Abstract

Fluorescence emission, polarization and subcellular localization of methylene blue (MB) were studied in four cancerous and two normal human brain cell lines. Fluorescence emission and polarization images were acquired and analyzed. The co-localization of MB with mitochondria, lysosomes and nuclei of the cells was evaluated. Glioblastoma cells exhibited significantly higher MB fluorescence polarization compared to normal astrocytes. Preferential accumulation of MB in mitochondria of glioblastoma cells may explain higher fluorescence polarization values in cancer cells as compared to normal. These findings may lead to the development of a quantitative method for the detection of brain cancer in single cells.

© 2019 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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References

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2019 (2)

A. N. Yaroslavsky, X. Feng, A. Muzikansky, and M. R. Hamblin, “Fluorescence polarization of methylene blue as a quantitative marker of breast cancer at the cellular level,” Sci. Rep. 9(1), 940 (2019).
[Crossref] [PubMed]

S. Malik, P. Jermain, X. Feng, and A. N. Yaroslavsky, “Multimodal optical imaging of renal cells,” Opt. Eng. 58(8), 082415 (2019).
[Crossref]

2018 (3)

F. S. Saadeh, R. Mahfouz, and H. I. Assi, “EGFR as a clinical marker in glioblastomas and other gliomas,” Int. J. Biol. Markers 33(1), 22–32 (2018).
[Crossref] [PubMed]

M. Haifler, I. Pence, Y. Sun, A. Kutikov, R. G. Uzzo, A. Mahadevan-Jansen, and C. A. Patil, “Discrimination of malignant and normal kidney tissue with short wave infrared dispersive Raman spectroscopy,” J. Biophotonics 11(6), e201700188 (2018).
[Crossref] [PubMed]

R. E. Kast, “Inhibiting the NLRP3 inflammasome with methylene blue as treatment adjunct in myelodysplasia,” Front. Oncol. 8(1), 280 (2018).
[Crossref] [PubMed]

2017 (2)

W. Szopa, T. A. Burley, G. Kramer-Marek, and W. Kaspera, “Diagnostic and therapeutic biomarkers in glioblastoma: current status and future perspectives,” BioMed Res. Int. 2017(1), 8013575 (2017).
[Crossref] [PubMed]

D. Cialla-May, X. S. Zheng, K. Weber, and J. Popp, “Recent progress in surface-enhanced Raman spectroscopy for biological and biomedical applications: from cells to clinics,” Chem. Soc. Rev. 46(13), 3945–3961 (2017).
[Crossref] [PubMed]

2016 (1)

L. Guntuku, V. G. Naidu, and V. G. Yerra, “Mitochondrial dysfunction in gliomas: pharmacotherapeutic potential of natural compounds,” Curr. Neuropharmacol. 14(6), 567–583 (2016).
[Crossref] [PubMed]

2015 (4)

T. F. Schmidt, L. Caseli, O. N. Oliveira, and R. Itri, “Binding of methylene blue onto Langmuir monolayers representing cell membranes may explain its efficiency as photosensitizer in photodynamic therapy,” Langmuir 31(14), 4205–4212 (2015).
[Crossref] [PubMed]

A. C. De Luca, K. Dholakia, and M. Mazilu, “Modulated Raman spectroscopy for enhanced cancer diagnosis at the cellular level,” Sensors (Basel) 15(6), 13680–13704 (2015).
[Crossref] [PubMed]

M. Jermyn, K. Mok, J. Mercier, J. Desroches, J. Pichette, K. Saint-Arnaud, L. Bernstein, M. C. Guiot, K. Petrecca, and F. Leblond, “Intraoperative brain cancer detection with Raman spectroscopy in humans,” Sci. Transl. Med. 7(274), 274ra19 (2015).
[Crossref] [PubMed]

D. Wirth, T. W. Smith, R. Moser, and A. N. Yaroslavsky, “Demeclocycline as a contrast agent for detecting brain neoplasms using confocal microscopy,” Phys. Med. Biol. 60(7), 3003–3011 (2015).
[Crossref] [PubMed]

2014 (1)

R. Patel, A. Khan, R. Quinlan, and A. N. Yaroslavsky, “Polarization-sensitive multimodal imaging for detecting breast cancer,” Cancer Res. 74(17), 4685–4693 (2014).
[Crossref] [PubMed]

2013 (3)

Z. Yang, Y. He, J.-H. Lee, N. Park, M. Suh, W.-S. Chae, J. Cao, X. Peng, H. Jung, C. Kang, and J. S. Kim, “A self-calibrating bipartite viscosity sensor for mitochondria,” J. Am. Chem. Soc. 135(24), 9181–9185 (2013).
[Crossref] [PubMed]

R. Patel, A. Khan, M. Kamionek, D. Kandil, R. Quinlan, and A. N. Yaroslavsky, “Delineating breast ductal carcinoma using combined dye-enhanced wide-field polarization imaging and optical coherence tomography,” J. Biophotonics 6(9), 679–686 (2013).
[Crossref] [PubMed]

M. Snuderl, D. Wirth, S. A. Sheth, S. K. Bourne, C. S. Kwon, M. Ancukiewicz, W. T. Curry, M. P. Frosch, and A. N. Yaroslavsky, “Dye-enhanced multimodal confocal imaging as a novel approach to intraoperative diagnosis of brain tumors,” Brain Pathol. 23(1), 73–81 (2013).
[Crossref] [PubMed]

2012 (2)

