Abstract
This experiment was designed to evaluate the effect of casein or ovomucin (OV) on the micellar solubility of cholesterol and the taurocholate binding capacity in vitro. We also evaluated the effects of casein or OV on cholesterol metabolism in rats and Caco-2 cells. OV has a significantly greater bile acid-binding capacity than that of casein in vitro. Micellar cholesterol solubility in vitro was significantly lower in the presence of OV compared to casein. The cholesterol micelles containing OV significantly suppressed cholesterol uptake by Caco-2 cells compared to the cholesterol micelles containing casein. Consistent with these in vitro findings, OV-feeding significantly increased the fecal excretion of bile acids or cholesterol compared with casein-feeding. Serum total cholesterol was significantly lower in rats fed OV than in those fed casein. The concentrations of total lipids in liver were significantly lower in the OV-fed group compared with the casein group. These results suggest that the suppression of cholesterol absorption by direct interaction between cholesterol mixed micelles and OV in the jejunal epithelia is part of the mechanism underlying the hypocholesterolemic action of OV. OV may also inhibit the reabsorption of bile acids in the ileum, thus lowering the serum cholesterol level.
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Abbreviations
- EWP:
-
egg white protein
- LTH:
-
β-lactoglobulin tryptic hydrolysate
- OV:
-
ovomucin
- SPH:
-
soy protein peptic hydrolysate
References
Carrol, K.K., and Hamilton, R.M.G. (1975) Effects of Dietary Protein and Carbohydrate on Plasma Cholesterol Levels in Relation to Atherosclerosis, J. Food Sci. 40, 18–23.
Roberts, S.L., McMurry, M.P., and Conner, W.E. (1981) Does Egg Feeding (i.e. dietary cholesterol) Affect Plasma Cholesterol Levels in Humans? Results of Double-Blind Study, Am. J. Clin. Nutr. 34, 2092–2099.
Nakamura, R., Takayama, M., Nakamura, K., and Umemura, O. (1980) Constituent Proteins of Globulin Fraction Obtained from Egg White, Agric. Biol. Chem. 44, 2357–2362.
Watanabe, K., Tsuge, Y., Shimoyamada, M., Ogama, N., and Ebina, T. (1998) Antitumor Effects of Pronase-Treated Fragments, Glycopeptides, from Ovomucin in Hen Egg White in a Double Grafted Tumor System, J. Agric. Food Chem. 46, 3033–3038.
Nagaoka, S., Kanamaru, Y., and Kuzuya, Y. (1991) Effects of Whey Protein and Casein on the Plasma and Liver Lipids in Rats, Agric. Biol. Chem. 55, 813–818.
Nagaoka, S., Kanamaru, Y., Kuzuya, Y., Kojima, T., and Kuwata, T. (1992) Comparative Studies on the Serum Cholesterol Lowering Action of Whey Protein and Soybean Protein in Rats, Biosci. Biotechnol. Biochem. 56, 1484–1485.
Potter, S.M. (1995) Overview of Proposed Mechanisms for the Hypocholesterolemic Effect of Soy, J. Nutr. 125, 606S-611S.
Zhang, X., and Beynen, A.C. (1993) Influence of Dietary Fish Proteins on Plasma and Liver Cholesterol Concentrations in Rats, Br. J. Nutr. 69, 767–777.
Sirtori, C.R., Even, R., and Lovati, M.S. (1993) Soybean Protein Diet and Plasma Cholesterol: From Therapy to Molecular Mechanisms, Ann. NY Acad. Sci. 676, 188–201.
Yamamoto, S., Kina, T., Yamagata, N., Kokubu, T., Shinjo, S., and Asato, L. (1993) Favorable Effects of Egg White Protein on Lipid Metabolism in Rats and Mice, Nutr. Res. 13, 1453–1457.
Asato, L., Wang, M.F., Chan, Y.C., Yeh, S.H., Chung, H.M., Chung, S.Y., Chida, S., Uezato, T., Suzuki, I., Yamagata, N., et al. (1996) Effect of Egg White on Serum Cholesterol Concentration in Young Women, J. Nutr. Sci. Vitaminol. 42, 87–96.
