{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,4]],"date-time":"2026-07-04T02:49:14Z","timestamp":1783133354736,"version":"3.54.6"},"reference-count":55,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2025,10,16]],"date-time":"2025-10-16T00:00:00Z","timestamp":1760572800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Mol. Biosci."],"abstract":"<jats:sec><jats:title>Background<\/jats:title><jats:p>In recent years, increasing attention has focused on the effect of exercise on redox balance and the expression of nuclear factor erythroid 2-related factor 2 (NRF2), widely recognized as the master regulator of antioxidant defense mechanisms. However, surprisingly little is known about how physical training influences H<jats:sub>2<\/jats:sub>O<jats:sub>2<\/jats:sub> production and NRF2 expression across various vital organs.<\/jats:p><\/jats:sec><jats:sec><jats:title>Methods<\/jats:title><jats:p>We investigated the effects of endurance training on the oxidative capacity, reactive oxygen species production, and antioxidant defense of various body organs in rats. Sixteen 4-month-old male Wistar rats were randomly assigned to either an endurance training group (8 weeks of treadmill running, <jats:italic>n<\/jats:italic> = 8) or a sedentary control group (<jats:italic>n<\/jats:italic> = 8).<\/jats:p><\/jats:sec><jats:sec><jats:title>Results<\/jats:title><jats:p>In the endurance training group, maximal oxidative activity increased in all examined tissues (lung, brain, liver, and hind limb skeletal muscle) except the heart. Under phosphorylating conditions, H<jats:sub>2<\/jats:sub>O<jats:sub>2<\/jats:sub> production remained unchanged in all tissues except the heart, where it increased. Under non-phosphorylating conditions, H<jats:sub>2<\/jats:sub>O<jats:sub>2<\/jats:sub> production increased only in the liver and heart. In all tissues, H<jats:sub>2<\/jats:sub>O<jats:sub>2<\/jats:sub> production was consistently lower under phosphorylating than non-phosphorylating conditions. The level of malondialdehyde, a marker of oxidative damage, did not increase in the examined tissues, except the lungs, where it even decreased. Superoxide dismutase 1 levels increased in the lung, brain, and skeletal muscle, but decreased in the heart and remained unchanged in the liver. NRF2 protein levels were significantly elevated in all examined tissues, accompanied by an increase in glutathione reductase levels.<\/jats:p><\/jats:sec><jats:sec><jats:title>Conclusion<\/jats:title><jats:p>Given the cytoprotective capacity of NRF2, we postulate that the NRF2-regulated adaptive multi-organ response may play a key role in the widely described beneficial effects of physical activity on various body organs and body health.<\/jats:p><\/jats:sec>","DOI":"10.3389\/fmolb.2025.1653162","type":"journal-article","created":{"date-parts":[[2025,10,16]],"date-time":"2025-10-16T04:16:45Z","timestamp":1760588205000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":5,"title":["Impact of endurance training on mitochondrial H2O2 production and NRF2 levels in different rat organs"],"prefix":"10.3389","volume":"12","author":[{"given":"Lukasz","family":"Galganski","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Krzysztof","family":"Wojcicki","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wieslawa","family":"Jarmuszkiewicz","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jerzy A.","family":"Zoladz","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2025,10,16]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"707","DOI":"10.1042\/bj1340707","article-title":"The mitochondrial generation of hydrogen peroxide. General properties and effect of hyperbaric oxygen","volume":"134","author":"Boveris","year":"1973","journal-title":"Biochem. J."},{"key":"B2","doi-asserted-by":"publisher","first-page":"755","DOI":"10.1016\/j.freeradbiomed.2004.05.034","article-title":"Mitochondrial superoxide: production, biological effects, and activation of uncoupling proteins","volume":"37","author":"Brand","year":"2004","journal-title":"Free Radic. Biol. Med."