Conformational Transitions in the Glycine-Bound GluN1 NMDA Receptor LBD via Single-Molecule FRET

Biophysical Journal

Volumn 109, Issue 1, 2015, Pages 66-75

  Cooper, David R ^a   Dolino, Drew M ^c   Jaurich, Henriette ^a   Shuang, Bo ^a   Ramaswamy, Swarna ^c   Nurik, Caitlin E ^c   Chen, Jixin ^a,d   Jayaraman, Vasanthi ^c   Landes, Christy F ^a,b  

^a RICE UNIVERSITY   (United States)

^b Rice University   (United States)

^c UNIVERSITY OF TEXAS   (United States)

^d OHIO UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCINE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ALGORITHM; ANISOTROPY; BINDING SITE; ESCHERICHIA COLI; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENETICS; KINETICS; METABOLISM; MOLECULAR MODEL; MUTATION; PROCEDURES; PROTEIN CONFORMATION; PROTEIN DENATURATION;

ALGORITHMS; ANISOTROPY; BINDING SITES; ESCHERICHIA COLI; FLUORESCENCE RESONANCE ENERGY TRANSFER; GLYCINE; KINETICS; MODELS, MOLECULAR; MUTATION; PROTEIN CONFORMATION; PROTEIN DENATURATION; RECEPTORS, N-METHYL-D-ASPARTATE;

EID: 84936758937     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2015.05.025     Document Type: Article

References (65)

