Recent Advances in Super-Resolution Fluorescence Imaging and Its Applications in Biology

Rongcheng Han; Zhenghong Li; Yanyan Fan; Yuqiang Jiang

doi:10.1016/j.jgg.2013.11.003

Volume 40 Issue 12

Dec. 2013

Turn off MathJax

Article Contents

Article Navigation > Journal of Genetics and Genomics > 2013 > 40(12): 583-595

PDF( 1313 KB)

Recent Advances in Super-Resolution Fluorescence Imaging and Its Applications in Biology

doi: 10.1016/j.jgg.2013.11.003

a
Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China
b
Institute of Opto-Electronic Materials and Technology, South China Normal University, Guangzhou 510631, China

More Information

Corresponding author: E-mail address: yqjiang@genetics.ac.cn (Yuqiang Jiang)
Received Date: 2013-07-10
Accepted Date: 2013-11-11
Rev Recd Date: 2013-11-11

Available Online: 2013-11-23

Publish Date: 2013-12-20

Abstract

Abstract

Fluorescence microscopy has become an essential tool for biological research because it can be minimally invasive, acquire data rapidly, and target molecules of interest with specific labeling strategies. However, the diffraction-limited spatial resolution, which is classically limited to about 200 nm in the lateral direction and about 500 nm in the axial direction, hampers its application to identify delicate details of subcellular structure. Extensive efforts have been made to break diffraction limit for obtaining high-resolution imaging of a biological specimen. Various methods capable of obtaining super-resolution images with a resolution of tens of nanometers are currently available. These super-resolution techniques can be generally divided into three primary classes: (1) patterned illumination-based super-resolution imaging, which employs spatially and temporally modulated illumination light to reconstruct sub-diffraction structures; (2) single-molecule localization-based super-resolution imaging, which localizes the profile center of each individual fluorophore at subdiffraction precision; (3) bleaching/blinking-based super-resolution imaging. These super-resolution techniques have been utilized in different biological fields and provide novel insights into several new aspects of life science. Given unique technical merits and commercial availability of super-resolution fluorescence microscope, increasing applications of this powerful technique in life science can be expected.
- Super-resolution,
- Bio-imaging,
- Fluorescence microscopy,
- Optical diffraction limit

FullText(HTML)

References(140)

