Abstract

We present a novel approach for three-dimensional localization of single molecules using adaptive optics. A 52-actuator deformable mirror is used to both correct aberrations and induce two-dimensional astigmatism in the point-spread-function. The dependence of the z-localization precision on the degree of astigmatism is discussed. We achieve a z-localization precision of 40 nm for fluorescent proteins and 20 nm for fluorescent dyes, over an axial depth of ~800 nm. We illustrate the capabilities of our approach for three-dimensional high-resolution microscopy with super-resolution images of actin filaments in fixed cells and single-molecule tracking of quantum-dot labeled transmembrane proteins in live HeLa cells.

© 2012 OSA

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    [CrossRef] [PubMed]

2012

2011

2010

S. J. Lord, H.-L. D. Lee, and W. E. Moerner, “Single-molecule spectroscopy and imaging of biomolecules in living cells,” Anal. Chem. 82(6), 2192–2203 (2010).
[CrossRef] [PubMed]

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).
[PubMed]

G. Patterson, M. Davidson, S. Manley, and J. Lippincott-Schwartz, “Superresolution imaging using single-molecule localization,” Annu. Rev. Phys. Chem. 61(1), 345–367 (2010).
[CrossRef] [PubMed]

P. Kner, J. W. Sedat, D. A. Agard, and Z. Kam, “High-resolution wide-field microscopy with adaptive optics for spherical aberration correction and motionless focusing,” J. Microsc. 237(2), 136–147 (2010).
[CrossRef] [PubMed]

R. Henriques, M. Lelek, E. F. Fornasiero, F. Valtorta, C. Zimmer, and M. M. Mhlanga, “QuickPALM: 3D real-time photoactivation nanoscopy image processing in ImageJ,” Nat. Methods 7(5), 339–340 (2010).
[CrossRef] [PubMed]

S. Wolter, M. Schüttpelz, M. Tscherepanow, S. VAN DE Linde, M. Heilemann, and M. Sauer, “Real-time computation of subdiffraction-resolution fluorescence images,” J. Microsc. 237(1), 12–22 (2010).
[CrossRef] [PubMed]

F. Pinaud, S. Clarke, A. Sittner, and M. Dahan, “Probing cellular events, one quantum dot at a time,” Nat. Methods 7(4), 275–285 (2010).
[CrossRef] [PubMed]

O. Azucena, J. Crest, J. Cao, W. Sullivan, P. Kner, D. Gavel, D. Dillon, S. Olivier, and J. Kubby, “Wavefront aberration measurements and corrections through thick tissue using fluorescent microsphere reference beacons,” Opt. Express 18(16), 17521–17532 (2010).
[CrossRef] [PubMed]

2009

P. N. Hedde, J. Fuchs, F. Oswald, J. Wiedenmann, and G. U. Nienhaus, “Online image analysis software for photoactivation localization microscopy,” Nat. Methods 6(10), 689–690 (2009).
[CrossRef] [PubMed]

S. R. P. Pavani, M. A. Thompson, J. S. Biteen, S. J. Lord, N. Liu, R. J. Twieg, R. Piestun, and W. E. Moerner, “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. 106(9), 2995–2999 (2009).
[CrossRef] [PubMed]

G. Shtengel, J. A. Galbraith, C. G. Galbraith, J. Lippincott-Schwartz, 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(9), 3125–3130 (2009).
[CrossRef] [PubMed]

F. V. Subach, G. H. Patterson, S. Manley, J. M. Gillette, J. Lippincott-Schwartz, and V. V. Verkhusha, “Photoactivatable mCherry for high-resolution two-color fluorescence microscopy,” Nat. Methods 6(2), 153–159 (2009).
[CrossRef] [PubMed]

2008

B. Huang, W. Wang, M. Bates, and X. Zhuang, “Three-dimensional super-resolution imaging by stochastic optical reconstruction microscopy,” Science 319(5864), 810–813 (2008).
[CrossRef] [PubMed]

