Effects of moderate electrical stimulation on reactive species production by primary rat skeletal muscle cells: Cross talk between superoxide and nitric oxide production

Journal of Cellular Physiology

Volumn 227, Issue 6, 2012, Pages 2511-2518

  Lambertucci, Rafael Herling ^a,b   dos Reis Silveira, Leonardo ^c   Hirabara, Sandro Massao ^a   Curi, Rui ^c   Sweeney, Gary ^b   Pithon Curi, Tania Cristina ^a  

^a UNIVERSIDADE CRUZEIRO DO SUL   (Brazil)

^b YORK UNIVERSITY   (Canada)

^c UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

4,5 DIAMINOFLUORESCEIN DIACETATE; CYTOCHROME C; HYDROETHIDINE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; NITRIC OXIDE; NITRITE; REACTIVE OXYGEN METABOLITE; SUPEROXIDE; XANTHINE OXIDASE INHIBITOR;

ANIMAL CELL; ARTICLE; CELL CULTURE; ELECTROSTIMULATION; FATIGUE; GLUCOSE METABOLISM; MUSCLE CONTRACTION; MUSCLE FORCE; NONHUMAN; PRIORITY JOURNAL; RAT; SKELETAL MUSCLE;

ANIMALS; CELLS, CULTURED; CYTOCHROMES C; ELECTRIC STIMULATION; ENZYME INHIBITORS; ETHIDIUM; FLUORESCEIN; FREE RADICAL SCAVENGERS; MITOCHONDRIA, MUSCLE; MUSCLE CONTRACTION; MUSCLE FIBERS, SKELETAL; NF-KAPPA B; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; NITRITES; OXIDATION-REDUCTION; OXIDATIVE STRESS; PRIMARY CELL CULTURE; RATS; RATS, WISTAR; SIGNAL TRANSDUCTION; SUPEROXIDES; TIME FACTORS; XANTHINE; XANTHINE OXIDASE;

RATTUS;

EID: 84857481124     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.22989     Document Type: Article

References (65)

