Structural basis of kainate subtype glutamate receptor desensitization

Nature

Volumn 537, Issue 7621, 2016, Pages 567-571

  Meyerson, Joel R ^a,c   Chittori, Sagar ^a,b   Merk, Alan ^a   Rao, Prashant ^a   Han, Tae Hee ^b   Serpe, Mihaela ^b   Mayer, Mark L ^b   Subramaniam, Sriram ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

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

^c BRANDEIS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

KAINIC ACID RECEPTOR; GLUK2 KAINATE RECEPTOR; LIGAND; PROTEIN SUBUNIT;

AMINO ACID; CHEMICAL BINDING; ION; LIGAND; NERVOUS SYSTEM; NUMERICAL MODEL; SYMMETRY; VERTEBRATE;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CRYOELECTRON MICROSCOPY; LIGAND BINDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN STRUCTURE; RECEPTOR DOWN REGULATION; STRUCTURE ANALYSIS; ANIMAL; BINDING SITE; CHANNEL GATING; CHEMISTRY; DOWN REGULATION; METABOLISM; MOLECULAR MODEL; PROTEIN DOMAIN; PROTEIN SUBUNIT; RAT; ULTRASTRUCTURE;

VERTEBRATA;

ANIMALS; BINDING SITES; CRYOELECTRON MICROSCOPY; DOWN-REGULATION; ION CHANNEL GATING; LIGANDS; MODELS, MOLECULAR; PROTEIN DOMAINS; PROTEIN SUBUNITS; RATS; RECEPTORS, KAINIC ACID;

EID: 84989157893     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature19352     Document Type: Article

References (40)

