Abstract

Three-dimensional single molecule localization microscopy relies on the fitting of the individual molecules with a point spread function (PSF) model. The reconstructed images often show local squeezing or expansion in z. A common cause is depth-induced aberrations in conjunction with an imperfect PSF model calibrated from beads on a coverslip, resulting in a mismatch between measured PSF and real PSF. Here, we developed a strategy for accurate z-localization in which we use the imperfect PSF model for fitting, determine the fitting errors and correct for them in a post-processing step. We present an open-source software tool and a simple experimental calibration procedure that allow retrieving accurate z-positions in any PSF engineering approach or fitting modality, even at large imaging depths.

© 2019 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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References

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    [Crossref] [PubMed]
  23. K. Xu, G. Zhong, and X. Zhuang, “Actin, spectrin, and associated proteins form a periodic cytoskeletal structure in axons,” Science 339(6118), 452–456 (2013).
    [Crossref] [PubMed]
  24. S. Otsuka, K. H. Bui, M. Schorb, M. J. Hossain, A. Z. Politi, B. Koch, M. Eltsov, M. Beck, and J. Ellenberg, “Nuclear pore assembly proceeds by an inside-out extrusion of the nuclear envelope,” eLife 5, 1–23 (2016).
    [Crossref] [PubMed]
  25. S. van de Linde, A. Löschberger, T. Klein, M. Heidbreder, S. Wolter, M. Heilemann, and M. Sauer, “Direct stochastic optical reconstruction microscopy with standard fluorescent probes,” Nat. Protoc. 6(7), 991–1009 (2011).
    [Crossref] [PubMed]
  26. L. Carlini, S. J. Holden, K. M. Douglass, and S. Manley, “Correction of a depth-dependent lateral distortion in 3d super-resolution imaging,” PLoS One 10(11), e0142949 (2015).
    [Crossref] [PubMed]

2018 (5)

Y. Li, M. Mund, P. Hoess, J. Deschamps, U. Matti, B. Nijmeijer, V. J. Sabinina, J. Ellenberg, I. Schoen, and J. Ries, “Real-time 3D single-molecule localization using experimental point spread functions,” Nat. Methods 15(5), 367–369 (2018).
[Crossref] [PubMed]

M. J. Mlodzianoski, P. J. Cheng-Hathaway, S. M. Bemiller, T. J. McCray, S. Liu, D. A. Miller, B. T. Lamb, G. E. Landreth, and F. Huang, “Active PSF shaping and adaptive optics enable volumetric localization microscopy through brain sections,” Nat. Methods 15(8), 583–586 (2018).
[Crossref] [PubMed]

A. Aristov, B. Lelandais, E. Rensen, and C. Zimmer, “ZOLA-3D allows flexible 3D localization microscopy over an adjustable axial range,” Nat. Commun. 9(1), 2409 (2018).
[Crossref] [PubMed]

C. Cabriel, N. Bourg, G. Dupuis, and S. Lévêque-Fort, “Aberration-accounting calibration for 3D single-molecule localization microscopy,” Opt. Lett. 43(2), 174–177 (2018).
[Crossref] [PubMed]

P. Hoess, M. Mund, M. Reitberger, and J. Ries, “Dual-color and 3D super-resolution microscopy of multi-protein assemblies,” Methods Mol. Biol. 1764, 237–251 (2018).
[Crossref] [PubMed]

2017 (2)

H. P. Babcock and X. Zhuang, “Analyzing single molecule localization microscopy data using cubic splines,” Sci. Rep. 7(1), 552 (2017).
[Crossref] [PubMed]

A. von Diezmann, Y. Shechtman, and W. E. Moerner, “Three-dimensional localization of single molecules for super-resolution imaging and single-particle tracking,” Chem. Rev. 117(11), 7244–7275 (2017).
[Crossref] [PubMed]

2016 (3)

J. Deschamps, A. Rowald, and J. Ries, “Efficient homogeneous illumination and optical sectioning for quantitative single-molecule localization microscopy,” Opt. Express 24(24), 28080–28090 (2016).
[Crossref] [PubMed]

R. Tafteh, D. R. L. Scriven, E. D. W. Moore, and K. C. Chou, “Single molecule localization deep within thick cells; a novel super-resolution microscope,” J. Biophotonics 9(1-2), 155–160 (2016).
[Crossref] [PubMed]

