Acute exercise stress activates Nrf2/ARE signaling and promotes antioxidant mechanisms in the myocardium

Free Radical Biology and Medicine

Volumn 52, Issue 2, 2012, Pages 366-376

  Muthusamy, Vasanthi R ^a   Kannan, Sankaranarayanan ^b   Sadhaasivam, Kamal ^a   Gounder, Sellamuthu S ^a   Davidson, Christopher J ^a   Boeheme, Christoph ^c   Hoidal, John R ^d   Wang, Li ^d   Rajasekaran, Namakkal Soorappan ^a  

^a UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF TEXAS   (United States)

^c UNIVERSITY OF UTAH   (United States)

^d UNIVERSITY OF UTAH HEALTH SCIENCES CENTER   (United States)

Author keywords

AES; Exercise; Keap1; Nrf2; Oxidative stress; ROS

Indexed keywords

ANTIOXIDANT; TRANSCRIPTION FACTOR NRF2;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EXERCISE; GENE ACTIVATION; HEART MUSCLE; HUMAN; MOUSE; NONHUMAN; OXIDATIVE STRESS; PHYSICAL STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; ANTIOXIDANTS; CELL NUCLEUS; CYTOSKELETAL PROTEINS; FEMALE; GENE KNOCKOUT TECHNIQUES; GLUTATHIONE; HEART; MALE; MICE; MICE, KNOCKOUT; MYOCARDIUM; NADPH OXIDASE; NF-E2-RELATED FACTOR 2; OXIDATIVE STRESS; PHYSICAL EXERTION; PROTEIN BINDING; PROTEIN TRANSPORT; REACTIVE OXYGEN SPECIES; RESPONSE ELEMENTS; SIGNAL TRANSDUCTION; SUPEROXIDE DISMUTASE; TRANSCRIPTIONAL ACTIVATION; UP-REGULATION;

ANIMALIA; MUS;

EID: 84855451533     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2011.10.440     Document Type: Article

References (71)

