Cell death pathways and phthalocyanine as an efficient agent for photodynamic cancer therapy

International Journal of Molecular Sciences

Volumn 16, Issue 5, 2015, Pages 10228-10241

  Mfouo Tynga, Ivan ^a   Abrahamse, Heidi ^a  

^a UNIVERSITY OF JOHANNESBURG   (South Africa)

Author keywords

Death mechanisms; Photodynamic cancer therapy; Photosensitizer; Phthalocyanine; Reactive oxygen species

Indexed keywords

BECLIN 1; CASPASE 2; CATALASE; CHLOROALUMINUM PHTHALOCYANINE; CYTOCHROME C; CYTOKINE; FAS ANTIGEN; HYPOXIA INDUCIBLE FACTOR; MAMMALIAN TARGET OF RAPAMYCIN; PHTHALOCYANINE; PHTHALOCYANINE ZINC; PORPHYRIN; PROTEIN BCL 2; PROTEIN BCL X; PROTEIN KINASE B; PROTEIN P53; REACTIVE OXYGEN METABOLITE; RECEPTOR INTERACTING PROTEIN 140; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SYNAPTOPHYSIN; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RECEPTOR 1; INDOLE DERIVATIVE; RADIOSENSITIZING AGENT;

APOPTOSIS; AUTOPHAGOSOME; AUTOPHAGY; B CELL LYMPHOMA; CANCER THERAPY; CELL DAMAGE; CELL DEATH; CELL PROLIFERATION; CELL STRUCTURE; CELL VIABILITY; CYTOTOXICITY; HUMAN; INFLAMMATION; LUNG CANCER; NECROSIS; PHOTOCHEMICAL EFFICIENCY; PHOTODYNAMIC THERAPY; PHOTODYNAMICS; PHOTOTOXICITY; REVIEW; SIGNAL TRANSDUCTION; STRESS; ANIMAL; CHEMISTRY; DRUG EFFECTS; METABOLISM; NEOPLASMS; PHOTOCHEMOTHERAPY; PROCEDURES;

ANIMALS; APOPTOSIS; HUMANS; INDOLES; NEOPLASMS; PHOTOCHEMOTHERAPY; RADIATION-SENSITIZING AGENTS; REACTIVE OXYGEN SPECIES;

EID: 84929353037     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms160510228     Document Type: Review

References (70)

