Improving FRET dynamic range with bright green and red fluorescent proteins

Nature Methods

Volumn 9, Issue 10, 2012, Pages 1005-1012

  Lam, Amy J ^a,b   St Pierre, François ^a,b   Gong, Yiyang ^b,c   Marshall, Jesse D ^b,c   Cranfill, Paula J ^d,e   Baird, Michelle A ^d,e   McKeown, Michael R ^f   Wiedenmann, Jörg ^g   Davidson, Michael W ^d,e   Schnitzer, Mark J ^b,c   Tsien, Roger Y ^f   Lin, Michael Z ^a,b  

^a Stanford University   (United States)

^b STANFORD UNIVERSITY   (United States)

^c STANFORD UNIVERSITY   (United States)

^d FLORIDA STATE UNIVERSITY   (United States)

^e FLORIDA STATE UNIVERSITY   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

^g UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

GREEN FLUORESCENT PROTEIN; GUANOSINE TRIPHOSPHATASE; RED FLUORESCENT PROTEIN;

ACTION POTENTIAL; ARTICLE; BIOCHEMISTRY; ENZYME ACTIVITY; FLUORESCENCE RESONANCE ENERGY TRANSFER; PHOTOTOXICITY; PRIORITY JOURNAL;

BASE SEQUENCE; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CYCLIC AMP-DEPENDENT PROTEIN KINASES; FLUORESCENCE RESONANCE ENERGY TRANSFER; GREEN FLUORESCENT PROTEINS; HEK293 CELLS; HELA CELLS; HUMANS; LUMINESCENT PROTEINS; MOLECULAR SEQUENCE DATA; RHOA GTP-BINDING PROTEIN;

TRIFOLIUM;

EID: 84867084476     PISSN: 15487091     EISSN: 15487105     Source Type: Journal    
DOI: 10.1038/nmeth.2171     Document Type: Article

References (51)

