10,274
Views
103
CrossRef citations to date
0
Altmetric
Research Paper/Report

The microbiome modulating activity of bile acids

ORCID Icon, , ORCID Icon, , ORCID Icon, , ORCID Icon, , & ORCID Icon show all
Pages 979-996 | Received 25 Oct 2019, Accepted 13 Feb 2020, Published online: 05 Mar 2020

References

  • Wahlstrom A, Sayin SI, Marschall HU, Backhed F. Intestinal crosstalk between bile acids and microbiota and its impact on host metabolism. Cell Metab. 2016;24:41–50. doi:10.1016/j.cmet.2016.05.005.
  • Urdaneta V, Casadesus J. Interactions between bacteria and bile salts in the gastrointestinal and hepatobiliary tracts. Front Med. 2017;4:163.
  • Ma C, Han MJ, Heinrich B, Fu Q, Zhang QF, Sandhu M, Agdashian D, Terabe M, Berzofsky JA, Fako V, et al. Gut microbiome-mediated bile acid metabolism regulates liver cancer via NKT cells. Science. 2018;360:eaan5931.
  • Tian Y, Cai J, Gui W, Nichols RG, Koo I, Zhang J, Anitha M, Patterson AD. Berberine directly affects the gut microbiota to promote intestinal farnesoid X receptor activation. Drug Metab Dispos. 2019;47:86–93. doi:10.1124/dmd.118.083691.
  • Begley M, Hill C, Gahan CGM. Bile salt hydrolase activity in probiotics. App Environ Microb. 2006;72:1729–1738. doi:10.1128/AEM.72.3.1729-1738.2006.
  • Li F, Jiang CT, Krausz KW, Li YF, Albert I, Hao HP, Fabre KM, Mitchell JB, Patterson AD, Gonzalez FJ. Microbiome remodelling leads to inhibition of intestinal farnesoid X receptor signalling and decreased obesity. Nat Commun. 2013;4:1–10.
  • Ridlon JM, Harris SC, Bhowmik S, Kang DJ, Hylemon PB. Consequences of bile salt biotransformations by intestinal bacteria. Gut Microbes. 2016;7:22–39. doi:10.1080/19490976.2015.1127483.
  • Lorenzo-Zuniga V, Bartoli R, Planas R, Hofmann AF, Vinado B, Hagey LR, Hernández JM, Mañé J, Alvarez MA, Ausina V, et al. Oral bile acids reduce bacterial overgrowth, bacterial translocation, and endotoxemia in cirrhotic rats. Hepatology. 2003;37:551–557. doi:10.1053/jhep.2003.50116.
  • Inagaki T, Moschetta A, Lee YK, Peng L, Zhao GX, Downes M, Yu RT, Shelton JM, Richardson JA, Repa JJ, et al. Regulation of antibacterial defense in the small intestine by the nuclear bile acid receptor. P Natl Acad Sci USA. 2006;103:3920–3925. doi:10.1073/pnas.0509592103.
  • Makishima M, Okamoto AY, Repa JJ, Tu H, Learned RM, Luk A, Hull MV, Lustig KD, Mangelsdorf DJ, Shan B. Identification of a nuclear receptor for bile acids. Science. 1999;284:1362–1365. doi:10.1126/science.284.5418.1362.
  • Parks DJ, Blanchard SG, Bledsoe RK, Chandra G, Consler TG, Kliewer SA, Stimmel JB, Willson TM, Zavacki AM, Moore DD, et al. Bile acids: natural ligands for an orphan nuclear receptor. Science. 1999;284:1365–1368. doi:10.1126/science.284.5418.1365.
  • Wang HB, Chen J, Hollister K, Sowers LC, Forman BM. Endogenous bile acids are ligands for the nuclear receptor FXR BAR. Mol Cell. 1999;3:543–553. doi:10.1016/S1097-2765(00)80348-2.
  • Binder HJ, Filburn B, Floch M. Bile-acid inhibition of intestinal anaerobic organisms. Am J Clin Nutr. 1975;28:119–125. doi:10.1093/ajcn/28.2.119.
  • Kishinaka M, Umeda A, Kuroki S. High-concentrations of conjugated bile-acids inhibit bacterial growth of Clostridium perferingens and induce its extracellular cholyglycine hydrolase. Steroids. 1994;59:485–489. doi:10.1016/0039-128X(94)90062-0.
  • Kurdi P, Kawanishi K, Mizutani K, Yokota A. Mechanism of growth inhibition by free bile acids in Lactobacilli and Bifidobacteria. J Bacteriol. 2006;188:1979–1986. doi:10.1128/JB.188.5.1979-1986.2006.
  • Sung JY, Shaffer EA, Costerton JW. Antibacterial activity of bile salts against common biliary pathogens-effects of hydrophobicity of the molecule and in the presence of phospholipids. Digest Dis Sci. 1993;38:2104–2112. doi:10.1007/BF01297092.
