Nitric oxide-induced resistance to lethal photooxidative damage in a breast tumor cell line

Free Radical Biology and Medicine

Volumn 40, Issue 8, 2006, Pages 1323-1331

  Niziolek, Magdalena ^a   Korytowski, Witold ^a,b   Girotti, Albert W ^a  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

^b JAGIELLONIAN UNIVERSITY   (Poland)

Author keywords

Ferritin; Free radicals; Intracellular free iron; Nitric oxide; Photodynamic therapy; Photooxidative stress; Protoporphyrin IX; Tumor cells

Indexed keywords

AMINOLEVULINIC ACID; CALCEIN; DICHLOROFLUORESCEIN; FERRITIN; FLUORESCENT DYE; HEME OXYGENASE 1; IRON; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; PROTOPORPHYRIN; SPERMINE DERIVATIVE; SPERMINE NONOATE; TERT BUTYL HYDROPEROXIDE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BREAST TUMOR; CELL ACTIVATION; CELL DEATH; CELL KILLING; CELL MEMBRANE; CELL PROTECTION; CONTROLLED STUDY; ENZYME BLOOD LEVEL; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IRON KINETICS; LETHALITY; MACROPHAGE; MITOCHONDRION; MOUSE; NONHUMAN; OXIDATIVE STRESS; PHOTODYNAMIC THERAPY; PHOTOOXIDATION; POROSITY; PRIORITY JOURNAL; RADIATION DOSE; RADIOSENSITIZATION; TUMOR CELL LINE; TUMOR RESISTANCE; UPREGULATION;

ANIMALS; BREAST NEOPLASMS; CELL DEATH; CELL LINE, TUMOR; DRUG RESISTANCE, NEOPLASM; FERRITINS; HEME OXYGENASE (DECYCLIZING); HUMANS; IONS; MACROPHAGES; MICE; NITRIC OXIDE; OXIDANTS; OXIDATION-REDUCTION; PHOTOSENSITIZING AGENTS; PROTOPORPHYRINS; SPERMINE;

EID: 33646035553     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2005.11.022     Document Type: Article

References (51)

