Abstract

In situ labeling of cells within living biological tissues using photoconversion has provided valuable information on cellular physiology in their natural environments. However, current photoconvertible probes typically require seconds to minutes of light exposure, limiting their uses in rapid biological processes such as intracellular diffusion and circulating cells. Here, we report that two-photon photoconversion of cyanine-based dyes offers unprecedentedly rapid photoconversion down to millisecond timescales per cell. We demonstrate potential biological applications including measuring intracellular diffusion kinetics in a spinal nerve, labeling of rapidly flowing cells in a microfluidic channel, and photoconversion of a circulating cell in vivo.

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

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References

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    [Crossref] [PubMed]
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    [Crossref] [PubMed]
  24. X. Kong, S. K. Mohanty, J. Stephens, J. T. Heale, V. Gomez-Godinez, L. Z. Shi, J.-S. Kim, K. Yokomori, and M. W. Berns, “Comparative analysis of different laser systems to study cellular responses to DNA damage in mammalian cells,” Nucleic Acids Res. 37(9), e68 (2009).
    [Crossref] [PubMed]
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    [Crossref] [PubMed]

2018 (2)

E. R. Pereira, D. Kedrin, G. Seano, O. Gautier, E. F. J. Meijer, D. Jones, S.-M. Chin, S. Kitahara, E. M. Bouta, J. Chang, E. Beech, H.-S. Jeong, M. C. Carroll, A. G. Taghian, and T. P. Padera, “Lymph node metastases can invade local blood vessels, exit the node, and colonize distant organs in mice,” Science 359(6382), 1403–1407 (2018).
[Crossref] [PubMed]

L. Dirix, K. Kennes, E. Fron, Z. Debyser, M. van der Auweraer, J. Hofkens, and S. Rocha, “Photoconversion of far-red organic dyes: implications for multi-color super-resolution imaging,” ChemPhotoChem 2(5), 433–441 (2018).
[Crossref]

2017 (3)

J. Konen, E. Summerbell, B. Dwivedi, K. Galior, Y. Hou, L. Rusnak, A. Chen, J. Saltz, W. Zhou, L. H. Boise, P. Vertino, L. Cooper, K. Salaita, J. Kowalski, and A. I. Marcus, “Image-guided genomics of phenotypically heterogeneous populations reveals vascular signalling during symbiotic collective cancer invasion,” Nat. Commun. 8, 15078 (2017).
[Crossref] [PubMed]

R. Turcotte, J. W. Wu, and C. P. Lin, “Intravital multiphoton photoconversion with a cell membrane dye,” J. Biophotonics 10(2), 206–210 (2017).
[Crossref] [PubMed]

T. Torcellan, H. R. Hampton, J. Bailey, M. Tomura, R. Brink, and T. Chtanova, “In vivo photolabeling of tumor-infiltrating cells reveals highly regulated egress of T-cell subsets from tumors,” Proc. Natl. Acad. Sci. U.S.A. 114(22), 5677–5682 (2017).
[Crossref] [PubMed]

2016 (2)

S. J. J. Kwok, M. Choi, B. Bhayana, X. Zhang, C. Ran, and S.-H. Yun, “Two-photon excited photoconversion of cyanine-based dyes,” Sci. Rep. 6(1), 23866 (2016).
[Crossref] [PubMed]

S. J. J. Kwok, M. Choi, B. Bhayana, X. Zhang, C. Ran, and S.-H. Yun, “Two-photon excited photoconversion of cyanine-based dyes,” Sci. Rep. 6(23866), 23866 (2016).
[Crossref] [PubMed]

2015 (2)

W. P. Dempsey, L. Georgieva, P. M. Helbling, A. Y. Sonay, T. V. Truong, M. Haffner, and P. Pantazis, “In vivo single-cell labeling by confined primed conversion,” Nat. Methods 12(7), 645–648 (2015).
[Crossref] [PubMed]

M. Choi, S. J. J. Kwok, and S. H. Yun, “In vivo fluorescence microscopy: lessons from observing cell behavior in their native environment,” Physiology (Bethesda) 30(1), 40–49 (2015).
[Crossref] [PubMed]

2014 (2)

T. Chtanova, H. R. Hampton, L. A. Waterhouse, K. Wood, M. Tomura, Y. Miwa, C. R. Mackay, R. Brink, and T. G. Phan, “Real-time interactive two-photon photoconversion of recirculating lymphocytes for discontinuous cell tracking in live adult mice,” J. Biophotonics 7(6), 425–433 (2014).
[Crossref] [PubMed]

D. A. Nedosekin, V. V. Verkhusha, A. V. Melerzanov, V. P. Zharov, and E. I. Galanzha, “In vivo photoswitchable flow cytometry for direct tracking of single circulating tumor cells,” Chem. Biol. 21(6), 792–801 (2014).
[Crossref] [PubMed]

2013 (3)

A. L. Carlson, J. Fujisaki, J. Wu, J. M. Runnels, R. Turcotte, J. A. Spencer, C. L. Celso, D. T. Scadden, T. B. Strom, and C. P. Lin, “Tracking Single Cells in Live Animals Using A Photoconvertible Near-Infrared Cell Membrane Label,” PLoS One 8(8), e69257 (2013).
[Crossref] [PubMed]

F. Persson, M. Lindén, C. Unoson, and J. Elf, “Extracting intracellular diffusive states and transition rates from single-molecule tracking data,” Nat. Methods 10(3), 265–269 (2013).
[Crossref] [PubMed]

E. Papagiakoumou, A. Bègue, B. Leshem, O. Schwartz, B. M. Stell, J. Bradley, D. Oron, and V. Emiliani, “Functional patterned multiphoton excitation deep inside scattering tissue,” Nat. Photonics 7(4), 274–278 (2013).
[Crossref]

2012 (1)

G. Katona, G. Szalay, P. Maák, A. Kaszás, M. Veress, D. Hillier, B. Chiovini, E. S. Vizi, B. Roska, and B. Rózsa, “Fast two-photon in vivo imaging with three-dimensional random-access scanning in large tissue volumes,” Nat. Methods 9(2), 201–208 (2012).
[Crossref] [PubMed]

2010 (1)

E. Papagiakoumou, F. Anselmi, A. Bègue, V. de Sars, J. Glückstad, E. Y. Isacoff, and V. Emiliani, “Scanless two-photon excitation of channelrhodopsin-2,” Nat. Methods 7(10), 848–854 (2010).
[Crossref] [PubMed]

