Applications of bioluminescence- and fluorescence resonance energy transfer to drug discovery at G protein-coupled receptors

European Journal of Pharmaceutical Sciences

Volumn 21, Issue 4, 2004, Pages 397-405

  Milligan, Graeme ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

Arrestin; BRET; FRET; G protein coupled receptor

Indexed keywords

G PROTEIN COUPLED RECEPTOR; PROTEIN KINASE;

BIOLUMINESCENCE; ENERGY TRANSFER; ENZYME ACTIVITY; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENE TRANSLOCATION; HUMAN; LIGAND BINDING; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; SHORT SURVEY;

EID: 1442309077     PISSN: 09280987     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ejps.2003.11.010     Document Type: Review

References (69)

1. Adams S.R., Campbell R.E., Gross L.A., Martin B.R., Walkup G.K., Yao Y., Llopis J., Tsien R.Y. New biarsenical ligands and tetracysteine motifs for protein labeling in vitro and in vivo: synthesis and biological applications. J. Am. Chem. Soc. 124:2002;6063-6076.
2. Angers S., Salahpour A., Joly E., Hilairet S., Chelsky D., Dennis M., Bouvier M. Detection of β-2-adrenergic receptor dimerization in living cells using bioluminescence resonance energy transfer (BRET). Proc. Natl. Acad. Sci. U.S.A. 97:2000;3684-3689.
3. Ayoub M.A., Couturier C., Lucas-Meunier E., Angers S., Fossier P., Bouvier M., 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.
4. Babcock G.J., Farzan M., Sodroski J. Ligand-independent dimerization of CXCR4, a principal HIV-1 coreceptor. J. Biol. Chem. 278:2003;3378-3385.
5. Barak L.S., Zhang J., Ferguson S.S., Laporte S.A., Caron M.G. Signaling, desensitization, and trafficking of G protein-coupled receptors revealed by green fluorescent protein conjugates. Methods Enzymol. 302:1999;153-171.
6. + channel as a biosensor. J. Biol. Chem. 278:2003;10851-10858.
7. Berglund M.M., Schober D.A., Statnick M.A., McDonald P.H., Gehlert D.R. The use of bioluminescence resonance energy transfer-2 to study neuropeptide Y receptor agonist-induced β-arrestin-2 interaction. J. Pharmacol. Exp. Ther. 306:2003;147-156.
8. Bertrand L., Parent S., Caron M., Legault M., Joly E., Angers S., Bouvier M., Brown M., Houle B., Menard L.J. The BRET2/arrestin assay in stable recombinant cells: a platform to screen for compounds that interact with G protein-coupled receptors (GPCRS). Receptor Signal Transduct. Res. 22:2002;533.
9. Boute N., Jockers R., Issad T. The use of resonance energy transfer in high-throughput screening: BRET versus FRET. Trends Pharmacol. Sci. 23:2002;351-354.
10. Boute N., Boubekeur S., Lacasa D., Issad T. Dynamics of the interaction between the insulin receptor and protein tyrosine-phosphatase 1B in living cells. EMBO Rep. 4:2003;313-319.
11. Carrillo J.J., Pediani J., Milligan G. Dimers of class A G protein-coupled receptors function via agonist-mediated trans-activation of associated G proteins. J. Biol. Chem. 278:2003;42578-42587.
12. Charest P.G., Bouvier M. Palmitoylation of the V2 vasopressin receptor carboxyl tail enhances arrestin recruitment leading to efficient receptor endocytosis and ERK1/2 activation. J. Biol. Chem. 278:2003;41541-41551.
13. Cheng Z.J., Miller L.J. Agonist-dependent dissociation of oligomeric complexes of G protein-coupled cholecystokinin receptors demonstrated in living cells using bioluminescence resonance energy transfer. J. Biol. Chem. 276:2001;48040-48047.
14. Cornea A., Conn P.M. Measurement of changes in fluorescence resonance energy transfer between gonadotropin-releasing hormone receptors in response to agonists. Methods. 27:2002;333-339.
15. Cornea A., Janovick J.A., Maya-Nunez G., Conn P.M. Gonadotropin- releasing hormone receptor microaggregation. Rate monitored by fluorescence resonance energy transfer. J. Biol. Chem. 276:2001;2153-2158.
