Kainate induces various domain closures in AMPA and kainate receptors

Neurochemistry International

Volumn 61, Issue 4, 2012, Pages 536-545

  Venskutonyte, Raminta ^a   Frydenvang, Karla ^a   Hald, Helle ^a,b   Rabassa, Anna Ceravalls De ^a   Gajhede, Michael ^a   Ahring, Philip K ^b   Kastrup, Jette Sandholm ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b NEUROSEARCH A S   (Denmark)

Author keywords

Binding site interactions; Crystal structures; Domain closure; Electrophysiology; Ionotropic glutamate receptors

Indexed keywords

ALPHA AMINO 3 HYDROXY 5 METHYL 4 ISOXAZOLEPROPIONIC ACID; GLYCEROL; KAINIC ACID; KAINIC ACID RECEPTOR;

ANIMAL CELL; ARTICLE; ARTIFACT; BINDING SITE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; CRYSTALLIZATION; ELECTROPHYSIOLOGY; LIGAND BINDING; LIGAND BINDING DOMAIN; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; PROTEIN DOMAIN;

ANIMALS; BINDING SITES; CRYSTALLIZATION; HUMANS; KAINIC ACID; MODELS, MOLECULAR; RECEPTORS, AMPA; RECEPTORS, KAINIC ACID;

EID: 84865722870     PISSN: 01970186     EISSN: 18729754     Source Type: Journal    
DOI: 10.1016/j.neuint.2012.02.016     Document Type: Article

References (47)

