Recent advances in bioluminescence resonance energy transfer technologies to study GPCR heteromerization

Current Opinion in Pharmacology

Volumn 10, Issue 1, 2010, Pages 44-52

  Ayoub, Mohammed A ^a   Pfleger, Kevin DG ^a,b  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^b Dimerix Bioscience Pty Ltd   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CCR2; CHEMOKINE RECEPTOR CXCR4; G PROTEIN COUPLED RECEPTOR; GREEN FLUORESCENT PROTEIN; HETEROMER; HYBRID PROTEIN; MELATONIN 1 RECEPTOR; MELATONIN 2 RECEPTOR; POLYMER; RENILLA LUCIFERIN 2 MONOOXYGENASE; UNCLASSIFIED DRUG; YELLOW FLUORESCENT PROTEIN;

BIOLUMINESCENCE RESONANCE ENERGY TRANSFER; BIOTECHNOLOGY; HETEROMERIZATION; LIGAND BINDING; NONHUMAN; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN INTERACTION; REVIEW;

ENERGY TRANSFER; HUMANS; LIGANDS; LUMINESCENT MEASUREMENTS; PROTEIN BINDING; PROTEIN MULTIMERIZATION; RECEPTORS, G-PROTEIN-COUPLED;

EID: 72449197630     PISSN: 14714892     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.coph.2009.09.012     Document Type: Review

References (51)