1. P.E. Chen, and D.J.A. Wyllie Pharmacological insights obtained from structure-function studies of ionotropic glutamate receptors Br. J. Pharmacol. 147 2006 839 853
2. K.A. Johnson, P.J. Conn, and C.M. Niswender Glutamate receptors as therapeutic targets for Parkinson's disease CNS Neurol. Disord. Drug Targets 8 2009 475 491
3. U. Madsen, B. Ebert, and P. Krogsgaard-Larsen Modulation of AMPA receptor function in relation to glutamatergic abnormalities in Alzheimer's disease Biomed. Pharmacother. 48 1994 305 311
4. H.W. Querfurth, and F.M. LaFerla Alzheimer's disease N. Engl. J. Med. 362 2010 329 344
5. S. Sase, and D. Khan G. Lubec Modafinil improves performance in the multiple T-maze and modifies GluR1, GluR2, D2 and NR1 receptor complex levels in the C57BL/6J mouse Amino Acids 43 2012 2285 2292
6. D. Zamanillo, and R. Sprengel B. Sakmann Importance of AMPA receptors for hippocampal synaptic plasticity but not for spatial learning Science 284 1999 1805 1811
7. R. Dingledine, and K. Borges S.F. Traynelis The glutamate receptor ion channels Pharmacol. Rev. 51 1999 7 61
8. M.L. Mayer Glutamate receptor ion channels Curr. Opin. Neurobiol. 15 2005 282 288
9. P. Paoletti, and J. Neyton NMDA receptor subunits: function and pharmacology Curr. Opin. Pharmacol. 7 2007 39 47
10. D.B. Reichling, and A.B. MacDermott NMDA receptor-mediated calcium entry in the absence of AMPA receptor activation in rat dorsal horn neurons Neurosci. Lett. 204 1996 17 20
11. H. Sun, and Y. Kawahara S. Kwak Expression profile of AMPA receptor subunit mRNA in single adult rat brain and spinal cord neurons in situ Neurosci. Res. 52 2005 228 234
12. M.H. Ulbrich, and E.Y. Isacoff Rules of engagement for NMDA receptor subunits Proc. Natl. Acad. Sci. USA 105 2008 14163 14168
13. M.L. Mayer, L. Vyklicky Jr., and J. Clements Regulation of NMDA receptor desensitization in mouse hippocampal neurons by glycine Nature 338 1989 425 427
14. S.F. Traynelis, and L.P. Wollmuth R. Dingledine Glutamate receptor ion channels: structure, regulation, and function Pharmacol. Rev. 62 2010 405 496
15. E. Karakas, and H. Furukawa Crystal structure of a heterotetrameric NMDA receptor ion channel Science 344 2014 992 997
16. C.H. Lee, and W. Lü E. Gouaux NMDA receptor structures reveal subunit arrangement and pore architecture Nature 511 2014 191 197
17. M.L. Mayer Glutamate receptors at atomic resolution Nature 440 2006 456 462
18. A. Rambhadran, J. Gonzalez, and V. Jayaraman Subunit arrangement in N-methyl-D-aspartate (NMDA) receptors J. Biol. Chem. 285 2010 15296 15301
19. J. Dai, and H.-X. Zhou An NMDA receptor gating mechanism developed from MD simulations reveals molecular details underlying subunit-specific contributions Biophys. J. 104 2013 2170 2181
20. A.B. MacDermott, and M.L. Mayer J.L. Barker NMDA-receptor activation increases cytoplasmic calcium concentration in cultured spinal cord neurones Nature 321 1986 519 522
21. D. Lemoine, and R. Jiang T. Grutter Ligand-gated ion channels: new insights into neurological disorders and ligand recognition Chem. Rev. 112 2012 6285 6318
22. S.J. Myers, R. Dingledine, and K. Borges Genetic regulation of glutamate receptor ion channels Annu. Rev. Pharmacol. Toxicol. 39 1999 221 241
23. K. Speranskiy, and M. Kurnikova On the binding determinants of the glutamate agonist with the glutamate receptor ligand binding domain Biochemistry 44 2005 11508 11517
24. H. Furukawa, and E. Gouaux Mechanisms of activation, inhibition and specificity: crystal structures of the NMDA receptor NR1 ligand-binding core EMBO J. 22 2003 2873 2885
25. A. Inanobe, H. Furukawa, and E. Gouaux Mechanism of partial agonist action at the NR1 subunit of NMDA receptors Neuron 47 2005 71 84
26. M. Ylilauri, and O.T. Pentikäinen Structural mechanism of N-methyl-D-aspartate receptor type 1 partial agonism PLoS ONE 7 2012 e47604
27. C.L. Kussius, and G.K. Popescu Kinetic basis of partial agonism at NMDA receptors Nat. Neurosci. 12 2009 1114 1120
28. C.L. Kussius, and G.K. Popescu NMDA receptors with locked glutamate-binding clefts open with high efficacy J. Neurosci. 30 2010 12474 12479
29. M.A. Paganelli, C.L. Kussius, and G.K. Popescu Role of cross-cleft contacts in NMDA receptor gating PLoS ONE 8 2013 e80953
30. B. Foucaud, and B. Laube H. Betz Structural model of the N-methyl-D-aspartate receptor glycine site probed by site-directed chemical coupling J. Biol. Chem. 278 2003 24011 24017
31. S.A. Amico-Ruvio, and G.K. Popescu Stationary gating of GluN1/GluN2B receptors in intact membrane patches Biophys. J. 98 2010 1160 1169
32. W. Zhang, J.R. Howe, and G.K. Popescu Distinct gating modes determine the biphasic relaxation of NMDA receptor currents Nat. Neurosci. 11 2008 1373 1375
33. R. Abele, K. Keinanen, and D.R. Madden Agonist-induced isomerization in a glutamate receptor ligand-binding domain. A kinetic and mutagenetic analysis J. Biol. Chem. 275 2000 21355 21363
34. R.L. McFeeters, and R.E. Oswald Emerging structural explanations of ionotropic glutamate receptor function FASEB J. 18 2004 428 438
