Nucleotides and transported substrates modulate different steps of the ATPase catalytic cycle of MRP1 multidrug transporter

Biochemical Journal

Volumn 380, Issue 2, 2004, Pages 549-560

  Kern, András ^a   Szentpétery, Zsófia ^a   Liliom, Károly ^a   Bakos, Éva ^a   Sarkadi, Balázs ^b   Váradi, András ^a  

^a INSTITUTE OF ENZYMOLOGY   (Hungary)

^b INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

Author keywords

ATP binding cassette transporter (ABC transporter); ATPase catalytic cycle; Multidrug resistance associated protein 1 (MRP1); Pre and post hydrolytic intermediate; Transition state; Vanadate cleavage

Indexed keywords

ADENOSINETRIPHOSPHATE; CATALYSIS; CELLS; COMPLEXATION; ENZYMES; HYDROLYSIS; METABOLITES; SUBSTRATES; TUMORS;

ATP-BINDING CASSETTE (ABC); CLEAVAGE REACTIONS; NUCLEOTIDES; TRANSITION STATES;

BIOCHEMISTRY;

ABC TRANSPORTER; ADENOSINE TRIPHOSPHATASE; GLYCOPROTEIN P; MULTIDRUG RESISTANCE PROTEIN 1; NUCLEOTIDE; ORTHOVANADIC ACID;

ALLOSTERISM; ARTICLE; BINDING AFFINITY; BINDING SITE; CATALYSIS; HYDROLYSIS; NONHUMAN; PHOTOOXIDATION; PRIORITY JOURNAL; PROTEIN DEGRADATION;

ADENOSINE TRIPHOSPHATASES; ADENOSINE TRIPHOSPHATE; ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; CELL LINE; HUMANS; HYDROLYSIS; MEMBRANE PROTEINS; MODELS, BIOLOGICAL; MODELS, CHEMICAL; MODELS, GENETIC; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; NUCLEOTIDES; OXIDATIVE STRESS; PROTEIN FOLDING; SPODOPTERA; VANADATES;

EID: 2942705747     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20031607     Document Type: Article

References (40)

