Direct stochastic optical reconstruction microscopy with standard fluorescent probes

Nature Protocols

Volumn 6, Issue 7, 2011, Pages 991-1009

  Van De Linde, Sebastian ^a   Löschberger, Anna ^a   Klein, Teresa ^a   Heidbreder, Meike ^a   Wolter, Steve ^a   Heilemann, Mike ^a   Sauer, Markus ^a  

^a UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY LABELING; ARTICLE; CELL ACTIVITY; CLINICAL PROTOCOL; DIRECT STOCHASTIC OPTICAL RECONSTRUCTION MICROSCOPY; EXPERIMENTAL DESIGN; FLUORESCENCE ANALYSIS; FLUORESCENCE MICROSCOPY; FLUORESCENT ANTIBODY TECHNIQUE; IMAGE ANALYSIS; IMAGE PROCESSING; IMAGE QUALITY; IMAGE RECONSTRUCTION; INTERMETHOD COMPARISON; MICROSCOPY; NONHUMAN; PRIORITY JOURNAL; SIGNAL DETECTION; WAVEFORM;

AUTOMATIC DATA PROCESSING; FLUORESCENT DYES; MICROSCOPY, FLUORESCENCE; PHOTONS; SOFTWARE; STAINING AND LABELING; STOCHASTIC PROCESSES;

EID: 79959898156     PISSN: 17542189     EISSN: 17502799     Source Type: Journal    
DOI: 10.1038/nprot.2011.336     Document Type: Article

References (101)

1. Abbe, E. Beiträge zur Theorie des Mikroskops und der mikroskopischen Wahrnehmung. Arch. Mikrosk. Anat. 9, 413-487 (1873).
2. Born, M. & Wolf, E. Principles of Optics: Electromagnetic Theory of Propagation, Interference and Diffraction of Light (Cambridge University Press, 1997).
3. Betzig, E. & Trautman, J.K. Near-field optics: Microscopy, spectroscopy, and surface modification beyond the diffraction limit. Science 257, 189-195 (1992).
4. Hell, S. & Stelzer, E.H.K. Fundamental improvement of resolution with a 4Pi-confocal fluorescence microscope using two-photon excitation. Opt. Commun. 93, 277-282 (1992). (Pubitemid 23635703)
5. Hell, S.W. & Wichmann, J. Breaking the diffraction resolution limit by stimulated emission: Stimulated-emission-depletion fluorescence microscopy. Opt. Lett. 19, 780-782 (1994).
6. Hell, SW. Far-field optical nanoscopy. Science 316, 1153-1158 (2007). (Pubitemid 46877470)
7. Gustafsson, M.G. Surpassing the lateral resolution limit by a factor of two using structured illumination microscopy. J. Microsc. 198, 82-87 (2000). (Pubitemid 30316807)
8. Kner, P., Chhun, B.B., Griffis, E.R., Winoto, L. & Gustafsson, M.G. Super-resolution video microscopy of live cells by structured illumination. Nat. Methods 6, 339-342 (2009).
9. Bobroff, N. Position measurement with a resolution and noise limited instrument. Rev. Sci. Instrum. 57, 1152-1157 (1986).
10. Betzig, E. Proposed method for molecular optical imaging. Opt. Lett. 20, 237-239 (1995).
11. Bornfleth, H., Sätzler, K., Eils, R. & Cremer, C. High-precision distance measurements and volume-conserving segmentation of objects near and below the resolution limit in three-dimensional confocal fluorescence microscopy. J. Microsc. 189, 118-136 (1998). (Pubitemid 28109122)
12. Lacoste, Th.D. et al. Ultrahigh-resolution multicolour colocalization of single fluorescent probes. Proc. Natl Acad. Sci. USA 97, 9461-9466 (2000).
