C-terminal domains of N-methyl-D-aspartic acid receptor modulate unitary channel conductance and gating

Journal of Biological Chemistry

Volumn 287, Issue 43, 2012, Pages 36071-36080

  Maki, Bruce A ^a   Aman, Teresa K ^a   Amico Ruvio, Stacy A ^a   Kussius, Cassandra L ^a   Popescu, Gabriela K ^a  

^a UNIVERSITY AT BUFFALO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACID RECEPTORS; ADULT BRAIN; BIOPHYSICAL PROPERTIES; C-TERMINAL DOMAINS; CHANNEL CONDUCTANCE; CHANNEL KINETICS; DEACTIVATION KINETICS; EXCITOTOXICITY; GATING MECHANISMS; INTRACELLULAR DOMAIN; KINETIC MECHANISM; NEURODEGENERATION; NMDA RECEPTOR; QUANTITATIVE APPROACH; SINGLE-CHANNEL;

AMINO ACIDS;

KINETICS;

ISOPROTEIN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2A; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2C;

ARTICLE; BIOPHYSICS; CARBOXY TERMINAL SEQUENCE; CELLULAR DISTRIBUTION; CHANNEL GATING; CONTROLLED STUDY; MEMBRANE CONDUCTANCE; NONHUMAN; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RAT; RECEPTOR DOWN REGULATION; STRUCTURE ACTIVITY RELATION;

ANIMALS; HEK293 CELLS; HUMANS; ION CHANNEL GATING; KINETICS; PROTEIN ISOFORMS; PROTEIN STRUCTURE, TERTIARY; RATS; RECEPTORS, N-METHYL-D-ASPARTATE;

EID: 84867815125     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.390013     Document Type: Article

References (66)

