Skip to main content

Advertisement

SpringerLink
Log in

The role of photodynamic therapy in overcoming cancer drug resistance

  • Perspective
  • Published:
Photochemical & Photobiological Sciences Aims and scope Submit manuscript

Abstract

Many modalities of cancer therapy induce mechanisms of treatment resistance and escape pathways during chronic treatments, including photodynamic therapy (PDT). It is conceivable that resistance induced by one treatment might be overcome by another treatment. Emerging evidence suggests that the unique mechanisms of tumor cell and microenvironment damage produced by PDT could be utilized to overcome cancer drug resistance, to mitigate the compensatory induction of survival pathways and even to re-sensitize resistant cells to standard therapies. Approaches that capture the unique features of PDT, therefore, offer promising factors for increasing the efficacy of a broad range of therapeutic modalities. Here, we highlight key preclinical findings utilizing PDT to overcome classical drug resistance or escape pathways and thus enhance the efficacy of many pharmaceuticals, possibly explaining the clinical observations of the PDT response to otherwise treatment-resistant diseases. With the development of nanotechnology, it is possible that light activation may be used not only to damage and sensitize tumors but also to enable controlled drug release to inhibit escape pathways that may lead to resistance or cell proliferation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. R. C. Bast, B. Hennessy, G. B. Mills, The biology of ovarian cancer new opportunities for translation, Nat. Rev. Cancer, 2009, 9, 415–428.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. M. T. Milano, et al., Patterns and timing of recurrence after temozolomide-based chemoradiation for glioblastoma, Int. J. Radiat. Oncol., Biol., Phys., 2010, 78, 1147–1155.

    Article  CAS  Google Scholar 

  3. C. Holohan, S. Van Schaeybroeck, D. B. Longley, P. G. Johnston, Cancer drug resistance an evolving paradigm, Nat. Rev. Cancer, 2013, 13, 714–726.

    Article  CAS  PubMed  Google Scholar 

  4. D. Hanahan, R. A. Weinberg, Hallmarks of Cancer: The Next Generation, Cell, 2011, 144, 646–674.

    Article  CAS  PubMed  Google Scholar 

  5. J. P. Thiery, H. Acloque, R. Y. Huang, M. A. Nieto, Epithelial-mesenchymal transitions in development and disease, Cell, 2009, 139, 871–890.

    Article  CAS  PubMed  Google Scholar 

  6. C. T. Jordan, M. L. Guzman, M. Noble, Cancer Stem Cells, N. Engl. J. Med., 2006, 355, 1253–1261.

    Article  CAS  PubMed  Google Scholar 

  7. S. Bao, et al., Glioma stem cells promote radioresistance by preferential activation of the DNA damage response, Nature, 2006, 444, 756–760.

    Article  CAS  PubMed  Google Scholar 

  8. I. Rizvi, et al., Flow induces epithelial-mesenchymal transition, cellular heterogeneity and biomarker modulation in 3D ovarian cancer nodules, Proc. Natl. Acad. Sci. U. S. A., 2013, 110, E1974–E1983.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. R. Kalluri, R. A. Weinberg, The basics of epithelial-mesenchymal transition, J. Clin. Invest., 2009, 119, 1420–1428.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. B. Sennino, et al., Suppression of tumor invasion and metastasis by concurrent inhibition of c-Met and VEGF signaling in pancreatic neuroendocrine tumors, Cancer Discovery, 2012, 2, 270–287.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. S. Thomson, et al., Epithelial to mesenchymal transition is a determinant of sensitivity of non-small-cell lung carcinoma cell lines and xenografts to epidermal growth factor receptor inhibition, Cancer Res., 2005, 65, 9455–9462.

    Article  CAS  PubMed  Google Scholar 

  12. A. M. Haslehurst, et al., EMT transcription factors snail and slug directly contribute to cisplatin resistance in ovarian cancer, BMC Cancer, 2012, 2, 91.

    Article  CAS  Google Scholar 

  13. M. Izumiya, et al., Chemoresistance is associated with cancer stem cell-like properties and epithelial-to-mesenchymal transition in pancreatic cancer cells, Anticancer Res., 2012, 32, 3847–3853.

