Photocontrollable fluorescent proteins for superresolution imaging

Annual Review of Biophysics

Volumn 43, Issue 1, 2014, Pages 303-329

  Shcherbakova, Daria M ^a,b   Sengupta, Prabuddha ^c   Lippincott Schwartz, Jennifer ^c   Verkhusha, Vladislav V ^a,b  

^a Department of Anatomy and Structural Biology ^*  (United States)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^c EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

Author keywords

EosFP; PAGFP; PALM; PAmCherry; RESOLFT

Indexed keywords

CYAN FLUORESCENT PROTEIN; FLUORESCENT DYE; GREEN FLUORESCENT PROTEIN; PAXILLIN; PEPTIDES AND PROTEINS; PHOTOCONTROLLABLE FLUORESCENT PROTEIN; PHOTOSWITCHABLE FLUORESCENT PROTEIN; TRANSFERRIN RECEPTOR; UNCLASSIFIED DRUG;

ACTIN FILAMENT; ARTICLE; BLEACHING; CELL MEMBRANE; CELL STRUCTURE; CELL VIABILITY; CONFOCAL MICROSCOPY; FLUORESCENCE IMAGING; FLUORESCENCE MICROSCOPY; FOCAL ADHESION; ILLUMINATION; IMAGE RECONSTRUCTION; MAMMAL CELL; MOLECULAR IMAGING; NONHUMAN; PHOTOACTIVATION; PHOTON; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN CONTENT; PROTEIN LIPID INTERACTION; REVERSIBLE SATURATABLE OPTICAL FLUORESCENCE TRANSITION IMAGING; SUPERRESOLUTION IMAGING;

EOSFP; PAGFP; PALM; PAMCHERRY; RESOLFT;

ANIMALS; CELLS; LUMINESCENT PROTEINS; MAMMALS; MICROSCOPY, FLUORESCENCE;

EID: 84902008399     PISSN: 1936122X     EISSN: 19361238     Source Type: Book Series    
DOI: 10.1146/annurev-biophys-051013-022836     Document Type: Article

References (88)

