Mechanism of positive allosteric modulators acting on AMPA receptors

Journal of Neuroscience

Volumn 25, Issue 39, 2005, Pages 9027-9036

  Jin, Rongsheng ^a,d   Clark, Suzanne ^b   Weeks, Autumn M ^b   Dudman, Joshua T ^a   Gouaux, Eric ^a,c   Partin, Kathryn M ^b  

^a Columbia University ^*  (United States)

^b Veterinary Dentistry and Oral Surgery   (United States)

^c OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^d STANFORD UNIVERSITY   (United States)

Author keywords

Aniracetam; Crystallography; CX614; Cyclothiazide; Deactivation; Desensitization; Glutamate receptor; Kinetics

Indexed keywords

6 NITRO 7 SULFAMOYLBENZO[F]QUINOXALINE 2,3 DIONE; AMPA RECEPTOR; AMPA RECEPTOR AGONIST; ANIRACETAM; CX 614; CYCLOTHIAZIDE; DIMER; GLUTAMATE RECEPTOR; GLUTAMIC ACID; ION CHANNEL; KAINIC ACID RECEPTOR; KYNURENIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PYRROLIDINO 1,3 OXAZINO BENZO 1,4 DIOXAN 10 ONE; QUISQUALIC ACID; UNCLASSIFIED DRUG;

ALLOSTERISM; ALZHEIMER DISEASE; ARTICLE; COGNITIVE DEFECT; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; CRYSTALLOGRAPHY; DEGENERATIVE DISEASE; DEPRESSION; DRUG BINDING SITE; DRUG RECEPTOR BINDING; EMBRYO; HUMAN; HUMAN CELL; LIGAND BINDING; PATCH CLAMP; POINT MUTATION; PRIORITY JOURNAL; RECEPTOR DOWN REGULATION; SEDIMENTATION;

ALLOSTERIC REGULATION; BENZOTHIADIAZINES; BINDING SITES; CELL LINE; CRYSTALLOGRAPHY; DIMERIZATION; DRUG SYNERGISM; ELECTRIC CONDUCTIVITY; HUMANS; LIGANDS; MOLECULAR CONFORMATION; OXAZINES; PATCH-CLAMP TECHNIQUES; PROTEIN STRUCTURE, TERTIARY; PYRROLIDINONES; RECEPTORS, AMPA; TIME FACTORS;

EID: 25644454403     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2567-05.2005     Document Type: Article

References (45)

