Where Do We Stand with Super-Resolution Optical Microscopy?

Journal of Molecular Biology

Volumn 428, Issue 2, 2016, Pages 308-322

  Nienhaus, Karin ^a   Nienhaus, G Ulrich ^a,b,c  

^a KARLSRUHE INSTITUTE OF TECHNOLOGY   (Germany)

^b KARLSRUHE INSTITUTE OF TECHNOLOGY   (Germany)

^c University of Illinois at Urbana Champaign   (United States)

Author keywords

fluorescence correlation spectroscopy; localization microscopy; raster image correlation spectroscopy; stimulated emission depletion microscopy; super resolution fluorescence microscopy

Indexed keywords

FLUORESCENT DYE; PAXILLIN; MACROMOLECULE;

ANALYTIC METHOD; BIOPHYSICS; CONFOCAL MICROSCOPY; CRISPR CAS SYSTEM; FLUORESCENCE FLUCTUATION SPECTROSCOPY; FLUORESCENCE IMAGING; FLUORESCENCE MICROSCOPY; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; NONHUMAN; PHOTORECEPTOR; PHOTOTOXICITY; PRIORITY JOURNAL; PROTEIN ASSEMBLY; REVIEW; SUPER RESOLUTION OPTICAL FLUORESCENCE MICROSCOPY; ANALYSIS; MACROMOLECULE; PROCEDURES;

MACROMOLECULAR SUBSTANCES; MICROSCOPY, FLUORESCENCE; OPTICAL IMAGING;

EID: 85047290103     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2015.12.020     Document Type: Review

References (98)

