Abstract

Today’s imaging flow cytometer (IFC) systems are limited by the projection problem: collapsing three-dimensional (3D) information onto a two-dimensional (2D) image causes a lack of tomographic 3D resolution and reduced information content, limiting the reliability of spot counting or co-localization crucial to cell phenotyping. We present 3D imaging flow cytometry as a solution to the problem. Our high-throughput 3D cell imager based on optical sectioning microscopy combines orthogonal light-sheet scanning illumination with our previous spatiotemporal transformation detection to produce 3D cell image reconstruction from a cameraless single-pixel photodetector readout. We demonstrate this capability by cocapturing 3D fluorescence and label-free side-scattering images of single cells in flow with a throughput of approximately 500 cells per second.

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

Full Article  |  PDF Article
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References

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2018 (3)

C. Martin, T. Li, E. Hegarty, P. Zhao, S. Mondal, and A. Ben-Yakar, “Line excitation array detection fluorescence microscopy at 0.8 million frames per second,” Nat. Commun. 9, 4499 (2018).
[Crossref]

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[Crossref]

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[Crossref]

2017 (4)

S. Quint, A. F. Christ, A. Guckenberger, S. Himbert, L. Kaestner, S. Gekle, and C. Wagner, “3D tomography of cells in micro-channels,” Appl. Phys. Lett. 111, 103701 (2017).
[Crossref]

F. Merola, P. Memmolo, L. Miccio, R. Savoia, M. Mugnano, A. Fontana, G. D’Ippolito, A. Sardo, A. Iolascon, A. Gambale, and P. Ferraro, “Tomographic flow cytometry by digital holography,” Light Sci. Appl. 6, e16241 (2017).
[Crossref]

Q. Zhang, L. Zhong, P. Tang, Y. Yuan, S. Liu, J. Tian, and X. Lu, “Quantitative refractive index distribution of single cell by combining phase-shifting interferometry and AFM imaging,” Sci. Rep. 7, 2532 (2017).
[Crossref]

Y. Hagiwara, A. Niimi, M. Isono, M. Yamauchi, T. Yasuhara, S. Limsirichaikul, T. Oike, H. Sato, K. D. Held, T. Nakano, A. Shibata, Y. Hagiwara, A. Niimi, M. Isono, M. Yamauchi, T. Yasuhara, S. Limsirichaikul, T. Oike, H. Sato, K. D. Held, T. Nakano, A. Shibata, Y. Hagiwara, A. Niimi, M. Isono, M. Yamauchi, T. Yasuhara, S. Limsirichaikul, T. Oike, H. Sato, K. D. Held, T. Nakano, and A. Shibata, “3D-structured illumination microscopy reveals clustered DNA double-strand break formation in widespread γH2AX foci after high LET heavy-ion particle radiation,” Oncotarget 8, 109370 (2017).
[Crossref]

2016 (5)

J. R. Heath, A. Ribas, and P. S. Mischel, “Single-cell analysis tools for drug discovery and development,” Nat. Rev. Drug Discov. 15, 204–216 (2016).
[Crossref]

P. Y. Liu, L. K. Chin, W. Ser, H. F. Chen, C.-M. Hsieh, C.-H. Lee, K.-B. Sung, T. C. Ayi, P. H. Yap, B. Liedberg, K. Wang, T. Bourouina, and Y. Leprince-Wang, “Cell refractive index for cell biology and disease diagnosis: past, present and future,” Lab Chip 16, 634–644 (2016).
[Crossref]

N. Gomez-Navarro and E. Miller, “Protein sorting at the ER-Golgi interface,” J. Cell Biol. 215, 769–778 (2016).
[Crossref]

Y. Han, Y. Gu, A. C. Zhang, and Y.-H. Lo, “Review: imaging technologies for flow cytometry,” Lab Chip 16, 4639–4647 (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, 1028–1040 (2016).
[Crossref]

2015 (1)

Y. Han and Y.-H. Lo, “Imaging cells in flow cytometer using spatial-temporal transformation,” Sci. Rep. 5, 13267 (2015).
[Crossref]

2014 (1)

Y. Sung, N. Lue, B. Hamza, J. Martel, D. Irimia, R. R. Dasari, W. Choi, Z. Yaqoob, and P. So, “Three-dimensional holographic refractive-index measurement of continuously flowing cells in a microfluidic channel,” Phys. Rev. Appl. 1, 1–8 (2014).
[Crossref]

2013 (4)

