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Differential Effects of Cod Proteins and Tuna Proteins on Serumand Liver Lipid Profiles in Rats Fed Non-Cholesterol- and Cholesterol-Containing Diets
1Laboratory of Food and Nutritional Sciences, Faculty of Chemistry, Materials, and Bioengineering, Kansai University, Osaka 564-8680, Japan 2Laboratory of Food Chemistry, Faculty of Agriculture and Life Science, Hirosaki University, Aomori 036-8561, Japan
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
Prev Nutr Food Sci 2017; 22(2): 90-99
Published June 30, 2017 https://doi.org/10.3746/pnf.2017.22.2.90
Copyright © The Korean Society of Food Science and Nutrition.
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Original
Prev Nutr Food Sci 2017; 22(2): 90-99
Published online June 30, 2017 https://doi.org/10.3746/pnf.2017.22.2.90
Copyright © The Korean Society of Food Science and Nutrition.
Differential Effects of Cod Proteins and Tuna Proteins on Serumand Liver Lipid Profiles in Rats Fed Non-Cholesterol- and Cholesterol-Containing Diets
Ryota Hosomi1, Hayato Maeda2, Yuki Ikeda1, Yuko Toda1, Munehiro Yoshida1, and Kenji Fukunaga1
1Laboratory of Food and Nutritional Sciences, Faculty of Chemistry, Materials, and Bioengineering, Kansai University, Osaka 564-8680, Japan 2Laboratory of Food Chemistry, Faculty of Agriculture and Life Science, Hirosaki University, Aomori 036-8561, Japan
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
Abstract
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 7α-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.
Keywords: cod protein, tuna protein, lipid metabolism, cholesterol, rat
Fig 1.
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Sodium dodecyl sulfate-polyacrylamide gel electrophoresis (SDS-PAGE) patterns of casein, WFP, and RFP. SDS-PAGE was performed using 12.5% polyacrylamide gels. M, molecular weight marker; CAS, casein; WFP, white muscle fish protein; RFP, red muscle fish protein.
Fig 2.
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Time courses of degree of hydrolysis and insoluble fraction production rate in simulated gastrointestinal digestions. Data represent means±SEM (n=4). (A) Significant effects of time, protein, and time-protein interactions were identified by two-factor repeated measure analysis of variance. (B) Values in the same row not sharing a common letters (a,b) are significantly different at
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Table 1 . Composition of the experimental diets (unit: g/kg)
Experiment 1 Experiment 2 CAS WFP RFP CAS+C WFP+C RFP+C Casein 230 – – 230 – – WFP – 230 – – 230 – RFP – – 230 – – 230 Dextrinized corn starch 92.1 92.1 92.1 92.1 92.1 92.1 Corn starch 277.386 277.386 277.386 271.386 271.386 271.386 Sucrose 100 100 100 100 100 100 Cellulose 50 50 50 50 50 50 AIN-93G mineral mixture 35 35 35 35 35 35 AIN-93 vitamin mixture 10 10 10 10 10 10 L-Cystine 3 3 3 3 3 3 Choline bitartrate 2.5 2.5 2.5 2.5 2.5 2.5 Soybean oil 70 70 70 70 70 70 Lard 130 130 130 130 130 130 Cholesterol – – – 5 5 5 Sodium cholate – – – 1 1 1 tert -Butylhydroquinone0.014 0.014 0.014 0.014 0.014 0.014 CAS, casein; WFP, white muscle fish protein; RFP, red muscle fish protein; CAS+C, casein with cholesterol; WFP+C, WFP with cholesterol; RFP+C, RFP with cholesterol; AIN, American Institute of Nutrition.
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Table 2 . Chemical composition of casein, WFP, and RFP
Component Casein WFP RFP Crude protein (g/100 g) 85.9 85.4 85.7 Amino acid compositions (wt %) Alanine 2.3 6.3 6.6 Arginine 3.6 8.0 7.2 Aspartic acid1) 4.9 10.1 9.8 Glutamic acid2) 18.5 16.6 14.5 Glycine 1.5 4.5 4.2 Histidine 2.5 2.6 8.2 Isoleucine 4.4 4.1 4.3 Leucine 8.3 7.9 7.5 Lysine 12.0 9.4 7.1 Methionine 2.3 3.2 3.3 Phenylalanine 5.5 4.1 3.8 Proline 13.6 4.6 3.5 Serine 4.4 4.5 3.9 Threonine 3.9 4.7 4.8 Tyrosine 6.5 3.7 3.5 Valine 5.7 4.5 4.4 Mb (g/100 g) ND 0.1 0.4 Crude fat (g/100 g) 0.7 1.0 0.7 EPA+DHA (g/100 g) ND 0.2 0.1 Cholesterol (mg/100 g) 20.0 10.0 13.0 Moisture (g/100 g) 5.6 5.9 5.3 Ash (g/100 g) 1.8 6.3 5.7 WFP, white muscle fish protein; RFP, red muscle fish protein.
