Fourth-generation Epac-based FRET sensors for cAMP feature exceptional brightness, photostability and dynamic range: Characterization of dedicated sensors for FLIM, for ratiometry and with high affinity

PLoS ONE

Volumn 10, Issue 4, 2015, Pages

  Klarenbeek, Jeffrey ^a,c   Goedhart, Joachim ^b,c   Van Batenburg, Aernoud ^a,c   Groenewald, Daniella ^a,c   Jalink, Kees ^a,c  

^a NETHERLANDS CANCER INSTITUTE   (Netherlands)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

^c Van Leeuwenhoek Centre of Advanced Microscopy   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP; CALCIUM BINDING PROTEIN; FLUORESCENT DYE; GREEN FLUORESCENT PROTEIN; GUANINE NUCLEOTIDE EXCHANGE FACTOR; HYBRID PROTEIN; RAPGEF3 PROTEIN, HUMAN; VC6.1 CAMELEON PROTEIN, RECOMBINANT;

ARTICLE; BINDING AFFINITY; BIOSENSOR; BRIGHTNESS; CLONING; CONTROLLED STUDY; DISSOCIATION CONSTANT; DYNAMIC RANGE; EMBRYO; EXCHANGE PROTEIN DIRECTLY ACTIVATED BY CYCLIC AMP BASED FLUORESCENCE RESONANCE ENERGY TRANSFER SENSOR; FLUORESCENCE IMAGING; FLUORESCENCE RESONANCE ENERGY TRANSFER; FLUORESCENT LIFETIME IMAGING; HUMAN; HUMAN CELL; MEASUREMENT; PHOTOSTABILITY; PHYSICAL PARAMETERS; POINT MUTATION; PROCESS DESIGN; RATIOMETRY; SIGNAL NOISE RATIO; ANIMAL; CHEMISTRY; DEVICES; GENE EXPRESSION; GENETIC PROCEDURES; GENETICS; HEK293 CELL LINE; METABOLISM; MOUSE; NERVE CELL; OSTEOBLAST; PROCEDURES; REPORTER GENE; SIGNAL TRANSDUCTION; STANDARDS; TUMOR CELL LINE; ULTRASTRUCTURE;

ANIMALS; BIOSENSING TECHNIQUES; CALCIUM-BINDING PROTEINS; CELL LINE, TUMOR; CYCLIC AMP; FLUORESCENCE RESONANCE ENERGY TRANSFER; FLUORESCENT DYES; GENE EXPRESSION; GENES, REPORTER; GREEN FLUORESCENT PROTEINS; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HEK293 CELLS; HUMANS; MICE; NEURONS; OPTICAL IMAGING; OSTEOBLASTS; RECOMBINANT FUSION PROTEINS; SIGNAL TRANSDUCTION;

EID: 84929486051     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0122513     Document Type: Article

References (19)