S. Otsuka, K. H. Bui, M. Schorb, M. J. Hossain, A. Z. Politi, B. Koch, M. Eltsov, M. Beck, and J. Ellenberg, “Nuclear pore assembly proceeds by an inside-out extrusion of the nuclear envelope,” eLife 5, 1–23 (2016).
[Crossref] [PubMed]

2015 (2)

L. Carlini, S. J. Holden, K. M. Douglass, and S. Manley, “Correction of a depth-dependent lateral distortion in 3d super-resolution imaging,” PLoS One 10(11), e0142949 (2015).
[Crossref] [PubMed]

D. Burke, B. Patton, F. Huang, J. Bewersdorf, and M. J. Booth, “Adaptive optics correction of specimen-induced aberrations in single-molecule switching microscopy,” Optica 2(2), 177–185 (2015).
[Crossref]

2014 (1)

2013 (3)

S. Liu, E. B. Kromann, W. D. Krueger, J. Bewersdorf, and K. A. Lidke, “Three dimensional single molecule localization using a phase retrieved pupil function,” Opt. Express 21(24), 29462–29487 (2013).
[Crossref] [PubMed]

D. Axelrod, “Evanescent excitation and emission in fluorescence microscopy,” Biophys. J. 104(7), 1401–1409 (2013).
[Crossref] [PubMed]

K. Xu, G. Zhong, and X. Zhuang, “Actin, spectrin, and associated proteins form a periodic cytoskeletal structure in axons,” Science 339(6118), 452–456 (2013).
[Crossref] [PubMed]

2012 (1)

J. Ries, C. Kaplan, E. Platonova, H. Eghlidi, and H. Ewers, “A simple, versatile method for GFP-based super-resolution microscopy via nanobodies,” Nat. Methods 9(6), 582–584 (2012).
[Crossref] [PubMed]

2011 (2)

S. van de Linde, A. Löschberger, T. Klein, M. Heidbreder, S. Wolter, M. Heilemann, and M. Sauer, “Direct stochastic optical reconstruction microscopy with standard fluorescent probes,” Nat. Protoc. 6(7), 991–1009 (2011).
[Crossref] [PubMed]

J. B. Doyon, B. Zeitler, J. Cheng, A. T. Cheng, J. M. Cherone, Y. Santiago, A. H. Lee, T. D. Vo, Y. Doyon, J. C. Miller, D. E. Paschon, L. Zhang, E. J. Rebar, P. D. Gregory, F. D. Urnov, and D. G. Drubin, “Rapid and efficient clathrin-mediated endocytosis revealed in genome-edited mammalian cells,” Nat. Cell Biol. 13(3), 331–337 (2011).
[Crossref] [PubMed]

2009 (2)

Y. Deng and J. W. Shaevitz, “Effect of aberration on height calibration in three-dimensional localization-based microscopy and particle tracking,” Appl. Opt. 48(10), 1886–1890 (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]

2008 (3)

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]

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]

B. Huang, S. A. Jones, B. Brandenburg, and X. Zhuang, “Whole-cell 3D STORM reveals interactions between cellular structures with nanometer-scale resolution,” Nat. Methods 5(12), 1047–1052 (2008).
[Crossref] [PubMed]

2004 (1)

B. M. Hanser, M. G. L. Gustafsson, D. A. Agard, and J. W. Sedat, “Phase-retrieved pupil functions in wide-field fluorescence microscopy,” J. Microsc. 216(Pt 1), 32–48 (2004).
[Crossref] [PubMed]

Agard, D. A.

B. M. Hanser, M. G. L. Gustafsson, D. A. Agard, and J. W. Sedat, “Phase-retrieved pupil functions in wide-field fluorescence microscopy,” J. Microsc. 216(Pt 1), 32–48 (2004).
[Crossref] [PubMed]

Aristov, A.

A. Aristov, B. Lelandais, E. Rensen, and C. Zimmer, “ZOLA-3D allows flexible 3D localization microscopy over an adjustable axial range,” Nat. Commun. 9(1), 2409 (2018).
[Crossref] [PubMed]

Axelrod, D.

D. Axelrod, “Evanescent excitation and emission in fluorescence microscopy,” Biophys. J. 104(7), 1401–1409 (2013).
[Crossref] [PubMed]

Babcock, H. P.

H. P. Babcock and X. Zhuang, “Analyzing single molecule localization microscopy data using cubic splines,” Sci. Rep. 7(1), 552 (2017).
[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]

Beck, M.

