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Oxidative Medicine and Cellular Longevity
Volume 2017, Article ID 2739721, 11 pages
https://doi.org/10.1155/2017/2739721
Research Article

Oleate Prevents Palmitate-Induced Atrophy via Modulation of Mitochondrial ROS Production in Skeletal Myotubes

1Division of Sports and Health Science, Kyungsung University, Busan, Republic of Korea
2Mechanical & Molecular Myology Lab, Department of Rehabilitation Medicine, College of Medicine, Seoul National University Bundang Hospital, Seongnam, Republic of Korea

Correspondence should be addressed to Seung-Jun Choi; rk.ca.sk@jsiohc

Received 22 May 2017; Revised 26 July 2017; Accepted 8 August 2017; Published 30 August 2017

Academic Editor: Jacek Zielonka

Copyright © 2017 Hojun Lee 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. S. C. Adams, R. J. Segal, M. K. DC et al., “Impact of resistance and aerobic exercise on sarcopenia and dynapenia in breast cancer patients receiving adjuvant chemotherapy: a multicenter randomized controlled trial,” Breast Cancer Research and Treatment, vol. 158, no. 3, pp. 497–507, 2016. View at Publisher · View at Google Scholar · View at Scopus
  2. W. K. Mitchell, J. Williams, P. Atherton, M. Larvin, J. Lund, and M. Narici, “Sarcopenia, dynapenia, and the impact of advancing age on human skeletal muscle size and strength; a quantitative review,” Frontiers in Physiology, vol. 3, p. 260, 2012. View at Publisher · View at Google Scholar · View at Scopus
  3. D. J. Tomlinson, R. M. Erskine, C. I. Morse, K. Winwood, and G. Onambélé-Pearson, “The impact of obesity on skeletal muscle strength and structure through adolescence to old age,” Biogerontology, vol. 17, no. 3, pp. 467–483, 2016. View at Publisher · View at Google Scholar · View at Scopus
  4. S. W. Park, B. H. Goodpaster, J. S. Lee et al., “Excessive loss of skeletal muscle mass in older adults with type 2 diabetes,” Diabetes Care, vol. 32, no. 11, pp. 1993–1997, 2009. View at Publisher · View at Google Scholar · View at Scopus
  5. R. W. Morton, C. McGlory, and S. M. Phillips, “Nutritional interventions to augment resistance training-induced skeletal muscle hypertrophy,” Frontiers in Physiology, vol. 6, p. 245, 2015. View at Publisher · View at Google Scholar · View at Scopus
  6. G. R. Adams and M. M. Bamman, “Characterization and regulation of mechanical loading-induced compensatory muscle hypertrophy,” Comprehensive Physiology, vol. 2, no. 4, pp. 2829–2870, 2012. View at Publisher · View at Google Scholar
  7. J. L. Areta, L. M. Burke, M. L. Ross et al., “Timing and distribution of protein ingestion during prolonged recovery from resistance exercise alters myofibrillar protein synthesis,” The Journal of Physiology, vol. 591, no. 9, pp. 2319–2331, 2013. View at Publisher · View at Google Scholar · View at Scopus
  8. C. Lipina and H. S. Hundal, “Lipid modulation of skeletal muscle mass and function,” Journal of Cachexia, Sarcopenia and Muscle, vol. 8, no. 2, pp. 190–201, 2017. View at Publisher · View at Google Scholar · View at Scopus
  9. M. Gueugneau, C. Coudy-Gandilhon, L. Théron et al., “Skeletal muscle lipid content and oxidative activity in relation to muscle fiber type in aging and metabolic syndrome,” The Journals of Gerontology. Series A, Biological Sciences and Medical Sciences, vol. 70, no. 5, pp. 566–576, 2015. View at Publisher · View at Google Scholar · View at Scopus
