Binding of modulators to mouse and human multidrug resistance P-glycoprotein. A computational study

Journal of Molecular Graphics and Modelling

Volumn 46, Issue , 2013, Pages 10-21

  Jara, Gabriel E ^b   Vera, D Mariano A ^a   Pierini, Adriana B ^b  

^a UNIVERSIDAD NACIONAL DE MAR DEL PLATA   (Argentina)

^b Instituto de Quimica Fisica de los Materiales Medio Ambiente y Energia   (Argentina)

Author keywords

ABC transporters; Free energies of binding; MDR; Molecular docking; Molecular dynamics; P glycoprotein

Indexed keywords

ABC TRANSPORTER; CLASSICAL MOLECULAR DYNAMICS; EXPERIMENTAL ACTIVITIES; HUMAN MULTIDRUG RESISTANCE; MDR; MOLECULAR DOCKING; P-GLYCOPROTEIN; RELATIVE BINDING ENERGIES;

ACTIVATION ANALYSIS; GLYCOPROTEINS; MAMMALS; MOLECULAR DYNAMICS; MOLECULAR MODELING;

MODULATORS;

MULTIDRUG RESISTANCE PROTEIN; PROPAFENONE; RHODAMINE 123; TARIQUIDAR;

ARTICLE; CRYSTAL STRUCTURE; DRUG BINDING SITE; DRUG INHIBITION; HUMAN; HYDROPHOBICITY; MOLECULAR DOCKING; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION;

ABC TRANSPORTERS; FREE ENERGIES OF BINDING; MDR; MOLECULAR DOCKING; MOLECULAR DYNAMICS; P-GLYCOPROTEIN;

AMINO ACID MOTIFS; ANIMALS; BINDING SITES; DRUG RESISTANCE, MULTIPLE; DRUG RESISTANCE, NEOPLASM; HUMANS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; MICE; MOLECULAR DOCKING SIMULATION; MOLECULAR DYNAMICS SIMULATION; P-GLYCOPROTEINS; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; QUINOLINES; RHODAMINE 123; THERMODYNAMICS;

EID: 84884937355     PISSN: 10933263     EISSN: 18734243     Source Type: Journal    
DOI: 10.1016/j.jmgm.2013.09.001     Document Type: Article

References (83)

