Skip to main content
Log in

Dietary methionine level affects linoleic acid metabolism through phosphatidylethanolamine N-methylation in rats

  • Article
  • Published:
Lipids

Abstract

The effects of dietary methionine level on the profiles of fatty acids and phospholipids and on the plasma cholesterol concentration were investigated to confirm whether the methionine content of dietary proteins is one of the major factors that cause differential effects on lipid metabolism. The effect of dietary supplementation with eritadenine, which is shown to be a potent inhibitor of phosphatidylethanolamine (PE) N-methylation, was also investigated. Rats were fed six diets containing casein (100 g/kg) and amino acid mixture (86.4 g/kg) differing in methionine content (2.5, 4.5, and 7.5 g/kg) and without or with eritadenine supplementation (30 mg/kg) for 14 d. The ratio of arachidonic to linoleic acid of liver microsomal and plasma phosphatidylcholine (PC) was significantly increased as the methionine level of diet was elevated, indicating that dietary methionine stimulates the metabolism of linoleic acid. The PC/PE ratio of liver microsomes and the plasma cholesterol concentration were also increased by dietary methionine. These effects of methionine were completely abolished by eritadenine supplementation The S-adenosylmethionine concentration in the liver reflected the methionine level of diet. These results support the idea that the differential effects of dietary proteins on lipid metabolism might be ascribed, at least in part, to their different methionine contents, and that methionine might exert its effects through alteration of PE N-methylation.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

GLC:

gas-liquid chromatography

HDL:

high density lipoprotein

HPLC:

high-performance liquid chromatography

LDL:

low density lipoprotein

PC:

phosphatidylcholine

PE:

phosphatidylethanolamine

SAH:

S-adenosylhomocysteine

SAM:

S-adenosylmethionine

TLC:

thin-layer chromatography

VLDL:

very low density lipoprotein

References

  1. Kritchevsky, D. (1993) Dietary Protein and Experimental Atherosclerosis, Ann. NY Acad. Sci. 676, 180–187.

    PubMed  CAS  Google Scholar 

  2. Sirtori, C.R., Even, R., and Lovati, M.R. (1993) Soybean Protein Diet and Plasma Cholesterol: From Therapy to Molecular Mechanism, Ann. NY Acad. Sci. 676, 188–201.

    PubMed  CAS  Google Scholar 

  3. Sugano, M., and Koba, K. (1993) Dietary Protein and Lipid Metabolism: A Multifunctional Effect, Ann. NY Acad. Sci. 676, 215–222.

    PubMed  CAS  Google Scholar 

  4. Carroll, K.K., and Kurowska, E.M. (1995) Soy Consumption and Cholesterol Reduction: Review of Animal and Human Studies, J. Nutr. 125, 594S-597S.

    PubMed  CAS  Google Scholar 

  5. Huang, Y.-S., Cunnane, S.C., and Horrobin, D.F. (1986) Effect of Different Dietary Proteins on Plasma and Liver Fatty Acid Composition in Growing Rats, Proc. Soc. Exp. Biol. Med. 181, 399–403.

    PubMed  CAS  Google Scholar 

  6. Sugano, M., Ishida, T., and Koba, K. (1988) Protein-Fat Interaction on Serum cholesterol Level, Fatty Acid Desaturation and Eicosanoid Production in Rats, J. Nutr. 118, 548–554.

    PubMed  CAS  Google Scholar 

  7. Sugiyama, K., Kanamori, H., Akachi, T., and Yamakawa, A. (1996) Amino Acid Composition of Dietary Proteins Affects Plasma Cholesterol Concentration Through Alteration of Hepatic Phospholipid Metabolism in Rats Fed a Cholesterol-Free Diet, J. Nutr. Biochem. 7, 40–48.

    Article  CAS  Google Scholar 

  8. Sugiyama, K., Yamakawa, A., Kumazawa, A., and Saeki, S. (1997) Methionine Content of Dietary Proteins Affects the Molecular Species Composition of Plasma Phosphatidylcholine in Rats Fed a Cholesterol-Free Diet, J. Nutr. 127, 600–607.

    PubMed  CAS  Google Scholar 

  9. Sugiyama, K., Akachi, T., and Yamakawa, A. (1995) Eritadenine-Induced Alteration of Hepatic Phospholipid Metabolism in Relation to Its Hypocholesterolemic Action in Rats, J. Nutr. Biochem. 6, 80–87.

    Article  CAS  Google Scholar 

  10. Sugiyama, K., Yamakawa, A., and Saeki, S. (1997) Correlation of Suppressed Linoleic Acid Metabolism with the Hypocholesterolemic Action of Eritadenine in Rats, Lipids, 32, 859–866.

