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

Moan, 1989, Intracellular localization of photosensitizers, CIBA Found. Symp., 146, 95 Agostinis, 2011, Photodynamic therapy of cancer: an update, CA Cancer J. Clin., 61, 250, 10.3322/caac.20114 Robertson, 2009, Photodynamic therapy (PDT): a short review on cellular mechanisms and cancer research applications for PDT, J. Photochem. Photobiol. B, 96, 1, 10.1016/j.jphotobiol.2009.04.001 Allison, 2010, Future of oncologic photodynamic therapy, Future Oncol., 6, 929, 10.2217/fon.10.51 Juarranz, 2001, Photodamage induced by Zinc(II)-phthalocyanine to microtubules, actin, alpha-actinin and keratin of HeLa cells, Photochem. Photobiol., 73, 283, 10.1562/0031-8655(2001)0730283PIBZIP2.0.CO2 Kudinova, 2010, Photodynamic therapy of cancer: search for ideal photosensitizer, Biochem. Sup. B. Biomed. Chem., 4, 95 Gois, 2010, Susceptibility of Staphylococcus aureus to porphyrin-mediated photodynamic antimicrobial chemotherapy: an in vitro study, Lasers Med. Sci., 25, 391, 10.1007/s10103-009-0705-0 Baltazar, 2015, Antimicrobial photodynamic therapy: an effective alternative approach to control fungal infections, Front. Microbiol., 6, 202, 10.3389/fmicb.2015.00202 Hanakova, 2014, The application of antimicrobial photodynamic therapy on S. aureus and E. coli using porphyrin photosensitizers bound to cyclodextrin, Microbiol. Res., 169, 163, 10.1016/j.micres.2013.07.005 Spring, 2015, The role of photodynamic therapy in overcoming cancer drug resistance, Photochem. Photobiol. Sci., 14, 1476, 10.1039/C4PP00495G Plaetzer, 2009, Photophysics and photochemistry of photodynamic therapy: fundamental aspects, Lasers Med. Sci., 24, 259, 10.1007/s10103-008-0539-1 Allison, 2010, Oncologic photodynamic therapy photosensitizers, Photodiagn. Photodyn. Ther., 7, 61, 10.1016/j.pdpdt.2010.02.001 Barata, 2015, Photodynamic effects induced by meso tris(pentafluorophenyl)corrole and its cyclodextrin conjugates on cytoskeletal components of HeLa cells, Eur. J. Med. Chem., 92, 135, 10.1016/j.ejmech.2014.12.025 Jordan, 2004, Microtubules as a target for anticancer drugs, Nat. Rev. Cancer, 4, 253, 10.1038/nrc1317 Uzdensky, 2005, The effect of sub-lethal ALA-PDT on the cytoskeleton and adhesion of cultured human cancer cells, Biochim. Biophys. Acta, 1722, 43, 10.1016/j.bbagen.2004.11.011 Rello-Varona, 2008, Mitotic catastrophe induced in HeLa cells by photodynamic treatment with Zn(II)-phthalocyanine, Int. J. Oncol., 32, 1189, 10.3892/ijo_32_6_1189 Chen, 2006, Tumor vascular permeabilization by vascular-targeting photosensitization: effects, mechanism, and therapeutic implications, Clin. Cancer Res., 12, 917, 10.1158/1078-0432.CCR-05-1673 Casas, 2008, Disorganisation of cytoskeleton in cells resistant to photodynamic treatment with decreased metastatic phenotype, Cancer Lett., 270, 56, 10.1016/j.canlet.2008.04.029 Di Venosa, 2012, Changes in actin and E-cadherin expression induced by 5-aminolevulinic acid photodynamic therapy in normal and Ras-transfected human mammary cell lines, J. Photochem. Photobiol. B, 106, 47, 10.1016/j.jphotobiol.2011.10.002 Heng, 2010, Actin cytoskeleton dynamics and the cell division cycle, Int. J. Biochem. Cell Biol., 42, 1622, 10.1016/j.biocel.2010.04.007 Di Venosa, 2015, The role of cytoskeleton and adhesion proteins in the resistance to photodynamic therapy. Possible therapeutic interventions, Photochem. Photobiol. Sci., 14, 1451, 10.1039/C4PP00445K Ferreira, 2004, Analysis of mitochondria, endoplamic reticulum and actin filaments after