Abstract

Genetically expressed fluorescent proteins have been shown to provide photoacoustic contrast. However, they can be limited by low photoacoustic generation efficiency and low optical absorption at red and near infrared wavelengths, thus limiting their usefulness in mammalian small animal models. In addition, many fluorescent proteins exhibit low photostability due to photobleaching and transient absorption effects. In this study, we explore these issues by synthesizing and characterizing a range of commonly used fluorescent proteins (dsRed, mCherry, mNeptune, mRaspberry, AQ143, E2 Crimson) and novel non-fluorescent chromoproteins (aeCP597 and cjBlue and a non-fluorescent mutant of E2 Crimson). The photoacoustic spectra, photoacoustic generation efficiency and photostability of each fluorescent protein and chromoprotein were measured. Compared to the fluorescent proteins, the chromoproteins were found to exhibit higher photoacoustic generation efficiency due to the absence of radiative relaxation and ground state depopulation, and significantly higher photostability. The feasibility of converting an existing fluorescent protein into a non-fluorescent chromoprotein via mutagenesis was also demonstrated. The chromoprotein mutant exhibited greater photoacoustic signal generation efficiency and better agreement between the photoacoustic and the specific extinction coefficient spectra than the original fluorescent protein. Lastly, the genetic expression of a chromoprotein in mammalian cells was demonstrated. This study suggests that chromoproteins may have potential for providing genetically encoded photoacoustic contrast.

© 2013 Optical Society of America

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    [CrossRef] [PubMed]
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    [CrossRef] [PubMed]
  27. E. Zhang, J. Laufer, P. Beard, “Backward-mode multiwavelength photoacoustic scanner using a planar Fabry-Perot polymer film ultrasound sensor for high-resolution three-dimensional imaging of biological tissues,” Appl. Opt. 47(4), 561–577 (2008).
    [CrossRef] [PubMed]
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    [CrossRef]
  33. N. C. Shaner, M. Z. Lin, M. R. McKeown, P. A. Steinbach, K. L. Hazelwood, M. W. Davidson, R. Y. Tsien, “Improving the photostability of bright monomeric orange and red fluorescent proteins,” Nat. Methods 5(6), 545–551 (2008).
    [CrossRef] [PubMed]
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    [CrossRef]
  35. B. T. Cox, S. R. Arridge, P. C. Beard, “Estimating chromophore distributions from multiwavelength photoacoustic images,” J. Opt. Soc. Am. A 26(2), 443–455 (2009).
    [CrossRef] [PubMed]
  36. J. Laufer, B. Cox, E. Zhang, P. Beard, “Quantitative determination of chromophore concentrations from 2D photoacoustic images using a nonlinear model-based inversion scheme,” Appl. Opt. 49(8), 1219–1233 (2010).
    [CrossRef] [PubMed]
  37. R. Y. Tsien, “The green fluorescent protein,” Annu. Rev. Biochem. 67(1), 509–544 (1998).
    [CrossRef] [PubMed]

2012

J. Laufer, A. Jathoul, P. Johnson, E. Zhang, M. Lythgoe, R. B. Pedley, M. Pule, P. Beard, “In vivo photoacoustic imaging of tyrosinase expressing tumours in mice,” Proc. SPIE 8223, 82230M (2012).
[CrossRef]

X. Cai, L. Li, A. Krumholz, Z. Guo, T. N. Erpelding, C. Zhang, Y. Zhang, Y. Xia, L. V. Wang, “Multi-scale molecular photoacoustic tomography of gene expression,” PLoS ONE 7(8), e43999 (2012).
[CrossRef] [PubMed]

G. S. Filonov, A. Krumholz, J. Xia, J. Yao, L. V. Wang, V. V. Verkhusha, “Deep-tissue photoacoustic tomography of a genetically encoded near-infrared fluorescent probe - supporting information,” Angew. Chem. 124(6), 1477–1480 (2012).
[CrossRef]

C. Ruckebusch, M. Sliwa, P. Pernot, A. de Juan, R. Tauler, “Comprehensive data analysis of femtosecond transient absorption spectra: A review,” J. Photochem. Photobiol. Photochem. Rev. 13(1), 1–27 (2012).
[CrossRef]

2011

G. S. Filonov, K. D. Piatkevich, L.-M. Ting, J. Zhang, K. Kim, V. V. Verkhusha, “Bright and stable near-infrared fluorescent protein for in vivo imaging,” Nat. Biotechnol. 29(8), 757–761 (2011).
[CrossRef] [PubMed]

P. Beard, “Biomedical photoacoustic imaging,” Interface Focus 1(4), 602–631 (2011).
[CrossRef] [PubMed]

A. Krumholz, S. J. Vanvickle-Chavez, J. Yao, T. P. Fleming, W. E. Gillanders, L. V. Wang, “Photoacoustic microscopy of tyrosinase reporter gene in vivo,” J. Biomed. Opt. 16(8), 080503 (2011).
[CrossRef] [PubMed]

2010

J. W. Borst, A. J. W. G. Visser, “Fluorescence lifetime imaging microscopy in life sciences,” Meas. Sci. Technol. 21(10), 102002 (2010).
[CrossRef]

K. D. Piatkevich, E. N. Efremenko, V. V. Verkhusha, S. D. Varfolomeev, “Red fluorescent proteins and their properties,” Russ. Chem. Rev. 79(3), 243–258 (2010).
[CrossRef]

D. Shcherbo, I. I. Shemiakina, A. V. Ryabova, K. E. Luker, B. T. Schmidt, E. A. Souslova, T. V. Gorodnicheva, L. Strukova, K. M. Shidlovskiy, O. V. Britanova, A. G. Zaraisky, K. A. Lukyanov, V. B. Loschenov, G. D. Luker, D. M. Chudakov, “Near-infrared fluorescent proteins,” Nat. Methods 7(10), 827–829 (2010).
[CrossRef] [PubMed]

J. Laufer, B. Cox, E. Zhang, P. Beard, “Quantitative determination of chromophore concentrations from 2D photoacoustic images using a nonlinear model-based inversion scheme,” Appl. Opt. 49(8), 1219–1233 (2010).
[CrossRef] [PubMed]

2009

B. T. Cox, S. R. Arridge, P. C. Beard, “Estimating chromophore distributions from multiwavelength photoacoustic images,” J. Opt. Soc. Am. A 26(2), 443–455 (2009).
[CrossRef] [PubMed]

W. Min, S. Lu, S. Chong, R. Roy, G. R. Holtom, X. S. Xie, “Imaging chromophores with undetectable fluorescence by stimulated emission microscopy,” Nature 461(7267), 1105–1109 (2009).
[CrossRef] [PubMed]

R. L. Strack, B. Hein, D. Bhattacharyya, S. W. Hell, R. J. Keenan, B. S. Glick, “A rapidly maturing far-red derivative of DsRed-Express2 for whole-cell labeling,” Biochemistry 48(35), 8279–8281 (2009).
[CrossRef] [PubMed]

D. Razansky, M. Distel, C. Vinegoni, R. Ma, N. Perrimon, R. W. Köster, V. Ntziachristos, “Multispectral opto-acoustic tomography of deep-seated fluorescent proteins in vivo,” Nat. Photonics 3(7), 412–417 (2009).
[CrossRef]

