Abstract

While laser scanning fluorescence lifetime imaging (FLIM) is a powerful approach for cell biology, its small field of view (typically less than 1 mm) makes it impractical for the imaging of large biological samples that is often required for biomedical applications. Here we present a system that allows performing FLIM on macroscopic samples as large as 18 mm with a lateral resolution of 15 μm. The performance of the system is verified with FLIM of endogenous metabolic cofactor reduced nicotinamide adenine dinucleotide (phosphate), NAD(P)H, and genetically encoded fluorescent protein mKate2 in a mouse tumor in vivo.

© 2018 Optical Society of America

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2017 (4)

M. Shirmanova, I. Druzhkova, M. Lukina, V. Dudenkova, N. Ignatova, L. Snopova, V. Shcheslavskiy, V. Belousov, and E. Zagaynova, Sci. Rep. 7, 8911, 2017.
[Crossref]

S. Alam, H. Wallrabe, Z. Svindrych, A. Chaudhary, K. Christopher, D. Chandra, and A. Periasamy, Sci. Rep. 7, 10451 (2017).
[Crossref]

M. Lukina, A. Orlova, M. Shirmanova, D. Shirokov, A. Pavlikov, A. Neubauer, H. Studier, W. Becker, E. Zagaynova, T. Yoshihara, S. Tobita, and V. Shcheslavskiy, Opt. Lett. 42, 731 (2017).
[Crossref]

T. Sergeeva, M. Shirmanova, O. Zlobovskaya, A. Gavrina, V. Dudenkova, M. Lukina, K. Lukyanov, and E. Zagaynova, Biochim. Biophys. Acta 1864, 604 (2017).
[Crossref]

2016 (4)

V. Shcheslavskiy, A. Neubauer, R. Bukowiecki, F. Dinter, and W. Becker, Appl. Phys. Lett. 108, 091111 (2016).
[Crossref]

S. Kalinina, J. Breymayer, P. Schäfer, E. Calzia, V. Shcheslavskiy, W. Becker, and A. Rück, J. Biophoton. 9, 800 (2016).
[Crossref]

O. Zlobovskaya, T. Sergeeva, M. Shirmanova, V. Dudenkova, G. Sharonov, E. Zagaynova, and K. Lukyanov, BioTechniques 60, 62 (2016).
[Crossref]

G. McConnel, J. Tragardh, R. Amor, J. Dempster, E. Reid, and W. Amos, eLife 5, e18659 (2016).
[Crossref]

2015 (1)

R. Hoffman, Lab. Invest. 95, 432 (2015).
[Crossref]

2014 (4)

T. Blacker, Z. Mann, J. Gale, M. Ziegler, A. Bain, G. Szabadkai, and M. Duchen, Nat. Commun. 5, 3936 (2014).
[Crossref]

T. Nakajima, K. Sano, K. Sato, R. Watanabe, T. Harada, H. Hanaoka, P. L. Choyke, and H. Kobayashi, Cancer Sci. 105, 308 (2014).
[Crossref]

K. Tainaka, S. I. Kubota, T. Q. Suyama, E. A. Susaki, D. Perrin, M. Tadenuma, H. Ukai, and H. Ueda, Cell 159, 911 (2014).
[Crossref]

A. Rueck, C. Hauser, S. Mosch, and S. Kalinina, J. Biomed. Opt. 19, 096005 (2014).
[Crossref]

2012 (1)

A. Miyawaki, D. M. Shcherbakova, and V. V. Verkhusha, Curr. Opin. Struct. Biol. 22, 679 (2012).
[Crossref]

2010 (3)

D. M. Chudakov, M. V. Matz, S. Lukyanov, and K. A. Lukyanov, Physiol. Rev. 90, 1103 (2010).
[Crossref]

A. Heikal, Biomark. Med. 4, 241 (2010).
[Crossref]

F. Leblond, S. C. Davis, P. A. Valdes, and B. W. Pogue, J. Photochem. Photobiol. B 98, 77 (2010).
[Crossref]

2008 (1)

I. V. Turchin, V. A. Kamensky, V. I. Plehanov, A. G. Orlova, M. S. Kleshnin, I. I. Fiks, M. V. Shirmanova, I. G. Meerovich, L. R. Arslanbaeva, V. V. Jerdeva, and A. P. Savitsky, J. Biomed. Opt. 13, 041310 (2008).
[Crossref]

2007 (2)

E. M. Hillman and A. Moore, Nat. Photonics 1, 526 (2007).
[Crossref]

M. C. Scala, K. M. Riching, A. Gendron-Fitzpatrick, J. Eickhoff, K. W. Eliceri, J. G. White, and N. Ramanujam, Proc. Natl. Acad. Sci. USA 104, 19494 (2007).
[Crossref]

2002 (1)

V. Ntziachristos, C. H. Tung, C. Bremer, and R. Weissleder, Nat. Med. 8, 757 (2002).
[Crossref]

2000 (1)

M. Yang, P. Jiang, F. Sun, X. Li, L. Li, S. Hasegawa, M. Bouvet, M. Tuwaijri, T. Chishima, H. Shimada, A. Moossa, S. Penman, and R. Hoffman, Proc. Natl. Acad. Sci. USA 97, 1206 (2000).
[Crossref]

1998 (1)

G. A. Wagniers, W. M. Star, and B. C. Wilson, Photochem. Photobiol. 68, 603 (1998).
[Crossref]

1992 (2)

H. Schneckenburger and K. Koenig, Opt. Eng. 31, 1447 (1992).
[Crossref]

J. Lakowicz, H. Szmacinski, K. Nowaczyk, and M. Johnson, Proc. Natl. Acad. Sci. USA 89, 1271 (1992).
[Crossref]

Alam, S.

S. Alam, H. Wallrabe, Z. Svindrych, A. Chaudhary, K. Christopher, D. Chandra, and A. Periasamy, Sci. Rep. 7, 10451 (2017).
[Crossref]

Amor, R.

