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The influence of a fish oil-enriched diet on the phospholipid fatty acid turnover in the rabbit red cell membranein vivo

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Lipids

Abstract

The influence of the polyunsaturated fatty acid (PUFA) composition of the diet on the rate of fatty acid turnover of individual phospholipids in the erythrocyte membranein vivo was studied. Following modification of the fatty acid composition of the membrane phospholipids by the use of a fish oil or a linoleic acid enriched diet, phospholipids—labelled in the unsaturated fatty acid at the 2-position of the glycerol moiety—were introduced into the membrane of freshly isolated rabbit erythrocytes. Thereafter, the labelled erythrocytes were reinjected into the bloodstream of the animal. It appears that, with the exception of 1-palmitoyl,2-linoleoyl phosphatidylcholine, all other phosphatidylcholines disappear faster from the erythrocytes of fish oil-fed rabbits than from the red cells of linoleic acid-fed rabbits. Another parameter, which possibly influences the turnover rates of PUFA containing phospholipids, can be peroxidation. An attempt was made to measure peroxidative damage of lipidsin vivo by the introduction of 1-palmitoyl,2-cis-parinaroyl phosphatidylcholine (PnPC)—a probe to measure oxidative stress—into the membrane of freshly isolated erythrocytes, in the same way as is described for the radioactive phospholipids. The data demonstrate that the fluorescent signal from the PnPC decreases at a fast rate which is independent of the dietary conditions.

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Abbreviations

ACD:

acid-citrate-dextrose

BHT:

butylhydroxy toluene

nsL-TP:

nonspecific lipid transfer protein

PC:

phosphatidylcholine

16:0,18:1PC:

1-palmitoyl,2-oleoyl-sn-glycero-3PC

16:0,18:2PC:

1-palmitoyl,2-linoleoyl-sn-glycero-3PC

18:0,20:4PC:

1-stearoyl,2-arachidonoyl-sn-glycero-3PC

PC-TP:

phosphatidylcholine specific transfer protein

PE:

phosphatidylethanolamine

16:0,20:4PE:

1-palmitoyl 1,2-arachidonoyl-sn-glycero-3PE

PnA:

parinaric acid

PnPC:

1-palmitoyl,2-cis-parinaroyl PC

PUFA:

polyunsaturated fatty acid(s)

α-TE:

R,R,R,-α-tocopherol

References

  1. Goodnight, S.H., Harris, W.S., Connor, W.E., and Illingworth, D.R. (1982) Polyunsaturated Fatty Acids, Hyperlipidemia and Thrombosis,Arteriosclerosis 2, 87–113.

    CAS  PubMed  Google Scholar 

  2. Grundy, S.M., and Denke, M.A. (1990) Dietary Influences on Serum Lipids and Lipoproteins.J. Lipid Res. 31, 1149–1172.

    CAS  PubMed  Google Scholar 

  3. Zöllner, N., and Tato, F. (1992) Fatty Acid Composition of the Diet: Impact on Serum Lipids and Atherosclerosis,Clin. Invest. 70, 968–1009.

    Google Scholar 

  4. Smith, D.L., Willis, A.L., Nguyen, N., Conner, D., Zahedi, S., and Fulks, J. (1989) Eskimo Plasma Constituents, Dihomo-γ-Linolenic Acid, Eicosapentaenoic Acid and Docosahexaenoic Acid Inhibit the Release of Atherogenic Mitogens,Lipids 24, 70–75.

    Article  CAS  PubMed  Google Scholar 

  5. Harris, W.S. (1989) Fish Oils and Plasma Lipid and Lipoprotein Metabolism in Humans: A Critical Review.J. Lipid Res. 30, 785–807.

    CAS  PubMed  Google Scholar 

  6. Cosgrove, J.P., Church, D.F., and Pryor, W.A. (1987) The Kinetics of the Autoxidation of Polyunsaturated Fatty Acids,Lipids 22, 299–304.

