Toward Sub-Diffraction Imaging of Single-DNA Molecule Sensors Based on Stochastic Switching Localization Microscopy

The natural characteristics of deoxyribonucleic acid (DNA) enable its advanced applications in nanotechnology as a special tool that can be detected by high-resolution imaging with precise localization. Super-resolution (SR) microscopy enables the examination of nanoscale molecules beyond the diffraction limit. With the development of SR microscopy methods, DNA nanostructures can now be optically assessed. Using the specific binding of fluorophores with their target molecules, advanced single-molecule localization microscopy (SMLM) has been expanded into different fields, allowing wide-range detection at the single-molecule level. This review discusses the recent progress in the SR imaging of DNA nano-objects using SMLM techniques, such as direct stochastic optical reconstruction microscopy, binding-activated localization microscopy, and point accumulation for imaging nanoscale topography. Furthermore, we discuss their advantages and limitations, present applications, and future perspectives.

[1]  Hao Yan,et al.  DNA tile based self-assembly: building complex nanoarchitectures. , 2006, Chemphyschem : a European journal of chemical physics and physical chemistry.

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

[3]  Ralf Jungmann,et al.  DNA origami as a nanoscopic ruler for super-resolution microscopy. , 2009, Angewandte Chemie.

[4]  Adam S. Backer,et al.  Enhanced DNA imaging using super-resolution microscopy and simultaneous single-molecule orientation measurements , 2016, 2016 Conference on Lasers and Electro-Optics (CLEO).

[5]  Ali Ebrahimi,et al.  DNA nanotechnology and bioassay development , 2019, TrAC Trends in Analytical Chemistry.

[6]  Ricardo Henriques,et al.  Fast live-cell conventional fluorophore nanoscopy with ImageJ through super-resolution radial fluctuations , 2016, Nature Communications.

[7]  Maximilian T. Strauss,et al.  Nanometer-scale Multiplexed Super-Resolution Imaging with an Economic 3D-DNA-PAINT Microscope. , 2018, Chemphyschem : a European journal of chemical physics and physical chemistry.

[8]  Nadrian C Seeman,et al.  Crystal structure of a continuous three-dimensional DNA lattice. , 2004, Chemistry & biology.

[9]  R. Holliday A mechanism for gene conversion in fungi. , 1964, Genetical research.

[10]  Peng Yin,et al.  DNA-barcoded labeling probes for highly multiplexed Exchange-PAINT imaging† †Electronic supplementary information (ESI) available. See DOI: 10.1039/c6sc05420j Click here for additional data file. , 2017, Chemical science.

[11]  Edward S Boyden,et al.  Rapid Sequential in Situ Multiplexing With DNA-Exchange-Imaging , 2017, bioRxiv.

[12]  N. Seeman,et al.  DNA double-crossover molecules. , 1993, Biochemistry.

[13]  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.

[14]  Peng Yin,et al.  Optical imaging of individual biomolecules in densely packed clusters , 2016 .

[15]  Hao Yan,et al.  Self-Assembled Water-Soluble Nucleic Acid Probe Tiles for Label-Free RNA Hybridization Assays , 2008, Science.

[16]  Philip Tinnefeld,et al.  Fluorescence microscopy with 6 nm resolution on DNA origami. , 2014, Chemphyschem : a European journal of chemical physics and physical chemistry.

[17]  P. Tinnefeld,et al.  Shifting molecular localization by plasmonic coupling in a single-molecule mirage , 2017, Nature Communications.

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

[19]  Johannes B. Woehrstein,et al.  Quantitative super-resolution imaging with qPAINT , 2016 .

[20]  Peng Yin,et al.  Universal Super-Resolution Multiplexing by DNA Exchange. , 2017, Angewandte Chemie.

[21]  Maximilian T. Strauss,et al.  An order of magnitude faster DNA-PAINT imaging by optimized sequence design and buffer conditions , 2019, Nature Methods.

[22]  S. Kang,et al.  Base Pair Distance in Single‐DNA Molecule via TIRF‐Based Super‐Resolution Radial Fluctuations‐Stream Module , 2020 .

[23]  Maximilian T. Strauss,et al.  DNA nanotechnology and fluorescence applications. , 2016, Current opinion in biotechnology.

[24]  C. Mao,et al.  Synergistic self-assembly of RNA and DNA molecules , 2010, Nature chemistry.

[25]  Veikko Linko,et al.  Evolution of Structural DNA Nanotechnology , 2018, Advanced materials.

