Redox Characterization of Functioning Skeletal Muscle
Open accessAbstract
Skeletal muscle physiology is influenced by the presence of chemically reactive molecules such as reactive oxygen species (ROS). These molecules regulate multiple redox-sensitive signaling pathways that play a critical role in cellular processes including gene expression and protein modification. While ROS have gained much attention for their harmful effects in muscle fatigue and dysfunction, research has also shown ROS to facilitate muscle adaptation after stressors such as physical exercise. This manuscript aims to provide a comprehensive review of the current understanding of redox signaling in skeletal muscle. ROS-induced oxidative stress and its role in the aging process are discussed. Mitochondria have been shown to generate large amounts of ROS during muscular contractions, and thus are susceptible to oxidative stress. ROS can modify proteins located in the mitochondrial membrane leading to cell death and osmotic swelling. ROS also contribute to the necrosis and inflammation of muscle fibers that is associated with muscular diseases including Duchenne muscular dystrophy. It is imperative that future research continues to investigate the exact role of ROS in normal skeletal muscle function as well as muscular dysfunction and disease.
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Oxidative stress is a major trigger of imbalance between protein synthesis and degradation leading to muscle atrophy.
“Oxidative stress, characterized by increased reactive oxygen species (ROS) production and impairment of antioxidant defense systems, is also a major trigger of imbalance between protein synthesis and degradation leading to muscle atrophy [10,11].”
From Nutraceuticals in the Prevention and Treatment of the Muscle Atrophy (2021) · cites this paper as [11]
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1 retracted
Mandal, D., Fu, P., & Levine, A. D. (2010) · Cellular Signalling · doi:10.1016/j.cellsig.2010.05.017 · Cited by 47 · see citing works
RetractedCalcium's Role in Mechanotransduction during Muscle Development
Damm, T. B., & Egli, M. (2014) · Cellular Physiology and Biochemistry · doi:10.1159/000356667 · Cited by 14,548 · see citing works
Free radicals, antioxidants and functional foods: impact on human health
Lobo, V, Patil, A., Phatak, A., & Chandra, N. (2010) · Pharmacognosy Reviews · doi:10.4103/0973-7847.70902 · Cited by 5,435 · see citing works
Mitochondrial formation of reactive oxygen species
Turrens, J. F. (2003) · The Journal of Physiology · doi:10.1113/jphysiol.2003.049478 · Cited by 5,084 · see citing works
Oxyl radicals, redox-sensitive signalling cascades and antioxidants
Genestra, M. (2007) · Cellular Signalling · doi:10.1016/j.cellsig.2007.04.009 · Cited by 4,930 · see citing works
Endothelial dysfunction in cardiovascular diseases: the role of oxidant stress
Cai, H., & Harrison, D. G. (2000) · Circulation Research · doi:10.1161/01.res.87.10.840 · Cited by 3,839 · see citing works
Mitochondrial free radical generation, oxidative stress, and aging
Cadenas, E., & Davies, K. J. A. (2000) · Free Radical Biology and Medicine · doi:10.1016/s0891-5849(00)00317-8 · Cited by 3,010 · see citing works
Exercise Metabolism and the Molecular Regulation of Skeletal Muscle Adaptation
Egan, B., & Zierath, J. R. (2013) · Cell Metabolism · doi:10.1016/j.cmet.2012.12.012 · Cited by 2,084 · see citing works
Oxidative stress: the mitochondria-dependent and mitochondria-independent pathways of apoptosis
Sinha, K., Das, J., Pal, P. B., & Sil, P. C. (2013) · Archives of Toxicology · doi:10.1007/s00204-013-1034-4 · Cited by 1,622 · see citing works
Beyond oxidative stress: an immunologist's guide to reactive oxygen species
