Abstract

The two-photon excitation action cross section of Hc-Red fluorescent proteins (Hc-RFPs) is measured and found to be of the same order as that of enhanced green fluorescent proteins. With a 618 nm emission wavelength in the far-red region and with an excitation wavelength around 1200 nm, Hc-RPF-based two-photon fluorescence microscopy (2PFM) can offer deep penetration capability inside live samples and is ideal for in vivo gene expression study and biomolecular imaging in live objects. In vivo 2PFM of the developing heart deep inside a transgenic zebrafish embryo tagged by Hc-RFP is also successfully demonstrated.

© 2006 Optical Society of America

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M. F. Yanik, H. Cinar, H. N. Cinar, A. D. Chisholm, Y. Jin, and A. Bem-Yakar, Nature 432, 822 (2004).
[CrossRef] [PubMed]

C.-K. Sun, S.-W. Chu, S.-Y. Chen, T.-H. Tsai, T.-M. Liu, C.-Y. Lin, and H.-J. Tsai, J. Struct. Biol. 147, 19 (2004).
[CrossRef] [PubMed]

2003 (3)

C.-J. Huang, C.-T. Tu, C.-D. Hsiao, F.-J. Hsieh, and H.-J. Tsai, Dev. Dyn. 228, 30 (2003).
[CrossRef] [PubMed]

A. J. Udvadia and E. Linney, Dev. Biol. 256, 1 (2003).
[CrossRef] [PubMed]

C.-J. Huang, C.-T. Tu, C.-D. Hsiao, F.-J. Hsieh, and H.-J. Tsai, Dev. Dyn. 228, 30 (2003).
[CrossRef] [PubMed]

2002 (2)

S.-W. Chu, I-S. Chen, T.-M. Liu, C.-K. Sun, S.-P. Lee, B.-L. Lin, P.-C. Cheng, M.-X. Kuo, D.-J. Lin, and H.-L. Liu, J. Microsc. 208(3), 190 (2002).
[CrossRef] [PubMed]

I.-H. Chen, S.-W. Chu, C.-K Sun, P.-C. Cheng, and B.-L. Lin, Opt. Quantum Electron. 34, 1251 (2002).
[CrossRef]

2001 (7)

N. G. Gurskaya, A. F. Fradkov, A. Terskikh, M. V. Matz, Y. A. Labas, V. I. Martynov, Y. G. Yanushevich, K. A. Lukyanov, and S. A. Lukyanov, FEBS Lett. 507, 16 (2001).
[CrossRef] [PubMed]

C.-D. Hsiao, F.-J. Hsieh, and H.-J. Tsai, Dev. Dyn. 220, 323 (2001).
[CrossRef] [PubMed]

P.-C. Cheng, B.-L. Lin, F.-J. Kao, M. Gu, X. Gan, M.-K. Huang, and Y.-S. Wang, Micron 32, 661 (2001).
[CrossRef] [PubMed]

G. A. Blab, P. H. M. Lommerse, L. Cognet, G. S. Harms, and T. Schmidt, Chem. Phys. Lett. 350, 71 (2001).
[CrossRef]

U. K. Tirlapur, K. König, C. Peuckert, R. Krieg, and K.-J. Halbjuber, Exp. Cell Res. 263, 88 (2001).
[CrossRef] [PubMed]

K. König, I. Riemann, and W. Fritzsche, Opt. Lett. 26, 819 (2001).
[CrossRef]

S.-W. Chu, I.-H. Chen, T.-M. Liu, P. C. Cheng, C.-K. Sun, and B.-L. Lin, Opt. Lett. 26, 1909 (2001).
[CrossRef]

1999 (2)

P. E. Hockberger, T. A. Skimina, V. E. Centonze, C. Lavin, S. Chu, S. Dadras, J. K. Reddy, and J. G. White, Proc. Natl. Acad. Sci. U.S.A. 96, 6255 (1999).
[CrossRef] [PubMed]

J. M. Squirrell, D. L. Wokosin, J. G. White, and B. D. Bavister, Nat. Biotechnol. 17, 763 (1999).
[CrossRef] [PubMed]

1997 (1)

1996 (1)

C. Xu and W. W. Webb, J. Opt. Soc. Am. B 18, 481 (1996).
[CrossRef]

1990 (1)

W. Denk, J. H. Strickler, and W. W. Webb, Science 248, 73 (1990).
[CrossRef] [PubMed]

1981 (1)

R. R. Anderson and J. A. Parrish, J. Invest. Dermatol. 77, 13 (1981).
[CrossRef] [PubMed]

Anderson, R. R.

