Highly Selective Photodynamic Therapy with a Short Drug-Light Interval Using a Cytotoxic Photosensitizer Porphyrus Envelope for Drug-Resistant Prostate Cancer Cells — Oak Academic Publishing
Research ArticleOpen AccessGoogle Scholar indexed
Highly Selective Photodynamic Therapy with a Short Drug-Light Interval Using a Cytotoxic Photosensitizer Porphyrus Envelope for Drug-Resistant Prostate Cancer Cells
Graduate School of Engineering, Osaka University, Osaka, Japan
,
Graduate School of Frontier Biosciences, Osaka University, Osaka, Japan
,
Institute of Academic Initiatives, Osaka University, Osaka, Japan
,
Graduate School of Engineering, Osaka University, Osaka, Japan
,
Institute of Innovative Research, Tokyo Institute of Technology, Kanagawa, Japan
,
Institute of Innovative Research, Tokyo Institute of Technology, Kanagawa, Japan
,
Graduate School of Medicine, Osaka University, Osaka, Japan
,
Graduate School of Medicine, Osaka University, Osaka, Japan
,
Global Centre for Medical Engineering and Informatics, Osaka University, Osaka, Japan
1 Graduate School of Engineering, Osaka University, Osaka, Japan
2 Graduate School of Frontier Biosciences, Osaka University, Osaka, Japan
3 Institute of Academic Initiatives, Osaka University, Osaka, Japan
4 Graduate School of Engineering, Osaka University, Osaka, Japan
5 Institute of Innovative Research, Tokyo Institute of Technology, Kanagawa, Japan
6 Institute of Innovative Research, Tokyo Institute of Technology, Kanagawa, Japan
7 Graduate School of Medicine, Osaka University, Osaka, Japan
8 Graduate School of Medicine, Osaka University, Osaka, Japan
9 Global Centre for Medical Engineering and Informatics, Osaka University, Osaka, Japan
Background: Photodynamic therapy (PDT) is a less invasive cancer treatment using photochemical reactions induced by light irradiation to a photosensitizer (PS). Highly selective PDT with fast accumulation of the PS in target site might be a promising treatment option for drug-resistant prostate cancer facing high incidence rate of elderly men who have no effective treatment options and require a minimally invasive treatment. Hemagglutinating virus of Japan envelope (HVJ-E) allows selective and fast drug delivery to the drug-resistant prostate cancer cells via rapid cell membrane fusion. PS named porphyrus envelope (PE) has been developed by insertion of lipidated protoporphyrin IX (PpIX lipid) into HVJ-E. In this study, we investigated the optimal conditions for PE preparation and laser irradiation for highly selective PDT using PE with a short drug-light interval. Materials and Methods: Human hormon refractory prostate cancer cell line PC-3 and human normal prostate epithelial cell line PNT2 were cultured. PpIX lipid uptake and cytotoxicity of PDT in the cells incubated with PE for 10 min were evaluated by measuring fluorescence intensity and by using a cell counting reagent 24 h after PDT, respectively. Results: PpIX lipid uptake and cytotoxicity of PDT were increased with PpIX lipid concentration. Cytotoxicity of PDT using PE was more than 9 times as strong as that with PpIX lipid and PpIX induced by 5-aminolevulinic acid. Much stronger cytotoxicity was induced in PC-3 cells than PNT2 cells with the ratio of cell death rate for cancer to normal cells up to 4.64 ± 0.09. Conclusions: Fast PS delivery with HVJ-E allows highly selective PDT with a short drug-light interval. Therefore, PDT using PE has a potential to shorten treatment period and reduce side effects of PDT.
