Modulation of agonist binding to AMPA receptors by 1-(1,4-benzodioxan-6- ylcarbonyl)piperidine (CX546): Differential effects across brain regions and GluA1-4/transmembrane AMPA receptor regulatory protein combinations

Journal of Pharmacology and Experimental Therapeutics

Volumn 331, Issue 3, 2009, Pages 965-974

  Montgomery, Kyle E ^a   Kessler, Markus ^a   Arai, Amy C ^a  

^a SOUTHERN ILLINOIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1,4 BENZODIOXAN 6 CARBOXYLIC ACID PIPERIDIDE; AMPA RECEPTOR; AMPA RECEPTOR AGONIST; AMPAKINE DERIVATIVE; TRITON X 100; UNCLASSIFIED DRUG; 1,3 DIOXOLANE DERIVATIVE; CX546 CPD; LIGAND; NOOTROPIC AGENT; PIPERIDINE DERIVATIVE; PROTEIN SUBUNIT;

ARTICLE; BRAIN REGION; COGNITION; CONTROLLED STUDY; DRUG BINDING; DRUG EFFECT; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; ANIMAL; BIOSYNTHESIS; BRAIN; CELL LINE; CELL MEMBRANE; DRUG POTENTIATION; GENETIC TRANSFECTION; HIPPOCAMPUS; METABOLISM; NEWBORN; PLASMID; PROTEIN BINDING; RADIOASSAY; RAT; SPRAGUE DAWLEY RAT; THALAMUS;

ANIMALS; ANIMALS, NEWBORN; BRAIN; CELL LINE; CELL MEMBRANE; DIOXOLES; HIPPOCAMPUS; HUMANS; LIGANDS; NOOTROPIC AGENTS; PIPERIDINES; PLASMIDS; PROTEIN BINDING; PROTEIN SUBUNITS; RADIOLIGAND ASSAY; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, AMPA; THALAMUS; TRANSFECTION;

EID: 73349095388     PISSN: 00223565     EISSN: 15210103     Source Type: Journal    
DOI: 10.1124/jpet.109.158014     Document Type: Article

References (49)