1. Pfleger K.D., and Eidne K.A. Monitoring the formation of dynamic G-protein-coupled receptor-protein complexes in living cells. Biochem J 385 (2005) 625-637
2. 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., et al. Building a new conceptual framework for receptor heteromers. Nat Chem Biol 5 (2009) 131-134
3. Pin J.P., Neubig R., Bouvier M., Devi L., Filizola M., Javitch J.A., Lohse M.J., Milligan G., Palczewski K., Parmentier M., et al. International Union of Basic and Clinical Pharmacology. LXVII. Recommendations for the recognition and nomenclature of G protein-coupled receptor heteromultimers. Pharmacol Rev 59 (2007) 5-13
4. Prinster S.C., Hague C., and Hall R.A. Heterodimerization of G protein-coupled receptors: specificity and functional significance. Pharmacol Rev 57 (2005) 289-298
5. Fuxe K., Marcellino D., Guidolin D., Woods A.S., and Agnati L.F. Heterodimers and receptor mosaics of different types of G-protein-coupled receptors. Physiology (Bethesda) 23 (2008) 322-332
6. Milligan G. G protein-coupled receptor hetero-dimerization: contribution to pharmacology and function. Br J Pharmacol 158 (2009) 5-14. A comprehensive review of GPCR oligomerization, with a particular emphasis on implications for ligand pharmacology and novel drug design.
7. Dalrymple M.B., Pfleger K.D., and Eidne K.A. G protein-coupled receptor dimers: Functional consequences, disease states and drug targets. Pharmacol Ther 118 (2008) 359-371. A comprehensive review of our understanding of GPCR oligomerization to this point, with a particular emphasis on the evidence for functional implications.
8. Franco R., Casado V., Cortes A., Perez-Capote K., Mallol J., Canela E., Ferre S., and Lluis C. Novel pharmacological targets based on receptor heteromers. Brain Res Rev 58 (2008) 475-482
9. Terrillon S., and Bouvier M. Roles of G-protein-coupled receptor dimerization. EMBO Rep 5 (2004) 30-34
10. Levoye A., Dam J., Ayoub M.A., Guillaume J.L., and Jockers R. Do orphan G-protein-coupled receptors have ligand-independent functions? New insights from receptor heterodimers. EMBO Rep 7 (2006) 1094-1098
11. Milligan G. Applications of bioluminescence- and fluorescence resonance energy transfer to drug discovery at G protein-coupled receptors. Eur J Pharm Sci 21 (2004) 397-405
12. Pfleger K.D., and Eidne K.A. Illuminating insights into protein-protein interactions using bioluminescence resonance energy transfer (BRET). Nat Methods 3 (2006) 165-174
13. Pin J.P., Ayoub M.A., Maurel D., Perroy J., and Trinquet E. Energy transfer technologies to monitor the dynamics and signaling properties of G-protein coupled receptors in living cells. In: Pebay-Peyroula E. (Ed). Biophysical Analysis of Membrane Proteins - Investigating Structure and Function (2008), Wiley-VCH 311-334
14. Marullo S., and Bouvier M. Resonance energy transfer approaches in molecular pharmacology and beyond. Trends Pharmacol Sci 28 (2007) 362-365
15. Gandia J., Lluis C., Ferre S., Franco R., and Ciruela F. Light resonance energy transfer-based methods in the study of G protein-coupled receptor oligomerization. Bioessays 30 (2008) 82-89
16. Mercier J.F., Salahpour A., Angers S., Breit A., and Bouvier M. Quantitative assessment of beta 1- and beta 2-adrenergic receptor homo- and heterodimerization by bioluminescence resonance energy transfer. J Biol Chem 277 (2002) 44925-44931
17. Ayoub M.A., Maurel D., Binet V., Fink M., Prezeau L., Ansanay H., and Pin J.P. Real-time analysis of agonist-induced activation of protease-activated receptor 1/Galphai1 protein complex measured by bioluminescence resonance energy transfer in living cells. Mol Pharmacol 71 (2007) 1329-1340
18. Gales C., Rebois R.V., Hogue M., Trieu P., Breit A., Hebert T.E., and Bouvier M. Real-time monitoring of receptor and G-protein interactions in living cells. Nat Methods 2 (2005) 177-184
19. Galés C., Van Durm J.J., Schaak S., Pontier S., Percherancier Y., Audet M., Paris H., and Bouvier M. Probing the activation-promoted structural rearrangements in preassembled receptor-G protein complexes. Nat Struct Mol Biol 13 (2006) 778-786
20. Hamdan F.F., Audet M., Garneau P., Pelletier J., and Bouvier M. High-throughput screening of G protein-coupled receptor antagonists using a bioluminescence resonance energy transfer 1-based beta-arrestin2 recruitment assay. J Biomol Screen 10 (2005) 463-475
21. Pfleger K.D., Dromey J.R., Dalrymple M.B., Lim E.M., Thomas W.G., and Eidne K.A. Extended bioluminescence resonance energy transfer (eBRET) for monitoring prolonged protein-protein interactions in live cells. Cell Signal 18 (2006) 1664-1670
22. Pfleger K.D., Dalrymple M.B., Dromey J.R., and Eidne K.A. Monitoring interactions between G-protein-coupled receptors and beta-arrestins. Biochem Soc Trans 35 (2007) 764-766
23. Kocan M., and Pfleger K.D. Detection of GPCR/beta-arrestin interactions in live cells using bioluminescence resonance energy transfer technology. Methods Mol Biol 552 (2009) 305-317
24. Guillaume J.L., Daulat A.M., Maurice P., Levoye A., Migaud M., Brydon L., Malpaux B., Borg-Capra C., and Jockers R. The PDZ protein mupp1 promotes Gi coupling and signaling of the MT1 melatonin receptor. J Biol Chem 283 (2008) 16762-16771
25. Pontier S.M., Percherancier Y., Galandrin S., Breit A., Gales C., and Bouvier M. Cholesterol-dependent separation of the beta2-adrenergic receptor from its partners determines signaling efficacy: insight into nanoscale organization of signal transduction. J Biol Chem 283 (2008) 24659-24672
26. Hamdan F.F., Percherancier Y., Breton B., and Bouvier M. Monitoring protein-protein interactions in living cells by bioluminescence resonance energy transfer (BRET). Curr Protoc Neurosci (2006) Chapter 5:Unit 5.23
