Conserved walker A cysteines 431 and 1074 in human P-glycoprotein are accessible to thiol-specific agents in the Apo and ADP-vanadate trapped conformations

Biochemistry

Volumn 52, Issue 41, 2013, Pages 7327-7338

  Sim, Hong May ^a   Bhatnagar, Jaya ^a   Chufan, Eduardo E ^a   Kapoor, Khyati ^a   Ambudkar, Suresh V ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATP-BINDING CASSETTE; CATALYTIC CYCLES; DISULFIDE CROSS-LINKING; EFFLUX TRANSPORTER; METHANETHIOSULFONATE; MULTIDRUG RESISTANCE; NUCLEOTIDE-BINDING DOMAIN; TRANS-MEMBRANE DOMAINS;

ACTIVATION ANALYSIS; AMINO ACIDS; GLYCOPROTEINS; SUBSTRATES;

CONFORMATIONS;

ADENOSINE DIPHOSPHATE; CYSTEINE; MULTIDRUG RESISTANCE PROTEIN; RHODAMINE; THIOL; VANADIC ACID; VERAPAMIL;

ARTICLE; BINDING SITE; CROSS LINKING; PRIORITY JOURNAL; PROTEIN BINDING;

ADENOSINE DIPHOSPHATE; AMINO ACID MOTIFS; AMINO ACID SEQUENCE; BINDING SITES; CONSERVED SEQUENCE; CYSTEINE; HUMANS; MOLECULAR SEQUENCE DATA; P-GLYCOPROTEIN; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; SUBSTRATE SPECIFICITY; SULFHYDRYL COMPOUNDS; VANADATES;

EID: 84885991911     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi4007786     Document Type: Article

References (30)

