Molecular-dynamics simulations of the ATP/apo state of a multidrug ATP-binding cassette transporter provide a structural and mechanistic basis for the asymmetric occluded state

Biophysical Journal

Volumn 100, Issue 12, 2011, Pages 3025-3034

  Jones, Peter M ^a   George, Anthony M ^a  

^a UNIVERSITY OF TECHNOLOGY SYDNEY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA (MICROORGANISMS);

EID: 79960308124     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2011.05.028     Document Type: Article

References (67)

1. Higgins, C. F. 1992. ABC transporters: from microorganisms to man. Annu. Rev. Cell Biol. 8:67-113. (Pubitemid 23000992)
2. 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. (Pubitemid 29516178)
3. Aravind, L., D. R.Walker, and E. V. Koonin. 1999. Conserved domains in DNA repair proteins and evolution of repair systems. Nucleic Acids Res. 27:1223-1242. (Pubitemid 29206430)
4. Jones, P. M., M. L. O'Mara, and A. M. George. 2009. ABC transporters: a riddle wrapped in a mystery inside an enigma. Trends Biochem. Sci. 34:520-531.
5. Dean, M., A. Rzhetsky, and R. Allikmets. 2001. The humanATP-binding cassette (ABC) transporter superfamily. Genome Res. 11:1156-1166. (Pubitemid 32677289)
6. Jones, P. M., and A. M. George. 2004. The ABC transporter structure and mechanism: perspectives on recent research. Cell. Mol. Life Sci. 61:682-699. (Pubitemid 38446412)
7. Toyoda, Y., Y. Hagiya, ..., T. Ishikawa. 2008. MRP class of human ATP binding cassette (ABC) transporters: historical background and new research directions. Xenobiotica. 38:833-862.
8. Jones, P. M., and A. M. George. 1999. Subunit interactions in ABC transporters: towards a functional architecture. FEMS Microbiol. Lett. 179:187-202. (Pubitemid 29460678)
9. Smith, P. C., N. Karpowich, ..., J. F. Hunt. 2002. ATP binding to the motor domain from an ABC transporter drives formation of a nucleotide sandwich dimer. Mol. Cell. 10:139-149. (Pubitemid 34876568)
10. 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. (Pubitemid 34517120)
11. Dawson, R. J., and K. P. Locher. 2006. Structure of a bacterial multidrug ABC transporter. Nature. 443:180-185. (Pubitemid 44387602)
12. Pinkett, H. W., A. T. Lee, ..., D. C. Rees. 2007. An inward-facing conformation of a putative metal-chelate-type ABC transporter. Science. 315:373-377. (Pubitemid 46175517)
13. Hollenstein, K., D. C. Frei, and K. P. Locher. 2007. Structure of an ABC transporter in complex with its binding protein. Nature. 446:213-216. (Pubitemid 46398672)
14. Oldham, M. L., D. Khare, ..., J. Chen. 2007. Crystal structure of a catalytic intermediate of the maltose transporter. Nature. 450:515-521. (Pubitemid 350190241)
15. Gerber, S., M. Comellas-Bigler, ..., K. P. Locher. 2008. Structural basis of trans-inhibition in a molybdate/tungstate ABC transporter. Science. 321:246-250. (Pubitemid 351989095)
16. Kadaba, N. S., J. T. Kaiser, ..., D. C. Rees. 2008. The high-affinity E. coli methionine ABC transporter: structure and allosteric regulation. Science. 321:250-253. (Pubitemid 351989096)
17. Velamakanni, S., Y. Yao, ..., H.W. van Veen. 2008. Multidrug transport by the ABC transporter Sav1866 from Staphylococcus aureus. Biochemistry. 47:9300-9308.
18. Kale, L., R. Skeel, ..., K. Shulten. 1999. NMAD2: greater scalability for parallel molecular dynamics. J. Comput. Phys. 151:283-312.
19. MacKerell, A. D., D. Bashford, R. L. Bellott, ..., M. Karplus. 1998. All-atom empirical potential for molecular modeling and dynamics studies of proteins. J. Phys. Chem. B. 102:3586-3616. (Pubitemid 128576688)
20. Lindahl, E., B. Hess, and D. van der Spoel. 2001. GROMACS 3.0: a package for molecular simulation and trajectory analysis. J. Mol. Model. 7:306-317. (Pubitemid 36153547)
21. Jorgensen, W. L., J. Chandrasekhar, ..., M. L. Klein. 1983. Comparison of simple potential functions for simulating liquid water. J. Chem. Phys. 79:926-935.
22. Ryckaert, J.-P., G. Ciccotti, and H. J. C. Berendsen. 1977. Numerical integration of the Cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes. J. Comput. Phys. 23: 327-341.
23. Darden, T., D. York, and L. Pedersen. 1993. Particle mesh Ewald: an Nl·og(N) method for Ewald sums in large systems. J. Chem. Phys. 98:10089-10092.
