Microbiota-generated metabolites promote metabolic benefits via gut-brain neural circuits

Cell

Volumn 156, Issue 1-2, 2014, Pages 84-96

  De Vadder, Filipe ^a,b,c   Kovatcheva Datchary, Petia ^d   Goncalves, Daisy ^a,b,c   Vinera, Jennifer ^a,b,c   Zitoun, Carine ^a,b,c   Duchampt, Adeline ^a,b,c   Bäckhed, Fredrik ^d,e   Mithieux, Gilles ^a,b,c  

^a INSTITUT NATIONAL DE LA SANTÉ ET DE LA RECHERCHE MÉDICALE   (France)

^b UNIVERSITÉ DE LYON   (France)

^c UNIVERSITÉ LYON 1   (France)

^d UNIVERSITY OF GOTHENBURG   (Sweden)

^e Capital Region   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

BUTYRIC ACID; CARBON 14; CYCLIC AMP; FATTY ACID RECEPTOR 3; FRUCTOSE OLIGOSACCHARIDE; G PROTEIN COUPLED RECEPTOR; GLUCOSE; INSULIN; PROPIONIC ACID; SHORT CHAIN FATTY ACID; UNCLASSIFIED DRUG; FFAR3 PROTEIN; GLUCOSE 6 PHOSPHATASE; MESSENGER RNA; PHOSPHOENOLPYRUVATE CARBOXYKINASE (GTP);

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BODY WEIGHT; BRAIN; COLON; CONTROLLED STUDY; DIETARY FIBER; DIETARY INTAKE; ENERGY METABOLISM; FERMENTATION; GENE EXPRESSION; GLUCOSE METABOLISM; GLUCOSE TOLERANCE; GLYCEMIC CONTROL; INSULIN SENSITIVITY; INTESTINE; INTESTINE FLORA; ISOTOPE LABELING; JEJUNUM; METABOLIC REGULATION; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; PRIORITY JOURNAL; RAT; ADULT; ANIMAL TISSUE; ENZYME ACTIVE SITE; GLUCONEOGENESIS; GLUCOSE BLOOD LEVEL; GLUCOSE HOMEOSTASIS; MALE; NERVE CELL NETWORK;

MUS;

ANIMALS; BRAIN; DIETARY FATS; DIETARY FIBER; FATTY ACIDS, VOLATILE; GLUCONEOGENESIS; GLUCOSE; GLUCOSE-6-PHOSPHATASE; HOMEOSTASIS; INSULIN RESISTANCE; INTESTINES; MICE; MICROBIOTA; OBESITY; OLIGOSACCHARIDES; RATS;

EID: 84892814749     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2013.12.016     Document Type: Article

References (56)

