Abstract

In fluorescence microscopy, the serial acquisition of two-dimensional images to form a three-dimensional (3D) volume limits the maximum imaging speed. This is particularly evident when imaging adherent cells in a light-sheet fluorescence microscopy format, as their elongated morphologies require 200 image planes per image volume. Here, by illuminating the specimen with three light sheets, each independently detected, we present a light-efficient, crosstalk-free, and volumetrically parallelized 3D microscopy technique that is optimized for high-speed (up to 14 Hz) subcellular (300 nm lateral, 600 nm axial resolution) imaging of adherent cells. We demonstrate 3D imaging of intracellular processes, including cytoskeletal dynamics in single-cell migration and collective wound healing for 1500 and 1000 time points, respectively. Furthermore, we capture rapid biological processes, including the trafficking of early endosomes with velocities exceeding 10 μm/s and calcium signaling in primary neurons.

© 2017 Optical Society of America

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References

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    [Crossref]
  24. R. D. Vale, “The molecular motor toolbox for intracellular transport,” Cell 112, 467–480 (2003).
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  25. W. Qiu, N. D. Derr, B. S. Goodman, E. Villa, D. Wu, W. Shih, and S. L. Reck-Peterson, “Dynein achieves processive motion using both stochastic and coordinated stepping,” Nat. Struct. Mol. Biol. 19, 193–200 (2012).
    [Crossref]
  26. A. M. Delprato, N. Flores-Rodriguez, S. S. Rogers, D. A. Kenwright, T. A. Waigh, P. G. Woodman, and V. J. Allan, “Roles of dynein and dynactin in early endosome dynamics revealed using automated tracking and global analysis,” PLoS ONE 6, e24479 (2011).
    [Crossref]
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    [Crossref]
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    [Crossref]
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    [Crossref]
  30. G. Schitter, P. Menold, H. F. Knapp, F. Allgöwer, and A. Stemmer, “High performance feedback for fast scanning atomic force microscopes,” Rev. Sci. Instrum. 72, 3320–3327 (2001).
    [Crossref]
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    [Crossref]
  32. T. V. Truong, W. Supatto, D. S. Koos, J. M. Choi, and S. E. Fraser, “Deep and fast live imaging with two-photon scanned light-sheet microscopy,” Nat. Methods 8, 757–760 (2011).
    [Crossref]
  33. E. S. Welf, M. K. Driscoll, K. M. Dean, C. Schäfer, J. Chu, M. W. Davidson, M. Z. Lin, G. Danuser, and R. Fiolka, “Quantitative multiscale cell imaging in controlled 3D microenvironments,” Dev. Cell 36, 462–475 (2016).
    [Crossref]
  34. H. H. Bock and J. Herz, “Reelin activates SRC family tyrosine kinases in neurons,” Curr. Biol. 13, 18–26 (2003).
    [Crossref]

2016 (6)

K. M. Dean, P. Roudot, C. R. Reis, E. S. Welf, M. Mettlen, and R. Fiolka, “Diagonally scanned light-sheet microscopy for fast volumetric imaging of adherent cells,” Biophys. J. 110, 1456–1465 (2016).
[Crossref]

S. Quirin, N. Vladimirov, C.-T. Yang, D. S. Peterka, R. Yuste, and M. Ahrens, “Calcium imaging of neural circuits with extended depth-of-field light-sheet microscopy,” Opt. Lett. 41, 855–858 (2016).
[Crossref]

M. B. Sikkel, S. Kumar, V. Maioli, C. Rowlands, F. Gordon, S. E. Harding, A. R. Lyon, K. T. MacLeod, and C. Dunsby, “High speed sCMOS-based oblique plane microscopy applied to the study of calcium dynamics in cardiac myocytes,” J. Biophoton. 9, 311–323 (2016).
[Crossref]