References

[1]	Abbe, E. Beiträge zur theorie des mikroskops und der mikroskopischen wahrnehmung Archiv für Mikroskopische Anatomie, 9 (1873),pp. 413-418
[2]	Andersen, J.S., Wilkinson, C.J., Mayor, T. et al. Proteomic characterization of the human centrosome by protein correlation profiling Nature, 426 (2003),pp. 570-574
[3]	Aquino, D., Schonle, A., Geisler, C. et al. Two-color nanoscopy of three-dimensional volumes by 4Pi detection of stochastically switched fluorophores Nat. Methods, 8 (2011),pp. 353-359
[4]	Baday, M., Cravens, A., Hastie, A. et al. Multicolor super-resolution DNA imaging for genetic analysis Nano Lett., 12 (2012),pp. 3861-3866
[5]	Bates, M., Blosser, T.R., Zhuang, X.W. Short-range spectroscopic ruler based on a single-molecule optical switch Phys. Rev. Lett., 94 (2005),p. 108101
[6]	Bates, M., Huang, B., Dempsey, G.T. et al. Multicolor super-resolution imaging with photo-switchable fluorescent probes Science, 317 (2007),pp. 1749-1753
[7]	Bates, M., Huang, B., Zhuang, X.W. Super-resolution microscopy by nanoscale localization of photo-switchable fluorescent probes Curr. Opin. Chem. Biol., 12 (2008),pp. 505-514
[8]	Betzig, E., Patterson, G.H., Sougrat, R. et al. Imaging intracellular fluorescent proteins at nanometer resolution Science, 313 (2006),pp. 1642-1645
[9]	Biteen, J.S., Goley, E.D., Shapiro, L. et al. Chemphyschem, 13 (2012),pp. 1007-1012
[10]	Biteen, J.S., Thompson, M.A., Tselentis, N.K. et al. Nat. Methods, 5 (2008),pp. 947-949
[11]	Bohn, M., Diesinger, P., Kaufmann, R. et al. Localization microscopy reveals expression-dependent parameters of chromatin nanostructure Biophys. J., 99 (2010),pp. 1358-1367
[12]	Bopp, M.A., Jia, Y.W., Li, L.Q. et al. Fluorescence and photobleaching dynamics of single light-harvesting complexes Proc. Natl. Acad. Sci. USA, 94 (1997),pp. 10630-10635
[13]	Bornens, M. The centrosome in cells and organisms Science, 335 (2012),pp. 422-426
[14]	Brakemann, T., Stiel, A.C., Weber, G. et al. A reversibly photoswitchable GFP-like protein with fluorescence excitation decoupled from switching Nat. Biotechnol., 29 (2011),pp. 942-947
[15]	Buckers, J., Wildanger, D., Vicidomini, G. et al. Simultaneous multi-lifetime multi-color STED imaging for colocalization analyses Opt. Express, 19 (2011),pp. 3130-3143
[16]	Burnette, D.T., Sengupta, P., Dai, Y.H. et al. Bleaching/blinking assisted localization microscopy for superresolution imaging using standard fluorescent molecules Proc. Natl. Acad. Sci. USA, 108 (2011),pp. 21081-21086
[17]	Cattoni, D., Fiche, J., Nollmann, M. Single-molecule super-resolution imaging in bacteria Curr. Opin. Microbiol., 15 (2012),pp. 758-763
[18]	Chakalova, L., Debrand, E., Mitchell, J.A. et al. Replication and transcription: shaping the landscape of the genome Nat. Rev. Genet., 6 (2005),pp. 669-677
[19]	Chang, H., Zhang, M.S., Ji, W. et al. A unique series of reversibly switchable fluorescent proteins with beneficial properties for various applications Proc. Natl. Acad. Sci. USA, 109 (2012),pp. 4455-4460
[20]	Chen, X., Liu, Y., Yang, X. et al.
[21]	Cho, S., Jang, J., Song, C. et al. Simple super-resolution live-cell imaging based on diffusion-assisted Forster resonance energy transfer Sci. Rep., 3 (2013),p. 1208
[22]	Chojnacki, J., Staudt, T., Glass, B. et al. Maturation-dependent HIV-1 surface protein redistribution revealed by fluorescence nanoscopy Science, 338 (2012),pp. 524-528
[23]	Coltharp, C., Xiao, J. Superresolution microscopy for microbiology Cell. Microbiol., 14 (2012),pp. 1808-1818
[24]	Cox, S., Rosten, E., Monypenny, J. et al. Bayesian localization microscopy reveals nanoscale podosome dynamics Nat. Methods, 9 (2012),pp. 195-200
