1932

Abstract

Super-resolution microscopy techniques, and specifically single-molecule localization microscopy (SMLM), are approaching nanometer resolution inside cells and thus have great potential to complement structural biology techniques such as electron microscopy for structural cell biology. In this review, we introduce the different flavors of super-resolution microscopy, with a special emphasis on SMLM and MINFLUX (minimal photon flux). We summarize recent technical developments that pushed these localization-based techniques to structural scales and review the experimental conditions that are key to obtaining data of the highest quality. Furthermore, we give an overview of different analysis methods and highlight studies that used SMLM to gain structural insights into biologically relevant molecular machines. Ultimately, we give our perspective on what is needed to push the resolution of these techniques even further and to apply them to investigating dynamic structural rearrangements in living cells.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-biophys-102521-112912
2022-05-09
2024-06-24
Loading full text...

Full text loading...

/deliver/fulltext/biophys/51/1/annurev-biophys-102521-112912.html?itemId=/content/journals/10.1146/annurev-biophys-102521-112912&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Altman RB, Terry DS, Zhou Z, Zheng Q, Geggier P et al. 2012. Cyanine fluorophore derivatives with enhanced photostability. Nat. Methods 9:68–71
    [Google Scholar]
  2. 2.
    Annibale P, Vanni S, Scarselli M, Rothlisberger U, Radenovic A 2011. Quantitative photo activated localization microscopy: unraveling the effects of photoblinking. PLOS ONE 6:7e22678
    [Google Scholar]
  3. 3.
    Aquino D, Schönle A, Geisler C, von Middendorff C, Wurm CA et al. 2011. Two-color nanoscopy of three-dimensional volumes by 4Pi detection of stochastically switched fluorophores. Nat. Methods 8:4353–59
    [Google Scholar]
  4. 4.
    Babcock HP, Zhuang X. 2017. Analyzing single molecule localization microscopy data using cubic splines. Sci. Rep. 7:552
    [Google Scholar]
  5. 5.
    Balinovic A, Albrecht D, Endesfelder U 2019. Spectrally red-shifted fluorescent fiducial markers for optimal drift correction in localization microscopy. J. Phys. D 52:204002
    [Google Scholar]
  6. 6.
    Balzarotti F, Eilers Y, Gwosch KC, Gynnå AH, Westphal V et al. 2017. Nanometer resolution imaging and tracking of fluorescent molecules with minimal photon fluxes. Science 355:6325606–12
    [Google Scholar]
  7. 7.
    Barasoain I, Díaz JF, Andreu JM. 2010. Fluorescent taxoid probes for microtubule research. Methods Cell Biol 95:353–72
    [Google Scholar]
  8. 8.
    Barentine AES, Lin Y, Liu M, Kidd P, Balduf L et al. 2019. 3D multicolor nanoscopy at 10,000 cells a day. bioRxiv 606954. https://doi.org/10.1101/606954
    [Crossref]
  9. 9.
    Bates M, Huang B, Dempsey GT, Zhuang X. 2007. Multicolor super-resolution imaging with photo-switchable fluorescent probes. Science 317:58451749–53
    [Google Scholar]
  10. 10.
    Beghin A, Kechkar A, Butler C, Levet F, Cabillic M et al. 2017. Localization-based super-resolution imaging meets high-content screening. Nat. Methods 14:121184–90
    [Google Scholar]
  11. 11.
    Beliu G, Kurz AJ, Kuhlemann AC, Behringer-Pliess L, Meub M et al. 2019. Bioorthogonal labeling with tetrazine-dyes for super-resolution microscopy. Commun. Biol. 2:261
    [Google Scholar]
  12. 12.
    Benesch RE, Benesch R. 1953. Enzymatic removal of oxygen for polarography and related methods. Science 118:3068447–48
    [Google Scholar]
  13. 13.
    Betzig E, Patterson GH, Sougrat R, Lindwasser OW, Olenych S et al. 2006. Imaging intracellular fluorescent proteins at nanometer resolution. Science 313:57931642–45
    [Google Scholar]
  14. 14.
    Bock H, Geisler C, Wurm CA, von Middendorff C, Jakobs S et al. 2007. Two-color far-field fluorescence nanoscopy based on photoswitchable emitters. Appl. Phys. B 88:2161–65
    [Google Scholar]
  15. 15.
    Bon P, Bourg N, Lécart S, Monneret S, Fort E et al. 2015. Three-dimensional nanometre localization of nanoparticles to enhance super-resolution microscopy. Nat. Commun. 6:7764
    [Google Scholar]
  16. 16.
    Bon P, Linarès-Loyez J, Feyeux M, Alessandri K, Lounis B et al. 2018. Self-interference 3D super-resolution microscopy for deep tissue investigations. Nat. Methods 15:6449–54
    [Google Scholar]
  17. 17.
    Bornens M. 2012. The centrosome in cells and organisms. Science 335:6067422–26
    [Google Scholar]
  18. 18.
