NR3A-containing NMDARs promote neurotransmitter release and spike timing-dependent plasticity

Nature Neuroscience

Volumn 14, Issue 3, 2011, Pages 338-344

  Larsen, Rylan S ^a   Corlew, Rebekah J ^a   Henson, Maile A ^a   Roberts, Adam C ^a,b   Mishina, Masayoshi ^c   Watanabe, Masahiko ^d   Lipton, Stuart A ^e   Nakanishi, Nobuki ^e   Pérez Otaño, Isabel ^f   Weinberg, Richard J ^a,b   Philpot, Benjamin D ^a,b  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF TOKYO   (Japan)

^d HOKKAIDO UNIVERSITY   (Japan)

^e BURNHAM INSTITUTE   (United States)

^f UNIVERSITY OF NAVARRA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTAMIC ACID; MAGNESIUM; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 3A; NEUROTRANSMITTER; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DEPOLARIZATION; FEMALE; LIGAND BINDING; LONG TERM DEPRESSION; MALE; MOUSE; NERVE CELL PLASTICITY; NEUROTRANSMISSION; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; SPIKE; SYNAPTIC TRANSMISSION; VISUAL CORTEX;

ACTION POTENTIALS; ANIMALS; EXCITATORY POSTSYNAPTIC POTENTIALS; GLUTAMIC ACID; LONG-TERM SYNAPTIC DEPRESSION; MAGNESIUM; MICE; MICE, TRANSGENIC; NEURONAL PLASTICITY; NEUROTRANSMITTER AGENTS; PROTEIN SUBUNITS; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPTIC TRANSMISSION; TIME FACTORS;

EID: 79951976380     PISSN: 10976256     EISSN: None     Source Type: Journal    
DOI: 10.1038/nn.2750     Document Type: Article

References (50)