},{"key":"B3","doi-asserted-by":"publisher","first-page":"460","DOI":"10.3389\/fphys.2017.00460","article-title":"Mitochondrial VDAC1: a key gatekeeper as potential therapeutic target","volume":"8","author":"Camara","year":"2017","journal-title":"Front. Physiol."},{"key":"B4","doi-asserted-by":"publisher","first-page":"1279","DOI":"10.1111\/bph.13828","article-title":"Reactive oxygen species: key regulators in vascular health and diseases","volume":"175","author":"Chen","year":"2018","journal-title":"Br. J. Pharmacol."},{"key":"B5","doi-asserted-by":"publisher","first-page":"273","DOI":"10.1038\/s41574-022-00641-2","article-title":"Exerkines in health, resilience and disease","volume":"18","author":"Chow","year":"2022","journal-title":"Nat. Rev. Endocrinol."},{"key":"B6","doi-asserted-by":"publisher","first-page":"1198","DOI":"10.1016\/S0006-291X(82)80124-1","article-title":"Free radicals and tissue damage produced by exercise","volume":"107","author":"Davies","year":"1982","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"B7","doi-asserted-by":"publisher","first-page":"896","DOI":"10.3390\/ijms23020896","article-title":"Effects of endurance training on the coenzyme Q redox state in rat heart, liver, and brain at the tissue and mitochondrial levels: implications for reactive oxygen species formation and respiratory chain remodeling","volume":"23","author":"Dominiak","year":"2022","journal-title":"Int. J. Mol. Sci."},{"key":"B8","first-page":"467","volume-title":"Exercise and the coronary circulation","author":"Dunker","year":"2019"},{"key":"B9","doi-asserted-by":"publisher","first-page":"136","DOI":"10.1016\/j.freeradbiomed.2022.07.013","article-title":"Nrf2 as a regulator of mitochondrial function: energy metabolism and beyond","volume":"189","author":"Esteras","year":"2022","journal-title":"Free Radic. Biol. Med."},{"key":"B10","doi-asserted-by":"publisher","first-page":"213","DOI":"10.1249\/JES.0000000000000257","article-title":"Skeletal muscle Nrf2 contributes to exercise-evoked systemic antioxidant defense via extracellular vesicular communication","volume":"49","author":"Gao","year":"2021","journal-title":"Exerc. Sport Sci. Rev."},{"key":"B11","doi-asserted-by":"publisher","first-page":"51","DOI":"10.1016\/j.mad.2016.06.009","article-title":"8-Oxoguanine DNA glycosylase1-driven DNA repair-A paradoxical role in lung aging","volume":"161","author":"German","year":"2017","journal-title":"Mech. Ageing Dev."},{"key":"B12","doi-asserted-by":"publisher","first-page":"142","DOI":"10.1093\/ajcn\/87.1.142","article-title":"Oral administration of vitamin C decreases muscle mitochondrial biogenesis and hampers training-induced adaptations in endurance performance","volume":"87","author":"Gomez-Cabrera","year":"2008","journal-title":"Am. J. Clin. Nutr."},{"key":"B13","doi-asserted-by":"publisher","first-page":"209","DOI":"10.1074\/jbc.M114.619072","article-title":"Sites of superoxide and hydrogen peroxide production by muscle mitochondria assessed ex vivo under conditions mimicking rest and exercise","volume":"290","author":"Goncalves","year":"2015","journal-title":"J. Biol. Chem."},{"key":"B14","doi-asserted-by":"publisher","first-page":"68","DOI":"10.2203\/dose-response.09-044.Goto","article-title":"Hormetic effects of reactive oxygen species by exercise: a view from animal studies for successful aging in human","volume":"8","author":"Goto","year":"2009","journal-title":"Dose. Response"},{"key":"B15","doi-asserted-by":"publisher","first-page":"435","DOI":"10.3389\/fgene.2019.00435","article-title":"Regulation of mitochondrial biogenesis as a way for active longevity: interaction between the Nrf2 and PGC-1\u03b1 signaling pathways","volume":"10","author":"Gureev","year":"2019","journal-title":"Front. Genet."