Abstract

We describe an angular multiplexed imaging technique for 3-D in vivo cell tracking of sparse cell distributions and optical projection tomography (OPT) with superior time-lapse resolution and a significantly reduced light dose compared to volumetric time-lapse techniques. We demonstrate that using dual axis OPT, where two images are acquired simultaneously at different projection angles, can enable localization and tracking of features in 3-D with a time resolution equal to the camera frame rate. This is achieved with a 200x reduction in light dose compared to an equivalent volumetric time-lapse single camera OPT acquisition with 200 projection angles. We demonstrate the application of this technique to mapping the 3-D neutrophil migration pattern observed over ~25.5 minutes in a live 2 day post-fertilisation transgenic LysC:GFP zebrafish embryo following a tail wound.

© 2015 Optical Society of America

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2014 (1)

2013 (1)

2012 (2)

R. Patalay, C. Talbot, Y. Alexandrov, M. O. Lenz, S. Kumar, S. Warren, I. Munro, M. A. A. Neil, K. König, P. M. W. French, A. Chu, G. W. H. Stamp, and C. Dunsby, “Multiphoton multispectral fluorescence lifetime tomography for the evaluation of basal cell carcinomas,” PLoS ONE 7(9), e43460 (2012).
[Crossref] [PubMed]

F. de Chaumont, S. Dallongeville, N. Chenouard, N. Hervé, S. Pop, T. Provoost, V. Meas-Yedid, P. Pankajakshan, T. Lecomte, Y. Le Montagner, T. Lagache, A. Dufour, and J. C. Olivo-Marin, “Icy: an open bioimage informatics platform for extended reproducible research,” Nat. Methods 9(7), 690–696 (2012), http://icy.bioimageanalysis.org .
[Crossref] [PubMed]

2011 (1)

S. K. Yoo, T. W. Starnes, Q. Deng, and A. Huttenlocher, “Lyn is a redox sensor that mediates leukocyte wound attraction in vivo,” Nature 480(7375), 109–112 (2011).
[Crossref] [PubMed]

2009 (1)

P. Niethammer, C. Grabher, A. T. Look, and T. J. Mitchison, “A tissue-scale gradient of hydrogen peroxide mediates rapid wound detection in zebrafish,” Nature 459(7249), 996–999 (2009).
[Crossref] [PubMed]

2008 (1)

A. F. Santos, A. B. Zaltsman, R. C. Martin, A. Kuzmin, Y. Alexandrov, E. P. Roquemore, R. A. Jessop, M. G. van Erck, and J. H. Verheijen, “Angiogenesis: an improved in vitro biological system and automated image-based workflow to aid identification and characterization of angiogenesis and angiogenic modulators,” Assay Drug Dev. Technol. 6(5), 693–710 (2008).
[Crossref] [PubMed]

2007 (1)

H. U. Dodt, U. Leischner, A. Schierloh, N. Jährling, C. P. Mauch, K. Deininger, J. M. Deussing, M. Eder, W. Zieglgänsberger, and K. Becker, “Ultramicroscopy: three-dimensional visualization of neuronal networks in the whole mouse brain,” Nat. Methods 4(4), 331–336 (2007).
[Crossref] [PubMed]

2006 (1)

J. R. Mathias, B. J. Perrin, T. X. Liu, J. Kanki, A. T. Look, and A. Huttenlocher, “Resolution of inflammation by retrograde chemotaxis of neutrophils in transgenic zebrafish,” J. Leukoc. Biol. 80(6), 1281–1288 (2006).
[Crossref] [PubMed]

2005 (3)

B. Stramer, W. Wood, M. J. Galko, M. J. Redd, A. Jacinto, S. M. Parkhurst, and P. Martin, “Live imaging of wound inflammation in Drosophila embryos reveals key roles for small GTPases during in vivo cell migration,” J. Cell Biol. 168(4), 567–573 (2005).
[Crossref] [PubMed]

J. A. Conchello and J. W. Lichtman, “Optical sectioning microscopy,” Nat. Methods 2(12), 920–931 (2005).
[Crossref] [PubMed]

M. Fauver, E. J. Seibel, J. R. Rahn, M. G. Meyer, F. Patten, T. Neumann, and A. C. Nelson, “Three-dimensional imaging of single isolated cell nuclei using optical projection tomography,” Opt. Express 13(11), 4210–4223 (2005).
[Crossref] [PubMed]

2004 (1)

J. Huisken, J. Swoger, F. Del Bene, J. Wittbrodt, and E. H. K. Stelzer, “Optical sectioning deep inside live embryos by selective plane illumination microscopy,” Science 305(5686), 1007–1009 (2004).
[Crossref] [PubMed]

2002 (1)

J. Sharpe, U. Ahlgren, P. Perry, B. Hill, A. Ross, J. Hecksher-Sørensen, R. Baldock, and D. Davidson, “Optical projection tomography as a tool for 3D microscopy and gene expression studies,” Science 296(5567), 541–545 (2002).
[Crossref] [PubMed]

1997 (1)

Y. Barad, H. Eisenberg, M. Horowitz, and Y. Silberberg, “Nonlinear scanning laser microscopy by third harmonic generation,” Appl. Phys. Lett. 70(8), 922–924 (1997).
[Crossref]

1990 (1)

W. Denk, J. H. Strickler, and W. W. Webb, “2-Photon Laser Scanning Fluorescence Microscopy,” Science 248(4951), 73–76 (1990).
[Crossref]

Ahlgren, U.

J. Sharpe, U. Ahlgren, P. Perry, B. Hill, A. Ross, J. Hecksher-Sørensen, R. Baldock, and D. Davidson, “Optical projection tomography as a tool for 3D microscopy and gene expression studies,” Science 296(5567), 541–545 (2002).
[Crossref] [PubMed]

Alexandrov, Y.

