Molecular alterations of canalicular transport systems in experimental models of cholestasis: Possible functional correlations

Yale Journal of Biology and Medicine

Volumn 70, Issue 4, 1997, Pages 365-378

  Trauner, Michael ^a  

^a MEDICAL UNIVERSITY OF GRAZ   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; ADENOSINE TRIPHOSPHATASE (CALCIUM MAGNESIUM); ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); ADENOSINE TRIPHOSPHATE; ANION; BICARBONATE; BILE SALT; CALCIUM CHANNEL BLOCKING AGENT; CARRIER PROTEIN; CATION; CHOLESTEROL; ENDOTOXIN; ESTROGEN; GLUTATHIONE; GLYCOPROTEIN P; MESSENGER RNA; NUCLEOTIDE; PHOSPHOLIPID;

BILE; CHOLESTASIS; CONFERENCE PAPER; GENE; GENETIC TRANSCRIPTION; HUMAN; HYPERBILIRUBINEMIA; INTRAHEPATIC BILE DUCT; MEMBRANE POTENTIAL; MEMBRANE TRANSPORT; NONHUMAN;

ADENOSINE TRIPHOSPHATE; ANIMALS; ANION TRANSPORT PROTEINS; BICARBONATES; BILE ACIDS AND SALTS; BILE CANALICULI; BIOLOGICAL TRANSPORT, ACTIVE; CARRIER PROTEINS; CHOLESTASIS; CHOLESTEROL; DISEASE MODELS, ANIMAL; GLUTATHIONE; HUMANS; P-GLYCOPROTEIN; PHOSPHOLIPIDS;

EID: 0031390738     PISSN: 00440086     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Conference Paper

References (88)

1. Nathanson, M.H. and Boyer, J.L. Mechanisms and regulation of bile secretion. Hepatology 14:551-566, 1991.
2. Boyer, J.L., Graf, J., and Meier, P.J. Hepatic transport systems regulating pHi, cell volume, and bile secretion. Ann. Rev. Physiol. 54:415-438, 1992.
3. Boyer, J.L. Bile duct epithelium:frontiers in transport physiology. Am. J. Physiol. 270:G1-G5, 1996.
4. Lomri, N., Fitz, J.G., and Scharschmidt, B.F. Hepatocellular Transport: Role of ATP-binding casette proteins. Sem. Liver Dis. 16:201-210, 1996.
5. Keppler, D. and Arias, I.M. Introduction: transport across the hepatocyte canalicular membrane. FASEB J. 11:15-18, 1997.
6. Mueller, M., Ishikawa, T., Berger, U., Kluenemann, C., Lucka, L., Schreyer, A., Kannicht, C., Reutter, W., Kurz, G., and Keppler, D. ATP-dependent transport of taurocholate across the hepatocyte canalicular membrane by a 110-kDa glycoprotein binding ATP and bile salt. J. Biol. Chem. 266:18920-18926, 1991.
7. Adachi, Y., Kobayashi, H., Kurumi, Y., Shouji, M., Kitano, M., and Yamamoto, T. ATP-dependent taurocholate transport by rat liver canalicular membrane vesicles. Hepatology 14:655-659, 1991.
8. Nishida, T., Gatmaitan, Z., Che, M., and Arias, I.M. Rat liver canalicular membrane vesicles contain an ATP-dependent bile acid transport system. Proc. Natl. Acad. Sci. U.S.A. 88:6590-6594, 1991.
9. Stieger, N., O'Neill, B., and Meier, P.J. ATP-dependent bile salt transport in canalicular rat liver plasma membrane vesicles. Biochem. J. 28:6-73, 1992.
10. Paulusma, C.C., Bosma, P.J., Zaman, G.J.R., Bakker, C.T.M., Otter, M., Scheffer, G.L., Scheper R.J., Borst, P., and Oude Elferink, R.P.J. Congenital jaundice in rats with a mutation in a multidrug resistance-associated protein gene. Science 271:1126-1128, 1996.