D. Wirth, M. Snuderl, S. Sheth, C. S. Kwon, M. P. Frosch, W. Curry, and A. N. Yaroslavsky, “Identifying brain neoplasms using dye-enhanced multimodal confocal imaging,” J. Biomed. Opt. 17(2), 026012 (2012).
[Crossref] [PubMed]

Y. Zhou, C. H. Liu, Y. Sun, Y. Pu, S. Boydston-White, Y. Liu, and R. R. Alfano, “Human brain cancer studied by resonance Raman spectroscopy,” J. Biomed. Opt. 17(11), 116021 (2012).
[Crossref] [PubMed]

2011 (1)

E. Kardash, J. Bandemer, and E. Raz, “Imaging protein activity in live embryos using fluorescence resonance energy transfer biosensors,” Nat. Protoc. 6(12), 1835–1846 (2011).
[Crossref] [PubMed]

2010 (2)

T. L. Chiu and C. C. Su, “Tanshinone IIA induces apoptosis in human lung cancer A549 cells through the induction of reactive oxygen species and decreasing the mitochondrial membrane potential,” Int. J. Mol. Med. 25(2), 231–236 (2010).
[PubMed]

Y. Sun, N. Hatami, M. Yee, J. Phipps, D. S. Elson, F. Gorin, R. J. Schrot, and L. Marcu, “Fluorescence lifetime imaging microscopy for brain tumor image-guided surgery,” J. Biomed. Opt. 15(5), 056022 (2010).
[Crossref] [PubMed]

2009 (1)

D. S. Kepshire, S. L. Gibbs-Strauss, J. A. O’Hara, M. Hutchins, N. Mincu, F. Leblond, M. Khayat, H. Dehghani, S. Srinivasan, and B. W. Pogue, “Imaging of glioma tumor with endogenous fluorescence tomography,” J. Biomed. Opt. 14(3), 030501 (2009).
[Crossref] [PubMed]

2007 (1)

M. C. Skala, K. M. Riching, D. K. Bird, A. Gendron-Fitzpatrick, J. Eickhoff, K. W. Eliceiri, P. J. Keely, and N. Ramanujam, “In vivo multiphoton fluorescence lifetime imaging of protein-bound and free nicotinamide adenine dinucleotide in normal and precancerous epithelia,” J. Biomed. Opt. 12(2), 024014 (2007).
[Crossref] [PubMed]

2005 (1)

J. P. Tardivo, A. Del Giglio, C. S. de Oliveira, D. S. Gabrielli, H. C. Junqueira, D. B. Tada, D. Severino, R. de Fátima Turchiello, and M. S. Baptista, “Methylene blue in photodynamic therapy: From basic mechanisms to clinical applications,” Photodiagn. Photodyn. Ther. 2(3), 175–191 (2005).
[Crossref] [PubMed]

2004 (2)

A. N. Yaroslavsky, V. Neel, and R. R. Anderson, “Fluorescence polarization imaging for delineating nonmelanoma skin cancers,” Opt. Lett. 29(17), 2010–2012 (2004).
[Crossref] [PubMed]

D. Gabrielli, E. Belisle, D. Severino, A. J. Kowaltowski, and M. S. Baptista, “Binding, aggregation and photochemical properties of methylene blue in mitochondrial suspensions,” Photochem. Photobiol. 79(3), 227–232 (2004).
[Crossref] [PubMed]

2003 (1)

J. Siegel, K. Suhling, S. Leveque-Fort, S. E. D. Webb, D. M. Davis, D. Phillips, Y. Sabharwal, and P. M. W. French, “Wide-field time-resolved fluorescence anisotropy imaging (TR-FAIM): imaging the rotational mobility of a fluorophore,” Rev. Sci. Instrum. 74(1), 182–192 (2003).
[Crossref]

1998 (2)

D. J. Ball, Y. Luo, D. Kessel, J. Griffiths, S. B. Brown, and D. I. Vernon, “The induction of apoptosis by a positively charged methylene blue derivative,” J. Photochem. Photobiol. B 42(2), 159–163 (1998).
[Crossref] [PubMed]

G. Marconi and R. Quintana, “Methylene blue dyeing of cellular nuclei during salpingoscopy, a new in-vivo method to evaluate vitality of tubal epithelium,” Hum. Reprod. 13(12), 3414–3417 (1998).
[Crossref] [PubMed]

1997 (1)

M. Wainwright, D. A. Phoenix, L. Rice, S. M. Burrow, and J. Waring, “Increased cytotoxicity and phototoxicity in the methylene blue series via chromophore methylation,” J. Photochem. Photobiol. B 40(3), 233–239 (1997).
[Crossref] [PubMed]

1993 (1)

D.-S. Yu, S.-Y. Chang, and C.-P. Ma, “The effect of methylene blue-sensitized photodynamic treatment on bladder cancer cells: a further study on flow cytometric basis,” J. Urol. 149(5), 1198–1201 (1993).
[Crossref] [PubMed]

1992 (1)

A. Rück, T. Köllner, A. Dietrich, W. Strauss, and H. Schneckenburger, “Fluorescence formation during photodynamic therapy in the nucleus of cells incubated with cationic and anionic water-soluble photosensitizers,” J. Photochem. Photobiol. B 12(4), 403–412 (1992).
[Crossref] [PubMed]

1990 (1)

F. Rashid and R. W. Horobin, “Interaction of molecular probes with living cells and tissues. Part 2. A structure-activity analysis of mitochondrial staining by cationic probes, and a discussion of the synergistic nature of image-based and biochemical approaches,” Histochemistry 94(3), 303–308 (1990).
[PubMed]

1988 (1)

L. B. Chen, “Mitochondrial membrane potential in living cells,” Annu. Rev. Cell Biol. 4(1), 155–181 (1988).
[Crossref] [PubMed]

1983 (1)

R. Santus, C. Kohen, E. Kohen, J. P. Reyftmann, P. Morliere, L. Dubertret, and P. M. Tocci, “Permeation of lysosomal membranes in the course of photosensitization with methylene blue and hematoporphyrin: study by cellular microspectrofluorometry,” Photochem. Photobiol. 38(1), 71–77 (1983).
[Crossref] [PubMed]

Alfano, R. R.

