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Super-resolution Microscopy with Adaptive Optics for Volumetric Imaging

  • Park, Sangjun (Department of Medical Life Sciences, College of Medicine, The Catholic University of Korea) ;
  • Min, Cheol Hong (Department of Medical Life Sciences, College of Medicine, The Catholic University of Korea) ;
  • Han, Seokyoung (Department of Mechanical Engineering, University of Louisville) ;
  • Choi, Eunjin (Department of Medical Life Sciences, College of Medicine, The Catholic University of Korea) ;
  • Cho, Kyung-Ok (Department of Biomedicine & Health Sciences, College of Medicine, The Catholic University of Korea) ;
  • Jang, Hyun-Jong (Department of Biomedicine & Health Sciences, College of Medicine, The Catholic University of Korea) ;
  • Kim, Moonseok (Department of Medical Life Sciences, College of Medicine, The Catholic University of Korea)
  • Received : 2022.10.16
  • Accepted : 2022.11.07
  • Published : 2022.12.25

Abstract

Optical microscopy is a useful tool for study in the biological sciences. With an optical microscope, we can observe the micro world of life such as tissues, cells, and proteins. A fluorescent dye or a fluorescent protein provides an opportunity to mark a specific target in the crowd of biological samples, so that an image of a specific target can be observed by an optical microscope. The optical microscope, however, is constrained in resolution due to diffraction limit. Super-resolution microscopy made a breakthrough with this diffraction limit. Using a super-resolution microscope, many biomolecules are observed beyond the diffraction limit in cells. In the case of volumetric imaging, the super-resolution techniques are only applied to a limited area due to long imaging time, multiple scattering of photons, and sample-induced aberration in deep tissue. In this article, we review recent advances in super-resolution microscopy for volumetric imaging. The super-resolution techniques have been integrated with various modalities, such as a line-scan confocal microscope, a spinning disk confocal microscope, a light sheet microscope, and point spread function engineering. Super-resolution microscopy combined with adaptive optics by compensating for wave distortions is a promising method for deep tissue imaging and biomedical applications.

Keywords

Acknowledgement

FIG. 1 and FIG. 4 were created with BioRender.com.

References

  1. E. Abbe, "Ueber einen neuen Beleuchtungsapparat am Mikroskop," Archiv fur Mikroskopische Anatomie 9, 469-480 (1873). https://doi.org/10.1007/BF02956177
  2. B. Huang, H. Babcock, and X. Zhuang, "Breaking the diffraction barrier: Super-resolution imaging of cells," Cell 143, 1047-1058 (2010). https://doi.org/10.1016/j.cell.2010.12.002
  3. Y. M. Sigal, R. Zhou, and X. Zhuang, "Visualizing and discovering cellular structures with super-resolution microscopy," Science 361, 880-887 (2018). https://doi.org/10.1126/science.aau1044
  4. L. Mockl and W. E. Moerner, "Super-resolution microscopy with single molecules in biology and beyond-Essentials, current trends, and future challenges," J. Am. Chem. Soc. 142, 17828-17844 (2020). https://doi.org/10.1021/jacs.0c08178
  5. S. W. Hell and J. Wichmann, "Breaking the diffraction resolution limit by stimulated emission: stimulated-emission-depletion fluorescence microscopy," Opt. Lett. 19, 780-782 (1994). https://doi.org/10.1364/OL.19.000780
  6. S. W. Hell and M. Kroug, "Ground-state-depletion fluorscence microscopy: A concept for breaking the diffraction resolution limit," Appl. Phys. B 60, 495-497 (1995). https://doi.org/10.1007/BF01081333
  7. T. A. Klar, S. Jakobs, M. Dyba, A. Egner, and S. W. Hell, "Fluorescence microscopy with diffraction resolution barrier broken by stimulated emission," Proc. Natl. Acad. Sci. U. S. A. 97, 8206-8210 (2000). https://doi.org/10.1073/pnas.97.15.8206
  8. J. Heine, M. Reuss, B. Harke, E. D'Este, S. J. Sahl, and S. W. Hell, "Adaptive-illumination STED nanoscopy," Proc. Natl. Acad. Sci. U. S. A. 114, 9797-9802 (2017). https://doi.org/10.1073/pnas.1708304114
  9. F. Gottfert, T. Pleiner, J. Heine, V. Westphal, D. Gorlich, S. J. Sahl, and S. W. Hell, "Strong signal increase in STED fluorescence microscopy by imaging regions of subdiffraction extent," Proc. Natl. Acad. Sci. U. S. A. 114, 2125-2130 (2017). https://doi.org/10.1073/pnas.1621495114
