Oxidative modification induced by photodynamic therapy with Photofrin®II and 2-methoxyestradiol in human ovarian clear carcinoma (OvBH-1) and human breast adenocarcinoma (MCF-7) cells

Biomedicine and Pharmacotherapy

Volumn 71, Issue , 2015, Pages 30-36

  Saczko, Jolanta ^a   Choromańska, Anna ^a   Rembiałkowska, Nina ^a   Dubińska Magiera, Magda ^b   Bednarz Misa, Iwona ^a   Bar, Julia ^a   Marcinkowska, Anna ^a   Kulbacka, Julita ^a  

^a WROCLAW MEDICAL UNIVERSITY   (Poland)

^b UNIVERSITY OF WROC AW   (Poland)

Author keywords

2 Methoxyestradiol; Breast adenocarcinoma; Cytoskeleton; Heat shock proteins; Ovarian carcinoma; Photodynamic reaction; Photofrin II

Indexed keywords

2 METHOXYESTRADIOL; HEAT SHOCK PROTEIN 27; HEAT SHOCK PROTEIN 70; PHOTOFRIN II; REACTIVE OXYGEN METABOLITE; UBIQUITIN PROTEIN LIGASE; 2-METHOXYESTRADIOL; ESTRADIOL; INDUCIBLE NITRIC OXIDE SYNTHASE;

ARTICLE; BREAST ADENOCARCINOMA; COMPARATIVE STUDY; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOSKELETON; FEMALE; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; LIPID MEMBRANE; MCF 7 CELL LINE; OVARY CARCINOMA; OXIDATION; OXIDATIVE STRESS; PHOTODYNAMIC THERAPY; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; UNFOLDED PROTEIN RESPONSE; WESTERN BLOTTING; ADENOCARCINOMA; ANALOGS AND DERIVATIVES; BREAST NEOPLASMS; DRUG EFFECTS; IMMUNOHISTOCHEMISTRY; METABOLISM; OVARIAN NEOPLASMS; OXIDATION REDUCTION REACTION; PATHOLOGY; PHOTOCHEMOTHERAPY; TUMOR CELL LINE;

ADENOCARCINOMA; BLOTTING, WESTERN; BREAST NEOPLASMS; CELL LINE, TUMOR; CYTOSKELETON; DIHEMATOPORPHYRIN ETHER; ESTRADIOL; FEMALE; HSP27 HEAT-SHOCK PROTEINS; HSP70 HEAT-SHOCK PROTEINS; HUMANS; IMMUNOHISTOCHEMISTRY; NITRIC OXIDE SYNTHASE TYPE II; OVARIAN NEOPLASMS; OXIDATION-REDUCTION; PHOTOCHEMOTHERAPY;

EID: 84928966725     PISSN: 07533322     EISSN: 19506007     Source Type: Journal    
DOI: 10.1016/j.biopha.2015.02.008     Document Type: Article

References (52)

