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Oxidative Medicine and Cellular Longevity
Volume 2018 (2018), Article ID 2063179, 17 pages
https://doi.org/10.1155/2018/2063179
Review Article

Role of Oxidative Stress as Key Regulator of Muscle Wasting during Cachexia

1Departamento de Ciencias Biológicas, Facultad de Ciencias Biológicas, Universidad Andres Bello, Santiago, Chile
2Millennium Institute of Immunology and Immunotherapy, Santiago, Chile
3Centro de Investigaciones Biomédicas, Facultad de Ciencias Biológicas & Facultad de Medicina, Universidad Andres Bello, Santiago, Chile
4Laboratory of Nanomedicine and Targeted Delivery, Center for Integrative Medicine and Innovative Science, Faculty of Medicine, and Center for Bioinformatics and Integrative Biology, Faculty of Biological Sciences, Universidad Andres Bello, Santiago, Chile
5Center for the Development of Nanoscience and Nanotechnology (CEDENNA), Universidad de Santiago de Chile, Santiago, Chile
6Departamento de Gastroenterología, Facultad de Medicina, Pontificia Universidad Católica de Chile, Santiago, Chile
7Departamento de Ciencias Químicas y Biológicas, Facultad de Salud, Universidad Bernardo O’Higgins, Santiago, Chile
8Centro Integrativo de Biología y Química Aplicada, Universidad Bernardo O’Higgins, Santiago, Chile

Correspondence should be addressed to Claudio Cabello-Verrugio; lc.banu@ollebac.oidualc

Received 11 November 2017; Accepted 7 February 2018; Published 28 March 2018

Academic Editor: Rodrigo Franco

Copyright © 2018 Johanna Ábrigo 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. R. W. Jackman and S. C. Kandarian, “The molecular basis of skeletal muscle atrophy,” American Journal of Physiology-Cell Physiology, vol. 287, no. 4, pp. C834–C843, 2004. View at Publisher · View at Google Scholar · View at Scopus
  2. P. Bonaldo and M. Sandri, “Cellular and molecular mechanisms of muscle atrophy,” Disease Models & Mechanisms, vol. 6, no. 1, pp. 25–39, 2013. View at Publisher · View at Google Scholar · View at Scopus
  3. A. Fanzani, V. M. Conraads, F. Penna, and W. Martinet, “Molecular and cellular mechanisms of skeletal muscle atrophy: an update,” Journal of Cachexia, Sarcopenia and Muscle, vol. 3, no. 3, pp. 163–179, 2012. View at Publisher · View at Google Scholar · View at Scopus
  4. N. E. Brooks and K. H. Myburgh, “Skeletal muscle wasting with disuse atrophy is multi-dimensional: the response and interaction of myonuclei, satellite cells and signaling pathways,” Frontiers in Physiology, vol. 5, p. 99, 2014. View at Publisher · View at Google Scholar · View at Scopus
  5. D. M. Callahan, M. S. Miller, A. P. Sweeny et al., “Muscle disuse alters skeletal muscle contractile function at the molecular and cellular levels in older adult humans in a sex-specific manner,” The Journal of Physiology, vol. 592, no. 20, pp. 4555–4573, 2014. View at Publisher · View at Google Scholar · View at Scopus
  6. M. S. Miller, D. M. Callahan, and M. J. Toth, “Skeletal muscle myofilament adaptations to aging, disease, and disuse and their effects on whole muscle performance in older adult humans,” Frontiers in Physiology, vol. 5, p. 369, 2014. View at Publisher · View at Google Scholar · View at Scopus
  7. S. C. Bodine, “Disuse-induced muscle wasting,” The International Journal of Biochemistry & Cell Biology, vol. 45, no. 10, pp. 2200–2208, 2013. View at Publisher · View at Google Scholar · View at Scopus
  8. F. W. Booth and P. D. Gollnick, “Effects of disuse on the structure and function of skeletal muscle,” Medicine & Science in Sports & Exercise, vol. 15, no. 5, pp. 415–420, 1983. View at Publisher · View at Google Scholar
  9. Y. Ohira, T. Yoshinaga, T. Nomura et al., “Gravitational unloading effects on muscle fiber size, phenotype and myonuclear number,” Advances in Space Research, vol. 30, no. 4, pp. 777–781, 2002. View at Publisher · View at Google Scholar · View at Scopus
  10. M. D. Allen, D. W. Stashuk, K. Kimpinski, T. J. Doherty, M. L. Hourigan, and C. L. Rice, “Increased neuromuscular transmission instability and motor unit remodelling with diabetic neuropathy as assessed using novel near fibre motor unit potential parameters,” Clinical Neurophysiology, vol. 126, no. 4, pp. 794–802, 2015. View at Publisher · View at Google Scholar · View at Scopus
  11. B. M. Carlson, “The biology of long-term denervated skeletal muscle,” European Journal of Translational Myology, vol. 24, no. 1, pp. 3293–3293, 2014. View at Publisher · View at Google Scholar
  12. M. J. Castro, D. F. Apple Jr, E. A. Hillegass, and G. A. Dudley, “Influence of complete spinal cord injury on skeletal muscle cross-sectional area within the first 6 months of injury,” European Journal of Applied Physiology and Occupational Physiology, vol. 80, no. 4, pp. 373–378, 1999. View at Publisher · View at Google Scholar · View at Scopus
  13. Y. Dionyssiotis, K. Stathopoulos, G. Trovas, N. Papaioannou, G. Skarantavos, and P. Papagelopoulos, “Impact on bone and muscle area after spinal cord injury,” BoneKEy Reports, vol. 4, p. 633, 2015. View at Publisher · View at Google Scholar
  14. L. Giangregorio and N. McCartney, “Bone loss and muscle atrophy in spinal cord injury: epidemiology, fracture prediction, and rehabilitation strategies,” The Journal of Spinal Cord Medicine, vol. 29, no. 5, pp. 489–500, 2006. View at Publisher · View at Google Scholar · View at Scopus
  15. R. R. Roy, K. M. Baldwin, and V. R. Edgerton, “8 The plasticity of skeletal muscle: effects of neuromuscular activity,” Exercise and Sport Sciences Reviews, vol. 19, pp. 269–312, 1991. View at Publisher · View at Google Scholar
  16. S. L. Rowan, K. Rygiel, F. M. Purves-Smith, N. M. Solbak, D. M. Turnbull, and R. T. Hepple, “Denervation causes fiber atrophy and myosin heavy chain co-expression in senescent skeletal muscle,” PLoS One, vol. 7, no. 1, article e29082, 2012. View at Publisher · View at Google Scholar · View at Scopus
  17. A. Doyle, G. Zhang, E. A. Abdel Fattah, N. T. Eissa, and Y. P. Li, “Toll-like receptor 4 mediates lipopolysaccharide-induced muscle catabolism via coordinate activation of ubiquitin-proteasome and autophagy-lysosome pathways,” The FASEB Journal, vol. 25, no. 1, pp. 99–110, 2011. View at Publisher · View at Google Scholar · View at Scopus
  18. G. Tiao, S. Hobler, J. J. Wang et al., “Sepsis is associated with increased mRNAs of the ubiquitin-proteasome proteolytic pathway in human skeletal muscle,” The Journal of Clinical Investigation, vol. 99, no. 2, pp. 163–168, 1997. View at Publisher · View at Google Scholar · View at Scopus
  19. G. Tiao, M. Lieberman, J. E. Fischer, and P. O. Hasselgren, “Intracellular regulation of protein degradation during sepsis is different in fast- and slow-twitch muscle,” The American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, vol. 272, 3 Part 2, pp. R849–R856, 1997. View at Publisher · View at Google Scholar
  20. M. R. Pinsky, “Dysregulation of the immune response in severe sepsis,” The American Journal of the Medical Sciences, vol. 328, no. 4, pp. 220–229, 2004. View at Publisher · View at Google Scholar · View at Scopus
  21. M. J. Dehoux, R. P. van Beneden, L. Fernández-Celemín, P. L. Lause, and J. P. Thissen, “Induction of MafBx and Murf ubiquitin ligase mRNAs in rat skeletal muscle after LPS injection,” FEBS Letters, vol. 544, no. 1–3, pp. 214–217, 2003. View at Publisher · View at Google Scholar · View at Scopus
  22. M. Vinciguerra, A. Musaro, and N. Rosenthal, “Regulation of muscle atrophy in aging and disease,” Advances in Experimental Medicine and Biology, vol. 694, pp. 211–233, 2010. View at Publisher · View at Google Scholar · View at Scopus
  23. W. J. Evans and W. W. Campbell, “Sarcopenia and age-related changes in body composition and functional capacity,” The Journal of Nutrition, vol. 123, Supplement 2, pp. 465–468, 1993. View at Publisher · View at Google Scholar
  24. R. A. Dennis, B. Przybyla, C. Gurley et al., “Aging alters gene expression of growth and remodeling factors in human skeletal muscle both at rest and in response to acute resistance exercise,” Physiological Genomics, vol. 32, no. 3, pp. 393–400, 2008. View at Publisher · View at Google Scholar · View at Scopus