2009 (1)

X. Kong, S. K. Mohanty, J. Stephens, J. T. Heale, V. Gomez-Godinez, L. Z. Shi, J.-S. Kim, K. Yokomori, and M. W. Berns, “Comparative analysis of different laser systems to study cellular responses to DNA damage in mammalian cells,” Nucleic Acids Res. 37(9), e68 (2009).
[Crossref] [PubMed]

2008 (1)

T. Matsuda, A. Miyawaki, and T. Nagai, “Direct measurement of protein dynamics inside cells using a rationally designed photoconvertible protein,” Nat. Methods 5(4), 339–345 (2008).
[Crossref] [PubMed]

2007 (1)

2006 (1)

M. L. Denton, M. S. Foltz, L. E. Estlack, D. J. Stolarski, G. D. Noojin, R. J. Thomas, D. Eikum, and B. A. Rockwell, “Damage Thresholds for Exposure to NIR and Blue Lasers in an In Vitro RPE Cell System,” Invest. Ophthalmol. Vis. Sci. 47(7), 3065–3073 (2006).
[Crossref] [PubMed]

2005 (2)

J. N. Post, K. A. Lidke, B. Rieger, and D. J. Arndt-Jovin, “One- and two-photon photoactivation of a paGFP-fusion protein in live Drosophila embryos,” FEBS Lett. 579(2), 325–330 (2005).
[Crossref] [PubMed]

A. Vogel, J. Noack, G. Hüttman, and G. Paltauf, “Mechanisms of femtosecond laser nanosurgery of cells and tissues,” Appl. Phys. B 81(8), 1015–1047 (2005).
[Crossref]

2003 (2)

R. Weissleder and V. Ntziachristos, “Shedding light onto live molecular targets,” Nat. Med. 9(1), 123–128 (2003).
[Crossref] [PubMed]

W. R. Zipfel, R. M. Williams, and W. W. Webb, “Nonlinear magic: multiphoton microscopy in the biosciences,” Nat. Biotechnol. 21(11), 1369–1377 (2003).
[Crossref] [PubMed]

2002 (2)

T. Nagai, K. Ibata, E. S. Park, M. Kubota, K. Mikoshiba, and A. Miyawaki, “A variant of yellow fluorescent protein with fast and efficient maturation for cell-biological applications,” Nat. Biotechnol. 20(1), 87–90 (2002).
[Crossref] [PubMed]

G. H. Patterson and J. Lippincott-Schwartz, “A photoactivatable GFP for selective photolabeling of proteins and cells,” Science 297(5588), 1873–1877 (2002).
[Crossref] [PubMed]

1995 (1)

T. G. Gorgels and D. van Norren, “Ultraviolet and green light cause different types of damage in rat retina,” Invest. Ophthalmol. Vis. Sci. 36(5), 851–863 (1995).
[PubMed]

Anselmi, F.

E. Papagiakoumou, F. Anselmi, A. Bègue, V. de Sars, J. Glückstad, E. Y. Isacoff, and V. Emiliani, “Scanless two-photon excitation of channelrhodopsin-2,” Nat. Methods 7(10), 848–854 (2010).
[Crossref] [PubMed]

Arndt-Jovin, D. J.

J. N. Post, K. A. Lidke, B. Rieger, and D. J. Arndt-Jovin, “One- and two-photon photoactivation of a paGFP-fusion protein in live Drosophila embryos,” FEBS Lett. 579(2), 325–330 (2005).
[Crossref] [PubMed]

Bailey, J.

T. Torcellan, H. R. Hampton, J. Bailey, M. Tomura, R. Brink, and T. Chtanova, “In vivo photolabeling of tumor-infiltrating cells reveals highly regulated egress of T-cell subsets from tumors,” Proc. Natl. Acad. Sci. U.S.A. 114(22), 5677–5682 (2017).
[Crossref] [PubMed]

Beech, E.

E. R. Pereira, D. Kedrin, G. Seano, O. Gautier, E. F. J. Meijer, D. Jones, S.-M. Chin, S. Kitahara, E. M. Bouta, J. Chang, E. Beech, H.-S. Jeong, M. C. Carroll, A. G. Taghian, and T. P. Padera, “Lymph node metastases can invade local blood vessels, exit the node, and colonize distant organs in mice,” Science 359(6382), 1403–1407 (2018).
[Crossref] [PubMed]

Bègue, A.

E. Papagiakoumou, A. Bègue, B. Leshem, O. Schwartz, B. M. Stell, J. Bradley, D. Oron, and V. Emiliani, “Functional patterned multiphoton excitation deep inside scattering tissue,” Nat. Photonics 7(4), 274–278 (2013).
[Crossref]

E. Papagiakoumou, F. Anselmi, A. Bègue, V. de Sars, J. Glückstad, E. Y. Isacoff, and V. Emiliani, “Scanless two-photon excitation of channelrhodopsin-2,” Nat. Methods 7(10), 848–854 (2010).
[Crossref] [PubMed]

Berns, M. W.

X. Kong, S. K. Mohanty, J. Stephens, J. T. Heale, V. Gomez-Godinez, L. Z. Shi, J.-S. Kim, K. Yokomori, and M. W. Berns, “Comparative analysis of different laser systems to study cellular responses to DNA damage in mammalian cells,” Nucleic Acids Res. 37(9), e68 (2009).
[Crossref] [PubMed]

Bhayana, B.

S. J. J. Kwok, M. Choi, B. Bhayana, X. Zhang, C. Ran, and S.-H. Yun, “Two-photon excited photoconversion of cyanine-based dyes,” Sci. Rep. 6(23866), 23866 (2016).
[Crossref] [PubMed]

S. J. J. Kwok, M. Choi, B. Bhayana, X. Zhang, C. Ran, and S.-H. Yun, “Two-photon excited photoconversion of cyanine-based dyes,” Sci. Rep. 6(1), 23866 (2016).
[Crossref] [PubMed]

Boise, L. H.

J. Konen, E. Summerbell, B. Dwivedi, K. Galior, Y. Hou, L. Rusnak, A. Chen, J. Saltz, W. Zhou, L. H. Boise, P. Vertino, L. Cooper, K. Salaita, J. Kowalski, and A. I. Marcus, “Image-guided genomics of phenotypically heterogeneous populations reveals vascular signalling during symbiotic collective cancer invasion,” Nat. Commun. 8, 15078 (2017).
[Crossref] [PubMed]

Bouta, E. M.

