Dietary supplementation with soy isoflavones or replacement with soy proteins prevents hepatic lipid droplet accumulation and alters expression of genes involved in lipid metabolism in rats

Genes and Nutrition

Volumn 9, Issue 1, 2014, Pages

  Xiao, Chao Wu ^a,d   Wood, Carla M ^a   Weber, Dorcas ^b   Aziz, Syed A ^c   Mehta, Rekha ^c   Griffin, Philip ^a   Cockell, Kevin A ^a  

^a Health Canada and World Health Organization Collaborating Center for Standardization and Evaluation of Biologicals   (Canada)

^b FOOD RESEARCH DIVISION   (Canada)

^c TOXICOLOGY RESEARCH DIVISION   (Canada)

^d UNIVERSITY OF OTTAWA   (Canada)

Author keywords

Fatty liver; Gene expression; Isoflavones; Lipid metabolism; Soy proteins

Indexed keywords

CASEIN; FAT DROPLET; FAT SPECIFIC PROTEIN 27; ISOFLAVONE; LIVER PROTEIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA 2; SOYBEAN PROTEIN; TRIACYLGLYCEROL; UNCLASSIFIED DRUG;

AMINO ACID METABOLISM; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CHOLESTEROL METABOLISM; CONTROLLED STUDY; DIET SUPPLEMENTATION; DOWN REGULATION; FATTY ACID OXIDATION; FEMALE; FOOD COMPOSITION; GENE EXPRESSION; GLYCOLYSIS; LIPID LIVER LEVEL; LIPID METABOLISM; LIPOGENESIS; LIPOLYSIS; LIVER WEIGHT; MALE; NONHUMAN; PROTEIN ANALYSIS; PROTEIN CONTENT; PROTEOMICS; RAT; UPREGULATION;

RATTUS;

EID: 84888227781     PISSN: 15558932     EISSN: 18653499     Source Type: Journal    
DOI: 10.1007/s12263-013-0373-3     Document Type: Article

References (47)

