Abstract

Ultrahigh-resolution optical coherence tomography (UR-OCT) has been used for the first time to our knowledge to study single-cell basal cell carcinoma (BCC) in vitro. This noninvasive, in situ, label-free technique with deep imaging depth enables three-dimensional analysis of scattering properties of single cells with cellular spatial resolution. From three-dimensional UR-OCT imaging, live and dead BCC cells can be easily identified based on morphological observation. We developed a novel method to automatically extract characteristic parameters of a single cell from data volume, and quantitative comparison and parametric analysis were performed. The results demonstrate the capability of UR-OCT to detect cell death at the cellular level.

© 2012 OSA

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2012 (4)

S. Earley, C. Vinegoni, J. Dunham, R. Gorbatov, P. F. Feruglio, and R. Weissleder, “In vivo imaging of drug-induced mitochondrial outer membrane permeabilization at single-cell resolution,” Cancer Res. 72(12), 2949–2956 (2012).
[CrossRef] [PubMed]

J. P. Dunkers, Y. J. Lee, and K. Chatterjee, “Single cell viability measurements in 3D scaffolds using in situ label free imaging by optical coherence microscopy,” Biomaterials 33(7), 2119–2126 (2012).
[CrossRef] [PubMed]

Y. Reis, M. Bernardo-Faura, D. Richter, T. Wolf, B. Brors, A. Hamacher-Brady, R. Eils, and N. R. Brady, “Multi-parametric analysis and modeling of relationships between mitochondrial morphology and apoptosis,” PLoS ONE 7(1), e28694 (2012).
[CrossRef] [PubMed]

X. Zhang, M. B. Roeffaers, S. Basu, J. R. Daniele, D. Fu, C. W. Freudiger, G. R. Holtom, and X. S. Xie, “Label-free live-cell imaging of nucleic acids using stimulated Raman scattering microscopy,” ChemPhysChem 13(4), 1054–1059 (2012).
[CrossRef] [PubMed]

2011 (7)

M. Rehberg, F. Krombach, U. Pohl, and S. Dietzel, “Label-free 3D visualization of cellular and tissue structures in intact muscle with second and third harmonic generation microscopy,” PLoS ONE 6(11), e28237 (2011).
[CrossRef] [PubMed]

P. O. Bagnaninchi, C. Holmes, N. Drummond, J. Daoud, and M. Tabrizian, “Two-dimensional and three-dimensional viability measurements of adult stem cells with optical coherence phase microscopy,” J. Biomed. Opt. 16(8), 086003 (2011).
[CrossRef] [PubMed]

L. Liu, J. A. Gardecki, S. K. Nadkarni, J. D. Toussaint, Y. Yagi, B. E. Bouma, and G. J. Tearney, “Imaging the subcellular structure of human coronary atherosclerosis using micro-optical coherence tomography,” Nat. Med. 17(8), 1010–1014 (2011).
[CrossRef] [PubMed]

J. D. Orth, R. H. Kohler, F. Foijer, P. K. Sorger, R. Weissleder, and T. J. Mitchison, “Analysis of mitosis and antimitotic drug responses in tumors by in vivo microscopy and single-cell pharmacodynamics,” Cancer Res. 71(13), 4608–4616 (2011).
[CrossRef] [PubMed]

S. B. Nicholls, J. Chu, G. Abbruzzese, K. D. Tremblay, and J. A. Hardy, “Mechanism of a genetically encoded dark-to-bright reporter for caspase activity,” J. Biol. Chem. 286(28), 24977–24986 (2011).
[CrossRef] [PubMed]

M. J. Pittet and R. Weissleder, “Intravital imaging,” Cell 147(5), 983–991 (2011).
[CrossRef] [PubMed]

S. L. Spencer and P. K. Sorger, “Measuring and modeling apoptosis in single cells,” Cell 144(6), 926–939 (2011).
[CrossRef] [PubMed]

2010 (3)

H. C. Huang, T. J. Mitchison, and J. Shi, “Stochastic competition between mechanistically independent slippage and death pathways determines cell fate during mitotic arrest,” PLoS ONE 5(12), e15724 (2010).
[CrossRef] [PubMed]

S. V. Sharma, D. Y. Lee, B. Li, M. P. Quinlan, F. Takahashi, S. Maheswaran, U. McDermott, N. Azizian, L. Zou, M. A. Fischbach, K. K. Wong, K. Brandstetter, B. Wittner, S. Ramaswamy, M. Classon, and J. Settleman, “A chromatin-mediated reversible drug-tolerant state in cancer cell subpopulations,” Cell 141(1), 69–80 (2010).
[CrossRef] [PubMed]

C. C. Tsai, T. H. Chen, Y. S. Lin, Y. T. Wang, W. Chang, K. Y. Hsu, Y. H. Chang, P. K. Hsu, D. Y. Jheng, K. Y. Huang, E. Sun, and S. L. Huang, “Ce3+:YAG double-clad crystal-fiber-based optical coherence tomography on fish cornea,” Opt. Lett. 35(6), 811–813 (2010).
[CrossRef] [PubMed]

2009 (6)

X. Liang, B. W. Graf, and S. A. Boppart, “Imaging engineered tissues using structural and functional optical coherence tomography,” J. Biophotonics 2(11), 643–655 (2009).
[CrossRef] [PubMed]

W. C. Kuo, C. H. Chan, C. H. Chou, and J. C. Cheng, “Swept source optical coherence tomography for radiation-enhanced hepatocellular carcinoma cell invasion imaging,” Phys. Med. Biol. 54(13), 4289–4297 (2009).
[CrossRef] [PubMed]

S. M. Rey, B. Povazay, B. Hofer, A. Unterhuber, B. Hermann, A. Harwood, and W. Drexler, “Three- and four-dimensional visualization of cell migration using optical coherence tomography,” J. Biophotonics 2(6-7), 370–379 (2009).
[CrossRef] [PubMed]

