Functional insight into development of positive allosteric modulators of AMPA receptors

Neuropharmacology

Volumn 85, Issue , 2014, Pages 57-66

  Weeks, Autumn M ^a   Harms, Jonathan E ^a   Partin, Kathryn M ^a   Benveniste, Morris ^b  

^a Department of Environmental and Radiological Health Sciences   (United States)

^b MOREHOUSE SCHOOL OF MEDICINE   (United States)

Author keywords

Allosteric modulation; AMPAkine; Deactivation; Desensitization; Electrophysiology; Ion channel gating; Mutagenesis; Neuropharmacology

Indexed keywords

AMPA RECEPTOR; AMPA RECEPTOR AGONIST; BISALKYLSULFONAMIDE; BISCARBOXYTHIOPHENE; CX 614; CYCLOTHIAZIDE; UNCLASSIFIED DRUG; 2H,3H,6AH-PYRROLIDINO(2'',1''-3',2')1,3-OXAZINO(6',5'-5,4)BENZO(E)1, 4-DIOXAN-10-ONE; AMINO ACID RECEPTOR AFFECTING AGENT; BENZOTHIADIAZINE DERIVATIVE; OXAZINE DERIVATIVE;

ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; DRUG EFFICACY; DRUG RECEPTOR BINDING; EMBRYO; HUMAN; HUMAN CELL; PRIORITY JOURNAL; VOLTAGE CLAMP TECHNIQUE; BINDING SITE; CHEMICAL STRUCTURE; CHEMISTRY; COMPARATIVE STUDY; COMPUTER SIMULATION; DRUG DEVELOPMENT; DRUG EFFECTS; GENETIC TRANSFECTION; GENETICS; HEK293 CELL LINE; KINETICS; MEMBRANE POTENTIAL; METABOLISM; MUTATION; PATCH CLAMP TECHNIQUE; PHYSIOLOGY;

BENZOTHIADIAZINES; BINDING SITES; COMPUTER SIMULATION; DRUG DISCOVERY; EXCITATORY AMINO ACID AGENTS; HEK293 CELLS; HUMANS; KINETICS; MEMBRANE POTENTIALS; MODELS, MOLECULAR; MUTATION; OXAZINES; PATCH-CLAMP TECHNIQUES; RECEPTORS, AMPA; TRANSFECTION;

EID: 84902162292     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2014.05.022     Document Type: Article

References (41)

