Selectivity and cooperativity of modulatory ions in a neurotransmitter receptor

Biophysical Journal

Volumn 96, Issue 5, 2009, Pages 1751-1760

  Vijayan, Ranjit ^a,b   Plested, Andrew J R ^c   Mayer, Mark L ^c   Biggin, Philip C ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALKALI METAL; ANION; DIMER; KAINIC ACID RECEPTOR; MONOVALENT CATION; NEUROTRANSMITTER RECEPTOR; GLUR5 KAINATE RECEPTOR; ION; OXYGEN;

ARTICLE; BINDING KINETICS; BINDING SITE; CALCULATION; CRYSTAL STRUCTURE; ENERGY; MOLECULAR DYNAMICS; PROTEIN BINDING; PROTEIN STRUCTURE; SIMULATION; THERMODYNAMICS; X RAY; CHEMICAL MODEL; CHEMISTRY; COMPUTER SIMULATION; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; X RAY CRYSTALLOGRAPHY;

BINDING SITES; COMPUTER SIMULATION; CRYSTALLOGRAPHY, X-RAY; IONS; METALS, ALKALI; MODELS, CHEMICAL; OXYGEN; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; RECEPTORS, KAINIC ACID; THERMODYNAMICS;

EID: 65549085773     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2008.11.039     Document Type: Article

References (60)

