Journal of Nutrition and Health

The Korean Nutrition Society (한국영양학회)
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Sour cherry ameliorates hepatic lipid synthesis in high-fat diet-induced obese mice via activation of adenosine monophosphate-activated protein kinase signaling

  • Songhee Ahn (Department of Food and Nutrition, Sookmyung Women's University) ;
  • Minseo Kim (Department of Food and Nutrition, Sookmyung Women's University) ;
  • Hyun-Sook Kim (Department of Food and Nutrition, Sookmyung Women's University)
  • Received : 2023.11.20
  • Accepted : 2023.12.05
  • Published : 2023.12.31
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Abstract

Purpose: Sour cherry (Prunus cerasus L.) contains abounding phytochemicals, such as polyphenols and anthocyanins, and has antioxidative effects. Adenosine monophosphate-activated protein kinase (AMPK) is a crucial regulator in enhancing the lipid metabolism. This study hypothesized that the intake of sour cherry affects AMPK signaling. Therefore, this study examined whether sour cherry regulates AMPK to balance the hepatic lipid metabolism and exert ameliorating effects. Methods: Male C57BL/6J mice had obesity induced with a 45% fat diet. The mice were divided into four groups: control (CON), high-fat diet (HFD), low percentage sour cherry powder (LSC), and high percentage sour cherry powder (HSC). The mice in the sour cherry groups were fed 1% sour cherry or 5% sour cherry in their respective diets for 12 weeks. Results: The body weight, visceral fat weight, and lipid droplet size significantly decreased in the treatment groups. The serum and hepatic triglyceride and total cholesterol levels improved significantly in the HSC group. The low-density lipoprotein cholesterol levels were also reduced significantly, whereas the high-density lipoprotein cholesterol levels were increased significantly in both treatment groups. The sterol regulator binding protein-1c and fatty acid synthase expression levels as fatty acid synthesis-related enzymes were significantly lower in the treatment groups than in the high-fat diet group. Furthermore, the adipose triglyceride lipase and hormone-sensitive lipase expression levels as lipolytic enzyme activity and AMPK/acetyl-CoA carboxylase/carnitine palmitoyltransferase-1 as fatty acid β-oxidation-related pathway were upregulated significantly in both sour cherry groups. Conclusions: These results show that sour cherry intake improves hepatic lipid synthesis and chronic diseases by activating AMPK signaling. Therefore, this study suggests that phytochemical-rich sour cherry can be developed as a healthy functional food.

