Conformational pathway provides unique sensitivity to a synaptic mGluR

Habrian, Chris H.; Levitz, Joshua; Vyklicky, Vojtech; Fu, Zhu; Hoagland, Adam; McCort-Tranchepain, Isabelle; Acher, Francine; Isacoff, Ehud Y.

doi:10.1038/s41467-019-13407-8

Conformational pathway provides unique sensitivity to a synaptic mGluR

Journal Article · Thu Dec 05 00:00:00 EST 2019 · Nature Communications

DOI:https://doi.org/10.1038/s41467-019-13407-8· OSTI ID:1591846

Habrian, Chris H. ^[1]; Levitz, Joshua ^[2]; ^[1]; Fu, Zhu ^[1]; Hoagland, Adam ^[1]; McCort-Tranchepain, Isabelle ^[3]; ^[3]; Isacoff, Ehud Y. ^[4]

Univ. of California, Berkeley, CA (United States)
Univ. of California, Berkeley, CA (United States); Weill Cornell Medical College, New York, NY (United States)
Paris Descartes Univ. (France)
Univ. of California, Berkeley, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)

Metabotropic glutamate receptors (mGluRs) are dimeric G-protein-coupled receptors that operate at synapses. Macroscopic and single molecule FRET to monitor structural rearrangements in the ligand binding domain (LBD) of the mGluR7/7 homodimer revealed it to have an apparent affinity ~4000-fold lower than other mGluRs and a maximal activation of only ~10%, seemingly too low for activation at synapses. However, mGluR7 heterodimerizes, and we find it to associate with mGluR2 in the hippocampus. Strikingly, the mGluR2/7 heterodimer has high affinity and efficacy. mGluR2/7 shows cooperativity in which an unliganded subunit greatly enhances activation by agonist bound to its heteromeric partner, and a unique conformational pathway to activation, in which mGluR2/7 partially activates in the Apo state, even when its LBDs are held open by antagonist. High sensitivity and an unusually broad dynamic range should enable mGluR2/7 to respond to both glutamate transients from nearby release and spillover from distant synapses.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1591846

Journal Information:: Nature Communications, Journal Name: Nature Communications Journal Issue: 1 Vol. 10; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

References (80)

