Angiotensin II can directly induce mitochondrial dysfunction, decrease oxidative fibre number and induce atrophy in mouse hindlimb skeletal muscle

Experimental Physiology

Volumn 100, Issue 3, 2015, Pages 312-322

  Kadoguchi, Tomoyasu ^a   Kinugawa, Shintaro ^a   Takada, Shingo ^a   Fukushima, Arata ^a   Furihata, Takaaki ^a   Homma, Tsuneaki ^a   Masaki, Yoshihiro ^a   Mizushima, Wataru ^a   Nishikawa, Mikito ^a   Takahashi, Masashige ^a   Yokota, Takashi ^a   Matsushima, Shouji ^a   Okita, Koichi ^b   Tsutsui, Hiroyuki ^a  

^a HOKKAIDO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b HOKUSHO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOTENSIN II; ATROGIN 1; CASPASE 3; CITRATE SYNTHASE; MUSCLE RING FINGER 1 PROTEIN; OXIDOREDUCTASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); SUPEROXIDE; UBIQUINOL CYTOCHROME C REDUCTASE; ANGIOTENSIN I; DNA NUCLEOTIDYLEXOTRANSFERASE; MUSCLE PROTEIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BLOOD PRESSURE MEASUREMENT; BODY WEIGHT; CONTROLLED STUDY; DIASTOLIC BLOOD PRESSURE; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENZYME ACTIVITY; EXERCISE; HEART RATE; HEART WEIGHT; HINDLIMB; LEG MUSCLE; MALE; MEAN ARTERIAL PRESSURE; MOUSE; MUSCLE ATROPHY; MUSCLE CELL; NICK END LABELING; NONHUMAN; ORGAN WEIGHT; OSMOTIC MINIPUMP; OXIDATIVE STRESS; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; SYSTOLIC BLOOD PRESSURE; TREADMILL TEST; WEIGHT REDUCTION; ANIMAL; C57BL MOUSE; CHEMICALLY INDUCED; DRUG EFFECTS; METABOLISM; MITOCHONDRION; OXIDATION REDUCTION REACTION; SKELETAL MUSCLE;

ANGIOTENSIN I; ANGIOTENSIN II; ANIMALS; CASPASE 3; DNA NUCLEOTIDYLEXOTRANSFERASE; HINDLIMB; MALE; MICE; MICE, INBRED C57BL; MITOCHONDRIA; MUSCLE FIBERS, SKELETAL; MUSCLE PROTEINS; MUSCULAR ATROPHY; NADPH OXIDASE; OXIDATION-REDUCTION; RENIN-ANGIOTENSIN SYSTEM;

EID: 84923632042     PISSN: 09580670     EISSN: 1469445X     Source Type: Journal    
DOI: 10.1113/expphysiol.2014.084095     Document Type: Article

References (44)

