Challenges for and current status of research into positive modulators of AMPA receptors

British Journal of Pharmacology

Volumn 160, Issue 2, 2010, Pages 181-190

  Ward, Simon E ^a   Bax, Benjamin D ^a   Harries, Mark ^a  

^a GLAXOSMITHKLINE   (United Kingdom)

Author keywords

AMPA; Electrophysiology; Ion channel; Positive modulator; X ray crystallography

Indexed keywords

2,3 DIHYDRO 3,4 CYCLOPENTANO 1,2,4 BENZOTHIADIAZINE 1,1 DIOXIDE; 6 QUINOXALINECARBOXYLIC ACID PIPERIDIDE; AMPA RECEPTOR; AMPA RECEPTOR AGONIST; ANIRACETAM; CX 1739; CX 701; CX 717; CYCLOTHIAZIDE; FARAMPATOR; IONOTROPIC RECEPTOR AGONIST; LY 450108; N [2 [4' (2 METHYLSULFONAMIDOETHYL)BIPHENYL 4 YL]PROPYL] 2 PROPANESULFONAMIDE; NEUROLEPTIC AGENT; ORG 26576; SCH 900460; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; ATTENTION DEFICIT DISORDER; CLINICAL TRIAL; DEPRESSION; DRUG PROTEIN BINDING; DRUG RESEARCH; DRUG SCREENING; DRUG STRUCTURE; HUMAN; LEARNING DISORDER; MAJOR DEPRESSION; MEMORY DISORDER; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; RESPIRATION DEPRESSION; REVIEW; SCHIZOPHRENIA; SLEEP APNEA SYNDROME; STRUCTURE ACTIVITY RELATION; X RAY CRYSTALLOGRAPHY;

ALLOSTERIC REGULATION; ANIMALS; CRYSTALLOGRAPHY, X-RAY; DRUG DELIVERY SYSTEMS; DRUG DESIGN; HIGH-THROUGHPUT SCREENING ASSAYS; HUMANS; PROTEIN SUBUNITS; RECEPTORS, AMPA; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 77951694715     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/j.1476-5381.2010.00726.x     Document Type: Review

References (67)

