Co-agonists differentially tune GluN2B-NMDA receptor trafficking at hippocampal synapses

eLife - Tập 6
Joana S. Ferreira1,2, Thomas Papouin3,3,4, Laurent Ladépêche1,2, Andrea Yao5, Valentin Langlais3,3, Delphine Bouchet1,2, Jérôme Dulong3,2, Jean‐Pierre Mothet6, Silvia Sacchi7,8, Loredano Pollegioni7,8, Pierre Paoletti5, Stéphane H. R. Oliet3,3, Laurent Groc1
1Interdisciplinary Institute for NeuroSciences, CNRS UMR 5297, Bordeaux, France;
2Université de Bordeaux, Bordeaux, France
3NSERM U862, Neurocentre Magendie, Bordeaux, France
4Neuroscience department, Tufts University School of Medicine, Boston, United States
5Institut de Biologie de l'ENS (IBENS), CNRS UMR 8197, INSERM U1024, Paris, France;
6Université Aix-Marseille, CNRS CRN2M UMR 7286, Marseille, France
7Dipartimento di Biotecnologie e Scienze della Vita, Universita’ degli Studi dell’Insubria, Varese, Italy
8The Protein Factory, Centro Interuniversitario di Biotecnologie Proteiche, Politecnico di Milano, Universita `degli Studi dell'Insubria, Varese, Italy

Tóm tắt

The subunit composition of synaptic NMDA receptors (NMDAR), such as the relative content of GluN2A- and GluN2B-containing receptors, greatly influences the glutamate synaptic transmission. Receptor co-agonists, glycine and D-serine, have intriguingly emerged as potential regulators of the receptor trafficking in addition to their requirement for its activation. Using a combination of single-molecule imaging, biochemistry and electrophysiology, we show that glycine and D-serine relative availability at rat hippocampal glutamatergic synapses regulate the trafficking and synaptic content of NMDAR subtypes. Acute manipulations of co-agonist levels, both ex vivo and in vitro, unveil that D-serine alter the membrane dynamics and content of GluN2B-NMDAR, but not GluN2A-NMDAR, at synapses through a process requiring PDZ binding scaffold partners. In addition, using FRET-based FLIM approach, we demonstrate that D-serine rapidly induces a conformational change of the GluN1 subunit intracellular C-terminus domain. Together our data fuels the view that the extracellular microenvironment regulates synaptic NMDAR signaling.

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Tài liệu tham khảo

Aow, 2015, Conformational signaling required for synaptic plasticity by the NMDA receptor complex, PNAS, 112, 14711, 10.1073/pnas.1520029112

Balu, 2011, Glutamate receptor composition of the post-synaptic density is altered in genetic mouse models of NMDA receptor hypo- and hyperfunction, Brain Research, 1392, 1, 10.1016/j.brainres.2011.03.051

Balu, 2015, The NMDA receptor 'glycine modulatory site' in schizophrenia: D-serine, glycine, and beyond, Current Opinion in Pharmacology, 20, 109, 10.1016/j.coph.2014.12.004

Bard, 2010, Dynamic and specific interaction between synaptic NR2-NMDA receptor and PDZ proteins, PNAS, 107, 19561, 10.1073/pnas.1002690107

Bard, 2011, Glutamate receptor dynamics and protein interaction: lessons from the NMDA receptor, Molecular and Cellular Neuroscience, 48, 298, 10.1016/j.mcn.2011.05.009

Barria, 2002, Subunit-specific NMDA receptor trafficking to synapses, Neuron, 35, 345, 10.1016/S0896-6273(02)00776-6

Barth, 2001, NMDAR EPSC kinetics do not regulate the critical period for LTP at thalamocortical synapses, Nature Neuroscience, 4, 235, 10.1038/85070

Basu, 2009, Targeted disruption of serine racemase affects glutamatergic neurotransmission and behavior, Molecular Psychiatry, 14, 719, 10.1038/mp.2008.130

Bellone, 2007, Rapid bidirectional switching of synaptic NMDA receptors, Neuron, 55, 779, 10.1016/j.neuron.2007.07.035

Bellone, 2011, In utero exposure to cocaine delays postnatal synaptic maturation of glutamatergic transmission in the VTA, Nature Neuroscience, 14, 1439, 10.1038/nn.2930

Bouvier, 2015, Presynaptic NMDA receptors: Roles and rules, Neuroscience, 311, 322, 10.1016/j.neuroscience.2015.10.033

Burnet, 2011, D-amino acid oxidase knockdown in the mouse cerebellum reduces NR2A mRNA, Molecular and Cellular Neuroscience, 46, 167, 10.1016/j.mcn.2010.08.018

