Purification of the human apical conjugate export pump MRP2: Reconstitution and functional characterization as substrate-stimulated ATPase

European Journal of Biochemistry

Volumn 265, Issue 1, 1999, Pages 281-289

  Hagmann, Wolfgang ^a   Nies, Anne T ^a   König, Jörg ^a   Frey, Manfred ^a   Zentgraf, Hanswalter ^a   Keppler, Dietrich ^a  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

ATPase; Immunoaffinity chromatography; Multidrug resistance protein 2 (MRP2); Photoaffinity labelling; Proteoliposomes

Indexed keywords

ADENOSINE TRIPHOSPHATASE; MULTIDRUG RESISTANCE PROTEIN; MULTIDRUG RESISTANCE PROTEIN 2; UNCLASSIFIED DRUG;

ARTICLE; ENZYME ACTIVITY; HUMAN; HUMAN CELL; MULTIDRUG RESISTANCE; PHOTOAFFINITY LABELING; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN PURIFICATION; PROTEOLIPOSOME;

ADENOSINE TRIPHOSPHATASES; ADENOSINE TRIPHOSPHATE; AZIDES; BIOLOGICAL TRANSPORT; CELL COMPARTMENTATION; CELL POLARITY; CLONING, MOLECULAR; DNA, COMPLEMENTARY; GLUTATHIONE; GLUTATHIONE DISULFIDE; HUMANS; LEUKOTRIENE C4; MEMBRANE TRANSPORT PROTEINS; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; P-GLYCOPROTEINS; PHOTOAFFINITY LABELS; PROTEOLIPIDS; RECOMBINANT PROTEINS; SOLUBILITY;

EID: 0033214154     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1432-1327.1999.00735.x     Document Type: Article

References (54)