E. R. Pereira, D. Kedrin, G. Seano, O. Gautier, E. F. J. Meijer, D. Jones, S.-M. Chin, S. Kitahara, E. M. Bouta, J. Chang, E. Beech, H.-S. Jeong, M. C. Carroll, A. G. Taghian, and T. P. Padera, “Lymph node metastases can invade local blood vessels, exit the node, and colonize distant organs in mice,” Science 359(6382), 1403–1407 (2018).
[Crossref] [PubMed]

Bradley, J.

E. Papagiakoumou, A. Bègue, B. Leshem, O. Schwartz, B. M. Stell, J. Bradley, D. Oron, and V. Emiliani, “Functional patterned multiphoton excitation deep inside scattering tissue,” Nat. Photonics 7(4), 274–278 (2013).
[Crossref]

Brink, R.

T. Torcellan, H. R. Hampton, J. Bailey, M. Tomura, R. Brink, and T. Chtanova, “In vivo photolabeling of tumor-infiltrating cells reveals highly regulated egress of T-cell subsets from tumors,” Proc. Natl. Acad. Sci. U.S.A. 114(22), 5677–5682 (2017).
[Crossref] [PubMed]

T. Chtanova, H. R. Hampton, L. A. Waterhouse, K. Wood, M. Tomura, Y. Miwa, C. R. Mackay, R. Brink, and T. G. Phan, “Real-time interactive two-photon photoconversion of recirculating lymphocytes for discontinuous cell tracking in live adult mice,” J. Biophotonics 7(6), 425–433 (2014).
[Crossref] [PubMed]

Carlson, A. L.

A. L. Carlson, J. Fujisaki, J. Wu, J. M. Runnels, R. Turcotte, J. A. Spencer, C. L. Celso, D. T. Scadden, T. B. Strom, and C. P. Lin, “Tracking Single Cells in Live Animals Using A Photoconvertible Near-Infrared Cell Membrane Label,” PLoS One 8(8), e69257 (2013).
[Crossref] [PubMed]

Carroll, M. C.

E. R. Pereira, D. Kedrin, G. Seano, O. Gautier, E. F. J. Meijer, D. Jones, S.-M. Chin, S. Kitahara, E. M. Bouta, J. Chang, E. Beech, H.-S. Jeong, M. C. Carroll, A. G. Taghian, and T. P. Padera, “Lymph node metastases can invade local blood vessels, exit the node, and colonize distant organs in mice,” Science 359(6382), 1403–1407 (2018).
[Crossref] [PubMed]

Celso, C. L.

A. L. Carlson, J. Fujisaki, J. Wu, J. M. Runnels, R. Turcotte, J. A. Spencer, C. L. Celso, D. T. Scadden, T. B. Strom, and C. P. Lin, “Tracking Single Cells in Live Animals Using A Photoconvertible Near-Infrared Cell Membrane Label,” PLoS One 8(8), e69257 (2013).
[Crossref] [PubMed]

Chang, J.

E. R. Pereira, D. Kedrin, G. Seano, O. Gautier, E. F. J. Meijer, D. Jones, S.-M. Chin, S. Kitahara, E. M. Bouta, J. Chang, E. Beech, H.-S. Jeong, M. C. Carroll, A. G. Taghian, and T. P. Padera, “Lymph node metastases can invade local blood vessels, exit the node, and colonize distant organs in mice,” Science 359(6382), 1403–1407 (2018).
[Crossref] [PubMed]

Chen, A.

J. Konen, E. Summerbell, B. Dwivedi, K. Galior, Y. Hou, L. Rusnak, A. Chen, J. Saltz, W. Zhou, L. H. Boise, P. Vertino, L. Cooper, K. Salaita, J. Kowalski, and A. I. Marcus, “Image-guided genomics of phenotypically heterogeneous populations reveals vascular signalling during symbiotic collective cancer invasion,” Nat. Commun. 8, 15078 (2017).
[Crossref] [PubMed]

Chin, S.-M.

E. R. Pereira, D. Kedrin, G. Seano, O. Gautier, E. F. J. Meijer, D. Jones, S.-M. Chin, S. Kitahara, E. M. Bouta, J. Chang, E. Beech, H.-S. Jeong, M. C. Carroll, A. G. Taghian, and T. P. Padera, “Lymph node metastases can invade local blood vessels, exit the node, and colonize distant organs in mice,” Science 359(6382), 1403–1407 (2018).
[Crossref] [PubMed]

Chiovini, B.

G. Katona, G. Szalay, P. Maák, A. Kaszás, M. Veress, D. Hillier, B. Chiovini, E. S. Vizi, B. Roska, and B. Rózsa, “Fast two-photon in vivo imaging with three-dimensional random-access scanning in large tissue volumes,” Nat. Methods 9(2), 201–208 (2012).
[Crossref] [PubMed]

Choi, M.

S. J. J. Kwok, M. Choi, B. Bhayana, X. Zhang, C. Ran, and S.-H. Yun, “Two-photon excited photoconversion of cyanine-based dyes,” Sci. Rep. 6(1), 23866 (2016).
[Crossref] [PubMed]

S. J. J. Kwok, M. Choi, B. Bhayana, X. Zhang, C. Ran, and S.-H. Yun, “Two-photon excited photoconversion of cyanine-based dyes,” Sci. Rep. 6(23866), 23866 (2016).
[Crossref] [PubMed]

M. Choi, S. J. J. Kwok, and S. H. Yun, “In vivo fluorescence microscopy: lessons from observing cell behavior in their native environment,” Physiology (Bethesda) 30(1), 40–49 (2015).
[Crossref] [PubMed]

Chtanova, T.

