Interaction of transported drugs with the lipid bilayer and P-glycoprotein through a solvation exchange mechanism

Biophysical Journal

Volumn 90, Issue 11, 2006, Pages 4046-4059

  Omote, Hiroshi ^a,b   Al Shawi, Marwan K ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

^b OKAYAMA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

COLCHICINE; DAUNORUBICIN; GLYCOPROTEIN P; HOE 33342; RHODAMINE 123; VERAPAMIL;

ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; DRUG BINDING SITE; DRUG DIFFUSION; DRUG PROTEIN BINDING; DRUG SPECIFICITY; DRUG TRANSPORT; ELECTRON SPIN RESONANCE; HUMAN; HYDROGEN BOND; LIPID BILAYER; MEMBRANE TRANSPORT; MOLECULAR DYNAMICS; PROTEIN STRUCTURE; PROTEIN TRANSPORT; SOLVATION;

EID: 33744902318     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.105.077743     Document Type: Article

References (89)

1. Gottesman, M. M., and I. Pastan. 1993. Biochemistry of multidrug resistance mediated by the multidrug transporter. Annu. Rev. Biochem. 62:385-427.
2. Borst, P., and R. O. Elferink. 2002. Mammalian ABC transporters in health and disease. Annu. Rev. Biochem. 71:537-592.
3. Ambudkar, S. V., C. Kimchi-Sarfaty, Z. E. Sauna, and M. M. Gottesman. 2003. P-glycoprotein: from genomics to mechanism. Oncogene. 22:7468-7485.
4. Leslie, E. M., R. G. Deeley, and S. P. Cole. 2005. Multidrug resistance proteins: role of P-glycoprotein, MRP1, MRP2, and BCRP (ABCG2) in tissue defense. Toxicol. Appl. Pharmacol. 204:216-237.
5. Senior, A. E., M. K. Al-Shawi, and I. L. Urbatsch. 1995. ATP hydrolysis by multidrug-resistance protein from Chinese hamster ovary cells. J. Bioenerg. Biomembr. 27:31-36.
6. Dean, M., and R. Allikmets. 2001. Complete characterization of the human ABC gene family. J. Bioenerg. Biomembr. 33:475-479.
7. Holland, I. B., and M. A. Blight. 1999. ABC-ATPases, adaptable energy generators fuelling transmembrane movement of a variety of molecules in organisms from bacteria to humans. J. Mol. Biol. 293:381-399.
8. Sharom, F. J. 1997. The P-glycoprotein efflux pump: how does it transport drugs. J. Membr. Biol. 160:161-175.
9. Seelig, A. 1998. A general pattern for substrate recognition by P-glycoprotein. Eur. J. Biochem. 251:252-261.
10. Ecker, G., M. Huber, D. Schmid, and P. Chiba. 1999. The importance of a nitrogen atom in modulators of multidrug resistance. Mol. Pharmacol. 56:791-796.
11. Pleban, K., A. Macchiarulo, G. Costantino, R. Pellicciari, P. Chiba, and G. F. Ecker. 2004. Homology model of the multidrug transporter LmrA from Lactococcus lactis. Bioorg. Med. Chem. Lett. 14:5823-5826.
12. Seelig, A., and E. Landwojtowicz. 2000. Structure-activity relationship of P-glycoprotein substrates and modifiers. Eur. J. Pharm. Sci. 12:31-40.
13. Greenberger, L. M., C. J. Lisanti, J. T. Silva, and S. B. Horwitz. 1991. Domain mapping of the photoaffinity drug-binding sites in P-glycoprotein encoded by mouse mdr1b. J. Biol. Chem. 266:20744-20751.
14. Pleban, K., S. Kopp, E. Csaszar, M. Peer, T. Hrebicek, A. Rizzi, G. F. Ecker, and P. Chiba. 2005. P-glycoprotein substrate binding domains are located at the transmembrane domain/transmembrane domain interfaces: a combined photoaffinity labeling-protein homology modeling approach. Mol. Pharmacol. 67:365-374.
15. Loo, T. W., and D. M. Clarke. 1993. Functional consequences of phenylalanine mutations in the predicted transmembrane domain of P-glycoprotein. J. Biol. Chem. 268:19965-19972.
