Defining the structural relationship between kainate-receptor deactivation and desensitization

Nature Structural and Molecular Biology

Volumn 20, Issue 9, 2013, Pages 1054-1061

  Dawe, G Brent ^a   Musgaard, Maria ^b   Andrews, Elizabeth D ^a   Daniels, Bryan A ^a   Aurousseau, Mark R P ^a   Biggin, Philip C ^b   Bowie, Derek ^a  

^a MCGILL UNIVERSITY   (Canada)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CATION; IONOTROPIC RECEPTOR; KAINIC ACID RECEPTOR; LIGAND; LIGAND GATED ION CHANNEL;

ALLOSTERISM; ANIMAL CELL; ARTICLE; CHANNEL GATING; CONTROLLED STUDY; MAMMAL CELL; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STRUCTURE; RAT; RECEPTOR DOWN REGULATION;

ANIMALS; BINDING SITES; HEK293 CELLS; HUMANS; ION CHANNEL GATING; LIGANDS; MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION; MUTAGENESIS, SITE-DIRECTED; PROTEIN MULTIMERIZATION; PROTEIN SUBUNITS; RATS; RECEPTORS, AMPA; RECEPTORS, KAINIC ACID; RECOMBINANT PROTEINS;

RATTUS;

EID: 84883743072     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.2654     Document Type: Article

References (53)