  10. V. V. G. K. Inavalli, M. O. Lenz, C. Butler, J. Angibaud, B. Compans, F. Levet, J. Tonnesen, O. Rossier, G. Giannone, O. Thoumine, E. Hosy, D. Choquet, J.-B. Sibarita, and U. V. Nagerl, "A super-resolution platform for correlative live single-molecule imaging and STED microscopy," Nat. Methods 16, 1263-1268 (2019). https://doi.org/10.1038/s41592-019-0611-8
  11. A. Barbotin, S. Galiani, I. Urbancic, C. Eggeling, and M. J. Booth, "Adaptive optics allows STED-FCS measurements in the cytoplasm of living cells," Opt. Express 27, 23378-23395 (2019). https://doi.org/10.1364/OE.27.023378
  12. L. Chu, J. Tyson, J. E. Shaw, F. Rivera-Molina, A. J. Koleske, A. Schepartz, and D. K. Toomre, "Two-color nanoscopy of organelles for extended times with HIDE probes," Nat. Commun. 11, 4271 (2020). https://doi.org/10.1038/s41467-020-17859-1
  13. M. G. L. Gustafsson, "Surpassing the lateral resolution limit by a factor of two using structured illumination microscopy," J. Microsc. 198, 82-87 (2000). https://doi.org/10.1046/j.1365-2818.2000.00710.x
  14. M. G. L. Gustafsson, "Nonlinear structured-illumination microscopy: Wide-field fluorescence imaging with theoretically unlimited resolution," Proc. Natl. Acad. Sci. U. S. A. 102, 13081-13086 (2005). https://doi.org/10.1073/pnas.0406877102
  15. P. Kner, B. B. Chhun, E. R. Griffis, L. Winoto, and M. G. L. Gustafsson, "Super-resolution video microscopy of live cells by structured illumination," Nat. Methods 6, 339-342 (2009). https://doi.org/10.1038/nmeth.1324
  16. R. Fiolka, L. Shao, E. H. Rego, M. W. Davidson, and M. G. L. Gustafsson, "Time-lapse two-color 3D imaging of live cells with doubled resolution using structured illumination," Proc. Natl. Acad. Sci. U. S. A. 109, 5311-5315 (2012). https://doi.org/10.1073/pnas.1119262109
  17. D. Li, L. Shao, B.-C. Chen, X. Zhang, M. Zhang, B. Moses, D. E. Milkie, J. R. Beach, J. A. Hammer III, M. Pasham, T. Kirchhausen, M. A. Baird, M. W. Davidson, P. Xu, and E. Betzig, "Extended-resolution structured illumination imaging of endocytic and cytoskeletal dynamics," Science 349, aab3500 (2015). https://doi.org/10.1126/science.aab3500
  18. Y. Guo, D. Li, S. Zhang, Y. Yang, J.-J. Liu, X. Wang, C. Liu, D. E. Milkie, R. P. Moore, U. S. Tulu, D. P. Kiehart, J. Hu, J. Lippincott-Schwartz, E. Betzig, and D. Li, "Visualizing intracellular organelle and cytoskeletal interactions at nanoscale resolution on millisecond timescales," Cell 175, 1430-1442.e17 (2018). https://doi.org/10.1016/j.cell.2018.09.057
  19. M. Guo, P. Chandris, J. P. Giannini, A. J. Trexler, R. Fischer, J. Chen, H. D. Vishwasrao, I. Rey-Suarez, Y. Wu, X. Wu, C. M. Waterman, G. H. Patterson, A. Upadhyaya, J. W. Taraska, and H. Shroff, "Single-shot super-resolution total internal reflection fluorescence microscopy," Nat. Methods 15, 425-428 (2018). https://doi.org/10.1038/s41592-018-0004-4
  20. A. Markwirth, M. Lachetta, V. Monkemoller, R. Heintzmann, W. Hubner, T. Huser, and M. Muller, "Video-rate multi-color structured illumination microscopy with simultaneous realtime reconstruction," Nat. Commun. 10, 4315 (2019). https://doi.org/10.1038/s41467-019-12165-x
  21. I. Kounatidis, M. L. Stanifer, M. A. Phillips, P. Paul-Gilloteaux, X. Heiligenstein, H. Wang, C. A. Okolo, T. M. Fish, M. C. Spink, D. I. Stuart, I. Davis, S. Boulant, J. M. Grimes, I. M. Dobbie, and M. Harkiolaki, "3D Correlative cryo-structured illumination fluorescence and soft X-ray microscopy elucidates reovirus intracellular release pathway," Cell 182, 515-530.e17 (2020). https://doi.org/10.1016/j.cell.2020.05.051
  22. T. Woo, S. H. Jung, C. Ahn, B. Hwang, H. Kim, J. H. Kang, and J.-H. Park, "Tunable SIM: observation at varying spatiotemporal resolutions across the FOV," Optica 7, 973-980 (2020). https://doi.org/10.1364/optica.392800
  23. E. Betzig, G. H. Patterson, R. Sougrat, O. W. Lindwasser, S. Olenych, J. S. Bonifacino, M. W. Davidson, J. Lippincott-Schwartz, and H. F. Hess, "Imaging intracellular fluorescent proteins at nanometer resolution," Science 313, 1642-1645 (2006). https://doi.org/10.1126/science.1127344
  24. A. Vaziri, J. Tang, H. Shroff, and C. V. Shank, "Multilayer three-dimensional super resolution imaging of thick biological samples," Proc. Natl. Acad. Sci. U. S. A. 105, 20221-20226 (2008). https://doi.org/10.1073/pnas.0810636105
  25. H. Shroff, C. G. Galbraith, J. A. Galbraith, and E. Betzig, "Live-cell photoactivated localization microscopy of nanoscale adhesion dynamics," Nat. Methods 5, 417-423 (2008). https://doi.org/10.1038/nmeth.1202
