Obstructive cholestasis induces TNF-α- and IL-1β-mediated periportal downregulation of Bsep and zonal regulation of Ntcp, Oatp1a4, and Oatp1b2

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 293, Issue 6, 2007, Pages

  Donner, Markus G ^a   Schumacher, Stephanie ^a   Warskulat, Ulrich ^a   Heinemann, Jane ^a   Haũssinger, Dieter ^a  

^a HEINRICH HEINE UNIVERSITY   (Germany)

Author keywords

Acinar regulation; Bile salts; Cytokines; Hepatobiliary transport; Organic anion transporters

Indexed keywords

CELL PROTEIN; GLUTAMATE AMMONIA LIGASE; INTERLEUKIN 1BETA; LIPOPOLYSACCHARIDE; MULTIDRUG RESISTANCE PROTEIN 4; PROTEIN BSEP; PROTEIN NTCP; PROTEIN OATP1A1; PROTEIN OATP1A4; PROTEIN OATP1B2; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BILE DUCT LIGATION; BILE DUCT OBSTRUCTION; CHOLESTASIS; CONTROLLED STUDY; DISEASE ASSOCIATION; DOWN REGULATION; HISTOPATHOLOGY; IMMUNOFLUORESCENCE; INFLAMMATION; LIVER CELL; MALE; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT;

ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; BILE DUCTS; CHOLESTASIS, EXTRAHEPATIC; DOWN-REGULATION; INTERLEUKIN-1; LIVER; MALE; ORGANIC ANION TRANSPORTERS; ORGANIC ANION TRANSPORTERS, SODIUM-DEPENDENT; ORGANIC ANION TRANSPORTERS, SODIUM-INDEPENDENT; RATS; RATS, SPRAGUE-DAWLEY; SYMPORTERS; TISSUE DISTRIBUTION; TUMOR NECROSIS FACTOR-ALPHA;

EID: 37149046027     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00079.2007     Document Type: Article

References (55)

