Physical exercise regulates p53 activity targeting SCO2 and increases Mitochondrial COX biogenesis in cardiac muscle with age

PLoS ONE

Volumn 6, Issue 7, 2011, Pages

  Qi, Zhengtang ^a,b   He, Jie ^a   Su, Yuhui ^a   He, Qiang ^a   Liu, Jingxia ^a   Yu, Lu ^a   Al Attas, Omar ^c   Hussain, Tajamul ^c   Ding, Shuzhe ^a,b   Ji, Liu ^a,b   Qian, Min ^b  

^a BEIJING UNIVERSITY OF POSTS AND TELECOMMUNICATIONS   (China)

^b EAST CHINA NORMAL UNIVERSITY   (China)

^c KING SAUD UNIVERSITY   (Saudi Arabia)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHROME C OXIDASE; CYTOCHROME OXIDASE DEFICIENT HOMOLOG 2; MESSENGER RNA; MITOCHONDRIAL DNA; OXIDOREDUCTASE; PROTEIN P53; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG; 2 PHENYLACETYLENESULFONAMIDE; 2-PHENYLACETYLENESULFONAMIDE; MITOCHONDRIAL PROTEIN; SCO2 PROTEIN, MOUSE; SULFONAMIDE;

AGE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOGENESIS; CELL FUNCTION; CONTROLLED STUDY; DNA CONTENT; GENE EXPRESSION; HEART MITOCHONDRION; HEART MUSCLE; MALE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PHYSICAL ACTIVITY; PROTEIN CONTENT; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TRANSPORT; AGING; ANIMAL; DRUG EFFECT; GENE EXPRESSION PROFILING; GENETICS; INSTITUTE FOR CANCER RESEARCH MOUSE; METABOLISM; PROTEIN SUBUNIT; RANDOMIZATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TIME; WESTERN BLOTTING;

MUS;

AGING; ANIMALS; BLOTTING, WESTERN; DNA, MITOCHONDRIAL; ELECTRON TRANSPORT COMPLEX IV; GENE EXPRESSION PROFILING; MALE; MICE; MICE, INBRED ICR; MITOCHONDRIA, HEART; MITOCHONDRIAL PROTEINS; MYOCARDIUM; PHYSICAL CONDITIONING, ANIMAL; PROTEIN SUBUNITS; PROTEIN TRANSPORT; RANDOM ALLOCATION; REACTIVE OXYGEN SPECIES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SULFONAMIDES; TIME FACTORS; TUMOR SUPPRESSOR PROTEIN P53;

EID: 79960071622     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0021140     Document Type: Article

References (65)