  26. A. G. York, A. Ghitani, A. Vaziri, M. W. Davidson, and H. Shroff, "Confined activation and subdiffractive localization enables whole-cell PALM with genetically expressed probes," Nat. Methods 8, 327-333 (2011). https://doi.org/10.1038/nmeth.1571
  27. J. Kwon, J.-S. Park, M. Kang, S. Choi, J. Park, G. T. Kim, C. Lee, S. Cha, H.-W. Rhee, and S.-H. Shim, "Bright ligand-activatable fluorescent protein for high-quality multicolor live-cell super-resolution microscopy," Nat. Commun. 11, 273 (2020). https://doi.org/10.1038/s41467-019-14067-4
  28. L. Xie, P. Dong, X. Chen, T.-H. S. Hsieh, S. Banala, M. De Marzio, B. P. English, Y. Qi, S. K. Jung, K.-R. Kieffer-Kwon, W. R. Legant, A. S. Hansen, A. Schulmann, R. Casellas, B. Zhang, E. Betzig, L. D. Lavis, H. Y. Chang, R. Tjian, and Z. Liu, "3D ATAC-PALM: super-resolution imaging of the accessible genome," Nat. Methods 17, 430-436 (2020). https://doi.org/10.1038/s41592-020-0775-2
  29. M. J. Rust, M. Bates, and X. Zhuang, "Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM)," Nat. Methods 3, 793-796 (2006). https://doi.org/10.1038/nmeth929
  30. M. Bates, B. Huang, G. T. Dempsey, and X. Zhuang, "Multicolor super-resolution imaging with photo-switchable fluorescent probes," Science 317, 1749-1753 (2007). https://doi.org/10.1126/science.1146598
  31. B. Huang, W. Wang, M. Bates, and X. Zhuang, "Three-dimensional super-resolution imaging by stochastic optical reconstruction microscopy," Science 319, 810-813 (2008). https://doi.org/10.1126/science.1153529
  32. B. Huang, S. A. Jones, B. Brandenburg, and X. Zhuang, "Whole-cell 3D STORM reveals interactions between cellular structures with nanometer-scale resolution," Nat. Methods 5, 1047-1052 (2008). https://doi.org/10.1038/nmeth.1274
  33. A. Dani, B. Huang, J. Bergan, C. Dulac, and X. Zhuang, "Superresolution imaging of chemical synapses in the brain," Neuron 68, 843-856 (2010). https://doi.org/10.1016/j.neuron.2010.11.021
  34. S.-H. Shim, C. Xia, G. Zhong, H. P. Babcock, J. C. Vaughan, B. Huang, X. Wang, C. Xu, G.-Q. Bi, and X. Zhuang, "Super-resolution fluorescence imaging of organelles in live cells with photoswitchable membrane probes," Proc. Natl. Acad. Sci. U. S. A. 109, 13978-13983 (2012). https://doi.org/10.1073/pnas.1201882109
  35. S.-H. Shim, R. A. Everley, S. P. Gygi, X. Zhuang, and D. E. Clapham, "Structurally distinct Ca2+ signaling domains of sperm flagella orchestrate tyrosine phosphorylation and motility," Cell 157, 808-822 (2014). https://doi.org/10.1016/j.cell.2014.02.056
  36. D. Kim, Z. Zhang, and K. Xu, "Spectrally resolved super-resolution microscopy unveils multipath reaction pathways of single spiropyran molecules," J. Am. Chem. Soc. 139, 9447-9450 (2017). https://doi.org/10.1021/jacs.7b04602
  37. M. Klevanski, F. Herrmannsdoerfer, S. Sass, V. Venkataramani, M. Heilemann, and T. Kuner, "Automated highly multiplexed super-resolution imaging of protein nano-architecture in cells and tissues," Nat. Commun. 11, 1552 (2020). https://doi.org/10.1038/s41467-020-15362-1
  38. S. T. Hess, T. P. K. Girirajan, and M. D. Mason, "Ultra-high resolution imaging by fluorescence photoactivation localization microscopy," Biophys. J. 91, 4258-4272 (2006). https://doi.org/10.1529/biophysj.106.091116
  39. M. F. Juette, T. J. Gould, M. D. Lessard, M. J. Mlodzianoski, B. S. Nagpure, B. T. Bennett, S. T. Hess, and J. Bewersdorf "Three-dimensional sub-100 nm resolution fluorescence microscopy of thick samples," Nat. Methods 5, 527-529 (2008). https://doi.org/10.1038/nmeth.1211
  40. C. Laplante, F. Huang, I. R. Tebbs, J. Bewersdorf, and T. D. Pollard, "Molecular organization of cytokinesis nodes and contractile rings by super-resolution fluorescence microscopy of live fission yeast," Proc. Natl. Acad. Sci. U. S. A. 113, E5876-E5885 (2016).
  41. G. Shtengel, J. A. Galbraith, C. G. Galbraith, J. LippincottSchwartz, J. M. Gillette, S. Manley, R. Sougrat, C. M. Waterman, P. Kanchanawong, M. W. Davidson, R. D. Fetter, and H. F. Hess, "Interferometric fluorescent super-resolution microscopy resolves 3D cellular ultrastructure," Proc. Natl. Acad. Sci. U. S. A. 106, 3125-3130 (2009). https://doi.org/10.1073/pnas.0813131106
  42. P. Kanchanawong, G. Shtengel, A. M. Pasapera, E. B. Ramko, M. W. Davidson, H. F. Hess, and C. M. Waterman, "Nanoscale architecture of integrin-based cell adhesions," Nature 468, 580-584 (2010). https://doi.org/10.1038/nature09621