1. Engelberg-Kulka, H.; Amitai, S.; Kolodkin-Gal, I.; Hazan, R. Bacterial programmed cell death and multicellular behavior in bacteria. PLoS Genet. 2006, 2, e135.
2. Schultz, D.R.; Harrington, W.J., Jr. Apoptosis: Programmed cell death at a molecular level. Semin. Arthritis Rheum. 2003, 32, 345–369.
3. Yuan, J.; Kroemer, G. Alternative cell death mechanisms in development and beyond. Genes Dev. 2010, 24, 2592–2602.
4. Melino, G. The Sirens’ song. Nature 2001, 412, 23–31.
5. Kroemer, G.; Galluzzi, L.; Vandenabeele, P.; Abrams, J.; Alnemri, E.S.; Baehrecke, E.H.; Blagosklonny, M.V.; El-Deiry, W.S.; Golstein, P.; Green, D.R.; et al. Classification of cell death. Cell Death Differ. 2009, 16, 3–11.
6. Erental, A.; Sharon, I.; Engelberg-Kulka, H. Two programmed cell death systems in Escherichia coli: An apoptotic-like death is inhibited by the mazEF-mediated death pathway. PLoS Biol. 2012, 10, e1001281.
7. Kim, K.S.; Cho, C.H.; Park, E.K.; Jung, M.H.; Yoon, K.S.; Park, H.K. AFM-Detected apoptotic changes in morphology and biophysical property caused by paclitaxel in ishikawa and heLa cells. PLoS ONE 2012, 7, e30066.
8. Kang, R.; Zeh, H.J.; Lotze, M.T.; Tang, D. The Beclin 1 network regulates autophagy and apoptosis. Cell Death Differ. 2011, 18, 571–580.
9. Lam, M; Lee, Y.J.; Deng, M.; Hsia A.H.; Morrissey K.A.; Yan, C.; Azzizudin, K.; Oleinick, N.L.; McCormick, T.S.; Cooper, K.D.; et al. Photodynamic therapy with the silicon phthalocyanine Pc 4 induces apoptosis inMycosis fungoides and sezary syndrome. Adv. Hematol. 2010, 2010, doi:10.1155/2010/896161.
10. Mfouo-Tynga, I.; Houreld, N.N.; Abrahamse, H. Induced cell death pathway post photodynamic therapy using a metallophthalocyanine photosensitizer in breast cancer cells. Photomed. Laser Surg. 2014, 32, 205–211.
11. Mroz, P.; Yaroslavsky, A.; Kharkwal, G.B.; Hamblin, M.R. Cell death pathways in photodynamic therapy of cancer. Cancers 2011, 3, 2516–2539.
12. Giorgi, C.; Bonora, M.; Sorrentino, G.; Missiroli, S.; Poletti, F.; Suski, J.M.; Ramirez, F.G.; Rizzuto, R.; di Virgilio, F.; Zito, E.; et al. P53 at the endoplasmic reticulum regulates apoptosis in a Ca2+-dependent manner. Proc. Natl Acad. Sci. USA 2015, 112, 1779–1784.
13. Giorgi, C.; Bonora, M.; Missiroli, S.; Poletti, F.; Ramirez, F.G.; Morciano, G.; Morganti, C.; Pandolfi, P.P.; Mammano, F.; Pinton, P. Intravital imaging reveals p53-dependent cancer cell death induced by phototherapy via calcium signaling. Oncotarget 2015, 6, 1435–1445.
14. Tsujimoto, Y.; Shimizu, S. Another way to die: Autophagic programmed cell death. Cell Death Differ. 2005, 12, 1528–1534.
15. Jain, K.; Paranandi, K.S.; Sridharan, S.; Basu, A. Autophagy in breast cancer and its implications for therapy. Am. J. Cancer Res. 2013, 3, 251–265.
16. Michaud, M.; Martins, I.; Sukkurwala, A.Q.; Adjemian, S.; Ma, Y.; Pellegatti, P.; Shen, S.; Kepp, O.; Scoazec, M.; Mignot, G.; et al. Autophagy-dependent anticancer immune responses induced by chemotherapeutic agents in mice. Science 2011, 334, 1573–1577.
17. Di, X.; Zhang G.; Zhang, Y.; Takeda, K.; Rivera Rosado, L.A.; Zhang, B. Accumulation of autophagosomes in breast cancer cells induces TRAIL resistance through downregulation of surface expression of death receptors 4 and 5. Oncotarget. 2013, 4, 1349–1364.
18. Xie, Z.; Klionsky, D.J. Autophagosome formation: Core machinery and adaptation. Nat. Cell Biol. 2007, 9, 1102–1109.
19. Nikoletopoulou, V.; Markaki, M.; Palikaras, K.; Tavernarakis, N. Crosstalk between apoptosis, necrosis and autophagy. Biochem. Biophys. Acta 2013, 1833, 3448–3459.