Y. Zhou, C. H. Liu, Y. Sun, Y. Pu, S. Boydston-White, Y. Liu, and R. R. Alfano, “Human brain cancer studied by resonance Raman spectroscopy,” J. Biomed. Opt. 17(11), 116021 (2012).
[Crossref] [PubMed]

Ancukiewicz, M.

M. Snuderl, D. Wirth, S. A. Sheth, S. K. Bourne, C. S. Kwon, M. Ancukiewicz, W. T. Curry, M. P. Frosch, and A. N. Yaroslavsky, “Dye-enhanced multimodal confocal imaging as a novel approach to intraoperative diagnosis of brain tumors,” Brain Pathol. 23(1), 73–81 (2013).
[Crossref] [PubMed]

Anderson, R. R.

Assi, H. I.

F. S. Saadeh, R. Mahfouz, and H. I. Assi, “EGFR as a clinical marker in glioblastomas and other gliomas,” Int. J. Biol. Markers 33(1), 22–32 (2018).
[Crossref] [PubMed]

Ball, D. J.

D. J. Ball, Y. Luo, D. Kessel, J. Griffiths, S. B. Brown, and D. I. Vernon, “The induction of apoptosis by a positively charged methylene blue derivative,” J. Photochem. Photobiol. B 42(2), 159–163 (1998).
[Crossref] [PubMed]

Bandemer, J.

E. Kardash, J. Bandemer, and E. Raz, “Imaging protein activity in live embryos using fluorescence resonance energy transfer biosensors,” Nat. Protoc. 6(12), 1835–1846 (2011).
[Crossref] [PubMed]

Baptista, M. S.

J. P. Tardivo, A. Del Giglio, C. S. de Oliveira, D. S. Gabrielli, H. C. Junqueira, D. B. Tada, D. Severino, R. de Fátima Turchiello, and M. S. Baptista, “Methylene blue in photodynamic therapy: From basic mechanisms to clinical applications,” Photodiagn. Photodyn. Ther. 2(3), 175–191 (2005).
[Crossref] [PubMed]

D. Gabrielli, E. Belisle, D. Severino, A. J. Kowaltowski, and M. S. Baptista, “Binding, aggregation and photochemical properties of methylene blue in mitochondrial suspensions,” Photochem. Photobiol. 79(3), 227–232 (2004).
[Crossref] [PubMed]

Belisle, E.

D. Gabrielli, E. Belisle, D. Severino, A. J. Kowaltowski, and M. S. Baptista, “Binding, aggregation and photochemical properties of methylene blue in mitochondrial suspensions,” Photochem. Photobiol. 79(3), 227–232 (2004).
[Crossref] [PubMed]

Bernstein, L.

M. Jermyn, K. Mok, J. Mercier, J. Desroches, J. Pichette, K. Saint-Arnaud, L. Bernstein, M. C. Guiot, K. Petrecca, and F. Leblond, “Intraoperative brain cancer detection with Raman spectroscopy in humans,” Sci. Transl. Med. 7(274), 274ra19 (2015).
[Crossref] [PubMed]

Bird, D. K.

M. C. Skala, K. M. Riching, D. K. Bird, A. Gendron-Fitzpatrick, J. Eickhoff, K. W. Eliceiri, P. J. Keely, and N. Ramanujam, “In vivo multiphoton fluorescence lifetime imaging of protein-bound and free nicotinamide adenine dinucleotide in normal and precancerous epithelia,” J. Biomed. Opt. 12(2), 024014 (2007).
[Crossref] [PubMed]

Bourne, S. K.

M. Snuderl, D. Wirth, S. A. Sheth, S. K. Bourne, C. S. Kwon, M. Ancukiewicz, W. T. Curry, M. P. Frosch, and A. N. Yaroslavsky, “Dye-enhanced multimodal confocal imaging as a novel approach to intraoperative diagnosis of brain tumors,” Brain Pathol. 23(1), 73–81 (2013).
[Crossref] [PubMed]

Boydston-White, S.

Y. Zhou, C. H. Liu, Y. Sun, Y. Pu, S. Boydston-White, Y. Liu, and R. R. Alfano, “Human brain cancer studied by resonance Raman spectroscopy,” J. Biomed. Opt. 17(11), 116021 (2012).
[Crossref] [PubMed]

Brown, S. B.

D. J. Ball, Y. Luo, D. Kessel, J. Griffiths, S. B. Brown, and D. I. Vernon, “The induction of apoptosis by a positively charged methylene blue derivative,” J. Photochem. Photobiol. B 42(2), 159–163 (1998).
[Crossref] [PubMed]

Burley, T. A.

W. Szopa, T. A. Burley, G. Kramer-Marek, and W. Kaspera, “Diagnostic and therapeutic biomarkers in glioblastoma: current status and future perspectives,” BioMed Res. Int. 2017(1), 8013575 (2017).
[Crossref] [PubMed]

Burrow, S. M.

