Farnesoid X receptor signaling shapes the gut microbiota and controls hepatic lipid metabolism

mSystems

Volumn 1, Issue 5, 2016, Pages

  Zhang, Limin ^a,b   Xie, Cen ^c   Nichols, Robert G ^a   Chan, Siu H J ^d   Jiang, Changtao ^e   Hao, Ruixin ^a   Smith, Philip B ^f   Cai, Jingwei ^a   Simons, Margaret N ^d   Hatzakis, Emmanuel ^a,g   Maranas, Costas D ^d   Gonzalez, Frank J ^c   Patterson, Andrew D ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^c NATIONAL CANCER INSTITUTE   (United States)

^d The Pennsylvania State University   (United States)

^e PEKING UNIVERSITY HEALTH SCIENCE CENTER   (China)

^f PENNSYLVANIA STATE UNIVERSITY   (United States)

^g OHIO STATE UNIVERSITY   (United States)

Author keywords

Bile acid; Farnesoid X receptor; Genome scale metabolic models; Gut microbiota; Metabolomics; Nonalcoholic fatty liver disease

Indexed keywords

EID: 85006765148     PISSN: None     EISSN: 23795077     Source Type: Journal    
DOI: 10.1128/mSystems.00070-16     Document Type: Article

References (43)

1. Waalen J. 2014. The genetics of human obesity. Transl Res 164:293-301. http://dx.doi.org/10.1016/j.trsl.2014.05.010. http://dx.doi.org/10.1016/j.trsl.2014.05.010.
2. Marti A, Moreno-Aliaga MJ, Hebebrand J, Martinez JA. 2004. Genes, lifestyles and obesity. Int J Obes Relat Metab Disord 28(Suppl 3): S29-S36. http://dx.doi.org/10.1038/sj.ijo.0802808.
3. Inadera H. 2013. Developmental origins of obesity and type 2 diabetes: molecular aspects and role of chemicals. Environ Health Prev Med 18:185-197. http://dx.doi.org/10.1007/s12199-013-0328-8.
4. Steinberger J, Daniels SR. 2003. Obesity, insulin resistance, diabetes, and cardiovascular risk in children: an American Heart Association scientific statement from the Atherosclerosis, Hypertension, and Obesity in the Young Committee (Council on Cardiovascular Disease in the Young) and the Diabetes Committee (Council on Nutrition, Physical Activity, and Metabolism). Circulation 107:1448-1453. http://dx.doi.org/10.1161/01.CIR.0000060923.07573.F2.
5. Mokdad AH, Ford ES, Bowman BA, Dietz WH, Vinicor F, Bales VS, Marks JS. 2003. Prevalence of obesity, diabetes, and obesity-related health risk factors. JAMA 289:76-79. http://dx.doi.org/10.1001/jama.289.1.76.
6. Ishigaki Y, Katagiri H, Yamada T, Ogihara T, Imai J, Uno K, Hasegawa Y, Gao J, Ishihara H, Shimosegawa T, Sakoda H, Asano T, Oka Y. 2005. Dissipating excess energy stored in the liver is a potential treatment strategy for diabetes associated with obesity. Diabetes 54: 322-332. http://dx.doi.org/10.2337/diabetes.54.2.322.
7. Lipina C, Rastedt W, Irving AJ, Hundal HS. 2012. New vistas for treatment of obesity and diabetes? Endocannabinoid signalling and metabolism in the modulation of energy balance. Bioessays 34:681-691. http://dx.doi.org/10.1002/bies.201200031.
8. Matsubara T, Li F, Gonzalez FJ. 2013. FXR signaling in the enterohepatic system. Mol Cell Endocrinol 368:17-29. http://dx.doi.org/10.1016/j.mce.2012.05.004.
9. Li F, Jiang C, Krausz KW, Li Y, Albert I, Hao H, Fabre KM, Mitchell JB, Patterson AD, Gonzalez FJ. 2013. Microbiome remodelling leads to inhibition of intestinal farnesoid X receptor signalling and decreased obesity. Nat Commun 4:2384. http://dx.doi.org/10.1038/ncomms3384.
10. Jiang C, Xie C, Li F, Zhang L, Nichols RG, Krausz KW, Cai J, Qi Y, Fang ZZ, Takahashi S, Tanaka N, Desai D, Amin SG, Albert I, Patterson AD, Gonzalez FJ. 2015. Intestinal farnesoid X receptor signaling promotes nonalcoholic fatty liver disease. J Clin Invest 125:386-402. http://dx.doi.org/10.1172/JCI76738.
11. Jiang C, Xie C, Lv Y, Li J, Krausz K, Shi J, Brocker C, Desai D, Amin S, Bisson W, Liu Y, Gavrilova O, Patterson A, Gonzalez F. 2015. Intestine-selective farnesoid X receptor inhibition improves obesityrelated metabolic dysfunction. Nat Commun 6:10166. http://dx.doi.org/10.1038/ncomms10166.
12. Sinal CJ, Tohkin M, Miyata M, Ward JM, Lambert G, Gonzalez FJ. 2000. Targeted disruption of the nuclear receptor FXR/BAR impairs bile acid and lipid homeostasis. Cell 102:731-744. http://dx.doi.org/10.1016/S0092-8674(00)00062-3.
