Soy protein isoflavones differentially regulate liver X receptor isoforms to modulate lipid metabolism and cholesterol transport in the liver and intestine in mice

Diabetologia

Volumn 55, Issue 9, 2012, Pages 2469-2478

  Gonzalez Granillo M ^a   Steffensen, K R ^b   Granados, O ^a   Torres, N ^a   Korach Andre M ^b   Ortiz V ^a   Aguilar Salinas, C ^a   Jakobsson, T ^b   Diaz Villasenor A ^a   Loza Valdes, A ^a   Hernandez Pando, R ^a   Gustafsson, J A ^b,c   Tovar, A R ^a  

^a INSTITUTO NACIONAL DE CIENCIAS MÉDICAS Y NUTRICIÓN SALVADOR ZUBIRÁN   (Mexico)

^b KAROLINSKA INSTITUTE   (Sweden)

^c University of Houston   (United States)

Author keywords

AMPK; Cholesterol; Insulin resistance; Intestine; Isoflavones; Liver; LXR ; LXR ; Mice; Soy protein

Indexed keywords

ABC TRANSPORTER; BILE ACID; CHOLESTEROL; GENISTEIN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; INSULIN; ISOFLAVONE; ISOPROTEIN; LIPID; LIVER X RECEPTOR; SOYBEAN PROTEIN; TRIACYLGLYCEROL;

ANIMAL EXPERIMENT; ARTICLE; CHOLESTEROL BLOOD LEVEL; CHOLESTEROL DIET; CHOLESTEROL METABOLISM; CHOLESTEROL TRANSPORT; FATTY ACID METABOLISM; FATTY LIVER; GENE CONTROL; GENE TARGETING; GLUCOSE METABOLISM; INSULIN SENSITIVITY; INSULIN TOLERANCE TEST; INTESTINE; LIPID METABOLISM; LIVER; LIVER CELL; MALE; MOUSE; NONHUMAN; ORAL GLUCOSE TOLERANCE TEST; PRIORITY JOURNAL; TRIACYLGLYCEROL BLOOD LEVEL; WILD TYPE;

ANIMALS; BILE ACIDS AND SALTS; BIOLOGICAL TRANSPORT; DIET, HIGH-FAT; GENE EXPRESSION REGULATION; HEPATOCYTES; INSULIN RESISTANCE; INTESTINES; ISOFLAVONES; LIPID METABOLISM; LIVER; MALE; MICE; MICE, TRANSGENIC; ORPHAN NUCLEAR RECEPTORS; PROTEIN ISOFORMS; SOYBEAN PROTEINS;

EID: 84866074532     PISSN: 0012186X     EISSN: 14320428     Source Type: Journal    
DOI: 10.1007/s00125-012-2599-9     Document Type: Article

References (45)