1. Fluorescence Fluctuation Spectroscopy (FFS), Parts A and B S.Y. Tetin Methods in Enzymology 518 and 519 2013 Elsevier
2. S. Diekmann, and C. Hoischen Biomolecular dynamics and binding studies in the living cell Phys. Life Rev. 11 2014 1 30
3. K. Nienhaus, and G.U. Nienhaus Fluorescence Labeling U. Kubitscheck, Fluorescence Microscopy: From Principles to Biological Applications 2013 Wiley-Blackwell 143 174
4. D. Jung, K. Min, J. Jung, W. Jang, and Y. Kwon Chemical biology-based approaches on fluorescent labeling of proteins in live cells Mol. BioSyst. 9 2013 862 872
5. K.M. Dean, and A.E. Palmer Advances in fluorescence labeling strategies for dynamic cellular imaging Nat. Chem. Biol. 10 2014 512 523
6. E. Abbe Beiträge zur theorie des mikroskops und der mikroskopischen wahrnehmung Arch. Mikrosk. Anat. 9 1873 413 468
7. Far-Field Optical Nanoscopy Springer Series on Fluorescence 14 2015 Springer Berlin Heidelberg
8. W.E. Moerner Single-molecule spectroscopy, imaging, and photocontrol: Foundations for super-resolution microscopy (Nobel Lecture) Angew. Chem. Int. Ed. Engl. 54 2015 8067 8093
9. E. Betzig Single molecules, cells, and super-resolution optics (Nobel Lecture) Angew. Chem. Int. Ed. Engl. 54 2015 8034 8053
10. S.W. Hell Nanoscopy with focused light (Nobel Lecture) Angew. Chem. Int. Ed. Engl. 54 2015 8054 8066
11. G.U. Nienhaus The green fluorescent protein: A key tool to study chemical processes in living cells Angew. Chem. Int. Ed. 47 2008 8992 8994
12. D.R. Whelan, and T.D.M. Bell Super-resolution single-molecule localization microscopy: Tricks of the trade J. Phys. Chem. Lett. 6 2015 374 382
13. M. Lakadamyali Super-resolution microscopy: Going live and going fast ChemPhysChem 15 2014 630 636
14. S.W. Hell, and E.H.K. Stelzer Fundamental improvement of resolution with a 4Pi-confocal microscope using two-photon excitation Opt. Commun. 93 1992 277 282
15. M.G. Gustafsson Extended resolution fluorescence microscopy Curr. Opin. Chem. Biol. 9 1999 627 634
16. M.G. Gustafsson Surpassing the lateral resolution limit by a factor of two using structured illumination microscopy J. Microsc. 198 2000 82 87
17. C. Eggeling, K.I. Willig, S.J. Sahl, and S.W. Hell Lens-based fluorescence nanoscopy Q. Rev. Biophys. 48 2015 178 243
18. 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
19. S.W. Hell Far-field optical nanoscopy Science 316 2007 1153 1158
20. A. Hense, B. Prunsche, P. Gao, Y. Ishitsuka, K. Nienhaus, and G.U. Nienhaus Monomeric Garnet, a far-red fluorescent protein for live-cell STED imaging Sci. Rep. 5 2015 18006
21. D. Wildanger, R. Medda, L. Kastrup, and S.W. Hell A compact STED microscope providing 3D nanoscale resolution J. Microsc. 236 2009 35 43
22. T.J. Gould, D. Burke, J. Bewersdorf, and J.M. Booth Adaptive optics enables 3D STED microscopy in aberrating specimens Opt. Express 20 2012 20998 21009
23. G. Vicidomini, G. Moneron, K.Y. Han, V. Westphal, H. Ta, M. Reuss, J. Engelhardt, C. Eggeling, and S.W. Hell Sharper low-power STED nanoscopy by time gating Nat. Methods 8 2011 571 573
24. M. Bossi, J. Fölling, M. Dyba, V. Westphal, and S.W. Hell Breaking the diffraction resolution barrier in far-field microscopy by molecular optical bistability New J. Phys. 8 2006 275
25. 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. U. S. A. 102 2005 17565 17569
26. K. Nienhaus, and G.U. Nienhaus Fluorescent proteins for live-cell imaging with super-resolution Chem. Soc. Rev. 43 2014 1088 1106
27. R. Bizzarri, M. Serresi, F. Cardarelli, S. Abbruzzetti, B. Campanini, C. Viappiani, and F. Beltram Single amino acid replacement makes Aequorea victoria fluorescent proteins reversibly photoswitchable J. Am. Chem. Soc. 132 2010 85 95
28. S. Gayda, K. Nienhaus, and G.U. Nienhaus Mechanistic insights into reversible photoactivation in proteins of the GFP family Biophys. J. 103 2012 2521 2531
29. M.G. Gustafsson Nonlinear structured-illumination microscopy: Wide-field fluorescence imaging with theoretically unlimited resolution Proc. Natl. Acad. Sci. U. S. A. 102 2005 13081 13086
30. E. Betzig, G.H. Patterson, R. Sougrat, O.W. Lindwasser, S. Olenych, J.S. Bonifacino, M.W. Davidson, J. Lippincott-Schwartz, and H.F. Hess Imaging intracellular fluorescent proteins at nanometer resolution Science 313 2006 1642 1645