  10. W. Ogawa, T. Matozaki, and M. Kasuga, “Role of binding proteins to IRS-1 in insulin signalling,” Molecular and Cellular Biochemistry, vol. 182, no. 1-2, pp. 13–22, 1998. View at Publisher · View at Google Scholar · View at Scopus
  11. Y. Y. Lam, G. Hatzinikolas, J. M. Weir et al., “Insulin-stimulated glucose uptake and pathways regulating energy metabolism in skeletal muscle cells: the effects of subcutaneous and visceral fat, and long-chain saturated, n-3 and n-6 polyunsaturated fatty acids,” Biochimica et Biophysica Acta, vol. 1811, no. 7-8, pp. 468–475, 2011. View at Publisher · View at Google Scholar · View at Scopus
  12. J. M. Peterson, Y. Wang, R. W. Bryner, D. L. Williamson, and S. E. Alway, “Bax signaling regulates palmitate-mediated apoptosis in C2C12 myotubes,” American Journal of Physiology. Endocrinology and Metabolism, vol. 295, no. 6, pp. E1307–E1314, 2008. View at Publisher · View at Google Scholar · View at Scopus
  13. Y. Wei, K. Chen, A. T. Whaley-Connell, C. S. Stump, J. A. Ibdah, and J. R. Sowers, “Skeletal muscle insulin resistance: role of inflammatory cytokines and reactive oxygen species,” American Journal of Physiology. Regulatory, Integrative and Comparative Physiology, vol. 294, no. 3, pp. R673–R680, 2008. View at Publisher · View at Google Scholar · View at Scopus
  14. J. M. Park, J. S. Lee, J. E. Song, Y. C. Sim, S. J. Ha, and E. K. Hong, “Cytoprotective effect of hispidin against palmitate-induced lipotoxicity in C2C12 myotubes,” Molecules, vol. 20, no. 4, pp. 5456–5467, 2015. View at Publisher · View at Google Scholar · View at Scopus
  15. P. J. Moulton, “Inflammatory joint disease: the role of cytokines, cyclooxygenases and reactive oxygen species,” British Journal of Biomedical Science, vol. 53, no. 4, pp. 317–324, 1996. View at Google Scholar
  16. J. A. Chavez and S. A. Summers, “Characterizing the effects of saturated fatty acids on insulin signaling and ceramide and diacylglycerol accumulation in 3T3-L1 adipocytes and C2C12 myotubes,” Archives of Biochemistry and Biophysics, vol. 419, no. 2, pp. 101–109, 2003. View at Publisher · View at Google Scholar · View at Scopus
  17. N. Dimopoulos, M. Watson, K. Sakamoto, and H. S. Hundal, “Differential effects of palmitate and palmitoleate on insulin action and glucose utilization in rat L6 skeletal muscle cells,” The Biochemical Journal, vol. 399, no. 3, pp. 473–481, 2006. View at Publisher · View at Google Scholar · View at Scopus
  18. S. M. Hirabara, R. Curi, and P. Maechler, “Saturated fatty acid-induced insulin resistance is associated with mitochondrial dysfunction in skeletal muscle cells,” Journal of Cellular Physiology, vol. 222, no. 1, pp. 187–194, 2010. View at Publisher · View at Google Scholar · View at Scopus
  19. D. J. Powell, S. Turban, A. Gray, E. Hajduch, and H. S. Hundal, “Intracellular ceramide synthesis and protein kinase Cζ activation play an essential role in palmitate-induced insulin resistance in rat L6 skeletal muscle cells,” The Biochemical Journal, vol. 382, Part 2, pp. 619–629, 2004. View at Publisher · View at Google Scholar · View at Scopus
  20. C. Weigert, K. Brodbeck, H. Staiger et al., “Palmitate, but not unsaturated fatty acids, induces the expression of interleukin-6 in human myotubes through proteasome-dependent activation of nuclear factor-κB,” The Journal of Biological Chemistry, vol. 279, no. 23, pp. 23942–23952, 2004. View at Publisher · View at Google Scholar · View at Scopus
