Time-resolved fluorescence ligand binding for G protein-coupled receptors

Nature Protocols

Volumn 8, Issue 7, 2013, Pages 1307-1320

  Emami Nemini, Alexander ^a,b   Roux, Thomas ^c   Leblay, Marion ^c   Bourrier, Emmanuel ^c   Lamarque, Laurent ^c   Trinquet, Eric ^c   Lohse, Martin J ^a,b  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b UNIVERSITY OF WÜRZBURG   (Germany)

^c Cisbio Bioassays   (France)

Author keywords

[No Author keywords available]

Indexed keywords

G PROTEIN COUPLED RECEPTOR; PARATHYROID HORMONE RECEPTOR; FLUORESCENT DYE; LIGAND; PARATHYROID HORMONE (1-34)AMIDE; PARATHYROID HORMONE[1-34]; PEPTIDE FRAGMENT; TERBIUM;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING ASSAY; CATALYSIS; CELL MEMBRANE; CONTROLLED STUDY; FLUORESCENCE RESONANCE ENERGY TRANSFER; HIGH THROUGHPUT SCREENING; HUMAN; HUMAN CELL; LIGAND BINDING; OLIGOMERIZATION; PRIORITY JOURNAL; PROCESS OPTIMIZATION; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS; RECEPTOR BINDING; SIGNAL NOISE RATIO; TIME RESOLVES FLUORESCENCE LIGAND BINDING; ANALOGS AND DERIVATIVES; CHEMISTRY; METABOLISM; PROCEDURES; TIME;

FLUORESCENCE RESONANCE ENERGY TRANSFER; FLUORESCENT DYES; LIGANDS; PEPTIDE FRAGMENTS; RECEPTORS, G-PROTEIN-COUPLED; TERBIUM; TERIPARATIDE; TIME FACTORS;

EID: 84879348833     PISSN: 17542189     EISSN: 17502799     Source Type: Journal    
DOI: 10.1038/nprot.2013.073     Document Type: Article

References (82)