M. Wainwright, D. A. Phoenix, L. Rice, S. M. Burrow, and J. Waring, “Increased cytotoxicity and phototoxicity in the methylene blue series via chromophore methylation,” J. Photochem. Photobiol. B 40(3), 233–239 (1997).
[Crossref] [PubMed]

Cao, J.

Z. Yang, Y. He, J.-H. Lee, N. Park, M. Suh, W.-S. Chae, J. Cao, X. Peng, H. Jung, C. Kang, and J. S. Kim, “A self-calibrating bipartite viscosity sensor for mitochondria,” J. Am. Chem. Soc. 135(24), 9181–9185 (2013).
[Crossref] [PubMed]

Caseli, L.

T. F. Schmidt, L. Caseli, O. N. Oliveira, and R. Itri, “Binding of methylene blue onto Langmuir monolayers representing cell membranes may explain its efficiency as photosensitizer in photodynamic therapy,” Langmuir 31(14), 4205–4212 (2015).
[Crossref] [PubMed]

Chae, W.-S.

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D. S. Kepshire, S. L. Gibbs-Strauss, J. A. O’Hara, M. Hutchins, N. Mincu, F. Leblond, M. Khayat, H. Dehghani, S. Srinivasan, and B. W. Pogue, “Imaging of glioma tumor with endogenous fluorescence tomography,” J. Biomed. Opt. 14(3), 030501 (2009).
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M. Jermyn, K. Mok, J. Mercier, J. Desroches, J. Pichette, K. Saint-Arnaud, L. Bernstein, M. C. Guiot, K. Petrecca, and F. Leblond, “Intraoperative brain cancer detection with Raman spectroscopy in humans,” Sci. Transl. Med. 7(274), 274ra19 (2015).
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Morliere, P.

R. Santus, C. Kohen, E. Kohen, J. P. Reyftmann, P. Morliere, L. Dubertret, and P. M. Tocci, “Permeation of lysosomal membranes in the course of photosensitization with methylene blue and hematoporphyrin: study by cellular microspectrofluorometry,” Photochem. Photobiol. 38(1), 71–77 (1983).
[Crossref] [PubMed]

Moser, R.

D. Wirth, T. W. Smith, R. Moser, and A. N. Yaroslavsky, “Demeclocycline as a contrast agent for detecting brain neoplasms using confocal microscopy,” Phys. Med. Biol. 60(7), 3003–3011 (2015).
[Crossref] [PubMed]

Muzikansky, A.

A. N. Yaroslavsky, X. Feng, A. Muzikansky, and M. R. Hamblin, “Fluorescence polarization of methylene blue as a quantitative marker of breast cancer at the cellular level,” Sci. Rep. 9(1), 940 (2019).
[Crossref] [PubMed]

Naidu, V. G.

L. Guntuku, V. G. Naidu, and V. G. Yerra, “Mitochondrial dysfunction in gliomas: pharmacotherapeutic potential of natural compounds,” Curr. Neuropharmacol. 14(6), 567–583 (2016).
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Neel, V.

O’Hara, J. A.

D. S. Kepshire, S. L. Gibbs-Strauss, J. A. O’Hara, M. Hutchins, N. Mincu, F. Leblond, M. Khayat, H. Dehghani, S. Srinivasan, and B. W. Pogue, “Imaging of glioma tumor with endogenous fluorescence tomography,” J. Biomed. Opt. 14(3), 030501 (2009).
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T. F. Schmidt, L. Caseli, O. N. Oliveira, and R. Itri, “Binding of methylene blue onto Langmuir monolayers representing cell membranes may explain its efficiency as photosensitizer in photodynamic therapy,” Langmuir 31(14), 4205–4212 (2015).
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Park, N.

Z. Yang, Y. He, J.-H. Lee, N. Park, M. Suh, W.-S. Chae, J. Cao, X. Peng, H. Jung, C. Kang, and J. S. Kim, “A self-calibrating bipartite viscosity sensor for mitochondria,” J. Am. Chem. Soc. 135(24), 9181–9185 (2013).
[Crossref] [PubMed]

Patel, R.

R. Patel, A. Khan, R. Quinlan, and A. N. Yaroslavsky, “Polarization-sensitive multimodal imaging for detecting breast cancer,” Cancer Res. 74(17), 4685–4693 (2014).
[Crossref] [PubMed]

R. Patel, A. Khan, M. Kamionek, D. Kandil, R. Quinlan, and A. N. Yaroslavsky, “Delineating breast ductal carcinoma using combined dye-enhanced wide-field polarization imaging and optical coherence tomography,” J. Biophotonics 6(9), 679–686 (2013).
[Crossref] [PubMed]

Patil, C. A.

M. Haifler, I. Pence, Y. Sun, A. Kutikov, R. G. Uzzo, A. Mahadevan-Jansen, and C. A. Patil, “Discrimination of malignant and normal kidney tissue with short wave infrared dispersive Raman spectroscopy,” J. Biophotonics 11(6), e201700188 (2018).
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M. Haifler, I. Pence, Y. Sun, A. Kutikov, R. G. Uzzo, A. Mahadevan-Jansen, and C. A. Patil, “Discrimination of malignant and normal kidney tissue with short wave infrared dispersive Raman spectroscopy,” J. Biophotonics 11(6), e201700188 (2018).
[Crossref] [PubMed]

Peng, X.

