Photodynamic Therapy : An Overview and Insights into a Prospective Mainstream Anticancer Therapy

Yıl 2022, Cilt: 9 Sayı: 3, 821 - 848, 31.08.2022

Vidujith Vithanage Jayasinghe C.d. Costa M.d.p. De. Senthilnithy Rajendram

https://doi.org/10.18596/jotcsa.1000980

Öz

Photodynamic therapy (PDT) procedure has minimum invasiveness in contrast to conventional anticancer surgical procedures. Although clinically approved a few decades ago, it is not commonly used due to its poor efficacy, mainly due to poor light penetration into deeper tissues. PDT uses a photosensitizer (PS), which is photoactivated on illumination by light of appropriate wavelength and oxygen in the tissue, leading to a series of photochemical reactions producing reactive oxygen species (ROS) triggering various mechanisms resulting in lethal effects on tumor cells. This review looks into the fundamental aspects of PDT, such as photochemistry, photobiological effects, and the current clinical applications in the light of improving PDT to become a mainstream therapeutic procedure against a broad spectrum of cancers and malignant lesions. The side effects of PDT, both early and late-onset, are elaborated on in detail to highlight the available options to minimize side effects without compromising therapeutic efficacy. This paper summarizes the benefits, drawbacks, and limitations of photodynamic therapy along with the recent attempts to achieve improved therapeutic efficacy via monitoring various cellular and molecular processes through fluorescent imagery aided by suitable biomarkers, prospective nanotechnology-based targeted delivery methods, the use of scintillating nanoparticles to deliver light to remote locations and also combining PDT with conventional anticancer therapies have opened up new dimensions for PDT in treating cancers. This review inquires and critically analyses prospective avenues in which a breakthrough would finally enable PDT to be integrated into mainstream anticancer therapy.

Anahtar Kelimeler

late-onset side effects, cell death, scintillating nanoparticles, Photodynamic therapy

Teşekkür

This paper is generously dedicated to the memory of the late Professor Ranil Dassanayake, an eminent biochemist, molecular biologist, and academician in Sri Lanka. This study did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

Kaynakça

• 1. Chiaviello A, Postiglione I, Palumbo G. Targets and Mechanisms of Photodynamic Therapy in Lung Cancer Cells: A Brief Overview. Cancers. 2011 Mar 3;3(1):1014–41.
• 2. Dougherty TJ, Gomer CJ, Henderson BW, Jori G, Kessel D, Korbelik M, et al. Photodynamic Therapy. JNCI Journal of the National Cancer Institute. 1998 Jun 17;90(12):889–905.
• 3. Abrahamse H, Hamblin MR. New photosensitizers for photodynamic therapy. Biochemical Journal. 2016 Feb 15;473(4):347–64.
• 4. Bechet D, Couleaud P, Frochot C, Viriot ML, Guillemin F, Barberi-Heyob M. Nanoparticles as vehicles for delivery of photodynamic therapy agents. Trends in Biotechnology. 2008 Nov;26(11):612–21.
• 5. Oleinick N, Morris R, Belichenko I. The role of apoptosis in response to photodynamic therapy: what, where, why, and how. Photochem Photobiol Sci. 2002 Jan 7;1(1):1–21.
• 6. Nyman ES, Hynninen PH. Research advances in the use of tetrapyrrolic photosensitizers for photodynamic therapy. Journal of Photochemistry and Photobiology B: Biology. 2004 Jan;73(1–2):1–28.
• 7. D’Hallewin MA, De Witte PA, Waelkens E, Merlevede W, Baert L. Fluorescence detection of flat bladder carcinoma in situ after intravesical instillation of hypericin. Journal of Urology. 2000 Aug;164(2):349–51.
• 8. Wang S, Bromley E, Xu L, Chen JC, Keltner L. Talaporfin sodium. Expert Opinion on Pharmacotherapy. 2010 Jan;11(1):133–40.
• 9. Kataoka H, Nishie H, Hayashi N, Tanaka M, Nomoto A, Yano S, et al. New photodynamic therapy with next-generation photosensitizers. Ann Transl Med. 2017 Apr;5(8):183.
• 10. Bonnett R, Djelal BD, Hamilton PA, Martinez G, Wierrani F. Photobleaching of 5,10,15,20-tetrakis(m-hydroxyphenyl)porphyrin (m-THPP) and the corresponding chlorin (m-THPC) and bacteriochlorin(m-THPBC). A comparative study. Journal of Photochemistry and Photobiology B: Biology. 1999 Nov;53(1–3):136–43.
• 11. Dysart JS, Singh G, Patterson MS. Calculation of Singlet Oxygen Dose from Photosensitizer Fluorescence and Photobleaching During mTHPC Photodynamic Therapy of MLL Cells¶. Photochemistry and Photobiology. 2007 May 23;81(1):196–205.
• 12. Jarvi MT, Patterson MS, Wilson BC. Insights into Photodynamic Therapy Dosimetry: Simultaneous Singlet Oxygen Luminescence and Photosensitizer Photobleaching Measurements. Biophysical Journal. 2012 Feb;102(3):661–71.
• 13. Sharwani A, Alharbi FA. Monitoring of photobleaching in photodynamic therapy using fluorescence spectroscopy. Gulf J Oncolog. 2014 Jul;1(16):79–83. PMID: 25316396.
• 14. Svanberg K, Bendsoe N, Axelesson J, Engles S, Svanberg S. Photodynamic therapy: superficial and interstitial illumination. J Biomed Opt. 2010 Jul 1;15(4):485–505.
• 15. Weersink R, Lilge L. Fluorescence in photodynamic therapy dosimetry. In: Hamblin MR, Mróz P, editors. Advances in photodynamic therapy: basic, translational, and clinical. Boston, Mass: Artech House; 2008. p. 91–110. (Artech House engineering in medicine & biology series). ISBN: 978-1-59693-277-7.
• 16. Jerjes W, Upile T, Alexander Mosse C, Hamdoon Z, Morcos M, Morley S, et al. Prospective evaluation of 110 patients following ultrasound-guided photodynamic therapy for deep seated pathologies. Photodiagnosis and Photodynamic Therapy. 2011 Dec;8(4):297–306.
