Role of gut microbiota, gut-brain and gut liver axes in physiological regulation of inflammation, energy balance, and metabolism: Fecal transplant from resveratrol-fed donors improves glycaemia and cardiovascular features of the metabolic syndrome in mice

American Journal of Physiology - Endocrinology and Metabolism

Volumn 315, Issue 4, 2018, Pages E511-E519

  Kim, Ty T ^a   Parajuli, Nirmal ^a   Sung, Miranda M ^a   Bairwa, Suresh C ^a   Levasseur, Jody ^a   Soltys, Carrie Lynn M ^a   Wishart, David S ^a   Madsen, Karen ^a   Schertzer, Jonathan D ^b   Dyck, Jason R B ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

^b MCMASTER UNIVERSITY   (Canada)

Author keywords

Fecal transplant; Glycemia; Hypertension; Metabolic syndrome; Resveratrol

Indexed keywords

GLUCOSE; RESVERATROL; ANTIOXIDANT; CYTOKINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARDIOVASCULAR DISEASE; CENTRAL NERVOUS SYSTEM; COLITIS; CONTROLLED STUDY; DIET INDUCED OBESITY; DIET SUPPLEMENTATION; DIGESTIVE SYSTEM; ENERGY BALANCE; ENERGY METABOLISM; FECAL MICROBIOTA TRANSPLANTATION; GLUCOSE BLOOD LEVEL; GLUCOSE HOMEOSTASIS; GUT BRAIN AXIS; GUT LIVER AXIS; HYPERGLYCEMIA; HYPERTENSION; INTESTINE FLORA; MALE; METABOLIC SYNDROME X; MOUSE; NONHUMAN; OBESITY; PHYSIOLOGICAL PROCESS; PRIORITY JOURNAL; SYSTOLIC BLOOD PRESSURE; TREATMENT DURATION; ANIMAL; BLOOD PRESSURE; COLON; DRUG EFFECT; IMMUNOLOGY; INFLAMMATION; LIPID DIET; METABOLISM; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; SUGAR INTAKE;

ANIMALS; ANTIOXIDANTS; BLOOD GLUCOSE; BLOOD PRESSURE; COLON; CYTOKINES; DIET, HIGH-FAT; DIETARY SUCROSE; FECAL MICROBIOTA TRANSPLANTATION; GASTROINTESTINAL MICROBIOME; HYPERGLYCEMIA; HYPERTENSION; INFLAMMATION; MAGNETIC RESONANCE SPECTROSCOPY; METABOLIC SYNDROME; MICE; OBESITY; RESVERATROL;

EID: 85054768429     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00471.2017     Document Type: Article

References (34)