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. 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
3. 2+ of NMDA responses in spinal cord neurones. Nature 309, 261-263
4. Nowak, L., Bregestovski, P., Ascher, P., Herbet, A., and Prochiantz, A. (1984) Magnesium gates glutamate-activated channels in mouse central neurones. Nature 307, 462-465 (Pubitemid 14132062)
5. Ascher, P., and Nowak, L. (1988) The role of divalent cations in the Nmethyl- D-aspartate responses of mouse central neurones in culture. J. Physiol. 399, 247-266
6. Mayer, M. L., and Westbrook, G. L. (1987) Permeation and block of N-methyl-D-aspartic acid receptor channels by divalent cations in mouse cultured central neurones. J. Physiol. 394, 501-527 (Pubitemid 18005147)
7. Lester, R. A., Clements, J. D., Westbrook, G. L., and Jahr, C. E. (1990) Channel kinetics determine the time course of NMDA receptor-mediated synaptic currents. Nature 346, 565-567
8. Hollmann, M., Boulter, J., Maron, C., Beasley, L., Sullivan, J., Pecht, G., and Heinemann, S. (1993) Zinc potentiates agonist-induced currents at certain splice variants of the NMDA receptor. Neuron 10, 943-954 (Pubitemid 23152049)
9. Monyer, H., Sprengel, R., Schoepfer, R., Herb, A., Higuchi, M., Lomeli, H., Burnashev, N., Sakmann, B., and Seeburg, P. H. (1992) Heteromeric NMDA receptors. Molecular and functional distinction of subtypes. Science 256, 1217-1221
10. Ishii, T., Moriyoshi, K., Sugihara, H., Sakurada, K., Kadotani, H., Yokoi, M., Akazawa, C., Shigemoto, R., Mizuno, N., and Masu, M. (1993) Molecular characterization of the family of the N-methyl-D-aspartate receptor subunits. J. Biol. Chem. 268, 2836-2843 (Pubitemid 23057917)
11. Monyer, H., Burnashev, N., Laurie, D. J., Sakmann, B., and Seeburg, P. H. (1994) Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron 12, 529-540 (Pubitemid 24100885)
12. Sheng, M., Cummings, J., Roldan, L. A., Jan, Y. N., and Jan, L. Y. (1994) Changing subunit composition of heteromeric NMDA receptors during development of rat cortex. Nature 368, 144-147 (Pubitemid 24101524)
13. Laurie, D. J., and Seeburg, P. H. (1994) Regional and developmental heterogeneity in splicing of the rat brain NMDAR1 mRNA. J. Neurosci. 14, 3180-3194 (Pubitemid 24139002)
14. Laube, B., Kuhse, J., and Betz, H. (1998) Evidence for a tetrameric structure of recombinant NMDA receptors. J. Neurosci. 18, 2954-2961 (Pubitemid 28163225)
15. Furukawa, H., Singh, S. K., Mancusso, R., and Gouaux, E. (2005) Subunit arrangement and function in NMDA receptors. Nature 438, 185-192 (Pubitemid 41599865)
16. Behe, P., Stern, P., Wyllie, D. J., Nassar, M., Schoepfer, R., and Colquhoun, D. (1995) Determination of NMDA NR1 subunit copy number in recombinant NMDA receptors. Proc. R. Soc. Lond. B Biol. Sci. 262, 205-213
17. Foster, K. A., McLaughlin, N., Edbauer, D., Phillips, M., Bolton, A., Constantine- Paton, M., and Sheng, M. (2010) Distinct roles of NR2A and NR2B cytoplasmic tails in long-term potentiation. J. Neurosci. 30, 2676-2685
18. Ryan, T. J., Emes, R. D., Grant, S. G., and Komiyama, N. H. (2008) Evolution of NMDA receptor cytoplasmic interaction domains. Implications for organisation of synaptic signalling complexes. BMC Neurosci. 9, 6
19. 2+-dependent inactivation of NMDA receptors. J. Neurosci. 19, 1165-1178
20. Zhang, S., Ehlers, M. D., Bernhardt, J. P., Su, C. T., and Huganir, R. L. (1998) Calmodulin mediates calcium-dependent inactivation of N-methyl- D-aspartate receptors. Neuron 21, 443-453 (Pubitemid 28399704)
21. Choi, U. B., Xiao, S., Wollmuth, L. P., and Bowen, M. E. (2011) Effect of Src kinase phosphorylation on disordered C-terminal domain of N-methyl-Daspartic acid (NMDA) receptor subunit GluN2B protein. J. Biol. Chem. 286, 29904-29912
22. Sprengel, R., Suchanek, B., Amico, C., Brusa, R., Burnashev, N., Rozov, A., Hvalby, O., Jensen, V., Paulsen, O., Andersen, P., Kim, J. J., Thompson, R. F., Sun, W., Webster, L. C., Grant, S. G., Eilers, J., Konnerth, A., Li, J., McNamara, J. O., and Seeburg, P. H. (1998) Importance of the intracellular domain of NR2 subunits for NMDA receptor function in vivo. Cell 92, 279-289 (Pubitemid 28073050)
