Pioglitazone ameliorates the lowered exercise capacity and impaired mitochondrial function of the skeletal muscle in type 2 diabetic mice

European Journal of Pharmacology

Volumn 740, Issue , 2014, Pages 690-696

  Takada, Shingo ^a,b   Hirabayashi, Kagami ^a   Kinugawa, Shintaro ^a   Yokota, Takashi ^a   Matsushima, Shouji ^a   Suga, Tadashi ^c   Kadoguchi, Tomoyasu ^a   Fukushima, Arata ^a   Homma, Tsuneaki ^a   Mizushima, Wataru ^a   Masaki, Yoshihiro ^a   Furihata, Takaaki ^a   Katsuyama, Ryoichi ^a   Okita, Koichi ^d   Tsutsui, Hiroyuki ^a  

^a HOKKAIDO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b JAPAN SOCIETY FOR THE PROMOTION OF SCIENCE   (Japan)

^c RITSUMEIKAN UNIVERSITY   (Japan)

^d HOKUSHO UNIVERSITY   (Japan)

Author keywords

Diabetes; Insulin resistance; Mitochondria; Muscle; Oxidative stress

Indexed keywords

ADENOSINE DIPHOSPHATE; CITRATE SYNTHASE; CYTOCHROME C OXIDASE; GLUCOSE; INSULIN; PIOGLITAZONE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SUCCINATE DEHYDROGENASE (UBIQUINONE); UBIQUINOL CYTOCHROME C REDUCTASE; 2,4 THIAZOLIDINEDIONE DERIVATIVE; AMILORIDE; ANTIDIABETIC AGENT; DIURETIC AGENT; GLUCOSE BLOOD LEVEL;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BODY WEIGHT; CONTROLLED STUDY; ENZYME ACTIVITY; EXERCISE; FLUID RETENTION; GLUCOSE BLOOD LEVEL; INSULIN BLOOD LEVEL; INSULIN RESISTANCE; LIPID DIET; MALE; MITOCHONDRIAL RESPIRATION; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OXIDATIVE STRESS; OXYGEN CONSUMPTION; SKELETAL MUSCLE; TREADMILL TEST; ANALYSIS; ANIMAL; C57BL MOUSE; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 2; DRUG EFFECTS; HINDLIMB; METABOLISM; MITOCHONDRION;

AMILORIDE; ANIMALS; BLOOD GLUCOSE; BODY WEIGHT; CITRATE (SI)-SYNTHASE; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 2; DIET, HIGH-FAT; DIURETICS; HINDLIMB; HYPOGLYCEMIC AGENTS; MALE; MICE; MICE, INBRED C57BL; MITOCHONDRIA; MUSCLE, SKELETAL; NADPH OXIDASE; OXYGEN CONSUMPTION; PHYSICAL CONDITIONING, ANIMAL; THIAZOLIDINEDIONES;

EID: 84919400464     PISSN: 00142999     EISSN: 18790712     Source Type: Journal    
DOI: 10.1016/j.ejphar.2014.06.008     Document Type: Article

References (37)

