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Oxidative Medicine and Cellular Longevity
Volume 2014, Article ID 315896, 10 pages
http://dx.doi.org/10.1155/2014/315896
Research Article

Antioxidant Supplement Inhibits Skeletal Muscle Constitutive Autophagy rather than Fasting-Induced Autophagy in Mice

1Key Laboratory of Adolescent Health Assessment and Exercise Intervention, Ministry of Education, East China Normal University, Shanghai 200241, China
2College of Physical Education and Health, East China Normal University, Shanghai 200241, China

Received 8 January 2014; Revised 28 April 2014; Accepted 16 May 2014; Published 15 June 2014

Academic Editor: Marcelo Paes de Barros

Copyright © 2014 Zhengtang Qi et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. M. Sandri, “Autophagy in skeletal muscle,” FEBS Letters, vol. 584, no. 7, pp. 1411–1416, 2010. View at Publisher · View at Google Scholar · View at Scopus
  2. G. Twig, B. Hyde, and O. S. Shirihai, “Mitochondrial fusion, fission and autophagy as a quality control axis: the bioenergetic view,” Biochimica et Biophysica Acta: Bioenergetics, vol. 1777, no. 9, pp. 1092–1097, 2008. View at Publisher · View at Google Scholar · View at Scopus
  3. Q. Sun, W. Fan, K. Chen, X. Ding, S. Chen, and Q. Zhong, “Identification of Barkor as a mammalian autophagy-specific factor for Beclin 1 and class III phosphatidylinositol 3-kinase,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 49, pp. 19211–19216, 2008. View at Publisher · View at Google Scholar · View at Scopus
  4. M. C. Maiuri, E. Zalckvar, A. Kimchi, and G. Kroemer, “Self-eating and self-killing: crosstalk between autophagy and apoptosis,” Nature Reviews Molecular Cell Biology, vol. 8, no. 9, pp. 741–752, 2007. View at Publisher · View at Google Scholar · View at Scopus
  5. T. Ueno, W. Sato, Y. Horie et al., “Loss of Pten, a tumor suppressor, causes the strong inhibition of autophagy without affecting LC3 lipidation,” Autophagy, vol. 4, no. 5, pp. 692–700, 2008. View at Google Scholar · View at Scopus
  6. F. Fortunato, H. Bürgers, F. Bergmann et al., “Impaired autolysosome formation correlates with lamp-2 depletion: role of apoptosis, autophagy, and necrosis in pancreatitis,” Gastroenterology, vol. 137, no. 1, pp. 350–360, 2009. View at Publisher · View at Google Scholar · View at Scopus
  7. F. A. Graca, D. A. Goncalves, W. A. Silveira et al., “Epinephrine depletion exacerbates the fasting-induced protein breakdown in fast-twitch skeletal muscles,” The American Journal of Physiology: Endocrinology and Metabolism, vol. 305, pp. E1483–E1494, 2013. View at Publisher · View at Google Scholar
  8. T. Ogata, Y. Oishi, M. Higuchi, and I. Muraoka, “Fasting-related autophagic response in slow- and fast-twitch skeletal muscle,” Biochemical and Biophysical Research Communications, vol. 394, no. 1, pp. 136–140, 2010. View at Publisher · View at Google Scholar · View at Scopus
  9. A. Doria, M. Gatto, and L. Punzi, “Autophagy in human health and disease,” New England Journal of Medicine, vol. 368, no. 19, p. 1845, 2013. View at Publisher · View at Google Scholar · View at Scopus
  10. S. Fulda, “Autophagy and cell death,” Autophagy, vol. 8, no. 8, pp. 1250–1251, 2012. View at Publisher · View at Google Scholar · View at Scopus
  11. E. Masiero, L. Agatea, C. Mammucari et al., “Autophagy is required to maintain muscle mass,” Cell Metabolism, vol. 10, no. 6, pp. 507–515, 2009. View at Publisher · View at Google Scholar · View at Scopus
  12. A. C. Nascimbeni, M. Fanin, E. Masiero, C. Angelini, and M. Sandri, “Impaired autophagy contributes to muscle atrophy in glycogen storage disease type II patients,” Autophagy, vol. 8, no. 11, pp. 1697–1700, 2012. View at Publisher · View at Google Scholar · View at Scopus