1. Katz, B. & Thesleff, S. A study of the desensitization produced by acetylcholine at the motor end-plate. J. Physiol. (Lond.) 138, 63-80 (1957).
2. Shelley, C. & Cull-Candy, S.G. Desensitization and models of receptor-channel activation. J. Physiol. (Lond.) 588, 1395-1397 (2010).
3. Jones, M.V. & Westbrook, G.L. The impact of receptor desensitization on fast synaptic transmission. Trends Neurosci. 19, 96-101 (1996). (Pubitemid 26059993)
4. Hille, B. Ion Channels of Excitable Membranes 169-200 (Sinauer Associates, 2001).
5. Patneau, D.K., Mayer, M.L., Jane, D.E. & Watkins, J.C. Activation and desensitization of AMPA/kainate receptors by novel derivatives of willardiine. J. Neurosci. 12, 595-606 (1992).
6. Traynelis, S.F. et al. Glutamate receptor ion channels: structure, regulation, and function. Pharmacol. Rev. 62, 405-496 (2010).
7. Corringer, P.J. et al. Structure and pharmacology of pentameric receptor channels: from bacteria to brain. Structure 20, 941-956 (2012).
8. Flynn, G.E., Johnson, J.P. Jr. & Zagotta, W.N. Cyclic nucleotide-gated channels: shedding light on the opening of a channel pore. Nat. Rev. Neurosci. 2, 643-651 (2001). (Pubitemid 33674056)
9. Hansen, K.B., Yuan, H. & Traynelis, S.F. Structural aspects of AMPA receptor activation, desensitization and deactivation. Curr. Opin. Neurobiol. 17, 281-288 (2007). (Pubitemid 46880320)
10. Wollmuth, L.P. & Sobolevsky, A.I. Structure and gating of the glutamate receptor ion channel. Trends Neurosci. 27, 321-328 (2004). (Pubitemid 38692413)
11. Madden, D.R. The structure and function of glutamate receptor ion channels. Nat. Rev. Neurosci. 3, 91-101 (2002). (Pubitemid 135706578)
12. 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). (Pubitemid 28503434)
13. Sun, Y. et al. Mechanism of glutamate receptor desensitization. Nature 417, 245-253 (2002). (Pubitemid 34534700)
14. 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). (Pubitemid 44466635)
15. Weston, M.C., Schuck, P., Ghosal, A., Rosenmund, C. & Mayer, M.L. Conformational restriction blocks glutamate receptor desensitization. Nat. Struct. Mol. Biol. 13, 1120-1127 (2006). (Pubitemid 44885924)
16. Priel, A., Selak, S., Lerma, J. & Stern-Bach, Y. Block of kainate receptor desensitization uncovers a key trafficking checkpoint. Neuron 52, 1037-1046 (2006). (Pubitemid 44909414)
17. Gielen, M. et al. Structural rearrangements of NR1/NR2A NMDA receptors during allosteric inhibition. Neuron 57, 80-93 (2008).
18. Borschel, W.F., Murthy, S.E., Kasperek, E.M. & Popescu, G.K. NMDA receptor activation requires remodelling of intersubunit contacts within ligand-binding heterodimers. Nat. Commun. 2, 498 (2011).
19. Nayeem, N., Zhang, Y., Schweppe, D.K., Madden, D.R. & Green, T. A nondesensitizing kainate receptor point mutant. Mol. Pharmacol. 76, 534-542 (2009).
20. Plested, A.J. & Mayer, M.L. Structure and mechanism of kainate receptor modulation by anions. Neuron 53, 829-841 (2007). (Pubitemid 46389565)
21. Plested, A.J., Vijayan, R., Biggin, P.C. & Mayer, M.L. Molecular basis of kainate receptor modulation by sodium. Neuron 58, 720-735 (2008). (Pubitemid 351784520)
22. Wong, A.Y., Fay, A.M. & Bowie, D. External ions are coactivators of kainate receptors. J. Neurosci. 26, 5750-5755 (2006). (Pubitemid 44315267)
23. Bowie, D. Ion-dependent gating of kainate receptors. J. Physiol. (Lond.) 588, 67-81 (2010).
24. Zhang, W. et al. A transmembrane accessory subunit that modulates kainate-type glutamate receptors. Neuron 61, 385-396 (2009).
25. Nayeem, N., Mayans, O. & Green, T. Conformational flexibility of the ligand-binding domain dimer in kainate receptor gating and desensitization. J. Neurosci. 31, 2916-2924 (2011).
26. Daniels, B.A., Andrews, E.D., Aurousseau, M.R., Accardi, M.V. & Bowie, D. Crosslinking the ligand-binding domain dimer interface locks kainate receptors out of the main open state. J. Physiol. (Lond.) http://dx.doi.org/10. 1113/jphysiol.2013.253666 (27 May 2013).
27. 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. 25, 2215-2225 (2005). (Pubitemid 40322262)
28. Stern-Bach, Y., Russo, S., Neuman, M. & Rosenmund, C. A point mutation in the glutamate binding site blocks desensitization of AMPA receptors. Neuron 21, 907-918 (1998). (Pubitemid 28498797)
