Redox characterization of functioning skeletal muscle

Frontiers in Physiology

Volumn 6, Issue NOV, 2015, Pages

  Zuo, Li ^a,b   Pannell, Benjamin K ^a  

^a THE OHIO STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

Atrophy; Disease; Oxidative stress; Redox; Signaling

Indexed keywords

HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE;

ADAPTATION; AGING; CELL DEATH; CELL SWELLING; HUMAN; MITOCHONDRIAL MEMBRANE; MOLECULAR PATHOLOGY; MUSCLE ATROPHY; MUSCLE CELL; MUSCLE FUNCTION; MUSCLE MITOCHONDRION; NEUROMUSCULAR DISEASE; NONHUMAN; OXIDATION REDUCTION STATE; OXIDATIVE STRESS; PROTEIN MODIFICATION; SHORT SURVEY; SIGNAL TRANSDUCTION; SKELETAL MUSCLE;

EID: 84949547698     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphys.2015.00338     Document Type: Short Survey

References (111)

1. Adhihetty, P. J., Irrcher, I., Joseph, A. M., Ljubicic, V., and Hood, D. A. (2003). Plasticity of skeletal muscle mitochondria in response to contractile activity. Exp. Physiol. 88, 99-107. doi: 10.1113/eph8802505.
2. Adhihetty, P. J., Oleary, M. F., Chabi, B., Wicks, K. L., and Hood, D. A. (2007). Effect of denervation on mitochondrially mediated apoptosis in skeletal muscle. J. Appl. Physiol. 102, 1143-1151. doi: 10.1152/japplphysiol.00768.2006.
3. Babu, D., Leclercq, G., Goossens, V., Vanden Berghe, T., Van Hamme, E., Vandenabeele, P., et al. (2015). Mitochondria and NADPH oxidases are the major sources of TNF-alpha/cycloheximide-induced oxidative stress in murine intestinal epithelial MODE-K cells. Cell. Signal. 27, 1141-1158. doi: 10.1016/j.cellsig.2015.02.019.
4. Barber, S. C., Mead, R. J., and Shaw, P. J. (2006). Oxidative stress in ALS: a mechanism of neurodegeneration and a therapeutic target. Biochim. Biophys. Acta 1762, 1051-1067. doi: 10.1016/j.bbadis.2006.03.008.
5. Barbieri, E., and Sestili, P. (2012). Reactive oxygen species in skeletal muscle signaling. J. Signal. Transduct. 2012:982794. doi: 10.1155/2012/982794.
6. Bassel-Duby, R., and Olson, E. N. (2006). Signaling pathways in skeletal muscle remodeling. Annu. Rev. Biochem. 75, 19-37. doi: 10.1146/annurev.biochem.75.103004.142622.
7. Bellinger, A. M., Reiken, S., Carlson, C., Mongillo, M., Liu, X., Rothman, L., et al. (2009). Hypernitrosylated ryanodine receptor calcium release channels are leaky in dystrophic muscle. Nat. Med. 15, 325-330. doi: 10.1038/nm.1916.
8. Berneburg, M., Grether-Beck, S., Kürten, V., Ruzicka, T., Briviba, K., Sies, H., et al. (1999). Singlet oxygen mediates the UVA-induced generation of the photoaging-associated mitochondrial common deletion. J. Biol. Chem. 274, 15345-15349. doi: 10.1074/jbc.274.22.15345.
9. Brandes, R. P., Fleming, I., and Busse, R. (2005). Endothelial aging. Cardiovasc. Res. 66, 286-294. doi: 10.1016/j.cardiores.2004.12.027.
10. Brieger, K., Schiavone, S., Miller, F. J. Jr., and Krause, K. H. (2012). Reactive oxygen species: from health to disease. Swiss Med. Wkly. 142:w13659. doi: 10.4414/smw.2012.13659.
11. Cadenas, E., and Davies, K. J. (2000). Mitochondrial free radical generation, oxidative stress, and aging. Free Radic. Biol. Med. 29, 222-230. doi: 10.1016/S0891-5849(00)00317-8.