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(6), 527–529 (2008).
[CrossRef] [PubMed]

S. Ram, P. Prabhat, J. Chao, E. S. Ward, and R. J. Ober, “High accuracy 3D quantum dot tracking with multifocal plane microscopy for the study of fast intracellular dynamics in live cells,” Biophys. J. 95(12), 6025–6043 (2008).
[CrossRef] [PubMed]

A. Sergé, N. Bertaux, H. Rigneault, and D. Marguet, “Dynamic multiple-target tracing to probe spatiotemporal cartography of cell membranes,” Nat. Methods 5(8), 687–694 (2008).
[CrossRef] [PubMed]

2007

H. Bannai, S. Lévi, C. Schweizer, M. Dahan, and A. Triller, “Imaging the lateral diffusion of membrane molecules with quantum dots,” Nat. Protoc. 1(6), 2628–2634 (2007).
[CrossRef] [PubMed]

M. J. Booth, “Wavefront sensorless adaptive optics for large aberrations,” Opt. Lett. 32(1), 5–7 (2007).
[CrossRef] [PubMed]

Z. Kam, P. Kner, D. Agard, and J. W. Sedat, “Modelling the application of adaptive optics to wide-field microscope live imaging,” J. Microsc. 226(1), 33–42 (2007).
[CrossRef] [PubMed]

2006

S. T. Hess, T. P. K. Girirajan, and M. D. Mason, “Ultra-high resolution imaging by fluorescence photoactivation localization microscopy,” Biophys. J. 91(11), 4258–4272 (2006).
[CrossRef] [PubMed]

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(5793), 1642–1645 (2006).
[CrossRef] [PubMed]

M. J. Rust, M. Bates, and X. Zhuang, “Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM),” Nat. Methods 3(10), 793–796 (2006).
[CrossRef] [PubMed]

2003

M. Dahan, S. Lévi, C. Luccardini, P. Rostaing, B. Riveau, and A. Triller, “Diffusion dynamics of glycine receptors revealed by single-quantum dot tracking,” Science 302(5644), 442–445 (2003).
[CrossRef] [PubMed]

2002

R. E. Thompson, D. R. Larson, and W. W. Webb, “Precise nanometer localization analysis for individual fluorescent probes,” Biophys. J. 82(5), 2775–2783 (2002).
[CrossRef] [PubMed]

2001

M. K. Cheezum, W. F. Walker, and W. H. Guilford, “Quantitative comparison of algorithms for tracking single fluorescent particles,” Biophys. J. 81(4), 2378–2388 (2001).
[CrossRef] [PubMed]

2000

M. A. Neil, R. Juskaitis, M. J. Booth, T. Wilson, T. Tanaka, and S. Kawata, “Adaptive aberration correction in a two-photon microscope,” J. Microsc. 200(2), 105–108 (2000).
[CrossRef] [PubMed]

1998

M. J. Booth, M. Neil, and T. Wilson, “Aberration correction for confocal imaging in refractive?index?mismatched media,” J. Microsc. 192(2), 90–98 (1998).
[CrossRef]

1994

H. P. Kao and A. S. Verkman, “Tracking of single fluorescent particles in three dimensions: use of cylindrical optics to encode particle position,” Biophys. J. 67(3), 1291–1300 (1994).
[CrossRef] [PubMed]

1993

S. Forrest, “Genetic algorithms: principles of natural selection applied to computation,” Science 261(5123), 872–878 (1993).
[CrossRef] [PubMed]

Agard, D.

Z. Kam, P. Kner, D. Agard, and J. W. Sedat, “Modelling the application of adaptive optics to wide-field microscope live imaging,” J. Microsc. 226(1), 33–42 (2007).
[CrossRef] [PubMed]

Agard, D. A.

P. Kner, J. W. Sedat, D. A. Agard, and Z. Kam, “High-resolution wide-field microscopy with adaptive optics for spherical aberration correction and motionless focusing,” J. Microsc. 237(2), 136–147 (2010).
[CrossRef] [PubMed]

Andilla, J.