1. Adams MR, Golden DL, Anthony MS, Register TC, Williams JK (2002) The inhibitory effect of soy protein isolate on atherosclerosis in mice does not require the presence of LDL receptors or alteration of plasma lipoproteins. J Nutr 132:43-49
2. Angulo P (2002) Nonalcoholic fatty liver disease. N Engl J Med 346:1221-1231
3. Anthony MS, Clarkson TB, Hughes CL, Morgan TM, Burke GL (1996) Soybean isoflavones improve cardiovascular risk factors without affecting the reproductive system of peripubertal rhesus monkeys. J Nutr 126:43-50
4. Badger TM, Ronis MJ, Wolff G, Stanley S, Ferguson M, Shankar K, Simpson P, Jo CH (2008) Soy protein isolate reduces hepatosteatosis in yellow Avy/a mice without altering coat color phenotype. Exp Biol Med (Maywood) 233:1242-1254
5. Bradbury MW (2006) Lipid metabolism and liver inflammation. I. Hepatic fatty acid uptake: possible role in steatosis. Am J Physiol Gastrointest Liver Physiol 290:G194-G198
6. Browning JD, Szczepaniak LS, Dobbins R, Nuremberg P, Horton JD, Cohen JC, Grundy SM, Hobbs HH (2004) Prevalence of hepatic steatosis in an urban population in the United States: impact of ethnicity. Hepatology 40:1387-1395
7. Crespillo A, Alonso M, Vida M, Pavon FJ, Serrano A, Rivera P, Romero-Zerbo Y, Fernandez-Llebrez P, Martinez A, Perez-Valero V, Bermudez-Silva FJ, Suarez J, de Fonseca FR (2011) Reduction of body weight, liver steatosis and expression of stearoyl-CoA desaturase 1 by the isoflavone daidzein in diet-induced obesity. Br J Pharmacol 164:1899-1915
8. Davis J, Higginbotham A, O'Connor T, Moustaid-Moussa N, Tebbe A, Kim YC, Cho KW, Shay N, Adler S, Peterson R, Banz W (2007) Soy protein and isoflavones influence adiposity and development of metabolic syndrome in the obese male ZDF rat. Ann Nutr Metab 51:42-52
9. Fassini PG, Noda RW, Ferreira ES, Silva MA, Neves VA, Demonte A (2011) Soybean glycinin improves HDL-C and suppresses the effects of rosuvastatin on hypercholesterolemic rats. Lipids Health Dis 10:165
10. Ferreira ES, Silva MA, Demonte A, Neves VA (2012) Beta-conglycinin combined with fenofibrate or rosuvastatin have exerted distinct hypocholesterolemic effects in rats. Lipids Health Dis 11:11
11. Folch J, Lees M, Sloane Stanley GH (1957) A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226:497-509
12. Forsythe WA (1995) Soy protein, thyroid regulation and cholesterol metabolism. J Nutr 125:619S-623S
13. Frigolet ME, Torres N, Uribe-Figueroa L, Rangel C, Jimenez-Sanchez G, Tovar AR (2011) White adipose tissue genome wide-expression profiling and adipocyte metabolic functions after soy protein consumption in rats. J Nutr Biochem 22:118-129
14. Greaves KA, Parks JS, Williams JK, Wagner JD (1999) Intact dietary soy protein, but not adding an isoflavone-rich soy extract to casein, improves plasma lipids in ovariectomized cynomolgus monkeys. J Nutr 129:1585-1592
15. Gudbrandsen OA, Wergedahl H, Mork S, Liaset B, Espe M, Berge RK (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 96:249-257
16. Hakkak R, Al Dwairi A, Fuchs GJ, Korourian S, Simmen FA (2012) Dietary soy protein induces hepatic lipogenic enzyme gene expression while suppressing hepatosteatosis in obese female Zucker rats bearing DMBA-initiated mammary tumors. Genes Nutr 7:549-558
17. Jenkins DJ, Kendall CW, Jackson CJ, Connelly PW, Parker T, Faulkner D, Vidgen E, Cunnane SC, Leiter LA, Josse RG (2002) Effects of high- and low-isoflavone soyfoods on blood lipids, oxidized LDL, homocysteine, and blood pressure in hyperlipidemic men and women. Am J Clin Nutr 76:365-372
18. Keller P, Petrie JT, De Rose P, Gerin I, Wright WS, Chiang SH, Nielsen AR, Fischer CP, Pedersen BK, MacDougald OA (2008) Fat-specific protein 27 regulates storage of triacylglycerol. J Biol Chem 283:14355-14365
19. Kim MH, Kang KS (2012) Isoflavones as a smart curer for non-alcoholic fatty liver disease and pathological adiposity via ChREBP and Wnt signaling. Prev Med 54:S57-S63
20. Kim MH, Kang KS, Lee YS (2010) The inhibitory effect of genistein on hepatic steatosis is linked to visceral adipocyte metabolism in mice with diet-induced non-alcoholic fatty liver disease. Br J Nutr 104:1333-1342
21. Kim MH, Park JS, Jung JW, Byun KW, Kang KS, Lee YS (2011) Daidzein supplementation prevents non-alcoholic fatty liver disease through alternation of hepatic gene expression profiles and adipocyte metabolism. Int J Obes 35:1019-1030
22. Kitawaki R, Nishimura Y, Takagi N, Iwasaki M, Tsuzuki K, Fukuda M (2009) Effects of Lactobacillus fermented soymilk and soy yogurt on hepatic lipid accumulation in rats fed a cholesterol-free diet. Biosci Biotechnol Biochem 73:1484-1488
23. Kumashiro N, Yoshimura T, Cantley JL, Majumdar SK, Guebre-Egziabher F, Kursawe R, Vatner DF, Fat I, Kahn M, Erion DM, Zhang XM, Zhang D, Manchem VP, Bhanot S, Gerhard GS, Petersen KF, Cline GW, Samuel VT, Shulman GI (2013) Role of patatin-like phospholipase domain-containing 3 on lipid-induced hepatic steatosis and insulin resistance in rats. Hepatology 57:1763-1772
24. Matsusue K, Kusakabe T, Noguchi T, Takiguchi S, Suzuki T, Yamano S, Gonzalez FJ (2008) Hepatic steatosis in leptin-deficient mice is promoted by the PPARgamma target gene Fsp27. Cell Metab 7:302-311