12. Cai, H., and Harrison, D. G. (2000). Endothelial dysfunction in cardiovascular diseases: the role of oxidant stress. Circ. Res. 87, 840-844. doi: 10.1161/01.RES.87.10.840.
13. Carletti, B., Passarelli, C., Sparaco, M., Tozzi, G., Pastore, A., Bertini, E., et al. (2011). Effect of protein glutathionylation on neuronal cytoskeleton: a potential link to neurodegeneration. Neuroscience 192, 285-294. doi: 10.1016/j.neuroscience.2011.05.060.
14. Carter, C. S., Hofer, T., Seo, A. Y., and Leeuwenburgh, C. (2007). Molecular mechanisms of life-and health-span extension: role of calorie restriction and exercise intervention. Appl. Physiol. Nutr. Metab. 32, 954-966. doi: 10.1139/H07-085.
15. Chen, Z. P., McConell, G. K., Michell, B. J., Snow, R. J., Canny, B. J., and Kemp, B. E. (2000). AMPK signaling in contracting human skeletal muscle: acetyl-CoA carboxylase and NO synthase phosphorylation. Am. J. Physiol. Endocrinol. Metab. 279, E1202-E1206.
16. Chin, E. R. (2005). Role of Ca2+/calmodulin-dependent kinases in skeletal muscle plasticity. J. Appl. Physiol. 99, 414-423. doi: 10.1152/japplphysiol.00015.2005.
17. Close, G. L., Ashton, T., Cable, T., Doran, D., and MacLaren, D. P. (2004). Eccentric exercise, isokinetic muscle torque and delayed onset muscle soreness: the role of reactive oxygen species. Eur. J. Appl. Physiol. 91, 615-621. doi: 10.1007/s00421-003-1012-2.
18. Cosso, R. G., Turim, J., Nantes, I. L., Almeida, A. M., Di Mascio, P., and Verces, A. E. (2002). Mitochondrial permeability transition induced by chemically generated singlet oxygen. J. Bioenerg. Biomembr. 34, 157-163. doi: 10.1023/A:1016075218162.
19. Crescenzo, R., Bianco, F., Mazzoli, A., Giacco, A., Liverini, G., and Iossa, S. (2015). Skeletal muscle mitochondrial energetic efficiency and aging. Int. J. Mol. Sci. 16, 10674-10685. doi: 10.3390/ijms160510674.
20. Cuschieri, J., and Maier, R. V. (2005). Mitogen-activated protein kinase (MAPK). Crit. Care Med. 33, S417-S419. doi: 10.1097/01.ccm.0000191714.39495.a6.
21. Daiber, A. (2010). Redox signaling (cross-talk) from and to mitochondria involves mitochondrial pores and reactive oxygen species. Biochim. Biophys. Acta 1797, 897-906. doi: 10.1016/j.bbabio.2010.01.032.
22. Di Nardo, A., Kramvis, I., Cho, N., Sadowski, A., Meikle, L., Kwiatkowski, D. J., et al. (2009). Tuberous sclerosis complex activity is required to control neuronal stress responses in an mTOR-dependent manner. J. Neurosci. 29, 5926-5937. doi: 10.1523/JNEUROSCI.0778-09.2009.
23. Duncan, J. G., Ravi, R., Stull, L. B., and Murphy, A. M. (2005). Chronic xanthine oxidase inhibition prevents myofibrillar protein oxidation and preserves cardiac function in a transgenic mouse model of cardiomyopathy. Am. J. Physiol. Heart Circ. Physiol. 289, H1512-H1518. doi: 10.1152/ajpheart.00168.2005.
24. Ebrahimian, T. G., Heymes, C., You, D., Blanc-Brude, O., Mees, B., Waeckel, L., et al. (2006). NADPH oxidase-derived overproduction of reactive oxygen species impairs postischemic neovascularization in mice with type 1 diabetes. Am. J. Pathol. 169, 719-728. doi: 10.2353/ajpath.2006.060042.
25. Egan, B., and Zierath, J. R. (2013). Exercise metabolism and the molecular regulation of skeletal muscle adaptation. Cell Metab 17, 162-184. doi: 10.1016/j.cmet.2012.12.012.
