Active oxygen intermediates in the degradation of hematoporphyrin derivative in tumor cells subjected to photodynamic therapy

Journal of Photochemistry and Photobiology B: Biology

Volumn 93, Issue 2, 2008, Pages 94-107

  Chekulayeva, Lyudmila V ^a   Chekulayev, Vladimir A ^a   Shevchuk, Igor N ^a  

^a TALLINN UNIVERSITY OF TECHNOLOGY   (Estonia)

Author keywords

Hematoporphyrin derivative; Photobleaching; Photodynamic therapy; Reactive oxygen species; Tumor

Indexed keywords

BENZOIC ACID; CATALASE; COPPER ZINC SUPEROXIDE DISMUTASE; DEFEROXAMINE; GLUTATHIONE; HEMATOPORPHYRIN DERIVATIVE; HYDROGEN PEROXIDE; HYDROXYL RADICAL; MANNITOL; PEROXIDE; PHOSPHATE; PHOSPHATE BUFFERED SALINE; PHOTOSENSITIZING AGENT; REACTIVE OXYGEN METABOLITE; SUPEROXIDE; TIRON;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIOXIDANT ACTIVITY; ARTICLE; BLEACHING; CONTROLLED STUDY; DRUG MECHANISM; EHRLICH ASCITES TUMOR CELL; FEMALE; IRRADIATION; MOUSE; NONHUMAN; OXIDATION; OXIDATION REDUCTION REACTION; PHOTODYNAMIC THERAPY; PHOTOSENSITIZATION; PRIORITY JOURNAL; RED LIGHT;

ANIMALS; CARCINOMA, EHRLICH TUMOR; CATALASE; DEUTERIUM OXIDE; DRUG STABILITY; FEMALE; GLUTATHIONE; HEMATOPORPHYRIN DERIVATIVE; KINETICS; MICE; PHOTOBLEACHING; PHOTOCHEMICAL PROCESSES; PHOTOCHEMOTHERAPY; PHOTOLYSIS; PHOTOSENSITIZING AGENTS; REACTIVE OXYGEN SPECIES; SUPEROXIDE DISMUTASE;

EID: 54849434815     PISSN: 10111344     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jphotobiol.2008.07.003     Document Type: Article

References (65)

