Domain architecture of a calcium-permeable AMPA receptor in a ligand-free conformation

Frontiers in Molecular Neuroscience

Volumn , Issue JANUARY 2012, 2012, Pages

  Midgett, Charles R ^a   Gill, Avinash ^a   Madden, Dean R ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

Author keywords

Electron microscopy; Ionotropic glutamate receptors; Ligand gated ion channels; Protein structure; Receptor activation; Single particle reconstruction

Indexed keywords

AMPA RECEPTOR; IONOTROPIC RECEPTOR; LIGAND GATED ION CHANNEL;

ARTICLE; CHANNEL GATING; CRYSTALLOGRAPHY; DIMERIZATION; ELECTRON MICROSCOPY; HYDRODYNAMICS; IMAGE PROCESSING; LIGAND BINDING; OLIGOMERIZATION; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PURIFICATION; PROTEIN STRUCTURE; STRUCTURE ANALYSIS;

EID: 84856790671     PISSN: 16625099     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnmol.2011.00056     Document Type: Article

References (76)

1. Abele, R., Keinänen, K., and Madden, D. R. (2000). Agonist-induced isomerization in a glutamate receptor ligand-binding domain: a kinetic and mutagenetic analysis. J. Biol. Chem. 275, 21355-21363.
2. Alam, A., and Jiang, Y. (2009). Highresolution structure of the open NaK channel. Nat. Struct. Mol. Biol. 16, 30-34.
3. Armstrong, N., Jasti, J., Beich-Frandsen, M., and Gouaux, E. (2006). Measurement of conformational changes accompanying desensitization in an ionotropic glutamate receptor. Cell 127, 85-97.
4. Armstrong, N. A., and Gouaux, E. (2000). Mechanisms for activation and antagonism of an AMPAsensitive glutamate receptor: crystal structures of the GluR2 ligand binding core. Neuron 28, 165-181.
5. Ayalon, G., and Stern-Bach, Y. (2001). Functional assembly of AMPA and kainate receptors is mediated by several discrete protein-protein interactions. Neuron 13, 103-113.
6. Braitenberg, V., and Schüz, A. (1998). Cortex: Statistics and Geometry of Neuronal Connectivity. Berlin: Springer Verlag.
7. Braithwaite, S. P., Xia, H., and Malenka, R. C. (2002). Differential roles for NSF and GRIP/ABP in AMPA receptor cycling. Proc. Natl. Acad. Sci. U.S.A. 99, 7096-7101.
8. Burnashev, N., Monyer, H., Seeburg, P. H., and Sakmann, B. (1992). Divalent ion permeability of AMPA receptor channels is dominated by the edited form of a single subunit. Neuron 8, 189-198.
9. Burnashev, N., Villarroel, A., and Sakmann, B. (1996). Dimensions and ion selectivity of recombinant AMPA and kainate receptor channels and their dependence on Q/R site residues. J. Physiol. 496, 165-173.
10. Clayton, A., Siebold, C., Gilbert, R. J., Sutton, G. C., Harlos, K., Mcilhinney, R. A., Jones, E. Y., and Aricescu, A. R. (2009). Crystal structure of the GluR2 amino-terminal domain provides insights into the architecture and assembly of ionotropic glutamate receptors. J. Mol. Biol. 392, 1125-1132.
11. Collingridge, G. L., Olsen, R. W., Peters, J., and Spedding, M. (2009). A nomenclature for ligand-gated ion channels. Neuropharmacology. 56, 2-5.
12. 2+- permeable AMPA receptors: synaptic plasticity and beyond. Curr. Opin. Neurobiol. 16, 288-297.
13. Derkach, V. A., Oh, M. C., Guire, E. S., and Soderling, T. R. (2007). Regulatory mechanisms of AMPA receptors in synaptic plasticity. Nat. Rev. Neurosci. 8, 101-113.
14. Emsley, P., and Cowtan, K. (2004). Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132.
15. Furukawa, H., Singh, S. K., Mancusso, R., and Gouaux, E. (2005). Subunit arrangement and function in NMDA receptors. Nature 438, 185-192.
16. Gill, A., Birdsey-Benson, A., Jones, B. L., Henderson, L. P., and Madden, D. R. (2008). Correlating AMPA receptor activation and cleft closure across subunits: crystal structures of the GluR4 ligand-binding domain in complex with full and partial agonists. Biochemistry 47, 13831-13841.