S. Otsuka, K. H. Bui, M. Schorb, M. J. Hossain, A. Z. Politi, B. Koch, M. Eltsov, M. Beck, and J. Ellenberg, “Nuclear pore assembly proceeds by an inside-out extrusion of the nuclear envelope,” eLife 5, 1–23 (2016).
[Crossref] [PubMed]

Bemiller, S. M.

M. J. Mlodzianoski, P. J. Cheng-Hathaway, S. M. Bemiller, T. J. McCray, S. Liu, D. A. Miller, B. T. Lamb, G. E. Landreth, and F. Huang, “Active PSF shaping and adaptive optics enable volumetric localization microscopy through brain sections,” Nat. Methods 15(8), 583–586 (2018).
[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]

Bewersdorf, J.

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]

Booth, M. J.

Bourg, N.

Brandenburg, B.

B. Huang, S. A. Jones, B. Brandenburg, and X. Zhuang, “Whole-cell 3D STORM reveals interactions between cellular structures with nanometer-scale resolution,” Nat. Methods 5(12), 1047–1052 (2008).
[Crossref] [PubMed]

Bui, K. H.

S. Otsuka, K. H. Bui, M. Schorb, M. J. Hossain, A. Z. Politi, B. Koch, M. Eltsov, M. Beck, and J. Ellenberg, “Nuclear pore assembly proceeds by an inside-out extrusion of the nuclear envelope,” eLife 5, 1–23 (2016).
[Crossref] [PubMed]

Burke, D.

Cabriel, C.

Carlini, L.

L. Carlini, S. J. Holden, K. M. Douglass, and S. Manley, “Correction of a depth-dependent lateral distortion in 3d super-resolution imaging,” PLoS One 10(11), e0142949 (2015).
[Crossref] [PubMed]

Cheng, A. T.

J. B. Doyon, B. Zeitler, J. Cheng, A. T. Cheng, J. M. Cherone, Y. Santiago, A. H. Lee, T. D. Vo, Y. Doyon, J. C. Miller, D. E. Paschon, L. Zhang, E. J. Rebar, P. D. Gregory, F. D. Urnov, and D. G. Drubin, “Rapid and efficient clathrin-mediated endocytosis revealed in genome-edited mammalian cells,” Nat. Cell Biol. 13(3), 331–337 (2011).
[Crossref] [PubMed]

Cheng, J.

J. B. Doyon, B. Zeitler, J. Cheng, A. T. Cheng, J. M. Cherone, Y. Santiago, A. H. Lee, T. D. Vo, Y. Doyon, J. C. Miller, D. E. Paschon, L. Zhang, E. J. Rebar, P. D. Gregory, F. D. Urnov, and D. G. Drubin, “Rapid and efficient clathrin-mediated endocytosis revealed in genome-edited mammalian cells,” Nat. Cell Biol. 13(3), 331–337 (2011).
[Crossref] [PubMed]

Cheng-Hathaway, P. J.

M. J. Mlodzianoski, P. J. Cheng-Hathaway, S. M. Bemiller, T. J. McCray, S. Liu, D. A. Miller, B. T. Lamb, G. E. Landreth, and F. Huang, “Active PSF shaping and adaptive optics enable volumetric localization microscopy through brain sections,” Nat. Methods 15(8), 583–586 (2018).
[Crossref] [PubMed]

Cherone, J. M.

J. B. Doyon, B. Zeitler, J. Cheng, A. T. Cheng, J. M. Cherone, Y. Santiago, A. H. Lee, T. D. Vo, Y. Doyon, J. C. Miller, D. E. Paschon, L. Zhang, E. J. Rebar, P. D. Gregory, F. D. Urnov, and D. G. Drubin, “Rapid and efficient clathrin-mediated endocytosis revealed in genome-edited mammalian cells,” Nat. Cell Biol. 13(3), 331–337 (2011).
[Crossref] [PubMed]

Chou, K. C.

R. Tafteh, D. R. L. Scriven, E. D. W. Moore, and K. C. Chou, “Single molecule localization deep within thick cells; a novel super-resolution microscope,” J. Biophotonics 9(1-2), 155–160 (2016).
[Crossref] [PubMed]

Deng, Y.

Deschamps, J.

Y. Li, M. Mund, P. Hoess, J. Deschamps, U. Matti, B. Nijmeijer, V. J. Sabinina, J. Ellenberg, I. Schoen, and J. Ries, “Real-time 3D single-molecule localization using experimental point spread functions,” Nat. Methods 15(5), 367–369 (2018).
[Crossref] [PubMed]

J. Deschamps, A. Rowald, and J. Ries, “Efficient homogeneous illumination and optical sectioning for quantitative single-molecule localization microscopy,” Opt. Express 24(24), 28080–28090 (2016).
[Crossref] [PubMed]

Douglass, K. M.

