This study investigated the effects of replacing casein with soy flour on the fatty acids profile and triglycerides metabolism in the liver of rats that were previously fed with normocaloric and hypercaloric diets based on casein. Wistar male rats were used; one group was fed with control diet (AIN-93) and another with hypercaloric diet (AIN-93 with 34.15% sucrose, 42% fat calories) for 9 weeks. Each group was then divided into two subgroups and casein was replaced with soybean in one of them, obtaining CC (control casein), CS (control soy), HC (hypercaloric casein) and HS (hypercaloric soy), which were fed for 6 weeks. We measured triglycerides in serum, and triglycerides, total lipids, fatty acids profile, the expression of apolipoprotein B (Apo B), acetyl-CoA carboxylase (ACC), fatty acid synthase (FAS), sterol-regulatory element-binding protein 1c (SREBP-1c), mitochondrial glycerol-3-phosphate acyltransferase (mGPAT), diacylglycerol acyltransferase 2 (DGAT-2), carnitine palmitoyltransferase 1 (CPT-1) and peroxisome proliferator-activated receptors alpha (PPARα) in liver. Histological studies were also performed. When comparing HS vs. HC, a positive effect of soybean flour on hepatic triglycerides deposits was found, possibly through the reduction in DGAT-2 expression (P < 0.01) and the increase in Apo B (P < 0.001) expression. Soybean flour also decreased fat deposits in control diets when compared with casein, decreasing the DGAT-2 (P < 0.001) expression and increasing Apo B (P < 0.001), CPT-1 (P < 0.05) and PPARα (P < 0.01) expressions. Both soy diet subgroups increased unsaturated fatty acids respect to casein diets (P < 0.01). Hepatocytes showed few lipid droplets in HS, whereas a fat deposit in HC was observed. These results suggest that replacing casein with soybean flour in normocaloric and hypercaloric diets reduces triglycerides and improves fatty acids profile in rat liver.
References
[1]
Akiyama, T., Tachibana, I., Shirohara, H., Watanabe, N. and Otsuki, M. (1996) High-Fat Hypercaloric Diet Induces Obesity, Glucose Intolerance and Hyperlipidemia in Normal Adult Male Wistar Rat. Diabetes Research and Clinical Practice, 31, 27-35. http://dx.doi.org/10.1016/0168-8227(96)01205-3
[2]
Schlienger, J.L. and Pradignac, A. (2009) Nutrition Approaches to Prevent Chronic Disease. La Revue du Praticien, 59, 61-65.
[3]
Sirtori, C.R., Galli, C., Anderson, J.W. and Arnoldi, A. (2009) Nutritional and Nutraceutical Approaches to Dyslipidemia and Atherosclerosis Prevention: Focus on Dietary Proteins. Atherosclerosis, 203, 8-17.
http://dx.doi.org/10.1016/j.atherosclerosis.2008.06.019
[4]
Barnes, S. (2004) Soy Isoflavones-Phytoestrogens and What Else? The Journal of Nutrition, 134, 1225S-1228S.
