Drug-protein hydrogen bonds govern the inhibition of the ATP hydrolysis of the multidrug transporter P-glycoprotein

Biochemical Pharmacology

Volumn 101, Issue , 2016, Pages 40-53

  Chufan, Eduardo E ^a   Kapoor, Khyati ^a   Ambudkar, Suresh V ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

ABC transporter; Drug binding site; Modulators; Multidrug resistance; Structural motifs

Indexed keywords

ADENOSINE TRIPHOSPHATE; ALANINE; CYSTEINE; ELACRIDAR; ISOLEUCINE; LEUCINE; METHIONINE; MULTIDRUG RESISTANCE PROTEIN; PHENYLALANINE; TARIQUIDAR; TYROSINE; VALINE; ZOSUQUIDAR; ABCB1 PROTEIN, HUMAN; ACRIDINE DERIVATIVE; AGENTS AFFECTING WATER, MOLECULE OR ION TRANSPORT; DIBENZO[A,D]CYCLOHEPTENE DERIVATIVE; LIGAND; MUTANT PROTEIN; QUINOLINE DERIVATIVE; RECOMBINANT PROTEIN; TETRAHYDROISOQUINOLINE DERIVATIVE;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARTICLE; BINDING AFFINITY; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; DOSE RESPONSE; DRUG BINDING SITE; DRUG PROTEIN BINDING; ENZYME INHIBITION; FEMALE; HELA CELL LINE; HUMAN; HUMAN CELL; HYDROGEN BOND; IC50; MOLECULAR MODEL; MUTAGENESIS; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN CROSS LINKING; PROTEIN HYDROLYSIS; PROTEIN MOTIF; PROTEIN TRANSPORT; STEADY STATE; ANIMAL; ANTAGONISTS AND INHIBITORS; BINDING SITE; BIOCATALYSIS; CHEMISTRY; CONFORMATION; DRUG EFFECTS; GENETICS; HYDROLYSIS; LEPIDOPTERA; METABOLISM; MOLECULAR DOCKING;

ACRIDINES; ADENOSINE TRIPHOSPHATE; AMINO ACID MOTIFS; AMINO ACID SUBSTITUTION; ANIMALS; BINDING SITES; BIOCATALYSIS; DIBENZOCYCLOHEPTENES; HELA CELLS; HUMANS; HYDROGEN BONDING; HYDROLYSIS; LEPIDOPTERA; LIGANDS; MEMBRANE TRANSPORT MODULATORS; MODELS, MOLECULAR; MOLECULAR CONFORMATION; MOLECULAR DOCKING SIMULATION; MUTANT PROTEINS; P-GLYCOPROTEINS; QUINOLINES; RECOMBINANT PROTEINS; TETRAHYDROISOQUINOLINES;

EID: 84957573493     PISSN: 00062952     EISSN: 18732968     Source Type: Journal    
DOI: 10.1016/j.bcp.2015.12.007     Document Type: Article

References (35)

