Resveratrol-induced white adipose tissue browning in obese mice by remodeling fecal microbiota

Molecules

Volumn 23, Issue 12, 2018, Pages

  Liao, Weiyao ^a   Yin, Xiaohan ^a   Li, Qingrong ^a   Zhang, Hongmin ^a   Liu, Zihui ^a   Zheng, Xinjie ^a   Zheng, Lin ^a   Feng, Xiang ^a  

^a SUN YAT SEN UNIVERSITY   (China)

Author keywords

Gut microbiota; Resveratrol; Sirt1; WAT browning

Indexed keywords

RESVERATROL; SIRTUIN 1;

ANIMAL; DRUG EFFECT; FECES; INTESTINE FLORA; LIPID DIET; MALE; METABOLISM; MICROBIOLOGY; MICROFLORA; MOUSE; OBESITY; RANDOMIZATION; WHITE ADIPOSE TISSUE;

ADIPOSE TISSUE, WHITE; ANIMALS; DIET, HIGH-FAT; FECES; GASTROINTESTINAL MICROBIOME; MALE; MICE; MICROBIOTA; OBESITY; RANDOM ALLOCATION; RESVERATROL; SIRTUIN 1;

EID: 85058871068     PISSN: None     EISSN: 14203049     Source Type: Journal    
DOI: 10.3390/molecules23123356     Document Type: Article

References (57)