1. DiPilato LM, Cheng X, Zhang J. Fluorescent indicators of cAMP and Epac activation reveal differential dynamics of cAMP signaling within discrete subcellular compartments. Proc Natl Acad Sci U S A 2004; 101: 16513-16518. PMID: 15545605
2. Nikolaev VO, Bunemann M, Hein L, Hannawacker A, Lohse MJ. Novel single chain cAMP sensors for receptor-induced signal propagation. J Biol Chem 2004; 279: 37215-37218. PMID: 15231839
3. Ponsioen B, Zhao J, Riedl J, Zwartkruis F, van der Krogt G, Zaccolo M, et al. Detecting cAMP-induced Epac activation by fluorescence resonance energy transfer: Epac as a novel cAMP indicator. EMBO Rep 2004; 5: 1176-1180. PMID: 15550931
4. Klarenbeek JB, Goedhart J, Hink MA, Gadella TW, Jalink K. A mTurquoise-based cAMP sensor for both FLIM and ratiometric read-out has improved dynamic range. PLoS One 2011; 6: e19170. doi: 10.1371/journal.pone.0019170 PMID: 21559477
5. van der Krogt GN, Ogink J, Ponsioen B, Jalink K. A comparison of donor-acceptor pairs for genetically encoded FRET sensors: application to the Epac cAMP sensor as an example. PLoS One 2008; 3: e1916. doi: 10.1371/journal.pone.0001916 PMID: 18382687
6. Salonikidis PS, Niebert M, Ullrich T, Bao G, Zeug A, Richter DW. An ion-insensitive cAMP biosensor for long term quantitative ratiometric fluorescence resonance energy transfer (FRET) measurements under variable physiological conditions. J Biol Chem 2011; 286: 23419-23431. doi: 10.1074/jbc.M111.236869 PMID: 21454618
7. Baird GS, Zacharias DA, Tsien RY. Circular permutation and receptor insertion within green fluorescent proteins. Proc Natl Acad Sci U S A 1999; 96: 11241-11246. PMID: 10500161
8. Nagai T, Yamada S, Tominaga T, Ichikawa M, Miyawaki A. Expanded dynamic range of fluorescent indicators for Ca(2+) by circularly permuted yellow fluorescent proteins. Proc Natl Acad Sci U S A 2004; 101: 10554-10559. PMID: 15247428
9. Katayama H, Yamamoto A, Mizushima N, Yoshimori T, Miyawaki A. GFP-like proteins stably accumulate in lysosomes. Cell Struct Funct 2008; 33: 1-12. PMID: 18256512
10. Goedhart J, von Stetten D, Noirclerc-Savoye M, Lelimousin M, Joosen L, Hink MA, et al. Structure-guided evolution of cyan fluorescent proteins towards a quantum yield of 93%. Nat Commun 2012; 3: 751. doi: 10.1038/ncomms1738 PMID: 22434194
11. Ganesan S, Ameer-Beg SM, Ng TT, Vojnovic B, Wouters FS. A dark yellow fluorescent protein (YFP)-based Resonance Energy-Accepting Chromoprotein (REACh) for Forster resonance energy transfer with GFP. Proc Natl Acad Sci U S A 2006; 103: 4089-4094. PMID: 16537489
12. Murakoshi H, Lee SJ, Yasuda R. Highly sensitive and quantitative FRET-FLIM imaging in single dendritic spines using improved non-radiative YFP. Brain Cell Biol 2008; 36: 31-42. doi: 10.1007/s11068-008-9024-9 PMID: 18512154
13. Dao KK, Teigen K, Kopperud R, Hodneland E, Schwede F, Christensen AE, et al. Epac1 and cAMP-dependent protein kinase holoenzyme have similar cAMP affinity, but their cAMP domains have distinct structural features and cyclic nucleotide recognition. J Biol Chem 2006; 281: 21500-21511. PMID: 16728394
14. Rehmann H, Schwede F, Doskeland SO, Wittinghofer A, Bos JL. Ligand-mediated activation of the cAMP-responsive guanine nucleotide exchange factor Epac. J Biol Chem 2003; 278: 38548-38556. PMID: 12888551
15. Goedhart J, van Weeren L, Hink MA, Vischer NO, Jalink K, Gadella TW. Bright cyan fluorescent protein variants identified by fluorescence lifetime screening. Nat Methods 2010; 7: 137-139. doi: 10.1038/nmeth.1415 PMID: 20081836
16. Qiao J, Mei FC, Popov VL, Vergara LA, Cheng X. Cell cycle-dependent subcellular localization of exchange factor directly activated by cAMP. J Biol Chem 2002; 277: 26581-26586. PMID: 12000763
17. Markwardt ML, Kremers GJ, Kraft CA, Ray K, Cranfill PJ, Wilson KA, et al. An improved cerulean fluorescent protein with enhanced brightness and reduced reversible photoswitching. PLoS One 2011; 6: e17896. doi: 10.1371/journal.pone.0017896 PMID: 21479270
18. Griesbeck O, Baird GS, Campbell RE, Zacharias DA, Tsien RY. Reducing the environmental sensitivity of yellow fluorescent protein. Mechanism and applications. J Biol Chem 2001; 276: 29188-29194. PMID: 11387331
19. Polito M, Klarenbeek J, Jalink K, Paupardin-Tritsch D, Vincent P, Castro LR. The NO/cGMP pathway inhibits transient cAMP signals through the activation of PDE2 in striatal neurons. Front Cell Neurosci 2013; 7: 211. doi: 10.3389/fncel.2013.00211 PMID: 24302895