1. Ljubicic V, Menzies KJ, Hood DA, (2010) Mitochondrial dysfunction is associated with a pro-apoptotic cellular environment in senescent cardiac muscle. MECHANISMS OF AGEING AND DEVELOPMENT 131: 79-88.
2. Jezek P, Plecita-Hlavata L, (2009) Mitochondrial reticulum network dynamics in relation to oxidative stress, redox regulation, and hypoxia. Int J Biochem Cell Biol 41: 1790-1804.
3. Lesnefsky EJ, Moghaddas S, Tandler B, Kerner J, Hoppel CL, (2001) Mitochondrial dysfunction in cardiac disease: Ischemia-reperfusion, aging, and heart failure. JOURNAL OF MOLECULAR AND CELLULAR CARDIOLOGY 33: 1065-1089.
4. Dai DF, Santana LF, Vermulst M, Tomazela DM, Emond MJ, et al. (2009) Overexpression of Catalase Targeted to Mitochondria Attenuates Murine Cardiac Aging. CIRCULATION 119: 2779-2789.
5. Dai DF, Rabinovitch PS, (2009) Cardiac aging in mice and humans: the role of mitochondrial oxidative stress. Trends Cardiovasc Med 19: 213-220.
6. Hao JJ, Shen WL, Tian C, Liu ZB, Ren JM, et al. (2009) Mitochondrial nutrients improve immune dysfunction in the type 2 diabetic Goto-Kakizaki rats. JOURNAL OF CELLULAR AND MOLECULAR MEDICINE 13: 701-711.
7. Liu JK, Shen WL, Zhao BL, Wang Y, Wertz K, et al. (2009) Targeting mitochondrial biogenesis for preventing and treating insulin resistance in diabetes and obesity: Hope from natural mitochondrial nutrients. ADVANCED DRUG DELIVERY REVIEWS 61: 1343-1352.
8. Liu JK, Ames BN, (2005) Reducing mitochondrial decay with mitochondrial nutrients to delay and treat cognitive dysfunction, Alzheimer's disease, and Parkinson's disease. NUTRITIONAL NEUROSCIENCE 8: 67-89.
9. Loh K, Deng HY, Fukushima A, Cai XC, Boivin B, et al. (2009) Reactive Oxygen Species Enhance Insulin Sensitivity. CELL METABOLISM 10: 260-272.
10. Gomez-Cabrera MC, Domenech E, Romagnoli M, Arduini A, Borras C, et al. (2008) Oral administration of vitamin C decreases muscle mitochondrial biogenesis and hampers training-induced adaptations in endurance performance. AMERICAN JOURNAL OF CLINICAL NUTRITION 87: 142-149.
11. Wadley GD, McConell GK, (2010) High-dose antioxidant vitamin C supplementation does not prevent acute exercise-induced increases in markers of skeletal muscle mitochondrial biogenesis in rats. JOURNAL OF APPLIED PHYSIOLOGY 108: 1719-1726.
12. Falkenberg M, Gaspari M, Rantanen A, Trifunovic A, Larsson NG, et al. (2002) Mitochondrial transcription factors B1 and B2 activate transcription of human mtDNA. Nat Genet 31: 289-294.
13. Chen JQ, Cammarata PP, Baines CP, Yager JD, (2009) Regulation of mitochondrial respiratory chain biogenesis by estrogens/estrogen receptors and physiological, pathological and pharmacological implications. BIOCHIMICA ET BIOPHYSICA ACTA-MOLECULAR CELL RESEARCH 1793: 1540-1570.
14. Matoba S, Kang JG, Patino WD, Wragg A, Boehm M, et al. (2006) p53 regulates mitochondrial respiration. SCIENCE 312: 1650-1653.
15. Freisinger P, Horvath R, Macmillan C, Peters J, Jaksch M, (2004) Reversion of hypertrophic cardiomyopathy in a patient with deficiency of the mitochondrial copper binding protein Sco2: Is there a potential effect of copper? JOURNAL OF INHERITED METABOLIC DISEASE 27: 67-79.
16. Vesela K, Hulkova H, Hansikova H, Zeman J, Elleder M, (2008) Structural analysis of tissues affected by cytochrome C oxidase deficiency due to mutations in the SCO2 gene. APMIS 116: 41-49.
