Resveratrol, a natural antioxidant attenuates intestinal ischemia/reperfusion injury in rats

Tohoku Journal of Experimental Medicine

Volumn 218, Issue 3, 2009, Pages 251-258

  Ozkan, Orhan Veli ^a   Yuzbasioglu, Mehmet Fatih ^b   Ciralik, Harun ^b   Kurutas, Ergul Belge ^b   Yonden, Zafer ^a   Aydin, Mehmet ^a   Bulbuloglu, Ertan ^b   Semerci, Ersan ^a   Goksu, Mustafa ^b   Atli, Yalcin ^b   Bakan, Vedat ^b   Duran, Nizami ^a  

^a MUSTAFA KEMAL UNIVERSITY   (Turkey)

^b KAHRAMANMARAS SUTCU IMAM UNIVERSITY   (Turkey)

Author keywords

Antioxidants; Bacterial translocation; Histopathological evaluation; Intestinal ischemia reperfusion injury; Resveratrol

Indexed keywords

ALCOHOL; MALONALDEHYDE; MYELOPEROXIDASE; NITRIC OXIDE; RESVERATROL; SUPEROXIDE DISMUTASE; ANTIOXIDANT; NITRATE; NITRITE; PEROXIDASE; PROTEIN; SCAVENGER; STILBENE DERIVATIVE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; BACTERIAL TRANSLOCATION; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; HISTOPATHOLOGY; INTESTINE ISCHEMIA; NONHUMAN; RAT; REPERFUSION INJURY; TISSUE INJURY; WISTAR RAT; ANIMAL; DRUG EFFECT; INTESTINE; INTESTINE MUCOSA; METABOLISM; PATHOLOGY;

ANIMALS; ANTIOXIDANTS; BACTERIAL TRANSLOCATION; FEMALE; FREE RADICAL SCAVENGERS; INTESTINAL MUCOSA; INTESTINES; MALONDIALDEHYDE; NITRATES; NITRIC OXIDE; NITRITES; PEROXIDASE; PROTEINS; RATS; RATS, WISTAR; REPERFUSION INJURY; STILBENES; SUPEROXIDE DISMUTASE;

EID: 68849086743     PISSN: 00408727     EISSN: 13493329     Source Type: Journal    
DOI: 10.1620/tjem.218.251     Document Type: Article

References (49)

