Microbiome remodelling leads to inhibition of intestinal farnesoid X receptor signalling and decreased obesity

Nature Communications

Volumn 4, Issue , 2013, Pages

  Li, Fei ^a   Jiang, Changtao ^a   Krausz, Kristopher W ^a   Li, Yunfei ^b   Albert, Istvan ^b   Hao, Haiping ^a   Fabre, Kristin M ^a   Mitchell, James B ^a   Patterson, Andrew D ^a,b   Gonzalez, Frank J ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BILE ACID; BILE SALT; CHOLIC ACID DERIVATIVE; FARNESOID X RECEPTOR; HYDROLASE; INSULIN; TAURINE; TEMPOL; AMIDASE; AMINE OXIDE; ANTIOBESITY AGENT; ANTIOXIDANT; BACTERIAL PROTEIN; CELL RECEPTOR; CHOLOYLGLYCINE HYDROLASE; FARNESOID X-ACTIVATED RECEPTOR; GLUCOSE; SPIN LABELING; TAUROCHOLIC ACID; TAUROMURICHOLIC ACID; DRUG DERIVATIVE;

ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; GENE SEQUENCE; HOMEOSTASIS; INSULIN BLOOD LEVEL; INSULIN RESISTANCE; INSULIN SENSITIVITY; INTESTINE FLORA; LACTOBACILLUS; LIPID DIET; METABOLOMICS; METAGENOMICS; MICROBIOME; MOUSE; NONHUMAN; OBESITY; SIGNAL TRANSDUCTION; WEIGHT GAIN; AGONISTS; ANALOGS AND DERIVATIVES; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; DEFICIENCY; DRUG EFFECTS; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; INTESTINE; INTESTINE ABSORPTION; KNOCKOUT MOUSE; LIPID METABOLISM; MALE; METABOLISM; MICROBIOLOGY; MICROFLORA; PHYSIOLOGY; SPIN LABELING; DRUG ANTAGONISM; DRUG EFFECT; DRUG POTENTIATION;

LACTOBACILLUS; MUS;

AMIDOHYDROLASES; ANIMALS; ANTI-OBESITY AGENTS; ANTIOXIDANTS; BACTERIAL PROTEINS; CYCLIC N-OXIDES; DIET, HIGH-FAT; GENE EXPRESSION REGULATION; GLUCOSE; INTESTINAL ABSORPTION; INTESTINES; LACTOBACILLUS; LIPID METABOLISM; MALE; MICE; MICE, KNOCKOUT; MICROBIOTA; OBESITY; RECEPTORS, CYTOPLASMIC AND NUCLEAR; SIGNAL TRANSDUCTION; SPIN LABELS; TAUROCHOLIC ACID;

EID: 84887960056     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms3384     Document Type: Article

References (45)