PDT with AlPcS4, Lasers Med. Sci., 18, 207, 10.1007/s10103-003-0282-6 Tsai, 2005, Reorganization of cytoskeleton induced by 5-aminolevulinic acid-mediated photodynamic therapy and its correlation with mitochondrial dysfunctioin, Lasers Surg. Med., 36, 398, 10.1002/lsm.20179 Pluskalová, 2006, Photodynamic treatment (ALA-PDT) suppresses the expression of the oncogenic Bcr-Abl kinase and affects the cytoskeleton organization in K562 cells, J. Photochem. Photobiol. B, 83, 205, 10.1016/j.jphotobiol.2006.01.003 Maftoum-Costa, 2008, Mitochondria, endoplasmic reticulum and actin filament behavior after PDT with chloroaluminum phthalocyanine liposomal in HeLa cells, Cell Biol. Int., 32, 1024, 10.1016/j.cellbi.2008.04.005 Panzarini, 2009, Photodynamic therapy-induced apoptosis of HeLa cells, Ann. N. Y. Acad. Sci., 1171, 617, 10.1111/j.1749-6632.2009.04908.x Jung, 2009, Identification and ultrastructural imaging of photodynamic therapy-induced microfilaments by atomic force microscopy, Ultramicroscopy, 109, 1428, 10.1016/j.ultramic.2009.07.009 Milla, 2011, Isolation and characterization of squamous carcinoma cells resistant to photodynamic therapy, J. Cell. Biochem., 112, 2266, 10.1002/jcb.23145 Acedo, 2014, Two combined photosensitizers: a goal for more effective photodynamic therapy of cancer, Cell Death Dis., 5, 1122, 10.1038/cddis.2014.77 Kiliç Süloğlu, 2015, Alterations in dysadherin expression and F-actin reorganization: a possible mechanism of hypericin-mediated photodynamic therapy in colon adenocarcinoma cells, Cytotechnology, 67, 311, 10.1007/s10616-013-9688-6 Beil, 2006, Fitting of random tessellation models to keratin filament networks, J. Theor. Biol., 241, 62, 10.1016/j.jtbi.2005.11.009 Liu, 2010, Prostate-specific membrane antigen-targeted photodynamic therapy induces rapid cytoskeletal disruption, Cancer Lett., 296, 106, 10.1016/j.canlet.2010.04.003 Uzdensky, 2012, Dynamics of signaling, cytoskeleton and cell cycle regulation proteins in glioblastoma cells after sub-lethal photodynamic treatment: antibody microarray study, Biochim. Biophys. Acta, 1820, 795, 10.1016/j.bbagen.2012.03.008 Kimura, 2013, Mitotic catastrophe and cell death induced by depletion of centrosomal proteins, Cell Death Dis., 4, 603, 10.1038/cddis.2013.108 Wang, 2015, Combination of a novel photosensitizer DTPP with 6506nm laser results in efficient apoptosis, arresting cell cycle and cytoskeleton protein changes in lung cancer A549 cells, Lasers Med. Sci., 30, 77, 10.1007/s10103-014-1617-1 Galluzzi, 2007, Cell death modalities: classification and pathophysiological implications, Cell Death Differ., 14, 1237, 10.1038/sj.cdd.4402148 Mansilla, 2006, Mitotic catastrophe results in cell death by caspase-dependent and caspase-independent mechanisms, Cell Cycle, 5, 53, 10.4161/cc.5.1.2267 Stevens, 2007, Mitotic cell death by chromosome fragmentation, Cancer Res., 67, 7686, 10.1158/0008-5472.CAN-07-0472 Castedo, 2004, Cell death by mitotic catastrophe: a molecular definition, Oncogene, 23, 2825, 10.1038/sj.onc.1207528 Castedo, 2006, Selective resistance of tetraploid cancer cells against DNA damage-induced apoptosis, Ann. N. Y. Acad. Sci., 1090, 35, 10.1196/annals.1378.004 Baker, 2005, The mitotic checkpoint in cancer and aging: what have mice taught us?, Curr. Opin. Cell Biol., 17, 583, 10.1016/j.ceb.2005.09.011 Xiao, 2004, Involvement of G1/checkpoint regulators during photodynamic-therapy-mediated cell cycle arrest in human colon carcinoma SW480 cells, World Chin. J. Digestol., 12, 1048, 