1. Reiff, D.F. et al. In vivo performance of genetically encoded indicators of neural activity in flies. J. Neurosci. 25, 4766-4778 (2005).
2. Shaner, N.C. et al. Improving the photostability of bright monomeric orange and red fluorescent proteins. Nat. Methods 5, 545-551 (2008).
3. Sinnecker, D., Voigt, P., Hellwig, N. & Schaefer, M. Reversible photobleaching of enhanced green fluorescent proteins. Biochemistry 44, 7085-7094 (2005).
4. Raarup, M.K. et al. Enhanced yellow fluorescent protein photoconversion to a cyan fluorescent protein-like species is sensitive to thermal and diffusion conditions. J. Biomed. Opt. 14, 034039 (2009).
5. Malkani, N. & Schmid, J.A. Some secrets of fluorescent proteins: distinct bleaching in various mounting fluids and photoactivation of cyan fluorescent proteins at YFP-excitation. PLoS ONE 6, e18586 (2011).
6. Dixit, R. & Cyr, R. Cell damage and reactive oxygen species production induced by fluorescence microscopy: effect on mitosis and guidelines for non-invasive fluorescence microscopy. Plant J. 36, 280-290 (2003).
7. Hockberger, P.E. et al. Activation of flavin-containing oxidases underlies light-induced production of H2O2 in mammalian cells. Proc. Natl. Acad. Sci. USA 96, 6255-6260 (1999).
8. Komatsu, N. et al. Development of an optimized backbone of FRET biosensors for kinases and GTPases. Mol. Biol. Cell 22, 4647-4656 (2011).
9. Kwok, S. et al. Genetically encoded probe for fluorescence lifetime imaging of CaMKII activity. Biochem. Biophys. Res. Commun. 369, 519-525 (2008).
10. Mutoh, H. et al. Spectrally-resolved response properties of the three most advanced FRET based fluorescent protein voltage probes. PLoS ONE 4, e4555 (2009).
11. Piston, D.W. & Kremers, G.J. Fluorescent protein FRET: the good, the bad and the ugly. Trends Biochem. Sci. 32, 407-414 (2007).
12. van der Krogt, G.N., 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 3, e1916 (2008).
13. Yasuda, R. et al. Supersensitive Ras activation in dendrites and spines revealed by two-photon fluorescence lifetime imaging. Nat. Neurosci. 9, 283-291 (2006).
14. Tsutsui, H., Karasawa, S., Okamura, Y. & Miyawaki, A. Improving membrane voltage measurements using FRET with new fluorescent proteins. Nat. Methods 5, 683-685 (2008).
15. Shcherbo, D. et al. Practical and reliable FRET/FLIM pair of fluorescent proteins. BMC Biotechnol. 9, 24 (2009).
16. Goedhart, J., Vermeer, J.E., Adjobo-Hermans, M.J., van Weeren, L. & Gadella, T.W.J. Sensitive detection of p65 homodimers using red-shifted and fluorescent protein-based FRET couples. PLoS ONE 2, e1011 (2007).
17. Piljic, A. & Schultz, C. Simultaneous recording of multiple cellular events by FRET. ACS Chem. Biol. 3, 156-160 (2008).
18. Kremers, G.J., Hazelwood, K.L., Murphy, C.S., Davidson, M.W. & Piston, D.W. Photoconversion in orange and red fluorescent proteins. Nat. Methods 6, 355-358 (2009).
19. Harvey, C.D. et al. A genetically encoded fluorescent sensor of ERK activity. Proc. Natl. Acad. Sci. USA 105, 19264-19269 (2008).
20. Kredel, S. et al. mRuby, a bright monomeric red fluorescent protein for labeling of subcellular structures. PLoS ONE 4, e4391 (2009).
21. 2+calmodulin- dependent protein kinase II activity in living neurons. J. Neurosci. 25, 3107-3112 (2005).
22. Zhang, J., Hupfeld, C.J., Taylor, S.S., Olefsky, J.M. & Tsien, R.Y. Insulin disrupts beta-adrenergic signalling to protein kinase A in adipocytes. Nature 437, 569-573 (2005).
23. Yoshizaki, H. et al. Activity of Rho-family GTPases during cell division as visualized with FRET-based probes. J. Cell Biol. 162, 223-232 (2003).
24. Monici, M. Cell and tissue autofluorescence research and diagnostic applications. Biotechnol. Annu. Rev. 11, 227-256 (2005).
25. Ormö, M. et al. Crystal structure of the Aequorea victoria green fluorescent protein. Science 273, 1392-1395 (1996).
26. Kennis, J.T. et al. Uncovering the hidden ground state of green fluorescent protein. Proc. Natl. Acad. Sci. USA 101, 17988-17993 (2004).