  21. T. Coll, M. Jové, R. Rodríguez-Calvo et al., “Palmitate-mediated downregulation of peroxisome proliferator-activated receptor-γ coactivator 1α in skeletal muscle cells involves MEK1/2 and nuclear factor-κB activation,” Diabetes, vol. 55, no. 10, pp. 2779–2787, 2006. View at Publisher · View at Google Scholar · View at Scopus
  22. J. H. Lim, Z. Gerhart-Hines, J. E. Dominy et al., “Oleic acid stimulates complete oxidation of fatty acids through protein kinase A-dependent activation of SIRT1-PGC1α complex,” The Journal of Biological Chemistry, vol. 288, no. 10, pp. 7117–7126, 2013. View at Publisher · View at Google Scholar · View at Scopus
  23. R. W. Bryner, M. E. Woodworth-Hobbs, D. L. Williamson, and S. E. Alway, “Docosahexaenoic acid protects muscle cells from palmitate-induced atrophy,” ISRN Obesity, vol. 2012, Article ID 647348, 14 pages, 2012. View at Publisher · View at Google Scholar
  24. N. J. Pillon, K. Arane, P. J. Bilan, T. T. Chiu, and A. Klip, “Muscle cells challenged with saturated fatty acids mount an autonomous inflammatory response that activates macrophages,” Cell Communication and Signaling: CCS, vol. 10, no. 1, p. 30, 2012. View at Publisher · View at Google Scholar · View at Scopus
  25. Y. P. Li, C. M. Atkins, J. D. Sweatt, and M. B. Reid, “Mitochondria mediate tumor necrosis factor-α/NF-κB signaling in skeletal muscle myotubes,” Antioxidants & Redox Signaling, vol. 1, no. 1, pp. 97–104, 1999. View at Publisher · View at Google Scholar
  26. I. Kosmidou, T. Vassilakopoulos, A. Xagorari, S. Zakynthinos, A. Papapetropoulos, and C. Roussos, “Production of interleukin-6 by skeletal myotubes: role of reactive oxygen species,” American Journal of Respiratory Cell and Molecular Biology, vol. 26, no. 5, pp. 587–593, 2002. View at Publisher · View at Google Scholar
  27. C. Paolini, M. Quarta, L. Wei-LaPierre et al., “Oxidative stress, mitochondrial damage, and cores in muscle from calsequestrin-1 knockout mice,” Skeletal Muscle, vol. 5, p. 10, 2015. View at Publisher · View at Google Scholar · View at Scopus
  28. H. Cui, Y. Kong, and H. Zhang, “Oxidative stress, mitochondrial dysfunction, and aging,” Journal of Signal Transduction, vol. 2012, Article ID 646354, 13 pages, 2012. View at Publisher · View at Google Scholar
  29. X. Gao, X. L. Zhao, Y. H. Zhu et al., “Tetramethylpyrazine protects palmitate-induced oxidative damage and mitochondrial dysfunction in C2C12 myotubes,” Life Sciences, vol. 88, no. 17-18, pp. 803–809, 2011. View at Publisher · View at Google Scholar · View at Scopus
  30. B. Kwon, H. K. Lee, and H. W. Querfurth, “Oleate prevents palmitate-induced mitochondrial dysfunction, insulin resistance and inflammatory signaling in neuronal cells,” Biochimica et Biophysica Acta, vol. 1843, no. 7, pp. 1402–1413, 2014. View at Publisher · View at Google Scholar · View at Scopus
  31. Y. Tsuchiya, H. Hatakeyama, N. Emoto, F. Wagatsuma, S. Matsushita, and M. Kanzaki, “Palmitate-induced down-regulation of sortilin and impaired GLUT4 trafficking in C2C12 myotubes,” The Journal of Biological Chemistry, vol. 285, no. 45, pp. 34371–34381, 2010. View at Publisher · View at Google Scholar · View at Scopus
  32. B. T. Wall, J. P. Morton, and L. J. v. Loon, “Strategies to maintain skeletal muscle mass in the injured athlete: nutritional considerations and exercise mimetics,” European Journal of Sport Science, vol. 15, no. 1, pp. 53–62, 2015. View at Publisher · View at Google Scholar · View at Scopus