R. R. Anderson and J. A. Parrish, J. Invest. Dermatol. 77, 13 (1981).
[CrossRef] [PubMed]

Bavister, B. D.

J. M. Squirrell, D. L. Wokosin, J. G. White, and B. D. Bavister, Nat. Biotechnol. 17, 763 (1999).
[CrossRef] [PubMed]

Bem-Yakar, A.

M. F. Yanik, H. Cinar, H. N. Cinar, A. D. Chisholm, Y. Jin, and A. Bem-Yakar, Nature 432, 822 (2004).
[CrossRef] [PubMed]

Blab, G. A.

G. A. Blab, P. H. M. Lommerse, L. Cognet, G. S. Harms, and T. Schmidt, Chem. Phys. Lett. 350, 71 (2001).
[CrossRef]

Centonze, V. E.

P. E. Hockberger, T. A. Skimina, V. E. Centonze, C. Lavin, S. Chu, S. Dadras, J. K. Reddy, and J. G. White, Proc. Natl. Acad. Sci. U.S.A. 96, 6255 (1999).
[CrossRef] [PubMed]

Chen, I.-H.

I.-H. Chen, S.-W. Chu, C.-K Sun, P.-C. Cheng, and B.-L. Lin, Opt. Quantum Electron. 34, 1251 (2002).
[CrossRef]

S.-W. Chu, I.-H. Chen, T.-M. Liu, P. C. Cheng, C.-K. Sun, and B.-L. Lin, Opt. Lett. 26, 1909 (2001).
[CrossRef]

Chen, I-S.

S.-W. Chu, I-S. Chen, T.-M. Liu, C.-K. Sun, S.-P. Lee, B.-L. Lin, P.-C. Cheng, M.-X. Kuo, D.-J. Lin, and H.-L. Liu, J. Microsc. 208(3), 190 (2002).
[CrossRef] [PubMed]

Chen, S.-Y.

C.-K. Sun, S.-W. Chu, S.-Y. Chen, T.-H. Tsai, T.-M. Liu, C.-Y. Lin, and H.-J. Tsai, J. Struct. Biol. 147, 19 (2004).
[CrossRef] [PubMed]

Cheng, P. C.

Cheng, P.-C.

S.-W. Chu, I-S. Chen, T.-M. Liu, C.-K. Sun, S.-P. Lee, B.-L. Lin, P.-C. Cheng, M.-X. Kuo, D.-J. Lin, and H.-L. Liu, J. Microsc. 208(3), 190 (2002).
[CrossRef] [PubMed]

I.-H. Chen, S.-W. Chu, C.-K Sun, P.-C. Cheng, and B.-L. Lin, Opt. Quantum Electron. 34, 1251 (2002).
[CrossRef]

P.-C. Cheng, B.-L. Lin, F.-J. Kao, M. Gu, X. Gan, M.-K. Huang, and Y.-S. Wang, Micron 32, 661 (2001).
[CrossRef] [PubMed]

Chisholm, A. D.

M. F. Yanik, H. Cinar, H. N. Cinar, A. D. Chisholm, Y. Jin, and A. Bem-Yakar, Nature 432, 822 (2004).
[CrossRef] [PubMed]

Chu, S.

P. E. Hockberger, T. A. Skimina, V. E. Centonze, C. Lavin, S. Chu, S. Dadras, J. K. Reddy, and J. G. White, Proc. Natl. Acad. Sci. U.S.A. 96, 6255 (1999).
[CrossRef] [PubMed]

Chu, S.-W.