[26]  Viola Vogel,et al.  Binding-activated localization microscopy of DNA structures. , 2011, Nano letters.

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

[28]  K. Gaus,et al.  Stoichiometric quantification of spatially dense assemblies with qPAINT , 2019, bioRxiv.

[29]  Matt A. King,et al.  Three-Dimensional Structures Self-Assembled from DNA Bricks , 2012 .

[30]  Maximilian T. Strauss,et al.  Correlating DNA-PAINT and single-molecule FRET for multiplexed super-resolution imaging , 2020, BiOS.

[31]  Hendrik Dietz,et al.  Building machines with DNA molecules , 2019, Nature Reviews Genetics.

[32]  Gaudenz Danuser,et al.  Multiplexed Exchange-PAINT imaging reveals ligand-dependent EGFR and Met interactions in the plasma membrane , 2017, Scientific Reports.

[33]  Helena Gradišar,et al.  Self-assembled bionanostructures: proteins following the lead of DNA nanostructures , 2014, Journal of Nanobiotechnology.

[34]  R. Hochstrasser,et al.  Wide-field subdiffraction imaging by accumulated binding of diffusing probes , 2006, Proceedings of the National Academy of Sciences.

[35]  Yang Liu,et al.  Super-resolution localization microscopy: Toward high throughput, high quality, and low cost. , 2020, APL photonics.

[36]  Ellen C. Jensen*,et al.  Technical Review: Types of Imaging—Direct STORM , 2014, Anatomical record.

[37]  D. Burnham,et al.  Three-dimensional super-resolution fluorescence imaging of DNA , 2019, Scientific Reports.

[38]  P. Schwille,et al.  Flat-top TIRF illumination boosts DNA-PAINT imaging and quantification , 2019, Nature Communications.

[39]  Jing Pan,et al.  Visible/near-infrared subdiffraction imaging reveals the stochastic nature of DNA walkers , 2017, Science Advances.

[40]  L. Albertazzi,et al.  Nanoscale Mapping Functional Sites on Nanoparticles by Points Accumulation for Imaging in Nanoscale Topography (PAINT). , 2018, ACS nano.

[41]  Chengde Mao,et al.  Self-assembly of hexagonal DNA two-dimensional (2D) arrays. , 2005, Journal of the American Chemical Society.

[42]  Johannes B. Woehrstein,et al.  Multiplexed 3D Cellular Super-Resolution Imaging with DNA-PAINT and Exchange-PAINT , 2014, Nature Methods.

[43]  C. Ravarani,et al.  Super-resolution imaging of DNA labelled with intercalating dyes. , 2009, Chemphyschem : a European journal of chemical physics and physical chemistry.

[44]  Na Liu,et al.  A rotary plasmonic nanoclock , 2019, Nature Communications.

[45]  DNA Structure and Supercoiling: Ribbons and a Yo-Yo Model , 2011 .

[46]  Ki-Hyun Kim,et al.  Advanced Selection Methodologies for DNAzymes in Sensing and Healthcare Applications. , 2019, Trends in biochemical sciences.

[47]  A. Meijering,et al.  Imaging unlabeled proteins on DNA with super-resolution , 2020, Nucleic acids research.

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

[49]  K. Gaus,et al.  DNA-Based Super-Resolution Microscopy: DNA-PAINT , 2018, Genes.

[50]  F. Simmel,et al.  Single-molecule kinetics and super-resolution microscopy by fluorescence imaging of transient binding on DNA origami. , 2010, Nano letters.

[51]  Hari K. K. Subramanian,et al.  The label-free unambiguous detection and symbolic display of single nucleotide polymorphisms on DNA origami. , 2011, Nano letters.

[52]  David Baddeley,et al.  3D super-resolution microscopy performance and quantitative analysis assessment using DNA-PAINT and DNA origami test samples , 2019, bioRxiv.

[53]  High-Speed Super-Resolution Imaging Using Protein-Assisted DNA-PAINT , 2020, Nano letters.

[54]  Maximilian T. Strauss,et al.  Correlative Single-Molecule FRET and DNA-PAINT Imaging. , 2018, Nano letters.

[55]  S. Kang,et al.  Super-resolution morphological dissemination of intercalating dye in single DNA molecules via binding activated localization microscopy , 2017 .

[56]  S. Hohng,et al.  Accelerated FRET-PAINT microscopy , 2018, Molecular Brain.

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