17. Arima Y, Nitta M, Kuninaka S, Zhang DW, Fujiwara T, et al. (2005) Transcriptional blockade induces p53-dependent apoptosis associated with translocation of p53 to mitochondria. JOURNAL OF BIOLOGICAL CHEMISTRY 280: 19166-19176.
18. Zhao YF, Chaiswing L, Velez JM, Batinic-Haberle I, Colburn NH, et al. (2005) p53 translocation to mitochondria precedes its nuclear translocation and targets mitochondrial oxidative defense protein-manganese superoxide dismutase. CANCER RESEARCH 65: 3745-3750.
19. Daosukho C, Noel T, Lien YC, Chen YM, St Clair D, (2005) Manganese superoxide dismutase (MnSOD) deficiency enhances adriamycin (ADR) and paclitaxel (Taxol)-induced p53 levels in heart mitochondria.FREE RADICAL BIOLOGY AND MEDICINE 39 (Suppl. 1): S150-S151.
20. Holley AK, Dhar SK, St CD, (2010) Manganese superoxide dismutase versus p53: the mitochondrial center. Ann N Y Acad Sci 1201: 72-78.
21. Tasdemir E, Maiuri MC, Morselli E, Criollo A, D'Amelio M, et al. (2008) A dual role of p53 in the control of autophagy. AUTOPHAGY 4: 810-814.
22. Liu B, Chen YM, Clair D, (2008) ROS and p53: A versatile partnership. FREE RADICAL BIOLOGY AND MEDICINE 44: 1529-1535.
23. Johnson WT, Anderson CM, (2008) Cardiac cytochrome c oxidase activity and contents of subunits 1 and 4 are altered in offspring by low prenatal copper intake by rat dams. JOURNAL OF NUTRITION 138: 1269-1273.
24. Johnson WT, Newman SM, (2007) Hearts in adult offspring of copper-deficient dams exhibit decreased cytochrome c oxidase activity, increased mitochondrial hydrogen peroxide generation and enhanced formation of intracellular residual bodies. JOURNAL OF NUTRITIONAL BIOCHEMISTRY 18: 97-104.
25. Kuo WW, Chu CY, Wu CH, Lin JA, Liu JY, et al. (2005) The profile of cardiac cytochrome c oxidase (COX) expression in an accelerated cardiac-hypertrophy model. JOURNAL OF BIOMEDICAL SCIENCE 12: 601-610.
26. Zuo XA, Xie HQ, Dong DY, Jiang NG, Zhu HM, et al. (2010) Cytochrome c Oxidase is Essential for Copper-Induced Regression of Cardiomyocyte Hypertrophy. CARDIOVASCULAR TOXICOLOGY 10: 208-215.
27. Leary SC, Cobine PA, Kaufman BA, Guercin GH, Mattman A, et al. (2007) The human cytochrome c oxidase assembly factors SCO1 and SCO2 have regulatory roles in the maintenance of cellular copper homeostasis. CELL METABOLISM 5: 9-20.
28. Hood DA, (2010) Mitochondrial biogenesis in skeletal muscle: Effect of exercise and age. BIOCHIMICA ET BIOPHYSICA ACTA-BIOENERGETICS 1797 (Suppl. S): 106-107.
29. Ljubicic V, Joseph AM, Saleem A, Uguccioni G, Collu-Marchese M, et al. (2010) Transcriptional and post-transcriptional regulation of mitochondrial biogenesis in skeletal muscle: Effects of exercise and aging. BIOCHIMICA ET BIOPHYSICA ACTA-GENERAL SUBJECTS 1800: 223-234.
30. Scarpulla RC, (2008) Transcriptional paradigms in mammalian mitochondrial biogenesis and function. PHYSIOLOGICAL REVIEWS 88: 611-638.
31. Gleyzer N, Vercauteren K, Scarpulla RC, (2005) Control of mitochondrial transcription specificity factors (TFB1M and TFB2M) by nuclear respiratory factors (NRF-1 and NRF-2) and PGC-1 family coactivators. MOLECULAR AND CELLULAR BIOLOGY 25: 1354-1366.