C.-K. Sun, S.-W. Chu, S.-Y. Chen, T.-H. Tsai, T.-M. Liu, C.-Y. Lin, and H.-J. Tsai, J. Struct. Biol. 147, 19 (2004).
[CrossRef] [PubMed]

S.-W. Chu, I-S. Chen, T.-M. Liu, C.-K. Sun, S.-P. Lee, B.-L. Lin, P.-C. Cheng, M.-X. Kuo, D.-J. Lin, and H.-L. Liu, J. Microsc. 208(3), 190 (2002).
[CrossRef] [PubMed]

I.-H. Chen, S.-W. Chu, C.-K Sun, P.-C. Cheng, and B.-L. Lin, Opt. Quantum Electron. 34, 1251 (2002).
[CrossRef]

S.-W. Chu, I.-H. Chen, T.-M. Liu, P. C. Cheng, C.-K. Sun, and B.-L. Lin, Opt. Lett. 26, 1909 (2001).
[CrossRef]

Cinar, H.

M. F. Yanik, H. Cinar, H. N. Cinar, A. D. Chisholm, Y. Jin, and A. Bem-Yakar, Nature 432, 822 (2004).
[CrossRef] [PubMed]

Cinar, H. N.

M. F. Yanik, H. Cinar, H. N. Cinar, A. D. Chisholm, Y. Jin, and A. Bem-Yakar, Nature 432, 822 (2004).
[CrossRef] [PubMed]

Cognet, L.

G. A. Blab, P. H. M. Lommerse, L. Cognet, G. S. Harms, and T. Schmidt, Chem. Phys. Lett. 350, 71 (2001).
[CrossRef]

Dadras, S.

P. E. Hockberger, T. A. Skimina, V. E. Centonze, C. Lavin, S. Chu, S. Dadras, J. K. Reddy, and J. G. White, Proc. Natl. Acad. Sci. U.S.A. 96, 6255 (1999).
[CrossRef] [PubMed]

Denk, W.

W. Denk, J. H. Strickler, and W. W. Webb, Science 248, 73 (1990).
[CrossRef] [PubMed]

Fradkov, A. F.

N. G. Gurskaya, A. F. Fradkov, A. Terskikh, M. V. Matz, Y. A. Labas, V. I. Martynov, Y. G. Yanushevich, K. A. Lukyanov, and S. A. Lukyanov, FEBS Lett. 507, 16 (2001).
[CrossRef] [PubMed]

Fritzsche, W.

Gan, X.

P.-C. Cheng, B.-L. Lin, F.-J. Kao, M. Gu, X. Gan, M.-K. Huang, and Y.-S. Wang, Micron 32, 661 (2001).
[CrossRef] [PubMed]

Gratton, E.

Gu, M.

P.-C. Cheng, B.-L. Lin, F.-J. Kao, M. Gu, X. Gan, M.-K. Huang, and Y.-S. Wang, Micron 32, 661 (2001).
[CrossRef] [PubMed]

Gurskaya, N. G.

N. G. Gurskaya, A. F. Fradkov, A. Terskikh, M. V. Matz, Y. A. Labas, V. I. Martynov, Y. G. Yanushevich, K. A. Lukyanov, and S. A. Lukyanov, FEBS Lett. 507, 16 (2001).
[CrossRef] [PubMed]

Halbjuber, K.-J.

U. K. Tirlapur, K. König, C. Peuckert, R. Krieg, and K.-J. Halbjuber, Exp. Cell Res. 263, 88 (2001).
[CrossRef] [PubMed]

Harms, G. S.

G. A. Blab, P. H. M. Lommerse, L. Cognet, G. S. Harms, and T. Schmidt, Chem. Phys. Lett. 350, 71 (2001).
[CrossRef]

Hockberger, P. E.

P. E. Hockberger, T. A. Skimina, V. E. Centonze, C. Lavin, S. Chu, S. Dadras, J. K. Reddy, and J. G. White, Proc. Natl. Acad. Sci. U.S.A. 96, 6255 (1999).
[CrossRef] [PubMed]

Hsiao, C.-D.

C.-J. Huang, C.-T. Tu, C.-D. Hsiao, F.-J. Hsieh, and H.-J. Tsai, Dev. Dyn. 228, 30 (2003).
[CrossRef] [PubMed]

C.-J. Huang, C.-T. Tu, C.-D. Hsiao, F.-J. Hsieh, and H.-J. Tsai, Dev. Dyn. 228, 30 (2003).
[CrossRef] [PubMed]

C.-D. Hsiao, F.-J. Hsieh, and H.-J. Tsai, Dev. Dyn. 220, 323 (2001).
[CrossRef] [PubMed]

Hsieh, F.-J.

