Red fluorescent protein with reversibly photoswitchable absorbance for photochromic FRET

Chemistry and Biology

Volumn 17, Issue 7, 2010, Pages 745-755

  Subach, Fedor V ^a   Zhang, Lijuan ^b   Gadella, Theodorus W J ^c   Gurskaya, Nadya G ^b   Lukyanov, Konstantin A ^b   Verkhusha, Vladislav V ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b SHEMYAKIN OVCHINNIKOV INSTITUTE OF BIOORGANIC CHEMISTRY   (Russian Federation)

^c UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

CHEMBIO

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; GROWTH FACTOR RECEPTOR BOUND PROTEIN 2; PHOTOPROTEIN; RED FLUORESCENT PROTEIN;

ARTICLE; CELL SURVIVAL; CHEMISTRY; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENETICS; HELA CELL; HUMAN; LIGHT; METABOLISM; METHODOLOGY; MUTAGENESIS; MUTATION; PROTEIN ENGINEERING; HELA CELL LINE; PROCEDURES;

CELL SURVIVAL; FLUORESCENCE RESONANCE ENERGY TRANSFER; GRB2 ADAPTOR PROTEIN; HELA CELLS; HUMANS; LIGHT; LUMINESCENT PROTEINS; MUTAGENESIS; MUTATION; PROTEIN ENGINEERING; RECEPTOR, EPIDERMAL GROWTH FACTOR;

EID: 77955452640     PISSN: 10745521     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.chembiol.2010.05.022     Document Type: Article

References (50)