23. Köhr, G., Jensen, V., Koester, H. J., Mihaljevic, A. L., Utvik, J. K., Kvello, A., Ottersen, O. P., Seeburg, P. H., Sprengel, R., and Hvalby, Ø. (2003) Intracellular domains of NMDA receptor subtypes are determinants for longterm potentiation induction. J. Neurosci. 23, 10791-10799
24. Rossi, P., Sola, E., Taglietti, V., Borchardt, T., Steigerwald, F., Utvik, J. K., Ottersen, O. P., Köhr, G., and D'Angelo, E. (2002) NMDA receptor 2 (NR2) C-terminal control of NR open probability regulates synaptic transmission and plasticity at a cerebellar synapse. J. Neurosci. 22, 9687-9697 (Pubitemid 35332852)
25. Steigerwald, F., Schulz, T. W., Schenker, L. T., Kennedy, M. B., Seeburg, P. H., and Köhr, G. (2000) C-Terminal truncation of NR2A subunits impairs synaptic but not extrasynaptic localization of NMDA receptors. J. Neurosci. 20, 4573-4581 (Pubitemid 30396623)
26. Krupp, J. J., Vissel, B., Thomas, C. G., Heinemann, S. F., and Westbrook, G. L. (2002) Calcineurin acts via the C-terminus of NR2A to modulate desensitization of NMDA receptors. Neuropharmacology 42, 593-602 (Pubitemid 34457739)
27. Mohrmann, R., Köhr, G., Hatt, H., Sprengel, R., and Gottmann, K. (2002) Deletion of the C-terminal domain of the NR2B subunit alters channel properties and synaptic targeting of N-methyl-D-aspartate receptors in nascent neocortical synapses. J. Neurosci. Res. 68, 265-275 (Pubitemid 34462531)
28. Punnakkal, P., Jendritza, P., and Köhr, G. (2012) Influence of the intracellular GluN2 C-terminal domain on NMDA receptor function. Neuropharmacology 62, 1985-1992
29. Chen, B., and Roche, K. (2007) Regulation of NMDA receptors by phosphorylation. Neuropharmacology 62, 471-478
30. Rycroft, B. K., and Gibb, A. J. (2004) Regulation of single NMDA receptor channel activity by α-actinin and calmodulin in rat hippocampal granule cells. J. Physiol. 557, 795-808 (Pubitemid 38961617)
31. Lin, Y., Skeberdis, V. A., Francesconi, A., Bennett, M. V., and Zukin, R. S. (2004) Postsynaptic density protein-95 regulates NMDA channel gating and surface expression. J. Neurosci. 24, 10138-10148 (Pubitemid 39492039)
32. Kussius, C. L., Kaur, N., and Popescu, G. K. (2009) Pregnanolone sulfate promotes desensitization of activated NMDA receptors. J. Neurosci. 29, 6819-6827
33. Qin, F., Auerbach, A., and Sachs, F. (2000) A direct optimization approach to hidden Markov modeling for single channel kinetics. Biophys. J. 79, 1915-1927
34. Amico-Ruvio, S. A., Murthy, S. E., Smith, T. P., and Popescu, G. K. (2011) Zinc effects on NMDA receptor gating kinetics. Biophys. J. 100, 1910-1918
35. Qin, F. (2004) Restoration of single-channel currents using the segmental k-means method based on hidden Markov modeling. Biophys. J. 86, 1488-1501
36. Qin, F., Auerbach, A., and Sachs, F. (1997) Maximum likelihood estimation of aggregated Markov processes. Proc. Biol. Sci. 264, 375-383 (Pubitemid 27144045)
37. Magleby, K. L., and Pallotta, B. S. (1983) Burst kinetics of single calcium-activated potassium channels in cultured rat muscle. J. Physiol. 344, 605-623 (Pubitemid 14233230)
38. Popescu, G., Robert, A., Howe, J. R., and Auerbach, A. (2004) Reaction mechanism determines NMDA receptor response to repetitive stimulation. Nature 430, 790-793 (Pubitemid 39071350)
39. Peters, S., Koh, J., and Choi, D. (1987) Zinc selectively blocks the action of N-methyl-D-aspartate on cortical neurons. Science 236, 589-593 (Pubitemid 17069929)
40. Paoletti, P., Ascher, P., and Neyton, J. (1997) High-affinity zinc inhibition of NMDA NR1-NR2A receptors. J. Neurosci. 17, 5711-5725 (Pubitemid 27310487)
41. Rachline, J., Perin-Dureau, F., Le Goff, A., Neyton, J., and Paoletti, P. (2005) The micromolar zinc-binding domain on the NMDA receptor subunit NR2B. J. Neurosci. 25, 308-317 (Pubitemid 40105601)