    Article  CAS  PubMed  Google Scholar 

  7. Halliwell, B., and Gutteridge, J.M.C. (1985)Free Radicals in Biology and Medicine, Clarendon Press, Oxford.

    Google Scholar 

  8. Koster, J.F., Biemond, P., Montfoort, A., and Stam, H. (1985) The Involvement of Free Radicals in Pathological Conditions,Life Chem. Rep. 3, 323–351.

    Google Scholar 

  9. Pryor, W.A. (1986) Oxy-Radicals and Related Species: Their Formation, Lifetimes and Reactions,Ann. Rev. Physiol. 48, 657–667.

    Article  CAS  Google Scholar 

  10. Pryor, W.A. (1984) inFree Radicals in Molecular Biology Aging and Disease (Armstrong, D., Sohal, R. S., Cutler, R.G., and Slater, T.F., eds.) pp. 13–43. Raven Press, New York.

    Google Scholar 

  11. Halliwell, B., and Gutteridge, J.M.C. (1990) Role of Free Radicals and Catalytic Metal Ions in Human Disease: An Overview,Methods Enzymol. 186, 1–85.

    CAS  PubMed  Google Scholar 

  12. Werns, S.W., Shea, M.J., and Lucchesi, B.R. (1985) Free Radicals in Ischemic Myocardial Injury,J. Free Rad. Biol. Med. 1, 103–110.

    Article  CAS  Google Scholar 

  13. Kuypers F.A., Easton, E.W., Van den Hoven, R., Wensing, T., Roelofsen, B., Op den Kamp, J.A.F., and Van Deenen, L.L.M. (1985) Survival of Rabbit and Horse Erythrocytesin vivo After Changing the Fatty Acyl Composition of Their Phosphatidylcholine.Biochim. Biophys. Acta 819, 170–178.

    Article  CAS  PubMed  Google Scholar 

  14. Van den Boom, M.A.P., Groot Wassink, M., Westerman, J., de Fouw, N.J., Roelofsen, B., Op den Kamp, J.A.F., and Van Deenen, L.L.M. (1994)In vivo Turnover of Phospholipids in Rabbit Erythrocytes,Biochim. Biophys. Acta 1215, 314–320.

    PubMed  Google Scholar 

  15. Kuypers, F.A., Van den Berg, J.J.M., Schalkwijk, C., Roelofsen, B., and Op den Kamp, J.A.F. (1987) Parinaric Acid as a Sensitive Fluorescent Probe for the Determination of Lipid Peroxidation.Biochim. Biophys. Acta 921, 266–274.

    CAS  PubMed  Google Scholar 

  16. Van den Berg, J.J.M. (1994) Effects of Oxidants and Antioxidants Evaluated Using Parinaric Acid as a Sensitive Probe for Oxidative Stress,Redox Report 1–11.

  17. Rose, H.G., and Oklander, M. (1965) Improved Procedure for the Extraction of Lipids from Human Erythrocytes,J. Lipid Res. 6, 428–431.

    CAS  PubMed  Google Scholar 

  18. Morrison, W.R., and Smith, L.M. (1964) Preparation of Fatty Acid Methyl Esters and Dimethylacetals from Lipids with Boron Fluoride-Methanol.J. Lipid Res. 5, 600–608.

    CAS  PubMed  Google Scholar 

  19. Broeckhuyse, R.M. (1969) Quantitative Two-Dimensional Thin-Layer Chromatography of Blood Phospholipids,Clin. Chim. Acta 23, 457–461.

    Article  Google Scholar 

  20. Bligh, E.G., and Dyer, W.J. (1959) A Rapid Method for Total Lipid Extraction and Purification,Can. J. Biochem. Physiol. 37, 911–917.

    CAS  PubMed  Google Scholar 

  21. Batzri, S., and Korn, E.D. (1973) Single Bilayer Liposomes Prepared Without Sonication,Biochim. Biophys. Acta 298, 1015–1019.

