Mechanisms of antagonism of the GluR2 AMPA receptor: Structure and dynamics of the complex of two willardiine antagonists with the glutamate binding domain

Biochemistry

Volumn 48, Issue 18, 2009, Pages 3894-3903

  Ahmed, Ahmed H ^a   Thompson, Melissa D ^a   Fenwick, Michael K ^a   Romero, Bethsabe ^a   Loh, Adrienne P ^b   Jane, David E ^c   Sondermann, Holger ^a   Oswald, Robert E ^a  

^a Cornell University ^*  (United States)

^b UNIVERSITY OF WISCONSIN LA CROSSE   (United States)

^c UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMPA-RECEPTOR; APO-STATE; BINDING DOMAIN; GLUTAMATE RECEPTOR; INTERNAL DYNAMICS; IONOTROPIC GLUTAMATE RECEPTORS; NATURAL PRODUCTS; NEUROLOGICAL DISORDERS; SPECIFIC INTERACTION; STRUCTURE AND DYNAMICS; SYNAPTIC TRANSMISSION; THERMAL STABILITY;

DYNAMICS;

CRYSTAL STRUCTURE;

3 (2 CARBOXYBENZYL)WILLARDIINE; 3 (2 CARBOXYETHYL)WILLARDIINE; 6 CYANO 7 NITRO 2,3 QUINOXALINEDIONE; 6,7 DINITRO 2,3 QUINOXALINEDIONE; AMPA RECEPTOR; GLUTAMIC ACID; IONOTROPIC RECEPTOR; UBP 277; UBP 282; UNCLASSIFIED DRUG; URACIL; WILLARDIINE;

ARTICLE; BINDING AFFINITY; BINDING SITE; COMPLEX FORMATION; DRUG MECHANISM; DRUG RECEPTOR BINDING; DRUG STRUCTURE; NEUROLOGIC DISEASE; PRIORITY JOURNAL; PROTEIN STRUCTURE; RECEPTOR BLOCKING; THERMOSTABILITY;

ALANINE; CALORIMETRY; CRYSTALLOGRAPHY, X-RAY; EXCITATORY AMINO ACID ANTAGONISTS; GLUTAMIC ACID; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; PROTEIN CONFORMATION; RADIOLIGAND ASSAY; RECEPTORS, AMPA; URACIL;

VERTEBRATA;

EID: 66149128065     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi900107m     Document Type: Article

References (41)

