Photodynamic activity of the dye methylene blue on murine melanoma cells
Abstract
Melanoma is an aggressive malignant tumor that is resistant to chemo- and radiotherapy. Taking into account that the mechanism of photodynamic damage significantly differs from the mechanism of cell destruction by cytotoxic drugs or ionizing radiation, it can be assumed that melanoma damage can be achieved with the help of photodynamic therapy.
The study was performed on murine melanoma cell line B16F10. Methylene blue (MB) dye was used as a photosensitizer (PS) because of its known affinity to the melanoma cell pigment – melanin.
It has been found that B16F10 cells possess sensitivity to photodynamic therapy with MB. But this effect was significantly lower than for tumor cells that lack multiple drug resistance phenotype (human transformed T-cell line Jurkat). It was shown that the photodynamic activity of MB in relation to melanoma cells can be increased by creating of its composite with gold nanoparticles (GNP), in the synthesis of which tetrachloroaurate reduction was made by sodium citrate, but not by poloxamer Pluronic F127.
After the sensitization of melanoma cells with MB in composition with citrate GNPs and subsequent laser irradiation, twofold increase of cell death was achieved in comparison with free MB used in the same concentration. The MB composite with GNPs, synthesized with the presence of Pluronic F127, on the contrary, after light exposure led to the elimination of a slightly reduced number of cells compared to free MB. This effect can be evidently explained by the partial reduction of the MB to the colorless leuko-form by the pluronic F127, which remained in the solution of GNP after their washing by centrifugation.
The effect of natural polysaccharide chitosan on photodynamic activity of MB was also studied. It has been shown that the use of chitosan together with MB increased the accumulation of PS in melanoma cells, which led to the elimination of 96% of irradiated cells.
Thus, murine melanoma cell line B16F10 exhibits sensitivity to photodynamic therapy with MB. The susceptibility of melanoma cells to this treatment is significantly reduced in comparison with the sensitivity of tumor cells, which do not have the phenotype of multiple drug resistance (transformed human T-cell line Jurkat). Nanocomposite PS based on citrate GNPs and MB demonstrated twice higher photodynamic activity with the respect to melanoma cells in comparison to free MB at the same concentration. Natural polysaccharide chitosan increased the accumulation of MB in melanoma cells, which allowed achieving cell mortality up to 96% after irradiation of the samples with laser light on a wavelength of 658 nm.
Downloads
References
Alakhova D.Y. Pluronics and MDR reversal: An update / D.Y.Alakhova, A.V.Kabanov // Mol. Pharm. – 2014. – Vol. 11, № 8. – P. 2566-2578.
Bhattacharya R. Biological properties of «naked» metal nanoparticles / R.Bhattacharya, P.Mukherjee // Adv. Drug Deliv. Rev. – 2008. – Vol. 60. – P. 1289-1306.
Bombelli F.B. The scope of nanoparticle therapies for future metastatic melanoma treatment / F.B.Bombelli, C.A.Webster, M.Moncrieff, V.Sherwood // Lancet Oncol. – 2014. – Vol. 15, № 1. – P. e22-e32.
Camerin M. The in vivo efficacy of phthalocyaninenanoparticle conjugates for the photodynamic therapy of amelanotic melanoma / M.Camerin, M.Magaraggia, M.Soncin et al. // Eur. J. Cancer.- 2010. – Vol. 46, № 10. – P. 1910-1918.
Camerin M. Delivery of a hydrophobic phthalocyanine photosensitizer using PEGylated gold nanoparticle conjugates for the in vivo photodynamic therapy of amelanotic melanoma / M.Camerin, M.Moreno, M.J.Marín et al. // Photochem. Photobiol. Sci. – 2016. – Vol. 15, № 5. – P. 889-905.
Chang C.-J. In vitro and in vivo photosensitizing applications of Photofrin in malignant melanoma cells / C.-J.Chang, J.-S.Yu, F.-C.Wei // Chang Gung Med. J. – 2008. – Vol. 31, № 3. – P. 260-267.
Davids L.M. Combating melanoma: The use of photodynamic therapy as a novel, adjuvant therapeutic tool / L.M.Davids, B.Kleemann // Cancer Treat. Rev. – 2010. – Vol. 37, № 6. – P. 465-75.
Gamaleia N. F. Photodynamic activity of hematoporphyrin conjugates with gold nanoparticles : Experimentsinvitro / N.F.Gamaleia, E.D.Shishko, G.A.Dolinsky et al. // Exp. Oncol. – 2010. – Vol. 32, № 1. – P. 44-47.
