Food Science of Animal Resources (한국축산식품학회지)

Korean Society for Food Science of Animal Resources (한국축산식품학회)
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High Density Lipoprotein from Egg Yolk (EYHDL) Improves Dyslipidemia by Mediating Fatty Acids Metabolism in High Fat Diet-induced Obese Mice

  • Yu, Zhihui (National R&D Center for Egg Processing, College of Food Science and Technology, Huazhong Agricultural University) ;
  • Mao, Changyi (National R&D Center for Egg Processing, College of Food Science and Technology, Huazhong Agricultural University) ;
  • Fu, Xing (National R&D Center for Egg Processing, College of Food Science and Technology, Huazhong Agricultural University) ;
  • Ma, Meihu (National R&D Center for Egg Processing, College of Food Science and Technology, Huazhong Agricultural University)
  • Received : 2018.07.31
  • Accepted : 2018.09.17
  • Published : 2019.04.30
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Abstract

We investigated the effect of high density lipoprotein from egg yolk (EYHDL) on serum, hepatic and fecal lipid and fatty acids (FAs) levels and on gene expression involved in FAs metabolism. Male KM mice were fed either normal diet (ND; n=20), high fat diet (HFD; n=20), or high fat diet containing EYHDL (EYHDL; 0.6 mg/g, every day by oral gavage, n=20) for 100 days. At the end of the experiment, the effects of treatments on biochemical parameters, FAs profiles and involved gene expression were analyzed. Our results revealed that EYHDL markedly suppressed the body weight gain, accumulation of abdominal fat tissues, serum concentrations of LDL-cholesterol (LDL-C) and triglycerides, hepatic triglycerides and cholesterol accumulation, while increased serum concentration of HDL-cholesterol (HDL-C). EYHDL intake also increased total cholesterol (TC) excretions compared with HFD group. Moreover, it alleviated the severity of fatty liver and improved glucose and insulin tolerance compared with HFD. More importantly, EYHDL partially normalized FAs profiles in serum, liver and fecaces and neutralized the HFD-induced upregulation of SREBP-1c, Acaca, Fasn, GPAT and Scd1. In conclusion, our findings indicate that EYHDL may have the potential to improve metabolic disturbances that occur in HFD mice and can be considered as an appropriate dietary recommendation for the treatment of metabolic syndrome (MetS).

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References

  1. Aguilar M, Bhuket T, Torres S, Liu B, Wong RJ. 2015. Prevalence of the metabolic syndrome in the United States, 2003-2012. JAMA 313:1973-1974. https://doi.org/10.1001/jama.2015.4260
  2. Anderson TJ, Mancini GBJ, Genest J Jr, Gregoire J, Lonn EM, Hegele RA. 2015. The new dyslipidemia guidelines: What is the debate? Can J Cardiol 31:605-612. https://doi.org/10.1016/j.cjca.2014.11.007
  3. Angrish MM, Dominici CY, Zacharewski TR. 2013. TCDD-elicited effects on liver, serum, and adipose lipid composition in C57BL/6 mice. Toxicol Sci 131:108-115. https://doi.org/10.1093/toxsci/kfs277
  4. Ansell BJ, Watson KE, Fogelman AM, Navab M, Fonarow GC. 2005. High-density lipoprotein function: Recent advances. J Am Coll Cardiol 46:1792-1798. https://doi.org/10.1016/j.jacc.2005.06.080
  5. Blesso CN, Andersen CJ, Barona J, Volek JS, Fernandez ML. 2013. Whole egg consumption improves lipoprotein profiles and insulin sensitivity to a greater extent than yolk-free egg substitute in individuals with metabolic syndrome. Metabolism 62:400-410. https://doi.org/10.1016/j.metabol.2012.08.014
  6. Blesso CN. 2015. Egg phospholipids and cardiovascular health. Nutrients 7:2731-2747. https://doi.org/10.3390/nu7042731
  7. Broin PO, Vaitheesvaran B, Saha S, Hartil K, Chen EI, Goldman D, Fleming WH, Kurland IJ, Guha C, Golden A. 2015. Intestinal microbiota-derived metabolomic blood plasma markers for prior radiation injury. Int J Radiat Oncol Biol Phys 91:360-367. https://doi.org/10.1016/j.ijrobp.2014.10.023
  8. Brossard C, Rance F, Juchet A, Drouet M, Paty E, Legoue-Morillon S, Nau F, Anton M, Denery S. 2013. Revisiting egg yolk involvement in children's food allergy to egg. Clin Transl Allergy 3:86. https://doi.org/10.1186/2045-7022-3-S3-P86
  9. Chen L, Ren J, Yang L, Li Y, Fu J, Li Y, Tian Y, Qiu F, Liu Z, Qiu Y. 2016. Stearoyl-CoA desaturase-1 mediated cell apoptosis in colorectal cancer by promoting ceramide synthesis. Sci Rep 6:19665. https://doi.org/10.1038/srep19665
  10. Chong J, Soufan O, Li C, Caraus I, Li S, Bourque G, Wishart DS, Xia J. 2018. MetaboAnalyst 4.0: Towards more transparent and integrative metabolomics analysis. Nucleic Acids Res 46:486-494.
