Abstract

Collagen is the main structural protein and the key determinant of mechanical and functional properties of tissues and organs. Proper balance between synthesis and degradation of collagen molecules is critical for maintaining normal physiological functions. In addition, collagen influences tumor development and drug delivery, which makes it a potential cancer therapy target. Using second harmonic generation, two-photon excited fluorescence microscopy, and spectrofluorimetry, we show that the natural pigment hypericin induces photosensitized destruction of collagen-based tissues. We demonstrate that hypericin–mediated processes in collagen fibers are irreversible and may be used for the treatment of cancer and collagen-related disorders.

© 2014 Optical Society of America

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    [CrossRef] [PubMed]
  25. I. Georgakoudi, B. C. Jacobson, M. G. Müller, E. E. Sheets, K. Badizadegan, D. L. Carr-Locke, C. P. Crum, C. W. Boone, R. R. Dasari, J. Van Dam, and M. S. Feld, “NAD(P)H and collagen as in vivo quantitative fluorescent biomarkers of epithelial precancerous changes,” Cancer Res.62(3), 682–687 (2002).
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2012 (4)

A. L. Maas, S. L. Carter, E. P. Wileyto, J. Miller, M. Yuan, G. Yu, A. C. Durham, and T. M. Busch, “Tumor vascular microenvironment determines responsiveness to photodynamic therapy,” Cancer Res.72(8), 2079–2088 (2012).
[CrossRef] [PubMed]

R. Ambekar, T. Y. Lau, M. Walsh, R. Bhargava, and K. C. Toussaint., “Quantifying collagen structure in breast biopsies using second-harmonic generation imaging,” Biomed. Opt. Express3(9), 2021–2035 (2012).
[CrossRef] [PubMed]

T. Lv, Z. F. Huang, H. W. Wang, J. Q. Lin, G. N. Chen, X. W. Chen, R. Chen, Z. Huang, and X. L. Wang, “Evaluation of collagen alteration after topical photodynamic therapy (PDT) using second harmonic generation (SHG) microscopy--in vivo study in a mouse model,” Photodiagn. Photodyn. Ther.9(2), 164–169 (2012).
[CrossRef] [PubMed]

P. Pande, B. E. Applegate, and J. A. Jo, “Application of non-negative matrix factorization to multispectral FLIM data analysis,” Biomed. Opt. Express3(9), 2244–2262 (2012).
[CrossRef] [PubMed]

2011 (3)

2009 (1)

V. A. Hovhannisyan, P. J. Su, S. J. Lin, and C.-Y. Dong, “Quantifying thermodynamics of collagen thermal denaturation by second harmonic generation imaging,” Appl. Phys. Lett.94(23), 233902 (2009).
[CrossRef]

2008 (4)

V. Hovhannisyan, W. Lo, C. Hu, S. J. Chen, and C. Y. Dong, “Dynamics of femtosecond laser photo-modification of collagen fibers,” Opt. Express16(11), 7958–7968 (2008).
[CrossRef] [PubMed]

G. Seitz, R. Krause, J. Fuchs, H. Heitmann, S. Armeanu, P. Ruck, and S. W. Warmann, “In vitro photodynamic therapy in pediatric epithelial liver tumors promoted by hypericin,” Oncol. Rep.20(5), 1277–1282 (2008).
[PubMed]

Y. Shintani, M. Maeda, N. Chaika, K. R. Johnson, and M. J. Wheelock, “Collagen I promotes epithelial-to-mesenchymal transition in lung cancer cells via transforming growth factor-β signaling,” Am. J. Respir. Cell Mol. Biol.38(1), 95–104 (2008).
[CrossRef] [PubMed]

L. M. Davids, B. Kleemann, D. Kacerovská, K. Pizinger, and S. H. Kidson, “Hypericin phototoxicity induces different modes of cell death in melanoma and human skin cells,” J. Photochem. Photobiol. B91(2-3), 67–76 (2008).
[CrossRef] [PubMed]

2005 (1)

2002 (2)

B. S. P. Miskovsky, “Hypericin--a new antiviral and antitumor photosensitizer: mechanism of action and interaction with biological macromolecules,” Curr. Drug Targets3(1), 55–84 (2002).
[CrossRef] [PubMed]

I. Georgakoudi, B. C. Jacobson, M. G. Müller, E. E. Sheets, K. Badizadegan, D. L. Carr-Locke, C. P. Crum, C. W. Boone, R. R. Dasari, J. Van Dam, and M. S. Feld, “NAD(P)H and collagen as in vivo quantitative fluorescent biomarkers of epithelial precancerous changes,” Cancer Res.62(3), 682–687 (2002).
[PubMed]

2001 (1)

D. Yova, V. Hovhannisyan, and T. Theodossiou, “Photochemical effects and hypericin photosensitized processes in collagen,” J. Biomed. Opt.6(1), 52–57 (2001).
[CrossRef] [PubMed]

2000 (1)

W. G. Liu, K. D. Yao, G. C. Wang, and H. X. Li, “Intrinsic fluorescence investigation on the change in conformation of cross-linked gelatin gel during volume phase transition,” Polymer (Guildf.)41(20), 7589–7592 (2000).
[CrossRef]

1997 (3)

J. M. Fernandez, M. D. Bilgin, and L. I. Grossweiner, “Singlet oxygen generation by photodynamic agents,” J. Photochem. Photobiol. B37(1–2), 131–140 (1997).
[CrossRef]

D. S. English, K. Das, K. D. Ashby, J. Park, J. W. Petrich, and E. W. Castner, “Confirmation of excited-state proton transfer and ground-state heterogeneity in hypericin by fluorescence upconversion,” J. Am. Chem. Soc.119(48), 11585–11590 (1997).
[CrossRef]

T. A. Wells, A. Losi, R. Dai, P. Scott, S. M. Park, J. Golbeck, and P. S. Song, “Electron transfer quenching and photoinduced EPR of hypericin and the ciliate photoreceptor stentorian,” J. Phys. Chem. A101(4), 366–372 (1997).
[CrossRef]

1996 (1)

H. Koren, G. M. Schenk, R. H. Jindra, G. Alth, R. Ebermann, A. Kubin, G. Koderhold, and M. Kreitner, “Hypericin in phototherapy,” J. Photochem. Photobiol. B36(2), 113–119 (1996).
[CrossRef] [PubMed]

1994 (1)

N. D. Weber, B. K. Murray, J. A. North, and S. G. Wood, “The antiviral agent hypericin has in vitro activity against HSV-1 through non-specific association with viral and cellular membranes,” AntiViral Chem. Chemother.5(2), 83–90 (1994).

