Structure and Assembly Mechanism for Heteromeric Kainate Receptors

Neuron

Volumn 71, Issue 2, 2011, Pages 319-331

  Kumar, Janesh ^a   Schuck, Peter ^b   Mayer, Mark L ^a  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTAMATE RECEPTOR; GLUTAMATE RECEPTOR 6; KAINIC ACID RECEPTOR;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; BINDING AFFINITY; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN CROSS LINKING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; REGULATORY MECHANISM; SEDIMENTATION RATE; STRUCTURE ANALYSIS;

ALANINE; ALPHA-AMINO-3-HYDROXY-5-METHYL-4-ISOXAZOLEPROPIONIC ACID; ANIMALS; CELL LINE, TRANSFORMED; CHROMATOGRAPHY, GEL; CRYSTALLOGRAPHY; CRYSTALLOGRAPHY, X-RAY; EXCITATORY AMINO ACID AGONISTS; GLUTAMIC ACID; HUMANS; MEMBRANE POTENTIALS; MICE; MODELS, MOLECULAR; MUTAGENESIS; OOCYTES; PROTEIN STRUCTURE, TERTIARY; PYRIMIDINES; RECEPTORS, AMPA; RECEPTORS, KAINIC ACID; TRANSFECTION; XENOPUS;

EID: 79960652046     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2011.05.038     Document Type: Article

References (62)

