Role of conformational dynamics in α-amino-3-hydroxy-5- methylisoxazole-4-propionic acid (AMPA) receptor partial agonism

Journal of Biological Chemistry

Volumn 287, Issue 52, 2012, Pages 43557-43564

  Ramaswamy, Swarna ^a   Cooper, David ^b   Poddar, Nitesh ^b   MacLean, David M ^a   Rambhadran, Anu ^a   Taylor, J Nick ^b   Uhm, Heui ^b   Landes, Christy F ^b   Jayaraman, Vasanthi ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^b RICE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPA-RECEPTOR; CHANNEL OPENING; CONFORMATIONAL DYNAMICS; CONFORMATIONAL STATE; MEAN CURRENTS; MUTANT PROTEINS; PROPIONIC ACIDS; SINGLE-MOLECULE; WILD TYPES;

DYNAMICS; MOLECULES; PROTEINS; SATURATED FATTY ACIDS;

CONFORMATIONS;

ALPHA AMINO 3 [(4 CARBOXYPHENYL)METHYL] 3,4 DIHYDRO 2,4 DIOXO 1 PYRIMIDINEPROPANOIC ACID; AMPA RECEPTOR; CHLOROWILLARDINE; NITROWILLARDINE; PROPIONIC ACID DERIVATIVE; UNCLASSIFIED DRUG; WILLARDIINE;

ARTICLE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; EMBRYO; FLUORESCENCE RESONANCE ENERGY TRANSFER; HUMAN; HUMAN CELL; MOLECULAR DYNAMICS; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DOMAIN; STRUCTURE ACTIVITY RELATION; WILD TYPE;

ALANINE; AMINO ACID SUBSTITUTION; FLUORESCENCE RESONANCE ENERGY TRANSFER; HEK293 CELLS; HUMANS; MUTATION, MISSENSE; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, AMPA; URACIL;

EID: 84871589157     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.371815     Document Type: Article

References (53)