    Article  CAS  PubMed  Google Scholar 

  22. Kamp, H.H., and Wirtz, K.W.A. (1974) Phosphatidylcholine Exchange Protein from Beef Liver,Methods Enzymol. 32, 140–146.

    Article  CAS  PubMed  Google Scholar 

  23. Middelkoop, E., Lubin, B.H., Bevers, B.M., Op den Kamp, J.A.F., Comfurius, P., Chiu, D.T.Y., Zwaal, R.F.A., Van Deenen, L.L.M., and Roelofsen, B. (1988) Studies on Sickled Erythrocytes Provide Evidence That the Asymmetric Distribution of Phosphatidylserine in the Red Cell Membrane Is Maintained by Both ATP-Dependent Translocation and Interaction with Membrane Skeletal Proteins.Biochim. Biophys. Acta 937, 281–288.

    Article  CAS  PubMed  Google Scholar 

  24. Hously, G., Born, G.V.R., Conroy, D.M., Belin, J., and Smith, A.D. (1986) Influence of Dietary Lipids on the Effect of Chlorpromazine on Membrane Properties of Rabbit Red Cells.Proc. Royal Soc. London B. 227, 43–51.

    Article  Google Scholar 

  25. Van den Berg, J.J.M., de Fouw, N.J., Kuypers, F.A., Roelofsen, B., Houtsmuller, U.M.T., and Op den Kamp, J.A.F. (1991) Increased (n-3) Polyunsaturated Fatty Acid Content of Red Blood Cells from Fish Oil-Fed Rabbits Increases Lipid Peroxidation, But Decreases Hemolysis.Free Rad. Biol. Med. 11, 393–399.

    Article  PubMed  Google Scholar 

  26. Carman, M.A., and Beare-Rogers, J.L. (1988) Influence of Diet on (n-3) and (n-6) Fatty Acids in Monkey Erythrocytes.Lipids 23, 501–503.

    Article  CAS  PubMed  Google Scholar 

  27. Huang, Y.S., Nassar, B.A., and Horrobin, D.F. (1986) Changes of Plasma Lipids and Long-Chain n-3 and n-6 Fatty Acids in Plasma, Liver, Heart and Kidney Phospholipids of Rats Fed Variable Levels of Fish Oil With or Without Cholesterol Supplementation,Biochim. Biophys. Acta 879, 22–27.

    CAS  PubMed  Google Scholar 

  28. Rao, C.V., Zang, E., and Reddy, B.S. (1993) Effect of High Fat Corn Oil, Olive Oil and Fish Oil on Phospholipid Fatty Acid Composition in Male F344 Rats,Lipids 28, 441–447.

    Article  CAS  PubMed  Google Scholar 

  29. Popp-Snijders, C., Schouten, J.A., de Jong, E.A., and Van der Veen, E.A. (1984) Effect of Dietary Cod-Liver Oil on the Lipid Composition of Human Erythrocyte Membranes,Scan. J. Clin. Lab. Invest. 44, 39–46.

    CAS  Google Scholar 

  30. Brown, A.J., Pang, E., and Roberts, D.C.K., (1991) Erythrocyte Eicosapentaenoic Acid Versus Docosahexaenoic Acid as a Marker for Fish and Fish Oil Consumption,Am. J. Clin. Nutr. 54, 668–673.

    CAS  PubMed  Google Scholar 

  31. Renooij, W. (1977) Renewal of Erythrocyte Phospholipids, Ph.D. Thesis, University of Utrecht, The Netherlands.

    Google Scholar 

  32. Van Meer, G., and Op den Kamp, J.A.F. (1982) Transbilayer Movement of Various Phosphatidylcholine Species in Intact Human Erythrocytes.J. Cell. Biochem. 19, 193–204.