1. Dougherty T.J., Gomer C.J., Henderson B.W., Jori G., Kessel D., Korbelik M., Moan J., and Peng Q. Photodynamic therapy. JNCI 90 (1998) 889-905
2. Juzeniene A., Peng Q., and Moan J. Milestones in the development of photodynamic therapy and fluorescence diagnosis. Photochem. Photobiol. Sci. 6 (2007) 1234-1245
3. Chekulayeva L.V., Shevchuk I.N., Chekulayev V.A., and Ilmarinen K. Hydrogen peroxide, superoxide, and hydroxyl radicals are involved in the phototoxic action of hematoporphyrin derivative against tumor cells. J. Environ. Pathol. Toxicol. Oncol. 25 (2006) 51-77
4. Pandey R.K., Siegel M.M., Tsao R., McReynolds J.H., and Dougherty T.J. Fast atom bombardment mass spectral analyses of Photofrin II and its synthetic analogs. Biomed. Environ Mass Spectrom. 19 (1990) 405-414
5. Weishaupt K.R., Gomer C.J., and Dougherty T.J. Identification of singlet oxygen as the cytotoxic agent in photoinactivation of a murine tumor. Cancer Res. 36 (1976) 2326-2329
6. Moan J. Effect of bleaching of porphyrin sensitizers during photodynamic therapy. Cancer Lett. 33 (1986) 45-53
7. Boyle D.G., and Potter W.R. Photobleaching of photofrin II as a means of eliminating skin photosensitivity. Photochem. Photobiol. 46 (1987) 997-1001
8. Mang T.S., Dougherty T.J., Potter W.R., Boyle D.G., Somer S., and Moan J. Photobleaching of porphyrins used in photodynamic therapy and implications for therapy. Photochem. Photobiol. 45 (1987) 501-506
9. Georgakoudi I., Nichols M.G., and Foster T.H. The mechanism of Photofrin photobleaching and its consequences for photodynamic dosimetry. Photochem. Photobiol. 65 (1997) 135-144
10. Moan J., and Kessel D. Photoproducts formed from photofrin II in cells. J. Photochem. Photobiol B 1 (1988) 429-436
11. Dysart J.S., and Patterson M.S. Characterization of Photofrin photobleaching for singlet oxygen dose estimation during photodynamic therapy of MLL cells in vitro. Phys. Med. Biol. 50 (2005) 2597-2616
12. Golab J., Nowis D., Skrzycki M., Czeczot H., Baranczyk-Kuzma A., Wilczynski G.M., Makowski M., Mroz P., Kozar K., Kaminski R., Jalili A., Kopec M., Grzela T., and Jakobisiak M. Antitumor effects of photodynamic therapy are potentiated by 2-methoxyestradiol. A superoxide dismutase inhibitor. J. Biol. Chem. 278 (2003) 407-414
13. Athar M., Elmets C.A., Bickers D.R., and Mukhtar H. A novel mechanism for the generation of superoxide anions in hematoporphyrin derivative-mediated cutaneous photosensitization. J. Clin. Invest. 83 (1989) 1137-1143
14. Korbelik M., Sun J., and Zeng H. Ischaemia-reperfusion injury in photodynamic therapy-treated mouse tumours. Br. J. Cancer 88 (2003) 760-766
15. Schafer F.Q., and Buettner G.R. Singlet oxygen toxicity is cell line-dependent: a study of lipid peroxidation in nine leukemia cell lines. Photochem. Photobiol. 70 (1999) 858-867
16. Shevchuk I.N., Chekulayev V.A., and Chekulayeva L.V. The role of lipid peroxidation and protein degradation in the photodestruction of Ehrlich ascites carcinoma cells sensitized by hematoporphyrin derivative. Exp. Oncol. 24 (2002) 216-224
17. Silvester J.A., Timmins G.S., and Davies M.J. Protein hydroperoxides and carbonyl groups generated by porphyrin-induced photo-oxidation of bovine serum albumin. Arch. Biochem. Biophys. 350 (1998) 249-258
18. Wright A., Bubb W.A., Hawkins C.L., and Davies M.J. Singlet oxygen-mediated protein oxidation: evidence for the formation of reactive side chain peroxides on tyrosine residues. Photochem. Photobiol. 76 (2002) 35-46
19. Gebicki S., and Gebicki J.M. Crosslinking of DNA and proteins induced by protein hydroperoxides. Biochem. J. 338 Pt 3 (1999) 629-636
20. Ostdal H., Davies M.J., and Andersen H.J. Reaction between protein radicals and other biomolecules, Free Radic. Biol. Med. 33 (2002) 201-209