T. Torcellan, H. R. Hampton, J. Bailey, M. Tomura, R. Brink, and T. Chtanova, “In vivo photolabeling of tumor-infiltrating cells reveals highly regulated egress of T-cell subsets from tumors,” Proc. Natl. Acad. Sci. U.S.A. 114(22), 5677–5682 (2017).
[Crossref] [PubMed]

T. Chtanova, H. R. Hampton, L. A. Waterhouse, K. Wood, M. Tomura, Y. Miwa, C. R. Mackay, R. Brink, and T. G. Phan, “Real-time interactive two-photon photoconversion of recirculating lymphocytes for discontinuous cell tracking in live adult mice,” J. Biophotonics 7(6), 425–433 (2014).
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E. Papagiakoumou, A. Bègue, B. Leshem, O. Schwartz, B. M. Stell, J. Bradley, D. Oron, and V. Emiliani, “Functional patterned multiphoton excitation deep inside scattering tissue,” Nat. Photonics 7(4), 274–278 (2013).
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E. Papagiakoumou, F. Anselmi, A. Bègue, V. de Sars, J. Glückstad, E. Y. Isacoff, and V. Emiliani, “Scanless two-photon excitation of channelrhodopsin-2,” Nat. Methods 7(10), 848–854 (2010).
[Crossref] [PubMed]

Park, E. S.

T. Nagai, K. Ibata, E. S. Park, M. Kubota, K. Mikoshiba, and A. Miyawaki, “A variant of yellow fluorescent protein with fast and efficient maturation for cell-biological applications,” Nat. Biotechnol. 20(1), 87–90 (2002).
[Crossref] [PubMed]

Patterson, G. H.

G. H. Patterson and J. Lippincott-Schwartz, “A photoactivatable GFP for selective photolabeling of proteins and cells,” Science 297(5588), 1873–1877 (2002).
[Crossref] [PubMed]

Pereira, E. R.

E. R. Pereira, D. Kedrin, G. Seano, O. Gautier, E. F. J. Meijer, D. Jones, S.-M. Chin, S. Kitahara, E. M. Bouta, J. Chang, E. Beech, H.-S. Jeong, M. C. Carroll, A. G. Taghian, and T. P. Padera, “Lymph node metastases can invade local blood vessels, exit the node, and colonize distant organs in mice,” Science 359(6382), 1403–1407 (2018).
[Crossref] [PubMed]

Persson, F.

F. Persson, M. Lindén, C. Unoson, and J. Elf, “Extracting intracellular diffusive states and transition rates from single-molecule tracking data,” Nat. Methods 10(3), 265–269 (2013).
[Crossref] [PubMed]

Phan, T. G.

T. Chtanova, H. R. Hampton, L. A. Waterhouse, K. Wood, M. Tomura, Y. Miwa, C. R. Mackay, R. Brink, and T. G. Phan, “Real-time interactive two-photon photoconversion of recirculating lymphocytes for discontinuous cell tracking in live adult mice,” J. Biophotonics 7(6), 425–433 (2014).
[Crossref] [PubMed]

Post, J. N.

J. N. Post, K. A. Lidke, B. Rieger, and D. J. Arndt-Jovin, “One- and two-photon photoactivation of a paGFP-fusion protein in live Drosophila embryos,” FEBS Lett. 579(2), 325–330 (2005).
[Crossref] [PubMed]

Ran, C.

S. J. J. Kwok, M. Choi, B. Bhayana, X. Zhang, C. Ran, and S.-H. Yun, “Two-photon excited photoconversion of cyanine-based dyes,” Sci. Rep. 6(23866), 23866 (2016).
[Crossref] [PubMed]

S. J. J. Kwok, M. Choi, B. Bhayana, X. Zhang, C. Ran, and S.-H. Yun, “Two-photon excited photoconversion of cyanine-based dyes,” Sci. Rep. 6(1), 23866 (2016).
[Crossref] [PubMed]

Rieger, B.

J. N. Post, K. A. Lidke, B. Rieger, and D. J. Arndt-Jovin, “One- and two-photon photoactivation of a paGFP-fusion protein in live Drosophila embryos,” FEBS Lett. 579(2), 325–330 (2005).
[Crossref] [PubMed]

Rocha, S.

L. Dirix, K. Kennes, E. Fron, Z. Debyser, M. van der Auweraer, J. Hofkens, and S. Rocha, “Photoconversion of far-red organic dyes: implications for multi-color super-resolution imaging,” ChemPhotoChem 2(5), 433–441 (2018).
[Crossref]

Rockwell, B. A.

M. L. Denton, M. S. Foltz, L. E. Estlack, D. J. Stolarski, G. D. Noojin, R. J. Thomas, D. Eikum, and B. A. Rockwell, “Damage Thresholds for Exposure to NIR and Blue Lasers in an In Vitro RPE Cell System,” Invest. Ophthalmol. Vis. Sci. 47(7), 3065–3073 (2006).
[Crossref] [PubMed]

Roska, B.

G. Katona, G. Szalay, P. Maák, A. Kaszás, M. Veress, D. Hillier, B. Chiovini, E. S. Vizi, B. Roska, and B. Rózsa, “Fast two-photon in vivo imaging with three-dimensional random-access scanning in large tissue volumes,” Nat. Methods 9(2), 201–208 (2012).
[Crossref] [PubMed]

Rózsa, B.

G. Katona, G. Szalay, P. Maák, A. Kaszás, M. Veress, D. Hillier, B. Chiovini, E. S. Vizi, B. Roska, and B. Rózsa, “Fast two-photon in vivo imaging with three-dimensional random-access scanning in large tissue volumes,” Nat. Methods 9(2), 201–208 (2012).
[Crossref] [PubMed]

Runnels, J. M.

A. L. Carlson, J. Fujisaki, J. Wu, J. M. Runnels, R. Turcotte, J. A. Spencer, C. L. Celso, D. T. Scadden, T. B. Strom, and C. P. Lin, “Tracking Single Cells in Live Animals Using A Photoconvertible Near-Infrared Cell Membrane Label,” PLoS One 8(8), e69257 (2013).
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Rusnak, L.

J. Konen, E. Summerbell, B. Dwivedi, K. Galior, Y. Hou, L. Rusnak, A. Chen, J. Saltz, W. Zhou, L. H. Boise, P. Vertino, L. Cooper, K. Salaita, J. Kowalski, and A. I. Marcus, “Image-guided genomics of phenotypically heterogeneous populations reveals vascular signalling during symbiotic collective cancer invasion,” Nat. Commun. 8, 15078 (2017).
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Salaita, K.

J. Konen, E. Summerbell, B. Dwivedi, K. Galior, Y. Hou, L. Rusnak, A. Chen, J. Saltz, W. Zhou, L. H. Boise, P. Vertino, L. Cooper, K. Salaita, J. Kowalski, and A. I. Marcus, “Image-guided genomics of phenotypically heterogeneous populations reveals vascular signalling during symbiotic collective cancer invasion,” Nat. Commun. 8, 15078 (2017).
[Crossref] [PubMed]

Saltz, J.