32. Litonin D, Sologub M, Shi YH, Savkina M, Anikin M, et al. (2010) Human Mitochondrial Transcription Revisited ONLY TFAM AND TFB2M ARE REQUIRED FOR TRANSCRIPTION OF THE MITOCHONDRIAL GENES IN VITRO. JOURNAL OF BIOLOGICAL CHEMISTRY 285: 18129-18133.
33. Park JY, Wang PY, Matsumoto T, Sung HJ, Ma W, et al. (2009) p53 improves aerobic exercise capacity and augments skeletal muscle mitochondrial DNA content. Circ Res 105: 705-712, 11-712.
34. Lebedeva MA, Eaton JS, Shadel GS, (2009) Loss of p53 causes mitochondrial DNA depletion and altered mitochondrial reactive oxygen species homeostasis. Biochim Biophys Acta 1787: 328-334.
35. Donahue RJ, Razmara M, Hoek JB, Knudsen TB, (2001) Direct influence of the p53 tumor suppressor on mitochondrial biogenesis and function. FASEB J 15: 635-644.
36. Saleem A, Adhihetty PJ, Hood DA, (2009) Role of p53 in mitochondrial biogenesis and apoptosis in skeletal muscle. Physiol Genomics 37: 58-66.
37. Achanta G, Sasaki R, Feng L, Carew JS, Lu W, et al. (2005) Novel role of p53 in maintaining mitochondrial genetic stability through interaction with DNA Pol gamma. EMBO J 24: 3482-3492.
38. Edwards MG, Anderson RM, Yuan M, Kendziorski CM, Weindruch R, et al. (2007) Gene expression profiling of aging reveals activation of a p53-mediated transcriptional program. BMC Genomics 8: 80.
39. Judge S, Jang YM, Smith A, Hagen T, Leeuwenburgh C, (2005) Age-associated increases in oxidative stress and antioxidant enzyme activities in cardiac interfibrillar mitochondria: implications for the mitochondrial theory of aging. FASEB J 19: 419-421.
40. Terman A, Dalen H, Eaton JW, Neuzil J, Brunk UT, (2004) Aging of cardiac myocytes in culture: oxidative stress, lipofuscin accumulation, and mitochondrial turnover. Ann N Y Acad Sci 1019: 70-77.
41. Judge S, Leeuwenburgh C, (2007) Cardiac mitochondrial bioenergetics, oxidative stress, and aging. Am J Physiol Cell Physiol 292: C1983-C1992.
42. Ren JC, Rebrin I, Klichko V, Orr WC, Sohal RS, (2010) Cytochrome c oxidase loses catalytic activity and structural integrity during the aging process in Drosophila melanogaster. Biochem Biophys Res Commun 401: 64-68.
43. Bertoni-Freddari C, Fattoretti P, Giorgetti B, Solazzi M, Balietti M, et al. (2004) Cytochrome oxidase activity in hippocampal synaptic mitochondria during aging: a quantitative cytochemical investigation. Ann N Y Acad Sci 1019: 33-36.
44. Ojaimi J, Masters CL, McLean C, Opeskin K, McKelvie P, et al. (1999) Irregular distribution of cytochrome c oxidase protein subunits in aging and Alzheimer's disease. Ann Neurol 46: 656-660.
45. Fattoretti P, Bertoni-Freddari C, Giorgetti B, Balietti M, (2004) Increased mitochondrial and nuclear gene expression of cytochrome oxidase subunits I and IV in neuronal aging. Ann N Y Acad Sci 1030: 303-309.
46. Barazzoni R, Short KR, Nair KS, (2000) Effects of aging on mitochondrial DNA copy number and cytochrome c oxidase gene expression in rat skeletal muscle, liver, and heart. J Biol Chem 275: 3343-3347.
47. Dyachenko V, Rueckschloss U, Isenberg G, (2006) Aging aggravates heterogeneities in cell-size and stress-intolerance of cardiac ventricular myocytes. Exp Gerontol 41: 489-496.
48. Holloszy JO, (1967) Biochemical adaptations in muscle. Effects of exercise on mitochondrial oxygen uptake and respiratory enzyme activity in skeletal muscle. J Biol Chem 242: 2278-2282.
