Trafficking of the Bile Salt Export Pump from the Golgi to the Canalicular Membrane Is Regulated by the p38 MAP Kinase

Gastroenterology

Volumn 126, Issue 2, 2004, Pages 541-553

  Kubitz, Ralf ^a   Sütfels, Gerrit ^a   Kühlkamp, Thomas ^a   Kölling, Ralf ^a   Häussinger, Dieter ^a  

^a HEINRICH HEINE UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

12 (2 CYANOETHYL) 6,7,12,13 TETRAHYDRO 13 METHYL 5 OXOINDOLO[2,3 A]PYRROLO[3,4 C]CARBAZOLE; 2 [1 (3 DIMETHYLAMINOPROPYL) 3 INDOLYL] 3 (3 INDOLYL)MALEIMIDE; BILE SALT; BILE SALT EXPORT PUMP; CALCIUM ION; CARRIER PROTEIN; CYCLOHEXIMIDE; ISOPROTEIN; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN KINASE C; TAUROCHOLIC ACID; TAUROURSOCHOLIC ACID; UNCLASSIFIED DRUG;

ARTICLE; BILE SECRETION; CELL ISOLATION; CELL STRAIN HEPG2; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME REGULATION; GOLGI COMPLEX; HUMAN; HUMAN CELL; INTRAHEPATIC BILE DUCT; MICROTUBULE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION;

EID: 0842299393     PISSN: 00165085     EISSN: None     Source Type: Journal    
DOI: 10.1053/j.gastro.2003.11.003     Document Type: Article

References (51)