    CAS  PubMed  Google Scholar 

  14. F. Du, et al., Acquisition of paclitaxel resistance via PI3K-dependent epithelial-mesenchymal transition in A2780 human ovarian cancer cells, Oncol. Rep., 2013, 30, 1113–1118.

    Article  CAS  PubMed  Google Scholar 

  15. S. A. Mani, et al., The epithelial-mesenchymal transition generates cells with properties of stem cells, Cell, 2008, 133, 704–715.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. M. Pàez-Ribes, et al., Antiangiogenic Therapy Elicits Malignant Progression of Tumors to Increased Local Invasion and Distant Metastasis, Cancer Cell, 2009, 15, 220–231.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  17. S. Pennacchietti, et al., Hypoxia promotes invasive growth by transcriptional activation of the met protooncogene, Cancer Cell, 2003, 3, 347–361.

    Article  PubMed  Google Scholar 

  18. B. Sennino, D. M. McDonald, Controlling escape from angiogenesis inhibitors, Nat. Rev. Cancer, 2012, 12, 699–709.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. R. K. Jain, Antiangiogenesis Strategies Revisited: From Starving Tumors to Alleviating Hypoxia, Cancer Cell, 2014, 26, 605–622.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. D. E. J. G. J. Dolmans, D. Fukumura, R. K. Jain, TIMELINE: Photodynamic therapy for cancer, Nat. Rev. Cancer, 2003, 3, 380–387.

    Article  CAS  PubMed  Google Scholar 

  21. C. Schweitzer, R. Schmidt, Physical mechanisms of generation and deactivation of singlet oxygen, Chem. Rev., 2003, 1685–1757.

    Google Scholar 

  22. J. F. Lovell, T. W. B. Liu, J. Chen, G. Zheng, Activatable photosensitizers for imaging and therapy, Chem. Rev., 2010, 110, 2839–2857.

    Article  CAS  PubMed  Google Scholar 

  23. J. P. Celli, et al., Imaging and photodynamic therapy: mechanisms, monitoring, and optimization, Chem. Rev., 2010, 110, 2795–2838.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. B. Spring, et al., Selective treatment and monitoring of disseminated cancer micrometastases in vivo using dual-function, activatable immunoconjugates, Proc. Natl. Acad. Sci. U. S. A., 2014, 111, E933–E942.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. M. L. Agarwal, et al., Photodynamic therapy induces rapid cell death by apoptosis in L5178Y mouse lymphoma cells, Cancer Res., 1991, 51, 5993–5996.

    CAS  PubMed  Google Scholar 

  26. D. Kessel, Death pathways associated with photodynamic therapy, Med. Laser Appl., 2006, 21, 219–224.

    Article  PubMed  PubMed Central  Google Scholar 

  27. R. Rahmanzadeh, et al., Ki-67 as a molecular target for therapy in an in vitro three-dimensional model for ovarian cancer, Cancer Res., 2010, 70, 9234–9242.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Q. Wan, L. Liu, D. Xing, Q. Chen, Bid Is Required in NPe6-PDT-induced Apoptosis, Photochem. Photobiol., 2007, 84, 250–257.

    Article  CAS  Google Scholar 

  29. J. J. Reiners, P. Agostinis, K. Berg, N. L. Oleinick, D. Kessel, Assessing autophagy in the context of photodynamic therapy, Autophagy, 2010, 6, 7–18.

    Article  CAS  PubMed  Google Scholar 

  30. J. Lindsay, M. D. Esposti, A. P. Gilmore, Bcl-2 proteins and mitochondria–specificity in membrane targeting for death, Biochim. Biophys. Acta, 2011, 1813, 532–539.

    Article  CAS  PubMed  Google Scholar 

  31. B. Schellenberg, et al., Bax exists in a dynamic equilibrium between the cytosol and mitochondria to control apoptotic priming, Mol. Cell, 2013, 49, 959–971.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. D. Kessel, Y. Luo, Photodynamic therapy: A mitochondrial inducer of apoptosis, Cell Death Differ., 1999, 6, 28–35.

