Altering the redox state of skeletal muscle by glutathione depletion increases the exercise-activation of PGC-1α

Physiological Reports

Volumn 2, Issue 12, 2014, Pages

  Strobel, Natalie A ^a   Matsumoto, Aya ^b   Peake, Jonathan M ^c   Marsh, Susan A ^d   Peternelj, Tina Tinkara ^a   Briskey, David ^a   Fassett, Robert G ^a   Coombes, Jeff S ^a   Wadley, Glenn D ^e,f  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b BAKER IDI HEART AND DIABETES INSTITUTE   (Australia)

^c QUEENSLAND UNIVERSITY OF TECHNOLOGY   (Australia)

^d WASHINGTON STATE UNIVERSITY   (United States)

^e UNIVERSITY OF MELBOURNE   (Australia)

^f DEAKIN UNIVERSITY   (Australia)

Author keywords

Diethyl maleate; Exercise; PGC 1 ; Reactive oxygen species

Indexed keywords

GLUTATHIONE; GLUTATHIONE PEROXIDASE 1; ISOPROSTANE DERIVATIVE; MALEIC ACID DIETHYL ESTER; MANGANESE SUPEROXIDE DISMUTASE; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 14; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; REACTIVE OXYGEN METABOLITE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; EXERCISE; GENE EXPRESSION; MALE; MASS FRAGMENTOGRAPHY; MITOCHONDRIAL BIOGENESIS; NONHUMAN; OXIDATION REDUCTION STATE; OXIDATIVE STRESS; PROTEIN DEPLETION; PROTEIN PHOSPHORYLATION; RAT; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; TREADMILL EXERCISE; WESTERN BLOTTING;

EID: 85003632874     PISSN: None     EISSN: 2051817X     Source Type: Journal    
DOI: 10.14814/phy2.12224     Document Type: Article

References (50)

