Correlated confocal and super-resolution imaging by VividSTORM

Nature Protocols

Volumn 11, Issue 1, 2016, Pages 163-183

  Barna, László ^a   Dudok, Barna ^a,b   Miczán, Vivien ^a,c   Horváth, András ^c   László, Zsófia I ^a,b   Katona, István ^a  

^a INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^b SEMMELWEIS UNIVERSITY   (Hungary)

^c PÁZMÁNY PÉTER CATHOLIC UNIVERSITY   (Hungary)

Author keywords

[No Author keywords available]

Indexed keywords

ALEXA FLUOR 488; ALEXA FLUOR 561; ALEXA FLUOR 647; ATTO488; ATTO565; CYANINE DYE 3; CYANINE DYE 3B; CYANINE DYE 5; DYE; UNCLASSIFIED DRUG;

ALGORITHM; ANTIBODY LABELING; ARTICLE; CONFOCAL MICROSCOPY; CORRELATION ANALYSIS; ELECTRON MICROSCOPY; FLUORESCENCE PHOTOACTIVATED LOCALIZATION MICROSCOPY; IMAGE ANALYSIS; IMMUNOHISTOCHEMISTRY; MICROSCOPY; NONHUMAN; PHOTOACTIVATED LOCALIZATION MICROSCOPY; PRIORITY JOURNAL; SINGLE MOLECULE LOCALIZATION MICROSCOPY; SOFTWARE; STIMULATED EMISSION DEPLETION MICROSCOPY; STRUCTURED ILLUMINATION MICROSCOPY; THREE DIMENSIONAL IMAGING; VIVIDSTORM; ANIMAL; CLUSTER ANALYSIS; COMPUTER INTERFACE; MOLECULAR IMAGING; MOUSE; PROCEDURES; SIGNAL NOISE RATIO; STAINING; TRANSPORT AT THE CELLULAR LEVEL;

ALGORITHMS; ANIMALS; BIOLOGICAL TRANSPORT; CLUSTER ANALYSIS; IMAGING, THREE-DIMENSIONAL; MICE; MICROSCOPY; MICROSCOPY, CONFOCAL; MOLECULAR IMAGING; SIGNAL-TO-NOISE RATIO; SOFTWARE; STAINING AND LABELING; USER-COMPUTER INTERFACE;

EID: 84988566258     PISSN: 17542189     EISSN: 17502799     Source Type: Journal    
DOI: 10.1038/nprot.2016.002     Document Type: Article

References (69)

