Mitochondria are a primary target of hypericin phototoxicity: Synergy of intracellular calcium mobilisation in cell killing

International Journal of Biochemistry and Cell Biology

Volumn 38, Issue 11, 2006, Pages 1946-1956

  Theodossiou, Theodossis A ^a   Noronha Dutra, Alberto ^a   Hothersall, John S ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Calcium; Glutathione; Hypericin photocytotoxicity; Mitochondria; Photodynamic therapy

Indexed keywords

ACONITATE HYDRATASE; BETA N ACETYLHEXOSAMINIDASE; CALCIUM ION; FORMAZAN; GLUTAMATE CYSTEINE LIGASE; GLUTATHIONE; HYDROGEN PEROXIDE; HYPERICIN; IONOMYCIN; LYSOSOME ENZYME; SUPEROXIDE DISMUTASE; TETRAZOLIUM; CALCIUM; DRUG DERIVATIVE; PERYLENE; RADIOSENSITIZING AGENT; REACTIVE OXYGEN METABOLITE;

ANTINEOPLASTIC ACTIVITY; ARTICLE; CALCIUM CELL LEVEL; CALCIUM MOBILIZATION; CALCIUM TRANSPORT; CELL KILLING; CELL LOSS; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOSOL; CYTOTOXICITY; DRUG EFFECT; DRUG MECHANISM; ENZYME ACTIVITY; HUMAN; HUMAN CELL; IRRADIATION; LIGHT IRRADIANCE; MALE; MITOCHONDRION; OXIDATION; PHOTOTOXICITY; PROSTATE CANCER; CELL RESPIRATION; CELL SURVIVAL; CYTOPLASM; LIGHT; METABOLISM; RADIATION EXPOSURE; RADIATION RESPONSE; TUMOR CELL LINE;

HYPERICUM;

ACONITATE HYDRATASE; CALCIUM; CELL LINE, TUMOR; CELL RESPIRATION; CELL SURVIVAL; CYTOPLASM; DOSE-RESPONSE RELATIONSHIP, RADIATION; GLUTATHIONE; HUMANS; HYDROGEN PEROXIDE; LIGHT; MALE; MITOCHONDRIA; PERYLENE; RADIATION-SENSITIZING AGENTS; REACTIVE OXYGEN SPECIES; SUPEROXIDE DISMUTASE;

EID: 33748645097     PISSN: 13572725     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biocel.2006.05.009     Document Type: Article

References (35)

