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Single-Molecule Localization Super-Resolution Microscopy: Deeper and Faster

Published online by Cambridge University Press:  31 October 2012

Sébastien Herbert
Affiliation:
Institut Pasteur, Groupe Imagerie et Modélisation, CNRS URA 2582, 25 rue du Docteur Roux, 75015 Paris, France Frontiers in Life Sciences PhD Program, University Paris Diderot, 5 rue Thomas-Mann, 75013 Paris, France
Helena Soares
Affiliation:
Institut Pasteur, Lymphocyte Cell Biology Unit, CNRS URA 1961, 28 rue du Docteur Roux, 75015 Paris, France
Christophe Zimmer*
Affiliation:
Institut Pasteur, Groupe Imagerie et Modélisation, CNRS URA 2582, 25 rue du Docteur Roux, 75015 Paris, France
Ricardo Henriques*
Affiliation:
Institut Pasteur, Groupe Imagerie et Modélisation, CNRS URA 2582, 25 rue du Docteur Roux, 75015 Paris, France
*
*Corresponding author: E-mail: czimmer@pasteur.fr
**Corresponding author: E-mail: ricardoh@pasteur.fr
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Abstract

For over a decade fluorescence microscopy has demonstrated the capacity to achieve single-molecule localization accuracies of a few nanometers, well below the ∼200 nm lateral and ∼500 nm axial resolution limit of conventional microscopy. Yet, only the recent development of new fluorescence labeling modalities, the increase in sensitivity of imaging hardware, and the creation of novel image analysis tools allow for the emergence of single-molecule-based super-resolution imaging techniques. Novel methods such as photoactivated localization microscopy and stochastic optical reconstruction microscopy can typically reach a tenfold increase in resolution compared to standard microscopy methods. Their implementation is relatively easy only requiring minimal changes to a conventional wide-field or total internal reflection fluorescence microscope. The recent translation of these two methods into commercial imaging systems has made them further accessible to researchers in biology. However, these methods are still evolving rapidly toward imaging live samples with high temporal resolution and depth. In this review, we recall the roots of single-molecule localization microscopy, summarize major recent developments, and offer perspective on potential applications.

Type
Biological Applications
Copyright
Copyright © Microscopy Society of America 2012

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References

Abbe, E. (1882). The relations of aperture and power in the microscope. J Roy Micro Soc 2, 300309.CrossRefGoogle Scholar
Abraham, A.V., Ram, S., Chao, J., Ward, E. & Ober, R.J. (2009). Quantitative study of single molecule location estimation techniques. Opt Express 17, 23352. CrossRefGoogle ScholarPubMed
Ando, T., Uchihashi, T., Kodera, N., Yamamoto, D., Miyagi, A., Taniguchi, M. & Yamashita, H. (2008). High-speed AFM and nano-visualization of biomolecular processes. Eur J Physiol 456, 211225.Google Scholar
Aquino, D., Schönle, A., Geisler, C., Middendorff, C.V., Wurm, C.A., Okamura, Y., Lang, T., Hell, S.W. & Egner, A. (2011). Two-color nanoscopy of three-dimensional volumes by 4Pi detection of stochastically switched fluorophores. Nat Methods 8, 353359.Google Scholar
