Neurotransmitter receptor complexes: methods for bioanalysis, their potentials and limitations

References

Agnati, L.F., Ferre, S., Lluis, C., Franco, R., and Fuxe, K. (2003). Molecular mechanisms and therapeutical implications of intramembrane receptor/receptor interactions among heptahelical receptors with examples from the striatopallidal GABA neurons. Pharmacol. Rev. 55, 509–550.10.1124/pr.55.3.2Search in Google Scholar

Alexander, J.K., Govind, A.P., Drisdel, R.C., Blanton, M.P., Vallejo, Y., Lam, T.T., and Green, W.N. (2010). Palmitoylation of nicotinic acetylcholine receptors. J. Mol. Neurosci. 40, 12–20.10.1007/s12031-009-9246-zSearch in Google Scholar

Anggono, V. and Huganir, R.L. (2012). Regulation of AMPA receptor trafficking and synaptic plasticity. Curr. Opin. Neurobiol. 22, 461–469.10.1016/j.conb.2011.12.006Search in Google Scholar

Atlason, P.T., Garside, M.L., Meddows, E., Whiting, P., and McIlhinney, R.A. (2007). N-methyl-D-aspartate (NMDA) receptor subunit NR1 forms the substrate for oligomeric assembly of the NMDA receptor. J. Biol. Chem. 282, 25299–25307.10.1074/jbc.M702778200Search in Google Scholar

Audet, N., Gales, C., Archer-Lahlou, E., Vallieres, M., Schiller, P.W., Bouvier, M., and Pineyro, G. (2008). Bioluminescence resonance energy transfer assays reveal ligand-specific conformational changes within preformed signaling complexes containing δ-opioid receptors and heterotrimeric G proteins. J. Biol. Chem. 283, 15078–15088.10.1074/jbc.M707941200Search in Google Scholar

Ayalon, G. and Stern-Bach, Y. (2001). Functional assembly of AMPA and kainate receptors is mediated by several discrete protein-protein interactions. Neuron 31, 103–113.10.1016/S0896-6273(01)00333-6Search in Google Scholar

Ball, S.M., Atlason, P.T., Shittu-Balogun, O.O., and Molnar, E. (2010). Assembly and intracellular distribution of kainate receptors is determined by RNA editing and subunit composition. J. Neurochem. 114, 1805–1818.10.1111/j.1471-4159.2010.06895.xSearch in Google Scholar

Bazin, H., Trinquet, E., and Mathis, G. (2002). Time resolved amplification of cryptate emission: a versatile technology to trace biomolecular interactions. J. Biotechnol. 82, 233–250.10.1016/S1389-0352(01)00040-XSearch in Google Scholar

Bettler, B. and Tiao, J.Y. (2006). Molecular diversity, trafficking and subcellular localization of GABA_B receptors. Pharmacol. Ther. 110, 533–543.10.1016/j.pharmthera.2006.03.006Search in Google Scholar PubMed

Boudreau, A.C., Milovanovic, M., Conrad, K.L., Nelson, C., Ferrario, C.R., and Wolf, M.E. (2012). A protein cross-linking assay for measuring cell surface expression of glutamate receptor subunits in the rodent brain after in vivo treatments. Curr. Protoc. Neurosci. Chapter 5:Unit 5.30.31–19.Search in Google Scholar

Bousquet-Dubouch, M.P., Baudelet, E., Guerin, F., Matondo, M., Uttenweiler-Joseph, S., Burlet-Schiltz, O., and Monsarrat, B. (2009). Affinity purification strategy to capture human endogenous proteasome complexes diversity and to identify proteasome-interacting proteins. Mol. Cell. Proteomics 8, 1150–1164.10.1074/mcp.M800193-MCP200Search in Google Scholar PubMed PubMed Central

Boyer, S.B., Clancy, S.M., Terunuma, M., Revilla-Sanchez, R., Thomas, S.M., Moss, S.J., and Slesinger, P.A. (2009). Direct interaction of GABA_B receptors with M2 muscarinic receptors enhances muscarinic signaling. J. Neurosci. 29, 15796–15809.10.1523/JNEUROSCI.4103-09.2009Search in Google Scholar PubMed PubMed Central

Briddon, S.J. and Hill, S.J. (2007). Pharmacology under the microscope: the use of fluorescence correlation spectroscopy to determine the properties of ligand-receptor complexes. Trends Pharmacol. Sci. 28, 637–645.10.1016/j.tips.2007.09.008Search in Google Scholar PubMed PubMed Central

Bruneau, E.G., Esteban, J.A., and Akaaboune, M. (2009). Receptor-associated proteins and synaptic plasticity. FASEB J. 23, 679–688.10.1096/fj.08-107946Search in Google Scholar PubMed PubMed Central

Bulenger, S., Marullo, S., and Bouvier, M. (2005). Emerging role of homo- and heterodimerization in G-protein-coupled receptor biosynthesis and maturation. Trends Pharmacol. Sci. 26, 131–137.10.1016/j.tips.2005.01.004Search in Google Scholar PubMed

Callen, L., Moreno, E., Barroso-Chinea, P., Moreno-Delgado, D., Cortes, A., Mallol, J., Casado, V., Lanciego, J.L., Franco, R., Lluis, C., et al. (2012). Cannabinoid receptors CB1 and CB2 form functional heteromers in brain. J. Biol. Chem. 287, 20851–20865.10.1074/jbc.M111.335273Search in Google Scholar PubMed PubMed Central

