Abstract

Photodynamic therapy (PDT) dosimetry is complex as many factors are involved and varied interdependently. Monitoring the biological consequence of PDT such as cell death is the most direct approach to assess treatment efficacy. In this study, we performed 5-aminolevlinic acid (ALA)-PDT in vitro to induce different cell death modes (i.e., slight cell cytotoxicity, apoptosis, and necrosis) by a fixed fluence rate of 10 mW/cm2 and varied fluences (1, 2, and 6 J/cm2). Time course measurements of cell viability, caspase-3 activity, and DNA fragmentation were conducted to determine the mode of cell death. We demonstrated that NADH fluorescence lifetime together with NADH fluorescence intensity permit us to detect apoptosis and differentiate it from necrosis. This feature will be unique in the use of optimizing apoptosis-favored treatments such as metronomic PDT.

© 2011 OSA

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  1. D. E. Dolmans, D. Fukumura, and R. K. Jain, “Photodynamic therapy for cancer,” Nat. Rev. Cancer 3(5), 380–387 (2003).
    [CrossRef] [PubMed]
  2. B. C. Wilson, M. S. Patterson, and L. Lilge, “Implicit and explicit dosimetry in photodynamic therapy: a New paradigm,” Lasers Med. Sci. 12(3), 182–199 (1997).
    [CrossRef] [PubMed]
  3. K. K.-H. Wang, S. Mitra, and T. H. Foster, “A comprehensive mathematical model of microscopic dose deposition in photodynamic therapy,” Med. Phys. 34(1), 282–293 (2007).
    [CrossRef] [PubMed]
  4. M. T. Jarvi, M. J. Niedre, M. S. Patterson, and B. C. Wilson, “Singlet oxygen luminescence dosimetry (SOLD) for photodynamic therapy: current status, challenges and future prospects,” Photochem. Photobiol. 82(5), 1198–1210 (2006).
    [CrossRef] [PubMed]
  5. M. J. Niedre, A. J. Secord, M. S. Patterson, and B. C. Wilson, “In vitro tests of the validity of singlet oxygen luminescence measurements as a dose metric in photodynamic therapy,” Cancer Res. 63(22), 7986–7994 (2003).
    [PubMed]
  6. K. K. Wang, S. Mitra, and T. H. Foster, “Photodynamic dose does not correlate with long-term tumor response to mTHPC-PDT performed at several drug-light intervals,” Med. Phys. 35(8), 3518–3526 (2008).
    [CrossRef] [PubMed]
  7. S. Gross, A. Gilead, A. Scherz, M. Neeman, and Y. Salomon, “Monitoring photodynamic therapy of solid tumors online by BOLD-contrast MRI,” Nat. Med. 9(10), 1327–1331 (2003).
    [CrossRef] [PubMed]
  8. J. C. Finlay and T. H. Foster, “Hemoglobin oxygen saturations in phantoms and in vivo from measurements of steady-state diffuse reflectance at a single, short source-detector separation,” Med. Phys. 31(7), 1949–1959 (2004).
    [CrossRef] [PubMed]
  9. A. A. Stratonnikov and V. B. Loschenov, “Evaluation of blood oxygen saturation in vivo from diffuse reflectance spectra,” J. Biomed. Opt. 6(4), 457–467 (2001).
    [CrossRef] [PubMed]
  10. G. Yu, T. Durduran, C. Zhou, H. W. Wang, M. E. Putt, H. M. Saunders, C. M. Sehgal, E. Glatstein, A. G. Yodh, and T. M. Busch, “Noninvasive monitoring of murine tumor blood flow during and after photodynamic therapy provides early assessment of therapeutic efficacy,” Clin. Cancer Res. 11(9), 3543–3552 (2005).
    [CrossRef] [PubMed]
  11. B. Chen, B. W. Pogue, I. A. Goodwin, J. A. O’Hara, C. M. Wilmot, J. E. Hutchins, P. J. Hoopes, and T. Hasan, “Blood flow dynamics after photodynamic therapy with verteporfin in the RIF-1 tumor,” Radiat. Res. 160(4), 452–459 (2003).
    [CrossRef] [PubMed]
  12. S. K. Bisland, L. Lilge, A. Lin, R. Rusnov, and B. C. Wilson, “Metronomic photodynamic therapy as a new paradigm for photodynamic therapy: rationale and preclinical evaluation of technical feasibility for treating malignant brain tumors,” Photochem. Photobiol. 80(1), 22–30 (2004).
    [CrossRef] [PubMed]
  13. A. Bogaards, A. Varma, K. Zhang, D. Zach, S. K. Bisland, E. H. Moriyama, L. Lilge, P. J. Muller, and B. C. Wilson, “Fluorescence image-guided brain tumour resection with adjuvant metronomic photodynamic therapy: pre-clinical model and technology development,” Photochem. Photobiol. Sci. 4(5), 438–442 (2005).
    [CrossRef] [PubMed]
  14. B. W. Henderson, T. M. Busch, and J. W. Snyder, “Fluence rate as a modulator of PDT mechanisms,” Lasers Surg. Med. 38(5), 489–493 (2006).
    [CrossRef] [PubMed]
  15. B. W. Henderson, S. O. Gollnick, J. W. Snyder, T. M. Busch, P. C. Kousis, R. T. Cheney, and J. Morgan, “Choice of oxygen-conserving treatment regimen determines the inflammatory response and outcome of photodynamic therapy of tumors,” Cancer Res. 64(6), 2120–2126 (2004).
    [CrossRef] [PubMed]
  16. D. K. Bird, L. Yan, K. M. Vrotsos, K. W. Eliceiri, E. M. Vaughan, P. J. Keely, J. G. White, and N. Ramanujam, “Metabolic mapping of MCF10A human breast cells via multiphoton fluorescence lifetime imaging of the coenzyme NADH,” Cancer Res. 65(19), 8766–8773 (2005).
    [CrossRef] [PubMed]
  17. M. C. Skala, K. M. Riching, A. Gendron-Fitzpatrick, J. Eickhoff, K. W. Eliceiri, J. G. White, and N. Ramanujam, “In vivo multiphoton microscopy of NADH and FAD redox states, fluorescence lifetimes, and cellular morphology in precancerous epithelia,” Proc. Natl. Acad. Sci. U.S.A. 104(49), 19494–19499 (2007).
    [CrossRef] [PubMed]
  18. H. W. Wang, Y. H. Wei, and H. W. Guo, “Reduced nicotinamide adenine dinucleotide (NADH) fluorescence for the detection of cell death,” Anticancer. Agents Med. Chem. 9(9), 1012–1017 (2009).
    [PubMed]
  19. H. W. Wang, V. Gukassyan, C. T. Chen, Y. H. Wei, H. W. Guo, J. S. Yu, and F. J. Kao, “Differentiation of apoptosis from necrosis by dynamic changes of reduced nicotinamide adenine dinucleotide fluorescence lifetime in live cells,” J. Biomed. Opt. 13(5), 054011 (2008).
    [CrossRef] [PubMed]
  20. J. S. Yu, H. W. Guo, C. H. Wang, Y. H. Wei, and H. W. Wang, “Increase of reduced nicotinamide adenine dinucleotide fluorescence lifetime precedes mitochondrial dysfunction in staurosporine-induced apoptosis of HeLa cells,” J. Biomed. Opt. 16(3), 036008 (2011).
    [CrossRef] [PubMed]
  21. H. W. Guo, Y. H. Wei, and H. W. Wang, “Reduced nicotinamide adenine dinucleotide fluorescence lifetime detected poly(adenosine-5?-diphosphate-ribose) polymerase-1-mediated cell death and therapeutic effect of pyruvate,” J. Biomed. Opt. 16(6), 068001 (2011).
    [CrossRef] [PubMed]
  22. D. Grebe?ová, K. Kuželová, K. Smetana, M. Pluskalová, H. Cajthamlová, I. Marinov, O. Fuchs, J. Sou?ek, P. Jarolím, and Z. Hrkal, “Mitochondrial and endoplasmic reticulum stress-induced apoptotic pathways are activated by 5-aminolevulinic acid-based photodynamic therapy in HL60 leukemia cells,” J. Photochem. Photobiol. B 69(2), 71–85 (2003).
    [CrossRef] [PubMed]
  23. N. L. Oleinick, R. L. Morris, and I. Belichenko, “The role of apoptosis in response to photodynamic therapy: what, where, why, and how,” Photochem. Photobiol. Sci. 1(1), 1–21 (2002).
    [CrossRef] [PubMed]
  24. F. Giuntini, L. Bourré, A. J. MacRobert, M. Wilson, and I. M. Eggleston, “Improved peptide prodrugs of 5-ALA for PDT: rationalization of cellular accumulation and protoporphyrin IX production by direct determination of cellular prodrug uptake and prodrug metabolization,” J. Med. Chem. 52(13), 4026–4037 (2009).
    [CrossRef] [PubMed]
  25. B. W. Pogue, J. D. Pitts, M. A. Mycek, R. D. Sloboda, C. M. Wilmot, J. F. Brandsema, and J. A. O’Hara, “In vivo NADH fluorescence monitoring as an assay for cellular damage in photodynamic therapy,” Photochem. Photobiol. 74(6), 817–824 (2001).
    [CrossRef] [PubMed]
  26. H. W. Guo, C. T. Chen, Y. H. Wei, O. K. Lee, V. Gukassyan, F. J. Kao, and H. W. Wang, “Reduced nicotinamide adenine dinucleotide fluorescence lifetime separates human mesenchymal stem cells from differentiated progenies,” J. Biomed. Opt. 13(5), 050505 (2008).
    [CrossRef] [PubMed]
  27. H. Okada and T. W. Mak, “Pathways of apoptotic and non-apoptotic death in tumour cells,” Nat. Rev. Cancer 4(8), 592–603 (2004).
    [CrossRef] [PubMed]
  28. S. Elmore, “Apoptosis: a review of programmed cell death,” Toxicol. Pathol. 35(4), 495–516 (2007).
    [CrossRef] [PubMed]

2011

J. S. Yu, H. W. Guo, C. H. Wang, Y. H. Wei, and H. W. Wang, “Increase of reduced nicotinamide adenine dinucleotide fluorescence lifetime precedes mitochondrial dysfunction in staurosporine-induced apoptosis of HeLa cells,” J. Biomed. Opt. 16(3), 036008 (2011).
[CrossRef] [PubMed]

