Preventive Nutrition and Food Science

The Korean Society of Food Science and Nutrition (한국식품영양과학회)
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Differential Effects of Cod Proteins and Tuna Proteins on Serum and Liver Lipid Profiles in Rats Fed Non-Cholesterol- and Cholesterol-Containing Diets

  • Hosomi, Ryota (Laboratory of Food and Nutritional Sciences, Faculty of Chemistry, Materials, and Bioengineering, Kansai University) ;
  • Maeda, Hayato (Laboratory of Food Chemistry, Faculty of Agriculture and Life Science, Hirosaki University) ;
  • Ikeda, Yuki (Laboratory of Food and Nutritional Sciences, Faculty of Chemistry, Materials, and Bioengineering, Kansai University) ;
  • Toda, Yuko (Laboratory of Food and Nutritional Sciences, Faculty of Chemistry, Materials, and Bioengineering, Kansai University) ;
  • Yoshida, Munehiro (Laboratory of Food and Nutritional Sciences, Faculty of Chemistry, Materials, and Bioengineering, Kansai University) ;
  • Fukunaga, Kenji (Laboratory of Food and Nutritional Sciences, Faculty of Chemistry, Materials, and Bioengineering, Kansai University)
  • Received : 2017.02.06
  • Accepted : 2017.03.17
  • Published : 2017.06.30
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Abstract

Fish muscles are classified into white and red muscles, and the chemical composition of the two fish muscles have many differences. Few reports have assessed the health-promoting functions of white fish muscle proteins (WFP) and red fish muscle proteins (RFP). We therefore evaluated the mechanisms underlying the alteration of lipid profiles and cholesterol metabolism following the intake of WFP prepared from cod and RFP prepared from light muscles of tuna. Male Wistar rats were divided into six dietary groups: casein (23%), WFP (23%), and RFP (23%), with or without 0.5% cholesterol and 0.1% sodium cholate. Compared to the WFP-containing diet, the RFP-containing diet supplemented with cholesterol and sodium cholate significantly increased serum and liver cholesterol contents. However, in the RFP groups, an alteration in cholesterol metabolism including an increased tendency to excrete fecal sterols and hepatic cholesterol $7{\alpha}$-hydroxylase was related to the reduction of hepatic cholesterol contents. This phenomenon might be related to the tendency of an increased food intake in RFP-containing diets. These results highlight the differential effects of WFP and RFP on serum and liver lipid profiles of Wistar rats fed non-cholesterol- or cholesterol-containing diets under no fasting condition.

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References

  1. Nanri A, Mizoue T, Noda M, Takahashi Y, Matsushita Y, Poudel-Tandukar K, Kato M, Oba S, Inoue M, Tsugane S; Japan Public Health Center-based Prospective Study Group. 2011. Fish intake and type 2 diabetes in Japanese men and women: the Japan Public Health Center-based Prospective Study. Am J Clin Nutr 94: 884-891. https://doi.org/10.3945/ajcn.111.012252
  2. Hosomi R, Yoshida M, Fukunaga K. 2012. Seafood consumption and components for health. Glob J Health Sci 4: 72-86.
  3. Telle-Hansen VH, Larsen LN, Hostmark AT, Molin M, Dahl L, Almendingen K, Ulven SM. 2012. Daily intake of cod or salmon for 2 weeks decreases the 18:1n-9/18:0 ratio and serum triacylglycerols in healthy subjects. Lipids 47: 151-160. https://doi.org/10.1007/s11745-011-3637-y
  4. Hosomi R, Fukunaga K, Arai H, Kanda S, Nishiyama T, Yoshida M. 2011. Fish protein decreases serum cholesterol in rats by inhibition of cholesterol and bile acid absorption. J Food Sci 76: H116-H121. https://doi.org/10.1111/j.1750-3841.2011.02130.x
  5. Hosomi R, Fukunaga K, Arai H, Nishiyama T, Yoshida M. 2009. Effects of dietary fish protein on serum and liver lipid concentrations in rats and the expression of hepatic genes involved in lipid metabolism. J Agric Food Chem 57: 9256-9262. https://doi.org/10.1021/jf901954r
  6. Shukla A, Bettzieche A, Hirche F, Brandsch C, Stangl GI, Eder K. 2006. Dietary fish protein alters blood lipid concentrations and hepatic genes involved in cholesterol homeostasis in the rat model. Br J Nutr 96: 674-682.
