Glutathione S-conjugate transport in hepatocytes entering the cell cycle is preserved by a switch in expression from the apical MRP2 to the basolateral MRP1 transporting protein

Journal of Cell Science

Volumn 112, Issue 9, 1999, Pages 1395-1404

  Roelofsen, Han ^a   Hooiveld, Guido J E J ^a   Koning, Hans ^a   Havinga, Rick ^b   Jansen, Peter L M ^a   Müller, Michael ^a  

^a Div of Gastroenterol and Hepatol   (Netherlands)

^b UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

Author keywords

Cell cycle; Glutathione S conjugate transport; Hepatocyte; Localization; Multidrug resistance protein

Indexed keywords

CARRIER PROTEIN; CELL MEMBRANE PROTEIN; GLUTATHIONE; MESSENGER RNA; MULTIDRUG RESISTANCE PROTEIN; QUINONE DERIVATIVE;

ANIMAL CELL; APICAL MEMBRANE; ARTICLE; BASOLATERAL MEMBRANE; CELL ADHESION; CELL CYCLE; CELL CYCLE G1 PHASE; CELL CYCLE S PHASE; CELL DENSITY; CELL MEMBRANE TRANSPORT; CELL POLARITY; CELL PROTECTION; CELL TRANSPORT; CELL VACUOLE; CELLULAR DISTRIBUTION; CONJUGATE; CONTROLLED STUDY; LIVER CELL; MALE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN TRANSPORT; RAT;

ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; CARRIER PROTEINS; CELL COUNT; CELL CYCLE; CELL MEMBRANE; DOWN-REGULATION; DRUG RESISTANCE, MULTIPLE; G1 PHASE; LIVER; MALE; MEMBRANE TRANSPORT PROTEINS; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; OXIDATIVE STRESS; RATS; RATS, WISTAR; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; S PHASE;

ANIMALIA;

EID: 0033052179     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (51)