    PubMed  CAS  Google Scholar 

  11. Nguyen, L.B., Shefer, G., Ness, G., Tanaka, R.D., Packin, V., Thomas, P., Shore, V., and Batta, A. (1990) Purification of Cholesterol 7α-Hydroxylase from Human and Rat Liver and Production of Inhibiting Polyclonal Antibodies, J. Biol. Chem. 265, 4541–4546.

    PubMed  CAS  Google Scholar 

  12. Folch, J., Lees, M., and Sloane-Stanley, G.H. (1957) A Simple Method for the Isolation and Purification of Total Lipids from Animal Tissues, J. Biol. Chem. 226, 497–509.

    PubMed  CAS  Google Scholar 

  13. Zak, B. (1957) Simple Rapid Microtechnic for Serum Total Cholesterol, Am. J. Clin. Pathol. 27, 583–588.

    PubMed  CAS  Google Scholar 

  14. Fletcher, M.J. (1968) A Colorimetric Method for Estimating Serum Triglycerides, Clin. Chim. Acta 22, 393–397.

    Article  PubMed  CAS  Google Scholar 

  15. Bartlett, G.R. (1959) Phosphorus Assay in Column Chromatography, J. Biol. Chem. 234, 466–468.

    PubMed  CAS  Google Scholar 

  16. Blank, M.L., Robinson, M., Fitzgerald, V., and Snyder, F. (1984) Novel Quantitative Method for Determination of Molecular Species of Phospholipids and Diglycerides, J. Chromatogr. 298, 473–482.

    Article  PubMed  CAS  Google Scholar 

  17. Sugiyama, K., and Yamakawa, A. (1996) Dietary Eritadenine-Induced Alteration of Molecular Species Composition of Phospholipids in Rats, Lipids, 31, 399–404.

    Article  PubMed  CAS  Google Scholar 

  18. Cook, R.J., Horne, D.W., and Wagner, C. (1989) Effect of Dietary Methyl Group Deficiency on One-Carbon Metabolism in Rats, J. Nutr. 119, 612–617.

    PubMed  CAS  Google Scholar 

  19. Lowry, O.H., Rosebrough, N.J., Farr, A.L., and Randall, R.J. (1951) Protein Measurement with the Folin Phenol Reagent, J. Biol. Chem. 193, 265–275.

    PubMed  CAS  Google Scholar 

  20. Duncan, D.B. (1957) Multiple Range Tests for Correlated and Heteroscedastic Means, Biometrics 13, 164–176.

    Article  Google Scholar 

  21. Ikeda, I., Wakamatsu, K., Inayoshi, A., Imaizumi, K., Sugano, M., and Yazawa, K. (1994) α-Linolenic, Eicosapentaenoic and Docosahexaenoic Acids Affect Lipid Metabolism Differentially in Rats, J. Nutr. 124, 1898–1906.

    PubMed  CAS  Google Scholar 

  22. Choy, Y.-S., Goto, S., Ikeda, I., and Sugano, M. (1989) Interaction of Dietary Proteins, Cholesterol and Age on Lipid Metabolism of the Rat, Br. J. Nutr. 61, 531–543.

    Article  Google Scholar 

  23. Voss, A., Reinhart, M., Sankarappa, S., and Sprecher, H.J. (1991) The Metabolism of 7,10,13,16,19-Docosapentaenoic Acid to 4,7,10,13,16,19-Docosahexaenoic Acid in Rat Liver Is Independent of a 4-Desaturase, J. Biol. Chem. 266, 19995–20000.

    PubMed  CAS  Google Scholar 

  24. Leikin, A.I., and Brenner, R.R. (1987) Cholesterol-Induced Microsomal Changes Modulate Desaturase Activities, Biochim. Biophys. Acta 922, 294–303.

    PubMed  CAS  Google Scholar 

  25. Leikin, A.I., and Brenner, R.R. (1988) In vitro Cholesterol Removal from Liver Microsomes Induces Changes in Fatty Acid Desaturase Activities, Biochim. Biophys. Acta 963, 311–319.

    PubMed  CAS  Google Scholar 

  26. Leikin, A.I., and Brenner, R.R. (1992) In vivo Phospholipid Modification Induces Changes in Microsomal Δ5-Desaturase Activity, Biochim. Biophys. Acta 1165, 189–193.

    PubMed  CAS  Google Scholar 

  27. She, Q., Hayakawa, T., and Tsuge, H. (1994) Effect of Vitamin B6 Deficiency on Linoleic Acid Desaturation in the Arachidonic Acid Biosynthesis of Rat Liver Microsomes, Biosci. Biotechnol. Biochem. 58, 459–463.

    Article  CAS  Google Scholar 

  28. Imaizumi, K., Mawatari, K., Murata, M., Ikeda, I., and Sugano, M. (1983) The Contrasting Effect of Dietary Phosphatidylethanolamine and Phosphatidylcholine on Serum Lipoproteins and Liver Lipids in Rats, J. Nutr. 113, 2403–2411.