  11. DiMarco DM, Norris GH, Millar CL, Blesso CN, Fernandez ML. 2017. Intake of up to 3 eggs per day is associated with changes in HDL function and increased plasma antioxidants in healthy, young adults-3. J Nutr 147:323-329. https://doi.org/10.3945/jn.116.241877
  12. Doria ML, Ribeiro AS, Wang J, Catrim CZ, Domingues P, Williams C, Domingues MR, Helguero LA. 2014. Fatty acid and phospholipid biosynthetic pathways are regulated throughout mammary epithelial cell differentiation and correlate to breast cancer survival. FASEB J 28:4247-4264. https://doi.org/10.1096/fj.14-249672
  13. Dossi CG, Tapia GS, Espinosa A, Videla LA, D'Espessailles A. 2014. Reversal of high-fat diet-induced hepatic steatosis by n-3 LCPUFA: role of PPAR-$\alpha$ and SREBP-1c. J Nutr Biochem 25:977-984. https://doi.org/10.1016/j.jnutbio.2014.04.011
  14. Eckel RH, Grundy SM, Zimmet PZ. 2005. The metabolic syndrome. Lancet 365:1415-1428. https://doi.org/10.1016/S0140-6736(05)66378-7
  15. Eftekhar S, Parsaei H, Keshavarzi Z, Yazdi AT, Hadjzadeh MAR, Rajabzadeh A, Malayeri SO. 2015. The prevention and treatment effects of egg yolk high density lipoprotein on the formation of atherosclerosis plaque in rabbits. Iran J Basic Med Sci 18:343.
  16. Eisinger K, Krautbauer S, Hebel T, Schmitz G, Aslanidis C, Liebisch G, Buechler C. 2014. Lipidomic analysis of the liver from high-fat diet induced obese mice identifies changes in multiple lipid classes. Exp Mol Pathol 97:37-43. https://doi.org/10.1016/j.yexmp.2014.05.002
  17. Erami K, Tanaka Y, Kawamura S, Miyago M, Sawazaki A, Imaizumi K, Sato M. 2016. Dietary egg yolk supplementation improves low-protein-diet-induced fatty liver in rats. J Nutr Sci Vitaminol 62:240-248. https://doi.org/10.3177/jnsv.62.240
  18. Farrell NJ, Norris GH, Ryan J, Porter CM, Jiang C, Blesso CN. 2015. Black elderberry extract attenuates inflammation and metabolic dysfunction in diet-induced obese mice. Br J Nutr 114:1123-1131. https://doi.org/10.1017/S0007114515002962
  19. Folch J, Lees M, Sloane Stanley GH. 1957. A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226:497-509. https://doi.org/10.1016/S0021-9258(18)64849-5
  20. Huang J, Feng S, Liu A, Dai Z, Wang H, Reuhl K, Lu W, Yang CS. 2017. Green tea polyphenol EGCG alleviates metabolic abnormality and fatty liver by decreasing bile acid and lipid absorption in mice. Mol Nutr Food Res 62:1700696. https://doi.org/10.1002/mnfr.201700696
  21. Jelinska M, Bialek A, Gielecinska I, Mojska H, Tokarz A. 2017. Impact of conjugated linoleic acid administered to rats prior and after carcinogenic agent on arachidonic and linoleic acid metabolites in serum and tumors. Prostaglandins Leukot Essent Fatty Acids 126:1-8. https://doi.org/10.1016/j.plefa.2017.08.013
  22. Jump DB. 2011. Fatty acid regulation of hepatic lipid metabolism. Curr Opin Clin Nutr Metab Care 14:115-120. https://doi.org/10.1097/MCO.0b013e328342991c
  23. Kapourchali FR, Surendiran G, Goulet A, Moghadasian MH. 2016. The role of dietary cholesterol in lipoprotein metabolism and related metabolic abnormalities: A mini-review. Crit Rev Food Sci Nutr 56:2408-2415. https://doi.org/10.1080/10408398.2013.842887
  24. Karlsson H, Kontush A, James, RW. 2015. Functionality of HDL: Antioxidation and detoxifying effects. In High density lipoproteins. Von Eckardstein A, Kardassis D (eds). Springer, Cham, Switzerland. pp 207-228.