1. Kusakari T., Kariya M., Mandai M., Tsuruta Y., Hamid A.A., Fukuhara K., et al. C-erbB-2 or mutant Ha-ras induced malignant transformation of immortalized human ovarian surface epithelial cells in vitro. Br J Cancer 2003, 89:2293-2298.
2. Allison R.R., Cuenca R., Downie G.H., Randall M.E., Bagnato V.S., Sibata C.H. PD/PDT for gynecological disease: a clinical review. Photodiagnosis Photodyn Ther 2005, 2(1):51-63.
3. Castano A.P., Demidova T.N., Hamblin M.R. Mechanisms in photodynamic therapy: Part two - Cellular signaling, cell metabolism and modes of cell death. Photodiagnosis Photodyn Ther 2005, 2:1-23.
4. Allison R.R., Bagnato R., Cuenca G.H., Downie G.H., Sibata C.H. The future of photodynamic therapy in oncology. Future Oncol 2006, 2:53-71.
5. Synder J.W., Greco W.R., Bellnier D.A., Vaughan L., Henderson B.W. Photodynamic therapy: a means to enhanced drug delivery to tumors. Cancer Res 2003, 63:8126-8131.
6. Oleinick N.L., Morris R.L., Belichenko I. The role of apoptosis in response to photodynamic therapy: what, where, why, and how. Photochem Photobiol Sci 2002, 1:1-21.
7. Saczko J., Chwiłkowska A., Ługowski M., Banaś T. Levels of lipid peroxidation in A549 cells after PDT in vitro. Rocz Akad Med Bialymst 2004, 49(Suppl. 1):82-84.
8. Girotti A.W. Photosensitized oxidation of membrane lipids: reaction pathways, cytotoxic effects, and cytoprotective mechanisms. Photochem Photobiol 2001, 63:103-113.
9. Golab J., Nowis D., Skrzycki M., Czeczot H., Baranczyk-Kuzma A., Wilczynski G.M., et al. Antitumor effects of photodynamic therapy are potentiated by 2-metoxyestradiol, a superoxide dismutase inhibitor. J Biol Chem 2003, 278:407-414.
10. Saczko J., Kulbacka J., Chwilkowsa A., Pola A., Lugowski M., Marcinkowska A., et al. Cytosolic superoxide dismutase activity after photodynamic therapy, intracellular distribution of Photofrin II and hypericin, and P-glycoprotein localization in human colon adenocarcinoma. Folia Histochem Cytobiol 2007, 45(2):93-98.
11. Dolgachev V., Oberley L.W., Huang T.T., Kraniak J.M., Tainsky M.A., Hanada K., et al. A role for manganese superoxide dismutase in apoptosis after photosensitization. Biochem Biophys Res Commun 2005, 332:411-417.
12. Mooberry S.L. Mechanism of action of 2-methoxyestradiol: new developments. Drug Resist Updat 2003, 6:355-561.
13. Wang P., Chen H., Qin H., Sankarapandi S., Becher M.W., Wong P.C., et al. Overexpression of human copper, zinc-superoxide dismutase (SOD1) prevents postischemic injury. Proc Natl Acad Sci USA 1998, 95:4556-4560.
14. Tinley T.L., Leal R.M., Randall-Hlubek D.A., Cessae J.W., Wilkens L.R., Rao P.N., et al. Novel 2 - methoxestradiol analogues with antitumor activity. Cancer Res 2003, 63:1538-1549.
15. Perez-Stable C. 2-Methoxyestradiol and paclitaxel have similar effects on the cell cycle and induction apoptosis in prostate cancer cells. Cancer Lett 2006, 231(1):49-64.
16. Saczko J., Mazurkiewicz M., Chwiłkowska A., Kulbacka J., Kramer G., Ługowski M., et al. Intracellular distribution of Photofrin in malignant and normal endothelial cell lines. Folia Biol (Praha) 2007, 53(1):7-12.
17. Song So S., Xing D., Zhou F.F., Chen W.R. PDT-treated apoptotic cells induce macrophage synthesis NO. Proc. SPIE 7507, 2009 International Conference on Optical Instruments and Technology: Optical Trapping and Microscopic Imaging 2009, 10.1117/12.838105.
18. Bar J.K., Saczko J., Ziółkowski P., Chwiłkowska A., Słomska I., Drąg Zalesiñska M., et al. Photofrin II-based photosensitization of human ovarian clear-cell carcinoma cell line (OvBH-1). Pharmacol Rep 2007, 59:150-160.
19. Bar J.K., Harlozinska A., Kartarius S., Montenarh M., Wyrodek E., Parkitna J.M., et al. Temperature-sensitive ovarian carcinoma cell line (OvBH-1). Jpn J Cancer Res 2002, 93(9):976-985.
20. Robertson C.A., Hawkins Evans D., Abrahamse H. Photodynamic therapy (PDT): a short review on cellular mechanisms and cancer research applications for PDT. J Photochem Photobiol B: Biol 2009, 96:1-8.
21. Almeida R.D., Manadas B.J., Carvalho A.P., Duarte C.B. Intracellular signaling mechanisms in photodynamic therapy. Biochim Biophys Acta 2004, 1704:59-86.
22. Dougherty T.J., Gomer G.J., Henderson B.W., Jori G., Kessel D., Korbelik M., et al. J Natl Cancer Inst 1998, 90:889-905.
23. Nowis D., Makowski M., Stokłosa T., Legat M., Issat T., Gołąb J. Direct tumor damage mechanisms of photodynamic therapy. Acta Biochim Pol 2005, 52:339-352.
24. Luksiene Z., de Witte P.A. Hypericin as novel and promising photodynamic therapy tool: studies on intracellular accumulation capacity and growth inhibition efficiency. Medicina (Kaunas) 2003, 39(7):677-682.
25. Nowis D., Szokalska A., Makowski M., Winiarska M., Gołąb J. Improvement of antitumor activity of photodynamic therapy through inhibition of cytoprotective mechanism in tumor cells. Proc of SPIE, vol. 7380 2009, 73804F. D.H. Kessel (Ed.).