1. Afshin, A.; Forouzanfar, M.H.; Reitsma, M.B.; Sur, P.; Estep, K.; Lee, A.; Marczak, L.; Mokdad, A.H.; Moradi-Lakeh, M.; Naghavi, M.; et al. Health effects of overweight and obesity in 195 countries over 25 years. N. Engl. J. Med. 2017, 377, 13–27. [CrossRef] [PubMed]
2. Hill, J.O.; Wyatt, H.R.; Peters, J.C. Energy balance and obesity. Circulation 2012, 126, 126–132. [CrossRef] [PubMed]
3. Larson-Meyer, D.E.; Newcomer, B.R.; Heilbronn, L.K.; Volaufova, J.; Smith, S.R.; Alfonso, A.J.; Lefevre, M.; Rood, J.C.; Williamson, D.A.; Ravussin, E. Effect of 6-month calorie restriction and exercise on serum and liver lipids and markers of liver function. Obesity 2008, 16, 1355–1362. [CrossRef] [PubMed]
4. Lin, J.Z.; Farmer, S.R. Morphogenetics in brown, beige and white fat development. Adipocyte 2016, 5, 130–135. [CrossRef] [PubMed]
5. Wu, J.; Cohen, P.; Spiegelman, B.M. Adaptive thermogenesis in adipocytes: Is beige the new brown? Genes Dev. 2013, 27, 234–250. [CrossRef] [PubMed]
6. Harms, M.; Seale, P. Brown and beige fat: Development, function and therapeutic potential. Nat. Med. 2013, 19, 1252–1263. [CrossRef] [PubMed]
7. Giralt, M.; Villarroya, F. White, brown, beige/brite: Different adipose cells for different functions? Endocrinology 2013, 154, 2992–3000. [CrossRef] [PubMed]
8. Turnbaugh, P.J.; Ley, R.E.; Mahowald, M.A.; Magrini, V.; Mardis, E.R.; Gordon, J.I. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 2006, 444, 1027–1031. [CrossRef] [PubMed]
9. Turnbaugh, P.J.; Hamady, M.; Yatsunenko, T.; Cantarel, B.L.; Duncan, A.; Ley, R.E.; Sogin, M.L.; Jones, W.J.; Roe, B.A.; Affourtit, J.P.; et al. A core gut microbiome in obese and lean twins. Nature 2009, 457, 480–484. [CrossRef] [PubMed]
10. Chevalier, C.; Stojanovic, O.; Colin, D.J.; Suarez-Zamorano, N.; Tarallo, V.; Veyrat-Durebex, C.; Rigo, D.; Fabbiano, S.; Stevanovic, A.; Hagemann, S.; et al. Gut microbiota orchestrates energy homeostasis during cold. Cell 2015, 163, 1360–1374. [CrossRef] [PubMed]
11. Ramirez-Garza, S.L.; Laveriano-Santos, E.P.; Marhuenda-Munoz, M.; Storniolo, C.E.; Tresserra-Rimbau, A.; Vallverdu-Queralt, A.; Lamuela-Raventos, R.M. Health effects of resveratrol: Results from human intervention trials. Nutrients 2018, 10, 1892. [CrossRef] [PubMed]
12. Lopez, M.S.; Dempsey, R.J.; Vemuganti, R. Resveratrol neuroprotection in stroke and traumatic CNS injury. Neurochem. Int. 2015, 89, 75–82. [CrossRef] [PubMed]
13. Annunziata, G.; Maisto, M.; Schisano, C.; Ciampaglia, R.; Narciso, V.; Tenore, G.; Novellino, E. Resveratrol as a novel anti-herpes simplex virus nutraceutical agent: An overview. Viruses 2018, 10, 473. [CrossRef] [PubMed]
14. Ardid-Ruiz, A.; Ibars, M.; Mena, P.; Del Rio, D.; Muguerza, B.; Bladé, C.; Arola, L.; Aragonès, G.; Suárez, M. Potential Involvement of Peripheral Leptin/STAT3 Signaling in the effects of resveratrol and its metabolites on reducing body fat accumulation. Nutrients 2018, 10, 1757. [CrossRef] [PubMed]
15. Lançon, A.; Frazzi, R.; Latruffe, N. Anti-Oxidant, Anti-Inflammatory and Anti-Angiogenic Properties of Resveratrol in Ocular Diseases. Molecules 2016, 21, 304. [CrossRef] [PubMed]
16. Ma, S.; Feng, J.; Zhang, R.; Chen, J.; Han, D.; Li, X.; Yang, B.; Li, X.; Fan, M.; Li, C.; et al. SIRT1 activation by resveratrol alleviates cardiac dysfunction via mitochondrial regulation in diabetic cardiomyopathy mice. Oxid. Med. Cell. Longev. 2017, 2017, 4602715. [CrossRef] [PubMed]