[25]	Cremer, C., Kaufmann, R., Gunkel, M. et al. Superresolution imaging of biological nanostructures by spectral precision distance microscopy Biotechnol. J., 6 (2011),pp. 1037-1051
[26]	Dan, D., Lei, M., Yao, B.L. et al. DMD-based LED-illumination super-resolution and optical sectioning microscopy Sci. Rep., 3 (2013),p. 1116
[27]	Dedecker, P., Mo, G.C.H., Dertinger, T. et al. Widely accessible method for superresolution fluorescence imaging of living systems Proc. Natl. Acad. Sci. USA, 109 (2012),pp. 10909-10914
[28]	Dempsey, G.T., Vaughan, J.C., Chen, K.H. et al. Evaluation of fluorophores for optimal performance in localization-based super-resolution imaging Nat. Methods, 8 (2011),pp. 1027-1036
[29]	Dertinger, T., Colyer, R., Iyer, G. et al. Fast, background-free, 3D super-resolution optical fluctuation imaging (SOFI) Proc. Natl. Acad. Sci. USA, 106 (2009),pp. 22287-22292
[30]	Dertinger, T., Heilemann, M., Vogel, R. et al. Superresolution optical fluctuation imaging with organic dyes Angew. Chem. Int. Ed. Engl., 49 (2010),pp. 9441-9443
[31]	Ding, Y.C., Xi, P., Ren, Q.S. Hacking the optical diffraction limit: review on recent developments of fluorescence nanoscopy Chinese Sci. Bull., 56 (2011),pp. 1857-1876
[32]	Donnert, G., Keller, J., Wurm, C.A. et al. Two-color far-field fluorescence nanoscopy Biophys. J., 92 (2007),pp. L67-L69
[33]	Fitzpatrick, J.A.J., Yan, Q., Sieber, J.J. et al. STED nanoscopy in living cells using fluorogen activating proteins Bioconjug. Chem., 20 (2009),pp. 1843-1847
[34]	Flors, C. DNA and chromatin imaging with super-resolution fluorescence microscopy based on single-molecule localization Biopolymers, 95 (2011),pp. 290-297
[35]	Flors, C., Earnshaw, W.C. Super-resolution fluorescence microscopy as a tool to study the nanoscale organization of chromosomes Curr. Opin. Chem. Biol., 15 (2011),pp. 838-844
[36]	Folling, J., Belov, V., Kunetsky, R. et al. Photochromic rhodamines provide nanoscopy with optical sectioning Angew. Chem. Int. Ed. Engl., 46 (2007),pp. 6266-6270
[37]	Folling, J., Bossi, M., Bock, H. et al. Fluorescence nanoscopy by ground-state depletion and single-molecule return Nat. Methods, 5 (2008),pp. 943-945
[38]	Galbraith, C.G., Galbraith, J.A. Super-resolution microscopy at a glance J. Cell Sci., 124 (2011),pp. 1607-1611
[39]	Geissbuehler, S., Dellagiacoma, C., Lasser, T. Comparison between SOFI and STORM Biomed. Opt. Express, 2 (2011),pp. 408-420
[40]	Gordon, M.P., Ha, T., Selvin, P.R. Single-molecule high-resolution imaging with photobleaching Proc. Natl. Acad. Sci. USA, 101 (2004),pp. 6462-6465
[41]	Gould, T.J., Hess, S.T. Nanoscale biological fluorescence imaging: breaking the diffraction barrier Method. Cell Biol., 89 (2008),pp. 329-358
[42]	Grotjohann, T., Testa, I., Leutenegger, M. et al. Diffraction-unlimited all-optical imaging and writing with a photochromic GFP Nature, 478 (2011),pp. 204-208
[43]	Gur, A., Zalevsky, Z., Mico, V. et al. The limitations of nonlinear fluorescence effect in super resolution saturated structured illumination microscopy system J. Fluoresc., 21 (2011),pp. 1075-1082
[44]	Gustafsson, M.G.L. Surpassing the lateral resolution limit by a factor of two using structured illumination microscopy J. Microsc., 198 (2000),pp. 82-87
[45]	Gustafsson, M.G.L. Nonlinear structured-illumination microscopy: wide-field fluorescence imaging with theoretically unlimited resolution Proc. Natl. Acad. Sci. USA, 102 (2005),pp. 13081-13086
[46]	Hao, X., Kuang, C., Gu, Z. et al. Super resolution microscopy of offline g-STED nanoscopy based on time-correlated single photon counting Chinese J. Lasers, 40 (2013),p. 0104001
[47]	Heilemann, M., van de Linde, S., Schuttpelz, M. et al. Subdiffraction-resolution fluorescence imaging with conventional fluorescent probes Angew. Chem. Int. Ed. Engl., 47 (2008),pp. 6172-6176