1. A.H. Ahmed, C.P. Ptak, and R.E. Oswald Molecular mechanism of flop selectivity and subsite recognition for an AMPA receptor allosteric modulator: structures of GluA2 and GluA3 in complexes with PEPA Biochemistry 49 2010 2843 2850
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. V. Anggano, and R.L. Huganir Regulation of AMPA receptor trafficking and synaptic plasticity Curr. Opin. Neurobiol. 22 2012 461 469
4. A. Arai, M. Kessler, G. Rogers, and G. Lynch Effects of the potent ampakine CX614 on hippocampal and recombinant AMPA receptors: interactions with cyclothiazide and GYKI 52466 Mol. Pharmacol. 58 2000 802 813
5. A.C. Arai, and M. Kessler Pharmacology of ampakine modulators: from AMPA receptors to synapses and behavior Curr. Drug Targets 8 2007 583 602 (Pubitemid 46785059)
6. M. Benveniste, J. Clements, L. Vyklicky, and M.L. Mayer A kinetic analysis of the modulation of N-methyl-D-aspartic acid receptors by glycine in mouse cultured hippocampal neurones J. Physiol. Lond. 428 1990 333 357 (Pubitemid 20313660)
7. M.D. Black Therapeutic potential of positive AMPA modulators and their relationship to AMPA receptor subunits. A review of preclinical data Psychopharmacol. Berl. 179 2005 154 163 (Pubitemid 40584805)
8. J. Boulter, B. Bettler, R. Dingledine, J. Edgebjerg, M. Hartley, I. Hermans-Borgmeyer, M. Hollmann, R.I. Hume, S. Rogers, and S. Heinemann Molecular biology of the glutamate receptors Clin. Neuropharmacol. 15 Suppl. 1, Pt A 1992 60A 61A
9. G.L. Collingridge, R. Olsen, J.A. Peters, and M. Spedding Ligand gated ion channels Neuropharmacology 56 2009 1
10. M.C. Fernandez, A. Castano, E. Dominguez, A. Escribano, D. Jiang, A. Jimenez, E. Hong, W.J. Hornback, E.S. Nisenbaum, and N. Rankl et al. A novel class of AMPA receptor allosteric modulators. Part 1: design, synthesis, and SAR of 3-aryl-4-cyano-5-substituted-heteroaryl-2-carboxylic acid derivatives Bioorg. Med. Chem. Lett. 16 2006 5057 5061 (Pubitemid 44247703)
11. 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
12. J.E. Harms, M. Benveniste, J.K. Maclean, K.M. Partin, and C. Jamieson Functional analysis of a novel positive allosteric modulator of AMPA receptors derived from a structure-based drug design strategy Neuropharmacology 64 2013 45 52
13. R.I. Hume, R. Dingledine, and S.F. Heinemann Identification of a site in glutamate receptor subunits that controls calcium permeability Science 253 1991 1028 1031 (Pubitemid 21917250)
14. C. Jamieson, J.K. Maclean, C.I. Brown, R.A. Campbell, K.J. Gillen, J. Gillespie, B. Kazemier, M. Kiczun, Y. Lamont, and A.J. Lyons et al. Structure based evolution of a novel series of positive modulators of the AMPA receptor Bioorg. Med. Chem. Lett. 21 2 2011 Jan 15 805 811
15. R. Jin, S. Clark, A.M. Weeks, J.T. Judman, E. Gouaux, and K.M. Partin Mechanism of positive allosteric modulators acting on AMPA receptors J. Neurosci. 25 2005 9027 9036 (Pubitemid 41384472)
16. M. Kessler, G. Rogers, and A. Arai The norbornenyl moiety of cyclothiazide determines the preference for flip-flop variants of AMPA receptor subunits Neurosci. Lett. 287 2000 161 165 (Pubitemid 30353071)
17. M. Koike, S. Tsukada, K. Tsuzuki, H. Kijima, and S. Ozawa Regulation of kinetic properties of GluR2 AMPA receptor channels by alternative splicing J. Neurosci. 20 2000 2166 2174 (Pubitemid 30230069)
18. C. Krintel, K. Frydenvang, L. Olsen, M.T. Kristensen, O. de Barrios, P. Naur, P. Francotte, B. Pirotte, M. Gajhede, and J.S. Kastrup Thermodynamics and structural analysis of positive allosteric modulation of the ionotropic glutamate receptor GluA2 Biochem. J. 441 2012 173 178
19. C. Krintel, K. Harpsoe, L.G. Zachariassen, D. Peters, K. Frydenvang, D.S. Pickering, M. Gajhede, and J.S. Kastrup Structural analysis of the positive AMPA receptor modulators CX516 and Me-CX516 in complex with the GluA2 ligand-binding domain Acta Crystallogr. D Biol. Crystallogr. 69 2013 1645 1652
20. G. Lynch, L.C. Palmer, and C.M. Gall The likelihood of cognitive enhancement Pharmacol. Biochem. Behav. 99 2011 116 129