26. Erickson, J. R., He, B. J., Grumbach, I. M., and Anderson, M. E. (2011). CaMKII in the cardiovascular system: sensing redox states. Physiol. Rev. 91, 889-915. doi: 10.1152/physrev.00018.2010.
27. Erickson, J. R., Joiner, M. L., Guan, X., Kutschke, W., Yang, J., Oddis, C. V., et al. (2008). A dynamic pathway for calcium-independent activation of CaMKII by methionine oxidation. Cell 133, 462-474. doi: 10.1016/j.cell.2008.02.048.
28. Esposito, L. A., Melov, S., Panov, A., Cottrell, B. A., and Wallace, D. C. (1999). Mitochondrial disease in mouse results in increased oxidative stress. Proc. Natl. Acad. Sci. U.S.A. 96, 4820-4825. doi: 10.1073/pnas.96.9.4820.
29. Fischer, L. R., Igoudjil, A., Magrané, J., Li, Y., Hansen, J. M., Manfredi, G., et al. (2011). SOD1 targeted to the mitochondrial intermembrane space prevents motor neuropathy in the Sod1 knockout mouse. Brain 134, 196-209. doi: 10.1093/brain/awq314.
30. Fischer, L. R., Li, Y., Asress, S. A., Jones, D. P., and Glass, J. D. (2012). Absence of SOD1 leads to oxidative stress in peripheral nerve and causes a progressive distal motor axonopathy. Exp. Neurol. 233, 163-171. doi: 10.1016/j.expneurol.2011.09.020.
31. Fittipaldi, S., Dimauro, I., Mercatelli, N., and Caporossi, D. (2014). Role of exercise-induced reactive oxygen species in the modulation of heat shock protein response. Free Radic. Res. 48, 52-70. doi: 10.3109/10715762.2013.835047.
32. Fleming, I. (2010). Molecular mechanisms underlying the activation of eNOS. Pflugers Arch. 459, 793-806. doi: 10.1007/s00424-009-0767-7.
33. Galea, E., Launay, N., Portero-Otin, M., Ruiz, M., Pamplona, R., Aubourg, P., et al. (2012). Oxidative stress underlying axonal degeneration in adrenoleukodystrophy: a paradigm for multifactorial neurodegenerative diseases? Biochim. Biophys. Acta 1822, 1475-1488. doi: 10.1016/j.bbadis.2012.02.005.
34. Goldstein, J. A., and McNally, E. M. (2010). Mechanisms of muscle weakness in muscular dystrophy. J. Gen. Physiol. 136, 29-34. doi: 10.1085/jgp.201010436.
35. Gomez-Cabrera, M. C., Close, G. L., Kayani, A., McArdle, A., Viña, J., and Jackson, M. J. (2010). Effect of xanthine oxidase-generated extracellular superoxide on skeletal muscle force generation. Am. J. Physiol. Regul. Integr. Comp. Physiol. 298, R2-R8. doi: 10.1152/ajpregu.00142.2009.
36. Gomez-Cabrera, M. C., Domenech, E., and Viña, J. (2008). Moderate exercise is an antioxidant: upregulation of antioxidant genes by training. Free Radic. Biol. Med. 44, 126-131. doi: 10.1016/j.freeradbiomed.2007.02.001.
37. Griendling, K. K., and Ushio-Fukai, M. (2000). Reactive oxygen species as mediators of angiotensin II signaling. Regul. Pept. 91, 21-27. doi: 10.1016/S0167-0115(00)00136-1.
38. Hart, J. D., and Dulhunty, A. F. (2000). Nitric oxide activates or inhibits skeletal muscle ryanodine receptors depending on its concentration, membrane potential and ligand binding. J. Membr. Biol. 173, 227-236. doi: 10.1007/s002320001022.
39. Hawley, J. A., Hargreaves, M., and Zierath, J. R. (2006). Signalling mechanisms in skeletal muscle: role in substrate selection and muscle adaptation. Essays Biochem. 42, 1-12. doi: 10.1042/bse0420001.
