Super‐resolution imaging with stochastic single‐molecule localization: Concepts, technical developments, and biological applications

Light microscopy has undergone a revolution with the advent of super‐resolution microscopy methods that can surpass the diffraction limit. These methods have generated much enthusiasm, in particular with regards to the new possibilities they offer for biological imaging. The recent years have seen a great advancement both in terms of new technological developments and exciting biological applications. Here, we review some of the important milestones in the field and highlight some recent biological applications. Microsc. Res. Tech. 77:502–509, 2014. © 2014 Wiley Periodicals, Inc.

[1]  M. Beck,et al.  Fourier ring correlation as a resolution criterion for super-resolution microscopy. , 2013, Journal of structural biology.

[2]  Mike Heilemann,et al.  Live-cell super-resolution imaging with trimethoprim conjugates , 2010, Nature Methods.

[3]  Mark Bates,et al.  Short-range spectroscopic ruler based on a single-molecule optical switch. , 2005, Physical review letters.

[4]  Mark Bates,et al.  Multicolor Super-Resolution Fluorescence Imaging via Multi-Parameter Fluorophore Detection , 2011, Chemphyschem : a European journal of chemical physics and physical chemistry.

[5]  Hazen P. Babcock,et al.  Dual-objective STORM reveals three-dimensional filament organization in the actin cytoskeleton , 2011, Nature Methods.

[6]  Mike Heilemann,et al.  Super-resolution imaging with small organic fluorophores. , 2009, Angewandte Chemie.

[7]  S. Holden,et al.  DAOSTORM: an algorithm for high- density super-resolution microscopy , 2011, Nature Methods.

[8]  J. Lichtman,et al.  3D Multicolor Super-Resolution Imaging Offers Improved Accuracy in Neuron Tracing , 2012, PloS one.

[9]  X. Zhuang,et al.  Actin, Spectrin, and Associated Proteins Form a Periodic Cytoskeletal Structure in Axons , 2013, Science.

[10]  Mike Heilemann,et al.  Super-resolution fluorescence imaging of chromosomal DNA. , 2012, Journal of structural biology.

[11]  Paul R Selvin,et al.  Myosin VI Steps via a Hand-over-Hand Mechanism with Its Lever Arm Undergoing Fluctuations when Attached to Actin* , 2004, Journal of Biological Chemistry.

[12]  Chenglong Xia,et al.  Super-resolution fluorescence imaging of organelles in live cells with photoswitchable membrane probes , 2012, Proceedings of the National Academy of Sciences.

[13]  P. Gönczy,et al.  Resolution Doubling in 3D-STORM Imaging through Improved Buffers , 2013, PloS one.

[14]  C. Flors,et al.  Photoswitching of monomeric and dimeric DNA-intercalating cyanine dyes for super-resolution microscopy applications , 2010, Photochemical & photobiological sciences : Official journal of the European Photochemistry Association and the European Society for Photobiology.

[15]  Yaron M Sigal,et al.  A high-density 3D localization algorithm for stochastic optical reconstruction microscopy , 2012, Optical Nanoscopy.

[16]  Tobias M. P. Hartwich,et al.  Video-rate nanoscopy using sCMOS camera- specific single-molecule localization algorithms , 2013 .

[17]  J. Lippincott-Schwartz,et al.  Photoactivatable fluorescent proteins for diffraction-limited and super-resolution imaging. , 2009, Trends in cell biology.

[18]  Mark Bates,et al.  Evaluation of fluorophores for optimal performance in localization-based super-resolution imaging , 2011, Nature Methods.

[19]  Mark Bates,et al.  Super-resolution fluorescence microscopy. , 2009, Annual review of biochemistry.

[20]  Samuel J. Lord,et al.  Three-dimensional, single-molecule fluorescence imaging beyond the diffraction limit by using a double-helix point spread function , 2009, Proceedings of the National Academy of Sciences.

[21]  M. Heilemann,et al.  Live-cell super-resolution imaging with synthetic fluorophores. , 2012, Annual review of physical chemistry.

[22]  Mark Bates,et al.  Three-Dimensional Super-Resolution Imaging by Stochastic Optical Reconstruction Microscopy , 2008, Science.

[23]  Dylan T Burnette,et al.  Bayesian localisation microscopy reveals nanoscale podosome dynamics , 2011, Nature Methods.

[24]  Suliana Manley,et al.  Live‐Cell dSTORM of Cellular DNA Based on Direct DNA Labeling , 2012, Chembiochem : a European journal of chemical biology.

[25]  H. Flyvbjerg,et al.  Optimized localization-analysis for single-molecule tracking and super-resolution microscopy , 2010, Nature Methods.

[26]  Joshua C Vaughan,et al.  Phosphine quenching of cyanine dyes as a versatile tool for fluorescence microscopy. , 2013, Journal of the American Chemical Society.

[27]  S. Hell.  Far-Field Optical Nanoscopy , 2007, Science.

[28]  X. Zhuang,et al.  Breaking the Diffraction Barrier: Super-Resolution Imaging of Cells , 2010, Cell.

[29]  Lei Zhu,et al.  Faster STORM using compressed sensing , 2012, Nature Methods.

[30]  M. Dahan,et al.  Quantitative Nanoscopy of Inhibitory Synapses: Counting Gephyrin Molecules and Receptor Binding Sites , 2013, Neuron.