Nagaoka, S., Awano, T., Nagata, N., Masaoka, M., Hori, G., and Hashimoto, K. (1997) Serum Cholesterol Reduction and Cholesterol Absorption Inhibition in CaCo-2 Cells by a Soyprotein Peptic Hydrolyzate, Biosci. Biotech. Biochem. 61, 354–356.
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.
Xu, J.Q., Shimoyamada, M., and Watanabe, K. (1998) Heat Aggregation of Dry-Heated Egg White and Its Inhibiting Effect on Heat Coagulation of Fresh Egg White, J. Agric. Food Chem. 46, 3027–3032.
Kato, A., Nakamura, R., and Sato, Y. (1970) Studies on Changes in Stored Shell Eggs. Part IV. Changes in the Chemical Composition of Ovomucin During Storage, Agric. Biol. Chem. 34, 1009–1013.
AOAC (1984) Official Methods of Analysis of the Association of Official Analytical Chemists, 14th edn., Association of Official Analytical Chemists, Arlington.
Dubois, M., Gilles, K.A., Hamilton, J.K., Rebers, P.A., and Smith, F. (1956) Colorimetric Method for Determination of Sugars and Related Substances, Anal. Chem. 28, 350–356.
Tsuge, Y., Shimoyamada, Y., and Watanabe, K. (1997) Structural Features of Newcastle Disease Virus- and Anti-Ovomucin Antibody-Binding Glycopeptides from Pronase-Treated Ovomucin, J. Agric. Food Chem. 45, 2393–2398
Spies, J.R., and Chambers, D.C. (1948) Chemical Determination of Tryptophan, Anal. Chem. 20, 30–39.
Spies, J.R., and Chambers, D.C. (1949) Chemical Determination of Tryptophan in Proteins, Anal. Chem. 20, 1249–1266.
Ikeda, I., Tanaka, K., Sugano, M., Vahouny, G.V., and Gallo, L.L. (1988) Inhibition of Cholesterol Absorption in Rats by Plant Sterols, J. Lipid Res. 29, 1573–1582.
American Institute of Nutrition (1977) Report of the American Institute of Nutrition ad hoc Committee on Standards for Nutritional Studies, J. Nutr. 107, 1340–1348.
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.
Nagaoka, S., Miyazaki, H., Oda, H., Aoyama, Y., and Yoshida, A. (1990) Effects of Excess Dietary Tyrosine on Cholesterol, Bile Acid Metabolism and Mixed-Function Oxidase System in Rats, J. Nutr. 120, 1134–1139.
Bruusgaard, A., Sørensen, H., Gilhuus-Moe, C.C., and Skalhegg, B.A. (1977) Bile Acid Determination with Different Preparations of 3 α-Hydroxysteroid Dehydrogenase, Clin. Chim. Acta 77, 387–395.
Malchow-Moller, A., Arffmann, S., Larusso, N.F., and Krag, E., (1982) Enzymatic Determination of Total 3 α-Hydroxy Bile Acids in Faeces. Validation in Healthy Subjects of a Rapid Method Suitable for Clinical Routine Purpose, Scand. J. Gastroenterol. 17, 331–333.
Miettinen, T.A., Ahrens, E.H., and Grundy, S.M. (1965) Quantitative Isolation and Gas-Liquid Chromatographic Analysis of Total Dietary and Fecal Neutral Steroids, J. Lipid Res. 6, 411–424.
Snedecor, C.W., and Cochran, W.G. (1967) Statistical Methods, 6th edn., The Iowa State University Press, Ames (Japanese Edition: Iwanami Publishing, Tokyo).
Huff, M.W., and Carroll, K.K. (1980) Effects of Dietary Proteins and Amino Acid Mixtures on Plasma Cholesterol Levels in Rabbits, J. Nutr. 110, 1676–1685.
Jacques, H., Deshaies, Y., and Savoie, L. (1986) Relationship Between Dietary Proteins, Their in vitro Digestion Products, and Serum Cholesterol in Rats, Atherosclerosis 61, 89–98.