10.11569/wcjd.v12.i5.1048 Soares, 2012, Glycophtahalocyanines as photosensitizer for triggering mitotic catastrophe and apoptosis in cancer cells, Chem.Res. Toxicol., 25, 940, 10.1021/tx300035a Pizova, 2015, C-MYC and C-FOS expression changes and cellular aspects of the photodynamic reaction with photosensitizers TMPyP and ClAlPcS2, J. Photochem. Photobiol. B, 142, 186, 10.1016/j.jphotobiol.2014.12.003 Lang, 2001, Photophysical properties and photoinduced electron transfer within host-guest complexes of 5,10,15,20-tetrakis(4-N-methylpyridyl)porphyrin with water-soluble calixarenes and cyclodextrins, Photochem. Photobiol., 74, 558, 10.1562/0031-8655(2001)074<0558:PPAPET>2.0.CO;2 O'Connor, 2009, Porphyrin and nonporphyrin photosensitizers in oncology: preclinical and clinical advances in photodynamic therapy, Photochem. Photobiol., 85, 1053, 10.1111/j.1751-1097.2009.00585.x Pereira, 2014, Galactodendritic phthalocyanine targets carbohydrate-binding proteins enhancing photodynamic therapy, PLoS One, 9, 95529, 10.1371/journal.pone.0095529 Lourenço, 2014, Amphiphilic phthalocyanine-cyclodextrin conjugates for cancer photodynamic therapy, Chem. Commun., 50, 8363, 10.1039/C4CC02226B Dryková, 2003, Plant γ-tubulin interacts with α,β-tubulin dimers and forms membrane-associated complexes, Plant Cell, 15, 465, 10.1105/tpc.007005 Sulimenko, 2006, Regulation of microtubule formation in activated mast cellsby complexes of γ-tubulin with Fyn and Syk kinases1, J. Immunol., 176, 7243, 10.4049/jimmunol.176.12.7243 Varmus, 2006, The new era in cancer research, Science, 312, 1162, 10.1126/science.1126758 Hani, 2016, Current perspectives on novel drug delivery systems and approaches for management of cervical cancer: a comprehensive review, Curr. Drug Targets, 17, 337, 10.2174/1389450116666150505154720 Floyd, 2015, Drug encapsulated polymeric microspheres for intracranial tumor therapy: a review of the literature, Adv. Drug Deliv. Rev., 91, 23, 10.1016/j.addr.2015.04.008 Wu, 2015, Nanoparticle-based targeted therapeutics in head-and-neck cancer, Int. J. Med. Sci., 12, 187, 10.7150/ijms.10083 Arrighetti, 2015, Drug combinations with HDAC inhibitors in antitumor therapy, Crit. Rev. Oncog., 20, 83, 10.1615/CritRevOncog.2014012378 Golden, 2012, The convergence of radiation and immunogenic cell death signaling pathways, Front. Oncol., 2, 88, 10.3389/fonc.2012.00088 Mfouo-Tynga, 2015, Cell death pathways and phthalocyanine as an efficient agent for photodynamic cancer therapy, Int. J. Mol. Sci., 16, 10228, 10.3390/ijms160510228 Vantieghem, 2002, Phosphorylation of Bcl-2 in G2/M phase-arrested cells following photodynamic therapy with hypericin involves a CDK1-mediated signal and delays the onset of apoptosis, J. Biol. Chem., 277, 37718, 10.1074/jbc.M204348200 Panzarini, 2011, Timing the multiple cell death pathways initiated by Rose Bengal acetate photodynamic therapy, Cell Death Dis., 2, 169, 10.1038/cddis.2011.51 Agostinis, 2002, Hypericin in cancer treatment: more light on the way, Int. J. Biochem. Cell Biol., 34, 221, 10.1016/S1357-2725(01)00126-1 Kroemer, 2005, Classification of cell death: recommendations of the Nomenclature Commitee on Cell Death, Cell Death Differ., 12, 1463, 10.1038/sj.cdd.4401724 Blagosklonny, 2007, Mitotic arrest and cell fate, Cell Cycle, 6, 70, 10.4161/cc.6.1.3682 Gordon, 2015, Protein phosphatase 2A inhibition with LB100 enhances radiation-induced mitotic catastrophe and tumor growth delay in glioblastoma, Mol. Cancer Ther., 14, 1540, 10.1158/1535-7163.MCT-14-0614 Li, 2015, Co-inhibition