1. C. Bonnard, A. Durand, S. Peyrol, E. Chanseaume, M.A. Chauvin, B. Morio, H. Vidal, and J. Rieusset Mitochondrial dysfunction results from oxidative stress in the skeletal muscle of diet-induced insulin-resistant mice J. Clin. Invest. 118 2008 789 800
2. L.L. Chen, H.H. Zhang, J. Zheng, X. Hu, W. Kong, D. Hu, S.X. Wang, and P. Zhang Resveratrol attenuates high-fat diet-induced insulin resistance by influencing skeletal muscle lipid transport and subsarcolemmal mitochondrial beta-oxidation Metabolism 60 2011 1598 1609
3. N. de Las Heras, M. Valero-Munoz, S. Ballesteros, A. Gomez-Hernandez, B. Martin-Fernandez, J. Blanco-Rivero, V. Cachofeiro, M. Benito, G. Balfagon, and V. Lahera Factors involved in rosuvastatin induction of insulin sensitization in rats fed a high fat diet Nutr., Metab. Cardiovasc. Dis 23 2013 1107 1114
4. C. Escande, C.C. Chini, V. Nin, K.M. Dykhouse, C.M. Novak, J. Levine, J. van Deursen, G.J. Gores, J. Chen, Z. Lou, and E.N. Chini Deleted in breast cancer-1 regulates SIRT1 activity and contributes to high-fat diet-induced liver steatosis in mice J. Clin. Investig. 120 2010 545 558
5. P. Garcia-Roves, J.M. Huss, D.H. Han, C.R. Hancock, E. Iglesias-Gutierrez, M. Chen, and J.O. Holloszy Raising plasma fatty acid concentration induces increased biogenesis of mitochondria in skeletal muscle Proc. Natl. Acad. Sci. U.S.A 104 2007 10709 10713
6. Y. Guan, C. Hao, D.R. Cha, R. Rao, W. Lu, D.E. Kohan, M.A. Magnuson, R. Redha, Y. Zhang, and M.D. Breyer Thiazolidinediones expand body fluid volume through PPARgamma stimulation of ENaC-mediated renal salt absorption Nat. Med. 11 2005 861 866
7. C.R. Hancock, D.H. Han, M. Chen, S. Terada, T. Yasuda, D.C. Wright, and J.O. Holloszy High-fat diets cause insulin resistance despite an increase in muscle mitochondria Proc. Natl. Acad. Sci. U.S.A 105 2008 7815 7820
8. S. Hasegawa, M. Nakano, Y. Taniguchi, S. Imai, K. Murata, and T. Suzuki Effects of Na(+)-H+ exchange blocker amiloride on left ventricular remodeling after anterior myocardial infarction in rats Cardiovasc. Drugs Ther. 9 1995 823 826
9. B.A. Houssay, and C. Martinez Experimental Diabetes and Diet Science 105 1947 548 549
10. W.H. Hsu, T.H. Chen, B.H. Lee, Y.W. Hsu, and T.M. Pan Monascin and ankaflavin act as natural AMPK activators with PPARalpha agonist activity to down-regulate nonalcoholic steatohepatitis in high-fat diet-fed C57BL/6 mice Food Chem. Toxicol. 64 2014 94 103
11. N. Inoue, S. Kinugawa, T. Suga, T. Yokota, K. Hirabayashi, S. Kuroda, K. Okita, and H. Tsutsui Angiotensin II-induced reduction in exercise capacity is associated with increased oxidative stress in skeletal muscle Am. J. Physiol. Heart Circ. Physiol. 302 2012 H1202 H1210
12. H. Ishida, M. Takizawa, S. Ozawa, Y. Nakamichi, S. Yamaguchi, H. Katsuta, T. Tanaka, M. Maruyama, H. Katahira, K. Yoshimoto, E. Itagaki, and S. Nagamatsu Pioglitazone improves insulin secretory capacity and prevents the loss of beta-cell mass in obese diabetic db/db mice: possible protection of beta cells from oxidative stress Metabolism 53 2004 488 494
13. M.S. Islam, and Loots du T. Experimental rodent models of type 2 diabetes: a review Methods Find. Exp. Clin. Pharmacol. 31 2009 249 261
