Lower fasting muscle mitochondrial activity relates to hepatic steatosis in humans

Diabetes Care

Volumn 37, Issue 2, 2014, Pages 468-474

  Szendroedi, Julia ^a,b   Kaul, Kirti ^a   Kloock, Lisa ^a   Straßburger, Klaus ^a   Schmid, Albrecht Ingo ^c,d   Chmelik, Marek ^c   Kacerovsky, Michaela ^e   Kacerovsky Bielesz, Gertrud ^e   Prikoszovich, Thomas ^c   Brehm, Attila ^e   Kršš Ák, Martin ^c   Gruber, Stephan ^c   Krebs, Michael ^c   Kautzky Willer, Alexandra ^c   Moser, Ewald ^c,d   Pacini, Giovanni ^f   Roden, Michael ^a,b  

^a LEIBNIZ CENTER FOR DIABETES RESEARCH AT HEINRICH HEINE UNIVERSITY DÜSSELDORF   (Germany)

^b HEINRICH HEINE UNIVERSITY   (Germany)

^c MEDICAL UNIVERSITY OF VIENNA   (Austria)

^d Christian Doppler Laboratory for Innovative Optical Imaging and its Translation to Medicine   (Austria)

^e HANUSCH HOSPITAL   (Austria)

^f CNR   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

C PEPTIDE; FATTY ACID; GLUCOSE; HEMOGLOBIN A1C; INSULIN; LIPOPROTEIN; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; TRIACYLGLYCEROL;

ADULT; AGE; ARTICLE; BODY MASS; CLAMP; DISEASE ASSOCIATION; EUGLYCEMIC HYPERINSULINEMIC CLAMP; FATTY ACID BLOOD LEVEL; FATTY LIVER; FEMALE; GLUCOSE BLOOD LEVEL; HEMOGLOBIN BLOOD LEVEL; HUMAN; HUMAN CELL; HUMAN EXPERIMENT; INSULIN BLOOD LEVEL; INSULIN SENSITIVITY; LIPID LIVER LEVEL; LIPOPROTEIN BLOOD LEVEL; LIVER METABOLISM; MALE; MUSCLE MITOCHONDRIAL ACTIVITY; MUSCLE MITOCHONDRION; NORMAL HUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; ORAL GLUCOSE TOLERANCE TEST; TRIACYLGLYCEROL BLOOD LEVEL; DIET RESTRICTION; ENZYMOLOGY; INSULIN RESISTANCE; METABOLISM; MIDDLE AGED; YOUNG ADULT;

ADULT; FASTING; FATTY LIVER; FEMALE; HUMANS; INSULIN RESISTANCE; MAGNETIC RESONANCE SPECTROSCOPY; MALE; MIDDLE AGED; MITOCHONDRIA, MUSCLE; MITOCHONDRIAL PROTON-TRANSLOCATING ATPASES; YOUNG ADULT;

EID: 84893027699     PISSN: 01495992     EISSN: 19355548     Source Type: Journal    
DOI: 10.2337/dc13-1359     Document Type: Article

References (40)