• 17. de Bruijn HS, Kruijt B, van der Ploeg – van den Heuvel A, Sterenborg HJCM, Robinson DJ. Increase in protoporphyrin IX after 5-aminolevulinic acid based photodynamic therapy is due to local re-synthesis. Photochem Photobiol Sci. 2007;6(8):857.
• 18. Pogue BW, Momma T, Wu HC, Hasan T. Transient absorption changes in vivo during photodynamic therapy with pulsed-laser light. Br J Cancer. 1999 May;80(3–4):344–51.
• 19. Grecco C, Moriyama LT, Cosci A, Pratavieira S, Bagnato VS, Kurachi C. Necrosis response to photodynamic therapy using light pulses in the femtosecond regime. Lasers in medical science. 2013;28(4):1177–82.
• 20. Pogue BW, Lilge L, Patterson MS, Wilson BC, Hasan T. Absorbed photodynamic dose from pulsed versus continuous wave light examined with tissue-simulating dosimeters. Appl Opt. 1997 Oct 1;36(28):7257.
• 21. Sterenborg HJCM, Gemert MJC van. Photodynamic therapy with pulsed light sources: a theoretical analysis. Phys Med Biol. 1996 May 1;41(5):835–49.
• 22. Swartling J, Höglund OV, Hansson K, Södersten F, Axelsson J, Lagerstedt AS. Online dosimetry for temoporfin-mediated interstitial photodynamic therapy using the canine prostate as model. J Biomed Opt. 2016 Feb 17;21(2):028002.
• 23. Davidson SRH, Weersink RA, Haider MA, Gertner MR, Bogaards A, Giewercer D, et al. Treatment planning and dose analysis for interstitial photodynamic therapy of prostate cancer. Phys Med Biol. 2009 Apr 21;54(8):2293–313.
• 24. Peng TI, Chang CJ, Guo MJ, Wang YH, Yu JS, Wu HY, et al. Mitochondrion-Targeted Photosensitizer Enhances the Photodynamic Effect-Induced Mitochondrial Dysfunction and Apoptosis. Annals of the New York Academy of Sciences. 2005 May;1042(1):419–28.
• 25. Vidhyapriya P, Divya D, Manimaran B, Sakthivel N. Photoactivated [Mn(CO)3Br(μ-bpcpd)]2 induces apoptosis in cancer cells via intrinsic pathway. Journal of Photochemistry and Photobiology B: Biology. 2018 Nov;188:28–41.
• 26. Morgan WF. Non-targeted and Delayed Effects of Exposure to Ionizing Radiation: II. Radiation-Induced Genomic Instability and Bystander Effects In Vivo, Clastogenic Factors and Transgenerational Effects. Radiation Research. 2003 May;159(5):581–96.
• 27. Luksiene Z, Juzenas P, Moan J. Radiosensitization of tumours by porphyrins. Cancer Letters. 2006 Apr;235(1):40–7.
• 28. Axelsson J, Davis SC, Gladstone DJ, Pogue BW. Cerenkov emission induced by external beam radiation stimulates molecular fluorescence: Cerenkov emission stimulates molecular fluorescence. Med Phys. 2011 Jun 23;38(7):4127–32.
• 29. Kotagiri N, Sudlow GP, Akers WJ, Achilefu S. Breaking the depth dependency of phototherapy with Cerenkov radiation and low-radiance-responsive nanophotosensitizers. Nature Nanotech. 2015 Apr;10(4):370–9.
• 30. Chen W, Zhang J. Using Nanoparticles to Enable Simultaneous Radiation and Photodynamic Therapies for Cancer Treatment. J Nanosci Nanotech. 2006 Apr 1;6(4):1159–66.
• 31. Morgan NY, Kramer-Marek G, Smith PD, Camphausen K, Capala J. Nanoscintillator Conjugates as Photodynamic Therapy-Based Radiosensitizers: Calculation of Required Physical Parameters. Radiation Research. 2009 Feb;171(2):236–44.
• 32. Bulin AL, Vasil’ev A, Belsky A, Amans D, Ledoux G, Dujardin C. Modelling energy deposition in nanoscintillators to predict the efficiency of the X-ray-induced photodynamic effect. Nanoscale. 2015;7(13):5744–51.
• 33. Bulin AL, Truillet C, Chouikrat R, Lux F, Frochot C, Amans D, et al. X-ray-Induced Singlet Oxygen Activation with Nanoscintillator-Coupled Porphyrins. J Phys Chem C. 2013 Oct 17;117(41):21583–9.
• 34. Chen H, Wang GD, Chuang YJ, Zhen Z, Chen X, Biddinger P, et al. Nanoscintillator-Mediated X-ray Inducible Photodynamic Therapy for In Vivo Cancer Treatment. Nano Lett. 2015 Apr 8;15(4):2249–56.
• 35. Zhang C, Zhao K, Bu W, Ni D, Liu Y, Feng J, et al. Marriage of Scintillator and Semiconductor for Synchronous Radiotherapy and Deep Photodynamic Therapy with Diminished Oxygen Dependence. Angew Chem Int Ed. 2015 Feb 2;54(6):1770–4.
• 36. Raychaudhuri S, Willgohs E, Nguyen TN, Khan EM, Goldkorn T. Monte Carlo Simulation of Cell Death Signaling Predicts Large Cell-to-Cell Stochastic Fluctuations through the Type 2 Pathway of Apoptosis. Biophysical Journal. 2008 Oct;95(8):3559–62.
• 37. Mahlbacher GE, Reihmer KC, Frieboes HB. Mathematical modeling of tumor-immune cell interactions. Journal of Theoretical Biology. 2019 May;469:47–60.
• 38. Standish BA, Jin X, Smolen J, Mariampillai A, Munce NR, Wilson BC, et al. Interstitial Doppler optical coherence tomography monitors microvascular changes during photodynamic therapy in a Dunning prostate model under varying treatment conditions. J Biomed Opt. 2007;12(3):034022.
