Fluorescence Lifetime Readouts of Troponin-C-Based Calcium FRET Sensors: A Quantitative Comparison of CFP and mTFP1 as Donor Fluorophores

PLoS ONE

Volumn 7, Issue 11, 2012, Pages

  Laine, Romain ^a   Stuckey, Daniel W ^a,b   Manning, Hugh ^a   Warren, Sean C ^a   Kennedy, Gordon ^a   Carling, David ^a   Dunsby, Chris ^a   Sardini, Alessandro ^a   French, Paul M W ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; CYAN FLUORESCENT PROTEIN; FLUORESCENT DYE; MONOMERIC TEAL FLUORESCENT PROTEIN 1; TROPONIN C; UNCLASSIFIED DRUG;

AFFINITY LABELING; ANIMAL CELL; ARTICLE; BIOSENSOR; CELL STRAIN HEK293; COMPARATIVE STUDY; CONFORMATION; CONTROLLED STUDY; CYTOSOL; DATA ANALYSIS; EMBRYO; EMISSION WAVELENGTH; FLUORESCENCE LIFETIME; FLUORESCENCE QUENCHING; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; NONHUMAN; PHOTON; PHYSICAL PARAMETERS; PHYSICAL PHENOMENA; TEMPERATURE; TITRIMETRY;

BIOSENSING TECHNIQUES; CALCIUM; CYTOSOL; FLUORESCENCE RESONANCE ENERGY TRANSFER; FLUORESCENT DYES; GREEN FLUORESCENT PROTEINS; HEK293 CELLS; HUMANS; LUMINESCENT PROTEINS; MICROSCOPY, FLUORESCENCE; MUTANT PROTEINS; PROTEIN CONFORMATION; REPRODUCIBILITY OF RESULTS; TEMPERATURE; TIME FACTORS; TITRIMETRY; TROPONIN C;

MAMMALIA;

EID: 84869044166     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0049200     Document Type: Article

References (51)

