Modulation of cholesterol-related gene expression by ergosterol and ergosterol-enriched extracts obtained from Agaricus bisporus

European Journal of Nutrition

Volumn 55, Issue 3, 2016, Pages 1041-1057

  Gil Ramírez, Alicia ^a   Caz, Víctor ^b   Martin Hernandez, Roberto ^c   Marín, Francisco R ^a   Largo, Carlota ^b   Rodríguez Casado, Arantxa ^c   Tabernero, María ^b   Ruiz Rodríguez, Alejandro ^a   Reglero, Guillermo ^a,c   Soler Rivas, Cristina ^a  

^a CSIC   (Spain)

^b HOSPITAL UNIVERSITARIO LA PAZ IDIPAZ   (Spain)

^c IMDEA FOOD INSTITUTE   (Spain)

Author keywords

Cholesterol; Ergosterol; Gene expression; Low density array (LDA); Supercritical CO2 extraction; White button mushroom

Indexed keywords

BETA GLUCAN; CHOLESTEROL; DIACYLGLYCEROL ACYLTRANSFERASE 1; ERGOSTEROL; EZETIMIBE; HIGH DENSITY LIPOPROTEIN; LIPID; LOW DENSITY LIPOPROTEIN RECEPTOR; MESSENGER RNA; SIMVASTATIN; STEROL; TRIACYLGLYCEROL; CELL RECEPTOR; CHOLESTEROL INTAKE; DGAT1 PROTEIN, MOUSE; DIACYLGLYCEROL ACYLTRANSFERASE; FARNESOID X-ACTIVATED RECEPTOR; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; LOW DENSITY LIPOPROTEIN CHOLESTEROL; SREBF2 PROTEIN, HUMAN; SREBF2 PROTEIN, MOUSE; STEROL REGULATORY ELEMENT BINDING PROTEIN 2;

AGARICUS BISPORUS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CACO 2 CELL LINE; CELL COMPARTMENTALIZATION; CELL CULTURE; CELL TRANSPORT; CHEMICAL COMPOSITION; CHOLESTEROL DIET; CHOLESTEROL METABOLISM; CONTROLLED STUDY; DOWN REGULATION; FECES; GENE; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; HEPG2 CELL LINE; HUMAN; HUMAN CELL; IN VITRO STUDY; INTESTINE; LIPID ANALYSIS; LIPID LIVER LEVEL; LIVER; MALE; MICELLE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; TRANSCRIPTION REGULATION; UPREGULATION; ADMINISTRATION AND DOSAGE; AGARICUS; ANIMAL; BLOOD; C57BL MOUSE; CACO-2 CELL LINE; CHEMISTRY; CHOLESTEROL INTAKE; DRUG EFFECTS; GENETICS; HEP-G2 CELL LINE; LIPID DIET; METABOLISM;

AGARICUS; ANIMALS; BETA-GLUCANS; CACO-2 CELLS; CHOLESTEROL, DIETARY; CHOLESTEROL, HDL; CHOLESTEROL, LDL; DIACYLGLYCEROL O-ACYLTRANSFERASE; DIET, HIGH-FAT; DOWN-REGULATION; ERGOSTEROL; EZETIMIBE; FECES; GENE EXPRESSION REGULATION; HEP G2 CELLS; HUMANS; LIVER; MALE; MICE; MICE, INBRED C57BL; RECEPTORS, CYTOPLASMIC AND NUCLEAR; RNA, MESSENGER; SIMVASTATIN; STEROL REGULATORY ELEMENT BINDING PROTEIN 2; STEROLS; TRIGLYCERIDES; UP-REGULATION;

EID: 84928975508     PISSN: 14366207     EISSN: 14366215     Source Type: Journal    
DOI: 10.1007/s00394-015-0918-x     Document Type: Article

References (48)

