Multicolor Caged dSTORM Resolves the Ultrastructure of Synaptic Vesicles in the Brain
Corresponding Author
Martin Lehmann
Leibniz Institut für Molekulare Pharmakologie (FMP), Robert-Roessle-Strasse 10, 13125 Berlin (Germany)
Freie Universität Berlin, Department of Biochemistry, Takustrasse 6, 14195 Berlin (Germany)
These authors contributed equally to this work.
Leibniz Institut für Molekulare Pharmakologie (FMP), Robert-Roessle-Strasse 10, 13125 Berlin (Germany)Search for more papers by this authorBenjamin Gottschalk
Leibniz Institut für Molekulare Pharmakologie (FMP), Robert-Roessle-Strasse 10, 13125 Berlin (Germany)
These authors contributed equally to this work.
Search for more papers by this authorDmytro Puchkov
Leibniz Institut für Molekulare Pharmakologie (FMP), Robert-Roessle-Strasse 10, 13125 Berlin (Germany)
Search for more papers by this authorPeter Schmieder
Leibniz Institut für Molekulare Pharmakologie (FMP), Robert-Roessle-Strasse 10, 13125 Berlin (Germany)
Search for more papers by this authorSergej Schwagerus
Leibniz Institut für Molekulare Pharmakologie (FMP), Robert-Roessle-Strasse 10, 13125 Berlin (Germany)
Search for more papers by this authorChristian P. R. Hackenberger
Leibniz Institut für Molekulare Pharmakologie (FMP), Robert-Roessle-Strasse 10, 13125 Berlin (Germany)
Humboldt Universität zu Berlin, Department of Chemistry, Brook-Taylor-Strasse. 2, 12489 Berlin (Germany)
Search for more papers by this authorVolker Haucke
Leibniz Institut für Molekulare Pharmakologie (FMP), Robert-Roessle-Strasse 10, 13125 Berlin (Germany)
Freie Universität Berlin, Department of Biochemistry, Takustrasse 6, 14195 Berlin (Germany)
Search for more papers by this authorCorresponding Author
Jan Schmoranzer
Leibniz Institut für Molekulare Pharmakologie (FMP), Robert-Roessle-Strasse 10, 13125 Berlin (Germany)
Freie Universität Berlin, Department of Biochemistry, Takustrasse 6, 14195 Berlin (Germany)
Charité - Universitätsmedizin Berlin, Charité Campus Mitte, Virchowweg 6, 10117 Berlin (Germany)
Leibniz Institut für Molekulare Pharmakologie (FMP), Robert-Roessle-Strasse 10, 13125 Berlin (Germany)Search for more papers by this authorCorresponding Author
Martin Lehmann
Leibniz Institut für Molekulare Pharmakologie (FMP), Robert-Roessle-Strasse 10, 13125 Berlin (Germany)
Freie Universität Berlin, Department of Biochemistry, Takustrasse 6, 14195 Berlin (Germany)
These authors contributed equally to this work.
Leibniz Institut für Molekulare Pharmakologie (FMP), Robert-Roessle-Strasse 10, 13125 Berlin (Germany)Search for more papers by this authorBenjamin Gottschalk
Leibniz Institut für Molekulare Pharmakologie (FMP), Robert-Roessle-Strasse 10, 13125 Berlin (Germany)
These authors contributed equally to this work.
