Abstract

Third harmonic generation (THG) microscopy can exploit endogenous harmonophores such as pigment macromolecules for enhanced image contrast, and therefore can be used without exogenous contrast agents. Previous studies have established that carotenoid compounds are ideal harmonophores for THG microscopy; we therefore sought to determine whether THG from endogenous carotenoid-derived compounds, such as retinal in photoreceptor cells, could serve as a new label-free method for developmental studies. Here we study the development of the pupal eye in Drosophila melanogaster and determine the localization of rhodopsin using THG microscopy technique. Additionally, by altering the chromophore or the opsin protein we were able to detect changes in both the retinal distribution morphology and in THG intensity age-dependent profiles. These results demonstrate that THG microscopy can be used to detect altered photoreceptor development and may be useful in clinically relevant conditions associated with photoreceptor degeneration.

© 2017 Optical Society of America

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    [Crossref] [PubMed]
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    [Crossref] [PubMed]
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  23. J. E. Treisman, “Retinal differentiation in Drosophila,” Wiley Interdiscip. Rev. Dev. Biol. 2(4), 545–557 (2013).
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2013 (1)

J. E. Treisman, “Retinal differentiation in Drosophila,” Wiley Interdiscip. Rev. Dev. Biol. 2(4), 545–557 (2013).
[Crossref] [PubMed]

2012 (5)

D. Tokarz, R. Cisek, M. Garbaczewska, D. Sandkuijl, X. Qiu, B. Stewart, J. D. Levine, U. Fekl, and V. Barzda, “Carotenoid based bio-compatible labels for third harmonic generation microscopy,” Phys. Chem. Chem. Phys. 14(30), 10653–10661 (2012).
[Crossref] [PubMed]

C. Montell, “Drosophila visual transduction,” Trends Neurosci. 35(6), 356–363 (2012).
[Crossref] [PubMed]

C. A. Schneider, W. S. Rasband, and K. W. Eliceiri, “NIH Image to ImageJ: 25 years of image analysis,” Nat. Methods 9(7), 671–675 (2012).
[Crossref] [PubMed]

J. P. Kumar, “Building an ommatidium one cell at a time,” Dev. Dyn. 241(1), 136–149 (2012).
[Crossref] [PubMed]

D. Tokarz, R. Cisek, N. Prent, U. Fekl, and V. Barzda, “Measuring the molecular second hyperpolarizability in absorptive solutions by the third harmonic generation ratio technique,” Anal. Chim. Acta 755, 86–92 (2012).
[Crossref] [PubMed]

2011 (1)

E. A. Gibson, O. Masihzadeh, T. C. Lei, D. A. Ammar, and M. Y. Kahook, “Multiphoton microscopy for ophthalmic imaging,” J. Ophthalmol. 2011, 870879 (2011).
[Crossref] [PubMed]

2009 (2)

R. Carriles, D. N. Schafer, K. E. Sheetz, J. J. Field, R. Cisek, V. Barzda, A. W. Sylvester, and J. A. Squier, “Invited review article: Imaging techniques for harmonic and multiphoton absorption fluorescence microscopy,” Rev. Sci. Instrum. 80(8), 081101 (2009).
[Crossref] [PubMed]

A. Major, D. Sandkuijl, and V. Barzda, “Efficient frequency doubling of a femtosecond Yb:KGW laser in a BiB3O6 crystal,” Opt. Express 17(14), 12039–12042 (2009).
[Crossref] [PubMed]

2007 (2)

T. Wang, Y. Jiao, and C. Montell, “Dissection of the pathway required for generation of vitamin A and for Drosophila phototransduction,” J. Cell Biol. 177(2), 305–316 (2007).
[Crossref] [PubMed]

T. Wang and C. Montell, “Phototransduction and retinal degeneration in Drosophila,” Pflugers Arch. 454(5), 821–847 (2007).
[Crossref] [PubMed]

2004 (1)

F. J. Kao, “The Use of Optical Parametric Oscillator for Harmonic Generation and Two-Photon UV Fluorescence Microscopy,” Microsc. Res. Tech. 63(3), 175–181 (2004).
[Crossref] [PubMed]

2001 (1)

1995 (2)