},{"key":"B16","doi-asserted-by":"publisher","first-page":"800","DOI":"10.1016\/s0891-5849(02)01431-4","article-title":"Exercise, antioxidants, and HSP72: protection against myocardial ischemia\/reperfusion","volume":"34","author":"Hamilton","year":"2003","journal-title":"Free Radic. Biol. Med."},{"key":"B17","doi-asserted-by":"publisher","first-page":"817","DOI":"10.1038\/s42255-020-0251-4","article-title":"Skeletal muscle energy metabolism during exercise","volume":"2","author":"Hargreaves","year":"2020","journal-title":"Nat. Metab."},{"key":"B18","doi-asserted-by":"publisher","first-page":"4777","DOI":"10.3390\/ijms21134777","article-title":"NRF2, a transcription factor for stress response and beyond","volume":"21","author":"He","year":"2020","journal-title":"Int. J. Mol. Sci."},{"key":"B19","doi-asserted-by":"publisher","first-page":"4623","DOI":"10.1038\/s41467-019-12523-9","article-title":"Cytosolic ROS production by NADPH oxidase 2 regulates muscle glucose uptake during exercise","volume":"10","author":"Henr\u00edquez-Olguin","year":"2019","journal-title":"Nat. Commun."},{"key":"B20","doi-asserted-by":"publisher","first-page":"2278","DOI":"10.1016\/s0021-9258(18)96046-1","article-title":"Biochemical adaptations in muscle","volume":"242","author":"Holloszy","year":"1967","journal-title":"J. Biol. Chem."},{"key":"B21","doi-asserted-by":"publisher","first-page":"12","DOI":"10.1016\/j.freeradbiomed.2015.02.012","article-title":"Temperature controls oxidative phosphorylation and reactive oxygen species production through uncoupling in rat skeletal muscle mitochondria","volume":"83","author":"Jarmuszkiewicz","year":"2015","journal-title":"Free Radic. Biol. Med."},{"key":"B22","doi-asserted-by":"publisher","first-page":"163","DOI":"10.1016\/j.freeradbiomed.2020.10.011","article-title":"Lung mitochondria adaptation to endurance training in rats","volume":"161","author":"Jarmuszkiewicz","year":"2020","journal-title":"Free Radic. Biol. Med."},{"key":"B23","doi-asserted-by":"publisher","first-page":"842","DOI":"10.1016\/j.freeradbiomed.2009.01.002","article-title":"Mechanical ventilation induces diaphragmatic mitochondrial dysfunction and increased oxidant production","volume":"46","author":"Kavazis","year":"2009","journal-title":"Free Radic. Biol. Med."},{"key":"B24","doi-asserted-by":"publisher","DOI":"10.1038\/s44161-025-00712-3","article-title":"Cardiac adaptation to endurance exercise training requires suppression of GDF15 via PGC-1\u03b1","author":"Khetarpal","year":"2025","journal-title":"Nat. Cardiovasc. Res."},{"key":"B25","doi-asserted-by":"publisher","first-page":"15","DOI":"10.1016\/s0014-5793(97)01159-9","article-title":"High protonic potential actuates a mechanism of production of reactive oxygen species in mitochondria","volume":"416","author":"Korshunov","year":"1997","journal-title":"FEBS Lett."},{"key":"B26","doi-asserted-by":"publisher","first-page":"333","DOI":"10.1016\/j.freeradbiomed.2009.05.004","article-title":"Mitochondria and reactive oxygen species","volume":"47","author":"Kowaltowski","year":"2009","journal-title":"Free Radic. Biol. Med."},{"key":"B27","doi-asserted-by":"publisher","first-page":"823","DOI":"10.3390\/biology12060823","article-title":"35 years of TFAM research: old protein, new puzzles","volume":"12","author":"Kozhukhar","year":"2023","journal-title":"Biol. (Basel)."},{"key":"B28","doi-asserted-by":"publisher","first-page":"3349","DOI":"10.1113\/jphysiol.2012.230185","article-title":"Biomarkers of mitochondrial content in skeletal muscle of healthy young human subjects","volume":"590","author":"Larsen","year":"2012","journal-title":"J. Physiol."},{"key":"B29","doi-asserted-by":"publisher","first-page":"199","DOI":"10.1038\/s43587-022-00191-2","article-title":"Pleiotropic effects of mitochondria in aging","volume":"2","author":"Lima","year":"2022","journal-title":"Nat. aging"},{"key":"B30","doi-asserted-by":"publisher","first-page":"261","DOI":"10.1016\/0014-5793(71)80459-3","article-title":"Respiratory chain linked H2O2 production in pigeon heart mitochondria","volume":"18","author":"Loschen","year":"1971","journal-title":"FEBS Lett."