1. Arumugam, T.V., Shiels, I.A., Margolin, S.B., Taylor, S.M. & Brown, L. (2002a) Pirfenidone attenuates ischaemia-reperfusion injury in the rat small intestine. Clin. Exp. Pharmacol. Physiol., 29, 996-1000.
2. Arumugam, T.V., Shiels, I.A., Woodruff, T.M., Reid, R.C., Fairlie, D.P. & Taylor, S.M. (2002b) Protective effect of a new C5a receptor antagonist against ischemia-reperfusion injury in the rat small intestine. J. Surg. Res., 103, 260-267.
3. Balakrishna, S., Lomnicki, S., McAvey, K.M., Cole, R.B., Dellinger, B. & Cormier, S.A. (2009) Environmentally persistent free radicals amplify ultrafine particle mediated cellular oxidative stress and cytotoxicity. Part Fibre Toxicol., 6, 11.
4. Chen, C.F., Hsueh, C.W., Tang, T.S., Wang, D., Shen, C.Y. & Pei, J.S. (2007) Reperfusion liver injury-induced superoxide dismutase and catalase expressions and the protective effects of N-acetyl cysteine. Transplant. Proc., 39, 858-860.
5. Cortas, N.K. & Wakid, N.W. (1990) Determination of inorganic nitrate in serum and urine by a kinetic cadmium-reduction method. Clin. Chem., 36, 1440-1443.
6. de la Lastra, C.A. & Villegas, I. (2007) Resveratrol as an antioxidant and pro-oxidant agent: mechanisms and clinical implications. Biochem. Soc. Trans., 35, 1156-1160.
7. Deitch, E.A., Feketeova, E., Lu, Q., Zaets, S., Berezina, T.L., Machiedo, G.W., Hauser, C.J., Livingston, D.H. & Xu, D.Z. (2008) Resistance of the female, as opposed to the male, intestine to I/ R-mediated injury is associated with increased resistance to gut-induced distant organ injury. Shock, 29, 78-83.
8. Dokmeci, D., Inan, M., Basaran, U.N., Yalcin, O., Aydogdu, N., Turan, F.N. & Uz, Y.H., (2007) Protective effect of L-carnitine on testicular ischaemia-reperfusion injury in rats. Cell. Biochem. Funct., 25, 611-618.
9. Elmali, N., Esenkaya, I., Karadag, N., Tas, F. & Elmali, N. (2007) Effects of resveratrol on skeletal muscle in ischemia-reperfusion injury. Ulus. Travma Acil Cerrahi Derg., 13, 274-280.
10. Ergun, O., Ergun, G., Oktem, G., Selvi, N., Dogan, H., Tuncyurek, M., Saydam, G. & Erdener, A. (2007) Enteral resveratrol supplementation attenuates intestinal epithelial inducible nitric oxide synthase activity and mucosal damage in experimental necrotizing enterocolitis. J. Pediatr. Surg., 42, 1687-1694.
11. Feng, Y.H., Zhou, W.L., Wu, Q.L., Li, X.Y., Zhao, W.M. & Zou, J.P. (2002) Low dose of resveratrol enhanced immune response of mice. Acta Pharmacol. Sin., 23, 893-897.
12. Fridovich, I. (1983) Superoxide radical: an endogenous toxicant. Annu. Rev. Pharmacol. Toxicol., 23, 239-257.
13. Gehm, B.D., McAndrews, J.M., Chien, P.Y. & Jameson, J.L. (1997) Resveratrol, a polyphenolic compound found in grapes and wine, is an agonist for the estrogen receptor. Proc. Natl. Acad. Sci. USA., 94, 14138-14143.
14. Giakoustidis, D., Papageorgiou, G., Iliadis, S., Giakoustidis, A., Kostopoulou, E., Kontos, N., Botsoglou, E., Tsantilas, D., Papanikolaou, V. & Takoudas, D. (2006) The protective effect of alpha-tocopherol and GdCl3 against hepatic ischemia/reperfusion injury. Surg. Today, 36, 450-456.
15. Grisham, M.B., Hernandez, L.A. & Granger, D.N. (1986) Xanthine oxidase and neutrophil infiltration in intestinal ischemia. Am. J. Physiol., 251, G567-G574.
16. Guneli, E., Cavdar, Z., Islekel, H., Sarioglu, S., Erbayraktar, S., Kiray, M., Sokmen, S., Yilmaz, O. & Gokmen, N. (2007) Erythropoietin protects the intestine against ischemia/reperfusion injury in rats. Mol. Med., 13, 509-517.