C. Blum, V. Subramaniam, “Single-molecule spectroscopy of fluorescent proteins,” Anal. Bioanal. Chem. 393(2), 527–541 (2009).
[CrossRef] [PubMed]

M. Z. Lin, M. R. McKeown, H.-L. Ng, T. A. Aguilera, N. C. Shaner, R. E. Campbell, S. R. Adams, L. A. Gross, W. Ma, T. Alber, R. Y. Tsien, “Autofluorescent proteins with excitation in the optical window for intravital imaging in mammals,” Chem. Biol. 16(11), 1169–1179 (2009).
[CrossRef] [PubMed]

2008

J. Hendrix, C. Flors, P. Dedecker, J. Hofkens, Y. Engelborghs, “Dark states in monomeric red fluorescent proteins studied by fluorescence correlation and single molecule spectroscopy,” Biophys. J. 94(10), 4103–4113 (2008).
[CrossRef] [PubMed]

N. C. Shaner, M. Z. Lin, M. R. McKeown, P. A. Steinbach, K. L. Hazelwood, M. W. Davidson, R. Y. Tsien, “Improving the photostability of bright monomeric orange and red fluorescent proteins,” Nat. Methods 5(6), 545–551 (2008).
[CrossRef] [PubMed]

E. Zhang, J. Laufer, P. Beard, “Backward-mode multiwavelength photoacoustic scanner using a planar Fabry-Perot polymer film ultrasound sensor for high-resolution three-dimensional imaging of biological tissues,” Appl. Opt. 47(4), 561–577 (2008).
[CrossRef] [PubMed]

2007

L. Li, R. J. Zemp, G. Lungu, G. Stoica, L. V. Wang, “Photoacoustic imaging of lacZ gene expression in vivo,” J. Biomed. Opt. 12(2), 020504 (2007).
[CrossRef] [PubMed]

2006

M. C. Y. Chan, S. Karasawa, H. Mizuno, I. Bosanac, D. Ho, G. G. Privé, A. Miyawaki, M. Ikura, “Structural characterization of a blue chromoprotein and its yellow mutant from the sea anemone Cnidopus japonicus,” J. Biol. Chem. 281(49), 37813–37819 (2006).
[CrossRef] [PubMed]

2005

M. A. Shkrob, Y. G. Yanushevich, D. M. Chudakov, N. G. Gurskaya, Y. A. Labas, S. Y. Poponov, N. N. Mudrik, S. Lukyanov, K. A. Lukyanov, “Far-red fluorescent proteins evolved from a blue chromoprotein from Actinia equina,” Biochem. J. 392(3), 649–654 (2005).
[CrossRef] [PubMed]

J. W. Lichtman, J. A. Conchello, “Fluorescence microscopy,” Nat. Methods 2(12), 910–919 (2005).
[CrossRef] [PubMed]

M. R. Soboleski, J. Oaks, W. P. Halford, “Green fluorescent protein is a quantitative reporter of gene expression in individual eukaryotic cells,” FASEB J. 19(3), 440–442 (2005).
[PubMed]

D. Stoner-Ma, A. A. Jaye, P. Matousek, M. Towrie, S. R. Meech, P. J. Tonge, “Observation of excited-state proton transfer in green fluorescent protein using ultrafast vibrational spectroscopy,” J. Am. Chem. Soc. 127(9), 2864–2865 (2005).
[CrossRef] [PubMed]

2004

L. Wang, W. C. Jackson, P. A. Steinbach, R. Y. Tsien, “Evolution of new nonantibody proteins via iterative somatic hypermutation,” Proc. Natl. Acad. Sci. U.S.A. 101(48), 16745–16749 (2004).
[CrossRef] [PubMed]

S. R. Cherry, “In vivo molecular and genomic imaging: new challenges for imaging physics,” Phys. Med. Biol. 49(3), R13–R48 (2004).
[CrossRef] [PubMed]

N. C. Shaner, R. E. Campbell, P. A. Steinbach, B. N. Giepmans, A. E. Palmer, R. Y. Tsien, “Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein,” Nat. Biotechnol. 22(12), 1567–1572 (2004).
[CrossRef] [PubMed]

2002

M. E. Bulina, D. M. Chudakov, N. N. Mudrik, K. A. Lukyanov, “Interconversion of Anthozoa GFP-like fluorescent and non-fluorescent proteins by mutagenesis,” BMC Biochem. 3(1), 7 (2002).
[CrossRef] [PubMed]

B. J. Bevis, B. S. Glick, “Rapidly maturing variants of the Discosoma red fluorescent protein (DsRed),” Nat. Biotechnol. 20(1), 83–87 (2002).
[CrossRef] [PubMed]

2001

M. Cotlet, J. Hofkens, S. Habuchi, G. Dirix, M. Van Guyse, J. Michiels, J. Vanderleyden, F. C. De Schryver, “Identification of different emitting species in the red fluorescent protein DsRed by means of ensemble and single-molecule spectroscopy,” Proc. Natl. Acad. Sci. U.S.A. 98(25), 14398–14403 (2001).
[CrossRef] [PubMed]

2000

Y. Yu, A. J. Annala, J. R. Barrio, T. Toyokuni, N. Satyamurthy, M. Namavari, S. R. Cherry, M. E. Phelps, H. R. Herschman, S. S. Gambhir, “Quantification of target gene expression by imaging reporter gene expression in living animals,” Nat. Med. 6(8), 933–937 (2000).
[CrossRef] [PubMed]

G. S. Baird, D. A. Zacharias, R. Y. Tsien, “Biochemistry, mutagenesis, and oligomerization of DsRed, a red fluorescent protein from coral,” Proc. Natl. Acad. Sci. U.S.A. 97(22), 11984–11989 (2000).
[CrossRef] [PubMed]

1998

R. Y. Tsien, “The green fluorescent protein,” Annu. Rev. Biochem. 67(1), 509–544 (1998).
[CrossRef] [PubMed]

1997

A. N. Warrens, M. D. Jones, R. I. Lechler, “Splicing by overlap extension by PCR using asymmetric amplification: an improved technique for the generation of hybrid proteins of immunological interest,” Gene 186(1), 29–35 (1997).
[CrossRef] [PubMed]

1995

W. P. Stemmer, A. Crameri, K. D. Ha, T. M. Brennan, H. L. Heyneker, “Single-step assembly of a gene and entire plasmid from large numbers of oligodeoxyribonucleotides,” Gene 164(1), 49–53 (1995).
[CrossRef] [PubMed]

Adams, S. R.

M. Z. Lin, M. R. McKeown, H.-L. Ng, T. A. Aguilera, N. C. Shaner, R. E. Campbell, S. R. Adams, L. A. Gross, W. Ma, T. Alber, R. Y. Tsien, “Autofluorescent proteins with excitation in the optical window for intravital imaging in mammals,” Chem. Biol. 16(11), 1169–1179 (2009).
[CrossRef] [PubMed]

Aguilera, T. A.