1. Khandekar, M. J., Cohen, P. & Spiegelman, B. M. Molecular mechanisms of cancer development in obesity. Nat. Rev. Cancer 11, 886-895 (2011).
2. Li, Y. et al. Homocysteine upregulates resistin production from adipocytes in vivo and in vitro. Diabetes 57, 817-827 (2008).
3. Wadikar, D. D. & Premavalli, K. S. Appetite control and obesity. Crit. Rev. Food. Sci. Nutr. 52, 949-956 (2012).
4. Soule, B. P. et al. The chemistry and biology of nitroxide compounds. Free Radic. Biol. Med. 42, 1632-1650 (2007).
5. Mitchell, J. B. et al. The antioxidant tempol reduces carcinogenesis and enhances survival in mice when administered after nonlethal total body radiation. Cancer Res. 72, 4846-4855 (2012).
6. Mitchell, J. B. et al. A low molecular weight antioxidant decreases weight and lowers tumor incidence. Free Radic. Biol. Med. 34, 93-102 (2003).
7. Li, F. et al. Stable isotope- and mass spectrometry-based metabolomics as tools in drug metabolism: a study expanding tempol pharmacology. J. Proteome Res. 12, 1369-1376 (2013).
8. Berber, I. et al. Tempol reduces bacterial translocation after ischemia/reperfusion injury in a rat model of superior mesenteric artery occlusion. Surg. Today 39, 407-413 (2009).
9. Idle, J. R. & Gonzalez, F. J. Metabolomics. Cell Metab. 6, 348-351 (2007).
10. Tuohy, K. M. et al. Studying the human gut microbiota in the trans-omics era - focus on metagenomics and metabonomics. Curr. Pharm. Des. 15, 1415-1427 (2009).
11. 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).
12. Turnbaugh, P. J. et al. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444, 1027-1031 (2006).
13. Turnbaugh, P. J. & Gordon, J. I. An invitation to the marriage of metagenomics and metabolomics. Cell 134, 708-713 (2008).
14. Shukla, O. P. Microbial transformation of quinoline by a Pseudomonas sp. Appl. Environ. Microbiol. 51, 1332-1342 (1986).
15. Wikoff, W. R. et al. Metabolomics analysis reveals large effects of gut microflora on mammalian blood metabolites. Proc. Natl Acad. Sci. USA 106, 3698-3703 (2009).
16. Ridlon, J. M., Kang, D. J. & Hylemon, P. B. Bile salt biotransformations by human intestinal bacteria. J. Lipid Res. 47, 241-259 (2006).
17. Zhang, Y., Limaye, P. B., Lehman-McKeeman, L. D. & Klaassen, C. D. Dysfunction of organic anion transporting polypeptide 1a1 alters intestinal bacteria and bile acid metabolism in mice. PLoS One 7, e34522 (2012).
18. Yoshimoto, S. et al. Obesity-induced gut microbial metabolite promotes liver cancer through senescence secretome. Nature 499, 97-101 (2013).
19. Swann, J. R. et al. Systemic gut microbial modulation of bile acid metabolism in host tissue compartments. Proc. Natl Acad. Sci. USA 108(Suppl 1): 4523-4530 (2011).
20. De Wit, N. J. et al. The role of the small intestine in the development of dietary fat-induced obesity and insulin resistance in C57BL/6J mice. BMC. Med. Genomics 1, 14 (2008).
21. Sayin, S. I. et al. 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 (2013).
22. Chavez, J. A. & Summers, S. A. A ceramide-centric view of insulin resistance. Cell Metab. 15, 585-594 (2012).
23. Phillips, S. A., Sylvester, F. A. & Frisbee, J. C. Oxidant stress and constrictor reactivity impair cerebral artery dilation in obese Zucker rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 288, R522-R530 (2005).
24. Kim, I. et al. Differential regulation of bile acid homeostasis by the farnesoid X receptor in liver and intestine. J. Lipid. Res. 48, 2664-2672 (2007).
25. Musso, G., Gambino, R. & Cassader, M. Obesity, diabetes, and gut microbiota: the hygiene hypothesis expanded? Diab. Care 33, 2277-2284 (2010).
26. Angelakis, E. & Raoult, D. The increase of Lactobacillus species in the gut flora of newborn broiler chicks and ducks is associated with weight gain. PLoS One 5, e10463 (2010).
27. Larsen, N. et al. Gut microbiota in human adults with type 2 diabetes differs from non-diabetic adults. PLoS One 5, e9085 (2010).
28. Liou, A. P. et al. Conserved shifts in the gut microbiota due to gastric bypass reduce host weight and adiposity. Sci. Transl. Med. 5, 178ra41 (2013).
29. Jiang, J. K. et al. Diversity of bile salt hydrolase activities in different lactobacilli toward human bile salts. Ann. Microbiol. 60, 81-88 (2010).
30. Donohoe, D. R. et al. The microbiome and butyrate regulate energy metabolism and autophagy in the mammalian colon. Cell Metab. 13, 517-526 (2011).
31. Beltowski, J., Jamroz-Wisniewska, A., Borkowska, E., Nazar, J. & Marciniak, A. Antioxidant treatment normalizes renal Na + ,K + -ATPase activity in leptin-treated rats. Pharmacol. Rep. 57, 219-228 (2005).
32. Kimura, I. et al. The gut microbiota suppresses insulin-mediated fat accumulation via the short-chain fatty acid receptor GPR43. Nat. Commun. 4, 1829 (2013).
33. Ma, K., Saha, P. K., Chan, L. & Moore, D. D. Farnesoid X receptor is essential for normal glucose homeostasis. J. Clin. Invest. 116, 1102-1109 (2006).
34. Zhang, Y. et al. Activation of the nuclear receptor FXR improves hyperglycemia and hyperlipidemia in diabetic mice. Proc. Natl Acad. Sci. USA 103, 1006-1011 (2006).
35. Prawitt, J. et al. Farnesoid X receptor deficiency improves glucose homeostasis in mouse models of obesity. Diabetes 60, 1861-1871 (2011).
36. Watanabe, M. et al. Lowering bile acid pool size with a synthetic farnesoid X receptor (FXR) agonist induces obesity and diabetes through reduced energy expenditure. J. Biol. Chem. 286, 26913-26920 (2011).
37. Samad, F., Hester, K. D., Yang, G., Hannun, Y. A. & Bielawski, J. Altered adipose and plasma sphingolipid metabolism in obesity: a potential mechanism for cardiovascular and metabolic risk. Diabetes 55, 2579-2587 (2006).
38. Gorski, J. Ceramide and insulin resistance: how should the issue be approached? Diabetes 61, 3081-3083 (2012).
39. Bruce, C. R. et al. Overexpression of sphingosine kinase 1 prevents ceramide accumulation and ameliorates muscle insulin resistance in high-fat diet-fed mice. Diabetes 61, 3148-3155 (2012).
40. Sinal, C. J. et al. Targeted disruption of the nuclear receptor FXR/BAR impairs bile acid and lipid homeostasis. Cell 102, 731-744 (2000).
41. Matsubara, T. et al. Lithocholic acid disrupts phospholipid and sphingolipid homeostasis leading to cholestasis in mice. Hepatology 53, 1282-1293 (2011).
42. Schloss, P. D. et al. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75, 7537-7541 (2009).
43. Wang, Q., Garrity, G. M., Tiedje, J. M. & Cole, J. R. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 73, 5261-5267 (2007).
44. Zhang, Y. et al. Abcb11 deficiency induces cholestasis coupled to impaired beta-fatty acid oxidation in mice. J. Biol. Chem. 287, 24784-24794 (2012).
45. Flores, R., Shi, J., Gail, M. H., Ravel, J. & Goedert, J. J. Assessment of the human faecal microbiota: I. Measurement and reproducibility of selected enzymatic activities. Eur. J. Clin. Invest. 42, 848-854 (2012).