21. Kessel D., Thompson P., Musselman B., and Chang C.K. Chemistry of hematoporphyrin-derived photosensitizers. Photochem. Photobiol. 46 (1987) 563-568
22. Gutteridge J.M.C. Thiobarbituric acid-reactivity following iron-dependent free-radical damage to amino acids and carbohydrates. FEBS Lett. 128 (1981) 343-346
23. Gay C., Collins J., and Gebicki J.M. Hydroperoxide assay with the ferric-xylenol orange complex. Anal. Biochem. 273 (1999) 149-155
24. Gebicki J.M., Du J., Collins J., and Tweeddale H. Peroxidation of proteins and lipids in suspensions of liposomes, in blood serum, and in mouse myeloma cells. Acta Biochim. Pol. 47 (2000) 901-911
25. Aebi H. Catalase in Vitro. Methods in Enzymol. 105 (1984) 121-126
26. Pinto R.E., and Bartley W. The effect of age and sex on glutathione reductase and glutathione peroxidase activities and on aerobic glutathione oxidation in rat liver homogenates. Biochem. J. 112 (1969) 109-115
27. Paglia D.E., and Valentine W.N. Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J. Lab. Clin. Med. 70 (1967) 158-169
28. Chekulayeva L.V., Shevchuk I.N., and Chekulayev V.A. Influence of temperature on the efficiency of photodestruction of Ehrlich ascites carcinoma cells sensitized by hematoporphyrin derivative. Exp. Oncol. 26 (2004) 125-139
29. Oberley L.W., and Spitz D.R. Assay of superoxide dismutase activity in tumour tissue. Methods in Enzymol. 105 (1984) 457-464
30. Shevchuk I., Chekulayev V., and Chekulayeva L. Enhancement of the efficiency of photodynamic therapy of tumours by t-butyl-4-hydroxyanisole. J. Photochem. Photobiol. B: Biol. 45 (1998) 136-143
31. Bailey H.H. L-S, R-buthionine sulfoximine: Historical development and clinical issues. Chem. Biol. Interact. 111-112 (1998) 239-254
32. Hissin P.J., and Hilf R. A fluorometric method for determination of oxidized and reduced glutathione in tissues. Anal. Biochem. 74 (1976) 214-226
33. Zang L.Y., Cosma G., Gardner H., and Vallyathan V. Scavenging of reactive oxygen species by melatonin. Biochim. Biophys. Acta 1425 (1998) 469-477
34. Halliwell B., Gutteridge J.M., and Aruoma O.I. The deoxyribose method: a simple "test-tube" assay for determination of rate constants for reactions of hydroxyl radicals. Anal. Biochem. 165 (1987) 215-219
35. Halliwell B., and Gutteridge J.M. Formation of thiobarbituric-acid-reactive substance from deoxyribose in the presence of iron salts: the role of superoxide and hydroxyl radicals. FEBS Lett. 128 (1981) 347-352
36. Kono Y., Takahashi M.A., and Asada K. Oxidation of manganous pyrophosphate by superoxide radicals and illuminated spinach chloroplasts. Arch. Biochem. Biophys. 174 (1976) 454-462
37. Bielski B.H.J., and Richter H.W. A study of the superoxide radical chemistry by stopped-flow radiolysis and radiation induced oxygen consumption. J. Am. Chem. Soc. 99 (1977) 3019-3023
38. Fridovich I. Quantitative aspects of the production of superoxide anion radical by milk xanthine oxidase. J. Biol. Chem. 245 (1970) 4053-4057
39. Bensasson R.V., Land E.J., and Truscott T.G. Excited States and Free Radicals in Biology and Medicine (1993), Oxford University Press, New York
40. g) (1.DELTA.g) bimolecular processes. Solvent and compartmentalization effects. Chem. Rev. 93 (1993) 699-723
41. 2 synthase. Biochem. J. 344 (1999) 747-754
42. {radical dot} scavenger in aqueous solution and in biological systems. Int. J. Radiat. Biol. 46 (1984) 725-729
43. Motohashi N., and Saito Y. Competitive measurement of rate constants for hydroxyl radical reactions using radiolytic hydroxylation of benzoate. Chem. Pharm. Bull. 41 (1993) 1842-1845
44. Stohs S.J., and Bagchi D. Oxidative mechanisms in the toxicity of metal ions. Free Radic. Biol. Med. 18 (1995) 321-336