1. Allen RG, Tresini M. 2000. Oxidative stress and gene regulation. Free Radic Biol Med 28:463-499.
2. Andrews NC, Faller DV. 1991. A rapid micropreparation technique for extraction of DNA-binding proteins from limiting numbers of mammalian cells. Nucleic Acids Res 19:2499.
3. Boengler K, Gres P, Cabestrero A, Ruiz-Meana M, Garcia-Dorado D, Heusch G, Schulz R. 2006. Prevention of the ischemia-induced decrease in mitochondrial Tom20 content by ischemic preconditioning. J Mol Cell Cardiol 41:426-430.
4. Borges F, Fernandes E, Roleira F. 2002. Progress towards the discovery of xanthine oxidase inhibitors. Curr Med Chem 9:195-217.
5. Catani MV, Savini I, Duranti G, Caporossi D, Ceci R, Sabatini S, Avigliano L. 2004. Nuclear factor kappaB and activating protein 1 are involved in differentiation-related resistance to oxidative stress in skeletal muscle cells. Free Radic Biol Med 37:1024-1036.
6. Cross AR, Jones OT. 1986. The effect of the inhibitor diphenylene iodonium on the superoxide-generating system of neutrophils. Specific labelling of a component polypeptide of the oxidase. Biochem J 237:111-116.
7. Dallaire P, Bellmann K, Laplante M, Gelinas S, Centeno-Baez C, Penfornis P, Peyot ML, Latour MG, Lamontagne J, Trujillo ME, Scherer PE, Prentki M, Deshaies Y, Marette A. 2008. Obese mice lacking inducible nitric oxide synthase are sensitized to the metabolic actions of peroxisome proliferator-activated receptor-gamma agonism. Diabetes 57:1999-2011.
8. Ding AH, Nathan CF, Stuehr DJ. 1988. Release of reactive nitrogen intermediates and reactive oxygen intermediates from mouse peritoneal macrophages. Comparison of activating cytokines and evidence for independent production. J Immunol 141:2407-2412.
9. 2+ stimulates ERK, CREB, early genes. J Cell Physiol 209:379-388.
10. Fink B, Laude K, McCann L, Doughan A, Harrison DG, Dikalov S. 2004. Detection of intracellular superoxide formation in endothelial cells and intact tissues using dihydroethidium and an HPLC-based assay. Am J Physiol 287:C895-C902.
11. Flohe L, Otting F. 1984. Superoxide dismutase assays. Methods Enzymol 105:93-104.
12. Galkin A, Brandt U. 2005. Superoxide radical formation by pure complex I (NADH:ubiquinone oxidoreductase) from Yarrowia lipolytica. J Biol Chem 280:30129-30135.
13. Gomez-Cabrera MC, Pallardo FV, Sastre J, Vina J, Garcia-del-Moral L. 2003. Allopurinol and markers of muscle damage among participants in the Tour de France. JAMA 289:2503-2504.
14. Gomez-Cabrera MC, Borras C, Pallardo FV, Sastre J, Ji LL, Vina J. 2005. Decreasing xanthine oxidase-mediated oxidative stress prevents useful cellular adaptations to exercise in rats. J Physiol 567:113-120.
15. Gomez-Cabrera MC, Domenech E, Vina J. 2008. Moderate exercise is an antioxidant: Upregulation of antioxidant genes by training. Free Radic Biol Med 44:126-131.
16. Gomez-Cabrera MC, Close GL, Kayani A, McArdle A, Vina J, Jackson MJ. 2010. Effect of xanthine oxidase-generated extracellular superoxide on skeletal muscle force generation. Am J Physiol Regul Integr Comp Physiol 298:R2-R8.
17. Grozdanovic Z. 2001. NO message from muscle. Microsc Res Tech 55:148-153.
18. Guhring H, Tegeder I, Lotsch J, Pahl A, Werner U, Reeh PW, Rehse K, Brune K, Geisslinger G. 2001. Role of nitric oxide in zymosan induced paw inflammation and thermal hyperalgesia. Inflamm Res 50:83-88.
19. Hang CH, Shi JX, Tian J, Li JS, Wu W, Yin HX. 2004. Effect of systemic LPS injection on cortical NF-kappaB activity and inflammatory response following traumatic brain injury in rats. Brain Res 1026:23-32.
20. Hellsten Y, Frandsen U. 1997. Adenosine formation in contracting primary rat skeletal muscle cells and endothelial cells in culture. J Physiol 504:695-704.
21. Hirabara SM, Silveira LR, Alberici LC, Leandro CV, Lambertucci RH, Polimeno GC, Cury Boaventura MF, Procopio J, Vercesi AE, Curi R. 2006. Acute effect of fatty acids on metabolism and mitochondrial coupling in skeletal muscle. Biochim Biophys Acta 1757:57-66.
