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Dietary fat source and cholesterol interactions alter plasma lipids and tissue susceptibility to oxidation in spontaneously hypertensive (SHR) and normotensive Wistar Kyoto (WKY) rats

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Abstract

Due to the potential for dietary fat source to alter plasma lipids and tissue antioxidant status, we hypothesized that blends of saturated, n-6 and n-3 fats with cholesterol would affect LDL and tissue susceptibility to in vitro oxidation. The effects of dietary fat blends of butter (B), beef tallow (T), soybean oil (SBO) or menhaden oil (MO) and cholesterol on systolic blood pressure (SBP), plasma lipoproteins and tissue susceptibility to glutathione (GSH) depletion and lipid peroxidation (TBARS) were examined in spontaneously hypertensive (SHR) and Wistar Kyoto (WKY) rats. SBP in SHRs was higher (p < 0.001) than in WKYs at 13-weeks of age but was not altered by dietary fat or cholesterol. LDL- and HDL-cholesterol were greater (p < 0.001) in WKY than SHR. LDL-cholesterol and (VLDL7- + LDL-cholesterol)/HDL-cholesterol ratios were reduced in MO vs. B, T and SBO groups. HDL-cholesterol levels tended to be lower and greater in B and MO groups, respectively vs. T and SBO groups. Initial LDL fluorescence was greater (p < 0.001) in high- vs. low-cholesterol groups. The change in LDL fluorescence was reduced (p < 0.001) in high-cholesterol groups, and MO vs. B, T and SBO rats. MO fed rats had reduced (p < 0.001) RBC, heart and liver GSH depletion and reduced (p < 0.01) tissue TBARS and RBC MDA production. In summary, a moderate level of dietary MO did not increase tissue and LDL in vitro oxidizability in SHR and WKY rats. High dietary cholesterol exhibited a protective effect against in vitro oxidation of LDL and selected tissues.

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References

  1. Krauss RM, Deckelbaum RJ, Ernst N, Fisher E, Howard BV, Knopp RH, Kotchen T, Lichtenstein AH, McGill HC, Pearson TA, Prewitt TE, Stone NJ, Van Horn L, Weinberg R: Dietary guidelines for healthy American adults - a statement for health professionals from the nutrition committee, American Heart Association. Circulation 94: 1795–1800, 1996

    Google Scholar 

  2. Jones PH, Kubow S: Lipid sterols and their metabolites. In J.A. Shils, J.A. Olson, M. Shike, A.C. Ross (eds). Modern Nutrition in Health and Disease. Lippincott Williams and Wilkins, Baltimore, 1999, pp 78–88

    Google Scholar 

  3. Juurlink BHJ: Management of oxidative stress in the CNS: The many roles of glutathione. Neurotox Res 1: 119–140, 1999

    Google Scholar 

  4. Yuan YV, Kitts DD: Endogenous antioxidants: Role of antioxidant enzymes in biological systems. In: F. Shahidi (ed). Natural Antioxidants: Chemistry, Health Effects, and Applications. AOCS Press, Illinois, 1996, pp 258–270

    Google Scholar 

  5. Ibrahim W, Lee US, Yeh CC, Szabo J, Bruckner G, Chow CK: Oxidative stress and antioxidant status in mouse liver: Effects of dietary lipid, vitamin E and iron. J Nutr 127: 1401–1406, 1997

    Google Scholar 

  6. L'Abbé MR, Trick KD, Beare-Rogers JL: Dietary (n-3) fatty acids affect rat heart, liver and aorta protective enzyme activities and lipid peroxidation. J Nutr 121: 1331–1340, 1991

    Google Scholar 

  7. Nardini M, D'Aquino M, Tomassi G, Gentili V, Di Felice M, Scaccini C: Dietary fish oil enhances plasma and LDL oxidative modification in rats. J Nutr Biochem 6: 474–480, 1995