1. Akimoto, T., S. C. Pohnert, P. Li, M. Zhang, C. Gumbs, P. B. Rosenberg, et al. 2005. Exercise stimulates Pgc-1alpha transcription in skeletal muscle through activation of the p38 MAPK pathway. J. Biol. Chem. 280:19587-19593.
2. Baar, K., A. R. Wende, T. E. Jones, M. Marison, L. A. Nolte, M. Chen, et al. 2002. Adaptations of skeletal muscle to exercise: rapid increase in the transcriptional coactivator PGC-1. FASEB J. 16:1879-1886.
3. Bailey, D. M., B. Davies, I. S. Young, M. J. Jackson, G. W. Davison, R. Isaacson, et al. 2003. EPR spectroscopic detection of free radical outflow from an isolated muscle bed in exercising humans. J. Appl. Physiol. 94:1714-1718.
4. Bailey, D. M., I. S. Young, J. McEneny, L. Lawrenson, J. Kim, J. Barden, et al. 2004. Regulation of free radical outflow from an isolated muscle bed in exercising humans. Am. J. Physiol. Heart Circ. Physiol. 287:H1689-H1699.
5. Bedford, T. G., C. M. Tipton, N. C. Wilson, R. A. Oppliger, and C. V. Gisolfi. 1979. Maximum oxygen consumption of rats and its changes with various experimental procedures. J. Appl. Physiol. 47:1278-1283.
6. Briskey, D. R., G. R. Wilson, R. G. Fassett, and J. S. Coombes. 2013. Optimized method for quantification of total F-isoprostanes using gas chromatography-tandem mass spectrometry. J. Pharm. Biomed. Anal. 90C:161-166.
7. Dudley, R. W., M. Khairallah, M. S, L. L, D. R. C, and P. BJ. 2006. Dynamic responses of the glutathione system to acute oxidative stress in dystrophic mouse (mdx) muscles. Am. J. Physiol. Regul. Integr. Comp. Physiol. 291:R704-R710.
8. Gerard-Monnier, D., S. Fougeat, and J. Chaudiere. 1992. Glutathione and cysteine depletion in rats and mice following acute intoxication with diethylmaleate. Biochem. Pharmacol. 43:451-456.
9. Goethals, F., G. Krack, D. Deboyser, and M. Roberfroid. 1983. Effects of diethyl maleate on protein synthesis in isolated hepatocytes. Toxicology 26:47-54.
10. Gomez-Cabrera, M. C., C. Borras, F. V. Pallardo, J. Sastre, L. L. Ji, and J. Vina. 2005. Decreasing xanthine oxidase-mediated oxidative stress prevents useful cellular adaptations to exercise in rats. J. Physiol. 567:113-120.
11. Gomez-Cabrera, M. C., E. Domenech, M. Romagnoli, A. Arduini, C. Borras, F. V. Pallardo, et al. 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.
12. Hellsten, Y., J. J. Nielsen, J. Lykkesfeldt, M. Bruhn, L. Silveira, H. Pilegaard, et al. 2007. Antioxidant supplementation enhances the exercise-induced increase in mitochondrial uncoupling protein 3 and endothelial nitric oxide synthase mRNA content in human skeletal muscle. Free Radic. Biol. Med. 43:353-361.
13. Higashida, K., S. H. Kim, M. Higuchi, J. O. Holloszy, and D. H. Han. 2011. Normal adaptations to exercise despite protection against oxidative stress. Am. J. Physiol. Endocrinol. Metab. 301:E779-E784.
14. Hollander, J., R. Fiebig, M. Gore, T. Ookawara, H. Ohno, and L. L. Ji. 2001. Superoxide dismutase gene expression is activated by a single bout of exercise in rat skeletal muscle. Pflugers Arch. 442:426-434.
15. Hood, D. A. 2009. Mechanisms of exercise-induced mitochondrial biogenesis in skeletal muscle. Appl. Physiol. Nutr. Metab. 34:465-472.
16. Irrcher, I., V. Ljubicic, A. F. Kirwan, and D. A. Hood. 2008. AMP-activated protein kinase-regulated activation of the PGC-1alpha promoter in skeletal muscle cells. PLoS ONE 3: e3614.
17. Irrcher, I., V. Ljubicic, and D. A. Hood. 2009. Interactions between ROS and AMP kinase activity in the regulation of PGC-1alpha transcription in skeletal muscle cells. Am. J. Physiol. Cell Physiol. 296:C116-C123.
18. Joseph, A. M., H. Pilegaard, A. Litvintsev, L. Leick, and D. A. Hood. 2006. Control of gene expression and mitochondrial biogenesis in the muscular adaptation to endurance exercise. Essays Biochem. 42:13-29.
19. Kang, C., K. M. O’Moore, J. R. Dickman, and L. L. Ji. 2009. Exercise activation of muscle peroxisome proliferator-activated receptor-gamma coactivator-1alpha signaling is redox sensitive. Free Radic. Biol. Med. 47:1394-1400.
20. Kramer, K., H. Dijkstra, and A. Bast. 1993. Control of physical exercise of rats in a swimming basin. Physiol. Behav. 53:271-276.
21. Lambert, M. I., C. Van Zyl, R. Jaunky, E. V. Lambert, and T. D. Noakes. 1996. Tests of running performance do not predict subsequent spontaneous running in rats. Physiol. Behav. 60:171-176.
22. Leeuwenburgh, C., and L. L. Ji. 1995. Glutathione depletion in rested and exercised mice: biochemical consequence and adaptation. Arch. Biochem. Biophys. 316:941-949.
23. Lew, H., S. Pyke, and A. Quintanilha. 1985. Changes in the glutathione status of plasma, liver and muscle following exhaustive exercise in rats. FEBS Lett. 185:262-266.
24. Lundby, C., N. Nordsborg, K. Kusuhara, K. M. Kristensen, P. D. Neufer, and H. Pilegaard. 2005. Gene expression in human skeletal muscle: alternative normalization method and effect of repeated biopsies. Eur. J. Appl. Physiol. 95:351-360.
25. Meier, P., M. Renga, H. Hoppeler, and O. Baum. 2013. The impact of antioxidant supplements and endurance exercise on genes of the carbohydrate and lipid metabolism in skeletal muscle of mice. Cell Biochem. Funct. 31:51-59.
26. Oyanagui, Y. 1984. Reevaluation of assay methods and establishment of kit for superoxide dismutase activity. Anal. Biochem. 142:290-296.