    Article  CAS  PubMed  Google Scholar 

  33. J. C. Reed, et al., BCL-2 family proteins: Regulators of cell death involved in the pathogenesis of cancer and resistance to therapy, J. Cell. Biochem., 1996, 60, 23–32.

    Article  CAS  PubMed  Google Scholar 

  34. A. Villanueva, J. C. Stockert, M. Cañete, P. Acedo, A new protocol in photodynamic therapy: enhanced tumour cell death by combining two different photosensitizers, Photochem. Photobiol. Sci., 2010, 9, 295–297.

    Article  CAS  PubMed  Google Scholar 

  35. P. Acedo, J. C. Stockert, M. Canete, A. Villanueva, Two combined photosensitizers: a goal for more effective photodynamic therapy of cancer, Cell Death Dis., 2014, 5, e1122.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. X. Schneider-Yin, et al., Hypericin and 5-aminolevulinic acid-induced protoporphyrin IX induce enhanced phototoxicity in human endometrial cancer cells with non-coherent white light, Photodiagn. Photodyn. Ther., 2009, 6, 12–18.

    Article  CAS  Google Scholar 

  37. E. B. Gyenge, et al., Photodynamic mechanisms induced by a combination of hypericin and a chlorin based-photosensitizer in head and neck squamous cell carcinoma cells, Photochem. Photobiol., 2013, 89, 150–162.

    Article  CAS  PubMed  Google Scholar 

  38. D. Kessel, J. J. Reiners, Enhanced Efficacy of Photodynamic Therapy via a Sequential Targeting Protocol, Photochem. Photobiol., 2014, 90, 889–895.

    CAS  PubMed  PubMed Central  Google Scholar 

  39. L. Cincotta, D. Szeto, E. Lampros, T. Hasan, A. H. Cincotta, Benzophenothiazine and Benzoporphyrin Derivative Combination Phototherapy Effectively Eradicates Large Murine Sarcomas, Photochem. Photobiol., 1996, 63, 229–237.

    Article  CAS  PubMed  Google Scholar 

  40. M. M. Gottesman, T. Fojo, S. E. Bates, Multidrug resistance in cancer: role of ATP[ndash] dependent transporters, Nat. Rev. Cancer, 2002, 2, 48–58.

    Article  CAS  PubMed  Google Scholar 

  41. V. Goler-Baron, Y. G. Assaraf, Overcoming multidrug resistance via photodestruction of ABCG2-rich extracellular vesicles sequestering photosensitive chemotherapeutics, PLoS One, 2012, 7, e35487.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. S. O. Gollnick, L. Vaughan, B. W. Henderson, Generation of effective antitumor vaccines using photodynamic therapy, Cancer Res., 2002, 62, 1604–1608.

    CAS  PubMed  Google Scholar 

  43. M. Shams, B. Owczarczak, P. Manderscheid-Kern, D. A. Bellnier, S. O. Gollnick, Development of photodynamic therapy regimens that control primary tumor growth and inhibit secondary disease, Cancer Immunol. Immunother., 2015, 64, 287–297.

    Article  CAS  PubMed  Google Scholar 

  44. A. P. Castano, P. Mroz, M. R. Hamblin, Photodynamic therapy and anti-tumour immunity, Nat. Rev. Cancer, 2006, 6, 535–545.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. B. Chen, B. W. Pogue, P. J. Hoopes, T. Hasan, Combining vascular and cellular targeting regimens enhances the efficacy of photodynamic therapy, Int. J. Radiat. Oncol., Biol., Phys., 2005, 61, 1216–1226.

    Article  CAS  Google Scholar 

  46. V. H. Fingar, et al., Analysis of acute vascular damage after photodynamic therapy using benzoporphyrin derivative (BPD), Br. J. Cancer, 1999, 79, 1702–1708.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. K. Kurohane, et al., Photodynamic therapy targeted to tumor-induced angiogenic vessels, Cancer Lett., 2001, 167, 49–56.

    Article  CAS  PubMed  Google Scholar 

  48. U. Schmidt-Erfurth, T. Hasan, Mechanisms of Action of Photodynamic Therapy with Verteporfin for the Treatment of Age-Related Macular Degeneration, Surv. Ophthalmol., 2000, 45, 195–214.