H. W. Guo, Y. H. Wei, and H. W. Wang, “Reduced nicotinamide adenine dinucleotide fluorescence lifetime detected poly(adenosine-5?-diphosphate-ribose) polymerase-1-mediated cell death and therapeutic effect of pyruvate,” J. Biomed. Opt. 16(6), 068001 (2011).
[CrossRef] [PubMed]

2009

H. W. Wang, Y. H. Wei, and H. W. Guo, “Reduced nicotinamide adenine dinucleotide (NADH) fluorescence for the detection of cell death,” Anticancer. Agents Med. Chem. 9(9), 1012–1017 (2009).
[PubMed]

F. Giuntini, L. Bourré, A. J. MacRobert, M. Wilson, and I. M. Eggleston, “Improved peptide prodrugs of 5-ALA for PDT: rationalization of cellular accumulation and protoporphyrin IX production by direct determination of cellular prodrug uptake and prodrug metabolization,” J. Med. Chem. 52(13), 4026–4037 (2009).
[CrossRef] [PubMed]

2008

H. W. Wang, V. Gukassyan, C. T. Chen, Y. H. Wei, H. W. Guo, J. S. Yu, and F. J. Kao, “Differentiation of apoptosis from necrosis by dynamic changes of reduced nicotinamide adenine dinucleotide fluorescence lifetime in live cells,” J. Biomed. Opt. 13(5), 054011 (2008).
[CrossRef] [PubMed]

H. W. Guo, C. T. Chen, Y. H. Wei, O. K. Lee, V. Gukassyan, F. J. Kao, and H. W. Wang, “Reduced nicotinamide adenine dinucleotide fluorescence lifetime separates human mesenchymal stem cells from differentiated progenies,” J. Biomed. Opt. 13(5), 050505 (2008).
[CrossRef] [PubMed]

K. K. Wang, S. Mitra, and T. H. Foster, “Photodynamic dose does not correlate with long-term tumor response to mTHPC-PDT performed at several drug-light intervals,” Med. Phys. 35(8), 3518–3526 (2008).
[CrossRef] [PubMed]

2007

K. K.-H. Wang, S. Mitra, and T. H. Foster, “A comprehensive mathematical model of microscopic dose deposition in photodynamic therapy,” Med. Phys. 34(1), 282–293 (2007).
[CrossRef] [PubMed]

M. C. Skala, K. M. Riching, A. Gendron-Fitzpatrick, J. Eickhoff, K. W. Eliceiri, J. G. White, and N. Ramanujam, “In vivo multiphoton microscopy of NADH and FAD redox states, fluorescence lifetimes, and cellular morphology in precancerous epithelia,” Proc. Natl. Acad. Sci. U.S.A. 104(49), 19494–19499 (2007).
[CrossRef] [PubMed]

S. Elmore, “Apoptosis: a review of programmed cell death,” Toxicol. Pathol. 35(4), 495–516 (2007).
[CrossRef] [PubMed]

2006

B. W. Henderson, T. M. Busch, and J. W. Snyder, “Fluence rate as a modulator of PDT mechanisms,” Lasers Surg. Med. 38(5), 489–493 (2006).
[CrossRef] [PubMed]

M. T. Jarvi, M. J. Niedre, M. S. Patterson, and B. C. Wilson, “Singlet oxygen luminescence dosimetry (SOLD) for photodynamic therapy: current status, challenges and future prospects,” Photochem. Photobiol. 82(5), 1198–1210 (2006).
[CrossRef] [PubMed]

2005

D. K. Bird, L. Yan, K. M. Vrotsos, K. W. Eliceiri, E. M. Vaughan, P. J. Keely, J. G. White, and N. Ramanujam, “Metabolic mapping of MCF10A human breast cells via multiphoton fluorescence lifetime imaging of the coenzyme NADH,” Cancer Res. 65(19), 8766–8773 (2005).
[CrossRef] [PubMed]

G. Yu, T. Durduran, C. Zhou, H. W. Wang, M. E. Putt, H. M. Saunders, C. M. Sehgal, E. Glatstein, A. G. Yodh, and T. M. Busch, “Noninvasive monitoring of murine tumor blood flow during and after photodynamic therapy provides early assessment of therapeutic efficacy,” Clin. Cancer Res. 11(9), 3543–3552 (2005).
[CrossRef] [PubMed]

A. Bogaards, A. Varma, K. Zhang, D. Zach, S. K. Bisland, E. H. Moriyama, L. Lilge, P. J. Muller, and B. C. Wilson, “Fluorescence image-guided brain tumour resection with adjuvant metronomic photodynamic therapy: pre-clinical model and technology development,” Photochem. Photobiol. Sci. 4(5), 438–442 (2005).
[CrossRef] [PubMed]

2004

S. K. Bisland, L. Lilge, A. Lin, R. Rusnov, and B. C. Wilson, “Metronomic photodynamic therapy as a new paradigm for photodynamic therapy: rationale and preclinical evaluation of technical feasibility for treating malignant brain tumors,” Photochem. Photobiol. 80(1), 22–30 (2004).
[CrossRef] [PubMed]

B. W. Henderson, S. O. Gollnick, J. W. Snyder, T. M. Busch, P. C. Kousis, R. T. Cheney, and J. Morgan, “Choice of oxygen-conserving treatment regimen determines the inflammatory response and outcome of photodynamic therapy of tumors,” Cancer Res. 64(6), 2120–2126 (2004).
[CrossRef] [PubMed]

J. C. Finlay and T. H. Foster, “Hemoglobin oxygen saturations in phantoms and in vivo from measurements of steady-state diffuse reflectance at a single, short source-detector separation,” Med. Phys. 31(7), 1949–1959 (2004).
[CrossRef] [PubMed]

H. Okada and T. W. Mak, “Pathways of apoptotic and non-apoptotic death in tumour cells,” Nat. Rev. Cancer 4(8), 592–603 (2004).
[CrossRef] [PubMed]

2003

D. Grebe?ová, K. Kuželová, K. Smetana, M. Pluskalová, H. Cajthamlová, I. Marinov, O. Fuchs, J. Sou?ek, P. Jarolím, and Z. Hrkal, “Mitochondrial and endoplasmic reticulum stress-induced apoptotic pathways are activated by 5-aminolevulinic acid-based photodynamic therapy in HL60 leukemia cells,” J. Photochem. Photobiol. B 69(2), 71–85 (2003).
[CrossRef] [PubMed]

S. Gross, A. Gilead, A. Scherz, M. Neeman, and Y. Salomon, “Monitoring photodynamic therapy of solid tumors online by BOLD-contrast MRI,” Nat. Med. 9(10), 1327–1331 (2003).
[CrossRef] [PubMed]

M. J. Niedre, A. J. Secord, M. S. Patterson, and B. C. Wilson, “In vitro tests of the validity of singlet oxygen luminescence measurements as a dose metric in photodynamic therapy,” Cancer Res. 63(22), 7986–7994 (2003).
[PubMed]

D. E. Dolmans, D. Fukumura, and R. K. Jain, “Photodynamic therapy for cancer,” Nat. Rev. Cancer 3(5), 380–387 (2003).
[CrossRef] [PubMed]

B. Chen, B. W. Pogue, I. A. Goodwin, J. A. O’Hara, C. M. Wilmot, J. E. Hutchins, P. J. Hoopes, and T. Hasan, “Blood flow dynamics after photodynamic therapy with verteporfin in the RIF-1 tumor,” Radiat. Res. 160(4), 452–459 (2003).
[CrossRef] [PubMed]

2002

N. L. Oleinick, R. L. Morris, and I. Belichenko, “The role of apoptosis in response to photodynamic therapy: what, where, why, and how,” Photochem. Photobiol. Sci. 1(1), 1–21 (2002).
[CrossRef] [PubMed]

2001

B. W. Pogue, J. D. Pitts, M. A. Mycek, R. D. Sloboda, C. M. Wilmot, J. F. Brandsema, and J. A. O’Hara, “In vivo NADH fluorescence monitoring as an assay for cellular damage in photodynamic therapy,” Photochem. Photobiol. 74(6), 817–824 (2001).
[CrossRef] [PubMed]

A. A. Stratonnikov and V. B. Loschenov, “Evaluation of blood oxygen saturation in vivo from diffuse reflectance spectra,” J. Biomed. Opt. 6(4), 457–467 (2001).
[CrossRef] [PubMed]

1997

B. C. Wilson, M. S. Patterson, and L. Lilge, “Implicit and explicit dosimetry in photodynamic therapy: a New paradigm,” Lasers Med. Sci. 12(3), 182–199 (1997).
[CrossRef] [PubMed]

Belichenko, I.

N. L. Oleinick, R. L. Morris, and I. Belichenko, “The role of apoptosis in response to photodynamic therapy: what, where, why, and how,” Photochem. Photobiol. Sci. 1(1), 1–21 (2002).
[CrossRef] [PubMed]

Bird, D. K.

D. K. Bird, L. Yan, K. M. Vrotsos, K. W. Eliceiri, E. M. Vaughan, P. J. Keely, J. G. White, and N. Ramanujam, “Metabolic mapping of MCF10A human breast cells via multiphoton fluorescence lifetime imaging of the coenzyme NADH,” Cancer Res. 65(19), 8766–8773 (2005).
[CrossRef] [PubMed]

Bisland, S. K.

A. Bogaards, A. Varma, K. Zhang, D. Zach, S. K. Bisland, E. H. Moriyama, L. Lilge, P. J. Muller, and B. C. Wilson, “Fluorescence image-guided brain tumour resection with adjuvant metronomic photodynamic therapy: pre-clinical model and technology development,” Photochem. Photobiol. Sci. 4(5), 438–442 (2005).
[CrossRef] [PubMed]

S. K. Bisland, L. Lilge, A. Lin, R. Rusnov, and B. C. Wilson, “Metronomic photodynamic therapy as a new paradigm for photodynamic therapy: rationale and preclinical evaluation of technical feasibility for treating malignant brain tumors,” Photochem. Photobiol. 80(1), 22–30 (2004).
[CrossRef] [PubMed]

Bogaards, A.

