Abstract

Apart from the spatial resolution enhancement, scaling of temporal resolution, equivalently the imaging throughput, of fluorescence microscopy is of equal importance in advancing cell biology and clinical diagnostics. Yet, this attribute has mostly been overlooked because of the inherent speed limitation of existing imaging strategies. To address the challenge, we employ an all-optical laser-scanning mechanism, enabled by an array of reconfigurable spatiotemporally-encoded virtual sources, to demonstrate ultrafast fluorescence microscopy at line-scan rate as high as 8 MHz. We show that this technique enables high-throughput single-cell microfluidic fluorescence imaging at 75,000 cells/second and high-speed cellular 2D dynamical imaging at 3,000 frames per second, outperforming the state-of-the-art high-speed cameras and the gold-standard laser scanning strategies. Together with its wide compatibility to the existing imaging modalities, this technology could empower new forms of high-throughput and high-speed biological fluorescence microscopy that was once challenged.

© 2017 Optical Society of America

Full Article  |  PDF Article
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References

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2016 (2)

J. L. Wu, Y. Q. Xu, J. J. Xu, X. X. Wei, A. C. S. Chan, A. H. L. Tang, A. K. S. Lau, B. M. F. Chung, H. Cheung Shum, E. Y. Lam, K. K. Y. Wong, and K. K. Tsia, “Ultrafast laser-scanning time-stretch imaging at visible wavelengths,” Light Sci. Appl. 6(1), e16196 (2016).
[Crossref]

A. K. S. Lau, H. C. Shum, K. K. Y. Wong, and K. K. Tsia, “Optofluidic time-stretch imaging - an emerging tool for high-throughput imaging flow cytometry,” Lab Chip 16(10), 1743–1756 (2016).
[Crossref] [PubMed]

2015 (2)

J. Schneider, J. Zahn, M. Maglione, S. J. Sigrist, J. Marquard, J. Chojnacki, H. G. Kräusslich, S. J. Sahl, J. Engelhardt, and S. W. Hell, “Ultrafast, temporally stochastic STED nanoscopy of millisecond dynamics,” Nat. Methods 12(9), 827–830 (2015).
[Crossref] [PubMed]

E. Betzig, “Single molecules, cells, and super-resolution optics (Nobel lecture),” Angew. Chem. Int. Ed. Engl. 54(28), 8034–8053 (2015).
[Crossref] [PubMed]

2014 (5)

G. R. B. E. Römera and P. Bechtold, “Electro-optic and acousto-optic laser beam scanners,” Phys. Procedia 56, 29–39 (2014).
[Crossref]

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

C. Alix-Panabières and K. Pantel, “Challenges in circulating tumour cell research,” Nat. Rev. Cancer 14(9), 623–631 (2014).
[Crossref] [PubMed]

N. Aceto, A. Bardia, D. T. Miyamoto, M. C. Donaldson, B. S. Wittner, J. A. Spencer, M. Yu, A. Pely, A. Engstrom, H. Zhu, B. W. Brannigan, R. Kapur, S. L. Stott, T. Shioda, S. Ramaswamy, D. T. Ting, C. P. Lin, M. Toner, D. A. Haber, and S. Maheswaran, “Circulating tumor cell clusters are oligoclonal precursors of breast cancer metastasis,” Cell 158(5), 1110–1122 (2014).
[Crossref] [PubMed]

A. C. S. Chan, T. T. W. Wong, K. K. Y. Wong, E. Y. Lam, and K. K. Tsia, “Speed-dependent resolution analysis of ultrafast laser-scanning fluorescence microscopy,” J. Opt. Soc. Am. B 31(4), 755–764 (2014).
[Crossref]

2013 (3)

X. Yao, M. Labelle, C. R. Lamb, J. M. Dugan, C. A. Williamson, D. R. Spencer, K. R. Christ, R. O. Keating, W. D. Lee, G. A. Paradis, S. Begum, R. O. Hynes, and K. D. Wittrup, “Determination of 35 cell surface antigen levels in malignant pleural effusions identifies CD24 as a marker of disseminated tumor cells,” Int. J. Cancer 133(12), 2925–2933 (2013).
[PubMed]

S. Abrahamsson, J. Chen, B. Hajj, S. Stallinga, A. Y. Katsov, J. Wisniewski, G. Mizuguchi, P. Soule, F. Mueller, C. Dugast Darzacq, X. Darzacq, C. Wu, C. I. Bargmann, D. A. Agard, M. Dahan, and M. G. Gustafsson, “Fast multicolor 3D imaging using aberration-corrected multifocus microscopy,” Nat. Methods 10(1), 60–63 (2013).
[Crossref] [PubMed]

E. D. Diebold, B. W. Buckley, D. R. Gossett, and B. Jalali, “Digitally synthesized beat frequency multiplexing for sub-millisecond fluorescence microscopy,” Nat. Photonics 7(10), 806–810 (2013).
[Crossref]

2011 (2)

M. Baker, “Faster frames, clearer pictures,” Nat. Methods 8(12), 1005–1009 (2011).
[Crossref]

A. Cheng, J. T. Gonçalves, P. Golshani, K. Arisaka, and C. Portera-Cailliau, “Simultaneous two-photon calcium imaging at different depths with spatiotemporal multiplexing,” Nat. Methods 8(2), 139–142 (2011).
[Crossref] [PubMed]

2010 (3)

2009 (2)

S. W. Hell, “Microscopy and its focal switch,” Nat. Methods 6(1), 24–32 (2009).
[Crossref] [PubMed]

B. Huang, M. Bates, and X. Zhuang, “Super-resolution fluorescence microscopy,” Annu. Rev. Biochem. 78(1), 993–1016 (2009).
[Crossref] [PubMed]

2008 (1)

K. Pantel, R. H. Brakenhoff, and B. Brandt, “Detection, clinical relevance and specific biological properties of disseminating tumour cells,” Nat. Rev. Cancer 8(5), 329–340 (2008).
[Crossref] [PubMed]

2007 (5)

D. A. Basiji, W. E. Ortyn, L. Liang, V. Venkatachalam, and P. Morrissey, “Cellular image analysis and imaging by flow cytometry,” Clin. Lab. Med. 27(3), 653–670 (2007).
[Crossref] [PubMed]