45. Sharma P., Mongan P.D., and Morgan P.D. Ascorbate reduces superoxide production and improves mitochondrial respiratory chain function in human fibroblasts with electron transport chain deficiencies. Mitochondrion 1 (2001) 191-198
46. Marquez L.A., and Dunford H.B. Transient and steady-state kinetics of the oxidation of scopoletin by horseradish peroxidase compounds I, II and III in the presence of NADH. Eur. J. Biochem. 233 (1995) 364-371
47. Heikkila R.E., Cabbat F.S., and Cohen G. In vivo inhibition of superoxide dismutase in mice by diethyldithiocarbamate. J. Biol. Chem. 251 (1976) 2182-2185
48. Margoliash E., Novogrodsky A., and Schejter A. Irreversible reaction of 3-amino-1, 2, 4-triazole and related inhibitors with the protein and catalase. Biochem. J. 74 (1962) 339-348
49. Nathan C.F., Arrick B.A., Murray H.W., DeSantis N.M., and Cohm Z.A. Tumor cell anti-oxidant defenses. Inhibition of the glutathione redox cycle enhances macrophage-mediated cytolysis. J. Exp. Med. 153 (1981) 766-782
50. Tanielian C., Schweitzer C., Mechin R., and Wolff C. Quantum yield of singlet oxygen production by monomeric and aggregated forms of hematoporphyrin derivative. Free Radic. Biol. Med. 30 (2001) 208-212
51. Georgakoudi I., and Foster T.H. Singlet oxygen- versus nonsinglet oxygen-mediated mechanisms of sensitizer photobleaching and their effects on photodynamic dosimetry. Photochem. Photobiol. 67 (1998) 612-625
52. 2 in mitochondria of intact cells. J. Biol. Chem. 278 (2003) 3298
53. Rougee M., Bensasson R.V., Land E.J., and Pariente R. Deactivation of singlet molecular oxygen by thiols and related compounds, possible protectors against skin photosensitivity. Photochem. Photobiol. 47 (1988) 485-489
54. Dikalov S., Khramtsov V., and Zimmer G. Determination of rate constants of the reactions of thiols with superoxide radical by electron paramagnetic resonance. critical remarks on spectrophotometric approaches. Arch. Biochem. Biophys. 326 (1996) 207-218
55. Tarr M., and Valenzeno D.P. Singlet oxygen: the relevance of extracellular production mechanisms to oxidative stress in vivo. Photochem. Photobiol. Sci. 2 (2003) 355-361
56. Mao Y., Zang L., and Shi X. Singlet oxygen generation in the superoxide reaction. Biochem. Mol. Biol. Int. 36 (1995) 227-232
57. Harris L.R., Cake M.H., and Macey D.J. Iron release from ferritin and its sensitivity to superoxide ions differs among vertebrates. Biochem. J. 301 (1994) 385-389
58. Getoff N., and Solar S. Radiation-induced formation of haematoporphyrin-transients in aqueous solution. A pulse radiolysis study. Int. J. Radiat. Biol. 67 (1995) 619-626
59. Krasnovskii A.A., Venediktov E.A., and Chernenko O.M. Quenching of singlet oxygen with chlorophylls and porphyrins. Biofizika 27 (1982) 966-972
60. Tanielian C., Heinrich G., and Entezami A. Quenching of singlet oxygen by haematoporphyrin derivative (and haematoporphyrin) and its consequences on the efficiency of photodynamic cancer therapy. J. Chem. Soc. Chem. Commun. (1988) 1197-1198
61. Roberts W.G., Smith K.M., McCullough J.L., and Berns M.W. Skin photosensitivity and photodestruction of several potential photodynamic sensitizers. Photochem. Photobiol. 49 (1989) 431-438
62. Shigenaga M.K., Hagen T.M., and Ames B.N. Oxidative damage and mitochondrial decay in aging. PNAS 91 (1994) 10771-10778
63. Salet C., Moreno G., and Ricchelli F. Effects of Photofrin photodynamic action on mitochondrial respiration and superoxide radical generation. Free Radic. Res. 26 (1997) 201-208
64. Kelley E.E., Buettner G.R., and Burns C.P. Production of lipid-derived free radicals in L1210 murine leukemia cells is an early oxidative event in the photodynamic action of Photofrin. Photochem. Photobiol. 65 (1997) 576-580
65. Bonnett R., and Martinez G. Photobleaching of sensitisers used in photodynamic therapy. Tetrahedron 57 (2001) 9513-9547