[31]  Shigeki Iwanaga,et al.  Superresolution imaging of targeted proteins in fixed and living cells using photoactivatable organic fluorophores. , 2010, Journal of the American Chemical Society.

[32]  Michael J Rust,et al.  Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM) , 2006, Nature Methods.

[33]  N. Daigle,et al.  Nuclear Pore Scaffold Structure Analyzed by Super-Resolution Microscopy and Particle Averaging , 2013, Science.

[34]  Melike Lakadamyali,et al.  Super-resolution microscopy: going live and going fast. , 2014, Chemphyschem : a European journal of chemical physics and physical chemistry.

[35]  M. Lakadamyali,et al.  Single-molecule evaluation of fluorescent protein photoactivation efficiency using an in vivo nanotemplate , 2014, Nature Methods.

[36]  S. Hell,et al.  Subdiffraction resolution in far-field fluorescence microscopy. , 1999, Optics letters.

[37]  J. Lippincott-Schwartz,et al.  Interferometric fluorescent super-resolution microscopy resolves 3D cellular ultrastructure , 2009, Proceedings of the National Academy of Sciences.

[38]  Jason M. Byars,et al.  Dual-color superresolution microscopy reveals nanoscale organization of mechanosensory podosomes , 2013, Molecular biology of the cell.

[39]  George H. Patterson,et al.  A Photoactivatable GFP for Selective Photolabeling of Proteins and Cells , 2002, Science.

[40]  Bernd Rieger,et al.  Super-resolution imaging visualizes the eightfold symmetry of gp210 proteins around the nuclear pore complex and resolves the central channel with nanometer resolution , 2012, Journal of Cell Science.

[41]  Michael W. Davidson,et al.  Dual-color superresolution imaging of genetically expressed probes within individual adhesion complexes , 2007, Proceedings of the National Academy of Sciences.

[42]  M. Heilemann,et al.  Super-Resolution Microscopy Reveals Specific Recruitment of HIV-1 Envelope Proteins to Viral Assembly Sites Dependent on the Envelope C-Terminal Tail , 2013, PLoS pathogens.

[43]  X. Zhuang,et al.  Superresolution Imaging of Chemical Synapses in the Brain , 2010, Neuron.

[44]  Michael D. Mason,et al.  Ultra-high resolution imaging by fluorescence photoactivation localization microscopy. , 2006, Biophysical journal.

[45]  M. Gustafsson.  Nonlinear structured-illumination microscopy: wide-field fluorescence imaging with theoretically unlimited resolution. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[46]  Mark Bates,et al.  Multicolor Super-Resolution Imaging with Photo-Switchable Fluorescent Probes , 2007, Science.

[47]  W. Webb,et al.  Precise nanometer localization analysis for individual fluorescent probes. , 2002, Biophysical journal.

[48]  Mike Heilemann,et al.  Multicolor photoswitching microscopy for subdiffraction-resolution fluorescence imaging , 2009, Photochemical & photobiological sciences : Official journal of the European Photochemistry Association and the European Society for Photobiology.

[49]  H. Ewers,et al.  A simple, versatile method for GFP-based super-resolution microscopy via nanobodies , 2012, Nature Methods.

[50]  M. Heilemann,et al.  Subdiffraction-resolution fluorescence imaging with conventional fluorescent probes. , 2008, Angewandte Chemie.

[51]  E. Betzig,et al.  Live-cell photoactivated localization microscopy of nanoscale adhesion dynamics , 2008, Nature Methods.

[52]  M. Heilemann,et al.  Carbocyanine dyes as efficient reversible single-molecule optical switch. , 2005, Journal of the American Chemical Society.

[53]  X. Zhuang,et al.  Fast three-dimensional super-resolution imaging of live cells , 2011, Nature Methods.

[54]  Sjoerd Stallinga,et al.  The effect of background on localization uncertainty in single emitter imaging , 2012, 2012 9th IEEE International Symposium on Biomedical Imaging (ISBI).

[55]  Štefan Bálint,et al.  Correlative live-cell and superresolution microscopy reveals cargo transport dynamics at microtubule intersections , 2013, Proceedings of the National Academy of Sciences.

[56]  Sjoerd Stallinga,et al.  Measuring image resolution in optical nanoscopy , 2013, Nature Methods.

[57]  Aleksandra Radenovic,et al.  Identification of the factors affecting co-localization precision for quantitative multicolor localization microscopy , 2012, Optical Nanoscopy.

[58]  A. Diaspro,et al.  Live-cell 3D super-resolution imaging in thick biological samples , 2011, Nature Methods.

[59]  A. Ting,et al.  Fluorescent probes for super-resolution imaging in living cells , 2008, Nature Reviews Molecular Cell Biology.

[60]  Jin-Soo Kim,et al.  Live-cell dSTORM with SNAP-tag fusion proteins , 2010, Nature Methods.

[61]  Peter J. Verveer,et al.  Chemically Induced Photoswitching of Fluorescent Probes—A General Concept for Super-Resolution Microscopy , 2011, Molecules.

[62]  F. Del Bene,et al.  Optical Sectioning Deep Inside Live Embryos by Selective Plane Illumination Microscopy , 2004, Science.

[63]  S. Hell,et al.  Fluorescence microscopy with diffraction resolution barrier broken by stimulated emission. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[64]  J. Lippincott-Schwartz,et al.  Imaging Intracellular Fluorescent Proteins at Nanometer Resolution , 2006, Science.