1. Lundstrom, K. Structural genomics of GPCRs. Trends Biotechnol. 23, 103-108 (2005).
2. Overington, J.P., Al-Lazikani, B. & Hopkins, A.L. How many drug targets are there? Nat. Rev. Drug Discov. 5, 993-996 (2006).
3. Rask-Andersen, M., Almen, M.S. & Schioth, H.B. Trends in the exploitation of novel drug targets. Nat. Rev. Drug Discov. 10, 579-590 (2011).
4. Bjarnadottir, T.K. et al. Comprehensive repertoire and phylogenetic analysis of the G protein-coupled receptors in human and mouse. Genomics 88, 263-273 (2006).
5. Foord, S.M. et al. International Union of Pharmacology. XLVI. G protein-coupled receptor list. Pharmacol Rev. 57, 279-288 (2005).
6. Lagerstrom, M.C. & Schioth, H.B. Structural diversity of G protein-coupled receptors and signifcance for drug discovery. Nat. Rev. Drug Discov. 7, 339-357 (2008).
7. Pin, J.P. & Acher, F. The metabotropic glutamate receptors: structure, activation mechanism and pharmacology. Curr. Drug Targets CNS Neurol. Disord. 1, 297-317 (2002).
8. Lefkowitz, R.J. Historical review: a brief history and personal retrospective of seven transmembrane receptors. Trends Pharmacol. Sci. 25, 413-422 (2004).
9. May, L.T. & Christopoulos, A. Allosteric modulators of G-protein-coupled receptors. Curr. Opin. Pharmacol. 3, 551-556 (2003).
10. Birdsall, N.J. Class A GPCR heterodimers: evidence from binding studies. Trends Pharmacol. Sci. 31, 499-508 (2010).
11. Christopoulos, A. & Kenakin, T. G protein-coupled receptor allosterism and complexing. Pharmacol. Rev. 54, 323-374 (2002).
12. Hoyer, D., Schoeffter, P., Waeber, C. & Palacios, J.M. Serotonin 5-HT1D receptors. Ann. N Y Acad. Sci. 600, 168-181 (1990).
13. Palacios, J.M., Mengod, G., Vilaro, M.T. & Ramm, P. Recent trends in receptor analysis techniques and instrumentation. J. Chem. Neuroanat. 4, 343-353 (1991).
14. Amenta, F., Ferrante, F. & Ricci, A. Pharmacological characterisation and autoradiographic localisation of dopamine receptor subtypes in the cardiovascular system and in the kidney. Hypertens Res. 18 (suppl. 1), S23-S27 (1995).
15. Katugampola, S.D., Kuc, R.E., Maguire, J.J. & Davenport, A.P. G-protein-coupled receptors in human atherosclerosis: comparison of vasoconstrictors (endothelin and thromboxane) with recently de-orphanized (urotensin-II, apelin and ghrelin) receptors. Clin. Sci. (Lond) 103 (suppl. 48), 171S-175S (2002).
16. Lohse, M.J., Nuber, S. & Hoffmann, C. Fluorescence/bioluminescence resonance energy transfer techniques to study G-protein-coupled receptor activation and signaling. Pharmacol. Rev. 64, 299-336 (2012).
17. Selvin, P.R. Principles and biophysical applications of lanthanide-based probes. Annu. Rev. Biophys. Biomol. Struct. 31, 275-302 (2002).
18. Degorce, F. et al. HTRF: a technology tailored for drug discovery-a review of theoretical aspects and recent applications. Curr. Chem. Genomics 3, 22-32 (2009).
19. Förster, T. Zwischenmolekulare Energiewanderung und Fluoreszenz. Ann. Phys. (Leipzig) 2, 55-75 1948)
20. Handl, H.L. & Gillies, R.J. Lanthanide-based luminescent assays for ligand-receptor interactions. Life Sci. 77, 361-371 (2005).
21. Hu, L.A., Zhou, T., Hamman, B.D. & Liu, Q. A homogeneous G protein-coupled receptor ligand binding assay based on time-resolved fuorescence resonance energy transfer. Assay Drug Dev. Technol. 6, 543-550 (2008).
22. Albizu, L. et al. Toward effcient drug screening by homogeneous assays based on the development of new fuorescent vasopressin and oxytocin receptor ligands. J. Med. Chem. 50, 4976-4985 (2007).
23. Zwier, J.M. et al. A fuorescent ligand-binding alternative using Tag-lite technology. J. Biomol. Screen 15, 1248-1259 (2010).