P. G. Pitrone, J. Schindelin, L. Stuyvenberg, S. Preibisch, M. Weber, K. W. Eliceiri, J. Huisken, and P. Tomancak, “OpenSPIM: an open-access light-sheet microscopy platform,” Nat. Methods 10, 598–599 (2013).
[Crossref]

F. Mueller, A. Senecal, K. Tantale, H. Marie-Nelly, N. Ly, O. Collin, E. Basyuk, E. Bertrand, X. Darzacq, and C. Zimmer, “FISH-quant: automatic counting of transcripts in 3D FISH images,” Nat. Methods 10, 277–278 (2013).
[Crossref]

J. Wu, J. Li, and R. K. Y. Chan, “A light sheet based high throughput 3D-imaging flow cytometer for phytoplankton analysis,” Opt. Express 21, 14474–14480 (2013).
[Crossref]

V. Almendro, A. Marusyk, and K. Polyak, “Cellular heterogeneity and molecular evolution in cancer,” Annu. Rev. Pathol. Mech. Dis. 8, 277–302 (2013).
[Crossref]

2012 (6)

L. Pelkmans, “Using cell-to-cell variability—a new era in molecular biology,” Science 336, 425–426 (2012).
[Crossref]

A. Ivashkevich, C. E. Redon, A. J. Nakamura, R. F. Martin, and O. A. Martin, “Use of the γ-H2AX assay to monitor DNA damage and repair in translational cancer research,” Cancer Lett. 327, 123–133 (2012).
[Crossref]

W. G. Telford, T. Hawley, F. Subach, V. Verkhusha, and R. G. Hawley, “Flow cytometry of fluorescent proteins,” Methods 57, 318–330 (2012).
[Crossref]

N. S. Barteneva, E. Fasler-Kan, and I. A. Vorobjev, “Imaging flow cytometry: coping with heterogeneity in biological systems,” J. Histochem. Cytochem. 60, 723–733 (2012).
[Crossref]

K. Goda, A. Ayazi, D. R. Gossett, J. Sadasivam, C. K. Lonappan, E. Sollier, A. M. Fard, S. C. Hur, J. Adam, C. Murray, C. Wang, N. Brackbill, D. Di Carlo, and B. Jalali, “High-throughput single-microparticle imaging flow analyzer,” Proc. Natl. Acad. Sci. USA 109, 11630–11635 (2012).
[Crossref]

O. O. Dada, B. J. Huge, and N. J. Dovichi, “Simplified sheath flow cuvette design for ultrasensitive laser induced fluorescence detection in capillary electrophoresis,” Analyst 137, 3099–3101 (2012).
[Crossref]

2011 (2)

B. Snijder and L. Pelkmans, “Origins of regulated cell-to-cell variability,” Nat. Rev. Mol. Cell Biol. 12, 119–125 (2011).
[Crossref]

A. Janssen, M. van der Burg, K. Szuhai, G. J. P. L. Kops, and R. H. Medema, “Chromosome segregation errors as a cause of DNA damage and structural chromosome aberrations,” Science 333, 1895–1898 (2011).
[Crossref]

2010 (1)

S. J. Altschuler and L. F. Wu, “Cellular heterogeneity: do differences make a difference?” Cell 141, 559–563 (2010).
[Crossref]

2009 (1)

J. S. Dickey, C. E. Redon, A. J. Nakamura, B. J. Baird, O. A. Sedelnikova, and W. M. Bonner, “H2AX: functional roles and potential applications,” Chromosoma 118, 683–692 (2009).
[Crossref]

2007 (2)

J. T. Chang, V. R. Palanivel, I. Kinjyo, F. Schambach, A. M. Intlekofer, A. Banerjee, S. A. Longworth, K. E. Vinup, P. Mrass, J. Oliaro, N. Killeen, J. S. Orange, S. M. Russell, W. Weninger, and S. L. Reiner, “Asymmetric T lymphocyte division in the initiation of adaptive immune responses,” Science 315, 1687–1691 (2007).
[Crossref]

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, 653–670 (2007).
[Crossref]

2006 (2)

V. M. Olkkonen and E. Ikonen, “When intracellular logistics fails: genetic defects in membrane trafficking,” J. Cell Sci. 119, 5031–5035 (2006).
[Crossref]

J. Q. Ling, T. Li, J. F. Hu, T. H. Vu, H. L. Chen, X. W. Qiu, A. M. Cherry, and A. R. Hoffman, “CTCF mediates interchromosomal colocalization between Igf2/H19 and Wsb1/Nf1,” Science 312, 269–272 (2006).
[Crossref]

2005 (1)

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

1992 (1)

J. F. Amara, S. H. Cheng, and A. E. Smith, “Intracellular protein trafficking defects in human disease,” Trends Cell Biol. 2, 145–149 (1992).
[Crossref]

1981 (1)

O. D. Laerum and T. Farsund, “Clinical application of flow cytometry: a review,” Cytometry 2, 1–13 (1981).
[Crossref]

Adam, J.

