Modulation of the intestinal bile acid/farnesoid X receptor/fibroblast growth factor 15 axis improves alcoholic liver disease in mice

Hepatology

Volumn 67, Issue 6, 2018, Pages 2150-2166

  Hartmann, Phillipp ^a,b   Hochrath, Katrin ^a   Horvath, Angela ^a,c   Chen, Peng ^a   Seebauer, Caroline T ^a   Llorente, Cristina ^a,d   Wang, Lirui ^a,d   Alnouti, Yazen ^e   Fouts, Derrick E ^f   Stärkel, Peter ^g   Loomba, Rohit ^a   Coulter, Sally ^h   Liddle, Christopher ^h   Yu, Ruth T ⁱ   Ling, Lei ^j   Rossi, Stephen J ^j   DePaoli, Alex M ^j   Downes, Michael ⁱ   Evans, Ronald M ^i,k   Brenner, David A ^a   Schnabl, Bernd ^a,d   more..

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c MEDICAL UNIVERSITY OF GRAZ   (Austria)

^d VA SAN DIEGO HEALTHCARE SYSTEM   (United States)

^e UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^f J CRAIG VENTER INSTITUTE   (United States)

^g CLINIQUES UNIVERSITAIRES SAINT LUC   (Belgium)

^h UNIVERSITY OF SYDNEY   (Australia)

ⁱ SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^j NGM Bio   (United States)

^k HOWARD HUGHES MEDICAL INSTITUTE   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 3; ANTIBIOTIC AGENT; BILE ACID; CARNITINE; CHOLESTEROL 7ALPHA MONOOXYGENASE; CHOLIC ACID; DEOXYCHOLIC ACID; FARNESOID X RECEPTOR; FATTY ACID BINDING PROTEIN 2; FATTY ACID BINDING PROTEIN 5; FATTY ACID SYNTHASE; FIBROBLAST GROWTH FACTOR; FIBROBLAST GROWTH FACTOR 15; GENOMIC DNA; LIPID; LIPOPROTEIN LIPASE; MESSENGER RNA; MURICHOLIC ACID; NUCLEAR RECEPTOR NR1D1; PALMITOYL COENZYME A HYDROLASE; PYRUVATE DEHYDROGENASE KINASE 4; RETINOID RELATED ORPHAN RECEPTOR GAMMA; TAUROCHOLIC ACID; TAURODEOXYCHOLIC ACID; TAUROMURICHOLIC ACID; TUBULIN; UNCLASSIFIED DRUG; ALCOHOL; CELL RECEPTOR; FARNESOID X-ACTIVATED RECEPTOR; FIBROBLAST GROWTH FACTOR 15, MOUSE;

ALCOHOL LIVER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BILE ACID METABOLISM; BILE ACID SYNTHESIS; CONTROLLED STUDY; ENTEROHEPATIC CIRCULATION; INTESTINE; INTESTINE CELL; INTESTINE FLORA; LIPID METABOLISM; METAGENOMICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN SECRETION; RNA SEQUENCE; ANIMAL; C57BL MOUSE; METABOLISM; MICROBIOLOGY; PHYSIOLOGY;

ANIMALS; BILE ACIDS AND SALTS; ETHANOL; FIBROBLAST GROWTH FACTORS; GASTROINTESTINAL MICROBIOME; INTESTINES; LIVER DISEASES, ALCOHOLIC; MICE; MICE, INBRED C57BL; RECEPTORS, CYTOPLASMIC AND NUCLEAR;

EID: 85045415551     PISSN: 02709139     EISSN: 15273350     Source Type: Journal    
DOI: 10.1002/hep.29676     Document Type: Article

References (50)