1. Betzig, E. et al. Imaging intracellular fluorescent proteins at nanometer resolution. Science 313, 1642-1645 (2006).
2. Hess, S.T., Girirajan, T.P. & Mason, M.D. Ultra-high-resolution imaging by fluorescence photoactivation localization microscopy. Biophys. J. 91, 4258-4272 (2006).
3. Rust, M.J., Bates, M. & Zhuang, X. Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM). Nat. Methods 3, 793-795 (2006).
4. Sauer, M. Localization microscopy coming of age: from concepts to biological impact. J. Cell Sci. 126, 3505-3513 (2013).
5. Dudok, B. et al. Cell-specific STORM super-resolution imaging reveals nanoscale organization of cannabinoid signaling. Nat. Neurosci. 18, 75-86 (2015).
6. Usoskin, D. et al. Unbiased classification of sensory neuron types by large-scale single-cell RNA sequencing. Nat. Neurosci. 18, 145-153 (2015).
7. Zeisel, A. et al. Brain structure. Cell types in the mouse cortex and hippocampus revealed by single-cell RNA-seq. Science 347, 1138-1142 (2015).
8. Darmanis, S. et al. A survey of human brain transcriptome diversity at the single cell level. Proc. Natl. Acad. Sci. USA 112, 7285-7290 (2015).
9. Klausberger, T. & Somogyi, P. Neuronal diversity and temporal dynamics: The unity of hippocampal circuit operations. Science 321, 53-57 (2008).
10. O'Rourke, N.A., Weiler, N.C., Micheva, K.D. & Smith, S.J. Deep molecular diversity of mammalian synapses: why it matters and how to measure it. Nat. Rev. Neurosci. 13, 365-379 (2012).
11. Choquet, D. & Triller, A. The dynamic synapse. Neuron 80, 691-703 (2013).
12. Ludányi, A. et al. Downregulation of the CB1 cannabinoid receptor and related molecular elements of the endocannabinoid system in epileptic human hippocampus. J. Neurosci. 28, 2976-2990 (2008).
13. Jung, K.M. et al. Uncoupling of the endocannabinoid signalling complex in a mouse model of fragile X syndrome. Nat. Commun. 3, 1080 (2012).
14. Nusser, Z. A new approach to estimate the number, density and variability of receptors at central synapses. Eur. J. Neurosci. 11, 745-752 (1999).
15. Masugi-Tokita, M. & Shigemoto, R. High-resolution quantitative visualization of glutamate and GABA receptors at central synapses. Curr. Opin. Neurobiol. 17, 387-393 (2007).
16. Requejo-Isidro, J. Fluorescence nanoscopy. Methods and applications. J. Chem. Biol. 6, 97-120 (2013).
17. Yamanaka, M., Smith, N.I. & Fujita, K. Introduction to super-resolution microscopy. Microscopy (Oxf) 63, 177-192 (2014).
18. Maglione, M. & Sigrist, S.J. Seeing the forest tree by tree: super-resolution light microscopy meets the neurosciences. Nat. Neurosci. 16, 790-797 (2013).
19. Oddone, A., Vilanova, I.V., Tam, J. & Lakadamyali, M. Super-resolution imaging with stochastic single-molecule localization: concepts, technical developments, and biological applications. Microsc. Res. Tech. 77, 502-509 (2014).
20. Lee, S.H. et al. Multiple forms of endocannabinoid and endovanilloid signaling regulate the tonic control of GABA release. J. Neurosci. 35, 10039-10057 (2015).
21. Dani, A., Huang, B., Bergan, J., Dulac, C. & Zhuang, X. Superresolution imaging of chemical synapses in the brain. Neuron 68, 843-856 (2010).
22. Heilemann, M. et al. Subdiffraction-resolution fluorescence imaging with conventional fluorescent probes. Angew. Chem. Int. Ed. Engl. 47, 6172-6176 (2008).
23. Godin, A.G., Lounis, B. & Cognet, L. Super-resolution microscopy approaches for live cell imaging. Biophys. J. 107, 1777-1784 (2014).
24. Dempsey, G.T., Vaughan, J.C., Chen, K.H., Bates, M. & Zhuang, X. Evaluation of fluorophores for optimal performance in localization-based super-resolution imaging. Nat. Methods 8, 1027-1036 (2011).