31. S.T. Hess, T.P. Girirajan, and M.D. Mason Ultra-high resolution imaging by fluorescence photoactivation localization microscopy Biophys. J. 91 2006 4258 4272
32. M.J. Rust, M. Bates, and X. Zhuang Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM) Nat. Methods 3 2006 793 795
33. P. Sengupta, S.B. van Engelenburg, and J. Lippincott-Schwartz Superresolution imaging of biological systems using photoactivated localization microscopy Chem. Rev. 114 2014 3189 3202
34. P.N. Hedde, and G.U. Nienhaus Super-resolution localization microscopy with photoactivatable fluorescent marker proteins Protoplasma 251 2014 349 362
35. J. Fuchs, S. Böhme, F. Oswald, P.N. Hedde, M. Krause, J. Wiedenmann, and G.U. Nienhaus A photoactivatable marker protein for pulse-chase imaging with superresolution Nat. Methods 7 2010 627 630
36. H. Shroff, C.G. Galbraith, J.A. Galbraith, H. White, J. Gillette, S. Olenych, M.W. Davidson, and E. Betzig Dual-color superresolution imaging of genetically expressed probes within individual adhesion complexes Proc. Natl. Acad. Sci. U. S. A. 104 2007 20308 20313
37. R.P.J. Nieuwenhuizen, K.A. Lidke, M. Bates, D.L. Puig, D. Grunwald, S. Stallinga, and B. Rieger Measuring image resolution in optical nanoscopy Nat. Methods 10 2013 557 562
38. A. Small, and S. Stahlheber Fluorophore localization algorithms for super-resolution microscopy Nat. Methods 11 2014 267 279
39. A.G. York, A. Ghitani, A. Vaziri, M.W. Davidson, and H. Shroff Confined activation and subdiffractive localization enables whole-cell PALM with genetically expressed probes Nat. Methods 8 2011 327 333
40. B. Huang, W. Wang, M. Bates, and X. Zhuang Three-dimensional super-resolution imaging by stochastic optical reconstruction microscopy Science 319 2008 810 813
41. M.F. Juette, T.J. Gould, M.D. Lessard, M.J. Mlodzianoski, B.S. Nagpure, B.T. Bennett, S.T. Hess, and J. Bewersdorf Three-dimensional sub-100 nm resolution fluorescence microscopy of thick samples Nat. Methods 5 2008 527 529
42. F.C. Zanacchi, Z. Lavagnino, M.P. Donnorso, A. Del Bue, L. Furia, M. Faretta, and A. Diaspro Live-cell 3D super-resolution imaging in thick biological samples Nat. Methods 8 2011 1047 1049
43. B.C. Chen, W.R. Legant, K. Wang, L. Shao, D.E. Milkie, M.W. Davidson, C. Janetopoulos, X.F.S. Wu, J.A. Hammer, Z. Liu, B.P. English, Y. Mimori-Kiyosue, D.P. Romero, A.T. Ritter, J. Lippincott-Schwartz, L. Fritz-Laylin, R.D. Mullins, D.M. Mitchell, J.N. Bembenek, A.C. Reymann, R. Böhme, S.W. Grill, J.T. Wang, G. Seydoux, U.S. Tulu, D.P. Kiehart, and E. Betzig Lattice light-sheet microscopy: Imaging molecules to embryos at high spatiotemporal resolution Science 346 2014 1257998
44. S. Manley, J.M. Gillette, G.H. Patterson, H. Shroff, H.F. Hess, E. Betzig, and J. Lippincott-Schwartz High-density mapping of single-molecule trajectories with photoactivated localization microscopy Nat. Methods 5 2008 155 157
45. D. Magde, W.W. Webb, and E. Elson Thermodynamic fluctuations in a reacting system - Measurement by fluorescence correlation spectroscopy Phys. Rev. Lett. 29 1972 705 708
46. M.A. Digman, C.M. Brown, P. Sengupta, P.W. Wiseman, A.R. Horwitz, and E. Gratton Measuring fast dynamics in solutions and cells with a laser scanning microscope Biophys. J. 89 2005 1317 1327
47. M.A. Digman, P.W. Wiseman, A.R. Horwitz, and E. Gratton Detecting protein complexes in living cells from laser scanning confocal image sequences by the cross correlation raster image spectroscopy method Biophys. J. 96 2009 707 716
48. J. Ries, S. Chiantia, and P. Schwille Accurate determination of membrane dynamics with line-scan FCS Biophys. J. 96 2009 1999 2008
49. P.N. Hedde, R.M. Dörlich, R. Blomley, D. Gradl, E. Oppong, A.C.B. Cato, and G.U. Nienhaus Stimulated emission depletion-based raster image correlation spectroscopy (STED-RICS) - A versatile method for studying biomolecular dynamics in live cells Nat. Commun. 4 2013 2093
50. L. Kastrup, H. Blom, C. Eggeling, and S.W. Hell Fluorescence fluctuation spectroscopy in subdiffraction focal volumes Phys. Rev. Lett. 94 2005 178104
51. A.P. Singh, and T. Wohland Applications of imaging fluorescence correlation spectroscopy Curr. Opin. Chem. Biol. 20 2014 29 35