  25. P. Kortebein, A. Ferrando, J. Lombeida, R. Wolfe, and W. J. Evans, “Effect of 10 days of bed rest on skeletal muscle in healthy older adults,” JAMA, vol. 297, no. 16, pp. 1769–1774, 2007. View at Publisher · View at Google Scholar
  26. M. Cesari, S. B. Kritchevsky, R. N. Baumgartner et al., “Sarcopenia, obesity, and inflammation—results from the Trial of Angiotensin Converting Enzyme Inhibition and Novel Cardiovascular Risk Factors study,” The American Journal of Clinical Nutrition, vol. 82, no. 2, pp. 428–434, 2005. View at Publisher · View at Google Scholar
  27. M. Cesari, B. W. Penninx, M. Pahor et al., “Inflammatory markers and physical performance in older persons: the InCHIANTI study,” The Journals of Gerontology Series A: Biological Sciences and Medical Sciences, vol. 59, no. 3, pp. M242–M248, 2004. View at Publisher · View at Google Scholar
  28. W. R. Frontera, V. A. Hughes, R. A. Fielding, M. A. Fiatarone, W. J. Evans, and R. Roubenoff, “Aging of skeletal muscle: a 12-yr longitudinal study,” Journal of Applied Physiology, vol. 88, no. 4, pp. 1321–1326, 2000. View at Publisher · View at Google Scholar
  29. V. E. Baracos, L. Martin, M. Korc, D. C. Guttridge, and K. C. H. Fearon, “Cancer-associated cachexia,” Nature Reviews Disease Primers, vol. 4, article 17105, 2018. View at Publisher · View at Google Scholar
  30. K. A. Kern and J. A. Norton, “Cancer cachexia,” JPEN Journal of Parenteral and Enteral Nutrition, vol. 12, no. 3, pp. 286–298, 1988. View at Publisher · View at Google Scholar · View at Scopus
  31. M. J. Tisdale, “Cachexia in cancer patients,” Nature Reviews Cancer, vol. 2, no. 11, pp. 862–871, 2002. View at Publisher · View at Google Scholar · View at Scopus
  32. Y. J. Akashi, J. Springer, and S. D. Anker, “Cachexia in chronic heart failure: prognostic implications and novel therapeutic approaches,” Current Heart Failure Reports, vol. 2, no. 4, pp. 198–203, 2005. View at Publisher · View at Google Scholar
  33. M. P. Okoshi, F. G. Romeiro, S. A. Paiva, and K. Okoshi, “Heart failure-induced cachexia,” Arquivos Brasileiros de Cardiologia, vol. 100, no. 5, pp. 476–482, 2013. View at Publisher · View at Google Scholar · View at Scopus
  34. M. Plauth and E. T. Schutz, “Cachexia in liver cirrhosis,” International Journal of Cardiology, vol. 85, no. 1, pp. 83–87, 2002. View at Publisher · View at Google Scholar · View at Scopus
  35. A. Laviano, Z. Krznaric, K. Sanchez-Lara, I. Preziosa, A. Cascino, and F. Rossi Fanelli, “Chronic renal failure, cachexia, and ghrelin,” International Journal of Peptide, vol. 2010, Article ID 648045, 5 pages, 2010. View at Publisher · View at Google Scholar · View at Scopus
  36. R. H. Mak, A. T. Ikizler, C. P. Kovesdy, D. S. Raj, P. Stenvinkel, and K. Kalantar-Zadeh, “Wasting in chronic kidney disease,” Journal of Cachexia, Sarcopenia and Muscle, vol. 2, no. 1, pp. 9–25, 2011. View at Publisher · View at Google Scholar · View at Scopus
  37. B. C. Frier, E. G. Noble, and M. Locke, “Diabetes-induced atrophy is associated with a muscle-specific alteration in NF-κB activation and expression,” Cell Stress and Chaperones, vol. 13, no. 3, pp. 287–296, 2008. View at Publisher · View at Google Scholar · View at Scopus
  38. B. Sishi, B. Loos, B. Ellis, W. Smith, E. F. du Toit, and A. M. Engelbrecht, “Diet-induced obesity alters signalling pathways and induces atrophy and apoptosis in skeletal muscle in a prediabetic rat model,” Experimental Physiology, vol. 96, no. 2, pp. 179–193, 2011. View at Publisher · View at Google Scholar · View at Scopus
  39. W. J. Evans, J. E. Morley, J. Argilés et al., “Cachexia: a new definition,” Clinical Nutrition, vol. 27, no. 6, pp. 793–799, 2008. View at Publisher · View at Google Scholar · View at Scopus
  40. J. E. Morley, D. R. Thomas, and M. M. Wilson, “Cachexia: pathophysiology and clinical relevance,” The American Journal of Clinical Nutrition, vol. 83, no. 4, pp. 735–743, 2006. View at Publisher · View at Google Scholar
  41. S. D. Anker and R. Sharma, “The syndrome of cardiac cachexia,” International Journal of Cardiology, vol. 85, no. 1, pp. 51–66, 2002. View at Publisher · View at Google Scholar · View at Scopus
  42. S. von Haehling and S. D. Anker, “Prevalence, incidence and clinical impact of cachexia: facts and numbers—update 2014,” Journal of Cachexia, Sarcopenia and Muscle, vol. 5, no. 4, pp. 261–263, 2014. View at Publisher · View at Google Scholar · View at Scopus
  43. L. M. Leitner, R. J. Wilson, Z. Yan, and A. Gödecke, “Reactive oxygen species/nitric oxide mediated inter-organ communication in skeletal muscle wasting diseases,” Antioxidants & Redox Signaling, vol. 26, no. 13, pp. 700–717, 2017. View at Publisher · View at Google Scholar · View at Scopus
  44. J. M. Argilés, S. Busquets, B. Stemmler, and F. J. López-Soriano, “Cancer cachexia: understanding the molecular basis,” Nature Reviews Cancer, vol. 14, no. 11, pp. 754–762, 2014. View at Publisher · View at Google Scholar · View at Scopus
  45. C. Cabello-Verrugio, G. Cordova, and J. D. Salas, “Angiotensin II: role in skeletal muscle atrophy,” Current Protein & Peptide Science, vol. 13, no. 6, pp. 560–569, 2012. View at Publisher · View at Google Scholar · View at Scopus
  46. P. Du Bois, C. Pablo Tortola, D. Lodka et al., “Angiotensin II induces skeletal muscle atrophy by activating TFEB-mediated MuRF1 expression,” Circulation Research, vol. 117, no. 5, pp. 424–436, 2015. View at Publisher · View at Google Scholar · View at Scopus
  47. S. Sukhanov, T. Yoshida, A. Michael Tabony et al., “Angiotensin II, oxidative stress and skeletal muscle wasting,” The American Journal of the Medical Sciences, vol. 342, no. 2, pp. 143–147, 2011. View at Publisher · View at Google Scholar · View at Scopus
  48. J. Abrigo, J. C. Rivera, F. Simon, D. Cabrera, and C. Cabello-Verrugio, “Transforming growth factor type beta (TGF-β) requires reactive oxygen species to induce skeletal muscle atrophy,” Cellular Signalling, vol. 28, no. 5, pp. 366–376, 2016. View at Publisher · View at Google Scholar · View at Scopus
  49. C. L. Mendias, J. P. Gumucio, M. E. Davis, C. W. Bromley, C. S. Davis, and S. V. Brooks, “Transforming growth factor-beta induces skeletal muscle atrophy and fibrosis through the induction of atrogin-1 and scleraxis,” Muscle & Nerve, vol. 45, no. 1, pp. 55–59, 2012. View at Publisher · View at Google Scholar · View at Scopus
  50. M. B. Reid and Y. P. Li, “Tumor necrosis factor-α and muscle wasting: a cellular perspective,” Respiratory Research, vol. 2, no. 5, pp. 269–272, 2001. View at Publisher · View at Google Scholar · View at Scopus
  51. F. Haddad, F. Zaldivar, D. M. Cooper, and G. R. Adams, “IL-6-induced skeletal muscle atrophy,” Journal of Applied Physiology, vol. 98, no. 3, pp. 911–917, 2005. View at Publisher · View at Google Scholar · View at Scopus
  52. S. P. Janssen, G. Gayan-Ramirez, A. van den Bergh et al., “Interleukin-6 causes myocardial failure and skeletal muscle atrophy in rats,” Circulation, vol. 111, no. 8, pp. 996–1005, 2005. View at Publisher · View at Google Scholar · View at Scopus
  53. O. Zamir, P. O. Hasselgren, T. Higashiguchi, J. A. Frederick, and J. E. Fischer, “Tumour necrosis factor (TNF) and interleukin-1 (IL-1) induce muscle proteolysis through different mechanisms,” Mediators of Inflammation, vol. 1, no. 4, pp. 247–250, 1992. View at Publisher · View at Google Scholar · View at Scopus
  54. B. M. Rezk, T. Yoshida, L. Semprun-Prieto, Y. Higashi, S. Sukhanov, and P. Delafontaine, “Angiotensin II infusion induces marked diaphragmatic skeletal muscle atrophy,” PLoS One, vol. 7, no. 1, article e30276, 2012. View at Publisher · View at Google Scholar · View at Scopus
  55. T. Kadoguchi, S. Kinugawa, S. Takada et al., “Angiotensin II can directly induce mitochondrial dysfunction, decrease oxidative fibre number and induce atrophy in mouse hindlimb skeletal muscle,” Experimental Physiology, vol. 100, no. 3, pp. 312–322, 2015. View at Publisher · View at Google Scholar · View at Scopus
  56. C. W. Keller, C. Fokken, S. G. Turville et al., “TNF-α induces macroautophagy and regulates MHC class II expression in human skeletal muscle cells,” The Journal of Biological Chemistry, vol. 286, no. 5, pp. 3970–3980, 2011. View at Publisher · View at Google Scholar · View at Scopus