1. Alexander SPH, Mathie A, Peters JA (2009). Guide to Receptors and Channels (GRAC), 4th edn. Br J Pharmacol 158 (Suppl. 1 S1 S254. (Pubitemid 351415518)
2. Arai A, Kessler M, Ambros-Ingerson J, Quan A, Yigiter E, Rogers G et al 1996). Effect of a centrally active benzoylpyrrolidine drug on AMPA receptor kinetics. Neuroscience 75 : 573 585. (Pubitemid 26361346)
3. Arai AC, Xia Y-F, Suzuki E (2004). Modulation of AMPA receptor kinetics differentially influences synaptic plasticity in the hippocampus. Neuroscience 123 : 1011 1024. (Pubitemid 38130109)
4. Barry MF, Ziff EB (2002). Receptor trafficking and the plasticity of excitatory synapses. Curr Opin Neurobiol 12 : 279 286. (Pubitemid 34615753)
5. Beneyto M, Meador-Woodruff JH (2004). Expression of transcripts encoding AMPA receptor subunits and associated postsynaptic proteins in the macaque brain. J Comp Neurol 468 : 530 554. (Pubitemid 38036694)
6. Bennett JA, Dingledine R (1995). Topology profile for a glutamate receptor: three transmembrane domains and a channel-lining re-entrant membrane loop. Neuron 14 : 373 384.
7. Bloss EB, Hunter RG, Waters EM, Munoz C, Bernard K, McEwen BS (2008). Behavioural and biological effects of chronic S18986, a positive AMPA receptor modulator, during aging. Exp Neurol 210 : 109 117. (Pubitemid 351258071)
8. Bradley DM, Chan WN, Harrison SA, Thewlis KM, Ward SE (2008). Compounds which potentiate AMPA receptor and uses thereof in medicine. International patent application WO 2008/110566.
9. Bramham C, Messaoudi E (2005). BDNF function in adult synaptic plasticity: the synaptic consolidation hypothesis. Prog Neurobiol 76 : 99 125. (Pubitemid 41242884)
10. Buccafusco JJ, Weiser T, Winter K, Klinder K, Terry AV (2004). The effects of IDRA 21, a positive modulator of the AMPA receptor, on delayed matching performance by young and aged rhesus monkeys. Neuropharmacology 46 : 10 22. (Pubitemid 37494735)
11. Chappell AS, Gonzales C, Williams J, Witte MM, Mohs RC, Sperling R (2007). AMPA potentiator treatment of cognitive deficits in Alzheimer's disease. Neurology 68 : 1008 1012. (Pubitemid 46569134)
12. Chen GQ, Sun Y, Rongsheng J, Gouaux E (1998). Probing the ligand binding domain of the GluR2 receptor by proteolysis and deletion mutagenesis defines domain boundaries and yields a crystallisable construct. Protein Sci 7 : 2623 2630. (Pubitemid 28565704)
13. Clayton A, Siebold C, Gilbert RJC, Sutton GC, Harlos K, McIlhinney RAJ et al 2009). Crystal structure of the GluR2 amino-terminal domain provides insights into the architecture and assembly of ionotropic glutamate receptors. J Mol Biol 392 : 1125 1132.
14. Collingridge GL, Isaac JT, Wang YT (2004). Receptor trafficking and synaptic plasticity. Nature Rev Neurosci 5 : 952 962.
15. Collingridge GL, Olsen RW, Peters J, Spedding M (2009). A nomenclature for ligand-gated ion channels. Neuropharmacol 56 : 2 5.
16. Congreve M, Murray CW, Blundell TL (2005). Structural biology and drug discovery. Drug Disc Today 10 : 895 907.
17. Cumin R, Bandle EF, Gamzu E, Haefely WE (1982). Effects of the novel compound Aniracetam (Ro 13-5057) upon impaired learning and memory in rodents. Psychopharmacology 78 : 104 111. (Pubitemid 13234084)
18. Derkach VA, Oh MC, Guire ES, Soderling TR (2007). Regulatory mechanisms of AMPA receptors in synaptic plasticity. Nat Rev Neurosci 8 : 101 113. (Pubitemid 46151040)
19. Dicou E, Rangon C-M, Guimiot F, Spedding M, Gressens P (2003). Positive allosteric modulators of AMPA receptors are neuroprotective against lesions induced by an NMDA agonist in neonatal mouse brain. Br Res 970 : 221 225. (Pubitemid 36423198)
20. Francotte P, de Tullio P, Fraikin P, Counerotte S, Goffin E, Pirotte B (2006). In search of novel AMPA potentiators. Recent Pat CNS Drug Discov 1 (3 239 246.
21. Goff DC, Leahy L, Berman I, Posever T, Herz L, Leon AC et al 2001). A placebo-controlled pilot study of the ampakine CX516 added to clozapine in schizophrenia. J Clin Psychopharm 21 : 484 487. (Pubitemid 32937430)
22. Goff DC, Lamberti JS, Leon AC, Green MF, Miller AL, Patel J et al 2007). A placebo-controlled add-on trial of the Ampakine, CX516, for cognitive deficits in schizophrenia. Neuropsychopharm 33 : 465 472.