1. J.W. Anderson, and S.R. Bridges Short-chain fatty acid fermentation products of plant fiber affect glucose metabolism of isolated rat hepatocytes Proc. Soc. Exp. Biol. Med. 177 1984 372 376
2. A. Battezzati, A. Caumo, F. Martino, L.P. Sereni, J. Coppa, R. Romito, M. Ammatuna, E. Regalia, D.E. Matthews, V. Mazzaferro, and L. Luzi Nonhepatic glucose production in humans Am. J. Physiol. Endocrinol. Metab. 286 2004 E129 E135
3. H.-R. Berthoud Anatomy and function of sensory hepatic nerves Anat. Rec. A Discov. Mol. Cell. Evol. Biol. 280 2004 827 835
4. L.B. Bindels, P. Porporato, E.M. Dewulf, J. Verrax, A.M. Neyrinck, J.C. Martin, K.P. Scott, P. Buc Calderon, O. Feron, and G.G. Muccioli et al. Gut microbiota-derived propionate reduces cancer cell proliferation in the liver Br. J. Cancer 107 2012 1337 1344
5. A.J. Brown, S.M. Goldsworthy, A.A. Barnes, M.M. Eilert, L. Tcheang, D. Daniels, A.I. Muir, M.J. Wigglesworth, I. Kinghorn, and N.J. Fraser et al. The Orphan G protein-coupled receptors GPR41 and GPR43 are activated by propionate and other short chain carboxylic acids J. Biol. Chem. 278 2003 11312 11319
6. P.D. Cani, A.M. Neyrinck, F. Fava, C. Knauf, R.G. Burcelin, K.M. Tuohy, G.R. Gibson, and N.M. Delzenne Selective increases of bifidobacteria in gut microflora improve high-fat-diet-induced diabetes in mice through a mechanism associated with endotoxaemia Diabetologia 50 2007 2374 2383
7. J.N. Clore, J. Stillman, and H. Sugerman Glucose-6-phosphatase flux in vitro is increased in type 2 diabetes Diabetes 49 2000 969 974
8. M. Croset, F. Rajas, C. Zitoun, J.M. Hurot, S. Montano, and G. Mithieux Rat small intestine is an insulin-sensitive gluconeogenic organ Diabetes 50 2001 740 746
9. J.H. Cummings, E.W. Pomare, W.J. Branch, C.P. Naylor, and G.T. Macfarlane Short chain fatty acids in human large intestine, portal, hepatic and venous blood Gut 28 1987 1221 1227
10. F. Delaere, A. Duchampt, L. Mounien, P. Seyer, C. Duraffourd, C. Zitoun, B. Thorens, and G. Mithieux The role of sodium-coupled glucose co-transporter 3 in the satiety effect of portal glucose sensing Mol Metab 2 2012 47 53
11. D.R. Donohoe, N. Garge, X. Zhang, W. Sun, T.M. O'Connell, M.K. Bunger, and S.J. Bultman The microbiome and butyrate regulate energy metabolism and autophagy in the mammalian colon Cell Metab. 13 2011 517 526
12. C. Duraffourd, F. De Vadder, D. Goncalves, F. Delaere, A. Penhoat, B. Brusset, F. Rajas, D. Chassard, A. Duchampt, and A. Stefanutti et al. Mu-opioid receptors and dietary protein stimulate a gut-brain neural circuitry limiting food intake Cell 150 2012 377 388
13. S. El Aidy, M. Derrien, C.A. Merrifield, F. Levenez, J. Doré, M.V. Boekschoten, J. Dekker, E. Holmes, E.G. Zoetendal, and P. van Baarlen et al. Gut bacteria-host metabolic interplay during conventionalisation of the mouse germfree colon ISME J. 7 2013 743 755
14. S. El Aidy, C.A. Merrifield, M. Derrien, P. van Baarlen, G. Hooiveld, F. Levenez, J. Doré, J. Dekker, E. Holmes, and S.P. Claus et al. The gut microbiota elicits a profound metabolic reorientation in the mouse jejunal mucosa during conventionalisation Gut 62 2013 1306 1314
15. H.J. Flint, K.P. Scott, P. Louis, and S.H. Duncan The role of the gut microbiota in nutrition and health Nat Rev Gastroenterol Hepatol 9 2012 577 589
16. Z. Gao, J. Yin, J. Zhang, R.E. Ward, R.J. Martin, M. Lefevre, W.T. Cefalu, and J. Ye Butyrate improves insulin sensitivity and increases energy expenditure in mice Diabetes 58 2009 1509 1517
17. A. Gautier-Stein, C. Zitoun, E. Lalli, G. Mithieux, and F. Rajas Transcriptional regulation of the glucose-6-phosphatase gene by cAMP/vasoactive intestinal peptide in the intestine. Role of HNF4alpha, CREM, HNF1alpha, and C/EBPalpha J. Biol. Chem. 281 2006 31268 31278
18. M.T. Hayes, J. Foo, V. Besic, Y. Tychinskaya, and R.S. Stubbs Is intestinal gluconeogenesis a key factor in the early changes in glucose homeostasis following gastric bypass? Obes. Surg. 21 2011 759 762
19. I.J. Hidalgo, T.J. Raub, and R.T. Borchardt Characterization of the human colon carcinoma cell line (Caco-2) as a model system for intestinal epithelial permeability Gastroenterology 96 1989 736 749
