Upregulation of uncoupling protein-3 in skeletal muscle during exercise: a potential antioxidant function
Abstract
Uncoupling protein-3 (UCP3) expression has been shown to increase dramatically in response to muscular contraction, but the physiological significance of UCP3 upregulation is still elusive. In this study, UCP3 mRNA and protein expression were investigated along with mitochondrial respiratory function, reactive oxygen species (ROS) generation, and antioxidant defense in rat skeletal muscle during and after an acute bout of prolonged exercise. UCP3 mRNA expression was elevated sharply at 45 min of exercise, reaching 7- to 8-fold above resting level at 150 min. The increase in UCP3 protein content showed a latent response but was elevated approximately 1.9-fold at 120 min of exercise. Both UCP3 mRNA and UCP3 protein gradually returned to resting levels 24 h postexercise. Mitochondrial ROS production was progressively increased during exercise. However, ROS showed a dramatic drop at 150 min although their levels remained severalfold higher during the recovery. Mitochondrial State 4 respiration rate was increased by 46 and 58% (p < 0.05) at 90 and 120 min, respectively, but returned to resting rate at 150 min, when State 3 respiration and respiratory control index (RCI) were suppressed. ADP-to-oxygen consumption (P/O) ratio and ATP synthase activity were lowered at 3 h postexercise, whereas proton motive force and mitochondrial malondialdehyde content were unchanged. Manganese superoxide dismutase gene expression was not affected by exercise except for an increase in mRNA abundance at 3 h postexercise. These data demonstrate that UCP3 expression in rat skeletal muscle can be rapidly upregulated during prolonged exercise, possibly owing to increased ROS generation. Increased UCP3 may partially alleviate the proton gradient across the inner membrane, thereby reducing further ROS production by the electron transport chain. However, prolonged exercise caused a decrease in energy coupling efficiency in muscle mitochondria revealed by an increased respiration rate due to proton leak (State 4/State 3 ratio) and decreased RCI. We thus propose that the compromise of the oxidative phosphorylation efficiency due to UCP3 upregulation may serve an antioxidant function to protect the muscle mitochondria from exercise-induced oxidative stress
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
UCP3 expression in cultured myotubes and rodent skeletal muscle has been linked to modulation of fatty acid oxidation, mitochondrial integrity, and management of ROS/oxidative stress.
“its expression in cultured myotubes and rodent skeletal muscle has been linked to modulation of fatty acid oxidation [56–58], mitochondrial integrity, and to management of ROS/oxidative stress [59–62].”
From Proinflammatory NFkB signalling promotes mitochondrial dysfunction in skeletal muscle in response to cellular fuel overloading (2019) · cites this paper as [60]
Cites
PROTEIN MEASUREMENT WITH THE FOLIN PHENOL REAGENT
Lowry, O. H., Rosebrough, N., Farr, A. L., & Randall, R. (1951) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)52451-6 · Cited by 315,771 · see citing works
Hydroperoxide metabolism in mammalian organs.
Chance, B., Sies, H., & Boveris, A. (1979) · Physiological Reviews · doi:10.1152/physrev.1979.59.3.527 · Cited by 5,827 · see citing works
St-Pierre, J., Drori, S., Uldry, M., Silvaggi, J. M., Rhee, J., Jäger, S., Handschin, C., Zheng, K., Lin, J., Yang, W., et al. (2006) · Cell · doi:10.1016/j.cell.2006.09.024 · Cited by 2,233 · see citing works
[7] Mitochondrial respiratory control and the polarographic measurement of ADP : O ratios
Estabrook, R. W. (1967) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/0076-6879(67)10010-4 · Cited by 1,782 · see citing works
Free radicals and tissue damage produced by exercise
Davies, K. J. A., Quintanilha, A. T., Brooks, G. A., & Packer, L. (1982) · Biochemical and Biophysical Research Communications · doi:10.1016/s0006-291x(82)80124-1 · Cited by 1,739 · see citing works
Superoxide activates mitochondrial uncoupling proteins
Echtay, K. S., Roussel, D., St-Pierre, J., Jekabsons, M. B., Cadenas, S., Stuart, J. A., Harper, J. A., Roebuck, S. J., Morrison, A., Pickering, S., et al. (2002) · Nature · doi:10.1038/415096a · Cited by 1,382 · see citing works