M. Niepel, S. L. Spencer, and P. K. Sorger, “Non-genetic cell-to-cell variability and the consequences for pharmacology,” Curr. Opin. Chem. Biol. 13(5-6), 556–561 (2009).
[CrossRef] [PubMed]

S. L. Spencer, S. Gaudet, J. G. Albeck, J. M. Burke, and P. K. Sorger, “Non-genetic origins of cell-to-cell variability in TRAIL-induced apoptosis,” Nature 459(7245), 428–432 (2009).
[CrossRef] [PubMed]

J. W. Tjiu, J. S. Chen, C. T. Shun, S. J. Lin, Y. H. Liao, C. Y. Chu, T. F. Tsai, H. C. Chiu, Y. S. Dai, H. Inoue, P. C. Yang, M. L. Kuo, and S. H. Jee, “Tumor-associated macrophage-induced invasion and angiogenesis of human basal cell carcinoma cells by cyclooxygenase-2 induction,” J. Invest. Dermatol. 129(4), 1016–1025 (2009).
[CrossRef] [PubMed]

2008 (5)

J. G. Albeck, J. M. Burke, B. B. Aldridge, M. Zhang, D. A. Lauffenburger, and P. K. Sorger, “Quantitative analysis of pathways controlling extrinsic apoptosis in single cells,” Mol. Cell 30(1), 11–25 (2008).
[CrossRef] [PubMed]

R. Weissleder and M. J. Pittet, “Imaging in the era of molecular oncology,” Nature 452(7187), 580–589 (2008).
[CrossRef] [PubMed]

A. Raj and A. van Oudenaarden, “Nature, nurture, or chance: stochastic gene expression and its consequences,” Cell 135(2), 216–226 (2008).
[CrossRef] [PubMed]

A. A. Cohen, N. Geva-Zatorsky, E. Eden, M. Frenkel-Morgenstern, I. Issaeva, A. Sigal, R. Milo, C. Cohen-Saidon, Y. Liron, Z. Kam, L. Cohen, T. Danon, N. Perzov, and U. Alon, “Dynamic proteomics of individual cancer cells in response to a drug,” Science 322(5907), 1511–1516 (2008).
[CrossRef] [PubMed]

K. E. Gascoigne and S. S. Taylor, “Cancer cells display profound intra- and interline variation following prolonged exposure to antimitotic drugs,” Cancer Cell 14(2), 111–122 (2008).
[CrossRef] [PubMed]

2007 (1)

O. J. Rando and K. J. Verstrepen, “Timescales of genetic and epigenetic inheritance,” Cell 128(4), 655–668 (2007).
[CrossRef] [PubMed]

2006 (3)

W. Tan, A. L. Oldenburg, J. J. Norman, T. A. Desai, and S. A. Boppart, “Optical coherence tomography of cell dynamics in three-dimensional tissue models,” Opt. Express 14(16), 7159–7171 (2006).
[CrossRef] [PubMed]

K. L. Reckamp, K. Krysan, J. D. Morrow, G. L. Milne, R. A. Newman, C. Tucker, R. M. Elashoff, S. M. Dubinett, and R. A. Figlin, “A phase I trial to determine the optimal biological dose of celecoxib when combined with erlotinib in advanced non-small cell lung cancer,” Clin. Cancer Res. 12(11), 3381–3388 (2006).
[CrossRef] [PubMed]

J. W. Tjiu, Y. H. Liao, S. J. Lin, Y. L. Huang, W. L. Tsai, C. Y. Chu, M. L. Kuo, and S. H. Jee, “Cyclooxygenase-2 overexpression in human basal cell carcinoma cell line increases antiapoptosis, angiogenesis, and tumorigenesis,” J. Invest. Dermatol. 126(5), 1143–1151 (2006).
[CrossRef] [PubMed]

2005 (3)

C. L. Evans, E. O. Potma, M. Puoris’haag, D. Côté, C. P. Lin, and X. S. Xie, “Chemical imaging of tissue in vivo with video-rate coherent anti-Stokes Raman scattering microscopy,” Proc. Natl. Acad. Sci. U.S.A. 102(46), 16807–16812 (2005).
[CrossRef] [PubMed]

I. Csiki, J. D. Morrow, A. Sandler, Y. Shyr, J. Oates, M. K. Williams, T. Dang, D. P. Carbone, and D. H. Johnson, “Targeting cyclooxygenase-2 in recurrent non-small cell lung cancer: a phase II trial of celecoxib and docetaxel,” Clin. Cancer Res. 11(18), 6634–6640 (2005).
[CrossRef] [PubMed]

C. Joo, T. Akkin, B. Cense, B. H. Park, and J. F. de Boer, “Spectral-domain optical coherence phase microscopy for quantitative phase-contrast imaging,” Opt. Lett. 30(16), 2131–2133 (2005).
[CrossRef] [PubMed]

2003 (2)

A. B. Vakhtin, D. J. Kane, W. R. Wood, and K. A. Peterson, “Common-path interferometer for frequency-domain optical coherence tomography,” Appl. Opt. 42(34), 6953–6958 (2003).
[CrossRef] [PubMed]

R. Drezek, M. Guillaud, T. Collier, I. Boiko, A. Malpica, C. Macaulay, M. Follen, and R. Richards-Kortum, “Light scattering from cervical cells throughout neoplastic progression: influence of nuclear morphology, DNA content, and chromatin texture,” J. Biomed. Opt. 8(1), 7–16 (2003).
[CrossRef] [PubMed]

2001 (2)

Z. Darzynkiewicz, E. Bedner, and P. Smolewski, “Flow cytometry in analysis of cell cycle and apoptosis,” Semin. Hematol. 38(2), 179–193 (2001).
[CrossRef] [PubMed]

T. Reya, S. J. Morrison, M. F. Clarke, and I. L. Weissman, “Stem cells, cancer, and cancer stem cells,” Nature 414(6859), 105–111 (2001).
[CrossRef] [PubMed]

1999 (1)

1998 (2)

1997 (1)

Z. Darzynkiewicz, G. Juan, X. Li, W. Gorczyca, T. Murakami, and F. Traganos, “Cytometry in cell necrobiology: analysis of apoptosis and accidental cell death (necrosis),” Cytometry 27(1), 1–20 (1997).
[CrossRef] [PubMed]

1991 (1)

D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and et, “Optical coherence tomography,” Science 254(5035), 1178–1181 (1991).
[CrossRef] [PubMed]

Abbruzzese, G.

