Induction of farnesoid X receptor signaling in germ-free mice colonized with a human microbiota

Journal of Lipid Research

Volumn 58, Issue 2, 2017, Pages 412-419

  Wahlström, Annika ^a   Kovatcheva Datchary, Petia ^a   Ståhlman, Marcus ^a   Khan, Muhammad Tanweer ^a   Bäckhed, Fredrik ^a,b   Marschall, Hanns Ulrich ^a  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b Capital Region   (Denmark)

Author keywords

Bile acids and salts; Biosynthesis and metabolism; Enzyme mechanisms and regulation; Farnesoid X receptor agonist; Farnesoid X receptor antagonist; Gut microbiota; Humanized mouse models; Intestine

Indexed keywords

BILE ACID; FARNESOID X RECEPTOR; PROTEIN TYROSINE PHOSPHATASE SHP; FIBROBLAST GROWTH FACTOR; FIBROBLAST GROWTH FACTOR 15, MOUSE; FXR1H PROTEIN, MOUSE; NERVE PROTEIN; RNA BINDING PROTEIN; SYNAPTO-PHLUORIN PROTEIN, MOUSE; TAUROCHOLIC ACID; TAUROMURICHOLIC ACID;

ADULT; ANIMAL TISSUE; ARTICLE; BILE ACID METABOLISM; CECUM; CONTROLLED STUDY; FECES; FEMALE; FGF15 GENE; GENE; GERMFREE MOUSE; HUMAN; ILEUM; INTESTINE FLORA; LIVER; MALE; MICROBIAL COLONIZATION; MOUSE; NONHUMAN; PROTEIN EXPRESSION; SHP GENE; SIGNAL TRANSDUCTION; AGONISTS; ANALOGS AND DERIVATIVES; ANIMAL; ANTAGONISTS AND INHIBITORS; GENETICS; INTESTINE; METABOLIC DISORDER; METABOLISM; MICROBIOLOGY; PATHOLOGY;

ANIMALS; BILE ACIDS AND SALTS; FECES; FIBROBLAST GROWTH FACTORS; GASTROINTESTINAL MICROBIOME; HUMANS; ILEUM; INTESTINES; LIVER; METABOLIC DISEASES; MICE; NERVE TISSUE PROTEINS; RNA-BINDING PROTEINS; TAUROCHOLIC ACID;

EID: 85011015649     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M072819     Document Type: Article

References (44)

