A multiplexed fluorescent assay for independent second-messenger systems: Decoding GPCR activation in living cells

Journal of Biomolecular Screening

Volumn 18, Issue 7, 2013, Pages 797-806

  Tewson, Paul H ^a   Quinn, Anne Marie ^a   Hughes, Thomas E ^a,b  

^a Montana Molecular   (United States)

^b MONTANA STATE UNIVERSITY   (United States)

Author keywords

cell based assays; fluorescence methods; G protein coupled receptors (GPCR); multiplex assays and technology

Indexed keywords

CALCIUM ION; DIACYLGLYCEROL; FLUORESCENT DYE; G PROTEIN COUPLED RECEPTOR; GREEN FLUORESCENT PROTEIN; INOSITOL TRISPHOSPHATE; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; PHOSPHOLIPASE C; PROTEIN KINASE C DELTA; RED FLUORESCENT PROTEIN;

ARTICLE; BIOSENSOR; CALCIUM CELL LEVEL; CELL ASSAY; CELL MEMBRANE; CELL TRANSPORT; CONTROLLED STUDY; CYTOSOL; ENZYME ACTIVATION; FLUORESCENCE ANALYSIS; HUMAN; HUMAN CELL; INTRACELLULAR SIGNALING; MICROPLATE READER; PRIORITY JOURNAL; PROTEIN CLEAVAGE; SECOND MESSENGER;

EID: 84880812952     PISSN: 10870571     EISSN: 1552454X     Source Type: Journal    
DOI: 10.1177/1087057113485427     Document Type: Article

References (34)