M. Z. Lin, M. R. McKeown, H.-L. Ng, T. A. Aguilera, N. C. Shaner, R. E. Campbell, S. R. Adams, L. A. Gross, W. Ma, T. Alber, R. Y. Tsien, “Autofluorescent proteins with excitation in the optical window for intravital imaging in mammals,” Chem. Biol. 16(11), 1169–1179 (2009).
[CrossRef] [PubMed]

Alber, T.

M. Z. Lin, M. R. McKeown, H.-L. Ng, T. A. Aguilera, N. C. Shaner, R. E. Campbell, S. R. Adams, L. A. Gross, W. Ma, T. Alber, R. Y. Tsien, “Autofluorescent proteins with excitation in the optical window for intravital imaging in mammals,” Chem. Biol. 16(11), 1169–1179 (2009).
[CrossRef] [PubMed]

Annala, A. J.

Y. Yu, A. J. Annala, J. R. Barrio, T. Toyokuni, N. Satyamurthy, M. Namavari, S. R. Cherry, M. E. Phelps, H. R. Herschman, S. S. Gambhir, “Quantification of target gene expression by imaging reporter gene expression in living animals,” Nat. Med. 6(8), 933–937 (2000).
[CrossRef] [PubMed]

Arridge, S. R.

Baird, G. S.

G. S. Baird, D. A. Zacharias, R. Y. Tsien, “Biochemistry, mutagenesis, and oligomerization of DsRed, a red fluorescent protein from coral,” Proc. Natl. Acad. Sci. U.S.A. 97(22), 11984–11989 (2000).
[CrossRef] [PubMed]

Barrio, J. R.

Y. Yu, A. J. Annala, J. R. Barrio, T. Toyokuni, N. Satyamurthy, M. Namavari, S. R. Cherry, M. E. Phelps, H. R. Herschman, S. S. Gambhir, “Quantification of target gene expression by imaging reporter gene expression in living animals,” Nat. Med. 6(8), 933–937 (2000).
[CrossRef] [PubMed]

Beard, P.

Beard, P. C.

Bevis, B. J.

B. J. Bevis, B. S. Glick, “Rapidly maturing variants of the Discosoma red fluorescent protein (DsRed),” Nat. Biotechnol. 20(1), 83–87 (2002).
[CrossRef] [PubMed]

Bhattacharyya, D.

R. L. Strack, B. Hein, D. Bhattacharyya, S. W. Hell, R. J. Keenan, B. S. Glick, “A rapidly maturing far-red derivative of DsRed-Express2 for whole-cell labeling,” Biochemistry 48(35), 8279–8281 (2009).
[CrossRef] [PubMed]

Blum, C.

C. Blum, V. Subramaniam, “Single-molecule spectroscopy of fluorescent proteins,” Anal. Bioanal. Chem. 393(2), 527–541 (2009).
[CrossRef] [PubMed]

Borst, J. W.

J. W. Borst, A. J. W. G. Visser, “Fluorescence lifetime imaging microscopy in life sciences,” Meas. Sci. Technol. 21(10), 102002 (2010).
[CrossRef]

Bosanac, I.

M. C. Y. Chan, S. Karasawa, H. Mizuno, I. Bosanac, D. Ho, G. G. Privé, A. Miyawaki, M. Ikura, “Structural characterization of a blue chromoprotein and its yellow mutant from the sea anemone Cnidopus japonicus,” J. Biol. Chem. 281(49), 37813–37819 (2006).
[CrossRef] [PubMed]

Brennan, T. M.

W. P. Stemmer, A. Crameri, K. D. Ha, T. M. Brennan, H. L. Heyneker, “Single-step assembly of a gene and entire plasmid from large numbers of oligodeoxyribonucleotides,” Gene 164(1), 49–53 (1995).
[CrossRef] [PubMed]

Britanova, O. V.

D. Shcherbo, I. I. Shemiakina, A. V. Ryabova, K. E. Luker, B. T. Schmidt, E. A. Souslova, T. V. Gorodnicheva, L. Strukova, K. M. Shidlovskiy, O. V. Britanova, A. G. Zaraisky, K. A. Lukyanov, V. B. Loschenov, G. D. Luker, D. M. Chudakov, “Near-infrared fluorescent proteins,” Nat. Methods 7(10), 827–829 (2010).
[CrossRef] [PubMed]

Bulina, M. E.

M. E. Bulina, D. M. Chudakov, N. N. Mudrik, K. A. Lukyanov, “Interconversion of Anthozoa GFP-like fluorescent and non-fluorescent proteins by mutagenesis,” BMC Biochem. 3(1), 7 (2002).
[CrossRef] [PubMed]

Cai, X.

X. Cai, L. Li, A. Krumholz, Z. Guo, T. N. Erpelding, C. Zhang, Y. Zhang, Y. Xia, L. V. Wang, “Multi-scale molecular photoacoustic tomography of gene expression,” PLoS ONE 7(8), e43999 (2012).
[CrossRef] [PubMed]

Campbell, R. E.

M. Z. Lin, M. R. McKeown, H.-L. Ng, T. A. Aguilera, N. C. Shaner, R. E. Campbell, S. R. Adams, L. A. Gross, W. Ma, T. Alber, R. Y. Tsien, “Autofluorescent proteins with excitation in the optical window for intravital imaging in mammals,” Chem. Biol. 16(11), 1169–1179 (2009).
[CrossRef] [PubMed]

N. C. Shaner, R. E. Campbell, P. A. Steinbach, B. N. Giepmans, A. E. Palmer, R. Y. Tsien, “Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein,” Nat. Biotechnol. 22(12), 1567–1572 (2004).
[CrossRef] [PubMed]

Chan, M. C. Y.

M. C. Y. Chan, S. Karasawa, H. Mizuno, I. Bosanac, D. Ho, G. G. Privé, A. Miyawaki, M. Ikura, “Structural characterization of a blue chromoprotein and its yellow mutant from the sea anemone Cnidopus japonicus,” J. Biol. Chem. 281(49), 37813–37819 (2006).
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S. R. Cherry, “In vivo molecular and genomic imaging: new challenges for imaging physics,” Phys. Med. Biol. 49(3), R13–R48 (2004).
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Y. Yu, A. J. Annala, J. R. Barrio, T. Toyokuni, N. Satyamurthy, M. Namavari, S. R. Cherry, M. E. Phelps, H. R. Herschman, S. S. Gambhir, “Quantification of target gene expression by imaging reporter gene expression in living animals,” Nat. Med. 6(8), 933–937 (2000).
[CrossRef] [PubMed]

Chong, S.

W. Min, S. Lu, S. Chong, R. Roy, G. R. Holtom, X. S. Xie, “Imaging chromophores with undetectable fluorescence by stimulated emission microscopy,” Nature 461(7267), 1105–1109 (2009).
[CrossRef] [PubMed]

Chudakov, D. M.