S. B. Nicholls, J. Chu, G. Abbruzzese, K. D. Tremblay, and J. A. Hardy, “Mechanism of a genetically encoded dark-to-bright reporter for caspase activity,” J. Biol. Chem. 286(28), 24977–24986 (2011).
[CrossRef] [PubMed]

Akkin, T.

Albeck, J. G.

S. L. Spencer, S. Gaudet, J. G. Albeck, J. M. Burke, and P. K. Sorger, “Non-genetic origins of cell-to-cell variability in TRAIL-induced apoptosis,” Nature 459(7245), 428–432 (2009).
[CrossRef] [PubMed]

J. G. Albeck, J. M. Burke, B. B. Aldridge, M. Zhang, D. A. Lauffenburger, and P. K. Sorger, “Quantitative analysis of pathways controlling extrinsic apoptosis in single cells,” Mol. Cell 30(1), 11–25 (2008).
[CrossRef] [PubMed]

Aldridge, B. B.

J. G. Albeck, J. M. Burke, B. B. Aldridge, M. Zhang, D. A. Lauffenburger, and P. K. Sorger, “Quantitative analysis of pathways controlling extrinsic apoptosis in single cells,” Mol. Cell 30(1), 11–25 (2008).
[CrossRef] [PubMed]

Alon, U.

A. A. Cohen, N. Geva-Zatorsky, E. Eden, M. Frenkel-Morgenstern, I. Issaeva, A. Sigal, R. Milo, C. Cohen-Saidon, Y. Liron, Z. Kam, L. Cohen, T. Danon, N. Perzov, and U. Alon, “Dynamic proteomics of individual cancer cells in response to a drug,” Science 322(5907), 1511–1516 (2008).
[CrossRef] [PubMed]

Azizian, N.

S. V. Sharma, D. Y. Lee, B. Li, M. P. Quinlan, F. Takahashi, S. Maheswaran, U. McDermott, N. Azizian, L. Zou, M. A. Fischbach, K. K. Wong, K. Brandstetter, B. Wittner, S. Ramaswamy, M. Classon, and J. Settleman, “A chromatin-mediated reversible drug-tolerant state in cancer cell subpopulations,” Cell 141(1), 69–80 (2010).
[CrossRef] [PubMed]

Bagnaninchi, P. O.

P. O. Bagnaninchi, C. Holmes, N. Drummond, J. Daoud, and M. Tabrizian, “Two-dimensional and three-dimensional viability measurements of adult stem cells with optical coherence phase microscopy,” J. Biomed. Opt. 16(8), 086003 (2011).
[CrossRef] [PubMed]

Basu, S.

X. Zhang, M. B. Roeffaers, S. Basu, J. R. Daniele, D. Fu, C. W. Freudiger, G. R. Holtom, and X. S. Xie, “Label-free live-cell imaging of nucleic acids using stimulated Raman scattering microscopy,” ChemPhysChem 13(4), 1054–1059 (2012).
[CrossRef] [PubMed]

Bedner, E.

Z. Darzynkiewicz, E. Bedner, and P. Smolewski, “Flow cytometry in analysis of cell cycle and apoptosis,” Semin. Hematol. 38(2), 179–193 (2001).
[CrossRef] [PubMed]

Bernardo-Faura, M.

Y. Reis, M. Bernardo-Faura, D. Richter, T. Wolf, B. Brors, A. Hamacher-Brady, R. Eils, and N. R. Brady, “Multi-parametric analysis and modeling of relationships between mitochondrial morphology and apoptosis,” PLoS ONE 7(1), e28694 (2012).
[CrossRef] [PubMed]

Boiko, I.

R. Drezek, M. Guillaud, T. Collier, I. Boiko, A. Malpica, C. Macaulay, M. Follen, and R. Richards-Kortum, “Light scattering from cervical cells throughout neoplastic progression: influence of nuclear morphology, DNA content, and chromatin texture,” J. Biomed. Opt. 8(1), 7–16 (2003).
[CrossRef] [PubMed]

Boppart, S. A.

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J. W. Tjiu, J. S. Chen, C. T. Shun, S. J. Lin, Y. H. Liao, C. Y. Chu, T. F. Tsai, H. C. Chiu, Y. S. Dai, H. Inoue, P. C. Yang, M. L. Kuo, and S. H. Jee, “Tumor-associated macrophage-induced invasion and angiogenesis of human basal cell carcinoma cells by cyclooxygenase-2 induction,” J. Invest. Dermatol. 129(4), 1016–1025 (2009).
[CrossRef] [PubMed]

Shyr, Y.

I. Csiki, J. D. Morrow, A. Sandler, Y. Shyr, J. Oates, M. K. Williams, T. Dang, D. P. Carbone, and D. H. Johnson, “Targeting cyclooxygenase-2 in recurrent non-small cell lung cancer: a phase II trial of celecoxib and docetaxel,” Clin. Cancer Res. 11(18), 6634–6640 (2005).
[CrossRef] [PubMed]

Sigal, A.