1. Nakanishi, S. (1992) Molecular diversity of glutamate receptors and implications for brain function. Science 258, 597-603
2. Nakanishi, S., and Masu, M. (1994) Molecular diversity and functions of glutamate receptors. Annu. Rev. Biophys. Biomol. Struct. 23, 319-348 (Pubitemid 24217371)
3. Madden, D. R. (2002) The structure and function of glutamate receptor ion channels. Nat. Rev. Neurosci. 3, 91-101
4. McFeeters, R. L., and Oswald, R. E. (2004) Emerging structural explanations of ionotropic glutamate receptor function. FASEB J. 18, 428-438 (Pubitemid 38326300)
5. Valentine, E. R., and Palmer, A. G., 3rd. (2005) Microsecond-to- millisecond conformational dynamics demarcate the GluR2 glutamate receptor bound to agonists glutamate, quisqualate, and AMPA. Biochemistry 44, 3410-3417 (Pubitemid 40322011)
6. Oswald, R. E., Ahmed, A., Fenwick, M. K., and Loh, A. P. (2007) Structure of glutamate receptors. Curr. Drug Targets 8, 573-582 (Pubitemid 46785058)
7. 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
8. Sommer, B., and Seeburg, P. H. (1992) Glutamate receptor channels. Novel properties and new clones. Trends Pharmacol. Sci. 13, 291-296
9. Madsen, U., Ebert, B., and Krogsgaard-Larsen, P. (1994) Modulation of AMPA receptor function in relation to glutamatergic abnormalities in Alzheimer's disease. Biomed. Pharmacother. 48, 305-311 (Pubitemid 24304994)
10. Zamanillo, D., Sprengel, R., Hvalby, O., Jensen, V., Burnashev, N., Rozov, A., Kaiser, K. M., Köster, H. J., Borchardt, T., Worley, P., Lübke, J., Frotscher, M., Kelly, P. H., Sommer, B., Andersen, P., Seeburg, P. H., and Sakmann, B. (1999) Importance of AMPA receptors for hippocampal synaptic plasticity but not for spatial learning. Science 284, 1805-1811
11. Kwak, S., and Kawahara, Y. (2005) Deficient RNA editing of GluR2 and neuronal death in amyotropic lateral sclerosis. J. Mol. Med. 83, 110-120 (Pubitemid 40379299)
12. Shepherd, J. D., and Huganir, R. L. (2007) The cell biology of synaptic plasticity. AMPA receptor trafficking. Annu. Rev. Cell Dev. Biol. 23, 613-643
13. O'Neill, M. J., and Witkin, J. M. (2007) AMPA receptor potentiators. Application for depression and Parkinson's disease. Curr. Drug Targets 8, 603-620 (Pubitemid 46794920)
14. Johnson, K. A., Conn, P. J., and Niswender, C. M. (2009) Glutamate receptors as therapeutic targets for Parkinson's disease. CNS Neurol. Disord. Drug Targets 8, 475-491
15. Keifer, J., and Zheng, Z. (2010) AMPA receptor trafficking and learning. Eur. J. Neurosci. 32, 269-277
16. 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
17. Du, M., Reid, S. A., and Jayaraman, V. (2005) Conformational changes in the ligand-binding domain of a functional ionotropic glutamate receptor. J. Biol. Chem. 280, 8633-8636 (Pubitemid 40409548)
18. Gonzalez, J., Rambhadran, A., Du, M., and Jayaraman, V. (2008) LRET investigations of conformational changes in the ligand binding domain of a functional AMPA receptor. Biochemistry 47, 10027-10032
19. Gonzalez, J., Du, M., Parameshwaran, K., Suppiramaniam, V., and Jayaraman, V. (2010) Role of dimer interface in activation and desensitization in AMPA receptors. Proc. Natl. Acad. Sci. U.S.A. 107, 9891-9896
20. Armstrong, N., Sun, Y., Chen, G. Q., and Gouaux, E. (1998) Structure of a glutamate-receptor ligand-binding core in complex with kainate. Nature 395, 913-917 (Pubitemid 28503434)
21. Armstrong, N., and Gouaux, E. (2000) Mechanisms for activation and antagonism of an AMPA-sensitive glutamate receptor. Crystal structures of the GluR2 ligand binding core. Neuron 28, 165-181
22. Armstrong, N., Mayer, M., and Gouaux, E. (2003) Tuning activation of the AMPA-sensitive GluR2 ion channel by genetic adjustment of agonist-induced conformational changes. Proc. Natl. Acad. Sci. U.S.A. 100, 5736-5741 (Pubitemid 36576877)
23. Gouaux, E. (2004) Structure and function of AMPA receptors. J. Physiol. 554, 249-253
24. Ahmed, A. H., Wang, Q., Sondermann, H., and Oswald, R. E. (2009) Structure of the S1S2 glutamate binding domain of GLuR3. Proteins 75, 628-637
25. Birdsey-Benson, A., Gill, A., Henderson, L. P., and Madden, D. R. (2010) Enhanced efficacy without further cleft closure. Reevaluating twist as a source of agonist efficacy in AMPA receptors. J. Neurosci. 30, 1463-1470
26. Robert, A., Armstrong, N., Gouaux, J. E., and Howe, J. R. (2005) AMPA receptor binding cleft mutations that alter affinity, efficacy, and recovery from desensitization. J. Neurosci. 25, 3752-3762 (Pubitemid 40570408)
27. Zhang, W., Cho, Y., Lolis, E., and Howe, J. R. (2008) 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 (Pubitemid 351158996)
28. Mankiewicz, K. A., Rambhadran, A., Wathen, L., and Jayaraman, V. (2008) Chemical interplay in the mechanism of partial agonist activation in α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptors. Biochemistry 47, 398-404
29. Ramanoudjame, G., Du, M., Mankiewicz, K. A., and Jayaraman, V. (2006) Allosteric mechanism inAMPAreceptors. A FRET-based investigation of conformational changes. Proc. Natl. Acad. Sci. U.S.A. 103, 10473-10478 (Pubitemid 44051191)