R. Patalay, C. Talbot, Y. Alexandrov, M. O. Lenz, S. Kumar, S. Warren, I. Munro, M. A. A. Neil, K. König, P. M. W. French, A. Chu, G. W. H. Stamp, and C. Dunsby, “Multiphoton multispectral fluorescence lifetime tomography for the evaluation of basal cell carcinomas,” PLoS ONE 7(9), e43460 (2012).
[Crossref] [PubMed]

A. F. Santos, A. B. Zaltsman, R. C. Martin, A. Kuzmin, Y. Alexandrov, E. P. Roquemore, R. A. Jessop, M. G. van Erck, and J. H. Verheijen, “Angiogenesis: an improved in vitro biological system and automated image-based workflow to aid identification and characterization of angiogenesis and angiogenic modulators,” Assay Drug Dev. Technol. 6(5), 693–710 (2008).
[Crossref] [PubMed]

Andrews, N.

Baldock, R.

J. Sharpe, U. Ahlgren, P. Perry, B. Hill, A. Ross, J. Hecksher-Sørensen, R. Baldock, and D. Davidson, “Optical projection tomography as a tool for 3D microscopy and gene expression studies,” Science 296(5567), 541–545 (2002).
[Crossref] [PubMed]

Barad, Y.

Y. Barad, H. Eisenberg, M. Horowitz, and Y. Silberberg, “Nonlinear scanning laser microscopy by third harmonic generation,” Appl. Phys. Lett. 70(8), 922–924 (1997).
[Crossref]

Becker, K.

H. U. Dodt, U. Leischner, A. Schierloh, N. Jährling, C. P. Mauch, K. Deininger, J. M. Deussing, M. Eder, W. Zieglgänsberger, and K. Becker, “Ultramicroscopy: three-dimensional visualization of neuronal networks in the whole mouse brain,” Nat. Methods 4(4), 331–336 (2007).
[Crossref] [PubMed]

Chen, L.

Chenouard, N.

F. de Chaumont, S. Dallongeville, N. Chenouard, N. Hervé, S. Pop, T. Provoost, V. Meas-Yedid, P. Pankajakshan, T. Lecomte, Y. Le Montagner, T. Lagache, A. Dufour, and J. C. Olivo-Marin, “Icy: an open bioimage informatics platform for extended reproducible research,” Nat. Methods 9(7), 690–696 (2012), http://icy.bioimageanalysis.org .
[Crossref] [PubMed]

Chu, A.

R. Patalay, C. Talbot, Y. Alexandrov, M. O. Lenz, S. Kumar, S. Warren, I. Munro, M. A. A. Neil, K. König, P. M. W. French, A. Chu, G. W. H. Stamp, and C. Dunsby, “Multiphoton multispectral fluorescence lifetime tomography for the evaluation of basal cell carcinomas,” PLoS ONE 7(9), e43460 (2012).
[Crossref] [PubMed]

Conchello, J. A.

J. A. Conchello and J. W. Lichtman, “Optical sectioning microscopy,” Nat. Methods 2(12), 920–931 (2005).
[Crossref] [PubMed]

Dallman, M. J.

Dallongeville, S.

F. de Chaumont, S. Dallongeville, N. Chenouard, N. Hervé, S. Pop, T. Provoost, V. Meas-Yedid, P. Pankajakshan, T. Lecomte, Y. Le Montagner, T. Lagache, A. Dufour, and J. C. Olivo-Marin, “Icy: an open bioimage informatics platform for extended reproducible research,” Nat. Methods 9(7), 690–696 (2012), http://icy.bioimageanalysis.org .
[Crossref] [PubMed]

Davidson, D.

J. Sharpe, U. Ahlgren, P. Perry, B. Hill, A. Ross, J. Hecksher-Sørensen, R. Baldock, and D. Davidson, “Optical projection tomography as a tool for 3D microscopy and gene expression studies,” Science 296(5567), 541–545 (2002).
[Crossref] [PubMed]

de Chaumont, F.

F. de Chaumont, S. Dallongeville, N. Chenouard, N. Hervé, S. Pop, T. Provoost, V. Meas-Yedid, P. Pankajakshan, T. Lecomte, Y. Le Montagner, T. Lagache, A. Dufour, and J. C. Olivo-Marin, “Icy: an open bioimage informatics platform for extended reproducible research,” Nat. Methods 9(7), 690–696 (2012), http://icy.bioimageanalysis.org .
[Crossref] [PubMed]

Deininger, K.

H. U. Dodt, U. Leischner, A. Schierloh, N. Jährling, C. P. Mauch, K. Deininger, J. M. Deussing, M. Eder, W. Zieglgänsberger, and K. Becker, “Ultramicroscopy: three-dimensional visualization of neuronal networks in the whole mouse brain,” Nat. Methods 4(4), 331–336 (2007).
[Crossref] [PubMed]

Del Bene, F.

J. Huisken, J. Swoger, F. Del Bene, J. Wittbrodt, and E. H. K. Stelzer, “Optical sectioning deep inside live embryos by selective plane illumination microscopy,” Science 305(5686), 1007–1009 (2004).
[Crossref] [PubMed]

Deng, Q.

S. K. Yoo, T. W. Starnes, Q. Deng, and A. Huttenlocher, “Lyn is a redox sensor that mediates leukocyte wound attraction in vivo,” Nature 480(7375), 109–112 (2011).
[Crossref] [PubMed]

Denk, W.

