Architecture of fully occupied GluA2 AMPA receptor-TARP complex elucidated by cryo-EM

Nature

Volumn 536, Issue 7614, 2016, Pages 108-111

  Zhao, Yan ^a   Chen, Shanshuang ^a   Yoshioka, Craig ^b   Baconguis, Isabelle ^a   Gouaux, Eric ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b Oregon Health and Science University Department of Biomedical Engineering   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DIMER; GLUTAMATE RECEPTOR 2; ION CHANNEL; REGULATOR PROTEIN; TRANSMEMBRANE AMPA RECEPTOR REGULATORY PROTEIN GAMMA 2; UNCLASSIFIED DRUG; AMPA RECEPTOR; CACNG2 PROTEIN, RAT; CALCIUM CHANNEL; GLUTAMATE RECEPTOR IONOTROPIC, AMPA 2; PROTEIN BINDING;

ASYMMETRY; DENSITY; ELECTRON MICROSCOPY; MEMBRANE; NERVOUS SYSTEM; PROTEIN;

ARTICLE; CRYOELECTRON MICROSCOPY; CRYSTAL STRUCTURE; HUMAN; LIGAND BINDING; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN STRUCTURE; ANIMAL; CHANNEL GATING; CHEMISTRY; METABOLISM; MOLECULAR MODEL; PROTEIN MULTIMERIZATION; PROTEIN TERTIARY STRUCTURE; RAT; ULTRASTRUCTURE;

MAMMALIA; RATTUS;

ANIMALS; CALCIUM CHANNELS; CRYOELECTRON MICROSCOPY; ION CHANNEL GATING; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; RATS; RECEPTORS, AMPA;

EID: 84982845575     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature18961     Document Type: Article

References (48)