21. R.C. Malenka Synaptic plasticity and AMPA receptor trafficking Ann. N. Y. Acad. Sci. 1003 2003 1 11 (Pubitemid 38083041)
22. R. Malinow, Z.F. Mainen, and Y. Hayashi LTP mechanisms: from silence to four-lane traffic Curr. Opin. Neurobiol. 10 2000 352 357 (Pubitemid 30389302)
23. M. Mansour, N. Nagarajan, R.B. Nehring, J. Clements, and C. Rosenmund Heteromeric AMPA receptors assemble with a preferred subunit stoichiometry and spatial arrangement Neuron 32 2001 841 853 (Pubitemid 34024845)
24. F.S. Menniti, C.W. Lindsley, P.J. Conn, J. Pandit, P. Zagouras, and R.A. Volkmann Allosteric modulators for the treatment of schizophrenia: targeting glutamatergic networks Curr. Top. Med. Chem. 13 2013 26 54
25. N.A. Mitchell, and M.W. Fleck Targeting AMPA receptor gating processes with allosteric modulators and mutations Biophys. J. 92 2007 2392 2402 (Pubitemid 46536421)
26. J.A. Morrow, J.K. Maclean, and C. Jamieson Recent advances in positive allosteric modulators of the AMPA receptor Curr. Opin. Drug Discov. Dev. 9 2006 571 579 (Pubitemid 44378825)
27. A.M. Moudy, K.A. Yamada, and S.M. Rothman Rapid desensitization determines the pharmacology of glutamate neurotoxicity Neuropharmacology 33 1994 953 962 (Pubitemid 24290522)
28. R. Mueller, S. Rachwal, S. Lee, S. Zhong, Y.X. Li, P. Haroldsen, T. Herbst, S. Tanimura, M. Varney, and S. Johnson et al. Benzotriazinone and benzopyrimidinone derivatives as potent positive allosteric AMPA receptor modulators Bioorg. Med. Chem. Lett. 21 2011 6170 6175
29. K.M. Partin, M.F. Fleck, and M.L. Mayer AMPA receptor flip/flop mutants affecting deactivation, desensitization and modulation by cyclothiazide, aniracetam and thiocyanate J. Neurosci. 16 1996 6634 6647 (Pubitemid 26359347)
30. C.P. Ptak, A.H. Ahmed, and R.E. Oswald Probing the allosteric modulator binding site of GluR2 with thiazide derivatives Biochemistry 48 2009 8594 8602
31. J.C. Quirk, and E.S. Nisenbaum LY404187: a novel positive allosteric modulator of AMPA receptors CNS Drug Rev. 8 2002 255 282 (Pubitemid 35191286)
32. C. Rosenmund, Y. Stern-Bach, and C.F. Stevens The tetrameric structure of a glutamate receptor channel Science 280 1998 1596 1599 (Pubitemid 28277703)
33. J. Schwenk, N. Harmel, A. Brechet, G. Zolles, H. Berkefeld, C.S. Muller, W. Bildl, D. Baehrens, B. Huber, and A. Kulik et al. High-resolution proteomics unravel architecture and molecular diversity of native AMPA receptor complexes Neuron 74 2012 621 633
34. B. Sommer, K. Keinänen, T.A. Verdoorn, W. Wisden, N. Burnashev, A. Herb, M. Köhler, T. Takagi, B. Sakmann, and P.H. Seeburg Flip and flop: a cell-specific functional switch in glutamate-operated channels of the CNS Science 249 1990 1580 1585
35. U. Staubli, Y. Perez, F.B. Xu, G. Rogers, M. Ingvar, S. Stone-Elander, and G. Lynch Centrally active modulators of glutamate receptors facilitate the induction of long-term potentiation in vivo Proc. Natl. Acad. Sci. U. S. A. 91 1994 11158 11162 (Pubitemid 24349645)
36. U. Staubli, G. Rogers, and G. Lynch Facilitation of glutamate receptors enhances memory Proc. Natl. Acad. Sci. U. S. A. 91 1994 777 781 (Pubitemid 24041485)
37. Y. Sun, R. Olson, M. Horning, N. Armstrong, M.L. Mayer, and E. Gouaux Mechanism of glutamate receptor desensitization Nature 417 2002 245 253 (Pubitemid 34534700)
38. D.E. Timm, M. Benveniste, A.M. Weeks, E.S. Nisenbaum, and K.M. Partin Structural and functional analysis of two new positive allosteric modulators of GluA2 desensitization and deactivation Mol. Pharmacol. 80 2011 267 280
39. 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
40. T.A. Verdoorn, N. Burnashev, H. Monyer, P.H. Seeburg, and B. Sakmann Structural determinants of ion flow through recombinant glutamate receptor channels Science 252 1991 1715 1718 (Pubitemid 21917095)
41. S.E. Ward, B.D. Bax, and M. Harries Challenges for and current status of research into positive modulators of AMPA receptors Br. J. Pharmacol. 160 2010 181 190