  33. S. Jeromson, I. J. Gallagher, S. D. Galloway, and D. L. Hamilton, “Omega-3 fatty acids and skeletal muscle health,” Marine Drugs, vol. 13, no. 11, pp. 6977–7004, 2015. View at Publisher · View at Google Scholar · View at Scopus
  34. L. P. Turcotte and J. S. Fisher, “Skeletal muscle insulin resistance: roles of fatty acid metabolism and exercise,” Physical Therapy, vol. 88, no. 11, pp. 1279–1296, 2008. View at Publisher · View at Google Scholar · View at Scopus
  35. M. Yang, D. Wei, C. Mo et al., “Saturated fatty acid palmitate-induced insulin resistance is accompanied with myotube loss and the impaired expression of health benefit myokine genes in C2C12 myotubes,” Lipids in Health and Disease, vol. 12, p. 104, 2013. View at Publisher · View at Google Scholar · View at Scopus
  36. P. Mishra, G. Varuzhanyan, A. H. Pham, and D. C. Chan, “Mitochondrial dynamics is a distinguishing feature of skeletal muscle fiber types and regulates organellar compartmentalization,” Cell Metabolism, vol. 22, no. 6, pp. 1033–1044, 2015. View at Publisher · View at Google Scholar · View at Scopus
  37. A. P. Russell, V. C. Foletta, R. J. Snow, and G. D. Wadley, “Skeletal muscle mitochondria: a major player in exercise, health and disease,” Biochimica et Biophysica Acta, vol. 1840, no. 4, pp. 1276–1284, 2014. View at Publisher · View at Google Scholar · View at Scopus
  38. S. K. Powers, M. P. Wiggs, J. A. Duarte, A. M. Zergeroglu, and H. A. Demirel, “Mitochondrial signaling contributes to disuse muscle atrophy,” American Journal of Physiology Endocrinology and Metabolism, vol. 303, no. 1, pp. E31–E39, 2012. View at Publisher · View at Google Scholar · View at Scopus
  39. S. Javadov, S. Jang, N. Rodriguez-Reyes et al., “Mitochondria-targeted antioxidant preserves contractile properties and mitochondrial function of skeletal muscle in aged rats,” Oncotarget, vol. 6, no. 37, pp. 39469–39481, 2015. View at Publisher · View at Google Scholar · View at Scopus
  40. B. Kim, J. S. Kim, Y. Yoon, M. C. Santiago, M. D. Brown, and J. Y. Park, “Inhibition of Drp1-dependent mitochondrial division impairs myogenic differentiation,” American Journal of Physiology Regulatory, Integrative and Comparative Physiology, vol. 305, no. 8, pp. R927–R938, 2013. View at Publisher · View at Google Scholar · View at Scopus
  41. C. Mammucari, G. Gherardi, I. Zamparo et al., “The mitochondrial calcium uniporter controls skeletal muscle trophism in vivo,” Cell Reports, vol. 10, no. 8, pp. 1269–1279, 2015. View at Publisher · View at Google Scholar · View at Scopus
  42. A. Wiederkehr and C. B. Wollheim, “Linking fatty acid stress to β-cell mitochondrial dynamics,” Diabetes, vol. 58, no. 10, pp. 2185-2186, 2009. View at Publisher · View at Google Scholar · View at Scopus
  43. T. Wai and T. Langer, “Mitochondrial dynamics and metabolic regulation,” Trends in Endocrinology and Metabolism, vol. 27, no. 2, pp. 105–117, 2016. View at Publisher · View at Google Scholar · View at Scopus
  44. M. Picard, O. S. Shirihai, B. J. Gentil, and Y. Burelle, “Mitochondrial morphology transitions and functions: implications for retrograde signaling?” American Journal of Physiology. Regulatory, Integrative and Comparative Physiology, vol. 304, no. 6, pp. R393–R406, 2013. View at Publisher · View at Google Scholar · View at Scopus