1. Burnashev, N. and Szepetowski, P. NMDA receptor subunit mutations in neurodevelopmental disorders. Curr. Opin. Pharmacol. 20, 73-82 (2015).
2. Lesca, G. et al. GRIN2A mutations in acquired epileptic aphasia and related childhood focal epilepsies and encephalopathies with speech and language dysfunction. Nat. Genet. 45, 1061-1066 (2013).
3. Durr, K. L. et al. Structure and dynamics of AMPA receptor GluA2 in resting, pre-open, and desensitized states. Cell 158, 778-792 (2014).
4. Meyerson, J. R. et al. Structural mechanism of glutamate receptor activation and desensitization. Nature 514, 328-334 (2014).
5. Schauder, D. M. et al. Glutamate receptor desensitization is mediated by changes in quaternary structure of the ligand binding domain. Proc. Natl Acad. Sci. USA 110, 5921-5926 (2013).
6. Sobolevsky, A. I., Rosconi, M. P. and Gouaux, E. X-ray structure, symmetry and mechanism of an AMPA-subtype glutamate receptor. Nature 462, 745-756 (2009).
7. Traynelis, S. F. et al. Glutamate receptor ion channels: structure, regulation, and function. Pharmacol. Rev. 62, 405-496 (2010).
8. Mayer, M. L. Glutamate receptors at atomic resolution. Nature 440, 456-462 (2006).
9. Watkins, J. C. and Evans, R. H. Excitatory amino acid transmitters. Annu. Rev. Pharmacol. Toxicol. 21, 165-204 (1981).
10. Chen, L., Durr, K. L. and Gouaux, E. X-ray structures of AMPA receptor-cone snail toxin complexes illuminate activation mechanism. Science 345, 1021-1026 (2014).
11. Herguedas, B. et al. Structure and organization of heteromeric AMPA-type glutamate receptors. Science 352, aad3873 (2016).
12. Nakagawa, T., Cheng, Y., Ramm, E., Sheng, M. and Walz, T. Structure and different conformational states of native AMPA receptor complexes. Nature 433, 545-549 (2005).
13. Twomey, E. C., Yelshanskaya, M. V., Grassucci, R. A., Frank, J. and Sobolevsky, A. I. Elucidation of AMPA receptor-stargazin complexes by cryo-electron microscopy. Science 353, 83-86 (2016).
14. Yelshanskaya, M. V., Li, M. and Sobolevsky, A. I. Structure of an agonist-bound ionotropic glutamate receptor. Science 345, 1070-1074 (2014).
15. Zhao, Y., Chen, S., Yoshioka, C., Baconguis, I. and Gouaux, E. Architecture of fully occupied GluA2 AMPA receptor-TARP complex elucidated by cryo-EM. Nature 536, 108-111 (2016).
16. Alushin, G. M., Jane, D. and Mayer, M. L. Binding site and ligand flexibility revealed by high resolution crystal structures of GluK1 competitive antagonists. Neuropharmacology 60, 126-134 (2011).
17. Jones, K. A., Wilding, T. J., Huettner, J. E. and Costa, A. M. Desensitization of kainate receptors by kainate, glutamate and diastereomers of 4-methylglutamate. Neuropharmacology 36, 853-863 (1997).
18. Moykkynen, T., Coleman, S. K., Semenov, A. and Keinanen, K. The N-terminal domain modulates a -amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptor desensitization. J. Biol. Chem. 289, 13197-13205 (2014).
19. Dutta, A. et al. Cooperative dynamics of intact AMPA and NMDA glutamate receptors: similarities and subfamily-specific differences. Structure 23, 1692-1704 (2015).
20. Carbone, A. L. and Plested, A. J. Coupled control of desensitization and gating by the ligand binding domain of glutamate receptors. Neuron 74, 845-857 (2012).
21. Fleck, M. W., Cornell, E. and Mah, S. J. Amino-acid residues involved in glutamate receptor 6 kainate receptor gating and desensitization. J. Neurosci. 23, 1219-1227 (2003).
22. Chaudhry, C., Plested, A. J., Schuck, P. and Mayer, M. L. Energetics of glutamate receptor ligand binding domain dimer assembly are modulated by allosteric ions. Proc. Natl Acad. Sci. USA 106, 12329-12334 (2009).
23. Dawe, G. B. et al. Distinct structural pathways coordinate the activation of AMPA peceptor-auxiliary subunit complexes. Neuron 89, 1264-1276 (2016).
24. Plested, A. J., Vijayan, R., Biggin, P. C. and Mayer, M. L. Molecular basis of kainate receptor modulation by sodium. Neuron 58, 720-735 (2008).
25. Patneau, D. K., Mayer, M. L., Jane, D. E. and Watkins, J. C. Activation and desensitization of AMPA/kainate receptors by novel derivatives of willardiine. J. Neurosci. 12, 595-606 (1992).
26. Mayer, M. L. Crystal structures of the GluR5 and GluR6 ligand binding cores: molecular mechanisms underlying kainate receptor selectivity. Neuron 45, 539-552 (2005).
27. Meyerson, J. R. et al. Self-assembled monolayers improve protein distribution on holey carbon cryo-EM supports. Sci. Rep. 4, 7084 (2014).
28. Li, X. et al. Electron counting and beam-induced motion correction enable near-atomic-resolution single-particle cryo-EM. Nat. Methods 10, 584-590 (2013).
29. Tang, G. et al. EMAN2: an extensible image processing suite for electron microscopy. J. Struct. Biol. 157, 38-46 (2007).
30. Scheres, S. H. RELION: implementation of a Bayesian approach to cryo-EM structure determination. J. Struct. Biol. 180, 519-530 (2012).
31. Mindell, J. A. and Grigorieff, N. Accurate determination of local defocus and specimen tilt in electron microscopy. J. Struct. Biol. 142, 334-347 (2003).
32. Scheres, S. H. Beam-induced motion correction for sub-megadalton cryo-EM particles. eLife 3, e03665 (2014).
33. Pettersen, E. F. et al. UCSF Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612 (2004).
34. The PyMOL Molecular Graphics System. Version 1.8 Schrodinger, LLC. (DeLano Scientific, 2002).
35. Smart, O. S., Goodfellow, J. M. and Wallace, B. A. The pore dimensions of gramicidin A. Biophys. J. 65, 2455-2460 (1993).
36. Heymann, J. B. Bsoft: image and molecular processing in electron microscopy. J. Struct. Biol. 133, 156-169 (2001).
37. Adams, P. D. et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221 (2010).
38. Emsley, P., Lohkamp, B., Scott, W. G. and Cowtan, K. Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501 (2010).
39. Wang, R. Y. et al. De novo protein structure determination from near-atomicresolution cryo-EM maps. Nat. Methods 12, 335-338 (2015).
40. Horning, M. S. and Mayer, M. L. Regulation of AMPA receptor gating by ligand binding core dimers. Neuron 41, 379-388 (2004).