1)Aspartic acid+asparagine. 2)Glutamic acid+glutamine.
EPA, eicosapentaenoic acid; DHA, docosahexaenoic acid; Mb, myoglobin; ND, not detected.
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Table 3 . Growth parameters and relative organ weights in rats fed experimental diets for 4 weeks
Experiment 1 Experiment 2 CAS WFP RFP CAS+C WFP+C RFP+C Growth parameters Initial BW (g) 72.9±1.1 71.9±0.9 71.8±1.1 84.6±2.5 83.5±1.9 84.5±2.3 Final BW (g) 303.6±10.8 305.1±4.5 320.2±3.9 317.1±8.3 322.9±5.4 344.2±10.4 BW gain (g/d) 8.2±0.4 8.3±0.2 8.9±0.1 8.6±0.4 8.9±0.2 9.6±0.3 Food intake (g/d) 17.3±0.8 17.3±0.8 19.6±0.9 17.9±0.7 17.7±0.7 20.0±0.9 Food efficiency (g/g) 0.48±0.02 0.48±0.01 0.45±0.01 0.48±0.02 0.50±0.01 0.48±0.02 Water intake (mL/d) 35.7±2.6 36.0±2.7 37.4±2.8 33.5±2.1 32.5±2.0 34.0±2.3 Organ weight (g/100 g BW) Liver weight 4.43±0.32 4.20±0.08 4.23±0.06 6.07±0.11b 5.32±0.13a 6.18±0.21b Perirenal WAT weight 1.28±0.14 1.32±0.10 1.46±0.19 1.36±0.09 1.35±0.11 1.80±0.26 Mesentery WAT weight 1.26±0.20 1.36±0.08 1.34±0.18 1.51±0.17 1.57±0.06 1.58±0.08 Epididymal WAT weight 1.33±0.15 1.42±0.07 1.41±0.05 1.57±0.15 1.37±0.17 1.54±0.24 Data represent means±SEM (n=6).
Values in the same row not sharing a common letters (a,b) are significantly different at
P <0.05 using the Tukey’s multiple comparisons test.CAS, casein; WFP, white muscle fish protein; RFP, red muscle fish protein; CAS+C, casein with cholesterol; WFP+C, WFP with cholesterol; RFP+C, RFP with cholesterol; BW, body weight; WAT, white adipose tissue.
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Table 4 . Biochemical parameters in serum, liver, and feces in rats fed experimental diets for 4 weeks
Experiment 1 Experiment 2 CAS WFP RFP CAS+C WFP+C RFP+C Serum biochemical parameters AST (IU/L) 73.7±3.8 69.2±1.0 72.3±1.4 65.7±3.6 65.2±2.5 69.0±3.0 ALT (IU/L) 42.8±3.0 40.8±1.7 38.0±1.3 34.8±3.5 39.5±2.6 34.7±2.8 TAG (mg/dL) 130.8±23.7 116.4±26.0 79.4±12.1 162.5±28.4 164.2±29.9 181.5±29.9 Cholesterol (mg/dL) 82.5±6.0 84.5±5.6 94.3±2.8 94.5±1.3a 85.0±3.5a 114.3±6.1b HDL-cholesterol (mg/dL) 55.5±5.3 58.8±4.2 67.5±2.5 52.8±2.2ab 48.0±2.2a 63.2±3.6b Non-HDL-cholesterol (mg/dL) 27.0±1.0 25.7±1.4 26.8±0.4 44.0±2.5ab 37.0±1.8a 51.2±3.8b PL (mg/dL) 149.5±9.8 151.7±5.2 168.2±3.5 156.3±7.2a 144.8±2.6a 187.0±7.1b NEFA (μEq/L) 1,036.3±133.1 926.5±62.0 978.6±197.4 653.8±33.3ab 551.0±12.3a 748.2±56.4b Liver lipid contents (mg/g) TAG 78.7±9.5AB 52.8±3.8A 111.8±18.9B 195.7±11.3 168.6±13.1 192.2±19.3 Cholesterol 4.11±0.48B 2.51±0.36A 3.26±0.31B 6.79±0.82a 4.76±0.45a 12.93±1.11b PL 21.2±1.2 20.0±0.6 19.2±1.3 21.7±0.8 22.0±0.4 20.0±0.8 Fecal biochemical parameters Dry weight (g/d) 7.77±0.24 8.16±0.14 8.61±0.31 6.10±0.33 8.88±1.4 8.09±0.52 FFA (mg/d) 124.0±8.4 138.1±4.7 141.2±10.5 316.7±32.8 435.4±61.1 414.9±65.7 Neutral sterols (mg/d) 14.2±1.3 17.7±2.7 18.8±1.6 37.5±2.8 72.4±16.0 59.8±8.0 Acidic sterols (mg/d) 13.6±2.3A 16.7±2.0AB 21.9±1.6B 22.0±2.2a 35.2±3.8ab 39.9±6.0b Nitrogen content (mg/d) 9.36±0.56A 10.21±0.27A 13.22±0.70B 6.05±0.90a 11.32±2.42ab 13.57±1.13b Data represent means±SEM (n=6).
