Bile Acid Uptake Transporters as Targets for Therapy

Digestive Diseases

Volumn 35, Issue 3, 2017, Pages 251-258

  Slijepcevic, Davor ^a   Van De Graaf, Stan F J ^a  

^a ACADEMIC MEDICAL CENTER   (Netherlands)

Author keywords

Apical sodium dependent bile acid transporter; Bile acid signaling; Cholestasis; Hepatitis B virus; Sodium taurocholate cotransporting polypeptide

Indexed keywords

BILE SALT EXPORT PUMP; CHOLESTEROL 7ALPHA MONOOXYGENASE; CHOLIC ACID; FARNESOID X RECEPTOR; G PROTEIN COUPLED RECEPTOR 5; GLUCAGON LIKE PEPTIDE 1; LOW DENSITY LIPOPROTEIN; PEPTIDES AND PROTEINS; SODIUM BILE ACID COTRANSPORTER; SOLUTE CARRIER ORGANIC ANION TRANSPORTER 1B1; SOLUTE CARRIER ORGANIC ANION TRANSPORTER 1B3; TENOFOVIR; UNCLASSIFIED DRUG; BILE ACID; CARRIER PROTEIN;

ARTICLE; ENTEROHEPATIC CIRCULATION; GLUCOSE METABOLISM; HEPATITIS B VIRUS; HEPATITIS DELTA VIRUS; HUMAN; INSULIN SENSITIVITY; KUPFFER CELL; LIVER INJURY; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN POLYMORPHISM; ANIMAL; CHOLESTASIS; LIVER; METABOLISM; MOLECULARLY TARGETED THERAPY;

ANIMALS; BILE ACIDS AND SALTS; CHOLESTASIS; ENTEROHEPATIC CIRCULATION; HUMANS; LIVER; MEMBRANE TRANSPORT PROTEINS; MOLECULAR TARGETED THERAPY;

EID: 85014586036     PISSN: 02572753     EISSN: 14219875     Source Type: Journal    
DOI: 10.1159/000450983     Document Type: Article

References (82)