Boss, O., Samec, S., Paoloni‐Giacobino, A., Rossier, C., Dulloo, A. G., Seydoux, J., Muzzin, P., & Giacobino, J. (1997) · FEBS Letters · doi:10.1016/s0014-5793(97)00384-0 · Cited by 1,041 · see citing works
Adaptations of skeletal muscle to exercise: rapid increase in the transcriptional coactivator PGC-1
Baar, K., Wende, A. R., Jones, T. E., Marison, M., Nolte, L. A., Chen, M., Kelly, D. P., & Holloszy, J. O. (2002) · The FASEB Journal · doi:10.1096/fj.02-0367com · Cited by 1,020 · see citing works
An improved spectrophotometric assay for superoxide dismutase based on epinephrine autoxidation
Sun, M., & Zigman, S. (1978) · Analytical Biochemistry · doi:10.1016/0003-2697(78)90010-6 · Cited by 782 · see citing works
Akimoto, T., Pohnert, S. C., Li, P., Zhang, M., Gumbs, C., Rosenberg, P. B., Williams, R. S., & Yan, Z. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m408862200 · Cited by 714 · see citing works
Vidal‐Puig, A., Solanes, G., Grujić, D., Flier, J. S., & Lowell, B. B. (1997) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1997.6740 · Cited by 711 · see citing works
Energy metabolism in uncoupling protein 3 gene knockout mice
Vidal-Puig, A. J., Grujic, D., Zhang, C.-Y., Hagen, T., Boss, O., Ido, Y., Szczepanik, A., Wade, J., Mootha, V., Cortright, R., et al. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.m910179199 · Cited by 677 · see citing works
The mitochondrial uncoupling-protein homologues
Krauss, S., Zhang, C., & Lowell, B. B. (2005) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1592 · Cited by 663 · see citing works
Thiobarbituric acid test for monitoring lipid oxidation in meat
Fernández‐López, J., Pérez‐Álvarez, J. Á., & Fernández-López, J. A. (1997) · Food Chemistry · doi:10.1016/s0308-8146(96)00114-8 · Cited by 657 · see citing works
Maximum oxygen consumption of rats and its changes with various experimental procedures
BEDFORD, T. G., Tipton, C. M., Wilson, N. C., Oppliger, R. A., & GISOLFI, C. V. (1979) · Journal of Applied Physiology · doi:10.1152/jappl.1979.47.6.1278 · Cited by 518 · see citing works
Intrinsic and extrinsic uncoupling of oxidative phosphorylation
Kadenbach, B. (2003) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/s0005-2728(03)00027-6 · Cited by 486 · see citing works
Reactive oxygen species, mitochondria, apoptosis and aging
Papa, S., & Skulachev, V. P. (1997) · Springer eBooks · doi:10.1007/978-1-4615-6111-8_47 · Cited by 462 · see citing works
Aging and acute exercise enhance free radical generation in rat skeletal muscle
Bejma, J., & Ji, L. L. (1999) · Journal of Applied Physiology · doi:10.1152/jappl.1999.87.1.465 · Cited by 445 · see citing works
Self-citationReactive oxygen species, mitochondria, apoptosis and aging
Papa, S., & Скулачев, В. П. (1997) · Molecular and Cellular Biochemistry · doi:10.1023/a:1006873518427 · Cited by 389 · see citing works
Structure and function of the uncoupling protein from brown adipose tissue
Klingenberg, M., & Huang, S. (1999) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/s0005-2736(98)00232-6 · Cited by 359 · see citing works
Salo, D. C., Donovan, C. M., & Davies, K. J. A. (1991) · Free Radical Biology and Medicine · doi:10.1016/0891-5849(91)90119-n · Cited by 357 · see citing works
Irrcher, I., Adhihetty, P. J., Sheehan, T. E., Joseph, A.-M., & Hood, D. A. (2003) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00409.2002 · Cited by 315 · see citing works
Sensitive and rapid quantitation of oxygen reactive species formation in rat synaptosomes
LeBel, C. P., & Bondy, S. C. (1990) · Neurochemistry International · doi:10.1016/0197-0186(90)90025-o · Cited by 313 · see citing works
Role of nitric oxide in skeletal muscle: synthesis, distribution and functional importance
Reid, M. B. (1998) · Acta Physiologica Scandinavica · doi:10.1046/j.1365-201x.1998.0303f.x · Cited by 263 · see citing works
PGC-1α mRNA expression is influenced by metabolic perturbation in exercising human skeletal muscle
Norrbom, J., Sundberg, C. J., Rundqvist, H., Kraus, W. E., Jansson, E., & Gustafsson, T. P. (2004) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00765.2003 · Cited by 263 · see citing works