  43. D. Aquino, A. Schonle, C. Geisler, C. V. Middendorff, C. A. Wurm, Y. Okamura, T. Lang, S. W. Hell, and A. Egner, "Two-color nanoscopy of three-dimensional volumes by 4Pi detection of stochastically switched fluorophores," Nat. Methods 8, 353-359 (2011). https://doi.org/10.1038/nmeth.1583
  44. M. Bossi, J. Folling, M. Dyba, V. Westphal, and S. W. Hell, "Breaking the diffraction resolution barrier in far-field microscopy by molecular optical bistability," New J. Phys. 8, 275 (2006). https://doi.org/10.1088/1367-2630/8/11/275
  45. A. Chmyrov, J. Keller, T. Grotjohann, M. Ratz, E. d'Este, S. Jakobs, C. Eggeling, and S. W. Hell, "Nanoscopy with more than 100,000 'doughnuts'," Nat. Methods 10, 737-740 (2013). https://doi.org/10.1038/nmeth.2556
  46. D. K. Tiwari, Y. Arai, M. Yamanaka, T. Matsuda, M. Agetsuma, M. Nakano, K. Fujita, and T. Nagai, "A fast- and positively photoswitchable fluorescent protein for ultralow-laser-power RESOLFT nanoscopy," Nat. Methods 12, 515-518 (2015). https://doi.org/10.1038/nmeth.3362
  47. U. Bohm, S. W. Hell, and R. Schmidt, "4Pi-RESOLFT nanoscopy," Nat. Commun. 7, 10504 (2016). https://doi.org/10.1038/ncomms10504
  48. L. A. Masullo, A. Boden, F. Pennacchietti, G. Coceano, M. Ratz, and I. Testa, "Enhanced photon collection enables four dimensional fluorescence nanoscopy of living systems," Nat. Commun. 9, 3281 (2018). https://doi.org/10.1038/s41467-018-05799-w
  49. T. Dertinger, R. Colyer, G. Iyer, S. Weiss, and J. Enderlein, "Fast, background-free, 3D super-resolution optical fluctuation imaging (SOFI)," Proc. Natl. Acad. Sci. U. S. A. 106, 22287-22292 (2009). https://doi.org/10.1073/pnas.0907866106
  50. S. Geissbuehler, A. Sharipov, A. Godinat, N. L. Bocchio, P. A. Sandoz, A. Huss, N. A. Jensen, S. Jakobs, J. Enderlein, F. G. van der Goot, E. A. Dubikovskaya, T. Lasser, and M. Leutenegger, "Live-cell multiplane three-dimensional super-resolution optical fluctuation imaging," Nat. Commun. 5, 5830 (2014). https://doi.org/10.1038/ncomms6830
  51. H. Deschout, T. Lukes, A. Sharipov, D. Szlag, L. Feletti, W. Vandenberg, P. Dedecker, J. Hofkens, M. Leutenegger, T. Lasser, and A. Radenovic, "Complementarity of PALM and SOFI for super-resolution live-cell imaging of focal adhesions," Nat. Commun. 7, 13693 (2016). https://doi.org/10.1038/ncomms13693
  52. T. Lukes, D. Glatzova, Z. Kvicalova, F. Levet, A. Benda, S. Letschert, M. Sauer, T. Brdicka, T. Lasser, and M. Cebecauer, "Quantifying protein densities on cell membranes using super-resolution optical fluctuation imaging," Nat. Commun. 8, 1731 (2017). https://doi.org/10.1038/s41467-017-01857-x
  53. F. Moser, V. Prazak, V. Mordhorst, D. M. Andrade, L. A. Baker, C. Hagen, K. Grunewald, and R. Kaufmann, "Cryo-SOFI enabling low-dose super-resolution correlative light and electron cryo-microscopy," Proc. Natl. Acad. Sci. U. S. A. 116, 4804-4809 (2019). https://doi.org/10.1073/pnas.1810690116
  54. K. S. Grussmayer, S. Geissbuehler, A. Descloux, T. Lukes, M. Leutenegger, A. Radenovic, and T. Lasser, "Spectral cross-cumulants for multicolor super-resolved SOFI imaging," Nat. Commun. 11, 3023 (2020). https://doi.org/10.1038/s41467-020-16841-1
  55. R. Jungmann, C. Steinhauer, M. Scheible, A. Kuzyk, P. Tinnefeld, and F. C. Simmel, "Single-molecule kinetics and super-resolution microscopy by fluorescence imaging of transient binding on DNA Origami," Nano Lett. 10, 4756-4761 (2010). https://doi.org/10.1021/nl103427w
  56. R. Jungmann, M. S. Avendano, J. B. Woehrstein, M. Dai, W. M. Shih, and P. Yin, "Multiplexed 3D cellular super-resolution imaging with DNA-PAINT and Exchange-PAINT," Nat. Methods 11, 313-318 (2014). https://doi.org/10.1038/nmeth.2835
  57. S. Strauss, P. C. Nickels, M. T. Strauss, V. J. Sabinina, J. Ellenberg, J. D. Carter, S. Gupta, N. Janjic, and R. Jungmann, "Modified aptamers enable quantitative sub-10-nm cellular DNA-PAINT imaging," Nat. Methods 15, 685-688 (2018). https://doi.org/10.1038/s41592-018-0105-0
  58. F. Schueder, J. Stein, F. Stehr, A. Auer, B. Sperl, M. T. Strauss, P. Schwille, and R. Jungmann, "An order of magnitude faster DNA-PAINT imaging by optimized sequence design and buffer conditions," Nat. Methods 16, 1101-1104 (2019). https://doi.org/10.1038/s41592-019-0584-7
  59. N. Liu, M. Dai, S. K. Saka, and P. Yin, "Super-resolution labelling with Action-PAINT," Nat. Chem. 11, 1001-1008 (2019). https://doi.org/10.1038/s41557-019-0325-7