KeywordsPhotodynamic TherapyHemagglutinating Virus of Japan EnvelopeDrug Delivery SystemShort Drug-Light IntervalDrug-Resistant Prostate Cancer
Quon, H., Loblaw, A. and Nam, R. (2011) Dramatic Increase in Prostate Cancer Cases by 2021. BJU International, 108, 1734-1738. https://doi.org/10.1111/j.1464-410X.2011.10197.x
Fuessel, S., Meye, A., Schmitz, M., Zastrow, S., Linné, C., Richter, K., Löbel, B., Hakenberg, O.W., Hoelig, K., Rieber, E.P. and Wirth, M.P. (2006) Vaccination of Hormone-Refractory Prostate Cancer Patients with Peptide Cocktail-Loaded Dendritic Cells: Results of a Phase I Clinical Trial. The Prostate, 66, 811-821. https://doi.org/10.1002/pros.20404
Bhandari, M.S., Petrylak, D.P. and Hussain, M. (2005) Clinical Trials in Metastatic Prostate Cancer—Has There Been Real Progress in the Past Decade? European Journal of Cancer, 41, 941-953. https://doi.org/10.1016/j.ejca.2005.02.008
Baier, J., Maier, M., Engl, R., Landthaler, M. and Bäumler, W. (2005) Time-Resolved Investigations of Singlet Oxygen Luminescence in Water, in Phosphatidylcholine, and in Aqueous Suspensions of Phosphatidylcholine or HT29 Cells. The Journal of Physical Chemistry B, 109, 3041-3046. https://doi.org/10.1021/jp0455531
Ethirajan, M., Chen, Y., Joshi, P. and Pandey, R.K. (2011) The Role of Porphyrin Chemistry in Tumor Imaging and Photodynamic Therapy. Chemical Society Reviews, 40, 340-362. https://doi.org/10.1039/B915149B
Usuda, J., Kato, H., Okunaka, T., Furukawa, K., Tsutsui, H., Yamada, K., Suga, Y., Honda, H., Nagatsuka, Y., Ohira, T., Tsuboi, M. and Hirano, T. (2006) Photodynamic Therapy (PDT) for Lung Cancers. Journal of Thoracic Oncology, 1, 489-493. https://doi.org/10.1016/S1556-0864(15)31616-6
Trachtenberg, J., Bogaards, A., Weersink, R.A., Haider, M.A., Evans, A., McCluskey, S.A., Scherz, A., Gertner, M.R., Yue, C., Appu, S., Aprikian, A., Savard, J., Wilson, B.C. and Elhilali, M. (2007) Vascular Targeted Photodynamic Therapy with Palladium-Bacteriopheophorbide Photosensitizer for Recurrent Prostate Cancer Following Definitive Radiation Therapy: Assessment of Safety and Treatment Response. The Journal of Urology, 178, 1974-1979. https://doi.org/10.1016/j.juro.2007.07.036
Trachtenberg, J., Weersink, R.A., Davidson, S.R.H., Haider, M.A., Bogaards, A., Gertner, M.R., Evans, A., Scherz, A., Savard, J., Chin, J.L., Wilson, B.C. and Elhilali, M. (2008) Vascular-Targeted Photodynamic Therapy (Padoporfin, WST09) for Recurrent Prostate Cancer after Failure of External Beam Radiotherapy: A Study of Escalating Light Doses. BJU International, 102, 556-562. https://doi.org/10.1111/j.1464-410X.2008.07753.x
Xua, D.D., Lamb, H.M., Hoevenc, R., Xu, C.B., Leung, A.W.N. and Cho, W.C.S. (2013) Photodynamic Therapy Induced Cell Death of Hormone Insensitive Prostate Cancer PC-3 Cells with Autophagic Characteristics. Photodiagnosis and Photodynamic Therapy, 10, 278-287. https://doi.org/10.1016/j.pdpdt.2013.01.002
Allison, R.R., Downie, G.H., Cuenca, R., Hu, X.H., Childs, C.J. and Sibata, C.H. (2004) Photosensitizers in Clinical PDT. Photodiagnosis and Photodynamic Therapy, 1, 27-42. https://doi.org/10.1016/S1572-1000(04)00007-9