24. Leyris, J.P. et al. Homogeneous time-resolved fuorescence-based assay to screen for ligands targeting the growth hormone secretagogue receptor type 1a. Anal. Biochem. 408, 253-262 (2011).
25. Inglese, J. et al. Chemokine receptor-ligand interactions measured using time-resolved fuorescence. Biochemistry 37, 2372-2377 (1998).
26. Gao, X. et al. Europium-labeled melanin-concentrating hormone analogues: ligands for measuring binding to melanin-concentrating hormone receptors 1 and 2. Anal. Biochem. 328, 187-195 (2004).
27. Carter, P.H. et al. Photochemically enhanced binding of small molecules to the tumor necrosis factor receptor-1 inhibits the binding of TNF-alpha. Proc. Natl. Acad. Sci. USA 98, 11879-11884 (2001).
28. Mazor, O. et al. Europium-labeled epidermal growth factor and neurotensin: novel probes for receptor-binding studies. Anal. Biochem. 301, 75-81 (2002).
29. Takeuchi, T., Nishikawa, T., Matsukawa, R. & Matsui, J. Nonisotopic receptor assay for benzodiazepine drugs using time-resolved fuorometry. Anal. Chem. 67, 2655-2658 (1995).
30. Handl, H.L., Vagner, J., Yamamura, H.I., Hruby, V.J. & Gillies, R.J. Lanthanide-based time-resolved fuorescence of in cyto ligand-receptor interactions. Anal. Biochem. 330, 242-250 (2004).
31. Maurel, D. et al. Cell surface detection of membrane protein interaction with homogeneous time-resolved fuorescence resonance energy transfer technology. Anal. Biochem. 329, 253-262 (2004).
32. Kern, A., Albarran-Zeckler, R., Walsh, H.E. & Smith, R.G. Apo-ghrelin receptor forms heteromers with DRD2 in hypothalamic neurons and is essential for anorexigenic effects of DRD2 agonism. Neuron 73, 317-332 (2012).
33. Cottet, A. & Kontos, T. Spin quantum bit with ferromagnetic contacts for circuit QED. Phys. Rev. Lett. 105, 160502 (2010).
34. Jares-Erijman, E.A. & Jovin, T.M. FRET imaging. Nat. Biotechnol. 21, 1387-1395 (2003).
35. Miyawaki, A. Development of probes for cellular functions using fuorescent proteins and fuorescence resonance energy transfer. Annu. Rev. Biochem. 80, 357-373 (2011).
36. Börner, S. et al. FRET measurements of intracellular cAMP concentrations and cAMP analog permeability in intact cells. Nat. Protoc. 6, 427-438 (2011).
37. Baker, J.G. et al. Synthesis and characterization of high-affnity 4, 4-difuoro-4-bora-3a, 4a-diaza-s-indacene-labeled fuorescent ligands for human β-adrenoceptors. J. Med. Chem. 54, 6874-6887 (2011).
38. Nomura, W. et al. Fluorophore labeling enables imaging and evaluation of specifc CXCR4-ligand interaction at the cell membrane for fuorescence-based screening. Bioconjug. Chem. 19, 1917-1920 (2008).
39. Kecskes, M., Kumar, T.S., Yoo, L., Gao, Z.G. & Jacobson, K.A. Novel Alexa Fluor-488 labeled antagonist of the A(2A) adenosine receptor: application to a fuorescence polarization-based receptor binding assay. Biochem. Pharmacol. 80, 506-511 (2010).
40. Kozma, E. et al. Novel fuorescent antagonist as a molecular probe in A3 adenosine receptor binding assays using fow cytometry. Biochem. Pharmacol. 83, 1552-1561 (2012).
41. Sletten, E.M. & Bertozzi, C.R. Bioorthogonal chemistry: fshing for selectivity in a sea of functionality. Angew. Chem. Int. Ed. Engl. 48, 6974-6998 (2009).
42. Daly, C.J. & McGrath, J.C. Fluorescent ligands, antibodies, and proteins for the study of receptors. Pharmacol. Ther. 100, 101-118 (2003).
43. Bazin, H., Trinquet, E. & Mathis, G. Time resolved amplifcation of cryptate emission: a versatile technology to trace biomolecular interactions. J. Biotechnol. 82, 233-250 (2002).