40. Hayashi, Y., Sawa, Y., Nishimura, M., Fukuyama, N., Ichikawa, H., Ohtake, S., et al. (2004). Peroxynitrite, a product between nitric oxide and superoxide anion, plays a cytotoxic role in the development of post-bypass systemic inflammatory response. Eur. J. Cardiothorac. Surg. 26, 276-280. doi: 10.1016/j.ejcts.2004.03.033.
41. Hensley, K., and Floyd, R. A. (2002). Reactive oxygen species and protein oxidation in aging: a look back, a look ahead. Arch. Biochem. Biophys. 397, 377-383. doi: 10.1006/abbi.2001.2630.
42. Hepple, R. T., Hagen, J. L., Krause, D. J., and Jackson, C. C. (2003). Aerobic power declines with aging in rat skeletal muscles perfused at matched convective O2 delivery. J. Appl. Physiol. 94, 744-751. doi: 10.1152/japplphysiol.00737.2002.
43. Hirschfield, W., Moody, M. R., O'Brien, W. E., Gregg, A. R., Bryan, R. M. Jr., and Reid, M. B. (2000). Nitric oxide release and contractile properties of skeletal muscles from mice deficient in type III NOS. Am. J. Physiol. Regul. Integr. Comp. Physiol. 278, R95-R100.
44. Hood, D. A. (2001). Invited Review: contractile activity-induced mitochondrial biogenesis in skeletal muscle. J. Appl. Physiol. 90, 1137-1157.
45. Irrcher, I., Ljubicic, V., and Hood, D. A. (2009). Interactions between ROS and AMP kinase activity in the regulation of PGC-1alpha transcription in skeletal muscle cells. Am. J. Physiol. Cell Physiol. 296, C116-C123. doi: 10.1152/ajpcell.00267.2007.
46. Jackson, J. R., Ryan, M. J., and Alway, S. E. (2011). Long-term supplementation with resveratrol alleviates oxidative stress but does not attenuate sarcopenia in aged mice. J. Gerontol. A Biol. Sci. Med. Sci. 66, 751-764. doi: 10.1093/gerona/glr047.
47. Jackson, J. R., Ryan, M. J., Hao, Y., and Alway, S. E. (2010). Mediation of endogenous antioxidant enzymes and apoptotic signaling by resveratrol following muscle disuse in the gastrocnemius muscles of young and old rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 299, R1572-R1581. doi: 10.1152/ajpregu.00489.2010.
48. Jackson, M. J. (2008). Free radicals generated by contracting muscle: by-products of metabolism or key regulators of muscle function? Free Radic. Biol. Med. 44, 132-141. doi: 10.1016/j.freeradbiomed.2007.06.003.
49. Jackson, M. J. (2011). Control of reactive oxygen species production in contracting skeletal muscle. Antioxid. Redox Signal. 15, 2477-2486. doi: 10.1089/ars.2011.3976.
50. Ji, L. L. (2008). Modulation of skeletal muscle antioxidant defense by exercise: role of redox signaling. Free Radic. Biol. Med. 44, 142-152. doi: 10.1016/j.freeradbiomed.2007.02.031.
51. Kirkinezos, I. G., and Moraes, C. T. (2001). Reactive oxygen species and mitochondrial diseases. Semin. Cell Dev. Biol. 12, 449-457. doi: 10.1006/scdb.2001.0282.
52. Kobzik, L., Reid, M. B., Bredt, D. S., and Stamler, J. S. (1994). Nitric oxide in skeletal muscle. Nature 372, 546-548. doi: 10.1038/372546a0.
53. Koga, T., Umeda, T., Kojima, A., Tanabe, M., Yamamoto, Y., Takahashi, I., et al. (2013). Influence of a 3-month training program on muscular damage and neutrophil function in male university freshman judoists. Luminescence 28, 136-142. doi: 10.1002/bio.2352.
54. Kothari, S., Thompson, A., Agarwal, A., and du Plessis, S. S. (2010). Free radicals: their beneficial and detrimental effects on sperm function. Indian J. Exp. Biol. 48, 425-435.
55. Kowaltowski, A. J., De Souza-Pinto, N. C., Castilho, R. F., and Vercesi, A. E. (2009). Mitochondria and reactive oxygen species. Free Radic. Biol. Med. 47, 333-343. doi: 10.1016/j.freeradbiomed.2009.05.004.