G. McConnel, J. Tragardh, R. Amor, J. Dempster, E. Reid, and W. Amos, eLife 5, e18659 (2016).
[Crossref]

Amos, W.

G. McConnel, J. Tragardh, R. Amor, J. Dempster, E. Reid, and W. Amos, eLife 5, e18659 (2016).
[Crossref]

Arslanbaeva, L. R.

I. V. Turchin, V. A. Kamensky, V. I. Plehanov, A. G. Orlova, M. S. Kleshnin, I. I. Fiks, M. V. Shirmanova, I. G. Meerovich, L. R. Arslanbaeva, V. V. Jerdeva, and A. P. Savitsky, J. Biomed. Opt. 13, 041310 (2008).
[Crossref]

Bain, A.

T. Blacker, Z. Mann, J. Gale, M. Ziegler, A. Bain, G. Szabadkai, and M. Duchen, Nat. Commun. 5, 3936 (2014).
[Crossref]

Becker, W.

M. Lukina, A. Orlova, M. Shirmanova, D. Shirokov, A. Pavlikov, A. Neubauer, H. Studier, W. Becker, E. Zagaynova, T. Yoshihara, S. Tobita, and V. Shcheslavskiy, Opt. Lett. 42, 731 (2017).
[Crossref]

V. Shcheslavskiy, A. Neubauer, R. Bukowiecki, F. Dinter, and W. Becker, Appl. Phys. Lett. 108, 091111 (2016).
[Crossref]

S. Kalinina, J. Breymayer, P. Schäfer, E. Calzia, V. Shcheslavskiy, W. Becker, and A. Rück, J. Biophoton. 9, 800 (2016).
[Crossref]

W. Becker, The bh TCSPC Handbook, 7th ed. (2017).

W. Becker, Advanced Time-Correlated Single Photon Counting Applications (Springer, 2015).

Belousov, V.

M. Shirmanova, I. Druzhkova, M. Lukina, V. Dudenkova, N. Ignatova, L. Snopova, V. Shcheslavskiy, V. Belousov, and E. Zagaynova, Sci. Rep. 7, 8911, 2017.
[Crossref]

Blacker, T.

T. Blacker, Z. Mann, J. Gale, M. Ziegler, A. Bain, G. Szabadkai, and M. Duchen, Nat. Commun. 5, 3936 (2014).
[Crossref]

Bouvet, M.

M. Yang, P. Jiang, F. Sun, X. Li, L. Li, S. Hasegawa, M. Bouvet, M. Tuwaijri, T. Chishima, H. Shimada, A. Moossa, S. Penman, and R. Hoffman, Proc. Natl. Acad. Sci. USA 97, 1206 (2000).
[Crossref]

Bremer, C.

V. Ntziachristos, C. H. Tung, C. Bremer, and R. Weissleder, Nat. Med. 8, 757 (2002).
[Crossref]

Breymayer, J.

S. Kalinina, J. Breymayer, P. Schäfer, E. Calzia, V. Shcheslavskiy, W. Becker, and A. Rück, J. Biophoton. 9, 800 (2016).
[Crossref]

Bukowiecki, R.

V. Shcheslavskiy, A. Neubauer, R. Bukowiecki, F. Dinter, and W. Becker, Appl. Phys. Lett. 108, 091111 (2016).
[Crossref]

Calzia, E.

S. Kalinina, J. Breymayer, P. Schäfer, E. Calzia, V. Shcheslavskiy, W. Becker, and A. Rück, J. Biophoton. 9, 800 (2016).
[Crossref]

Chandra, D.

S. Alam, H. Wallrabe, Z. Svindrych, A. Chaudhary, K. Christopher, D. Chandra, and A. Periasamy, Sci. Rep. 7, 10451 (2017).
[Crossref]

Chaudhary, A.

S. Alam, H. Wallrabe, Z. Svindrych, A. Chaudhary, K. Christopher, D. Chandra, and A. Periasamy, Sci. Rep. 7, 10451 (2017).
[Crossref]

Chishima, T.

M. Yang, P. Jiang, F. Sun, X. Li, L. Li, S. Hasegawa, M. Bouvet, M. Tuwaijri, T. Chishima, H. Shimada, A. Moossa, S. Penman, and R. Hoffman, Proc. Natl. Acad. Sci. USA 97, 1206 (2000).
[Crossref]

Choyke, P. L.

T. Nakajima, K. Sano, K. Sato, R. Watanabe, T. Harada, H. Hanaoka, P. L. Choyke, and H. Kobayashi, Cancer Sci. 105, 308 (2014).
[Crossref]

Christopher, K.

S. Alam, H. Wallrabe, Z. Svindrych, A. Chaudhary, K. Christopher, D. Chandra, and A. Periasamy, Sci. Rep. 7, 10451 (2017).
[Crossref]

Chudakov, D. M.

D. M. Chudakov, M. V. Matz, S. Lukyanov, and K. A. Lukyanov, Physiol. Rev. 90, 1103 (2010).
[Crossref]

Davis, S. C.

F. Leblond, S. C. Davis, P. A. Valdes, and B. W. Pogue, J. Photochem. Photobiol. B 98, 77 (2010).
[Crossref]

Dempster, J.

G. McConnel, J. Tragardh, R. Amor, J. Dempster, E. Reid, and W. Amos, eLife 5, e18659 (2016).
[Crossref]

Dinter, F.

V. Shcheslavskiy, A. Neubauer, R. Bukowiecki, F. Dinter, and W. Becker, Appl. Phys. Lett. 108, 091111 (2016).
[Crossref]

Druzhkova, I.

M. Shirmanova, I. Druzhkova, M. Lukina, V. Dudenkova, N. Ignatova, L. Snopova, V. Shcheslavskiy, V. Belousov, and E. Zagaynova, Sci. Rep. 7, 8911, 2017.
[Crossref]

Duchen, M.

T. Blacker, Z. Mann, J. Gale, M. Ziegler, A. Bain, G. Szabadkai, and M. Duchen, Nat. Commun. 5, 3936 (2014).
[Crossref]

Dudenkova, V.

