Super-resolution fluorescence imaging with single molecules

Current Opinion in Structural Biology

Volumn 23, Issue 5, 2013, Pages 778-787

  Sahl, Steffen J ^a   Moerner, W E ^a  

^a STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL COUNT; CELL LABELING; CELL ORGANELLE; CELL STRUCTURE; CELLULAR DISTRIBUTION; DIFFRACTION; ELECTRON MICROSCOPY; FLUORESCENCE IMAGING; FLUORESCENCE MICROSCOPY; FLUORESCENCE PHOTOACTIVATED LOCALIZATION MICROSCOPY; IMAGE ENHANCEMENT; IMAGE QUALITY; IMAGE RECONSTRUCTION; IMAGING; MOLECULAR IMAGING; NANOIMAGING; NONHUMAN; OPTICAL RESOLUTION; POINTS ACCUMULATION FOR IMAGING IN NANOSCALE TOPOGRAPHY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN STRUCTURE; REVIEW; SPATIOTEMPORAL ANALYSIS; STANDARD SINGLE MOLECULE IMAGING; STOCHASTIC OPTICAL RECONSTRUCTION MICROSCOPY; SUPER RESOLUTION FLUORESCENCE IMAGING; THREE DIMENSIONAL IMAGING; TIME LAPSE IMAGING;

IMAGING, THREE-DIMENSIONAL; MICROSCOPY, FLUORESCENCE; MOLECULAR IMAGING; MULTIPROTEIN COMPLEXES; ORGANELLES; TIME-LAPSE IMAGING;

EID: 84885862934     PISSN: 0959440X     EISSN: 1879033X     Source Type: Journal    
DOI: 10.1016/j.sbi.2013.07.010     Document Type: Review

References (94)

1. Abbe E. Contributions to the theory of the microscope and microscopic detection (Translated from German). Arch Mikroskop Anat 1873, 9:413-468.
2. Moerner W.E. Single-molecule optical spectroscopy and imaging: from early steps to recent advances. Single Molecule Spectroscopy in Chemistry, Physics and Biology: Nobel Symposium 138 Proceedings 2009, 25-60. Springer-Verlag, Berlin. A. Graslund, R. Rigler, J. Widengren (Eds.).
3. Moerner W.E. Single-molecule mountains yield nanoscale images. Nat Methods 2006, 3:781-782.
4. Moerner W.E., Orrit M. Illuminating single molecules in condensed matter. Science 1999, 283:1670-1676.
5. Moerner W.E. New directions in single-molecule imaging and analysis. Proc Natl Acad Sci U S A 2007, 104:12596-12602.
6. Hell S.W. Microscopy and its focal switch. Nat Methods 2009, 6:24-32.
7. Hell S.W., Wichmann J. Breaking the diffraction resolution limit by stimulated emission: stimulated-emission-depletion fluorescence microscopy. Opt Lett 1994, 19:780-782.
8. Klar T.W., Hell S.W. Subdiffraction resolution in far-field fluoresence microscopy. Opt Lett 1999, 24:954-956.
9. Donnert G., Keller J., Medda R., Andrei M.A., Rizzoli S.O., Luehrmann R., et al. Macromolecular-scale resolution in biological fluorescence microscopy. Proc Natl Acad Sci U S A 2006, 103:11440-11445.
10. Hell S.W. Toward fluorescence nanoscopy. Nat Biotechnol 2003, 21:1347-1355.
11. Hofmann M., Eggeling C., Jakobs S., Hell S.W. Breaking the diffraction barrier in fluorescence microscopy at low light intensities by using reversibly photoswitchable proteins. Proc Natl Acad Sci U S A 2005, 102:17565-17569.
12. Grotjohann T., Testa I., Leutenegger M., Bock H., Urban N.T., Lavoie-Cardinal F., et al. Diffraction-unlimited all-optical imaging and writing with a photochromic GFP. Nature 2011, 478:204-208.
13. Gustafsson M.G.L Surpassing the lateral resolution limit by a factor of two using structured illumination microscopy. J Microsc 2000, 198:82-87.
14. Gustafsson M.G.L Nonlinear structured-illumination microscopy: Wide-field fluorescence imaging with theoretically unlimited resolution. Proc Natl Acad Sci U S A 2005, 102:13081-13086.