J. Konen, E. Summerbell, B. Dwivedi, K. Galior, Y. Hou, L. Rusnak, A. Chen, J. Saltz, W. Zhou, L. H. Boise, P. Vertino, L. Cooper, K. Salaita, J. Kowalski, and A. I. Marcus, “Image-guided genomics of phenotypically heterogeneous populations reveals vascular signalling during symbiotic collective cancer invasion,” Nat. Commun. 8, 15078 (2017).
[Crossref] [PubMed]

Scadden, D. T.

A. L. Carlson, J. Fujisaki, J. Wu, J. M. Runnels, R. Turcotte, J. A. Spencer, C. L. Celso, D. T. Scadden, T. B. Strom, and C. P. Lin, “Tracking Single Cells in Live Animals Using A Photoconvertible Near-Infrared Cell Membrane Label,” PLoS One 8(8), e69257 (2013).
[Crossref] [PubMed]

Schwartz, O.

E. Papagiakoumou, A. Bègue, B. Leshem, O. Schwartz, B. M. Stell, J. Bradley, D. Oron, and V. Emiliani, “Functional patterned multiphoton excitation deep inside scattering tissue,” Nat. Photonics 7(4), 274–278 (2013).
[Crossref]

Seano, G.

E. R. Pereira, D. Kedrin, G. Seano, O. Gautier, E. F. J. Meijer, D. Jones, S.-M. Chin, S. Kitahara, E. M. Bouta, J. Chang, E. Beech, H.-S. Jeong, M. C. Carroll, A. G. Taghian, and T. P. Padera, “Lymph node metastases can invade local blood vessels, exit the node, and colonize distant organs in mice,” Science 359(6382), 1403–1407 (2018).
[Crossref] [PubMed]

Shi, L. Z.

X. Kong, S. K. Mohanty, J. Stephens, J. T. Heale, V. Gomez-Godinez, L. Z. Shi, J.-S. Kim, K. Yokomori, and M. W. Berns, “Comparative analysis of different laser systems to study cellular responses to DNA damage in mammalian cells,” Nucleic Acids Res. 37(9), e68 (2009).
[Crossref] [PubMed]

Shimada, T.

Shin-Ichi Arimura, S.

Sonay, A. Y.

W. P. Dempsey, L. Georgieva, P. M. Helbling, A. Y. Sonay, T. V. Truong, M. Haffner, and P. Pantazis, “In vivo single-cell labeling by confined primed conversion,” Nat. Methods 12(7), 645–648 (2015).
[Crossref] [PubMed]

Spencer, J. A.

A. L. Carlson, J. Fujisaki, J. Wu, J. M. Runnels, R. Turcotte, J. A. Spencer, C. L. Celso, D. T. Scadden, T. B. Strom, and C. P. Lin, “Tracking Single Cells in Live Animals Using A Photoconvertible Near-Infrared Cell Membrane Label,” PLoS One 8(8), e69257 (2013).
[Crossref] [PubMed]

Stell, B. M.

E. Papagiakoumou, A. Bègue, B. Leshem, O. Schwartz, B. M. Stell, J. Bradley, D. Oron, and V. Emiliani, “Functional patterned multiphoton excitation deep inside scattering tissue,” Nat. Photonics 7(4), 274–278 (2013).
[Crossref]

Stephens, J.

X. Kong, S. K. Mohanty, J. Stephens, J. T. Heale, V. Gomez-Godinez, L. Z. Shi, J.-S. Kim, K. Yokomori, and M. W. Berns, “Comparative analysis of different laser systems to study cellular responses to DNA damage in mammalian cells,” Nucleic Acids Res. 37(9), e68 (2009).
[Crossref] [PubMed]

Stolarski, D. J.

M. L. Denton, M. S. Foltz, L. E. Estlack, D. J. Stolarski, G. D. Noojin, R. J. Thomas, D. Eikum, and B. A. Rockwell, “Damage Thresholds for Exposure to NIR and Blue Lasers in an In Vitro RPE Cell System,” Invest. Ophthalmol. Vis. Sci. 47(7), 3065–3073 (2006).
[Crossref] [PubMed]

Strom, T. B.

A. L. Carlson, J. Fujisaki, J. Wu, J. M. Runnels, R. Turcotte, J. A. Spencer, C. L. Celso, D. T. Scadden, T. B. Strom, and C. P. Lin, “Tracking Single Cells in Live Animals Using A Photoconvertible Near-Infrared Cell Membrane Label,” PLoS One 8(8), e69257 (2013).
[Crossref] [PubMed]

Summerbell, E.

J. Konen, E. Summerbell, B. Dwivedi, K. Galior, Y. Hou, L. Rusnak, A. Chen, J. Saltz, W. Zhou, L. H. Boise, P. Vertino, L. Cooper, K. Salaita, J. Kowalski, and A. I. Marcus, “Image-guided genomics of phenotypically heterogeneous populations reveals vascular signalling during symbiotic collective cancer invasion,” Nat. Commun. 8, 15078 (2017).
[Crossref] [PubMed]

Szalay, G.

G. Katona, G. Szalay, P. Maák, A. Kaszás, M. Veress, D. Hillier, B. Chiovini, E. S. Vizi, B. Roska, and B. Rózsa, “Fast two-photon in vivo imaging with three-dimensional random-access scanning in large tissue volumes,” Nat. Methods 9(2), 201–208 (2012).
[Crossref] [PubMed]

Taghian, A. G.

E. R. Pereira, D. Kedrin, G. Seano, O. Gautier, E. F. J. Meijer, D. Jones, S.-M. Chin, S. Kitahara, E. M. Bouta, J. Chang, E. Beech, H.-S. Jeong, M. C. Carroll, A. G. Taghian, and T. P. Padera, “Lymph node metastases can invade local blood vessels, exit the node, and colonize distant organs in mice,” Science 359(6382), 1403–1407 (2018).
[Crossref] [PubMed]

Thomas, R. J.

M. L. Denton, M. S. Foltz, L. E. Estlack, D. J. Stolarski, G. D. Noojin, R. J. Thomas, D. Eikum, and B. A. Rockwell, “Damage Thresholds for Exposure to NIR and Blue Lasers in an In Vitro RPE Cell System,” Invest. Ophthalmol. Vis. Sci. 47(7), 3065–3073 (2006).
[Crossref] [PubMed]

Tomura, M.

