Abstract
Purpose
Decaffeinated green tea (GT) and black tea (BT) polyphenols inhibit weight gain in mice fed an obesogenic diet. Since the intestinal microflora is an important contributor to obesity, it was the objective of this study to determine whether the intestinal microflora plays a role in the anti-obesogenic effect of GT and BT.
Methods
C57BL/6J mice were fed a high-fat/high-sucrose diet (HF/HS, 32% energy from fat; 25% energy from sucrose) or the same diet supplemented with 0.25% GTP or BTP or a low-fat/high-sucrose (LF/HS, 10.6% energy from fat, 25% energy from sucrose) diet for 4 weeks. Bacterial composition was assessed by MiSeq sequencing of the 16S rRNA gene.
Results
GTP and BTP diets resulted in a decrease of cecum Firmicutes and increase in Bacteroidetes. The relative proportions of Blautia, Bryantella, Collinsella, Lactobacillus, Marvinbryantia, Turicibacter, Barnesiella, and Parabacteroides were significantly correlated with weight loss induced by tea extracts. BTP increased the relative proportion of Pseudobutyrivibrio and intestinal formation of short-chain fatty acids (SCFA) analyzed by gas chromatography. Cecum propionic acid content was significantly correlated with the relative proportion of Pseudobutyrivibrio. GTP and BTP induced a significant increase in hepatic 5′adenosylmonophosphate-activated protein kinase (AMPK) phosphorylation by 70 and 289%, respectively (P < 0.05) determined by Western blot.
Conclusion
In summary, both BTP and GTP induced weight loss in association with alteration of the microbiota and increased hepatic AMPK phosphorylation. We hypothesize that BTP increased pAMPK through increased intestinal SCFA production, while GTPs increased hepatic AMPK through GTP present in the liver.
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References
Hayat K, Iqbal H, Malik U, Bilal U, Mushtaq S (2015) Tea and its consumption: benefits and risks. Crit Rev Food Sci Nutr 55(7):939–954. doi:10.1080/10408398.2012.678949
Sharma V, Rao LJ (2009) A thought on the biological activities of black tea. Crit Rev Food Sci Nutr 49(5):379–404. doi:10.1080/10408390802068066
Heber D, Zhang Y, Yang J, Ma JE, Henning SM, Li Z (2014) Green tea, black tea, and oolong tea polyphenols reduce visceral fat and inflammation in mice fed high-fat, high-sucrose obesogenic diets. J Nutr 144(9):1385–1393. doi:10.3945/jn.114.191007
Yang CS, Zhang J, Zhang L, Huang J, Wang Y (2016) Mechanisms of body weight reduction and metabolic syndrome alleviation by tea. Mol Nutr Food Res 60(1):160–174. doi:10.1002/mnfr.201500428
Sae-Tan S, Grove KA, Kennett MJ, Lambert JD (2011) (−)-Epigallocatechin-3-gallate increases the expression of genes related to fat oxidation in the skeletal muscle of high fat-fed mice. Food Funct 2(2):111–116. doi:10.1039/c0fo00155d
Lee LS, Choi JH, Sung MJ, Hur JY, Hur HJ, Park JD, Kim YC, Gu EJ, Min B, Kim HJ (2015) Green tea changes serum and liver metabolomic profiles in mice with high-fat diet-induced obesity. Mol Nutr Food Res 59(4):784–794. doi:10.1002/mnfr.201400470
Ikeda I, Hamamoto R, Uzu K, Imaizumi K, Nagao K, Yanagita T, Suzuki Y, Kobayashi M, Kakuda T (2005) Dietary gallate esters of tea catechins reduce deposition of visceral fat, hepatic triacylglycerol, and activities of hepatic enzymes related to fatty acid synthesis in rats. Biosci Biotechnol Biochem 69(5):1049–1053
Korpela K, Flint HJ, Johnstone AM, Lappi J, Poutanen K, Dewulf E, Delzenne N, de Vos WM, Salonen A (2014) Gut microbiota signatures predict host and microbiota responses to dietary interventions in obese individuals. PLoS One 9(6):e90702. doi:10.1371/journal.pone.0090702
Tilg H, Moschen AR (2014) Microbiota and diabetes: an evolving relationship. Gut 63(9):1513–1521. doi:10.1136/gutjnl-2014-306928
Tuohy KM, Fava F, Viola R (2014) ’The way to a man’s heart is through his gut microbiota’—dietary pro- and prebiotics for the management of cardiovascular risk. Proc Nutr Soc 73(2):172–185. doi:10.1017/S0029665113003911
