A broad G protein-coupled receptor internalization assay that combines SNAP-tag labeling, diffusion-enhanced resonance energy transfer, and a highly emissive terbium cryptate

Frontiers in Endocrinology

Volumn 6, Issue NOV, 2015, Pages

  Levoye, Angélique ^a   Zwier, Jurriaan M ^b   Jaracz Ros, Agnieszka ^c   Klipfel, Laurence ^c   Cottet, Martin ^d,e   Maurel, Damien ^d   Bdioui, Sara ^b   Balabanian, Karl ^c   Prézeau, Laurent ^d   Trinquet, Eric ^b   Durroux, Thierry ^d   Bachelerie, Françoise ^c  

^a Site Xavier Bichat and Département Hospitalo Universitaire Fibrosis Inflammation and Remodeling   (France)

^b CisBio Bioassays   (France)

^c INSERM   (France)

^d INSTITUT DE GÉNOMIQUE FONCTIONNELLE   (France)

^e CENTRE DE RECHERCHE DE L INSTITUT UNIVERSITAIRE EN SANTÉ MENTALE DE QUÉBEC   (Canada)

Author keywords

CXCR4; CXCR7; DERET; GPCRs; HTRF; Internalization; Lumi4 Tb; V1a

Indexed keywords

CHEMOKINE RECEPTOR CXCR4; CHEMOKINE RECEPTOR CXCR7; DELTA OPIATE RECEPTOR; G PROTEIN COUPLED RECEPTOR; OPIATE RECEPTOR; SNARE PROTEIN; VASOPRESSIN; VASOPRESSIN V1A RECEPTOR;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DIFFUSION ENHANCED RESONANCE ENERGY TRANSFER; EC50; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; MEASUREMENT; NONHUMAN; POLYMERASE CHAIN REACTION; PROTEIN EXPRESSION; SIGNAL NOISE RATIO;

EID: 84949808121     PISSN: None     EISSN: 16642392     Source Type: Journal    
DOI: 10.3389/fendo.2015.00167     Document Type: Article

References (57)