  57. J. Y. Lee, N. S. Hopkinson, and P. R. Kemp, “Myostatin induces autophagy in skeletal muscle in vitro,” Biochemical and Biophysical Research Communications, vol. 415, no. 4, pp. 632–636, 2011. View at Publisher · View at Google Scholar · View at Scopus
  58. Y. P. Li, Y. Chen, J. John et al., “TNF-α acts via p38 MAPK to stimulate expression of the ubiquitin ligase atrogin1/MAFbx in skeletal muscle,” The FASEB Journal, vol. 19, no. 3, pp. 362–370, 2005. View at Publisher · View at Google Scholar · View at Scopus
  59. P. M. Sanders, S. T. Russell, and M. J. Tisdale, “Angiotensin II directly induces muscle protein catabolism through the ubiquitin-proteasome proteolytic pathway and may play a role in cancer cachexia,” British Journal of Cancer, vol. 93, no. 4, pp. 425–434, 2005. View at Publisher · View at Google Scholar · View at Scopus
  60. Y. P. Li, R. J. Schwartz, I. D. Waddell, B. R. Holloway, and M. B. Reid, “Skeletal muscle myocytes undergo protein loss and reactive oxygen-mediated NF-ĸB activation in response to tumor necrosis factor α,” The FASEB Journal, vol. 12, no. 10, pp. 871–880, 1998. View at Publisher · View at Google Scholar
  61. A. Laviano, M. M. Meguid, I. Preziosa, and F. R. Fanelli, “Oxidative stress and wasting in cancer,” Current Opinion in Clinical Nutrition and Metabolic Care, vol. 10, no. 4, pp. 449–456, 2007. View at Publisher · View at Google Scholar · View at Scopus
  62. M. C. Gomes-Marcondes and M. J. Tisdale, “Induction of protein catabolism and the ubiquitin-proteasome pathway by mild oxidative stress,” Cancer Letters, vol. 180, no. 1, pp. 69–74, 2002. View at Publisher · View at Google Scholar · View at Scopus
  63. S. K. Powers, A. B. Morton, B. Ahn, and A. J. Smuder, “Redox control of skeletal muscle atrophy,” Free Radical Biology and Medicine, vol. 98, pp. 208–217, 2016. View at Publisher · View at Google Scholar · View at Scopus
  64. 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 · View at Scopus
  65. S. K. Powers and M. J. Jackson, “Exercise-induced oxidative stress: cellular mechanisms and impact on muscle force production,” Physiological Reviews, vol. 88, no. 4, pp. 1243–1276, 2008. View at Publisher · View at Google Scholar · View at Scopus
  66. E. Barreiro, B. de la Puente, S. Busquets, F. J. López-Soriano, J. Gea, and J. M. Argilés, “Both oxidative and nitrosative stress are associated with muscle wasting in tumour-bearing rats,” FEBS Letters, vol. 579, no. 7, pp. 1646–1652, 2005. View at Publisher · View at Google Scholar · View at Scopus
  67. J. G. Tidball, “Inflammatory processes in muscle injury and repair,” American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, vol. 288, no. 2, pp. R345–R353, 2005. View at Publisher · View at Google Scholar · View at Scopus
  68. P. J. Adhihetty, I. Irrcher, A. M. Joseph, V. Ljubicic, and D. A. Hood, “Plasticity of skeletal muscle mitochondria in response to contractile activity,” Experimental Physiology, vol. 88, no. 1, pp. 99–107, 2003. View at Publisher · View at Google Scholar · View at Scopus
  69. P. A. Kramer, J. Duan, W. J. Qian, and D. J. Marcinek, “The measurement of reversible redox dependent post-translational modifications and their regulation of mitochondrial and skeletal muscle function,” Frontiers in Physiology, vol. 6, p. 347, 2015. View at Publisher · View at Google Scholar · View at Scopus
  70. P. Mecocci, G. Fanó, S. Fulle et al., “Age-dependent increases in oxidative damage to DNA, lipids, and proteins in human skeletal muscle,” Free Radical Biology and Medicine, vol. 26, no. 3-4, pp. 303–308, 1999. View at Publisher · View at Google Scholar · View at Scopus
  71. L. A. Callahan, Z. W. She, and T. M. Nosek, “Superoxide, hydroxyl radical, and hydrogen peroxide effects on single-diaphragm fiber contractile apparatus,” Journal of Applied Physiology, vol. 90, no. 1, pp. 45–54, 2001. View at Publisher · View at Google Scholar
  72. M. B. Reid and W. J. Durham, “Generation of reactive oxygen and nitrogen species in contracting skeletal muscle: potential impact on aging,” Annals of the New York Academy of Sciences, vol. 959, no. 1, pp. 108–116, 2002. View at Publisher · View at Google Scholar
  73. J. M. Gutteridge and B. Halliwell, “Free radicals and antioxidants in the year 2000. A historical look to the future,” Annals of the New York Academy of Sciences, vol. 899, pp. 136–147, 2000. View at Publisher · View at Google Scholar
  74. E. A. Veal, A. M. Day, and B. A. Morgan, “Hydrogen peroxide sensing and signaling,” Molecular Cell, vol. 26, no. 1, pp. 1–14, 2007. View at Publisher · View at Google Scholar · View at Scopus
  75. M. Altun, E. Edström, E. Spooner et al., “Iron load and redox stress in skeletal muscle of aged rats,” Muscle & Nerve, vol. 36, no. 2, pp. 223–233, 2007. View at Publisher · View at Google Scholar · View at Scopus
  76. D. Trachootham, W. Lu, M. A. Ogasawara, N. R. D. Valle, and P. Huang, “Redox regulation of cell survival,” Antioxidants & Redox Signaling, vol. 10, no. 8, pp. 1343–1374, 2008. View at Publisher · View at Google Scholar · View at Scopus
  77. T. Maraldi, “Natural compounds as modulators of NADPH oxidases,” Oxidative Medicine and Cellular Longevity, vol. 2013, Article ID 271602, 10 pages, 2013. View at Publisher · View at Google Scholar · View at Scopus
  78. K. Bedard and K. H. Krause, “The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology,” Physiological Reviews, vol. 87, no. 1, pp. 245–313, 2007. View at Publisher · View at Google Scholar · View at Scopus
  79. D. I. Brown and K. K. Griendling, “Nox proteins in signal transduction,” Free Radical Biology and Medicine, vol. 47, no. 9, pp. 1239–1253, 2009. View at Publisher · View at Google Scholar · View at Scopus
  80. T. Ueyama, K. Lekstrom, S. Tsujibe, N. Saito, and T. L. Leto, “Subcellular localization and function of alternatively spliced Noxo1 isoforms,” Free Radical Biology and Medicine, vol. 42, no. 2, pp. 180–190, 2007. View at Publisher · View at Google Scholar · View at Scopus
  81. A. N. Lyle, N. N. Deshpande, Y. Taniyama et al., “Poldip2, a novel regulator of Nox4 and cytoskeletal integrity in vascular smooth muscle cells,” Circulation Research, vol. 105, no. 3, pp. 249–259, 2009. View at Publisher · View at Google Scholar · View at Scopus
  82. S. Coso, I. Harrison, C. B. Harrison et al., “NADPH oxidases as regulators of tumor angiogenesis: current and emerging concepts,” Antioxidants & Redox Signaling, vol. 16, no. 11, pp. 1229–1247, 2012. View at Publisher · View at Google Scholar · View at Scopus
  83. I. Takac, K. Schröder, L. Zhang et al., “The E-loop is involved in hydrogen peroxide formation by the NADPH oxidase Nox4,” Journal of Biological Chemistry, vol. 286, no. 15, pp. 13304–13313, 2011. View at Publisher · View at Google Scholar · View at Scopus
  84. G. Cheng, Z. Cao, X. Xu, E. G. V. Meir, and J. D. Lambeth, “Homologs of gp91phox: cloning and tissue expression of Nox3, Nox4, and Nox5,” Gene, vol. 269, no. 1-2, pp. 131–140, 2001. View at Publisher · View at Google Scholar · View at Scopus
  85. D. Javeshghani, S. A. Magder, E. Barreiro, M. T. Quinn, and S. N. Hussain, “Molecular characterization of a superoxide-generating NAD(P)H oxidase in the ventilatory muscles,” American Journal of Respiratory and Critical Care Medicine, vol. 165, no. 3, pp. 412–418, 2002. View at Publisher · View at Google Scholar · View at Scopus
  86. A. Mansouri, F. L. Muller, Y. Liu et al., “Alterations in mitochondrial function, hydrogen peroxide release and oxidative damage in mouse hind-limb skeletal muscle during aging,” Mechanisms of Ageing and Development, vol. 127, no. 3, pp. 298–306, 2006. View at Publisher · View at Google Scholar · View at Scopus
  87. T. F. Cunha, L. R. G. Bechara, A. V. N. Bacurau et al., “Exercise training decreases NADPH oxidase activity and restores skeletal muscle mass in heart failure rats,” Journal of Applied Physiology, vol. 122, no. 4, pp. 817–827, 2017. View at Publisher · View at Google Scholar · View at Scopus
  88. D. A. Kostić, D. S. Dimitrijević, G. S. Stojanović, I. R. Palić, A. S. Đorđević, and J. D. Ickovski, “Xanthine oxidase: isolation, assays of activity, and inhibition,” Journal of Chemistry, vol. 2015, Article ID 294858, 8 pages, 2015. View at Publisher · View at Google Scholar · View at Scopus
