Altered enterohepatic circulation of bile acids in Crohn's disease and their clinical significance: A new perspective

Expert Review of Gastroenterology and Hepatology

Volumn 7, Issue 1, 2013, Pages 49-56

  Nolan, Jonathan D ^a   Johnston, Ian M ^a   Walters, Julian R F ^a  

^a HAMMERSMITH HOSPITAL   (United Kingdom)

Author keywords

bile acid malabsorption; bile acids; Crohn's disease; FGF19; FXR; FXR agonists

Indexed keywords

3 [2 [2 CHLORO 4 [3 (2,6 DICHLOROPHENYL) 5 ISOPROPYL 4 ISOXAZOLYLMETHOXY]PHENYL]VINYL]BENZOIC ACID; BILE ACID; BUDESONIDE; CHENODEOXYCHOLIC ACID; CYTOKINE; FARNESOID X RECEPTOR; FIBROBLAST GROWTH FACTOR 19; FIBROBLAST GROWTH FACTOR 4; INTERLEUKIN 1BETA; OBETICHOLIC ACID; TUMOR NECROSIS FACTOR ALPHA; URSODEOXYCHOLIC ACID;

ANTIINFLAMMATORY ACTIVITY; BILE ACID SYNTHESIS; COLITIS; CROHN DISEASE; CYTOKINE PRODUCTION; ENTEROHEPATIC CIRCULATION; ENZYME INHIBITION; HUMAN; ILEUM RESECTION; INTESTINE FUNCTION; MALABSORPTION; NONHUMAN; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; ANTI-INFLAMMATORY AGENTS; BILE ACIDS AND SALTS; CROHN DISEASE; CYTOKINES; DRUG DESIGN; ENTEROHEPATIC CIRCULATION; FIBROBLAST GROWTH FACTORS; GASTROINTESTINAL AGENTS; HUMANS; INFLAMMATION MEDIATORS; INTESTINAL ABSORPTION; INTESTINES; LIGANDS; LIVER; RECEPTORS, CYTOPLASMIC AND NUCLEAR; SIGNAL TRANSDUCTION;

EID: 84871550471     PISSN: 17474124     EISSN: 17474132     Source Type: Journal    
DOI: 10.1586/egh.12.66     Document Type: Review

References (57)