56. Kruska, N., Schönfeld, P., Pujol, A., and Reiser, G. (2015). Astrocytes and mitochondria from adrenoleukodystrophy protein (ABCD1)-deficient mice reveal that the adrenoleukodystrophy-associated very long-chain fatty acids target several cellular energy-dependent functions. Biochim. Biophys. Acta 1852, 925-936. doi: 10.1016/j.bbadis.2015.01.005.
57. Kuwahara, H., Horie, T., Ishikawa, S., Tsuda, C., Kawakami, S., Noda, Y., et al. (2010). Oxidative stress in skeletal muscle causes severe disturbance of exercise activity without muscle atrophy. Free Radic. Biol. Med. 48, 1252-1262. doi: 10.1016/j.freeradbiomed.2010.02.011.
58. Lecker, S. H., Jagoe, R. T., Gilbert, A., Gomes, M., Baracos, V., Bailey, J., et al. (2004). Multiple types of skeletal muscle atrophy involve a common program of changes in gene expression. FASEB J. 18, 39-51. doi: 10.1096/fj.03-0610com.
59. Lemasters, J. J., Nieminen, A. L., Qian, T., Trost, L. C., Elmore, S. P., Nishimura, Y., et al. (1998). The mitochondrial permeability transition in cell death: a common mechanism in necrosis, apoptosis and autophagy. Biochim. Biophys. Acta 1366, 177-196. doi: 10.1016/S0005-2728(98)00112-1.
60. Lemasters, J. J., Theruvath, T. P., Zhong, Z., and Nieminen, A. L. (2009). Mitochondrial calcium and the permeability transition in cell death. Biochim. Biophys. Acta 1787, 1395-1401. doi: 10.1016/j.bbabio.2009.06.009.
61. Lightfoot, A. P., McCormick, R., Nye, G. A., and McArdle, A. (2014). Mechanisms of skeletal muscle ageing; avenues for therapeutic intervention. Curr. Opin. Pharmacol. 16, 116-121. doi: 10.1016/j.coph.2014.05.005.
62. Liochev, S. I. (2013). Reactive oxygen species and the free radical theory of aging. Free Radic. Biol. Med. 60, 1-4. doi: 10.1016/j.freeradbiomed.2013.02.011.
63. Lobo, V., Patil, A., Phatak, A., and Chandra, N. (2010). Free radicals, antioxidants and functional foods: Impact on human health. Pharmacogn. Rev. 4, 118-126. doi: 10.4103/0973-7847.70902.
64. Lustgarten, M. S., Jang, Y. C., Liu, Y., Qi, W., Qin, Y., Dahia, P. L., et al. (2011). MnSOD deficiency results in elevated oxidative stress and decreased mitochondrial function but does not lead to muscle atrophy during aging. Aging Cell 10, 493-505. doi: 10.1111/j.1474-9726.2011.00695.x.
65. Malik, V., Rodino-Klapac, L. R., and Mendell, J. R. (2012). Emerging drugs for Duchenne muscular dystrophy. Expert Opin. Emerg. Drugs. 17, 261-277. doi: 10.1517/14728214.2012.691965.
66. Mandal, D., Fu, P., and Levine, A. D. (2010). REDOX regulation of IL-13 signaling in intestinal epithelial cells: usage of alternate pathways mediates distinct gene expression patterns. Cell. Signal. 22, 1485-1494. doi: 10.1016/j.cellsig.2010.05.017.
67. Meng, S. J., and Yu, L. J. (2010). Oxidative stress, molecular inflammation and sarcopenia. Int. J. Mol. Sci. 11, 1509-1526. doi: 10.3390/ijms11041509.
68. Merry, T. L., Steinberg, G. R., Lynch, G. S., and McConell, G. K. (2010). Skeletal muscle glucose uptake during contraction is regulated by nitric oxide and ROS independently of AMPK. Am. J. Physiol. Endocrinol. Metab. 298, E577-E585. doi: 10.1152/ajpendo.00239.2009.
