Transport of glutathione, glucuronate, and sulfate conjugates by the MRP gene-encoded conjugate export pump

Cancer Research

Volumn 56, Issue 5, 1996, Pages 988-994

  Jedlitschky, Gabriele ^a   Leier, Inka ^a   Buchholz, Ulrike ^a   Barnouin, Karin ^a   Kurz, Gerhart ^b   Keppler, Dietrich ^a  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b UNIVERSITY OF FREIBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; DAUNORUBICIN; DOXORUBICIN; ETOPOSIDE; GLUCURONIC ACID; GLUTATHIONE; MELPHALAN; SULFATE; VINBLASTINE;

ARTICLE; CANCER; CANCER CHEMOTHERAPY; DRUG CONJUGATION; DRUG TRANSPORT; HUMAN; HUMAN CELL; MULTIDRUG RESISTANCE; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANTINEOPLASTIC AGENTS; BIOLOGICAL TRANSPORT; DRUG RESISTANCE, MULTIPLE; ESTROGENS, CONJUGATED (USP); GENE TRANSFER TECHNIQUES; GLUCURONATES; GLUCURONIC ACID; GLUTATHIONE; HELA CELLS; HUMANS; P-GLYCOPROTEIN; SULFATES;

EID: 0030063480     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (44)

1. 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 Overexpression of a transporter gene in a multidrug-resistant human lung cancer cell Line. Science (Washington DC), 258: 1650-1654, 1992.
2. Cole, S. P. C., Sparks, K. E., Fraser, K., Loe, D W , Grant, C. E , Wilson, G. M., and Deeley, R. G. Pharmacological characterization of multidrug resistant MRP-transfected human tumor cells Cancer Res., 54: 5902-5910, 1994
3. Jedlitschky, G , Leier, I., Buchholz, U., Center, M , and Keppler, D. ATP-dependent transport of glutathione S-conjugates by the multidrug resistance-associated protein. Cancer Res., 54: 4833-4836, 1994.
4. 4 and structurally related conjugates. J Biol. Chem., 269: 27807-27810, 1994
5. Muller, 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. Overexpression of the gene encoding the multidrug resistance associated protein results in increased ATP-dependent glutathione S-conjugate transport Proc. Natl. Acad. Sci USA, 91 13033-13037, 1994.
6. Barrand, M. A., Rhodes, T., Center, M. S., and Twentyman, P R. Chemosensitization and drug accumulation effects of cyclosporin A, PSC 833, and verapamil in human MDR large cell lung cancer cells expressing a 190 kDa membrane protein distinct from P-glycoprotein. Eur. J. Cancer, 29. 408-415, 1993.
7. Krishnamachary, N., and Center, M. S The MRP gene associated with a non-P-glycoprotein multidrug resistance encodes a 190-kDa membrane bound glycoprotein. Cancer Res., 53: 3658-3661, 1993.
8. Zaman, G J. R , Versantvoort, C. H. M., Smit, J. J. M., Eijdems, E. W. H M., de Haas, M., Smith, A. J., Broxterman, H J., Mulder, N. H., de Vries, E G. E., Baas, F., and Borst, P. Analysis of the expression of MRP, the gene for a new putative transmembrane drug transporter, in human multidrug resistant lung cancer cell lines. Cancer Res., 53: 1747-1750, 1993.
9. Mayer, R., Kartenbeck, J. Büchler, M., Jedlitschky, G., Leier, I., and Keppler, D. 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, 1995
10. Ishikawa, T., Muller, M., Klunemann, C., Schaub, T., and Keppler, D ATP-dependent primary active transport of cysteinyl leukotrienes across liver canalicular membrane. Role of the ATP-dependent transport system for glutathione S-conjugates. J. Biol. Chem , 265: 19279-19286, 1990.
11. Huber, M., Guhlmann, A., Jansen, P. L. M., and Keppler, D. Hereditary defect of hepatobiliary cysteinyl leukotriene elimination in mutant rats with defective hepatic anion excretion. Hepatology, 7: 224-223, 1987.