1. Karlsson, F., V. Tremaroli, J. Nielsen, and F. Backhed. 2013. Assessing the human gut microbiota in metabolic diseases. Diabetes. 62: 3341-3349.
2. Lefebvre, P., B. Cariou, F. Lien, F. Kuipers, and B. Staels. 2009. Role of bile acids and bile acid receptors in metabolic regulation. Physiol. Rev. 89: 147-191.
3. Ma, H., and M. E. Patti. 2014. Bile acids, obesity, and the metabolic syndrome. Best Pract. Res. Clin. Gastroenterol. 28: 573-583.
4. Sato, H., A. Macchiarulo, C. Thomas, A. Gioiello, M. Une, A. F. Hofmann, R. Saladin, K. Schoonjans, R. Pellicciari, and J. Auwerx. 2008. Novel potent and selective bile acid derivatives as TGR5 agonists: biological screening, structure-activity relationships, and molecular modeling studies. J. Med. Chem. 51: 1831-1841.
5. Parks, D. J., S. G. Blanchard, R. K. Bledsoe, G. Chandra, T. G. Consler, S. A. Kliewer, J. B. Stimmel, T. M. Willson, A. M. Zavacki, D. D. Moore, et al. 1999. Bile acids: natural ligands for an orphan nuclear receptor. Science. 284: 1365-1368.
6. Wang, H., J. Chen, K. Hollister, L. C. Sowers, and B. M. Forman. 1999. Endogenous bile acids are ligands for the nuclear receptor FXR/BAR. Mol. Cell. 3: 543-553.
7. Sayin, S. I., A. Wahlstrom, J. Felin, S. Jantti, H. U. Marschall, K. Bamberg, B. Angelin, T. Hyotylainen, M. Oresic, and F. Backhed. 2013. Gut microbiota regulates bile acid metabolism by reducing the levels of tauro-beta-muricholic acid, a naturally occurring FXR antagonist. Cell Metab. 17: 225-235.
8. Li, F., C. T. Jiang, K. W. Krausz, Y. F. Li, I. Albert, H. P. Hao, K. M. Fabre, J. B. Mitchell, A. D. Patterson, and F. J. Gonzalez. 2013. Microbiome remodelling leads to inhibition of intestinal farnesoid X receptor signalling and decreased obesity. Nat. Commun. 4: 2384.
9. Wahlström, A., S. Sayin, H. Marschall, and F. Bäckhed. 2016. Intestinal crosstalk between bile acids and microbiota and its impact on host metabolism. Cell Metab. 24: 41-50.
10. Turnbaugh, P. J., R. E. Ley, M. A. Mahowald, V. Magrini, E. R. Mardis, and J. I. Gordon. 2006. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature. 444: 1027-1031.
11. Turnbaugh, P. J., V. K. Ridaura, J. J. Faith, F. E. Rey, R. Knight, and J. I. Gordon. 2009. The effect of diet on the human gut microbiome: a metagenomic analysis in humanized gnotobiotic mice. Sci. Transl. Med. 1: 6ra14.
12. Seedorf, H., N. W. Griffin, V. K. Ridaura, A. Reyes, J. Cheng, F. E. Rey, M. I. Smith, G. M. Simon, R. H. Scheffrahn, D. Woebken, et al. 2014. Bacteria from diverse habitats colonize and compete in the mouse gut. Cell. 159: 253-266.
13. Segata, N., J. Izard, L. Waldron, D. Gevers, L. Miropolsky, W. S. Garrett, and C. Huttenhower. 2011. Metagenomic biomarker discovery and explanation. Genome Biol. 12: R60.
14. Tremaroli, V., F. Karlsson, M. Werling, M. Stahlman, P. Kovatcheva-Datchary, T. Olbers, L. Fandriks, C. W. le Roux, J. Nielsen, and F. Backhed. 2015. Roux-en-Y gastric bypass and vertical banded gastroplasty induce long-term changes on the human gut microbiome contributing to fat mass regulation. Cell Metab. 22: 228-238.
15. Festing, M. F., and D. G. Altman. 2002. Guidelines for the design and statistical analysis of experiments using laboratory animals. ILAR J. 43: 244-258.
16. Holt, J. A., G. Luo, A. N. Billin, J. Bisi, Y. Y. McNeill, K. F. Kozarsky, M. Donahee, D. Y. Wang, T. A. Mansfield, S. A. Kliewer, et al. 2003. Definition of a novel growth factor-dependent signal cascade for the suppression of bile acid biosynthesis. Genes Dev. 17: 1581-1591.
17. Inagaki, T., M. Choi, A. Moschetta, L. Peng, C. L. Cummins, J. G. McDonald, G. Luo, S. A. Jones, B. Goodwin, J. A. Richardson, et al. 2005. Fibroblast growth factor 15 functions as an enterohepatic signal to regulate bile acid homeostasis. Cell Metab. 2: 217-225.
18. Lundåsen, T., C. Galman, B. Angelin, and M. Rudling. 2006. Circulating intestinal fibroblast growth factor 19 has a pronounced diurnal variation and modulates hepatic bile acid synthesis in man. J. Intern. Med. 260: 530-536.
19. Kim, I., S. H. Ahn, T. Inagaki, M. Choi, S. Ito, G. L. Guo, S. A. Kliewer, and F. J. Gonzalez. 2007. Differential regulation of bile acid homeostasis by the farnesoid X receptor in liver and intestine. J. Lipid Res. 48: 2664-2672.
20. Lu, T. T., M. Makishima, J. J. Repa, K. Schoonjans, T. A. Kerr, J. Auwerx, and D. J. Mangelsdorf. 2000. Molecular basis for feedback regulation of bile acid synthesis by nuclear receptors. Mol. Cell. 6: 507-515.
21. Goodwin, B., S. A. Jones, R. R. Price, M. A. Watson, D. D. McKee, L. B. Moore, C. Galardi, J. G. Wilson, M. C. Lewis, M. E. Roth, et al. 2000. A regulatory cascade of the nuclear receptors FXR, SHP-1, and LRH-1 represses bile acid biosynthesis. Mol. Cell. 6: 517-526.