    Article  CAS  PubMed  Google Scholar 

  49. J. W. Snyder, W. R. Greco, D. A. Bellnier, L. Vaughan, B. W. Henderson, Photodynamic therapy: a means to enhanced drug delivery to tumors, Cancer Res., 2003, 63, 8126–8131.

    CAS  PubMed  Google Scholar 

  50. B. Chen, B. W. Pogue, J. M. Luna, R. L. Hardman, P. J. Hoopes, Tumor vascular permeabilization by vascular-targeting photosensitization: effects, mechanism, and therapeutic implications, Clin. Cancer Res., 2006, 12, 917–923.

    Article  CAS  PubMed  Google Scholar 

  51. M. Gil, et al., Photodynamic therapy augments the efficacy of oncolytic vaccinia virus against primary and metastatic tumours in mice, Br. J. Cancer, 2011, 105, 1512–1521.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. K. Sano, T. Nakajima, P. L. Choyke, H. Kobayashi, Markedly enhanced permeability and retention effects induced by photo-immunotherapy of tumors, ACS Nano, 2013, 7, 717–724.

    Article  CAS  PubMed  Google Scholar 

  53. O.-J. Norum, P. K. Selbo, A. Weyergang, K.-E. Giercksky, K. Berg, Photochemical internalization (PCI) in cancer therapy: From bench towards bedside medicine, J. Photochem. Photobiol., B, 2009, 96, 83–92.

    Article  CAS  Google Scholar 

  54. P. K. Selbo, et al., Strongly amphiphilic photosensitizers are not substrates of the cancer stem cell marker ABCG2 and provides specific and efficient light-triggered drug delivery of an EGFR-targeted cytotoxic drug, J. Controlled Release, 2012, 159, 197–203.

    Article  CAS  Google Scholar 

  55. M. Bostad, et al., Photochemical internalization (PCI) of immunotoxins targeting CD133 is specific and highly potent at femtomolar levels in cells with cancer stem cell properties, J. Controlled Release, 2013, 168, 317–326.

    Article  CAS  Google Scholar 

  56. M. Bostad, et al., Light-triggered, efficient cytosolic release of IM7-saporin targeting the putative cancer stem cell marker CD44 by photochemical internalization, Mol. Pharm., 2014, 11, 2764–2776.

    Article  CAS  PubMed  Google Scholar 

  57. A. Casas, G. Di Venosa, A. Batlle, Mechanisms of resistance to photodynamic therapy, Curr. Med. Chem., 2011, 18, 2486–2515.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. C. L. Evans, et al., Killing hypoxic cell populations in a 3D tumor model with EtNBS-PDT, PLoS One, 2011, 6, e23434.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. M. C. Luna, C. J. Gomer, Isolation and initial characterization of mouse tumor cells resistant to porphyrin-mediated photodynamic therapy, Cancer Res., 1991, 51, 4243–4249.

    CAS  PubMed  Google Scholar 

  60. B. C. Wilson, M. Olivo, G. Singh, Subcellular Localization of Photofrin and Aminolevulinic Acid and Photodynamic Cross-Resistance in Vitro in Radiation-Induced Fibrosarcoma Cells Sensitive or Resistant to Photofrin-Mediated Photodynamic Therapy, Photochem. Photobiol., 1997, 65, 166–176.

    Article  CAS  PubMed  Google Scholar 

  61. R. A. Moorehead, S. G. Armstrong, B. C. Wilson, G. Singh, Cross-Resistance to Cisplatin in Cells Resistant to Photofrin-mediated Photodynamic Therapy, Cancer Res., 1994, 54, 2556–2559.

    CAS  PubMed  Google Scholar 

  62. A. Casas, et al., Tumor cell lines resistant to ALA-mediated photodynamic therapy and possible tools to target surviving cells, Int. J. Oncol., 2006, 29, 397–405.

    CAS  PubMed  Google Scholar 

  63. Z. Duan, D. E. Lamendola, Y. Duan, R. Z. Yusuf, M. V. Seiden, Description of paclitaxel resistance-associated genes in ovarian and breast cancer cell lines, Cancer Chemother. Pharmacol., 2004, 55, 277–285.

