Abstract
Exercise leads to the production of reactive oxygen species (ROS) via several sources in the skeletal muscle. In particular, the mitochondrial electron transport chain in the muscle cells produces ROS along with an elevation in the oxygen consumption during exercise. Such ROS generated during exercise can cause oxidative modification of proteins and affect their functionality. Many evidences have been suggested that some muscle proteins, i.e., myofiber proteins, metabolic signaling proteins, and sarcoplasmic reticulum proteins can be a targets modified by ROS generated due to exercise. We detected the modification of carnitine palmitoyltransferase I (CPT I) by Nε-(hexanoyl)lysine (HEL), one of the lipid peroxides, in exercised muscles, while the antioxidant astaxanthin reduced this oxidative stress-induced modification. Exercise-induced ROS may diminish CPT I activity caused by HEL modification, leading to a partly limited lipid utilization in the mitochondria. This oxidative protein modification may be useful as a potential biomarker to examine the oxidative stress levels, antioxidant compounds, and their possible benefits in exercise.
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References
Aikawa KM, Quintanilha AT, de Lumen BO, Brooks GA, Packer L (1984) Exercise endurance training alters vitamin E tissue level and red blood cell hemolysis in rodents. Biosci Rep 4:253–257
Anzueto A, Andrade FH, Maxwell LC, Levine SM, Lawrence RA, Gibbons WJ, Jenkinson SG (1992) Resistive breathing activates the glutathione redox cycle and impairs performance of rat diaphragm. J Appl Physiol 72:529–534
Aoi W, Naito Y, Sakuma K, Kuchide M, Tokuda H, Maoka T, Toyokuni S, Oka S, Yasuhara M, Yoshikawa T (2003) Astaxanthin limits exercise-induced skeletal and cardiac muscle damage in mice. Antioxid Redox Signal 5:139–144
Aoi W, Naito Y, Takanami Y, Kawai Y, Sakuma K, Ichikawa H, Yoshida N, Yoshikawa T (2004) Oxidative stress and delayed-onset muscle damage after exercise. Free Radic Biol Med 37:480–487
Aoi W, Naito Y, Takanami Y, Ishii T, Kawai Y, Akagiri S, Kato Y, Osawa T, Yoshikawa T (2008) Astaxanthin improves muscle lipid metabolism in exercise via inhibitory effect of oxidative CPT I modification. Biochem Biophys Res Commun 366:892–897
Aoi W, Naito Y, Tokuda H, Tanimura Y, Oya-Ito T, Yoshikawa T (2012) Exercise-induced muscle damage impairs insulin signaling pathway associated with IRS-1 oxidative modification. Physiol Res 61:81–88
Ashton T, Young IS, Peters JR, Jones E, Jackson SK, Davies B, Rowlands CC (1999) Electron spin resonance spectroscopy, exercise, and oxidative stress: an ascorbic acid intervention study. J Appl Physiol 87:2032–2036
Barreiro E, Hussain SN (2010) Protein carbonylation in skeletal muscles: impact on function. Antioxid Redox Signal 12:417–429
Bidasee KR, Zhang Y, Shao CH, Wang M, Patel KP, Dincer UD, Besch HR Jr (2004) Diabetes increases formation of advanced glycation end products on sarco(endo)plasmic reticulum Ca2+-ATPase. Diabetes 53:463–473
Blomstrand E, Rådegran G, Saltin B (1997) Maximum rate of oxygen uptake by human skeletal muscle in relation to maximal activities of enzymes in the Krebs cycle. J Physiol 501:455–460
Bryer SC, Goldfarb AH (2006) Effect of high dose vitamin C supplementation on muscle soreness, damage, function, and oxidative stress to eccentric exercise. Int J Sport Nutr Exerc Metab 16:270–280