20. M.A. Hildebrandt, C. Hoffmann, S.A. Sherrill-Mix, S.A. Keilbaugh, M. Hamady, Y.-Y. Chen, R. Knight, R.S. Ahima, F. Bushman, and G.D. Wu High-fat diet determines the composition of the murine gut microbiome independently of obesity Gastroenterology 137 2009 1716 1724 e1-e2
21. F.H. Karlsson, V. Tremaroli, I. Nookaew, G. Bergström, C.J. Behre, B. Fagerberg, J. Nielsen, and F. Bäckhed Gut metagenome in European women with normal, impaired and diabetic glucose control Nature 498 2013 99 103
22. I. Kimura, D. Inoue, T. Maeda, T. Hara, A. Ichimura, S. Miyauchi, M. Kobayashi, A. Hirasawa, and G. Tsujimoto Short-chain fatty acids and ketones directly regulate sympathetic nervous system via G protein-coupled receptor 41 (GPR41) Proc. Natl. Acad. Sci. USA 108 2011 8030 8035
23. E. Larsson, V. Tremaroli, Y.S. Lee, O. Koren, I. Nookaew, A. Fricker, J. Nielsen, R.E. Ley, and F. Bäckhed Analysis of gut microbial regulation of host gene expression along the length of the gut and regulation of gut microbial ecology through MyD88 Gut 61 2012 1124 1131
24. B.T. Layden, A.R. Angueira, M. Brodsky, V. Durai, and W.L. Lowe Jr. Short chain fatty acids and their receptors: new metabolic targets Transl. Res. 161 2013 131 140
25. H.V. Lin, A. Frassetto, E.J. Kowalik Jr., A.R. Nawrocki, M.M. Lu, J.R. Kosinski, J.A. Hubert, D. Szeto, X. Yao, G. Forrest, and D.J. Marsh Butyrate and propionate protect against diet-induced obesity and regulate gut hormones via free fatty acid receptor 3-independent mechanisms PLoS ONE 7 2012 e35240
26. C. Lozupone, and R. Knight UniFrac: a new phylogenetic method for comparing microbial communities Appl. Environ. Microbiol. 71 2005 8228 8235
27. I. Magnusson, D.L. Rothman, L.D. Katz, R.G. Shulman, and G.I. Shulman Increased rate of gluconeogenesis in type II diabetes mellitus. A 13C nuclear magnetic resonance study J. Clin. Invest. 90 1992 1323 1327
28. A.I. Mendeloff Dietary fiber and human health N. Engl. J. Med. 297 1977 811 814
29. G. Mithieux Comment about intestinal gluconeogenesis after gastric bypass in human in relation with the paper by Hayes et al., Obes. Surg. 2011 Obes. Surg. 22 2012 1920 1922 author reply 1923-1924
30. G. Mithieux Nutrient control of hunger by extrinsic gastrointestinal neurons Trends Endocrinol. Metab. 24 2013 378 384
31. G. Mithieux, I. Bady, A. Gautier, M. Croset, F. Rajas, and C. Zitoun Induction of control genes in intestinal gluconeogenesis is sequential during fasting and maximal in diabetes Am. J. Physiol. Endocrinol. Metab. 286 2004 E370 E375
32. G. Mithieux, F. Rajas, and A. Gautier-Stein A novel role for glucose 6-phosphatase in the small intestine in the control of glucose homeostasis J. Biol. Chem. 279 2004 44231 44234
33. G. Mithieux, P. Misery, C. Magnan, B. Pillot, A. Gautier-Stein, C. Bernard, F. Rajas, and C. Zitoun Portal sensing of intestinal gluconeogenesis is a mechanistic link in the diminution of food intake induced by diet protein Cell Metab. 2 2005 321 329
34. E. Mutel, A. Gautier-Stein, A. Abdul-Wahed, M. Amigó-Correig, C. Zitoun, A. Stefanutti, I. Houberdon, J.-A. Tourette, G. Mithieux, and F. Rajas Control of blood glucose in the absence of hepatic glucose production during prolonged fasting in mice: induction of renal and intestinal gluconeogenesis by glucagon Diabetes 60 2011 3121 3131
35. A.M. Neyrinck, S. Possemiers, W. Verstraete, F. De Backer, P.D. Cani, and N.M. Delzenne Dietary modulation of clostridial cluster XIVa gut bacteria (Roseburia spp.) by chitin-glucan fiber improves host metabolic alterations induced by high-fat diet in mice J. Nutr. Biochem. 23 2012 51 59
36. M.K. Nøhr, M.H. Pedersen, A. Gille, K.L. Egerod, M.S. Engelstoft, A.S. Husted, R.M. Sichlau, K.V. Grunddal, S.S. Poulsen, and S. Han et al. GPR41/FFAR3 and GPR43/FFAR2 as cosensors for short-chain fatty acids in enteroendocrine cells vs FFAR3 in enteric neurons and FFAR2 in enteric leukocytes Endocrinology 154 2013 3552 3564
37. B.W. Parks, E. Nam, E. Org, E. Kostem, F. Norheim, S.T. Hui, C. Pan, M. Civelek, C.D. Rau, and B.J. Bennett et al. Genetic control of obesity and gut microbiota composition in response to high-fat, high-sucrose diet in mice Cell Metab. 17 2013 141 152
38. A. Penhoat, E. Mutel, M. Amigo-Correig, B. Pillot, A. Stefanutti, F. Rajas, and G. Mithieux Protein-induced satiety is abolished in the absence of intestinal gluconeogenesis Physiol. Behav. 105 2011 89 93
