The human gut sterolbiome: Bile acid-microbiome endocrine aspects and therapeutics

Acta Pharmaceutica Sinica B

Volumn 5, Issue 2, 2015, Pages 99-105

  Ridlon, Jason M ^a,b   Bajaj, Jasmohan S ^a,b  

^a VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Bile acids; Gut microbiome; Metabolite; Sterolbiome; Therapeutic agent

Indexed keywords

BILE ACID; CELL NUCLEUS RECEPTOR; CHOLESTANETRIOL 26 MONOOXYGENASE; CHOLESTEROL 7ALPHA MONOOXYGENASE; DEOXYCHOLIC ACID; FARNESOID X RECEPTOR; FIBROBLAST GROWTH FACTOR; G PROTEIN COUPLED RECEPTOR; PREGNANE X RECEPTOR; URSODEOXYCHOLIC ACID; VITAMIN D RECEPTOR;

BILE ACID SYNTHESIS; COLON; ENDOCRINE SYSTEM; ENERGY BALANCE; ENTEROHEPATIC CIRCULATION; GENETIC ANALYSIS; GLUCOSE HOMEOSTASIS; HUMAN; HYDROPHILICITY; HYDROPHOBICITY; INTESTINE FLORA; LIPID HOMEOSTASIS; METABOLITE; METAGENOME; MICROBIAL COMMUNITY; MITOCHONDRIAL MEMBRANE; REVIEW;

EID: 84947202455     PISSN: 22113835     EISSN: 22113843     Source Type: Journal    
DOI: 10.1016/j.apsb.2015.01.006     Document Type: Review

References (66)