1. Agostinis P., Vandenbogaerde A., Donella-Deana A., Pinna L.A., Lee K.T., Goris J., et al. Photosensitized inhibition of growth factor-regulated protein kinases by hypericin. Biochem. Pharmacol. 49 (1995) 1615-1622
2. Ali S.M., Chee S.K., Yuen G.Y., and Olivo M. Hypericin induced death receptor-mediated apoptosis in photoactivated tumor cells. Int. J. Mol. Med. 9 (2002) 601-616
3. Ali S.M., Chee S.K., Yuen G.Y., and Olivo M. Hypocrellins and hypericin induced apoptosis in human tumor cells: A possible role of hydrogen peroxide. Int. J. Mol. Med. 9 (2002) 461-472
4. Ali S.M., and Olivo M. Bio-distribution and subcellular localization of hypericin and its role in PDT induced apoptosis in cancer cells. Int. J. Oncol. 21 (2002) 531-540
5. Beinert H., Kennedy M.C., and Stout C.D. Aconitase as iron-sulfur protein, enzyme, and iron-regulatory protein. Chem. Rev. 96 (1996) 2335-2374
6. Bolkent S., and Zierold K. Effects of the ionophores valinomycin, ionomycin and gramicidin A on the element compartmentation in cultured rat hepatocytes. Toxicol. In Vitro 16 (2002) 159-165
7. Bulteau A.L., Ikeda-Saito M., and Szweda L.I. Redox-dependent modulation of aconitase activity in intact mitochondria. Biochemistry 42 (2003) 14846-14855
8. Chakraborti T., Das S., Mondal M., Roychoudhury S., and Chakraborti S. Oxidant, mitochondria and calcium: An overview. Cell Signal. 11 (1999) 77-85
9. Chaloupka R., Obsil T., Plasek J., and Sureau F. The effect of hypericin and hypocrellin-A on lipid membranes and membrane potential of 3T3 fibroblasts. Biochim. Biophys. Acta 1418 (1999) 39-47
10. Diwu Z., and Lown J.W. Photosensitization with anticancer agents. 17. EPR studies of photodynamic action of hypericin: Formation of semiquinone radical and activated oxygen species on illumination. Free Radic. Biol. Med. 14 (1993) 209-215
11. Ehrenberg B., Anderson J.L., and Foote C.S. Kinetics and yield of singlet oxygen photosensitized by hypericin in organic and biological media. Photochem. Photobiol. 68 (1998) 135-140
12. English D.S., Doyle R.T., Petrich J.W., and Haydon P.G. Subcellular distributions and excited-state processes of hypericin in neurons. Photochem. Photobiol. 69 (1999) 301-305
13. Escobar J.A., Rubio M.A., and Lissi E.A. Sod and catalase inactivation by singlet oxygen and peroxyl radicals. Free Radic. Biol. Med. 20 (1996) 285-290
14. Flint D.H., Tuminello J.F., and Emptage M.H. The inactivation of Fe-S cluster containing hydrolyases by superoxide. J. Biol. Chem. 268 (1993) 22369-22376
15. Gardner P.R. Aconitase: Sensitive target and measure of superoxide 497. Meth. Enzymol. 349 (2002) 9-23
16. Hadjur C., Richard M.J., Parat M.O., Favier A., and Jardon P. Photodynamically induced cytotoxicity of hypericin dye on human fibroblast cell line MRC5. J. Photochem. Photobiol. B 27 (1995) 139-146
17. Hadjur C., Richard M.J., Parat M.O., Jardon P., and Favier A. Photodynamic effects of hypericin on lipid peroxidation and antioxidant status in melanoma cells. Photochem. Photobiol. 64 (1996) 375-381
18. Hoek J.B., Farber J.L., Thomas A.P., and Wang X. Calcium ion-dependent signalling and mitochondrial dysfunction: Mitochondrial calcium uptake during hormonal stimulation in intact liver cells and its implication for the mitochondrial permeability transition. Biochim. Biophys. Acta 1271 (1995) 93-102
19. Hothersall J.S., Cunha F.Q., Neild G.H., and Norohna-Dutra A.A. Induction of nitric oxide synthesis in J774 cells lowers intracellular glutathione: Effect of modulated glutathione redox status on nitric oxide synthase induction. Biochem. J. 322 (1997) 477-481
20. Johnson S.A., and Pardini R.S. Antioxidant enzyme response to hypericin in EMT6 mouse mammary carcinoma cells. Free Radic. Biol. Med. 24 (1998) 817-826
21. Kim S.Y., Kwon O.J., and Park J.W. Inactivation of catalase and superoxide dismutase by singlet oxygen derived from photoactivated dye. Biochimie 83 (2001) 437-444
22. Lax A., Soler F., and Fernandez-Belda F. Intracellular ca(2+) pools and fluxes in cardiac muscle-derived h9c2 cells. J. Bioenerg. Biomembr. 37 (2005) 249-259
23. Landegren U. Measurement of cell numbers by means of the endogenous enzyme hexosaminidase. Applications to detection of lymphokines and cell surface antigens. J. Immunol. Meth. 67 (1984) 379-388
24. Miccoli L., Beurdeley-Thomas A., De P.G., Sureau F., Oudard S., Dutrillaux B., et al. Light-induced photoactivation of hypericin affects the energy metabolism of human glioma cells by inhibiting hexokinase bound to mitochondria. Cancer Res. 58 (1998) 5777-5786
25. 2+ influx by stimulating store-regulated cation entry and not by a direct action at the plasma membrane. Biochem. J. 300 Pt 3 (1994) 665-672
26. Nicholls D.G. Simultaneous monitoring of ionophore- and inhibitor-mediated plasma and mitochondrial membrane potential changes in cultured neurons. J. Biol. Chem. 281 (2006) 14864-14874
27. Schapira A.H. Mitochondrial involvement in Parkinson's disease, Huntington's disease, hereditary spastic paraplegia and Friedreich's ataxia. Biochim. Biophys. Acta 1410 (1999) 159-170
28. Siboni G., Weitman H., Freeman D., Mazur Y., Malik Z., and Ehrenberg B. The correlation between hydrophilicity of hypericins and helianthrone: Internalization mechanisms, subcellular distribution and photodynamic action in colon carcinoma cells. Photochem. Photobiol. Sci. 1 (2002) 483-491
29. Sureau F., Miskovsky P., Chinsky L., and Turpin P. Hypericin-induced cell photosensitization involves an intracellular pH decrease. J. Am. Chem. Soc. 118 (1996) 9484-9487
30. Theodossiou T., Spiro M.D., Jacobson J., Hothersall J.S., and MacRobert A.J. Evidence for intracellular aggregation of hypericin and the impact on its photocytotoxicity in PAM 212 murine keratinocytes. Photochem. Photobiol. 80 (2004) 438-443
31. Thomas C., MacGill R.S., Miller G.C., and Pardini R.S. Photoactivation of hypericin generates singlet oxygen in mitochondria and inhibits succinoxidase. Photochem. Photobiol. 55 (1992) 47-53
32. Thomas C., and Pardini R.S. Oxygen dependence of hypericin-induced phototoxicity to EMT6 mouse mammary carcinoma cells. Photochem. Photobiol. 55 (1992) 831-837
33. Uzdensky A.B., Ma L.W., Iani V., Hjortland G.O., Steen H.B., and Moan J. Intracellular localisation of hypericin in human glioblastoma and carcinoma cell lines. Lasers Med. Sci. 16 (2001) 276-283
34. Vasquez-Vivar J., Kalyanaraman B., and Kennedy M.C. Mitochondrial aconitase is a source of hydroxyl radical. An electron spin resonance investigation. J. Biol. Chem. 275 (2000) 14064-14069
35. Yan L.J., Levine R.L., and Sohal R.S. Oxidative damage during aging targets mitochondrial aconitase. Proc. Natl. Acad. Sci. U.S.A. 94 (1997) 11168-11172