1. M.M. Gottesman, T. Fojo, and S.E. Bates Multidrug resistance in cancer: role of ATP-dependent transporters Nat. Rev. Cancer 2 2002 48 58 (Pubitemid 37328807)
2. C.A. Hrycyna Molecular genetic analysis and biochemical characterization of mammalian P-glycoproteins involved in multidrug resistance Semin. Cell Dev. Biol. 2001 247 256
3. T.W. Loo, and D.M. Clarke Molecular dissection of the human multidrug resistance P-glycoprotein Biochem. Cell Biol. 77 1999 11 23 (Pubitemid 29342829)
4. C.G. Lee, M.M. Gottesman, C.O. Cardarelli, M. Ramachandra, K.T. Jeang, S.V. Ambudkar, I. Pastan, and S. Dey HIV-1 protease inhibitors are substrates for the mdr1 multidrug transporter Biochemistry 37 1998 3594 3601 (Pubitemid 28162914)
5. H. Thomas, and H.M. Coley Overcoming multidrug resistance in cancer: an update on the strategy of inhibiting P-glycoprotein Cancer Control 10 2003 159 165 (Pubitemid 36437822)
6. K. Paterson, J.A. Ludwig, C. Booth-Genthe, and M.M. Gottesman Targeting multidrug resistance in cancer Nat. Rev. Drug Discov. 5 2006 219 234 (Pubitemid 43336035)
7. C.F. Higgins ABC transporters: from microorganisms to man Annu. Rev. Cell Biol. 8 1992 67 113 (Pubitemid 23000992)
8. M. Dean The human ATP-binding cassette (ABC) transporter superfamily Genome Res. 11 2001 1156 1166 (Pubitemid 32677289)
9. A.H. Schinkel, and J.W. Jonker Mammalian drug efflux transporters of the ATP binding cassette (ABC) family: an overview Adv. Drug Deliv. Rev. 55 2003 3 29 (Pubitemid 36078452)
10. K.J. Linton Structure and function of ABC transporters Physiology 22 2007 122 130
11. J. Lubelski, W.N. Konings, and A.J.M. Driessen Distribution and physiology of ABC-type transporters contributing to multidrug resistance in bacteria Microbiol. Mol. Biol. Rev. 71 2007 463 476 (Pubitemid 47429281)
12. F.J. Sharom ABC multidrug transporters: structure, function and role in chemoresistance Pharmacogenomics 9 2008 105 127 (Pubitemid 351560534)
13. C.J. Chen, J.E. Chin, K. Ueda, D.P. Clark, I. Pastan, M.M. Gottesman, and I.B. Roninson Internal duplication and homology with bacterial transport proteins in the mdr1 (P-glycoprotein) gene from multidrug-resistant human cells Cell 47 1986 381 389 (Pubitemid 17210152)
14. 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
15. C. Kast, V. Canfield, V. Levenson, and P. Gross Transmembrane organization of mouse P-glycoprotein determined by epitope insertion and immunofluorescence J. Biol. Chem. 271 1996 9240 9248 (Pubitemid 26137325)
16. T.W. Loo, and D.M. Clarke The minimum functional unit of human P-glycoprotein appears to be a monomer J. Biol. Chem. 271 1996 27488 27492 (Pubitemid 26367310)
17. T.W. Loo, and D.M. Clarke Reconstitution of drug-stimulated ATPase activity following co-expression of each half of human P-glycoprotein as separate polypeptides J. Biol. Chem. 269 1994 7750 7755 (Pubitemid 24217990)
18. T.W. Loo, and D.M. Clarke The transmembrane domains of the human multidrug resistance P-glycoprotein are sufficient to mediate drug binding and trafficking to the cell surface J. Biol. Chem. 274 1999 24759 24765
19. N. Dodic, B. Dumaitre, M. Daugan, and P. Pianetti Synthesis and activity against multidrug resistance in Chinese hamster ovary cells of new acridone-4-carboxamides J. Med. Chem. 38 1995 2418 2426
20. A. Dhainaut, G. Regnier, A. Tizot, S. Leonce, N. Guilbaud, N. Kraus-Berthier, and G. Atassi New purines and purine analogs as modulators of multidrug resistance J. Med. Chem. 29 1996 4099 4108 (Pubitemid 26327446)
21. G. Ecker, P. Chiba, M. Hitzler, D. Schmid, K. Visser, and H.P. Cordes Structure-activity relationship studies on benzofuran analogs of propafenone-type modulators of tumor cell multidrug resistance J. Med. Chem. 39 1996 4767 4774
22. I. Pajeva, and M. Wiese Molecular modeling of phenothiazines and related drugs as multidrug resistance modifiers: a comparative molecular field analysis study J. Med. Chem. 41 1998 1815 1826 (Pubitemid 28248657)