Artigas, D.

Aviles-Espinosa, R.

Azucena, O.

Bannai, H.

H. Bannai, S. Lévi, C. Schweizer, M. Dahan, and A. Triller, “Imaging the lateral diffusion of membrane molecules with quantum dots,” Nat. Protoc. 1(6), 2628–2634 (2007).
[CrossRef] [PubMed]

Bates, M.

B. Huang, W. Wang, M. Bates, and X. Zhuang, “Three-dimensional super-resolution imaging by stochastic optical reconstruction microscopy,” Science 319(5864), 810–813 (2008).
[CrossRef] [PubMed]

M. J. Rust, M. Bates, and X. Zhuang, “Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM),” Nat. Methods 3(10), 793–796 (2006).
[CrossRef] [PubMed]

Bennett, B. T.

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(6), 527–529 (2008).
[CrossRef] [PubMed]

Bertaux, N.

A. Sergé, N. Bertaux, H. Rigneault, and D. Marguet, “Dynamic multiple-target tracing to probe spatiotemporal cartography of cell membranes,” Nat. Methods 5(8), 687–694 (2008).
[CrossRef] [PubMed]

Betzig, E.

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).
[PubMed]

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(5793), 1642–1645 (2006).
[CrossRef] [PubMed]

Bewersdorf, J.

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(6), 527–529 (2008).
[CrossRef] [PubMed]

Biteen, J. S.

S. R. P. Pavani, M. A. Thompson, J. S. Biteen, S. J. Lord, N. Liu, R. J. Twieg, R. Piestun, and W. E. Moerner, “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. 106(9), 2995–2999 (2009).
[CrossRef] [PubMed]

Bonifacino, J. S.

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(5793), 1642–1645 (2006).
[CrossRef] [PubMed]

Booth, M. J.

M. J. Booth, “Wavefront sensorless adaptive optics for large aberrations,” Opt. Lett. 32(1), 5–7 (2007).
[CrossRef] [PubMed]

M. A. Neil, R. Juskaitis, M. J. Booth, T. Wilson, T. Tanaka, and S. Kawata, “Adaptive aberration correction in a two-photon microscope,” J. Microsc. 200(2), 105–108 (2000).
[CrossRef] [PubMed]

M. J. Booth, M. Neil, and T. Wilson, “Aberration correction for confocal imaging in refractive?index?mismatched media,” J. Microsc. 192(2), 90–98 (1998).
[CrossRef]

Boulanger, J.

Cao, J.

Chao, J.

S. Ram, P. Prabhat, J. Chao, E. S. Ward, and R. J. Ober, “High accuracy 3D quantum dot tracking with multifocal plane microscopy for the study of fast intracellular dynamics in live cells,” Biophys. J. 95(12), 6025–6043 (2008).
[CrossRef] [PubMed]

Cheezum, M. K.

M. K. Cheezum, W. F. Walker, and W. H. Guilford, “Quantitative comparison of algorithms for tracking single fluorescent particles,” Biophys. J. 81(4), 2378–2388 (2001).
[CrossRef] [PubMed]

Chen, D. C.

Choquet, D.

Clarke, S.

F. Pinaud, S. Clarke, A. Sittner, and M. Dahan, “Probing cellular events, one quantum dot at a time,” Nat. Methods 7(4), 275–285 (2010).
[CrossRef] [PubMed]

Crest, J.

Dahan, M.

