ATP-induced conformational changes of nucleotide-binding domains in an ABC transporter. Importance of the water-mediated entropic force

Journal of Physical Chemistry B

Volumn 118, Issue 44, 2014, Pages 12612-12620

  Hayashi, Tomohiko ^a   Chiba, Shuntaro ^a   Kaneta, Yusuke ^a   Furuta, Tadaomi ^a   Sakurai, Minoru ^a  

^a TOKYO INSTITUTE OF TECHNOLOGY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; CONFORMATIONAL CHANGE; NUCLEOTIDE-BINDING DOMAIN;

ABC TRANSPORTER; ADENOSINE TRIPHOSPHATE; ESCHERICHIA COLI PROTEIN; MALTOSE TRANSPORT SYSTEM, E COLI; PROTEIN BINDING; WATER;

BINDING SITE; CHEMISTRY; DIMERIZATION; ENTROPY; ENZYMOLOGY; ESCHERICHIA COLI; HYDROLYSIS; MOLECULAR DYNAMICS; PROTEIN CONFORMATION; PROTEIN TERTIARY STRUCTURE;

ADENOSINE TRIPHOSPHATE; ATP-BINDING CASSETTE TRANSPORTERS; BINDING SITES; DIMERIZATION; ENTROPY; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; HYDROLYSIS; MOLECULAR DYNAMICS SIMULATION; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; WATER;

EID: 84908635294     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/jp507930e     Document Type: Article

References (63)