  • Marion S, Studer N, Desharnais L, Menin L, Escrig S, Meibom A, Hapfelmeier S, Bernier-Latmani R. In vitro and in vivo characterization of Clostridium scindens bile acid transformations. Gut Microbes. 2019;10:481–503. doi:10.1080/19490976.2018.1549420.
  • Kang JD, Myers CJ, Harris SC, Kakiyama G, Lee IK, Yun BS, Matsuzaki K, Furukawa M, Min HK, Bajaj JS, et al. Bile acid 7 alpha-dehydroxylating gut bacteria secrete antibiotics that inhibit clostridium difficile: role of secondary bile acids. Cell Chem Biol. 2019;26:27–34. doi:10.1016/j.chembiol.2018.10.003.
  • Ridlon JM, Devendran S, Alves JM, Doden H, Wolf PG, Pereira GV, Ly L, Volland A, Takei H, Nittono H, et al. The ‘in vivo lifestyle’ of bile acid 7α-dehydroxylating bacteria: comparative genomics, metatranscriptomic, and bile acid metabolomics analysis of a defined microbial community in gnotobiotic mice. Gut Microbes. 2019;9:1–24. doi:10.1080/19490976.2019.1618173.
  • Perez MJ, Briz O. Bile-acid-induced cell injury and protection. World J Gastroentero. 2009;15:1677–1689. doi:10.3748/wjg.15.1677.
  • Ruiz L, Margolles A, Sanchez B. Bile resistance mechanisms in Lactobacillus and Bifidobacterium. Front Microbiol. 2013;4:396.
  • Hyronimus B, Le Marrec C, Sassi AH, Deschamps A. Acid and bile tolerance of spore-forming lactic acid bacteria. Int J Food Microbiol. 2000;61:193–197. doi:10.1016/S0168-1605(00)00366-4.
  • Sun LL, Xie C, Wang G, Wu Y, Wu Q, Wang XM, Liu J, Deng Y, Xia J, Chen B, et al. Gut microbiota and intestinal FXR mediate the clinical benefits of metformin. Nat Med. 2018;24:1919–1929. doi:10.1038/s41591-018-0222-4.
  • Ze XL, Duncan SH, Louis P, Flint HJ. Ruminococcus bromii is a keystone species for the degradation of resistant starch in the human colon. Isme J. 2012;6:1535–1543. doi:10.1038/ismej.2012.4.
  • Staudinger JL, Goodwin B, Jones SA, Hawkins-Brown D, MacKenzie KI, Latour A, Liu Y, Klaassen CD, Brown KK, Reinhard J, et al. The nuclear receptor PXR is a lithocholic acid sensor that protects against liver toxicity. P Natl Acad Sci USA. 2001;98:3369–3374. doi:10.1073/pnas.051551698.
  • Ridlon JM, Bajaj JS. The human gut sterolbiome: bile acid-microbiome endocrine aspects and therapeutics. Acta Pharm Sin B. 2015;5:99–105. doi:10.1016/j.apsb.2015.01.006.
  • Trabelsi MS, Daoudi M, Prawitt J, Ducastel S, Touche V, Sayin SI, Perino A, Brighton CA, Sebti Y, Kluza J, Briand O, et al. Farnesoid X receptor inhibits glucagon-like peptide-1 production by enteroendocrine L cells. Nat Commun. 2015;6:7629.
  • Chiang JYL. Bile acid metabolism and signaling. Compr Physiol. 2013;3:1191–1212.
  • Attili AF, Angelico M, Cantafora A, Alvaro D, Capocaccia L. Bile acid-induced liver toxicity-relation to the hydrophobichydrophilic balance of bile acids. Med Hypotheses. 1986;19:57–69. doi:10.1016/0306-9877(86)90137-4.
  • 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. doi:10.1016/0378-4274(92)90156-E.
  • Tsuda H, Masui T, Imaida K, Fukushima S, Ito N. Promotive effect of primary and secondary bile acids on the induction of Gamma-glutamyl-transferase transpeptidase-positive liver-cell foci as a possible endogenous factor for hepatocarcinogensis in rats. Gann. 1984;75:871–875.
  • Hofmann AF. Detoxification of lithocholic acid, a toxic bile acid: relevance to drug hepatotoxicity. Drug Metab Rev. 2004;36:703–722. doi:10.1081/DMR-200033475.
  • Carey JB, Williams G. Metabolism of lithocholic acid in bile fistula patients. J Clin Invest. 1963;42:450-&. doi:10.1172/JCI104733.
  • Sannasiddappa TH, Lund PA, Clarke SR. In Vitro antibacterial activity of unconjugated and conjugated bile salts on staphylococcus aureus. Front Microbiol. 2017;8:1581.
  • Hofmann AF. The continuing importance of bile acids in liver and intestinal disease. Arch Intern Med. 1999;159:2647–2658. doi:10.1001/archinte.159.22.2647.
  • Bustos AY, de Valdez GF, Fadda S, Taranto MP. New insights into bacterial bile resistance mechanisms: the role of bile salt hydrolase and its impact on human health. Food Res Int. 2018;112:250–262. doi:10.1016/j.foodres.2018.06.035.