    Bossi M, Fölling J, Belov VN, Boyarskiy VP, Medda R et al. 2008. Multicolor far-field fluorescence nanoscopy through isolated detection of distinct molecular species. Nano Lett 8:82463–68
    [Google Scholar]
  19. 19.
    Bourg N, Mayet C, Dupuis G, Barroca T, Bon P et al. 2015. Direct optical nanoscopy with axially localized detection. Nat. Photon. 9:9587–93
    [Google Scholar]
  20. 20.
    Bowler M, Kong D, Sun S, Nanjundappa R, Evans L et al. 2019. High-resolution characterization of centriole distal appendage morphology and dynamics by correlative STORM and electron microscopy. Nat. Commun. 10:993
    [Google Scholar]
  21. 21.
    Briggs JA. 2013. Structural biology in situ—the potential of subtomogram averaging. Curr. Opin. Struct. Biol. 23:2261–67
    [Google Scholar]
  22. 22.
    Broeken J, Johnson H, Lidke DS, Liu S, Nieuwenhuizen RPJ et al. 2015. Resolution improvement by 3D particle averaging in localization microscopy. Methods Appl. Fluoresc. 3:1014003
    [Google Scholar]
  23. 23.
    Carrington G, Tomlinson D, Peckham M. 2019. Exploiting nanobodies and affimers for superresolution imaging in light microscopy. Mol. Biol. Cell 30:222737–40
    [Google Scholar]
  24. 24.
    Cheng Y, Grigorieff N, Penczek PA, Walz T. 2015. A primer to single-particle cryo-electron microscopy. Cell 161:3438–49
    [Google Scholar]
  25. 25.
    Cnossen J, Cui TJ, Joo C, Smith C 2021. Drift correction in localization microscopy using entropy minimization. Opt. Express 29:1827961–74
    [Google Scholar]
  26. 26.
    Cnossen J, Hinsdale T, Thorsen , Siemons M, Schueder F et al. 2020. Localization microscopy at doubled precision with patterned illumination. Nat. Methods 17:59–63
    [Google Scholar]
  27. 27.
    Coelho S, Baek J, Graus MS, Halstead JM, Nicovich PR et al. 2020. Ultraprecise single-molecule localization microscopy enables in situ distance measurements in intact cells. Sci. Adv. 6:16eaay8271
    [Google Scholar]
  28. 28.
    Coelho S, Baek J, Walsh J, Gooding JJ, Gaus K. 2021. 3D active stabilization for single-molecule imaging. Nat. Protoc. 16:497–515
    [Google Scholar]
  29. 29.
    Dahlberg PD, Moerner WE. 2021. Cryogenic super-resolution fluorescence and electron microscopy correlated at the nanoscale. Annu. Rev. Phys. Chem. 72:253–78
    [Google Scholar]
  30. 30.
    Dasgupta A, Deschamps J, Matti U, Hübner U, Becker J et al. 2021. Direct supercritical angle localization microscopy for nanometer 3D superresolution. Nat. Commun. 12:1180
    [Google Scholar]
  31. 31.
    Dempsey GT, Vaughan JC, Chen KH, Bates M, Zhuang X. 2011. Evaluation of fluorophores for optimal performance in localization-based super-resolution imaging. Nat. Methods 8:121027–36
    [Google Scholar]
  32. 32.
    Deschamps J, Mund M, Ries J. 2014. 3D superresolution microscopy by supercritical angle detection. Opt. Express 22:2329081–91
    [Google Scholar]
  33. 33.
    Deschamps J, Rowald A, Ries J 2016. Efficient homogeneous illumination and optical sectioning for quantitative single-molecule localization microscopy. Opt. Express 24:2428080–90
    [Google Scholar]
  34. 34.
    Diekmann R, Kahnwald M, Schoenit A, Deschamps J, Matti U, Ries J 2020. Optimizing imaging speed and excitation intensity for single-molecule localization microscopy. Nat. Methods 17:9909–12
    [Google Scholar]
  35. 35.
    Douglass KM, Sieben C, Archetti A, Lambert A, Manley S 2016. Super-resolution imaging of multiple cells by optimized flat-field epi-illumination. Nat. Photon. 10:11705–8
    [Google Scholar]
  36. 36.
    Durisic N, Laparra-Cuervo L, Sandoval-Álvarez Á, Borbely JS, Lakadamyali M. 2014. Single-molecule evaluation of fluorescent protein photoactivation efficiency using an in vivo nanotemplate. Nat. Methods 11:2156–62
    [Google Scholar]
  37. 37.
    Eilers Y, Ta H, Gwosch KC, Balzarotti F, Hell SW. 2018. MINFLUX monitors rapid molecular jumps with superior spatiotemporal resolution. PNAS 115:246117–22
    [Google Scholar]
  38. 38.
    Fernández-Suárez M, Ting AY. 2008. Fluorescent probes for super-resolution imaging in living cells. Nat. Rev. Mol. Cell Biol. 9:12929–43
    [Google Scholar]
  39. 39.
