Effect of exercise training on skeletal muscle SIRT1 and PGC-1α expression levels in rats of different age

International Journal of Medical Sciences

Volumn 13, Issue 4, 2016, Pages 260-270

  Huang, Chi Chang ^a   Wang, Ting ^b   Tung, Yu Tang ^a   Lin, Wan Teng ^b  

^a NATIONAL TAIWAN SPORT UNIVERSITY   (Taiwan)

^b TUNGHAI UNIVERSITY   (Taiwan)

Author keywords

Aging; Exercise training; PGC 1 ; SIRT1; Skeletal muscle

Indexed keywords

ADENYLATE KINASE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; SIRTUIN 1; TRANSCRIPTION FACTOR FKHRL1; FOXO3A PROTEIN, RAT; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; PPARGC1A PROTEIN, RAT; SIRT1 PROTEIN, RAT;

ADULT; AGE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CONTROLLED STUDY; EPIDIDYMIS FAT; FEMALE; GASTROCNEMIUS MUSCLE; MALE; MUSCLE CELL; MUSCLE MASS; NONHUMAN; PHYSICAL ACTIVITY; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; RAT; SEDENTARY LIFESTYLE; SIGNAL TRANSDUCTION; SOLEUS MUSCLE; SWIMMING; UPREGULATION; AGING; ANIMAL; BIOSYNTHESIS; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; PHYSIOLOGY; SKELETAL MUSCLE; SPRAGUE DAWLEY RAT;

AGING; AMP-ACTIVATED PROTEIN KINASES; ANIMALS; FORKHEAD BOX PROTEIN O3; GENE EXPRESSION REGULATION; HUMANS; MUSCLE, SKELETAL; PEROXISOME PROLIFERATOR-ACTIVATED RECEPTOR GAMMA COACTIVATOR 1-ALPHA; PHYSICAL CONDITIONING, ANIMAL; RATS; RATS, SPRAGUE-DAWLEY; SIRTUIN 1; SWIMMING;

EID: 84962044930     PISSN: 14491907     EISSN: None     Source Type: Journal    
DOI: 10.7150/ijms.14586     Document Type: Article

References (50)

