A new approach to analyze cell surface protein complexes reveals specific heterodimeric metabotropic glutamate receptors

FASEB Journal

Volumn 25, Issue 1, 2011, Pages 66-77

  Doumazane, Etienne ^a,b,c   Scholler, Pauline ^a,b,c   Zwier, Jurriaan M ^d   Trinquet, Eric ^d   Rondard, Philippe ^a,b,c   Pin, Jean Philippe ^a,b,c  

^a INSTITUT DE GÉNOMIQUE FONCTIONNELLE   (France)

^b INSERM   (France)

^c UNIV MONTPELLIER   (France)

^d Cisbio Bioassays   (France)

Author keywords

GPCR; Heteromerization; Multilabeling; Oligomerization; Time resolved fluorescence resonance energy transfer

Indexed keywords

CELL SURFACE PROTEIN; HETERODIMER; METABOTROPIC RECEPTOR; METABOTROPIC RECEPTOR 2; METABOTROPIC RECEPTOR 3; METABOTROPIC RECEPTOR 4; METABOTROPIC RECEPTOR 7; METABOTROPIC RECEPTOR 8;

ARTICLE; BIOCHEMISTRY; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENE EXPRESSION; PRIORITY JOURNAL; PROTEIN ANALYSIS;

ANIMALS; BLOTTING, WESTERN; CERCOPITHECUS AETHIOPS; COS CELLS; FLUORESCENCE RESONANCE ENERGY TRANSFER; HEK293 CELLS; HUMANS; MEMBRANE PROTEINS; PHYLOGENY; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN SUBUNITS; RATS; RECEPTORS, METABOTROPIC GLUTAMATE; TRANSFECTION;

MAMMALIA; RATTUS;

EID: 79251591614     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.10-163147     Document Type: Article

References (71)