69. Morris, G., Anderson, G., Berk, M., and Maes, M. (2013). Coenzyme Q10 depletion in medical and neuropsychiatric disorders: potential repercussions and therapeutic implications. Mol. Neurobiol. 48, 883-903. doi: 10.1007/s12035-013-8477-8.
70. Moylan, J. S., and Reid, M. B. (2007). Oxidative stress, chronic disease, and muscle wasting. Muscle Nerve 35, 411-429. doi: 10.1002/mus.20743.
71. Muller, F. L., Song, W., Jang, Y. C., Liu, Y., Sabia, M., Richardson, A., et al. (2007). Denervation-induced skeletal muscle atrophy is associated with increased mitochondrial ROS production. Am. J. Physiol. Regul. Integr. Comp. Physiol. 293, R1159-R1168. doi: 10.1152/ajpregu.00767.2006.
72. Nathan, C., and Cunningham-Bussel, A. (2013). Beyond oxidative stress: an immunologist's guide to reactive oxygen species. Nat. Rev. Immunol. 13, 349-361. doi: 10.1038/nri3423.
73. Ochala, J., Gustafson, A. M., Diez, M. L., Renaud, G., Li, M., Aare, S., et al. (2011). Preferential skeletal muscle myosin loss in response to mechanical silencing in a novel rat intensive care unit model: underlying mechanisms. J. Physiol. 589, 2007-2026. doi: 10.1113/jphysiol.2010.202044.
74. Ojuka, E. O., Goyaram, V., and Smith, J. A. (2012). The role of CaMKII in regulating GLUT4 expression in skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 303, E322-E331. doi: 10.1152/ajpendo.00091.2012.
75. Ozcan, U., Ozcan, L., Yilmaz, E., Düvel, K., Sahin, M., Manning, B. D., et al. (2008). Loss of the tuberous sclerosis complex tumor suppressors triggers the unfolded protein response to regulate insulin signaling and apoptosis. Mol. Cell 29, 541-551. doi: 10.1016/j.molcel.2007.12.023.
76. Picard, M., Juster, R. P., and McEwen, B. S. (2014). Mitochondrial allostatic load puts the 'gluc' back in glucocorticoids. Nat. Rev. Endocrinol. 10, 303-310. doi: 10.1038/nrendo.2014.22.
77. Powers, S. K., Duarte, J., Kavazis, A. N., and Talbert, E. E. (2010). Reactive oxygen species are signalling molecules for skeletal muscle adaptation. Exp. Physiol. 95, 1-9. doi: 10.1113/expphysiol.2009.050526.
78. Powers, S. K., Talbert, E. E., and Adhihetty, P. J. (2011). Reactive oxygen and nitrogen species as intracellular signals in skeletal muscle. J. Physiol. 589, 2129-2138. doi: 10.1113/jphysiol.2010.201327.
79. Radak, Z., Chung, H. Y., and Goto, S. (2005). Exercise and hormesis: oxidative stress-related adaptation for successful aging. Biogerontology 6, 71-75. doi: 10.1007/s10522-004-7386-7.
80. Reid, M. B., and Moylan, J. S. (2011). Beyond atrophy: redox mechanisms of muscle dysfunction in chronic inflammatory disease. J. Physiol. 589, 2171-2179. doi: 10.1113/jphysiol.2010.203356.
81. Ryan, M. J., Jackson, J. R., Hao, Y., Williamson, C. L., Dabkowski, E. R., Hollander, J. M., et al. (2010). Suppression of oxidative stress by resveratrol after isometric contractions in gastrocnemius muscles of aged mice. J. Gerontol. A Biol. Sci. Med. Sci. 65, 815-831. doi: 10.1093/gerona/glq080.
82. Schroeder, M. A., Atherton, H. J., Ball, D. R., Cole, M. A., Heather, L. C., Griffin, J. L., et al. (2009). Real-time assessment of Krebs cycle metabolism using hyperpolarized 13C magnetic resonance spectroscopy. FASEB J. 23, 2529-2538. doi: 10.1096/fj.09-129171.
