Elucidating the role of oxidative stress in the therapeutic effect of rutin on experimental acute pancreatitis

Free Radical Research

Volumn 50, Issue 12, 2016, Pages 1350-1360

  Abreu, Fabíula Francisca ^a   Souza, Ana Carla Araújo ^a   Teixeira, Simone Aparecida ^b   Soares, Antônio Garcia ^b   Teixeira, Daiane Franco ^a   Soares, Rosilene Calazans ^a   Santana, Marilia Trindade ^a   Lauton Santos, Sandra ^a   Costa, Soraia Kátia Pereira ^b   Muscará, Marcelo Nicolas ^b   Camargo, Enilton Aparecido ^a  

^a FEDERAL UNIVERSITY OF SERGIPE   (Brazil)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

antioxidant; flavonoid; inflammation; pain; Pancreatic injury

Indexed keywords

1 CHLORO 2,4 DINITROBENZENE; 3 NITROTYROSINE; AMYLASE; ARGININE; C REACTIVE PROTEIN; CATALASE; GLUTATHIONE; GLUTATHIONE PEROXIDASE; GLUTATHIONE REDUCTASE; GLUTATHIONE TRANSFERASE; INTERLEUKIN 6; MALONALDEHYDE; MYELOPEROXIDASE; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; RUTOSIDE; SUPEROXIDE DISMUTASE; TRIACYLGLYCEROL LIPASE; ANTIOXIDANT; FLAVONOID;

ACUTE PANCREATITIS; AMYLASE BLOOD LEVEL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; CONTROLLED STUDY; DRUG EFFECT; ENZYME ACTIVITY; HISTOPATHOLOGY; HYPERALGESIA; LIPID PEROXIDATION; MALE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PANCREATIC TISSUE; TRIACYLGLYCEROL LIPASE BLOOD LEVEL; ACUTE DISEASE; ANIMAL; CHEMISTRY; PANCREAS; PANCREATITIS; PATHOLOGY;

ACUTE DISEASE; ANIMALS; ANTIOXIDANTS; FLAVONOIDS; MALE; MICE; OXIDATIVE STRESS; PANCREAS; PANCREATITIS; RUTIN;

EID: 84996879794     PISSN: 10715762     EISSN: 10292470     Source Type: Journal    
DOI: 10.1080/10715762.2016.1247494     Document Type: Article

References (61)