  89. P. Cos, L. Ying, M. Calomme et al., “Structure-activity relationship and classification of flavonoids as inhibitors of xanthine oxidase and superoxide scavengers,” Journal of Natural Products, vol. 61, no. 1, pp. 71–76, 1998. View at Publisher · View at Google Scholar · View at Scopus
  90. A. Mittal, A. R. J. Phillips, B. Loveday, and J. A. Windsor, “The potential role for xanthine oxidase inhibition in major intra-abdominal surgery,” World Journal of Surgery, vol. 32, no. 2, pp. 288–295, 2008. View at Publisher · View at Google Scholar · View at Scopus
  91. E. E. Kelley, N. K. H. Khoo, N. J. Hundley, U. Z. Malik, B. A. Freeman, and M. M. Tarpey, “Hydrogen peroxide is the major oxidant product of xanthine oxidase,” Free Radical Biology and Medicine, vol. 48, no. 4, pp. 493–498, 2010. View at Publisher · View at Google Scholar · View at Scopus
  92. W. Doehner and U. Landmesser, “Xanthine oxidase and uric acid in cardiovascular disease: clinical impact and therapeutic options,” Seminars in Nephrology, vol. 31, no. 5, pp. 433–440, 2011. View at Publisher · View at Google Scholar · View at Scopus
  93. M. C. I. Lee, M. Velayutham, T. Komatsu, R. Hille, and J. L. Zweier, “Measurement and characterization of superoxide generation from xanthine dehydrogenase: a redox-regulated pathway of radical generation in ischemic tissues,” Biochemistry, vol. 53, no. 41, pp. 6615–6623, 2014. View at Publisher · View at Google Scholar · View at Scopus
  94. F. Sanchis-Gomar, H. Pareja-Galeano, C. Perez-Quilis et al., “Effects of allopurinol on exercise-induced muscle damage: new therapeutic approaches?” Cell Stress and Chaperones, vol. 20, no. 1, pp. 3–13, 2015. View at Publisher · View at Google Scholar · View at Scopus
  95. Y. Hellsten, U. Frandsen, N. Orthenblad, B. Sjødin, and E. A. Richter, “Xanthine oxidase in human skeletal muscle following eccentric exercise: a role in inflammation,” The Journal of Physiology, vol. 498, no. 1, pp. 239–248, 1997. View at Publisher · View at Google Scholar · View at Scopus
  96. A. Kadambi and T. C. Skalak, “Role of leukocytes and tissue-derived oxidants in short-term skeletal muscle ischemia-reperfusion injury,” American Journal of Physiology-Heart and Circulatory Physiology, vol. 278, no. 2, pp. H435–H443, 2000. View at Publisher · View at Google Scholar
  97. M. C. Gomez-Cabrera, A. Martínez, G. Santangelo, F. V. Pallardó, J. Sastre, and J. Viña, “Oxidative stress in marathon runners: interest of antioxidant supplementation,” The British Journal of Nutrition, vol. 96, Supplement 1, no. S1, pp. S31–S33, 2006. View at Publisher · View at Google Scholar · View at Scopus
  98. M. C. Gómez-Cabrera, F. V. Pallardó, J. Sastre, J. Viña, and L. García-del-Moral, “Allopurinol and markers of muscle damage among participants in the Tour de France,” JAMA, vol. 289, no. 19, pp. 2503-2504, 2003. View at Publisher · View at Google Scholar · View at Scopus
  99. J. Viña, M. C. Gomez-Cabrera, A. Lloret et al., “Free radicals in exhaustive physical exercise: mechanism of production, and protection by antioxidants,” IUBMB Life, vol. 50, no. 4, pp. 271–277, 2000. View at Publisher · View at Google Scholar
  100. N. Linder, J. Rapola, and K. O. Raivio, “Cellular expression of xanthine oxidoreductase protein in normal human tissues,” Laboratory Investigation, vol. 79, no. 8, pp. 967–974, 1999. View at Google Scholar
  101. J. K. Barclay and M. Hansel, “Free radicals may contribute to oxidative skeletal muscle fatigue,” Canadian Journal of Physiology and Pharmacology, vol. 69, no. 2, pp. 279–284, 1991. View at Publisher · View at Google Scholar · View at Scopus
  102. D. A. Stofan, L. A. Callahan, A. DiMARCO, D. E. Nethery, and G. S. Supinski, “Modulation of release of reactive oxygen species by the contracting diaphragm,” American Journal of Respiratory and Critical Care Medicine, vol. 161, 3 Part 1, pp. 891–898, 2000. View at Google Scholar
  103. M. J. Ryan, J. R. Jackson, Y. Hao, S. S. Leonard, and S. E. Alway, “Inhibition of xanthine oxidase reduces oxidative stress and improves skeletal muscle function in response to electrically stimulated isometric contractions in aged mice,” Free Radical Biology and Medicine, vol. 51, no. 1, pp. 38–52, 2011. View at Publisher · View at Google Scholar · View at Scopus
  104. F. Derbre, B. Ferrando, M. C. Gomez-Cabrera et al., “Inhibition of xanthine oxidase by allopurinol prevents skeletal muscle atrophy: role of p38 MAPKinase and E3 ubiquitin ligases,” PLoS One, vol. 7, no. 10, p. e46668, 2012. View at Publisher · View at Google Scholar · View at Scopus
  105. F. Sanchis-Gomar, H. Pareja-Galeano, J. Cortell-Ballester, and C. Perez-Quilis, “Prevention of acute skeletal muscle wasting in critical illness,” Minerva Anestesiologica, vol. 80, p. 748, 2014. View at Google Scholar
  106. K. Schulze-Osthoff, A. C. Bakker, B. Vanhaesebroeck, R. Beyaert, W. A. Jacob, and W. Fiers, “Cytotoxic activity of tumor necrosis factor is mediated by early damage of mitochondrial functions. Evidence for the involvement of mitochondrial radical generation,” The Journal of Biological Chemistry, vol. 267, no. 8, pp. 5317–5323, 1992. View at Google Scholar
  107. A. Boveris, “[57] Determination of the production of superoxide radicals and hydrogen peroxide in mitochondria,” Methods in Enzymology, vol. 105, pp. 429–435, 1984. View at Publisher · View at Google Scholar · View at Scopus
  108. I. N. Zelko, T. J. Mariani, and R. J. Folz, “Superoxide dismutase multigene family: a comparison of the CuZn-SOD (SOD1), Mn-SOD (SOD2), and EC-SOD (SOD3) gene structures, evolution, and expression,” Free Radical Biology and Medicine, vol. 33, no. 3, pp. 337–349, 2002. View at Publisher · View at Google Scholar · View at Scopus
  109. F. L. Muller, W. Song, Y. Liu et al., “Absence of CuZn superoxide dismutase leads to elevated oxidative stress and acceleration of age-dependent skeletal muscle atrophy,” Free Radical Biology and Medicine, vol. 40, no. 11, pp. 1993–2004, 2006. View at Publisher · View at Google Scholar · View at Scopus
  110. D. F. Dai, Y. A. Chiao, G. M. Martin et al., “Mitochondrial-targeted catalase: extended longevity and the roles in various disease models,” Progress in Molecular Biology and Translational Science, vol. 146, pp. 203–241, 2017. View at Publisher · View at Google Scholar · View at Scopus
  111. G. K. Sakellariou, A. P. Lightfoot, K. E. Earl, M. Stofanko, and B. McDonagh, “Redox homeostasis and age-related deficits in neuromuscular integrity and function,” Journal of Cachexia, Sarcopenia and Muscle, vol. 8, no. 6, pp. 881–906, 2017. View at Publisher · View at Google Scholar · View at Scopus
  112. B. Pereira, L. F. B. Costa Rosa, D. A. Safi, M. H. G. Medeiros, R. Curi, and E. J. H. Bechara, “Superoxide dismutase, catalase, and glutathione peroxidase activities in muscle and lymphoid organs of sedentary and exercise-trained rats,” Physiology & Behavior, vol. 56, no. 5, pp. 1095–1099, 1994. View at Publisher · View at Google Scholar · View at Scopus
  113. R. Brigelius-Flohe, “Glutathione peroxidases and redox-regulated transcription factors,” Biological Chemistry, vol. 387, no. 10-11, pp. 1329–1335, 2006. View at Publisher · View at Google Scholar · View at Scopus
  114. L. L. Ji, “Antioxidant signaling in skeletal muscle: a brief review,” Experimental Gerontology, vol. 42, no. 7, pp. 582–593, 2007. View at Publisher · View at Google Scholar · View at Scopus
  115. J. M. McCord and M. A. Edeas, “SOD, oxidative stress and human pathologies: a brief history and a future vision,” Biomedicine & Pharmacotherapy, vol. 59, no. 4, pp. 139–142, 2005. View at Publisher · View at Google Scholar · View at Scopus
  116. S. Kinugawa, S. Takada, S. Matsushima, K. Okita, and H. Tsutsui, “Skeletal muscle abnormalities in heart failure,” International Heart Journal, vol. 56, no. 5, pp. 475–484, 2015. View at Publisher · View at Google Scholar · View at Scopus
  117. A. Kaltsatou, G. K. Sakkas, K. P. Poulianiti et al., “Uremic myopathy: is oxidative stress implicated in muscle dysfunction in uremia?” Frontiers in Physiology, vol. 6, p. 102, 2015. View at Publisher · View at Google Scholar · View at Scopus