1. Hensch, T.K. Critical period plasticity in local cortical circuits. Nat. Rev. Neurosci. 6, 877-888 (2005).
2. Philpot, B.D., Sekhar, A.K., Shouval, H.Z. & Bear, M.F. Visual experience and deprivation bidirectionally modify the composition and function of NMDA receptors in visual cortex. Neuron 29, 157-169 (2001).
3. Dudek, S.M. & Bear, M.F. Bidirectional long-term modification of synaptic effectiveness in the adult and immature hippocampus. J. Neurosci. 13, 2910-2918 (1993).
4. Corlew, R., Wang, Y., Ghermazien, H., Erisir, A. & Philpot, B.D. Developmental switch in the contribution of presynaptic and postsynaptic NMDA receptors to longterm depression. J. Neurosci. 27, 9835-9845 (2007).
5. Banerjee, A. et al. Double dissociation of spike timing-dependent potentiation and depression by subunit-preferring NMDA receptor antagonists in mouse barrel cortex. Cereb. Cortex 19, 2959-2969 (2009).
6. Kemp, J.A. & McKernan, R.M. NMDA receptor pathways as drug targets. Nat. Neurosci. 5 Suppl: 1039-1042 (2002).
7. Cull-Candy, S.G. & Leszkiewicz, D.N. Role of distinct NMDA receptor subtypes at central synapses. Sci. STKE 2004, re16 (2004).
8. Rodríguez-Moreno, A., Banerjee, A. & Paulsen, O. Presynaptic NMDA receptors and spike timing-dependent long-term depression at cortical synapses. Front. Synaptic Neurosci 2, 12 (2010).
9. Corlew, R., Brasier, D.J., Feldman, D.E. & Philpot, B.D. Presynaptic NMDA receptors: newly appreciated roles in cortical synaptic function and plasticity. Neuroscientist 14, 609-625 (2008).
10. Sjöström, P.J., Turrigiano, G.G. & Nelson, S.B. Neocortical LTD via coincident activation of presynaptic NMDA and cannabinoid receptors. Neuron 39, 641-654 (2003).
11. Brasier, D.J. & Feldman, D.E. Synapse-specific expression of functional presynaptic NMDA receptors in rat somatosensory cortex. J. Neurosci. 28, 2199-2211 (2008).
12. Bender, V.A., Bender, K.J., Brasier, D.J. & Feldman, D.E. Two coincidence detectors for spike timing-dependent plasticity in somatosensory cortex. J. Neurosci. 26, 4166-4177 (2006).
13. Berretta, N. & Jones, R.S. Tonic facilitation of glutamate release by presynaptic N-methyl-D-aspartate autoreceptors in the entorhinal cortex. Neuroscience 75, 339-344 (1996).
14. Rodríguez-Moreno, A. & Paulsen, O. Spike timing-dependent long-term depression requires presynaptic NMDA receptors. Nat. Neurosci. 11, 744-745 (2008).
15. Yang, J., Woodhall, G.L. & Jones, R.S. Tonic facilitation of glutamate release by presynaptic NR2B-containing NMDA receptors is increased in the entorhinal cortex of chronically epileptic rats. J. Neurosci. 26, 406-410 (2006).
16. Henson, M.A., Roberts, A.C., Perez-Otano, I. & Philpot, B.D. Influence of the NR3A subunit on NMDA receptor functions. Prog. Neurobiol. 91, 23-37 (2010).
17. Karavanova, I., Vasudevan, K., Cheng, J. & Buonanno, A. Novel regional and developmental NMDA receptor expression patterns uncovered in NR2C subunitbeta-galactosidase knock-in mice. Mol. Cell. Neurosci. 34, 468-480 (2007).
18. Nishi, M., Hinds, H., Lu, H.P., Kawata, M. & Hayashi, Y. Motoneuron-specific expression of NR3B, a novel NMDA-type glutamate receptor subunit that works in a dominant-negative manner. J. Neurosci. 21, RC185 (2001).
19. Wong, H.K. et al. Temporal and regional expression of NMDA receptor subunit NR3A in the mammalian brain. J. Comp. Neurol. 450, 303-317 (2002).
20. Roberts, A.C. et al. Downregulation of NR3A-containing NMDARs is required for synapse maturation and memory consolidation. Neuron 63, 342-356 (2009).
21. Laurie, D.J. & Seeburg, P.H. Ligand affinities at recombinant N-methyl-D-aspartate receptors depend on subunit composition. Eur. J. Pharmacol. 268, 335-345 (1994).
22. Laube, B., Hirai, H., Sturgess, M., Betz, H. & Kuhse, J. Molecular determinants of agonist discrimination by NMDA receptor subunits: analysis of the glutamate binding site on the NR2B subunit. Neuron 18, 493-503 (1997).
23. Costa, B.M. et al. N-methyl-D-aspartate (NMDA) receptor NR2 subunit selectivity of a series of novel piperazine-2,3-dicarboxylate derivatives: preferential blockade of extrasynaptic NMDA receptors in the rat hippocampal CA3-CA1 synapse. J. Pharmacol. Exp. Ther. 331, 618-626 (2009).
24. Charton, J.P., Herkert, M., Becker, C.M. & Schroder, H. Cellular and subcellular localization of the 2B-subunit of the NMDA receptor in the adult rat telencephalon. Brain Res. 816, 609-617 (1999).