29. Mitchell, N.A. & Fleck, M.W. Targeting AMPA receptor gating processes with allosteric modulators and mutations. Biophys. J. 92, 2392-2402 (2007). (Pubitemid 46536421)
30. Bowie, D. & Lange, G.D. Functional stoichiometry of glutamate receptor desensitization. J. Neurosci. 22, 3392-3403 (2002). (Pubitemid 37465745)
31. 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).
32. Bowie, D. External anions and cations distinguish between AMPA and kainate receptor gating mechanisms. J. Physiol. (Lond.) 539, 725-733 (2002). (Pubitemid 35175424)
33. Del Castillo, J. & Katz, B. Interaction at end-plate receptors between different choline derivatives. Proc. R. Soc. Lond. B Biol. Sci. 146, 369-381 (1957).
34. Hodgkin, A.L. & Huxley, A.F. The dual effect of membrane potential on sodium conductance in the giant axon of Loligo. J. Physiol. (Lond.) 116, 497-506 (1952).
35. Hoshi, T., Zagotta, W.N. & Aldrich, R.W. Biophysical and molecular mechanisms of Shaker potassium channel inactivation. Science 250, 533-538 (1990). (Pubitemid 120031778)
36. Stühmer, W. et al. Structural parts involved in activation and inactivation of the sodium channel. Nature 339, 597-603 (1989). (Pubitemid 19174342)
37. Unwin, N., Toyoshima, C. & Kubalek, E. Arrangement of the acetylcholine receptor subunits in the resting and desensitized states, determined by cryoelectron microscopy of crystallized Torpedo postsynaptic membranes. J. Cell Biol. 107, 1123-1138 (1988).
38. Armstrong, C.M. & Bezanilla, F. Inactivation of the sodium channel: II. gating current experiments. J. Gen. Physiol. 70, 567-590 (1977). (Pubitemid 8239322)
39. Mano, I., Lamed, Y. & Teichberg, V.I. A venus flytrap mechanism for activation and desensitization of ?-amino-3-hydroxy-5-methyl-4-isoxazole propionic acid receptors. J. Biol. Chem. 271, 15299-15302 (1996). (Pubitemid 26225293)
40. Barberis, A., Sachidhanandam, S. & Mulle, C. GluR6/KA2 kainate receptors mediate slow-deactivating currents. J. Neurosci. 28, 6402-6406 (2008).
41. Copits, B.A. & Swanson, G.T. Dancing partners at the synapse: auxiliary subunits that shape kainate receptor function. Nat. Rev. Neurosci. 13, 675-686 (2012).
42. Miesenböck, G., De Angelis, D.A. & Rothman, J.E. Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature 394, 192-195 (1998). (Pubitemid 28325974)
43. Khiroug, S.S. et al. Dynamic visualization of membrane-inserted fraction of pHluorin-tagged channels using repetitive acidification technique. BMC Neurosci. 10, 141 (2009).
44. Zhang, W., Cho, Y., Lolis, E. & Howe, J.R. Structural and single-channel results indicate that the rates of ligand binding domain closing and opening directly impact AMPA receptor gating. J. Neurosci. 28, 932-943 (2008). (Pubitemid 351158996)
45. Colquhoun, D. & Sigworth, F.J. in Single Channel Recording (eds. Sakmann, B. & Neher, E.) 483-587 (Plenum Press, 1995).
46. Chaudhry, C., Weston, M.C., Schuck, P., Rosenmund, C. & Mayer, M.L. Stability of ligand-binding domain dimer assembly controls kainate receptor desensitization. EMBO J. 28, 1518-1530 (2009).
47. Jorgensen, W.L., Chandrasekhar, J., Madura, J.D., Impey, R.W. & Klein, M.L. Comparison of simple potential functions for simulating liquid water. J. Chem. Phys. 79, 926-935 (1983).
48. Hess, B., Kutzner, C., Van Der Spoel, D. & Lindahl, E. GROMACS 4: algorithms for highly efficient, load-balanced, and scalable molecular simulation. J. Chem. Theory Comput. 4, 435-447 (2008).
49. Jorgensen, W.L., Maxwell, D.S. & Tirado-Rives, J. Development and testing of the OPLS all-atom force field on conformational energetics and properties of organic liquids. J. Am. Chem. Soc. 118, 11225-11236 (1996). (Pubitemid 26399746)
50. Kaminski, G.A., Friesner, R.A., Tirado-Rives, J. & Jorgensen, W.L. Evaluation and reparametrization of the OPLS-AA force field for proteins via comparison with accurate quantum chemical calculations on peptides. J. Phys. Chem. B 105, 6474-6487 (2001). (Pubitemid 35339015)
51. Berendsen, H.J.C., Postma, J.P.M., Van Gunsteren, W.F., Dinola, A. & Haak, J.R. Molecular dynamics with coupling to an external bath. J. Chem. Phys. 81, 3684-3690 (1984).
52. Darden, T., York, D. & Pedersen, L. Particle mesh Ewald: an N•log(N ) method for Ewald sums in large systems. J. Chem. Phys. 98, 10089-10092 (1993).
53. Humphrey, W., Dalke, A. & Schulten, K. VMD: visual molecular dynamics. J. Mol. Graph. 14, 33-38 (1996).