Skip to main content
SpringerLink
Log in

The influence of dietary lipids on the composition and membrane fluidity of rat hepatocyte plasma membrane

  • Published:
Lipids

Abstract

Weanling male Wistar rats were fed for five weeks on standard rat chow (23 g fat/kg diet) or one of four synthetic diets with butterfat, coconut oil, corn oil, or fish oil as the main lipid source (100 g fat/kg diet). In all diets, 10% of the fat was provided as corn oil to prevent essential fatty acid deficiency. Significant differences were observed in the saturated, monounsaturated, and polyunsaturated fatty acid composition, and in the ratio of cholesterol to phospholipid, in the hepatocyte membranes. The fluidity of hepatocyte plasma membranes was assessed using the fluorescence recovery after photobleaching technique and steady-state fluorescence anisotropy of diphenylhexatriene. No significant differences were found in the fluidity of plasma membranes between animals on the different fat diets, despite diet-induced changes in their fatty acid composition. However, the proportion of lipid free to diffuse in the plasma membrane varied with diet, being significantly greater (P<0.05) in animals fed chow (63.7%), coconut oil (61.5%), and butterfat (57.6%) diets than in those fed the corn oil (47.3%) diet. Animals fed fish oil showed an intermediate (50.0%) proportion of lipid free to diffuse. The data support the hypothesis that dietary lipids can change both the chemical composition and lateral organization (lipid domain structure) of rat hepatocyte plasma membranes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

C/PL:

cholesterol to phospholipid

D:

lateral diffusion coefficient

DPH:

diphenylhexatriene

FRAP:

fluorescence recovery after photobleaching

HBSS:

Hank’s balanced salts solution

ODAF:

5-N-(octadecanoyl) aminofluorescein

%R:

percentage recovery

References

  1. Brenner, R.R. (1984) Effect of Unsaturated Acids on Membrane Structure and Enzyme Kinetics, Prog. Lipid Res. 23, 69–96.

    Article  PubMed  CAS  Google Scholar 

  2. Opmeer, F.A., Adolfs, M.J.P., and Bonta, I.L. (1984) Regulation of Prostaglandin E2 Receptors in vivo by Dietary Fatty Acids in Peritoneal Macrophages from Rats, J. Lipid Res. 25, 262–268.

    PubMed  CAS  Google Scholar 

  3. Hornstra, G. (1984) Regulation of Prostanoid Production by Dietary Fatty Acids, Med. Biol. 62, 261–262.

    PubMed  CAS  Google Scholar 

  4. Johnston, P.V. (1985) Dietary Fat, Eicosanoids, and Immunity, Adv. Lipid Res. 21, 103–141.

    PubMed  CAS  Google Scholar 

  5. Merrill, A.H. (1992) Ceramide: A New Lipid “Second Messenger”?, Nutr. Rev. 50, 78–90.

    Article  PubMed  CAS  Google Scholar 

  6. Mitchell, R.H., Kirk, C.J., Jones, L.M., Downes, C.P., and Creba, J.A. (1981) The Stimulation of Inositol Lipid Metabolism That Accompanies Calcium Mobilization in Stimulated Cells: Defined Characteristics and Unanswered Questions, Phillos. Trans. R. Soc. Lond. Biol. 296, 123–137.

    Google Scholar 

  7. Kinsella, J.E. (1990) Lipids, Membrane Receptors, and Enzymes: Effects of Dietary Fatty Acids, J. Parenter. Enteral Nutr. 14, 200S-217S.

    Article  CAS  Google Scholar 

  8. Criado, M., Eibl, H., and Barrantes, F.J. (1982) Effects of Lipids on Acetylcholine Receptor. Essential Need of Cholesterol for Maintenance of Agonist-Induced State Transitions in Lipid Vesicles, Biochemistry 21, 3622–3629.

    Article  PubMed  CAS  Google Scholar 

  9. Shinitzky, M., and Souroujon, M. (1979) Passive Modulation of Bloodgroup Antigens, Proc. Natl. Acad. Sci. USA 76, 4438–4440.

    Article  PubMed  CAS  Google Scholar 

  10. Mead, J.F. (1984) The Noneicosanoid Functions of the Essential Fatty Acids, J. Lipid Res. 25, 1517–1521.

    PubMed  CAS  Google Scholar 

  11. Kimelberg, H.K. (1977) The Influence of Membrane Fluidity on the Activity of Membrane-Bound Enzymes, in Cell Surface Reviews (Poste, G., and Nicolson, G.L., eds.), Vol. 3, pp. 205–293, Elsevier/North Holland Biomedical, New York.