K. Goda, A. Ayazi, D. R. Gossett, J. Sadasivam, C. K. Lonappan, E. Sollier, A. M. Fard, S. C. Hur, J. Adam, C. Murray, C. Wang, N. Brackbill, D. Di Carlo, and B. Jalali, “High-throughput single-microparticle imaging flow analyzer,” Proc. Natl. Acad. Sci. USA 109, 11630–11635 (2012).
[Crossref]

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, 1028–1040 (2016).
[Crossref]

Almendro, V.

V. Almendro, A. Marusyk, and K. Polyak, “Cellular heterogeneity and molecular evolution in cancer,” Annu. Rev. Pathol. Mech. Dis. 8, 277–302 (2013).
[Crossref]

Altschuler, S. J.

S. J. Altschuler and L. F. Wu, “Cellular heterogeneity: do differences make a difference?” Cell 141, 559–563 (2010).
[Crossref]

Amara, J. F.

J. F. Amara, S. H. Cheng, and A. E. Smith, “Intracellular protein trafficking defects in human disease,” Trends Cell Biol. 2, 145–149 (1992).
[Crossref]

Arai, F.

N. Nitta, T. Sugimura, A. Isozaki, H. Mikami, K. Hiraki, S. Sakuma, T. Iino, F. Arai, T. Endo, Y. Fujiwaki, H. Fukuzawa, M. Hase, T. Hayakawa, K. Hiramatsu, Y. Hoshino, M. Inaba, T. Ito, H. Karakawa, Y. Kasai, K. Koizumi, S. Lee, C. Lei, M. Li, T. Maeno, S. Matsusaka, D. Murakami, A. Nakagawa, Y. Oguchi, M. Oikawa, T. Ota, K. Shiba, H. Shintaku, Y. Shirasaki, K. Suga, Y. Suzuki, N. Suzuki, Y. Tanaka, H. Tezuka, C. Toyokawa, Y. Yalikun, M. Yamada, M. Yamagishi, T. Yamano, A. Yasumoto, Y. Yatomi, M. Yazawa, D. Di Carlo, Y. Hosokawa, S. Uemura, Y. Ozeki, and K. Goda, “Intelligent image-activated cell sorting,” Cell 175, 266–276 (2018).
[Crossref]

Ayazi, A.

K. Goda, A. Ayazi, D. R. Gossett, J. Sadasivam, C. K. Lonappan, E. Sollier, A. M. Fard, S. C. Hur, J. Adam, C. Murray, C. Wang, N. Brackbill, D. Di Carlo, and B. Jalali, “High-throughput single-microparticle imaging flow analyzer,” Proc. Natl. Acad. Sci. USA 109, 11630–11635 (2012).
[Crossref]

Ayi, T. C.

P. Y. Liu, L. K. Chin, W. Ser, H. F. Chen, C.-M. Hsieh, C.-H. Lee, K.-B. Sung, T. C. Ayi, P. H. Yap, B. Liedberg, K. Wang, T. Bourouina, and Y. Leprince-Wang, “Cell refractive index for cell biology and disease diagnosis: past, present and future,” Lab Chip 16, 634–644 (2016).
[Crossref]

Baird, B. J.

J. S. Dickey, C. E. Redon, A. J. Nakamura, B. J. Baird, O. A. Sedelnikova, and W. M. Bonner, “H2AX: functional roles and potential applications,” Chromosoma 118, 683–692 (2009).
[Crossref]

Banerjee, A.

J. T. Chang, V. R. Palanivel, I. Kinjyo, F. Schambach, A. M. Intlekofer, A. Banerjee, S. A. Longworth, K. E. Vinup, P. Mrass, J. Oliaro, N. Killeen, J. S. Orange, S. M. Russell, W. Weninger, and S. L. Reiner, “Asymmetric T lymphocyte division in the initiation of adaptive immune responses,” Science 315, 1687–1691 (2007).
[Crossref]

Barteneva, N. S.

N. S. Barteneva, E. Fasler-Kan, and I. A. Vorobjev, “Imaging flow cytometry: coping with heterogeneity in biological systems,” J. Histochem. Cytochem. 60, 723–733 (2012).
[Crossref]

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, 653–670 (2007).
[Crossref]

Basyuk, E.