L. Carlini, S. J. Holden, K. M. Douglass, and S. Manley, “Correction of a depth-dependent lateral distortion in 3d super-resolution imaging,” PLoS One 10(11), e0142949 (2015).
[Crossref] [PubMed]

Doyon, J. B.

J. B. Doyon, B. Zeitler, J. Cheng, A. T. Cheng, J. M. Cherone, Y. Santiago, A. H. Lee, T. D. Vo, Y. Doyon, J. C. Miller, D. E. Paschon, L. Zhang, E. J. Rebar, P. D. Gregory, F. D. Urnov, and D. G. Drubin, “Rapid and efficient clathrin-mediated endocytosis revealed in genome-edited mammalian cells,” Nat. Cell Biol. 13(3), 331–337 (2011).
[Crossref] [PubMed]

Doyon, Y.

J. B. Doyon, B. Zeitler, J. Cheng, A. T. Cheng, J. M. Cherone, Y. Santiago, A. H. Lee, T. D. Vo, Y. Doyon, J. C. Miller, D. E. Paschon, L. Zhang, E. J. Rebar, P. D. Gregory, F. D. Urnov, and D. G. Drubin, “Rapid and efficient clathrin-mediated endocytosis revealed in genome-edited mammalian cells,” Nat. Cell Biol. 13(3), 331–337 (2011).
[Crossref] [PubMed]

Drubin, D. G.

J. B. Doyon, B. Zeitler, J. Cheng, A. T. Cheng, J. M. Cherone, Y. Santiago, A. H. Lee, T. D. Vo, Y. Doyon, J. C. Miller, D. E. Paschon, L. Zhang, E. J. Rebar, P. D. Gregory, F. D. Urnov, and D. G. Drubin, “Rapid and efficient clathrin-mediated endocytosis revealed in genome-edited mammalian cells,” Nat. Cell Biol. 13(3), 331–337 (2011).
[Crossref] [PubMed]

Dupuis, G.

Eghlidi, H.

J. Ries, C. Kaplan, E. Platonova, H. Eghlidi, and H. Ewers, “A simple, versatile method for GFP-based super-resolution microscopy via nanobodies,” Nat. Methods 9(6), 582–584 (2012).
[Crossref] [PubMed]

Ellenberg, J.

Y. Li, M. Mund, P. Hoess, J. Deschamps, U. Matti, B. Nijmeijer, V. J. Sabinina, J. Ellenberg, I. Schoen, and J. Ries, “Real-time 3D single-molecule localization using experimental point spread functions,” Nat. Methods 15(5), 367–369 (2018).
[Crossref] [PubMed]

S. Otsuka, K. H. Bui, M. Schorb, M. J. Hossain, A. Z. Politi, B. Koch, M. Eltsov, M. Beck, and J. Ellenberg, “Nuclear pore assembly proceeds by an inside-out extrusion of the nuclear envelope,” eLife 5, 1–23 (2016).
[Crossref] [PubMed]

Eltsov, M.

S. Otsuka, K. H. Bui, M. Schorb, M. J. Hossain, A. Z. Politi, B. Koch, M. Eltsov, M. Beck, and J. Ellenberg, “Nuclear pore assembly proceeds by an inside-out extrusion of the nuclear envelope,” eLife 5, 1–23 (2016).
[Crossref] [PubMed]

Ewers, H.

J. Ries, C. Kaplan, E. Platonova, H. Eghlidi, and H. Ewers, “A simple, versatile method for GFP-based super-resolution microscopy via nanobodies,” Nat. Methods 9(6), 582–584 (2012).
[Crossref] [PubMed]

Gould, T. 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]

Gregory, P. D.

J. B. Doyon, B. Zeitler, J. Cheng, A. T. Cheng, J. M. Cherone, Y. Santiago, A. H. Lee, T. D. Vo, Y. Doyon, J. C. Miller, D. E. Paschon, L. Zhang, E. J. Rebar, P. D. Gregory, F. D. Urnov, and D. G. Drubin, “Rapid and efficient clathrin-mediated endocytosis revealed in genome-edited mammalian cells,” Nat. Cell Biol. 13(3), 331–337 (2011).
[Crossref] [PubMed]

Gustafsson, M. G. L.