Distributions of the mRNAs for L-2-amino-4-phosphonobutyrate-sensitive metabotropic glutamate receptors, mGluR4 and mGluR7, in the rat brain Ohishi, Hitoshi; Akazawa, Chihiro; Shigemoto, Ryuichi The Journal of Comparative Neurology, Vol. 360, Issue 4 https://doi.org/10.1002/cne.903600402	journal	October 1995
Distribution of metabotropic glutamate receptor 7 messenger RNA in the developing and adult rat brain Kinzie, J. M.; Saugstad, J. A.; Westbrook, G. L. Neuroscience, Vol. 69, Issue 1 https://doi.org/10.1016/0306-4522(95)00244-d	journal	November 1995
Lack of the metabotropic glutamate receptor subtype 7 selectively impairs short-term working memory but not long-term memory Hölscher, Christian; Schmid, Susanne; Pilz, Peter K. D. Behavioural Brain Research, Vol. 154, Issue 2 https://doi.org/10.1016/j.bbr.2004.03.015	journal	October 2004
Kinetics and mechanism of G protein-coupled receptor activation Lohse, Martin J.; Maiellaro, Isabella; Calebiro, Davide Current Opinion in Cell Biology, Vol. 27 https://doi.org/10.1016/j.ceb.2013.11.009	journal	April 2014
The role of protein dynamics in GPCR function: insights from the β2AR and rhodopsin Manglik, Aashish; Kobilka, Brian Current Opinion in Cell Biology, Vol. 27 https://doi.org/10.1016/j.ceb.2014.01.008	journal	April 2014
The Dynamic Process of β2-Adrenergic Receptor Activation Nygaard, Rie; Zou, Yaozhong; Dror, Ron O. Cell, Vol. 152, Issue 3 https://doi.org/10.1016/j.cell.2013.01.008	journal	January 2013
Noise reduction in single-molecule fluorescence trajectories of folding proteins Haran, Gilad Chemical Physics, Vol. 307, Issue 2-3 https://doi.org/10.1016/j.chemphys.2004.05.017	journal	December 2004
Therapeutic potential of group III metabotropic glutamate receptor ligands in pain Acher, Francine; Goudet, Cyril Current Opinion in Pharmacology, Vol. 20 https://doi.org/10.1016/j.coph.2014.11.007	journal	February 2015
Dynamics and modulation of metabotropic glutamate receptors Rondard, Philippe; Pin, Jean-Philippe Current Opinion in Pharmacology, Vol. 20 https://doi.org/10.1016/j.coph.2014.12.001	journal	February 2015
The therapeutic potential of metabotropic glutamate receptor modulation for schizophrenia Stansley, Branden J.; Conn, P. Jeffrey Current Opinion in Pharmacology, Vol. 38 https://doi.org/10.1016/j.coph.2018.02.003	journal	February 2018
How to Dismantle a Detonator Synapse Pelkey, Kenneth A.; McBain, Chris J. Neuron, Vol. 45, Issue 3 https://doi.org/10.1016/j.neuron.2005.01.018	journal	February 2005
mGluR7 Is a Metaplastic Switch Controlling Bidirectional Plasticity of Feedforward Inhibition Pelkey, Kenneth A.; Lavezzari, Gabriela; Racca, Claudia Neuron, Vol. 46, Issue 1 https://doi.org/10.1016/j.neuron.2005.02.011	journal	April 2005
Mechanism of Assembly and Cooperativity of Homomeric and Heteromeric Metabotropic Glutamate Receptors Levitz, Joshua; Habrian, Chris; Bharill, Shashank Neuron, Vol. 92, Issue 1 https://doi.org/10.1016/j.neuron.2016.08.036	journal	October 2016
The intra-molecular activation mechanisms of the dimeric metabotropic glutamate receptor 1 differ depending on the type of G proteins Tateyama, Michihiro; Kubo, Yoshihiro Neuropharmacology, Vol. 61, Issue 4 https://doi.org/10.1016/j.neuropharm.2011.05.031	journal	September 2011
A novel mGlu4 selective agonist LSP4-2022 increases behavioral despair in mouse models of antidepressant action Podkowa, Karolina; Rzeźniczek, Szymon; Marciniak, Marcin Neuropharmacology, Vol. 97 https://doi.org/10.1016/j.neuropharm.2015.05.039	journal	October 2015
Deficits in acquisition and extinction of conditioned responses in mGluR7 knockout mice Goddyn, Hannelore; Callaerts-Vegh, Zsuzsanna; Stroobants, Stijn Neurobiology of Learning and Memory, Vol. 90, Issue 1 https://doi.org/10.1016/j.nlm.2008.01.001	journal	July 2008
Subcellular Organization of GPCR Signaling Eichel, Kelsie; von Zastrow, Mark Trends in Pharmacological Sciences, Vol. 39, Issue 2 https://doi.org/10.1016/j.tips.2017.11.009	journal	February 2018