J. P. Kumar and D. F. Ready, “Rhodopsin plays an essential structural role in Drosophila photoreceptor Development,” Development 121(12), 4359–4370 (1995).
[PubMed]

T. Y. F. Tsang, “Optical third-harmonic generation at interfaces,” Phys. Rev. A 52(5), 4116–4125 (1995).
[Crossref] [PubMed]

1989 (4)

R. L. Cagan and D. F. Ready, “The emergence of order in the Drosophila pupal retina,” Dev. Biol. 136(2), 346–362 (1989).
[Crossref] [PubMed]

D. F. Ready, “A Multifaceted Approach to Neural Development,” Trends Neurosci. 12(3), 102–110 (1989).
[Crossref] [PubMed]

T. Washburn and J. E. O’Tousa, “Molecular defects in drosophila rhodopsin mutants,” J. Biol. Chem. 264(26), 15464–15466 (1989).
[PubMed]

T. Washburn and J. E. O’Tousa, “Molecular defects in Drosophila rhodopsin mutants,” J. Biol. Chem. 264(26), 15464–15466 (1989).
[PubMed]

1988 (1)

J. R. Heflin, K. Y. Wong, O. Zamani-Khamiri, and A. F. Garito, “Nonlinear optical properties of linear chains and electron-correlation effects,” Phys. Rev. B Condens. Matter 38(2), 1573–1576 (1988).
[Crossref] [PubMed]

1987 (1)

A. F. Garito and K. Y. Wong, “Nonlinear optical processes in organic and polymer structures,” Polym. J. 19(1), 51 (1987).
[Crossref]

1977 (1)

W. A. Harris, D. F. Ready, E. D. Lipson, A. J. Hudspeth, and W. S. Stark, “Vitamin A deprivation and Drosophila photopigments,” Nature 266(5603), 648–650 (1977).
[Crossref] [PubMed]

Ammar, D. A.

E. A. Gibson, O. Masihzadeh, T. C. Lei, D. A. Ammar, and M. Y. Kahook, “Multiphoton microscopy for ophthalmic imaging,” J. Ophthalmol. 2011, 870879 (2011).
[Crossref] [PubMed]

Barzda, V.

D. Tokarz, R. Cisek, M. Garbaczewska, D. Sandkuijl, X. Qiu, B. Stewart, J. D. Levine, U. Fekl, and V. Barzda, “Carotenoid based bio-compatible labels for third harmonic generation microscopy,” Phys. Chem. Chem. Phys. 14(30), 10653–10661 (2012).
[Crossref] [PubMed]

D. Tokarz, R. Cisek, N. Prent, U. Fekl, and V. Barzda, “Measuring the molecular second hyperpolarizability in absorptive solutions by the third harmonic generation ratio technique,” Anal. Chim. Acta 755, 86–92 (2012).
[Crossref] [PubMed]

R. Carriles, D. N. Schafer, K. E. Sheetz, J. J. Field, R. Cisek, V. Barzda, A. W. Sylvester, and J. A. Squier, “Invited review article: Imaging techniques for harmonic and multiphoton absorption fluorescence microscopy,” Rev. Sci. Instrum. 80(8), 081101 (2009).
[Crossref] [PubMed]

A. Major, D. Sandkuijl, and V. Barzda, “Efficient frequency doubling of a femtosecond Yb:KGW laser in a BiB3O6 crystal,” Opt. Express 17(14), 12039–12042 (2009).
[Crossref] [PubMed]

Cagan, R. L.

R. L. Cagan and D. F. Ready, “The emergence of order in the Drosophila pupal retina,” Dev. Biol. 136(2), 346–362 (1989).
[Crossref] [PubMed]

Carriles, R.

R. Carriles, D. N. Schafer, K. E. Sheetz, J. J. Field, R. Cisek, V. Barzda, A. W. Sylvester, and J. A. Squier, “Invited review article: Imaging techniques for harmonic and multiphoton absorption fluorescence microscopy,” Rev. Sci. Instrum. 80(8), 081101 (2009).
[Crossref] [PubMed]

Chen, I. H.

Chen, P. C.

Chu, S. W.

Cisek, R.