Nathan, C., & Cunningham-Bussel, A. (2013) · Nature Reviews Immunology · doi:10.1038/nri3423 · Cited by 1,619 · see citing works
Multiple types of skeletal muscle atrophy involve a common program of changes in gene expression
Lecker, S. H., Jagoe, R. T., Gilbert, A., Gomes, M., Baracos, V., Bailey, J., Price, S. R., Mitch, W. E., & Goldberg, A. L. (2004) · The FASEB Journal · doi:10.1096/fj.03-0610com · Cited by 1,539 · see citing works
Lemasters, J. J., Nieminen, A.-L., Qian, T., Trost, L. C., Elmore, S. P., Nishimura, Y., Crowe, R. A., Cascio, W. E., Bradham, C. A., Brenner, D. A., et al. (1998) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/s0005-2728(98)00112-1 · Cited by 1,387 · see citing works
Regulation of the mTOR Complex 1 Pathway by Nutrients, Growth Factors, and Stress
Sengupta, S., Peterson, T. R., & Sabatini, D. M. (2010) · Molecular Cell · doi:10.1016/j.molcel.2010.09.026 · Cited by 1,234 · see citing works
Alcohol, oxidative stress and free radical damage
Albano, E. (2006) · Proceedings of The Nutrition Society · doi:10.1079/pns2006496 · Cited by 1,216 · see citing works
Mitochondria and reactive oxygen species
Kowaltowski, A. J., de Souza-Pinto, N. C., Castilho, R. F., & Vercesi, A. E. (2009) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2009.05.004 · Cited by 1,162 · see citing works
Reactive oxygen species: from health to disease
Brieger, K., Schiavone, S., Miller Jr., F. J., & Krause, K.-H. (2012) · Swiss Medical Weekly · doi:10.4414/smw.2012.13659 · Cited by 1,133 · see citing works
A Dynamic Pathway for Calcium-Independent Activation of CaMKII by Methionine Oxidation
Erickson, J. R., Joiner, M.-L. A., Guan, X., Kutschke, W., Yang, J., Oddis, C. V., Bartlett, R. K., Lowe, J. S., O'Donnell, S. E., Aykin-Burns, N., et al. (2008) · Cell · doi:10.1016/j.cell.2008.02.048 · Cited by 1,122 · see citing works
Physiology of Nitric Oxide in Skeletal Muscle
Stamler, J. S., & Meissner, G. (2001) · Physiological Reviews · doi:10.1152/physrev.2001.81.1.209 · Cited by 1,080 · see citing works
Krötz, F., Sohn, H., & Pohl, U. (2004) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.0000145574.90840.7d · Cited by 1,026 · see citing works
Moderate exercise is an antioxidant: Upregulation of antioxidant genes by training
Gomez-Cabrera, M.-C., Domenech, E., & Viña, J. (2008) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2007.02.001 · Cited by 1,020 · see citing works
Nitric oxide in skeletal muscle
Kobzik, L., Reid, M. B., Bredt, D. S., & Stamler, J. S. (1994) · Nature · doi:10.1038/372546a0 · Cited by 955 · see citing works
An overview of sarcopenia: facts and numbers on prevalence and clinical impact
von Haehling, S., Morley, J. E., & Anker, S. D. (2010) · Journal of Cachexia, Sarcopenia and Muscle · doi:10.1007/s13539-010-0014-2 · Cited by 888 · see citing works
Signaling Pathways in Skeletal Muscle Remodeling
Bassel‐Duby, R., & Olson, E. N. (2006) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.75.103004.142622 · Cited by 799 · see citing works
Reactive oxygen species and the free radical theory of aging
Liochev, S. I. (2013) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2013.02.011 · Cited by 768 · see citing works
Fatty acid metabolism: Target for metabolic syndrome
Wakil, S. J., & Abu-Elheiga, L. A. (2009) · Journal of Lipid Research · doi:10.1194/jlr.r800079-jlr200 · Cited by 731 · see citing works
Invited Review: Contractile activity-induced mitochondrial biogenesis in skeletal muscle
Hood, D. A. (2001) · Journal of Applied Physiology · doi:10.1152/jappl.2001.90.3.1137 · Cited by 692 · see citing works
Mitochondrial calcium and the permeability transition in cell death
Lemasters, J. J., Theruvath, T. P., Zhong, Z., & Nieminen, A. (2009) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2009.06.009 · Cited by 656 · see citing works
Alcohol, oxidative stress, and free radical damage.