F. Mueller, A. Senecal, K. Tantale, H. Marie-Nelly, N. Ly, O. Collin, E. Basyuk, E. Bertrand, X. Darzacq, and C. Zimmer, “FISH-quant: automatic counting of transcripts in 3D FISH images,” Nat. Methods 10, 277–278 (2013).
[Crossref]

Ben-Yakar, A.

C. Martin, T. Li, E. Hegarty, P. Zhao, S. Mondal, and A. Ben-Yakar, “Line excitation array detection fluorescence microscopy at 0.8 million frames per second,” Nat. Commun. 9, 4499 (2018).
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Bertrand, E.

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Y. Hagiwara, A. Niimi, M. Isono, M. Yamauchi, T. Yasuhara, S. Limsirichaikul, T. Oike, H. Sato, K. D. Held, T. Nakano, A. Shibata, Y. Hagiwara, A. Niimi, M. Isono, M. Yamauchi, T. Yasuhara, S. Limsirichaikul, T. Oike, H. Sato, K. D. Held, T. Nakano, A. Shibata, Y. Hagiwara, A. Niimi, M. Isono, M. Yamauchi, T. Yasuhara, S. Limsirichaikul, T. Oike, H. Sato, K. D. Held, T. Nakano, and A. Shibata, “3D-structured illumination microscopy reveals clustered DNA double-strand break formation in widespread γH2AX foci after high LET heavy-ion particle radiation,” Oncotarget 8, 109370 (2017).
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Y. Hagiwara, A. Niimi, M. Isono, M. Yamauchi, T. Yasuhara, S. Limsirichaikul, T. Oike, H. Sato, K. D. Held, T. Nakano, A. Shibata, Y. Hagiwara, A. Niimi, M. Isono, M. Yamauchi, T. Yasuhara, S. Limsirichaikul, T. Oike, H. Sato, K. D. Held, T. Nakano, A. Shibata, Y. Hagiwara, A. Niimi, M. Isono, M. Yamauchi, T. Yasuhara, S. Limsirichaikul, T. Oike, H. Sato, K. D. Held, T. Nakano, and A. Shibata, “3D-structured illumination microscopy reveals clustered DNA double-strand break formation in widespread γH2AX foci after high LET heavy-ion particle radiation,” Oncotarget 8, 109370 (2017).
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Y. Hagiwara, A. Niimi, M. Isono, M. Yamauchi, T. Yasuhara, S. Limsirichaikul, T. Oike, H. Sato, K. D. Held, T. Nakano, A. Shibata, Y. Hagiwara, A. Niimi, M. Isono, M. Yamauchi, T. Yasuhara, S. Limsirichaikul, T. Oike, H. Sato, K. D. Held, T. Nakano, A. Shibata, Y. Hagiwara, A. Niimi, M. Isono, M. Yamauchi, T. Yasuhara, S. Limsirichaikul, T. Oike, H. Sato, K. D. Held, T. Nakano, and A. Shibata, “3D-structured illumination microscopy reveals clustered DNA double-strand break formation in widespread γH2AX foci after high LET heavy-ion particle radiation,” Oncotarget 8, 109370 (2017).
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Y. Hagiwara, A. Niimi, M. Isono, M. Yamauchi, T. Yasuhara, S. Limsirichaikul, T. Oike, H. Sato, K. D. Held, T. Nakano, A. Shibata, Y. Hagiwara, A. Niimi, M. Isono, M. Yamauchi, T. Yasuhara, S. Limsirichaikul, T. Oike, H. Sato, K. D. Held, T. Nakano, A. Shibata, Y. Hagiwara, A. Niimi, M. Isono, M. Yamauchi, T. Yasuhara, S. Limsirichaikul, T. Oike, H. Sato, K. D. Held, T. Nakano, and A. Shibata, “3D-structured illumination microscopy reveals clustered DNA double-strand break formation in widespread γH2AX foci after high LET heavy-ion particle radiation,” Oncotarget 8, 109370 (2017).
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N. Nitta, T. Sugimura, A. Isozaki, H. Mikami, K. Hiraki, S. Sakuma, T. Iino, F. Arai, T. Endo, Y. Fujiwaki, H. Fukuzawa, M. Hase, T. Hayakawa, K. Hiramatsu, Y. Hoshino, M. Inaba, T. Ito, H. Karakawa, Y. Kasai, K. Koizumi, S. Lee, C. Lei, M. Li, T. Maeno, S. Matsusaka, D. Murakami, A. Nakagawa, Y. Oguchi, M. Oikawa, T. Ota, K. Shiba, H. Shintaku, Y. Shirasaki, K. Suga, Y. Suzuki, N. Suzuki, Y. Tanaka, H. Tezuka, C. Toyokawa, Y. Yalikun, M. Yamada, M. Yamagishi, T. Yamano, A. Yasumoto, Y. Yatomi, M. Yazawa, D. Di Carlo, Y. Hosokawa, S. Uemura, Y. Ozeki, and K. Goda, “Intelligent image-activated cell sorting,” Cell 175, 266–276 (2018).
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K. Goda, A. Ayazi, D. R. Gossett, J. Sadasivam, C. K. Lonappan, E. Sollier, A. M. Fard, S. C. Hur, J. Adam, C. Murray, C. Wang, N. Brackbill, D. Di Carlo, and B. Jalali, “High-throughput single-microparticle imaging flow analyzer,” Proc. Natl. Acad. Sci. USA 109, 11630–11635 (2012).
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S. Ota, R. Horisaki, Y. Kawamura, M. Ugawa, I. Sato, K. Hashimoto, R. Kamesawa, K. Setoyama, S. Yamaguchi, K. Fujiu, K. Waki, and H. Noji, “Ghost cytometry,” Science 360, 1246–1251 (2018).
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Karakawa, H.