Camacho-Carvajal, M.M., Wollscheid, B., Aebersold, R., Steimle, V., and Schamel, W.W. (2004). Two-dimensional blue native/SDS gel electrophoresis of multi-protein complexes from whole cellular lysates: a proteomics approach. Mol. Cell. Proteomics 3, 176–182.10.1074/mcp.T300010-MCP200Search in Google Scholar PubMed

Carriba, P., Navarro, G., Ciruela, F., Ferre, S., Casado, V., Agnati, L., Cortes, A., Mallol, J., Fuxe, K., Canela, E.I., et al. (2008). Detection of heteromerization of more than two proteins by sequential BRET-FRET. Nat. Methods 5, 727–733.10.1038/nmeth.1229Search in Google Scholar PubMed

Choquet, D. and Triller, A. (2013). The dynamic synapse. Neuron 80, 691–703.10.1016/j.neuron.2013.10.013Search in Google Scholar PubMed

Choy, R.W., Park, M., Temkin, P., Herring, B.E., Marley, A., Nicoll, R.A., and von Zastrow, M. (2014). Retromer mediates a discrete route of local membrane delivery to dendrites. Neuron 82, 55–62.10.1016/j.neuron.2014.02.018Search in Google Scholar PubMed PubMed Central

Ciruela, F., Fernandez-Duenas, V., Sahlholm, K., Fernandez-Alacid, L., Nicolau, J.C., Watanabe, M., and Lujan, R. (2010). Evidence for oligomerization between GABA_B receptors and GIRK channels containing the GIRK1 and GIRK3 subunits. Eur. J. Neurosci. 32, 1265–1277.10.1111/j.1460-9568.2010.07356.xSearch in Google Scholar PubMed

Collins, C.J., Schilling, B., Young, M., Dollinger, G., and Guy, R.K. (2003). Isotopically labeled crosslinking reagents: resolution of mass degeneracy in the identification of crosslinked peptides. Bioorg. Med. Chem. Lett. 13, 4023–4026.10.1016/j.bmcl.2003.08.053Search in Google Scholar PubMed

Colombo, S.F., Mazzo, F., Pistillo, F., and Gotti, C. (2013). Biogenesis, trafficking and up-regulation of nicotinic ACh receptors. Biochem. Pharmacol. 86, 1063–1073.10.1016/j.bcp.2013.06.023Search in Google Scholar PubMed

Comenencia-Ortiz, E., Moss, S.J., and Davies, P.A. (2014). Phosphorylation of GABA_A receptors influences receptor trafficking and neurosteroid actions. Psychopharmacology (Berl.) 231, 3453–3465.10.1007/s00213-014-3617-zSearch in Google Scholar PubMed PubMed Central

Comps-Agrar, L., Kniazeff, J., Norskov-Lauritsen, L., Maurel, D., Gassmann, M., Gregor, N., Prezeau, L., Bettler, B., Durroux, T., Trinquet, E., et al. (2011). The oligomeric state sets GABA(B) receptor signalling efficacy. Eur. Mol. Biol. Organ. J. 30, 2336–2349.10.1038/emboj.2011.143Search in Google Scholar PubMed PubMed Central

Conn, P.M. and Ulloa-Aguirre, A. (2010). Trafficking of G-protein-coupled receptors to the plasma membrane: insights for pharmacoperone drugs. Trends Endocrinol. Metab. 21, 190–197.10.1016/j.tem.2009.11.003Search in Google Scholar PubMed PubMed Central

Connolly, C.N., Wooltorton, J.R., Smart, T.G., and Moss, S.J. (1996). Subcellular localization of γ-aminobutyric acid type A receptors is determined by receptor β subunits. Proc. Natl. Acad. Sci. USA. 93, 9899–9904.10.1073/pnas.93.18.9899Search in Google Scholar PubMed PubMed Central

Corgiat, B.A., Nordman, J.C., and Kabbani, N. (2014). Chemical crosslinkers enhance detection of receptor interactomes. Front. Pharmacol. 4, 171.10.3389/fphar.2013.00171Search in Google Scholar PubMed PubMed Central

Couve, A., Filippov, A.K., Connolly, C.N., Bettler, B., Brown, D.A., and Moss, S.J. (1998). Intracellular retention of recombinant GABA_B receptors. J. Biol. Chem. 273, 26361–26367.10.1074/jbc.273.41.26361Search in Google Scholar PubMed

Couve, A., Moss, S.J., and Pangalos, M.N. (2000). GABA_B receptors: a new paradigm in G protein signaling. Mol. Cell. Neurosci. 16, 296–312.10.1006/mcne.2000.0908Search in Google Scholar PubMed

Delille, H.K., Becker, J.M., Burkhardt, S., Bleher, B., Terstappen, G.C., Schmidt, M., Meyer, A.H., Unger, L., Marek, G.J., and Mezler, M. (2012). Heterocomplex formation of 5-HT_2A-mGlu2 and its relevance for cellular signaling cascades. Neuropharmacology 62, 2184–2191.10.1016/j.neuropharm.2012.01.010Search in Google Scholar PubMed

Drisdel, R.C., Manzana, E., and Green, W.N. (2004). The role of palmitoylation in functional expression of nicotinic α7 receptors. J. Neurosci. 24, 10502–10510.10.1523/JNEUROSCI.3315-04.2004Search in Google Scholar PubMed PubMed Central

Farias, G.G., Gershlick, D.C., and Bonifacino, J.S. (2014). Going forward with retromer. Dev. Cell 29, 3–4.10.1016/j.devcel.2014.03.018Search in Google Scholar PubMed PubMed Central

Feng, G., Tintrup, H., Kirsch, J., Nichol, M.C., Kuhse, J., Betz, H., and Sanes, J.R. (1998). Dual requirement for gephyrin in glycine receptor clustering and molybdoenzyme activity. Science 282, 1321–1324.10.1126/science.282.5392.1321Search in Google Scholar PubMed