1. WHO. Global Status Report on Alcohol and Health. Geneva, Switzerland: WHO; 2014.
2. Bull-Otterson L, Feng W, Kirpich I, Wang Y, Qin X, Liu Y, et al. Metagenomic analyses of alcohol induced pathogenic alterations in the intestinal microbiome and the effect of Lactobacillus rhamnosus GG treatment. PLoS One 2013;8:e53028.
3. Yan AW, Fouts DE, Brandl J, Stärkel P, Torralba M, Schott E, et al. Enteric dysbiosis associated with a mouse model of alcoholic liver disease. Hepatology 2011;53:96-105.
4. Mutlu E, Keshavarzian A, Engen P, Forsyth CB, Sikaroodi M, Gillevet P. Intestinal dysbiosis: a possible mechanism of alcohol-induced endotoxemia and alcoholic steatohepatitis in rats. Alcohol Clin Exp Res 2009;33:1836-1846.
5. Mutlu EA, Gillevet PM, Rangwala H, Sikaroodi M, Naqvi A, Engen PA, et al. Colonic microbiome is altered in alcoholism. Am J Physiol Gastrointest Liver Physiol 2012;302:G966-G978.
6. Leclercq S, Matamoros S, Cani PD, Neyrinck AM, Jamar F, Starkel P, et al. Intestinal permeability, gut-bacterial dysbiosis, and behavioral markers of alcohol-dependence severity. Proc Natl Acad Sci U S A 2014;111:E4485-E4493.
7. Bode JC, Bode C, Heidelbach R, Durr HK, Martini GA. Jejunal microflora in patients with chronic alcohol abuse. Hepatogastroenterology 1984;31:30-34.
8. Chen P, Stärkel P, Turner JR, Ho SB, Schnabl B. Dysbiosis-induced intestinal inflammation activates TNFRI and mediates alcoholic liver disease in mice. Hepatology 2015;61:883-894.
9. Parlesak A, Schafer C, Schutz T, Bode JC, Bode C. Increased intestinal permeability to macromolecules and endotoxemia in patients with chronic alcohol abuse in different stages of alcohol-induced liver disease. J Hepatol 2000;32:742-747.
10. Petrasek J, Bala S, Csak T, Lippai D, Kodys K, Menashy V, et al. IL-1 receptor antagonist ameliorates inflammasome-dependent alcoholic steatohepatitis in mice. J Clin Invest 2012;122:3476-3489.
11. Petrasek J, Iracheta-Vellve A, Csak T, Satishchandran A, Kodys K, Kurt-Jones EA, et al. STING-IRF3 pathway links endoplasmic reticulum stress with hepatocyte apoptosis in early alcoholic liver disease. Proc Natl Acad Sci U S A 2013;110:16544-16549.
12. Chen P, Torralba M, Tan J, Embree M, Zengler K, Stärkel P, et al. Supplementation of saturated long-chain fatty acids maintains intestinal eubiosis and reduces ethanol-induced liver injury in mice. Gastroenterology 2015;148:203-214.
13. Dawson PA, Karpen SJ. Intestinal transport and metabolism of bile acids. J Lipid Res 2015;56:1085-1099.
14. Schaap FG, Trauner M, Jansen PL. Bile acid receptors as targets for drug development. Nat Rev Gastroenterol Hepatol 2014;11:55-67.
15. Ridlon JM, Kang DJ, Hylemon PB. Bile salt biotransformations by human intestinal bacteria. J Lipid Res 2006;47:241-259.
16. Tomlinson E, Fu L, John L, Hultgren B, Huang X, Renz M, et al. Transgenic mice expressing human fibroblast growth factor-19 display increased metabolic rate and decreased adiposity. Endocrinology 2002;143:1741-1747.
17. Swann JR, Want EJ, Geier FM, Spagou K, Wilson ID, Sidaway JE, et al. Systemic gut microbial modulation of bile acid metabolism in host tissue compartments. Proc Natl Acad Sci U S A 2011;108(Suppl 1):4523-4530.