D. Tokarz, R. Cisek, M. Garbaczewska, D. Sandkuijl, X. Qiu, B. Stewart, J. D. Levine, U. Fekl, and V. Barzda, “Carotenoid based bio-compatible labels for third harmonic generation microscopy,” Phys. Chem. Chem. Phys. 14(30), 10653–10661 (2012).
[Crossref] [PubMed]

D. Tokarz, R. Cisek, N. Prent, U. Fekl, and V. Barzda, “Measuring the molecular second hyperpolarizability in absorptive solutions by the third harmonic generation ratio technique,” Anal. Chim. Acta 755, 86–92 (2012).
[Crossref] [PubMed]

R. Carriles, D. N. Schafer, K. E. Sheetz, J. J. Field, R. Cisek, V. Barzda, A. W. Sylvester, and J. A. Squier, “Invited review article: Imaging techniques for harmonic and multiphoton absorption fluorescence microscopy,” Rev. Sci. Instrum. 80(8), 081101 (2009).
[Crossref] [PubMed]

Elgin, S.C.R.

S.C.R. Elgin and D.W. Miller, “Mass rearing of flies and mass production and harvesting embryos,” (1978)

Eliceiri, K. W.

C. A. Schneider, W. S. Rasband, and K. W. Eliceiri, “NIH Image to ImageJ: 25 years of image analysis,” Nat. Methods 9(7), 671–675 (2012).
[Crossref] [PubMed]

Fekl, U.

D. Tokarz, R. Cisek, M. Garbaczewska, D. Sandkuijl, X. Qiu, B. Stewart, J. D. Levine, U. Fekl, and V. Barzda, “Carotenoid based bio-compatible labels for third harmonic generation microscopy,” Phys. Chem. Chem. Phys. 14(30), 10653–10661 (2012).
[Crossref] [PubMed]

D. Tokarz, R. Cisek, N. Prent, U. Fekl, and V. Barzda, “Measuring the molecular second hyperpolarizability in absorptive solutions by the third harmonic generation ratio technique,” Anal. Chim. Acta 755, 86–92 (2012).
[Crossref] [PubMed]

Field, J. J.

R. Carriles, D. N. Schafer, K. E. Sheetz, J. J. Field, R. Cisek, V. Barzda, A. W. Sylvester, and J. A. Squier, “Invited review article: Imaging techniques for harmonic and multiphoton absorption fluorescence microscopy,” Rev. Sci. Instrum. 80(8), 081101 (2009).
[Crossref] [PubMed]

Garbaczewska, M.

D. Tokarz, R. Cisek, M. Garbaczewska, D. Sandkuijl, X. Qiu, B. Stewart, J. D. Levine, U. Fekl, and V. Barzda, “Carotenoid based bio-compatible labels for third harmonic generation microscopy,” Phys. Chem. Chem. Phys. 14(30), 10653–10661 (2012).
[Crossref] [PubMed]

Garito, A. F.

J. R. Heflin, K. Y. Wong, O. Zamani-Khamiri, and A. F. Garito, “Nonlinear optical properties of linear chains and electron-correlation effects,” Phys. Rev. B Condens. Matter 38(2), 1573–1576 (1988).
[Crossref] [PubMed]

A. F. Garito and K. Y. Wong, “Nonlinear optical processes in organic and polymer structures,” Polym. J. 19(1), 51 (1987).
[Crossref]

Gibson, E. A.

E. A. Gibson, O. Masihzadeh, T. C. Lei, D. A. Ammar, and M. Y. Kahook, “Multiphoton microscopy for ophthalmic imaging,” J. Ophthalmol. 2011, 870879 (2011).
[Crossref] [PubMed]

Harris, W. A.

W. A. Harris, D. F. Ready, E. D. Lipson, A. J. Hudspeth, and W. S. Stark, “Vitamin A deprivation and Drosophila photopigments,” Nature 266(5603), 648–650 (1977).
[Crossref] [PubMed]

Heflin, J. R.

J. R. Heflin, K. Y. Wong, O. Zamani-Khamiri, and A. F. Garito, “Nonlinear optical properties of linear chains and electron-correlation effects,” Phys. Rev. B Condens. Matter 38(2), 1573–1576 (1988).
[Crossref] [PubMed]

Hudspeth, A. J.

