tetracationic porphyrins; photo therapy; breast cacer
Abstract :
[en] Photodynamic therapy (PDT) is an alternative to conventional chemotherapy for the treatment of several types of cancer. Its advantages are reduced side effects and development of resistance mechanisms. In this work, we evaluated the photosensitization capabilities of 5,10,15,20-tetrakis[4-(pyridinium-1-yl-methyl)phenyl]porphyrin, its N-confused isomer and tow if its neutral precursors. The results were compared with the ones obtained with the cationic 5,10,15,20-tetrakis(1-methylpyridinium-4-yl)porphyrin (TMPyP) used as positive control. Both regular porphyrin derivatives showed higher efficiency to generate singlet oxygen than TMPyP. Next, we demonstrated that one of the cationic porphyrin is an efficient photosentitizer kills MCF7 breast cancer cells. The study of the cell death mechanisms induced by the photodynamic process showed that 5,10,15,20-tetrakis[4-(pyridinium-1-yl-methyl)phenyl]porphyrin and TMPyP caused cell death by autophagic flux and necrosis.
Disciplines :
Biochemistry, biophysics & molecular biology
Author, co-author :
Gamelas, Sara; University of Aveiro > Deparment of Chemistry > LAQV-REQUIMTE
Moura, Nuno; University of Aveiro > Department of Chemistry > LAQV-REQUIMTE
Habraken, Yvette ; Université de Liège - ULiège > GIGA Molecul. Biolog. of Diseases - Gene Expression & Cancer
Piette, Jacques; University of Liege - ULiege > GIGA-MBD > Virology and Immunology
Neves, Maria; University of Aveiro > Department of Chemistry > LAQV-REQUIMTE
Faustino, Maria; University of Aveiro > Department of Chemistry > LAQV-REQUIMTE
Language :
English
Title :
Tetracationic porphyrin derivatives against human breast cancer
Alternative titles :
[en] Dérivés des Porphyrines Tétracationique dans le cancer du sein
Publication date :
September 2021
Journal title :
Journal of Photochemistry and Photobiology B: Biology
Tan, C., Hu, W., He, Y., Zhang, Y., Zhang, G., Xu, Y., Tang, J., Cytokine-mediated therapeutic resistance in breast cancer. Cytokine 108 (2018), 151–159, 10.1016/j.cyto.2018.03.020.
Kovalchuk, O., Filkowski, J., Meservy, J., Ilnytskyy, Y., Tryndyak, V.P., Chekhun, V.F., Pogribny, I.P., Involvement of microRNA-451 in resistance of the MCF-7 breast cancer cells to chemotherapeutic drug doxorubicin. Mol. Cancer Ther. 7 (2008), 2152–2159, 10.1158/1535-7163.MCT-08-0021.
Dewangan, J., Srivastava, S., Rath, S.K., Salinomycin: a new paradigm in cancer therapy. Tumor Biol. 39 (2017), 1–12, 10.1177/1010428317695035.
Inoue, K., 5-Aminolevulinic acid-mediated photodynamic therapy for bladder cancer. Int. J. Urol. 24 (2017), 97–101, 10.1111/iju.13291.
Xue, J., Liu, C., Liu, Y., Photodynamic therapy as an alternative treatment for relapsed or refractory mycosis fungoides: a systemic review. Photodiagn. Photodyn. Ther. 17 (2016), 87–91, 10.1016/j.pdpdt.2016.11.010.
Agostinis, P., Berg, K., Cengel, K.A., Foster, T.H., Girotti, A.W., Gollnick, S.O., Hahn, S.M., Hamblin, M.R., Juzeniene, A., Kessel, D., Korbelik, M., Moan, J., Mroz, P., Nowiz, D., Piette, J., Willson, B.C., Golab, J., Photodynamic therapy of cancer : an update. CA Cancer J. Clin. 61 (2011), 250–281, 10.3322/caac.20114.
Mesquita, M.Q., Dias, C.J., Neves, M.G.P.M.S., Almeida, A., Faustino, M.A.F., Revisiting current photoactive materials for antimicrobial photodynamic therapy. Molecules, 23, 2018, 2424, 10.3390/molecules23102424.