C.-J. Huang, C.-T. Tu, C.-D. Hsiao, F.-J. Hsieh, and H.-J. Tsai, Dev. Dyn. 228, 30 (2003).
[CrossRef] [PubMed]

C.-J. Huang, C.-T. Tu, C.-D. Hsiao, F.-J. Hsieh, and H.-J. Tsai, Dev. Dyn. 228, 30 (2003).
[CrossRef] [PubMed]

C.-D. Hsiao, F.-J. Hsieh, and H.-J. Tsai, Dev. Dyn. 220, 323 (2001).
[CrossRef] [PubMed]

Huang, C.-J.

C.-J. Huang, C.-T. Tu, C.-D. Hsiao, F.-J. Hsieh, and H.-J. Tsai, Dev. Dyn. 228, 30 (2003).
[CrossRef] [PubMed]

C.-J. Huang, C.-T. Tu, C.-D. Hsiao, F.-J. Hsieh, and H.-J. Tsai, Dev. Dyn. 228, 30 (2003).
[CrossRef] [PubMed]

Huang, M.-K.

P.-C. Cheng, B.-L. Lin, F.-J. Kao, M. Gu, X. Gan, M.-K. Huang, and Y.-S. Wang, Micron 32, 661 (2001).
[CrossRef] [PubMed]

Jin, Y.

M. F. Yanik, H. Cinar, H. N. Cinar, A. D. Chisholm, Y. Jin, and A. Bem-Yakar, Nature 432, 822 (2004).
[CrossRef] [PubMed]

Kao, F.-J.

P.-C. Cheng, B.-L. Lin, F.-J. Kao, M. Gu, X. Gan, M.-K. Huang, and Y.-S. Wang, Micron 32, 661 (2001).
[CrossRef] [PubMed]

König, K.

Krieg, R.

U. K. Tirlapur, K. König, C. Peuckert, R. Krieg, and K.-J. Halbjuber, Exp. Cell Res. 263, 88 (2001).
[CrossRef] [PubMed]

Kuo, M.-X.

S.-W. Chu, I-S. Chen, T.-M. Liu, C.-K. Sun, S.-P. Lee, B.-L. Lin, P.-C. Cheng, M.-X. Kuo, D.-J. Lin, and H.-L. Liu, J. Microsc. 208(3), 190 (2002).
[CrossRef] [PubMed]

Labas, Y. A.

N. G. Gurskaya, A. F. Fradkov, A. Terskikh, M. V. Matz, Y. A. Labas, V. I. Martynov, Y. G. Yanushevich, K. A. Lukyanov, and S. A. Lukyanov, FEBS Lett. 507, 16 (2001).
[CrossRef] [PubMed]

Lavin, C.

P. E. Hockberger, T. A. Skimina, V. E. Centonze, C. Lavin, S. Chu, S. Dadras, J. K. Reddy, and J. G. White, Proc. Natl. Acad. Sci. U.S.A. 96, 6255 (1999).
[CrossRef] [PubMed]

Lee, S.-P.

S.-W. Chu, I-S. Chen, T.-M. Liu, C.-K. Sun, S.-P. Lee, B.-L. Lin, P.-C. Cheng, M.-X. Kuo, D.-J. Lin, and H.-L. Liu, J. Microsc. 208(3), 190 (2002).
[CrossRef] [PubMed]

Lin, B.-L.

S.-W. Chu, I-S. Chen, T.-M. Liu, C.-K. Sun, S.-P. Lee, B.-L. Lin, P.-C. Cheng, M.-X. Kuo, D.-J. Lin, and H.-L. Liu, J. Microsc. 208(3), 190 (2002).
[CrossRef] [PubMed]

I.-H. Chen, S.-W. Chu, C.-K Sun, P.-C. Cheng, and B.-L. Lin, Opt. Quantum Electron. 34, 1251 (2002).
[CrossRef]

S.-W. Chu, I.-H. Chen, T.-M. Liu, P. C. Cheng, C.-K. Sun, and B.-L. Lin, Opt. Lett. 26, 1909 (2001).
[CrossRef]

P.-C. Cheng, B.-L. Lin, F.-J. Kao, M. Gu, X. Gan, M.-K. Huang, and Y.-S. Wang, Micron 32, 661 (2001).
[CrossRef] [PubMed]

Lin, C.-Y.