    Finan K, Raulf A, Heilemann M 2015. A set of homo-oligomeric standards allows accurate protein counting. Angew. Chem. Int. Ed. 54:4112049–52
    [Google Scholar]
  40. 40.
    Früh SM, Matti U, Spycher PR, Rubini M, Lickert S et al. 2021. Site-specifically-labeled antibodies for super-resolution microscopy reveal in situ linkage errors. ACS Nano 15:712161–70Quantification of linkage error in SMLM.
    [Google Scholar]
  41. 41.
    Früh SM, Schoen I, Ries J, Vogel V 2015. Molecular architecture of native fibronectin fibrils. Nat. Commun. 6:7275
    [Google Scholar]
  42. 42.
    Gautier A, Juillerat A, Heinis C, Corrêa IR, Kindermann M et al. 2008. An engineered protein tag for multiprotein labeling in living cells. Chem. Biol. 15:2128–36
    [Google Scholar]
  43. 43.
    Goodsell DS, Autin L, Olson AJ 2019. Illustrate: software for biomolecular illustration. Structure 27:111716–20.e1
    [Google Scholar]
  44. 44.
    Götzke H, Kilisch M, Martínez-Carranza M, Sograte-Idrissi S, Rajavel A et al. 2019. The ALFA-tag is a highly versatile tool for nanobody-based bioscience applications. Nat. Commun. 10:4403
    [Google Scholar]
  45. 45.
    Grimm JB, English BP, Chen J, Slaughter JP, Zhang Z et al. 2015. A general method to improve fluorophores for live-cell and single-molecule microscopy. Nat. Methods 12:3244–50
    [Google Scholar]
  46. 46.
    Grimm JB, English BP, Choi H, Muthusamy AK, Mehl BP et al. 2016. Bright photoactivatable fluorophores for single-molecule imaging. Nat. Methods 13:12985–88
    [Google Scholar]
  47. 47.
    Gu L, Li Y, Zhang S, Xue Y, Li W et al. 2019. Molecular resolution imaging by repetitive optical selective exposure. Nat. Methods 16:111114–18
    [Google Scholar]
  48. 48.
    Gu L, Li Y, Zhang S, Zhou M, Xue Y et al. 2021. Molecular-scale axial localization by repetitive optical selective exposure. . Nat. Methods 18:4369–73Demonstrated that ROSE-z achieves comparable performance with 4Pi-SMLM using axially modulated illumination.
    [Google Scholar]
  49. 49.
    Gwosch KC, Pape JK, Balzarotti F, Hoess P, Ellenberg J et al. 2020. MINFLUX nanoscopy delivers 3D multicolor nanometer resolution in cells. Nat. Methods 17:2217–24Extension of MINFLUX to large FoVs and to 3D, dual-color, and live cells.
    [Google Scholar]
  50. 50.
    Hajj B, Wisniewski J, Beheiry ME, Chen J, Revyakin A et al. 2014. Whole-cell, multicolor superresolution imaging using volumetric multifocus microscopy. PNAS 111:4917480–85
    [Google Scholar]
  51. 51.
    Hauser M, Wojcik M, Kim D, Mahmoudi M, Li W, Xu K. 2017. Correlative super-resolution microscopy: new dimensions and new opportunities. Chem. Rev. 117:117428–56
    [Google Scholar]
  52. 52.
    Heilemann M, vandeLinde S, Schüttpelz M, Kasper R, Seefeldt B et al. 2008. Subdiffraction-resolution fluorescence imaging with conventional fluorescent probes. Angew. Chem. Int. Ed. 47:336172–76Established dSTORM as an experimentally simpler version of STORM.
    [Google Scholar]
  53. 53.
    Hess ST, Girirajan TPK, Mason MD. 2006. Ultra-high resolution imaging by fluorescence photoactivation localization microscopy. Biophys. J. 91:114258–72
    [Google Scholar]
  54. 54.
    Heydarian H, Joosten M, Przybylski A, Schueder F, Jungmann R et al. 2021. 3D particle averaging and detection of macromolecular symmetry in localization microscopy. Nat. Commun. 12:2847Template-free 3D particle averaging for SMLM.
    [Google Scholar]
  55. 55.
    Heydarian H, Schueder F, Strauss MT, van Werkhoven B, Fazel M et al. 2018. Template-free 2D particle fusion in localization microscopy. Nat. Methods 15:10781–84
    [Google Scholar]
  56. 56.
    Hoess P, Mund M, Reitberger M, Ries J 2018. Dual-color and 3D super-resolution microscopy of multi-protein assemblies. Methods Mol. Biol. 1764:237–51
    [Google Scholar]
  57. 57.
    Hoffman DP, Shtengel G, Xu CS, Campbell KR, Freeman M et al. 2020. Correlative three-dimensional super-resolution and block-face electron microscopy of whole vitreously frozen cells. Science 367:6475eaaz5357
    [Google Scholar]
  58. 58.
