ERK1/2 and p38 MAPKs Are Complementarily Involved in Estradiol 17ß-d-Glucuronide-Induced Cholestasis: Crosstalk with cPKC and PI3K

PLoS ONE

Volumn 7, Issue 11, 2012, Pages

  Boaglio, Andrea C ^a   Zucchetti, Andrés E ^a   Toledo, Flavia D ^a   Barosso, Ismael R ^a   Sánchez Pozzi, Enrique J ^a   Crocenzi, Fernando A ^a   Roma, Marcelo G ^a  

^a Universidad Nacional de Río Cuarto Consejo Nacional de Investigaciones Científicas y Técnicas   (Argentina)

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 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 2,4 DINITROPHENYL GLUTATHIONE; 4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; ANTHRA[1,9 CD]PYRAZOL 6(2H) ONE; CARRIER PROTEINS AND BINDING PROTEINS; ESTRADIOL 17 GLUCURONIDE; FLUORESCENT DYE; GLUTATHIONE DERIVATIVE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; MULTIDRUG RESISTANCE PROTEIN 2; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN BSEP; PROTEIN KINASE C; TAUROCHOLIC ACID; UNCLASSIFIED DRUG; WORTMANNIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BILIARY EXCRETION; CELLULAR DISTRIBUTION; CHOLESTASIS; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENDOCYTOSIS; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; FEMALE; IMAGE ANALYSIS; INTERNALIZATION; ISOLATED RAT HEPATOCYTE COUPLET; LIVER; LIVER CELL; NONHUMAN; PROTEIN LOCALIZATION; PROTEIN SECRETION; RAT; WESTERN BLOTTING;

ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; BLOTTING, WESTERN; CHOLESTASIS; ESTRADIOL; FEMALE; HEPATOCYTES; IMAGE PROCESSING, COMPUTER-ASSISTED; MAP KINASE SIGNALING SYSTEM; MICROSCOPY, CONFOCAL; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHORYLATION; PROTEIN KINASE C; RATS; RATS, WISTAR; SIGNAL TRANSDUCTION; STATISTICS, NONPARAMETRIC; TAUROCHOLIC ACID;

RATTUS;

EID: 84869138342     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0049255     Document Type: Article

References (64)