T. Torcellan, H. R. Hampton, J. Bailey, M. Tomura, R. Brink, and T. Chtanova, “In vivo photolabeling of tumor-infiltrating cells reveals highly regulated egress of T-cell subsets from tumors,” Proc. Natl. Acad. Sci. U.S.A. 114(22), 5677–5682 (2017).
[Crossref] [PubMed]

T. Chtanova, H. R. Hampton, L. A. Waterhouse, K. Wood, M. Tomura, Y. Miwa, C. R. Mackay, R. Brink, and T. G. Phan, “Real-time interactive two-photon photoconversion of recirculating lymphocytes for discontinuous cell tracking in live adult mice,” J. Biophotonics 7(6), 425–433 (2014).
[Crossref] [PubMed]

Torcellan, T.

T. Torcellan, H. R. Hampton, J. Bailey, M. Tomura, R. Brink, and T. Chtanova, “In vivo photolabeling of tumor-infiltrating cells reveals highly regulated egress of T-cell subsets from tumors,” Proc. Natl. Acad. Sci. U.S.A. 114(22), 5677–5682 (2017).
[Crossref] [PubMed]

Truong, T. V.

W. P. Dempsey, L. Georgieva, P. M. Helbling, A. Y. Sonay, T. V. Truong, M. Haffner, and P. Pantazis, “In vivo single-cell labeling by confined primed conversion,” Nat. Methods 12(7), 645–648 (2015).
[Crossref] [PubMed]

Tsutsumi, N.

Turcotte, R.

R. Turcotte, J. W. Wu, and C. P. Lin, “Intravital multiphoton photoconversion with a cell membrane dye,” J. Biophotonics 10(2), 206–210 (2017).
[Crossref] [PubMed]

A. L. Carlson, J. Fujisaki, J. Wu, J. M. Runnels, R. Turcotte, J. A. Spencer, C. L. Celso, D. T. Scadden, T. B. Strom, and C. P. Lin, “Tracking Single Cells in Live Animals Using A Photoconvertible Near-Infrared Cell Membrane Label,” PLoS One 8(8), e69257 (2013).
[Crossref] [PubMed]

Unoson, C.

F. Persson, M. Lindén, C. Unoson, and J. Elf, “Extracting intracellular diffusive states and transition rates from single-molecule tracking data,” Nat. Methods 10(3), 265–269 (2013).
[Crossref] [PubMed]

van der Auweraer, M.

L. Dirix, K. Kennes, E. Fron, Z. Debyser, M. van der Auweraer, J. Hofkens, and S. Rocha, “Photoconversion of far-red organic dyes: implications for multi-color super-resolution imaging,” ChemPhotoChem 2(5), 433–441 (2018).
[Crossref]

van Norren, D.

T. G. Gorgels and D. van Norren, “Ultraviolet and green light cause different types of damage in rat retina,” Invest. Ophthalmol. Vis. Sci. 36(5), 851–863 (1995).
[PubMed]

Veress, M.

G. Katona, G. Szalay, P. Maák, A. Kaszás, M. Veress, D. Hillier, B. Chiovini, E. S. Vizi, B. Roska, and B. Rózsa, “Fast two-photon in vivo imaging with three-dimensional random-access scanning in large tissue volumes,” Nat. Methods 9(2), 201–208 (2012).
[Crossref] [PubMed]

Verkhusha, V. V.

D. A. Nedosekin, V. V. Verkhusha, A. V. Melerzanov, V. P. Zharov, and E. I. Galanzha, “In vivo photoswitchable flow cytometry for direct tracking of single circulating tumor cells,” Chem. Biol. 21(6), 792–801 (2014).
[Crossref] [PubMed]

Vertino, P.

J. Konen, E. Summerbell, B. Dwivedi, K. Galior, Y. Hou, L. Rusnak, A. Chen, J. Saltz, W. Zhou, L. H. Boise, P. Vertino, L. Cooper, K. Salaita, J. Kowalski, and A. I. Marcus, “Image-guided genomics of phenotypically heterogeneous populations reveals vascular signalling during symbiotic collective cancer invasion,” Nat. Commun. 8, 15078 (2017).
[Crossref] [PubMed]

Vizi, E. S.

G. Katona, G. Szalay, P. Maák, A. Kaszás, M. Veress, D. Hillier, B. Chiovini, E. S. Vizi, B. Roska, and B. Rózsa, “Fast two-photon in vivo imaging with three-dimensional random-access scanning in large tissue volumes,” Nat. Methods 9(2), 201–208 (2012).
[Crossref] [PubMed]

Vogel, A.

A. Vogel, J. Noack, G. Hüttman, and G. Paltauf, “Mechanisms of femtosecond laser nanosurgery of cells and tissues,” Appl. Phys. B 81(8), 1015–1047 (2005).
[Crossref]

Watanabe, W.

Waterhouse, L. A.

T. Chtanova, H. R. Hampton, L. A. Waterhouse, K. Wood, M. Tomura, Y. Miwa, C. R. Mackay, R. Brink, and T. G. Phan, “Real-time interactive two-photon photoconversion of recirculating lymphocytes for discontinuous cell tracking in live adult mice,” J. Biophotonics 7(6), 425–433 (2014).
[Crossref] [PubMed]

Webb, W. W.

W. R. Zipfel, R. M. Williams, and W. W. Webb, “Nonlinear magic: multiphoton microscopy in the biosciences,” Nat. Biotechnol. 21(11), 1369–1377 (2003).
[Crossref] [PubMed]

Weissleder, R.

R. Weissleder and V. Ntziachristos, “Shedding light onto live molecular targets,” Nat. Med. 9(1), 123–128 (2003).
[Crossref] [PubMed]

Williams, R. M.

W. R. Zipfel, R. M. Williams, and W. W. Webb, “Nonlinear magic: multiphoton microscopy in the biosciences,” Nat. Biotechnol. 21(11), 1369–1377 (2003).
[Crossref] [PubMed]

Wood, K.

T. Chtanova, H. R. Hampton, L. A. Waterhouse, K. Wood, M. Tomura, Y. Miwa, C. R. Mackay, R. Brink, and T. G. Phan, “Real-time interactive two-photon photoconversion of recirculating lymphocytes for discontinuous cell tracking in live adult mice,” J. Biophotonics 7(6), 425–433 (2014).
[Crossref] [PubMed]

Wu, J.