1. Adams P.D., Afonine P.V., Bunkóczi G., Chen V.B., Davis I.W., Echols N., Headd J.J., Hung L.W., Kapral G.J., Grosse-Kunstleve R.W., et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 2010, 66:213-221.
2. Ayalon G., Stern-Bach Y. Functional assembly of AMPA and kainate receptors is mediated by several discrete protein-protein interactions. Neuron 2001, 31:103-113.
3. Ayalon G., Segev E., Elgavish S., Stern-Bach Y. Two regions in the N-terminal domain of ionotropic glutamate receptor 3 form the subunit oligomerization interfaces that control subtype-specific receptor assembly. J. Biol. Chem. 2005, 280:15053-15060.
4. Brose N., Huntley G.W., Stern-Bach Y., Sharma G., Morrison J.H., Heinemann S.F. Differential assembly of coexpressed glutamate receptor subunits in neurons of rat cerebral cortex. J. Biol. Chem. 1994, 269:16780-16784.
5. Brown P.H., Balbo A., Schuck P. Characterizing protein-protein interactions by sedimentation velocity analytical ultracentrifugation. Curr. Protoc. Immunol. 2008, Chapter 18, Unit 18.15.
6. Burnashev N., Monyer H., Seeburg P.H., Sakmann B. Divalent ion permeability of AMPA receptor channels is dominated by the edited form of a single subunit. Neuron 1992, 8:189-198.
7. Carter P.J., Winter G., Wilkinson A.J., Fersht A.R. The use of double mutants to detect structural changes in the active site of the tyrosyl-tRNA synthetase (Bacillus stearothermophilus). Cell 1984, 38:835-840.
8. Chen G.Q., Cui C., Mayer M.L., Gouaux E. Functional characterization of a potassium-selective prokaryotic glutamate receptor. Nature 1999, 402:817-821.
9. Clayton A., Siebold C., Gilbert R.J., Sutton G.C., Harlos K., McIlhinney R.A., Jones E.Y., Aricescu A.R. Crystal structure of the GluR2 amino-terminal domain provides insights into the architecture and assembly of ionotropic glutamate receptors. J. Mol. Biol. 2009, 392:1125-1132.
10. Dalva M.B., Takasu M.A., Lin M.Z., Shamah S.M., Hu L., Gale N.W., Greenberg M.E. EphB receptors interact with NMDA receptors and regulate excitatory synapse formation. Cell 2000, 103:945-956.
11. Das U., Kumar J., Mayer M.L., Plested A.J. Domain organization and function in GluK2 subtype kainate receptors. Proc. Natl. Acad. Sci. USA 2010, 107:8463-8468.
12. Egebjerg J., Bettler B., Hermans-Borgmeyer I., Heinemann S. Cloning of a cDNA for a glutamate receptor subunit activated by kainate but not AMPA. Nature 1991, 351:745-748.
13. Emsley P., Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 2004, 60:2126-2132.
14. Farina A.N., Blain K.Y., Maruo T., Kwiatkowski W., Choe S., Nakagawa T. Separation of domain contacts is required for heterotetrameric assembly of functional NMDA receptors. J. Neurosci. 2011, 31:3565-3579.
15. Furukawa H., Singh S.K., Mancusso R., Gouaux E. Subunit arrangement and function in NMDA receptors. Nature 2005, 438:185-192.
16. Geiger J.R.P., Melcher T., Koh D.S., Sakmann B., Seeburg P.H., Jonas P., Monyer H. Relative abundance of subunit mRNAs determines gating and Ca2+ permeability of AMPA receptors in principal neurons and interneurons in rat CNS. Neuron 1995, 15:193-204.
17. Gielen M., Siegler Retchless B., Mony L., Johnson J.W., Paoletti P. Mechanism of differential control of NMDA receptor activity by NR2 subunits. Nature 2009, 459:703-707.
18. Greger I.H., Esteban J.A. AMPA receptor biogenesis and trafficking. Curr. Opin. Neurobiol 2007, 17:289-297.
19. Herb A., Burnashev N., Werner P., Sakmann B., Wisden W., Seeburg P.H. The KA-2 subunit of excitatory amino acid receptors shows widespread expression in brain and forms ion channels with distantly related subunits. Neuron 1992, 8:775-785.
20. Hidalgo P., MacKinnon R. Revealing the architecture of a K+ channel pore through mutant cycles with a peptide inhibitor. Science 1995, 268:307-310.
21. Hollmann M., O'Shea-Greenfield A., Rogers S.W., Heinemann S. Cloning by functional expression of a member of the glutamate receptor family. Nature 1989, 342:643-648.