W. Denk, J. H. Strickler, and W. W. Webb, “2-Photon Laser Scanning Fluorescence Microscopy,” Science 248(4951), 73–76 (1990).
[Crossref]

Deussing, J. M.

H. U. Dodt, U. Leischner, A. Schierloh, N. Jährling, C. P. Mauch, K. Deininger, J. M. Deussing, M. Eder, W. Zieglgänsberger, and K. Becker, “Ultramicroscopy: three-dimensional visualization of neuronal networks in the whole mouse brain,” Nat. Methods 4(4), 331–336 (2007).
[Crossref] [PubMed]

Dodt, H. U.

H. U. Dodt, U. Leischner, A. Schierloh, N. Jährling, C. P. Mauch, K. Deininger, J. M. Deussing, M. Eder, W. Zieglgänsberger, and K. Becker, “Ultramicroscopy: three-dimensional visualization of neuronal networks in the whole mouse brain,” Nat. Methods 4(4), 331–336 (2007).
[Crossref] [PubMed]

Dufour, A.

F. de Chaumont, S. Dallongeville, N. Chenouard, N. Hervé, S. Pop, T. Provoost, V. Meas-Yedid, P. Pankajakshan, T. Lecomte, Y. Le Montagner, T. Lagache, A. Dufour, and J. C. Olivo-Marin, “Icy: an open bioimage informatics platform for extended reproducible research,” Nat. Methods 9(7), 690–696 (2012), http://icy.bioimageanalysis.org .
[Crossref] [PubMed]

Dunsby, C.

R. Patalay, C. Talbot, Y. Alexandrov, M. O. Lenz, S. Kumar, S. Warren, I. Munro, M. A. A. Neil, K. König, P. M. W. French, A. Chu, G. W. H. Stamp, and C. Dunsby, “Multiphoton multispectral fluorescence lifetime tomography for the evaluation of basal cell carcinomas,” PLoS ONE 7(9), e43460 (2012).
[Crossref] [PubMed]

Eder, M.

H. U. Dodt, U. Leischner, A. Schierloh, N. Jährling, C. P. Mauch, K. Deininger, J. M. Deussing, M. Eder, W. Zieglgänsberger, and K. Becker, “Ultramicroscopy: three-dimensional visualization of neuronal networks in the whole mouse brain,” Nat. Methods 4(4), 331–336 (2007).
[Crossref] [PubMed]

Eisenberg, H.

Y. Barad, H. Eisenberg, M. Horowitz, and Y. Silberberg, “Nonlinear scanning laser microscopy by third harmonic generation,” Appl. Phys. Lett. 70(8), 922–924 (1997).
[Crossref]

Fauver, M.

Frankel, P.

French, P. M. W.

Galko, M. J.

B. Stramer, W. Wood, M. J. Galko, M. J. Redd, A. Jacinto, S. M. Parkhurst, and P. Martin, “Live imaging of wound inflammation in Drosophila embryos reveals key roles for small GTPases during in vivo cell migration,” J. Cell Biol. 168(4), 567–573 (2005).
[Crossref] [PubMed]

Grabher, C.

P. Niethammer, C. Grabher, A. T. Look, and T. J. Mitchison, “A tissue-scale gradient of hydrogen peroxide mediates rapid wound detection in zebrafish,” Nature 459(7249), 996–999 (2009).
[Crossref] [PubMed]

Hecksher-Sørensen, J.

J. Sharpe, U. Ahlgren, P. Perry, B. Hill, A. Ross, J. Hecksher-Sørensen, R. Baldock, and D. Davidson, “Optical projection tomography as a tool for 3D microscopy and gene expression studies,” Science 296(5567), 541–545 (2002).
[Crossref] [PubMed]

Hervé, N.

F. de Chaumont, S. Dallongeville, N. Chenouard, N. Hervé, S. Pop, T. Provoost, V. Meas-Yedid, P. Pankajakshan, T. Lecomte, Y. Le Montagner, T. Lagache, A. Dufour, and J. C. Olivo-Marin, “Icy: an open bioimage informatics platform for extended reproducible research,” Nat. Methods 9(7), 690–696 (2012), http://icy.bioimageanalysis.org .
[Crossref] [PubMed]

Hill, B.

J. Sharpe, U. Ahlgren, P. Perry, B. Hill, A. Ross, J. Hecksher-Sørensen, R. Baldock, and D. Davidson, “Optical projection tomography as a tool for 3D microscopy and gene expression studies,” Science 296(5567), 541–545 (2002).
[Crossref] [PubMed]

Horowitz, M.

Y. Barad, H. Eisenberg, M. Horowitz, and Y. Silberberg, “Nonlinear scanning laser microscopy by third harmonic generation,” Appl. Phys. Lett. 70(8), 922–924 (1997).
[Crossref]

Huisken, J.

J. Huisken, J. Swoger, F. Del Bene, J. Wittbrodt, and E. H. K. Stelzer, “Optical sectioning deep inside live embryos by selective plane illumination microscopy,” Science 305(5686), 1007–1009 (2004).
[Crossref] [PubMed]

Huttenlocher, A.

S. K. Yoo, T. W. Starnes, Q. Deng, and A. Huttenlocher, “Lyn is a redox sensor that mediates leukocyte wound attraction in vivo,” Nature 480(7375), 109–112 (2011).
[Crossref] [PubMed]

J. R. Mathias, B. J. Perrin, T. X. Liu, J. Kanki, A. T. Look, and A. Huttenlocher, “Resolution of inflammation by retrograde chemotaxis of neutrophils in transgenic zebrafish,” J. Leukoc. Biol. 80(6), 1281–1288 (2006).
[Crossref] [PubMed]

Jacinto, A.