1. Klingenberg, M. (1981) Membrane protein oligomeric structure and transport function. Nature 290, 449-454
2. Salter, M. W. (2003) D1 and NMDA receptors hook up: expanding on an emerging theme. Trends Neurosci. 26, 235-237
3. Altier, C., Khosravani, H., Evans, R. M., Hameed, S., Peloquin, J. B., Vartian, B. A., Chen, L., Beedle, A. M., Ferguson, S. S., Mezghrani, A., Dubel, S. J., Bourinet, E., McRory, J. E., and Zamponi, G. W. (2006) ORL1 receptor-mediated internalization of N-type calcium channels. Nat. Neurosci. 9, 31-40
4. Gonzalez-Maeso, J., Ang, R. L., Yuen, T., Chan, P., Weisstaub, N. V., Lopez-Gimenez, J. F., Zhou, M., Okawa, Y., Callado, L. F., Milligan, G., Gingrich, J. A., Filizola, M., Meana, J. J., and Sealfon, S. C. (2008) Identification of a serotonin/glutamate receptor complex implicated in psychosis. Nature 452, 93-97
5. Prezeau, L., Rives, M. L., Comps-Agrar, L., Maurel, D., Kniazeff, J., and Pin, J. P. (2010) Functional crosstalk between GPCRs: with or without oligomerization. Curr. Opin. Pharmacol. 10, 6-13
6. Overington, J. P., Al-Lazikani, B., and Hopkins, A. L. (2006) How many drug targets are there? Nat. Rev. Drug Discov. 5, 993-996
7. Lagerstrom, M. C., and Schioth, H. B. (2008) Structural diversity of G protein-coupled receptors and significance for drug discovery. Nat. Rev. Drug Discov. 7, 339-357
8. Ernst, O. P., Gramse, V., Kolbe, M., Hofmann, K. P., and Heck, M. (2007) Monomeric G protein-coupled receptor rhodopsin in solution activates its G protein transducin at the diffusion limit. Proc. Natl. Acad. Sci. U. S. A. 104, 10859-10864
9. Whorton, M. R., Bokoch, M. P., Rasmussen, S. G., Huang, B., Zare, R. N., Kobilka, B., and Sunahara, R. K. (2007) A monomeric G protein-coupled receptor isolated in a high-density lipoprotein particle efficiently activates its G protein. Proc. Natl. Acad. Sci. U. S. A. 104, 7682-7687
10. 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
11. Milligan, G., and Smith, N. J. (2007) Allosteric modulation of heterodimeric G-protein-coupled receptors. Trends Pharmacol. Sci. 28, 615-620
12. Gurevich, V. V., and Gurevich, E. V. (2008) GPCR monomers and oligomers: it takes all kinds. Trends Neurosci. 31, 74-81
13. Ferre, S., Baler, R., Bouvier, M., Caron, M. G., Devi, L. A., Durroux, T., Fuxe, K., George, S. R., Javitch, J. A., Lohse, M. J., Mackie, K., Milligan, G., Pfleger, K. D., Pin, J. P., Volkow, N. D., Waldhoer, M., Woods, A. S., and Franco, R. (2009) Building a new conceptual framework for receptor heteromers. Nat. Chem. Biol. 5, 131-134
14. Rozenfeld, R., and Devi, L. A. (2010) Receptor heteromerization and drug discovery. Trends Pharmacol. Sci. 31, 124-130
15. Cottet, M., Albizu, L., Perkovska, S., Jean-Alphonse, F., Rahmeh, R., Orcel, H., Mejean, C., Granier, S., Mendre, C., Mouillac, B., and Durroux, T. (2010) Past, present and future of vasopressin and oxytocin receptor oligomers, prototypical GPCR models to study dimerization processes. Curr. Opin. Pharmacol. 10, 59-66
16. Guo, W., Urizar, E., Kralikova, M., Mobarec, J. C., Shi, L., Filizola, M., and Javitch, J. A. (2008) Dopamine D2 receptors form higher order oligomers at physiological expression levels. EMBO J. 27, 2293-2304
17. Albizu, L., Cottet, M., Kralikova, M., Stoev, S., Seyer, R., Brabet, I., Roux, T., Bazin, H., Bourrier, E., Lamarque, L., Breton, C., Rives, M. L., Newman, A., Javitch, J., Trinquet, E., Manning, M., Pin, J. P., Mouillac, B., and Durroux, T. (2010) Time-resolved FRET between GPCR ligands reveals oligomers in native tissues. Nat. Chem. Biol. 6, 587-594
18. Pisterzi, L. F., Jansma, D. B., Georgiou, J., Woodside, M. J., Chou, J. T., Angers, S., Raicu, V., and Wells, J. W. (2010) Oligomeric size of the m2 muscarinic receptor in live cells as determined by quantitative fluorescence resonance energy transfer. J. Biol. Chem. 285, 16723-16738
