.J., Klingensmith, G., Zeitler, P., Type 2 diabetes in children is frequently associated with elevated alanine aminotransferase. Journal of Pediatric Gastroenterology and Nutrition 41 (2005), 94–98.
27. Nadeau, K.J., Regensteiner, J.G., Bauer, T.A., Brown, M.S., Dorosz, J.L., Hull, A., Reusch, J.E.B., Insulin resistance in adolescents with type 1 diabetes and its relationship to cardiovascular function. Journal of Clinical Endocrinology & Metabolism 95 (2010), 513–521.
28. Nadeau, K.J., Zeitler, P.S., Bauer, T.A., Brown, M.S., Dorosz, J.L., Draznin, B., Regensteiner, J.G., Insulin resistance in adolescents with type 2 diabetes is associated with impaired exercise capacity. The Journal of Clinical Endocrinology and Metabolism 94 (2009), 3687–3695.
29. Newcomer, B.R., Boska, M.D., 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 20 (1997), 336–346.
30. Pedersen, B.L., Baekgaard, N., Quistorff, B., Muscle mitochondrial function in patients with type 2 diabetes mellitus and peripheral arterial disease: Implications in vascular surgery. European Journal of Vascular and Endovascular Surgery: The Official journal of the European Society for Vascular Surgery 38 (2009), 356–364.
31. Phielix, E., Jelenik, T., Nowotny, P., Szendroedi, J., Roden, M., Reduction of non-esterified fatty acids improves insulin sensitivity and lowers oxidative stress, but fails to restore oxidative capacity in type 2 diabetes: A randomised clinical trial. Diabetologia 57 (2014), 572–581.
32. Rabol, R., Hojberg, P.M., Almdal, T., Boushel, R., Haugaard, S.B., Madsbad, S., Dela, F., Effect of hyperglycemia on mitochondrial respiration in type 2 diabetes. The Journal of Clinical Endocrinology and Metabolism 94 (2009), 1372–1378.
33. Rico-Sanz, J., Thomas, E.L., Jenkinson, G., Mierisova, S., Iles, R., Bell, J.D., Diversity in levels of intracellular total creatine and triglycerides in human skeletal muscles observed by 1H-MRS. Journal of Applied Physiology 87 (1999), 2068–2072.
34. Schocke, M., Esterhammer, R., Greiner, A., High-energy phosphate metabolism in the exercising muscle of patients with peripheral arterial disease. VASA Zeitschrift fur Gefasskrankheiten Journal for Vascular Diseases 37 (2008), 199–210.
35. Schrauwen-Hinderling, V.B., Kooi, M.E., Hesselink, M.K., Jeneson, J.A., Backes, W.H., van Echteld, C.J., Schrauwen, P., Impaired in vivo mitochondrial function but similar intramyocellular lipid content in patients with type 2 diabetes mellitus and BMI-matched control subjects. Diabetologia 50 (2007), 113–120.
36. Shulman, G.I., Ectopic fat in insulin resistance, dyslipidemia, and cardiometabolic disease. The New England Journal of Medicine 371 (2014), 1131–1141.
37. Sirikul, B., Hunter, G.R., Larson-Meyer, D.E., Desmond, R., Newcomer, B.R., Relationship between metabolic function and skeletal muscle fatigue during a 90 s maximal isometric contraction. Applied Physiology, Nutrition, and Metabolism = Physiologie Appliquee, Nutrition et Metabolisme 32 (2007), 394–399.
38. van den Boogaart, A., MRUI MANUAL V. 96.3. A user's guide to the magnetic resonance user Interface software package. 1997, Delft Technical University Press, Delft.
39. Wu, F.Y., Tu, H.J., Qin, B., Chen, T., Xu, H.F., Qi, J., Wang, D.H., Value of dynamic (3)(1)P magnetic resonance spectroscopy technique in in vivo assessment of the skeletal muscle mitochondrial function in type 2 diabetes. Chinese Medical Journal 125 (2012), 281–286.
40. Zeitler, P., Hirst, K., Pyle, L., Linder, B., Copeland, K., Arslanian, S., Kaufman, F., A clinical trial to maintain glycemic control in youth with type 2 diabetes. The New England Journal of Medicine 366 (2012), 2247–2256.