1. 1. Cole, S.P., Bhardwaj, G., Gerlach, J.H., Mackie, J.E., Grant, C.E., Almquist, K.C., Stewart, A.J., Kurz, E.U., Duncan, A.M. & Deeley, R.G. (1992) Overexpression of a transporter gene in a multidrug-resistant human lung cancer cell line. Science 258, 1650-1654.
2. 2. Paulusma, C.C., Bosma, P.J., Zaman, G.J., Bakker, C.T., Otter, M., Scheffer, G.L., Scheper, R.J., Borst, P. & Oude Elferink, R.P. (1996) Congenital jaundice in rats with a mutation in a multidrug resistance-associated protein gene. Science 271, 1126-1128.
3. 3. Büchler, M., König, J., Brom, M., Kartenbeck, J., Spring, H., Horie, T. & 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.
4. 4. Taniguchi, K., Wada, M., Kohno, K., Nakamura, T., Kawabe, T., Kawakami, M., Kagotani, K., Okumura, K., Akiyama, S. & Kuwano, M. (1996) A human canalkular multispecific organic anion transporter (cMOAT) gene is overexpressed in cisplatin-resistant human cancer cell lines with decreased drug accumulation. Cancer Res. 56, 4124-4129.
5. 5. Evers, R., Kool, M., van Deemter, L., Janssen, H., Calafat, J., Oomen, L.C., Paulusma, C.C., Oude Elferink, R.P., Baas, F., Schinkel, A.H. & Borst, P. (1998) Drug export activity of the human canalicular multispecific organic anion transporter in polarized kidney MDCK cells expressing cMOAT (MRP2) cDNA. J. Clin. Invest. 101, 1310-1319.
6. 6. König, J., Rost, D., Cui, Y. & Keppler, D. (1999) Characterization of the human multidrug resistance protein isoform MRP3 localized to the basolateral hepatocyte membrane. Hepatology 29, 1156-1163.
7. 7. Hirohashi, T., Suzuki, H. & Sugiyama, Y. (1999) Characterization of the transport properties of cloned rat multidrug resistance-associated protein 3 (MRP3). J. Biol. Chem. 274, 15181-15185.
8. 8. Grant, C.E., Valdimarsson, G., Hipfner, D.R., Almquist, K.C., Cole, S.P. & Deeley, R.G. (1994) Overexpression of multidrug resistance-associated protein (MRP) increases resistance to natural product drugs. Cancer Res. 54, 357-361.
9. 9. Zaman, G.J., Lankelma, J., van Tellingen, O., Beijnen, J., Dekker, H., Paulusma, C., Oude Elferink, R.P., Baas, F. & Borst, P. (1995) Role of glutathione in the export of compounds from cells by the multidrug-resistance-associated protein. Proc. Natl Acad. Sci. USA 92, 7690-7694.
10. 10. Cui, Y., König, J., Buchholz, U., Spring, H., Leier, I. & Keppler, D. (1999) Drug resistance and ATP-dependent conjugate transport mediated by the apical multidrug resistance protein, MRP2, permanently expressed in human and canine cells. Mol. Pharmacol. 55, 929-937.
11. 11. Jedlitschky, G., Leier, I., Buchholz, U., Center, M. & Keppler, D. (1994) ATP-dependent transport of glutathione S-conjugates by the multidrug resistance-associated protein. Cancer Res. 54, 4833-4836.
12. 4 and structurally related conjugates. J. Biol. Chem. 269, 27807-27810.
13. 13. Müller, M., Meijer, C., Zaman, G.J., Borst, P., Scheper, R.J., Mulder, N.H., de Vries, E.G. & Jansen, P.L. (1994) 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.
14. 14. Loe, D.W., Almquist, K.C., Cole, S.P. & Deeley, R.G. (1996) ATP-dependent 17 beta-estradiol 17-(beta-D-glucuronide) transport by multidrug resistance protein (MRP). Inhibition by cholestatic steroids. J. Biol. Chem. 271, 9683-9689.
15. 4 and chemotherapeutic agents in membrane vesicles. Demonstration of glutathione-dependent vincristine transport. J. Biol. Chem. 271, 9675-9682.
16. 16. Leier, I., Jedlitschky, G., Buchholz, U., Center, M., Cole, S.P., Deeley, R.G. & Keppler, D. (1996) ATP-dependent glutathione disulphide transport mediated by the MRP gene-encoded conjugate export pump. Biochem. J. 314, 433-437.
17. 4 transport by co-expression of both half-molecules of human multidrug resistance protein in insect cells. J. Biol. Chem. 271, 27782-27787.