1. Bollen TL, van Santvoort HC, Besselink MG, van Leeuwen MS, Horvath KD, Freeny PC, Gooszen HG., Dutch Acute Pancreatitis Study Group. The Atlanta Classification of acute pancreatitis revisited. Br J Surg 2008;95:6–21.
2. Yadav D, Lowenfels AB., The epidemiology of pancreatitis and pancreatic cancer. Gastroenterology 2013;144:1252–1261.
3. Frossard J-L., Experimental evidence of obesity as a risk factor for severe acute pancreatitis. World J Gastroenterol 2009;15:5260.
4. Granger J, Remick D., Acute pancreatitis:models, markers, and mediators. Shock 2005;24:45–51.
5. Schütte K, Malfertheiner P., Markers for predicting severity and progression of acute pancreatitis. Best Pract Res Clin Gastroenterol 2008;22:75–90.
6. Pérez S, Pereda J, Sabater L, Sastre J., Redox signaling in acute pancreatitis. Redox Biol 2015;5:1–14.
7. Arjumand W, Seth A, Sultana S., Rutin attenuates cisplatin induced renal inflammation and apoptosis by reducing NFκB, TNF-α and caspase-3 expression in wistar rats. Food Chem Toxicol 2011;49:2013–2021.
8. Chvanov M, Petersen OH, Tepikin A., Free radicals and the pancreatic acinar cells:role in physiology and pathology. Philos Trans R Soc Lond, B, Biol Sci 2005;360:2273–2284.
9. Tonsi A-F., Acute pancreatitis at the beginning of the 21st century:the state of the art. World J Gastroenterol 2009;15:2945.
10. Phillip V, Steiner JM, Algül H., Early phase of acute pancreatitis:assessment and management. World J Gastrointest Pathophysiol 2014;5:158–168.
11. Carvalho KMMB, Morais TC, de Melo TS, de Castro Brito GA, de Andrade GM, Rao VS, Santos FA., The natural flavonoid quercetin ameliorates cerulein-induced acute pancreatitis in mice. Biol Pharm Bull 2010;33:1534–1539.
12. Comert B, Isik AT, Aydin S, Bozoglu E, Unal B, Deveci S, et al. Combination of allopurinol and hyperbaric oxygen therapy:a new treatment in experimental acute necrotizing pancreatitis? World J Gastroenterol 2007;13:6203.
13. de Oliveira TT, Gomes SM, Nagem TJ, Costa NMB, Secom PR., Efeito de diferentes doses de flavonóides em ratos hiperlipidêmicos. Rev Nutr 2002;15:45–51.
14. Azevedo MI, Pereira AF, Nogueira RB, Rolim FE, Brito GA, Wong DVT, et al. The antioxidant effects of the flavonoids rutin and quercetin inhibit oxaliplatin-induced chronic painful peripheral neuropathy. Mol Pain 2013;9:53.
15. Aruna R, Geetha A, Suguna P., Rutin modulates ASC expression in NLRP3 inflammasome:a study in alcohol and cerulein-induced rat model of pancreatitis. Mol Cell Biochem 2014;396:269–280.
16. Aruna R, Geetha A, Suguna P, Suganya V., Rutin rich Emblica officinalis Geart. fruit extract ameliorates inflammation in the pancreas of rats subjected to alcohol and cerulein administration. J Complement Integr Med 2014;11:9–18.
17. Dawra R, Sharif R, Phillips P, Dudeja V, Dhaulakhandi D, Saluja AK., Development of a new mouse model of acute pancreatitis induced by administration of l-arginine. Am J Physiol Gastrointest Liver Physiol 2007;292:G1009–G1018.
18. Camargo EA, Zanoni CI, Toyama MH, Muscara MN, Docherty RJ, Costa SKP., Abdominal hyperalgesia in secretory phospholipase A2-induced rat pancreatitis:distinct roles of NK1 receptors. Eur J Pain 2011;15:900–906.
19. Bradley PP, Priebat DA, Christensen RD, Rothstein G., Measurement of cutaneous inflammation:estimation of neutrophil content with an enzyme marker. J Invest Dermatol 1982;78:206–209.
20. Zhang J, Rouse RL., Histopathology and pathogenesis of caerulein-, duct ligation-, and arginine-induced acute pancreatitis in Sprague–Dawley rats and C57BL6 mice. Histol Histopathol 2014;29:1135–1152.
21. Bose R, Sutherland GR, Pinsky C., Biological and methodological implications of prostaglandin involvement in mouse brain lipid peroxidation measurements. Neurochem Res 1989;14:217–220.
