Mitochondrial fission contributes to mitochondrial dysfunction and insulin resistance in skeletal muscle

Molecular and Cellular Biology

Volumn 32, Issue 2, 2012, Pages 309-319

  Jheng, Huei Fen ^a   Tsai, Pei Jane ^a   Guo, Syue Maio ^a   Kuo, Li Hua ^a   Chang, Cherng Shyang ^a   Su, Ih Jen ^a,b   Chang, Chuang Rung ^a   Tsaia, Yau Sheng ^a,c  

^a NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^b NATIONAL HEALTH RESEARCH INSTITUTES   (Taiwan)

^c NATIONAL TSING HUA UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; DYNAMIN RELATED PROTEIN 1; ESTROGEN RELATED RECEPTOR ALPHA; MITOCHONDRIAL DNA; MITOCHONDRIAL PROTEIN; MITOCHONDRIAL TRANSCRIPTION FACTOR A; MITOGEN ACTIVATED PROTEIN KINASE; PALMITIC ACID; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; REACTIVE OXYGEN METABOLITE; SINGLE STRANDED DNA BINDING PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CALORIC INTAKE; CELL DAMAGE; CELL DIVISION; CELL MEMBRANE DEPOLARIZATION; CELL STRUCTURE; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENERGY YIELD; ENZYME INHIBITION; GLUCOSE TRANSPORT; IN VITRO STUDY; IN VIVO STUDY; INSULIN RESISTANCE; INSULIN SENSITIVITY; MALE; MITOCHONDRIAL FISSION; MITOCHONDRION; MOUSE; MUSCLE METABOLISM; NONHUMAN; OBESITY; ORAL GLUCOSE TOLERANCE TEST; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SKELETAL MUSCLE;

ANIMALS; CELL LINE; DYNAMINS; FATTY ACIDS; GLUCOSE; INSULIN RESISTANCE; MICE; MITOCHONDRIA, MUSCLE; MITOCHONDRIAL PROTEINS; MUSCLE, SKELETAL; OBESITY; PALMITIC ACID; PROTEIN KINASES; REACTIVE OXYGEN SPECIES;

EID: 84863011641     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.05603-11     Document Type: Article

References (48)