12. 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
13. Arias, I M., Che, M , Gatmaitan, Z., Leveille, C., Nishida, T., and Pierre, M. ST. The biology of the bile canaliculus Hepatology, 17. 318-329, 1993.
14. Ishikawa, T. The ATP-dependent glutathione S-conjugate export pump. Trends Biochem. Sci , 17: 463-468, 1992
15. Jansen, P. L. M., Peters, W. H., and Lamers, W H. Hereditary chronic conjugated hyperbilirubinemia in mutant rats caused by defective hepatic anion transport. Hepatology, 5. 573-579, 1995.
16. Kuipers, F., Enserink, M., Havinga, R., Van der Steen, A. B., Hardonk, M. J., Fevery, J , and Vonk, R. J. Separate transport systems for biliary secretion of sulfated and unsulfated bile acids in the rat J. Clin. Invest., 81: 1593-1599, 1988.
17. Grant, C. E., Valdimarsson, G., Hipfner, D. R., Almquist, K. C., Cole, S., and Deeley, R. G. Overexpression of multidrug resistance-associated protein (MRP) increases resistance to natural product drugs. Cancer Res., 54: 357-361, 1994.
18. Guhlmann, A., Krauss, K., Oberdorfer, F., Siegel, T., Scheuber, P. H., Muller, J , Csuk-Glanzer, B., Ziegler, S., Ostertag, H., and Keppler, D. Noninvasive assessment of hepatobiliary and renal elimination of cysteinyl leukotrienes by positron emission tomography. Hepatology, 21. 1568-1575, 1995.
19. 4 receptor antagonist. Can. J. Physiol Pharmacol., 67: 17-28, 1989
20. Akerboom, T P M., and Sies H. Transport of glutathione disulfide and glutathione S-coajugates in hepatocyte plasma membrane vesicles. Methods Enzymol , 233: 416-425, 1994.
21. Hall, A. G., Matheson, E., Hickson, I. D., Foster, S. A., and Hogarth, L. Purification of an a class glutathione S-transferase from melphalan-resistant Chinese hamster ovary cells and demonstration of its ability to catalyze melphalan-glutathione adduct formation. Cancer Res., 54: 3369-3372, 1994.
22. Yasmashita, M., and Fenn, J. B. Electrospray ion source. Another variation on the free-yet theme. J. Phys. Chem., 88: 4451-4459, 1984.
23. Jedlitschky, G., Leier, I., Böhme, M., Buchholz, U., Bar-Tana, J., and Keppler, D. Hepatobiliary elimination of the peroxisome proliferator nafenopin by conjugation and subsequent ATP-dependent transport across the canalicular membrane. Biochem. Pharmacol , 48. 1113-1120, 1994.
24. Hande, K., Anthony, L., Hamilton, R., Bennett, R., Sweetman, B., and Branch, R. Identification of etoposide glucuronide as a major metabolite of etoposide in the rat and rabbit. Cancer Res., 48: 1829-1834, 1988.
25. Marschall, H-U., Matern, H., Egestad, B., Matern, S., and Sjövall, J 6α-Glucuronidation of hyodeoxycholic acid by human liver, kidney and small bowel microsomes. Biochim. Biophys. Acta, 921: 392-397, 1987.
26. Kramer, W , and Kurz, G Photolabile derivative of bile salts. Synthesis and suitability for photoaffinity labeling J Lipid Res., 24: 910-923, 1983.
27. 4 export carrier in mastocytoma cells. Eur J Biochem., 220: 599-606, 1994.
28. Böhme, M., Buchler, M., Müller, M , and Keppler, D Differential inhibition by cyclosporins of primary-active ATP-dependent transporters in the hepatocyte canalicular membrane FEBS Lett., 333. 193-196, 1993.
29. Zaman, G J. R., Flens, M J., van Leusden, M. R., de Haas, M , Mulder, H. S., Lankelma, J., Pinedo, H. M., Scheper, R. J., Baas, F., Broxterman, H. J., and Borst, P The human multidrug resistance-associated protein MRP is a plasma membrane drug- efflux pump. Proc. Natl. Acad. Sci USA, 91: 8822-8826, 1994.
