Heteromerization of ligand binding domains of N-methyl-D-aspartate receptor requires both coagonists, L-glutamate and glycine

Biochemistry

Volumn 54, Issue 3, 2015, Pages 787-794

  Cheriyan, John ^a   Mezes, Christina ^a   Zhou, Ning ^a   Balsara, Rashna D ^a   Castellino, Francis J ^a  

^a UNIVERSITY OF NOTRE DAME   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; IONS; LIGANDS; PLANTS (BOTANY);

BRAIN PLASTICITY; HIGHER ORDER FUNCTIONS; ION CHANNEL; L-GLUTAMATE; LIGAND BINDING DOMAIN; N METHYL D ASPARTATE RECEPTOR; NEURONAL SYNAPSIS; NMDA RECEPTOR;

BINDING SITES;

GLUTAMIC ACID; GLYCINE; ION CHANNEL; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; LIGAND; N METHYLASPARTIC ACID; PROTEIN SUBUNIT;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIMERIZATION; EMBRYO; LIGAND BINDING; MOUSE; NONHUMAN; PRIORITY JOURNAL; AGONISTS; ANIMAL; CHANNEL GATING; CHEMICAL STRUCTURE; CHEMISTRY; DRUG EFFECTS; METABOLISM; PROTEIN MULTIMERIZATION; PROTEIN SUBUNIT; PROTEIN TERTIARY STRUCTURE; RAT;

ANIMALS; GLUTAMIC ACID; GLYCINE; ION CHANNEL GATING; LIGANDS; MICE; MODELS, MOLECULAR; N-METHYLASPARTATE; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; PROTEIN SUBUNITS; RATS; RECEPTORS, N-METHYL-D-ASPARTATE;

EID: 84921780550     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi501437s     Document Type: Article

References (34)