A. Bogaards, A. Varma, K. Zhang, D. Zach, S. K. Bisland, E. H. Moriyama, L. Lilge, P. J. Muller, and B. C. Wilson, “Fluorescence image-guided brain tumour resection with adjuvant metronomic photodynamic therapy: pre-clinical model and technology development,” Photochem. Photobiol. Sci. 4(5), 438–442 (2005).
[CrossRef] [PubMed]

Bourré, L.

F. Giuntini, L. Bourré, A. J. MacRobert, M. Wilson, and I. M. Eggleston, “Improved peptide prodrugs of 5-ALA for PDT: rationalization of cellular accumulation and protoporphyrin IX production by direct determination of cellular prodrug uptake and prodrug metabolization,” J. Med. Chem. 52(13), 4026–4037 (2009).
[CrossRef] [PubMed]

Brandsema, J. F.

B. W. Pogue, J. D. Pitts, M. A. Mycek, R. D. Sloboda, C. M. Wilmot, J. F. Brandsema, and J. A. O’Hara, “In vivo NADH fluorescence monitoring as an assay for cellular damage in photodynamic therapy,” Photochem. Photobiol. 74(6), 817–824 (2001).
[CrossRef] [PubMed]

Busch, T. M.

B. W. Henderson, T. M. Busch, and J. W. Snyder, “Fluence rate as a modulator of PDT mechanisms,” Lasers Surg. Med. 38(5), 489–493 (2006).
[CrossRef] [PubMed]

G. Yu, T. Durduran, C. Zhou, H. W. Wang, M. E. Putt, H. M. Saunders, C. M. Sehgal, E. Glatstein, A. G. Yodh, and T. M. Busch, “Noninvasive monitoring of murine tumor blood flow during and after photodynamic therapy provides early assessment of therapeutic efficacy,” Clin. Cancer Res. 11(9), 3543–3552 (2005).
[CrossRef] [PubMed]

B. W. Henderson, S. O. Gollnick, J. W. Snyder, T. M. Busch, P. C. Kousis, R. T. Cheney, and J. Morgan, “Choice of oxygen-conserving treatment regimen determines the inflammatory response and outcome of photodynamic therapy of tumors,” Cancer Res. 64(6), 2120–2126 (2004).
[CrossRef] [PubMed]

Cajthamlová, H.

D. Grebe?ová, K. Kuželová, K. Smetana, M. Pluskalová, H. Cajthamlová, I. Marinov, O. Fuchs, J. Sou?ek, P. Jarolím, and Z. Hrkal, “Mitochondrial and endoplasmic reticulum stress-induced apoptotic pathways are activated by 5-aminolevulinic acid-based photodynamic therapy in HL60 leukemia cells,” J. Photochem. Photobiol. B 69(2), 71–85 (2003).
[CrossRef] [PubMed]

Chen, B.

B. Chen, B. W. Pogue, I. A. Goodwin, J. A. O’Hara, C. M. Wilmot, J. E. Hutchins, P. J. Hoopes, and T. Hasan, “Blood flow dynamics after photodynamic therapy with verteporfin in the RIF-1 tumor,” Radiat. Res. 160(4), 452–459 (2003).
[CrossRef] [PubMed]

Chen, C. T.

H. W. Guo, C. T. Chen, Y. H. Wei, O. K. Lee, V. Gukassyan, F. J. Kao, and H. W. Wang, “Reduced nicotinamide adenine dinucleotide fluorescence lifetime separates human mesenchymal stem cells from differentiated progenies,” J. Biomed. Opt. 13(5), 050505 (2008).
[CrossRef] [PubMed]

H. W. Wang, V. Gukassyan, C. T. Chen, Y. H. Wei, H. W. Guo, J. S. Yu, and F. J. Kao, “Differentiation of apoptosis from necrosis by dynamic changes of reduced nicotinamide adenine dinucleotide fluorescence lifetime in live cells,” J. Biomed. Opt. 13(5), 054011 (2008).
[CrossRef] [PubMed]

Cheney, R. T.

B. W. Henderson, S. O. Gollnick, J. W. Snyder, T. M. Busch, P. C. Kousis, R. T. Cheney, and J. Morgan, “Choice of oxygen-conserving treatment regimen determines the inflammatory response and outcome of photodynamic therapy of tumors,” Cancer Res. 64(6), 2120–2126 (2004).
[CrossRef] [PubMed]

Dolmans, D. E.

D. E. Dolmans, D. Fukumura, and R. K. Jain, “Photodynamic therapy for cancer,” Nat. Rev. Cancer 3(5), 380–387 (2003).
[CrossRef] [PubMed]

Durduran, T.

G. Yu, T. Durduran, C. Zhou, H. W. Wang, M. E. Putt, H. M. Saunders, C. M. Sehgal, E. Glatstein, A. G. Yodh, and T. M. Busch, “Noninvasive monitoring of murine tumor blood flow during and after photodynamic therapy provides early assessment of therapeutic efficacy,” Clin. Cancer Res. 11(9), 3543–3552 (2005).
[CrossRef] [PubMed]

Eggleston, I. M.

F. Giuntini, L. Bourré, A. J. MacRobert, M. Wilson, and I. M. Eggleston, “Improved peptide prodrugs of 5-ALA for PDT: rationalization of cellular accumulation and protoporphyrin IX production by direct determination of cellular prodrug uptake and prodrug metabolization,” J. Med. Chem. 52(13), 4026–4037 (2009).
[CrossRef] [PubMed]

Eickhoff, J.

M. C. Skala, K. M. Riching, A. Gendron-Fitzpatrick, J. Eickhoff, K. W. Eliceiri, J. G. White, and N. Ramanujam, “In vivo multiphoton microscopy of NADH and FAD redox states, fluorescence lifetimes, and cellular morphology in precancerous epithelia,” Proc. Natl. Acad. Sci. U.S.A. 104(49), 19494–19499 (2007).
[CrossRef] [PubMed]

Eliceiri, K. W.

M. C. Skala, K. M. Riching, A. Gendron-Fitzpatrick, J. Eickhoff, K. W. Eliceiri, J. G. White, and N. Ramanujam, “In vivo multiphoton microscopy of NADH and FAD redox states, fluorescence lifetimes, and cellular morphology in precancerous epithelia,” Proc. Natl. Acad. Sci. U.S.A. 104(49), 19494–19499 (2007).
[CrossRef] [PubMed]

D. K. Bird, L. Yan, K. M. Vrotsos, K. W. Eliceiri, E. M. Vaughan, P. J. Keely, J. G. White, and N. Ramanujam, “Metabolic mapping of MCF10A human breast cells via multiphoton fluorescence lifetime imaging of the coenzyme NADH,” Cancer Res. 65(19), 8766–8773 (2005).
[CrossRef] [PubMed]

Elmore, S.

S. Elmore, “Apoptosis: a review of programmed cell death,” Toxicol. Pathol. 35(4), 495–516 (2007).
[CrossRef] [PubMed]

Finlay, J. C.

J. C. Finlay and T. H. Foster, “Hemoglobin oxygen saturations in phantoms and in vivo from measurements of steady-state diffuse reflectance at a single, short source-detector separation,” Med. Phys. 31(7), 1949–1959 (2004).
[CrossRef] [PubMed]

Foster, T. H.

K. K. Wang, S. Mitra, and T. H. Foster, “Photodynamic dose does not correlate with long-term tumor response to mTHPC-PDT performed at several drug-light intervals,” Med. Phys. 35(8), 3518–3526 (2008).
[CrossRef] [PubMed]

K. K.-H. Wang, S. Mitra, and T. H. Foster, “A comprehensive mathematical model of microscopic dose deposition in photodynamic therapy,” Med. Phys. 34(1), 282–293 (2007).
[CrossRef] [PubMed]

J. C. Finlay and T. H. Foster, “Hemoglobin oxygen saturations in phantoms and in vivo from measurements of steady-state diffuse reflectance at a single, short source-detector separation,” Med. Phys. 31(7), 1949–1959 (2004).
[CrossRef] [PubMed]

Fuchs, O.

D. Grebe?ová, K. Kuželová, K. Smetana, M. Pluskalová, H. Cajthamlová, I. Marinov, O. Fuchs, J. Sou?ek, P. Jarolím, and Z. Hrkal, “Mitochondrial and endoplasmic reticulum stress-induced apoptotic pathways are activated by 5-aminolevulinic acid-based photodynamic therapy in HL60 leukemia cells,” J. Photochem. Photobiol. B 69(2), 71–85 (2003).
[CrossRef] [PubMed]

Fukumura, D.

D. E. Dolmans, D. Fukumura, and R. K. Jain, “Photodynamic therapy for cancer,” Nat. Rev. Cancer 3(5), 380–387 (2003).
[CrossRef] [PubMed]

Gendron-Fitzpatrick, A.

M. C. Skala, K. M. Riching, A. Gendron-Fitzpatrick, J. Eickhoff, K. W. Eliceiri, J. G. White, and N. Ramanujam, “In vivo multiphoton microscopy of NADH and FAD redox states, fluorescence lifetimes, and cellular morphology in precancerous epithelia,” Proc. Natl. Acad. Sci. U.S.A. 104(49), 19494–19499 (2007).
[CrossRef] [PubMed]

Gilead, A.

S. Gross, A. Gilead, A. Scherz, M. Neeman, and Y. Salomon, “Monitoring photodynamic therapy of solid tumors online by BOLD-contrast MRI,” Nat. Med. 9(10), 1327–1331 (2003).
[CrossRef] [PubMed]

Giuntini, F.

F. Giuntini, L. Bourré, A. J. MacRobert, M. Wilson, and I. M. Eggleston, “Improved peptide prodrugs of 5-ALA for PDT: rationalization of cellular accumulation and protoporphyrin IX production by direct determination of cellular prodrug uptake and prodrug metabolization,” J. Med. Chem. 52(13), 4026–4037 (2009).
[CrossRef] [PubMed]

Glatstein, E.

G. Yu, T. Durduran, C. Zhou, H. W. Wang, M. E. Putt, H. M. Saunders, C. M. Sehgal, E. Glatstein, A. G. Yodh, and T. M. Busch, “Noninvasive monitoring of murine tumor blood flow during and after photodynamic therapy provides early assessment of therapeutic efficacy,” Clin. Cancer Res. 11(9), 3543–3552 (2005).
[CrossRef] [PubMed]

Gollnick, S. O.