16. Ambudkar, S. V., S. Dey, C. A. Hrycyna, M. Ramachandra, I. Pastan, and M. M. Gottesman. 1999. Biochemical, cellular, and pharmacological aspects of the multidrug transporter. Annu. Rev. Pharmacol. Toxicol. 39:361-398.
17. Shapiro, A. B., A. B. Corder, and V. Ling. 1997. P-glycoprotein-mediated Hoechst 33342 transport out of the lipid bilayer. Eur. J. Biochem. 250:115-121.
18. Shapiro, A. B., and V. Ling. 1997. Extraction of Hoechst 33342 from the cytoplasmic leaflet of the plasma membrane by P-glycoprotein. Eur. J. Biochem. 250:122-129.
19. Shapiro, A. B., and V. Ling. 1998. Transport of LDS-751 from the cytoplasmic leaflet of the plasma membrane by the rhodamine-123-selective site of P-glycoprotein. Eur. J. Biochem. 254:181-188.
20. Bolhuis, H., H. W. van Veen, D. Molenaar, B. Poolman, A. J. Driessen, and W. N. Konings. 1996. Multidrug resistance in Lactococcus lactis: evidence for ATP-dependent drug extrusion from the inner leaflet of the cytoplasmic membrane. EMBO J. 15:4239-4245.
21. Omote, H., and M. K. Al-Shawi. 2002. A novel electron paramagnetic resonance approach to determine the mechanism of drug transport by P-glycoprotein. J. Biol. Chem. 277:45688-45694.
22. Bassolino-Klimas, D., H. E. Alper, and T. R. Stouch. 1993. Solute diffusion in lipid bilayer membranes: an atomic level study by molecular dynamics simulation. Biochemistry. 32:12624-12637.
23. Marrink, S. J., and H. J. C. Berendsen. 1996. Permeation process of small molecules across lipid membranes studied by molecular dynamics simulations. J. Phys. Chem. 100:16729-16738.
24. Shepherd, C. M., H. J. Vogel, and D. P. Tieleman. 2003. Interactions of the designed antimicrobial peptide MB21 and truncated dermaseptin S3 with lipid bilayers: molecular-dynamics simulations. Biochem. J. 370:233-243.
25. van Aalten, D. M., R. Bywater, J. B. Findlay, M. Hendlich, R. W. Hooft, and G. Vriend. 1996. PRODRG, a program for generating molecular topologies and unique molecular descriptors from coordinates of small molecules. J. Comput. Aided Mol. Des. 10:255-262.
26. Stewart, J. J. 1990. MOPAC: a semiempirical molecular orbital program. J. Comput. Aided Mol. Des. 4:1-105.
27. Tieleman, D. P., and H. J. C. Berendsen. 1996. Molecular dynamics simulations of a hydrated dipalmitoylphosphatidylcholine bilayer with different macroscopic boundary conditions and parameters. J. Chem. Phys. 105:4871-4880.
28. Berger, O., O. Edholm, and F. Jahnig. 1997. Molecular dynamics simulations of a fluid bilayer of dipalmitoylphosphatidylcholine at full hydration, constant pressure, and constant temperature. Biophys. J. 72:2002-2013.
29. Berendsen, H. J. C., D. van der Spoel, and R. van Drunen. 1995. GROMACS: a message-passing parallel molecular dynamics implementation. Comput. Phys. Commun. 91:43-56.
30. Lindahl, E., B. Hess, and D. van der Spoel. 2001. GROMACS 3.0: a package for molecular simulation and trajectory analysis. J. Mol. Model. [Online]. 7:306-317.
31. Hess, B., H. Bekker, H. J. C. Berendsen, and J. G. E. M. Fraaije. 1997. LINCS: a linear constraint solver for molecular simulations. J. Comput. Chem. 18:1463-1472.
32. Sali, A., and T. L. Blundell. 1993. Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol. 234:779-815.
33. Omote, H., R. A. Figler, M. K. Polar, and M. K. Al-Shawi. 2004. Improved energy coupling of human P-glycoprotein by the glycine 185 to valine mutation. Biochemistry. 43:3917-3928.