N. Nitta, T. Sugimura, A. Isozaki, H. Mikami, K. Hiraki, S. Sakuma, T. Iino, F. Arai, T. Endo, Y. Fujiwaki, H. Fukuzawa, M. Hase, T. Hayakawa, K. Hiramatsu, Y. Hoshino, M. Inaba, T. Ito, H. Karakawa, Y. Kasai, K. Koizumi, S. Lee, C. Lei, M. Li, T. Maeno, S. Matsusaka, D. Murakami, A. Nakagawa, Y. Oguchi, M. Oikawa, T. Ota, K. Shiba, H. Shintaku, Y. Shirasaki, K. Suga, Y. Suzuki, N. Suzuki, Y. Tanaka, H. Tezuka, C. Toyokawa, Y. Yalikun, M. Yamada, M. Yamagishi, T. Yamano, A. Yasumoto, Y. Yatomi, M. Yazawa, D. Di Carlo, Y. Hosokawa, S. Uemura, Y. Ozeki, and K. Goda, “Intelligent image-activated cell sorting,” Cell 175, 266–276 (2018).
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N. Nitta, T. Sugimura, A. Isozaki, H. Mikami, K. Hiraki, S. Sakuma, T. Iino, F. Arai, T. Endo, Y. Fujiwaki, H. Fukuzawa, M. Hase, T. Hayakawa, K. Hiramatsu, Y. Hoshino, M. Inaba, T. Ito, H. Karakawa, Y. Kasai, K. Koizumi, S. Lee, C. Lei, M. Li, T. Maeno, S. Matsusaka, D. Murakami, A. Nakagawa, Y. Oguchi, M. Oikawa, T. Ota, K. Shiba, H. Shintaku, Y. Shirasaki, K. Suga, Y. Suzuki, N. Suzuki, Y. Tanaka, H. Tezuka, C. Toyokawa, Y. Yalikun, M. Yamada, M. Yamagishi, T. Yamano, A. Yasumoto, Y. Yatomi, M. Yazawa, D. Di Carlo, Y. Hosokawa, S. Uemura, Y. Ozeki, and K. Goda, “Intelligent image-activated cell sorting,” Cell 175, 266–276 (2018).
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J. T. Chang, V. R. Palanivel, I. Kinjyo, F. Schambach, A. M. Intlekofer, A. Banerjee, S. A. Longworth, K. E. Vinup, P. Mrass, J. Oliaro, N. Killeen, J. S. Orange, S. M. Russell, W. Weninger, and S. L. Reiner, “Asymmetric T lymphocyte division in the initiation of adaptive immune responses,” Science 315, 1687–1691 (2007).
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N. Nitta, T. Sugimura, A. Isozaki, H. Mikami, K. Hiraki, S. Sakuma, T. Iino, F. Arai, T. Endo, Y. Fujiwaki, H. Fukuzawa, M. Hase, T. Hayakawa, K. Hiramatsu, Y. Hoshino, M. Inaba, T. Ito, H. Karakawa, Y. Kasai, K. Koizumi, S. Lee, C. Lei, M. Li, T. Maeno, S. Matsusaka, D. Murakami, A. Nakagawa, Y. Oguchi, M. Oikawa, T. Ota, K. Shiba, H. Shintaku, Y. Shirasaki, K. Suga, Y. Suzuki, N. Suzuki, Y. Tanaka, H. Tezuka, C. Toyokawa, Y. Yalikun, M. Yamada, M. Yamagishi, T. Yamano, A. Yasumoto, Y. Yatomi, M. Yazawa, D. Di Carlo, Y. Hosokawa, S. Uemura, Y. Ozeki, and K. Goda, “Intelligent image-activated cell sorting,” Cell 175, 266–276 (2018).
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A. Janssen, M. van der Burg, K. Szuhai, G. J. P. L. Kops, and R. H. Medema, “Chromosome segregation errors as a cause of DNA damage and structural chromosome aberrations,” Science 333, 1895–1898 (2011).
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Lee, S.