1. Cremo, C. R., Grammer, J. C. and Yount, R. G. (1989) Direct chemical evidence that serine 180 in the glycine-rich loop of myosin binds to ATP. J. Biol. Chem. 264, 6608-6611
2. Grammer, J. C., Loo, J. A., Edmonds, C. G., Cremo, C. R. and Yount, R. G. (1996) Chemistry and mechanism of vanadate-promoted photooxidative cleavage of myosin. Biochemistry 35, 15582-15592
3. Smith, C. A. and Rayment, I. (1996) X-ray structure of the magnesium(II)-ADP-vanadate complex of the Dictyostelium discoideum myosin motor domain to 1.9 Å resolution. Biochemistry 35, 5404-5417
4. Fisher, A. J., Smith, C. A., Thoden, J. B., Smith, R., Sutoh, K., Holden, H. M. and Rayment, I. (1995) X-ray structures of the myosin motor domain of Dictyostelium discoideum complexed with MgADP.BeFx and MgADP.AIF4-. Biochemistry 34, 8960-8972
5. Daoud, R., Julien, M., Gros, P. and Georges, E. (2001) Major photoaffinity drug binding sites in multidrug resistance protein 1 (MRP1) are within transmembrane domains 10-11 and 16-17. J. Biol. Chem. 276, 12324-12330
6. Haimeur, A., Deeley, R. G. and Cole, S. P. C. (2002) Charged amino acids in the sixth transmembrane helix of multidrug resistance protein 1 (MRP1/ABCC1) are critical determinants of transport activity. J. Biol. Chem. 277, 41326-41333
7. Ito, K., Olsen, S. L., Qiu, W., Deeley, R. G. and Cole, S. P. C. (2001) Mutation of a single conserved tryptophan in multidrug resistance protein 1 (MRP1/ABCC1) results in loss of drug resistance and selective loss of organic anion transport. J. Biol. Chem. 276, 15616-15624
8. Ren, X. Q., Furukawa, T., Aoki, S., Nakajima, T., Sumizawa, T., Haraguchi, M., Chen, Z. S., Kobayashi, M. and Akiyama, S. (2001) Glutathione-dependent binding of a photoaffinity analog of agosterol A to the C-terminal half of human multidrug resistance protein. J. Biol. Chem. 276, 23197-23206
9. Karwatsky, J., Daoud, R., Cai, J., Gros, P. and Georges, E. (2003) Binding of a photoaffinity analogue of glutathione to MRP1 (ABCC1) within two cytoplasmic regions (L0 and L1) as well as transmembrane domains 10-11 and 16-17. Biochemistry 42, 3286-3294
10. Hopfner, K. P., Karcher, A., Shin, D. S., Craig, L., Arthur, L. M., Carney, J. P. and Tainer, J. A. (2000) Structural biology of Rad50 ATPase: ATP-driven conformational control in DNA double-strand break repair and the ABC-ATPase superfamily. Cell 101, 789-800
11. Locher, K. P., Lee, A. T. and Rees, D. C. (2002) The E. coli BtuCD structure: a framework for ABC transporter architecture and mechanism. Science 296, 1091-1098
12. Smith, P. C., Karpowich, N., Millen, L., Moody, J. E., Rosen, J., Thomas, P. J. and Hunt, J. F. (2002) ATP binding to the motor domain from an ABC transporter drives formation of a nucleotide sandwich dimer. Mol. Cell 10, 139-149
13. Chen, J., Lu, G., Lin, J., Davidson, A. L. and Quiocho, F. A. (2003) A tweezers-like motion of the ATP-binding cassette dimer in an ABC transport cycle. Mol. Cell 12, 651-661
14. Chang, G. (2003) Structure of MsbA from Vibrio cholera: A multidrug resistance ABC transporter homolog in closed conformation. J. Mol. Biol. 330, 419-430
15. Urbatsch, I. L., Sankaran, B., Weber, J. and 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
16. Sankaran, B., Bhagat, S. and Senior, A. E. (1997) Inhibition of P-glycoprotein ATPase activity by beryllium fluoride. Biochemistry 36, 6847-6853
17. Taguchi, Y., Yoshida, A., Takada, Y., Komano, T. and 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
18. Szabó, K., Welker, E., Bakos, É., Müller, M., Roninson, I., Váradi, A. and Sarkadi, B. (1998) Drug-stimulated nucleotide trapping in the human multidrug transporter MDR1: cooperation of the nucleotide binding domains. J. Biol. Chem. 273, 10132-10138
19. Urbatsch, I. L., Sankaran, B., Bhagat, S. and Senior, A. E. (1995) Both P-glycoprotein nucleotide-binding sites are catalytically active. J. Biol. Chem. 270, 26956-26961
20. Sauna, Z. E. and Ambudkar, S. V. (2000) Evidence for a requirement for ATP hydrolysis at two distinct steps during a single turnover of the catalytic cycle of human P-glycoprotein. Proc. Natl. Acad. Sci. U.S.A. 97, 2515-2520
21. Hrycyna, C. A., Ramachandra, M., Ambudkar, S. V., Ko, Y. H., Pedersen, P. L., Pastan, I. and 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