13. Seyer P, Vallois D, Poitry-Yamate C, Schutz F, Metref S, Tarussio D, Maechler P, Staels B, Lanz B, Grueter R, Decaris J, Turner S, da Costa A, Preitner F, Minehira K, Foretz M, Thorens B. 2013. Hepatic glucose sensing is required to preserve beta cell glucose competence. J Clin Invest 123:1662-1676. http://dx.doi.org/10.1172/JCI65538.
14. Claudel T, Staels B, Kuipers F. 2005. The farnesoid X receptor: a molecular link between bile acid and lipid and glucose metabolism. Arterioscler Thromb Vasc Biol 25:2020-2030. http://dx.doi.org/10.1161/01.ATV.0000178994.21828.a7.
15. Lefebvre P, Cariou B, Lien F, Kuipers F, Staels B. 2009. Role of bile acids and bile acid receptors in metabolic regulation. Physiol Rev 89: 147-191. http://dx.doi.org/10.1152/physrev.00010.2008.
16. Tsuchida T, Shiraishi M, Ohta T, Sakai K, Ishii S. 2012. Ursodeoxycholic acid improves insulin sensitivity and hepatic steatosis by inducing the excretion of hepatic lipids in high-fat diet-fed KK-Ay mice. Metabolism 61:944-953. http://dx.doi.org/10.1016/j.metabol.2011.10.023.
17. Ratziu V, de Ledinghen V, Oberti F, Mathurin P, Wartelle-Bladou C, Renou C, Sogni P, Maynard M, Larrey D, Serfaty L, Bonnefont-Rousselot D, Bastard JP, Riviere M, Spenard J, FRESGUN. 2011. A randomized controlled trial of high-dose ursodesoxycholic acid for nonalcoholic steatohepatitis. J Hepatol 54:1011-1019. http://dx.doi.org/10.1016/j.hep.2010.08.030.
18. Sayin SI, Wahlstrom A, Felin J, Jantti S, Marschall HU, Bamberg K, Angelin B, Hyotylainen T, Orešič M, Backhed F. 2013. Gut microbiota regulates bile acid metabolism by reducing the levels of tauro-betamuricholic acid, a naturally occurring FXR antagonist. Cell Metab 17: 225-235. http://dx.doi.org/10.1016/j.cmet.2013.01.003.
19. Ridlon JM, Kang DJ, Hylemon PB, Bajaj JS. 2014. Bile acids and the gut microbiome. Curr Opin Gastroenterol 30:332-338. http://dx.doi.org/10.1097/MOG.0000000000000057.
20. Tuominen I, Beaven SW. 2015. Intestinal farnesoid X receptor puts a fresh coat of wax on fatty liver. Hepatology 62:646-648. http://dx.doi.org/10.1002/hep.27910.
21. Joyce SA, MacSharry J, Casey PG, Kinsella M, Murphy EF, Shanahan F, Hill C, Gahan CG. 2014. Regulation of host weight gain and lipid metabolism by bacterial bile acid modification in the gut. Proc Natl Acad Sci U S A 111:7421-7426. http://dx.doi.org/10.1073/pnas.1323599111.
22. Caricilli AM, Saad MJ. 2014. Gut microbiota composition and its effects on obesity and insulin resistance. Curr Opin Clin Nutr Metab Care 17:312-318. http://dx.doi.org/10.1097/MCO.0000000000000067.
23. Gonzalez FJ, Jiang C, Bisson WH, Patterson AD. 2015. Inhibition of farnesoid X receptor signaling shows beneficial effects in human obesity. J Hepatol 62:1234-1236. http://dx.doi.org/10.1016/j.jhep.2015.02.043.
24. Fang S, Suh JM, Reilly SM, Yu E, Osborn O, Lackey D, Yoshihara E, Perino A, Jacinto S, Lukasheva Y, Atkins AR, Khvat A, Schnabl B, Yu RT, Brenner DA, Coulter S, Liddle C, Schoonjans K, Olefsky JM, Saltiel AR, Downes M, Evans RM. 2015. Intestinal FXR agonism promotes adipose tissue browning and reduces obesity and insulin resistance. Nat Med 21:159-165. http://dx.doi.org/10.1038/nm.3760.
25. Zhang L, Hatzakis E, Nichols RG, Hao R, Correll J, Smith PB, Chiaro CR, Perdew GH, Patterson AD. 2015. Metabolomics reveals that aryl hydrocarbon receptor activation by environmental chemicals induces systemic metabolic dysfunction in mice. Environ Sci Technol 49: 8067-8077. http://dx.doi.org/10.1021/acs.est.5b01389.
26. Bervoets L, Van Hoorenbeeck K, Kortleven I, Van Noten C, Hens N, Vael C, Goossens H, Desager KN, Vankerckhoven V. 2013. Differences in gut microbiota composition between obese and lean children: a cross-sectional study. Gut Pathog 5:10. http://dx.doi.org/10.1186/1757-4749-5-10.
27. Clarke SF, Murphy EF, Nilaweera K, Ross PR, Shanahan F, O'Toole PW, Cotter PD. 2012. The gut microbiota and its relationship to diet and obesity: new insights. Gut Microbes 3:186-202. http://dx.doi.org/10.4161/gmic.20168.