1. Gil-Ramirez A, Soler-Rivas C (2014) The use of edible mushroom extracts as bioactive ingredients to design novel functional foods with hypocholesterolemic activities. In: Pesti G (ed) Cultivation, antioxidant properties and health benefits. Nova Publishers, New York, pp 43–73
2. Jeong SC, Jeong YT, Yang BK, Islam R, Koyyalamudi SR, Pang G, Cho KY, Song CH (2010) White button mushroom (Agaricus bisporus) lowers blood glucose and cholesterol levels in diabetic and hypercholesterolemic rats. Nutr Res 30(1):49–56
3. Calpe-Berdiel L, Escolà-Gil JC, Blanco-Vaca F (2009) New insights into the molecular actions of plant sterols and stanols in cholesterol metabolism. Atherosclerosis 203:18–31
4. Lammert F, Wang DQH (2005) New insights into the genetic regulation of intestinal cholesterol absorption. Gastroenterol J 129:718–734
5. Gil-Ramírez A, Ruiz-Rodríguez A, Marín FR, Reglero G, Soler-Rivas C (2014) Effect of ergosterol-enriched extracts obtained from Agaricus bisporus on cholesterol absorption using an in vitro digestion model. J Funct Foods 11:589–597
6. Kaneko E, Matsuda M, Yamada Y, Tachibana Y, Shimomura I, Makishima M (2003) Induction of intestinal ATP-binding cassette transporters by a phytosterol-derived liver X receptor agonist. J Biol Chem 278(19):36098
7. Matsubara T, Li F, Gonzalez FJ (2013) FXR signaling in the enterohepatic system. Moll Cell Endocrinol 368(1–2):17–29
8. Miyata M, Hata T, Yamazoe Y, Yoshinari K (2014) SREBP-2 negatively regulates FXR-dependent transcription of FGF19 in human intestinal cells. Biochem Biophys Res Commun 443(2):477–482
9. Jesch ED, Seo JM, Carr TP, Lee JY (2009) Sitosterol reduces messenger RNA and protein expression levels of Niemann-Pick C1-like 1 in FHs 74 Int cells. Nutr Res 29:859–866
10. Gil-Ramírez A, Aldars-García L, Palanisamy M, Jiverdeanu RM, Ruiz-Rodríguez A, Marín FR, Reglero G, Soler-Rivas C (2013) Sterol enriched fractions obtained from Agaricus bisporus fruiting bodies and by-products by compressed fluid technologies (PLE and SFE). Innov Food Sci Emerg Technol 18:101–107
11. Van de Steeg E, Kleemann R, Jansen HT, van Duyvenvoorde W, Offerman EH, Wortelboer HM, Degroot J (2013) Combined analysis of pharmacokinetic and efficacy data of preclinical studies with statins markedly improves translation of drug efficacy to human trials. J Pharmacol Exp Ther 347:635–644
12. Lei YF, Chen JL, Wei H, Xiong CM, Zhang YH, Ruan JL (2011) Hypolipidemic and anti-inflammatory properties of Abacopterin A from Abacopteris penangiana in high-fat diet-induced hyperlipidemia mice. Food Chem Toxicol 49:3206–3210
13. Qin YW, Ye P, He JQ, Sheng L, Wang LY, Du J (2010) Simvastatin inhibited cardiac hypertrophy and fibrosis in apolipoprotein E-deficient mice fed a “Western-style diet” by increasing PPAR α and γ expression and reducing TC, MMP-9, and Cat S levels. Acta Pharmacol Sin 31:1350–1358
14. Zúñiga S, Molina H, Azocar L, Amigo L, Nervi F, Pimentel F, Jarufe N, Arrese M, Lammert F, Miquel JF (2008) Ezetimibe prevents cholesterol gallstone formation in mice. Liver Int 28:935–947
15. Wang HH, Portincasa P, Mendez-Sanchez N, Uribe M, Wang DQ (2008) Effect of ezetimibe on the prevention and dissolution of cholesterol gallstones. Gastroenterology 134:2101–2110
16. Muraoka T, Aoki K, Iwasaki T, Shinoda K, Nakamura A, Aburatani H, Mori S, Tokuyama K, Kubota N, Kadowaki T, Terauchi Y (2011) Ezetimibe decreases SREBP-1c expression in liver and reverses hepatic insulin resistance in mice fed a high-fat diet. Metabolism 60:617–628
