Skip to main content
Log in

Effects of dietary defatted squid on cholesterol metabolism and hepatic lipogenesis in rats

  • Articles
  • Published:
Lipids

Abstract

Male Sprague-Dawley rats were fed a cholesterol-free (Exp. 1) or cholesterol-supplemented (Exp. 2) diet containing 20% casein (control group) or 15% defatted squid and 5% casein (defatted squid group), as protein, for 14 d. Serum and hepatic cholesterol concentrations were lower in rats fed defatted squid than in those fed casein in both cholesterol-free (−20%, P<0.05 and −15%, P<0.05, respectively) and cholesterol-supplemented (−25%, P<0.05 and −15%, P<0.05, respectively) diets. Hepatic triglyceride concentration was lower in the defatted squid than in the control groups in both cholesterol-free (−51%, P<0.05) and cholesterol-supplemented diets (−38%, P<0.01). The activities of cytosolic fatty acid synthase and the NADPH-generating enzymes, malic enzyme and glucose-6-phosphate dehydrogenase, in the liver were lower in the defatted squid than in the control groups in both cholesterol-free (−21%, P<0.01, −33%, P<0.05, and −33%, P<0.01, respectively) and cholesterol-supplemented diets (−34%, P<0.05, −57%, P<0.05, and −67%, P<0.05, respectively). The activity of mitochondrial carnitine palmitoyltransferase in the liver was comparable between the control and defatted squid groups. The activity of Mg2+-dependent phosphatidate phosphohydrolase in the liver cytosol was lower in the defatted squid (−9%, P<0.05) than in the control groups only in the cholesterol-free diet. Fecal excretion of total steroids was stimulated by the feeding of defatted squid in both cholesterol-free (+77%, P<0.005) and cholesterol-supplemented diets (+29%, P<0.01). These results suggest that the nonlipid fraction of squid exerts a hypocholesterolemic effect by increasing the excretion of total steroids in feces. The fraction also induces a triglyceride-lowering activity in the liver by decreasing hepatic lipogenesis.

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

CPT:

carnitine palmitoyltransferase

DHA:

docosahexaenoic acid

EPA:

eicosapentaenoic acid

FAS:

fatty acid synthase

G6PDH:

glucose-6-phosphate dehydrogenase

HDL:

high density lipoprotein

PAP:

phosphatidate phosphohydrolase

PUFA:

polyunsaturated fatty acids

VLDL:

very low density lipoprotein

References

  1. Crombie, I.K., McLoone, P., Smith, W.C., Thompson, M., and Pedoe, J.T. (1987) International Differences in Coronary Heart Disease Mortality and Consumption of Fish and Other Food-stuffs, Eur. Heart J. 8, 560–563.

    PubMed  CAS  Google Scholar 

  2. Daviglus, M.L., Stamlaer, J., Orencia, A.J., Dyer, A.R., Liu, K., Greenland, P., Walsh, M.K., Morris, D., and Shekelle, R.B. (1997) Fish Consumption and the 30-Year Risk of Fatal Myocardial Infarction, N. Engl. J. Med., 336, 1046–1053.

    Article  PubMed  CAS  Google Scholar 

  3. Harris, W.S., Connor, W.E., and McMurry, M.P. (1983) The Comparative Reductions of Plasma Lipids and Lipoproteins by Dietary Polyunsaturated Fats: Salmon Oil versus Vegetable Oils, Metabolism 32, 179–184.

    Article  PubMed  CAS  Google Scholar 

  4. Harris, W.S. (1996) n−3 Fatty Acids and Lipoproteins: Comparison of Results from Human and Animal Studies, Lipids 31, 243–252.

    PubMed  CAS  Google Scholar 

  5. Sanders, T.A.B., and Roshanai, F. (1983) The Influence of Different Types of Omega-3 Polyunsaturated Fatty Acids on Blood Lipids and Platelet Function in Healthy Volunteers, Circ. Sci. 64, 91–99.

    CAS  Google Scholar 

  6. Childs, M.T., Dorsett, C.S., King, I.B., Ostrander, J.G., and Yamanaka, W.K. (1990) Effects of Shellfish Consumption on Lipoproteins in Normolipidemic Men, Am. J. Clin. Nutr. 51, 1020–1027.

    PubMed  CAS  Google Scholar 

  7. Tanaka, K., Fukuda, M., Ikeda, I., and Sugano, M. (1994) Effects of Dietary Short-Necked Clam, Tapes japonica, on Serum and Liver Cholesterol Levels in Mice, J. Nutr. Sci. Vitaminol. 40, 325–333.