20. 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. 2012, 45, 487–498.
21. Lamkanfi, M.; Festjens, N.; Declercq, W.; Vanden Berghe, T.; Vandenabeele, P. Caspases in cell survival, proliferation and differentiation. Cell Death Differ. 2007, 14, 44–55.
22. Yu, L.; Wan, F.; Dutta, S.; Welsh, S.; Liu, Z.; Freundt, E.; Baehrecke, E.H.; Lenardo, M. Autophagic programmed cell death by selective catalase degradation. Proc. Natl. Acad. Sci. USA 2006, 103, 4952–4957.
23. Mizushima, N.; Klionsky, D.J. Protein turnover via autophagy: Implications for metabolism. Annu. Rev. Nutr. 2007, 27, 19–40.
24. Separovic, D.; Joseph, N.; Breen, P.; Bielawski, J.; Pierce, J.S.; van Buren, E.; Bhatti, G.; Saad, Z.H.; Bai, A.; Bielawska, A. Combining anticancer agents photodynamic therapy and LCL85 leads to distinct changes in the sphingolipid profile, autophagy, caspase-3 activation in the absence of cell death, and long-term sensitization. Biochem. Biophys. Res. Commun. 2011, 409, 372–377.
25. Patel, A.S.; Lin, L.; Geyer, A.; Haspel, J.A.; An, C.H.; J. Cao, Rosas, I.O.; Morse, D. Autophagy in Idiopathic Pulmonary Fibrosis. PLoS ONE, 2012, 7, e41394.
26. Peracchio, C.; Alabiso, O.; Valente, G.; Isidoro, C. Involvement of autophagy in ovarian cancer: A working hypothesis. J. Ovarian Res. 2012, 5, 22–32.
27. Xue, L.Y.; Chiu, S.M.; Oleinick, N.L. Atg7 deficiency increases resistance of MCF-7 human breast cancer cells to photodynamic therapy. Autophagy 2010, 6, 248–255.
28. Garg, A.D.; Maes, H.; Romanoa, E.; Agostinis, P. Autophagy, a major adaptation pathway shaping cancer cell death and anticancer immunity responses following photodynamic therapy. Photochem. Photobiol. Sci. 2015, doi:10.1039/C4PP00466C.
29. Lemasters, J.J. Dying a thousand deaths: Redundant pathways from different organelles to apoptosis and necrosis. Gastroentrology 2005, 129, 351–360.
30. Cho, Y.; McQuade, T.; Zhang, H.; Zhang J.; Chan, F.K.M. RIP1-Dependent and independent effects of necrostatin-1 in necrosis and T cell activation. PLoS ONE 2011, 6, e23209.
31. Christofferson, D.E.; Li, Y.; Hitomi, J.; Zhou, W.; Upperman, C.; Zhu, H.; Gerber, S.A.; Gygi, S.; Yuan, J. A novel role for RIP1 kinase in mediating TNFα production. Cell Death Dis. 2012, 3, doi:1038/cdd15.2012.64.
32. Longo, J.P.F.; Lozzi, S.P.; Simioni, A.R.; Morais, P.C.; Tedesco, A.C.; Azevedo, R.B. Photodynamic therapy with aluminum-chloro-phthalocyanine induces necrosis and vascular damage in mice tongue tumors, J. Photochem. Photobiol. B 2009, 94, 143–146.
33. Longo, J.P.F.; de Melo, L.N.D.; Mijan, M.C.; Valois, C.R.A.; Joanitti, G.A.; Simioni, A.R.; Tedesco, A.C.; de Azevedo, R.B. Photodynamic therapy mediated by liposomal chloroaluminum-phthalocyanine induces necrosis in oral cancer cells. J. Biomater. Tissue Eng. 2013, 3, 148–156.
34. Portilho, F.A.; Cavalcanti, C.E.O.; Miranda-Vilela, A.L.; Estevanato, L.L.C.; Longo, J.P.F.; Santos, M.F.M.A.; Bocca, A.L.; Martins, O.P.; Simioni, A.R.; Morais, P.C.; et al. Antitumor activity of photodynamic therapy performed with nanospheres containing zinc-phthalocyanine. J. Nanobiotechnol. 2013, 11, 41–65.
35. Wood, S.R.; Holroyd, J.A.; Brown S.B. The subcellular localization of Zn (II) phthalocyanines and their redistribution on exposure to light. Photochem. Photobiol. 1997, 65, 397–402.
36. Rada, B.; Leto, T.L. Oxidative innate immune defenses by Nox/Duox family NADPH oxidases. Contrib. Microbiol. 2008, 15, 164–187.
37. Arwert, E.N.; Hoste, E.; Watt, F.W. Epithelial stem cells, wound healing and cancer. Nat. Rev. Cancer 2012, 12, 170–180.