44. Alpha, B., Lehn, J.M. & Mathis, G. Energy-transfer luminescence of europium(iii) and terbium(iii) cryptates of macrobicyclic polypyridine ligands. Angew. Chem. Int. Edit. 26, 266-267 (1987).
45. Kobilka, B.K. G protein-coupled receptor structure and activation. Biochim. Biophys. Acta. 1768, 794-807 (2007).
46. Castro, M., Nikolaev, V.O., Palm, D., Lohse, M.J. & Vilardaga, J.P. Turn-on switch in parathyroid hormone receptor by a two-step parathyroid hormone binding mechanism. Proc. Natl. Acad. Sci. USA 102, 16084-16089 (2005).
47. Hoffmann, C. et al. A FlAsH-based FRET approach to determine G protein-coupled receptor activation in living cells. Nat. Methods 2, 171-176 (2005).
48. Maurel, D. et al. Cell-surface protein-protein interaction analysis with time-resolved FRET and snap-tag technologies: application to GPCR oligomerization. Nat. Methods 5, 561-567 (2008).
49. Keppler, A. et al. A general method for the covalent labeling of fusion proteins with small molecules in vivo. Nat. Biotechnol. 21, 86-89 (2003).
50. Albizu, L. et al. Time-resolved FRET between GPCR ligands reveals oligomers in native tissues. Nat. Chem. Biol. 6, 587-594 (2010).
51. Weiland, G.A. & Molinoff, P.B. Quantitative analysis of drug-receptor interactions: I. Determination of kinetic and equilibrium properties. Life Sci. 29, 313-330 (1981).
52. Lohse, M.J. et al. 8-Cyclopentyl-1, 3-dipropylxanthine (DPCPX)-a selective high-affnity antagonist radioligand for A1 adenosine receptors. Naunyn. Schmiedebergs Arch. Pharmacol. 336, 204-210 (1987).
53. Klotz, K.N. et al. 2-Chloro-N6-[3H]cyclopentyladenosine ([3H]CCPA)-a high-affnity agonist radioligand for A1 adenosine receptors. Naunyn. Schmiedebergs Arch. Pharmacol. 340, 679-683 (1989).
54. Weber, R.G., Jones, C.R., Lohse, M.J. & Palacios, J.M. Autoradiographic visualization of A1 adenosine receptors in rat brain with 3H8-cyclopentyl-1, 3-dipropylxanthine. J. Neurochem. 54, 1344-1353 (1990).
55. Abou-Samra, A.B. et al. Expression cloning of a common receptor for parathyroid hormone and parathyroid hormone-related peptide from rat osteoblast-like cells: a single receptor stimulates intracellular accumulation of both cAMP and inositol trisphosphates and increases intracellular free calcium. Proc. Natl. Acad. Sci. USA 89, 2732-2736 (1992).
56. Raisz, L.G., Lorenzo, J., Gworek, S., Kream, B. & Rosenblatt, M. Comparison of the effects of a potent synthetic analog of bovine parathyroid hormone with native bPTH-(1-84) and synthetic bPTH-(1-34) on bone resorption and collagen synthesis. Calcif. Tissue Int. 29, 215-218 (1979).
57. Rosenblatt, M. & Potts, J.T. Jr. Design and synthesis of parathyroid hormone analogues of enhanced biological activity. Endocr. Res. Commun. 4, 115-133 (1977).
58. Pioszak, A.A. & Xu, H.E. Molecular recognition of parathyroid hormone by its G protein-coupled receptor. Proc. Natl. Acad. Sci. USA 105, 5034-5039 (2008).
59. Jin, L. et al. Crystal structure of human parathyroid hormone 1-34 at 0.9-A resolution. J. Biol. Chem. 275, 27238-27244 (2000).
60. Potts, J.T. Parathyroid hormone: past and present. J. Endocrinol. 187, 311-325 (2005).
61. Xu, J. et al. Octadentate cages of Tb(III) 2-hydroxyisophthalamides: a new standard for luminescent lanthanide labels. J. Am. Chem. Soc. 133, 19900-19910 (2011).
62. Kupcho, K.R. et al. Simultaneous monitoring of discrete binding events using dual-acceptor terbium-based LRET. J. Am. Chem. Soc. 129, 13372-13373 (2007).
63. Dean, T., Vilardaga, J.P., Potts, J.T. Jr. & Gardella, T.J. Altered selectivity of parathyroid hormone (PTH) and PTH-related protein (PTHrP) for distinct conformations of the PTH/PTHrP receptor. Mol. Endocrinol. 22, 156-166 (2008).
