Abstract

We present a new approach for three-dimensional (3D) live single-cell imaging with isotropic sub-micron spatial resolution using fluorescence computed tomography (fCT). A thin, highly inclined and laminated optical (HILO) sheet of light is used for fluorescence excitation in live single cells that are rotated around an axis perpendicular to the optical axis. During a full rotation, 400-500 two-dimensional (2D) projection images of the cell are acquired from multiple viewing perspectives by rapidly scanning the HILO light sheet along the optical axis. We report technical characteristics of the HILO approach and the results of a quantitative comparison with conventional epi fCT, demonstrating that HILO fCT offers significantly (about 17 times) reduced photobleaching and a two-fold improvement in 3D imaging contrast. We discuss potential application areas of the method for cell structure studies in live single cells with isotropic 3D spatial resolution.

© 2018 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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2017 (2)

B. Cao, L. Kelbauskas, S. Chan, R. M. Shetty, D. Smith, and D. R. Meldrum, “Rotation of single live mammalian cells using dynamic holographic optical tweezers,” Opt. Lasers Eng. 92, 70–75 (2017).
[Crossref]

L. Kelbauskas, R. Shetty, B. Cao, K. C. Wang, D. Smith, H. Wang, S. H. Chao, S. Gangaraju, B. Ashcroft, M. Kritzer, H. Glenn, R. H. Johnson, and D. R. Meldrum, “Optical computed tomography for spatially isotropic four-dimensional imaging of live single cells,” Sci. Adv. 3(12), e1602580 (2017).
[Crossref] [PubMed]

2016 (2)

R. M. Shetty, J. R. Myers, M. Sreenivasulu, W. Teller, J. Vela, J. Houkal, S.-H. Chao, R. H. Johnson, L. Kelbauskas, H. Wang, and D. R. Meldrum, “Characterization and comparison of three microfabrication methods to generate out-of-plane microvortices for single cell rotation and 3d imaging,” J. Micromech. Microeng. 27(1), 015004 (2016).
[Crossref]

F. Huang, G. Sirinakis, E. S. Allgeyer, L. K. Schroeder, W. C. Duim, E. B. Kromann, T. Phan, F. E. Rivera-Molina, J. R. Myers, I. Irnov, M. Lessard, Y. Zhang, M. A. Handel, C. Jacobs-Wagner, C. P. Lusk, J. E. Rothman, D. Toomre, M. J. Booth, and J. Bewersdorf, “Ultra-high resolution 3d imaging of whole cells,” Cell 166(4), 1028–1040 (2016).
[Crossref] [PubMed]

2015 (1)

2014 (2)

J. Mayer, A. Robert-Moreno, R. Danuser, J. V. Stein, J. Sharpe, and J. Swoger, “OPTiSPIM: integrating optical projection tomography in light sheet microscopy extends specimen characterization to nonfluorescent contrasts,” Opt. Lett. 39(4), 1053–1056 (2014).
[Crossref] [PubMed]

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. Böhme, 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(6208), 1257998 (2014).
[Crossref] [PubMed]

2013 (2)

Y. Wu, P. Wawrzusin, J. Senseney, R. S. Fischer, R. Christensen, A. Santella, A. G. York, P. W. Winter, C. M. Waterman, Z. Bao, D. A. Colón-Ramos, M. McAuliffe, and H. Shroff, “Spatially isotropic four-dimensional imaging with dual-view plane illumination microscopy,” Nat. Biotechnol. 31(11), 1032–1038 (2013).
[Crossref] [PubMed]

C. Nombela-Arrieta, G. Pivarnik, B. Winkel, K. J. Canty, B. Harley, J. E. Mahoney, S.-Y. Park, J. Lu, A. Protopopov, and L. E. Silberstein, “Quantitative imaging of haematopoietic stem and progenitor cell localization and hypoxic status in the bone marrow microenvironment,” Nat. Cell Biol. 15(5), 533–543 (2013).
[Crossref] [PubMed]

2012 (1)

V. Nandakumar, L. Kelbauskas, K. F. Hernandez, K. M. Lintecum, P. Senechal, K. J. Bussey, P. C. Davies, R. H. Johnson, and D. R. Meldrum, “Isotropic 3D nuclear morphometry of normal, fibrocystic and malignant breast epithelial cells reveals new structural alterations,” PLoS One 7(1), e29230 (2012).
[Crossref] [PubMed]

2011 (2)

V. Nandakumar, L. Kelbauskas, R. Johnson, and D. Meldrum, “Quantitative characterization of preneoplastic progression using single-cell computed tomography and three-dimensional karyometry,” Cytometry A 79(1), 25–34 (2011).
[Crossref] [PubMed]

M. Rieckher, U. J. Birk, H. Meyer, J. Ripoll, and N. Tavernarakis, “Microscopic optical projection tomography in vivo,” PLoS One 6(4), e18963 (2011).
[Crossref] [PubMed]

2010 (1)

2009 (3)

C. Li, G. S. Mitchell, J. Dutta, S. Ahn, R. M. Leahy, and S. R. Cherry, “A three-dimensional multispectral fluorescence optical tomography imaging system for small animals based on a conical mirror design,” Opt. Express 17(9), 7571–7585 (2009).
[Crossref] [PubMed]

Q. Miao, J. R. Rahn, A. Tourovskaia, M. G. Meyer, T. Neumann, A. C. Nelson, and E. J. Seibel, “Dual-modal three-dimensional imaging of single cells with isometric high resolution using an optical projection tomography microscope,” J. Biomed. Opt. 14, 064035 (2009).

J.-F. Colas and J. Sharpe, “Live optical projection tomography,” Organogenesis 5(4), 211–216 (2009).
[Crossref] [PubMed]

2008 (4)

M. Tokunaga, N. Imamoto, and K. Sakata-Sogawa, “Highly inclined thin illumination enables clear single-molecule imaging in cells,” Nat. Methods 5(2), 159–161 (2008).
[Crossref] [PubMed]

P. J. Keller, A. D. Schmidt, J. Wittbrodt, and E. H. Stelzer, “Reconstruction of zebrafish early embryonic development by scanned light sheet microscopy,” Science 322(5904), 1065–1069 (2008).
[Crossref] [PubMed]

C. Dunsby, “Optically sectioned imaging by oblique plane microscopy,” Opt. Express 16(25), 20306–20316 (2008).
[Crossref] [PubMed]

J. McGinty, K. B. Tahir, R. Laine, C. B. Talbot, C. Dunsby, M. A. Neil, L. Quintana, J. Swoger, J. Sharpe, and P. M. French, “Fluorescence lifetime optical projection tomography,” J. Biophotonics 1(5), 390–394 (2008).
[Crossref] [PubMed]

2005 (1)

2003 (2)