Wu, D., & Cederbaum, A. I. (2003) · Europe PMC (PubMed Central) · Cited by 651 · see citing works
Oxidative Stress, Molecular Inflammation and Sarcopenia
Meng, S.-J., & Yu, L.-J. (2010) · International Journal of Molecular Sciences · doi:10.3390/ijms11041509 · Cited by 637 · see citing works
Mitochondrial disease in mouse results in increased oxidative stress
Esposito, L., Melov, S., Panov, A. V., Cottrell, B. A., & Wallace, D. C. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.9.4820 · Cited by 637 · see citing works
Aldosterone-Induced Inflammation in the Rat Heart
Sun, Y., Zhang, J., Lu, L., Chen, S. S., Quinn, M. T., & Weber, K. T. (2002) · American Journal Of Pathology · doi:10.1016/s0002-9440(10)64454-9 · Cited by 568 · see citing works
BRANDES, R., FLEMING, I., & BUSSE, R. (2005) · Cardiovascular Research · doi:10.1016/j.cardiores.2004.12.027 · Cited by 563 · see citing works
Hypernitrosylated ryanodine receptor calcium release channels are leaky in dystrophic muscle
Bellinger, A. M., Reiken, S. R., Carlson, C., Mongillo, M., Liu, X., Rothman, L. R., Matecki, S., Lacampagne, A., & Marks, A. R. (2009) · Nature Medicine · doi:10.1038/nm.1916 · Cited by 532 · see citing works
Oxidative stress in ALS: A mechanism of neurodegeneration and a therapeutic target
Barber, S. C., Mead, R. J., & Shaw, P. J. (2006) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2006.03.008 · Cited by 475 · see citing works
Williams, M. D., Remmen, H. V., Conrad, C. C., Huang, T., Epstein, C. J., & Richardson, A. G. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.43.28510 · Cited by 453 · see citing works
Reactive Oxygen Species Are Signalling Molecules for Skeletal Muscle Adaptation
Powers, S. K., Duarte, J., Kavazis, A. N., & Talbert, E. E. (2010) · Experimental Physiology · doi:10.1113/expphysiol.2009.050526 · Cited by 440 · see citing works
Structure of a mammalian ryanodine receptor
Zalk, R., Clarke, O. B., Georges, A. D., Grassucci, R. A., Reiken, S. R., Mancia, F., Hendrickson, W. A., Frank, J., & Marks, A. R. (2014) · Nature · doi:10.1038/nature13950 · Cited by 439 · see citing works
Molecular mechanisms underlying the activation of eNOS
Fleming, I. (2010) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-009-0767-7 · Cited by 437 · see citing works
Özcan, U., Özcan, L., Yılmaz, E., Düvel, K., Şahin, M., Manning, B. D., & Hotamışlıgil, G. S. (2008) · Molecular Cell · doi:10.1016/j.molcel.2007.12.023 · Cited by 434 · see citing works
Biological and physiological role of reactive oxygen species - the good, the bad and the ugly
Zuo, L., Zhou, T., Pannell, B. K., Ziegler, A. C., & Best, T. M. (2015) · Acta Physiologica · doi:10.1111/apha.12515 · Cited by 430 · see citing works
Reactive oxygen species as mediators of angiotensin II signaling
Griendling, K. K., & Ushio‐Fukai, M. (2000) · Regulatory Peptides · doi:10.1016/s0167-0115(00)00136-1 · Cited by 417 · see citing works
Oxidative Stress, Chronic Disease, and Muscle Wasting
Moylan, J. S., & Reid, M. B. (2007) · Muscle & Nerve · doi:10.1002/mus.20743 · Cited by 416 · see citing works
Reactive Oxygen Species in Skeletal Muscle Signaling
Barbieri, E., & Sestili, P. (2011) · Journal of Signal Transduction · doi:10.1155/2012/982794 · Cited by 414 · see citing works
Exercise and hormesis: oxidative stress-related adaptation for successful aging
Radak, Z. O., Chung, H. Y., & Goto, S. (2005) · Biogerontology · doi:10.1007/s10522-004-7386-7 · Cited by 413 · see citing works
Mitochondrial allostatic load puts the 'gluc' back in glucocorticoids
Picard, M., Juster, R.-P., & McEwen, B. S. (2014) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2014.22 · Cited by 405 · see citing works
Ca2+ and AMPK Both Mediate Stimulation of Glucose Transport by Muscle Contractions
Wright, D. C., Hucker, K. A., Holloszy, J. O., & Han, D. H. (2004) · Diabetes · doi:10.2337/diabetes.53.2.330 · Cited by 398 · see citing works