1. A.M. Kulminski, S.V. Ukraintseva, K.G. Arbeev, K.G. Manton, J. Oshima, G.M. Martin, D. Il'yasova, and A.I. Yashin Health-protective and adverse effects of the apolipoprotein E epsilon2 allele in older men J. Am. Geriatr. Soc. 56 2008 478 483 (Pubitemid 351327926)
2. K.G. Manton Recent declines in chronic disability in the elderly U.S. population: risk factors and future dynamics Annu. Rev. Public Health 29 2008 91 113 (Pubitemid 351600401)
3. K.G. Manton, X. Gu, and G.R. Lowrimore Cohort changes in active life expectancy in the U.S. elderly population: experience from the 1982-2004 National Long-Term Care Survey J. Gerontol. B Psychol. Sci. Soc. Sci. 63 2008 S269 S281
4. M.H. Jacob, R. Janner Dda, A.S. Araujo, M.P. Jahn, L.C. Kucharski, T.B. Moraes, C.S. Dutra Filho, M.F. Ribeiro, A. Bello-Klein, Redox imbalance influence in the myocardial Akt activation in aged rats treated with DHEA. Exp. Gerontol. 45:957-963; 2010.
5. M. Li, N.K. Fukagawa, Age-related changes in redox signaling and VSMC function. Antioxid. Redox Signal. 12:641-655; 2010.
6. C.D. Morrison, P.J. Pistell, D.K. Ingram, W.D. Johnson, Y. Liu, S.O. Fernandez-Kim, C.L. White, M.N. Purpera, R.M. Uranga, A.J. Bruce-Keller, J.N. Keller, High fat diet increases hippocampal oxidative stress and cognitive impairment in aged mice: implications for decreased Nrf2 signaling. J. Neurochem. 114:1581-1589; 2010.
7. A.R. Collins, C.J. Lyon, X. Xia, J.Z. Liu, R.K. Tangirala, F. Yin, R. Boyadjian, A. Bikineyeva, D. Pratico, D.G. Harrison, and W.A. Hsueh Age-accelerated atherosclerosis correlates with failure to upregulate antioxidant genes Circ. Res. 104 2009 e42 e54
8. Y. Du, M.C. Wooten, M. Gearing, and M.W. Wooten Age-associated oxidative damage to the p62 promoter: implications for Alzheimer disease Free Radic. Biol. Med. 46 2009 492 501
9. B.C. Capell, F.S. Collins, and E.G. Nabel Mechanisms of cardiovascular disease in accelerated aging syndromes Circ. Res. 101 2007 13 26 (Pubitemid 47094620)
10. W.R. Hazzard, and W.H. Ettinger Jr. Aging and atherosclerosis: changing considerations in cardiovascular disease prevention as the barrier to immortality is approached in old age Am. J. Geriatr. Cardiol. 4 1995 16 36
11. J.R. Jennings, T. Kamarck, S. Manuck, S.A. Everson, G. Kaplan, and J.T. Salonen Aging or disease? Cardiovascular reactivity in Finnish men over the middle years Psychol. Aging 12 1997 225 238 (Pubitemid 27250173)
12. D.A. Rhoades, T.K. Welty, W. Wang, F. Yeh, R.B. Devereux, R.R. Fabsitz, E.T. Lee, and B.V. Howard Aging and the prevalence of cardiovascular disease risk factors in older American Indians: the Strong Heart Study J. Am. Geriatr. Soc. 55 2007 87 94 (Pubitemid 46046233)
13. B.L. Segal, M.A. Tecce, and F.T. Sherman Cardiovascular disease and the aging U.S. population Geriatrics 58 2003 43 (Pubitemid 36091453)
14. B.F. Waller, T. Bloch, B.G. Barker, S.J. Roe, D.A. Hawley, J.C. Pless, and J.N. Eble The old-age heart: aging changes of the normal elderly heart and cardiovascular disease in 12 necropsy patients aged 90 to 101 years Cardiol. Clin. 2 1984 753 779
15. R.W. Wissler, and L. Robert Aging and cardiovascular disease: a summary of the Eighth Munster International Arteriosclerosis Symposium Circulation 93 1996 1608 1612 (Pubitemid 26131332)
16. T. Rangasamy, C.Y. Cho, R.K. Thimmulappa, L. Zhen, S.S. Srisuma, T.W. Kensler, M. Yamamoto, I. Petrache, R.M. Tuder, and S. Biswal Genetic ablation of Nrf2 enhances susceptibility to cigarette smoke-induced emphysema in mice J. Clin. Invest. 114 2004 1248 1259 (Pubitemid 40385296)