22. Hou, Y. X., Cui, L., Riordan, J. R. and Chang, X. B. (2000) Allosteric interactions between the two non-equivalent nucleotide binding domains of multidrug resistance protein MRP1. J. Biol. Chem. 275, 20280-20287
23. Gao, M., Cui, H. R., Loe, D. W., Grant, C. E., Almquist, K. C., Cole, S. P. C. and Deeley, R. G. (2000) Comparison of the functional characteristics of the nucleotide binding domains of multidrug resistance protein 1. J. Biol. Chem. 275, 13098-13108
24. Nagata, K., Nishitani, M., Matsuo, M., Kioka, N., Amachi, T. and Ueda, K. (2000) Nonequivalent nucleotide trapping in the two nucleotide binding folds of the human multidrug resistance protein MRP1. J. Biol. Chem. 275, 17626-17630
25. Hou, Y. X., Cui, L., Riordan, J. R. and Chang, X. B. (2002) ATP binding to the first nucleotide-binding domain of multidrug resistance protein MRP1 increases binding and hydrolysis of ATP and trapping of ADP at the second domain. J. Biol. Chem. 277, 5110-5119
26. Manciu, L., Chang, X. B., Buyse, F., Hou, Y. X., Gustot, A., Riordan, J. R. and Ruysschaert, J. M. (2003) Intermediate structural states involved in MRP1-mediated drug transport: role of glutathione. J. Biol. Chem. 278, 3347-3356
27. Hou, Y. X., Riordan, J. R. and Chang, X. B. (2003) ATP binding, not hydrolysis, at the first nucleotide-binding domain of multidrug resistance-associated protein MRP1 enhances ADP·Vi trapping at the second domain. J. Biol. Chem. 278, 3599-3605
28. 4 transport. J. Biol. Chem. 278, 30764-30771
29. Bakos, É., Hegedüs, T., Holló, Z., Welker, E., Tusnády, G. E., Zaman, G. J. R., Flens, M. J., Váradi, A. and Sarkadi, B. (1996) Membrane topology and glycosylation of the human multidrug resistance-associated protein. J. Biol. Chem. 271, 12322-12326
30. Müller, M., Bakos, É., Welker, E., Váradi, A., Germann, U. A., Gottesman, M. M., Morse, B. S., Roninson, I. B. and Sarkadi, B. (1996) Altered drug-stimulated ATPase activity in mutants of the human multidrug resistance protein. J. Biol. Chem. 271, 1877-1883
31. Sarkadi, B., Price, E. M., Boucher, R. C., Germann, U. A. and Scarborough, G. A. (1992) Expression of the human multidrug resistance cDNA in insect cells generates a high activity drug-stimulated membrane ATPase. J. Biol. Chem. 267, 4854-4858
32. Bakos, É., Evers, R., Sinkó, E., Váradi, A., Borst, P. and Sarkadi, B. (2000) Interactions of the human multidrug resistance proteins MRP1 and MRP2 with organic anions. Mol. Pharmacol. 57, 760-768
33. Goodno, C. C. (1982) Myosin active-site trapping with vanadate ion. Methods Enzymol. 85, 116-123
34. Bakos, É., Evers, R., Szakács, G., Tusnády, G. E., Welker, E., Szabó, K., de Haas, M., van Deemter, L., Borst, P., Váradi, A. and Sarkadi, B. (1998) Functional multidrug resistance protein (MRP1) lacking the N-terminal transmembrane domain. J. Biol. Chem. 273, 32167-32175
35. Flens, M. J., Izquerido, M. A., Scheffer, G. L., Fritz, J. M., Meijer, C. J. L. M., Scheper, R. J. and Zaman, G. J. R. (1994) Immunochemical detection of the multidrug resistance-associated protein MRP in human multidrug-resistant tumor cells by monoclonal antibodies. Cancer Res. 54, 4557-4563
36. Tusnády, G. E., Bakos, É., Váradi, A. and Sarkadi, B. (1997) Membrane topology distinguishes a subfamily of the ATP-binding cassette (ABC) transporters. FEBS Lett. 402, 1-3
37. Holló, Z., Homolya, L., Hegedüs, T. and Sarkadi, B. (1996) Transport properties of the multidrug resistance-associated protein (MRP) in human tumour cells. FEBS Lett. 383, 99-104
38. Rosenberg, M. F., Velarde, G., Ford, R. C., Martin, C., Berridge, G., Kerr, I. D., Callaghan, R., Schmidlin, A., Wooding, C., Linton, K. J. and Higgins, C. F. (2001) Repacking of the transmembrane domains of P-glycoprotein during the transport ATPase cycle. EMBO J. 20, 5615-5625
39. Rosenberg, M. F., Kamis, A. B., Callaghan, R., Higgins, C. F. and Ford, R. C. (2003) Three-dimensional structures of the mammalian multidrug resistance P-glycoprotein demonstrate major conformational changes in the transmembrane domains upon nucleotide binding. J. Biol. Chem. 278, 8294-8299
40. Chang, X. B., Hou, Y. X. and Riordan, J. R. (1997) ATPase activity of purified multidrug resistance-associated protein. J. Biol. Chem. 272, 30962-30968