C.-K. Sun, S.-W. Chu, S.-Y. Chen, T.-H. Tsai, T.-M. Liu, C.-Y. Lin, and H.-J. Tsai, J. Struct. Biol. 147, 19 (2004).
[CrossRef] [PubMed]

Lin, D.-J.

S.-W. Chu, I-S. Chen, T.-M. Liu, C.-K. Sun, S.-P. Lee, B.-L. Lin, P.-C. Cheng, M.-X. Kuo, D.-J. Lin, and H.-L. Liu, J. Microsc. 208(3), 190 (2002).
[CrossRef] [PubMed]

Linney, E.

A. J. Udvadia and E. Linney, Dev. Biol. 256, 1 (2003).
[CrossRef] [PubMed]

Liu, H.-L.

S.-W. Chu, I-S. Chen, T.-M. Liu, C.-K. Sun, S.-P. Lee, B.-L. Lin, P.-C. Cheng, M.-X. Kuo, D.-J. Lin, and H.-L. Liu, J. Microsc. 208(3), 190 (2002).
[CrossRef] [PubMed]

Liu, T.-M.

C.-K. Sun, S.-W. Chu, S.-Y. Chen, T.-H. Tsai, T.-M. Liu, C.-Y. Lin, and H.-J. Tsai, J. Struct. Biol. 147, 19 (2004).
[CrossRef] [PubMed]

S.-W. Chu, I-S. Chen, T.-M. Liu, C.-K. Sun, S.-P. Lee, B.-L. Lin, P.-C. Cheng, M.-X. Kuo, D.-J. Lin, and H.-L. Liu, J. Microsc. 208(3), 190 (2002).
[CrossRef] [PubMed]

S.-W. Chu, I.-H. Chen, T.-M. Liu, P. C. Cheng, C.-K. Sun, and B.-L. Lin, Opt. Lett. 26, 1909 (2001).
[CrossRef]

Lommerse, P. H.

G. A. Blab, P. H. M. Lommerse, L. Cognet, G. S. Harms, and T. Schmidt, Chem. Phys. Lett. 350, 71 (2001).
[CrossRef]

Lukyanov, K. A.

N. G. Gurskaya, A. F. Fradkov, A. Terskikh, M. V. Matz, Y. A. Labas, V. I. Martynov, Y. G. Yanushevich, K. A. Lukyanov, and S. A. Lukyanov, FEBS Lett. 507, 16 (2001).
[CrossRef] [PubMed]

Lukyanov, S. A.

N. G. Gurskaya, A. F. Fradkov, A. Terskikh, M. V. Matz, Y. A. Labas, V. I. Martynov, Y. G. Yanushevich, K. A. Lukyanov, and S. A. Lukyanov, FEBS Lett. 507, 16 (2001).
[CrossRef] [PubMed]

Mantulin, W. W.

Martynov, V. I.

N. G. Gurskaya, A. F. Fradkov, A. Terskikh, M. V. Matz, Y. A. Labas, V. I. Martynov, Y. G. Yanushevich, K. A. Lukyanov, and S. A. Lukyanov, FEBS Lett. 507, 16 (2001).
[CrossRef] [PubMed]

Matz, M. V.

N. G. Gurskaya, A. F. Fradkov, A. Terskikh, M. V. Matz, Y. A. Labas, V. I. Martynov, Y. G. Yanushevich, K. A. Lukyanov, and S. A. Lukyanov, FEBS Lett. 507, 16 (2001).
[CrossRef] [PubMed]

Parrish, J. A.

R. R. Anderson and J. A. Parrish, J. Invest. Dermatol. 77, 13 (1981).
[CrossRef] [PubMed]

Peuckert, C.

U. K. Tirlapur, K. König, C. Peuckert, R. Krieg, and K.-J. Halbjuber, Exp. Cell Res. 263, 88 (2001).
[CrossRef] [PubMed]

Reddy, J. K.

