Energetics of the cleft closing transition and the role of electrostatic interactions in conformational rearrangements of the glutamate receptor ligand binding domain

Biochemistry

Volumn 47, Issue 42, 2008, Pages 11077-11085

  Mamonova, Tatyana ^a   Yonkunas, Michael J ^a   Kurnikova, Maria G ^a  

^a CARNEGIE MELLON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING SITES; BIOCHEMISTRY; CRYSTAL STRUCTURE; ELECTROSTATICS; FLOW INTERACTIONS; LIGANDS;

CONFORMATIONAL REARRANGEMENTS; CONFORMATIONAL STATES; DIRECT INTERACTIONS; ELECTROSTATIC INTERACTION ENERGIES; ELECTROSTATIC INTERACTIONS; ENERGETIC DIFFERENCES; ENERGY WELLS; GLUTAMATE RECEPTORS; ION CONDUCTIONS; IONOTROPIC GLUTAMATE RECEPTORS; LIGAND BINDINGS; MODELING METHODS; PROTEIN RESIDUES; SOLVATION ENERGIES; STRUCTURAL SIMILARITIES; TRANSITION PATHWAYS; UMBRELLA SAMPLINGS; X-RAY STRUCTURES;

BINDING ENERGY;

GLUTAMATE RECEPTOR; LIGAND;

ARTICLE; BINDING SITE; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; ELECTRICITY; ENERGY TRANSFER; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN STRUCTURE; SOLVATION; THERMODYNAMICS; X RAY;

ANIMALS; APOPROTEINS; BINDING SITES; ELECTROSTATICS; LIGANDS; MODELS, MOLECULAR; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; RATS; RECEPTORS, AMPA; THERMODYNAMICS;

EID: 54349125556     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi801367d     Document Type: Article

References (37)