D. Shcherbo, I. I. Shemiakina, A. V. Ryabova, K. E. Luker, B. T. Schmidt, E. A. Souslova, T. V. Gorodnicheva, L. Strukova, K. M. Shidlovskiy, O. V. Britanova, A. G. Zaraisky, K. A. Lukyanov, V. B. Loschenov, G. D. Luker, D. M. Chudakov, “Near-infrared fluorescent proteins,” Nat. Methods 7(10), 827–829 (2010).
[CrossRef] [PubMed]

M. A. Shkrob, Y. G. Yanushevich, D. M. Chudakov, N. G. Gurskaya, Y. A. Labas, S. Y. Poponov, N. N. Mudrik, S. Lukyanov, K. A. Lukyanov, “Far-red fluorescent proteins evolved from a blue chromoprotein from Actinia equina,” Biochem. J. 392(3), 649–654 (2005).
[CrossRef] [PubMed]

M. E. Bulina, D. M. Chudakov, N. N. Mudrik, K. A. Lukyanov, “Interconversion of Anthozoa GFP-like fluorescent and non-fluorescent proteins by mutagenesis,” BMC Biochem. 3(1), 7 (2002).
[CrossRef] [PubMed]

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J. W. Lichtman, J. A. Conchello, “Fluorescence microscopy,” Nat. Methods 2(12), 910–919 (2005).
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M. Cotlet, J. Hofkens, S. Habuchi, G. Dirix, M. Van Guyse, J. Michiels, J. Vanderleyden, F. C. De Schryver, “Identification of different emitting species in the red fluorescent protein DsRed by means of ensemble and single-molecule spectroscopy,” Proc. Natl. Acad. Sci. U.S.A. 98(25), 14398–14403 (2001).
[CrossRef] [PubMed]

Cox, B.

Cox, B. T.

Crameri, A.

W. P. Stemmer, A. Crameri, K. D. Ha, T. M. Brennan, H. L. Heyneker, “Single-step assembly of a gene and entire plasmid from large numbers of oligodeoxyribonucleotides,” Gene 164(1), 49–53 (1995).
[CrossRef] [PubMed]

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N. C. Shaner, M. Z. Lin, M. R. McKeown, P. A. Steinbach, K. L. Hazelwood, M. W. Davidson, R. Y. Tsien, “Improving the photostability of bright monomeric orange and red fluorescent proteins,” Nat. Methods 5(6), 545–551 (2008).
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C. Ruckebusch, M. Sliwa, P. Pernot, A. de Juan, R. Tauler, “Comprehensive data analysis of femtosecond transient absorption spectra: A review,” J. Photochem. Photobiol. Photochem. Rev. 13(1), 1–27 (2012).
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M. Cotlet, J. Hofkens, S. Habuchi, G. Dirix, M. Van Guyse, J. Michiels, J. Vanderleyden, F. C. De Schryver, “Identification of different emitting species in the red fluorescent protein DsRed by means of ensemble and single-molecule spectroscopy,” Proc. Natl. Acad. Sci. U.S.A. 98(25), 14398–14403 (2001).
[CrossRef] [PubMed]

Dedecker, P.

J. Hendrix, C. Flors, P. Dedecker, J. Hofkens, Y. Engelborghs, “Dark states in monomeric red fluorescent proteins studied by fluorescence correlation and single molecule spectroscopy,” Biophys. J. 94(10), 4103–4113 (2008).
[CrossRef] [PubMed]

Dirix, G.

M. Cotlet, J. Hofkens, S. Habuchi, G. Dirix, M. Van Guyse, J. Michiels, J. Vanderleyden, F. C. De Schryver, “Identification of different emitting species in the red fluorescent protein DsRed by means of ensemble and single-molecule spectroscopy,” Proc. Natl. Acad. Sci. U.S.A. 98(25), 14398–14403 (2001).
[CrossRef] [PubMed]

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D. Razansky, M. Distel, C. Vinegoni, R. Ma, N. Perrimon, R. W. Köster, V. Ntziachristos, “Multispectral opto-acoustic tomography of deep-seated fluorescent proteins in vivo,” Nat. Photonics 3(7), 412–417 (2009).
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K. D. Piatkevich, E. N. Efremenko, V. V. Verkhusha, S. D. Varfolomeev, “Red fluorescent proteins and their properties,” Russ. Chem. Rev. 79(3), 243–258 (2010).
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J. Hendrix, C. Flors, P. Dedecker, J. Hofkens, Y. Engelborghs, “Dark states in monomeric red fluorescent proteins studied by fluorescence correlation and single molecule spectroscopy,” Biophys. J. 94(10), 4103–4113 (2008).
[CrossRef] [PubMed]

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X. Cai, L. Li, A. Krumholz, Z. Guo, T. N. Erpelding, C. Zhang, Y. Zhang, Y. Xia, L. V. Wang, “Multi-scale molecular photoacoustic tomography of gene expression,” PLoS ONE 7(8), e43999 (2012).
[CrossRef] [PubMed]

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G. S. Filonov, A. Krumholz, J. Xia, J. Yao, L. V. Wang, V. V. Verkhusha, “Deep-tissue photoacoustic tomography of a genetically encoded near-infrared fluorescent probe - supporting information,” Angew. Chem. 124(6), 1477–1480 (2012).
[CrossRef]

G. S. Filonov, K. D. Piatkevich, L.-M. Ting, J. Zhang, K. Kim, V. V. Verkhusha, “Bright and stable near-infrared fluorescent protein for in vivo imaging,” Nat. Biotechnol. 29(8), 757–761 (2011).
[CrossRef] [PubMed]

Fleming, T. P.

A. Krumholz, S. J. Vanvickle-Chavez, J. Yao, T. P. Fleming, W. E. Gillanders, L. V. Wang, “Photoacoustic microscopy of tyrosinase reporter gene in vivo,” J. Biomed. Opt. 16(8), 080503 (2011).
[CrossRef] [PubMed]

Flors, C.

J. Hendrix, C. Flors, P. Dedecker, J. Hofkens, Y. Engelborghs, “Dark states in monomeric red fluorescent proteins studied by fluorescence correlation and single molecule spectroscopy,” Biophys. J. 94(10), 4103–4113 (2008).
[CrossRef] [PubMed]

Gambhir, S. S.

Y. Yu, A. J. Annala, J. R. Barrio, T. Toyokuni, N. Satyamurthy, M. Namavari, S. R. Cherry, M. E. Phelps, H. R. Herschman, S. S. Gambhir, “Quantification of target gene expression by imaging reporter gene expression in living animals,” Nat. Med. 6(8), 933–937 (2000).
[CrossRef] [PubMed]

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N. C. Shaner, R. E. Campbell, P. A. Steinbach, B. N. Giepmans, A. E. Palmer, R. Y. Tsien, “Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein,” Nat. Biotechnol. 22(12), 1567–1572 (2004).
[CrossRef] [PubMed]

Gillanders, W. E.

A. Krumholz, S. J. Vanvickle-Chavez, J. Yao, T. P. Fleming, W. E. Gillanders, L. V. Wang, “Photoacoustic microscopy of tyrosinase reporter gene in vivo,” J. Biomed. Opt. 16(8), 080503 (2011).
[CrossRef] [PubMed]

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R. L. Strack, B. Hein, D. Bhattacharyya, S. W. Hell, R. J. Keenan, B. S. Glick, “A rapidly maturing far-red derivative of DsRed-Express2 for whole-cell labeling,” Biochemistry 48(35), 8279–8281 (2009).
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B. J. Bevis, B. S. Glick, “Rapidly maturing variants of the Discosoma red fluorescent protein (DsRed),” Nat. Biotechnol. 20(1), 83–87 (2002).
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D. Shcherbo, I. I. Shemiakina, A. V. Ryabova, K. E. Luker, B. T. Schmidt, E. A. Souslova, T. V. Gorodnicheva, L. Strukova, K. M. Shidlovskiy, O. V. Britanova, A. G. Zaraisky, K. A. Lukyanov, V. B. Loschenov, G. D. Luker, D. M. Chudakov, “Near-infrared fluorescent proteins,” Nat. Methods 7(10), 827–829 (2010).
[CrossRef] [PubMed]

Gross, L. A.