11. Buechler, M., Koenig, J., Brom, M., Kartenbeck, J., Spring, H., Horie, T., and Keppler, D.. cDNA cloning of the hepatocyte canalicular isoform of the multidrug restance protein, cMrp, reveals a novel conjugate export pump deficient in hyperbilirubinemic mutant rats. J. Biol. Chem. 271:15091-15098, 1996.
12. Koenig, J., Kartenbeck, J., Kron, A., Buechler, M., Brom, M., and Keppler, D. Identification and cloning of the hepatocyte canalicular conjugate export pump deficient in Dubin-Johnson syndrome (Abstract). Hepatology 24:131A, 1996.
13. Taniguchi, K., Wada, M., Kohno, K., Nakamura, T., Kawabe, T., Kawakami, M., Kagotani, K,. Okumura, K., Akiyama, S., and Kuwano, M. A human canalicular multispecific organic anion transporter (cMOAT) gene is overexpressed in cisplatin-resistant human cancer cell lines with decreased drug accumulation. Cancer Res. 56:4124-4129, 1996.
14. - rats. In: Tavoloni, N. and Berk, P.D., eds. Hepatic Transport and Bile Secretion. Physiology and Pathophysiology. 1st ed. New York: Raven Press Ltd, 1993. pp. 721-730.
15. Oude Elferink, R.P.J. and Jansen, P.L.M. The role of the canalicular multispecific organic anion transporter in the disposal of endo-and xenobiotics. Pharmacol. Ther. 64:77-97, 1994.
16. Oude Elferink, R.P.J., Meijer, D.K.F., Kuipers, F., Jansen, P.L.M., Groen, A.K., and Groothuis, G.M.M. Hepatobiliary secretion of organic compounds; molecular mechanisms of membrane transport. Biochim. Biophys. Acta 1241:215-268, 1995.
17. Mueller, M., Roelofsen, H., and Jansen, P.L.M. Secretion of organic anions by hepatocytes: involvement of homologues of the multidrug resistance protein. Sem. Liver Dis. 16:211-220, 1996.
18. Gottesman, M.M. and Pastan, I. Biochemistry of multidrug resistance mediated by the multidrug transporter. Ann. Rev. Biochem. 62:385-427, 1993.
19. Silverman, J.A. and Thorgeirson, S.S. Regulation and function of the multidrug resistance genes in liver. In: Boyer, J.L. and Ockner, R.K., eds. Progress in Liver Disease. Volume 13. Philadelphia: WB Saunders, 1995. pp. 101-123.
20. Smit, J.J.M., Schinkel, A.M., Oude Elferink, R.P.J., Groen, A.K., Wagenaar, E., Van Deemter, L., Mol, C.C.A., Ottenhof, R., Van der Lugt, N.M.T., Van Roon, M.A., Van der Valk, M.A., Offerhaus, G.J.A., Berns, A.J.M., and Borst, P. Homozygous disruption of the murine mdr2 P-glycoprotein gene leads to complete absence of phospholipids from bile and to liver disease. Cell 75:451-462, 1993.
21. Ruetz, S. and Gros, P. Phophatidylcholine translocase:a physiological role for the mdr2 gene. Cell 77:1071-1081, 1994.
22. Yi, J., Lu, S., Fernandez-Checa, J., and Kaplowitz, N. Expression cloning of a rat hepatic reduced glutathione transporter with canalicular characteristics. J. Clin. Invest. 93:1841-1845, 1994.
23. Lu, S.C., Kuhlenkamp, J., Wu, H., Sun, W.M., Stone, L., and Kaplowitz, N. Progressive defect in biliary GSH secretion in streptozotocin-induced diabetic rats. Am. J. Physiol. 272:G374-G382, 1997.
24. Mueller, M. and Jansen, P.L.M. Molecular aspects of hepatobiliary transport. Am. J. Physiol. 272:G1285-1303, 1997.
25. Kopito, R.R. Molecular biology of the anion exchanger gene family. Int. Rev. Cytol. 123:177-199, 1990.
26. Martinez-Anso, E., Castillo, J.E., Diez, J., Medina, J.F., and Prieo, J. Immunohistochemical detection of chloride/bicarbonate anion exchangers in human liver. Hepatology 19:1400-1406, 1994.
