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Theabrownin from Pu-erh tea together with swinging exercise synergistically ameliorates obesity and insulin resistance in rats

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Abstract

Purpose

Theabrownin (TB)-containing Pu-erh tea has been shown to be hypolipidemic in rats fed a high-fat diet. Physical exercise such as swinging is also known to reduce obesity. We hypothesized that TB in combination with swinging can synergistically ameliorate obesity and insulin resistance in rats with metabolic syndrome.

Methods

TB, rosiglitazone, or lovastatin (controls) was administered by gavage to rats fed a diet high in fat, sugar, and salt. A subgroup of the rats was subjected to a 30-min daily swinging exercise regimen, whereas the other rats did not exercise.

Results

Theabrownin in combination with swinging was found to significantly improve serum lipid status and prevent development of obesity and insulin resistance in rats. Liver transcriptomics data suggested that theabrownin activated circadian rhythm, protein kinase A, the adenosine monophosphate-activated protein kinase, and insulin signaling pathways by enhancing cyclic adenosine monophosphate levels and, hence, accelerating nutrient metabolism and the consumption of sugar and fat. The serum dopamine levels in rats increased significantly after exercise. In parallel work, intraperitoneal dopamine injections were shown to significantly reduce weight gain and prevent the elevation in triglyceride levels that would otherwise be induced by the high fat-sugar–salt diet. Theabrownin prevented obesity and insulin resistance mainly by affecting the circadian rhythm, while swinging exercise stimulated the overproduction of dopamine to accelerate metabolism of glucose and lipid.

Conclusions

Theabrownin and exercise synergistically ameliorated metabolic syndrome in rats and effectively prevented obesity.

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References

  1. Lv HP, Zhang YJ, Lin Z, Liang YR (2013) Processing and chemical constituents of Pu-erh tea: a review. Food Res Int 53:608–618. https://doi.org/10.1016/j.foodres.2013.02.043

    Article  CAS  Google Scholar 

  2. Cao ZH, Gu DH, Lin QY, Xu ZQ, Huang QC, Rao H, Liu EW, Jia JJ, Ge CR (2011) Effect of Pu-erh tea on body fat and lipid profiles in rats with diet-induced obesity. Phytother Res 25:234–238. https://doi.org/10.1002/ptr.3247

    Article  CAS  PubMed  Google Scholar 

  3. Ding Y, Zou X, Jiang X, Wu J, Zhang Y, Chen D, Liang B (2015) Pu-erh tea down-regulates sterol regulatory element-binding protein and stearyol-COA desaturase to reduce fat storage in Caenorhabditis elegans. PLoS One 10:e0113815. https://doi.org/10.1371/journal.pone.0113815

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Hou Y, Shao W, Xiao R, Xu K, Ma Z, Johnstone BH, Du Y (2009) Pu-erh tea aqueous extracts lower atherosclerotic risk factors in a rat hyperlipidemia model. Exp Gerontol 44:434–439. https://doi.org/10.1016/j.exger.2009.03.007

    Article  PubMed  Google Scholar 

  5. Hu WY, Ma XH, Zhou WY, Li XX, Sun TT, Sun H (2017) Preventive effect of Silibinin in combination with Pu-erh tea extract on non-alcoholic fatty liver disease in ob/ob mice. Food Funct 8:1105–1115. https://doi.org/10.1039/C6FO01591C

    Article  CAS  PubMed  Google Scholar 

  6. Zeng L, Yan J, Luo L, Zhang D (2015) Effects of Pu-erh tea aqueous extract (PTAE) on blood lipid metabolism enzymes. Food Funct 6:2008–2016. https://doi.org/10.1039/c5fo00362h

    Article  CAS  PubMed  Google Scholar 

  7. Gong JS, Tang C, Peng CX (2012) Characterization of the chemical differences between solvent extracts from Pu-erh tea and Dian Hong black tea by CP–Py–GC/MS. J Anal Appl Pyrol 95:189–197. https://doi.org/10.1016/j.jaap.2012.02.006

    Article  CAS  Google Scholar 

  8. Gong J, Peng C, Chen T, Gao B, Zhou H (2010) Effects of theabrownin from pu-erh tea on the metabolism of serum lipids in rats: mechanism of action. J Food Sci 75:H182–H189. https://doi.org/10.1111/j.1750-3841.20

    Article  CAS  PubMed  Google Scholar 

  9. Peng CX, Liu J, Liu HR, Zhou HJ, Gong JS (2013) Influence of different fermentation raw materials on pyrolyzates of Pu-erh tea theabrownin by Curie-point pyrolysis-gas chromatography–mass spectroscopy. Int J Biol Macromol 54:197–203. https://doi.org/10.1016/j.ijbiomac.2012.12.021

    Article  CAS  PubMed  Google Scholar 

  10. Chen DX (2012) Psychological clairvoyance of traditional sports-swing. J Guizhou Norm Univ (Nat Sci) 30:26–29

    Google Scholar 

  11. Zhang XX, Tao ZB, Wang JB (2004) Folk sports in Chinese festivals. J Beijing Univ Phys Educ 27:1581–1583

    Google Scholar 

  12. Meyns P, Bruijn SM, Duysens J (2013) The how and why of arm swing during human walking. Gait Posture 38:555–562. https://doi.org/10.1016/j.gaitpost.2013.02.006