},{"key":"B31","doi-asserted-by":"publisher","first-page":"7","DOI":"10.1186\/s13024-017-0150-7","article-title":"NADPH oxidase in brain injury and neurodegenerative disorders","volume":"12","author":"Ma","year":"2017","journal-title":"Mol. Neurodegener."},{"key":"B32","doi-asserted-by":"publisher","first-page":"2686","DOI":"10.3390\/ijms23052686","article-title":"Nitrite concentration in the striated muscles is reversely related to myoglobin and mitochondrial proteins content in rats","volume":"23","author":"Majerczak","year":"2022","journal-title":"Int. J. Mol. Sci."},{"key":"B33","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1007\/978-1-4613-4609-8_8","article-title":"Effects of long-term exercise on human muscle mitochondria","volume-title":"Muscle metab. Dur. Exerc","author":"Morgan","year":"1971"},{"key":"B34","doi-asserted-by":"publisher","first-page":"349","DOI":"10.1038\/nri3423","article-title":"Beyond oxidative stress: an immunologist\u2019s guide to reactive oxygen species","volume":"13","author":"Nathan","year":"2013","journal-title":"Nat. Rev. Immunol."},{"key":"B35","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1111\/sms.12581","article-title":"Exercise as medicine - evidence for prescribing exercise as therapy in 26 different chronic diseases","volume":"25","author":"Pedersen","year":"2015","journal-title":"Scand. J. Med. Sci. Sports"},{"key":"B36","doi-asserted-by":"publisher","first-page":"1243","DOI":"10.1152\/physrev.00031.2007","article-title":"Exercise-induced oxidative stress: cellular mechanisms and impact on muscle force production","volume":"88","author":"Powers","year":"2008","journal-title":"Physiol. Rev."},{"key":"B37","doi-asserted-by":"publisher","first-page":"470","DOI":"10.1016\/j.freeradbiomed.2024.07.041","article-title":"Exercise-induced Nrf2 activation increases antioxidant defenses in skeletal muscles","volume":"224","author":"Powers","year":"","journal-title":"Free Radic. Biol. Med."},{"key":"B38","doi-asserted-by":"publisher","first-page":"780","DOI":"10.1016\/j.jshs.2024.05.001","article-title":"Reactive oxygen species promote endurance exercise-induced adaptations in skeletal muscles","volume":"13","author":"Powers","year":"","journal-title":"J. Sport Heal. Sci."},{"key":"B39","doi-asserted-by":"publisher","first-page":"165778","DOI":"10.1016\/j.bbadis.2020.165778","article-title":"Exercise, redox system and neurodegenerative diseases","volume":"1866","author":"Quan","year":"2020","journal-title":"Biochim. Biophys. acta. Mol. basis Dis."},{"key":"B40","doi-asserted-by":"publisher","first-page":"187","DOI":"10.1016\/j.freeradbiomed.2016.01.024","article-title":"Physical exercise, reactive oxygen species and neuroprotection","volume":"98","author":"Radak","year":"2016","journal-title":"Free Radic. Biol. Med."},{"key":"B41","doi-asserted-by":"publisher","first-page":"8665","DOI":"10.1073\/pnas.0903485106","article-title":"Antioxidants prevent health-promoting effects of physical exercise in humans","volume":"106","author":"Ristow","year":"2009","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"B42","doi-asserted-by":"publisher","first-page":"560","DOI":"10.1016\/j.cell.2015.10.001","article-title":"Mitochondrial ROS signaling in organismal homeostasis","volume":"163","author":"Shadel","year":"2015","journal-title":"Cell"},{"key":"B43","doi-asserted-by":"publisher","first-page":"933","DOI":"10.1016\/j.freeradbiomed.2024.11.002","article-title":"Dynamics of intracellular and intercellular redox communication","volume":"225","author":"Sies","year":"2024","journal-title":"Free Radic. Biol. Med."