25. DeBiasi, S., Minelli, A., Melone, M. & Conti, F. Presynaptic NMDA receptors in the neocortex are both auto- and heteroreceptors. Neuroreport 7, 2773-2776 (1996).
26. Li, Y.H., Wang, J. & Zhang, G. Presynaptic NR2B-containing NMDA autoreceptors mediate glutamatergic synaptic transmission in the rat visual cortex. Curr. Neurovasc. Res. 6, 104-109 (2009).
27. Mayford, M. et al. Control of memory formation through regulated expression of a CaMKII transgene. Science 274, 1678-1683 (1996).
28. Pérez-Otaño, I. et al. Endocytosis and synaptic removal of NR3A-containing NMDA receptors by PACSIN1/syndapin1. Nat. Neurosci. 9, 611-621 (2006).
29. Cheetham, C.E. & Fox, K. Presynaptic development at L4 to l2/3 excitatory synapses follows different time courses in visual and somatosensory cortex. J. Neurosci. 30, 12566-12571 (2010).
30. Larsen, R.S., Rao, D., Manis, P.B. & Philpot, B.D. STDP in the developing sensory neocortex. Front. Synaptic Neurosci. 2, 12 (2010).
31. Froemke, R.C., Poo, M.M. & Dan, Y. Spike timing-dependent synaptic plasticity depends on dendritic location. Nature 434, 221-225 (2005).
32. McKinney, R.A., Capogna, M., Durr, R., Gahwiler, B.H. & Thompson, S.M. Miniature synaptic events maintain dendritic spines via AMPA receptor activation. Nat. Neurosci. 2, 44-49 (1999).
33. Smith, S.L. & Trachtenberg, J.T. Experience-dependent binocular competition in the visual cortex begins at eye opening. Nat. Neurosci. 10, 370-375 (2007).
34. Hatton, C.J. & Paoletti, P. Modulation of triheteromeric NMDA receptors by N-terminal domain ligands. Neuron 46, 261-274 (2005).
35. Smothers, C.T. & Woodward, J.J. Effect of the NR3 subunit on ethanol inhibition of recombinant NMDA receptors. Brain Res. 987, 117-121 (2003).
36. Pérez-Otaño, I. et al. Assembly with the NR1 subunit is required for surface expression of NR3A-containing NMDA receptors. J. Neurosci. 21, 1228-1237 (2001).
37. Das, S. et al. Increased NMDA current and spine density in mice lacking the NMDA receptor subunit NR3A. Nature 393, 377-381 (1998).
38. Yao, Y. & Mayer, M.L. Characterization of a soluble ligand binding domain of the NMDA receptor regulatory subunit NR3A. J. Neurosci. 26, 4559-4566 (2006).
39. Piña-Crespo, J.C. et al. Excitatory glycine responses of CNS myelin mediated by NR1/NR3 "NMDA" receptor subunits. J. Neurosci. 30, 11501-11505 (2010).
40. Chatterton, J.E. et al. Excitatory glycine receptors containing the NR3 family of NMDA receptor subunits. Nature 415, 793-798 (2002).
41. Herkert, M., Rottger, S. & Becker, C.M. The NMDA receptor subunit NR2B of neonatal rat brain: complex formation and enrichment in axonal growth cones. Eur. J. Neurosci. 10, 1553-1562 (1998).
42. McGuinness, L. et al. Presynaptic NMDARs in the hippocampus facilitate transmitter release at theta frequency. Neuron 68, 1109-1127 (2010).
43. Mameli, M., Carta, M., Partridge, L.D. & Valenzuela, C.F. Neurosteroid-induced plasticity of immature synapses via retrograde modulation of presynaptic NMDA receptors. J. Neurosci. 25, 2285-2294 (2005).
44. Christie, J.M. & Jahr, C.E. Dendritic NMDA receptors activate axonal calcium channels. Neuron 60, 298-307 (2008).
45. Christie, J.M. & Jahr, C.E. Selective expression of ligand-gated ion channels in L5 pyramidal cell axons. J. Neurosci. 29, 11441-11450 (2009).
46. Lin, H. et al. Axonal á7 nicotinic ACh receptors modulate presynaptic NMDA receptor expression and structural plasticity of glutamatergic presynaptic boutons. Proc. Natl. Acad. Sci. USA 107, 16661-16666 (2010).
47. Ikeda, K. et al. Reduced spontaneous activity of mice defective in the epsilon 4 subunit of the NMDA receptor channel. Brain Res. Mol. Brain Res. 33, 61-71 (1995).
48. Li, Y.H. & Han, T.Z. Glycine binding sites of presynaptic NMDA receptors may tonically regulate glutamate release in the rat visual cortex. J. Neurophysiol. 97, 817-823 (2007).
49. Kharazia, V.N. & Weinberg, R.J. Immunogold localization of AMPA and NMDA receptors in somatic sensory cortex of albino rat. J. Comp. Neurol. 412, 292-302 (1999).
50. Jacob, A.L., Jordan, B.A. & Weinberg, R.J. Organization of amyloid-beta protein precursor intracellular domain-associated protein-1 in the rat brain. J. Comp. Neurol. 518, 3221-3236 (2010).