  7. Wergedahl H, Liaset B, Gudbrandsen OA, Lied E, Espe M, Muna Z, Mork S, Berge RK. 2004. Fish protein hydrolysate reduces plasma total cholesterol, increases the proportion of HDL cholesterol, and lowers acyl-CoA: cholesterol acyltransferase activity in liver of Zucker rats. J Nutr 134: 1320-1327. https://doi.org/10.1093/jn/134.6.1320
  8. Boukortt FO, Girard A, Prost JL, Ait-Yahia D, Bouchenak M, Belleville J. 2004. Fish protein improves the total antioxidant status of streptozotocin-induced diabetes in spontaneously hypertensive rat. Med Sci Monit 10: BR397-BR404.
  9. Murata M, Sano Y, Bannai S, Ishihara K, Matsushima R, Uchida M. 2004. Fish protein stimulated the fibrinolysis in rats. Ann Nutr Metab 48: 348-356. https://doi.org/10.1159/000081971
  10. Maeda H, Hosomi R, Koizumi M, Toda Y, Mitsui M, Fukunaga K. 2015. Dietary cod protein decreases triacylglycerol accumulation and fatty acid desaturase indices in the liver of obese type-2 diabetic KK-Ay mice. J Funct Foods 14: 87-94. https://doi.org/10.1016/j.jff.2015.01.038
  11. Oishi Y, Dohmoto N. 2009. Alaska pollack protein prevents the accumulation of visceral fat in rats fed a high fat diet. J Nutr Sci Vitaminol 55: 156-161. https://doi.org/10.3177/jnsv.55.156
  12. Abe H. 1983. Distribution of free L-histidine and its related compounds in marine fishes. Nippon Suisan Gakkaishi 49: 1683-1687. https://doi.org/10.2331/suisan.49.1683
  13. Beauchesne-Rondeau E, Gascon A, Bergeron J, Jacques H. 2003. Plasma lipids and lipoproteins in hypercholesterolemic men fed a lipid-lowering diet containing lean beef, lean fish, or poultry. Am J Clin Nutr 77: 587-593. https://doi.org/10.1093/ajcn/77.3.587
  14. Mann N, Sinclair A, Pille M, Johnson L, Warrick G, Reder E, Lorenz R. 1997. The effect of short-term diets rich in fish, red meat, or white meat on thromboxane and prostacyclin synthesis in humans. Lipids 32: 635-644. https://doi.org/10.1007/s11745-997-0081-5
  15. Liu CH, Huang MT, Huang PC. 1995. Sources of triacylglycerol accumulation in livers of rats fed a cholesterol-supplemented diet. Lipids 30: 527-531. https://doi.org/10.1007/BF02537027
  16. Bligh EG, Dyer WJ. 1959. A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37: 911-917. https://doi.org/10.1139/y59-099
  17. Fukunaga K, Hosomi R, Fukao M, Miyauchi K, Kanda S, Nishiyama T, Yoshida M. 2016. Hypolipidemic effects of phospholipids (PL) containing n-3 polyunsaturated fatty acids (PUFA) are not dependent on esterification of n-3 PUFA to PL. Lipids 51: 279-289. https://doi.org/10.1007/s11745-016-4118-0
  18. White JA, Hart RJ, Fry JC. 1986. An evaluation of the Waters Pico-Tag system for the amino-acid analysis of food materials. J Automat Chem 8: 170-177. https://doi.org/10.1155/S1463924686000330
  19. de Duve C. 1948. A spectrophotometric method for the simultaneous determination of myoglobin and hemoglobin in extracts of human muscle. Acta Chem Scand 2: 264-289. https://doi.org/10.3891/acta.chem.scand.02-0264
  20. Laemmli UK. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685. https://doi.org/10.1038/227680a0
  21. Reeves PG, Nielsen FH, Fahey GC Jr. 1993. AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet. J Nutr 123: 1939-1951. https://doi.org/10.1093/jn/123.11.1939
  22. Rouser G, Fkeischer S, Yamamoto A. 1970. Two dimensional then layer chromatographic separation of polar lipids and determination of phospholipids by phosphorus analysis of spots. Lipids 5: 494-496. https://doi.org/10.1007/BF02531316
  23. van de Kamer JH, ten Bokkel Huinink H, Weyers HA. 1949. Rapid method for the determination of fat in feces. J Biol Chem 177: 347-355.