23. Gouaux E, MacKinnon R (2005). Principles of selective ion transport in channels and pumps. Science 310 : 1461 1465. (Pubitemid 41746336)
24. Greger IH, Khatri L, Kong X, Ziff EB (2003). AMPA receptor tetramerization is mediated by Q/R editing. Neuron 40 : 763 774. (Pubitemid 37431036)
25. Greger IH, Ziff EB, Penn AC (2007). Molecular determinants of AMPA receptor subunit assembly. TINS 30 : 407 416. (Pubitemid 47088718)
26. Hampson RE, Rogers G, Lynch G, Deadwyler SA (1998). Facilitative effects of the ampakine CX516 on short-term memory in rats: enhancement of delayed-nonmatch-to-sample performance. J Neurosci 18 : 2740 2747. (Pubitemid 28141819)
27. Hollmann M, Heinemann S (1994). Cloned glutamate receptors. Ann Rev Neurosci 17 : 31 108. (Pubitemid 24117025)
28. Ingvar M, Ambros-Ingerson J, Davis M, Granger R, Kessler M, Rogers GA et al 1997). Enhancement by an ampakine of memory encoding in humans. Exp Neurol 146 : 553 559. (Pubitemid 27381863)
29. Javitt DC (2004). Glutamate as a therapeutic target in psychiatric disorders. Mol Psychiatr 9 : 984 979.
30. Jin R, Clark S, Weeks AM, Dudman JT, Gouaux E, Partin KM (2005). Mechanism of positive allosteric modulators acting on AMPA receptors. J Neurosci 25 : 9027 9036. (Pubitemid 41384472)
31. Jin R, Singh SK, Gu S, Furukawa H, Sobolevsky AI, Zhou J et al 2009). Crystal structure and association behaviour of the GluR2 amino-terminal domain. EMBO J 28 : 1812 1823.
32. Jones N, O'Neill MJ, Tricklebank M, Libri V, Williams SCR (2005). Examining the neural targets of the AMPA receptor potentiator LY404187 in the rat brain using pharmacological magnetic resonance imaging. Psychopharmacology 180 : 743 751. (Pubitemid 41317870)
33. Klein RM, Howe JR (2004). Effects of the lurcher mutation of GluR1 desensitization and activation kinetics. J Neurocsi 24 : 4941 4951.
34. Lebrun C, Piliere E, Lestage P (2000). Effects of S18986-1, a novel cognitive enhancer, on memory performance in an object recognition task in rats. Eur J Pharmacol 401 : 205 212. (Pubitemid 30488198)
35. 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 Pharm 64 : 5 10. (Pubitemid 36759812)
36. Legutko B, Li X, Skolnick P (2001). Regulation of BDNF expression in primary neuron culture by LY392098, a novel AMPA receptor potentiator. Neuropharmacology 40 : 1019 1027. (Pubitemid 32530608)
37. Lynch G (2002). Memory enhancement: the search for mechanism-based drugs. Nat Neurosci 5 : 1035 1038. (Pubitemid 35247193)
38. Lynch G, Granger R, Ambros-Ingerson J, Davis M, Kessler M, Schehr R (1997). Evidence that a positive modulator of AMPA-type glutamate receptors improves delayed recall in aged humans. Exp Neurol 145 : 89 92. (Pubitemid 27244283)
39. Mayer ML (2006). Glutamate receptors at atomic resolution. Nature 440 : 456 462.
40. Milstein AD, Zhou W, Karimzadegan S, Bredt DS, Nicoll RA (2008). Regulation of AMPA receptor gating and pharmacology by TARP auxiliary subunits. Trends Pharmacol Sci 29 : 333 339.
41. Morrow JA, Maclean JK, Jamieson C (2006). Recent advances in positive allosteric modulators of the AMPA receptor. Curr Opin Drug Discov Devel 9 (5 571 579. (Pubitemid 44378825)
42. Nicoll RA, Tomita S, Bredt DS (2006). Auxilliary subunits assist AMPA-type glutamate receptors. Science 311 : 1253 1256. (Pubitemid 43334707)
43. O'Neill MJ, Witkin JM (2007). AMPA receptor potentiators: application for depression and Parkinson's disease. Curr Drug Targets 8 : 603 620.
44. Ornstein PL, Zimmerman DM, Arnold BM, Bleisch TJ, Cantrell B, Simon R et al 2000). Biarylpropylsulfonamides as novel, potent potentiators of 2-amino-3-(5-methyl-3-hydroxyisoxazol-4-yl)-propanoic acid (AMPA) receptors. J Med Chem 43 : 4345 4358. (Pubitemid 32046858)
45. Ozawa S, Kamiya H, Tsuzuki K (1998). Glutamate receptors in the mammalian central nervous system. Prog Neurobiol 54 : 581 618. (Pubitemid 28123327)
46. Passafaro M, Piech V, Sheng M (2001). Subunit-specific temporal and spatial patterns of AMPA receptor exocytosis in hippocampal neurons. Nat Neurosci 4 : 917 926. (Pubitemid 32801595)
47. Petralia RS, Wenthold RJ (1992). Light and electron imunocytochemical localization of AMPA-selective glutamate receptors in the rat brain. J Comp Neurol 318 : 329 354.