B. M. Hanser, M. G. L. Gustafsson, D. A. Agard, and J. W. Sedat, “Phase-retrieved pupil functions in wide-field fluorescence microscopy,” J. Microsc. 216(Pt 1), 32–48 (2004).
[Crossref] [PubMed]

Hanser, B. M.

B. M. Hanser, M. G. L. Gustafsson, D. A. Agard, and J. W. Sedat, “Phase-retrieved pupil functions in wide-field fluorescence microscopy,” J. Microsc. 216(Pt 1), 32–48 (2004).
[Crossref] [PubMed]

Heidbreder, M.

S. van de Linde, A. Löschberger, T. Klein, M. Heidbreder, S. Wolter, M. Heilemann, and M. Sauer, “Direct stochastic optical reconstruction microscopy with standard fluorescent probes,” Nat. Protoc. 6(7), 991–1009 (2011).
[Crossref] [PubMed]

Heilemann, M.

S. van de Linde, A. Löschberger, T. Klein, M. Heidbreder, S. Wolter, M. Heilemann, and M. Sauer, “Direct stochastic optical reconstruction microscopy with standard fluorescent probes,” Nat. Protoc. 6(7), 991–1009 (2011).
[Crossref] [PubMed]

Hess, S. 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]

Hoess, P.

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J. Ries, C. Kaplan, E. Platonova, H. Eghlidi, and H. Ewers, “A simple, versatile method for GFP-based super-resolution microscopy via nanobodies,” Nat. Methods 9(6), 582–584 (2012).
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Krueger, W. D.

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M. J. Mlodzianoski, P. J. Cheng-Hathaway, S. M. Bemiller, T. J. McCray, S. Liu, D. A. Miller, B. T. Lamb, G. E. Landreth, and F. Huang, “Active PSF shaping and adaptive optics enable volumetric localization microscopy through brain sections,” Nat. Methods 15(8), 583–586 (2018).
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J. B. Doyon, B. Zeitler, J. Cheng, A. T. Cheng, J. M. Cherone, Y. Santiago, A. H. Lee, T. D. Vo, Y. Doyon, J. C. Miller, D. E. Paschon, L. Zhang, E. J. Rebar, P. D. Gregory, F. D. Urnov, and D. G. Drubin, “Rapid and efficient clathrin-mediated endocytosis revealed in genome-edited mammalian cells,” Nat. Cell Biol. 13(3), 331–337 (2011).
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S. van de Linde, A. Löschberger, T. Klein, M. Heidbreder, S. Wolter, M. Heilemann, and M. Sauer, “Direct stochastic optical reconstruction microscopy with standard fluorescent probes,” Nat. Protoc. 6(7), 991–1009 (2011).
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L. Carlini, S. J. Holden, K. M. Douglass, and S. Manley, “Correction of a depth-dependent lateral distortion in 3d super-resolution imaging,” PLoS One 10(11), e0142949 (2015).
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Y. Li, M. Mund, P. Hoess, J. Deschamps, U. Matti, B. Nijmeijer, V. J. Sabinina, J. Ellenberg, I. Schoen, and J. Ries, “Real-time 3D single-molecule localization using experimental point spread functions,” Nat. Methods 15(5), 367–369 (2018).
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M. J. Mlodzianoski, P. J. Cheng-Hathaway, S. M. Bemiller, T. J. McCray, S. Liu, D. A. Miller, B. T. Lamb, G. E. Landreth, and F. Huang, “Active PSF shaping and adaptive optics enable volumetric localization microscopy through brain sections,” Nat. Methods 15(8), 583–586 (2018).
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Miller, D. A.

