Sequential Activation of Classic PKC and Estrogen Receptor α Is Involved in Estradiol 17ß-D-Glucuronide-Induced Cholestasis

PLoS ONE

Volumn 7, Issue 11, 2012, Pages

  Barosso, Ismael R ^a   Zucchetti, Andrés E ^a   Boaglio, Andrea C ^a   Larocca, M Cecilia ^a   Taborda, Diego R ^a   Luquita, Marcelo G ^a   Roma, Marcelo G ^a   Crocenzi, Fernando A ^a   Sánchez Pozzi, Enrique J ^a  

^a UNIVERSIDAD NACIONAL DE ROSARIO   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

CARRIER PROTEIN; DINITROPHENYLGLUTATHIONE; ESTRADIOL 17 GLUCURONIDE; ESTROGEN RECEPTOR ALPHA; FLUORESCEIN; GLUTATHIONE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN ABCB11; PROTEIN ABCC2; PROTEIN KINASE C; TAUROCHOLIC ACID; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BILE FLOW; CELL PROTECTION; CHOLESTASIS; CONTROLLED STUDY; ENZYME ACTIVATION; FEMALE; INTERNALIZATION; INTRAHEPATIC BILE DUCT; LIVER CELL; LIVER PERFUSION; NONHUMAN; PROTEIN LOCALIZATION; RAT;

ANIMALS; CARBAZOLES; CELLS, CULTURED; CHOLESTASIS; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; FEMALE; HEPATOCYTES; LIVER; PROTEIN KINASE C; RATS; RATS, WISTAR;

RATTUS;

EID: 84870284019     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0050711     Document Type: Article

References (47)

