Tethered ligands reveal glutamate receptor desensitization depends on subunit occupancy

Nature Chemical Biology

Volumn 10, Issue 4, 2014, Pages 273-280

  Reiner, Andreas ^a   Isacoff, Ehud Y ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AZOBENZENE; CONCANAVALIN A; DIMER; GLUTAMATE RECEPTOR; GLUTAMATE RECEPTOR 2; GLUTAMATE RECEPTOR 5; GLUTAMIC ACID; IONOTROPIC RECEPTOR; KAINIC ACID RECEPTOR; LIGAND; LIGAND GATED ION CHANNEL; RECEPTOR SUBUNIT;

ARTICLE; BINDING AFFINITY; HUMAN; LIGAND BINDING; NERVE ENDING; NEUROTRANSMISSION; PHOTOACTIVATION; PRIORITY JOURNAL; RECEPTOR DOWN REGULATION; RECEPTOR OCCUPANCY; SYNAPSE; SYNAPTIC TRANSMISSION; VOLTAGE CLAMP TECHNIQUE;

ANIMALS; DATA INTERPRETATION, STATISTICAL; GLUTAMIC ACID; HEK293 CELLS; HUMANS; ION CHANNEL GATING; ION CHANNELS; KAINIC ACID; KINETICS; LIGANDS; LIGHT; NEURONAL PLASTICITY; PATCH-CLAMP TECHNIQUES; RATS; RECEPTORS, GLUTAMATE; SIGNAL TRANSDUCTION; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 84897024230     PISSN: 15524450     EISSN: 15524469     Source Type: Journal    
DOI: 10.1038/nchembio.1458     Document Type: Article

References (59)