1. Traynelis, S. F. et al. Glutamate receptor ion channels: structure, regulation, and function. Pharmacol. Rev. 62, 405-496 (2010).
2. Jackson, A. C. & Nicoll, R. A. The expanding social network of ionotropic glutamate receptors: TARPs and other transmembrane auxiliary subunits. Neuron 70, 178-199 (2011).
3. Chen, L. et al. Stargazin regulates synaptic targeting of AMPA receptors by two distinct mechanisms. Nature 408, 936-943 (2000).
4. Saitoh, Y. et al. Tight junctions. Structural insight into tight junction disassembly by Clostridium perfringens enterotoxin. Science 347, 775-778 (2015).
5. Milstein, A. D. & Nicoll, R. A. Regulation of AMPA receptor gating and pharmacology by TARP auxiliary subunits. Trends Pharmacol. Sci. 29, 333-339 (2008).
6. Shi, Y., Lu, W., Milstein, A. D. & Nicoll, R. A. The stoichiometry of AMPA receptors and TARPs varies by neuronal cell type. Neuron 62, 633-640 (2009).
7. Tomita, S. et al. Stargazin modulates AMPA receptor gating and trafficking by distinct domains. Nature 435, 1052-1058 (2005).
8. Milstein, A. D., Zhou, W., Karimzadegan, S., Bredt, D. S. & Nicoll, R. A. TARP subtypes differentially and dose-dependently control synaptic AMPA receptor gating. Neuron 55, 905-918 (2007).
9. Soto, D., Coombs, I. D., Kelly, L., Farrant, M. & Cull-Candy, S. G. Stargazin attenuates intracellular polyamine block of calcium-permeable AMPA receptors. Nat. Neurosci. 10, 1260-1267 (2007).
10. Nakagawa, T., Cheng, Y., Ramm, E., Sheng, M. & Walz, T. Structure and different conformational states of native AMPA receptor complexes. Nature 433, 545-549 (2005).
11. Sobolevsky, A. I., Rosconi, M. P. & Gouaux, E. X-ray structure, symmetry and mechanism of an AMPA-subtype glutamate receptor. Nature 462, 745-756 (2009).
12. Chen, L., Dürr, K. L. & Gouaux, E. X-ray structures of AMPA receptor-cone snail toxin complexes illuminate activation mechanism. Science 345, 1021-1026 (2014).
13. Dürr, K. L. et al. Structure and dynamics of AMPA receptor GluA2 in resting, pre-open, and desensitized states. Cell 158, 778-792 (2014).
14. Meyerson, J. R. et al. Structural mechanism of glutamate receptor activation and desensitization. Nature 514, 328-334 (2014).
15. Herguedas, B. et al. Structure and organization of heteromeric AMPA-type glutamate receptors. Science 352, aad3873 (2016).
16. Kuusinen, A., Abele, R., Madden, D. R. & Keinänen, K. Oligomerization and ligand-binding properties of the ectodomain of the a-amino-3-hydroxy-5-methyl-4-isoxazole propionic acid receptor subunit GluRD. J. Biol. Chem. 274, 28937-28943 (1999).
17. Sun, Y. et al. Mechanism of glutamate receptor desensitization. Nature 417, 245-253 (2002).
18. Armstrong, N., Sun, Y., Chen, G.-Q. & Gouaux, E. Structure of a glutamate-receptor ligand-binding core in complex with kainate. Nature 395, 913-917 (1998).
19. Armstrong, N. & Gouaux, E. Mechanisms for activation and antagonism of an AMPA-sensitive glutamate receptor: crystal structures of the GluR2 ligand binding core. Neuron 28, 165-181 (2000).
20. Armstrong, N., Jasti, J., Beich-Frandsen, M. & Gouaux, E. Measurement of conformational changes accompanying desensitization in an ionotropic glutamate receptor. Cell 127, 85-97 (2006).
21. Keinänen, K. et al. A family of AMPA-selective glutamate receptors. Science 249, 556-560 (1990).
22. Sommer, B., Köhler, M., Sprengel, R. & Seeburg, P. H. RNA editing in brain controls a determinant of ion flow in glutamate-gated channels. Cell 67, 11-19 (1991).
23. Sommer, B. et al. Flip and flop: a cell-specific functional switch in glutamateoperated channels of the CNS. Science 249, 1580-1585 (1990).
24. Letts, V. A. et al. The mouse stargazer gene encodes a neuronal Ca2+-channel gamma subunit. Nat. Genet. 19, 340-347 (1998).
25. 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. 30, 2728-2740 (2010).
26. Turetsky, D., Garringer, E. & Patneau, D. K. Stargazin modulates native AMPA receptor functional properties by two distinct mechanisms. J. Neurosci. 25, 7438-7448 (2005).
27. Kawate, T. & Gouaux, E. Fluorescence-detection size-exclusion chromatography for precrystallization screening of integral membrane proteins. Structure 14, 673-681 (2006).
28. Turski, L. et al. ZK200775: a phosphonate quinoxalinedione AMPA antagonist for neuroprotection in stroke and trauma. Proc. Natl Acad. Sci. USA 95, 10960-10965 (1998).
29. Kazi, R., Dai, J., Sweeney, C., Zhou, H. X. & Wollmuth, L. P. Mechanical coupling maintains the fidelity of NMDA receptor-mediated currents. Nat. Neurosci. 17, 914-922 (2014).
30. Dawe, G. B. et al. Distinct structural pathways coordinate the activation of AMPA receptor-auxiliary subunit complexes. Neuron 89, 1264-1276 (2016).
31. Kaae, B. H. et al. Structural proof of a dimeric positive modulator bridging two identical AMPA receptor-binding sites. Chem. Biol. 14, 1294-1303 (2007).
32. Grant, T. & Grigorieff, N. Measuring the optimal exposure for single particle cryo-EM using a 2.6 A reconstruction of rotovirus VP6. eLife 4, e06980 (2015).
33. Mindell, J. A. & Grigorieff, N. Accurate determination of local defocus and specimen tilt in electron microscopy. J. Struct. Biol. 142, 334-347 (2003).
34. Voss, N. R., Yoshioka, C. K., Radermacher, M. & Potter, C. S. & Carragher, B. DoG Picker and TiltPicker: software tools to facilitate particle selection in single particle electron microscopy. J. Struct. Biol. 166, 205-213 (2009).
35. Penczek, P. A., Frank, J. & Spahn, C. M. A method of focused classification, based on the bootstrap 3D variance analysis, and its application to EF-G-dependent translocation. J. Struct. Biol. 154, 184-194 (2006).
36. Zhu, S. et al. Mechanism of NMDA receptor inhibition and activation. Cell 165, 704-714 (2016).
37. Scheres, S. H. RELION: implementation of a Bayesian approach to cryo-EM structure determination. J. Struct. Biol. 180, 519-530 (2012).
38. Arnold, K., Bordoli, L., Kopp, J. & Schwede, T. The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22, 195-201 (2006).
39. Sievers, F. et al. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol. Syst. Biol. 7, 539 (2011).
40. Stothard, P. The sequence manipulation suite: JavaScript programs for analyzing and formatting protein and DNA sequences. Biotechniques 28, 1102, 1104 (2000).
41. Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D 60, 2126-2132 (2004).
42. Drozdetskiy, A., Cole, C., Procter, J. & Barton, G. J. JPred4: a protein secondary structure prediction server. Nucleic Acids Res. 43 (W1), W389-W394 (2015).
43. Baker, M. L., Ju, T. & Chiu, W. Identification of secondary structure elements in intermediate-resolution density maps. Structure 15, 7-19 (2007).
44. Pettersen, E. F. et al. UCSF Chimera - a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612 (2004).
45. Pintilie, G. D., Zhang, J., Goddard, T. D., Chiu, W. & Gossard, D. C. Quantitative analysis of cryo-EM density map segmentation by watershed and scale-space filtering, and fitting of structures by alignment to regions. J. Struct. Biol. 170, 427-438 (2010).
46. Adams, P. D. et al. PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr. D 58, 1948-1954 (2002).
47. The PyMOL Molecular Graphics System. (DeLano Scientific, San Carlos, California, USA, 2002).
48. Kucukelbir, A., Sigworth, F. J. & Tagare, H. D. Quantifying the local resolution of cryo-EM density maps. Nat. Methods 11, 63-65 (2014).