34. Campbell, J. D., P. C. Biggin, M. Baaden, and M. S. Sansom. 2003. Extending the structure of an ABC transporter to atomic resolution: modeling and simulation studies of MsbA. Biochemistry. 42:3666-3673.
35. Thompson, J. D., D. G. Higgins, and T. J. Gibson. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680.
36. Rost, B., and C. Sander. 1993. Prediction of protein secondary structure at better than 70% accuracy. J. Mol. Biol. 232:584-599.
37. Rost, B. 1996. PHD: predicting one-dimensional protein structure by profile-based neural networks. Methods Enzymol. 266:525-539.
38. Chang, G. 2003. Structure of MsbA from Vibrio cholera: a multidrug resistance ABC transporter homolog in a closed conformation. J. Mol. Biol. 330:419-430.
39. Hung, L. W., I. X. Wang, K. Nikaido, P. Q. Liu, G. F. Ames, and S. H. Kim. 1998. Crystal structure of the ATP-binding subunit of an ABC transporter. Nature. 396:703-707.
40. Laskowski, R. A., M. W. Macarthur, D. S. Moss, and J. M. Thornton. 1993. PROCHECK: a program to check the stereochemical quality of protein structures. J. App. Crystallogr. 26:283-291.
41. Gaudet, R., and D. C. Wiley. 2001. Structure of the ABC ATPase domain of human TAP1, the transporter associated with antigen processing. EMBO J. 20:4964-4972.
42. Ramachandran, G. N., and V. Sasisekharan. 1968. Conformation of polypeptides and proteins. Adv. Protein Chem. 23:283-438.
43. Locher, K. P., A. T. Lee, and D. C. Rees. 2002. The E. coli BtuCD structure: a framework for ABC transporter architecture and mechanism. Science. 296:1091-1098.
44. Davidson, A. L., and J. Chen. 2004. ATP-binding cassette transporters in bacteria. Annu. Rev. Biochem. 73:241-268.
45. Seigneuret, M., and A. Garnier-Suillerot. 2003. A structural model for the open conformation of the mdr1 P-glycoprotein based on the MsbA crystal structure. J. Biol. Chem. 278:30115-30124.
46. Stenham, D. R., J. D. Campbell, M. S. Sansom, C. F. Higgins, I. D. Kerr, and K. J. Linton. 2003. An atomic detail model for the human ATP binding cassette transporter P-glycoprotein derived from disulfide cross-linking and homology modeling. FASEB J. 17:2287-2289.
47. Shilling, R. A., L. Balakrishnan, S. Shahi, H. Venter, and H. W. van Veen. 2003. A new dimer interface for an ABC transporter. Int. J. Antimicrob. Agents. 22:200-204.
48. Higgins, C. F., and K. J. Linton. 2004. The ATP switch model for ABC transporters. Nat. Struct. Mol. Biol. 11:918-926.
49. Loo, T. W., M. C. Bartlett, and D. M. Clarke. 2004. Val133 and Cys137 in transmembrane segment 2 are close to residues Arg935 and Gly939 in transmembrane segment 11 of human P-glycoprotein. J. Biol. Chem. 279:18232-18238.
50. Loo, T. W., M. C. Bartlett, and D. M. Clarke. 2004. Disulfide crosslinking 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.
51. Reyes, C. L., and G. Chang. 2005. Structure of the ABC transporter MsbA in complex with ADP.vanadate and lipopolysaccharide. Science. 308:1028-1031.
52. Al-Shawi, M. K., M. K. Polar, H. Omote, and R. A. Figler. 2003. Transition state analysis of the coupling of drug transport to ATP hydrolysis by P-glycoprotein. J. Biol. Chem. 278:52629-52640.
53. Demeule, M., J. Jodoin, D. Gingras, and R. Beliveau. 2000. P-glycoprotein is localized in caveolae in resistant cells and in brain capillaries. FEBS Lett. 466:219-224.
54. Eytan, G. D., and P. W. Kuchel. 1999. Mechanism of action of P-glycoprotein in relation to passive membrane permeation. Int. Rev. Cytol. 190:175-250.