Molecular characterization of a new metabotropic glutamate receptor mGluR7 coupled to inhibitory cyclic AMP signal transduction. Okamoto, N.; Hori, S.; Akazawa, C. Journal of Biological Chemistry, Vol. 269, Issue 2 https://doi.org/10.1016/s0021-9258(17)42247-2	journal	January 1994
Comparative effect of l-CCG-I, DCG-IV and γ-carboxy-l-glutamate on all cloned metabotropic glutamate receptor subtypes Brabet, Isabelle; Parmentier, Marie-Laure; De Colle, Cyril Neuropharmacology, Vol. 37, Issue 8 https://doi.org/10.1016/s0028-3908(98)00091-4	journal	August 1998
Synthesis of heterocyclic enol ethers and their use as group 2 metabotropic glutamate receptor antagonists Kolczewski, Sabine; Adam, Geo; Stadler, Heinz Bioorganic & Medicinal Chemistry Letters, Vol. 9, Issue 15 https://doi.org/10.1016/s0960-894x(99)00346-7	journal	August 1999
Increased Potency and Selectivity for Group III Metabotropic Glutamate Receptor Agonists Binding at Dual sites Selvam, Chelliah; Lemasson, Isabelle A.; Brabet, Isabelle Journal of Medicinal Chemistry, Vol. 61, Issue 5 https://doi.org/10.1021/acs.jmedchem.7b01438	journal	January 2018
Orthogonal Optical Control of a G Protein-Coupled Receptor with a SNAP-Tethered Photochromic Ligand Broichhagen, Johannes; Damijonaitis, Arunas; Levitz, Joshua ACS Central Science, Vol. 1, Issue 7 https://doi.org/10.1021/acscentsci.5b00260	journal	October 2015
Constitutive activation of opsin: Influence of charge at position 134 and size at position 296 Cohen, George B.; Yang, Tong; Robinson, Phyllis R. Biochemistry, Vol. 32, Issue 23 https://doi.org/10.1021/bi00074a024	journal	June 1993
Crystal structure of the β2 adrenergic receptor–Gs protein complex Rasmussen, Søren G. F.; DeVree, Brian T.; Zou, Yaozhong Nature, Vol. 477, Issue 7366 https://doi.org/10.1038/nature10361	journal	July 2011
Molecular signatures of G-protein-coupled receptors Venkatakrishnan, A. J.; Deupi, Xavier; Lebon, Guillaume Nature, Vol. 494, Issue 7436 https://doi.org/10.1038/nature11896	journal	February 2013
Conformational dynamics of a class C G-protein-coupled receptor Vafabakhsh, Reza; Levitz, Joshua; Isacoff, Ehud Y. Nature, Vol. 524, Issue 7566 https://doi.org/10.1038/nature14679	journal	August 2015
Propagation of conformational changes during μ-opioid receptor activation Sounier, Rémy; Mas, Camille; Steyaert, Jan Nature, Vol. 524, Issue 7565 https://doi.org/10.1038/nature14680	journal	August 2015
Single-molecule analysis of ligand efficacy in β2AR–G-protein activation Gregorio, G. Glenn; Masureel, Matthieu; Hilger, Daniel Nature, Vol. 547, Issue 7661 https://doi.org/10.1038/nature22354	journal	June 2017
Major ligand-induced rearrangement of the heptahelical domain interface in a GPCR dimer Xue, Li; Rovira, Xavier; Scholler, Pauline Nature Chemical Biology, Vol. 11, Issue 2 https://doi.org/10.1038/nchembio.1711	journal	December 2014
Optical control of metabotropic glutamate receptors Levitz, Joshua; Pantoja, Carlos; Gaub, Benjamin Nature Neuroscience, Vol. 16, Issue 4 https://doi.org/10.1038/nn.3346	journal	March 2013
Closed state of both binding domains of homodimeric mGlu receptors is required for full activity Kniazeff, Julie; Bessis, Anne-Sophie; Maurel, Damien Nature Structural & Molecular Biology, Vol. 11, Issue 8 https://doi.org/10.1038/nsmb794	journal	July 2004
Mechanisms of photoswitch conjugation and light activation of an ionotropic glutamate receptor Gorostiza, P.; Volgraf, M.; Numano, R. Proceedings of the National Academy of Sciences, Vol. 104, Issue 26 https://doi.org/10.1073/pnas.0701274104	journal	June 2007
Optical measurement of synaptic glutamate spillover and reuptake by linker optimized glutamate-sensitive fluorescent reporters Hires, S. A.; Zhu, Y.; Tsien, R. Y. Proceedings of the National Academy of Sciences, Vol. 105, Issue 11 https://doi.org/10.1073/pnas.0712008105	journal	March 2008