Z. Yang, Y. He, J.-H. Lee, N. Park, M. Suh, W.-S. Chae, J. Cao, X. Peng, H. Jung, C. Kang, and J. S. Kim, “A self-calibrating bipartite viscosity sensor for mitochondria,” J. Am. Chem. Soc. 135(24), 9181–9185 (2013).
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M. Jermyn, K. Mok, J. Mercier, J. Desroches, J. Pichette, K. Saint-Arnaud, L. Bernstein, M. C. Guiot, K. Petrecca, and F. Leblond, “Intraoperative brain cancer detection with Raman spectroscopy in humans,” Sci. Transl. Med. 7(274), 274ra19 (2015).
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J. Siegel, K. Suhling, S. Leveque-Fort, S. E. D. Webb, D. M. Davis, D. Phillips, Y. Sabharwal, and P. M. W. French, “Wide-field time-resolved fluorescence anisotropy imaging (TR-FAIM): imaging the rotational mobility of a fluorophore,” Rev. Sci. Instrum. 74(1), 182–192 (2003).
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Y. Sun, N. Hatami, M. Yee, J. Phipps, D. S. Elson, F. Gorin, R. J. Schrot, and L. Marcu, “Fluorescence lifetime imaging microscopy for brain tumor image-guided surgery,” J. Biomed. Opt. 15(5), 056022 (2010).
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M. Wainwright, D. A. Phoenix, L. Rice, S. M. Burrow, and J. Waring, “Increased cytotoxicity and phototoxicity in the methylene blue series via chromophore methylation,” J. Photochem. Photobiol. B 40(3), 233–239 (1997).
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M. Jermyn, K. Mok, J. Mercier, J. Desroches, J. Pichette, K. Saint-Arnaud, L. Bernstein, M. C. Guiot, K. Petrecca, and F. Leblond, “Intraoperative brain cancer detection with Raman spectroscopy in humans,” Sci. Transl. Med. 7(274), 274ra19 (2015).
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D. S. Kepshire, S. L. Gibbs-Strauss, J. A. O’Hara, M. Hutchins, N. Mincu, F. Leblond, M. Khayat, H. Dehghani, S. Srinivasan, and B. W. Pogue, “Imaging of glioma tumor with endogenous fluorescence tomography,” J. Biomed. Opt. 14(3), 030501 (2009).
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Popp, J.

D. Cialla-May, X. S. Zheng, K. Weber, and J. Popp, “Recent progress in surface-enhanced Raman spectroscopy for biological and biomedical applications: from cells to clinics,” Chem. Soc. Rev. 46(13), 3945–3961 (2017).
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Y. Zhou, C. H. Liu, Y. Sun, Y. Pu, S. Boydston-White, Y. Liu, and R. R. Alfano, “Human brain cancer studied by resonance Raman spectroscopy,” J. Biomed. Opt. 17(11), 116021 (2012).
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R. Patel, A. Khan, R. Quinlan, and A. N. Yaroslavsky, “Polarization-sensitive multimodal imaging for detecting breast cancer,” Cancer Res. 74(17), 4685–4693 (2014).
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R. Patel, A. Khan, M. Kamionek, D. Kandil, R. Quinlan, and A. N. Yaroslavsky, “Delineating breast ductal carcinoma using combined dye-enhanced wide-field polarization imaging and optical coherence tomography,” J. Biophotonics 6(9), 679–686 (2013).
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G. Marconi and R. Quintana, “Methylene blue dyeing of cellular nuclei during salpingoscopy, a new in-vivo method to evaluate vitality of tubal epithelium,” Hum. Reprod. 13(12), 3414–3417 (1998).
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A. N. Yaroslavsky, X. Feng, Y. Ramirez, Y. Huang, A. Ross, and M. R. Hamblin, “Detecting brain cancer using fluorescence polarization imaging,” Proc. SPIE, 1048017 (2018).

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F. Rashid and R. W. Horobin, “Interaction of molecular probes with living cells and tissues. Part 2. A structure-activity analysis of mitochondrial staining by cationic probes, and a discussion of the synergistic nature of image-based and biochemical approaches,” Histochemistry 94(3), 303–308 (1990).
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R. Santus, C. Kohen, E. Kohen, J. P. Reyftmann, P. Morliere, L. Dubertret, and P. M. Tocci, “Permeation of lysosomal membranes in the course of photosensitization with methylene blue and hematoporphyrin: study by cellular microspectrofluorometry,” Photochem. Photobiol. 38(1), 71–77 (1983).
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Rice, L.

M. Wainwright, D. A. Phoenix, L. Rice, S. M. Burrow, and J. Waring, “Increased cytotoxicity and phototoxicity in the methylene blue series via chromophore methylation,” J. Photochem. Photobiol. B 40(3), 233–239 (1997).
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M. C. Skala, K. M. Riching, D. K. Bird, A. Gendron-Fitzpatrick, J. Eickhoff, K. W. Eliceiri, P. J. Keely, and N. Ramanujam, “In vivo multiphoton fluorescence lifetime imaging of protein-bound and free nicotinamide adenine dinucleotide in normal and precancerous epithelia,” J. Biomed. Opt. 12(2), 024014 (2007).
[Crossref] [PubMed]

Ross, A.

A. N. Yaroslavsky, X. Feng, Y. Ramirez, Y. Huang, A. Ross, and M. R. Hamblin, “Detecting brain cancer using fluorescence polarization imaging,” Proc. SPIE, 1048017 (2018).

Rück, A.

A. Rück, T. Köllner, A. Dietrich, W. Strauss, and H. Schneckenburger, “Fluorescence formation during photodynamic therapy in the nucleus of cells incubated with cationic and anionic water-soluble photosensitizers,” J. Photochem. Photobiol. B 12(4), 403–412 (1992).
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F. S. Saadeh, R. Mahfouz, and H. I. Assi, “EGFR as a clinical marker in glioblastomas and other gliomas,” Int. J. Biol. Markers 33(1), 22–32 (2018).
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Sabharwal, Y.

