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Dietary fish protein hydrolysates containing bioactive motifs affect serum and adipose tissue fatty acid compositions, serum lipids, postprandial glucose regulation and growth in obese Zucker fa/fa rats

  • Aslaug Drotningsvik (a1), Svein A. Mjøs (a2) (a3), Daniela M. Pampanin (a4), Rasa Slizyte (a5), Ana Carvajal (a5), Tore Remman (a6), Ingmar Høgøy (a7) and Oddrun A. Gudbrandsen (a1)...

Abstract

The world’s fisheries and aquaculture industries produce vast amounts of protein-containing by-products that can be enzymatically hydrolysed to smaller peptides and possibly be used as additives to functional foods and nutraceuticals targeted for patients with obesity-related metabolic disorders. To investigate the effects of fish protein hydrolysates on markers of metabolic disorders, obese Zucker fa/fa rats consumed diets with 75 % of protein from casein/whey (CAS) and 25 % from herring (HER) or salmon (SAL) protein hydrolysate from rest raw material, or 100 % protein from CAS for 4 weeks. The fatty acid compositions were similar in the experimental diets, and none of them contained any long-chain n-3 PUFA. Ratios of lysine:arginine and methionine:glycine were lower in HER and SAL diets when compared with CAS, and taurine was detected only in fish protein hydrolysate diets. Motifs with reported hypocholesterolemic or antidiabetic activities were identified in both fish protein hydrolysates. Rats fed HER diet had lower serum HDL-cholesterol and LDL-cholesterol, and higher serum TAG, MUFA and n-3:n-6 PUFA ratio compared with CAS-fed rats. SAL rats gained more weight and had better postprandial glucose regulation compared with CAS rats. Serum lipids and fatty acids were only marginally affected by SAL, but adipose tissue contained less total SFA and more total n-3 PUFA when compared with CAS. To conclude, diets containing hydrolysed rest raw material from herring or salmon proteins may affect growth, lipid metabolism, postprandial glucose regulation and fatty acid composition in serum and adipose tissue in obese Zucker rats.

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      Dietary fish protein hydrolysates containing bioactive motifs affect serum and adipose tissue fatty acid compositions, serum lipids, postprandial glucose regulation and growth in obese Zucker fa/fa rats
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      Dietary fish protein hydrolysates containing bioactive motifs affect serum and adipose tissue fatty acid compositions, serum lipids, postprandial glucose regulation and growth in obese Zucker fa/fa rats
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      Dietary fish protein hydrolysates containing bioactive motifs affect serum and adipose tissue fatty acid compositions, serum lipids, postprandial glucose regulation and growth in obese Zucker fa/fa rats
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Corresponding author

* Corresponding author: O. A. Gudbrandsen; fax +47 5597 5890; email oddrun.gudbrandsen@k1.uib.no