25. Bates, M., Huang, B., Dempsey, G.T. & Zhuang, X. Multicolor super-resolution imaging with photo-switchable fluorescent probes. Science 317, 1749-1753 (2007).
26. Lakadamyali, M. Super-resolution microscopy: going live and going fast. Chemphyschem 15, 630-636 (2014).
27. Jones, S.A., Shim, S.H., He, J. & Zhuang, X. Fast, three-dimensional super-resolution imaging of live cells. Nat. Methods 8, 499-508 (2011).
28. Shim, S.H. et al. Super-resolution fluorescence imaging of organelles in live cells with photoswitchable membrane probes. Proc. Natl. Acad. Sci. USA 109, 13978-13983 (2012).
29. Zhong, G. et al. Developmental mechanism of the periodic membrane skeleton in axons. Elife 3 http://dx.doi.org/10.7554/eLife.04581 (23 December 2014).
30. van de Linde, S. et al. Direct stochastic optical reconstruction microscopy with standard fluorescent probes. Nat. Protoc. 6, 991-1009 (2011).
31. Gould, T.J., Verkhusha, V.V. & Hess, S.T. Imaging biological structures with fluorescence photoactivation localization microscopy. Nat. Protoc. 4, 291-308 (2009).
32. MacGillavry, H.D. & Blanpied, T.A. Single-molecule tracking photoactivated localization microscopy to map nano-scale structure and dynamics in living spines. Curr. Protoc. Neurosci. 2, 2.20.1-2.20.19 (2013).
33. Löschberger, A., Franke, C., Krohne, G., van de Linde, S. & Sauer, M. Correlative super-resolution fluorescence and electron microscopy of the nuclear pore complex with molecular resolution. J. Cell Sci. 127, 4351-4355 (2014).
34. Tam, J. et al. A microfluidic platform for correlative live-cell and super-resolution microscopy. PLoS ONE 9, e115512 (2014).
35. Tam, J. & Merino, D. STORM in comparison with STED and other imaging methods. J. Neurochem. 135, 643-658 (2015).
36. Tønnesen, J. & Nägerl, U.V. Superresolution imaging for neuroscience. Exp. Neurol. 242, 33-40 (2013).
37. Specht, C.G. et al. Quantitative nanoscopy of inhibitory synapses: counting gephyrin molecules and receptor binding sites. Neuron 79, 308-321 (2013).
38. Puchner, E.M., Walter, J.M., Kasper, R., Huang, B. & Lim, W.A. Counting molecules in single organelles with superresolution microscopy allows tracking of the endosome maturation trajectory. Proc. Natl. Acad. Sci. USA 110, 16015-16020 (2013).
39. Schöcker, K., Holm, T., Franke, C., Sauer, M. & Benavente, R. Elucidation of synaptonemal complex organization by super-resolution imaging with isotropic resolution. Proc. Natl. Acad. Sci. USA 112, 2029-2033 (2015).
40. Lampe, A., Haucke, V., Sigrist, S.J., Heilemann, M. & Schmoranzer, J. Multi-colour direct STORM with red emitting carbocyanines. Biol. Cell 104, 229-237 (2012).
41. Lehmann, M., Lichtner, G., Klenz, H. & Schmoranzer, J. Novel organic dyes for multicolor localization-based super-resolution microscopy. J. Biophotonics http://dx.doi.org/10.1002/jbio.201500119 (13 May 2015).
42. Huang, B., Wang, W., Bates, M. & Zhuang, X. Three-dimensional super-resolution imaging by stochastic optical reconstruction microscopy. Science 319, 810-813 (2008).
43. Lakadamyali, M., Babcock, H., Bates, M., Zhuang, X. & Lichtman, J. 3D multicolor super-resolution imaging offers improved accuracy in neuron tracing. PLoS ONE 7, e30826 (2012).
44. Min, J. et al. 3D high-density localization microscopy using hybrid astigmatic/biplane imaging and sparse image reconstruction. Biomed. Opt. Express 5, 3935-3948 (2014).
45. Kim, D. et al. Correlative stochastic optical reconstruction microscopy and electron microscopy. PLoS ONE 10, e0124581 (2015).
46. Crossman, D.J., Hou, Y., Jayasinghe, I., Baddeley, D. & Soeller, C. Combining confocal and single molecule localisation microscopy: A correlative approach to multi-scale tissue imaging. Methods 88, 98-108 (2015).