1991 (1)

S. Carpenter and G. A. Kraus, “Photosensitization is required for inactivation of equine infectious anemia virus by hypericin,” Photochem. Photobiol.53(2), 169–174 (1991).
[CrossRef] [PubMed]

1988 (1)

D. Meruelo, G. Lavie, and D. Lavie, “Therapeutic agents with dramatic antiretroviral activity and little toxicity at effective doses: Aromatic polycyclic diones hypericin and pseudohypericin,” Proc. Natl. Acad. Sci. U.S.A.85(14), 5230–5234 (1988).
[CrossRef] [PubMed]

1978 (1)

T. Hayashi, “Time-dependent increase in the stability of collagen fibrils formed in vitro. I. Effects of pH and salt concentration on the dissolution of the fibrils,” J. Biochem.84(2), 245–249 (1978).
[PubMed]

1977 (1)

D. Fujimoto, K. Akiba, and N. Nakamura, “Isolation and characterization of a fluorescent material in bovine Achilles tendon collagen,” Biochem. Biophys. Res. Commun.76(4), 1124–1129 (1977).
[CrossRef] [PubMed]

1971 (1)

Akiba, K.

D. Fujimoto, K. Akiba, and N. Nakamura, “Isolation and characterization of a fluorescent material in bovine Achilles tendon collagen,” Biochem. Biophys. Res. Commun.76(4), 1124–1129 (1977).
[CrossRef] [PubMed]

Alth, G.

H. Koren, G. M. Schenk, R. H. Jindra, G. Alth, R. Ebermann, A. Kubin, G. Koderhold, and M. Kreitner, “Hypericin in phototherapy,” J. Photochem. Photobiol. B36(2), 113–119 (1996).
[CrossRef] [PubMed]

Ambekar, R.

Applegate, B. E.

Appley, A. J.

W. T. Couldwell, A. A. Surnock, A. J. Tobia, B. E. Cabana, C. B. Stillerman, P. A. Forsyth, A. J. Appley, A. M. Spence, D. R. Hinton, and T. C. Chen, “A phase 1/2 study of orally administered synthetic hypericin for treatment of recurrent malignant gliomas,” Cancer117(21), 4905–4915 (2011).
[CrossRef] [PubMed]

Armeanu, S.

G. Seitz, R. Krause, J. Fuchs, H. Heitmann, S. Armeanu, P. Ruck, and S. W. Warmann, “In vitro photodynamic therapy in pediatric epithelial liver tumors promoted by hypericin,” Oncol. Rep.20(5), 1277–1282 (2008).
[PubMed]

Artal, P.

Ashby, K. D.

D. S. English, K. Das, K. D. Ashby, J. Park, J. W. Petrich, and E. W. Castner, “Confirmation of excited-state proton transfer and ground-state heterogeneity in hypericin by fluorescence upconversion,” J. Am. Chem. Soc.119(48), 11585–11590 (1997).
[CrossRef]

Badizadegan, K.

I. Georgakoudi, B. C. Jacobson, M. G. Müller, E. E. Sheets, K. Badizadegan, D. L. Carr-Locke, C. P. Crum, C. W. Boone, R. R. Dasari, J. Van Dam, and M. S. Feld, “NAD(P)H and collagen as in vivo quantitative fluorescent biomarkers of epithelial precancerous changes,” Cancer Res.62(3), 682–687 (2002).
[PubMed]

Becker, D. L.

Bhargava, R.

Bilgin, M. D.

J. M. Fernandez, M. D. Bilgin, and L. I. Grossweiner, “Singlet oxygen generation by photodynamic agents,” J. Photochem. Photobiol. B37(1–2), 131–140 (1997).
[CrossRef]

Boone, C. W.

I. Georgakoudi, B. C. Jacobson, M. G. Müller, E. E. Sheets, K. Badizadegan, D. L. Carr-Locke, C. P. Crum, C. W. Boone, R. R. Dasari, J. Van Dam, and M. S. Feld, “NAD(P)H and collagen as in vivo quantitative fluorescent biomarkers of epithelial precancerous changes,” Cancer Res.62(3), 682–687 (2002).
[PubMed]

Bueno, J. M.

Busch, T. M.

A. L. Maas, S. L. Carter, E. P. Wileyto, J. Miller, M. Yuan, G. Yu, A. C. Durham, and T. M. Busch, “Tumor vascular microenvironment determines responsiveness to photodynamic therapy,” Cancer Res.72(8), 2079–2088 (2012).
[CrossRef] [PubMed]

Cabana, B. E.

W. T. Couldwell, A. A. Surnock, A. J. Tobia, B. E. Cabana, C. B. Stillerman, P. A. Forsyth, A. J. Appley, A. M. Spence, D. R. Hinton, and T. C. Chen, “A phase 1/2 study of orally administered synthetic hypericin for treatment of recurrent malignant gliomas,” Cancer117(21), 4905–4915 (2011).
[CrossRef] [PubMed]

Carpenter, S.

S. Carpenter and G. A. Kraus, “Photosensitization is required for inactivation of equine infectious anemia virus by hypericin,” Photochem. Photobiol.53(2), 169–174 (1991).
[CrossRef] [PubMed]

Carr-Locke, D. L.

I. Georgakoudi, B. C. Jacobson, M. G. Müller, E. E. Sheets, K. Badizadegan, D. L. Carr-Locke, C. P. Crum, C. W. Boone, R. R. Dasari, J. Van Dam, and M. S. Feld, “NAD(P)H and collagen as in vivo quantitative fluorescent biomarkers of epithelial precancerous changes,” Cancer Res.62(3), 682–687 (2002).
[PubMed]

Carter, S. L.

A. L. Maas, S. L. Carter, E. P. Wileyto, J. Miller, M. Yuan, G. Yu, A. C. Durham, and T. M. Busch, “Tumor vascular microenvironment determines responsiveness to photodynamic therapy,” Cancer Res.72(8), 2079–2088 (2012).
[CrossRef] [PubMed]

Castner, E. W.

D. S. English, K. Das, K. D. Ashby, J. Park, J. W. Petrich, and E. W. Castner, “Confirmation of excited-state proton transfer and ground-state heterogeneity in hypericin by fluorescence upconversion,” J. Am. Chem. Soc.119(48), 11585–11590 (1997).
[CrossRef]

Chaika, N.

Y. Shintani, M. Maeda, N. Chaika, K. R. Johnson, and M. J. Wheelock, “Collagen I promotes epithelial-to-mesenchymal transition in lung cancer cells via transforming growth factor-β signaling,” Am. J. Respir. Cell Mol. Biol.38(1), 95–104 (2008).
[CrossRef] [PubMed]

Chen, G. N.