  45. S. Wu, F. Zhou, Z. Zhang, and D. Xing, “Mitochondrial oxidative stress causes mitochondrial fragmentation via differential modulation of mitochondrial fission-fusion proteins,” The FEBS Journal, vol. 278, no. 6, pp. 941–954, 2011. View at Publisher · View at Google Scholar · View at Scopus
  46. V. Romanello, E. Guadagnin, L. Gomes et al., “Mitochondrial fission and remodelling contributes to muscle atrophy,” The EMBO Journal, vol. 29, no. 10, pp. 1774–1785, 2010. View at Publisher · View at Google Scholar · View at Scopus
  47. S. Frank, B. Gaume, E. S. Bergmann-Leitner et al., “The role of dynamin-related protein 1, a mediator of mitochondrial fission, in apoptosis,” Developmental Cell, vol. 1, no. 4, pp. 515–525, 2001. View at Publisher · View at Google Scholar · View at Scopus
  48. S. M. Hirabara, L. R. Silveira, L. C. Alberici et al., “Acute effect of fatty acids on metabolism and mitochondrial coupling in skeletal muscle,” Biochimica et Biophysica Acta (BBA) - Bioenergetics, vol. 1757, no. 1, pp. 57–66, 2006. View at Publisher · View at Google Scholar · View at Scopus
  49. U. Spate and P. C. Schulze, “Proinflammatory cytokines and skeletal muscle,” Current Opinion in Clinical Nutrition and Metabolic Care, vol. 7, no. 3, pp. 265–269, 2004. View at Publisher · View at Google Scholar · View at Scopus
  50. E. Kaufman, S. Hall, Y. Surova, H. Widner, O. Hansson, and D. Lindqvist, “Proinflammatory cytokines are elevated in serum of patients with multiple system atrophy,” PloS One, vol. 8, no. 4, article e62354, 2013. View at Publisher · View at Google Scholar · View at Scopus
  51. A. Maeda and B. Fadeel, “Mitochondria released by cells undergoing TNF-α-induced necroptosis act as danger signals,” Cell Death & Disease, vol. 5, article e1312, 2014. View at Publisher · View at Google Scholar · View at Scopus
  52. J. H. Yoon, D. Kim, J. H. Jang et al., “Proteomic analysis of the palmitate-induced myotube secretome reveals involvement of the annexin A1-formyl peptide receptor 2 (FPR2) pathway in insulin resistance,” Molecular & Cellular Proteomics, vol. 14, no. 4, pp. 882–892, 2015. View at Publisher · View at Google Scholar · View at Scopus
  53. K. A. Cho, M. Park, Y. H. Kim, S. Y. Woo, and K. H. Ryu, “Conditioned media from human palatine tonsil mesenchymal stem cells regulates the interaction between myotubes and fibroblasts by IL-1Ra activity,” Journal of Cellular and Molecular Medicine, vol. 21, no. 1, pp. 130–141, 2017. View at Publisher · View at Google Scholar
  54. N. Huang, M. Kny, F. Riediger et al., “Deletion of Nlrp3 protects from inflammation-induced skeletal muscle atrophy,” Intensive Care Medicine Experimental, vol. 5, no. 1, p. 3, 2017. View at Publisher · View at Google Scholar
  55. S. Acharyya, K. J. Ladner, L. L. Nelsen et al., “Cancer cachexia is regulated by selective targeting of skeletal muscle gene products,” The Journal of Clinical Investigation, vol. 114, no. 3, pp. 370–378, 2004. View at Publisher · View at Google Scholar
  56. D. C. Guttridge, M. W. Mayo, L. V. Madrid, C. Y. Wang, and A. S. Baldwin Jr., “NF-κB-induced loss of MyoD messenger RNA: possible role in muscle decay and cachexia,” Science, vol. 289, no. 5488, pp. 2363–2366, 2000. View at Publisher · View at Google Scholar · View at Scopus