1. Gatmaitan ZC, Arias IM, (1995) ATP-dependent transport systems in the canalicular membrane of the hepatocyte. Physiol Rev 75: 261-275.
2. Borst P, Elferink RO, (2002) Mammalian ABC transporters in health and disease. Annu Rev Biochem 71: 537-592.
3. Esteller A, (2008) Physiology of bile secretion. World J Gastroenterol 14: 5641-5649.
4. Crocenzi F, Mottino A, Roma M, (2004) Regulation of synthesis and trafficking of canalicular transporters and its alteration in acquired hepatocellular cholestasis: Experimental therapeutic strategies for its prevention. Curr Med Chem 11: 501-524.
5. Vore M, Liu Y, Huang L, (1997) Cholestatic properties and hepatic transport of steroid glucuronides. Drug Metabol Rev 29: 183-203.
6. Adlercreutz H, Tikkanen MJ, Wichmann K, Svanborg A, Anberg A, (1974) Recurrent jaundice in pregnancy. IV. Quantitative determination of urinary and biliary estrogens, including studies in pruritus gravidarum. J Clin Endocrinol Metab 38: 51-57.
7. Crocenzi FA, Mottino AD, Cao J, Veggi LM, Sanchez Pozzi EJ, et al. (2003) Estradiol-17-ßD-glucuronide induces endocytic internalization of Bsep in rats. Am J Physiol Gastrointest Liver Physiol 285: G449-G459.
8. Mottino AD, Crocenzi FA, Pozzi EJ, Veggi LM, Roma MG, et al. (2005) Role of microtubules in estradiol-17beta-D-glucuronide-induced alteration of canalicular Mrp2 localization and activity. Am J Physiol Gastrointest Liver Physiol 288: G327-G336.
9. Mottino AD, Cao J, Veggi LM, Crocenzi FA, Roma MG, et al. (2002) Altered localization and activity of canalicular Mrp2 in estradiol-17ß-D-glucuronide-induced cholestasis. Hepatology 35: 1409-1419.
10. Kubitz R, Saha N, Kuhlkamp T, Dutta S, vom Dahl S, et al. (2004) Ca2+-dependent protein kinase C-isoforms induce cholestasis in rat liver. J Biol Chem 279: 10323-10330.
11. Perez LM, Milkiewicz P, Ahmed-Choudhury J, Elias E, Ochoa JE, et al. (2006) Oxidative stress induces actin-cytoskeletal and tight-junctional alterations in hepatocytes by a Ca2+-dependent, PKC-mediated mechanism: protective effect of PKA. Free Radic Biol Med 40: 2005-2017.
12. Crocenzi FA, Sanchez Pozzi EJ, Ruiz ML, Zucchetti AE, Roma MG, et al. (2008) Ca(2+)-dependent protein kinase C isoforms are critical to estradiol 17beta-D-glucuronide-induced cholestasis in the rat. Hepatology 48: 1885-1895.
13. Boaglio AC, Zucchetti AE, Sanchez Pozzi EJ, Pellegrino JM, Ochoa JE, et al. (2010) Phosphoinositide 3-kinase/protein kinase B signaling pathway is involved in estradiol 17beta-D-glucuronide-induced cholestasis: complementarity with classical protein kinase C. Hepatology 52: 1465-1476.
14. Beuers U, Denk GU, Soroka CJ, Wimmer R, Rust C, et al. (2003) Taurolithocholic acid exerts cholestatic effects via phosphatidylinositol 3-kinase-dependent mechanisms in perfused rat livers and rat hepatocyte couplets. J Biol Chem 278: 17810-17818.
15. Guo RX, Wei LH, Tu Z, Sun PM, Wang JL, et al. (2006) 17 beta-estradiol activates PI3K/Akt signaling pathway by estrogen receptor (ER)-dependent and ER-independent mechanisms in endometrial cancer cells. J Steroid Biochem Mol Biol 99: 9-18.
16. Marino M, Pallottini V, Trentalance A, (1998) Estrogens cause rapid activation of IP3-PKC-alpha signal transduction pathway in HEPG2 cells. Biochem Biophys Res Commun 245: 254-258.
17. Acconcia F, Kumar R, (2006) Signaling regulation of genomic and nongenomic functions of estrogen receptors. Cancer Lett 238: 1-14.
18. Kuiper GG, Carlsson B, Grandien K, Enmark E, Haggblad J, et al. (1997) Comparison of the ligand binding specificity and transcript tissue distribution of estrogen receptors alpha and beta. Endocrinology 138: 863-870.
19. Tollefsen KE, Mathisen R, Stenersen J, (2002) Estrogen mimics bind with similar affinity and specificity to the hepatic estrogen receptor in Atlantic salmon (Salmo salar) and rainbow trout (Oncorhynchus mykiss). Gen Comp Endocrinol 126: 14-22.
20. Crocenzi FA, Mottino AD, Sanchez Pozzi EJ, Pellegrino JM, Rodríguez Garay EA, et al. (2003) Impaired localisation and transport function of canalicular Bsep in taurolithocholate-induced cholestasis in the rat. Gut 52: 1170-1177.
21. Gautam A, Ng OC, Boyer JL, (1987) Isolated rat hepatocyte couplets in short-term culture: structural characteristics and plasma membrane reorganization. Hepatology 7: 216-223.
22. Wilton JC, Williams DE, Strain AJ, Parslow RA, Chipman JK, et al. (1991) Purification of hepatocyte couplets by centrifugal elutriation. Hepatology 14: 180-183.
23. Maglova LM, Jackson AM, Meng XJ, Carruth MW, Schteingart CD, et al. (1995) Transport characteristics of three fluorescent conjugated bile acid analogs in isolated rat hepatocytes and couplets. Hepatology 22: 637-647.
24. Wang L, Soroka CJ, Boyer JL, (2002) The role of bile salt export pump mutations in progressive familial intrahepatic cholestasis type II. J Clin Invest 110: 965-972.
