Quercetin decreases the triglyceride content through the PPAR signalling pathway in primary hepatocytes of broiler chickens

References

• Panche AN, Diwan AD, Chandra SR. Flavonoids: an overview. J Nutr Sci. 2016 [cited 2019 Jun 13];5:e47.
   PubMed Web of Science ®Google Scholar
• González-Gallego J, García-Mediavilla MV, Sánchez-Campos S, et al. Fruit polyphenols, immunity and inflammation. Br J Nutr. 2010;104:S15–S27.
   PubMed Web of Science ®Google Scholar
• Brenes A, Viveros A, Goni I, et al. Effect of grape pomace concentrate and vitamin e on digestibility of polyphenols and antioxidant activity in chickens. Poult. Sci. 2008;87:307–316.
   PubMed Web of Science ®Google Scholar
• Goni I, Brenes A, Centeno C, et al. Effect of dietary grape Pomace and vitamin e on growth performance, nutrient digestibility, and susceptibility to meat lipid oxidation in chickens. Poult. Sci. 2007;86:508–516.
   PubMed Web of Science ®Google Scholar
• Ouyang KH, Xu MS, Jiang Y, et al. Effects of alfalfa flavonoids on broiler performance, meat quality, and gene expression. Can J Anim Sci. 2016;96:332–341.
   Web of Science ®Google Scholar
• Wang Y, Cheng QM, Cao WX, et al. The effects of the extract mixture of alfalfa and perilla oil lowering serum lipid, protecting liver and aortic wall in rats. Parenter Enter Nutr. 2005;12:219–222.
   Google Scholar
• Formica JV, Regelson W. Review of the biology of quercetin and related bioflavonoids. Food Chem. Toxicol. 1995;33:1061–1080.
   PubMed Web of Science ®Google Scholar
• Ross JA, Kasum CM. Dietary flavonoids: bioavailability, metabolic effects, and safety. Annu Rev Nutr. 2002;22:19–34.
   PubMed Web of Science ®Google Scholar
• Simona B, Mohamed MAD, Delia MT, et al. Health benefits of polyphenols and carotenoids in age-related eye diseases. Oxid Med Cell Longev. 2019;2019:1–22.
   Web of Science ®Google Scholar
• Perez-Vizcaino F, Duarte J, Jimenez R, et al. Antihypertensive effects of the flavonoid quercetin. Pharmacol Rep. 2009;61:67–75.
   PubMed Web of Science ®Google Scholar
• Han JJ, Hao J, Kim CH, et al. Quercetin prevents cardiac hypertrophy induced by pressure overload in rats. J Vet Med Sci. 2009;71:737–743.
   PubMed Web of Science ®Google Scholar
• Jung CH, Cho I, Ahn J, et al. Quercetin reduces high-fat diet-induced fat accumulation in the liver by regulating lipid metabolism genes. Phytother Res. 2013;27:139–143.
   PubMed Web of Science ®Google Scholar
• Aguirre L, Arias N, Macarulla MT, et al. Beneficial effects of quercetin on obesity and diabetes. Open Nutraceuticals J. 2011;4:189–198.
   Google Scholar
• Tang Z, Gao W, Yang J, et al. Effect of quercetin on cholesterol distribution in rats. Acta Nutr Sin. 2013;35:172–175.
   Google Scholar
• Liu W, Zhang M, Feng J, et al. The influence of quercetin on maternal immunity, oxidative stress, and inflammation in mice with exposure of fine particulate matter during gestation. Int J Environ Res Public Health. 2017;14:592.
   Web of Science ®Google Scholar
• Goliomytis M, Tsoureki D, Simitzis PE, et al. The effects of quercetin dietary supplementation on broiler growth performance, meat quality, and oxidative stability. Poult Sci. 2014;93:1957–1962.
   PubMed Web of Science ®Google Scholar
• Seglen PO. Preparation of isolated rat liver cells. Methods Cell Biol. 1976;13:29–83.
   PubMedGoogle Scholar
• Chen L, Jiang Q, Zhu X, et al. Isolation and primary culture of adult chicken liver cells. J. Jau. 2008;30:385–389.
   Google Scholar
• Liu K, Huang XH, Gao H, et al. In situ separation and long-term culture of adult chicken hepatocytes. Chin J Vet Sci. 2009;9:1193–1196.