17. Chen, Y.; Lin, Y.; Lin, J.; Yang, N.; Chen, M. Sugary Kefir strain lactobacillus mali APS1 ameliorated hepatic steatosis by regulation of SIRT1/NRF-2 and gut microbiota in rats. Mol. Nutr. Food Res. 2018, 62, 1700903. [CrossRef] [PubMed]
18. Qiao, Y.; Sun, J.; Xia, S.; Tang, X.; Shi, Y.; Le, G. Effects of resveratrol on gut microbiota and fat storage in a mouse model with high-fat-induced obesity. Food Funct. 2014, 5, 1241–1249. [CrossRef] [PubMed]
19. Sung, M.M.; Kim, T.T.; Denou, E.; Soltys, C.M.; Hamza, S.M.; Byrne, N.J.; Masson, G.; Park, H.; Wishart, D.S.; Madsen, K.L.; et al. Improved glucose homeostasis in obese mice treated with resveratrol is associated with alterations in the gut microbiome. Diabetes 2017, 66, 418–425. [CrossRef] [PubMed]
20. Zhang, C.; Zhang, M.; Wang, S.; Han, R.; Cao, Y.; Hua, W.; Mao, Y.; Zhang, X.; Pang, X.; Wei, C.; et al. Interactions between gut microbiota, host genetics and diet relevant to development of metabolic syndromes in mice. ISME J. 2010, 4, 232–241. [CrossRef] [PubMed]
21. Baur, J.A.; Pearson, K.J.; Price, N.L.; Jamieson, H.A.; Lerin, C.; Kalra, A.; Prabhu, V.V.; Allard, J.S.; Lopez-Lluch, G.; Lewis, K.; et al. Resveratrol improves health and survival of mice on a high-calorie diet. Nature 2006, 444, 337–342. [CrossRef] [PubMed]
22. Kim, S.; Jin, Y.; Choi, Y.; Park, T. Resveratrol exerts anti-obesity effects via mechanisms involving down-regulation of adipogenic and inflammatory processes in mice. Biochem. Pharmacol. 2011, 81, 1343–1351. [CrossRef] [PubMed]
23. Chen, S.; Xiao, X.; Feng, X.; Li, W.; Zhou, N.; Zheng, L.; Sun, Y.; Zhang, Z.; Zhu, W. Resveratrol induces Sirt1-dependent apoptosis in 3T3-L1 preadipocytes by activating AMPK and suppressing AKT activity and survivin expression. J. Nutr. Biochem. 2012, 23, 1100–1112. [CrossRef] [PubMed]
24. Wang, S.; Liang, X.; Yang, Q.; Fu, X.; Rogers, C.J.; Zhu, M.; Rodgers, B.D.; Jiang, Q.; Dodson, M.V.; Du, M. Resveratrol induces brown-like adipocyte formation in white fat through activation of AMP-activated protein kinase (AMPK) α1. Int. J. Obes. 2015, 39, 967–976. [CrossRef] [PubMed]
25. Vitrac, X.; Desmouliere, A.; Brouillaud, B.; Krisa, S.; Deffieux, G.; Barthe, N.; Rosenbaum, J.; Merillon, J.M. Distribution of [14C]-trans-resveratrol, a cancer chemopreventive polyphenol, in mouse tissues after oral administration. Life Sci. 2003, 72, 2219–2233. [CrossRef]
26. Kaldas, M.I.; Walle, U.K.; Walle, T. Resveratrol transport and metabolism by human intestinal Caco-2 cells. J. Pharm. Pharmacol. 2003, 55, 307–312. [CrossRef] [PubMed]
27. Jung, M.; Lee, J.; Shin, N.; Kim, M.; Hyun, D.; Yun, J.; Kim, P.S.; Whon, T.W.; Bae, J. Chronic repression of mTOR complex 2 induces changes in the gut microbiota of diet-induced obese mice. Sci. Rep. 2016, 6, 30887. [CrossRef] [PubMed]
28. Musso, G.; Gambino, R.; Cassader, M. Gut microbiota as a regulator of energy homeostasis and ectopic fat deposition: Mechanisms and implications for metabolic disorders. Curr. Opin. Lipidol. 2010, 21, 76–83. [CrossRef] [PubMed]
29. Mujico, J.R.; Baccan, G.C.; Gheorghe, A.; Diaz, L.E.; Marcos, A. Changes in gut microbiota due to supplemented fatty acids in diet-induced obese mice. Br. J. Nutr. 2013, 110, 711–720. [CrossRef] [PubMed]