A. L. Carlson, J. Fujisaki, J. Wu, J. M. Runnels, R. Turcotte, J. A. Spencer, C. L. Celso, D. T. Scadden, T. B. Strom, and C. P. Lin, “Tracking Single Cells in Live Animals Using A Photoconvertible Near-Infrared Cell Membrane Label,” PLoS One 8(8), e69257 (2013).
[Crossref] [PubMed]

Wu, J. W.

R. Turcotte, J. W. Wu, and C. P. Lin, “Intravital multiphoton photoconversion with a cell membrane dye,” J. Biophotonics 10(2), 206–210 (2017).
[Crossref] [PubMed]

Yokomori, K.

X. Kong, S. K. Mohanty, J. Stephens, J. T. Heale, V. Gomez-Godinez, L. Z. Shi, J.-S. Kim, K. Yokomori, and M. W. Berns, “Comparative analysis of different laser systems to study cellular responses to DNA damage in mammalian cells,” Nucleic Acids Res. 37(9), e68 (2009).
[Crossref] [PubMed]

Yun, S. H.

M. Choi, S. J. J. Kwok, and S. H. Yun, “In vivo fluorescence microscopy: lessons from observing cell behavior in their native environment,” Physiology (Bethesda) 30(1), 40–49 (2015).
[Crossref] [PubMed]

Yun, S.-H.

S. J. J. Kwok, M. Choi, B. Bhayana, X. Zhang, C. Ran, and S.-H. Yun, “Two-photon excited photoconversion of cyanine-based dyes,” Sci. Rep. 6(23866), 23866 (2016).
[Crossref] [PubMed]

S. J. J. Kwok, M. Choi, B. Bhayana, X. Zhang, C. Ran, and S.-H. Yun, “Two-photon excited photoconversion of cyanine-based dyes,” Sci. Rep. 6(1), 23866 (2016).
[Crossref] [PubMed]

Zhang, X.

S. J. J. Kwok, M. Choi, B. Bhayana, X. Zhang, C. Ran, and S.-H. Yun, “Two-photon excited photoconversion of cyanine-based dyes,” Sci. Rep. 6(1), 23866 (2016).
[Crossref] [PubMed]

S. J. J. Kwok, M. Choi, B. Bhayana, X. Zhang, C. Ran, and S.-H. Yun, “Two-photon excited photoconversion of cyanine-based dyes,” Sci. Rep. 6(23866), 23866 (2016).
[Crossref] [PubMed]

Zharov, V. P.

D. A. Nedosekin, V. V. Verkhusha, A. V. Melerzanov, V. P. Zharov, and E. I. Galanzha, “In vivo photoswitchable flow cytometry for direct tracking of single circulating tumor cells,” Chem. Biol. 21(6), 792–801 (2014).
[Crossref] [PubMed]

Zhou, W.

J. Konen, E. Summerbell, B. Dwivedi, K. Galior, Y. Hou, L. Rusnak, A. Chen, J. Saltz, W. Zhou, L. H. Boise, P. Vertino, L. Cooper, K. Salaita, J. Kowalski, and A. I. Marcus, “Image-guided genomics of phenotypically heterogeneous populations reveals vascular signalling during symbiotic collective cancer invasion,” Nat. Commun. 8, 15078 (2017).
[Crossref] [PubMed]

Zipfel, W. R.

W. R. Zipfel, R. M. Williams, and W. W. Webb, “Nonlinear magic: multiphoton microscopy in the biosciences,” Nat. Biotechnol. 21(11), 1369–1377 (2003).
[Crossref] [PubMed]

Appl. Phys. B (1)

A. Vogel, J. Noack, G. Hüttman, and G. Paltauf, “Mechanisms of femtosecond laser nanosurgery of cells and tissues,” Appl. Phys. B 81(8), 1015–1047 (2005).
[Crossref]

Chem. Biol. (1)

D. A. Nedosekin, V. V. Verkhusha, A. V. Melerzanov, V. P. Zharov, and E. I. Galanzha, “In vivo photoswitchable flow cytometry for direct tracking of single circulating tumor cells,” Chem. Biol. 21(6), 792–801 (2014).
[Crossref] [PubMed]

ChemPhotoChem (1)

L. Dirix, K. Kennes, E. Fron, Z. Debyser, M. van der Auweraer, J. Hofkens, and S. Rocha, “Photoconversion of far-red organic dyes: implications for multi-color super-resolution imaging,” ChemPhotoChem 2(5), 433–441 (2018).
[Crossref]

FEBS Lett. (1)

J. N. Post, K. A. Lidke, B. Rieger, and D. J. Arndt-Jovin, “One- and two-photon photoactivation of a paGFP-fusion protein in live Drosophila embryos,” FEBS Lett. 579(2), 325–330 (2005).
[Crossref] [PubMed]

Invest. Ophthalmol. Vis. Sci. (2)

T. G. Gorgels and D. van Norren, “Ultraviolet and green light cause different types of damage in rat retina,” Invest. Ophthalmol. Vis. Sci. 36(5), 851–863 (1995).
[PubMed]

M. L. Denton, M. S. Foltz, L. E. Estlack, D. J. Stolarski, G. D. Noojin, R. J. Thomas, D. Eikum, and B. A. Rockwell, “Damage Thresholds for Exposure to NIR and Blue Lasers in an In Vitro RPE Cell System,” Invest. Ophthalmol. Vis. Sci. 47(7), 3065–3073 (2006).
[Crossref] [PubMed]

J. Biophotonics (2)

T. Chtanova, H. R. Hampton, L. A. Waterhouse, K. Wood, M. Tomura, Y. Miwa, C. R. Mackay, R. Brink, and T. G. Phan, “Real-time interactive two-photon photoconversion of recirculating lymphocytes for discontinuous cell tracking in live adult mice,” J. Biophotonics 7(6), 425–433 (2014).
[Crossref] [PubMed]

R. Turcotte, J. W. Wu, and C. P. Lin, “Intravital multiphoton photoconversion with a cell membrane dye,” J. Biophotonics 10(2), 206–210 (2017).
[Crossref] [PubMed]

Nat. Biotechnol. (2)

T. Nagai, K. Ibata, E. S. Park, M. Kubota, K. Mikoshiba, and A. Miyawaki, “A variant of yellow fluorescent protein with fast and efficient maturation for cell-biological applications,” Nat. Biotechnol. 20(1), 87–90 (2002).
[Crossref] [PubMed]