19. Fotiadis, D., Liang, Y., Filipek, S., Saperstein, D. A., Engel, A., and Palczewski, K. (2003) Atomic-force microscopy: rhodopsin dimers in native disc membranes. Nature 421, 127-128
20. Maurel, D., Comps-Agrar, L., Brock, C., Rives, M. L., Bourrier, E., Ayoub, M. A., Bazin, H., Tinel, N., Durroux, T., Prezeau, L., Trinquet, E., and Pin, J. P. (2008) Cell-surface protein-protein interaction analysis with time-resolved FRET and snap-tag technologies: application to GPCR oligomerization. Nat. Methods 5, 561-567
21. 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. U. S. A. 107, 2693-2698
22. Carriba, P., Navarro, G., Ciruela, F., Ferre, S., Casado, V., Agnati, L., Cortes, A., Mallol, J., Fuxe, K., Canela, E. I., Lluis, C., and Franco, R. (2008) Detection of heteromerization of more than two proteins by sequential BRET-FRET. Nat. Methods 5, 727-733
23. Vogel, S. S., Thaler, C., and Koushik, S. V. (2006) Fanciful FRET. Sci STKE 2006, re2
24. Pfleger, K. D., and Eidne, K. A. (2006) Illuminating insights into protein-protein interactions using bioluminescence resonance energy transfer (BRET). Nat. Methods 3, 165-174
25. 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
26. Degorce, F., Card, A., Soh, S., Trinquet, E., Knapik, G. P., and Xie, B. (2009) HTRF: A Technology Tailored for Drug Discovery -A Review of Theoretical Aspects and Recent Applications. Curr. Chem. Genomics 3, 22-32
27. Selvin, P. R. (2002) Principles and biophysical applications of lanthanide-based probes. Annu. Rev. Biophys. Biomol. Struct. 31, 275-302
28. McVey, M., Ramsay, D., Kellett, E., Rees, S., Wilson, S., Pope, A. J., and Milligan, G. (2001) Monitoring receptor oligomerization using time-resolved fluorescence resonance energy transfer and bioluminescence resonance energy transfer. The human delta -opioid receptor displays constitutive oligomerization at the cell surface, which is not regulated by receptor occupancy. J. Biol. Chem. 276, 14092-14099
29. Maurel, D., Kniazeff, J., Mathis, G., Trinquet, E., Pin, J. P., and Ansanay, H. (2004) Cell surface detection of membrane protein interaction with homogeneous time-resolved fluorescence resonance energy transfer technology. Anal. Biochem. 329, 253-262
30. Juillerat, A., Gronemeyer, T., Keppler, A., Gendreizig, S., Pick, H., Vogel, H., and Johnsson, K. (2003) Directed evolution of O6-alkylguanine-DNA alkyltransferase for efficient labeling of fusion proteins with small molecules in vivo. Chem. Biol. 10, 313-317
31. Gautier, A., Juillerat, A., Heinis, C., Correa, I. R., Jr., Kindermann, M., Beaufils, F., and Johnsson, K. (2008) An engineered protein tag for multiprotein labeling in living cells. Chem. Biol. 15, 128-136
32. O'Hare, H. M., Johnsson, K., and Gautier, A. (2007) Chemical probes shed light on protein function. Curr. Opin. Struct. Biol. 17, 488-494
33. Conn, P., and Pin, J. -P. (1997) Pharmacology and functions of metabotropic glutamate receptors. Ann. Rev. Pharmacol. Toxicol. 37, 205-237
34. Ferraguti, F., and Shigemoto, R. (2006) Metabotropic glutamate receptors. Cell Tissue Res. 326, 483-504
35. Swanson, C. J., Bures, M., Johnson, M. P., Linden, A. M., Monn, J. A., and Schoepp, D. D. (2005) Metabotropic glutamate receptors as novel targets for anxiety and stress disorders. Nat. Rev. Drug Discov. 4, 131-144
36. Patil, S. T., Zhang, L., Martenyi, F., Lowe, S. L., Jackson, K. A., Andreev, B. V., Avedisova, A. S., Bardenstein, L. M., Gurovich, I. Y., Morozova, M. A., Mosolov, S. N., Neznanov, N. G., Reznik, A. M., Smulevich, A. B., Tochilov, V. A., Johnson, B. G., Monn, J. A., and Schoepp, D. D. (2007) Activation of mGlu2/3 receptors as a new approach to treat schizophrenia: a randomized Phase 2 clinical trial. Nat. Med. 13, 1102-1107