    Holden SJ, Pengo T, Meibom KL, Fernandez CF, Collier J, Manley S. 2014. High throughput 3D super-resolution microscopy reveals Caulobacter crescentus in vivo Z-ring organization. PNAS 111:124566–71
    [Google Scholar]
  59. 59.
    Holden SJ, Uphoff S, Kapanidis AN 2011. DAOSTORM: an algorithm for high-density super-resolution microscopy. Nat. Methods 8:4279–80
    [Google Scholar]
  60. 60.
    Huang B, Wang W, Bates M, Zhuang X. 2008. Three-dimensional super-resolution imaging by stochastic optical reconstruction microscopy. Science 319:5864810–13
    [Google Scholar]
  61. 61.
    Huang F, Hartwich TMP, Rivera-Molina FE, Lin Y, Duim WC et al. 2013. Video-rate nanoscopy using sCMOS camera-specific single-molecule localization algorithms. Nat. Methods 10:7653–58
    [Google Scholar]
  62. 62.
    Huang F, Schwartz SL, Byars JM, Lidke KA. 2011. Simultaneous multiple-emitter fitting for single molecule super-resolution imaging. Biomed. Opt. Express 2:51377–93
    [Google Scholar]
  63. 63.
    Huang F, Sirinakis G, Allgeyer ES, Schroeder LK, Duim WC et al. 2016. Ultra-high resolution 3D imaging of whole cells. Cell 166:41028–403D whole-cell imaging at 10 nm resolution using 4Pi-SMLM.
    [Google Scholar]
  64. 64.
    Huhle A, Klaue D, Brutzer H, Daldrop P, Joo S et al. 2015. Camera-based three-dimensional real-time particle tracking at kHz rates and Ångström accuracy. Nat. Commun. 6:5885
    [Google Scholar]
  65. 65.
    Hurlock ME, Čavka I, Kursel LE, Haversat J, Wooten M et al. 2020. Identification of novel synaptonemal complex components in C. elegans. J. Cell Biol. 219:5e20190043
    [Google Scholar]
  66. 66.
    Isselstein M, Zhang L, Glembockyte V, Brix O, Cosa G et al. 2020. Self-healing dyes—keeping the promise?. J. Phys. Chem. Lett. 11:114462–80
    [Google Scholar]
  67. 67.
    Jimenez Sabinina V, Hossain MJ, Hériché J-K, Hoess P, Nijmeijer B et al. 2021. Three-dimensional superresolution fluorescence microscopy maps the variable molecular architecture of the nuclear pore complex. Mol. Biol. Cell 32:171523–33
    [Google Scholar]
  68. 68.
    Jouchet P, Cabriel C, Bourg N, Bardou M, Poüs C et al. 2021. Nanometric axial localization of single fluorescent molecules with modulated excitation. Nat. Photon. 15:297–304
    [Google Scholar]
  69. 69.
    Juette MF, Gould TJ, Lessard MD, Mlodzianoski MJ, Nagpure BS et al. 2008. Three-dimensional sub-100 nm resolution fluorescence microscopy of thick samples. Nat. Methods 5:6527–29
    [Google Scholar]
  70. 70.
    Jungmann R, Avendaño MS, Dai M, Woehrstein JB, Agasti SS et al. 2016. Quantitative super-resolution imaging with qPAINT. Nat. Methods 13:5439–42
    [Google Scholar]
  71. 71.
    Jungmann R, Avendaño MS, Woehrstein JB, Dai M, Shih WM, Yin P 2014. Multiplexed 3D cellular super-resolution imaging with DNA-PAINT and Exchange-PAINT. Nat. Methods 11:3313–18Established DNA-PAINT and the corresponding multiplexing.
    [Google Scholar]
  72. 72.
    Kanchanawong P, Shtengel G, Pasapera AM, Ramko EB, Davidson MW et al. 2010. Nanoscale architecture of integrin-based cell adhesions. Nature 468:7323580–84
    [Google Scholar]
  73. 73.
    Keppler A, Gendreizig S, Gronemeyer T, Pick H, Vogel H, Johnsson K. 2003. A general method for the covalent labeling of fusion proteins with small molecules in vivo. Nat. Biotechnol. 21:186–89
    [Google Scholar]
  74. 74.
    Kim D, Deerinck TJ, Sigal YM, Babcock HP, Ellisman MH, Zhuang X. 2015. Correlative stochastic optical reconstruction microscopy and electron microscopy. PLOS ONE 10:4e0124581
    [Google Scholar]
  75. 75.
    Klehs K, Spahn C, Endesfelder U, Lee SF, Fürstenberg A, Heilemann M 2014. Increasing the brightness of cyanine fluorophores for single-molecule and superresolution imaging. Chem. Phys. Chem. 15:4637–41
    [Google Scholar]
  76. 76.
    Köhler S, Wojcik M, Xu K, Dernburg AF. 2017. Superresolution microscopy reveals the three-dimensional organization of meiotic chromosome axes in intact Caenorhabditis elegans tissue. PNAS 114:24E4734–43
    [Google Scholar]
  77. 77.