  57. L. L. Moldawer, G. Svaninger, J. Gelin, and K. G. Lundholm, “Interleukin 1 and tumor necrosis factor do not regulate protein balance in skeletal muscle,” The American Journal of Physiology, vol. 253, no. 6, Part 1, pp. C766–C773, 1987. View at Google Scholar
  58. H. M. Alessio, A. H. Goldfarb, and R. G. Cutler, “MDA content increases in fast- and slow-twitch skeletal muscle with intensity of exercise in a rat,” The American Journal of Physiology, vol. 255, no. 6, Part 1, pp. C874–C877, 1988. View at Google Scholar
  59. M. B. Reid, K. E. Haack, K. M. Franchek, P. A. Valberg, L. Kobzik, and M. S. West, “Reactive oxygen in skeletal muscle. I. Intracellular oxidant kinetics and fatigue in vitro,” Journal of Applied Physiology, vol. 73, no. 5, pp. 1797–1804, 1992. View at Google Scholar
  60. A. R. Martins, R. T. Nachbar, R. Gorjao et al., “Mechanisms underlying skeletal muscle insulin resistance induced by fatty acids: importance of the mitochondrial function,” Lipids in Health and Disease, vol. 11, p. 30, 2012. View at Publisher · View at Google Scholar · View at Scopus
  61. W. Droge, “Free radicals in the physiological control of cell function,” Physiological Reviews, vol. 82, no. 1, pp. 47–95, 2002. View at Publisher · View at Google Scholar
  62. M. Valko, D. Leibfritz, J. Moncol, M. T. Cronin, M. Mazur, and J. Telser, “Free radicals and antioxidants in normal physiological functions and human disease,” The International Journal of Biochemistry & Cell Biology, vol. 39, no. 1, pp. 44–84, 2007. View at Publisher · View at Google Scholar · View at Scopus
  63. M. B. Reid, “Nitric oxide, reactive oxygen species, and skeletal muscle contraction,” Medicine and Science in Sports and Exercise, vol. 33, no. 3, pp. 371–376, 2001. View at Publisher · View at Google Scholar
  64. T. L. Merry and G. K. McConell, “Skeletal muscle glucose uptake during exercise: a focus on reactive oxygen species and nitric oxide signaling,” IUBMB Life, vol. 61, no. 5, pp. 479–484, 2009. View at Publisher · View at Google Scholar · View at Scopus
  65. K. L. Pokrzywinski, T. G. Biel, D. Kryndushkin, and V. A. Rao, “Therapeutic targeting of the mitochondria initiates excessive superoxide production and mitochondrial depolarization causing decreased mtDNA integrity,” PloS One, vol. 11, no. 12, article e0168283, 2016. View at Publisher · View at Google Scholar · View at Scopus
  66. A. E. Dikalova, A. T. Bikineyeva, K. Budzyn et al., “Therapeutic targeting of mitochondrial superoxide in hypertension,” Circulation Research, vol. 107, no. 1, pp. 106–116, 2010. View at Publisher · View at Google Scholar · View at Scopus
  67. E. M. Jeong, J. Chung, H. Liu et al., “Role of mitochondrial oxidative stress in glucose tolerance, insulin resistance, and cardiac diastolic dysfunction,” Journal of the American Heart Association, vol. 5, no. 5, 2016. View at Publisher · View at Google Scholar
  68. X. Wang, Z. Hu, J. Hu, J. Du, and W. E. Mitch, “Insulin resistance accelerates muscle protein degradation: activation of the ubiquitin-proteasome pathway by defects in muscle cell signaling,” Endocrinology, vol. 147, no. 9, pp. 4160–4168, 2006. View at Publisher · View at Google Scholar · View at Scopus
  69. M. A. Honors and K. P. Kinzig, “The role of insulin resistance in the development of muscle wasting during cancer cachexia,” Journal of Cachexia, Sarcopenia and Muscle, vol. 3, no. 1, pp. 5–11, 2012. View at Publisher · View at Google Scholar · View at Scopus