30. Neyrinck, A.M.; Possemiers, S.; Druart, C.; Van de Wiele, T.; De Backer, F.; Cani, P.D.; Larondelle, Y.; Delzenne, N.M. Prebiotic effects of wheat arabinoxylan related to the increase in bifidobacteria, Roseburia and Bacteroides/Prevotella in diet-induced obese mice. PLoS ONE 2011, 6, e20944. [CrossRef] [PubMed]
31. Parnell, J.A.; Reimer, R.A. Prebiotic fiber modulation of the gut microbiota improves risk factors for obesity and the metabolic syndrome. Gut Microbes. 2012, 3, 29–34. [CrossRef] [PubMed]
32. Everard, A.; Belzer, C.; Geurts, L.; Ouwerkerk, J.P.; Druart, C.; Bindels, L.B.; Guiot, Y.; Derrien, M.; Muccioli, G.G.; Delzenne, N.M.; et al. Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity. Proc. Natl. Acad. Sci. USA 2013, 110, 9066–9071. [CrossRef] [PubMed]
33. Neyrinck, A.M.; Van Hee, V.F.; Bindels, L.B.; De Backer, F.; Cani, P.D.; Delzenne, N.M. Polyphenol-rich extract of pomegranate peel alleviates tissue inflammation and hypercholesterolaemia in high-fat diet-induced obese mice: Potential implication of the gut microbiota. Br. J. Nutr. 2013, 109, 802–809. [CrossRef] [PubMed]
34. Rossato, M.; Granzotto, M.; Macchi, V.; Porzionato, A.; Petrelli, L.; Calcagno, A.; Vencato, J.; De Stefani, D.; Silvestrin, V.; Rizzuto, R.; et al. Human white adipocytes express the cold receptor TRPM8 which activation induces UCP1 expression, mitochondrial activation and heat production. Mol. Cell. Endocrinol. 2014, 383, 137–146. [CrossRef] [PubMed]
35. Vitali, A.; Murano, I.; Zingaretti, M.C.; Frontini, A.; Ricquier, D.; Cinti, S. The adipose organ of obesity-prone C57BL/6J mice is composed of mixed white and brown adipocytes. J. Lipid Res. 2012, 53, 619–629. [CrossRef] [PubMed]
36. Rosenwald, M.; Perdikari, A.; Rulicke, T.; Wolfrum, C. Bi-directional interconversion of brite and white adipocytes. Nat. Cell. Biol. 2013, 15, 659–667. [CrossRef] [PubMed]
37. Petrovic, N.; Walden, T.B.; Shabalina, I.G.; Timmons, J.A.; Cannon, B.; Nedergaard, J. Chronic peroxisome proliferator-activated receptor gamma (PPARgamma) activation of epididymally derived white adipocyte cultures reveals a population of thermogenically competent, UCP1-containing adipocytes molecularly distinct from classic brown adipocytes. J. Biol. Chem. 2010, 285, 7153–7164. [CrossRef] [PubMed]
38. Virtanen, K.A.; Lidell, M.E.; Orava, J.; Heglind, M.; Westergren, R.; Niemi, T.; Taittonen, M.; Laine, J.; Savisto, N.J.; Enerback, S.; et al. Functional brown adipose tissue in healthy adults. N. Engl. J. Med. 2009, 360, 1518–1525. [CrossRef] [PubMed]
39. Cypess, A.M.; Lehman, S.; Williams, G.; Tal, I.; Rodman, D.; Goldfine, A.B.; Kuo, F.C.; Palmer, E.L.; Tseng, Y.H.; Doria, A.; et al. Identification and importance of brown adipose tissue in adult humans. N Engl. J. Med. 2009, 360, 1509–1517. [CrossRef] [PubMed]
40. Qiang, L.; Wang, L.; Kon, N.; Zhao, Y.; Zhao, W.; Lee, S.; Zhang, Y.; Rosenbaum, M.; Gu, W.; Farmer, S.R.; et al. Brown remodeling of white adipose tissue by Sirt1-dependent deacetylation of Pparγ. Cell 2012, 150, 620–632. [CrossRef] [PubMed]
41. Lagouge, M.; Argmann, C.; Gerhart-Hines, Z.; Meziane, H.; Lerin, C.; Daussin, F.; Messadeq, N.; Milne, J.; Lambert, P.; Elliott, P.; et al. Resveratrol improves mitochondrial function and protects against metabolic disease by activating SIRT1 and PGC-1alpha. Cell 2006, 127, 1109–1122. [CrossRef] [PubMed]
42. Lakhan, S.E.; Kirchgessner, A. Gut inflammation in chronic fatigue syndrome. Nutr. Metab. 2010, 7, 79. [CrossRef] [PubMed]