    Kopek BG, Paez-Segala MG, Shtengel G, Sochacki KA, Sun MG et al. 2017. Diverse protocols for correlative super-resolution fluorescence imaging and electron microscopy of chemically fixed samples. Nat. Protoc. 12:5916–46
    [Google Scholar]
  78. 78.
    Laplante C, Huang F, Tebbs IR, Bewersdorf J, Pollard TD. 2016. Molecular organization of cytokinesis nodes and contractile rings by super-resolution fluorescence microscopy of live fission yeast. PNAS 113:40E5876–85
    [Google Scholar]
  79. 79.
    Lardon N, Wang L, Tschanz A, Hoess P, Tran M et al. 2021. Systematic tuning of rhodamine spirocyclization for super-resolution microscopy. J. Am. Chem. Soc 143:3614592600
    [Google Scholar]
  80. 80.
    Lee SF, Vérolet Q, Fürstenberg A. 2013. Improved super-resolution microscopy with oxazine fluorophores in heavy water. Angew. Chem. Int. Ed. 52:348948–51
    [Google Scholar]
  81. 81.
    Lee S-H, Shin JY, Lee A, Bustamante C. 2012. Counting single photoactivatable fluorescent molecules by photoactivated localization microscopy (PALM). PNAS 109:4317436–41
    [Google Scholar]
  82. 82.
    Lelek M, Gyparaki MT, Beliu G, Schueder F, Griffié J et al. 2021. Single-molecule localization microscopy. Nat. Rev. Methods Primers 1:39
    [Google Scholar]
  83. 83.
    Li Y, Mund M, Hoess P, Deschamps J, Matti U et al. 2018. Real-time 3D single-molecule localization using experimental point spread functions. Nat. Methods 15:5367–69
    [Google Scholar]
  84. 84.
    Lin Y, Long JJ, Huang F, Duim WC, Kirschbaum S et al. 2015. Quantifying and optimizing single-molecule switching nanoscopy at high speeds. PLOS ONE 10:5e0128135
    [Google Scholar]
  85. 85.
    Liu S, Huang F. 2020. Enhanced 4Pi single-molecule localization microscopy with coherent pupil based localization. Commun. Biol. 3:220
    [Google Scholar]
  86. 86.
    Los GV, Encell LP, McDougall MG, Hartzell DD, Karassina N et al. 2008. HaloTag: a novel protein labeling technology for cell imaging and protein analysis. ACS Chem. Biol. 3:6373–82
    [Google Scholar]
  87. 87.
    Löschberger A, Franke C, Krohne G, van de Linde S, Sauer M. 2014. Correlative super-resolution fluorescence and electron microscopy of the nuclear pore complex with molecular resolution. J. Cell Sci. 127:204351–55
    [Google Scholar]
  88. 88.
    Löschberger A, van de Linde S, Dabauvalle M-C, Rieger B, Heilemann M et al. 2012. Super-resolution imaging visualizes the eightfold symmetry of gp210 proteins around the nuclear pore complex and resolves the central channel with nanometer resolution. J. Cell Sci. 125:3570–75
    [Google Scholar]
  89. 89.
    McEvoy AL, Hoi H, Bates M, Platonova E, Cranfill PJ et al. 2012. mMaple: a photoconvertible fluorescent protein for use in multiple imaging modalities. PLOS ONE 7:12e51314
    [Google Scholar]
  90. 90.
    McGorty R, Kamiyama D, Huang B. 2013. Active microscope stabilization in three dimensions using image correlation. Opt. Nanosc. 2:110
    [Google Scholar]
  91. 91.
    Mlodzianoski MJ, Schreiner JM, Callahan SP, Smolková K, Dlasková A et al. 2011. Sample drift correction in 3D fluorescence photoactivation localization microscopy. Opt. Express 19:1615009–19
    [Google Scholar]
  92. 92.
    Möckl L, Moerner WE. 2020. Super-resolution microscopy with single molecules in biology and beyond: essentials, current trends, and future challenges. J. Am. Chem. Soc. 142:4217828–44
    [Google Scholar]
  93. 93.
    M'Saad O, Bewersdorf J. 2020. Light microscopy of proteins in their ultrastructural context. Nat. Commun. 11:3850
    [Google Scholar]
  94. 94.
    Mund M, van der Beek JA, Deschamps J, Dmitrieff S, Hoess P et al. 2018. Systematic nanoscale analysis of endocytosis links efficient vesicle formation to patterned actin nucleation. Cell 174:4884–96.e17Protein organization and assembly at endocytic sites in yeast cells using particle averaging and dynamic reconstruction.
    [Google Scholar]
  95. 95.
    Nehme E, Freedman D, Gordon R, Ferdman B, Weiss LE et al. 2020. DeepSTORM3D: dense 3D localization microscopy and PSF design by deep learning. Nat. Methods 17:734–40
    [Google Scholar]
  96. 96.
