The effects of palmitic acid on nitric oxide production by rat skeletal muscle: Mechanism via superoxide and iNOS activation

Cellular Physiology and Biochemistry

Volumn 30, Issue 5, 2012, Pages 1169-1180

  Lambertucci, Rafael Herling ^a,b   Leandro, Carol Góis ^c   Vinolo, Marco Aurélio ^a   Nachbar, Renato Tadeu ^a   Dos Reis Silveira, Leonardo ^a   Hirabara, Sandro Massao ^a,b   Curi, Rui ^a   Pithon Curi, Tania Cristina ^b  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b UNIVERSIDADE CRUZEIRO DO SUL   (Brazil)

^c FEDERAL UNIVERSITY OF PERNAMBUCO   (Brazil)

Author keywords

Fatty acids; Nitric oxide synthase; Nuclear factor kappa B

Indexed keywords

4,5 DIAMINOFLUORESCEIN DIACETATE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; MACROGOL; N(G) NITROARGININE; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE; NITRITE; PALMITIC ACID; SUPEROXIDE DISMUTASE;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL TISSUE; ARTICLE; CELL VIABILITY; CONTROLLED STUDY; DRUG CYTOTOXICITY; GASTROCNEMIUS MUSCLE; GEL MOBILITY SHIFT ASSAY; MUSCLE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN EXPRESSION; QUADRICEPS FEMORIS MUSCLE; RAT; SOLEUS MUSCLE; WESTERN BLOTTING;

RATTUS;

ANIMALS; CELLS, CULTURED; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME ACTIVATION; MUSCLE, SKELETAL; NG-NITROARGININE METHYL ESTER; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; NITROARGININE; PALMITIC ACID; RATS; RATS, WISTAR; STRUCTURE-ACTIVITY RELATIONSHIP; SUPEROXIDES;

EID: 84869229267     PISSN: 10158987     EISSN: 14219778     Source Type: Journal    
DOI: 10.1159/000343307     Document Type: Article

References (58)

