Type 2 inositol 1,4,5-trisphosphate receptor modulates bile salt export pump activity in rat hepatocytes

Hepatology

Volumn 54, Issue 5, 2011, Pages 1790-1799

  Kruglov, Emma A ^a   Gautam, Samir ^a   Guerra, Mateus T ^a   Nathanson, Michael H ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; BILE SALT; BILE SALT EXPORT PUMP; CALCIUM ION; CHOLESTEROL; CHOLYLGLYCYLAMIDO FLUORESCEIN; FLUORESCEIN; INOSITOL 1,4,5 TRISPHOSPHATE RECEPTOR; INOSITOL 1,4,5 TRISPHOSPHATE TYPE 2 RECEPTOR; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; XESTOSPONGIN C;

ANIMAL EXPERIMENT; ARTICLE; BILE DUCT; CALCIUM SIGNALING; CELL MEMBRANE; CHOLESTASIS; IMMUNOFLUORESCENCE; IN VITRO STUDY; LIVER CELL; MALE; NONHUMAN; PRIORITY JOURNAL; RAT;

ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; BILE ACIDS AND SALTS; BILE CANALICULI; CALCIUM; CALCIUM SIGNALING; CELL CULTURE TECHNIQUES; CELLS, CULTURED; CHOLESTASIS; COLLAGEN; DISEASE MODELS, ANIMAL; HEPATOCYTES; INOSITOL 1,4,5-TRISPHOSPHATE RECEPTORS; LIPOPOLYSACCHARIDES; MALE; PROTEIN PROCESSING, POST-TRANSLATIONAL; RATS; RATS, SPRAGUE-DAWLEY;

EID: 80055050290     PISSN: 02709139     EISSN: 15273350     Source Type: Journal    
DOI: 10.1002/hep.24548     Document Type: Article

References (49)