17. Gill, A., and Madden, D. R. (2006).Glutamate receptor ion channels: structural insights into molecular mechanisms, in Structural Biology of Membrane Proteins, eds R. Grisshammer and S. Buchanan (Cambridge, UK: Royal Society of Chemistry), 349-372.
18. Greger, I. H., Khatri, L., Kong, X., and Ziff, E. B. (2003). AMPA receptor tetramerization is mediated by Q/R editing. Neuron 40, 763-774.
19. Hansen, K. B., Furukawa, H., and Traynelis, S. F. (2010). Control of assembly and function of glutamate receptors by the aminoterminal domain. Mol. Pharmacol. 78, 535-549.
20. Hinoi, E., Takarada, T., Ueshima, T., Tsuchihashi, Y., and Yoneda, Y. (2004). Glutamate signaling in peripheral tissues. Eur. J. Biochem. 271, 1-13.
21. Horning, M. S., and Mayer, M. L. (2004). Regulation of AMPA receptor gating by ligand binding core dimers. Neuron 41, 379-388.
22. Jin, R., and Gouaux, E. (2003). Probing the function, confomational plasticity, and dimer-dimer contacts of the GluR2 ligand-binding core: studies of 5-substituted willardiines and GluR2 S1S2 in the crystal. Biochemistry 42, 5201-5213.
23. Jin, R., Singh, S. K., Gu, S., Furukawa, H., Sobolevsky, A. I., Zhou, J., Jin, Y., and Gouaux, E. (2009). Crystal structure and association behaviour of the GluR2 amino-terminal domain. EMBO J. 28, 1812-1823.
24. Kaczor, A. A., Kijkowska-Murak, U. A., and Matosiuk, D. (2008). Theoretical studies on the structure and symmetry of the transmembrane region of glutamatergic GluR5 receptor. J. Med. Chem. 51, 3765-3776.
25. Keinänen, K., Jouppila, A., and Kuusinen, A. (1998). Characterization of the kainate-binding domain of the glutamate receptor GluR-6 subunit. Biochem. J. 330, 1461-1467.
26. Kelly, L., Farrant, M., and Cull-Candy, S. G. (2009). Synaptic mGluR activation drives plasticity of calciumpermeable AMPA receptors. Nat. Neurosci. 12, 593-601.
27. Klein, R. M., and Howe, J. R. (2004). Effects of the lurcher mutation on GluR1 desensitization and activation kinetics. J. Neurosci. 24, 4941-4951.
28. Kuner, T., Beck, C., Sakmann, B., and Seeburg, P. H. (2001). Channellining residues of the AMPA receptor M2 segment: structural environment of the Q/R site and identification of the selectivity filter. J. Neurosci. 21, 4162-4172.
29. + channels and ionotropic glutamate receptors? Trends Neurosci. 26, 27-32.
30. Kuusinen, A., Abele, R., Madden, D. R., and Keinänen, K. (1999). Oligomerization and ligand-binding properties of the ectodomain of the AMPA receptor subunit GluRD. J. Biol. Chem. 274, 28937-28943.
31. Laue, T. M., Shah, B. D., Ridgeway, T. M., and Pelletier, S. L. (1992). Computer-aided interpretation of analytical sedimentation data for proteins, in Analytical Ultracentrifugation in Biochemistry and Polymer Sciences, eds S. E. Harding, A. J. Rowe, and J. C. Horton (Cambridge, UK: Royal Society for Chemistry), 90-125.
32. Lebart, L., Morineau, A., and Warwick, K. M. (1984). Automatic classification-clustering techniques used with principal axes methods, in Multivariate Descriptive Statistical Analysis, ed. E. M. Berry (New York: John Wiley and Sons), 109-145.
33. 2+-permeable AMPA receptors in synaptic plasticity and neuronal death. Trends Neurosci. 30, 126-134.
34. Ludtke, S. J., Baldwin, P. R., and Chiu, W. (1999). EMAN: semiautomated software for high-resolution singleparticle reconstructions. J. Struct. Biol. 128, 82-97.
35. Madden, D. R. (2002). The structure and function of glutamate receptorion channels. Nat. Rev. Neurosci. 3, 91-101.