1. Merry TL, McConell GK: Skeletal muscle glucose uptake during exercise: A focus on reactive oxygen species and nitric oxide signaling. IUBMB Life 2009;61:479-484.
2. Hirabara SM, Silveira LR, Abdulkader FR, Alberici LC, Procopio J, Carvalho CR, Pithon-Curi TC, Curi R: Role of fatty acids in the transition from anaerobic to aerobic metabolism in skeletal muscle during exercise. Cell Biochem Funct 2006;24:475-481.
3. Ji LL: Oxidative stress during exercise: Implication of antioxidant nutrients. Free Radic Biol Med 1995;18:1079-1086.
4. Fulle S, Protasi F, Di Tano G, Pietrangelo T, Beltramin A, Boncompagni S, Vecchiet L, Fano G: The contribution of reactive oxygen species to sarcopenia and muscle ageing. Exp Gerontol 2004;39:17-24. (Pubitemid 38068255)
5. Badal S, Brown PD, Ragoobirsingh D: Nitric oxide agents impair insulin-mediated signal transduction in rat skeletal muscle. BMC Biochem 2006;7:17.
6. McGrowder D, Ragoobirsingh D, Brown P: Acute effects of exogenous nitric oxide on glucose uptake in skeletal muscle of normoglycaemic and diabetic rats. Med Sci Monit 2006;12:BR28-35. (Pubitemid 43116650)
7. Jackson MJ, Pye D, Palomero J: The production of reactive oxygen and nitrogen species by skeletal muscle. J Appl Physiol 2007;102:1664-1670. (Pubitemid 46571066)
8. Patwell DM, McArdle A, Morgan JE, Patridge TA, Jackson MJ: Release of reactive oxygen and nitrogen species from contracting skeletal muscle cells. Free Radic Biol Med 2004;37:1064-1072. (Pubitemid 39172132)
9. McCann SM, Mastronardi C, De Laurentiis A, Rettori V: The nitric oxide theory of aging revisited. Ann N Y Acad Sci 2005;1057:64-84. (Pubitemid 43211628)
10. Marletta MA, Hurshman AR, Rusche KM: Catalysis by nitric oxide synthase. Curr Opin Chem Biol 1998;2:656-663. (Pubitemid 128645724)
11. Grozdanovic Z: No message from muscle. Microsc Res Tech 2001;55:148-153. (Pubitemid 33029627)
12. Vassilakopoulos T, Govindaraju K, Parthenis D, Eidelman DH, Watanabe Y, Hussain SN: Nitric oxide production in the ventilatory muscles in response to acute resistive loading. Am J Physiol 2007;292:L1013-1022. (Pubitemid 46608248)
13. Song W, Kwak HB, Kim JH, Lawler JM: Exercise training modulates the nitric oxide synthase profile in skeletal muscle from old rats. J Gerontol A Biol Sci Med Sci 2009;64:540-549.
14. Zhou LZ, Johnson AP, Rando TA: Nf kappa b and ap-1 mediate transcriptional responses to oxidative stress in skeletal muscle cells. Free Radic Biol Med 2001;31:1405-1416. (Pubitemid 33145310)
15. Ji LL, Gomez-Cabrera MC, Vina J: Exercise and hormesis: Activation of cellular antioxidant signaling pathway. Ann N Y Acad Sci 2006;1067:425-435. (Pubitemid 43806355)
16. Hirabara SM, Silveira LR, Abdulkader F, Carvalho CR, Procopio J, Curi R: Time-dependent effects of fatty acids on skeletal muscle metabolism. J Cell Physiol 2007;210:7-15. (Pubitemid 44904696)
17. Hickson-Bick DL, Sparagna GC, Buja LM, McMillin JB: Palmitate-induced apoptosis in neonatal cardiomyocytes is not dependent on the generation of ros. Am J Physiol Heart Circ Physiol 2002;282:H656-664. (Pubitemid 34654991)
18. Richieri GV, Kleinfeld AM: Unbound free fatty acid levels in human serum. J Lipid Res 1995;36:229-240.
19. Miyasaka CK, Mendonca JR, Nishiyama A, De Souza JA, Pires De Melo M, Pithon-Curi TC, Curi R: Comparative effects of fish oil given by gavage and fish oil-enriched diet on leukocytes. Life Sci 2001;69:1739-1751. (Pubitemid 32781762)
20. Lambertucci RH, Hirabara SM, Silveira Ldos R, Levada-Pires AC, Curi R, Pithon-Curi TC: Palmitate increases superoxide production through mitochondrial electron transport chain and nadph oxidase activity in skeletal muscle cells. J Cell Physiol 2008;216:796-804.
21. Rachek LI, Musiyenko SI, Le Doux SP, Wilson GL: Palmitate induced mitochondrial deoxyribonucleic acid damage and apoptosis in l6 rat skeletal muscle cells. Endocrinology 2007;148:293-299. (Pubitemid 46021461)
22. Jensen L, Schjerling P, Hellsten Y: Regulation of vegf and bfgf mrna expression and other proliferative compounds in skeletal muscle cells. Angiogenesis 2004;7:255-267.
23. Lambertucci RH, Silveira L, Dos R, Hirabara SM, Curi R, Sweeney G, Pithon-Curi TC: Effects of moderate electrical stimulation on reactive species production by primary rat skeletal muscle cells: Cross talk between superoxide and nitric oxide production. J Cell Physiol 2012;227:2511-2518.
24. Martins De Lima T, Cury-Boaventura MF, Giannocco G, Nunes MT, Curi R: Comparative toxicity of fatty acids on a macrophage cell line (j774). Clin Sci (Lond) 2006;111:307-317. (Pubitemid 44690189)
25. Ding AH, Nathan CF, Stuehr DJ: Release of reactive nitrogen intermediates and reactive oxygen intermediates from mouse peritoneal macrophages. Comparison of activating cytokines and evidence for independent production. J Immunol 1988;141:2407-2412.
26. Kojima H, Sakurai K, Kikuchi K, Kawahara S, Kirino Y, Nagoshi H, Hirata Y, Nagano T: Development of a fluorescent indicator for nitric oxide based on the fluorescein chromophore. Chem Pharm Bull (Tokyo) 1998;46:373-375. (Pubitemid 28124233)
27. Nagata N, Momose K, Ishida Y: 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 1999;125:658-661. (Pubitemid 29192484)
28. Fink B, Laude K, McCann L, Doughan A, Harrison DG, Dikalov S: Detection of intracellular superoxide formation in endothelial cells and intact tissues using dihydroethidium and an hplc-based assay. Am J Physiol Cell Physiol 2004;287:C895-902. (Pubitemid 39238312)