Calmeiro, J.M.D., Gamelas, S.R.D., Gomes, A.T.P.C., Faustino, M.A.F., Neves, M.G.P.M.S., Almeida, A., Tomé, J.P.C., Lourenço, L.M.O., Versatile thiopyridyl/pyridinone porphyrins combined with potassium iodide and thiopyridinium/methoxypyridinium porphyrins on E. coli photoinactivation. Dyes Pigments, 181, 2020, 108476, 10.1016/j.dyepig.2020.108476.
Maruyama, T., Muragaki, Y., Nitta, M., Tsuzuki, S., Yasuda, T., Ikuta, S., Kawamata, T., Photodynamic therapy for malignant brain tumors. Japanese J. Neurosurg. 25 (2016), 895–904, 10.2176/nmc.ra.2015-0296.
Mesquita, M.Q., Dias, C.J., Gamelas, S., Fardilha, M., Neves, M.G.P.M.S., Faustino, M.A.F., An insight on the role of photosensitizer nanocarriers for photodynamic therapy. An. Acad. Bras. Cienc. 90 (2018), 1101–1130, 10.1590/0001-3765201720170800.
Almeida, A., Cunha, A., Faustino, M.A.F., Tomé, A.C., Neves, M.G.P.M.S., Porphyrins as antimicrobial photosensitizing agents. Hambiln, M.R., Jori, G., (eds.) Photodyn. Inact. Microb. Pathog. Med. Environ. Appl, 2011, 83–160, 10.1039/9781849733083-00083.
Huang, Y.Y., Sharma, S.K., Yin, R., Agrawal, T., Chiang, L.Y., Hamblin, M.R., Functionalized fullerenes in photodynamic therapy. J. Biomed. Nanotechnol. 10 (2014), 1918–1936, 10.1166/jbn.2014.1963.
Hamblin, M.R., Sabino, C.P., Photosensitizers. Photodyn. Ther. Vet. Med. From Basics to Clin. Pract, 2016, 25–44, 10.1007/978-3-319-45007-0.
Yan, X., Lu, N., Gu, Y., Li, C., Zhang, T., Liu, H., Zhang, Z., Zhai, S., Catalytic activity of biomimetic model of cytochrome P450 in oxidation of dopamine. Talanta. 179 (2018), 401–408, 10.1016/j.talanta.2017.11.038.
Zanardi, F.B., Barbosa, I.A., de Sousa Filho, P.C., Zanatta, L.D., da Silva, D.L., Serra, O.A., Iamamoto, Y., Manganese porphyrin functionalized on Fe3O4@nSiO2@MCM-41 magnetic composite: structural characterization and catalytic activity as cytochrome P450 model. Microporous Mesoporous Mater. 219 (2016), 161–171, 10.1016/j.micromeso.2015.07.035.
Cerqueira, A.F.R., Moura, N.M.M., Serra, V.V., Faustino, M.A.F., Tomé, A.C., Cavaleiro, J.A.S., Neves, M.G.P.M.S., β-Formyl- and β-vinylporphyrins: magic building blocks for novel porphyrin derivatives. Molecules, 22, 2017, 10.3390/molecules22081269.
Prabphal, J., Vilaivan, T., Praneenararat, T., Fabrication of a paper-based turn-off fluorescence sensor for Cu 2+ ion from a pyridinium porphyrin. ChemistrySelect 3 (2018), 894–899, 10.1002/slct.201702382.
Ding, Y., Zhu, W.H., Xie, Y., Development of ion chemosensors based on porphyrin analogues. Chem. Rev. 117 (2017), 2203–2256, 10.1021/acs.chemrev.6b00021.
Fallah, A.H., Endud, S., Alizadeh, A., Chien, L.S., Metalloporphyrin/dendrimer-decorated MCM-41 biomimetic hybrid catalysts: high stability combined with facile catalyst recyclability. J. Porous. Mater., 2018, 1–11, 10.1007/s10934-018-0595-2.
Pereira, C., Simões, M., Tomé, J., Almeida Paz, F., Porphyrin-based metal-organic frameworks as heterogeneous catalysts in oxidation reactions. Molecules., 21, 2016, 1348, 10.3390/molecules21101348.