[5]
de Meijer, V.E., Le, H.D., Meisel, J.A., Akhavan Sharif, M.R., Pan, A., Nosé, V. and Puder, M. (2010) Dietary Fat Intake Promotes the Development of Hepatic Steatosis Independently from Excess Caloric Consumption in a Murine Model. Metabolism, 59, 1092-1105. http://dx.doi.org/10.1016/j.metabol.2009.11.006
[6]
Shimano, H., Yahagi, N., Amemiya-Kudo, M., Hasty, A.H., Osuga, J., Tamura, Y., Shionoiri, F., Iizuka, Y., Ohashi, K., Harada, K., Gotoda, T., Ishibashi, S. and Yamada, N. (1999) Sterol Regulatory Element-Binding Protein-1 as a Key Transcription Factor for Nutritional Induction of Lipogenic Enzyme Genes. The Journal of Biological Chemistry, 274, 35832-35839. http://dx.doi.org/10.1074/jbc.274.50.35832
[7]
Shimomura, I., Bashmakov, Y., Ikemoto, S., Horton, J.D., Brown, M.S. and Goldstein, J.L. (1999) Insulin Selectively Increases SREBP-1c mRNA in the Livers of Rats with Streptozotocin-Induced Diabetes. Proceedings of the National Academy of Sciences of the United States of America, 96, 13656-13661. http://dx.doi.org/10.1073/pnas.96.24.13656
[8]
Kersten, S., Seydoux, J., Peters, J.M., Gonzalez, F.J., Desvergne, B. and Wahli, W. (1999) Peroxisome Proliferator-Activated Receptor α Mediates the Adaptive Response to Fasting. The Journal of Clinical Investigation, 103, 1489-1498. http://dx.doi.org/10.1172/JCI6223
[9]
Reeves, P.G., Nielsen, F.H. and Fahey Jr., G.C. (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. The Journal of Nutrition, 123, 1939-1951.
[10]
Yang, B., Chen, L., Qian, Y., Triantafillou, J.A., McNulty, J.A., Carrick, K., Clifton, L.G., Han, B., Geske, R., Strum, J., Brown, K.K., Stimpson, S.A. and Pahel, G. (2006) Changes of Skeletal Muscle Adiponectin Content in Diet-Induced Insulin Resistant Rats. Biochemical and Biophysical Research Communications, 341, 209-217.
http://dx.doi.org/10.1016/j.bbrc.2005.12.172
[11]
Hara, A. and Radin, N.S. (1978) Lipid Extraction of Tissues with a Low-Toxicity Solvent. Analytical Biochemistry, 90, 420-426. http://dx.doi.org/10.1016/0003-2697(78)90046-5
[12]
Folch, J., Lees, M. and Sloane Stanley, G.H. (1957) A Simple Method for the Isolation and Purification of Total Lipides from Animal Tissues. The Journal of Biological Chemistry, 226, 497-509.
[13]
Sardesai, V.M. and Manning, J.A. (1968) Determination of Triglycerides in Plasma and Tissues. Clinical Chemistry, 14, 156-161.
[14]
Layne, E. (1957) Spectrophotometric and Turbidimetric Methods for Measuring Proteins. In: Colowick, P.S. and Kaplan, N.O., Eds., Method in Enzymology, Academic Press, Inc., New York, 447-454.
http://dx.doi.org/10.1016/s0076-6879(57)03413-8
[15]
Marra, C.A. and de Alaniz, M.J. (1989) Influence of Testosterone Administration on the Biosynthesis of Unsaturated Fatty Acids in Male and Female Rats. Lipids, 24, 1014-1019. http://dx.doi.org/10.1007/BF02544071
[16]
Yamamoto, K., Shibahara, A., Nakayama, T. and Kajimoto, G. (1991) Determination of Double-Bond Positions in Methylene-Interrupted Dienoic Fatty Acids by GC-MS as Their Dimethyl Disulfide Adducts. Chemistry and Physics of Lipids, 60, 39-50. http://dx.doi.org/10.1016/0009-3084(91)90013-2
[17]
Snedecor, G.W. and Cochran, W.G. (1980) Statistical Methods. 7th Edition, Iowa State University Press, Ames.
