Separate intramolecular targets for protein kinase A control N-Methyl-D-aspartate receptor gating and Ca2+ permeability

Journal of Biological Chemistry

Volumn 289, Issue 27, 2014, Pages 18805-18817

  Aman, Teresa K ^a   Maki, Bruce A ^a   Ruffino, Thomas J ^a   Kasperek, Eileen M ^a   Popescu, Gabriela K ^a  

^a UNIVERSITY AT BUFFALO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PLANTS (BOTANY);

C-TERMINAL DOMAINS; FUNDAMENTAL MECHANISMS; N METHYL D ASPARTATE RECEPTOR; NMDA RECEPTOR; PROTEIN KINASE A;

CALCIUM;

CALCIUM ION; CYCLIC AMP DEPENDENT PROTEIN KINASE; 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; RECOMBINANT RECEPTOR; SERINE; SODIUM ION;

ARTICLE; CALCIUM CONDUCTANCE; CHANNEL GATING; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVITY; ENZYME INHIBITION; HUMAN; HUMAN CELL; MEMBRANE PERMEABILITY; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; RECEPTOR DOWN REGULATION; SODIUM CONDUCTANCE;

CALCIUM SIGNALING; CAMP PROTEIN KINASE; IONOTROPIC GLUTAMATE RECEPTOR; NEUROTRANSMITTER RECEPTOR; PERMEATION MECHANISM; PROTEIN PHOSPHORYLATION; REACTION MECHANISM; RECEPTOR DESENSITIZATION; SINGLE-CHANNEL KINETICS;

ANIMALS; CALCIUM; CYCLIC AMP-DEPENDENT PROTEIN KINASES; ELECTROPHYSIOLOGICAL PROCESSES; HEK293 CELLS; HUMANS; ION CHANNEL GATING; PERMEABILITY; PROTEIN KINASE INHIBITORS; PROTEIN STRUCTURE, TERTIARY; PROTEIN SUBUNITS; RATS; RECEPTORS, N-METHYL-D-ASPARTATE; SERINE;

EID: 84903839990     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.537282     Document Type: Article

References (48)