Ferre, S., Ciruela, F., Woods, A.S., Lluis, C., and Franco, R. (2007). Functional relevance of neurotransmitter receptor heteromers in the central nervous system. Trends Neurosci. 30, 440–446.10.1016/j.tins.2007.07.001Search in Google Scholar PubMed

Filizola, M. and Weinstein, H. (2005). The study of G-protein coupled receptor oligomerization with computational modeling and bioinformatics. FEBS J. 272, 2926–2938.10.1111/j.1742-4658.2005.04730.xSearch in Google Scholar PubMed

Fiorentini, C. and Missale, C. (2004). Oligomeric assembly of dopamine D1 and glutamate NMDA receptors: molecular mechanisms and functional implications. Biochem. Soc. Trans. 32, 1025–1028.10.1042/BST0321025Search in Google Scholar PubMed

Fischer, L., Chen, Z.A., and Rappsilber, J. (2013). Quantitative cross-linking/mass spectrometry using isotope-labelled cross-linkers. J. Proteomics 88, 120–128.10.1016/j.jprot.2013.03.005Search in Google Scholar PubMed PubMed Central

Flower, D.R. (2006). Receptor-binding sites: bioinformatic approaches. Methods Mol Biol. 316, 291–358.Search in Google Scholar

Fritzsche, R., Ihling, C.H., Gotze, M., and Sinz, A. (2012). Optimizing the enrichment of cross-linked products for mass spectrometric protein analysis. Rapid Commun. Mass Spectrom. 26, 653–658.10.1002/rcm.6150Search in Google Scholar PubMed

Fukata, Y. and Fukata, M. (2010). Protein palmitoylation in neuronal development and synaptic plasticity. Nat. Rev. Neurosci. 11, 161–175.10.1038/nrn2788Search in Google Scholar PubMed

Gahring, L.C. and Rogers, S.W. (2010). Nicotinic receptor subunit α5 modifies assembly, up-regulation, and response to pro-inflammatory cytokines. J. Biol. Chem. 285, 26049–26057.10.1074/jbc.M110.105346Search in Google Scholar PubMed PubMed Central

Gales, C., Rebois, R.V., Hogue, M., Trieu, P., Breit, A., Hebert, T.E., and Bouvier, M. (2005). Real-time monitoring of receptor and G-protein interactions in living cells. Nat. Methods 2, 177–184.10.1038/nmeth743Search in Google Scholar PubMed

Gardoni, F., Caputi, A., Cimino, M., Pastorino, L., Cattabeni, F., and Di Luca, M. (1998). Calcium/calmodulin-dependent protein kinase II is associated with NR2A/B subunits of NMDA receptor in postsynaptic densities. J. Neurochem. 71, 1733–1741.10.1046/j.1471-4159.1998.71041733.xSearch in Google Scholar PubMed

Gascon, S., Garcia-Gallo, M., Renart, J., and Diaz-Guerra, M. (2007). Endoplasmic reticulum-associated degradation of the NR1 but not the NR2 subunits of the N-methyl-D-aspartate receptor induced by inhibition of the N-glycosylation in cortical neurons. J. Neurosci. Res. 85, 1713–1723.10.1002/jnr.21309Search in Google Scholar PubMed

George, S.R. and O’Dowd, B.F. (2007). A novel dopamine receptor signaling unit in brain: heterooligomers of D1 and D2 dopamine receptors. Sci. World J. 7, 58–63.10.1100/tsw.2007.223Search in Google Scholar PubMed PubMed Central

George, S.R., O’Dowd, B.F., and Lee, S.P. (2002). G-protein-coupled receptor oligomerization and its potential for drug discovery. Nat. Rev. Drug Discov. 1, 808–820.10.1038/nrd913Search in Google Scholar PubMed

Gerges, N.Z., Backos, D.S., Rupasinghe, C.N., Spaller, M.R., and Esteban, J.A. (2006). Dual role of the exocyst in AMPA receptor targeting and insertion into the postsynaptic membrane. Eur. Mol. Biol. Organ. J. 25, 1623–1634.10.1038/sj.emboj.7601065Search in Google Scholar PubMed PubMed Central

Gonzalez-Maeso, J. (2011). GPCR oligomers in pharmacology and signaling. Mol. Brain 4, 20.10.1186/1756-6606-4-20Search in Google Scholar PubMed PubMed Central

Gonzalez, S., Moreno-Delgado, D., Moreno, E., Perez-Capote, K., Franco, R., Mallol, J., Cortes, A., Casado, V., Lluis, C., Ortiz, J., et al. (2012a). Circadian-related heteromerization of adrenergic and dopamine D₄ receptors modulates melatonin synthesis and release in the pineal gland. PLoS Biol. 10, e1001347.10.1371/journal.pbio.1001347Search in Google Scholar PubMed PubMed Central

Gonzalez, S., Rangel-Barajas, C., Peper, M., Lorenzo, R., Moreno, E., Ciruela, F., Borycz, J., Ortiz, J., Lluis, C., Franco, R., et al. (2012b). Dopamine D4 receptor, but not the ADHD-associated D4.7 variant, forms functional heteromers with the dopamine D2S receptor in the brain. Mol. Psychiatry 17, 650–662.10.1038/mp.2011.93Search in Google Scholar PubMed PubMed Central