  24. Kelley DS, Nelson GJ, Hunt JE. 1986. Effect of prior nutritional status on the activity of lipogenic enzymes in primary monolayer cultures of rat hepatocytes. Biochem J 235: 87-90. https://doi.org/10.1042/bj2350087
  25. Inoue H, Lowenstein JM. 1975. Acetyl coenzyme A carboxylase from rat liver. In Methods in Enzymology. Academic Press, New York, NY, USA. Vol 35, p 3-11.
  26. Kelley DS, Kletzien RF. 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. https://doi.org/10.1042/bj2170543
  27. Hsu RY, Lardy HA. 1969. Malic enzyme. In Methods in Enzymology. Academic Press, New York, NY, USA. Vol 13, p 230-235.
  28. Markwell MA, McGroarty EJ, Bieber LL, Tolbert NE. 1973. The subcellular distribution of carnitine acyltransferases in mammalian liver and kidney. A new peroxisomal enzyme. J Biol Chem 248: 3426-3432.
  29. Ide T, Watanabe M, Sugano M, Yamamoto I. 1987. Activities of liver mitochondrial and peroxisomal fatty acid oxidation enzymes in rats fedtrans fat. Lipids 22: 6-10. https://doi.org/10.1007/BF02534867
  30. Hosomi R, Miyauchi K, Yamamoto D, Arai H, Nishiyama T, Yoshida M, Fukunaga K. 2015. Salmon protamine decreases serum and liver lipid contents by inhibiting lipid absorption in an in vitro gastrointestinal digestion model and in rats. J Food Sci 80: H2346-H2353. https://doi.org/10.1111/1750-3841.13003
  31. Adler-Nissen J. 1979. Determination of the degree of hydrolysis of food protein hydrolysates by trinitrobenzenesulfonic acid. J Agric Food Chem 27: 1256-1262. https://doi.org/10.1021/jf60226a042
  32. Benaicheta N, Labbaci FZ, Bouchenak M, Boukortt FO. 2016. Effect of sardine proteins on hyperglycaemia, hyperlipidaemia and lecithin:cholesterol acyltransferase activity, in highfat diet-induced type 2 diabetic rats. Br J Nutr 115: 6-13. https://doi.org/10.1017/S0007114515004195
  33. Higaki N, Sato K, Suda H, Suzuka T, Komori T, Saeki T, Nakamura Y, Ohtsuki K, Iwami K, Kanamoto R. 2006. Evidence for the existence of a soybean resistant protein that captures bile acid and stimulates its fecal excretion. Biosci Biotechnol Biochem 70: 2844-2852. https://doi.org/10.1271/bbb.60237
  34. Gupta S, Stravitz RT, Dent P, Hylemon PB. 2001. Down-regulation of cholesterol $7{\alpha}$-hydroxylase (CYP7A1) gene expression by bile acids in primary rat hepatocytes is mediated by the c-Jun N-terminal kinase pathway. J Biol Chem 276: 15816-15822. https://doi.org/10.1074/jbc.M010878200
  35. Morita T, Oh-hashi A, Takei K, Ikai M, Kasaoka S, 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. https://doi.org/10.1093/jn/127.3.470
  36. Lin CC, Yin MC. 2008. Effects of cysteine-containing compounds on biosynthesis of triacylglycerol and cholesterol and anti-oxidative protection in liver from mice consuming a high-fat diet. Br J Nutr 99: 37-43.