1. Esteller A: Physiology of bile secretion. World J Gastroenterol 2008; 14: 5641-5649.
2. Russell DW: The enzymes, regulation, and genetics of bile acid synthesis. Annu Rev Biochem 2003; 72: 137-174.
3. Hofmann AF, Sjovall J, Kurz G, et al: A proposed nomenclature for bile acids. J Lipid Res 1992; 33: 599-604.
4. Hofmann AF: The enterohepatic circulation of bile acids in mammals: form and functions. Front Biosci (Landmark Ed) 2009; 14: 2584-2598.
5. Dawson PA, Karpen SJ: Intestinal transport and metabolism of bile acids. J Lipid Res 2015; 56: 1085-1099.
6. Vlahcevic ZR, Pandak WM, Stravitz RT: Regulation of bile acid biosynthesis. Gastroenterol Clin North Am 1999; 28: 1-25.
7. Kullak-Ublick GA, Stieger B, Meier PJ: Enterohepatic bile salt transporters in normal physiology and liver disease. Gastroenterology 2004; 126: 322-342.
8. Meier PJ, Stieger B: Bile salt transporters. Annu Rev Physiol 2002; 64: 635-661.
9. Angelin B, Bjorkhem I, Einarsson K, et al: Hepatic uptake of bile acids in man. Fasting and postprandial concentrations of individual bile acids in portal venous and systemic blood serum. J Clin Invest 1982; 70: 724-731.
10. Linnet K: Postprandial plasma concentrations of glycine and taurine conjugated bile acids in healthy subjects. Gut 1983; 24: 249-252.
11. Meier PJ: Molecular mechanisms of hepatic bile salt transport from sinusoidal blood into bile. Am J Physiol 1995; 269(6 pt 1):G801-G812.
12. Bijsmans IT, Bouwmeester RA, Geyer J, et al: Homo-and hetero-dimeric architecture of the human liver Na+-dependent taurocholate co-transporting protein. Biochem J 2012; 441: 1007-1016.
13. Hu NJ, Iwata S, Cameron AD, et al: Crystal structure of a bacterial homologue of the bile acid sodium symporter ASBT. Nature 2011; 478: 408-411.
14. Stieger B: The role of the sodium-taurocholate cotransporting polypeptide (NTCP) and of the bile salt export pump (BSEP) in physiology and pathophysiology of bile formation. Handb Exp Pharmacol 2011; 201: 205-259.
15. Kim RB, Leake B, Cvetkovic M, et al: Modulation by drugs of human hepatic sodium-dependent bile acid transporter (sodium taurocholate cotransporting polypeptide) activity. J Pharmacol Exp Ther 1999; 291: 1204-1209.
16. Visser WE, Wong WS, van Mullem AA, et al: Study of the transport of thyroid hormone by transporters of the SLC10 family. Mol Cell Endocrinol 2010; 315: 138-145.
17. Groothuis GM, Hardonk MJ, Keulemans KP, et al: Autoradiographic and kinetic demonstration of acinar heterogeneity of taurocholate transport. Am J Physiol 1982; 243:G455-G462.
18. Ho RH, Leake BF, Roberts RL, et al: Ethnicitydependent polymorphism in Na+-taurocholate cotransporting polypeptide (SLC10A1) reveals a domain critical for bile acid substrate recognition. J Biol Chem 2004; 279: 7213-7222.
19. Vaz FM, Paulusma CC, Huidekoper H, et al: Sodium taurocholate cotransporting polypeptide (SLC10A1) deficiency: conjugated hypercholanemia without a clear clinical phenotype. Hepatology 2015; 61: 260-267.
20. Slijepcevic D, Kaufman C, Wichers CG, et al: Impaired uptake of conjugated bile acids and hepatitis b virus pres1-binding in na(+)-taurocholate cotransporting polypeptide knockout mice. Hepatology 2015; 62: 207-219.
21. Von Dippe P, Amoui M, Alves C, et al: Na(+)-dependent bile acid transport by hepatocytes is mediated by a protein similar to microsomal epoxide hydrolase. Am J Physiol 1993; 264(3 pt 1):G528-G534.
22. Honscha W, Platte HD, Oesch F, et al: Relationship between the microsomal epoxide hydrolase and the hepatocellular transport of bile acids and xenobiotics. Biochem J 1995; 311(pt 3):975-979.
23. Kullak-Ublick GA, Stieger B, Hagenbuch B, et al: Hepatic transport of bile salts. Semin Liver Dis 2000; 20: 273-292.