   Google Scholar
• Hamamoto I, Nemoto EM, Zhang S, et al. Assessment of hepatic viability during cold ischemic preservation. Transpl Int. 1995;8:6.
   Web of Science ®Google Scholar
• Quesada H, Del-Bas JM, Pajuelo D, et al. Grape seed proanthocyanidins correct dyslipidemia associated with a high-fat diet in rats and repress genes controlling lipogenesis and VLDL assembling in liver. Int J Obes. 2009;33:1007–1012.
   PubMed Web of Science ®Google Scholar
• Jung UJ, Kim HJ, Lee JS, et al. Naringin supplementation lowers plasma lipids and enhances erythrocyte antioxidant enzyme activities in hypercholesterolemic subjects. Clin Nutr. 2003;22:561–568.
   PubMed Web of Science ®Google Scholar
• Zhai SW, Shi QC, Chen XH. Effects of dietary surfactin supplementation on growth performance, intestinal digestive enzymes activities and some serum biochemical parameters of tilapia (Oreochromis niloticus) fingerlings. Ital J Anim Sci. 2016;15:318–324.
   Web of Science ®Google Scholar
• Kuipers EN, Van Dam AD, et al. Quercetin lowers plasma triglycerides accompanied by white adipose tissue browning in diet-induced obese mice. Int J Mol Sci. 2018;9:1786.
   Google Scholar
• Dong PZ, Pan LL, Zhang XT, et al. Hawthorn (Crataegus pinnatifida Bunge) leave flavonoids attenuate atherosclerosis development in apo E knock-out mice. J Ethnopharmacol. 2017;198:479–488.
   PubMed Web of Science ®Google Scholar
• Jayaraman J, Namasivayam N. Effect of naringenin (Citrus Flavanone) on lipid profile in ethanol-induced toxicity in rats. J Food Biol. 2012;36:502–511.
   Web of Science ®Google Scholar
• Mandard S, Muller M, Kersten S. Peroxisome proliferator activated receptor alpha target genes. Cell Mol. Life Sci. 2004;61:393–416.
   PubMed Web of Science ®Google Scholar
• Roepstorff C, Halberg N, Hillig T, et al. Malonyl-CoA and carnitine in regulation of fat oxidation in human skeletal muscle during exercise. Am J Physiol Endocrinol Metab. 2005;288:133–142.
   Web of Science ®Google Scholar
• Costet P, Legendre C, More J, et al. Peroxisome proliferator-activated receptor α- isoform deficiency leads to progressive dyslipidemia with sexually dimorphic obesity and steatosis. J Biol Chem. 1998;273:29577–29585.
   PubMed Web of Science ®Google Scholar
• Wu XC, Xu J. New role of hispidulin in lipid metabolism: PPARα activator. Lipids. 2016;51:1249–1257.
   PubMed Web of Science ®Google Scholar
• Cho KW, Kim YO, Andrade JE, et al. Dietary naringenin increases hepatic peroxisome proliferators-activated receptor α protein expression and decreases plasma triglyceride and adiposity in rats. Eur J Nutr. 2011;50:81–88.
   PubMed Web of Science ®Google Scholar
• Kim GS, Park HJ, Woo JH, et al. Citrus aurantium flavonoids inhibit adipogenesis through the Akt signaling pathway in 3T3-L1 cells. BMC Complement Altern Med. 2012;12:31.
   PubMed Web of Science ®Google Scholar
• Kim S, Shin HJ, Kim SY, et al. Genistein enhances expression of genes involved in fatty acid catabolism through activation of PPARα. Mol Cell Endocrinol. 2004;220:51–58.
   PubMed Web of Science ®Google Scholar
• Somerset SM, Johannot L. Dietary flavonoid sources in Australian adults. Nutr. Cancer. 2008;60:442–449.
   PubMed Web of Science ®Google Scholar
• Ding L, Liang XG, Zhu YD, et al. Icariin promotes expression of PGC-1α, PPARα, andNRF-1during cardiomyocyte differentiation of murine embryonic stem cells in vitro. Acta Pharm Sin. 2007;28:1541–1549.