B. Stramer, W. Wood, M. J. Galko, M. J. Redd, A. Jacinto, S. M. Parkhurst, and P. Martin, “Live imaging of wound inflammation in Drosophila embryos reveals key roles for small GTPases during in vivo cell migration,” J. Cell Biol. 168(4), 567–573 (2005).
[Crossref] [PubMed]

Jährling, N.

H. U. Dodt, U. Leischner, A. Schierloh, N. Jährling, C. P. Mauch, K. Deininger, J. M. Deussing, M. Eder, W. Zieglgänsberger, and K. Becker, “Ultramicroscopy: three-dimensional visualization of neuronal networks in the whole mouse brain,” Nat. Methods 4(4), 331–336 (2007).
[Crossref] [PubMed]

Jessop, R. A.

A. F. Santos, A. B. Zaltsman, R. C. Martin, A. Kuzmin, Y. Alexandrov, E. P. Roquemore, R. A. Jessop, M. G. van Erck, and J. H. Verheijen, “Angiogenesis: an improved in vitro biological system and automated image-based workflow to aid identification and characterization of angiogenesis and angiogenic modulators,” Assay Drug Dev. Technol. 6(5), 693–710 (2008).
[Crossref] [PubMed]

Kanki, J.

J. R. Mathias, B. J. Perrin, T. X. Liu, J. Kanki, A. T. Look, and A. Huttenlocher, “Resolution of inflammation by retrograde chemotaxis of neutrophils in transgenic zebrafish,” J. Leukoc. Biol. 80(6), 1281–1288 (2006).
[Crossref] [PubMed]

Kelly, D.

König, K.

R. Patalay, C. Talbot, Y. Alexandrov, M. O. Lenz, S. Kumar, S. Warren, I. Munro, M. A. A. Neil, K. König, P. M. W. French, A. Chu, G. W. H. Stamp, and C. Dunsby, “Multiphoton multispectral fluorescence lifetime tomography for the evaluation of basal cell carcinomas,” PLoS ONE 7(9), e43460 (2012).
[Crossref] [PubMed]

Kumar, S.

Kuzmin, A.

A. F. Santos, A. B. Zaltsman, R. C. Martin, A. Kuzmin, Y. Alexandrov, E. P. Roquemore, R. A. Jessop, M. G. van Erck, and J. H. Verheijen, “Angiogenesis: an improved in vitro biological system and automated image-based workflow to aid identification and characterization of angiogenesis and angiogenic modulators,” Assay Drug Dev. Technol. 6(5), 693–710 (2008).
[Crossref] [PubMed]

Lagache, T.

F. de Chaumont, S. Dallongeville, N. Chenouard, N. Hervé, S. Pop, T. Provoost, V. Meas-Yedid, P. Pankajakshan, T. Lecomte, Y. Le Montagner, T. Lagache, A. Dufour, and J. C. Olivo-Marin, “Icy: an open bioimage informatics platform for extended reproducible research,” Nat. Methods 9(7), 690–696 (2012), http://icy.bioimageanalysis.org .
[Crossref] [PubMed]

Le Montagner, Y.

F. de Chaumont, S. Dallongeville, N. Chenouard, N. Hervé, S. Pop, T. Provoost, V. Meas-Yedid, P. Pankajakshan, T. Lecomte, Y. Le Montagner, T. Lagache, A. Dufour, and J. C. Olivo-Marin, “Icy: an open bioimage informatics platform for extended reproducible research,” Nat. Methods 9(7), 690–696 (2012), http://icy.bioimageanalysis.org .
[Crossref] [PubMed]

Lecomte, T.

F. de Chaumont, S. Dallongeville, N. Chenouard, N. Hervé, S. Pop, T. Provoost, V. Meas-Yedid, P. Pankajakshan, T. Lecomte, Y. Le Montagner, T. Lagache, A. Dufour, and J. C. Olivo-Marin, “Icy: an open bioimage informatics platform for extended reproducible research,” Nat. Methods 9(7), 690–696 (2012), http://icy.bioimageanalysis.org .
[Crossref] [PubMed]

Leischner, U.

H. U. Dodt, U. Leischner, A. Schierloh, N. Jährling, C. P. Mauch, K. Deininger, J. M. Deussing, M. Eder, W. Zieglgänsberger, and K. Becker, “Ultramicroscopy: three-dimensional visualization of neuronal networks in the whole mouse brain,” Nat. Methods 4(4), 331–336 (2007).
[Crossref] [PubMed]

Lenz, M. O.

R. Patalay, C. Talbot, Y. Alexandrov, M. O. Lenz, S. Kumar, S. Warren, I. Munro, M. A. A. Neil, K. König, P. M. W. French, A. Chu, G. W. H. Stamp, and C. Dunsby, “Multiphoton multispectral fluorescence lifetime tomography for the evaluation of basal cell carcinomas,” PLoS ONE 7(9), e43460 (2012).
[Crossref] [PubMed]

Lichtman, J. W.

J. A. Conchello and J. W. Lichtman, “Optical sectioning microscopy,” Nat. Methods 2(12), 920–931 (2005).
[Crossref] [PubMed]

Liu, T. X.

J. R. Mathias, B. J. Perrin, T. X. Liu, J. Kanki, A. T. Look, and A. Huttenlocher, “Resolution of inflammation by retrograde chemotaxis of neutrophils in transgenic zebrafish,” J. Leukoc. Biol. 80(6), 1281–1288 (2006).
[Crossref] [PubMed]

Look, A. T.