T. Sergeeva, M. Shirmanova, O. Zlobovskaya, A. Gavrina, V. Dudenkova, M. Lukina, K. Lukyanov, and E. Zagaynova, Biochim. Biophys. Acta 1864, 604 (2017).
[Crossref]

M. Shirmanova, I. Druzhkova, M. Lukina, V. Dudenkova, N. Ignatova, L. Snopova, V. Shcheslavskiy, V. Belousov, and E. Zagaynova, Sci. Rep. 7, 8911, 2017.
[Crossref]

O. Zlobovskaya, T. Sergeeva, M. Shirmanova, V. Dudenkova, G. Sharonov, E. Zagaynova, and K. Lukyanov, BioTechniques 60, 62 (2016).
[Crossref]

Eickhoff, J.

M. C. Scala, K. M. Riching, A. Gendron-Fitzpatrick, J. Eickhoff, K. W. Eliceri, J. G. White, and N. Ramanujam, Proc. Natl. Acad. Sci. USA 104, 19494 (2007).
[Crossref]

Eliceri, K. W.

M. C. Scala, K. M. Riching, A. Gendron-Fitzpatrick, J. Eickhoff, K. W. Eliceri, J. G. White, and N. Ramanujam, Proc. Natl. Acad. Sci. USA 104, 19494 (2007).
[Crossref]

Fiks, I. I.

I. V. Turchin, V. A. Kamensky, V. I. Plehanov, A. G. Orlova, M. S. Kleshnin, I. I. Fiks, M. V. Shirmanova, I. G. Meerovich, L. R. Arslanbaeva, V. V. Jerdeva, and A. P. Savitsky, J. Biomed. Opt. 13, 041310 (2008).
[Crossref]

Gale, J.

T. Blacker, Z. Mann, J. Gale, M. Ziegler, A. Bain, G. Szabadkai, and M. Duchen, Nat. Commun. 5, 3936 (2014).
[Crossref]

Gavrina, A.

T. Sergeeva, M. Shirmanova, O. Zlobovskaya, A. Gavrina, V. Dudenkova, M. Lukina, K. Lukyanov, and E. Zagaynova, Biochim. Biophys. Acta 1864, 604 (2017).
[Crossref]

Gendron-Fitzpatrick, A.

M. C. Scala, K. M. Riching, A. Gendron-Fitzpatrick, J. Eickhoff, K. W. Eliceri, J. G. White, and N. Ramanujam, Proc. Natl. Acad. Sci. USA 104, 19494 (2007).
[Crossref]

Hanaoka, H.

T. Nakajima, K. Sano, K. Sato, R. Watanabe, T. Harada, H. Hanaoka, P. L. Choyke, and H. Kobayashi, Cancer Sci. 105, 308 (2014).
[Crossref]

Harada, T.

T. Nakajima, K. Sano, K. Sato, R. Watanabe, T. Harada, H. Hanaoka, P. L. Choyke, and H. Kobayashi, Cancer Sci. 105, 308 (2014).
[Crossref]

Hasegawa, S.

M. Yang, P. Jiang, F. Sun, X. Li, L. Li, S. Hasegawa, M. Bouvet, M. Tuwaijri, T. Chishima, H. Shimada, A. Moossa, S. Penman, and R. Hoffman, Proc. Natl. Acad. Sci. USA 97, 1206 (2000).
[Crossref]

Hauser, C.

A. Rueck, C. Hauser, S. Mosch, and S. Kalinina, J. Biomed. Opt. 19, 096005 (2014).
[Crossref]

Heikal, A.

A. Heikal, Biomark. Med. 4, 241 (2010).
[Crossref]

Hillman, E. M.

E. M. Hillman and A. Moore, Nat. Photonics 1, 526 (2007).
[Crossref]

Hoffman, R.

R. Hoffman, Lab. Invest. 95, 432 (2015).
[Crossref]

M. Yang, P. Jiang, F. Sun, X. Li, L. Li, S. Hasegawa, M. Bouvet, M. Tuwaijri, T. Chishima, H. Shimada, A. Moossa, S. Penman, and R. Hoffman, Proc. Natl. Acad. Sci. USA 97, 1206 (2000).
[Crossref]

Ignatova, N.

M. Shirmanova, I. Druzhkova, M. Lukina, V. Dudenkova, N. Ignatova, L. Snopova, V. Shcheslavskiy, V. Belousov, and E. Zagaynova, Sci. Rep. 7, 8911, 2017.
[Crossref]

Jerdeva, V. V.

I. V. Turchin, V. A. Kamensky, V. I. Plehanov, A. G. Orlova, M. S. Kleshnin, I. I. Fiks, M. V. Shirmanova, I. G. Meerovich, L. R. Arslanbaeva, V. V. Jerdeva, and A. P. Savitsky, J. Biomed. Opt. 13, 041310 (2008).
[Crossref]

Jiang, P.

M. Yang, P. Jiang, F. Sun, X. Li, L. Li, S. Hasegawa, M. Bouvet, M. Tuwaijri, T. Chishima, H. Shimada, A. Moossa, S. Penman, and R. Hoffman, Proc. Natl. Acad. Sci. USA 97, 1206 (2000).
[Crossref]

Johnson, M.

J. Lakowicz, H. Szmacinski, K. Nowaczyk, and M. Johnson, Proc. Natl. Acad. Sci. USA 89, 1271 (1992).
[Crossref]

Kalinina, S.

S. Kalinina, J. Breymayer, P. Schäfer, E. Calzia, V. Shcheslavskiy, W. Becker, and A. Rück, J. Biophoton. 9, 800 (2016).
[Crossref]

A. Rueck, C. Hauser, S. Mosch, and S. Kalinina, J. Biomed. Opt. 19, 096005 (2014).
[Crossref]

Kamensky, V. A.