23. D.J. Gruol, M.N. King, and M.E. Kuehne Evidence for the locations of distinct steroid and Vinca alkaloid interaction domains within the murine mdr1b P-glycoprotein Mol. Pharm. 62 2002 1238 1248 (Pubitemid 35222516)
24. T.W. Loo, M.C. Bartlett, and D.M. Clarke Methanethiosulfonate derivatives of rhodamine and verapamil activate human P-glycoprotein at different sites J. Biol. Chem. 278 2003 50136 50141 (Pubitemid 37548851)
25. C. Martin, G. Berridge, C.F. Higgins, P. Mistry, P. Charlton, and R. Callaghan Communication between multiple drug binding sites on P-glycoprotein Mol. Pharmacol. 58 2000 624 632
26. A. Garrigues, N. Loiseau, M. Delaforge, J. Ferté, M. Garrigos, F.O. André, and S. Orlowski Characterization of two pharmacophores on the multidrug transporter P-glycoprotein Mol. Pharm. 62 2002 1288 1299
27. F.J. Sharom Shedding light on drug transport: structure and function of the P-glycoprotein multidrug transporter (ABCB1) Chem. Cell Biol. 84 2006 979 992 (Pubitemid 46450697)
28. See for example: D.R. Stenham, J.D. Campbell, M.S.P. Sansom, C.F. Higgins, I.D. Kerr, and K.J. Linton An atomic detail model for the human ATP binding cassette transporter P-glycoprotein derived from disulfide cross-linking and homology modeling FASEB J 17 2003 2287 2289 (Pubitemid 39561468)
29. 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 (Pubitemid 47301854)
30. R.J.P. Dawson, and K.P. Locher Structure of a bacterial multidrug ABC transporter Nature 443 2006 180 185 (Pubitemid 44387602)
31. Despite its natural substrate profile, it has been proved that Sav1866 is capable of translocate typical human P-gp substrate, as well as being inhibited by verapamil, also a known P-gp modulator. See: S. Velamakanni, Y. Yao, and D. Gutmann Multidrug transport by the ABC transporter Sav1866 from Staphylococcus aureus Biochemistry 47 2008 9300 9308
32. G.F. Ecker, M. Huber, D. Schmid, and P. Chiba The importance of a nitrogen atom in modulators of multidrug resistance Mol. Pharmacol. 56 1999 791 796 (Pubitemid 29491182)
33. S.G. Aller, J. Yu, A. Ward, Y. Weng, S. Chittaboina, and R. Zhuo Structure of P-glycoprotein reveals a molecular basis for poly-specific drug binding Science 323 2009 1718 1722
34. D.A.P. Gutmann, A. Ward, I.L. Urbatsch, G. Chang, and H.W. van Veen Understanding polyspecificity of multidrug ABC transporters: closing in on the gaps in ABCB1 Trends Biochem. Sci. 35 2010 36 42
35. M.S. Jin, M.L. Oldham, and Q. Zhang J. Chen Crystal structure of the multidrug transporter P-glycoprotein from Caenorhabditis elegans Nature 490 2012 566 569
36. A.D. Becke Density-functional exchange-energy approximation with correct asymptotic behavior Phys. Rev. A 38 1988 3098 3100
37. C. Lee, W. Yang, and R.G. Parr Development of the Colle-Salvetti correlation-energy formula into a functional of the electron density Phys. Rev. B 37 1988 785 789
38. W. Kohn, and I. Sham Self-consistent equations including exchange and correlation effects J. Phys. Rev. 140 1965 A1133 A1138
39. Gaussian 03, Revision B.04 2003 Gaussian, Inc. Pittsburgh, PA http://www.gaussian.com
40. G.S. Retzingerl, L. Cohen, S.H. Lau, and F.J. Kézdy Ionization and surface properties of Verapamil and several Verapamil analogues J. Pharm. Sci. 75 1986 976 982 (Pubitemid 17182374)
41. D.A. Pearlman, D.A. Case, J.W. Caldwell, W.S. Ross, T.E. Cheatham, S. Debolt, D. Ferguson, G. Seibel, and P. Kollman Amber, a package of computer programs for applying molecular mechanics, normal mode analysis, molecular dynamics and free energy calculations to simulate the structural and energetic properties of molecules Comput. Phys. Commun. 91 1995 1 41
42. J. Wang, M. Romain, J.W. Caldwell, P.A. Kollman, and D.A. Case Development and testing of a general Amber force field J. Comput. Chem. 25 2004 1157 1174
43. C.I. Bayly, P. Cieplak, W.D. Cornell, and P.A. Kollman The procedure of the determination of RESP charges J. Phys. Chem. 97 1993 10269 10275
44. D. Suarez, and K.M. Merz Jr. Molecular dynamics simulations of the mononuclear zinc-β-lactamase from Bacillus cereus J. Am. Chem. Soc. 123 2001 3759 3770 (Pubitemid 32879538)