29. Flohe L, Otting F: Superoxide dismutase assays. Methods Enzymol 1984;105:93-104. (Pubitemid 14165376)
30. Bradford MM: A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976;72:248-254.
31. Towbin H, Staehelin T, Gordon J: Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: Procedure and some applications. Proc Natl Acad Sci U S A 1979;76:4350-4354. (Pubitemid 9256559)
32. Boengler K, Gres P, Cabestrero A, Ruiz-Meana M, Garcia-Dorado D, Heusch G, Schulz R: Prevention of the ischemia-induced decrease in mitochondrial tom20 content by ischemic preconditioning. J Mol Cell Cardiol 2006;41:426-430. (Pubitemid 44344278)
33. Andrews NC, Faller DV: A rapid micropreparation technique for extraction of DNA-binding proteins from limiting numbers of mammalian cells. Nucleic Acids Res 1991;19:2499.
34. Hang CH, Shi JX, Tian J, Li JS, Wu W, Yin HX: Effect of systemic lps injection on cortical nf-kappab activity and inflammatory response following traumatic brain injury in rats. Brain Res 2004;1026:23-32. (Pubitemid 39336413)
35. Hamilton JA, Kamp F: How are free fatty acids transported in membranes? Is it by proteins or by free diffusion through the lipids? Diabetes 1999;48:2255-2269. (Pubitemid 30395415)
36. Kampf JP, Kleinfeld AM: Is membrane transport of ffa mediated by lipid, protein, or both? An unknown protein mediates free fatty acid transport across the adipocyte plasma membrane. Physiology (Bethesda) 2007;22:7-14.
37. Steinberg H: Regulation of lipid and lipoprotein metabolism. In: Best and taylor's physiological basis of medical practice, ed 7th. Baltimore, Williams & Wilkins, 1985.
38. Di Paola M, Lorusso M: Interaction of free fatty acids with mitochondria: Coupling, uncoupling and permeability transition. Biochim Biophys Acta 2006;1757:1330-1337. (Pubitemid 44442109)
39. Martins AR, Nachbar RT, Gorjao R, Vinolo MA, Festuccia WT, Lambertucci RH, Cury-Boaventura MF, Silveira LR, Curi R, Hirabara SM: Mechanisms underlying skeletal muscle insulin resistance induced by fatty acids: Importance of the mitochondrial function. Lipids Health Dis 2012;11:30.
40. Barbieri E, Sestili P: Reactive oxygen species in skeletal muscle signaling. J Signal Transduct 2012;2012:982794.
41. Knapp LT, Klann E: Superoxide-induced stimulation of protein kinase c via thiol modification and modulation of zinc content. J Biol Chem 2000;275:24136-24145. (Pubitemid 30624705)
42. Shim J, Karin M: The control of mrna stability in response to extracellular stimuli. Mol Cells 2002;14:323-331. (Pubitemid 41582954)
43. Martins De Lima T, Gorjao R, Hatanaka E, Cury-Boaventura MF, Portioli Silva EP, Procopio J, Curi R: Mechanisms by which fatty acids regulate leucocyte function. Clin Sci (Lond) 2007;113:65-77. (Pubitemid 47066026)
44. Brown K, Park S, Kanno T, Franzoso G, Siebenlist U: Mutual regulation of the transcriptional activator nfkappa b and its inhibitor, i kappa b-alpha. Proc Natl Acad Sci U S A 1993;90:2532-2536. (Pubitemid 23078662)
45. Ji LL, Gomez-Cabrera MC, Steinhafel N, Vina J: Acute exercise activates nuclear factor (nf)-kappab signaling pathway in rat skeletal muscle. Faseb J 2004;18:1499-1506. (Pubitemid 39336631)
46. Pahl HL: Activators and target genes of rel/nf-kappab transcription factors. Oncogene 1999;18:6853-6866.
47. Takahashi HK, Cambiaghi TD, Luchessi AD, Hirabara SM, Vinolo MA, Newsholme P, Curi R: Activation of survival and apoptotic signaling pathways in lymphocytes exposed to palmitic acid. J Cell Physiol 2012;227:339-350.
48. Jove M, Planavila A, Laguna JC, Vazquez-Carrera M: Palmitate-induced interleukin 6 production is mediated by protein kinase c and nuclear-factor kappab activation and leads to glucose transporter 4 downregulation in skeletal muscle cells. Endocrinology 2005;146:3087-3095. (Pubitemid 41002818)
49. Boden G, Lebed B, Schatz M, Homko C, Lemieux S: Effects of acute changes of plasma free fatty acids on intramyocellular fat content and insulin resistance in healthy subjects. Diabetes 2001;50:1612-1617. (Pubitemid 33639602)
50. Blaak EE: Basic disturbances in skeletal muscle fatty acid metabolism in obesity and type 2 diabetes mellitus. Proc Nutr Soc 2004;63:323-330. (Pubitemid 38787485)
51. Bartesaghi S, Ferrer-Sueta G, Peluffo G, Valez V, Zhang H, Kalyanaraman B, Radi R: Protein tyrosine nitration in hydrophilic and hydrophobic environments. Amino Acids 2007;32:501-515. (Pubitemid 46790931)
52. Radi R: Nitric oxide, oxidants, and protein tyrosine nitration. Proc Natl Acad Sci USA 2004;101:4003-4008. (Pubitemid 38405874)
53. Victor VM, Nunez C, D'Ocon P, Taylor CT, Esplugues JV, Moncada S: Regulation of oxygen distribution in tissues by endothelial nitric oxide. Circ Res 2009;104:1178-1183.
54. Moncada S, Erusalimsky JD: Does nitric oxide modulate mitochondrial energy generation and apoptosis? Nat Rev Mol Cell Biol 2002;3:214-220.
55. Giulivi C, Poderoso JJ, Boveris A: Production of nitric oxide by mitochondria. J Biol Chem 1998;273:11038-11043. (Pubitemid 28204947)
56. Navarro A, Sanchez Del Pino MJ, Gomez C, Peralta JL, Boveris A: Behavioral dysfunction, brain oxidative stress, and impaired mitochondrial electron transfer in aging mice. Am J Physiol Regul Integr Comp Physiol 2002;282:R985-992. (Pubitemid 34664549)
57. Tisdale MJ: Molecular pathways leading to cancer cachexia. Physiology (Bethesda) 2005;20:340-348. (Pubitemid 41457399)
58. + channel activity. Gastroenterology 2006;131:1228-1234. (Pubitemid 44498696)