I. V. Turchin, V. A. Kamensky, V. I. Plehanov, A. G. Orlova, M. S. Kleshnin, I. I. Fiks, M. V. Shirmanova, I. G. Meerovich, L. R. Arslanbaeva, V. V. Jerdeva, and A. P. Savitsky, J. Biomed. Opt. 13, 041310 (2008).
[Crossref]

Kleshnin, M. S.

I. V. Turchin, V. A. Kamensky, V. I. Plehanov, A. G. Orlova, M. S. Kleshnin, I. I. Fiks, M. V. Shirmanova, I. G. Meerovich, L. R. Arslanbaeva, V. V. Jerdeva, and A. P. Savitsky, J. Biomed. Opt. 13, 041310 (2008).
[Crossref]

Kobayashi, H.

T. Nakajima, K. Sano, K. Sato, R. Watanabe, T. Harada, H. Hanaoka, P. L. Choyke, and H. Kobayashi, Cancer Sci. 105, 308 (2014).
[Crossref]

Koenig, K.

H. Schneckenburger and K. Koenig, Opt. Eng. 31, 1447 (1992).
[Crossref]

Kubota, S. I.

K. Tainaka, S. I. Kubota, T. Q. Suyama, E. A. Susaki, D. Perrin, M. Tadenuma, H. Ukai, and H. Ueda, Cell 159, 911 (2014).
[Crossref]

Lakowicz, J.

J. Lakowicz, H. Szmacinski, K. Nowaczyk, and M. Johnson, Proc. Natl. Acad. Sci. USA 89, 1271 (1992).
[Crossref]

Leblond, F.

F. Leblond, S. C. Davis, P. A. Valdes, and B. W. Pogue, J. Photochem. Photobiol. B 98, 77 (2010).
[Crossref]

Li, L.

M. Yang, P. Jiang, F. Sun, X. Li, L. Li, S. Hasegawa, M. Bouvet, M. Tuwaijri, T. Chishima, H. Shimada, A. Moossa, S. Penman, and R. Hoffman, Proc. Natl. Acad. Sci. USA 97, 1206 (2000).
[Crossref]

Li, X.

M. Yang, P. Jiang, F. Sun, X. Li, L. Li, S. Hasegawa, M. Bouvet, M. Tuwaijri, T. Chishima, H. Shimada, A. Moossa, S. Penman, and R. Hoffman, Proc. Natl. Acad. Sci. USA 97, 1206 (2000).
[Crossref]

Lukina, M.

M. Lukina, A. Orlova, M. Shirmanova, D. Shirokov, A. Pavlikov, A. Neubauer, H. Studier, W. Becker, E. Zagaynova, T. Yoshihara, S. Tobita, and V. Shcheslavskiy, Opt. Lett. 42, 731 (2017).
[Crossref]

T. Sergeeva, M. Shirmanova, O. Zlobovskaya, A. Gavrina, V. Dudenkova, M. Lukina, K. Lukyanov, and E. Zagaynova, Biochim. Biophys. Acta 1864, 604 (2017).
[Crossref]

M. Shirmanova, I. Druzhkova, M. Lukina, V. Dudenkova, N. Ignatova, L. Snopova, V. Shcheslavskiy, V. Belousov, and E. Zagaynova, Sci. Rep. 7, 8911, 2017.
[Crossref]

Lukyanov, K.

T. Sergeeva, M. Shirmanova, O. Zlobovskaya, A. Gavrina, V. Dudenkova, M. Lukina, K. Lukyanov, and E. Zagaynova, Biochim. Biophys. Acta 1864, 604 (2017).
[Crossref]

O. Zlobovskaya, T. Sergeeva, M. Shirmanova, V. Dudenkova, G. Sharonov, E. Zagaynova, and K. Lukyanov, BioTechniques 60, 62 (2016).
[Crossref]

Lukyanov, K. A.

D. M. Chudakov, M. V. Matz, S. Lukyanov, and K. A. Lukyanov, Physiol. Rev. 90, 1103 (2010).
[Crossref]

Lukyanov, S.

D. M. Chudakov, M. V. Matz, S. Lukyanov, and K. A. Lukyanov, Physiol. Rev. 90, 1103 (2010).
[Crossref]

Mann, Z.

T. Blacker, Z. Mann, J. Gale, M. Ziegler, A. Bain, G. Szabadkai, and M. Duchen, Nat. Commun. 5, 3936 (2014).
[Crossref]

Matz, M. V.

D. M. Chudakov, M. V. Matz, S. Lukyanov, and K. A. Lukyanov, Physiol. Rev. 90, 1103 (2010).
[Crossref]

McConnel, G.

G. McConnel, J. Tragardh, R. Amor, J. Dempster, E. Reid, and W. Amos, eLife 5, e18659 (2016).
[Crossref]

Meerovich, I. G.

I. V. Turchin, V. A. Kamensky, V. I. Plehanov, A. G. Orlova, M. S. Kleshnin, I. I. Fiks, M. V. Shirmanova, I. G. Meerovich, L. R. Arslanbaeva, V. V. Jerdeva, and A. P. Savitsky, J. Biomed. Opt. 13, 041310 (2008).
[Crossref]

Miyawaki, A.

A. Miyawaki, D. M. Shcherbakova, and V. V. Verkhusha, Curr. Opin. Struct. Biol. 22, 679 (2012).
[Crossref]

Moore, A.

E. M. Hillman and A. Moore, Nat. Photonics 1, 526 (2007).
[Crossref]

Moossa, A.

M. Yang, P. Jiang, F. Sun, X. Li, L. Li, S. Hasegawa, M. Bouvet, M. Tuwaijri, T. Chishima, H. Shimada, A. Moossa, S. Penman, and R. Hoffman, Proc. Natl. Acad. Sci. USA 97, 1206 (2000).
[Crossref]

Mosch, S.

A. Rueck, C. Hauser, S. Mosch, and S. Kalinina, J. Biomed. Opt. 19, 096005 (2014).
[Crossref]

Nakajima, T.