1. Dingledine, R., K. Borges, D. Bowie, and S. F. Traynelis. 1999. The glutamate receptor ion channels. Pharmacol. Rev. 51:7-61.
2. Mayer, M. L. 2006. Glutamate receptors at atomic resolution. Nature. 440:456-462.
3. Hollmann, M., and S. F. Heinemann. 1994. Cloned glutamate receptors. Annu. Rev. Neurosci. 17:31-108.
4. Yamakura, T., and K. Shimoji. 1999. Subunit and site specific pharmacology of the NMDA receptor channel. Prog. Neurobiol. 59:279-298.
5. Lerma, J., M. Morales, M. A. Vicente, and O. Herreras. 1997. Glutamate receptors of the kainate type and synaptic transmission. Trends Neurosci. 20:9-12.
6. Watkins, J. C., and D. E. Jane. 2006. The glutamate story. Br. J. Pharmacol. 147:S100-S108.
7. DeVries, S. H., and E. A. Schwartz. 1999. Kainate receptors mediate synaptic transmission between cones and "Off" bipolar cells in a mammalian retina. Nature. 397:157-160.
8. Kidd, F. L., and J. T. R. Isaac. 1999. Developmental and activity-dependent regulation of kainate receptors at thalamocortical synapses. Nature. 400:569-573.
9. Collins, K. D., G. W. Neilson, and J. E. Enderby. 2007. Ions in water: characterizing the forces that control chemical processes and biological structure. Biophys. Chem. 128:95-104.
10. Glossmann, H., and P. Presek. 1979. Alpha-noradrenergic receptors in brain membranes: sodium, magnesium and guanyl nucleotides modulate agonist binding. Naunyn Schmiedebergs Arch. Pharmacol. 306:67-73.
11. Mayer, M. L., L. Vyklicky, Jr., and G. L. Westbrook. 1989. Modulation of excitatory amino acid receptors by group IIB metal cations in cultured mouse hippocampal neurones. J. Physiol. 415:329-350.
12. Smart, T. G., X. Xie, and B. J. Krishek. 1994. Modulation of inhibitory and excitatory amino acid receptor ion channels by zinc. Prog. Neurobiol. 42:393-441.
13. Vernino, S., M. Amador, C. W. Luetje, J. Patrick, and J. A. Dani. 1992. Calcium modulation and high calcium permeability of neuronal nicotinic acetylcholine receptors. Neuron. 8:127-134.
14. Bowie, D. 2002. External anions and cations distinguish betweenAMPA and kainate receptor gating mechanisms. J. Physiol. 539:725-733.
15. Plested, A., and M. L. Mayer. 2007. Structure and mechanism of kainate receptor modulation by anions. Neuron. 53:829-841.
16. - dipole couples agonist binding to kainate receptor activation. J. Neurosci. 27:6800-6809.
17. 2. Biophys. J. 82:676-683.
18. Arinaminpathy, Y., M. S. P. Sansom, and P. C. Biggin. 2006. Binding site flexibility: Molecular simulation of partial and full agonists within a glutamate receptor. Mol. Pharm. 69:11-18.
19. Kubo, M., and E. Ito. 2004. Structural dynamics of an ionotropic glutamate receptor. Proteins Struct. Funct. Bioinf. 56:411-419.
20. Lau, A. Y., and B. Roux. 2007. The free energy landscapes governing conformational changes in a glutamate receptor ligand binding domain. Structure. 15:1203-1214.
21. Mendieta, J., G. Ramirez, and F. Gago. 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. Genet. 44:460-469.
22. Speranskiy, K., and M. Kurnikova. 2005. On the binding determinants of the glutamate agonist with the glutamate receptor ligand binding domain. Biochemistry. 44:11508-11517.
23. Kollman, P. A. 1993. Free energy calculations: applications to chemical and biochemical phenomena. Chem. Rev. 93:2395-2417.
24. Mobley, D. L., J. D. Chodera, and K. A. Dill. 2006. On the use of orientational restraints and symmetry corrections in alchemical free energy calculations. J. Chem. Phys. 125:084902.
25. + binding sites with two differentmechanisms. J.Mol. Biol. 377:804-818.
26. Roux, B., M. Nina, R. Pomes, and J. C. Smith. 1996. Thermodynamic stability of water molecules in the bacteriorhodopsin proton channel: a molecular dynamics free energy perturbation study. Biophys. J. 71:670-681.
27. Roux, B. 1995. The calculation of the potential of mean force from computer simulations. Comput. Phys. Commun. 91:275-282.
28. Ivanov, I., X. Cheng, S. M. Sine, and J. A. McCammon. 2007. Barriers to ion translocation in cationic and anionic receptors from the Cys-loop family. J. Am. Chem. Soc. 129:8217-8224.
29. Khurana, E., S. O. Nielsen, B. Ensing, and M. L. Klein. 2006. Self-assembling cyclic peptides: molecular dynamics studies of dimers in polar and nonpolar solvents. J. Phys. Chem. B. 110:18965-18972.
30. Lu, D., P. Grayson, and K. Schulten. 2003. Glycerol conductance and physical asymmetry of the Escherichia coli glycerol facilitator GlpF. Biophys. J. 85:2977-2987.
31. Allen, T. W., O. S. Andersen, and B. Roux. 2004. Energetics of ion conduction through the gramicidin channel. Proc. Natl. Acad. Sci. USA. 101:117-122.