1. Abdul-Ghani MA, et al. 2008. Deleterious action of FA metabolites on ATP synthesis: possible link between lipotoxicity, mitochondrial dysfunc-tion, and insulin resistance. Am. J. Physiol. Endocrinol. Metab. 295: E678-E685.
2. Bonen A, et al. 2004. Triacylglycerol accumulation in human obesity and type 2 diabetes is associated with increased rates of skeletal muscle fatty acid transport and increased sarcolemmal FAT/CD36. FASEB J. 18: 1144-1146.
3. Bonnard C, et al. 2008. Mitochondrial dysfunction results from oxidative stress in the skeletal muscle of diet-induced insulin-resistant mice. J. Clin. Invest. 118:789-800.
4. Brands M, et al. 2011. Short-term increase of plasma free fatty acids does not interfere with intrinsic mitochondrial function in healthy young men. Metabolism 60:1398 -1405.
5. Brooks C, Wei Q, Cho SG, Dong Z. 2009. Regulation of mitochondrial dynamics in acute kidney injury in cell culture and rodent models. J. Clin. Invest. 119:1275-1285.
6. Cartoni R, et al. 2005. Mitofusins 1/2 and ERRalpha expression are increased in human skeletal muscle after physical exercise. J. Physiol. 567: 349-358.
7. Cassidy-Stone A, et al. 2008. Chemical inhibition of the mitochondrial division dynamin reveals its role in Bax/Bak-dependent mitochondrial outer membrane permeabilization. Dev. Cell 14:193-204.
8. Chan DC. 2006. Mitochondrial fusion and fission in mammals. Annu. Rev. Cell Dev. Biol. 22:79 -99.
9. Chang CR, Blackstone C. 2007. Cyclic AMP-dependent protein kinase phosphorylation of Drp1 regulates its GTPase activity and mitochondrial morphology. J. Biol. Chem. 282:21583-21587.
10. Chavez AO, et al. 2010. Effect of short-term free fatty acids elevation on mitochondrial function in skeletal muscle of healthy individuals. J. Clin. Endocrinol. Metab. 95:422- 429.
11. Chen H, Chomyn A, Chan DC. 2005. Disruption of fusion results in mitochondrial heterogeneity and dysfunction. J. Biol. Chem. 280: 26185-26192.
12. De Fea K, Roth RA. 1997. Modulation of insulin receptor substrate-1 tyrosine phosphorylation and function by mitogen-activated protein kinase. J. Biol. Chem. 272:31400 -31406.
13. Detmer SA, Chan DC. 2007. Functions and dysfunctions of mitochondrial dynamics. Nat. Rev. Mol. Cell Biol. 8:870-879.
14. Edwards JL, et al. 2010. Diabetes regulates mitochondrial biogenesis and fission in mouse neurons. Diabetologia 53:160 -169.
15. Evans JL, Goldfine ID, Maddux BA, Grodsky GM. 2003. Are oxidative stress-activated signaling pathways mediators of insulin resistance and beta-cell dysfunction? Diabetes 52:1- 8.
16. Frank S, et al. 2001. The role of dynamin-related protein 1, a mediator of mitochondrial fission, in apoptosis. Dev. Cell 1:515-525.
17. Fraser DA, Thoen J, Rustan AC, Forre O, Kjeldsen-Kragh J. 1999. Changes in plasma free fatty acid concentrations in rheumatoid arthritis patients during fasting and their effects upon T-lymphocyte proliferation. Rheumatology (Oxford) 38:948 -952.
18. Guilherme A, Virbasius JV, Puri V, Czech MP. 2008. Adipocyte dysfunctions linking obesity to insulin resistance and type 2 diabetes. Nat. Rev. Mol. Cell Biol. 9:367-377.
19. Hancock CR, et al. 2008. High-fat diets cause insulin resistance despite an increase in muscle mitochondria. Proc. Natl. Acad. Sci. U. S. A. 105: 7815-7820.
20. Hegarty BD, Cooney GJ, Kraegen EW, Furler SM. 2002. Increased efficiency of fatty acid uptake contributes to lipid accumulation in skeletal muscle of high fat-fed insulin-resistant rats. Diabetes 51:1477-1484.
21. Hirabara SM, Curi R, Maechler P. 2010. Saturated fatty acid-induced insulin resistance is associated with mitochondrial dysfunction in skeletal muscle cells. J. Cell. Physiol. 222:187-194.
22. Kelley DE, He J, Menshikova EV, Ritov VB. 2002. Dysfunction of mitochondria in human skeletal muscle in type 2 diabetes. Diabetes 51: 2944-2950.
23. Kuda O, et al. 2009. n-3 fatty acids and rosiglitazone improve insulin sensitivity through additive stimulatory effects on muscle glycogen synthesis in mice fed a high-fat diet. Diabetologia 52:941-951.
24. Lowell BB, Shulman GI. 2005. Mitochondrial dysfunction and type 2 diabetes. Science 307:384 -387.