45. AMBER 9 2009 University of California San Francisco, CA
46. D.M. Moreno, M.A. Martí, P.M. De Biase, D.A. Estrín, V. Demicheli, R. Redi, and L. Boechi Exploring the molecular basis of human manganese superoxide dismutase inactivation mediated by tyrosine 34 nitration Arch. Biochem. Biophys. 507 2011 304 309
47. T.C. Ramalho, T.C.C. França, W.A. Cortopassi, A.S. Gonçalves, A.W.S. Da Silva, and E.F.F. Da Cunha Topology and dynamics of the interaction between 5-nitroimidazole radiosensitizers and duplex DNA studied by a combination of docking, molecular dynamic simulations and NMR spectroscopy J. Mol. Struct. 992 2011 65 71
48. R.A. Laskowski, M.W. MacArthur, D.S. Moss, and J.M. Thornton PROCHECK: a program to check the stereochemical quality of protein structures J. Appl. Cryst. 26 1993 283 291
49. J.D. Thompson, D.G. Higgins, and T.J. Gibson CLUSTALW. Improving the sensivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice Nucleic Acids Res. 22 1994 4673 4680 (Pubitemid 24354800)
50. N. Eswar, M.A. Marti-Renom, B. Webb, M.S. Madhusudhan, D. Eramian, M. Shen, U. Pieper, and A. Sali Comparative protein structure modeling with MODELLER Curr. Prot. Bioinfor. 15 Suppl. 2006 5.6.1-5.6.30
51. A. Clementi, H. Nymeyer, and J.N. Onuchic Topological and energetic factors: what determines the structural details of the transition state ensemble and "en-route" intermediates for protein folding? An investigation for small globular proteins J. Mol. Biol. 298 2000 937 953
52. B. Hess, C. Kutzner, D. van der Spoel, and E. Lindahl GROMACS 4: Algorithms for highly efficient, load-balanced, and scalable molecular simulation J. Chem. Theory Comput. 4 2008 435 447
53. J.K. Noel, P.C. Whitford, K.Y. Sanbonmatsu, and J.N. Onuchic SMOG@ctbp: simplified deployment of structure-based models in GROMACS Nucleic Acids Res. 38 2010 W657 W661
54. F.K. von Gottberg, K.A. Smith, and T.A. Hatton Stochastic dynamics simulation of surfactant self-assembly J. Chem. Phys. 106 1997 9850
55. H.J.C. Berendsen, J.P.M. Postman, W.F. Gunsteren, A. Di Nola, and J.R. Haak Molecular dynamics with coupling to an external bath J. Chem. Phys. 81 1984 3684 3690
56. T. Darden, D. York, and L.G. Pedersen Particle mesh Ewald: an N log(N) method for Ewald sums in large systems J. Chem. Phys. 98 1983 10089 10094
57. U. Essman, L. Perera, M.L. Berkowitz, T. Darden, H. Lee, and L. Pedersen A smooth particle mesh Ewald method J. Chem. Phys. 103 1995 8577 8593
58. J.P. Ryckaert, G. Ciccotti, and H.J.D.C. Berendsen Numerical integration of the cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes J. Comput. Phys. 23 1997 327 341
59. M. Naïm, S. Bhat, K.N. Rankin, S. Dennis, S.F. Chowdhury, and I. Siddiqi Solvated interaction energy (SIE) for scoring protein-ligand binding affinities. 1. Exploring the parameter space J. Chem. Inf. Model. 47 2007 122 133 (Pubitemid 46225568)
60. H. Humphrey, A. Dalke, and K. Schulten VMD - visual molecular dynamics J. Mol. Graph. 14 1996 33 38
61. G.M. Morris, D.S. Goodsell, R.S. Halliday, R. Huey, W.E. Hart, R.K. Belew, and A.J. Olson Automated docking using a Lamarckian genetic algorithm and an empirical binding free energy function J. Comp. Chem. 19 1998 1639 1662 (Pubitemid 128590223)
62. C. Globisch, I.K. Pajeva, and M. Wiese Identification of putative binding sites of P-glycoprotein based on its homology model ChemMedChem 3 2008 280 295
63. T.W. Loo, and D.M. Clarke Determining the dimensions of the drug-binding domain of human P-glycoprotein using thiol cross-linking compounds as molecular rulers J. Biol. Chem. 276 2001 36877 36880
64. T.W. Loo, and D.M. Clarke Vanadate trapping of nucleotide at the ATP-binding sites of human multidrug resistance P-glycoprotein exposes different residues to the drug-binding site Proc. Nat. Acad. Sci. U.S.A. 99 2002 3511 3516 (Pubitemid 34252139)
65. À. Tarcsay, and G. Keserü Homology modeling and binding site assessment of human P-glycoprotein Fut. Med. Chem. 3 2011 297 307