1. Crocenzi FA, Zucchetti AE, Boaglio AC, Barosso IR, Sanchez Pozzi EJ, et al. (2012) Localization status of hepatocellular transporters in cholestasis. Front Biosci 17: 1201-1218.
2. Vore M, Liu Y, Huang L, (1997) Cholestatic properties and hepatic transport of steroid glucuronides. Drug Metabol Rev 29: 183-203.
3. Stieger B, Fattinger K, Madon J, Kullak-Ublick GA, Meier PJ, (2000) Drug- and estrogen-induced cholestasis through inhibition of the hepatocellular bile salt export pump (Bsep) of rat liver. Gastroenterology 118: 422-430.
4. Kan KS, Monte M, Parslow RA, Coleman R, (1989) Oestradiol 17β-glucuronide increases tight junctional permeability in rat liver. Biochem J 261: 297-300.
5. Crocenzi FA, Mottino AD, Cao J, Veggi LM, Pozzi EJ, et al. (2003) Estradiol-17β-D-glucuronide induces endocytic internalization of Bsep in rats. Am J Physiol Gastrointest Liver Physiol 285: G449-459.
6. Mottino AD, Cao J, Veggi LM, Crocenzi FA, Roma MG, et al. (2002) Altered localization and activity of canalicular Mrp2 in estradiol-17β-D-glucuronide-induced cholestasis. Hepatology 35: 1409-1419.
7. Mottino AD, Crocenzi FA, Pozzi EJ, Veggi LM, Roma MG, et al. (2005) Role of microtubules in estradiol-17β-D-glucuronide-induced alteration of canalicular Mrp2 localization and activity. Am J Physiol GastrointestLiver Physiol 288: G327-G336.
8. Crocenzi FA, Sanchez Pozzi EJ, Ruiz ML, Zucchetti AE, Roma MG, et al. (2008) Ca2+-dependent protein kinase C isoforms are critical to estradiol 17β-D-glucuronide-induced cholestasis in the rat. Hepatology 48: 1885-1895.
9. 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 17β-D-glucuronide-induced cholestasis: complementarity with classical protein kinase C. Hepatology 52: 1465-1476.
10. Lee MY, Park SH, Lee YJ, Heo JS, Lee JH, et al. (2006) EGF-induced inhibition of glucose transport is mediated by PKC and MAPK signal pathways in primary cultured chicken hepatocytes. Am J Physiol Gastrointest Liver Physiol 291: G744-750.
11. Torres LM, Cefaratti C, Perry B, Romani A, (2006) Involvement of ERK1/2 and p38 in Mg2+ accumulation in liver cells. Mol Cell Biochem 288: 191-199.
12. Gnocchi D, Leoni S, Incerpi S, Bruscalupi G, (2012) 3,5,3′-Triiodothyronine (T(3)) stimulates cell proliferation through the activation of the PI3K/Akt pathway and reactive oxygen species (ROS) production in chick embryo hepatocytes. Steroids 77: 589-595.
13. Scassa ME, Guberman AS, Varone CL, Canepa ET, (2001) Phosphatidylinositol 3-kinase and Ras/mitogen-activated protein kinase signaling pathways are required for the regulation of 5-aminolevulinate synthase gene expression by insulin. Exp Cell Res 271: 201-213.
14. Roux PP, Blenis J, (2004) ERK and p38 MAPK-activated protein kinases: a family of protein kinases with diverse biological functions. Microbiol Mol Biol Rev 68: 320-344.
15. Pimienta G, Pascual J, (2007) Canonical and alternative MAPK signaling. Cell Cycle 6: 2628-2632.
16. Marino M, Distefano E, Pallottini V, Caporali S, Bruscalupi G, et al. (2001) Activation of IP(3)-protein kinase C-alpha signal transduction pathway precedes the changes of plasma cholesterol, hepatic lipid metabolism and induction of low-density lipoprotein receptor expression in 17-β-oestradiol-treated rats. Exp Physiol 86: 39-45.
17. Marino M, Distefano E, Caporali S, Ceracchi G, Pallottini V, et al. (2001) β-estradiol stimulation of DNA synthesis requires different PKC isoforms in HepG2 and MCF7 cells. J Cell Physiol 188: 170-177.
18. Nuedling S, Kahlert S, Loebbert K, Meyer R, Vetter H, et al. (1999) Differential effects of 17β-estradiol on mitogen-activated protein kinase pathways in rat cardiomyocytes. FEBS Lett 454: 271-276.
19. Singh M, Setalo G Jr, Guan X, Warren M, Toran-Allerand CD, (1999) Estrogen-induced activation of mitogen-activated protein kinase in cerebral cortical explants: convergence of estrogen and neurotrophin signaling pathways. J Neurosci 19: 1179-1188.