T. Lv, Z. F. Huang, H. W. Wang, J. Q. Lin, G. N. Chen, X. W. Chen, R. Chen, Z. Huang, and X. L. Wang, “Evaluation of collagen alteration after topical photodynamic therapy (PDT) using second harmonic generation (SHG) microscopy--in vivo study in a mouse model,” Photodiagn. Photodyn. Ther.9(2), 164–169 (2012).
[CrossRef] [PubMed]

Chen, R.

T. Lv, Z. F. Huang, H. W. Wang, J. Q. Lin, G. N. Chen, X. W. Chen, R. Chen, Z. Huang, and X. L. Wang, “Evaluation of collagen alteration after topical photodynamic therapy (PDT) using second harmonic generation (SHG) microscopy--in vivo study in a mouse model,” Photodiagn. Photodyn. Ther.9(2), 164–169 (2012).
[CrossRef] [PubMed]

Chen, S. J.

Chen, T. C.

W. T. Couldwell, A. A. Surnock, A. J. Tobia, B. E. Cabana, C. B. Stillerman, P. A. Forsyth, A. J. Appley, A. M. Spence, D. R. Hinton, and T. C. Chen, “A phase 1/2 study of orally administered synthetic hypericin for treatment of recurrent malignant gliomas,” Cancer117(21), 4905–4915 (2011).
[CrossRef] [PubMed]

Chen, X. W.

T. Lv, Z. F. Huang, H. W. Wang, J. Q. Lin, G. N. Chen, X. W. Chen, R. Chen, Z. Huang, and X. L. Wang, “Evaluation of collagen alteration after topical photodynamic therapy (PDT) using second harmonic generation (SHG) microscopy--in vivo study in a mouse model,” Photodiagn. Photodyn. Ther.9(2), 164–169 (2012).
[CrossRef] [PubMed]

Couldwell, W. T.

W. T. Couldwell, A. A. Surnock, A. J. Tobia, B. E. Cabana, C. B. Stillerman, P. A. Forsyth, A. J. Appley, A. M. Spence, D. R. Hinton, and T. C. Chen, “A phase 1/2 study of orally administered synthetic hypericin for treatment of recurrent malignant gliomas,” Cancer117(21), 4905–4915 (2011).
[CrossRef] [PubMed]

Crum, C. P.

I. Georgakoudi, B. C. Jacobson, M. G. Müller, E. E. Sheets, K. Badizadegan, D. L. Carr-Locke, C. P. Crum, C. W. Boone, R. R. Dasari, J. Van Dam, and M. S. Feld, “NAD(P)H and collagen as in vivo quantitative fluorescent biomarkers of epithelial precancerous changes,” Cancer Res.62(3), 682–687 (2002).
[PubMed]

Dai, R.

T. A. Wells, A. Losi, R. Dai, P. Scott, S. M. Park, J. Golbeck, and P. S. Song, “Electron transfer quenching and photoinduced EPR of hypericin and the ciliate photoreceptor stentorian,” J. Phys. Chem. A101(4), 366–372 (1997).
[CrossRef]

Das, K.

D. S. English, K. Das, K. D. Ashby, J. Park, J. W. Petrich, and E. W. Castner, “Confirmation of excited-state proton transfer and ground-state heterogeneity in hypericin by fluorescence upconversion,” J. Am. Chem. Soc.119(48), 11585–11590 (1997).
[CrossRef]

Dasari, R. R.

I. Georgakoudi, B. C. Jacobson, M. G. Müller, E. E. Sheets, K. Badizadegan, D. L. Carr-Locke, C. P. Crum, C. W. Boone, R. R. Dasari, J. Van Dam, and M. S. Feld, “NAD(P)H and collagen as in vivo quantitative fluorescent biomarkers of epithelial precancerous changes,” Cancer Res.62(3), 682–687 (2002).
[PubMed]

Davids, L. M.

L. M. Davids, B. Kleemann, D. Kacerovská, K. Pizinger, and S. H. Kidson, “Hypericin phototoxicity induces different modes of cell death in melanoma and human skin cells,” J. Photochem. Photobiol. B91(2-3), 67–76 (2008).
[CrossRef] [PubMed]

Dong, C. Y.

Dong, C.-Y.

V. A. Hovhannisyan, P. J. Su, S. J. Lin, and C.-Y. Dong, “Quantifying thermodynamics of collagen thermal denaturation by second harmonic generation imaging,” Appl. Phys. Lett.94(23), 233902 (2009).
[CrossRef]

Durham, A. C.

A. L. Maas, S. L. Carter, E. P. Wileyto, J. Miller, M. Yuan, G. Yu, A. C. Durham, and T. M. Busch, “Tumor vascular microenvironment determines responsiveness to photodynamic therapy,” Cancer Res.72(8), 2079–2088 (2012).
[CrossRef] [PubMed]

Ebermann, R.

H. Koren, G. M. Schenk, R. H. Jindra, G. Alth, R. Ebermann, A. Kubin, G. Koderhold, and M. Kreitner, “Hypericin in phototherapy,” J. Photochem. Photobiol. B36(2), 113–119 (1996).
[CrossRef] [PubMed]

English, D. S.

D. S. English, K. Das, K. D. Ashby, J. Park, J. W. Petrich, and E. W. Castner, “Confirmation of excited-state proton transfer and ground-state heterogeneity in hypericin by fluorescence upconversion,” J. Am. Chem. Soc.119(48), 11585–11590 (1997).
[CrossRef]

Feld, M. S.

I. Georgakoudi, B. C. Jacobson, M. G. Müller, E. E. Sheets, K. Badizadegan, D. L. Carr-Locke, C. P. Crum, C. W. Boone, R. R. Dasari, J. Van Dam, and M. S. Feld, “NAD(P)H and collagen as in vivo quantitative fluorescent biomarkers of epithelial precancerous changes,” Cancer Res.62(3), 682–687 (2002).
[PubMed]

Fernandez, J. M.

J. M. Fernandez, M. D. Bilgin, and L. I. Grossweiner, “Singlet oxygen generation by photodynamic agents,” J. Photochem. Photobiol. B37(1–2), 131–140 (1997).
[CrossRef]

Fine, S.

Forsyth, P. A.

W. T. Couldwell, A. A. Surnock, A. J. Tobia, B. E. Cabana, C. B. Stillerman, P. A. Forsyth, A. J. Appley, A. M. Spence, D. R. Hinton, and T. C. Chen, “A phase 1/2 study of orally administered synthetic hypericin for treatment of recurrent malignant gliomas,” Cancer117(21), 4905–4915 (2011).
[CrossRef] [PubMed]

Fuchs, J.