17. T. Rangasamy, J. Guo, W.A. Mitzner, J. Roman, A. Singh, A.D. Fryer, M. Yamamoto, T.W. Kensler, R.M. Tuder, S.N. Georas, and S. Biswal Disruption of Nrf2 enhances susceptibility to severe airway inflammation and asthma in mice J. Exp. Med. 202 2005 47 59 (Pubitemid 41002909)
18. N.M. Reddy, S.R. Kleeberger, T.W. Kensler, M. Yamamoto, P.M. Hassoun, and S.P. Reddy Disruption of Nrf2 impairs the resolution of hyperoxia-induced acute lung injury and inflammation in mice J. Immunol. 182 2009 7264 7271
19. W.O. Osburn, and T.W. Kensler Nrf2 signaling: an adaptive response pathway for protection against environmental toxic insults Mutat. Res. 659 2008 31 39
20. J.H. Suh, S.V. Shenvi, B.M. Dixon, H. Liu, A.K. Jaiswal, R.M. Liu, and T.M. Hagen Decline in transcriptional activity of Nrf2 causes age-related loss of glutathione synthesis, which is reversible with lipoic acid Proc. Natl. Acad. Sci. U. S. A. 101 2004 3381 3386 (Pubitemid 38338203)
21. T.W. Kensler, N. Wakabayashi, and S. Biswal Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway Annu. Rev. Pharmacol. Toxicol. 47 2007 89 116
22. L. Packer, E. Cadenas, and K.J. Davies Free radicals and exercise: an introduction Free Radic. Biol. Med. 44 2008 123 125
23. Z. Radak, M. Atalay, J. Jakus, I. Boldogh, K. Davies, and S. Goto Exercise improves import of 8-oxoguanine DNA glycosylase into the mitochondrial matrix of skeletal muscle and enhances the relative activity Free Radic. Biol. Med. 46 2009 238 243
24. S. Sachdev, and K.J. Davies Production, detection, and adaptive responses to free radicals in exercise Free Radic. Biol. Med. 44 2008 215 223
25. M. Asghar, L. George, and M.F. Lokhandwala Exercise decreases oxidative stress and inflammation and restores renal dopamine D1 receptor function in old rats Am. J. Physiol. Renal Physiol. 293 2007 F914 F919
26. A. Safdar, J. deBeer, M.A. Tarnopolsky, Dysfunctional Nrf2-Keap1 redox signaling in skeletal muscle of the sedentary old. Free Radic. Biol. Med. 49:1487-1493; 2010.
27. L. George, M.F. Lokhandwala, and M. Asghar Exercise activates redox-sensitive transcription factors and restores renal D1 receptor function in old rats Am. J. Physiol. Renal Physiol. 297 2009 F1174 F1180
28. K. Itoh, T. Chiba, S. Takahashi, T. Ishii, K. Igarashi, Y. Katoh, T. Oyake, N. Hayashi, K. Satoh, I. Hatayama, M. Yamamoto, and Y. Nabeshima An Nrf2/small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements Biochem. Biophys. Res. Commun. 236 1997 313 322 (Pubitemid 27373291)
29. M. Hoene, R. Lehmann, A.M. Hennige, A.K. Pohl, H.U. Haring, E.D. Schleicher, and C. Weigert Acute regulation of metabolic genes and insulin receptor substrates in the liver of mice by one single bout of treadmill exercise J. Physiol. 587 2009 241 252
30. A. Safdar, A. Abadi, M. Akhtar, B.P. Hettinga, and M.A. Tarnopolsky miRNA in the regulation of skeletal muscle adaptation to acute endurance exercise in C57Bl/6J male mice PLoS One 4 2009 e5610
31. N.S. Rajasekaran, P. Connell, E.S. Christians, L.J. Yan, R.P. Taylor, A. Orosz, X.Q. Zhang, T.J. Stevenson, R.M. Peshock, J.A. Leopold, W.H. Barry, J. Loscalzo, S.J. Odelberg, and I.J. Benjamin Human alpha B-crystallin mutation causes oxido-reductive stress and protein aggregation cardiomyopathy in mice Cell 130 2007 427 439 (Pubitemid 47208522)
32. N.S. Rajasekaran, S. Sathyanarayanan, N.S. Devaraj, and H. Devaraj Chronic depletion of glutathione (GSH) and minimal modification of LDL in vivo: its prevention by glutathione mono ester (GME) therapy Biochim. Biophys. Acta 1741 2005 103 112 (Pubitemid 40824995)