P. Niethammer, C. Grabher, A. T. Look, and T. J. Mitchison, “A tissue-scale gradient of hydrogen peroxide mediates rapid wound detection in zebrafish,” Nature 459(7249), 996–999 (2009).
[Crossref] [PubMed]

J. R. Mathias, B. J. Perrin, T. X. Liu, J. Kanki, A. T. Look, and A. Huttenlocher, “Resolution of inflammation by retrograde chemotaxis of neutrophils in transgenic zebrafish,” J. Leukoc. Biol. 80(6), 1281–1288 (2006).
[Crossref] [PubMed]

Martin, P.

B. Stramer, W. Wood, M. J. Galko, M. J. Redd, A. Jacinto, S. M. Parkhurst, and P. Martin, “Live imaging of wound inflammation in Drosophila embryos reveals key roles for small GTPases during in vivo cell migration,” J. Cell Biol. 168(4), 567–573 (2005).
[Crossref] [PubMed]

Martin, R. C.

A. F. Santos, A. B. Zaltsman, R. C. Martin, A. Kuzmin, Y. Alexandrov, E. P. Roquemore, R. A. Jessop, M. G. van Erck, and J. H. Verheijen, “Angiogenesis: an improved in vitro biological system and automated image-based workflow to aid identification and characterization of angiogenesis and angiogenic modulators,” Assay Drug Dev. Technol. 6(5), 693–710 (2008).
[Crossref] [PubMed]

Mathias, J. R.

J. R. Mathias, B. J. Perrin, T. X. Liu, J. Kanki, A. T. Look, and A. Huttenlocher, “Resolution of inflammation by retrograde chemotaxis of neutrophils in transgenic zebrafish,” J. Leukoc. Biol. 80(6), 1281–1288 (2006).
[Crossref] [PubMed]

Mauch, C. P.

H. U. Dodt, U. Leischner, A. Schierloh, N. Jährling, C. P. Mauch, K. Deininger, J. M. Deussing, M. Eder, W. Zieglgänsberger, and K. Becker, “Ultramicroscopy: three-dimensional visualization of neuronal networks in the whole mouse brain,” Nat. Methods 4(4), 331–336 (2007).
[Crossref] [PubMed]

McGinty, J.

Meas-Yedid, V.

F. de Chaumont, S. Dallongeville, N. Chenouard, N. Hervé, S. Pop, T. Provoost, V. Meas-Yedid, P. Pankajakshan, T. Lecomte, Y. Le Montagner, T. Lagache, A. Dufour, and J. C. Olivo-Marin, “Icy: an open bioimage informatics platform for extended reproducible research,” Nat. Methods 9(7), 690–696 (2012), http://icy.bioimageanalysis.org .
[Crossref] [PubMed]

Meyer, M. G.

Mitchison, T. J.

P. Niethammer, C. Grabher, A. T. Look, and T. J. Mitchison, “A tissue-scale gradient of hydrogen peroxide mediates rapid wound detection in zebrafish,” Nature 459(7249), 996–999 (2009).
[Crossref] [PubMed]

Munro, I.

R. Patalay, C. Talbot, Y. Alexandrov, M. O. Lenz, S. Kumar, S. Warren, I. Munro, M. A. A. Neil, K. König, P. M. W. French, A. Chu, G. W. H. Stamp, and C. Dunsby, “Multiphoton multispectral fluorescence lifetime tomography for the evaluation of basal cell carcinomas,” PLoS ONE 7(9), e43460 (2012).
[Crossref] [PubMed]

Neil, M. A. A.

R. Patalay, C. Talbot, Y. Alexandrov, M. O. Lenz, S. Kumar, S. Warren, I. Munro, M. A. A. Neil, K. König, P. M. W. French, A. Chu, G. W. H. Stamp, and C. Dunsby, “Multiphoton multispectral fluorescence lifetime tomography for the evaluation of basal cell carcinomas,” PLoS ONE 7(9), e43460 (2012).
[Crossref] [PubMed]

Nelson, A. C.

Neumann, T.

Niethammer, P.

P. Niethammer, C. Grabher, A. T. Look, and T. J. Mitchison, “A tissue-scale gradient of hydrogen peroxide mediates rapid wound detection in zebrafish,” Nature 459(7249), 996–999 (2009).
[Crossref] [PubMed]

Olivo-Marin, J. C.

F. de Chaumont, S. Dallongeville, N. Chenouard, N. Hervé, S. Pop, T. Provoost, V. Meas-Yedid, P. Pankajakshan, T. Lecomte, Y. Le Montagner, T. Lagache, A. Dufour, and J. C. Olivo-Marin, “Icy: an open bioimage informatics platform for extended reproducible research,” Nat. Methods 9(7), 690–696 (2012), http://icy.bioimageanalysis.org .
[Crossref] [PubMed]

Pankajakshan, P.

F. de Chaumont, S. Dallongeville, N. Chenouard, N. Hervé, S. Pop, T. Provoost, V. Meas-Yedid, P. Pankajakshan, T. Lecomte, Y. Le Montagner, T. Lagache, A. Dufour, and J. C. Olivo-Marin, “Icy: an open bioimage informatics platform for extended reproducible research,” Nat. Methods 9(7), 690–696 (2012), http://icy.bioimageanalysis.org .
[Crossref] [PubMed]

Parkhurst, S. M.

B. Stramer, W. Wood, M. J. Galko, M. J. Redd, A. Jacinto, S. M. Parkhurst, and P. Martin, “Live imaging of wound inflammation in Drosophila embryos reveals key roles for small GTPases during in vivo cell migration,” J. Cell Biol. 168(4), 567–573 (2005).
[Crossref] [PubMed]

Patalay, R.