M. J. Mlodzianoski, P. J. Cheng-Hathaway, S. M. Bemiller, T. J. McCray, S. Liu, D. A. Miller, B. T. Lamb, G. E. Landreth, and F. Huang, “Active PSF shaping and adaptive optics enable volumetric localization microscopy through brain sections,” Nat. Methods 15(8), 583–586 (2018).
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J. B. Doyon, B. Zeitler, J. Cheng, A. T. Cheng, J. M. Cherone, Y. Santiago, A. H. Lee, T. D. Vo, Y. Doyon, J. C. Miller, D. E. Paschon, L. Zhang, E. J. Rebar, P. D. Gregory, F. D. Urnov, and D. G. Drubin, “Rapid and efficient clathrin-mediated endocytosis revealed in genome-edited mammalian cells,” Nat. Cell Biol. 13(3), 331–337 (2011).
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M. J. Mlodzianoski, P. J. Cheng-Hathaway, S. M. Bemiller, T. J. McCray, S. Liu, D. A. Miller, B. T. Lamb, G. E. Landreth, and F. Huang, “Active PSF shaping and adaptive optics enable volumetric localization microscopy through brain sections,” Nat. Methods 15(8), 583–586 (2018).
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A. von Diezmann, Y. Shechtman, and W. E. Moerner, “Three-dimensional localization of single molecules for super-resolution imaging and single-particle tracking,” Chem. Rev. 117(11), 7244–7275 (2017).
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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).
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R. Tafteh, D. R. L. Scriven, E. D. W. Moore, and K. C. Chou, “Single molecule localization deep within thick cells; a novel super-resolution microscope,” J. Biophotonics 9(1-2), 155–160 (2016).
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Y. Li, M. Mund, P. Hoess, J. Deschamps, U. Matti, B. Nijmeijer, V. J. Sabinina, J. Ellenberg, I. Schoen, and J. Ries, “Real-time 3D single-molecule localization using experimental point spread functions,” Nat. Methods 15(5), 367–369 (2018).
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P. Hoess, M. Mund, M. Reitberger, and J. Ries, “Dual-color and 3D super-resolution microscopy of multi-protein assemblies,” Methods Mol. Biol. 1764, 237–251 (2018).
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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).
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Y. Li, M. Mund, P. Hoess, J. Deschamps, U. Matti, B. Nijmeijer, V. J. Sabinina, J. Ellenberg, I. Schoen, and J. Ries, “Real-time 3D single-molecule localization using experimental point spread functions,” Nat. Methods 15(5), 367–369 (2018).
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J. B. Doyon, B. Zeitler, J. Cheng, A. T. Cheng, J. M. Cherone, Y. Santiago, A. H. Lee, T. D. Vo, Y. Doyon, J. C. Miller, D. E. Paschon, L. Zhang, E. J. Rebar, P. D. Gregory, F. D. Urnov, and D. G. Drubin, “Rapid and efficient clathrin-mediated endocytosis revealed in genome-edited mammalian cells,” Nat. Cell Biol. 13(3), 331–337 (2011).
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Pavani, S. R. P.

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).
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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).
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J. Ries, C. Kaplan, E. Platonova, H. Eghlidi, and H. Ewers, “A simple, versatile method for GFP-based super-resolution microscopy via nanobodies,” Nat. Methods 9(6), 582–584 (2012).
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S. Otsuka, K. H. Bui, M. Schorb, M. J. Hossain, A. Z. Politi, B. Koch, M. Eltsov, M. Beck, and J. Ellenberg, “Nuclear pore assembly proceeds by an inside-out extrusion of the nuclear envelope,” eLife 5, 1–23 (2016).
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J. B. Doyon, B. Zeitler, J. Cheng, A. T. Cheng, J. M. Cherone, Y. Santiago, A. H. Lee, T. D. Vo, Y. Doyon, J. C. Miller, D. E. Paschon, L. Zhang, E. J. Rebar, P. D. Gregory, F. D. Urnov, and D. G. Drubin, “Rapid and efficient clathrin-mediated endocytosis revealed in genome-edited mammalian cells,” Nat. Cell Biol. 13(3), 331–337 (2011).
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P. Hoess, M. Mund, M. Reitberger, and J. Ries, “Dual-color and 3D super-resolution microscopy of multi-protein assemblies,” Methods Mol. Biol. 1764, 237–251 (2018).
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A. Aristov, B. Lelandais, E. Rensen, and C. Zimmer, “ZOLA-3D allows flexible 3D localization microscopy over an adjustable axial range,” Nat. Commun. 9(1), 2409 (2018).
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P. Hoess, M. Mund, M. Reitberger, and J. Ries, “Dual-color and 3D super-resolution microscopy of multi-protein assemblies,” Methods Mol. Biol. 1764, 237–251 (2018).
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Y. Li, M. Mund, P. Hoess, J. Deschamps, U. Matti, B. Nijmeijer, V. J. Sabinina, J. Ellenberg, I. Schoen, and J. Ries, “Real-time 3D single-molecule localization using experimental point spread functions,” Nat. Methods 15(5), 367–369 (2018).
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J. Deschamps, A. Rowald, and J. Ries, “Efficient homogeneous illumination and optical sectioning for quantitative single-molecule localization microscopy,” Opt. Express 24(24), 28080–28090 (2016).
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J. Ries, C. Kaplan, E. Platonova, H. Eghlidi, and H. Ewers, “A simple, versatile method for GFP-based super-resolution microscopy via nanobodies,” Nat. Methods 9(6), 582–584 (2012).
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Sabinina, V. J.

