Pharmacological inhibition of apical sodium-dependent bile acid transporter changes bile composition and blocks progression of sclerosing cholangitis in multidrug resistance 2 knockout mice

Hepatology

Volumn 63, Issue 2, 2016, Pages 512-523

  Miethke, Alexander G ^a,c   Zhang, Wujuan ^a   Simmons, Julia ^a   Taylor, Amy E ^a   Shi, Tiffany ^a   Shanmukhappa, Shiva Kumar ^a,c   Karns, Rebekah ^a   White, Shana ^a   Jegga, Anil G ^a,c   Lages, Celine S ^a   Nkinin, Stephenson ^a   Keller, Bradley T ^b   Setchell, Kenneth D R ^a,c  

^a CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^b Consultant to Shire plc ^*  (United States)

^c UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE AMINOTRANSFERASE; ALKALINE PHOSPHATASE; ANTIINFLAMMATORY AGENT; APICAL SODIUM DEPENDENT BILE ACID TRANSPORTER; BILE ACID; BILIRUBIN; MONOCYTE CHEMOTACTIC PROTEIN 1; NEUTROPHIL GELATINASE ASSOCIATED LIPOCALIN; PEPTIDES AND PROTEINS; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; PHOSPHATIDYLCHOLINE; SC 435; SOMATOMEDIN C; UNCLASSIFIED DRUG; 1-(4-(4-(3,3-DIBUTYL-7-(DIMETHYLAMINO)-2,3,4,5-TETRAHYDRO-4-HYDROXY-1,1-DIOXIDO-1-BENZOTHIEPIN-5-YL)PHENOXY)BUTYL)-4-AZA-1-AZONIABICYCLO(2.2.2)OCTANE; AMINE OXIDE; COTRANSPORTER; MULTIDRUG RESISTANCE PROTEIN; ORGANIC ANION TRANSPORTER; P-GLYCOPROTEIN 2; SODIUM-BILE ACID COTRANSPORTER; TROPANE DERIVATIVE;

ALANINE AMINOTRANSFERASE BLOOD LEVEL; ALKALINE PHOSPHATASE BLOOD LEVEL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BILE COMPOSITION; CONTROLLED STUDY; DISEASE COURSE; DOWN REGULATION; FEMALE; MASS SPECTROMETRY; MOUSE; NONHUMAN; PRIORITY JOURNAL; RNA SEQUENCE; SCLEROSING CHOLANGITIS; ANIMAL; ANTAGONISTS AND INHIBITORS; BILE; CHEMISTRY; CHOLANGITIS, SCLEROSING; DEFICIENCY; KNOCKOUT MOUSE;

ANIMALS; BILE; CHOLANGITIS, SCLEROSING; CYCLIC N-OXIDES; DISEASE PROGRESSION; FEMALE; MICE; MICE, KNOCKOUT; ORGANIC ANION TRANSPORTERS, SODIUM-DEPENDENT; P-GLYCOPROTEINS; SYMPORTERS; TROPANES;

EID: 84956606917     PISSN: 02709139     EISSN: 15273350     Source Type: Journal    
DOI: 10.1002/hep.27973     Document Type: Article

References (38)