14. M. Iwabu, T. Yamauchi, M. Okada-Iwabu, K. Sato, T. Nakagawa, M. Funata, M. Yamaguchi, S. Namiki, R. Nakayama, M. Tabata, H. Ogata, N. Kubota, I. Takamoto, Y.K. Hayashi, N. Yamauchi, H. Waki, M. Fukayama, I. Nishino, K. Tokuyama, K. Ueki, Y. Oike, S. Ishii, K. Hirose, T. Shimizu, K. Touhara, and T. Kadowaki Adiponectin and AdipoR1 regulate PGC-1alpha and mitochondria by Ca(2+) and AMPK/SIRT1 Nature 464 2010 1313 1319
15. S. Kinugawa, Z. Wang, P.M. Kaminski, M.S. Wolin, J.G. Edwards, G. Kaley, and T.H. Hintze Limited exercise capacity in heterozygous manganese superoxide dismutase gene-knockout mice: roles of superoxide anion and nitric oxide Circulation 111 2005 1480 1486
16. H. Kumagai, N. Kubota, T. Kubota, T. Takahashi, M. Inoue, T. Kawai, K. Iwayama, M. Moroi, K. Sugi, and T. Kadowaki Combined treatment with low-dose pioglitazone and beraprost sodium improves glucose intolerance without causing body weight gain Diabetol. Int. 4 2013 226 232
17. S. Lee, H. Zhang, J. Chen, K.C. Dellsperger, M.A. Hill, and C. Zhang Adiponectin abates diabetes-induced endothelial dysfunction by suppressing oxidative stress, adhesion molecules, and inflammation in type 2 diabetic mice Am. J. Physiol. Heart Circ. Physiol. 303 2012 H106 H115
18. Z. Lin, H. Tian, K.S. Lam, S. Lin, R.C. Hoo, M. Konishi, N. Itoh, Y. Wang, S.R. Bornstein, A. Xu, and X. Li Adiponectin mediates the metabolic effects of FGF21 on glucose homeostasis and insulin sensitivity in mice Cell Metab. 17 2013 779 789
19. Y. Matsui, Y. Hirasawa, T. Sugiura, T. Toyoshi, K. Kyuki, and M. Ito Metformin reduces body weight gain and improves glucose intolerance in high-fat diet-fed C57BL/6J mice Biol. Pharm. Bull. 33 2010 963 970
20. M. Mogensen, K. Sahlin, M. Fernström, D. Glintborg, B.F. Vind, H. Beck-Nielsen, and K. Højlund Mitochondrial respiration is decreased in skeletal muscle of patients with type 2 diabetes Diabetes 56 2007 1592 1599
21. K. Okita, K. Yonezawa, H. Nishijima, A. Hanada, M. Ohtsubo, T. Kohya, T. Murakami, and A. Kitabatake Skeletal muscle metabolism limits exercise capacity in patients with chronic heart failure Circulation 98 1998 1886 1891
22. N.L. Price, A.P. Gomes, A.J. Ling, F.V. Duarte, A. Martin-Montalvo, B.J. North, B. Agarwal, L. Ye, G. Ramadori, J.S. Teodoro, B.P. Hubbard, A.T. Varela, J.G. Davis, B. Varamini, A. Hafner, R. Moaddel, A.P. Rolo, R. Coppari, C.M. Palmeira, R. de Cabo, J.A. Baur, and D.A. Sinclair SIRT1 is required for AMPK activation and the beneficial effects of resveratrol on mitochondrial function Cell Metab. 15 2012 675 690
23. J.G. Regensteiner, T.A. Bauer, and J.E. Reusch Rosiglitazone improves exercise capacity in individuals with type 2 diabetes Diabetes Care 28 2005 2877 2883
24. C.K. Roberts, R.J. Barnard, R.K. Sindhu, M. Jurczak, A. Ehdaie, and N.D. Vaziri Oxidative stress and dysregulation of NAD(P)H oxidase and antioxidant enzymes in diet-induced metabolic syndrome Metabolism 55 2006 928 934
25. Y. Safwat, N. Yassin, M. Gamal El Din, and L. Kassem Modulation of skeletal muscle performance and SERCA by exercise and adiponectin gene therapy in insulin-resistant rat DNA Cell Biol. 32 2013 378 385
