Acute high-intensity interval exercise-induced redox signaling is associated with enhanced insulin sensitivity in obese middle-aged men

Frontiers in Physiology

Volumn 7, Issue SEP, 2016, Pages

  Parker, Lewan ^a   Stepto, Nigel K ^a   Shaw, Christopher S ^b   Serpiello, Fabio R ^a   Anderson, Mitchell ^a   Hare, David L ^c   Levinger, Itamar ^a  

^a VICTORIA UNIVERSITY   (Australia)

^b DEAKIN UNIVERSITY   (Australia)

^c UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

High intensity exercise; Insulin sensitivity; Obesity; Oxidative stress; Redox signaling; Stress kinase

Indexed keywords

4 HYDROXYNONENAL; CATALASE; HYDROGEN PEROXIDE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; STRESS ACTIVATED PROTEIN KINASE; SUPEROXIDE DISMUTASE; THIOBARBITURIC ACID REACTIVE SUBSTANCE; TRANSCRIPTION FACTOR RELA;

ADULT; AGED; ARTICLE; BLOOD LEVEL; CLINICAL ARTICLE; CORRELATIONAL STUDY; ENZYME ACTIVITY; EXERCISE; GLUCOSE TRANSPORT; HIGH INTENSITY INTERVAL EXERCISE; HUMAN; HUMAN TISSUE; HYPERINSULINEMIC-EUGLYCEMIC CLAMP TECHNIQUE; INSULIN SENSITIVITY; MALE; MIDDLE AGED; MUSCLE LEVEL; OBESITY; OXIDATION REDUCTION STATE; OXIDATIVE STRESS; PROTEIN ANALYSIS; PROTEIN CONTENT; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

EID: 84992130238     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphys.2016.00411     Document Type: Article

References (50)