17. Hassan-Khabbar, S., Cottart, C.H., Wendum, D., Vibert, F., Clot, J.P., Savouret, J.F., Conti, M. & Nivet-Antoine, V. (2008) Postischemic treatment by trans-resveratrol in rat liver ischemia-reperfusion: a possible strategy in liver surgery. Liver Transpl., 14, 451-459.
18. Higa, O.H., Parra, E.R., Ab'Saber, A.M., Farhat, C., Higa, R. & Capelozzi, V.L. (2007) Protective effects of ascorbic acid pretreatment in a rat model of intestinal ischemia-reperfusion injury: a histomorphometric study. Clinics, 62, 315-320.
19. Homma, H., Hoy, E., Xu, D.Z., Lu, Q., Feinman, R. & Deitch, E.A. (2005) The female intestine is more resistant than the male intestine to gut injury and inflammation when subjected to conditions associated with shock states. Am. J. Physiol. Gastrointest. Liver Physiol., 288, G466-G472.
20. Juan, M.E., Maijó, M. & Planas, J.M. (2009) Quantification of trans-resveratrol and its metabolites in rat plasma and tissues by HPLC. J. Pharm. Biomed. Anal., Apr 5. [Epub ahead of print]
21. Karabulut, A.B., Kirimlioglu, V., Kirimlioglu, H., Yilmaz, S., Isik, B. & Isikgil, O. (2006) Protective effects of resveratrol on spleen and ileum in rats subjected to ischemia-reperfusion. Transplant. Proc., 38, 375-377.
22. Klinge, C.M., Blankenship, K.A., Risinger, K.E., Bhatnagar, S., Noisin, E.L., Sumanasekera, W.K., Zhao, L., Brey, D.M. & Keynton, R.S. (2005) Resveratrol and estradiol rapidly activate MAPK signaling through estrogen receptors alpha and beta in endothelial cells. J. Biol. Chem., 280, 7460-7468.
23. Lee, M.A., McCauley, R.D., Kong, S.E. & Hall, J.C. (2001) Pretreatment with glycine reduces the severity of warm intestinal ischemic-reperfusion injury in the rat. Ann. Plast. Surg., 46, 320-326.
24. Leonard, S.S., Xia, C., Jiang, B.H., Stinefelt, B., Klandorf, H., Harris, G.K. & Shi, X. (2003) Resveratrol scavenges reactive oxygen species and effects radical-induced cellular responses. Biochem. Biophys. Res. Commun., 309, 1017-1026.
25. Lowry, O.H., Rosebrough, N.J., Farr, A.L. & Randall, R.J. (1951) Protein measurement with the Folin phenol reagent. J. Biol. Chem.,193, 265-275
26. Mallick, I.H., Yang, W., Winslet, M.C. & Seifalian, A.M. (2004) Ischemia-reperfusion injury of the intestine and protective strategies against injury. Dig. Dis. Sci., 49, 1359-1377.
27. Martin, A.R., Villegas, I., La Casa, C. & de la Lastra, C.A. (2004) Resveratrol, a polyphenol found in grapes, suppresses oxidative damage and stimulates apoptosis during early colonic inflammation in rats. Biochem. Pharmacol., 67, 1399-1410.
28. Medeiros, A.C., Chacon, D.A., Sales, V.S., Egito, E.S., Brandao-Neto, J., Pinheiro, L.A. & Carvalho, M.R. (2006) Glucan and glutamine reduce bacterial translocation in rats subjected to intestinal ischemia-reperfusion. J. Invest. Surg., 19, 39-46.
29. Mishima, S., Xu, D., Lu, Q. & Deitch, E.A. (1997) Bacterial translocation is inhibited in inducible nitric oxide synthase knockout mice after endotoxin challenge but not in a model of bacterial overgrowth. Arch. Surg., 132, 1190-1195.
30. Mojzis, J., Hviscova, K., Germanova, D., Bukovicova, D. & Mirossay, L. (2001) Protective effect of quercetin on ischemia/reperfusion-induced gastric mucosal injury in rats. Physiol. Res., 50, 501-506.
31. Munzel, T., Daiber, A., Ullrich, V. & Mulsch, A. (2005) Vascular consequences of endothelial nitric oxide synthase uncoupling for the activity and expression of the soluble guanylyl cyclase and the cGMP-dependent protein kinase. Arterioscler. Thromb. Vasc. Biol., 25, 1551-1557.
32. Offner, P.J., Moore, E.E. & Biffl, W.L. (1999) Male gender is a risk factor for major infections after surgery. Arch. Surg., 134, 935-940.