55. Reuter, G., T. Janvilisri, H. Venter, S. Shahi, L. Balakrishnan, and H. W. Van Veen. 2003. The ATP-binding cassette multidrug transporter LmrA and lipid transporter MsbA have overlapping substrate specificities. J. Biol. Chem. 278:35193-35198.
56. Ruetz, S., and P. Gros. 1994. Phosphatidylcholine translocase: a physiological role for the mdr2 gene. Cell. 77:1071-1081.
57. Yang, A. S., and B. Honig. 2000. An integrated approach to the analysis and modeling of protein sequences and structures. II. On the relationship between sequence and structural similarity for proteins that are not obviously related in sequence. J. Mol. Biol. 301:679-689.
58. Chang, G., and C. B. Roth. 2001. Structure of MsbA from E. coli: a homolog of the multidrug resistance ATP binding cassette (ABC) transporters. Science. 293:1793-1800.
59. Shilling, R., L. Federici, F. Walas, H. Venter, S. Velamakanni, B. Woebking, L. Balakrishnan, B. Luisi, and H. W. van Veen. 2005. A critical role of a carboxylate in proton conduction by the ATP-binding cassette multidrug transporter LmrA. FASEB J. 19:1698-1700.
60. Pajeva, I. K., and M. Wiese. 2002. Pharmacophore model of drugs involved in P-glycoprotein multidrug resistance: explanation of structural variety (hypothesis). J. Med. Chem. 45:5671-5686.
61. Yu, E. W., G. McDermott, H. I. Zgurskaya, H. Nikaido, and D. E. Koshland. 2003. Structural basis of multiple drug-binding capacity of the AcrB multidrug efflux pump. Science. 300:976-980.
62. Seelig, A., X. Li Blatter, and F. Wohnsland. 2000. Substrate recognition by P-glycoprotein and by the multidrug resistance-associated protein MRP1: a comparison. Eur. J. Pharm. Sci. 12:31-40.
63. Qu, Q., and F. J. Sharom. 2002. Proximity of bound Hoechst 33342 to the ATPase catalytic sites places the drug binding site of P-glycoprotein within the cytoplasmic membrane leaflet. Biochemistry. 41:4744-4752.
64. Lugo, M. R., and F. J. Sharom. 2005. Interaction of LDS-751 with P-glycoprotein and mapping of the location of the R drug binding site. Biochemistry. 44:643-655.
65. Seelig, A., and E. Gatlik-Landwojtoxicz. 2005. Biophysical characterization of inhibitors of multidrug efflux transporters: their membrane and protein interactions. Mini Rev. Med. Chem. 5:135-151.
66. Romsicki, Y., and F. J. Sharom. 1999. The membrane lipid environment modulates drug interactions with the P-glycoprotein multidrug transporter. Biochemistry. 38:6887-6896.
67. de Wolf, F. A., M. Maliepaard, F. van Dorsten, I. Berghuis, K. Nicolay, and B. de Kruijff. 1990. Comparable interaction of doxorubicin with various acidic phospholipids results in changes of lipid order and dynamics. Biochim. Biophys. Acta. 1096:67-80.
68. Chow, A., J. Kennedy, R. Pottier, and T. Truscott. 1986. Rhodamine 123: photophysical and photochemical properties. Photobiochem. Photobiophys. 11:139-148.
69. Ferguson, M. W., P. C. Beaumont, S. E. Jones, S. Navaratnam, and B. J. Parsons. 1999. Excited state and free radical properties of Rhodamine 123: a laser flash photolysis and radiolysis study. Phys. Chem. Chem. Phys. 1:261-268.
70. Loo, T. W., and D. M. Clarke. 2005. Do drug substrates enter the common drug-binding pocket of P-glycoprotein through "gates"? Biochem. Biophys. Res. Commun. 329:419-422.
71. Rosenberg, M. F., A. B. Kamis, R. Callaghan, C. F. Higgins, and R. C. Ford. 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.