1. De Angelis K, Schaan BD, Maeda CY, Dall'Ago P, Wichi RB, Irigoyen MC. Cardiovascular control in experimental diabetes. Braz J Med Biol Res. 2002; 35:1091-1100.
2. Ghosh S, Pulinilkunnil T, Yuen G, Kewalramani G, An D, Qi D, Abrahani A, Rodrigues B. Cardiomyocyte apoptosis induced by short-term diabetes requires mitochondrial GSH depletion. Am J Physiol Heart Circ Physiol. 2005; 289:H768-H776.
3. Hu FB, Manson JE, Stampfer MJ, Colditz G, Liu S, Solomon CG, Willett WC. Diet, lifestyle, and the risk of type 2 diabetes mellitus in women. N Engl J Med. 2001; 345:790-797.
4. Anitha V, Asha Devi S. Age-related responses of right ventricle in swim-trained rats: changes in lactate and pyruvate contents and lactate dehydrogenase activity. Mech Ageing Dev. 1996; 90:91-102.
5. Stampfer MJ, Hu FB, Manson JE, Rimm EB, Willett WC. Primary prevention of coronary heart disease in women through diet and lifestyle. N Engl J Med. 2000; 343:16-22.
6. Tan N, Morimoto K, Sugiura T, Morimoto A, Murakami N. The effects of running training on the blood glucose and lactate in rats during rest and swimming. Phvsiol Behav. 1992; 51:927-931.
7. Bhagavathi R, Devi SA. Interaction of exercise and age on substrates of carbohydrate metabolism. Indian J Esp Biol. 1993; 31:72-75.
8. Kramer K, Dijkstra H, Bast A. Control of physical exercise of rats in a swimming basin. Physiol Behav. 1993; 53:271-276.
9. Ravi Kiran T, Subramanyam MV, Asha Devi S. Swim exercise training and adaptations in the antioxidant defense system of myocardium of old rats: relationship to swim intensity and duration. Comp. Biochem Physiol B Biochem Mol Biol. 2004; 137:187-196.
10. Frazzi R, Valli R, Tamagnini I, Casali B, Latruffe N, Merli F. Resveratrol-mediated apoptosis of Hodgkin lymphoma cells involves SIRT1 inhibition and FOXO3a hyperacetylation. Int J Cancer. 2013; 132:1013-1021.
11. Lakshminarasimhan M, Rauth D, Schutkowski M, Steegborn C. Sirt1 activation by resveratrol is substrate sequenceselective. Aging (Albany NY). 2013; 5:151-154.
12. Li T, Zhang J, Feng J, Li Q, Wu L, Ye Q, Sun J, Lin Y, Zhang M, Huang R, Cheng J, Cao Y, Xiang G, Zhang J, Wu Q. Resveratrol reduces acute lung injury in a LPS? Induced sepsis mouse model via activation of Sirt1. Mol Med Rep. 2013; 7:1889-1895.
13. Oellerich MF, Potente M. FOXOs and sirtuins in vascular growth, maintenance, and aging. Circ Res. 2012; 110:1238-1251.
14. Zarzuelo MJ, López-Sepúlveda R, Sánchez M, Romero M, Gómez-Guzmán M, Ungvary Z, Pérez-Vizcaíno F, Jiménez R, Duarte J. SIRT1 inhibits NADPH oxidase activation and protects endothelial function in the rat aorta: implications for vascular aging. Biochem Pharmacol. 2013; 85:1288-1296.
15. Ferrer MD, Tauler P, Sureda A, Tur JA, Pons A. Antioxidant regulatory mechanisms in neutrophils and lymphocytes after intense exercise. J Sports Sci. 2009; 27:49-58.
16. Lanza IR, Short DK, Short KR, Raghavakaimal S, Basu R, Joyner MJ, McConnell JP, Nair KS. Endurance exercise as a countermeasure for aging. Diabetes. 2008; 57:2933-2942.
17. Palacios OM, Carmona JJ, Michan S, Chen KY, Manabe Y, Ward JL 3rd, Goodyear LJ, Tong Q. Diet and exercise signals regulate SIRT3 and activate AMPK and PGC-1α in skeletal muscle. Aging (Albany NY). 2009; 1:771-783.
18. Oscai LB, Spirakis CN, Wolff CA, Beck RJ. Effects of exercise and of food restriction on adipose tissue cellularity. J Lipid Res. 1972; 13:588-592.
19. Hirsch J, Han PW. Cellularity of rat adipose tissue: effects of growth, starvation, and obesity. J Lipid Res. 1969; 10:77-82.
20. Johnson PR, Zucker LM, Cruce JA, Hirsch J. Cellularity of adipose depots in the genetically obese Zucker rat. J Lipid Res. 1971; 12:706-714.
21. Kraemer WJ, Fleck SJ, Evans WJ. Strength and power training: physiological mechanisms of adaptation. In: Exercise and Sport Sciences Reviews, edited by Holloszy JO, Baltimore MD. Williams andWilkins. 1996: 363-397.
22. Viboolvorakul S, Niimi H, Wongeak-in N, Eksakulkla S, Patumraj S. Increased capillary vascularity in the femur of aged rats by exercise training. Microvasc Res. 2009; 78:459-463.
23. Lloyd PG, Prior BM, Yang HT, Terjung RL. Angiogenic growth factor expression in rat skeletal muscle in response to exercise training. Am J Physiol Heart Circ Physiol. 2003; 284:H1668-H1678.
24. Iemitsu M, Maeda S, Jesmin S, Otsuki T, Miyauchi T. Exercise training improves aging-induced downregulation of VEGF angiogenic signaling cascade in hearts. Am J Physiol Heart Circ Physiol. 2006; 291:H1290-H1298.
25. Falone S, D'Alessandro A, Mirabilio A, Cacchio M, Di Ilio C, Di Loreto S, Amicarelli F. Late-onset running biphasically improves redox balance, energyand methylglyoxal-related status, as well as SIRT1 expression in mouse hippocampus. PLoS One. 2012; 7:e48334.
26. Moreau M, Neveu M, Stéphan S, Noblesse E, Nizard C, Sadick NS, Schnebert S, Bonté F, Dumas M, Andre P, Perrier E. Enhancing cell longevity for cosmetic application: a complementary approach. J Drugs Dermatol. 2007; 6: s14-s19.