    Article  PubMed  CAS  Google Scholar 

  64. D. Roberts, et al., Identification of genes associated with platinum drug sensitivity and resistance in human ovarian cancer cells, Br. J. Cancer, 2005, 92, 1149–1158.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. R. W. Robey, K. Steadman, O. Polgar, S. E. Bates, ABCG2-mediated transport of photosensitizers: potential impact on photodynamic therapy, Cancer Biol. Ther., 2005, 4, 187–194.

    Article  CAS  PubMed  Google Scholar 

  66. W. Liu, et al., The Tyrosine Kinase Inhibitor Imatinib Mesylate Enhances the Efficacy of Photodynamic Therapy by Inhibiting ABCG2, Clin. Cancer Res., 2007, 13, 2463–2470.

    Article  CAS  PubMed  Google Scholar 

  67. J. Morgan, J. D. Jackson, X. Zheng, S. K. Pandey, R. K. Pandey, Substrate affinity of photosensitizers derived from chlorophyll-a: the ABCG2 transporter affects the phototoxic response of side population stem cell-like cancer cells to photodynamic therapy, Mol. Pharm., 2010, 7, 1789–1804.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. C.-H. Yu, C.-C. Yu, Photodynamic therapy with 5-aminolevulinic acid (ALA) impairs tumor initiating and chemo-resistance property in head and neck cancer-derived cancer stem cells, PLoS One, 2014, 9, e87129.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  69. T. A. Yap, C. P. Carden, S. B. Kaye, Beyond chemotherapy: targeted therapies in ovarian cancer, Nat. Rev. Cancer, 2009, 9, 167–181.

    Article  CAS  PubMed  Google Scholar 

  70. T. Conroy, et al., FOLFIRINOX versus gemcitabine for metastatic pancreatic cancer, N. Engl. J. Med., 2011, 364, 1817–1825.

    Article  CAS  PubMed  Google Scholar 

  71. M. G. del Carmen, et al., Synergism of epidermal growth factor receptor-targeted immunotherapy with photodynamic treatment of ovarian cancer in vivo, J. Natl. Cancer Inst., 2005, 97, 1516–1524.

    Article  CAS  PubMed  Google Scholar 

  72. I. Rizvi, et al., Synergistic enhancement of carboplatin efficacy with photodynamic therapy in a three-dimensional model for micrometastatic ovarian cancer, Cancer Res., 2010, 70, 9319–9328.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. L. R. Duska, M. R. Hamblin, J. L. Miller, T. Hasan, Combination photoimmunotherapy and cisplatin: effects on human ovarian cancer ex vivo, J. Natl. Cancer Inst., 1999, 91, 1557–1563.

    Article  CAS  PubMed  Google Scholar 

  74. M. F. Zuluaga, N. Lange, Combination of photodynamic therapy with anti-cancer agents, Curr Med Chem., 2008, 15, 1655–1673.

    Article  CAS  PubMed  Google Scholar 

  75. M. Y. Nahabedian, R. A. Cohen, M. F. Contino, et al. Combination cytotoxic chemotherapy with cisplatin or doxorubicin and photodynamic therapy in murine tumors, J. Natl. Cancer Inst., 1988, 80, 739–743.

    Article  CAS  PubMed  Google Scholar 

  76. G. Canti, A. Nicolin, R. Cubeddu, P. Taroni, G. Bandieramonte, G. Valentini, Antitumor efficacy of the combination of photodynamic therapy and chemotherapy in murine tumors, Cancer Lett., 1998, 125, 39–44.

    Article  CAS  PubMed  Google Scholar 

  77. C. M. Peterson, J. M. Lu, Y. Sun, et al. Combination chemotherapy and photodynamic therapy with N-(2-hydroxypropyl) methacrylamide copolymer-bound anticancer drugs inhibit human ovarian carcinoma heterotransplanted in nude mice, Cancer Res., 1996, 56, 3980–3985.

    CAS  PubMed  Google Scholar 

  78. J. P. Celli, N. Solban, A. Liang, S. P. Pereira, T. Hasan, Verteporfin-based photodynamic therapy overcomes gemcitabine insensitivity in a panel of pancreatic cancer cell lines, Lasers Surg. Med., 2011, 43, 565–574.