  60. A. Archetti, E. Glushkov, C. Sieben, A. Stroganov, A. Radenovic, and S. Manley, "Waveguide-PAINT offers an open platform for large field-of-view super-resolution imaging," Nat. Commun. 10, 1267 (2019). https://doi.org/10.1038/s41467-019-09247-1
  61. J. M. Brockman, H. Su, A. T. Blanchard, Y. Duan, T. Meyer, M. E. Quach, R. Glazier, A. Bazrafshan, R. L. Bender, A. V. Kellner, H. Ogasawara, R. Ma, F. Schueder, B. G. Petrich, R. Jungmann, R. Li, A. L. Mattheyses, Y. Ke, and K. Salaita, "Live-cell super-resolved PAINT imaging of piconewton cellular traction forces," Nat. Methods 17, 1018-1024 (2020). https://doi.org/10.1038/s41592-020-0929-2
  62. J. Lee, S. Park, W. Kang, and S. Hohng, "Accelerated super-resolution imaging with FRET-PAINT," Mol. Brain 10, 63 (2017). https://doi.org/10.1186/s13041-017-0344-5
  63. A. Auer, M. T. Strauss, T. Schlichthaerle, and R. Jungmann, "Fast, background-free DNA-PAINT imaging using FRET-based probes," Nano Lett. 17, 6428-6434 (2017). https://doi.org/10.1021/acs.nanolett.7b03425
  64. J. Lee, S. Park, and S. Hohng, "Accelerated FRET-PAINT microscopy," Mol. Brain 11, 70 (2018). https://doi.org/10.1186/s13041-018-0414-3
  65. N. S. Deussner-Helfmann, A. Auer, M. T. Strauss, S. Malkusch, M. S. Dietz, H.-D. Barth, R. Jungmann, and M. Heilemann, "Correlative Single-Molecule FRET and DNA-PAINT Imaging," Nano Lett. 18, 4626-4630 (2018). https://doi.org/10.1021/acs.nanolett.8b02185
  66. D. Sage, T.-A. Pham, H. Babcock, T. Lukes, T. Pengo, J. Chao, R. Velmurugan, A. Herbert, A. Agrawal, S. Colabrese, A. Wheeler, A. Archetti, B. Rieger, R. Ober, G. M. Hagen, J.-B. Sibarita, J. Ries, R. Henriques, M. Unser, and S. Holden, "Super-resolution fight club: assessment of 2D and 3D single-molecule localization microscopy software," Nat. Methods 16, 387-395 (2019). https://doi.org/10.1038/s41592-019-0364-4
  67. S. Culley, D. Albrecht, C. Jacobs, P. M. Pereira, C. Leterrier, J. Mercer, and R. Henriques, "Quantitative mapping and minimization of super-resolution optical imaging artifacts," Nat. Methods 15, 263-266 (2018). https://doi.org/10.1038/nmeth.4605
  68. R. J. Marsh, K. Pfisterer, P. Bennett, L. M. Hirvonen, M. Gautel, G. E. Jones, and S. Cox, "Artifact-free high-density localization microscopy analysis," Nat. Methods 15, 689-692 (2018). https://doi.org/10.1038/s41592-018-0072-5
  69. L. Barna, B. Dudok, V. Miczan, A. Horvath, Z. I Laszlo, and I. Katona, "Correlated confocal and super-resolution imaging by VividSTORM," Nat. Protoc. 11, 163-183 (2016). https://doi.org/10.1038/nprot.2016.002
  70. P. Bon, J. Linares-Loyez, M. Feyeux, K. Alessandri, B. Lounis, P. Nassoy, and L. Cognet, "Self-interference 3D super-resolution microscopy for deep tissue investigations," Nat. Methods 15, 449-454 (2018). https://doi.org/10.1038/s41592-018-0005-3
  71. C. Sieben, N. Banterle, K. M. Douglass, P. Gonczy, and S. Manley, "Multicolor single-particle reconstruction of protein complexes," Nat. Methods 15, 777-780 (2018). https://doi.org/10.1038/s41592-018-0140-x
  72. Y. Li, M. Mund, P. Hoess, J. Deschamps, U. Matti, B. Nijmeijer, V. J. Sabinina, J. Ellenberg, I. Schoen, and J. Ries, "Real-time 3D single-molecule localization using experimental point spread functions," Nat. Methods 15, 367-369 (2018). https://doi.org/10.1038/nmeth.4661
  73. C.-H. Lu, W.-C. Tang, Y.-T. Liu, S.-W. Chang, F. C. M. Wu, C.-Y. Chen, Y.-C. Tsai, S.-M. Yang, C.-W. Kuo, Y. Okada, Y.-K. Hwu, P. Chen, and B.-C. Chen, "Lightsheet localization microscopy enables fast, large-scale, and three-dimensional super-resolution imaging," Commun. Biol. 2, 177 (2019). https://doi.org/10.1038/s42003-019-0403-9
  74. M. Pascucci, S. Ganesan, A. Tripathi, O. Katz, V. Emiliani, and M. Guillon, "Compressive three-dimensional super-resolution microscopy with speckle-saturated fluorescence excitation," Nat. Commun. 10, 1327 (2019). https://doi.org/10.1038/s41467-019-09297-5
  75. C. Cabriel, N. Bourg, P. Jouchet, G. Dupuis, C. Leterrier, A. Baron, M.-A. Badet-Denisot, B. Vauzeilles, E. Fort, and S. Leveque-Fort, "Combining 3D single molecule localization strategies for reproducible bioimaging," Nat. Commun. 10, 1980 (2019). https://doi.org/10.1038/s41467-019-09901-8
  76. F. Xu, D. Ma, K. P. MacPherson, S. Liu, Y. Bu, Y. Wang, Y. Tang, C. Bi, T. Kwok, A. A. Chubykin, P. Yin, S. Calve, G. E. Landreth, and F. Huang, "Three-dimensional nanoscopy of whole cells and tissues with in situ point spread function retrieval," Nat. Methods 17, 531-540 (2020). https://doi.org/10.1038/s41592-020-0816-x