Values in the same row not sharing a common letters (a,b or A,B) are significantly different at
P <0.05 using the Tukey’s multiple comparisons test.CAS, casein; WFP, white muscle fish protein; RFP, red muscle fish protein; CAS+C, casein with cholesterol; WFP+C, WFP with cholesterol; RFP+C, RFP with cholesterol; AST, aspartate aminotransferase; ALT, alanine aminotransferase; TAG, triacylglycerol; HDL, high-density lipoprotein; PL, phospholipid; NEFA, non-esterified fatty acid; FFA, free fatty acid.
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Table 5 . Enzymes activities and relative mRNA expression levels in livers from rats fed experimental diets for 4 weeks
Experiment 1 Experiment 2 CAS WFP RFP CAS+C WFP+C RFP+C Enzyme activity (nmol/min/mg protein) CPT-2 1.46±0.23 1.38±0.44 1.32±0.22 1.37±0.08 1.15±0.46 0.70±0.16 ACOX 2.17±0.47 3.06±0.32 2.23±0.60 1.90±0.12b 1.72±0.24ab 1.08±0.15a FAS 1.39±0.17AB 1.20±0.15A 1.97±0.21B 1.35±0.13 1.26±0.05 1.25±0.07 ACC 56.8±5.2A 55.8±8.2A 91.7±10.1B 66.5±4.8 84.6±10.9 97.6±5.4 G6PDH 10.8±0.9A 12.5±1.7AB 24.4±5.4B 4.5±0.2a 3.8±0.2a 7.5±1.1b ME 9.7±1.1A 16.2±.4AB 21.8±2.2B 4.2±0.3 4.4±0.3 4.9±0.2 mRNA expression level (arbitrary units) ABCA1 100.0±23.0 96.6±23.8 82.5±20.9 100.0±16.5 85.1±24.1 100.2±48.4 ABCG5 100.0±21.2 102.8±16.6 101.1±17.8 100.0±11.9 89.5±13.9 91.8±16.4 ABCG8 100.0±28.7 153.4±20.5 182.3±66.2 100.0±16.1 55.9±24.1 41.5±14.0 ACAT-1 100.0±2.8 92.2±12.7 70.6±13.6 100.0±18.7 92.7±27.5 106.3±48.3 CYP7A1 100.0±19.0 161.6±45.8 91.7±31.4 100.0±17.9 201.4±36.0 213.9±35.2 HMGCR 100.0±7.3 115.6±29.8 106.2±13.9 100.0±12.5 58.4±17.6 86.6±15.7 LDLR 100.0±19.6 59.6±15.0 61.2±12.1 100.0±22.6 62.3±8.1 51.6±7.2 SRB1 100.0±24.6 66.1±9.3 44.2±12.3 100.0±36.8 54.0±15.1 71.4±19.3 SHP-1 100.0±21.4 158.7±50.0 147.3±72.6 100.0±19.0 50.3±11.0 50.1±9.8 SREBF-2 100.0±22.2 64.5±17.7 59.1±10.4 100.0±8.2 61.1±19.3 75.2±15.3 Data represent means±SEM (n=6).
Values in the same row not sharing a common letters (a,b or A,B) are significantly different at
P <0.05 using the Tukey’s multiple comparisons test.The mRNA expression levels were determined by real-time polymerase chain reaction analysis using the glyceraldehyde 3-phosphate dehydrogenase mRNA expression level for normalization. mRNA expression levels of genes are shown relative to those determined from livers of rats fed the CAS (Experimental 1) and CAS+C (Experimental 2) diets (set at 100).
CAS, casein; WFP, white muscle fish protein; RFP, red muscle fish protein; CAS+C, casein with cholesterol; WFP+C, WFP with cholesterol; RFP+C, RFP with cholesterol; CPT-2, carnitine palmitoyltransferase-2 ACOX, acetyl-CoA oxidase; FAS, fatty acid synthase; ACC, acetyl-CoA carboxylase; G6PDH, glucose-6-phosphate dehydrogenase; ME, malic enzyme; ABCA1, ATP-binding cassette subfamily A1 ABCG, ATP-binding cassette subfamily G ACAT-1, acetyl-CoA acetyltransferase-1 CYP7A1, cholesterol 7α-hydroxylase; HMGCR, 3-hydroxy-3-methyl-glutaryl-CoA reductase; LDLR, low-density lipoprotein receptor; SRB1, scavenger receptor class B member 1; SHP-1, small heterodimer partner-1; SREBF-2, sterol regulatory element binding factor-2.
