High-speed super-resolution imaging of rotationally symmetric structures using SPEED microscopy and 2D-to-3D transformation

Yichen Li, Mark Tingey, Andrew Ruba, Weidong Yang

Published: 2020-12-13 DOI: 10.1038/s41596-020-00440-x

SPEED microscopy

3D super-resolution

rotational symmetry

subcellular structures

data transformation

AI 解读

Reliable detection of somatic mutations in solid tissues by laser-capture microdissection and low-input DNA sequencing

Large-scale preparation of fluorescence multiplex host cell reactivation (FM-HCR) reporters

Constructing and interpreting volcano plots and activity maps to navigate homogeneous catalyst landscapes

The use of methanol as a C1 building block

Yeast-based bioproduction of disulfide-rich peptides and their cyclization via asparaginyl endopeptidases

The maternal serum metabolome by multisegment injection-capillary electrophoresis-mass spectrometry: a high-throughput platform and standardized data workflow for large-scale epidemiological studies

3D human induced pluripotent stem cell–derived bioengineered skeletal muscles for tissue, disease and therapy modeling

Temporally resolved transcriptional recording inE. coliDNA using a Retro-Cascorder

Constructing a cost-efficient, high-throughput and high-quality single-molecule localization microscope for super-resolution imaging

Comprehensive multi-attribute method workflow for biotherapeutic characterization and current good manufacturing practices testing

查看全部

Sections

Figures

References

Various super-resolution imaging techniques have been developed to break the diffraction-limited resolution of light microscopy. However, it still remains challenging to obtain three-dimensional (3D) super-resolution information of structures and dynamic
Introduction
Materials
Procedure
Troubleshooting
Timing
Anticipated results
References
ACKNOWLEDGMENTS