A. A. Cohen, N. Geva-Zatorsky, E. Eden, M. Frenkel-Morgenstern, I. Issaeva, A. Sigal, R. Milo, C. Cohen-Saidon, Y. Liron, Z. Kam, L. Cohen, T. Danon, N. Perzov, and U. Alon, “Dynamic proteomics of individual cancer cells in response to a drug,” Science 322(5907), 1511–1516 (2008).
[CrossRef] [PubMed]

Smolewski, P.

Z. Darzynkiewicz, E. Bedner, and P. Smolewski, “Flow cytometry in analysis of cell cycle and apoptosis,” Semin. Hematol. 38(2), 179–193 (2001).
[CrossRef] [PubMed]

Sorger, P. K.

S. L. Spencer and P. K. Sorger, “Measuring and modeling apoptosis in single cells,” Cell 144(6), 926–939 (2011).
[CrossRef] [PubMed]

J. D. Orth, R. H. Kohler, F. Foijer, P. K. Sorger, R. Weissleder, and T. J. Mitchison, “Analysis of mitosis and antimitotic drug responses in tumors by in vivo microscopy and single-cell pharmacodynamics,” Cancer Res. 71(13), 4608–4616 (2011).
[CrossRef] [PubMed]

M. Niepel, S. L. Spencer, and P. K. Sorger, “Non-genetic cell-to-cell variability and the consequences for pharmacology,” Curr. Opin. Chem. Biol. 13(5-6), 556–561 (2009).
[CrossRef] [PubMed]

S. L. Spencer, S. Gaudet, J. G. Albeck, J. M. Burke, and P. K. Sorger, “Non-genetic origins of cell-to-cell variability in TRAIL-induced apoptosis,” Nature 459(7245), 428–432 (2009).
[CrossRef] [PubMed]

J. G. Albeck, J. M. Burke, B. B. Aldridge, M. Zhang, D. A. Lauffenburger, and P. K. Sorger, “Quantitative analysis of pathways controlling extrinsic apoptosis in single cells,” Mol. Cell 30(1), 11–25 (2008).
[CrossRef] [PubMed]

Spencer, S. L.

S. L. Spencer and P. K. Sorger, “Measuring and modeling apoptosis in single cells,” Cell 144(6), 926–939 (2011).
[CrossRef] [PubMed]

S. L. Spencer, S. Gaudet, J. G. Albeck, J. M. Burke, and P. K. Sorger, “Non-genetic origins of cell-to-cell variability in TRAIL-induced apoptosis,” Nature 459(7245), 428–432 (2009).
[CrossRef] [PubMed]

M. Niepel, S. L. Spencer, and P. K. Sorger, “Non-genetic cell-to-cell variability and the consequences for pharmacology,” Curr. Opin. Chem. Biol. 13(5-6), 556–561 (2009).
[CrossRef] [PubMed]

Stinson, W. G.

D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and et, “Optical coherence tomography,” Science 254(5035), 1178–1181 (1991).
[CrossRef] [PubMed]

Sun, E.

Swanson, E. A.

D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and et, “Optical coherence tomography,” Science 254(5035), 1178–1181 (1991).
[CrossRef] [PubMed]

Tabrizian, M.

P. O. Bagnaninchi, C. Holmes, N. Drummond, J. Daoud, and M. Tabrizian, “Two-dimensional and three-dimensional viability measurements of adult stem cells with optical coherence phase microscopy,” J. Biomed. Opt. 16(8), 086003 (2011).
[CrossRef] [PubMed]

Takahashi, F.

S. V. Sharma, D. Y. Lee, B. Li, M. P. Quinlan, F. Takahashi, S. Maheswaran, U. McDermott, N. Azizian, L. Zou, M. A. Fischbach, K. K. Wong, K. Brandstetter, B. Wittner, S. Ramaswamy, M. Classon, and J. Settleman, “A chromatin-mediated reversible drug-tolerant state in cancer cell subpopulations,” Cell 141(1), 69–80 (2010).
[CrossRef] [PubMed]

Tan, W.

Taylor, S. S.

K. E. Gascoigne and S. S. Taylor, “Cancer cells display profound intra- and interline variation following prolonged exposure to antimitotic drugs,” Cancer Cell 14(2), 111–122 (2008).
[CrossRef] [PubMed]

Tearney, G. J.

L. Liu, J. A. Gardecki, S. K. Nadkarni, J. D. Toussaint, Y. Yagi, B. E. Bouma, and G. J. Tearney, “Imaging the subcellular structure of human coronary atherosclerosis using micro-optical coherence tomography,” Nat. Med. 17(8), 1010–1014 (2011).
[CrossRef] [PubMed]

Tjiu, J. W.

J. W. Tjiu, J. S. Chen, C. T. Shun, S. J. Lin, Y. H. Liao, C. Y. Chu, T. F. Tsai, H. C. Chiu, Y. S. Dai, H. Inoue, P. C. Yang, M. L. Kuo, and S. H. Jee, “Tumor-associated macrophage-induced invasion and angiogenesis of human basal cell carcinoma cells by cyclooxygenase-2 induction,” J. Invest. Dermatol. 129(4), 1016–1025 (2009).
[CrossRef] [PubMed]

J. W. Tjiu, Y. H. Liao, S. J. Lin, Y. L. Huang, W. L. Tsai, C. Y. Chu, M. L. Kuo, and S. H. Jee, “Cyclooxygenase-2 overexpression in human basal cell carcinoma cell line increases antiapoptosis, angiogenesis, and tumorigenesis,” J. Invest. Dermatol. 126(5), 1143–1151 (2006).
[CrossRef] [PubMed]

Toussaint, J. D.