26. Gilaberte Y., Pereboom D., Carapeto F.J., Alda J.O. Flow cytometry study of the role of superoxide anion and hydrogen peroxide in cellular photodestruction with 5-aminolevulinic acid-induced protoporphyrin IX. Photodermatol Photoimmunol Photomed 1997, 13(1-2):43-49.
27. Lala P.K., Charkraborty C. Role of nitric oxide for cancer therapy. Lancet Oncol 2001, 3:149-156.
28. Thomsen L.L., Lawton F.G., Knowles R.G., Beesley J.E., Riveros-Moreno V., Moncada S. Nitric oxide synthase activity in human gynecological cancer. Cancer Res 1994, 54:1352-1354.
29. Ambrosio G., Zweier J.L., Becker L.C. Apoptosis is prevented by administration of superoxide dismutase in dogs with reperfused myocardial infraction. Basic Res Cardiol 1998, 93:94-96.
30. Shi J., Wang Z., Wang L., Wang H., Li L., Yu X., et al. Photodynamic therapy of a 2-methoxyestradiol tumor-targeting drug delivery system mediated by Asn-Gly-Arg in breast cancer. Int J Nanomed 2013, 8:1551-1562.
31. Huang P., Feng L., Oldham E.A., Keating M.J., Plunket W. Superoxide dismutase as a target for the selective killing of cancer cells. Nature 2000, 407(6802):390-395.
32. Huober J.B., Nakamura S., Meyen R., Roth J.A., Mukhopadhyay T. Oral administration of an estrogen metabolite-induced potentiation of radiation antitumor effects in presence of wide-type p53 in non small-cell lung cancer. Int J Radiat Oncol Biol Phys 2000, 48(4):1127-1137.
33. Sporn L.A., Foster T.H. Photofrin and light induces microtubule depolymerization in cultured human endothelial cells. Cancer Res 1992, 52(12):3443-3448.
34. Uzdensky A., Kristiansen B., Moan J., Juzeniene A. Dynamics of signaling, cytoskeleton and cell cycle regulation proteins in glioblastoma cells after sub-lethal photodynamic treatment: antibody microarray study. Biochim Biophys Acta 2012, 1820(7):795-803.
35. Machado A.H., Moraes K.C., Pacheco Soares C., Junior M.B., da Silva N.S. Cellular changes after photodynamic therapy on HEp-2 cells using the new ZnPcBr(8) phthalocyanine. Photomed Laser Surg 2010, (Suppl. 1):S143-S149.
36. Hirst D., Robson T. Targeting nitric oxide for cancer therapy. J Pharm Pharmacol 2007, 59:3-13.
37. Mocellin S., Bronte V., Nitti D. Nitric oxide, a double-edged sword in cancer biology: searching for therapeutic opportunities. Med Res Rev 2007, 27(3):317-352.
38. Korbelik M., Parkins C.S., Shibuya H., Cecic I., Stratford M.R., Chaplin D.J. Nitric oxide production by tumor tissue. Br J Cancer 2000, 82:1835-1843.
39. Rapozzi V., Della Pietra E., Zorzet S., Zacchigna M., Bonavida B., Xodo L.E. Nitric oxide-mediated activity in anti-cancer photodynamic therapy. Nitric Oxide 2013, 30:26-35.
40. Reeves K.J., Reed M.W.R., Brown N.J. It is nitric oxide important in photodynamic therapy?. J Photochem Photobiol 2009, 95:141-147.
41. Fukumura D., Jain R.K. Role of nitric oxide in tumor microcirculation. Blood flow, vascular permeability and leucocyte-endothelial interactions. Am J Pathol 1997, 150:713-725.
42. Lu Z., Tao Z.Y., Zhou Z., Zhang J., Li C., Ou L., et al. Mitochondrial reactive oxygen species and nitric oxide-mediated cancer cell apoptosis in 2-butylamino-2-demethoksyhypocellin B photodynamic treatment. Free Radic 2006, 41:1590-1605.
43. Thomsen L.L., Miles D.W., Happerfield L., Bobrow L.G., Knowles R.G., Moncada S. Nitric oxide synthase activity in human breast cancer. Br J Cancer 1995, 72:41-44.
44. Caneba C.A., Yang L., Baddour J., Curtis R., Win J., Hartig S., et al. Nitric oxide is a positive regulator of the Warburg effect in ovarian cancer cells. Cell Death Dis 2014, 5:e1302. 10.1038/cddis.2014.264.
45. Lechner M., Lirk P., Rieder J. Inducible nitric oxide synthase (iNOS) in tumor biology: the two sides of the same coin. Semin Cancer Biol 2005, 15(4):277-289.
46. Brennan P.A., Moncada S. From pollutant gas to biological messenger: the diverse actions of nitric oxide in cancer. Ann R Coll Surg Engl 2002, 84(2):75-78.
47. Ambs S., Merriam W.G., Ogunfusika M.O., Bennett W.P., Ishibe N., Hussain S.P., et al. p53 and vascular endothelial growth factor regulate tumor growth of NOS2-expressing human carcinoma cells. Nat Med 1998, 4(12):1371-1376.
48. Brodsky J.L., Chiosis G. Hsp70 molecular chaperones: emerging roles in human disease and identification of small molecule modulators. Curr Top Med Chem 2006, 6:1215-1225.
49. Aliya S., Reddanna P., Thyagaraju K. Does glutathione S-transferase Pi (GST-Pi) a marker protein for cancer?. Mol Cell Biochem 2003, 253(1-2):319-327.
50. Luna M.C., Ferrario A., Wong S., Fisher A.M., Gomer C.J. Photodynamic therapy-mediated oxidative stress as a molecular switch for the temporal expression of genes ligated to the human heat shock promoter. Cancer Res 2000, 60(6):1637-1644.
51. Leu J.I., Pimkina J., Frank A., Murphy M.E., George D.L. A small molecule inhibitor of inducible heat shock protein 70. Mol Cell 2009, 36(1):15-27.
52. Szokalska A., Makowski M., Nowis D., Wilczyński G.M., Kujawa M., Wójcik C., et al. Proteasome inhibition potentiates antitumor effects of photodynamic therapy in mice through induction of endoplasmic reticulum stress and unfolded protein response. Cancer Res 2009, 69:4235-4423.