J. J. Unternaehrer, A. Chow, M. Pypaert, K. Inaba, and I. Mellman, “The tetraspanin CD9 mediates lateral association of MHC class II molecules on the dendritic cell surface,” Proc. Natl. Acad. Sci. U.S.A. 104(1), 234–239 (2007).
[Crossref] [PubMed]

D. Di Carlo, D. Irimia, R. G. Tompkins, and M. Toner, “Continuous inertial focusing, ordering, and separation of particles in microchannels,” Proc. Natl. Acad. Sci. U.S.A. 104(48), 18892–18897 (2007).
[Crossref] [PubMed]

D. Li, S. Zeng, X. Lv, J. Liu, R. Du, R. Jiang, W. R. Chen, and Q. Luo, “Dispersion characteristics of acousto-optic deflector for scanning Gaussian laser beam of femtosecond pulses,” Opt. Express 15(8), 4726–4734 (2007).
[Crossref] [PubMed]

M. Trzpis, P. M. McLaughlin, L. M. de Leij, and M. C. Harmsen, “Epithelial cell adhesion molecule: more than a carcinoma marker and adhesion molecule,” Am. J. Pathol. 171(2), 386–395 (2007).
[Crossref] [PubMed]

2006 (1)

F. Wu, X. Zhang, J. Y. Cheung, K. Shi, Z. Liu, C. Luo, S. Yin, and P. Ruffin, “Frequency division multiplexed multichannel high-speed fluorescence confocal microscope,” Biophys. J. 91(6), 2290–2296 (2006).
[Crossref] [PubMed]

2003 (1)

A. L. Kindzelskii and H. R. Petty, “Intracellular calcium waves accompany neutrophil polarization, formylmethionylleucylphenylalanine stimulation, and phagocytosis: a high speed microscopy study,” J. Immunol. 170(1), 64–72 (2003).
[Crossref] [PubMed]

1951 (1)

J. A. Curcio and C. C. Petty, “The near infrared absorption spectrum of liquid water,” J. Opt. Soc. Am. A 41(5), 302–304 (1951).
[Crossref]

Abrahamsson, S.

S. Abrahamsson, J. Chen, B. Hajj, S. Stallinga, A. Y. Katsov, J. Wisniewski, G. Mizuguchi, P. Soule, F. Mueller, C. Dugast Darzacq, X. Darzacq, C. Wu, C. I. Bargmann, D. A. Agard, M. Dahan, and M. G. Gustafsson, “Fast multicolor 3D imaging using aberration-corrected multifocus microscopy,” Nat. Methods 10(1), 60–63 (2013).
[Crossref] [PubMed]

Aceto, N.

N. Aceto, A. Bardia, D. T. Miyamoto, M. C. Donaldson, B. S. Wittner, J. A. Spencer, M. Yu, A. Pely, A. Engstrom, H. Zhu, B. W. Brannigan, R. Kapur, S. L. Stott, T. Shioda, S. Ramaswamy, D. T. Ting, C. P. Lin, M. Toner, D. A. Haber, and S. Maheswaran, “Circulating tumor cell clusters are oligoclonal precursors of breast cancer metastasis,” Cell 158(5), 1110–1122 (2014).
[Crossref] [PubMed]

Agard, D. A.

S. Abrahamsson, J. Chen, B. Hajj, S. Stallinga, A. Y. Katsov, J. Wisniewski, G. Mizuguchi, P. Soule, F. Mueller, C. Dugast Darzacq, X. Darzacq, C. Wu, C. I. Bargmann, D. A. Agard, M. Dahan, and M. G. Gustafsson, “Fast multicolor 3D imaging using aberration-corrected multifocus microscopy,” Nat. Methods 10(1), 60–63 (2013).
[Crossref] [PubMed]

Alix-Panabières, C.

C. Alix-Panabières and K. Pantel, “Challenges in circulating tumour cell research,” Nat. Rev. Cancer 14(9), 623–631 (2014).
[Crossref] [PubMed]

Arisaka, K.

A. Cheng, J. T. Gonçalves, P. Golshani, K. Arisaka, and C. Portera-Cailliau, “Simultaneous two-photon calcium imaging at different depths with spatiotemporal multiplexing,” Nat. Methods 8(2), 139–142 (2011).
[Crossref] [PubMed]

Baker, M.

M. Baker, “Faster frames, clearer pictures,” Nat. Methods 8(12), 1005–1009 (2011).
[Crossref]

Bardia, A.

N. Aceto, A. Bardia, D. T. Miyamoto, M. C. Donaldson, B. S. Wittner, J. A. Spencer, M. Yu, A. Pely, A. Engstrom, H. Zhu, B. W. Brannigan, R. Kapur, S. L. Stott, T. Shioda, S. Ramaswamy, D. T. Ting, C. P. Lin, M. Toner, D. A. Haber, and S. Maheswaran, “Circulating tumor cell clusters are oligoclonal precursors of breast cancer metastasis,” Cell 158(5), 1110–1122 (2014).
[Crossref] [PubMed]

Bargmann, C. I.

S. Abrahamsson, J. Chen, B. Hajj, S. Stallinga, A. Y. Katsov, J. Wisniewski, G. Mizuguchi, P. Soule, F. Mueller, C. Dugast Darzacq, X. Darzacq, C. Wu, C. I. Bargmann, D. A. Agard, M. Dahan, and M. G. Gustafsson, “Fast multicolor 3D imaging using aberration-corrected multifocus microscopy,” Nat. Methods 10(1), 60–63 (2013).
[Crossref] [PubMed]

Basiji, D. A.

D. A. Basiji, W. E. Ortyn, L. Liang, V. Venkatachalam, and P. Morrissey, “Cellular image analysis and imaging by flow cytometry,” Clin. Lab. Med. 27(3), 653–670 (2007).
[Crossref] [PubMed]

Bates, M.

B. Huang, M. Bates, and X. Zhuang, “Super-resolution fluorescence microscopy,” Annu. Rev. Biochem. 78(1), 993–1016 (2009).
[Crossref] [PubMed]

Bechtold, P.

G. R. B. E. Römera and P. Bechtold, “Electro-optic and acousto-optic laser beam scanners,” Phys. Procedia 56, 29–39 (2014).
[Crossref]

Begum, S.

X. Yao, M. Labelle, C. R. Lamb, J. M. Dugan, C. A. Williamson, D. R. Spencer, K. R. Christ, R. O. Keating, W. D. Lee, G. A. Paradis, S. Begum, R. O. Hynes, and K. D. Wittrup, “Determination of 35 cell surface antigen levels in malignant pleural effusions identifies CD24 as a marker of disseminated tumor cells,” Int. J. Cancer 133(12), 2925–2933 (2013).
[PubMed]

Betzig, E.