Gotti, C., Moretti, M., Zanardi, A., Gaimarri, A., Champtiaux, N., Changeux, J.P., Whiteaker, P., Marks, M.J., Clementi, F., and Zoli, M. (2005). Heterogeneity and selective targeting of neuronal nicotinic acetylcholine receptor (nAChR) subtypes expressed on retinal afferents of the superior colliculus and lateral geniculate nucleus: identification of a new native nAChR subtype a3b2 (a5 or b3) enriched in retinocollicular afferents. Mol. Pharmacol. 68, 1162–1171.10.1124/mol.105.015925Search in Google Scholar PubMed

Gouldson, P.R., Higgs, C., Smith, R.E., Dean, M.K., Gkoutos, G.V., and Reynolds, C.A. (2000). Dimerization and domain swapping in G-protein-coupled receptors: a computational study. Neuropsychopharmacology 23, S60–S77.10.1016/S0893-133X(00)00153-6Search in Google Scholar

Green, W.N. and Millar, N.S. (1995). Ion-channel assembly. Trends Neurosci. 18, 280–287.10.1016/0166-2236(95)80009-QSearch in Google Scholar

Greger, I.H., Khatri, L., and Ziff, E.B. (2002). RNA editing at arg607 controls AMPA receptor exit from the endoplasmic reticulum. Neuron 34, 759–772.10.1016/S0896-6273(02)00693-1Search in Google Scholar

Greger, I.H., Khatri, L., Kong, X., and Ziff, E.B. (2003). AMPA receptor tetramerization is mediated by Q/R editing. Neuron 40, 763–774.10.1016/S0896-6273(03)00668-8Search in Google Scholar

Guidolin, D., Ciruela, F., Genedani, S., Guescini, M., Tortorella, C., Albertin, G., Fuxe, K., and Agnati, L.F. (2011). Bioinformatics and mathematical modelling in the study of receptor-receptor interactions and receptor oligomerization: focus on adenosine receptors. Biochim. Biophys. Acta 1808, 1267–1283.10.1016/j.bbamem.2010.09.022Search in Google Scholar PubMed

Gurba, K. N. (2010). Assembly and heterogeneity of GABAA receptors. Vanderbilt Reviews Neurosci. 2, 25–32.Search in Google Scholar

Haack, K. K. V., McCarty, N. A. (2011). Functional consequences of GPCR heterodimerization: GPCRs as allosteric modulators. Pharmaceuticals 4, 509–523.10.3390/ph4030509Search in Google Scholar

Hanna, E.M. and Zaki, N. (2014). Detecting protein complexes in protein interaction networks using a ranking algorithm with a refined merging procedure. BMC Bioinformatics 15, 204.10.1186/1471-2105-15-204Search in Google Scholar PubMed PubMed Central

Hasbi, A., O’Dowd, B.F., and George, S.R. (2010). Heteromerization of dopamine D2 receptors with dopamine D1 or D5 receptors generates intracellular calcium signaling by different mechanisms. Curr. Opin. Pharmacol. 10, 93–99.10.1016/j.coph.2009.09.011Search in Google Scholar PubMed PubMed Central

Hayashi, T., Rumbaugh, G., and Huganir, R.L. (2005). Differential regulation of AMPA receptor subunit trafficking by palmitoylation of two distinct sites. Neuron 47, 709–723.10.1016/j.neuron.2005.06.035Search in Google Scholar PubMed

Heo, S. and Lubec, G. (2010). Generation and characterization of a specific polyclonal antibody against the mouse serotonin receptor 1A: a state-of-the-art recommendation on how to characterize antibody specificity. Electrophoresis 31, 3789–3796.10.1002/elps.201000374Search in Google Scholar PubMed

Hermann, R., Walther, P., and Muller, M. (1996). Immunogold labeling in scanning electron microscopy. Histochem. Cell. Biol. 106, 31–39.10.1007/BF02473200Search in Google Scholar PubMed

Hern, J.A., Baig, A.H., Mashanov, G.I., Birdsall, B., Corrie, J.E., Lazareno, S., Molloy, J.E., and Birdsall, N.J. (2010). Formation and dissociation of M1 muscarinic receptor dimers seen by total internal reflection fluorescence imaging of single molecules. Proc. Natl. Acad. Sci. USA. 107, 2693–2698.10.1073/pnas.0907915107Search in Google Scholar PubMed PubMed Central

Herrick-Davis, K. and Mazurkiewicz, J.E. (2013). Fluorescence correlation spectroscopy and photon-counting histogram analysis of receptor-receptor interactions. Methods Cell. Biol. 117, 181–196.10.1016/B978-0-12-408143-7.00010-4Search in Google Scholar PubMed

Herrick-Davis, K., Grinde, E., Lindsley, T., Cowan, A., and Mazurkiewicz, J.E. (2012). Oligomer size of the serotonin 5-hydroxytryptamine 2C (5-HT_2C) receptor revealed by fluorescence correlation spectroscopy with photon counting histogram analysis: evidence for homodimers without monomers or tetramers. J. Biol. Chem. 287, 23604–23614.10.1074/jbc.M112.350249Search in Google Scholar PubMed PubMed Central

Herrick-Davis, K., Grinde, E., Cowan, A., and Mazurkiewicz, J.E. (2013). Fluorescence correlation spectroscopy analysis of serotonin, adrenergic, muscarinic, and dopamine receptor dimerization: the oligomer number puzzle. Mol. Pharmacol. 84, 630–642.10.1124/mol.113.087072Search in Google Scholar PubMed PubMed Central

Huang, B.X. and Kim, H.Y. (2013). Effective identification of Akt interacting proteins by two-step chemical crosslinking, co-immunoprecipitation and mass spectrometry. PLoS One 8, e61430.10.1371/journal.pone.0061430Search in Google Scholar PubMed PubMed Central