1. Dean, M. and Annilo, T. (2005) Evolution of the ATP-binding cassette (ABC) transporter superfamily in vertebrates Annu. Rev. Genomics Hum. Genet. 6, 123-142
2. Gottesman, M. M. and Ambudkar, S. V. (2001) Overview: ABC transporters and human disease J. Bioenerg. Biomembr. 33, 453-458
3. Aller, S. G., Yu, J., Ward, A., Weng, Y., Chittaboina, S., Zhuo, R., Harrell, P. M., Trinh, Y. T., Zhang, Q., Urbatsch, I. L., and Chang, G. (2009) Structure of P-glycoprotein reveals a molecular basis for poly-specific drug binding Science 323, 1718-1722
4. Jin, M. S., Oldham, M. L., Zhang, Q., and Chen, J. (2012) Crystal structure of the multidrug transporter P-glycoprotein from Caenorhabditis elegans Nature 490, 566-569
5. Sauna, Z. E., Kim, I. W., Nandigama, K., Kopp, S., Chiba, P., and Ambudkar, S. V. (2007) Catalytic cycle of ATP hydrolysis by P-glycoprotein: Evidence for formation of the E·S reaction intermediate with ATP-γ-S, a nonhydrolyzable analogue of ATP Biochemistry 46, 13787-13799
6. Loo, T. W., Bartlett, M. C., and Clarke, D. M. (2004) Disulfide cross-linking analysis shows that transmembrane segments 5 and 8 of human P-glycoprotein are close together on the cytoplasmic side of the membrane J. Biol. Chem. 279, 7692-7697
7. Loo, T. W., Bartlett, M. C., and Clarke, D. M. (2006) Transmembrane segment 7 of human P-glycoprotein forms part of the drug-binding pocket Biochem. J. 399, 351-359
8. Loo, T. W. and Clarke, D. M. (1995) Membrane topology of a cysteine-less mutant of human P-glycoprotein J. Biol. Chem. 270, 843-848
9. Sauna, Z. E., Muller, M., Peng, X. H., and Ambudkar, S. V. (2002) Importance of the conserved Walker B glutamate residues, 556 and 1201, for the completion of the catalytic cycle of ATP hydrolysis by human P-glycoprotein (ABCB1) Biochemistry 41, 13989-14000
10. Ramachandra, M., Ambudkar, S. V., Chen, D., Hrycyna, C. A., Dey, S., Gottesman, M. M., and Pastan, I. (1998) Human P-glycoprotein exhibits reduced affinity for substrates during a catalytic transition state Biochemistry 37, 5010-5019
11. Kerr, K. M., Sauna, Z. E., and Ambudkar, S. V. (2001) Correlation between steady-state ATP hydrolysis and vanadate-induced ADP trapping in human P-glycoprotein. Evidence for ADP release as the rate-limiting step in the catalytic cycle and its modulation by substrates J. Biol. Chem. 276, 8657-8664
12. Shukla, S., Schwartz, C., Kapoor, K., Kouanda, A., and Ambudkar, S. V. (2012) Use of Baculovirus BacMam Vectors for Expression of ABC Drug Transporters in Mammalian Cells Drug Metab. Dispos. 40, 304-312
13. Ambudkar, S. V. (1998) Drug-stimulatable ATPase activity in crude membranes of human MDR1-transfected mammalian cells Methods Enzymol. 292, 504-514
14. Altschul, S. F., Madden, T. L., Schaffer, A. A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D. J. (1997) Gapped BLAST and PSI-BLAST: A new generation of protein database search programs Nucleic Acids Res. 25, 3389-3402
15. Laskowski, R. A., Macarthur, M. W., Moss, D. S., and Thornton, J. M. (1993) Procheck: A Program to Check the Stereochemical Quality of Protein Structures J. Appl. Crystallogr. 26, 283-291
16. Emsley, P. and Cowtan, K. (2004) Coot: Model-building tools for molecular graphics Acta Crystallogr. D60, 2126-2132
17. Ohnuma, S., Chufan, E., Nandigama, K., Jenkins, L. M. M., Durell, S. R., Appella, E., Sauna, Z. E., and Ambudkar, S. V. (2011) Inhibition of Multidrug Resistance-Linked P-Glycoprotein (ABCB1) Function by 5′- Fluorosulfonylbenzoyl 5′-Adenosine: Evidence for an ATP Analogue That Interacts with Both Drug-Substrate-and Nucleotide-Binding Sites Biochemistry 50, 3724-3735
18. Brooks, B. R., Brooks, C. L., Mackerell, A. D., Nilsson, L., Petrella, R. J., Roux, B., Won, Y., Archontis, G., Bartels, C., Boresch, S., Caflisch, A., Caves, L., Cui, Q., Dinner, A. R., Feig, M., Fischer, S., Gao, J., Hodoscek, M., Im, W., Kuczera, K., Lazaridis, T., Ma, J., Ovchinnikov, V., Paci, E., Pastor, R. W., Post, C. B., Pu, J. Z., Schaefer, M., Tidor, B., Venable, R. M., Woodcock, H. L., Wu, X., Yang, W., York, D. M., and Karplus, M. (2009) CHARMM: The Biomolecular Simulation Program J. Comput. Chem. 30, 1545-1614
19. Trott, O. and Olson, A. J. (2010) Software News and Update AutoDock Vina: Improving the Speed and Accuracy of Docking with a New Scoring Function, Efficient Optimization, and Multithreading J. Comput. Chem. 31, 455-461
20. Sanner, M. F. (1999) Python: A programming language for software integration and development J. Mol. Graphics Modell. 17, 57-61
21. O'Mara, M. L. and Tieleman, D. P. (2007) P-glycoprotein models of the apo and ATP-bound states based on homology with Sav1866 and MalK FEBS Lett. 581, 4217-4222
22. Dawson, R. J. and Locher, K. P. (2006) Structure of a bacterial multidrug ABC transporter Nature 443, 180-185
23. Schmitt, L., Benabdelhak, H., Blight, M. A., Holland, I. B., and Stubbs, M. T. (2003) Crystal structure of the nucleotide-binding domain of the ABC-transporter haemolysin B: Identification of a variable region within ABC helical domains J. Mol. Biol. 330, 333-342
24. Loo, T. W., Bartlett, M. C., and Clarke, D. M. (2003) Simultaneous binding of two different drugs in the binding pocket of the human multidrug resistance P-glycoprotein J. Biol. Chem. 278, 39706-39710
25. Wen, P. C., Verhalen, B., Wilkens, S., McHaourab, H. S., and Tajkhorshid, E. (2013) On the Origin of Large Flexibility of P-glycoprotein in the Inward-facing State J. Biol. Chem. 288, 19211-19220
26. Loo, T. W. and Clarke, D. M. (1995) Covalent modification of human P-glycoprotein mutants containing a single cysteine in either nucleotide-binding fold abolishes drug-stimulated ATPase activity J. Biol. Chem. 270, 22957-22961
27. Vigano, C., Julien, M., Carrier, I., Gros, P., and Ruysschaert, J. M. (2002) Structural and functional asymmetry of the nucleotide-binding domains of P-glycoprotein investigated by attenuated total reflection Fourier transform infrared spectroscopy J. Biol. Chem. 277, 5008-5016
28. Urbatsch, I. L., Gimi, K., Wilke-Mounts, S., Lerner-Marmarosh, N., Rousseau, M. E., Gros, P., and Senior, A. E. (2001) Cysteines 431 and 1074 are responsible for inhibitory disulfide cross-linking between the two nucleotide-binding sites in human P-glycoprotein J. Biol. Chem. 276, 26980-26987
29. Oldham, M. L. and Chen, J. (2011) Snapshots of the maltose transporter during ATP hydrolysis Proc. Natl. Acad. Sci. U.S.A. 108, 15152-15156
30. Loo, T. W. and Clarke, D. M. (2000) Drug-stimulated ATPase activity of human P-glycoprotein is blocked by disulfide cross-linking between the nucleotide-binding sites J. Biol. Chem. 275, 19435-19438