13. Heilemann, M. et al. High-resolution colocalization of single dye molecules by fluorescence lifetime imaging microscopy. Anal. Chem. 74, 3511-3517 (2002). (Pubitemid 34764961)
14. Thompson, R.E., Larson, D.R. & Webb, W.W. Precise nanometer localization analysis for individual fluorescent probes. Biophys. J. 82, 2775-2783 (2002). (Pubitemid 34441314)
15. Yildiz, A. et al. Myosin V walks hand-over-hand: Single fluorophore imaging with 1.5-nm localization. Science 300, 2061-2065 (2003). (Pubitemid 36760126)
16. Qu, X., Wu, D., Mets, L. & Scherer, N.F. Nanometer-localized multiple single-molecule fluorescene microscopy. Proc. Natl Acad. Sci. USA 101, 11298-11303 (2004). (Pubitemid 39038341)
17. Lidke, K.A., Rieger, B., Jovin, T.M. & Heintzmann, R. Superresolution by localization of quantum dots using blinking statistics. Opt. Exp. 13, 7052-7062 (2005). (Pubitemid 41305581)
18. Betzig, E. et al. Imaging intracellular fluorescent proteins at nanometer resolution. Science 313, 1642-1645 (2006). (Pubitemid 44414039)
19. Hess, S.T., Girirajan, T.P. & Mason, M.D. Ultra-high resolution imaging by fluorescence photoactivation localization microscopy. Biophys. J. 91, 4258-4272 (2006). (Pubitemid 44887284)
20. Rust, M.J., Bates, B. & Zhuang, X. Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM). Nat. Methods 3, 793-795 (2006). (Pubitemid 44445825)
21. Heilemann, M. et al. Subdiffraction-resolution fluorescence imaging with conventional fluorescent probes. Angew. Chem. Int. Ed. 47, 6172-6176 (2008).
22. Heilemann, M., van de Linde, S., Mukherjee, A. & Sauer, M. Super-resolution imaging with small organic fluorophores. Angew. Chem. Int. Ed. 48, 6903-6908 (2009).
23. Lemmer, P. et al. SPDM: Light microscopy with single-molecule resolution at the nanoscale. Appl. Phys. B 93, 1-12 (2008).
24. Baddeley, D. et al. Light-induced dark states of organic fluochromes enable 30 nm resolution imaging in standard media. Biophys. J. 96, L22-L24 (2009).
25. Gunkel, M. et al. Dual color localization microscopy of cellular nanostructures. Biotechnol. J. 4, 927-938 (2009).
26. Fölling, J. et al. Fluorescence nanoscopy by ground-state depletion and single-molecule return. Nat. Methods 5, 943-945 (2008).
27. Steinhauer, C., Forthmann, C., Vogelsang, J. & Tinnefeld, P. Superresolution microscopy on the basis of engineered dark states. J. Am. Chem. Soc. 130, 16840-16841 (2008).
28. Vogelsang, J., Cordes, T., Forthmann, C., Steinhauer, C. & Tinnefeld, P. Controlling the fluorescence of ordinary oxazine dyes for single-molecule switching and superresolution microscopy. Proc. Natl Acad. Sci. USA 106, 8107-8112 (2009).
29. Dertinger, T., Colyer, R., Iyer, G., Weiss, S. & Enderlein, J. Fast background-free 3D superresolution optical fluctuation imaging (SOFI). Proc. Natl Acad. Sci. USA 106, 22287-22292 (2009).
30. Dertinger, T., Heilemann, M., Vogel, R., Sauer, M. & Weiss, S. Super-resolution optical fluctuation imaging with organic dyes. Angew. Chem. Int. Ed. 49, 9441-9443 (2010).
31. Flors, C. et al. A stroboscopic approach for fast photoactivation- localization microscopy with dronpa mutants. J. Am. Chem. Soc. 129, 13970-13977 (2007). (Pubitemid 350106088)
32. Flors, C., Ravarani, C.N. & Dryden, D.T. Super-resolution imaging of DNA labeled with intercalating dyes. Chemphyschem 10, 2201-2204 (2009).
33. Gould, T.J., Verkhusha, V.V. & Hess, S.T. Imaging biological structures with fluorescence photoactivation localization microscopy. Nat. Protoc. 4, 291-308 (2009).
34. Shroff, H., White, H. & Betzig, E. Photoactivation localization microscopy (PALM) of adhesion complexes. Curr. Protoc. Cell Biol. 41, 4.21.1-4.21.27 (2008).
35. Ji, N., Shroff, H., Zhong, H & Betzig, E. Advances in the speed and resolution of light microscopy. Curr. Opin. Neurobiol. 18, 605-616 (2008).