Schnitzbauer, J., Strauss, M. T., Schlichthaerle, T., Schueder, F. & Jungmann, R. Super-resolution microscopy with DNA-PAINT. Nat. Protoc. 12, 1198–1228 (2017).
Pellett, P. A. et al. Two-color STED microscopy in living cells. Biomed. Opt. Express 2, 2364–2371 (2011).
Gwosch, K. C. et al. MINFLUX nanoscopy delivers 3D multicolor nanometer resolution in cells. Nat. Methods 17, 217–224 (2020).
Giannone, G. et al. Dynamic superresolution imaging of endogenous proteins on living cells at ultra-high density. Biophys. J. 99, 1303–1310 (2010).
Agasti, S. S. et al. DNA-barcoded labeling probes for highly multiplexed Exchange-PAINT imaging. Chem. Sci. 8, 3080–3091 (2017).
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).
Abbe, E. Beiträge zur Theorie des Mikroskops und der mikroskopischen Wahrnehmung. Archiv für Mikroskopische Anatomie 9, 413–468 (1873).
Mockl, L., Lamb, D. C. & Brauchle, C. Super-resolved fluorescence microscopy: Nobel Prize in Chemistry 2014 for Eric Betzig, Stefan Hell, and William E. Moerner. Angew. Chem. Int. Ed. Engl. 53, 13972–13977 (2014).
Schermelleh, L., Heintzmann, R. & Leonhardt, H. A guide to super-resolution fluorescence microscopy. J. Cell Biol. 190, 165–175 (2010).
Schermelleh, L. et al. Super-resolution microscopy demystified. Nat. Cell Biol. 21, 72–84 (2019).
Rust, M. J., Bates, M. & Zhuang, X. Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM). Nat. Methods 3, 793–796 (2006).
Kner, P., Chhun, B. B., Griffis, E. R., Winoto, L. & Gustafsson, M. G. L. Super-resolution video microscopy of live cells by structured illumination. Nat. Methods 6, 339–342 (2009).
Hell, S. W. & Wichmann, J. Breaking the diffraction resolution limit by stimulated emission: stimulated-emission-depletion fluorescence microscopy. Opt. Lett. 19, 780–782 (1994).
Betzig, E. et al. Imaging intracellular fluorescent proteins at nanometer resolution. Science 313, 1642–1645 (2006).
Hess, S. T., Girirajan, T. P. & Mason, M. D. Ultra-high resolution imaging by fluorescence photoactivation localization microscopy. Biophys. J. 91, 4258–4272 (2006).
Babcock, H., Sigal, Y. M. & Zhuang, X. A high-density 3D localization algorithm for stochastic optical reconstruction microscopy. Opt. Nanoscopy https://doi.org/10.1186/2192-2853-1-6 (2012).
von Diezmann, A., Shechtman, Y. & Moerner, W. E. Three-dimensional localization of single molecules for super-resolution imaging and single-particle tracking. Chem. Rev. 117, 7244–7275 (2017).
Fuchs, J. et al. A photoactivatable marker protein for pulse-chase imaging with superresolution. Nat. Methods 7, 627–630 (2010).
Zhu, L., Zhang, W., Elnatan, D. & Huang, B. Faster STORM using compressed sensing. Nat. Methods 9, 721–723 (2012).
Manley, S. et al. High-density mapping of single-molecule trajectories with photoactivated localization microscopy. Nat. Methods 5, 155–157 (2008).
Hoze, N. et al. Heterogeneity of AMPA receptor trafficking and molecular interactions revealed by superresolution analysis of live cell imaging. Proc. Natl Acad. Sci. USA 109, 17052–17057 (2012).
Yang, T. T., Tran, M. N. T., Chong, W. M., Huang, C. E. & Liao, J. C. Single-particle tracking localization microscopy reveals nonaxonemal dynamics of intraflagellar transport proteins at the base of mammalian primary cilia. Mol. Biol. Cell 30, 828–837 (2019).
Izeddin, I. et al. Wavelet analysis for single molecule localization microscopy. Opt. Express 20, 2081–2095 (2012).
Gustafsson, M. G. Surpassing the lateral resolution limit by a factor of two using structured illumination microscopy. J. Microsc. 198, 82–87 (2000).
Heintzmann, R. & Cremer, C. G. in Optical Biopsies and Microscopic Techniques III 185–196 (International Society for Optics and Photonics, 1999).
Gustafsson, M. G. et al. Three-dimensional resolution doubling in wide-field fluorescence microscopy by structured illumination. Biophys. J. 94, 4957–4970 (2008).
Schermelleh, L. et al. Subdiffraction multicolor imaging of the nuclear periphery with 3D structured illumination microscopy. Science 320, 1332–1336 (2008).
Heintzmann, R. & Ficz, G. Breaking the resolution limit in light microscopy. Brief. Funct. Genomic. Proteomic. 5, 289–301 (2006).
Vicidomini, G., Bianchini, P. & Diaspro, A. STED super-resolved microscopy. Nat. Methods 15, 173–182 (2018).
Westphal, V., Lauterbach, M. A., Di Nicola, A. & Hell, S. W. Dynamic far-field fluorescence nanoscopy. N. J. Phys. 9, 435–435 (2007).
Willig, K., Keller, J., Bossi, M. & Hell, S. W. STED microscopy resolves nanoparticle assemblies. N. J. Phys. 8, 106 (2006).
Willig, K. I., Rizzoli, S. O., Westphal, V., Jahn, R. & Hell, S. W. STED microscopy reveals that synaptotagmin remains clustered after synaptic vesicle exocytosis. Nature 440, 935–939 (2006).