47. Hou, Y. et al. Super-resolution fluorescence imaging to study cardiac biophysics: α-Actinin distribution and Z-disk topologies in optically thick cardiac tissue slices. Prog. Biophys. Mol. Biol. 115, 328-339 (2014).
48. Suleiman, H. et al. Nanoscale protein architecture of the kidney glomerular basement membrane. Elife 2, e01149 (2013).
49. Bates, M., Dempsey, G.T., Chen, K.H. & Zhuang, X. Multicolor super-resolution fluorescence imaging via multi-parameter fluorophore detection. Chemphyschem 13, 99-107 (2012).
50. Babcock, H., Sigal, Y.M. & Zhuang, X. A high-density 3D localization algorithm for stochastic optical reconstruction microscopy. Opt. Nanoscopy 1, 6 (2012).
51. Holden, S.J., Uphoff, S. & Kapanidis, A.N. DAOSTORM: An algorithm for high-density super-resolution microscopy. Nat. Methods 8, 279-280 (2011).
52. Dedecker, P., Duwé, S., Neely, R.K. & Zhang, J. Localizer: fast, accurate, open-source, and modular software package for superresolution microscopy. J. Biomed. Opt. 17, 126008 (2012).
53. Hedde, P.N., Fuchs, J., Oswald, F., Wiedenmann, J. & Nienhaus, G.U. Online image analysis software for photoactivation localization microscopy. Nat. Methods 6, 689-690 (2009).
54. Henriques, R. et al. QuickPALM: 3D real-Time photoactivation nanoscopy image processing in ImageJ. Nat. Methods 7, 339-340 (2010).
55. Wolter, S. et al. rapidSTORM: Accurate, fast open-source software for localization microscopy. Nat. Methods 9, 1040-1041 (2012).
56. MacGillavry, H.D., Song, Y., Raghavachari, S. & Blanpied, T.A. Nanoscale scaffolding domains within the postsynaptic density concentrate synaptic AMPA receptors. Neuron 78, 615-622 (2013).
57. Ehmann, N. et al. Quantitative super-resolution imaging of Bruchpilot distinguishes active zone states. Nat. Commun. 5, 4650 (2014).
58. Lu, H.E., MacGillavry, H.D., Frost, N.A. & Blanpied, T.A. Multiple spatial and kinetic subpopulations of CaMKII in spines and dendrites as resolved by single-molecule tracking PALM. J. Neurosci. 34, 7600-7610 (2014).
59. Nair, D. et al. Super-resolution imaging reveals that AMPA receptors inside synapses are dynamically organized in nanodomains regulated by PSD95. J. Neurosci. 33, 13204-13224 (2013).
60. Márquez-Neila, P., Baumela, L. & Alvarez, L. A morphological approach to curvature-based evolution of curves and surfaces. IEEE Trans. Pattern Anal. Mach. Intell. 36, 2-17 (2014).
61. Lorincz, A. & Nusser, Z. Specificity of immunoreactions: The importance of testing specificity in each method. J. Neurosci. 28, 9083-9086 (2008).
62. Andersen, P., Bliss, T.V. & Skrede, K.K. Lamellar organization of hippocampal pathways. Exp. Brain Res. 13, 222-238 (1971).
63. Teyler, T.J. Brain slice preparation: hippocampus. Brain Res. Bull. 5, 391-403 (1980).
64. Song, I. & Semyanov, A. Single cell electrophysiologic recordings in hippocampal slices. Protoc. Exchange http://dx.doi.org/10.1038/protex.2011.253 (2011).
65. Thévenaz, P., Ruttimann, U.E. & Unser, M. A pyramid approach to subpixel registration based on intensity. IEEE Trans. Image Process. 7, 27-41 (1998).
66. Lee, S.H., Földy, C. & Soltesz, I. Distinct endocannabinoid control of GABA release at perisomatic and dendritic synapses in the hippocampus. J. Neurosci. 30, 7993-8000 (2010).
67. Huang, B., Jones, S.A., Brandenburg, B. & Zhuang, X. Whole-cell 3D STORM reveals interactions between cellular structures with nanometer-scale resolution. Nat. Methods 5, 1047-1052 (2008).
68. Thompson, R.E., Larson, D.R. & Webb, W.W. Precise nanometer localization analysis for individual fluorescent probes. Biophys. J. 82, 2775-2783 (2002).
69. 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).