Strenuous exercise induces mitochondrial damage in skeletal muscle of old mice

Biochemical and Biophysical Research Communications

Volumn 461, Issue 2, 2015, Pages 354-360

  Lee, Sangho ^a   Kim, Minjung ^a   Lim, Wonchung ^b   Kim, Taeyoung ^a   Kang, Chounghun ^a,c  

^a Hankuk University of Foreign Studies   (South Korea)

^b Chongju University   (South Korea)

^c UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Exercise; Inflammation; Mitochondria; Redox signals; Skeletal muscle

Indexed keywords

CYTOKINE; REACTIVE OXYGEN METABOLITE;

AGING; ANIMAL; ANIMAL EXPERIMENT; AUTOPHAGY; C57BL MOUSE; MALE; METABOLISM; MOUSE; MUSCLE MITOCHONDRION; OXIDATION REDUCTION REACTION; PATHOLOGY; PHYSIOLOGY; SKELETAL MUSCLE;

AGING; ANIMALS; AUTOPHAGY; CYTOKINES; MALE; MICE; MICE, INBRED C57BL; MITOCHONDRIA, MUSCLE; MUSCLE, SKELETAL; OXIDATION-REDUCTION; PHYSICAL CONDITIONING, ANIMAL; REACTIVE OXYGEN SPECIES;

EID: 84937762557     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2015.04.038     Document Type: Article

References (38)