1. Trauner M, Meier PJ, Boyer JL. Molecular pathogenesis of cholestasis. N Engl J Med 1998;339:1217-1227.
2. Kubitz R, Warskulat U, Schmitt M, Häussinger D. Dexamethasone- and osmolarity-dependent expression of the multidrug-resistance protein 2 in cultured rat hepatocytes. Biochem J 1999; 340:585-591.
3. Häussinger D, Schmitt M, Weiergraber O, Kubitz R. Short-term regulation of canalicular transport. Semin Liver Dis 2000;20: 307-321.
4. Kubitz R, Wettstein M, Warskulat U, Häussinger D. Regulation of the multidrug resistance protein 2 in the rat liver by lipopolysaccharide and dexamethasone. Gastroenterology 1999;116:401-410.
5. Kubitz R, D' Urso D, Keppler D, Häussinger D. Osmodependent dynamic localization of the multidrug resistance protein 2 in the rat hepatocyte canalicular membrane. Gastroenterology 1997; 113:1438-1442.
6. Noé J, Hagenbuch B, Meier PJ, St Pierre MV. Characterization of the mouse bile salt export pump overexpressed in the baculovirus system. Hepatology 2001;33:1223-1231.
7. Gerloff T, Stieger B, Hagenbuch B, Madon J, Landmann L, Roth J, Hofmann AF, Meier PJ. The sister of P-glycoprotein represents the canalicular bile salt export pump of mammalian liver. J Biol Chem 1998;273:10046-10050.
8. Strautnieks SS, Bull LN, Knisely AS, Kocoshis SA, Dahl N, Arnell H, Sokal E, Dahan K, Childs S, Ling V, Tanner MS, Kagalwalla AF, Nemeth A, Pawlowska J, Baker A, Mieli-Vergani G, Freimer NB, Gardiner RM, Thompson RJ. A gene encoding a liver-specific ABC transporter is mutated in progressive familial intrahepatic cholestasis. Nat Genet 1998;20:233-238.
9. Hartmann G, Cheung AK, Piquette-Miller M. Inflammatory cytokines, but not bile acids, regulate expression of murine hepatic anion transporters in endotoxemia. J Pharmacol Exp Ther 2002; 303:273-281.
10. Hyogo H, Tazuma S, Nishioka T, Ochi H, Yamaguchi A, Numata Y, Kanno K, Sakomoto M, Asamoto Y, Tsuboi K, Nakai K, Yasumiba S, Sunami Y, Kajiyama G. Phospholipid alterations in hepatocyte membranes and transporter protein changes in cholestatic rat model. Dig Dis Sci 2001;46:2089-2097.
11. Micheline D, Emmanuel J, Serge E. Effect of ursodeoxycholic acid on the expression of the hepatocellular bile acid transporters (Ntcp and bsep) in rats with estrogen-induced cholestasis. J Pediatr Gastroenterol Nutr 2002;35:185-191.
12. Warskulat U, Kubitz R, Wettstein M, Stieger B, Meier PJ, Häussinger D. Regulation of bile salt export pump mRNA levels by dexamethasone and osmolarity in cultured rat hepatocytes. Biol Chem 1999;380:1273-1279.
13. 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 2001;33: 509-518.
14. Kurz AK, Graf D, Schmitt M, vom Dahl S, Häussinger D. Tauroursodesoxycholate-induced choleresis involves p38(MAPK) activation and translocation of the bile salt export pump in rats. Gastroenterology 2001;121:407-419.
15. Paumgartner G, Beuers U. Ursodeoxycholic acid in cholestatic liver disease: mechanisms of action and therapeutic use revisited. Hepatology 2002;36:525-531.
16. Noé B, Schliess F, Wettstein M, Heinrich S, Häussinger D. Regulation of taurocholate excretion by a hypo-osmolarity-activated signal transduction pathway in rat liver. Gastroenterology 1996; 110:858-865.
17. Schliess F, Kurz AK, vom Dahl S, Häussinger D. Mitogen-activated protein kinases mediate the stimulation of bile acid secretion by tauroursodeoxycholate in rat liver. Gastroenterology 1997;113:1306-1314.
18. Widmann C, Gibson S, Jarpe MB, Johnson GL. Mitogen-activated protein kinase: conservation of a three-kinase module from yeast to human. Physiol Rev 1999;79:143-180.
19. Gatmaitan ZC, Nies AT, Arias IM. Regulation and translocation of ATP-dependent apical membrane proteins in rat liver. Am J Physiol 1997;272:G1041-G1049.
20. Roelofsen H, Ottenhoff R, Oude Elferink RP, Jansen PL. Hepatocanalicular organic-anion transport is regulated by protein kinase C. Biochem J 1991;278:637-641.
21. Corasanti JG, Smith ND, Gordon ER, Boyer JL. Protein kinase C agonists inhibit bile secretion independently of effects on the microcirculation in the isolated perfused rat liver. Hepatology 1989;10:8-13.
22. Beuers U, Probst I, Soroka C, Boyer JL, Kullak-Ublick GA, Paumgartner G. Modulation of protein kinase C by taurolithocholic acid in isolated rat hepatocytes. Hepatology 1999;29:477-482.
23. Beuers U, Throckmorton DC, Anderson MS, Isales CM, Thasler W, Kullak-Ublick GA, Sauter G, Koebe HG, Paumgartner G, Boyer JL. Tauroursodeoxycholic acid activates protein kinase C in isolated rat hepatocytes. Gastroenterology 1996;110: 1553-1563.
24. Kubitz R, Huth C, Schmitt M, Horbach A, Kullak-Ublick GA, Haussinger D. Protein kinase C-dependent distribution of the multidrug resistance protein 2 from the canalicular to the basolateral membrane in human HepG2 cells. Hepatology 2001;34:340-350.
25. Beuers U, Bilzer M, Chittattu A, Kullak-Ublick GA, Keppler D, Paumgartner G, Dombrowski F. Tauroursodeoxycholic acid inserts the apical conjugate export pump, Mrp2, into canalicular membranes and stimulates organic anion secretion by protein kinase C-dependent mechanisms in cholestatic rat liver. Hepatology 2001;33:1206-1216.