[48]	Hein, B., Willig, K.I., Wurm, C.A. et al. Stimulated emission depletion nanoscopy of living cells using SNAP-tag fusion proteins Biophys. J., 98 (2010),pp. 158-163
[49]	Heintzmann, R. Saturated patterned excitation microscopy with two-dimensional excitation patterns Micron, 34 (2003),pp. 283-291
[50]	Heintzmann, R., Jovin, T.M., Cremer, C. Saturated patterned excitation microscopy ‒ a concept for optical resolution improvement J. Opt. Soc. Am. A., 19 (2002),pp. 1599-1609
[51]	Hell, S.W. Toward fluorescence nanoscopy Nat. Biotechnol., 21 (2003),pp. 1347-1355
[52]	Hell, S.W. Far-field optical nanoscopy Science, 316 (2007),pp. 1153-1158
[53]	Hell, S.W. Microscopy and its focal switch Nat. Methods, 6 (2009),pp. 24-32
[54]	Hell, S.W., Dyba, M., Jakobs, S. Concepts for nanoscale resolution in fluorescence microscopy Curr. Opin. Neurobiol., 14 (2004),pp. 599-609
[55]	Hell, S.W., Wichmann, J. Breaking the diffraction resolution limit by stimulated-emission-depletion fluorescence microscopy Opt. Lett., 19 (1994),pp. 780-782
[56]	Hess, S.T., Girirajan, T.P.K., Mason, M.D. Ultra-high resolution imaging by fluorescence photoactivation localization microscopy Biophys. J., 91 (2006),pp. 4258-4272
[57]	Hofmann, M., Eggeling, C., Jakobs, S. et al. Breaking the diffraction barrier in fluorescence microscopy at low light intensities by using reversibly photoswitchable proteins Proc. Natl. Acad. Sci. USA, 102 (2005),pp. 17565-17569
[58]	Holden, S.J., Uphoff, S., Kapanidis, A.N. DAOSTORM: an algorithm for high-density super-resolution microscopy Nat. Methods, 8 (2011),pp. 279-280
[59]	Huang, B., Babcock, H., Zhuang, X.W. Breaking the diffraction barrier: super-resolution imaging of cells Cell, 143 (2010),pp. 1047-1058
[60]	Huang, B., Bates, M., Dempsey, G. et al. PHYS 168-sub-diffraction-limit imaging by stochastic optical reconstruction microscopy Abstr. Pap. Am. Chem. S, 234 (2007)
[61]	Huang, B., Bates, M., Zhuang, X.W. Super-resolution fluorescence microscopy Annu. Rev. Biochem., 78 (2009),pp. 993-1016
[62]	Huang, B., Wang, W.Q., Bates, M. et al. Three-dimensional super-resolution imaging by stochastic optical reconstruction microscopy Science, 319 (2008),pp. 810-813
[63]	Huang, P.S., Zhang, S. Fast three-step phase-shifting algorithm Appl. Opt., 45 (2006),pp. 5086-5091
[64]	Jakobsen, L., Vanselow, K., Skogs, M. et al. Novel asymmetrically localizing components of human centrosomes identified by complementary proteomics methods EMBO J., 30 (2011),pp. 1520-1535
[65]	Jing, J.P., Reed, J., Huang, J. et al. Automated high resolution optical mapping using arrayed, fluid-fixed DNA molecules Proc. Natl. Acad. Sci. USA, 95 (1998),pp. 8046-8051
[66]	Jones, S.A., Shim, S.H., He, J. et al. Fast, three-dimensional super-resolution imaging of live cells Nat. Methods, 8 (2011)
[67]	Juette, M.F., Gould, T.J., Lessard, M.D. et al. Three-dimensional sub-100 nm resolution fluorescence microscopy of thick samples Nat. Methods, 5 (2008),pp. 527-529
[68]	Klar, T.A., Hell, S.W. Subdiffraction resolution in far-field fluorescence microscopy Opt. Lett., 24 (1999),pp. 954-956
[69]	Klar, T.A., Jakobs, S., Dyba, M. et al. Fluorescence microscopy with diffraction resolution barrier broken by stimulated emission Proc. Natl. Acad. Sci. USA, 97 (2000),pp. 8206-8210
[70]	Koster, A.J., Klumperman, J. Electron microscopy in cell biology: integrating structure and function Nat. Rev. Mol. Cell Biol., 4 (2003),pp. SS6-SS10
[71]	Kuang, C., Li, S., Liu, W. et al. Breaking the diffraction barrier using fluorescence emission difference microscopy Sci. Rep., 3 (2013),p. 1441
[72]	Lakowicz, J.R. Radiative decay engineering: biophysical and biomedical applications Anal. Biochem., 298 (2001),pp. 1-24