49. Holloszy JO, (2008) Regulation by exercise of skeletal muscle content of mitochondria and GLUT4. J Physiol Pharmacol 59 (Suppl 7): 5-18.
50. Hood DA, (2009) Mechanisms of exercise-induced mitochondrial biogenesis in skeletal muscle. APPLIED PHYSIOLOGY NUTRITION AND METABOLISM-PHYSIOLOGIE APPLIQUEE NUTRITION ET METABOLISME 34: 465-472.
51. Vina J, Gomez-Cabrera MC, Borras C, Froio T, Sanchis-Gomar F, et al. (2009) Mitochondrial biogenesis in exercise and in ageing. ADVANCED DRUG DELIVERY REVIEWS 61: 1369-1374.
52. Wright DC, Han DH, Garcia-Roves PM, Geiger PC, Jones TE, et al. (2007) Exercise-induced mitochondrial biogenesis begins before the increase in muscle PGC-1alpha expression. J Biol Chem 282: 194-199.
53. Garcia-Roves PM, Huss J, Holloszy JO, (2006) Role of calcineurin in exercise-induced mitochondrial biogenesis. Am J Physiol Endocrinol Metab 290: E1172-E1179.
54. Boveris A, Navarro A, (2008) Systemic and mitochondrial adaptive responses to moderate exercise in rodents. Free Radic Biol Med 44: 224-229.
55. Marin-Garcia J, Ananthakrishnan R, Agrawal N, Goldenthal MJ, (1994) Mitochondrial gene expression during bovine cardiac growth and development. J Mol Cell Cardiol 26: 1029-1036.
56. Corcoran CA, Huang Y, Sheikh MS, (2006) The regulation of energy generating metabolic pathways by p53. Cancer Biol Ther 5: 1610-1613.
57. Zhang XD, Qin ZH, Wang J, (2010) The role of p53 in cell metabolism. Acta Pharmacol Sin 31: 1208-1212.
58. Charlot JF, Pretet JL, Haughey C, Mougin C, (2004) Mitochondrial translocation of p53 and mitochondrial membrane potential (Delta Psi m) dissipation are early events in staurosporine-induced apoptosis of wild type and mutated p53 epithelial cells. Apoptosis 9: 333-343.
59. Nemajerova A, Wolff S, Petrenko O, Moll UM, (2005) Viral and cellular oncogenes induce rapid mitochondrial translocation of p53 in primary epithelial and endothelial cells early in apoptosis. FEBS Lett 579: 6079-6083.
60. Liu J, St CD, Gu X, Zhao Y, (2008) Blocking mitochondrial permeability transition prevents p53 mitochondrial translocation during skin tumor promotion. FEBS Lett 582: 1319-1324.
61. Fernandez-Vizarra E, Ferrin G, Perez-Martos A, Fernandez-Silva P, Zeviani M, et al. (2010) Isolation of mitochondria for biogenetical studies: An update. MITOCHONDRION 10: 253-262.
62. Ding H, Jiang N, Liu HJ, Liu XR, Liu DX, et al. (2010) Response of mitochondrial fusion and fission protein gene expression to exercise in rat skeletal muscle. BIOCHIMICA ET BIOPHYSICA ACTA-GENERAL SUBJECTS 1800: 250-256.
63. Chen K, Zhang QY, Wang J, Liu FJ, Mi MT, et al. (2009) Taurine protects transformed rat retinal ganglion cells from hypoxia-induced apoptosis by preventing mitochondrial dysfunction. BRAIN RESEARCH 1279: 131-138.
64. Koopman R, Zorenc A, Gransier R, Cameron-Smith D, van Loon L, (2006) Increase in S6K1 phosphorylation in human skeletal muscle following resistance exercise occurs mainly in type II muscle fibers. AMERICAN JOURNAL OF PHYSIOLOGY-ENDOCRINOLOGY AND METABOLISM 290: E1245-E1252.
65. Smith J, Collins M, Grobler LA, Magee CJ, Ojuka EO, (2007) Exercise and CaMK activation both increase the binding of MEF2A to the Glut4 promoter in skeletal muscle in vivo. AMERICAN JOURNAL OF PHYSIOLOGY-ENDOCRINOLOGY AND METABOLISM 292: E413-E420.