1. Wiklund P, Toss F, Weinehall L et al (2008) Abdominal and gynoid fat mass are associated with cardiovascular risk factors in men and women. J Clin Endocrinol Metab 93:4360-4366
2. Houston DK, Nicklas BJ, Zizza CA (2009) Weighty concerns: the growing prevalence of obesity among older adults. J Am Diet Assoc 109:1886-1895
3. Despres JP, Lemieux I (2006) Abdominal obesity and metabolic syndrome. Nature 444:881-887
4. Cornier MA, Dabelea D, Hernandez TL et al (2008) The metabolic syndrome. Endocr Rev 29:777-822
5. Doria A, Patti ME, Kahn CR (2008) The emerging genetic architecture of type 2 diabetes. Cell Metab 8:186-200
6. Grundy SM, Cleeman JI, Merz CN et al (2004) Implications of recent clinical trials for the National Cholesterol Education Program Adult Treatment Panel III guidelines. Circulation 110:227-239
7. Mathieu P, Poirier P, Pibarot P, Lemieux I, Despres JP (2009) Visceral obesity: the link among inflammation, hypertension, and cardiovascular disease. Hypertension 53:577-584
8. Olaiz-Fernandez G, Rivera-Dommarco J, Shamah-Levy T et al (2006) Encuesta Nacional de Salud y Nutricion. Instituo Nacional de Salud Publica, Cuernavaca
9. Ginsberg HN (2006) REVIEW: Efficacy and mechanisms of action of statins in the treatment of diabetic dyslipidemia. J Clin Endocrinol Metab 91:383-392
10. Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults (2001) Executive Summary of The Third Report of The National Cholesterol Education Program (NCEP) Expert Panel on Detection, Evaluation, And Treatment of High Blood Cholesterol In Adults (Adult Treatment Panel III). JAMA 285:2486-2497
11. Anderson JW, Johnstone BM, Cook-Newell ME (1995) Meta-analysis of the effects of soy protein intake on serum lipids. N Engl J Med 333:276-282
12. Zhan S, Ho SC (2005) Meta-analysis of the effects of soy protein containing isoflavones on the lipid profile. Am J Clin Nutr 81:397-408
13. Tovar AR, Murguia F, Cruz C et al (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
14. Tovar AR, Torre-Villalvazo I, Ochoa M et al (2005) Soy protein reduces hepatic lipotoxicity in hyperinsulinemic obese Zucker fa/fa rats. J Lipid Res 46:1823-1832
15. 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
16. Noriega-Lopez L, Tovar AR, Gonzalez-Granillo M et al (2007) Pancreatic insulin secretion in rats fed a soy protein high fat diet depends on the interaction between the amino acid pattern and isoflavones. J Biol Chem 282:20657-20666
17. Potter SM (1995) Overview of proposed mechanisms for the hypocholesterolemic effect of soy. J Nutr 125:606S-611S
18. Peet DJ, Turley SD, Ma W et al (1998) Cholesterol and bile acid metabolism are impaired in mice lacking the nuclear oxysterol receptor LXR alpha. Cell 93:693-704
19. Repa JJ, Berge KE, Pomajzl C, Richardson JA, Hobbs H, Mangelsdorf DJ (2002) Regulation of ATP-binding cassette sterol transporters ABCG5 and ABCG8 by the liver X receptors alpha and beta. J Biol Chem 277:18793-18800
20. Schroepfer GJ Jr (2000) Oxysterols: modulators of cholesterol metabolism and other processes. Physiol Rev 80:361-554
21. Gabbi C, Warner M, Gustafsson JA (2009) Minireview: liver X receptor beta: emerging roles in physiology and diseases. Mol Endocrinol 23:129-136
22. Lewis GF, Rader DJ (2005) New insights into the regulation of HDL metabolism and reverse cholesterol transport. Circ Res 96:1221-1232
23. Repa JJ, Mangelsdorf DJ (2000) The role of orphan nuclear receptors in the regulation of cholesterol homeostasis. Annu Rev Cell Dev Biol 16:459-481
24. Zelcer N, Tontonoz P (2006) Liver X receptors as integrators of metabolic and inflammatory signaling. J Clin Invest 116:607-614
25. Hwahng SH, Ki SH, Bae EJ, Kim HE, Kim SG (2009) Role of adenosine monophosphate-activated protein kinase-p70 ribosomal S6 kinase-1 pathway in repression of liver X receptor-alpha-dependent lipogenic gene induction and hepatic steatosis by a novel class of dithiolethiones. Hepatology 49:1913-1925
26. Torra IP, Ismaili N, Feig JE et al (2008) Phosphorylation of liver X receptor alpha selectively regulates target gene expression in macrophages. Mol Cell Biol 28:2626-2636
27. Shen P, Liu MH, Ng TY, Chan YH, Yong EL (2006) Differential effects of isoflavones, from Astragalus membranaceus and Pueraria thomsonii, on the activation of PPARalpha, PPARgamma, and adipocyte differentiation in vitro. J Nutr 136:899-905
28. Kuiper GG, Lemmen JG, Carlsson B et al (1998) Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor beta. Endocrinology 139:4252-4263
29. Shay NF, Banz WJ (2005) Regulation of gene transcription by botanicals: novel regulatory mechanisms. Annu Rev Nutr 25:297-315
30. Alberti S, Schuster G, Parini P et al (2001) Hepatic cholesterol metabolism and resistance to dietary cholesterol in LXRbeta-deficient mice. J Clin Invest 107:565-573
31. 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
32. Chomczynski P, Sacchi N (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162:156-159
33. Barakat HA, Dohm GL, Loesche P, Tapscott EB, Smith C (1976) Lipid content and fatty acid composition of heart and muscle of the BIO 82.62 cardiomyopathic hamster. Lipids 11:747-751
34. Keller S, Jahreis G (2004) Determination of underivatised sterols and bile acid trimethyl silyl ether methyl esters by gas chromatography-mass spectrometry-single ion monitoring in faeces. J Chromatogr B Analyt Technol Biomed Life Sci 813:199-207
35. Berry MN, Friend DS (1969) High-yield preparation of isolated rat liver parenchymal cells: a biochemical and fine structural study. J Cell Biol 43:506-520
36. Korach-Andre M, Parini P, Larsson L, Arner A, Steffensen KR, Gustafsson JA (2010) Separate and overlapping metabolic functions of LXRalpha and LXRbeta in C57Bl/6 female mice. Am J Physiol Endocrinol Metab 298:E167-E178
37. Samuel VT, Petersen KF, Shulman GI (2010) Lipid-induced insulin resistance: unravelling the mechanism. Lancet 375:2267-2277
38. Ronis MJ, Chen Y, Badeaux J, Badger TM (2009) Dietary soy protein isolate attenuates metabolic syndrome in rats via effects on PPAR, LXR, and SREBP signaling. J Nutr 139:1431-1438
39. Ricketts ML, Moore DD, Banz WJ, Mezei O, Shay NF (2005) Molecular mechanisms of action of the soy isoflavones includes activation of promiscuous nuclear receptors. A review. J Nutr Biochem 16:321-330
40. Hwang JT, Park IJ, Shin JI et al (2005) Genistein, EGCG, and capsaicin inhibit adipocyte differentiation process via activating AMP-activated protein kinase. Biochem Biophys Res Commun 338:694-699
41. Palacios-Gonzalez B, Torres N, Tovar AR (2011) Genistein stimulates AMPK-phosphorylation and expression of genes involved in fatty acid oxidation in skeletal muscle. FASEB J 25:772.777
42. Fabbrini E, Magkos F, Mohammed BS et al (2009) Intrahepatic fat, not visceral fat, is linked with metabolic complications of obesity. Proc Natl Acad Sci U S A 106:15430-15435
43. Hessvik NP, Boekschoten MV, Baltzersen MA et al (2010) LXR{beta} is the dominant LXR subtype in skeletal muscle regulating lipogenesis and cholesterol efflux. Am J Physiol Endocrinol Metab 298:E602-E613
44. Anderson JW, Bush HM (2011) Soy protein effects on serum lipoproteins: a quality assessment and meta-analysis of randomized, controlled studies. J Am Coll Nutr 30:79-91
45. Jenkins DJ, Mirrahimi A, Srichaikul K et al (2010) Soy protein reduces serum cholesterol by both intrinsic and food displacement mechanisms. J Nutr 140:2302S-2311S