22. Holland PC, Clark MG, Bloxham DP, Lardy HA. 1973. Mechanism of action of the hypoglycemic agent diphenyleneiodonium. J Biol Chem 248:6050-6056.
23. Hollander J, Fiebig R, Gore M, Ookawara T, Ohno H, Ji LL. 2001. Superoxide dismutase gene expression is activated by a single bout of exercise in rat skeletal muscle. Pflugers Arch 442:426-434.
24. Jackson MJ. 2005. Reactive oxygen species and redox-regulation of skeletal muscle adaptations to exercise. Philos Trans R Soc Lond B Biol Sci 360:2285-2291.
25. Jackson MJ. 2008a. Free radicals generated by contracting muscle: By-products of metabolism or key regulators of muscle function? Free Radic Biol Med 44:132-141.
26. Jackson MJ. 2008b. Redox regulation of skeletal muscle. IUBMB Life 60:497-501.
27. Jackson MJ. 2009. Redox regulation of adaptive responses in skeletal muscle to contractile activity. Free Radic Biol Med 47:1267-1275.
28. Jackson MJ, Pye D, Palomero J. 2007. The production of reactive oxygen and nitrogen species by skeletal muscle. J Appl Physiol 102:1664-1670.
29. Javesghani D, Magder SA, Barreiro E, Quinn MT, Hussain SN. 2002. Molecular characterization of a superoxide-generating NAD(P)H oxidase in the ventilatory muscles. Am J Respir Crit Care Med 165:412-418.
30. Jensen L, Schjerling P, Hellsten Y. 2004. Regulation of VEGF and bFGF mRNA expression and other proliferative compounds in skeletal muscle cells. Angiogenesis 7:255-267.
31. Ji LL, Gomez-Cabrera MC, Steinhafel N, Vina J. 2004. Acute exercise activates nuclear factor (NF)-kappaB signaling pathway in rat skeletal muscle. FASEB J 18:1499-1506.
32. Ji LL, Gomez-Cabrera MC, Vina J. 2006. Exercise and hormesis: Activation of cellular antioxidant signaling pathway. Ann NY Acad Sci 1067:425-435.
33. Khassaf M, McArdle A, Esanu C, Vasilaki A, McArdle F, Griffiths RD, Brodie DA, Jackson MJ. 2003. Effect of vitamin C supplements on antioxidant defence and stress proteins in human lymphocytes and skeletal muscle. J Physiol 549:645-652.
34. Kojima H, Sakurai K, Kikuchi K, Kawahara S, Kirino Y, Nagoshi H, Hirata Y, Nagano T. 1998. Development of a fluorescent indicator for nitric oxide based on the fluorescein chromophore. Chem Pharm Bull 46:373-375.
35. Kua CH. 2006. Uncoupling the relationship between fatty acids and longevity. IUBMB Life 58:153-155.
36. Lambertucci RH, Hirabara SM, Silveira Ldos R, Levada-Pires AC, Curi R, Pithon-Curi TC. 2008. Palmitate increases superoxide production through mitochondrial electron transport chain and NADPH oxidase activity in skeletal muscle cells. J Cell Physiol 216:796-804.
37. Lee JS, Zhang Y, Ro JY. 2009. Involvement of neuronal, inducible and endothelial nitric oxide synthases in capsaicin-induced muscle hypersensitivity. Eur J Pain 13:924-928.
38. Li Y, Trush MA. 1998. Diphenyleneiodonium, an NAD(P)H oxidase inhibitor, also potently inhibits mitochondrial reactive oxygen species production. Biochem Biophys Res Commun 253:295-299.
39. Majander A, Finel M, Wikstrom M. 1994. Diphenyleneiodonium inhibits reduction of iron-sulfur clusters in the mitochondrial NADH-ubiquinone oxidoreductase (Complex I). J Biol Chem 269:21037-21042.
40. Marletta MA, Hurshman AR, Rusche KM. 1998. Catalysis by nitric oxide synthase. Curr Opin Chem Biol 2:656-663.
41. McArdle A, Jackson MJ. 2000. Exercise, oxidative stress and ageing. J Anat 197:539-541.
42. McCann SM, Mastronardi C, de Laurentiis A, Rettori V. 2005. The nitric oxide theory of aging revisited. Ann NY Acad Sci 1057:64-84.
43. McCord JM, Fridovich I. 1969. Superoxide dismutase. An enzymic function for erythrocuprein (hemocuprein). J Biol Chem 244:6049-6055.
44. Merry TL, McConell GK. 2009. Skeletal muscle glucose uptake during exercise: A focus on reactive oxygen species and nitric oxide signaling. IUBMB Life 61:479-484.
45. Muller JM, Rupec RA, Baeuerle PA. 1997. Study of gene regulation by NF-kappa B and AP-1 in response to reactive oxygen intermediates. Methods 11:301-312.