72. Pepe, G., G. Guiliani, S. Loustalet, and P. Halfon. 2002. Hydration free energy a fragmental model and drug design. Eur. J. Med. Chem. 37:865-872.
73. Marrink, S. J., and H. J. C. Berendsen. 1994. Simulation of water transport through a lipid membrane. J. Phys. Chem. 98:4155-4168.
74. Zhang, D. W., H. M. Gu, D. Situ, A. Haimeur, S. P. Cole, and R. G. Deeley. 2003. Functional importance of polar and charged amino acid residues in transmembrane helix 14 of multidrug resistance protein 1 (MRP1/ABCC1): identification of an aspartate residue critical for conversion from a high to low affinity substrate binding state. J. Biol. Chem. 278:46052-46063.
75. Yerushalmi, H., and S. Schuldiner. 2000. An essential glutamyl residue in EmrE, a multidrug antiporter from Escherichia coli. J. Biol. Chem. 275:5264-5269.
76. Edgar, R., and E. Bibi. 1999. A single membrane-embedded negative charge is critical for recognizing positively charged drugs by the Escherichia coli multidrug resistance protein MdfA. EMBO J. 18:822-832.
77. Brown, M. H., and R. A. Skurray. 2001. Staphylococcal multidrug efflux protein QacA. J. Mol. Microbiol. Biotechnol. 3:163-170.
78. Tamura, N., S. Konishi, and A. Yamaguchi. 2003. Mechanisms of drug/H+ antiport: complete cysteine-scanning mutagenesis and the protein engineering approach. Curr. Opin. Chem. Biol. 7:570-579.
79. Otsuka, M., M. Yasuda, Y. Morita, C. Otsuka, T. Tsuchiya, H. Omote, and Y. Moriyama. 2005. Identification of essential amino acid residues of the NorM Na+/multidrug antiporter in Vibrio parahaemolyticus. J. Bacteriol. 187:1552-1558.
80. Hopfner, K. P., A. Karcher, D. S. Shin, L. Craig, L. M. Arthur, J. P. Carney, and J. A. Tainer. 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.
81. Urbatsch, I. L., K. Gimi, S. Wilke-Mounts, and A. E. Senior. 2000. Investigation of the role of glutamine-471 and glutamine-1114 in the two catalytic sites of P-glycoprotein. Biochemistry. 39:11921-11927.
82. Loo, T. W., and D. M. Clarke. 2001. Cross-linking of human multidrug resistance P-glycoprotein by the substrate, Tris-(2-maleimidoethyl)-amine, is altered by ATP hydrolysis. J. Biol. Chem. 276:31800-31805.
83. Rothnie, A., J. Storm, J. Campbell, K. J. Linton, I. D. Kerr, and R. Callaghan. 2004. The topography of transmembrane segment six is altered during the catalytic cycle of P-glycoprotein. J. Biol. Chem. 279:34913-34921.
84. Morais-Cabral, J. H., Y. Zhou, and R. MacKinnon. 2001. Energetic optimization of ion conduction rate by the K+ selectivity filter. Nature. 414:37-42.
85. Poelarends, G. J., and W. N. Konings. 2002. The transmembrane domains of the ABC multidrug transporter LmrA form a cytoplasmic exposed, aqueous chamber within the membrane. J. Biol. Chem. 277:42891-42898.
86. Loo, T. W., M. C. Bartlett, and D. M. Clarke. 2004. The drug-binding pocket of the human multidrug resistance P-glycoprotein is accessible to the aqueous medium. Biochemistry. 43:12081-12089.
87. Senior, A. E., M. K. Al-Shawi, and I. L. Urbatsch. 1995. The catalytic cycle of P-glycoprotein. FEBS Lett. 377:285-289.
88. Zeuthen, T., and W. D. Stein. 1994. Cotransport of salt and water in membrane proteins: membrane proteins as osmotic engines. J. Membr. Biol. 137:179-195.
89. Kraulis, P. J. 1991. MOLSCRIPT:A program to produce both detailed and schematic plots of protein structures. J. App. Crystallogr. 24: 946-950.