E. Betzig, “Single molecules, cells, and super-resolution optics (Nobel lecture),” Angew. Chem. Int. Ed. Engl. 54(28), 8034–8053 (2015).
[Crossref] [PubMed]

Boudoux, C.

Brakenhoff, R. H.

K. Pantel, R. H. Brakenhoff, and B. Brandt, “Detection, clinical relevance and specific biological properties of disseminating tumour cells,” Nat. Rev. Cancer 8(5), 329–340 (2008).
[Crossref] [PubMed]

Brandt, B.

K. Pantel, R. H. Brakenhoff, and B. Brandt, “Detection, clinical relevance and specific biological properties of disseminating tumour cells,” Nat. Rev. Cancer 8(5), 329–340 (2008).
[Crossref] [PubMed]

Brannigan, B. W.

N. Aceto, A. Bardia, D. T. Miyamoto, M. C. Donaldson, B. S. Wittner, J. A. Spencer, M. Yu, A. Pely, A. Engstrom, H. Zhu, B. W. Brannigan, R. Kapur, S. L. Stott, T. Shioda, S. Ramaswamy, D. T. Ting, C. P. Lin, M. Toner, D. A. Haber, and S. Maheswaran, “Circulating tumor cell clusters are oligoclonal precursors of breast cancer metastasis,” Cell 158(5), 1110–1122 (2014).
[Crossref] [PubMed]

Bub, G.

G. Bub, M. Tecza, M. Helmes, P. Lee, and P. Kohl, “Temporal pixel multiplexing for simultaneous high-speed, high-resolution imaging,” Nat. Methods 7(3), 209–211 (2010).
[Crossref] [PubMed]

Buckley, B. W.

E. D. Diebold, B. W. Buckley, D. R. Gossett, and B. Jalali, “Digitally synthesized beat frequency multiplexing for sub-millisecond fluorescence microscopy,” Nat. Photonics 7(10), 806–810 (2013).
[Crossref]

Chan, A. C. S.

J. L. Wu, Y. Q. Xu, J. J. Xu, X. X. Wei, A. C. S. Chan, A. H. L. Tang, A. K. S. Lau, B. M. F. Chung, H. Cheung Shum, E. Y. Lam, K. K. Y. Wong, and K. K. Tsia, “Ultrafast laser-scanning time-stretch imaging at visible wavelengths,” Light Sci. Appl. 6(1), e16196 (2016).
[Crossref]

A. C. S. Chan, T. T. W. Wong, K. K. Y. Wong, E. Y. Lam, and K. K. Tsia, “Speed-dependent resolution analysis of ultrafast laser-scanning fluorescence microscopy,” J. Opt. Soc. Am. B 31(4), 755–764 (2014).
[Crossref]

Chen, J.

S. Abrahamsson, J. Chen, B. Hajj, S. Stallinga, A. Y. Katsov, J. Wisniewski, G. Mizuguchi, P. Soule, F. Mueller, C. Dugast Darzacq, X. Darzacq, C. Wu, C. I. Bargmann, D. A. Agard, M. Dahan, and M. G. Gustafsson, “Fast multicolor 3D imaging using aberration-corrected multifocus microscopy,” Nat. Methods 10(1), 60–63 (2013).
[Crossref] [PubMed]

Chen, W. R.

Cheng, A.

A. Cheng, J. T. Gonçalves, P. Golshani, K. Arisaka, and C. Portera-Cailliau, “Simultaneous two-photon calcium imaging at different depths with spatiotemporal multiplexing,” Nat. Methods 8(2), 139–142 (2011).
[Crossref] [PubMed]

Cheung, J. Y.

F. Wu, X. Zhang, J. Y. Cheung, K. Shi, Z. Liu, C. Luo, S. Yin, and P. Ruffin, “Frequency division multiplexed multichannel high-speed fluorescence confocal microscope,” Biophys. J. 91(6), 2290–2296 (2006).
[Crossref] [PubMed]

Cheung Shum, H.

J. L. Wu, Y. Q. Xu, J. J. Xu, X. X. Wei, A. C. S. Chan, A. H. L. Tang, A. K. S. Lau, B. M. F. Chung, H. Cheung Shum, E. Y. Lam, K. K. Y. Wong, and K. K. Tsia, “Ultrafast laser-scanning time-stretch imaging at visible wavelengths,” Light Sci. Appl. 6(1), e16196 (2016).
[Crossref]

Chojnacki, J.

J. Schneider, J. Zahn, M. Maglione, S. J. Sigrist, J. Marquard, J. Chojnacki, H. G. Kräusslich, S. J. Sahl, J. Engelhardt, and S. W. Hell, “Ultrafast, temporally stochastic STED nanoscopy of millisecond dynamics,” Nat. Methods 12(9), 827–830 (2015).
[Crossref] [PubMed]

Chow, A.

J. J. Unternaehrer, A. Chow, M. Pypaert, K. Inaba, and I. Mellman, “The tetraspanin CD9 mediates lateral association of MHC class II molecules on the dendritic cell surface,” Proc. Natl. Acad. Sci. U.S.A. 104(1), 234–239 (2007).
[Crossref] [PubMed]

Christ, K. R.

X. Yao, M. Labelle, C. R. Lamb, J. M. Dugan, C. A. Williamson, D. R. Spencer, K. R. Christ, R. O. Keating, W. D. Lee, G. A. Paradis, S. Begum, R. O. Hynes, and K. D. Wittrup, “Determination of 35 cell surface antigen levels in malignant pleural effusions identifies CD24 as a marker of disseminated tumor cells,” Int. J. Cancer 133(12), 2925–2933 (2013).
[PubMed]

Chung, B. M. F.

J. L. Wu, Y. Q. Xu, J. J. Xu, X. X. Wei, A. C. S. Chan, A. H. L. Tang, A. K. S. Lau, B. M. F. Chung, H. Cheung Shum, E. Y. Lam, K. K. Y. Wong, and K. K. Tsia, “Ultrafast laser-scanning time-stretch imaging at visible wavelengths,” Light Sci. Appl. 6(1), e16196 (2016).
[Crossref]

Curcio, J. A.