L. Liu, J. A. Gardecki, S. K. Nadkarni, J. D. Toussaint, Y. Yagi, B. E. Bouma, and G. J. Tearney, “Imaging the subcellular structure of human coronary atherosclerosis using micro-optical coherence tomography,” Nat. Med. 17(8), 1010–1014 (2011).
[CrossRef] [PubMed]

Traganos, F.

Z. Darzynkiewicz, G. Juan, X. Li, W. Gorczyca, T. Murakami, and F. Traganos, “Cytometry in cell necrobiology: analysis of apoptosis and accidental cell death (necrosis),” Cytometry 27(1), 1–20 (1997).
[CrossRef] [PubMed]

Tremblay, K. D.

S. B. Nicholls, J. Chu, G. Abbruzzese, K. D. Tremblay, and J. A. Hardy, “Mechanism of a genetically encoded dark-to-bright reporter for caspase activity,” J. Biol. Chem. 286(28), 24977–24986 (2011).
[CrossRef] [PubMed]

Tsai, C. C.

Tsai, T. F.

J. W. Tjiu, J. S. Chen, C. T. Shun, S. J. Lin, Y. H. Liao, C. Y. Chu, T. F. Tsai, H. C. Chiu, Y. S. Dai, H. Inoue, P. C. Yang, M. L. Kuo, and S. H. Jee, “Tumor-associated macrophage-induced invasion and angiogenesis of human basal cell carcinoma cells by cyclooxygenase-2 induction,” J. Invest. Dermatol. 129(4), 1016–1025 (2009).
[CrossRef] [PubMed]

Tsai, W. L.

J. W. Tjiu, Y. H. Liao, S. J. Lin, Y. L. Huang, W. L. Tsai, C. Y. Chu, M. L. Kuo, and S. H. Jee, “Cyclooxygenase-2 overexpression in human basal cell carcinoma cell line increases antiapoptosis, angiogenesis, and tumorigenesis,” J. Invest. Dermatol. 126(5), 1143–1151 (2006).
[CrossRef] [PubMed]

Tucker, C.

K. L. Reckamp, K. Krysan, J. D. Morrow, G. L. Milne, R. A. Newman, C. Tucker, R. M. Elashoff, S. M. Dubinett, and R. A. Figlin, “A phase I trial to determine the optimal biological dose of celecoxib when combined with erlotinib in advanced non-small cell lung cancer,” Clin. Cancer Res. 12(11), 3381–3388 (2006).
[CrossRef] [PubMed]

Unterhuber, A.

S. M. Rey, B. Povazay, B. Hofer, A. Unterhuber, B. Hermann, A. Harwood, and W. Drexler, “Three- and four-dimensional visualization of cell migration using optical coherence tomography,” J. Biophotonics 2(6-7), 370–379 (2009).
[CrossRef] [PubMed]

Vakhtin, A. B.

van Oudenaarden, A.

A. Raj and A. van Oudenaarden, “Nature, nurture, or chance: stochastic gene expression and its consequences,” Cell 135(2), 216–226 (2008).
[CrossRef] [PubMed]

Verstrepen, K. J.

O. J. Rando and K. J. Verstrepen, “Timescales of genetic and epigenetic inheritance,” Cell 128(4), 655–668 (2007).
[CrossRef] [PubMed]

Vinegoni, C.

S. Earley, C. Vinegoni, J. Dunham, R. Gorbatov, P. F. Feruglio, and R. Weissleder, “In vivo imaging of drug-induced mitochondrial outer membrane permeabilization at single-cell resolution,” Cancer Res. 72(12), 2949–2956 (2012).
[CrossRef] [PubMed]

Wang, Y. T.

Weissleder, R.

S. Earley, C. Vinegoni, J. Dunham, R. Gorbatov, P. F. Feruglio, and R. Weissleder, “In vivo imaging of drug-induced mitochondrial outer membrane permeabilization at single-cell resolution,” Cancer Res. 72(12), 2949–2956 (2012).
[CrossRef] [PubMed]

J. D. Orth, R. H. Kohler, F. Foijer, P. K. Sorger, R. Weissleder, and T. J. Mitchison, “Analysis of mitosis and antimitotic drug responses in tumors by in vivo microscopy and single-cell pharmacodynamics,” Cancer Res. 71(13), 4608–4616 (2011).
[CrossRef] [PubMed]

M. J. Pittet and R. Weissleder, “Intravital imaging,” Cell 147(5), 983–991 (2011).
[CrossRef] [PubMed]

R. Weissleder and M. J. Pittet, “Imaging in the era of molecular oncology,” Nature 452(7187), 580–589 (2008).
[CrossRef] [PubMed]

Weissman, I. L.

T. Reya, S. J. Morrison, M. F. Clarke, and I. L. Weissman, “Stem cells, cancer, and cancer stem cells,” Nature 414(6859), 105–111 (2001).
[CrossRef] [PubMed]

Williams, M. K.

I. Csiki, J. D. Morrow, A. Sandler, Y. Shyr, J. Oates, M. K. Williams, T. Dang, D. P. Carbone, and D. H. Johnson, “Targeting cyclooxygenase-2 in recurrent non-small cell lung cancer: a phase II trial of celecoxib and docetaxel,” Clin. Cancer Res. 11(18), 6634–6640 (2005).
[CrossRef] [PubMed]

Wittner, B.

S. V. Sharma, D. Y. Lee, B. Li, M. P. Quinlan, F. Takahashi, S. Maheswaran, U. McDermott, N. Azizian, L. Zou, M. A. Fischbach, K. K. Wong, K. Brandstetter, B. Wittner, S. Ramaswamy, M. Classon, and J. Settleman, “A chromatin-mediated reversible drug-tolerant state in cancer cell subpopulations,” Cell 141(1), 69–80 (2010).
[CrossRef] [PubMed]

Wolf, T.