1. Perseghin G, Scifo P, De Cobelli F, et al. Intramyocellular triglyceride content is a determinant of in vivo insulin resistance in humans: a 1H-13C nuclear magnetic resonance spectroscopy assessment in offspring of type 2 diabetic parents.Diabetes 1999;48:1600-1606
2. Krssak M, Falk Petersen K, Dresner A, et al. Intramyocellular lipid concentrations are correlated with insulin sensitivity in humans: a 1H NMR spectroscopy study. Diabetologia 1999;42:113-116
3. Flannery C, Dufour S, Rabøl R, Shulman GI, Petersen KF. Skeletal muscle insulin resistance promotes increased hepatic de novo lipogenesis, hyperlipidemia, and hepatic steatosis in the elderly. Diabetes 2012;61:2711-2717
4. Petersen KF, Dufour S, Savage DB, et al. The role of skeletal muscle insulin resistance in the pathogenesis of the metabolic syndrome. Proc Natl Acad Sci USA 2007;104:12587- 12594
5. Bhat G, Baba CS, Pandey A, Kumari N, Choudhuri G. Life style modification improves insulin resistance and liver histology in patients with non-alcoholicfatty liver disease. World J Hepatol 2012;4: 209-217
6. Schmid AI, Szendroedi J, Chmelik M, Krss'ak M, Moser E, Roden M. Liver ATP synthesis is lower and relates to insulin sensitivity in patients with type 2 diabetes. Diabetes Care 2011;34:448-453
7. Brehm A, Krssak M, Schmid AI, Nowotny P, Waldh?ausl W, Roden M. Increased lipid availability impairs insulin-stimulated ATP synthesis in human skeletal muscle. Diabetes 2006;55:136-140
8. Boden G, Chen X, Ruiz J, White JV, Rossetti L. Mechanisms of fatty acid-induced inhibition of glucose uptake. J Clin Invest i1994;93:2438-2446
9. Szendroedi J, Schmid AI, Chmelik M, et al. Muscle mitochondrial ATP synthesis and glucose transport/phosphorylation in type 2 diabetes. PLoS Med 2007;4:e154
10. Perseghin G, Scifo P, Danna M, et al. Normal insulin sensitivity and IMCL content in overweight humans are associated with higher fasting lipid oxidation. Am J Physiol Endocrinol Metab 2002;283:E556-E564
11. Szendroedi J, Phielix E, Roden M. The role of mitochondria in insulin resistance and type 2 diabetes mellitus. Nat Rev Endocrinol2012;8:92-103
12. Petersen KF, Dufour S, Befroy D, Garcia R, Shulman GI. Impaired mitochondrial activity in the insulin-resistant offspring ofpatients with type 2 diabetes. N Engl J Med 2004;350:664-671
13. Karakelides H, Irving BA, Short KR, O'Brien P, Nair KS. Age, obesity, and sex effects on insulin sensitivity and skeletal muscle mitochondrial function. Diabetes 2010;59: 89-97
14. 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
15. Kacerovsky-Bielesz G, Kacerovsky M, Chmelik M, et al. A single nucleotide polymorphism associates with the response of muscle ATP synthesis to longterm exercise training in relatives of type 2iabetic humans. Diabetes Care 2012;35:350-357
16. Prikoszovich T, Winzer C, Schmid AI, et al. Body and liver fat mass rather than muscle mitochondrial function determine glucose metabolism in women with a history of gestational diabetes mellitus. Diabetes Care 2011;34:430-436
17. Szendroedi J, Zwettler E, Schmid AI, et al. Reduced basal ATP synthetic flux of skeletal muscle in patients with previous acromegaly. PLoS ONE 2008;3:e3958
18. Baecke JA, Burema J, Frijters JE. A short questionnaire for the measurement of habitual physical activity in epidemiological studies. Am J Clin Nutr 1982;36:936-942
19. Mari A, Pacini G, Murphy E, Ludvik B, Nolan JJ. A model-based method for assessing insulin sensitivity from the oral glucose tolerance test. Diabetes Care 2001;24:539- 548
20. Pacini G, Mari A. Methods for clinical assessment of insulin sensitivity and betacell function. Best Pract Res Clin Endocrinol Metab 2003;17:305-322