T. Nakajima, K. Sano, K. Sato, R. Watanabe, T. Harada, H. Hanaoka, P. L. Choyke, and H. Kobayashi, Cancer Sci. 105, 308 (2014).
[Crossref]

Neubauer, A.

Nowaczyk, K.

J. Lakowicz, H. Szmacinski, K. Nowaczyk, and M. Johnson, Proc. Natl. Acad. Sci. USA 89, 1271 (1992).
[Crossref]

Ntziachristos, V.

V. Ntziachristos, C. H. Tung, C. Bremer, and R. Weissleder, Nat. Med. 8, 757 (2002).
[Crossref]

Orlova, A.

Orlova, A. G.

I. V. Turchin, V. A. Kamensky, V. I. Plehanov, A. G. Orlova, M. S. Kleshnin, I. I. Fiks, M. V. Shirmanova, I. G. Meerovich, L. R. Arslanbaeva, V. V. Jerdeva, and A. P. Savitsky, J. Biomed. Opt. 13, 041310 (2008).
[Crossref]

Pavlikov, A.

Penman, S.

M. Yang, P. Jiang, F. Sun, X. Li, L. Li, S. Hasegawa, M. Bouvet, M. Tuwaijri, T. Chishima, H. Shimada, A. Moossa, S. Penman, and R. Hoffman, Proc. Natl. Acad. Sci. USA 97, 1206 (2000).
[Crossref]

Periasamy, A.

S. Alam, H. Wallrabe, Z. Svindrych, A. Chaudhary, K. Christopher, D. Chandra, and A. Periasamy, Sci. Rep. 7, 10451 (2017).
[Crossref]

Perrin, D.

K. Tainaka, S. I. Kubota, T. Q. Suyama, E. A. Susaki, D. Perrin, M. Tadenuma, H. Ukai, and H. Ueda, Cell 159, 911 (2014).
[Crossref]

Plehanov, V. I.

I. V. Turchin, V. A. Kamensky, V. I. Plehanov, A. G. Orlova, M. S. Kleshnin, I. I. Fiks, M. V. Shirmanova, I. G. Meerovich, L. R. Arslanbaeva, V. V. Jerdeva, and A. P. Savitsky, J. Biomed. Opt. 13, 041310 (2008).
[Crossref]

Pogue, B. W.

F. Leblond, S. C. Davis, P. A. Valdes, and B. W. Pogue, J. Photochem. Photobiol. B 98, 77 (2010).
[Crossref]

Ramanujam, N.

M. C. Scala, K. M. Riching, A. Gendron-Fitzpatrick, J. Eickhoff, K. W. Eliceri, J. G. White, and N. Ramanujam, Proc. Natl. Acad. Sci. USA 104, 19494 (2007).
[Crossref]

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G. McConnel, J. Tragardh, R. Amor, J. Dempster, E. Reid, and W. Amos, eLife 5, e18659 (2016).
[Crossref]

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M. C. Scala, K. M. Riching, A. Gendron-Fitzpatrick, J. Eickhoff, K. W. Eliceri, J. G. White, and N. Ramanujam, Proc. Natl. Acad. Sci. USA 104, 19494 (2007).
[Crossref]

Rück, A.

S. Kalinina, J. Breymayer, P. Schäfer, E. Calzia, V. Shcheslavskiy, W. Becker, and A. Rück, J. Biophoton. 9, 800 (2016).
[Crossref]

Rueck, A.

A. Rueck, C. Hauser, S. Mosch, and S. Kalinina, J. Biomed. Opt. 19, 096005 (2014).
[Crossref]

Sano, K.

T. Nakajima, K. Sano, K. Sato, R. Watanabe, T. Harada, H. Hanaoka, P. L. Choyke, and H. Kobayashi, Cancer Sci. 105, 308 (2014).
[Crossref]

Sato, K.

T. Nakajima, K. Sano, K. Sato, R. Watanabe, T. Harada, H. Hanaoka, P. L. Choyke, and H. Kobayashi, Cancer Sci. 105, 308 (2014).
[Crossref]

Savitsky, A. P.

I. V. Turchin, V. A. Kamensky, V. I. Plehanov, A. G. Orlova, M. S. Kleshnin, I. I. Fiks, M. V. Shirmanova, I. G. Meerovich, L. R. Arslanbaeva, V. V. Jerdeva, and A. P. Savitsky, J. Biomed. Opt. 13, 041310 (2008).
[Crossref]

Scala, M. C.

M. C. Scala, K. M. Riching, A. Gendron-Fitzpatrick, J. Eickhoff, K. W. Eliceri, J. G. White, and N. Ramanujam, Proc. Natl. Acad. Sci. USA 104, 19494 (2007).
[Crossref]

Schäfer, P.

S. Kalinina, J. Breymayer, P. Schäfer, E. Calzia, V. Shcheslavskiy, W. Becker, and A. Rück, J. Biophoton. 9, 800 (2016).
[Crossref]

Schneckenburger, H.

H. Schneckenburger and K. Koenig, Opt. Eng. 31, 1447 (1992).
[Crossref]

Sergeeva, T.

T. Sergeeva, M. Shirmanova, O. Zlobovskaya, A. Gavrina, V. Dudenkova, M. Lukina, K. Lukyanov, and E. Zagaynova, Biochim. Biophys. Acta 1864, 604 (2017).
[Crossref]

O. Zlobovskaya, T. Sergeeva, M. Shirmanova, V. Dudenkova, G. Sharonov, E. Zagaynova, and K. Lukyanov, BioTechniques 60, 62 (2016).
[Crossref]

Sharonov, G.

O. Zlobovskaya, T. Sergeeva, M. Shirmanova, V. Dudenkova, G. Sharonov, E. Zagaynova, and K. Lukyanov, BioTechniques 60, 62 (2016).
[Crossref]

Shcherbakova, D. M.

A. Miyawaki, D. M. Shcherbakova, and V. V. Verkhusha, Curr. Opin. Struct. Biol. 22, 679 (2012).
[Crossref]

Shcheslavskiy, V.