35. C.F. Landes, and A. Rambhadran V. Jayaraman Structural landscape of isolated agonist-binding domains from single AMPA receptors Nat. Chem. Biol. 7 2011 168 173
36. S. Ramaswamy, and D. Cooper V. Jayaraman Role of conformational dynamics in α-amino-3-hydroxy-5-methylisoxazole-4-propionic acid (AMPA) receptor partial agonism J. Biol. Chem. 287 2012 43557 43564
37. D.M. Dolino, and D. Cooper V. Jayaraman Structural dynamics of the glycine-binding domain of the N-methyl-D-aspartate receptor J. Biol. Chem. 290 2015 797 804
38. Y. Yao, and J. Belcher A.Y. Lau Conformational analysis of NMDA receptor GluN1, GluN2, and GluN3 ligand-binding domains reveals subtype-specific characteristics Structure 21 2013 1788 1799
39. B. Schuler, and W.A. Eaton Protein folding studied by single-molecule FRET Curr. Opin. Struct. Biol. 18 2008 16 26
40. P.A. Postila, M. Ylilauri, and O.T. Pentikäinen Full and partial agonism of ionotropic glutamate receptors indicated by molecular dynamics simulations J. Chem. Inf. Model. 51 2011 1037 1047
41. J.W.F. Robertson, J.J. Kasianowicz, and S. Banerjee Analytical approaches for studying transporters, channels and porins Chem. Rev. 112 2012 6227 6249
42. E. Braselmann, J.L. Chaney, and P.L. Clark Folding the proteome Trends Biochem. Sci. 38 2013 337 344
43. D. Baker, and D.A. Agard Kinetics versus thermodynamics in protein folding Biochemistry 33 1994 7505 7509
44. M.B. Borgia, and A. Borgia J. Clarke Single-molecule fluorescence reveals sequence-specific misfolding in multidomain proteins Nature 474 2011 662 665
45. H.S. Chung, and K. McHale W.A. Eaton Single-molecule fluorescence experiments determine protein folding transition path times Science 335 2012 981 984
46. Q. Darugar, and H. Kim C. Landes Human T-cell lymphotropic virus type 1 nucleocapsid protein-induced structural changes in transactivation response DNA hairpin measured by single-molecule fluorescence resonance energy transfer J. Virol. 82 2008 12164 12171
47. B. Schuler Single-molecule FRET of protein structure and dynamics - a primer J. Nanobiotechnol. 11 Suppl 1 2013 S2
48. J.D. Clements, and G.L. Westbrook Activation kinetics reveal the number of glutamate and glycine binding sites on the N-methyl-D-aspartate receptor Neuron 7 1991 605 613
49. A. Dutta, and I.H. Shrivastava I. Bahar Comparative dynamics of NMDA- and AMPA-glutamate receptor N-terminal domains Structure 20 2012 1838 1849
50. D. Cooper, and H. Uhm C.F. Landes Photobleaching lifetimes of cyanine fluorophores used for single-molecule Förster resonance energy transfer in the presence of various photoprotection systems ChemBioChem 14 2013 1075 1080
51. B. Shuang, and D. Cooper C.F. Landes Fast step transition and state identification (STaSI) for discrete single-molecule data analysis J. Phys. Chem. Lett 5 2014 3157 3161
52. J. Vogelsang, and R. Kasper P. Tinnefeld A reducing and oxidizing system minimizes photobleaching and blinking of fluorescent dyes Angew. Chem. Int. Ed. Engl. 47 2008 5465 5469
53. 2+ for extended single-molecule imaging: old tricks for new techniques J. Am. Chem. Soc. 137 2015 1116 1122
54. A.Y. Lau, and B. Roux The free energy landscapes governing conformational changes in a glutamate receptor ligand-binding domain Structure 15 2007 1203 1214
55. H. Gelman, and M. Gruebele Fast protein folding kinetics Quart. Rev. Biophys 47 2014 95 142
56. R. Brust, and A. Lukacs S.R. Meech Proteins in action: femtosecond to millisecond structural dynamics of a photoactive flavoprotein J. Am. Chem. Soc. 135 2013 16168 16174
57. T.S. Young, and I. Ahmad P.G. Schultz An enhanced system for unnatural amino acid mutagenesis in E. coli J. Mol. Biol. 395 2010 361 374
58. J.N. Taylor, D.E. Makarov, and C.F. Landes Denoising single-molecule FRET trajectories with wavelets and Bayesian inference Biophys. J. 98 2010 164 173
59. J.N. Taylor, and C.F. Landes Improved resolution of complex single-molecule FRET systems via wavelet shrinkage J. Phys. Chem. B 115 2011 1105 1114
60. S.A. McKinney, C. Joo, and T. Ha Analysis of single-molecule FRET trajectories using hidden Markov modeling Biophys. J. 91 2006 1941 1951
61. J.E. Bronson, and J. Fei C.H. Wiggins Learning rates and states from biophysical time series: a Bayesian approach to model selection and single-molecule FRET data Biophys. J. 97 2009 3196 3205
62. L.P. Watkins, and H. Yang Detection of intensity change points in time-resolved single-molecule measurements J. Phys. Chem. B 109 2005 617 628
63. A.J. Hanson, and P.C.-W. Fu Application of MDL to selected families of models P.D. Grunwald, I.J. Myung, M.A. Pitt, Advances in Minimum Description Length: Theory and Applications (Neural Information Processing series) 2005 The MIT Press Cambridge, MA 125 150
64. B.W. van der Meer Kappa-squared: from nuisance to new sense J. Biotechnol. 82 2002 181 196
65. C. Camilloni, and A.G. Rocco G. Tiana Urea and guanidinium chloride denature protein L in different ways in molecular dynamics simulations Biophys. J. 94 2008 4654 4661