18. Kakiyama G, Hylemon PB, Zhou H, Pandak WM, Heuman DM, Kang DJ, et al. Colonic inflammation and secondary bile acids in alcoholic cirrhosis. Am J Physiol Gastrointest Liver Physiol 2014;306:G929-G937.
19. Nicolaou KC, Evans RM, Roecker AJ, Hughes R, Downes M, Pfefferkorn JA. Discovery and optimization of non-steroidal FXR agonists from natural product-like libraries. Org Biomol Chem 2003;1:908-920.
20. Meyer F, Paarmann D, D'Souza M, Olson R, Glass EM, Kubal M, et al. The metagenomics RAST server—a public resource for the automatic phylogenetic and functional analysis of metagenomes. BMC Bioinformatics 2008;9:386.
21. Alnouti Y, Csanaky IL, Klaassen CD. Quantitative-profiling of bile acids and their conjugates in mouse liver, bile, plasma, and urine using LC-MS/MS. J Chromatogr B Analyt Technol Biomed Life Sci 2008;873:209-217.
22. Huang J, Bathena SP, Csanaky IL, Alnouti Y. Simultaneous characterization of bile acids and their sulfate metabolites in mouse liver, plasma, bile, and urine using LC-MS/MS. J Pharm Biomed Anal 2011;55:1111-1119.
23. Wang L, Hartmann P, Haimerl M, Bathena SP, Sjowall C, Almer S, et al. Nod2 deficiency protects mice from cholestatic liver disease by increasing renal excretion of bile acids. J Hepatol 2014;60:1259-1267.
24. Fang S, Suh JM, Reilly SM, Yu E, Osborn O, Lackey D, et al. Intestinal FXR agonism promotes adipose tissue browning and reduces obesity and insulin resistance. Nat Med 2015;21:159-165.
25. Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 2013;29:15-21.
26. Trapnell C, Hendrickson DG, Sauvageau M, Goff L, Rinn JL, Pachter L. Differential analysis of gene regulation at transcript resolution with RNA-seq. Nat Biotechnol 2013;31:46-53.
27. Roberts A, Pimentel H, Trapnell C, Pachter L. Identification of novel transcripts in annotated genomes using RNA-Seq. Bioinformatics 2011;27:2325-2329.
28. Jones BV, Begley M, Hill C, Gahan CG, Marchesi JR. Functional and comparative metagenomic analysis of bile salt hydrolase activity in the human gut microbiome. Proc Natl Acad Sci U S A 2008;105:13580-13585.
29. Inagaki T, Moschetta A, Lee YK, Peng L, Zhao G, Downes M, et al. Regulation of antibacterial defense in the small intestine by the nuclear bile acid receptor. Proc Natl Acad Sci U S A 2006;103:3920-3925.
30. Jiang C, Xie C, Li F, Zhang L, Nichols RG, Krausz KW, et al. Intestinal farnesoid X receptor signaling promotes nonalcoholic fatty liver disease. J Clin Invest 2015;125:386-402.
31. Inagaki T, Choi M, Moschetta A, Peng L, Cummins CL, McDonald JG, et al. Fibroblast growth factor 15 functions as an enterohepatic signal to regulate bile acid homeostasis. Cell Metab 2005;2:217-225.
32. Studer E, Zhou X, Zhao R, Wang Y, Takabe K, Nagahashi M, et al. Conjugated bile acids activate the sphingosine-1-phosphate receptor 2 in primary rodent hepatocytes. Hepatology 2012;55:267-276.
33. Arroyo V, Moreau R, Kamath PS, Jalan R, Gines P, Nevens F, et al. Acute-on-chronic liver failure in cirrhosis. Nat Rev Dis Primers 2016;2:16041.
34. Song P, Zhang Y, Klaassen CD. Dose-response of five bile acids on serum and liver bile Acid concentrations and hepatotoxicty in mice. Toxicol Sci 2011;123:359-367.