48. Porrino LJ, Daunais JB, Rogers GA, Hampson RE, Deadwyler SA (2005). Facilitation of task performance and removal of the effects of sleep deprivation by an ampakine (CX717) in nonhuman primates. PLoS Biol 3 : e299.
49. Ptak CP, Ahmed AH, Oswald RE (2009). Probing the allosteric modulator binding site of GluR2 with thiazide derivatives. Biochemistry 48 : 8594 8602.
50. Quirk JC, Nisenbaum ES (2002). LY404187: a novel positive allosteric modulator of AMPA receptors. CNS Drug Rev 8 : 255 282.
51. Rogan MT, Staubli UV, LeDoux JE (1997). AMPA receptor facilitation accelerates fear learning without altering the level of conditioned fear acquired. J Neurosci 17 : 5928 5935.
52. Rosenbaum DM, Rasmussen SGF, Kobilka BK (2009). The structure and function of G-protein coupled receptors. Nature 459 : 356 363.
53. Seeburg PH, Higuchi M, Sprengel R (1998). RNA editing of brain glutamate receptor channels: mechanism and physiology. Brain Res Brain Res Rev 26 : 217 229. (Pubitemid 28318077)
54. Seeburg PH, Single F, Kuner T, Higuchi M, Sprengel R (2001). Genetic manipulation of key determinants of ion flow in glutamate receptor channels in the mouse. Brain Res 907 : 233 243. (Pubitemid 32595532)
55. Simmons DA, Rex CS, Palmer L, Pandyarajan V, Fedulov V, Gall CM et al 2009). Up-regulating BDNF with an ampakine rescues synaptic plasticity and memory in Huntington's disease knockin mice. Proc Natl Acad Sci U S A 106 : 4906 4911.
56. Sirvio J, Larson J, Quach CN, Rogers GA, Lynch G (1996). Effects of pharmacologically facilitating glutamatergic transmission in the trisynaptic intrahippocampal circuit. Neuroscience 74 : 1025 1035. (Pubitemid 26313346)
57. Sommer B, Kohler M, Sprengel R, Seeberg PH (1991). RNA editing in brain controls a determinant of ion flow in glutamate-gated channels. Cell 105 : 11 19. (Pubitemid 121001421)
58. Soto D, Coombs ID, Kelly L, Farrant M, Cull-Candy SG (2007). Stargazin attenuates intracellular polyamine block of calcium-permeable AMPA receptors. Nat Neurosci 10 : 1260 1267. (Pubitemid 47480295)
59. Staubli U, Rogers G, Lynch G (1994). Facilitation of glutamate receptors enhances memory. Proc Natl Acad Sci U S A 91 : 777 781. (Pubitemid 24041485)
60. Stern-Bach Y, Russo S, Neuman M, Rosenmund C (1998). A point mutation in the glutamate binding site blocks desensitisation of AMPA receptors. Neuron 21 : 907 918. (Pubitemid 28498797)
61. Sun Y, Olson R, Horning M, Armstrong N, Mayer M, Gouaux E (2002). Mechanism of glutamate receptor desensitization. Nature 417 : 245 253. (Pubitemid 34534700)
62. Thompson DM, Guidotti A, DiBella M, Costa E (1995). 7-chloro-3-methyl-3, 4-dihydro-2H-1,2,4-benzothiadiazine S,S-dioxide (IDRA 21), a congener of aniracetam, potently abates pharmacologically induced cognitive impairments in patas monkeys. Proc Natl Acad Sci U S A 92 : 7667 7771.
63. Tichelaar W, Safferling M, Keinanen K, Stark H, Madden DR (2004). The three-dimensional structure of an ionotropic glutamate receptor reveals a dimer-of-dimers assembly. J Mol Biol 344 : 435 442. (Pubitemid 39441215)
64. Tomita S, Adesnik H, Sekiguchi M, Zhang W, Howe JR, Nicoll RA et al 2005). Stargazin modulates AMPA receptor gating and trafficking by distinct domains. Nature 435 : 1052 1058. (Pubitemid 40910507)
65. Vandergriff J, Huff K, Bond A, Lodge D (2001). Potentiation of responses to AMPA on central neurones by LY392098 and LY404187 in vivo. Neuropharmacology 40 : 1003 1009. (Pubitemid 32530606)
66. Woolley ML, Waters KA, Gartlon JE, Lacroix LP, Jennings C, Shaugnessey F et al 2009). Evaluation of the pro-cognitive effects of the AMPA receptor positive modulator, 5-(1-piperidinylcarbonyl)-2,1,3-benzoxadiazole (CX691), in the rat. Psychopharmacology 202 : 343 354.
67. Zivkovic I, Thompson DM, Bertolino M, Uzunov D, DiBella M, Costa E et al 1995). 7-chloro-3-methyl-3,4-dihydro-2H-1,2,4-benzothiadiazine S,S-dioxide (IDRA 21): a benzothidiazine derivative that enhances cognition by attenuating DL-alpha-amino-2,3-dihydro-5-methyl-3-oxo-4-isoxazolepropanoic acid (AMPA) receptor desensitization. J Pharmacol Exp Ther 272 : 300 309.