P. Dubey, H. Su, N. Adonai, S. Du, A. Rosato, J. Braun, S. S. Gambhir, and O. N. Witte, “Quantitative imaging of the T cell antitumor response by positron-emission tomography,” Proc. Natl. Acad. Sci. U.S.A. 100(3), 1232–1237 (2003).
[Crossref] [PubMed]

D. J. Stephens and V. J. Allan, “Light microscopy techniques for live cell imaging,” Science 300(5616), 82–86 (2003).
[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]

1999 (2)

M. G. Gustafsson, D. A. Agard, and J. W. Sedat, “I5M: 3D widefield light microscopy with better than 100 nm axial resolution,” J. Microsc. 195(Pt 1), 10–16 (1999).
[Crossref] [PubMed]

S. Weiss, “Fluorescence spectroscopy of single biomolecules,” Science 283(5408), 1676–1683 (1999).
[Crossref] [PubMed]

1997 (2)

A. H. Iwane, T. Funatsu, Y. Harada, M. Tokunaga, O. Ohara, S. Morimoto, and T. Yanagida, “Single molecular assay of individual ATP turnover by a myosin-GFP fusion protein expressed in vitro,” FEBS Lett. 407(2), 235–238 (1997).
[Crossref] [PubMed]

D. W. Pierce, N. Hom-Booher, and R. D. Vale, “Imaging individual green fluorescent proteins,” Nature 388(6640), 338 (1997).
[Crossref] [PubMed]

1995 (1)

1986 (1)

G. Fuhr, R. Glaser, and R. Hagedorn, “Rotation of dielectrics in a rotating electric high-frequency field. Model experiments and theoretical explanation of the rotation effect of living cells,” Biophys. J. 49(2), 395–402 (1986).
[Crossref] [PubMed]

Adonai, N.

P. Dubey, H. Su, N. Adonai, S. Du, A. Rosato, J. Braun, S. S. Gambhir, and O. N. Witte, “Quantitative imaging of the T cell antitumor response by positron-emission tomography,” Proc. Natl. Acad. Sci. U.S.A. 100(3), 1232–1237 (2003).
[Crossref] [PubMed]

Agard, D. A.

M. G. Gustafsson, D. A. Agard, and J. W. Sedat, “I5M: 3D widefield light microscopy with better than 100 nm axial resolution,” J. Microsc. 195(Pt 1), 10–16 (1999).
[Crossref] [PubMed]

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]

Ahn, S.

Allan, V. J.

D. J. Stephens and V. J. Allan, “Light microscopy techniques for live cell imaging,” Science 300(5616), 82–86 (2003).
[Crossref] [PubMed]

Allgeyer, E. S.

F. Huang, G. Sirinakis, E. S. Allgeyer, L. K. Schroeder, W. C. Duim, E. B. Kromann, T. Phan, F. E. Rivera-Molina, J. R. Myers, I. Irnov, M. Lessard, Y. Zhang, M. A. Handel, C. Jacobs-Wagner, C. P. Lusk, J. E. Rothman, D. Toomre, M. J. Booth, and J. Bewersdorf, “Ultra-high resolution 3d imaging of whole cells,” Cell 166(4), 1028–1040 (2016).
[Crossref] [PubMed]

Andilla, J.

Artigas, D.

Ashcroft, B.

L. Kelbauskas, R. Shetty, B. Cao, K. C. Wang, D. Smith, H. Wang, S. H. Chao, S. Gangaraju, B. Ashcroft, M. Kritzer, H. Glenn, R. H. Johnson, and D. R. Meldrum, “Optical computed tomography for spatially isotropic four-dimensional imaging of live single cells,” Sci. Adv. 3(12), e1602580 (2017).
[Crossref] [PubMed]

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]

Bao, Z.

Y. Wu, P. Wawrzusin, J. Senseney, R. S. Fischer, R. Christensen, A. Santella, A. G. York, P. W. Winter, C. M. Waterman, Z. Bao, D. A. Colón-Ramos, M. McAuliffe, and H. Shroff, “Spatially isotropic four-dimensional imaging with dual-view plane illumination microscopy,” Nat. Biotechnol. 31(11), 1032–1038 (2013).
[Crossref] [PubMed]

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. Böhme, 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(6208), 1257998 (2014).
[Crossref] [PubMed]

Betzig, E.

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. Böhme, 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(6208), 1257998 (2014).
[Crossref] [PubMed]

Bewersdorf, J.

F. Huang, G. Sirinakis, E. S. Allgeyer, L. K. Schroeder, W. C. Duim, E. B. Kromann, T. Phan, F. E. Rivera-Molina, J. R. Myers, I. Irnov, M. Lessard, Y. Zhang, M. A. Handel, C. Jacobs-Wagner, C. P. Lusk, J. E. Rothman, D. Toomre, M. J. Booth, and J. Bewersdorf, “Ultra-high resolution 3d imaging of whole cells,” Cell 166(4), 1028–1040 (2016).
[Crossref] [PubMed]

Birk, U. J.

M. Rieckher, U. J. Birk, H. Meyer, J. Ripoll, and N. Tavernarakis, “Microscopic optical projection tomography in vivo,” PLoS One 6(4), e18963 (2011).
[Crossref] [PubMed]

Böhme, R.

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. Böhme, 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(6208), 1257998 (2014).
[Crossref] [PubMed]

Booth, M. J.

F. Huang, G. Sirinakis, E. S. Allgeyer, L. K. Schroeder, W. C. Duim, E. B. Kromann, T. Phan, F. E. Rivera-Molina, J. R. Myers, I. Irnov, M. Lessard, Y. Zhang, M. A. Handel, C. Jacobs-Wagner, C. P. Lusk, J. E. Rothman, D. Toomre, M. J. Booth, and J. Bewersdorf, “Ultra-high resolution 3d imaging of whole cells,” Cell 166(4), 1028–1040 (2016).
[Crossref] [PubMed]

Braun, J.

P. Dubey, H. Su, N. Adonai, S. Du, A. Rosato, J. Braun, S. S. Gambhir, and O. N. Witte, “Quantitative imaging of the T cell antitumor response by positron-emission tomography,” Proc. Natl. Acad. Sci. U.S.A. 100(3), 1232–1237 (2003).
[Crossref] [PubMed]

Bussey, K. J.

V. Nandakumar, L. Kelbauskas, K. F. Hernandez, K. M. Lintecum, P. Senechal, K. J. Bussey, P. C. Davies, R. H. Johnson, and D. R. Meldrum, “Isotropic 3D nuclear morphometry of normal, fibrocystic and malignant breast epithelial cells reveals new structural alterations,” PLoS One 7(1), e29230 (2012).
[Crossref] [PubMed]

Canty, K. J.

C. Nombela-Arrieta, G. Pivarnik, B. Winkel, K. J. Canty, B. Harley, J. E. Mahoney, S.-Y. Park, J. Lu, A. Protopopov, and L. E. Silberstein, “Quantitative imaging of haematopoietic stem and progenitor cell localization and hypoxic status in the bone marrow microenvironment,” Nat. Cell Biol. 15(5), 533–543 (2013).
[Crossref] [PubMed]

Cao, B.