1. O'Hara A.M., Shanahan F. The gut flora as a forgotten organ. EMBO Rep 2006, 7:688-693.
2. The Human Microbiome Project Consortium Structure, function and diversity of the healthy human microbiome. Nature 2012, 486:207-214.
3. Grice E.A., Segre J.A. The human microbiome: our second genome. Annu Rev Genomics Hum Genet 2012, 13:151-170.
4. The Human Microbiome Project Consortium A framework for human microbiome research. Nature 2012, 486:215-221.
5. Qin J.J., Li R.Q., Raes J., Arumugam M., Burgdorf K.S., Manichanh C., et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature 2009, 464:59-65.
6. Zhou H.P., Hylemon P.B. Bile acids are nutrient signaling hormones. Steroids 2014, 86:62-68.
7. Li T., Chiang J.Y. Bile acid signaling in metabolic disease and drug therapy. Pharmacol Rev 2014, 66:948-983.
8. Evans J.M., Morris L.S., Marchesi J.R. The gut microbiome: the role of a virtual organ in the endocrinology of the host. J Endocrinol 2013, 218:R37-R47.
9. Lyte M., Freestone P. Microbial endocrinology comes of age. Microbe 2009, 4:169-175.
10. Kaji I., Karaki S., Kuwahara A. Short-chain fatty acid receptor and its contribution to glucagon-like peptide-1 release. Digestion 2014, 89:31-36.
11. Bokkenheuser V.D., Winter J. Biotransformation of steroid hormones by gut bacteria. Am J Clin Nutr 1980, 33:2502-2506.
12. Ridlon J.M., Kang D., Hylemon P.B. Bile salt biotransformations by human intestinal bacteria. J Lipid Res 2006, 47:241-259.
13. Chiang J.Y.L. Bile acids: regulation of synthesis. J Lipid Res 2009, 50:1955-1966.
14. Jones S.A. Physiology of FGF15/19. Endocrine FGFs and klothos 2012, 171-182. Springer, US. M. Kuro-o (Ed.).
15. Inagaki T., Choi M., Moschetta A., Peng L., Cummins C.L., McDonald J.G., et al. Fibroblast growth factor 15 functions as an enterohepatic signal to regulate bile acid homeostasis. Cell Metab 2005, 2:217-225.
16. Potthoff M.J., Kliewer S.A., Mangelsdorf D.J. Endocrine fibroblast growth factors 15/19 and 21: from feast to famine. Genes Dev 2012, 26:312-324.
17. Cicione C., Degirolamo C., Moschetta A. Emerging role of fibroblast growth factors 15/19 and 21 as metabolic integrators in the liver. Hepatology 2012, 56:2404-2411.
18. Dikopoulos N., Weidenbach H., Adler G., Schmid R.M. Lipopolysaccharide represses cholesterol 7-α hydroxylase and induces binding activity to the bile acid response element II. Eur J Clin Invest 2003, 33:58-64.
19. Begley M., Gahan C.G.M., Hill C. The interaction between bacteria and bile. FEMS Microbiol Rev 2005, 29:625-651.
20. Jones B.V., Begley M., Hill C., Gahan C.G.M., Marchesi J.R. Functional and comparative metagenomic analysis of bile salt hydrolase activity in the human gut microbiome. Proc Natl Acad Sci USA 2008, 105:13580-13585.
21. Odermatt A., Da Cunha T., Penno C.A., Chandsawangbhuwana C., Reichert C., Wolf A., et al. Hepatic reduction of the secondary bile acid 7-oxolithocholic acid is mediated by 11β-hydroxysteroid dehydrogenase 1. Biochem J 2011, 436:621-629.
22. Hylemon P.B., Melone P.D., Franklund C.V., Lund E., Björkhem I. Mechanism of intestinal 7α-dehydroxylation of cholic acid: evidence that allo-deoxycholic acid is an inducible side-product. J Lipid Res 1991, 32:89-96.
23. Tadano T., Kanoh M., Kondoh H., Matsumoto M., Mimura K., Kanoh Y., et al. Kinetic analysis of bile acids in the feces of colorectal cancer patients by gas chromatography-mass spectrometry (GC-MS). Rinsho Byori 2007, 55:417-427.
24. Britton R.A., Young V.B. Role of the intestinal microbiota in resistance to colonization by Clostridium difficile. Gastroenterology 2014, 146:1547-1553.
25. Buffie C.G., Bucci V., Stein R.R., McKenney P.T., Ling L., Gobourne A., et al. Precision microbiome reconstitution restores bie acid mediated resistance to Clostridium difficile. Nature 2015, 517:205-208.
