Muscular mitochondrial dysfunction and type 2 diabetes mellitus

Current Opinion in Clinical Nutrition and Metabolic Care

Volumn 10, Issue 6, 2007, Pages 698-703

  Schrauwen Hinderling, Vera B ^a,c   Roden, Michael ^b   Kooi, M Eline ^a   Hesselink, Matthijs K C ^a   Schrauwen, Patrick ^a  

^a MAASTRICHT UNIVERSITY   (Netherlands)

^b MEDICAL UNIVERSITY OF VIENNA   (Austria)

^c MAASTRICHT UNIVERSITY   (Netherlands)

Author keywords

Insulin resistance; Mitochondrial function; Skeletal muscle; Type 2 diabetes

Indexed keywords

ADENOSINE TRIPHOSPHATE; CREATINE PHOSPHATE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA;

CELL DAMAGE; CELL DENSITY; CELL FUNCTION; DISORDERS OF MITOCHONDRIAL FUNCTIONS; EX VIVO STUDY; HUMAN; IN VIVO STUDY; INSULIN RESISTANCE; INSULIN SENSITIVITY; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; MUSCLE; NON INSULIN DEPENDENT DIABETES MELLITUS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; OXIDATION; REVIEW; SKELETAL MUSCLE;

ADENOSINE TRIPHOSPHATE; ADIPOSE TISSUE; CELL RESPIRATION; DIABETES MELLITUS, TYPE 2; EXERCISE; HUMANS; INSULIN RESISTANCE; MAGNETIC RESONANCE SPECTROSCOPY; MITOCHONDRIA, MUSCLE; MUSCLE, SKELETAL; OXIDATIVE PHOSPHORYLATION;

EID: 37349023268     PISSN: 13631950     EISSN: 15353885     Source Type: Journal    
DOI: 10.1097/MCO.0b013e3282f0eca9     Document Type: Review

References (35)