27. Pfleger K.D., Seeber R.M., and Eidne K.A. Bioluminescence resonance energy transfer (BRET) for the real-time detection of protein-protein interactions. Nat Protoc 1 (2006) 337-345
28. Pfleger K.D. Analysis of protein-protein interactions using bioluminescence resonance energy transfer. Methods Mol Biol 574 (2009) 173-183
29. Levi J., De A., Cheng Z., and Gambhir S.S. Bisdeoxycoelenterazine derivatives for improvement of bioluminescence resonance energy transfer assays. J Am Chem Soc 129 (2007) 11900-11901
30. De A., Loening A.M., and Gambhir S.S. An improved bioluminescence resonance energy transfer strategy for imaging intracellular events in single cells and living subjects. Cancer Res 67 (2007) 7175-7183. The first description of the use of the new luciferases Rluc2 and Rluc8 in BRET assays, with a particular emphasis on imaging in single cells and small living animals.
31. Kamal M., Marquez M., Vauthier V., Leloire A., Froguel P., Jockers R., and Couturier C. Improved donor/acceptor BRET couples for monitoring beta-arrestin recruitment to G protein-coupled receptors. Biotechnol J 4 (2009) 1337-1344
32. 2 and eBRET for assaying ligand-induced interactions between GPCRs and β-arrestins, to an extent that has important consequences for enabling robust high throughput screening.
33. Guo W., Urizar E., Kralikova M., Mobarec J.C., Shi L., Filizola M., and Javitch J.A. Dopamine D2 receptors form higher order oligomers at physiological expression levels. EMBO J 27 (2008) 2293-2304. A very nice study using a range of BRET and other techniques to provide evidence for dopamine D2 receptors forming higher order complexes. Includes, BRET-BiFC, BRET-BiLC, BRET saturation and BRET competition assays.
34. De A., Ray P., Loening A.M., and Gambhir S.S. BRET3: a red-shifted bioluminescence resonance energy transfer (BRET)-based integrated platform for imaging protein-protein interactions from single live cells and living animals. FASEB J 23 (2009) 2702-2709. Description of new third generation BRET (BRET3) using Rluc8 and mOrange. Increased photon intensity, red-shifted light output and good spectral resolution make BRET3 a good BRET combination, particularly for imaging in small animals.
35. 2A receptors in living cells and showing the utility of this approach to study higher order GPCR heteromers.
36. Robitaille M., Heroux I., Baragli A., and Hebert T.E. Novel tools for use in bioluminescence resonance energy transfer (BRET) assays. Methods Mol Biol 574 (2009) 215-234
37. 2A receptors, leading to the conclusion that these receptors form oligomers containing more than two protomers.
38. Issad T., and Jockers R. Bioluminescence resonance energy transfer to monitor protein-protein interactions. Methods Mol Biol 332 (2006) 195-209
39. Terrillon S., Durroux T., Mouillac B., Breit A., Ayoub M.A., Taulan M., Jockers R., Barberis C., and Bouvier M. Oxytocin and vasopressin V1a and V2 receptors form constitutive homo- and heterodimers during biosynthesis. Mol Endocrinol 17 (2003) 677-691
40. Ayoub M.A., Levoye A., Delagrange P., and Jockers R. Preferential formation of MT1/MT2 melatonin receptor heterodimers with distinct ligand interaction properties compared with MT2 homodimers. Mol Pharmacol 66 (2004) 312-321
41. Goin J.C., and Nathanson N.M. Quantitative analysis of muscarinic acetylcholine receptor homo- and heterodimerization in live cells: regulation of receptor down-regulation by heterodimerization. J Biol Chem 281 (2006) 5416-5425
42. Bulenger S., Marullo S., and Bouvier M. Emerging role of homo- and heterodimerization in G-protein-coupled receptor biosynthesis and maturation. Trends Pharmacol Sci 26 (2005) 131-137
43. Breit A., Lagace M., and Bouvier M. Hetero-oligomerization between beta2- and beta3-adrenergic receptors generates a beta-adrenergic signaling unit with distinct functional properties. J Biol Chem 279 (2004) 28756-28765
44. Ramsay D., Carr I.C., Pediani J., Lopez-Gimenez J.F., Thurlow R., Fidock M., and Milligan G. High-affinity interactions between human alpha1A-adrenoceptor C-terminal splice variants produce homo- and heterodimers but do not generate the alpha1L-adrenoceptor. Mol Pharmacol 66 (2004) 228-239
45. Small K.M., Schwarb M.R., Glinka C., Theiss C.T., Brown K.M., Seman C.A., and Liggett S.B. alpha(2A)- and alpha(2C)-adrenergic receptors form homo- and heterodimers: the heterodimeric state impairs agonist-promoted GRK phosphorylation and beta-arrestin recruitment. Biochemistry 45 (2006) 4760-4767
46. Percherancier Y., Berchiche Y.A., Slight I., Volkmer-Engert R., Tamamura H., Fujii N., Bouvier M., and Heveker N. Bioluminescence resonance energy transfer reveals ligand-induced conformational changes in CXCR4 homo- and heterodimers. J Biol Chem 280 (2005) 9895-9903
47. Zheng Y., Akgun E., Harikumar K.G., Hopson J., Powers M.D., Lunzer M.M., Miller L.J., and Portoghese P.S. Induced association of mu opioid (MOP) and type 2 cholecystokinin (CCK2) receptors by novel bivalent ligands. J Med Chem 52 (2009) 247-258
48. Ayoub M.A., Couturier C., Lucas-Meunier E., Angers S., Fossier P., Bouvier M., and Jockers R. Monitoring of ligand-independent dimerization and ligand-induced conformational changes of melatonin receptors in living cells by bioluminescence resonance energy transfer. J Biol Chem 277 (2002) 21522-21528
49. Jockers R., Maurice P., Boutin J.A., and Delagrange P. Melatonin receptors, heterodimerization, signal transduction and binding sites: what's new?. Br J Pharmacol 154 (2008) 1182-1195
50. Pfleger K.D. New technology to identify potential novel G-protein-coupled receptor heterodimers and heterodimer-specific compounds. J Biomol Screen 14 (2009) 890
51. Veatch W., and Stryer L. The dimeric nature of the gramicidin A transmembrane channel: conductance and fluorescence energy transfer studies of hybrid channels. J Mol Biol 113 (1977) 89-102