1. Linton, K. J.; Higgins, C. F. The Escherichia coli ATP-Binding Cassette (ABC) Proteins. Mol. Microbiol. 1998, 28, 5-13.
2. Hollenstein, K.; Frei, D. C.; Locher, K. P. Structure of an ABC Transporter in Complex with Its Binding Protein. Nature 2007, 446, 213-216.
3. Oldham, M. L.; Davidson, A. L.; Chen, J. Structural Insights into ABC Transporter Mechanism. Curr. Opin. Struct. Biol. 2008, 18, 726-733.
4. Rees, D. C.; Johnson, E.; Lewinson, O. ABC Transporters: The Power to Change. Nat. Rev. Mol. Cell Biol. 2009, 10, 218-227.
5. Aller, S. G.; Yu, J.; Ward, A.; Weng, Y.; Chittaboina, S.; Zhuo, R.; Harrell, P. M.; Trinh, Y. T.; Zhang, Q.; Urbatsch, I. L.; Chang, G. Structure of P-Glycoprotein Reveals a Molecular Basis for Poly-Specific Drug Binding. Science 2009, 323, 1718-1722.
6. Khare, D.; Oldham, M. L.; Orelle, C.; Davidson, A. L.; Chen, J. Alternating Access in Maltose Transporter Mediated by Rigid-Body Rotations. Mol. Cell 2009, 33, 528-536.
7. Oldham, M. L.; Khare, D.; Quiocho, F. A.; Davidson, A. L.; Chen, J. Crystal Structure of a Catalytic Intermediate of the Maltose Transporter. Nature 2007, 450, 515-521.
8. Ward, A.; Reyes, C. L.; Yu, J.; Roth, C. B.; Chang, G. Flexibility in the ABC Transporter MsbA: Alternating Access with a Twist. Proc. Natl. Acad. Sci. U.S.A. 2007, 104, 19005-19010.
9. Jardetzky, O. Simple Allosteric Model for Membrane Pumps. Nature 1966, 211, 969-970.
10. Smith, P. C.; Karpowich, N.; Millen, L.; Moody, J. E.; Rosen, J.; Thomas, P. J.; Hunt, J. F. ATP Binding to the Motor Domain from an ABC Transporter Drives Formation of a Nucleotide Sandwich Dimer. Mol. Cell 2002, 10, 139-149.
11. Oswalt, C.; Holland, I. B.; Schmitt, L. The Motor Domains of ABC-Transporters, What Can Structures Tell Us? Naunyn-Schmiedeberg's Arch. Pharmacol. 2006, 372, 385-399.
12. Moody, J. E.; Millen, L.; Binns, D.; Hunt, J. F.; Thomas, P. J. Cooperative, ATP-dependent Association of the Nucleotide Binding Cassettes during the Catalytic Cycle of ATP-binding Cassette Transporters. J. Biol. Chem. 2002, 277, 21111-21114.
13. Janas, E.; Hofacker, M.; Chen, M.; Gompf, S.; van der Dose, C.; Tampe, R. The ATP Hydrolysis Cycle of the Nucleotide-Binding Domain of the Mitochondrial ATP-Binding Cassette Transporter Mdl1p. J. Biol. Chem. 2003, 278, 26862-26869.
14. Higgins, C. F.; Linton, K. J. The ATP Switch Model for ABC Transporters. Nat. Struct. Mol. Biol. 2004, 11, 918-926.
15. Linton, K. J.; Higgins, C. F. Structure and Function of ABC Transporters: The ATP Switch Provides Flexible Control. Pflügers Archiv: European Journal of Physiology 2007, 453, 555-567.
16. Wen, P. C.; Tajkhorshid, E. Dimer Opening of the Nucleotide Binding Domains of ABC Transporters after ATP Hydrolysis. Biophys. J. 2008, 95, 5100-5110.
17. Newstead, S.; Fowler, P. W.; Bilton, P.; Carpenter, E. P.; Sadler, P. J.; Campopiano, D. J.; Sansom, M. S. P.; Iwata, S. Insights into How Nucleotide-Binding Domains Power ABC Transport. Structure 2009, 17, 1213-1222.
18. Watanabe, Y.; Hsu, W. L.; Chiba, S.; Hayashi, T.; Furuta, T.; Sakurai, M. Dynamics and Structural Changes Induced by ATP and/or Substrate Binding in the Inward-Facing Conformation State of P-glycoprotein. Chem. Phys. Lett. 2013, 557, 145-149.
19. Furukawa-Hagiya, T.; Furuta, T.; Chiba, S.; Sohma, Y.; Sakurai, M. The Power Stroke Driven by ATP Binding in CFTR as Studied by Molecular Dynamics Simulations. J. Phys. Chem. B 2013, 117, 83-93.
20. Beglov, D.; Roux, B. Numerical Solution of the Hypernetted Chain Equation for a Solute of Arbitrary Geometry in Three Dimensions. J. Chem. Phys. 1995, 103, 360-364.
21. Kovalenko, A.; Hirata, F. Self-Consistent Description of a Metal-Water Interface by the Kohn-Sham Density Functional Theory and the Three-Dimensional Reference Interaction Site Model. J. Chem. Phys. 1999, 110, 10095-10112.