J. A. Curcio and C. C. Petty, “The near infrared absorption spectrum of liquid water,” J. Opt. Soc. Am. A 41(5), 302–304 (1951).
[Crossref]

Dahan, M.

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M. Trzpis, P. M. McLaughlin, L. M. de Leij, and M. C. Harmsen, “Epithelial cell adhesion molecule: more than a carcinoma marker and adhesion molecule,” Am. J. Pathol. 171(2), 386–395 (2007).
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E. D. Diebold, B. W. Buckley, D. R. Gossett, and B. Jalali, “Digitally synthesized beat frequency multiplexing for sub-millisecond fluorescence microscopy,” Nat. Photonics 7(10), 806–810 (2013).
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N. Aceto, A. Bardia, D. T. Miyamoto, M. C. Donaldson, B. S. Wittner, J. A. Spencer, M. Yu, A. Pely, A. Engstrom, H. Zhu, B. W. Brannigan, R. Kapur, S. L. Stott, T. Shioda, S. Ramaswamy, D. T. Ting, C. P. Lin, M. Toner, D. A. Haber, and S. Maheswaran, “Circulating tumor cell clusters are oligoclonal precursors of breast cancer metastasis,” Cell 158(5), 1110–1122 (2014).
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S. Abrahamsson, J. Chen, B. Hajj, S. Stallinga, A. Y. Katsov, J. Wisniewski, G. Mizuguchi, P. Soule, F. Mueller, C. Dugast Darzacq, X. Darzacq, C. Wu, C. I. Bargmann, D. A. Agard, M. Dahan, and M. G. Gustafsson, “Fast multicolor 3D imaging using aberration-corrected multifocus microscopy,” Nat. Methods 10(1), 60–63 (2013).
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A. Cheng, J. T. Gonçalves, P. Golshani, K. Arisaka, and C. Portera-Cailliau, “Simultaneous two-photon calcium imaging at different depths with spatiotemporal multiplexing,” Nat. Methods 8(2), 139–142 (2011).
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E. D. Diebold, B. W. Buckley, D. R. Gossett, and B. Jalali, “Digitally synthesized beat frequency multiplexing for sub-millisecond fluorescence microscopy,” Nat. Photonics 7(10), 806–810 (2013).
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S. Abrahamsson, J. Chen, B. Hajj, S. Stallinga, A. Y. Katsov, J. Wisniewski, G. Mizuguchi, P. Soule, F. Mueller, C. Dugast Darzacq, X. Darzacq, C. Wu, C. I. Bargmann, D. A. Agard, M. Dahan, and M. G. Gustafsson, “Fast multicolor 3D imaging using aberration-corrected multifocus microscopy,” Nat. Methods 10(1), 60–63 (2013).
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N. Aceto, A. Bardia, D. T. Miyamoto, M. C. Donaldson, B. S. Wittner, J. A. Spencer, M. Yu, A. Pely, A. Engstrom, H. Zhu, B. W. Brannigan, R. Kapur, S. L. Stott, T. Shioda, S. Ramaswamy, D. T. Ting, C. P. Lin, M. Toner, D. A. Haber, and S. Maheswaran, “Circulating tumor cell clusters are oligoclonal precursors of breast cancer metastasis,” Cell 158(5), 1110–1122 (2014).
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M. Trzpis, P. M. McLaughlin, L. M. de Leij, and M. C. Harmsen, “Epithelial cell adhesion molecule: more than a carcinoma marker and adhesion molecule,” Am. J. Pathol. 171(2), 386–395 (2007).
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D. Di Carlo, D. Irimia, R. G. Tompkins, and M. Toner, “Continuous inertial focusing, ordering, and separation of particles in microchannels,” Proc. Natl. Acad. Sci. U.S.A. 104(48), 18892–18897 (2007).
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E. D. Diebold, B. W. Buckley, D. R. Gossett, and B. Jalali, “Digitally synthesized beat frequency multiplexing for sub-millisecond fluorescence microscopy,” Nat. Photonics 7(10), 806–810 (2013).
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A. K. S. Lau, H. C. Shum, K. K. Y. Wong, and K. K. Tsia, “Optofluidic time-stretch imaging - an emerging tool for high-throughput imaging flow cytometry,” Lab Chip 16(10), 1743–1756 (2016).
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G. Bub, M. Tecza, M. Helmes, P. Lee, and P. Kohl, “Temporal pixel multiplexing for simultaneous high-speed, high-resolution imaging,” Nat. Methods 7(3), 209–211 (2010).
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X. Yao, M. Labelle, C. R. Lamb, J. M. Dugan, C. A. Williamson, D. R. Spencer, K. R. Christ, R. O. Keating, W. D. Lee, G. A. Paradis, S. Begum, R. O. Hynes, and K. D. Wittrup, “Determination of 35 cell surface antigen levels in malignant pleural effusions identifies CD24 as a marker of disseminated tumor cells,” Int. J. Cancer 133(12), 2925–2933 (2013).
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N. Aceto, A. Bardia, D. T. Miyamoto, M. C. Donaldson, B. S. Wittner, J. A. Spencer, M. Yu, A. Pely, A. Engstrom, H. Zhu, B. W. Brannigan, R. Kapur, S. L. Stott, T. Shioda, S. Ramaswamy, D. T. Ting, C. P. Lin, M. Toner, D. A. Haber, and S. Maheswaran, “Circulating tumor cell clusters are oligoclonal precursors of breast cancer metastasis,” Cell 158(5), 1110–1122 (2014).
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F. Wu, X. Zhang, J. Y. Cheung, K. Shi, Z. Liu, C. Luo, S. Yin, and P. Ruffin, “Frequency division multiplexed multichannel high-speed fluorescence confocal microscope,” Biophys. J. 91(6), 2290–2296 (2006).
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Morneau, D.