1. Andersen JL (2003). Muscle fibre type adaptation in the elderly human muscle. Scand J Med Sci Sports 13, 40-47.
2. ATP channel Kir6.2 subunit content is higher in glycolytic than oxidative skeletal muscle fibers. Am J Physiol Regul Integr Comp Physiol 301, R916-R925.
3. Basso N, Cini R, Pietrelli A, Ferder L, Terragno NA & Inserra F (2007). Protective effect of long-term angiotensin II inhibition. Am J Physiol Heart Circ Physiol 293, H1351-H1358.
4. Blough ER & Linderman JK (2000). Lack of skeletal muscle hypertrophy in very aged male Fischer 344 × Brown Norway rats. J Appl Physiol 88, 1265-1270.
5. Brink M, Wellen J & Delafontaine P (1996). Angiotensin II causes weight loss and decreases circulating insulin-like growth factor I in rats through a pressor-independent mechanism. J Clin Invest 97, 2509-2516.
6. Burniston JG, Saini A, Tan LB & Goldspink DF (2005). Angiotensin II induces apoptosis in vivo in skeletal, as well as cardiac, muscle of the rat. Exp Physiol 90, 755-761.
7. Chabi B, Ljubicic V, Menzies KJ, Huang JH, Saleem A & Hood DA (2008). Mitochondrial function and apoptotic susceptibility in aging skeletal muscle. Aging Cell 7, 2-12.
8. Clavel S, Coldefy AS, Kurkdjian E, Salles J, Margaritis I & Derijard B (2006). Atrophy-related ubiquitin ligases, atrogin-1 and MuRF1 are up-regulated in aged rat Tibialis Anterior muscle. Mech Ageing Dev 127, 794-801.
9. Dai DF, Johnson SC, Villarin JJ, Chin MT, Nieves-Cintrón M, Chen T, Marcinek DJ, Dorn GW 2nd, Kang YJ, Prolla TA, Santana LF & Rabinovitch PS (2011). Mitochondrial oxidative stress mediates angiotensin II-induced cardiac hypertrophy and Gαq overexpression-induced heart failure. Circ Res 108, 837-846.
10. Drexler H, Riede U, Münzel T, König H, Funke E & Just H (1992). Alterations of skeletal muscle in chronic heart failure. Circulation 85, 1751-1759.
11. Dunant P, Larochelle N, Thirion C, Stucka R, Ursu D, Petrof BJ, Wolf E & Lochmüller H (2003). Expression of dystrophin driven by the 1.35-kb MCK promoter ameliorates muscular dystrophy in fast, but not in slow muscles of transgenic mdx mice. Mol Ther 8, 80-89.
12. 2 max. J Appl Physiol 65, 1147-1151.
13. Frontera WR, Hughes VA, Fielding RA, Fiatarone MA, Evans WJ & Roubenoff R (2000). Aging of skeletal muscle: a 12-yr longitudinal study. J Appl Physiol 88, 1321-1326.
14. Fukushima A, Kinugawa S, Takada S, Matsushima S, Sobirin MA, Ono T, Takahashi M, Suga T, Homma T, Masaki Y, Furihata T, Kadoguchi T, Yokota T, Okita K & Tsutsui H (2014). (Pro)renin receptor in skeletal muscle is involved in the development of insulin resistance associated with postinfarct heart failure in mice. Am J Physiol Endocrinol Metab 307, E503-E514.
15. Gielen S, Sandri M, Kozarez I, Kratzsch J, Teupser D, Thiery J, Erbs S, Mangner N, Lenk K, Hambrecht R, Schuler G & Adams V (2012). Exercise training attenuates MuRF-1 expression in the skeletal muscle of patients with chronic heart failure independent of age: the randomized Leipzig Exercise Intervention in Chronic Heart Failure and Aging catabolism study. Circulation 125, 2716-2727.
16. 1 receptor blockade improves metabolic function and provides renoprotection in Fischer-344 rats. Am J Physiol Heart Circ Physiol 293, H1327-H1333.
17. Harada K, Sugaya T, Murakami K, Yazaki Y & Komuro I (1999). Angiotensin II type 1A receptor knockout mice display less left ventricular remodeling and improved survival after myocardial infarction. Circulation 100, 2093-2099.
18. Hirabayashi K, Kinugawa S, Yokota T, Takada S, Fukushima A, Suga T, Takahashi M, Ono T, Morita N, Omokawa M, Harada K, Oyama-Manabe N, Shirato H, Matsushima S, Okita K & Tsutsui H (2014). Intramyocellular lipid is increased in the skeletal muscle of patients with dilated cardiomyopathy with lowered exercise capacity. Int J Cardiol 176, 1110-1112.
19. Houmard JA, Weidner ML, Gavigan KE, Tyndall GL, Hickey MS & Alshami A (1998). Fiber type and citrate synthase activity in the human gastrocnemius and vastus lateralis with aging. J Appl Physiol 85, 1337-1341.
20. Inoue N, Kinugawa S, Suga T, Yokota T, Hirabayashi K, Kuroda S, Okita K & Tsutsui H (2012). Angiotensin II-induced reduction in exercise capacity is associated with increased oxidative stress in skeletal muscle. Am J Physiol Heart Circ Physiol 302, H1202-H1210.
21. Kelley DE, He J, Menshikova EV & Ritov VB (2002). Dysfunction of mitochondria in human skeletal muscle in type 2 diabetes. Diabetes 51, 2944-2950.
22. Kerner J, Turkaly PJ, Minkler PE & Hoppel CL (2001). Aging skeletal muscle mitochondria in the rat: decreased uncoupling protein-3 content. Am J Physiol Endocrinol Metab 281, E1054-E1062.
23. Kinugawa S, Wang Z, Kaminski PM, Wolin MS, Edwards JG, Kaley G & Hintze TH (2005). Limited exercise capacity in heterozygous manganese superoxide dismutase gene-knockout mice: roles of superoxide anion and nitric oxide. Circulation 111, 1480-1486.
24. Li YP, Chen Y, Li AS & Reid MB (2003). Hydrogen peroxide stimulates ubiquitin-conjugating activity and expression of genes for specific E2 and E3 proteins in skeletal muscle myotubes. Am J Physiol Cell Physiol 285, C806-C812.