Zahran, Z.N., Mohamed, E.A., Haleem, A.A., Naruta, Y., Efficient solar-assisted O2 reduction using a cofacial iron porphyrin dimer catalyst integrated into a p-CuBi2O4 photocathode. Chem. - A Eur. J. 24 (2018), 10606–10611, 10.1002/chem.201704143.
Huang, N., Wang, K., Drake, H., Cai, P., Pang, J., Li, J., Che, S., Huang, L., Wang, Q., Zhou, H.C., Tailor-made pyrazolide-based metal-organic frameworks for selective catalysis. J. Am. Chem. Soc. 140 (2018), 6383–6390, 10.1021/jacs.8b02710.
Zaragoza, J.P.T., Siegler, M.A., Goldberg, D.P., A reactive manganese(IV)-hydroxide complex: a missing intermediate in hydrogen atom transfer by high-valent metal-oxo porphyrinoid compounds. J. Am. Chem. Soc. 140 (2018), 4380–4390, 10.1021/jacs.8b00350.
Zhao, X., Liu, X., Yu, M., Wang, C., Li, J., The highly efficient and stable Cu, Co, Zn-porphyrin–TiO2 photocatalysts with heterojunction by using fashioned one-step method. Dyes Pigm. 136 (2017), 648–656, 10.1016/j.dyepig.2016.09.025.
Ahmed, M.A., Abou-Gamra, Z.M., Medien, H.A.A., Hamza, M.A., Effect of porphyrin on photocatalytic activity of TiO2 nanoparticles toward Rhodamine B photodegradation. J. Photochem. Photobiol. B Biol. 176 (2017), 25–35, 10.1016/j.jphotobiol.2017.09.016.
Ji, X., Wang, J., Mei, L., Tao, W., Barrett, A., Su, Z., Wang, S., Ma, G., Shi, J., Zhang, S., Porphyrin/SiO2/Cp*Rh(bpy)Cl hybrid nanoparticles mimicking chloroplast with enhanced electronic energy transfer for biocatalyzed artificial photosynthesis. Adv. Funct. Mater., 28, 2018, 1705083, 10.1002/adfm.201705083.
Martínez-Klimov, M.E., Organista-Mateos, U., Borja-Miranda, A., Rivera, M., Amelines-Sarria, O., Martínez-García, M., Electrical properties of multi-pyrene/porphyrin-dendrimers. Molecules 20 (2015), 17533–17543, 10.3390/molecules200917533.
Syu, Y.K., Tingare, Y., Lin, S.Y., Yeh, C.Y., Wu, J.J., Porphyrin dye-sensitized zinc oxide aggregated anodes for use in solar cells. Molecules, 21, 2016, 10.3390/molecules21081025.
Follana-Berná, J., Seetharaman, S., Martín-Gomis, L., Charalambidis, G., Trapali, A., Karr, P.A., Coutsolelos, A.G., Fernández-Lázaro, F., D'Souza, F., Sastre-Santos, Á., Supramolecular complex of a fused zinc phthalocyanine–zinc porphyrin dyad assembled by two imidazole - C60 units: ultrafast photoevents. Phys. Chem. Chem. Phys. 20 (2018), 7798–7807, 10.1039/C8CP00382C.
Serra, V.V., Zamarrón, A., Faustino, M.A.F., la Cruz, M.C.I., Blázquez, A., Rodrigues, J.M.M., Neves, M.G.P.M.S., Cavaleiro, J.A.S., Juarranz, A., Sanz-Rodríguez, F., New porphyrin amino acid conjugates: synthesis and photodynamic effect in human epithelial cells. Bioorg. Med. Chem. 18 (2010), 6170–6178, 10.1016/j.bmc.2010.06.030.
Cordeiro, R.M., Miotto, R., Baptista, M.S., Photodynamic efficiency of cationic meso-porphyrins at lipid bilayers: insights from molecular dynamics simulations. J. Phys. Chem. B 116 (2012), 14618–14627, 10.1021/jp308179h.
Castano, A.P., Demidova, T.N., Hamblin, M.R., Mechanisms in photodynamic therapy: part one - photosensitizers, photochemistry and cellular localization. Photodiagn. Photodyn. Ther. 1 (2004), 279–293, 10.1016/S1572-1000(05)00007-4.