Goldman, M.P., Fitzpatrick, R.E., Ross, E.V., Kilmer, S.L. and Weiss, R.A. (2013) Lasers and Energy Devices for the Skin. CRC Press Llc., Florida. https://doi.org/10.3109/9781841849348
Jang, Y.H., Lee, D.J., Shin, J., Kang, H.Y., Lee, E.S. and Kim, Y.C. (2013) Photodynamic Therapy with Ablative Carbon Dioxide Fractional Laser in Treatment of Actinic Keratosis. Annals of Dermatology, 25, 417-422. https://doi.org/10.5021/ad.2013.25.4.417
Kaneda, Y., Yamamoto, S. and Nakajima, T. (2005) Development of HVJ Envelope Vector and Its Application to Gene Therapy. Advances in Genetics, 53, 307-332. https://doi.org/10.1016/S0065-2660(05)53012-8
Mima, H., Yamamoto, S., Ito, M., Tomoshige, R., Tabata, Y., Tamai, K. and Kaneda, Y. (2006) Targeted Chemotherapy against Intraperitoneally Disseminated Colon Carcinoma Using a Cationized Gelatin-Conjugated HVJ Envelope Vector. Molecular Cancer Therapeutics, 5, 1021-1028. https://doi.org/10.1158/1535-7163.MCT-05-0352
Kaneda, Y. (2012) Virosome: A Novel Vector to Enable Multi-Modal Strategies for Cancer Therapy. Advanced Drug Delivery Reviews, 64, 730-738. https://doi.org/10.1016/j.addr.2011.03.007
Tsurudome, M. (1999) Analyses of Paramyxovirus Glycoproteins Involved in the Induction of Cell Fusion. Uirusu, 49, 61-70. https://doi.org/10.2222/jsv.49.61
Kawaguchi, Y., Miyamoto, Y., Inoue, T. and Kaneda, Y. (2009) Efficient Eradication of Hormone-Resistant Human Prostate Cancers by Inactivated Sendai Virus Particle. International Journal of Cancer, 124, 2478-2487. https://doi.org/10.1002/ijc.24234
Kim, J. and Okada, Y. (1982) Morphological Changes in Ehrlich Ascites Tumor Cells during the Cell Fusion Reaction with HVJ (Sendai Virus): III. Morphological Characterization of HVJ Glycoproteins Integrated into the Plasma Membrane and Their Internalization by Coated Vesicles. Experimental Cell Research, 140, 127-136. https://doi.org/10.1016/0014-4827(82)90164-1
Kim, J., Santos, O.A. and Park, J.H. (2014) Selective Photosensitizer Delivery into Plasma Membrane for Effective Photodynamic Therapy. Journal of Controlled Release, 191, 98-104. https://doi.org/10.1016/j.jconrel.2014.05.049
Tachikawa, S., El-Zaria, M.E., Inomata, R., Sato, S. and Nakamura, H. (2014) Synthesis of Protoporphyrin-Lipids and Biological Evaluation of Micelles and Liposomes. Bioorganic & Medicinal Chemistry, 22, 4745-4751. https://doi.org/10.1016/j.bmc.2014.07.003
Yamauchi, M., Honda, N., Hazama, H., Tachikawa, S., Nakamura, H., Kaneda, Y. and Awazu, K. (2014) A Novel Photodynamic Therapy for Drug-Resistant Prostate Cancer Cells using Porphyrus Envelope as a Novel Photosensitizer. Photodiagnosis and Photodynamic Therapy, 11, 48-54. https://doi.org/10.1016/j.pdpdt.2013.10.001
Inai, M., Ymauchi, M., Honda, N., Hazama, H., Tachikawa, S., Nakamura, H., Nishida, T., Yasuda, H., Kaneda, Y. and Awazu, K. (2015) Hemagglutinating Virus of Japan Envelope (HVJ-E) Allows Targeted and Efficient Delivery of Photosensitizer for Photodynamic Therapy against Advanced Prostate Cancer. Proceedings of Optics in the Life Sciences 2015, Vancouver, 12-15 April 2015, OM2D.3.