27. Brejc, K. et al. Structural basis for dual excitation and photoisomerization of the Aequorea victoria green fluorescent protein. Proc. Natl. Acad. Sci. USA 94, 2306-2311 (1997).
28. Henderson, J.N. et al. Structure and mechanism of the photoactivatable green fluorescent protein. J. Am. Chem. Soc. 131, 4176-4177 (2009).
29. Pédelacq, J.D., Cabantous, S., Tran, T., Terwilliger, T.C. & Waldo, G.S. Engineering and characterization of a superfolder green fluorescent protein. Nat. Biotechnol. 24, 79-88 (2006).
30. Goedhart, J. et al. Bright cyan fluorescent protein variants identified by fluorescence lifetime screening. Nat. Methods 7, 137-139 (2010).
31. Lin, M.Z. et al. Autofluorescent proteins with excitation in the optical window for intravital imaging in mammals. Chem. Biol. 16, 1169-1179 (2009).
32. Kredel, S. et al. Optimized and far-red-emitting variants of fluorescent protein eqFP611. Chem. Biol. 15, 224-233 (2008).
33. Aoki, K. & Matsuda, M. Visualization of small GTPase activity with fluorescence resonance energy transfer-based biosensors. Nat. Protoc. 4, 1623-1631 (2009).
34. Kotera, I., Iwasaki, T., Imamura, H., Noji, H. & Nagai, T. Reversible dimerization of Aequorea victoria fluorescent proteins increases the dynamic range of FRET-based indicators. ACS Chem. Biol. 5, 215-222 (2010).
35. Sakai, R., Repunte-Canonigo, V., Raj, C.D. & Knöpfel, T. Design and characterization of a DNA-encoded, voltage-sensitive fluorescent protein. Eur. J. Neurosci. 13, 2314-2318 (2001).
36. Lundby, A., Mutoh, H., Dimitrov, D., Akemann, W. & Knöpfel, T. Engineering of a genetically encodable fluorescent voltage sensor exploiting fast Ci-VSP voltage-sensing movements. PLoS ONE 3, e2514 (2008).
37. Akemann, W., Middleton, S.J. & Knöpfel, T. Optical imaging as a link between cellular neurophysiology and circuit modeling. Front. Cell. Neurosci. 3, 5 (2009).
38. Lundby, A., Akemann, W. & Knöpfel, T. Biophysical characterization of the fluorescent protein voltage probe VSFP2.3 based on the voltage-sensing domain of Ci-VSP. Eur. Biophys. J. 39, 1625-1635 (2010).
39. Wilt, B.A., Fitzgerald, J.E. & Schnitzer, M.J. Photon shot-noise limits on optical detection of neuronal spikes and estimation of spike timing. Biophys. J. (in the press).
40. Wahl, S., Barth, H., Ciossek, T., Aktories, K. & Mueller, B.K. Ephrin-A5 induces collapse of growth cones by activating Rho and Rho kinase. J. Cell Biol. 149, 263-270 (2000).
41. Shamah, S.M. et al. EphA receptors regulate growth cone dynamics through the novel guanine nucleotide exchange factor ephexin. Cell 105, 233-244 (2001).
42. Nestor, M.W., Mok, L.P., Tulapurkar, M.E. & Thompson, S.M. Plasticity of neuron-glial interactions mediated by astrocytic EphARs. J. Neurosci. 27, 12817-12828 (2007).
43. Nakamura, T., Aoki, K. & Matsuda, M. Monitoring spatio-temporal regulation of Ras and Rho GTPase with GFP-based FRET probes. Methods 37, 146-153 (2005).
44. Goedhart, J. et al. Structure-guided evolution of cyan fluorescent proteins towards a quantum yield of 93%. Nat. Commun. 3, 751 (2012).
45. Kralj, J.M., Douglass, A.D., Hochbaum, D.R., Maclaurin, D. & Cohen, A.E. Optical recording of action potentials in mammalian neurons using a microbial rhodopsin. Nat. Methods 9, 90-95 (2012).
46. Akemann, W. et al. Imaging neural circuit dynamics with a voltage-sensitive fluorescent protein. J. Neurophysiol. published online, doi:10.1152/jn.00452.2012 (18 July 2012).
47. Day, R.N. & Davidson, M.W. The fluorescent protein palette: tools for cellular imaging. Chem. Soc. Rev. 38, 2887-2921 (2009).
48. Cormack, B.P., Valdivia, R.H. & Falkow, S. FACS-optimized mutants of the green fluorescent protein (GFP). Gene 173, 33-38 (1996).
49. Merzlyak, E.M. et al. Bright monomeric red fluorescent protein with an extended fluorescence lifetime. Nat. Methods 4, 555-557 (2007).
50. 2+dependent calmodulin-target binding by Fura-2 and CFP and YFP FRET imaging in living cells. Biochemistry 50, 4685-4696 (2011).
51. Edelstein, A., Amodaj, N., Hoover, K., Vale, R. & Stuurman, N. Computer control of microscopes using μManager. Curr. Protoc. Mol. Biol. 92, 14.20 (2010).