J. Siegel, K. Suhling, S. Leveque-Fort, S. E. D. Webb, D. M. Davis, D. Phillips, Y. Sabharwal, and P. M. W. French, “Wide-field time-resolved fluorescence anisotropy imaging (TR-FAIM): imaging the rotational mobility of a fluorophore,” Rev. Sci. Instrum. 74(1), 182–192 (2003).
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M. Jermyn, K. Mok, J. Mercier, J. Desroches, J. Pichette, K. Saint-Arnaud, L. Bernstein, M. C. Guiot, K. Petrecca, and F. Leblond, “Intraoperative brain cancer detection with Raman spectroscopy in humans,” Sci. Transl. Med. 7(274), 274ra19 (2015).
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Santus, R.

R. Santus, C. Kohen, E. Kohen, J. P. Reyftmann, P. Morliere, L. Dubertret, and P. M. Tocci, “Permeation of lysosomal membranes in the course of photosensitization with methylene blue and hematoporphyrin: study by cellular microspectrofluorometry,” Photochem. Photobiol. 38(1), 71–77 (1983).
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Schmidt, T. F.

T. F. Schmidt, L. Caseli, O. N. Oliveira, and R. Itri, “Binding of methylene blue onto Langmuir monolayers representing cell membranes may explain its efficiency as photosensitizer in photodynamic therapy,” Langmuir 31(14), 4205–4212 (2015).
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Schneckenburger, H.

A. Rück, T. Köllner, A. Dietrich, W. Strauss, and H. Schneckenburger, “Fluorescence formation during photodynamic therapy in the nucleus of cells incubated with cationic and anionic water-soluble photosensitizers,” J. Photochem. Photobiol. B 12(4), 403–412 (1992).
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Y. Sun, N. Hatami, M. Yee, J. Phipps, D. S. Elson, F. Gorin, R. J. Schrot, and L. Marcu, “Fluorescence lifetime imaging microscopy for brain tumor image-guided surgery,” J. Biomed. Opt. 15(5), 056022 (2010).
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J. P. Tardivo, A. Del Giglio, C. S. de Oliveira, D. S. Gabrielli, H. C. Junqueira, D. B. Tada, D. Severino, R. de Fátima Turchiello, and M. S. Baptista, “Methylene blue in photodynamic therapy: From basic mechanisms to clinical applications,” Photodiagn. Photodyn. Ther. 2(3), 175–191 (2005).
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D. Gabrielli, E. Belisle, D. Severino, A. J. Kowaltowski, and M. S. Baptista, “Binding, aggregation and photochemical properties of methylene blue in mitochondrial suspensions,” Photochem. Photobiol. 79(3), 227–232 (2004).
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D. Wirth, M. Snuderl, S. Sheth, C. S. Kwon, M. P. Frosch, W. Curry, and A. N. Yaroslavsky, “Identifying brain neoplasms using dye-enhanced multimodal confocal imaging,” J. Biomed. Opt. 17(2), 026012 (2012).
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Sheth, S. A.

M. Snuderl, D. Wirth, S. A. Sheth, S. K. Bourne, C. S. Kwon, M. Ancukiewicz, W. T. Curry, M. P. Frosch, and A. N. Yaroslavsky, “Dye-enhanced multimodal confocal imaging as a novel approach to intraoperative diagnosis of brain tumors,” Brain Pathol. 23(1), 73–81 (2013).
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J. Siegel, K. Suhling, S. Leveque-Fort, S. E. D. Webb, D. M. Davis, D. Phillips, Y. Sabharwal, and P. M. W. French, “Wide-field time-resolved fluorescence anisotropy imaging (TR-FAIM): imaging the rotational mobility of a fluorophore,” Rev. Sci. Instrum. 74(1), 182–192 (2003).
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M. C. Skala, K. M. Riching, D. K. Bird, A. Gendron-Fitzpatrick, J. Eickhoff, K. W. Eliceiri, P. J. Keely, and N. Ramanujam, “In vivo multiphoton fluorescence lifetime imaging of protein-bound and free nicotinamide adenine dinucleotide in normal and precancerous epithelia,” J. Biomed. Opt. 12(2), 024014 (2007).
[Crossref] [PubMed]

Smith, T. W.

D. Wirth, T. W. Smith, R. Moser, and A. N. Yaroslavsky, “Demeclocycline as a contrast agent for detecting brain neoplasms using confocal microscopy,” Phys. Med. Biol. 60(7), 3003–3011 (2015).
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Snuderl, M.

M. Snuderl, D. Wirth, S. A. Sheth, S. K. Bourne, C. S. Kwon, M. Ancukiewicz, W. T. Curry, M. P. Frosch, and A. N. Yaroslavsky, “Dye-enhanced multimodal confocal imaging as a novel approach to intraoperative diagnosis of brain tumors,” Brain Pathol. 23(1), 73–81 (2013).
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D. Wirth, M. Snuderl, S. Sheth, C. S. Kwon, M. P. Frosch, W. Curry, and A. N. Yaroslavsky, “Identifying brain neoplasms using dye-enhanced multimodal confocal imaging,” J. Biomed. Opt. 17(2), 026012 (2012).
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Srinivasan, S.