37. Niswender, C. M., and Conn, P. J. (2010) Metabotropic glutamate receptors: physiology, pharmacology, and disease. Annu. Rev. Pharmacol. Toxicol. 50, 295-322
38. Romano, C., Yang, W. L., and O'Malley, K. L. (1996) Metabotropic glutamate receptor 5 is a disulfide-linked dimer. J. Biol. Chem. 271, 28612-28616
39. Kunishima, N., Shimada, Y., Tsuji, Y., Sato, T., Yamamoto, M., Kumasaka, T., Nakanishi, S., Jingami, H., and Morikawa, K. (2000) Structural basis of glutamate recognition by a dimeric metabotropic glutamate receptor. Nature 407, 971-977
40. Jingami, H., Nakanishi, S., and Morikawa, K. (2003) Structure of the metabotropic glutamate receptor. Curr. Opin. Neurobiol. 13, 271-278
41. Pin, J. P., Kniazeff, J., Liu, J., Binet, V., Goudet, C., Rondard, P., and Prezeau, L. (2005) Allosteric functioning of dimeric class C G-protein-coupled receptors. FEBS J. 272, 2947-2955
42. Kubo, Y., and Tateyama, M. (2005) Towards a view of functioning dimeric metabotropic receptors. Curr. Opin. Neurobiol. 15, 289-295
43. Fung, J. J., Deupi, X., Pardo, L., Yao, X. J., Velez-Ruiz, G. A., Devree, B. T., Sunahara, R. K., and Kobilka, B. K. (2009) Ligand-regulated oligomerization of beta(2)-adrenoceptors in a model lipid bilayer. EMBO J. 28, 3315-3328
44. Kaupmann, K., Malitschek, B., Schuler, V., Heid, J., Froestl, W., Beck, P., Mosbacher, J., Bischoff, S., Kulik, A., Shigemoto, R., Karschin, A., and Bettler, B. (1998) GABA(B)-receptor subtypes assemble into functional heteromeric complexes. Nature 396, 683-687
45. Nelson, G., Hoon, M. A., Chandrashekar, J., Zhang, Y., Ryba, N. J., and Zuker, C. S. (2001) Mammalian sweet taste receptors. Cell 106, 381-390
46. Nelson, G., Chandrashekar, J., Hoon, M. A., Feng, L., Zhao, G., Ryba, N. J., and Zuker, C. S. (2002) An amino-acid taste receptor. Nature 416, 199-202
47. Brabet, I., Parmentier, M. L., De Colle, C., Bockaert, J., Acher, F., and Pin, J. P. (1998) Comparative effect of L-CCG-I, DCG-IV and gamma-carboxy-L-glutamate on all cloned metabotropic glutamate receptor subtypes. Neuropharmacology 37, 1043-1051
48. Brock, C., Oueslati, N., Soler, S., Boudier, L., Rondard, P., and Pin, J. P. (2007) Activation of a dimeric metabotropic glutamate receptor by intersubunit rearrangement. J. Biol. Chem. 282, 33000-33008
49. Rives, M. L., Vol, C., Fukazawa, Y., Tinel, N., Trinquet, E., Ayoub, M. A., Shigemoto, R., Pin, J. P., and Prezeau, L. (2009) Crosstalk between GABA(B) and mGlu1a receptors reveals new insight into GPCR signal integration. EMBO J. 28, 2195-2208
50. Raicu, V. (2007) Efficiency of resonance energy transfer in homo-oligomeric complexes of proteins. J. Biol. Phys. 33, 109-127
51. Frauli, M., Neuville, P., Vol, C., Pin, J. P., and Prezeau, L. (2006) Among the twenty classical L-amino acids, only glutamate directly activates metabotropic glutamate receptors. Neuropharmacology 50, 245-253
52. Margeta-Mitrovic, M., Jan, Y. N., and Jan, L. Y. (2000) A trafficking checkpoint controls GABA(B) receptor heterodimerization. Neuron 27, 97-106
53. Brock, C., Boudier, L., Maurel, D., Blahos, J., and Pin, J. P. (2005) Assembly-dependent surface targeting of the heterodimeric GABAB receptor is controlled by COPI but not 14-3-3. Mol. Biol. Cell 16, 5572-5578
54. Mercier, J. F., Salahpour, A., Angers, S., Breit, A., and Bouvier, M. (2002) Quantitative assessment of beta 1- and beta 2-adrenergic receptor homo- and heterodimerization by bioluminescence resonance energy transfer. J. Biol. Chem. 277, 44925-44931
55. Meyer, B. H., Segura, J. M., Martinez, K. L., Hovius, R., George, N., Johnsson, K., and Vogel, H. (2006) FRET imaging reveals that functional neurokinin-1 receptors are monomeric and reside in membrane microdomains of live cells. Proc. Natl. Acad. Sci. U. S. A. 103, 2138-2143