B. W. Henderson, S. O. Gollnick, J. W. Snyder, T. M. Busch, P. C. Kousis, R. T. Cheney, and J. Morgan, “Choice of oxygen-conserving treatment regimen determines the inflammatory response and outcome of photodynamic therapy of tumors,” Cancer Res. 64(6), 2120–2126 (2004).
[CrossRef] [PubMed]

Goodwin, I. A.

B. Chen, B. W. Pogue, I. A. Goodwin, J. A. O’Hara, C. M. Wilmot, J. E. Hutchins, P. J. Hoopes, and T. Hasan, “Blood flow dynamics after photodynamic therapy with verteporfin in the RIF-1 tumor,” Radiat. Res. 160(4), 452–459 (2003).
[CrossRef] [PubMed]

Grebenová, D.

D. Grebe?ová, K. Kuželová, K. Smetana, M. Pluskalová, H. Cajthamlová, I. Marinov, O. Fuchs, J. Sou?ek, P. Jarolím, and Z. Hrkal, “Mitochondrial and endoplasmic reticulum stress-induced apoptotic pathways are activated by 5-aminolevulinic acid-based photodynamic therapy in HL60 leukemia cells,” J. Photochem. Photobiol. B 69(2), 71–85 (2003).
[CrossRef] [PubMed]

Gross, S.

S. Gross, A. Gilead, A. Scherz, M. Neeman, and Y. Salomon, “Monitoring photodynamic therapy of solid tumors online by BOLD-contrast MRI,” Nat. Med. 9(10), 1327–1331 (2003).
[CrossRef] [PubMed]

Gukassyan, V.

H. W. Guo, C. T. Chen, Y. H. Wei, O. K. Lee, V. Gukassyan, F. J. Kao, and H. W. Wang, “Reduced nicotinamide adenine dinucleotide fluorescence lifetime separates human mesenchymal stem cells from differentiated progenies,” J. Biomed. Opt. 13(5), 050505 (2008).
[CrossRef] [PubMed]

H. W. Wang, V. Gukassyan, C. T. Chen, Y. H. Wei, H. W. Guo, J. S. Yu, and F. J. Kao, “Differentiation of apoptosis from necrosis by dynamic changes of reduced nicotinamide adenine dinucleotide fluorescence lifetime in live cells,” J. Biomed. Opt. 13(5), 054011 (2008).
[CrossRef] [PubMed]

Guo, H. W.

J. S. Yu, H. W. Guo, C. H. Wang, Y. H. Wei, and H. W. Wang, “Increase of reduced nicotinamide adenine dinucleotide fluorescence lifetime precedes mitochondrial dysfunction in staurosporine-induced apoptosis of HeLa cells,” J. Biomed. Opt. 16(3), 036008 (2011).
[CrossRef] [PubMed]

H. W. Guo, Y. H. Wei, and H. W. Wang, “Reduced nicotinamide adenine dinucleotide fluorescence lifetime detected poly(adenosine-5?-diphosphate-ribose) polymerase-1-mediated cell death and therapeutic effect of pyruvate,” J. Biomed. Opt. 16(6), 068001 (2011).
[CrossRef] [PubMed]

H. W. Wang, Y. H. Wei, and H. W. Guo, “Reduced nicotinamide adenine dinucleotide (NADH) fluorescence for the detection of cell death,” Anticancer. Agents Med. Chem. 9(9), 1012–1017 (2009).
[PubMed]

H. W. Guo, C. T. Chen, Y. H. Wei, O. K. Lee, V. Gukassyan, F. J. Kao, and H. W. Wang, “Reduced nicotinamide adenine dinucleotide fluorescence lifetime separates human mesenchymal stem cells from differentiated progenies,” J. Biomed. Opt. 13(5), 050505 (2008).
[CrossRef] [PubMed]

H. W. Wang, V. Gukassyan, C. T. Chen, Y. H. Wei, H. W. Guo, J. S. Yu, and F. J. Kao, “Differentiation of apoptosis from necrosis by dynamic changes of reduced nicotinamide adenine dinucleotide fluorescence lifetime in live cells,” J. Biomed. Opt. 13(5), 054011 (2008).
[CrossRef] [PubMed]

Hasan, T.

B. Chen, B. W. Pogue, I. A. Goodwin, J. A. O’Hara, C. M. Wilmot, J. E. Hutchins, P. J. Hoopes, and T. Hasan, “Blood flow dynamics after photodynamic therapy with verteporfin in the RIF-1 tumor,” Radiat. Res. 160(4), 452–459 (2003).
[CrossRef] [PubMed]

Henderson, B. W.

B. W. Henderson, T. M. Busch, and J. W. Snyder, “Fluence rate as a modulator of PDT mechanisms,” Lasers Surg. Med. 38(5), 489–493 (2006).
[CrossRef] [PubMed]

B. W. Henderson, S. O. Gollnick, J. W. Snyder, T. M. Busch, P. C. Kousis, R. T. Cheney, and J. Morgan, “Choice of oxygen-conserving treatment regimen determines the inflammatory response and outcome of photodynamic therapy of tumors,” Cancer Res. 64(6), 2120–2126 (2004).
[CrossRef] [PubMed]

Hoopes, P. J.

B. Chen, B. W. Pogue, I. A. Goodwin, J. A. O’Hara, C. M. Wilmot, J. E. Hutchins, P. J. Hoopes, and T. Hasan, “Blood flow dynamics after photodynamic therapy with verteporfin in the RIF-1 tumor,” Radiat. Res. 160(4), 452–459 (2003).
[CrossRef] [PubMed]

Hrkal, Z.

D. Grebe?ová, K. Kuželová, K. Smetana, M. Pluskalová, H. Cajthamlová, I. Marinov, O. Fuchs, J. Sou?ek, P. Jarolím, and Z. Hrkal, “Mitochondrial and endoplasmic reticulum stress-induced apoptotic pathways are activated by 5-aminolevulinic acid-based photodynamic therapy in HL60 leukemia cells,” J. Photochem. Photobiol. B 69(2), 71–85 (2003).
[CrossRef] [PubMed]

Hutchins, J. E.

B. Chen, B. W. Pogue, I. A. Goodwin, J. A. O’Hara, C. M. Wilmot, J. E. Hutchins, P. J. Hoopes, and T. Hasan, “Blood flow dynamics after photodynamic therapy with verteporfin in the RIF-1 tumor,” Radiat. Res. 160(4), 452–459 (2003).
[CrossRef] [PubMed]

Jain, R. K.

D. E. Dolmans, D. Fukumura, and R. K. Jain, “Photodynamic therapy for cancer,” Nat. Rev. Cancer 3(5), 380–387 (2003).
[CrossRef] [PubMed]

Jarolím, P.

D. Grebe?ová, K. Kuželová, K. Smetana, M. Pluskalová, H. Cajthamlová, I. Marinov, O. Fuchs, J. Sou?ek, P. Jarolím, and Z. Hrkal, “Mitochondrial and endoplasmic reticulum stress-induced apoptotic pathways are activated by 5-aminolevulinic acid-based photodynamic therapy in HL60 leukemia cells,” J. Photochem. Photobiol. B 69(2), 71–85 (2003).
[CrossRef] [PubMed]

Jarvi, M. T.

M. T. Jarvi, M. J. Niedre, M. S. Patterson, and B. C. Wilson, “Singlet oxygen luminescence dosimetry (SOLD) for photodynamic therapy: current status, challenges and future prospects,” Photochem. Photobiol. 82(5), 1198–1210 (2006).
[CrossRef] [PubMed]

Kao, F. J.

H. W. Wang, V. Gukassyan, C. T. Chen, Y. H. Wei, H. W. Guo, J. S. Yu, and F. J. Kao, “Differentiation of apoptosis from necrosis by dynamic changes of reduced nicotinamide adenine dinucleotide fluorescence lifetime in live cells,” J. Biomed. Opt. 13(5), 054011 (2008).
[CrossRef] [PubMed]

H. W. Guo, C. T. Chen, Y. H. Wei, O. K. Lee, V. Gukassyan, F. J. Kao, and H. W. Wang, “Reduced nicotinamide adenine dinucleotide fluorescence lifetime separates human mesenchymal stem cells from differentiated progenies,” J. Biomed. Opt. 13(5), 050505 (2008).
[CrossRef] [PubMed]

Keely, P. J.

D. K. Bird, L. Yan, K. M. Vrotsos, K. W. Eliceiri, E. M. Vaughan, P. J. Keely, J. G. White, and N. Ramanujam, “Metabolic mapping of MCF10A human breast cells via multiphoton fluorescence lifetime imaging of the coenzyme NADH,” Cancer Res. 65(19), 8766–8773 (2005).
[CrossRef] [PubMed]

Kousis, P. C.

B. W. Henderson, S. O. Gollnick, J. W. Snyder, T. M. Busch, P. C. Kousis, R. T. Cheney, and J. Morgan, “Choice of oxygen-conserving treatment regimen determines the inflammatory response and outcome of photodynamic therapy of tumors,” Cancer Res. 64(6), 2120–2126 (2004).
[CrossRef] [PubMed]

Kuželová, K.

D. Grebe?ová, K. Kuželová, K. Smetana, M. Pluskalová, H. Cajthamlová, I. Marinov, O. Fuchs, J. Sou?ek, P. Jarolím, and Z. Hrkal, “Mitochondrial and endoplasmic reticulum stress-induced apoptotic pathways are activated by 5-aminolevulinic acid-based photodynamic therapy in HL60 leukemia cells,” J. Photochem. Photobiol. B 69(2), 71–85 (2003).
[CrossRef] [PubMed]

Lee, O. K.

H. W. Guo, C. T. Chen, Y. H. Wei, O. K. Lee, V. Gukassyan, F. J. Kao, and H. W. Wang, “Reduced nicotinamide adenine dinucleotide fluorescence lifetime separates human mesenchymal stem cells from differentiated progenies,” J. Biomed. Opt. 13(5), 050505 (2008).
[CrossRef] [PubMed]

Lilge, L.