Ivankova, K., Turecek, R., Fritzius, T., Seddik, R., Prezeau, L., Comps-Agrar, L., Pin, J.P., Fakler, B., Besseyrias, V., Gassmann, M., and Bettler, B. (2013). Up-regulation of GABA_B receptor signaling by constitutive assembly with the K⁺ channel tetramerization domain-containing protein 12 (KCTD12). J. Biol. Chem. 288, 24848–24856.10.1074/jbc.M113.476770Search in Google Scholar PubMed PubMed Central

Jordan, B.A., Gomes, I., Rios, C., Filipovska, J., and Devi, L.A. (2003). Functional interactions between μ opioid and c-adrenergic receptors. Mol. Pharmacol. 64, 1317–1324.10.1124/mol.64.6.1317Search in Google Scholar PubMed

Kabbani, N. and Levenson, R. (2007). A proteomic approach to receptor signaling: molecular mechanisms and therapeutic implications derived from discovery of the dopamine D2 receptor signalplex. Eur. J. Pharmacol. 572, 83–93.10.1016/j.ejphar.2007.06.059Search in Google Scholar PubMed

Kabbani, N. and Nordman, J.C. (2013). Capture of D2 dopamine receptor signaling complexes in striatal cells for mass spectrometry proteomic analysis. Methods Mol Biol. 964, 43–60.10.1007/978-1-62703-251-3_4Search in Google Scholar PubMed

Kang, S.U., Fuchs, K., Sieghart, W., and Lubec, G. (2008). Gel-based mass spectrometric analysis of recombinant GABA(A) receptor subunits representing strongly hydrophobic transmembrane proteins. J. Proteome Res. 7, 3498–3506.10.1021/pr800236uSearch in Google Scholar

Kilpatrick, L.E., Briddon, S.J., and Holliday, N.D. (2012). Fluorescence correlation spectroscopy, combined with bimolecular fluorescence complementation, reveals the effects of β-arrestin complexes and endocytic targeting on the membrane mobility of neuropeptide Y receptors. Biochim. Biophys. Acta 1823, 1068–1081.10.1016/j.bbamcr.2012.03.002Search in Google Scholar

Kim, K.M., Yi, E.C., and Kim, Y. (2012). Mapping protein receptor-ligand interactions via in vivo chemical crosslinking, affinity purification, and differential mass spectrometry. Methods 56, 161–165.10.1016/j.ymeth.2011.10.013Search in Google Scholar

Kisilevsky, A.E. and Zamponi, G.W. (2008). Presynaptic calcium channels: structure, regulators, and blockers. Handb. Exp. Pharmacol. 184, 45–75.10.1007/978-3-540-74805-2_3Search in Google Scholar

Kneussel, M. and Betz, H. (2000). Receptors, gephyrin and gephyrin-associated proteins: novel insights into the assembly of inhibitory postsynaptic membrane specializations. J. Physiol. 525, 1–9.10.1111/j.1469-7793.2000.t01-4-00001.xSearch in Google Scholar

Lai, C., Zeng, G.M., Huang, D.L., Feng, C.L., Hu, S.A., Su, F.F., Zhao, M.H., Huang, C., and Wei, Z. (2010). Detection based on immunogold labeling technique and its expected application in composting. Chin. J. Anal. Chem. 38, 909–914.10.1016/S1872-2040(09)60051-7Search in Google Scholar

Laviv, T., Vertkin, I., Berdichevsky, Y., Fogel, H., Riven, I., Bettler, B., Slesinger, P.A., and Slutsky, I. (2011). Compartmentalization of the GABA_B receptor signaling complex is required for presynaptic inhibition at hippocampal synapses. J. Neurosci. 31, 12523–12532.10.1523/JNEUROSCI.1527-11.2011Search in Google Scholar

Lee, Y.J., Lackner, L.L., Nunnari, J.M., and Phinney, B.S. (2007). Shotgun cross-linking analysis for studying quaternary and tertiary protein structures. J. Proteome Res. 6, 3908–3917.10.1021/pr070234iSearch in Google Scholar

Leitner, A., Reischl, R., Walzthoeni, T., Herzog, F., Bohn, S., Forster, F., and Aebersold, R. (2012). Expanding the chemical cross-linking toolbox by the use of multiple proteases and enrichment by size exclusion chromatography. Mol. Cell. Proteomics 11, M111.014126.10.1074/mcp.M111.014126Search in Google Scholar

Levac, B.A., O’Dowd, B.F., and George, S.R. (2002). Oligomerization of opioid receptors: generation of novel signaling units. Curr. Opin. Pharmacol. 2, 76–81.10.1016/S1471-4892(02)00124-8Search in Google Scholar

Li, K.W., Chen, N., and Smit, A.B. (2013). Interaction proteomics of the AMPA receptor: towards identification of receptor sub-complexes. Amino Acids 44, 1247–1251.10.1007/s00726-013-1461-9Search in Google Scholar

Liu, H., Wang, F., Xu, W., May, K., and Richardson, D. (2013). Quantitation of asparagine deamidation by isotope labeling and liquid chromatography coupled with mass spectrometry analysis. Anal. Biochem. 432, 16–22.10.1016/j.ab.2012.09.024Search in Google Scholar

Lo, W.Y., Lagrange, A.H., Hernandez, C.C., Harrison, R., Dell, A., Haslam, S.M., Sheehan, J.H., and Macdonald, R.L. (2010). Glycosylation of β2 subunits regulates GABA_A receptor biogenesis and channel gating. J. Biol. Chem. 285, 31348–31361.10.1074/jbc.M110.151449Search in Google Scholar