S. Abrahamsson, R. Ilic, J. Wisniewski, B. Mehl, L. Yu, L. Chen, M. Davanco, L. Oudjedi, J.-B. Fiche, B. Hajj, X. Jin, J. Pulupa, C. Cho, M. Mir, M. El Beheiry, X. Darzacq, M. Nollmann, M. Dahan, C. Wu, T. Lionnet, J. A. Liddle, and C. I. Bargmann, “Multifocus microscopy with precise color multi-phase diffractive optics applied in functional neuronal imaging,” Biomed. Opt. Express 7, 855–869 (2016).
[Crossref]

Q. Ma, B. Khademhosseinieh, E. Huang, H. Qian, M. A. Bakowski, E. R. Troemel, and Z. Liu, “Three-dimensional fluorescent microscopy via simultaneous illumination and detection at multiple planes,” Sci. Rep. 6, 31445 (2016).
[Crossref]

E. S. Welf, M. K. Driscoll, K. M. Dean, C. Schäfer, J. Chu, M. W. Davidson, M. Z. Lin, G. Danuser, and R. Fiolka, “Quantitative multiscale cell imaging in controlled 3D microenvironments,” Dev. Cell 36, 462–475 (2016).
[Crossref]

2015 (8)

K. M. Dean, P. Roudot, E. S. Welf, G. Danuser, and R. Fiolka, “Deconvolution-free subcellular imaging with axially swept light sheet microscopy,” Biophys. J. 108, 2807–2815 (2015).
[Crossref]

S. Wäldchen, J. Lehmann, T. Klein, S. van de Linde, and M. Sauer, “Light-induced cell damage in live-cell super-resolution microscopy,” Sci. Rep. 5, 15348 (2015).
[Crossref]

R. K. Chhetri, F. Amat, Y. Wan, B. Höckendorf, W. C. Lemon, and P. J. Keller, “Whole-animal functional and developmental imaging with isotropic spatial resolution,” Nat. Methods 12, 1171–1178 (2015).
[Crossref]

M. B. Bouchard, V. Voleti, C. S. Mendes, C. Lacefield, W. B. Grueber, R. S. Mann, R. M. Bruno, and E. M. C. Hillman, “Swept confocally-aligned planar excitation (SCAPE) microscopy for high-speed volumetric imaging of behaving organisms,” Nat. Photonics 9, 113–119 (2015).
[Crossref]

L. Kong, J. Tang, J. P. Little, Y. Yu, T. Lämmermann, C. P. Lin, R. N. Germain, and M. Cui, “Continuous volumetric imaging via an optical phase-locked ultrasound lens,” Nat. Methods 12, 759–762 (2015).
[Crossref]

M. A. Cianfrocco, M. E. DeSantis, A. E. Leschziner, and S. L. Reck-Peterson, “Mechanism and regulation of cytoplasmic dynein,” Annu. Rev. Cell Dev. Biol. 31, 83–108 (2015).
[Crossref]

R. Tomer, M. Lovett-Barron, I. Kauvar, A. Andalman, V. M. Burns, S. Sankaran, L. Grosenick, M. Broxton, S. Yang, and K. Deisseroth, “SPED light sheet microscopy: Fast mapping of biological system structure and function,” Cell 163, 1796–1806 (2015).
[Crossref]

Y.-J. Liu, M. Le Berre, F. Lautenschlaeger, P. Maiuri, A. Callan-Jones, M. Heuzé, T. Takaki, R. Voituriez, and M. Piel, “Confinement and low adhesion induce fast amoeboid migration of slow mesenchymal cells,” Cell 160, 659–672 (2015).
[Crossref]

2014 (6)

K. M. Dean and A. E. Palmer, “Advances in fluorescence labeling strategies for dynamic cellular imaging,” Nat. Chem. Biol. 10, 512–523 (2014).
[Crossref]

G. Danuser, “Reply to ‘acquisition frame rate affects microtubule plus-end tracking analysis’,” Nat. Methods 11, 220 (2014).
[Crossref]