Gorzelanny C. Specific interaction between chitosan and matrix metalloprotease 2 decreases the invasive activity of human melanoma cells / C.Gorzelanny, B.Pöppelmann, E.Strozyk et al. // Biomacromolecules. – 2007. – Vol. 8, № 10. – P. 3035-3040.
Huang X. Gold nanoparticles: Optical properties and implementations in cancer diagnosis and photothermal therapy / X.Huang, M.El-Sayed // J. Adv. Res. – 2010. – Vol. 1, № 1. – P. 13-28.
Jain P.K. Au nanoparticles target cancer / P.K.Jain, I.H.El-Sayed, M.A.El-Sayed // Nano Today. – 2007. – Vol. 2, № 1. – P. 18-29.
Kawczyk-Krupka A. Photodynamic therapy in treatment of cutaneous and choroidal melanoma / A.Kawczyk-Krupka, A.M.Bugaj, W.Latos et al. // Photodiagnosis Photodyn. Ther. – 2013. – Vol. 10, № 4. – P. 503-509.
Link E.M. Targeting melanoma with 211At/31Jmethylene blue. Preclinical and clinical experience // Hybridoma. – 1999. – Vol.1 8, № 1. – P. 77-82.
Link E. M. Uptake and therapeutic effectiveness of 125I- and 211At-methylene blue for pigmented melanoma in an animal model system / E.M.Link, I.Brown, R.N.Carpenter, J.S.Mitchell // Cancer Res. – 1989. – Vol. 49, № 15. – P. 4332-4337.
Mbakidi J.P. Hydrophilic chlorin-conjugated magnetic nanoparticles — potential anticancer agent for the treatment of melanoma by PDT / J.P.Mbakidi, N.Drogat, R.Granet et al. // Bioorg. Med. Chem. Lett. – 2013. – Vol. 23, № 9. – P. 2486-2490.
Muanprasat C. Chitosan oligosaccharide: biological activities and potential therapeutic applications / C.Muanprasat, V.Chatsudthipong // Pharmacol. Ther. – 2017. – Vol. 170. – P. 80-97.
Razzaq H. Interaction of gold nanoparticles with free radicals and their role in enhancing the scavenging activity of ascorbic acid / H.Razzaq, F.Saira, A.Yaqub et al. // J. Photochem. Photobiol. B Biol. – 2016. – Vol. 161. – P. 266-272.
Rigon R.B. Nanotechnology-based drug delivery systems for melanoma antitumoral therapy: A review / R.B.Rigon, M.H.Oyafuso, A.T.Fujimura et al. // Biomed Res. Int. – 2015. – Article ID 841817, 22 p.; http://dx.doi.org/10.1155/2015/841817.
Schmidt T.F. Binding of methylene blue onto Langmuir monolayers representing cell membranes may explain its efficiency as photosensitizer in photodynamic therapy / T.F.Schmidt, L.Caseli, O.N.Oliveira, R.Itri // Langmuir. – 2015. – Vol. 31, № 14. – P. 4205-4212.
Simon T. LED-activated methylene blueloaded Pluronic-nanogold hybrids for in vitro photodynamic therapy / T.Simon, S.Boca-Farcau, A.-M.Gabudean et al. // J. Biophotonics. – 2013. – Vol. 6, № 11-12. – P. 950-959.
Singh B. Updates in therapy for advanced melanoma / B.Singh, A.Salama // Cancers (Basel). – 2016. – Vol. 8, № 1. – P. 17.
Sobal G. Radioiodinated methylene blue – a promising agent for melanoma scintigraphy: Labelling, stability and in vitro uptake by melanoma cells / G.Sobal, M.Rodrigues, H.Sinzinger // Anticancer Res. – 2008. – Vol. 28, № 6A. – P. 3691-3693.
Tardivo J.P. Methylene blue in photodynamic therapy: from basic mechanisms to clinical applications / J.P.Tardivo, A. Del Giglio, C.S. de Oliveira et al. // Photodiagnosis Photodyn. Ther. – 2005. – Vol. 2, № 3. – P. 175-191.
Verdier M. Photodynamic treatment induces cell death by apoptosis or autophagy depending on the melanin content in two B16 melanoma cell lines / M.Verdier, S.Bellaton, T.Naves et al. // Oncol. Rep. – 2012. – Vol. 29, № 3. – P. 1196-200.