16. Dinger M.C., Bader J.E., Kobor A.D., Kretzschmar A.K., Beck-Sickinger A.G. Homodimerization of neuropeptide Y receptors investigated by fluorescence resonance energy transfer in living cells. J. Biol. Chem. 278:2003;10562-10571.
17. Eidne K.A., Kroeger K.M., Hanyaloglu A.C. Applications of novel resonance energy transfer techniques to study dynamic hormone receptor interactions in living cells. Trends Endocrinol. Metabol. 13:2002;415-421.
18. Ferguson S.S. Evolving concepts in G protein-coupled receptor endocytosis: the role in receptor desensitization and signaling. Pharmacol. Rev. 53:2001;1-24.
19. Floyd D.H., Geva A., Bruinsma S.P., Overton M.C., Blumer K.J., Baranski T.J. C5a receptor oligomerization. Part II. Fluorescence resonance energy transfer studies of a human G protein-coupled receptor expressed in yeast. J. Biol. Chem. 278:2003;35354-35361.
20. George S.R., O'Dowd B.F., Lee S.P. G protein-coupled receptor oligomerization and its potential for drug discovery. Nature Rev. Drug Discov. 1:2002;808-820.
21. Gonzalez J.E., Maher M.P. Cellular fluorescent indicators and voltage/ ion probe reader (VIPR) tools for ion channel and receptor drug discovery. Receptors Channels. 8:2002;283-289.
22. Hamman B.D., Pollok B.A., Bennett T., Allen J., Heim R. Binding of a Pleckstrin homology domain protein to phosphoinositide in membranes: a miniaturized FRET-based assay for drug screening. J. Biomol. Screen. 7:2002;45-55.
23. Hanyaloglu A.C., Seeber R.M., Kohout T.A., Lefkowitz R.J., Eidne K.A. Homo- and hetero-oligomerization of thyrotropin-releasing hormone (TRH) receptor subtypes. Differential regulation of β-arrestins 1 and 2. J. Biol. Chem. 277:2002;50422-50430.
24. Horvat R.D., Roess D.A., Nelson S.E., Barisas B.G., Clay C.M. Binding of agonist but not antagonist leads to fluorescence resonance energy transfer between intrinsically fluorescent gonadotropin-releasing hormone receptors. Mol. Endocrinol. 15:2001;695-703.
25. Hughes T.E., Zhang H., Logothetis D.E., Berlot C.H. Visualization of a functional G alpha q-green fluorescent protein fusion in living cells. Association with the plasma membrane is disrupted by mutational activation and by elimination of palmitoylation sites, but not by activation mediated by receptors or AlF4. J. Biol. Chem. 276:2001;4227-4235.
26. Ilien B., Franchet C., Bernard P., Morisset S., Weill C.O., Bourguignon J.J., Hibert M., Galzi J.L. Fluorescence resonance energy transfer to probe human M1 muscarinic receptor structure and drug binding properties. J. Neurochem. 85:2003;768-778.
27. Issad T., Boute N., Boubekeur S., Lacasa D., Pernet K. Looking for an insulin pill? Use the BRET methodology. Diabetes Metab. 29:2003;111-117.
28. Issafras H., Angers S., Bulenger S., Blanpain C., Parmentier M., Labbe-Jullie C., Bouvier M., Marullo S. Constitutive agonist-independent CCR5 oligomerization and antibody-mediated clustering occurring at physiological levels of receptors. J. Biol. Chem. 277:2002;34666-34673.
29. Janetopoulos C., Devreotes P. Monitoring receptor-mediated activation of heterotrimeric G proteins by fluorescence resonance energy transfer. Methods. 27:2002;366-373.
30. Janetopoulos C., Jin T., Devreotes P. Receptor-mediated activation of heterotrimeric G proteins in living cells. Science. 291:2001;2408-2411.
31. Jensen A.A., Hansen J.L., Sheikh S.P., Brauner-Osborne H. Probing intermolecular protein-protein interactions in the calcium-sensing receptor homodimer using bioluminescence resonance energy transfer (BRET). Eur. J. Biochem. 269:2002;5076-5087.