N. Nitta, T. Sugimura, A. Isozaki, H. Mikami, K. Hiraki, S. Sakuma, T. Iino, F. Arai, T. Endo, Y. Fujiwaki, H. Fukuzawa, M. Hase, T. Hayakawa, K. Hiramatsu, Y. Hoshino, M. Inaba, T. Ito, H. Karakawa, Y. Kasai, K. Koizumi, S. Lee, C. Lei, M. Li, T. Maeno, S. Matsusaka, D. Murakami, A. Nakagawa, Y. Oguchi, M. Oikawa, T. Ota, K. Shiba, H. Shintaku, Y. Shirasaki, K. Suga, Y. Suzuki, N. Suzuki, Y. Tanaka, H. Tezuka, C. Toyokawa, Y. Yalikun, M. Yamada, M. Yamagishi, T. Yamano, A. Yasumoto, Y. Yatomi, M. Yazawa, D. Di Carlo, Y. Hosokawa, S. Uemura, Y. Ozeki, and K. Goda, “Intelligent image-activated cell sorting,” Cell 175, 266–276 (2018).
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Y. Hagiwara, A. Niimi, M. Isono, M. Yamauchi, T. Yasuhara, S. Limsirichaikul, T. Oike, H. Sato, K. D. Held, T. Nakano, A. Shibata, Y. Hagiwara, A. Niimi, M. Isono, M. Yamauchi, T. Yasuhara, S. Limsirichaikul, T. Oike, H. Sato, K. D. Held, T. Nakano, A. Shibata, Y. Hagiwara, A. Niimi, M. Isono, M. Yamauchi, T. Yasuhara, S. Limsirichaikul, T. Oike, H. Sato, K. D. Held, T. Nakano, and A. Shibata, “3D-structured illumination microscopy reveals clustered DNA double-strand break formation in widespread γH2AX foci after high LET heavy-ion particle radiation,” Oncotarget 8, 109370 (2017).
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Y. Hagiwara, A. Niimi, M. Isono, M. Yamauchi, T. Yasuhara, S. Limsirichaikul, T. Oike, H. Sato, K. D. Held, T. Nakano, A. Shibata, Y. Hagiwara, A. Niimi, M. Isono, M. Yamauchi, T. Yasuhara, S. Limsirichaikul, T. Oike, H. Sato, K. D. Held, T. Nakano, A. Shibata, Y. Hagiwara, A. Niimi, M. Isono, M. Yamauchi, T. Yasuhara, S. Limsirichaikul, T. Oike, H. Sato, K. D. Held, T. Nakano, and A. Shibata, “3D-structured illumination microscopy reveals clustered DNA double-strand break formation in widespread γH2AX foci after high LET heavy-ion particle radiation,” Oncotarget 8, 109370 (2017).
[Crossref]

Y. Hagiwara, A. Niimi, M. Isono, M. Yamauchi, T. Yasuhara, S. Limsirichaikul, T. Oike, H. Sato, K. D. Held, T. Nakano, A. Shibata, Y. Hagiwara, A. Niimi, M. Isono, M. Yamauchi, T. Yasuhara, S. Limsirichaikul, T. Oike, H. Sato, K. D. Held, T. Nakano, A. Shibata, Y. Hagiwara, A. Niimi, M. Isono, M. Yamauchi, T. Yasuhara, S. Limsirichaikul, T. Oike, H. Sato, K. D. Held, T. Nakano, and A. Shibata, “3D-structured illumination microscopy reveals clustered DNA double-strand break formation in widespread γH2AX foci after high LET heavy-ion particle radiation,” Oncotarget 8, 109370 (2017).
[Crossref]