P. E. Hockberger, T. A. Skimina, V. E. Centonze, C. Lavin, S. Chu, S. Dadras, J. K. Reddy, and J. G. White, Proc. Natl. Acad. Sci. U.S.A. 96, 6255 (1999).
[CrossRef] [PubMed]

Riemann, I.

Schmidt, T.

G. A. Blab, P. H. M. Lommerse, L. Cognet, G. S. Harms, and T. Schmidt, Chem. Phys. Lett. 350, 71 (2001).
[CrossRef]

Skimina, T. A.

P. E. Hockberger, T. A. Skimina, V. E. Centonze, C. Lavin, S. Chu, S. Dadras, J. K. Reddy, and J. G. White, Proc. Natl. Acad. Sci. U.S.A. 96, 6255 (1999).
[CrossRef] [PubMed]

So, P. T.

Squirrell, J. M.

J. M. Squirrell, D. L. Wokosin, J. G. White, and B. D. Bavister, Nat. Biotechnol. 17, 763 (1999).
[CrossRef] [PubMed]

Strickler, J. H.

W. Denk, J. H. Strickler, and W. W. Webb, Science 248, 73 (1990).
[CrossRef] [PubMed]

Sun, C.-K

I.-H. Chen, S.-W. Chu, C.-K Sun, P.-C. Cheng, and B.-L. Lin, Opt. Quantum Electron. 34, 1251 (2002).
[CrossRef]

Sun, C.-K.

C.-K. Sun, S.-W. Chu, S.-Y. Chen, T.-H. Tsai, T.-M. Liu, C.-Y. Lin, and H.-J. Tsai, J. Struct. Biol. 147, 19 (2004).
[CrossRef] [PubMed]

S.-W. Chu, I-S. Chen, T.-M. Liu, C.-K. Sun, S.-P. Lee, B.-L. Lin, P.-C. Cheng, M.-X. Kuo, D.-J. Lin, and H.-L. Liu, J. Microsc. 208(3), 190 (2002).
[CrossRef] [PubMed]

S.-W. Chu, I.-H. Chen, T.-M. Liu, P. C. Cheng, C.-K. Sun, and B.-L. Lin, Opt. Lett. 26, 1909 (2001).
[CrossRef]

Takamatsu, T.

T. Tanabe and T. Takamatsu, paper presented at the Focus on Microscopy, Jena, Germany, March 20-23, 2005.

Tanabe, T.

T. Tanabe and T. Takamatsu, paper presented at the Focus on Microscopy, Jena, Germany, March 20-23, 2005.

Terskikh, A.

N. G. Gurskaya, A. F. Fradkov, A. Terskikh, M. V. Matz, Y. A. Labas, V. I. Martynov, Y. G. Yanushevich, K. A. Lukyanov, and S. A. Lukyanov, FEBS Lett. 507, 16 (2001).
[CrossRef] [PubMed]

Tirlapur, U. K.

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Figures (3)

Fig. 1
Fig. 1

(a) 2PF spectrum excited with a 1230 nm fs Cr:forsterite laser from Hc-RFP in myocardial cells of a live zebrafish embryo. (b) Dependence between 618 nm fluorescence power (squares) and 1230 nm excitation power measured from the Hc-RFP in myocardial cells of a live zebrafish embryo. The well-matched solid line is the slope = 2 fit confirming the two-photon nature of light absorption. Note that both axes are log scaled.

Fig. 2
Fig. 2

Absolute two-photon excitation action cross sections ( σ TPE , y axis) of Hc-RFP. 1 GM = 10 50 cm 4 s photon .

Fig. 3
Fig. 3

(a)–(c) Reconstructed 3D in vivo two-photon fluorescence images of a live transgenic zebrafish heart taken at 30-hpf (prim-16 stage) without removing its chorion. (a)–(c) Images with different view angles of 0°, 60°, and 180°, respectively, rotating along the horizontal axis. AT, atrium, VE, ventricle. Image size, 240 μ m × 240 μ m × 180 μ m . (d)–(g) High-resolution cross-sectional in vivo images of the heart surface of a live transgenic zebrafish taken at the prim-16 stage without removing its chorion: (d) 2PF image, (e) SHG image, (f) THG image, (g) combined image. Image size, 60 μ m × 60 μ m .

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