    Article  PubMed  Google Scholar 

  13. Modica JR, Kram R (2005) Metabolic energy and muscular activity required for leg swing in running. J Appl Physiol 98:2126–2131. https://doi.org/10.1152/japplphysiol.00511.2004

    Article  PubMed  Google Scholar 

  14. Biddinger SB, Hernandez-Ono A, Rask-Madsen C, Haas JT, Alemãn JO, Suzuki R, Scapa EF, Agarwal C, Carey MC, Stephanopoulos G (2008) Hepatic insulin resistance is sufficient to produce dyslipidemia and susceptibility to atherosclerosis. Cell Metab 7:125–134. https://doi.org/10.1016/j.cmet.2007.11.013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Eckel RH, Grundy SM, Zimmet PZ (2005) The metabolic syndrome. Lancet 365:1415–1428. https://doi.org/10.1016/S0140-6736(05)67777-X

    Article  CAS  PubMed  Google Scholar 

  16. Liu J, Peng CX, Gao B, Gong JS (2016) Serum metabolomics analysis of rat after intragastric infusion of Pu-erh theabrownin. J Sci Food Agric 96:3708–3716. https://doi.org/10.1002/jsfa.7556

    Article  CAS  PubMed  Google Scholar 

  17. Wu EK, Wang QP, Gong JS, Zhang TT (2019) Effect of fermentation methods on theabrownin composition of Pu-erh tea. Food Sci 40:215–221. https://doi.org/10.7506/spkx1002-6630-20171201-006

    Article  Google Scholar 

  18. United States Food and Drug Administration (2005) Guidance for industry: estimating the maximum safe starting dose in initial clinical trials for therapeutics in adult healthy volunteers. Center for Drug Evaluation and Research (CDER), Rockville

    Google Scholar 

  19. Matthews DR, Hosker JR, Rudenski AS, Naylor BA, Treacher DF, Turner RC (1985) Homeostasis model assessment: insulin resistance and β-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 28:412–419. https://doi.org/10.1007/BF00280883

    Article  CAS  PubMed  Google Scholar 

  20. Zhang TT, Wu EK, Peng CX, Tan C, Gong JS (2018) Effects of theabrownins extracted from Pu-erh tea on blood glucose and blood lipid indexes of rats with high sugar diet. Food Sci Technol 43:7. https://doi.org/10.13684/j.cnki.spkj.2018.07.011

    Article  Google Scholar 

  21. Nieto-Vazquez I, Fernã N-VS, De AC, Lorenzo M (2008) Dual role of interleukin-6 in regulating insulin sensitivity in murine skeletal muscle. Diabetes 57:3211–3221. https://doi.org/10.2337/db07-1062

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Tilg H, Shapiro L, Atkins MB, Dinarello CA, Mier JW (1993) Induction of circulating and erythrocyte-bound IL-8 by IL-2 immunotherapy and suppression of its in vitro production by IL-1 receptor antagonist and soluble tumor necrosis factor receptor (p75) chimera. J Immunol 151(6):3299–3307

    CAS  PubMed  Google Scholar 

  23. Grippo RM, Purohit AM, Zhang Q, Zweifel LS, Güler AD (2017) Direct midbrain dopamine input to the suprachiasmatic nucleus accelerates circadian entrainment. Curr Biol 27:2475–2645. https://doi.org/10.1016/j.cub.2017.06.084

    Article  CAS  Google Scholar 

  24. Stauffer W, Lak A, Yang A, Borel M, Paulsen O, Boyden E, Schultz W (2016) Dopamine neuron-specific optogenetic stimulation in rhesus macaques. Cell 166:1564–1571. https://doi.org/10.1016/j.cell.2016.08.024

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Kebabian JW (1978) Multiple classes of dopamine receptors in mammalian central nervous system: the involvement of dopamine-sensitive adenylyl cyclase. Life Sci 23:479–483. https://doi.org/10.1016/0024-3205(78)90157-1

    Article  CAS  PubMed  Google Scholar 

  26. Kohlie R, Perwitz N, Resch J, Schmid SM, Lehnert H, Klein J, Iwen KA (2016) Dopamine directly increases mitochondrial mass and thermogenesis in brown adipocytes. J Mol Endocrinol 58:57–66. https://doi.org/10.1530/JME-16-0159

    Article  PubMed  Google Scholar 

  27. Pappa KI, Gazouli M, Anastasiou E, Iliodromiti Z, Antsaklis A, Anagnou NP (2013) The major circadian pacemaker ARNT-like protein-1 (BMAL1) is associated with susceptibility to gestational diabetes mellitus. Diabetes Res Clin Pract 99:151–157. https://doi.org/10.1016/j.diabres.2012.10.015