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[Crossref] [PubMed]

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V. Nandakumar, L. Kelbauskas, K. F. Hernandez, K. M. Lintecum, P. Senechal, K. J. Bussey, P. C. Davies, R. H. Johnson, and D. R. Meldrum, “Isotropic 3D nuclear morphometry of normal, fibrocystic and malignant breast epithelial cells reveals new structural alterations,” PLoS One 7(1), e29230 (2012).
[Crossref] [PubMed]

V. Nandakumar, L. Kelbauskas, R. Johnson, and D. Meldrum, “Quantitative characterization of preneoplastic progression using single-cell computed tomography and three-dimensional karyometry,” Cytometry A 79(1), 25–34 (2011).
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V. Nandakumar, L. Kelbauskas, K. F. Hernandez, K. M. Lintecum, P. Senechal, K. J. Bussey, P. C. Davies, R. H. Johnson, and D. R. Meldrum, “Isotropic 3D nuclear morphometry of normal, fibrocystic and malignant breast epithelial cells reveals new structural alterations,” PLoS One 7(1), e29230 (2012).
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Lippincott-Schwartz, J.

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. Böhme, 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(6208), 1257998 (2014).
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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. Böhme, 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(6208), 1257998 (2014).
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Lu, J.

C. Nombela-Arrieta, G. Pivarnik, B. Winkel, K. J. Canty, B. Harley, J. E. Mahoney, S.-Y. Park, J. Lu, A. Protopopov, and L. E. Silberstein, “Quantitative imaging of haematopoietic stem and progenitor cell localization and hypoxic status in the bone marrow microenvironment,” Nat. Cell Biol. 15(5), 533–543 (2013).
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F. Huang, G. Sirinakis, E. S. Allgeyer, L. K. Schroeder, W. C. Duim, E. B. Kromann, T. Phan, F. E. Rivera-Molina, J. R. Myers, I. Irnov, M. Lessard, Y. Zhang, M. A. Handel, C. Jacobs-Wagner, C. P. Lusk, J. E. Rothman, D. Toomre, M. J. Booth, and J. Bewersdorf, “Ultra-high resolution 3d imaging of whole cells,” Cell 166(4), 1028–1040 (2016).
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C. Nombela-Arrieta, G. Pivarnik, B. Winkel, K. J. Canty, B. Harley, J. E. Mahoney, S.-Y. Park, J. Lu, A. Protopopov, and L. E. Silberstein, “Quantitative imaging of haematopoietic stem and progenitor cell localization and hypoxic status in the bone marrow microenvironment,” Nat. Cell Biol. 15(5), 533–543 (2013).
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Y. Wu, P. Wawrzusin, J. Senseney, R. S. Fischer, R. Christensen, A. Santella, A. G. York, P. W. Winter, C. M. Waterman, Z. Bao, D. A. Colón-Ramos, M. McAuliffe, and H. Shroff, “Spatially isotropic four-dimensional imaging with dual-view plane illumination microscopy,” Nat. Biotechnol. 31(11), 1032–1038 (2013).
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J. McGinty, K. B. Tahir, R. Laine, C. B. Talbot, C. Dunsby, M. A. Neil, L. Quintana, J. Swoger, J. Sharpe, and P. M. French, “Fluorescence lifetime optical projection tomography,” J. Biophotonics 1(5), 390–394 (2008).
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V. Nandakumar, L. Kelbauskas, R. Johnson, and D. Meldrum, “Quantitative characterization of preneoplastic progression using single-cell computed tomography and three-dimensional karyometry,” Cytometry A 79(1), 25–34 (2011).
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L. Kelbauskas, R. Shetty, B. Cao, K. C. Wang, D. Smith, H. Wang, S. H. Chao, S. Gangaraju, B. Ashcroft, M. Kritzer, H. Glenn, R. H. Johnson, and D. R. Meldrum, “Optical computed tomography for spatially isotropic four-dimensional imaging of live single cells,” Sci. Adv. 3(12), e1602580 (2017).
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R. M. Shetty, J. R. Myers, M. Sreenivasulu, W. Teller, J. Vela, J. Houkal, S.-H. Chao, R. H. Johnson, L. Kelbauskas, H. Wang, and D. R. Meldrum, “Characterization and comparison of three microfabrication methods to generate out-of-plane microvortices for single cell rotation and 3d imaging,” J. Micromech. Microeng. 27(1), 015004 (2016).
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V. Nandakumar, L. Kelbauskas, K. F. Hernandez, K. M. Lintecum, P. Senechal, K. J. Bussey, P. C. Davies, R. H. Johnson, and D. R. Meldrum, “Isotropic 3D nuclear morphometry of normal, fibrocystic and malignant breast epithelial cells reveals new structural alterations,” PLoS One 7(1), e29230 (2012).
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M. Rieckher, U. J. Birk, H. Meyer, J. Ripoll, and N. Tavernarakis, “Microscopic optical projection tomography in vivo,” PLoS One 6(4), e18963 (2011).
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Meyer, M. G.

Q. Miao, J. Hayenga, M. G. Meyer, T. Neumann, A. C. Nelson, and E. J. Seibel, “Resolution improvement in optical projection tomography by the focal scanning method,” Opt. Lett. 35(20), 3363–3365 (2010).
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Q. Miao, J. R. Rahn, A. Tourovskaia, M. G. Meyer, T. Neumann, A. C. Nelson, and E. J. Seibel, “Dual-modal three-dimensional imaging of single cells with isometric high resolution using an optical projection tomography microscope,” J. Biomed. Opt. 14, 064035 (2009).

Miao, Q.

Q. Miao, J. Hayenga, M. G. Meyer, T. Neumann, A. C. Nelson, and E. J. Seibel, “Resolution improvement in optical projection tomography by the focal scanning method,” Opt. Lett. 35(20), 3363–3365 (2010).
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Q. Miao, J. R. Rahn, A. Tourovskaia, M. G. Meyer, T. Neumann, A. C. Nelson, and E. J. Seibel, “Dual-modal three-dimensional imaging of single cells with isometric high resolution using an optical projection tomography microscope,” J. Biomed. Opt. 14, 064035 (2009).