52. L. Zemanova, A. Schenk, M.J. Valler, G.U. Nienhaus, and R. Heilker Confocal optics microscopy for biochemical and cellular high-throughput screening Drug Discov. Today 8 2003 1085 1093
53. M. Minsky Memoir on inventing the confocal scanning microscope Scanning 10 1988 128 138
54. J. Jonkman, C.M. Brown, and R.W. Cole Quantitative confocal microscopy: Beyond a pretty picture Methods Cell Biol. 123 2014 113 134
55. T. Tanaami, S. Otsuki, N. Tomosada, Y. Kosugi, M. Shimizu, and H. Ishida High-speed 1-frame/ms scanning confocal microscope with a microlens and Nipkow disks Appl. Opt. 41 2002 4704 4708
56. J. Oreopoulos, R. Berman, and M. Browne Spinning-disk confocal microscopy: Present technology and future trends Methods Cell Biol. 123 2014 153 175
57. J. Huisken, J. Swoger, F. Del Bene, J. Wittbrodt, and E.H. Stelzer Optical sectioning deep inside live embryos by selective plane illumination microscopy Science 305 2004 1007 1009
58. A.Y. Kobitski, J.C. Otte, M. Takamiya, B. Schäfer, J. Mertes, J. Stegmaier, S. Rastegar, F. Rindone, V. Hartmann, R. Stotzka, A. Garcia, J. van Wezel, R. Mikut, U. Strähle, and G.U. Nienhaus An ensemble-averaged, cell density-based digital model of zebrafish embryo development derived from light-sheet microscopy data with single-cell resolution Sci. Rep. 5 2015 8601
59. R. Heintzmann, and C. Cremer Axial tomographic confocal fluorescence microscopy J. Microsc. 206 2002 7 23
60. J. Ries, S.R. Yu, M. Burkhardt, M. Brand, and P. Schwille Modular scanning FCS quantifies receptor-ligand interactions in living multicellular organisms Nat. Methods 6 2009 643 645
61. R.M. Dörlich, Q. Chen, P.N. Hedde, V. Schuster, M. Hippler, J. Wesslowski, G. Davidson, and G.U. Nienhaus Dual-color dual-focus line-scanning FCS for quantitative analysis of receptor-ligand interactions in living specimens Sci. Rep. 5 2015 10149
62. C.M. Brown, R.B. Dalal, B. Hebert, M.A. Digman, A.R. Horwitz, and E. Gratton Raster image correlation spectroscopy (RICS) for measuring fast protein dynamics and concentrations with a commercial laser scanning confocal microscope J. Microsc. 229 2008 78 91
63. M.J. Rossow, J.M. Sasaki, M.A. Digman, and E. Gratton Raster image correlation spectroscopy in live cells Nat. Protoc. 5 2010 1761 1774
64. P.W. Wiseman Image correlation spectroscopy: Mapping correlations in space, time, and reciprocal space Methods Enzymol. 518 2013 245 267
65. P. Bianchini, C. Peres, M. Oneto, S. Galiani, G. Vicidomini, and A. Diaspro STED nanoscopy: A glimpse into the future Cell Tissue Res. 360 2015 143 150
66. N.C. Shaner Fluorescent proteins for quantitative microscopy: Important properties and practical evaluation Methods Cell Biol. 123 2014 95 111
67. L. Shang, S. Dong, and G.U. Nienhaus Ultra-small fluorescent metal nanoclusters: Synthesis and biological applications Nano Today 6 2011 401 418
68. T.L. Doane, and C. Burda The unique role of nanoparticles in nanomedicine: Imaging, drug delivery and therapy Chem. Soc. Rev. 41 2012 2885 2911
69. M. Baker Nanotechnology imaging probes: Smaller and more stable Nat. Methods 7 2010 957 962
70. B.N. Giepmans, S.R. Adams, M.H. Ellisman, and R.Y. Tsien The fluorescent toolbox for assessing protein location and function Science 312 2006 217 224
71. H.W. Ai, M.A. Baird, Y. Shen, M.W. Davidson, and R.E. Campbell Engineering and characterizing monomeric fluorescent proteins for live-cell imaging applications Nat. Protoc. 9 2014 910 928
72. D.K. Tiwari, and T. Nagai Smart fluorescent proteins: Innovation for barrier-free superresolution imaging in living cells Develop. Growth Differ. 55 2013 491 507
73. R.N. Day, and M.W. Davidson The fluorescent protein palette: Tools for cellular imaging Chem. Soc. Rev. 38 2009 2887 2921
74. M. Fernandez-Suarez, and A.Y. Ting Fluorescent probes for super-resolution imaging in living cells Nat. Rev. Mol. Cell Biol. 9 2008 929 943
75. O.V. Stepanenko, I.M. Kuznetsova, V.V. Verkhusha, and K.K. Turoverov Beta-barrel scaffold of fluorescent proteins: Folding, stability and role in chromophore formation Int. Rev. Cell Mol. Biol. 302 2013 221 278
76. B. Hein, K.I. Willig, and S.W. Hell Stimulated emission depletion (STED) nanoscopy of a fluorescent protein-labeled organelle inside a living cell Proc. Natl. Acad. Sci. U. S. A. 105 2008 14271 14276