39. B. Pillot, M. Soty, A. Gautier-Stein, C. Zitoun, and G. Mithieux Protein feeding promotes redistribution of endogenous glucose production to the kidney and potentiates its suppression by insulin Endocrinology 150 2009 616 624
40. F. Rajas, N. Bruni, S. Montano, C. Zitoun, and G. Mithieux The glucose-6 phosphatase gene is expressed in human and rat small intestine: regulation of expression in fasted and diabetic rats Gastroenterology 117 1999 132 139
41. T.K. Ray, K.M. Mansell, L.C. Knight, L.S. Malmud, O.E. Owen, and G. Boden Long-term effects of dietary fiber on glucose tolerance and gastric emptying in noninsulin-dependent diabetic patients Am. J. Clin. Nutr. 37 1983 376 381
42. M. Roberfroid, G.R. Gibson, L. Hoyles, A.L. McCartney, R. Rastall, I. Rowland, D. Wolvers, B. Watzl, H. Szajewska, and B. Stahl et al. Prebiotic effects: metabolic and health benefits Br. J. Nutr. 104 Suppl 2 2010 S1 S63
43. M.D. Robertson, J.M. Currie, L.M. Morgan, D.P. Jewell, and K.N. Frayn Prior short-term consumption of resistant starch enhances postprandial insulin sensitivity in healthy subjects Diabetologia 46 2003 659 665
44. M.D. Robertson, A.S. Bickerton, A.L. Dennis, H. Vidal, and K.N. Frayn Insulin-sensitizing effects of dietary resistant starch and effects on skeletal muscle and adipose tissue metabolism Am. J. Clin. Nutr. 82 2005 559 567
45. S.M. Sagar, F.R. Sharp, and T. Curran Expression of c-fos protein in brain: metabolic mapping at the cellular level Science 240 1988 1328 1331
46. A. Salonen, J. Nikkilä, J. Jalanka-Tuovinen, O. Immonen, M. Rajilić-Stojanović, R.A. Kekkonen, A. Palva, and W.M. de Vos Comparative analysis of fecal DNA extraction methods with phylogenetic microarray: effective recovery of bacterial and archaeal DNA using mechanical cell lysis J. Microbiol. Methods 81 2010 127 134
47. B.S. Samuel, A. Shaito, T. Motoike, F.E. Rey, F. Bäckhed, J.K. Manchester, R.E. Hammer, S.C. Williams, J. Crowley, M. Yanagisawa, and J.I. Gordon Effects of the gut microbiota on host adiposity are modulated by the short-chain fatty-acid binding G protein-coupled receptor, Gpr41 Proc. Natl. Acad. Sci. USA 105 2008 16767 16772
48. J. Schmidt, N.J. Smith, E. Christiansen, I.G. Tikhonova, M. Grundmann, B.D. Hudson, R.J. Ward, C. Drewke, G. Milligan, E. Kostenis, and T. Ulven Selective orthosteric free fatty acid receptor 2 (FFA2) agonists: identification of the structural and chemical requirements for selective activation of FFA2 versus FFA3 J. Biol. Chem. 286 2011 10628 10640
49. A. Schwiertz, D. Taras, K. Schäfer, S. Beijer, N.A. Bos, C. Donus, and P.D. Hardt Microbiota and SCFA in lean and overweight healthy subjects Obesity (Silver Spring) 18 2010 190 195
50. G. Tolhurst, H. Heffron, Y.S. Lam, H.E. Parker, A.M. Habib, E. Diakogiannaki, J. Cameron, J. Grosse, F. Reimann, and F.M. Gribble Short-chain fatty acids stimulate glucagon-like peptide-1 secretion via the G-protein-coupled receptor FFAR2 Diabetes 61 2012 364 371
51. S. Troy, M. Soty, L. Ribeiro, L. Laval, S. Migrenne, X. Fioramonti, B. Pillot, V. Fauveau, R. Aubert, and B. Viollet et al. Intestinal gluconeogenesis is a key factor for early metabolic changes after gastric bypass but not after gastric lap-band in mice Cell Metab. 8 2008 201 211
52. P.J. Turnbaugh, R.E. Ley, M.A. Mahowald, V. Magrini, E.R. Mardis, and J.I. Gordon An obesity-associated gut microbiome with increased capacity for energy harvest Nature 444 2006 1027 1031
53. P.J. Turnbaugh, F. Bäckhed, L. Fulton, and J.I. Gordon Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome Cell Host Microbe 3 2008 213 223
54. P.J. Turnbaugh, M. Hamady, T. Yatsunenko, B.L. Cantarel, A. Duncan, R.E. Ley, M.L. Sogin, W.J. Jones, B.A. Roe, and J.P. Affourtit et al. A core gut microbiome in obese and lean twins Nature 457 2009 480 484
55. P.J. Turnbaugh, V.K. Ridaura, J.J. Faith, F.E. Rey, R. Knight, and J.I. Gordon The effect of diet on the human gut microbiome: a metagenomic analysis in humanized gnotobiotic mice Sci. Transl. Med. 1 2009 ra14
56. A. Wang, H. Si, D. Liu, and H. Jiang Butyrate activates the cAMP-protein kinase A-cAMP response element-binding protein signaling pathway in Caco-2 cells J. Nutr. 142 2012 1 6