Axelrod, D. (1981). Cell-substrate contacts illuminated by total internal reflection fluorescence. J Cell Biol 89, 141145.Google Scholar
Baddeley, D., Crossman, D., Rossberger, S., Cheyne, J.E., Montgomery, J.M., Jayasinghe, I.D., Cremer, C., Cannell, M.B. & Soeller, C. (2011). 4D super-resolution microscopy with conventional fluorophores and single wavelength excitation in optically thick cells and tissues. PLoS One 6, e20645. CrossRefGoogle ScholarPubMed
Bates, M., Huang, B., Dempsey, G.T. & Zhuang, X. (2007). Multicolor super-resolution imaging with photo-switchable fluorescent probes. Science 317, 17491753.Google Scholar
Betzig, E. (1995). Proposed method for molecular optical imaging. Opt Lett 20, 237239.CrossRefGoogle ScholarPubMed
Betzig, E., Patterson, G.H., Sougrat, R., Lindwasser, O.W., Olenych, S., Bonifacino, J.S., Davidson, M.W., Lippincott-Schwartz, J. & Hess, H.F. (2006). Imaging intracellular fluorescent proteins at nanometer resolution. Science 313, 16421645.CrossRefGoogle ScholarPubMed
Biteen, J.S., Thompson, M.A., Tselentis, N.K., Bowman, G.R., Shapiro, L. & Moerner, W.E. (2008). Super-resolution imaging in live Caulobacter crescentus cells using photoswitchable EYFP. Nat Methods 5, 947949.CrossRefGoogle ScholarPubMed
Burnette, D.T., Sengupta, P., Dai, Y., Lippincott-Schwartz, J. & Kachar, B. (2011). Bleaching/blinking assisted localization microscopy for superresolution imaging using standard fluorescent molecules. Proc Natl Acad Sci USA 108, 2108121086.CrossRefGoogle ScholarPubMed
Chao, J., Ram, S., Abraham, A.V., Sally Ward, E. & Ober, R.J. (2009a). A resolution measure for three-dimensional microscopy. Optics Comm 282, 17511761.Google Scholar
Chao, J., Ram, S., Ward, E.S. & Ober, R.J. (2009b). A comparative study of high resolution microscopy imaging modalities using a three-dimensional resolution measure. Opt Express 17, 2437724402.CrossRefGoogle ScholarPubMed
Cheezum, M.K., Walker, W.F. & Guilford, W.H. (2001). Quantitative comparison of algorithms for tracking single fluorescent particles. Biophys J 81, 23782388.Google Scholar
Cox, S., Rosten, E., Monypenny, J., Jovanovic-Talisman, T., Burnette, D.T., Lippincott-Schwartz, J., Jones, G.E. & Heintzmann, R. (2011). Bayesian localization microscopy reveals nanoscale podosome dynamics. Nat Methods 9, 195200.Google Scholar
Cremer, C. & Cremer, T. (1978). Considerations on a laser-scanning-microscope with high-resolution and depth of field. Microsc Acta 81, 3144.Google Scholar
Crocker, J.C. & Grier, D.G. (1996). Methods of digital video microscopy for colloidal studies. J Colloid Interf Sci 179, 298310.CrossRefGoogle Scholar
Dedecker, P., Mo, G.C.H., Dertinger, T. & Zhang, J. (2012). Widely accessible method for superresolution fluorescence imaging of living systems. Proc Natl Acad Sci USA 109, 1090910914.Google Scholar
de Jonge, N., Peckys, D.B., Kremers, G.J. & Piston, D.W. (2009). Electron microscopy of whole cells in liquid with nanometer resolution. Proc Natl Acad Sci USA 106, 21592164.CrossRefGoogle ScholarPubMed
Dertinger, T., Colyer, R., Iyer, G., Weiss, S. & Enderlein, J. (2009). Fast, background-free, 3D super-resolution optical fluctuation imaging (SOFI). Proc Natl Acad Sci USA 106, 2228722292.CrossRefGoogle ScholarPubMed
