A eukaryotic specific transmembrane segment is required for tetramerization in AMPA receptors

Journal of Neuroscience

Volumn 33, Issue 23, 2013, Pages 9840-9845

  Salussolia, Catherine L ^a   Gan, Quan ^a   Kazi, Rashek ^a   Singh, Puja ^c   Allopenna, Janet ^a   Furukawa, Hiro ^c   Wollmuth, Lonnie P ^a,b  

^a STONY BROOK UNIVERSITY   (United States)

^b Stony Brook University   (United States)

^c Simons Center for Quantitative Biology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPA RECEPTOR; IONOTROPIC RECEPTOR;

AMINO ACID SUBSTITUTION; ARTICLE; CHEMICAL REACTION; EUKARYOTE; GEL PERMEATION CHROMATOGRAPHY; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; M4 SEGMENT; MEMBRANE; NATIVE POLYACRYLAMIDE GEL ELECTROPHORESIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SITE DIRECTED MUTAGENESIS; TETRAMERIZATION; TRANSMEMBRANE SEGMENT;

ANIMALS; CELL MEMBRANE; EUKARYOTIC CELLS; HEK293 CELLS; HUMANS; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, SECONDARY; PROTEIN SUBUNITS; RATS; RECEPTORS, AMPA;

EID: 84878485837     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2626-12.2013     Document Type: Article

References (34)

