ISSN: 2375-379X
Health Sciences Research  
Manuscript Information
Nitrosative Stress in Skeletal Muscle of Diabetic Rats Submitted to Aerobic Exercise
Health Sciences Research
Vol.4 , No. 6, Publication Date: Oct. 17, 2017, Page: 57-63
616 Views Since October 17, 2017, 286 Downloads Since Oct. 17, 2017

Deyse Yorgos Lima, Translational Medicine, Universidade Federal de Sao Paulo, Sao Paulo, Brazil.


Adelson Marçal Rodrigues, Translational Medicine, Universidade Federal de Sao Paulo, Sao Paulo, Brazil.


Giovana Rita Punaro, Nephrology Division, Universidade Federal de Sao Paulo, Sao Paulo, Brazil.


Margaret Gori Mouro, Translational Medicine, Universidade Federal de Sao Paulo, Sao Paulo, Brazil; Nephrology Division, Universidade Federal de Sao Paulo, Sao Paulo, Brazil.


Elisa Mieko Suemitsu Higa, Translational Medicine, Universidade Federal de Sao Paulo, Sao Paulo, Brazil; Nephrology Division, Universidade Federal de Sao Paulo, Sao Paulo, Brazil.


The aim of this study was to assess the nitrosative stress in muscle tissue of diabetic rats submitted to aerobic training. Diabetes mellitus was induced by streptozotocin in male adult Wistar rats. The animals were submitted to aerobic training on treadmill and after 8 weeks, the gastrocnemius was removed for analysis. Data are shown as mean ±SEM; statistical analysis by One-Way ANOVA, with significance at p<0.05. DM+SE when compared with CTL+SE showed a reduction of body weight followed by other changes as increased chow and water intake, diuresis, glycemia and TBARS in the muscle. There was a significant improvement in all metabolic parameters in the trained diabetic animals when compared to the untrained; moderate exercise in diabetic animals reduced significantly the lipoperoxidation in the muscle. There was also an increase of superoxide anion and antioxidant defenses; this defense neutralized the action of anion, shown by reduction of the nitrotyrosine levels. Therefore, the results show that moderate exercise promotes benefits to the skeletal muscle, reducing the diabetic complications i.e., the oxidative stress, the glutathionylation and the nitrosative stress. It is suggested, that the aerobic training can be an adjuvant treatment, which could enhance the life quality of diabetic patients.


Diabetes, Gastrocnemius, Glutathionylation, Nitrosative/Oxidative Stress


A. Chawla, R. Chawla, S. Jaggi, Microvasular and macrovascular complications in diabetes mellitus: Distinct or continuum? Indian J Endocr Metab 20 (2016) 546-51.


S. K. Powers, J. Duarte, A. N. Kavazis, E. E. Talbert, Reactive oxygen species are signalling molecules for skeletal muscle adaptation, Exp Physiol 95 (2010) 1-9.


S. Tangvarasittichai Oxidative stress, insulin resistance, dyslipidemia and type 2 diabetes mellitus. World J. Diabetes 6 (2015) 456-480.


J. Calles-Escandon, M. Cipolla, Diabetes and endothelial dysfunction: a clinical perspective, Endocr Rev 22 (2001) 36-52.


D. S. Bredt, S. H. Snyder, Nitric oxide: a physiologic messenger molecule, Annu Rev Biochem 63 (1994) 175-95.


Halim MA, Gillberg L, Boghus S, Sundbom M, Karlbom U, Webb DL, Hellstm PM. Nitric oxide regulation of migrating motor complex: randomized trial of N (G)-monomethyl-L-arginine effects in relation to muscarinic and serotonergic receptor blockade. Acta Physiol (Oxf) 215. (2015) 105-118.


S. L. Maiocchi, J. C. Morris, M. D. Rees, S. R. Thomas. Regulation of the nitric oxide oxidase activity of myeloperoxidase by pharmacological agents. Biochemical Pharmacology, 135 (2017) 90-115.


Y. Zhao, P. M. Vanhoutte, S. W. S. Leung. Vascular nitric oxide: Beyond eNOS. Journal of Pharmacological Sciences. 129 (2015) 83-94.


A. Katz. Role of reactive oxygen species in regulation of glucose transport in skeletal muscle during exercise. J Physiol. 594 (2016) 2787–2794.


N. Jessen, L. J. Goodyear, Contraction signaling to glucose transport in skeletal muscle, J Appl Physiol (1985) 99 (2005) 330-7.


B. Chance, H. Sies, A. Boveris, Hydroperoxide metabolism in mammalian organs, Physiol Rev 59 (1979) 527-605.


M. Zargari, O. Sedighi. Influence of hemodialysis on lipid peroxidation, enzymatic and non-enzymatic antioxidant capacity in chronic renal failure patients. Nephro-Urology Monthly. 7 (2015) e28526.


S. Y. Park, Y. S. Kwak. Impact of aerobic and anaerobic exercise training on oxidative stress and antioxidant defense in athletes. J. Exerc. Rehabil. 12 (2016) 113–117.


vb M. Valko, D. Leibfritz, J. Moncol, M. T. Cronin, M. Mazur, J. Telser, Free radicals and antioxidants in normal physiological functions and human disease, Int J Biochem Cell Biol 39 (2007) 44-84.


A. M. Rodrigues, C. T. Bergamaschi, R. C. Araujo, M. G. Mouro, T. S. Rosa, E. M. Higa, Effects of training and nitric oxide on diabetic nephropathy progression in type I diabetic rats, Exp Biol Med (Maywood) 236 (2011) 1180-7.