15. Rego E.H., Shao L., Macklin J.J., Winoto L., Johansson G.A., Kamps-Hughes N., et al. Nonlinear structured-illumination microscopy with a photoswitchable protein reveals cellular structures at 50-nm resolution. Proc Natl Acad Sci U S A 2012, 109:E135-E143.
16. Moerner W.E., Kador L. Optical detection and spectroscopy of single molecules in a solid. Phys Rev Lett 1989, 62:2535-2538.
17. Moerner W.E., Basché T. Optical spectroscopy of single impurity molecules in solids. Angew Chem Int Ed 1993, 105:537.
18. Xie X.S. Single-molecule spectroscopy and dynamics at room temperature. Acc Chem Res 1996, 29:598-606.
19. Betzig E., Chichester R.J. Single molecules observed by near-field scanning optical microscopy. Science 1993, 262:1422-1425.
20. Bobroff N. Position measurement with a resolution and noise-limited instrument. Rev Sci Instrum 1986, 57:1152-1157.
21. Thompson R.E., Larson D.R., Webb W.W. Precise nanometer localization analysis for individual fluorescent probes. Biophys J 2002, 82:2775-2783.
22. Betzig E., Patterson G.H., Sougrat R., Lindwasser O.W., Olenych S., Bonifacino J.S., et al. Imaging intracellular fluorescent proteins at nanometer resolution. Science 2006, 313:1642-1645.
23. Hess S.T., Girirajan T.P.K., Mason M.D. Ultra-high resolution imaging by fluorescence photoactivation localization microscopy. Biophys J 2006, 91:4258-4272.
24. Rust M.J., Bates M., Zhuang X. Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM). Nat Methods 2006, 3:793-796.
25. Sharonov A., Hochstrasser R.M. Wide-field subdiffraction imaging by accumulated binding of diffusing probes. Proc Natl Acad Sci U S A 2006, 103:18911-18916.
26. Dickson R.M., Cubitt A.B., Tsien R.Y., Moerner W.E. On/off blinking and switching behavior of single green fluorescent protein molecules. Nature 1997, 388:355-358.
27. Biteen J.S., Thompson M.A., Tselentis N.K., Bowman G.R., Shapiro L., Moerner W.E. Super-resolution imaging in live Caulobacter crescentus cells using photoswitchable EYFP. Nat Methods 2008, 5:947-949.
28. Fölling J., Bossi M., Bock H., Medda R., Wurm C.A., Hein B., et al. Fluorescence nanoscopy by ground-state depletion and single-molecule return. Nat Methods 2008, 5:943-945.
29. Heilemann M., van de Linde S., Schüttpelz M., Kasper R., Seefeldt B., Mukherjee A., et al. Subdiffraction-resolution fluorescence imaging with conventional fluorescent probes. Angew Chem Int Ed 2008, 47:6172-6176.
30. Vogelsang J., Cordes T., Forthmann C., Steinhauer C., Tinnefeld P. Controlling the fluorescence of ordinary oxazine dyes for single-molecule switching and superresolution microscopy. Proc Natl Acad Sci U S A 2009, 106:8107-8112.
31. Shroff H., Galbraith C.G., Galbraith J.A., Betzig E. Live-cell photoactivated localization microscopy of nanoscale adhesion dynamics. Nat Methods 2008, 5:417-423.
32. Lee H.D., Sahl S.J., Lew M.D., Moerner W.E. The double-helix microscope super-resolves extended biological structures by localizing single blinking molecules in three dimensions with nanoscale precision. Appl Phys Lett 2012, 100:153701.
33. Xu K., Babcock H.P., Zhuang X. Dual-objective STORM reveals three-dimensional filament organization in the actin cytoskeleton. Nat Methods 2012, 9:185-188.
34. Xu K., Zhong G., Zhuang X. Actin, spectrin, and associated proteins form a periodic cytoskeletal structure in axons. Science 2013, 339:452-456.
35. Lee S.F., Thompson M.A., Schwartz M.A., Shapiro L., Moerner W.E. Super-resolution imaging of the nucleoid-associated protein HU in Caulobacter crescentus. Biophys J 2011, 100:L31-L33.
36. Wang W., Li G., Chen C., Xie X.S., Zhuang X. Chromosome organization by a nucleoid-associated protein in live bacteria. Science 2011, 333:1445-1449.