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References

  1. Korean Society of Lipid and Atherosclerosis. Dyslipidemia fact sheet 2022 [Internet]. Seoul: Korean Society of Lipid and Atherosclerosis; 2022 [cited 2023 Oct 10]. Available from: https://www.lipid.or.kr/bbs/index.html?code=fact_sheet&category=&gubun=&page=1&number=1264&mode=view&keyfield=&key=.
  2. Han KT, Kim SJ. Association between early treatment hospitals, serum cholesterol level and cardiovascular disease risk in dyslipidemia patients. Eur J Public Health 2021; 31(2): 265-271. https://doi.org/10.1093/eurpub/ckaa139
  3. Guo X, Zhang T, Shi L, Gong M, Jin J, Zhang Y, et al. The relationship between lipid phytochemicals, obesity and its related chronic diseases. Food Funct 2018; 9(12): 6048-6062. https://doi.org/10.1039/C8FO01026A
  4. Eslami O, Khoshgoo M, Shidfar F. Dietary phytochemical index and overweight/obesity in children: a cross-sectional study. BMC Res Notes 2020; 13(1): 132.
  5. Wojdylo A, Nowicka P, Laskowski P, Oszmianski J. Evaluation of sour cherry (Prunus cerasus L.) fruits for their polyphenol content, antioxidant properties, and nutritional components. J Agric Food Chem 2014; 62(51): 12332-12345. https://doi.org/10.1021/jf504023z
  6. Casedas G, Les F, Gomez-Serranillos MP, Smith C, Lopez V. Bioactive and functional properties of sour cherry juice (Prunus cerasus). Food Funct 2016; 7(11): 4675-4682. https://doi.org/10.1039/C6FO01295G
  7. Moruzzi M, Kloting N, Bluher M, Martinelli I, Tayebati SK, Gabrielli MG, et al. Tart cherry juice and seeds affect pro-inflammatory markers in visceral adipose tissue of high-fat diet obese rats. Molecules 2021; 26(5): 1403.
  8. Lee YM, Yoon Y, Yoon H, Park HM, Song S, Yeum KJ. Dietary anthocyanins against obesity and inflammation. Nutrients 2017; 9(10): 1089.
  9. Wang Y, Zhang Y, Wang X, Liu Y, Xia M. Cyanidin-3-O-β-glucoside induces oxysterol efflux from endothelial cells: role of liver X receptor alpha. Atherosclerosis 2012; 223(2): 299-305. https://doi.org/10.1016/j.atherosclerosis.2012.06.004
  10. Kim DO, Heo HJ, Kim YJ, Yang HS, Lee CY. Sweet and sour cherry phenolics and their protective effects on neuronal cells. J Agric Food Chem 2005; 53(26): 9921-9927. https://doi.org/10.1021/jf0518599
  11. Nguyen P, Leray V, Diez M, Serisier S, Le Bloc'h J, Siliart B, et al. Liver lipid metabolism. J Anim Physiol Anim Nutr (Berl) 2008; 92(3): 272-283. https://doi.org/10.1111/j.1439-0396.2007.00752.x
  12. Fang C, Pan J, Qu N, Lei Y, Han J, Zhang J, et al. The AMPK pathway in fatty liver disease. Front Physiol 2022; 13: 970292.
  13. Kim SJ, Tang T, Abbott M, Viscarra JA, Wang Y, Sul HS. AMPK phosphorylates desnutrin/ATGL and hormone-sensitive lipase to regulate lipolysis and fatty acid oxidation within adipose tissue. Mol Cell Biol 2016; 36(14): 1961-1976. https://doi.org/10.1128/MCB.00244-16
  14. Wang Q, Liu S, Zhai A, Zhang B, Tian G. AMPK-mediated regulation of lipid metabolism by phosphorylation. Biol Pharm Bull 2018; 41(7): 985-993. https://doi.org/10.1248/bpb.b17-00724
  15. Steinberg GR, Hardie DG. New insights into activation and function of the AMPK. Nat Rev Mol Cell Biol 2023; 24(4): 255-272. https://doi.org/10.1038/s41580-022-00547-x
  16. Bajcan D, Harangozo LHrabovska D, Boncikova D. Optimizing conditions for spectrophotometric determination of total polyphenols in wines using Folin-Ciocalteu reagent. J Microbiol Biotechnol Food Sci 2013; 2(1): 1699-1708.
  17. Monica Giusti M, Wrolstad RE. Characterization and measurement of anthocyanins by UV-visible spectroscopy. Handbook of food analytical chemistry. Hoboken (NJ): John Willey and Sons; 2005. p.19-31.
  18. Doeing DC, Borowicz JL, Crockett ET. Gender dimorphism in differential peripheral blood leukocyte counts in mice using cardiac, tail, foot, and saphenous vein puncture methods. BMC Clin Pathol 2003; 3(1): 3.