1. V. Adam , M. Lelimousin , S. Boehme , G. Desfonds , K. Nienhaus , M.J. Field , J. Wiedenmann , S. McSweeney , G.U. Nienhaus , and D. Bourgeois Structural characterization of IrisFP, an optical highlighter undergoing multiple photo-induced transformations Proc. Natl. Acad. Sci. USA 105 2008 18343 18348
2. R. Ando , C. Flors , H. Mizuno , J. Hofkens , and A. Miyawaki Highlighted generation of fluorescence signals using simultaneous two-color irradiation on Dronpa mutants Biophys. J. 92 2007 L97 L99
3. R. Ando , H. Mizuno , and A. Miyawaki Regulated fast nucleocytoplasmic shuttling observed by reversible protein highlighting Science 306 2004 1370 1373
4. M. Andresen , A.C. Stiel , J. Folling , D. Wenzel , A. Schonle , A. Egner , C. Eggeling , S.W. Hell , and S. Jakobs Photoswitchable fluorescent proteins enable monochromatic multilabel imaging and dual color fluorescence nanoscopy Nat. Biotechnol. 26 2008 1035 1040
5. D.M. Chudakov , V.V. Belousov , A.G. Zaraisky , V.V. Novoselov , D.B. Staroverov , D.B. Zorov , S. Lukyanov , and K.A. Lukyanov Kindling fluorescent proteins for precise in vivo photolabeling Nat. Biotechnol. 21 2003 191 194
6. D.M. Chudakov , A.V. Feofanov , N.N. Mudrik , S. Lukyanov , and K.A. Lukyanov Chromophore environment provides clue to «kindling fluorescent protein» riddle J. Biol. Chem. 278 2003 7215 7219
7. F. Ciruela Fluorescence-based methods in the study of protein-protein interactions in living cells Curr. Opin. Biotechnol. 19 2008 338 343
8. P. Dedecker , J. Hotta , C. Flors , M. Sliwa , H. Uji-i , M.B. Roeffaers , R. Ando , H. Mizuno , A. Miyawaki , and J. Hofkens Subdiffraction imaging through the selective donut-mode depletion of thermally stable photoswitchable fluorophores: numerical analysis and application to the fluorescent protein Dronpa J. Am. Chem. Soc. 129 2007 16132 16141
9. A. Egner , C. Geisler , C. von Middendorff , H. Bock , D. Wenzel , R. Medda , M. Andresen , A.C. Stiel , S. Jakobs , and C. Eggeling Fluorescence nanoscopy in whole cells by asynchronous localization of photoswitching emitters Biophys. J. 93 2007 3285 3290
10. C. Flors , J. Hotta , H. Uji-i , P. Dedecker , R. Ando , H. Mizuno , A. Miyawaki , and J. Hofkens A stroboscopic approach for fast photoactivation- localization microscopy with Dronpa mutants J. Am. Chem. Soc. 129 2007 13970 13977
11. E. Galperin , V.V. Verkhusha , and A. Sorkin Three-chromophore FRET microscopy to analyze multiprotein interactions in living cells Nat. Methods 1 2004 209 217
12. C. Geisler , A. Schonle , C.V. Middendorff , H. Bock , C. Eggeling , A. Egner , and S.W. Hell Resolution of 1/10 in fluorescence microscopy using fast single molecule photo-switching Appl. Phys. A. 88 2007 223 226
13. L. Giordano , T.M. Jovin , M. Irie , and E.A. Jares-Erijman Diheteroarylethenes as thermally stable photoswitchable acceptors in photochromic fluorescence resonance energy transfer (pcFRET) J. Am. Chem. Soc. 124 2002 7481 7489
14. J. Goedhart , J.E. Vermeer , M.J. Adjobo-Hermans , L. van Weeren , and T.W. Gadella Jr. Sensitive detection of p65 homodimers using red-shifted and fluorescent protein-based FRET couples PLoS ONE 2 2007 e1011
15. S.W. Hell Microscopy and its focal switch Nat. Methods 6 2009 24 32
16. S.W. Hell , and J. Wichmann Breaking the diffraction resolution limit by stimulated emission: stimulated-emission-depletion fluorescence microscopy Opt. Lett. 19 1994 780 782
17. J.N. Henderson , H.W. Ai , R.E. Campbell , and S.J. Remington Structural basis for reversible photobleaching of a green fluorescent protein homologue Proc. Natl. Acad. Sci. USA 104 2007 6672 6677
18. R.S. Herbst Review of epidermal growth factor receptor biology Int. J. Radiat. Oncol. Biol. Phys. 59 2004 21 26
19. S.N. Ho , H.D. Hunt , R.M. Horton , J.K. Pullen , and L.R. Pease Site-directed mutagenesis by overlap extension using the polymerase chain reaction Gene 77 1989 51 59
20. A. Hoffmann , G. Natoli , and G. Ghosh Transcriptional regulation via the NF-kappaB signaling module Oncogene 25 2006 6706 6716
21. M. Hofmann , C. Eggeling , S. Jakobs , and S.W. Hell Breaking the diffraction barrier in fluorescence microscopy at low light intensities by using reversibly photoswitchable proteins Proc. Natl. Acad. Sci. USA 102 2005 17565 17569
22. E.A. Jares-Erijman , and T.M. Jovin Imaging molecular interactions in living cells by FRET microscopy Curr. Opin. Chem. Biol. 10 2006 409 416
23. G.J. Kremers , K.L. Hazelwood , C.S. Murphy , M.W. Davidson , and D.W. Piston Photoconversion in orange and red fluorescent proteins Nat. Methods 6 2009 355 358
24. K.A. Lukyanov , D.M. Chudakov , S. Lukyanov , and V.V. Verkhusha Innovation: Photoactivatable fluorescent proteins Nat. Rev. Mol. Cell Biol. 6 2005 885 891
25. K.A. Lukyanov , A.F. Fradkov , N.G. Gurskaya , M.V. Matz , Y.A. Labas , A.P. Savitsky , M.L. Markelov , A.G. Zaraisky , X. Zhao , and Y. Fang Natural animal coloration can Be determined by a nonfluorescent green fluorescent protein homolog J. Biol. Chem. 275 2000 25879 25882
26. S. Mao , R.K. Benninger , Y. Yan , C. Petchprayoon , D. Jackson , C.J. Easley , D.W. Piston , and G. Marriott Optical lock-in detection of FRET using synthetic and genetically encoded optical switches Biophys. J. 94 2008 4515 4524