33. N.S. Rajasekaran, S. Varadharaj, G.D. Khanderao, C.J. Davidson, S. Kannan, M.A. Firpo, J.L. Zweier, I.J. Benjamin, Sustained activation of nuclear erythroid 2-related factor 2/antioxidant response element signaling promotes reductive stress in the human mutant protein aggregation cardiomyopathy in mice. Antioxid. Redox Signal. 14:957-971; 2011.
34. A. Hirayama, K. Yoh, S. Nagase, A. Ueda, K. Itoh, N. Morito, K. Hirayama, S. Takahashi, M. Yamamoto, and A. Koyama EPR imaging of reducing activity in Nrf2 transcriptional factor-deficient mice Free Radic. Biol. Med. 34 2003 1236 1242 (Pubitemid 36513966)
35. S.B. Lee, C.Y. Kim, H.J. Lee, J.H. Yun, and C.W. Nho Induction of the phase II detoxification enzyme NQO1 in hepatocarcinoma cells by lignans from the fruit of Schisandra chinensis through nuclear accumulation of Nrf2 Planta Med. 75 2009 1314 1318
36. S.K. Powers, L.L. Ji, and C. Leeuwenburgh Exercise training-induced alterations in skeletal muscle antioxidant capacity: a brief review Med. Sci. Sports Exerc. 31 1999 987 997 (Pubitemid 29316195)
37. K. Sugamura, J.F. Keaney, Jr. Reactive oxygen species in cardiovascular disease. Free Radic. Biol. Med. 51:978-992; 2011.
38. J. Kuroda, J. Sadoshima, NADPH oxidase and cardiac failure. J. Cardiovasc. Transl. Res. 3:314-320; 2010.
39. U. Rueckschloss, M. Villmow, U. Klockner, NADPH oxidase-derived superoxide impairs calcium transients and contraction in aged murine ventricular myocytes. Exp. Gerontol. 45:788-796; 2010.
40. 2 and cumene hydroperoxide treatment on heart mitochondria J. Bioenerg. Biomembr. 38 2006 121 127
41. M. Seddon, Y.H. Looi, and A.M. Shah Oxidative stress and redox signalling in cardiac hypertrophy and heart failure Heart (Br. Cardiac Soc.) 93 2007 903 907 (Pubitemid 47122034)
42. T. Ago, T. Liu, P. Zhai, W. Chen, H. Li, J.D. Molkentin, S.F. Vatner, and J. Sadoshima A redox-dependent pathway for regulating class II HDACs and cardiac hypertrophy Cell 133 2008 978 993 (Pubitemid 351787743)
43. T. Ago, and J. Sadoshima Thioredoxin1 as a negative regulator of cardiac hypertrophy Antioxid. Redox Signal. 9 2007 679 687 (Pubitemid 46799100)
44. M. Yamamoto, G. Yang, C. Hong, J. Liu, E. Holle, X. Yu, T. Wagner, S.F. Vatner, and J. Sadoshima Inhibition of endogenous thioredoxin in the heart increases oxidative stress and cardiac hypertrophy J. Clin. Invest. 112 2003 1395 1406 (Pubitemid 38057693)
45. A. Meister Selective modification of glutathione metabolism Science 220 1983 472 477 (Pubitemid 13114104)
46. A. Meister, and M.E. Anderson Glutathione Annu. Rev. Biochem. 52 1983 711 760 (Pubitemid 13030692)
47. O.W. Griffith, and A. Meister Glutathione: interorgan translocation, turnover, and metabolism Proc. Natl. Acad. Sci. U. S. A. 76 1979 5606 5610 (Pubitemid 10161666)
48. A. Meister Glutathione, metabolism and function via the gamma-glutamyl cycle Life Sci. 15 1974 177 190
49. A. Meister, O.W. Griffith, A. Novogrodsky, and S.S. Tate New aspects of glutathione metabolism and translocation in mammals Ciba Found. Symp. 1979 135 161
50. A. Meister, and S.S. Tate Glutathione and related gamma-glutamyl compounds: biosynthesis and utilization Annu. Rev. Biochem. 45 1976 559 604
51. J.F. Bean, A. Vora, and W.R. Frontera Benefits of exercise for community-dwelling older adults Arch. Phys.Med. Rehabil. 85 2004 S31 S42 quiz S43-S34
52. A. Navarro, C. Gomez, J.M. Lopez-Cepero, and A. Boveris Beneficial effects of moderate exercise on mice aging: survival, behavior, oxidative stress, and mitochondrial electron transfer Am. J. Physiol. Regul. Integr. Comp. Physiol. 286 2004 R505 R511