    Google Scholar 

  12. Clandinin, M.T., Field, C.J., Hargreaves, K., Morson, L., and Zsigmond, E. (1985) Role of Diet Fat in Subcellular Structure and Function, Can. J. Physiol. Pharmacol. 63, 546–556.

    PubMed  CAS  Google Scholar 

  13. Stubbs, C.D., and Smith, A.D. (1984) The Modification of Mammalian Membrane Polyunsaturated Fatty Acid Composition in Relation to Membrane Fluidity and Function, Biochim. Biophys. Acta 779, 89–137.

    PubMed  CAS  Google Scholar 

  14. Quinn, P.J. (1981) The Fluidity of Cell Membranes and Its Regulation. Prog. Biophys. Mol. Biol. 38, 1–104.

    Article  PubMed  CAS  Google Scholar 

  15. Stubbs, C.D. (1983) Membrane Fluidity: Structure and Dynamics of Membrane Lipids, in Essays in Biochemistry (Campbell, P.N., and Marshall, R.D., eds.), Vol. 19, pp. 1–39, Academic Press, London.

    Google Scholar 

  16. Barenholz, Y. (1984) Sphingomyelin-Lecithin Balance in Membranes: Composition, Structure, and Function Relationships, in Physiology of Membrane Fluidity (Shinitzky, M., ed.), Vol. 1, pp. 131–173, CRC Press, Boca Raton.

    Google Scholar 

  17. Cooper, R.A., and Strauss, J.F. (1984) Regulation of Cell Membrane Cholesterol, in Physiology of Membrane Fluidity (Shinitzky, M., ed.), Vol. 1, pp. 73–97, CRC Press, Boca Raton.

    Google Scholar 

  18. Yeagle, P.L. (1985) Cholesterol and the Cell Membrane, Biochim. Biophys. Acta 822, 267–287.

    PubMed  CAS  Google Scholar 

  19. Shinitzky, M. (1984) Membrane Fluidity and Cellular Functions, in Physiology of Membrane Fluidity (Shinitzky, M., ed.), Vol. 1, pp. 1–51, CRC Press, Boca Raton.

    Google Scholar 

  20. McMurchie, E.J. (1988) Dietary Lipids and the Regulation of Membrane Fluidity and Function. Advances in Membrane Fluidity, in Physiological Regulation of Membrane Fluidity (Aloia, R.C., Curtain, C.C., and Gordon, L.M., eds.), pp. 189–237. Alan R. Liss, New York.

    Google Scholar 

  21. Gill, R., and Clark, W. (1980) Membrane Structure-Function Relationships in Cell-Mediated Cytolysis. I. Effect of Exogenously Incorporated Fatty Acids on Effector Cell Function in Cell-Mediated Cytolysis, J. Immunol. 125, 689–695.

    PubMed  CAS  Google Scholar 

  22. Heron, D.S., Shinitzky, M., Hershowitz, M., and Samuel, D. (1980) Lipid Fluidity Markedly Modulates the Binding of Serotonin to Mouse Brain Membranes. Proc. Natl. Acad. Sci. USA 77, 7463–7467.

    Article  PubMed  CAS  Google Scholar 

  23. Houslay, M.D. (1981) Mobile Receptor and Collision Coupling Mechanisms for the Activation of Adenylate Cyclase by Glucagon, Adv. Cyclic Nucleotide Res. 14, 111–119.

    PubMed  CAS  Google Scholar 

  24. Edwards-Webb, J.D., and Gurr, M.I. (1988) The Influence of Dietary Fats on the Chemical Composition and Physical Properties of Biological Membranes, Nutr. Res. 8, 1297–1305.

    Article  Google Scholar 

  25. Schroeder, F. (1983) Lipid Domains in Plasma Membranes from Rat Liver, Eur. J. Biochem. 132, 509–516.

    Article  PubMed  CAS  Google Scholar 

  26. Loten, E.G., and Redshaw-Loten, J.C. (1986) Preparation of Rat Liver Plasma Membranes in a High Yield, Anal. Biochem. 154, 183–185.

    Article  PubMed  CAS  Google Scholar 

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

    CAS  Google Scholar 

  28. Stähler, F., Gruber, W., and Stinshoff, K. (1977) A Practical Enzymatic Cholesterol Determination, Med. Lab. 30, 29–37.

    Google Scholar 

  29. Trinder, P. (1969) Determination of Glucose in the Blood Using Glucose Oxidase with an Alternative Oxygen Acceptor, Ann. Clin. Biochem. 6, 24–27.