66. F. Klepsch, P. Chiba, and G.F. Ecker Exhaustive sampling of docking poses reveals binding hypotheses for propafenone type inhibitors of p-glycoprotein PLoS Comput. Biol. 7 2011 e1002036
67. C. Globisch, I.K. Pajeva, and M. Wiese Structure-activity relationships of a series of tariquidar analogs as multidrug resistance modulators Bioorg. Med. Chem. 14 2006 1588 1598 (Pubitemid 43120295)
68. Y. Taguchi, M. Morishima, T. Komano, and K. Ueda Amino acid substitutions in the first transmembrane domain (TM1) of P-glycoprotein that alter substrate specificity FEBS Lett. 413 1997 142
69. T.W. Loo, and D.M. Clarke Mutations to amino acids located in predicted transmembrane segment 6 (TM6) modulate the activity and substrate specificity of human P-glycoprotein Biochemistry 33 1994 14049 14057 (Pubitemid 24382347)
70. T.W. Loo, and D.M. Clarke Identification of residues in the drug-binding site of human P-glycoprotein using a thiol-reactive substrate J. Biol. Chem. 272 1997 31945 31948 (Pubitemid 28011858)
71. A. Rothnie, J. Storm, R. McMahon, A. Taylor, I.D. Kerr, and R. Callaghan The coupling mechanism of P-glycoprotein involves residue L339 in the sixth membrane spanning segment FEBS Lett. 579 2005 3984 3990 (Pubitemid 40961900)
72. T.W. Loo, and D.M. Clarke Drug-stimulated ATPase activity of human P-glycoprotein requires movement between transmembrane segments 6 and 12 J. Biol. Chem. 272 1997 20986 20989 (Pubitemid 27373952)
73. T.W. Loo, M.C. Bartlett, and D.M. Clarke Val133 and Cys137 in transmembrane segment 2 are close to Arg935 and Gly939 in transmembrane segment 11 of human P-glycoprotein J. Biol. Chem. 279 2004 18232 18238 (Pubitemid 38623236)
74. E. Lanzarotti, R.R. Biekofsky, D.A. Estrín, M.A. Martí, and A.G. Turjanski Aromatic-aromatic interactions in proteins: beyond the dimmer J. Chem. Inf. Model. 51 2011 1623 1633
75. T.W. Loo, M.C. Bartlett, and D.M. Clarke Suppressor mutations in the transmembrane segments of P-glycoprotein promote maturation of processing mutants and disrupt a subset of drug-binding sites J. Biol. Chem. 282 2007 32043 32052 (Pubitemid 350106425)
76. T.W. Loo, and D.M. Clarke Defining the drug-binding site in the human multidrug resistance P-glycoprotein using a methanethiosulfonate analog of verapamil, MTS-verapamil J. Biol. Chem. 276 2001 14972 14979
77. T.W. Loo, and D.M. Clarke Identification of residues within the drug-binding domain of the human multidrug resistance P-glycoprotein by cysteine-scanning mutagenesis and reaction with dibromobimane J. Biol. Chem. 275 2000 39272 39278 (Pubitemid 32058947)
78. G.F. Ecker, E. Csaszar, S. Kopp, B. Plagens, W. Holzer, W. Ernst, and P. Chiba Identification of ligand-binding regions of P-glycoprotein by activated-pharmacophore photoaffinity labeling and matrix-assisted laser desorption/ionization-time-of-flight mass spectrometry Mol. Pharmacol. 61 2002 637 648 (Pubitemid 34171930)
79. J. Storm, M.L. O'Mara, E.H. Crowley, J. Peall, D.P. Tieleman, I.D. Kerr, and R. Callaghan Residue G346 in transmembrane segment six is involved in inter-domain communication in P-glycoprotein Biochemistry 46 2007 9899 9910 (Pubitemid 47378580)
80. T.W. Loo, M.C. Bartlett, and D.M. Clarke Transmembrane segment 7 of human P-glycoprotein forms part of the drug-binding pocket Biochem. J. 399 2006 351 359 (Pubitemid 44570297)
81. T.W. Loo, and D.M. Clarke Mutational analysis of ABC proteins Arch. Biochem. Biophys. 476 2008 51 64
82. A. Sakurai, Y. Onishi, H. Hirano, M. Seigneuret, K. Obanayama, G. Kim, E.L. Liew, T. Sakaeda, K. Yoshiura, K. Niikawa, M. Sakurai, and T. Ishikawa Quantitative structure-activity relationship analysis and molecular dynamics simulation to functionally validate nonsynonymous polymorphisms of human ABC transporter ABCB1 (P-glycoprotein/MDR1) Biochemistry 46 2007 7678 7693 (Pubitemid 47016053)
83. M. Roe, A. Folkes, P. Ashworth, J. Brumwell, L. Chima, S. Hunjan, I. Pretswell, W. Dangerfield, H. Ryder, and P. Charlton Reversal of P-glycoprotein mediated multidrug resistance by novel anthranilamide derivatives Bioorg. Med. Chem. Lett. 9 1999 595 600 (Pubitemid 29090660)