32. Beckstein, O., and M. S. P. Sansom. 2006. A hydrophobic gate in an ion channel: the closed state of the nicotinic acetylcholine receptor. Phys. Biol. 3:147-159.
33. Tieleman, D. P., and S. J. Marrink. 2006. Lipids out of equilibrium: energetics of desorption and pore mediated flip-flop. J. Am. Chem. Soc. 128:12462-12467.
34. Plested, A. J. R., R. Vijayan, P. C. Biggin, and M. L. Mayer. 2008. Molecular basis of kainate receptor modulation by sodium. Neuron. 58:720-735.
35. Deming, D., Q. Cheng, and V. Jayaraman. 2003. Is the isolated ligand binding domain a good model of the domain in the native receptor? J. Biol. Chem. 278:17589-17592.
36. van der Spoel, D., E. Lindahl, B. Hess, G. Groenhof, A. E. Mark, et al. 2005. GROMACS: fast, flexible and free. J. Comput. Chem. 26: 1701-1718.
37. Jorgensen, W. L., D. S. Maxwell, and J. Tirado-Rives. 1996. Development and testing of the OPLS all-atom force field on conformational energetics and properties of organic liquids. J. Am. Chem. Soc. 118:11225-11236.
38. Kaminski, G. A., R. A. Friesner, J. Tirado-Rives, and W. L. Jorgensen. 2001. Evaluation and reparameterization of the OPLS-AA force field for proteins via comparison with accurate quantum chemical calculations on peptides. J. Phys. Chem. B. 105:6474-6487.
39. Van Gunsteren, W. F., and H. J. C. Berendsen. 1988. A leap-frog algorithm for stochastic dynamics. Mol. Simul. 1:173-185.
40. Hess, B., J. 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.
41. Miyamoto, S., and P. A. Kollman. 1992. SETTLE: an analytical version of the SHAKE and RATTLE algorithms for rigid water molecules. J. Comput. Chem. 18:1463-1472.
42. Essman, U., L. Perera, M. L. Berkowitz, T. Darden, H. Lee, et al. 1995. A smooth particle mesh Ewald method. J. Chem. Phys. 103:8577-8593.
43. Mobley, D. L., M. L. Dumont, J. D. Chodera, and K. A. Dill. 2007. Comparison of charge models for fixed-charged force fields: small molecule hydration free energies in explicit solvent. J. Phys. Chem. B. 111:2242-2254.
44. Jorgensen, W. L., J. Chandresekhar, J. D. Madura, R. W. Impey, and M. L. Klein. 1983. Comparison of simple potential functions for simulating liquid water. J. Chem. Phys. 79:926-935.
45. Humphrey, W., A. Dalke, and K. Schulten. 1996. VMD - visual molecular dynamics. J. Mol. Graph. 14:33-38.
46. DeLano, W. L. 2004. The PyMOL Molecular Graphics System. DeLano Scientific, San Carlos, CA.
47. Allen, M. P., and D. J. Tildesley. 1987. Computer Simulation of Liquids. Oxford University Press, Oxford.
48. Kumar, S., D. Bouzida, R. H. Swendsen, P. A. Kollman, and J. M. Rosenberg. 1992. The weighted histogram analysis method for free energy calculations of biomolecules. I. The method. J. Comput. Chem. 13:1011-1021.
49. Harding, M. 2002. Metal-ligand geometry relevant to proteins and in proteins: sodium and potassium. Acta Crystallogr. D. 58:872-874.
50. Marcus,Y. 1988. Ionic radii in aqueous solutions. Chem.Rev. 88:1475-1498.
51. Vrbka, L., J. Vondrasek, B. Jagoda-Cwiklik, R. Vacha, and P. Jungwirth. 2006. Quantification and rationalization of the higher affinity of sodium over potassium to protein surfaces. Proc. Natl. Acad. Sci. USA. 103:15440-15444.
52. Baker, N. A., D. Sept, S. Joseph, M. J. Holst, and J. A. McCammon. 2001. Electrostatics of nanosystems: application to microtubules and the ribosome. Proc. Natl. Acad. Sci. USA. 98:10037-10041.
53. Jope, R. S. 1999. Anti-bipolar therapy: mechanism of action of lithium. Mol. Psychiatry. 4:117-128.
54. 3H-γ-aminobutyric acid from striatal neurons in primary culture: potentiation by lithium ions. Mol. Pharmacol. 38:229-236.
55. Altschul, S. F., W. Gish, W. Miller, E. W. Myers, and D. J. Lipman. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410.
56. Pineda, A. O., Z. -W. Chen, S. Caccia, A. M. Cantwell, S. N. Savvides, et al. 2004. The anticoagulant thrombin mutant W215A/E217A has a collapsed primary specificity pocket. J. Biol. Chem. 279:39824-39828.
57. Tikhonov, D. B., and B. S. Zhorov. 2005. Modeling P-loops domain of sodium channel: homology with potassium channels and interaction with ligands. Biophys. J. 88:184-197.
58. Eisenman, G. 1962. Cation-selective glass electrodes and their mode of operation. Biophys. J. 2:259-323.
59. Noskov, S. Y., and B. Roux. 2006. Ion selectivity in potassium channels. Biophys. Chem. 124:279-291.
60. Noskov, S. Y., and B. Roux. 2007. Importance of hydration and dynamics on the selectivity of the KcsA and NaK channels. J. Gen. Physiol. 129:135-143.