1. Beuers U, Trauner M, Jansen P, Poupon R. New paradigms in the treatment of hepatic cholestasis: from UDCA to FXR, PXR and beyond. J Hepatol 2015;62(1 Suppl):S25-S37.
2. Hirschfield GM, Heathcote EJ, Gershwin ME. Pathogenesis of cholestatic liver disease and therapeutic approaches. Gastroenterology 2010;139:1481-1496.
3. Ghonem NS, Assis DN, Boyer JL. On fibrates and cholestasis: a review. Hepatology 2015.
4. Patel T, Gores GJ. Apoptosis and hepatobiliary disease. Hepatology 1995;21:1725-1741.
5. Karlsen TH, Franke A, Melum E, Kaser A, Hov JR, Balschun T, et al. Genome-wide association analysis in primary sclerosing cholangitis. Gastroenterology 2010;138:1102-1111.
6. Hoegenauer K, Arista L, Schmiedeberg N, Werner G, Jaksche H, Bouhelal R, et al. G-protein-coupled bile acid receptor 1 (GPBAR1, TGR5) agonists reduce the production of pro-inflammatory cytokines and stabilize the alternative macrophage phenotype. J Med Chem 2014;57:10343-10354.
7. Gonzales E, Davit-Spraul A, Baussan C, Buffet C, Maurice M, Jacquemin E. Liver diseases related to MDR3 (ABCB4) gene deficiency. Front Biosci 2009;14:4242-4256.
8. Trauner M, Fickert P, Baghdasaryan A, Claudel T, Halilbasic E, Moustafa T, et al. New insights into autoimmune cholangitis through animal models. Dig Dis 2010;28:99-104.
9. -/- mice: a model for low phospholipid-associated cholelithiasis. Hepatology 2004;39:117-128.
10. Fickert P, Fuchsbichler A, Wagner M, Zollner G, Kaser A, Tilg H, et al. Regurgitation of bile acids from leaky bile ducts causes sclerosing cholangitis in Mdr2 (Abcb4) knockout mice. Gastroenterology 2004;127:261-274.
11. Fickert P, Wagner M, Marschall HU, Fuchsbichler A, Zollner G, Tsybrovskyy O, et al. 24-norUrsodeoxycholic acid is superior to ursodeoxycholic acid in the treatment of sclerosing cholangitis in Mdr2 (Abcb4) knockout mice. Gastroenterology 2006;130:465-481.
12. Stiedl P, McMahon R, Blaas L, Stanek V, Svinka J, Grabner B, et al. Growth hormone resistance exacerbates cholestasis-induced murine liver fibrosis. Hepatology 2015;61:613-626.
13. West KL, Ramjiganesh T, Roy S, Keller BT, Fernandez ML. 1-[4-[4[(4R, 5R)-3, 3-Dibutyl-7-(dimethylamino)-2, 3, 4, 5-tetrahydro-4-hydroxy-1, 1-di oxido-1-benzothiepin-5-yl]phenoxy]butyl]-4-aza-1-azoniabicyclo[2.2.2] octane methanesulfonate (SC-435), an ileal apical sodium-codependent bile acid transporter inhibitor alters hepatic cholesterol metabolism and lowers plasma low-density lipoprotein-cholesterol concentrations in guinea pigs. J Pharmacol Exp Ther 2002;303:293-299.
14. Lages CS, Simmons J, Chougnet CA, Miethke AG. Regulatory T cells control the CD8 adaptive immune response at the time of ductal obstruction in experimental biliary atresia. Hepatology 2012;56:219-227.
15. Hagio M, Matsumoto M, Fukushima M, Hara H, Ishizuka S. Improved analysis of bile acids in tissues and intestinal contents of rats using LC/ESI-MS. J Lipid Res 2009;50:173-180.
16. He H, Mennone A, Boyer JL, Cai SY. Combination of retinoic acid and ursodeoxycholic acid attenuates liver injury in bile duct-ligated rats and human hepatic cells. Hepatology 2011;53:548-557.
17. Macri SC, Bailey CC, de Oca NM, Silva NA, Rosene DL, Mansfield KG, Miller AD. Immunophenotypic alterations in resident immune cells and myocardial fibrosis in the aging rhesus macaque (Macaca mulatta) heart. Toxicol Pathol 2012;40:637-646.
18. Trapnell C, Pachter L, Salzberg SL. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 2009;25:1105-1111.
19. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, et al. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 2010;28:511-515.
20. Chen J, Bardes EE, Aronow BJ, Jegga AG. ToppGene Suite for gene list enrichment analysis and candidate gene prioritization. Nucleic Acids Res 2009;37:W305-W311.
