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Dietary Monounsaturated n-3 and n-6 Long-Chain Polyunsaturated Fatty Acids Affect Cellular Antioxidant Defense System in Rats with Experimental Ulcerative Colitis Induced by Trinitrobenzene Sulfonic Acid

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Abstract

The intrarectal administration oftrinitrobenzene sulfonic acid in rats induces ulcerativecolitis, which results in histological alterations ofcolonic mucosa, severe modification of the cellularantioxidant defense system, and enhanced production ofinflammatory eicosanoids. This study evaluated theinfluence of different dietary fatty acids, ie,monounsaturated, n-3, and n-3 + n-6 polyunsaturatedfatty acids, on the recovery of the colonic mucosahistological pattern, the cellular antioxidant defensesystem of colon, and PGE2 and LTB4colonic mucosa contents in a model of ulcerative colitisinduced by intrarectal administration of trinitrobenzene sulfonicacid. Administration of dietary n-3 polyunsaturatedfatty acids led to a minimum stenosis score, a higherhistological recovery, lower colon alkaline phosphatase and gamma-glutamyltranspeptidase activities,and lower mucosal levels of PGE2 andLTB4 compared with the other two experimentalgroups. However, glutathione transferase, glutathionereductase, glutathione peroxidase, and catalase activities were lowerin the group treated with n-3 polyunsaturated fattyacids than in the groups fed with either themonounsaturated or the n-6 + n-3 polyunsaturatedenriched diet. We conclude that n-3 polyunsaturatedfatty acids can be administered to prevent inflammationin ulcerative colitis, but they cause a decrease in thecolonic antioxidant defense system, promoting oxidative injury at the site of inflammation.

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REFERENCES

  1. Riddel RH: Pathology of idiopathic inflammatory bowel disease. InInflammatory Bowel Disease. JB Kirsner, RG Shorter (eds). Philadelphia, Lea and Febiger, 1988, pp 329–350

    Google Scholar 

  2. Grisham MB, Grange r DN: Neutrophil-mediated mucosal injury: role of reactive oxyge n me tabolites. Dig Dis Sci 33(suppl):6S–15S, 1988

    Google Scholar 

  3. Samuelsson B: Leukotrienes: Mediators of immediate hypersensitivity reactions and inflammation. Science 220:568–575, 1983

    Google Scholar 

  4. Ingram LT, Coates T, Aden J, Higge ns C, Baebne r R, Boxer L: Metabolic, membrane and functional re sponses of human polymorphonuclear leukocyte s to platelet activating factor. Blood 59:1259–1266, 1982

    Google Scholar 

  5. Sharon P, Stenson WF. Enhanced synthesis of leukotriene B4 by colonic mucosa in inflammatory bowel disease. Gastroenterology 86:453–460, 1984

    Google Scholar 

  6. Wengrower D, Liakim R, Karmeli F, Razin E, Rachmile witz D: Pathogenesis of ulcerative colitis (UC): enhanced colonic formation of inositol phosphates (IP) and platelet activating factor (PAF). Gastroenterology 92:169, 1987

    Google Scholar 

  7. Kitahora T, Suzuki K, Asakura H, Yoshida T, Suematsu M, Tsuchiya M: Active oxygen species generate d by monocyte s and polymorphonuclear leukocytes in Crohn' s disease. Dig Dis Sci 33:951–955, 1988

    Google Scholar 

  8. Anton PA, Targan SR, Shanahan F: Increase d neutrophil receptors for and re sponse to the proinflammatory bacterial peptide formyl-methionyl-leucyl-phenylalanine in Crohn's disease. Gastroenterology 97:20–28, 1989

    Google Scholar 

  9. Shirabata Y, Aoki S, Takada S, Kiriyama H, Ohta K, Kami K: Oxygen derived free radical gene rating capacity of PMN in patients with ulcerative colitis. Digestion 44:163–171, 1989

    Google Scholar 

  10. Keshavarzian A, Kanofsky JR, Ibrahim CM, Doria MI: Exce ssive generation of reactive oxygen me tabolites by colonic mucosa in expe rimental colitis: Analysis using chemiluminiscence probe. FASEB J 4:761, 1990

    Google Scholar 

  11. Aruoma OI, Wasil M, Halliwell B, Hoey BM, Butler J: The scavenging of oxidants by sulphasalazine and its me tabolites. A possible contribution to their antiinflammatory effects? Biochem Pharmacol 36:3739–3742, 1987

    Google Scholar 

  12. Pacheco S, Hillier K, Smith CL: Inflammatory bowel disease: The in vitroeffects of sulphasalazine and other agents on prostaglandin synthesis by human rectal mucosa. Braz J Med Biol 20:221–230, 1987