cDNA Cloning and mRNA Analysis of PGC-1 in Epitrochlearis Muscle in Swimming-Exercised Rats
Goto, M., Terada, S., Kato, M., Katoh, M., Yokozeki, T., Tabata, I., & Shimokawa, T. (2000) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.2000.3134 · Cited by 258 · see citing works
Hollander, J. M., Fiebig, R., Gore, M. T., Ookawara, T., Ohno, H., & Ji, L. (2001) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s004240100539 · Cited by 231 · see citing works
Self-citationGoglia, F., & Skulachev, V. P. (2003) · The FASEB Journal · doi:10.1096/fj.03-0159hyp · Cited by 229 · see citing works
Nedergaard, J., & Cannon, B. (2003) · Experimental Physiology · doi:10.1113/eph8802502 · Cited by 226 · see citing works
Generating, Partitioning, Targeting and Functioning of Superoxide in Mitochondria
Liu, S. (1997) · Bioscience Reports · doi:10.1023/a:1027328510931 · Cited by 217 · see citing works
Self-citationGomez, J. M. (2003) · Journal of Experimental Botany · doi:10.1093/jxb/erh013 · Cited by 191 · see citing works
Cytokines and oxidative signalling in skeletal muscle
Reid, M. B., & Li, Y. ‐. (2001) · Acta Physiologica Scandinavica · doi:10.1046/j.1365-201x.2001.00824.x · Cited by 187 · see citing works
BRAND, M. D., PAMPLONA, R., PORTERO-OTÍN, M., REQUENA, J. R., ROEBUCK, S. J., BUCKINGHAM, J. A., CLAPHAM, J. C., & CADENAS, S. (2002) · Biochemical Journal · doi:10.1042/bj20021077 · Cited by 184 · see citing works
Effect of duration of exercise on excess postexercise O2 consumption
Bahr, R., Ingnes, I., VAAGE, O., Sejersted, O. M., & Newsholme, E. A. (1987) · Journal of Applied Physiology · doi:10.1152/jappl.1987.62.2.485 · Cited by 181 · see citing works
Lee, I., Bender, E., & Kadenbach, B. (2002) · Molecular and Cellular Biochemistry · doi:10.1023/a:1015921513720 · Cited by 173 · see citing works
UCP-3 expression in skeletal muscle: effects of exercise, hypoxia, and AMP-activated protein kinase
Zhou, M., Lin, B.-Z., Coughlin, S., Vallega, G., & Pilch, P. F. (2000) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.2000.279.3.e622 · Cited by 166 · see citing works
Anderson, E. J., Yamazaki, H., & Neufer, P. D. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m706129200 · Cited by 151 · see citing works
Cabrero, À., Alegret, M., Sánchez, R. M., Adzet, T., Laguna, J. C., & Vázquez‐Carrera, M. (2001) · Diabetes · doi:10.2337/diabetes.50.8.1883 · Cited by 124 · see citing works
Liu, S. (1999) · Journal of Bioenergetics and Biomembranes · doi:10.1023/a:1018650103259 · Cited by 119 · see citing works
Self-citationHai, B., Jiang, N., Ma, G., Qu, J., Zhang, G., Cao, D., Wen, L., Liu, S., Ji, L. L., & Zhang, Y. (2008) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2007.12.033 · Cited by 108 · see citing works
Self-citationAging skeletal muscle mitochondria in the rat: decreased uncoupling protein-3 content
Kerner, J., Turkaly, P. J., Minkler, P. E., & Hoppel, C. L. (2001) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.2001.281.5.e1054 · Cited by 106 · see citing works
Busquets, S., Sanchı́s, D., Alvarez, B., Ricquier, D., López-Soriano, F. J., & Argilés, J. M. A. (1998) · FEBS Letters · doi:10.1016/s0014-5793(98)01485-9 · Cited by 101 · see citing works
Regulation of skeletal muscle UCP-2 and UCP-3 gene expression by exercise and denervation
Cortright, R. N., Zheng, D., Jones, J. P., Fluckey, J. D., DiCarlo, S. E., Grujić, D., Lowell, B. B., & Dohm, G. L. (1999) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1999.276.1.e217 · Cited by 88 · see citing works
Free radicals and exercise: An introduction
Packer, L., Cadenas, E., & Davies, K. J. A. (2007) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2007.05.031 · Cited by 86 · see citing works
Tumor necrosis factor-α regulates in vivo expression of the rat UCP family differentially
Masaki, T., Yoshimatsu, H., Chiba, S., Hidaka, S., Tajima, D., Kakuma, T., Kurokawa, M., & Sakata, T. (1999) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/s0005-2760(98)00173-8 · Cited by 55 · see citing works
Role of UCP3 in state 4 respiration during contractile activity-induced mitochondrial biogenesis
Ljubicic, V., Adhihetty, P. J., & Hood, D. A. (2004) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00336.2004 · Cited by 45 · see citing works