17. Palanisamy M, Aldars-García L, Gil-Ramírez A, Ruiz-Rodríguez A, Marín FR, Reglero G, Soler-Rivas C (2014) Pressurized water extraction of β-glucan enriched fractions with bile acids-binding capacities obtained from edible mushrooms. Biotechnol Progr 30:391–400
18. Nitschke J, Altenbach HJ, Malolepszy T, Mölleken H (2011) A new method for the quantification of chitin and chitosan in edible mushrooms. Carbohydr Res 346:1307–1310
19. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3(7):1–12
20. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT–PCR. Nucleic Acids Res 29(9):e45
21. Fukushima M, Nakano M, Morii Y, Ohashi T, Fujiwara Y, Sonoyama K (2010) Hepatic LDL receptor mRNA in rats is increased by dietary mushroom (Agaricus bisporus) fiber and sugar beet fiber. J Nutr 130:2151–2156
22. Ikemoto S, Takahashi M, Tsunoda N, Maruyama K, Itakura H, Kawanaka K, Tabata I, Higuchi M, Tange T, Yamamoto TT, Ezaki O (1997) Cholate inhibits high-fat diet-induced hyperglycemia and obesity with acyl-CoA synthetase mRNA decrease. Am J Physiol 273:E37–E45
23. Duan L-P, Wang HH, Wang DQ-H (2004) Cholesterol absorption is mainly regulated by the jejunal and ileal ATP-binding cassette sterol efflux transporters Abcg5 and Abcg8 in mice. J Lipid Res 45(7):1312–1323
24. Field FJ, Born E, Mathur SN (1997) Effect of micellar β-sitosterol on cholesterol metabolism in CaCo-2 cells. J Lipid Res 38:348–360
25. Plat J, Mensink RP (2002) Increased intestinal ABCA1 expression contributes to the decrease in cholesterol absorption after plant stanol consumption. FASEB J 16(10):1248–1253
26. Field FJ, Born E, Mathur SN (2004) LXR/RXR ligand activation enhances basolateral efflux of β-sitosterol in CaCo-2 cells. J Lipid Res 45:905–913
27. Petruzzelli M, Groen AK, van Erpecum KJ, Vrins C, van der Velde AE, Portincasa P, Palasciano G, van Berge Henegouwen GP, Lo Sasso G, Morgano A, Moschetta A (2009) Micellar lipid composition profoundly affects LXR-dependent cholesterol transport across CaCo2 cells. FEBS Lett 583:1274–1280
28. EFSA Panel on Dietetic Products, Nutrition and Allergies (NDA) (2010) Scientific Opinion on the substantiation of health claims related to plant sterols and plant stanols and maintenance of normal blood cholesterol concentrations (ID 549, 550, 567, 713, 1234, 1235, 1466, 1634, 1984, 2909, 3140), and maintenance of normal prostate size and normal urination (ID 714, 1467, 1635) pursuant to Article 13(1) of Regulation (EC) No 1924/2006. EFSA J 8:1813–1834. Available online: www.efsa.europa.eu/en/publications/efsajournal.htm
29. Reagan-Shaw S, Nihal M, Ahmad N (2008) Dose translation from animal to human studies revisited. FASEB J 22:659–661
30. Verbraecken J, Van de Heyning P, De Backer W, Van Gaal L (2006) Body surface area in normal-weight, overweight, and obese adults. A comparison study. Metabolism 5:515–524
31. EFSA Panel on Dietetic Products, Nutrition and Allergies (NDA) (2008) Scientific opinion of the panel on dietetic products nutrition and allergies on a request from Unilever PLC/NV on plant sterols and lower/reduced blood cholesterol, reduced the risk of (coronary) heart disease. EFSA J 781:1–12. Available online: www.efsa.europa.eu/en/publications/efsajournal.htm
32. Plat J, Mensink RP (2001) Effects of plant stanol esters on LDL receptor protein expression and on LDL receptor and HMG-CoA reductase mRNA expression in mononuclear blood cells of healthy men and women. FASEB J 16(2):258–260
33. Calpe-Berdiel L, Escolΰ-Gil JC, Ribas V, Navarro-Sastre A, Garcιs-Garcιs J, Blanco-Vaca F (2005) Changes in intestinal and liver global gene expression in response to a phytosterol-enriched diet. Atherosclerosis 181(1):75–85