Dyba, M. & Hell, S. W. Focal spots of size lambda/23 open up far-field florescence microscopy at 33 nm axial resolution. Phys. Rev. Lett. 88, 163901 (2002).
Dyba, M., Jakobs, S. & Hell, S. W. Immunofluorescence stimulated emission depletion microscopy. Nat. Biotechnol. 21, 1303–1304 (2003).
Dyba, M., Keller, J. & Hell, S. W. Phase filter enhanced STED-4Pi fluorescence microscopy: theory and experiment. N. J. Phys. 7, 134–134 (2005).
Klar, T. A., Jakobs, S., Dyba, M., Egner, A. & Hell, S. W. Fluorescence microscopy with diffraction resolution barrier broken by stimulated emission. Proc. Natl Acad. Sci. USA 97, 8206–8210 (2000).
Sidenstein, S. C. et al. Multicolour multilevel STED nanoscopy of actin/spectrin organization at synapses. Sci. Rep. 6, 26725 (2016).
Kilian, N. et al. Assessing photodamage in live-cell STED microscopy. Nat. Methods 15, 755–756 (2018).
Lauterbach, M. A. et al. Comparing video-rate STED nanoscopy and confocal microscopy of living neurons. J. Biophotonics 3, 417–424 (2010).
Ma, J. & Yang, W. Three-dimensional distribution of transient interactions in the nuclear pore complex obtained from single-molecule snapshots. Proc. Natl Acad. Sci. USA 107, 7305–7310 (2010).
Goryaynov, A., Ma, J. & Yang, W. Single-molecule studies of nucleocytoplasmic transport: from one dimension to three dimensions. Integr. Biol. 4, 10–21 (2012).
Goryaynov, A. & Yang, W. Role of molecular charge in nucleocytoplasmic transport. PLoS ONE 9, e88792 (2014).
Junod, S. L., Kelich, J. M., Ma, J. & Yang, W. Nucleocytoplasmic transport of intrinsically disordered proteins studied by high-speed super-resolution microscopy. Protein Sci. 29, 1459–1472 (2020).
Luo, W. et al. Axonemal lumen dominates cytosolic protein diffusion inside the primary cilium. Sci. Rep. 7, 1–11 (2017).
Ma, J., Goryaynov, A., Sarma, A. & Yang, W. Self-regulated viscous channel in the nuclear pore complex. Proc. Natl Acad. Sci. USA 109, 7326–7331 (2012).
Ma, J., Goryaynov, A. & Yang, W. Super-resolution 3D tomography of interactions and competition in the nuclear pore complex. Nat. Struct. Mol. Biol. 23, 239–247 (2016).
Ma, J. et al. High-resolution three-dimensional mapping of mRNA export through the nuclear pore. Nat. Commun. 4, 1–9 (2013).
Mudumbi, K. C. et al. Nucleoplasmic signals promote directed transmembrane protein import simultaneously via multiple channels of nuclear pores. Nat. Commun. 11, 1–14 (2020).
Westphal, V. et al. Video-rate far-field optical nanoscopy dissects synaptic vesicle movement. Science 320, 246–249 (2008).
Li, Y., Luo, W. & Yang, W. Nuclear transport and accumulation of smad proteins studied by single-molecule microscopy. Biophys. J. 114, 2243–2251 (2018).
Sun, C., Yang, W., Tu, L.-C. & Musser, S. M. Single-molecule measurements of importin α/cargo complex dissociation at the nuclear pore. Proc. Natl Acad. Sci. USA 105, 8613–8618 (2008).
Yang, W. & Musser, S. M. Visualizing single molecules interacting with nuclear pore complexes by narrow-field epifluorescence microscopy. Methods 39, 316–328 (2006).
Solovei, I. et al. LBR and lamin A/C sequentially tether peripheral heterochromatin and inversely regulate differentiation. Cell 152, 584–598 (2013).
Mudumbi, K. C., Yang, W., Ma, J. & Schirmer, E. C. Single-point frap distinguishes inner and outer nuclear membrane protein distribution. Biophys. J. 110, 596a (2016).
Daigle, N. et al. Nuclear pore complexes form immobile networks and have a very low turnover in live mammalian cells. J. Cell Biol. 154, 71–84 (2001).
Feldherr, C. M., Kallenbach, E. & Schultz, N. Movement of a karyophilic protein through the nuclear pores of oocytes. J. Cell Biol. 99, 2216–2222 (1984).
Kubitscheck, U., Wedekind, P., Zeidler, O., Grote, M. & Peters, R. Single nuclear pores visualized by confocal microscopy and image processing. Biophys. J. 70, 2067–2077 (1996).
Tokunaga, M., Imamoto, N. & Sakata-Sogawa, K. Highly inclined thin illumination enables clear single-molecule imaging in cells. Nat. Methods 5, 159–161 (2008).
Mudumbi, K. C., Schirmer, E. C. & Yang, W. Single-point single-molecule FRAP distinguishes inner and outer nuclear membrane protein distribution. Nat. Commun. 7, 1–6 (2016).
Tingey, M., Mudumbi, K. C., Schirmer, E. C. & Yang, W. Casting a wider net: differentiating between inner nuclear envelope and outer nuclear envelope transmembrane proteins. Int. J. Mol. Sci. 20, 5248 (2019).
Ott, C. & Lippincott-Schwartz, J. Visualization of live primary cilia dynamics using fluorescence microscopy. Curr. Protoc. Cell Biol. Chapter 4, Unit 4 26 (2012).
Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676–682 (2012).
