Visualization of structural changes accompanying activation of N-methyl-D-aspartate (NMDA) receptors using fast-scan atomic force microscopy imaging

Journal of Biological Chemistry

Volumn 288, Issue 2, 2013, Pages 778-784

  Suzuki, Yuki ^a   Goetze, Tom A ^b   Stroebel, David ^c   Balasuriya, Dilshan ^b   Yoshimura, Shige H ^a   Henderson, Robert M ^b   Paoletti, Pierre ^c   Takeyasu, Kunio ^a   Edwardson, J Michael ^b  

^a KYOTO UNIVERSITY   (Japan)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c PSL RESEARCH UNIVERSITY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

AFM IMAGING; ATOMIC FORCE; BILAYER SURFACE; CENTRAL NERVOUS SYSTEMS; EXTRACELLULAR; EXTRACELLULAR REGION; INTRACELLULAR DOMAIN; N-METHYL-D-ASPARTATE; NMDA RECEPTOR; RAPID REDUCTION; RECEPTOR ACTIVATION; REDUCTION IN HEIGHT; SINGLE MOLECULE LEVEL; STRUCTURAL CHANGE; SYNAPTIC TRANSMISSION; UV PHOTOLYSIS;

AMINO ACIDS; ATOMIC FORCE MICROSCOPY; LIPID BILAYERS; PHOTOLYSIS;

ENZYME ACTIVITY;

2 AMINO 5 PHOSPHONOVALERIC ACID; GLUTAMIC ACID; GLYCINE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2A; N METHYL DEXTRO ASPARTIC ACID RECEPTOR STIMULATING AGENT; RECEPTOR ANTIBODY;

ANIMAL CELL; ARTICLE; ATOMIC FORCE MICROSCOPY; CONTROLLED STUDY; EXTRACELLULAR MATRIX; FATS SCAN ATOMIC FORCE MICROSCOPY; LIPID BILAYER; NONHUMAN; PHOTOLYSIS; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN DOMAIN; PROTEIN LIPID INTERACTION; PROTEIN MODIFICATION; PROTEIN STRUCTURE; RECEPTOR BINDING; STRUCTURE ANALYSIS; SYNAPSE; ULTRAVIOLET RADIATION;

HEK293 CELLS; HUMANS; MICROSCOPY, ATOMIC FORCE; PROTEIN CONFORMATION; RECEPTORS, N-METHYL-D-ASPARTATE;

EID: 84872346106     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.422311     Document Type: Article

References (34)