D. S. Kepshire, S. L. Gibbs-Strauss, J. A. O’Hara, M. Hutchins, N. Mincu, F. Leblond, M. Khayat, H. Dehghani, S. Srinivasan, and B. W. Pogue, “Imaging of glioma tumor with endogenous fluorescence tomography,” J. Biomed. Opt. 14(3), 030501 (2009).
[Crossref] [PubMed]

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A. Rück, T. Köllner, A. Dietrich, W. Strauss, and H. Schneckenburger, “Fluorescence formation during photodynamic therapy in the nucleus of cells incubated with cationic and anionic water-soluble photosensitizers,” J. Photochem. Photobiol. B 12(4), 403–412 (1992).
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J. Siegel, K. Suhling, S. Leveque-Fort, S. E. D. Webb, D. M. Davis, D. Phillips, Y. Sabharwal, and P. M. W. French, “Wide-field time-resolved fluorescence anisotropy imaging (TR-FAIM): imaging the rotational mobility of a fluorophore,” Rev. Sci. Instrum. 74(1), 182–192 (2003).
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Sun, Y.

M. Haifler, I. Pence, Y. Sun, A. Kutikov, R. G. Uzzo, A. Mahadevan-Jansen, and C. A. Patil, “Discrimination of malignant and normal kidney tissue with short wave infrared dispersive Raman spectroscopy,” J. Biophotonics 11(6), e201700188 (2018).
[Crossref] [PubMed]

Y. Zhou, C. H. Liu, Y. Sun, Y. Pu, S. Boydston-White, Y. Liu, and R. R. Alfano, “Human brain cancer studied by resonance Raman spectroscopy,” J. Biomed. Opt. 17(11), 116021 (2012).
[Crossref] [PubMed]

Y. Sun, N. Hatami, M. Yee, J. Phipps, D. S. Elson, F. Gorin, R. J. Schrot, and L. Marcu, “Fluorescence lifetime imaging microscopy for brain tumor image-guided surgery,” J. Biomed. Opt. 15(5), 056022 (2010).
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J. P. Tardivo, A. Del Giglio, C. S. de Oliveira, D. S. Gabrielli, H. C. Junqueira, D. B. Tada, D. Severino, R. de Fátima Turchiello, and M. S. Baptista, “Methylene blue in photodynamic therapy: From basic mechanisms to clinical applications,” Photodiagn. Photodyn. Ther. 2(3), 175–191 (2005).
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J. P. Tardivo, A. Del Giglio, C. S. de Oliveira, D. S. Gabrielli, H. C. Junqueira, D. B. Tada, D. Severino, R. de Fátima Turchiello, and M. S. Baptista, “Methylene blue in photodynamic therapy: From basic mechanisms to clinical applications,” Photodiagn. Photodyn. Ther. 2(3), 175–191 (2005).
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Tocci, P. M.

R. Santus, C. Kohen, E. Kohen, J. P. Reyftmann, P. Morliere, L. Dubertret, and P. M. Tocci, “Permeation of lysosomal membranes in the course of photosensitization with methylene blue and hematoporphyrin: study by cellular microspectrofluorometry,” Photochem. Photobiol. 38(1), 71–77 (1983).
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M. Haifler, I. Pence, Y. Sun, A. Kutikov, R. G. Uzzo, A. Mahadevan-Jansen, and C. A. Patil, “Discrimination of malignant and normal kidney tissue with short wave infrared dispersive Raman spectroscopy,” J. Biophotonics 11(6), e201700188 (2018).
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M. Wainwright, D. A. Phoenix, L. Rice, S. M. Burrow, and J. Waring, “Increased cytotoxicity and phototoxicity in the methylene blue series via chromophore methylation,” J. Photochem. Photobiol. B 40(3), 233–239 (1997).
[Crossref] [PubMed]

Waring, J.

M. Wainwright, D. A. Phoenix, L. Rice, S. M. Burrow, and J. Waring, “Increased cytotoxicity and phototoxicity in the methylene blue series via chromophore methylation,” J. Photochem. Photobiol. B 40(3), 233–239 (1997).
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Webb, S. E. D.

J. Siegel, K. Suhling, S. Leveque-Fort, S. E. D. Webb, D. M. Davis, D. Phillips, Y. Sabharwal, and P. M. W. French, “Wide-field time-resolved fluorescence anisotropy imaging (TR-FAIM): imaging the rotational mobility of a fluorophore,” Rev. Sci. Instrum. 74(1), 182–192 (2003).
[Crossref]

Weber, K.

D. Cialla-May, X. S. Zheng, K. Weber, and J. Popp, “Recent progress in surface-enhanced Raman spectroscopy for biological and biomedical applications: from cells to clinics,” Chem. Soc. Rev. 46(13), 3945–3961 (2017).
[Crossref] [PubMed]

Wirth, D.

D. Wirth, T. W. Smith, R. Moser, and A. N. Yaroslavsky, “Demeclocycline as a contrast agent for detecting brain neoplasms using confocal microscopy,” Phys. Med. Biol. 60(7), 3003–3011 (2015).
[Crossref] [PubMed]

M. Snuderl, D. Wirth, S. A. Sheth, S. K. Bourne, C. S. Kwon, M. Ancukiewicz, W. T. Curry, M. P. Frosch, and A. N. Yaroslavsky, “Dye-enhanced multimodal confocal imaging as a novel approach to intraoperative diagnosis of brain tumors,” Brain Pathol. 23(1), 73–81 (2013).
[Crossref] [PubMed]

D. Wirth, M. Snuderl, S. Sheth, C. S. Kwon, M. P. Frosch, W. Curry, and A. N. Yaroslavsky, “Identifying brain neoplasms using dye-enhanced multimodal confocal imaging,” J. Biomed. Opt. 17(2), 026012 (2012).
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Z. Yang, Y. He, J.-H. Lee, N. Park, M. Suh, W.-S. Chae, J. Cao, X. Peng, H. Jung, C. Kang, and J. S. Kim, “A self-calibrating bipartite viscosity sensor for mitochondria,” J. Am. Chem. Soc. 135(24), 9181–9185 (2013).
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Yaroslavsky, A. N.