27. Paulsen, G., K. T. Cumming, G. Holden, J. Hallen, B. R. Ronnestad, O. Sveen, et al. 2014. Vitamin C and E supplementation hampers cellular adaptation to endurance training in humans: a double-blind, randomised, controlled trial. J. Physiol. 592:1887-1901.
28. Perry, C. G., J. Lally, G. P. Holloway, G. J. Heigenhauser, A. Bonen, and L. L. Spriet. 2010. Repeated transient mRNA bursts precede increases in transcriptional and mitochondrial proteins during training in human skeletal muscle. J. Physiol. 588:4795-4810.
29. Petersen, A. C., M. J. McKenna, I. Medved, K. T. Murphy, M. J. Brown, P. Della Gatta, et al. 2012. Infusion with the antioxidant N-acetylcysteine attenuates early adaptive responses to exercise in human skeletal muscle. Acta Physiol. (Oxf) 204:382-392.
30. Pilegaard, H., B. Saltin, and P. D. Neufer. 2003. Exercise induces transient transcriptional activation of the PGC-1alpha gene in human skeletal muscle. J. Physiol. 546:851-858.
31. Pimenta Ada, S., R. H. Lambertucci, R. Gorjao, R. Silveira Ldos, and R. Curi. 2007. Effect of a single session of electrical stimulation on activity and expression of citrate synthase and antioxidant enzymes in rat soleus muscle. Eur. J. Appl. Physiol. 102:119-126.
32. Psilander, N., P. Frank, M. Flockhart, and K. Sahlin. 2013. Exercise with low glycogen increases PGC-1alpha gene expression in human skeletal muscle. Eur. J. Appl. Physiol. 113:951-963.
33. Rhinn, H., C. Marchand-Leroux, N. Croci, M. Plotkine, D. Scherman, and V. Escriou. 2008a. Housekeeping while brain’s storming Validation of normalizing factors for gene expression studies in a murine model of traumatic brain injury. BMC Mol. Biol. 9:62.
34. Rhinn, H., D. Scherman, and V. Escriou. 2008b. One-step quantification of single-stranded DNA in the presence of RNA using Oligreen in a real-time polymerase chain reaction thermocycler. Anal. Biochem. 372:116-118.
35. Ristow, M., K. Zarse, A. Oberbach, N. Kloting, M. Birringer, M. Kiehntopf, et al. 2009. Antioxidants prevent health-promoting effects of physical exercise in humans. Proc. Natl. Acad. Sci. U.S.A. 106:8665-8670.
36. Sen, C. K., M. Atalay, and O. Hanninen. 1994. Exercise-induced oxidative stress: glutathione supplementation and deficiency. J. Appl. Physiol. 77:2177-2187.
37. Silveira, L. R., H. Pilegaard, K. Kusuhara, R. Curi, and Y. Hellsten. 2006. The contraction induced increase in gene expression of peroxisome proliferator-activated receptor (PPAR)-gamma coactivator 1alpha (PGC-1alpha), mitochondrial uncoupling protein 3 (UCP3) and hexokinase II (HKII) in primary rat skeletal muscle cells is dependent on reactive oxygen species. Biochim. Biophys. Acta 1763:969-976.
38. St-Pierre, J., S. Drori, M. Uldry, J. M. Silvaggi, J. Rhee, S. Jager, et al. 2006. Suppression of reactive oxygen species and neurodegeneration by the PGC-1 transcriptional coactivators. Cell 127:397-408.
39. Strobel, N. A., J. M. Peake, A. Matsumoto, S. A. Marsh, J. S. Coombes, and G. D. Wadley. 2011. Antioxidant supplementation reduces skeletal muscle mitochondrial biogenesis. Med. Sci. Sports Exerc. 43:1017-1024.
40. Terada, S., and I. Tabata. 2004. Effects of acute bouts of running and swimming exercise on PGC-1alpha protein expression in rat epitrochlearis and soleus muscle. Am. J. Physiol. Endocrinol. Metab. 286:E208-E216.
41. Wadley, G. D., and G. K. McConell. 2007. Effect of nitric oxide synthase inhibition on mitochondrial biogenesis in rat skeletal muscle. J. Appl. Physiol. 102:314-320.
42. Wadley, G. D., and G. K. McConell. 2010. High-dose antioxidant vitamin C supplementation does not prevent acute exercise-induced increases in markers of skeletal muscle mitochondrial biogenesis in rats. J. Appl. Physiol. 108:1719-1726.
43. Wadley, G. D., R. J. Tunstall, A. Sanigorski, G. R. Collier, M. Hargreaves, and D. Cameron-Smith. 2001. Differential effects of exercise on insulin-signaling gene expression in human skeletal muscle. J. Appl. Physiol. 90:436-440.
44. Wadley, G. D., M. A. Nicolas, D. S. Hiam, and G. K. McConell. 2013. Xanthine oxidase inhibition attenuates skeletal muscle signaling following acute exercise but does not impair mitochondrial adaptations to endurance training. Am. J. Physiol. Endocrinol. Metab. 304: E853-E862.
45. Wheeler, C. R., J. A. Salzman, N. M. Elsayed, S. T. Omaye, and D. W. Korte Jr. 1990. Automated assays for superoxide dismutase, catalase, glutathione peroxidase, and glutathione reductase activity. Anal. Biochem. 184:193-199.
46. Williams, S. L., N. A. Strobel, L. A. Lexis, and J. S. Coombes. 2006. Antioxidant requirements of endurance athletes: implications for health. Nutr. Rev. 64:93-108.
47. Wright, D. C., D. H. Han, P. M. Garcia-Roves, P. C. Geiger, T. E. Jones, and J. O. Holloszy. 2007. Exercise-induced mitochondrial biogenesis begins before the increase in muscle PGC-1alpha expression. J. Biol. Chem. 282:194-199.
48. Wu, H., S. B. Kanatous, F. A. Thurmond, T. Gallardo, E. Isotani, R. Bassel-Duby, et al. 2002. Regulation of mitochondrial biogenesis in skeletal muscle by CaMK. Science 296:349-352.
49. Wu, Z., X. Huang, Y. Feng, C. Handschin, P. S. Gullicksen, O. Bare, et al. 2006. Transducer of regulated CREB-binding proteins (TORCs) induce PGC-1alpha transcription and mitochondrial biogenesis in muscle cells. Proc. Natl. Acad. Sci. U.S.A. 103:14379-14384.
50. Yfanti, C., T. Akerstrom, S. Nielsen, A. R. Nielsen, R. Mounier, O. H. Mortensen, et al. 2010. Antioxidant supplementation does not alter endurance training adaptation. Med. Sci. Sports Exerc. 42:1388-1395.