  • Begley M, Gahan CGM, Hill C. The interaction between bacteria and bile. FEMS Microbiol Rev. 2005;29:625–651. doi:10.1016/j.femsre.2004.09.003.
  • Miller SI. Antibiotic resistance and regulation of the gram-negative bacterial outer membrane barrier by host innate immune molecules. Mbio. 2016;7:e01541–16.
  • Sanchez B, Champomier-Verges MC, Stuer-Lauridsen B, Ruas-Madiedo P, Anglade P, Baraige F, de Los Reyes-gavilan CG, Johansen E, Zagorec M, Margolles A, et al. Adaptation and response of Bifidobacterium animalis subsp lactis to bile: a proteomic and physiological approach. Appl Environ Microbiol. 2007;73:6757–6767. doi:10.1128/AEM.00637-07.
  • Maier L, Pruteanu M, Kuhn M, Zeller G, Telzerow A, Anderson EE, Brochado AR, Fernandez KC, Dose H, Mori H, et al. Extensive impact of non-antibiotic drugs on human gut bacteria. Nature. 2018;555:623-+. doi:10.1038/nature25979.
  • Tian Y, Nichols RG, Cai JW, Patterson AD, Cantorna MT. Vitamin A deficiency in mice alters host and gut microbial metabolism leading to altered energy homeostasis. J Nutr Biochem. 2018;54:28–34. doi:10.1016/j.jnutbio.2017.10.011.
  • Maurice CF, Turnbaugh PJ. Quantifying and identifying the active and damaged subsets of indigenous microbial communities. In: DeLong EF, editor. Microbial metagenomics, metatranscriptomics, and metaproteomics. Methods in Enzymology. 2013. p. 91–107.
  • Cai JW, Nichols RG, Koo I, Kalikow ZA, Zhang LM, Tian Y, Zhang J, Smith PB, Patterson AD. multiplatform physiologic and metabolic phenotyping reveals microbial toxicity. Msystems. 2018;3:e00123–18.
  • Maurice CF, Haiser HJ, Turnbaugh PJ. Xenobiotics shape the physiology and gene expression of the active human gut microbiome. Cell. 2013;152:39–50. doi:10.1016/j.cell.2012.10.052.
  • Sarafian MH, Lewis MR, Pechlivanis A, Ralphs S, McPhail MJW, Patel VC, Dumas M-E, Holmes E, Nicholson JK. Bile acid profiling and quantification in biofluids using ultra-performance liquid chromatography tandem mass spectrometry. Anal Chem. 2015;87:9662–9670. doi:10.1021/acs.analchem.5b01556.
  • Kolek J, Branska B, Drahokoupil M, Patakova P, Melzoch K. Evaluation of viability, metabolic activity and spore quantity in clostridial cultures during ABE fermentation. FEMS Microbiol Rev. 2016;363: 1–7.
  • Shi XH, Xiao CN, Wang YL, Tang HR. Gallic acid intake induces alterations to systems metabolism in rats. J Proteome Re. 2013;12:991–1006. doi:10.1021/pr301041k.
  • Tian Y, Zhang LM, Wang YL, Tang HR. Age-related topographical metabolic signatures for the rat gastrointestinal contents. J Proteome Res. 2012;11:1397–1411. doi:10.1021/pr2011507.
  • Fang H, Gough J. supraHex: an R/Bioconductor package for tabular omics data analysis using a supra-hexagonal map. Biochem Bioph Res Comm. 2014;443:285–289. doi:10.1016/j.bbrc.2013.11.103.
  • Allman EL, Painter HJ, Samra J, Carrasquilla M, Llinas M. metabolomic profiling of the malaria box reveals antimalarial target pathways. Antimicrob Agents Chemother. 2016;60:6635–6649. doi:10.1128/AAC.01224-16.
  • Tsugawa H, Cajka T, Kind T, Ma Y, Higgins B, Ikeda K, Kanazawa M, VanderGheynst J, Fiehn O, Arita M, et al. MS-DIAL: data-independent MS/MS deconvolution for comprehensive metabolome analysis. Nat Methods. 2015;12:523-+. doi:10.1038/nmeth.3393.
  • Barupal DK, Haldiya PK, Wohlgemuth G, Kind T, Kothari SL, Pinkerton KE, Fiehn O. MetaMapp: mapping and visualizing metabolomic data by integrating information from biochemical pathways and chemical and mass spectral similarity. BMC Bioinf. 2012;13:99.
  • Hartman AL, Lough DM, Barupal DK, Fiehn O, Fishbein T, Zasloff M, Eisen JA. Human gut microbiome adopts an alternative state following small bowel transplantation. P Natl Acad Sci USA. 2009;106:17187–17192. doi:10.1073/pnas.0904847106.
  • Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T. Cytoscape: A software environment for integrated models of biomolecular interaction networks. Genome Res. 2003;13:2498–2504. doi:10.1101/gr.1239303.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.