1. Bockaert J, Pin J-P. Molecular tinkering of G protein-coupled receptors: an evolutionary success. EMBO J (1999) 18(7):1723-9. doi: 10.1093/emboj/18.7.1723
2. Ferguson SSG. Evolving concepts in G protein-coupled receptor endocytosis: the role in receptor desensitization and signaling. Pharmacol Rev (2001) 53:1-24.
3. Calebiro D, Nikolaev VO, Persani L, Lohse MJ. Signaling by internalized G-protein-coupled receptors. Trends Pharmacol Sci (2010) 31:221-8. doi:10.1016/j.tips.2010.02.002
4. Graham GJ, Locati M, Mantovani A, Rot A, Thelen M. The biochemistry and biology of the atypical chemokine receptors. Immunol Lett (2012) 145(1-2):30-8. doi:10.1016/j.imlet.2012.04.004
5. Garippa RJ, Hoffman AF, Gradl G, Kirsch A. High-Throughput Confocal Microscopy for β-arrestin Green Fluorescent Protein Translocation G Protein-Coupled Receptor Assays Using the Evotec Opera. In: Inglese J, editor. Measuring Biological Responses with Automated Microscopy (Vol. 414), San Diego, CA: Academic Press (2006). p. 99-120. doi:10.1016/S0076-6879(06)14007-0
6. Eriksen J, Bjørn-Yoshimoto WE, Jørgensen TN, Newman AH, Gether U. Postendocytic sorting of constitutively internalized dopamine transporter in cell lines and dopaminergic neurons 10.1074/jbc.M110.131003. J Biol Chem (2010) 285(35):27289-301. doi:10.1074/jbc.M110.131003
7. Hamdan FF, Audet M, Garneau P, Pelletier J, Bouvier M. High-throughput screening of G protein-coupled receptor antagonists using a bioluminescence resonance energy transfer 1-Based β-Arrestin2 recruitment assay 10.1177/1087057105275344. J Biomol Screen (2005) 10(5):463-75. doi:10.1177/1087057105275344
8. Lam VM, Beerepoot P, Angers S, Salahpour A. A novel assay for measurement of membrane-protein surface expression using a beta-lactamase. Traffic (2013) 14(7):778-84. doi:10.1111/tra.12073
9. Hammer MM, Wehrman TS, Blau HM. A novel enzyme complementation-based assay for monitoring G-protein-coupled receptor internalization. FASEB J (2007) 21(14):3827-34. doi:10.1096/fj.07-8777com
10. Alvarez-Curto E, Prihandoko R, Tautermann CS, Zwier JM, Pediani JD, Lohse MJ, et al. Developing chemical genetic approaches to explore G protein-coupled receptor function: validation of the use of a receptor activated solely by synthetic ligand (RASSL). Mol Pharmacol (2011) 80(6):1033-46. doi:10.1124/mol.111.074674
11. Ashby MC, Ibaraki K, Henley JM. It's green outside: tracking cell surface proteins with pH-sensitive GFP. Trends Neurosci (2004) 27(5):257-61. doi:10.1016/j.tins.2004.03.010
12. Robers MB, Binkowski BF, Cong M, Zimprich C, Corona C, McDougall M, et al. A luminescent assay for real-time measurements of receptor endocytosis in living cells. Anal Biochem (2015) 489:1-8. doi:10.1016/j.ab.2015.08.005
13. Fisher GW, Adler SA, Fuhrman MH, Waggoner AS, Bruchez MP, Jarvik JW. Detection and quantification of beta2AR internalization in living cells using FAP-based biosensor technology. J Biomol Screen (2010) 15(6):703-9. doi:10.1177/1087057110370892
14. Maurel D, Comps-Agrar L, Brock C, Rives ML, Bourrier E, Ayoub MA, et al. Cell-surface protein-protein interaction analyses with time-resolved FRET and snap-tag technologies: application to GPCR oligomerization. Nat Methods (2008) 5:561-7. doi:10.1038/nmeth.1213
15. Levoye A, Balabanian K, Baleux F, Bachelerie F, Lagane B. CXCR7 heterodimerizes with CXCR4 and regulates CXCL12-mediated G protein signaling 10.1182/blood-2008-12-196618. Blood (2009) 113(24):6085-93. doi:10.1182/blood-2008-12-196618
16. Doumazane E, Scholler P, Zwier JM, Trinquet E, Rondard P, Pin JP. A new approach to analyze cell surface protein complexes reveals specific heterodimeric metabotropic glutamate receptors. FASEB J (2011) 25(1):66-77. doi:10.1096/fj.10-163147
17. Zwier JM, Roux T, Cottet M, Durroux T, Douzon S, Bdioui S, et al. A fluorescent ligand-binding alternative using Tag-lite(R) technology. J Biomol Screen (2010) 15(10):1248-59. doi:10.1177/1087057110384611
18. Faklaris O, Cottet M, Falco A, Villier B, Laget M, Zwier JM, et al. Multicolor time-resolved Forster resonance energy transfer microscopy reveals the impact of GPCR oligomerization on internalization processes. FASEB J (2015) 29(6):2235-46. doi:10.1096/fj.14-260059
19. Mathis G. Probing molecular interactions with homogeneous techniques based on rare earth cryptates and fluorescence energy transfer. Clin Chem (1995) 41:1391-7.