1. Adam V, Lelimousin M, Boehme S, Desfonds G, Nienhaus K, et al. 2008. Structural characterization of IrisFP, an optical highlighter undergoing multiple photo-induced transformations. Proc. Natl. Acad. Sci. USA 105:18343-488
2. Adam V, Moeyaert B, David CC, Mizuno H, Lelimousin M, et al. 2011. Rational design of photoconvertible and biphotochromic fluorescent proteins for advanced microscopy applications. Chem. Biol. 18:1241-511
3. Ando R, Mizuno H, Miyawaki A. 2004. Regulated fast nucleocytoplasmic shuttling observed by reversible protein highlighting. Science 306:1370-733
4. Andresen M, Stiel AC, Folling J, Wenzel D, Schonle A, et al. 2008. Photoswitchable fluorescent proteins enable monochromatic multilabel imaging and dual color fluorescence nanoscopy. Nat. Biotechnol. 26:1035-400
5. Annibale P, Vanni S, Scarselli M, Rothlisberger U, Radenovic A. 2011. Quantitative photo activated localization microscopy: unraveling the effects of photoblinking. PLoS ONE 6:e226788
6. Betzig E, Patterson GH, Sougrat R, Lindwasser OW, Olenych S, et al. 2006. Imaging intracellular fluorescent proteins at nanometer resolution. Science 313:1642-455
7. Brakemann T, Stiel AC,Weber G, AndresenM, Testa I, et al. 2011. A reversibly photoswitchable GFP-like protein with fluorescence excitation decoupled from switching. Nat. Biotechnol. 29:942-477
8. Bulina ME, Verkhusha VV, Staroverov DB, Chudakov DM, Lukyanov KA. 2003. Heterooligomeric tagging diminishes non-specific aggregation of target proteins fused with Anthozoa fluorescent proteins. Biochem. J. 371:109-1144
9. ChangH, Zhang M, Ji W, Chen J, Zhang Y, et al. 2012. A unique series of reversibly switchable fluorescent proteins with beneficial properties for various applications. Proc. Natl. Acad. Sci. USA 109:4455-600
10. Chmyrov A, Keller J, Grotjohann T, Ratz M, d'Este E, et al. 2013. Nanoscopy with more than 100,000 'doughnuts.' Nat. Methods 10:737-400
11. Chudakov DM, Verkhusha VV, Staroverov DB, Souslova EA, Lukyanov S, Lukyanov KA. 2004. Photoswitchable cyan fluorescent protein for protein tracking. Nat. Biotechnol. 22:1435-399
12. Chudakov DM, Matz MV, Lukyanov S, Lukyanov KA. 2010. Fluorescent proteins and their applications in imaging living cells and tissues. Physiol. Rev. 90:1103-633
13. Chudakov DM, Lukyanov S, Lukyanov KA. 2007. Tracking intracellular protein movements using photoswitchable fluorescent proteins PS-CFP2 and Dendra2. Nat. Protoc. 2:2024-322
14. Cox S, Rosten E, Monypenny J, Jovanovic-Talisman T, Burnette DT, et al. 2012. Bayesian localization microscopy reveals nanoscale podosome dynamics. Nat. Methods 9:195-2000
15. Dedecker P, Hotta J, Flors C, Sliwa M, Uji-i H, et al. 2007. 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. 129:16132-411
16. Dedecker P, Mo GC, Dertinger T, Zhang J. 2012. Widely accessible method for superresolution fluorescence imaging of living systems. Proc. Natl. Acad. Sci. USA 109:10909-144
17. Dickson RM, Cubitt AB, Tsien RY, Moerner WE. 1997. On/off blinking and switching behaviour of single molecules of green fluorescent protein. Nature 388:355-588
18. Egner A, Geisler C, von Middendorff C, Bock H, Wenzel D, et al. 2007. Fluorescence nanoscopy in whole cells by asynchronous localization of photoswitching emitters. Biophys. J. 93:3285-900
19. Flors C, Hotta J, Uji-i H, Dedecker P, Ando R, et al. 2007. A stroboscopic approach for fast photoactivation-localization microscopy with Dronpa mutants. J. Am. Chem. Soc. 129:13970-711
20. Folling J, Bossi M, Bock H, Medda R, Wurm CA, et al. 2008. Fluorescence nanoscopy by ground-state depletion and single-molecule return. Nat. Methods 5:943-455
21. Fuchs J, Bohme S, Oswald F, Hedde PN, KrauseM, et al. 2010. A photoactivatable marker protein for pulse-chase imaging with superresolution. Nat. Methods 7:627-300