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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. Böhme, 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(6208), 1257998 (2014).
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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. Böhme, 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(6208), 1257998 (2014).
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F. Huang, G. Sirinakis, E. S. Allgeyer, L. K. Schroeder, W. C. Duim, E. B. Kromann, T. Phan, F. E. Rivera-Molina, J. R. Myers, I. Irnov, M. Lessard, Y. Zhang, M. A. Handel, C. Jacobs-Wagner, C. P. Lusk, J. E. Rothman, D. Toomre, M. J. Booth, and J. Bewersdorf, “Ultra-high resolution 3d imaging of whole cells,” Cell 166(4), 1028–1040 (2016).
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R. M. Shetty, J. R. Myers, M. Sreenivasulu, W. Teller, J. Vela, J. Houkal, S.-H. Chao, R. H. Johnson, L. Kelbauskas, H. Wang, and D. R. Meldrum, “Characterization and comparison of three microfabrication methods to generate out-of-plane microvortices for single cell rotation and 3d imaging,” J. Micromech. Microeng. 27(1), 015004 (2016).
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V. Nandakumar, L. Kelbauskas, K. F. Hernandez, K. M. Lintecum, P. Senechal, K. J. Bussey, P. C. Davies, R. H. Johnson, and D. R. Meldrum, “Isotropic 3D nuclear morphometry of normal, fibrocystic and malignant breast epithelial cells reveals new structural alterations,” PLoS One 7(1), e29230 (2012).
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V. Nandakumar, L. Kelbauskas, R. Johnson, and D. Meldrum, “Quantitative characterization of preneoplastic progression using single-cell computed tomography and three-dimensional karyometry,” Cytometry A 79(1), 25–34 (2011).
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J. McGinty, K. B. Tahir, R. Laine, C. B. Talbot, C. Dunsby, M. A. Neil, L. Quintana, J. Swoger, J. Sharpe, and P. M. French, “Fluorescence lifetime optical projection tomography,” J. Biophotonics 1(5), 390–394 (2008).
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Q. Miao, J. Hayenga, M. G. Meyer, T. Neumann, A. C. Nelson, and E. J. Seibel, “Resolution improvement in optical projection tomography by the focal scanning method,” Opt. Lett. 35(20), 3363–3365 (2010).
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Q. Miao, J. R. Rahn, A. Tourovskaia, M. G. Meyer, T. Neumann, A. C. Nelson, and E. J. Seibel, “Dual-modal three-dimensional imaging of single cells with isometric high resolution using an optical projection tomography microscope,” J. Biomed. Opt. 14, 064035 (2009).

Neumann, T.

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C. Nombela-Arrieta, G. Pivarnik, B. Winkel, K. J. Canty, B. Harley, J. E. Mahoney, S.-Y. Park, J. Lu, A. Protopopov, and L. E. Silberstein, “Quantitative imaging of haematopoietic stem and progenitor cell localization and hypoxic status in the bone marrow microenvironment,” Nat. Cell Biol. 15(5), 533–543 (2013).
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A. H. Iwane, T. Funatsu, Y. Harada, M. Tokunaga, O. Ohara, S. Morimoto, and T. Yanagida, “Single molecular assay of individual ATP turnover by a myosin-GFP fusion protein expressed in vitro,” FEBS Lett. 407(2), 235–238 (1997).
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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).
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F. Huang, G. Sirinakis, E. S. Allgeyer, L. K. Schroeder, W. C. Duim, E. B. Kromann, T. Phan, F. E. Rivera-Molina, J. R. Myers, I. Irnov, M. Lessard, Y. Zhang, M. A. Handel, C. Jacobs-Wagner, C. P. Lusk, J. E. Rothman, D. Toomre, M. J. Booth, and J. Bewersdorf, “Ultra-high resolution 3d imaging of whole cells,” Cell 166(4), 1028–1040 (2016).
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C. Nombela-Arrieta, G. Pivarnik, B. Winkel, K. J. Canty, B. Harley, J. E. Mahoney, S.-Y. Park, J. Lu, A. Protopopov, and L. E. Silberstein, “Quantitative imaging of haematopoietic stem and progenitor cell localization and hypoxic status in the bone marrow microenvironment,” Nat. Cell Biol. 15(5), 533–543 (2013).
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C. Nombela-Arrieta, G. Pivarnik, B. Winkel, K. J. Canty, B. Harley, J. E. Mahoney, S.-Y. Park, J. Lu, A. Protopopov, and L. E. Silberstein, “Quantitative imaging of haematopoietic stem and progenitor cell localization and hypoxic status in the bone marrow microenvironment,” Nat. Cell Biol. 15(5), 533–543 (2013).
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J. McGinty, K. B. Tahir, R. Laine, C. B. Talbot, C. Dunsby, M. A. Neil, L. Quintana, J. Swoger, J. Sharpe, and P. M. French, “Fluorescence lifetime optical projection tomography,” J. Biophotonics 1(5), 390–394 (2008).
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Q. Miao, J. R. Rahn, A. Tourovskaia, M. G. Meyer, T. Neumann, A. C. Nelson, and E. J. Seibel, “Dual-modal three-dimensional imaging of single cells with isometric high resolution using an optical projection tomography microscope,” J. Biomed. Opt. 14, 064035 (2009).

M. Fauver, E. Seibel, J. R. Rahn, M. Meyer, F. Patten, T. Neumann, and A. Nelson, “Three-dimensional imaging of single isolated cell nuclei using optical projection tomography,” Opt. Express 13(11), 4210–4223 (2005).
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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. Böhme, 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(6208), 1257998 (2014).
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M. Rieckher, U. J. Birk, H. Meyer, J. Ripoll, and N. Tavernarakis, “Microscopic optical projection tomography in vivo,” PLoS One 6(4), e18963 (2011).
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M. Rieckher, U. J. Birk, H. Meyer, J. Ripoll, and N. Tavernarakis, “Microscopic optical projection tomography in vivo,” PLoS One 6(4), e18963 (2011).
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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. Böhme, 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(6208), 1257998 (2014).
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Romero, D. P.

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. Böhme, 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(6208), 1257998 (2014).
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F. Huang, G. Sirinakis, E. S. Allgeyer, L. K. Schroeder, W. C. Duim, E. B. Kromann, T. Phan, F. E. Rivera-Molina, J. R. Myers, I. Irnov, M. Lessard, Y. Zhang, M. A. Handel, C. Jacobs-Wagner, C. P. Lusk, J. E. Rothman, D. Toomre, M. J. Booth, and J. Bewersdorf, “Ultra-high resolution 3d imaging of whole cells,” Cell 166(4), 1028–1040 (2016).
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Senechal, P.

V. Nandakumar, L. Kelbauskas, K. F. Hernandez, K. M. Lintecum, P. Senechal, K. J. Bussey, P. C. Davies, R. H. Johnson, and D. R. Meldrum, “Isotropic 3D nuclear morphometry of normal, fibrocystic and malignant breast epithelial cells reveals new structural alterations,” PLoS One 7(1), e29230 (2012).
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[Crossref] [PubMed]

Sharpe, J.