W. A. Harris, D. F. Ready, E. D. Lipson, A. J. Hudspeth, and W. S. Stark, “Vitamin A deprivation and Drosophila photopigments,” Nature 266(5603), 648–650 (1977).
[Crossref] [PubMed]

Jiao, Y.

T. Wang, Y. Jiao, and C. Montell, “Dissection of the pathway required for generation of vitamin A and for Drosophila phototransduction,” J. Cell Biol. 177(2), 305–316 (2007).
[Crossref] [PubMed]

Kahook, M. Y.

E. A. Gibson, O. Masihzadeh, T. C. Lei, D. A. Ammar, and M. Y. Kahook, “Multiphoton microscopy for ophthalmic imaging,” J. Ophthalmol. 2011, 870879 (2011).
[Crossref] [PubMed]

Kao, F. J.

F. J. Kao, “The Use of Optical Parametric Oscillator for Harmonic Generation and Two-Photon UV Fluorescence Microscopy,” Microsc. Res. Tech. 63(3), 175–181 (2004).
[Crossref] [PubMed]

Kumar, J. P.

J. P. Kumar, “Building an ommatidium one cell at a time,” Dev. Dyn. 241(1), 136–149 (2012).
[Crossref] [PubMed]

J. P. Kumar and D. F. Ready, “Rhodopsin plays an essential structural role in Drosophila photoreceptor Development,” Development 121(12), 4359–4370 (1995).
[PubMed]

Lei, T. C.

E. A. Gibson, O. Masihzadeh, T. C. Lei, D. A. Ammar, and M. Y. Kahook, “Multiphoton microscopy for ophthalmic imaging,” J. Ophthalmol. 2011, 870879 (2011).
[Crossref] [PubMed]

Levine, J. D.

D. Tokarz, R. Cisek, M. Garbaczewska, D. Sandkuijl, X. Qiu, B. Stewart, J. D. Levine, U. Fekl, and V. Barzda, “Carotenoid based bio-compatible labels for third harmonic generation microscopy,” Phys. Chem. Chem. Phys. 14(30), 10653–10661 (2012).
[Crossref] [PubMed]

Lin, B. L.

Lipson, E. D.

W. A. Harris, D. F. Ready, E. D. Lipson, A. J. Hudspeth, and W. S. Stark, “Vitamin A deprivation and Drosophila photopigments,” Nature 266(5603), 648–650 (1977).
[Crossref] [PubMed]

Liu, T. M.

Major, A.

Masihzadeh, O.

E. A. Gibson, O. Masihzadeh, T. C. Lei, D. A. Ammar, and M. Y. Kahook, “Multiphoton microscopy for ophthalmic imaging,” J. Ophthalmol. 2011, 870879 (2011).
[Crossref] [PubMed]

Miller, D.W.

S.C.R. Elgin and D.W. Miller, “Mass rearing of flies and mass production and harvesting embryos,” (1978)

Montell, C.

C. Montell, “Drosophila visual transduction,” Trends Neurosci. 35(6), 356–363 (2012).
[Crossref] [PubMed]

T. Wang, Y. Jiao, and C. Montell, “Dissection of the pathway required for generation of vitamin A and for Drosophila phototransduction,” J. Cell Biol. 177(2), 305–316 (2007).
[Crossref] [PubMed]

T. Wang and C. Montell, “Phototransduction and retinal degeneration in Drosophila,” Pflugers Arch. 454(5), 821–847 (2007).
[Crossref] [PubMed]

O’Tousa, J. E.

T. Washburn and J. E. O’Tousa, “Molecular defects in Drosophila rhodopsin mutants,” J. Biol. Chem. 264(26), 15464–15466 (1989).
[PubMed]

T. Washburn and J. E. O’Tousa, “Molecular defects in drosophila rhodopsin mutants,” J. Biol. Chem. 264(26), 15464–15466 (1989).
[PubMed]

Prent, N.

D. Tokarz, R. Cisek, N. Prent, U. Fekl, and V. Barzda, “Measuring the molecular second hyperpolarizability in absorptive solutions by the third harmonic generation ratio technique,” Anal. Chim. Acta 755, 86–92 (2012).
[Crossref] [PubMed]

Qiu, X.