Search for more papers by this authorDmytro Puchkov
Leibniz Institut für Molekulare Pharmakologie (FMP), Robert-Roessle-Strasse 10, 13125 Berlin (Germany)
Search for more papers by this authorPeter Schmieder
Leibniz Institut für Molekulare Pharmakologie (FMP), Robert-Roessle-Strasse 10, 13125 Berlin (Germany)
Search for more papers by this authorSergej Schwagerus
Leibniz Institut für Molekulare Pharmakologie (FMP), Robert-Roessle-Strasse 10, 13125 Berlin (Germany)
Search for more papers by this authorChristian P. R. Hackenberger
Leibniz Institut für Molekulare Pharmakologie (FMP), Robert-Roessle-Strasse 10, 13125 Berlin (Germany)
Humboldt Universität zu Berlin, Department of Chemistry, Brook-Taylor-Strasse. 2, 12489 Berlin (Germany)
Search for more papers by this authorVolker Haucke
Leibniz Institut für Molekulare Pharmakologie (FMP), Robert-Roessle-Strasse 10, 13125 Berlin (Germany)
Freie Universität Berlin, Department of Biochemistry, Takustrasse 6, 14195 Berlin (Germany)
Search for more papers by this authorCorresponding Author
Jan Schmoranzer
Leibniz Institut für Molekulare Pharmakologie (FMP), Robert-Roessle-Strasse 10, 13125 Berlin (Germany)
Freie Universität Berlin, Department of Biochemistry, Takustrasse 6, 14195 Berlin (Germany)
Charité - Universitätsmedizin Berlin, Charité Campus Mitte, Virchowweg 6, 10117 Berlin (Germany)
Leibniz Institut für Molekulare Pharmakologie (FMP), Robert-Roessle-Strasse 10, 13125 Berlin (Germany)Search for more papers by this authorGraphical Abstract
dSTORM gets colorful: A screen for fluorescence recovery following reduction revealed several dyes suitable for high-resolution caged dSTORM imaging. Using dye pairs, multicolor localization precision could be achieved below 15 nm. This system is used to resolve the ultrastructure of single synaptic vesicles. Scale bar: 20 nm.
Abstract
The precision of single-molecule localization-based super-resolution microscopy, including dSTORM, critically depends on the number of detected photons per localization. Recently, reductive caging of fluorescent dyes followed by UV-induced recovery in oxidative buffer systems was used to increase the photon yield and thereby the localization precision in single-color dSTORM. By screening 39 dyes for their fluorescence caging and recovery kinetics, we identify novel dyes that are suitable for multicolor caged dSTORM. Using a dye pair suited for registration error-free multicolor dSTORM based on spectral demixing (SD), a multicolor localization precision below 15 nm was achieved. Caged SD-dSTORM can resolve the ultrastructure of single 40 nm synaptic vesicles in brain sections similar to images obtained by immuno-electron microscopy, yet with much improved label density in two independent channels.
Supporting Information
As a service to our authors and readers, this journal provides supporting information supplied by the authors. Such materials are peer reviewed and may be re-organized for online delivery, but are not copy-edited or typeset. Technical support issues arising from supporting information (other than missing files) should be addressed to the authors.
Filename | Description |
---|---|
anie_201505138_sm_miscellaneous_information.pdf1.6 MB | miscellaneous_information |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
References
- 1E. Betzig, G. H. Patterson, R. Sougrat, O. W. Lindwasser, S. Olenych, J. S. Bonifacino, M. W. Davidson, J. Lippincott-Schwartz, H. F. Hess, Science 2006, 313, 1642–1645.
- 2S. T. Hess, T. P. K. Girirajan, M. D. Mason, Biophys. J. 2006, 91, 4258–4272.
- 3M. J. Rust, M. Bates, X. Zhuang, Nat. Methods 2006, 3, 793–796.
- 4M. Heilemann, S. van de Linde, M. Schüttpelz, R. Kasper, B. Seefeldt, A. Mukherjee, P. Tinnefeld, M. Sauer, Angew. Chem. Int. Ed. 2008, 47, 6172–6176; Angew. Chem. 2008, 120, 6266–6271.
- 5A. Egner, C. Geisler, C. von Middendorff, H. Bock, D. Wenzel, R. Medda, M. Andresen, A. C. Stiel, S. Jakobs, C. Eggeling, et al., Biophys. J. 2007, 93, 3285–3290.
- 6J. C. Vaughan, S. Jia, X. Zhuang, Nat. Methods 2012, 9, 1181–1184.
- 7K. Kundu, S. F. Knight, N. Willett, S. Lee, W. R. Taylor, N. Murthy, Angew. Chem. Int. Ed. 2009, 48, 299–303; Angew. Chem. 2009, 121, 305–309.
- 8L. Carlini, A. Benke, L. Reymond, G. Lukinavičius, S. Manley, ChemPhysChem 2014, 15, 750–755.
- 9A. Lampe, V. Haucke, S. J. Sigrist, M. Heilemann, J. Schmoranzer, Biol. Cell 2012, 104, 229–237.
- 10M. Bossi, J. Fölling, V. N. Belov, V. P. Boyarskiy, R. Medda, A. Egner, C. Eggeling, A. Schönle, S. W. Hell, Nano Lett. 2008, 8, 2463–2468.