24. Wriggers, W., and K. Schulten. 1997. Protein domain movements: detection of rigid domains and visualization of hinges in comparisons of atomic coordinates. Proteins. 29:1-14. (Pubitemid 27377415)
25. Humphrey, W., A. Dalke, and K. Schulten. 1996. VMD: visual molecular dynamics. J. Mol. Graph. 14:33-38, 27-38. (Pubitemid 26152973)
26. Schwieters, C. D., J. J. Kuszewski, ..., G. M. Clore. 2003. The Xplor- NIH NMR molecular structure determination package. J. Magn. Reson. 160:65-73.
27. Mezei, M. 2010. Simulaid: a simulation facilitator and analysis program. J. Comput. Chem. 31:2658-2668.
28. Haliloglu, T., I. Bahar, and B. Erman. 1997. Gaussian dynamics of folded proteins. Phys. Rev. Lett. 79:3090.
29. Haubertin, D. Y., H. Madaoui, ..., S. Orlowski. 2006. Molecular dynamics simulations of E. coli MsbA transmembrane domain: formation of a semipore structure. Biophys. J. 91:2517-2531. (Pubitemid 44511707)
30. Sun, T., M. Liu, ..., C. Wang. 2010. Molecular dynamics simulation of the transmembrane subunit of BtuCD in the lipid bilayer. Sci. China. Life Sci. 53:620-630.
31. Jones, P. M., and A. M. George. 2007. Nucleotide-dependent allostery within the ABC transporter ATP-binding cassette: a computational study of the MJ0796 dimer. J. Biol. Chem. 282:22793-22803. (Pubitemid 47267351)
32. Jones, P. M., and A. M. George. 2002. Mechanism of ABC transporters: a molecular dynamics simulation of a well characterized nucleotidebinding subunit. Proc. Natl. Acad. Sci. USA. 99:12639-12644.
33. Campbell, J. D., S. S. Deol, ..., M. S. Sansom. 2004. Nucleotidedependent conformational changes in HisP: molecular dynamics simulations of an ABC transporter nucleotide-binding domain. Biophys. J. 87:3703-3715. (Pubitemid 39602880)
34. Campbell, J. D., and M. S. Sansom. 2005. Nucleotide binding to the homodimeric MJ0796 protein: a computational study of a prokaryotic ABC transporter NBD dimer. FEBS Lett. 579:4193-4199. (Pubitemid 41021811)
35. Oloo, E. O., E. Y. Fung, and D. P. Tieleman. 2006. The dynamics of the MgATP-driven closure of MalK, the energy-transducing subunit of the maltose ABC transporter. J. Biol. Chem. 281:28397-28407. (Pubitemid 44414553)
36. Wen, P. C., and E. Tajkhorshid. 2008. Dimer opening of the nucleotide binding domains of ABC transporters after ATP hydrolysis. Biophys. J. 95:5100-5110.
37. Jones, P. M., and A. M. George. 2009. Opening of the ADP-bound active site in the ABC transporter ATPase dimer: evidence for a constant contact, alternating sites model for the catalytic cycle. Proteins. 75:387-396.
38. Newstead, S., P.W. Fowler, ..., S. Iwata. 2009. Insights into how nucleotide- binding domains power ABC transport. Structure. 17:1213-1222.
39. Oliveira, A. S., A. M. Baptista, and C. M. Soares. 2010. Insights into the molecular mechanism of an ABC transporter: conformational changes in the NBD dimer of MJ0796. J. Phys. Chem. B. 114:5486- 5496.
40. Aittoniemi, J., H. deWet, ..., M. S. Sansom. 2010. Asymmetric switching in a homodimeric ABC transporter: a simulation study. PLOS Comput. Biol. 6:e1000762.
41. Becker, J.-P., F. Van Bambeke, ..., M. Prévost. 2010. Dynamics and structural changes induced by ATP binding in SAV1866, a bacterial ABC exporter. J. Phys. Chem. B. 114:15948-15957.
42. Atilgan, A. R., S. R. Durell, ..., I. Bahar. 2001. Anisotropy of fluctuation dynamics of proteins with an elastic network model. Biophys. J. 80:505-515.
43. Bahar, I., A. R. Atilgan, and B. Erman. 1997. Direct evaluation of thermal fluctuations in proteins using a single-parameter harmonic potential. Fold. Des. 2:173-181. (Pubitemid 127740467)
44. Chen, J., G. Lu, ..., F. A. Quiocho. 2003. A tweezers-like motion of the ATP-binding cassette dimer in an ABC transport cycle. Mol. Cell. 12:651-661. (Pubitemid 37222486)
45. Karpowich, N., O. Martsinkevich, ..., J. F. Hunt. 2001. Crystal structures of the MJ1267 ATP binding cassette reveal an induced-fit effect at the ATPase active site of an ABC transporter. Structure. 9:571-586. (Pubitemid 32695582)
46. Zaitseva, J., C. Oswald, ..., L. Schmitt. 2006. A structural analysis of asymmetry required for catalytic activity of an ABC-ATPase domain dimer. EMBO J. 25:3432-3443. (Pubitemid 44141799)