56. Kniazeff, J., Bessis, A. S., Maurel, D., Ansanay, H., Prezeau, L., and Pin, J. P. (2004) Closed state of both binding domains of homodimeric mGlu receptors is required for full activity. Nat. Struct. Mol. Biol. 11, 706-713
57. Goudet, C., Kniazeff, J., Hlavackova, V., Malhaire, F., Maurel, D., Acher, F., Blahos, J., Prezeau, L., and Pin, J. P. (2005) Asymmetric functioning of dimeric metabotropic glutamate receptors disclosed by positive allosteric modulators. J. Biol. Chem. 280, 24380-24385
58. Rajapakse, H. E., Gahlaut, N., Mohandessi, S., Yu, D., Turner, J. R., and Miller, L. W. (2010) Time-resolved luminescence resonance energy transfer imaging of protein-protein interactions in living cells. Proc. Natl. Acad. Sci. U. S. A. 107, 13582-13587
59. Veatch, W., and Stryer, L. (1977) The dimeric nature of the gramicidin A transmembrane channel: conductance and fluorescence energy transfer studies of hybrid channels. J. Mol. Biol. 113, 89-102
60. Ferraguti, F., Klausberger, T., Cobden, P., Baude, A., Roberts, J. D., Szucs, P., Kinoshita, A., Shigemoto, R., Somogyi, P., and Dalezios, Y. (2005) Metabotropic glutamate receptor 8-expressing nerve terminals target subsets of GABAergic neurons in the hippocampus. J. Neurosci. 25, 10520-10536
61. Tallaksen-Greene, S. J., Kaatz, K. W., Romano, C., and Albin, R. L. (1998) Localization of mGluR1a-like immunoreactivity and mGluR5-like immunoreactivity in identified populations of striatal neurons. Brain Res. 780, 210-217
62. Koulen, P., Kuhn, R., Wassle, H., and Brandstatter, J. H. (1997) Group I metabotropic glutamate receptors mGluR1alpha and mGluR5a: localization in both synaptic layers of the rat retina. J. Neurosci. 17, 2200-2211
63. Van Hooft, J. A., Giuffrida, R., Blatow, M., and Monyer, H. (2000) Differential expression of group I metabotropic glutamate receptors in functionally distinct hippocampal interneurons. J. Neurosci. 20, 3544-3551 (Pubitemid 30266216)
64. Thoreson, W. B., and Witkovsky, P. (1999) Glutamate receptors and circuits in the vertebrate retina. Prog. Retin. Eye Res. 18, 765-810
65. Melchiorri, D., Cappuccio, I., Ciceroni, C., Spinsanti, P., Mosillo, P., Sarichelou, I., Sale, P., and Nicoletti, F. (2007) Metabotropic glutamate receptors in stem/progenitor cells. Neuropharmacology 53, 473-480
66. Volk, L. J., Daly, C. A., and Huber, K. M. (2006) Differential roles for group 1 mGluR subtypes in induction and expression of chemically induced hippocampal long-term depression. J. Neurophysiol. 95, 2427-2438
67. Hlavackova, V., Goudet, C., Kniazeff, J., Zikova, A., Maurel, D., Vol, C., Trojanova, J., Prezeau, L., Pin, J. P., and Blahos, J. (2005) Evidence for a single heptahelical domain being turned on upon activation of a dimeric GPCR. EMBO J. 24, 499-509
68. Iacovelli, L., Molinaro, G., Battaglia, G., Motolese, M., Di Menna, L., Alfiero, M., Blahos, J., Matrisciano, F., Corsi, M., Corti, C., Bruno, V., De Blasi, A., and Nicoletti, F. (2009) Regulation of group II metabotropic glutamate receptors by G protein-coupled receptor kinases: mGlu2 receptors are resistant to homologous desensitization. Mol. Pharmacol. 75, 991-1003
69. Ferraguti, F., Corti, C., Valerio, E., Mion, S., and Xuereb, J. (2001) Activated astrocytes in areas of kainate-induced neuronal injury upregulate the expression of the metabotropic glutamate receptors 2/3 and 5. Exp. Brain Res. 137, 1-11
70. Gama, L., Wilt, S. G., and Breitwieser, G. E. (2001) Heterodimerization of calcium sensing receptors with metabotropic glutamate receptors in neurons. J. Biol. Chem. 276, 39053-39059
71. Cabello, N., Gandia, J., Bertarelli, D. C., Watanabe, M., Lluis, C., Franco, R., Ferre, S., Lujan, R., and Ciruela, F. (2009) Metabotropic glutamate type 5, dopamine D2 and adenosine A2a receptors form higher-order oligomers in living cells. J. Neurochem. 109, 1497-1507