26. Swann J.R., Want E.J., Geier F.M., Spagou K., Wilson I.D., Sidaway J.E., et al. Systemic gut microbial modulation of bile acid metabolism in host tissue compartments. Proc Natl Acad Sci USA 2011, 108:4523-4530.
27. de Aguiar Vallim T.Q., Tarling E.J., Edwards P.A. Pleiotropic roles of bile acids in metabolism. Cell Metab 2013, 17:657-669.
28. Sayin S.I., Wahlström A., Felin J., Jäntti S., Marschall H.U., Bamberg K., et al. Gut microbiota regulates bile acid metabolism by reducing the levels of tauro-beta-muricholic acid, a naturally occurring FXR antagonist. Cell Metab 2013, 17:225-235.
29. Inagaki T., Moschetta A., Lee Y.K., 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 USA 2006, 103:3920-3925.
30. Makishima M., Lu T.T., Xie W., Whitfield G.K., Domoto H., Evans R.M., et al. Vitamin D receptor as an intestinal bile acid sensor. Science 2002, 296:1313-1316.
31. Kulkarni M.S., Heidepriem P.M., Yielding K.L. Production by lithocholic acid of DNA strand breaks in L1210 cells. Cancer Res 1980, 40:2666-2669.
32. Duboc H., Taché Y., Hofmann A.F. The bile acid TGR5 membrane receptor: from basic research to clinical application. Dig Liver Dis 2014, 46:302-312.
33. Watanabe M., Houten S.M., Mataki C., Christoffolete M.A., Kim B.W., Sato H., et al. Bile acids induce energy expenditure by promoting intracellular thyroid hormone activation. Nature 2006, 439:484-489.
34. Cancer Facts & Figures 2010 2010, American Cancer Society, American Cancer Society, Atlanta.
35. Howlader N, Noone AM, Krapcho M, Garshell J, Neyman N, Altekruse SF, et al. editors. SEER Cancer Statistics Review, 1975-2010, National Cancer Institute. Bethesda, MD. Based on November 2012 SEER data submission, posted to the SEER web site; April 2013.
36. O'Shaughnessy J.A., Kelloff G.J., Gordon G.B., Dannenberg A.J., Hong W.K., Fabian C.J., et al. Treatment and prevention of intraepithelial neoplasia: an important target for accelerated new agent development. Clin Cancer Res 2002, 8:314-346.
37. Parkin D.M., Muir C.S., Whelan S.L., Gao J.T., Ferlay J., Powell J. Cancer incidence in five continents 1997, International Agency for Research on Cancer, Lyons, France.
38. Reddy B.S. Diet and excretion of bile acids. Cancer Res 1981, 41:3766-3768.
39. Reddy B.S., Wynder E.L. Metabolic epidemiology of colon cancer. Fecal bile acids and neutral sterols in colon cancer patients and patients with adenomatous polyps. Cancer 1977, 39:2533-2539.
40. Bayerdörffer E., Mannes G.A., Richter W.O., Ochsenkurhn T., Wiebecke B., Kopcke W., et al. Increased serum deoxycholic acid levels in men with colorectal adenomas. Gastroenterology 1993, 104:145-151.
41. Hylemon P.B., Zhou H., Pandak W.M., Ren S., Gil G., Dent P. Bile acids as regulatory molecules. J Lipid Res 2009, 50:1509-1520.
42. Lamlum H., Papadopoulou A., Ilyas M., Rowan A., Gillet C., Hanby A., et al. APC mutations are sufficient for the growth of early colorectal adenomas. Proc Natl Acad Sci USA 2000, 97:2225-2228.
43. Munemitsu S., Albert I., Souza B., Rubinfeld B., Polakis P. Regulation of intracellular β-catenin levels by the adenomatous polyposis coli (APC) tumor-suppressor protein. Proc Natl Acad Sci USA 1995, 92:3046-3050.
44. Oshima M., Oshima H., Kitagawa K., Kobayashi M., Itakura C., Taketo M. Loss of Apc heterozygosity and abnormal tissue building in nascent intestinal polyps in mice carrying a truncated Apc gene. Proc Natl Acad Sci USA 1995, 92:4482-4486.
45. Brown J.R., DuBois R.N. COX-2: a molecular target for colorectal cancer prevention. J Clin Oncol 2005, 23:2840-2855.
46. δ716 knockout mice by inhibition of cyclooxygenase 2 (COX-2). Cell 1996, 87:803-809.
47. Coffey R., Hawkey C.J., Damstrup L., Graves-Deal R., Daniel V.C., Dempsey P.J., et al. Epidermal growth factor receptor activation induces nuclear targeting of cyclooxygenase-2, basolateral release of prostaglandins, and mitogenesis in polarizing colon cancer cells. Proc Natl Acad Sci USA 1997, 94:657-662.