42. Forsythe, I. D., Westbrook, G. L., and Mayer, M. L. (1988) Modulation of excitatory synaptic transmission by glycine and zinc in cultures of mouse hippocampal neurons. J. Neurosci. 8, 3733-3741
43. Banke, T. G., Dravid, S. M., and Traynelis, S. F. (2005) Protons trap NR1/ NR2B NMDA receptors in a nonconducting state. J. Neurosci. 25, 42-51 (Pubitemid 40110764)
44. Traynelis, S. F., and Cull-Candy, S. G. (1990) Proton inhibition of N-methyl-D-aspartate receptors in cerebellar neurons. Nature 345, 347-350
45. +. Proc. Natl. Acad. Sci. U.S.A. 87, 6445-6449
46. Banke, T. G., and Traynelis, S. F. (2003) Activation of NR1/NR2B NMDA receptors. Nat. Neurosci. 6, 144-152 (Pubitemid 36182783)
47. Popescu, G., and Auerbach, A. (2003) Modal gating of NMDA receptors and the shape of their synaptic response. Nat. Neurosci. 6, 476-483 (Pubitemid 36514695)
48. Erreger, K., Dravid, S. M., Banke, T. G., Wyllie, D. J., and Traynelis, S. F. (2005) Subunit-specific gating controls rat NR1/NR2A and NR1/NR2B NMDA channel kinetics and synaptic signalling profiles. J. Physiol. 563, 345-358 (Pubitemid 40360896)
49. Amico-Ruvio, S. A., and Popescu, G. K. (2010) Stationary gating of GluN1/ GluN2B receptors in intact membrane patches. Biophys. J. 98, 1160-1169
50. Dravid, S. M., Prakash, A., and Traynelis, S. F. (2008) Activation of recombinant NR1/NR2C NMDA receptors. J. Physiol. 586, 4425-4439
51. Popescu, G. K. (2012) Modes of glutamate receptor gating. J. Physiol. 590, 73-91
52. Kussius, C. L., and Popescu, G. K. (2009) Kinetic basis of partial agonism at NMDA receptors. Nat. Neurosci. 12, 1114-1120
53. Collingridge, G. (1987) Synaptic plasticity. The role of NMDA receptors in learning and memory. Nature 330, 604-605
54. Burnashev, N., Zhou, Z., Neher, E., and Sakmann, B. (1995) Fractional calcium currents through recombinant GluR channels of the NMDA, AMPA and kainate receptor subtypes. J. Physiol. 485, 403-418
55. Skeberdis, V. A., Chevaleyre, V., Lau, C. G., Goldberg, J. H., Pettit, D. L., Suadicani, S. O., Lin, Y., Bennett, M. V., Yuste, R., Castillo, P. E., and Zukin, R. S. (2006) Protein kinase A regulates calcium permeability of NMDA receptors. Nat. Neurosci. 9, 501-510
56. SieglerRetchless, B., Gao, W., and Johnson, J. W. (2012) A single GluN2 subunit residue controls NMDA receptor channel properties via intersubunit interaction. Nat. Neurosci. 15, 406-413
57. Rycroft, B. K., and Gibb, A. J. (2002) Direct effects of calmodulin on NMDA receptor single-channel gating in rat hippocampal granule cells. J. Neurosci. 22, 8860-8868
58. Ehlers, M. D., Zhang, S., Bernhadt, J. P., and Huganir, R. L. (1996) Inactivation of NMDA receptors by direct interaction of calmodulin with the NR1 subunit. Cell 84, 745-755 (Pubitemid 26094204)
59. Tingley, W. G., Ehlers, M. D., Kameyama, K., Doherty, C., Ptak, J. B., Riley, C. T., and Huganir, R. L. (1997) Characterization of protein kinase A and protein kinase C phosphorylation of the N-methyl-D-aspartate receptor NR1 subunit using phosphorylation site-specific antibodies. J. Biol. Chem. 272, 5157-5166 (Pubitemid 27090073)
60. 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)
61. 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
62. Müllner, C., Yakubovich, D., Dessauer, C. W., Platzer, D., and Schreibmayer, W. (2003) Single channel analysis of the regulation of GIRK1/ GIRK4 channels by protein phosphorylation. Biophys. J. 84, 1399-1409 (Pubitemid 36133460)
63. Singer-Lahat, D., Dascal, N., and Lotan, I. (1999) Modal behavior of the Kv1.1 channel conferred by the Kvß1.1 subunit and its regulation by dephosphorylation of Kv1.1. Pflügers Arch. Eur. J. Physiol. 439, 18-26 (Pubitemid 30055503)
64. 2+ channels in human vascular smoothmuscle cells. Biochem. J. 318, 513-517
65. Hardingham, G. E. (2009) Coupling of the NMDA receptor to neuroprotective and neurodestructive events. Biochem. Soc. Trans. 37, 1147-1160
66. Clements, J. D., Lester, R. A., Tong, G., Jahr, C. E., and Westbrook, G. L. (1992) The time course of glutamate in the synaptic cleft. Science 258, 1498-1501 (Pubitemid 23011008)