83. Sengupta, S., Peterson, T. R., and Sabatini, D. M. (2010). Regulation of the mTOR complex 1 pathway by nutrients, growth factors, and stress. Mol. Cell 40, 310-322. doi: 10.1016/j.molcel.2010.09.026.
84. Shahar, S., Kamaruddin, N. S., Badrasawi, M., Sakian, N. I., Abd Manaf, Z., Yassin, Z., et al. (2013). Effectiveness of exercise and protein supplementation intervention on body composition, functional fitness, and oxidative stress among elderly Malays with sarcopenia. Clin. Interv. Aging 8, 1365-1375. doi: 10.2147/CIA.S46826.
85. Shi, Y., Pulliam, D. A., Liu, Y., Hamilton, R. T., Jernigan, A. L., Bhattacharya, A., et al. (2013). Reduced mitochondrial ROS, enhanced antioxidant defense, and distinct age-related changes in oxidative damage in muscles of long-lived Peromyscus leucopus. Am. J. Physiol. Regul. Integr. Comp. Physiol. 304, R343-R355. doi: 10.1152/ajpregu.00139.2012.
86. Sindler, A. L., Delp, M. D., Reyes, R., Wu, G., and Muller-Delp, J. M. (2009). Effects of ageing and exercise training on eNOS uncoupling in skeletal muscle resistance arterioles. J. Physiol. 587, 3885-3897. doi: 10.1113/jphysiol.2009.172221.
87. Sinha, K., Das, J., Pal, P. B., and Sil, P. C. (2013). Oxidative stress: the mitochondria-dependent and mitochondria-independent pathways of apoptosis. Arch. Toxicol. 87, 1157-1180. doi: 10.1007/s00204-013-1034-4.
88. Stamler, J. S., and Meissner, G. (2001). Physiology of nitric oxide in skeletal muscle. Physiol. Rev. 81, 209-237.
89. Sun, Y., Zhang, J., Lu, L., Chen, S. S., Quinn, M. T., and Weber, K. T. (2002). Aldosterone-induced inflammation in the rat heart: role of oxidative stress. Am. J. Pathol. 161, 1773-1781. doi: 10.1016/S0002-9440(10)64454-9.
90. Thomas, C., Mackey, M. M., Diaz, A. A., and Cox, D. P. (2009). Hydroxyl radical is produced via the Fenton reaction in submitochondrial particles under oxidative stress: implications for diseases associated with iron accumulation. Redox Rep. 14, 102-108. doi: 10.1179/135100009X392566.
91. Tidball, J. G., and Wehling-Henricks, M. (2007). The role of free radicals in the pathophysiology of muscular dystrophy. J. Appl. Physiol. 102, 1677-1686. doi: 10.1152/japplphysiol.01145.2006.
92. Turrens, J. F. (2003). Mitochondrial formation of reactive oxygen species. J. Physiol. 552, 335-344. doi: 10.1113/jphysiol.2003.049478.
93. Vollaard, N. B., Shearman, J. P., and Cooper, C. E. (2005). Exercise-induced oxidative stress:myths, realities and physiological relevance. Sports Med. 35, 1045-1062. doi: 10.2165/00007256-200535120-00004.
94. von Haehling, S., Morley, J. E., and Anker, S. D. (2010). An overview of sarcopenia: facts and numbers on prevalence and clinical impact. J. Cachexia Sarcopenia Muscle 1, 129-133. doi: 10.1007/s13539-010-0014-2.
95. Wakil, S. J., and Abu-Elheiga, L. A. (2009). Fatty acid metabolism: target for metabolic syndrome. J. Lipid Res. 50(Suppl.), S138-S143. doi: 10.1194/jlr. R800079-JLR200.
96. Weinberg, J. B. (2000). Nitric oxide synthase 2 and cyclooxygenase 2 interactions in inflammation. Immunol. Res. 22, 319-341. doi: 10.1385/IR:22:2-3:319.
97. Westerblad, H., and Allen, D. G. (2011). Emerging roles of ROS/RNS in muscle function and fatigue. Antioxid. Redox Signal. 15, 2487-2499. doi: 10.1089/ars.2011.3909.