Y. Hagiwara, A. Niimi, M. Isono, M. Yamauchi, T. Yasuhara, S. Limsirichaikul, T. Oike, H. Sato, K. D. Held, T. Nakano, A. Shibata, Y. Hagiwara, A. Niimi, M. Isono, M. Yamauchi, T. Yasuhara, S. Limsirichaikul, T. Oike, H. Sato, K. D. Held, T. Nakano, A. Shibata, Y. Hagiwara, A. Niimi, M. Isono, M. Yamauchi, T. Yasuhara, S. Limsirichaikul, T. Oike, H. Sato, K. D. Held, T. Nakano, and A. Shibata, “3D-structured illumination microscopy reveals clustered DNA double-strand break formation in widespread γH2AX foci after high LET heavy-ion particle radiation,” Oncotarget 8, 109370 (2017).
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P. Y. Liu, L. K. Chin, W. Ser, H. F. Chen, C.-M. Hsieh, C.-H. Lee, K.-B. Sung, T. C. Ayi, P. H. Yap, B. Liedberg, K. Wang, T. Bourouina, and Y. Leprince-Wang, “Cell refractive index for cell biology and disease diagnosis: past, present and future,” Lab Chip 16, 634–644 (2016).
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[Crossref]

Y. Hagiwara, A. Niimi, M. Isono, M. Yamauchi, T. Yasuhara, S. Limsirichaikul, T. Oike, H. Sato, K. D. Held, T. Nakano, A. Shibata, Y. Hagiwara, A. Niimi, M. Isono, M. Yamauchi, T. Yasuhara, S. Limsirichaikul, T. Oike, H. Sato, K. D. Held, T. Nakano, A. Shibata, Y. Hagiwara, A. Niimi, M. Isono, M. Yamauchi, T. Yasuhara, S. Limsirichaikul, T. Oike, H. Sato, K. D. Held, T. Nakano, and A. Shibata, “3D-structured illumination microscopy reveals clustered DNA double-strand break formation in widespread γH2AX foci after high LET heavy-ion particle radiation,” Oncotarget 8, 109370 (2017).
[Crossref]

Y. Hagiwara, A. Niimi, M. Isono, M. Yamauchi, T. Yasuhara, S. Limsirichaikul, T. Oike, H. Sato, K. D. Held, T. Nakano, A. Shibata, Y. Hagiwara, A. Niimi, M. Isono, M. Yamauchi, T. Yasuhara, S. Limsirichaikul, T. Oike, H. Sato, K. D. Held, T. Nakano, A. Shibata, Y. Hagiwara, A. Niimi, M. Isono, M. Yamauchi, T. Yasuhara, S. Limsirichaikul, T. Oike, H. Sato, K. D. Held, T. Nakano, and A. Shibata, “3D-structured illumination microscopy reveals clustered DNA double-strand break formation in widespread γH2AX foci after high LET heavy-ion particle radiation,” Oncotarget 8, 109370 (2017).
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Supplementary Material (2)

NameDescription
» Supplement 1       Fluidic system and sample preparation
» Visualization 1       Videos

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Figures (5)