1. Aiso M, Takikawa H, Yamanaka M. Biliary excretion of bile acids and organic anions in zone 1- and zone 3-injured rats. Liver 20: 38-44, 2000.
2. Assem M, Schuetz EG, Leggas M, Sun D, Yasuda K, Reid G, Zelcer N, Adachi M, Strom S, Evans RM, Moore DD, Borst P, Schuetz JD. Interactions between hepatic Mrp4 and Sult2a as revealed by the constitutive androstane receptor and Mrp4 knockout mice. J Biol Chem 279: 22250-22257, 2004.
3. Baier PK, Hempel S, Waldvogel B, Baumgartner U. Zonation of hepatic bile salt transporters. Dig Dis Sci 51: 587-593, 2006.
4. Beierle EA, Vauthey JN, Moldawer LL, Copeland EM. Hepatic tumor necrosis factor-alpha production and distant organ dysfunction in a murine model of obstructive jaundice. Am J Surg 171: 202-206, 1996.
5. Boyer JL, Trauner M, Mennone A, Soroka CJ, Cai SY, Moustafa T, Zollner G, Lee JY, Ballatori N. Upregulation of a basolateral FXR-dependent bile acid efflux transporter OSTalpha-OSTbeta in cholestasis in humans and rodents. Am J Physiol Gastrointest Liver Physiol 290: G1124-G1130, 2006.
6. Cantz T, Nies AT, Brom M, Hofmann AF, Keppler D. MRP2, a human conjugate export pump, is present and transports fluo 3 into apical vacuoles of Hep G2 cells. Am J Physiol Gastrointest Liver Physiol 278: G522-G531, 2000.
7. Cattori V, van Montfoort JE, Stieger B, Landmann L, Meijer DK, Winterhalter KH, Meier PJ, Hagenbuch B. Localization of organic anion transporting polypeptide 4 (Oatp4) in rat liver and comparison of its substrate specificity with Oatp1, Oatp2 and Oatp3. Pflügers Arch 443: 188-195, 2001.
8. Chen G, Baron J, Duffel MW. Enzyme- and sex-specific differences in the intralobular localizations and distributions of aryl sulfotransferase IV (tyrosine-ester sulfotransferase) and alcohol (hydroxysteroid) sulfotransferase a in rat liver. Drug Metab Dispos 23: 1346-1353, 1995.
9. Davis RA, Miyake JH, Hui TY, Spann NJ. Regulation of cholesterol-7alpha-hydroxylase: barely missing a SHP. J Lipid Res 43: 533-543, 2002.
10. Denk GU, Soroka CJ, Takeyama Y, Chen WS, Schuetz JD, Boyer JL. Multidrug resistance-associated protein 4 is up-regulated in liver but down-regulated in kidney in obstructive cholestasis in the rat. J Hepatol 40: 585-591, 2004.
11. Dionne S, Russo P, Tuchweber B, Plaa GL, Yousef IM. Cholic acid and chenodeoxycholic acid transport in the hepatic acinus in rats. Effect of necrosis of zone 3 induced by bromobenzene. Liver 10: 336-342, 1990.
12. Donner MG, Keppler D. Up-regulation of basolateral multidrug resistance protein 3 (Mrp3) in cholestatic rat liver. Hepatology 34: 351-359, 2001.
13. Donner MG, Warskulat U, Saha N, Häussinger D. Enhanced expression of basolateral multidrug resistance protein isoforms Mrp3 and Mrp5 in rat liver by LPS. Biol Chem 385: 331-339, 2004.
14. Ekberg K, Chandramouli V, Kumaran K, Schumann WC, Wahren J, Landau BR. Gluconeogenesis and glucuronidation in liver in vivo and the heterogeneity of hepatocyte function. J Biol Chem 270: 21715-21717, 1995.
15. El Mouelhi M, Kauffman FC. Sublobular distribution of transferases and hydrolases associated with glucuronide, sulfate and glutathione conjugation in human liver. Hepatology 6: 450-456, 1986.
16. Elferink MG, Olinga P, Draaisma AL, Merema MT, Faber KN, Slooff MJ, Meijer DK, Groothius GM. LPS-induced downregulation of MRP2 and BSEP in human liver is due to a posttranscriptional process. Am J Physiol Gastrointest Liver Physiol 287: G1008-G1016, 2004.
17. Geier A, Zollner G, Dietrich CG, Wagner M, Fickert P, Denk H, Van Rooijen N, Matern S, Gartung C, Trauner M. Cytokine-independent repression of rodent Ntcp in obstructive cholestasis. Hepatology 41: 470-477, 2005.
18. Geier A, Dietrich CG, Voigt S, Ananthanarayanan M, Lammert F, Schmitz A, Trauner M, Wasmuth HE, Boraschi D, Balasubramaniyan N, Suchy FJ, Matern S, Gartung C. Cytokine-dependent regulation of hepatic organic anion transporter gene transactivators in mouse liver. Am J Physiol Gastrointest Liver Physiol 289: G831-G841, 2005.