    Nieuwenhuizen RPJ, Bates M, Szymborska A, Lidke KA, Rieger B, Stallinga S 2015. Quantitative localization microscopy: effects of photophysics and labeling stoichiometry. PLOS ONE 10:5e0127989
    [Google Scholar]
  97. 97.
    Olivier N, Keller D, Gönczy P, Manley S 2013. Resolution doubling in 3D-STORM imaging through improved buffers. PLOS ONE 8:7e69004
    [Google Scholar]
  98. 98.
    Ong WQ, Citron YR, Schnitzbauer J, Kamiyama D, Huang B. 2015. Heavy water: a simple solution to increasing the brightness of fluorescent proteins in super-resolution imaging. Chem. Commun. 51:7013451–53
    [Google Scholar]
  99. 99.
    Opazo F, Levy M, Byrom M, Schäfer C, Geisler C et al. 2012. Aptamers as potential tools for super-resolution microscopy. Nat. Methods 9:10938–39
    [Google Scholar]
  100. 100.
    Pape JK, Stephan T, Balzarotti F, Büchner R, Lange F et al. 2020. Multicolor 3D MINFLUX nanoscopy of mitochondrial MICOS proteins. PNAS 117:3420607–14
    [Google Scholar]
  101. 101.
    Pavani SRP, Thompson MA, Biteen JS, Lord SJ, Liu N et al. 2009. Three-dimensional, single-molecule fluorescence imaging beyond the diffraction limit by using a double-helix point spread function. PNAS 106:92995–99
    [Google Scholar]
  102. 102.
    Pertsinidis A, Zhang Y, Chu S 2010. Subnanometre single-molecule localization, registration and distance measurements. Nature 466:7306647–51
    [Google Scholar]
  103. 103.
    Puchner EM, Walter JM, Kasper R, Huang B, Lim WA. 2013. Counting molecules in single organelles with superresolution microscopy allows tracking of the endosome maturation trajectory. PNAS 110:4016015–20
    [Google Scholar]
  104. 104.
    Punjani A, Rubinstein JL, Fleet DJ, Brubaker MA. 2017. cryoSPARC: algorithms for rapid unsupervised cryo-EM structure determination. Nat. Methods 14:3290–96
    [Google Scholar]
  105. 105.
    Reymond L, Huser T, Ruprecht V, Wieser S. 2020. Modulation-enhanced localization microscopy. J. Phys. Photon. 2:4041001
    [Google Scholar]
  106. 106.
    Reymond L, Ziegler J, Knapp C, Wang F-C, Huser TR et al. 2019. SIMPLE: structured illumination based point localization estimator with enhanced precision. Opt. Express 27:1724578–90
    [Google Scholar]
  107. 107.
    Ries J, Kaplan C, Platonova E, Eghlidi H, Ewers H. 2012. A simple, versatile method for GFP-based super-resolution microscopy via nanobodies. Nat. Methods 9:6582–84
    [Google Scholar]
  108. 108.
    Rollins GC, Shin JY, Bustamante C, Pressé S. 2015. Stochastic approach to the molecular counting problem in superresolution microscopy. PNAS 112:2E110–18
    [Google Scholar]
  109. 109.
    Ruckstuhl T, Verdes D. 2004. Supercritical angle fluorescence (SAF) microscopy. Opt. Express 12:184246–54
    [Google Scholar]
  110. 110.
    Rust MJ, Bates M, Zhuang X. 2006. Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM). Nat. Methods 3:10793–96
    [Google Scholar]
  111. 111.
    Schlichthaerle T, Eklund AS, Schueder F, Strauss MT, Tiede C et al. 2018. Site-specific labeling of affimers for DNA-PAINT microscopy. Angew. Chem. Int. Ed. 57:3411060–63
    [Google Scholar]
  112. 112.
    Schmidt R, Weihs T, Wurm CA, Jansen I, Rehman J et al. 2021. MINFLUX nanometer-scale 3D imaging and microsecond-range tracking on a common fluorescence microscope. Nat. Commun. 12:1478
    [Google Scholar]
  113. 113.
    Schnitzbauer J, Strauss MT, Schlichthaerle T, Schueder F, Jungmann R. 2017. Super-resolution microscopy with DNA-PAINT. Nat. Protoc. 12:61198–228
    [Google Scholar]
  114. 114.
    Schnitzbauer J, Wang Y, Zhao S, Bakalar M, Nuwal T et al. 2018. Correlation analysis framework for localization-based superresolution microscopy. PNAS 115:33219–24
    [Google Scholar]
  115. 115.
    Sharonov A, Hochstrasser RM. 2006. Wide-field subdiffraction imaging by accumulated binding of diffusing probes. PNAS 103:5018911–16
    [Google Scholar]
  116. 116.
    Shechtman Y, Weiss LE, Backer AS, Sahl SJ, Moerner WE. 2015. Precise three-dimensional scan-free multiple-particle tracking over large axial ranges with tetrapod point spread functions. Nano Lett 15:64194–99
    [Google Scholar]
  117. 117.