I. Izeddin, J. Boulanger, V. Racine, C. Specht, A. Kechkar, D. Nair, A. Triller, D. Choquet, M. Dahan, and J. Sibarita, “Wavelet analysis for single molecule localization microscopy,” Opt. Express 20(3), 2081–2095 (2012).
[CrossRef]

I. Izeddin, C. G. Specht, M. Lelek, X. Darzacq, A. Triller, C. Zimmer, and M. Dahan, “Super-resolution dynamic imaging of dendritic spines using a low-affinity photoconvertible actin probe,” PLoS ONE 6(1), e15611 (2011).
[CrossRef] [PubMed]

F. Pinaud, S. Clarke, A. Sittner, and M. Dahan, “Probing cellular events, one quantum dot at a time,” Nat. Methods 7(4), 275–285 (2010).
[CrossRef] [PubMed]

H. Bannai, S. Lévi, C. Schweizer, M. Dahan, and A. Triller, “Imaging the lateral diffusion of membrane molecules with quantum dots,” Nat. Protoc. 1(6), 2628–2634 (2007).
[CrossRef] [PubMed]

M. Dahan, S. Lévi, C. Luccardini, P. Rostaing, B. Riveau, and A. Triller, “Diffusion dynamics of glycine receptors revealed by single-quantum dot tracking,” Science 302(5644), 442–445 (2003).
[CrossRef] [PubMed]

Darzacq, X.

I. Izeddin, C. G. Specht, M. Lelek, X. Darzacq, A. Triller, C. Zimmer, and M. Dahan, “Super-resolution dynamic imaging of dendritic spines using a low-affinity photoconvertible actin probe,” PLoS ONE 6(1), e15611 (2011).
[CrossRef] [PubMed]

Davidson, M.

G. Patterson, M. Davidson, S. Manley, and J. Lippincott-Schwartz, “Superresolution imaging using single-molecule localization,” Annu. Rev. Phys. Chem. 61(1), 345–367 (2010).
[CrossRef] [PubMed]

Davidson, M. W.

G. Shtengel, J. A. Galbraith, C. G. Galbraith, J. Lippincott-Schwartz, 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(9), 3125–3130 (2009).
[CrossRef] [PubMed]

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(5793), 1642–1645 (2006).
[CrossRef] [PubMed]

Dillon, D.

Fernandez, B.

Fetter, R. D.

G. Shtengel, J. A. Galbraith, C. G. Galbraith, J. Lippincott-Schwartz, 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(9), 3125–3130 (2009).
[CrossRef] [PubMed]

Fornasiero, E. F.

R. Henriques, M. Lelek, E. F. Fornasiero, F. Valtorta, C. Zimmer, and M. M. Mhlanga, “QuickPALM: 3D real-time photoactivation nanoscopy image processing in ImageJ,” Nat. Methods 7(5), 339–340 (2010).
[CrossRef] [PubMed]

Forrest, S.

S. Forrest, “Genetic algorithms: principles of natural selection applied to computation,” Science 261(5123), 872–878 (1993).
[CrossRef] [PubMed]

Fu, M.

Fuchs, J.

P. N. Hedde, J. Fuchs, F. Oswald, J. Wiedenmann, and G. U. Nienhaus, “Online image analysis software for photoactivation localization microscopy,” Nat. Methods 6(10), 689–690 (2009).
[CrossRef] [PubMed]

Galbraith, C. G.

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G. Patterson, M. Davidson, S. Manley, and J. Lippincott-Schwartz, “Superresolution imaging using single-molecule localization,” Annu. Rev. Phys. Chem. 61(1), 345–367 (2010).
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F. V. Subach, G. H. Patterson, S. Manley, J. M. Gillette, J. Lippincott-Schwartz, and V. V. Verkhusha, “Photoactivatable mCherry for high-resolution two-color fluorescence microscopy,” Nat. Methods 6(2), 153–159 (2009).
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Prabhat, P.