28. Clarke SF, Murphy EF, O'Sullivan O, Ross RP, O'Toole PW, Shanahan F, Cotter PD. 2013. Targeting the microbiota to address diet-induced obesity: a time dependent challenge. PLoS One 8:e65790. http://dx.doi.org/10.1371/journal.pone.0065790.
29. Turnbaugh PJ, Hamady M, Yatsunenko T, Cantarel BL, Duncan A, Ley RE, Sogin ML, Jones WJ, Roe BA, Affourtit JP, Egholm M, Henrissat B, Heath AC, Knight R, Gordon JI. 2009. A core gut microbiome in obese and lean twins. Nature 457:480-484. http://dx.doi.org/10.1038/nature07540.
30. Parseus A, Sommer N, Sommer F, Caesar R, Molinaro A, Stahlman M, Greiner TU, Perkins R, Backhed F. January 6 2016. Microbiota-induced obesity requires farnesoid X receptor. Gut http://dx.doi.org/10.1136/gutjnl-2015-310283.
31. Larsen N, Vogensen FK, van den Berg FW, Nielsen DS, Andreasen AS, Pedersen BK, Al-Soud WA, Sorensen SJ, Hansen LH, Jakobsen M. 2010. Gut microbiota in human adults with type 2 diabetes differs from non-diabetic adults. PLoS One 5:e9085. http://dx.doi.org/10.1371/journal.pone.0009085.
32. Liou AP, Paziuk M, Luevano JM, Jr, Machineni S, Turnbaugh PJ, Kaplan LM. 2013. Conserved shifts in the gut microbiota due to gastric bypass reduce host weight and adiposity. Sci Transl Med 5:178ra141. http://dx.doi.org/10.1126/scitranslmed.3005687.
33. Schwiertz A, Taras D, Schafer K, Beijer S, Bos NA, Donus C, Hardt PD. 2010. Microbiota and SCFA in lean and overweight healthy subjects. Obesity 18:190-195. http://dx.doi.org/10.1038/oby.2009.167.
34. Den Besten G, van Eunen K, Groen AK, Venema K, Reijngoud DJ, Bakker BM. 2013. The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism. J Lipid Res 54:2325-2340. http://dx.doi.org/10.1194/jlr.R036012.
35. Zhang L, Nichols RG, Correll J, Murray IA, Tanaka N, Smith PB, Hubbard TD, Sebastian A, Albert I, Hatzakis E, Gonzalez FJ, Perdew GH, Patterson AD. 2015. Persistent organic pollutants modify gut microbiota-host metabolic homeostasis in mice through aryl hydrocarbon receptor activation. Environ Health Perspect 123:679-688. http://dx.doi.org/10.1289/ehp.1409055.
36. Lahti L, Salonen A, Kekkonen RA, Salojarvi J, Jalanka-Tuovinen J, Palva A, Orešič M, de Vos WM. 2013. Associations between the human intestinal microbiota, Lactobacillus rhamnosus GG and serum lipids indicated by integrated analysis of high-throughput profiling data. PeerJ 1:e32. http://dx.doi.org/10.7717/peerj.32.
37. Vajro P, Paolella G, Fasano A. 2013. Microbiota and gut-liver axis: their influences on obesity and obesity-related liver disease. J Pediatr Gastroe n t e r o l Nutr 5 6:461-4 6 8. h t t p://d x. d o i. o r g/1 0. 1 0 9 7/MPG.0b013e318284abb5.
38. Kozich JJ, Westcott SL, Baxter NT, Highlander SK, Schloss PD. 2013. Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl Environ Microbiol 79:5112-5120. http://dx.doi.org/10.1128/AEM.01043-13.
39. Langille MG, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA, Clemente JC, Burkepile DE, Vega Thurber RL, Knight R, Beiko RG, Huttenhower C. 2013. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences Nat Biotechnol 31:814-821. http://dx.doi.org/10.1038/nbt.2676.
40. Abubucker S, Segata N, Goll J, Schubert AM, Izard J, Cantarel BL, Rodriguez-Mueller B, Zucker J, Thiagarajan M, Henrissat B, White O, Kelley ST, Methe B, Schloss PD, Gevers D, Mitreva M, Huttenhower C. 2012. Metabolic reconstruction for metagenomic data and its application to the human microbiome. PLoS Comput Biol 8:e1002358. http://dx.doi.org/10.1371/journal.pcbi.1002358.
41. Orth JD, Thiele I, Palsson BO. 2010. What is flux balance analysis? Nat Biotechnol 28:245-248. http://dx.doi.org/10.1038/nbt.1614.
42. Mahadevan R, Schilling CH. 2003. The effects of alternate optimal solutions in constraint-based genome-scale metabolic models. Metab Eng 5:264-276. http://dx.doi.org/10.1016/j.ymben.2003.09.002.
43. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF. 2009. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537-7541. http://dx.doi.org/10.1128/AEM.01541-09.