Impaired Cardiac Mitochondrial Membrane Potential and Respiration in Copper-Deficient Rats
Chen, X., Jennings, D. B., & Medeiros, D. M. (2002) · Journal of Bioenergetics and Biomembranes · doi:10.1023/a:1021258204921 · Cited by 31 · see citing works
Superoxide Dismutase Is Induced During Rat Pancreatic Acinar Cell Injury
Su, S.-B., Motoo, Y., Xie, M.-J., Mouri, H., Asayama, K., & Sawabu, N. (2002) · Pancreas · doi:10.1097/00006676-200203000-00005 · Cited by 20 · see citing works
Mitochondrial cytochrome c reacts with nitric oxide via S-nitrosation
Larson, S. K., Dwyer, D. S., Lo, H., & Ghafourifar, P. (2006) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2006.02.067 · Cited by 9 · see citing works
Flagged first, then by citations
2 of the 51 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Uncoupling proteins and the control of mitochondrial reactive oxygen species production
Mailloux, R. J., & Harper, M. (2011) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2011.06.022 · Cited by 534 · see citing works
Exercise alters SIRT1, SIRT6, NAD and NAMPT levels in skeletal muscle of aged rats
Koltai, E., Szabo, Z., Atalay, M., Boldogh, I., Naito, H., Goto, S., Nyakas, C., & Radak, Z. (2010) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2009.11.002 · Cited by 283 · see citing works
Trevellin, E., Scorzeto, M., Olivieri, M., Granzotto, M., Valerio, A., Tedesco, L., Fabris, R., Serra, R., Quarta, M., Reggiani, C., et al. (2014) · Diabetes · doi:10.2337/db13-1234 · Cited by 176 · see citing works
Exercise-induced hormesis and skeletal muscle health
Ji, L. L., Kang, C., & Zhang, Y. (2016) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2016.02.025 · Cited by 176 · see citing works
Self-citationRedox biology of exercise: an integrative and comparative consideration of some overlooked issues
Nikolaidis, M. G., Kyparos, A., Spanou, C., Paschalis, V., Theodorou, A. A., & Vrabas, I. S. (2012) · Journal of Experimental Biology · doi:10.1242/jeb.067470 · Cited by 152 · see citing works
Ding, H., Jiang, N., Liu, H., Liu, X., Liu, D., Zhao, F., Wen, L., Liu, S., Ji, L. L., & Zhang, Y. (2009) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2009.08.007 · Cited by 149 · see citing works
Self-citationThe regulation and turnover of mitochondrial uncoupling proteins
Azzu, V., Jastroch, M., Divakaruni, A. S., & Brand, M. D. (2010) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2010.02.035 · Cited by 146 · see citing works
Ferreira‐Pêgo, C., Guelinckx, I., Moreno, L. A., Kavouras, S. A., Gandy, J., Martı́nez, H., Bardosono, S., Abdollahi, M., Nasseri, E., Jarosz, A., et al. (2015) · European Journal of Nutrition · doi:10.1007/s00394-015-0943-9 · Cited by 144 · see citing works
Nisr, R. B., Shah, D. S., Ganley, I. G., & Hundal, H. S. (2019) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-019-03148-8 · Cited by 142 · see citing works
Exercise with low glycogen increases PGC-1α gene expression in human skeletal muscle
Psilander, N., Frank, P., Flockhart, M., & Sahlin, K. (2013) · European Journal of Applied Physiology · doi:10.1007/s00421-012-2504-8 · Cited by 101 · see citing works
Shabalina, I. G., Joris Hoeks, J., Kramarova, T. V., Schrauwen, P., Cannon, B., & Nedergaard, J. (2010) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2010.02.033 · Cited by 101 · 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
Liao, P., Zhou, J.-P., Ji, L. L., & Zhang, Y. (2010) · American Journal of Physiology. Regulatory Integrative and Comparative Physiology · doi:10.1152/ajpregu.00480.2009 · Cited by 103 · see citing works
Self-citationAnedda, A., López-Bernardo, E., Acosta‐Iborra, B., Suleiman, M. S., Landázuri, M. O., & Cadenas, S. (2013) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2013.04.007 · Cited by 92 · see citing works
Mutation in dystrophin-encoding gene affects energy metabolism in mouse myoblasts
Onopiuk, M., Brutkowski, W., Wierzbicka, K., Wojciechowska, S., Szczepanowska, J., Fronk, J., Lochmüller, H., Górecki, D. C., & Zabłocki, K. (2009) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2009.06.053 · Cited by 85 · see citing works
Cannon, D. T., Bimson, W. E., Hampson, S. A., Bowen, T. S., Murgatroyd, S. R., Marwood, S., Kemp, G. J., & Rossiter, H. B. (2014) · The Journal of Physiology · doi:10.1113/jphysiol.2014.279174 · Cited by 82 · see citing works