  13. M. Sandri, “Protein breakdown in muscle wasting: role of autophagy-lysosome and ubiquitin-proteasome,” International Journal of Biochemistry and Cell Biology, vol. 45, pp. 2121–2129, 2013. View at Publisher · View at Google Scholar · View at Scopus
  14. E. Masiero and M. Sandri, “Autophagy inhibition induces atrophy and myopathy in adult skeletal muscles,” Autophagy, vol. 6, no. 2, pp. 307–309, 2010. View at Publisher · View at Google Scholar · View at Scopus
  15. R. Scherz-Shouval and Z. Elazar, “Regulation of autophagy by ROS: physiology and pathology,” Trends in Biochemical Sciences, vol. 36, no. 1, pp. 30–38, 2011. View at Publisher · View at Google Scholar · View at Scopus
  16. C. R. Morales, Z. Pedrozo, S. Lavandero, and J. A. Hill, “Oxidative stress and autophagy in cardiovascular homeostasis,” Antioxidants & Redox Signaling, vol. 20, pp. 507–518, 2014. View at Publisher · View at Google Scholar
  17. C. Luo, Y. Li, H. Wang et al., “Mitochondrial accumulation under oxidative stress is due to defects in autophagy,” Journal of Cellular Biochemistry, vol. 114, no. 1, pp. 212–219, 2013. View at Publisher · View at Google Scholar · View at Scopus
  18. Y. Wang, Y. Nartiss, B. Steipe, G. A. McQuibban, and P. K. Kim, “ROS-induced mitochondrial depolarization initiates PARK2/PARKIN-dependent mitochondrial degradation by autophagy,” Autophagy, vol. 8, no. 10, pp. 1462–1476, 2012. View at Publisher · View at Google Scholar · View at Scopus
  19. T. Zhang, Y. Li, K. A. Park et al., “Cucurbitacin induces autophagy through mitochondrial ROS production which counteracts to limit caspase-dependent apopt,” Autophagy, vol. 8, no. 4, pp. 559–576, 2012. View at Publisher · View at Google Scholar · View at Scopus
  20. R. Sandhir, A. Sood, A. Mehrotra, and S. S. Kamboj, “N-acetylcysteine reverses mitochondrial dysfunctions and behavioral abnormalities in 3-nitropropionic acid-induced Huntington's disease,” Neurodegenerative Diseases, vol. 9, no. 3, pp. 145–157, 2012. View at Publisher · View at Google Scholar · View at Scopus
  21. S. S. Kamboj and R. Sandhir, “Protective effect of N-acetylcysteine supplementation on mitochondrial oxidative stress and mitochondrial enzymes in cerebral cortex of streptozotocin-treated diabetic rats,” Mitochondrion, vol. 11, no. 1, pp. 214–222, 2011. View at Publisher · View at Google Scholar · View at Scopus
  22. M. Zafarullah, W. Q. Li, J. Sylvester, and M. Ahmad, “Molecular mechanisms of N-acetylcysteine actions,” Cellular and Molecular Life Sciences, vol. 60, no. 1, pp. 6–20, 2003. View at Publisher · View at Google Scholar · View at Scopus
  23. 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,” Medicine and Science in Sports and Exercise, vol. 43, no. 6, pp. 1017–1024, 2011. View at Publisher · View at Google Scholar · View at Scopus
  24. M.-C. Gomez-Cabrera, E. Domenech, M. Romagnoli et al., “Oral administration of vitamin C decreases muscle mitochondrial biogenesis and hampers training-induced adaptations in endurance performance,” The American Journal of Clinical Nutrition, vol. 87, no. 1, pp. 142–149, 2008. View at Google Scholar · View at Scopus
  25. N. P. Whitehead, C. Pham, O. L. Gervasio, and D. G. Allen, “N-Acetylcysteine ameliorates skeletal muscle pathophysiology in mdx mice,” Journal of Physiology, vol. 586, no. 7, pp. 2003–2014, 2008. View at Publisher · View at Google Scholar · View at Scopus
  26. C.-H. Lin, S.-C. Kuo, L.-J. Huang, and P.-W. Gean, “Neuroprotective effect of N-acetylcysteine on neuronal apoptosis induced by a synthetic gingerdione compound: involvement of ERK and p38 phosphorylation,” Journal of Neuroscience Research, vol. 84, no. 7, pp. 1485–1494, 2006. View at Publisher · View at Google Scholar · View at Scopus
  27. O. B. Kotoulas, S. A. Kalamidas, and D. J. Kondomerkos, “Glycogen autophagy in glucose homeostasis,” Pathology Research and Practice, vol. 202, no. 9, pp. 631–638, 2006. View at Publisher · View at Google Scholar · View at Scopus