    Shi X, Garcia G, Van De Weghe JC, McGorty R, Pazour GJ et al. 2017. Super-resolution microscopy reveals that disruption of ciliary transition-zone architecture causes Joubert syndrome. Nat. Cell Biol. 19:101178–88
    [Google Scholar]
  118. 118.
    Shroff H, Galbraith CG, Galbraith JA, White H, Gillette JM et al. 2007. Dual-color superresolution imaging of genetically expressed probes within individual adhesion complexes. PNAS 104:5120308–13
    [Google Scholar]
  119. 119.
    Shtengel G, Galbraith JA, Galbraith CG, Lippincott-Schwartz J, Gillette JM et al. 2009. Interferometric fluorescent super-resolution microscopy resolves 3D cellular ultrastructure. PNAS 106:93125–30
    [Google Scholar]
  120. 120.
    Sieben C, Banterle N, Douglass KM, Gönczy P, Manley S 2018. Multicolor single-particle reconstruction of protein complexes. Nat. Methods 15:10777–80
    [Google Scholar]
  121. 121.
    Sillibourne JE, Specht CG, Izeddin I, Hurbain I, Tran P et al. 2011. Assessing the localization of centrosomal proteins by PALM/STORM nanoscopy. Cytoskeleton 68:11619–27
    [Google Scholar]
  122. 122.
    Sochacki KA, Dickey AM, Strub M-P, Taraska JW. 2017. Endocytic proteins are partitioned at the edge of the clathrin lattice in mammalian cells. Nat. Cell Biol. 19:4352–61
    [Google Scholar]
  123. 123.
    Speiser A, Müller L-R, Hoess P, Matti U, Obara CJ et al. 2021. Deep learning enables fast and dense single-molecule localization with high accuracy. Nat. Methods 18:1082–90
    [Google Scholar]
  124. 124.
    Stehr F, Stein J, Schueder F, Schwille P, Jungmann R. 2019. Flat-top TIRF illumination boosts DNA-PAINT imaging and quantification. Nat. Commun. 10:1268
    [Google Scholar]
  125. 125.
    Szymborska A, de Marco A, Daigle N, Cordes VC, Briggs JAG, Ellenberg J. 2013. Nuclear pore scaffold structure analyzed by super-resolution microscopy and particle averaging. Science 341:6146655–58
    [Google Scholar]
  126. 126.
    Takakura H, Zhang Y, Erdmann RS, Thompson AD, Lin Y et al. 2017. Long time-lapse nanoscopy with spontaneously blinking membrane probes. Nat. Biotechnol. 35:8773–80
    [Google Scholar]
  127. 127.
    Tam J, Cordier GA, Borbely JS, Álvarez ÁS, Lakadamyali M. 2014. Cross-talk-free multi-color STORM imaging using a single fluorophore. PLOS ONE 9:7e101772
    [Google Scholar]
  128. 128.
    Testa I, Wurm CA, Medda R, Rothermel E, von Middendorff C et al. 2010. Multicolor fluorescence nanoscopy in fixed and living cells by exciting conventional fluorophores with a single wavelength. Biophys. J. 99:82686–94
    [Google Scholar]
  129. 129.
    Thevathasan JV, Kahnwald M, Cieśliński K, Hoess P, Peneti SK et al. 2019. Nuclear pores as versatile reference standards for quantitative superresolution microscopy. Nat. Methods 16:101045–53Introduced NPC cell lines as a reference standard for resolution, counting, and labeling in SMLM.
    [Google Scholar]
  130. 130.
    Traenkle B, Rothbauer U. 2017. Under the microscope: single-domain antibodies for live-cell imaging and super-resolution microscopy. Front. Immunol. 8:1030
    [Google Scholar]
  131. 131.
    Turkowyd B, Balinovic A, Virant D, Carnero HGG, Caldana F et al. 2017. A general mechanism of photoconversion of green-to-red fluorescent proteins based on blue and infrared light reduces phototoxicity in live-cell single-molecule imaging. Angew. Chem. Int. Ed. 56:3811634–39
    [Google Scholar]
  132. 132.
    Uno S, Kamiya M, Yoshihara T, Sugawara K, Okabe K et al. 2014. A spontaneously blinking fluorophore based on intramolecular spirocyclization for live-cell super-resolution imaging. Nat. Chem. 6:8681–89
    [Google Scholar]
  133. 133.
    Uttamapinant C, Howe JD, Lang K, Beránek V, Davis L et al. 2015. Genetic code expansion enables live-cell and super-resolution imaging of site-specifically labeled cellular proteins. J. Am. Chem. Soc. 137:144602–5
    [Google Scholar]
  134. 134.
    Valley CC, Liu S, Lidke DS, Lidke KA. 2015. Sequential superresolution imaging of multiple targets using a single fluorophore. PLOS ONE 10:4e0123941
    [Google Scholar]
  135. 135.
    Vicidomini G, Bianchini P, Diaspro A. 2018. STED super-resolved microscopy. Nat. Methods 15:3173–82
    [Google Scholar]
  136. 136.