M. Z. Lin, M. R. McKeown, H.-L. Ng, T. A. Aguilera, N. C. Shaner, R. E. Campbell, S. R. Adams, L. A. Gross, W. Ma, T. Alber, R. Y. Tsien, “Autofluorescent proteins with excitation in the optical window for intravital imaging in mammals,” Chem. Biol. 16(11), 1169–1179 (2009).
[CrossRef] [PubMed]

Guo, Z.

X. Cai, L. Li, A. Krumholz, Z. Guo, T. N. Erpelding, C. Zhang, Y. Zhang, Y. Xia, L. V. Wang, “Multi-scale molecular photoacoustic tomography of gene expression,” PLoS ONE 7(8), e43999 (2012).
[CrossRef] [PubMed]

Gurskaya, N. G.

M. A. Shkrob, Y. G. Yanushevich, D. M. Chudakov, N. G. Gurskaya, Y. A. Labas, S. Y. Poponov, N. N. Mudrik, S. Lukyanov, K. A. Lukyanov, “Far-red fluorescent proteins evolved from a blue chromoprotein from Actinia equina,” Biochem. J. 392(3), 649–654 (2005).
[CrossRef] [PubMed]

Ha, K. D.

W. P. Stemmer, A. Crameri, K. D. Ha, T. M. Brennan, H. L. Heyneker, “Single-step assembly of a gene and entire plasmid from large numbers of oligodeoxyribonucleotides,” Gene 164(1), 49–53 (1995).
[CrossRef] [PubMed]

Habuchi, S.

M. Cotlet, J. Hofkens, S. Habuchi, G. Dirix, M. Van Guyse, J. Michiels, J. Vanderleyden, F. C. De Schryver, “Identification of different emitting species in the red fluorescent protein DsRed by means of ensemble and single-molecule spectroscopy,” Proc. Natl. Acad. Sci. U.S.A. 98(25), 14398–14403 (2001).
[CrossRef] [PubMed]

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M. R. Soboleski, J. Oaks, W. P. Halford, “Green fluorescent protein is a quantitative reporter of gene expression in individual eukaryotic cells,” FASEB J. 19(3), 440–442 (2005).
[PubMed]

Hazelwood, K. L.

N. C. Shaner, M. Z. Lin, M. R. McKeown, P. A. Steinbach, K. L. Hazelwood, M. W. Davidson, R. Y. Tsien, “Improving the photostability of bright monomeric orange and red fluorescent proteins,” Nat. Methods 5(6), 545–551 (2008).
[CrossRef] [PubMed]

Hein, B.

R. L. Strack, B. Hein, D. Bhattacharyya, S. W. Hell, R. J. Keenan, B. S. Glick, “A rapidly maturing far-red derivative of DsRed-Express2 for whole-cell labeling,” Biochemistry 48(35), 8279–8281 (2009).
[CrossRef] [PubMed]

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R. L. Strack, B. Hein, D. Bhattacharyya, S. W. Hell, R. J. Keenan, B. S. Glick, “A rapidly maturing far-red derivative of DsRed-Express2 for whole-cell labeling,” Biochemistry 48(35), 8279–8281 (2009).
[CrossRef] [PubMed]

Hendrix, J.

J. Hendrix, C. Flors, P. Dedecker, J. Hofkens, Y. Engelborghs, “Dark states in monomeric red fluorescent proteins studied by fluorescence correlation and single molecule spectroscopy,” Biophys. J. 94(10), 4103–4113 (2008).
[CrossRef] [PubMed]

Herschman, H. R.

Y. Yu, A. J. Annala, J. R. Barrio, T. Toyokuni, N. Satyamurthy, M. Namavari, S. R. Cherry, M. E. Phelps, H. R. Herschman, S. S. Gambhir, “Quantification of target gene expression by imaging reporter gene expression in living animals,” Nat. Med. 6(8), 933–937 (2000).
[CrossRef] [PubMed]

Heyneker, H. L.

W. P. Stemmer, A. Crameri, K. D. Ha, T. M. Brennan, H. L. Heyneker, “Single-step assembly of a gene and entire plasmid from large numbers of oligodeoxyribonucleotides,” Gene 164(1), 49–53 (1995).
[CrossRef] [PubMed]

Ho, D.

M. C. Y. Chan, S. Karasawa, H. Mizuno, I. Bosanac, D. Ho, G. G. Privé, A. Miyawaki, M. Ikura, “Structural characterization of a blue chromoprotein and its yellow mutant from the sea anemone Cnidopus japonicus,” J. Biol. Chem. 281(49), 37813–37819 (2006).
[CrossRef] [PubMed]

Hofkens, J.

J. Hendrix, C. Flors, P. Dedecker, J. Hofkens, Y. Engelborghs, “Dark states in monomeric red fluorescent proteins studied by fluorescence correlation and single molecule spectroscopy,” Biophys. J. 94(10), 4103–4113 (2008).
[CrossRef] [PubMed]

M. Cotlet, J. Hofkens, S. Habuchi, G. Dirix, M. Van Guyse, J. Michiels, J. Vanderleyden, F. C. De Schryver, “Identification of different emitting species in the red fluorescent protein DsRed by means of ensemble and single-molecule spectroscopy,” Proc. Natl. Acad. Sci. U.S.A. 98(25), 14398–14403 (2001).
[CrossRef] [PubMed]

Holtom, G. R.

W. Min, S. Lu, S. Chong, R. Roy, G. R. Holtom, X. S. Xie, “Imaging chromophores with undetectable fluorescence by stimulated emission microscopy,” Nature 461(7267), 1105–1109 (2009).
[CrossRef] [PubMed]

Ikura, M.

M. C. Y. Chan, S. Karasawa, H. Mizuno, I. Bosanac, D. Ho, G. G. Privé, A. Miyawaki, M. Ikura, “Structural characterization of a blue chromoprotein and its yellow mutant from the sea anemone Cnidopus japonicus,” J. Biol. Chem. 281(49), 37813–37819 (2006).
[CrossRef] [PubMed]

Jackson, W. C.

L. Wang, W. C. Jackson, P. A. Steinbach, R. Y. Tsien, “Evolution of new nonantibody proteins via iterative somatic hypermutation,” Proc. Natl. Acad. Sci. U.S.A. 101(48), 16745–16749 (2004).
[CrossRef] [PubMed]

Jathoul, A.

J. Laufer, A. Jathoul, P. Johnson, E. Zhang, M. Lythgoe, R. B. Pedley, M. Pule, P. Beard, “In vivo photoacoustic imaging of tyrosinase expressing tumours in mice,” Proc. SPIE 8223, 82230M (2012).
[CrossRef]

Jaye, A. A.