21. Szendroedi J, Chmelik M, Schmid AI, et al. Abnormal hepatic energy homeostasis in type 2 diabetes. Hepatology 2009;50:1079-1086
22. Pessayre D, Fromenty B, Mansouri A. Mitochondrial injury in steatohepatitis. Eur J Gastroenterol Hepatol 2004;16:1095-1105
23. Machado MV, Ferreira DM, Castro RE, et al. Liver and muscle in morbid obesity: the interplay of fatty liver and insulin resistance. PLoS ONE 2012;7:e31738
24. Abdelmalek MF, Lazo M, Horska A, et al.; Fatty Liver Subgroup of Look AHEAD Research Group. Higher dietary fructose is associated with impaired hepatic adenosine triphosphate homeostasis in obese individuals with type 2 diabetes.Hepatology 2012;56:952-960
25. Roden M. How free fatty acids inhibit glucose utilization in human skeletal muscle. News Physiol Sci 2004;19:92-96
26. Petersen KF, Dufour S, Shulman GI. Decreased insulin-stimulated ATP synthesis and phosphate transport in muscle of insulin-resistant offspring of type 2 diabetic parents. PLoS Med 2005;2:e233
27. Schrauwen-Hinderling VB, Kooi ME, Hesselink MK, et al. Impaired in vivo mitochondrial function but similar intramyocellular lipid content in patientswith type 2 diabetes mellitus and BMImatched control subjects. Diabetologia2007;50:113-120
28. Hwang H, Bowen BP, Lefort N, et al. Proteomics analysis of human skeletal muscle reveals novel abnormalities in obesity and type 2 diabetes. Diabetes 2010; 59:33-42
29. He J, Watkins S, Kelley DE. Skeletal muscle lipid content and oxidative enzyme ctivityin relation to muscle fiber type in type 2 diabetes and obesity. Diabetes 2001;50: 817-823
30. Ritov VB, Menshikova EV, He J, Ferrell RE, Goodpaster BH, Kelley DE. Deficiency of subsarcolemmal mitochondria in obesity and type 2 diabetes. Diabetes 2005;54: 8-14
31. Kelley DE, Kuller LH, McKolanis TM, Harper P, Mancino J, Kalhan S. Effects of oderate weight loss and orlistat on insulin resistance, regional adiposity, and fatty acids in type 2 diabetes. Diabetes Care 2004;27:33-40
32. Kelley DE, He J, Menshikova EV, Ritov VB. Dysfunction of mitochondria in human skeletal muscle in type 2 diabetes. Diabetes 2002;51:2944-2950
33. Lim EL, Hollingsworth KG, Smith FE, Thelwall PE, Taylor R. Effects of raising muscle glycogen synthesis rate on skeletalmuscle ATP turnover rate in type 2diabetes. Am J Physiol Endocrinol Metab 2011;301:E1155-E1162
34. Toledo FG, Menshikova EV, Ritov VB, et al. Effects of physical activity and weight loss on skeletal muscle mitochondria and relationship with glucose control in type 2diabetes. Diabetes 2007;56:2142-2147
35. Short KR, Vittone JL, Bigelow ML, et al. Impact of aerobic exercise training on agerelated changes in insulin sensitivity and muscle oxidative capacity. Diabetes 2003; 52:1888-1896
36. Turner N, Bruce CR, Beale SM, et al. Excess lipid availability increases mitochondrial fatty acid oxidative capacity in muscle: evidence against a role for reduced fatty acid oxidation in lipid-induced insulin resistance in rodents. Diabetes 2007;56: 2085-2092
37. 31P- magnetization transfer magnetic resonance spectroscopy measurements of in vivo metabolism. Diabetes i2012;61:2669-2678
38. Jucker BM, Dufour S, Ren J, et al. Assessment of mitochondrial energy coupling in vivo by 13C/31P NMR. Proc Natl Acad Sci USA 2000;97:6880-6884
39. Schmid AI, Schrauwen-Hinderling VB, Andreas M, Wolzt M, Moser E, Roden M. Comparison of measuring energy metabolism by different (31) P-magnetic resonance spectroscopy techniques in resting, ischemic, and exercising muscle.Magn Reson Med 2012;67:898-905
40. Petersen KF, Dufour S, Feng J, et al. Increased prevalence of insulin resistance and nonalcoholic fatty liver disease inAsian-Indian men. Proc Natl Acad Sci USA 2006;103:18273-182773