G. Seitz, R. Krause, J. Fuchs, H. Heitmann, S. Armeanu, P. Ruck, and S. W. Warmann, “In vitro photodynamic therapy in pediatric epithelial liver tumors promoted by hypericin,” Oncol. Rep.20(5), 1277–1282 (2008).
[PubMed]

Fujimoto, D.

D. Fujimoto, K. Akiba, and N. Nakamura, “Isolation and characterization of a fluorescent material in bovine Achilles tendon collagen,” Biochem. Biophys. Res. Commun.76(4), 1124–1129 (1977).
[CrossRef] [PubMed]

Georgakoudi, I.

I. Georgakoudi, B. C. Jacobson, M. G. Müller, E. E. Sheets, K. Badizadegan, D. L. Carr-Locke, C. P. Crum, C. W. Boone, R. R. Dasari, J. Van Dam, and M. S. Feld, “NAD(P)H and collagen as in vivo quantitative fluorescent biomarkers of epithelial precancerous changes,” Cancer Res.62(3), 682–687 (2002).
[PubMed]

Golbeck, J.

T. A. Wells, A. Losi, R. Dai, P. Scott, S. M. Park, J. Golbeck, and P. S. Song, “Electron transfer quenching and photoinduced EPR of hypericin and the ciliate photoreceptor stentorian,” J. Phys. Chem. A101(4), 366–372 (1997).
[CrossRef]

Grossweiner, L. I.

J. M. Fernandez, M. D. Bilgin, and L. I. Grossweiner, “Singlet oxygen generation by photodynamic agents,” J. Photochem. Photobiol. B37(1–2), 131–140 (1997).
[CrossRef]

Gualda, E. J.

Hansen, W. P.

Hayashi, T.

T. Hayashi, “Time-dependent increase in the stability of collagen fibrils formed in vitro. I. Effects of pH and salt concentration on the dissolution of the fibrils,” J. Biochem.84(2), 245–249 (1978).
[PubMed]

Heitmann, H.

G. Seitz, R. Krause, J. Fuchs, H. Heitmann, S. Armeanu, P. Ruck, and S. W. Warmann, “In vitro photodynamic therapy in pediatric epithelial liver tumors promoted by hypericin,” Oncol. Rep.20(5), 1277–1282 (2008).
[PubMed]

Hernández-Toro, J.

Hinton, D. R.

W. T. Couldwell, A. A. Surnock, A. J. Tobia, B. E. Cabana, C. B. Stillerman, P. A. Forsyth, A. J. Appley, A. M. Spence, D. R. Hinton, and T. C. Chen, “A phase 1/2 study of orally administered synthetic hypericin for treatment of recurrent malignant gliomas,” Cancer117(21), 4905–4915 (2011).
[CrossRef] [PubMed]

Hovhannisyan, V.

V. Hovhannisyan, W. Lo, C. Hu, S. J. Chen, and C. Y. Dong, “Dynamics of femtosecond laser photo-modification of collagen fibers,” Opt. Express16(11), 7958–7968 (2008).
[CrossRef] [PubMed]

D. Yova, V. Hovhannisyan, and T. Theodossiou, “Photochemical effects and hypericin photosensitized processes in collagen,” J. Biomed. Opt.6(1), 52–57 (2001).
[CrossRef] [PubMed]

Hovhannisyan, V. A.

V. A. Hovhannisyan, P. J. Su, S. J. Lin, and C.-Y. Dong, “Quantifying thermodynamics of collagen thermal denaturation by second harmonic generation imaging,” Appl. Phys. Lett.94(23), 233902 (2009).
[CrossRef]

Hsiao, C. Y.

Hu, C.

Huang, Z.

T. Lv, Z. F. Huang, H. W. Wang, J. Q. Lin, G. N. Chen, X. W. Chen, R. Chen, Z. Huang, and X. L. Wang, “Evaluation of collagen alteration after topical photodynamic therapy (PDT) using second harmonic generation (SHG) microscopy--in vivo study in a mouse model,” Photodiagn. Photodyn. Ther.9(2), 164–169 (2012).
[CrossRef] [PubMed]

Huang, Z. F.

T. Lv, Z. F. Huang, H. W. Wang, J. Q. Lin, G. N. Chen, X. W. Chen, R. Chen, Z. Huang, and X. L. Wang, “Evaluation of collagen alteration after topical photodynamic therapy (PDT) using second harmonic generation (SHG) microscopy--in vivo study in a mouse model,” Photodiagn. Photodyn. Ther.9(2), 164–169 (2012).
[CrossRef] [PubMed]

Jacobson, B. C.

I. Georgakoudi, B. C. Jacobson, M. G. Müller, E. E. Sheets, K. Badizadegan, D. L. Carr-Locke, C. P. Crum, C. W. Boone, R. R. Dasari, J. Van Dam, and M. S. Feld, “NAD(P)H and collagen as in vivo quantitative fluorescent biomarkers of epithelial precancerous changes,” Cancer Res.62(3), 682–687 (2002).
[PubMed]

Jan, G. J.

Jee, S. H.

Jindra, R. H.

H. Koren, G. M. Schenk, R. H. Jindra, G. Alth, R. Ebermann, A. Kubin, G. Koderhold, and M. Kreitner, “Hypericin in phototherapy,” J. Photochem. Photobiol. B36(2), 113–119 (1996).
[CrossRef] [PubMed]

Jo, J. A.

Johnson, K. R.

Y. Shintani, M. Maeda, N. Chaika, K. R. Johnson, and M. J. Wheelock, “Collagen I promotes epithelial-to-mesenchymal transition in lung cancer cells via transforming growth factor-β signaling,” Am. J. Respir. Cell Mol. Biol.38(1), 95–104 (2008).
[CrossRef] [PubMed]

Kacerovská, D.

L. M. Davids, B. Kleemann, D. Kacerovská, K. Pizinger, and S. H. Kidson, “Hypericin phototoxicity induces different modes of cell death in melanoma and human skin cells,” J. Photochem. Photobiol. B91(2-3), 67–76 (2008).
[CrossRef] [PubMed]

Kidson, S. H.

L. M. Davids, B. Kleemann, D. Kacerovská, K. Pizinger, and S. H. Kidson, “Hypericin phototoxicity induces different modes of cell death in melanoma and human skin cells,” J. Photochem. Photobiol. B91(2-3), 67–76 (2008).
[CrossRef] [PubMed]

Kleemann, B.