[18]
Biesalski, H.K., Erdman Jr., J.W., Hathcock, J., Ellwood, K., Beatty, S., Johnson, E., Marchioli, R., Lauritzen, L., Rice, H.B., Shao, A. and Griffiths, J.C. (2013) Nutrient Reference Values for Bioactives: New Approaches Needed? A Conference Report. European Journal of Nutrition, 52, 1-9. http://dx.doi.org/10.1007/s00394-013-0503-0
[19]
Buettner, R., Scholmerich, J. and Bollheimer, L.C. (2007) High-Fat Diets: Modeling the Metabolic Disorders of Human Obesity in Rodents. Obesity, 15, 798-808. http://dx.doi.org/10.1038/oby.2007.608
[20]
Al-Dwairi, A., Pabona, J.M., Simmen, R.C. and Simmen, F.A. (2012) Cytosolic Malic Enzyme 1 (ME1) Mediates High Fat Diet-Induced Adiposity, Endocrine Profile, and Gastrointestinal Tract Proliferation-Associated Biomarkers in Male Mice. PLoS ONE, 7, e46716. http://dx.doi.org/10.1371/journal.pone.0046716
[21]
Torre-Villalvazo, I., Tovar, A.R., Ramos-Barragán, V.E., Cerbón-Cervantes, M.A. and Torres, N. (2008) Soy Protein Ameliorates Metabolic Abnormalities in Liver and Adipose Tissue of Rats Fed a High Fat Diet. The Journal of Nutrition, 138, 462-468.
[22]
Takahashi, Y. and Ide, T. (2008) Effects of Soy Protein and Isoflavone on Hepatic Fatty Acid Synthesis and Oxidation and mRNA Expression of Uncoupling Proteins and Peroxisome Proliferator-Activated Receptor Gamma in Adipose Tissues of Rats. The Journal of Nutritional Biochemistry, 19, 682-693. http://dx.doi.org/10.1016/j.jnutbio.2007.09.003
[23]
Li, J.J., Huang, C.J. and Xie, D. (2008) Anti-Obesity Effects of Conjugated Linoleic Acid, Docosahexaenoic Acid, and Eicosapentaenoic Acid. Molecular Nutrition and Food Research, 52, 631-645.
http://dx.doi.org/10.1002/mnfr.200700399
[24]
Grundy, S.M. and Abrams, J.J. (1983) Comparison of Actions of Soy Protein and Casein on Metabolism of Plasma Lipoproteins and Cholesterol in Humans. The American Journal of Clinical Nutrition, 38, 245-252.
[25]
Duane, W.C. (1999) Effects of Soybean Protein and Very Low Dietary Cholesterol on Serum Lipids, Biliary Lipids, and Fecal Sterols in Humans. Metabolism, 48, 489-494. http://dx.doi.org/10.1016/S0026-0495(99)90109-9
[26]
Crouse III, J.R., Morgan, T., Terry, J.G., Ellis, J., Vitolins, M. and Burke, G.L. (1999) A Randomized Trial Comparing the Effect of Casein with That of Soy Protein Containing Varying Amounts of Isoflavones on Plasma Concentrations of Lipids and Lipoproteins. Archives of Internal Medicine, 159, 2070-2076.
http://dx.doi.org/10.1001/archinte.159.17.2070
[27]
Ascencio, C., Torres, N., Isoard-Acosta, F., Gómez-Pérez, F.J., Hernández-Pando, R. and Tovar, A.R. (2004) Soy Protein Affects Serum Insulin and Hepatic SREBP-1 mRNA and Reduces Fatty Liver in Rats. The Journal of Nutrition, 134, 522-529.
[28]
Olofsson, S.O. and Boren, J. (2005) Apolipoprotein B: A Clinically Important Apolipoprotein Which Assembles Athe-rogenic Lipoproteins and Promotes the Development of Atherosclerosis. Journal of Internal Medicine, 258, 395-410.