36. Hell, S.W. Microscopy and its focal switch. Nat. Methods 6, 24-32 (2009).
37. Huang, B., Bates, M. & Zhuang, X. Super-resolution fluorescence microscopy. Annu. Rev. Biochem. 78, 993-1016 (2009).
38. Heilemann, M. Fluorescence microscopy beyond the diffraction limit. J. Biotechnol. 149, 243-251 (2010).
39. Lippincott-Schwartz, J. & Patterson, G.H. Fluorescent proteins: A cell biologist's user guide. Methods Cell Biol. 85, 45-61 (2008).
40. Shroff, H., Galbraith, C.G., Galbraith, J.A. & Betzig, E. Live-cell photoactivated localization microscopy of nanoscale adhesion dynamics. Nat. Methods 5, 417-423 (2008). (Pubitemid 351619100)
41. Manley, S. et al. High-density mapping of single-molecule trajectories with photoactivated localization microscopy. Nat. Methods 5, 155-157 (2008). (Pubitemid 351181741)
42. Ormo, M. et al. Crystal structure of the Aequorea Victoria green fluorescent protein. Science 273, 1392-1395 (1996). (Pubitemid 26296528)
43. Shannon, C.E. Communication in the presence of noise. Proc. Inst. Radio Eng. 37, 10-21 (1949).
44. Shaner, N.C. Improving the photostability of bright monomeric orange and red fluorescent proteins. Nat. Methods 5, 545-551 (2008). (Pubitemid 351761763)
45. Tang, J., Akerboom, J., Vaziri, A., Looger, L.L. & Shank, S.V. Near-isotropic 3D optical nanoscopy with photon-limited chromophores. Proc. Natl Acad. Sci. USA 107, 10068-10073 (2010).
46. van de Linde, S., Sauer, M. & Heilemann, M. Subdiffraction-resolution fluorescence imaging of proteins in the inner mitochondrial membrane with photoswitchable fluorophores. J. Struct. Biol. 164, 250-254 (2008).
47. van de Linde, S., Kasper, R., Heilemann, M. & Sauer, M. Photoswitching microscopy with standard fluorophores. Appl. Phys. B. 93, 725-731 (2008).
48. Heilemann, M., Dedecker, P., Hofkens, J. & Sauer, M. Photoswitches: Key molecules for subdiffraction-resolution fluorescecne imaging and molecular quantification. Laser Photon. Rev. 3, 180-202 (2009).
49. van de Linde, S. et al. Multicolor photoswitching microscopy for subdiffraction-resolution fluorescence imaging. Photochem. Photobiol. Sci. 8, 465-469 (2009).
50. Owen, D.M. et al. PALM imaging and cluster analysis of protein heterogeneity at the cell surface. J. Biophotonics 3, 446-454 (2009).
51. Endesfelder, U., van de Linde, S., Wolter, S., Sauer, M. & Heilemann, M. Subdiffraction-resolution fluorescence microscopy of myosin-actin motility. Chemphyschem 11, 836-840 (2010).
52. Wombacher, R. et al. Live cell super-resolution imaging with trimethoprim conjugates. Nat. Methods 7, 717-719 (2010).
53. Klein, T. et al. Live-cell dSTORM with SNAP-tag fusion proteins. Nat. Methods 8, 7-9 (2011).
54. Wolter, S. et al. Real-time computation of subdiffraction-resolution fluorescence images,. J. Microsc. 237, 12-22 (2010).
55. Beaumont, P.C., Johnson, D.G. & Parsons, B.J. Excited state and free radical properties of rhodamine dyes in aqueous solution: A laser flash photolysis and pulse radiolysis study. J. Photochem. Photobiol. 107, 175-183 (1997). (Pubitemid 127166002)
56. Doose, S., Neuweiler, H. & Sauer, M. Fluorescence quenching by photoinduced electron transfer: A reporter for conformational dynamics of macromolecules. Chemphyschem 10, 1389-1398 (2009).