38. Jung, S.N.; Yang, W.K.; Kim, J.; Kim, H.S.; Kim, E.J.; Yun, H.; Park, H.; Kim, S.S.; Choe, W.; Kang, I.; et al. Reactive oxygen species stabilize hypoxia-inducible factor-1 alpha protein and stimulate transcriptional activity via AMP-activated protein kinase in DU145 human prostate cancer cells. Carcinogenesis 2008, 29, 713–721.
39. Serra, A.; Pineiro, M.; Pereira, N.; Gonsalves, A.R.; Laranjo, M.; Abrantes, M. A look at clinical applications and developments of photodynamic therapy. Oncol. Rev. 2008, 2, 235–249.
40. Brown, S.B.; Brown, E.A.; Walker, I. The present and future role of photodynamic therapy in cancer treatment. Lancet Oncol. 2004, 5, 497–508.
41. Kudinova, N.V.; Berezov, T.T. Photodynamic therapy: Search for ideal photosensitizer (in Russian). Biomed. Khim. 2009, 55, 558–569.
42. Dougherty, T.J.; Gomer, C.J.; Henderson, B.W.; Jori, G.; Kessel, D.; Korbelik, M.; Moan, J.; Peng, Q. Photodynamic therapy. J. Natl. Cancer Inst. 1998, 90, 889–905.
43. Manoto, S.L.; Abrahamse, H. Effect of a newly synthesized Zn sulfophthalocyanine derivative on cell morphology, viability, proliferation, and cytotoxicity in a human lung cancer cell line (A549). Lasers Med. Sci. 2011, 26, 523–530.
44. Mroz, P.; Szekalska, A.; Wu, M.X.; Hamblin, M.R. Photodynamic therapy of tumors can lead to development of system antigen specific immune response. PLoS ONE 2010, 5, e15194.
45. 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.; et al. Photodynamic therapy of cancer: An update CA: A cancer. J. Clin. 2011, 61, 250–281.
46. Ahn, J.C.; Biswas, R.; Moon, J.H.; Chung, P.S. Cellular uptake of 9-hydroxypheophorbide-α and its photoactivation to induce ER stress-related apoptosis in human cervical cancer cells. Lasers Med. Sci. 2014, 29, 289–299.
47. Oliveira, C.S.; Turchiello, R.; Kowaltowski, A.J.; Indig, G.L.; Baptista, M.S. Major determinants of photoinduced cell death: Subcellular localization versus photosensitization efficiency. Free Radic. Biol. Med. 2011, 51, 824–833.
48. Firdous, S.; Nawaz, M.; Ikram, M.; Ahmed, M. In vitro study of cell death with 5-aminolevulinic acid based photodynamic therapy to improve the efficiency of cancer treatment. Laser Phys. 2012, 22, 626–633.
49. Brackett, C.; Gollnick, S. Photodynamic therapy enhancement of anti-tumour immunity. Photochem. Photobiol. 2011, 83, 1063–1068.
50. Pereira, P.M.R.; Silva, S.; Cavaleiro, J.A.S.; Ribeiro, C.A.F.; Tome, J.P.C.; Fernandes, R. Galactodendritic phthalocyanine targets carbohydrate-binding proteins enhancing photodynamic therapy. PLoS ONE 2014, 9, e95529.
51. Dent, C.E.; Linstead, P.R.; Lowe, A.R. Phthalocyanines. Part VI. The structure of the phthalocyanines. J. Chem. Soc. 1934, 1033–1039, doi:10.1039/JR9340001033.
52. Guillaud, G.; Simon, J.; Germain, J.P. Metallophthalocyanines: Gas sensors, resistors and field effect transistors. Coord. Chem. Rev. 1998, 178–180, 1433–1484.
53. Allen, C.M.; Sharman, W.M.; van Lier, J.E. Current status of phthalocyanines in the photodynamic therapy of cancer. J. Porphyr. Phthalocyanines 2001, 5, 161–169.
54. Coupienne, I.; Fettweis, G.; Piette, J. RIP3 expression induces a death profile change in U2OS osteosarcoma cells after 5-ALA-PDT. Lasers Surg. Med. 2011, 43, 557–564.
55. Coupienne, I.; Fettweis, G.; Rubio, N.; Agostinis, P.; Piette, J. 5-ALA-PDT induces RIP3-dependent necrosis in glioblastoma. Photochem. Photobiol. Sci. 2011, 10, 1868–1878.
56. Scheer, H.; Inhoffen, H.H. In The Porphyrins; Dolphin, D., Ed.; Academic Press: New York, NY, USA, 1978; Volume 2; pp. 45–62.