    PubMed  CAS  Google Scholar 

  8. Tanaka, K., Sakai, T., Ikeda, I., Imaizumi, K., and Sugano, M. (1998) Effects of Dietary Shrimp, Squid and Octopus on Serum and Liver Lipid Levels in Mice, Biosci. Biotech. Biochem. 62, 1369–1375.

    Article  CAS  Google Scholar 

  9. Sugano, M., Yamada, Y., Yoshida, K., Hashimoto, Y., Matsuo, T., and Kimoto, M. (1988) The Hypocholesterolemic Action of the Undigested Fraction of Soybean Protein in Rats, Atherosclerosis 72, 115–122.

    Article  PubMed  CAS  Google Scholar 

  10. Sugano, M., Goto, S., Yamada, Y., Yoshida, K., Hashimoto, Y., Matsuo, T., and Kimoto, M. (1990) Cholesterol-Lowering Activity of Various Undigested Fractions of Soybean Protein in Rats, J. Nutr. 120, 977–985.

    PubMed  CAS  Google Scholar 

  11. Koba, K., Wakamatsu, K., Obata, K., and Sugano, M. (1993) Effects of Dietary Proteins on Linoleic Acid Desaturation and Membrane Fluidity in Rat Liver Microsomes, Lipids 28, 457–464.

    PubMed  CAS  Google Scholar 

  12. Ikeda, I., Cha, J.-Y., Yanagita, T., Nakatani, N., Oogami, K., Imaizumi, K., and Yazawa, K. (1998) Effects of Dietary α-Linolenic, Eicosapentaenoic and Docosahexaenoic Acids on Hepatic Lipogenesis and β-Oxidation in Rats, Biosci. Biotech. Biochem. 62, 675–680.

    Article  CAS  Google Scholar 

  13. Yoshida, H., Mawatari, M., Ikeda, I., Imaizumi, K., Seto, A., and Tsuji, H. (1999) Effect of Dietary Seal and Fish Oils on Triacylglycerol Metabolism in Rats, J. Nutr. Sci. Vitaminol. 45, 411–421.

    PubMed  CAS  Google Scholar 

  14. Harper, A.E. (1959) Amino Acid Balance and Imbalance. I. Dietary Level of Protein and Amino Acid Imbalance, J. Nutr. 68, 405–418.

    PubMed  CAS  Google Scholar 

  15. Folch, J., Lees, M., and Sloane Stanley, G.J. (1957) A Simple Method for the Isolation and Purification of Total Lipids from Animal Tissues, J. Biol. Chem. 226, 497–506.

    PubMed  CAS  Google Scholar 

  16. Nagata, Y., Imaizumi, K., and Sugano, M. (1980) Effects of Soya-Bean Protein and Casein on Serum Cholesterol Levels in Rats, Br. J. Nutr. 44, 113–121.

    Article  PubMed  CAS  Google Scholar 

  17. Grundy, S.M., Ahrens, E.H., and Mietinen, T.A. (1965) Quantitative Isolation and Gas-Liquid Chromatographic Analysis of Total Dietary and Fecal Neutral Steroids, J. Lipid Res. 6, 411–424.

    PubMed  Google Scholar 

  18. Kuriyama, K., Ban, Y., and Nakashima, T. (1979) Simultaneous Determination of Biliary Bile Acids in Rat: Electron Impact and Ammonia Chemical Ionization Mass Spectrometric Analysis of Bile Acids, Steroids 34, 717–728.

    Article  PubMed  CAS  Google Scholar 

  19. Kelly, D.S., Nelson, G.J., and Hunt, J.E. (1986) Effect of Prior Nutritional Status on the Activity of Lipogenic Enzymes in Primary Monolayer Cultures of Rat Hepatocytes, Biochem. J. 235, 87–90.

    Google Scholar 

  20. Kelly, D.S., and Kletzien, R.F. (1984) Ethanol Modulation of the Hormonal and Nutritional Regulation of Glucose-6-phosphate Dehydrogenase Activity in Primary Cultures of Rat Hepatocytes, Biochem. J. 217, 543–549.

    Google Scholar 

  21. Ochoa, S. (1955) Malic Enzyme, in Methods in Enzymology (Colowick, S.P., and Kaplan, N.O., eds.), Vol. 1, pp. 739–753, Academic Press, New York.