1. Akerboom, T., Bultmann, T. and Sies, H. (1988). Inhibition of biliary taurocholale excretion during menadione metabolism in perfused rat liver. Arch. Biochem. Biophys. 263, 10-18.
2. Akimaru, K., Kuo, M. T., Furuta, K., Suzuki, M., Noyori, R. and Ishikawa, T. (1996). Induction of MRP/GS-X pump and cellular resistance to anticancer prostaglandins. Cytotechnology 19, 221-227.
3. Almquist, K. C., Loe, D. W., Hipfner, D. R. and Mackie, J. E. (1995). Characterization of the Mr 190, 000 multidrug resistance protein (MRP) in drug-selected and transfected human tumor cells. Cancer Res. 55, 102-110.
4. Ben-Ze'ev, A., Robinson, G. S., Bucher, N. L. R. and Farmer, S. R. (1988). Cell-Cell and cell-matrix interactions differentially regulate the expression of hepatic and cytoskeletal genes in primary cultures of rat hepatocytes. Proc. Nat. Acad Sci. USA 85, 2161-2165.
5. - exchanger in rat hepatocytes. Proc. Nat. Acad. Sci. USA 91, 792-796.
6. Berry, M. N. and Friend, D. S. (1969). High-yield preparation of isolated rat liver parenchymal cells: a biochemical and fine structural study. J. Cell Biol. 43, 506-520.
7. Boyer, J. L. and Soroka, C. J. (1995). Vesicle targeting to the apical domain regulates bile excretory function in isolated rat hepatocyte couplets. Gastroenterology 109, 1600-1611.
8. Büchler, M., Konig, J., Brom, M., Kartenbeck, J., Spring, H., Horie, T. and Keppler, D. (1996). cDNA cloning of the hepatocyte canalicular isoform of the multidrug resistance protein, cmrp, reveals a novel conjugate export pump deficient in hyperbilirubinemic mutant rats. J. Biol. Chem. 271, 15091-15098.
9. Cole, S. P. C., Bhardwaj, G., Gerlach, J. H., Mackie, J. E., Grant, C. E., Almquist, K. C., Stewart, A. J., Kurz, E. U., Duncan, A. M. V. and Deeley, R. G. (1992). Overexpression of a transporter gene in a multidrug-resistant human lung cancer cell line. Science 258, 1650-1654.
10. Fardel, O., Ratanasavanh, D., Loyer, P., Ketterer, B. and Guillouzo, A. (1992). Overexpression of the multidrug resistance gene product in adult rat hepatocytes during primary culture. Eur. J. Biochem. 205, 847-852.
11. Fialka, I., Schwartz, H., Reichmann, E., Oft, M., Busslinger, M. and Beug, H. (1996). The estrogen-dependent c-JunER protein causes a reversible loss of mammary epithelial cell polarity involving a destabilization of adherens junctions. J. Cell Biol. 132, 1115-1132.
12. Flens, M. J., Zaman, G. J. R., van der Valk, P., Izquierdo, M. A., Schroeijers, A. B., Scheffer, G. L., van der Groep, P., de Haas, M., Meijer, C. J. L. M. and Scheper, R. J. (1996). Tissue distribution of the multidrug resistance protein. Am. J. Pathol. 148, 1237-1247.
13. Fort, P., Marty, L., Piechaczyk, M., el Sabrouty, S., Dani, C., Jeanteur, P. and Blanchard, J. M. (1985). Various rat adult tissues express only one major mRNA species from the glyceraldehyde-3-phosphate-dehydrogenase multigenic family. Nucl. Acids Res. 13, 1431-1442.
14. 4 receptor antagonist MK571 specifically modulates MRP associated multidrug resistance. Biochem. Biophys. Res. Commun. 208, 345-352.
15. Hann, S. R., King, M. W., Bentley, D. L., Anderson, C. W. and Eisenman, R. N. (1988). A non-AUG translational initiation in c-myc exon 1 generates an N-terminally distinct protein whose synthesis is disrupted in Burkitt's lymphomas. Cell 52, 185-195.
16. Hirohashi, T., Suzuki, H., Ito, K., Ogawa, K., Kume, K., Shimizu, T. and Sugiyama, Y. (1998). Hepatic expression of multidrug resistance-associated protein-like proteins maintained in Eisai hyperbilirubinemic rats. Mol. Pharmacol. 53, 1068-1075.
17. Hirsch-Ernst, K. I., Ziemann, C., Schmitz-Salue, C., Foth, H. and Kahl, G. F. (1995). Modulation of P-glycoprotein and mdrlb mRNA expression by growth factors in primary rat hepatocyte culture. Biochem. Biophys. Res. Commun. 215, 179-185.