    Google Scholar 

  13. Ligumsky M, Karmeli F, Sharon P, Zor D, Rachmilewitz D: Enhanced thromboxane A2 and prostacyclin production by cultured rectal mucosa in ulcerative colitis and its inhibition by steroids and sulphasalazine. Gastroenterology 81:444–449, 1981

    Google Scholar 

  14. Hawke y CJ, Karmeli F, Rachmile witz D: Imbalance of prostacyclin and thromboxane synthe sis in Crohn's disease. Gut 24:881–885, 1983

    Google Scholar 

  15. Lauritsen K, Laurse n LS, Bukhave K, Rask-Madsen J: The in vivoe ffects of orally administered prednisolone on prostaglandin and leukotriene production in ulcerative colitis. Gut 28:1095–1099, 1987

    Google Scholar 

  16. Pacheco S, Hillier K, Smith CL: Increased arachidonic acid leve ls in phospholipids of human colonic mucosa in inflammatory bowel disease. Clin Sci 73:361–364, 1987

    Google Scholar 

  17. Nishida T, Miwa H, Shigematsu A, Yamamoto M, Iida M, Fujishima M: Incre ased arachidonic acid composition of phospholipids in colonic mucosa from patients with active ulcerative colitis. Gut 28:1002–1007, 1987

    Google Scholar 

  18. Needleman P, Turk J, Jaschik BA, Morrison AR, Lefkowith JB: Arachidonic acid me tabolism. Annu Rev Biochem 55:69 - 101, 1986

    Google Scholar 

  19. Smith WL: The eicosanoids and their biochemical mechanisms of action. Biochem J 259:315–324, 1989

    Google Scholar 

  20. Terrano T, Salmon JA, Higgs GA, Moncada S: Eicosapentaenoic acid as a modulator of inflammation. Effect on prostaglandin and leukotrie ne synthe sis. Biochem Pharmacol 35:779–785, 1986

    Google Scholar 

  21. Lugea A, Videla S, Vilaseca J, Guarner F: Antiulcerogenic and antiinflammatory actions of fatty acids on the gastrointestinal tract. Prostaglandins, Leukot Essent Fatty Acids 43:135–140, 1991

    Google Scholar 

  22. Vilaseca J, Salas A, Guarner F, Rodriguez R, Martínez M, Malagelada JR: Dietary fish oil reduces progre ssion of chronic inflammatory lesions in a rat mode l of granulomatous colitis. Gut 31:539–544, 1990

    Google Scholar 

  23. Hillier K, Jewell R, Dorre ll L, Smith CL: Incorporation of fatty acids from fish oil and olive oil into colonic mucosal lipids and effects upon eicosanoid synthe sis in inflammatory bowel disease. Gut 32:1151–1155, 1991

    Google Scholar 

  24. Mourelle M, Guarner F, Malagelada JA: Polyunsaturated phosphatidylcholine prevents stricture formation in a rat model of colitis. Gastroenterology 110:1093–1097, 1996

    Google Scholar 

  25. Suarez A, Faus MJ, Gil A. Dietary supplementation with long-chain polyunsaturated fatty acids increases susceptibility of weanling rat tissue lipids to in vitro lipid peroxidation. Nutr Biochem 7:252–260, 1996

    Google Scholar 

  26. Periago JL, De-Lucchi C, Gil A, Suarez MD, Pita ML: Lipid composition of liver microsomes in rats fed a high monounsaturated fatty acid diet. Biochim Biophys Acta 962:66–72, 1988

    Google Scholar 

  27. Morris GP, Beck PL, Herridge MS, Depew WT, Szewczuk MR, Wallace JL: Hapten-induced models of chronic inflammation and ulceration in the rat colon. Gastroenterology 96:795–803, 1989

    Google Scholar 

  28. Grisham MB, Benon JN, Nen Gragne r D: Assessment of leukocyte involvement during ischemia and reperfussion of intestine. Methods Enzymol 186:729–741, 1990

    Google Scholar 

  29. Kelly RW, Graham BJM, O'Sullivan MJ: Prostaglandin extraction procedure. Prostaglandins Leukotr Essent Fatty Acids 37:187–204, 1989

    Google Scholar 

  30. Powell WS: Solid phase extraction for LTB4. Methods Enzymol 86:467–477, 1982

    Google Scholar 

  31. Habig WH, Pabst MJ, Jakoby WB: Glutathione-S-transferases, the first enzymatic step in me rcapturic acid formation. J Biol Chem 249:7130–7139, 1984