http://dx.doi.org/10.1111/j.1365-2796.2005.01556.x
[29]
Xiao, C.W., Wood, C., Huang, W., L’Abbé, M.R., Gilani, G.S., Cooke, G.M. and Curran, I. (2006) Tissue-Specific Regulation of Acetyl-CoA Carboxylase Gene Expression by Dietary Soya Protein Isolate in Rats. British Journal of Nutrition, 95, 1048-1054. http://dx.doi.org/10.1079/BJN20061776
[30]
Shukla, A., Brandsch, C., Bettzieche, A., Hirche, F., Stangl, G.I. and Eder, K. (2007) Isoflavone-Poor Soy Protein Alters the Lipid Metabolism of Rats by SREBP-Mediated Down-Regulation of Hepatic Genes. The Journal of Nutritional Biochemistry, 18, 313-321. http://dx.doi.org/10.1016/j.jnutbio.2006.05.007
[31]
Rustan, A.C., Nossen, J.O., Christiansen, E.N. and Drevon, C.A. (1988) Eicosapentaenoic Acid Reduces Hepatic Synthesis and Secretion of Triacylglycerol by Decreasing the Activity of Acyl-Coenzyme A:1,2-Diacylglycerol Acyltrans-ferase. Journal of Lipid Research, 29, 1417-1426.
[32]
Mezei, O., Banz, W.J., Steger, R.W., Peluso, M.R., Winters, T.A. and Shay, N. (2003) Soy Isoflavones Exert Antidiabetic and Hypolipidemic Effects through the PPAR Pathways in Obese Zucker Rats and Murine RAW 264.7 Cells. The Journal of Nutrition, 133, 1238-1243.
[33]
Morifuji, M., Sanbongi, C. and Sugiura, K. (2006) Dietary Soya Protein Intake and Exercise Training Have an Additive Effect on Skeletal Muscle Fatty Acid Oxidation Enzyme Activities and mRNA Levels in Rats. British Journal of Nutrition, 96, 469-475.
[34]
Sampath, H. and Ntambi, J.M. (2004) Polyunsaturated Fatty Acid Regulation of Gene Expression. Nutrition Reviews, 62, 333-339. http://dx.doi.org/10.1111/j.1753-4887.2004.tb00058.x
[35]
Kassem, A.A., Abu Bakar, M.Z., Yong Meng, G. and Mustapha, N.M. (2012) Dietary (n-6:n-3) Fatty Acids Alter Plasma and Tissue Fatty Acid Composition in Pregnant Sprague Dawley Rats. The Scientific World Journal, 2012, Article ID: 851437. http://dx.doi.org/10.1100/2012/851437
[36]
Mohamed, A.I., Hussein, A.S., Bhathena, S.J. and Hafez, Y.S. (2002) The Effect of Dietary Menhaden, Olive, and Coconut Oil Fed with Three Levels of Vitamin E on Plasma and Liver Lipids and Plasma Fatty Acid Composition in Rats. The Journal of Nutritional Biochemistry, 13, 435-441. http://dx.doi.org/10.1016/S0955-2863(02)00196-1
[37]
Gentile, C.L. and Pagliassotti, M.J. (2008) The Role of Fatty Acids in the Development and Progression of Nonalcoholic Fatty Liver Disease. The Journal of Nutritional Biochemistry, 19, 567-576.
http://dx.doi.org/10.1016/j.jnutbio.2007.10.001
[38]
Simopoulos, A.P. (2008) The Importance of the Omega-6/Omega-3 Fatty Acid Ratio in Cardiovascular Disease and Other Chronic Diseases. Experimental Biology and Medicine, 233, 674-768. http://dx.doi.org/10.3181/0711-MR-311
[39]
Nakagawa, H., Yamamoto, D., Kiyozuka, Y., Tsuta, K., Uemura, Y., Hioki, K., Tsutsui, Y. and Tsubura, A. (2000) Effects of Genistein and Synergistic Action in Combination with Eicosapentaenoic Acid on the Growth of Breast Cancer Cell Lines. The Journal of Cancer Research and Clinical Oncology, 126, 448-454.
http://dx.doi.org/10.1007/s004320050012
[40]
Ward, W.E. and Fonseca, D. (2007) Soy Isoflavones and Fatty Acids: Effects on Bone Tissue Postovariectomy in Mice. Molecular Nutrition and Food Research, 51, 824-831. http://dx.doi.org/10.1002/mnfr.200600187