36. Madden, D. R., Abele, R., Andersson, A., and Keinänen, K. (2000). Large-scale expression and thermodynamic characterization of a glutamate receptor agonist-binding domain. Eur. J. Biochem. 267, 4281-4289.
37. Madden, D. R., Armstrong, N., Svergun, D., Pérez, J., and Vachette, P. (2005). Solution-scattering evidence for agonist- and antagonist- induced modulation of cleft closure in a glutamate receptor ligandbinding domain. J. Biol. Chem. 280, 23637-23642.
38. Madden, D. R., and Safferling, M. (2007). Baculoviral expression of an integral membrane protein for structural studies. Methods Mol. Biol. 363, 39-57.
39. Man, H. Y. (2011). GluA2-lacking, calcium-permeable AMPA receptors - inducers of plasticity? Curr. Opin. Neurobiol. 21, 291-298.
40. Mansour, M., Nagarajan, N., Nehring, R., Clements, J., and Rosenmund, C. (2001). Heteromeric AMPA receptors assemble with a preferred subunit stoichiometry and spatial arrangement. Neuron 32, 841-853.
41. Mayer, M. L. (2011). Structure and mechanism of glutamate receptor ion channel assembly, activation and modulation. Curr. Opin. Neurobiol. 21, 283-290.
42. Midgett, C. R., and Madden, D. R. (2008). The quaternary structure of a calcium-permeable AMPA receptor: conservation of shape and symmetry across functionally distinct subunit assemblies. J. Mol. Biol. 382, 578-584.
43. Milstein, A. D., and Nicoll, R. A. (2008). Regulation of AMPA receptor gating and pharmacology by TARP auxiliary subunits. Trends Pharmacol. Sci. 29, 333-339.
44. Mullins, L. J. (1960). An analysis of pore size in excitable membranes. J. Gen. Physiol. 43, 105-117.
45. Nakagawa, T., Cheng, Y., Ramm, E., Sheng, M., and Walz, T. (2005). Structure and different conformational states of native AMPA receptor complexes. Nature 433, 545-549.
46. Nakagawa, T., Cheng, Y., Sheng, M., and Walz, T. (2006). Three-dimensional structure of an AMPA receptor without associated stargazin/TARP proteins. Biol. Chem. 387, 179-187.
47. + channels examined by scanning mutagenesis. J. Gen. Physiol. 117, 345-359.
48. Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C., and Ferrin, T. E. (2004). UCSF Chimera - a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612.
49. Philipps, B., Rotmann, D., Wicki, M., Mayr, L. M., and Forstner, M. (2005). Time reduction and process optimization of the baculovirus expression system for more efficient recombinant protein production in insect cells. Protein Expr. Purif. 42, 211-218.
50. Poon, K., Nowak, L. M., and Oswald, R. E. (2010). Characterizing singlechannel behavior of GluA3 receptors. Biophys. J. 99, 1437-1446.
51. Prieto, M. L., and Wollmuth, L. P. (2010). Gating modes in AMPA receptors. J. Neurosci. 30, 4449-4459.
52. Rossmann, M., Sukumaran, M., Penn, A. C., Veprintsev, D. B., Babu, M. M., and Greger, I. H. (2011). Subunitselective N-terminal domain associations organize the formation of AMPA receptor heteromers. EMBO J. 30, 959-971.
53. Safferling, M., Tichelaar, W., Kümmerle, G., Jouppila, A., Kuusinen, A., Keinänen, K., and Madden, D. R. (2001). First images of a glutamate receptor ion channel: oligomeric state and molecular dimensions of GluRB homomers. Biochemistry 40, 13948-13953.
54. Schägger, H., Cramer, W. A., and Von Jagow, G. (1994). Analysis of molecular masses and oligomeric states of protein complexes by blue native electrophoresis and isolation of membrane protein complexes by two-dimensional native electrophoresis. Anal. Biochem. 217, 220-230.
55. Schorge, S., and Colquhoun, D. (2003). Studies of NMDA receptor function and stoichiometry with truncated and tandem subunits. J. Neurosci. 23, 1151-1158.
56. Shanks, N. F., Maruo, T., Farina, A. N., Ellisman, M. H., and Nakagawa, T. (2010). Contribution of the global subunit structure and stargazin on the maturation of AMPA receptors. J. Neurosci. 30, 2728-2740.