1. Ambros-Ingerson J and Lynch G (1993) Channel gating kinetics and synaptic efficacy: A hypothesis for the expression of long-term potentiation. Proc Natl Acad Sci U S A 90:7903-7907.
2. Arai AC and Kessler M (2007) Pharmacology of ampakine modulators: from AMPA receptors to synapses and behavior. Curr Drug Targets 8:583-602.
3. Arai A, Kessler M, Rogers G, and Lynch G (1996) Effects of a memory-enhancing drug on DL-α-amino-3-hydroxy-5-methyl-4- isoxazolepropionic acid receptor currents and synaptic transmission in hippocampus. J Pharmacol Exp Ther 278:627-638.
4. Arai AC, Kessler M, Rogers G, and 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.
5. Arai AC, Xia YF, Rogers G, Lynch G, and Kessler M (2002) Benzamide-type AMPA receptor modulators form two subfamilies with distinct modes of action. J Pharmacol Exp Ther 303:1075-1085.
6. Arai AC, Xia YF, and Suzuki E (2004) Modulation of AMPA receptor kinetics differentially influences synaptic plasticity in the hippocampus. Neuroscience 123: 1011-1024.
7. Beneyto M and 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.
8. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254.
9. Catania MV, Tölle TR, and Monyer H (1995) Differential expression of AMPA receptor subunits in NOS-positive neurons of cortex, striatum, and hippocampus. J Neurosci 15:7046-7061.
10. Cho CH, St-Gelais F, Zhang W, Tomita S, and Howe JR (2007) Two families of TARP isoforms that have distinct effects on the kinetic properties of AMPA receptors and synaptic currents. Neuron 55:890-904.
11. Condorelli DF, Dell'Albani P, Corsaro M, Barresi V, and Giuffrida Stella AM (1993) AMPA-selective glutamate receptor subunits in astroglial cultures. J Neurosci Res 36:344-356.
12. Fukaya M, Tsujita M, Yamazaki M, Kushiya E, Abe M, Akashi K, Natsume R, Kano M, Kamiya H, Watanabe M, et al. (2006) Abundant distribution of TARP gamma-8 in synaptic and extrasynaptic surface of hippocampal neurons and its major role in AMPA receptor expression on spines and dendrites. Eur J Neurosci 24:2177-2190.
13. Geiger JR, Melcher T, Koh DS, Sakmann B, Seeburg PH, Jonas P, and Monyer H (1995) Relative abundance of subunit mRNAs determines gating and Ca2+ permeability of AMPA receptors in principal neurons and interneurons in rat CNS. Neuron 15:193-204.
14. Hall RA, Kessler M, and Lynch G (1992) Evidence that high- and low-affinity DL-α-amino-3-hydroxy-5-methylisoxazole-4-propionic acid (AMPA) binding sites reflect membrane-dependent states of a single receptor. J Neurochem 59:1997-2004.
15. 3H]AMPA binding to rat brain membranes: evidence that AMPA receptor desensitization increases agonist affinity. Brain Res 628:345-348.
16. Hampson RE, Rogers G, Lynch G, and 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.
17. Jin R, Clark S, Weeks AM, Dudman JT, Gouaux E, and Partin KM (2005) Mechanism of positive allosteric modulators acting on AMPA receptors. J Neurosci 25:9027-9036.
18. Kato AS, Siuda ER, Nisenbaum ES, and Bredt DS (2008) AMPA receptor subunit-specific regulation by a distinct family of type II TARPs. Neuron 59:986-996.
19. Keinänen K, Wisden W, Sommer B, Werner P, Herb A, Verdoorn TA, Sakmann B, and Seeburg PH (1990) A family of AMPA-selective glutamate receptors. Science 249:556-560.
20. Kessler M, Arai A, Quan A, and Lynch G (1996) Effect of cyclothiazide on binding properties of AMPA-type glutamate receptors: lack of competition between cyclothiazide and GYKI 52466. Mol Pharmacol 49:123-131.
21. 3H]fluorowillardiine to study properties of AMPA receptor allosteric modulators. Brain Res 1076:25-41.
22. Kessler M, Suzuki E, Montgomery K, and Arai AC (2008) Physiological significance of high- and low-affinity agonist binding to neuronal and recombinant AMPA receptors. Neurochem Int 52:1383-1393.
23. Klugbauer N, Dai S, Specht V, Lacinová L, Marais E, Bohn G, and Hofmann F (2000) A family of gamma-like calcium channel subunits. FEBS Lett 470:189-197.
24. Kott S, Werner M, Körber C, and Hollmann M (2007) Electrophysiological properties of AMPA receptors are differentially modulated depending on the associated member of the TARP family. J Neurosci 27:3780-3789.
25. Leranth C, Szeidemann Z, Hsu M, and Buzsáki G (1996) AMPA receptors in the rat and primate hippocampus: a possible absence of GluR2/3 subunits in most inter-neurons. Neuroscience 70:631-652.