21. Galman C, Arvidsson I, Angelin B, Rudling M. Monitoring hepatic cholesterol 7alpha-hydroxylase activity by assay of the stable bile acid intermediate 7alpha-hydroxy-4-cholesten-3-one in peripheral blood. J Lipid Res 2003;44:859-866.
22. Hofmann AF. Bile acid secretion, bile flow and biliary lipid secretion in humans. Hepatology 1990;12:17S-22S; discussion, 22S-25S.
23. Hofmann AF, Small DM. Detergent properties of bile salts: correlation with physiological function. Annu Rev Med 1967;18:333-376.
24. Wang DQ, Carey MC. Complete mapping of crystallization pathways during cholesterol precipitation from model bile: influence of physical-chemical variables of pathophysiologic relevance and identification of a stable liquid crystalline state in cold, dilute and hydrophilic bile salt-containing systems. J Lipid Res 1996;37:606-630.
25. Golbar HM, Izawa T, Wijesundera KK, Tennakoon AH, Katou-Ichikawa C, Tanaka M, et al. Expression of nestin in remodelling of alpha-naphthylisothiocyanate-induced acute bile duct injury in rats. J Comp Pathol 2014;151:255-263.
26. West KL, Zern TL, Butteiger DN, Keller BT, Fernandez ML. SC-435, an ileal apical sodium co-dependent bile acid transporter (ASBT) inhibitor lowers plasma cholesterol and reduces atherosclerosis in guinea pigs. Atherosclerosis 2003;171:201-210.
27. Hulzebos CV, Voshol PJ, Wolters H, Kruit JK, Ottenhof R, Groen AK, et al. Bile duct proliferation associated with bile salt-induced hypercholeresis in Mdr2 P-glycoprotein-deficient mice. Liver Int 2005;25:604-612.
28. van Nieuwerk CM, Groen AK, Ottenhoff R, van Wijland M, van den Bergh Weerman MA, Tytgat GN, et al. The role of bile salt composition in liver pathology of mdr2 (-/-) mice: differences between males and females. J Hepatol 1997;26:138-145.
29. Billington D, Evans CE, Godfrey PP, Coleman R. Effects of bile salts on the plasma membranes of isolated rat hepatocytes. Biochem J 1980;188:321-327.
30. Faubion WA, Guicciardi ME, Miyoshi H, Bronk SF, Roberts PJ, Svingen PA, et al. Toxic bile salts induce rodent hepatocyte apoptosis via direct activation of Fas. J Clin Invest 1999;103:137-145.
31. Yerushalmi B, Dahl R, Devereaux MW, Gumpricht E, Sokol RJ. Bile acid-induced rat hepatocyte apoptosis is inhibited by antioxidants and blockers of the mitochondrial permeability transition. Hepatology 2001;33:616-626.
32. Banales JM, Prieto J, Medina JF. Cholangiocyte anion exchange and biliary bicarbonate excretion. World J Gastroenterol 2006;12:3496-3511.
33. Beuers U, Hohenester S, de Buy Wenniger LJ, Kremer AE, Jansen PL, Elferink RP. The biliary HCO(3)(-) umbrella: a unifying hypothesis on pathogenetic and therapeutic aspects of fibrosing cholangiopathies. Hepatology 2010;52:1489-1496.
34. Lamireau T, Zoltowska M, Levy E, Yousef I, Rosenbaum J, Tuchweber B, Desmouliere A. Effects of bile acids on biliary epithelial cells: proliferation, cytotoxicity, and cytokine secretion. Life Sci 2003;72:1401-1411.
35. Ramm GA, Shepherd RW, Hoskins AC, Greco SA, Ney AD, Pereira TN, et al. Fibrogenesis in pediatric cholestatic liver disease: role of taurocholate and hepatocyte-derived monocyte chemotaxis protein-1 in hepatic stellate cell recruitment. Hepatology 2009;49:533-544.
36. Labbus K, Henning M, Borkham-Kamphorst E, Geisler C, Berger T, Mak TW, et al. Proteomic profiling in Lipocalin 2 deficient mice under normal and inflammatory conditions. J Proteomics 2013;78:188-196.
37. McMahan RH, Wang XX, Cheng LL, Krisko T, Smith M, El Kasmi K, et al. Bile acid receptor activation modulates hepatic monocyte activity and improves nonalcoholic fatty liver disease. J Biol Chem 2013;288:11761-11770.
38. Harach T, Pols TW, Nomura M, Maida A, Watanabe M, Auwerx J, Schoonjans K. TGR5 potentiates GLP-1 secretion in response to anionic exchange resins. Sci Rep 2012;2:430.