L. M. Davids, B. Kleemann, D. Kacerovská, K. Pizinger, and S. H. Kidson, “Hypericin phototoxicity induces different modes of cell death in melanoma and human skin cells,” J. Photochem. Photobiol. B91(2-3), 67–76 (2008).
[CrossRef] [PubMed]

Koderhold, G.

H. Koren, G. M. Schenk, R. H. Jindra, G. Alth, R. Ebermann, A. Kubin, G. Koderhold, and M. Kreitner, “Hypericin in phototherapy,” J. Photochem. Photobiol. B36(2), 113–119 (1996).
[CrossRef] [PubMed]

Koren, H.

H. Koren, G. M. Schenk, R. H. Jindra, G. Alth, R. Ebermann, A. Kubin, G. Koderhold, and M. Kreitner, “Hypericin in phototherapy,” J. Photochem. Photobiol. B36(2), 113–119 (1996).
[CrossRef] [PubMed]

Korom, I.

Kraus, G. A.

S. Carpenter and G. A. Kraus, “Photosensitization is required for inactivation of equine infectious anemia virus by hypericin,” Photochem. Photobiol.53(2), 169–174 (1991).
[CrossRef] [PubMed]

Krause, R.

G. Seitz, R. Krause, J. Fuchs, H. Heitmann, S. Armeanu, P. Ruck, and S. W. Warmann, “In vitro photodynamic therapy in pediatric epithelial liver tumors promoted by hypericin,” Oncol. Rep.20(5), 1277–1282 (2008).
[PubMed]

Kreitner, M.

H. Koren, G. M. Schenk, R. H. Jindra, G. Alth, R. Ebermann, A. Kubin, G. Koderhold, and M. Kreitner, “Hypericin in phototherapy,” J. Photochem. Photobiol. B36(2), 113–119 (1996).
[CrossRef] [PubMed]

Krenacs, T.

Kubin, A.

H. Koren, G. M. Schenk, R. H. Jindra, G. Alth, R. Ebermann, A. Kubin, G. Koderhold, and M. Kreitner, “Hypericin in phototherapy,” J. Photochem. Photobiol. B36(2), 113–119 (1996).
[CrossRef] [PubMed]

Lau, T. Y.

Lavie, D.

D. Meruelo, G. Lavie, and D. Lavie, “Therapeutic agents with dramatic antiretroviral activity and little toxicity at effective doses: Aromatic polycyclic diones hypericin and pseudohypericin,” Proc. Natl. Acad. Sci. U.S.A.85(14), 5230–5234 (1988).
[CrossRef] [PubMed]

Lavie, G.

D. Meruelo, G. Lavie, and D. Lavie, “Therapeutic agents with dramatic antiretroviral activity and little toxicity at effective doses: Aromatic polycyclic diones hypericin and pseudohypericin,” Proc. Natl. Acad. Sci. U.S.A.85(14), 5230–5234 (1988).
[CrossRef] [PubMed]

Li, H. X.

W. G. Liu, K. D. Yao, G. C. Wang, and H. X. Li, “Intrinsic fluorescence investigation on the change in conformation of cross-linked gelatin gel during volume phase transition,” Polymer (Guildf.)41(20), 7589–7592 (2000).
[CrossRef]

Lin, J. Q.

T. Lv, Z. F. Huang, H. W. Wang, J. Q. Lin, G. N. Chen, X. W. Chen, R. Chen, Z. Huang, and X. L. Wang, “Evaluation of collagen alteration after topical photodynamic therapy (PDT) using second harmonic generation (SHG) microscopy--in vivo study in a mouse model,” Photodiagn. Photodyn. Ther.9(2), 164–169 (2012).
[CrossRef] [PubMed]

Lin, S. J.

V. A. Hovhannisyan, P. J. Su, S. J. Lin, and C.-Y. Dong, “Quantifying thermodynamics of collagen thermal denaturation by second harmonic generation imaging,” Appl. Phys. Lett.94(23), 233902 (2009).
[CrossRef]

S. J. Lin, C. Y. Hsiao, Y. Sun, W. Lo, W. C. Lin, G. J. Jan, S. H. Jee, and C. Y. Dong, “Monitoring the thermally induced structural transitions of collagen by use of second-harmonic generation microscopy,” Opt. Lett.30(6), 622–624 (2005).
[CrossRef] [PubMed]

Lin, W. C.

Liu, W. G.

W. G. Liu, K. D. Yao, G. C. Wang, and H. X. Li, “Intrinsic fluorescence investigation on the change in conformation of cross-linked gelatin gel during volume phase transition,” Polymer (Guildf.)41(20), 7589–7592 (2000).
[CrossRef]

Lo, W.

Losi, A.

T. A. Wells, A. Losi, R. Dai, P. Scott, S. M. Park, J. Golbeck, and P. S. Song, “Electron transfer quenching and photoinduced EPR of hypericin and the ciliate photoreceptor stentorian,” J. Phys. Chem. A101(4), 366–372 (1997).
[CrossRef]

Lv, T.

T. Lv, Z. F. Huang, H. W. Wang, J. Q. Lin, G. N. Chen, X. W. Chen, R. Chen, Z. Huang, and X. L. Wang, “Evaluation of collagen alteration after topical photodynamic therapy (PDT) using second harmonic generation (SHG) microscopy--in vivo study in a mouse model,” Photodiagn. Photodyn. Ther.9(2), 164–169 (2012).
[CrossRef] [PubMed]

Maas, A. L.

A. L. Maas, S. L. Carter, E. P. Wileyto, J. Miller, M. Yuan, G. Yu, A. C. Durham, and T. M. Busch, “Tumor vascular microenvironment determines responsiveness to photodynamic therapy,” Cancer Res.72(8), 2079–2088 (2012).
[CrossRef] [PubMed]

Maeda, M.

Y. Shintani, M. Maeda, N. Chaika, K. R. Johnson, and M. J. Wheelock, “Collagen I promotes epithelial-to-mesenchymal transition in lung cancer cells via transforming growth factor-β signaling,” Am. J. Respir. Cell Mol. Biol.38(1), 95–104 (2008).
[CrossRef] [PubMed]

Martínez-García, M. C.

Meruelo, D.

D. Meruelo, G. Lavie, and D. Lavie, “Therapeutic agents with dramatic antiretroviral activity and little toxicity at effective doses: Aromatic polycyclic diones hypericin and pseudohypericin,” Proc. Natl. Acad. Sci. U.S.A.85(14), 5230–5234 (1988).
[CrossRef] [PubMed]

Miller, J.