A. Bogaards, A. Varma, K. Zhang, D. Zach, S. K. Bisland, E. H. Moriyama, L. Lilge, P. J. Muller, and B. C. Wilson, “Fluorescence image-guided brain tumour resection with adjuvant metronomic photodynamic therapy: pre-clinical model and technology development,” Photochem. Photobiol. Sci. 4(5), 438–442 (2005).
[CrossRef] [PubMed]

S. K. Bisland, L. Lilge, A. Lin, R. Rusnov, and B. C. Wilson, “Metronomic photodynamic therapy as a new paradigm for photodynamic therapy: rationale and preclinical evaluation of technical feasibility for treating malignant brain tumors,” Photochem. Photobiol. 80(1), 22–30 (2004).
[CrossRef] [PubMed]

B. C. Wilson, M. S. Patterson, and L. Lilge, “Implicit and explicit dosimetry in photodynamic therapy: a New paradigm,” Lasers Med. Sci. 12(3), 182–199 (1997).
[CrossRef] [PubMed]

Lin, A.

S. K. Bisland, L. Lilge, A. Lin, R. Rusnov, and B. C. Wilson, “Metronomic photodynamic therapy as a new paradigm for photodynamic therapy: rationale and preclinical evaluation of technical feasibility for treating malignant brain tumors,” Photochem. Photobiol. 80(1), 22–30 (2004).
[CrossRef] [PubMed]

Loschenov, V. B.

A. A. Stratonnikov and V. B. Loschenov, “Evaluation of blood oxygen saturation in vivo from diffuse reflectance spectra,” J. Biomed. Opt. 6(4), 457–467 (2001).
[CrossRef] [PubMed]

MacRobert, A. J.

F. Giuntini, L. Bourré, A. J. MacRobert, M. Wilson, and I. M. Eggleston, “Improved peptide prodrugs of 5-ALA for PDT: rationalization of cellular accumulation and protoporphyrin IX production by direct determination of cellular prodrug uptake and prodrug metabolization,” J. Med. Chem. 52(13), 4026–4037 (2009).
[CrossRef] [PubMed]

Mak, T. W.

H. Okada and T. W. Mak, “Pathways of apoptotic and non-apoptotic death in tumour cells,” Nat. Rev. Cancer 4(8), 592–603 (2004).
[CrossRef] [PubMed]

Marinov, I.

D. Grebe?ová, K. Kuželová, K. Smetana, M. Pluskalová, H. Cajthamlová, I. Marinov, O. Fuchs, J. Sou?ek, P. Jarolím, and Z. Hrkal, “Mitochondrial and endoplasmic reticulum stress-induced apoptotic pathways are activated by 5-aminolevulinic acid-based photodynamic therapy in HL60 leukemia cells,” J. Photochem. Photobiol. B 69(2), 71–85 (2003).
[CrossRef] [PubMed]

Mitra, S.

K. K. Wang, S. Mitra, and T. H. Foster, “Photodynamic dose does not correlate with long-term tumor response to mTHPC-PDT performed at several drug-light intervals,” Med. Phys. 35(8), 3518–3526 (2008).
[CrossRef] [PubMed]

K. K.-H. Wang, S. Mitra, and T. H. Foster, “A comprehensive mathematical model of microscopic dose deposition in photodynamic therapy,” Med. Phys. 34(1), 282–293 (2007).
[CrossRef] [PubMed]

Morgan, J.

B. W. Henderson, S. O. Gollnick, J. W. Snyder, T. M. Busch, P. C. Kousis, R. T. Cheney, and J. Morgan, “Choice of oxygen-conserving treatment regimen determines the inflammatory response and outcome of photodynamic therapy of tumors,” Cancer Res. 64(6), 2120–2126 (2004).
[CrossRef] [PubMed]

Moriyama, E. H.

A. Bogaards, A. Varma, K. Zhang, D. Zach, S. K. Bisland, E. H. Moriyama, L. Lilge, P. J. Muller, and B. C. Wilson, “Fluorescence image-guided brain tumour resection with adjuvant metronomic photodynamic therapy: pre-clinical model and technology development,” Photochem. Photobiol. Sci. 4(5), 438–442 (2005).
[CrossRef] [PubMed]

Morris, R. L.

N. L. Oleinick, R. L. Morris, and I. Belichenko, “The role of apoptosis in response to photodynamic therapy: what, where, why, and how,” Photochem. Photobiol. Sci. 1(1), 1–21 (2002).
[CrossRef] [PubMed]

Muller, P. J.

A. Bogaards, A. Varma, K. Zhang, D. Zach, S. K. Bisland, E. H. Moriyama, L. Lilge, P. J. Muller, and B. C. Wilson, “Fluorescence image-guided brain tumour resection with adjuvant metronomic photodynamic therapy: pre-clinical model and technology development,” Photochem. Photobiol. Sci. 4(5), 438–442 (2005).
[CrossRef] [PubMed]

Mycek, M. A.

B. W. Pogue, J. D. Pitts, M. A. Mycek, R. D. Sloboda, C. M. Wilmot, J. F. Brandsema, and J. A. O’Hara, “In vivo NADH fluorescence monitoring as an assay for cellular damage in photodynamic therapy,” Photochem. Photobiol. 74(6), 817–824 (2001).
[CrossRef] [PubMed]

Neeman, M.

S. Gross, A. Gilead, A. Scherz, M. Neeman, and Y. Salomon, “Monitoring photodynamic therapy of solid tumors online by BOLD-contrast MRI,” Nat. Med. 9(10), 1327–1331 (2003).
[CrossRef] [PubMed]

Niedre, M. J.

M. T. Jarvi, M. J. Niedre, M. S. Patterson, and B. C. Wilson, “Singlet oxygen luminescence dosimetry (SOLD) for photodynamic therapy: current status, challenges and future prospects,” Photochem. Photobiol. 82(5), 1198–1210 (2006).
[CrossRef] [PubMed]

M. J. Niedre, A. J. Secord, M. S. Patterson, and B. C. Wilson, “In vitro tests of the validity of singlet oxygen luminescence measurements as a dose metric in photodynamic therapy,” Cancer Res. 63(22), 7986–7994 (2003).
[PubMed]

O’Hara, J. A.

B. Chen, B. W. Pogue, I. A. Goodwin, J. A. O’Hara, C. M. Wilmot, J. E. Hutchins, P. J. Hoopes, and T. Hasan, “Blood flow dynamics after photodynamic therapy with verteporfin in the RIF-1 tumor,” Radiat. Res. 160(4), 452–459 (2003).
[CrossRef] [PubMed]

B. W. Pogue, J. D. Pitts, M. A. Mycek, R. D. Sloboda, C. M. Wilmot, J. F. Brandsema, and J. A. O’Hara, “In vivo NADH fluorescence monitoring as an assay for cellular damage in photodynamic therapy,” Photochem. Photobiol. 74(6), 817–824 (2001).
[CrossRef] [PubMed]

Okada, H.

H. Okada and T. W. Mak, “Pathways of apoptotic and non-apoptotic death in tumour cells,” Nat. Rev. Cancer 4(8), 592–603 (2004).
[CrossRef] [PubMed]

Oleinick, N. L.

N. L. Oleinick, R. L. Morris, and I. Belichenko, “The role of apoptosis in response to photodynamic therapy: what, where, why, and how,” Photochem. Photobiol. Sci. 1(1), 1–21 (2002).
[CrossRef] [PubMed]

Patterson, M. S.

M. T. Jarvi, M. J. Niedre, M. S. Patterson, and B. C. Wilson, “Singlet oxygen luminescence dosimetry (SOLD) for photodynamic therapy: current status, challenges and future prospects,” Photochem. Photobiol. 82(5), 1198–1210 (2006).
[CrossRef] [PubMed]

M. J. Niedre, A. J. Secord, M. S. Patterson, and B. C. Wilson, “In vitro tests of the validity of singlet oxygen luminescence measurements as a dose metric in photodynamic therapy,” Cancer Res. 63(22), 7986–7994 (2003).
[PubMed]

B. C. Wilson, M. S. Patterson, and L. Lilge, “Implicit and explicit dosimetry in photodynamic therapy: a New paradigm,” Lasers Med. Sci. 12(3), 182–199 (1997).
[CrossRef] [PubMed]

Pitts, J. D.

B. W. Pogue, J. D. Pitts, M. A. Mycek, R. D. Sloboda, C. M. Wilmot, J. F. Brandsema, and J. A. O’Hara, “In vivo NADH fluorescence monitoring as an assay for cellular damage in photodynamic therapy,” Photochem. Photobiol. 74(6), 817–824 (2001).
[CrossRef] [PubMed]

Pluskalová, M.

D. Grebe?ová, K. Kuželová, K. Smetana, M. Pluskalová, H. Cajthamlová, I. Marinov, O. Fuchs, J. Sou?ek, P. Jarolím, and Z. Hrkal, “Mitochondrial and endoplasmic reticulum stress-induced apoptotic pathways are activated by 5-aminolevulinic acid-based photodynamic therapy in HL60 leukemia cells,” J. Photochem. Photobiol. B 69(2), 71–85 (2003).
[CrossRef] [PubMed]

Pogue, B. W.

B. Chen, B. W. Pogue, I. A. Goodwin, J. A. O’Hara, C. M. Wilmot, J. E. Hutchins, P. J. Hoopes, and T. Hasan, “Blood flow dynamics after photodynamic therapy with verteporfin in the RIF-1 tumor,” Radiat. Res. 160(4), 452–459 (2003).
[CrossRef] [PubMed]

B. W. Pogue, J. D. Pitts, M. A. Mycek, R. D. Sloboda, C. M. Wilmot, J. F. Brandsema, and J. A. O’Hara, “In vivo NADH fluorescence monitoring as an assay for cellular damage in photodynamic therapy,” Photochem. Photobiol. 74(6), 817–824 (2001).
[CrossRef] [PubMed]

Putt, M. E.

G. Yu, T. Durduran, C. Zhou, H. W. Wang, M. E. Putt, H. M. Saunders, C. M. Sehgal, E. Glatstein, A. G. Yodh, and T. M. Busch, “Noninvasive monitoring of murine tumor blood flow during and after photodynamic therapy provides early assessment of therapeutic efficacy,” Clin. Cancer Res. 11(9), 3543–3552 (2005).
[CrossRef] [PubMed]

Ramanujam, N.