20. Alvaro D, Onori P, Metalli VD, Svegliati-Baroni G, Folli F, et al. (2002) Intracellular pathways mediating estrogen-induced cholangiocyte proliferation in the rat. Hepatology 36: 297-304.
21. Geraldes P, Sirois MG, Tanguay JF, (2003) Specific contribution of estrogen receptors on mitogen-activated protein kinase pathways and vascular cell activation. Circ Res 93: 399-405.
22. 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.
23. Denk GU, Hohenester S, Wimmer R, Böhland C, Rust C, et al. (2008) Role of mitogen-activated protein kinases in tauroursodeoxycholic acid-induced bile formation in cholestatic rat liver. Hepatol Res 38: 717-726.
24. Crocenzi FA, Mottino AD, Sanchez Pozzi EJ, Pellegrino JM, Rodriguez Garay EA, et al. (2003) Impaired localisation and transport function of canalicular Bsep in taurolithocholate-induced cholestasis in the rat. Gut 52: 1170-1177.
25. Wilton JC, Williams DE, Strain AJ, Parslow RA, Chipman JK, et al. (1991) Purification of hepatocyte couplets by centrifugal elutriation. Hepatology 14: 180-183.
26. 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.
27. Mita S, Suzuki H, Akita H, Hayashi H, Onuki R, et al. (2006) Inhibition of bile acid transport across Na+/taurocholate cotransporting polypeptide (SLC10A1) and bile salt export pump (ABCB 11)-coexpressing LLC-PK1 cells by cholestasis-inducing drugs. Drug Metab Dispos 34: 1575-1581.
28. 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.
29. 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.
30. Zucchetti AE, Barosso IR, Boaglio A, Pellegrino JM, Ochoa EJ, et al. (2011) Prevention of estradiol 17β-D-glucuronide-induced canalicular transporter internalization by hormonal modulation of cAMP in rat hepatocytes. Mol Biol Cell 22: 3902-3915.
31. 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.
32. Lowry OH, Rosembrough NJ, Farr AL, Randall RJ, (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193: 265-275.
33. Bessems M, t Hart NA, Tolba R, Doorschodt BM, Leuvenink HG, et al. (2006) The isolated perfused rat liver: standardization of a time-honoured model. Lab Anim 40: 236-246.
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: G1261-1273.
35. Berthelot P, Erlinger S, Dhumeaux D, Preaux AM, (1970) Mechanism of phenobarbital-induced hypercholeresis in the rat. Am J Physiol 219: 809-813.
36. Rahner C, Stieger B, Landmann L, (2000) Apical Endocytosis in Rat Hepatocytes In Situ Involves Clathrin, Traverses a Subapical Compartment, and Leads to Lysosomes. Gastroenterology 119: 1692-1707.
37. Kimura M, Okamoto H, Ogihara M, (2007) Activation of mitogen-activated protein kinase by hepatocyte growth factor is stimulated by both alpha1- and beta2-adrenergic agonists in primary cultures of adult rat hepatocytes. J Pharmacol Sci 103: 398-407.
38. Band CJ, Posner BI, (1997) Phosphatidylinositol 3′-kinase and p70s6k are required for insulin but not bisperoxovanadium 1,10-phenanthroline (bpV(phen)) inhibition of insulin-like growth factor binding protein gene expression. Evidence for MEK-independent activation of mitogen-activated protein kinase by bpV(phen). J Biol Chem 272: 138-145.
39. Qiao L, Yacoub A, Studer E, Gupta S, Pei XY, et al. (2002) Inhibition of the MAPK and PI3K pathways enhances UDCA-induced apoptosis in primary rodent hepatocytes. Hepatology 35: 779-789.
40. Lee SH, Lee MY, Lee JH, Han HJ, (2008) A potential mechanism for short time exposure to hypoxia-induced DNA synthesis in primary cultured chicken hepatocytes: Correlation between Ca2+/PKC/MAPKs and PI3K/Akt/mTOR. J Cell Biochem 104: 1598-1611.
41. Spector M, Nguyen VA, Sheng X, He L, Woodward J, et al. (2000) Activation of mitogen-activated protein kinases is required for alpha1-adrenergic agonist-induced cell scattering in transfected HepG2 cells. Exp Cell Res 258: 109-120.
42. Vergarajauregui S, San Miguel A, Puertollano R, (2006) Activation of p38 mitogen-activated protein kinase promotes epidermal growth factor receptor internalization. Traffic 7: 686-698.