27. Meier, P.J., Knickelbein, R.G., Moseley, R.H., Dobbins, J.W., and Boyer, J.L. evidence for carrier-mediated chloride/bicarbonate exchange in canalicular rat liver plasma membrane vesicles. J. Clin. Invest. 75:1256-1263, 1985.
28. Bossard, R., Stieger, B., O'Neill, B., Fricker, G., and Meier, P.J. Ethinylestradiol treatment induces multiple canalicular membrane transport alterations in rat liver. J. Clin. Invest. 91:2714-2720, 1993.
29. Moseley, R.H., Wang, W., Takeda, H., Lown, K., Shick, L., Ananthanarayanan, M., and Suchy, F.J. Effect of endotoxin on bile acid transport in rat liver: a potential model for sepsis-associated cholestasis. Am. J. Physiol. 271:G137-G146, 1996.
30. Bolder, U., Ton-Nu, H.T., Schteingart, C., Frick, E., and Hofmann, A.F. Hepatocyte transport of bile acids and organic anions in endotoxemic rats: impaired uptake and secretion. Gastroenterology 112:214-225, 1997.
31. Boehme, M., Mueller, M., Leier, I., Jedlitschky, G., and Keppler, D. Cholestasis caused by inhibition of the adenosine triphosphate-dependent bile salt transport in rat liver. Gastroenterology 107:255-265, 1994.
32. Childs, S., Yeh, R.L., Georges, E., and Ling, V. Identification of a sister gene to P-glycoprotein. Cancer Res. 55:2029-2034, 1995.
33. Mueller, M., Vos, T.A., Koopen, N.R., Roelofsen, H., Kuipers, F., and Jansen, P.L.M. Localization and regulation of a novel canalicular ABC-transporter (Abstract). Hepatology 24:368A, 1996.
34. Suchy, F.J., Sippel, C.J., and Ananthanarayanan, M. Hepatic canalicular membrane. 3. Bile acid transport across the hepatocyte canalicular membrane. FASEB J. 11:199-205, 1997.
35. Oritz, D.F, St-Pierre, M.V., Abdulmessih, A., and Arias, I.M. A yeast ATP-binding cassette-type protein mediating ATP-dependent bile acid transport, J. Biol. Chem. 272:15358-15365, 1997.
36. Brown, R.S., Lomri, N., Devoss, J., Rahmaoui, C.M., Xie, M.H., Hua, T., Lidofsky, S.D., and Scharschmidt, B.F. Enhanced secretion of glycocholic acid in a specially adapted cell line is associated with overexpression of apparently novel ATP-binding casette proteins. Proc. Natl. Acad. Sci. U.S.A. 92:5421-5425, 1995.
37. Luther, T.T., Hammerman, P., Rahmaoui, C.M., Lee, P.P., Sela-Herman, S., Matula, G.S., Ananthanarayanan, M., Suchy, F.J., Cavalieri, R.R., Lomri, N., and Scharschmidt, B.F. Evidence for an ATP-dependent bile acid transport protein other than the ecto-ATPase in rats. Gastroenterology 113:249-254, 1997.
38. Lin, S.H. and Guidotti, G. Cloning and expression of a cDNA coding for a rat liver plasma membrane ecto-ATPase. J. Biol. Chem. 264:14408-14414, 1989.
39. Sippel, C.J., Suchy, F.J., Ananthanarayanan, M., and Perlmutter, D.H. The rat liver ecto-ATPase is also a canalicular bile acid transport protein. J. Biol. Chem. 268:2083-2091, 1993.
40. Sippel, C.J., McCollum, M.J., and Perlmutter, D.H. Bile acid transport by the rat livercanalicular bile acid transport/ecto-ATPase protein is dependent on ATP but not on its own ecto-ATPase activity. J. Biol. Chem. 269:2820-2826, 1994.
41. Green, R.M., Beier, D., and Gollan, J.L. Regulation of hepatocyte bile salt transporters by endotoxin and inflammatory cytokines in rodents. Gastroenterology 111:193-198, 1996.
42. Trauner, M., Gartung, C., Schlosser, S.F., and Boyer, J.L. Role of nitric oxide in the transcriptional regulation of bile acid transporters in endotoxin-induced cholestasis (Abstract). Gastroenterology 110:A1349, 1996.