22. Imai, T.; Harano, Y.; Kinoshita, M.; Kovalenko, A.; Hirata, F. A Theoretical Analysis on Hydration Thermodynamics of Proteins. J. Chem. Phys. 2006, 125, 024911-1-024911-7).
23. Luchko, T.; Gusarov, S.; Roe, D. R.; Simmerling, C.; Case, D. A.; Tuszynski, J.; Kovalenko, A. Three-Dimensional Molecular Theory of Solvation Coupled with Molecular Dynamics in Amber. J. Chem. Theory Comput. 2010, 6, 607-624.
24. Honig, B.; Nicholls, A. Classical Electrostatics in Biology and Chemistry. Science 1995, 268, 1144-1149.
25. Imai, T.; Harano, Y.; Kinoshita, M.; Kovalenko, A.; Hirata, F. Theoretical Analysis on Changes in Thermodynamic Quantities upon Protein Folding: Essential Role of Hydration. J. Chem. Phys. 2007, 126, 225102-1-225102-9.
26. Imai, T.; Oda, K.; Kovalenko, A.; Hirata, F.; Kidera, A. Ligand Mapping on Protein Surfaces by the 3D-RISM Theory: Toward Computational Fragment-Based Drug Design. J. Am. Chem. Soc. 2009, 131, 12430-12440.
27. Imai, T.; Miyashita, N.; Sugita, Y.; Kovalenko, A.; Hirata, F.; Kidera, A. Functionality Mapping on Internal Surfaces of Multidrug Transporter AcrB Based on Molecular Theory of Solvation: Implications for Drug Efflux Pathway. J. Phys. Chem. B 2011, 115, 8288-8295.
28. Chong, S.-H.; Park, M.; Ham, S. Structural and Thermodynamic Characteristics That Seed Aggregation of Amyloid-β Protein in Water. J. Chem. Theory Comput. 2012, 8, 724-734.
29. Chong, S.-H.; Ham, S. Impact of Chemical Heterogeneity on Protein Self-Assembly in Water. Proc. Natl. Acad. Sci. U.S.A. 2012, 109, 7636-7641.
30. Genheden, S.; Ryde, U. How to Obtain Statistically Converged MM/GBSA Results. J. Comput. Chem. 2010, 31, 837-846.
31. Swanson, J. M.; Henchman, R. H.; McCammon, J. A. Revisiting Free Energy Calculations: A Theoretical Connection to MM/PBSA and Direct Calculation of the Association Free Energy. Biophys. J. 2004, 86, 67-74.
32. Hornak, V.; Abel, R.; Okur, A.; Strockbine, B.; Roitberg, A.; Simmerling, C. Comparison of Multiple Amber Force Fields and Development of Improved Protein Backbone Parameters. Proteins 2006, 65, 712-725.
33. Meagher, K. L.; Redman, L. T.; Carlson, H. A. Development of Polyphosphate Parameters for Use with the AMBER Force Field. J. Comput. Chem. 2003, 24, 1016-1025.
34. Lepšík, M.; Kříž, Z.; Havlas, Z. Efficiency of a Second-Generation HIV-1 Protease Inhibitor Studied by Molecular Dynamics and Absolute Binding Free Energy Calculations. Proteins 2004, 57, 279-293.
35. Lu, G.; Westbrooks, J. M.; Davidson, A. L.; Chen, J. ATP Hydrolysis Is Required to Reset the ATP-Binding Cassette Dimer into the Resting-State Conformation. Proc. Natl. Acad. Sci. U.S.A. 2005, 102, 17969-17974.
36. Neria, E.; Fischer, S.; Karplus, M. Simulation of Activation Free Energies in Molecular Systems. J. Chem. Phys. 1996, 105, 1902-1921.
37. Case, D. A.; Darden, T. A.; Cheatham, T. E., III; Simmerling, C. L.; Wang, J.; Duke, R. E.; Luo, R.; Walker, R. C.; Zhang, W.; Merz, K. M. et al. AMBER 12; University of California: San Francisco, 2012.
38. Amaro, R. E.; Cheng, X.; Ivanov, L.; Xu, D.; McCammon, J. A. Characterizing Loop Dynamics and Ligand Recognition in Human- and Avian-Type Influenza Neuraminidases via Generalized Born Molecular Dynamics and End-Point Free Energy Calculations. J. Am. Chem. Soc. 2009, 131, 4702-4709.
39. Chang, C. A.; Chen, W.; Gilson, M. K. Ligand Configurational Entropy and Protein Binding. Proc. Natl. Acad. Sci. U.S.A. 2007, 104, 1534-1539.
40. Oldham, M. L.; Chen, J. Snapshots of the Maltose Transporter During ATP Hydrolysis. Proc. Natl. Acad. Sci. U.S.A. 2011, 108, 15152-15156.
41. Zoghbi, M. E.; Fuson, K. L.; Sutton, R. B.; Altenberg, G. A. Kinetics of the Association/Dissociation Cycle of an ATP-Binding Cassette Nucleotide-Binding Domain. J. Biol. Chem. 2012, 287, 4157-4164.