1. A. Bratic, and N. Larsson The role of mitochondria in aging J. Clin. Invest. 123 2013 951 957
2. T. Finkel, and N.J. Holbrook Oxidants, oxidative stress and the biology of ageing Nature 408 2000 239 247
3. M.T. Ryan, and N.J. Hoogenraad Mitochondrial-nuclear communications Annu. Rev. Biochem. 76 2007 701 722
4. D.C. Wallace A mitochondrial paradigm of metabolic and degenerative diseases, aging, and cancer: a dawn for evolutionary medicine Annu. Rev. Genet. 39 2005 359
5. M.K. Shigenaga, T.M. Hagen, and B.N. Ames Oxidative damage and mitochondrial decay in aging Proc. Natl. Acad. Sci. U. S. A. 91 1994 10771 10778
6. R.S. Sohal, H. Ku, S. Agarwal, M.J. Forster, and H. Lal Oxidative damage, mitochondrial oxidant generation and antioxidant defenses during aging and in response to food restriction in the mouse Mech. Ageing Dev. 74 1994 121 133
7. P. Nagley, and Y. Wei Ageing and mammalian mitochondrial genetics Trends Genet. 14 1998 513 517
8. Y. Higami, and I. Shimokawa Apoptosis in the aging process Cell Tissue Res. 301 2000 125 132
9. K. Palikaras, and N. Tavernarakis Mitochondrial homeostasis: the interplay between mitophagy and mitochondrial biogenesis Exp. Gerontol. 56 2014 182 188
10. G. Twig, A. Elorza, A.J. Molina, H. Mohamed, J.D. Wikstrom, G. Walzer, L. Stiles, S.E. Haigh, S. Katz, and G. Las Fission and selective fusion govern mitochondrial segregation and elimination by autophagy EMBO J. 27 2008 433 446
11. A.E. Civitarese, S. Carling, L.K. Heilbronn, M.H. Hulver, B. Ukropcova, W.A. Deutsch, S.R. Smith, and E. Ravussin Calorie restriction increases muscle mitochondrial biogenesis in healthy humans PLoS Med. 4 2007 e76
12. E. Nisoli, C. Tonello, A. Cardile, V. Cozzi, R. Bracale, L. Tedesco, S. Falcone, A. Valerio, O. Cantoni, E. Clementi, S. Moncada, and M.O. Carruba Calorie restriction promotes mitochondrial biogenesis by inducing the expression of eNOS Science 310 2005 314 317
13. M. Lagouge, C. Argmann, Z. Gerhart-Hines, H. Meziane, C. Lerin, F. Daussin, N. Messadeq, J. Milne, P. Lambert, and P. Elliott Resveratrol improves mitochondrial function and protects against metabolic disease by activating SIRT1 and PGC-1α Cell 127 2006 1109 1122
14. R.M. Reznick, H. Zong, J. Li, K. Morino, I.K. Moore, H.J. Yu, Z. Liu, J. Dong, K.J. Mustard, and S.A. Hawley Aging-associated reductions in AMP-activated protein kinase activity and mitochondrial biogenesis Cell Metab. 5 2007 151 156
15. M.C. Gomez-Cabrera, E. Domenech, M. Romagnoli, A. Arduini, C. Borras, F.V. Pallardo, J. Sastre, and J. Vina Oral administration of vitamin C decreases muscle mitochondrial biogenesis and hampers training-induced adaptations in endurance performance Am. J. Clin. Nutr. 87 2008 142 149
16. N.A. Strobel, J.M. Peake, A. Matsumoto, S.A. Marsh, J.S. Coombes, and G.D. Wadley Antioxidant supplementation reduces skeletal muscle mitochondrial biogenesis Med. Sci. Sports Exerc. 43 2011 1017 1024
17. J.O. Holloszy Biochemical adaptations in muscle. Effects of exercise on mitochondrial oxygen uptake and respiratory enzyme activity in skeletal muscle J. Biol. Chem. 242 1967 2278 2282
18. E.V. Menshikova, V.B. Ritov, L. Fairfull, R.E. Ferrell, D.E. Kelley, and B.H. Goodpaster Effects of exercise on mitochondrial content and function in aging human skeletal muscle J. Gerontol. A Biol. Sci. Med. Sci. 61 2006 534 540
19. K. Baar, A.R. Wende, T.E. Jones, M. Marison, L.A. Nolte, M. Chen, D.P. Kelly, and J.O. Holloszy Adaptations of skeletal muscle to exercise: rapid increase in the transcriptional coactivator PGC-1 FASEB J. 16 2002 1879 1886
20. J.P. Little, A. Safdar, G.P. Wilkin, M.A. Tarnopolsky, and M.J. Gibala A practical model of low-volume high-intensity interval training induces mitochondrial biogenesis in human skeletal muscle: potential mechanisms J. Physiol. (Lond.) 588 2010 1011 1022
21. J.P. Little, A. Safdar, D. Bishop, M.A. Tarnopolsky, and M.J. Gibala An acute bout of high-intensity interval training increases the nuclear abundance of PGC-1alpha and activates mitochondrial biogenesis in human skeletal muscle Am. J. Physiol. Regul. Integr. Comp. Physiol. 300 2011 R1303 R1310
22. 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
23. N. Suematsu, H. Tsutsui, J. Wen, D. Kang, M. Ikeuchi, T. Ide, S. Hayashidani, T. Shiomi, T. Kubota, N. Hamasaki, and A. Takeshita Oxidative stress mediates tumor necrosis factor-alpha-induced mitochondrial DNA damage and dysfunction in cardiac myocytes Circulation 107 2003 1418 1423
24. R. Zell, P. Geck, K. Werdan, and P. Boekstegers TNF-α and IL-1α inhibit both pyruvate dehydrogenase activity and mitochondrial function in cardiomyocytes: evidence for primary impairment of mitochondrial function Mol. Cell. Biochem. 177 1997 61 67
25. Z. Radak, A.W. Taylor, H. Ohno, and S. Goto Adaptation to exercise-induced oxidative stress: from muscle to brain Exerc. Immunol. Rev. 7 2001 90 107
26. K. Ostrowski, T. Rohde, S. Asp, P. Schjerling, and B.K. Pedersen Pro-and anti-inflammatory cytokine balance in strenuous exercise in humans J. Physiol. (Lond.) 515 1999 287 291
27. B.K. Pedersen Exercise and cytokines Immunol. Cell Biol. 78 2000 532 535
28. C. Kang, and L.L. Ji Muscle immobilization and remobilization downregulates PGC-1α signaling and the mitochondrial biogenesis pathway J. Appl. Physiol. 115 2013 1618 1625
29. Z. Wu, P. Puigserver, U. Andersson, C. Zhang, G. Adelmant, V. Mootha, A. Troy, S. Cinti, B. Lowell, and R.C. Scarpulla Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1 Cell 98 1999 115 124
30. C. Kang, E. Chung, G. Diffee, and L.L. Ji Exercise training attenuates aging-associated mitochondrial dysfunction in rat skeletal muscle: role of PGC-1α Exp. Gerontol. 48 2013 1343 1350
31. C. Kang, K.M. O'Moore, J.R. Dickman, and L.L. Ji Exercise activation of muscle peroxisome proliferator-activated receptor-γ coactivator-1α signaling is redox sensitive Free Radic. Biol. Med. 47 2009 1394 1400
32. M.J. Morgan, and Z. Liu Crosstalk of reactive oxygen species and NF-κB signaling Cell Res. 21 2011 103 115
33. D. Alvarez-Guardia, X. Palomer, T. Coll, M.M. Davidson, T.O. Chan, A.M. Feldman, J.C. Laguna, and M. Vazquez-Carrera The p65 subunit of NF-kappaB binds to PGC-1alpha, linking inflammation and metabolic disturbances in cardiac cells Cardiovasc. Res. 87 2010 449 458
34. P.S. Eisele, S. Salatino, J. Sobek, M.O. Hottiger, and C. Handschin The peroxisome proliferator-activated receptor gamma coactivator 1alpha/beta (PGC-1) coactivators repress the transcriptional activity of NF-kappaB in skeletal muscle cells J. Biol. Chem. 288 2013 2246 2260
35. D.C. Chan Mitochondrial fusion and fission in mammals Annu. Rev. Cell Dev. Biol. 22 2006 79 99
36. A.Y. Seo, A.M. Joseph, D. Dutta, J.C. Hwang, J.P. Aris, and C. Leeuwenburgh New insights into the role of mitochondria in aging: mitochondrial dynamics and more J. Cell. Sci. 123 2010 2533 2542
37. H.F. Jheng, P.J. Tsai, S.M. Guo, L.H. Kuo, C.S. Chang, I.J. Su, C.R. Chang, and Y.S. Tsai Mitochondrial fission contributes to mitochondrial dysfunction and insulin resistance in skeletal muscle Mol. Cell. Biol. 32 2012 309 319
38. R. Scherz-Shouval, and Z. Elazar Regulation of autophagy by ROS: physiology and pathology Trends Biochem. Sci. 36 2011 30 38