Not all desensitizations are created equal: Physiological evidence that AMPA receptor desensitization differs for kainate and glutamate

Journal of Neuroscience

Volumn 31, Issue 25, 2011, Pages 9359-9367

  Levchenko Lambert, Yanina ^a   Turetsky, Dorothy M ^a   Patneau, Doris K ^a  

^a OKLAHOMA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPA RECEPTOR; GLUTAMIC ACID; KAINIC ACID;

ARTICLE; CONTROLLED STUDY; EMBRYO; GENE MUTATION; HUMAN; HUMAN CELL; MOLECULAR STABILITY; MUTANT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; RECEPTOR DOWN REGULATION; WILD TYPE;

GLUTAMIC ACID; HEK293 CELLS; HUMANS; KAINIC ACID; RECEPTORS, AMPA; SIGNAL TRANSDUCTION;

EID: 79959628263     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.6761-10.2011     Document Type: Article

References (32)

1. 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.
2. Armstrong N, Sun Y, Chen GQ, Gouaux E (1998) Structure of a glutamatereceptor ligand-binding core in complex with kainate. Nature 395:913-917.
3. Armstrong N, Mayer M, Gouaux E (2003) Tuning activation of the AMPAsensitive GluR2 ion channel by genetic adjustment of agonist-induced conformational changes. Proc Natl Acad Sci USA 100:5736-5741.
4. Balannik V, Menniti FS, Paternain AV, Lerma J, Stern-Bach Y (2005) Molecular mechanism of AMPA receptor noncompetitive antagonism. Neuron 48:279-288.
5. Birdsey-Benson A, Gill A, Henderson LP, Madden DR (2010) Enhanced efficacy without further cleft closure: re-evaluating twist as a source of agonist efficacy in AMPA receptors. J Neurosci 30:1463-1470.
6. Bjerrum EJ, Biggin PC (2008) Rigid body essential x-ray crystallography: distinguishing the bend and twist of glutamate receptor ligand binding domains. Proteins 72:434-446.
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. Fenwick MK, Oswald RE (2010) On the mechanisms of alpha-amino-3-hydroxy-5-methylisoxazole-4-propionic acid (AMPA) receptor binding to glutamate and kainate. J Biol Chem 285:12334-12343.
9. Gonzalez J, Du M, Parameshwaran K, Suppiramaniam V, Jayaraman V (2010) Role of dimer interface in activation and desensitization inAMPA receptors. Proc Natl Acad Sci USA 107:9891-9896.
10. Hollmann M, O'Shea-Greenfield A, Rogers SW, Heinemann S (1989) Cloning by functional expression of a member of the glutamate receptor family. Nature 342:643-648.
11. Holm MM, Naur P, Vestergaard B, Geballe MT, Gajhede M, Kastrup JS, Traynelis SF, Egebjerg J (2005) A binding site tyrosine shapes desensitization kinetics and agonist potency at GluR2. A mutagenic, kinetic, and crystallographic study. J Biol Chem 280:35469-35476.
12. Horning MS, Mayer ML (2004) Regulation of AMPA receptor gating by ligand binding core dimers. Neuron 41:379-388.
13. Jin R, Banke TG, Mayer ML, Traynelis SF, Gouaux E (2003) Structural basis for partial agonist action at ionotropic glutamate receptors. Nat Neurosci 6:803-810.
14. 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.
15. Madden DR, Cheng Q, Thiran S, Rajan S, Rigo F, Keinänen K, Reinelt S, Zimmermann H, Jayaraman V (2004) Stereochemistry of glutamate receptor agonist efficacy: engineering a dual-specificity AMPA/kainate receptor. Biochemistry 43:15838-15844.
16. Maltsev AS, Oswald RE (2010) Hydrophobic side chain dynamics of a glutamate receptor ligand binding domain. J Biol Chem 285:10154-10162.
17. Mano I, Lamed Y, Teichberg VI (1996) A venus flytrap mechanism for activation and desensitization of alpha-amino-3-hydroxy-5-methyl-4-isoxazole propionic acid receptors. J Biol Chem 271:15299-15302.
18. Mosbacher J, Schoepfer R, Monyer H, Burnashev N, Seeburg PH, Ruppersberg JP (1994) A molecular determinant for submillisecond desensitization in glutamate receptors. Science 266:1059-1062.
19. Nayeem N, Mayans O, Green T (2011) Conformational flexibility of the ligand-binding domain dimer in kainate receptor gating and desensitization. J Neurosci 31:2916-2924.
20. Partin KM, Patneau DK, Winters CA, Mayer ML, Buonanno A (1993) Selective modulation of desensitization at AMPA versus kainate receptors by cyclothiazide and concanavalin A. Neuron 11:1069-1082.
21. Partin KM, Patneau DK, Mayer ML (1994) Cyclothiazide differentially modulates desensitization of alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor splice variants. Mol Pharmacol 46:129-138.
22. Patneau DK, Vyklicky L Jr, Mayer ML (1993) Hippocampal neurons exhibit cyclothiazide-sensitive rapidly desensitizing responses to kainate. J Neurosci 13:3496-3509.
23. Plested AJ, Mayer ML (2009) AMPA receptor ligand binding domain mobility revealed by functional cross linking. J Neurosci 29:11912-11923.
24. Priel A, Kolleker A, Ayalon G, Gillor M, Osten P, Stern-Bach Y (2005) Stargazin reduces desensitization and slows deactivation of the AMPA-type glutamate receptors. J Neurosci 25:2682-2686.
25. Raman IM, Trussell LO (1992) The kinetics of the response to glutamate and kainate in neurons of the avian cochlear nucleus. Neuron 9:173-186.
26. Rosenmund C, Stern-Bach Y, Stevens CF (1998) The tetrameric structure of a glutamate receptor channel. Science 280:1596-1599.
27. Sommer B, Köhler M, Sprengel R, Seeburg PH (1991) RNA editing in brain controls a determinant of ion flow in glutamate-gated channels. Cell 67:11-19.
28. 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.
29. Stern-Bach Y, Russo S, Neuman M, Rosenmund C (1998) A point mutation in the glutamate binding site blocks desensitization of AMPA receptors. Neuron 21:907-918.
30. Sun Y, Olson R, Horning M, Armstrong N, Mayer M, Gouaux E (2002) Mechanism of glutamate receptor desensitization. Nature 417:245-253.
31. Tomita S, Adesnik H, Sekiguchi M, Zhang W, Wada K, Howe JR, Nicoll RA, Bredt DS (2005) Stargazin modulates AMPA receptor gating and trafficking by distinct domains. Nature 435:1052-1058.
32. Turetsky D, Garringer E, Patneau DK (2005) Stargazin modulates native AMPAreceptor functional properties by two distinct mechanisms. J Neurosci 25:7438-7448.