  25. Kassaify ZG, Li EWY, Mine Y. 2005. Identification of antiadhesive fraction(s) in nonimmunized egg yolk powder: In vitro study. J Agr Food Chem 53:4607-4614. https://doi.org/10.1021/jf0500031
  26. Kaur J. 2014. A comprehensive review on metabolic syndrome. Cardiol Res Pract 2014:943162. https://doi.org/10.1155/2014/943162
  27. Kim HJ, Miyazaki M, Ntambi JM. 2002. Dietary cholesterol opposes PUFA-mediated repression of the stearoyl-CoA desaturase-1 gene by SREBP-1 independent mechanism. J Lipid Res 43:1750-1757. https://doi.org/10.1194/jlr.M100433-JLR200
  28. Kontush A. 2015. HDL particle number and size as predictors of cardiovascular disease. Front Pharmacol 6:218. https://doi.org/10.3389/fphar.2015.00218
  29. Kotronen A, Velagapudi VR, Yetukuri L, Westerbacka J, Bergholm R, Ekroos K, Makkonen J, Taskinen MR, Oresic M, Yki-Jarvinen H. 2009. Serum saturated fatty acids containing triacylglycerols are better markers of insulin resistance than total serum triacylglycerol concentrations. Diabetologia 52:684-690. https://doi.org/10.1007/s00125-009-1282-2
  30. Kumadaki S, Matsuzaka T, Kato T, Yahagi N, Yamamoto T, Okada S, Kobayashi K, Takahashi A, Yatoh S, Suzuki H, Yamada N, Shimano H. 2008. Mouse Elovl-6 promoter is an SREBP target. Biochem Biophys Res Commun 368:261-266. https://doi.org/10.1016/j.bbrc.2008.01.075
  31. Lei B, Wu J. 2012. Purification of egg yolk phosvitin by anion exchange chromatography. J Chromatogr A 1223:41-46. https://doi.org/10.1016/j.chroma.2011.12.023
  32. Lemos BS, Medina-Vera I, Blesso CN, Fernandez ML. 2018. Intake of 3 eggs per day when compared to a choline bitartrate supplement, downregulates cholesterol synthesis without changing the LDL/HDL ratio. Nutrients 10:258. https://doi.org/10.3390/nu10020258
  33. Li X, Huang W, Gu J, Du X, Lei L, Yuan X, Sun G, Wang Z, Li X, Liu G. 2015. SREBP-1c overactivates ROS-mediated hepatic NF-${\kappa}B$ inflammatory pathway in dairy cows with fatty liver. Cell Signal 27:2099-2109. https://doi.org/10.1016/j.cellsig.2015.07.011
  34. Listenberger LL, Han X, Lewis SE, Cases S, Farese RV, Ory DS, Schaffer JE. 2003. Triglyceride accumulation protects against fatty acid-induced lipotoxicity. Proc Natl Acad Sci USA 100:3077-3082. https://doi.org/10.1073/pnas.0630588100
  35. Luo Y, Xiong R, Hou L, Li J, Chen J. 2010. Process for coproduction of crude immunoglobulin y and high-density lipoproteins from hen egg yolk. J Agric Food Chem 58:11420-11427. https://doi.org/10.1021/jf101808b
  36. Martineau MG, Raker C, Dixon PH, Chambers J, Machirori M, King NM, Hooks ML, Manoharan R, Chen K, Powrie R, Williamson C. 2015. The metabolic profile of intrahepatic cholestasis of pregnancy is associated with impaired glucose tolerance, dyslipidemia, and increased fetal growth. Diabetes Care 38:243-248. https://doi.org/10.2337/dc14-2143
  37. Missimer A, DiMarco DM, Andersen CJ, Murillo AG, Vergara-Jimenez M, Fernandez ML. 2017. Consuming two eggs per day, as compared to an oatmeal breakfast, decreases plasma ghrelin while maintaining the LDL/HDL ratio. Nutrients 9:89. https://doi.org/10.3390/nu9020089
  38. Murase T, Misawa K, Minegishi Y, Aoki M, Ominami H, Suzuki Y, Shibuya Y, Hase T. 2011. Coffee polyphenols suppress diet-induced body fat accumulation by downregulating SREBP-1c and related molecules in C57BL/6J mice. Am J Physiol Endocrinol Metab 300:122-133. https://doi.org/10.1152/ajpendo.00441.2010