Y. Reis, M. Bernardo-Faura, D. Richter, T. Wolf, B. Brors, A. Hamacher-Brady, R. Eils, and N. R. Brady, “Multi-parametric analysis and modeling of relationships between mitochondrial morphology and apoptosis,” PLoS ONE 7(1), e28694 (2012).
[CrossRef] [PubMed]

Wong, K. K.

S. V. Sharma, D. Y. Lee, B. Li, M. P. Quinlan, F. Takahashi, S. Maheswaran, U. McDermott, N. Azizian, L. Zou, M. A. Fischbach, K. K. Wong, K. Brandstetter, B. Wittner, S. Ramaswamy, M. Classon, and J. Settleman, “A chromatin-mediated reversible drug-tolerant state in cancer cell subpopulations,” Cell 141(1), 69–80 (2010).
[CrossRef] [PubMed]

Wood, W. R.

Xie, X. S.

X. Zhang, M. B. Roeffaers, S. Basu, J. R. Daniele, D. Fu, C. W. Freudiger, G. R. Holtom, and X. S. Xie, “Label-free live-cell imaging of nucleic acids using stimulated Raman scattering microscopy,” ChemPhysChem 13(4), 1054–1059 (2012).
[CrossRef] [PubMed]

C. L. Evans, E. O. Potma, M. Puoris’haag, D. Côté, C. P. Lin, and X. S. Xie, “Chemical imaging of tissue in vivo with video-rate coherent anti-Stokes Raman scattering microscopy,” Proc. Natl. Acad. Sci. U.S.A. 102(46), 16807–16812 (2005).
[CrossRef] [PubMed]

Yagi, Y.

L. Liu, J. A. Gardecki, S. K. Nadkarni, J. D. Toussaint, Y. Yagi, B. E. Bouma, and G. J. Tearney, “Imaging the subcellular structure of human coronary atherosclerosis using micro-optical coherence tomography,” Nat. Med. 17(8), 1010–1014 (2011).
[CrossRef] [PubMed]

Yang, P. C.

J. W. Tjiu, J. S. Chen, C. T. Shun, S. J. Lin, Y. H. Liao, C. Y. Chu, T. F. Tsai, H. C. Chiu, Y. S. Dai, H. Inoue, P. C. Yang, M. L. Kuo, and S. H. Jee, “Tumor-associated macrophage-induced invasion and angiogenesis of human basal cell carcinoma cells by cyclooxygenase-2 induction,” J. Invest. Dermatol. 129(4), 1016–1025 (2009).
[CrossRef] [PubMed]

Zhang, M.

J. G. Albeck, J. M. Burke, B. B. Aldridge, M. Zhang, D. A. Lauffenburger, and P. K. Sorger, “Quantitative analysis of pathways controlling extrinsic apoptosis in single cells,” Mol. Cell 30(1), 11–25 (2008).
[CrossRef] [PubMed]

Zhang, X.

X. Zhang, M. B. Roeffaers, S. Basu, J. R. Daniele, D. Fu, C. W. Freudiger, G. R. Holtom, and X. S. Xie, “Label-free live-cell imaging of nucleic acids using stimulated Raman scattering microscopy,” ChemPhysChem 13(4), 1054–1059 (2012).
[CrossRef] [PubMed]

Zou, L.

S. V. Sharma, D. Y. Lee, B. Li, M. P. Quinlan, F. Takahashi, S. Maheswaran, U. McDermott, N. Azizian, L. Zou, M. A. Fischbach, K. K. Wong, K. Brandstetter, B. Wittner, S. Ramaswamy, M. Classon, and J. Settleman, “A chromatin-mediated reversible drug-tolerant state in cancer cell subpopulations,” Cell 141(1), 69–80 (2010).
[CrossRef] [PubMed]

Appl. Opt. (3)

Biomaterials (1)

J. P. Dunkers, Y. J. Lee, and K. Chatterjee, “Single cell viability measurements in 3D scaffolds using in situ label free imaging by optical coherence microscopy,” Biomaterials 33(7), 2119–2126 (2012).
[CrossRef] [PubMed]

Cancer Cell (1)

K. E. Gascoigne and S. S. Taylor, “Cancer cells display profound intra- and interline variation following prolonged exposure to antimitotic drugs,” Cancer Cell 14(2), 111–122 (2008).
[CrossRef] [PubMed]

Cancer Res. (2)

S. Earley, C. Vinegoni, J. Dunham, R. Gorbatov, P. F. Feruglio, and R. Weissleder, “In vivo imaging of drug-induced mitochondrial outer membrane permeabilization at single-cell resolution,” Cancer Res. 72(12), 2949–2956 (2012).
[CrossRef] [PubMed]

J. D. Orth, R. H. Kohler, F. Foijer, P. K. Sorger, R. Weissleder, and T. J. Mitchison, “Analysis of mitosis and antimitotic drug responses in tumors by in vivo microscopy and single-cell pharmacodynamics,” Cancer Res. 71(13), 4608–4616 (2011).
[CrossRef] [PubMed]

Cell (5)

S. L. Spencer and P. K. Sorger, “Measuring and modeling apoptosis in single cells,” Cell 144(6), 926–939 (2011).
[CrossRef] [PubMed]

M. J. Pittet and R. Weissleder, “Intravital imaging,” Cell 147(5), 983–991 (2011).
[CrossRef] [PubMed]

S. V. Sharma, D. Y. Lee, B. Li, M. P. Quinlan, F. Takahashi, S. Maheswaran, U. McDermott, N. Azizian, L. Zou, M. A. Fischbach, K. K. Wong, K. Brandstetter, B. Wittner, S. Ramaswamy, M. Classon, and J. Settleman, “A chromatin-mediated reversible drug-tolerant state in cancer cell subpopulations,” Cell 141(1), 69–80 (2010).
[CrossRef] [PubMed]