24. Klaassen CD, Aleksunes LM: Xenobiotic, bile acid, and cholesterol transporters: function and regulation. Pharmacol Rev 2010; 62: 1-96.
25. van de Steeg E, Stranecky V, Hartmannova H, et al: Complete OATP1B1 and OATP1B3 deficiency causes human Rotor syndrome by interrupting conjugated bilirubin reuptake into the liver. J Clin Invest 2012; 122: 519-528.
26. van de Steeg E, Wagenaar E, van der Kruijssen CM, et al: Organic anion transporting polypeptide 1a/1b-knockout mice provide insights into hepatic handling of bilirubin, bile acids, and drugs. J Clin Invest 2010; 120: 2942-2952.
27. Csanaky IL, Lu H, Zhang Y, Ogura K, et al: Organic anion-transporting polypeptide 1b2 (Oatp1b2) is important for the hepatic uptake of unconjugated bile acids: Studies in Oatp1b2-null mice. Hepatology 2011; 53: 272-281.
28. Gong L, Aranibar N, Han YH, et al: Characterization of organic anion-transporting polypeptide (Oatp) 1a1 and 1a4 null mice reveals altered transport function and urinary metabolomic profiles. Toxicol Sci 2011; 122: 587-597.
29. Zhang Y, Csanaky IL, Selwyn FP, et al: Organic anion-transporting polypeptide 1a4 (Oatp1a4) is important for secondary bile acid metabolism. Biochem Pharmacol 2013; 86: 437-445.
30. Zhang Y, Csanaky IL, Lehman-McKeeman LD, et al: Loss of organic anion transporting polypeptide 1a1 increases deoxycholic acid absorption in mice by increasing intestinal permeability. Toxicol Sci 2011; 124: 251-260.
31. Yan H, Zhong G, Xu G, et al: Sodium taurocholate cotransporting polypeptide is a functional receptor for human hepatitis B and D virus. Elife 2012; 1:e00049.
32. Bogomolov P, Alexandrov A, Voronkova N, et al: Treatment of chronic hepatitis D with the entry inhibitor myrcludex B: first results of a phase Ib/IIa study. J Hepatol 2016; 65: 490-498.
33. Blank A, Markert C, Hohmann N, et al: Firstin-human application of the novel hepatitis B and hepatitis D virus entry inhibitor myrcludex B. J Hepatol 2016; 65: 483-489.
34. Schulze A, Schieck A, Ni Y, et al: Fine mapping of pre-S sequence requirements for hepatitis B virus large envelope protein-mediated receptor interaction. J Virol 2010; 84: 1989-2000.
35. Volz T, Allweiss L, Ben MBarek M, et al: The entry inhibitor Myrcludex-B efficiently blocks intrahepatic virus spreading in humanized mice previously infected with hepatitis B virus. J Hepatol 2013; 58: 861-867.
36. Schieck A, Schulze A, Gahler C, et al: Hepatitis B virus hepatotropism is mediated by specific receptor recognition in the liver and not restricted to susceptible hosts. Hepatology 2013; 58: 43-53.
37. Beuers U, Trauner M, Jansen P, et al: New paradigms in the treatment of hepatic cholestasis: from UDCA to FXR, PXR and beyond. J Hepatol 2015; 62(1 suppl):S25-S37.
38. Eloranta JJ, Kullak-Ublick GA: Coordinate transcriptional regulation of bile acid homeostasis and drug metabolism. Arch Biochem Biophys 2005; 433: 397-412.
39. Makishima M, Okamoto AY, Repa JJ, et al: Identification of a nuclear receptor for bile acids. Science 1999; 284: 1362-1365.
40. Parks DJ, Blanchard SG, Bledsoe RK, et al: Bile acids: natural ligands for an orphan nuclear receptor. Science 1999; 284: 1365-1368.
41. Wang H, Chen J, Hollister K, et al: Endogenous bile acids are ligands for the nuclear receptor FXR/BAR. Mol Cell 1999; 3: 543-553.
42. 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 2000; 6: 517-526.
43. Lu TT, Makishima M, Repa JJ, et al: Molecular basis for feedback regulation of bile acid synthesis by nuclear receptors. Mol Cell 2000; 6: 507-515.