42. Marti-Renom, M. A.; Madhusudhan, M. S.; Šali, A. Alignment of Protein Sequences by Their Profiles. Protein Sci. 2004, 13, 1071-1087.
43. Šali, A.; Potterton, L.; Yuan, F.; van Vlijmen, H.; Karplus, M. Evaluation of Comparative Protein Modeling by MODELLER. Proteins 1995, 23, 318-326.
44. Dolinsky, T. J.; Nielsen, J. E.; McCammon, J. A.; Baker, N. PDB2PQR: An Automated Pipeline for the Setup of Poisson-Boltzmann Electrostatics Calculations. Nucleic Acids Res. 2004, 32, W665-W667.
45. Allen, M. P.; Tildesley, D. J. Computer Simulation of Liquids; Oxford University Press: New York, 1987.
46. Berendsen, H. J. C.; Postma, J. P. M.; van Gunsteren, W. F.; DiNola, A.; Haak, J. Molecular Dynamics with Coupling to an External Bath. R. J. Chem. Phys. 1984, 81, 3684-3690.
47. Andersen, H. C. Rattle: A "Velocity" Version of the Shake Algorithm for Molecular Dynamics Calculations. J. Comput. Phys. 1983, 52, 24-34.
48. Darden, T.; York, D.; Pedersen, L. Particle Mesh Ewald: An Nlog(N) Method for Ewald Sums in Large Systems. J. Chem. Phys. 1993, 98, 10089-10092.
49. Essmann, U.; Perera, L.; Berkowitz, M. L.; Darden, T.; Lee, H.; Pedersen, L. G. A Smooth Particle Mesh Ewald Method. J. Chem. Phys. 1995, 103, 8577-8593.
50. Gilson, M. K.; Given, J. A.; Bush, B. L.; McCammon, J. A. The Statistical-Thermodynamic Basis for Computation of Binding Affinities: A Critical Review. Biophys. J. 1997, 72, 1047-1069.
51. Kinoshita, M. Spatial Distribution of a Depletion Potential Between a Big Solute of Arbitrary Geometry and a Big Sphere Immersed in Small Spheres. J. Chem. Phys. 2002, 116, 3493-3501.
52. Kinoshita, M. Ordered Aggregation of Big Bodies with High Asphericity in Small Spheres: A Possible Mechanism of the Amyloid Fibril Formation. Chem. Phys. Lett. 2004, 387, 54-60.
53. Yoshidome, T.; Kinoshita, M.; Hirota, S.; Baden, N.; Terazima, M. Molecular Origin of the Hydrophobic Effect: Analysis Using the Angle-Dependent Integral Equation Theory. J. Chem. Phys. 2008, 128, 225104-1-225104-9.
54. Oshima, H.; Yasuda, S.; Yoshidome, T.; Ikeguchi, M.; Kinoshita, M. Crucial Importance of the Water-Entropy Effect in Predicting Hot Spots in Protein-Protein Complexes. Phys. Chem. Chem. Phys. 2011, 13, 16236-16246.
55. Chiba, S.; Harano, Y.; Roth, R.; Kinoshita, M.; Sakurai, M. Evaluation of Protein-Ligand Binding Free Energy Focused on Its Entropic Components. J. Comput. Chem. 2012, 33, 550-560.
56. Dill, K. A. Dominant Forces in Protein Folding. Biochemistry 1990, 29, 7133-7155.
57. Kinoshita, M. Molecular Origin of the Hydrophobic Effect: Analysis Using the Angle-Dependent Integral Equation Theory. J. Chem. Phys. 2008, 128, 024507-1-024507-14.
58. Sanchez, I. C.; Truskett, T. M.; in 't Veld, P. J. Configurational Properties and Corresponding States in Simple Fluids and Water. J. Phys. Chem. B 1999, 103, 5106-5116.
59. Imai, T.; Harano, Y.; Kinoshita, M.; Kovalenko, A.; Hirata, F. Theoretical Analysis on Changes in Thermodynamic Quantities upon Protein Folding: Essential Role of Hydration. J. Chem. Phys. 2007, 126, 225102-1-225102-9.
60. Fischer, S.; Verma, C. S. Binding of Buried Structural Water Increases the Flexibility of Proteins. Proc. Natl. Acad. Sci. U.S.A. 1999, 96, 9613-9615.
61. Fischer, S.; Smith, J. C.; Verma, C. S. Dissecting the Vibrational Entropy Change on Protein/Ligand Binding: Burial of a Water Molecule in Bovine Pancreatic Trypsin Inhibitor. J. Phys. Chem. B 2001, 105, 8050-8055.
62. Moritsugu, K. B.; Njunda, M.; Smith, J. C. Theory and Normal-Mode Analysis of Change in Protein Vibrational Dynamics on Ligand Binding. J. Phys. Chem. B 2010, 114, 1479-1485.
63. Oliveira, A. S. F.; Baptista, A. M.; Soares, C. M. Inter-domain Communication Mechanisms in an ABC Importer: A Molecular Dynamics Study of the MalFGK2E Complex. PLOS Comput. Biol. 2011, 7, e1002128-1-e1002128-12.