25. Medina-Gomez G, Virtue S, Lelliott C, Boiani R, Campbell M, Christodoulides C, Perrin C, Jimenez-Linan M, Blount M, Dixon J, Zahn D, Thresher RR, Aparicio S, Carlton M, Colledge WH, Kettunen MI, Seppanen-Laakso T, Sethi JK, O'Rahilly S, Brindle K, Cinti S, Oresic M, Burcelin R, Vidal-Puig A (2005) The link between nutritional status and insulin sensitivity is dependent on the adipocyte-specific peroxisome proliferator-activated receptor-gamma2 isoform. Diabetes 54:1706-1716
26. Miniello VL, Moro GE, Tarantino M, Natile M, Granieri L, Armenio L (2003) Soy-based formulas and phyto-oestrogens: a safety profile. Acta Paediatr Suppl 91:93-100
27. Mochizuki Y, Maebuchi M, Kohno M, Hirotsuka M, Wadahama H, Moriyama T, Kawada T, Urade R (2009) Changes in lipid metabolism by soy beta-conglycinin- derived peptides in HepG2 cells. J Agric Food Chem 57:1473-1480
28. Mohamed SS, Nallasamy P, Muniyandi P, Periyasami V, Carani VA (2009) Genistein improves liver function and attenuates non-alcoholic fatty liver disease in a rat model of insulin resistance. J Diabetes 1:278-287
29. Ong JP, Younossi ZM (2007) Epidemiology and natural history of NAFLD and NASH. Clin Liver Dis 11:1-16, vii
30. Pirazzi C, Adiels M, Burza MA, Mancina RM, Levin M, Ståhlman M, Taskinen MR, Orho-Melander M, Perman J, Pujia A, Andersson L, Maglio C, Montalcini T, Wiklund O, Boérn J, Romeo S (2012) Patatin-like phospholipase domain-containing 3 (PNPLA3) I148 M (rs738409) affects hepatic VLDL secretion in humans and in vitro. J Hepatol 57:1276-1282
31. Puri V, Konda S, Ranjit S, Aouadi M, Chawla A, Chouinard M, Chakladar A, Czech MP (2007) Fat-specific protein 27, a novel lipid droplet protein that enhances triglyceride storage. J Biol Chem 282:34213-34218
32. Puri V, Virbasius JV, Guilherme A, Czech MP (2008) RNAi screens reveal novel metabolic regulators: RIP140, MAP4k4 and the lipid droplet associated fat specific protein (FSP) 27. Acta Physiol (Oxf) 192:103-115
33. 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
34. Romeo S, Kozlitina J, Xing C, Pertsemlidis A, Cox D, Pennacchio LA, Boerwinkle E, Cohen JC, Hobbs HH (2008) Genetic variation in PNPLA3 confers susceptibility to nonalcoholic fatty liver disease. Nat Genet 40:1461-1465
35. Simmen FA, Mercado CP, Zavacki AM, Huang SA, Greenway AD, Kang P, Bowman MT, Prior RL (2010) Soy protein diet alters expression of hepatic genes regulating fatty acid and thyroid hormone metabolism in the male rat. J Nutr Biochem 21:1106-1113
36. Tachibana N, Iwaoka Y, Hirotsuka M, Horio F, Kohno M (2010) Beta-conglycinin lowers very-low-density lipoprotein-triglyceride levels by increasing adiponectin and insulin sensitivity in rats. Biosci Biotechnol Biochem 74:1250-1255
37. Takahashi Y, Konishi T (2011) Tofu (soybean curd) lowers serum lipid levels and modulates hepatic gene expression involved in lipogenesis primarily through its protein, not isoflavone, component in rats. J Agric Food Chem 59:8976-8984
38. Torres N, Torre-Villalvazo I, Tovar AR (2006) Regulation of lipid metabolism by soy protein and its implication in diseases mediated by lipid disorders. J Nutr Biochem 17:365-373
39. Torre-Villalvazo I, Tovar AR, Ramos-Barragan VE, Cerbon-Cervantes MA, Torres N (2008) Soy protein ameliorates metabolic abnormalities in liver and adipose tissue of rats fed a high fat diet. J Nutr 138:462-468
40. Tovar AR, Torres N (2010) The role of dietary protein on lipotoxicity. Biochim Biophys Acta 1801:367-371
41. Tovar AR, Murguia F, Cruz C, Hernandez-Pando R, Aguilar-Salinas CA, Pedraza-Chaverri J, Correa-Rotter R, Torres N (2002) A soy protein diet alters hepatic lipid metabolism gene expression and reduces serum lipids and renal fibrogenic cytokines in rats with chronic nephrotic syndrome. J Nutr 132:2562-2569
42. Tovar AR, Torre-Villalvazo I, Ochoa M, Elias AL, Ortiz V, Aguilar-Salinas CA, Torres N (2005) Soy protein reduces hepatic lipotoxicity in hyperinsulinemic obese Zucker fa/fa rats. J Lipid Res 46:1823-1832
43. Uno K, Yamada T, Ishigaki Y, Imai J, Hasegawa Y, Gao J, Kaneko K, Matsusue K, Yamazaki T, Oka Y, Katagiri H (2012) Hepatic peroxisome proliferator-activated receptor-gamma-fat-specific protein 27 pathway contributes to obesity-related hypertension via afferent vagal signals. Eur Heart J 33:1279-1289
44. Vidal-Puig A, Jimenez-Linan M, Lowell BB, Hamann A, Hu E, Spiegelman B, Flier JS, Moller DE (1996) Regulation of PPAR gamma gene expression by nutrition and obesity in rodents. J Clin Invest 97:2553-2561
45. Wang HJ, Murphy P (1994) Isoflavone content in commercial soybean foods. J Agric Food Chem 42:1666-1673
46. Yamazaki T, Kishimoto K, Miura S, Ezaki O (2012) Dietary beta-conglycinin prevents fatty liver induced by a high-fat diet by a decrease in peroxisome proliferator-activated receptor gamma2 protein. J Nutr Biochem 23:123-132
47. Zhou D, Lezmi S, Wang H, Davis J, Banz W, Chen H (2013) Fat accumulation in the liver of obese rats is alleviated by soy protein isolate through beta-catenin signaling. Obesity (Silver Spring). doi: 10.1002/oby.20421