Oxidative Stress, Mitochondrial Function and Adaptation to Exercise: New Perspectives in Nutrition
Vargas-Mendoza, N., Ángeles-Valencia, M., Morales‐González, Á., Madrigal‐Santillán, E., Morales-Martínez, M., Madrigal‐Bujaidar, E., Álvarez‐González, I., Gutiérrez‐Salinas, J., Esquivel-Chirino, C., Chamorro, G., et al. (2021) · Life · doi:10.3390/life11111269 · Cited by 83 · see citing works
Xu, R., Andrés‐Mateos, E., Mejı́as, R., MacDonald, E. M., Leinwand, L. A., Merriman, D. K., Fink, R., & Cohn, R. D. (2013) · Experimental Neurology · doi:10.1016/j.expneurol.2013.01.005 · Cited by 67 · see citing works
Nox4 mediates skeletal muscle metabolic responses to exercise
Specht, K. S., Kant, S., Addington, A. K., McMillan, R. P., Hulver, M. W., Learnard, H., Campbell, M., Donnelly, S. R., Caliz, A. D., Pei, Y., et al. (2021) · Molecular Metabolism · doi:10.1016/j.molmet.2020.101160 · Cited by 64 · see citing works
4-Hydroxynonenal induces Nrf2-mediated UCP3 upregulation in mouse cardiomyocytes
López-Bernardo, E., Anedda, A., Sánchez-Pérez, P., Acosta‐Iborra, B., & Cadenas, S. (2015) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2015.03.032 · Cited by 57 · see citing works
Capó, X., Martorell, M., Sureda, A., Llompart, I., Tur, J. A., & Pons, A. (2014) · European Journal of Nutrition · doi:10.1007/s00394-014-0683-2 · Cited by 56 · see citing works
Clark, I. E., Vanhatalo, A., Thompson, C., Wylie, L. J., Bailey, S. J., Kirby, B. S., Wilkins, B. W., & JONES, A. M. (2019) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00031.2019 · Cited by 52 · see citing works
Li, J., Zhang, S., Li, C., Zhang, X., Shan, Y., Zhang, Z., Hai, B., & Zhang, Y. (2024) · Scientific Reports · doi:10.1038/s41598-024-72088-6 · Cited by 57 · see citing works
Self-citationThe role of mitochondria in redox signaling of muscle homeostasis
Ji, L. L., Yeo, D., Kang, C., & Zhang, T. (2020) · Journal of sport and health science/Journal of Sport and Health Science · doi:10.1016/j.jshs.2020.01.001 · Cited by 51 · see citing works
Self-citationMonteiro, B. S., Freire‐Brito, L., Carrageta, D. F., Oliveira, P. F., & Alves, M. G. (2021) · Antioxidants · doi:10.3390/antiox10111746 · Cited by 47 · see citing works
Busquets-Cortés, C., Capó, X., Martorell, M., Tur, J. A., Sureda, A., & Pons, A. (2016) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2016/8950384 · Cited by 45 · see citing works
How the mitochondrion was shaped by radical differences in substrates
Speijer, D. (2014) · BioEssays · doi:10.1002/bies.201400033 · Cited by 44 · see citing works
Being right on Q: shaping eukaryotic evolution
Speijer, D. (2016) · Biochemical Journal · doi:10.1042/bcj20160647 · Cited by 41 · see citing works
Saborido, A., Naudí, A., Portero‐Otín, M., Pamplona, R., & Megı́as, A. (2010) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00790.2010 · Cited by 42 · see citing works
Eivers, S. S., McGivney, B. A., Gu, J., MacHugh, D. E., Katz, L. M., & Hill, E. W. (2011) · Animal Genetics · doi:10.1111/j.1365-2052.2011.02238.x · Cited by 41 · see citing works
Carfagna, S., Napolitano, G., Barone, D., Pinto, G., Pollio, A., & Venditti, P. (2015) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2015/732090 · Cited by 40 · see citing works
Uncoupling Proteins: Molecular, Functional, Regulatory, Physiological and Pathological Aspects
Sluse, F. E. (2011) · Advances in experimental medicine and biology · doi:10.1007/978-94-007-2869-1_6 · Cited by 40 · see citing works
Antioxidant and anti-inflammatory effects of exercise: role of redox signaling
Ji, L. L., & Zhang, Y. (2013) · Free Radical Research · doi:10.3109/10715762.2013.844341 · Cited by 39 · see citing works
Self-citationNabben, M., Shabalina, I. G., Moonen‐Kornips, E., van Beurden, D., Cannon, B., Schrauwen, P., Nedergaard, J., & Joris Hoeks, J. (2011) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2011.04.003 · Cited by 39 · see citing works
Mailloux, R. J., Dumouchel, T., Aguer, C., deKemp, R., Beanlands, R. S., & Harper, M. (2011) · Biochemical Journal · doi:10.1042/bj20110571 · Cited by 38 · see citing works