Pathway and mechanism of drug binding to G-protein-coupled receptors Dror, Ron O.; Pan, Albert C.; Arlow, Daniel H. Proceedings of the National Academy of Sciences, Vol. 108, Issue 32 https://doi.org/10.1073/pnas.1104614108	journal	July 2011
Distinct roles of metabotropic glutamate receptor dimerization in agonist activation and G-protein coupling El Moustaine, D.; Granier, S.; Doumazane, E. Proceedings of the National Academy of Sciences, Vol. 109, Issue 40 https://doi.org/10.1073/pnas.1205838109	journal	September 2012
Dual optical control and mechanistic insights into photoswitchable group II and III metabotropic glutamate receptors Levitz, Joshua; Broichhagen, Johannes; Leippe, Philipp Proceedings of the National Academy of Sciences, Vol. 114, Issue 17 https://doi.org/10.1073/pnas.1619652114	journal	April 2017
Molecular Determinants of High Affinity Binding to Group III Metabotropic Glutamate Receptors Rosemond, Erica; Peltekova, Vanya; Naples, Mark Journal of Biological Chemistry, Vol. 277, Issue 9 https://doi.org/10.1074/jbc.m110476200	journal	December 2001
A novel selective metabotropic glutamate receptor 4 agonist reveals new possibilities for developing subtype selective ligands with therapeutic potential Goudet, Cyril; Vilar, Bruno; Courtiol, Tiphanie The FASEB Journal, Vol. 26, Issue 4 https://doi.org/10.1096/fj.11-195941	journal	December 2011
Activation of Metabotropic Glutamate Receptor 1 Dimers Requires Glutamate Binding in Both Subunits Kammermeier, Paul J.; Yun, June Journal of Pharmacology and Experimental Therapeutics, Vol. 312, Issue 2 https://doi.org/10.1124/jpet.104.073155	journal	October 2004
A Novel Family of Potent Negative Allosteric Modulators of Group II Metabotropic Glutamate Receptors Hemstapat, Kamondanai; Da Costa, Herve; Nong, Yi Journal of Pharmacology and Experimental Therapeutics, Vol. 322, Issue 1 https://doi.org/10.1124/jpet.106.117093	journal	April 2007
ADX71743, a Potent and Selective Negative Allosteric Modulator of Metabotropic Glutamate Receptor 7: In Vitro and In Vivo Characterization Kalinichev, Mikhail; Rouillier, Mélanie; Girard, Francoise Journal of Pharmacology and Experimental Therapeutics, Vol. 344, Issue 3 https://doi.org/10.1124/jpet.112.200915	journal	December 2012
Glutamate Receptor Ion Channels: Structure, Regulation, and Function Traynelis, Stephen F.; Wollmuth, Lonnie P.; McBain, Chris J. Pharmacological Reviews, Vol. 62, Issue 3 https://doi.org/10.1124/pr.109.002451	journal	August 2010
Structural Basis for Allosteric Regulation of GPCRs by Sodium Ions Liu, W.; Chun, E.; Thompson, A. A. Science, Vol. 337, Issue 6091 https://doi.org/10.1126/science.1219218	journal	July 2012
The time course of glutamate in the synaptic cleft Clements, J.; Lester, R.; Tong, G. Science, Vol. 258, Issue 5087 https://doi.org/10.1126/science.1359647	journal	November 1992
The Molecular Basis of G Protein–Coupled Receptor Activation Weis, William I.; Kobilka, Brian K. Annual Review of Biochemistry, Vol. 87, Issue 1 https://doi.org/10.1146/annurev-biochem-060614-033910	journal	June 2018
Structural Basis for G Protein–Coupled Receptor Signaling Erlandson, Sarah C.; McMahon, Conor; Kruse, Andrew C. Annual Review of Biophysics, Vol. 47, Issue 1 https://doi.org/10.1146/annurev-biophys-070317-032931	journal	May 2018
Metabotropic Glutamate Receptors: Physiology, Pharmacology, and Disease Niswender, Colleen M.; Conn, P. Jeffrey Annual Review of Pharmacology and Toxicology, Vol. 50, Issue 1 https://doi.org/10.1146/annurev.pharmtox.011008.145533	journal	February 2010
Pharmacology and Functions of Metabotropic Glutamate Receptors Conn, P. Jeffrey; Pin, Jean-Philippe Annual Review of Pharmacology and Toxicology, Vol. 37, Issue 1 https://doi.org/10.1146/annurev.pharmtox.37.1.205	journal	April 1997
Dopamine Receptors: From Structure to Function Missale, Cristina; Nash, S. Russel; Robinson, Susan W. Physiological Reviews, Vol. 78, Issue 1 https://doi.org/10.1152/physrev.1998.78.1.189	journal	January 1998