57. Sternberg, E.D.; Dolphin, D. Porphyrin-based photosensitizers for use in photodynamic therapy. Tetrahedron 1988, 54, 4151–4202.
58. Barrett, P.A.; Dent, C.E.; Linstead, R.P. Phthalocyanines. Part VII. Phthalocyanine as a co-ordinating group. A general investigation of the metallic derivatives. J. Chem. Soc. 1934, 179, 1718–1736.
59. Cid, J.-J.; Yum, J.-H.; Jang, S.-R.; Nazeeruddin, M.K.; Martinez-Ferrero, E.; Palomares, E.; Ko, J.; Graetzel, M.; Torres, T. Molecular cosensitization for efficient panchromatic dye-sensitized solar cells. Angew. Chem. Int. Ed. 2007, 46, 8358–8362.
60. Kadish, K.M.; Smith, K.M.; Guilard, R. The Porphyrin Handbook; Academic Press: San Diego, CA, USA, 2003.
61. Pinzon, J.R.; Plonska-Brzezinska, M.E.; Cadona, C.M.; Athans, A.J.; Gayathri, S.S.; Guldi, D.M.; Herranz, M.A.; Martin, N.; Torres, T.; Echegoyen, L. Sc3N@C80-ferrocene electrondonor/acceptor conjugates as promising materials for photovoltalic applications. Angew. Chem. Int. Ed. 2008, 47, 4173–4176.
62. Campidelli, S.; Ballesteros, B.; Filoramo, A.; Diaz, D.; de la Torre, G.; Torres, T.; Rahman, G.M.A.; Aminur, E.C.; Kiessling, D.; Werner, F.; et al. Facile decoration of functionalized single-wall carbon nanotubes with phthalocyanines via “Click Chemistry”. J. Am. Chem. Soc. 2008, 130, 11503–11509.
63. Whitacre, C.M.; Feyes, D.K.; Satoh, T.; Grossmann, J.; Mulvihill, J.W.; Mukhtar, H.; Oleinick, N.L. Photodynamic therapy with the phthalocyanine photosensitizer Pc 4 of SW480 human colon cancer xenografts in athymic mice. Clin. Cancer Res. 2000, 6, 2021–2027.
64. Velloso, N.V.; Muehlmann, L.A.; Longo, J.P.F.; Silva, J.R.D.; Zancanela, D.C.; Tedesco, A.C.; Azevedo, R.B.D. Aluminum-phthalocyanine chloride-based photodynamic therapy inhibits PI3K/Akt/Mtor pathway in oral squamous cell carcinoma cells in vitro. Chemo 2012, 1, 107–111.
65. Staicu, A.; Pascu, A.; Nuta, A.; Sorescu, A.; Raditoiu, V.; Pascu, M.L. Studies about phthalocyanine photosensitizers to be used in photodynamic therapy. Romanian Rep. Phys. 2013, 65, 1032–1051.
66. Manoto, S.L.; Sekhejane, P.R.; Houreld, N.N.; Abrahamse, H. Localization and phototoxic effect of zinc sulfophthalocyanine photosensitizer in human colon (DLD-1) and lung (A549) carcinoma cells (in vitro). Photodiagn. Photodyn. Ther. 2012, 9, 52–59.
67. Mfouo-Tynga, I.; Houreld, N.N.; Abrahamse, H. The primary subcellular localization of Zinc phthalocyanine and its cellular impact on viability, proliferation and structure of breast cancer cells (MCF-7). J. Photochem. Photobiol. B 2012, 120, 171–176.
68. Manoto, S.L.; Houreld, N.N.; Abrahamse, H. Phototoxic effect of photodynamic therapy on lung cancer cells grown as a monolayer and three dimensional multicellular spheroids. Lasers Surg. Med. 2013, 45, 186–194.
69. Abrahamse, H.; Kresfelder, T.; Horne, T.; Cronje, M.; Nyokong, T. Apoptotic inducing ability of a novel photosensitizing agent, Ge sulfophthalocyanine, on oesophageal and breast cancer cell lines. In Optical Methods for Tumor Treatment and Detection: Mechanisms and Techniques in Photodynamic Therapy XV. In Proceedings of the SPIE, San Jose, CA, USA, 21 January 2006; Kessel, D., Ed.; SPIE: Bellingham, WA, USA, 2006; 613904, doi:10.1117/12.641604.
70. Seotsanyana-Mokhosi, I.; Kresfelder, T.; Abrahamse, H.; Nyokong, T. The effect of Ge, Si and Sn phthalocyanine photosensitizers on cell proliferation and viability of human oesophageal carcinoma cells. J. Photochem. Photobiol. B 2006, 83, 55–62.