M. C. Skala, K. M. Riching, A. Gendron-Fitzpatrick, J. Eickhoff, K. W. Eliceiri, J. G. White, and N. Ramanujam, “In vivo multiphoton microscopy of NADH and FAD redox states, fluorescence lifetimes, and cellular morphology in precancerous epithelia,” Proc. Natl. Acad. Sci. U.S.A. 104(49), 19494–19499 (2007).
[CrossRef] [PubMed]

D. K. Bird, L. Yan, K. M. Vrotsos, K. W. Eliceiri, E. M. Vaughan, P. J. Keely, J. G. White, and N. Ramanujam, “Metabolic mapping of MCF10A human breast cells via multiphoton fluorescence lifetime imaging of the coenzyme NADH,” Cancer Res. 65(19), 8766–8773 (2005).
[CrossRef] [PubMed]

Riching, K. M.

M. C. Skala, K. M. Riching, A. Gendron-Fitzpatrick, J. Eickhoff, K. W. Eliceiri, J. G. White, and N. Ramanujam, “In vivo multiphoton microscopy of NADH and FAD redox states, fluorescence lifetimes, and cellular morphology in precancerous epithelia,” Proc. Natl. Acad. Sci. U.S.A. 104(49), 19494–19499 (2007).
[CrossRef] [PubMed]

Rusnov, R.

S. K. Bisland, L. Lilge, A. Lin, R. Rusnov, and B. C. Wilson, “Metronomic photodynamic therapy as a new paradigm for photodynamic therapy: rationale and preclinical evaluation of technical feasibility for treating malignant brain tumors,” Photochem. Photobiol. 80(1), 22–30 (2004).
[CrossRef] [PubMed]

Salomon, Y.

S. Gross, A. Gilead, A. Scherz, M. Neeman, and Y. Salomon, “Monitoring photodynamic therapy of solid tumors online by BOLD-contrast MRI,” Nat. Med. 9(10), 1327–1331 (2003).
[CrossRef] [PubMed]

Saunders, H. M.

G. Yu, T. Durduran, C. Zhou, H. W. Wang, M. E. Putt, H. M. Saunders, C. M. Sehgal, E. Glatstein, A. G. Yodh, and T. M. Busch, “Noninvasive monitoring of murine tumor blood flow during and after photodynamic therapy provides early assessment of therapeutic efficacy,” Clin. Cancer Res. 11(9), 3543–3552 (2005).
[CrossRef] [PubMed]

Scherz, A.

S. Gross, A. Gilead, A. Scherz, M. Neeman, and Y. Salomon, “Monitoring photodynamic therapy of solid tumors online by BOLD-contrast MRI,” Nat. Med. 9(10), 1327–1331 (2003).
[CrossRef] [PubMed]

Secord, A. J.

M. J. Niedre, A. J. Secord, M. S. Patterson, and B. C. Wilson, “In vitro tests of the validity of singlet oxygen luminescence measurements as a dose metric in photodynamic therapy,” Cancer Res. 63(22), 7986–7994 (2003).
[PubMed]

Sehgal, C. M.

G. Yu, T. Durduran, C. Zhou, H. W. Wang, M. E. Putt, H. M. Saunders, C. M. Sehgal, E. Glatstein, A. G. Yodh, and T. M. Busch, “Noninvasive monitoring of murine tumor blood flow during and after photodynamic therapy provides early assessment of therapeutic efficacy,” Clin. Cancer Res. 11(9), 3543–3552 (2005).
[CrossRef] [PubMed]

Skala, M. C.

M. C. Skala, K. M. Riching, A. Gendron-Fitzpatrick, J. Eickhoff, K. W. Eliceiri, J. G. White, and N. Ramanujam, “In vivo multiphoton microscopy of NADH and FAD redox states, fluorescence lifetimes, and cellular morphology in precancerous epithelia,” Proc. Natl. Acad. Sci. U.S.A. 104(49), 19494–19499 (2007).
[CrossRef] [PubMed]

Sloboda, R. D.

B. W. Pogue, J. D. Pitts, M. A. Mycek, R. D. Sloboda, C. M. Wilmot, J. F. Brandsema, and J. A. O’Hara, “In vivo NADH fluorescence monitoring as an assay for cellular damage in photodynamic therapy,” Photochem. Photobiol. 74(6), 817–824 (2001).
[CrossRef] [PubMed]

Smetana, K.

D. Grebe?ová, K. Kuželová, K. Smetana, M. Pluskalová, H. Cajthamlová, I. Marinov, O. Fuchs, J. Sou?ek, P. Jarolím, and Z. Hrkal, “Mitochondrial and endoplasmic reticulum stress-induced apoptotic pathways are activated by 5-aminolevulinic acid-based photodynamic therapy in HL60 leukemia cells,” J. Photochem. Photobiol. B 69(2), 71–85 (2003).
[CrossRef] [PubMed]

Snyder, J. W.

B. W. Henderson, T. M. Busch, and J. W. Snyder, “Fluence rate as a modulator of PDT mechanisms,” Lasers Surg. Med. 38(5), 489–493 (2006).
[CrossRef] [PubMed]

B. W. Henderson, S. O. Gollnick, J. W. Snyder, T. M. Busch, P. C. Kousis, R. T. Cheney, and J. Morgan, “Choice of oxygen-conserving treatment regimen determines the inflammatory response and outcome of photodynamic therapy of tumors,” Cancer Res. 64(6), 2120–2126 (2004).
[CrossRef] [PubMed]

Soucek, J.

D. Grebe?ová, K. Kuželová, K. Smetana, M. Pluskalová, H. Cajthamlová, I. Marinov, O. Fuchs, J. Sou?ek, P. Jarolím, and Z. Hrkal, “Mitochondrial and endoplasmic reticulum stress-induced apoptotic pathways are activated by 5-aminolevulinic acid-based photodynamic therapy in HL60 leukemia cells,” J. Photochem. Photobiol. B 69(2), 71–85 (2003).
[CrossRef] [PubMed]

Stratonnikov, A. A.

A. A. Stratonnikov and V. B. Loschenov, “Evaluation of blood oxygen saturation in vivo from diffuse reflectance spectra,” J. Biomed. Opt. 6(4), 457–467 (2001).
[CrossRef] [PubMed]

Varma, A.

A. Bogaards, A. Varma, K. Zhang, D. Zach, S. K. Bisland, E. H. Moriyama, L. Lilge, P. J. Muller, and B. C. Wilson, “Fluorescence image-guided brain tumour resection with adjuvant metronomic photodynamic therapy: pre-clinical model and technology development,” Photochem. Photobiol. Sci. 4(5), 438–442 (2005).
[CrossRef] [PubMed]

Vaughan, E. M.

D. K. Bird, L. Yan, K. M. Vrotsos, K. W. Eliceiri, E. M. Vaughan, P. J. Keely, J. G. White, and N. Ramanujam, “Metabolic mapping of MCF10A human breast cells via multiphoton fluorescence lifetime imaging of the coenzyme NADH,” Cancer Res. 65(19), 8766–8773 (2005).
[CrossRef] [PubMed]

Vrotsos, K. M.

D. K. Bird, L. Yan, K. M. Vrotsos, K. W. Eliceiri, E. M. Vaughan, P. J. Keely, J. G. White, and N. Ramanujam, “Metabolic mapping of MCF10A human breast cells via multiphoton fluorescence lifetime imaging of the coenzyme NADH,” Cancer Res. 65(19), 8766–8773 (2005).
[CrossRef] [PubMed]

Wang, C. H.

J. S. Yu, H. W. Guo, C. H. Wang, Y. H. Wei, and H. W. Wang, “Increase of reduced nicotinamide adenine dinucleotide fluorescence lifetime precedes mitochondrial dysfunction in staurosporine-induced apoptosis of HeLa cells,” J. Biomed. Opt. 16(3), 036008 (2011).
[CrossRef] [PubMed]

Wang, H. W.

J. S. Yu, H. W. Guo, C. H. Wang, Y. H. Wei, and H. W. Wang, “Increase of reduced nicotinamide adenine dinucleotide fluorescence lifetime precedes mitochondrial dysfunction in staurosporine-induced apoptosis of HeLa cells,” J. Biomed. Opt. 16(3), 036008 (2011).
[CrossRef] [PubMed]

H. W. Guo, Y. H. Wei, and H. W. Wang, “Reduced nicotinamide adenine dinucleotide fluorescence lifetime detected poly(adenosine-5?-diphosphate-ribose) polymerase-1-mediated cell death and therapeutic effect of pyruvate,” J. Biomed. Opt. 16(6), 068001 (2011).
[CrossRef] [PubMed]

H. W. Wang, Y. H. Wei, and H. W. Guo, “Reduced nicotinamide adenine dinucleotide (NADH) fluorescence for the detection of cell death,” Anticancer. Agents Med. Chem. 9(9), 1012–1017 (2009).
[PubMed]

H. W. Guo, C. T. Chen, Y. H. Wei, O. K. Lee, V. Gukassyan, F. J. Kao, and H. W. Wang, “Reduced nicotinamide adenine dinucleotide fluorescence lifetime separates human mesenchymal stem cells from differentiated progenies,” J. Biomed. Opt. 13(5), 050505 (2008).
[CrossRef] [PubMed]

H. W. Wang, V. Gukassyan, C. T. Chen, Y. H. Wei, H. W. Guo, J. S. Yu, and F. J. Kao, “Differentiation of apoptosis from necrosis by dynamic changes of reduced nicotinamide adenine dinucleotide fluorescence lifetime in live cells,” J. Biomed. Opt. 13(5), 054011 (2008).
[CrossRef] [PubMed]

G. Yu, T. Durduran, C. Zhou, H. W. Wang, M. E. Putt, H. M. Saunders, C. M. Sehgal, E. Glatstein, A. G. Yodh, and T. M. Busch, “Noninvasive monitoring of murine tumor blood flow during and after photodynamic therapy provides early assessment of therapeutic efficacy,” Clin. Cancer Res. 11(9), 3543–3552 (2005).
[CrossRef] [PubMed]

Wang, K. K.

K. K. Wang, S. Mitra, and T. H. Foster, “Photodynamic dose does not correlate with long-term tumor response to mTHPC-PDT performed at several drug-light intervals,” Med. Phys. 35(8), 3518–3526 (2008).
[CrossRef] [PubMed]

Wang, K. K.-H.

K. K.-H. Wang, S. Mitra, and T. H. Foster, “A comprehensive mathematical model of microscopic dose deposition in photodynamic therapy,” Med. Phys. 34(1), 282–293 (2007).
[CrossRef] [PubMed]

Wei, Y. H.