   PubMed Web of Science ®Google Scholar
• Xiong D, Deng Y, Huang B, et al. Icariin attenuates cerebral ischemia-reperfusion injury through inhibition of inflammatory response mediated by NF-κB, PPARα and PPARγ in rats. Int Immunopharmacol. 2016;30:157–162.
   PubMed Web of Science ®Google Scholar
• Kobor I. M, Masumoto S, Akimoto Y, et al. Chronic dietary intake of quercetin alleviates hepatic fat accumulation associated with consumption of a Western-style diet in C57/BL6J mice. Mol Nutr Food Res. 2011;55:530–540.
   PubMed Web of Science ®Google Scholar
• Zimmerman AW, Veerkamp JH. New insights into the structure and function of fatty acid-binding proteinsl. Cell Mol Life Sci. 2002;59:1096–1116.
   PubMed Web of Science ®Google Scholar
• Olivares-Rubio HF, Vega-López A. Fatty acid metabolism in fish species as a biomarker for environmental monitoring. Environ Pollut. 2016;218:297–312.
   PubMed Web of Science ®Google Scholar
• Chmurzynska A. The multigene family of fatty acid-binding proteins (FABPs): function, structure and polymorphism. J Appl Gene. 2006;47:39–48.
   PubMed Web of Science ®Google Scholar
• Poirier H, Niot I, Monnot MC, et al. Differential involvement of peroxisome-proliferator activated receptors alpha and delta in fibrate and fatty-acid-mediated inductions of the gene encoding liver fatty-acid-binding protein in the liver and the small intestine. Biochem J. 2001;355:481–488.
   PubMed Web of Science ®Google Scholar
• Hertzel AV, Bernlohr DA. The mammalian fatty acid-binding protein multigene family: molecular and genetic insights into function. Trends Endocrinol Metab. 2000;11:175–180.
   PubMed Web of Science ®Google Scholar
• Gordon JI, Elshourbagy N, Low JB, et al. Tissue specific expression and developmental regulation of two genes coding for rat fatty acid binding proteins. J Biol Chem. 1985;260:1995–1998.
   PubMed Web of Science ®Google Scholar
• Newberry EP, Xie Y, Kennedy S, et al. Decreased hepatic triglyceride accumulation and altered fatty acid uptake in mice with deletion of the liver fatty acid-binding protein gene. J Biol Chem. 2003;278:51664–51672.
   PubMed Web of Science ®Google Scholar
• Wolfrum C, Borrmann CM, Borchers T, et al. Fatty acids and hypolipidemic drugs regulate peroxisome proliferator-activated receptors a- and g-mediated gene expression via liver fatty acid binding protein: a signaling path to the nucleus. PNAS. 2001;98:2323–2328.
   PubMed Web of Science ®Google Scholar
• Kim HK, Kim DS, Cho HY. Protective Effects of platycodi radix on alcohol-induced fatty liver. J Biosci Biotechnol Biochem. 2007;71:1550–1552.
   PubMed Web of Science ®Google Scholar
• Hostetler HA, Mcintosh AL, Atshaves BP, et al. L-FABP directly interacts with PPARα in cultured primary hepatocytes. J Lipid Res. 2009;50:1663–1675.
   PubMed Web of Science ®Google Scholar
• Brunham LR, Kruit JK, Jahangir I, et al. Intestinal ABCA1 directly contributes to HDL biogenesis in vivo. J Clin Investig. 2006;116:1052–1062.
   PubMed Web of Science ®Google Scholar
• Sliwkowski MB, Windmueller HG. Rat liver and small intestine produce proapo- lipoprotein A-I which is slowly processed to apolipoprotein A-I in the circulation. J Biol Chem. 1984;259:6459.
   PubMed Web of Science ®Google Scholar
• Wu AL, Windmueller HG. Relative contributions by liver and intestine to individual plasma apolipoproteins in the rat. J Biol Chem. 1979;254:7316–7322.
   PubMed Web of Science ®Google Scholar
• Mahley RW, Innerarity TL, Rall SC, et al. Plasma lipoproteins: apolipoprotein structure and function. J Lipid Res. 1984;25:1277–1294.
   PubMed Web of Science ®Google Scholar
• Mashek DG, Li LO, Coleman RA. Long-chain acyl-CoA synthetases and fatty acid channeling. Future Lipidol. 2007;2:465–476.