• 39. Johansson A, Johansson T, Thompson MS, Bendsoe N, Svanberg K, Svanberg S, et al. In vivo measurement of parameters of dosimetric importance during interstitial photodynamic therapy of thick skin tumors. J Biomed Opt. 2006;11(3):034029.
• 40. Johansson A, Soto Thompson M, Johansson T, Bendsoe N, Svanberg K, Svanberg S, et al. System for integrated interstitial photodynamic therapy and dosimetric monitoring. In: Kessel D, editor. San Jose, CA; 2005 [cited 2022 May 7]. p. 130.
• 41. Johansson A, Hjelm J, Eriksson A, Andersson-Engels S. Pre-Treatment Dosimetry for Interstitial Photodynamic Therapy. In: Therapeutic Laser Applications and Laser-Tissue Interactions II [Internet]. Munich, Germany: OSA; 2005 [cited 2022 May 7]. p. TuA1.
• 42. Johansson A, Axelsson J, Andersson-Engels S, Swartling J. Realtime light dosimetry software tools for interstitial photodynamic therapy of the human prostate: Realtime prostate-PDT dosimetry. Med Phys. 2007 Oct 19;34(11):4309–21.
• 43. Stenberg M, Thompson MS, Johansson T, Palsson S, af Klinteberg C, Andersson-Engels S, et al. Interstitial photodynamic therapy: diagnostic measurements and treatment in experimental malignant rat tumors. In: Bigio IJ, Mueller GJ, Puppels GJ, Steiner RW, Svanberg K, editors. Amsterdam, Netherlands; 2000 [cited 2022 May 7]. p. 151.
• 44. Johansson T, Soto Thompson M, Stenberg M, Klinteberg C af, Andersson-Engels S, Svanberg S, et al. Feasibility study of a system for combined light dosimetry and interstitial photodynamic treatment of massive tumors. Appl Opt. 2002 Mar 1;41(7):1462.
• 45. Soto Thompson M, Johansson A, Johansson T, Andersson-Engels S, Svanberg S, Bendsoe N, et al. Clinical system for interstitial photodynamic therapy with combined on-line dosimetry measurements. Appl Opt. 2005 Jul 1;44(19):4023.
• 46. Johansson A, Johansson T, Thompson MS, Bendsoe N, Svanberg K, Svanberg S, et al. In vivo measurement of parameters of dosimetric importance during interstitial photodynamic therapy of thick skin tumors. J Biomed Opt. 2006;11(3):034029.
• 47. Dahle J, Kaalhus O, Moan J, Steen HB. Cooperative effects of photodynamic treatment of cells in microcolonies. Proc Natl Acad Sci USA. 1997 Mar 4;94(5):1773–8.
• 48. Dahle J, Steen HB, Moan J. The Mode of Cell Death Induced by Photodynamic Treatment Depends on Cell Density. Photochem Photobiol. 1999 Sep;70(3):363–7.
• 49. Dahle J. The bystander effect in photodynamic inactivation of cells. Biochimica et Biophysica Acta (BBA) - General Subjects. 2000 Jul 26;1475(3):273–80.
• 50. Dahle J, Mikalsen SO, Rivedal E, Steen HB. Gap Junctional Intercellular Communication is not a Major Mediator in the Bystander Effect in Photodynamic Treatment of MDCK II Cells. Radiation Research. 2000 Sep;154(3):331–41.
• 51. Shamas-Din A, Kale J, Leber B, Andrews DW. Mechanisms of Action of Bcl-2 Family Proteins. Cold Spring Harbor Perspectives in Biology. 2013 Apr 1;5(4):a008714–a008714.
• 52. Kroemer G, Reed JC. Mitochondrial control of cell death. Nat Med. 2000 May;6(5):513–9.
• 53. Reed JC. Mechanisms of Apoptosis. The American Journal of Pathology. 2000 Nov;157(5):1415–30.
• 54. Oseroff AR, Ohuoha D, Ara G, McAuliffe D, Foley J, Cincotta L. Intramitochondrial dyes allow selective in vitro photolysis of carcinoma cells. Proc Natl Acad Sci USA. 1986 Dec;83(24):9729–33.
• 55. Ball DJ, Luo Y, Kessel D, Griffiths J, Brown SB, Vernon DI. The induction of apoptosis by a positively charged methylene blue derivative. Journal of Photochemistry and Photobiology B: Biology. 1998 Feb;42(2):159–63.
• 56. Pluskalová M, Pešlová G, Grebeňová D, Halada P, Hrkal Z. Photodynamic treatment (ALA-PDT) suppresses the expression of the oncogenic Bcr-Abl kinase and affects the cytoskeleton organization in K562 cells. Journal of Photochemistry and Photobiology B: Biology. 2006 Jun;83(3):205–12.
• 57. Tedesco AC, Sousa G, Zângaro RA, Silva NS, Pacheco MTT, Pacheco-Soares C, et al. Analysis of mitochondria, endoplasmic reticulum and actin filaments after PDT with AlPcS 4. Lasers in Medical Science. 2004 Mar 1;18(4):207–12.
• 58. Tsai JC, Wu CL, Chien HF, Chen CT. Reorganization of cytoskeleton induced by 5-aminolevulinic acid-mediated photodynamic therapy and its correlation with mitochondrial dysfunction. Lasers Surg Med. 2005 Jun;36(5):398–408.
• 59. Kvam E, Stokke T, Moan J. The lengths of DNA fragments light-induced in the presence of a photosensitizer localized at the nuclear membrane of human cells. Biochimica et Biophysica Acta (BBA) - Gene Structure and Expression. 1990 May;1049(1):33–7.
• 60. Akhlynina TV, Jans DA, Rosenkranz AA, Statsyuk NV, Balashova IY, Toth G, et al. Nuclear Targeting of Chlorin e6 Enhances Its Photosensitizing Activity. Journal of Biological Chemistry. 1997 Aug;272(33):20328–31.
• 61. Xue L yan, Chiu S mao, Oleinick NL. Photodynamic Therapy-Induced Death of MCF-7 Human Breast Cancer Cells: A Role for Caspase-3 in the Late Steps of Apoptosis but Not for the Critical Lethal Event. Experimental Cell Research. 2001 Feb;263(1):145–55.