30. Landes, C. F., Rambhadran, A., Taylor, J. N., Salatan, F., and Jayaraman, V. (2011) Structural landscape of isolated agonist-binding domains from single AMPA receptors. Nat. Chem. Biol. 7, 168-173
31. Fenwick, M. K., and Oswald, R. E. (2008)NMRspectroscopy of the ligand-binding core of ionotropic glutamate receptor 2 bound to 5-substituted willardiine partial agonists. J. Mol. Biol. 378, 673-685
32. Maltsev, A. S., and Oswald, R. E. (2010) Hydrophobic side chain dynamics of a glutamate receptor ligand binding domain. J. Biol. Chem. 285, 10154-10162
33. Karam, P., Ngo, A. T., Rouiller, I., and Cosa, G. (2010) Unraveling electronic energy transfer in single conjugated polyelectrolytes encapsulated in lipid vesicles. Proc. Natl. Acad. Sci. U.S.A. 107, 17480-17485
34. Vogelsang, J., Doose, S., Sauer, M., and Tinnefeld, P. (2007) Single-molecule fluorescence resonance energy transfer in nanopipets. Improving distance resolution and concentration range. Anal. Chem. 79, 7367-7375 (Pubitemid 47606103)
35. Darugar, Q., Kim, H., Gorelick, R. J., and Landes, C. (2008) Human T-cell lympotropic virus type 1 nucleocapsid protein-induced structural changes in transactivation response DNA measured by single molecule fluorescence resonance energy transfer. J. Virol. 82, 12164-12171
36. Taylor, J. N., Darugar, Q., Kourentzi, K., Willson, R. C., and Landes, C. F. (2008) Dynamics of an anti-VEGF aptamer. A single molecule study. Biochem. Biophys. Res. Commun. 373, 213-218
37. Taylor, J. N., Makarov, D. E., and Landes, C. F. (2010) Denoising single-molecule FRET trajectories with wavelets and Bayesian inference. Biophys. J. 98, 164-173
38. Taylor, J. N., and Landes, C. F. (2011) Improved resolution of complex single-molecule FRET systems via wavelet shrinkage. J. Phys. Chem. B 115, 1105-1114
39. Poon, K., Ahmed, A. H., Nowak, L. M., and Oswald, R. E. (2011) Mechanisms of modal activation of GluA3 receptors. Mol. Pharmacol. 80, 49-59
40. Jayaraman, V., Keesey, R., and Madden, D. R. (2000) Ligand-protein interactions in the glutamate receptor. Biochemistry 39, 8693-8697 (Pubitemid 30602777)
41. Jayaraman, V., Thiran, S., and Madden, D. R. (2000) Fourier transform infrared spectroscopic characterization of a photolabile precursor of glutamate. FEBS Lett. 475, 278-282 (Pubitemid 30408468)
42. Madden, D. R., Thiran, S., Zimmermann, H., Romm, J., and Jayaraman, V. (2001) Stereochemistry of quinoxaline antagonist binding to a glutamate receptor investigated by Fourier transform infrared spectroscopy. J. Biol. Chem. 276, 37821-37826
43. Madden, D. R., Cheng, Q., Thiran, S., Rajan, S., Rigo, F., Keinänen, K., Reinelt, S., Zimmermann, H., and Jayaraman, V. (2004) Stereochemistry of glutamate receptor agonist efficacy. Engineering a dual-specificity AMPA/kainate receptor. Biochemistry 43, 15838-15844 (Pubitemid 39665082)
44. Jayaraman, V. (2004) Spectroscopic and kinetic methods for ligand-protein interactions of glutamate receptor. Methods Enzymol. 380, 170-187
45. Cheng, Q., Du, M., Ramanoudjame, G., and Jayaraman, V. (2005) Evolution of glutamate interactions during binding to a glutamate receptor. Nat. Chem. Biol. 1, 329-332
46. Mankiewicz, K. A., and Jayaraman, V. (2007) Glutamate receptors as seen by light. Spectroscopic studies of structure-function relationships. Braz. J. Med. Biol. Res. 40, 1419-1427 (Pubitemid 350302853)
47. McFeeters, R. L., and Oswald, R. E. (2002) Structural mobility of the extracellular ligand-binding core of an ionotropic glutamate receptor. Analysis of NMR relaxation dynamics. Biochemistry 41, 10472-10481
48. Ahmed, A. H., Loh, A. P., Jane, D. E., and Oswald, R. E. (2007) Dynamics of the S1S2 glutamate binding domain of GluR2 measured using 19F NMR spectroscopy. J. Biol. Chem. 282, 12773-12784 (Pubitemid 47100589)
49. Maltsev, A. S., Ahmed, A. H., Fenwick, M. K., Jane, D. E., and Oswald, R. E. (2008) Mechanism of partial agonism at the GluR2 AMPA receptor. Measurements of lobe orientation in solution. Biochemistry 47, 10600-10610
50. Jin, R., Banke, T. G., Mayer, M. L., Traynelis, S. F., and Gouaux, E. (2003) Structural basis for partial agonist action at ionotropic glutamate receptors. Nat. Neurosci. 6, 803-810 (Pubitemid 36929700)
51. Ahmed, A. H., Wang, S., Chuang, H. H., and Oswald, R. E. (2011) Mechanism of AMPA receptor activation by partial agonists. Disulfide trapping of closed lobe conformations. J. Biol. Chem. 286, 35257-35266
52. Maclean, D. M., Wong, A. Y., Fay, A. M., and Bowie, D. (2011) Cations but not anions regulate the responsiveness of kainate receptors. J. Neurosci. 31, 2136-2144
53. Ahmed, A. H., Thompson, M. D., Fenwick, M. K., Romero, B., Loh, A. P., Jane, D. E., Sondermann, H., and Oswald, R. E. (2009) Mechanisms of antagonism of the GluR2 AMPA receptor. Structure and dynamics of the complex of two willardiine antagonists with the glutamate binding domain. Biochemistry 48, 3894-3903