Campbell SE, Tandon NN, Woldegiorgis G, Luiken JJ, Glatz JF, Bonen A (2004) A novel function for fatty acid translocase (FAT)/CD36: involvement in long chain fatty acid transfer into the mitochondria. J Biol Chem 279:36235–36241
Chang CK, Huang HY, Tseng HF, Hsuuw YD, Tso TK (2007) Interaction of vitamin E and exercise training on oxidative stress and antioxidant enzyme activities in rat skeletal muscles. J Nutr Biochem 18:39–45
Chen W, Ruell PA, Ghoddusi M, Kee A, Hardeman EC, Hoffman KM, Thompson MW (2007) Ultrastructural changes and sarcoplasmic reticulum Ca2+ regulation in red vastus muscle following eccentric exercise in the rat. Exp Physiol 92:437–447
Cobley JN, McGlory C, Morton JP, Close GL (2011) N-Acetylcysteine’s attenuation of fatigue after repeated bouts of intermittent exercise: practical implications for tournament situations. Int J Sport Nutr Exerc Metab 21:451–461
Couillard A, Maltais F, Saey D, Debigaré R, Michaud A, Koechlin C, LeBlanc P, Préfaut C (2003) Exercise-induced quadriceps oxidative stress and peripheral muscle dysfunction in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 167:1664–1669
Crowder MS, Cooke R (1984) The effect of myosin sulphydryl modification on the mechanics of fibre contraction. J Muscle Res Cell Motil 5:131–146
Daiho T, Kanazawa T (1994) Reduction of disulfide bonds in sarcoplasmic reticulum Ca2+-ATPase by dithiothreitol causes inhibition of phosphoenzyme isomerization in catalytic cycle. This reduction requires binding of both purine nucleotide and Ca2+ to enzyme. J Biol Chem 269:11060–11064
Davies KJ, Quintanilha AT, Brooks GA, Packer L (1982) Free radicals and tissue damage produced by exercise. Biochem Biophys Res Commun 107:1198–1205
Dolinsky VW, Jones KE, Sidhu RS, Haykowsky M, Czubryt MP, Gordon T, Dyck JR (2012) Improvements in skeletal muscle strength and cardiac function induced by resveratrol during exercise training contribute to enhanced exercise performance in rats. J Physiol 590:2783–2799
Duarte JA, Appell HJ, Carvalho F, Bastos ML, Soares JM (1993) Endothelium-derived oxidative stress may contribute to exercise-induced muscle damage. Int J Sports Med 14:440–443
Fedorova M, Kuleva N, Hoffmann R (2009) Reversible and irreversible modifications of skeletal muscle proteins in a rat model of acute oxidative stress. Biochim Biophys Acta 1792:1185–1193
Ferguson RA, Ball D, Krustrup P, Aagaard P, Kjaer M, Sargeant AJ, Hellsten Y, Bangsbo J (2001) Muscle oxygen uptake and energy turnover during dynamic exercise at different contraction frequencies in humans. J Physiol 536:261–271
Flamm SD, Taki J, Moore R et al (1990) Redistribution of regional and organ blood volume and effect on cardiac function in relation to upright exercise intensity in healthy human subjects. Circulation 81:1550–1559
Gissel H, Clausen T (2001) Excitation-induced Ca2+ influx and skeletal muscle cell damage. Acta Physiol Scand 171:327–334
Goldfarb AH, Garten RS, Cho C, Chee PD, Chambers LA (2011) Effects of a fruit/berry/vegetable supplement on muscle function and oxidative stress. Med Sci Sports Exerc 43:501–508
Gomez-Cabrera MC, Domenech E, Romagnoli M, Arduini A, Borras C, Pallardo FV, Sastre J, Viña J (2008) Oral administration of vitamin C decreases muscle mitochondrial biogenesis and hampers training-induced adaptations in endurance performance. Am J Clin Nutr 87:142–149