1. Afshin A, Forouzanfar MH, Reitsma MB, Sur P, Estep K, Lee A, Marczak L, Mokdad AH, Moradi-Lakeh M, Naghavi M, Salama JS, Vos T, Abate KH, Abbafati C, Ahmed MB, Al-Aly Z, Alkerwi A, Al-Raddadi R, Amare AT, Amberbir A, Amegah AK, Amini E, Amrock SM, Anjana RM, Ärnlöv J, Asayesh H, Banerjee A, Barac A, Baye E, Bennett DA, Beyene AS, Biadgilign S, Biryukov S, Bjertness E, Boneya DJ, Campos-Nonato I, Carrero JJ, Cecilio P, Cercy K, Ciobanu LG, Cornaby L, Damtew SA, Dandona L, Dandona R, Dharmaratne SD, Duncan BB, Eshrati B, Esteghamati A, Feigin VL, Fernandes JC, Fürst T, Gebrehiwot TT, Gold A, Gona PN, Goto A, Habtewold TD, Hadush KT, Hafezi-Nejad N, Hay SI, Horino M, Islami F, Kamal R, Kasaeian A, Katikireddi SV, Kengne AP, Kesav-achandran CN, Khader YS, Khang YH, Khubchandani J, Kim D, Kim YJ, Kinfu Y, Kosen S, Ku T, Defo BK, Kumar GA, Larson HJ, Leinsalu M, Liang X, Lim SS, Liu P, Lopez AD, Lozano R, Majeed A, Malekzadeh R, Malta DC, Mazidi M, McAlinden C, McGarvey ST, Mengistu DT, Mensah GA, Mensink GBM, Mezgebe HB, Mirrakhi-mov EM, Mueller UO, Noubiap JJ, Obermeyer CM, Ogbo FA, Owolabi MO, Patton GC, Pourmalek F, Qorbani M, Rafay A, Rai RK, Ranabhat CL, Reinig N, Safiri S, Salomon JA, Sanabria JR, Santos IS, Sartorius B, Sawhney M, Schmidhuber J, Schutte AE, Schmidt MI, Sepanlou SG, Shamsizadeh M, Sheikhbahaei S, Shin MJ, Shiri R, Shiue I, Roba HS, Silva DAS, Silverberg JI, Singh JA, Stranges S, Swaminathan S, Tabarés-Seisdedos R, Tadese F, Tedla BA, Tegegne BS, Terkawi AS, Thakur JS, Tonelli M, Topor-Madry R, Tyrovolas S, Ukwaja KN, Uthman OA, Vaezghasemi M, Vasankari T, Vlassov VV, Vollset SE, Weiderpass E, Werdecker A, Wesana J, Westerman R, Yano Y, Yonemoto N, Yonga G, Zaidi Z, Zenebe ZM, Zipkin B, Murray CJL; GBD 2015 Obesity Collaborators. Health effects of overweight and obesity in 195 countries over 25 years. N Engl J Med 377: 13–27, 2017. doi:10.1056/NEJMoa1614362.
2. Anhê FF, Marette A. A microbial protein that alleviates metabolic syndrome. Nat Med 23: 11–12, 2017. doi:10.1038/nm.4261.
3. Baur JA, Pearson KJ, Price NL, Jamieson HA, Lerin C, Kalra A, Prabhu VV, Allard JS, Lopez-Lluch G, Lewis K, Pistell PJ, Poosala S, Becker KG, Boss O, Gwinn D, Wang M, Ramaswamy S, Fishbein KW, Spencer RG, Lakatta EG, Le Couteur D, Shaw RJ, Navas P, Puigserver P, Ingram DK, de Cabo R, Sinclair DA. Resveratrol improves health and survival of mice on a high-calorie diet. Nature 444: 337–342, 2006. doi:10.1038/nature05354.
4. Benjamin EJ, Blaha MJ, Chiuve SE, Cushman M, Das SR, Deo R, de Ferranti SD, Floyd J, Fornage M, Gillespie C, Isasi CR, Jiménez MC, Jordan LC, Judd SE, Lackland D, Lichtman JH, Lisabeth L, Liu S, Longenecker CT, Mackey RH, Matsushita K, Mozaffarian D, Mussolino ME, Nasir K, Neumar RW, Palaniappan L, Pandey DK, Thiagarajan RR, Reeves MJ, Ritchey M, Rodriguez CJ, Roth GA, Rosamond WD, Sasson C, Towfighi A, Tsao CW, Turner MB, Virani SS, Voeks JH, Willey JZ, Wilkins JT, Wu JH, Alger HM, Wong SS, Muntner P; American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Heart disease and stroke statistics-2017 update: a report from the american heart association. Circulation 135: e146–e603, 2017. [Errata in Circulation 135: e646, 2017 and Circulation 136: e196 2017]. doi:10.1161/CIR.0000000000000485.
5. Bo S, Ponzo V, Ciccone G, Evangelista A, Saba F, Goitre I, Procopio M, Pagano GF, Cassader M, Gambino R. Six months of resveratrol supplementation has no measurable effect in type 2 diabetic patients. A randomized, double blind, placebo-controlled trial. Pharmacol Res 111: 896–905, 2016. doi:10.1016/j.phrs.2016.08.010.