22. Russell, D. W. 2003. The enzymes, regulation, and genetics of bile acid synthesis. Annu. Rev. Biochem. 72: 137-174.
23. Out, C., J. Hageman, V. W. Bloks, H. Gerrits, M. D. Sollewijn Gelpke, T. Bos, R. Havinga, M. J. Smit, F. Kuipers, and A. K. Groen. 2011. Liver receptor homolog-1 is critical for adequate up-regulation of Cyp7a1 gene transcription and bile salt synthesis during bile salt sequestration. Hepatology. 53: 2075-2085.
24. Inoue, Y., A. M. Yu, S. H. Yim, X. Ma, K. W. Krausz, J. Inoue, C. C. Xiang, M. J. Brownstein, G. Eggertsen, I. Bjorkhem, et al. 2006. Regulation of bile acid biosynthesis by hepatocyte nuclear factor 4alpha. J. Lipid Res. 47: 215-227.
25. Abrahamsson, A., U. Gustafsson, E. Ellis, L. M. Nilsson, S. Sahlin, I. Bjorkhem, and C. Einarsson. 2005. Feedback regulation of bile acid synthesis in human liver: importance of HNF-4alpha for regulation of CYP7A1. Biochem. Biophys. Res. Commun. 330: 395-399.
26. Song, P., C. E. Rockwell, J. Y. Cui, and C. D. Klaassen. 2015. Individual bile acids have differential effects on bile acid signaling in mice. Toxicol. Appl. Pharmacol. 283: 57-64.
27. Sacquet, E. C., D. P. Gadelle, M. J. Riottot, and P. M. Raibaud. 1984. Absence of transformation of beta-muricholic acid by human microflora implanted in the digestive tracts of germfree male rats. Appl. Environ. Microbiol. 47: 1167-1168.
28. Sacquet, E., M. Parquet, M. Riottot, A. Raizman, B. Nordlinger, and R. Infante. 1985. Metabolism of beta-muricholic acid in man. Steroids. 45: 411-426.
29. Frese, S. A., A. K. Benson, G. W. Tannock, D. M. Loach, J. Kim, M. Zhang, P. L. Oh, N. C. Heng, P. B. Patil, N. Juge, et al. 2011. The evolution of host specialization in the vertebrate gut symbiont Lactobacillus reuteri. PLoS Genet. 7: e1001314.
30. Martin, F. P., M. E. Dumas, Y. Wang, C. Legido-Quigley, I. K. Yap, H. Tang, S. Zirah, G. M. Murphy, O. Cloarec, J. C. Lindon, et al. 2007. A top-down systems biology view of microbiome-mammalian metabolic interactions in a mouse model. Mol. Syst. Biol. 3: 112.
31. Martin, F. P., Y. Wang, N. Sprenger, I. K. Yap, T. Lundstedt, P. Lek, S. Rezzi, Z. Ramadan, P. van Bladeren, L. B. Fay, et al. 2008. Probiotic modulation of symbiotic gut microbial-host metabolic interactions in a humanized microbiome mouse model. Mol. Syst. Biol. 4: 157.
32. Zhang, Y., P. B. Limaye, H. J. Renaud, and C. D. Klaassen. 2014. Effect of various antibiotics on modulation of intestinal microbiota and bile acid profile in mice. Toxicol. Appl. Pharmacol. 277: 138-145.
33. Sacquet, E. C., P. M. Raibaud, C. Mejean, M. J. Riottot, C. Leprince, and P. C. Leglise. 1979. Bacterial formation of omega-muricholic acid in rats. Appl. Environ. Microbiol. 37: 1127-1131.
34. Eyssen, H., G. De Pauw, J. Stragier, and A. Verhulst. 1983. Cooperative formation of omega-muricholic acid by intestinal microorganisms. Appl. Environ. Microbiol. 45: 141-147.
35. Degirolamo, C., S. Rainaldi, F. Bovenga, S. Murzilli, and A. Moschetta. 2014. Microbiota modification with probiotics induces hepatic bile acid synthesis via downregulation of the Fxr-Fgf15 axis in mice. Cell Reports. 7: 12-18.
36. Bayerdörffer, E., G. A. Mannes, T. Ochsenkühn, P. Dirschedl, B. Wiebecke, and G. Paumgartner. 1995. Unconjugated secondary bile acids in the serum of patients with colorectal adenomas. Gut. 36: 268-273.
37. Hamilton, J. P., G. Xie, J. P. Raufman, S. Hogan, T. L. Griffin, C. A. Packard, D. A. Chatfield, L. R. Hagey, J. H. Steinbach, and A. F. Hofmann. 2007. Human cecal bile acids: concentration and spectrum. Am. J. Physiol. Gastrointest. Liver Physiol. 293: G256-G263.
38. Devlin, A. S., and M. A. Fischbach. 2015. A biosynthetic pathway for a prominent class of microbiota-derived bile acids. Nat. Chem. Biol. 11: 685-690.
39. Eyssen, H. J., G. G. Parmentier, and J. A. Mertens. 1976. Sulfate bile acids in germ-free and conventional mice. Eur. J. Biochem. 66: 507-514.
40. Zhang, Y., and C. D. Klaassen. 2010. Effects of feeding bile acids and a bile acid sequestrant on hepatic bile acid composition in mice. J. Lipid Res. 51: 3230-3242.
41. Alnouti, Y. 2009. Bile Acid sulfation: a pathway of bile acid elimination and detoxification. Toxicol. Sci. 108: 225-246.
42. Hagey, L. R., and M. D. Krasowski. 2013. Microbial biotransformations of bile acids as detected by electrospray mass spectrometry. Adv. Nutr. 4: 29-35.
43. Jiang, C., C. Xie, F. Li, L. Zhang, R. G. Nichols, K. W. Krausz, J. Cai, Y. Qi, Z. Z. Fang, S. Takahashi, et al. 2015. Intestinal farnesoid X receptor signaling promotes nonalcoholic fatty liver disease. J. Clin. Invest. 125: 386-402.
44. Takahashi, S., T. Fukami, Y. Masuo, C. N. Brocker, C. Xie, K. W. Krausz, C. R. Wolf, C. J. Henderson, and F. J. Gonzalez. 2016. Cyp2c70 is responsible for the species difference in bile acid metabolism between mice and humans. J. Lipid Res. 57: 2130-2137.