Sugiyama, K., Ohkawa, S., and Muramatsu, K. (1986) Relationship Between Amino Acid Composition of Diet and Plasma Cholesterol Level in Growing Rats Fed a High Cholesterol Diet, J. Nutr. Sci. Vitaminol. 32, 413–423.
Itoh, T., Miyazaki, J., Sugawara, H., and Adachi, S. (1987) Studies on the Characterization of Ovomucin and Chalaza of the Hen’s Egg, J. Food Sci. 52, 1518–1521.
Tsuge, Y., Shimoyamada, M., and Watanabe, K. (1997) Binding of Ovomucin to Newcastle Disease Virus and Anti-Ovomucin Antibodies and Its Heat Stability Based on Binding Abilities, J. Agric. Food Chem. 45, 4629–4634.
Robinson, D.S., and Monsey, J.B. (1971) Studies on the Composition of Egg-White Ovomucin, Biochem. J. 121, 537–547.
Nagata, Y., Ishiwaki, N., and Sugano, M. (1982) Studies on the Mechanisms of Antihypercholesterolemic Action of Soy Protein and Soy Protein-Type Amino Mixtures in Relation to the Casein Counterparts in Rats, J. Nutr. 112, 1614–1625.
Smith, B.F. (1987) Human Gallbadder Mucin Binds Biliary Lipids and Promotes Cholesterol Crystal Nucleation in Model Bile, J. Lipid Res. 28, 1088–1097.
Iwami, K., Sakakibara, K., and Ibuki, F. (1986) Involvement of Post-Digestion “Hydrophobic” Peptides in Plasma Cholesterol-Lowering Effect of Dietary Plant Proteins, Agric. Biol. Chem. 50, 1217–1222.
Wilson, M.D., and Rudel, L.L. (1994) Review of Cholesterol Absorption with Emphasis on Dietary and Biliary Cholesterol, J. Lipid Res. 28, 1057–1066.
Nagaoka, S., Futamura, Y., Miwa, K., Awano, T., Yamauchi, K., Kanamaru, Y., Kojima, T., and Kuwata, T. (2001) Identification of Novel Hypocholesterolemic Peptides Derived from Bovine Milk β-Lactoglobulin, Biochem. Biophys. Res. Commun. 281, 11–17.
Hirose, N., Inoue, T., Nishihara, K., Sugano, M., Akimoto, K., Shimizu, S., and Yamada, H. (1991) Inhibition of Cholesterol Absorption and Synthesis in Rats by Sesamin, J. Lipid Res. 32, 629–638.
Ikeda, I., Imasato, Y., Sasaki, E., Nakayama, M., Nagao, H., Takeo, T., Yayabe, F., and Sugano, M. (1992) Tea Catechins Decrease Micellar Solubility and Intestinal Absorption of Cholesterol in Rats, Biochim. Biophys. Acta 1127, 141–146.
Field, F.J., Albright, E., and Mathur, S. (1987) Regulation of Cholesterol Esterification by Micellar Cholesterol in CaCo-2 Cells, J. Lipid Res. 28, 1057–1066.
Hughes, T.E., Sasak, W.V., Ordovas, J.M., Forte, T.M., Lamon-Fava, S., and Schaefer, E.J. (1987) A Novel Cell Line (Caco-2) for the Study of Intestinal Lipoprotein Synthesis, J. Biol. Chem. 262, 3762–3767.
Ranheim, T., Gedde-Dahl, A., Rustan, A.C., and Drevon, C.A. (1992) Influence of Eicosapentaenoic Acid (20∶5, n−3) on Secretion of Lipoproteins in CaCo-2 Cells, J. Lipid Res. 33, 1281–1293.
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Nagaoka, S., Masaoka, M., Zhang, Q. et al. Egg ovomucin attenuates hypercholesterolemia in rats and inhibits cholesterol absorption in Caco-2 cells. Lipids 37, 267–272 (2002). https://doi.org/10.1007/s11745-002-0890-6
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DOI: https://doi.org/10.1007/s11745-002-0890-6