  118. P. Delafontaine and M. Akao, “Angiotensin II as candidate of cardiac cachexia,” Current Opinion in Clinical Nutrition and Metabolic Care, vol. 9, no. 3, pp. 220–224, 2006. View at Publisher · View at Google Scholar · View at Scopus
  119. S. D. Anker, W. Steinborn, and S. Strassburg, “Cardiac cachexia,” Annals of Medicine, vol. 36, no. 7, pp. 518–529, 2004. View at Publisher · View at Google Scholar · View at Scopus
  120. A. Q. Adigun and A. A. L. Ajayi, “The effects of enalapril-digoxin-diuretic combination therapy on nutritional and anthropometric indices in chronic congestive heart failure: preliminary findings in cardiac cachexia,” European Journal of Heart Failure, vol. 3, no. 3, pp. 359–363, 2001. View at Publisher · View at Google Scholar · View at Scopus
  121. J. S. Chamberlain, “ACE inhibitor bulks up muscle,” Nature Medicine, vol. 13, no. 2, pp. 125-126, 2007. View at Publisher · View at Google Scholar · View at Scopus
  122. Y. Wei, J. R. Sowers, R. Nistala et al., “Angiotensin II-induced NADPH oxidase activation impairs insulin signaling in skeletal muscle cells,” The Journal of Biological Chemistry, vol. 281, no. 46, pp. 35137–35146, 2006. View at Publisher · View at Google Scholar · View at Scopus
  123. L. C. Semprun-Prieto, S. Sukhanov, T. Yoshida et al., “Angiotensin II induced catabolic effect and muscle atrophy are redox dependent,” Biochemical and Biophysical Research Communications, vol. 409, no. 2, pp. 217–221, 2011. View at Publisher · View at Google Scholar · View at Scopus
  124. S. T. Russell, H. Eley, and M. J. Tisdale, “Role of reactive oxygen species in protein degradation in murine myotubes induced by proteolysis-inducing factor and angiotensin II,” Cellular Signalling, vol. 19, no. 8, pp. 1797–1806, 2007. View at Publisher · View at Google Scholar · View at Scopus
  125. W. Zhao, S. A. Swanson, J. Ye et al., “Reactive oxygen species impair sympathetic vasoregulation in skeletal muscle in angiotensin II–dependent hypertension,” Hypertension, vol. 48, no. 4, pp. 637–643, 2006. View at Publisher · View at Google Scholar · View at Scopus
  126. C. Cabello-Verrugio, M. G. Morales, J. C. Rivera, D. Cabrera, and F. Simon, “Renin-angiotensin system: an old player with novel functions in skeletal muscle,” Medicinal Research Reviews, vol. 35, no. 3, pp. 437–463, 2015. View at Publisher · View at Google Scholar · View at Scopus
  127. A. K. Doughan, D. G. Harrison, and S. I. Dikalov, “Molecular mechanisms of angiotensin II–mediated mitochondrial dysfunction: linking mitochondrial oxidative damage and vascular endothelial dysfunction,” Circulation Research, vol. 102, no. 4, pp. 488–496, 2008. View at Publisher · View at Google Scholar · View at Scopus
  128. H. L. Eley and M. J. Tisdale, “Skeletal muscle atrophy, a link between depression of protein synthesis and increase in degradation,” The Journal of Biological Chemistry, vol. 282, no. 10, pp. 7087–7097, 2007. View at Publisher · View at Google Scholar · View at Scopus
  129. G. Mantovani, A. Macciò, C. Madeddu et al., “Antioxidant agents are effective in inducing lymphocyte progression through cell cycle in advanced cancer patients: assessment of the most important laboratory indexes of cachexia and oxidative stress,” Journal of Molecular Medicine, vol. 81, no. 10, pp. 664–673, 2003. View at Publisher · View at Google Scholar · View at Scopus
  130. D. Sanchis, S. Busquets, B. Alvarez, D. Ricquier, F. J. López-Soriano, and J. M. Argilés, “Skeletal muscle UCP2 and UCP3 gene expression in a rat cancer cachexia model,” FEBS Letters, vol. 436, no. 3, pp. 415–418, 1998. View at Publisher · View at Google Scholar · View at Scopus
  131. C. Bing, M. Brown, P. King, P. Collins, M. J. Tisdale, and G. Williams, “Increased gene expression of brown fat uncoupling protein (UCP)1 and skeletal muscle UCP2 and UCP3 in MAC16-induced cancer cachexia,” Cancer Research, vol. 60, no. 9, pp. 2405–2410, 2000. View at Google Scholar
  132. S. Busquets, V. Almendro, E. Barreiro, M. Figueras, J. M. Argilés, and F. J. López-Soriano, “Activation of UCPs gene expression in skeletal muscle can be independent on both circulating fatty acids and food intake. Involvement of ROS in a model of mouse cancer cachexia,” FEBS Letters, vol. 579, no. 3, pp. 717–722, 2005. View at Publisher · View at Google Scholar · View at Scopus
  133. P. Collins, C. Bing, P. McCulloch, and G. Williams, “Muscle UCP-3 mRNA levels are elevated in weight loss associated with gastrointestinal adenocarcinoma in humans,” British Journal of Cancer, vol. 86, no. 3, pp. 372–375, 2002. View at Publisher · View at Google Scholar · View at Scopus
  134. G. Strassmann, M. Fong, J. S. Kenney, and C. O. Jacob, “Evidence for the involvement of interleukin 6 in experimental cancer cachexia,” The Journal of Clinical Investigation, vol. 89, no. 5, pp. 1681–1684, 1992. View at Publisher · View at Google Scholar · View at Scopus
  135. J. Gelin, L. L. Moldawer, C. Lönnroth, B. Sherry, R. Chizzonite, and K. Lundholm, “Role of endogenous tumor necrosis factor alpha and interleukin 1 for experimental tumor growth and the development of cancer cachexia,” Cancer Research, vol. 51, no. 1, pp. 415–421, 1991. View at Google Scholar
  136. G. Mantovani, A. Macciò, P. Lai, E. Massa, M. Ghiani, and M. C. Santona, “Cytokine activity in cancer-related anorexia/cachexia: role of megestrol acetate and medroxyprogesterone acetate,” Seminars in Oncology, vol. 25, Supplement 6, no. 2, pp. 45–52, 1998. View at Google Scholar
  137. H. J. Smith and M. J. Tisdale, “Signal transduction pathways involved in proteolysis-inducing factor induced proteasome expression in murine myotubes,” British Journal of Cancer, vol. 89, no. 9, pp. 1783–1788, 2003. View at Publisher · View at Google Scholar · View at Scopus
  138. R. C. Langen, A. M. Schols, M. C. Kelders, J. L. Van Der Velden, E. F. Wouters, and Y. M. Janssen-Heininger, “Tumor necrosis factor-α inhibits myogenesis through redox-dependent and -independent pathways,” American Journal of Physiology-Cell Physiology, vol. 283, no. 3, pp. C714–C721, 2002. View at Publisher · View at Google Scholar
  139. Y. S. Kim, M. J. Morgan, S. Choksi, and Z. G. Liu, “TNF-induced activation of the Nox1 NADPH oxidase and its role in the induction of necrotic cell death,” Molecular Cell, vol. 26, no. 5, pp. 675–687, 2007. View at Publisher · View at Google Scholar · View at Scopus
  140. M. J. Sullivan-Gunn, S. P. Campbell-O'Sullivan, M. J. Tisdale, and P. A. Lewandowski, “Decreased NADPH oxidase expression and antioxidant activity in cachectic skeletal muscle,” Journal of Cachexia, Sarcopenia and Muscle, vol. 2, no. 3, pp. 181–188, 2011. View at Publisher · View at Google Scholar · View at Scopus
  141. G. Mantovani and C. Madeddu, “Cancer cachexia: medical management,” Support Care Cancer, vol. 18, no. 1, pp. 1–9, 2010. View at Publisher · View at Google Scholar · View at Scopus
  142. J. Springer, A. Tschirner, K. Hartman et al., “Inhibition of xanthine oxidase reduces wasting and improves outcome in a rat model of cancer cachexia,” International Journal of Cancer, vol. 131, no. 9, pp. 2187–2196, 2012. View at Publisher · View at Google Scholar · View at Scopus
  143. V. Banduseela, J. Ochala, K. Lamberg, H. Kalimo, and L. Larsson, “Muscle paralysis and myosin loss in a patient with cancer cachexia,” Acta Myologica, vol. 26, no. 3, pp. 136–144, 2007. View at Google Scholar
  144. S. H. Lecker, R. T. Jagoe, A. Gilbert et al., “Multiple types of skeletal muscle atrophy involve a common program of changes in gene expression,” The FASEB Journal, vol. 18, no. 1, pp. 39–51, 2004. View at Publisher · View at Google Scholar · View at Scopus
  145. M. Sandri, “Protein breakdown in muscle wasting: role of autophagy-lysosome and ubiquitin-proteasome,” The International Journal of Biochemistry & Cell Biology, vol. 45, no. 10, pp. 2121–2129, 2013. View at Publisher · View at Google Scholar · View at Scopus
  146. J. P. Gumucio and C. L. Mendias, “Atrogin-1, MuRF-1, and sarcopenia,” Endocrine, vol. 43, no. 1, pp. 12–21, 2013. View at Publisher · View at Google Scholar · View at Scopus
  147. D. L. Waning, K. S. Mohammad, S. Reiken et al., “Excess TGF-β mediates muscle weakness associated with bone metastases in mice,” Nature Medicine, vol. 21, no. 11, pp. 1262–1271, 2015. View at Publisher · View at Google Scholar · View at Scopus