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N. Aceto, A. Bardia, D. T. Miyamoto, M. C. Donaldson, B. S. Wittner, J. A. Spencer, M. Yu, A. Pely, A. Engstrom, H. Zhu, B. W. Brannigan, R. Kapur, S. L. Stott, T. Shioda, S. Ramaswamy, D. T. Ting, C. P. Lin, M. Toner, D. A. Haber, and S. Maheswaran, “Circulating tumor cell clusters are oligoclonal precursors of breast cancer metastasis,” Cell 158(5), 1110–1122 (2014).
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A. Cheng, J. T. Gonçalves, P. Golshani, K. Arisaka, and C. Portera-Cailliau, “Simultaneous two-photon calcium imaging at different depths with spatiotemporal multiplexing,” Nat. Methods 8(2), 139–142 (2011).
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J. J. Unternaehrer, A. Chow, M. Pypaert, K. Inaba, and I. Mellman, “The tetraspanin CD9 mediates lateral association of MHC class II molecules on the dendritic cell surface,” Proc. Natl. Acad. Sci. U.S.A. 104(1), 234–239 (2007).
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J. Schneider, J. Zahn, M. Maglione, S. J. Sigrist, J. Marquard, J. Chojnacki, H. G. Kräusslich, S. J. Sahl, J. Engelhardt, and S. W. Hell, “Ultrafast, temporally stochastic STED nanoscopy of millisecond dynamics,” Nat. Methods 12(9), 827–830 (2015).
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[Crossref] [PubMed]

Soule, P.

S. Abrahamsson, J. Chen, B. Hajj, S. Stallinga, A. Y. Katsov, J. Wisniewski, G. Mizuguchi, P. Soule, F. Mueller, C. Dugast Darzacq, X. Darzacq, C. Wu, C. I. Bargmann, D. A. Agard, M. Dahan, and M. G. Gustafsson, “Fast multicolor 3D imaging using aberration-corrected multifocus microscopy,” Nat. Methods 10(1), 60–63 (2013).
[Crossref] [PubMed]

Spencer, D. R.

X. Yao, M. Labelle, C. R. Lamb, J. M. Dugan, C. A. Williamson, D. R. Spencer, K. R. Christ, R. O. Keating, W. D. Lee, G. A. Paradis, S. Begum, R. O. Hynes, and K. D. Wittrup, “Determination of 35 cell surface antigen levels in malignant pleural effusions identifies CD24 as a marker of disseminated tumor cells,” Int. J. Cancer 133(12), 2925–2933 (2013).
[PubMed]

Spencer, J. A.

N. Aceto, A. Bardia, D. T. Miyamoto, M. C. Donaldson, B. S. Wittner, J. A. Spencer, M. Yu, A. Pely, A. Engstrom, H. Zhu, B. W. Brannigan, R. Kapur, S. L. Stott, T. Shioda, S. Ramaswamy, D. T. Ting, C. P. Lin, M. Toner, D. A. Haber, and S. Maheswaran, “Circulating tumor cell clusters are oligoclonal precursors of breast cancer metastasis,” Cell 158(5), 1110–1122 (2014).
[Crossref] [PubMed]

Stallinga, S.

S. Abrahamsson, J. Chen, B. Hajj, S. Stallinga, A. Y. Katsov, J. Wisniewski, G. Mizuguchi, P. Soule, F. Mueller, C. Dugast Darzacq, X. Darzacq, C. Wu, C. I. Bargmann, D. A. Agard, M. Dahan, and M. G. Gustafsson, “Fast multicolor 3D imaging using aberration-corrected multifocus microscopy,” Nat. Methods 10(1), 60–63 (2013).
[Crossref] [PubMed]

Stott, S. L.

N. Aceto, A. Bardia, D. T. Miyamoto, M. C. Donaldson, B. S. Wittner, J. A. Spencer, M. Yu, A. Pely, A. Engstrom, H. Zhu, B. W. Brannigan, R. Kapur, S. L. Stott, T. Shioda, S. Ramaswamy, D. T. Ting, C. P. Lin, M. Toner, D. A. Haber, and S. Maheswaran, “Circulating tumor cell clusters are oligoclonal precursors of breast cancer metastasis,” Cell 158(5), 1110–1122 (2014).
[Crossref] [PubMed]

Strupler, M.

Tang, A. H. L.

J. L. Wu, Y. Q. Xu, J. J. Xu, X. X. Wei, A. C. S. Chan, A. H. L. Tang, A. K. S. Lau, B. M. F. Chung, H. Cheung Shum, E. Y. Lam, K. K. Y. Wong, and K. K. Tsia, “Ultrafast laser-scanning time-stretch imaging at visible wavelengths,” Light Sci. Appl. 6(1), e16196 (2016).
[Crossref]

Tecza, M.

G. Bub, M. Tecza, M. Helmes, P. Lee, and P. Kohl, “Temporal pixel multiplexing for simultaneous high-speed, high-resolution imaging,” Nat. Methods 7(3), 209–211 (2010).
[Crossref] [PubMed]

Ting, D. T.

N. Aceto, A. Bardia, D. T. Miyamoto, M. C. Donaldson, B. S. Wittner, J. A. Spencer, M. Yu, A. Pely, A. Engstrom, H. Zhu, B. W. Brannigan, R. Kapur, S. L. Stott, T. Shioda, S. Ramaswamy, D. T. Ting, C. P. Lin, M. Toner, D. A. Haber, and S. Maheswaran, “Circulating tumor cell clusters are oligoclonal precursors of breast cancer metastasis,” Cell 158(5), 1110–1122 (2014).
[Crossref] [PubMed]

Tompkins, R. G.

D. Di Carlo, D. Irimia, R. G. Tompkins, and M. Toner, “Continuous inertial focusing, ordering, and separation of particles in microchannels,” Proc. Natl. Acad. Sci. U.S.A. 104(48), 18892–18897 (2007).
[Crossref] [PubMed]

Toner, M.

N. Aceto, A. Bardia, D. T. Miyamoto, M. C. Donaldson, B. S. Wittner, J. A. Spencer, M. Yu, A. Pely, A. Engstrom, H. Zhu, B. W. Brannigan, R. Kapur, S. L. Stott, T. Shioda, S. Ramaswamy, D. T. Ting, C. P. Lin, M. Toner, D. A. Haber, and S. Maheswaran, “Circulating tumor cell clusters are oligoclonal precursors of breast cancer metastasis,” Cell 158(5), 1110–1122 (2014).
[Crossref] [PubMed]

D. Di Carlo, D. Irimia, R. G. Tompkins, and M. Toner, “Continuous inertial focusing, ordering, and separation of particles in microchannels,” Proc. Natl. Acad. Sci. U.S.A. 104(48), 18892–18897 (2007).
[Crossref] [PubMed]

Trzpis, M.

M. Trzpis, P. M. McLaughlin, L. M. de Leij, and M. C. Harmsen, “Epithelial cell adhesion molecule: more than a carcinoma marker and adhesion molecule,” Am. J. Pathol. 171(2), 386–395 (2007).
[Crossref] [PubMed]

Tsia, K. K.