18. Ishikawa, T., Wright, C. D. and Ishizuka, H. (1994). GS-x pump is functionally overexpressed in cis-diamminedichloroplatinum(II)-resistant human leukemia HL-60 cells and down-regulated by cell differentiation. J Biol. Chem. 269, 29085-29093.
19. Jedlitschky, G., Leier, I., Buchholz, U., Center, M. and Keppler, D. (1994). ATP-dependent transport of glutathtone S-conjugates by the multidrug resistance-associated protein. Cancer Res. 54, 4833-4836.
20. Kiuchi, Y., Suzuki, H., Hirohashi, T., Tyson, C. A. and Sugiyama, Y. (1998). cDNA cloning and inducible expression of human multidrug resistance associated protein 3 (MRP3). FEBS Lett. 433, 149-152.
21. Kool, M., de Haas, M., Scheffer, G. L., Scheper, R. J., van Eijk, M. J., Juijn, J. A., Baas, F. and Borst, P. (1997). Analysis of expression of cMOAT (MRP2), MRP3, MRP4, and MRP5, homologues of the multidrug resistance-associated protein gene (MRP1), in human cancer cell lines. Cancer Res. 57, 3537-3547.
22. Kumatori, A., Nakamura, T. and Ichihara, A. (1991). Cell-density dependent expression of the c-myc gene in primary cultured rat hepatocytes. Biochem. Biophys. Res. Commun. 178, 480-485.
23. Lautier, D., Canitrot, Y., Deeley, R. G. and Cole, S. P. C. (1996) Multidrug resistance mediated by the multidrug resistance protein (MRP) gene. Biochem. Pharmacol. 52, 967-977.
24. Lee, C. H., Bradley, G., Zhang, J. T. and Ling, V. (1993). Differential expression of P-glycoprotein genes in primary rat hepatocyte culture. J. Cell Physiol. 157, 392-402.
25. Leier, I., Jedlitschky, G., Buchholz, U., Cole, S. P., Deeley, R. G. and Keppler, D. (1994). The MRP gene encodes an ATP-dependent export pump for leukotriene C4 and structurally related conjugates. J. Biol. Chem. 269, 27807-27810.
26. Leier, I., Jedlitschky, G., Buchholz, U., Center, M., Cole, S. P. C., Deeley, R. G. and Keppler, D. (1996). ATP-dependent glutathione disulphide transport mediated by the MRP gene-encoded conjugate export pump. Biochem. J. 314, 433-437.
27. Loe, D. W., Deeley, R. G. and Cole, S. P. C. (1996). Biology of the multidrug resistance-associated protein. MRP. Eur. J. Cancer 32A, 945-957.
28. 1 and S phases of adult rat hepalocytes in vitro. J. Biol. Chem. 271, 11484-11492.
29. Mayer, R., Kartenbeck, J., Büchler, M., Jedlitschky, G., Leier, I. and Keppler, D. (1995). Expression of the MRP gene-encoded conjugate export pump in liver and its selective absence from the canalicular membrane in transport-deficient mutant hepatocytes. J. Cell Biol. 131, 137-150.
30. Müller, M., Meijer, C., Zaman, G. J. R., Borst, P., Scheper, R. J., Mulder, N. H., de Vries, E. G. E. and Jansen, P. L. M. (1994). Overexpression of the gene encoding the multidrug resistance-associated protein results in increased ATP-dependent glutathione S-conjugate transport. Proc. Nat Acad. Sci. USA 91, 13033-13037.
31. Müller, M., Roelofsen, H. and Jansen, P. L. M. (1996). Secretion of organic anions by hepatocytes: involvement of homologues of the multidrug resistance protein. Semin. Liver. Dis. 16, 211-220.
32. Müller, M. and Jansen, P. L. M. (1997). Molecular aspects of hepatobiliary transport. Am. J. Physiol. 272, G1285-G1303.
33. Nakamura, T., Yoshimoto, K., Nakayama, Y., Tomita, Y. and Ichihara, A. (1983). Reciprocal modulation of growth and differentiated functions of mature rat hepatocytes in primary culture by cell-cell contact and cell membranes. Proc. Nat. Acad. Sci. USA 80, 7229-7233.
34. Norris, M. D., Bordow, S. B., Marshall, G. M., Haber, P. S., Cohn, S. L. and Haber, M. (1996). Expression of the gene for multidrug-resistance-associated protein and outcome in patients with neuroblastoma. New Engl. J. Med. 334, 231-238.
35. O'Brien, P. J. (1991). Molecular mechanisms of quinone cytotoxicity. Chem. Biol. Interact. 80, 1-41.