22. Gould TJ, Gunewardene MS, Gudheti MV, Verkhusha VV, Yin SR, et al. 2008. Nanoscale imaging of molecular positions and anisotropies. Nat. Methods 5:1027-300
23. GouldTJ, Verkhusha VV, Hess ST. 2009. Imaging biological structures with fluorescence photoactivation localization microscopy. Nat. Protoc. 4:291-3088
24. Greenfield D, McEvoy AL, Shroff H, Crooks GE, Wingreen NS, et al. 2009. Self-organization of the Escherichia coli chemotaxis network imaged with super-resolution light microscopy. PLoS Biol. 7:e10001377
25. Grotjohann T, Testa I, Leutenegger M, Bock H, Urban NT, et al. 2011. Diffraction-unlimited all-optical imaging and writing with a photochromic GFP. Nature 478:204-88
26. Grotjohann T, Testa I, Reuss M, BrakemannT, EggelingC, et al. 2012. rsEGFP2 enables fast RESOLFT nanoscopy of living cells. eLIFE 1:e002488
27. Gunewardene MS, Subach FV, Gould TJ, Penoncello GP, Gudheti MV, et al. 2011. Superresolution imaging of multiple fluorescent proteins with highly overlapping emission spectra in living cells. Biophys. J. 101:1522-288
28. Gurskaya NG, Verkhusha VV, Shcheglov AS, Staroverov DB, Chepurnykh TV, et al. 2006. Engineering of a monomeric green-to-red photoactivatable fluorescent protein induced by blue light. Nat. Biotechnol. 24:461-655
29. Gustafsson MG. 2005. Nonlinear structured-illumination microscopy: wide-field fluorescence imaging with theoretically unlimited resolution. Proc. Natl. Acad. Sci. USA 102:13081-866
30. Habuchi S, Ando R, Dedecker P, VerheijenW, Mizuno H, et al. 2005. Reversible single-molecule photoswitching in the GFP-like fluorescent protein Dronpa. Proc. Natl. Acad. Sci. USA 102:9511-166
31. Habuchi S, Tsutsui H, Kochaniak AB,Miyawaki A, van Oijen AM. 2008. mKikGR, a monomeric photoswitchable fluorescent protein. PLoS ONE 3:e39444
32. Hell SW. 2003. Toward fluorescence nanoscopy. Nat. Biotechnol. 21:1347-555
33. Hell SW. 2007. Far-field optical nanoscopy. Science 316:1153-588
34. Hell SW. 2009. Microscopy and its focal switch. Nat. Methods 6:24-322
35. Hell SW,Wichmann J. 1994. Breaking the diffraction resolution limit by stimulated emission: stimulatedemission-depletion fluorescence microscopy. Opt. Lett. 19:780-822
36. Hess ST,Girirajan TP, MasonMD. 2006. Ultra-high resolution imaging by fluorescence photoactivation localization microscopy. Biophys. J. 91:4258-722
37. Hess ST, Gould TJ, Gudheti MV, Maas SA, Mills KD, Zimmerberg J. 2007. Dynamic clustered distribution of hemagglutinin resolved at 40 nm in living cell membranes discriminates between raft theories. Proc. Natl. Acad. Sci. USA 104:17370-755
38. Hofmann M, Eggeling C, Jakobs S, Hell SW. 2005. Breaking the diffraction barrier in fluorescence microscopy at low light intensities by using reversibly photoswitchable proteins. Proc. Natl. Acad. Sci. USA 102:17565-699
39. Hoi H, Shaner NC, Davidson MW, Cairo CW, Wang J, Campbell RE. 2010. A monomeric photoconvertible fluorescent protein for imaging of dynamic protein localization. J. Mol. Biol. 401:776-911
40. Holden SJ,Uphoff S,Kapanidis AN. 2011. DAOSTORM: an algorithm for high-density super-resolution microscopy. Nat. Methods 8:279-800
41. Hoze N, Nair D, Hosy E, Sieben C, Manley S, et al. 2012. Heterogeneity of AMPA receptor trafficking and molecular interactions revealed by superresolution analysis of live cell imaging. Proc. Natl. Acad. Sci. USA 109:17052-577
42. Huang B,WangW, Bates M, Zhuang X. 2008 Three-dimensional super-resolution imaging by stochastic optical reconstruction microscopy. Science 319:810-133
43. Huang B, Babcock H, Zhuang X. 2010. Breaking the diffraction barrier: super-resolution imaging of cells. Cell 143:1047-588
44. Huang F, Hartwich TM, Rivera-Molina FE, Lin Y, DuimWC, et al. 2013. Video-rate nanoscopy using sCMOS camera-specific single-molecule localization algorithms. Nat. Methods 10:653-588