53. A. Navarro-Arevalo, C. Canavate, and M.J. Sanchez-del-Pino Myocardial and skeletal muscle aging and changes in oxidative stress in relationship to rigorous exercise training Mech. Ageing Dev. 108 1999 207 217 (Pubitemid 29240626)
54. A. Navarro-Arevalo, and M.J. Sanchez-del-Pino Age and exercise-related changes in lipid peroxidation and superoxide dismutase activity in liver and soleus muscle tissues of rats Mech. Ageing Dev. 104 1998 91 102 (Pubitemid 28408324)
55. J.M. Lee, J. Li, D.A. Johnson, T.D. Stein, A.D. Kraft, M.J. Calkins, R.J. Jakel, and J.A. Johnson Nrf2, a multi-organ protector? FASEB J. 19 2005 1061 1066 (Pubitemid 40946431)
56. J. Li, C. Zhang, Y. Xing, J.S. Janicki, M. Yamamoto, X.L. Wang, D.Q. Tang, T. Cui, Up-regulation of p27kip1 contributes to Nrf2-mediated protection against angiotensin II-induced cardiac hypertrophy. Cardiovasc. Res. 90:315-324; 2011.
57. K. Itoh, N. Wakabayashi, Y. Katoh, T. Ishii, T. O'Connor, and M. Yamamoto Keap1 regulates both cytoplasmic-nuclear shuttling and degradation of Nrf2 in response to electrophiles Genes Cells 8 2003 379 391 (Pubitemid 36504013)
58. M. McMahon, K. Itoh, M. Yamamoto, and J.D. Hayes Keap1-dependent proteasomal degradation of transcription factor Nrf2 contributes to the negative regulation of antioxidant response element-driven gene expression J. Biol. Chem. 278 2003 21592 21600 (Pubitemid 36792558)
59. D.D. Zhang, The Nrf2-Keap1-ARE signaling pathway: the regulation and dual function of Nrf2 in cancer. Antioxid. Redox Signal. 13:1623-1626; 2010.
60. J.W. Kaspar, S.K. Niture, and A.K. Jaiswal Nrf2:INrf2 (Keap1) signaling in oxidative stress Free Radic. Biol. Med. 47 2009 1304 1309
61. T.W. Kensler, N. Wakabayashi, Nrf2: friend or foe for chemoprevention? Carcinogenesis 31:90-99; 2010.
62. N. Wakabayashi, S.L. Slocum, J.J. Skoko, S. Shin, T.W. Kensler, When NRF2 talks, who's listening? Antioxid. Redox Signal. 13:1649-1663; 2010.
63. C.E. Hochmuth, B. Biteau, D. Bohmann, H. Jasper, Redox regulation by Keap1 and Nrf2 controls intestinal stem cell proliferation in Drosophila. Cell Stem Cell 8:188-199; 2010.
64. G.P. Sykiotis, D. Bohmann, Stress-activated cap'n'collar transcription factors in aging and human disease. Sci. Signal. 3:re3; 2010.
65. G.P. Sykiotis, and D. Bohmann Keap1/Nrf2 signaling regulates oxidative stress tolerance and lifespan in Drosophila Dev. Cell 14 2008 76 85
66. A. Saborido, A. Naudi, M. Portero-Otin, R. Pamplona, A. Megias, Stanozolol treatment decreases the mitochondrial ROS generation and oxidative stress induced by acute exercise in rat skeletal muscle. J. Appl. Physiol. 110:661-669; 2010.
67. T. Ago, S. Matsushima, J. Kuroda, D. Zablocki, T. Kitazono, J. Sadoshima, The NADPH oxidase Nox4 and aging in the heart. Aging 2:1012-1016; 2010.
68. J. Kuroda, T. Ago, S. Matsushima, P. Zhai, M.D. Schneider, J. Sadoshima, NADPH oxidase 4 (Nox4) is a major source of oxidative stress in the failing heart. Proc. Natl. Acad. Sci. U. S. A. 107:15565-15570; 2010.
69. E. Cadenas, and K.J. Davies Mitochondrial free radical generation, oxidative stress, and aging Free Radic. Biol. Med. 29 2000 222 230
70. K.J. Davies, and P. Hochstein Ubisemiquinone radicals in liver: implications for a mitochondrial Q cycle in vivo Biochem. Biophys. Res. Commun. 107 1982 1292 1299
71. J. Li, T. Ichikawa, L. Villacorta, J.S. Janicki, G.L. Brower, M. Yamamoto, and T. Cui Nrf2 protects against maladaptive cardiac responses to hemodynamic stress Arterioscler. Thromb. Vasc. Biol. 29 2009 1843 1850