Stargazin promotes closure of the AMPA receptor ligand-binding domain

Journal of General Physiology

Volumn 144, Issue 6, 2014, Pages 503-512

  MacLean, David M ^a   Ramaswamy, Swarna S ^a   Du, Mei ^a   Howe, James R ^b   Jayaraman, Vasanthi ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPA RECEPTOR; CACNG2 PROTEIN, HUMAN; CALCIUM CHANNEL; LIGAND; PROTEIN BINDING;

CELL MEMBRANE PERMEABILITY; CHANNEL GATING; CHEMISTRY; HEK293 CELL LINE; HUMAN; METABOLISM; PHYSIOLOGY; PROTEIN CONFORMATION; PROTEIN TERTIARY STRUCTURE; ULTRASTRUCTURE;

CALCIUM CHANNELS; CELL MEMBRANE PERMEABILITY; HEK293 CELLS; HUMANS; ION CHANNEL GATING; LIGANDS; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, AMPA;

EID: 84918506500     PISSN: 00221295     EISSN: 15407748     Source Type: Journal    
DOI: 10.1085/jgp.201411287     Document Type: Article

References (45)

1. Armstrong, N., and E. Gouaux. 2000. Mechanisms for activation and antagonism of an AMPA-sensitive glutamate receptor: Crystal structures of the GluR2 ligand binding core. Neuron. 28:165-181. http://dx.doi.org/10.1016/S0896-6273(00)00094-5
2. Armstrong, N., M. Mayer, and E. Gouaux. 2003. Tuning activation of the AMPA-sensitive GluR2 ion channel by genetic adjustment of agonist-induced conformational changes. Proc. Natl. Acad. Sci. USA. 100:5736-5741. http://dx.doi.org/10.1073/pnas .1037393100
3. Cho, C.H., F. St-Gelais, W. Zhang, S. Tomita, and J.R. Howe. 2007. Two families of TARP isoforms that have distinct effects on the kinetic properties of AMPA receptors and synaptic currents. Neuron. 55:890-904. http://dx.doi.org/10.1016/j.neuron.2007.08.024
4. Cokic, B., and V. Stein. 2008. Stargazin modulates AMPA receptor antagonism. Neuropharmacology. 54:1062-1070. http://dx.doi.org/ 10.1016/j.neuropharm.2008.02.012
5. Coombs, I.D., D. Soto, M. Zonouzi, M. Renzi, C. Shelley, M. Farrant, and S.G. Cull-Candy. 2012. Cornichons modify channel properties of recombinant and glial AMPA receptors. J. Neurosci. 32:9796- 9804. http://dx.doi.org/10.1523/JNEUROSCI.0345-12.2012
6. Copits, B.A., J.S. Robbins, S. Frausto, and G.T. Swanson. 2011. Synaptic targeting and functional modulation of GluK1 kainate receptors by the auxiliary neuropilin and tolloid-like (NETO) proteins. J. Neurosci. 31:7334-7340. http://dx.doi.org/10.1523/ JNEUROSCI.0100-11.2011
7. dos Remedios, C.G., and P.D. Moens. 1995. Fluorescence resonance energy transfer spectroscopy is a reliable "ruler" for measuring structural changes in proteins. Dispelling the problem of the unknown orientation factor. J. Struct. Biol. 115:175-185. http://dx.doi .org/10.1006/jsbi.1995.1042
8. Du, M., S.A. Reid, and V. Jayaraman. 2005. Conformational changes in the ligand-binding domain of a functional ionotropic glutamate receptor. J. Biol. Chem. 280:8633-8636. http://dx.doi.org/10 .1074/jbc.C400590200
9. Gonzalez, J., A. Rambhadran, M. Du, and V. Jayaraman. 2008. LRET investigations of conformational changes in the ligand binding domain of a functional AMPA receptor. Biochemistry. 47:10027- 10032. http://dx.doi.org/10.1021/bi800690b
10. Hollmann, M., A. O'Shea-Greenfield, S.W. Rogers, and S. Heinemann. 1989. Cloning by functional expression of a member of the glutamate receptor family. Nature. 342:643-648. http://dx.doi.org/ 10.1038/342643a0
11. Howe, J.R. 2013. CrossTalk proposal: TARPs modulate AMPA receptor gating transitions. J. Physiol. 591:1581-1583. http://dx.doi .org/10.1113/jphysiol.2012.247486
12. Jin, R., T.G. Banke, M.L. Mayer, S.F. Traynelis, and E. Gouaux. 2003. Structural basis for partial agonist action at ionotropic glutamate receptors. Nat. Neurosci. 6:803-810. http://dx.doi.org/10.1038/ nn1091
13. Jones, M.V., Y. Sahara, J.A. Dzubay, and G.L. Westbrook. 1998. Defining affinity with the GABAA receptor. J. Neurosci. 18:8590-8604.
14. Körber, C., M. Werner, S. Kott, Z.L. Ma, and M. Hollmann. 2007. The transmembrane AMPA receptor regulatory protein gamma 4 is a more effective modulator of AMPA receptor function than stargazin (gamma 2). J. Neurosci. 27:8442-8447. http://dx.doi.org/10.1523/ JNEUROSCI.0424-07.2007
