Abstract

Standard histopathology techniques (including paraffin embedding) are incompatible with thick tissue multiphoton imaging, and standard clearing techniques on those specimens destroy some molecular information. We demonstrate multiphoton imaging in specimens prepared according to standard histopathology techniques. This permits unlabeled 3-dimensional histology on archival tissue banks, which is of great value in evaluating prognostic indicators.

© 2012 OSA

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2012

2011

P. Mahou, N. Olivier, G. Labroille, L. Duloquin, J.-M. Sintes, N. Peyriéras, R. Legouis, D. Débarre, and E. Beaurepaire, “Combined third-harmonic generation and four-wave mixing microscopy of tissues and embryos,” Biomed. Opt. Express2(10), 2837–2849 (2011).
[CrossRef] [PubMed]

O. Katz, E. Small, Y. Bromberg, and Y. Silberberg, “Focusing and compression of ultrashort pulses through scattering media,” Nat. Photonics5(6), 372–377 (2011).
[CrossRef]

T. E. Matthews, J. W. Wilson, S. Degan, M. J. Simpson, J. Y. Jin, J. Y. Zhang, and W. S. Warren, “In vivo and ex vivo epi-mode pump-probe imaging of melanin and microvasculature,” Biomed. Opt. Express2(6), 1576–1583 (2011).
[CrossRef] [PubMed]

W. Min, C. W. Freudiger, S. Lu, and X. S. Xie, “Coherent nonlinear optical imaging: beyond fluorescence microscopy,” Annu. Rev. Phys. Chem.62(1), 507–530 (2011).
[CrossRef] [PubMed]

T. E. Matthews, I. R. Piletic, M. A. Selim, M. J. Simpson, and W. S. Warren, “Pump-probe imaging differentiates melanoma from melanocytic nevi,” Sci. Transl. Med.3(71), 71ra15 (2011).
[CrossRef] [PubMed]

H. Hama, H. Kurokawa, H. Kawano, R. Ando, T. Shimogori, H. Noda, K. Fukami, A. Sakaue-Sawano, and A. Miyawaki, “Scale: a chemical approach for fluorescence imaging and reconstruction of transparent mouse brain,” Nat. Neurosci.14(11), 1481–1488 (2011).
[CrossRef] [PubMed]

M. A. Smith, E. L. Barnes, and S. I. Chiosea, “Pathology archive: evaluation of integrity, regulatory compliance, and construction of searchable database from print reports,” Am. J. Clin. Pathol.135(5), 753–759 (2011).
[CrossRef] [PubMed]

J. Wang, Y. Liang, S. Zhang, Y. Zhou, H. Ni, and Y. Li, “Evaluation of optical clearing with the combined liquid paraffin and glycerol mixture,” Biomed. Opt. Express2(8), 2329–2338 (2011).
[CrossRef] [PubMed]

2010

N. Sudheendran, M. Mohamed, M. G. Ghosn, V. V. Tuchin, and K. V. Larin, “Assessment of tissue optical clearing as a function of glucose concentration using optical coherence tomography,” J. Innov. Opt. Health Sci.03(3), 169–176 (2010).
[CrossRef] [PubMed]

E. A. Genina, A. N. Bashkatov, and V. V. Tuchin, “Tissue optical immersion clearing,” Expert Rev. Med. Devices7(6), 825–842 (2010).
[CrossRef] [PubMed]

S. G. Parra, T. H. Chia, J. P. Zinter, and M. J. Levene, “Multiphoton microscopy of cleared mouse organs,” J. Biomed. Opt.15(3), 036017 (2010).
[CrossRef] [PubMed]

U. Leischner, A. Schierloh, W. Zieglgänsberger, and H.-U. Dodt, “Formalin-induced fluorescence reveals cell shape and morphology in biological tissue samples,” PLoS ONE5(4), e10391 (2010).
[CrossRef] [PubMed]

2009

2007

H.-U. Dodt, U. Leischner, A. Schierloh, N. Jährling, C. P. Mauch, K. Deininger, J. M. Deussing, M. Eder, W. Zieglgänsberger, and K. Becker, “Ultramicroscopy: three-dimensional visualization of neuronal networks in the whole mouse brain,” Nat. Methods4(4), 331–336 (2007).
[CrossRef] [PubMed]