22. Horning M.S., Mayer M.L. Regulation of AMPA receptor gating by ligand binding core dimers. Neuron 2004, 41:379-388.
23. Jin R., Singh S.K., Gu S., Furukawa H., Sobolevsky A.I., Zhou J., Jin Y., Gouaux E. Crystal structure and association behaviour of the GluR2 amino-terminal domain. EMBO J. 2009, 28:1812-1823.
24. Karakas E., Simorowski N., Furukawa H. Structure of the zinc-bound amino-terminal domain of the NMDA receptor NR2B subunit. EMBO J. 2009, 28:3910-3920.
25. Keinänen K., Wisden W., Sommer B., Werner P., Herb A., Verdoorn T.A., Sakmann B., Seeburg P.H. A family of AMPA-selective glutamate receptors. Science 1990, 249:556-560.
26. Kumar J., Mayer M.L. Crystal structures of the glutamate receptor ion channel GluK3 and GluK5 amino-terminal domains. J. Mol. Biol. 2010, 404:680-696.
27. Kumar J., Schuck P., Jin R., Mayer M.L. The N-terminal domain of GluR6-subtype glutamate receptor ion channels. Nat. Struct. Mol. Biol. 2009, 16:631-638.
28. Leuschner W.D., Hoch W. Subtype-specific assembly of alpha-amino-3-hydroxy-5-methyl-4-isoxazole propionic acid receptor subunits is mediated by their n-terminal domains. J. Biol. Chem. 1999, 274:16907-16916.
29. Mah S.J., Cornell E., Mitchell N.A., Fleck M.W. Glutamate receptor trafficking: endoplasmic reticulum quality control involves ligand binding and receptor function. J. Neurosci. 2005, 25:2215-2225.
30. Matsuda K., Miura E., Miyazaki T., Kakegawa W., Emi K., Narumi S., Fukazawa Y., Ito-Ishida A., Kondo T., Shigemoto R., et al. Cbln1 is a ligand for an orphan glutamate receptor delta2, a bidirectional synapse organizer. Science 2010, 328:363-368.
31. McCoy A.J., Grosse-Kunstleve R.W., Adams P.D., Winn M.D., Storoni L.C., Read R.J. Phaser crystallographic software. J. Appl. Cryst. 2007, 40:658-674.
32. Monyer H., Sprengel R., Schoepfer R., Herb A., Higuchi M., Lomeli H., Burnashev N., Sakmann B., Seeburg P.H. Heteromeric NMDA receptors: molecular and functional distinction of subtypes. Science 1992, 256:1217-1221.
33. O'Brien R.J., Xu D., Petralia R.S., Steward O., Huganir R.L., Worley P. Synaptic clustering of AMPA receptors by the extracellular immediate-early gene product Narp. Neuron 1999, 23:309-323.
34. Otwinowski Z., Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 1997, 277:307-344.
35. Partin K.M., Patneau D.K., Winters C.A., Mayer M.L., Buonanno A. Selective modulation of desensitization at AMPA versus kainate receptors by cyclothiazide and concanavalin A. Neuron 1993, 11:1069-1082.
36. Pasternack A., Coleman S.K., Jouppila A., Mottershead D.G., Lindfors M., Pasternack M., Keinänen K. Alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptor channels lacking the N-terminal domain. J. Biol. Chem. 2002, 277:49662-49667.
37. Penn A.C., Williams S.R., Greger I.H. Gating motions underlie AMPA receptor secretion from the endoplasmic reticulum. EMBO J. 2008, 27:3056-3068.
38. Petralia R.S., Wang Y.X., Wenthold R.J. Histological and ultrastructural localization of the kainate receptor subunits, KA2 and GluR6/7, in the rat nervous system using selective antipeptide antibodies. J. Comp. Neurol. 1994, 349:85-110.
39. Plested A.J., Mayer M.L. Structure and mechanism of kainate receptor modulation by anions. Neuron 2007, 53:829-841.
40. Reeves P.J., Callewaert N., Contreras R., Khorana H.G. Structure and function in rhodopsin: high-level expression of rhodopsin with restricted and homogeneous N-glycosylation by a tetracycline-inducible N-acetylglucosaminyltransferase I-negative HEK293S stable mammalian cell line. Proc. Natl. Acad. Sci. USA 2002, 99:13419-13424.
41. Ren Z., Riley N.J., Garcia E.P., Sanders J.M., Swanson G.T., Marshall J. Multiple trafficking signals regulate kainate receptor KA2 subunit surface expression. J. Neurosci. 2003, 23:6608-6616.
42. Ripley B., Otto S., Tiglio K., Williams M.E., Ghosh A. Regulation of synaptic stability by AMPA receptor reverse signaling. Proc. Natl. Acad. Sci. USA 2011, 108:367-372.