1. Trauner M, Meier PJ, Boyer JL. Molecular pathogenesis of cholestasis. N Engl J Med 1998; 339: 1217-1227.
2. Kullak-Ublick GA, Stieger B, Hagenbuch B, Meier PJ. Hepatic transport of bile salts. Semin Liver Dis 2000; 20: 273-292.
3. 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 2001; 276: 28857-28865.
4. 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.
5. Boyer JL, Soroka CJ. Vesicle targeting to the apical domain regulates bile excretory function in isolated rat hepatocyte couplets. Gastroenterology 1995; 109: 1600-1611.
6. Misra S, Varticovski L, Arias IM. Mechanisms by which cAMP increases bile acid secretion in rat liver and canalicular membrane vesicles. Am J Physiol Gastrointest Liver Physiol 2003; 285: G316-324.
7. Dombrowski F, Stieger B, Beuers U. Tauroursodeoxycholic acid inserts the bile salt export pump into canalicular membranes of cholestatic rat liver. Lab Invest 2006; 86: 166-174.
8. Kurz AK, Graf D, Schmitt M, Vom Dahl S, Haussinger D. Tauroursodesoxycholate-induced choleresis involves p38(MAPK) activation and translocation of the bile salt export pump in rats. Gastroenterology 2001; 121: 407-419.
9. Wimmer R, Hohenester S, Pusl T, Denk GU, Rust C, Beuers U. Tauroursodeoxycholic acid exerts anticholestatic effects by a cooperative cPKC alpha-/PKA-dependent mechanism in rat liver. Gut 2008; 57: 1448-1454.
10. Sudhof TC, Rothman JE. Membrane fusion: grappling with SNARE and SM proteins. Science 2009; 323: 474-477.
11. Hirata K, Dufour JF, Shibao K, Knickelbein R, O'Neill AF, Bode HP, et al. Regulation of Ca(2+) signaling in rat bile duct epithelia by inositol 1, 4, 5-trisphosphate receptor isoforms. HEPATOLOGY 2002; 36: 284-296.
12. Matovcik LM, Maranto AR, Soroka CJ, Gorelick FS, Smith J, Goldenring JR. Co-distribution of calmodulin-dependent protein kinase II and inositol trisphosphate receptors in an apical domain of gastrointestinal mucosal cells. J Histochem Cytochem 1996; 44: 1243-1250.
13. Leite MF, Burgstahler AD, Nathanson MH. Ca2+ waves require sequential activation of inositol 1, 4, 5-trisphosphate receptors and ryanodine receptors in pancreatic acinar cells. Gastroenterology 2002; 122: 415-427.
14. Nathanson MH, Padfield PJ, O'Sullivan AJ, Burgstahler AD, Jamieson JD. Mechanism of Ca2+ wave propagation in pancreatic acinar cells. J Biol Chem 1992; 267: 18118-18121.
15. Fitz JG, Basavappa S, McGill J, Melhus O, Cohn JA. Regulation of membrane chloride currents in rat bile duct epithelial cells. J Clin Invest 1993; 91: 319-328.
16. Hirata K, Pusl T, O'Neill AF, Dranoff JA, Nathanson MH. The type II inositol 1, 4, 5-trisphosphate receptor can trigger Ca2+ waves in rat hepatocytes. Gastroenterology 2002; 122: 1088-1100.
17. Bruck R, Nathanson MH, Roelofsen H, Boyer JL. Effects of protein kinase C and cytosolic Ca2+ on exocytosis in the isolated perfused rat liver. HEPATOLOGY 1994; 20: 1032-1040.
18. Nathanson MH, Gautam A, Bruck R, Isales CM, Boyer JL. Effects of Ca2+ agonists on cytosolic Ca2+ in isolated hepatocytes and on bile secretion in the isolated perfused rat liver. HEPATOLOGY 1992; 15: 107-116.
19. Beuers U, Nathanson MH, Isales CM, Boyer JL. Tauroursodeoxycholic acid stimulates hepatocellular exocytosis by mobilization of extracellular Ca++, a mechanism defective in cholestasis. J Clin Invest 1993; 92: 2984-2993.
20. Clapham DE. Calcium signaling. Cell 2007; 131: 1047-1058.
21. Wojcikiewicz RJ. Type I, II, and III inositol 1, 4, 5-trisphosphate receptors are unequally susceptible to down-regulation and are expressed in markedly different proportions in different cell types. J Biol Chem 1995; 270: 11678-11683.
22. Cruz LN, Guerra MT, Kruglov E, Mennone A, Garcia CR, Chen J, et al. Regulation of multidrug resistance-associated protein 2 by calcium signaling in mouse liver. HEPATOLOGY 2010; 52: 327-337.
23. Nagata J, Guerra MT, Shugrue CA, Gomes DA, Nagata N, Nathanson MH. Lipid rafts establish calcium waves in hepatocytes. Gastroenterology 2007; 133: 256-267.
24. Cai SY, Gautam S, Nguyen T, Soroka CJ, Rahner C, Boyer JL. ATP8B1 deficiency disrupts the bile canalicular membrane bilayer structure in hepatocytes, but FXR expression and activity are maintained. Gastroenterology 2009; 136: 1060-1069.
25. Holzinger F, Schteingart CD, Ton-Nu HT, Eming SA, Monte MJ, Hagey LR, et al. Fluorescent bile acid derivatives: relationship between chemical structure and hepatic and intestinal transport in the rat. HEPATOLOGY 1997; 26: 1263-1271.