Y. Li, M. Mund, P. Hoess, J. Deschamps, U. Matti, B. Nijmeijer, V. J. Sabinina, J. Ellenberg, I. Schoen, and J. Ries, “Real-time 3D single-molecule localization using experimental point spread functions,” Nat. Methods 15(5), 367–369 (2018).
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J. B. Doyon, B. Zeitler, J. Cheng, A. T. Cheng, J. M. Cherone, Y. Santiago, A. H. Lee, T. D. Vo, Y. Doyon, J. C. Miller, D. E. Paschon, L. Zhang, E. J. Rebar, P. D. Gregory, F. D. Urnov, and D. G. Drubin, “Rapid and efficient clathrin-mediated endocytosis revealed in genome-edited mammalian cells,” Nat. Cell Biol. 13(3), 331–337 (2011).
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Sauer, M.

S. van de Linde, A. Löschberger, T. Klein, M. Heidbreder, S. Wolter, M. Heilemann, and M. Sauer, “Direct stochastic optical reconstruction microscopy with standard fluorescent probes,” Nat. Protoc. 6(7), 991–1009 (2011).
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Schoen, I.

Y. Li, M. Mund, P. Hoess, J. Deschamps, U. Matti, B. Nijmeijer, V. J. Sabinina, J. Ellenberg, I. Schoen, and J. Ries, “Real-time 3D single-molecule localization using experimental point spread functions,” Nat. Methods 15(5), 367–369 (2018).
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S. Otsuka, K. H. Bui, M. Schorb, M. J. Hossain, A. Z. Politi, B. Koch, M. Eltsov, M. Beck, and J. Ellenberg, “Nuclear pore assembly proceeds by an inside-out extrusion of the nuclear envelope,” eLife 5, 1–23 (2016).
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Scriven, D. R. L.

R. Tafteh, D. R. L. Scriven, E. D. W. Moore, and K. C. Chou, “Single molecule localization deep within thick cells; a novel super-resolution microscope,” J. Biophotonics 9(1-2), 155–160 (2016).
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B. M. Hanser, M. G. L. Gustafsson, D. A. Agard, and J. W. Sedat, “Phase-retrieved pupil functions in wide-field fluorescence microscopy,” J. Microsc. 216(Pt 1), 32–48 (2004).
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Shechtman, Y.

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Tafteh, R.

R. Tafteh, D. R. L. Scriven, E. D. W. Moore, and K. C. Chou, “Single molecule localization deep within thick cells; a novel super-resolution microscope,” J. Biophotonics 9(1-2), 155–160 (2016).
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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).
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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).
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J. B. Doyon, B. Zeitler, J. Cheng, A. T. Cheng, J. M. Cherone, Y. Santiago, A. H. Lee, T. D. Vo, Y. Doyon, J. C. Miller, D. E. Paschon, L. Zhang, E. J. Rebar, P. D. Gregory, F. D. Urnov, and D. G. Drubin, “Rapid and efficient clathrin-mediated endocytosis revealed in genome-edited mammalian cells,” Nat. Cell Biol. 13(3), 331–337 (2011).
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S. van de Linde, A. Löschberger, T. Klein, M. Heidbreder, S. Wolter, M. Heilemann, and M. Sauer, “Direct stochastic optical reconstruction microscopy with standard fluorescent probes,” Nat. Protoc. 6(7), 991–1009 (2011).
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J. B. Doyon, B. Zeitler, J. Cheng, A. T. Cheng, J. M. Cherone, Y. Santiago, A. H. Lee, T. D. Vo, Y. Doyon, J. C. Miller, D. E. Paschon, L. Zhang, E. J. Rebar, P. D. Gregory, F. D. Urnov, and D. G. Drubin, “Rapid and efficient clathrin-mediated endocytosis revealed in genome-edited mammalian cells,” Nat. Cell Biol. 13(3), 331–337 (2011).
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A. von Diezmann, Y. Shechtman, and W. E. Moerner, “Three-dimensional localization of single molecules for super-resolution imaging and single-particle tracking,” Chem. Rev. 117(11), 7244–7275 (2017).
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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).
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S. van de Linde, A. Löschberger, T. Klein, M. Heidbreder, S. Wolter, M. Heilemann, and M. Sauer, “Direct stochastic optical reconstruction microscopy with standard fluorescent probes,” Nat. Protoc. 6(7), 991–1009 (2011).
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J. B. Doyon, B. Zeitler, J. Cheng, A. T. Cheng, J. M. Cherone, Y. Santiago, A. H. Lee, T. D. Vo, Y. Doyon, J. C. Miller, D. E. Paschon, L. Zhang, E. J. Rebar, P. D. Gregory, F. D. Urnov, and D. G. Drubin, “Rapid and efficient clathrin-mediated endocytosis revealed in genome-edited mammalian cells,” Nat. Cell Biol. 13(3), 331–337 (2011).
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Zhong, G.

