Aged green tea reduces high-fat diet-induced fat accumulation and inflammation via activating the AMP-activated protein kinase signaling pathway

  • Ruohong Chen Tea Research Institute, Guangdong Academy of Agricultural Sciences/Guangdong Provincial Key Laboratory of Tea Plant Resources Innovation and Utilization, Guangzhou, China
  • Xingfei Lai Tea Research Institute, Guangdong Academy of Agricultural Sciences/Guangdong Provincial Key Laboratory of Tea Plant Resources Innovation and Utilization, Guangzhou, China
  • Limin Xiang Tea Research Institute, Guangdong Academy of Agricultural Sciences/Guangdong Provincial Key Laboratory of Tea Plant Resources Innovation and Utilization, Guangzhou, China
  • Qiuhua Li Tea Research Institute, Guangdong Academy of Agricultural Sciences/Guangdong Provincial Key Laboratory of Tea Plant Resources Innovation and Utilization, Guangzhou, China
  • Lingli Sun Tea Research Institute, Guangdong Academy of Agricultural Sciences/Guangdong Provincial Key Laboratory of Tea Plant Resources Innovation and Utilization, Guangzhou, China
  • Zhaoxiang Lai Tea Research Institute, Guangdong Academy of Agricultural Sciences/Guangdong Provincial Key Laboratory of Tea Plant Resources Innovation and Utilization, Guangzhou, China
  • Zhigang Li Tea Research Institute, Guangdong Academy of Agricultural Sciences/Guangdong Provincial Key Laboratory of Tea Plant Resources Innovation and Utilization, Guangzhou, China
  • Wenji Zhang Tea Research Institute, Guangdong Academy of Agricultural Sciences/Guangdong Provincial Key Laboratory of Tea Plant Resources Innovation and Utilization, Guangzhou, China
  • Shuai Wen Tea Research Institute, Guangdong Academy of Agricultural Sciences/Guangdong Provincial Key Laboratory of Tea Plant Resources Innovation and Utilization, Guangzhou, China
  • Junxi Cao Tea Research Institute, Guangdong Academy of Agricultural Sciences/Guangdong Provincial Key Laboratory of Tea Plant Resources Innovation and Utilization, Guangzhou, China
  • Shili Sun Tea Research Institute, Guangdong Academy of Agricultural Sciences/ Guangdong Provincial Key Laboratory of Tea Plant Resources Innovation & Utilization
Keywords: anti-obesity, anti-inflammation, AMPK, aged green tea, metabolism

Abstract

Background: Obesity is a global public health concern and increases the risk of metabolic syndrome and other diseases. The anti-obesity effects of various plant-derived bioactive compounds, such as tea extracts, are well-established. The mechanisms underlying the anti-obesity activity of Jinxuan green tea (JXGT) from different storage years are still unclear.

Objective: The aim of this study was to evaluate the effects of JXGTs from three different years on the high fat diet (HFD)-fed mouse model.

Design: The mice were divided into six groups, the control group received normal diet and the obese model group received HFD. We analyzed the effects of JXGTs from 2005, 2008, and 2016 on HFD-fed obese mice over a period of 7 weeks.

Results: The JXGTs reduced the body weight of the obese mice, and also alleviated fat accumulation and hepatic steatosis. Mechanistically, JXGTs increased the phosphorylation of AMP-activated protein kinase (p-AMPK)/AMP-activated protein kinase (AMPK) ratio, up-regulated carnitine acyl transferase 1A (CPT-1A), and down-regulated fatty acid synthase (FAS), Glycogen synthase kinase-3beta (GSK-3β), Peroxisome proliferator-activated receptor-gamma co-activator-1alpha (PGC-1α), Interleukin 6 (IL-6), and Tumour necrosis factor alpha (TNFα). Thus, JXGTs can alleviate HFD-induced obesity by inhibiting lipid biosynthesis and inflammation, thereby promoting fatty acid oxidation via the AMPK pathway.

Discussion: The anti-obesity effect of three aged JXGTs were similar. However, JXGT2016 exhibited a more potent activation of AMPK, and JXGT2005 and JXGT2008 exhibited a more potent inhibiting glycogen synthase and inflammation effect. Furthermore, the polyphenol (–)-epicatechin (EC) showed the strongest positive correlation with the anti-obesity effect of JXGT.