    Article  PubMed  PubMed Central  Google Scholar 

  79. B. A. Goff, M. Bamberg, T. Hasan, Photoimmunotherapy of human ovarian carcinoma cells ex vivo, Cancer Res., 1991, 51, 4762–4767.

    CAS  PubMed  Google Scholar 

  80. J. M. Stommel, et al., Coactivation of Receptor Tyrosine Kinases Affects the Response of Tumor Cells to Targeted Therapies, Science, 2007, 318, 287–290.

    Article  CAS  PubMed  Google Scholar 

  81. A. D. Rhim, et al., Stromal elements act to restrain, rather than support, pancreatic ductal adenocarcinoma, Cancer Cell, 2014, 25, 735–747.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. B. C. Özdemir, et al., Depletion of carcinoma-associated fibroblasts and fibrosis induces immunosuppression and accelerates pancreas cancer with reduced survival, Cancer Cell, 2014, 25, 719–734.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  83. M. Upreti, et al., Tumor-Endothelial Cell Three-dimensional Spheroids: New Aspects to Enhance Radiation and Drug Therapeutics, Transl. Oncol., 2011, 4, 365–376.

    Article  PubMed  PubMed Central  Google Scholar 

  84. J. W. Franses, A. B. Baker, V. C. Chitalia, E. R. Edelman, Stromal endothelial cells directly influence cancer progression, Sci. Transl. Med., 2011, 3, 665.

    Article  CAS  Google Scholar 

  85. S. K. Chang, I. Rizvi, N. Solban, In vivo optical molecular imaging of vascular endothelial growth factor for monitoring cancer treatment, Clin. Cancer Res., 2008, 14, 4146–4153.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. C. J. Gomer, et al., Photodynamic Therapy-mediated Oxidative Stress Can Induce Expression of Heat Shock Proteins, Cancer Res., 1996, 56, 2355–2360.

    CAS  PubMed  Google Scholar 

  87. A. Ferrario, et al., Antiangiogenic treatment enhances photodynamic therapy responsiveness in a mouse mammary carcinoma, Cancer Res., 2000, 60, 4066–4069.

    CAS  PubMed  Google Scholar 

  88. A. Ferrario, N. Rucker, S. Wong, M. Luna, C. J. Gomer, Survivin, a Member of the Inhibitor of Apoptosis Family, Is Induced by Photodynamic Therapy and Is a Target for Improving Treatment Response, Cancer Res., 2007, 67, 4989–4995.

    Article  CAS  PubMed  Google Scholar 

  89. D. L. Wheeler, E. F. Dunn, P. M. Harari, Understanding resistance to EGFR inhibitors-impact on future treatment strategies, Nat. Rev. Clin. Oncol., 2010, 7, 493–507.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Y. Gilaberte, et al., Cellular intrinsic factors involved in the resistance of squamous cell carcinoma to photodynamic therapy, J. Invest. Dermatol., 2014, 134, 2428–2437.

    Article  CAS  PubMed  Google Scholar 

  91. N. Solban, et al., Mechanistic investigation and implications of photodynamic therapy induction of vascular endothelial growth factor in prostate cancer, Cancer Res., 2006, 66, 5633–5640.

    Article  CAS  PubMed  Google Scholar 

  92. P. Nowak-Sliwinska, J. R. van Beijnum, M. van Berkel, H. van den Bergh, A. W. Griffioen, Vascular regrowth following photodynamic therapy in the chicken embryo chorioallantoic membrane, Angiogenesis, 2010, 13, 281–292.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. A. Weiss, et al., Low-dose angiostatic tyrosine kinase inhibitors improve photodynamic therapy for cancer: lack of vascular normalization, J. Cell. Mol. Med., 2014, 18, 480–491.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. P. Nowak-Sliwinska, et al., Angiostatic kinase inhibitors to sustain photodynamic angio-occlusion, J. Cell. Mol. Med., 2012, 16, 1553–1562.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. D. H. Gorski, et al., Blockade of the vascular endothelial growth factor stress response increases the antitumor effects of ionizing radiation, Cancer Res., 1999, 59, 3374–3378.