Gutierrez-Martin Y, Martin-Romero FJ, Inesta-Vaquera FA, Gutierrez-Merino C, Henao F (2004) Modulation of sarcoplasmic reticulum Ca2+-ATPase by chronic and acute exposure to peroxynitrite. Eur J Biochem 271:2647–2657
Haus JM, Carrithers JA, Trappe SW, Trappe TA (2007) Collagen, cross-linking, and advanced glycation end products in aging human skeletal muscle. J Appl Physiol 103:2068–2076
Henriksen EJ (2006) Exercise training and the antioxidant alpha-lipoic acid in the treatment of insulin resistance and type 2 diabetes. Free Radic Biol Med 40:3–12
Hill BG, Bhatnagar A (2012) Protein S-glutathiolation: redox-sensitive regulation of protein function. J Mol Cell Cardiol 52:559–567
Holloway GP, Bezaire V, Heigenhauser GJ, Tandon NN, Glatz JF, Luiken JJ, Bonen A, Spriet LL (2006) Mitochondrial long chain fatty acid oxidation, fatty acid translocase/CD36 content and carnitine palmitoyltransferase I activity in human skeletal muscle during aerobic exercise. J Physiol 571:201–210
Ikeuchi M, Koyama T, Takahashi J, Yazawa K (2006) Effects of astaxanthin supplementation on exercise-induced fatigue in mice. Biol Pharm Bull 29:2106–2110
Joneschild ES, Chen LE, Seaber AV, Frankel ES, Urbaniak JR (1999) Effect of a NOS inhibitor, L-NMMA, on the contractile function of reperfused skeletal muscle. J J Reconstr Microsurg 15:55–60
Kato Y, Mori Y, Makino Y, Morimitsu Y, Hiroi S, Ishikawa T, Osawa T (1999) Formation of Nε-(hexanonyl)lysine in protein exposed to lipid hydroperoxide. A plausible marker for lipid hydroperoxide-derived protein modification. J Biol Chem 274:20406–20414
Kato Y, Miyake K, Yamamoto Y, Shimomura H, Ochi Y, Mori T, Osawa T (2000) Preparation of a monoclonal antibody to Nε-(hexanonyl)lysine: application to the evaluation of protective effects of flavonoid supplementation against exercise-induced oxidative stress in rat skeletal muscle. Biochem Biophys Res Commun 274:389–393
Kobzik L, Reid MB, Bredt DS, Stamler JS (1994) Nitric oxide in skeletal muscle. Nature 372:546–548
Kobzik L, Stringer B, Balligand JL, Reid MB, Stamler JS (1995) Endothelial type nitric oxide synthase in skeletal muscle fibers: mitochondrial relationships. Biochem Biophys Res Commun 211:375–381
Komulainen J, Takala TE, Kuipers H, Hesselink MK (1998) The disruption of myofibre structures in rat skeletal muscle after forced lengthening contractions. Pflugers Arch 436:735–741
Liao P, Zhou J, Ji LL, Zhang Y (2010) Eccentric contraction induces inflammatory responses in rat skeletal muscle: role of tumor necrosis factor-α. Am J Physiol Regul Integr Comp Physiol 298:R599–R607
Liu DF, Wang D, Stracher A (1990) The accessibility of the thiol groups on G- and F-actin of rabbit muscle. Biochem J 266:453–459
Liu J, Yeo HC, Overvik-Douki E, Hagen T, Doniger SJ, Chyu DW, Brooks GA, Ames BN (2000) Chronically and acutely exercised rats: biomarkers of oxidative stress and endogenous antioxidants. J Appl Physiol 89:21–28
Liu JF, Chang WY, Chan KH, Tsai WY, Lin CL, Hsu MC (2005) Blood lipid peroxides and muscle damage increased following intensive resistance training of female weightlifters. Ann N Y Acad Sci 1042:255–261
Magherini F, Abruzzo PM, Puglia M, Bini L, Gamberi T, Esposito F, Veicsteinas A, Marini M, Fiorillo C, Gulisano M, Modesti A (2012) Proteomic analysis and protein carbonylation profile in trained and untrained rat muscles. J Proteomics 75:978–992