K. Xu, G. Zhong, and X. Zhuang, “Actin, spectrin, and associated proteins form a periodic cytoskeletal structure in axons,” Science 339(6118), 452–456 (2013).
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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).
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A. Aristov, B. Lelandais, E. Rensen, and C. Zimmer, “ZOLA-3D allows flexible 3D localization microscopy over an adjustable axial range,” Nat. Commun. 9(1), 2409 (2018).
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eLife (1)

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Figures (5)

Fig. 1
Fig. 1 Schematic of the approach to calibrate the depth-dependent z-correction. (a) Fluorescent beads are embedded in agarose gel at random depths and are imaged at different focal planes. (b) Example of fitted z-position versus nominal focal plane position (objective position from piezo stage) for two beads at different heights (red and green in a). Due to aberrations, the fitted position is not linear with the nominal z position (focal plane). This allows us to determine the correction dz in dependence on the focal plane. (c) Calibration curve showing the correction dz of fitted z-values in dependence on the fitted z-values and the position of the focal plane above the coverslip. (d) In an SMLM experiment, the data is fitted with the same PSF model as the beads in gel, and the fitted z-positions of the fluorophores are corrected using the calibration from (c).
Fig. 2
Fig. 2 Correction of depth-induced aberrations. (a) 482 beads, embedded in an agarose gel, were fitted with a PSF model that was calibrated using beads on the coverslip. For deeper beads, the fitted z-position increasingly deviates from their distance from the focal plane. (b) Correction for fitted z-values in dependence on the fitted z-values and the position of the focal plane above the coverslip. (c) The left panel shows the fitted z-positions of 15 beads from new data sets at different depths in dependence on the distance of the bead from the focal plane. For beads not directly on the coverslip, these are not equal (root mean square (rms) error 171 nm, Pearson correlation coefficient c = 0.9847). The right panel shows the corrected z-positions, which now show a very high correlation with their distance from the focal plane (rms error 12 nm, Pearson correlation coefficient c = 0.9997). The color bar indicates the depth of the beads to coverslip.
Fig. 3
Fig. 3 Imaging of clathrin-coated pits. (a) Clathrin-coated pits, close to the coverslip, immunolabeled with Alexa Fluor 647 conjugated antibodies, measured using dSTORM [25] and fitted with an experimental PSF determined from beads on the coverslip. (b) Clathrin-coated pits on the upper cell membrane, imaged 2 µm above the coverslip using an oil objective, show deformations in the side-view reconstructions. After correction of aberration-induced artifacts the spherical shape of the pits is recovered. Width of the line profiles: 50 nm. Scale bars: 1 µm for x-y reconstruction panels and 100 nm for x-z reconstruction panels.
Fig. 4
Fig. 4 Imaging of nuclear pore complex protein Nup107 about 5 µm deep in the cell. (a) Nup107-SNAP-Alexa Fluor 647 imaged with dSTORM reconstructed by the PSF model obtained on the coverslip. (b) dSTORM image after applying the depth dependent z correction to a. (c) Side-view reconstruction of the region bounded by dashed line in a. (d) Side-view reconstruction of the same region as in c after applying the depth-dependent z-correction. Scale bars, 1 µm.
Fig. 5
Fig. 5 Imaging of Nup107 at 340 nm above the coverslip. (a) Nup107-SNAP-Alexa Fluor 647 imaged with dSTORM reconstructed by the PSF model obtained on the coverslip. (b) dSTORM image of a representative single NPC as indicated in the squared region in (a). Top images are x-y and x-z views. Bottom image is the intensity plot along z and a two Gaussian model was fitted on the data. (c) Side-view reconstruction of the region bounded by dashed lines in (a). (d) The distance of the two rings as a function of the central z position of each individual NPC before correction (Pearson correlation coefficient c = 0.55). (e) The distance of the two rings as a function of the central z position of each individual NPC after correction (Pearson correlation coefficient c = −0.03). Scale bars, (a) and (c) 1 µm, (b) 50 nm.