47. Urbatsch, I. L., B. Sankaran, ..., A. E. Senior. 1995. P-glycoprotein is stably inhibited by vanadate-induced trapping of nucleotide at a single catalytic site. J. Biol. Chem. 270:19383-19390.
48. Sankaran, B., S. Bhagat, and A. E. Senior. 1997. Inhibition of P-glycoprotein ATPase activity by beryllium fluoride. Biochemistry. 36:6847- 6853. (Pubitemid 27242346)
49. Russell, P. L., and F. J. Sharom. 2006. Conformational and functional characterization of trapped complexes of the P-glycoprotein multidrug transporter. Biochem. J. 399:315-323. (Pubitemid 44570294)
50. Sauna, Z. E., M. Müller, ..., S. V. Ambudkar. 2002. Importance of the conservedWalker 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. (Pubitemid 35364871)
51. Tombline, G., L. A. Bartholomew, ..., A. E. Senior. 2004. Properties of P-glycoprotein with mutations in the "catalytic carboxylate" glutamate residues. J. Biol. Chem. 279:46518-46526. (Pubitemid 39518295)
52. Sauna, Z. E., I. W. Kim, ..., S. V. Ambudkar. 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. (Pubitemid 350223906)
53. Siarheyeva, A., R. Liu, and F. J. Sharom. 2010. Characterization of an asymmetric occluded state of P-glycoprotein with two bound nucleotides: implications for catalysis. J. Biol. Chem. 285:7575-7586.
54. Fetsch, E. E., and A. L. Davidson. 2002. Vanadate-catalyzed photocleavage of the signature motif of an ATP-binding cassette (ABC) transporter. Proc. Natl. Acad. Sci. USA. 99:9685-9690. (Pubitemid 34831108)
55. Hunke, S., S. Döse, and E. Schneider. 1995. Vanadate and bafilomycin A1 are potent inhibitors of the ATPase activity of the reconstituted bacterial ATP-binding cassette transporter for maltose (MalFGK2). Biochem. Biophys. Res. Commun. 216:589-594.
56. Davidson, A. L., S. S. Laghaeian, and D. E. Mannering. 1996. The maltose transport system of Escherichia coli displays positive cooperativity in ATP hydrolysis. J. Biol. Chem. 271:4858-4863. (Pubitemid 26074972)
57. Oloo, E. O., and D. P. Tieleman. 2004. Conformational transitions induced by the binding of MgATP to the vitamin B12 ATP-binding cassette (ABC) transporter BtuCD. J. Biol. Chem. 279:45013-45019. (Pubitemid 39430915)
58. Kandt, C., and D. P. Tieleman. 2010. Holo-BtuF stabilizes the open conformation of the vitamin B12 ABC transporter BtuCD. Proteins. 78:738-753.
59. Orelle, C., F. J. Alvarez, ..., A. L. Davidson. 2010. Dynamics of α-helical subdomain rotation in the intact maltose ATP-binding cassette transporter. Proc. Natl. Acad. Sci. USA. 107:20293-20298.
60. Sonne, J., C. Kandt, ..., D. P. Tieleman. 2007. Simulation of the coupling between nucleotide binding and transmembrane domains in the ATP binding cassette transporter BtuCD. Biophys. J. 92:2727- 2734. (Pubitemid 46557848)
61. Daus, M. L., M. Grote, ..., E. Schneider. 2007. ATP-driven MalK dimer closure and reopening and conformational changes of the "EAA" motifs are crucial for function of the maltose ATP-binding cassette transporter (MalFGK2). J. Biol. Chem. 282:22387-22396. (Pubitemid 47267345)
62. Oancea, G., M. L. O'Mara, ..., R. Tampé. 2009. Structural arrangement of the transmission interface in the antigen ABC transport complex TAP. Proc. Natl. Acad. Sci. USA. 106:5551-5556.
63. Zolnerciks, J. K., C. Wooding, and K. J. Linton. 2007. Evidence for a Sav1866-like architecture for the human multidrug transporter P-glycoprotein. FASEB J. 21:3937-3948. (Pubitemid 350232351)
64. Serohijos, A. W., T. Hegedus, ..., N. V. Dokholyan. 2008. Diminished self-chaperoning activity of the DeltaF508 mutant of CFTR results in protein misfolding. PLOS Comput. Biol. 4:e1000008.
65. Siarheyeva, A., J. J. Lopez, ..., C. Glaubitz. 2007. Probing the molecular dynamics of the ABC multidrug transporter LmrA by deuterium solid-state nuclear magnetic resonance. Biochemistry. 46:3075-3083. (Pubitemid 46449131)
66. Dalmas, O., C. Orelle, ..., J. M. Jault. 2005. The Q-loop disengages from the first intracellular loop during the catalytic cycle of the multidrug ABC transporter BmrA. J. Biol. Chem. 280:36857-36864. (Pubitemid 41587767)
67. Buchaklian, A. H., and C. S. Klug. 2005. Characterization of the Walker A motif of MsbA using site-directed spin labeling electron paramagnetic resonance spectroscopy. Biochemistry. 44:5503-5509. (Pubitemid 40489990)