25. Roelofsen H, Soroka CJ, Keppler D, Boyer JL, (1998) Cyclic AMP stimulates sorting of the canalicular organic anion transporter (Mrp2/cMoat) to the apical domain in hepatocyte couplets. J Cell Sci 111: 1137-1145.
26. Roma MG, Milkiewicz P, Elias E, Coleman R, (2000) Control by signaling modulators of the sorting of canalicular transporters in rat hepatocyte couplets: role of the cytoskeleton. Hepatology 32: 1342-1356.
27. Le Goff P, Montano MM, Schodin DJ, Katzenellenbogen BS, (1994) Phosphorylation of the human estrogen receptor. Identification of hormone-regulated sites and examination of their influence on transcriptional activity. J Biol Chem 269: 4458-4466.
28. Garcia F, Kierbel A, Larocca MC, Gradilone SA, Splinter P, et al. (2001) The water channel aquaporin-8 is mainly intracellular in rat hepatocytes, and its plasma membrane insertion is stimulated by cyclic AMP. J Biol Chem 276: 12147-12152.
29. Carreras FI, Gradilone SA, Mazzone A, Garcia F, Huang BQ, et al. (2003) Rat hepatocyte aquaporin-8 water channels are down-regulated in extrahepatic cholestasis. Hepatology 37: 1026-1033.
30. Lowry OH, Rosembrough NJ, Farr AL, Randall RJ, (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193: 265-275.
31. Newton AC, (2003) Regulation of the ABC kinases by phosphorylation: protein kinase C as a paradigm. Biochem J 370: 361-371.
32. Yuan B, Latek R, Hossbach M, Tuschl T, Lewitter F, (2004) siRNA Selection Server: an automated siRNA oligonucleotide prediction server. Nucleic Acids Res 32: W130-W134.
33. Aranda V, Martinez I, Melero S, Lecanda J, Banales JM, et al. (2004) Shared apical sorting of anion exchanger isoforms AE2a, AE2b1, and AE2b2 in primary hepatocytes. Biochem Biophys Res Commun 319: 1040-1046.
34. Mottino AD, Hoffman T, Jennes L, Cao J, Vore M, (2001) Expression of multidrug resistance-associated protein 2 in small intestine from pregnant and postpartum rats. Am J Physiol Gastrointest Liver Physiol 280: G1261-G1273.
35. Talalay P, (1960) Enzymatic analysis of steroid hormones. Methods Biochem Anal 8: 119-143.
36. Mottino AD, Hoffman T, Crocenzi FA, Pozzi Sanchez EJ, Roma MG, et al. (2007) Disruption of function and localization of tight junctional structures and Mrp2 in sustained estradiol-17beta-D-glucuronide-induced cholestasis. Am J Physiol Gastrointest Liver Physiol 293: G391-G402.
37. Roma MG, Stone V, Shaw R, Coleman R, (1998) Vasopressin-induced disruption of actin cytoskeletal organization and canalicular function in isolated rat hepatocyte couplets: possible involvement of protein kinase C. Hepatology 28: 1031-1041.
38. Beuers U, Probst I, Soroka C, Boyer JL, Kullak-Ublick GA, et al. (1999) Modulation of protein kinase C by taurolithocholic acid in isolated rat hepatocytes. Hepatology 29: 477-482.
39. Wakeling AE, Dukes M, Bowler J, (1991) A potent specific pure antiestrogen with clinical potential. Cancer Res 51: 3867-3873.
40. Di Leo A, Jerusalem G, Petruzelka L, Torres R, Bondarenko IN, et al. (2010) Results of the CONFIRM phase III trial comparing fulvestrant 250 mg with fulvestrant 500 mg in postmenopausal women with estrogen receptor-positive advanced breast cancer. J Clin Oncol 28: 4594-4600.
41. Medunjanin S, Hermani A, De SB, Grisouard J, Rincke G, et al. (2005) Glycogen synthase kinase-3 interacts with and phosphorylates estrogen receptor alpha and is involved in the regulation of receptor activity. J Biol Chem 280: 33006-33014.
42. Goode N, Hughes K, Woodgett JR, Parker PJ, (1992) Differential regulation of glycogen synthase kinase-3 beta by protein kinase C isotypes. J Biol Chem 267: 16878-16882.
43. Ali AS, Ali S, El-Rayes BF, Philip PA, Sarkar FH, (2009) Exploitation of protein kinase C: a useful target for cancer therapy. Cancer Treat Rev 35: 1-8 S0305-7372(08)00266-1 [pii];10.1016/j.ctrv.2008.07.006 [doi].
44. Likhite VS, Stossi F, Kim K, Katzenellenbogen BS, Katzenellenbogen JA, (2006) Kinase-specific phosphorylation of the estrogen receptor changes receptor interactions with ligand, deoxyribonucleic acid, and coregulators associated with alterations in estrogen and tamoxifen activity. Mol Endocrinol 20: 3120-3132.
45. Zucchetti A, Barosso I, Boaglio A, Ochoa E, Davio CA, et al. (2012) Role of GPR30-adenylyl cyclase (AC)-PKA pathway in Estradiol 17ß-glucuronide (E17G) induced cholestasis in isolated rat hepatocytes couplets (IRHC) and isolated perfused rat liver (IPRL). J Hepatol 56: S144.
46. Alzamora R, Harvey BJ, (2008) Direct binding and activation of protein kinase C isoforms by steroid hormones. Steroids 73: 885-888.
47. Boonyaratanakornkit V, (2011) Scaffolding proteins mediating membrane-initiated extra-nuclear actions of estrogen receptor. Steroids 76: 877-884.