22. Fossati P, Prencipe L, Berti G., Use of 3,5-dichloro-2-hydroxybenzenesulfonic acid/4-aminophenazone chromogenic system in direct enzymic assay of uric acid in serum and urine. Clin Chem 1980;26:227–231.
23. Nebot C, Moutet M, Huet P, Xu JZ, Yadan JC, Chaudiere J., Spectrophotometric assay of superoxide dismutase activity based on the activated autoxidation of a tetracyclic catechol. Anal Biochem 1993;214:442–451.
24. Ukeda H, Maeda S, Ishii T, Sawamura M., Spectrophotometric assay for superoxide dismutase based on tetrazolium salt 3’-1-(phenylamino)-carbonyl-3, 4-tetrazolium]-bis(4-methoxy-6-nitro)benzenesulfonic acid hydrate reduction by xanthine-xanthine oxidase. Anal Biochem 1997;251:206–209.
25. Paglia DE, Valentine WN., Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med 1967;70:158–169.
26. Carlberg I, Mannervik B., Purification and characterization of the flavoenzyme glutathione reductase from rat liver. J Biol Chem 1975;250:5475–5480.
27. Habig WH, Pabst MJ, Jakoby WB., Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. J Biol Chem 1974;249:7130–7139.
28. 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.
29. Sultana R, Butterfield DA., Slot-blot analysis of 3-nitrotyrosine-modified brain proteins. Meth Enzymol 2008;440:309–316.
30. Aruna R, Geetha A, Suguna P., Expression of caspase activation recruitment and pyrin domain levels of apoptosis-associated speck-like protein complex in the pancreas of rats subjected to experimental pancreatitis:influence of rutin administration. Hum Exp Toxicol 2014;33:940–948.
31. Abela JE, Carter CR., Acute pancreatitis–a review. Surg Oxf 2010;28:205–211.
32. Abdel-Raheem IT., Gastroprotective effect of rutin against indomethacin-induced ulcers in rats:gastroprotective effect of rutin in rats. Basic Clin Pharmacol Toxicol 2010;107:742–750.
33. Liu Y, Gou L, Fu X, Li S, Lan N, Yin X., Protective effect of rutin against acute gastric mucosal lesions induced by ischemia–reperfusion. Pharm Biol 2013;51:914–919.
34. Khan MM, Ahmad A, Ishrat T, Khuwaja G, Srivastawa P, Khan MB, et al. Rutin protects the neural damage induced by transient focal ischemia in rats. Brain Res 2009;1292:123–135.
35. Gong G, Qin Y, Huang W, Zhou S, Yang X, Li D., Rutin inhibits hydrogen peroxide-induced apoptosis through regulating reactive oxygen species mediated mitochondrial dysfunction pathway in human umbilical vein endothelial cells. Eur J Pharmacol 2010;628:27–35.
36. Chen J, Cai Q, Shen P, Yan R, Wang C, Yang D, et al. Netrin-1 protects against l-arginine-induced acute pancreatitis in mice. PLoS One 2012;7:e46201.
37. Bhatia M., Apoptosis of pancreatic acinar cells in acute pancreatitis:is it good or bad? J Cell Mol Med 2004;8:402–409.
38. Chen G, Xu F, Li J, Lu S., Depletion of neutrophils protects against l-arginine-induced acute pancreatitis in mice. Cell Physiol Biochem 2015;35:2111–2120.
39. Lin Z, Guo J, Xue P, Huang L, Deng L, Yang X, Xia Q., Chaiqinchengqi decoction regulates necrosis-apoptosis via regulating the release of mitochondrial cytochrome c and caspase-3 in rats with acute necrotizing pancreatitis. J Tradit Chin Med Chung Tsa Chih Ying Wen Pan Spons–China Assoc Tradit Chin Med Acad Tradit Chin Med 2014;34:178–183.
40. Winston JH, Toma H, Shenoy M, He Z-J, Zou L, Xiao S-Y, et al. Acute pancreatitis results in referred mechanical hypersensitivity and neuropeptide up-regulation that can be suppressed by the protein kinase inhibitor k252a. J Pain 2003;4:329–337.
41. Kawabata A, Matsunami M, Tsutsumi M, Ishiki T, Fukushima O, Sekiguchi F, et al. Suppression of pancreatitis-related allodynia/hyperalgesia by proteinase-activated receptor-2 in mice. Br J Pharmacol 2006;148:54–60.