1. Lack L, Weiner IM. In vitro absorption of bile salts by small intestine of rats and guinea pigs. Am. J. Physiol. 200, 313-317 (1961).
2. Wong MH, Oelkers P, Craddock AL, Dawson PA. Expression cloning and characterization of the hamster ileal sodium-dependent bile acid transporter. J. Biol. Chem. 269(2), 1340-1347 (1994).
3. Krag E, Phillips SF. Active and passive bile acid absorption in man. Perfusion studies of the ileum and jejunum. J. Clin. Invest. 53(6), 1686-1694 (1974).
4. Shefer S, Hauser S, Bekersky I, Mosbach EH. Feedback regulation of bile acid biosynthesis in the rat. J. Lipid Res. 10(6), 646-655 (1969).
5. Dueland S, Reichen J, Everson GT, Davis RA. Regulation of cholesterol and bile acid homoeostasis in bile-obstructed rats. Biochem. J. 280(Pt 2), 373-377 (1991).
6. Pandak WM, Heuman DM, Hylemon PB, Chiang JY, Vlahcevic ZR. Failure of intravenous infusion of taurocholate to down-regulate cholesterol 7α-hydroxylase in rats with biliary fistulas. Gastroenterology 108(2), 533-544 (1995).
7. Inagaki T, Choi M, Moschetta A et al. Fibroblast growth factor 15 functions as an enterohepatic signal to regulate bile acid homeostasis. Cell Metab. 2(4), 217-225 (2005).
8. Spiller RC, Trotman IF, Higgins BE et al. The ileal brake-inhibition of jejunal motility after ileal fat perfusion in man. Gut 25(4), 365-374 (1984).
9. Wen J, Phillips SF, Sarr MG, Kost LJ, Holst JJ. PYY and GLP-1 contribute to feedback inhibition from the canine ileum and colon. Am. J. Physiol. 269(6 Pt 1), G945-G952 (1995).
10. Song KH, Li T, Owsley E, Strom S, Chiang JY. Bile acids activate fibroblast growth factor 19 signaling in human hepatocytes to inhibit cholesterol 7alpha-hydroxylase gene expression. Hepatology 49(1), 297-305 (2009).
11. Parks DJ, Blanchard SG, Bledsoe RK et al. Bile acids: natural ligands for an orphan nuclear receptor. Science 284(5418), 1365-1368 (1999).
12. Inagaki T, Moschetta A, Lee YK et al. Regulation of antibacterial defense in the small intestine by the nuclear bile acid receptor. Proc. Natl Acad. Sci. USA 103(10), 3920-3925 (2006).
13. Fon Tacer K, Bookout AL, Ding X et al. Research resource: comprehensive expression atlas of the fibroblast growth factor system in adult mouse. Mol. Endocrinol. 24(10), 2050-2064 (2010).
14. Zhou J, Hegsted M, McCutcheon KL et al. Peptide YY and proglucagon mRNA expression patterns and regulation in the gut. Obesity (Silver Spring) 14(4), 683-689 (2006).
15. Goodwin B, Jones SA, Price RR et al. A regulatory cascade of the nuclear receptors FXR, SHP-1, and LRH-1 represses bile acid biosynthesis. Mol. Cell 6(3), 517-526 (2000).
16. Kim I, Ahn SH, Inagaki T et al. Differential regulation of bile acid homeostasis by the farnesoid X receptor in liver and intestine. J. Lipid Res. 48(12), 2664-2672 (2007).
17. Ananthanarayanan M, Balasubramanian N, Makishima M, Mangelsdorf DJ, Suchy FJ. Human bile salt export pump promoter is transactivated by the farnesoid X receptor/bile acid receptor. J. Biol. Chem. 276(31), 28857-28865 (2001).
18. Brydon WG, Nyhlin H, Eastwood MA, Merrick MV. Serum 7α-hydroxy-4- cholesten-3-one and selenohomocholyltaurine (SeHCAT) whole body retention in the assessment of bile acid induced diarrhoea. Eur. J. Gastroenterol. Hepatol. 8(2), 117-123 (1996).
19. Lundåsen T, Gälman C, Angelin B, Rudling M. Circulating intestinal fibroblast growth factor 19 has a pronounced diurnal variation and modulates hepatic bile acid synthesis in man. J. Intern. Med. 260(6), 530-536 (2006).
20. Choi M, Moschetta A, Bookout AL et al. Identification of a hormonal basis for gallbladder filling. Nat. Med. 12(11), 1253-1255 (2006).
21. Van Schaik FD, Gadaleta RM, Schaap FG et al. Tu1883 activation of the nuclear receptor FXR by oral chenodeoxycholic acid in patients with Crohn's colitis: potential therapeutic consequences for inflammatory bowel disease. Gastroenterology 142(5), S869 (2012).
22. Kawamata Y, Fujii R, Hosoya M et al. A G protein-coupled receptor responsive to bile acids. J. Biol. Chem. 278(11), 9435-9440 (2003).
23. Chen X, Lou G, Meng Z, Huang W. TGR5: a novel target for weight maintenance and glucose metabolism. Exp. Diabetes Res. 2011, 853501 (2011).
24. Aldini R, Roda A, Festi D et al. Bile acid malabsorption and bile acid diarrhea in intestinal resection. Dig. Dis. Sci. 27(6), 495-502 (1982).
25. Hofmann AF. The syndrome of ileal disease and the broken enterohepatic circulation: cholerhetic enteropathy. Gastroenterology 52(4), 752-757 (1967).
26. Grundy SM, Ahrens EH Jr, Salen G. Interruption of the enterohepatic circulation of bile acids in man: comparative effects of cholestyramine and ileal exclusion on cholesterol metabolism. J. Lab. Clin. Med. 78(1), 94-121 (1971).
27. Smith MJ, Cherian P, Raju GS, Dawson BF, Mahon S, Bardhan KD. Bile acid malabsorption in persistent diarrhoea. J. R. Coll. Physicians Lond. 34(5), 448-451 (2000).
28. Hofmann AF, Poley JR. Role of bile acid malabsorption in pathogenesis of diarrhea and steatorrhea in patients with ileal resection. I. Response to cholestyramine or replacement of dietary long chain triglyceride by medium chain triglyceride. Gastroenterology 62(5), 918-934 (1972).