25. Libera LD, Zennaro R, Sandri M, Ambrosio GB & Vescovo G (1999). Apoptosis and atrophy in rat slow skeletal muscles in chronic heart failure. Am J Physiol Cell Physiol 277, C982-C986.
26. Mancini DM, Eisen H, Kussmaul W, Mull R, Edmunds LH Jr & Wilson JR (1991). Value of peak exercise oxygen consumption for optimal timing of cardiac transplantation in ambulatory patients with heart failure. Circulation 83, 778-786.
27. Maxwell AJ, Schauble E, Bernstein D & Cooke JP (1998). Limb blood flow during exercise is dependent on nitric oxide. Circulation 98, 369-374.
28. Odden MC, Whooley MA & Shlipak MG (2004). Association of chronic kidney disease and anemia with physical capacity: the heart and soul study. J Am Soc Nephrol 15, 2908-2915.
29. Ohta Y, Kinugawa S, Matsushima S, Ono T, Sobirin MA, Inoue N, Yokota T, Hirabayashi K & Tsutsui H (2011). Oxidative stress impairs insulin signal in skeletal muscle and causes insulin resistance in postinfarct heart failure. Am J Physiol Heart Circ Physiol 300, H1637-H1644.
30. Okita K, Kinugawa S & Tsutsui H (2013). Exercise intolerance in chronic heart failure - skeletal muscle dysfunction and potential therapies. Circ J 77, 293-300.
31. Ribisl PM, Lang W, Jaramillo SA, Jakicic JM, Stewart KJ, Bahnson J, Bright R, Curtis JF, Crow RS & Soberman JE; Look AHEAD Research Group (2007). Exercise capacity and cardiovascular/metabolic characteristics of overweight and obese individuals with type 2 diabetes: the Look AHEAD clinical trial. Diabetes Care 30, 2679-2684.
32. Rooyackers OE, Adey DB, Ades PA & Nair KS (1996). Effect of age on in vivo rates of mitochondrial protein synthesis in human skeletal muscle. Proc Natl Acad Sci USA 93, 15364-15369.
33. Schulze PC, Fang J, Kassik KA, Gannon J, Cupesi M, MacGillivray C, Lee RT & Rosenthal N (2005). Transgenic overexpression of locally acting insulin-like growth factor-1 inhibits ubiquitin-mediated muscle atrophy in chronic left-ventricular dysfunction. Circ Res 97, 418-426.
34. Song YH, Li Y, Du J, Mitch WE, Rosenthal N & Delafontaine P (2005). Muscle-specific expression of IGF-1 blocks angiotensin II-induced skeletal muscle wasting. J Clin Invest 115, 451-458.
35. Sriram S, Subramanian S, Juvvuna PK, Ge X, Lokireddy S, McFarlane CD, Wahli W, Kambadur R & Sharma M (2014). Myostatin augments muscle-specific ring finger protein-1 expression through an NF-κB independent mechanism in SMAD3 null muscle. Mol Endocrinol 28, 317-330.
36. Suga T, Kinugawa S, Takada S, Kadoguchi T, Fukushima A, Homma T, Masaki Y, Furihata T, Takahashi M, Sobirin MA, Ono T, Hirabayashi K, Yokota T, Tanaka S, Okita K & Tsutsui H (2014). Combination of exercise training and diet restriction normalizes limited exercise capacity and impaired skeletal muscle function in diet-induced diabetic mice. Endocrinology 155, 68-80.
37. Sullivan MJ, Green HJ & Cobb FR (1990). Skeletal muscle biochemistry and histology in ambulatory patients with long-term heart failure. Circulation 81, 518-527.
38. Takada S, Hirabayashi K, Kinugawa S, Yokota T, Matsushima S, Suga T, Kadoguchi T, Fukushima A, Homma T, Mizushima W, Masaki Y, Furihata T, Katsuyama R, Okita K & Tsutsui H (2014). Pioglitazone ameliorates the lowered exercise capacity and impaired mitochondrial function of the skeletal muscle in type 2 diabetic mice. Eur J Pharmacol 740, 690-696.
39. Takada S, Kinugawa S, Hirabayashi K, Suga T, Yokota T, Takahashi M, Fukushima A, Homma T, Ono T, Sobirin MA, Masaki Y, Mizushima W, Kadoguchi T, Okita K & Tsutsui H (2013). 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, 844-857.
40. Tamaki M, Miyashita K, Wakino S, Mitsuishi M, Hayashi K & Itoh H (2014). Chronic kidney disease reduces muscle mitochondria and exercise endurance and its exacerbation by dietary protein through inactivation of pyruvate dehydrogenase. Kidney Int 85, 1330-1339.
41. Wei Y, Sowers JR, Nistala R, Gong H, Uptergrove GM, Clark SE, Morris EM, Szary N, Manrique C & Stump CS (2006). Angiotensin II-induced NADPH oxidase activation impairs insulin signaling in skeletal muscle cells. J Biol Chem 281, 35137-35146.
42. Yokota T, Kinugawa S, Hirabayashi K, Matsushima S, Inoue N, Ohta Y, Hamaguchi S, Sobirin MA, Ono T, Suga T, Kuroda S, Tanaka S, Terasaki F, Okita K & Tsutsui H (2009). Oxidative stress in skeletal muscle impairs mitochondrial respiration and limits exercise capacity in type 2 diabetic mice. Am J Physiol Heart Circ Physiol 297, H1069-H1077.
43. Yoshida T, Semprun-Prieto L, Sukhanov S & Delafontaine P (2010). IGF-1 prevents ANG II-induced skeletal muscle atrophy via Akt- and Foxo-dependent inhibition of the ubiquitin ligase atrogin-1 expression. Am J Physiol Heart Circ Physiol 298, H1565-H1570.
44. Zoll J, Monassier L, Garnier A, N'Guessan B, Mettauer B, Veksler V, Piquard F, Ventura-Clapier R & Geny B (2006). ACE inhibition prevents myocardial infarction-induced skeletal muscle mitochondrial dysfunction. J Appl Physiol 101, 385-391.