D. Fu, T. Ye, T. E. Matthews, G. Yurtsever, and W. S. Warren, “Two-color, two-photon, and excited-state absorption microscopy,” J. Biomed. Opt.12(5), 054004 (2007).
[CrossRef] [PubMed]

2006

S. V. Plotnikov, A. C. Millard, P. J. Campagnola, and W. A. Mohler, “Characterization of the myosin-based source for second-harmonic generation from muscle sarcomeres,” Biophys. J.90(2), 693–703 (2006).
[CrossRef] [PubMed]

R. M. Zucker, “Whole insect and mammalian embryo imaging with confocal microscopy: morphology and apoptosis,” Cytometry A69A(11), 1143–1152 (2006).
[CrossRef] [PubMed]

P. Theer and W. Denk, “On the fundamental imaging-depth limit in two-photon microscopy,” J. Opt. Soc. Am. A23(12), 3139–3149 (2006).
[CrossRef] [PubMed]

2005

V. V. Tuchin, “Optical clearing of tissues and blood using the immersion method,” J. Phys. D Appl. Phys.38(15), 2497–2518 (2005).
[CrossRef]

2003

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

A. T. Yeh, B. Choi, J. S. Nelson, and B. J. Tromberg, “Reversible dissociation of collagen in tissues,” J. Invest. Dermatol.121(6), 1332–1335 (2003).
[CrossRef] [PubMed]

C.-K. Sun, C.-C. Chen, S.-W. Chu, T.-H. Tsai, Y.-C. Chen, and B.-L. Lin, “Multiharmonic-generation biopsy of skin,” Opt. Lett.28(24), 2488–2490 (2003).
[CrossRef] [PubMed]

2002

P. J. Campagnola, A. C. Millard, M. Terasaki, P. E. Hoppe, C. J. Malone, and W. A. Mohler, “Three-dimensional high-resolution second-harmonic generation imaging of endogenous structural proteins in biological tissues,” Biophys. J.82(1), 493–508 (2002).
[CrossRef] [PubMed]

2000

R. J. Buesa, “Mineral oil: the best xylene substitute for tissue processing yet?” J. Histotechnol.23(2), 143–149 (2000).
[CrossRef]

1998

J. E. Gershenwald, M. I. Colome, J. E. Lee, P. F. Mansfield, C. Tseng, J. J. Lee, C. M. Balch, and M. I. Ross, “Patterns of recurrence following a negative sentinel lymph node biopsy in 243 patients with stage I or II melanoma,” J. Clin. Oncol.16(6), 2253–2260 (1998).
[PubMed]

1990

W. Denk, J. H. Strickler, and W. W. Webb, “Two-photon laser scanning fluorescence microscopy,” Science248(4951), 73–76 (1990).
[CrossRef] [PubMed]

1985

S. D. Russell and C. P. Daghlian, “Scanning electron microscopic observations on deembedded biological tissue sections: comparison of different fixatives and embedding materials,” J. Electron Microsc. Tech.2(5), 489–495 (1985).
[CrossRef]

1970

V. Williams and F. Morriss, “Formaldehyde-induced fluorescence as a means for differentiating epinephrine cells from norepinephrine cells in adrenal medulla,” Stain Technol.45(5), 205–213 (1970).
[PubMed]

1952

A. J. Lea, “Solubility of melanins,” Nature170(4330), 709 (1952).
[CrossRef] [PubMed]

Ando, R.

H. Hama, H. Kurokawa, H. Kawano, R. Ando, T. Shimogori, H. Noda, K. Fukami, A. Sakaue-Sawano, and A. Miyawaki, “Scale: a chemical approach for fluorescence imaging and reconstruction of transparent mouse brain,” Nat. Neurosci.14(11), 1481–1488 (2011).
[CrossRef] [PubMed]

Balch, C. M.