1. Archuleta, T. L., Lemieux, A. M., Saengsirisuwan, V., Teachey, M. K., Lindborg, K. A., Kim, J. S., et al. (2009). Oxidant stress-induced loss of irs-1 and irs-2 proteins in rat skeletal muscle: role of p38 mapk. Free Radic. Biol. Med. 47, 1486-1493. doi: 10.1016/j.freeradbiomed.2009.08.014
2. Bashan, N., Kovsan, J., Kachko, I., Ovadia, H., and Rudich, A. (2009). Positive and negative regulation of insulin signaling by reactive oxygen and nitrogen species. Physiol. Rev. 89, 27-71. doi: 10.1152/physrev.00014.2008
3. Berdichevsky, A., Guarente, L., and Bose, A. (2010). Acute oxidative stress can reverse insulin resistance by inactivation of cytoplasmic jnk. J. Biol. Chem. 285, 21581-21589. doi: 10.1074/jbc.M109.093633
4. Boden, G. (2008). Obesity and free fatty acids. Endocrinol. Metab. Clin. North Am. 37, 635-646, viii-ix. doi: 10.1016/j.ecl.2008.06.007
5. Castorena, C. M., Arias, E. B., Sharma, N., and Cartee, G. D. (2014). Postexercise improvement in insulin-stimulated glucose uptake occurs concomitant with greater as160 phosphorylation in muscle from normal and insulin-resistant rats. Diabetes 63, 2297-2308. doi: 10.2337/db13-1686
6. Cook, R. D. (1979). Influential observations in linear regression. J. Am. Stat. Assoc. 74, 169-174. doi: 10.1080/01621459.1979.10481634
7. Danielsson, A., �st, A., Nystrom, F. H., and Str�lfors, P. (2005). Attenuation of insulin-stimulated insulin receptor substrate-1 serine 307 phosphorylation in insulin resistance of type 2 diabetes. J. Biol. Chem. 280, 34389-34392. doi: 10.1074/jbc.C500230200
8. de Alvaro, C., Teruel, T., Hernandez, R., and Lorenzo, M. (2004). Tumor necrosis factor alpha produces insulin resistance in skeletal muscle by activation of inhibitor kappab kinase in a p38 mapk-dependent manner. J. Biol. Chem. 279, 17070-17078. doi: 10.1074/jbc.M312021200
9. Diamond-Stanic, M. K., Marchionne, E. M., Teachey, M. K., Durazo, D. E., Kim, J. S., and Henriksen, E. J. (2011). Critical role of the transient activation of p38 mapk in the etiology of skeletal muscle insulin resistance induced by low-level in vitro oxidant stress. Biochem. Biophys. Res. Commun. 405, 439-444. doi: 10.1016/j.bbrc.2011.01.049
10. Dokken, B. B., Saengsirisuwan, V., Kim, J. S., Teachey, M. K., and Henriksen, E. J. (2008). Oxidative stress-induced insulin resistance in rat skeletal muscle: role of glycogen synthase kinase-3. Am. J. Physiol. Endocrinol. Metab. 294, E615-E621. doi: 10.1152/ajpendo.00578.2007
11. Egan, B., and Zierath, J. R. (2013). Exercise metabolism and the molecular regulation of skeletal muscle adaptation. Cell Metab. 17, 162-184. doi: 10.1016/j.cmet.2012.12.012
12. Evans, W. J., Phinney, S. D., and Young, V. R. (1982). Suction applied to a muscle biopsy maximizes sample size. Med. Sci. Sports Exerc. 14, 101-102.
13. Fr�sig, C., and Richter, E. A. (2009). Improved insulin sensitivity after exercise: focus on insulin signaling. Obesity 17(Suppl. 3), S15-S20. doi: 10.1038/oby.2009.383
14. Geiger, P. C., Wright, D. C., Han, D. H., and Holloszy, J. O. (2005). Activation of p38 map kinase enhances sensitivity of muscle glucose transport to insulin. Am. J. Physiol. Endocrinol. Metab. 288, E782-E788. doi: 10.1152/ajpendo.00477.2004
15. Gibala, M. J., Little, J. P., Macdonald, M. J., and Hawley, J. A. (2012). Physiological adaptations to low-volume, high-intensity interval training in health and disease. J. Physiol. 590, 1077-1084. doi: 10.1113/jphysiol.2011.224725
16. Greene, M. W., Morrice, N., Garofalo, R. S., and Roth, R. A. (2004). Modulation of human insulin receptor substrate-1 tyrosine phosphorylation by protein kinase cdelta. Biochem. J. 378, 105-116. doi: 10.1042/bj20031493
17. Gual, P., Le Marchand-Brustel, Y., and Tanti, J. F. (2005). Positive and negative regulation of insulin signaling through irs-1 phosphorylation. Biochimie 87, 99-109. doi: 10.1016/j.biochi.2004.10.019
18. Howlett, K. F., Mathews, A., Garnham, A., and Sakamoto, K. (2008). The effect of exercise and insulin on as160 phosphorylation and 14-3-3 binding capacity in human skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 294, E401-E407. doi: 10.1152/ajpendo.00542.2007