  148. C. Cabello-Verrugio, J. C. Rivera, and D. Garcia, “Skeletal muscle wasting: new role of nonclassical renin-angiotensin system,” Current Opinion in Clinical Nutrition and Metabolic Care, vol. 20, no. 3, pp. 158–163, 2017. View at Publisher · View at Google Scholar · View at Scopus
  149. Y. P. Li, Y. Chen, A. S. Li, and M. B. Reid, “Hydrogen peroxide stimulates ubiquitin-conjugating activity and expression of genes for specific E2 and E3 proteins in skeletal muscle myotubes,” American Journal of Physiology-Cell Physiology, vol. 285, no. 4, pp. C806–C812, 2003. View at Publisher · View at Google Scholar
  150. S. T. Russell, P. M. A. Siren, M. J. Siren, and M. J. Tisdale, “Attenuation of skeletal muscle atrophy in cancer cachexia by D-myo-inositol 1,2,6-triphosphate,” Cancer Chemotherapy and Pharmacology, vol. 64, no. 3, pp. 517–527, 2009. View at Publisher · View at Google Scholar · View at Scopus
  151. Y. P. Li and M. B. Reid, “NF-κB mediates the protein loss induced by TNF-α in differentiated skeletal muscle myotubes,” American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, vol. 279, no. 4, pp. R1165–R1170, 2000. View at Publisher · View at Google Scholar
  152. M. D. Layne and S. R. Farmer, “Tumor necrosis factor-α and basic fibroblast growth factor differentially inhibit the insulin-like growth factor-I induced expression of myogenin in C2C12 myoblasts,” Experimental Cell Research, vol. 249, no. 1, pp. 177–187, 1999. View at Publisher · View at Google Scholar · View at Scopus
  153. M. Pedersen, H. Bruunsgaard, N. Weis et al., “Circulating levels of TNF-alpha and IL-6-relation to truncal fat mass and muscle mass in healthy elderly individuals and in patients with type-2 diabetes,” Mechanisms of Ageing and Development, vol. 124, no. 4, pp. 495–502, 2003. View at Publisher · View at Google Scholar · View at Scopus
  154. R. L. Campbell and P. L. Davies, “Structure-function relationships in calpains,” The Biochemical Journal, vol. 447, no. 3, pp. 335–351, 2012. View at Publisher · View at Google Scholar · View at Scopus
  155. D. E. Goll, V. F. Thompson, H. Li, W. Wei, and J. Cong, “The calpain system,” Physiological Reviews, vol. 83, no. 3, pp. 731–801, 2003. View at Publisher · View at Google Scholar · View at Scopus
  156. A. J. Smuder, A. N. Kavazis, M. B. Hudson, W. B. Nelson, and S. K. Powers, “Oxidation enhances myofibrillar protein degradation via calpain and caspase-3,” Free Radical Biology and Medicine, vol. 49, no. 7, pp. 1152–1160, 2010. View at Publisher · View at Google Scholar · View at Scopus
  157. J. M. McClung, A. R. Judge, E. E. Talbert, and S. K. Powers, “Calpain-1 is required for hydrogen peroxide-induced myotube atrophy,” American Journal of Physiology-Cell Physiology, vol. 296, no. 2, pp. C363–C371, 2009. View at Publisher · View at Google Scholar · View at Scopus
  158. E. Dargelos, C. Brulé, P. Stuelsatz et al., “Up-regulation of calcium-dependent proteolysis in human myoblasts under acute oxidative stress,” Experimental Cell Research, vol. 316, no. 1, pp. 115–125, 2010. View at Publisher · View at Google Scholar · View at Scopus
  159. M. A. Whidden, A. J. Smuder, M. Wu, M. B. Hudson, W. B. Nelson, and S. K. Powers, “Oxidative stress is required for mechanical ventilation-induced protease activation in the diaphragm,” Journal of Applied Physiology, vol. 108, no. 5, pp. 1376–1382, 2010. View at Publisher · View at Google Scholar · View at Scopus
  160. S. K. Powers, A. N. Kavazis, and J. M. McClung, “Oxidative stress and disuse muscle atrophy,” Journal of Applied Physiology, vol. 102, no. 6, pp. 2389–2397, 2007. View at Publisher · View at Google Scholar · View at Scopus
  161. E. Dargelos, S. Poussard, C. Brulé, L. Daury, and P. Cottin, “Calcium-dependent proteolytic system and muscle dysfunctions: a possible role of calpains in sarcopenia,” Biochimie, vol. 90, no. 2, pp. 359–368, 2008. View at Publisher · View at Google Scholar · View at Scopus
  162. J. I. Kourie, “Interaction of reactive oxygen species with ion transport mechanisms,” The American Journal of Physiology-Cell Physiology, vol. 275, no. 1, pp. C1–C24, 1998. View at Publisher · View at Google Scholar
  163. J. R. Florini, D. Z. Ewton, and S. A. Coolican, “Growth hormone and the insulin-like growth factor system in myogenesis,” Endocrine Reviews, vol. 17, no. 5, pp. 481–517, 1996. View at Publisher · View at Google Scholar
  164. D. Chrysis and L. E. Underwood, “Regulation of components of the ubiquitin system by insulin-like growth factor I and growth hormone in skeletal muscle of rats made catabolic with dexamethasone,” Endocrinology, vol. 140, no. 12, pp. 5635–5641, 1999. View at Publisher · View at Google Scholar
  165. D. Hong and N. E. Forsberg, “Effects of serum and insulin-like growth factor I on protein degradation and protease gene expression in rat L8 myotubes,” Journal of Animal Science, vol. 72, no. 9, pp. 2279–2288, 1994. View at Publisher · View at Google Scholar
  166. M. A. Lawlor and P. Rotwein, “Insulin-like growth factor-mediated muscle cell survival: central roles for Akt and cyclin-dependent kinase inhibitor p21,” Molecular and Cellular Biology, vol. 20, no. 23, pp. 8983–8995, 2000. View at Publisher · View at Google Scholar · View at Scopus
  167. S. P. Attard-Montalto, C. Camacho-Hübner, A. M. Cotterill et al., “Changes in protein turnover, IGF-I and IGF binding proteins in children with cancer,” Acta Paediatrica, vol. 87, no. 1, pp. 54–60, 1998. View at Publisher · View at Google Scholar
  168. P. Costelli, M. Muscaritoli, M. Bossola et al., “IGF-1 is downregulated in experimental cancer cachexia,” American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, vol. 291, no. 3, pp. R674–R683, 2006. View at Publisher · View at Google Scholar · View at Scopus
  169. J. Fan, P. E. Molina, M. C. Gelato, and C. H. Lang, “Differential tissue regulation of insulin-like growth factor-I content and binding proteins after endotoxin,” Endocrinology, vol. 134, no. 4, pp. 1685–1692, 1994. View at Publisher · View at Google Scholar · View at Scopus
  170. M. Sandri, C. Sandri, A. Gilbert et al., “Foxo transcription factors induce the atrophy-related ubiquitin ligase atrogin-1 and cause skeletal muscle atrophy,” Cell, vol. 117, no. 3, pp. 399–412, 2004. View at Publisher · View at Google Scholar · View at Scopus
  171. J. Papaconstantinou, “Insulin/IGF-1 and ROS signaling pathway cross-talk in aging and longevity determination,” Molecular and Cellular Endocrinology, vol. 299, no. 1, pp. 89–100, 2009. View at Publisher · View at Google Scholar · View at Scopus
  172. N. Bashan, J. Kovsan, I. Kachko, H. Ovadia, and A. Rudich, “Positive and negative regulation of insulin signaling by reactive oxygen and nitrogen species,” Physiological Reviews, vol. 89, no. 1, pp. 27–71, 2009. View at Publisher · View at Google Scholar · View at Scopus
  173. M. Genestra, “Oxyl radicals, redox-sensitive signalling cascades and antioxidants,” Cellular Signalling, vol. 19, no. 9, pp. 1807–1819, 2007. View at Publisher · View at Google Scholar · View at Scopus
  174. J. V. Cross and D. J. Templeton, “Regulation of signal transduction through protein cysteine oxidation,” Antioxidants & Redox Signaling, vol. 8, no. 9-10, pp. 1819–1827, 2006. View at Publisher · View at Google Scholar · View at Scopus
  175. R. Wani, J. Qian, L. Yin et al., “Isoform-specific regulation of Akt by PDGF-induced reactive oxygen species,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 26, pp. 10550–10555, 2011. View at Publisher · View at Google Scholar · View at Scopus
  176. L. Coderre, K. V. Kandror, G. Vallega, and P. F. Pilch, “Identification and characterization of an exercise-sensitive pool of glucose transporters in skeletal muscle,” The Journal of Biological Chemistry, vol. 270, no. 46, pp. 27584–27588, 1995. View at Publisher · View at Google Scholar · View at Scopus
  177. S. Lund, G. D. Holman, O. Schmitz, and O. Pedersen, “Contraction stimulates translocation of glucose transporter GLUT4 in skeletal muscle through a mechanism distinct from that of insulin,” Proceedings of the National Academy of Sciences of the United States of America, vol. 92, no. 13, pp. 5817–5821, 1995. View at Publisher · View at Google Scholar · View at Scopus