48. Qiao L., Studer E., Leach K., McKinstry R., Gupta S., Decker R., et al. Deoxycholic acid (DCA) causes ligand-independent activation of epidermal growth factor receptor (EGFR) and FAS receptor in primary hepatocytes: inhibition of EGFR/mitogen-activated protein kinase-signaling module enhances DCA-induced apoptosis. Mol Biol Cell 2001, 12:2629-2645.
49. Lee H.Y., Crawley S., Hokari R., Kwon S., Kim Y.S. Bile acid regulates MUC2 transcription in colon cancer cells via positive EGFR/PKC/Ras/ERK/CREB, PI3K/Akt/IκB/NF-κB and p38/MSK1/CREB pathways and negative JNK/c-Jun/AP-1 pathway. Int J Oncol 2010, 36:941-953.
50. Cheng K., Raufman J.P. Bile acid-induced proliferation of a human colon cancer cell line is mediated by transactivation of epidermal growth factor receptors. Biochem Pharmacol 2005, 70:1035-1047.
51. Pai R., Tarnawski A.S., Tran T. Deoxycholic acid activates β-catenin signaling pathway and increases colon cell cancer growth and invasiveness. Mol Biol Cell 2004, 15:2156-2163.
52. Lee H.K., Jeong S. β-catenin stabilizes cyclooxygenase-2 mRNA by interacting with AU-rich elements of 3'-UTR. Nucleic Acids Res 2006, 34:5705-5714.
53. Rao Y., Stravitz R.T., Vlahcevic Z.R., Gurley E.C., Sando J.J., Hylemon P.B. Activation of protein kinase C α and δ by bile acids: correlation with bile acid structure and diacylglycerol formation. J Lipid Res 1997, 38:2446-2454.
54. Bernstein H., Bernstein C., Payne C.M., Dvorakova K., Garewal H. Bile acids as carcinogens in human gastrointestinal cancers. Mutat Res 2005, 589:47-65.
55. Qiao D., Gaitonde S.V., Qi W., Martinez J.D. Deoxycholic acid suppresses p53 by stimulating proteasome-mediated p53 protein degradation. Carcinogenesis 2001, 22:957-964.
56. Yoshimoto S., Loo T.M., Atarashi K., Kanda H., Sato S., Oyadomari S., et al. Obesity-induced gut microbial metabolite promotes liver cancer through senescence secretome. Nature 2013, 499:97-101.
57. Hofmann A.F., Hagey L.R. Key discoveries in bile acid chemistry and biology and their clinical applications: history of the last eight decades. J Lipid Res 2014, 55:1553-1595.
58. Serfaty L. Chemoprevention of colorectal cancer with ursodeoxycholic acid: pro. Clin Res Hepatol Gastroenterol 2012, 36 Suppl 1:S53-S60.
59. Carey E.J., Lindor K.D. Chemoprevention of colorectal cancer with ursodeoxycholic acid: cons. Clin Res Hepatol Gastroenterol 2012, 36 Suppl 1:S61-S64.
60. Khare S., Mustafi R., Cerda S., Yuan W., Jagadeeswaran S., Dougherty U., et al. Ursodeoxycholic acid suppresses COX-2 expression in colon cancer: roles of Ras, p38, and CCAAT/enhancer-binding protein. Nutr Cancer 2008, 60:389-400.
61. Macdonald I.A., White B.A., Hylemon P.B. Separation of 7α- and 7β-hydroxysteroid dehydrogenase activities from Clostridium absonum ATCC# 27555 and cellular response of this organism to bile acid inducers. J Lipid Res 1983, 24:1119-1126.
62. Baron S.F., Franklund C.V., Hylemon P.B. Cloning, sequencing, and expression of the gene coding for bile acid 7 alpha-hydroxysteroid dehydrogenase from Eubacterium sp. strain VPI 12708. J Bacteriol 1991, 173:4558-4569.
63. Dawson J.A., Mallonee D.H., Bjorkhem I., Hylemon P.B. Expression and characterization of a C24 bile acid 7α-dehydratase from Eubacterium sp. strain VPI 12708 in Escherichia coli. J Lipid Res 1996, 37:1258-1267.
64. White B.A., Lipsky R.L., Fricke R.J., Hylemon P.B. Bile acid induction specificity of 7α-dehydroxylase activity in an intestinal Eubacterium species. Steroids 1980, 35:103-109.
65. 4-cholenoic acid oxidoreductases. Biochim Biophys Acta 2008, 1781:16-25.
66. Lee J.Y., Arai H., Nakamura Y., Fukiya S., Wada M., Yokota A. Contribution of the 7β-hydroxysteroid dehydrogenase from Ruminococcus gnavus N53 to ursodeoxycholic acid formation in the human colon. J Lipid Res 2013, 54:3062-3069.