  77. Y. Zhang, L. K. Schroeder, M. D. Lessard, P. Kidd, J. Chung, Y. Song, L. Benedetti, Y. Li, J. Ries, J. B. Grimm, L. D. Lavis, P. De Camilli, J. E. Rothman, D. Baddeley, and J. Bewersdorf, "Nanoscale subcellular architecture revealed by multicolor three-dimensional salvaged fluorescence imaging," Nat. Methods 17, 225-231 (2020). https://doi.org/10.1038/s41592-019-0676-4
  78. V. Curcio, L. A. Aleman-Castaneda, T. G. Brown, S. Brasselet, and M. A. Alonso, "Birefringent Fourier filtering for single molecule coordinate and height super-resolution imaging with dithering and orientation," Nat. Commun. 11, 5307 (2020). https://doi.org/10.1038/s41467-020-19064-6
  79. R. E. Thompson, D. R. Larson, and W. W. Webb, "Precise nanometer localization analysis for individual fluorescent probes," Biophys. J. 82, 2775-2783 (2002). https://doi.org/10.1016/S0006-3495(02)75618-X
  80. M. Tokunaga, N. Imamoto, and K. Sakata-Sogawa, "Highly inclined thin illumination enables clear single-molecule imaging in cells," Nat. Methods 5, 159-161 (2008). https://doi.org/10.1038/nmeth1171
  81. B.-C. Chen, W. R. Legant, K. Wang, L. Shao, D. E. Milkie, M. W. Davidson, C. Janetopoulos, X. S. Wu, J. A. Hammer III, Z. Liu, B. P. English, Y. Mimori-Kiyosue, D. P. Romero, A. T. Ritter, J. Lippincott-Schwartz, L. Fritz-Laylin, R. D. Mullins, D. M. Mitchell, J. N. Bembenek, A.-C. Reymann, R. Bohme, S. W. Grill, J. T. Wang, G. Seydoux, U. S. Tulu, D. P. Kiehart, and E. Betzig, "Lattice light-sheet microscopy: Imaging molecules to embryos at high spatiotemporal resolution," Science 346, 1257998 (2014). https://doi.org/10.1126/science.1257998
  82. W. R. Legant, L. Shao, J. B. Grimm, T. A. Brown, D. E. Milkie, B. B. Avants, L. D. Lavis, and E. Betzig, "High-density three-dimensional localization microscopy across large volumes," Nat. Methods 13, 359-365 (2016). https://doi.org/10.1038/nmeth.3797
  83. B. Yang, X. Chen, Y. Wang, S. Feng, V. Pessino, N. Stuurman, N. H. Cho, K. W. Cheng, S. J. Lord, L. Xu, D. Xie, R. D. Mullins, M. D. Leonetti, and B. Huang, "Epi-illumination SPIM for volumetric imaging with high spatial-temporal resolution," Nat. Methods 16, 501-504 (2019). https://doi.org/10.1038/s41592-019-0401-3
  84. S. Jia, J. C. Vaughan, and X. Zhuang, "Isotropic three-dimensional super-resolution imaging with a self-bending point spread function," Nat. Photonics 8, 302-306 (2014). https://doi.org/10.1038/nphoton.2014.13
  85. F. Schueder, J. Lara-Gutierrez, B. J. Beliveau, S. K. Saka, H. M. Sasaki, J. B. Woehrstein, M. T. Strauss, H. Grabmayr, P. Yin, and R. Jungmann, "Multiplexed 3D super-resolution imaging of whole cells using spinning disk confocal microscopy and DNA-PAINT," Nat. Commun. 8, 2090 (2017). https://doi.org/10.1038/s41467-017-02028-8
  86. E. Nehme, D. Freedman, R. Gordon, B. Ferdman, L. E. Weiss, O. Alalouf, T. Naor, R. Orange, T. Michaeli, and Y. Shechtman, "DeepSTORM3D: dense 3D localization microscopy and PSF design by deep learning," Nat. Methods 17, 734-740 (2020). https://doi.org/10.1038/s41592-020-0853-5
  87. A. Aristov, B. Lelandais, E. Rensen, and C. Zimmer, "ZOLA3D allows flexible 3D localization microscopy over an adjustable axial range," Nat. Commun. 9, 2409 (2018). https://doi.org/10.1038/s41467-018-04709-4
  88. J. Lee, Y. Miyanaga, M. Ueda, and S. Hohng, "Video-rate confocal microscopy for single-molecule imaging in live cells and superresolution fluorescence imaging," Biophys. J. 103, 1691-1697 (2012). https://doi.org/10.1016/j.bpj.2012.09.014
  89. Y. Wu, X. Han, Y. Su, M. Glidewell, J. S. Daniels, J. Liu, T. Sengupta, I. Rey-Suarez, R. Fischer, A. Patel, C. Combs, J. Sun, X. Wu, R. Christensen, C. Smith, L. Bao, Y. Sun, L. H. Duncan, J. Chen, Y. Pommier, Y.-B. Shi, E. Murphy, S. Roy, A. Upadhyaya, D. Colon-Ramos, P. La Riviere, and H. Shroff, "Multiview confocal super-resolution microscopy," Nature 600, 279-284 (2021). https://doi.org/10.1038/s41586-021-04110-0
  90. S. Park, W. Kang, Y.-D. Kwon, J. Shim, S. Kim, B.-K. Kaang, and S. Hohng, "Superresolution fluorescence microscopy for 3D reconstruction of thick samples," Mol. Brain 11, 17 (2018). https://doi.org/10.1186/s13041-018-0361-z
  91. A.-K. Gustavsson, P. N. Petrov, M. Y. Lee, Y. Shechtman, W. E. Moerner, "3D single-molecule super-resolution microscopy with a tilted light sheet," Nat. Commun. 9, 123 (2018). https://doi.org/10.1038/s41467-017-02563-4