[73]	Larson, D.R., Thompson, R., Webb, W.W. Precise nanometer localization analysis for individual fluorescent probes Biophys. J., 82 (2002),pp. 2775-2783
[74]	Lau, L., Lee, Y.L., Sahl, S.J. et al. STED microscopy with optimized labeling density reveals 9-fold arrangement of a centriole protein Biophys. J., 102 (2012),pp. 2926-2935
[75]	Lawo, S., Hasegan, M., Gupta, G.D. et al. Subdiffraction imaging of centrosomes reveals higher-order organizational features of pericentriolar material Nat. Cell Biol., 14 (2012),pp. 1148-1158
[76]	Lehmann, M., Rocha, S., Mangeat, B. et al. Quantitative multicolor super-resolution microscopy reveals tetherin HIV-1 interaction PLoS Pathog., 7 (2011),p. e1002456
[77]	Lelek, M., Di Nunzio, F., Henriques, R. et al. Superresolution imaging of HIV in infected cells with FlAsH-PALM Proc. Natl. Acad. Sci. USA, 109 (2012),pp. 8564-8569
[78]	Leung, B.O., Chou, K.C. Review of super-resolution fluorescence microscopy for biology Appl. Spectrosc., 65 (2011),pp. 967-980
[79]	Lew, M.D., Lee, S.F., Ptacin, J.L. et al. Three-dimensional superresolution colocalization of intracellular protein superstructures and the cell surface in live Caulobacter crescentus Proc. Natl. Acad. Sci. USA, 108 (2011),pp. E1102-E1110
[80]	Lidke, K.A. Super resolution for common probes and common microscopes Nat. Methods, 9 (2012),pp. 139-141
[81]	Liu, Y.J., Ding, Y.C., Alonas, E. et al. Achieving lambda/10 resolution CW STED nanoscopy with a Ti: sapphire oscillator (2012)
[82]	Liu, Z.W., Lee, H., Xiong, Y. et al. Far-field optical hyperlens magnifying sub-diffraction-limited objects Science, 315 (2007),p. 1686
[83]	Lubeck, E., Cai, L. Single-cell systems biology by super-resolution imaging and combinatorial labeling Nat. Methods, 9 (2012),pp. 743-748
[84]	Luders, J. The amorphous pericentriolar cloud takes shape Nat. Cell Biol., 14 (2012),pp. 1126-1128
[85]	Malkusch, S., Muranyi, W., Müller, B. et al. Single-molecule coordinate-based analysis of the morphology of HIV-1 assembly sites with near-molecular spatial resolution Histochem. Cell Biol., 139 (2013),pp. 173-179
[86]	Matsuda, A., Shao, L., Boulanger, J. et al. Condensed mitotic chromosome structure at nanometer resolution using PALM and EGFP-histones PLoS ONE, 5 (2010),p. e12768
[87]	McKinney, S.A., Murphy, C.S., Hazelwood, K.L. et al. A bright and photostable photoconvertible fluorescent protein Nat. Methods, 6 (2009),pp. 131-133
[88]	Mennella, V., Keszthelyi, B., McDonald, K.L. et al. Subdiffraction-resolution fluorescence microscopy reveals a domain of the centrosome critical for pericentriolar material organization Nat. Cell Biol., 14 (2012),pp. 1159-1168
[89]	Meyer, L., Wildanger, D., Medda, R. et al. Dual-color STED microscopy at 30-nm focal-plane resolution Small, 4 (2008),pp. 1095-1100
[90]	Mukamel, E.A., Babcock, H., Zhuang, X.W. Statistical deconvolution for superresolution fluorescence microscopy Biophys. J., 102 (2012),pp. 2391-2400
[91]	Muller, P., Schmitt, E., Jacob, A. et al. COMBO-FISH enables high precision localization microscopy as a prerequisite for nanostructure analysis of genome loci Int. J. Mol. Sci., 11 (2010),pp. 4094-4105
[92]	Nienhaus, G.U. A fatigue-resistant photoswitchable fluorescent protein for optical nanoscopy Angew. Chem. Int. Ed. Engl., 51 (2012),pp. 1312-1314
[93]	Paintrand, M., Moudjou, M., Delacroix, H. et al. Centrosome organization and centriole architecture: their sensitivity to divalent cations J. Struct. Biol., 108 (1992),pp. 107-128
[94]	Panchenko, T., Sorensen, T.C., Woodcock, C.L. et al. Replacement of histone H3 with CENP-A directs global nucleosome array condensation and loosening of nucleosome superhelical termini Proc. Natl. Acad. Sci. USA, 108 (2011),pp. 16588-16593