27. E.M. Merzlyak , J. Goedhart , D. Shcherbo , M.E. Bulina , A.S. Shcheglov , A.F. Fradkov , A. Gaintzeva , K.A. Lukyanov , S. Lukyanov , T.W. Gadella , and D.M. Chudakov Bright monomeric red fluorescent protein with an extended fluorescence lifetime Nat. Methods 4 2007 555 557
28. H. Mizuno , T.K. Mal , M. Walchli , A. Kikuchi , T. Fukano , R. Ando , J. Jeyakanthan , J. Taka , Y. Shiro , M. Ikura , and A. Miyawaki Light-dependent regulation of structural flexibility in a photochromic fluorescent protein Proc. Natl. Acad. Sci. USA 105 2008 9227 9232
29. G.U. Nienhaus , and J. Wiedenmann Structure, dynamics and optical properties of fluorescent proteins: perspectives for marker development ChemPhysChem 10 2009 1369 1379
30. C.N. Pace , F. Vajdos , L. Fee , G. Grimsley , and T. Gray How to measure and predict the molar absorption coefficient of a protein Protein Sci. 4 1995 2411 2423
31. D.W. Piston , and G.J. Kremers Fluorescent protein FRET: the good, the bad and the ugly Trends Biochem. Sci. 32 2007 407 414
32. S. Pletnev , D. Shcherbo , D.M. Chudakov , N. Pletneva , E.M. Merzlyak , A. Wlodawer , Z. Dauter , and V. Pletnev A crystallographic study of bright far-red fluorescent protein mKate reveals pH-induced cis-trans isomerization of the chromophore J. Biol. Chem. 283 2008 28980 28987
33. M.L. Quillin , D.M. Anstrom , X. Shu , S. O'Leary , K. Kallio , D.M. Chudakov , and S.J. Remington Kindling fluorescent protein from Anemonia sulcata: dark-state structure at 1.38 A resolution Biochemistry 44 2005 5774 5787
34. M.A. Rizzo , G. Springer , K. Segawa , W.R. Zipfel , and D.W. Piston Optimization of pairings and detection conditions for measurement of FRET between cyan and yellow fluorescent proteins Microsc. Microanal. 12 2006 238 254
35. J.A. Schmid , A. Birbach , R. Hofer-Warbinek , M. Pengg , U. Burner , P.G. Furtmüller , B.R. Binder , and R. de Martin Dynamics of NFkappaB and IkappaBalpha studied with green fluorescent protein (GFP) fusion proteins. Investigation of GFP-p65 binding to DNA by fluorescence resonance energy transfer J. Biol. Chem. 275 2000 17035 17042
36. N.C. Shaner , R.E. Campbell , P.A. Steinbach , B.N. Giepmans , A.E. Palmer , and R.Y. Tsien Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein Nat. Biotechnol. 22 2004 1567 1572
37. N.C. Shaner , M.Z. Lin , M.R. McKeown , P.A. Steinbach , K.L. Hazelwood , M.W. Davidson , and R.Y. Tsien Improving the photostability of bright monomeric orange and red fluorescent proteins Nat. Methods 5 2008 545 551
38. D. Sinnecker , P. Voigt , N. Hellwig , and M. Schaefer Reversible photobleaching of enhanced green fluorescent proteins Biochemistry 44 2005 7085 7094
39. A. Sorkin , M. McClure , F. Huang , and R. Carter Interaction of EGF receptor and grb2 in living cells visualized by fluorescence resonance energy transfer (FRET) microscopy Curr. Biol. 10 2000 1395 1398
40. A. Sorkin , and M. von Zastrow Endocytosis and signalling: intertwining molecular networks Nat. Rev. Mol. Cell Biol. 10 2009 609 622
41. A.C. Stiel , M. Andresen , H. Bock , M. Hilbert , J. Schilde , A. Schonle , C. Eggeling , A. Egner , S.W. Hell , and S. Jakobs Generation of monomeric reversibly switchable red fluorescent proteins for far-field fluorescence nanoscopy Biophys. J. 95 2008 2989 2997
42. A.C. Stiel , S. Trowitzsch , G. Weber , M. Andresen , C. Eggeling , S.W. Hell , S. Jakobs , and M.C. Wahl 1.8 A bright-state structure of the reversibly switchable fluorescent protein Dronpa guides the generation of fast switching variants Biochem. J. 402 2007 35 42
43. F.V. Subach , G.H. Patterson , S. Manley , J.M. Gillette , J. Lippincott-Schwartz , and V.V. Verkhusha Photoactivatable mCherry for high-resolution two-color fluorescence microscopy Nat. Methods 6 2009 153 159
44. G.N. van der Krogt , J. Ogink , B. Ponsioen , and K. Jalink A comparison of donor-acceptor pairs for genetically encoded FRET sensors: application to the Epac cAMP sensor as an example PLoS One 3 2008 e1916
45. E.B. Van Munster , and T.W. Gadella Jr. phiFLIM: a new method to avoid aliasing in frequency-domain fluorescence lifetime imaging microscopy J. Microsc. 213 2004 29 38
46. E.B. van Munster , and T.W. Gadella Jr. Suppression of photobleaching-induced artifacts in frequency-domain FLIM by permutation of the recording order Cytometry A 58 2004 185 194
47. H. Wallrabe , and A. Periasamy Imaging protein molecules using FRET and FLIM microscopy Curr. Opin. Biotechnol. 16 2005 19 27
48. T. Yamazaki , K. Zaal , D. Hailey , J. Presley , J. Lippincott-Schwartz , and L.E. Samelson Role of Grb2 in EGF-stimulated EGFR internalization J. Cell Sci. 115 2002 1791 1802
49. I.V. Yampolsky , A.A. Kislukhin , T.T. Amatov , D. Shcherbo , V.K. Potapov , S. Lukyanov , and K.A. Lukyanov Synthesis and properties of the red chromophore of the green-to-red photoconvertible fluorescent protein Kaede and its analogs Bioorg. Chem. 36 2008 96 104
50. L. Zhang , N.G. Gurskaya , E.M. Merzlyak , D.B. Staroverov , N.N. Mudrik , O.N. Samarkina , L.M. Vinokurov , S. Lukyanov , and K.A. Lukyanov Method for real-time monitoring of protein degradation at the single cell level Biotechniques 42 2007 446, 448, 450