26. Kipp H, Arias IM. Intracellular trafficking and regulation of canalicular ATP-binding cassette transporters. Semin Liver Dis 2000; 20:339-351.
27. Roelofsen H, Soroka CJ, Keppler D, Boyer JL. Cyclic AMP stimulates sorting of the canalicular organic action transporter (Mrp2/cMoat) to the apical domain in hepatocyte couplets. J Cell Sci 1998;111:1137-1145.
28. Hipfner DR, Gao M, Scheffer G, Scheper RJ, Deeley RG, Cole SP. Epitope mapping of monoclonal antibodies specific for the 190-kDa multidrug resistance protein (MRP). Br J Cancer 1998;78: 1134-1140.
29. +-taurocholate cotransporting green fluorescent protein in human hepatoblastome HepG2 cells. Cytotechnology 2000;34:1-9.
30. Nakamura N, Rabouille C, Watson R, Nilsson T, Hui N, Slusarewicz P, Kreis TE, Warren G. Characterization of a cis-Golgi matrix protein, GM130. J Cell Biol 1995;131:1715-1726.
31. Felicetti L, Colombo B, Baglioni C. Inhibition of protein synthesis in reticulocytes by antibiotics. II. The site of action of cycloheximide, streptovitacin A and pactamycin. Biochim Biophys Acta 1966;119:120-129.
32. Stanners CP. The effect of cycloheximide on polyribosomes from hamster cells. Biochem Biophys Res Commun 1966;22:758-764.
33. Kim YH, Choi MR, Song DK, Huh SO, Jang CG, Suh HW. Regulation of c-fos gene expression by lipopolysaccharide and cycloheximide in C6 rat glioma cells. Brain Res 2000;872:227-230.
34. Lin WW, Hsu YW. Cycloheximide-induced cPLA(2) activation is via the MKP-1 down-regulation and ERK activation. Cell Signal 2000; 12:457-461.
35. Kato K, Ito H, Kamei K, Iwamoto I. Selective stimulation of Hsp27 and κB-crystallin but not Hsp70 expression by p38 MAP kinase activation. Cell Stress Chaperones 1999;4:94-101.
36. Wustner D, Mukhedee S, Maxfield FR, Müller P, Herrmann A. Vesicular and nonvesicular transport of phosphatidylcholine in polarized HepG2 cells. Traffic 2001;2:277-296.
37. Zegers MM, Hoekstra D. Sphingolipid transport to the apical plasma membrane domain in human hepatoma cells is controlled by PKC and PKA activity: a correlation with cell polarity in HepG2 cells. J Cell Biol 1997;138:307-321.
38. Roelofsen H, Vos TA, Schippers IJ, Kuipers F, Koning H, Moshage H, Jansen PL, Müller M. Increased levels of the multidrug resistance protein in lateral membranes of proliferating hepatocyte-derived cells. Gastroenterology 1997;112:511-521.
39. Lee G, Piquette-Miller M. Influence of IL-6 on MDR and MRP-mediated multidrug resistance in human hepatoma cells. Can J Physiol Pharmacol 2001;79:876-884.
40. 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 2000;278:G522-G531.
41. Schrenk D, Baus PR, Ermel N, Klein C, Vorderstemann B, Kauffmann HM. Up-regulation of transporters of the MRP family by drugs and toxins. Toxicol Lett 2001;120:51-57.
42. Kipp H, Arias IM. Newly synthesized canalicular ABC transporters are directly targeted from the Golgi to the hepatocyte apical domain in rat liver. J Biol Chem 2000;275:15917-15925.
43. Sai Y, Nies AT, Arias IM. Bile acid secretion and direct targeting of mdrl-green fluorescent protein from Golgi to the canalicular membrane in polarized WIF-B cells. J Cell Sci 1999;112:4535-4545.
44. Kipp H, Pichetshote N, Arias IM. Transporters on demand. Intrahepatic pools of canalicular ATP binding cassette transporters in rat liver. J Biol Chem 2001;276:7218-7224.
45. Wang L, Soroka CJ, Boyer JL. The role of bile salt export pump mutations in progressive familial intrahepatic cholestasis type II. J Clin Invest 2002;110:965-972.
46. Stokoe D, Engel K, Campbell DG, Cohen P, Gaestel M. Identification of MAPKAP kinase 2 as a major enzyme responsible for the phosphorylation of the small mammalian heat shock proteins. FEBS Lett 1992;313:307-313.
47. Ducher L, Croquet F, Gil S, Davy J, Feger J, Brehier A. Differential expression of five protein kinase C isoenzymes in FAO and HepG2 hepatoma cell lines compared with normal rat hepatocytes. Biochem Biophys Res Commun 1995;217:546-553.
48. Duronio V, Huber BE, Jacobs S. Partial down-regulation of protein kinase C reverses the growth inhibitory effect of phorbol esters on HepG2 cells. J Cell Physiol 1990;145:381-389.
49. Schuringa JJ, Dekker LV, Vellenga E, Kruijer W. Sequential activation of Rac-1, SEK-1/MKK-4, and protein kinase Cδ is required for interleukin-6-induced STAT3 Ser-727 phosphorylation and transactivation. J Biol Chem 2001;276:27709-27715.
50. Gekeler V, Boer R, Uberall F, Ise W, Schubert C, Utz I, Hofmann J, Sanders KH, Schächtele C, Klemm K, Grunicke H. Effects of the selective bisindolylmaleimide protein kinase C inhibitor GF 109203X on P-glycoprotein-mediated multidrug resistance. Br J Cancer 1996;74:897-905.
51. Martiny-Baron G, Kazanietz MG, Mischak H, Blumberg PM, Kochs G, Hug H, Marme D, Schächtele C. Selective inhibition of protein kinase C isozymes by the indolocarbazole Gö 6976. J Biol Chem 1993;268:9194-9197.