Busquets-Cortés, C., Capó, X., Martorell, M., Tur, J. A., Sureda, A., & Pons, A. (2017) · European Journal of Applied Physiology · doi:10.1007/s00421-017-3684-z · Cited by 37 · see citing works
Espinosa, A., Casas, M., & Jaimovich, E. (2023) · Antioxidants · doi:10.3390/antiox12081624 · Cited by 31 · see citing works
Bermejo-Nogales, A., Calduch-Giner, J. À., & Pérez‐Sánchez, J. (2010) · Journal of Comparative Physiology B · doi:10.1007/s00360-009-0441-6 · Cited by 31 · see citing works
Voltarelli, V. A., Coronado, M. J., Fernandes, L. G., Campos, J. C., Jannig, P. R., Ferreira, J. C. B., Fajardo, G., Brum, P. C., & Bernstein, D. (2021) · Cells · doi:10.3390/cells10010146 · Cited by 31 · see citing works
Exercise influences circadian gene expression in equine skeletal muscle
Murphy, B. A., Wagner, A. L., McGlynn, O. F., Kharazyan, F., Browne, J. A., & Elliott, J. A. (2014) · The Veterinary Journal · doi:10.1016/j.tvjl.2014.03.028 · Cited by 30 · see citing works
Liu, D., Huang, L., Wang, Y., Wang, W., Wehrens, X. H. T., Belousova, T., Abdelrahim, M., DiMattia, G. E., & Sheikh‐Hamad, D. (2012) · PLoS ONE · doi:10.1371/journal.pone.0036994 · Cited by 30 · see citing works
Mitochondrial redox metabolism in aging: Effect of exercise interventions
Hai, B., Jiang, N., Ji, L. L., & Zhang, Y. (2013) · Journal of sport and health science/Journal of Sport and Health Science · doi:10.1016/j.jshs.2013.03.006 · Cited by 28 · see citing works
Self-citationMolecular Mechanisms of Diaphragm Myopathy in Humans With Severe Heart Failure
Mangner, N., Garbade, J., Heyne, E., van den Berg, M., Winzer, E. B., Hommel, J., Sandri, M., Jozwiak‐Nozdrzykowska, J., Meyer, A. L., Lehmann, S., et al. (2021) · Circulation Research · doi:10.1161/circresaha.120.318060 · Cited by 28 · see citing works
Gutgesell, A., Ringseis, R., Schmidt, E., Brandsch, C., Stangl, G. I., & Eder, K. (2009) · Journal of Molecular Endocrinology · doi:10.1677/jme-09-0064 · Cited by 27 · see citing works
Krueger, K., Koch, K., Jühling, A., Tepel, M., & Scholze, A. (2009) · Clinical Biochemistry · doi:10.1016/j.clinbiochem.2009.08.005 · Cited by 27 · see citing works
Braun, N., Klumpp, D., Hennenlotter, J., Bedke, J., Duranton, C., Bleif, M., & Huber, S. M. (2015) · Scientific Reports · doi:10.1038/srep13450 · Cited by 26 · see citing works
Liu, W., Wang, Z., Xia, Y., Kuang, H., Liu, S., Li, L., Tang, C., & Yin, D. (2019) · Experimental Gerontology · doi:10.1016/j.exger.2019.110647 · Cited by 26 · see citing works
Self-citationImpact of methylmercury exposure on mitochondrial energetics in AC16 and H9C2 cardiomyocytes
Truong, J., Mailloux, R. J., & Chan, H. M. (2015) · Toxicology in Vitro · doi:10.1016/j.tiv.2015.03.016 · Cited by 23 · see citing works
Bermejo-Nogales, A., Benedito‐Palos, L., Calduch-Giner, J. À., & Pérez‐Sánchez, J. (2011) · Comparative Biochemistry and Physiology Part A Molecular & Integrative Physiology · doi:10.1016/j.cbpa.2011.03.024 · Cited by 23 · see citing works
Jordan, A., Perry, C. G. R., & Cheng, A. J. (2021) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2021.09.014 · Cited by 22 · see citing works
Ferrer, M. D., Sureda, A., Tauler, P., Palacín, C., Tur, J. A., & Pons, A. (2010) · British Journal of Haematology · doi:10.1111/j.1365-2141.2010.08149.x · Cited by 20 · see citing works
Kazerouni, E. G., Franklin, C. E., & Seebacher, F. (2015) · Journal of Experimental Biology · doi:10.1242/jeb.131615 · Cited by 20 · see citing works
Chen, J., Wong, H. S., Leung, H. Y., Leong, P. K., Chan, W. M., & Ko, K. M. (2014) · Journal of Functional Foods · doi:10.1016/j.jff.2014.04.021 · Cited by 19 · see citing works
Adenylate kinase derived ATP shapes respiration and calcium storage of isolated mitochondria
Deline, M. L., Grashei, M., van Heijster, F. H. A., Schilling, F., Straub, J., & Fromme, T. (2021) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2021.148409 · Cited by 17 · see citing works
Ma, G., Liu, Y., Zhang, Q., Zhang, B.-G., Zhao, N. O., Wang, Q.-L., & Wang, X. (2014) · Hepatology International · doi:10.1007/s12072-014-9529-5 · Cited by 15 · see citing works
Self-citationShi, X., Wang, J., & Qin, Y. (2014) · Journal of Cardiovascular Pharmacology · doi:10.1097/fjc.0000000000000146 · Cited by 15 · see citing works
Human mitochondrial uncoupling protein 3 functions as a metabolite transporter