B. C. Chen, W. R. Legant, K. Wang, L. Shao, D. E. Milkie, M. W. Davidson, C. Janetopoulos, X. S. Wu, J. A. Hammer, Z. Liu, B. P. English, Y. Mimori-Kiyosue, D. P. Romero, A. T. Ritter, J. Lippincott-Schwartz, L. Fritz-Laylin, R. D. Mullins, D. M. Mitchell, J. N. Bembenek, A. C. Reymann, R. Bohme, S. W. Grill, J. T. Wang, G. Seydoux, U. S. Tulu, D. P. Kiehart, and E. Betzig, “Lattice light-sheet microscopy: Imaging molecules to embryos at high spatiotemporal resolution,” Science 346, 1257998 (2014).
[Crossref]

B. Hajj, J. Wisniewski, M. El Beheiry, J. Chen, A. Revyakin, C. Wu, and M. Dahan, “Whole-cell, multicolor superresolution imaging using volumetric multifocus microscopy,” Proc. Natl. Acad. Sci. USA 111, 17480–17485 (2014).

P. W. Winter and H. Shroff, “Faster fluorescence microscopy: Advances in high speed biological imaging,” Curr. Opin. Chem. Biol. 20, 46–53 (2014).
[Crossref]

S. Geissbuehler, A. Sharipov, A. Godinat, N. L. Bocchio, P. A. Sandoz, A. Huss, N. A. Jensen, S. Jakobs, J. Enderlein, F. Gisou van der Goot, E. A. Dubikovskaya, T. Lasser, and M. Leutenegger, “Live-cell multiplane three-dimensional super-resolution optical fluctuation imaging,” Nat. Commun. 5, 5830 (2014).
[Crossref]

2013 (3)

F. O. Fahrbach, F. F. Voigt, B. Schmid, F. Helmchen, and J. Huisken, “Rapid 3D light-sheet microscopy with a tunable lens,” Opt. Express 21, 21010–21026 (2013).
[Crossref]

T.-W. Chen, T. J. Wardill, Y. Sun, S. R. Pulver, S. L. Renninger, A. Baohan, E. R. Schreiter, R. A. Kerr, M. B. Orger, V. Jayaraman, L. L. Looger, K. Svoboda, and D. S. Kim, “Ultrasensitive fluorescent proteins for imaging neuronal activity,” Nature 499, 295–300 (2013).
[Crossref]

A. G. York, P. Chandris, D. D. Nogare, J. Head, P. Wawrzusin, R. S. Fischer, A. Chitnis, and H. Shroff, “Instant super-resolution imaging in live cells and embryos via analog image processing,” Nat. Methods 10, 1122–1126 (2013).
[Crossref]

2012 (3)

W. Qiu, N. D. Derr, B. S. Goodman, E. Villa, D. Wu, W. Shih, and S. L. Reck-Peterson, “Dynein achieves processive motion using both stochastic and coordinated stepping,” Nat. Struct. Mol. Biol. 19, 193–200 (2012).
[Crossref]

E. J. Botcherby, C. W. Smith, M. M. Kohl, D. Debarre, M. J. Booth, R. Juskaitis, O. Paulsen, and T. Wilson, “Aberration-free three-dimensional multiphoton imaging of neuronal activity at kHz rates,” Proc. Natl. Acad. Sci. USA 109, 2919–2924 (2012).

S. Abrahamsson, J. Chen, B. Hajj, S. Stallinga, A. Y. Katsov, J. Wisniewski, G. Mizuguchi, P. Soule, F. Mueller, C. D. Darzacq, X. Darzacq, C. Wu, C. I. Bargmann, D. A. Agard, M. Dahan, and M. G. L. Gustafsson, “Fast multicolor 3D imaging using aberration-corrected multifocus microscopy,” Nat. Methods 10, 60–63 (2012).
[Crossref]

2011 (3)

S. Kumar, D. Wilding, M. B. Sikkel, A. R. Lyon, K. T. MacLeod, and C. Dunsby, “High-speed 2D and 3D fluorescence microscopy of cardiac myocytes,” Opt. Express 19, 13839–13847 (2011).
[Crossref]