15. Kott, S., M. Werner, C. Körber, and M. Hollmann. 2007. Electrophysiological properties of AMPA receptors are differentially modulated depending on the associated member of the TARP family. J. Neurosci. 27:3780-3789. http://dx.doi.org/10.1523/ JNEUROSCI.4185-06.2007
16. Landes, C.F., A. Rambhadran, J.N. Taylor, F. Salatan, and V. Jayaraman. 2011. Structural landscape of isolated agonist-binding domains from single AMPA receptors. Nat. Chem. Biol. 7:168-173. http:// dx.doi.org/10.1038/nchembio.523
17. Lau, A.Y., and B. Roux. 2011. The hidden energetics of ligand binding and activation in a glutamate receptor. Nat. Struct. Mol. Biol. 18:283-287. http://dx.doi.org/10.1038/nsmb.2010
18. Lau, A.Y., H. Salazar, L. Blachowicz, V. Ghisi, A.J. Plested, and B. Roux. 2013. A conformational intermediate in glutamate receptor activation. Neuron. 79:492-503. http://dx.doi.org/10.1016/j .neuron.2013.06.003
19. Lomeli, H., J. Mosbacher, T. Melcher, T. Höger, J.R. Geiger, T. Kuner, H. Monyer, M. Higuchi, A. Bach, and P.H. Seeburg. 1994. Control of kinetic properties of AMPA receptor channels by nuclear RNA editing. Science. 266:1709-1713. http://dx.doi.org/ 10.1126/science.7992055
20. MacLean, D.M. 2013. CrossTalk opposing view: TARPs modulate AMPA receptor conformations before the gating transitions. J. Physiol. 591:1585-1586. http://dx.doi.org/10.1113/jphysiol.2012.247726
21. Maclean, D.M., and D. Bowie. 2011. Transmembrane AMPA receptor regulatory protein regulation of competitive antagonism: a problem of interpretation. J. Physiol. 589:5383-5390.
22. Menuz, K., R.M. Stroud, R.A. Nicoll, and F.A. Hays. 2007. TARP auxiliary subunits switch AMPA receptor antagonists into partial agonists. Science. 318:815-817. http://dx.doi.org/10.1126/science.1146317
23. Menuz, K., J.L. O'Brien, S. Karmizadegan, D.S. Bredt, and R.A. Nicoll. 2008. TARP redundancy is critical for maintaining AMPA receptor function. J. Neurosci. 28:8740-8746. http://dx.doi.org/10 .1523/JNEUROSCI.1319-08.2008
24. Menuz, K., G.A. Kerchner, J.L. O'Brien, and R.A. Nicoll. 2009. Critical role for TARPs in early development despite broad functional redundancy. Neuropharmacology. 56:22-29. http://dx.doi.org/10 .1016/j.neuropharm.2008.06.037
25. Meyerson, J.R., J. Kumar, S. Chittori, P. Rao, J. Pierson, A. Bartesaghi, M.L. Mayer, and S. Subramaniam. 2014. Structural mechanism of glutamate receptor activation and desensitization. Nature. 514: 328-334. http://dx.doi.org/10.1038/nature13603
26. Priel, A., A. Kolleker, G. Ayalon, M. Gillor, P. Osten, and Y. Stern-Bach. 2005. Stargazin reduces desensitization and slows deactivation of the AMPA-type glutamate receptors. J. Neurosci. 25:2682-2686. http://dx.doi.org/10.1523/JNEUROSCI.4834-04.2005
27. Ramanoudjame, G., M. Du, K.A. Mankiewicz, and V. Jayaraman. 2006. Allosteric mechanism in AMPA receptors: A FRET-based investigation of conformational changes. Proc. Natl. Acad. Sci. USA. 103:10473-10478. http://dx.doi.org/10.1073/pnas.0603225103
28. Ramaswamy, S., D. Cooper, N. Poddar, D.M. MacLean, A. Rambhadran, J.N. Taylor, H. Uhm, C.F. Landes, and V. Jayaraman. 2012. Role of conformational dynamics in α-amino-3-hydroxy-5-methylisoxazole- 4-propionic acid (AMPA) receptor partial agonism. J. Biol. Chem. 287:43557-43564. http://dx.doi.org/10.1074/jbc.M112.371815
29. Rambhadran, A., J. Gonzalez, and V. Jayaraman. 2011. Conformational changes at the agonist binding domain of the N-methyl-d-aspartic acid receptor. J. Biol. Chem. 286:16953-16957. http://dx.doi.org/ 10.1074/jbc.M111.224576
30. Robert, A., N. Armstrong, J.E. Gouaux, and J.R. Howe. 2005. AMPA receptor binding cleft mutations that alter affinity, efficacy, and recovery from desensitization. J. Neurosci. 25:3752-3762. http:// dx.doi.org/10.1523/JNEUROSCI.0188-05.2005