D. Stoner-Ma, A. A. Jaye, P. Matousek, M. Towrie, S. R. Meech, P. J. Tonge, “Observation of excited-state proton transfer in green fluorescent protein using ultrafast vibrational spectroscopy,” J. Am. Chem. Soc. 127(9), 2864–2865 (2005).
[CrossRef] [PubMed]

Johnson, P.

J. Laufer, A. Jathoul, P. Johnson, E. Zhang, M. Lythgoe, R. B. Pedley, M. Pule, P. Beard, “In vivo photoacoustic imaging of tyrosinase expressing tumours in mice,” Proc. SPIE 8223, 82230M (2012).
[CrossRef]

Jones, M. D.

A. N. Warrens, M. D. Jones, R. I. Lechler, “Splicing by overlap extension by PCR using asymmetric amplification: an improved technique for the generation of hybrid proteins of immunological interest,” Gene 186(1), 29–35 (1997).
[CrossRef] [PubMed]

Karasawa, S.

M. C. Y. Chan, S. Karasawa, H. Mizuno, I. Bosanac, D. Ho, G. G. Privé, A. Miyawaki, M. Ikura, “Structural characterization of a blue chromoprotein and its yellow mutant from the sea anemone Cnidopus japonicus,” J. Biol. Chem. 281(49), 37813–37819 (2006).
[CrossRef] [PubMed]

Keenan, R. J.

R. L. Strack, B. Hein, D. Bhattacharyya, S. W. Hell, R. J. Keenan, B. S. Glick, “A rapidly maturing far-red derivative of DsRed-Express2 for whole-cell labeling,” Biochemistry 48(35), 8279–8281 (2009).
[CrossRef] [PubMed]

Kim, K.

G. S. Filonov, K. D. Piatkevich, L.-M. Ting, J. Zhang, K. Kim, V. V. Verkhusha, “Bright and stable near-infrared fluorescent protein for in vivo imaging,” Nat. Biotechnol. 29(8), 757–761 (2011).
[CrossRef] [PubMed]

Köster, R. W.

D. Razansky, M. Distel, C. Vinegoni, R. Ma, N. Perrimon, R. W. Köster, V. Ntziachristos, “Multispectral opto-acoustic tomography of deep-seated fluorescent proteins in vivo,” Nat. Photonics 3(7), 412–417 (2009).
[CrossRef]

Krumholz, A.

X. Cai, L. Li, A. Krumholz, Z. Guo, T. N. Erpelding, C. Zhang, Y. Zhang, Y. Xia, L. V. Wang, “Multi-scale molecular photoacoustic tomography of gene expression,” PLoS ONE 7(8), e43999 (2012).
[CrossRef] [PubMed]

G. S. Filonov, A. Krumholz, J. Xia, J. Yao, L. V. Wang, V. V. Verkhusha, “Deep-tissue photoacoustic tomography of a genetically encoded near-infrared fluorescent probe - supporting information,” Angew. Chem. 124(6), 1477–1480 (2012).
[CrossRef]

A. Krumholz, S. J. Vanvickle-Chavez, J. Yao, T. P. Fleming, W. E. Gillanders, L. V. Wang, “Photoacoustic microscopy of tyrosinase reporter gene in vivo,” J. Biomed. Opt. 16(8), 080503 (2011).
[CrossRef] [PubMed]

Labas, Y. A.

M. A. Shkrob, Y. G. Yanushevich, D. M. Chudakov, N. G. Gurskaya, Y. A. Labas, S. Y. Poponov, N. N. Mudrik, S. Lukyanov, K. A. Lukyanov, “Far-red fluorescent proteins evolved from a blue chromoprotein from Actinia equina,” Biochem. J. 392(3), 649–654 (2005).
[CrossRef] [PubMed]

Laufer, J.

Lechler, R. I.

A. N. Warrens, M. D. Jones, R. I. Lechler, “Splicing by overlap extension by PCR using asymmetric amplification: an improved technique for the generation of hybrid proteins of immunological interest,” Gene 186(1), 29–35 (1997).
[CrossRef] [PubMed]

Li, L.

X. Cai, L. Li, A. Krumholz, Z. Guo, T. N. Erpelding, C. Zhang, Y. Zhang, Y. Xia, L. V. Wang, “Multi-scale molecular photoacoustic tomography of gene expression,” PLoS ONE 7(8), e43999 (2012).
[CrossRef] [PubMed]

L. Li, R. J. Zemp, G. Lungu, G. Stoica, L. V. Wang, “Photoacoustic imaging of lacZ gene expression in vivo,” J. Biomed. Opt. 12(2), 020504 (2007).
[CrossRef] [PubMed]

Lichtman, J. W.

J. W. Lichtman, J. A. Conchello, “Fluorescence microscopy,” Nat. Methods 2(12), 910–919 (2005).
[CrossRef] [PubMed]

Lin, M. Z.

M. Z. Lin, M. R. McKeown, H.-L. Ng, T. A. Aguilera, N. C. Shaner, R. E. Campbell, S. R. Adams, L. A. Gross, W. Ma, T. Alber, R. Y. Tsien, “Autofluorescent proteins with excitation in the optical window for intravital imaging in mammals,” Chem. Biol. 16(11), 1169–1179 (2009).
[CrossRef] [PubMed]

N. C. Shaner, M. Z. Lin, M. R. McKeown, P. A. Steinbach, K. L. Hazelwood, M. W. Davidson, R. Y. Tsien, “Improving the photostability of bright monomeric orange and red fluorescent proteins,” Nat. Methods 5(6), 545–551 (2008).
[CrossRef] [PubMed]

Loschenov, V. B.

D. Shcherbo, I. I. Shemiakina, A. V. Ryabova, K. E. Luker, B. T. Schmidt, E. A. Souslova, T. V. Gorodnicheva, L. Strukova, K. M. Shidlovskiy, O. V. Britanova, A. G. Zaraisky, K. A. Lukyanov, V. B. Loschenov, G. D. Luker, D. M. Chudakov, “Near-infrared fluorescent proteins,” Nat. Methods 7(10), 827–829 (2010).
[CrossRef] [PubMed]

Lu, S.

W. Min, S. Lu, S. Chong, R. Roy, G. R. Holtom, X. S. Xie, “Imaging chromophores with undetectable fluorescence by stimulated emission microscopy,” Nature 461(7267), 1105–1109 (2009).
[CrossRef] [PubMed]

Luker, G. D.

D. Shcherbo, I. I. Shemiakina, A. V. Ryabova, K. E. Luker, B. T. Schmidt, E. A. Souslova, T. V. Gorodnicheva, L. Strukova, K. M. Shidlovskiy, O. V. Britanova, A. G. Zaraisky, K. A. Lukyanov, V. B. Loschenov, G. D. Luker, D. M. Chudakov, “Near-infrared fluorescent proteins,” Nat. Methods 7(10), 827–829 (2010).
[CrossRef] [PubMed]

Luker, K. E.