    CAS  PubMed  Google Scholar 

  96. J. Tran, et al., A role for survivin in chemoresistance of endothelial cells mediated by VEGF, Proc. Natl. Acad. Sci. U. S. A., 2002, 99, 4349–4354.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. C. Justinger, et al., Increased growth factor expression after hepatic and pancreatic resection, Oncol. Rep., 2008, 20, 1527–1531.

    PubMed  Google Scholar 

  98. B. Kosharskyy, et al., A mechanism-based combination therapy reduces local tumor growth and metastasis in an orthotopic model of prostate cancer, Cancer Res., 2006, 66, 10953–10958.

    Article  CAS  PubMed  Google Scholar 

  99. H.-C. Huang, T. Hasan, The ‘Nano’ World in Photodynamic Therapy, Aust. J. Nanomed. Nanotechnol., 2014, 2, 4.

    Google Scholar 

  100. J. F. Lovell, et al., Porphysome nanovesicles generated by porphyrin bilayers for use as multimodal biophotonic contrast agents, Nat. Mater., 2011, 10, 324–332.

    Article  CAS  PubMed  Google Scholar 

  101. K. A. Carter, et al., Porphyrin-phospholipid liposomes permeabilized by near-infrared light, Nat. Commun., 2014, 5, 3546.

    Article  PubMed  CAS  Google Scholar 

  102. T. Nomoto, et al., Three-layered polyplex micelle as a multifunctional nanocarrier platform for light-induced systemic gene transfer, Nat. Commun., 2014, 5, 3545.

    Article  PubMed  CAS  Google Scholar 

  103. T. R. Wilson, et al., Widespread potential for growth-factor-driven resistance to anticancer kinase inhibitors, Nature, 2012, 487, 505–509.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. C. Hage, et al., The novel c-Met inhibitor cabozantinib overcomes gemcitabine resistance and stem cell signaling in pancreatic cancer, Cell Death Dis., 2013, 4, e627.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. E. Gherardi, W. Birchmeier, C. Birchmeier, G. Vande-Woude, Targeting MET in cancer: rationale and progress, Nat. Rev. Cancer, 2012, 12, 89–103.

    Article  CAS  PubMed  Google Scholar 

  106. S. Peters, A. A. Adjei, MET: a promising anticancer therapeutic target, Nat. Rev. Clin. Oncol., 2012, 9, 314–326.

    Article  CAS  PubMed  Google Scholar 

  107. B. Sennino, T. Ishiguro-Oonuma, B. J. Schriver, J. G. Christensen, D. M. McDonald, Inhibition of c-Met reduces lymphatic metastasis in RIP-Tag2 transgenic mice, Cancer Res., 2013, 73, 3692–3703.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. L. Z. Zheng, et al., Abstract A127: Combination therapy targeting EGFR/MET crosstalk using nanotechnology improves photodynamic therapy treatment of pancreatic cancer, Mol. Cancer Ther., 2009, 8, A127–A127.

    Article  CAS  Google Scholar 

  109. M. Bernstein and M. S. Berger, Neuro-oncology: The Essentials, Thieme, 2011.

    Google Scholar 

  110. M. T. Huggett, et al., Phase I/II study of verteporfin photodynamic therapy in locally advanced pancreatic cancer, Br. J. Cancer, 2014, 110, 1698–1704.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. M. S. Eljamel, C. Goodman, H. Moseley, ALA and Photofrin fluorescence-guided resection and repetitive PDT in glioblastoma multiforme: a single centre Phase III randomised controlled trial, Lasers Med. Sci., 2008, 23, 361–367.

    Article  PubMed  Google Scholar 

  112. J. S. Friedberg, et al., Phase II trial of pleural photodynamic therapy and surgery for patients with non-small-cell lung cancer with pleural spread, J. Clin. Oncol., 2004, 22, 2192–2201.

    Article  CAS  PubMed  Google Scholar 

  113. S. M. Hahn, et al., A phase II trial of intraperitoneal photodynamic therapy for patients with peritoneal carcinomatosis and sarcomatosis, Clin. Cancer Res., 2006, 12, 2517–2525.