    Google Scholar 

  8. Hau MF, Smelt AMH, Bindels AJGH, Sijbrands EJG, Van der Laarse A, Onkenhout W, Van Duyvenvoorde W, Princen HMG: Effects of fish oil on oxidation resistance of VLDL in hypertriglyceridemic patients. Arterioscler Thromb Vasc Biol 16: 1197–1202, 1996

    Google Scholar 

  9. Palozza P, Sgarlata E, Luberto C, Piccioni E, Anti M, Marra G, Armelao F, Franceschelli P, Bartoli, GM: n-3 Fatty acids induce oxidative modifications in human erythrocytes depending on dose and duration of dietary supplementation. Am J Clin Nutr 64: 297–304, 1996

    Google Scholar 

  10. Brude IR, Drevon C, Hjermann I, Seljeflot I, Lund-Katz S, Saarem K, Sandstad B, Solvol K, Halvorsen B, Anesen H, Nenseter MS: Peroxidation of LDL from combined-hyperlipidemic male smokers supplied with omega-3 fatty acids and antioxidants. Arterio Thromb Vasc Biol 17: 2576–2588, 1997

    Google Scholar 

  11. Frei B, Gaziano JM: Content of antioxidants, preformed lipid hydroperoxides, and cholesterol as predictors of the susceptibility of human LDL to metal ion-dependent and-independent oxidation. J Lipid Res 34: 2135–2145, 1993

    Google Scholar 

  12. Lasch J, Schönfelder U, Walke M, Zellmer S, Beckert D: Oxidative damage of human skin lipids - dependence of lipid peroxidation on sterol concentration. Biochim Biophys Acta 1349: 171–181, 1997

    Google Scholar 

  13. Girao H, Mota C, Pereira P: Cholesterol may act as an antioxidant in lens membranes. Curr Eye Res 18: 448–454, 1999

    Google Scholar 

  14. Smith LL: Another cholesterol hypothesis: Cholesterol as antioxidant. Free Rad Biol Med 11: 47–61, 1991

    Google Scholar 

  15. Mosinger BJ: Higher cholesterol in human LDL is associated with the increase of oxidation susceptibility and the decrease of antioxidant defence: Experimental and simulation data. Biochim Biophys Acta 1453: 180–184, 1999

    Google Scholar 

  16. Mosinger BJ: Copper-induced and photosensitive oxidation of serum low-density lipoprotein. The relation of cholesterol level and interspecies differences. Biochim Biophys Acta 1270: 73–80, 1995

    Google Scholar 

  17. Özdemirler G, Öztezcan S, Toker G, Uysal M: Peroxidation status of erythrocytes and apolipoprotein B containing lipoproteins in hypercholesterolemic subjects. Int J Vit Nutr Res 67: 130–133, 1997

    Google Scholar 

  18. Yuan YV, Kitts DD, Godin DV: Influence of dietary cholesterol and fat source on atherosclerosis in the Japanese quail (Coturnix japonica). Br J Nutr 78: 993–1014, 1997

    Google Scholar 

  19. Kitts DD, Yuan YV, Godin DV: Plasma and lipoprotein lipid composition and hepatic antioxidant status in spontaneously hypertensive (SHR) and normotensive (WKY) rats. Can J Physiol Pharmacol 76: 202–209, 1998

    Google Scholar 

  20. Yuan YV, Kitts DD, Godin DV: Heart and red blood cell antioxidant status and plasma lipid levels in the spontaneously hypertensive (SHR) and normotensive Wistar Kyoto (WKY) rat. Can J Physiol Pharmacol 74: 290–297, 1996

    Google Scholar 

  21. Yuan YV, Kitts DD, Godin DV: Variations in dietary fats and cholesterol intake modify antioxidant status of SHR and WKY rats. J Nutr 128: 1620–1630, 1998

    Google Scholar 

  22. Canadian Council on Animal Care: In: E.D. Olfert, B.M. Cross, A.A. McWilliam (eds). Guide to the Care and Use of Experimental Animals, vol. 1, 2nd edn. Canadian Council on Animal Care, Ottawa, Ontario, 1993