25. Maddux BA, et al. 2001. Protection against oxidative stress-induced insulin resistance in rat L6 muscle cells by micromolar concentrations of alpha-lipoic acid. Diabetes 50:404-410.
26. Makino A, Scott BT, Dillmann WH. 2010. Mitochondrial fragmentation and superoxide anion production in coronary endothelial cells from a mouse model of type 1 diabetes. Diabetologia 53:1783-1794.
27. McGarry JD. 2002. Banting lecture 2001: dysregulation of fatty acid metabolism in the etiology of type 2 diabetes. Diabetes 51:7-18.
28. Men X, et al. 2009. Dynamin-related protein 1 mediates high glucose induced pancreatic beta cell apoptosis. Int. J. Biochem. Cell Biol. 41: 879-890.
29. Molina AJ, et al. 2009. Mitochondrial networking protects beta-cells from nutrient-induced apoptosis. Diabetes 58:2303-2315.
30. Montell E, et al. 2001. DAG accumulation from saturated fatty acids desensitizes insulin stimulation of glucose uptake in muscle cells. Am. J. Physiol. Endocrinol. Metab. 280:E229 -E237.
31. Muoio DM, Newgard CB. 2008. Mechanisms of disease: molecular and metabolic mechanisms of insulin resistance and beta-cell failure in type 2 diabetes. Nat. Rev. Mol. Cell Biol. 9:193-205.
32. Ong SB, et al. 2010. Inhibiting mitochondrial fission protects the heart against ischemia/reperfusion injury. Circulation 121:2012-2022.
33. Parone PA, et al. 2008. Preventing mitochondrial fission impairs mitochondrial function and leads to loss of mitochondrial DNA. PLoS One 3:e3257.
34. Petersen KF, Dufour S, Befroy D, Garcia R, Shulman GI. 2004. Impaired mitochondrial activity in the insulin-resistant offspring of patients with type 2 diabetes. N. Engl. J. Med. 350:664-671.
35. Powell DJ, Turban S, Gray A, Hajduch E, Hundal HS. 2004. Intracellular ceramide synthesis and protein kinase Czeta activation play an essential role in palmitate-induced insulin resistance in rat L6 skeletal muscle cells. Biochem. J. 382:619-629.
36. Ritov VB, et al. 2005. Deficiency of subsarcolemmal mitochondria in obesity and type 2 diabetes. Diabetes 54:8 -14.
37. Sabin MA, et al. 2007. Fatty acid-induced defects in insulin signalling, in myotubes derived from children, are related to ceramide production from palmitate rather than the accumulation of intramyocellular lipid. J. Cell. Physiol. 211:244 -252.
38. Schenk S, Saberi M, Olefsky JM. 2008. Insulin sensitivity: modulation by nutrients and inflammation. J. Clin. Invest. 118:2992-3002.
39. Simoneau JA, Veerkamp JH, Turcotte LP, Kelley DE. 1999. Markers of capacity to utilize fatty acids in human skeletal muscle: relation to insulin resistance and obesity and effects of weight loss. FASEB J. 13:2051-2060.
40. Sparks LM, et al. 2005. A high-fat diet coordinately downregulates genes required for mitochondrial oxidative phosphorylation in skeletal muscle. Diabetes 54:1926 -1933.
41. Suen DF, Norris KL, Youle RJ. 2008. Mitochondrial dynamics and apoptosis. Genes Dev. 22:1577-1590.
42. Thyfault JP, et al. 2004. Impaired plasma fatty acid oxidation in extremely obese women. Am. J. Physiol. Endocrinol. Metab. 287:E1076 -E1081.
43. Turner N, et al. 2007. 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 56:2085-2092.
44. Uusitupa M, et al. 1994. Effects of two high-fat diets with different fatty acid compositions on glucose and lipid metabolism in healthy young women. Am. J. Clin. Nutr. 59:1310 -1316.
45. Vincent AM, et al. 2010. Mitochondrial biogenesis and fission in axons in cell culture and animal models of diabetic neuropathy. Acta Neuropathol. 120:477- 489.
46. Wellen KE, Thompson CB. 2010. Cellular metabolic stress: considering how cells respond to nutrient excess. Mol. Cell 40:323-332.
47. Yang ZH, Miyahara H, Mori T, Doisaki N, Hatanaka A. 2011. Beneficial effects of dietary fish-oil-derived monounsaturated fatty acids on metabolic syndrome risk factors and insulin resistance in mice. J. Agric. Food Chem. 59:7482-7489.
48. Yu T, Sheu SS, Robotham JL, Yoon Y. 2008. Mitochondrial fission mediates high glucose-induced cell death through elevated production of reactive oxygen species. Cardiovasc. Res. 79:341-351.