19. Hutchison, S. K., Stepto, N. K., Harrison, C. L., Moran, L. J., Strauss, B. J., and Teede, H. J. (2011). Effects of exercise on insulin resistance and body composition in overweight and obese women with and without polycystic ovary syndrome. J. Clin. Endocrinol. Metab. 96, E48-E56. doi: 10.1210/jc.2010-0828
20. Iwakami, S., Misu, H., Takeda, T., Sugimori, M., Matsugo, S., Kaneko, S., et al. (2011). Concentration-dependent dual effects of hydrogen peroxide on insulin signal transduction in h4iiec hepatocytes. PLoS ONE 6:e27401. doi: 10.1371/journal.pone.0027401
21. Kim, J. S., Saengsirisuwan, V., Sloniger, J. A., Teachey, M. K., and Henriksen, E. J. (2006). Oxidant stress and skeletal muscle glucose transport: roles of insulin signaling and p38 mapk. Free Radic. Biol. Med. 41, 818-824. doi: 10.1016/j.freeradbiomed.2006.05.031
22. Kramer, H. F., and Goodyear, L. J. (2007). Exercise, MAPK, and NK-?B signaling in skeletal muscle. J. Appl. Physiol. 103, 388-395. doi: 10.1152/japplphysiol.00085.2007
23. Lee, Y. H., Giraud, J., Davis, R. J., and White, M. F. (2003). C-jun n-terminal kinase (jnk) mediates feedback inhibition of the insulin signaling cascade. J. Biol. Chem. 278, 2896-2902. doi: 10.1074/jbc.M208359200
24. Levinger, I., Goodman, C., Hare, D. L., Jerums, G., and Selig, S. (2007). The effect of resistance training on functional capacity and quality of life in individuals with high and low numbers of metabolic risk factors. Diabetes Care 30, 2205-2210. doi: 10.2337/dc07-0841
25. Levinger, I., Jerums, G., Stepto, N. K., Parker, L., Serpiello, F. R., McConell, G. K., et al. (2014). The effect of acute exercise on undercarboxylated osteocalcin and insulin sensitivity in obese men. J. Bone Miner. Res. 29, 2571-2576. doi: 10.1002/jbmr.2285
26. Li, Y., Soos, T. J., Li, X. H., Wu, J., Degennaro, M., Sun, X. J., et al. (2004). Protein kinase c theta inhibits insulin signaling by phosphorylating IRS1 at ser(1101). J. Biol. Chem. 279, 45304-45307. doi: 10.1074/jbc.C400186200
27. Liubaoerjijin, Y., Terada, T., Fletcher, K., and Boul�, N. G. (2016). Effect of aerobic exercise intensity on glycemic control in type 2 diabetes: a meta-analysis of head-to-head randomized trials. Acta Diabetol. 53, 769-781. doi: 10.1007/s00592-016-0870-0
28. Loh, K., Deng, H., Fukushima, A., Cai, X., Boivin, B., Galic, S., et al. (2009). Reactive oxygen species enhance insulin sensitivity. Cell Metab. 10, 260-272. doi: 10.1016/j.cmet.2009.08.009
29. Mahadev, K., Motoshima, H., Wu, X., Ruddy, J. M., Arnold, R. S., Cheng, G., et al. (2004). The nad(p)h oxidase homolog nox4 modulates insulin-stimulated generation of h2o2 and plays an integral role in insulin signal transduction. Mol. Cell. Biol. 24, 1844-1854. doi: 10.1128/MCB.24.5.1844-1854.2004
30. Malin, S. K., and Braun, B. (2016). Impact of metformin on exercise-induced metabolic adaptations to lower type 2 diabetes risk. Exerc. Sport Sci. Rev. 44, 4-11. doi: 10.1249/JES.0000000000000070
31. Murphy, R. M., and Lamb, G. D. (2013). Important considerations for protein analyses using antibody based techniques: down-sizing western blotting up-sizes outcomes. J. Physiol. 591, 5823-5831. doi: 10.1113/jphysiol.2013.263251
32. Parker, L., McGuckin, T. A., and Leicht, A. S. (2014). Influence of exercise intensity on systemic oxidative stress and antioxidant capacity. Clin. Physiol. Funct. Imaging 34, 377-383. doi: 10.1111/cpf.12108
33. Pillon, N. J., Croze, M. L., Vella, R. E., Soul�re, L., Lagarde, M., and Soulage, C. O. (2012). The lipid peroxidation by-product 4-hydroxy-2-nonenal (4-hne) induces insulin resistance in skeletal muscle through both carbonyl and oxidative stress. Endocrinology 153, 2099-2111. doi: 10.1210/en.2011-1957
34. Radak, Z., Zhao, Z., Koltai, E., Ohno, H., and Atalay, M. (2013). Oxygen consumption and usage during physical exercise: the balance between oxidative stress and ros-dependent adaptive signaling. Antioxid. Redox Signal. 18, 1208-1246. doi: 10.1089/ars.2011.4498