Fig. 1.
Fig. 1. Implementation of the 3D-IFC System and demonstration of time to 3D space mapping. (a) Schematic diagram of the 3D-IFC system. AOD, acousto-optic deflector; CL, cylindrical lens; IO, 50X/0.55 illumination objective lens; DO, 10X/0.28 detection objective lens; SF, spatial filter; DMs, dichroic mirrors; PMT, photomultiplier tube; DIG, 125    MSs 1 digitizer. The AOD and CL produce a scanning light sheet. The sample is 2D hydrodynamically focused by sheath before entering the square cross section quartz flow cell. (b) Optical interrogation area. H , the height of the light sheet; ϑ , tilt angle between flow ( y axis) and vertical line. Illumination light sheet propagates horizontally and scans in the z axis; the sample flows in the y axis; x is the orthogonal axis. The spatial filter at the image plane uses pinholes to produce line scans across the x axis. (c) 3D reconstructed space. The resolution on the x axis is determined by the number of pinholes (pixelated field of view in the x direction); resolution of Y by the distance between two slits (pixelated field of view in the y direction); and resolution of Z by the light-sheet scanning range (pixelated field of view in the z direction); (d) one light-sheet scan period produces a 1D light intensity profile in the z axis. The PMT voltage readout of one sample point corresponds to the light intensity of one voxel in the z -axis. (e) While object travels along the y axis, multiple scans produce a 2D profile in the y z plane within one pinhole scan period. Each section—separated by dotted lines—corresponds to the light intensity of one row in the 2D image stack. (f) When an object completely passes through the spatial filter covering the area, the time-domain signal contains the complete information of the 3D profile in the x y z space. Each section corresponds to one 2D image slice. AOD, tuning voltage of the AOD driver; FL1, PMT readout of fluorescence detection channel 1; FL2, PMT readout of fluorescence detection channel 2; SSC, PMT readout of SSC light detection channel.
Fig. 2.
Fig. 2. Spatial filter design. Two examples of spatial filters placed at the image plane. The top two and bottom two long slits with dimensions of 10 μm by 200 μm are for speed detection. The other pinholes on the spatial filter are 10 μm by 20 μm (left) and 10 μm by 10 μm (right), for 3D image capturing with a pixel size of 2 μm and 1 μm in the x direction, respectively.
Fig. 3.
Fig. 3. Simulated and measured PSF. (a) Simulated detection PSF with a 10X/0.28 objective lens in y z plane; (b) simulated light-sheet cross section in y z plane; (c) effective PSF in y z plane, FWHM, Δ y = 1.38    μm , Δ z = 0.73    μm ; (d) PSF variation along y and z axes; (e) experimental y z -plane image of a 1 μm fluorescent bead. The red curves in the profile plot are PMT raw signals; the black curves are fitted Gaussian curves. Scale bars, 5 μm.
Fig. 4.
Fig. 4. Cells and beads imaged by the 3D-IFC. CFSE-stained HEK-293 cells bound with 1 μm fluorescent beads. (a) Recovered 2D y z -plane images and the assembled 3D surface-rendered view of CFSE fluorescence, bead, and SSC (bottom row); (b) representative 3D images of cells bound with beads (see also Visualization 1) and histogram detection events. The explicit relative position relationship in 3D space indicates that the particle counting in the 3D-IFC is independent of cell orientation. In the example of cell bound with four beads, occlusion in a specific perspective is a likely source of error for particle counting with 2D images. (c) Intensity-based processing of 3D SSC images. Left column, intensity histograms of 3D SSC image of the cell shown in (a). P ( x , y , z ) is the position of 1 μm size bead determined using the 3D fluorescent image; within each bead position’s ± 1    μm area, the local intensity peak in 3D SSC image can be found. Scale bars, 5 μm. Flow speed 0.2 m/s. CFSE, intracellular carboxyfluorescein dye, Ex/Em: 488/517; bead, carboxylate-modified fluorescent microspheres, Ex/Em: 488/645; SSC, 90 deg SSC.
Fig. 5.
Fig. 5. Fluorescent γ H 2 AX foci imaged by the 3D-IFC. (a) Representative 3D images of irradiation-damaged glioblastoma CMK3 cells stained with CFSE and γ H 2 AX antibody-conjugated PerCP/Cy5.5 and their two-color fluorescence 2D y z plane merged image slices at x = 10    μm . The high quality of the 3D images shows that the 3D-IFC is suitable for DNA damaged foci-related study. (b) Scatterplot of 917 detection events in the γ H 2 AX intensity and foci count together with images of the cells within the marked regions (i)–(iv) in the scatterplot. The data show that foci count is unrelated to the fluorescence intensity from labeled γ H 2 AX ; thus, intensity-based measurements with conventional flow cytometry metrics are unable to evaluate the extent of DNA damage. Scale bars, 5 μm; flow speed, 0.2 m/s; CFSE, intracellular carboxyfluorescein dye, Ex/Em, 488/517; PerCP-Cy5.5, DNA damage antibody-conjugated dye, Ex/Em, 490/677.

Equations (11)

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Im ( x , y , z , t ) = O ( x , y , z , t ) · psf ( x x , y y , z z ) d x d y d z ,
O ( x , y , z , t ) = C ( x , y v C t , z ) · I ( z , t ) ,
S ( t ) = Im ( x , y , z c , t ) · F ( M x , M y ) d x d y ,
S ( t ) = { C ( x , y v C t , z ) · I ( z , t ) · psf ( x x , y y , z C z ) d x d y d z } · F ( M x , M y ) d x d y .
z 0 ( t ( n T , ( n + 1 ) T ) ) = v i ( t n T ) n = 0 , 1 , 2 , ,
I ( z , t ) = k · e ( z z 0 ( t ) ) 2 σ 2 ,
I ( z , t ) k · δ ( z z 0 ( t ) ) .
p s f ( x , y , z ) δ ( x , y ) .
S ( t ) = k F ( M x , M y ) · C ( x , y v C t , z 0 ( t ) ) d x d y .
F ( x , y ) = q = 1 N δ ( x x q ) · δ ( y y q ) with    x q = q X , y q = q Y ,
S ( t ) = k M 2 C ( x , y v C t , z 0 ( t ) ) δ ( x x j M ) δ ( y y j M ) d x d y = k M 2 C ( x j M , y j M v C t , z 0 ( t ) ) .

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