57. Görner, H. Oxygen uptake induced by electron transfer from donors to the triplet state of methylene blue and xanthene dyes in air-saturated aqueous solution. Photochem. Photobiol. Sci. 7, 371-376 (2008). (Pubitemid 351501305)
58. Burner, U., Jantschko, W. & Obinger, C. Kinetics of oxidation of aliphatic and aromatic thiols by myeloperoxidase compounds I and II. FEBS Lett. 443, 290-296 (1999). (Pubitemid 29080813)
59. Burner, U. & Obinger, C. Transient-state and steady-state kinetics of the oxidation of aliphatic and aromatic thiols by horseradish peroxidase. FEBS Lett. 411, 269-274 (1997). (Pubitemid 27301468)
60. Madej, E. & Wardman, P. The oxidizing power of the glutathione thiyl radical as measured by its electrode potential at physiological pH. Arch. Biochem. Biophys. 462, 94-102 (2007). (Pubitemid 46755135)
61. Wardmann, P. Reduction potentials of one-electron couples involving free radicals in aqueous solution. J. Phys. Chem. Ref. Data 18, 1637-1755 (1989).
62. van de Linde, S. et al. Photoinduced formation of reversible dye radicals and their impact on super-resolution imaging. Photochem. Photobiol. Sci. 10, 499-506 (2011).
63. Michaelis, L., Schubert, M.P. & Granick, S. Semiquinone radicals of thiazines. J. Am. Chem. Soc. 62, 204-211 (1940).
64. Heineken, F.W., Bruin, M. & Bruin, F. ESR investigation of some thiazine and oxazine dye radicals. J. Chem Phys. 37, 1479-1482 (1962).
65. Kottke, T., van de Linde, S., Sauer, M., Kakorin, S. & Heilemann, M. Identification of the product of photoswitching of an oxazine fluorophore using FT-IR difference spectroscopy. J. Phys. Chem. Lett. 1, 3156-3159 (2010).
66. Sies, H. Glutathione and its role in cellular functions. Free Radic. Biol. Med. 27, 916-921 (1999). (Pubitemid 29507465)
67. Benesch, R.E. & Benesch, R. Enzymatic removal of oxygen for polarography and related methods. Science 118, 447-448 (1953).
68. Rasnik, I., McKinney, S.A. & Ha, T. Nonblinking and long-lasting single-molecule fluorescence imaging. Nat. Methods 3, 891-893 (2006). (Pubitemid 44614723)
69. Lenhard, J.R. & Cameron, A.D. Electrochemistry and electronic spectra of cyanine dye radicals in acetonitrile. J. Phys. Chem. 97, 4916-4925 (1993).
70. Dempsey, G.T. et al. Photoswitching mechanism of cyanine dyes. J. Am. Chem. Soc. 131, 18192-18193 (2009).
71. Lord, S.J. et al. A photoactivatable push-pull fluorophore for single-molecule imaging in live cells. J. Am. Chem. Soc. 130, 9204-9205 (2008). (Pubitemid 352031111)
72. Lee, H.D. et al. Superresolution imaging of targeted proteins in fixed and living cells using photoactivatable organic fluorophores. J. Am. Chem. Soc. 132, 15099-15101 (2010).
73. Fölling, J. et al. Photochromic rhodamines provide nanoscopy with optical sectioning. Angew. Chem. Int. Ed. 46, 6266-6270 (2007). (Pubitemid 47329414)
74. Bossi, M. et al. Multicolor far-field fluorescence nanoscopy through isolated detection of distinct molecular species. Nano Lett. 8, 2463-2468 (2008).
75. van de Linde, S., Wolter, S., Heilemann, M. & Sauer, M. The effect of photoswitching kinetics and labeling densities on super-resolution fluorescence imaging. J. Biotechnol. 149, 260-266 (2010).
76. Cordes, T. et al. Resolving single-molecule assembled patterns with superresolution blink-microscopy. Nano Lett. 10, 645-651 (2010).
77. Vogelsang, J. et al. Make them blink: Probes for super-resolution microscopy. Chemphyschem 11, 2475-2490 (2010).
78. Tokunaga, M., Imamoto, N. & Sakata-Sogawa, K. Highly inclined thin illumination enables clear single-molecule imaging in cells. Nat. Methods 5, 159-161 (2008). (Pubitemid 351181742)
79. Pavani, S.R. et al. Three-dimensional, single-molecule fluorescence imaging beyond the diffraction limit by using a double-helix point spread function. Proc. Natl Acad. Sci. USA 106, 2995-2999 (2009).
80. Shtengel, G. et al. Interferometric fluorescent super-resolution microscopy resolves 3D cellular ultrastructure. Proc. Natl Acad. Sci. USA 106, 3125-3130 (2009).