Leonardis, F. D., Ahmed, A., Vozza, A., Capobianco, L., Riley, C. L., Barile, S. N., Molfetta, D. D., Tiziani, S., DiGiovanni, J., Palmieri, L., et al. (2023) · FEBS Letters · doi:10.1002/1873-3468.14784 · Cited by 14 · see citing works
Increased vulnerability with aging to MPTP: the mechanisms underlying mitochondrial dynamics
Jiang, N., Hai, B., Song, C., Guo, J., Zhao, F., Feng, H., Ding, H., Ji, L., & Zhang, Y. (2013) · Neurological Research · doi:10.1179/1743132813y.0000000296 · Cited by 14 · see citing works
Self-citationO’Leary, A. J., & O’Halloran, K. D. (2015) · Respiratory Physiology & Neurobiology · doi:10.1016/j.resp.2015.10.018 · Cited by 14 · see citing works
Martins, E. L., Ricardo, J. C., de‐Souza‐Ferreira, E., Camacho-Pereira, J., Filho, D. M. R., & Galina, A. (2017) · Comparative Biochemistry and Physiology Part B Biochemistry and Molecular Biology · doi:10.1016/j.cbpb.2017.11.013 · Cited by 13 · see citing works
Moderate‐Intensity Exercise Maintains Redox Homeostasis for Cardiovascular Health
Jiang, J., Ni, L., Zhang, X., Gokulnath, P., Vulugundam, G., Li, G., Wang, H., & Xiao, J. (2023) · Advanced Biology · doi:10.1002/adbi.202200204 · Cited by 13 · see citing works
Wu, D., & Liu, J. (2019) · Archives of Oral Biology · doi:10.1016/j.archoralbio.2019.04.022 · Cited by 12 · see citing works
Majerczak, J., Rychlik, B., Grzelak, A., Grzmil, P., Karasiński, J., Pierzchalski, P., Pułaski, Ł., Bartosz, G., & Zoladz, J. A. (2010) · PubMed · Cited by 12 · see citing works
Wang, X., Liu, J., Chen, S., Yin, Y., Liu, Y., & Zhang, C. (2020) · Communications Biology · doi:10.1038/s42003-020-0919-z · Cited by 12 · see citing works
One Health: Circadian Medicine Benefits Both Non-human Animals and Humans Alike
Farag, H. I., Murphy, B. A., Templeman, J. R., Hanlon, C., Joshua, J., Koch, T. G., Niel, L., Shoveller, A. K. K., Bédécarrats, G. Y., Ellison, A., et al. (2024) · Journal of Biological Rhythms · doi:10.1177/07487304241228021 · Cited by 10 · see citing works
Fallahi, A. A., Shekarfroush, S., Rahimi, M., Jalali, A., & Khoshbaten, A. (2016) · PubMed Central · Cited by 11 · see citing works
Wong, H. S., Chen, J., Leong, P. K., Leung, H. Y., Chan, W. M., & Ko, K. M. (2015) · Evidence-based Complementary and Alternative Medicine · doi:10.1155/2015/142059 · Cited by 11 · see citing works
Wong, H. S., Chen, J., Leong, P. K., Leung, H. Y., Chan, W. M., & Ko, K. M. (2014) · Journal of Functional Foods · doi:10.1016/j.jff.2014.06.019 · Cited by 10 · see citing works
Makri, V., Giantsis, I. Α., Feidantsis, K. G., Georgoulis, I., Gougousi, A., & Michaelidis, B. (2025) · Fish Physiology and Biochemistry · doi:10.1007/s10695-025-01513-y · Cited by 8 · see citing works
Hrometz, S. L., Ebert, J. A., Grice, K. E., Nowinski, S. M., Mills, E., Myers, B. J., & Sprague, J. E. (2016) · Temperature · doi:10.1080/23328940.2016.1166310 · Cited by 6 · see citing works
Espinosa, A., Casas, M., & Jaimovich, E. (2023) · Preprints.org · doi:10.20944/preprints202305.2112.v1 · Cited by 6 · see citing works
Age-Dependent Skeletal Muscle Mitochondrial Response to Short-Term Increased Dietary Fructose
Gatto, C., Porzio, A. D., Crescenzo, R., Barrella, V., Iossa, S., & Mazzoli, A. (2023) · Antioxidants · doi:10.3390/antiox12020299 · Cited by 5 · see citing works
Leong, P. K., Leung, H. Y., Wong, H. S., Chen, J., Ma, C. W., Yang, Y., & Ko, K. M. (2013) · Chinese Medicine · doi:10.4236/cm.2013.43010 · Cited by 4 · see citing works
Antioxidant effects of LEDT in dystrophic muscle cells: involvement of PGC-1α and UCP-3 pathways
da Rocha, G. L., Guimarães, D. S. P. S. F., da Cruz, M. V., Mizobuti, D. S., da Silva, H. N. M., Pereira, E. C. L., Silveira, L. R., & Minatel, E. (2023) · Photochemical & Photobiological Sciences · doi:10.1007/s43630-023-00506-1 · Cited by 4 · see citing works
Chorna, S. V., Talanov, S. O., Strutynska, N. A., Vavilova, G. L., Kotsuruba, A. V., Gaidai, N. M., & Sagach, V. F. (2010) · Fìzìologìčnij žurnal · doi:10.15407/fz56.01.013 · Cited by 4 · see citing works
Ceusters, J. D., Mouithys-Mickalad, A. A., Franck, T. J., Deby-Dupont, G. P., Derochette, S., & Serteyn, D. A. (2013) · Research in Veterinary Science · doi:10.1016/j.rvsc.2013.09.004 · Cited by 4 · see citing works