    Chapter  Google Scholar 

  22. Walton, P.A., and Possmayer, F. (1985) Mg2+-Dependent Phosphatidate Phosphohydrolase of Rat Lung: Development of an Assay Employing a Defined Chemical Substrate Which Reflects the Phosphohydrolase Activity Measured Using Membrane-Bound Substrate, Anal. Biochem. 151, 479–486.

    Article  PubMed  CAS  Google Scholar 

  23. Markwell, M.A.K., McGroarty, E.J., Bieber, L.L., and Tolbert, N.E. (1973) The Subcellular Distribution of Carnitine Acyltransferases in Mammalian Liver and Kidney, J. Biol. Chem. 248, 3426–3432.

    PubMed  CAS  Google Scholar 

  24. Raicht, R.F., Cohen, B.I., Shefer, S., and Mosbach, E.H. (1975) Sterol Balance Studies in the Rat. Effects of Dietary Cholesterol and Beta-Sitosterol on Sterol Balance and Rate-Limiting Enzymes of Sterol Metabolism, Biochim. Biophys. Acta 388, 374–384.

    PubMed  CAS  Google Scholar 

  25. Madani, S., Lopez, S., Blond, J.P., Prost, J., and Belleville, J. (1998) Highly Purified Soybean Protein Is Not Hypocholesterolemic in Rats but Stimulates Cholesterol Synthesis and Excretion and Reduces Polyunsaturated Fatty Acid Biosynthesis, J. Nutr. 128, 1084–1091.

    PubMed  CAS  Google Scholar 

  26. Nagaoka, S., Miwa, K., Eto, M., Kuzuya, Y., Hori, G., and Yamamoto, K. (1999) Soy Protein Peptic Hydrolysate with Bound Phospholipids Decreases Micellar Solubility and Cholesterol Absorption in Rats and Caco-2 Cells, J. Nutr. 129, 1725–1730.

    PubMed  CAS  Google Scholar 

  27. Tanaka, K., Aso, B., and Sugano, M. (1984) Biliary Steroid Excretion in Rats Fed Soybean Protein and Casein or Their Amino Acid Mixture, J. Nutr. 114, 26–32.

    PubMed  CAS  Google Scholar 

  28. Lapre, J.A., West, C.E., Lovati, M.R., Sirtori, C.R., and Beynen, A.C. (1989) Dietary Animal Proteins and Cholesterol Metabolism in Rats, Internat. J. Vit. Nutr. Res. 59, 93–100.

    CAS  Google Scholar 

  29. Ogawa, T., Gatchalian-Yee, M., Sugano, M., Kimoto, M., Matsuo, T., and Hashimoto, Y. (1992) Hypocholesterolemic Effect of Undigested Fraction of Soybean Protein in Rats Fed No Cholesterol, Biosci. Biotech. Biochem. 56, 1845–1848.

    Article  CAS  Google Scholar 

  30. Nagata, Y., Tanaka, K., and Sugano, M. (1981) Further Studies on the Hypocholesterolaemic Effect of Soya-Bean Protein in Rats, Br. J. Nutr. 45, 233–241.

    Article  PubMed  CAS  Google Scholar 

  31. Morita, T., Oh-hashi, A., Takei, K., Ikai, M., Kasaoka, S., and Kiriyama, S. (1997) Cholesterol-Lowering Effects of Soybean, Potato and Rice Proteins Depend on Their Low Methionine Contents in Rats Fed a Cholesterol-Free Purified Diet, J. Nutr. 127, 470–477.

    PubMed  CAS  Google Scholar 

  32. Iritani, N., Nagashima, K., Fukuda, H., Katsurada, A., and Tanaka, T. (1986) Effects of Dietary Proteins on Lipogenic Enzyme in Rat Liver, J. Nutr. 116, 190–197.

    PubMed  CAS  Google Scholar 

  33. Brindley, D.N. (1991) Metabolism of Triacylglycerols, in Biochemistry of Lipids, Lipoproteins and Membranes (Vance, D.E., and Vance, J., eds.), pp. 171–203, Elsevier Science Publishers, New York.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Kazunari Tanaka.

About this article

Cite this article

Tanaka, K., Ikeda, I., Yoshida, H. et al. Effects of dietary defatted squid on cholesterol metabolism and hepatic lipogenesis in rats. Lipids 36, 461–466 (2001). https://doi.org/10.1007/s11745-001-0743-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11745-001-0743-3

Keywords

Navigation