A. Akbarzadeh, D. Norouzian, M. R. Mehrabi, S. Jamshidi, A. Farhangi, A. A. Verdi, S. M. Mofidian, B. L. Rad, Induction of diabetes by Streptozotocin in rats, Indian J Clin Biochem 22 (2007) 60-4.


A. M. Rodrigues, C. T. Bergamaschi, M. J. Fernandes, E. J. Paredes-Gamero, M. V. Curi, A. T. Ferreira, S. R. Araujo, G. R. Punaro, F. R. Maciel, G. B. Nogueira, E. M. Higa, P2x (7) receptor in the kidneys of diabetic rats submitted to aerobic training or to N-acetylcysteine supplementation, PLoS One 9 (2014) e97452.


J. Stocks, J. M. Gutteridge, R. J. Sharp, T. L. Dormandy, Assay using brain homogenate for measuring the antioxidant activity of biological fluids, Clin Sci Mol Med 47 (1974) 215-22.


H. S. Choi, J. W. Kim, Y. N. Cha, C. Kim, A quantitative nitroblue tetrazolium assay for determining intracellular superoxide anion production in phagocytic cells, J Immunoassay Immunochem 27 (2006) 31-44.


S. Archer, Measurement of nitric oxide in biological models, Faseb J 7 (1993) 349-60.


G. K. McConell, S. J. Bradley, T. J. Stephens, B. J. Canny, B. A. Kingwell, R. S. Lee-Young, Skeletal muscle nNOS mu protein content is increased by exercise training in humans, Am J Physiol Regul Integr Comp Physiol 293 (2007) R821-8.


P. Bjornstad, J. Snell-Bergeon, K. Nadeau, D. Maahs. Insulin sensitivity and complications in type 1 diabetes: new insights. World J Diabetes. (2015).


E. A. Richter, M. Hargreaves, Exercise, GLUT4, and skeletal muscle glucose uptake, Physiol Rev 93 (2013) 993-1017.


B. Halliwell, J. M. Gutteridge, Role of free radicals and catalytic metal ions in human disease: an overview, Methods Enzymol 186 (1990) 1-85.


M. Pittaluga, A. Sgadari, I. Dimauro, B. Tavazzi, P. Parisi, D. Caporossi. Physical Exercise and Redox Balance in Type 2 Diabetics: Effects of Moderate Training on Biomarkers of Oxidative Stress and DNA Damage Evaluated through Comet Assay. 2015 (2015) 7.


G. Q. Chen, C. Y. Mou, Y. Q. Yang, S. Wang, Z. W. Zhao, Exercise training has beneficial anti-atrophy effects by inhibiting oxidative stress-induced MuRF1 upregulation in rats with diabetes, Life Sci 89 (2011) 44-9.


M. J. Gomes, P. F. Martinez, L. U. Pagan, R. L. Damatto, M. D. M. Cezar, A. R. R. Lima, K. Okoshi, M. P. Okoshi. Skeletal muscle aging: influence of oxidative stress and physical exercise. Oncotarget. 8 (2017) 20428–20440.


A. S. Veskoukis, M. G. Nikolaidis, A. Kyparos, D. Kouretas, Blood reflects tissue oxidative stress depending on biomarker and tissue studied, Free Radic Biol Med 47 (2009) 1371-4.


A. Aguilo, P. Tauler, M. Pilar Guix, G. Villa, A. Cordova, J. A. Tur, A. Pons, Effect of exercise intensity and training on antioxidants and cholesterol profile in cyclists, J Nutr Biochem 14 (2003) 319-25.


C. Villanueva, R. D. Kross, Antioxidant-induced stress, Int J Mol Sci 13 (2012) 2091-109.


S. K. Powers, E. E. Talbert, P. J. Adhihetty, Reactive oxygen and nitrogen species as intracellular signals in skeletal muscle, J Physiol 589 (2011) 2129-38.


D. P. Jones, Redefining oxidative stress, Antioxid Redox Signal 8 (2006) 1865-79.


J. S. Beckman, W. H. Koppenol, Nitric oxide, superoxide, and peroxynitrite: the good, the bad, and ugly, Am J Physiol 271 (1996) C1424-37.


V. Adams, H. Jiang, J. Yu, S. Mobius-Winkler, E. Fiehn, A. Linke, C. Weigl, G. Schuler, R. Hambrecht, Apoptosis in skeletal myocytes of patients with chronic heart failure is associated with exercise intolerance, J Am Coll Cardiol 33 (1999) 959-65.


M. Suwa, H. Nakano, Z. Radak, S. Kumagai. Effects of nitric oxide synthase inhibition on fiber-type composition, mitochondrial biogenesis, and SIRT1 expression in rat skeletal muscle. J. Sport. Sci. Med. 14 (2015) 548–555.


M. G. Nikolaidis, A. Kyparos, I. S. Vrabas, Cell redox homeostasis: reading Conti et al. data from a blood-centric perspective, Med Sci Sports Exerc 44 (2012) 190; author reply 191.


K. L. Hamilton, S. K. Powers, T. Sugiura, S. Kim, S. Lennon, N. Tumer, J. L. Mehta, Short-term exercise training can improve myocardial tolerance to I/R without elevation in heat shock proteins, Am J Physiol Heart Circ Physiol 281 (2001) H1346-52.


P. Maher, Redox control of neural function: background, mechanisms, and significance, Antioxid Redox Signal 8 (2006) 1941-70.

  Join Us
  Join as Reviewer
  Join Editorial Board