  178. 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
  179. J. Navarro-Yepes, M. Burns, A. Anandhan et al., “Oxidative stress, redox signaling, and autophagy: cell death versus survival,” Antioxidants & Redox Signaling, vol. 21, no. 1, pp. 66–85, 2014. View at Publisher · View at Google Scholar · View at Scopus
  180. J. J. Lum, R. J. DeBerardinis, and C. B. Thompson, “Autophagy in metazoans: cell survival in the land of plenty,” Nature Reviews Molecular Cell Biology, vol. 6, no. 6, pp. 439–448, 2005. View at Publisher · View at Google Scholar · View at Scopus
  181. B. Levine and G. Kroemer, “Autophagy in the pathogenesis of disease,” Cell, vol. 132, no. 1, pp. 27–42, 2008. View at Publisher · View at Google Scholar · View at Scopus
  182. G. G. Rodney, R. Pal, and R. Abo-Zahrah, “Redox regulation of autophagy in skeletal muscle,” Free Radical Biology and Medicine, vol. 98, pp. 103–112, 2016. View at Publisher · View at Google Scholar · View at Scopus
  183. R. Pal, M. Palmieri, J. A. Loehr et al., “Src-dependent impairment of autophagy by oxidative stress in a mouse model of Duchenne muscular dystrophy,” Nature Communications, vol. 5, article 4425, 2014. View at Publisher · View at Google Scholar · View at Scopus
  184. M. Chrisam, M. Pirozzi, S. Castagnaro et al., “Reactivation of autophagy by spermidine ameliorates the myopathic defects of collagen VI-null mice,” Autophagy, vol. 11, no. 12, pp. 2142–2152, 2015. View at Publisher · View at Google Scholar · View at Scopus
  185. Y. Xiao, C. Ma, J. Yi et al., “Suppressed autophagy flux in skeletal muscle of an amyotrophic lateral sclerosis mouse model during disease progression,” Physiological Reports, vol. 3, no. 1, article e12271, 2015. View at Publisher · View at Google Scholar · View at Scopus
  186. Y. Guo, H. R. Gosker, A. M. W. J. Schols et al., “Autophagy in locomotor muscles of patients with chronic obstructive pulmonary disease,” American Journal of Respiratory and Critical Care Medicine, vol. 188, no. 11, pp. 1313–1320, 2013. View at Publisher · View at Google Scholar
  187. J. Gea, S. Pascual, C. Casadevall, M. Orozco-Levi, and E. Barreiro, “Muscle dysfunction in chronic obstructive pulmonary disease: update on causes and biological findings,” Journal of Thoracic Disease, vol. 7, no. 10, pp. E418–E438, 2015. View at Publisher · View at Google Scholar · View at Scopus
  188. F. Stana, M. Vujovic, D. Mayaki et al., “Differential regulation of the autophagy and proteasome pathways in skeletal muscles in sepsis,” Critical Care Medicine, vol. 45, no. 9, pp. e971–e979, 2017. View at Publisher · View at Google Scholar · View at Scopus
  189. G. Gortan Cappellari, A. Semolic, G. Ruozi et al., “Unacylated ghrelin normalizes skeletal muscle oxidative stress and prevents muscle catabolism by enhancing tissue mitophagy in experimental chronic kidney disease,” The FASEB Journal, vol. 31, no. 12, pp. 5159–5171, 2017. View at Publisher · View at Google Scholar · View at Scopus
  190. E. Pigna, E. Berardi, P. Aulino et al., “Aerobic exercise and pharmacological treatments counteract cachexia by modulating autophagy in colon cancer,” Scientific Reports, vol. 6, no. 1, article 26991, 2016. View at Publisher · View at Google Scholar · View at Scopus
  191. G. Dobrowolny, M. Aucello, E. Rizzuto et al., “Skeletal muscle is a primary target of SOD1G93A-mediated toxicity,” Cell Metabolism, vol. 8, no. 5, pp. 425–436, 2008. View at Publisher · View at Google Scholar · View at Scopus
  192. Y. Chen, M. B. Azad, and S. B. Gibson, “Superoxide is the major reactive oxygen species regulating autophagy,” Cell Death and Differentiation, vol. 16, no. 7, pp. 1040–1052, 2009. View at Publisher · View at Google Scholar · View at Scopus
  193. 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
  194. M. Rahman, M. Mofarrahi, A. S. Kristof, B. Nkengfac, S. Harel, and S. N. A. 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 · View at Scopus
  195. E. E. Talbert, A. J. Smuder, K. Min, O. S. Kwon, H. H. Szeto, and S. K. Powers, “Immobilization-induced activation of key proteolytic systems in skeletal muscles is prevented by a mitochondria-targeted antioxidant,” Journal of Applied Physiology, vol. 115, no. 4, pp. 529–538, 2013. View at Publisher · View at Google Scholar · View at Scopus
  196. P. L. Tan, T. Shavlakadze, M. D. Grounds, and P. G. Arthur, “Differential thiol oxidation of the signaling proteins Akt, PTEN or PP2A determines whether Akt phosphorylation is enhanced or inhibited by oxidative stress in C2C12 myotubes derived from skeletal muscle,” The International Journal of Biochemistry & Cell Biology, vol. 62, pp. 72–79, 2015. View at Publisher · View at Google Scholar · View at Scopus
  197. A. Nakanishi, Y. Wada, Y. Kitagishi, and S. Matsuda, “Link between PI3K/AKT/PTEN pathway and NOX proteinin diseases,” Aging and Disease, vol. 5, no. 3, pp. 203–211, 2014. View at Publisher · View at Google Scholar · View at Scopus
  198. J. M. McClung, A. R. Judge, S. K. Powers, and Z. Yan, “p38 MAPK links oxidative stress to autophagy-related gene expression in cachectic muscle wasting,” American Journal of Physiology-Cell Physiology, vol. 298, no. 3, pp. C542–C549, 2010. View at Publisher · View at Google Scholar · View at Scopus
  199. L. Yuan, S. Wei, J. Wang, and X. Liu, “Isoorientin induces apoptosis and autophagy simultaneously by reactive oxygen species (ROS)-related p53, PI3K/Akt, JNK, and p38 signaling pathways in HepG2 cancer cells,” Journal of Agricultural and Food Chemistry, vol. 62, no. 23, pp. 5390–5400, 2014. View at Publisher · View at Google Scholar · View at Scopus
  200. W. J. Duan, Q. S. Li, M. Y. Xia, S. I. Tashiro, S. Onodera, and T. Ikejima, “Silibinin activated p53 and induced autophagic death in human fibrosarcoma HT1080 cells via reactive oxygen species-p38 and c-Jun N-terminal kinase pathways,” Biological and Pharmaceutical Bulletin, vol. 34, no. 1, pp. 47–53, 2011. View at Publisher · View at Google Scholar · View at Scopus
  201. S. B. Jorgensen, E. A. Richter, and J. F. Wojtaszewski, “Role of AMPK in skeletal muscle metabolic regulation and adaptation in relation to exercise,” The Journal of Physiology, vol. 574, no. 1, pp. 17–31, 2006. View at Publisher · View at Google Scholar · View at Scopus
  202. I. Irrcher, V. Ljubicic, and D. A. Hood, “Interactions between ROS and AMP kinase activity in the regulation of PGC-1α transcription in skeletal muscle cells,” The American Journal of Physiology-Cell Physiology, vol. 296, no. 1, pp. C116–C123, 2009. View at Publisher · View at Google Scholar · View at Scopus
  203. D. L. Allen, J. K. Linderman, R. R. Roy et al., “Apoptosis: a mechanism contributing to remodeling of skeletal muscle in response to hindlimb unweighting,” The American Journal of Physiology-Cell Physiology, vol. 273, no. 2, pp. C579–C587, 1997. View at Publisher · View at Google Scholar
  204. A. B. Borisov and B. M. Carlson, “Cell death in denervated skeletal muscle is distinct from classical apoptosis,” The Anatomical Record, vol. 258, no. 3, pp. 305–318, 2000. View at Publisher · View at Google Scholar
  205. D. L. Allen, R. R. Roy, and V. R. Edgerton, “Myonuclear domains in muscle adaptation and disease,” Muscle & Nerve, vol. 22, no. 10, pp. 1350–1360, 1999. View at Publisher · View at Google Scholar
  206. S. Gupta, “Molecular steps of tumor necrosis factor receptor-mediated apoptosis,” Current Molecular Medicine, vol. 1, no. 3, pp. 317–324, 2001. View at Publisher · View at Google Scholar · View at Scopus
  207. A. G. Agusti, J. Sauleda, C. Miralles et al., “Skeletal muscle apoptosis and weight loss in chronic obstructive pulmonary disease,” American Journal of Respiratory and Critical Care Medicine, vol. 166, no. 4, pp. 485–489, 2002. View at Publisher · View at Google Scholar · View at Scopus
  208. D. Verzola, V. Procopio, A. Sofia et al., “Apoptosis and myostatin mRNA are upregulated in the skeletal muscle of patients with chronic kidney disease,” Kidney International, vol. 79, no. 7, pp. 773–782, 2011. View at Publisher · View at Google Scholar · View at Scopus