20. Olofsson L, Felekyan S, Doumazane E, Scholler P, Fabre L, Zwier JM, et al. Fine tuning of sub-millisecond conformational dynamics controls metabotropic glutamate receptors agonist efficacy. Nat Commun (2014) 5:5206. doi:10.1038/ncomms6206
21. Degorce F, Card A, Soh S, Trinquet E, Knapik GP, Xie B. HTRF: a technology tailored for drug discovery - a review of theoretical aspects and recent applications. Curr Chem Genomics (2009) 3:22-32. doi:10.2174/1875397300903010022
22. Trinquet E, Bouhelal R, Dietz M. Monitoring Gq-coupled receptor response through inositol phosphate quantification with the IP-One assay. Expert Opin Drug Discovery (2011) 6(10):981-94. doi:10.1517/17460441.2011.608658
23. Thomas DD, Carlsen WF, Stryer L. Fluorescence energy transfer in the rapid-diffusion limit. Proc Natl Acad Sci USA (1978) 75:5746-50. doi:10.1073/pnas.75.12.5746
24. Meares CF, Yeh SM, Stryer L. Exchange interaction contribution to energy transfer between ions in the rapid diffusion limit. J Am Chem Soc (1981) 103:1607-9. doi:10.1021/ja00396a073
25. Koresawa M, Kikuchi K, Mizukami S, Kojima H, Urano Y, Higuchi T, et al. Development of a time-resolved fluorometric detection system using diffusion-enhanced energy transfer. Anal Chem (2000) 72:4904-7. doi:10.1021/ac000356t
26. Meltzer RH, Lurtz MM, Wensel TG, Pedersen SE. Nicotinic acetylcholine receptor channel electrostatics determined by diffusion enhanced luminescence energy transfer. Biophys J (2006) 91:1315-24. doi:10.1529/biophysj.106.081448
27. Northrup SH, Wensel TG, Meares CF, Wendoloski JJ, Matthew JB. Electrostatic field around cytochrome c: theory and energy transfer experiment. Proc Natl Acad Sci USA (1990) 87:9503-7. doi:10.1073/pnas.87.23.9503
28. Zheng Q, Dai H, Merritt ME, Malloy C, Pan CY, Li WH. A new class of macrocyclic lanthanide complexes for cell labeling and magnetic resonance imaging applications. J Am Chem Soc (2005) 127:16178-88. doi:10.1021/ja054593v
29. Roed SN, Wismann P, Underwood CR, Kulahin N, Iversen H, Cappelen KA, et al. Real-time trafficking and signaling of the glucagon-like peptide-1 receptor. Mol Cell Endocrinol (2014) 382(2):938-49. doi:10.1016/j.mce.2013.11.010
30. Xu J, Corneillie TM, Moore EG, Law GL, Butlin NG, Raymond KN. Octodentate cages of Tb(III) 2-hydroxyisophtalamides: a new standard for luminescence lanthanide labels. J Am Chem Soc (2011) 133:19900-10. doi:10.1021/ja2079898
31. Keppler A, Gendreizig S, Gronemeyer T, Pick H, Vogel H, Johnsson K. A general method for the covalent labeling of fusion proteins with small molecules in vivo. Nat Biotechnol (2003) 21:86-9. doi:10.1038/nbt765
32. Komatsu T, Johnsson K, Okuno H, Bito H, Inoue T, Nagano T, et al. Real-time measurements of protein dynamics using fluorescence activation-coupled protein labeling method. J Am Chem Soc (2011) 133(17):6745-51. doi:10.1021/ja200225m
33. Cole NB, Donaldson JG. Releasable SNAP-tag probes for studying endocytosis and recycling. ACS Chem. Biol (2012) 7:464-9. doi:10.1021/cb2004252
34. Zwier JM, Bazin H, Lamarque L, Mathis G. Luminescent lanthanide cryptates: from the bench to the bedside. Inorg Chem (2014) 53(4):1854-66. doi:10.1021/ic402234k
35. Innamorati G, Le Gouill C, Balamotis M, Birnbaumer M. The long and the short cycle. Alternative intracellular routes for trafficking of G-protein-coupled receptors. J Biol Chem (2001) 276(16):13096-103. doi:10.1074/jbc.M009780200
36. Yang J, Yang H, Du X, Ma Q, Song J, Chen M, et al. Morphine and DAMGO produce an opposite effect on presynaptic glutamate release via different downstream pathways of mu opioid receptors in the basolateral amygdala. Neuropharmacology (2014) 86:353-61. doi:10.1016/j.neuropharm.2014.08.021
37. Charfi I, Nagi K, Mnie-Filali O, Thibault D, Balboni G, Schiller PW, et al. Ligand-and cell-dependent determinants of internalization and cAMP modulation by delta opioid receptor (DOR) agonists. Cell Mol Life Sci (2014) 71(8):1529-46. doi:10.1007/s00018-013-1461-7
38. Pradhan AAA, Becker JA, Scherrer G, Tryoen-Toth P, Filliol D, Matifas A, et al. Delta opioid receptor internalization controls behavioral effects of agonists. PLoS One (2009) 4(5):e5425. doi:10.1371/journal.pone.0005425