26. Lilliu V, Pernas-Alonso R, Trelles RD, di Porzio U, Zuddas A, and Perrone-Capano C (2001) Ontogeny of AMPA receptor gene expression in the developing rat midbrain and striatum. Brain Res Mol Brain Res 96:133-141.
27. Lu W, Shi Y, Jackson AC, Bjorgan K, During MJ, Sprengel R, Seeburg PH, and Nicoll RA (2009) Subunit composition of synaptic AMPA receptors revealed by a single-cell genetic approach. Neuron 62:254-268.
28. Lynch G, Granger R, Ambros-Ingerson J, Davis CM, Kessler M, and Schehr R (1997) Evidence that a positive modulator of AMPA-type glutamate receptors improves delayed recall in aged humans. Exp Neurol 145:89-92.
29. Lynch G (2006) Glutamate-based therapeutic approaches: ampakines. Curr Opin Pharmacol 6:82-88.
30. Milstein AD, Zhou W, Karimzadegan S, Bredt DS, and Nicoll RA (2007) TARP subtypes differentially and dose-dependently control synaptic AMPA receptor gating. Neuron 55:905-918.
31. Moss FJ, Dolphin AC, and Clare JJ (2003) Human neuronal stargazin-like proteins, gamma2, gamma3 and gamma4; an investigation of their specific localization in human brain and their influence on CaV2.1 voltage-dependent calcium channels expressed in Xenopus oocytes. BMC Neurosci 4:23.
32. Nagarajan N, Quast C, Boxall AR, Shahid M, and Rosenmund C (2001) Mechanism and impact of allosteric AMPA receptor modulation by the ampakine CX546. Neuropharmacology 41:650-663.
33. Nicoll RA, Tomita S, and Bredt DS (2006) Auxiliary subunits assist AMPA-type glutamate receptors. Science 311:1253-1256.
34. Partin KM, Patneau DK, and Mayer ML (1994) Cyclothiazide differentially modulates desensitization of α-amino-3-hydroxy-5-methyl-4- isoxazolepropionic acid receptor splice variants. Mol Pharmacol 46:129-138.
35. Petralia RS and Wenthold RJ (1992) Light and electron immunocytochemical localization of AMPA-selective glutamate receptors in the rat brain. J Comp Neurol 318:329-354.
36. Robert A and Howe JR (2003) How AMPA receptor desensitization depends on receptor occupancy. J Neurosci 23:847-858.
37. Sekiguchi M, Nishikawa K, Aoki S, and Wada K (2002) A desensitization-selective potentiator of AMPA-type glutamate receptors. Br J Pharmacol 136:1033-1041.
38. Sommer B, Keinänen K, Verdoorn TA, Wisden W, Burnashev N, Herb A, Köhler M, Takagi T, Sakmann B, and Seeburg PH (1990) Flip and flop: a cell-specific functional switch in glutamate-operated channels of the CNS. Science 249:1580-1585.
39. Staubli U, Rogers G, and Lynch G (1994) Facilitation of glutamate receptors enhances memory. Proc Natl Acad Sci U S A 91:777-781.
40. Sun Y, Olson R, Horning M, Armstrong N, Mayer M, and Gouaux E (2002) Mechanism of glutamate receptor desensitization. Nature 417:245-253.
41. Suzuki E, Kessler M, and Arai AC (2008) The fast kinetics of AMPA GluR3 receptors is selectively modulated by the TARPs gamma 4 and gamma 8. Mol Cell Neurosci 38:117-123.
42. Schwenk J, Harmel N, Zolles G, Bildl W, Kulik A, Heimrich B, Chisaka O, Jonas P, Schulte U, Fakler B, et al. (2009) Functional proteomics identify cornichon proteins as auxiliary subunits of AMPA receptors. Science 323:1313-1319.
43. Tomita S, Chen L, Kawasaki Y, Petralia RS, Wenthold RJ, Nicoll RA, and Bredt DS (2003) Functional studies and distribution define a family of transmembrane AMPA receptor regulatory proteins. J Cell Biol 161:805-816.
44. Tomita S, Adesnik H, Sekiguchi M, Zhang W, Wada K, Howe JR, Nicoll RA, and Bredt DS (2005) Stargazin modulates AMPA receptor gating and trafficking by distinct domains. Nature 435:1052-1058.
45. Tomita S, Sekiguchi M, Wada K, Nicoll RA, and Bredt DS (2006) Stargazin controls the pharmacology of AMPA receptor potentiators. Proc Natl Acad Sci U S A 103:10064-10067.
46. Wang YV, Wade M, Wong E, Li YC, Rodewald LW, and Wahl GM (2007) Quantitative analyses reveal the importance of regulated Hdmx degradation for p53 activation. Proc Natl Acad Sci U S A 104:12365-12370.
47. Xia YF, Kessler M, and Arai AC (2005) Positive α-amino-3-hydroxy-5- methyl-4-isoxazolepropionic acid (AMPA) receptor modulators have different impact on synaptic transmission in the thalamus and hippocampus. J Pharmacol Exp Ther 313:277-285.
48. Xia YF and Arai AC (2005) AMPA receptor modulators have different impact on hippocampal pyramidal cells and interneurons. Neuroscience 135:555-567.
49. Zhang W, Robert A, Vogensen SB, and Howe JR (2006) The relationship between agonist potency and AMPA receptor kinetics. Biophys J 91:1336-1346.