6. Cani PD, Delzenne NM, Amar J, Burcelin R. Role of gut microflora in the development of obesity and insulin resistance following high-fat diet feeding. Pathol Biol (Paris) 56: 305–309, 2008. doi:10.1016/j.patbio. 2007.09.008.
7. Cornier MA, Dabelea D, Hernandez TL, Lindstrom RC, Steig AJ, Stob NR, Van Pelt RE, Wang H, Eckel RH. The metabolic syndrome. Endocr Rev 29: 777–822, 2008. doi:10.1210/er.2008-0024.
8. Côté CD, Rasmussen BA, Duca FA, Zadeh-Tahmasebi M, Baur JA, Daljeet M, Breen DM, Filippi BM, Lam TKT. Resveratrol activates duodenal Sirt1 to reverse insulin resistance in rats through a neuronal network. Nat Med 21: 498–505, 2015. doi:10.1038/nm.3821.
9. Dao TMA, Waget A, Klopp P, Serino M, Vachoux C, Pechere L, Drucker DJ, Champion S, Barthélemy S, Barra Y, Burcelin R, Sérée E. Resveratrol increases glucose induced GLP-1 secretion in mice: a mechanism which contributes to the glycemic control. PLoS One 6: e20700, 2011. doi:10.1371/journal.pone.0020700.
10. Deng JY, Hsieh PS, Huang JP, Lu LS, Hung LM. Activation of estrogen receptor is crucial for resveratrol-stimulating muscular glucose uptake via both insulin-dependent and-independent pathways. Diabetes 57: 1814–1823, 2008. doi:10.2337/db07-1750.
11. Dolinsky VW, Chakrabarti S, Pereira TJ, Oka T, Levasseur J, Beker D, Zordoky BN, Morton JS, Nagendran J, Lopaschuk GD, Davidge ST, Dyck JRB. Resveratrol prevents hypertension and cardiac hypertrophy in hypertensive rats and mice. Biochim Biophys Acta 1832: 1723– 1733, 2013. doi:10.1016/j.bbadis.2013.05.018.
12. Dolinsky VW, Chan AYM, Robillard Frayne I, Light PE, Des Rosiers C, Dyck JRB. Resveratrol prevents the prohypertrophic effects of oxidative stress on LKB1. Circulation 119: 1643–1652, 2009. doi:10.1161/CIRCULATIONAHA.108.787440.
13. Gao Z, Yin J, Zhang J, Ward RE, Martin RJ, Lefevre M, Cefalu WT, Ye J. Butyrate improves insulin sensitivity and increases energy expenditure in mice. Diabetes 58: 1509–1517, 2009. doi:10.2337/db08-1637.
14. Guasch-Ferré M, Hruby A, Toledo E, Clish CB, Martínez-González MA, Salas-Salvadó J, Hu FB. Metabolomics in prediabetes and diabetes: a systematic review and meta-analysis. Diabetes Care 39: 833–846, 2016. doi:10.2337/dc15-2251.
15. Hall JE, do Carmo JM, da Silva AA, Wang Z, Hall ME. Obesity-induced hypertension: interaction of neurohumoral and renal mechanisms. Circ Res 116: 991–1006, 2015. doi:10.1161/CIRCRESAHA.116.305697.
16. Holmes E, Li JV, Athanasiou T, Ashrafian H, Nicholson JK. Understanding the role of gut microbiome-host metabolic signal disruption in health and disease. Trends Microbiol 19: 349–359, 2011. doi:10.1016/j. tim.2011.05.006.
17. Kang W, Hong HJ, Guan J, Kim DG, Yang EJ, Koh G, Park D, Han CH, Lee YJ, Lee DH. Resveratrol improves insulin signaling in a tissue-specific manner under insulin-resistant conditions only: in vitro and in vivo experiments in rodents. Metabolism 61: 424–433, 2012. doi:10. 1016/j.metabol.2011.08.003.
18. Koonen DPY, Sung MMY, Kao CKC, Dolinsky VW, Koves TR, Ilkayeva O, Jacobs RL, Vance DE, Light PE, Muoio DM, Febbraio M, Dyck JRB. Alterations in skeletal muscle fatty acid handling predisposes middle-aged mice to diet-induced insulin resistance. Diabetes 59: 1366– 1375, 2010. doi:10.2337/db09-1142.
19. Kootte RS, Levin E, Salojärvi J, Smits LP, Hartstra AV, Udayappan SD, Hermes G, Bouter KE, Koopen AM, Holst JJ, Knop FK, Blaak EE, Zhao J, Smidt H, Harms AC, Hankemeijer T, Bergman JJGHM, Romijn HA, Schaap FG, Olde Damink SWM, Ackermans MT, Dal-linga-Thie GM, Zoetendal E, de Vos WM, Serlie MJ, Stroes ESG, Groen AK, Nieuwdorp M. Improvement of insulin sensitivity after lean donor feces in metabolic syndrome is driven by baseline intestinal microbiota composition. Cell Metab 26: 611–619.e6, 2017. doi:10.1016/j.cmet. 2017.09.008.