36. Oude Elferink, R. P. J. and Jansen, P. L. M. (1994). The role of the canalicular multispecific organic anion transporter in the disposal of endo-and xenobiotics. Pharmacol. Ther. 64, 77-97.
37. 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. (1996). Congenital jaundice in rats with a mutation in a multidrug resistance-associated protein gene. Science 271, 1126-1128.
38. Peters, M. M., Lau, S. S., Dulik, D., Murphy, D., van Ommen, B., van Bladeren, P. J. and Monks, T. J. (1996a). Metabolism of tert-butylhydroquinone to S-substiluted conjugates in the male Fischer 344 rat. Chem. Res. Toxicol. 9, 133-139.
39. Peters, M. M., Rivera, M. I., Jones, T. W., Monks, T. J. and Lau, S. S. (1996b). Glutathione conjugates of tert-butyl-hydroquinone, a metabolite of the urinary tract tumor promoter 3-tert-butyl-hydroxyanisole, are toxic to kidney and bladder. Cancer Res. 56, 1006-1011.
40. Rappa, G., Lorico, A., Flavell, R. A. and Sartorelli, A. C. (1997). Evidence that the multidrug resistance protein (MRP) functions as a co-transporter of glutathione and natural product toxins. Cancer Res. 57, 5232-5237.
41. Roelofsen, H., Bakker, C. T., Schoemaker, B., Heijn, M., Jansen, P. L. M. and Oude Elferink, R. P. J. (1995). Redistribution of canalicular organic anion transport activity in isolated and cultured rat hepatocytes. Hepatology 21, 1649-1657.
42. Roelofsen, H., Müller, M. and Jansen, P. L. M. (1997a). Regulation of organic anion transport in the liver. Yale J. Biol. Med. 70, 435-445.
43. Roelofsen, H., Vos, T. A., Schippers, I. J., Kuipers, F., Koning, H., Moshage, H., Jansen, P. L. M. and Müller, M. (1997b). Increased levels of the multidrug resistance protein in lateral membranes of proliferating hepatocyte-derived cells. Gastroenterology 112, 511-521.
44. Roelofsen, H., Soroka, C. J., Keppler, D. and Boyer, J. L. (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.
45. Schippers, I. J., Moshage, H., Roelofsen, H., Müller, M., Heymans, H. S., Ruiters, M. and Kuipers, F. (1997). Immortalized human hepatocytes as a tool for the study of hepatocytic (de-)differentiation. Cell Biol. Toxicol. 13, 375-386.
46. Shimbara, N., Takashina, M., Sato, C., Iizuka, M., Kobayashi, S., Tanaka, K. and Ichihara, A. (1992). c-myc expression is down-regulated by cell-cell and cell-extracellular matrix contacts in normal hepatocytes, but not in hepatoma cells. Biochem. Biophys. Res. Commun. 184, 825-831.
47. Trauner, M., Arrese, M., Soroka, C. J., Ananthanarayanan, M., Koeppel, T. A., Schlosser, S. F., Suchy, F. J., Keppler, D. and Boyer, J. L. (1997). The rat canalicular conjugate export pump (Mrp2) is down-regulated in intrahepatic and obstructive cholestasis. Gastroenterology 113, 255-264.
48. Van Luyn, M. J., Müller, M., Renes, J., Meijer, C., Scheper, R. J., Nienhuis, E. F., Mulder, N. H., Jansen, P. L. and de Vries, E. G. (1998). Transport of glutathione conjugates into secretory vesicles is mediated by the multidrug-resistance protein 1. Int. J. Cancer 76, 55-62.
49. Vos, T. A., Hooiveld, G. J. E. J., Koning, H., Childs, S., Meijer, D. K. F., Moshage, H., Jansen, P. L. M. and Müller, M. (1998). Upregulation of the multidrug resistance genes, mrp1 and mdr1b, and down-regulation of the organic anion transporter, mrp2, and bile salt transporter, spgp, in endotoxemic rat liver. Hepatology 28, 1637-1644.
50. Zhang, F., Riley, J. and Gant, T. W. (1996). Use of internally controlled reverse transcriptase-polymerase chain reaction for absolute quantitation of individual multidrug resistant gene transcripts in tissue samples. Electrophoresis 17, 255-260.
51. Zhu, Q. C. and Center, M. S. (1994). Cloning and sequence analysis of the promoter region of the MRP gene of HL60 cells isolated for resistance to adriamycin. Cancer Res. 54, 4488-4492.