Chen, 2008, Modulation of glycine potency in rat recombinant NMDA receptors containing chimeric NR2A/2D subunits expressed in xenopus laevis oocytes, The Journal of Physiology, 586, 227, 10.1113/jphysiol.2007.143172

Chen, 2012, SAP102 Mediates synaptic clearance of NMDA receptors, Cell Reports, 2, 1120, 10.1016/j.celrep.2012.09.024

Dore, 2015, Agonist binding to the NMDA receptor drives movement of its cytoplasmic domain without ion flow, PNAS, 112, 14705, 10.1073/pnas.1520023112

Doré, 2014, FRET-FLIM investigation of PSD95-NMDA receptor interaction in dendritic spines; control by calpain, CaMKII and src family kinase, PLoS One, 9, e112170, 10.1371/journal.pone.0112170

Dupuis, 2014, Surface dynamics of GluN2B-NMDA receptors controls plasticity of maturing glutamate synapses, The EMBO Journal, 33, 842, 10.1002/embj.201386356

Ehlers, 2007, Diffusional trapping of GluR1 AMPA receptors by input-specific synaptic activity, Neuron, 54, 447, 10.1016/j.neuron.2007.04.010

Elias, 2007, Synaptic trafficking of glutamate receptors by MAGUK scaffolding proteins, Trends in Cell Biology, 17, 343, 10.1016/j.tcb.2007.07.005

Ferreira, 2015, GluN2B-Containing NMDA receptors regulate AMPA receptor traffic through anchoring of the synaptic proteasome, Journal of Neuroscience, 35, 8462, 10.1523/JNEUROSCI.3567-14.2015

Fossat, 2012, Glial D-serine gates NMDA receptors at excitatory synapses in prefrontal cortex, Cerebral Cortex, 22, 595, 10.1093/cercor/bhr130

Groc, 2004, Differential activity-dependent regulation of the lateral mobilities of AMPA and NMDA receptors, Nature Neuroscience, 7, 695, 10.1038/nn1270

Groc, 2006, NMDA receptor surface mobility depends on NR2A-2B subunits, PNAS, 103, 18769, 10.1073/pnas.0605238103

Groc, 2007, NMDA receptor surface trafficking and synaptic subunit composition are developmentally regulated by the extracellular matrix protein Reelin, Journal of Neuroscience, 27, 10165, 10.1523/JNEUROSCI.1772-07.2007

Henneberger, 2010, Long-term potentiation depends on release of D-serine from astrocytes, Nature, 463, 232, 10.1038/nature08673

Imamura, 2008, Sustained saturating level of glycine induces changes in NR2B-containing-NMDA receptor localization in the CA1 region of the Hippocampus, Journal of Neurochemistry, 105, 2454, 10.1111/j.1471-4159.2008.05324.x

Job, 2002, Overexpression of a recombinant wild-type and His-tagged Bacillus subtilis glycine oxidase in Escherichia coli, European Journal of Biochemistry, 269, 1456, 10.1046/j.1432-1033.2002.02790.x

Lau, 2007, NMDA receptor trafficking in synaptic plasticity and neuropsychiatric disorders, Nature Reviews Neuroscience, 8, 1, 10.1038/nrn2171

Le Bail, 2015, Identity of the NMDA receptor coagonist is synapse specific and developmentally regulated in the hippocampus, PNAS, 112, E204, 10.1073/pnas.1416668112

Li, 2004, The importance of dendritic mitochondria in the morphogenesis and plasticity of spines and synapses, Cell, 119, 873, 10.1016/j.cell.2004.11.003

Martina, 2005, Reduced glycine transporter type 1 expression leads to major changes in glutamatergic neurotransmission of CA1 hippocampal neurones in mice, The Journal of Physiology, 563, 777, 10.1113/jphysiol.2004.080655

Matta, 2011, mGluR5 and NMDA receptors drive the experience- and activity-dependent NMDA receptor NR2B to NR2A subunit switch, Neuron, 70, 339, 10.1016/j.neuron.2011.02.045

Monyer, 1994, Developmental and regional expression in the rat brain and functional properties of four NMDA receptors, Neuron, 12, 529, 10.1016/0896-6273(94)90210-0

Nabavi, 2013, Metabotropic NMDA receptor function is required for NMDA receptor-dependent long-term depression, PNAS, 110, 4027, 10.1073/pnas.1219454110

Nolt, 2011, EphB controls NMDA receptor function and synaptic targeting in a subunit-specific manner, Journal of Neuroscience, 31, 5353, 10.1523/JNEUROSCI.0282-11.2011