• 62. Mroz P, Yaroslavsky A, Kharkwal GB, Hamblin MR. Cell Death Pathways in Photodynamic Therapy of Cancer. Cancers. 2011 Jun 3;3(2):2516–39.
• 63. Kim H, Luo Y, Li G, Kessel D. Enhanced Apoptotic Response to Photodynamic Therapy after bcl-2 Transfection. Cancer Res. 1999;59(14):3429–32.
• 64. Srivastava M, Ahmad N, Gupta S, Mukhtar H. Involvement of Bcl-2 and Bax in Photodynamic Therapy-mediated Apoptosis. Journal of Biological Chemistry. 2001 Jan;276(18):15481–8.
• 65. Duprez L, Wirawan E, Berghe TV, Vandenabeele P. Major cell death pathways at a glance. Microbes and Infection. 2009 Nov;11(13):1050–62.
• 66. Granville DJ, Carthy CM, Jiang H, Levy JG, McManus BM, Matroule JY, et al. Nuclear factor-κB activation by the photochemotherapeutic agent verteporfin. Blood. 2000 Jan 1;95(1):256–62.
• 67. Assefa Z, Vantieghem A, Declercq W, Vandenabeele P, Vandenheede JR, Merlevede W, et al. The Activation of the c-Jun N-terminal Kinase and p38 Mitogen-activated Protein Kinase Signaling Pathways Protects HeLa Cells from Apoptosis Following Photodynamic Therapy with Hypericin. Journal of Biological Chemistry. 1999 Mar;274(13):8788–96.
• 68. Danial NN, Korsmeyer SJ. Cell Death. Cell. 2004 Jan;116(2):205–19.
• 69. Lin Y, Choksi S, Shen HM, Yang QF, Hur GM, Kim YS, et al. Tumor Necrosis Factor-induced Nonapoptotic Cell Death Requires Receptor-interacting Protein-mediated Cellular Reactive Oxygen Species Accumulation. Journal of Biological Chemistry. 2004 Mar;279(11):10822–8.
• 70. Holler N, Zaru R, Micheau O, Thome M, Attinger A, Valitutti S, et al. Fas triggers an alternative, caspase-8–independent cell death pathway using the kinase RIP as effector molecule. Nat Immunol. 2000 Dec;1(6):489–95.
• 71. Maiuri MC, Zalckvar E, Kimchi A, Kroemer G. Self-eating and self-killing: crosstalk between autophagy and apoptosis. Nat Rev Mol Cell Biol. 2007 Sep;8(9):741–52.
• 72. Fingar VH. Vascular Effects of Photodynamic Therapy. Journal of Clinical Laser Medicine & Surgery. 1996 Oct;14(5):323–8.
• 73. Agostinis P, Berg K, Cengel KA, Foster TH, Girotti AW, Gollnick SO, et al. Photodynamic therapy of cancer: An update. CA: A Cancer Journal for Clinicians. 2011 Jul;61(4):250–81.
• 74. Crescenzi E, Chiaviello A, Canti G, Reddi E, Veneziani BM, Palumbo G. Low doses of cisplatin or gemcitabine plus Photofrin/photodynamic therapy: Disjointed cell cycle phase-related activity accounts for synergistic outcome in metastatic non–small cell lung cancer cells (H1299). Mol Cancer Ther. 2006 Mar;5(3):776–85.
• 75. Reginato E. Immune response after photodynamic therapy increases anti-cancer and anti-bacterial effects. WJI. 2014;4(1):1.
• 76. Preise D, Oren R, Glinert I, Kalchenko V, Jung S, Scherz A, et al. Systemic antitumor protection by vascular-targeted photodynamic therapy involves cellular and humoral immunity. Cancer Immunol Immunother. 2009 Jan;58(1):71–84.
• 77. Thong PSP, Ong KW, Goh NSG, Kho KW, Manivasager V, Bhuvaneswari R, et al. Photodynamic-therapy-activated immune response against distant untreated tumours in recurrent angiosarcoma. The Lancet Oncology. 2007 Oct;8(10):950–2.
• 78. Kabingu E, Oseroff AR, Wilding GE, Gollnick SO. Enhanced Systemic Immune Reactivity to a Basal Cell Carcinoma Associated Antigen Following Photodynamic Therapy. Clin Cancer Res. 2009 Jul 1;15(13):4460–6.
• 79. Crescenzi E, Chiaviello A, Canti G, Reddi E, Veneziani BM, Palumbo G. Low doses of cisplatin or gemcitabine plus Photofrin/photodynamic therapy: Disjointed cell cycle phase-related activity accounts for synergistic outcome in metastatic non–small cell lung cancer cells (H1299). Mol Cancer Ther. 2006 Mar;5(3):776–85.
• 80. Crescenzi E, Varriale L, Iovino M, Chiaviello A, Veneziani BM, Palumbo G. Photodynamic therapy with indocyanine green complements and enhances low-dose cisplatin cytotoxicity in MCF-7 breast cancer cells. Molecular cancer therapeutics. 2004;3(5):537–44.
• 81. Ahmad N, Feyes DK, Agarwal R, Mukhtar H. Photodynamic therapy results in induction of WAF1/CIP1/P21 leading to cell cycle arrest and apoptosis. Proc Natl Acad Sci USA. 1998 Jun 9;95(12):6977–82.
• 82. Xue L yan, He J, Oleinick NL. Promotion of photodynamic therapy-induced apoptosis by stress kinases. Cell Death Differ. 1999 Sep;6(9):855–64.
• 83. Assefa Z, Vantieghem A, Declercq W, Vandenabeele P, Vandenheede JR, Merlevede W, et al. The Activation of the c-Jun N-terminal Kinase and p38 Mitogen-activated Protein Kinase Signaling Pathways Protects HeLa Cells from Apoptosis Following Photodynamic Therapy with Hypericin. Journal of Biological Chemistry. 1999 Mar;274(13):8788–96.