    Virant D, Traenkle B, Maier J, Kaiser PD, Bodenhöfer M et al. 2018. A peptide tag-specific nanobody enables high-quality labeling for dSTORM imaging. Nat. Commun. 9:930
    [Google Scholar]
  137. 137.
    Virant D, Turkowyd B, Balinovic A, Endesfelder U. 2017. Combining primed photoconversion and UV-photoactivation for aberration-free, live-cell compliant multi-color single-molecule localization microscopy imaging. Int. J. Mol. Sci. 18:71524
    [Google Scholar]
  138. 138.
    Vogelsang J, Kasper R, Steinhauer C, Person B, Heilemann M et al. 2008. A reducing and oxidizing system minimizes photobleaching and blinking of fluorescent dyes. Angew. Chem. Int. Ed. 47:295465–69
    [Google Scholar]
  139. 139.
    von Appen A, Kosinski J, Sparks L, Ori A, DiGuilio AL et al. 2015. In situ structural analysis of the human nuclear pore complex. Nature 526:7571140–43
    [Google Scholar]
  140. 140.
    Wang J, Allgeyer ES, Sirinakis G, Zhang Y, Hu K et al. 2021. Implementation of a 4Pi-SMS super-resolution microscope. Nat. Protoc. 16:2677–727
    [Google Scholar]
  141. 141.
    Wang L, Frei MS, Salim A, Johnsson K 2019. Small-molecule fluorescent probes for live-cell super-resolution microscopy. J. Am. Chem. Soc. 141:72770–81
    [Google Scholar]
  142. 142.
    Wang Y, Schnitzbauer J, Hu Z, Li X, Cheng Y et al. 2014. Localization events-based sample drift correction for localization microscopy with redundant cross-correlation algorithm. Opt. Express 22:1315982–91
    [Google Scholar]
  143. 143.
    Wassie AT, Zhao Y, Boyden ES. 2018. Expansion microscopy: principles and uses in biological research. Nat. Methods 16:133–41
    [Google Scholar]
  144. 144.
    Weisenburger S, Boening D, Schomburg B, Giller K, Becker S et al. 2017. Cryogenic optical localization provides 3D protein structure data with Angstrom resolution. Nat. Methods 14:2141–44
    [Google Scholar]
  145. 145.
    Wu Y-L, Hoess P, Tschanz A, Matti U, Mund M, Ries J 2021. Maximum-likelihood model fitting for quantitative analysis of SMLM data. bioRxiv 2021.08.30.456756. https://doi.org/10.1101/2021.08.30.456756
    [Crossref]
  146. 146.
    Wu Y-L, Tschanz A, Krupnik L, Ries J. 2020. Quantitative data analysis in single-molecule localization microscopy. Trends Cell Biol 30:11837–51
    [Google Scholar]
  147. 147.
    Wulf E, Deboben A, Bautz FA, Faulstich H, Wieland T. 1979. Fluorescent phallotoxin, a tool for the visualization of cellular actin. PNAS 76:94498–502
    [Google Scholar]
  148. 148.
    Xu K, Zhong G, Zhuang X 2013. Actin, spectrin, and associated proteins form a periodic cytoskeletal structure in axons. Science 339:6118452–56Discovered the periodic organization of actin and spectrin in axons using dual-objective SMLM.
    [Google Scholar]
  149. 149.
    Zanacchi FC, Manzo C, Alvarez AS, Derr ND, Garcia-Parajo MF, Lakadamyali M. 2017. A DNA origami platform for quantifying protein copy number in super-resolution. Nat. Methods 14:8789–92
    [Google Scholar]
  150. 150.
    Zhang M, Chang H, Zhang Y, Yu J, Wu L et al. 2012. Rational design of true monomeric and bright photoactivatable fluorescent proteins. Nat. Methods 9:7727–29
    [Google Scholar]
  151. 151.
    Zhang Y, Schroeder LK, Lessard MD, Kidd P, Chung J et al. 2020. Nanoscale subcellular architecture revealed by multicolor three-dimensional salvaged fluorescence imaging. Nat. Methods 17:2225–31
    [Google Scholar]
  152. 152.
    Zhao T, Wang Y, Zhai Y, Qu X, Cheng A et al. 2015. A user-friendly two-color super-resolution localization microscope. Opt. Express 23:21879–87
    [Google Scholar]
  153. 153.
    Zhu L, Zhang W, Elnatan D, Huang B. 2012. Faster STORM using compressed sensing. Nat. Methods 9:7721–23
    [Google Scholar]
  154. 154.
    Zwettler FU, Reinhard S, Gambarotto D, Bell TDM, Hamel V et al. 2020. Molecular resolution imaging by post-labeling expansion single-molecule localization microscopy (Ex-SMLM). Nat. Commun. 11:3388
    [Google Scholar]
/content/journals/10.1146/annurev-biophys-102521-112912
Loading
/content/journals/10.1146/annurev-biophys-102521-112912
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error