81. Juette, M.F. et al. Three-dimensional sub-100 nm resolution fluorescecne microscopy of thick samples. Nat. Methods 5, 527-529 (2008). (Pubitemid 351761759)
82. Huang, B., Wang, W.Q., Bates, M. & Zhuang, X.W. Three-dimensional super-resolution imaging by stochastic optical reconstruction microscopy. Science 319, 810-813 (2008). (Pubitemid 351225870)
83. Neubeck, A. & van Gool, L. Efficient non-maximum suppression. in ICPR '06: Proceedings of the 18th International Conference on Pattern Recognition. Hong Kong, pp 850-855 (IEEE Computer Society, 2006). (Pubitemid 46553254)
84. Galassi, M. et al. Gnu Scientific Library: Reference Manual (Network Theory, 2003).
85. Yaroslavsky, L.P. Digital Picture Processing. (Springer, 1985).
86. Thomann, D., Dorn, J., Sorger, P.K. & Danuser, G. Automatic fluorescent tag localization II: Improvement in super-resolution by relative tracking. J. Microsc. 211, 230-248 (2003). (Pubitemid 37100359)
87. Hess, S.T. et al. Dynamic clustered distribution of hemaglutinin resolved at 40 nm in living cell membranes discriminates between raft theories. Proc. Natl Acad. Sci. USA 104, 17370-17375 (2007). (Pubitemid 350219826)
88. Zhang, J., Campbell, R.E., Ting, A.Y. & Tsien, R.Y. Creating new fluorescent probes for cell biology. Nat. Rev. Mol. Cell Biol. 3, 906-918 (2002). (Pubitemid 35477369)
89. Lippincott-Schwartz, J. & Patterson, G.H. Development and use of fluorescent protein markers in living cells. Science 300, 87-91 (2003). (Pubitemid 36423032)
90. Miyawaki, A., Sawano, A. & Kogure, T. Lighting up cells: Labelling proteins with fluorophores. Nat. Cell Biol. 5, S1-S7 (2003). (Pubitemid 37082166)
91. Riedl, J. et al. Lifeact: A versatile marker to visualize F-actin. Nat. Methods 5, 605-607 (2008). (Pubitemid 351911864)
92. Griffin, B.A., Adams, S.R. & Tsien, R.Y. Specific covalent labeling of recombinant protein molecules inside live cells. Science 281, 269-272 (1998). (Pubitemid 28334512)
93. Keppler, A. et al. A general method for the covalent labeling of fusion proteins with small molecules in vivo. Nat. Biotechnol. 21, 86-89 (2003). (Pubitemid 36055833)
94. Keppler, A., Pick, H., Arrivoli, C., Vogel, H. & Johnsson, K. Labelling of fusion proteins with synthetic fluorophores in live cells. Proc. Natl Acad. Sci. USA 101, 9955-9959 (2004). (Pubitemid 38891177)
95. Los, G.V. et al. HaloTag: A novel protein labeling technology for cell imaging and protein analysis. ACS Chem. Biol. 3, 373-382 (2008).
96. Miller, L.W. & Cornish, V.W. Selective chemical labeling of proteins in living cells. Curr. Opin. Chem. Biol. 9, 56-61 (2005). (Pubitemid 40208625)
97. Miller, L.W., Cai, Y., Sheetz, M.P. & Cornish, V.W. In vivo protein labelling with trimethoprim conjugates: A flexible chemical tag. Nat. Methods 2, 255-257 (2005). (Pubitemid 41131005)
98. Gallagher, S. et al. An in vivo covalent TMP-tag based on proximity-induced reactivity. ACS Chem. Biol. 7, 547-556 (2009).
99. Michalet, X. et al. Quantum dots for live cells, in vivo imaging, and diagnostics. Science 307, 538-544 (2005). (Pubitemid 40165671)
100. Robinson, R.W. & Snyder, J.A. An innovative fixative for cytoskeletal components allows high resolution in colocalization studies using immunofluorescence techniques. Histochem. Cell. Biol. 122, 1-5 (2004). (Pubitemid 39070587)
101. Vogelsang, J. et al. A reducing and oxidizing system minimizes photobleaching and blinking of fluorescent dyes. Angew. Chem. Int. Ed. 47, 5465-5469 (2008).