31. Schnell, E., M. Sizemore, S. Karimzadegan, L. Chen, D.S. Bredt, and R.A. Nicoll. 2002. Direct interactions between PSD-95 and stargazin control synaptic AMPA receptor number. Proc. Natl. Acad. Sci. USA. 99:13902-13907. http://dx.doi.org/10.1073/pnas .172511199
32. Schwenk, J., N. Harmel, G. Zolles, W. Bildl, A. Kulik, B. Heimrich, O. Chisaka, P. Jonas, U. Schulte, B. Fakler, and N. Klöcker. 2009. Functional proteomics identify cornichon proteins as auxiliary subunits of AMPA receptors. Science. 323:1313-1319. http://dx .doi.org/10.1126/science.1167852
33. Shanks, N.F., J.N. Savas, T. Maruo, O. Cais, A. Hirao, S. Oe, A. Ghosh, Y. Noda, I.H. Greger, J.R. Yates III, and T. Nakagawa. 2012. Differences in AMPA and kainate receptor interactomes facilitate identification of AMPA receptor auxiliary subunit GSG1L. Cell Reports. 1:590-598. http://dx.doi.org/10.1016/j.celrep.2012 .05.004
34. Shelley, C., M. Farrant, and S.G. Cull-Candy. 2012. TARP-associated AMPA receptors display an increased maximum channel conductance and multiple kinetically distinct open states. J. Physiol. 590:5723-5738. http://dx.doi.org/10.1113/jphysiol.2012.238006
35. Sirrieh, R.E., D.M. MacLean, and V. Jayaraman. 2013. Amino-terminal domain tetramer organization and structural effects of zinc binding in the N-methyl-d-aspartate (NMDA) receptor. J. Biol. Chem. 288:22555-22564. http://dx.doi.org/10.1074/jbc.M113.482356
36. Sommer, B., K. Keinänen, T.A. Verdoorn, W. Wisden, N. Burnashev, A. Herb, M. Köhler, T. Takagi, B. Sakmann, and P.H. Seeburg. 1990. Flip and flop: a cell-specific functional switch in glutamateoperated channels of the CNS. Science. 249:1580-1585. http:// dx.doi.org/10.1126/science.1699275
37. Sommer, B., M. Köhler, R. Sprengel, and P.H. Seeburg. 1991. RNA editing in brain controls a determinant of ion flow in glutamategated channels. Cell. 67:11-19. http://dx.doi.org/10.1016/0092- 8674(91)90568-J
38. Soto, D., I.D. Coombs, E. Gratacòs-Batlle, M. Farrant, and S.G. Cull-Candy. 2014. Molecular mechanisms contributing to TARP regulation of channel conductance and polyamine block of calcium- permeable AMPA receptors. J. Neurosci. 34:11673-11683. http://dx.doi.org/10.1523/JNEUROSCI.0383-14.2014
39. Tomita, S., H. Adesnik, M. Sekiguchi, W. Zhang, K. Wada, J.R. Howe, R.A. Nicoll, and D.S. Bredt. 2005. Stargazin modulates AMPA receptor gating and trafficking by distinct domains. Nature. 435:1052-1058. http://dx.doi.org/10.1038/nature03624
40. von Engelhardt, J., V. Mack, R. Sprengel, N. Kavenstock, K.W. Li, Y. Stern-Bach, A.B. Smit, P.H. Seeburg, and H. Monyer. 2010. CKAMP44: A brain-specific protein attenuating short-term synaptic plasticity in the dentate gyrus. Science. 327:1518-1522. http:// dx.doi.org/10.1126/science.1184178
41. Yao, Y., J. Belcher, A.J. Berger, M.L. Mayer, and A.Y. Lau. 2013. Conformational analysis of NMDA receptor GluN1, GluN2, and GluN3 ligand-binding domains reveals subtype-specific characteristics. Structure. 21:1788-1799. http://dx.doi.org/10.1016/j.str .2013.07.011
42. Zhang, W., Y. Cho, E. Lolis, and J.R. Howe. 2008. Structural and singlechannel results indicate that the rates of ligand binding domain closing and opening directly impact AMPA receptor gating. J. Neurosci. 28:932-943. http://dx.doi.org/10.1523/JNEUROSCI.3309-07.2008
43. Zhang, W., F. St-Gelais, C.P. Grabner, J.C. Trinidad, A. Sumioka, M. Morimoto-Tomita, K.S. Kim, C. Straub, A.L. Burlingame, J.R. Howe, and S. Tomita. 2009. A transmembrane accessory subunit that modulates kainate-type glutamate receptors. Neuron. 61:385- 396. http://dx.doi.org/10.1016/j.neuron.2008.12.014
44. Zhang, W., S.P. Devi, S. Tomita, and J.R. Howe. 2014. Auxiliary proteins promote modal gating of AMPA- and kainate-type glutamate receptors. Eur. J. Neurosci. 39:1138-1147. http://dx.doi.org/10.1111/ejn .12519
45. Zheng, F., K. Erreger, C.M. Low, T. Banke, C.J. Lee, P.J. Conn, and S.F. Traynelis. 2001. Allosteric interaction between the amino terminal domain and the ligand binding domain of NR2A. Nat. Neurosci. 4:894-901. http://dx.doi.org/10.1038/ nn0901-894