J. E. Gershenwald, M. I. Colome, J. E. Lee, P. F. Mansfield, C. Tseng, J. J. Lee, C. M. Balch, and M. I. Ross, “Patterns of recurrence following a negative sentinel lymph node biopsy in 243 patients with stage I or II melanoma,” J. Clin. Oncol.16(6), 2253–2260 (1998).
[PubMed]

Barnes, E. L.

M. A. Smith, E. L. Barnes, and S. I. Chiosea, “Pathology archive: evaluation of integrity, regulatory compliance, and construction of searchable database from print reports,” Am. J. Clin. Pathol.135(5), 753–759 (2011).
[CrossRef] [PubMed]

Bashkatov, A. N.

E. A. Genina, A. N. Bashkatov, and V. V. Tuchin, “Tissue optical immersion clearing,” Expert Rev. Med. Devices7(6), 825–842 (2010).
[CrossRef] [PubMed]

Beaurepaire, E.

Becker, K.

H.-U. Dodt, U. Leischner, A. Schierloh, N. Jährling, C. P. Mauch, K. Deininger, J. M. Deussing, M. Eder, W. Zieglgänsberger, and K. Becker, “Ultramicroscopy: three-dimensional visualization of neuronal networks in the whole mouse brain,” Nat. Methods4(4), 331–336 (2007).
[CrossRef] [PubMed]

Bromberg, Y.

O. Katz, E. Small, Y. Bromberg, and Y. Silberberg, “Focusing and compression of ultrashort pulses through scattering media,” Nat. Photonics5(6), 372–377 (2011).
[CrossRef]

Buesa, R. J.

R. J. Buesa, “Mineral oil: the best xylene substitute for tissue processing yet?” J. Histotechnol.23(2), 143–149 (2000).
[CrossRef]

Campagnola, P. J.

S. V. Plotnikov, A. C. Millard, P. J. Campagnola, and W. A. Mohler, “Characterization of the myosin-based source for second-harmonic generation from muscle sarcomeres,” Biophys. J.90(2), 693–703 (2006).
[CrossRef] [PubMed]

P. J. Campagnola, A. C. Millard, M. Terasaki, P. E. Hoppe, C. J. Malone, and W. A. Mohler, “Three-dimensional high-resolution second-harmonic generation imaging of endogenous structural proteins in biological tissues,” Biophys. J.82(1), 493–508 (2002).
[CrossRef] [PubMed]

Chen, C.-C.

Chen, Y.-C.

Chia, T. H.

S. G. Parra, T. H. Chia, J. P. Zinter, and M. J. Levene, “Multiphoton microscopy of cleared mouse organs,” J. Biomed. Opt.15(3), 036017 (2010).
[CrossRef] [PubMed]

Chiosea, S. I.

M. A. Smith, E. L. Barnes, and S. I. Chiosea, “Pathology archive: evaluation of integrity, regulatory compliance, and construction of searchable database from print reports,” Am. J. Clin. Pathol.135(5), 753–759 (2011).
[CrossRef] [PubMed]

Choi, B.

A. T. Yeh, B. Choi, J. S. Nelson, and B. J. Tromberg, “Reversible dissociation of collagen in tissues,” J. Invest. Dermatol.121(6), 1332–1335 (2003).
[CrossRef] [PubMed]

Chu, S.-W.

Colome, M. I.

J. E. Gershenwald, M. I. Colome, J. E. Lee, P. F. Mansfield, C. Tseng, J. J. Lee, C. M. Balch, and M. I. Ross, “Patterns of recurrence following a negative sentinel lymph node biopsy in 243 patients with stage I or II melanoma,” J. Clin. Oncol.16(6), 2253–2260 (1998).
[PubMed]

Daghlian, C. P.

S. D. Russell and C. P. Daghlian, “Scanning electron microscopic observations on deembedded biological tissue sections: comparison of different fixatives and embedding materials,” J. Electron Microsc. Tech.2(5), 489–495 (1985).
[CrossRef]

Débarre, D.

Degan, S.