J. Mayer, A. Robert-Moreno, R. Danuser, J. V. Stein, J. Sharpe, and J. Swoger, “OPTiSPIM: integrating optical projection tomography in light sheet microscopy extends specimen characterization to nonfluorescent contrasts,” Opt. Lett. 39(4), 1053–1056 (2014).
[Crossref] [PubMed]

J.-F. Colas and J. Sharpe, “Live optical projection tomography,” Organogenesis 5(4), 211–216 (2009).
[Crossref] [PubMed]

J. McGinty, K. B. Tahir, R. Laine, C. B. Talbot, C. Dunsby, M. A. Neil, L. Quintana, J. Swoger, J. Sharpe, and P. M. French, “Fluorescence lifetime optical projection tomography,” J. Biophotonics 1(5), 390–394 (2008).
[Crossref] [PubMed]

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]

Shetty, R.

L. Kelbauskas, R. Shetty, B. Cao, K. C. Wang, D. Smith, H. Wang, S. H. Chao, S. Gangaraju, B. Ashcroft, M. Kritzer, H. Glenn, R. H. Johnson, and D. R. Meldrum, “Optical computed tomography for spatially isotropic four-dimensional imaging of live single cells,” Sci. Adv. 3(12), e1602580 (2017).
[Crossref] [PubMed]

Shetty, R. M.

B. Cao, L. Kelbauskas, S. Chan, R. M. Shetty, D. Smith, and D. R. Meldrum, “Rotation of single live mammalian cells using dynamic holographic optical tweezers,” Opt. Lasers Eng. 92, 70–75 (2017).
[Crossref]

R. M. Shetty, J. R. Myers, M. Sreenivasulu, W. Teller, J. Vela, J. Houkal, S.-H. Chao, R. H. Johnson, L. Kelbauskas, H. Wang, and D. R. Meldrum, “Characterization and comparison of three microfabrication methods to generate out-of-plane microvortices for single cell rotation and 3d imaging,” J. Micromech. Microeng. 27(1), 015004 (2016).
[Crossref]

Shroff, H.

Y. Wu, P. Wawrzusin, J. Senseney, R. S. Fischer, R. Christensen, A. Santella, A. G. York, P. W. Winter, C. M. Waterman, Z. Bao, D. A. Colón-Ramos, M. McAuliffe, and H. Shroff, “Spatially isotropic four-dimensional imaging with dual-view plane illumination microscopy,” Nat. Biotechnol. 31(11), 1032–1038 (2013).
[Crossref] [PubMed]

Silberstein, L. E.

C. Nombela-Arrieta, G. Pivarnik, B. Winkel, K. J. Canty, B. Harley, J. E. Mahoney, S.-Y. Park, J. Lu, A. Protopopov, and L. E. Silberstein, “Quantitative imaging of haematopoietic stem and progenitor cell localization and hypoxic status in the bone marrow microenvironment,” Nat. Cell Biol. 15(5), 533–543 (2013).
[Crossref] [PubMed]

Sirinakis, G.

F. Huang, G. Sirinakis, E. S. Allgeyer, L. K. Schroeder, W. C. Duim, E. B. Kromann, T. Phan, F. E. Rivera-Molina, J. R. Myers, I. Irnov, M. Lessard, Y. Zhang, M. A. Handel, C. Jacobs-Wagner, C. P. Lusk, J. E. Rothman, D. Toomre, M. J. Booth, and J. Bewersdorf, “Ultra-high resolution 3d imaging of whole cells,” Cell 166(4), 1028–1040 (2016).
[Crossref] [PubMed]

Smith, D.

L. Kelbauskas, R. Shetty, B. Cao, K. C. Wang, D. Smith, H. Wang, S. H. Chao, S. Gangaraju, B. Ashcroft, M. Kritzer, H. Glenn, R. H. Johnson, and D. R. Meldrum, “Optical computed tomography for spatially isotropic four-dimensional imaging of live single cells,” Sci. Adv. 3(12), e1602580 (2017).
[Crossref] [PubMed]

B. Cao, L. Kelbauskas, S. Chan, R. M. Shetty, D. Smith, and D. R. Meldrum, “Rotation of single live mammalian cells using dynamic holographic optical tweezers,” Opt. Lasers Eng. 92, 70–75 (2017).
[Crossref]

Sreenivasulu, M.

R. M. Shetty, J. R. Myers, M. Sreenivasulu, W. Teller, J. Vela, J. Houkal, S.-H. Chao, R. H. Johnson, L. Kelbauskas, H. Wang, and D. R. Meldrum, “Characterization and comparison of three microfabrication methods to generate out-of-plane microvortices for single cell rotation and 3d imaging,” J. Micromech. Microeng. 27(1), 015004 (2016).
[Crossref]

Stein, J. V.

Stelzer, E. H.

P. J. Keller, A. D. Schmidt, J. Wittbrodt, and E. H. Stelzer, “Reconstruction of zebrafish early embryonic development by scanned light sheet microscopy,” Science 322(5904), 1065–1069 (2008).
[Crossref] [PubMed]

Stephens, D. J.

D. J. Stephens and V. J. Allan, “Light microscopy techniques for live cell imaging,” Science 300(5616), 82–86 (2003).
[Crossref] [PubMed]

Su, H.

P. Dubey, H. Su, N. Adonai, S. Du, A. Rosato, J. Braun, S. S. Gambhir, and O. N. Witte, “Quantitative imaging of the T cell antitumor response by positron-emission tomography,” Proc. Natl. Acad. Sci. U.S.A. 100(3), 1232–1237 (2003).
[Crossref] [PubMed]

Swoger, J.

J. Mayer, A. Robert-Moreno, R. Danuser, J. V. Stein, J. Sharpe, and J. Swoger, “OPTiSPIM: integrating optical projection tomography in light sheet microscopy extends specimen characterization to nonfluorescent contrasts,” Opt. Lett. 39(4), 1053–1056 (2014).
[Crossref] [PubMed]

J. McGinty, K. B. Tahir, R. Laine, C. B. Talbot, C. Dunsby, M. A. Neil, L. Quintana, J. Swoger, J. Sharpe, and P. M. French, “Fluorescence lifetime optical projection tomography,” J. Biophotonics 1(5), 390–394 (2008).
[Crossref] [PubMed]

Tahir, K. B.

J. McGinty, K. B. Tahir, R. Laine, C. B. Talbot, C. Dunsby, M. A. Neil, L. Quintana, J. Swoger, J. Sharpe, and P. M. French, “Fluorescence lifetime optical projection tomography,” J. Biophotonics 1(5), 390–394 (2008).
[Crossref] [PubMed]

Talbot, C. B.

J. McGinty, K. B. Tahir, R. Laine, C. B. Talbot, C. Dunsby, M. A. Neil, L. Quintana, J. Swoger, J. Sharpe, and P. M. French, “Fluorescence lifetime optical projection tomography,” J. Biophotonics 1(5), 390–394 (2008).
[Crossref] [PubMed]

Tavernarakis, N.

M. Rieckher, U. J. Birk, H. Meyer, J. Ripoll, and N. Tavernarakis, “Microscopic optical projection tomography in vivo,” PLoS One 6(4), e18963 (2011).
[Crossref] [PubMed]

Teller, W.