1. Wild S, Roglic G, Green A, et al. Global prevalence of diabetes: estimates for the year 2000 and projections for 2030. Diabetes Care 2004; 27:1047-1053.
2. 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.
3. Shulman GI. Cellular mechanisms of insulin resistance. J Clin Invest 2000; 106:171-176.
4. Roden M. How free fatty acids inhibit glucose utilization in human skeletal muscle. News Physiol Sci 2004; 19:92-96.
5. Kelley DE, Simoneau J-A. Impaired free fatty acid utilization by skeletal muscle in noninsulin dependent diabetes mellitus. J Clin Invest 1994; 94:2349-2356.
6. Kim JY, Hickner RC, Cortright RL, et al. Lipid oxidation is reduced in obese human skeletal muscle. Am J Physiol Endocrinol Metab 2000; 279:E1039-E1044.
7. Kelley DE, Mandarino LJ. Fuel selection in human skeletal muscle in insulin resistance: a reexamination. Diabetes 2000; 49:677-683.
8. Ukropcova B, McNeil M, Sereda O, et al. Dynamic changes in fat oxidation in human primary myocytes mirror metabolic characteristics of the donor. J Clin Invest 2005; 115:1934-1941.
9. Mootha VK, Lindgren CM, Eriksson KF, et al. PGC-1alpha-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat Genet 2003; 34:267-273.
10. Patti ME, Butte AJ, Crunkhorn S, et al. Coordinated reduction of genes of oxidative metabolism in humans with insulin resistance and diabetes: Potential role of PGC1 and NRF1. Proc Natl Acad Sci U S A 2003; 100:8466-8471.
11. Mensink M, Hesselink MK, Russell AP, Schaart G, Sels JP, Schrauwen P. Improved skeletal muscle oxidative enzyme activity and restoration of PGC-1alpha and PPARbeta/delta gene expression upon rosiglitazone treatment in obese patients with type 2 diabetes mellitus. Int J Obes (Lond) 2007; 31:1302-1310. Type 2 diabetic patients were treated for 8 weeks with the antidiabetic PPARγ agonist Rosiglitazone. Muscle biopsies revealed improved oxidative enzyme capacity and a restoration of the mRNA levels of PGC1a and PPARd, which before treatment were reduced by ∼ 60% when compared to control subjects.
12. Heilbronn LK, Gan SK, Turner N, et al. Markers of mitochondrial biogenesis and metabolism are lower in overweight and obese insulin-resistant subjects. J Clin Endocrinol Metab 2007; 92:1467-1473. The study shows that the reduction of markers of mitochondrial metabolism are reduced in the insulin resistant group, and that this is independent of age, body fat percentage and aerobic fitness.
13. Russell AP, Hesselink MK, Lo SK, Schrauwen P. Regulation of metabolic transcriptional co-activators and transcription factors with acute exercise. FASEB J 2005; 19:986-988.
14. Russell AP, Feilchenfeldt J, Schreiber S, et al. Endurance training in humans leads to fiber type-specific increases in levels of peroxisome proliferator-activated receptor-gamma coactivator-1 and peroxisome proliferator-activated receptor-alpha in skeletal muscle. Diabetes 2003; 52:2874-2881.
15. Sparks LM, Xie H, Koza RA, et al. A high-fat diet coordinately downregulates genes required for mitochondrial oxidative phosphorylation in skeletal muscle. Diabetes 2005; 54:1926-1933.
16. Hoeks J, Hesselink MK, Russell AP, et al. Peroxisome proliferator-activated receptor-gamma coactivator-1 and insulin resistance: acute effect of fatty acids. Diabetologia 2006; 49:2419-2426. Acute induction of insulin resistance by infusion of lipid emulsions in healthy humans under hyperinsulinemic euglycemic clamps conditions increased plasma FFA levels and decreased PGC1α gene expression. The study may provide an explanation for the reduced PGC1 α expression observed in type 2 diabetic patients.
17. Richardson DK, Kashyap S, Bajaj M, et al. Lipid infusion decreases the expression of nuclear encoded mitochondrial genes and increases the expression of extracellular matrix genes in human skeletal muscle. J Biol Chem 2005; 280:10290-10297.
18. Petersen KF, Befroy D, Dufour S, et al. Mitochondrial dysfunction in the elderly: possible role in insulin resistance. Science 2003; 300:1140-1142.
19. Petersen KF, Dufour S, Befroy D, et al. Impaired mitochondrial activity in the insulin-resistant offspring of patients with type 2 diabetes. N Engl J Med 2004; 350:664-671.
20. 13C MRS and found to be reduced to a similar extent as the earlier reported ATP synthase flux by ∼30% in offspring of diabetic patients.
21. Meyer RA. A linear model of muscle respiration explains monoexponential phosphocreatine changes. Am J Physiol 1988; 254:C548-C553.
22. Kemp GJ, Radda GK. Quantitative interpretation of bioenergetic data from 31P and 1H magnetic resonance spectroscopic studies of skeletal muscle: an analytical review. Magn Reson Q 1994; 10:43-63.
23. Sahlin K, Harris RC, Hultman E. Resynthesis of creatine phosphate in human muscle after exercise in relation to intramuscular pH and availability of oxygen. Scand J Clin Lab Invest 1979; 39:551-558.
24. Mattei JP, Bendahan D, Cozzone P. P-31 magnetic resonance spectroscopy. A tool for diagnostic purposes and pathophysiological insights in muscle diseases. Reumatismo 2004; 56:9-14.
25. Schrauwen-Hinderling VB, Kooi ME, Hesselink MK, et al. Impaired in vivo mitochondrial function but similar intramyocellular lipid content in patients with type 2 diabetes mellitus and BMI-matched control subjects. Diabetologia 2007; 50:113-120. An alternative MRS methodology to measure 'mitochondrial oxidative functionality' was applied in diabetic patients and revealed a reduction compared to BMI-matched controls. Muscular fat content was similar, suggesting an important role for mitochondrial dysfunction in the etiology of diabetes.
26. 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. Study reporting similar ATP synthase flux in diabetic subjects compared to BMIand age matched controls but a lower flux compared to younger controls. Insulin stimulation increased ATP synthesis only in the control groups. All three groups had similar IMCL content.
27. 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. [Epub ahead of print]
28. Brehm A, Krssak M, Schmid AI, et al. Increased lipid availability impairs insulin-stimulated ATP synthesis in human skeletal muscle. Diabetes 2006; 55:136-140. Elegant study combining the classic lipid-induced insulin resistance protocol and MRS. High fatty acid levels impair ATP synthesis in parallel with inducing insulin resistance.
29. Rabol R, Boushel R, Dela F. Mitochondrial oxidative function and type 2 diabetes. Appl Physiol Nutr Metab 2006; 31:675-683. Extensive overview of mitochondrial function and type 2 diabetes.
30. Boushel R, Gnaiger E, Schjerling P, et al. Patients with type 2 diabetes have normal mitochondrial function in skeletal muscle. Diabetologia 2007; 50:790-796. One of the two reports that determined intrinsic mitochondrial function in type 2 diabetic patients, in this case using permeabilized muscle fibers. After correction for mitochondrial density, normal mitochondrial function was observed in the diabetic state.
31. Mogensen M, Sahlin K, Fernstrom M, Glintborg D, Vind BF, Beck-Nielsen H, et al. Mitochondrial respiration is decreased in skeletal muscle of patients with type 2 diabetes. Diabetes 2007; 56:000-000. One of the two reports that determined intrinsic mitochondrial function in type 2 diabetic patients, in this case using isolated mitochondria. A modest but significant reduction in mitochondrial function was observed in the diabetic state. [Epub ahead of print]
32. Ritov VB, Menshikova EV, He J, et al. Deficiency of subsarcolemmal mitochondria in obesity and type 2 diabetes. Diabetes 2005; 54:8-14.
33. Morino K, Petersen KF, Dufour S, et al. Reduced mitochondrial density and increased IRS-1 serine phosphorylation in muscle of insulin-resistant offspring of type 2 diabetic parents. J Clin Invest 2005; 115:3587-3593.
34. Kelley DE, He J, Menshikova EV, Ritov VB. Dysfunction of mitochondria in human skeletal muscle in type 2 diabetes. Diabetes 2002; 51:2944-2950.
35. Schrauwen P, Hesselink MK. Oxidative capacity, lipotoxicity, and mitochondrial damage in type 2 diabetes. Diabetes 2004; 53:1412-1417.