43. Mace G, Miaczynska M, Zerial M, Nebreda AR, (2005) Phosphorylation of EEA1 by p38 MAP kinase regulates mu opioid receptor endocytosis. EMBO J 24: 3235-3246.
44. Huang CC, You JL, Wu MY, Hsu KS, (2004) Rap1-induced p38 mitogen-activated protein kinase activation facilitates AMPA receptor trafficking via the GDI.Rab5 complex. Potential role in (S)-3,5-dihydroxyphenylglycene-induced long term depression. J Biol Chem 279: 12286-12292.
45. Lam P, Xu S, Soroka CJ, Boyer JL, (2012) A C-terminal tyrosine-based motif in the bile salt export pump directs clathrin-dependent endocytosis. Hepatology 55: 1901-1911.
46. Grandal MV, Grovdal LM, Henriksen L, Andersen MH, Holst MR, et al. (2011) Differential Roles of Grb2 and AP-2 in p38 MAPK- and EGF-Induced EGFR Internalization. Traffic Dec 22 doi: 10.1111/j.1600-0854.2011.01322.x.
47. Seachrist JL, Ferguson SS, (2003) Regulation of G protein-coupled receptor endocytosis and trafficking by Rab GTPases. Life Sci 74: 225-235.
48. Cavalli V, Vilbois F, Corti M, Marcote MJ, Tamura K, et al. (2001) The stress-induced MAP kinase p38 regulates endocytic trafficking via the GDI:Rab5 complex. Mol Cell 7: 421-432.
49. Apodaca G, (2001) Endocytic traffic in polarized epithelial cells: role of the actin and microtubule cytoskeleton. Traffic 2: 149-159.
50. Soroka CJ, Pate MK, Boyer JL, (1999) Canalicular export pumps traffic with polymeric immunoglobulin A receptor on the same microtubule-associated vesicle in rat liver. J Biol Chem 274: 26416-26424.
51. Wakabayashi Y, Lippincott-Schwartz J, Arias IM, (2004) 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 15: 3485-3496.
52. Vagnoni A, Rodriguez L, Manser C, De Vos KJ, Miller CC, (2011) Phosphorylation of kinesin light chain 1 at serine 460 modulates binding and trafficking of calsyntenin-1. J Cell Sci 124: 1032-1042.
53. Pol A, Ortega D, Enrich C, (1997) Identification of cytoskeleton-associated proteins in isolated rat liver endosomes. Biochem J 327 (Pt 3): 741-746.
54. Kurz AK, Graf D, Schmitt M, vom Dahl S, Häussinger D, (2001) Tauroursodesoxycholate-Induced Choleresis Involves p38MAPK Activation and Translocation of the Bile Salt Export Pump in Rats. Gastroenterology 121: 407-419.
55. Schliess F, Kurz AK, vom Dahl S, Haussinger D, (1997) Mitogen-activated protein kinases mediate the stimulation of bile acid secretion by tauroursodeoxycholate in rat liver. Gastroenterology 113: 1306-1314.
56. Kubitz R, Sutfels G, Kuhlkamp T, Kolling R, Haussinger D, (2004) Trafficking of the bile salt export pump from the Golgi to the canalicular membrane is regulated by the p38 MAP kinase. Gastroenterology 126: 541-553.
57. Schonhoff CM, Webster CR, Anwer MS, (2010) Cyclic AMP stimulates Mrp2 translocation by activating p38{alpha} MAPK in hepatic cells. Am J Physiol Gastrointest Liver Physiol 298: G667-674.
58. Haussinger D, Kurz A, Wettstein M, Graf D, Vomdahl S, et al. (2003) Involvement of integrins and Src in tauroursodeoxycholate-induced and swelling-induced choleresis. Gastroenterology 124: 1476-1487.
59. Kurz AK, Block C, Graf D, Dahl SV, Schliess F, et al. (2000) Phosphoinositide 3-kinase-dependent Ras activation by tauroursodesoxycholate in rat liver. Biochem J 350 Pt 1: 207-213.
60. Philips MR, (2005) Compartmentalized signalling of Ras. Biochem Soc Trans 33: 657-661.
61. Pol A, Calvo M, Enrich C, (1998) Isolated endosomes from quiescent rat liver contain the signal transduction machinery. Differential distribution of activated Raf-1 and Mek in the endocytic compartment. FEBS Lett 441: 34-38.
62. Philips MR, (2004) Sef: a MEK/ERK catcher on the Golgi. Mol Cell 15: 168-169.
63. Wang Y, Huang S, Sah VP, Ross J Jr, Brown JH, et al. (1998) Cardiac muscle cell hypertrophy and apoptosis induced by distinct members of the p38 mitogen-activated protein kinase family. J Biol Chem 273: 2161-2168.
64. Chapman MS, Miner JN, (2011) Novel mitogen-activated protein kinase kinase inhibitors. Expert Opin Investig Drugs 20: 209-220.