Ehsani, S., Santos, J.C., Rodrigues, C.D., Henriques, R., Audry, L., Zimmer, C., Sansonetti, P., Tran Van Nhieu, G. & Enninga, J. (2012). Hierarchies of host factor dynamics at the entry site of Shigella flexneri during host cell invasion. Infect Immun 80, 25482557.Google Scholar
Erni, R., Rossell, M.D., Kisielowski, C. & Dahmen, U. (2009). Atomic-resolution imaging with a sub-50-pm electron probe. Phys Rev Lett 102, 96101. Google Scholar
Folling, J., Bossi, M., Bock, H., Medda, R., Wurm, C.A., Hein, B., Jakobs, S., Eggeling, C. & Hell, S.W. (2008). Fluorescence nanoscopy by ground-state depletion and single-molecule return. Nat Methods 5, 943945.Google Scholar
Gautier, A., Juillerat, A., Heinis, C., Correa, I.R. Jr., Kindermann, M., Beaufils, F. & Johnsson, K. (2008). An engineered protein tag for multiprotein labeling in living cells. Chem Biol 15, 128136.Google Scholar
Gelles, J., Schnapp, B.J. & Sheetz, M.P. (1988). Tracking kinesin-driven movements with nanometre-scale precision. Nature 331, 450453.CrossRefGoogle ScholarPubMed
Giessibl, F.J. (1995). Atomic resolution of the silicon (111)-(7×7) surface by atomic force microscopy. Science 267, 6871.CrossRefGoogle Scholar
Gordon, M.P., Ha, T. & Selvin, P.R. (2004). Single-molecule high-resolution imaging with photobleaching. Proc Natl Acad Sci USA 101, 6462. CrossRefGoogle ScholarPubMed
Greenfield, D., McEvoy, A.L., Shroff, H., Crooks, G.E., Wingreen, N.S., Betzig, E. & Liphardt, J. (2009). Self-organization of the Escherichia coli chemotaxis network imaged with super-resolution light microscopy. PLoS Biol 7, e1000137. CrossRefGoogle ScholarPubMed
Gustafsson, M.G.L. (2000). Surpassing the lateral resolution limit by a factor of two using structured illumination microscopy. J Microsc 198, 8287.Google Scholar
Hänninen, P., Hell, S., Salo, J., Soini, E. & Cremer, C. (1995). Two-photon excitation 4Pi confocal microscope: Enhanced axial resolution microscope for biological research. Appl Phys Lett 66, 1698. CrossRefGoogle Scholar
Hedde, P.N., Fuchs, J., Oswald, F., Wiedenmann, J. & Nienhaus, G.U. (2009). Online image analysis software for photoactivation localization microscopy. Nat Methods 6, 689690.CrossRefGoogle ScholarPubMed
Heilemann, M., van de Linde, S., Mukherjee, A. & Sauer, M. (2009). Super-resolution imaging with small organic fluorophores. Angew Chem Int Edit 48, 69036908.CrossRefGoogle ScholarPubMed
Hell, S.W. & Wichmann, J. (1994). Breaking the diffraction resolution limit by stimulated emission: Stimulated-emission-depletion fluorescence microscopy. Opt Lett 19, 780782.Google Scholar
Henriques, R., Griffiths, C., Hesper Rego, E. & Mhlanga, M.M. (2011). PALM and STORM: Unlocking live-cell super-resolution. Biopolymers 95, 322331.Google Scholar
Henriques, R., Lelek, M., Fornasiero, E.F., Valtorta, F., Zimmer, C. & Mhlanga, M.M. (2010). QuickPALM: 3D real-time photoactivation nanoscopy image processing in ImageJ. Nat Methods 7, 339340.CrossRefGoogle ScholarPubMed
Henriques, R. & Mhlanga, M.M. (2009). PALM and STORM: What hides beyond the Rayleigh limit? Biotechnol J 4, 846857.Google Scholar
Hess, S.T., Girirajan, T.P. & Mason, M.D. (2006). Ultra-high resolution imaging by fluorescence photoactivation localization microscopy. Biophys J 91, 42584272.CrossRefGoogle ScholarPubMed