19. Guo GL, Staudinger J, Ogura K, Klaassen CD. Induction of rat organic anion transporting polypeptide 2 by pregnenolone-16alpha-carbonitrile is via interaction with pregnane X receptor. Mol Pharmacol 61: 832-839, 2002.
20. Groothuis GM, Hardonk MJ, Keulemans KP, Nieuwenhuis P, Meijer DK. Autoradiographic and kinetic demonstration of acinar heterogeneity of taurocholate transport. Am J Physiol Gastrointest Liver Physiol 243: G455-G462, 1982.
21. Groothuis GM, Weitering JG, Keulemans KP, Hardonk MJ, Mulder D, Meijer DK. Heterogeneity of rat hepatocytes in bile acid and DBSP transport studied after induction of selective acinar damage by N-hydroxy-2- acetylaminofluorene and carbon tetrachloride. Naunyn Schmiedebergs Arch Pharmacol 322: 310-318, 1983.
22. Gumucio JJ, Balabaud C, Miller DL, DeMason LJ, Appelman HD, Stoecker TJ, Franzblau DR. Bile secretion and liver cell heterogeneity in the rat. J Lab Clin Med 91: 350-362, 1978.
23. Häussinger D, Lamers WH, Moorman AF. Hepatocyte heterogeneity in the metabolism of amino acids and ammonia. Enzyme 46: 72-93, 1992.
24. Haga Y, Sakamoto K, Egami H, Yokoyama Y, Arai M, Mori K, Akagi M. Changes in production of interleukin-1 and interleukin-2 associated with obstructive jaundice and biliary drainage in patients with gastrointestinal cancer. Surgery 106: 842-848, 1989.
25. Hagenbuch N, Reichel C, Stieger B, Cattori V, Fattinger KE, Landmann L, Meier PJ, Kullak-Ublick GA. Effect of phenobarbital on the expression of bile salt and organic anion transporters of rat liver. J Hepatol 34: 881-887, 2001.
26. Homma H, Tada M, Nakamura T, Yamagata S, Matsui M. Heterogeneous zonal distribution of sulfotransferase isoenzymes in rat liver. Arch Biochem Biophys 339: 235-241, 1997.
27. Jones AL, Schmucker DL, Mooney JS, Ockner RK, Adler RD. Alterations in hepatic pericanalicular cytoplasm during enhanced bile secretory activity. Lab Invest 40: 512-517, 1979.
28. Jungermann K. Zonation of metabolism and gene expression in liver. Histochem Cell Biol 103: 81-91, 1995.
29. Katz NR. Methods for the study of liver cell heterogeneity. Histochem J 21: 517-529, 1989.
30. Kera Y, Sippel HW, Penttila KE, Lindros KO. Acinar distribution of glutathione-dependent detoxifying enzymes. Low glutathione peroxidase activity in perivenous hepatocytes. Biochem Pharmacol 36: 2003-2006, 1987.
31. Kubitz R, Wettstein M, Warskulat U, Häussinger D. Regulation of the multidrug resistance protein 2 in the rat liver by lipopolysaccharide and dexamethasone. Gastroenterology 116: 401-410, 1999.
32. Layden TJ, Boyer JL. Influence of bile acids on bile canalicular membrane morphology and the lobular gradient in canalicular size. Lab Invest 39: 110-119, 1978.
33. Lee JM, Trauner M, Soroka CJ, Stieger B, Meier PJ, Boyer JL. Expression of the bile salt export pump is maintained after chronic cholestasis in the rat. Gastroenterology 118: 163-172, 2000.
34. Li L, Meier PJ, Ballatori N. Oatp2 mediates bidirectional organic solute transport: a role for intracellular glutathione. Mol Pharmacol 58: 335-340, 2000.
35. Mühlfeld A, Kubitz R, Dransfeld O, Häussinger D, Wettstein M. Taurine supplementation induces multidrug resistance protein 2 and bile salt export pump expression in rats and prevents endotoxin-induced cholestasis. Arch Biochem Biophys 413: 32-40, 2003.
36. Pang KS, Schwab AJ, Goresky CA, Chiba M. Transport, binding, and metabolism of sulfate conjugates in the liver. Chem Biol Interact 92: 179-207, 1994.
37. Paulusma CC, Kothe MJC, Bakker CTM, Bosma P, van Bokhoven I, van Marle J, Bolder U, Tytgat GN, Oude Elferink RP. Zonal downregulation and redistribution of the multidrug resistance protein 2 during bile duct ligation in rat liver. Hepatology 31: 684-693, 2000.
38. Perez LM, Milkiewicz P, Elias E, Coleman R, Sanchez Pozzi EJ, Roma MG. Bile salt secretory failure in isolated rat hepatocyte couplets: a role for protein kinase C and prevention by protein kinase A. Toxicol Sci 91: 150-158, 2006.