43. Simon, F.R., Fortune, J., Iwahashi, M., Gartung, C., Wolkoff, A., and Sutherland, E. Ethinyl estradiol cholestasis involves alterations in expression of liver sinusoidal transporters. Am J Physiol. 271:G1043-G1052, 1997.
44. +/ bile acid cotransporter in extrahepatic cholestasis. Gastroenterology 110:199-209, 1996.
45. Che, M., Gatmaitman, Z., and Arias, I.M. Ectonucleotidases, purine nucleoside transporter, and function of the bile canalicular plasma membrane of the hepatocyte. FASEB J. 11:101-108, 1997.
46. Kothe, M.J.C., Bakker, C.T.M., de Haan, J., Maas, A., Jansen, P.L.M., and Oude Elferink, R.P.J. Canalicular organic anion transport after bile duct ligation and reconstruction in the rat (Abstract). Hepatology 18:138A, 1993.
47. Roelofsen, H., van der Veere, C., Ottenhoff, R., Schoemaker, B., Jansen, P.L.M., and Oude Elferink, R.P.J. Decreased bilirubin transport in the perfused liver of endotoxemic rats. Gastroenterology 107:1075-1084, 1994.
48. Roelofsen, H., Schoemaker, B., Bakker, C., Ottenhoff, R., Jansen, P.L.M., and Oude Elferink, R.P.J. Impaired hepatocanalicular organic anion transport in endotoxemic rats. Am. J. Physiol. 269:G427-G434, 1995.
49. Wettstein, M., Noe, B., and Haeussinger, D. Metabolism of cysteinyl leukotrienes in the perfused rat liver:the influence of endotoxin pretreatment and the cellular hydration state. Hepatology 22:135-140, 1995.
50. - excretion and blocks the choleretic effect of nitric oxide in rat liver. Hepatology 25:1184-1191, 1997.
51. Trauner, M., Arrese, M., Soroka ,C.J., Ananthanarayanan, M., Koeppel, T.A., Schlosser, S.F., Suchy, F.J., Keppler, D., and Boyer, J.L. The rat canalicular conjugate export pump (mrp2) Is down-regulated in intrahepatic and obstructive cholestasis. Gastroenterology 113:255-264, 1997.
52. Abrams, G.A., Trauner, M., and Nathanson, M.H. Nitric oxide and liver disease. The Gastroenterologist 3:220-233, 1995.
53. Zimmerman, H.J., Fang, M., Utili, R., Seeff, L.B., and Hoofnagle, J. Jaundice due to bacterial infection. Gastroenterology 77:362-374, 1979.
54. Latham, P.S., Menkes, E., Phillips, M.J., and Jeejeebhoy, K.N. Hyperalimentation-associated jaundice:an example of a serum factor inducing cholestasis in rats. Am. J. Clin. Nutr. 41:61-65, 1985.
55. Nolan, J.P. Intestinal endotoxins as mediators of hepatic injury - an idea whose time has come again. Hepatology 10:887-891, 1989.
56. Bird, G.L.A., Sheron, N., Goka, A.K.J., Alexander, G.J., and Williams, R.J. Increased plasma tumor necrosis factor in severe alcoholic hepatitis. Ann. Intern. Med. 112:917-920, 1990.
57. Guarner, C., Soriano, G., Thomas, A., Bulbrena, O., Novella, M.T., Balanzo, J., Vilardell, F., Mourelle, M., and Moncada, S. Increased serum nitrite and nitrate levels in patients with cirrhosis:relationship to endotoxemia. Hepatology 18:1139-1143, 1993.
58. Keppler, D. and Kartenbeck, J. The canalicular conjugate export pump encoded by the cmrp/cmoat gene. In: Boyer, J.L. and Ockner, R.K., eds. Progress in Liver Disease. Volume 14. Philadelphia: W.B. Saunders; 1996. pp. 55-67.
59. Leung, J.W.C., Chan, R.C.Y., Cheung, S.W., Sung, J.Y., Chung, S.C.S., and French, G.L. The effect of obstruction on the biliary excretion of cefoperazone and ceftazidime. J. Antimicrob. Chemother. 25:399-406, 1990.