  39. Neave HW, von Keyserlingk MAG, Weary DM, Zobel G. 2018. Feed intake and behavior of dairy goats when offered an elevated feed bunk. J Dairy Sci 101:3303-3310. https://doi.org/10.3168/jds.2017-13934
  40. Omasaki SK, Janssen K, Besson M, Komen H. 2017. Economic values of growth rate, feed intake, feed conversion ratio, mortality and uniformity for Nile tilapia. Aquaculture 481:124-132. https://doi.org/10.1016/j.aquaculture.2017.04.013
  41. Orsoni A, Therond P, Tan R, Giral P, Robillard P, Kontush A, Meikle PJ, Chapman MJ. 2016. Statin action enriches HDL3 in polyunsaturated phospholipids and plasmalogens and reduces LDL-derived phospholipid hydroperoxides in atherogenic mixed dyslipidemia. J Lipid Res 57:2073-2087. https://doi.org/10.1194/jlr.P068585
  42. Poret JM, Souza-Smith F, Marcell SJ, Gaudet DA, Tzeng TH, Braymer HD, Harrison-Bernard LM, Primeaux SD. 2018. High fat diet consumption differentially affects adipose tissue inflammation and adipocyte size in obesity-prone and obesityresistant rats. Int J Obes 42:535-541. https://doi.org/10.1038/ijo.2017.280
  43. Richard C, Cristall L, Fleming E, Lewis ED, Ricupero M, Jacobs RL, Field CJ. 2017. Impact of egg consumption on cardiovascular risk factors in individuals with type 2 diabetes and at risk for developing diabetes: A systematic review of randomized nutritional intervention studies. Can J Diabetes 41:453-463. https://doi.org/10.1016/j.jcjd.2016.12.002
  44. Shin S, Lee HW, Kim CE, Lim J, Lee JK, Lee SA, Kang D. 2017. Egg consumption and risk of metabolic syndrome in Korean adults: Results from the health examinees study. Nutrients 9:687. https://doi.org/10.3390/nu9070687
  45. Silva Figueiredo P, Inada AC, Ribeiro Fernandes M, Granja Arakaki D, Freitas KC, Avellaneda Guimaraes RC, Aragao do Nascimento V, Aiko Hiane P. 2018. An overview of novel dietary supplements and food ingredients in patients with metabolic syndrome and non-alcoholic fatty liver disease. Molecules 23:877. https://doi.org/10.3390/molecules23040877
  46. Spencer M, Yang L, Adu A, Finlin BS, Zhu B, Shipp LR, Rasouli N, Peterson CA, Kern PA. 2014. Pioglitazone treatment reduces adipose tissue inflammation through reduction of mast cell and macrophage number and by improving vascularity. PLoS One 9:e102190. https://doi.org/10.1371/journal.pone.0102190
  47. Stankovic MN, Mladenovic DR, Duricic I, Sobajic SS, Timic J, Jorgacevic B, Aleksic V, Vucevic DB, Jesic-Vukicevic R, Radosavljevic TS. 2014. Time-dependent changes and association between liver free fatty acids, serum lipid profile and histological features in mice model of nonalcoholic fatty liver disease. Arch Med Res 45:116-124. https://doi.org/10.1016/j.arcmed.2013.12.010
  48. Yang F, Ma M, Xu J, Yu X, Qiu N. 2012. An egg-enriched diet attenuates plasma lipids and mediates cholesterol metabolism of high-cholesterol fed rats. Lipids 47:269-277. https://doi.org/10.1007/s11745-011-3646-x
  49. Zhang X, Qiu N, Geng F, Ma M. 2011. Simply and effectively preparing high-purity phosvitin using polyethylene glycol and anion-exchange chromatography. J Sep Sci 34:3295-3301. https://doi.org/10.1002/jssc.201100601
  50. Zhang Y, Meng T, Zuo L, Bei Y, Zhang Q, Su Z, Huang Y, Pang J, Xiang Q, Yang H. 2017. Xyloketal B attenuates fatty acidinduced lipid accumulation via the SREBP-1c pathway in NAFLD models. Mar Drugs 15:163. https://doi.org/10.3390/md15060163

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