  28. J. Zirin, J. Nieuwenhuis, and N. Perrimon, “Role of autophagy in glycogen breakdown and its relevance to chloroquine myopathy,” PLoS Biology, vol. 11, no. 11, Article ID e1001708, 2013. View at Publisher · View at Google Scholar
  29. P. Castets, S. Lin, N. Rion et al., “Sustained activation of mTORC1 in skeletal muscle inhibits constitutive and starvation-induced autophagy and causes a severe, late-onset myopathy,” Cell Metabolism, vol. 17, no. 5, pp. 731–744, 2013. View at Publisher · View at Google Scholar · View at Scopus
  30. M. Rahman, M. Mofarrahi, A. S. Kristof, B. Nkengfac, S. Harel, and S. N. Hussain, “Reactive oxygen species regulation of autophagy in skeletal muscles,” Antioxidants & Redox Signaling, vol. 20, no. 3, pp. 443–459, 2014. View at Publisher · View at Google Scholar
  31. J. Yan, Z. Feng, J. Liu et al., “Enhanced autophagy plays a cardinal role in mitochondrial dysfunction in type 2 diabetic Goto-Kakizaki (GK) rats: ameliorating effects of (-)-epigallocatechin-3-gallate,” Journal of Nutritional Biochemistry, vol. 23, no. 7, pp. 716–724, 2012. View at Publisher · View at Google Scholar · View at Scopus
  32. L. V. Yuzefovych, S. I. Musiyenko, G. L. Wilson, and L. I. Rachek, “Mitochondrial DNA damage and dysfunction, and oxidative stress are associated with endoplasmic reticulum stress, protein degradation and apoptosis in high fat diet-induced Insulin resistance mice,” PLoS ONE, vol. 8, no. 1, Article ID e54059, 2013. View at Publisher · View at Google Scholar · View at Scopus
  33. L. Li, Y. Chen, and S. B. Gibson, “Starvation-induced autophagy is regulated by mitochondrial reactive oxygen species leading to AMPK activation,” Cellular Signalling, vol. 25, no. 1, pp. 50–65, 2013. View at Publisher · View at Google Scholar · View at Scopus
  34. S. Takikita, C. Schreiner, R. Baum et al., “Fiber type conversion by PGC-1α activates lysosomal and autophagosomal biogenesis in both unaffected and pompe skeletal muscle,” PLoS ONE, vol. 5, no. 12, Article ID e15239, 2010. View at Publisher · View at Google Scholar · View at Scopus
  35. K. Hollinger, D. Gardan-Salmon, C. Santana, D. Rice, E. Snella, and J. T. Selsby, “Rescue of dystrophic skeletal muscle by PGC-1α involves restored expression of dystrophin-associated protein complex components and satellite cell signaling,” The American Journal of Physiology: Regulatory Integrative and Comparative Physiology, vol. 305, no. 1, pp. R13–R23, 2013. View at Publisher · View at Google Scholar · View at Scopus
  36. T. Wenz, S. G. Rossi, R. L. Rotundo, B. M. Spiegelman, and C. T. Moraes, “Increased muscle PGC-1α expression protects from sarcopenia and metabolic disease during aging,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 48, pp. 20405–20410, 2009. View at Publisher · View at Google Scholar · View at Scopus
  37. I. Grattagliano, P. Portincasa, T. Cocco et al., “Effect of dietary restriction and N-acetylcysteine supplementation on intestinal mucosa and liver mitochondrial redox status and function in aged rats,” Experimental Gerontology, vol. 39, no. 9, pp. 1323–1332, 2004. View at Publisher · View at Google Scholar · View at Scopus
  38. S. Kumar and S. L. Sitasawad, “N-acetylcysteine prevents glucose/glucose oxidase-induced oxidative stress, mitochondrial damage and apoptosis in H9c2 cells,” Life Sciences, vol. 84, no. 11-12, pp. 328–336, 2009. View at Publisher · View at Google Scholar · View at Scopus
  39. L. Bevilacqua, J. J. Ramsey, K. Hagopian, R. Weindruch, and M.-E. Harper, “Effects of short- and medium-term calorie restriction on muscle mitochondrial proton leak and reactive oxygen species production,” The American Journal of Physiology: Endocrinology and Metabolism, vol. 286, no. 5, pp. E852–E861, 2004. View at Publisher · View at Google Scholar · View at Scopus