45. Huang F, Schwartz SL, Byars JM, Lidke KA. 2011. Simultaneous multiple-emitter fitting for single molecule super-resolution imaging. Biomed. Opt. Express 2:1377-933
46. JooC, Balci H, Ishitsuka Y, Buranachai C, Ha T. 2008. Advances in single-molecule fluorescencemethods for molecular biology. Annu. Rev. Biochem. 77:51-766
47. Juette MF, Gould TJ, Lessard MD, Mlodzianoski MJ, Nagpure BS, et al. 2008. Three-dimensional sub-100 nm resolution fluorescence microscopy of thick samples. Nat. Methods 5:527-299
48. Kanchanawong P, Shtengel G, Pasapera AM, Ramko EB, Davidson MW, et al. 2010. Nanoscale architecture of integrin-based cell adhesions. Nature 468:580-844
49. Kopek BG, ShtengelG,XuCS, Clayton DA, Hess HF. 2012. Correlative 3Dsuperresolution fluorescence and electronmicroscopy reveal the relationship ofmitochondrial nucleoids to membranes. Proc.Natl. Acad. Sci. USA 109:6136-411
50. Lee SH, Shin JY, Lee A, Bustamante C. 2012. Counting single photoactivatable fluorescent molecules by photoactivated localization microscopy (PALM). Proc. Natl. Acad. Sci. USA 109:17436-411
51. Manley S, Gillette JM, Patterson GH, Shroff H, Hess HF, et al. 2008. High-density mapping of singlemolecule trajectories with photoactivated localization microscopy. Nat. Methods 5:155-577
52. Manley S, Gunzenhauser J, Olivier N. 2011. A starter kit for point-localization super-resolution imaging. Curr. Opin. Chem. Biol. 15:813-211
53. McEvoy AL,Hoi H, BatesM, PlatonovaE,Cranfill PJ, et al. 2012. mMaple: a photoconvertible fluorescent protein for use in multiple imaging modalities. PLoS ONE 7:e513144
54. McKinney SA, Murphy CS, Hazelwood KL, DavidsonMW, Looger LL. 2009. A bright and photostable photoconvertible fluorescent protein. Nat. Methods 6:131-333
55. Mizuno H, Dedecker P, Ando R, Fukano T, Hofkens J,MiyawakiA. 2010. Higher resolution in localization microscopy by slower switching of a photochromic protein. Photochem. Photobiol. Sci. 9:239-488
56. Nieuwenhuizen RP, Lidke KA, BatesM, Puig DL, Grunwald D, et al. 2013. Measuring image resolution in optical nanoscopy. Nat. Methods 10:557-622
57. Patterson G, Davidson M, Manley S, Lippincott-Schwartz J. 2010. Superresolution imaging using singlemolecule localization. Annu. Rev. Phys. Chem. 61:345-677
58. Patterson GH, Lippincott-Schwartz J. 2002. A photoactivatable GFP for selective photolabeling of proteins and cells. Science 297:1873-777
59. Post JN, Lidke KA, Rieger B, Arndt-Jovin DJ. 2005. One-and two-photon photoactivation of a paGFPfusion protein in live Drosophila embryos. FEBS Lett. 579:325-300
60. Rego EH, Shao L, Macklin JJ, Winoto L, Johansson GA, et al. 2012. Nonlinear structured-illumination microscopy with a photoswitchable protein reveals cellular structures at 50-nm resolution. Proc. Natl. Acad. Sci. USA 109:E135-433
61. Renz M, Daniels BR, Vamosi G, Arias IM, Lippincott-Schwartz J. 2012. Plasticity of the asialoglycoprotein receptor deciphered by ensemble FRET imaging and single-molecule counting PALM imaging. Proc. Natl. Acad. Sci. USA 109:E2989-977
62. Rossi A, Moritz TJ, Ratelade J, Verkman AS. 2012. Super-resolution imaging of aquaporin-4 orthogonal arrays of particles in cell membranes. J. Cell Sci. 125:4405-122
63. Rust MJ, Bates M, Zhuang X. 2006. Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM). Nat. Methods 3:793-955
64. Sengupta P, Jovanovic-Talisman T, Skoko D, Renz M, Veatch SL, Lippincott-Schwartz J. 2011. Probing protein heterogeneity in the plasma membrane using PALM and pair correlation analysis. Nat. Methods 8:969-755
65. Sengupta P, Lippincott-Schwartz J. 2012. Quantitative analysis of photoactivated localizationmicroscopy (PALM) datasets using pair-correlation analysis. BioEssays 34:396-4055
66. Sengupta P, Van Engelenburg S, Lippincott-Schwartz J. 2012. Visualizing cell structure and function with point-localization superresolution imaging. Dev. Cell 23:1092-1022
67. Shannon CE. 1949. Communication in the presence of noise. Proc. IRE 37:10-211