33. Ohkawa, H., Ohishi, N. & Yagi, K. (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal. Biochem., 95, 351-358.
34. Olas, B., Wachowicz, B., Bald, E. & Glowacki, R. (2004) The protective effects of resveratrol against changes in blood platelet thiols induced by platinum compounds. J. Physiol. Pharmacol., 55, 467-476.
35. Ozturk, C., Avlan, D., Cinel, I., Cinel, L., Unlu, A., Camdeviren, H., Atik, U. & Oral, U. (2002) Selenium pretreatment prevents bacterial translocation in rat intestinal ischemia/reperfusion model. Pharmacol. Res., 46, 171-175.
36. Park, P.O., Haglund, U., Bulkley, G.B. & Falt, K. (1990) The sequence of development of intestinal tissue injury after strangulation ischemia and reperfusion. Surgery, 107, 574-580.
37. Parks, D.A. & Granger, D.N. (1986) Contributions of ischemia and reperfusion to mucosal lesion formation. Am. J. Physiol., 250, G749-G753.
38. Roviezzo, F., Cuzzocrea, S., Di Lorenzo, A., Brancaleone, V., Mazzon, E., Di Paola, R., Bucci, M. & Cirino, G. (2007) Protective role of PI3-kinase-Akt-eNOS signalling pathway in intestinal injury associated with splanchnic artery occlusion shock. Br. J. Pharmacol., 151, 377-383.
39. Sayan, H., Ozacmak, V.H., Altaner, S., Aktas, R.G. & Arslan, S.O. (2008) Protective effects of L-arginine on rat terminal ileum subjected to ischemia/reperfusion. J. Pediatr. Gastroenterol. Nutr., 46, 29-35.
40. Sebai, H., Ben-Attia, M., Sani, M., Aouani, E. & Ghanem-Boughanmi, N. (2008) Protective effect of resveratrol on acute endotoxemia-induced nephrotoxicity in rat through nitric oxide independent mechanism. Free Radic. Res., 42, 913-920.
41. Sorrells, D.L., Friend, C., Koltuksuz, U., Courcoulas, A., Boyle, P., Garrett, M., Watkins, S., Rowe, M.I. & Ford, H.R. (1996) Inhibition of nitric oxide with aminoguanidine reduces bacterial translocation after endotoxin challenge in vivo. Arch. Surg., 131, 1155-1163.
42. Soylemez, S., Gurdal, H., Sepici, A. & Akar, F. (2008) The effect of long-term resveratrol treatment on relaxation to estrogen in aortae from male and female rats: role of nitric oxide and superoxide. Vascul. Pharmacol., 49, 97-105.
43. Teke, Z., Kabay, B., Aytekin, F.O., Yenisey, C., Demirkan, N.C., Sacar, M., Erdem, E. & Ozden, A. (2007) Pyrrolidine dithiocarbamate prevents 60 minutes of warm mesenteric ischemia/reperfusion injury in rats. Am. J. Surg., 194, 255-262.
44. Tsai, S.H., Lin-Shiau, S.Y. & Lin, J.K. (1999) Suppression of nitric oxide synthase and the down-regulation of the activation of NFkappaB in macrophages by resveratrol. Br. J. Pharmacol. 126, 673-680.
45. Ustundag, B., Kazez, A., Demirbag, M., Canatan, H., Halifeoglu, I. & Ozercan, I. H. (2000) Protective effect of melatonin on antioxidative system in experimental ischemia-reperfusion of rat small intestine. Cell. Physiol. Biochem., 10, 229-236.
46. Worthington, E.M. (1972) Freehold (NJ):, Worthington Biochemical Corporation, 100-101 p.
47. Yamaguchi, Y., Akizuki, E., Ichiguchi, O., Matsumura, F., Goto, M., Miyanari, N., Mori, K., Yamada, S. & Ogawa, M. (1997) Neutrophil elastase inhibitor reduces neutrophil chemoattractant production after ischemia-reperfusion in rat liver. Gastroenterol., 112, 551-560.
48. Yen, G.C., Duh, P.D. & Lin, C.W. (2003) Effects of resveratrol and 4-hexylresorcinol on hydrogen peroxide-induced oxidative DNA damage in human lymphocytes. Free Radic. Res., 37, 509-514.
49. Yoshida, Y., Shioi, T. & Izumi, T. (2007) Resveratrol ameliorates experimental autoimmune myocardilis. Circ. J., 71, 397-404.