1. Moncada S.R., Palmer R.M.J., and Higgs E.A. Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacol. Rev. 43 (1991) 109-143
2. Radomski M.W. Nitric oxide: biological mediator, modulator, and effector. Ann. Med. 27 (1995) 321-329
3. Hogg N. Prooxidant and antioxidant effects of nitric oxide. In: Favier A.E., Cadet J., Kalyanaraman B., Fontecave M., and Pierre J.L.; (Eds). Analysis of free radicals in biological systems (1995), Birkhauser-Verlag, Basel 37-49
4. Wink D.A., and Mitchell J.B. Chemical biology of nitric oxide: insights into regulatory, cytotoxic, and cytoprotective mechanisms of nitric oxide. Free Radic. Biol. Med. 25 (1998) 434-456
5. Beckman J.S. Oxidative damage and tyrosine nitration from peroxynitrite. Chem. Res. Toxicol. 9 (1996) 836-844
6. Kalyanaraman B., Joseph J., Struck A., and Parthasarathy S. Inhibition of low density lipoprotein oxidation by nitric oxide: potential role in atherogenesis. FEBS Lett. 334 (1993) 170-174
7. Rubbo H., Radi R., Trujillo M., Kalyanaraman B., Barnes S., and Freeman B.A. Nitric oxide regulation of superoxide and peroxynitrite-dependent lipid peroxidation. J. Biol. Chem. 269 (1994) 26066-26075
8. Korytowski W., Zareba M., and Girotti A.W. Nitric oxide inhibition of free radical-mediated cholesterol peroxidation in liposomal membranes. Biochemistry 39 (2000) 6918-6928
9. Korytowski W., Zareba M., and Girotti A.W. Inhibition of free radical-mediated cholesterol peroxidation by diazeniumdiolate-derived nitric oxide: effect of release rate on mechanism of action in a membrane system. Chem. Res. Toxicol. 13 (2000) 1265-1274
10. Wink D.A., Cook J.A., Krishna M.C., Hanbauer I., DeGraff W., Gamson J., and Mitchell J.B. Nitric oxide protects against alkyl peroxide-mediated cytotoxicity: further insights into the role nitric oxide plays in oxidative stress. Arch. Biochem. Biophys. 319 (1995) 402-407
11. Wink D.A., Cook J.A., Pacelli R., DeGraff W., Gamson J., Liebman J., Krishna M., and Mitchell J.B. The effects of various nitric oxide donor agents on hydroperoxide-mediated toxicity: a direct correlation between nitric oxide formation and protection. Arch. Biochem. Biophys. 331 (1996) 241-248
12. Chang J., Rao N.V., Markewitz B.A., Hoedal J.R., and Mitchell J.B. Nitric oxide donor prevents peroxide-mediated endothelial cell injury. Am. J. Physiol. 270 (1996) L931-L940
13. Kelley E.E., Wagner B.A., Buettner G.R., and Burns C.P. Nitric oxide inhibits iron-induced lipid peroxidaiton in HL-60 cells. Arch. Biochem. Biophys. 370 (1999) 97-104
14. Kim Y.-M., Bergonia H., and Lancaster J.R. Nitric oxide-induced autoprotection of isolated rat hepatocytes. FEBS Lett. 374 (1995) 228-232
15. Joshi M.S., Ponthier J.L., and Lancaster J.R. Cellular antioxidant and prooxidant actions of nitric oxide. Free Radic. Biol. Med. 27 (1999) 1357-1366
16. Bishop A., Marquis J.C., Cashman N.R., and Demple B. Adaptive resistance to nitric oxide in motor neurons. Free Radic. Biol. Med. 26 (1999) 978-986
17. Niziolek M., Korytowski W., and Girotti A.W. Nitric oxide inhibition of free radical-mediated lipid peroxidation in photodynamically treated membranes and cells. Free Radic. Biol. Med. 34 (2003) 997-1005
18. Niziolek M., Korytowski W., and Girotti A.W. Chain-breaking antioxidant and cytoprotective effects of nitric oxide on photodynamically stressed tumor cells. Photochem. Photobiol. 78 (2003) 262-270
19. Dougherty T.J., Gomer C.J., Henderson B.W., Jori G., Kessel D., Korbelik M., Moan J., and Peng Q. Photodynamic therapy. J. Natl. Cancer Inst. 90 (1998) 889-905
20. Keefer L.K., Nims R.W., Davies K.M., and Wink D.A. "NONOates" (1-substituted diazen-1-ium-1,2-diolates) as nitric oxide donors: convenient nitric oxide dosage forms. Methods Enzymol. 268 (1996) 281-293
21. Esworthy R.S., Baker M.A., and Chu F.-F. Expression of selenium-dependent glutathione peroxidase in human breast tumor cell lines. Cancer Res. 55 (1995) 957-962
22. Hurst R., Korytowski W., Kriska T., Esworthy R.S., Chu F.-F., and Girotti A.W. Hyperresistance to cholesterol hydroperoxide-induced peroxidative injury and apoptotic death in a tumor cell line that overexpresses glutathione peroxidase isotype-4. Free Radic. Biol. Med. 31 (2001) 1051-1065