A. M. Delprato, N. Flores-Rodriguez, S. S. Rogers, D. A. Kenwright, T. A. Waigh, P. G. Woodman, and V. J. Allan, “Roles of dynein and dynactin in early endosome dynamics revealed using automated tracking and global analysis,” PLoS ONE 6, e24479 (2011).
[Crossref]

T. V. Truong, W. Supatto, D. S. Koos, J. M. Choi, and S. E. Fraser, “Deep and fast live imaging with two-photon scanned light-sheet microscopy,” Nat. Methods 8, 757–760 (2011).
[Crossref]

2009 (1)

J. Huisken and D. Y. R. Stainier, “Selective plane illumination microscopy techniques in developmental biology,” Development 136, 1963–1975 (2009).
[Crossref]

2008 (1)

K. Jaqaman, D. Loerke, M. Mettlen, H. Kuwata, S. Grinstein, S. L. Schmid, and G. Danuser, “Robust single-particle tracking in live-cell time-lapse sequences,” Nat. Methods 5, 695–702 (2008).
[Crossref]

2003 (2)

R. D. Vale, “The molecular motor toolbox for intracellular transport,” Cell 112, 467–480 (2003).
[Crossref]

H. H. Bock and J. Herz, “Reelin activates SRC family tyrosine kinases in neurons,” Curr. Biol. 13, 18–26 (2003).
[Crossref]

2001 (1)

G. Schitter, P. Menold, H. F. Knapp, F. Allgöwer, and A. Stemmer, “High performance feedback for fast scanning atomic force microscopes,” Rev. Sci. Instrum. 72, 3320–3327 (2001).
[Crossref]

Abrahamsson, S.

S. Abrahamsson, R. Ilic, J. Wisniewski, B. Mehl, L. Yu, L. Chen, M. Davanco, L. Oudjedi, J.-B. Fiche, B. Hajj, X. Jin, J. Pulupa, C. Cho, M. Mir, M. El Beheiry, X. Darzacq, M. Nollmann, M. Dahan, C. Wu, T. Lionnet, J. A. Liddle, and C. I. Bargmann, “Multifocus microscopy with precise color multi-phase diffractive optics applied in functional neuronal imaging,” Biomed. Opt. Express 7, 855–869 (2016).
[Crossref]

S. Abrahamsson, J. Chen, B. Hajj, S. Stallinga, A. Y. Katsov, J. Wisniewski, G. Mizuguchi, P. Soule, F. Mueller, C. D. Darzacq, X. Darzacq, C. Wu, C. I. Bargmann, D. A. Agard, M. Dahan, and M. G. L. Gustafsson, “Fast multicolor 3D imaging using aberration-corrected multifocus microscopy,” Nat. Methods 10, 60–63 (2012).
[Crossref]

Agard, D. A.

S. Abrahamsson, J. Chen, B. Hajj, S. Stallinga, A. Y. Katsov, J. Wisniewski, G. Mizuguchi, P. Soule, F. Mueller, C. D. Darzacq, X. Darzacq, C. Wu, C. I. Bargmann, D. A. Agard, M. Dahan, and M. G. L. Gustafsson, “Fast multicolor 3D imaging using aberration-corrected multifocus microscopy,” Nat. Methods 10, 60–63 (2012).
[Crossref]

Ahrens, M.

Allan, V. J.

A. M. Delprato, N. Flores-Rodriguez, S. S. Rogers, D. A. Kenwright, T. A. Waigh, P. G. Woodman, and V. J. Allan, “Roles of dynein and dynactin in early endosome dynamics revealed using automated tracking and global analysis,” PLoS ONE 6, e24479 (2011).
[Crossref]

Allgöwer, F.

G. Schitter, P. Menold, H. F. Knapp, F. Allgöwer, and A. Stemmer, “High performance feedback for fast scanning atomic force microscopes,” Rev. Sci. Instrum. 72, 3320–3327 (2001).
[Crossref]

Amat, F.