A. L. Maas, S. L. Carter, E. P. Wileyto, J. Miller, M. Yuan, G. Yu, A. C. Durham, and T. M. Busch, “Tumor vascular microenvironment determines responsiveness to photodynamic therapy,” Cancer Res.72(8), 2079–2088 (2012).
[CrossRef] [PubMed]

Miskovsky, B. S. P.

B. S. P. Miskovsky, “Hypericin--a new antiviral and antitumor photosensitizer: mechanism of action and interaction with biological macromolecules,” Curr. Drug Targets3(1), 55–84 (2002).
[CrossRef] [PubMed]

Moreno, P.

Müller, M. G.

I. Georgakoudi, B. C. Jacobson, M. G. Müller, E. E. Sheets, K. Badizadegan, D. L. Carr-Locke, C. P. Crum, C. W. Boone, R. R. Dasari, J. Van Dam, and M. S. Feld, “NAD(P)H and collagen as in vivo quantitative fluorescent biomarkers of epithelial precancerous changes,” Cancer Res.62(3), 682–687 (2002).
[PubMed]

Murray, B. K.

N. D. Weber, B. K. Murray, J. A. North, and S. G. Wood, “The antiviral agent hypericin has in vitro activity against HSV-1 through non-specific association with viral and cellular membranes,” AntiViral Chem. Chemother.5(2), 83–90 (1994).

Nakamura, N.

D. Fujimoto, K. Akiba, and N. Nakamura, “Isolation and characterization of a fluorescent material in bovine Achilles tendon collagen,” Biochem. Biophys. Res. Commun.76(4), 1124–1129 (1977).
[CrossRef] [PubMed]

North, J. A.

N. D. Weber, B. K. Murray, J. A. North, and S. G. Wood, “The antiviral agent hypericin has in vitro activity against HSV-1 through non-specific association with viral and cellular membranes,” AntiViral Chem. Chemother.5(2), 83–90 (1994).

Pande, P.

Park, J.

D. S. English, K. Das, K. D. Ashby, J. Park, J. W. Petrich, and E. W. Castner, “Confirmation of excited-state proton transfer and ground-state heterogeneity in hypericin by fluorescence upconversion,” J. Am. Chem. Soc.119(48), 11585–11590 (1997).
[CrossRef]

Park, S. M.

T. A. Wells, A. Losi, R. Dai, P. Scott, S. M. Park, J. Golbeck, and P. S. Song, “Electron transfer quenching and photoinduced EPR of hypericin and the ciliate photoreceptor stentorian,” J. Phys. Chem. A101(4), 366–372 (1997).
[CrossRef]

Petrich, J. W.

D. S. English, K. Das, K. D. Ashby, J. Park, J. W. Petrich, and E. W. Castner, “Confirmation of excited-state proton transfer and ground-state heterogeneity in hypericin by fluorescence upconversion,” J. Am. Chem. Soc.119(48), 11585–11590 (1997).
[CrossRef]

Pizinger, K.

L. M. Davids, B. Kleemann, D. Kacerovská, K. Pizinger, and S. H. Kidson, “Hypericin phototoxicity induces different modes of cell death in melanoma and human skin cells,” J. Photochem. Photobiol. B91(2-3), 67–76 (2008).
[CrossRef] [PubMed]

Roso, L.

Ruck, P.

G. Seitz, R. Krause, J. Fuchs, H. Heitmann, S. Armeanu, P. Ruck, and S. W. Warmann, “In vitro photodynamic therapy in pediatric epithelial liver tumors promoted by hypericin,” Oncol. Rep.20(5), 1277–1282 (2008).
[PubMed]

Schenk, G. M.

H. Koren, G. M. Schenk, R. H. Jindra, G. Alth, R. Ebermann, A. Kubin, G. Koderhold, and M. Kreitner, “Hypericin in phototherapy,” J. Photochem. Photobiol. B36(2), 113–119 (1996).
[CrossRef] [PubMed]

Scott, P.

T. A. Wells, A. Losi, R. Dai, P. Scott, S. M. Park, J. Golbeck, and P. S. Song, “Electron transfer quenching and photoinduced EPR of hypericin and the ciliate photoreceptor stentorian,” J. Phys. Chem. A101(4), 366–372 (1997).
[CrossRef]

Seitz, G.

G. Seitz, R. Krause, J. Fuchs, H. Heitmann, S. Armeanu, P. Ruck, and S. W. Warmann, “In vitro photodynamic therapy in pediatric epithelial liver tumors promoted by hypericin,” Oncol. Rep.20(5), 1277–1282 (2008).
[PubMed]

Sheets, E. E.

I. Georgakoudi, B. C. Jacobson, M. G. Müller, E. E. Sheets, K. Badizadegan, D. L. Carr-Locke, C. P. Crum, C. W. Boone, R. R. Dasari, J. Van Dam, and M. S. Feld, “NAD(P)H and collagen as in vivo quantitative fluorescent biomarkers of epithelial precancerous changes,” Cancer Res.62(3), 682–687 (2002).
[PubMed]

Shintani, Y.

Y. Shintani, M. Maeda, N. Chaika, K. R. Johnson, and M. J. Wheelock, “Collagen I promotes epithelial-to-mesenchymal transition in lung cancer cells via transforming growth factor-β signaling,” Am. J. Respir. Cell Mol. Biol.38(1), 95–104 (2008).
[CrossRef] [PubMed]

Song, P. S.

T. A. Wells, A. Losi, R. Dai, P. Scott, S. M. Park, J. Golbeck, and P. S. Song, “Electron transfer quenching and photoinduced EPR of hypericin and the ciliate photoreceptor stentorian,” J. Phys. Chem. A101(4), 366–372 (1997).
[CrossRef]

Spence, A. M.

W. T. Couldwell, A. A. Surnock, A. J. Tobia, B. E. Cabana, C. B. Stillerman, P. A. Forsyth, A. J. Appley, A. M. Spence, D. R. Hinton, and T. C. Chen, “A phase 1/2 study of orally administered synthetic hypericin for treatment of recurrent malignant gliomas,” Cancer117(21), 4905–4915 (2011).
[CrossRef] [PubMed]

Stillerman, C. B.

W. T. Couldwell, A. A. Surnock, A. J. Tobia, B. E. Cabana, C. B. Stillerman, P. A. Forsyth, A. J. Appley, A. M. Spence, D. R. Hinton, and T. C. Chen, “A phase 1/2 study of orally administered synthetic hypericin for treatment of recurrent malignant gliomas,” Cancer117(21), 4905–4915 (2011).
[CrossRef] [PubMed]

Su, P. J.