  92. N. Ji, D. E. Milkie, and E. Betzig, "Adaptive optics via pupil segmentation for high-resolution imaging in biological tissues," Nat. Methods 7, 141-147 (2010). https://doi.org/10.1038/nmeth.1411
  93. N. Ji, "Adaptive optical fluorescence microscopy," Nat. Methods 14, 374-380 (2017). https://doi.org/10.1038/nmeth.4218
  94. S. Yoon, M. Kim, M. Jang, Y. Choi, W. Choi, S. Kang, and W. Choi, "Deep optical imaging within complex scattering media," Nat. Rev. Phys. 2, 141-158 (2020). https://doi.org/10.1038/s42254-019-0143-2
  95. F. Huang, G. Sirinakis, E. S. Allgeyer, L. K. Schroeder, W. C. Duim, B. Kromann, T. Phan, F. E. Rivera-Molina, J. R. Myers, I. Irnov, M. Lessard, Y. Zhang, M. A. Handel, C. JacobsWagner, C. P. Lusk, J. E. Rothman, D. Toomre, M. J. Booth, and J. Bewersdorf, "Ultra-High resolution 3D imaging of whole cells," Cell 166, 1028-1040 (2016). https://doi.org/10.1016/j.cell.2016.06.016
  96. M. J. Mlodzianoski, P. J. Cheng-Hathaway, S. M. Bemiller, T. J. McCray, S. Liu, D. A. Miller, B. T. Lamb, G. E. Landreth, and F. Huang, "Active PSF shaping and adaptive optics enable volumetric localization microscopy through brain sections," Nat. Methods 15, 583-586 (2018). https://doi.org/10.1038/s41592-018-0053-8
  97. Y. M. Sigal, C. M. Speer, H. P. Babcock, X. Zhuang, "Mapping synaptic input fields of neurons with super-resolution imaging," Cell 163, 493-505 (2015). https://doi.org/10.1016/j.cell.2015.08.033
  98. B. R. Patton, D. Burke, D. Owald, T. J. Gould, J. Bewersdorf, and M. J. Booth, "Three-dimensional STED microscopy of aberrating tissue using dual adaptive optics," Opt. Express 24, 8862-8876 (2016). https://doi.org/10.1364/OE.24.008862
  99. J. Antonello, A. Barbotin, E. Z. Chong, J. Rittscher, and M. J. Booth, "Multi-scale sensorless adaptive optics: application to stimulated emission depletion microscopy," Opt. Express 28, 16749-16763 (2020). https://doi.org/10.1364/oe.393363
  100. M. Zurauskas, I. M. Dobbie, R. M. Parton, M. A. Phillips, A. Gohler, I. Davis, and M. J. Booth, "IsoSense: frequency enhanced sensorless adaptive optics through structured illumination," Optica 6, 370-379 (2019). https://doi.org/10.1364/optica.6.000370
  101. R. Turcotte, Y. Liang, M. Tanimoto, Q. Zhang, Z. Li, M. Koyama, E. Betzig, and N. Ji, "Dynamic super-resolution structured illumination imaging in the living brain," Proc. Natl. Acad. Sci. U. S. A. 116, 9586-9591 (2019). https://doi.org/10.1073/pnas.1819965116
  102. Z. Li, Q. Zhang, S.-W. Chou, Z. Newman, R. Turcotte, R. Natan, Q. Dai, E. Y. Isacoff, and N. Ji, "Fast widefield imaging of neuronal structure and function with optical sectioning in vivo," Sci. Adv. 6, eaaz3870 (2020). https://doi.org/10.1126/sciadv.aaz3870
  103. R. Lin, E. T. Kipreos, J. Zhu, C. H. Khang, and P. Kner, "Subcellular three-dimensional imaging deep through multicellular thick samples by structured illumination microscopy and adaptive optics," Nat. Commun. 12, 3148 (2021). https://doi.org/10.1038/s41467-021-23449-6
  104. Y. Chen, W. Liu, Z. Zhang, C. Zheng, Y. Huang, R. Cao, D. Zhu, L. Xu, M. Zhang, Y.-H. Zhang, J. Fan, L. Jin, Y. Xu, C. Kuang, and X. Liu, "Multi-color live-cell super-resolution volume imaging with multi-angle interference microscopy," Nat. Commun. 9, 4818 (2018). https://doi.org/10.1038/s41467-018-07244-4
  105. J. Kim, M. Wojcik, Y. Wang, S. Moon, E. A. Zin, N. Marnani, Z. L. Newman, J. G. Flannery, K. Xu, and X. Zhang, "Oblique-plane single-molecule localization microscopy for tissues and small intact animals," Nat. Methods 16, 853-857 (2019). https://doi.org/10.1038/s41592-019-0510-z
  106. D. Mahecic, D. Gambarotto, K. M. Douglass, D. Fortun, N. Banterle, K. A. Ibrahim, M. Le Guennec, P. Gonczy, V. Hamel, P. Guichard, and S. Manley, "Homogeneous multifocal excitation for high-throughput super-resolution imaging," Nat. Methods 17, 726-733 (2020). https://doi.org/10.1038/s41592-020-0859-z
  107. S. Liu and F. Huang, "Enhanced 4Pi single-molecule localization microscopy with coherent pupil based localization," Commun. Biol. 3, 220 (2020). https://doi.org/10.1038/s42003-020-0908-2
  108. S. Liu, H. Huh, S.-H. Lee, and F. Huang, "Three-dimensional single-molecule localization microscopy in whole-cell and tissue specimens," Annu. Rev. Biomed. Eng. 22, 155-184 (2020). https://doi.org/10.1146/annurev-bioeng-060418-052203
  109. M. G. M. Velasco, M. Zhang, J. Antonello, P. Yuan, E. S. Allgeyer, D. May, O. M'Saad, P. Kidd, A. E. S. Barentine, V. Greco, J. Grutzendler, M. J. Booth, and J. Bewersdorf, "3D super-resolution deep-tissue imaging in living mice," Optica 8, 442-450 (2021). https://doi.org/10.1364/OPTICA.416841