- 11D. Baddeley, D. Crossman, S. Rossberger, J. E. Cheyne, J. M. Montgomery, I. D. Jayasinghe, C. Cremer, M. B. Cannell, C. Soeller, PLoS ONE2011, 6, e20645.
- 12G. Tadeus, A. Lampe, J. Schmoranzer, Methods Appl. Fluoresc. 2015, DOI: 10.1088/2050-6120/3/3/037001.
- 13S. Doose, H. Neuweiler, M. Sauer, ChemPhysChem 2009, 10, 1389–1398.
- 14I. H. Stein, S. Capone, J. H. Smit, F. Baumann, T. Cordes, P. Tinnefeld, ChemPhysChem 2012, 13, 931–937.
- 15S. van de Linde, M. Sauer, Chem. Soc. Rev. 2014, 43, 1076–1087.
- 16I. Rasnik, S. A. McKinney, T. Ha, Nat. Methods 2006, 3, 891–893.
- 17J. Vogelsang, R. Kasper, C. Steinhauer, B. Person, M. Heilemann, M. Sauer, P. Tinnefeld, Angew. Chem. Int. Ed. 2008, 47, 5465–5469; Angew. Chem. 2008, 120, 5545–5550.
- 18T. Cordes, J. Vogelsang, P. Tinnefeld, J. Am. Chem. Soc. 2009, 131, 5018–5019.
- 19R. B. Altman, Q. Zheng, Z. Zhou, D. S. Terry, J. D. Warren, S. C. Blanchard, Nat. Methods 2012, 9, 428–429.
- 20V. Glembockyte, R. Lincoln, G. Cosa, J. Am. Chem. Soc. 2015, 137, 1116–1122.
- 21C. C. Valley, S. Liu, D. S. Lidke, K. A. Lidke, PLoS One 2015, 10, e 0123941.
- 22J. Tam, G. A. Cordier, J. S. Borbely, Á. S. Álvarez, M. Lakadamyali, PLoS One 2014, 9, e 101772.
- 23M. Bates, B. Huang, G. T. Dempsey, X. Zhuang, Science 2007, 317, 1749–1753.
- 24U. Endesfelder, S. Malkusch, F. Fricke, M. Heilemann, Histochem. Cell Biol. 2014, 141, 629–638.
- 25R. P. J. Nieuwenhuizen, K. A. Lidke, M. Bates, D. L. Puig, D. Grünwald, S. Stallinga, B. Rieger, Nat. Methods 2013, 10, 557–562.
- 26K. I. Willig, S. O. Rizzoli, V. Westphal, R. Jahn, S. W. Hell, Nature 2006, 440, 935–939.
- 27K. T. Tokuyasu, J. Cell Biol. 1973, 57, 551–565.
- 28P. R. Maycox, E. Link, A. Reetz, S. A. Morris, R. Jahn, J. Cell Biol. 1992, 118, 1379–1388.
- 29F. Blondeau, B. Ritter, P. D. Allaire, S. Wasiak, M. Girard, N. K. Hussain, A. Angers, V. Legendre-Guillemin, L. Roy, D. Boismenu, et al., Proc. Natl. Acad. Sci. USA 2004, 101, 3833–3838.
- 30N. L. Kononenko, D. Puchkov, G. A. Classen, A. M. Walter, A. Pechstein, L. Sawade, N. Kaempf, T. Trimbuch, D. Lorenz, C. Rosenmund, et al., Neuron 2014, 82, 981–988.
- 31S. Watanabe, T. Trimbuch, M. Camacho-Pérez, B. R. Rost, B. Brokowski, B. Söhl-Kielczynski, A. Felies, M. W. Davis, C. Rosenmund, E. M. Jorgensen, Nature 2014, 515, 228–233.
- 32S. Takamori, M. Holt, K. Stenius, E. A. Lemke, M. Grønborg, D. Riedel, H. Urlaub, S. Schenck, B. Brügger, P. Ringler, et al., Cell 2006, 127, 831–846.
- 33F. Opazo, M. Levy, M. Byrom, C. Schäfer, C. Geisler, T. W. Groemer, A. D. Ellington, S. O. Rizzoli, Nat. Methods 2012, 9, 938–939.
- 34J. Ries, C. Kaplan, E. Platonova, H. Eghlidi, H. Ewers, Nat. Methods 2012, 9, 582–584.