A. Raj and A. van Oudenaarden, “Nature, nurture, or chance: stochastic gene expression and its consequences,” Cell 135(2), 216–226 (2008).
[CrossRef] [PubMed]

O. J. Rando and K. J. Verstrepen, “Timescales of genetic and epigenetic inheritance,” Cell 128(4), 655–668 (2007).
[CrossRef] [PubMed]

ChemPhysChem (1)

X. Zhang, M. B. Roeffaers, S. Basu, J. R. Daniele, D. Fu, C. W. Freudiger, G. R. Holtom, and X. S. Xie, “Label-free live-cell imaging of nucleic acids using stimulated Raman scattering microscopy,” ChemPhysChem 13(4), 1054–1059 (2012).
[CrossRef] [PubMed]

Clin. Cancer Res. (2)

I. Csiki, J. D. Morrow, A. Sandler, Y. Shyr, J. Oates, M. K. Williams, T. Dang, D. P. Carbone, and D. H. Johnson, “Targeting cyclooxygenase-2 in recurrent non-small cell lung cancer: a phase II trial of celecoxib and docetaxel,” Clin. Cancer Res. 11(18), 6634–6640 (2005).
[CrossRef] [PubMed]

K. L. Reckamp, K. Krysan, J. D. Morrow, G. L. Milne, R. A. Newman, C. Tucker, R. M. Elashoff, S. M. Dubinett, and R. A. Figlin, “A phase I trial to determine the optimal biological dose of celecoxib when combined with erlotinib in advanced non-small cell lung cancer,” Clin. Cancer Res. 12(11), 3381–3388 (2006).
[CrossRef] [PubMed]

Curr. Opin. Chem. Biol. (1)

M. Niepel, S. L. Spencer, and P. K. Sorger, “Non-genetic cell-to-cell variability and the consequences for pharmacology,” Curr. Opin. Chem. Biol. 13(5-6), 556–561 (2009).
[CrossRef] [PubMed]

Cytometry (1)

Z. Darzynkiewicz, G. Juan, X. Li, W. Gorczyca, T. Murakami, and F. Traganos, “Cytometry in cell necrobiology: analysis of apoptosis and accidental cell death (necrosis),” Cytometry 27(1), 1–20 (1997).
[CrossRef] [PubMed]

J. Biol. Chem. (1)

S. B. Nicholls, J. Chu, G. Abbruzzese, K. D. Tremblay, and J. A. Hardy, “Mechanism of a genetically encoded dark-to-bright reporter for caspase activity,” J. Biol. Chem. 286(28), 24977–24986 (2011).
[CrossRef] [PubMed]

J. Biomed. Opt. (3)

P. O. Bagnaninchi, C. Holmes, N. Drummond, J. Daoud, and M. Tabrizian, “Two-dimensional and three-dimensional viability measurements of adult stem cells with optical coherence phase microscopy,” J. Biomed. Opt. 16(8), 086003 (2011).
[CrossRef] [PubMed]

G. Häusler and M. W. Lindner, “Coherence radar and spectral radar—new tools for dermatological diagnosis,” J. Biomed. Opt. 3(1), 21–31 (1998).
[CrossRef]

R. Drezek, M. Guillaud, T. Collier, I. Boiko, A. Malpica, C. Macaulay, M. Follen, and R. Richards-Kortum, “Light scattering from cervical cells throughout neoplastic progression: influence of nuclear morphology, DNA content, and chromatin texture,” J. Biomed. Opt. 8(1), 7–16 (2003).
[CrossRef] [PubMed]

J. Biophotonics (2)

X. Liang, B. W. Graf, and S. A. Boppart, “Imaging engineered tissues using structural and functional optical coherence tomography,” J. Biophotonics 2(11), 643–655 (2009).
[CrossRef] [PubMed]

S. M. Rey, B. Povazay, B. Hofer, A. Unterhuber, B. Hermann, A. Harwood, and W. Drexler, “Three- and four-dimensional visualization of cell migration using optical coherence tomography,” J. Biophotonics 2(6-7), 370–379 (2009).
[CrossRef] [PubMed]

J. Invest. Dermatol. (2)

J. W. Tjiu, Y. H. Liao, S. J. Lin, Y. L. Huang, W. L. Tsai, C. Y. Chu, M. L. Kuo, and S. H. Jee, “Cyclooxygenase-2 overexpression in human basal cell carcinoma cell line increases antiapoptosis, angiogenesis, and tumorigenesis,” J. Invest. Dermatol. 126(5), 1143–1151 (2006).
[CrossRef] [PubMed]

J. W. Tjiu, J. S. Chen, C. T. Shun, S. J. Lin, Y. H. Liao, C. Y. Chu, T. F. Tsai, H. C. Chiu, Y. S. Dai, H. Inoue, P. C. Yang, M. L. Kuo, and S. H. Jee, “Tumor-associated macrophage-induced invasion and angiogenesis of human basal cell carcinoma cells by cyclooxygenase-2 induction,” J. Invest. Dermatol. 129(4), 1016–1025 (2009).
[CrossRef] [PubMed]

Mol. Cell (1)

J. G. Albeck, J. M. Burke, B. B. Aldridge, M. Zhang, D. A. Lauffenburger, and P. K. Sorger, “Quantitative analysis of pathways controlling extrinsic apoptosis in single cells,” Mol. Cell 30(1), 11–25 (2008).
[CrossRef] [PubMed]

Nat. Med. (1)

L. Liu, J. A. Gardecki, S. K. Nadkarni, J. D. Toussaint, Y. Yagi, B. E. Bouma, and G. J. Tearney, “Imaging the subcellular structure of human coronary atherosclerosis using micro-optical coherence tomography,” Nat. Med. 17(8), 1010–1014 (2011).
[CrossRef] [PubMed]