    Google Scholar 

  23. Kitts DD, Yuan YV, Nagasawa T, Moriyama Y: Effect of casein, casein phosphopeptides and calcium intake on ileal 45Ca disappearance and temporal systolic blood pressure in spontaneously hypertensive rats. Br J Nutr 68: 765–781, 1992

    Google Scholar 

  24. Siedel J, Hagele EO, Ziegenhorn J, Wahlefeld AW: Reagent for the enzymatic determination of serum cholesterol with improved lipolytic efficiency. Clin Chem 29: 1075–1080, 1983

    Google Scholar 

  25. Ziegenhorn J: Improved method for enzymatic determination of serum triglycerides. Clin Chem 21: 1627–1629, 1975

    Google Scholar 

  26. Takayama M, Itoh S, Nagasaki T, Tanimizu I: A new enzymatic method for determination of serum choline-containing phospholipids. Clin Chim Acta 79: 93–98, 1977

    Google Scholar 

  27. Folch J, Lees M, Sloane-Stanley GH: A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226: 497–509, 1957

    Google Scholar 

  28. Terpstra AHM, Woodward CJH, Sanchez-Muniz FJ: Improved techniques for the separation of serum lipoproteins by density gradient ultracentrifugation: Visualization by prestaining and rapid separation of serum lipoproteins from small volumes of serum. Anal Biochem 111: 149–157, 1981

    Google Scholar 

  29. Cominacini L, Garbin U, Davoli A, Micciolo R, Bosello O, Gaviraghi G, Scuro LA, Pastorino AM: A simple test for predisposition to LDL oxidation based on the fluorescence development during copper-catalyzed oxidative modification. J Lipid Res 32: 349–358, 1991

    Google Scholar 

  30. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ: Protein measurement with the Folin phenol reagent. J Biol Chem 193: 265–275, 1951

    Google Scholar 

  31. Capel ID: Factors affecting antioxidant defense potential. In: C.K. Chow (ed). Cellular Antioxidant Defence Mechanisms. CRC Press, Boca Raton, Florida, 1988, pp 191–215

    Google Scholar 

  32. Suzuki H, Swei A, Zweifach BW, Schmid-Schönbein GW: In vivo evidence for microvascular oxidative stress in spontaneously hypertensive rats: Hydroethidine microfluorography. Hypertension 25: 1083–1089, 1995

    Google Scholar 

  33. Ratnayake WMN, L'Abbé MR, Mueller R, Hayward S, Plouffe L, Hollywood R, Trick K: Vegetable oils high in phytosterols make erythrocytes less deformable and shorten the life span of stroke-prone spontaneously hypertensive rats. J Nutr 130: 1166–1178, 2000

    Google Scholar 

  34. Yamori Y, Nara Y, Horie R, Ooshima A: Abnormal membrane characteristics of erythrocytes in rat models and men with predisposition to stroke. Clin Exp Hypertens 2: 1009–1021, 1980

    Google Scholar 

  35. Chabanel A, Schacter D, Chien S: Increased rigidity of red blood cell membrane in young spontaneously hypertensive rats. Hypertension 10: 603–607, 1987

    Google Scholar 

  36. Cooper RA, Archer EC, Wiley JS, Shattil SJ: Modification of red cell membrane structure by cholesterol rich lipid dispersions. J Clin Invest 55: 115, 1975

    Google Scholar 

  37. Iritani N, Fukuda E, Nara Y, Yamori Y: Lipid metabolism in spontaneously hypertensive rats (SHR). Atherosclerosis 28: 217–222, 1977