1. Mayer, M. L. (2006) Glutamate receptors at atomic resolution. Nature 440, 456-462.
2. Oswald, R. E., Ahmed, A., Fenwick, M. K., and Loh, A. P. (2007) Structure of glutamate receptors. Curr. Drug Targets 8, 573-582.
3. Mendieta, J., Ramirez, G., and Gago, F. (2001) Molecular dynamics simulations of the conformational changes of the glutamate receptor ligand-binding core in the presence of glutamate and kainate. Proteins: Struct., Funct., Bioinf. 44, 460-469.
4. Arinaminpathy, Y., Sansom, M. S. P., and Biggin, P. C. (2002) Molecular dynamics simulations of the ligand-binding domain of the ionotropic glutamate receptor GluR2. Biophys. J. 82, 676-683.
5. Speranskiy, K., and Kurnikova, M. (2004) Accurate theoretical prediction of vibrational frequencies in an inhomogeneous dynamic environment: A case study of a glutamate molecule in water solution and in a protein-bound form. J. Chem. Phys. 121, 1516-1524.
6. Speranskiy, K., and Kurnikova, M. (2005) On the binding determinants of the glutamate agonist with the glutamate receptor ligand binding domain. Biochemistry 44, 11508-11517.
7. Arinaminpathy, Y., Sansom, M. S. P., and Biggin, P. C. (2006) Binding site flexibility: Molecular simulation of partial and full agonists within a glutamate receptor. Mol. Pharmacol. 69, 5-12.
8. Lau, A. Y., and Roux, B. (2007) The free energy landscapes governing conformational changes in a glutamate receptor ligand-binding domain. Structure 15, 1203-1214.
9. Mamonova, T., Speranskiy, K., and Kurnikova, M. (2008) Interplay between structural rigidity and electrostatic interactions in the ligand binding domain of GluR2. Proteins: Struct., Funct., Bioinf. (in press).
10. Meir, A., Ginsburg, S., Butkevich, A., Kachalsky, S. G., Kaiserman, I., Ahdut, R., Demirgoren, S., and Rahamimoff, R. (1999) Ion channels in presynaptic nerve terminals and control of transmitter release. Physiol. Rev. 79, 1019-1088.
11. Armstrong, N., and Gouaux, E. (2000) Mechanisms for activation and antagonism of an AMPA-sensitive glutamate receptor: Crystal structures of the GluR2 ligand binding core. Neuron 28, 165-181.
12. Armstrong, N., Sun, Y., Chen, G. Q., and Gouaux, E. (1998) Structure of a glutamate-receptor ligand-binding core in complex with kainate. Nature 395, 913-917.
13. Jin, R., and Gouaux, E. (2003) Probing the function, conformational plasticity, and dimer-dimer contacts of the GluR2 ligand-binding core: Studies of 5-substituted willardiines and GluR2 S1S2 in the crystal. Biochemistry 42, 5201-5213.
14. Mayer, M. L. (2005) Crystal structures of the GluR5 and GluR6 ligand binding cores: Molecular mechanisms underlying kainate receptor selectivity. Neuron 45, 539-552.
15. Du, M., Reid, S. A., and Jayaraman, V. (2005) Conformational changes in the ligand-binding domain of a functional ionotropic glutamate receptor. J. Biol. Chem. 280, 8633-8636.
16. Li, G., Sheng, Z., Huang, Z., and Niu, L. (2005) Kinetic mechanism of channel opening of the GluRDflip AMPA receptor. Biochemistry 44, 5835-5841.
17. Ramanoudjame, G., Du, M., Mankiewicz, K. A., and Jayaraman, V. (2006) Allosteric mechanism in AMPA receptors: A FRET-based investigation of conformational changes. Proc. Natl. Acad. Sci. U.S.A. 103, 10473-10478.
18. Hogner, A., Kastrup, J. S., Jin, R., Liljefors, T., Mayer, M. L., Egebjerg, J., Larsen, I. K., and Gouaux, E. (2002) Structural basis for AMPA receptor activation and ligand selectivity: Crystal structures of five agonist complexes with the GluR2 ligand-binding core. J. Mol. Biol. 322, 93-109.
19. Jayaraman, V., Keesey, R., and Madden, D. R. (2000) Ligand-protein interactions in the glutamate receptor. Biochemistry 39, 8693-8697.
20. Robert, A., Armstrong, N., Gouaux, J. E., and Howe, J. R. (2005) AMPA receptor binding cleft mutations that alter affinity, efficacy, and recovery from desensitization. J. Neurosci. 25, 3752-3762.
21. Ahmed, A. H., Loh, A. P., Jane, D. E., and Oswald, R. E. (2007) Dynamics of the S1S2 glutamate binding domain of GluR2 measured using F-19 NMR spectroscopy. J. Biol. Chem. 282, 12773-12784.
22. Mankiewicz, K. A., Rambhadran, A., Du, M., Ramanoudjame, G., and Jayaraman, V. (2007) Role of the chemical interactions of the agonist in controlling α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor activation. Biochemistry 46, 1343-1349.
23. Abele, R., Keinanen, K., and Madden, D. R. (2000) Agonist-induced isomerization in a glutamate receptor ligand-binding domain: A kinetic and mutagenetic analysis. J. Biol. Chem. 275, 21355-21363.
24. Jin, R., Horning, M., Mayer, M. L., and Gouaux, E. (2002) Mechanism of activation and selectivity in a ligand-gated ion channel: Structural and functional studies of GluR2 and quisqualate. Biochemistry 41, 15635-15643.
25. Leach, A. R. (2001) Molecular modelling: Principles and applications, Pearson Education Ltd., Harlow, England.
26. Torrie, G. M., and Valleau, J. P. (1977) Nonphysical sampling distributions in Monte Carlo free-energy estimation: Umbrella sampling. J. Comput. Physiol. 23, 187-199.
27. Mamonova, T., and Kurnikova, M. (2006) Structure and energetics of channel-forming protein-polysaccharide complexes inferred via computational statistical thermodynamics. J. Phys. Chem. B 110, 25091-25100.
28. Case, D. A., Darden, T. A., Cheatham, T. E., III, Simmerling, C. L., Wang, J., Duke, R. E., Luo, R., Merz, K. M., Wang, B., Pearlman, D. A., Crowley, M., Brozell, S., Tsui, V., Gohlke, H., Mongan, J., Hornak, G., Beroza, P., Schafmeister, C., Caldwell, J. W., Ross, W. S., and Kollman, P. A. (2004) AMBER 8, University of California, San Francisco.
29. Cornell, W. D., Cieplak, P., Bayly, C. I., Gould, I. R., Merz, K. M., Ferguson, D. M., Spellmeyer, D. C., Fox, T., Caldwell, J. W., and Kollman, P. A. (1995) A 2Nd generation force-field for the simulation of proteins, nucleic-acids, and organic-molecules. J. Am. Chem. Soc. 117, 5179-5197.
30. Berendsen, H. J. C., Postma, J. P. M., Vangunsteren, W. F., Dinola, A., and Haak, J. R. (1984) Molecular dynamics with coupling to an external bath. J. Chem. Phys. 81, 3684-3690.
31. Ryckaert, J. P. C., and Berendsen, H. J. C. (1977) Numerical-integration of cartesian equations of motion of a system with constraints: Molecular-dynamics of n-alkanes. J. Comput. Phys. 23, 327-341.
32. Grossfield, A. (2004) An implementation of WHAM: The weighted histogram analysis method. http://dasher.wustl.edu/alan/wham.
33. Kurnikov, I. V. (1996) HARLEM: Molecular modeling program. http://harlemprog.org.
34. Kollman, P. A., Massova, I., Reyes, C., Kuhn, B., Huo, S., Chong, L., Lee, M., Lee, T., Duan, Y., Wang, W., Donini, O., Cieplak, P., Srinivasan, J., Case, D. A., and Cheatham, T. E., III (2000) Calculating structures and free energies of complex molecules: Combining molecular mechanics and continuum models. Acc. Chem. Res. 33, 889-897.
35. Deming, D., Cheng, Q., and Jayaraman, V. (2003) Is the isolated ligand binding domain a good model of the domain in the native receptor? J. Biol. Chem. 278, 17589-17592.
36. Weston, M. C., Gertler, C., Mayer, M. L., and Rosenmund, C. (2006) Interdomain interactions in AMPA and kainate receptors regulate affinity for glutamate. J. Neurosci. 26, 7650-7658.
37. Mayer, M. L., Olson, R., and Gouaux, E. (2001) Mechanisms for ligand binding to GluR0 ion channels: Crystal structures of the glutamate and serine complexes and a closed apo state. J. Mol. Biol. 311, 815-836.