• 84. Coupienne I, Piette J, Bontems S. How to Monitor NF-κB Activation After Photodynamic Therapy. In: Gomer CJ, editor. Photodynamic Therapy [Internet]. Totowa, NJ: Humana Press; 2010 [cited 2022 May 7]. p. 79–95. (Methods in Molecular Biology; vol. 635).
• 85. Karin M, Cao Y, Greten FR, Li ZW. NF-κB in cancer: from innocent bystander to major culprit. Nat Rev Cancer. 2002 Apr;2(4):301–10.
• 86. Palombella V, Rando O, Goldberg A, Maniatis T. The Ubiquitin-Proteasome Pathway is required for processing the NF-kappa B1 Precursor Protein and the Activation of NF-kappa B. Cell. 1994;78:773–85.
• 87. Chiaviello A, Paciello I, Postiglione I, Crescenzi E, Palumbo G. Combination of photodynamic therapy with aspirin in human-derived lung adenocarcinoma cells affects proteasome activity and induces apoptosis: PDT and aspirin. Cell Proliferation. 2010 Aug 30;43(5):480–93.
• 88. Uzdensky A, Kolpakova E, Juzeniene A, Juzenas P, Moan J. The effect of sub-lethal ALA-PDT on the cytoskeleton and adhesion of cultured human cancer cells. Biochimica et Biophysica Acta (BBA) - General Subjects. 2005 Feb;1722(1):43–50.
• 89. Schreiber S, Gross S, Brandis A, Harmelin A, Rosenbach-Belkin V, Scherz A, et al. Local photodynamic therapy (PDT) of rat C6 glioma xenografts with Pd-bacteriopheophorbide leads to decreased metastases and increase of animal cure compared with surgery. Int J Cancer. 2002 May 10;99(2):279–85.
• 90. Tsai T, Ji HT, Chiang PC, Chou RH, Chang WSW, Chen CT. ALA-PDT results in phenotypic changes and decreased cellular invasion in surviving cancer cells: sustained ala-pdt reduced cellular invasion. Lasers Surg Med. 2009 Apr;41(4):305–15.
• 91. Yang TH, Chen CT, Wang CP, Lou PJ. Photodynamic therapy suppresses the migration and invasion of head and neck cancer cells in vitro. Oral Oncology. 2007 Apr;43(4):358–65.
• 92. Triesscheijn M, Baas P, Schellens JHM, Stewart FA. Photodynamic Therapy in Oncology. The Oncologist. 2006 Oct 1;11(9):1034–44.
• 93. Borgia F, Giuffrida R, Caradonna E, Vaccaro M, Guarneri F, Cannavò S. Early and Late Onset Side Effects of Photodynamic Therapy. Biomedicines. 2018 Jan 29;6(1):12.
• 94. Waidelich R, Beyer W, Knchel R, Stepp H, Baumgartner R, Schrder J, et al. Whole bladder photodynamic therapy with 5-aminolevulinic acid using a white light source. Urology. 2003 Feb;61(2):332–7.
• 95. Kriegmair M, Baumgartner R, Lumper W, Waidelich R, Hofstetter A. Early clinical experience with 5-aminolevulinic acid for the photodynamic therapy of superficial bladder cancer. BJU Int. 1996 May;77(5):667–71.
• 96. Skyrme RJ, French AJ, Datta SN, Allman R, Mason MD, Matthews PN. A phase-1 study of sequential mitomycin C and 5-aminolaevulinic acid-mediated photodynamic therapy in recurrent superficial bladder carcinoma. BJU Int. 2005 Jun;95(9):1206–10.
• 97. Copper MP, Tan IB, Oppelaar H, Ruevekamp MC, Stewart FA. Meta-tetra(hydroxyphenyl)chlorin Photodynamic Therapy in Early-Stage Squamous Cell Carcinoma of the Head and Neck. Arch Otolaryngol Head Neck Surg. 2003 Jul 1;129(7):709.
• 98. Hopper C, Kübler A, Lewis H, Tan IB, Putnam G, the Foscan 01 Study Group. mTHPC-mediated photodynamic therapy for early oral squamous cell carcinoma: mTHPC in Early Oral Cancer. Int J Cancer. 2004 Aug 10;111(1):138–46.
• 99. Kübler AC, de Carpentier J, Hopper C, Leonard AG, Putnam G. Treatment of squamous cell carcinoma of the lip using Foscan-mediated Photodynamic Therapy. International Journal of Oral and Maxillofacial Surgery. 2001 Dec;30(6):504–9.
• 100. McCaughan JS, Williams TE. Photodynamic therapy for endobronchial malignant disease: A prospective fourteen-year study. The Journal of Thoracic and Cardiovascular Surgery. 1997 Dec;114(6):940–7.
• 101. Kato H. Photodynamic therapy for lung cancer — A review of 19 years’ experience. Journal of Photochemistry and Photobiology B: Biology. 1998 Feb;42(2):96–9.
• 102. Diaz-Jimenez J, Martinez-Ballarin J, Llunell A, Farrero E, Rodriguez A, Castro M. Efficacy and safety of photodynamic therapy versus Nd-YAG laser resection in NSCLC with airway obstruction. Eur Respir J. 1999 Oct 1;14(4):800.
• 103. Moghissi K, Dixon K, Stringer M, Freeman T, Thorpe A, Brown S. The place of bronchoscopic photodynamic therapy in advanced unresectable lung cancer: experience of 100 cases. European Journal of Cardio-Thoracic Surgery. 1999 Jan;15(1):1–6.
• 104. Furuse K, Fukuoka M, Kato H, Horai T, Kubota K, Kodama N, et al. A prospective phase II study on photodynamic therapy with photofrin II for centrally located early-stage lung cancer. The Japan Lung Cancer Photodynamic Therapy Study Group. JCO. 1993 Oct;11(10):1852–7.
• 105. Imamura S, Kusunoki Y, Takifuji N, Kudo S, Matsui K, Masuda N, et al. Photodynamic therapy and/or external beam radiation therapy for roentgenologically occult lung cancer. Cancer. 1994 Mar 15;73(6):1608–14.