60. Calhoun, P., Brown, K.B., Strunk, R., Krusch, D.A., Scheld, W.M., and Hanks, J.B. Experimental studies of biliary excretion of piperacillin. Ann. Surg. 205:420-427, 1987.
61. Ito, K., Suzuki, H., Hirohashi, T, Kume, K., Shimizu, T., and Sugiyama, Y. Molecular cloning of canalicular multispecific organic anion transporter defective in EHBR. Am. J. Physiol. 272:G16-G22, 1997.
62. Suzuki, H., Ito, K., Hirohashi, T., Kume, K., Shimizu, T., and Sugiyama, Y. Molecular cloning of canalicular multipsecific organic anion transporter from SD rat liver: mechanism for the impaired expression in Eisai hyperbilirubinemic rats (Abstract). Hepatology 24:131A, 1996.
63. Kartenbeck, J., Leuschner, U., Mayer, R., and Keppler, D. Absence of the canalicular isoform of the MRP gene encoded conjugate export pump from the hepatocytes in Dubin-Johnson syndrome. Hepatology 23:1061-1066, 1996.
64. Paulusma, C.C., Kool, M., Bosma, P.J, Scheffer, G.L., terBorg, F., Scheper, R.J., Tytgat, G.N., Borst, P., Baas, F., and Oude Elferink, R.P. A mutation in the human canalicular multispecific organic anion transporter gene causes the Dubin-Johnson syndrome. Hepatology 25:1539-1542, 1997.
65. Roy Chowdhury, J., Roy Chowdhury, N., Wolkoff, A.W., and Arias, I.M. Heme and bile pigment metabolism. In Arias, I.M., Boyer, J.L., Fausto, N,. Lakoby, W.B., Schachter, D.A., and Shafritz, D.A., eds. The Liver: Biology and Pathobiology. 3rd ed. New York: Raven Press; 1994. pp. 471-504.
66. Schrenk, D., Gant, T.W., Preisegger, K.H., Silverman, J.A., Marino, P.A., and Thorgeirsson, S.S. Induction of multidrug restance gene expression during cholestasis in rats and nonhuman primates. Hepatology 17:854-860, 1993.
67. Accatino, L., Pizzaro, M., Solis, N., Koenig, C.S., Vollrath, V., and Chianale, J. Modulation of hepatic content and biliary excretion of P-glycoproteins in hepatocellular and obstructive cholestasis in the rat. J. Hepatol. 25:349-361, 1996.
68. Schinkel, A.H., Smit, J.J.M., vanTellingen, M., Beijnen, J.H., Wagenaar, E., vanDeemter, L., Mol, C.A.A.M., vanderValk, M.A., Robanus-Maandag, E.C., teRiele, H.P.J., Berns, A.J.M., and Borst, P. Disruption of the mouse mdr1a P-glycoprotein leads to deficiency in the blood brain barrier and to increased sensitivity to drugs. Cell 77:491-502, 1994.
69. Borst P. and Schinkel, A.H. What have we learnt thus far from mice with disrupted P-glycoprotein genes. Eur. J. Cancer 32A:985-990, 1996.
70. Smit, J.W., Schinkel, A.H., Borst, P., and Meijer, D.K.F. Involvement of P-glycoprotein in the biliary and intestinal excretion of amphiphilic drugs: mdr gene knockout studies (Abstract). Hepatology 24:214A, 1996.
71. Kadmon, M., Kluenemann, C., Boehme, M., Ishikawa, T., Gorgas, K., Otto, G., Herfarth, C., and Keppler, D. Inhibition by cyclosporin A of adenosine triphosphate-dependent transport from the hepatocyte into bile. Gastroenterology 104:1507-1514, 1993.
72. Arrese, M., Pizzaro, M., Solis, N., Koenig, C., and Accatino, L. Enhanced biliary excretion of canalicular membrane enzymes in ethynylestradiol-induced cholestasis. Effect of ursodeoxycholic acid administration. Biochem. Pharmacol. 50:1223-1232, 1995.
73. Galan, A.I., Roman, I.D., Munoz, M.E., Cava, F., Gonzalez-Buitrago, J.M., Esteller, A., and Jiminez, R. Inhibition of biliary lipid and protein secretion by cyclosporine A in the rat. Biochem. Pharmacol. 44:1105-1113, 1992.