Masugi-Tokita, M., and Shigemoto, R. (2007). High-resolution quantitative visualization of glutamate and GABA receptors at central synapses. Curr. Opin. Neurobiol. 17, 387–393.10.1016/j.conb.2007.04.012Search in Google Scholar

Milligan, G. (2009). G protein-coupled receptor hetero-dimerization: contribution to pharmacology and function. Br. J. Pharmacol. 158, 5–14.10.1111/j.1476-5381.2009.00169.xSearch in Google Scholar

Moreira, J.M., Thorsen, S.B., Brunner, N., and Stenvang, J. (2013). Proximity probing assays for simultaneous visualization of protein complexes in situ. Expert Rev. Proteomics 10, 219–221.10.1586/epr.13.22Search in Google Scholar

Moreno, E., Hoffmann, H., Gonzalez-Sepulveda, M., Navarro, G., Casado, V., Cortes, A., Mallol, J., Vignes, M., McCormick, P.J., Canela, E.I., et al. (2011). Dopamine D1-histamine H3 receptor heteromers provide a selective link to MAPK signaling in GABAergic neurons of the direct striatal pathway. J. Biol. Chem. 286, 5846–5854.10.1074/jbc.M110.161489Search in Google Scholar

Mu, Y., Otsuka, T., Horton, A.C., Scott, D.B., and Ehlers, M.D. (2003). Activity-dependent mRNA splicing controls ER export and synaptic delivery of NMDA receptors. Neuron 40, 581–594.10.1016/S0896-6273(03)00676-7Search in Google Scholar

Mueller, T.M., Haroutunian, V., and Meador-Woodruff, J.H. (2014). N-glycosylation of GABA_A receptor subunits is altered in schizophrenia. Neuropsychopharmacology 39, 528–537.10.1038/npp.2013.190Search in Google Scholar PubMed PubMed Central

Nakagawa, T. (2010). The biochemistry, ultrastructure, and subunit assembly mechanism of AMPA receptors. Mol. Neurobiol. 42, 161–184.10.1007/s12035-010-8149-xSearch in Google Scholar PubMed PubMed Central

Nakazawa, K., Fujimori, K., Takanaka, A., and Inoue, K. (1991). Comparison of adenosine triphosphate- and nicotine-activated inward currents in rat phaeochromocytoma cells. J. Physiol. 434, 647–660.10.1113/jphysiol.1991.sp018491Search in Google Scholar PubMed PubMed Central

Namba, K., Suzuki, T., and Nakata, H. (2010). Immunogold electron microscopic evidence of in situ formation of homo- and heteromeric purinergic adenosine A1 and P2Y2 receptors in rat brain. BMC Res. Notes 3, 323.10.1186/1756-0500-3-323Search in Google Scholar PubMed PubMed Central

Navarro, G., Ferre, S., Cordomi, A., Moreno, E., Mallol, J., Casado, V., Cortes, A., Hoffmann, H., Ortiz, J., Canela, E.I., et al. (2010). Interactions between intracellular domains as key determinants of the quaternary structure and function of receptor heteromers. J. Biol. Chem. 285, 27346–27359.10.1074/jbc.M110.115634Search in Google Scholar PubMed PubMed Central

Navarro, G., Moreno, E., Bonaventura, J., Brugarolas, M., Farre, D., Aguinaga, D., Mallol, J., Cortes, A., Casado, V., Lluis, C., et al. (2013). Cocaine inhibits dopamine D2 receptor signaling via sigma-1-D2 receptor heteromers. PLoS One 8, e61245.10.1371/journal.pone.0061245Search in Google Scholar PubMed PubMed Central

Nordman, J.C. and Kabbani, N. (2012). An interaction between α7 nicotinic receptors and a G-protein pathway complex regulates neurite growth in neural cells. J. Cell. Sci. 125, 5502–5513.Search in Google Scholar

Oner, S.S., An, N., Vural, A., Breton, B., Bouvier, M., Blumer, J.B., and Lanier, S.M. (2010). Regulation of the AGS3.Gαi signaling complex by a seven-transmembrane span receptor. J. Biol. Chem. 285, 33949–33958.10.1074/jbc.M110.138073Search in Google Scholar PubMed PubMed Central

Panchaud, A., Singh, P., Shaffer, S.A., and Goodlett, D.R. (2010). xComb: a cross-linked peptide database approach to protein-protein interaction analysis. J. Proteome Res. 9, 2508–2515.10.1021/pr9011816Search in Google Scholar PubMed PubMed Central

Patel, R.C., Kumar, U., Lamb, D.C., Eid, J.S., Rocheville, M., Grant, M., Rani, A., Hazlett, T., Patel, S.C., Gratton, E., et al. (2002). Ligand binding to somatostatin receptors induces receptor-specific oligomer formation in live cells. Proc. Natl. Acad. Sci. USA 99, 3294–3299.10.1073/pnas.042705099Search in Google Scholar PubMed PubMed Central

Paulo, J.A., Brucker, W.J., and Hawrot, E. (2009). Proteomic analysis of an α7 nicotinic acetylcholine receptor interactome. J. Proteome Res. 8, 1849–1858.10.1021/pr800731zSearch in Google Scholar PubMed PubMed Central

Pei, L., Li, S., Wang, M., Diwan, M., Anisman, H., Fletcher, P.J., Nobrega, J.N., and Liu, F. (2010). Uncoupling the dopamine D1-D2 receptor complex exerts antidepressant-like effects. Nat. Med. 16, 1393–1395.10.1038/nm.2263Search in Google Scholar PubMed