18. 18. Chang, X.B., Hou, Y.X. & Riordan, J.R. (1997) ATPase activity of purified multidrug resistance-associated protein. J. Biol. Chem. 272, 30962-30968.
19. 19. Chang, X.B., Hou, Y.X. & Riordan, J.R. (1998) Stimulation of ATPase activity of purified multidrug resistance-associated protein by nucleoside diphosphates. J. Biol. Chem. 273, 23844-23848.
20. 20. Jedlitschky, G., Leier, I., Buchholz, U., Hummel-Eisenbeiss, J., Burchell, B. & Keppler, D. (1997) ATP-dependent transport of bilirubin glucuronides by the multidrug resistance protein MRP1 and its hepatocyte canalicular isoform MRP2. Biochem. J. 327, 305-310.
21. 21. van Aubel, R.A., van Kuijck, M.A., Koenderink, J.B., Deen, P.M., van Os, C.H. & Russel, F.G. (1998) Adenosine triphosphate-dependent transport of anionic conjugates by the rabbit multidrug resistance-associated protein Mrp2 expressed in insect cells. Mol. Pharmacol. 53, 1062-1067.
22. 22. Chen, W.Y., Bailey, E.C., McCune, S.L., Dong, J.Y. & Townes, T.M. (1997) Reactivation of silenced, virally transduced genes by inhibitors of histone deacetylase. Proc. Natl Acad. Sci. USA 94, 5798-5803.
23. 23. Schneider, C., Newman, R.A., Sutherland, D.R., Asser, U. & Greaves, M.F. (1982) A one-step purification of membrane proteins using a high efficiency immunomatrix. J. Biol. Chem. 257, 10766-10769.
24. 24. Zentgraf, H., Frey, M., Schwinn, S., Tessmer, C., Willemann, B., Samstag, Y. & Velhagen, I. (1995) Detection of histidine-tagged fusion proteins by using a high-specific mouse monoclonal anti-histidine tag antibody. Nucleic Acids Res. 23, 3347-3348.
25. 25. Büchler, M., Böhme, M., Ortlepp, H. & Keppler, D. (1994) Functional reconstitution of ATP-dependent transporters from the solubilized hepatocyte canalicular membrane. Eur. J. Biochem. 224, 345-352.
26. 26. Ambudkar, S.V., Lelong, I.H., Zhang, J., Cardarelli, C.O., Gottesman, M.M. & Pastan, I. (1992) Partial purification and reconstitution of the human multidrug-resistance pump: characterization of the drug-stimulatable ATP hydrolysis. Proc. Natl Acad Sci. USA 89, 8472-8476.
27. 27. Bradford, M.M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254.
28. 4 express the MRP1 gene-encoded conjugate export pump. Biol. Chem. 379, 1121-1126.
29. 29. Wigge, P.A., Jensen, O.N., Holmes, S., Soues, S., Mann, M. & Kilmartnin, J.V. (1998) Analysis of the Saccharomyces spindle pole by matrix-assisted laser desorption/ionization (MALDI) mass spectrometry. J. Cell Biol. 141, 967-977.
30. 30. Horigome, T. & Sugano, H. (1983) A rapid method for removal of detergents from protein solution. Anal. Biochem. 130, 393-396.
31. 31. Loo, T.W. & Clarke, D.M. (1995) Rapid purification of human P-glycoprotein mutants expressed transiently in HEK 293 cells by nickel-chelate chromatography and characterization of their drug-stimulated ATPase activities. J. Biol. Chem. 270, 21449-21452.
32. 32. Keppler, D. & Kartenbeck, J. (1996) The canalicular conjugate export pump encoded by the cmrp/cmoat gene. Prog. Liver Dis. 14, 55-67.
33. 33. Schaub, T.P., Kartenbeck, J., König, J., Vogel, O., Witzgall, R., Kriz, W. & Keppler, D. (1997) Expression of the conjugate export pump encoded by the mrp2 gene in the apical membrane of kidney proximal tubules. J. Am. Soc. Nephrol. 8, 1213-1221.
34. 34. Cornwell, M.M., Tsuruo, T., Gottesman, M.M. & Pastan, I. (1987) ATP-binding properties of P glycoprotein from multidrug-resistant KB cells. FASEB J. 1, 51-54.
35. 35. Urbatsch, I.L., Sankaran, B., Weber, J. & Senior, A.E. (1995) P-glycoprotein is stably inhibited by vanadate-induced trapping of nucleotide at a single catalytic site. J. Biol. Chem. 270, 19383-19390.
36. 36. Taguchi, Y., Yoshida, A., Takada, Y., Komano, T. & Ueda, K. (1997) Anti-cancer drugs and glutathione stimulate vanadate-induced trapping of nucleotide in multidrug resistance-associated protein (MRP). FEBS Lett. 401, 11-14.