    Article  CAS  PubMed  Google Scholar 

  114. K. L. Molpus, et al., Intraperitoneal photodynamic therapy of human epithelial ovarian carcinomatosis in a xenograft murine model, Cancer Res., 1996, 56, 1075–1082.

    CAS  PubMed  Google Scholar 

  115. M. A. Biel, Photodynamic Therapy Treatment of Early Oral and Laryngeal Cancers, Photochem. Photobiol., 2007, 83, 1063–1068.

    Article  CAS  PubMed  Google Scholar 

  116. V. C. K. Lo, et al., The benefits of photodynamic therapy on vertebral bone are maintained and enhanced by combination treatment with bisphosphonates and radiation therapy, J. Orthop. Res., 2013, 31, 1398–1405.

    Article  CAS  PubMed  Google Scholar 

  117. M. Mitsunaga, et al., Cancer cell-selective in vivo near infrared photoimmunotherapy targeting specific membrane molecules, Nat. Med., 2011, 17, 1685–1691.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. T. L. Doane, C.-H. Chuang, A. Chomas, C. Burda, Photophysics of silicon phthalocyanines in aqueous media, Chem.–Eur. J. Chem. Phys., 2013, 14, 321–330.

    Article  CAS  Google Scholar 

  119. J. D. Miller, et al., Photodynamic therapy with the phthalocyanine photosensitizer Pc 4: the case experience with preclinical mechanistic and early clinical-translational studies, Toxicol. Appl. Pharmacol., 2007, 224, 290–299.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. M. B. Vrouenraets, et al., Targeting of Aluminum (III) Phthalocyanine Tetrasulfonate by Use of Internalizing Monoclonal Antibodies Improved Efficacy in Photodynamic Therapy, Cancer Res., 2001, 61, 1970–1975.

    CAS  PubMed  Google Scholar 

  121. M. B. Vrouenraets, et al., Comparison of aluminium (III) phthalocyanine tetrasulfonate- and meta-tetrahydroxyphenylchlorin-monoclonal antibody conjugates for their efficacy in photodynamic therapy in vitro, Int. J. Cancer, 2002, 98, 793–798.

    Article  CAS  PubMed  Google Scholar 

  122. D. Mew, C. K. Wat, G. H. Towers, J. G. Levy, Photoimmunotherapy: treatment of animal tumors with tumor-specific monoclonal antibody-hematoporphyrin conjugates, J. Immunol., 1983, 130, 1473–1477.

    CAS  PubMed  Google Scholar 

  123. W. Stummer, et al., Fluorescence-guided surgery with 5-aminolevulinic acid for resection of malignant glioma: a randomised controlled multicentre phase III trial, Lancet Oncol., 2006, 7, 392–401.

    Article  CAS  PubMed  Google Scholar 

  124. I. Rizvi, et al., Photoimmunotherapy and irradiance modulation reduce chemotherapy cycles and toxicity in a murine model for ovarian carcinomatosis: perspective and results, Isr. J. Chem., 2012, 52, 776–787.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. K. Meirelles, et al., Human ovarian cancer stem/progenitor cells are stimulated by doxorubicin but inhibited by Mullerian inhibiting substance, Proc. Natl. Acad. Sci. U. S. A., 2012, 109, 2358–2363.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Wellman Center for Photomedicine, Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts, USA

    Bryan Q. Spring, Imran Rizvi & Nan Xu

  2. Department of Medicine, Brigham and Women’s Hospital, Boston, Massachusetts, USA

    Imran Rizvi

  3. Department of Dermatology, Shanghai East Hospital and Tongji University, Shanghai, China

    Nan Xu

  4. Division of Health Sciences and Technology, Harvard University and Massachusetts Institute of Technology, Cambridge, Massachusetts, USA

    Tayyaba Hasan

Authors
  1. Bryan Q. Spring
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Imran Rizvi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Nan Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Tayyaba Hasan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Tayyaba Hasan.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Spring, B.Q., Rizvi, I., Xu, N. et al. The role of photodynamic therapy in overcoming cancer drug resistance. Photochem Photobiol Sci 14, 1476–1491 (2015). https://doi.org/10.1039/c4pp00495g

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1039/c4pp00495g

Search

Navigation