Holden, S.J., Uphoff, S. & Kapanidis, A.N. (2011). DAOSTORM: An algorithm for high-density super-resolution microscopy. Nat Methods 8, 279280.Google Scholar
Hu, K., Ji, L., Applegate, K.T., Danuser, G. & Waterman-Storer, C.M. (2007). Differential transmission of actin motion within focal adhesions. Science's STKE 315, 111.Google ScholarPubMed
Huang, B., Bates, M. & Zhuang, X. (2009). Super-resolution fluorescence microscopy. Annu Rev Biochem 78, 9931016.Google Scholar
Huang, B., Jones, S.A., Brandenburg, B. & Zhuang, X. (2008a). Whole-cell 3D STORM reveals interactions between cellular structures with nanometer-scale resolution. Nat Methods 5, 10471052.Google Scholar
Huang, B., Wang, W., Bates, M. & Zhuang, X. (2008b). Three-dimensional super-resolution imaging by stochastic optical reconstruction microscopy. Science 319, 810813.Google Scholar
Huang, F., Schwartz, S.L., Byars, J.M. & Lidke, K.A. (2011). Simultaneous multiple-emitter fitting for single molecule super-resolution imaging. Biomed Opt Express 2, 13771393.CrossRefGoogle ScholarPubMed
Jares-Erijman, E.A. & Jovin, T.M. (2003). FRET imaging. Nat Biotechnol 21, 13871395.Google Scholar
Jones, S.A., Shim, S.H., He, J. & Zhuang, X. (2011). Fast, three-dimensional super-resolution imaging of live cells. Nat Methods 8, 499505.Google Scholar
Juette, M.F., Gould, T.J., Lessard, M.D., Mlodzianoski, M.J., Nagpure, B.S., Bennett, B.T., Hess, S.T. & Bewersdorf, J. (2008). Three-dimensional sub-100 nm resolution fluorescence microscopy of thick samples. Nat Methods 5, 527529.CrossRefGoogle ScholarPubMed
Kao, H.P. & Verkman, A. (1994). Tracking of single fluorescent particles in three dimensions: Use of cylindrical optics to encode particle position. Biophys J 67, 12911300.Google Scholar
Klar, T.A., Jakobs, S., Dyba, M., Egner, A. & Hell, S.W. (2000). Fluorescence microscopy with diffraction resolution barrier broken by stimulated emission. Proc Natl Acad Sci USA 97, 8206. CrossRefGoogle ScholarPubMed
Klein, T., Löschberger, A., Proppert, S., Wolter, S., van de Linde, S. & Sauer, M. (2010). Live-cell dSTORM with SNAP-tag fusion proteins. Nat Methods 8, 79.Google Scholar
Kner, P., Chhun, B.B., Griffis, E.R., Winoto, L. & Gustafsson, M.G.L. (2009). Super-resolution video microscopy of live cells by structured illumination. Nat Methods 6, 339342.CrossRefGoogle ScholarPubMed
Lacoste, T.D., Michalet, X., Pinaud, F., Chemla, D.S., Alivisatos, A.P. & Weiss, S. (2000). Ultrahigh-resolution multicolor colocalization of single fluorescent probes. Proc Natl Acad Sci USA 97, 9461. Google Scholar
Lelek, M., Di Nunzio, F., Henriques, R., Charneau, P., Arhel, N. & Zimmer, C. (2012). Superresolution imaging of HIV in infected cells with FlAsH-PALM. Proc Natl Acad Sci USA 109, 85648569.Google Scholar
Lidke, K., Rieger, B., Jovin, T. & Heintzmann, R. (2005). Superresolution by localization of quantum dots using blinking statistics. Opt Express 13, 70527062.Google Scholar
Löschberger, A., van de Linde, S., Dabauvalle, M.C., Rieger, B., Heilemann, M., Krohne, G. & Sauer, M. (2012). Super-resolution imaging visualizes the eightfold symmetry of gp210 proteins around the nuclear pore complex and resolves the central channel with nanometer resolution. J Cell Sci 125, 570575.CrossRefGoogle ScholarPubMed