M. Shirmanova, I. Druzhkova, M. Lukina, V. Dudenkova, N. Ignatova, L. Snopova, V. Shcheslavskiy, V. Belousov, and E. Zagaynova, Sci. Rep. 7, 8911, 2017.
[Crossref]

M. Lukina, A. Orlova, M. Shirmanova, D. Shirokov, A. Pavlikov, A. Neubauer, H. Studier, W. Becker, E. Zagaynova, T. Yoshihara, S. Tobita, and V. Shcheslavskiy, Opt. Lett. 42, 731 (2017).
[Crossref]

V. Shcheslavskiy, A. Neubauer, R. Bukowiecki, F. Dinter, and W. Becker, Appl. Phys. Lett. 108, 091111 (2016).
[Crossref]

S. Kalinina, J. Breymayer, P. Schäfer, E. Calzia, V. Shcheslavskiy, W. Becker, and A. Rück, J. Biophoton. 9, 800 (2016).
[Crossref]

Shimada, H.

M. Yang, P. Jiang, F. Sun, X. Li, L. Li, S. Hasegawa, M. Bouvet, M. Tuwaijri, T. Chishima, H. Shimada, A. Moossa, S. Penman, and R. Hoffman, Proc. Natl. Acad. Sci. USA 97, 1206 (2000).
[Crossref]

Shirmanova, M.

T. Sergeeva, M. Shirmanova, O. Zlobovskaya, A. Gavrina, V. Dudenkova, M. Lukina, K. Lukyanov, and E. Zagaynova, Biochim. Biophys. Acta 1864, 604 (2017).
[Crossref]

M. Lukina, A. Orlova, M. Shirmanova, D. Shirokov, A. Pavlikov, A. Neubauer, H. Studier, W. Becker, E. Zagaynova, T. Yoshihara, S. Tobita, and V. Shcheslavskiy, Opt. Lett. 42, 731 (2017).
[Crossref]

M. Shirmanova, I. Druzhkova, M. Lukina, V. Dudenkova, N. Ignatova, L. Snopova, V. Shcheslavskiy, V. Belousov, and E. Zagaynova, Sci. Rep. 7, 8911, 2017.
[Crossref]

O. Zlobovskaya, T. Sergeeva, M. Shirmanova, V. Dudenkova, G. Sharonov, E. Zagaynova, and K. Lukyanov, BioTechniques 60, 62 (2016).
[Crossref]

Shirmanova, M. V.

I. V. Turchin, V. A. Kamensky, V. I. Plehanov, A. G. Orlova, M. S. Kleshnin, I. I. Fiks, M. V. Shirmanova, I. G. Meerovich, L. R. Arslanbaeva, V. V. Jerdeva, and A. P. Savitsky, J. Biomed. Opt. 13, 041310 (2008).
[Crossref]

Shirokov, D.

Snopova, L.

M. Shirmanova, I. Druzhkova, M. Lukina, V. Dudenkova, N. Ignatova, L. Snopova, V. Shcheslavskiy, V. Belousov, and E. Zagaynova, Sci. Rep. 7, 8911, 2017.
[Crossref]

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G. A. Wagniers, W. M. Star, and B. C. Wilson, Photochem. Photobiol. 68, 603 (1998).
[Crossref]

Studier, H.

Sun, F.

M. Yang, P. Jiang, F. Sun, X. Li, L. Li, S. Hasegawa, M. Bouvet, M. Tuwaijri, T. Chishima, H. Shimada, A. Moossa, S. Penman, and R. Hoffman, Proc. Natl. Acad. Sci. USA 97, 1206 (2000).
[Crossref]

Susaki, E. A.

K. Tainaka, S. I. Kubota, T. Q. Suyama, E. A. Susaki, D. Perrin, M. Tadenuma, H. Ukai, and H. Ueda, Cell 159, 911 (2014).
[Crossref]

Suyama, T. Q.

K. Tainaka, S. I. Kubota, T. Q. Suyama, E. A. Susaki, D. Perrin, M. Tadenuma, H. Ukai, and H. Ueda, Cell 159, 911 (2014).
[Crossref]

Svindrych, Z.

S. Alam, H. Wallrabe, Z. Svindrych, A. Chaudhary, K. Christopher, D. Chandra, and A. Periasamy, Sci. Rep. 7, 10451 (2017).
[Crossref]

Szabadkai, G.

T. Blacker, Z. Mann, J. Gale, M. Ziegler, A. Bain, G. Szabadkai, and M. Duchen, Nat. Commun. 5, 3936 (2014).
[Crossref]

Szmacinski, H.

J. Lakowicz, H. Szmacinski, K. Nowaczyk, and M. Johnson, Proc. Natl. Acad. Sci. USA 89, 1271 (1992).
[Crossref]

Tadenuma, M.

K. Tainaka, S. I. Kubota, T. Q. Suyama, E. A. Susaki, D. Perrin, M. Tadenuma, H. Ukai, and H. Ueda, Cell 159, 911 (2014).
[Crossref]

Tainaka, K.

K. Tainaka, S. I. Kubota, T. Q. Suyama, E. A. Susaki, D. Perrin, M. Tadenuma, H. Ukai, and H. Ueda, Cell 159, 911 (2014).
[Crossref]

Tobita, S.

Tragardh, J.

G. McConnel, J. Tragardh, R. Amor, J. Dempster, E. Reid, and W. Amos, eLife 5, e18659 (2016).
[Crossref]

Tung, C. H.

V. Ntziachristos, C. H. Tung, C. Bremer, and R. Weissleder, Nat. Med. 8, 757 (2002).
[Crossref]

Turchin, I. V.

I. V. Turchin, V. A. Kamensky, V. I. Plehanov, A. G. Orlova, M. S. Kleshnin, I. I. Fiks, M. V. Shirmanova, I. G. Meerovich, L. R. Arslanbaeva, V. V. Jerdeva, and A. P. Savitsky, J. Biomed. Opt. 13, 041310 (2008).
[Crossref]

Tuwaijri, M.