1. P.D. Adams, R.W. Grosse-Kunstleve, L.W. Hung, T.R. Ioerger, A.J. McCoy, N.W. Moriarty, R.J. Read, J.C. Sacchettini, N.K. Sauter, and T.C. Terwilliger PHENIX: building new software for automated crystallographic structure determination Acta Crystallogr.; Sect. D: Biol. Crystallogr. 58 2002 1948 1954
2. A.H. Ahmed, Q. Wang, H. Sondermann, and R.E. Oswald Structure of the S1S2 glutamate binding domain of GluR3 Proteins 75 2009 628 637
3. N. Armstrong, and E. Gouaux Mechanisms for activation and antagonism of an AMPA-sensitive glutamate receptor: crystal structures of the GluR2 ligand binding core Neuron 28 2000 165 181
4. N. Armstrong, M. Mayer, and E. Gouaux 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 2003 5736 5741
5. N. Armstrong, J. Jasti, M. Beich-Frandsen, and E. Gouaux Measurement of conformational changes accompanying desensitization in an ionotropic glutamate receptor Cell 127 2006 85 97
6. P.T. Atlason, C.L. Scholefield, R.J. Eaves, M.B. Mayo-Martin, D.E. Jane, and E. Molnár Mapping the ligand binding sites of kainate receptors: molecular determinants of subunit-selective binding of the antagonist [3H]UBP310 Mol. Pharmacol. 78 2010 1036 1045
7. D. Bowie Ionotropic glutamate receptors & CNS disorders CNS Neurol. Disord. Drug Targets 7 2008 129 143
8. Collaborative Computational Project, No.4, 1994. The CCP4 suite: programs for protein crystallography. Acta Crystallogr.; Sect. D: Biol. Crystallogr. 50, 760-763.
9. A. Contractor, C. Mulle, and G.T. Swanson Kainate receptors coming of age: milestones of two decades of research Trends Neurosci. 34 2011 154 163
10. P. Emsley, and K. Cowtan Coot: model-building tools for molecular graphics Acta Crystallogr.; Sect. D: Biol. Crystallogr. 60 2004 2126 2132
11. M.W. Fleck, E. Cornell, and S.J. Mah Amino-acid residues involved in glutamate receptor 6 kainate receptor gating and desensitization J. Neurosci. 23 2003 1219 1227
12. A. Frandsen, D.S. Pickering, B. Vestergaard, C. Kasper, B.B. Nielsen, J.R. Greenwood, G. Campiani, C. Fattorusso, M. Gajhede, A. Schousboe, and J.S. Kastrup Tyr702 is an important determinant of agonist binding and domain closure of the ligand-binding core of GluR2 Mol. Pharmacol. 67 2005 703 713
13. K. Frydenvang, L.L. Lash, P. Naur, P.A. Postila, D.S. Pickering, C.M. Smith, M. Gajhede, M. Sasaki, R. Sakai, O.T. Pentikaïnen, G.T. Swanson, and J.S. Kastrup Full domain closure of the ligand-binding core of the ionotropic glutamate receptor iGluR5 induced by the high affinity agonist dysiherbaine and the functional antagonist 8,9-dideoxyneodysiherbaine J. Biol. Chem. 284 2009 14219 14229
14. A. Gill, A. Birdsey-Benson, B.L. Jones, L.P. Henderson, and D.R. Madden Correlating AMPA receptor activation and cleft closure across subunits: crystal structures of the GluR4 ligand-binding domain in complex with full and partial agonists Biochemistry 47 2008 13831 13841
15. H. Hald, P. Naur, D.S. Pickering, D. Sprogoe, U. Madsen, D.B. Timmermann, P.K. Ahring, T. Liljefors, A. Schousboe, J. Egebjerg, M. Gajhede, and J.S. Kastrup Partial agonism and antagonism of the ionotropic glutamate receptor iGLuR5: structures of the ligand-binding core in complex with domoic acid and 2-amino-3-[5-tert-butyl-3-(phosphonomethoxy)-4-isoxazolyl]propionic acid J. Biol. Chem. 282 2007 25726 25736
16. H. Hald, P.K. Ahring, D.B. Timmermann, T. Liljefors, M. Gajhede, and J.S. Kastrup Distinct structural features of cyclothiazide are responsible for effects on peak current amplitude and desensitization kinetics at iGluR2 J. Mol. Biol. 391 2009 906 917
17. S. Hayward, and R.A. Lee Improvements in the analysis of domain motions in proteins from conformational change: DynDom version 1.50 J. Mol. Graphics Modell. 21 2002 181 183
18. R. Jin, T.G. Banke, M.L. Mayer, S.F. Traynelis, and E. Gouaux Structural basis for partial agonist action at ionotropic glutamate receptors Nat. Neurosci. 6 2003 803 810
19. R. Jin, S.K. Singh, S. Gu, H. Furukawa, A.I. Sobolevsky, J. Zhou, Y. Jin, and E. Gouaux Crystal structure and association behaviour of the GluR2 amino-terminal domain EMBO J. 28 2009 1812 1823
20. W. Kabsch XDS Acta Crystallogr.; Sect. D: Biol. Crystallogr. 66 2010 125 132
21. E. Karakas, N. Simorowski, and H. Furukawa Structure of the zinc-bound amino-terminal domain of the NMDA receptor NR2B subunit EMBO J. 28 2009 3910 3920
22. C. Kasper, K. Frydenvang, P. Naur, M. Gajhede, D.S. Pickering, and J.S. Kastrup Molecular mechanism of agonist recognition by the ligand-binding core of the ionotropic glutamate receptor 4 FEBS Lett. 582 2008 4089 4094
23. K. Keinänen, W. Wisden, B. Sommer, P. Werner, A. Herb, T.A. Verdoorn, B. Sakmann, and P.H. Seeburg A family of AMPA-selective glutamate receptors Science 249 1990 556 560