Lukyanov, K.A., Chudakov, D.M., Lukyanov, S. & Verkhusha, V.V. (2005). Innovation: Photoactivatable fluorescent proteins. Nat Rev Mol Cell Biol 6, 885891.Google Scholar
Ma, H., Long, F., Zeng, S. & Huang, Z.L. (2012). Fast and precise algorithm based on maximum radial symmetry for single molecule localization. Opt Lett 37, 24812483.CrossRefGoogle ScholarPubMed
Manley, S., Gillette, J.M., Patterson, G.H., Shroff, H., Hess, H.F., Betzig, E. & Lippincott-Schwartz, J. (2008). High-density mapping of single-molecule trajectories with photoactivated localization microscopy. Nat Methods 5, 155157.CrossRefGoogle ScholarPubMed
Matsuda, A., Shao, L., Boulanger, J., Kervrann, C., Carlton, P.M., Kner, P., Agard, D. & Sedat, J.W. (2010). Condensed mitotic chromosome structure at nanometer resolution using PALM and EGFP-histones. PLoS One 5, e12768. Google Scholar
Mattheyses, A.L., Simon, S.M. & Rappoport, J.Z. (2010). Imaging with total internal reflection fluorescence microscopy for the cell biologist. J Cell Sci 123, 36213628.CrossRefGoogle ScholarPubMed
Ober, R.J., Ram, S. & Ward, E.S. (2004). Localization accuracy in single-molecule microscopy. Biophys J 86, 11851200.CrossRefGoogle ScholarPubMed
Parthasarathy, R. (2012). Rapid, accurate particle tracking by calculation of radial symmetry centers. Nat Methods 9, 724726.Google Scholar
Pavani, S.R., Thompson, M.A., Biteen, J.S., Lord, S.J., Liu, N., Twieg, R.J., Piestun, R. & Moerner, W.E. (2009). Three-dimensional, single-molecule fluorescence imaging beyond the diffraction limit by using a double-helix point spread function. Proc Natl Acad Sci USA 106, 29952999.CrossRefGoogle ScholarPubMed
Pertsinidis, A., Zhang, Y. & Chu, S. (2010). Subnanometre single-molecule localization, registration and distance measurements. Nature 466, 647651.CrossRefGoogle ScholarPubMed
Qu, X., Wu, D., Mets, L. & Scherer, N.F. (2004). Nanometer-localized multiple single-molecule fluorescence microscopy. Proc Natl Acad Sci USA 101, 11298. Google Scholar
Ries, J., Kaplan, C., Platonova, E., Eghlidi, H. & Ewers, H. (2012). A simple, versatile method for GFP-based super-resolution microscopy via nanobodies. Nat Methods 9, 582584.Google Scholar
Rino, J., Braga, J., Henriques, R. & Carmo-Fonseca, M. (2009). Frontiers in fluorescence microscopy. Int J Dev Biol 53, 15691579.Google Scholar
Rogers, S.S., Waigh, T.A., Zhao, X. & Lu, J.R. (2007). Precise particle tracking against a complicated background: Polynomial fitting with Gaussian weight. Phys Biol 4, 220.Google Scholar
Rust, M.J., Bates, M. & Zhuang, X. (2006). Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM). Nat Methods 3, 793795.CrossRefGoogle ScholarPubMed
Schermelleh, L., Heintzmann, R. & Leonhardt, H. (2010). A guide to super-resolution fluorescence microscopy. J Cell Biol 190, 165175.Google Scholar
Schmidt, R., Wurm, C.A., Jakobs, S., Engelhardt, J., Egner, A. & Hell, S.W. (2008). Spherical nanosized focal spot unravels the interior of cells. Nat Methods 5, 539544.Google Scholar
Shroff, H., Galbraith, C.G., Galbraith, J.A. & Betzig, E. (2008). Live-cell photoactivated localization microscopy of nanoscale adhesion dynamics. Nat Methods 5, 417423.CrossRefGoogle ScholarPubMed