[95]	Patterson, G., Davidson, M., Manley, S. et al. Superresolution imaging using single-molecule localization Annu. Rev. Phys. Chem., 61 (2010),pp. 345-367
[96]	Patterson, G.H., Lippincott-Schwartz, J. A photoactivatable GFP for selective photolabeling of proteins and cells Science, 297 (2002),pp. 1873-1877
[97]	Pavani, S.R.P., Thompson, M.A., Biteen, J.S. et al. Three-dimensional, single-molecule fluorescence imaging beyond the diffraction limit by using a double-helix point spread function Proc. Natl. Acad. Sci. USA, 106 (2009),pp. 2995-2999
[98]	Pellett, P.A., Sun, X.L., Gould, T.J. et al. Two-color STED microscopy in living cells Biomed. Opt. Express, 2 (2011),pp. 2364-2371
[99]	Pereira, C.F., Rossy, J., Owen, D.M. et al. HIV taken by STORM: super-resolution fluorescence microscopy of a viral infection Virol. J., 9 (2012),p. 84
[100]	Pohl, D.W., Denk, W., Lanz, M. Optical stethoscopy: image recording with resolution lambda/20 Appl. Phys. Lett., 44 (1984),pp. 651-653
[101]	Ptacin, J.L., Lee, S.F., Garner, E.C. et al. A spindle-like apparatus guides bacterial chromosome segregation Nat. Cell Biol., 12 (2010),pp. 791-798
[102]	Punge, A., Rizzoli, S.O., Jahn, R. et al. 3D reconstruction of high-resolution STED microscope images Microsc. Res. Tech., 71 (2008),pp. 644-650
[103]	Qu, X.H., Wu, D., Mets, L. et al. Nanometer-localized multiple single-molecule fluorescence microscopy Proc. Natl. Acad. Sci. USA, 101 (2004),pp. 11298-11303
[104]	Quan, T.W., Zhu, H.Y., Liu, X.M. et al. High-density localization of active molecules using structured sparse model and Bayesian information criterion Opt. Express, 19 (2011),pp. 16963-16974
[105]	Rego, E.H., Shao, L., Macklin, J.J. et al. Nonlinear structured-illumination microscopy with a photoswitchable protein reveals cellular structures at 50-nm resolution Proc. Natl. Acad. Sci. USA, 109 (2012),pp. E135-E143
[106]	Reymann, J., Baddeley, D., Gunkel, M. et al. High-precision structural analysis of subnuclear complexes in fixed and live cells via spatially modulated illumination (SMI) microscopy Chromosome Res., 16 (2008),pp. 367-382
[107]	Ribeiro, S.A., Vagnarelli, P., Dong, Y.M. et al. A super-resolution map of the vertebrate kinetochore Proc. Natl. Acad. Sci. USA, 107 (2010),pp. 10484-10489
[108]	Rittweger, E., Rankin, B.R., Westphal, V. et al. Fluorescence depletion mechanisms in super-resolving STED microscopy Chem. Phys. Lett., 442 (2007),pp. 483-487
[109]	Rust, M.J., Bates, M., Zhuang, X.W. Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM) Nat. Methods, 3 (2006),pp. 793-795
[110]	Sauer, M. Reversible molecular photoswitches: A key technology for nanoscience and fluorescence imaging Proc. Natl. Acad. Sci. USA, 102 (2005),pp. 9433-9434
[111]	Schermelleh, L., Carlton, P.M., Haase, S. et al. Subdiffraction multicolor imaging of the nuclear periphery with 3D structured illumination microscopy Science, 320 (2008),pp. 1332-1336
[112]	Schermelleh, L., Heintzmann, R., Leonhardt, H. A guide to super-resolution fluorescence microscopy J. Cell Biol., 190 (2010),pp. 165-175
[113]	Schmid, S.L. The mechanism of receptor-mediated endocytosis: more questions than answers Bioessays, 14 (1992),pp. 589-596
[114]	Schmid, S.L. Clathrin-coated vesicle formation and protein sorting: an integrated process Annu. Rev. Biochem., 66 (1997),pp. 511-548
[115]	Schmidt, R., Wurm, C.A., Punge, A. et al. Mitochondrial cristae revealed with focused light Nano Lett., 9 (2009),pp. 2508-2510
[116]	Shaner, N.C., Lin, M.Z., McKeown, M.R. et al. Improving the photostability of bright monomeric orange and red fluorescent proteins Nat. Methods, 5 (2008),pp. 545-551