39. Rausch-Derra LC, Hartley DP, Meier PJ, Klaassen CD. Differential effects of microsomal enzyme-inducing chemicals on the hepatic expression of rat organic anion transporters, OATP1 and OATP2. Hepatology 33: 1469-1478, 2001.
40. Redick JA, Jakoby WB, Baron J. Immunohistochemical localization of glutathione S-transferases in livers of untreated rats. J Biol Chem 257: 15200-15203, 1982.
41. Reichel C, Gao B, Van Montfoort J, Cattori V, Rahner C, Hagenbuch B, Stieger B, Kamisako T, Meier PJ. Localization and function of the organic anion-transporting polypeptide Oatp2 in rat liver. Gastroenterology 117: 688-695, 1999.
42. Rius M, Nies AT, Hummel-Eisenbeiss J, Jedlitschky G, Keppler D. Cotransport of reduced glutathione with bile salts by MRP4 (ABCC4) localized to the basolateral hepatocyte membrane. Hepatology 38: 374-384, 2003.
43. Rost D, Herrmann T, Sauer P, Schmidts HL, Stieger B, Meier PJ, Stremmel W, Stiehl A. Regulation of rat organic anion transporters in bile salt-induced cholestatic hepatitis: effect of ursodeoxycholate. Hepatology 38: 187-195, 2003.
44. Sasamoto T, Sano N, Takikawa H. Biliary excretion of sulfated bile acids and organic anions in zone 1- and zone 3-injured rats. J Gastroenterol Hepatol 21: 26-31, 2006.
45. Schmitt M, Kubitz R, Lizun S, Wettstein M, Häussinger D. Regulation of the dynamic localization of the rat Bsep gene-encoded bile salt export pump by anisoosmolarity. Hepatology 33: 509-518, 2001.
46. Soroka CJ, Lee JM, Azzaroli F, Boyer J. Cellular localization and up-regulation of multidrug resistance-associated protein 3 in hepatocytes and cholangiocytes during obstructive cholestasis in rat liver. Hepatology 33: 783-791, 2001.
47. Staudinger JL, Goodwin B, Jones SA, Hawkins-Brown D, MacKenzie KI, LaTour A, Liu Y, Klaassen CD, Brown KK, Reinhard J, Willson TM, Koller BH, Kliewer SA. The nuclear receptor PXR is a lithocholic acid sensor that protects against liver toxicity. Proc Natl Acad Sci USA 98: 3369-3374, 2001.
48. Stedman CA, Liddle C, Coulter SA, Sonoda J, Alvarez JG, Moore DD, Evans RM, Downes M. Nuclear receptors constitutive androstane receptor and pregnane X receptor ameliorate cholestatic liver injury. Proc Natl Acad Sci USA 98: 2063-2068, 2005.
49. Stedman CA, Liddle C, Coulter S, Sonoda J, Alvarez JG, Evans RM, Downes M. Benefit of farnesoid X receptor inhibition in obstructive cholestasis. Proc Natl Acad Sci USA 103: 11323-11328, 2006.
50. Takikawa H, Sano N, Onishi T, Toda A, Tanaka H, Hojo M, Marumo T, Hanawa N, Tachizawa H, Nishikawa K. Biliary excretion of taurolithocholate-sulfate and temocaprilat in cholestatic rats induced by bile duct-ligation and ethinylestradiol. Hepatol Res 24: 136-140, 2002.
51. Tan E, Pang KS. Sulfation is rate limiting in the futile cycling between estrone and estrone sulfate in enriched periportal and perivenous rat hepatocytes. Drug Metab Dispos 29: 335-346, 2001.
52. Twisk J, Hoekman MF, Mager WH, Moorman AF, de Boer PA, Scheja L, Princen HM, Gebhardt R. Heterogeneous expression of cholesterol 7 alpha-hydroxylase and sterol 27-hydroxylase genes in the rat liver lobulus. J Clin Invest 95: 1235-1243, 1995.
53. Vanhaecke T, Lindros KO, Oinonen T, Vercruysse A, Rogiers V. Effect of long-term ethanol exposure on the acinar distribution of hepatic glutathione S-transferase. Drug Metab Dispos 28: 1470-1474, 2000.
54. Zollner G, Fickert P, Fuchsbichler A, Silbert D, Wagner M, Arbeiter S, Gonzalez FJ, Marschall HU, Zatloukal K, Denk H, Trauner M. Role of nuclear bile acid receptor, FXR, in adaptive ABC transporter regulation by cholic and ursodeoxycholic acid in mouse liver, kidney and intestine. J Hepatol 39: 480-488, 2003.
55. Zollner G, Wagner M, Fickert P, Geier A, Fuchsbichler A, Silbert D, Gumhold J, Zatloukal K, Kaser A, Tilg H, Denk H, Trauner M. Role of nuclear receptors and hepatocyte-enriched transcription factors for Ntcp repression in biliary obstruction in mouse liver. Am J Physiol Gastrointest Liver Physiol 289: G798-G805, 2005.