1. Paoletti, P., Bellone, C., and Zhou, Q. (2013) NMDA receptor subunit diversity: impact on receptor properties, synaptic plasticity and disease. Nat. Rev. Neurosci. 14, 383-400.
2. Dan, Y., and Poo, M. M. (2004) Spike timing-dependent plasticity of neural circuits. Neuron 44, 23-30.
3. Lai, T. W., Shyu, W. C., and Wang, Y. T. (2011) Stroke intervention pathways: NMDA receptors and beyond. Trends Mol. Med. 17, 266-275.
4. Ahmed, I., Bose, S. K., Pavese, N., Ramlackhansingh, A., Turkheimer, F., Hotton, G., Hammers, A., and Brooks, D. J. (2011) Glutamate NMDA receptor dysregulation in Parkinson's disease with dyskinesias. Brain 134, 979-986.
5. Ghasemi, M., and Schachter, S. C. (2011) The NMDA receptor complex as a therapeutic target in epilepsy: a review. Epilepsy Behav. 22, 617-640.
6. 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.
7. Kleckner, N. W., and Dingledine, R. (1988) Requirement for glycine in activation of NMDA-receptors expressed in Xenopus oocytes. Science 241, 835-837.
8. Johnson, J. W., and Ascher, P. (1987) Glycine potentiates the NMDA response in cultured mouse brain neurons. Nature 325, 529-531.
9. Mothet, J. P., Parent, A. T., Wolosker, H., Brady, R. O., Linden, D. J., Ferris, C. D., Rogawski, M. A., and Snyder, S. H. (2000) D-serine is an endogenous ligand for the glycine site of the N-methyl-Daspartate receptor. Proc. Natl. Acad. Sci. U.S.A. 97, 4926-4931.
10. Papouin, T., Ladepeche, L., Ruel, J., Sacchi, S., Labasque, M., Hanini, M., Groc, L., Pollegioni, L., Mothet, J. P., and Oliet, S. H. (2012) Synaptic and extrasynaptic NMDA receptors are gated by different endogenous coagonists. Cell 150, 633-646.
11. Kazi, R., Gan, Q., Talukder, I., Markowitz, M., Salussolia, C. L., and Wollmuth, L. P. (2013) Asynchronous movements prior to pore opening in NMDA receptors. J. Neurosci. 33, 12052-12066.
12. Jespersen, A., Tajima, N., Fernandez-Cuervo, G., Garnier-Amblard, E. C., and Furukawa, H. (2014) Structural insights into competitive antagonism in NMDA receptors. Neuron 81, 366-378.
13. Karakas, E., and Furukawa, H. (2014) Crystal structure of a heterotetrameric NMDA receptor ion channel. Science 344, 992-997.
14. Lee, C. H., Lu, W., Michel, J. C., Goehring, A., Du, J., Song, X., and Gouaux, E. (2014) NMDA receptor structures reveal subunit arrangement and pore architecture. Nature 511, 191-197.
15. Kussius, C. L., and Popescu, G. K. (2010) NMDA receptors with locked glutamate-binding clefts open with high efficacy. J. Neurosci. 30, 12474-12479.
16. Borschel, W. F., Murthy, S. E., Kasperek, E. M., and Popescu, G. K. (2011) NMDA receptor activation requires remodelling of intersubunit contacts within ligand-binding heterodimers. Nat. Commun. 2, 498.
17. Kumar, J., and Mayer, M. L. (2013) Functional insights from glutamate receptor ion channel structures. Annu. Rev. Physiol. 75, 313-337.
18. Iwaki, T., Figuera, M., Ploplis, V. A., and Castellino, F. J. (2003) Rapid selection of Drosophila S2 cells with the puromycin-resistant gene. BioTechniques 35, 482-486.
19. Schuck, P., Perugini, M. A., Gonzales, N. R., Howlett, G. J., and Schubert, D. (2002) Size-distribution analysis of proteins by analytical ultracentrifugation: strategies and application to model systems. Biophys. J. 82, 1096-1111.
20. Schuck, P. (2000) Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and lamm equation modeling. Biophys. J. 78, 1606-1619.
21. Veran, J., Kumar, J., Pinheiro, P. S., Athane, A., Mayer, M. L., Perrais, D., and Mulle, C. (2012) Zinc potentiates GluK3 glutamate receptor function by stabilizing the ligand binding domain dimer interface. Neuron 76, 565-578.
22. Furukawa, H., Singh, S. K., Mancusso, R., and Gouaux, E. (2005) Subunit arrangement and function in NMDA receptors. Nature 438, 185-192.
23. Ivanovic, A., Reilander, H., Laube, B., and Kuhse, J. (1998) Expression and initial characterization of a soluble glycine binding domain of the N-Methyl-D-aspartate receptor NR1 subunit. J. Biol. Chem. 273, 19933-19937.
24. Fadda, E., Danysz, W., Wroblewski, J. T., and Costa, E. (1988) Glycine and D-serine increase the affinity of N-methyl-D-aspartate sensitive glutamate binding sites in rat brain synaptic membranes. Neuropharmacology 27, 1183-1185.
25. Grimwood, S., Wilde, G. J., and Foster, A. C. (1993) Interactions between the glutamate and glycine recognition sites of the N-methyl-D-aspartate receptor from rat brain, as revealed from radioligand binding studies. J. Neurochem. 60, 1729-1738.
26. Danysz, W., and Parsons, C. G. (1998) Glycine and N-methyl-D-aspartate receptors: physiological significance and possible therapeutic applications. Pharmacol. Rev. 50, 597-664.
27. Regalado, M. P., Villarroel, A., and Lerma, J. (2001) Intersubunit cooperativity in the NMDA receptor. Neuron 32, 1085-1096.
28. Riou, M., Stroebel, D., Edwardson, J. M., and Paoletti, P. (2012) An alternating GluN1-2-1-2 subunit arrangement in mature NMDA receptors. PloS One 7, e35134.
29. Madry, C., Mesic, I., Betz, H., and Laube, B. (2007) The N-terminal domains of both NR1 and NR2 subunits determine allosteric Zn2+ inhibition and glycine affinity of N-methyl-D-aspartate receptors. Mol. Pharmacol. 72, 1535-1544.
30. 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.
31. Furukawa, H., Singh, S. K., Mancusso, R., and Gouaux, E. (2005) Subunit arrangement and function in NMDA receptors. Nature 438, 185-192.
32. Kussius, C. L., Popescu, A. M., and Popescu, G. K. (2010) Agonist-specific gating of NMDA receptors. Channels 4, 78-82.
33. Schauder, D. M., Kuybeda, O., Zhang, J., Klymko, K., Bartesaghi, A., Borgnia, M. J., Mayer, M. L., and Subramaniam, S. (2013) Glutamate receptor desensitization is mediated by changes in quaternary structure of the ligand binding domain. Proc. Natl. Acad. Sci. U.S.A. 110, 5921-5926.
34. Kazi, R., Dai, J., Sweeney, C., Zhou, H. X., and Wollmuth, L. P. (2014) Mechanical coupling maintains the fidelity of NMDA receptor-mediated currents. Nat. Neurosci. 17, 914-922.