Conclusions: These findings demonstrate that JXGT treatment has a potential protection on HFD-induced obesity mice via activating the AMPK/CPT-1A and down-regulating FAS/GSK-3β/PGC-1α and IL-6/TNFα. Our study results also revealed that different storage time would not affect the anti-obesity and anti-inflammation effect of JXGT.

Downloads

Download data is not yet available.

References


  1. Lam DW, LeRoith D. The worldwide diabetes epidemic. Curr Opin Endocrinol Diabetes Obes 2012; 19: 93–96. doi: 10.1097/MED.0b013e328350583a

  2. Pichard C, Plu-Bureau G, Neves ECM, Gompel A. Insulin resistance, obesity and breast cancer risk. Maturitas 2008; 60: 19–30. doi: 10.1016/j.maturitas.2008.03.002

  3. Seravalle G, Grassi G. Obesity and hypertension. Pharmacol Res 2017; 122: 1–7. doi: 10.1016/j.phrs.2017.05.013

  4. Vecchie A, Dallegri F, Carbone F, Bonaventura A, Liberale L, Portincasa P, et al. Obesity phenotypes and their paradoxical association with cardiovascular diseases. Eur J Intern Med 2018; 48: 6–17. doi: 10.1016/j.ejim.2017.10.020

  5. Luo Y, Blackledge WC. Microbiome-based mechanisms hypothesized to initiate obesity-associated rheumatoid arthritis. Obes Rev 2018; 19: 786–97. doi: 10.1111/obr.12671

  6. Zhang WL, Zhu L, Jiang JG. Active ingredients from natural botanicals in the treatment of obesity. Obes Rev 2014; 15: 957–67. doi: 10.1111/obr.12228

  7. Hu S, Xu Y, Gao X, Li S, Jiang W, Liu Y, et al. Long-chain bases from sea cucumber alleviate obesity by modulating gut microbiota. Mar Drugs 2019; 17: 455. doi: 10.3390/md17080455

  8. Sheng Y, Liu J, Zheng S, Liang F, Luo Y, Huang K, et al. Mulberry leaves ameliorate obesity through enhancing brown adipose tissue activity and modulating gut microbiota. Food Funct 2019; 10: 4771–81. doi: 10.1039/c9fo00883g

  9. Chen G, Ni Y, Nagata N, Zhuge F, Xu L, Nagashimada M, et al. Lycopene alleviates obesity-induced inflammation and insulin resistance by regulating M1/M2 status of macrophages. Mol Nutr Food Res 2019; 63: e1900602. doi: 10.1002/mnfr.201900602

  10. Khan N, Mukhtar H. Tea polyphenols in promotion of human health. Nutrients 2018; 11: 39. doi: 10.3390/nu11010039

  11. Chen G, Chen R, Chen D, Ye H, Hu B, Zeng X, et al. Tea polysaccharides as potential therapeutic options for metabolic diseases. J Agricult Food Chem 2019; 67: 5350–60. doi: 10.1021/acs.jafc.8b05338

  12. Huang J, Wang Y, Xie Z, Zhou Y, Zhang Y, Wan X. The anti-obesity effects of green tea in human intervention and basic molecular studies. Eur J Clin Nnutr 2014; 68: 1075–87. doi: 10.1038/ejcn.2014.143

  13. Ling W, Li S, Zhang X, Xu Y, Gao Y, Du Q, et al. Evaluation of anti-obesity activity, acute toxicity, and subacute toxicity of probiotic dark tea. Biomolecules 2018; 8(4): 99. doi: 10.3390/biom8040099

  14. Jing N, Liu X, Jin M, Yang X, Hu X, Li C, et al. Fubrick tea attenuates high-fat diet induced fat deposition and metabolic disorder by regulating gut microbiota and caffeine metabolism. Food Funct 2020; 11: 6971–86. doi: 10.1039/d0fo01282c

  15. Ronnett GV, Kleman AM, Kim EK, Landree LE, Tu Y. Fatty acid metabolism, the central nervous system, and feeding. Obesity 2006; 14(Suppl 5): 201S–7S. doi: 10.1038/oby.2006.309

  16. Fang K, Wu F, Chen G, Dong H, Li J, Zhao Y, et al. Diosgenin ameliorates palmitic acid-induced lipid accumulation via AMPK/ACC/CPT-1A and SREBP-1c/FAS signaling pathways in LO2 cells. BMC Complement Alternat Med 2019; 19: 255. doi: 10.1186/s12906-019-2671-9