D. Tokarz, R. Cisek, M. Garbaczewska, D. Sandkuijl, X. Qiu, B. Stewart, J. D. Levine, U. Fekl, and V. Barzda, “Carotenoid based bio-compatible labels for third harmonic generation microscopy,” Phys. Chem. Chem. Phys. 14(30), 10653–10661 (2012).
[Crossref] [PubMed]

Rasband, W. S.

C. A. Schneider, W. S. Rasband, and K. W. Eliceiri, “NIH Image to ImageJ: 25 years of image analysis,” Nat. Methods 9(7), 671–675 (2012).
[Crossref] [PubMed]

Ready, D. F.

J. P. Kumar and D. F. Ready, “Rhodopsin plays an essential structural role in Drosophila photoreceptor Development,” Development 121(12), 4359–4370 (1995).
[PubMed]

R. L. Cagan and D. F. Ready, “The emergence of order in the Drosophila pupal retina,” Dev. Biol. 136(2), 346–362 (1989).
[Crossref] [PubMed]

D. F. Ready, “A Multifaceted Approach to Neural Development,” Trends Neurosci. 12(3), 102–110 (1989).
[Crossref] [PubMed]

W. A. Harris, D. F. Ready, E. D. Lipson, A. J. Hudspeth, and W. S. Stark, “Vitamin A deprivation and Drosophila photopigments,” Nature 266(5603), 648–650 (1977).
[Crossref] [PubMed]

Sandkuijl, D.

D. Tokarz, R. Cisek, M. Garbaczewska, D. Sandkuijl, X. Qiu, B. Stewart, J. D. Levine, U. Fekl, and V. Barzda, “Carotenoid based bio-compatible labels for third harmonic generation microscopy,” Phys. Chem. Chem. Phys. 14(30), 10653–10661 (2012).
[Crossref] [PubMed]

A. Major, D. Sandkuijl, and V. Barzda, “Efficient frequency doubling of a femtosecond Yb:KGW laser in a BiB3O6 crystal,” Opt. Express 17(14), 12039–12042 (2009).
[Crossref] [PubMed]

Schafer, D. N.

R. Carriles, D. N. Schafer, K. E. Sheetz, J. J. Field, R. Cisek, V. Barzda, A. W. Sylvester, and J. A. Squier, “Invited review article: Imaging techniques for harmonic and multiphoton absorption fluorescence microscopy,” Rev. Sci. Instrum. 80(8), 081101 (2009).
[Crossref] [PubMed]

Schneider, C. A.

C. A. Schneider, W. S. Rasband, and K. W. Eliceiri, “NIH Image to ImageJ: 25 years of image analysis,” Nat. Methods 9(7), 671–675 (2012).
[Crossref] [PubMed]

Sheetz, K. E.

R. Carriles, D. N. Schafer, K. E. Sheetz, J. J. Field, R. Cisek, V. Barzda, A. W. Sylvester, and J. A. Squier, “Invited review article: Imaging techniques for harmonic and multiphoton absorption fluorescence microscopy,” Rev. Sci. Instrum. 80(8), 081101 (2009).
[Crossref] [PubMed]

Squier, J. A.

R. Carriles, D. N. Schafer, K. E. Sheetz, J. J. Field, R. Cisek, V. Barzda, A. W. Sylvester, and J. A. Squier, “Invited review article: Imaging techniques for harmonic and multiphoton absorption fluorescence microscopy,” Rev. Sci. Instrum. 80(8), 081101 (2009).
[Crossref] [PubMed]

Stark, W. S.

W. A. Harris, D. F. Ready, E. D. Lipson, A. J. Hudspeth, and W. S. Stark, “Vitamin A deprivation and Drosophila photopigments,” Nature 266(5603), 648–650 (1977).
[Crossref] [PubMed]

Stewart, B.

D. Tokarz, R. Cisek, M. Garbaczewska, D. Sandkuijl, X. Qiu, B. Stewart, J. D. Levine, U. Fekl, and V. Barzda, “Carotenoid based bio-compatible labels for third harmonic generation microscopy,” Phys. Chem. Chem. Phys. 14(30), 10653–10661 (2012).
[Crossref] [PubMed]

Sun, C. K.