32. Kamiya T., Saitoh O., Yoshioka K., Nakata H. Oligomerization of adenosine A2A and dopamine D2 receptors in living cells. Biochem. Biophys. Res. Commun. 306:2003;544-549.
33. Kroeger K.M., Hanyaloglu A.C., Seeber R.M., Miles L.E., Eidne K.A. Constitutive and agonist-dependent homo-oligomerization of the thyrotropin-releasing hormone receptor. Detection in living cells using bioluminescence resonance energy transfer. J. Biol. Chem. 276:2001;12736-12743.
34. Latif R., Graves P., Davies T.F. Ligand-dependent inhibition of oligomerization at the human thyrotropin receptor. J. Biol. Chem. 277:2002;45059-45067.
35. Lavine N., Ethier N., Oak J.N., Pei L., Liu F., Trieu P., Rebois R.V., Bouvier M., Hebert T.E., Van Tol H.H. G protein-coupled receptors form stable complexes with inwardly rectifying potassium channels and adenylyl cyclase. J. Biol. Chem. 277:2002;46010-46019.
36. Leaney J.L., Benians A., Graves F.M., Tinker A. A novel strategy to engineer functional fluorescent inhibitory G protein alpha subunits. J. Biol. Chem. 277:2002;28803-28809.
37. McVey M., Ramsay D., Kellett E., Rees S., Wilson S., Pope A.J., Milligan G. 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. 276:2001;14092-14099.
38. Matz M.V., Lukyanov K.A., Lukyanov S.A. Family of the green fluorescent protein: journey to the end of the rainbow. Bioessays. 24:2002;953-959.
39. Mellado M., Vila-Coro A.J., Martinez C., Rodriguez-Frade J.M. Receptor dimerization: a key step in chemokine signaling. Cell Mol. Biol. 47:2001;575-582.
40. Mercier J.F., Salahpour A., Angers S., Breit A., Bouvier M. Quantitative assessment of β-1- and β-2-adrenergic receptor homo- and heterodimerization by bioluminescence resonance energy transfer. J. Biol. Chem. 277:2002;44925-44931.
41. Milligan G. Oligomerisation of G protein-coupled receptors. J. Cell Sci. 114:2001;1265-1271.
42. Milligan G. High-content assays for ligand regulation of G protein-coupled receptors. Drug Discov. Today. 8:2003;579-585.
43. Miyawaki A. Visualization of the spatial and temporal dynamics of intracellular signaling. Dev. Cell. 4:2003;295-305.
44. Oakley R.H., Hudson C.C., Cruikshank R.D., Meyers D.M., Payne R.E. Jr., Rhem S.M., Loomis C.R. The cellular distribution of fluorescently labeled arrestins provides a robust, sensitive, and universal assay for screening G protein-coupled receptors. Assay Drug Dev. Technol. 1:2002;21-30.
45. Oliveria S.F., Gomez L.L., Dell'Acqua M.L. Imaging kinase - AKAP79 - phosphatase scaffold complexes at the plasma membrane in living cells using FRET microscopy. J. Cell Biol. 160:2003;101-112.
46. Overton M.C., Blumer K.J. G protein-coupled receptors function as oligomers in vivo. Curr. Biol. 10:2000;341-344.
47. Overton M.C., Blumer K.J. The extracellular N-terminal domain and transmembrane domains 1 and 2 mediate oligomerization of a yeast G protein-coupled receptor. J. Biol. Chem. 277:2002;41463-41472.
48. Patel R.C., Kumar U., Lamb D.C., Eid J.S., Rocheville M., Grant M., Rani A., Hazlett T., Patel S.C., Gratton E., Patel Y.C. Ligand binding to somatostatin receptors induces receptor-specific oligomer formation in live cells. Proc. Natl. Acad. Sci. U.S.A. 99:2002;3294-3299.
49. Ramsay D., Kellett E., McVey M., Rees S., Milligan G. Homo- and hetero-oligomeric interactions between G protein-coupled receptors in living cells monitored by two variants of bioluminescence resonance energy transfer (BRET): hetero-oligomers between receptor subtypes form more efficiently than between less closely related sequences. Biochem. J. 365:2002;429-440.
50. Rocheville M., Lange D.C., Kumar U., Patel S.C., Patel R.C., Patel Y.C. Receptors for dopamine and somatostatin: formation of hetero-oligomers with enhanced functional activity. Science. 288:2000a;154-157.