1. Anggono V, Huganir RL (2012) Regulation of AMPA receptor trafficking and synaptic plasticity. Curr Opin Neurobiol 22:461-469.CrossRef Medline
2. Atlason PT, Garside ML, Meddows E, Whiting P, McIlhinney RA (2007) N-Methyl-D-aspartate (NMDA) receptor subunit NR1 forms the substrate for oligomeric assembly of the NMDA receptor. J Biol Chem 282: 25299-25307.CrossRef Medline
3. Ayalon G, Stern-Bach Y (2001) Functional assembly of AMPA and kainite receptors is mediated by several discrete protein-protein interactions. Neuron 31:103-113.CrossRef Medline
4. Cao JY, Qiu S, Zhang J, Wang JJ, Zhang XM, Luo JH (2011) Transmembrane region of N-methyl-D-aspartate receptor (NMDAR) subunit is required for receptor subunit assembly. J Biol Chem 286:27698-27705.CrossRef Medline
5. Chen GQ, Cui C, Mayer ML, Gouaux E (1999) Functional characterization of a potassium-selective prokaryotic glutamate receptor. Nature 402:817-821.CrossRef Medline
6. Citri A, Malenka RC (2008) Synaptic plasticity: multiple forms, functions, and mechanisms. Neuropsychopharmacology 33:18-41.CrossRef Medline
7. Deutsch C (2002) Potassium channel ontogeny. Annu Rev Physiol 64: 19-46.CrossRef Medline
8. Farina AN, Blain KY, Maruo T, Kwiatkowski W, Choe S, Nakagawa T (2011) Separation of domain contacts is required for heterotetrameric assembly of functional NMDA receptors. J Neurosci 31:3565-3579.CrossRef Medline
9. Fleck MW (2006) Glutamate receptors and endoplasmic reticulum quality control: looking beneath the surface. Neuroscientist 12:232-244.CrossRef Medline
10. Furukawa H, Singh SK, Mancusso R, Gouaux E (2005) Subunit arrangement and function in NMDA receptors. Nature 438:185-192.CrossRef Medline
11. Horak M, Chang K, Wenthold RJ (2008) Masking of the endoplasmic reticulum retention signals during assembly of the NMDA receptor. J Neurosci 28:3500-3509.CrossRef Medline
12. Huh KH, Wenthold RJ (1999) Turnover analysis of glutamate receptors identifies a rapidly degraded pool of the N-methyl-D-aspartate receptor subunit, NR1, in cultured cerebellar granule cells. J Biol Chem 274:151-157.CrossRef Medline
13. Karakas E, Simorowski N, Furukawa H (2011) Subunit arrangement and phenylethanolamine binding in GluN1/GluN2B NMDA receptors. Nature 475:249-253.CrossRef Medline
14. Kawate T, Gouaux E (2006) Fluorescence-detection size-exclusion chromatography for precrystallization screening of integral membrane proteins. Structure 14:673-681.CrossRef Medline
15. Lee CH, Gouaux E (2011) Amino terminal domains of the NMDA receptor are organized as local heterodimers. PLoS One 6:e19180.CrossRef Medline
16. Lu W, Roche KW (2012) Posttranslational regulation of AMPA receptor trafficking and function. Curr Opin Neurobiol 22:470-479.Medline
17. Lu W, Shi Y, Jackson AC, Bjorgan K, During MJ, Sprengel R, Seeburg PH, Nicoll RA (2009) Subunit composition of synaptic AMPA receptors revealed by a single-cell genetic approach. Neuron 62:254-268.CrossRef Medline
18. Man HY, Lin JW, Ju WH, Ahmadian G, Liu L, Becker LE, Sheng M, Wang YT (2000) Regulation ofAMPAreceptor-mediated synaptic transmission by clathrin-dependent receptor internalization. Neuron 25:649-662.CrossRef Medline
19. Mayer ML (2011) Structure and mechanism of glutamate receptor ion channel assembly, activation and modulation. Curr Opin Neurobiol 21: 283-290.CrossRef Medline
20. Meddows E, Le Bourdelles B, Grimwood S, Wafford K, Sandhu S, Whiting P, McIlhinney RA (2001) Identification of molecular determinants that are important in the assembly of N-methyl-D-aspartate receptors. J Biol Chem 276:18795-18803.CrossRef Medline
21. Nakagawa T (2010) The biochemistry, ultrastructure, and subunit assembly mechanism of AMPA receptors. Mol Neurobiol 42:161-184.CrossRef Medline
22. Papadakis M, Hawkins LM, Stephenson FA (2004) Appropriate NR1-NR1 disulfide-linked homodimer formation is requisite for efficient expression of functional, cell surface N-methyl-D-aspartate NR1/NR2 receptors. J Biol Chem 279:14703-14712.CrossRef Medline
23. Pasternack A, Coleman SK, Jouppila A, Mottershead DG, Lindfors M, Pasternack M, Keinänen K (2002) Alpha-amino-3-hydroxy-5-methyl-4- isoxazolepropionic acid (AMPA) receptor channels lacking the N-terminal domain. J Biol Chem 277:49662-49667.CrossRef Medline
24. Puddifoot CA, Chen PE, Schoepfer R, Wyllie DJ (2009) Pharmacological characterization of recombinant NR1/NR2ANMDAreceptors with truncated and deleted carboxy termini expressed in Xenopus laevis oocytes. Br J Pharmacol 156:509-518.CrossRef Medline
25. Rossmann M, Sukumaran M, Penn AC, Veprintsev DB, Babu MM, Greger IH (2011) Subunit-selective N-terminal domain associations organize the formation of AMPA receptor heteromers. EMBO J 30:959-971.CrossRef Medline
26. Salussolia CL, Corrales A, Talukder I, Kazi R, Akgul G, Bowen M, Wollmuth LP (2011) Interaction of the M4 segment with other transmembrane segments is required for surface expression of mammalian alpha-amino- 3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptors. J Biol Chem 286:40205-40218.CrossRef Medline
27. Schüler T, Mesic I, Madry C, Bartholomäus I, Laube B (2008) Formation of NR1/NR2 and NR1/NR3 heterodimers constitutes the initial step in N-methyl-D-aspartate receptor assembly. J Biol Chem 283:37-46. Medline
28. Sobolevsky AI, Rosconi MP, Gouaux E (2009) X-ray structure, symmetry and mechanism of an AMPA-subtype glutamate receptor. Nature 462: 745-756.CrossRef Medline
29. Stephenson FA, Cousins SL, Kenny AV (2008) Assembly and forward trafficking of NMDA receptors (Review). Mol Membr Biol 25:311-320.CrossRef Medline
30. Sukumaran M, Penn AC, Greger IH (2012) AMPA receptor assembly: atomic determinants and built-in modulators. Advances in experimental medicine and biology 970:241-264.CrossRef Medline
31. Sun Y, Olson R, Horning M, Armstrong N, Mayer M, Gouaux E (2002) Mechanism of glutamate receptor desensitization. Nature 417:245-253.CrossRef Medline
32. Traynelis SF, Wollmuth LP, McBain CJ, Menniti FS, Vance KM, Ogden KK, Hansen KB, Yuan H, Myers SJ, Dingledine R (2010) Glutamate receptor ion channels: structure, regulation, and function. Pharmacol Rev 62:405-496.CrossRef Medline
33. Wo ZG, Oswald RE (1995) Unraveling the modular design of glutamategated ion channels. Trends Neurosci 18:161-168.CrossRef Medline
34. Yelshansky MV, Sobolevsky AI, Jatzke C, Wollmuth LP (2004) Block of AMPA receptor desensitization by a point mutation outside the ligandbinding domain. J Neurosci 24:4728-4736.CrossRef Medline