74. Alpini, G., Lenzi, R., Sarkozi, L., and Tavoloni, N. Biliary physiology in rats with ductular cell hyperplasia. Evidence for a secretory function of proliferated bile ductules. J. Clin. Invest. 81:569-578, 1988.
75. Oude Elferink, R.P.J. and Groen, A.K. The role of mdr2 P-glycoprotein in biliary lipid secretion. Cross-talk between cancer research and biliary physiology. J. Hepatol. 23:617-625, 1995.
76. Deleuze, J.F, Jacuemin, E., Dubuisson, C., Crestell, D., Dumont, M., Erlinger, S., Bernard, O., and Hadchouel, M. Defect of multidrug resistance 3 gene expression in a subtype of progressive familial intrahepatic cholestasis. Hepatology 23:904-908, 1996.
77. Dumoulin, F.L., Reichel, C., Sauerbruch, T., and Spengler, U. Semiquantitation of intrahepatic MDR3 mRNA levels by reverse transcrition/competitive polymerase chain reaction. J. Hepatol. 26:852-856, 1997.
78. Oude Elferink, R.P.J., Ottenhof, R., van Wijland, M., Smith, J.J.M., Schinkel, A.H., and Groen, A.K. Regulation of biliary lipid secretion by mdr2 P-glycoprotein in the mouse. J. Clin. Invest. 95:31-38, 1995.
79. Kozarsky, K.F., Donahee, M.H., Rigotti, A., Iqbal, S.N., Edelman, E.R., and Krieger, M. Overexpression of the HDL receptor SR-B1 alters plasma HDL and bile cholesterol levels. Nature 387:414-417, 1997.
80. Takikama, H., Wako, Y., Sano, N., and Yamanaka, M. Changes in biliary excretory mechanisms in bile duct-ligated rat. Dig. Dis. Sci. 41:256-262, 1996.
81. Trauner, M., Ananthanarayanan, M., Yi, J.R., Arrese, M., Kaplowitz, N., and Boyer, J.L. Effects of endotoxin on the expression of the canalicular glutathione (GSH) and multispecific organic anion transporters (cMOAT) in rat liver (Abstract). Hepatology 24:216A, 1996.
82. Fernandez-Checa, J.C., Takikawa, H., Horie, T., Ookhtens, M., and Kaplowitz, N. Canalicular transport of reduced glutathione in normal and mutant Eisai hyperbilirubinemic rats. J. Bio.1 Chem, 267:1667-1673,1992.
83. Lu, S.C., Cai, J., Kuhlenkamp, J., Sun, W.M., Takikawa, H., Takenaka, O., Horie, T., Yi, J., and Kaplowitz, N. Alterations in glutathione homeostasis in mutant Eisai hyperbilirubinemic rats. Hepatology 24:253-258, 1996.
84. Zaman, G.J.R., Lankelma, J., van Telligen, O., Beijnen, J., Deeker, H., Paulusma, C., Oude Elferink, R.P.J., Baas, F., and Borst P. Role of gluatathione in the export of compounds from cells by the multidrug-resistance-associated protein. Proc. Natl. Acad. Sci. U.S.A. 92:7690-7694, 1995.
85. - exchanger in rat. J. Hepatol. 26:146-157, 1997.
86. Prieto, J., Qian, C., Garcia, N., Diez, J., and Medina, J.F. Abnormal expression of anion exchanger genes in primary biliary cirrhosis. Gastroenterology 105:572-578, 1993.
87. Vazquez, J.J. Vazquez, M., Idoate, M.A., Montuenga, L., Martinez-Anso, E., Castillo, J.E., Garcia, N., Medina, J.F., and Prieto, J. Anion excahnger immunoreactivity in human salivary glands in health and Sjogren's syndrome. Am. J. Pathol. 146:1422-1432, 1995.
88. Medina, J.F, Martinez-Anso, E., Vazquez, J.J., and Prieto, J. Decreased anion exchanger 2 immunoreactivity in the liver of patients with primary biliary cirrhosis. Hepatology 25:12-17, 1997.