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M. Dahan, S. Lévi, C. Luccardini, P. Rostaing, B. Riveau, and A. Triller, “Diffusion dynamics of glycine receptors revealed by single-quantum dot tracking,” Science 302(5644), 442–445 (2003).
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M. Dahan, S. Lévi, C. Luccardini, P. Rostaing, B. Riveau, and A. Triller, “Diffusion dynamics of glycine receptors revealed by single-quantum dot tracking,” Science 302(5644), 442–445 (2003).
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H. Bannai, S. Lévi, C. Schweizer, M. Dahan, and A. Triller, “Imaging the lateral diffusion of membrane molecules with quantum dots,” Nat. Protoc. 1(6), 2628–2634 (2007).
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P. Kner, J. W. Sedat, D. A. Agard, and Z. Kam, “High-resolution wide-field microscopy with adaptive optics for spherical aberration correction and motionless focusing,” J. Microsc. 237(2), 136–147 (2010).
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Sibarita, J.

Sittner, A.

F. Pinaud, S. Clarke, A. Sittner, and M. Dahan, “Probing cellular events, one quantum dot at a time,” Nat. Methods 7(4), 275–285 (2010).
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Nat. Protoc.

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Supplementary Material (4)

» Media 1: MOV (191 KB)     
» Media 2: AVI (7854 KB)     
» Media 3: AVI (4869 KB)     
» Media 4: AVI (11424 KB)     

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Figures (5)

Fig. 1
Fig. 1

A) Experimental set-up. B) Measurement of the wavefront on the WFS: with the factory calibration of the DM (B1), after correction using an artifical star (B2), after the genetic algorithm (B3). The color scale corresponds to the distortion of the wavefront (in μm). C-E) Cross-sections of the PSF of a bead immobilized on a coverslip: PSF without the deformable mirror (C), after correction with deformable mirror (D). In each case, the spots are an image of the bead on the camera at positions 300 nm, 0 and – 300 nm (top to bottom), corresponding to the dotted lines. E) Measurement of the wavefront with a cylindrical lens in the optical pathway (E1) and after substracing the Zernike modes corresponding to an astigmatic distortion (E2). Experimental wavefront when using astigmatic deformation with amplitude A = 0.2 μm (E4). F) Cross-section of the PSF when using an astigmatic deformation, see also supplementary Media 1.

Fig. 5
Fig. 5

Plot of x- and y-localization precision at focal plane for microscope configuration (A) without use of deformable mirror, (B) with use of deformable mirror, and (C) with DM-induced astigmatism (amplitude 0.20 μm).

Fig. 2
Fig. 2

A-B) Widths wx and wy of bead astigmatic PSF with respect to distance from the focal plane for AO-induced astigmatism with an amplitude A = 0.20 μm (panel A) and a cylindrical lens (panel B). Data are computed with a Gaussian fit of the PSF in a 6-nm step z-series. (C) Calibration curve of the difference (Δw = wx - wy) in different astigmatic conditions.

Fig. 3
Fig. 3

A) Plot of z-localization precision at the focal plane with respect to number of photons. B) Quadratic curve fits of the z-localization precision with respect to the distance from the focal plane. C) “Stair graph” of a single bead displaced along z in consecutive steps of 50 nm with a piezo stage. Between two steps, 100 frames were acquired. The data (circle) correspond to the estimated localization in each frame and the plain line to the expected position.

Fig. 4
Fig. 4

B) Conventional image and three-dimensional PALM images of actin bundles in fibroblasts transfected with ABP-tdEos, with cylindrical lens and AO. The color scale represents molecular density. Scale bar, 2 μm; bounding box, 8.6μm x 13.7μm x 0.6 μm. B) 3D PALM images of actin bundles with AO and controlled astigmatism of A = 0.2 μm. Scale bar, 1 μm; bounding box, 10μm x 5.4μm x 1.3μm. Inset, diffraction limited 2D image of the same region. See also supplementary Media 2. C) Three-dimensional trajectory of quantum dot bound to a transmembrane protein diffusing in the plasma membrane of a cultured HeLa cell. Scale bar, 1 μm; bounding box, 10μm x 5.4μm x 1.3μm. In B and C, the color bar corresponds to the z position, in nm. See also supplementary Media 3 and Media 4.

Equations (1)

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φ= e i( 2π λ Aρcos( 2θ ) )

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