Reactive oxygen species and mitochondrial diseases
Kirkinezos, I. G., & Moraes, C. T. (2001) · Seminars in Cell and Developmental Biology · doi:10.1006/scdb.2001.0282 · Cited by 385 · see citing works
Berneburg, M., Grether‐Beck, S., Kürten, V., Ruzicka, T., Briviba, K., Sies, H., & Krutmann, J. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.22.15345 · Cited by 369 · see citing works
Irrcher, I., Ljubicic, V., & Hood, D. A. (2009) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00267.2007 · Cited by 356 · see citing works
Muller, F. L., Song, W., Jang, Y. C., Liu, Y., Sabia, M., Richardson, A., & Van Remmen, H. (2007) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00767.2006 · Cited by 355 · see citing works
Daiber, A. (2010) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2010.01.032 · Cited by 347 · see citing works
Chen, Z., McConell, G. K., Michell, B. J., Snow, R. J., Canny, B. J., & Kemp, B. E. (2000) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.2000.279.5.e1202 · Cited by 342 · see citing works
Reactive oxygen and nitrogen species as intracellular signals in skeletal muscle
Powers, S. K., Talbert, E. E., & Adhihetty, P. J. (2011) · The Journal of Physiology · doi:10.1113/jphysiol.2010.201327 · Cited by 340 · see citing works
Exercise-Induced Oxidative Stress
Vollaard, N. B. J., Shearman, J., & Cooper, C. E. (2005) · Sports Medicine · doi:10.2165/00007256-200535120-00004 · Cited by 326 · see citing works
Thomas, C., Mackey, M. M., Diaz, A. A., & Cox, D. P. (2009) · Redox Report · doi:10.1179/135100009x392566 · Cited by 307 · see citing works
Modulation of skeletal muscle antioxidant defense by exercise: Role of redox signaling
Ji, L. L. (2007) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2007.02.031 · Cited by 291 · see citing works
Free radicals: their beneficial and detrimental effects on sperm function.
Kothari, S., Thompson, A., Agarwal, A. K., & du Plessis, S. S. (2010) · PubMed · Cited by 271 · see citing works
Reactive Oxygen Species and Protein Oxidation in Aging: A Look Back, A Look Ahead
Hensley, K., & Floyd, R. A. (2002) · Archives of Biochemistry and Biophysics · doi:10.1006/abbi.2001.2630 · Cited by 255 · see citing works
Zuo, L., He, F., Sergakis, G. G., Koozehchian, M., Stimpfl, J. N., Rong, Y., Diaz, P. T., & Best, T. M. (2014) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.00330.2013 · Cited by 247 · see citing works
Effect of denervation on mitochondrially mediated apoptosis in skeletal muscle.
Adhihetty, P. J., O'Leary, M. F. N., Chabi, B., Wicks, K. L., & Hood, D. A. (2007) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00768.2006 · Cited by 240 · see citing works
CaMKII in the Cardiovascular System: Sensing Redox States
Erickson, J. R., He, B. J., Grumbach, I. M., & Anderson, M. E. (2011) · Physiological Reviews · doi:10.1152/physrev.00018.2010 · Cited by 238 · see citing works
The role of free radicals in the pathophysiology of muscular dystrophy
Tidball, J. G., & Wehling‐Henricks, M. (2006) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01145.2006 · Cited by 232 · see citing works
Role of Ca2+/calmodulin-dependent kinases in skeletal muscle plasticity
Chin, E. R. (2005) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00015.2005 · Cited by 229 · see citing works
Schroeder, M., Atherton, H. J., Ball, D. R., Cole, M. A., Heather, L. C., Griffin, J. L., Clarke, K., Radda, G. K., & Tyler, D. J. (2009) · The FASEB Journal · doi:10.1096/fj.09-129171 · Cited by 221 · see citing works
Xie, Z., Dong, Y., Zhang, M., Cui, M.-Z., Cohen, R. A., Riek, U., Neumann, D., Schlattner, U., & Zou, M.-H. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m511178200 · Cited by 172 · see citing works
Di Nardo, A., Kramvis, I., Cho, N., Sadowski, A., Meikle, L., Kwiatkowski, D. J., & Sahin, M. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.0778-09.2009 · Cited by 165 · see citing works