S. Malik, P. Jermain, X. Feng, and A. N. Yaroslavsky, “Multimodal optical imaging of renal cells,” Opt. Eng. 58(8), 082415 (2019).
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A. N. Yaroslavsky, X. Feng, A. Muzikansky, and M. R. Hamblin, “Fluorescence polarization of methylene blue as a quantitative marker of breast cancer at the cellular level,” Sci. Rep. 9(1), 940 (2019).
[Crossref] [PubMed]

D. Wirth, T. W. Smith, R. Moser, and A. N. Yaroslavsky, “Demeclocycline as a contrast agent for detecting brain neoplasms using confocal microscopy,” Phys. Med. Biol. 60(7), 3003–3011 (2015).
[Crossref] [PubMed]

R. Patel, A. Khan, R. Quinlan, and A. N. Yaroslavsky, “Polarization-sensitive multimodal imaging for detecting breast cancer,” Cancer Res. 74(17), 4685–4693 (2014).
[Crossref] [PubMed]

M. Snuderl, D. Wirth, S. A. Sheth, S. K. Bourne, C. S. Kwon, M. Ancukiewicz, W. T. Curry, M. P. Frosch, and A. N. Yaroslavsky, “Dye-enhanced multimodal confocal imaging as a novel approach to intraoperative diagnosis of brain tumors,” Brain Pathol. 23(1), 73–81 (2013).
[Crossref] [PubMed]

R. Patel, A. Khan, M. Kamionek, D. Kandil, R. Quinlan, and A. N. Yaroslavsky, “Delineating breast ductal carcinoma using combined dye-enhanced wide-field polarization imaging and optical coherence tomography,” J. Biophotonics 6(9), 679–686 (2013).
[Crossref] [PubMed]

D. Wirth, M. Snuderl, S. Sheth, C. S. Kwon, M. P. Frosch, W. Curry, and A. N. Yaroslavsky, “Identifying brain neoplasms using dye-enhanced multimodal confocal imaging,” J. Biomed. Opt. 17(2), 026012 (2012).
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A. N. Yaroslavsky, V. Neel, and R. R. Anderson, “Fluorescence polarization imaging for delineating nonmelanoma skin cancers,” Opt. Lett. 29(17), 2010–2012 (2004).
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A. N. Yaroslavsky, X. Feng, Y. Ramirez, Y. Huang, A. Ross, and M. R. Hamblin, “Detecting brain cancer using fluorescence polarization imaging,” Proc. SPIE, 1048017 (2018).

Yee, M.

Y. Sun, N. Hatami, M. Yee, J. Phipps, D. S. Elson, F. Gorin, R. J. Schrot, and L. Marcu, “Fluorescence lifetime imaging microscopy for brain tumor image-guided surgery,” J. Biomed. Opt. 15(5), 056022 (2010).
[Crossref] [PubMed]

Yerra, V. G.

L. Guntuku, V. G. Naidu, and V. G. Yerra, “Mitochondrial dysfunction in gliomas: pharmacotherapeutic potential of natural compounds,” Curr. Neuropharmacol. 14(6), 567–583 (2016).
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D.-S. Yu, S.-Y. Chang, and C.-P. Ma, “The effect of methylene blue-sensitized photodynamic treatment on bladder cancer cells: a further study on flow cytometric basis,” J. Urol. 149(5), 1198–1201 (1993).
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D. Cialla-May, X. S. Zheng, K. Weber, and J. Popp, “Recent progress in surface-enhanced Raman spectroscopy for biological and biomedical applications: from cells to clinics,” Chem. Soc. Rev. 46(13), 3945–3961 (2017).
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Figures (4)

Fig. 1
Fig. 1 Schematic of the point scanning confocal fluorescence polarization imaging system. 1 – 642 nm laser, 2 – dichroic mirror, 3 – polygon mirror, 4 – galvanometric mirror, 5 – objective, 6 – sample plane, 7 – focusing lens, 8 – fluorescence filter, 9 – pinhole, 10 – polarizing beam splitter, 11 – PMT for cross-polarized fluorescence, 12 – PMT for co-polarized fluorescence, 13 – computer.
Fig. 2
Fig. 2 Methylene blue (MB) fluorescence emission images of normal astrocytes (a, b) and glioblastoma cells (c-f). Cells were stained with 0.05 mg/ml MB. Bar: 50 µm.
Fig. 3
Fig. 3 Methylene blue (MB) fluorescence polarization images of normal astrocytes (a, b) and glioblastoma cells (c-f). Cells were stained with 0.05 mg/ml MB. Bar: 50 µm
Fig. 4
Fig. 4 Degree of co-localization between MB staining and the stain used to visualize (a) nucleus (Hoechst-33342), (b) lysosomes (LysoTracker) and (c) mitochondria (MitoTracker). N is the number of cells analyzed. *p<0.0001

Tables (2)

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Table 1 Cell line information and percentage differences of MB FP between glioblastoma cells and normal astrocytes (all the cells).

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Table 2 Cell line information, MB FP values and percentage differences of MB FP between glioblastoma cells and normal astrocytes. (a) Analysis of the entire cell; (b) analysis of these cells with nuclei excluded; (c) analysis of the cell nuclei.

Equations (2)

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G= F vv F hh × F hv F vh
FP= F // G× F F // +G× F

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