The role of metabotropic glutamate receptor 5 in learning and memory processes Simonyi, A.; Schachtman, T. R.; Christoffersen, G. R. J. Drug News & Perspectives, Vol. 18, Issue 6 https://doi.org/10.1358/dnp.2005.18.6.927927	journal	January 2005
Compartmental Localization of a Metabotropic Glutamate Receptor (mGluR7): Two Different Active Sites at a Retinal Synapse Brandstätter, Johann Helmut; Koulen, Peter; Kuhn, Rainer The Journal of Neuroscience, Vol. 16, Issue 15 https://doi.org/10.1523/jneurosci.16-15-04749.1996	journal	August 1996
Differential Presynaptic Localization of Metabotropic Glutamate Receptor Subtypes in the Rat Hippocampus Shigemoto, Ryuichi; Kinoshita, Ayae; Wada, Eiki The Journal of Neuroscience, Vol. 17, Issue 19 https://doi.org/10.1523/jneurosci.17-19-07503.1997	journal	October 1997
Metabotropic Glutamate Receptor Subtype 7 Ablation Causes Deficit in Fear Response and Conditioned Taste Aversion Masugi, Miwako; Yokoi, Mineto; Shigemoto, Ryuichi The Journal of Neuroscience, Vol. 19, Issue 3 https://doi.org/10.1523/jneurosci.19-03-00955.1999	journal	February 1999
The Concentration of Synaptically Released Glutamate Outside of the Climbing Fiber–Purkinje Cell Synaptic Cleft Dzubay, Jeffrey A.; Jahr, Craig E. The Journal of Neuroscience, Vol. 19, Issue 13 https://doi.org/10.1523/jneurosci.19-13-05265.1999	journal	July 1999
Probing Heterotrimeric G Protein Activation: Applications to Biased Ligands Denis, Colette; Sauliere, Aude; Galandrin, Segolene Current Pharmaceutical Design, Vol. 18, Issue 2 https://doi.org/10.2174/138161212799040466	journal	January 2012
Therapeutic Potential of Metabotropic Glutamate Receptor Modulators Hovelso, N.; Sotty, F.; P. Montezinho, L. Current Neuropharmacology, Vol. 10, Issue 1 https://doi.org/10.2174/157015912799362805	journal	March 2012
Extracellular Glutamate: Functional Compartments Operate in Different Concentration Ranges Moussawi, Khaled; Riegel, Arthur; Nair, Satish Frontiers in Systems Neuroscience, Vol. 5 https://doi.org/10.3389/fnsys.2011.00094	journal	January 2011
Distribution of metabotropic glutamate receptor 7 messenger RNA in the developing and adult rat brain Kinzie, J. M.; Saugstad, J. A.; Westbrook, G. L. Neuroscience, Vol. 69, Issue 1 https://doi.org/10.1016/0306-4522(95)00244-D	journal	November 1995
Molecular characterization of a new metabotropic glutamate receptor mGluR7 coupled to inhibitory cyclic AMP signal transduction. Okamoto, N.; Hori, S.; Akazawa, C. Journal of Biological Chemistry, Vol. 269, Issue 2 https://doi.org/10.1016/S0021-9258(17)42247-2	journal	January 1994
Comparative effect of l-CCG-I, DCG-IV and γ-carboxy-l-glutamate on all cloned metabotropic glutamate receptor subtypes Brabet, Isabelle; Parmentier, Marie-Laure; De Colle, Cyril Neuropharmacology, Vol. 37, Issue 8 https://doi.org/10.1016/S0028-3908(98)00091-4	journal	August 1998
Synthesis of heterocyclic enol ethers and their use as group 2 metabotropic glutamate receptor antagonists Kolczewski, Sabine; Adam, Geo; Stadler, Heinz Bioorganic & Medicinal Chemistry Letters, Vol. 9, Issue 15 https://doi.org/10.1016/S0960-894X(99)00346-7	journal	August 1999
Pathway and Mechanism of Drug Binding to G-Protein-Coupled Receptors Dror, Ron O.; Pan, Albert C.; Arlow, Daniel H. Biophysical Journal, Vol. 102, Issue 3 https://doi.org/10.1016/j.bpj.2011.11.2241	journal	January 2012
Backbone NMR reveals allosteric signal transduction networks in the β1-adrenergic receptor Isogai, Shin; Deupi, Xavier; Opitz, Christian Nature, Vol. 530, Issue 7589 https://doi.org/10.1038/nature16577	journal	February 2016
Organization and functions of mGlu and GABAB receptor complexes Pin, Jean-Philippe; Bettler, Bernhard Nature, Vol. 540, Issue 7631 https://doi.org/10.1038/nature20566	journal	December 2016
Fine tuning of sub-millisecond conformational dynamics controls metabotropic glutamate receptors agonist efficacy Olofsson, Linnea; Felekyan, Suren; Doumazane, Etienne Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms6206	journal	October 2014