Inai, M., Honda, N., Hazama, H., Akter, S., Fuse, S., Nakamura, H., Nishikawa, T., Kaneda, Y. and Awazu, K. (2017) Photodynamic Therapy using a Cytotoxic Photosensitizer Porphyrus Envelope That Targets the Cell Membrane. Photodiagnosis and Photodynamic Therapy, 20, 238-245. https://doi.org/10.1016/j.pdpdt.2017.10.017
Andrejevic-Blant, S., Hadjur, C.H., BalIini, J.P., Wagnieres, G., Fontolliet, C.H., Van Den Bergh, H. and Monnier, P.H. (1997) Photodynamic Therapy of Early Squamous Cell Carcinoma with Tetra(M-Hydroxyphenyl)Chlorin: Optimal Drug-Light Interval. British Journal of Cancer, 76, 1021-1028. https://doi.org/10.1038/bjc.1997.502
D’Hallewin, M.A., Kochetkov, D., Viry-Babel, Y., Leroux, A., Werkmeister, E., Dumas, D., Gräfe, S., Zorin, V., Guillemin, F. and Bezdetnaya, L. (2008) Photodynamic Therapy with Intratumoral Administration of Lipid-Based mTHPC in a Model of Breast Cancer Recurrence. Lasers in Surgery and Medicine, 40, 543-549. https://doi.org/10.1002/lsm.20662
Matsushima-Miyagi, T., Hatano, K., Nomura, M., Li-Wen, L., Nishikawa, T., Saga, K., Shimbo, T. and Kaneda, Y. (2012) TRAIL and Noxa Are Selectively Upregulated in Prostate Cancer Cells Downstream of the RIG-I/MAVS Signaling Pathway by Nonreplicating Sendai Virus Particles. Clinical Cancer Research, 18, 6271-6283. https://doi.org/10.1158/1078-0432.CCR-12-1595
Iinuma, S., Farshi, S.S., Ortel, B. and Hasan, T. (1994) A Mechanistic Study of Cellular Photodestruction with 5-Aminolaevulinic Acid-Induced Porphyrin. British Journal of Cancer, 70, 21-28. https://doi.org/10.1038/bjc.1994.244
Colasanti, A., Kisslinger, A., Quarto, M. and Riccio, P. (2004) Combined Effects of Radiotherapy and Photodynamic Therapy on an in Vivo Human Prostate Model. ActaBiochimicaPolonica, 51, 1039-1046.
Lin, T.Y., Guo, W., Long, Q., Ma, A., Liu, Q., Zhang, H., Huang, Y., Chandrasekaran, S., Pan, C., Lam, K.S. and Li, Y. (2016) HSP90 Inhibitor Encapsulated Photo-Theranostic Nanoparticles for Synergistic Combination Cancer Therapy. Theranostics, 6, 1324-1335. https://doi.org/10.7150/thno.14882
Nakajima, T., Itai, T., Wada, H., Yamauchi, T., Kiyohara, E. and Kaneda, Y. (2013) A Novel Therapy for Melanoma and Prostate Cancer using a Non-Replicating Sendai Virus Particle (HVJ-E). In: Wei, M. and Good, D., Eds., Novel Gene Therapy Approaches, Intech, London, 157-181. https://doi.org/10.5772/55014
Fujita, K., Nakai, Y., Kawashima, A., Ujike, T., Nagahara, A., Nakajima, T., Inoue, T., Lee, C.M., Uemura, M., Miyagawa, Y., Kaneda, Y. and Nonomura, N. (2017) Phase I/II Clinical Trial to Assess Safety and Efficacy of Intratumoral and Subcutaneous Injection of HVJ-E in Castration-Resistant Prostate Cancer Patients. Cancer Gene Therapy, 24, 277-281. https://doi.org/10.1038/cgt.2017.15
Foster, T.H., Giesselman, B.R., Hu, R., Kenney, M.E. and Mitra, S. (2010) Intratumor Administration of the Photosensitizer Pc 4 Affords Photodynamic Therapy Efficacy and Selectivity at Short Drug-Light Intervals. Translational Oncology, 3, 135-141. https://doi.org/10.1593/tlo.09295
Mannino, S., Molinari, A., Sabatino, G., Ciafrè, S.A., Colonel, M., Maira, G., Anile, C., Arancia, G. and Mangiola, A. (2008) Intratumoral vs. Systemic Administration of Meta-Tetrahydroxyphenylchlorin for Photodynamic Therapy of Malignant Gliomas: Assessment of Uptake and Spatial Distribution in C6 Rat Glioma Model. International Journal of Immunopathology and Pharmacology, 21, 227-231. https://doi.org/10.1177/039463200802100126
Anatelli, F., Mroz, P., Liu, Q., Yang, C., Castano, A.P., Swietlik, E. and Hamblin, M.R. (2006) Macrophage-Targeted Photosensitizer Conjugate Delivered by Intratumoral Injection. Molecular Pharmaceutics, 3, 654-664. https://doi.org/10.1021/mp060024y
Goins, B., Phillips, W.T. and Bao, A. (2016) Strategies for Improving the Intratumoral Distribution of Liposomal Drugs in Cancer Therapy. Expert Opinion on Drug Delivery, 13, 873-889.