42. Santana DG, Santos CA, Santos ADC, Nogueira PCL, Thomazzi SM, Estevam CS, et al. Beneficial effects of the ethanol extract of Caesalpinia pyramidalis on the inflammatory response and abdominal hyperalgesia in rats with acute pancreatitis. J Ethnopharmacol 2012;142:445–455.
43. Hernandez-Leon A, Fernández-Guasti A, González-Trujano ME., Rutin antinociception involves opioidergic mechanism and descending modulation of ventrolateral periaqueductal grey matter in rats. Eur J Pain 2016;20:274–283.
44. Leser HG, Gross V, Scheibenbogen C, Heinisch A, Salm R, Lausen M, et al. Elevation of serum interleukin-6 concentration precedes acute-phase response and reflects severity in acute pancreatitis. Gastroenterology 1991;101:782–785.
45. Sathyanarayan G, Garg PK, Prasad H, Tandon RK., Elevated level of interleukin-6 predicts organ failure and severe disease in patients with acute pancreatitis. J Gastroenterol Hepatol 2007;22:550–554.
46. Yamamoto K, Rose-John S., Therapeutic blockade of interleukin-6 in chronic inflammatory disease. Clin Pharmacol Ther 2012;91:574–576.
47. Kuo L, Hein TW., Vasomotor regulation of coronary microcirculation by oxidative stress:role of Arginase. Front Immunol 2013;4:237.
48. Babu BI, Malleo G, Genovese T, Mazzon E, Di Paola R, Crisafulli C, et al. Green tea polyphenols ameliorate pancreatic injury in cerulein-induced murine acute pancreatitis. Pancreas 2009;38:954–967.
49. Leung PS, Chan YC., Role of oxidative stress in pancreatic inflammation. Antioxid Redox Signal 2009;11:135–166.
50. Itagaki S, Oikawa S, Ogura J, Kobayashi M, Hirano T, Iseki K., Protective effects of quercetin-3-rhamnoglucoside (rutin) on ischemia–reperfusion injury in rat small intestine. Food Chem 2010;118:426–429.
51. Khan R, Khan M, Sahreen S., Protective effects of rutin against potassium bromate induced nephrotoxicity in rats. BMC Complement Altern Med 2012;12:204.
52. Kostyuk VA, Kraemer T, Sies H, Schewe T., Myeloperoxidase/nitrite-mediated lipid peroxidation of low-density lipoprotein as modulated by flavonoids. FEBS Lett 2003;537:146–150.
53. Afanas’ev IB, Dcrozhko AI, Brodskii AV, Kostyuk VA, Potapovitch AI., Chelating and free radical scavenging mechanisms of inhibitory action of rutin and quercetin in lipid peroxidation. Biochem Pharmacol 1989;38:1763–1769.
54. Poch B, Gansauge F, Rau B, Wittel U, Gansauge S, Nüssler AK, et al. The role of polymorphonuclear leukocytes and oxygen-derived free radicals in experimental acute pancreatitis:mediators of local destruction and activators of inflammation. FEBS Lett 1999;461:268–272.
55. Gow AJ, Duran D, Malcolm S, Ischiropoulos H., Effects of peroxynitrite-induced protein modifications on tyrosine phosphorylation and degradation. FEBS Lett 1996;385:63–66.
56. Hazen SL, Zhang R, Shen Z, Wu W, Podrez EA, MacPherson JC, et al. Formation of nitric oxide-derived oxidants by myeloperoxidase in monocytes:pathways for monocyte-mediated protein nitration and lipid peroxidation in vivo. Circ Res 1999;85:950–958.
57. Gaut JP, Byun J, Tran HD, Lauber WM, Carroll JA, Hotchkiss RS, et al. Myeloperoxidase produces nitrating oxidants in vivo. J Clin Invest 2002;109:1311–1319.
58. Czakó L, Takács T, Varga IS, Tiszlavicz L, Hai DQ, Hegyi P, et al. Oxidative stress in distant organs and the effects of allopurinol during experimental acute pancreatitis. IJGC 2000;27:209–216.
59. Sowjanya J, Sandhya T, Veeresh B., Ameliorating effect of eugenol on l-arginine induced acute pancreatitis and associated pulmonary complications in rats. Pharmacologia 2012;3:657–664.
60. Pandurangan AK., Modulatory influence of Green tea polyphenols on lipid peroxidation during l-arginine induced acute pancreatitis in Wistar rats. IOSR-JESTFT 2013;3:77–82.
61. Szabolcs A, Varga IS, Varga C, Berkó A, Kaszaki J, Letoha T, et al. Beneficial effect of resveratrol on cholecystokinin-induced experimental pancreatitis. Eur J Pharmacol 2006;532:187–193.