Million M, Lagier JC, Yahav D, Paul M (2013) Gut bacterial microbiota and obesity. Clin Microbiol Infect 19(4):305–313. doi:10.1111/1469-0691.12172
Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI (2006) An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444(7122):1027–1031. doi:10.1038/nature05414
Parks BW, Nam E, Org E, Kostem E, Norheim F, Hui ST, Pan C, Civelek M, Rau CD, Bennett BJ, Mehrabian M, Ursell LK, He A, Castellani LW, Zinker B, Kirby M, Drake TA, Drevon CA, Knight R, Gargalovic P, Kirchgessner T, Eskin E, Lusis AJ (2013) Genetic control of obesity and gut microbiota composition in response to high-fat, high-sucrose diet in mice. Cell Metab 17(1):141–152. doi:10.1016/j.cmet.2012.12.007
Tzounis X, Vulevic J, Kuhnle GG, George T, Leonczak J, Gibson GR, Kwik-Uribe C, Spencer JP (2008) Flavanol monomer-induced changes to the human faecal microflora. Br J Nutr 99(4):782–792. doi:10.1017/S0007114507853384
Lee HC, Jenner AM, Low CS, Lee YK (2006) Effect of tea phenolics and their aromatic fecal bacterial metabolites on intestinal microbiota. Res Microbiol 157(9):876–884. doi:10.1016/j.resmic.2006.07.004
Jin JS, Touyama M, Hisada T, Benno Y (2012) Effects of green tea consumption on human fecal microbiota with special reference to Bifidobacterium species. Microbiol Immunol 56(11):729–739. doi:10.1111/j.1348-0421.2012.00502.x
Liu Z, Chen Z, Guo H, He D, Zhao H, Wang Z, Zhang W, Liao L, Zhang C, Ni L (2016) The modulatory effect of infusions of green tea, oolong tea, and black tea on gut microbiota in high-fat-induced obese mice. Food Funct 7(12):4869–4879. doi:10.1039/c6fo01439a
den Besten G, Gerding A, van Dijk TH, Ciapaite J, Bleeker A, van Eunen K, Havinga R, Groen AK, Reijngoud DJ, Bakker BM (2015) Protection against the metabolic syndrome by guar gum-derived short-chain fatty acids depends on peroxisome proliferator-activated receptor gamma and glucagon-like peptide-1. PLoS One 10(8):e0136364. doi:10.1371/journal.pone.0136364
Ruderman NB, Xu XJ, Nelson L, Cacicedo JM, Saha AK, Lan F, Ido Y (2010) AMPK and SIRT1: a long-standing partnership? Am J Physiol Endocrinol Metab 298(4):E751–E760. doi:10.1152/ajpendo.00745.2009
Xie B, Shi H, Chen Q, Ho CT (1993) Antioxidant properties of fractions and polyphenol constituents from green, oolong and black teas. Proc Natl Sci Counc Repub China B 17(2):77–84
Kuhnert N, Drynan JW, Obuchowicz J, Clifford MN, Witt M (2010) Mass spectrometric characterization of black tea thearubigins leading to an oxidative cascade hypothesis for thearubigin formation. Rapid Commun Mass Spectrom 24(23):3387–3404. doi:10.1002/rcm.4778
Singleton VL, Esau P (1969) Phenolic substances in grapes and wine, and their significance. Adv Food Res Suppl 1:1–261
Zhao G, Liu JF, Nyman M, Jonsson JA (2007) Determination of short-chain fatty acids in serum by hollow fiber supported liquid membrane extraction coupled with gas chromatography. J Chromatogr B Anal Technol Biomed Life Sci 846(1–2):202–208. doi:10.1016/j.jchromb.2006.09.027
DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72(7):5069–5072. doi:10.1128/AEM.03006-05
Lozupone C, Knight R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71(12):8228–8235. doi:10.1128/AEM.71.12.8228-8235.2005
Seo DB, Jeong HW, Cho D, Lee BJ, Lee JH, Choi JY, Bae IH, Lee SJ (2015) Fermented green tea extract alleviates obesity and related complications and alters gut microbiota composition in diet-induced obese mice. J Med Food 18(5):549–556. doi:10.1089/jmf.2014.3265
Yang J, Martinez I, Walter J, Keshavarzian A, Rose DJ (2013) In vitro characterization of the impact of selected dietary fibers on fecal microbiota composition and short chain fatty acid production. Anaerobe 23:74–81. doi:10.1016/j.anaerobe.2013.06.012