39. Balabanian K, Lagane B, Infantino S, Chow KY, Harriague J, Moepps B, et al. The chemokine SDF-1/CXCL12 binds to and signals through the orphan receptor RDC1 in T lymphocytes 10.1074/jbc.M508234200. J Biol Chem (2005) 280(42):35760-6. doi:10.1074/jbc.M508234200
40. Boldajipour B, Mahabaleshwar H, Kardash E, Reichman-Fried M, Blaser H, Minina S, et al. Control of chemokine-guided cell migration by ligand sequestration. Cell (2008) 132(3):463-73. doi:10.1016/j.cell.2007.12.034
41. Naumann U, Cameroni E, Pruenster M, Mahabaleshwar H, Raz E, Zerwes HG, et al. CXCR7 functions as a scavenger for CXCL12 and CXCL11. PLoS One (2010) 5(2):e9175. doi:10.1371/journal.pone.0009175
42. Kryczek I, Wei S, Keller E, Liu R, Zou W. Stroma-derived factor (SDF-1/CXCL12) and human tumor pathogenesis 10.1152/ajpcell.00406.2006. Am J Physiol Cell Physiol (2007) 292(3):C987-95. doi:10.1152/ajpcell.00406.2006
43. Freitas C, Desnoyer A, Meuris F, Bachelerie F, Balabanian K, Machelon V. The relevance of the chemokine receptor ACKR3/CXCR7 on CXCL12-mediated effects in cancers with a focus on virus-related cancers. Cytokine Growth Factor Rev (2014) 25(3):307-16. doi:10.1016/j.cytogfr.2014.04.006
44. Rajagopal S, Kim J, Ahn S, Craig S, Lam CM, Gerard NP, et al. Beta-arrestin-but not G protein-mediated signaling by the "decoy" receptor CXCR7. Proc Natl Acad Sci U S A (2009) 107:628-32. doi:10.1073/pnas.0912852107
45. Luker KE, Steele JM, Mihalko LA, Ray P, Luker GD. Constitutive and chemokine-dependent internalization and recycling of CXCR7 in breast cancer cells to degrade chemokine ligands. Oncogene (2010) 29(32):4599-610. doi:10.1038/onc.2010.212
46. Thelen M, Thelen S. CXCR7, CXCR4 and CXCL12: an eccentric trio? J Neuroimmunol (2008) 198(1-2):9-13. doi:10.1016/j.jneuroim.2008.04.020
47. De Clercq E. The AMD3100 story: the path to the discovery of a stem cell mobilizer (Mozobil). Biochem Pharmacol (2009) 77(11):1655-64. doi:10.1016/j.bcp.2008.12.014
48. Hachet-Haas M, Balabanian K, Rohmer F, Pons F, Franchet C, Lecat S, et al. Small neutralizing molecules to inhibit actions of the chemokine CXCL12. J Biol Chem (2008) 283(34):23189-99. doi:10.1074/jbc.M803947200
49. Di Salvo J, Koch GE, Johnson KE, Blake AD, Daugherty BL, DeMartino JA, et al. The CXCR4 agonist ligand stromal derived factor-1 maintains high affinity for receptors in both Galpha(i)-coupled and uncoupled states. Eur J Pharmacol (2000) 409(2):143-54. doi:10.1016/S0014-2999(00)00846-3
50. Gravel SP, Malouf C, Boulais PE, Berchiche YA, Oishi S, Fujii N, et al. The peptidomimetic CXCR4 antagonist TC14012 recruits β-Arrestin to CXCR7 10.1074/jbc.C110.147470. J Biol Chem (2010) 285(49):37939-43. doi:10.1074/jbc.C110.147470
51. Luker KE, Gupta M, Steele JM, Foerster BR, Luker GD. Imaging ligand-dependent activation of CXCR7. Neoplasia (2009) 11:1022-35. doi:10.1593/neo.09724
52. Zhang JH, Chung TD, Oldenburg KR. A simple statistical parameter for use in evaluation and validation of high throughput screening assays. J Biomol Screen (1999) 4(2):67-73. doi:10.1177/108705719900400206
53. Fourgeaud L, Bessis AS, Rossignol F, Pin JP, Olivo-Marin JC, Hémar A. The metabotropic glutamate receptor mGluR5 is endocytosed by a clathrin-independent pathway. J Biol Chem (2003) 278(14):12222-30. doi:10.1074/jbc.M205663200
54. Pou C, Mannoury la Cour C, Stoddart LA, Millan MJ, Milligan G. Functional homomers and heteromers of dopamine D2L and D3 receptors co-exist at the cell surface. J Biol Chem (2012) 287(12):8864-78. doi:10.1074/jbc.M111.326678
55. Loison S, Cottet M, Orcel H, Adihou H, Rahmeh R, Lamarque L, et al. Selective fluorescent nonpeptidic antagonists for vasopressin V(2) GPCR: application to ligand screening and oligomerization assays. J Med Chem (2012) 55(20):8588-602. doi:10.1021/jm3006146
56. Maurel D, Kniazeff J, Mathis G, Trinquet E, Pin JP, Ansanay H. Cell surface detection of membrane protein interaction with homogeneous time-resolved fluorescence resonance energy transfer technology. Anal Biochem (2004) 329(2):253-62. doi:10.1016/j.ab.2004.02.013
57. Hounsou C, Margathe JF, Oueslati N, Belhocine A, Dupuis E, Thomas C, et al. Time-resolved FRET binding assay to investigate hetero-oligomer binding properties: proof of concept with dopamine D1/D3 heterodimer. ACS Chem Biol (2015) 10(2):466-74. doi:10.1021/cb5007568