Nature (3)

R. Weissleder and M. J. Pittet, “Imaging in the era of molecular oncology,” Nature 452(7187), 580–589 (2008).
[CrossRef] [PubMed]

T. Reya, S. J. Morrison, M. F. Clarke, and I. L. Weissman, “Stem cells, cancer, and cancer stem cells,” Nature 414(6859), 105–111 (2001).
[CrossRef] [PubMed]

S. L. Spencer, S. Gaudet, J. G. Albeck, J. M. Burke, and P. K. Sorger, “Non-genetic origins of cell-to-cell variability in TRAIL-induced apoptosis,” Nature 459(7245), 428–432 (2009).
[CrossRef] [PubMed]

Opt. Express (1)

Opt. Lett. (2)

Phys. Med. Biol. (1)

W. C. Kuo, C. H. Chan, C. H. Chou, and J. C. Cheng, “Swept source optical coherence tomography for radiation-enhanced hepatocellular carcinoma cell invasion imaging,” Phys. Med. Biol. 54(13), 4289–4297 (2009).
[CrossRef] [PubMed]

PLoS ONE (3)

Y. Reis, M. Bernardo-Faura, D. Richter, T. Wolf, B. Brors, A. Hamacher-Brady, R. Eils, and N. R. Brady, “Multi-parametric analysis and modeling of relationships between mitochondrial morphology and apoptosis,” PLoS ONE 7(1), e28694 (2012).
[CrossRef] [PubMed]

M. Rehberg, F. Krombach, U. Pohl, and S. Dietzel, “Label-free 3D visualization of cellular and tissue structures in intact muscle with second and third harmonic generation microscopy,” PLoS ONE 6(11), e28237 (2011).
[CrossRef] [PubMed]

H. C. Huang, T. J. Mitchison, and J. Shi, “Stochastic competition between mechanistically independent slippage and death pathways determines cell fate during mitotic arrest,” PLoS ONE 5(12), e15724 (2010).
[CrossRef] [PubMed]

Proc. Natl. Acad. Sci. U.S.A. (1)

C. L. Evans, E. O. Potma, M. Puoris’haag, D. Côté, C. P. Lin, and X. S. Xie, “Chemical imaging of tissue in vivo with video-rate coherent anti-Stokes Raman scattering microscopy,” Proc. Natl. Acad. Sci. U.S.A. 102(46), 16807–16812 (2005).
[CrossRef] [PubMed]

Science (2)

A. A. Cohen, N. Geva-Zatorsky, E. Eden, M. Frenkel-Morgenstern, I. Issaeva, A. Sigal, R. Milo, C. Cohen-Saidon, Y. Liron, Z. Kam, L. Cohen, T. Danon, N. Perzov, and U. Alon, “Dynamic proteomics of individual cancer cells in response to a drug,” Science 322(5907), 1511–1516 (2008).
[CrossRef] [PubMed]

D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and et, “Optical coherence tomography,” Science 254(5035), 1178–1181 (1991).
[CrossRef] [PubMed]

Semin. Hematol. (1)

Z. Darzynkiewicz, E. Bedner, and P. Smolewski, “Flow cytometry in analysis of cell cycle and apoptosis,” Semin. Hematol. 38(2), 179–193 (2001).
[CrossRef] [PubMed]

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Figures (6)

Fig. 1
Fig. 1

A schema of UR-OCT system. LD: laser diode; L1 and L2: 40X and 60X aspheric lenses; OL: 4X objective lens; LPF: long-pass filters; M: mirror; BS: beam splitter; LWDO: 10X long working distance objective; FM: flipper mirror; PZA: piezo actuator; S: sample; LS: 2D linear stage; EP: eyepiece; PD: photo diode.

Fig. 2
Fig. 2

For each B-scan, intensity image (a) was transform into binary image by applying a threshold (b) which was higher than noise level by 3 dB on every pixels (c). The corresponding image of cell region which was found by automatically boundary detecting method (d). Cellular density can also calculated by dividing the area above the threshold and the total area of the bell shape intensity distribution diagram (e).

Fig. 3
Fig. 3

Microscopic image of BCC cell line and UR-OCT/confocal microscopy images of live and dead BCC cells. BCC cell line was suspended in Matrigel and imaged by a bright-field microscope (a). Live and dead BCC cells were randomly selected from the sample and scanned by UR-OCT and confocal microscopy. Live cell were encoded in green (b) and dead cell which was were encoded in red (e), according to the calcein and propidium’s fluorescence spectrum. Two-dimensional cross-sectional imaging (c, f) were performed across the center of each cell. Three-dimensional imaging of the whole cell (d, g) were realized by combining several cross-sectional images whose covering range were slightly larger than the size of the cells.

Fig. 4
Fig. 4

Co-registered BCC cells image of UR-OCT and confocal microscopy. En face image of UR-OCT (a) with corresponding CFM and CRM images (b, c) of BCC cells. The CFM and CRM images were acquired before UR-OCT imaging since the fluorescence decayed rapidly after staining procedure. Red arrows, strong scattering from small organelles.

Fig. 5
Fig. 5

Different properties between live and dead BCC cells. (a) Signal average; (b) cellular density; (c) average dynamic range; (d) cell volume of BCC cells. White bar, normal group (n = 7); black group, apoptotic group (n = 7); **P < 0.05. NS, not significant.

Fig. 6
Fig. 6

Correlation of signal average, cellular density, and average dynamic range between live and dead BCC cells. Scatter plots of cellular density and signal average, average dynamic range and signal average of live (a, c) and dead group (b, d). Significant positive correlations of the three parameters were observed in dead group.

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