24. T. Kistler, and M.W. Fleck Functional consequences of natural substitutions in the GluR6 kainate receptor subunit ligand-binding site Channels (Austin) 1 2007 417 428
25. J. Kumar, and M.L. Mayer Crystal structures of the glutamate receptor ion channel GluK3 and GluK5 amino-terminal domains J. Mol. Biol. 404 2010 680 696
26. R.A. Laskowski, M.W. MacArthur, D.S. Moss, and J.M. Thornton PROCHECK: a program to check the stereochemical quality of protein structures J. Appl. Crystallogr. 26 1993 283 291
27. M.L. Mayer Crystal structures of the GluR5 and GluR6 ligand binding cores: molecular mechanisms underlying kainate receptor selectivity Neuron 45 2005 539 552
28. M.L. Mayer, A. Ghosal, N.P. Dolman, and D.E. Jane Crystal structures of the kainate receptor GluR5 ligand binding core dimer with novel GluR5-selective antagonists J. Neurosci. 26 2006 2852 2861
29. A.J. McCoy, R.W. Grosse-Kunstleve, P.D. Adams, M.D. Winn, L.C. Storoni, and R.J. Read Phaser crystallographic software J. Appl. Crystallogr. 40 2007 658 674
30. Moloney, M. G.;1998. Excitatory amino acids. Nat. Prod. Rep. 15, 205-219.
31. N.W. Moriarty, R.W. Grosse-Kunstleve, and P.D. Adams Electronic ligand builder and optimization workbench (eLBOW): a tool for ligand coordinate and restraint generation Acta Crystallogr.; Sect. D: Biol. Crystallogr. 65 2009 1074 1080
32. P. Naur, B. Vestergaard, L.K. Skov, J. Egebjerg, M. Gajhede, and J.S. Kastrup Crystal structure of the kainate receptor GluR5 ligand-binding core in complex with (S)-glutamate FEBS Lett. 579 2005 1154 1160
33. M.M. Nielsen, T. Liljefors, P. Krogsgaard-Larsen, and J. Egebjerg The selective activation of the glutamate receptor GluR5 by ATPA is controlled by serine 741 Mol. Pharmacol. 63 2003 19 25
34. A. Perrakis, R. Morris, and V.S. Lamzin Automated protein model building combined with iterative structure refinement Nat. Struct. Biol. 6 1999 458 463
35. D. Perrais, F. Coussen, and C. Mulle Atypical functional properties of GluK3-containing kainate receptors J. Neurosci. 29 2009 15499 15510
36. A.J. Plested, R. Vijayan, P.C. Biggin, and M.L. Mayer Molecular basis of kainate receptor modulation by sodium Neuron 58 2008 720 735
37. J. Pohlsgaard, K. Frydenvang, U. Madsen, and J.S. Kastrup Lessons from more than 80 structures of the GluA2 ligand-binding domain in complex with agonists, antagonists and allosteric modulators Neuropharmacology 60 2011 135 150
38. E. Sagot, D.S. Pickering, X. Pu, M. Umberti, T.B. Stensbol, B. Nielsen, M. Chapelet, J. Bolte, T. Gefflaut, and L. Bunch Chemo-enzymatic synthesis of a series of 2,4-syn-functionalized (S)-glutamate analogues: new insight into the structure-activity relation of ionotropic glutamate receptor subtypes 5, 6, and 7 J. Med. Chem. 51 2008 4093 4103
39. A.I. Sobolevsky, M.P. Rosconi, and E. Gouaux X-ray structure, symmetry and mechanism of an AMPA-subtype glutamate receptor Nature 462 2009 745 756
40. G.T. Swanson, R.W. Gereau 4th, T. Green, and S.F. Heinemann Identification of amino acid residues that control functional behavior in GluR5 and GluR6 kainate receptors Neuron 19 1997 913 926
41. G.T. Swanson, T. Green, and S.F. Heinemann Kainate receptors exhibit differential sensitivities to (S)-5-iodowillardiine Mol. Pharmacol. 53 1998 942 949
42. G.T. Swanson Targeting AMPA and kainate receptors in neurological disease: therapies on the horizon? Neuropsychopharmacology 34 2009 249 250
43. T. Tanaka, S. Tanaka, T. Fujita, K. Takano, H. Fukuda, K. Sako, and Y. Yonemasu Experimental complex partial seizures induced by a microinjection of kainic acid into limbic structures Prog. Neurobiol. 38 1992 317 334
44. S.F. Traynelis, L.P. Wollmuth, C.J. McBain, F.S. Menniti, K.M. Vance, K.K. Ogden, K.B. Hansen, H. Yuan, S.J. Myers, and R. Dingledine Glutamate receptor ion channels: structure, regulation, and function Pharmacol. Rev. 62 2010 405 496
45. R. Venskutonytė, K. Frydenvang, M. Gajhede, L. Bunch, D.S. Pickering, and J.S. Kastrup Binding site and interlobe interactions of the ionotropic glutamate receptor GluK3 ligand binding domain revealed by high resolution crystal structure in complex with (S)-glutamate J. Struct. Biol. 176 2011 307 314
46. R. Venskutonytė, S. Butini, S.S. Coccone, S. Gemma, M. Brindisi, V. Kumar, E. Guarino, S. Maramai, S. Valenti, A. Amir, E.A. Valadés, K. Frydenvang, J.S. Kastrup, E. Novellino, G. Campiani, and D.S. Pickering Selective kainate receptor (GluK1) ligands structurally based upon 1H-cyclopentapyrimidin-2,4(1H,3H)-dione: synthesis, molecular modeling, and pharmacological and biostructural characterization J. Med. Chem. 54 2011 4793 4805
47. M.C. Weston, C. Gertler, M.L. Mayer, and C. Rosenmund Interdomain interactions in AMPA and kainate receptors regulate affinity for glutamate J. Neurosci. 26 2006 7650 7658