  40. S. S. Korshunov, V. P. Skulachev, and A. A. Starkov, “High protonic potential actuates a mechanism of production of reactive oxygen species in mitochondria,” FEBS Letters, vol. 416, no. 1, pp. 15–18, 1997. View at Publisher · View at Google Scholar · View at Scopus
  41. E. J. Anderson, M. E. Lustig, K. E. Boyle et al., “Mitochondrial H2O2 emission and cellular redox state link excess fat intake to insulin resistance in both rodents and humans,” Journal of Clinical Investigation, vol. 119, no. 3, pp. 573–581, 2009. View at Publisher · View at Google Scholar · View at Scopus
  42. V. M. Gohil, S. A. Sheth, R. Nilsson et al., “Nutrient-sensitized screening for drugs that shift energy metabolism from mitochondrial respiration to glycolysis,” Nature Biotechnology, vol. 28, no. 3, pp. 249–255, 2010. View at Publisher · View at Google Scholar · View at Scopus
  43. N. Parajuli and L. A. MacMillan-Crow, “Role of reduced manganese superoxide dismutase in ischemia-reperfusion injury: a possible trigger for autophagy and mitochondrial biogenesis?” The American Journal of Physiology: Renal Physiology, vol. 304, no. 3, pp. F257–F267, 2013. View at Publisher · View at Google Scholar · View at Scopus
  44. S. L. Mehta, Y. Lin, W. Chen et al., “Manganese superoxide dismutase deficiency exacerbates ischemic brain damage under hyperglycemic conditions by altering autophagy,” Translational Stroke Research, vol. 2, no. 1, pp. 42–50, 2011. View at Publisher · View at Google Scholar · View at Scopus
  45. Z. Li, K. Shi, L. Guan et al., “ROS leads to MnSOD upregulation through ERK2 translocation and p53 activation in selenite-induced apoptosis of NB4 cells,” FEBS Letters, vol. 584, no. 11, pp. 2291–2297, 2010. View at Publisher · View at Google Scholar · View at Scopus
  46. S. B. Mustafi, P. K. Chakraborty, R. S. Dey, and S. Raha, “Heat stress upregulates chaperone heat shock protein 70 and antioxidant manganese superoxide dismutase through reactive oxygen species (ROS), p38MAPK, and Akt,” Cell Stress and Chaperones, vol. 14, no. 6, pp. 579–589, 2009. View at Publisher · View at Google Scholar · View at Scopus
  47. K. Bensaad, E. C. Cheung, and K. H. Vousden, “Modulation of intracellular ROS levels by TIGAR controls autophagy,” EMBO Journal, vol. 28, no. 19, pp. 3015–3026, 2009. View at Publisher · View at Google Scholar · View at Scopus
  48. C. Wanka, J. P. Steinbach, and J. Rieger, “Tp53-induced glycolysis and apoptosis regulator (TIGAR) protects glioma cells from starvation-induced cell death by up-regulating respiration and improving cellular redox homeostasis,” Journal of Biological Chemistry, vol. 287, no. 40, pp. 33436–33446, 2012. View at Publisher · View at Google Scholar · View at Scopus
  49. A. Hoshino, S. Matoba, E. Iwai-Kanai et al., “P53-TIGAR axis attenuates mitophagy to exacerbate cardiac damage after ischemia,” Journal of Molecular and Cellular Cardiology, vol. 52, no. 1, pp. 175–184, 2012. View at Publisher · View at Google Scholar · View at Scopus
  50. E. C. Cheung, R. L. Ludwig, and K. H. Vousden, “Mitochondrial localization of TIGAR under hypoxia stimulates HK2 and lowers ROS and cell death,” Proceedings of the National Academy of Sciences of the United States of America, vol. 109, no. 50, pp. 20491–20496, 2012. View at Publisher · View at Google Scholar · View at Scopus
  51. E. Fernández-Vizarra, G. Ferrín, A. Pérez-Martos, P. Fernández-Silva, M. Zeviani, and J. A. Enríquez, “Isolation of mitochondria for biogenetical studies: an update,” Mitochondrion, vol. 10, no. 3, pp. 253–262, 2010. View at Publisher · View at Google Scholar · View at Scopus
  52. Z. Qi, J. He, Y. Su et al., “Physical exercise regulates p53 activity targeting SCO2 and increases Mitochondrial COX biogenesis in cardiac muscle with age,” PLoS ONE, vol. 6, no. 7, Article ID e21140, 2011. View at Publisher · View at Google Scholar · View at Scopus