Shtengel, G., Galbraith, J.A., Galbraith, C.G., Lippincott-Schwartz, J., Gillette, J.M., Manley, S., Sougrat, R., Waterman, C.M., Kanchanawong, P. & Davidson, M.W. (2009). Interferometric fluorescent super-resolution microscopy resolves 3D cellular ultrastructure. Proc Natl Acad Sci USA 106, 3125. Google Scholar
Simonson, P.D., Rothenberg, E. & Selvin, P.R. (2011). Single-molecule-based super-resolution images in the presence of multiple fluorophores. Nano Lett 11(11), 50905096.Google Scholar
Smith, C.S., Joseph, N., Rieger, B. & Lidke, K.A. (2010). Fast, single-molecule localization that achieves theoretically minimum uncertainty. Nat Methods 7, 373375.Google Scholar
Steinhauer, C., Forthmann, C., Vogelsang, J. & Tinnefeld, P. (2008). Superresolution microscopy on the basis of engineered dark states. J Am Chem Soc 130, 1684016841.Google Scholar
Thompson, R.E., Larson, D.R. & Webb, W.W. (2002). Precise nanometer localization analysis for individual fluorescent probes. Biophys J 82, 27752783.Google Scholar
Tokunaga, M., Imamoto, N. & Sakata-Sogawa, K. (2008). Highly inclined thin illumination enables clear single-molecule imaging in cells. Nat Methods 5, 159161.CrossRefGoogle ScholarPubMed
Truong, T.V., Supatto, W., Koos, D.S., Choi, J.M. & Fraser, S.E. (2011). Deep and fast live imaging with two-photon scanned light-sheet microscopy. Nat Methods 8, 757760.Google Scholar
Van Oijen, A., Köhler, J., Schmidt, J., Müller, M. & Brakenhoff, G. (1998). 3-Dimensional super-resolution by spectrally selective imaging. Chem Phys Lett 292, 183187.CrossRefGoogle Scholar
Vaziri, A., Tang, J., Shroff, H. & Shank, C.V. (2008). Multilayer three-dimensional super resolution imaging of thick biological samples. Proc Natl Acad Sci USA 105, 2022120226.Google Scholar
Vogelsang, J., Kasper, R., Steinhauer, C., Person, B., Heilemann, M., Sauer, M. & Tinnefeld, P. (2008). A reducing and oxidizing system minimizes photobleaching and blinking of fluorescent dyes. Angew Chem Int Ed Engl 47, 54655469.Google Scholar
Wolter, S., Schüttpelz, M., Tscherepanow, M., Van de Linde, S., Heilemann, M. & Sauer, M. (2010). Real-time computation of sub-diffraction-resolution fluorescence images. J Microsc 237, 1222.Google Scholar
Wombacher, R., Heidbreder, M., van de Linde, S., Sheetz, M.P., Heilemann, M., Cornish, V.W. & Sauer, M. (2010). Live-cell super-resolution imaging with trimethoprim conjugates. Nat Methods 7, 717719.CrossRefGoogle ScholarPubMed
Xu, K., Babcock, H.P. & Zhuang, X. (2012). Dual-objective STORM reveals three-dimensional filament organization in the actin cytoskeleton. Nat Methods 9, 185188.CrossRefGoogle ScholarPubMed
Yildiz, A., Forkey, J.N., McKinney, S.A., Ha, T., Goldman, Y.E. & Selvin, P.R. (2003). Myosin V walks hand-over-hand: Single fluorophore imaging with 1.5-nm localization. Science 300, 20612065.Google Scholar
York, A.G., Ghitani, A., Vaziri, A., Davidson, M.W. & Shroff, H. (2011). Confined activation and subdiffractive localization enables whole-cell PALM with genetically expressed probes. Nat Methods 8, 327333.CrossRefGoogle ScholarPubMed
Zanacchi, F.C., Lavagnino, Z., Donnorso, M.P., Del Bue, A., Furia, L., Faretta, M. & Diaspro, A. (2011). Live-cell 3D super-resolution imaging in thick biological samples. Nat Methods 8, 10471049.Google Scholar
Zhu, L., Zhang, W., Elnatan, D. & Huang, B. (2012). Faster STORM using compressed sensing. Nat Methods 9(7), 721723.CrossRefGoogle ScholarPubMed