of polo-like kinase 1 and Aurora kinases promotes mitotic catastrophe, Oncotarget, 6, 9327, 10.18632/oncotarget.3313 Zhou, 2014, Induction of mitotic catastrophe by PKC inhibition in Nf1-deficient cells, Cell Cycle, 13, 2340, 10.4161/cc.29297 Vakifahmetoglu, 2008, DNA damage induces two distinct modes of cell death in ovarian carcinomas, Cell Death Differ., 15, 555, 10.1038/sj.cdd.4402286 Niikura, 2007, BUB1 mediation of caspase independent mitotic death determines cell fate, J. Cell Biol., 178, 283, 10.1083/jcb.200702134 Huang, 2008, Aurora kinase inhibitory VX-680 increases Bax/Bcl-2 ratio and induces apoptosis in Aurora-A-high acute myeloid leukemia, Blood, 111, 2854, 10.1182/blood-2007-07-099325 Vogel, 2007, Mechanisms of mitotic cell death induced by chemotherapy mediated G2 checkpoint abrogation, Cancer Res., 67, 339, 10.1158/0008-5472.CAN-06-2548 Jordan, 1996, Mitotic block induced in HeLa cells by low concentrations of paclitaxel (taxol) results in abnormal mitotic exit and apoptotic cell death, Cancer Res., 56, 816 Jackson, 2007, Targeted antimitotik therapies: can we improve on tubulin agents?, Nat. Rev. Cancer, 7, 107, 10.1038/nrc2049 Bhalla, 2003, Microtubule-targeted anticancer agents and apoptosis, Oncogene, 22, 9075, 10.1038/sj.onc.1207233 Moss, 2006, A novel role for microtubules in apoptotic chromatin dynamics and cellular fragmentation, J. Cell Sci., 119, 2362, 10.1242/jcs.02959 Chan, 2012, Mitosis-targeted anti-cancer therapies: where they stand, Cell Death Dis., 3, 411, 10.1038/cddis.2012.148 Berg, 1997, Lysosomes and microtubules as targets for photochemotherapy of cancer, Photochem. Photobiol., 65, 403, 10.1111/j.1751-1097.1997.tb08578.x Runnels, 1999, BPD-MA–mediated photosensitization in vitro and in vivo: cellular adhesion and b1 integrin expression in ovarian cancer cells, Br. J. Cancer, 80, 946, 10.1038/sj.bjc.6690448 Rousset, 1999, Effects of photodynamic therapy on adhesion molecules and metastasis, J. Photochem. Photobiol. B, 52, 65, 10.1016/S1011-1344(99)00104-9 Stockert, 1996, Photodynamic damage to HeLa cell microtubules induced by thiazine dyes, Cancer Chemother. Pharmacol., 39, 167, 10.1007/s002800050554 Juarranz, 1995, Photodynamic effects of the cationic porphyrin, mesotetra(4 Nmethylpyridyl) porphine, on microtubules of HeLa cells, J. Photochem. Photobiol. B Biol., 27, 47, 10.1016/1011-1344(94)07055-S Sporn, 1992, Photofrin and light induces microtubule depolymerization in cultured human endothelial cells, Cancer Res., 52, 3443 Xia, 2011, New hydrophilic/lipophilic tetra-alpha-(4-carboxyphenoxy) phthalocyanine zinc-mediated photodynamic therapy inhibits the proliferation of human hepatocellular carcinoma Bel-7402 cells by triggering apoptosis and arresting cell cycle, Molecules, 16, 1389, 10.3390/molecules16021389 Radzi, 2012, Photodynamic hyperthermal therapy with indocyanine green (ICG) induces apoptosis and cell cycle arrest in B16F10 murine melanoma cells, J. Vet. Med. Sci., 74, 545, 10.1292/jvms.11-0464 Wang, 2014, Combination of a novel photosensitizer DTPP with 650nm laser results in efficient apoptosis and cytoskeleton collapse in breast cancer MCF-7 cells, Cell Biochem. Biophys., 69, 549, 10.1007/s12013-014-9830-x Shao, 2012, Inhibition of human hepatocellular carcinoma HepG2 by phthalocyanine photosensitiser photocyanine: ROS production, apoptosis, cell cycle arrest, Eur. J. Cancer, 48, 2086, 10.1016/j.ejca.2011.10.013 Celli, 2010, Imaging and photodynamic therapy: mechanisms, monitoring and optimization, Chem. Rev., 