Sylvester, A. W.

R. Carriles, D. N. Schafer, K. E. Sheetz, J. J. Field, R. Cisek, V. Barzda, A. W. Sylvester, and J. A. Squier, “Invited review article: Imaging techniques for harmonic and multiphoton absorption fluorescence microscopy,” Rev. Sci. Instrum. 80(8), 081101 (2009).
[Crossref] [PubMed]

Tokarz, D.

D. Tokarz, R. Cisek, M. Garbaczewska, D. Sandkuijl, X. Qiu, B. Stewart, J. D. Levine, U. Fekl, and V. Barzda, “Carotenoid based bio-compatible labels for third harmonic generation microscopy,” Phys. Chem. Chem. Phys. 14(30), 10653–10661 (2012).
[Crossref] [PubMed]

D. Tokarz, R. Cisek, N. Prent, U. Fekl, and V. Barzda, “Measuring the molecular second hyperpolarizability in absorptive solutions by the third harmonic generation ratio technique,” Anal. Chim. Acta 755, 86–92 (2012).
[Crossref] [PubMed]

Treisman, J. E.

J. E. Treisman, “Retinal differentiation in Drosophila,” Wiley Interdiscip. Rev. Dev. Biol. 2(4), 545–557 (2013).
[Crossref] [PubMed]

Tsang, T. Y. F.

T. Y. F. Tsang, “Optical third-harmonic generation at interfaces,” Phys. Rev. A 52(5), 4116–4125 (1995).
[Crossref] [PubMed]

Wang, T.

T. Wang and C. Montell, “Phototransduction and retinal degeneration in Drosophila,” Pflugers Arch. 454(5), 821–847 (2007).
[Crossref] [PubMed]

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Anal. Chim. Acta (1)

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D. Tokarz, R. Cisek, M. Garbaczewska, D. Sandkuijl, X. Qiu, B. Stewart, J. D. Levine, U. Fekl, and V. Barzda, “Carotenoid based bio-compatible labels for third harmonic generation microscopy,” Phys. Chem. Chem. Phys. 14(30), 10653–10661 (2012).
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Figures (6)

Fig. 1
Fig. 1

THG microscopy images of the developing retina during the pupal stage along with a schematic of an ommatidium. (A) A simplified schematic of a single ommatidium showing three focal depths of interest. (B) THG images at the three focal depths of interest (rows) at four stages of pupal development (columns, %). Images are normalized to excitation energy. The scale bar represents 10 µm.

Fig. 2
Fig. 2

A method to measure the localized THG intensity, and corresponding THG intensity-dependent curve for w1118 pupal retinas. The THG localized in either the pigment cells (A) or in the rhabdomeres (B) were measured. (C) The resulting THG intensity graph shows changes in THG intensities of the pigment cells and the rhabdomeres during pupal development. Highlighted regions in (A) and (B) are used to calculate the THG intensities. Error bars represent standard error of the average THG intensity measured from 11 pupae.

Fig. 3
Fig. 3

THG microscopy images of the vitamin A deficient developing retina during the pupal stage. Three focal depths of interest (see Fig. 1(A)) are shown in rows, and pupal development stages are shown in columns. The scale bar represents 10 µm.

Fig. 4
Fig. 4

THG intensity curves localized in pigment cells and in the rhabdomeres in vitamin A deficient pupae in comparison to cornmeal reared w1118. (A) Comparison of the THG intensities in pigment cells. (B) Comparison of the THG intensities in the rhabdomeres.

Fig. 5
Fig. 5

THG images of pigment cells and rhabdomeres during the latter stages in each ninaE mutant. For each genotype, THG images of the pigment cells and rhabdomeres are shown for 64 and 80% pd. Scale bar represents 10 µm.

Fig. 6
Fig. 6

Comparison of THG intensities between ninaE mutants and the control pupal retinas. (A) THG intensities localized in the pigment cells of each mutant were shown to produce a different curve compared to the wild type. (B) THG intensities localized in the rhabdomeres in each mutant were found to have a similar curve as the wild type until 64% pd.

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