References

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1. Harris, WS (1989) Fish oils and plasma lipid and lipoprotein metabolism in humans: a critical review. J Lipid Res 30, 785807.
2. Harris, WS (1997) n-3 Fatty acids and serum lipoproteins: human studies. Am J Clin Nutr 65, 1645S1654S.
3. Smith, KM, Barraj, LM, Kantor, M, et al. (2009) Relationship between fish intake, n-3 fatty acids, mercury and risk markers of CHD (National Health and Nutrition Examination Survey 1999–2002). Public Health Nutr 12, 12611269.
4. Kromhout, D & de Goede, J (2014) Update on cardiometabolic health effects of omega-3 fatty acids. Curr Opin Lipidol 25, 8590.
5. Glauber, H, Wallace, P, Griver, K, et al. (1988) Adverse metabolic effect of omega-3 fatty acids in non-insulin-dependent diabetes mellitus. Ann Intern Med 108, 663668.
6. Popp-Snijders, C, Schouten, JA, Heine, RJ, et al. (1987) Dietary supplementation of omega-3 polyunsaturated fatty acids improves insulin sensitivity in non-insulin-dependent diabetes. Diabetes Res 4, 141147.
7. Eslick, GD, Howe, PR, Smith, C, et al. (2009) Benefits of fish oil supplementation in hyperlipidemia: a systematic review and meta-analysis. Int J Cardiol 136, 416.
8. Nettleton, JA & Katz, R (2005) n-3 Long-chain polyunsaturated fatty acids in type 2 diabetes: a review. J Am Diet Assoc 105, 428440.
9. Balk, EM, Lichtenstein, AH, Chung, M, et al. (2006) Effects of omega-3 fatty acids on serum markers of cardiovascular disease risk: a systematic review. Atherosclerosis 189, 1930.
10. Jacques, H (1990) Effects of dietary fish protein on plasma cholesterol and lipoproteins in animal models and in humans. Monogr Atheroscler 16, 5970.
11. Thorsdottir, I, Tomasson, H, Gunnarsdottir, I, et al. (2007) Randomized trial of weight-loss-diets for young adults varying in fish and fish oil content. Int J Obes (Lond) 31, 15601566.
12. Vikoren, LA, Nygard, OK, Lied, E, et al. (2013) A randomised study on the effects of fish protein supplement on glucose tolerance, lipids and body composition in overweight adults. Br J Nutr 109, 648657.
13. Ouellet, V, Marois, J, Weisnagel, SJ, et al. (2007) Dietary cod protein improves insulin sensitivity in insulin-resistant men and women: a randomized controlled trial. Diabetes Care 30, 28162821.
14. Wergedahl, H, Liaset, B, Gudbrandsen, OA, et al. (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, 13201327.
15. Hosomi, R, Fukunaga, K, Arai, H, et al. (2011) Fish protein decreases serum cholesterol in rats by inhibition of cholesterol and bile acid absorption. J Food Sci 76, H116H121.
16. Lavigne, C, Marette, A & Jacques, H (2000) Cod and soy proteins compared with casein improve glucose tolerance and insulin sensitivity in rats. Am J Physiol Endocrinol Metab 278, E491E500.
17. Pilon, G, Ruzzin, J, Rioux, LE, et al. (2011) Differential effects of various fish proteins in altering body weight, adiposity, inflammatory status, and insulin sensitivity in high-fat-fed rats. Metabolism 60, 11221130.
18. Madani, Z, Louchami, K, Sener, A, et al. (2012) Dietary sardine protein lowers insulin resistance, leptin and TNF-alpha and beneficially affects adipose tissue oxidative stress in rats with fructose-induced metabolic syndrome. Int J Mol Med 29, 311318.
19. Lavigne, C, Tremblay, F, Asselin, G, et al. (2001) Prevention of skeletal muscle insulin resistance by dietary cod protein in high fat-fed rats. Am J Physiol Endocrinol Metab 281, E62E71.
20. Shukla, A, Bettzieche, A, Hirche, F, et al. (2006) Dietary fish protein alters blood lipid concentrations and hepatic genes involved in cholesterol homeostasis in the rat model. Br J Nutr 96, 674682.
21. Drotningsvik, A, Mjos, SA, Hogoy, I, et al. (2015) A low dietary intake of cod protein is sufficient to increase growth, improve serum and tissue fatty acid compositions, and lower serum postprandial glucose and fasting non-esterified fatty acid concentrations in obese Zucker fa/fa rats. Eur J Nutr 54, 11511160.
22. Hagen, IV, Helland, A, Bratlie, M, et al. (2016) High intake of fatty fish, but not of lean fish, affects serum concentrations of TAG and HDL-cholesterol in healthy, normal-weight adults: a randomised trial. Br J Nutr 116, 648657.
23. FAO Fisheries Department (2014) The State of World Fisheries and Aquaculture. Rome: FAO.