Plasticity of Skeletal Muscle Mitochondria in Response to Contractile Activity
Adhihetty, P. J., Irrcher, I., Joseph, A., Ljubicic, V., & Hood, D. A. (2003) · Experimental Physiology · doi:10.1113/eph8802505 · Cited by 165 · see citing works
Ebrahimian, T. G., Heymes, C., Broquères-You, D., Blanc‐Brude, O., Mees, B., Waeckel, L., Duriez, M., Vilar, J., Brandes, R. P., Levy, B. I., et al. (2006) · American Journal Of Pathology · doi:10.2353/ajpath.2006.060042 · Cited by 163 · see citing works
Jackson, M. J. (2007) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2007.06.003 · Cited by 161 · see citing works
Effects of ageing and exercise training on eNOS uncoupling in skeletal muscle resistance arterioles
Sindler, A. L., Delp, M. D., Reyes, R., Wu, G., & Muller‐Delp, J. M. (2009) · The Journal of Physiology · doi:10.1113/jphysiol.2009.172221 · Cited by 156 · see citing works
Close, G. L., Ashton, T., Cable, N. T., Doran, D. A., & MacLaren, D. P. M. (2004) · European Journal of Applied Physiology · doi:10.1007/s00421-003-1012-2 · Cited by 146 · see citing works
Control of Reactive Oxygen Species Production in Contracting Skeletal Muscle
Jackson, M. J. (2011) · Antioxidants and Redox Signaling · doi:10.1089/ars.2011.3976 · Cited by 145 · see citing works
Jackson, J. R., Ryan, M. J., & Alway, S. E. (2011) · The Journals of Gerontology Series A · doi:10.1093/gerona/glr047 · Cited by 145 · see citing works
Ochala, J., Gustafson, A., Llano‐Diez, M., Renaud, G., Li, M., Aare, S., Qaisar, R., Banduseela, V. C., Hedström, Y., Tang, X., et al. (2011) · The Journal of Physiology · doi:10.1113/jphysiol.2010.202044 · Cited by 139 · see citing works
Kuwahara, H., Horie, T., Ishikawa, S., Tsuda, C., Kawakami, S., Noda, Y., Kaneko, T., Tahara, S., Tachibana, T., Okabe, M., et al. (2010) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2010.02.011 · Cited by 129 · see citing works
Beyond atrophy: redox mechanisms of muscle dysfunction in chronic inflammatory disease
Reid, M. B., & Moylan, J. S. (2011) · The Journal of Physiology · doi:10.1113/jphysiol.2010.203356 · Cited by 126 · see citing works
Emerging Roles of ROS/RNS in Muscle Function and Fatigue
Westerblad, H., & Allen, D. G. (2011) · Antioxidants and Redox Signaling · doi:10.1089/ars.2011.3909 · Cited by 126 · see citing works
Ryan, M. J., Jackson, J. R., Hao, Y., Williamson, C. L., Dabkowski, E. R., Hollander, J. M., & Alway, S. E. (2010) · The Journals of Gerontology Series A · doi:10.1093/gerona/glq080 · Cited by 125 · see citing works
Merry, T. L., Steinberg, G. R., Lynch, G. S., & McConell, G. K. (2010) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00239.2009 · Cited by 122 · see citing works
Nitric oxide synthase 2 and cyclooxygenase 2 interactions in inflammation
Weinberg, J. B. (2000) · Immunologic Research · doi:10.1385/ir:22:2-3:319 · Cited by 121 · see citing works
Fischer, L. R., Igoudjil, A., Magrané, J., Li, Y., Hansen, J. M., Manfredi, G., & Glass, J. D. (2010) · Brain · doi:10.1093/brain/awq314 · Cited by 117 · see citing works
Galea, E., Launay, N., Portero-Otin, M., Ruiz, M., Pamplona, R., Aubourg, P., Ferrer, I., & Pujol, A. (2012) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2012.02.005 · Cited by 108 · see citing works
Jackson, J. R., Ryan, M. J., Hao, Y., & Alway, S. E. (2010) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00489.2010 · Cited by 105 · see citing works
Fischer, L. R., Li, Y., Asress, S. A., Jones, D. P., & Glass, J. D. (2011) · Experimental Neurology · doi:10.1016/j.expneurol.2011.09.020 · Cited by 98 · see citing works
Emerging drugs for Duchenne muscular dystrophy
Malik, V., Rodino‐Klapac, L. R., & Mendell, J. R. (2012) · Expert Opinion on Emerging Drugs · doi:10.1517/14728214.2012.691965 · Cited by 98 · see citing works
Mitogen-activated protein kinase (MAPK)
Cuschieri, J., & Maier, R. V. (2005) · Critical Care Medicine · doi:10.1097/01.ccm.0000191714.39495.a6 · Cited by 96 · see citing works