    PubMed  CAS  Google Scholar 

  29. Imaizumi, K., Sakono, M., Mawatari, K., Murata, M., and Sugano, M. (1989) Effect of Phosphatidylethanolamine and Its Constituent Base on the Metabolism of Linoleic Acid in Rat Liver, Biochim. Biophys. Acta 1005, 253–259.

    PubMed  CAS  Google Scholar 

  30. Faas, F.H., and Carter, W.J. (1983) Altered Microsomal Phospholipid Composition in the Streptozotocin Diabetic Rat, Lipids 18, 339–342.

    PubMed  CAS  Google Scholar 

  31. Pelech, S.L., and Vance, D.E. (1984) Regulation of Phosphatidylcholine Biosynthesis, Biochim. Biophys. Acta 779, 217–251.

    PubMed  CAS  Google Scholar 

  32. Audubert, F., and Vance, D.E. (1983) Pitfalls and Problems in Studies on the Methylation of Phosphatidylethanolamine, J. Biol. Chem. 258, 10695–10701.

    PubMed  CAS  Google Scholar 

  33. Oda, H., Okumura, Y., Hitomi, Y., Ozaki, K., Nagaoka, S., and Yoshida, A. (1989) Effect of Dietary Methionine and Polychlorinated Biphenyls on Cholesterol Metabolism in Rats Fed a Diet Containing Soy Protein Isolate, J. Nutr. Sci. Vitaminol. 35, 333–348.

    PubMed  CAS  Google Scholar 

  34. Tanaka, K., and Sugano, M. (1989) Effects of Addition of Sulfur-Containing Amino Acids and Glycine to Soybean Protein and Casein on Serum Cholesterol Levels in Rats, J. Nutr. Sci. Vitaminol. 35, 323–332.

    PubMed  CAS  Google Scholar 

  35. Saeki, S., Kanauchi, O., and Kiriyama, S. (1990) Some Metabolic Aspects of the Hypocholesterolemic Effect of Soybean Protein in Rats Fed a Cholesterol-Free Diet, J. Nutr. Sci. Vitaminol. 36, 125S-131S.

    Google Scholar 

  36. Sugiyama, K., Kushima, Y., and Muramatsu, K. (1985) Effects of Sulfur-Containing Amino Acids and Glycine on Plasma Cholesterol Levels in Rats Fed on a High Cholesterol Diet, Agric. Biol. Chem. 49, 3455–3461.

    CAS  Google Scholar 

  37. Kadowaki, H., Patton, G.M., and Robins, S.J. (1993) Effect of Phosphatidylcholine Molecular Species on the Uptake of HDL Triglycerides and Cholesteryl Esters by the Liver, J. Lipid Res. 34, 180–189.

    PubMed  CAS  Google Scholar 

  38. Kadowaki, H., Patton, G.M., and Robins, S.J. (1992) Metabolism of High Density Lipoprotein Lipids by the Rat Liver: Evidence for Participation of Hepatic Lipase in the Uptake of Cholesteryl Ester, J. Lipid Res. 33, 1689–1698.

    PubMed  CAS  Google Scholar 

  39. Shafi, S., Brady, S.E., Bensadoun, A., and Havel, R.J. (1994) Role of Hepatic Lipase in the Uptake and Processing of Chylomicron Remnants in Rat Liver, J. Lipid Res. 35, 709–720.

    PubMed  CAS  Google Scholar 

  40. Ji, Z.-S., Lauer, S.J., Fazio, S., Bensadoun, A., Taylor, J.M., and Mahley, R.W. (1994) Enhanced Binding and Uptake of Remnant Lipoproteins by Hepatic Lipase-Secreting Cells in Culture, J. Biol. Chem. 269, 13429–13436.

    PubMed  CAS  Google Scholar 

  41. Sirtori, C.R., Galli, G., Lovati, M.R., Carrara, P., Bosisio, E., and Galli-Kienle, M. (1984) Effect of Dietary Proteins on the Regulation of Liver Lipoprotein Receptors in Rats, J. Nutr. 114, 1493–1500.

    PubMed  CAS  Google Scholar 

  42. Brousseau, M.E., Stucchi, A.F., Vespa, D.B., Schaefer, E.J., and Nicolosi, R.J. (1993) A Diet Enriched in Monosaturated Fats Decreases Low Density Lipoprotein Concentrations in Cynomolgus Monkeys by a Different Mechanism Than Does a Diet Enriched in Polyunsaturated Fats, J. Nutr. 123, 2049–2058.

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Kimio Sugiyama.

About this article

Cite this article

Sugiyama, K., Kumazawa, A., Zhou, H. et al. Dietary methionine level affects linoleic acid metabolism through phosphatidylethanolamine N-methylation in rats. Lipids 33, 235–242 (1998). https://doi.org/10.1007/s11745-998-0201-2

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11745-998-0201-2

Keywords

Navigation