  110. F. Balzarotti, Y. Eilers, K. C. Gwosch, A. H. Gynna, V. Westphal, F. D. Stefani, J. Elf, and S. W. Hell, "Nanometer resolution imaging and tracking of fluorescent molecules with minimal photon fluxes," Science 355, 606-612 (2017). https://doi.org/10.1126/science.aak9913
  111. K. C. Gwosch, J. K. Pape, F. Balzarotti, P. Hoess, J. Ellenberg, J. Ries, and S. W. Hell, "MINFLUX nanoscopy delivers 3D multicolor nanometer resolution in cells," Nat. Methods 17, 217-224 (2020). https://doi.org/10.1038/s41592-019-0688-0
  112. J. Cnossen, T. Hinsdale, R. O. Thorsen, M. Siemons, F. Schueder, R. Jungmann, C. S. Smith, B. Rieger, and S. Stallinga, "Localization microscopy at doubled precision with patterned illumination," Nat. Methods 17, 59-63 (2020). https://doi.org/10.1038/s41592-019-0657-7
  113. Z. Fu, D. Peng, M. Zhang, F. Xue, R. Zhang, W. He, T. Xu, and P. Xu, "mEosEM withstands osmium staining and Epon embedding for super-resolution CLEM," Nat. Methods 17, 55-58 (2020). https://doi.org/10.1038/s41592-019-0613-6
  114. D. P. Hoffman, G. Shtengel, C. S. Xu, K. R. Campbell, M. Freeman, L. Wang, D. E. Milkie, H. A. Pasolli, N. Iyer, J. A. Bogovic, D. R. Stabley, A. Shirinifard, S. Pang, D. Peale, K. Schaefer, W. Pomp, C.-L. Chang, J. Lippincott-Schwartz, T. Kirchhausen, D. J. Solecki, E. Betzig, and H. F. Hess, "Correlative three-dimensional super-resolution and block-face electron microscopy of whole vitreously frozen cells," Science 367, eaaz5357 (2020). https://doi.org/10.1126/science.aaz5357
  115. M. Filius, T. J. Cui, A. N. Ananth, M. W. Docter, J. W. Hegge, J. van der Oost, and C. Joo, "High-speed super-resolution imaging using protein-assisted DNA-PAINT," Nano Lett. 20, 2264-2270 (2020). https://doi.org/10.1021/acs.nanolett.9b04277
  116. S. Strauss and R. Jungmann, "Up to 100-fold speed-up and multiplexing in optimized DNA-PAINT," Nat. Methods 17, 789-791 (2020). https://doi.org/10.1038/s41592-020-0869-x
  117. M. Weigert, U. Schmidt, T. Boothe, A. Muller, A. Dibrov, A. Jain, B. Wilhelm, D. Schmidt, C. Broaddus, S. Culley, M. Rocha-Martins, F. Segovia-Miranda, C. Norden, R. Henriques, M. Zerial, M. Solimena, J. Rink, P. Tomancak, L. Royer, F. Jug, and E. W. Myers, "Content-aware image restoration: pushing the limits of fluorescence microscopy," Nat. Methods 15, 1090-1097 (2018). https://doi.org/10.1038/s41592-018-0216-7
  118. W. Ouyang, A. Aristov, M. Lelek, X. Hao, and C. Zimmer, "Deep learning massively accelerates super-resolution localization microscopy," Nat. Biotechnol. 36, 460-468 (2018). https://doi.org/10.1038/nbt.4106
  119. E. Nehme, L. E. Weiss, T. Michaeli, and Y. Shechtman, "Deep-STORM: super-resolution single-molecule microscopy by deep learning," Optica 5, 458-464 (2018). https://doi.org/10.1364/optica.5.000458
  120. P. Zhang, S. Liu, A. Chaurasia, D. Ma, M. J. Mlodzianoski, E. Culurciello, and F. Huang, "Analyzing complex single-molecule emission patterns with deep learning," Nat. Methods 15, 913-916 (2018). https://doi.org/10.1038/s41592-018-0153-5
  121. H. Wang, Y. Rivenson, Y. Jin, Z. Wei, R. Gao, H. Gunaydin, L. A. Bentolila, C. Kural, and A. Ozcan, "Deep learning enables cross-modality super-resolution in fluorescence microscopy," Nat. Methods 16, 103-110 (2019). https://doi.org/10.1038/s41592-018-0239-0
  122. L. von Chamier, R. F. Laine, and R. Henriques, "Artificial intelligence for microscopy: what you should know," Biochem. Soc. Trans. 47, 1029-1040 (2019). https://doi.org/10.1042/bst20180391
  123. T. Kim, S. Moon, and K. Xu, "Information-rich localization microscopy through machine learning," Nat. Commun. 10, 1996 (2019). https://doi.org/10.1038/s41467-019-10036-z
  124. C. Belthangady and L. A. Royer, "Applications, promises, and pitfalls of deep learning for fluorescence image reconstruction," Nat. Methods 16, 1215-1225 (2019). https://doi.org/10.1038/s41592-019-0458-z
  125. L. Jin, B. Liu, F. Zhao, S. Hahn, B. Dong, R. Song, T. C. Elston, Y. Xu, and K. M. Hahn, "Deep learning enables structured illumination microscopy with low light levels and enhanced speed," Nat. Commun. 11, 1934 (2020). https://doi.org/10.1038/s41467-020-15784-x
  126. P. Padmanabhan, A. Kneynsberg, and J. Gotz, "Super-resolution microscopy: a closer look at synaptic dysfunction in Alzheimer disease," Nat. Rev. Neurosci. 22, 723-740 (2021). https://doi.org/10.1038/s41583-021-00531-y