M. Yang, P. Jiang, F. Sun, X. Li, L. Li, S. Hasegawa, M. Bouvet, M. Tuwaijri, T. Chishima, H. Shimada, A. Moossa, S. Penman, and R. Hoffman, Proc. Natl. Acad. Sci. USA 97, 1206 (2000).
[Crossref]

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K. Tainaka, S. I. Kubota, T. Q. Suyama, E. A. Susaki, D. Perrin, M. Tadenuma, H. Ukai, and H. Ueda, Cell 159, 911 (2014).
[Crossref]

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K. Tainaka, S. I. Kubota, T. Q. Suyama, E. A. Susaki, D. Perrin, M. Tadenuma, H. Ukai, and H. Ueda, Cell 159, 911 (2014).
[Crossref]

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F. Leblond, S. C. Davis, P. A. Valdes, and B. W. Pogue, J. Photochem. Photobiol. B 98, 77 (2010).
[Crossref]

Verkhusha, V. V.

A. Miyawaki, D. M. Shcherbakova, and V. V. Verkhusha, Curr. Opin. Struct. Biol. 22, 679 (2012).
[Crossref]

Wagniers, G. A.

G. A. Wagniers, W. M. Star, and B. C. Wilson, Photochem. Photobiol. 68, 603 (1998).
[Crossref]

Wallrabe, H.

S. Alam, H. Wallrabe, Z. Svindrych, A. Chaudhary, K. Christopher, D. Chandra, and A. Periasamy, Sci. Rep. 7, 10451 (2017).
[Crossref]

Watanabe, R.

T. Nakajima, K. Sano, K. Sato, R. Watanabe, T. Harada, H. Hanaoka, P. L. Choyke, and H. Kobayashi, Cancer Sci. 105, 308 (2014).
[Crossref]

Weissleder, R.

V. Ntziachristos, C. H. Tung, C. Bremer, and R. Weissleder, Nat. Med. 8, 757 (2002).
[Crossref]

White, J. G.

M. C. Scala, K. M. Riching, A. Gendron-Fitzpatrick, J. Eickhoff, K. W. Eliceri, J. G. White, and N. Ramanujam, Proc. Natl. Acad. Sci. USA 104, 19494 (2007).
[Crossref]

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G. A. Wagniers, W. M. Star, and B. C. Wilson, Photochem. Photobiol. 68, 603 (1998).
[Crossref]

Yang, M.

M. Yang, P. Jiang, F. Sun, X. Li, L. Li, S. Hasegawa, M. Bouvet, M. Tuwaijri, T. Chishima, H. Shimada, A. Moossa, S. Penman, and R. Hoffman, Proc. Natl. Acad. Sci. USA 97, 1206 (2000).
[Crossref]

Yoshihara, T.

Zagaynova, E.

M. Lukina, A. Orlova, M. Shirmanova, D. Shirokov, A. Pavlikov, A. Neubauer, H. Studier, W. Becker, E. Zagaynova, T. Yoshihara, S. Tobita, and V. Shcheslavskiy, Opt. Lett. 42, 731 (2017).
[Crossref]

M. Shirmanova, I. Druzhkova, M. Lukina, V. Dudenkova, N. Ignatova, L. Snopova, V. Shcheslavskiy, V. Belousov, and E. Zagaynova, Sci. Rep. 7, 8911, 2017.
[Crossref]

T. Sergeeva, M. Shirmanova, O. Zlobovskaya, A. Gavrina, V. Dudenkova, M. Lukina, K. Lukyanov, and E. Zagaynova, Biochim. Biophys. Acta 1864, 604 (2017).
[Crossref]

O. Zlobovskaya, T. Sergeeva, M. Shirmanova, V. Dudenkova, G. Sharonov, E. Zagaynova, and K. Lukyanov, BioTechniques 60, 62 (2016).
[Crossref]

Ziegler, M.

T. Blacker, Z. Mann, J. Gale, M. Ziegler, A. Bain, G. Szabadkai, and M. Duchen, Nat. Commun. 5, 3936 (2014).
[Crossref]

Zlobovskaya, O.

T. Sergeeva, M. Shirmanova, O. Zlobovskaya, A. Gavrina, V. Dudenkova, M. Lukina, K. Lukyanov, and E. Zagaynova, Biochim. Biophys. Acta 1864, 604 (2017).
[Crossref]

O. Zlobovskaya, T. Sergeeva, M. Shirmanova, V. Dudenkova, G. Sharonov, E. Zagaynova, and K. Lukyanov, BioTechniques 60, 62 (2016).
[Crossref]

Appl. Phys. Lett. (1)

V. Shcheslavskiy, A. Neubauer, R. Bukowiecki, F. Dinter, and W. Becker, Appl. Phys. Lett. 108, 091111 (2016).
[Crossref]

Biochim. Biophys. Acta (1)

T. Sergeeva, M. Shirmanova, O. Zlobovskaya, A. Gavrina, V. Dudenkova, M. Lukina, K. Lukyanov, and E. Zagaynova, Biochim. Biophys. Acta 1864, 604 (2017).
[Crossref]

Biomark. Med. (1)

A. Heikal, Biomark. Med. 4, 241 (2010).
[Crossref]

BioTechniques (1)

O. Zlobovskaya, T. Sergeeva, M. Shirmanova, V. Dudenkova, G. Sharonov, E. Zagaynova, and K. Lukyanov, BioTechniques 60, 62 (2016).
[Crossref]

Cancer Sci. (1)

T. Nakajima, K. Sano, K. Sato, R. Watanabe, T. Harada, H. Hanaoka, P. L. Choyke, and H. Kobayashi, Cancer Sci. 105, 308 (2014).
[Crossref]

Cell (1)

K. Tainaka, S. I. Kubota, T. Q. Suyama, E. A. Susaki, D. Perrin, M. Tadenuma, H. Ukai, and H. Ueda, Cell 159, 911 (2014).
[Crossref]