57. Sheridan, D. L., Robert, A., Cho, C. H., Howe, J. R., and Hughes, T. E. (2006). Regions of α-amino-5- methyl-3-hydroxy-4-isoxazole propionic acid receptor subunits that are permissive for the insertion of green fluorescent protein. Neuroscience 141, 837-849.
58. +-conducting channel. Nature 440, 570-574.
59. Sobolevsky, A. I., Beck, C., and Wollmuth, L. P. (2002). Molecular Rearrangements of the extracellular vestibule in NMDAR channels during gating. Neuron 33, 75-85.
60. Sobolevsky, A. I., Prodromou, M. L., Yelshansky, M. V., and Wollmuth, L. P. (2007). Subunit-specific contribution of pore-forming domains to NMDA receptor channel structure and gating. J. Gen. Physiol. 129, 509-525.
61. Sobolevsky, A. I., Rosconi, M. P., and Gouaux, E. (2009). X-ray structure, symmetry and mechanism of an AMPA-subtype glutamate receptor. Nature 462, 745-756.
62. Sobolevsky, A. I., Yelshansky, M. V., and Wollmuth, L. P. (2004). The outer pore of the glutamate receptor channel has 2-fold rotational symmetry. Neuron 41, 367-378.
63. Sommer, B., Köhler, M., Sprengel, R., and Seeburg, P. H. (1991). RNA editing in brain controls a determinant of ion flow in glutamate-gated channels. Cell 67, 11-19.
64. Stafford, W. F., and Sherwood, P. J. (2004). Analysis of heterologous interacting systems by sedimentation velocity: curve fitting algorithms for estimation of sedimentation coefficients, equilibrium and kinetic constants. Biophys. Chem. 108, 231-243.
65. Stern-Bach, Y., Russo, S., Neuman, M., and Rosenmund, C. (1998). A point mutation in the glutamate binding site blocks desensitization of AMPA receptors. Neuron 21, 907-918.
66. Sukumaran, M., Rossmann, M., Shrivastava, I., Dutta, A., Bahar, I., and Greger, I. H. (2011). Dynamics and allosteric potential of the AMPA receptor N-terminal domain. EMBO J. 30, 972-982.
67. Sun, Y., Olson, R., Horning, M., Armstrong, N., Mayer, M., and Gouaux, E. (2002). Mechanism of glutamate receptor desensitization. Nature 417, 245-253.
68. Tichelaar, W., Safferling, M., Keinänen, K., Stark, H., and Madden, D. R. (2004). The three-dimensional structure of an ionotropic glutamate receptor reveals a dimer-of- dimers assembly. J. Mol. Biol. 344, 435-442.
69. Tomita, S. (2010). Regulation of ionotropic glutamate receptors by their auxiliary subunits. Physiology (Bethesda) 25, 41-49.
70. 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., and Dingledine, R. (2010). Glutamate receptor ion channels: structure, regulation, and function. Pharmacol. Rev. 62, 405-496.
71. Tsien, R. Y. (1998). The green fluorescent protein. Annu. Rev. Biochem. 67, 509-544.
72. Turski, L., Huth, A., Sheardown, M., Mcdonald, F., Neuhaus, R., Schneider, H. H., Dirnagl, U., Wiegand, F., Jacobsen, P., and Ottow, E. (1998). ZK200775: a phosphonate quinoxalinedione AMPA antagonist for neuroprotection in stroke and trauma. Proc. Natl. Acad. Sci. U.S.A. 95, 10960-10965.
73. Verdoorn, T. A., Burnashev, N., Monyer, H., Seeburg, P. H., and Sakmann, B. (1991). Structural determinants of ion flow through recombinant glutamate receptor channels. Science 252, 1715-1718.
74. Verschoor, A., Frank, J., Radermacher, M., Wagenknecht, T., and Boublik, M. (1984). Three-dimensional reconstruction of the 30 S ribosomal subunit from randomly oriented particles. J. Mol. Biol. 178, 677-698.
75. Wo, Z. G., and Oswald, R. E. (1995). Unraveling the modular design of glutamate-gated ion channels. Trends Neurosci. 18, 161-168.
76. Zhang, W., Howe, J. R., and Popescu, G. K. (2008). Distinct gating modes determine the biphasic relaxation of NMDA receptor currents. Nat. Neurosci. 11, 1373-1375.