  17. Abbas NAT, Kabil SL. Liraglutide ameliorates cardiotoxicity induced by doxorubicin in rats through the Akt/GSK-3beta signaling pathway. Naunyn-Schmiedeberg’s Arch Pharmacol 2017; 390: 1145–53. doi: 10.1007/s00210-017-1414-z

  18. Timm KN, Tyler DJ. The role of AMPK activation for cardioprotection in doxorubicin-induced cardiotoxicity. Cardiovasc Drugs Ther 2020; 34: 255–69. doi: 10.1007/s10557-020-06941-x

  19. Liu C, Guo Y, Sun L, Lai X, Li Q, Zhang W, et al. Six types of tea reduce high-fat-diet-induced fat accumulation in mice by increasing lipid metabolism and suppressing inflammation. Food Funct 2019; 10: 2061–74. doi: 10.1039/c8fo02334d

  20. Zhang XB, Du XF. Effects of exogenous enzymatic treatment during processing on the sensory quality of summer tieguanyin oolong tea from the Chinese Anxi county. Food Technol Biotechnol 2015; 53: 180–9. doi: 10.17113/ftb.53.02.15.3642

  21. Du H, Wang Q, Yang X. Fu Brick tea alleviates chronic kidney disease of rats with high fat diet consumption through attenuating insulin resistance in skeletal muscle. J Agricult Food Chem 2019; 67: 2839–47. doi: 10.1021/acs.jafc.8b06927

  22. An R, Wen S, Li DL, Li QH, Lai XF, Zhang WJ, et al. Mixtures of tea and citrus maxima (pomelo) alleviate lipid deposition in HepG2 cells through the AMPK/ACC signaling pathway. J Med Food 2020; 23: 943–51. doi: 10.1089/jmf.2020.4706

  23. Li Q, Lai X, Sun L, Cao J, Ling C, Zhang W, et al. Antiobesity and anti-inflammation effects of Hakka stir-fried tea of different storage years on high-fat diet-induced obese mice model via activating the AMPK/ACC/CPT1 pathway. Food Nutr Res 2020; 64: 1681. doi: 10.29219/fnr.v64.1681

  24. Yuan E, Duan X, Xiang L, Ren J, Lai X, Li Q, et al. Aged oolong tea reduces high-fat diet-induced fat accumulation and dyslipidemia by regulating the AMPK/ACC signaling pathway. Nutrients 2018; 10: 187. doi: 10.3390/nu10020187

  25. Tiegs G. Cellular and cytokine-mediated mechanisms of inflammation and its modulation in immune-mediated liver injury. Zeitschrift fur Gastroenterologie 2007; 45: 63–70. doi: 10.1055/s-2006-927397

  26. Dorresteijn JA, Visseren FL, Spiering W. Mechanisms linking obesity to hypertension. Obes Rev 2012; 13: 17–26. doi: 10.1111/j.1467-789X.2011.00914.x

  27. Grundy SM. Metabolic syndrome update. Trends Cardiovasc Med 2016; 26: 364–73. doi: 10.1016/j.tcm.2015.10.004

  28. Diabetes Prevention Program Research G, Knowler WC, Fowler SE, Hamman RF, Christophi CA, Hoffman HJ, et al. 10-year follow-up of diabetes incidence and weight loss in the Diabetes Prevention Program Outcomes Study. Lancet 2009; 374: 1677–86. doi: 10.1016/S0140-6736(09)61457-4

  29. Jung UJ, Choi MS. Obesity and its metabolic complications: the role of adipokines and the relationship between obesity, inflammation, insulin resistance, dyslipidemia and nonalcoholic fatty liver disease. Int J Mol Sci 2014; 15: 6184–223. doi: 10.3390/ijms15046184

  30. Padwal RS, Majumdar SR. Drug treatments for obesity: orlistat, sibutramine, and rimonabant. Lancet 2007; 369: 71–77. doi: 10.1016/S0140-6736(07)60033-6

  31. Misawa K, Hashizume K, Yamamoto M, Minegishi Y, Hase T, Shimotoyodome A. Ginger extract prevents high-fat diet-induced obesity in mice via activation of the peroxisome proliferator-activated receptor delta pathway. J Nutr Biochem 2015; 26: 1058–67. doi: 10.1016/j.jnutbio.2015.04.014