24. Ryan, JT, Ross, RP, Bolton, D, et al. (2011) Bioactive peptides from muscle sources: meat and fish. Nutrients 3, 765791.
25. Kim, SK & Wijesekara, I (2010) Development and biological activities of marine-derived bioactive peptides: a review. J Funct Foods 2, 19.
26. Pampanin, DM, Larssen, E, Provan, F, et al. (2012) Detection of small bioactive peptides from Atlantic herring (Clupea harengus L.). Peptides 34, 423426.
27. Pampanin, DM, Haarr, MB & Sydnes, MO (2016) Natural peptides with antioxidant activity from Atlantic cod and Atlantic salmon residual materia. Int J Appl Res Nat Prod 9, 18.
28. de Artinano, AA & Castro, MM (2009) Experimental rat models to study the metabolic syndrome. Br J Nutr 102, 12461253.
29. 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, 19391951.
30. Oterhals, A & Samuelsen, TA (2015) Plasticization effect of solubles in fishmeal. Food Res Int 69, 313321.
31. Bligh, EG & Dyer, WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37, 911917.
32. Meier, S, Mjos, SA, Joensen, H, et al. (2006) Validation of a one-step extraction/methylation method for determination of fatty acids and cholesterol in marine tissues. J Chromatogr A 1104, 291298.
33. Sciotto, C & Mjos, SA (2012) Trans isomers of EPA and DHA in omega-3 products on the European market. Lipids 47, 659667.
34. Wasta, Z & Mjos, SA (2013) A database of chromatographic properties and mass spectra of fatty acid methyl esters from omega-3 products. J Chromatogr A 1299, 94102.
35. Nagaoka, S, Futamura, Y, Miwa, K, et al. (2001) Identification of novel hypocholesterolemic peptides derived from bovine milk beta-lactoglobulin. Biochem Biophys Res Commun 281, 1117.
36. Li-Chan, EC, Hunag, SL, Jao, CL, et al. (2012) Peptides derived from Atlantic salmon skin gelatin as dipeptidyl-peptidase IV inhibitors. J Agric Food Chem 60, 973978.
37. Ben Henda, Y, Laamari, M, Lanneluc, I, et al. (2015) Di and tripeptides from marine sources can target adipogenic process and contribute to decrease adipocyte number and functions. J Funct Foods 17, 110.
38. Yamauchi, R, Ohinata, K & Yoshikawa, M (2003) Beta-lactotensin and neurotensin rapidly reduce serum cholesterol via NT2 receptor. Peptides 24, 19551961.
39. Yoshikawa, M, Fujita, H, Matoba, N, et al. (2000) Bioactive peptides derived from food proteins preventing lifestyle-related diseases. Biofactors 12, 143146.
40. Lammi, C, Zanoni, C & Arnoldi, A (2015) IAVPGEVA, IAVPTGVA, and LPYP, three peptides from soy glycinin, modulate cholesterol metabolism in HepG2 cells through the activation of the LDLR-SREBP2 pathway. J Funct Foods 14, 469478.
41. Umezawa, H, Aoyagi, T, Ogawa, K, et al. (1984) Diprotins A and B, inhibitors of dipeptidyl aminopeptidase IV, produced by bacteria. J Antibiot (Tokyo) 37, 422425.
42. Lyapina, LA, Myasoedov, NF, Grigorjeva, ME, et al. (2013) The modern concept of the regulatory role of peptides of the glyproline family in the correction of hemostasis system function during development of diabetes mellitus. Biol Bull 40, 386393.
43. Myasoedov, NF, Lyapina, LA, Grigorjeva, ME, et al. (2016) Mechanisms for glyproline protection in hypercholesterolemia. Pathophysiology 23, 2733.
44. Yoshikawa, M (2015) Bioactive peptides derived from natural proteins with respect to diversity of their receptors and physiological effects. Peptides 72, 208225.
45. Takenaka, Y, Nakamura, F, Yamamoto, T, et al. (2003) Enterostatin (VPDPR) and its peptide fragment DPR reduce serum cholesterol levels after oral administration in mice. Biosci Biotechnol Biochem 67, 16201622.
46. Kagawa, K, Matsutaka, H, Fukuhama, C, et al. (1996) Globin digest, acidic protease hydrolysate, inhibits dietary hypertriglyceridemia and Val-Val-Tyr-Pro, one of its constituents, possesses most superior effect. Life Sci 58, 17451755.
47. Matsui, T, Oki, T & Osajima, Y (1999) Isolation and identification of peptidic alpha-glucosidase inhibitors derived from sardine muscle hydrolyzate. Z Naturforsch C 54, 259263.
48. Yamada, Y, Muraki, A, Oie, M, et al. (2012) Soymorphin-5, a soy-derived mu-opioid peptide, decreases glucose and triglyceride levels through activating adiponectin and PPARalpha systems in diabetic KKAy mice. Am J Physiol Endocrinol Metab 302, E433E440.
49. Suckling, KE, Benson, GM, Bond, B, et al. (1991) Cholesterol lowering and bile acid excretion in the hamster with cholestyramine treatment. Atherosclerosis 89, 183190.