V. A. Hovhannisyan, P. J. Su, S. J. Lin, and C.-Y. Dong, “Quantifying thermodynamics of collagen thermal denaturation by second harmonic generation imaging,” Appl. Phys. Lett.94(23), 233902 (2009).
[CrossRef]

Sun, Y.

Surnock, A. A.

W. T. Couldwell, A. A. Surnock, A. J. Tobia, B. E. Cabana, C. B. Stillerman, P. A. Forsyth, A. J. Appley, A. M. Spence, D. R. Hinton, and T. C. Chen, “A phase 1/2 study of orally administered synthetic hypericin for treatment of recurrent malignant gliomas,” Cancer117(21), 4905–4915 (2011).
[CrossRef] [PubMed]

Theodossiou, T.

D. Yova, V. Hovhannisyan, and T. Theodossiou, “Photochemical effects and hypericin photosensitized processes in collagen,” J. Biomed. Opt.6(1), 52–57 (2001).
[CrossRef] [PubMed]

Thrasivoulou, C.

Tobia, A. J.

W. T. Couldwell, A. A. Surnock, A. J. Tobia, B. E. Cabana, C. B. Stillerman, P. A. Forsyth, A. J. Appley, A. M. Spence, D. R. Hinton, and T. C. Chen, “A phase 1/2 study of orally administered synthetic hypericin for treatment of recurrent malignant gliomas,” Cancer117(21), 4905–4915 (2011).
[CrossRef] [PubMed]

Toussaint, K. C.

Van Dam, J.

I. Georgakoudi, B. C. Jacobson, M. G. Müller, E. E. Sheets, K. Badizadegan, D. L. Carr-Locke, C. P. Crum, C. W. Boone, R. R. Dasari, J. Van Dam, and M. S. Feld, “NAD(P)H and collagen as in vivo quantitative fluorescent biomarkers of epithelial precancerous changes,” Cancer Res.62(3), 682–687 (2002).
[PubMed]

Vázquez de Aldana, J. R.

Virich, G.

Walsh, M.

Wang, G. C.

W. G. Liu, K. D. Yao, G. C. Wang, and H. X. Li, “Intrinsic fluorescence investigation on the change in conformation of cross-linked gelatin gel during volume phase transition,” Polymer (Guildf.)41(20), 7589–7592 (2000).
[CrossRef]

Wang, H. W.

T. Lv, Z. F. Huang, H. W. Wang, J. Q. Lin, G. N. Chen, X. W. Chen, R. Chen, Z. Huang, and X. L. Wang, “Evaluation of collagen alteration after topical photodynamic therapy (PDT) using second harmonic generation (SHG) microscopy--in vivo study in a mouse model,” Photodiagn. Photodyn. Ther.9(2), 164–169 (2012).
[CrossRef] [PubMed]

Wang, X. L.

T. Lv, Z. F. Huang, H. W. Wang, J. Q. Lin, G. N. Chen, X. W. Chen, R. Chen, Z. Huang, and X. L. Wang, “Evaluation of collagen alteration after topical photodynamic therapy (PDT) using second harmonic generation (SHG) microscopy--in vivo study in a mouse model,” Photodiagn. Photodyn. Ther.9(2), 164–169 (2012).
[CrossRef] [PubMed]

Warmann, S. W.

G. Seitz, R. Krause, J. Fuchs, H. Heitmann, S. Armeanu, P. Ruck, and S. W. Warmann, “In vitro photodynamic therapy in pediatric epithelial liver tumors promoted by hypericin,” Oncol. Rep.20(5), 1277–1282 (2008).
[PubMed]

Weber, N. D.

N. D. Weber, B. K. Murray, J. A. North, and S. G. Wood, “The antiviral agent hypericin has in vitro activity against HSV-1 through non-specific association with viral and cellular membranes,” AntiViral Chem. Chemother.5(2), 83–90 (1994).

Wells, T. A.

T. A. Wells, A. Losi, R. Dai, P. Scott, S. M. Park, J. Golbeck, and P. S. Song, “Electron transfer quenching and photoinduced EPR of hypericin and the ciliate photoreceptor stentorian,” J. Phys. Chem. A101(4), 366–372 (1997).
[CrossRef]

Wheelock, M. J.

Y. Shintani, M. Maeda, N. Chaika, K. R. Johnson, and M. J. Wheelock, “Collagen I promotes epithelial-to-mesenchymal transition in lung cancer cells via transforming growth factor-β signaling,” Am. J. Respir. Cell Mol. Biol.38(1), 95–104 (2008).
[CrossRef] [PubMed]

Wileyto, E. P.

A. L. Maas, S. L. Carter, E. P. Wileyto, J. Miller, M. Yuan, G. Yu, A. C. Durham, and T. M. Busch, “Tumor vascular microenvironment determines responsiveness to photodynamic therapy,” Cancer Res.72(8), 2079–2088 (2012).
[CrossRef] [PubMed]

Wood, S. G.

N. D. Weber, B. K. Murray, J. A. North, and S. G. Wood, “The antiviral agent hypericin has in vitro activity against HSV-1 through non-specific association with viral and cellular membranes,” AntiViral Chem. Chemother.5(2), 83–90 (1994).

Yao, K. D.

W. G. Liu, K. D. Yao, G. C. Wang, and H. X. Li, “Intrinsic fluorescence investigation on the change in conformation of cross-linked gelatin gel during volume phase transition,” Polymer (Guildf.)41(20), 7589–7592 (2000).
[CrossRef]

Yova, D.

D. Yova, V. Hovhannisyan, and T. Theodossiou, “Photochemical effects and hypericin photosensitized processes in collagen,” J. Biomed. Opt.6(1), 52–57 (2001).
[CrossRef] [PubMed]

Yu, G.

A. L. Maas, S. L. Carter, E. P. Wileyto, J. Miller, M. Yuan, G. Yu, A. C. Durham, and T. M. Busch, “Tumor vascular microenvironment determines responsiveness to photodynamic therapy,” Cancer Res.72(8), 2079–2088 (2012).
[CrossRef] [PubMed]

Yuan, M.

A. L. Maas, S. L. Carter, E. P. Wileyto, J. Miller, M. Yuan, G. Yu, A. C. Durham, and T. M. Busch, “Tumor vascular microenvironment determines responsiveness to photodynamic therapy,” Cancer Res.72(8), 2079–2088 (2012).
[CrossRef] [PubMed]

Am. J. Respir. Cell Mol. Biol. (1)

Y. Shintani, M. Maeda, N. Chaika, K. R. Johnson, and M. J. Wheelock, “Collagen I promotes epithelial-to-mesenchymal transition in lung cancer cells via transforming growth factor-β signaling,” Am. J. Respir. Cell Mol. Biol.38(1), 95–104 (2008).
[CrossRef] [PubMed]

AntiViral Chem. Chemother. (1)

N. D. Weber, B. K. Murray, J. A. North, and S. G. Wood, “The antiviral agent hypericin has in vitro activity against HSV-1 through non-specific association with viral and cellular membranes,” AntiViral Chem. Chemother.5(2), 83–90 (1994).