Detty, M.R., Gibson, S.L., Wagner, S.J., Current clinical and preclinical photosensitizers for use in photodynamic therapy. J. Med. Chem. 47 (2004), 3897–3915, 10.1021/jm040074b.
Acedo, P., Stockert, J.C., Cañete, M., Villanueva, A., Two combined photosensitizers: a goal for more effective photodynamic therapy of cancer. Cell Death Dis. 5 (2014), 1–12, 10.1038/cddis.2014.77.
Hanakova, A., Bogdanova, K., Tomankova, K., Binder, S., Bajgar, R., Langova, K., Kolar, M., Mosinger, J., Kolarova, H., Study of photodynamic effects on NIH 3T3 cell line and bacteria. Biomed. Pap. 158 (2014), 201–207, 10.5507/bp.2012.057.
Jänicke, R.U., MCF-7 breast carcinoma cells do not express caspase-3. Breast Cancer Res. Treat. 117 (2009), 219–221, 10.1242/jcs.01610.
Mc Gee, M.M., Hyland, E., Campiani, G., Ramunno, A., Nacci, V., Zisterer, D.M., Caspase-3 is not essential for DNA fragmentation in MCF-7 cells during apoptosis induced by the pyrrolo-1,5-benzoxazepine, PBOX-6. FEBS Lett. 515 (2002), 66–70, 10.1016/s0014-5793(02)02440-7.
Tang, D., Kang, R., Vanden Berghe, T., Vandenabeele, P., Kroemer, G., The molecular machinery of regulated cell death. Cell Res. 29 (2019), 347–364, 10.1038/s41422-019-0164-5.
Wirawan, E., Vanden Berghe, T., Lippens, S., Agostinis, P., Vandenabeele, P., Autophagy: for better or for worse. Cell Res. 22 (2012), 43–61, 10.1038/cr.2011.152.
Lalaoui, N., Brumatti, G., Relevance of necroptosis in cancer. Immunol. Cell Biol., 2016, 1–25, 10.1038/icb.2016.120.
Chen, Q., Kang, J., Fu, C., The independence of and associations among apoptosis, autophagy, and necrosis. Signal Transduct. Target. Ther., 3, 2018, 18, 10.1038/s41392-018-0018-5.
Christofferson, D.E., Yuan, J., Cyclophilin A release as a biomarker of necrotic cell death. Cell Death Differ. 17 (2010), 1942–1943, 10.1038/cdd.2010.123.
Gobeil, S., Boucher, C.C., Nadeau, D., Poirier, G.G., Characterization of the necrotic cleavage of poly(ADP-ribose) polymerase (PARP-1): implication of lysosomal proteases. Cell Death Differ. 8 (2001), 588–594, 10.1038/sj.cdd.4400851.
Ouyang, L., Shi, Z., Zhao, S., Wang, F.-T., Zhou, T.-T., Liu, B., Bao, J.-K., Programmed cell death pathways in cancer: a review of apoptosis, autophagy and programmed necrosis. Cell Prolif. 45 (2012), 487–498, 10.1111/j.1365-2184.2012.00845.x.
Vanden Berghe, T., Grootjans, S., Goossens, V., Dondelinger, Y., Krysko, D.V., Takahashi, N., Vandenabeele, P., Determination of apoptotic and necrotic cell death in vitro and in vivo. Methods 61 (2013), 117–129, 10.1016/j.ymeth.2013.02.011.
Domagala, A., Stachura, J., Gabrysiak, M., Muchowicz, A., Zagozdzon, R., Golab, J., Firczuk, M., Inhibition of autophagy sensitizes cancer cells to Photofrin-based photodynamic therapy. BMC Cancer 18 (2018), 1–10, 10.1186/s12885-018-4126-y.
Basoglu, H., Bilgin, M.D., Demir, M.M., Protoporphyrin IX-loaded magnetoliposomes as a potential drug delivery system for photodynamic therapy: fabrication, characterization and in vitro study. Photodiagn. Photodyn. Ther. 13 (2016), 81–90, 10.1016/j.pdpdt.2015.12.010.