44. Pellicciari R, Fiorucci S, Camaioni E, et al: 6alpha-ethyl-chenodeoxycholic acid (6-ECDCA), a potent and selective FXR agonist endowed with anticholestatic activity. J Med Chem 2002; 45: 3569-3572.
45. Liu Y, Binz J, Numerick MJ, et al: Hepatoprotection by the farnesoid X receptor agonist GW4064 in rat models of intra-and extrahepatic cholestasis. J Clin Invest 2003; 112: 1678-1687.
46. Hirschfield GM, Mason A, Luketic V, et al: Efficacy of obeticholic acid in patients with primary biliary cirrhosis and inadequate response to ursodeoxycholic acid. Gastroenterology 2015; 148: 751-761.e8.
47. Anwer MS, Stieger B: Sodium-dependent bile salt transporters of the SLC10A transporter family: more than solute transporters. Pflugers Arch 2014; 466: 77-89.
48. Zhang Y, Csanaky IL, Cheng X, et al: Organic anion transporting polypeptide 1a1 null mice are sensitive to cholestatic liver injury. Toxicol Sci 2012; 127: 451-462.
49. Kuiper EM, van Erpecum KJ, Beuers U, et al: The potent bile acid sequestrant colesevelam is not effective in cholestatic pruritus: results of a double-blind, randomized, placebo-controlled trial. Hepatology 2010; 52: 1334-1340.
50. Graffner H, Gillberg PG, Rikner L, et al: The ileal bile acid transporter inhibitor A4250 decreases serum bile acids by interrupting the enterohepatic circulation. Aliment Pharmacol Ther 2016; 43: 303-310.
51. Baghdasaryan A, Fuchs CD, Osterreicher CH, et al: Inhibition of intestinal bile acid absorption improves cholestatic liver and bile duct injury in a mouse model of sclerosing cholangitis. J Hepatol 2016; 64: 674-681.
52. Miethke AG, Zhang W, Simmons J, et al: Pharmacological inhibition of apical sodiumdependent bile acid transporter changes bile composition and blocks progression of sclerosing cholangitis in multidrug resistance 2 knockout mice. Hepatology 2016; 63: 512-523.
53. Inagaki T, Choi M, Moschetta A, et al: Fibroblast growth factor 15 functions as an enterohepatic signal to regulate bile acid homeostasis. Cell Metab 2005; 2: 217-225.
54. Modica S, Petruzzelli M, Bellafante E, et al: Selective activation of nuclear bile acid receptor FXR in the intestine protects mice against cholestasis. Gastroenterology 2012; 142: 355-365.e1-e4.
55. Luo J, Ko B, Elliott M, et al: A nontumorigenic variant of FGF19 treats cholestatic liver diseases. Sci Transl Med 2014; 6: 247ra100.
56. Zhou M, Learned RM, Rossi SJ, et al: Engineered fibroblast growth factor 19 reduces liver injury and resolves sclerosing cholangitis in Mdr2-deficient mice. Hepatology 2016; 63: 914-929.
57. Mayo MJ, Wigg AJ, Roberts SK, Arnold H, et al: NGM282, a novel variant of FGF-19, demonstrates biologic activity in primary biliary cirrhosis patients with an incomplete response to ursodeoxycholic acid:results of a phase 2 multicenter, randomized, double blinded, placebo controlled trial. Hepatology 2015; 62: 263A-264A.
58. Schaap FG, Trauner M, Jansen PL: Bile acid receptors as targets for drug development. Nat Rev Gastroenterol Hepatol 2014; 11: 55-67.
59. de Aguiar Vallim TQ, Tarling EJ, Edwards PA. Pleiotropic roles of bile acids in metabolism. Cell Metab 2013; 17: 657-669.
60. Rudling M, Camilleri M, Graffner H, et al: Specific inhibition of bile acid transport alters plasma lipids and GLP-1. BMC Cardiovasc Disord 2015; 15: 75.
61. Lundasen T, Andersson EM, Snaith M, et al: Inhibition of intestinal bile acid transporter Slc10a2 improves triglyceride metabolism and normalizes elevated plasma glucose levels in mice. PLoS One 2012; 7:e37787.
62. Rao A, Kosters A, Mells J, et al: Administration of an ileal apical sodium-dependent bile acid transporter inhibitor protects against non-alcoholic fatty liver disease in high fat diet-fed mice. Hepatology 2015; 62: 217A.