68. Sherman E, Barr V, Manley S, Patterson G, Balagopalan L, et al. 2011. Functional nanoscale organization of signaling molecules downstream of the T cell antigen receptor. Immunity 35:705-200
69. Shroff H, Galbraith CG, Galbraith JA, Betzig E. 2008. Live-cell photoactivated localization microscopy of nanoscale adhesion dynamics. Nat. Methods 5:417-233
70. Shroff H, Galbraith CG, Galbraith JA, White H, Gillette J, et al. 2007. Dual-color superresolution imaging of genetically expressed probes within individual adhesion complexes. Proc. Natl. Acad. Sci. USA 104:20308-133
71. Shtengel G, Galbraith JA, Galbraith CG, Lippincott-Schwartz J, Gillette JM, et al. 2009. Interferometric fluorescent super-resolution microscopy resolves 3D cellular ultrastructure. Proc. Natl. Acad. Sci. USA 106:3125-300
72. Smith CS, Joseph N, Rieger B, Lidke KA. 2010. Fast, single-molecule localization that achieves theoretically minimum uncertainty. Nat. Methods 7:373-755
73. Stiel AC, Andresen M, Bock H, Hilbert M, Schilde J, et al. 2008. Generation of monomeric reversibly switchable red fluorescent proteins for far-field fluorescence nanoscopy. Biophys. J. 95:2989-977
74. Stiel AC, Trowitzsch S, WeberG, AndresenM, Eggeling C, et al. 2007. 1.8 A bright-state structure of the reversibly switchable fluorescent proteinDronpa guides the generation of fast switching variants. Biochem. J. 402:35-422
75. Subach FV, Patterson GH, Manley S, Gillette JM, Lippincott-Schwartz J, Verkhusha VV. 2009. Photoactivatable mCherry for high-resolution two-color fluorescence microscopy. Nat. Methods 6:153-599
76. Subach FV, Patterson GH, Renz M, Lippincott-Schwartz J, Verkhusha VV. 2010. Bright monomeric photoactivatable red fluorescent protein for two-color super-resolution sptPALM of live cells. J. Am. Chem. Soc. 132:6481-911
77. Subach FV, Piatkevich KD, Verkhusha VV. 2011. Directed molecular evolution to design advanced red fluorescent proteins. Nat. Methods 8:1019-266
78. Subach FV, Zhang L, Gadella TW, Gurskaya NG, Lukyanov KA, Verkhusha VV. 2010. Red fluorescent protein with reversibly photoswitchable absorbance for photochromic FRET. Chem. Biol. 17:745-555
79. Subach OM, Entenberg D, Condeelis JS, Verkhusha VV. 2012. A FRET-facilitated photoswitching using an orange fluorescent protein with the fast photoconversion kinetics. J. Am. Chem. Soc. 134:14789-999
80. Subach OM, Patterson GH, Ting LM, Wang Y, Condeelis JS, Verkhusha VV. 2011. A photoswitchable orange-to-far-red fluorescent protein, PSmOrange. Nat. Methods 8:771-777
81. Testa I, Urban NT, Jakobs S, Eggeling C, Willig KI, Hell SW. 2012. Nanoscopy of living brain slices with low light levels. Neuron 75:992-10000
82. Thompson RE, Larson DR, Webb WW. 2002. Precise nanometer localization analysis for individual fluorescent probes. Biophys. J. 82:2775-833
83. Verkhusha VV, Sorkin A. 2005. Conversion of the monomeric red fluorescent protein into a photoactivatable probe. Chem. Biol. 12:279-855
84. Wiedenmann J, Ivanchenko S, Oswald F, Schmitt F, Rocker C, et al. 2004. EosFP, a fluorescent marker protein withUV-inducible green-to-red fluorescence conversion. Proc.Natl. Acad. Sci. USA 101:15905-100
85. Williamson DJ, Owen DM, Rossy J, Magenau A,Wehrmann M, et al. 2011. Pre-existing clusters of the adaptor Lat do not participate in early T cell signaling events. Nat. Immunol. 12:655-622
86. York AG, Ghitani A, Vaziri A, Davidson MW, Shroff H. 2011. Confined activation and subdiffractive localization enables whole-cell PALM with genetically expressed probes. Nat. Methods 8:327-333
87. Zhang M, Chang H, Zhang Y, Yu J, Wu L, et al. 2012. Rational design of true monomeric and bright photoactivatable fluorescent proteins. Nat. Methods 9:727-299
88. Zhu L, Zhang W, Elnatan D, Huang B. 2012. Faster STORM using compressed sensing. Nat. Methods 9:721-233