26. G. Schernthaner, C.J. Currie, and G.H. Schernthaner Do we still need pioglitazone for the treatment of type 2 diabetes? A risk-benefit critique in 2013 Diabetes Care 36 Suppl 2 2013 S155 S161
27. M. Silvennoinen, R. Rinnankoski-Tuikka, M. Vuento, J.J. Hulmi, S. Torvinen, M. Lehti, R. Kivela, and H. Kainulainen High-fat feeding induces angiogenesis in skeletal muscle and activates angiogenic pathways in capillaries Angiogenesis 16 2013 297 307
28. T. Suga, S. Kinugawa, S. Takada, T. Kadoguchi, A. Fukushima, T. Homma, Y. Masaki, T. Furihata, M. Takahashi, M.A. Sobirin, T. Ono, K. Hirabayashi, T. Yokota, S. Tanaka, K. Okita, and H. Tsutsui Combination of exercise training and diet restriction normalizes limited exercise capacity and impaired skeletal muscle function in diet-induced diabetic mice Endocrinology 155 2014 68 80
29. S. Takada, S. Kinugawa, K. Hirabayashi, T. Suga, T. Yokota, M. Takahashi, A. Fukushima, T. Homma, T. Ono, M.A. Sobirin, Y. Masaki, W. Mizushima, T. Kadoguchi, K. Okita, and H. Tsutsui Angiotensin II receptor blocker improves the lowered exercise capacity and impaired mitochondrial function of the skeletal muscle in type 2 diabetic mice J. Appl. Physiol. 114 2013 844 857
30. N. Turner, C.R. Bruce, S.M. Beale, K.L. Hoehn, T. So, M.S. Rolph, and G.J. Cooney 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 2007 2085 2092
31. M. Wei, L.W. Gibbons, J.B. Kampert, M.Z. Nichaman, and S.N. Blair Low cardiorespiratory fitness and physical inactivity as predictors of mortality in men with type 2 diabetes Ann. Intern. Med. 132 2000 605 611
32. M. Yang, and A.M. Kahn Insulin-stimulated NADH/NAD+ redox state increases NAD(P)H oxidase activity in cultured rat vascular smooth muscle cells Am. J. Hypertens. 19 2006 587 592
33. T. Yokota, S. Kinugawa, K. Hirabayashi, S. Matsushima, N. Inoue, Y. Ohta, S. Hamaguchi, M.A. Sobirin, T. Ono, T. Suga, S. Kuroda, S. Tanaka, F. Terasaki, K. Okita, and H. Tsutsui Oxidative stress in skeletal muscle impairs mitochondrial respiration and limits exercise capacity in type 2 diabetic mice Am. J. Physiol. Heart Circ. Physiol. 297 2009 H1069 H1077
34. T. Yokota, S. Kinugawa, K. Okita, K. Hirabayashi, T. Suga, M. Hattori, Y. Nakagawa, N. Oyama-Manabe, H. Shirato, and H. Tsutsui Lower aerobic capacity was associated with abnormal intramuscular energetics in patients with metabolic syndrome Hypertens. Res. 34 2011 1029 1034
35. T. Yokota, S. Kinugawa, M. Yamato, K. Hirabayashi, T. Suga, S. Takada, K. Harada, N. Morita, N. Oyama-Manabe, Y. Kikuchi, K. Okita, and H. Tsutsui Systemic oxidative stress is associated with lower aerobic capacity and impaired skeletal muscle energy metabolism in patients with metabolic syndrome Diabetes Care 36 2013 1341 1346
36. H. Zhang, Y. Park, and C. Zhang Coronary and aortic endothelial function affected by feedback between adiponectin and tumor necrosis factor alpha in type 2 diabetic mice Arterioscler. Thromb. Vasc. Biol. 30 2010 2156 2163
37. Y. Zhou, H. Huang, H.H. Chang, J. Du, J.F. Wu, C.Y. Wang, and M.H. Wang Induction of renal 20-hydroxyeicosatetraenoic acid by clofibrate attenuates high-fat diet-induced hypertension in rats J. Pharmacol. Exp. Ther. 317 2006 11 18