51. Rocheville M., Lange D.C., Kumar U., Sasi R., Patel R.C., Patel Y.C. Subtypes of the somatostatin receptor assemble as functional homo- and heterodimers. J. Biol. Chem. 275:2000b;7862-7869.
52. Ruehr M.L., Zakhary D.R., Damron D.S., Bond M. Cyclic AMP-dependent protein kinase binding to A-kinase anchoring proteins in living cells by fluorescence resonance energy transfer of green fluorescent protein fusion proteins. J. Biol. Chem. 274:1999;33092-33096.
53. Ruiz-Velasco V., Ikeda S.R. Functional expression and FRET analysis of green fluorescent proteins fused to G protein subunits in rat sympathetic neurons. J. Physiol. 537:2001;679-692.
54. Sato M., Ozawa T., Inukai K., Asano T., Umezawa Y. Fluorescent indicators for imaging protein phosphorylation in single living cells. Nature Biotechnol. 20:2002;287-294.
55. Shenoy S.K., Lefkowitz R.J. Multifaceted roles of β-arrestins in the regulation of seven-membrane-spanning receptor trafficking and signalling. Biochem. J. 375:2003;503-515.
56. Stanasila L., Perez J.B., Vogel H., Cotecchia S. Oligomerization of the alpha1a and alpha1b-adrenergic receptor subtypes: potential implications in receptor internalization. J. Biol. Chem. 278:2003;40239-40251.
57. Terrillon S., Durroux T., Mouillac B., Breit A., Ayoub M.A., Taulan M., Jockers R., Barberis C., Bouvier M. Oxytocin and vasopressin V1a and V2 receptors form constitutive homo- and heterodimers during biosynthesis. Mol. Endocrinol. 17:2003;677-691.
58. Ting A.Y., Kain K.H., Klemke R.L., Tsien R.Y. Genetically encoded fluorescent reporters of protein tyrosine kinase activities in living cells. Proc. Natl. Acad. Sci. U.S.A. 98:2001;15003-15008.
59. van Roessel P., Brand A.H. Imaging into the future: visualizing gene expression and protein interactions with fluorescent proteins. Nature Cell Biol. 4:2002;E15-E20.
60. Vila-Coro A.J., Rodriguez-Frade J.M., Martin De Ana A., Moreno-Ortiz M.C., Martinez-A C., Mellado M. The chemokine SDF-1alpha triggers CXCR4 receptor dimerization and activates the JAK/STAT pathway. FASEB J. 13:1999;1699-1710.
61. Vilardaga J.P., Bunemann M., Krasel C., Lohse M.J. Measurement of the millisecond activation switch of G protein-coupled receptors in living cells. Nature Biotechnol. 7:2003;807-812.
62. Violin J.D., Zhang J., Tsien R.Y., Newton A.C. A genetically encoded fluorescent reporter reveals oscillatory phosphorylation by protein kinase C. J. Cell Biol. 161:2003;899-909.
63. Vollmer J.Y., Alix P., Chollet A., Takeda K., Galzi J.L. Subcellular compartmentalization of activation and desensitization of responses mediated by NK2 neurokinin receptors. J. Biol. Chem. 274:1999;37915-37922.
64. Wurch T., Matsumoto A., Pauwels P.J. Agonist-independent and -dependent oligomerization of dopamine D(2) receptors by fusion to fluorescent proteins. FEBS Lett. 507:2001;109-113.
65. Xu Y., Piston D.W., Johnson C.H. A bioluminescence resonance energy transfer (BRET) system: application to interacting circadian clock proteins. Proc. Natl. Acad. Sci. U.S.A. 96:1999;151-156.
66. Xu Y., Kanauchi A., von Arnim A.G., Piston D.W., Johnson C.H. Bioluminescence resonance energy transfer: monitoring protein-protein interactions in living cells. Methods Enzymol. 360:2003;289-301.
67. Yoshioka K., Saitoh O., Nakata H. Agonist-promoted heteromeric oligomerization between adenosine A(1) and P2Y(1) receptors in living cells. FEBS Lett. 523:2002;147-151.
68. Yu J.Z., Rasenick M.M. Real-time visualization of a fluorescent G(alpha)(s): dissociation of the activated G protein from plasma membrane. Mol. Pharmacol. 61:2002;352-359.
69. Zhang J., Campbell R.E., Ting A.Y., Tsien R.Y. Creating new fluorescent probes for cell biology. Nature Rev. Mol. Cell Biol. 3:2002;906-918.