A. K. S. Lau, H. C. Shum, K. K. Y. Wong, and K. K. Tsia, “Optofluidic time-stretch imaging - an emerging tool for high-throughput imaging flow cytometry,” Lab Chip 16(10), 1743–1756 (2016).
[Crossref] [PubMed]

J. L. Wu, Y. Q. Xu, J. J. Xu, X. X. Wei, A. C. S. Chan, A. H. L. Tang, A. K. S. Lau, B. M. F. Chung, H. Cheung Shum, E. Y. Lam, K. K. Y. Wong, and K. K. Tsia, “Ultrafast laser-scanning time-stretch imaging at visible wavelengths,” Light Sci. Appl. 6(1), e16196 (2016).
[Crossref]

A. C. S. Chan, T. T. W. Wong, K. K. Y. Wong, E. Y. Lam, and K. K. Tsia, “Speed-dependent resolution analysis of ultrafast laser-scanning fluorescence microscopy,” J. Opt. Soc. Am. B 31(4), 755–764 (2014).
[Crossref]

Unternaehrer, J. J.

J. J. Unternaehrer, A. Chow, M. Pypaert, K. Inaba, and I. Mellman, “The tetraspanin CD9 mediates lateral association of MHC class II molecules on the dendritic cell surface,” Proc. Natl. Acad. Sci. U.S.A. 104(1), 234–239 (2007).
[Crossref] [PubMed]

Venkatachalam, V.

D. A. Basiji, W. E. Ortyn, L. Liang, V. Venkatachalam, and P. Morrissey, “Cellular image analysis and imaging by flow cytometry,” Clin. Lab. Med. 27(3), 653–670 (2007).
[Crossref] [PubMed]

Wei, X. X.

J. L. Wu, Y. Q. Xu, J. J. Xu, X. X. Wei, A. C. S. Chan, A. H. L. Tang, A. K. S. Lau, B. M. F. Chung, H. Cheung Shum, E. Y. Lam, K. K. Y. Wong, and K. K. Tsia, “Ultrafast laser-scanning time-stretch imaging at visible wavelengths,” Light Sci. Appl. 6(1), e16196 (2016).
[Crossref]

Williamson, C. A.

X. Yao, M. Labelle, C. R. Lamb, J. M. Dugan, C. A. Williamson, D. R. Spencer, K. R. Christ, R. O. Keating, W. D. Lee, G. A. Paradis, S. Begum, R. O. Hynes, and K. D. Wittrup, “Determination of 35 cell surface antigen levels in malignant pleural effusions identifies CD24 as a marker of disseminated tumor cells,” Int. J. Cancer 133(12), 2925–2933 (2013).
[PubMed]

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

Wisniewski, J.

S. Abrahamsson, J. Chen, B. Hajj, S. Stallinga, A. Y. Katsov, J. Wisniewski, G. Mizuguchi, P. Soule, F. Mueller, C. Dugast Darzacq, X. Darzacq, C. Wu, C. I. Bargmann, D. A. Agard, M. Dahan, and M. G. Gustafsson, “Fast multicolor 3D imaging using aberration-corrected multifocus microscopy,” Nat. Methods 10(1), 60–63 (2013).
[Crossref] [PubMed]

Wittner, B. S.

N. Aceto, A. Bardia, D. T. Miyamoto, M. C. Donaldson, B. S. Wittner, J. A. Spencer, M. Yu, A. Pely, A. Engstrom, H. Zhu, B. W. Brannigan, R. Kapur, S. L. Stott, T. Shioda, S. Ramaswamy, D. T. Ting, C. P. Lin, M. Toner, D. A. Haber, and S. Maheswaran, “Circulating tumor cell clusters are oligoclonal precursors of breast cancer metastasis,” Cell 158(5), 1110–1122 (2014).
[Crossref] [PubMed]

Wittrup, K. D.

X. Yao, M. Labelle, C. R. Lamb, J. M. Dugan, C. A. Williamson, D. R. Spencer, K. R. Christ, R. O. Keating, W. D. Lee, G. A. Paradis, S. Begum, R. O. Hynes, and K. D. Wittrup, “Determination of 35 cell surface antigen levels in malignant pleural effusions identifies CD24 as a marker of disseminated tumor cells,” Int. J. Cancer 133(12), 2925–2933 (2013).
[PubMed]

Wong, K. K. Y.

A. K. S. Lau, H. C. Shum, K. K. Y. Wong, and K. K. Tsia, “Optofluidic time-stretch imaging - an emerging tool for high-throughput imaging flow cytometry,” Lab Chip 16(10), 1743–1756 (2016).
[Crossref] [PubMed]

J. L. Wu, Y. Q. Xu, J. J. Xu, X. X. Wei, A. C. S. Chan, A. H. L. Tang, A. K. S. Lau, B. M. F. Chung, H. Cheung Shum, E. Y. Lam, K. K. Y. Wong, and K. K. Tsia, “Ultrafast laser-scanning time-stretch imaging at visible wavelengths,” Light Sci. Appl. 6(1), e16196 (2016).
[Crossref]

A. C. S. Chan, T. T. W. Wong, K. K. Y. Wong, E. Y. Lam, and K. K. Tsia, “Speed-dependent resolution analysis of ultrafast laser-scanning fluorescence microscopy,” J. Opt. Soc. Am. B 31(4), 755–764 (2014).
[Crossref]

Wong, T. T. W.

Wu, C.

S. Abrahamsson, J. Chen, B. Hajj, S. Stallinga, A. Y. Katsov, J. Wisniewski, G. Mizuguchi, P. Soule, F. Mueller, C. Dugast Darzacq, X. Darzacq, C. Wu, C. I. Bargmann, D. A. Agard, M. Dahan, and M. G. Gustafsson, “Fast multicolor 3D imaging using aberration-corrected multifocus microscopy,” Nat. Methods 10(1), 60–63 (2013).
[Crossref] [PubMed]

Wu, F.

F. Wu, X. Zhang, J. Y. Cheung, K. Shi, Z. Liu, C. Luo, S. Yin, and P. Ruffin, “Frequency division multiplexed multichannel high-speed fluorescence confocal microscope,” Biophys. J. 91(6), 2290–2296 (2006).
[Crossref] [PubMed]

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J. L. Wu, Y. Q. Xu, J. J. Xu, X. X. Wei, A. C. S. Chan, A. H. L. Tang, A. K. S. Lau, B. M. F. Chung, H. Cheung Shum, E. Y. Lam, K. K. Y. Wong, and K. K. Tsia, “Ultrafast laser-scanning time-stretch imaging at visible wavelengths,” Light Sci. Appl. 6(1), e16196 (2016).
[Crossref]

Xu, J. J.