• 106. McCaughan JS, Hicks W, Laufman L, May E, Roach R. Palliation of esophageal malignancy with photoradiation therapy. Cancer. 1984 Dec 15;54(12):2905–10.
• 107. Moghissi K, Dixon K, Thorpe JAC, Stringer M, Moore PJ. The role of photodynamic therapy (PDT) in inoperable oesophageal cancer. European Journal of Cardio-Thoracic Surgery. 2000 Feb;17(2):95–100.
• 108. Schweitzer VG, Bologna S, Batra SK. Photodynamic therapy for treatment of esophageal cancer: a preliminary report. The Laryngoscope. 1993;103(6):699–703.
• 109. Sibille A, Lambert R, Souquet JC, Sabben G, Descos F. Long-term survival after photodynamic therapy for esophageal cancer. Gastroenterology. 1995 Feb;108(2):337–44.
• 110. Grosjean P, Savary JF, Mizeret J, Wagnieres G, Woodtli A, Theumann JF, et al. Photodynamic Therapy for Cancer of the Upper Aerodigestive Tract Using Tetra( m -hydroxyphenyl)chlorin. Journal of Clinical Laser Medicine & Surgery. 1996 Oct;14(5):281–7.
• 111. Wolfsen HC. Carpe luz—seize the light: endoprevention of esophageal adenocarcinoma when using photodynamic therapy with porfimer sodium. Gastrointestinal Endoscopy. 2005 Oct;62(4):499–503.
• 112. Pacifico RJ, Wang KK, Wongkeesong L Michel, Buttar NS, Lutzke LS. Combined endoscopic mucosal resection and photodynamic therapy versus esophagectomy for management of early adenocarcinoma in Barrett’s esophagus. Clinical Gastroenterology and Hepatology. 2003 Jul;1(4):252–7.
• 113. Patel G, Armstrong AW, Eisen DB. Efficacy of Photodynamic Therapy vs Other Interventions in Randomized Clinical Trials for the Treatment of Actinic Keratoses: A Systematic Review and Meta-analysis. JAMA Dermatol. 2014 Dec 1;150(12):1281.
• 114. Chhatre S, Vachani A, Allison RR, Jayadevappa R. Survival Outcomes with Photodynamic Therapy, Chemotherapy and Radiation in Patients with Stage III or Stage IV Non-Small Cell Lung Cancer. Cancers. 2021 Feb 15;13(4):803.
• 115. Li L bo, Xie J ming, Zhang X na, Chen J zhang, Luo Y ling, Zhang L ying, et al. Retrospective study of photodynamic therapy vs photodynamic therapy combined with chemotherapy and chemotherapy alone on advanced esophageal cancer. Photodiagnosis and Photodynamic Therapy. 2010 Sep;7(3):139–43.
• 116. Rigual N, Shafirstein G, Cooper MT, Baumann H, Bellnier DA, Sunar U, et al. Photodynamic Therapy with 3-(1′-Hexyloxyethyl) Pyropheophorbide a for Cancer of the Oral Cavity. Clin Cancer Res. 2013 Dec 1;19(23):6605–13.
• 117. Wilson BC. Photodynamic Therapy for Cancer: Principles. Canadian Journal of Gastroenterology. 2002;16(6):393–6.
• 118. Gonzalgo M, Pavlovich C, Lee S, Nelson W. Prostate Cancer Detection by GSTP1 Methylation Analysis of Postbiopsy Urine Specimens. Clinical Cancer Research. 2003;9(7):2673–7.
• 119. Lane KLS, Hovenic W, Ball K, Zachary CB. Daylight photodynamic therapy: The Southern California experience: Daylight photodynamic therapy. Lasers Surg Med. 2015 Feb;47(2):168–72.
• 120. Wiegell SR, HæDERSDAL M, Christian Wulf H. Cold water and pauses in illumination reduces pain during photodynamic therapy: a randomized clinical study. Acta dermato-venereologica. 2009;89(2):145–9.
• 121. Golub TR, Slonim DK, Tamayo P, Huard C, Gaasenbeek M, Mesirov JP, et al. Molecular Classification of Cancer: Class Discovery and Class Prediction by Gene Expression Monitoring. Science. 1999 Oct 15;286(5439):531–7.
• 122. Tyagi S, Kramer FR. Molecular Beacons: Probes that Fluoresce upon Hybridization. Nat Biotechnol. 1996 Mar;14(3):303–8.
• 123. Woodhams JH, MacRobert AJ, Bown SG. The role of oxygen monitoring during photodynamic therapy and its potential for treatment dosimetry. Photochem Photobiol Sci. 2007;6(12):1246.
• 124. Hong EJ, Choi DG, Shim MS. Targeted and effective photodynamic therapy for cancer using functionalized nanomaterials. Acta Pharmaceutica Sinica B. 2016 Jul;6(4):297–307.
• 125. Calixto G, Bernegossi J, de Freitas L, Fontana C, Chorilli M. Nanotechnology-Based Drug Delivery Systems for Photodynamic Therapy of Cancer: A Review. Molecules. 2016 Mar 11;21(3):342.
• 126. Wei Y, Zhou F, Zhang D, Chen Q, Xing D. A graphene oxide based smart drug delivery system for tumor mitochondria-targeting photodynamic therapy. Nanoscale. 2016;8(6):3530–8.
• 127. James N, Cheruku R, Missert J, Sunar U, Pandey R. Measurement of Cyanine Dye Photobleaching in Photosensitizer Cyanine Dye Conjugates Could Help in Optimizing Light Dosimetry for Improved Photodynamic Therapy of Cancer. Molecules. 2018 Jul 24;23(8):1842.
• 128. Wezgowiec J, Derylo MB, Teissie J, Orio J, Rols MP, Kulbacka J, et al. Electric Field-Assisted Delivery of Photofrin to Human Breast Carcinoma Cells. J Membrane Biol. 2013 Oct;246(10):725–35.
• 129. Sahu NK, Shilakari G, Nayak A, Kohli DV. Antisense Technology: A Selective Tool for Gene Expression Regulation and Gene Targeting. Current Pharmaceutical Biotechnology. 2007;8(5):291–304.