1. 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
2. Mayer, M. L. (2011) Emerging models of glutamate receptor ion channel structure and function. Structure 19, 1370-1380
3. 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
4. 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
5. Sun, Y., Olson, R., Horning, M., Armstrong, N., Mayer, M., and Gouaux, E. (2002) Mechanism of glutamate receptor desensitization. Nature 417, 245-253 (Pubitemid 34534700)
6. Mony, L., Kew, J. N., Gunthorpe, M. J., and Paoletti, P. (2009) Allosteric modulators of NR2B-containing NMDA receptors: molecular mechanisms and therapeutic potential. Br. J. Pharmacol. 157, 1301-1317
7. Paoletti, P. (2011) Molecular basis ofNMDAreceptor functional diversity. Eur. J. Neurosci. 33, 1351-1365
8. Furukawa, H., Singh, S. K., Mancusso, R., and Gouaux, E. (2005) Subunit arrangement and function in NMDA receptors. Nature 438, 185-192 (Pubitemid 41599865)
9. Gielen, M., Le Goff, A., Stroebel, D., Johnson, J. W., Neyton, J., and Paoletti, P. (2008) Structural rearrangements of NR1/NR2A NMDA receptors during allosteric inhibition. Neuron 57, 80-93
10. Lee, C. H., and Gouaux, E. (2011) Amino-terminal domains of theNMDA receptor are organized as local heterodimers. PLoS ONE 6, e19180
11. Mony, L., Zhu, S., Carvalho, S., and Paoletti, P. (2011) Molecular basis of positive allosteric modulation of GluN2B NMDA receptors by polyamines. EMBO J. 30, 3134-3146
12. Karakas, E., Simorowski, N., and Furukawa, H. (2011) Subunit arrangement and phenylethanolamine binding in GluN1/GluN2B NMDA receptors. Nature 475, 249-253
13. Paoletti, P., Perin-Dureau, F., Fayyazuddin, A., Le Goff, A., Callebaut, I., and Neyton, J. (2000) Molecular organization of a zinc-binding N-terminal modulatory domain in a NMDA receptor subunit. Neuron 28, 911-925 (Pubitemid 32038081)
14. Paoletti, P., Ascher, P., and Neyton, J. (1997) High-affinity zinc inhibition of NMDA NR1-NR2A receptors. J. Neurosci. 17, 5711-5725 (Pubitemid 27310487)
15. Ando, T., Kodera, N., Takai, E., Maruyama, D., Saito, K., and Toda, A. (2001)Ahigh-speed atomic force microscope for studying biological macromolecules. Proc. Natl. Acad. Sci. U.S.A. 98, 12468-12472 (Pubitemid 33019969)
16. Yokokawa, M., Carnally, S. M., Henderson, R. M., Takeyasu, K., and Edwardson, J. M. (2010) Acid-sensing ion channel (ASIC) 1a undergoes a height transition in response to acidification. FEBS Lett. 584, 3107-3110
17. Schneider, S. W., Lärmer, J., Henderson, R. M., and Oberleithner, H. (1998) Molecular weights of individual proteins correlate with molecular volumes measured by atomic force microscopy. Pflügers Arch. 435, 362-367
18. Wenthold, R. J., Prybylowski, K., Standley, S., Sans, N., and Petralia, R. S. (2003) Trafficking of NMDA receptors. Annu. Rev. Pharmacol. Toxicol. 43, 335-358 (Pubitemid 37372645)
19. Farina, A. N., Blain, K. Y., Maruo, T., Kwiatkowski, W., Choe, S., and Nakagawa, T. (2011) Separation of domain contacts is required for heterotetrameric assembly of functional NMDA receptors. J. Neurosci. 31, 3565-3579
20. Sprong, H., van der Sluijs, P., and van Meer, G. (2001) How proteins move lipids and lipids move proteins. Nat. Rev. Mol. Cell Biol. 2, 504-513 (Pubitemid 33673400)
21. Lester, R. A., and Jahr, C. E. (1992) NMDA channel behavior depends on agonist affinity. J. Neurosci. 12, 635-643
22. Spruston, N., Jonas, P., and Sakmann, B. (1995) Dendritic glutamate receptor channels in rat hippocampal CA3 and CA1 pyramidal neurons. J. Physiol. 482, 325-352
23. Tichelaar, W., Safferling, M., Keinänen, K., Stark, H., and Madden, D. R. (2004) The three-dimensional structure of an ionotropic glutamate receptor reveals a dimer-of-dimers assembly. J. Mol. Biol. 344, 435-442 (Pubitemid 39441215)
24. Nakagawa, T., Cheng, Y., Ramm, E., Sheng, M., and Walz, T. (2005) Structure and different conformational states of native AMPA receptor complexes. Nature 433, 545-549 (Pubitemid 40204314)
25. Nakagawa, T. (2010) The biochemistry, ultrastructure, and subunit assembly mechanism of AMPA receptors. Mol. Neurobiol. 42, 161-184
26. Shanks, N. F., Maruo, T., Farina, A. N., Ellisman, M. H., and Nakagawa, T. (2010) Contribution of the global subunit structure and stargazin on the maturation of AMPA receptors. J. Neurosci. 30, 2728-2740
27. Gielen, M., Siegler Retchless, B., Mony, L., Johnson, J. W., and Paoletti, P. (2009) Mechanism of differential control of NMDA receptor activity by NR2 subunits. Nature 459, 703-707
28. Yokokawa, M., Wada, C., Ando, T., Sakai, N., Yagi, A., Yoshimura, S. H., and Takeyasu, K. (2006) Fast-scanning atomic force microscopy reveals the ATP/ADP-dependent conformational changes of GroEL.EMBOJ. 25, 4567-4576 (Pubitemid 44498130)
29. Shinozaki, Y., Sumitomo, K., Tsuda, M., Koizumi, S., Inoue, K., and Torimitsu, K. (2009) Direct observation of ATP-induced conformational changes in single P2X4 receptors. PLoS Biol. 7, e1000103
30. Yokokawa, M., and Takeyasu, K. (2011) Motion of the Ca2+-pump captured. FEBS J. 278, 3025-3031
31. Dalva, M. B., Takasu, M. A., Lin, M. Z., Shamah, S. M., Hu, L., Gale, N. W., and Greenberg, M. E. (2000) EphB receptors interact with NMDA receptors and regulate excitatory synapse formation. Cell 103, 945-956
32. Takasu, M. A., Dalva, M. B., Zigmond, R. E., and Greenberg, M. E. (2002) Modulation of NMDA receptor-dependent calcium influx and gene expression through EphB receptors. Science 295, 491-495 (Pubitemid 34101638)
33. Wang, C.-Y., Chang, K., Petralia, R. S., Wang, Y. X., Seabold, G. K., and Wenthold, R. J. (2006) A novel family of adhesion-like molecules that interacts with the NMDA receptor. J. Neurosci. 26, 2174-2183 (Pubitemid 44699026)
34. Hansen, K. B., Furukawa, H., and Traynelis, S. F. (2010) Control of assembly and function of glutamate receptors by the amino-terminal domain. Mol. Pharmacol. 78, 535-549