Morris, G., Anderson, G., Berk, M., & Maes, M. (2013) · Molecular Neurobiology · doi:10.1007/s12035-013-8477-8 · Cited by 96 · see citing works
Hart, J. D. E., & Dulhunty, A. F. (2000) · The Journal of Membrane Biology · doi:10.1007/s002320001022 · Cited by 95 · see citing works
Lustgarten, M. S., Jang, Y. C., Liu, Y., Qi, W., Qin, Y., Dahia, P. L. M., Shi, Y., Bhattacharya, A., Müller, F. L., Shimizu, T., et al. (2011) · Aging Cell · doi:10.1111/j.1474-9726.2011.00695.x · Cited by 92 · see citing works
Shahar, S., Norshafarina, Badrasawi, M., Noor, N., Manaf, Z. A., Yassin, M. Z., & Joseph, L. (2013) · Clinical Interventions in Aging · doi:10.2147/cia.s46826 · Cited by 85 · see citing works
Effect of xanthine oxidase-generated extracellular superoxide on skeletal muscle force generation
Gómez‐Cabrera, M. C., Close, G. L., Kayani, A., McArdle, A., Viña, J., & Jackson, M. J. (2009) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00142.2009 · Cited by 81 · see citing works
Hirschfield, W., Moody, M. R., O’Brien, W. E., Gregg, A. R., Bryan, R. M., & Reid, M. B. (2000) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.2000.278.1.r95 · Cited by 76 · see citing works
Carter, C. S., Hofer, T., Seo, A. Y., & Leeuwenburgh, C. (2007) · Applied Physiology, Nutrition, and Metabolism · doi:10.1139/h07-085 · Cited by 74 · see citing works
Mechanisms of muscle weakness in muscular dystrophy
Goldstein, J. A., & McNally, E. M. (2010) · The Journal of General Physiology · doi:10.1085/jgp.201010436 · Cited by 74 · see citing works
The role of CaMKII in regulating GLUT4 expression in skeletal muscle
Ojuka, E. O., Goyaram, V., & Smith, J. A. H. (2012) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00091.2012 · Cited by 71 · see citing works
Role of exercise-induced reactive oxygen species in the modulation of heat shock protein response
Fittipaldi, S., Dimauro, I., Mercatelli, N., & Caporossi, D. (2013) · Free Radical Research · doi:10.3109/10715762.2013.835047 · Cited by 70 · see citing works
Signalling mechanisms in skeletal muscle: role in substrate selection and muscle adaptation
Hawley, J. A., Hargreaves, M., & Zierath, J. R. (2006) · Essays in Biochemistry · doi:10.1042/bse0420001 · Cited by 69 · see citing works
Aerobic power declines with aging in rat skeletal muscles perfused at matched convective O2 delivery
Hepple, R. T., Hagen, J. L., Krause, D. J., & Jackson, C. C. (2003) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00737.2002 · Cited by 61 · see citing works
Kruska, N., Schönfeld, P., Pujol, A., & Reiser, G. (2015) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2015.01.005 · Cited by 56 · see citing works
Duncan, J. G., Ravi, R., Stull, L. B., & Murphy, A. M. (2005) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00168.2005 · Cited by 55 · see citing works
Zuo, L., Youtz, D. J., & Wold, L. E. (2011) · PLoS ONE · doi:10.1371/journal.pone.0023116 · Cited by 53 · see citing works
Hayashi, Y., Sawa, Y., Nishimura, M., Fukuyama, N., Ichikawa, H., Ohtake, S., Nakazawa, H. K., & Matsuda, H. (2004) · European Journal of Cardio-Thoracic Surgery · doi:10.1016/j.ejcts.2004.03.033 · Cited by 48 · see citing works
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Carletti, B., Passarelli, C., Sparaco, M., Tozzi, G., Pastore, A., Bertini, E., & Piemonte, F. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.05.060 · Cited by 32 · see citing works
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Babu, D., Leclercq, G., Goossens, V., Berghe, T. V., Hamme, E. V., Vandenabeele, P., & Lefebvre, R. A. (2015) · Cellular Signalling · doi:10.1016/j.cellsig.2015.02.019 · Cited by 29 · see citing works
Strzałkowski, A., & Antoszewski, Z. (2005) · PubMed · Cited by 29 · see citing works
Koga, T., Umeda, T., Kojima, A., Tanabe, M., Yamamoto, Y., Takahashi, I., Iwasaki, H., Iwane, K., Matsuzaka, M., & Nakaji, S. (2012) · Luminescence · doi:10.1002/bio.2352 · Cited by 17 · see citing works