Perreault, M.L., Hasbi, A., O’Dowd, B.F., and George, S.R. (2014). Heteromeric dopamine receptor signaling complexes: emerging neurobiology and disease relevance. Neuropsychopharmacology 39, 156–168.10.1038/npp.2013.148Search in Google Scholar PubMed PubMed Central

Pin, J.P., Comps-Agrar, L., Maurel, D., Monnier, C., Rives, M.L., Trinquet, E., Kniazeff, J., Rondard, P., and Prezeau, L. (2009). G-protein-coupled receptor oligomers: two or more for what? Lessons from mGlu and GABA_B receptors. J. Physiol. 587, 5337–5344.10.1113/jphysiol.2009.179978Search in Google Scholar PubMed PubMed Central

Qiu, S., Hua, Y.L., Yang, F., Chen, Y.Z., and Luo, J.H. (2005). Subunit assembly of N-methyl-D-aspartate receptors analyzed by fluorescence resonance energy transfer. J. Biol. Chem. 280, 24923–24930.10.1074/jbc.M413915200Search in Google Scholar PubMed

Quarta, D., Ciruela, F., Patkar, K., Borycz, J., Solinas, M., Lluis, C., Franco, R., Wise, R.A., Goldberg, S.R., Hope, B.T., et al. (2007). Heteromeric nicotinic acetylcholine-dopamine autoreceptor complexes modulate striatal dopamine release. Neuropsychopharmacology 32, 35–42.10.1038/sj.npp.1301103Search in Google Scholar PubMed

Quirk, P.L., Rao, S., Roth, B.L., and Siegel, R.E. (2004). Three putative N-glycosylation sites within the murine 5-HT_3A receptor sequence affect plasma membrane targeting, ligand binding, and calcium influx in heterologous mammalian cells. J. Neurosci. Res. 77, 498–506.10.1002/jnr.20185Search in Google Scholar PubMed

Rinner, O., Seebacher, J., Walzthoeni, T., Mueller, L.N., Beck, M., Schmidt, A., Mueller, M., and Aebersold, R. (2008). Identification of cross-linked peptides from large sequence databases. Nat. Methods 5, 315–318.10.1038/nmeth.1192Search in Google Scholar PubMed PubMed Central

Sarto-Jackson, I. and Sieghart, W. (2008). Assembly of GABA_A receptors. Mol. Membr. Biol. 25, 302–310.10.1080/09687680801914516Search in Google Scholar PubMed

Savatier, J., Jalaguier, S., Ferguson, M.L., Cavailles, V., and Royer, C.A. (2010). Estrogen receptor interactions and dynamics monitored in live cells by fluorescence cross-correlation spectroscopy. Biochemistry 49, 772–781.10.1021/bi9013006Search in Google Scholar PubMed

Scavone, J.L., Asan, E., and Van Bockstaele, E.J. (2011). Unraveling glutamate-opioid receptor interactions using high-resolution electron microscopy: implications for addiction-related processes. Exp. Neurol. 229, 207–213.10.1016/j.expneurol.2011.03.016Search in Google Scholar PubMed PubMed Central

Schuler, T., Mesic, I., Madry, C., Bartholomaus, I., and Laube, B. (2008). Formation of NR1/NR2 and NR1/NR3 heterodimers constitutes the initial step in N-methyl-D-aspartate receptor assembly. J. Biol. Chem. 283, 37–46.10.1074/jbc.M703539200Search in Google Scholar PubMed

Schwenk, J., Harmel, N., Zolles, G., Bildl, W., Kulik, A., Heimrich, B., Chisaka, O., Jonas, P., Schulte, U., Fakler, B., et al. (2009). Functional proteomics identify cornichon proteins as auxiliary subunits of AMPA receptors. Science 323, 1313–1319.10.1126/science.1167852Search in Google Scholar PubMed

Schwenk, J., Harmel, N., Brechet, A., Zolles, G., Berkefeld, H., Muller, C.S., Bildl, W., Baehrens, D., Huber, B., Kulik, A., et al. (2012). High-resolution proteomics unravel architecture and molecular diversity of native AMPA receptor complexes. Neuron 74, 621–633.10.1016/j.neuron.2012.03.034Search in Google Scholar

Selvin, P.R. (2002). Principles and biophysical applications of lanthanide-based probes. Annu. Rev. Biophys. Biomol. Struct. 31, 275–302.10.1146/annurev.biophys.31.101101.140927Search in Google Scholar

Singh, P., Shaffer, S.A., Scherl, A., Holman, C., Pfuetzner, R.A., Larson Freeman, T.J., Miller, S.I., Hernandez, P., Appel, R.D., and Goodlett, D.R. (2008). Characterization of protein cross-links via mass spectrometry and an open-modification search strategy. Anal. Chem. 80, 8799–8806.10.1021/ac801646fSearch in Google Scholar

Smart, T.G. and Paoletti, P. (2012). Synaptic neurotransmitter-gated receptors. Cold Spring Harb. Perspect. Biol. 4, a009662.10.1101/cshperspect.a009662Search in Google Scholar

Snyder, S.H. (2009). Neurotransmitters, receptors, and second messengers galore in 40 years. J. Neurosci. 29, 12717–12721.10.1523/JNEUROSCI.3670-09.2009Search in Google Scholar

Snyder, S.H. and Ferris, C.D. (2000). Novel neurotransmitters and their neuropsychiatric relevance. Am. J. Psychiatry 157, 1738–1751.10.1176/appi.ajp.157.11.1738Search in Google Scholar

Soderberg, O., Gullberg, M., Jarvius, M., Ridderstrale, K., Leuchowius, K.J., Jarvius, J., Wester, K., Hydbring, P., Bahram, F., Larsson, L.G., et al. (2006). Direct observation of individual endogenous protein complexes in situ by proximity ligation. Nat. Methods 3, 995–1000.10.1038/nmeth947Search in Google Scholar