R. M. Shetty, J. R. Myers, M. Sreenivasulu, W. Teller, J. Vela, J. Houkal, S.-H. Chao, R. H. Johnson, L. Kelbauskas, H. Wang, and D. R. Meldrum, “Characterization and comparison of three microfabrication methods to generate out-of-plane microvortices for single cell rotation and 3d imaging,” J. Micromech. Microeng. 27(1), 015004 (2016).
[Crossref]

Tokunaga, M.

M. Tokunaga, N. Imamoto, and K. Sakata-Sogawa, “Highly inclined thin illumination enables clear single-molecule imaging in cells,” Nat. Methods 5(2), 159–161 (2008).
[Crossref] [PubMed]

A. H. Iwane, T. Funatsu, Y. Harada, M. Tokunaga, O. Ohara, S. Morimoto, and T. Yanagida, “Single molecular assay of individual ATP turnover by a myosin-GFP fusion protein expressed in vitro,” FEBS Lett. 407(2), 235–238 (1997).
[Crossref] [PubMed]

Toomre, D.

F. Huang, G. Sirinakis, E. S. Allgeyer, L. K. Schroeder, W. C. Duim, E. B. Kromann, T. Phan, F. E. Rivera-Molina, J. R. Myers, I. Irnov, M. Lessard, Y. Zhang, M. A. Handel, C. Jacobs-Wagner, C. P. Lusk, J. E. Rothman, D. Toomre, M. J. Booth, and J. Bewersdorf, “Ultra-high resolution 3d imaging of whole cells,” Cell 166(4), 1028–1040 (2016).
[Crossref] [PubMed]

Tourovskaia, A.

Q. Miao, J. R. Rahn, A. Tourovskaia, M. G. Meyer, T. Neumann, A. C. Nelson, and E. J. Seibel, “Dual-modal three-dimensional imaging of single cells with isometric high resolution using an optical projection tomography microscope,” J. Biomed. Opt. 14, 064035 (2009).

Tulu, U. S.

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. Böhme, 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(6208), 1257998 (2014).
[Crossref] [PubMed]

Vale, R. D.

D. W. Pierce, N. Hom-Booher, and R. D. Vale, “Imaging individual green fluorescent proteins,” Nature 388(6640), 338 (1997).
[Crossref] [PubMed]

Vela, J.

R. M. Shetty, J. R. Myers, M. Sreenivasulu, W. Teller, J. Vela, J. Houkal, S.-H. Chao, R. H. Johnson, L. Kelbauskas, H. Wang, and D. R. Meldrum, “Characterization and comparison of three microfabrication methods to generate out-of-plane microvortices for single cell rotation and 3d imaging,” J. Micromech. Microeng. 27(1), 015004 (2016).
[Crossref]

Wang, H.

L. Kelbauskas, R. Shetty, B. Cao, K. C. Wang, D. Smith, H. Wang, S. H. Chao, S. Gangaraju, B. Ashcroft, M. Kritzer, H. Glenn, R. H. Johnson, and D. R. Meldrum, “Optical computed tomography for spatially isotropic four-dimensional imaging of live single cells,” Sci. Adv. 3(12), e1602580 (2017).
[Crossref] [PubMed]

R. M. Shetty, J. R. Myers, M. Sreenivasulu, W. Teller, J. Vela, J. Houkal, S.-H. Chao, R. H. Johnson, L. Kelbauskas, H. Wang, and D. R. Meldrum, “Characterization and comparison of three microfabrication methods to generate out-of-plane microvortices for single cell rotation and 3d imaging,” J. Micromech. Microeng. 27(1), 015004 (2016).
[Crossref]

Wang, J. T.

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. Böhme, 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(6208), 1257998 (2014).
[Crossref] [PubMed]

Wang, K.

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. Böhme, 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(6208), 1257998 (2014).
[Crossref] [PubMed]

Wang, K. C.

L. Kelbauskas, R. Shetty, B. Cao, K. C. Wang, D. Smith, H. Wang, S. H. Chao, S. Gangaraju, B. Ashcroft, M. Kritzer, H. Glenn, R. H. Johnson, and D. R. Meldrum, “Optical computed tomography for spatially isotropic four-dimensional imaging of live single cells,” Sci. Adv. 3(12), e1602580 (2017).
[Crossref] [PubMed]

Waterman, C. M.

Y. Wu, P. Wawrzusin, J. Senseney, R. S. Fischer, R. Christensen, A. Santella, A. G. York, P. W. Winter, C. M. Waterman, Z. Bao, D. A. Colón-Ramos, M. McAuliffe, and H. Shroff, “Spatially isotropic four-dimensional imaging with dual-view plane illumination microscopy,” Nat. Biotechnol. 31(11), 1032–1038 (2013).
[Crossref] [PubMed]

Wawrzusin, P.

Y. Wu, P. Wawrzusin, J. Senseney, R. S. Fischer, R. Christensen, A. Santella, A. G. York, P. W. Winter, C. M. Waterman, Z. Bao, D. A. Colón-Ramos, M. McAuliffe, and H. Shroff, “Spatially isotropic four-dimensional imaging with dual-view plane illumination microscopy,” Nat. Biotechnol. 31(11), 1032–1038 (2013).
[Crossref] [PubMed]

Weiss, S.

S. Weiss, “Fluorescence spectroscopy of single biomolecules,” Science 283(5408), 1676–1683 (1999).
[Crossref] [PubMed]

Winkel, B.

C. Nombela-Arrieta, G. Pivarnik, B. Winkel, K. J. Canty, B. Harley, J. E. Mahoney, S.-Y. Park, J. Lu, A. Protopopov, and L. E. Silberstein, “Quantitative imaging of haematopoietic stem and progenitor cell localization and hypoxic status in the bone marrow microenvironment,” Nat. Cell Biol. 15(5), 533–543 (2013).
[Crossref] [PubMed]

Winter, P. W.

Y. Wu, P. Wawrzusin, J. Senseney, R. S. Fischer, R. Christensen, A. Santella, A. G. York, P. W. Winter, C. M. Waterman, Z. Bao, D. A. Colón-Ramos, M. McAuliffe, and H. Shroff, “Spatially isotropic four-dimensional imaging with dual-view plane illumination microscopy,” Nat. Biotechnol. 31(11), 1032–1038 (2013).
[Crossref] [PubMed]

Wittbrodt, J.

P. J. Keller, A. D. Schmidt, J. Wittbrodt, and E. H. Stelzer, “Reconstruction of zebrafish early embryonic development by scanned light sheet microscopy,” Science 322(5904), 1065–1069 (2008).
[Crossref] [PubMed]

Witte, O. N.

P. Dubey, H. Su, N. Adonai, S. Du, A. Rosato, J. Braun, S. S. Gambhir, and O. N. Witte, “Quantitative imaging of the T cell antitumor response by positron-emission tomography,” Proc. Natl. Acad. Sci. U.S.A. 100(3), 1232–1237 (2003).
[Crossref] [PubMed]

Wu, X. S.