Structural insights into the activation of metabotropic glutamate receptors Koehl, Antoine; Hu, Hongli; Feng, Dan Nature, Vol. 566, Issue 7742 https://doi.org/10.1038/s41586-019-0881-4	journal	January 2019
Role of the Second and Third Intracellular Loops of Metabotropic Glutamate Receptors in Mediating Dual Signal Transduction Activation Francesconi, Anna; Duvoisin, Robert M. Journal of Biological Chemistry, Vol. 273, Issue 10 https://doi.org/10.1074/jbc.273.10.5615	journal	March 1998
Molecular Determinants of High Affinity Binding to Group III Metabotropic Glutamate Receptors Rosemond, Erica; Peltekova, Vanya; Naples, Mark Journal of Biological Chemistry, Vol. 277, Issue 9 https://doi.org/10.1074/jbc.M110476200	journal	December 2001
Activation of a Dimeric Metabotropic Glutamate Receptor by Intersubunit Rearrangement Brock, Carsten; Oueslati, Nadia; Soler, Stéphan Journal of Biological Chemistry, Vol. 282, Issue 45 https://doi.org/10.1074/jbc.M702542200	journal	September 2007
A new approach to analyze cell surface protein complexes reveals specific heterodimeric metabotropic glutamate receptors Doumazane, Etienne; Scholler, Pauline; Zwier, Jurriaan M. The FASEB Journal, Vol. 25, Issue 1 https://doi.org/10.1096/fj.10-163147	journal	September 2010
Structural Basis for a Ca2+-Sensing Function of the Metabotropic Glutamate Receptors Kubo, Y. Science, Vol. 279, Issue 5357 https://doi.org/10.1126/science.279.5357.1722	journal	March 1998
Structure-Function of the G Protein–Coupled Receptor Superfamily Katritch, Vsevolod; Cherezov, Vadim; Stevens, Raymond C. Annual Review of Pharmacology and Toxicology, Vol. 53, Issue 1 https://doi.org/10.1146/annurev-pharmtox-032112-135923	journal	January 2013
Selective Actions of Novel Allosteric Modulators Reveal Functional Heteromers of Metabotropic Glutamate Receptors in the CNS Yin, S.; Noetzel, M. J.; Johnson, K. A. Journal of Neuroscience, Vol. 34, Issue 1 https://doi.org/10.1523/JNEUROSCI.1129-13.2014	journal	December 2013
Compartmental Localization of a Metabotropic Glutamate Receptor (mGluR7): Two Different Active Sites at a Retinal Synapse Brandstätter, Johann Helmut; Koulen, Peter; Kuhn, Rainer The Journal of Neuroscience, Vol. 16, Issue 15 https://doi.org/10.1523/JNEUROSCI.16-15-04749.1996	journal	August 1996
Differential Presynaptic Localization of Metabotropic Glutamate Receptor Subtypes in the Rat Hippocampus Shigemoto, Ryuichi; Kinoshita, Ayae; Wada, Eiki The Journal of Neuroscience, Vol. 17, Issue 19 https://doi.org/10.1523/JNEUROSCI.17-19-07503.1997	journal	October 1997
Metabotropic Glutamate Receptor Subtype 7 Ablation Causes Deficit in Fear Response and Conditioned Taste Aversion Masugi, Miwako; Yokoi, Mineto; Shigemoto, Ryuichi The Journal of Neuroscience, Vol. 19, Issue 3 https://doi.org/10.1523/JNEUROSCI.19-03-00955.1999	journal	February 1999
The Concentration of Synaptically Released Glutamate Outside of the Climbing Fiber–Purkinje Cell Synaptic Cleft Dzubay, Jeffrey A.; Jahr, Craig E. The Journal of Neuroscience, Vol. 19, Issue 13 https://doi.org/10.1523/JNEUROSCI.19-13-05265.1999	journal	July 1999
Structure, Pharmacology and Therapeutic Prospects of Family C G-Protein Coupled Receptors Brauner-Osborne, Hans; Wellendorph, Petrine; Jensen, Anders Current Drug Targets, Vol. 8, Issue 1 https://doi.org/10.2174/138945007779315614	journal	January 2007
A versatile GPCR toolkit to track in vivo neuromodulation: not a one-size-fits-all sensor Labouesse, Marie A.; Patriarchi, Tommaso Nature Publishing Group https://doi.org/10.5167/uzh-200784	text	January 2021
Pharmacological evidence for a metabotropic glutamate receptor heterodimer in neuronal cells Moreno Delgado, David; Møller, Thor C.; Ster, Jeanne eLife, Vol. 6 https://doi.org/10.7554/eLife.25233	journal	June 2017

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