63. Harach T, Pols TW, Nomura M, Maida A, et al: TGR5 potentiates GLP-1 secretion in response to anionic exchange resins. Sci Rep 2012; 2: 430.
64. Potthoff MJ, Potts A, He T, et al: Colesevelam suppresses hepatic glycogenolysis by TGR5-mediated induction of GLP-1 action in DIO mice. Am J Physiol Gastrointest Liver Physiol 2013; 304:G371-G380.
65. Nwose OM, Jones MR: Atypical mechanism of glucose modulation by colesevelam in patients with type 2 diabetes. Clin Med Insights Endocrinol Diabetes 2013; 6: 75-79.
66. Ullmer C, Alvarez Sanchez R, Sprecher U, et al: Systemic bile acid sensing by G proteincoupled bile acid receptor 1 (GPBAR1) promotes PYY and GLP-1 release. Br J Pharmacol 2013; 169: 671-684.
67. Brighton CA, Rievaj J, Kuhre RE, et al: Bile acids trigger GLP-1 release predominantly by accessing basolaterally located G proteincoupled bile acid receptors. Endocrinology 2015; 156: 3961-3970.
68. Thomas C, Gioiello A, Noriega L, et al: TGR5-mediated bile acid sensing controls glucose homeostasis. Cell Metab 2009; 10: 167-177.
69. Watanabe M, Houten SM, Mataki C, et al: Bile acids induce energy expenditure by promoting intracellular thyroid hormone activation. Nature 2006; 439: 484-489.
70. Pournaras DJ, Glicksman C, Vincent RP, et al: The role of bile after Roux-en-Y gastric bypass in promoting weight loss and improving glycaemic control. Endocrinology 2012; 153: 3613-3619.
71. Cummings BP, Bettaieb A, Graham JL, et al: Vertical sleeve gastrectomy improves glucose and lipid metabolism and delays diabetes onset in UCD-T2DM rats. Endocrinology 2012; 153: 3620-3632.
72. Kohli R, Kirby M, Setchell KD, et al: Intestinal adaptation after ileal interposition surgery increases bile acid recycling and protects against obesity-related comorbidities. Am J Physiol Gastrointest Liver Physiol 2010; 299:G652-G660.
73. Ryan KK, Tremaroli V, Clemmensen C, et al: FXR is a molecular target for the effects of vertical sleeve gastrectomy. Nature 2014; 509: 183-188.
74. Ding L, Sousa KM, Jin L, Dong B, et al: Vertical sleeve gastrectomy activates GPBAR-1/ TGR5 to sustain weight loss, improve fatty liver, and remit insulin resistance in mice. Hepatology 2016; 64: 760-773.
75. Myronovych A, Kirby M, Ryan KK, et al: Vertical sleeve gastrectomy reduces hepatic steatosis while increasing serum bile acids in a weight-loss-independent manner. Obesity (Silver Spring) 2014; 22: 390-400.
76. Keitel V, Reinehr R, Gatsios P, et al: The Gprotein coupled bile salt receptor TGR5 is expressed in liver sinusoidal endothelial cells. Hepatology 2007; 45: 695-704.
77. Kawamata Y, Fujii R, Hosoya M, et al: A G protein-coupled receptor responsive to bile acids. J Biol Chem 2003; 278: 9435-9440.
78. Calmus Y, Guechot J, Podevin P, et al: Differential effects of chenodeoxycholic and ursodeoxycholic acids on interleukin 1, interleukin 6 and tumor necrosis factor-alpha production by monocytes. Hepatology 1992; 16: 719-723.
79. Pols TW, Nomura M, Harach T, et al: TGR5 activation inhibits atherosclerosis by reducing macrophage inflammation and lipid loading. Cell Metab 2011; 14: 747-757.
80. Vassileva G, Hu W, Hoos L, Tetzloff G, et al: Gender-dependent effect of Gpbar1 genetic deletion on the metabolic profiles of diet-induced obese mice. J Endocrinol 2010; 205: 225-232.
81. Rose AJ, Berriel Diaz MB, Reimann A, et al: Molecular control of systemic bile acid homeostasis by the liver glucocorticoid receptor. Cell Metab 2011; 14: 123-130.
82. Oehler N, Volz T, Bhadra OD, et al: Binding of hepatitis B virus to its cellular receptor alters the expression profile of genes of bile acid metabolism. Hepatology 2014; 60: 1483-1493.