37. Greenfield D., McEvoy A.L., Shroff H., Crooks G.E., Wingreen N.S., Betzig E., et al. Self-organization of the Escherichia coli chemotaxis network imaged with super-resolution light microscopy. PLoS Biol 2009, 7:e1000137.
38. Ptacin J.L., Lee S.F., Garner E.C., Toro E., Eckart M., Comolli L.R., et al. A spindle-like apparatus guides bacterial chromosome segregation. Nat Cell Biol 2010, 12:791-798.
39. Benke A., Manley S. Live-cell dSTORM of cellular DNA based on direct DNA labeling. ChemBioChem 2012, 13:298-301.
40. Löschberger A., van de Linde S., Dabauvalle M.C., Rieger B., Heilemann M., Krohne G., et al. 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 2012, 125:570-575.
41. Kaminski Schierle G.S., van de Linde S., Erdelyi M., Esbjorner E.K., Klein T., Rees E., et al. In situ measurements of the formation and morphology of intracellular beta-amyloid fibrils by super-resolution fluorescence imaging. J Am Chem Soc 2011, 133:12902-12905.
42. Roberti M.J., Fölling J., Celej M.S., Bossi M., Jovin T.M., Jares-Erijman E.A. Imaging nanometer-sized α-synuclein aggregates by superresolution fluorescence localization microscopy. Biophys J 2012, 102:1598-1607.
43. Duim W.C., Chen B., Frydman J., Moerner W.E. Sub-diffraction imaging of huntingtin protein aggregates by fluorescence blink-microscopy and atomic force microscopy. ChemPhysChem 2011, 12:2387-2390.
44. Sahl S.J., Weiss L.E., Duim W.C., Frydman J., Moerner W.E. Cellular inclusion bodies of mutant huntingtin exon 1 obscure small fibrillar aggregate species. Sci Rep 2012, 2:895.
45. Lee M.K., Williams J., Twieg R.J., Rao J., Moerner W.E. Enzymatic activation of nitro-aryl fluorogens in live bacterial cells for enzymatic turnover-activated localization microscopy. Chem Sci 2013, 4:220-225.
46. Ondrus A.E., Lee H.D., Iwanaga S., Parsons W.H., Andresen B.M., Moerner W.E., et al. Fluorescent saxitoxins for live cell imaging of single voltage-gated sodium ion channels beyond the optical diffraction limit. Chem Biol 2012, 19:902-912.
47. Vrljic M., Nishimura S.Y., Brasselet S., Moerner W.E., McConnell.H.M. Uncorrelated diffusion of MHC class II proteins in the plasma membrane. Biophys J 2002, 82:523A.
48. Kim S.Y., Gitai Z., Kinkhabwala A., Shapiro L., Moerner W.E. Single molecules of the bacterial actin MreB undergo directed treadmilling motion in Caulobacter crescentus. Proc Natl Acad Sci U S A 2006, 103:10929-10934.
49. Sahl S.J., Leutenegger M., Hilbert M., Hell S.W., Eggeling C. Fast molecular tracking maps nanoscale dynamics of plasma membrane lipids. Proc Natl Acad Sci U S A 2010, 107:6829-6834.
50. Manley S., Gillette J.M., Patterson G.H., Shroff H., Hess H.F., Betzig E., et al. High-density mapping of single-molecule trajectories with photoactivated localization microscopy. Nat Methods 2008, 5:155-157.
51. Shim S., Xia C., Zhong G., Babcock H.P., Vaughan J.C., Huang B., et al. Super-resolution fluorescence imaging of organelles in live cells with photoswitchable membrane probes. Proc Natl Acad Sci U S A 2012, 109:13978-13983.
52. Hell S.W. Far-field optical nanoscopy. Science 2007, 316:1153-1158.
53. Hell S.W., Stelzer E.H.K Properties of a 4Pi-confocal fluorescence microscope. J Opt Soc Am A 1992, 9:2159-2166.
54. Middendorff C.v., Egner A., Geisler C., Hell S.W., Schönle A. Isotropic 3D nanoscopy based on single emitter switching. Opt Express 2008, 16:20774-20788.
55. Shtengel G., Galbraith J.A., Galbraith C.G., Lippincott-Schwartz J., Gillette J.M., Manley S., et al. Interferometric fluorescent super-resolution microscopy resolves 3D cellular ultrastructure. Proc Natl Acad Sci U S A 2009, 106:3125-3130.