[117]	Shroff, H., Galbraith, C.G., Galbraith, J.A. et al. Live-cell photoactivated localization microscopy of nanoscale adhesion dynamics Nat. Methods, 5 (2008),pp. 417-423
[118]	Shtengel, G., Galbraith, J.A., Galbraith, C.G. et al. Interferometric fluorescent super-resolution microscopy resolves 3D cellular ultrastructure Proc. Natl. Acad. Sci. USA, 106 (2009),pp. 3125-3130
[119]	Sigrist, S.J., Sabatini, B.L. Optical super-resolution microscopy in neurobiology Curr. Opin. Neurobiol., 22 (2012),pp. 86-93
[120]	Smolyaninov, I.I., Hung, Y.J., Davis, C.C. Magnifying superlens in the visible frequency range Science, 315 (2007),pp. 1699-1701
[121]	Tonnesen, J., Nadrigny, F., Willig, K.I. et al. Two-color STED microscopy of living synapses using a single laser-beam pair Biophys. J., 101 (2011),pp. 2545-2552
[122]	Tonnesen, J., Nagerl, U.V. Superresolution imaging for neuroscience Exp. Neurol., 242 (2013),pp. 33-40
[123]	van de Linde, S., Heilemann, M., Sauer, M. Live-cell super-resolution imaging with synthetic fluorophores Annu. Rev. Phys. Chem., 63 (2012),pp. 519-540
[124]	Vaughan, J.C., Zhuang, X. New fluorescent probes for super-resolution imaging Nat. Biotechnol., 29 (2011),pp. 880-881
[125]	Vorobjev, I.A., Chentsov, Y.S. The ultrastructure of centriole in mammalian tissue-culture cells Cell Biol. Int. Rep., 4 (1980),pp. 1037-1044
[126]	Wang, W.Q., Li, G.W., Chen, C.Y. et al. Chromosome organization by a nucleoid-associated protein in live bacteria Science, 333 (2011),pp. 1445-1449
[127]	Wang, Y., Quan, T.W., Zeng, S.Q. et al. PALMER: a method capable of parallel localization of multiple emitters for high-density localization microscopy Opt. Express, 20 (2012),pp. 16039-16049
[128]	Westphal, V., Rizzoli, S.O., Lauterbach, M.A. et al. Video-rate far-field optical nanoscopy dissects synaptic vesicle movement Science, 320 (2008),pp. 246-249
[129]	Wiedenmann, J., Ivanchenko, S., Oswald, F. et al. EosFP, a fluorescent marker protein with UV-inducible green-to-red fluorescence conversion Proc. Natl. Acad. Sci. USA, 101 (2004),pp. 15905-15910
[130]	Willig, K.I., Rizzoli, S.O., Westphal, V. et al. STED microscopy reveals that synaptotagmin remains clustered after synaptic vesicle exocytosis Nature, 440 (2006),pp. 935-939
[131]	Willig, K.I., Stiel, A.C., Brakemann, T. et al. Dual-label STED nanoscopy of living cells using photochromism Nano Lett., 11 (2011),pp. 3970-3973
[132]	Wombacher, R., Cornish, V.W. Chemical tags: applications in live cell fluorescence imaging J. Biophotonics, 4 (2011),pp. 391-402
[133]	Wombacher, R., Heidbreder, M., van de Linde, S. et al. Live-cell super-resolution imaging with trimethoprim conjugates Nat. Methods, 7 (2010),pp. 717-719
[134]	Wu, M., Huang, B., Graham, M. et al. Coupling between clathrin-dependent endocytic budding and F-BAR-dependent tubulation in a cell-free system Nat. Cell Biol., 12 (2010),pp. 902-908
[135]	Xiao, M., Gordon, M.P., Phong, A. et al. Determination of haplotypes from single DNA molecules: a method for single-molecule barcoding Hum. Mutat., 28 (2007),pp. 913-921
[136]	Xiao, M., Phong, A., Ha, C. et al. Rapid DNA mapping by fluorescent single molecule detection Nucleic Acids Res., 35 (2007),p. e16
[137]	Xiao, M., Wan, E., Chu, C. et al. Direct determination of haplotypes from single DNA molecules Nat. Methods, 6 (2009),pp. 199-201
[138]	Zessin, P.J.M., Finan, K., Heilemann, M. Super-resolution fluorescence imaging of chromosomal DNA J. Struct. Biol., 177 (2012),pp. 344-348
[139]	Zhang, M.S., Chang, H., Zhang, Y.D. et al. Rational design of true monomeric and bright photoactivatable fluorescent proteins Nat. Methods, 9 (2012),pp. 727-729
[140]	Zhu, L., Zhang, W., Elnatan, D. et al. Faster STORM using compressed sensing Nat. Methods, 9 (2012),pp. 721-723