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. Böhme, 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(6208), 1257998 (2014).
[Crossref] [PubMed]

Wu, Y.

Y. Wu, P. Wawrzusin, J. Senseney, R. S. Fischer, R. Christensen, A. Santella, A. G. York, P. W. Winter, C. M. Waterman, Z. Bao, D. A. Colón-Ramos, M. McAuliffe, and H. Shroff, “Spatially isotropic four-dimensional imaging with dual-view plane illumination microscopy,” Nat. Biotechnol. 31(11), 1032–1038 (2013).
[Crossref] [PubMed]

Yanagida, T.

A. H. Iwane, T. Funatsu, Y. Harada, M. Tokunaga, O. Ohara, S. Morimoto, and T. Yanagida, “Single molecular assay of individual ATP turnover by a myosin-GFP fusion protein expressed in vitro,” FEBS Lett. 407(2), 235–238 (1997).
[Crossref] [PubMed]

York, A. G.

Y. Wu, P. Wawrzusin, J. Senseney, R. S. Fischer, R. Christensen, A. Santella, A. G. York, P. W. Winter, C. M. Waterman, Z. Bao, D. A. Colón-Ramos, M. McAuliffe, and H. Shroff, “Spatially isotropic four-dimensional imaging with dual-view plane illumination microscopy,” Nat. Biotechnol. 31(11), 1032–1038 (2013).
[Crossref] [PubMed]

Zhang, Y.

F. Huang, G. Sirinakis, E. S. Allgeyer, L. K. Schroeder, W. C. Duim, E. B. Kromann, T. Phan, F. E. Rivera-Molina, J. R. Myers, I. Irnov, M. Lessard, Y. Zhang, M. A. Handel, C. Jacobs-Wagner, C. P. Lusk, J. E. Rothman, D. Toomre, M. J. Booth, and J. Bewersdorf, “Ultra-high resolution 3d imaging of whole cells,” Cell 166(4), 1028–1040 (2016).
[Crossref] [PubMed]

Appl. Opt. (1)

Biophys. J. (1)

G. Fuhr, R. Glaser, and R. Hagedorn, “Rotation of dielectrics in a rotating electric high-frequency field. Model experiments and theoretical explanation of the rotation effect of living cells,” Biophys. J. 49(2), 395–402 (1986).
[Crossref] [PubMed]

Cell (1)

F. Huang, G. Sirinakis, E. S. Allgeyer, L. K. Schroeder, W. C. Duim, E. B. Kromann, T. Phan, F. E. Rivera-Molina, J. R. Myers, I. Irnov, M. Lessard, Y. Zhang, M. A. Handel, C. Jacobs-Wagner, C. P. Lusk, J. E. Rothman, D. Toomre, M. J. Booth, and J. Bewersdorf, “Ultra-high resolution 3d imaging of whole cells,” Cell 166(4), 1028–1040 (2016).
[Crossref] [PubMed]

Cytometry A (1)

V. Nandakumar, L. Kelbauskas, R. Johnson, and D. Meldrum, “Quantitative characterization of preneoplastic progression using single-cell computed tomography and three-dimensional karyometry,” Cytometry A 79(1), 25–34 (2011).
[Crossref] [PubMed]

FEBS Lett. (1)

A. H. Iwane, T. Funatsu, Y. Harada, M. Tokunaga, O. Ohara, S. Morimoto, and T. Yanagida, “Single molecular assay of individual ATP turnover by a myosin-GFP fusion protein expressed in vitro,” FEBS Lett. 407(2), 235–238 (1997).
[Crossref] [PubMed]

J. Biomed. Opt. (1)

Q. Miao, J. R. Rahn, A. Tourovskaia, M. G. Meyer, T. Neumann, A. C. Nelson, and E. J. Seibel, “Dual-modal three-dimensional imaging of single cells with isometric high resolution using an optical projection tomography microscope,” J. Biomed. Opt. 14, 064035 (2009).

J. Biophotonics (1)

J. McGinty, K. B. Tahir, R. Laine, C. B. Talbot, C. Dunsby, M. A. Neil, L. Quintana, J. Swoger, J. Sharpe, and P. M. French, “Fluorescence lifetime optical projection tomography,” J. Biophotonics 1(5), 390–394 (2008).
[Crossref] [PubMed]

J. Micromech. Microeng. (1)

R. M. Shetty, J. R. Myers, M. Sreenivasulu, W. Teller, J. Vela, J. Houkal, S.-H. Chao, R. H. Johnson, L. Kelbauskas, H. Wang, and D. R. Meldrum, “Characterization and comparison of three microfabrication methods to generate out-of-plane microvortices for single cell rotation and 3d imaging,” J. Micromech. Microeng. 27(1), 015004 (2016).
[Crossref]

J. Microsc. (1)

M. G. Gustafsson, D. A. Agard, and J. W. Sedat, “I5M: 3D widefield light microscopy with better than 100 nm axial resolution,” J. Microsc. 195(Pt 1), 10–16 (1999).
[Crossref] [PubMed]

Nat. Biotechnol. (1)

Y. Wu, P. Wawrzusin, J. Senseney, R. S. Fischer, R. Christensen, A. Santella, A. G. York, P. W. Winter, C. M. Waterman, Z. Bao, D. A. Colón-Ramos, M. McAuliffe, and H. Shroff, “Spatially isotropic four-dimensional imaging with dual-view plane illumination microscopy,” Nat. Biotechnol. 31(11), 1032–1038 (2013).
[Crossref] [PubMed]

Nat. Cell Biol. (1)

C. Nombela-Arrieta, G. Pivarnik, B. Winkel, K. J. Canty, B. Harley, J. E. Mahoney, S.-Y. Park, J. Lu, A. Protopopov, and L. E. Silberstein, “Quantitative imaging of haematopoietic stem and progenitor cell localization and hypoxic status in the bone marrow microenvironment,” Nat. Cell Biol. 15(5), 533–543 (2013).
[Crossref] [PubMed]

Nat. Methods (1)

M. Tokunaga, N. Imamoto, and K. Sakata-Sogawa, “Highly inclined thin illumination enables clear single-molecule imaging in cells,” Nat. Methods 5(2), 159–161 (2008).
[Crossref] [PubMed]

Nature (1)

D. W. Pierce, N. Hom-Booher, and R. D. Vale, “Imaging individual green fluorescent proteins,” Nature 388(6640), 338 (1997).
[Crossref] [PubMed]

Opt. Express (3)

Opt. Lasers Eng. (1)

B. Cao, L. Kelbauskas, S. Chan, R. M. Shetty, D. Smith, and D. R. Meldrum, “Rotation of single live mammalian cells using dynamic holographic optical tweezers,” Opt. Lasers Eng. 92, 70–75 (2017).
[Crossref]

Opt. Lett. (2)

Optica (1)