56. Aquino D., Schönle A., Geisler C., Middendorff C.V., Wurm C.A., Okamura Y., et al. Two-color nanoscopy of three-dimensional volumes by 4Pi detection of stochastically switched fluorophores. Nat Methods 2011, 8:353-359.
57. Huang B., Wang W., Bates M., Zhuang X. Three-dimensional super-resolution imaging by stochastic optical reconstruction microscopy. Science 2008, 319:810-813.
58. 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 2011, 8:327-333.
59. Prabhat P., Ram S., Ward E.S., Ober R.J. Simultaneous imaging of different focal planes in fluorescence microscopy for the study of cellular dynamics in three dimensions. IEEE Trans Nanobiosci 2004, 3:237-242.
60. Juette M.F., Gould T.J., Lessard M.D., Mlodzianoski M.J., Nagpure B.S., Bennett B.T., et al. Three-dimensional sub-100nm resolution fluorescence microscopy of thick samples. Nat Methods 2008, 5:527-529.
61. Pavani S.R.P, Thompson M.A., Biteen J.S., Lord S.J., Liu N., Twieg R.J., et al. Three-dimensional, single-molecule fluorescence imaging beyond the diffraction limit by using a double-helix point spread function. Proc Natl Acad Sci U S A 2009, 106:2995-2999.
62. Badieirostami M., Lew M.D., Thompson M.A., Moerner W.E. Three-dimensional localization precision of the double-helix point spread function versus astigmatism and biplane. Appl Phys Lett 2010, 97:161103.
63. Thompson M.A., Lew M.D., Badieirostami M., Moerner W.E. Localizing and tracking single nanoscale emitters in three dimensions with high spatiotemporal resolution using a double-helix point spread function. Nano Lett 2010, 10:211-218.
64. Lew M.D., Lee S.F., Badieirostami M., Moerner W.E. Corkscrew point spread function for far-field three-dimensional nanoscale localization of pointlike objects. Opt Lett 2011, 36:202-204.
65. Annibale P., Vanni S., Scarselli M., Rothlisberger U., Radenovic A. Quantitative photo activated localization microscopy: unraveling the effects of photoblinking. PLoS ONE 2011, 6:e22678.
66. Lee S., Shin J.Y., Lee A., Bustamante C. Counting single photoactivatable fluorescent molecules by photoactivated localization microscopy (PALM). Proc Natl Acad Sci U S A 2012, 109:17436-17441.
67. Chao J., Sripad R., Ward E.S., Ober R.J. Ultrahigh accuracy imaging modality for super-localization microscopy. Nat Methods 2013, 10:335-338.
68. Engelhardt J., Keller J., Hoyer P., Reuss M., Staudt T., Hell S.W. Molecular orientation affects localization accuracy in superresolution far-field fluorescence microscopy. Nano Lett 2011, 11:209-213.
69. Backlund M.P., Lew M.D., Backer A.S., Sahl S.J., Grover G., Agrawal A., et al. Simultaneous, accurate measurement of the 3D position and orientation of single molecules. Proc Natl Acad Sci U S A 2012, 109:19087-19092.
70. Lew M.D., Backlund M.P., Moerner W.E. Rotational mobility of single molecules affects localization accuracy in super-resolution fluorescence microscopy. Nano Lett 2013, 10.1021/nl304359p.
71. Vaughan J.C., Jia S., Zhuang X. Ultrabright photoactivatable fluorophores created by reductive caging. Nat Methods 2012, 9:1181-1184.
72. Lau L., Lee Y.L., Sahl S.J., Stearns T., Moerner W.E. STED microscopy with optimized labeling density reveals 9-fold arrangement of a centriole protein. Biophys J 2012, 102:2926-2935.
73. Opazo F., Levy M., Byrom M., Schaefer C., Geisler C., Groemer T.W., et al. Aptamers as potential tools for super-resolution microscopy. Nat Methods 2012, 9:938-939.
74. Ries J., Kaplan C., Platonova E., Eghlidi H., Ewers H. A simple, versatile method for GFP-based super-resolution microscopy via nanobodies. Nat Methods 2012, 9:582-584.
75. Jones S.A., Shim S., He J., Zhuang X. Fast, three-dimensional super-resolution imaging of live cells. Nat Methods 2011, 8:499-505.