1. Shouval, H. Z., Bear, M. F., and Cooper, L. N. (2002) A unified model of NMDA receptor-dependent bidirectional synaptic plasticity. Proc. Natl. Acad. Sci. U. S. A. 99, 10831-10836
2. Choi, D. W. (1994) Calcium and excitotoxic neuronal injury. Ann. N. Y. Acad. Sci. 747, 162-171
3. Bliss, T. V., and Collingridge, G. L. (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361, 31-39
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
5. MacDermott, A. B., Mayer, M. L., Westbrook, G. L., Smith, S. J., and Barker, J. L. (1986) NMDA-receptor activation increases cytoplasmic calcium concentration in cultured spinal cord neurones. Nature 321, 519-522
6. Lester, R. A., Clements, J. D., Westbrook, G. L., and Jahr, C. E. (1990) Channel kinetics determine the time course ofNMDAreceptor-mediated synaptic currents. Nature 346, 565-567
7. 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
8. Burnashev, N., Schoepfer, R., Monyer, H., Ruppersberg, J. P., Günther, W., Seeburg, P. H., and Sakmann, B. (1992) Control by asparagine residues of calcium permeability and magnesium blockade in the NMDA receptor. Science 257, 1415-1419
9. Watanabe, J., Beck, C., Kuner, T., Premkumar, L. S., and Wollmuth, L. P. (2002) DRPEER: a motif in the extracellular vestibule conferring high Ca2- flux rates inNMDAreceptor channels. J. Neurosci. 22, 10209-10216
10. Chen, B. S., and Roche, K. W. (2007) Regulation of NMDA receptors by phosphorylation. Neuropharmacology 53, 362-368
11. Leonard, A. S., and Hell, J. W. (1997) Cyclic AMP-dependent protein kinase and protein kinase C phosphorylate N -methyl-D-aspartate receptors at different sites. J. Biol. Chem. 272, 12107-12115
12. 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
13. 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
14. Chalifoux, J. R., and Carter, A. G. (2010) GABAB receptors modulate NMDA receptor calcium signals in dendritic spines. Neuron 66, 101-113
15. Higley, M. J., and Sabatini, B. L. (2010) Competitive regulation of synaptic Ca2- influx by D2 dopamine and A2A adenosine receptors. Nat. Neurosci. 13, 958-966
16. Cerne, R., Rusin, K. I., and Randić, M. (1993) Enhancement of the N -methyl- D-aspartate response in spinal dorsal horn neurons by cAMP-dependent protein kinase. Neurosci. Lett. 161, 124-128
17. Westphal, R. S., Tavalin, S. J., Lin, J. W., Alto, N. M., Fraser, I. D., Langeberg, L. K., Sheng, M., and Scott, J. D. (1999) Regulation of NMDA receptors by an associated phosphatase-kinase signaling complex. Science 285, 93-96
18. Bird, G. C., Lash, L. L., Han, J. S., Zou, X., Willis, W. D., and Neugebauer, V. (2005) PKA-dependent enhanced NMDA receptor function in painrelated synaptic plasticity in amygdala neurons. J. Physiol. 5, 907-921
19. Raman, I. M., Tong, G., and Jahr, C. E. (1996) -Adrenergic regulation of synaptic NMDA receptors by cAMP-dependent protein kinase. Neuron 16, 415-421
20. 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
21. Lau, C. G., Takeuchi, K., Rodenas-Ruano, A., Takayasu, Y., Murphy, J., Bennett, M. V., and Zukin, R. S. (2009) Regulation of NMDA receptor Ca2- signalling and synaptic plasticity. Biochem. Soc. Trans. 37, 1369-1374
22. Li, B., Devidze, N., Barengolts, D., Prostak, N., Sphicas, E., Apicella, A. J., Malinow, R., and Emamian, E. S. (2009)NMDAreceptor phosphorylation at a site affected in schizophrenia controls synaptic and behavioral plasticity. J. Neurosci. 29, 11965-11972
23. 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
24. 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
25. Krupp, J. J., Vissel, B., Thomas, C. G., Heinemann, S. F., and Westbrook, G. L. (1999) Interactions of calmodulin and -actinin with the NR1 subunit modulate Ca2-dependent inactivation of NMDA receptors. J. Neurosci. 19, 1165-1178
26. Maki, B. A., Aman, T. K., Amico-Ruvio, S. A., Kussius, C. L., and Popescu, G. K. (2012) C-terminal domains of N -methyl-D-aspartic acid receptor modulate unitary channel conductance and gating. J. Biol. Chem. 287, 36071-36080
27. Xu, M., Smothers, C. T., and Woodward, J. J. (2011) Effects of ethanol on phosphorylation site mutants of recombinant N -methyl-D-aspartate receptors. Alcohol 45, 373-380
28. Murphy, J. A., Stein, I. S., Lau, C. G., Peixoto, R. T., Aman, T. K., Kaneko, N., Aromolaran, K., Saulnier, J. L., Popescu, G. K., Sabatini, B. L., Hell, J. W., and Zukin, R. S. (2014) Phosphorylation of Ser1166 on GluN2B by PKA is critical to synapticNMDAreceptor function and Ca2- signaling in spines. J. Neurosci. 34, 869-879
29. Tash, J. S., Welsh, M. J., and Means, A. R. (1980) Protein inhibitor of cAMP-dependent protein kinase: production and characterization of antibodies and intracellular localization. Cell 21, 57-65
30. Chen, T.-W., Wardill, T. J., Sun, Y., Pulver, S. R., Renninger, S. L., Baohan, A., Schreiter, E. R., Kerr, R. A., Orger, M. B., Jayaraman, V., Looger, L. L., Svoboda, K., and Kim, D. S. (2013) Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature 499, 295-300
31. Qin, F., Auerbach, A., and Sachs, F. (1996) Estimating single-channel kinetic parameters from idealized patch-clamp data containing missed events. Biophys. J. 70, 264-280
32. Qin, F., Auerbach, A., and Sachs, F. (1997) Maximum likelihood estimation of aggregated Markov processes. Proc. Biol. Sci. 264, 375-383
33. Kussius, C. L., Kaur, N., and Popescu, G. K. (2009) Pregnanolone sulfate promotes desensitization of activated NMDA receptors. J. Neurosci. 29, 6819-6827
34. Dalton, G. D., and Dewey, W. L. (2006) Protein kinase inhibitor peptide (PKI): a family of endogenous neuropeptides that modulate neuronal cAMP-dependent protein kinase function. Neuropeptides 40, 23-34
35. Amico-Ruvio, S. A., and Popescu, G. K. (2010) Stationary gating of GluN1/ GluN2B receptors in intact membrane patches. Biophys. J. 98, 1160-1169
36. Popescu, G., and Auerbach, A. (2003) Modal gating of NMDA receptors and the shape of their synaptic response. Nat. Neurosci. 6, 476-483
37. Krupp, J. J., Vissel, B., Heinemann, S. F., and Westbrook, G. L. (1996) Calcium-dependent inactivation of recombinant N -methyl-D-aspartate receptors is NR2 subunit specific. Mol. Pharmacol. 50, 1680-1688
38. Legendre, P., Rosenmund, C., and Westbrook, G. L. (1993) Inactivation of NMDA channels in cultured hippocampal neurons by intracellular calcium. J. Neurosci. 13, 674-684
39. Rosenmund, C., and Westbrook, G. L. (1993) Rundown of N -methyl-Daspartate channels during whole-cell recording in rat hippocampal neurons: role of Ca2- and ATP. J. Physiol. 470, 705-729
40. Tong, G., Shepherd, D., and Jahr, C. E. (1995) Synaptic desensitization of NMDA receptors by calcineurin. Science 267, 1510-1512
41. Borschel, W. F., Myers, J. M., Kasperek, E. M., Smith, T. P., Graziane, N. M., Nowak, L. M., and Popescu, G. K. (2012) Gating reaction mechanism of neuronal NMDA receptors. J. Neurophysiol. 108, 3105-3115
42. Ascher, P., and Nowak, L. (1988) The role of divalent cations in the N methyl- D-aspartate responses of mouse central neurones in culture. J. Physiol. 399, 247-266
43. 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
44. Townsend, M., Liu, Y., and Constantine-Paton, M. (2004) Retina-driven dephosphorylation of the NR2A subunit correlates with faster NMDA receptor kinetics at developing retinocollicular synapses. J. Neurosci. 24, 11098-11107
45. Maki, B. A., Cole, R., and Popescu, G. K. (2013) Two serine residues on GluN2A C-terminal tails control NMDA receptor current decay times. Channels 7, 126-132
46. Sobczyk, A., and Svoboda, K. (2007) Activity-dependent plasticity of the NMDA-receptor fractional Ca2- current. Neuron 53, 17-24
47. Chatterjea, D., Hamid, E., Leonard, J. P., and Alford, S. (2010) Phosphorylation- state-dependent regulation of NMDA receptor short-term plasticity modifies hippocampal dendritic Ca2- transients. J. Neurophysiol. 104, 2203-2213
48. Gambrill, A. C., Storey, G. P., and Barria, A. (2011) Dynamic regulation of NMDA-Receptor transmission. J. Neurophysiol. 105, 162-171