    Google Scholar 

  32. Carlberg I, Mannervick B: Glutathione reductase. Methods Enzymol 113:484–495, 1985

    Google Scholar 

  33. Flohe L, Günzler WA: Assays for glutathione peroxidase. Methods Enzymol 105:114–121, 1984

    Google Scholar 

  34. Paoletti F, Mocali A: Determination of superoxide dismutase activity by pure ly chemical system based on NAD(P)H oxidation. Methods Enzymol 186:209–221, 1990

    Google Scholar 

  35. Anderson ME: Determination of glutathione and glutathione disulfide in biological samples. Methods Enzymol 113:548–554, 1985

    Google Scholar 

  36. Cohen G, Dembie c D, Marcus J: Measurement of catalase activity in tissue extracts. Anal Biochem 34:30–38, 1970

    Google Scholar 

  37. Dixon WJ, Brown MB, Enge lman L, Jennrich RI: BMDP Statistical Software Manual. University of California Press, Berkeley, California, 1990

    Google Scholar 

  38. Grange r DN: Role of xanthine oxidase and granulocytes in ischemia-reperfusion injury. Am J Physiol 255:H1269–H1275, 1988

    Google Scholar 

  39. Seidman E, Leleiko N, Ament M, Be rman W, Caplan D, Shutphen J: Nutritional issues in pedriatic inflammatory bowel disease. J Pediatr Gastroenterol Nutr 12(4):424–438, 1991

    Google Scholar 

  40. Janowitz HD: Extrainte stinal manifestations of ileitis and colitis. Pract Gastroenterol 1:11, 1977

    Google Scholar 

  41. Kirschne r BS: Growth and development in chronic inflammatory bowel disease. Acta Pediatr Scand 366:98–104, 1990

    Google Scholar 

  42. Higgs GA, Moncada S, Vane JR: Eicosanoids in inflammation. Ann Clin Res 16:287–299, 1984

    Google Scholar 

  43. Terano T, Salmon JA, Moncada S: Biosynthesis and biological activity of leukotriene B5. Prostaglandins 27:217–232, 1985

    Google Scholar 

  44. Ikehata A, Hiwatashi N, Kinouchi Y, Yamazaki H: Effect of intravenously infused eicosapentaenoic acid on the leukotriene generation in patients with active Crohn's disease. Am J Clin Nutr 56:938–942, 1992

    Google Scholar 

  45. Rampton DS, Sladen GE: Relationship between rectal mucosal prostaglandin production and water and ele ctrolyte transport in ulcerative colitis. Dige stion 217:1255–1256, 1984

    Google Scholar 

  46. Segal AW, Dorling J, Coade S: Oxidative stress and mye loperoxidase. J Cell Biol 85:42–59, 1980

    Google Scholar 

  47. Cameron JB, Grant D, Wallace JL: Disruption of colonic ale ctrolite transport in experime ntal colitis. Am Physiol Soc 00:G622–G630, 1995

    Google Scholar 

  48. Boughton-Smith NK, Wallace JL: Temporal relationship between arachidonic acid metabolism and myeloperoxidase activity in a rat model of Crohn's disease. Gastroenterology 88:1332, 1993

    Google Scholar 

  49. Hertevig E, Nilson Å, Seidegard J: The expression of glutathione transferase m in patients with inflammatory bowel disease. Carcinogenesis 11:33–36, 1990

    Google Scholar 

  50. Lobell A, López-Ruíz A, Peinado J, López-Barea J: Glutathione reductase directly mediates the stimulation of yeast glucose-6-phosphate de hydroge nase by GSSG. Biochem J 249:293, 1988

    Google Scholar 

  51. López-Barea J, Bárcena JA: Redox control of glutathione and thioredoxin reductase s. InPlasma Membrane Oxidoreductases in Control of Animal and Plant Growth. FL Crane, (eds). Plenum Press, New York, 1988, p 349

    Google Scholar 

  52. Michelson AM, Jadot G, Puget K: Mechanisms of antiinflammatory effect of superoxide dismutase. InThe Biological Role of Reactive Oxygen Species in Skin. O Hayashu, S Imamura, Y Miyachi, (eds). Tokyo, Unive rsity of Tokyo Press, 1987, pp 199–210

    Google Scholar 

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Authors
  1. N. Nieto
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  2. M. I. Fernandez
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  3. M. I. Torres
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  4. A. Rios
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  5. M. D. Suarez
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  6. A. Gil
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Nieto, N., Fernandez, M.I., Torres, M.I. et al. Dietary Monounsaturated n-3 and n-6 Long-Chain Polyunsaturated Fatty Acids Affect Cellular Antioxidant Defense System in Rats with Experimental Ulcerative Colitis Induced by Trinitrobenzene Sulfonic Acid. Dig Dis Sci 43, 2676–2687 (1998). https://doi.org/10.1023/A:1026655311878

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