J. L. Wu, Y. Q. Xu, J. J. Xu, X. X. Wei, A. C. S. Chan, A. H. L. Tang, A. K. S. Lau, B. M. F. Chung, H. Cheung Shum, E. Y. Lam, K. K. Y. Wong, and K. K. Tsia, “Ultrafast laser-scanning time-stretch imaging at visible wavelengths,” Light Sci. Appl. 6(1), e16196 (2016).
[Crossref]

Xu, Y. Q.

J. L. Wu, Y. Q. Xu, J. J. Xu, X. X. Wei, A. C. S. Chan, A. H. L. Tang, A. K. S. Lau, B. M. F. Chung, H. Cheung Shum, E. Y. Lam, K. K. Y. Wong, and K. K. Tsia, “Ultrafast laser-scanning time-stretch imaging at visible wavelengths,” Light Sci. Appl. 6(1), e16196 (2016).
[Crossref]

Yao, X.

X. Yao, M. Labelle, C. R. Lamb, J. M. Dugan, C. A. Williamson, D. R. Spencer, K. R. Christ, R. O. Keating, W. D. Lee, G. A. Paradis, S. Begum, R. O. Hynes, and K. D. Wittrup, “Determination of 35 cell surface antigen levels in malignant pleural effusions identifies CD24 as a marker of disseminated tumor cells,” Int. J. Cancer 133(12), 2925–2933 (2013).
[PubMed]

Yelin, D.

Yin, S.

F. Wu, X. Zhang, J. Y. Cheung, K. Shi, Z. Liu, C. Luo, S. Yin, and P. Ruffin, “Frequency division multiplexed multichannel high-speed fluorescence confocal microscope,” Biophys. J. 91(6), 2290–2296 (2006).
[Crossref] [PubMed]

Yu, M.

N. Aceto, A. Bardia, D. T. Miyamoto, M. C. Donaldson, B. S. Wittner, J. A. Spencer, M. Yu, A. Pely, A. Engstrom, H. Zhu, B. W. Brannigan, R. Kapur, S. L. Stott, T. Shioda, S. Ramaswamy, D. T. Ting, C. P. Lin, M. Toner, D. A. Haber, and S. Maheswaran, “Circulating tumor cell clusters are oligoclonal precursors of breast cancer metastasis,” Cell 158(5), 1110–1122 (2014).
[Crossref] [PubMed]

Zahn, J.

J. Schneider, J. Zahn, M. Maglione, S. J. Sigrist, J. Marquard, J. Chojnacki, H. G. Kräusslich, S. J. Sahl, J. Engelhardt, and S. W. Hell, “Ultrafast, temporally stochastic STED nanoscopy of millisecond dynamics,” Nat. Methods 12(9), 827–830 (2015).
[Crossref] [PubMed]

Zeng, S.

Zhang, X.

F. Wu, X. Zhang, J. Y. Cheung, K. Shi, Z. Liu, C. Luo, S. Yin, and P. Ruffin, “Frequency division multiplexed multichannel high-speed fluorescence confocal microscope,” Biophys. J. 91(6), 2290–2296 (2006).
[Crossref] [PubMed]

Zhu, H.

N. Aceto, A. Bardia, D. T. Miyamoto, M. C. Donaldson, B. S. Wittner, J. A. Spencer, M. Yu, A. Pely, A. Engstrom, H. Zhu, B. W. Brannigan, R. Kapur, S. L. Stott, T. Shioda, S. Ramaswamy, D. T. Ting, C. P. Lin, M. Toner, D. A. Haber, and S. Maheswaran, “Circulating tumor cell clusters are oligoclonal precursors of breast cancer metastasis,” Cell 158(5), 1110–1122 (2014).
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B. Huang, M. Bates, and X. Zhuang, “Super-resolution fluorescence microscopy,” Annu. Rev. Biochem. 78(1), 993–1016 (2009).
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Am. J. Pathol. (1)

M. Trzpis, P. M. McLaughlin, L. M. de Leij, and M. C. Harmsen, “Epithelial cell adhesion molecule: more than a carcinoma marker and adhesion molecule,” Am. J. Pathol. 171(2), 386–395 (2007).
[Crossref] [PubMed]

Angew. Chem. Int. Ed. Engl. (1)

E. Betzig, “Single molecules, cells, and super-resolution optics (Nobel lecture),” Angew. Chem. Int. Ed. Engl. 54(28), 8034–8053 (2015).
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B. Huang, M. Bates, and X. Zhuang, “Super-resolution fluorescence microscopy,” Annu. Rev. Biochem. 78(1), 993–1016 (2009).
[Crossref] [PubMed]

Biophys. J. (1)

F. Wu, X. Zhang, J. Y. Cheung, K. Shi, Z. Liu, C. Luo, S. Yin, and P. Ruffin, “Frequency division multiplexed multichannel high-speed fluorescence confocal microscope,” Biophys. J. 91(6), 2290–2296 (2006).
[Crossref] [PubMed]

Cell (1)

N. Aceto, A. Bardia, D. T. Miyamoto, M. C. Donaldson, B. S. Wittner, J. A. Spencer, M. Yu, A. Pely, A. Engstrom, H. Zhu, B. W. Brannigan, R. Kapur, S. L. Stott, T. Shioda, S. Ramaswamy, D. T. Ting, C. P. Lin, M. Toner, D. A. Haber, and S. Maheswaran, “Circulating tumor cell clusters are oligoclonal precursors of breast cancer metastasis,” Cell 158(5), 1110–1122 (2014).
[Crossref] [PubMed]

Clin. Lab. Med. (1)

D. A. Basiji, W. E. Ortyn, L. Liang, V. Venkatachalam, and P. Morrissey, “Cellular image analysis and imaging by flow cytometry,” Clin. Lab. Med. 27(3), 653–670 (2007).
[Crossref] [PubMed]

Curr. Opin. Chem. Biol. (1)

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

Int. J. Cancer (1)