   PubMed Web of Science ®Google Scholar
• Hertz R, Bishara-Shieban J, Bar-Tana J. Mode of action of peroxisome proliferators as hypolipidemic drugs. Suppression of apolipoprotein C-III. J Biol Chem. 1995;270:13470–13475.
   PubMed Web of Science ®Google Scholar
• Ooi EM, Barrett PH, Chan DC, et al. Apolipoprotein C-III: understanding an emerging cardiovascular risk factor. Clin Sci. 2008;114: 611–624.
   PubMed Web of Science ®Google Scholar
• Del-Bas JM, Fernandez-Larrea J, Blay M, et al. Grape seed procyanidins improve atherosclerotic risk index and induce liver CYP7a1 and SHP expression in healthy rats. FASEB J. 2005;19:479–481.
   PubMed Web of Science ®Google Scholar
• Haas MJ, Onstead-Haas LM, Szafran-Swietlik A, et al. Induction of hepatic apolipoprotein A-I gene expression by the isoflavones quercetin and isoquercetrin. Life Sci. 2014;110:8–14.
   PubMed Web of Science ®Google Scholar
• Tocher DR. Metabolism and functions of lipids and fatty acids in teleost fish. Fish Sci. 2003;11:107–184.
   Web of Science ®Google Scholar
• Mashek DG, Li LO, Coleman RA. Rat long-chain acyl-CoA synthetase mRNA, protein, and activity vary in tissue distribution and in response to diet. J Lipid Res. 2006;47:2004–2010.
   PubMed Web of Science ®Google Scholar
• Li LO, Ellis JM, Paich HA, et al. Liver-specific loss of long chain acyl-CoA synthetase-1 decreases triacylglycerol synthesis and β-oxidation and alters phospholipid fatty acid composition. J Biol Chem. 2009;284:27816–27826.
   PubMed Web of Science ®Google Scholar
• Patsouris D, Reddy JK, Muller M, et al. Peroxisome proliferator activated receptor alpha mediates the effects of high-fat diet on hepatic gene expression. Endocrinology. 2006;147:1508–1516.
   PubMed Web of Science ®Google Scholar
• Cao A, Li H, Zhou Y, et al. Long chain acyl-coa synthetase-3 is a molecular target for peroxisome proliferator-activated receptor in hepg2 hepat- oma cells. J Biol Chem. 2010;285:16664–16674.
   PubMed Web of Science ®Google Scholar
• Martin G, Schoonjans K, Lefebvre AM, et al. Coordinate regulation of the expression of the fatty acid transport protein and acyl-CoA synthetase genes by PPARα and PPARγ activators. J Biol Chem. 1997;272:28210–28217.
   PubMed Web of Science ®Google Scholar
• Rakhshandehroo M, Hooiveld G, Muller M, et al. Comparative analysis of gene regulation by the transcription factor PPARα between mouse and human. Pub Lib Sci One. 2009;4:e6796.
   PubMed Web of Science ®Google Scholar
• Peters JM, Cattley RC, Gonzalez FJ. Role of PPARα in the mechanism of action of the nongenotoxic carcinogen and peroxisome proliferator Wy-14,643. Carcinogenesis. 1997;18:2029–2033.
   PubMed Web of Science ®Google Scholar
• Bonnefont JP, Djouadi F, Prip-Buus C, et al. Carnitine palmitoyltransferases 1 and 2: biochemical, molecular and medical aspects. Mol Asp Med. 2004;25:495–520.
   PubMedGoogle Scholar
• Muthukumaran P, Thiyagarajan G, Arun Babu R, et al. Raffinose from, Costus speciosus, attenuates lipid synthesis through modulation of PPARs/SREBP1c and improves insulin sensitivity through PI3K/AKT. Chem Biol Int. 2018;284:80–89.
   PubMed Web of Science ®Google Scholar
• Saneyasu T, Shiragaki M, Nakanishi K, et al. Effects of short term fasting on the expression of genes involved in lipid metabolism in chicks. Comp Biochem Phys B. 2013;165:114–118.
   PubMed Web of Science ®Google Scholar
• Arias N, Macarulla MT, Aguirre L, et al. Quercetin can reduce insulin resistance without decreasing adipose tissue and skeletal muscle fat accumulation. Genes Nutr. 2014;9:361.
   PubMed Web of Science ®Google Scholar