D. Shcherbo, I. I. Shemiakina, A. V. Ryabova, K. E. Luker, B. T. Schmidt, E. A. Souslova, T. V. Gorodnicheva, L. Strukova, K. M. Shidlovskiy, O. V. Britanova, A. G. Zaraisky, K. A. Lukyanov, V. B. Loschenov, G. D. Luker, D. M. Chudakov, “Near-infrared fluorescent proteins,” Nat. Methods 7(10), 827–829 (2010).
[CrossRef] [PubMed]

Lukyanov, K. A.

D. Shcherbo, I. I. Shemiakina, A. V. Ryabova, K. E. Luker, B. T. Schmidt, E. A. Souslova, T. V. Gorodnicheva, L. Strukova, K. M. Shidlovskiy, O. V. Britanova, A. G. Zaraisky, K. A. Lukyanov, V. B. Loschenov, G. D. Luker, D. M. Chudakov, “Near-infrared fluorescent proteins,” Nat. Methods 7(10), 827–829 (2010).
[CrossRef] [PubMed]

M. A. Shkrob, Y. G. Yanushevich, D. M. Chudakov, N. G. Gurskaya, Y. A. Labas, S. Y. Poponov, N. N. Mudrik, S. Lukyanov, K. A. Lukyanov, “Far-red fluorescent proteins evolved from a blue chromoprotein from Actinia equina,” Biochem. J. 392(3), 649–654 (2005).
[CrossRef] [PubMed]

M. E. Bulina, D. M. Chudakov, N. N. Mudrik, K. A. Lukyanov, “Interconversion of Anthozoa GFP-like fluorescent and non-fluorescent proteins by mutagenesis,” BMC Biochem. 3(1), 7 (2002).
[CrossRef] [PubMed]

Lukyanov, S.

M. A. Shkrob, Y. G. Yanushevich, D. M. Chudakov, N. G. Gurskaya, Y. A. Labas, S. Y. Poponov, N. N. Mudrik, S. Lukyanov, K. A. Lukyanov, “Far-red fluorescent proteins evolved from a blue chromoprotein from Actinia equina,” Biochem. J. 392(3), 649–654 (2005).
[CrossRef] [PubMed]

Lungu, G.

L. Li, R. J. Zemp, G. Lungu, G. Stoica, L. V. Wang, “Photoacoustic imaging of lacZ gene expression in vivo,” J. Biomed. Opt. 12(2), 020504 (2007).
[CrossRef] [PubMed]

Lythgoe, M.

J. Laufer, A. Jathoul, P. Johnson, E. Zhang, M. Lythgoe, R. B. Pedley, M. Pule, P. Beard, “In vivo photoacoustic imaging of tyrosinase expressing tumours in mice,” Proc. SPIE 8223, 82230M (2012).
[CrossRef]

Ma, R.

D. Razansky, M. Distel, C. Vinegoni, R. Ma, N. Perrimon, R. W. Köster, V. Ntziachristos, “Multispectral opto-acoustic tomography of deep-seated fluorescent proteins in vivo,” Nat. Photonics 3(7), 412–417 (2009).
[CrossRef]

Ma, W.

M. Z. Lin, M. R. McKeown, H.-L. Ng, T. A. Aguilera, N. C. Shaner, R. E. Campbell, S. R. Adams, L. A. Gross, W. Ma, T. Alber, R. Y. Tsien, “Autofluorescent proteins with excitation in the optical window for intravital imaging in mammals,” Chem. Biol. 16(11), 1169–1179 (2009).
[CrossRef] [PubMed]

Matousek, P.

D. Stoner-Ma, A. A. Jaye, P. Matousek, M. Towrie, S. R. Meech, P. J. Tonge, “Observation of excited-state proton transfer in green fluorescent protein using ultrafast vibrational spectroscopy,” J. Am. Chem. Soc. 127(9), 2864–2865 (2005).
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G. S. Filonov, K. D. Piatkevich, L.-M. Ting, J. Zhang, K. Kim, V. V. Verkhusha, “Bright and stable near-infrared fluorescent protein for in vivo imaging,” Nat. Biotechnol. 29(8), 757–761 (2011).
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W. Min, S. Lu, S. Chong, R. Roy, G. R. Holtom, X. S. Xie, “Imaging chromophores with undetectable fluorescence by stimulated emission microscopy,” Nature 461(7267), 1105–1109 (2009).
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M. A. Shkrob, Y. G. Yanushevich, D. M. Chudakov, N. G. Gurskaya, Y. A. Labas, S. Y. Poponov, N. N. Mudrik, S. Lukyanov, K. A. Lukyanov, “Far-red fluorescent proteins evolved from a blue chromoprotein from Actinia equina,” Biochem. J. 392(3), 649–654 (2005).
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G. S. Filonov, A. Krumholz, J. Xia, J. Yao, L. V. Wang, V. V. Verkhusha, “Deep-tissue photoacoustic tomography of a genetically encoded near-infrared fluorescent probe - supporting information,” Angew. Chem. 124(6), 1477–1480 (2012).
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Zacharias, D. A.

G. S. Baird, D. A. Zacharias, R. Y. Tsien, “Biochemistry, mutagenesis, and oligomerization of DsRed, a red fluorescent protein from coral,” Proc. Natl. Acad. Sci. U.S.A. 97(22), 11984–11989 (2000).
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Zaraisky, A. G.

D. Shcherbo, I. I. Shemiakina, A. V. Ryabova, K. E. Luker, B. T. Schmidt, E. A. Souslova, T. V. Gorodnicheva, L. Strukova, K. M. Shidlovskiy, O. V. Britanova, A. G. Zaraisky, K. A. Lukyanov, V. B. Loschenov, G. D. Luker, D. M. Chudakov, “Near-infrared fluorescent proteins,” Nat. Methods 7(10), 827–829 (2010).
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Zemp, R. J.

L. Li, R. J. Zemp, G. Lungu, G. Stoica, L. V. Wang, “Photoacoustic imaging of lacZ gene expression in vivo,” J. Biomed. Opt. 12(2), 020504 (2007).
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Zhang, C.

X. Cai, L. Li, A. Krumholz, Z. Guo, T. N. Erpelding, C. Zhang, Y. Zhang, Y. Xia, L. V. Wang, “Multi-scale molecular photoacoustic tomography of gene expression,” PLoS ONE 7(8), e43999 (2012).
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Zhang, E.

Zhang, J.

G. S. Filonov, K. D. Piatkevich, L.-M. Ting, J. Zhang, K. Kim, V. V. Verkhusha, “Bright and stable near-infrared fluorescent protein for in vivo imaging,” Nat. Biotechnol. 29(8), 757–761 (2011).
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Zhang, Y.

X. Cai, L. Li, A. Krumholz, Z. Guo, T. N. Erpelding, C. Zhang, Y. Zhang, Y. Xia, L. V. Wang, “Multi-scale molecular photoacoustic tomography of gene expression,” PLoS ONE 7(8), e43999 (2012).
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Anal. Bioanal. Chem.

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Appl. Opt.

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Biochemistry

R. L. Strack, B. Hein, D. Bhattacharyya, S. W. Hell, R. J. Keenan, B. S. Glick, “A rapidly maturing far-red derivative of DsRed-Express2 for whole-cell labeling,” Biochemistry 48(35), 8279–8281 (2009).
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Biophys. J.