26. Nathanson MH, Burgstahler AD, Mennone A, Dranoff JA, Rios-Velez L. Stimulation of bile duct epithelial secretion by glybenclamide in normal and cholestatic rat liver. J Clin Invest 1998; 101: 2665-2676.
27. Shibao K, Hirata K, Robert ME, Nathanson MH. Loss of inositol 1, 4, 5-trisphosphate receptors from bile duct epithelia is a common event in cholestasis. Gastroenterology 2003; 125: 1175-1187.
28. Wang W, Soroka CJ, Mennone A, Rahner C, Harry K, Pypaert M, et al. Radixin is required to maintain apical canalicular membrane structure and function in rat hepatocytes. Gastroenterology 2006; 131: 878-884.
29. Gerloff T, Steiger B, Hagenbuch B, Madon J, Landmann L, Roth J, et al. The sister of p-glycoprotein represents the canalicular bile salt export pump of mammalian liver. J Biol Chem 1998; 273: 10046-10050.
30. Wojcikiewicz RJ, He Y. Type I, II and III inositol 1, 4, 5-trisphosphate receptor co-immunoprecipitation as evidence for the existence of heterotetrameric receptor complexes. Biochem Biophys Res Commun 1995; 213: 334-341.
31. Trauner M, Arrese M, Soroka CJ, Ananthanarayanan M, Koeppel TA, Schlosser SF, et al. The rat canalicular conjugate export pump (mrp2) is down-regulated in intrahepatic and obstructive cholestasis. Gastroenterology 1997; 113: 255-264.
32. Gafni J, Munsch JA, Lam TH, Catlin MC, Costa LG, Molinski TF, et al. Xestospongins: potent membrane permeable blockers of the inositol 1, 4, 5-trisphosphate receptor. Neuron 1997; 19: 723-733.
33. Crocenzi FA, Mottino AD, Cao J, Veggi LM, Pozzi EJ, Vore M, et al. Estradiol-17beta-D-glucuronide induces endocytic internalization of Bsep in rats. Am J Physiol Gastrointest Liver Physiol 2003; 285: G449-459.
34. Elferink MG, Olinga P, Draaisma AL, Merema MT, Faber KN, Slooff MJ, et al. LPS-induced downregulation of MRP2 and BSEP in human liver is due to a posttranscriptional process. Am J Physiol Gastrointest Liver Physiol 2004; 287: G1008-1016.
35. Augustine GJ, Santamaria F, Tanaka K. Local calcium signaling in neurons. Neuron 2003; 40: 331-346.
36. Fadool DA, Ache BW. Plasma membrane inositol 1, 4, 5-trisphosphate-activated channels mediate signal transduction in lobster olfactory receptor neurons. Neuron 1992; 9: 907-918.
37. Wakabayashi Y, Lippincott-Schwartz J, Arias IM. Intracellular trafficking of bile salt export pump (ABCB11) in polarized hepatic cells: constitutive cycling between the canalicular membrane and rab11-positive endosomes. Mol Biol Cell 2004; 15: 3485-3496.
38. 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 2000; 118: 163-172.
39. Kubitz R, Wettstein M, Warskulat U, Haussinger D. Regulation of the multidrug resistance protein 2 in the rat liver by lipopolysaccharide and dexamethasone. Gastroenterology 1999; 116: 401-410.
40. 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.
41. Mottino AD, Cao J, Veggi LM, Crocenzi F, Roma MG, Vore M. Altered localization and activity of canalicular Mrp2 in estradiol-17beta-D-glucuronide-induced cholestasis. HEPATOLOGY 2002; 35: 1409-1419.
42. Beuers U, Nathanson MH, Boyer JL. Effects of tauroursodeoxycholic acid on cytosolic Ca2+ signals in isolated rat hepatocytes. Gastroenterology 1993; 104: 604-612.
43. Minagawa N, Nagata J, Shibao K, Masyuk AI, Gomes DA, Rodrigues MA, et al. Cyclic AMP regulates bicarbonate secretion in cholangiocytes through release of ATP into bile. Gastroenterology 2007; 133: 1592-1602.
44. Pani B, Singh BB. Lipid rafts/caveolae as microdomains of calcium signaling. Cell Calcium 2009; 45: 625-633.
45. Weaver AK, Olsen ML, McFerrin MB, Sontheimer H. BK channels are linked to inositol 1, 4, 5-triphosphate receptors via lipid rafts: a novel mechanism for coupling [Ca(2+)](i) to ion channel activation. J Biol Chem 2007; 282: 31558-31568.
46. Rosado JA, Sage SO. Coupling between inositol 1, 4, 5-trisphosphate receptors and human transient receptor potential channel 1 when intracellular Ca2+ stores are depleted. Biochem J 2000; 350 Pt 3: 631-635.
47. Murata T, Lin MI, Stan RV, Bauer PM, Yu J, Sessa WC. Genetic evidence supporting caveolae microdomain regulation of calcium entry in endothelial cells. J Biol Chem 2007; 282: 16631-16643.
48. Prakash YS, Thompson MA, Vaa B, Matabdin I, Peterson TE, He T, et al. Caveolins and intracellular calcium regulation in human airway smooth muscle. Am J Physiol Lung Cell Mol Physiol 2007; 293: L1118-1126.
49. Weerth SH, Holtzclaw LA, Russell JT. Signaling proteins in raft-like microdomains are essential for Ca2+ wave propagation in glial cells. Cell Calcium 2007; 41: 155-167.