• 130. Brown PK, Qureshi AT, Moll AN, Hayes DJ, Monroe WT. Silver Nanoscale Antisense Drug Delivery System for Photoactivated Gene Silencing. ACS Nano. 2013 Apr 23;7(4):2948–59.
• 131. Chou TC, Talalay P. Quantitative analysis of dose-effect relationships: the combined effects of multiple drugs or enzyme inhibitors. Advances in Enzyme Regulation. 1984 Jan;22:27–55.
• 132. Postiglione I, Chiaviello A, Palumbo G. Enhancing Photodynamyc Therapy Efficacy by Combination Therapy: Dated, Current and Oncoming Strategies. Cancers. 2011 Jun 9;3(2):2597–629.
• 133. Crescenzi E, Varriale L, Iovino M, Chiaviello A, Veneziani BM, Palumbo G. Photodynamic therapy with indocyanine green complements and enhances low-dose cisplatin cytotoxicity in MCF-7 breast cancer cells. Molecular Cancer Therapeutics. 2004 May 12;3(5):537–44.
• 134. Brodin NP, Guha C, Tomé WA. Photodynamic Therapy and Its Role in Combined Modality Anticancer Treatment. Technol Cancer Res Treat. 2015 Aug;14(4):355–68.
• 135. St. Denis TG, Aziz K, Waheed AA, Huang YY, Sharma SK, Mroz P, et al. Combination approaches to potentiate immune response after photodynamic therapy for cancer. Photochem Photobiol Sci. 2011;10(5):792.
• 136. Korbelik M, Sun J, Posakony JJ. Interaction Between Photodynamic Therapy and BCG Immunotherapy Responsible for the Reduced Recurrence of Treated Mouse Tumors¶. Photochemistry and Photobiology. 2007 May 1;73(4):403–9.
• 137. Korbelik M, Cecic I. Enhancement of tumour response to photodynamic therapy by adjuvant mycobacterium cell-wall treatment. Journal of Photochemistry and Photobiology B: Biology. 1998 Jul;44(2):151–8.
• 138. Chen WR, Korbelik M, Battels KE, Liu H, Sun J, Nordquist RE. Enhancement of Laser Cancer Treatment by a Chitosan-derived Immunoadjuvant. Photochemistry and Photobiology. 2007 May 23;81(1):190–5.
• 139. Korbelik M, Sun J, Cecic I, Serrano K. Adjuvant treatment for complement activation increases the effectiveness of photodynamic therapy of solid tumors. Photochem Photobiol Sci. 2004;3(8):812.
• 140. Winters U, Daayana S, Lear JT, Tomlinson AE, Elkord E, Stern PL, et al. Clinical and Immunologic Results of a Phase II Trial of Sequential Imiquimod and Photodynamic Therapy for Vulval Intraepithelial Neoplasia. Clin Cancer Res. 2008 Aug 15;14(16):5292–9.
• 141. Uehara M, Sano K, Wang ZL, Sekine J, Ikeda H, Inokuchi T. Enhancement of the photodynamic antitumor effect by streptococcal preparation OK-432 in the mouse carcinoma. Cancer Immunology, Immunotherapy. 2000 Oct 22;49(8):401–9.
• 142. Korbelik M, Sun J, Posakony JJ. Interaction Between Photodynamic Therapy and BCG Immunotherapy Responsible for the Reduced Recurrence of Treated Mouse Tumors¶. Photochemistry and Photobiology. 2007 May 1;73(4):403–9.
• 143. Korbelik M, Cecic I. Enhancement of tumour response to photodynamic therapy by adjuvant mycobacterium cell-wall treatment. Journal of Photochemistry and Photobiology B: Biology. 1998 Jul;44(2):151–8.
• 144. Korbelik M, Naraparaju V, Yamamoto N. Macrophage-directed immunotherapy as adjuvant to photodynamic therapy of cancer. Br J Cancer. 1997 Jan;75(2):202–7.
• 145. Reginato E, Mroz P, Chung H, Kawakubo M, Wolf P, Hamblin MR. Photodynamic therapy plus regulatory T-cell depletion produces immunity against a mouse tumour that expresses a self-antigen. Br J Cancer. 2013 Oct;109(8):2167–74.
• 146. Goląb J, Wilczyński G, Zagożdżon R, Stoklosa T, Dąbrowska A, Rybczyńska J, et al. Potentiation of the anti-tumour effects of Photofrin®-based photodynamic therapy by localized treatment with G-CSF. Br J Cancer. 2000 Apr;82(8):1485–91.
• 147. Jalili A, Makowski M, Świtaj T, Nowis D, Wilczyński GM, Wilczek E, et al. Effective Photoimmunotherapy of Murine Colon Carcinoma Induced by the Combination of Photodynamic Therapy and Dendritic Cells. Clin Cancer Res. 2004 Jul 1;10(13):4498–508.
• 148. Saji H, Song W, Furumoto K, Kato H, Engleman EG. Systemic Antitumor Effect of Intratumoral Injection of Dendritic Cells in Combination with Local Photodynamic Therapy. Clin Cancer Res. 2006 Apr 15;12(8):2568–74.
• 149. Luksiene Z, Kalvelyte A, Supino R. On the combination of photodynamic therapy with ionizing radiation. Journal of Photochemistry and Photobiology B: Biology. 1999 Oct;52(1–3):35–42.
• 150. Allman R, Cowburn P, Mason M. Effect of photodynamic therapy in combination with ionizing radiation on human squamous cell carcinoma cell lines of the head and neck. Br J Cancer. 2000 Sep;83(5):655–61.
• 151. Lehmann P. Methyl aminolaevulinate?photodynamic therapy: a review of clinical trials in the treatment of actinic keratoses and nonmelanoma skin cancer. Br J Dermatol. 2007 May;156(5):793–801.
• 152. Nakano A, Watanabe D, Akita Y, Kawamura T, Tamada Y, Matsumoto Y. Treatment efficiency of combining photodynamic therapy and ionizing radiation for Bowen’s disease: Combination of PDT and radiation for Bowen’s disease. Journal of the European Academy of Dermatology and Venereology. 2011 Apr;25(4):475–8.