Sommer, B., Kohler, M., Sprengel, R., and Seeburg, P.H. (1991). RNA editing in brain controls a determinant of ion flow in glutamate-gated channels. Cell 67, 11–19.10.1016/0092-8674(91)90568-JSearch in Google Scholar

Stephenson, F.A., Cousins, S.L., and Kenny, A.V. (2008). Assembly and forward trafficking of NMDA receptors (review). Mol. Membr. Biol. 25, 311–320.10.1080/09687680801971367Search in Google Scholar PubMed

Strecker, V., Wumaier, Z., Wittig, I., and Schagger, H. (2010). Large pore gels to separate mega protein complexes larger than 10 MDa by blue native electrophoresis: isolation of putative respiratory strings or patches. Proteomics 10, 3379–3387.10.1002/pmic.201000343Search in Google Scholar PubMed

Swamy, M., Minguet, S., Siegers, G.M., Alarcon, B., and Schamel, W.W. (2007). A native antibody-based mobility-shift technique (NAMOS-assay) to determine the stoichiometry of multiprotein complexes. J. Immunol. Methods 324, 74–83.10.1016/j.jim.2007.05.003Search in Google Scholar PubMed

Szidonya, L., Cserzo, M., and Hunyady, L. (2008). Dimerization and oligomerization of G-protein-coupled receptors: debated structures with established and emerging functions. J. Endocrinol. 196, 435–453.10.1677/JOE-07-0573Search in Google Scholar PubMed

Takanishi, C.L., Bykova, E.A., Cheng, W., and Zheng, J. (2006). GFP-based FRET analysis in live cells. Brain Res. 1091, 132–139.10.1016/j.brainres.2006.01.119Search in Google Scholar PubMed

Tang, Y., Chen, Y., Lichti, C.F., Hall, R.A., Raney, K.D., and Jennings, S.F. (2005). CLPM: a cross-linked peptide mapping algorithm for mass spectrometric analysis. BMC Bioinformatics 6, S9.10.1186/1471-2105-6-S2-S9Search in Google Scholar PubMed PubMed Central

Terrillon, S. and Bouvier, M. (2004). Roles of G-protein-coupled receptor dimerization. Eur. Mol. Biol. Organ. Rep. 5, 30–34.10.1038/sj.embor.7400052Search in Google Scholar PubMed PubMed Central

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, 405–496.10.1124/pr.109.002451Search in Google Scholar PubMed PubMed Central

Trifilieff, P., Rives, M.L., Urizar, E., Piskorowski, R.A., Vishwasrao, H.D., Castrillon, J., Schmauss, C., Slattman, M., Gullberg, M., and Javitch, J.A. (2011). Detection of antigen interactions ex vivo by proximity ligation assay: endogenous dopamine D2-adenosine A2A receptor complexes in the striatum. Biotechniques 51, 111–118.10.2144/000113719Search in Google Scholar PubMed PubMed Central

Vasilescu, J., Guo, X., and Kast, J. (2004). Identification of protein-protein interactions using in vivo cross-linking and mass spectrometry. Proteomics 4, 3845–3854.10.1002/pmic.200400856Search in Google Scholar PubMed

Vilardaga, J.P., Nikolaev, V.O., Lorenz, K., Ferrandon, S., Zhuang, Z., and Lohse, M.J. (2008). Conformational cross-talk between α_2A-adrenergic and μ-opioid receptors controls cell signaling. Nat. Chem. Biol. 4, 126–131.10.1038/nchembio.64Search in Google Scholar PubMed

Wanamaker, C.P. and Green, W.N. (2005). N-linked glycosylation is required for nicotinic receptor assembly but not for subunit associations with calnexin. J. Biol. Chem. 280, 33800–33810.10.1074/jbc.M501813200Search in Google Scholar PubMed PubMed Central

White, J.H., Wise, A., Main, M.J., Green, A., Fraser, N.J., Disney, G.H., Barnes, A.A., Emson, P., Foord, S.M., and Marshall, F.H. (1998). Heterodimerization is required for the formation of a functional GABA(B) receptor. Nature 396, 679–682.10.1038/25354Search in Google Scholar PubMed

Yang, W., Zheng, C., Song, Q., Yang, X., Qiu, S., Liu, C., Chen, Z., Duan, S., and Luo, J. (2007). A three amino acid tail following the TM4 region of the N-methyl-D-aspartate receptor (NR) 2 subunits is sufficient to overcome endoplasmic reticulum retention of NR1-1a subunit. J. Biol. Chem. 282, 9269–9278.10.1074/jbc.M700050200Search in Google Scholar PubMed

Ye, X., Luke, B., Andresson, T., and Blonder, J. (2009). ¹⁸O stable isotope labeling in MS-based proteomics. Brief Funct. Genomic Proteomic 8, 136–144.10.1093/bfgp/eln055Search in Google Scholar PubMed PubMed Central

Zhang, F., Guo, A., Liu, C., Comb, M. and Hu, B. (2013). Phosphorylation and assembly of glutamate receptors after brain ischemia. Stroke 44, 170–176.10.1161/STROKEAHA.112.667253Search in Google Scholar PubMed PubMed Central

Zybailov, B.L., Glazko, G.V., Jaiswal, M., and Raney, K.D. (2013). Large scale chemical cross-linking mass spectrometry perspectives. J. Proteomics Bioinform. 6, 001.10.4172/jpb.S2-001Search in Google Scholar PubMed PubMed Central