R. Patalay, C. Talbot, Y. Alexandrov, M. O. Lenz, S. Kumar, S. Warren, I. Munro, M. A. A. Neil, K. König, P. M. W. French, A. Chu, G. W. H. Stamp, and C. Dunsby, “Multiphoton multispectral fluorescence lifetime tomography for the evaluation of basal cell carcinomas,” PLoS ONE 7(9), e43460 (2012).
[Crossref] [PubMed]

Patten, F.

Perrin, B. J.

J. R. Mathias, B. J. Perrin, T. X. Liu, J. Kanki, A. T. Look, and A. Huttenlocher, “Resolution of inflammation by retrograde chemotaxis of neutrophils in transgenic zebrafish,” J. Leukoc. Biol. 80(6), 1281–1288 (2006).
[Crossref] [PubMed]

Perry, P.

J. Sharpe, U. Ahlgren, P. Perry, B. Hill, A. Ross, J. Hecksher-Sørensen, R. Baldock, and D. Davidson, “Optical projection tomography as a tool for 3D microscopy and gene expression studies,” Science 296(5567), 541–545 (2002).
[Crossref] [PubMed]

Pop, S.

F. de Chaumont, S. Dallongeville, N. Chenouard, N. Hervé, S. Pop, T. Provoost, V. Meas-Yedid, P. Pankajakshan, T. Lecomte, Y. Le Montagner, T. Lagache, A. Dufour, and J. C. Olivo-Marin, “Icy: an open bioimage informatics platform for extended reproducible research,” Nat. Methods 9(7), 690–696 (2012), http://icy.bioimageanalysis.org .
[Crossref] [PubMed]

Provoost, T.

F. de Chaumont, S. Dallongeville, N. Chenouard, N. Hervé, S. Pop, T. Provoost, V. Meas-Yedid, P. Pankajakshan, T. Lecomte, Y. Le Montagner, T. Lagache, A. Dufour, and J. C. Olivo-Marin, “Icy: an open bioimage informatics platform for extended reproducible research,” Nat. Methods 9(7), 690–696 (2012), http://icy.bioimageanalysis.org .
[Crossref] [PubMed]

Rahn, J. R.

Redd, M. J.

B. Stramer, W. Wood, M. J. Galko, M. J. Redd, A. Jacinto, S. M. Parkhurst, and P. Martin, “Live imaging of wound inflammation in Drosophila embryos reveals key roles for small GTPases during in vivo cell migration,” J. Cell Biol. 168(4), 567–573 (2005).
[Crossref] [PubMed]

Roquemore, E. P.

A. F. Santos, A. B. Zaltsman, R. C. Martin, A. Kuzmin, Y. Alexandrov, E. P. Roquemore, R. A. Jessop, M. G. van Erck, and J. H. Verheijen, “Angiogenesis: an improved in vitro biological system and automated image-based workflow to aid identification and characterization of angiogenesis and angiogenic modulators,” Assay Drug Dev. Technol. 6(5), 693–710 (2008).
[Crossref] [PubMed]

Ross, A.

J. Sharpe, U. Ahlgren, P. Perry, B. Hill, A. Ross, J. Hecksher-Sørensen, R. Baldock, and D. Davidson, “Optical projection tomography as a tool for 3D microscopy and gene expression studies,” Science 296(5567), 541–545 (2002).
[Crossref] [PubMed]

Santos, A. F.

A. F. Santos, A. B. Zaltsman, R. C. Martin, A. Kuzmin, Y. Alexandrov, E. P. Roquemore, R. A. Jessop, M. G. van Erck, and J. H. Verheijen, “Angiogenesis: an improved in vitro biological system and automated image-based workflow to aid identification and characterization of angiogenesis and angiogenic modulators,” Assay Drug Dev. Technol. 6(5), 693–710 (2008).
[Crossref] [PubMed]

Schierloh, A.

H. U. Dodt, U. Leischner, A. Schierloh, N. Jährling, C. P. Mauch, K. Deininger, J. M. Deussing, M. Eder, W. Zieglgänsberger, and K. Becker, “Ultramicroscopy: three-dimensional visualization of neuronal networks in the whole mouse brain,” Nat. Methods 4(4), 331–336 (2007).
[Crossref] [PubMed]

Seibel, E. J.

Sharpe, J.

J. Sharpe, U. Ahlgren, P. Perry, B. Hill, A. Ross, J. Hecksher-Sørensen, R. Baldock, and D. Davidson, “Optical projection tomography as a tool for 3D microscopy and gene expression studies,” Science 296(5567), 541–545 (2002).
[Crossref] [PubMed]

Silberberg, Y.

Y. Barad, H. Eisenberg, M. Horowitz, and Y. Silberberg, “Nonlinear scanning laser microscopy by third harmonic generation,” Appl. Phys. Lett. 70(8), 922–924 (1997).
[Crossref]

Stamp, G. W. H.

R. Patalay, C. Talbot, Y. Alexandrov, M. O. Lenz, S. Kumar, S. Warren, I. Munro, M. A. A. Neil, K. König, P. M. W. French, A. Chu, G. W. H. Stamp, and C. Dunsby, “Multiphoton multispectral fluorescence lifetime tomography for the evaluation of basal cell carcinomas,” PLoS ONE 7(9), e43460 (2012).
[Crossref] [PubMed]

Starnes, T. W.

S. K. Yoo, T. W. Starnes, Q. Deng, and A. Huttenlocher, “Lyn is a redox sensor that mediates leukocyte wound attraction in vivo,” Nature 480(7375), 109–112 (2011).
[Crossref] [PubMed]

Stelzer, E. H. K.

J. Huisken, J. Swoger, F. Del Bene, J. Wittbrodt, and E. H. K. Stelzer, “Optical sectioning deep inside live embryos by selective plane illumination microscopy,” Science 305(5686), 1007–1009 (2004).
[Crossref] [PubMed]

Stramer, B.