43. Rossmann M., Sukumaran M., Penn A.C., Veprintsev D.B., Babu M.M., Greger I.H. Subunit-selective N-terminal domain associations organize the formation of AMPA receptor heteromers. EMBO J. 2011, 30:959-971.
44. Saglietti L., Dequidt C., Kamieniarz K., Rousset M.C., Valnegri P., Thoumine O., Beretta F., Fagni L., Choquet D., Sala C., et al. Extracellular interactions between GluR2 and N-cadherin in spine regulation. Neuron 2007, 54:461-477.
45. Schiffer H.H., Swanson G.T., Heinemann S.F. Rat GluR7 and a carboxy-terminal splice variant, GluR7b, are functional kainate receptor subunits with a low sensitivity to glutamate. Neuron 1997, 19:1141-1146.
46. Schröder G.F., Levitt M., Brunger A.T. Super-resolution biomolecular crystallography with low-resolution data. Nature 2010, 464:1218-1222.
47. Schuck P. Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and lamm equation modeling. Biophys. J. 2000, 78:1606-1619.
48. Schuck P. On the analysis of protein self-association by sedimentation velocity analytical ultracentrifugation. Anal. Biochem. 2003, 320:104-124.
49. Shanks N.F., Maruo T., Farina A.N., Ellisman M.H., Nakagawa T. Contribution of the global subunit structure and stargazin on the maturation of AMPA receptors. J. Neurosci. 2010, 30:2728-2740.
50. Shi Y., Suh Y.H., Milstein A.D., Isozaki K., Schmid S.M., Roche K.W., Nicoll R.A. Functional comparison of the effects of TARPs and cornichons on AMPA receptor trafficking and gating. Proc. Natl. Acad. Sci. USA 2010, 107:16315-16319.
51. Sia G.M., Béïque J.C., Rumbaugh G., Cho R., Worley P.F., Huganir R.L. Interaction of the N-terminal domain of the AMPA receptor GluR4 subunit with the neuronal pentraxin NP1 mediates GluR4 synaptic recruitment. Neuron 2007, 55:87-102.
52. Sobolevsky A.I., Rosconi M.P., Gouaux E. X-ray structure, symmetry and mechanism of an AMPA-subtype glutamate receptor. Nature 2009, 462:745-756.
53. Swanson G.T., Green T., Heinemann S.F. Kainate receptors exhibit differential sensitivities to (S)-5-iodowillardiine. Mol. Pharmacol. 1998, 53:942-949.
54. Takasu M.A., Dalva M.B., Zigmond R.E., Greenberg M.E. Modulation of NMDA receptor-dependent calcium influx and gene expression through EphB receptors. Science 2002, 295:491-495.
55. Traynelis S.F., Wollmuth L.P., McBain C.J., Menniti F.S., Vance K.M., Ogden K.K., Hansen K.B., Yuan H., Myers S.J., Dingledine R. Glutamate receptor ion channels: structure, regulation, and function. Pharmacol. Rev. 2010, 62:405-496.
56. Uemura T., Lee S.J., Yasumura M., Takeuchi T., Yoshida T., Ra M., Taguchi R., Sakimura K., Mishina M. Trans-synaptic interaction of GluRdelta2 and Neurexin through Cbln1 mediates synapse formation in the cerebellum. Cell 2010, 141:1068-1079.
57. Valluru L., Xu J., Zhu Y., Yan S., Contractor A., Swanson G.T. Ligand binding is a critical requirement for plasma membrane expression of heteromeric kainate receptors. J. Biol. Chem. 2005, 280:6085-6093.
58. Vistica J., Dam J., Balbo A., Yikilmaz E., Mariuzza R.A., Rouault T.A., Schuck P. Sedimentation equilibrium analysis of protein interactions with global implicit mass conservation constraints and systematic noise decomposition. Anal. Biochem. 2004, 326:234-256.
59. Watkins J.C., Evans R.H. Excitatory amino acid transmitters. Annu. Rev. Pharmacol. Toxicol. 1981, 21:165-204.
60. Werner P., Voigt M., Keinänen K., Wisden W., Seeburg P.H. Cloning of a putative high-affinity kainate receptor expressed predominantly in hippocampal CA3 cells. Nature 1991, 351:742-744.
61. Xu D., Hopf C., Reddy R., Cho R.W., Guo L., Lanahan A., Petralia R.S., Wenthold R.J., O'Brien R.J., Worley P. Narp and NP1 form heterocomplexes that function in developmental and activity-dependent synaptic plasticity. Neuron 2003, 39:513-528.
62. Yuan H., Hansen K.B., Vance K.M., Ogden K.K., Traynelis S.F. Control of NMDA receptor function by the NR2 subunit amino-terminal domain. J. Neurosci. 2009, 29:12045-12058.