43. Radak, Z.; Zhao, Z.; Koltai, E.; Ohno, H.; Atalay, M. Oxygen consumption and usage during physical exercise: The balance between oxidative stress and ROS-dependent adaptive signaling. Antioxid. Redox Signal. 2013, 18, 1208–1246. [CrossRef] [PubMed]
44. Wang, Y.; Shi, X.; Qi, J.; Li, X.; Uray, K.; Guan, X. SIRT1 inhibits the mouse intestinal motility and epithelial proliferation. Am. J. Physiol. Gastrointest. Liver Physiol. 2012, 302, G207–G217. [CrossRef] [PubMed]
45. Igarashi, M.; Guarente, L. mTORC1 and SIRT1 Cooperate to Foster Expansion of Gut Adult Stem Cells during Calorie Restriction. Cell 2016, 166, 436–450. [CrossRef] [PubMed]
46. Ma, Y.; Xu, C.; Wang, W.; Sun, L.; Yang, S.; Lu, D.; Liu, Y.; Yang, H. Role of SIRT1 in the protection of intestinal epithelial barrier under hypoxia and its mechanism. Zhonghua Wei Chang. Wai Ke Za Zhi 2014, 17, 602–606. [PubMed]
47. Shi, H.; Kokoeva, M.V.; Inouye, K.; Tzameli, I.; Yin, H.; Flier, J.S. TLR4 links innate immunity and fatty acid-induced insulin resistance. J. Clin. Investig. 2006, 116, 3015–3025. [CrossRef] [PubMed]
48. Fujisaka, S.; Usui, I.; Bukhari, A.; Ikutani, M.; Oya, T.; Kanatani, Y.; Tsuneyama, K.; Nagai, Y.; Takatsu, K.; Urakaze, M.; et al. Regulatory mechanisms for adipose tissue M1 and M2 macrophages in diet-induced obese mice. Diabetes 2009, 58, 2574–2582. [CrossRef] [PubMed]
49. Lin, Y.W.; Wei, L.N. Innate immunity orchestrates adipose tissue homeostasis. Horm. Mol. Biol. Clin. Investig. 2017, 31. [CrossRef] [PubMed]
50. Nie, Y.F.; Hu, J.; Yan, X.H. Cross-talk between bile acids and intestinal microbiota in host metabolism and health. J. Zhejiang Univ. Sci. B 2015, 16, 436–446. [CrossRef] [PubMed]
51. Kuipers, F.; Bloks, V.W.; Groen, A.K. Beyond intestinal soap–bile acids in metabolic control. Nat. Rev. Endocrinol. 2014, 10, 488–498. [CrossRef] [PubMed]
52. Gao, Z.; Yin, J.; Zhang, J.; Ward, R.E.; Martin, R.J.; Lefevre, M.; Cefalu, W.T.; Ye, J. Butyrate improves insulin sensitivity and increases energy expenditure in mice. Diabetes 2009, 58, 1509–1517. [CrossRef] [PubMed]
53. Caron, A.Z.; He, X.; Mottawea, W.; Seifert, E.L.; Jardine, K.; Dewar-Darch, D.; Cron, G.O.; Harper, M.E.; Stintzi, A.; McBurney, M.W. The SIRT1 deacetylase protects mice against the symptoms of metabolic syndrome. FASEB J. 2014, 28, 1306–1316. [CrossRef] [PubMed]
54. Kazgan, N.; Metukuri, M.R.; Purushotham, A.; Lu, J.; Rao, A.; Lee, S.; Pratt-Hyatt, M.; Lickteig, A.; Csanaky, I.L.; Zhao, Y.; et al. Intestine-specific deletion of SIRT1 in mice impairs DCoH2-HNF-1alpha-FXR signaling and alters systemic bile acid homeostasis. Gastroenterology 2014, 146, 1006–1016. [CrossRef] [PubMed]
55. Lo, S.G.; Ryu, D.; Mouchiroud, L.; Fernando, S.C.; Anderson, C.L.; Katsyuba, E.; Piersigilli, A.; Hottiger, M.O.; Schoonjans, K.; Auwerx, J. Loss of Sirt1 function improves intestinal anti-bacterial defense and protects from colitis-induced colorectal cancer. PLoS ONE 2014, 9, e102495. [CrossRef]
56. Caesar, R.; Tremaroli, V.; Kovatcheva-Datchary, P.; Cani, P.D.; Bäckhed, F. Crosstalk between Gut Microbiota and Dietary Lipids Aggravates WAT Inflammation through TLR Signaling. Cell Metab. 2015, 22, 658–668. [CrossRef] [PubMed]
57. Chang, C.; Lin, C.; Lu, C.; Martel, J.; Ko, Y.; Ojcius, D.M.; Tseng, S.; Wu, T.; Chen, Y.M.; Young, J.D.; et al. Ganoderma lucidum reduces obesity in mice by modulating the composition of the gut microbiota. Nat. Commun. 2015, 6, 16130. [CrossRef] [PubMed]