1. Clapham DE, (1995) CALCIUM SIGNALING. Cell 80: 259-268.
2. Berridge MJ, Lipp P, Bootman MD, (2000) The versatility and universality of calcium signalling. Nature Reviews Molecular Cell Biology 1: 11-21.
3. Carafoli E, (2004) Calcium-mediated cellular signals: a story of failures. Trends in Biochemical Sciences 29: 371-379.
4. Mank M, Griesbeck O, (2008) Genetically encoded calcium indicators. Chemical Reviews 108: 1550-1564.
5. Nakai J, Ohkura M, Imoto K, (2001) A high signal-to-noise Ca2+ probe composed of a single green fluorescent protein. Nature Biotechnology 19: 137-141.
6. Nagai T, Sawano A, Park ES, Miyawaki A, (2001) Circularly permuted green fluorescent proteins engineered to sense Ca2+. Proceedings of the National Academy of Sciences of the United States of America 98: 3197-3202.
7. Zhao YX, Araki S, Jiahui WH, Teramoto T, Chang YF, et al. (2011) An Expanded Palette of Genetically Encoded Ca2+ Indicators. Science 333: 1888-1891.
8. Tang S, Wong HC, Wang ZM, Huang Y, Zou J, et al. (2011) Design and application of a class of sensors to monitor Ca2+ dynamics in high Ca2+ concentration cellular compartments. Proceedings of the National Academy of Sciences of the United States of America 108: 16265-16270.
9. Miyawaki A, Llopis J, Heim R, McCaffery JM, Adams JA, et al. (1997) Fluorescent indicators for Ca2+ based on green fluorescent proteins and calmodulin. Nature 388: 882-887.
10. Garaschuk O, Griesbeck O, Konnerth A, (2007) Troponin C-based biosensors: A new family of genetically encoded indicators for in vivo calcium imaging in the nervous system. Cell Calcium 42: 351-361.
11. Heim N, Griesbeck O, (2004) Genetically encoded indicators of cellular calcium dynamics based on troponin C and green fluorescent protein. J Biol Chem 279: 14280-14286.
12. Mank M, Reiff DF, Heim N, Friedrich MW, Borst A, et al. (2006) A FRET-based calcium biosensor with fast signal kinetics and high fluorescence change. Biophys J 90: 1790-1796.
13. Griesbeck O, Baird GS, Campbell RE, Zacharias DA, Tsien RY, (2001) Reducing the environmental sensitivity of yellow fluorescent protein- Mechanism and applications. Journal of Biological Chemistry 276: 29188-29194.
14. Lakowicz JR (2006) Pinciples of Fluorescence Spectroscopy. NY: Springer.
15. Ting AY, Kain KH, Klemke RL, Tsien RY, (2001) Genetically encoded fluorescent reporters of protein tyrosine kinase activities in living cells. Proceedings of the National Academy of Sciences of the United States of America 98: 15003-15008.
16. Markova O, Mukhtarov M, Real E, Jacob Y, Bregestovski P, (2008) Genetically encoded chloride indicator with improved sensitivity. Journal of Neuroscience Methods 170: 67-76.
17. Becker W, Bergmann A, Hink MA, Konig K, Benndorf K, et al. (2004) Fluorescence lifetime imaging by time-correlated single-photon counting. Microscopy Research and Technique 63: 58-66.
18. Wouters FS, Bastiaens PIH, (1999) Fluorescence lifetime imaging of receptor tyrosine kinase activity in cells. Current Biology 9: 1127-1130.
19. Tramier M, Gautier I, Piolot T, Ravalet S, Kemnitz K, et al. (2002) Picosecond-hetero-FRET microscopy to probe protein-protein interactions in live cells. Biophysical Journal 83: 3570-3577.
20. Berney C, Danuser G, (2003) FRET or no FRET: A quantitative comparison. Biophysical Journal 84: 3992-4010.
21. Suhling K, French PMW, Phillips D, (2005) Time-resolved fluorescence microscopy. Photochemical & Photobiological Sciences 4: 13-22.
22. Heim R, Tsien RY, (1996) Engineering green fluorescent protein for improved brightness, longer wavelengths and fluorescence resonance energy transfer. Current Biology 6: 178-182.
23. Rizzo MA, Springer GH, Granada B, Piston DW, (2004) An improved cyan fluorescent protein variant useful for FRET. Nature Biotechnology 22: 445-449.
24. Bourett TM, Sweigard JA, Czymmek KJ, Carroll A, Howard RJ, (2002) Reef coral fluorescent proteins for visualizing fungal pathogens. Fungal Genetics and Biology 37: 211-220.
25. Villoing A, Ridhoir M, Cinquin B, Erard M, Alvarez L, et al. (2008) Complex Fluorescence of the Cyan Fluorescent Protein: Comparisons with the H148D Variant and Consequences for Quantitative Cell Imaging. Biochemistry 47: 12483-12492.
26. Yasuda R, Harvey CD, Zhong HN, Sobczyk A, van Aelst L, et al. (2006) Supersensitive Ras activation in dendrites and spines revealed by two-photon fluorescence lifetime imaging. Nature Neuroscience 9: 283-291.
27. Goedhart J, van Weeren L, Hink MA, Vischer NOE, Jalink K, et al. (2010) Bright cyan fluorescent protein variants identified by fluorescence lifetime screening. Nature Methods 7: 137-U174.
28. Ai HW, Henderson JN, Remington SJ, Campbell RE, (2006) Directed evolution of a monomeric, bright and photostable version of Clavularia cyan fluorescent protein: structural characterization and applications in fluorescence imaging. Biochemical Journal 400: 531-540.