37. 37. Szabo, K., Welker, E., Bakos, E., Muller, M., Roninson, I., Varadi, A. & Sarkadi, B. (1998) Drug-stimulated nucleotide trapping in the human multidrug transporter MDRI. Cooperation of the nucleotide binding domains. J. Biol. Chem. 273, 10132-10138.
38. 38. Hrycyna, C.A., Ramachandra, M., Ambudkar, S.V., Ko, Y.H., Pedersen, P.L., Pastan, I. & Gottesman, M.M. (1998) Mechanism of action of human P-glycoprotein ATPase activity. Photochemical cleavage during a catalytic transition state using orthovanadate reveals cross-talk between the two ATP sites. J. Biol. Chem. 273, 16631-16634.
39. 39. Urbatsch, I.L., al-Shawi, M.K. & Senior, A.E. (1994) Characterization of the ATPase activity of purified Chinese hamster P-glycoprotein. Biochemistry 33, 7069-7076.
40. 40. Sharom, F.J., Yu, X., Chu, J.W. & Doige, C.A. (1995) Characterization of the ATPase activity of P-glycoprotein from multidrug-resistant Chinese hamster ovary cells. Biochem. J. 308, 381-390.
41. 41. Dong, B., Horowitz, D.S., Kobayashi, R. & Krainer, A.R. (1993) Purification and cDNA cloning of HeLa cell p54nrb, a nuclear protein with two RNA recognition motifs and extensive homology to human splicing factor PSF and Drosophila NONA/BJ6. Nucleic Acids. Res. 21, 4085-4092.
42. 42. Patton, J.G., Porro, E.B., Galceran, J., Tempst, P. & Nadal-Ginard, B. (1993) Cloning and characterization of PSF, a novel pre-mRNA splicing factor. Genes Dev. 7, 393-406.
43. 43. Müller, K.M., Arndt, K.M., Bauer, K. & Plückthun, A. (1998) Tandem immobilized metal-ion affinity chromatography/immunoaffinity purification of His-tagged proteins-evaluation of two anti-His-tag monoclonal antibodies. Anal. Biochem. 259, 54-61.
44. 44. Sun, H., Molday, R.S. & Nathans, J. (1999) Retinal stimulates ATP hydrolysis by purified and reconstituted ABCR, the photoreceptor-specific ATP-binding cassette transporter responsible for Stargardt disease. J. Biol. Chem. 274, 8269-8281.
45. 45. Böhme, M., Müller, M., Leier, I., Jedlitschky, G. & Keppler, D. (1994) Cholestasis caused by inhibition of the adenosine triphosphate-dependent bile salt transport in rat liver. Gastroenterology 107, 255-265.
46. 46. Shapiro, A.B. & Ling, V. (1994) ATPase activity of purified and reconstituted P-glycoprotein from Chinese hamster ovary cells. J. Biol. Chem. 269, 3745-3754.
47. 47. Ramachandra, M., Ambudkar, S.V., Chen, D., Hrycyna, C.A., Dey, S., Gottesman, M.M. & Pastan, I. (1998) Human P-glycoprotein exhibits reduced affinity for substrates during a catalytic transition state. Biochemistry 37, 5010-5019.
48. 48. Paulusma, C.C., Geer, M.A., Evers, R., Heijn, M., Ottenhoff, R., Borst, P. & Oude Elferink, R.P. (1999) Canalicular multispecific organic anion transporter/multidrug resistance protein 2 mediates low-affinity transport of reduced glutathione. Biochem. J. 338, 393-401.
49. 49. Kast, C. & Gros, P. (1997) Topology mapping of the amino-terminal half of multidrug resistance-associated protein by epitope insertion and immunofluorescence. J. Biol. Chem. 272, 26479-26487.
50. 50. Zhu, Q., Sun, H. & Center, M.S. (1997) Functional analysis of the nucleotide binding domains of the multidrug resistance protein (MRP). Oncol. Res. 9, 229-236.
51. 51. Bakos, E., Evers, R., Szakacs, G., Tusnady, G.E., Welker, E., Szabo, K., de Haas, M., van Deemter, L., Borst, P., Varadi, A. & Sarkadi, B. (1998) Functional multidrug resistance protein (MRP1) lacking the N-terminal transmembrane domain. J. Biol. Chem. 273, 32167-32175.
52. 4. J. Biol. Chem. 273, 10733-10740.
53. 53. Shapiro, A.B. & Ling, V. (1995) Reconstitution of drug transport by purified P-glycoprotein. J. Biol. Chem. 270, 16167-16175.
54. 54. Ambudkar, S.V., Lelong, I.H., Zhang, J. & Cardarelli, C.O. (1998) Purification and reconstitution of human P-glycoprotein. Methods Enzymol. 292, 492-504.