Manabe E, Handa O, Naito Y, Mizushima K, Akagiri S, Adachi S, Takagi T, Kokura S, Maoka T, Yoshikawa T (2008) Astaxanthin protects mesangial cells from hyperglycemia-induced oxidative signaling. J Cell Biochem 103:1925–1937
Matuszczak Y, Farid M, Jones J, Lansdowne S, Smith MA, Taylor AA, Reid MB (2005) Effects of N-acetylcysteine on glutathione oxidation and fatigue during handgrip exercise. Muscle Nerve 32:633–638
McGarry JD, Brown NF (1997) The mitochondrial carnitine palmitoyltransferase system. From concept to molecular analysis. Eur J Biochem 244:1–14
McKenna MJ, Medved I, Goodman CA, Brown MJ, Bjorksten AR, Murphy KT, Petersen AC, Sostaric S, Gong X (2006) N-acetylcysteine attenuates the decline in muscle Na+, K+-pump activity and delays fatigue during prolonged exercise in humans. J Physiol 576:279–288
Medved I, Brown MJ, Bjorksten AR, McKenna MJ (2004) Effects of intravenous N-acetylcysteine infusion on time to fatigue and potassium regulation during prolonged cycling exercise. J Appl Physiol 96:211–217
Miyazaki H, Oh-ishi S, Ookawara T, Kizaki T, Toshinai K, Ha S, Haga S, Ji LL, Ohno H (2001) Strenuous endurance training in humans reduces oxidative stress following exhausting exercise. Eur J Appl Physiol 84:1–6
Morrison RJ, Miller CC 3rd, Reid MB (1998) Nitric oxide effects on force-velocity characteristics of the rat diaphragm. Comp Biochem Physiol A Mol Integr Physiol 119:203–209
Naito Y, Yoshikawa T (2009) Oxidative stress-induced posttranslational modification of proteins as a target of functional food. Forum Nutr 61:39–54
Novelli GP, Bracciotti G, Falsini S (1990) Spin-trappers and vitamin E prolong endurance to muscle fatigue in mice. Free Radic Biol Med 8:9–13
Osawa T, Kato Y (2005) Protective role of antioxidative food factors in oxidative stress caused by hyperglycemia. Ann N Y Acad Sci 1043:440–451
Oya-Ito T, Naito Y, Takagi T, Handa O, Matsui H, Yamada M, Shima K, Yoshikawa T (2011) Heat-shock protein 27 (Hsp27) as a target of methylglyoxal in gastrointestinal cancer. Biochim Biophys Acta 1812:769–781
Perkins WJ, Han YS, Sieck GC (1997) Skeletal muscle force and actomyosin ATPase activity reduced by nitric oxide donor. J Appl Physiol 83:1326–1332
Powers SK, Jackson MJ (2008) Exercise-induced oxidative stress: cellular mechanisms and impact on muscle force production. Physiol Rev 88:1243–1276
Proske U, Morgan DL (2001) Muscle damage from eccentric exercise: mechanism, mechanical signs, adaptation and clinical applications. J Physiol 537:333–345
Reid MB, Stokic DS, Koch SM, Khawli FA, Leis AA (1994) N-acetylcysteine inhibits muscle fatigue in humans. J Clin Invest 94:2468–2474
Richards JC, Lonac MC, Johnson TK, Schweder MM, Bell C (2010) Epigallocatechin-3-gallate increases maximal oxygen uptake in adult humans. Med Sci Sports Exerc 42:739–744
Richmonds CR, Kaminski HJ (2001) Nitric oxide synthase expression and effects of nitric oxide modulation on contractility of rat extraocular muscle. FASEB J 15:1764–1770
Rietjens SJ, Beelen M, Koopman R, VAN Loon LJ, Bast A, Haenen GR (2007) A single session of resistance exercise induces oxidative damage in untrained men. Med Sci Sports Exerc 39:2145–2151