J. S. Yu, H. W. Guo, C. H. Wang, Y. H. Wei, and H. W. Wang, “Increase of reduced nicotinamide adenine dinucleotide fluorescence lifetime precedes mitochondrial dysfunction in staurosporine-induced apoptosis of HeLa cells,” J. Biomed. Opt. 16(3), 036008 (2011).
[CrossRef] [PubMed]

H. W. Guo, Y. H. Wei, and H. W. Wang, “Reduced nicotinamide adenine dinucleotide fluorescence lifetime detected poly(adenosine-5?-diphosphate-ribose) polymerase-1-mediated cell death and therapeutic effect of pyruvate,” J. Biomed. Opt. 16(6), 068001 (2011).
[CrossRef] [PubMed]

H. W. Wang, Y. H. Wei, and H. W. Guo, “Reduced nicotinamide adenine dinucleotide (NADH) fluorescence for the detection of cell death,” Anticancer. Agents Med. Chem. 9(9), 1012–1017 (2009).
[PubMed]

H. W. Guo, C. T. Chen, Y. H. Wei, O. K. Lee, V. Gukassyan, F. J. Kao, and H. W. Wang, “Reduced nicotinamide adenine dinucleotide fluorescence lifetime separates human mesenchymal stem cells from differentiated progenies,” J. Biomed. Opt. 13(5), 050505 (2008).
[CrossRef] [PubMed]

H. W. Wang, V. Gukassyan, C. T. Chen, Y. H. Wei, H. W. Guo, J. S. Yu, and F. J. Kao, “Differentiation of apoptosis from necrosis by dynamic changes of reduced nicotinamide adenine dinucleotide fluorescence lifetime in live cells,” J. Biomed. Opt. 13(5), 054011 (2008).
[CrossRef] [PubMed]

White, J. G.

M. C. Skala, K. M. Riching, A. Gendron-Fitzpatrick, J. Eickhoff, K. W. Eliceiri, J. G. White, and N. Ramanujam, “In vivo multiphoton microscopy of NADH and FAD redox states, fluorescence lifetimes, and cellular morphology in precancerous epithelia,” Proc. Natl. Acad. Sci. U.S.A. 104(49), 19494–19499 (2007).
[CrossRef] [PubMed]

D. K. Bird, L. Yan, K. M. Vrotsos, K. W. Eliceiri, E. M. Vaughan, P. J. Keely, J. G. White, and N. Ramanujam, “Metabolic mapping of MCF10A human breast cells via multiphoton fluorescence lifetime imaging of the coenzyme NADH,” Cancer Res. 65(19), 8766–8773 (2005).
[CrossRef] [PubMed]

Wilmot, C. M.

B. Chen, B. W. Pogue, I. A. Goodwin, J. A. O’Hara, C. M. Wilmot, J. E. Hutchins, P. J. Hoopes, and T. Hasan, “Blood flow dynamics after photodynamic therapy with verteporfin in the RIF-1 tumor,” Radiat. Res. 160(4), 452–459 (2003).
[CrossRef] [PubMed]

B. W. Pogue, J. D. Pitts, M. A. Mycek, R. D. Sloboda, C. M. Wilmot, J. F. Brandsema, and J. A. O’Hara, “In vivo NADH fluorescence monitoring as an assay for cellular damage in photodynamic therapy,” Photochem. Photobiol. 74(6), 817–824 (2001).
[CrossRef] [PubMed]

Wilson, B. C.

M. T. Jarvi, M. J. Niedre, M. S. Patterson, and B. C. Wilson, “Singlet oxygen luminescence dosimetry (SOLD) for photodynamic therapy: current status, challenges and future prospects,” Photochem. Photobiol. 82(5), 1198–1210 (2006).
[CrossRef] [PubMed]

A. Bogaards, A. Varma, K. Zhang, D. Zach, S. K. Bisland, E. H. Moriyama, L. Lilge, P. J. Muller, and B. C. Wilson, “Fluorescence image-guided brain tumour resection with adjuvant metronomic photodynamic therapy: pre-clinical model and technology development,” Photochem. Photobiol. Sci. 4(5), 438–442 (2005).
[CrossRef] [PubMed]

S. K. Bisland, L. Lilge, A. Lin, R. Rusnov, and B. C. Wilson, “Metronomic photodynamic therapy as a new paradigm for photodynamic therapy: rationale and preclinical evaluation of technical feasibility for treating malignant brain tumors,” Photochem. Photobiol. 80(1), 22–30 (2004).
[CrossRef] [PubMed]

M. J. Niedre, A. J. Secord, M. S. Patterson, and B. C. Wilson, “In vitro tests of the validity of singlet oxygen luminescence measurements as a dose metric in photodynamic therapy,” Cancer Res. 63(22), 7986–7994 (2003).
[PubMed]

B. C. Wilson, M. S. Patterson, and L. Lilge, “Implicit and explicit dosimetry in photodynamic therapy: a New paradigm,” Lasers Med. Sci. 12(3), 182–199 (1997).
[CrossRef] [PubMed]

Wilson, M.

F. Giuntini, L. Bourré, A. J. MacRobert, M. Wilson, and I. M. Eggleston, “Improved peptide prodrugs of 5-ALA for PDT: rationalization of cellular accumulation and protoporphyrin IX production by direct determination of cellular prodrug uptake and prodrug metabolization,” J. Med. Chem. 52(13), 4026–4037 (2009).
[CrossRef] [PubMed]

Yan, L.

D. K. Bird, L. Yan, K. M. Vrotsos, K. W. Eliceiri, E. M. Vaughan, P. J. Keely, J. G. White, and N. Ramanujam, “Metabolic mapping of MCF10A human breast cells via multiphoton fluorescence lifetime imaging of the coenzyme NADH,” Cancer Res. 65(19), 8766–8773 (2005).
[CrossRef] [PubMed]

Yodh, A. G.

G. Yu, T. Durduran, C. Zhou, H. W. Wang, M. E. Putt, H. M. Saunders, C. M. Sehgal, E. Glatstein, A. G. Yodh, and T. M. Busch, “Noninvasive monitoring of murine tumor blood flow during and after photodynamic therapy provides early assessment of therapeutic efficacy,” Clin. Cancer Res. 11(9), 3543–3552 (2005).
[CrossRef] [PubMed]

Yu, G.

G. Yu, T. Durduran, C. Zhou, H. W. Wang, M. E. Putt, H. M. Saunders, C. M. Sehgal, E. Glatstein, A. G. Yodh, and T. M. Busch, “Noninvasive monitoring of murine tumor blood flow during and after photodynamic therapy provides early assessment of therapeutic efficacy,” Clin. Cancer Res. 11(9), 3543–3552 (2005).
[CrossRef] [PubMed]

Yu, J. S.

J. S. Yu, H. W. Guo, C. H. Wang, Y. H. Wei, and H. W. Wang, “Increase of reduced nicotinamide adenine dinucleotide fluorescence lifetime precedes mitochondrial dysfunction in staurosporine-induced apoptosis of HeLa cells,” J. Biomed. Opt. 16(3), 036008 (2011).
[CrossRef] [PubMed]

H. W. Wang, V. Gukassyan, C. T. Chen, Y. H. Wei, H. W. Guo, J. S. Yu, and F. J. Kao, “Differentiation of apoptosis from necrosis by dynamic changes of reduced nicotinamide adenine dinucleotide fluorescence lifetime in live cells,” J. Biomed. Opt. 13(5), 054011 (2008).
[CrossRef] [PubMed]

Zach, D.

A. Bogaards, A. Varma, K. Zhang, D. Zach, S. K. Bisland, E. H. Moriyama, L. Lilge, P. J. Muller, and B. C. Wilson, “Fluorescence image-guided brain tumour resection with adjuvant metronomic photodynamic therapy: pre-clinical model and technology development,” Photochem. Photobiol. Sci. 4(5), 438–442 (2005).
[CrossRef] [PubMed]

Zhang, K.

A. Bogaards, A. Varma, K. Zhang, D. Zach, S. K. Bisland, E. H. Moriyama, L. Lilge, P. J. Muller, and B. C. Wilson, “Fluorescence image-guided brain tumour resection with adjuvant metronomic photodynamic therapy: pre-clinical model and technology development,” Photochem. Photobiol. Sci. 4(5), 438–442 (2005).
[CrossRef] [PubMed]

Zhou, C.

G. Yu, T. Durduran, C. Zhou, H. W. Wang, M. E. Putt, H. M. Saunders, C. M. Sehgal, E. Glatstein, A. G. Yodh, and T. M. Busch, “Noninvasive monitoring of murine tumor blood flow during and after photodynamic therapy provides early assessment of therapeutic efficacy,” Clin. Cancer Res. 11(9), 3543–3552 (2005).
[CrossRef] [PubMed]

Anticancer. Agents Med. Chem.

H. W. Wang, Y. H. Wei, and H. W. Guo, “Reduced nicotinamide adenine dinucleotide (NADH) fluorescence for the detection of cell death,” Anticancer. Agents Med. Chem. 9(9), 1012–1017 (2009).
[PubMed]

Cancer Res.

M. J. Niedre, A. J. Secord, M. S. Patterson, and B. C. Wilson, “In vitro tests of the validity of singlet oxygen luminescence measurements as a dose metric in photodynamic therapy,” Cancer Res. 63(22), 7986–7994 (2003).
[PubMed]

B. W. Henderson, S. O. Gollnick, J. W. Snyder, T. M. Busch, P. C. Kousis, R. T. Cheney, and J. Morgan, “Choice of oxygen-conserving treatment regimen determines the inflammatory response and outcome of photodynamic therapy of tumors,” Cancer Res. 64(6), 2120–2126 (2004).
[CrossRef] [PubMed]

D. K. Bird, L. Yan, K. M. Vrotsos, K. W. Eliceiri, E. M. Vaughan, P. J. Keely, J. G. White, and N. Ramanujam, “Metabolic mapping of MCF10A human breast cells via multiphoton fluorescence lifetime imaging of the coenzyme NADH,” Cancer Res. 65(19), 8766–8773 (2005).
[CrossRef] [PubMed]

Clin. Cancer Res.