110, 2795, 10.1021/cr900300p Oliveira, 2011, Major determinants of photoinduced cell death: subcellular localization versus photosensitization efficiency, Free Radic. Biol. Med., 51, 824, 10.1016/j.freeradbiomed.2011.05.023 Ruiz-González, 2013, Efficient induction of apoptosis in HeLa cell by a novel cationic porphycene photosensitizer, Eur. J. Med. Chem., 63, 401, 10.1016/j.ejmech.2013.02.028 Alvarez, 2005, Photodynamic damage induced by a monocationic porphyrin derivative in a human carcinoma cell line, Int. J. Biochem. Cell Biol., 37, 2504, 10.1016/j.biocel.2005.06.016 Csík, 2009, Role of structure proteins In the porphyrin-DNA interaction, J. Photochem. Photobiol. B Biol., 96, 207, 10.1016/j.jphotobiol.2009.06.008 Fujiwara, 2015, TMPyP4, a stabilizer of nucleic acid secondary structure, is a novel acetylcholinesterase inhibitor, PLoS One, 10, 10.1371/journal.pone.0139167 Villanueva, 2010, A new protocol in photodynamic therapy: enhanced tumour cell death by combining two different photosensitizers, Photochem. Photobiol. Sci. 93 (2010) 295–297, 1649 Georgiou, 1994, Measurement of the rate of uptake and subcellular localization of porphyrins in cells using fluorescence digital imaging microscopy, Photochem. Photobiol., 59, 419, 10.1111/j.1751-1097.1994.tb05058.x Pasternack, 1983, Interactions of porphyrins with nucleic acids, Biochemistry, 22, 2406, 10.1021/bi00279a016 Berg, 1992, Mitotic inhibition by phenylporphines and tetrasulfonated aluminium phthalocyanine in combination with light, Photochem. Photobiol., 56, 333, 10.1111/j.1751-1097.1992.tb02168.x Winkelman, 1993, Stereochemical factors in the transport and binding of photosensitizer in biological systems and photodynamic therapy, J. Photochem. Photobiol. B Biol., 18, 181, 10.1016/1011-1344(93)80061-D Zheng, 2016, TMPyP4 promotes cancer cell migration at low doses, but induces cell death at high doses, Sci Rep, 6, 26592, 10.1038/srep26592 Shimada, 2013, High LET radiation amplifies centrosome overduplication through a pathway of γ-tubulin monoubiquitination, Int. J. Radiat. Oncol. Biol. Phys., 86, 358, 10.1016/j.ijrobp.2013.01.010 Giet, 2005, Aurora kinases, aneuploidy and cancer, a coincidence or a real link?, Trends Cell Biol., 15, 241, 10.1016/j.tcb.2005.03.004 Steinhusen, 2000, Apoptosis-induced cleavage of betacatenin by caspase-3 results in proteolytic fragments with reduced transactivation potential, J. Biol. Chem., 275, 16345, 10.1074/jbc.M001458200 You, 2011, Proteomics displays cytoskeletal proteins and chaperones involvement in Hedyotis corymbosa-induced photokilling in skin cancer cells, Exp. Dermatol., 20, 653, 10.1111/j.1600-0625.2011.01290.x Mian, 2008, Cleavage of focal adhesion kinase is an early marker and modulator of oxidative stress-induced apoptosis, Chem. Biol. Interact., 171, 57, 10.1016/j.cbi.2007.08.009 Chatzizacharias, 2008, Disruption of FAK signaling: a side mechanism in cytotoxicity, Toxicology, 245, 1, 10.1016/j.tox.2007.12.003 Berg, 1992, The unpolymerized form of tubulin is the target for microtubule inhibition by photoactivated tetra(4-sulfonatopheny1) porphine, Biochim. Biophys. Acta, 1135, 147, 10.1016/0167-4889(92)90130-4 Lee, 1995, Photosensitization by 3,3′-dihexyloxacarbocyanine iodide: specific disruption of microtubules and inactivation of organelle motility, Cancer Res., 55, 2063 Ringel, 1996, Photodynamic activity of porphyrins on tubulin assembly, 2625, 156 Casas, 2011, Mechanisms of resistance to photodynamic therapy, Curr. Med. Chem., 18, 2486, 10.2174/092986711795843272