R. K. Chhetri, F. Amat, Y. Wan, B. Höckendorf, W. C. Lemon, and P. J. Keller, “Whole-animal functional and developmental imaging with isotropic spatial resolution,” Nat. Methods 12, 1171–1178 (2015).
[Crossref]

Andalman, A.

R. Tomer, M. Lovett-Barron, I. Kauvar, A. Andalman, V. M. Burns, S. Sankaran, L. Grosenick, M. Broxton, S. Yang, and K. Deisseroth, “SPED light sheet microscopy: Fast mapping of biological system structure and function,” Cell 163, 1796–1806 (2015).
[Crossref]

Bakowski, M. A.

Q. Ma, B. Khademhosseinieh, E. Huang, H. Qian, M. A. Bakowski, E. R. Troemel, and Z. Liu, “Three-dimensional fluorescent microscopy via simultaneous illumination and detection at multiple planes,” Sci. Rep. 6, 31445 (2016).
[Crossref]

Baohan, A.

T.-W. Chen, T. J. Wardill, Y. Sun, S. R. Pulver, S. L. Renninger, A. Baohan, E. R. Schreiter, R. A. Kerr, M. B. Orger, V. Jayaraman, L. L. Looger, K. Svoboda, and D. S. Kim, “Ultrasensitive fluorescent proteins for imaging neuronal activity,” Nature 499, 295–300 (2013).
[Crossref]

Bargmann, C. I.

S. Abrahamsson, R. Ilic, J. Wisniewski, B. Mehl, L. Yu, L. Chen, M. Davanco, L. Oudjedi, J.-B. Fiche, B. Hajj, X. Jin, J. Pulupa, C. Cho, M. Mir, M. El Beheiry, X. Darzacq, M. Nollmann, M. Dahan, C. Wu, T. Lionnet, J. A. Liddle, and C. I. Bargmann, “Multifocus microscopy with precise color multi-phase diffractive optics applied in functional neuronal imaging,” Biomed. Opt. Express 7, 855–869 (2016).
[Crossref]

S. Abrahamsson, J. Chen, B. Hajj, S. Stallinga, A. Y. Katsov, J. Wisniewski, G. Mizuguchi, P. Soule, F. Mueller, C. D. Darzacq, X. Darzacq, C. Wu, C. I. Bargmann, D. A. Agard, M. Dahan, and M. G. L. Gustafsson, “Fast multicolor 3D imaging using aberration-corrected multifocus microscopy,” Nat. Methods 10, 60–63 (2012).
[Crossref]

Bembenek, J. N.

B. C. Chen, W. R. Legant, K. Wang, L. Shao, D. E. Milkie, M. W. Davidson, C. Janetopoulos, X. S. Wu, J. A. Hammer, Z. Liu, B. P. English, Y. Mimori-Kiyosue, D. P. Romero, A. T. Ritter, J. Lippincott-Schwartz, L. Fritz-Laylin, R. D. Mullins, D. M. Mitchell, J. N. Bembenek, A. C. Reymann, R. Bohme, S. W. Grill, J. T. Wang, G. Seydoux, U. S. Tulu, D. P. Kiehart, and E. Betzig, “Lattice light-sheet microscopy: Imaging molecules to embryos at high spatiotemporal resolution,” Science 346, 1257998 (2014).
[Crossref]

Betzig, E.

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Supplementary Material (8)

NameDescription
» Supplement 1: PDF (3837 KB)      Supplemental Information
» Visualization 1: AVI (13199 KB)      Visualization 1
» Visualization 2: AVI (10937 KB)      Visualization 2
» Visualization 3: AVI (1710 KB)      Visualization 3
» Visualization 4: AVI (2084 KB)      Visualization 4
» Visualization 5: AVI (7653 KB)      Visualization 5
» Visualization 6: AVI (8440 KB)      Visualization 6
» Visualization 7: AVI (11343 KB)      Visualization 7

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Figures (4)

Fig. 1.
Fig. 1.