35. Delzenne NM, Calderon PB, Taper HS, Roberfroid MB. Comparative hepatotoxicity of cholic acid, deoxycholic acid and lithocholic acid in the rat: in vivo and in vitro studies. Toxicol Lett 1992;61:291-304.
36. Betrapally NS, Gillevet PM, Bajaj JS. Changes in the intestinal microbiome and alcoholic and nonalcoholic liver diseases: causes or effects? Gastroenterology 2016;150:1745-1755.e3.
37. Massey VL, Beier JI, Ritzenthaler JD, Roman J, Arteel GE. Potential role of the gut/liver/lung axis in alcohol-induced tissue pathology. Biomolecules 2015;5:2477-2503.
38. Bajaj JS, Kakiyama G, Zhao D, Takei H, Fagan A, Hylemon P, et al. Continued alcohol misuse in human cirrhosis is associated with an impaired gut-liver axis. Alcohol Clin Exp Res 2017 Sep 19. doi: 10.1111/acer.13498. [Epub ahead of print]
39. Kang DJ, Hylemon PB, Gillevet PM, Sartor RB, Betrapally NS, Kakiyama G, et al. Gut microbial composition can differentially regulate bile acid synthesis in humanized mice. Hepatol Commun 2017;1:61-70.
40. Bode C, Kolepke R, Schafer K, Bode JC. Breath hydrogen excretion in patients with alcoholic liver disease—evidence of small intestinal bacterial overgrowth. Z Gastroenterol 1993;31:3-7.
41. Adachi Y, Moore LE, Bradford BU, Gao W, Thurman RG. Antibiotics prevent liver injury in rats following long-term exposure to ethanol. Gastroenterology 1995;108:218-224.
42. Lowe PP, Gyongyosi B, Satishchandran A, Iracheta-Vellve A, Ambade A, Kodys K, et al. Alcohol-related changes in the intestinal microbiome influence neutrophil infiltration, inflammation and steatosis in early alcoholic hepatitis in mice. PLoS One 2017;12:e0174544.
43. Bode C, Schafer C, Fukui H, Bode JC. Effect of treatment with paromomycin on endotoxemia in patients with alcoholic liver disease—a double-blind, placebo-controlled trial. Alcohol Clin Exp Res 1997;21:1367-1373.
44. Li F, Jiang C, Krausz KW, Li Y, Albert I, Hao H, et al. Microbiome remodelling leads to inhibition of intestinal farnesoid X receptor signalling and decreased obesity. Nat Commun 2013;4:2384.
45. Jiang C, Xie C, Lv Y, Li J, Krausz KW, Shi J, et al. Intestine-selective farnesoid X receptor inhibition improves obesity-related metabolic dysfunction. Nat Commun 2015;6:10166.
46. Wu W, Zhu B, Peng X, Zhou M, Jia D, Gu J. Activation of farnesoid X receptor attenuates hepatic injury in a murine model of alcoholic liver disease. Biochem Biophys Res Commun 2014;443:68-73.
47. Manley S, Ni HM, Williams JA, Kong B, DiTacchio L, Guo G, Ding WX. Farnesoid X receptor regulates forkhead Box O3a activation in ethanol-induced autophagy and hepatotoxicity. Redox Biol 2014;2:991-1002.
48. Lu Y, Zhuge J, Wang X, Bai J, Cederbaum AI. Cytochrome P450 2E1 contributes to ethanol-induced fatty liver in mice. Hepatology 2008;47:1483-1494.
49. Hu X, Jogasuria A, Wang J, Kim C, Han Y, Shen H, et al. MitoNEET deficiency alleviates experimental alcoholic steatohepatitis in mice by stimulating endocrine adiponectin-Fgf15 axis. J Biol Chem 2016;291:22482-22495.
50. Neuschwander-Tetri BA, Loomba R, Sanyal AJ, Lavine JE, Van Natta ML, Abdelmalek MF, et al. Farnesoid X nuclear receptor ligand obeticholic acid for non-cirrhotic, non-alcoholic steatohepatitis (FLINT): a multicentre, randomised, placebo-controlled trial. Lancet 2015;385:956-965.