27. Sauve AA, Wolberger C, Schramm VL, Boeke JD. The biochemistry of sirtuins. Annu Rev Biochem. 2006; 75:435-465.
28. Milne JC, Denu JM. The Sirtuin family: therapeutic targets to treat diseases of aging. Curr Opin Chem Biol. 2008; 12:11-17.
29. Yoshizaki T, Schenk S, Imamura T, Babendure JL, Sonoda N, Bae EJ, Oh DY, Lu M, Milne JC, Westphal C, Bandyopadhyay G, Olefsky JM. SIRT1 inhibits inflammatory pathways in macrophages and modulates insulin sensitivity. Am J Physiol Endocrinol Metab. 2010; 298:E419-E428.
30. Baar K, Wende AR, Jones TE, Marison M, Nolte LA, Chen M, Kelly DP, Holloszy JO. Adaptations of skeletal muscle to exercise: rapid increase in the transcriptional coactivator PGC-1. FASEB J. 2002; 16:1879-1886.
31. Pilegaard H, Saltin B, Neufer PD. Exercise induces transient transcriptional activation of the PGC-1α gene in human skeletal muscle. J Physiol. 2003; 546:851-858.
32. Terada S, Goto M, Kato M, Kawanaka K, Shimokawa T, Tabata I. Effects of low-intensity prolonged exercise on PGC-1 mRNA expression in rat epitrochlearis muscle. Biochem Biophys Res Commun. 2002; 296:350-354.
33. Terada S, Tabata I. Effects of acute bouts of running and swimming exercise on PGC-1α protein expression in rat epitrochlearis and soleus muscle. Am J Physiol Endocrinol Metab. 2004; 286:E208-216.
34. Russell AP, Feilchenfeldt J, Schreiber S, Praz M, Crettenand A, Gobelet C, Meier CA, Bell DR, Kralli A, Giacobino JP, Dériaz O. Endurance training in humans leads to fiber type-specific increases in levels of peroxisome proliferator-activated receptor-γ coactivator-1 and peroxisome proliferator-activated receptor-α in skeletal muscle. Diabetes. 2003; 52:2874-2881.
35. Taylor EB, Lamb JD, Hurst RW, Chesser DG, Ellingson WJ, Greenwood LJ, Porter BB, Herway ST, Winder WW. Endurance training increases skeletal muscle LKB1 and PGC-1 protein abundance: effects of time and intensity. Am J Physiol Endocrinol Metab. 2005; 289:E960-968.
36. Lezi E, Lu J, Burns JM, Swerdlow RH. Effect of exercise on mouse liver and brain bioenergetic infrastructures. Exp Physiol. 2013; 98:207-219.
37. Akimoto T, Pohnert SC, Li P, Zhang M, Gumbs C, Rosenberg PB, Williams RS, Yan Z. Exercise stimulates Pgc-1α transcription in skeletal muscle through activation of the p38 MAPK pathway. J Biol Chem. 2005; 280:19587-19593.
38. Chen ZP, Stephens TJ, Murthy S, Canny BJ, Hargreaves M, Witters LA, Kemp BE, McConell GK. Effect of exercise intensity on skeletal muscle AMPK signaling in humans. Diabetes. 2003; 52:2205-2212.
39. Fujii N, Hayashi T, Hirshman MF, Smith JT, Habinowski SA, Kaijser L, Mu J, Ljungqvist O, Birnbaum MJ, Witters LA, Thorell A, Goodyear LJ. Exercise induces isoformspecific increase in 5'AMP-activated protein kinase activity in human skeletal muscle. Biochem Biophys Res Commun. 2000; 273:1150-1155.
40. Irrcher I, Adhihetty PJ, Sheehan T, Joseph AM, Hood DA. PPARγ coactivator-1α expression during thyroid hormone-and contractile activity-induced mitochondrial adaptations. Am J Physiol Cell Physiol. 2003; 284:C1669-1677.
41. Boppart MD, Asp S, Wojtaszewski JF, Fielding RA, Mohr T, Goodyear LJ. Marathon running transiently increases c-Jun NH2-terminal kinase and p38 activities in human skeletal muscle. J Physiol. 2000; 526:663-669.
42. Suwa M, Nakano H, Radak Z, Kumagai S. Endurance exercise increases the SIRT1 and peroxisome proliferator-activated receptor γ coactivator-1α protein expressions in rat skeletal muscle. Metabolism. 2008; 57:986-998.
43. Salminen A, Kaarniranta K. Insulin/IGF-1 paradox of aging: regulation via AKT/IKK/NF-κB signaling. Cell Signal. 2010; 22:573-577.
44. Yeung F, Hoberg JE, Ramsey CS, Keller MD, Jones DR, Frye RA, Mayo MW. Modulation of NF-κB-dependent transcription and cell survival by the SIRT1 deacetylase. EMBO J. 2004; 23:2369-2380.
45. Lavu S, Boss O, Elliott PJ, Lambert PD. Sirtuins-novel therapeutic targets to treat age-associated diseases. Nat Rev Drug Discov. 2008; 7:841-853.
46. Lagouge M, Argmann C, Gerhart-Hines Z, Meziane H, Lerin C, Daussin F, Messadeq N, Milne J, Lambert P, Elliott P, Geny B, Laakso M, Puigserver P, Auwerx J. Resveratrol improves mitochondrial function and protects against metabolic disease by activating SIRT1 and PGC-1α. Cell. 2006; 127:1109-1122.
47. Rodgers JT, Lerin C, Haas W, Gygi SP, Spiegelman BM, Puigserver P. Nutrient control of glucose homeostasis through a complex of PGC-1α and SIRT1. Nature. 2005; 434:113-118.
48. Gerhart-Hines Z, Rodgers JT, Bare O, Lerin C, Kim SH, Mostoslavsky R, Alt FW, Wu Z, Puigserver P. Metabolic control of muscle mitochondrial function and fatty acid oxidation through SIRT1/PGC-1α. EMBO J. 2007; 26:1913-1923.
49. Fulco M, Schiltz RL, Iezzi S, King MT, Zhao P, Kashiwaya Y, Hoffman E, Veech RL, Sartorelli V. Sir2 regulates skeletal muscle differentiation as a potential sensor of the redox state. Mol Cell. 2003; 12:51-62.
50. Robergs RA, Ghiasvand F, Parker D. Biochemistry of exercise-induced metabolic acidosis. Am J Physiol Regul Integr Comp Physiol. 2004; 287:R502-516.