  37. Katan MB, Vroomen LH, Hermus RJ. 1982. Reduction of casein- induced hypercholesterolaemia and atherosclerosis in rabbits and rats by dietary glycine, arginine and alanine. Atherosclerosis 43: 381-391. https://doi.org/10.1016/0021-9150(82)90037-5
  38. Liaset B, Madsen L, Hao Q, Criales G, Mellgren G, Marschall HU, Hallenborg P, Espe M, Froyland L, Kristiansen K. 2009. Fish protein hydrolysate elevates plasma bile acids and reduces visceral adipose tissue mass in rats. Biochim Biophys Acta 1791: 254-262. https://doi.org/10.1016/j.bbalip.2009.01.016
  39. Martini C, Pallottini V, Cavallini G, Donati A, Bergamini E, Trentalance A. 2007. Caloric restrictions affect some factors involved in age-related hypercholesterolemia. J Cell Biochem 101: 235-243. https://doi.org/10.1002/jcb.21158
  40. Sufian MK, Hira T, Miyashita K, Nishi T, Asano K, Hara H. 2006. Pork peptone stimulates cholecystokinin secretion from enteroendocrine cells and suppresses appetite in rats. Biosci Biotechnol Biochem 70: 1869-1874. https://doi.org/10.1271/bbb.60046
  41. Betz MJ, Bielohuby M, Mauracher B, Abplanalp W, Müller HH, Pieper K, Ramisch J, Tschöp MH, Beuschlein F, Bidlingmaier M, Slawik M. 2012. Isoenergetic feeding of low carbohydrate-high fat diets does not increase brown adipose tissue thermogenic capacity in rats. PLoS One 7: e38997. https://doi.org/10.1371/journal.pone.0038997
  42. Ikeda I, Metoki K, Yamahira T, Kato M, Inoue N, Nagao K, Yanagita T, Shirakawa H, Komai M. 2014. Impact of fasting time on hepatic lipid metabolism in nutritional animal studies. Biosci Biotechnol Biochem 78: 1584-1591. https://doi.org/10.1080/09168451.2014.923297
  43. Halminski MA, Marsh JB, Harrison EH. 1991. Differential effects of fish oil, safflower oil and palm oil on fatty acid oxidation and glycerolipid synthesis in rat liver. J Nutr 121: 1554-1561. https://doi.org/10.1093/jn/121.10.1554
  44. Voshol PJ, Haemmerle G, Ouwens DM, Zimmermann R, Zechner R, Teusink B, Maassen JA, Havekes LM, Romijn JA. 2003. Increased hepatic insulin sensitivity together with decreased hepatic triglyceride stores in hormone-sensitive lipase- deficient mice. Endocrinology 144: 3456-3462. https://doi.org/10.1210/en.2002-0036
  45. Frayn KN. 1993. Insulin resistance and lipid metabolism. Curr Opin Lipidol 4: 197-204. https://doi.org/10.1097/00041433-199306000-00004
  46. Kawabata F, Mizushige T, Uozumi K, Hayamizu K, Han L, Tsuji T, Kishida T. 2015. Fish protein intake induces fast-muscle hypertrophy and reduces liver lipids and serum glucose levels in rats. Biosci Biotechnol Biochem 79: 109-116. https://doi.org/10.1080/09168451.2014.951025
  47. Ayabe T, Mizushige T, Ota W, Kawabata F, Hayamizu K, Han L, Tsuji T, Kanamoto R, Ohinata K. 2015. A novel Alaska pollack- derived peptide, which increases glucose uptake in skeletal muscle cells, lowers the blood glucose level in diabetic mice. Food Funct 6: 2749-2757. https://doi.org/10.1039/C5FO00401B

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