29. Visser A, Laptenok SP, Visser NV, van Hoek A, Birch DJS, et al. (2010) Time-resolved FRET fluorescence spectroscopy of visible fluorescent protein pairs. European Biophysics Journal with Biophysics Letters 39: 241-253.
30. Day RN, Booker CF, Periasamy A, (2008) Characterization of an improved donor fluorescent protein for Forster resonance energy transfer microscopy. Journal of Biomedical Optics 13.
31. Geiger A, Russo L, Gensch T, Thestrup T, Becker S, et al. (2012) Correlating Calcium Binding, Forster Resonance Energy Transfer, and Conformational Change in the Biosensor TN-XXL. Biophysical Journal 102: 2401-2410.
32. McGinty J, Stuckey DW, Soloviev VY, Laine R, Wylezinska-Arridge M, et al. (2011) In vivo fluorescence lifetime tomography of a FRET probe expressed in mouse. Biomedical optics express 2: 1907-1917.
33. Borst JW, Laptenok SP, Westphal AH, Kuhnemuth R, Hornen H, et al. (2008) Structural changes of yellow Cameleon domains observed by quantitative FRET analysis and polarized fluorescence correlation spectroscopy. Biophys J 95: 5399-5411.
34. Manning HB, Kennedy GT, Owen DM, Grant DM, Magee AI, et al. (2008) A compact, multidimensional spectrofluorometer exploiting supercontinuum generation. J Biophotonics 1: 494-505.
35. Tsien R, Pozzan T, (1989) MEASUREMENT OF CYTOSOLIC FREE CA-2+ WITH QUIN2. Methods in Enzymology 172: 230-262.
36. Clayton AHA, Hanley QS, Verveer PJ, (2004) Graphical representation and multicomponent analysis of single-frequency fluorescence lifetime imaging microscopy data. Journal of Microscopy-Oxford 213: 1-5.
37. Verveer PJ, Bastiaens PIH, (2003) Evaluation of global analysis algorithms for single frequency fluorescence lifetime imaging microscopy data. Journal of Microscopy-Oxford 209: 1-7.
38. Kumar S, Alibhai D, Margineanu A, Laine R, Kennedy G, et al. (2011) FLIM FRET Technology for Drug Discovery: Automated Multiwell-Plate High-Content Analysis, Multiplexed Readouts and Application in Situ. Chemphyschem 12: 609-626.
39. Palmer AE, Tsien RY, (2006) Measuring calcium signaling using genetically targetable fluorescent indicators. Nature Protocols 1: 1057-1065.
40. Swaminathan R, Hoang CP, Verkman AS, (1997) Photobleaching recovery and anisotropy decay of green fluorescent protein GFP-S65T in solution and cells: Cytoplasmic viscosity probed by green fluorescent protein translational and rotational diffusion. Biophysical Journal 72: 1900-1907.
41. Gautier I, Tramier M, Durieux C, Coppey J, Pansu RB, et al. (2001) Homo-FRET microscopy in living cells to measure monomer-dimer transition of GFP-tagged proteins. Biophysical Journal 80: 3000-3008.
42. Subramaniam V, Hanley QS, Clayton AHA, Jovin TM, (2003) Photophysics of green and red fluorescent proteins: Implications for quantitative microscopy. Biophotonics, Pt A 360: 178-201.
43. Tramier M, Zahid M, Mevel JC, Masse MJ, Coppey-Moisan M, (2006) Sensitivity of CFP/YFP and GFP/mCherry pairs to donor photobleaching on FRET determination by fluorescence lifetime imaging microscopy in living cells. Microscopy Research and Technique 69: 933-939.
44. Sun YS, Wallrabe H, Booker CF, Day RN, Periasamy A, (2010) Three-Color Spectral FRET Microscopy Localizes Three Interacting Proteins in Living Cells. Biophysical Journal 99: 1274-1283.
45. Sun YS, Booker CF, Kumari S, Day RN, Davidson M, et al. (2009) Characterization of an orange acceptor fluorescent protein for sensitized spectral fluorescence resonance energy transfer microscopy using a white-light laser. Journal of Biomedical Optics 14.
46. Kim J, Kwon D, Lee J, Pasquier H, Grailhe R, (2009) The use of cyan fluorescent protein variants with a distinctive lifetime signature. Molecular Biosystems 5: 151-153.
47. Millington M, Grindlay GJ, Altenbach K, Neely RK, Kolch W, et al. (2007) High-precision FLIM-FRET in fixed and living cells reveals heterogeneity in a simple CFP-YFP fusion protein. Biophysical Chemistry 127: 155-164.
48. Seifert MH, Ksiazek D, Azim MK, Smialowski P, Budisa N, et al. (2002) Slow exchange in the chromophore of a green fluorescent protein variant. Journal of the American Chemical Society 124: 7932-7942.
49. Koushik SV, Chen H, Thaler C, Puhl HL, Vogel SS, (2006) Cerulean, Venus, and Venus(Y67C) FRET reference standards. Biophysical Journal 91: L99-L101.
50. Koushik SV, Blank PS, Vogel SS, (2009) Anomalous Surplus Energy Transfer Observed with Multiple FRET Acceptors. Plos One 4.
51. Padilla-Parra S, Auduge N, Lalucque H, Mevel JC, Coppey-Moisan M, et al. (2009) Quantitative Comparison of Different Fluorescent Protein Couples for Fast FRET-FLIM Acquisition. Biophysical Journal 97: 2368-2376.