  32. Hocayen Pde A, Grassiolli S, Leite NC, Pochapski MT, Pereira RA, da Silva LA, et al. Baccharis dracunculifolia methanol extract enhances glucose-stimulated insulin secretion in pancreatic islets of monosodium glutamate induced-obesity model rats. Pharm Biol 2016; 54: 1263–71. doi: 10.3109/13880209.2015.1067232

  33. Wang S, Wang Y, Pan MH, Ho CT. Anti-obesity molecular mechanism of soy isoflavones: weaving the way to new therapeutic routes. Food Funct 2017; 8: 3831–46. doi: 10.1039/c7fo01094j

  34. Choi EO, Park C, Shin SS, Cho EJ, Kim BW, Hwang JA, et al. Zanthoxylum schinifolium leaf ethanol extract inhibits adipocyte differentiation through inactivation of the extracellular signal regulated kinase and phosphoinositide 3-kinase/Akt signaling pathways in 3T3-L1 pre-adipocytes. Mol Med Rep 2015; 12: 1314–20. doi: 10.3892/mmr.2015.3463

  35. Lyu C, Chen, C, Ge F, Liu D, Zhao S, Chen D. A preliminary metagenomic study of puer tea during pile fermentation. J Sci Food Agricult 2013; 93: 3165–74. doi: 10.1002/jsfa.6149.

  36. Roh E, Kim JE, Kwon JY, Park JS, Bode AM, Dong Z, et al. Molecular mechanisms of green tea polyphenols with protective effects against skin photoaging. Crit Rev Food Sci Nutr 2017; 57: 1631–7. doi: 10.1080/10408398.2014.1003365

  37. Prasanth MI, Sivamaruthi BS, Chaiyasut C, Tencomnao T. A review of the role of green tea (Camellia sinensis) in antiphotoaging, stress resistance, neuroprotection, and autophagy. Nutrients 2019; 11: 747. doi: 10.3390/nu11020474

  38. Jochmann N, Baumann G, Stangl V. Green tea and cardiovascular disease: from molecular targets towards human health. Curr Opin Clin Nutr Metabol Care 2008; 11: 758–65. doi: 10.1097/MCO.0b013e328314b68b

  39. Okuda MH, Zemdegs JC, de Santana AA, Santamarina AB, Moreno MF, Hachul AC, et al. Green tea extract improves high fat diet-induced hypothalamic inflammation, without affecting the serotoninergic system. J Nutr Biochem 2014; 25: 1084–9. doi: 10.1016/j.jnutbio.2014.05.012

  40. Kogawa AC, Pires A, Salgado HRN. Atorvastatin: a review of analytical methods for pharmaceutical quality control and monitoring. J AOAC Int 2019; 102: 801–9. doi: 10.5740/jaoacint.18-0200

  41. Thatiparthi J, Dodoala S, Koganti B, Kvsrg P. Barley grass juice (Hordeum vulgare L.) inhibits obesity and improves lipid profile in high fat diet-induced rat model. J Ethnopharmacol 2019; 238: 111843. doi: 10.1016/j.jep.2019.111843

  42. Kuang W, Zhang X, Lan Z. Flavonoids extracted from Linaria vulgaris protect against hyperlipidemia and hepatic steatosis induced by western-type diet in mice. Arch Pharm Res 2018; 41: 1190–8. doi: 10.1007/s12272-017-0941-y

  43. Chung KW, Kim KM, Choi YJ, An HJ, Lee B, Kim DH, et al. The critical role played by endotoxin-induced liver autophagy in the maintenance of lipid metabolism during sepsis. Autophagy 2017; 13: 1113–29. doi: 10.1080/15548627.2017.1319040

  44. Garcia D, Hellberg K, Chaix A, Wallace M, Herzig S, Badur MG, et al. Genetic liver-specific AMPK activation protects against diet-induced obesity and NAFLD. Cell Rep 2019; 26: 192–208 e196. doi: 10.1016/j.celrep.2018.12.036

  45. Li F, Gao C, Yan P, Zhang M, Wang Y, Hu Y, et al. EGCG reduces obesity and white adipose tissue gain partly through AMPK activation in mice. Front Pharmacol 2018; 9: 1366. doi: 10.3389/fphar.2018.01366

  46. Lio, CJ, Dai YW, Wang CL, Fang LW, Huang WC. Maslinic acid protects against obesity-induced nonalcoholic fatty liver disease in mice through regulation of the Sirt1/AMPK signaling pathway. FASEB J 2019; 33: 11791–803. doi: 10.1096/fj.201900413RRR