J. W. Wilson, S. Degan, T. Mitropoulos, M. A. Selim, J. Y. Zhang, and W. S. Warren, “In vivo pump-probe microscopy of melanoma and pigmented lesions,” Proc. SPIE8226, 822602, 822602-8 (2012).
[CrossRef]

T. E. Matthews, J. W. Wilson, S. Degan, M. J. Simpson, J. Y. Jin, J. Y. Zhang, and W. S. Warren, “In vivo and ex vivo epi-mode pump-probe imaging of melanin and microvasculature,” Biomed. Opt. Express2(6), 1576–1583 (2011).
[CrossRef] [PubMed]

Deininger, K.

H.-U. Dodt, U. Leischner, A. Schierloh, N. Jährling, C. P. Mauch, K. Deininger, J. M. Deussing, M. Eder, W. Zieglgänsberger, and K. Becker, “Ultramicroscopy: three-dimensional visualization of neuronal networks in the whole mouse brain,” Nat. Methods4(4), 331–336 (2007).
[CrossRef] [PubMed]

Denk, W.

P. Theer and W. Denk, “On the fundamental imaging-depth limit in two-photon microscopy,” J. Opt. Soc. Am. A23(12), 3139–3149 (2006).
[CrossRef] [PubMed]

W. Denk, J. H. Strickler, and W. W. Webb, “Two-photon laser scanning fluorescence microscopy,” Science248(4951), 73–76 (1990).
[CrossRef] [PubMed]

Deussing, J. M.

H.-U. Dodt, U. Leischner, A. Schierloh, N. Jährling, C. P. Mauch, K. Deininger, J. M. Deussing, M. Eder, W. Zieglgänsberger, and K. Becker, “Ultramicroscopy: three-dimensional visualization of neuronal networks in the whole mouse brain,” Nat. Methods4(4), 331–336 (2007).
[CrossRef] [PubMed]

Dodt, H.-U.

U. Leischner, A. Schierloh, W. Zieglgänsberger, and H.-U. Dodt, “Formalin-induced fluorescence reveals cell shape and morphology in biological tissue samples,” PLoS ONE5(4), e10391 (2010).
[CrossRef] [PubMed]

H.-U. Dodt, U. Leischner, A. Schierloh, N. Jährling, C. P. Mauch, K. Deininger, J. M. Deussing, M. Eder, W. Zieglgänsberger, and K. Becker, “Ultramicroscopy: three-dimensional visualization of neuronal networks in the whole mouse brain,” Nat. Methods4(4), 331–336 (2007).
[CrossRef] [PubMed]

Duff, K.

Duloquin, L.

Durst, M. E.

Eder, M.

H.-U. Dodt, U. Leischner, A. Schierloh, N. Jährling, C. P. Mauch, K. Deininger, J. M. Deussing, M. Eder, W. Zieglgänsberger, and K. Becker, “Ultramicroscopy: three-dimensional visualization of neuronal networks in the whole mouse brain,” Nat. Methods4(4), 331–336 (2007).
[CrossRef] [PubMed]

Fischer, M. C.

Freudiger, C. W.

W. Min, C. W. Freudiger, S. Lu, and X. S. Xie, “Coherent nonlinear optical imaging: beyond fluorescence microscopy,” Annu. Rev. Phys. Chem.62(1), 507–530 (2011).
[CrossRef] [PubMed]

Fu, D.

D. Fu, T. Ye, T. E. Matthews, G. Yurtsever, and W. S. Warren, “Two-color, two-photon, and excited-state absorption microscopy,” J. Biomed. Opt.12(5), 054004 (2007).
[CrossRef] [PubMed]

Fukami, K.

H. Hama, H. Kurokawa, H. Kawano, R. Ando, T. Shimogori, H. Noda, K. Fukami, A. Sakaue-Sawano, and A. Miyawaki, “Scale: a chemical approach for fluorescence imaging and reconstruction of transparent mouse brain,” Nat. Neurosci.14(11), 1481–1488 (2011).
[CrossRef] [PubMed]

Genina, E. A.

E. A. Genina, A. N. Bashkatov, and V. V. Tuchin, “Tissue optical immersion clearing,” Expert Rev. Med. Devices7(6), 825–842 (2010).
[CrossRef] [PubMed]

Gershenwald, J. E.