G. Yu, T. Durduran, C. Zhou, H. W. Wang, M. E. Putt, H. M. Saunders, C. M. Sehgal, E. Glatstein, A. G. Yodh, and T. M. Busch, “Noninvasive monitoring of murine tumor blood flow during and after photodynamic therapy provides early assessment of therapeutic efficacy,” Clin. Cancer Res. 11(9), 3543–3552 (2005).
[CrossRef] [PubMed]

J. Biomed. Opt.

H. W. Wang, V. Gukassyan, C. T. Chen, Y. H. Wei, H. W. Guo, J. S. Yu, and F. J. Kao, “Differentiation of apoptosis from necrosis by dynamic changes of reduced nicotinamide adenine dinucleotide fluorescence lifetime in live cells,” J. Biomed. Opt. 13(5), 054011 (2008).
[CrossRef] [PubMed]

J. S. Yu, H. W. Guo, C. H. Wang, Y. H. Wei, and H. W. Wang, “Increase of reduced nicotinamide adenine dinucleotide fluorescence lifetime precedes mitochondrial dysfunction in staurosporine-induced apoptosis of HeLa cells,” J. Biomed. Opt. 16(3), 036008 (2011).
[CrossRef] [PubMed]

H. W. Guo, Y. H. Wei, and H. W. Wang, “Reduced nicotinamide adenine dinucleotide fluorescence lifetime detected poly(adenosine-5?-diphosphate-ribose) polymerase-1-mediated cell death and therapeutic effect of pyruvate,” J. Biomed. Opt. 16(6), 068001 (2011).
[CrossRef] [PubMed]

A. A. Stratonnikov and V. B. Loschenov, “Evaluation of blood oxygen saturation in vivo from diffuse reflectance spectra,” J. Biomed. Opt. 6(4), 457–467 (2001).
[CrossRef] [PubMed]

H. W. Guo, C. T. Chen, Y. H. Wei, O. K. Lee, V. Gukassyan, F. J. Kao, and H. W. Wang, “Reduced nicotinamide adenine dinucleotide fluorescence lifetime separates human mesenchymal stem cells from differentiated progenies,” J. Biomed. Opt. 13(5), 050505 (2008).
[CrossRef] [PubMed]

J. Med. Chem.

F. Giuntini, L. Bourré, A. J. MacRobert, M. Wilson, and I. M. Eggleston, “Improved peptide prodrugs of 5-ALA for PDT: rationalization of cellular accumulation and protoporphyrin IX production by direct determination of cellular prodrug uptake and prodrug metabolization,” J. Med. Chem. 52(13), 4026–4037 (2009).
[CrossRef] [PubMed]

J. Photochem. Photobiol. B

D. Grebe?ová, K. Kuželová, K. Smetana, M. Pluskalová, H. Cajthamlová, I. Marinov, O. Fuchs, J. Sou?ek, P. Jarolím, and Z. Hrkal, “Mitochondrial and endoplasmic reticulum stress-induced apoptotic pathways are activated by 5-aminolevulinic acid-based photodynamic therapy in HL60 leukemia cells,” J. Photochem. Photobiol. B 69(2), 71–85 (2003).
[CrossRef] [PubMed]

Lasers Med. Sci.

B. C. Wilson, M. S. Patterson, and L. Lilge, “Implicit and explicit dosimetry in photodynamic therapy: a New paradigm,” Lasers Med. Sci. 12(3), 182–199 (1997).
[CrossRef] [PubMed]

Lasers Surg. Med.

B. W. Henderson, T. M. Busch, and J. W. Snyder, “Fluence rate as a modulator of PDT mechanisms,” Lasers Surg. Med. 38(5), 489–493 (2006).
[CrossRef] [PubMed]

Med. Phys.

K. K.-H. Wang, S. Mitra, and T. H. Foster, “A comprehensive mathematical model of microscopic dose deposition in photodynamic therapy,” Med. Phys. 34(1), 282–293 (2007).
[CrossRef] [PubMed]

K. K. Wang, S. Mitra, and T. H. Foster, “Photodynamic dose does not correlate with long-term tumor response to mTHPC-PDT performed at several drug-light intervals,” Med. Phys. 35(8), 3518–3526 (2008).
[CrossRef] [PubMed]

J. C. Finlay and T. H. Foster, “Hemoglobin oxygen saturations in phantoms and in vivo from measurements of steady-state diffuse reflectance at a single, short source-detector separation,” Med. Phys. 31(7), 1949–1959 (2004).
[CrossRef] [PubMed]

Nat. Med.

S. Gross, A. Gilead, A. Scherz, M. Neeman, and Y. Salomon, “Monitoring photodynamic therapy of solid tumors online by BOLD-contrast MRI,” Nat. Med. 9(10), 1327–1331 (2003).
[CrossRef] [PubMed]

Nat. Rev. Cancer

D. E. Dolmans, D. Fukumura, and R. K. Jain, “Photodynamic therapy for cancer,” Nat. Rev. Cancer 3(5), 380–387 (2003).
[CrossRef] [PubMed]

H. Okada and T. W. Mak, “Pathways of apoptotic and non-apoptotic death in tumour cells,” Nat. Rev. Cancer 4(8), 592–603 (2004).
[CrossRef] [PubMed]

Photochem. Photobiol.

B. W. Pogue, J. D. Pitts, M. A. Mycek, R. D. Sloboda, C. M. Wilmot, J. F. Brandsema, and J. A. O’Hara, “In vivo NADH fluorescence monitoring as an assay for cellular damage in photodynamic therapy,” Photochem. Photobiol. 74(6), 817–824 (2001).
[CrossRef] [PubMed]

M. T. Jarvi, M. J. Niedre, M. S. Patterson, and B. C. Wilson, “Singlet oxygen luminescence dosimetry (SOLD) for photodynamic therapy: current status, challenges and future prospects,” Photochem. Photobiol. 82(5), 1198–1210 (2006).
[CrossRef] [PubMed]

S. K. Bisland, L. Lilge, A. Lin, R. Rusnov, and B. C. Wilson, “Metronomic photodynamic therapy as a new paradigm for photodynamic therapy: rationale and preclinical evaluation of technical feasibility for treating malignant brain tumors,” Photochem. Photobiol. 80(1), 22–30 (2004).
[CrossRef] [PubMed]

Photochem. Photobiol. Sci.

A. Bogaards, A. Varma, K. Zhang, D. Zach, S. K. Bisland, E. H. Moriyama, L. Lilge, P. J. Muller, and B. C. Wilson, “Fluorescence image-guided brain tumour resection with adjuvant metronomic photodynamic therapy: pre-clinical model and technology development,” Photochem. Photobiol. Sci. 4(5), 438–442 (2005).
[CrossRef] [PubMed]

N. L. Oleinick, R. L. Morris, and I. Belichenko, “The role of apoptosis in response to photodynamic therapy: what, where, why, and how,” Photochem. Photobiol. Sci. 1(1), 1–21 (2002).
[CrossRef] [PubMed]

Proc. Natl. Acad. Sci. U.S.A.

M. C. Skala, K. M. Riching, A. Gendron-Fitzpatrick, J. Eickhoff, K. W. Eliceiri, J. G. White, and N. Ramanujam, “In vivo multiphoton microscopy of NADH and FAD redox states, fluorescence lifetimes, and cellular morphology in precancerous epithelia,” Proc. Natl. Acad. Sci. U.S.A. 104(49), 19494–19499 (2007).
[CrossRef] [PubMed]

Radiat. Res.

B. Chen, B. W. Pogue, I. A. Goodwin, J. A. O’Hara, C. M. Wilmot, J. E. Hutchins, P. J. Hoopes, and T. Hasan, “Blood flow dynamics after photodynamic therapy with verteporfin in the RIF-1 tumor,” Radiat. Res. 160(4), 452–459 (2003).
[CrossRef] [PubMed]

Toxicol. Pathol.

S. Elmore, “Apoptosis: a review of programmed cell death,” Toxicol. Pathol. 35(4), 495–516 (2007).
[CrossRef] [PubMed]

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Figures (4)

Fig. 1
Fig. 1

Effect of different light fluences in response to controls and ALA-PDT treated H1299 cells on (A) cell viability, (B) caspase-3 activity and (C) sub-G1 contents. Sub-G1 contents were determined by FACS analysis of propidium iodide-stained cells for control cells (a), 5-ALA only treated cells (b), light only treated cells (6 J/cm2) (c), 5-ALA treated cells irradiated with light dose of 1 J/cm2 (d), 2 J/cm2 (e), and 6 J/cm2 (f). A total of 3 samples were used for each condition for average ± standard deviation. Symbol * indicates a statistic difference from controls (a) with a p-value less than 0.05 by student t-test.

Fig. 2
Fig. 2

Time course of NADH fluorescence lifetime micrographs of H1299 cells at the condition of 3 controls (treatment with 5-ALA only, light irradiation (6 J/cm2) only, and without 5-ALA and light). The light fluence rate was fixed at 10 mW/cm2 for the light control. The time course images at all conditions were taken at time points of 0 to 20 min (a), 20 to 40 min (b), 60 to 80 min (c), 100 to 120 min (d) after 4 hr serum-free medium treatment for drug controls or after the light irradiation for light controls. Each micrograph has a field of view 100 x 100 μm. The white scale bar indicates 20 μm.

Fig. 3
Fig. 3

Time course of NADH fluorescence lifetime micrographs of H1299 cells at the condition of 5-ALA PDT treatment where cells with the light fluence of 1, 2, 6 J/cm2 in response to PDT were recorded from the same field of view. The light fluence rate was fixed at 10 mW/cm2 for all ALA-PDT treatment conditions. The time course images at all conditions were taken at time points of 0 to 20 min (a), 20 to 40 min (b), 60 to 80 min (c), 100 to 120 min (d) after 4 hour serum-free medium treatment and after the light irradiation. Each micrograph has a field of view 100 x 100 μm. The white scale bar indicates 20 μm.

Fig. 4
Fig. 4

The average ± standard deviation of NADH fluorescence lifetime (τm) (A) and NADH fluorescence intensity (B) respond to ALA-PDT with different light fluences. All PDT-treated cells were incubated with 5-ALA for 4 hours, and then irradiated with different light doses. A total of 6 and 3 samples for lifetime and intensity measurements, respectively, were repeated at each condition. Symbols ** and * indicates a statistic difference from controls with a p-value less than 0.005 and 0.05, respectively, by student t-test. P-values are summarized in Table 1. NADH fluorescence intensity was normalized to cell numbers.

Tables (1)

Tables Icon

Table 1 Statistic Summary for Experiments Statistically Different from Controls

Metrics