76. Huang F., Hartwich T.M.P., Rivera-Molina F.E., Lin Y., Duim W.C., Long J.J., et al. Video-rate nanoscopy using sCMOS camera - specific single-molecule localization algorithms. Nat Methods 2013, 10:653-658.
77. 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 2011, 8:1027-1036.
78. Lee H.D., Lord S.J., Iwanaga S., Zhan K., Xie H., Williams J.C., et al. Superresolution imaging of targeted proteins in fixed and living cells using photoactivatable organic fluorophores. J Am Chem Soc 2010, 132:15099-15101.
79. Zanacchi F.C., Lavagnino Z., Donnorso P., Del Bue A., Furia L., Faretta M., et al. Live-cell 3D super-resolution imaging in thick biological samples. Nat Methods 2011, 8:1047-1049.
80. Holden S.J., Uphoff S., Kapanidis A.N. DAOSTORM: an algorithm for high-density super-resolution microscopy. Nat Methods 2011, 8:279-280.
81. Cox S., Rosten E., Monypenny J., Jovanovic-Talisman T., Burnette D.T., Lippincott-Schwartz J., et al. Bayesian localization microscopy reveals nanoscale podosome dynamics. Nat Methods 2012, 9:195-200.
82. Zhu L., Zhang W., Elnatan D., Huang B. Faster STORM using compressed sensing. Nat Methods 2012, (advance online publication).
83. Sengupta P., Jovanovic-Talisman T., Skoko D., Renz M., Veatch S.L., Lippincott-Schwartz.J. Probing protein heterogeneity in the plasma membrane using PALM and pair correlation analysis. Nat Methods 2011, 8:969-975.
84. Lubeck E., Cai L. Single-cell systems biology by super-resolution imaging and combinatorial labeling. Nat Methods 2012, 9:743-748.
85. Berk V., Fong N., Dempsey G., Develioglu O., Zhuang X., Yildiz F., et al. Superresolution imaging of intact microbial communities reveals molecular architecture of biofilm development and bacterial organization. Biophys J 2011, 100:617a.
86. Berk V., Fong J.C.N., Dempsey G.T., Develioglu O.N., Zhuang X., Liphardt J., et al. Molecular architecture and assembly principles of vibrio cholerae biofilms. Science 2012, 337:236-239.
87. Risselada H.J., Grubmüller H. How SNARE molecules mediate membrane fusion: recent insights from molecular simulations. Curr Opin Struct Biol 2012, 22:187-196.
88. Lew M.D., Lee S.F., Ptacin J.L., Lee M.K., Twieg R.J., Shapiro L., et al. Three-dimensional superresolution colocalization of intracellular protein superstructures and the cell surface in live Caulobacter crescentus. Proc Natl Acad Sci U S A 2011, 108:E1102-E1110.
89. Gahlmann A., Ptacin J.L., Grover G., Quirin S., von Diezmann A.R.S., Lee M.K., et al. Quantitative multicolor subdiffraction imaging of bacterial protein ultrastructures in three dimensions. Nano Lett 2013, 13:987-993.
90. Kanchanawong P., Shtengel G., Pasapera A.M., Ramko E.B., Davidson M.W., Hess H.F., et al. Nanoscale architecture of integrin-based cell adhesions. Nature 2010, 468:580-584.
91. Biteen J.S., Goley E.D., Shapiro L., Moerner W.E. Three-dimensional super-resolution imaging of the midplane protein FtsZ in live Caulobacter crescentus cells using astigmatism. ChemPhysChem 2012, 13:1007-1012.
92. Dani A., Huang B., Bergan J., Dulac C., Zhuang X. Superresolution imaging of chemical synapses in the brain. Neuron 2010, 68:843-856.
93. Beaudoin G.M.J., Schofield C.M., Nuwal T., Zang K., Ullian E.M., Huang B., et al. Afadin, A Ras/Rap effector that controls cadherin function, promotes spine and excitatory synapse density in the hippocampus. J Neurosci 2012, 32:99-110.
94. Mennella V., Keszthelyi B., McDonald K.L., Chhun B., Kan F., Rogers G.C., et al. Subdiffraction-resolution fluorescence microscopy reveals a domain of the centrosome critical for pericentriolar material organization. Nat Cell Biol 2012, 14:1159-1168.