B. Stramer, W. Wood, M. J. Galko, M. J. Redd, A. Jacinto, S. M. Parkhurst, and P. Martin, “Live imaging of wound inflammation in Drosophila embryos reveals key roles for small GTPases during in vivo cell migration,” J. Cell Biol. 168(4), 567–573 (2005).
[Crossref] [PubMed]

Strickler, J. H.

W. Denk, J. H. Strickler, and W. W. Webb, “2-Photon Laser Scanning Fluorescence Microscopy,” Science 248(4951), 73–76 (1990).
[Crossref]

Swoger, J.

J. Huisken, J. Swoger, F. Del Bene, J. Wittbrodt, and E. H. K. Stelzer, “Optical sectioning deep inside live embryos by selective plane illumination microscopy,” Science 305(5686), 1007–1009 (2004).
[Crossref] [PubMed]

Talbot, C.

R. Patalay, C. Talbot, Y. Alexandrov, M. O. Lenz, S. Kumar, S. Warren, I. Munro, M. A. A. Neil, K. König, P. M. W. French, A. Chu, G. W. H. Stamp, and C. Dunsby, “Multiphoton multispectral fluorescence lifetime tomography for the evaluation of basal cell carcinomas,” PLoS ONE 7(9), e43460 (2012).
[Crossref] [PubMed]

van Erck, M. G.

A. F. Santos, A. B. Zaltsman, R. C. Martin, A. Kuzmin, Y. Alexandrov, E. P. Roquemore, R. A. Jessop, M. G. van Erck, and J. H. Verheijen, “Angiogenesis: an improved in vitro biological system and automated image-based workflow to aid identification and characterization of angiogenesis and angiogenic modulators,” Assay Drug Dev. Technol. 6(5), 693–710 (2008).
[Crossref] [PubMed]

Verheijen, J. H.

A. F. Santos, A. B. Zaltsman, R. C. Martin, A. Kuzmin, Y. Alexandrov, E. P. Roquemore, R. A. Jessop, M. G. van Erck, and J. H. Verheijen, “Angiogenesis: an improved in vitro biological system and automated image-based workflow to aid identification and characterization of angiogenesis and angiogenic modulators,” Assay Drug Dev. Technol. 6(5), 693–710 (2008).
[Crossref] [PubMed]

Warren, S.

R. Patalay, C. Talbot, Y. Alexandrov, M. O. Lenz, S. Kumar, S. Warren, I. Munro, M. A. A. Neil, K. König, P. M. W. French, A. Chu, G. W. H. Stamp, and C. Dunsby, “Multiphoton multispectral fluorescence lifetime tomography for the evaluation of basal cell carcinomas,” PLoS ONE 7(9), e43460 (2012).
[Crossref] [PubMed]

Webb, W. W.

W. Denk, J. H. Strickler, and W. W. Webb, “2-Photon Laser Scanning Fluorescence Microscopy,” Science 248(4951), 73–76 (1990).
[Crossref]

Wittbrodt, J.

J. Huisken, J. Swoger, F. Del Bene, J. Wittbrodt, and E. H. K. Stelzer, “Optical sectioning deep inside live embryos by selective plane illumination microscopy,” Science 305(5686), 1007–1009 (2004).
[Crossref] [PubMed]

Wood, W.

B. Stramer, W. Wood, M. J. Galko, M. J. Redd, A. Jacinto, S. M. Parkhurst, and P. Martin, “Live imaging of wound inflammation in Drosophila embryos reveals key roles for small GTPases during in vivo cell migration,” J. Cell Biol. 168(4), 567–573 (2005).
[Crossref] [PubMed]

Yoo, S. K.

S. K. Yoo, T. W. Starnes, Q. Deng, and A. Huttenlocher, “Lyn is a redox sensor that mediates leukocyte wound attraction in vivo,” Nature 480(7375), 109–112 (2011).
[Crossref] [PubMed]

Zaltsman, A. B.

A. F. Santos, A. B. Zaltsman, R. C. Martin, A. Kuzmin, Y. Alexandrov, E. P. Roquemore, R. A. Jessop, M. G. van Erck, and J. H. Verheijen, “Angiogenesis: an improved in vitro biological system and automated image-based workflow to aid identification and characterization of angiogenesis and angiogenic modulators,” Assay Drug Dev. Technol. 6(5), 693–710 (2008).
[Crossref] [PubMed]

Zieglgänsberger, W.

H. U. Dodt, U. Leischner, A. Schierloh, N. Jährling, C. P. Mauch, K. Deininger, J. M. Deussing, M. Eder, W. Zieglgänsberger, and K. Becker, “Ultramicroscopy: three-dimensional visualization of neuronal networks in the whole mouse brain,” Nat. Methods 4(4), 331–336 (2007).
[Crossref] [PubMed]

Appl. Phys. Lett. (1)

Y. Barad, H. Eisenberg, M. Horowitz, and Y. Silberberg, “Nonlinear scanning laser microscopy by third harmonic generation,” Appl. Phys. Lett. 70(8), 922–924 (1997).
[Crossref]

Assay Drug Dev. Technol. (1)

A. F. Santos, A. B. Zaltsman, R. C. Martin, A. Kuzmin, Y. Alexandrov, E. P. Roquemore, R. A. Jessop, M. G. van Erck, and J. H. Verheijen, “Angiogenesis: an improved in vitro biological system and automated image-based workflow to aid identification and characterization of angiogenesis and angiogenic modulators,” Assay Drug Dev. Technol. 6(5), 693–710 (2008).
[Crossref] [PubMed]

Biomed. Opt. Express (1)