Optical principle and imaging performance of pLSFM. (A) Three axially and laterally staggered light sheets (blue) illuminate different sections of a specimen. Fluorescence (green) is only generated within the beam waist of each light sheet. (B) Image of staggered light sheets in a solution of fluorescein. Scale bar 20 μm. (C) Simplified diagram of detection light path. Owing to their lateral and axial displacement, the fluorescence from each section can be independently detected in image space. (D) 3D rendering of volumetric pLSFM data before and (E) after stitching. (F) Lateral and axial point-spread functions for the three cameras before and after 10 iterations of Richardson–Lucy deconvolution. Scale bar 1 μm. (G) Sagittal cross section of cell shown in (E). Scale bar 10 μm. (H)–(K): Cross sections from G, shown normal to the coverslip. Scale bar 10 μm.

Fig. 2.
Fig. 2.

pLSFM enables sensitive time-lapse imaging. (A) 3D rendering of migrating MDA-MB-231 breast cancer cell as imaged by pLSFM, labeled with GFP-Tractin. (B) 3D rendering of same cell after 750 and (C) 1500 time points. (D) Wound healing response in collectively migrating and genome edited RPE cells heterozygously expressing GFP-vimentin. Lateral ( X Y ) maximum intensity projection. (E) Single-plane cross sections normal to the coverslip show the distribution of vimentin at both the dorsal and ventral surfaces of migrating cells. Each plane taken from different positions relative to the front of the migrating epithelial sheet. (F) Lateral maximum intensity projection of filopodial dynamics in an RPE cell, labeled with LifeAct-mNeonGreen. (G) Montage of filopodia formation from subregion in (F). (H) Dynamics of microtubule plus tips ( + TIPs ), labeled with EB3-mNeonGreen, in a confluent layer of U2OS cells, shown as a lateral maximum intensity projection. (I) Photobleaching comparison between pLSFM ( N = 6 ) and single-plane LSFM ( N = 8 ). The mean normalized intensity is shown, and the error bars report the standard deviation. For each mode, the camera integration time and illumination intensity remained constant. pLSFM achieves 2.7-fold faster volumetric image acquisition rate than single-plane LSFM, without increasing the rate of photobleaching. All scale bars are 10 μm.

Fig. 3.
Fig. 3.

pLSFM enables the observation of rapid vesicular dynamics in 3D. (A) Dynamics of Rab5a vesicles, visualized at a volumetric image acquisition rate of 2.92 Hz over 500 time points. Maximum intensity projection parallel to the coverslip and in the lateral imaging plane for top and bottom panels, respectively. Scale bar 10 μm. (B) Montage of vesicle translocation toward the dorsal surface of the cell from the subregion in (A). Image contrast has been inverted to better highlight weak features. Scale bar 5 μm. (C) Rapid Rab5a-vesicle movement in an RPE cell, volumetrically imaged at 7.26 Hz, for 400 time points, shown as a lateral maximum intensity projection. Scale bar 10 μm. (D) Selected tracks of Rab5a-vesicle undergoing directed transport pseudocoloring according to their maximum velocity shown on top of all cumulative tracks detected in this area from the subregion in (C).

Fig. 4.
Fig. 4.

Calcium signaling in primary cortical neurons visualized with pLSFM. (A) 3D rendering of primary cortical neurons labeled with GCaMP-6f. Action potentials were volumetrically imaged at 14.37 Hz for 500 time points. (B) Propagation of a calcium wave through a dendritic arbor. Subregion from (A). (C) Kymograph of action potential propagating along dendrite shown in (B). (D) Temporal analysis of calcium bursts from regions specified in (A). (E) Dense, overlapping region of axonal projections from region specified in (A). Image shown as a maximum intensity projection parallel to the coverslip. (F) Cross section normal to the coverslip of the boxed region in (E), shown as a maximum intensity projection over a depth of 3.2 μm. Arrows point at crossing dendrites that are also labeled in (E). Scale bar 10 μm.

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