• 153. Wang J, Hyun W, Lamborn K, Deen D. Measurement of Radiation-induced Damage in Human Glioma Cells with Flow Cytometry. Cancer Research. 1996;56(1):154–7.
• 154. Sanfilippo NJ, Hsi A, DeNittis AS, Ginsberg GG, Kochman ML, Friedberg JS, et al. Toxicity of photodynamic therapy after combined external beam radiotherapy and intraluminal brachytherapy for carcinoma of the upper aerodigestive tract. Lasers Surg Med. 2001;28(3):278–81.
• 155. Xu J, Gao J, Wei Q. Combination of Photodynamic Therapy with Radiotherapy for Cancer Treatment. Journal of Nanomaterials. 2016;2016:1–7.
• 156. Chen W, Zhang J. Using Nanoparticles to Enable Simultaneous Radiation and Photodynamic Therapies for Cancer Treatment. J Nanosci Nanotech. 2006 Apr 1;6(4):1159–66.
• 157. Juzenas P, Chen W, Sun YP, Coelho MAN, Generalov R, Generalova N, et al. Quantum dots and nanoparticles for photodynamic and radiation therapies of cancer. Advanced Drug Delivery Reviews. 2008 Dec;60(15):1600–14.
• 158. Ran C, Zhang Z, Hooker J, Moore A. In Vivo Photoactivation Without “Light”: Use of Cherenkov Radiation to Overcome the Penetration Limit of Light. Mol Imaging Biol. 2012 Apr;14(2):156–62.
• 159. Allman R, Cowburn P, Mason M. Effect of photodynamic therapy in combination with ionizing radiation on human squamous cell carcinoma cell lines of the head and neck. Br J Cancer. 2000 Sep;83(5):655–61.
• 160. Sharma P, Farrell T, Patterson MS, Singh G, Wright JR, Sur R, et al. In Vitro Survival of Nonsmall Cell Lung Cancer Cells Following Combined Treatment with Ionizing Radiation and Photofrin-mediated Photodynamic Therapy. Photochemistry and Photobiology. 2009 Jan;85(1):99–106.
• 161. Nakano A, Watanabe D, Akita Y, Kawamura T, Tamada Y, Matsumoto Y. Treatment efficiency of combining photodynamic therapy and ionizing radiation for Bowen’s disease: Combination of PDT and radiation for Bowen’s disease. Journal of the European Academy of Dermatology and Venereology. 2011 Apr;25(4):475–8.
• 162. Sazgarnia A, Montazerabadi AR, Bahreyni-Toosi MH, Ahmadi A, Aledavood A. In vitro survival of MCF-7 breast cancer cells following combined treatment with ionizing radiation and mitoxantrone-mediated photodynamic therapy. Photodiagnosis and Photodynamic Therapy. 2013 Feb;10(1):72–8.
• 163. Ahn JC, Biswas R, Mondal A, Lee YK, Chung PS. Cisplatin enhances the efficacy of 5-Aminolevulinic acid mediated photodynamic therapy in human head and neck squamous cell carcinoma. gpb. 2014;33(01):53–62.
• 164. Wei XQ, Ma HQ, Liu AH, Zhang YZ. Synergistic Anticancer Activity of 5-Aminolevulinic Acid Photodynamic Therapy in Combination with Low-dose Cisplatin on Hela Cells. Asian Pacific Journal of Cancer Prevention. 2013 May 30;14(5):3023–8.
• 165. Cheung KKY, Chan JYW, Fung KP. Antiproliferative effect of pheophorbide a–mediated photodynamic therapy and its synergistic effect with doxorubicin on multiple drug-resistant uterine sarcoma cell MES-SA/Dx5. Drug and Chemical Toxicology. 2013 Oct;36(4):474–83.
• 166. Sun W, Kajimoto Y, Inoue H, Miyatake SI, Ishikawa T, Kuroiwa T. Gefitinib enhances the efficacy of photodynamic therapy using 5-aminolevulinic acid in malignant brain tumor cells. Photodiagnosis and Photodynamic Therapy. 2013 Feb;10(1):42–50.
• 167. Fang X, Wu P, Li J, Qi L, Tang Y, Jiang W, et al. Combination of apoptin with photodynamic therapy induces nasopharyngeal carcinoma cell death in vitro and in vivo. Oncology Reports. 2012 Dec;28(6):2077–82.
• 168. Nonaka Y, Nanashima A, Nonaka T, Uehara M, Isomoto H, Abo T, et al. Synergic effect of photodynamic therapy using talaporfin sodium with conventional anticancer chemotherapy for the treatment of bile duct carcinoma. Journal of Surgical Research. 2013 May;181(2):234–41.
• 169. Tong Z Sheng, Miao P Tian, Liu T Ting, Jia Y Sheng, Liu X Dong. Enhanced antitumor effects of BPD-MA-mediated photodynamic therapy combined with adriamycin on breast cancer in mice. Acta Pharmacol Sin. 2012 Oct;33(10):1319–24.
• 170. Diez B, Ernst G, Teijo MJ, Batlle A, Hajos S, Fukuda H. Combined chemotherapy and ALA-based photodynamic therapy in leukemic murine cells. Leukemia Research. 2012 Sep;36(9):1179–84.
• 171. Canti G, Calastretti A, Bevilacqua A, Reddi E, Palumbo G, Nicolin A. Combination of photodynamic therapy + immunotherapy + chemotherapy in murine leukiemia. neo. 2010 Jan;57(2):184–8.
• 172. Kramarenko GG, Wilke WW, Dayal D, Buettner GR, Schafer FQ. Ascorbate enhances the toxicity of the photodynamic action of Verteporfin in HL-60 cells. Free Radical Biology and Medicine. 2006 May;40(9):1615–27.
• 173. Melnikova V, Bezdetnaya L, Belitchenko I, Potapenko A, Merlin JL, Guillemin F. Meta-tetra(hydroxyphenyl)chlorin-sensitized photodynamic damage of cultured tumor and normal cells in the presence of high concentrations of α-tocopherol. Cancer Letters. 1999 May;139(1):89–95.