X. Yao, M. Labelle, C. R. Lamb, J. M. Dugan, C. A. Williamson, D. R. Spencer, K. R. Christ, R. O. Keating, W. D. Lee, G. A. Paradis, S. Begum, R. O. Hynes, and K. D. Wittrup, “Determination of 35 cell surface antigen levels in malignant pleural effusions identifies CD24 as a marker of disseminated tumor cells,” Int. J. Cancer 133(12), 2925–2933 (2013).
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Lab Chip (1)

A. K. S. Lau, H. C. Shum, K. K. Y. Wong, and K. K. Tsia, “Optofluidic time-stretch imaging - an emerging tool for high-throughput imaging flow cytometry,” Lab Chip 16(10), 1743–1756 (2016).
[Crossref] [PubMed]

Light Sci. Appl. (1)

J. L. Wu, Y. Q. Xu, J. J. Xu, X. X. Wei, A. C. S. Chan, A. H. L. Tang, A. K. S. Lau, B. M. F. Chung, H. Cheung Shum, E. Y. Lam, K. K. Y. Wong, and K. K. Tsia, “Ultrafast laser-scanning time-stretch imaging at visible wavelengths,” Light Sci. Appl. 6(1), e16196 (2016).
[Crossref]

Nat. Methods (6)

J. Schneider, J. Zahn, M. Maglione, S. J. Sigrist, J. Marquard, J. Chojnacki, H. G. Kräusslich, S. J. Sahl, J. Engelhardt, and S. W. Hell, “Ultrafast, temporally stochastic STED nanoscopy of millisecond dynamics,” Nat. Methods 12(9), 827–830 (2015).
[Crossref] [PubMed]

G. Bub, M. Tecza, M. Helmes, P. Lee, and P. Kohl, “Temporal pixel multiplexing for simultaneous high-speed, high-resolution imaging,” Nat. Methods 7(3), 209–211 (2010).
[Crossref] [PubMed]

S. Abrahamsson, J. Chen, B. Hajj, S. Stallinga, A. Y. Katsov, J. Wisniewski, G. Mizuguchi, P. Soule, F. Mueller, C. Dugast Darzacq, X. Darzacq, C. Wu, C. I. Bargmann, D. A. Agard, M. Dahan, and M. G. Gustafsson, “Fast multicolor 3D imaging using aberration-corrected multifocus microscopy,” Nat. Methods 10(1), 60–63 (2013).
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Nat. Photonics (1)

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Opt. Express (1)

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[Crossref] [PubMed]

D. Di Carlo, D. Irimia, R. G. Tompkins, and M. Toner, “Continuous inertial focusing, ordering, and separation of particles in microchannels,” Proc. Natl. Acad. Sci. U.S.A. 104(48), 18892–18897 (2007).
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Supplementary Material (1)

NameDescription
» Visualization 1       Dynamic imaging of single living MCF-7 cells subject to photothermal perturbations at 3000 fps

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Figures (6)

Fig. 1
Fig. 1

Schematic of the all-optical laser-scanning fluorescence microscope based on FACED. Laser repetition rate = 80 MHz; pulse width = 150 fs; center wavelength = 710 nm. Cylindrical lens, focal length = 500 mm; BF, band pass filter (FF01-769/41-25, Semrock); DM, dichroic mirror (FF740-Di01, Semrock); AOM, acoustic optical modulator; PMT, photomultiplier tube; L1-L8, lens, focal length f1 = 50 mm, f2 = 200 mm; f3 = f4 = f5 = f6 = 150 mm; f7 = 150 mm; f8 = 25 mm. α, misaligned angle, < 1 mrad; separation S = 300 mm; length D = 200 mm. The flip mirror is used to deliver the 1,440-nm laser to the focal plane to generate photothermal perturbation. Note that the PMT is replaced by a scientific CMOS camera (Zyla 5.5, Andor) for performing conventional wide-field fluorescence imaging, which is compared to FACED imaging (See Fig. 4).

Fig. 2
Fig. 2

Spatial and temporal characteristics of the all-optical laser-scanning beam at the focal plane. (a) Beam profile; average intensity, ~20 kW/cm2; scale bar is 5 μm. (b) the corresponding temporal waveform of the transmitted beam measured by the photodiode (Fig. 1). (c) Zoom-in view of the gray area in (b).

Fig. 3
Fig. 3

Imaging performance of the all-optical, ultrafast laser beam scanner. (a) SNR (at a line-scan rate of 8 MHz) measured at different fluorescent dye concentrations in solution; inset shows the SNR against the square root of the number of averaging line-scan. The lines show the linear fit to the data; error bars represent the standard deviations obtained from 18 measurements. (b) Intensity profiles of the microbead along slow and fast axis; The FWHM values represent the mean ± standard deviation obtained from 20 beads; inset shows the averaged microbead image.

Fig. 4
Fig. 4

Ultrafast dual-contrast flowing single-cell imaging by FACED microscopy. (a) Imagery of MCF-7 cells flowing at 1.5 m/s. Left and middle columns show the FACED bright-field and fluorescence images, and right column shows the overlaid images. (b) Flowing MCF-7 cells at 1.5 m/s and (c) static MCF-7 cells captured by a sCMOS camera with an exposure time of 5 ms. All scale bars are 10 μm.

Fig. 5
Fig. 5

High throughput imaging flow cytometry analysis of PBMC and MCF-7 mixtures. (a) Scatter plot of the peak SNR (PSNR) in fluorescence images against the equivalent diameter (i.e. the diameter of an equivalent circle with an area equal to the cell area); for non MCF-7 cell group, the fluorescence images show background noise. (b) Scatter plot of the cell circularity against the kurtosis of intensity distribution in the fluorescence images of the gated MCF-7 cell group. (Inset) The representative images from four regions highlighted in blue, green, orange and violet. All images have FOV of 30 μm × 30 μm. Total cell counts: ~5,500.

Fig. 6
Fig. 6

High-speed dynamic imaging of single live MCF-7 cells subject to photothermal perturbations (Visualization 1). (a) Cell size variation over time under different perturbation frequencies F. Top panel: the NIR laser is off. Other panels: the NIR laser is on from the 21st to 146th frame. Inset in top panel: images of the first and last frame with yellow curves showing the cell outlines (b) Frequency spectra of corresponding time signals in (a). Inset in top panel: galvanometric mirror scanning time sequence (O, odd frame; E, even frame) which shows the dead-time slots (~20 μs) results in the apparent 1,500 Hz scanning pattern.

Equations (2)

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M= Δθ α < θ max α = N max ,
τ 2S c ,

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