  19. Friedewald WT, Levy RI, Fredrickson DS. Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin Chem 1972; 18(6): 499-502. https://doi.org/10.1093/clinchem/18.6.499
  20. Folch J, Lees M, Sloane Stanley GH. A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 1957; 226(1): 497-509. https://doi.org/10.1016/S0021-9258(18)64849-5
  21. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976; 72(1-2): 248-254. https://doi.org/10.1006/abio.1976.9999
  22. Hussain MM. Intestinal lipid absorption and lipoprotein formation. Curr Opin Lipidol 2014; 25(3): 200-206. https://doi.org/10.1097/MOL.0000000000000084
  23. Danielewski M, Gomulkiewicz A, Kucharska AZ, Matuszewska A, Nowak B, Piorecki N, et al. Cornelian cherry (Cornus mas L.) iridoid and anthocyanin-rich extract reduces various oxidation, inflammation, and adhesion markers in a cholesterol-rich diet rabbit model. Int J Mol Sci 2023; 24(4): 3890.
  24. Seymour EM, Tanone II, Urcuyo-Llanes DE, Lewis SK, Kirakosyan A, Kondoleon MG, et al. Blueberry intake alters skeletal muscle and adipose tissue peroxisome proliferator-activated receptor activity and reduces insulin resistance in obese rats. J Med Food 2011; 14(12): 1511-1518. https://doi.org/10.1089/jmf.2010.0292
  25. Wang Y, Zhao L, Wang D, Huo Y, Ji B. Anthocyanin-rich extracts from blackberry, wild blueberry, strawberry, and chokeberry: antioxidant activity and inhibitory effect on oleic acid-induced hepatic steatosis in vitro. J Sci Food Agric 2016; 96(7): 2494-2503. https://doi.org/10.1002/jsfa.7370
  26. Bergman RN, Kim SP, Catalano KJ, Hsu IR, Chiu JD, Kabir M, et al. Why visceral fat is bad: mechanisms of the metabolic syndrome. Obesity (Silver Spring) 2006; 14 Suppl 1: 16S-19S. https://doi.org/10.1038/oby.2006.277
  27. Li Z, Liu H, Luo X. Lipid droplet and its implication in cancer progression. Am J Cancer Res 2020; 10(12): 4112-4122.
  28. Bonnefont-Rousselot D, Motta C, Khalil AO, Sola R, La Ville AE, Delattre J, et al. Physicochemical changes in human high-density lipoproteins (HDL) oxidized by gamma radiolysis-generated oxyradicals. Effect on their cholesterol effluxing capacity. Biochim Biophys Acta 1995; 1255(1): 23-30. https://doi.org/10.1016/0005-2760(94)00211-G
  29. Thilakarathna SH, Rupasinghe HP. Anti-atherosclerotic effects of fruit bioactive compounds: a review of current scientific evidence. Can J Plant Sci 2012; 92(3): 407-419. https://doi.org/10.4141/cjps2011-090
  30. Fan JG, Li F, Cai XB, Peng YD, Ao QH, Gao Y. Effects of nonalcoholic fatty liver disease on the development of metabolic disorders. J Gastroenterol Hepatol 2007; 22(7): 1086-1091. https://doi.org/10.1111/j.1440-1746.2006.04781.x
  31. Horton JD, Goldstein JL, Brown MS. SREBPs: activators of the complete program of cholesterol and fatty acid synthesis in the liver. J Clin Invest 2002; 109(9): 1125-1131. https://doi.org/10.1172/JCI0215593
  32. Wu JH, Lemaitre RN, Imamura F, King IB, Song X, Spiegelman D, et al. Fatty acids in the de novo lipogenesis pathway and risk of coronary heart disease: the Cardiovascular Health Study. Am J Clin Nutr 2011; 94(2): 431-438. https://doi.org/10.3945/ajcn.111.012054
  33. Tung YC, Hsieh PH, Pan MH, Ho CT. Cellular models for the evaluation of the antiobesity effect of selected phytochemicals from food and herbs. J Food Drug Anal 2017; 25(1): 100-110. https://doi.org/10.1016/j.jfda.2016.10.018
  34. Watt MJ, Steinberg GR. Regulation and function of triacylglycerol lipases in cellular metabolism. Biochem J 2008; 414(3): 313-325. https://doi.org/10.1042/BJ20080305
  35. Rupasinghe HP, Sekhon-Loodu S, Mantso T, Panayiotidis MI. Phytochemicals in regulating fatty acid β-oxidation: potential underlying mechanisms and their involvement in obesity and weight loss. Pharmacol Ther 2016; 165: 153-163. https://doi.org/10.1016/j.pharmthera.2016.06.005