Ridaura VK, Faith JJ, Rey FE, Cheng J, Duncan AE, Kau AL, Griffin NW, Lombard V, Henrissat B, Bain JR, Muehlbauer MJ, Ilkayeva O, Semenkovich CF, Funai K, Hayashi DK, Lyle BJ, Martini MC, Ursell LK, Clemente JC, Van Treuren W, Walters WA, Knight R, Newgard CB, Heath AC, Gordon JI (2013) Gut microbiota from twins discordant for obesity modulate metabolism in mice. Science 341(6150):1241214. doi:10.1126/science.1241214
Kasperowicz A, Stan-Glasek K, Guczynska W, Piknova M, Pristas P, Nigutova K, Javorsky P, Michalowski T (2010) Fructanolytic and saccharolytic enzymes of the rumen bacterium Pseudobutyrivibrio ruminis strain 3—preliminary study. Folia Microbiol 55(4):329–331. doi:10.1007/s12223-010-0051-4
Zhong Y, Nyman M, Fak F (2015) Modulation of gut microbiota in rats fed high-fat diets by processing whole-grain barley to barley malt. Mol Nutr Food Res 59(10):2066–2076. doi:10.1002/mnfr.201500187
Brahe LK, Astrup A, Larsen LH (2013) Is butyrate the link between diet, intestinal microbiota and obesity-related metabolic diseases? Obes Rev 14(12):950–959. doi:10.1111/obr.12068
Nyambe-Silavwe H, Williamson G (2016) Polyphenol- and fibre-rich dried fruits with green tea attenuate starch-derived postprandial blood glucose and insulin: a randomised, controlled, single-blind, cross-over intervention. Br J Nutr 116(3):443–450. doi:10.1017/S0007114516002221
Striegel L, Kang B, Pilkenton SJ, Rychlik M, Apostolidis E (2015) Effect of black tea and black tea pomace polyphenols on alpha-glucosidase and alpha-amylase inhibition, relevant to type 2 diabetes prevention. Front Nutr 2:3. doi:10.3389/fnut.2015.00003
den Besten G, Havinga R, Bleeker A, Rao S, Gerding A, van Eunen K, Groen AK, Reijngoud DJ, Bakker BM (2014) The short-chain fatty acid uptake fluxes by mice on a guar gum supplemented diet associate with amelioration of major biomarkers of the metabolic syndrome. PLoS One 9(9):e107392. doi:10.1371/journal.pone.0107392
Hardie DG (2015) AMPK: positive and negative regulation, and its role in whole-body energy homeostasis. Curr Opin Cell Biol 33:1–7. doi:10.1016/j.ceb.2014.09.004
Henning SM, Wang P, Abgaryan N, Vicinanza R, de Oliveira DM, Zhang Y, Lee RP, Carpenter CL, Aronson WJ, Heber D (2013) Phenolic acid concentrations in plasma and urine from men consuming green or black tea and potential chemopreventive properties for colon cancer. Mol Nutr Food Res 57(3):483–493. doi:10.1002/mnfr.201200646
Pereira-Caro G, Moreno-Rojas JM, Brindani N, Del Rio D, Lean MEJ, Hara Y, Crozier A (2017) Bioavailability of black tea theaflavins: absorption, metabolism, and colonic catabolism. J Agric Food Chem 65(26):5365–5374. doi:10.1021/acs.jafc.7b01707
Rocha A, Bolin AP, Cardoso CA, Otton R (2016) Green tea extract activates AMPK and ameliorates white adipose tissue metabolic dysfunction induced by obesity. Eur J Nutr 55(7):2231–2244. doi:10.1007/s00394-015-1033-8
Santamarina AB, Oliveira JL, Silva FP, Carnier J, Mennitti LV, Santana AA, de Souza GH, Ribeiro EB, Oller do Nascimento CM, Lira FS, Oyama LM (2015) Green tea extract rich in epigallocatechin-3-gallate prevents fatty liver by AMPK activation via LKB1 in mice fed a high-fat diet. PLoS One 10(11):e0141227. doi:10.1371/journal.pone.0141227
Acknowledgements
This work was supported by the National Institute of Health (R03CA171583 and P50CA092131) and departmental funds of the Center for Human Nutrition, Department of Medicine, David Geffen School of Medicine, University of California, Los Angeles.
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Henning, S.M., Yang, J., Hsu, M. et al. Decaffeinated green and black tea polyphenols decrease weight gain and alter microbiome populations and function in diet-induced obese mice. Eur J Nutr 57, 2759–2769 (2018). https://doi.org/10.1007/s00394-017-1542-8
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DOI: https://doi.org/10.1007/s00394-017-1542-8