1. Dingledine, R., Borges, K., Bowie, D. & Traynelis, S.F. The glutamate receptor ion channels. Pharmacol. Rev. 51, 7-61 (1999).
2. Traynelis, S.F. et al. Glutamate receptor ion channels: structure, regulation, and function. Pharmacol. Rev. 62, 405-496 (2010).
3. Contractor, A., Mulle, C. & Swanson, G.T. Kainate receptors coming of age: milestones of two decades of research. Trends Neurosci. 34, 154-163 (2011).
4. Lerma, J. & Marques, J.M. Kainate receptors in health and disease. Neuron 80, 292-311 (2013).
5. Mosbacher, J. et al. A molecular determinant for submillisecond desensitization in glutamate receptors. Science 266, 1059-1062 (1994).
6. Straub, C. & Tomita, S. The regulation of glutamate receptor trafficking and function by TARPs and other transmembrane auxiliary subunits. Curr. Opin. Neurobiol. 22, 488-495 (2012).
7. Christie, L.A. et al. AMPA receptor desensitization mutation results in severe developmental phenotypes and early postnatal lethality. Proc. Natl. Acad. Sci. USA 107, 9412-9417 (2010).
8. Rosenmund, C., Stern-Bach, Y. & Stevens, C.F. The tetrameric structure of a glutamate receptor channel. Science 280, 1596-1599 (1998).
9. 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).
10. Jin, R., Banke, T.G., Mayer, M.L., Traynelis, S.F. & Gouaux, E. Structural basis for partial agonist action at ionotropic glutamate receptors. Nat. Neurosci. 6, 803-810 (2003).
11. Mayer, M.L. Crystal structures of the GluR5 and GluR6 ligand binding cores: molecular mechanisms underlying kainate receptor selectivity. Neuron 45, 539-552 (2005).
12. 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).
13. Sun, Y. et al. Mechanism of glutamate receptor desensitization. Nature 417, 245-253 (2002).
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).
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).
16. Paternain, A.V., Cohen, A., Stern-Bach, Y. & Lerma, J. A role for extracellular Na+ in the channel gating of native and recombinant kainate receptors. J. Neurosci. 23, 8641-8648 (2003).
17. Plested, A.J. & Mayer, M.L. Structure and mechanism of kainate receptor modulation by anions. Neuron 53, 829-841 (2007).
18. 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).
19. Zhang, Y., Nayeem, N., Nanao, M.H. & Green, T. Interface interactions modulating desensitization of the kainate-selective ionotropic glutamate receptor subunit GluR6. J. Neurosci. 26, 10033-10042 (2006).
20. Dawe, G.B. et al. Defining the structural relationship between kainate-receptor deactivation and desensitization. Nat. Struct. Mol. Biol. 20, 1054-1061 (2013).
21. Smith, T.C. & Howe, J.R. Concentration-dependent substate behavior of native AMPA receptors. Nat. Neurosci. 3, 992-997 (2000).
22. Robert, A. & Howe, J.R. How AMPA receptor desensitization depends on receptor occupancy. J. Neurosci. 23, 847-858 (2003).
23. Robert, A., Irizarry, S.N., Hughes, T.E. & Howe, J.R. Subunit interactions and AMPA receptor desensitization. J. Neurosci. 21, 5574-5586 (2001).
24. Bowie, D. & Lange, G.D. Functional stoichiometry of glutamate receptor desensitization. J. Neurosci. 22, 3392-3403 (2002).
25. Swanson, G.T. et al. Differential activation of individual subunits in heteromeric kainate receptors. Neuron 34, 589-598 (2002).
26. Mott, D.D., Rojas, A., Fisher, J.L., Dingledine, R.J. & Benveniste, M. Subunit-specific desensitization of heteromeric kainate receptors. J. Physiol. (Lond.) 588, 683-700 (2010).
27. Fisher, J.L. & Mott, D.D. Distinct functional roles of subunits within the heteromeric kainate receptor. J. Neurosci. 31, 17113-17122 (2011).
28. Barberis, A., Sachidhanandam, S. & Mulle, C. GluR6/KA2 kainate receptors mediate slow-deactivating currents. J. Neurosci. 28, 6402-6406 (2008).
29. Heckmann, M., Bufler, J., Franke, C. & Dudel, J. Kinetics of homomeric GluR6 glutamate receptor channels. Biophys. J. 71, 1743-1750 (1996).
30. Jayaraman, V. Channel-opening mechanism of a kainate-activated glutamate receptor: kinetic investigations using a laser-pulse photolysis technique. Biochemistry 37, 16735-16740 (1998).
31. Li, G., Oswald, R.E. & Niu, L. Channel-opening kinetics of GluR6 kainate receptor. Biochemistry 42, 12367-12375 (2003).
32. Bartels, E., Wassermann, N.H. & Erlanger, B.F. Photochromic activators of the acetylcholine receptor. Proc. Natl. Acad. Sci. USA 68, 1820-1823 (1971).