1. Arai A, Lynch G (1998) The waveform of synaptic transmission at hippocampal synapses is not determined by AMPA receptor desensitization. Brain Res 799:230-234.
2. Arai A, Kessler M, Xiao P, Ambros-Ingerson J, Rogers G, Lynch G (1994) A centrally active drug that modulates AMPA receptor gated currents. Brain Res 638:343-346.
3. Arai A, Kessler M, Ambros-Ingerson J, Quan A, Yigiter E, Rogers G, Lynch G (1996a) Effects of a centrally active benzoylpyrrolidine drug on AMPA receptors kinetics. Neuroscience 75:573-585.
4. Arai A, Kessler M, Rogers G, Lynch G (1996b) Effects of a memory-enhancing drug on D,L-alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor currents and synaptic transmission in hippocampus. J Pharmacol Exp Ther 278:627-638.
5. Arai AC, Kessler M, Rogers G, Lynch G (2000) Effects of the potent ampakine CX614 on hippocampal and recombinant AMPA receptors: interactions with cyclothiazide and GYKI 52466. Mol Pharmacol 58:802-813.
6. Armstrong N, 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.
7. Boulter J, Hollmann M, O'Shea-Greenfield A, Hartley M, Deneris E, Maron C, Heinemann S (1990) Molecular cloning and functional expression of glutamate receptor subunit genes. Science 249:1033-1037.
8. Brünger AT (1992) Free R value: a novel statistical quantity for assessing the accuracy of crystal structures. Nature 355:472-475.
9. Brünger AT, Adams PD, Clore GM, DeLano WL, Gros P, Grosse-Kunstleve RW, Jiang JS, Kuszewski J, Nilges M, Pannu NS, Read RJ, Rice LM, Simonson T, Warren GL (1998) Crystallography and NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr D Biol Crystallogr 54:905-921.
10. Chen GQ, 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 USA 94:13431-13436.
11. Delano WL (2005) The PyMOL molecular graphics system. San Carlos, CA: DeLano Scientific.
12. Dingledine R, Borges K, Bowie D, Traynelis SF (1999) The glutamate receptor ion channels. Pharmacol Rev 51:7-61.
13. Esnouf RM (1999) Further additions to MolScript version 1.4, including reading and contouring of electron density maps. Acta Crystallogr D Biol Crystallogr 55:938-940.
14. Fleck MW, Cornell E, Mah SJ (2003) Amino-acid residues involved in glutamate receptor 6 kainate receptor gating and desensitization. J Neurosci 23:1219-1227.
15. Horning M, Mayer M (2004) Regulation of AMPA receptor gating by ligand binding core dimers. Neuron 41:379-388.
16. Ingvar M, Ambros-Ingerson J, Davis M, Granger R, Kessler M, Rogers GA, Schehr RS, Lynch G (1997) Enhancement by an ampakine of memory encoding in humans. Exp Neurol 146:553-559.
17. Isaacson JS, Nicoll RA (1991) Aniracetam reduces glutamate receptor desensitization and slows the decay of fast excitatory synaptic currents in the hippocampus. Proc Natl Acad Sci USA 88:10936-10940.
18. Jin R, 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.
19. Jin R, Horning M, Mayer ML, 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.
20. Jin R, Banke T, Mayer ML, Traynelis SF, Gouaux E (2003) Structural basis for partial agonist action at ionotropic glutamate receptors. Nat Neurosci 6:803-810.
21. Jones TA, Kjeldgaard M (1997) Electron-density map interpretation. Methods Enzymol 277:173-208.
22. Jones TA, Zou JY, Cowan SW (1991) Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr A 47:110-119.
23. Kandel ER (2001) The molecular biology of memory storage: a dialogue between genes and synapses. Science 294:1030-1038.
24. Keinänen K, Wisden W, Sommer B, Werner P, Herb A, Verdoorn TA, Sakmann B, Seeburg PH (1990) A family of AMPA-selective glutamate receptors. Science 249:556-560.
25. Kleywegt GJ (1999) Experimental assessment of differences between related protein crystal structures. Acta Crystallogr D Biol Crystallogr 55:1878-1884.
26. Kraulis PJ (1991) MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J Appl Cryst 24:946-950.
27. Lawrence JJ, Brenowitz S, Trussell LO (2003) The mechanism of action of aniracetam at synaptic a-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptors: indirect and direct effects on desensitization. Mol Pharmacol 64:269-278.
28. Leever JD, Clark S, Weeks AM, Partin KM (2003) Identification of a site in GluR1 and GluR2 that is important for modulation of deactivation and desensitization. Mol Pharmacol 64:5-10.
29. Mayer ML, Armstrong N (2004) Structure and function of glutamate receptor ion channels. Annu Rev Physiol 66:161-181.
30. McFeeters RL, Oswald RE (2002) Structural mobility of the extracellular ligand-binding core of an ionotropic glutamate receptor. Analysis of NMR relaxation dynamics. Biochemistry 41:10472-10481.
31. Merritt EA, Murphy MEP (1994) Raster3D, version 2.0. A program for photorealistic molecular graphics. Acta Crystallogr D Biol Crystallogr 50:869-873.
32. Miu P, Jarvie KR, Radhakrishnan V, Gates MR, Ogden A, Ornstein PL, Zarrinmayeh H, Ho K, Peters D, Grabell J, Gupta A, Zimmerman DM, Bleakman D (2001) Novel AMPA receptor potentiators LY392098 and LY404187: effects on recombinant human AMPA receptors in vitro. Neuropharmacology 40:976-983.
33. Morris RG, Anderson E, Lynch GS, Baudry M (1986) Selective impairment of learning and blockage of long-term potentiation by an N-methyl-D-aspartate receptor antagonist, AP5. Nature 319:774-776.
34. Nagarajan N, Quast C, Boxall AR, Shahid M, Rosenmund C (2001) Mechanism and impact of allosteric AMPA receptor modulation by the ampakine CX546. Neuropharmacology 41:650-663.
35. Navaza J (1994) AMoRe: an automated package for molecular replacement. Acta Crystallogr A 50:157-163.
36. O'Neill MJ, Bleakman D, Zimmerman DM, Nisenbaum ES (2004) AMPA receptor potentiators for the treatment of CNS disorders. Curr Drug Targets 3:181-194.
37. Partin KM, Fleck MW, Mayer ML (1996) AMPA receptor flip/flop mutants affecting deactivation, desensitization, and modulation by cyclothiazide, aniracetam, and thiocyanate. J Neurosci 16:6634-6647.
38. Quirk JC, Nisenbaum ES (2003) Multiple molecular determinants for allosteric modulation of alternatively spliced AMPA receptors. J Neurosci 23:10953-10962.
39. Rammsayer TH (2001) Effects of pharmacologically induced changes in NMDA-receptor activity on long-term memory in humans. Learn Mem 8:20-25.
40. Robert A, Armstrong N, Gouaux E, Howe JR (2005) AMPA receptor binding cleft mutations that alter affinity, efficacy, and recovery from desensitization. J Neurosci 25:3752-3762.
41. Sun Y, Olson RA, Horning M, Armstrong N, Mayer ML, Gouaux E (2002) Mechanism of glutamate receptor desensitization. Nature 417:245-253.
42. Tang CM, Shi QY, Katchman A, Lynch G (1991) Modulation of the time course of fast EPSCs and glutamate channel kinetics by aniracetam. Science 254:288-290.
43. Tsien JZ, Huerta PT, Tonegawa S (1996) The essential role of hippocampal CA1 NMDA receptor-dependent synaptic plasticity in spatial memory. Cell 87:1327-1338.
44. van Aalten DM, Bywater R, Findlay JB, Hendlich M, Hooft RW, Vriend G (1996) PRODRG, a program for generating molecular topologies and unique molecular descriptors from coordinates of small molecules. J Comput Aided Mol Des 10:255-262.
45. Vyklicky LJ, Patneau DK, Mayer ML (1991) Modulation of excitatory synaptic transmission by drugs that reduce desensitization at AMPA/kainate receptors. Neuron 7:971-984.