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Shaw, P. J. (2007) · The biomedical & life sciences collection. · doi:10.69645/ocxq3852 · Cited by 6 · see citing works
Lynch, G. S. (2010) · Springer eBooks · doi:10.1007/978-90-481-9713-2_1 · Cited by 5 · see citing works
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Arcaro, A., Lepore, A., Cetrangolo, G. P., Paventi, G., Ames, P. R. J., & Gentile, F. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26167787 · Cited by 10 · see citing works
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Pozzi, G., Presta, V., Masselli, E., Condello, G., Cortellazzi, S., Arcari, M., Micheloni, C., Vitale, M., Gobbi, G., Mirandola, P., et al. (2023) · Cells · doi:10.3390/cells12131792 · Cited by 9 · see citing works
Espinosa, A., Casas, M., & Jaimovich, E. (2023) · Preprints.org · doi:10.20944/preprints202305.2112.v1 · Cited by 6 · see citing works
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Ramezani, S., Farzizadeh, R., & Seifi-Asgshahr, F. (2026) · Metabolism Open · doi:10.1016/j.metop.2026.100475 · Cited by 4 · see citing works
Chhabrani, A., Shivamallu, A. B., Bharadwaj, R. S., Kale, R., & Kathuria, A. (2024) · Acta Astronautica · doi:10.1016/j.actaastro.2024.03.014 · Cited by 4 · see citing works
Vicencio, F., Jiménez, P., Huerta, F., Cofré-Bolados, C., Zamorano, S. G., García‐Díaz, D. F., Rodrigo, R., & Poblete-Aro, C. (2019) · Sport Sciences for Health · doi:10.1007/s11332-019-00561-1 · Cited by 3 · see citing works
Niu, M., Li, J., Zhuang, X., Yangyang, C., Chen, Y., Zhang, Y., & Maes, M. H. J. (2025) · Molecular Pain · doi:10.1177/17448069251332140 · Cited by 2 · see citing works
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Toniolo, L., & Giacomello, E. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-818698-5.00032-8 · Cited by 2 · see citing works
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Moreira‐Pais, A., Amado, F. M. L., Vitorino, R. M. P., Coriolano, H.-J. A., Duarte, J. A., & Ferreira, R. M. (2020) · Springer eBooks · doi:10.1007/978-3-030-44436-5_14 · Cited by 2 · see citing works
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Cuccio, G., Franzini, M., & Valdenassi, L. (2017) · Ozone Therapy · doi:10.4081/ozone.2017.7246
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Al-Mshhdani, B. A. (2021) · UWA Profiles and Research Repository (University of Western Australia) · doi:10.26182/x6kn-cr56
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Rudd, H., & Toborek, M. J. (2024) · Elsevier eBooks · doi:10.1016/b978-0-323-99744-7.00030-4
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- Authors
- Zuo, L., & Pannell, B. K.
- Affiliations
- The Ohio State University (US)
- Corresponding author
- Zuo, Li
- ORCID
- Zuo, Li
- Venue
- Frontiers in Physiology
- Publisher
- Frontiers Media SA
- Published
- 2015-11-18
- Volume
- 6
- Pages
- 338-338
- ISSN
- 1664-042X (ISSN-L)
- PMC
- PMC4649055
- OpenAlex
- W2160351118
- Cited by
- 60
- References
- 118
- Citations by year
- 2026: 3 · 2025: 5 · 2024: 3 · 2023: 6 · 2022: 5 · 2021: 4 · 2020: 5 · 2019: 6 · 2018: 7 · 2017: 10 · 2016: 6
- FWCI
- 1.06
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- cc-by
- Locations
- Frontiers in Physiology (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- OSUCOM-HRS (013000)
- Topics
- Health Sciences › Medicine › Rehabilitation › Exercise and Physiological Responses
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Redox biology and oxidative stress
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
- Keywords
- reactive oxygen species, skeletal muscle, redox signaling, oxidative stress, mitochondria, muscle fatigue, exercise adaptation, aging, Duchenne muscular dystrophy, muscle inflammation, protein oxidation
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