Nam, G., Rangasamy, S., Ju, H., Samson, A.A.S., Song, J.M., Cell death mechanistic study of photodynamic therapy against breast cancer cells utilizing liposomal delivery of 5,10,15,20-tetrakis(benzo[b]thiophene) porphyrin. J. Photochem. Photobiol. B Biol. 166 (2017), 116–125, 10.1016/j.jphotobiol.2016.11.006.
Ezzeddine, R., Al-Banaw, A., Tovmasyan, A., Craik, J.D., Batinic-Haberle, I., Benov, L.T., Effect of molecular characteristics on cellular uptake, subcellular localization, and phototoxicity of Zn(II) N-Alkylpyridylporphyrins. J. Biol. Chem. 288 (2013), 36579–36588, 10.1074/jbc.M113.511642.
Ikawa, Y., Moriyama, S., Harada, H., Furuta, H., Acid–base properties and DNA-binding of water soluble N-confused porphyrins with cationic side-arms. Org. Biomol. Chem. 6 (2008), 4157–4166, 10.1039/B810171J.
Kubát, P., Lang, K., Anzenbacher, P., Jursíková, K., Král, V., Ehrenberg, B., Interaction of novel cationic meso-tetraphenylporphyrins in the ground and excited states with DNA and nucleotides. J. Chem. Soc. Perkin Trans. 1 (2000), 933–941 https://doi.org/10.1039/A909466K.
Yamashita, T., Uno, T., Ishikawa, Y., Stabilization of guanine quadruplex DNA by the binding of porphyrins with cationic side arms. Bioorg. Med. Chem. 13 (2005), 2423–2430, 10.1016/j.bmc.2005.01.041.
Maximiano, R.V., Piovesan, E., Zílio, S.C., MacHado, A.E.H., De Paula, R., Cavaleiro, J.A.S., Borissevitch, I.E., Ito, A.S., Gonçalves, P.J., Barbosa Neto, N.M., Excited-state absorption investigation of a cationic porphyrin derivative. J. Photochem. Photobiol. A Chem. 214 (2010), 115–120, 10.1016/j.jphotochem.2010.06.007.
Alemán, E.A., Manríquez Rocha, J., Wongwitwichote, W., Godínez Mora-Tovar, L.A., Modarelli, D.A., Spectroscopy of free-base N-confused tetraphenylporphyrin radical anion and radical cation. J. Phys. Chem. A 115 (2011), 6456–6471, 10.1021/jp200411q.
Marchand, G., Roy, H., Mendive-Tapia, D., Jacquemin, D., N-confused porphyrin tautomers: lessons from density functional theory. Phys. Chem. Chem. Phys. 17 (2015), 5290–5297, 10.1039/C4CP05158K.
Baskin, J.S., Yu, H.-Z., Zewail, A.H., Ultrafast dynamics of porphyrins in the condensed phase: I. Free base tetraphenylporphyrin. J. Phys. Chem. A 106 (2002), 9837–9844, 10.1021/jp020398g.
Durantini, J., Otero, L., Funes, M., Durantini, E.N., Fungo, F., Gervaldo, M., Electrochemical oxidation-induced polymerization of 5,10,15,20-tetrakis[3-(N-ethylcarbazoyl)]porphyrin. Formation and characterization of a novel electroactive porphyrin thin film. Electrochim. Acta 56 (2011), 4126–4134, 10.1016/j.electacta.2011.01.111.
Strachan, J.P., Gentemann, S., Seth, J., Kalsbeck, W.A., Lindsey, J.S., Holten, D., Bocian, D.F., Effects of orbital ordering on electronic communication in multiporphyrin arrays. J. Am. Chem. Soc. 119 (1997), 11191–11201, 10.1021/ja971678q.
Belair, J.P., Ziegler, C.J., Rajesh, C.S., Modarelli, D.A., Photophysical characterization of free-base N-confused tetraphenylporphyrins. J. Phys. Chem. A 106 (2002), 6445–6451, 10.1021/jp025569w.
Lee, J.S., Lim, J.M., Toganoh, M., Furuta, H., Kim, D., Comparative spectroscopic studies on porphyrin derivatives: electronic perturbation of N-confused and N-fused porphyrins. Chem. Commun. 46 (2010), 285–287, 10.1039/B916521E.