J. E. Gershenwald, M. I. Colome, J. E. Lee, P. F. Mansfield, C. Tseng, J. J. Lee, C. M. Balch, and M. I. Ross, “Patterns of recurrence following a negative sentinel lymph node biopsy in 243 patients with stage I or II melanoma,” J. Clin. Oncol.16(6), 2253–2260 (1998).
[PubMed]

Ghosn, M. G.

N. Sudheendran, M. Mohamed, M. G. Ghosn, V. V. Tuchin, and K. V. Larin, “Assessment of tissue optical clearing as a function of glucose concentration using optical coherence tomography,” J. Innov. Opt. Health Sci.03(3), 169–176 (2010).
[CrossRef] [PubMed]

Gouras, G. K.

Hama, H.

H. Hama, H. Kurokawa, H. Kawano, R. Ando, T. Shimogori, H. Noda, K. Fukami, A. Sakaue-Sawano, and A. Miyawaki, “Scale: a chemical approach for fluorescence imaging and reconstruction of transparent mouse brain,” Nat. Neurosci.14(11), 1481–1488 (2011).
[CrossRef] [PubMed]

Hoppe, P. E.

P. J. Campagnola, A. C. Millard, M. Terasaki, P. E. Hoppe, C. J. Malone, and W. A. Mohler, “Three-dimensional high-resolution second-harmonic generation imaging of endogenous structural proteins in biological tissues,” Biophys. J.82(1), 493–508 (2002).
[CrossRef] [PubMed]

Isobe, K.

Jährling, N.

H.-U. Dodt, U. Leischner, A. Schierloh, N. Jährling, C. P. Mauch, K. Deininger, J. M. Deussing, M. Eder, W. Zieglgänsberger, and K. Becker, “Ultramicroscopy: three-dimensional visualization of neuronal networks in the whole mouse brain,” Nat. Methods4(4), 331–336 (2007).
[CrossRef] [PubMed]

Jin, J. Y.

Katz, O.

O. Katz, E. Small, Y. Bromberg, and Y. Silberberg, “Focusing and compression of ultrashort pulses through scattering media,” Nat. Photonics5(6), 372–377 (2011).
[CrossRef]

Kawano, H.

K. Isobe, H. Kawano, T. Takeda, A. Suda, A. Kumagai, H. Mizuno, A. Miyawaki, and K. Midorikawa, “Background-free deep imaging by spatial overlap modulation nonlinear optical microscopy,” Biomed. Opt. Express3(7), 1594–1608 (2012).
[CrossRef] [PubMed]

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Supplementary Material (12)

» Media 1: MOV (956 KB)     
» Media 2: MOV (1050 KB)     
» Media 3: MOV (1047 KB)     
» Media 4: MOV (1055 KB)     
» Media 5: MOV (1060 KB)     
» Media 6: MOV (1053 KB)     
» Media 7: MOV (1066 KB)     
» Media 8: MOV (1050 KB)     
» Media 9: MOV (1059 KB)     
» Media 10: MOV (1056 KB)     
» Media 11: MOV (4100 KB)     
» Media 12: MOV (4103 KB)     

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Figures (7)

Fig. 1
Fig. 1

Kidney, 130 μm FOV. (NP image acquired with 256 x 256 pixel resolution for the 260 μm field of view) For full 260 μm FOV, see Media 1 and Media 2.

Fig. 2
Fig. 2

Liver, 130 μm FOV. For full 260 μm FOV, see Media 3 and Media 4.

Fig. 3
Fig. 3

Spleen, 130 μm FOV. For full 260 μm FOV, see Media 5 and Media 6.

Fig. 4
Fig. 4

Heart, 130 μm FOV. For full 260 μm FOV, see Media 7 and Media 8.

Fig. 5
Fig. 5

Lung, 130 μm FOV. For full 260 μm FOV, see Media 9 and Media 10.

Fig. 6
Fig. 6

Brain, 130 μm FOV. For full 260 μm FOV, see Media 11 and Media 12.

Fig. 7
Fig. 7

Volume rendering of a 260 × 260 × 65 μm section of lung.

Metrics