    Article  CAS  PubMed  Google Scholar 

  28. Richards J, Diaz AN, Gumz ML (2014) Clock genes in hypertension: novel insights from rodent models. Blood Press Monit 19:249–254. https://doi.org/10.1097/MBP.0000000000000060

    Article  PubMed  PubMed Central  Google Scholar 

  29. Hatanaka F, Matsubara C, Myung J, Yoritaka T, Kamimura N, Tsutsumi S, Kanai A, Suzuki Y, Sassone-Corsi P, Aburatani H (2010) Genome-wide profiling of the core clock protein bmal1 targets reveals a strict relationship with metabolism. Mol Cell Biol 30:5636–5648. https://doi.org/10.1016/j.neures.2011.07.226

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Rudic RD, Mcnamara P, Curtis AM, Boston RC, Panda S, Hogenesch JB, Fitzgerald GA (2004) BMAL1 and CLOCK, two essential components of the circadian clock, are involved in glucose homeostasis. PLoS Biol 2:e377. https://doi.org/10.1371/journal.pbio.0020377

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Turek FW, Joshu C, Kohsaka A, Lin E, Ivanova G, Mcdearmon E, Laposky A, Losee-Olson S, Easton A, Jensen DR (2005) Obesity and metabolic syndrome in circadian clock mutant mice. Science 308:1043–1045. https://doi.org/10.1126/science.1108750

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Marcheva B, Ramsey KM, Buhr ED, Kobayashi Y, Su H, Ko CH, Ivanova G, Omura C, Mo S, Vitaterna MH (2010) Disruption of the clock components CLOCK and BMAL1 leads to hypoinsulinemia and diabetes. Nature 466:627–631. https://doi.org/10.1038/nature09253

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Lee YJ, Han DH, Pak YK, Cho S (2012) Circadian regulation of low density lipoprotein receptor promoter activity by CLOCK/BMAL1, Hes1 and Hes6. Exp Mol Med 44:642–652. https://doi.org/10.3858/emm.2012.44.11.073

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Finck BN, Kelly DP (2006) PGC-1 coactivators: inducible regulators of energy metabolism in health and disease. J Clin Invest 116:615–622. https://doi.org/10.1172/JCI27794

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Wang YX, Lee CH, Tiep S, Yu RT, Ham J, Kang H, Evans RM (2003) Peroxisome-proliferator-activated receptor δ activates fat metabolism to prevent obesity. Cell 113:159–170. https://doi.org/10.1016/S0092-8674(03)00269-1

    Article  CAS  PubMed  Google Scholar 

  36. Hubacek JA, Bobkova D (2006) Role of Cholesterol 7α-hydroxylase (CYP7A1) in nutrigenetics and pharmacogenetics of cholesterol lowering. Mol Diagn Ther 10:93–100. https://doi.org/10.1007/BF03256448

    Article  CAS  PubMed  Google Scholar 

  37. Shi Y, Liu C (2017) Study on the integration of circadian clock and energy metabolism. Chin J Cell Biol 39:261–270

    CAS  Google Scholar 

  38. Hatori M, Vollmers C, Zarrinpar A, Ditacchio L, Bushong E, Gill S, Leblanc M, Chaix A, Joens M, Fitzpatrick JJ (2012) Time-restricted feeding without reducing caloric intake prevents metabolic diseases in mice fed a high-fat diet. Cell Metab 15:848–860. https://doi.org/10.1016/j.cmet.2012.04.019

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Paschos GK, Ibrahim S, Song WL, Kunieda T, Grant G, Reyes TM, Bradfield CA, Vaughan CH, Eiden M, Masoodi M (2012) Obesity in mice with adipocyte-specific deletion of clock component Arntl. Nat Med 18:1768–1777. https://doi.org/10.1038/nm.2979

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Bass J, Takahashi JS (2010) Circadian integration of metabolism and energetics. Science 330:1349–1354. https://doi.org/10.1126/science.1195027

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This study was supported by the National Natural Science Foundation of China (31560456, 81860608) and Yunnan Agricultural Foundation Projects [2017FG001(-011) and 2017FG001(-089)].

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Authors and Affiliations

Authors

Contributions

JSG obtained financial support, and designed and oversaw this study. EKW performed the swinging research and analyzed data. TTZ performed the non-swinging research and analyzed data. CT designed the experimental swing. QPW, CXP, and YC prepared, reviewed, and edited the manuscript. All authors contributed to the discussion, read the final manuscript and approved it. JSG is the guarantor of this work.

Corresponding authors

Correspondence to Qiuping Wang or Jiashun Gong.

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Conflict of interest

The authors declare no conflict of interest.

Animal ethics statement

Experiments on animals were conducted in full compliance with the Yunnan Agricultural University institutional and Chinese national guidelines for care and use of laboratory animals.

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Wu, E., Zhang, T., Tan, C. et al. Theabrownin from Pu-erh tea together with swinging exercise synergistically ameliorates obesity and insulin resistance in rats. Eur J Nutr 59, 1937–1950 (2020). https://doi.org/10.1007/s00394-019-02044-y

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  • DOI: https://doi.org/10.1007/s00394-019-02044-y

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