64. Vilardaga, J.P., Bunemann, M., Krasel, C., Castro, M. & Lohse, M.J. Measurement of the millisecond activation switch of G protein-coupled receptors in living cells. Nat. Biotechnol. 21, 807-812 (2003).
65. Seifert, R., Wenzel-Seifert, K., Gether, U. & Kobilka, B.K. Functional differences between full and partial agonists: evidence for ligand-specifc receptor conformations. J. Pharmacol. Exp. Ther. 297, 1218-1226 (2001).
66. Lee, C. et al. Role of the extracellular regions of the parathyroid hormone (PTH)/PTH-related peptide receptor in hormone binding. Endocrinology 135, 1488-1495 (1994).
67. McGrath, J.C., Arribas, S. & Daly, C.J. Fluorescent ligands for the study of receptors. Trends Pharmacol. Sci. 17, 393-399 (1996).
68. Daly, C.J. et al. Fluorescent ligand binding reveals heterogeneous distribution of adrenoceptors and 'cannabinoid-like' receptors in small arteries. Br. J. Pharmacol. 159, 787-796 (2010).
69. Lea, W.A. & Simeonov, A. Fluorescence polarization assays in small molecule screening. Expert. Opin. Drug Discov. 6, 17-32 (2011).
70. de Jong, L.A., Uges, D.R., Franke, J.P. & Bischoff, R. Receptor-ligand binding assays: technologies and applications. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 829, 1-25 (2005).
71. Gagne, A., Banks, P. & Hurt, S.D. Use of fuorescence polarization detection for the measurement of fuopeptidetm binding to G protein-coupled receptors. J. Recept. Signal Transduct. Res. 22, 333-343 (2002).
72. Briddon, S.J. & Hill, S.J. Pharmacology under the microscope: the use of fuorescence correlation spectroscopy to determine the properties of ligand-receptor complexes. Trends Pharmacol. Sci. 28, 637-645 (2007).
73. Rose, R.H., Briddon, S.J. & Hill, S.J. A novel fuorescent histamine H1 receptor antagonist demonstrates the advantage of using fuorescence correlation spectroscopy to study the binding of lipophilic ligands. Br. J. Pharmacol. 165, 1789-1800 (2012).
74. Kumar, S. et al. FLIM FRET technology for drug discovery: automated multiwell-plate high-content analysis, multiplexed readouts and application in situ. Chemphyschem 12, 609-626 (2011).
75. Waller, A. et al. Techniques: GPCR assembly, pharmacology and screening by fow cytometry. Trends Pharmacol. Sci. 25, 663-669 (2004).
76. Dicker, F., Quitterer, U., Winstel, R., Honold, K. & Lohse, M.J. Phosphorylation-independent inhibition of parathyroid hormone receptor signaling by G protein-coupled receptor kinases. Proc. Natl. Acad. Sci. USA 96, 5476-5481 (1999).
77. Motulsky, H.J. & Neubig, R.R. Analyzing binding data. Curr. Protoc. Neurosci. 52, 7.5.1-7.5.65 (2010).
78. Motulsky, H.J. & Christopoulos, A. Fitting models to biological data using linear and nonlinear regression-a practical guide to curve ftting. Graphpad Software (2003).
79. Lohse, M.J., Lenschow, V. & Schwabe, U. Two affnity states of Ri adenosine receptors in brain membranes. Analysis of guanine nucleotide and temperature effects on radioligand binding. Mol. Pharmacol. 26, 1-9 (1984).
80. De Lean, A., Hancock, A.A. & Lefkowitz, R.J. Validation and statistical analysis of a computer modeling method for quantitative analysis of radioligand binding data for mixtures of pharmacological receptor subtypes. Mol. Pharmacol. 21, 5-16 (1982).
81. Nagasaki, K. et al. In vitro and in vivo antagonists against parathyroid hormone-related protein. Biochem. Biophys. Res. Commun. 158, 1036-1042 (1989).
82. Gardella, T.J., Luck, M.D., Fan, M.H. & Lee, C. Transmembrane residues of the parathyroid hormone (PTH)/PTH-related peptide receptor that specifcally affect binding and signaling by agonist ligands. J. Biol. Chem. 271, 12820-12825 (1996).