Alemán, E.A., Rajesh, C.S., Ziegler, C.J., Modarelli, D.A., Ultrafast spectroscopy of free-base N-confused tetraphenylporphyrins. J. Phys. Chem. A 110 (2006), 8605–8612, 10.1021/jp062061a.
Toganoh, M., Furuta, H., Blooming of confused porphyrinoids—fusion, expansion, contraction, and more confusion. Chem. Commun. 48 (2012), 937–954, 10.1039/C1CC14633E.
Wojaczyński, J., Latos-Grażyński, L., Photooxidation of N-confused porphyrin: a route to N-confused biliverdin analogues. Chem. Eur. J. 16 (2010), 2679–2682, 10.1002/chem.200903182.
Wojaczyński, J., Popiel, M., Szterenberg, L., Latos-Grażyński, L., Common origin, common fate: regular porphyrin and N-confused porphyrin yield an identical tetrapyrrolic degradation product. J. Organomet. Chem. 76 (2011), 9956–9961, 10.1021/jo201489z.
Bacellar, I.O.L., Tsubone, T.M., Pavani, C., Baptista, M.S., Photodynamic efficiency: from molecular photochemistry to cell death. Int. J. Therm. Sci. 16 (2015), 20523–20559, 10.3390/ijms160920523.
Liu, H., Lv, C., Ding, B., Wang, J., Li, S., Zhang, Y., Antitumor activity of G-quadruplex-interactive agent TMPyP4 with photodynamic therapy in ovarian carcinoma cells. Oncol. Lett. 8 (2014), 409–413, 10.3892/ol.2014.2125.
Cenklová, V., Photodynamic therapy with TMPyP – porphyrine induces mitotic catastrophe and microtubule disorganization in HeLa and G361 cells, a comprehensive view of the action of the photosensitizer. J. Photochem. Photobiol. B 173 (2017), 522–537, 10.1016/j.jphotobiol.2017.06.029.
Berridge, M., Tan, A., McCoy, K., Wang, R., The biochemical and cellular basis of cell proliferation assays that use tetrazolium salts. Biochemica, 1996, 4–9.
Moan, J., Berg, K., The photodegradation of porphyrins in cells can be used to estimate the lifetime of singlet oxygen. Photochem. Photobiol. 53 (1991), 549–553, 10.1111/j.1751-1097.1991.tb03669.x.
Rangasamy, S., Ju, H., Um, S., Oh, D.C., Song, J.M., Mitochondria and DNA targeting of 5,10,15,20-tetrakis(7-sulfonatobenzo[b]thiophene) porphyrin-induced photodynamic therapy via intrinsic and extrinsic apoptotic cell death. J. Med. Chem. 58 (2015), 6864–6874, 10.1021/acs.jmedchem.5b01095.
Charara, M., Tovmasyan, A., Batinic-Haberle, I., Craik, J., Benov, L., Post-illumination cellular effects of photodynamic treatment. PLoS One 12 (2017), 1–19, 10.1371/journal.pone.0188535.
Tanida, I., Ueno, T., Kominami, E., LC3 conjugation system in mammalian autophagy. Int. J. Biochem. Cell Biol. 36 (2004), 2503–2518, 10.1016/j.biocel.2004.05.009.
Portt, L., Norman, G., Clapp, C., Greenwood, M., Greenwood, M.T., Anti-apoptosis and cell survival: a review. Biochem. Biophys. 1813 (2011), 238–259, 10.1016/j.bbamcr.2010.10.010.
Khan, M.J., Alam, M.R., Waldeck-Weiermair, M., Karsten, F., Groschner, L., Riederer, M., Hallström, S., Rockenfeller, P., Konya, V., Heinemann, A., Madeo, F., Graier, W.F., Malli, R., Inhibition of autophagy rescues palmitic acid-induced necroptosis of endothelial cells. J. Biol. Chem. 287 (2012), 21110–21120, 10.1074/jbc.M111.319129.
Xue, L.Y., Chiu, S.M., Oleinick, N.L., Atg7 deficiency increases resistance of MCF-7 human breast cancer cells to photodynamic therapy. Autophagy 6 (2010), 248–255, 10.4161/auto.6.2.11077.