29. Ung KA, Olofsson G, Fae A, Kilander A, Ohlsson C, Jonsson O. In vitro determination of active bile acid absorption in small biopsy specimens obtained endoscopically or surgically from the human intestine. Eur. J. Clin. Invest. 32(2), 115-121 (2002).
30. Holdstock G, Phillips G, Hames TK et al. Potential of SeHCAT retention as an indicator of terminal ileal involvement in inflammatory bowel disease. Eur. J. Nucl. Med. 10(11-12), 528-530 (1985).
31. Scheurlen C, Kruis W, Büll U, Stellaard F, Lang P, Paumgartner G. Comparison of 75SeHCAT retention half-life and fecal content of individual bile acids in patients with chronic diarrheal disorders. Digestion 35(2), 102-108 (1986).
32. Vantrappen G, Ghoos Y, Rutgeerts P, Janssens J. Bile acid studies in uncomplicated Crohn's disease. Gut 18(9), 730-735 (1977).
33. Rutgeerts P, Ghoos Y, Vantrappen G. Kinetics of primary bile acids in patients with non-operated Crohn's disease. Eur. J. Clin. Invest. 12(2), 135-143 (1982).
34. Stelzner M, Somasundaram S, Khakberdiev T. Systemic effects of acute terminal ileitis on uninflamed gut aggravate bile acid malabsorption. J. Surg. Res. 99(2), 359-364 (2001).
35. Rutgeerts P, Ghoos Y, Vantrappen G. Bile acid studies in patients with Crohn's colitis. Gut 20(12), 1072-1077 (1979).
36. Davie RJ, Hosie KB, Grobler SP, Newbury-Ecob RA, Keighley MR, Birch NJ. Ileal bile acid malabsorption in colonic Crohn's disease. Br. J. Surg. 81(2), 289-290 (1994).
37. Jung D, Fantin AC, Scheurer U, Fried M, Kullak-Ublick GA. Human ileal bile acid transporter gene ASBT (SLC10A2) is transactivated by the glucocorticoid receptor. Gut 53(1), 78-84 (2004).
38. Best WR, Becktel JM, Singleton JW, Kern F Jr. Development of a Crohn's disease activity index. National Cooperative Crohn's Disease Study. Gastroenterology 70(3), 439-444 (1976).
39. Kwon RS, Carey MC. Do steroids ameliorate bile acid malabsorption in Crohn's disease? Gut 53(1), 10-11 (2004).
40. Bajor A, Kilander A, Gälman C, Rudling M, Ung KA. Budesonide treatment is associated with increased bile acid absorption in collagenous colitis. Aliment. Pharmacol. Ther. 24(11-12), 1643-1649 (2006).
41. Wang L, Lee YK, Bundman D et al. Redundant pathways for negative feedback regulation of bile acid production. Dev. Cell 2(6), 721-731 (2002).
42. Pai R, French D, Ma N et al. Antibodymediated inhibition of fibroblast growth factor 19 results in increased bile acids synthesis and ileal malabsorption of bile acids in cynomolgus monkeys. Toxicol. Sci. 126(2), 446-456 (2012).
43. Neimark E, Chen F, Li X et al. c-Fos is a critical mediator of inflammatory-mediated repression of the apical sodium-dependent bile acid transporter. Gastroenterology 131(2), 554-567 (2006).
44. Nijmeijer RM, Gadaleta RM, van Mil SW et al. ; Dutch Initiative on Crohn, Colitis (ICC). Farnesoid X receptor (FXR) activation and FXR genetic variation in inflammatory bowel disease. PLoS One 6(8), e23745 (2011).
45. Gadaleta RM, Oldenburg B, Willemsen EC et al. Activation of bile salt nuclear receptor FXR is repressed by pro-inflammatory cytokines activating NF-kB signaling in the intestine. Biochim. Biophys. Acta 1812(8), 851-858 (2011).
46. Vavassori P, Mencarelli A, Renga B, Distrutti E, Fiorucci S. The bile acid receptor FXR is a modulator of intestinal innate immunity. J. Immunol. 183(10), 6251-6261 (2009).
47. Lenicek M, Duricova D, Komarek V et al. Bile acid malabsorption in inflammatory bowel disease: assessment by serum markers. Inflamm. Bowel Dis. 17(6), 1322-1327 (2011).
48. Walters JR, Tasleem AM, Omer OS, Brydon WG, Dew T, le Roux CW. A new mechanism for bile acid diarrhea: defective feedback inhibition of bile acid biosynthesis. Clin. Gastroenterol. Hepatol. 7(11), 1189-1194 (2009).
49. Lapidus A, Akerlund JE, Einarsson C. Gallbladder bile composition in patients with Crohn's disease. World J. Gastroenterol. 12(1), 70-74 (2006).
50. Jung D, Inagaki T, Gerard RD et al. FXR agonists and FGF15 reduce fecal bile acid excretion in a mouse model of bile acid malabsorption. J. Lipid Res. 48(12), 2693-2700 (2007).
51. Percy-Robb IW, Collee JG. Bile acids: a pH dependent antibacterial system in the gut? Br. Med. J. 3(5830), 813-815 (1972).
52. Berg RD. Bacterial translocation from the gastrointestinal tract. Trends Microbiol. 3(4), 149-154 (1995).
53. Ding JW, Andersson R, Soltesz V, Willén R, Bengmark S. The role of bile and bile acids in bacterial translocation in obstructive jaundice in rats. Eur. Surg. Res. 25(1), 11-19 (1993).
54. Parks RW, Halliday MI, McCrory DC et al. Host immune responses and intestinal permeability in patients with jaundice. Br. J. Surg. 90(2), 239-245 (2003).
55. Pellicciari R, Costantino G, Fiorucci S. Farnesoid X receptor: from structure to potential clinical applications. J. Med. Chem. 48(17), 5383-5403 (2005).
56. Gadaletta RM, van Erpecum KJ, Oldenburg B et al. Farnesoid X receptor activation inhibits inflammation and preserves the intestinal barrier in inflammatory bowel disease. Gut 60(4), 463-472 (2011).
57. Marschall HU, Luketic V, Lovgren-Sandblom A et al. 964 The farnesoid X receptor (FXR) agonist obeticholic acid (OCA) increases plasma FGF-19 concentrations and decreases bile acid synthesis in primary biliary cirrhosis (PBC). J. Hepatol. 56, S377 (2012).