98. Williams, M. D., Van Remmen, H., Conrad, C. C., Huang, T. T., Epstein, C. J., and Richardson, A. (1998). Increased oxidative damage is correlated to altered mitochondrial function in heterozygous manganese superoxide dismutase knockout mice. J. Biol. Chem. 273, 28510-28515. doi: 10.1074/jbc.273.43.28510.
99. Wright, D. C., Hucker, K. A., Holloszy, J. O., and Han, D. H. (2004). Ca2+ and AMPK both mediate stimulation of glucose transport by muscle contractions. Diabetes 53, 330-335. doi: 10.2337/diabetes.53.2.330.
100. Wu, D., and Cederbaum, A. I. (2003). Alcohol, oxidative stress, and free radical damage. Alcohol Res. Health 27, 277-284.
101. Xie, Z., Dong, Y., Zhang, M., Cui, M. Z., Cohen, R. A., Riek, U., et al. (2006). Activation of protein kinase C zeta by peroxynitrite regulates LKB1-dependent AMP-activated protein kinase in cultured endothelial cells. J. Biol. Chem. 281, 6366-6375. doi: 10.1074/jbc. M511178200.
102. Zalk, R., Clarke, O. B., des Georges, A., Grassucci, R. A., Reiken, S., Mancia, F., et al. (2015). Structure of a mammalian ryanodine receptor. Nature 517, 44-49. doi: 10.1038/nature13950.
103. Zuo, L., Best, T. M., Roberts, W. J., Diaz, P. T., and Wagner, P. D. (2015a). Characterization of reactive oxygen species in diaphragm. Acta Physiol. 213, 700-710. doi: 10.1111/apha.12410.
104. Zuo, L., Diaz, P. T., Chien, M. T., Roberts, W. J., Kishek, J., Best, T. M., et al. (2014a). PO2 cycling reduces diaphragm fatigue by attenuating ROS formation. PLoS ONE 9:e109884. doi: 10.1371/journal.pone.0109884.
105. Zuo, L., Hallman, A. H., Roberts, W. J., Wagner, P. D., and Hogan, M. C. (2014b). Superoxide release from contracting skeletal muscle in pulmonary TNF-alpha overexpression mice. Am. J. Physiol. Regul. Integr. Comp. Physiol. 306, R75-R81. doi: 10.1152/ajpregu.00425.2013.
106. Zuo, L., Hallman, A. H., Yousif, M. K., and Chien, M. T. (2012). Oxidative stress, respiratory muscle dysfunction, and potential therapeutics in chronic obstructive pulmonary disease. Front. Biol. 7, 506-513. doi: 10.1007/s11515-012-1251-x.
107. Zuo, L., He, F., Sergakis, G. G., Koozehchian, M. S., Stimpfl, J. N., Rong, Y., et al. (2014c). Interrelated role of cigarette smoking, oxidative stress, and immune response in COPD and corresponding treatments. Am. J. Physiol. Lung Cell Mol. Physiol. 307, L205-L218. doi: 10.1152/ajplung.00330.2013.
108. Zuo, L., Nogueira, L., and Hogan, M. C. (2011a). Reactive oxygen species formation during tetanic contractions in single isolated Xenopus myofibers. J. Appl. Physiol. 111, 898-904. doi: 10.1152/japplphysiol.00398.2011.
109. Zuo, L., Shiah, A., Roberts, W. J., Chien, M. T., Wagner, P. D., and Hogan, M. C. (2013). Low Po(2) conditions induce reactive oxygen species formation during contractions in single skeletal muscle fibers. Am. J. Physiol. Regul. Integr. Comp. Physiol. 304, R1009-R1016. doi: 10.1152/ajpregu.00563.2012.
110. Zuo, L., Youtz, D. J., and Wold, L. E. (2011b). Particulate matter exposure exacerbates high glucose-induced cardiomyocyte dysfunction through ROS generation. PLoS ONE 6:e23116. doi: 10.1371/journal.pone.0023116.
111. Zuo, L., Zhou, T., Pannell, B. K., Ziegler, A. C., and Best, T. M. (2015b). Biological and physiological role of reactive oxygen species-the good, the bad and the ugly. Acta Physiol. 214, 329-348. doi: 10.1111/apha.12515.