34. Fukushima M, Ohashi T, Fujiwara Y, Sonoyama K, Nakano M (2001) Cholesterol-lowering effects of maitake (Grifola frondosa) fiber, shiitake (Lentinus edodes) fiber, and enokitake (Flammulina velutipes) fiber in rats. Exp Biol Med 226:758–765
35. Gil-Ramirez A, Soler-Rivas C (2014) The use of edible mushroom extracts as bioactive ingredients to design novel functional foods with hypocholesterolemic activities. In: GrégoirePesti (ed) Mushrooms: cultivation, antioxidant properties and health benefits. Nova Science Publishers, Inc. Hauppauge, NY, pp 43–73
36. Bobek P, Ozdín L, Kuniak L (1997) Effect of oyster mushroom and isolated β-glucan on lipid peroxidation and on the activities of antioxidative enzymes in rats fed the cholesterol diet. J Nut Biochem 8:469–471
37. Carter SJ, Roberts MB, Salter J, Eaton CB (2010) Relationship between Mediterranean Diet Score and atherothrombotic risk: findings from the Third National Health and Nutrition Examination Survey (NHANES III), 1988–1994. Atherosclerosis 210:630–636
38. Carter B, Taylor O, Prendergast D, Zimmerman T, Von Furstenberg R, Moore D, Karpen S (2007) Stigmasterol, a soy lipid–derived phytosterol, is an antagonist of the bile acid Nnuclear receptor FXR. Pediatr Res 62(3):301–306
39. Yang C, Yu L, Li W, Xu F, Cohen JC, Hobbs HH (2004) Disruption of cholesterol homeostasis by plant sterols. J Clin Invest 114(6):813–822
40. Yang C, McDonald JG, Patel A, Zhang Y, Umetani M, Xu F, Westover EJ, Covey DF, Mangelsdorf DJ, Cohen JC, Hobbs HH (2006) Sterol intermediates from cholesterol biosynthetic pathway as liver X receptor ligands. J BiolChem 281(38):27816–27826
41. Cui J, Huang L, Zhao A, Lew J-L, Yu J, Sahoo S, Meinke PT, Royo I, Pelαez F, Wright SD (2003) Guggulsterone is a farnesoid X receptor antagonist in coactivator association assays but acts to enhance transcription of bile salt export pump. J BiolChem 278(12):10214–10220
42. Garcia-Calvo M, Lisnock J, Bull HG, Hawes BE, Burnett DA, Braun MP, Crona JH, Davis HR, Dean DC, Detmers PA, Graziano MP, Hughes M, MacIntyre DE, Ogawa A, O’Neill KA, Iyer SPN, Shevell DE, Smith MM, Tang YS, Makarewicz AM, Ujjainwalla F, Altmann SW, Chapman KT, Thornberry NA (2005) The target of ezetimibe is Niemann-Pick C1-Like 1 (NPC1L1). Proc Natl Acad Sci USA 102(23):8132–8137
43. Watanabe M, Houten SM, Wang L, Moschetta A, Mangelsdorf DJ, Heyman RA, Moore DD, Auwerx J (2004) Bile acids lower triglyceride levels via a pathway involving FXR, SHP, and SREBP-1c. J Clin Invest 113:1408–1418
44. Kanaya N, Kubo M, Liu Z, Chu P, Wang C, Yuan YC, Chen S (2011) Protective effects of white button mushroom (Agaricus bisporus) against hepatic steatosis in ovariectomized mice as a model of postmenopausal women. PLoS ONE 6:e26654
45. Inoue N, Inafuku M, Shirouchi B, Nagao K, Yanagita T (2013) Effect of Mukitake mushroom (Panellus serotinus) on the pathogenesis of lipid abnormalities in obese, diabetic ob/ob mice. Lipids Health Dis 12:18
46. Inafuku M, Nagao K, Nomura S, Shirouchi B, Inoue N, Nagamori N, Nakayama H, Toda T, Yanagita T (2012) Protective effects of fractional extracts from Panellus serotinus on non-alcoholic fatty liver disease in obese, diabetic db/db mice. Br J Nutr 107:639–646
47. Volger OL, van der Boom H, de Wit ECM, van Duyvenvoorde W, Hornstra G, Plat J, Havekes LM, Mensink RP, Princen HMG (2001) Dietary plant stanol esters reduce VLDL cholesterol secretion and bile saturation in apolipoprotein E*3-Leiden transgenic mice. Arterioscler Thromb Vasc Biol 21(6):1046–1052
48. Igel M, Giesa U, Lόtjohann D, von Bergmann K (2003) Comparison of the intestinal uptake of cholesterol, plant sterols, and stanols in mice. J Lipid Res 44(3):533–538