20. Liu K, Zhou R, Wang B, Mi MT. Effect of resveratrol on glucose control and insulin sensitivity: a meta-analysis of 11 randomized controlled trials. Am J Clin Nutr 99: 1510–1519, 2014. doi:10.3945/ajcn.113.082024.
21. Manach C, Scalbert A, Morand C, Rémésy C, Jiménez L. Polyphenols: food sources and bioavailability. Am J Clin Nutr 79: 727–747, 2004. doi:10.1093/ajcn/79.5.727.
22. Kawanaka M, Nishino K, Oka T, Urata N, Nakamura J, Suehiro M, Kawamoto H, Chiba Y, Yamada G. Tyrosine levels are associated with insulin resistance in patients with nonalcoholic fatty liver disease. Hepat Med 7: 29–35, 2015. doi:10.2147/HMER.S79100.
23. Muoio DM, Newgard CB. Molecular and metabolic mechanisms of insulin resistance and beta-cell failure in type 2 diabetes. Nat Rev Mol Cell Biol 9: 193–205, 2008. doi:10.1038/nrm2327.
24. Musso G, Gambino R, Cassader M. Interactions between gut microbiota and host metabolism predisposing to obesity and diabetes. Annu Rev Med 62: 361–380, 2011. doi:10.1146/annurev-med-012510-175505.
25. Ott SJ, Waetzig GH, Rehman A, Moltzau-Anderson J, Bharti R, Grasis JA, Cassidy L, Tholey A, Fickenscher H, Seegert D, Rosenstiel P, Schreiber S. Efficacy of sterile fecal filtrate transfer for treating patients with clostridium difficile infection. Gastroenterology 152: 799– 811.e7, 2017. doi:10.1053/j.gastro.2016.11.010.
26. Plovier H, Everard A, Druart C, Depommier C, Van Hul M, Geurts L, Chilloux J, Ottman N, Duparc T, Lichtenstein L, Myridakis A, Delzenne NM, Klievink J, Bhattacharjee A, van der Ark KCH, Aalvink S, Martinez LO, Dumas ME, Maiter D, Loumaye A, Hermans MP, Thissen JP, Belzer C, de Vos WM, Cani PD. A purified membrane protein from Akkermansia muciniphila or the pasteurized bacterium improves metabolism in obese and diabetic mice. Nat Med 23: 107–113, 2017. doi:10.1038/nm.4236.
27. Poulsen MM, Vestergaard PF, Clasen BF, Radko Y, Christensen LP, Stødkilde-Jørgensen H, Møller N, Jessen N, Pedersen SB, Jørgensen JO. High-dose resveratrol supplementation in obese men: an investigator-initiated, randomized, placebo-controlled clinical trial of substrate metabolism, insulin sensitivity, and body composition. Diabetes 62: 1186–1195, 2013. doi:10.2337/db12-0975.
28. Richards EM, Pepine CJ, Raizada MK, Kim S. The gut, its microbiome, and hypertension. Curr Hypertens Rep 19: 36, 2017. doi:10.1007/s11906-017-0734-1.
29. Shin NR, Whon TW, Bae JW. Proteobacteria: microbial signature of dysbiosis in gut microbiota. Trends Biotechnol 33: 496–503, 2015. doi: 10.1016/j.tibtech.2015.06.011.
30. Sung MM, Kim TT, Denou E, Soltys CM, Hamza SM, Byrne NJ, Masson G, Park H, Wishart DS, Madsen KL, Schertzer JD, Dyck JRB. Improved glucose homeostasis in obese mice treated with resveratrol is associated with alterations in the gut microbiome. Diabetes 66: 418– 425, 2017. doi:10.2337/db16-0680.
31. Szkudelski T, Szkudelska K. Resveratrol and diabetes: from animal to human studies. Biochim Biophys Acta 1852: 1145–1154, 2015. doi:10. 1016/j.bbadis.2014.10.013.
32. Upadhyaya S, Banerjee G. Type 2 diabetes and gut microbiome: at the intersection of known and unknown. Gut Microbes 6: 85–92, 2015. doi:10.1080/19490976.2015.1024918.
33. Yadav H, Lee J-H, Lloyd J, Walter P, Rane SG. Beneficial metabolic effects of a probiotic via butyrate-induced GLP-1 hormone secretion. J Biol Chem 288: 25088–25097, 2013. doi:10.1074/jbc.M113.452516.
34. Zordoky BNM, Robertson IM, Dyck JRB. Preclinical and clinical evidence for the role of resveratrol in the treatment of cardiovascular diseases. Biochim Biophys Acta 1852: 1155–1177, 2015. doi:10.1016/j. bbadis.2014.10.016.