Ristow M, Zarse K, Oberbach A, Klöting N, Birringer M, Kiehntopf M, Stumvoll M, Kahn CR, Blüher M (2009) Antioxidants prevent health-promoting effects of physical exercise in humans. Proc Natl Acad Sci U S A 106:8665–8670
Rosa EF, Ribeiro RF, Pereira FM, Freymüller E, Aboulafia J, Nouailhetas VL (2009) Vitamin C and E supplementation prevents mitochondrial damage of ileum myocytes caused by intense and exhaustive exercise training. J Appl Physiol 107:1532–1538
Sahlin K, Shabalina IG, Mattsson CM, Bakkman L, Fernström M, Rozhdestvenskaya Z, Enqvist JK, Nedergaard J, Ekblom B, Tonkonogi M (2010) Ultraendurance exercise increases the production of reactive oxygen species in isolated mitochondria from human skeletal muscle. J Appl Physiol 108:780–787
Salama G, Abramson JJ, Pike GK (1992) Sulphydryl reagents trigger Ca2+ release from the sarcoplasmic reticulum of skinned rabbit psoas fibres. J Physiol 454:389–420
Sultana R, Butterfield DA (2009) Proteomics identification of carbonylated and HNE-bound brain proteins in Alzheimer’s disease. Methods Mol Biol 566:123–135
Sun J, Xu L, Eu JP, Stamler JS, Meissner G (2001) Classes of thiols that influence the activity of the skeletal muscle calcium release channel. J Biol Chem 276:15625–15630
Vassilakopoulos T, Deckman G, Kebbewar M, Rallis G, Harfouche R, Hussain SN (2003) Regulation of nitric oxide production in limb and ventilatory muscles during chronic exercise training. Am J Physiol Lung Cell Mol Physiol 284:L452–L457
Veskoukis AS, Nikolaidis MG, Kyparos A, Kokkinos D, Nepka C, Barbanis S, Kouretas D (2008) Effects of xanthine oxidase inhibition on oxidative stress and swimming performance in rats. Appl Physiol Nutr Metab 33:1140–1154
Viner RI, Krainev AG, Williams TD, Schoneich C, Bigelow DJ (1997) Identification of oxidation-sensitive peptides within the cytoplasmic domain of the sarcoplasmic reticulum Ca2+-ATPase. Biochemistry 36:7706–7716
Viner RI, Williams TD, Schoneich C (2000) Nitric oxide-dependent modification of the sarcoplasmic reticulum Ca-ATPase: localization of cysteine target sites. Free Radic Biol Med 29:489–496
Williams DL Jr, Swenson CA (1982) Disulfide bridges in tropomyosin effect on ATPase activity of actomyosin. Eur J Biochem 127:495–499
Xia R, Webb JA, Gnall LL, Cutler K, Abramson JJ (2003) Skeletal muscle sarcoplasmic reticulum contains a NADH-dependent oxidase that generates superoxide. Am J Physiol Cell Physiol 285:C215–C221
Xu KY, Zweier JL, Becker LC (1997) Hydroxyl radical inhibits sarcoplasmic reticulum Ca2+-ATPase function by direct attack on the ATP binding site. Circ Res 80:76–81
Yamada T, Mishima T, Sakamoto M, Sugiyama M, Matsunaga S, Wada M (2007) Myofibrillar protein oxidation and contractile dysfunction in hyperthyroid rat diaphragm. J Appl Physiol 102:1850–1855
Zhang JZ, Wu Y, Williams BY, Rodney G, Mandel F, Strasburg GM, Hamilton SL (1999) Oxidation of the skeletal muscle Ca2+ release channel alters calmodulin binding. Am J Physiol Cell Physiol 276:C46–C53
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Aoi, W., Naito, Y., Yoshikawa, T. (2014). Potential Role of Oxidative Protein Modification in Energy Metabolism in Exercise. In: Kato, Y. (eds) Lipid Hydroperoxide-Derived Modification of Biomolecules. Subcellular Biochemistry, vol 77. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-7920-4_15
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