  209. V. Adams, H. Jiang, J. Yu et al., “Apoptosis in skeletal myocytes of patients with chronic heart failure is associated with exercise intolerance,” Journal of the American College of Cardiology, vol. 33, no. 4, pp. 959–965, 1999. View at Publisher · View at Google Scholar · View at Scopus
  210. G. Vescovo, M. Volterrani, R. Zennaro et al., “Apoptosis in the skeletal muscle of patients with heart failure: investigation of clinical and biochemical changes,” Heart, vol. 84, no. 4, pp. 431–437, 2000. View at Publisher · View at Google Scholar
  211. M. Brink, S. R. Price, J. Chrast et al., “Angiotensin II induces skeletal muscle wasting through enhanced protein degradation and down-regulates autocrine insulin-like growth factor I,” Endocrinology, vol. 142, no. 4, pp. 1489–1496, 2001. View at Publisher · View at Google Scholar
  212. M. Brink, J. Wellen, and P. Delafontaine, “Angiotensin II causes weight loss and decreases circulating insulin-like growth factor I in rats through a pressor-independent mechanism,” The Journal of Clinical Investigation, vol. 97, no. 11, pp. 2509–2516, 1996. View at Publisher · View at Google Scholar · View at Scopus
  213. C. Meneses, M. G. Morales, J. Abrigo, F. Simon, E. Brandan, and C. Cabello-Verrugio, “The angiotensin-(1–7)/Mas axis reduces myonuclear apoptosis during recovery from angiotensin II-induced skeletal muscle atrophy in mice,” Pflügers Archiv - European Journal of Physiology, vol. 467, no. 9, pp. 1975–1984, 2015. View at Publisher · View at Google Scholar · View at Scopus
  214. P. M. Siu, Y. Wang, and S. E. Alway, “Apoptotic signaling induced by H2O2-mediated oxidative stress in differentiated C2C12 myotubes,” Life Sciences, vol. 84, no. 13-14, pp. 468–481, 2009. View at Publisher · View at Google Scholar · View at Scopus
  215. S. D. Anker, W. Doehner, M. Rauchhaus et al., “Uric acid and survival in chronic heart failure: validation and application in metabolic, functional, and hemodynamic staging,” Circulation, vol. 107, no. 15, pp. 1991–1997, 2003. View at Publisher · View at Google Scholar · View at Scopus
  216. J. Abrigo, J. C. Rivera, J. Aravena et al., “High fat diet-induced skeletal muscle wasting is decreased by mesenchymal stem cells administration: implications on oxidative stress, ubiquitin proteasome pathway activation, and myonuclear apoptosis,” Oxidative Medicine and Cellular Longevity, vol. 2016, Article ID 9047821, 13 pages, 2016. View at Publisher · View at Google Scholar · View at Scopus
  217. E. Barreiro and S. Tajbakhsh, “Epigenetic regulation of muscle development,” Journal of Muscle Research and Cell Motility, vol. 38, no. 1, pp. 31–35, 2017. View at Publisher · View at Google Scholar · View at Scopus
  218. R. M. Carr, E. Enriquez-Hesles, R. L. O. Olson, A. Jatoi, J. Doles, and M. E. Fernandez-Zapico, “Epigenetics of cancer-associated muscle catabolism,” Epigenomics, vol. 9, no. 10, pp. 1259–1265, 2017. View at Publisher · View at Google Scholar · View at Scopus
  219. D. T. Shaughnessy, K. McAllister, L. Worth et al., “Mitochondria, energetics, epigenetics, and cellular responses to stress,” Environmental Health Perspectives, vol. 122, no. 12, pp. 1271–1278, 2014. View at Publisher · View at Google Scholar · View at Scopus
  220. M. Liesa, M. Palacin, and A. Zorzano, “Mitochondrial dynamics in mammalian health and disease,” Physiological Reviews, vol. 89, no. 3, pp. 799–845, 2009. View at Publisher · View at Google Scholar · View at Scopus
  221. I. Novak, “Mitophagy: a complex mechanism of mitochondrial removal,” Antioxidants & Redox Signaling, vol. 17, no. 5, pp. 794–802, 2012. View at Publisher · View at Google Scholar · View at Scopus
  222. B. Westermann, “Mitochondrial fusion and fission in cell life and death,” Nature Reviews. Molecular Cell Biology, vol. 11, no. 12, pp. 872–884, 2010. View at Publisher · View at Google Scholar · View at Scopus
  223. R. J. Youle and D. P. Narendra, “Mechanisms of mitophagy,” Nature Reviews Molecular Cell Biology, vol. 12, no. 1, pp. 9–14, 2011. View at Publisher · View at Google Scholar · View at Scopus
  224. E. Marzetti, M. Lorenzi, F. Landi et al., “Altered mitochondrial quality control signaling in muscle of old gastric cancer patients with cachexia,” Experimental Gerontology, vol. 87, Part A, pp. 92–99, 2017. View at Publisher · View at Google Scholar · View at Scopus
  225. R. F. Roberts, M. Y. Tang, E. A. Fon, and T. M. Durcan, “Defending the mitochondria: the pathways of mitophagy and mitochondrial-derived vesicles,” The International Journal of Biochemistry & Cell Biology, vol. 79, pp. 427–436, 2016. View at Publisher · View at Google Scholar · View at Scopus
  226. P. S. Brookes, Y. Yoon, J. L. Robotham, M. W. Anders, and S. S. Sheu, “Calcium, ATP, and ROS: a mitochondrial love-hate triangle,” American Journal of Physiology-Cell Physiology, vol. 287, no. 4, pp. C817–C833, 2004. View at Publisher · View at Google Scholar · View at Scopus
  227. N. Cheema, A. Herbst, D. McKenzie, and J. M. Aiken, “Apoptosis and necrosis mediate skeletal muscle fiber loss in age-induced mitochondrial enzymatic abnormalities,” Aging Cell, vol. 14, no. 6, pp. 1085–1093, 2015. View at Publisher · View at Google Scholar · View at Scopus
  228. N. M. Held and R. H. Houtkooper, “Mitochondrial quality control pathways as determinants of metabolic health,” BioEssays, vol. 37, no. 8, pp. 867–876, 2015. View at Publisher · View at Google Scholar · View at Scopus
  229. S. G. Rhee, H. A. Woo, I. S. Kil, and S. H. Bae, “Peroxiredoxin functions as a peroxidase and a regulator and sensor of local peroxides,” The Journal of Biological Chemistry, vol. 287, no. 7, pp. 4403–4410, 2012. View at Publisher · View at Google Scholar · View at Scopus
  230. R. Scherz-Shouval and Z. Elazar, “ROS, mitochondria and the regulation of autophagy,” Trends in Cell Biology, vol. 17, no. 9, pp. 422–427, 2007. View at Publisher · View at Google Scholar · View at Scopus
  231. G. Twig, A. Elorza, A. J. A. Molina et al., “Fission and selective fusion govern mitochondrial segregation and elimination by autophagy,” The EMBO Journal, vol. 27, no. 2, pp. 433–446, 2008. View at Publisher · View at Google Scholar · View at Scopus
  232. J. A. Carson, J. P. Hardee, and B. N. VanderVeen, “The emerging role of skeletal muscle oxidative metabolism as a biological target and cellular regulator of cancer-induced muscle wasting,” Seminars in Cell & Developmental Biology, vol. 54, pp. 53–67, 2016. View at Publisher · View at Google Scholar · View at Scopus
  233. K. Boengler, M. Kosiol, M. Mayr, R. Schulz, and S. Rohrbach, “Mitochondria and ageing: role in heart, skeletal muscle and adipose tissue,” Journal of Cachexia, Sarcopenia and Muscle, vol. 8, no. 3, pp. 349–369, 2017. View at Publisher · View at Google Scholar · View at Scopus
  234. M. Chen, Z. Chen, Y. Wang et al., “Mitophagy receptor FUNDC1 regulates mitochondrial dynamics and mitophagy,” Autophagy, vol. 12, no. 4, pp. 689–702, 2016. View at Publisher · View at Google Scholar · View at Scopus
  235. A. Lang, R. Anand, S. Altinoluk-Hambüchen et al., “SIRT4 interacts with OPA1 and regulates mitochondrial quality control and mitophagy,” Aging, vol. 9, no. 10, pp. 2163–2189, 2017. View at Publisher · View at Google Scholar · View at Scopus
  236. K. Palikaras, E. Lionaki, and N. Tavernarakis, “Balancing mitochondrial biogenesis and mitophagy to maintain energy metabolism homeostasis,” Cell Death and Differentiation, vol. 22, no. 9, pp. 1399–1401, 2015. View at Publisher · View at Google Scholar · View at Scopus
  237. K. Palikaras, E. Lionaki, and N. Tavernarakis, “Coordination of mitophagy and mitochondrial biogenesis during ageing in C. elegans,” Nature, vol. 521, no. 7553, pp. 525–528, 2015. View at Publisher · View at Google Scholar · View at Scopus
  238. C. Ploumi, I. Daskalaki, and N. Tavernarakis, “Mitochondrial biogenesis and clearance: a balancing act,” The FEBS Journal, vol. 284, no. 2, pp. 183–195, 2017. View at Publisher · View at Google Scholar · View at Scopus
  239. J. Sin, A. M. Andres, D. J. R. Taylor et al., “Mitophagy is required for mitochondrial biogenesis and myogenic differentiation of C2C12 myoblasts,” Autophagy, vol. 12, no. 2, pp. 369–380, 2016. View at Publisher · View at Google Scholar · View at Scopus