Quantitative super-resolution microscopy: Pitfalls and strategies for image analysis

Current Opinion in Chemical Biology

Volumn 20, Issue 1, 2014, Pages 22-28

  Durisic, Nela ^a   Cuervo, Lara Laparra ^a   Lakadamyali, Melike ^a  

^a ICFO INSTITUT DE CIENCIES FOTONIQUES   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

FLUORESCENT DYE;

BLEACHING; CELL STRUCTURE; DATA ANALYSIS; DIFFRACTION; FOURIER TRANSFORMATION; GENOME; HUMAN; IMAGE ANALYSIS; MICROSCOPY; PHOTOACTIVATION; PHOTON; QUANTITATIVE ANALYSIS; REVIEW; STEREOSPECIFICITY; STOICHIOMETRY; TANDEM REPEAT; TRANSIENT TRANSFECTION;

ANIMALS; CLUSTER ANALYSIS; FLUORESCENT DYES; HUMANS; MICROSCOPY; MOLECULAR IMAGING;

EID: 84899797358     PISSN: 13675931     EISSN: 18790402     Source Type: Journal    
DOI: 10.1016/j.cbpa.2014.04.005     Document Type: Review

References (49)

1. Klar T.A., Jakobs S., Dyba M., Egner A., Hell S.W. Fluorescence microscopy with diffraction resolution barrier broken by stimulated emission. Proc Natl Acad Sci U S A 2000, 97:8206-8210.
2. Gustafsson M.G. Nonlinear structured-illumination microscopy: wide-field fluorescence imaging with theoretically unlimited resolution. Proc Natl Acad Sci U S A 2005, 102:13081-13086.
3. Rust M.J., Bates M., Zhuang X. Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM). Nat Methods 2006, 3:793-795.
4. Betzig E., Patterson G.H., Sougrat R., Lindwasser O.W., Olenych S., Bonifacino J.S., Davidson M.W., Lippincott-Schwartz J., Hess H.F. Imaging intracellular fluorescent proteins at nanometer resolution. Science 2006, 313:1642-1645.
5. Hess S.T., Girirajan T.P., Mason M.D. Ultra-high resolution imaging by fluorescence photoactivation localization microscopy. Biophys J 2006, 91:4258-4272.
6. Heilemann M. Fluorescence microscopy beyond the diffraction limit. J Biotechnol 2010, 149:243-251.
7. Huang B., Babcock H., Zhuang X. Breaking the diffraction barrier: super-resolution imaging of cells. Cell 2010, 143:1047-1058.
8. Patterson G., Davidson M., Manley S., Lippincott-Schwartz J. Superresolution imaging using single-molecule localization. Annu Rev Phys Chem 2010, 61:345-367.
9. Thompson R.E., Larson D.R., Webb W.W. Precise nanometer localization analysis for individual fluorescent probes. Biophys J 2002, 82:2775-2783.
10. Patterson G.H., Lippincott-Schwartz J. A photoactivatable GFP for selective photolabeling of proteins and cells. Science 2002, 297:1873-1877.
11. Bates M., Blosser T.R., Zhuang X. Short-range spectroscopic ruler based on a single-molecule optical switch. Phys Rev Lett 2005, 94:108101.
12. Heilemann M., Margeat E., Kasper R., Sauer M., Tinnefeld P. Carbocyanine dyes as efficient reversible single-molecule optical switch. J Am Chem Soc 2005, 127:3801-3806.
13. Fernandez-Suarez M., Ting A.Y. Fluorescent probes for super-resolution imaging in living cells. Nat Rev Mol Cell Biol 2008, 9:929-943.
14. Lippincott-Schwartz J., Patterson G.H. Photoactivatable fluorescent proteins for diffraction-limited and super-resolution imaging. Trends Cell Biol 2009, 19:555-565.
15. 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.
16. Habuchi S., Ando R., Dedecker P., Verheijen W., Mizuno H., Miyawaki A., Hofkens J. Reversible single-molecule photoswitching in the GFP-like fluorescent protein Dronpa. Proc Natl Acad Sci U S A 2005, 102:9511-9516.
17. Wiedenmann J., Ivanchenko S., Oswald F., Schmitt F., Rocker C., Salih A., Spindler K.D., Nienhaus G.U. EosFP, a fluorescent marker protein with UV-inducible green-to-red fluorescence conversion. Proc Natl Acad Sci U S A 2004, 101:15905-15910.
18. Mortensen K.I., Churchman L.S., Spudich J.A., Flyvbjerg H. Optimized localization analysis for single-molecule tracking and super-resolution microscopy. Nat Methods 2010, 7:377-381.
19. Stallinga S., Rieger B. The effect of background on localization uncertainty in single emitter imaging. IEEE Int Symp Biomedical Imaging 2012, 988-991.
20. 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.
21. Lakadamyali M., Babcock H., Bates M., Zhuang X., Lichtman J. 3D multicolor super-resolution imaging offers improved accuracy in neuron tracing. PLOS ONE 2012, 7:e30826.
22. Vaughan J.C., Jia S., Zhuang X. Ultrabright photoactivatable fluorophores created by reductive caging. Nat Methods 2012, 9:1181-1184.
23. Saxton W.O., Baumeister W. The correlation averaging of a regularly arranged bacterial cell envelope protein. J Microsc 1982, 127:127-138.
24. Nieuwenhuizen R.P., Lidke K.A., Bates M., Puig D.L., Grunwald D., Stallinga S., Rieger B. Measuring image resolution in optical nanoscopy. Nat Methods 2013, 10:557-562.