35. Ragheb, R., Shanab, G. M., Medhat, A. M., Seoudi, D. M., Adeli, K., and Fantus, I. G. (2009). Free fatty acid-induced muscle insulin resistance and glucose uptake dysfunction: evidence for pkc activation and oxidative stress-activated signaling pathways. Biochem. Biophys. Res. Commun. 389, 211-216. doi: 10.1016/j.bbrc.2009.08.106
36. Ristow, M., Zarse, K., Oberbach, A., Kl�ting, N., Birringer, M., Kiehntopf, M., et al. (2009). Antioxidants prevent health-promoting effects of physical exercise in humans. Proc. Natl. Acad. Sci. U.S.A. 106, 8665-8670. doi: 10.1073/pnas.0903485106
37. Ropelle, E. R., Pauli, J. R., Prada, P. O., De Souza, C. T., Picardi, P. K., Faria, M. C., et al. (2006). Reversal of diet-induced insulin resistance with a single bout of exercise in the rat: The role of ptp1b and irs-1 serine phosphorylation. J. Physiol. 577, 997-1007. doi: 10.1113/jphysiol.2006.120006
38. Sandstr�m, M. E., Zhang, S. J., Bruton, J., Silva, J. P., Reid, M. B., Westerblad, H., et al. (2006). Role of reactive oxygen species in contraction-mediated glucose transport in mouse skeletal muscle. J. Physiol. 575, 251-262. doi: 10.1113/jphysiol.2006.110601
39. Schneider, C. D., Barp, J., Ribeiro, J. L., Bell�-Klein, A., and Oliveira, A. R. (2005). Oxidative stress after three different intensities of running. Can. J. Appl. Physiol. 30, 723-734. doi: 10.1139/h05-151
40. Somwar, R., Perreault, M., Kapur, S., Taha, C., Sweeney, G., Ramlal, T., et al. (2000). Activation of p38 mitogen-activated protein kinase alpha and beta by insulin and contraction in rat skeletal muscle: potential role in the stimulation of glucose transport. Diabetes 49, 1794-1800. doi: 10.2337/diabetes.49.11.1794
41. Stepto, N. K., Cassar, S., Joham, A. E., Hutchison, S. K., Harrison, C. L., Goldstein, R. F., et al. (2013). Women with polycystic ovary syndrome have intrinsic insulin resistance on euglycaemic-hyperinsulaemic clamp. Hum. Reprod. 28, 777-784. doi: 10.1093/humrep/des463
42. Tanti, J. F., and Jager, J. (2009). Cellular mechanisms of insulin resistance: role of stress-regulated serine kinases and insulin receptor substrates (irs) serine phosphorylation. Curr. Opin. Pharmacol. 9, 753-762. doi: 10.1016/j.coph.2009.07.004
43. Thong, F. S., Derave, W., Urso, B., Kiens, B., and Richter, E. A. (2003). Prior exercise increases basal and insulin-induced p38 mitogen-activated protein kinase phosphorylation in human skeletal muscle. J. Appl. Physiol. (1985) 94, 2337-2341. doi: 10.1152/japplphysiol.00036.2003
44. Tiganis, T. (2011). Reactive oxygen species and insulin resistance: the good, the bad and the ugly. Trends Pharmacol. Sci. 32, 82-89. doi: 10.1016/j.tips.2010.11.006
45. Trewin, A. J., Lundell, L. S., Perry, B. D., Patil, K. V., Chibalin, A. V., Levinger, I., et al. (2015). Effect of n-acetylcysteine infusion on exercise-induced modulation of insulin sensitivity and signaling pathways in human skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 309, E388-E397. doi: 10.1152/ajpendo.00605.2014
46. Valko, M., Leibfritz, D., Moncol, J., Cronin, M. T. D., Mazur, M., and Telser, J. (2007). Free radicals and antioxidants in normal physiological functions and human disease. Int. J. Biochem. Cell Biol. 39, 44-84. doi: 10.1016/j.biocel.2006.07.001
47. Veskoukis, A. S., Nikolaidis, M. G., Kyparos, A., and Kouretas, D. (2009). Blood reflects tissue oxidative stress depending on biomarker and tissue studied. Free Radic. Biol. Med. 47, 1371-1374. doi: 10.1016/j.freeradbiomed.2009.07.014
48. Vincent, H. K., Morgan, J. W., and Vincent, K. R. (2004). Obesity exacerbates oxidative stress levels after acute exercise. Med. Sci. Sports Exerc. 36, 772-779. doi: 10.1249/01.MSS.0000126576.53038.E9
49. Vincent, H. K., Vincent, K. R., Bourguignon, C., and Braith, R. W. (2005). Obesity and postexercise oxidative stress in older women. Med. Sci. Sports Exerc. 37, 213-219. doi: 10.1249/01.MSS.0000152705.77073.B3
50. Werner, E. D., Lee, J. S., Hansen, L., Yuan, M. S., and Shoelson, S. E. (2004). Insulin resistance due to phosphorylation of insulin receptor substrate-1 at serine 302. J. Biol. Chem. 279, 35298-35305. doi: 10.1074/jbc.M405203200