    Article  PubMed  Google Scholar 

  33. Middelkoop, E., Lubin, B.H., Op den Kamp, J.A.F., and Roelofsen, B. (1986) Flip-Flop Rates of Individual Molecular Species of Phosphatidylcholine in the Human Red Cell,Biochim. Biophys. Acta 855, 412–424.

    Google Scholar 

  34. Tilley, L., Cribier, S., Roelofsen, B., Op den Kamp, J.A.F., and Van Deenen, L.L.M. (1986) ATP-Dependent Translocation of Amino Phospholipids Across the Human Erythrocyte Membrane.FEBS Letters 194, 21–27.

    Article  CAS  PubMed  Google Scholar 

  35. Renooij, W., Van Golde, L.M.G., Zwaal, R.F.A., Roelofsen, B. and Van Deenen, L.L.M. (1974) Preferential Incorporation of Fatty Acids at the Inside of Human Erythrocyte Membranes,Biochim. Biophys. Acta 363, 287–292.

    Article  CAS  PubMed  Google Scholar 

  36. Renooij, W., Van Golde, L.M.G., Zwaal, R.F.A., and van Deenen, L.L.M. (1976) Topological Asymmetry of Phospholipid Metabolism in Rat Erythrocyte Membranes. Evidence for Flip-Flop of Lecithin,Eur. J. Biochem. 61, 53–58.

    Article  CAS  PubMed  Google Scholar 

  37. Renooij, W., and Van Golde, L.M.G. (1977) The Transposition of Molecular Classes of Phosphatidylcholine Across the Rat Erythrocyte Membrane and Their Exchange Between the Red Cell Membrane and Plasma Lipoproteins,Biochim. Biophys. Acta 470, 465–474.

    Article  CAS  PubMed  Google Scholar 

  38. Renooij, W., and Van Golde, L.M.G. (1979) Asymmetry in the Renewal of Molecular Classes of Phosphatidylcholine in the Rat Erythrocyte Membrane,Biochim. Biophys. Acta 558, 314–319.

    Article  CAS  PubMed  Google Scholar 

  39. Sklar, L.A., Hudson, B.S., and Simoni, R.D. (1975) Conjugated Polyene Fatty Acids as Membrane Probes: Preliminary Characterization,Proc. Natl. Acad. Sci. USA 72, 1649–1653.

    Article  CAS  PubMed  Google Scholar 

  40. Burton, G.W., Joyce, A., and Ingold, R.U. (1983) Is Vitamin E the Only Lipid-Soluble, Chain-Breaking Antioxidant in Human Blood Plasma and Erythrocyte Membranes?Arch. Biochem. Biophys. 221, 281–290.

    Article  CAS  PubMed  Google Scholar 

  41. Nair, P.P., Judd, J.T., Berlin, E., Taylor, P.R., Shami, S., Sainz, E., and Bhagavan, H.N. (1993) The Dietary Fish-Oil Induced Changes in the Distribution of Alpha-Tocopherol, Retinol and Beta-Carotene in Plasma Red Blood Cells and Platelets: Modulation by Vitamin E.Am. J. Clin. Nutr. 58, 98–102.

    CAS  PubMed  Google Scholar 

  42. Bjornson, L.K., Gniewkowski, C., and Kayden, H.J. (1975) Comparison of Exchange of α-Tocopherol and Free Cholesterol Between Rat Plasma Lipoprotein and Erythrocytes.J. Lipid Res. 16, 39–53.

    CAS  PubMed  Google Scholar 

  43. Burton, G.W., and Traber, M.G. (1990) Vitamin E: Antioxidant Activity, Biokinetics and Bioavailability,Ann. Rev. Nutr. 10, 357–382.

    Article  CAS  Google Scholar 

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van den Boom, M.A.P., Groot Wassink, M., Roelofsen, B. et al. The influence of a fish oil-enriched diet on the phospholipid fatty acid turnover in the rabbit red cell membranein vivo . Lipids 31, 285–293 (1996). https://doi.org/10.1007/BF02529875

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