Organogenesis (1)

J.-F. Colas and J. Sharpe, “Live optical projection tomography,” Organogenesis 5(4), 211–216 (2009).
[Crossref] [PubMed]

PLoS One (2)

M. Rieckher, U. J. Birk, H. Meyer, J. Ripoll, and N. Tavernarakis, “Microscopic optical projection tomography in vivo,” PLoS One 6(4), e18963 (2011).
[Crossref] [PubMed]

V. Nandakumar, L. Kelbauskas, K. F. Hernandez, K. M. Lintecum, P. Senechal, K. J. Bussey, P. C. Davies, R. H. Johnson, and D. R. Meldrum, “Isotropic 3D nuclear morphometry of normal, fibrocystic and malignant breast epithelial cells reveals new structural alterations,” PLoS One 7(1), e29230 (2012).
[Crossref] [PubMed]

Proc. Natl. Acad. Sci. U.S.A. (1)

P. Dubey, H. Su, N. Adonai, S. Du, A. Rosato, J. Braun, S. S. Gambhir, and O. N. Witte, “Quantitative imaging of the T cell antitumor response by positron-emission tomography,” Proc. Natl. Acad. Sci. U.S.A. 100(3), 1232–1237 (2003).
[Crossref] [PubMed]

Sci. Adv. (1)

L. Kelbauskas, R. Shetty, B. Cao, K. C. Wang, D. Smith, H. Wang, S. H. Chao, S. Gangaraju, B. Ashcroft, M. Kritzer, H. Glenn, R. H. Johnson, and D. R. Meldrum, “Optical computed tomography for spatially isotropic four-dimensional imaging of live single cells,” Sci. Adv. 3(12), e1602580 (2017).
[Crossref] [PubMed]

Science (5)

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]

P. J. Keller, A. D. Schmidt, J. Wittbrodt, and E. H. Stelzer, “Reconstruction of zebrafish early embryonic development by scanned light sheet microscopy,” Science 322(5904), 1065–1069 (2008).
[Crossref] [PubMed]

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. Böhme, 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(6208), 1257998 (2014).
[Crossref] [PubMed]

D. J. Stephens and V. J. Allan, “Light microscopy techniques for live cell imaging,” Science 300(5616), 82–86 (2003).
[Crossref] [PubMed]

S. Weiss, “Fluorescence spectroscopy of single biomolecules,” Science 283(5408), 1676–1683 (1999).
[Crossref] [PubMed]

Other (3)

E. R. Dowski, Jr. and G. E. Johnson, “Wavefront coding: A modern method of achieving high-performance and/or low-cost imaging systems,” in SPIE's International Symposium on Optical Science, Engineering, and Instrumentation (International Society for Optics and Photonics1999), pp. 137–145.

H. Lodish, Molecular Cell Biology (Macmillan, 2008).

J. G. Black, Microbiology: Principles and Explorations (John Wiley & Sons, 2008).

Supplementary Material (3)

NameDescription
» Visualization 1       A live single-cell 3D image obtained by eLCCT.
» Visualization 2       A live single-cell 3D image obtained by hLCCT.
» Visualization 3       Live single-cell 3D image obtained by confocal microscopy.

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Figures (6)

Fig. 1
Fig. 1 (a) Optical system setup of hLCCT. FL: fiber-coupled laser; L1, L2: achromatic lenses; MM: multichroic mirror; EF: emission filter; M: mirror; TL: tube lens; EMCCD: cooled electron-multiplying charge-coupled device; PZT: piezoelectric transducer; OL: objective lens; MS: microscope stage; ECC: electrocage chip; PT: pipette tip; S: syringe; RA: rotation area (electrocage). The illumination beam and the fluorescence are shown in purple and blue, respectively. (b) A detailed schematic of the HILO illumination. R is the diameter of the field of view (FOV). The calculated incident angle is 77.8°, and the thickness of the HILO illumination is 1.7 μm.
Fig. 2
Fig. 2 (a) Changes in HILO beam thickness at different locations of the objective lens along the optical axis; (b) Experimental setup for measuring the HILO beam thickness; Quantitative measurement of the HILO beam thickness at the center (c) and four corners (d) of the FOV, as a function of the objective lens position along the optical Z axis. Five independent measurements were performed to characterize the thickness in the center of the FOV, whereas one measurement was used for the beam thickness in each of the four corners. The error bars in (c) represent the standard deviation of the thickness measurements obtained with five independent measurements with different beads at each Zobj location, the variation of the error bars at different objective lens Zobj position may be caused by the PZT electrical noise. The black dot indicates the average thickness of the HILO beam at the corresponding Zobj location. A thickness change in (d) at Zobj = 2 μm at the corner point X = −4 μm, Y = 4 μm is 0.25 μm, and is within the measurement error. (e) Representative intensity profiles of the beads at the center of the imaging plane when the objective lens was located at 70 µm. The result was averaged over five different single beads. Zb indicates the beads location along the optical axis.
Fig. 3
Fig. 3 (a) Comparison of photobleaching kinetics between hLCCT (black squares) and eLCCT (red circles). The measurements were fit with an exponential decay function (solid curves). The fluorescence intensity decay rate observed with hLCCT was 17.1 times lower than eLCCT. (b) and (c) A comparison of photobleaching observed with hLCCT and eLCCT. Mitochondria of two different CP-A cells were fluorescently stained with Mitotracker Red. The cells were continuously illuminated for 300 s in both cases. The imaging conditions were set to provide comparable maximum fluorescence signals by adjusting the excitation power. The fluorescence emission intensity was calculated by averaging the signal of a feature inside of the solid yellow and red box in hLCCT and eLCCT, respectively.
Fig. 4
Fig. 4 (a) Contrast comparison of reconstructed 3D images of five K562 cell nuclei obtained using the hLCCT and eLCCT imaging methods. The contrast is two or more times higher in hLCCT than that obtained with eLCCT. (b) A representative example of 3D cell images contrast comparison using the eLCCT and hLCCT methods. The contrast is computed using the average intensities in the red box as Imax and blue box as Imin. The contrast of the 3D cell image acquired with hLCCT is enhanced two-fold compared with eLCCT.
Fig. 5
Fig. 5 Comparison of (a) eLCCT, (b) hLCCT, and (c) confocal images of a K562 cell nucleus. Maximum intensity projections of a 3D reconstructed volumetric image showing the nucleus in two orthogonal orientations (0° - upper panel, 90° - lower panel) generated with the corresponding imaging modalities. Scale bars: 5 µm. Visualization 1, Visualization 2, and Visualization 3 demonstrate the reconstructed 3D images of the nucleus in case of eLCCT, hLCCT, and confocal Z-stacks.
Fig. 6
Fig. 6 Schematic of how the FOV was determined in the hLCCT setup. R is the diameter of the FOV.

Equations (2)

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dz=R/tanθ
θ=arcsin[ x/( n× f obj ) ]

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