    Google Scholar 

  38. Jain SK: The neonatal erythrocyte and its oxidative susceptibility. Seminars in Hematol 26: 286–300, 1989

    Google Scholar 

  39. Yamori Y, Horie R, Ohtaka M, Nara Y, Fukase M: Effect of hypercholesterolaemic diet on the incidence of cerebrovascular and myocardial lesions in spontaneously hypertensive rats (SHR). Clin Exp Pharmacol Physiol 3(suppl): 205–208, 1976

    Google Scholar 

  40. Yuan YV: Dietary Lipids and In Vivo Antioxidant Status in Atherosclerosis Resistant (Rat) and Sensitive (Quail) Animals. University of British Columbia, Vancouver, Canada, 1995

    Google Scholar 

  41. Godin DV, Garnett ME: Species-related variations in tissue antioxidant status-II. Differences in susceptibility to oxidative challenge. Comp Biochem Physiol 103B: 743–748, 1992

    Google Scholar 

  42. Godin DV, Wohaieb SA, Garnett ME, Goumeniouk AD: Antioxidant enzyme alterations in experimental and clinical diabetes. Mol Cell Biochem 84: 223–231, 1988

    Google Scholar 

  43. Jain SK, McVie R, Duett J, Herbst JJ: Erythrocyte membrane lipid peroxidation and glycosylated haemoglobin in diabetes. Diabetes 38: 1539–1543, 1989

    Google Scholar 

  44. Bulur H, Özdemirler G, Öz B, Toker G, Öztürk M, Uysal M: High cholesterol diet supplemented with sunflower seed oil but not olive oil stimulates lipid peroxidation in plasma, liver, and aorta of rats. J Nutr Biochem 6: 547–550, 1995

    Google Scholar 

  45. Simopoulos AP: ω-3 fatty acids in the prevention-management of cardiovascular disease. Can J Physiol Pharmacol 75: 234–239, 1997

    Google Scholar 

  46. Rustan AC, Hustvedt BE, Drevon CA: Dietary supplemention of very long-chain n-3 fatty acids decreases whole body lipid utilization in the rat. J Lipid Res 34: 1299–1309, 1993

    Google Scholar 

  47. Fernandez ML, Lin ECK, McNamara DJ: Differential effects of saturated fatty acids on low density lipoprotein metabolism in guinea pig. J Lipid Res 33: 1833–1842, 1992

    Google Scholar 

  48. Karanja N, Phanouvong T, McCarron DA: Blood pressure in spontaneously hypertensive rats fed butterfat, corn oil, or fish oil. Hypertension 14: 674–679, 1989

    Google Scholar 

  49. Steinbrecher UP, Lougheed M: Scavenger receptor-independent stimulation of cholesterol esterification in macrophages by low density lipoprotein extracted from human aortic intima. Arterio Thromb 12: 608–625, 1992

    Google Scholar 

  50. Palinksi W, Rosenfeld ME, Ylä-Herttuala S, Gurtner GC, Socher SS, Butler SW, Parthasarathy S, Carew TE, Steinberg D, Witztum JL: Low density lipoprotein undergoes oxidative modification in vivo. Proc Natl Acad Sci USA 86: 1372–1376, 1989

    Google Scholar 

  51. Gutteridge JMC: The membrane effects of vitamin E, cholesterol and their acetates on peroxidative susceptibility. Res Commun Chem Pathol Pharmacol 22: 563–572, 1978

    Google Scholar 

  52. Cominacini L, Garbin U, Cenci B, Davoli A, Pasini C, Ratti E, Garviraghi G, Lo Cascio V, Pastorino AM: Predisposition to LDL oxidation during copper-catalyzed oxidative modification and its relation to α-tocopherol content in humans. Clin Chim Acta 204: 57–68, 1991

    Google Scholar 

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Yuan, Y.V., Kitts, D.D. Dietary fat source and cholesterol interactions alter plasma lipids and tissue susceptibility to oxidation in spontaneously hypertensive (SHR) and normotensive Wistar Kyoto (WKY) rats. Mol Cell Biochem 232, 33–47 (2002). https://doi.org/10.1023/A:1014837131439

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