  47. Zang L, Shimada Y, Nakayama H, Kim Y, Chu DC, Juneja LR, et al. RNA-seq based transcriptome analysis of the anti-obesity effect of green tea extract using Zebrafish Obesity Models. Molecules 2019; 24: 3256. doi: 10.3390/molecules24183256

  48. Lally JSV, Ghoshal S, DePeralta DK, Moaven O, Wei L, Masia R, et al. Inhibition of acetyl-CoA carboxylase by pPhosphorylation or the inhibitor ND-654 suppresses lipogenesis and hepatocellular carcinoma. Cell Metabol 2019; 29: 174–82 e175. doi: 10.1016/j.cmet.2018.08.020

  49. Long YC, Zierath JR. AMP-activated protein kinase signaling in metabolic regulation. J Clin Investig 2006; 116: 1776–83. doi: 10.1172/JCI29044

  50. Weikel KA, Cacicedo JM, Ruderman NB, Ido Y. Knockdown of GSK3beta increases basal autophagy and AMPK signalling in nutrient-laden human aortic endothelial cells. Biosci Rep 2016; 36: e00382. doi: 10.1042/BSR20160174

  51. Anderson R, Prolla T. PGC-1alpha in aging and anti-aging interventions. Biochim Biophys Acta 2009; 1790: 1059–66. doi: 10.1016/j.bbagen.2009.04.005

  52. Lan F, Cacicedo JM, Ruderman N, Ido Y. SIRT1 modulation of the acetylation status, cytosolic localization, and activity of LKB1. Possible role in AMP-activated protein kinase activation. J Biol Chem 2008; 283: 27628–35. doi: 10.1074/jbc.M805711200

  53. Beh BK, Mohamad NE, Yeap SK, Ky H, Boo SY, Chua JYH, et al. Anti-obesity and anti-inflammatory effects of synthetic acetic acid vinegar and Nipa vinegar on high-fat-diet-induced obese mice. Sci Rep 2017; 7: 6664. doi: 10.1038/s41598-017-06235-7

  54. Juneja LR, Kapoor MP, Okubo T, Rao T. Green tea polyphenols: nutraceuticals of modern life. Herbalgram, 2013. pp. xiii, 348 p.

  55. Xing L, Zhang H, Qi R, Tsao R, Mine Y. Recent advances in the understanding of the health benefits and molecular mechanisms associated with green tea polyphenols. J Agricult Food Chem 2019; 67: 1029–43. doi: 10.1021/acs.jafc.8b06146

  56. Suzuki T, Pervin M, Goto S, Isemura M, Nakamura Y. Beneficial effects of tea and the green tea catechin epigallocatechin-3-gallate on obesity. Molecules 2016; 21: 1305. doi: 10.3390/molecules21101305

  57. Furuyashiki T, Nagayasu H, Aoki Y, Bessho H, Hashimoto T, Kanazawa K, et al. Tea catechin suppresses adipocyte differentiation accompanied by down-regulation of PPARgamma2 and C/EBPalpha in 3T3-L1 cells. Biosci Biotechnol Biochem 2004; 68: 2353–9. doi: 10.1271/bbb.68.2353

  58. Tanaka M, Sato A, Kishimoto Y, Mabashi-Asazuma H, Kondo K, Iida K. Gallic acid inhibits lipid accumulation via AMPK pathway and suppresses apoptosis and macrophage-mediated inflammation in hepatocytes. Nutrients 2020; 12: 1479. doi: 10.3390/nu12051479.

  59. Berube-Parent S, Pelletier C, Dore J, Tremblay A. Effects of encapsulated green tea and Guarana extracts containing a mixture of epigallocatechin-3-gallate and caffeine on 24 h energy expenditure and fat oxidation in men. Br J Nutr 2005; 94: 432–6. doi: 10.1079/bjn20051502

Published
2022-03-10
How to Cite
ChenR., LaiX., XiangL., LiQ., SunL., LaiZ., LiZ., ZhangW., WenS., CaoJ., & SunS. (2022). Aged green tea reduces high-fat diet-induced fat accumulation and inflammation via activating the AMP-activated protein kinase signaling pathway. Food & Nutrition Research, 66. https://doi.org/10.29219/fnr.v66.7923
Section
Original Articles