33. Lester, H.A., Krouse, M.E., Nass, M.M., Wassermann, N.H. & Erlanger, B.F. A covalently bound photoisomerizable agonist: comparison with reversibly bound agonists at Electrophorus electroplaques. J. Gen. Physiol. 75, 207-232 (1980).
34. Volgraf, M. et al. Allosteric control of an ionotropic glutamate receptor with an optical switch. Nat. Chem. Biol. 2, 47-52 (2006).
35. Gorostiza, P. et al. Mechanisms of photoswitch conjugation and light activation of an ionotropic glutamate receptor. Proc. Natl. Acad. Sci. USA 104, 10865-10870 (2007).
36. Fehrentz, T., Schönberger, M. & Trauner, D. Optochemical genetics. Angew. Chem. 50, 12156-12182 (2011).
37. Levitz, J. et al. Optical control of metabotropic glutamate receptors. Nat. Neurosci. 16, 507-516 (2013).
38. Tochitsky, I. et al. Optochemical control of genetically engineered neuronal nicotinic acetylcholine receptors. Nat. Chem. 4, 105-111 (2012).
39. Kienzler, M.A. & Reiner, A. et al. A red-shifted, fast-relaxing azobenzene photoswitch for visible light control of an ionotropic glutamate receptor. J. Am. Chem. Soc. 135, 17683-17686 (2013).
40. Herb, A. et al. The KA-2 subunit of excitatory amino acid receptors shows widespread expression in brain and forms ion channels with distantly related subunits. Neuron 8, 775-785 (1992).
41. Wisden, W. & Seeburg, P.H. A complex mosaic of high-affinity kainate receptors in rat brain. J. Neurosci. 13, 3582-3598 (1993).
42. Contractor, A. et al. Loss of kainate receptor-mediated heterosynaptic facilitation of mossy-fiber synapses in KA2 mice. J. Neurosci. 23, 422-429 (2003).
43. Gallyas, F. Jr., Ball, S.M. & Molnar, E. Assembly and cell surface expression of KA-2 subunit-containing kainate receptors. J. Neurochem. 86, 1414-1427 (2003).
44. Ren, Z. et al. Multiple trafficking signals regulate kainate receptor KA2 subunit surface expression. J. Neurosci. 23, 6608-6616 (2003).
45. Nasu-Nishimura, Y. et al. Identification of an endoplasmic reticulum-retention motif in an intracellular loop of the kainate receptor subunit KA2. J. Neurosci. 26, 7014-7021 (2006).
46. Reiner, A., Arant, R.J. & Isacoff, E.Y. Assembly stoichiometry of the GluK2/GluK5 kainate receptor complex. Cell Rep. 1, 234-240 (2012).
47. Kumar, J., Schuck, P. & Mayer, M.L. Structure and assembly mechanism for heteromeric kainate receptors. Neuron 71, 319-331 (2011).
48. Swanson, G.T., Green, T. & Heinemann, S.F. Kainate receptors exhibit differential sensitivities to (S)-5-iodowillardiine. Mol. Pharmacol. 53, 942-949 (1998).
49. Cui, C. & Mayer, M.L. Heteromeric kainate receptors formed by the coassembly of GluR5, GluR6, and GluR7. J. Neurosci. 19, 8281-8291 (1999).
50. Pinheiro, P.S. et al. Selective block of postsynaptic kainate receptors reveals their function at hippocampal mossy fiber aynapses. Cereb. Cortex 23, 323-331 (2013).
51. Ma-Högemeier, Z.L. et al. Oligomerization in the endoplasmic reticulum and intracellular trafficking of kainate receptors are subunit-dependent but not editing-dependent. J. Neurochem. 113, 1403-1415 (2010).
52. Zhou, L.M. et al. (2S,4R)-4-methylglutamic acid (SYM 2081): a selective, high-affinity ligand for kainate receptors. J. Pharmacol. Exp. Ther. 280, 422-427 (1997).
53. Numano, R. et al. Nanosculpting reversed wavelength sensitivity into a photoswitchable iGluR. Proc. Natl. Acad. Sci. USA 106, 6814-6819 (2009).
54. Everts, I., Villmann, C. & Hollmann, M. N-Glycosylation is not a prerequisite for glutamate receptor function but is essential for lectin modulation. Mol. Pharmacol. 52, 861-873 (1997).
55. 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).
56. Jane, D.E. et al. Synthesis of willardiine and 6-azawillardiine analogs: pharmacological characterization on cloned homomeric human AMPA and kainate receptor subtypes. J. Med. Chem. 40, 3645-3650 (1997).
57. Jonas, P. Fast application of agonists to isolated membrane patches. In Single-Channel Recording (eds. Sakmann, B. & Neher, E.) 231-242 (Plemum Press, 1995).
58. Schwarz, G. Kinetic analysis by chemical relaxation methods. Rev. Mod. Phys. 40, 206-218 (1968).
59. Colquhoun, D. & Hawkes, A.G. A Q-matrix cookbook. In Single-Channel Recording (eds. Sakmann, B. & Neher, E.) 589-633 (Plenum Press, 1995).