Grünwald, D. & Singer, R. H. In vivo imaging of labelled endogenous β-actin mRNA during nucleocytoplasmic transport. Nature 467, 604–607 (2010).
Herbert, A. Single Molecule Light Microscopy ImageJ Plugins. http://www.sussex.ac.uk/gdsc/intranet/pdfs/SMLM.pdf (2014).
Punge, A. et al. 3D reconstruction of high-resolution STED microscope images. Microsc. Res. Tech. 71, 644–650 (2008).
Banterle, N., Bui, K. H., Lemke, E. A. & Beck, M. Fourier ring correlation as a resolution criterion for super-resolution microscopy. J. Struct. Biol. 183, 363–367 (2013).
Nieuwenhuizen, R. P. et al. Measuring image resolution in optical nanoscopy. Nat. Methods 10, 557–562 (2013).
Bates, M., Blosser, T. R. & Zhuang, X. Short-range spectroscopic ruler based on a single-molecule optical switch. Phys. Rev. Lett. 94, 108101 (2005).
Bates, M. et al. in Single Molecule Spectroscopy in Chemistry, Physics and Biology 399–415 (Springer, 2010).
Gordon, M. P., Ha, T. & Selvin, P. R. Single-molecule high-resolution imaging with photobleaching. Proc. Natl Acad. Sci. USA 101, 6462–6465 (2004).
Heilemann, M., Margeat, E., Kasper, R., Sauer, M. & Tinnefeld, P. Carbocyanine dyes as efficient reversible single-molecule optical switch. J. Am. Chem. Soc. 127, 3801–3806 (2005).
Kubitscheck, U. et al. Nuclear transport of single molecules: dwell times at the nuclear pore complex. J. Cell Biol. 168, 233–243 (2005).
Ober, R. J., Ram, S. & Ward, E. S. Localization accuracy in single-molecule microscopy. Biophys. J. 86, 1185–1200 (2004).
Qu, X., Wu, D., Mets, L. & Scherer, N. F. Nanometer-localized multiple single-molecule fluorescence microscopy. Proc. Natl Acad. Sci. USA 101, 11298–11303 (2004).
Owen, D. M., Williamson, D., Magenau, A., Rossy, J. & Gaus, K. in Methods in Enzymology Vol. 504 221–235 (Elsevier, 2012).
York, A. G., Ghitani, A., Vaziri, A., Davidson, M. W. & Shroff, H. Confined activation and subdiffractive localization enables whole-cell PALM with genetically expressed probes. Nat. Methods 8, 327–333 (2011).
Temprine, K., York, A. G. & Shroff, H. Three-dimensional photoactivated localization microscopy with genetically expressed probes. Methods Mol. Biol. 1251, 231–261 (2015).
Sharonov, A. & Hochstrasser, R. M. Wide-field subdiffraction imaging by accumulated binding of diffusing probes. Proc. Natl Acad. Sci. USA 103, 18911–18916 (2006).
Jungmann, R. et al. Multiplexed 3D cellular super-resolution imaging with DNA-PAINT and Exchange-PAINT. Nat. Methods 11, 313–318 (2014).
Iinuma, R. et al. Polyhedra self-assembled from DNA tripods and characterized with 3D DNA-PAINT. Science 344, 65–69 (2014).
Schueder, F. et al. Multiplexed 3D super-resolution imaging of whole cells using spinning disk confocal microscopy and DNA-PAINT. Nat. Commun. 8, 1–9 (2017).
Lin, R., Clowsley, A. H., Lutz, T., Baddeley, D. & Soeller, C. 3D super-resolution microscopy performance and quantitative analysis assessment using DNA-PAINT and DNA origami test samples. Methods 174, 56–71 (2020).
Strauss, S. et al. Modified aptamers enable quantitative sub-10-nm cellular DNA-PAINT imaging. Nat. Methods 15, 685–688 (2018).
Nieves, D. J., Gaus, K. & Baker, M. A. DNA-based super-resolution microscopy: DNA-PAINT. Genes 9, 621 (2018).
Chung, E., Kim, D. & So, P. T. Extended resolution wide-field optical imaging: objective-launched standing-wave total internal reflection fluorescence microscopy. Opt. Lett. 31, 945–947 (2006).
Richter, V., Piper, M., Wagner, M. & Schneckenburger, H. Increasing resolution in live cell microscopy by structured illumination (SIM). Appl. Sci. 9, 1188 (2019).
Förster, R. et al. Simple structured illumination microscope setup with high acquisition speed by using a spatial light modulator. Opt. Express 22, 20663–20677 (2014).
Strohl, F. & Kaminski, C. F. Speed limits of structured illumination microscopy. Opt. Lett. 42, 2511–2514 (2017).
Schmidt, R. et al. Spherical nanosized focal spot unravels the interior of cells. Nat. Methods 5, 539–544 (2008).
Hell, S. W. Toward fluorescence nanoscopy. Nat. Biotechnol. 21, 1347–1355 (2003).
Manley, S., Gillette, J. M. & Lippincott-Schwartz, J. in Methods in Enzymology Vol. 475 109–120 (Elsevier, 2010).
Subach, F. V., Patterson, G. H., Renz, M., Lippincott-Schwartz, J. & Verkhusha, V. V. Bright monomeric photoactivatable red fluorescent protein for two-color super-resolution sptPALM of live cells. J. Am. Chem. Soc. 132, 6481–6491 (2010).
Ruba, A., Luo, W., Kelich, J., Tingey, M. & Yang, W. 3D tracking-free approach for obtaining 3D super-resolution information in rotationally symmetric biostructures. J. Phys. Chem. B 123, 5107–5120 (2019).

High-speed super-resolution imaging of rotationally symmetric structures using SPEED microscopy and 2D-to-3D transformation

Supplementary information

推荐阅读