77. U.V. Nägerl, K.I. Willig, B. Hein, S.W. Hell, and T. Bonhoeffer Live-cell imaging of dendritic spines by STED microscopy Proc. Natl. Acad. Sci. U. S. A. 105 2008 18982 18987
78. R.L. Strack, B. Hein, D. Bhattacharyya, S.W. Hell, R.J. Keenan, and B.S. Glick A rapidly maturing far-red derivative of DsRed-Express2 for whole-cell labeling Biochemistry 48 2009 8279 8281
79. K.S. Morozova, K.D. Piatkevich, T.J. Gould, J. Zhang, J. Bewersdorf, and V.V. Verkhusha Far-red fluorescent protein excitable with red lasers for flow cytometry and superresolution STED nanoscopy Biophys. J. 99 2010 L13 L15
80. M. Bates, B. Huang, G.T. Dempsey, and X. Zhuang Multicolor super-resolution imaging with photo-switchable fluorescent probes Science 317 2007 1749 1753
81. G.T. Dempsey, J.C. Vaughan, K.H. Chen, M. Bates, and X. Zhuang Evaluation of fluorophores for optimal performance in localization-based super-resolution imaging Nat. Methods 8 2011 1027 1036
82. 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
83. J. Lippincott-Schwartz, and G.H. Patterson Photoactivatable fluorescent proteins for diffraction-limited and super-resolution imaging Trends Cell Biol. 19 2009 555 565
84. J. Wiedenmann, S. Ivanchenko, F. Oswald, F. Schmitt, C. Röcker, A. Salih, K.D. Spindler, and G.U. Nienhaus EosFP, a fluorescent marker protein with UV-inducible green-to-red fluorescence conversion Proc. Natl. Acad. Sci. U. S. A. 101 2004 15905 15910
85. J. Wiedenmann, and G.U. Nienhaus Live-cell imaging with EosFP and other photoactivatable marker proteins of the GFP family Expert Rev. Proteomics 3 2006 361 374
86. J. Wiedenmann, S. Gayda, V. Adam, F. Oswald, K. Nienhaus, D. Bourgeois, and G.U. Nienhaus From EosFP to mIrisFP: Structure-based development of advanced photoactivatable marker proteins of the GFP-family J. Biophotonics 4 2011 377 390
87. S.A. McKinney, C.S. Murphy, K.L. Hazelwood, M.W. Davidson, and L.L. Looger A bright and photostable photoconvertible fluorescent protein Nat. Methods 6 2009 131 133
88. V. Adam, B. Moeyaert, C.C. David, H. Mizuno, M. Lelimousin, P. Dedecker, R. Ando, A. Miyawaki, J. Michiels, Y. Engelborghs, and J. Hofkens Rational design of photoconvertible and biphotochromic fluorescent proteins for advanced microscopy applications Chem. Biol. 18 2011 1241 1251
89. 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. U. S. A. 105 2008 18343 18348
90. Y. Ishitsuka, N. Azadfar, A.Y. Kobitski, K. Nienhaus, N. Johnsson, and G.U. Nienhaus Evaluation of genetically encoded chemical tags as orthogonal fluorophore labeling tools for single-molecule FRET applications J. Phys. Chem. B 119 2015 6611 6619
91. P.D. Hsu, E.S. Lander, and F. Zhang Development and applications of CRISPR-Cas9 for genome engineering Cell 157 2014 1262 1278
92. S.A. Wacker, C. Alvarado, G. von Wichert, U. Knippschild, J. Wiedenmann, K. Clauss, G.U. Nienhaus, H. Hameister, B. Baumann, T. Borggrefe, W. Knöchel, and F. Oswald RITA, a novel modulator of Notch signalling, acts via nuclear export of RBP-J EMBO J. 30 2011 43 56
93. M.D. Schaller Paxillin: A focal adhesion-associated adaptor protein Oncogene 20 2001 6459 6472
94. C. Eggeling, C. Ringemann, R. Medda, G. Schwarzmann, K. Sandhoff, S. Polyakova, V.N. Belov, B. Hein, C. von Middendorff, A. Schonle, and S.W. Hell Direct observation of the nanoscale dynamics of membrane lipids in a living cell Nature 457 2009 1159 1162
95. N. Scherf, and J. Huisken The smart and gentle microscope Nat. Biotechnol. 33 2015 815 818
96. J. Chu, R.D. Haynes, S.Y. Corbel, P. Li, E. Gonzalez-Gonzalez, J.S. Burg, N.J. Ataie, A.J. Lam, P.J. Cranfill, M.A. Baird, M.W. Davidson, H.L. Ng, K.C. Garcia, C.H. Contag, K. Shen, H.M. Blau, and M.Z. Lin Non-invasive intravital imaging of cellular differentiation with a bright red-excitable fluorescent protein Nat. Methods 11 2014 572 578
97. P. Dedecker, F.C. De Schryver, and J. Hofkens Fluorescent proteins: Shine on, you crazy diamond J. Am. Chem. Soc. 135 2013 2387 2402
98. D.M. Shcherbakova, M. Baloban, and V.V. Verkhusha Near-infrared fluorescent proteins engineered from bacterial phytochromes Curr. Opin. Chem. Biol. 27 2015 52 63