30. Gottesman, M M. and Pastan, I. Biochemistry of multidrug resistance mediated by the multidrug transporter. Annu. Rev Biochem., 62: 385-427, 1993.
31. Kobayashi, K., Sogame, Y , Hayashi, K., Nicotera, P., and Orrenius, S. ATP stimulates the uptake of S-dinitrophenylglutathione by rat liver plasma membrane vesicles. FEBS Lett , 240: 55-58, 1988.
32. Akerboom, T. P M., Narayanaswami, V., Kunst, M , and Sies, H. ATP-dependent S-(2,4-dinitrophenyl)glutathione transport in canalicular plasma membrane vesicles from rat liver. J Biol. Chem , 266. 13147-13152, 1991,
33. -) with inherited conjugated hyperbilirubinemia J. Clin. Invest., 90: 227-232, 1992.
34. Kobayashi, K., Komatsu, S., Nishi, T., Hara, H , and Hayashi, K ATP-dependent transport for glucuronides in canalicular plasma membrane vesicles. Biochem. Biophys. Res. Commun., 176. 622-626, 1991.
35. Gosland, M., Tsuboi, C , Hoffman, T., Goodin, S., and Vore, M. 17β-estradiol glucuronide. An inducer of cholestasis and a physiological substrate for the multidrug resistance transporter. Cancer Res., 53. 5382-5385, 1993
36. Green, J A , Vistica, D. T., Young, R. C., Hamilton, T. C., Rogan, A M., and Ozols, R. F Potentiation of melphalan cytotoxicity in human ovarian cancer cell lines by glutathione depletion Cancer Res., 44: 5427-5431, 1984
37. Hamilton, T. C , Winker, M. A , Louie, K. G., Batist, G., Behrens, B C., Tsuruo, T , Grotzinger, K. R., McKoy, W. M., Young, R. C., and Ozols, R. F Augmentation of Adriamycin, melphalan, and cisplatin cytotoxicity in drug-resistant and -sensitive human ovarian carcinoma cell lines by buthionine sulphoximine mediated glutathione depletion. Biochem. Pharmacol., 34: 2583-2586, 1985
38. Lutzky, J., Astor, M B , Taub, R. N., Baker, M. A., Bhalla, K., Gervasoni, J. E., Rosado, M., Stewart, V., Krishna, S., and Hiddenburg, A. A. Role of glutathione and dependent enzymes in anthracyclin-resistant HL60/AR cells. Cancer Res., 49: 4120-4115, 1989
39. 4 receptor antagonist MK 571 specifically modulates MRP associated multidrug resistance. Biochem. Biophys. Res. Commun., 208. 345-352, 1995.
40. Versantvoort, C. H. M , Broxterman, H. J., Bagrij, T., Scheper, R. J., and Twentyman, P. R. Regulation by glutathione of a drug transport in multidrug-resistant human lung tumour cell lines overexpressing multidrug resistance-associated protein. Br J. Cancer, 72: 82-89, 1995.
41. Schneider, E., Yamazaki, H., Sinha, B. K., and Cowan, K. H Buthionine sulphoximine-mediated sensitisation of etoposide-resistant human breast cancer MCF7 cells overexpressing the multidrug resistance-associated protein involves increased drug accumulation. Br. J. Cancer, 71: 738-743, 1995.
42. Zaman, G. J. R., Lankelma, J., van Tellingen, O., Beijnen, J., Dekker, H., Paulusma, C., Oude-Elferink, R. P. J., Baas, F , and Borst, P. Role of glutathione in the export of compounds from cells by the multidrug-resistance-associated protein. Proc Natl. Acad. Sci. USA, 92: 7690-7694, 1995.
43. Dulik, D , Fenselau, C., and Hilton, J. Characterization of melphalan-glutathione adducts whose formation is catalyzed by glutathione transferases. Biochem. Pharmacol., 35. 3405-3409, 1986.
44. Hayes, J. D., and Wolf, C. R. Role of glutathione transferase in drug resistance. In: H Sies and B. Ketterer (eds.), Glutathione Conjugation, Mechanisms and Biological Significance, pp. 315-355 London Academic Press, 1988.