Nong, 2003, Glycine binding primes NMDA receptor internalization, Nature, 422, 302, 10.1038/nature01497

Oliet, 2009, Regulation of N-methyl-D-aspartate receptors by astrocytic D-serine, Neuroscience, 158, 275, 10.1016/j.neuroscience.2008.01.071

Paoletti, 1997, High-affinity zinc inhibition of NMDA NR1-NR2A receptors, Journal of Neuroscience, 17, 5711, 10.1523/JNEUROSCI.17-15-05711.1997

Paoletti, 2007, NMDA receptor subunits: function and pharmacology, Current Opinion in Pharmacology, 7, 39, 10.1016/j.coph.2006.08.011

Paoletti, 2013, NMDA receptor subunit diversity: impact on receptor properties, synaptic plasticity and disease, Nature Reviews Neuroscience, 14, 383, 10.1038/nrn3504

Papouin, 2012, Synaptic and extrasynaptic NMDA receptors are gated by different endogenous coagonists, Cell, 150, 633, 10.1016/j.cell.2012.06.029

Piguel, 2014, Scribble1/AP2 complex coordinates NMDA receptor endocytic recycling, Cell Reports, 9, 712, 10.1016/j.celrep.2014.09.017

Pollegioni, 1992, Specificity and kinetics of rhodotorula gracilis D-amino acid oxidase, Biochimica Et Biophysica Acta (BBA) - Protein Structure and Molecular Enzymology, 1120, 11, 10.1016/0167-4838(92)90418-D

Potier, 2016, Temporal memory and its enhancement by estradiol requires surface dynamics of hippocampal CA1 N-methyl-d-aspartate receptors, Biological Psychiatry, 79, 735, 10.1016/j.biopsych.2015.07.017

Priestley, 1995, Pharmacological properties of recombinant human N-methyl-D-aspartate receptors comprising NR1a/NR2A and NR1a/NR2B subunit assemblies expressed in permanently transfected mouse fibroblast cells, Molecular Pharmacology, 48, 841

Prybylowski, 2005, The synaptic localization of NR2B-containing NMDA receptors is controlled by interactions with PDZ proteins and AP-2, Neuron, 47, 845, 10.1016/j.neuron.2005.08.016

Roche, 2001, ‘No Title’, Nature Neuroscience, 4, 794, 10.1038/90498

Rodenas-Ruano, 2012, REST-dependent epigenetic remodeling promotes the developmental switch in synaptic NMDA receptors, Nature Neuroscience, 15, 1382, 10.1038/nn.3214

Rosenberg, 2013, Neuronal D-serine and glycine release via the Asc-1 transporter regulates NMDA receptor-dependent synaptic activity, Journal of Neuroscience, 33, 3533, 10.1523/JNEUROSCI.3836-12.2013

Scott, 2004, Endocytosis and degradative sorting of NMDA receptors by conserved membrane-proximal signals, Journal of Neuroscience, 24, 7096, 10.1523/JNEUROSCI.0780-04.2004

Sheng, 1994, Changing subunit composition of heteromeric NMDA receptors during development of rat cortex, Nature, 368, 144, 10.1038/368144a0

Sonia, 2001, Engineering, expression and purification of a his-tagged chimeric D-amino acid oxidase from rhodotorula gracilis, Enzyme and Microbial Technology, 29, 407, 10.1016/S0141-0229(01)00400-8

Sullivan, 2012, AMPA receptor-dependent, light-evoked D-serine release acts on retinal ganglion cell NMDA receptors, Journal of Neurophysiology, 108, 1044, 10.1152/jn.00264.2012

Vieira, 2016, Multiple domains in the C-terminus of NMDA receptor GluN2B subunit contribute to neuronal death following in vitro ischemia, Neurobiology of Disease, 89, 223, 10.1016/j.nbd.2015.11.007

Wafford, 1995, Identification of amino acids in the N-methyl-D-aspartate receptor NR1 subunit that contribute to the glycine binding site, Molecular Pharmacology, 47, 374

Yang, 2003, Contribution of astrocytes to hippocampal long-term potentiation through release of D-serine, PNAS, 100, 15194, 10.1073/pnas.2431073100

Yashiro, 2008, Regulation of NMDA receptor subunit expression and its implications for LTD, LTP, and metaplasticity, Neuropharmacology, 55, 1081, 10.1016/j.neuropharm.2008.07.046

Zhu, 2015, Allosteric modulators of NMDA receptors: multiple sites and mechanisms, Current Opinion in Pharmacology, 20, 14, 10.1016/j.coph.2014.10.009