25. Banterle N., Bui K.H., Lemke E.A., Beck M. Fourier ring correlation as a resolution criterion for super-resolution microscopy. J Struct Biol 2013, 183:363-367.
26. Dani A., Huang B., Bergan J., Dulac C., Zhuang X. Superresolution imaging of chemical synapses in the brain. Neuron 2010, 68:843-856.
27. Annibale P., Scarselli M., Kodiyan A., Radenovic A. Photoactivatable fluorescent protein mEos2 displays repeated photoactivation after a long-lived dark state in the red photoconverted form. J Phys Chem Lett 2010, 1:1506-1510.
28. Annibale P., Vanni S., Scarselli M., Rothlisberger U., Radenovic A. Identification of clustering artifacts in photoactivated localization microscopy. Nat Methods 2011, 8:527-528.
29. 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.
30. Lee S.H., 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.
31. Durisic N., Laparra-Cuervo L., Sandoval-Alvarez A., Borbely J.S., Lakadamyali M. Single-molecule evaluation of fluorescent protein photoactivation efficiency using an in vivo nanotemplate. Nat Methods 2014, 11:156-162.
32. Zhao Z.W., Roy R., Gebhardt J.C., Suter D.M., Chapman A.R., Xie X.S. Spatial organization of RNA polymerase II inside a mammalian cell nucleus revealed by reflected light-sheet superresolution microscopy. Proc Natl Acad Sci U S A 2014, 111:681-686.
33. Sengupta P., Jovanovic-Talisman T., Lippincott-Schwartz J. Quantifying spatial organization in point-localization superresolution images using pair correlation analysis. Nat Protoc 2013, 8:345-354.
34. 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.
35. Veatch S.L., Machta B.B., Shelby S.A., Chiang E.N., Holowka D.A., Baird B.A. Correlation functions quantify super-resolution images and estimate apparent clustering due to over-counting. PLOS ONE 2012, 7:e31457.
36. Helmuth J.A., Paul G., Sbalzarini I.F. Beyond co-localization: inferring spatial interactions between sub-cellular structures from microscopy images. BMC Bioinformatics 2010, 11:372.
37. Shivanandan A., Radenovic A., Sbalzarini I.F. MosaicIA: an ImageJ/Fiji plugin for spatial pattern and interaction analysis. BMC Bioinformatics 2013, 14:349.
38. Opazo F., Levy M., Byrom M., Schafer C., Geisler C., Groemer T.W., Ellington A.D., Rizzoli S.O. Aptamers as potential tools for super-resolution microscopy. Nat Methods 2012, 9:938-939.
39. 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.
40. Ran F.A., Hsu P.D., Wright J., Agarwala V., Scott D.A., Zhang F. Genome engineering using the CRISPR-Cas9 system. Nat Protoc 2013, 8:2281-2308.
41. Wood A.J., Lo T.W., Zeitler B., Pickle C.S., Ralston E.J., Lee A.H., Amora R., Miller J.C., Leung E., Meng X., et al. Targeted genome editing across species using ZFNs and TALENs. Science 2011, 333:307.
42. Gunzenhauser J., Olivier N., Pengo T., Manley S. Quantitative super-resolution imaging reveals protein stoichiometry and nanoscale morphology of assembling HIV-Gag virions. Nano Lett 2012, 12:4705-4710.
43. Nan X., Collisson E.A., Lewis S., Huang J., Tamguney T.M., Liphardt J.T., McCormick F., Gray J.W., Chu S. Single-molecule superresolution imaging allows quantitative analysis of RAF multimer formation and signaling. Proc Natl Acad Sci U S A 2013, 110:18519-18524.
44. Puchner E.M., Walter J.M., Kasper R., Huang B., Lim W.A. Counting molecules in single organelles with superresolution microscopy allows tracking of the endosome maturation trajectory. Proc Natl Acad Sci U S A 2013, 110:16015-16020.
45. Durisic N., Godin A.G., Wever C.M., Heyes C.D., Lakadamyali M., Dent J.A. Stoichiometry of the human glycine receptor revealed by direct subunit counting. J Neurosci 2012, 32:12915-12920.
46. Renz M., Daniels B.R., Vamosi G., Arias I.M., Lippincott-Schwartz J. Plasticity of the asialoglycoprotein receptor deciphered by ensemble FRET imaging and single-molecule counting PALM imaging. Proc Natl Acad Sci U S A 2012, 109:E2989-E2997.
47. Lehmann M., Rocha S., Mangeat B., Blanchet F., Uji I.H., Hofkens J., Piguet V. Quantitative multicolor super-resolution microscopy reveals tetherin HIV-1 interaction. PLoS Pathog 2011, 7:e1002456.
48. Lando D., Endesfelder U., Berger H., Subramanian L., Dunne P.D., McColl J., Klenerman D., Carr A.M., Sauer M., Allshire R.C., et al. Quantitative single-molecule microscopy reveals that CENP-A(Cnp1) deposition occurs during G2 in fission yeast. Open Biol 2012, 2:120078.
49. Scarselli M., Annibale P., Radenovic A. Cell type-specific beta2-adrenergic receptor clusters identified using photoactivated localization microscopy are not lipid raft related, but depend on actin cytoskeleton integrity. J Biol Chem 2012, 287:16768-16780.