    CAS  Google Scholar 

  30. Ladha, S., Mackie, A.R., and Clark, D.C. (1994) Cheek Cell Membrane Fluidity Measured by Fluorescence Recovery After Photobleaching and Steadystate Fluorescence Anisotropy, J. Memb. Biol. 142, 223–229.

    Article  CAS  Google Scholar 

  31. Schedl, H.P., Wilson, H.D., Mathur, S.N., Murthy, S., and Field, F.J. (1989) Effects of Phospholipid or Cholesterol Enrichment of Rat Intestinal Brush Border Membrane on Membrane Order and Transport of Calcium, Metabolism 38, 1164–1169.

    Article  PubMed  CAS  Google Scholar 

  32. Kuhry, J.E., Duportail, G., Bronner, C., Laustriat, G. (1985) Plasma Membrane Fluidity Measurements on Whole Living Cells by Fluorescence Anisotropy of Trimethylammoniumdiphenylhexatriene, Biochim. Biophys. Acta 845, 60–67.

    Article  PubMed  CAS  Google Scholar 

  33. Deguercy, A., Schrevel, J., Duportail, G., Laustriat, G., and Kuhry, J.G. (1986) Membrane Fluidity Changes in P. berghei-Infected Erythrocytes, Investigated with a Specific Plasma Membrane Fluorescent Probe, Biochem. Int. 12, 21–31.

    PubMed  CAS  Google Scholar 

  34. Berlin, E., Bhathena, S.J., Judd, J.T., Nair, P.P., Peters, R.C., Bhagavan, H.N., Ballard-Barbash, R., and Taylor, P.R. (1992) Effects of Omega-3 Fatty Acid and Vitamin-e Supplementation on Erythrocyte-Membrane Fluidity, Tocopherols, Insulin Binding, and Lipid-Composition in Adult Men, J. Nutr. Biochem. 3, 392–400.

    Article  CAS  Google Scholar 

  35. Popp-Snijders, C., Schouten, J.A., van Blitterswijk, W.J., and van der Veen, E.A. (1986) Changes in Membrane Lipid Composition of Human Erythrocytes After Dietary Supplementation of (n-3) Polyunsaturated Fatty Acids. Maintenance of Membrane Fluidity, Biochem. Biophys. Acta 854, 31–37.

    PubMed  CAS  Google Scholar 

  36. Wahnon, R., Cogan, U., and Mokady, S. (1992) Dietary Fish Oil Modulates the Alkaline Phosphatase Activity and Not the Fluidity of Rat Intestinal Microvillus Membrane, J. Nutr. Metab. 29, 279–288.

    Google Scholar 

  37. Charnock, J.S., McLennan, P.L., Abeywardena, M.Y., and Russell, G.R. (1985) Altered Levels of n-6/n-3 Fatty Acids in Rat Heart and Storage Fat Following Variable Dietary Intake of Linoleic Acids, Ann. Nutr. Metab. 29, 279–288.

    Article  PubMed  CAS  Google Scholar 

  38. Lippiello, P.M., Holloway, C.T., Garfield, S.A., and Holloway, P.W. (1979) The Effects of Estradiol on Stearyl-CoA Desaturase Activity and Microsomal Membrane Properties in Rooster Liver, J. Biol. Chem. 254, 2004–2009.

    PubMed  CAS  Google Scholar 

  39. Van-Blitterswijk, W.J., van der Meer, B.W., and Hilkmann, H. (1987) Quantitative Contributions of Cholesterol and the Individual Classes of Phospholipids and Their Degree of Fatty Acyl(un)saturation to Membrane Fluidity Measured by Fluorescence Polarization, Biochemistry 26, 1746–1756.

    Article  PubMed  CAS  Google Scholar 

  40. McCance and Widdowson’s: The Composition of Foods (1979) (Paul, A., Southgate, D.A.T., and Russell, J., eds.), HMSO, London.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Human Nutrition, University of Southampton, SO9 3TU, Southampton

    A. G. Clamp & R. F. Grimble

  2. Institute of Food Research, Norwich Laboratory, Norwich Research Park, Colney, NR4 7UA, Norwich, UK

    S. Ladha, D. C. Clark & E. K. Lund

Authors
  1. A. G. Clamp
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. S. Ladha
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. D. C. Clark
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. R. F. Grimble
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. E. K. Lund
    View author publications

    You can also search for this author in PubMed Google Scholar

About this article

Cite this article

Clamp, A.G., Ladha, S., Clark, D.C. et al. The influence of dietary lipids on the composition and membrane fluidity of rat hepatocyte plasma membrane. Lipids 32, 179–184 (1997). https://doi.org/10.1007/s11745-997-0022-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11745-997-0022-3

Keywords

Search

Navigation