1. Dingledine, R., Borges, K., Bowie, D., and Traynelis, S. (1999) The glutamate receptor ion channels. Pharmacol. Rev. 51, 7-61. (Pubitemid 29113865)
2. Asztely, F., and Gustafsson, B. (1996) Ionotropic glutamate receptors. Their possible role in the expression of hippocampal synaptic plasticity. Mol. Neurobiol. 12, 1-11.
3. Rzeski, W., Turski, L., and Ikonomidou, C. (2001) Glutamate antagonists limit tumor growth. Proc. Natl. Acad. Sci. U. S. A. 98, 6372-6377. (Pubitemid 32488244)
4. Mayer, M. L. (2006) Glutamate receptors at atomic resolution. Nature 440, 456-462.
5. 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. (Pubitemid 36062468)
6. Sun, Y., Olson, R., Horning, M., Armstrong, N., Mayer, M., and Gouaux, E. (2002) Mechanism of glutamate receptor desensitization. Nature 417, 245-253. (Pubitemid 34534700)
7. Jin, R., Banke, T. G., Mayer, M. L., Traynelis, S. F., and Gouaux, E. (2003) Structural basis for partial agonist action at ionotropic glutamate receptors. Nat. Neurosci. 6, 803-810. (Pubitemid 36929700)
8. 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. (Pubitemid 36560416)
9. Fenwick, M. K., and Oswald, R. E. (2008) NMR spectroscopy of the ligand-binding core of ionotropic glutamate receptor 2 bound to 5- substituted willardiine partial agonists. J. Mol. Biol. 378, 673-685.
10. Maltsev, A. S., Ahmed, A. H., Fenwick, M. K., Jane, D. E., and Oswald, R. E. (2008) Mechanism of partial agonism at the GluR2 AMPA receptor: Measurements of lobe orientation in solution. Biochemistry 47, 10600-10610.
11. 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. (Pubitemid 28503434)
12. 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 19F NMR spectroscopy. J. Biol. Chem. 282, 12773-12784. (Pubitemid 47100589)
13. Armstrong, N., Mayer, M., and Gouaux, E. (2003) Tuning activation of the AMPA-sensitive GluR2 ion channel by genetic adjustment of agonist-induced conformational changes. Proc. Natl. Acad. Sci. U. S. A. 100, 5736-5741. (Pubitemid 36576877)
14. 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. (Pubitemid 44051191)
15. 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.
16. Hogner, A., Greenwood, J. R., Liljefors, T., Lunn, M. L., Egebjerg, J., Larsen, I. K., Gouaux, E., and Kastrup, J. S. (2003) Competitive antagonism of AMPA receptors by ligands of different classes: crystal structure of ATPO bound to the GluR2 ligand-binding core, in comparison with DNQX. J. Med. Chem. 46, 214-221. (Pubitemid 36082867)
17. Menuz, K., Stroud, R. M., Nicoll, R. A., and Hays, F. A. (2007) TARP auxiliary subunits switch AMPA receptor antagonists into partial agonists. Science 318, 815-817.
18. Kasper, C., Pickering, D. S., Mirza, O., Olsen, L., Kristensen, A. S., Greenwood, J. R., Liljefors, T., Schousboe, A., Watjen, F., Gajhede, M., Sigurskjold, B. W., and Kastrup, J. S. (2006) The structure of a mixed GluR2 ligand-binding core dimer in complex with (S)-glutamate and the antagonist (S)-NS1209. J. Mol. Biol. 357, 1184-1201. (Pubitemid 43357980)
19. 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. (Pubitemid 47542487)
20. Jane, D. E., Hoo, K., Kamboj, R., Deverill, M., Bleakman, D., and Mandelzys, A. (1997) Synthesis of willardiine and 6-azawillardiine analogs: pharmacological characterization on cloned homomeric human AMPA and kainate receptor subtypes. J. Med. Chem. 40, 3645-3650. (Pubitemid 27465096)
21. Dolman, N. P., Troop, H. M., More, J. C., Alt, A., Knauss, J. L., Nistico, R., Jack, S., Morley, R. M., Bortolotto, Z. A., Roberts, P. J., Bleakman, D., Collingridge, G. L., and Jane, D. E. (2005) Synthesis and pharmacology of willardiine derivatives acting as antagonists of kainate receptors. J. Med. Chem. 48, 7867-7881. (Pubitemid 41699834)
22. Hollmann, M., and Heinemann, S. (1994) Cloned glutamate receptors. Annu. Rev. Neurosci. 17, 31-108. (Pubitemid 24117025)
23. Chen, G. Q., Sun, Y., Jin, R., and Gouaux, E. (1998) Probing the ligand binding domain of the GluR2 receptor by proteolysis and deletion mutagenesis defines domain boundaries and yields a crystallizable construct. Protein Sci. 7, 2623-2630. (Pubitemid 28565704)
24. McFeeters, R. L., and Oswald, R. E. (2002) Structural mobility of the extracellular ligand-binding core of an ionotropic glutamate receptor. Analysis of NMR relaxation dynamics. Biochemistry 41, 10472-10481.
25. Maniatis, T., Fritsch, E. F., and Sambrook, J. ((1982) ) Molecular Cloning, Cold Spring Harbor Laboratory, New York..
26. Pace, C. N., Vajdos, F., Fee, L., Grimsley, G., and Gray, T. (1995) How to measure and predict the molar absorption coefficient of a protein. Protein Sci. 4, 2411-2423.
27. Salopek-Sondi, B., and Luck, L. A. (2002) 19F NMR study of the leucine-specific binding protein of Escherichia coli: mutagenesis and assignment of the 5-fluorotryptophan-labeled residues. Protein Eng. 15, 855-859. (Pubitemid 36172722)
28. Otwinowski, Z., and Minor, W. ((1997) ) Processing of X-ray diffraction data collected in oscillation mode, in Methods Enzymol., Vol.276, Macromolecular Crystallography, Part A (Carter, C. W., and Sweet, R. M., Eds.) pp 307-326, Academic Press, New York.. (Pubitemid 27085611)
29. Adams, P. D., Grosse-Kunstleve, R. W., Hung, L. W., Ioerger, T. R., McCoy, A. J., Moriarty, N. W., Read, R. J., Sacchettini, J. C., Sauter, N. K., and Terwilliger, T. C. (2002) PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr. D Biol. Crystallogr. 58, 1948-1954. (Pubitemid 35337293)
30. Brunger, A. T. (2007) Version 1.2 of the Crystallography and NMR system. Nat. Protoc. 2, 2728-2733.
31. Emsley, P., and Cowtan, K. (2004) Coot: model-building tools formolecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132. (Pubitemid 41742764)
32. Chen, G. Q., and Gouaux, E. (1997) Overexpression of a glutamate receptor (GluR2) ligand binding domain in Escherichia coli: application of a novel protein folding screen. Proc. Natl. Acad. Sci. U. S. A. 94, 13431-13436. (Pubitemid 28009599)
33. Sigurskjold, B. W. (2000) Exact analysis of competition ligand binding by displacement isothermal titration calorimetry. Anal. Biochem. 277, 260-266. (Pubitemid 30055877)
34. Madden, D. R., Abele, R., Andersson, A., and Keinanen, K. (2000) Large-scale expression and thermodynamic characterization of a glutamate receptor agonist-binding domain. Eur. J. Biochem. 267, 4281-4289. (Pubitemid 30436125)
35. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., and Bax, A. (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6, 277-293.
36. Mayer, M. L., Ghosal, A., Dolman, N. P., and Jane, D. E. (2006) Crystal structures of the kainate receptor GluR5 ligand binding core dimer with novel GluR5-selective antagonists. J. Neurosci. 26, 2852-2861.
37. Ahmed, A. H., Wang, Q., Sondermann, H., and Oswald, R. E. (2009) Structure of the S1S2 glutamate binding domain of GluR3. Proteins: Struct., Funct., Bioinf. 75, 628-637.
38. Valentine, E. R., and Palmer, A. G.3rd (2005) Microsecond-to-millisecond conformational dynamics demarcate the GluR2 glutamate receptor bound to agonists glutamate, quisqualate, and AMPA. Biochemistry 44, 3410-3417. (Pubitemid 40322011)
39. Zeng, L., Lu, L., Muller, M., Gouaux, E., and Zhou, M. M. (2002) Structure-based functional design of chemical ligands for AMPA-subtype glutamate receptors. J. Mol. Neurosci. 19, 113-116.
40. Wagner, G., Pardi, A., and Wuthrich, K. (1983) Hydrogen-bond length and H-1-NMR chemical-shifts in proteins. J. Am. Chem. Soc. 105, 5948-5949.
41. Hayward, S., and Lee, R. A. (2002) Improvements in the analysis of domain motions in proteins from conformational change: DynDom version 1.50. J. Mol. Graph. Model. 21, 181-183. (Pubitemid 35279848)