1. Depry C., Mehta S., Zhang J.. Multiplexed Visualization of Dynamic Signaling Networks Using Genetically Encoded Fluorescent Protein-Based Biosensors. Pflugers Arch. 2013 ; 465: 373-381
2. Aye-Han N.-N., Allen M. D., Ni Q., Zhang J.. Parallel Tracking of cAMP and PKA Signaling Dynamics in Living Cells with FRET-Based Fluorescent Biosensors. Mol. Biosyst. 2012 ; 8: 1435-1440
3. Zaccolo M., Pozzan T.. cAMP and Ca2+ Interplay: A Matter of Oscillation Patterns. Trends Neurosci. 2003 ; 26: 53-55
4. Borodinsky L. N., Spitzer N. C.. Second Messenger Pas de Deux: The Coordinated Dance Between Calcium and cAMP. Sci. STKE. 2006 ; 2006: pe22
5. Violin J. D., Lefkowitz R. J.. Beta-Arrestin-Biased Ligands at Seven-Transmembrane Receptors. Trends Pharmacol. Sci. 2007 ; 28: 416-422
6. Rajagopal S., Ahn S., Rominger D. H., Gowen-MacDonald W., Lam C. M., DeWire S. M., Violin J. D., Lefkowitz R. J.. Quantifying Ligand Bias at Seven-Transmembrane Receptors. Mol. Pharmacol. 2011 ; 80: 367-377
7. Rajagopal S., Rajagopal K., Lefkowitz R. J.. Teaching Old Receptors New Tricks: Biasing Seven-Transmembrane Receptors. Nat. Rev. Drug Discov. 2010 ; 9: 373-386
8. Liu J. J., Horst R., Katritch V., Stevens R. C., Wuthrich K.. Biased Signaling Pathways in 2-Adrenergic Receptor Characterized by 19F-NMR. Science. 2012 ; 335: 1106-1110
9. Saulière A., Bellot M., Paris H., Denis C., Finana F., Hansen J. T., Altié M.-F., Seguelas M.-H., Pathak A., Hansen J. L., et al. Deciphering Biased-Agonism Complexity Reveals a New Active AT1 Receptor Entity. Nat. Chem. Biol. 2012 ; 8: 622-630
10. Raehal K. M., Walker J. K. L., Bohn L. M.. Morphine Side Effects in Beta-Arrestin 2 Knockout Mice. J. Pharmacol. Exp. Ther. 2005 ; 314: 1195-1201
11. Palmer A. E., Qin Y., Park J. G., McCombs J. E.. Design and Application of Genetically Encoded Biosensors. Trends Biotechnol. 2011 ; 29: 144-152
12. Ibraheem A., Campbell R. E.. Designs and Applications of Fluorescent Protein-Based Biosensors. Curr. Opin. Chem. Biol. 2010 ; 14: 30-36
13. Akerboom J., Rivera J. D. V., Guilbe M. M. R., Malave E. C. A., Hernandez H. H., Tian L., Hires S. A., Marvin J. S., Looger L. L., Schreiter E. R.. Crystal Structures of the GCaMP Calcium Sensor Reveal the Mechanism of Fluorescence Signal Change and Aid Rational Design. J. Biol. Chem. 2008 ; 284: 6455-6464
14. Akerboom J., Chen T.-W., Wardill T. J., Tian L., Marvin J. S., Mutlu S., Calderón N. C., Esposti F., Borghuis B. G., Sun X. R., et al. Optimization of a GCaMP Calcium Indicator for Neural Activity Imaging. J. Neurosci. 2012 ; 32: 13819-13840
15. Nakai J., Ohkura M., Imoto K.. A High Signal-to-Noise Ca(2+) Probe Composed of a Single Green Fluorescent Protein. Nat. Biotechnol. 2001 ; 19: 137-141
16. Zhao Y., Araki S., Wu J., Teramoto T., Chang Y.-F., Nakano M., Abdelfattah A. S., Fujiwara M., Ishihara T., Nagai T.. An Expanded Palette of Genetically Encoded Ca2+ Indicators. Sci. Signal. 2011 1888 ; 333 :
17. Barnett L., Platisa J., Popovic M., Pieribone V. A., Hughes T.. A Fluorescent, Genetically-Encoded Voltage Probe Capable of Resolving Action Potentials. PLoS ONE. 2012 ; 7: e43454
18. Nausch L. W. M., Ledoux J., Bonev A. D., Nelson M. T., Dostmann W. R.. Differential Patterning of cGMP in Vascular Smooth Muscle Cells Revealed by Single GFP-Linked Biosensors. Proc. Natl. Acad. Sci. U. S. A. 2007 ; 105: 365
19. Tewson P., Westenberg M., Zhao Y., Campbell R. E., Quinn A. M., Hughes T. E.. Simultaneous Detection of Ca2+ and Diacylglycerol Signaling in Living Cells. PLoS ONE. 2012 ; 7: e42791
20. Shaw G., Morse S., Ararat M., Graham F. L.. Preferential Transformation of Human Neuronal Cells by Human Adenoviruses and the Origin of HEK 293 Cells. FASEB J. 2002 ; 16: 869-871
21. Dries D. R., Gallegos L. L., Newton A. C.. A Single Residue in the C1 Domain Sensitizes Novel Protein Kinase C Isoforms to Cellular Diacylglycerol Production. J. Biol. Chem. 2007 ; 282: 826-830
22. Giorgione J. R., Lin J.-H., McCammon J. A., Newton A. C.. Increased Membrane Affinity of the C1 Domain of Protein Kinase Cdelta Compensates for the Lack of Involvement of Its C2 Domain in Membrane Recruitment. J. Biol. Chem. 2006 ; 281: 1660-1669
23. Jensen J. B., Lyssand J. S., Hague C., Hille B.. Fluorescence Changes Reveal Kinetic Steps of Muscarinic Receptor-Mediated Modulation of Phosphoinositides and Kv7.2/7.3 K+ Channels. J. Gen. Physiol. 2009 ; 133: 347-359
24. Falkenburger B. H., Jensen J. B., Hille B.. Kinetics of M1 Muscarinic Receptor and G protein Signaling to Phospholipase C in Living Cells. J. Gen. Physiol. 2010 ; 135: 81-97
25. Alford S. C., Abdelfattah A. S., Ding Y., Campbell R. E.. A Fluorogenic Red Fluorescent Protein Heterodimer. Chem. Biol. 2012 ; 19: 353-360
26. Kavran J. M., Klein D. E., Lee A., Falasca M., Isakoff S. J., Skolnik E. Y., Lemmon M. A.. Specificity and Promiscuity in Phosphoinositide Binding by Pleckstrin Homology Domains. J. Biol. Chem. 1998 ; 273: 30497-30508
27. van der Wal J.. Monitoring Agonist-Induced Phospholipase C Activation in Live Cells by Fluorescence Resonance Energy Transfer. J. Biol. Chem. 2001 ; 276: 15337-15344
28. White P. J., Webb T. E., Boarder M. R.. Characterization of a Ca2+ Response to Both UTP and ATP at Human P2Y11 Receptors: Evidence for Agonist-Specific Signaling. Mol. Pharmacol. 2003 ; 63: 1356-1363
29. Zhang J., Chung T., Oldenburg K.. A Simple Statistical Parameter for Use in Evaluation and Validation of High Throughput Screening Assays. J. Biomol. Screen. 1999 ; 4: 67-73
30. Wu J., Liu L., Matsuda T., Zhao Y., Rebane A., Drobizhev M., Chang Y.-F., Araki S., Arai Y., March K., et al. Improved Orange and Red Ca2+ Indicators and Photophysical Considerations for Optogenetic Applications. ACS Chem. Neurosci.. in press ;:
31. Kost T. A., Condreay J. P., Ames R. S., Rees S., Romanos M. A.. Implementation of BacMam Virus Gene Delivery Technology in a Drug Discovery Setting. Drug Discov. Today. 2007 ; 12: 396-403
32. Schroeder K. S.. FLIPR: A New Instrument for Accurate, High Throughput Optical Screening. J. Biomol. Screen. 1996 ; 1: 75-80
33. Poul E. L., Hisada S., Mizuguchi Y., Dupriez V. J., Burgeon E., Detheux M.. Adaptation of Aequorin Functional Assay to High Throughput Screening. J. Biomol. Screen. 2002 ; 7: 57-65
34. Conklin B. R., Farfel Z., Lustig K. D., Julius D., Bourne H. R.. Substitution of Three Amino Acids Switches Receptor Specificity of Gq Alpha to That of Gi Alpha. Nature. 1993 ; 363: 274-276