50. Farris, EJ & Griffith, JQ (1949) The Rat in Laboratory Investigation. Philadelphia, PA: J. B. Lippincott Company.
51. Feskens, EJ, Bowles, CH & Kromhout, D (1991) Inverse association between fish intake and risk of glucose intolerance in normoglycemic elderly men and women. Diabetes Care 14, 935941.
52. Whelton, SP, He, J, Whelton, PK, et al. (2004) Meta-analysis of observational studies on fish intake and coronary heart disease. Am J Cardiol 93, 11191123.
53. Patel, PS, Forouhi, NG, Kuijsten, A, et al. (2012) The prospective association between total and type of fish intake and type 2 diabetes in 8 European countries: EPIC-InterAct Study. Am J Clin Nutr 95, 14451453.
54. Nkondjock, A & Receveur, O (2003) Fish-seafood consumption, obesity, and risk of type 2 diabetes: an ecological study. Diabetes Metab 29, 635642.
55. Kromhout, D, Bosschieter, EB & de Lezenne Coulander, C (1985) The inverse relation between fish consumption and 20-year mortality from coronary heart disease. N Engl J Med 312, 12051209.
56. Byun, HG & Kim, SK (2002) Structure and activity of angiotensin I converting enzyme inhibitory peptides derived from Alaskan pollack skin. J Biochem Mol Biol 35, 239243.
57. Bhathena, SJ, Berlin, E, Judd, JT, et al. (1991) Effects of omega 3 fatty acids and vitamin E on hormones involved in carbohydrate and lipid metabolism in men. Am J Clin Nutr 54, 684688.
58. Mori, TA, Bao, DQ, Burke, V, et al. (1999) Dietary fish as a major component of a weight-loss diet: effect on serum lipids, glucose, and insulin metabolism in overweight hypertensive subjects. Am J Clin Nutr 70, 817825.
59. Lara, JJ, Economou, M, Wallace, AM, et al. (2007) Benefits of salmon eating on traditional and novel vascular risk factors in young, non-obese healthy subjects. Atherosclerosis 193, 213221.
60. Kulakowski, EC & Maturo, J (1984) Hypoglycemic properties of taurine: not mediated by enhanced insulin release. Biochem Pharmacol 33, 28352838.
61. Roden, M, Price, TB, Perseghin, G, et al. (1996) Mechanism of free fatty acid-induced insulin resistance in humans. J Clin Invest 97, 28592865.
62. Jao, CL, Hung, CC, Tung, YS, et al. (2015) The development of bioactive peptides from dietary proteins as a dipeptidyl peptidase IV inhibitor for the management of type 2 diabetes. Biomedicine (Taipei) 5, 14.
63. Kritchevsky, D, Tepper, SA, Czarnecki, SK, et al. (1982) Atherogenicity of animal and vegetable protein. Influence of the lysine to arginine ratio. Atherosclerosis 41, 429431.
64. Morita, T, Oh-hashi, A, Takei, K, et al. (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, 470477.
65. Murakami, S, Nara, Y & Yamori, Y (1996) Taurine accelerates the regression of hypercholesterolemia in stroke-prone spontaneously hypertensive rats. Life Sci 58, 16431651.
66. Bremer, J (1955) The conjugation of glycine with cholic acid and benzoic acid in rat liver homogenate. Acta Chem Scand 9, 268271.
67. Morikawa, K, Kondo, I, Kanamaru, Y, et al. (2007) A novel regulatory pathway for cholesterol degradation via lactostatin. Biochem Biophys Res Commun 352, 697702.
68. Wergedahl, H, Gudbrandsen, OA, Rost, TH, et al. (2009) Combination of fish oil and fish protein hydrolysate reduces the plasma cholesterol level with a concurrent increase in hepatic cholesterol level in high-fat-fed Wistar rats. Nutrition 25, 98104.
69. Gudbrandsen, OA, Wergedahl, H, Liaset, B, et al. (2005) Dietary proteins with high isoflavone content or low methionine-glycine and lysine-arginine ratios are hypocholesterolaemic and lower the plasma homocysteine level in male Zucker fa/fa rats. Br J Nutr 94, 321330.
70. Gudbrandsen, OA, Wergedahl, H, Liaset, B, et al. (2008) Dietary single cell protein reduces fatty liver in obese Zucker rats. Br J Nutr 100, 776785.
71. Gudbrandsen, OA, Wergedahl, H, Mork, S, et al. (2006) Dietary soya protein concentrate enriched with isoflavones reduced fatty liver, increased hepatic fatty acid oxidation and decreased the hepatic mRNA level of VLDL receptor in obese Zucker rats. Br J Nutr 96, 249257.
72. Sugano, M, Ishiwaki, N, Nagata, Y, et al. (1982) Effects of arginine and lysine addition to casein and soya-bean protein on serum lipids, apolipoproteins, insulin and glucagon in rats. Br J Nutr 48, 211221.
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