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BMC Biochem.

M. E. Bulina, D. M. Chudakov, N. N. Mudrik, K. A. Lukyanov, “Interconversion of Anthozoa GFP-like fluorescent and non-fluorescent proteins by mutagenesis,” BMC Biochem. 3(1), 7 (2002).
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Chem. Biol.

M. Z. Lin, M. R. McKeown, H.-L. Ng, T. A. Aguilera, N. C. Shaner, R. E. Campbell, S. R. Adams, L. A. Gross, W. Ma, T. Alber, R. Y. Tsien, “Autofluorescent proteins with excitation in the optical window for intravital imaging in mammals,” Chem. Biol. 16(11), 1169–1179 (2009).
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FASEB J.

M. R. Soboleski, J. Oaks, W. P. Halford, “Green fluorescent protein is a quantitative reporter of gene expression in individual eukaryotic cells,” FASEB J. 19(3), 440–442 (2005).
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J. Am. Chem. Soc.

D. Stoner-Ma, A. A. Jaye, P. Matousek, M. Towrie, S. R. Meech, P. J. Tonge, “Observation of excited-state proton transfer in green fluorescent protein using ultrafast vibrational spectroscopy,” J. Am. Chem. Soc. 127(9), 2864–2865 (2005).
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J. Biomed. Opt.

A. Krumholz, S. J. Vanvickle-Chavez, J. Yao, T. P. Fleming, W. E. Gillanders, L. V. Wang, “Photoacoustic microscopy of tyrosinase reporter gene in vivo,” J. Biomed. Opt. 16(8), 080503 (2011).
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L. Li, R. J. Zemp, G. Lungu, G. Stoica, L. V. Wang, “Photoacoustic imaging of lacZ gene expression in vivo,” J. Biomed. Opt. 12(2), 020504 (2007).
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Meas. Sci. Technol.

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Nat. Biotechnol.

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G. S. Filonov, K. D. Piatkevich, L.-M. Ting, J. Zhang, K. Kim, V. V. Verkhusha, “Bright and stable near-infrared fluorescent protein for in vivo imaging,” Nat. Biotechnol. 29(8), 757–761 (2011).
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N. C. Shaner, R. E. Campbell, P. A. Steinbach, B. N. Giepmans, A. E. Palmer, R. Y. Tsien, “Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein,” Nat. Biotechnol. 22(12), 1567–1572 (2004).
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Nat. Med.

Y. Yu, A. J. Annala, J. R. Barrio, T. Toyokuni, N. Satyamurthy, M. Namavari, S. R. Cherry, M. E. Phelps, H. R. Herschman, S. S. Gambhir, “Quantification of target gene expression by imaging reporter gene expression in living animals,” Nat. Med. 6(8), 933–937 (2000).
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Nat. Methods

D. Shcherbo, I. I. Shemiakina, A. V. Ryabova, K. E. Luker, B. T. Schmidt, E. A. Souslova, T. V. Gorodnicheva, L. Strukova, K. M. Shidlovskiy, O. V. Britanova, A. G. Zaraisky, K. A. Lukyanov, V. B. Loschenov, G. D. Luker, D. M. Chudakov, “Near-infrared fluorescent proteins,” Nat. Methods 7(10), 827–829 (2010).
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N. C. Shaner, M. Z. Lin, M. R. McKeown, P. A. Steinbach, K. L. Hazelwood, M. W. Davidson, R. Y. Tsien, “Improving the photostability of bright monomeric orange and red fluorescent proteins,” Nat. Methods 5(6), 545–551 (2008).
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Nat. Photonics

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Nature

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Phys. Med. Biol.

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PLoS ONE

X. Cai, L. Li, A. Krumholz, Z. Guo, T. N. Erpelding, C. Zhang, Y. Zhang, Y. Xia, L. V. Wang, “Multi-scale molecular photoacoustic tomography of gene expression,” PLoS ONE 7(8), e43999 (2012).
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Proc. Natl. Acad. Sci. U.S.A.

L. Wang, W. C. Jackson, P. A. Steinbach, R. Y. Tsien, “Evolution of new nonantibody proteins via iterative somatic hypermutation,” Proc. Natl. Acad. Sci. U.S.A. 101(48), 16745–16749 (2004).
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G. S. Baird, D. A. Zacharias, R. Y. Tsien, “Biochemistry, mutagenesis, and oligomerization of DsRed, a red fluorescent protein from coral,” Proc. Natl. Acad. Sci. U.S.A. 97(22), 11984–11989 (2000).
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M. Cotlet, J. Hofkens, S. Habuchi, G. Dirix, M. Van Guyse, J. Michiels, J. Vanderleyden, F. C. De Schryver, “Identification of different emitting species in the red fluorescent protein DsRed by means of ensemble and single-molecule spectroscopy,” Proc. Natl. Acad. Sci. U.S.A. 98(25), 14398–14403 (2001).
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Proc. SPIE

J. Laufer, A. Jathoul, P. Johnson, E. Zhang, M. Lythgoe, R. B. Pedley, M. Pule, P. Beard, “In vivo photoacoustic imaging of tyrosinase expressing tumours in mice,” Proc. SPIE 8223, 82230M (2012).
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Figures (7)

Fig. 1
Fig. 1

Experimental set-up for measuring the photoacoustic signal amplitude in sample solutions of purified fluorescent proteins and chromoproteins.

Fig. 2
Fig. 2

Photoacoustic spectra (circles) of purified fluorescent protein solutions of (a) mCherry, (b) mRaspberry, (c) E2 Crimson, (d) mNeptune, (e) AQ143, and (f) dsRed in distilled water (triangles represent a repeat measurement after 24h) together with their specific extinction coefficient spectra (dashed lines). The error bars represent the standard deviation of the photoacoustic measurements.

Fig. 3
Fig. 3

Photoacoustic spectra (circles) of purified chromoprotein solutions of (a) cjBlue, (b) aeCP597, and (c) E2 Crimson NF in distilled water. The corresponding specific extinction coefficient spectra are shown as a dashed line. The error bars represent the standard deviation of the photoacoustic measurements.

Fig. 4
Fig. 4

Absorption-normalized photoacoustic spectra of fluorescent proteins (mNeptune, mRaspberry, mCherry, E2 Crimson) and chromoproteins (aeCP597, cjBlue, E2 Crimson NF).

Fig. 5
Fig. 5

Photobleaching of fluorescent proteins and chromoproteins under prolonged exposure to nanosecond laser pulses. The fluence at the sample ranged from 1.5 to 1.7 mJ cm−2.

Fig. 6
Fig. 6

(a) Photoacoustic amplitude spectra of normal type (NT) and aeCP597-expressing mammalian tumor cells (K562). (b) The difference in the spectra shown in (a) and the specific extinction spectrum of aeCP597.

Fig. 7
Fig. 7

Histogram of a fluorescence activated cell sorting (FACS) analysis of the expression levels of the CD34 surface protein, which was co-expressed with aeCP597, in normal type (NT) and transduced K562 cells.

Tables (1)

Tables Icon

Table 1 Reported properties of selected fluorescent proteins and chromoproteins (italics).

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