},{"key":"B44","doi-asserted-by":"publisher","first-page":"363","DOI":"10.1038\/s41580-020-0230-3","article-title":"Reactive oxygen species (ROS) as pleiotropic physiological signalling agents","volume":"21","author":"Sies","year":"2020","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"B45","doi-asserted-by":"publisher","first-page":"758","DOI":"10.1038\/s41580-024-00754-8","article-title":"Author correction: fundamentals of redox regulation in biology","volume":"25","author":"Sies","year":"2024","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"B46","doi-asserted-by":"publisher","first-page":"141","DOI":"10.1038\/s41580-021-00415-0","article-title":"The assembly, regulation and function of the mitochondrial respiratory chain","volume":"23","author":"Vercellino","year":"2022","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"B47","doi-asserted-by":"publisher","first-page":"1915","DOI":"10.1083\/jcb.201708007","article-title":"Superoxide dismutases: dual roles in controlling ROS damage and regulating ROS signaling","volume":"217","author":"Wang","year":"2018","journal-title":"J. Cell Biol."},{"key":"B48","doi-asserted-by":"publisher","first-page":"541","DOI":"10.1097\/HCO.0000000000000437","article-title":"Health benefits of physical activity: a systematic review of current systematic reviews","volume":"32","author":"Warburton","year":"2017","journal-title":"Curr. Opin. Cardiol."},{"key":"B49","doi-asserted-by":"publisher","first-page":"2044","DOI":"10.3390\/jcm8122044","article-title":"Health benefits of physical activity: a strengths-based approach","volume":"8","author":"Warburton","year":"2019","journal-title":"J. Clin. Med."},{"key":"B50","doi-asserted-by":"publisher","first-page":"2004","DOI":"10.1152\/jappl.1992.73.5.2004","article-title":"Adaptation of mitochondrial ATP production in human skeletal muscle to endurance training and detraining","volume":"73","author":"Wibom","year":"1992","journal-title":"J. Appl. Physiol."},{"key":"B51","doi-asserted-by":"publisher","first-page":"109643","DOI":"10.1016\/j.isci.2024.109643","article-title":"Redox signaling and skeletal muscle adaptation during aerobic exercise","volume":"27","author":"Zhou","year":"2024","journal-title":"iScience"},{"key":"B52","doi-asserted-by":"publisher","first-page":"R1101","DOI":"10.1152\/ajpregu.00046.2014","article-title":"Mechanisms responsible for the acceleration of pulmonary V\u0307O2 on-kinetics in humans after prolonged endurance training","volume":"307","author":"Zoladz","year":"2014","journal-title":"Am. J. Physiol. Regul. Integr. Comp. Physiol."},{"key":"B53","doi-asserted-by":"publisher","first-page":"719","DOI":"10.1016\/j.pharep.2015.06.002","article-title":"Coronary and muscle blood flow during physical exercise in humans; heterogenic alliance","volume":"67","author":"Zoladz","year":"2015","journal-title":"Pharmacol. Rep."},{"key":"B54","doi-asserted-by":"publisher","first-page":"1709","DOI":"10.1007\/s00424-016-1867-9","article-title":"Endurance training increases the efficiency of rat skeletal muscle mitochondria","volume":"468","author":"Zoladz","year":"2016","journal-title":"Pflugers Arch."},{"key":"B55","doi-asserted-by":"publisher","first-page":"10843","DOI":"10.3390\/ijms231810843","article-title":"Endurance training increases the running performance of untrained men without changing the mitochondrial volume density in the gastrocnemius muscle","volume":"23","author":"Zoladz","year":"2022","journal-title":"Int. J. Mol. Sci."}],"container-title":["Frontiers in Molecular Biosciences"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fmolb.2025.1653162\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,16]],"date-time":"2025-10-16T04:16:47Z","timestamp":1760588207000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fmolb.2025.1653162\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,10,16]]},"references-count":55,"alternative-id":["10.3389\/fmolb.2025.1653162"],"URL":"https:\/\/doi.org\/10.3389\/fmolb.2025.1653162","relation":{},"ISSN":["2296-889X"],"issn-type":[{"value":"2296-889X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,10,16]]},"article-number":"1653162"}}