Appl. Opt. (1)

Appl. Phys. Lett. (1)

V. A. Hovhannisyan, P. J. Su, S. J. Lin, and C.-Y. Dong, “Quantifying thermodynamics of collagen thermal denaturation by second harmonic generation imaging,” Appl. Phys. Lett.94(23), 233902 (2009).
[CrossRef]

Biochem. Biophys. Res. Commun. (1)

D. Fujimoto, K. Akiba, and N. Nakamura, “Isolation and characterization of a fluorescent material in bovine Achilles tendon collagen,” Biochem. Biophys. Res. Commun.76(4), 1124–1129 (1977).
[CrossRef] [PubMed]

Biomed. Opt. Express (4)

Cancer (1)

W. T. Couldwell, A. A. Surnock, A. J. Tobia, B. E. Cabana, C. B. Stillerman, P. A. Forsyth, A. J. Appley, A. M. Spence, D. R. Hinton, and T. C. Chen, “A phase 1/2 study of orally administered synthetic hypericin for treatment of recurrent malignant gliomas,” Cancer117(21), 4905–4915 (2011).
[CrossRef] [PubMed]

Cancer Res. (2)

I. Georgakoudi, B. C. Jacobson, M. G. Müller, E. E. Sheets, K. Badizadegan, D. L. Carr-Locke, C. P. Crum, C. W. Boone, R. R. Dasari, J. Van Dam, and M. S. Feld, “NAD(P)H and collagen as in vivo quantitative fluorescent biomarkers of epithelial precancerous changes,” Cancer Res.62(3), 682–687 (2002).
[PubMed]

A. L. Maas, S. L. Carter, E. P. Wileyto, J. Miller, M. Yuan, G. Yu, A. C. Durham, and T. M. Busch, “Tumor vascular microenvironment determines responsiveness to photodynamic therapy,” Cancer Res.72(8), 2079–2088 (2012).
[CrossRef] [PubMed]

Curr. Drug Targets (1)

B. S. P. Miskovsky, “Hypericin--a new antiviral and antitumor photosensitizer: mechanism of action and interaction with biological macromolecules,” Curr. Drug Targets3(1), 55–84 (2002).
[CrossRef] [PubMed]

J. Am. Chem. Soc. (1)

D. S. English, K. Das, K. D. Ashby, J. Park, J. W. Petrich, and E. W. Castner, “Confirmation of excited-state proton transfer and ground-state heterogeneity in hypericin by fluorescence upconversion,” J. Am. Chem. Soc.119(48), 11585–11590 (1997).
[CrossRef]

J. Biochem. (1)

T. Hayashi, “Time-dependent increase in the stability of collagen fibrils formed in vitro. I. Effects of pH and salt concentration on the dissolution of the fibrils,” J. Biochem.84(2), 245–249 (1978).
[PubMed]

J. Biomed. Opt. (1)

D. Yova, V. Hovhannisyan, and T. Theodossiou, “Photochemical effects and hypericin photosensitized processes in collagen,” J. Biomed. Opt.6(1), 52–57 (2001).
[CrossRef] [PubMed]

J. Photochem. Photobiol. B (3)

H. Koren, G. M. Schenk, R. H. Jindra, G. Alth, R. Ebermann, A. Kubin, G. Koderhold, and M. Kreitner, “Hypericin in phototherapy,” J. Photochem. Photobiol. B36(2), 113–119 (1996).
[CrossRef] [PubMed]

L. M. Davids, B. Kleemann, D. Kacerovská, K. Pizinger, and S. H. Kidson, “Hypericin phototoxicity induces different modes of cell death in melanoma and human skin cells,” J. Photochem. Photobiol. B91(2-3), 67–76 (2008).
[CrossRef] [PubMed]

J. M. Fernandez, M. D. Bilgin, and L. I. Grossweiner, “Singlet oxygen generation by photodynamic agents,” J. Photochem. Photobiol. B37(1–2), 131–140 (1997).
[CrossRef]

J. Phys. Chem. A (1)

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Oncol. Rep. (1)

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Figures (5)

Fig. 1
Fig. 1

Experimental setup for spectrofluorimetric measurement of laser-induced photoprocesses.

Fig. 2
Fig. 2

Fluorescence spectra of BAT (a) and gelatin (b) before and after Hyp sensitization and UV (337 nm) or green (532 nm) laser irradiation. Samples were illuminated for 15 min at the intensity of 15 mW/cm2. Excitation of the samples was carried out at 337 nm and intensity of 0.5 mW/cm2.

Fig. 3
Fig. 3

Fluorescence spectra of chicken tendon, before and after 8μM Hyp sensitization and UV (337 nm) illumination. The sample was illuminated at the intensity of 15 mW/cm2 for 30 minutes. Excitation was carried out at 337 nm at the intensity of 0.5 mW/cm2.

Fig. 4
Fig. 4

(a) Multiphoton images of Hyp-sensitized BAT acquired with a 20 × /NA 0.5 objective at different time points of halogen lamp illumination. Red pseudocolor is the SHG from collagen fibers, green pseudocolor represents the TPEF signal from Hyp and collagen autofluorescence (spectral range of 435-700 nm). (b) Dynamics of TPEF (series 2) and SHG (series 4) intensities in ROI 2 localized within collagen fibers during the irradiation of Hyp-sensitized BAT with a halogen lamp. Series 1 and 3 show the dynamics of the fluorescence in the range of 435-700 nm measured from outside of the collagen fibers (ROIs 1 and 3, respectively). Arrow indicates the starting point of the light illumination.

Fig. 5
Fig. 5

TPEF (green) and SHG (red) imaging of Hyp-induced destruction of CLT acquired with 20x/NA 0.5 objective. (a), (b): Native collagen fibers after 40 min treatment with EtOH(75%)–PBS. Same samples after 60 min treatment with 10 μM (c) and 20 μM (d) of Hyp in EtOH(75%)–PBS solutions. Dynamics of SHG and TPEF intensities during collagen treatment with 20 μM Hyp-EtOH(75%)–PBS solution, and EtOH–PBS solvent is shown in (e).

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