46. Muller FL, Liu Y, Van Remmen H. 2004. Complex III releases superoxide to both sides of the inner mitochondrial membrane. J Biol Chem 279:49064-49073.
47. Nagata N, Momose K, Ishida Y. 1999. Inhibitory effects of catecholamines and anti-oxidants on the fluorescence reaction of 4, 5-diaminofluorescein, DAF-2, a novel indicator of nitric oxide. J Biochem 125:658-661.
48. Otton R, Carvalho CR, Mendonca JR, Curi R. 2002. Low proliferation capacity of lymphocytes from alloxan-diabetic rats: Involvement of high glucose and tyrosine phosphorylation of Shc and IRS-1. Life Sci 71:2759-2771.
49. Pattwell DM, McArdle A, Morgan JE, Patridge TA, Jackson MJ. 2004. Release of reactive oxygen and nitrogen species from contracting skeletal muscle cells. Free Radic Biol Med 37:1064-1072.
50. Patwell DM, McArdle A, Morgan JE, Patridge TA, Jackson MJ. 2004. Release of reactive oxygen and nitrogen species from contracting skeletal muscle cells. Free Radic Biol Med 37:1064-1072.
51. Pilon G, Charbonneau A, White PJ, Dallaire P, Perreault M, Kapur S, Marette A. 2010. Endotoxin mediated-iNOS induction causes insulin resistance via ONOO induced tyrosine nitration of IRS-1 in skeletal muscle. PLoS One 5:e15912.
52. Ragan CI, Bloxham DP. 1977. Specific labelling of a constituent polypeptide of bovine heart mitochondrial reduced nicotinamide-adenine dinucleotide-ubiquinone reductase by the inhibitor diphenyleneiodonium. Biochem J 163:605-615.
53. Rand MJ, Li CG. 1993. The inhibition of nitric oxide-mediated relaxations in rat aorta and anococcygeus muscle by diphenylene iodonium. Clin Exp Pharmacol Physiol 20:141-148.
54. Rattan SI. 2006. Theories of biological aging: Genes, proteins, and free radicals. Free Radic Res 40:1230-1238.
55. Reid MB, Durham WJ. 2002. Generation of reactive oxygen and nitrogen species in contracting skeletal muscle: Potential impact on aging. Ann NY Acad Sci 959:108-116.
56. Saborido A, Naudi A, Portero-Otin M, Pamplona R, Megias A. 2011. Stanozolol treatment decreases the mitochondrial ROS generation and oxidative stress induced by acute exercise in rat skeletal muscle. J Appl Physiol 110:661-669.
57. Sandstrom ME, Zhang SJ, Bruton J, Silva JP, Reid MB, Westerblad H, Katz A. 2006. Role of reactive oxygen species in contraction-mediated glucose transport in mouse skeletal muscle. J Physiol 575:251-262.
58. Sauer H, Sharifpanah F, Hatry M, Steffen P, Bartsch C, Heller R, Padmasekar M, Howaldt HP, Bein G, Wartenberg M. 2011. NOS inhibition synchronizes calcium oscillations in human adipose tissue-derived mesenchymal stem cells by increasing gap-junctional coupling. J Cell Physiol 226:1642-1650.
59. Silveira LR, Pereira-Da-Silva L, Juel C, Hellsten Y. 2003. Formation of hydrogen peroxide and nitric oxide in rat skeletal muscle cells during contractions. Free Radic Biol Med 35:455-464.
60. Skulachev VP. 1998. Uncoupling: New approaches to an old problem of bioenergetics. Biochim Biophys Acta 1363:100-124.
61. Stofan DA, Callahan LA, Di MA, Nethery DE, Supinski GS. 2000. Modulation of release of reactive oxygen species by the contracting diaphragm. Am J Respir Crit Care Med 161:891-898.
62. Truglio JJ, Theis K, Leimkuhler S, Rappa R, Rajagopalan KV, Kisker C. 2002. Crystal structures of the active and alloxanthine-inhibited forms of xanthine dehydrogenase from Rhodobacter capsulatus. Structure 10:115-125.
63. Vina J, Gomez-Cabrera MC, Lloret A, Marquez R, Minana JB, Pallardo FV, Sastre J. 2000. Free radicals in exhaustive physical exercise: Mechanism of production, and protection by antioxidants. IUBMB Life 50:271-277.
64. Wei YH, Lee HC. 2002. Oxidative stress, mitochondrial DNA mutation, and impairment of antioxidant enzymes in aging. Exp Biol Med (Maywood) 227:671-682.
65. Zhou LZ, Johnson AP, Rando TA. 2001. NF kappa B and AP-1 mediate transcriptional responses to oxidative stress in skeletal muscle cells. Free Radic Biol Med 31:1405-1416.