1. S.V. Ambudkar, S. Dey, C.A. Hrycyna, M. Ramachandra, I. Pastan, and M.M. Gottesman Biochemical, cellular, and pharmacological aspects of the multidrug transporter Annu. Rev. Pharmacol. Toxicol. 39 1999 361 398
2. E.E. Chufan, H.M. Sim, and S.V. Ambudkar Molecular basis of the polyspecificity of P-glycoprotein (ABCB1): recent biochemical and structural studies Adv. Cancer Res. 125 2015 71 96
3. J.Z. Li, K.F. Jaimes, and S.G. Aller Refined structures of mouse P-glycoprotein Protein Sci. 23 2014 34 46
4. M.S. Jin, M.L. Oldham, Q.J. Zhang, and J. Chen Crystal structure of the multidrug transporter P-glycoprotein from Caenorhabditis elegans Nature 490 2012 566 569
5. P. Szewczyk, H. Tao, A.P. McGrath, M. Villaluz, S.D. Rees, S.C. Lee, and et al. Snapshots of ligand entry, malleable binding and induced helical movement in P-glycoprotein Acta Crystallogr. D: Biol. Crystallogr. 71 2015 732 741
6. R.J.P. Dawson, and K.P. Locher Structure of a bacterial multidrug ABC transporter Nature 443 2006 180 185
7. J.W. Polli, S.A. Wring, J.E. Humphreys, L.Y. Huang, J.B. Morgan, L.O. Webster, and et al. Rational use of in vitro P-glycoprotein assays in drug discovery J. Pharmacol. Exp. Ther. 299 2001 620 628
8. A.H. Dantzig, R.L. Shepard, J. Cao, K.L. Law, W.J. Ehlhardt, T.M. Baughman, and et al. Reversal of P-glycoprotein-mediated multidrug resistance by a potent cyclopropyldibenzosuberane modulator, LY335979 Cancer Res. 56 1996 4171 4179
9. A. Sparreboom, A.S. Planting, R.C. Jewell, M.E. van der Burg, A. van der Gaast, P. de Bruijn, and et al. Clinical pharmacokinetics of doxorubicin in combination with GF120918, a potent inhibitor of MDR1 P-glycoprotein Anticancer Drugs 10 1999 719 728
10. E. Fox, and S.E. Bates Tariquidar (XR9576): a P-glycoprotein drug efflux pump inhibitor Expert Rev. Anticancer Ther. 7 2007 447 459
11. S. Shukla, C.P. Wu, and S.V. Ambudkar Development of inhibitors of ATP-binding cassette drug transporters - present status and challenges Expert Opin. Drug Metab. Toxicol. 4 2008 205 223
12. J.J. Hendrikx, J.S. Lagas, E. Wagenaar, H. Rosing, J.H. Schellens, J.H. Beijnen, and et al. Oral co-administration of elacridar and ritonavir enhances plasma levels of oral paclitaxel and docetaxel without affecting relative brain accumulation Br. J. Cancer 110 2014 2669 2676
13. K. Kapoor, J. Bhatnagar, E.E. Chufan, and S.V. Ambudkar Mutations in intracellular Loops 1 and 3 lead to misfolding of human P-glycoprotein (ABCB1) that can be rescued by cyclosporine A, which reduces its association with chaperone Hsp70 J. Biol. Chem. 288 2013 32622 32636
14. S. Shukla, C. Schwartz, K. Kapoor, A. Kouanda, and S.V. Ambudkar Use of baculovirus BacMam vectors for expression of ABC drug transporters in mammalian cells Drug Metab. Dispos. 40 2012 304 312
15. Z.E. Sauna, M. Muller, X.H. Peng, and S.V. Ambudkar 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 2002 13989 14000
16. M. Ramachandra, S.V. Ambudkar, D. Chen, C.A. Hrycyna, S. Dey, M.M. Gottesman, and et al. Human P-glycoprotein exhibits reduced affinity for substrates during a catalytic transition state Biochemistry 37 1998 5010 5019
17. K.M. Kerr, Z.E. Sauna, and S.V. Ambudkar 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 2001 8657 8664
18. Z.E. Sauna, and S.V. Ambudkar 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 2000 2515 2520
19. S.V. Ambudkar Drug-stimulatable ATPase activity in crude membranes of human MDR1- transfected mammalian cells Methods Enzymol. 292 1998 504 514
20. S. Singh, N.R. Prasad, E.E. Chufan, B.A. Patel, Y.J. Wang, Z.S. Chen, and et al. Design and synthesis of human ABCB1 (P-glycoprotein) inhibitors by peptide coupling of diverse chemical scaffolds on carboxyl and amino termini of (S)-valine-derived thiazole amino acid J. Med. Chem. 57 2014 4058 4072
21. E.E. Chufan, K. Kapoor, H.M. Sim, S. Singh, T.T. Talele, S.R. Durell, and et al. Multiple transport-active binding sites are available for a single substrate on human P-glycoprotein (ABCB1) PLoS One 8 2013 e82463
22. O. Trott, and A.J. Olson AutoDock Vina: improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading J. Comput. Chem. 31 2009 455 461
23. M.F. Sanner Python: a programming language for software integration and development J. Mol. Graphics Modell. 17 1999 57 61
24. Y. Donmez Cakil, N. Khunweeraphong, Z. Parveen, D. Schmid, M. Artaker, G.F. Ecker, and et al. Pore-exposed tyrosine residues of P-glycoprotein are important hydrogen-bonding partners for drugs Mol. Pharmacol. 85 2014 420 428
25. T.W. Loo, and D.M. Clarke Mapping the binding site of the inhibitor tariquidar that stabilizes the first transmembrane domain of P-glycoprotein J. Biol. Chem. 290 2015 29389 29401
26. T.W. Loo, and D.M. Clarke Membrane topology of a cysteine-less mutant of human P-glycoprotein J. Biol. Chem. 270 1995 843 848
27. A.E. Senior, M.K. al-Shawi, and I.L. Urbatsch The catalytic cycle of P-glycoprotein FEBS Lett. 377 1995 285 289
28. M. Scian, M. Acchione, M. Li, and W.M. Atkins Reaction dynamics of ATP hydrolysis catalyzed by P-glycoprotein Biochemistry 53 2014 991 1000
29. T.W. Loo, M.C. Bartlett, and D.M. Clarke Substrate-induced conformational, changes in the transmembrane segments of human P-glycoprotein - direct evidence for the substrate-induced fit mechanism for drug binding J. Biol. Chem. 278 2003 13603 13606
30. E. Dolghih, C. Bryant, A.R. Renslo, and M.P. Jacobson Predicting binding to P-glycoprotein by flexible receptor docking PLoS Comput. Biol. 7 2011
31. H.F. Lodish, A. Berk, C. Kaiser, M. Krieger, A. Bretscher, H.L. Ploegh, and et al. Molecular Cell Biology seventh ed. 2013 W.H. Freeman New York
32. S.V. Ambudkar, C.O. Cardarelli, I. Pashinsky, and W.D. Stein Relation between the turnover number for vinblastine transport and for vinblastine-stimulated ATP hydrolysis by human P-glycoprotein J. Biol. Chem. 272 1997 21160 21166
33. A. Kodan, T. Yamaguchi, T. Nakatsu, K. Sakiyama, C.J. Hipolito, A. Fujioka, and et al. Structural basis for gating mechanisms of a eukaryotic P-glycoprotein homolog Proc. Natl. Acad. Sci. U. S. A. 111 2014 4049 4054
34. R. Chelli, F.L. Gervasio, P. Procacci, and V. Schettino Stacking and T-shape competition in aromatic-aromatic amino acid interactions J. Am. Chem. Soc. 124 2002 6133 6143
35. M.L. O'Mara, and D.P. Tieleman P-glycoprotein models of the apo and ATP-bound states based on homology with Sav1866 and MalK FEBS Lett. 581 2007 4217 4222