Hilse, K. E., Rupprecht, A., Ford, K., Andrukhova, O., Erben, R. G., & Pohl, E. E. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.07.01.181768 · Cited by 2 · see citing works
Liu, D., Huang, L., Wang, Y., Wang, W., Wehrens, X. H. T., Belousova, T., Abdelrahim, M., DiMattia, G. E., & Sheikh‐Hamad, D. (2012) · PLoS ONE · doi:10.1371/annotation/52d155b7-66af-425f-9a6a-2d853d5fd95d · Cited by 1 · see citing works
Metabolic and Antioxidant Adaptation to Exercise: Role of Redox Signaling
Ji, L. L. (2015) · Healthy ageing and longevity · doi:10.1007/978-3-319-14830-4_6
Self-citationGenomics of the Circadian Clock
Murphy, B. A. (2013) · Wiley eBooks · doi:10.1002/9781118522158.ch18
Insulin Resistance and Progression of Heart Failure in the Older Adult
Sinha, S. S., & Shannon, R. P. (2011) · Aging Health · doi:10.2217/ahe.10.92
The influence of exercise on entrainment of skeletal muscle transcription in the horse
McGlynn, O. F., Browne, J. A., Blake, C., & Murphy, B. A. (2011) · Journal of Equine Veterinary Science · doi:10.1016/j.jevs.2011.03.047
The Metabolic Effects of Low Grade Inflammation on Postprandial Metabolism Following a High Fat Meal
Pittman, J. T. (2013) · VTechWorks (Virginia Tech)
Voltarelli, V. A. (2017) · Digital Library of Theses and Dissertations (Universidade de São Paulo) · doi:10.11606/t.39.2017.tde-12012017-104741
Acute hypoxia-induced diaphragm dysfunction is prevented by antioxidant pre-treatment
O’Leary, A. J. (2016) · Arrow@dit (Dublin Institute of Technology)
Goshovska, Y. V., Strutynska, N. A., & Sagach, V. F. (2020) · Fìzìologìčnij žurnal · doi:10.15407/fz66.06.003
Oxidative stress in athletes: From the scientific basis to practical aspects
Martinović, J., & Dopsaj, V. (2014) · FarFar (University of Belgrade, Faculty of Chemistry (Belgrade, Serbia))
Role of Antioxidant Signaling in Mitochondrial Adaptation to Muscle Contraction
Ji, L. L. (2014) · Springer eBooks · doi:10.1007/978-3-642-30018-9_195
Self-citationExplore the role of irisin in mitohormesis by PGC-1α
HAIBO, X., Ahmad, A., Phuoc, J. C., & BAOGUI, W. (2022) · Gazzetta Medica Italiana Archivio per le Scienze Mediche · doi:10.23736/s0393-3660.22.04790-8
Bartlett, M. F. (2019) · Carolina Digital Repository (University of North Carolina at Chapel Hill) · doi:10.17615/gma3-kv20
Wang, Y., Qin, M., Liu, X., & Ma, J. (2026) · Frontiers in Physiology · doi:10.3389/fphys.2026.1957316
- Authors
- Jiang, N., Zhang, G., Bo, H., Qu, J., Ma, G., Cao, D., Wen, L., Liu, S., Ji, L. L., & Zhang, Y.
- Affiliations
- Tianjin University of Sport (CN)
- Chinese Academy of Sciences (CN)
- University of Wisconsin–Madison (US)
- Corresponding author
- Ji, Li Li
- Zhang, Yong
- Venue
- Free Radical Biology and Medicine
- Publisher
- Elsevier BV
- Published
- 2009-01
- Volume
- 46
- Issue
- 2
- Pages
- 138-145
- ISSN
- 0891-5849 (ISSN-L)
- OpenAlex
- W2022049302
- Cited by
- 93
- References
- 51
- Citations by year
- 2026: 1 · 2025: 1 · 2024: 2 · 2023: 6 · 2022: 1 · 2021: 7 · 2020: 5 · 2019: 5 · 2017: 3 · 2016: 6 · 2015: 9 · 2014: 11 · 2013: 10 · 2012: 5
- FWCI
- 7.48
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Free Radical Biology and Medicine (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Natural Science Foundation of China
- Topics
- Health Sciences › Medicine › Rehabilitation › Exercise and Physiological Responses
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
- Health Sciences › Medicine › Complementary and alternative medicine › Cardiovascular and exercise physiology
- Keywords
- UCP3, skeletal muscle, prolonged exercise, reactive oxygen species, mitochondrial respiration, oxidative stress, antioxidant defense, manganese superoxide dismutase, proton leak, respiratory control index, oxidative phosphorylation efficiency, ATP synthase, post-exercise recovery
- MeSH terms
- Uncoupling Protein 3, Animals, Antioxidants, Enzyme Induction, Ion Channels, Male, Mitochondria, Oxidative Phosphorylation, Oxygen Consumption, Physical Conditioning, Animal, Superoxide Dismutase, Up-Regulation, Rats, Sprague-Dawley, Oxidative Stress, Muscle, Skeletal, Cell Respiration, Mitochondrial Proteins, Feedback, Physiological, Electron Transport Chain Complex Proteins, Rats
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review