Curr. Opin. Struct. Biol. (1)

A. Miyawaki, D. M. Shcherbakova, and V. V. Verkhusha, Curr. Opin. Struct. Biol. 22, 679 (2012).
[Crossref]

eLife (1)

G. McConnel, J. Tragardh, R. Amor, J. Dempster, E. Reid, and W. Amos, eLife 5, e18659 (2016).
[Crossref]

J. Biomed. Opt. (2)

I. V. Turchin, V. A. Kamensky, V. I. Plehanov, A. G. Orlova, M. S. Kleshnin, I. I. Fiks, M. V. Shirmanova, I. G. Meerovich, L. R. Arslanbaeva, V. V. Jerdeva, and A. P. Savitsky, J. Biomed. Opt. 13, 041310 (2008).
[Crossref]

A. Rueck, C. Hauser, S. Mosch, and S. Kalinina, J. Biomed. Opt. 19, 096005 (2014).
[Crossref]

J. Biophoton. (1)

S. Kalinina, J. Breymayer, P. Schäfer, E. Calzia, V. Shcheslavskiy, W. Becker, and A. Rück, J. Biophoton. 9, 800 (2016).
[Crossref]

J. Photochem. Photobiol. B (1)

F. Leblond, S. C. Davis, P. A. Valdes, and B. W. Pogue, J. Photochem. Photobiol. B 98, 77 (2010).
[Crossref]

Lab. Invest. (1)

R. Hoffman, Lab. Invest. 95, 432 (2015).
[Crossref]

Nat. Commun. (1)

T. Blacker, Z. Mann, J. Gale, M. Ziegler, A. Bain, G. Szabadkai, and M. Duchen, Nat. Commun. 5, 3936 (2014).
[Crossref]

Nat. Med. (1)

V. Ntziachristos, C. H. Tung, C. Bremer, and R. Weissleder, Nat. Med. 8, 757 (2002).
[Crossref]

Nat. Photonics (1)

E. M. Hillman and A. Moore, Nat. Photonics 1, 526 (2007).
[Crossref]

Opt. Eng. (1)

H. Schneckenburger and K. Koenig, Opt. Eng. 31, 1447 (1992).
[Crossref]

Opt. Lett. (1)

Photochem. Photobiol. (1)

G. A. Wagniers, W. M. Star, and B. C. Wilson, Photochem. Photobiol. 68, 603 (1998).
[Crossref]

Physiol. Rev. (1)

D. M. Chudakov, M. V. Matz, S. Lukyanov, and K. A. Lukyanov, Physiol. Rev. 90, 1103 (2010).
[Crossref]

Proc. Natl. Acad. Sci. USA (3)

M. Yang, P. Jiang, F. Sun, X. Li, L. Li, S. Hasegawa, M. Bouvet, M. Tuwaijri, T. Chishima, H. Shimada, A. Moossa, S. Penman, and R. Hoffman, Proc. Natl. Acad. Sci. USA 97, 1206 (2000).
[Crossref]

J. Lakowicz, H. Szmacinski, K. Nowaczyk, and M. Johnson, Proc. Natl. Acad. Sci. USA 89, 1271 (1992).
[Crossref]

M. C. Scala, K. M. Riching, A. Gendron-Fitzpatrick, J. Eickhoff, K. W. Eliceri, J. G. White, and N. Ramanujam, Proc. Natl. Acad. Sci. USA 104, 19494 (2007).
[Crossref]

Sci. Rep. (2)

M. Shirmanova, I. Druzhkova, M. Lukina, V. Dudenkova, N. Ignatova, L. Snopova, V. Shcheslavskiy, V. Belousov, and E. Zagaynova, Sci. Rep. 7, 8911, 2017.
[Crossref]

S. Alam, H. Wallrabe, Z. Svindrych, A. Chaudhary, K. Christopher, D. Chandra, and A. Periasamy, Sci. Rep. 7, 10451 (2017).
[Crossref]

Other (2)

W. Becker, The bh TCSPC Handbook, 7th ed. (2017).

W. Becker, Advanced Time-Correlated Single Photon Counting Applications (Springer, 2015).

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Figures (3)

Fig. 1.
Fig. 1. (a) Schematic of DCS-120 scanner for imaging macroscopic objects. BC: beam combiner (442bcm, Chroma, USA), MDM: main dichroic mirror (z 405/488/594); GM, galvanometric mirrors; SL, scanning lens (f=40  mm); IP, image plane; S, sample; A, pinhole: F1 and F2: longpass HQ435 and bandpass ET460/50 filters; F3 and F4: longpass ET 610 and bandpass ET 645/75 filters, respectively. (b) Fluorescence image of beads (diameter 14.6 μm) (c) Fluorescence image of cancer cells labeled with Calcein AM on a glass-bottom dish. Excitation: 488 nm, detection: 500–550 nm. Scale bar: 100 μm. Collection time: 10 s.
Fig. 2.
Fig. 2. (a) Fluorescence time-resolved image of NAD(P)H in a tumor. τm is an amplitude weighted fluorescence lifetime, and the borders of the tumor are marked with a white line. (b) Color-coded image of the ratio of free (a1) and bound (a2) NAD(P)H; red: 1.0–3.5, green: 3.5–5.5, blue: 5.5–7. (c) Fluorescence decay curve of NAD(P)H in the selected spot marked with red square in muscle: bi-exponential fit (red curve); instrument response function (green curve). Scale bar: 2 mm. Collection time: 90 s. (d) Same as in (c) but in tumor.
Fig. 3.
Fig. 3. FLIM of tumors labeled with (a) mKate2-DEVD-iRFP or (b) mKate2; (c) and (d) fluorescence decay profiles of mKate2 in the selected spots marked with red color, corresponding to the figures (a) and (b), respectively. Monoexponential fit (red curve); instrument response function (green curve). Scale bar: 2 mm. Collection time: 10 s. Tumor in (a) is the same as in Fig. 2.