J. Cell Biol. (1)

B. Stramer, W. Wood, M. J. Galko, M. J. Redd, A. Jacinto, S. M. Parkhurst, and P. Martin, “Live imaging of wound inflammation in Drosophila embryos reveals key roles for small GTPases during in vivo cell migration,” J. Cell Biol. 168(4), 567–573 (2005).
[Crossref] [PubMed]

J. Leukoc. Biol. (1)

J. R. Mathias, B. J. Perrin, T. X. Liu, J. Kanki, A. T. Look, and A. Huttenlocher, “Resolution of inflammation by retrograde chemotaxis of neutrophils in transgenic zebrafish,” J. Leukoc. Biol. 80(6), 1281–1288 (2006).
[Crossref] [PubMed]

Nat. Methods (3)

J. A. Conchello and J. W. Lichtman, “Optical sectioning microscopy,” Nat. Methods 2(12), 920–931 (2005).
[Crossref] [PubMed]

F. de Chaumont, S. Dallongeville, N. Chenouard, N. Hervé, S. Pop, T. Provoost, V. Meas-Yedid, P. Pankajakshan, T. Lecomte, Y. Le Montagner, T. Lagache, A. Dufour, and J. C. Olivo-Marin, “Icy: an open bioimage informatics platform for extended reproducible research,” Nat. Methods 9(7), 690–696 (2012), http://icy.bioimageanalysis.org .
[Crossref] [PubMed]

H. U. Dodt, U. Leischner, A. Schierloh, N. Jährling, C. P. Mauch, K. Deininger, J. M. Deussing, M. Eder, W. Zieglgänsberger, and K. Becker, “Ultramicroscopy: three-dimensional visualization of neuronal networks in the whole mouse brain,” Nat. Methods 4(4), 331–336 (2007).
[Crossref] [PubMed]

Nature (2)

S. K. Yoo, T. W. Starnes, Q. Deng, and A. Huttenlocher, “Lyn is a redox sensor that mediates leukocyte wound attraction in vivo,” Nature 480(7375), 109–112 (2011).
[Crossref] [PubMed]

P. Niethammer, C. Grabher, A. T. Look, and T. J. Mitchison, “A tissue-scale gradient of hydrogen peroxide mediates rapid wound detection in zebrafish,” Nature 459(7249), 996–999 (2009).
[Crossref] [PubMed]

Opt. Express (1)

Opt. Lett. (1)

PLoS ONE (1)

R. Patalay, C. Talbot, Y. Alexandrov, M. O. Lenz, S. Kumar, S. Warren, I. Munro, M. A. A. Neil, K. König, P. M. W. French, A. Chu, G. W. H. Stamp, and C. Dunsby, “Multiphoton multispectral fluorescence lifetime tomography for the evaluation of basal cell carcinomas,” PLoS ONE 7(9), e43460 (2012).
[Crossref] [PubMed]

Science (3)

W. Denk, J. H. Strickler, and W. W. Webb, “2-Photon Laser Scanning Fluorescence Microscopy,” Science 248(4951), 73–76 (1990).
[Crossref]

J. Sharpe, U. Ahlgren, P. Perry, B. Hill, A. Ross, J. Hecksher-Sørensen, R. Baldock, and D. Davidson, “Optical projection tomography as a tool for 3D microscopy and gene expression studies,” Science 296(5567), 541–545 (2002).
[Crossref] [PubMed]

J. Huisken, J. Swoger, F. Del Bene, J. Wittbrodt, and E. H. K. Stelzer, “Optical sectioning deep inside live embryos by selective plane illumination microscopy,” Science 305(5686), 1007–1009 (2004).
[Crossref] [PubMed]

Other (1)

A. C. Kak and M. Slaney, Principles of Computerized Tomographic Imaging, R. E. O’Malley ed. (SIAM,IEEE Press, New York, 1988).

Supplementary Material (3)

» Media 1: MP4 (415 KB)     
» Media 2: MP4 (4397 KB)     
» Media 3: MP4 (3980 KB)     

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Figures (5)

Fig. 1
Fig. 1 Schematic of dual axis OPT set-up (inset shows the focusing of the orthogonal imaging systems to planes intersecting at the axis of rotation). EF – emission filter, AP – aperture, L1 and L2 – tube lens, FP – focal plane, ϕ – sample diameter, DOF – depth of field.
Fig. 2
Fig. 2 (a,b) Simultaneously acquired orthogonal pair of fluorescence images of a 2 dpf LysC: GFP zebrafish to which the size-selective cell segmentation has been applied and (c) the corresponding transmitted light image for (b) showing cell localization within the zebrafish (only the tail is shown here). Scale bar 200 μm. The white interrupt on the scale bar indicates the cell localization accuracy (2 pixels). Inserts show magnified view.
Fig. 3
Fig. 3 (a) 3-D plot (Media 1) showing the neutrophil migration tracks over ~25.5 minutes with (b) corresponding migration mapping within the zebrafish (color used to differentiate tracks). Scale bar 200 μm. Scale and orientation of (a) and (b) are approximately equal.
Fig. 4
Fig. 4 Individual cell migration paths along the Z axis (approximately aligned with the zebrafish tail) during the ~25.5 minutes time-lapse. Negative displacements indicate travel towards the tip of the tail. The red vertical scale bar indicates the resolution of the cell localization algorithm.
Fig. 5
Fig. 5 3-D cell tracks color-coded by (a) average speed (Media 2) and (b) the average directionality (Media 3).

Equations (1)

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[ X k + 1 X A o R Y k + 1 Y A o R ] k = [ cos θ sin θ sin θ cos θ ] . [ X k X A o R Y k Y A o R ] k a n d ( Z k + 1 ) k = ( Z k ) k

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