W. R. Zipfel, R. M. Williams, and W. W. Webb, “Nonlinear magic: multiphoton microscopy in the biosciences,” Nat. Biotechnol. 21(11), 1369–1377 (2003).
[Crossref] [PubMed]

Nat. Commun. (1)

J. Konen, E. Summerbell, B. Dwivedi, K. Galior, Y. Hou, L. Rusnak, A. Chen, J. Saltz, W. Zhou, L. H. Boise, P. Vertino, L. Cooper, K. Salaita, J. Kowalski, and A. I. Marcus, “Image-guided genomics of phenotypically heterogeneous populations reveals vascular signalling during symbiotic collective cancer invasion,” Nat. Commun. 8, 15078 (2017).
[Crossref] [PubMed]

Nat. Med. (1)

R. Weissleder and V. Ntziachristos, “Shedding light onto live molecular targets,” Nat. Med. 9(1), 123–128 (2003).
[Crossref] [PubMed]

Nat. Methods (5)

T. Matsuda, A. Miyawaki, and T. Nagai, “Direct measurement of protein dynamics inside cells using a rationally designed photoconvertible protein,” Nat. Methods 5(4), 339–345 (2008).
[Crossref] [PubMed]

W. P. Dempsey, L. Georgieva, P. M. Helbling, A. Y. Sonay, T. V. Truong, M. Haffner, and P. Pantazis, “In vivo single-cell labeling by confined primed conversion,” Nat. Methods 12(7), 645–648 (2015).
[Crossref] [PubMed]

F. Persson, M. Lindén, C. Unoson, and J. Elf, “Extracting intracellular diffusive states and transition rates from single-molecule tracking data,” Nat. Methods 10(3), 265–269 (2013).
[Crossref] [PubMed]

G. Katona, G. Szalay, P. Maák, A. Kaszás, M. Veress, D. Hillier, B. Chiovini, E. S. Vizi, B. Roska, and B. Rózsa, “Fast two-photon in vivo imaging with three-dimensional random-access scanning in large tissue volumes,” Nat. Methods 9(2), 201–208 (2012).
[Crossref] [PubMed]

E. Papagiakoumou, F. Anselmi, A. Bègue, V. de Sars, J. Glückstad, E. Y. Isacoff, and V. Emiliani, “Scanless two-photon excitation of channelrhodopsin-2,” Nat. Methods 7(10), 848–854 (2010).
[Crossref] [PubMed]

Nat. Photonics (1)

E. Papagiakoumou, A. Bègue, B. Leshem, O. Schwartz, B. M. Stell, J. Bradley, D. Oron, and V. Emiliani, “Functional patterned multiphoton excitation deep inside scattering tissue,” Nat. Photonics 7(4), 274–278 (2013).
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Nucleic Acids Res. (1)

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Supplementary Material (6)

NameDescription
» Visualization 1       Photoconversion of SYTO62
» Visualization 1       Photoconversion of SYTO62
» Visualization 2       Photoconversion of flowing cells in a microfluidic chip
» Visualization 2       Photoconversion of flowing cells in a microfluidic chip
» Visualization 3       Photoonversion of a circulating cell in vivo
» Visualization 3       Photoonversion of a circulating cell in vivo

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Figures (5)

Fig. 1
Fig. 1 Two-photon photoconversion kinetics of a SYTO62 dye. (a) Representative photoconversion of SYTO62 from red to green under two-photon excitation at 810 nm. The red ring around the converted area (lower image) is due to diffusion of the surrounding dye. (b) Quantification of conversion rate for different irradiance. The solid curve indicates the best-fit to a quadratic function and solid dashed lines indicate the equivalent-fluence lines.
Fig. 2
Fig. 2 Multiplexed photoconversion. (a) Multiplexed photoconversion of cultured HeLa cells stained with fast-converting SYTO62 (red to green) and slow-converting SYTO82 (red to blue). (b) Wavelength dependency of photoconversion rate.
Fig. 3
Fig. 3 Quantification of diffusion kinetics along axon fibers. (a) Schematic of the diffusion measurement along the axon fiber by photoconversion. (b) Representative time-series images of an axon before and after photoconversion. (c) Quantification of spatial profiles along the axon fibers over time. The dashed curves indicate the best-fit to the 1D diffusion equation (Eq. (1). (d) Measured diffusion coefficients from the axons and cerebrospinal fluid (CSF). *, P < 0.001.
Fig. 4
Fig. 4 Photoconversion of flowing cells in a microfluidic channel. (a) Schematic of photoconversion of flowing cells in a microfluidic channel. (b) Photoconversion of RBCs using full-field scanning. (c) Photoconversion of RBCs using a line-scan along the direction of flow. Cells flowing at 3.4 mm/s were photoconverted at 150 mW. (d) Photoconversion exposure time per RBC at 120, 150 and 210 mW, NA = 0.8. The line represents predicted exposure times based on previous spectroscopic data. f.f.: full-field scanning, l.s.: line-scanning. (e) Apparent conversion times for platelets, red blood cells (RBCs) and white blood cells (WBCs) plotted against peak laser irradiance. Lines represent predicted conversion times for full-field (f.f.) and line-scan (l.s.) methods.
Fig. 5
Fig. 5 Photoconversion of flowing cells in vivo. (a) Experimental scheme. An anesthetized mouse with a cranial window was intravenously injected with SYTO62 and studied under a two-photon microscopy. (b) A cortical vasculature imaged by two-photon fluorescence of SYTO62. Dotted white box is the cortical venue where photoconversion was observed. (c) Time-lapse images of photoconversion of a flowing WBC (indicated by an arrow) in vivo. Inset shows magnified image of the WBC. (d) A merged image showing leukocyte trajectory for annotated time points.

Tables (1)

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Table 1 Single-cell conversion times for photoconvertible cyanine-based fluorophores (the area of the cell is assumed to be 80 μm2).

Equations (8)

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c(x,t)= 1 2 c 0 (erf hx 2 Dt +erf h+x 2 Dt )
τp= k (1)
τ p 2 = k (2)
k (1) = k (2) /p
τ= k (2) ( I p fσ) 2 ×{duty cycle}
τ 3× 10 18 Jc m 2 I p 2
τ cell 3.7× 10 18 Jc m 2 I p 2 × cell area focal area
τ conversion τ cell ×{illumination efficiency}

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