23. Kriska T., Korytowski W., and Girotti A.W. Hyperresistance to photosensitized lipid peroxidation and apoptotic killing in 5-aminolevulinate-treated tumor cells overexpressing mitochondrial GPx4. Free Radic. Biol. Med. 33 (2003) 1389-1402
24. Zhang Y., and Hogg N. Formation and stability of S-nitrosothiols in RAW 264.7 cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 287 (2004) L467-L474
25. Spector D.L., Goldman R.D., and Leinwald L.A. Cells: a laboratory manual, volume 1, chapter 15 (1997), Cold Spring Harbor Press, New York
26. Thomas J.P., Geiger P.G., and Girotti A.W. Lethal damage to endothelial cells by oxidized low density lipoprotein: role of selenoperoxidases in cytoprotection against lipid hydroperoxide- and iron-mediated reactions. J. Lipid Res. 34 (1993) 479-490
27. Lin F., and Girotti A.W. Hyperresistance of leukemia cells to phododynamic inactivation after long-term exposure to hemin. Cancer Res. 56 (1996) 4543-4636
28. Bradford M.M. A rapid and sensitive method for the quantitaiton of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72 (1976) 248-254
29. Lin F., and Girotti A.W. Hemin-enhanced resistance of human leukemia cells to oxidative killing: antisense determination of ferritin involvement. Arch. Biochem. Biophys. 352 (1998) 51-58
30. Breuer W., Epsztejn S., and Cabantchik Z.I. Iron acquired from transferring by K52 cells is delivered into a cytoplasmic pool of chelatable iron (II). J. Biol. Chem. 270 (1995) 24209-24215
31. Epsztejn S., Kakhlon O., Glickstein H., Breuer W., and Cabantchik Z.I. Fluorescence analysis of the labile iron pool of mammalian cells. Anal. Biochem. 248 (1997) 31-40
32. Kakhlon O., and Cabantchik Z.I. The labile iron pool: characterization, measurement, and participation in cellular processes. Free Radic. Biol. Med. 33 (2002) 1037-1046
33. Le Bel C.P., Ischiropoulos H., and Bondy S.C. Evaluation of the probe 2′,7′-dichlorofluorescin as an indicator of reactive oxygen species formation and oxidative stress. Chem. Res. Toxicol. 5 (1992) 227-231
34. Bilski P., Belanger A.G., and Chignell C.F. Photosensitized oxidation of 2′,7′-dichlorofluorescin: singlet oxygen does not contribute to the formation of fluorescent oxidation product 2′,7′-dichlorofluorescein. Free Radic. Biol. Med. 33 (2002) 938-946
35. Girotti A.W. Photosensitized oxidation of membrane lipids: reaction pathways, cytotoxic effects, and cytoprotective mechanisms. J. Photochem. Photobiol. 63 (2001) 103-113
36. Masaki N., Kyle M.E., and Farber J.C. tert-Butyl hydroperoxide kills cultured hepatocytes by peroxidizing membrane lipids. Arch. Biochem. Biophys. 269 (1989) 390-399
37. Niziolek M., Korytowski W., and Girotti A.W. Self-sensitized photodegradation of membrane-bound protoporphyrin mediated by chain lipid peroxidation: inhibition by nitric oxide with sustained singlet oxygen damage. Photochem. Photobiol. 81 (2005) 299-305
38. Kim Y.-M., Bergonia H.A., Muller C., Pitt B.R., Watkins W.D., and Lancaster J.R. Loss and degradation of enzyme-bound heme induced by cellular nitric oxide synthesis. J. Biol. Chem. 270 (1995) 5710-5713
39. Kim Y.-M., Bergonia H.A., Muller C., Pitt B.R., Watkins W.D., and Lancaster J.R. Nitric oxide and intracellular heme. Adv. Pharmacol. 14 (1995) 277-291
40. Balla G., Jacob H.S., Balla J., Rosenberg M., Nath K., Apple F., Eaton J.W., and Vercelotti G.M. Ferritin: a cytoprotective antioxidant stratagem of endothelium. J. Biol. Chem. 267 (1992) 18148-18153
41. Lin F., and Girotti A.W. Hyperresistance of leukemia cells to photodynamic inactivation after long-term exposure to hemin. Cancer Res. 56 (1996) 4636-4643
42. O'Donnell V.B., Chumley P.H., Hogg N., Bloodsworth A., Darley-Usmar V., and Freeman B.A. Nitric oxide inhibition of lipid peroxidation: kinetics of reaction with lipid peroxyl radicals and comparison with α-tocopherol. Biochemistry 36 (1997) 15216-15223
43. Gillissen M.J.G., Van der Merbel-de Wit E.A., Star W.M., Koster J.F., and Sluiter W. Effect of photodynamic therapy on the endothelium-dependent relaxation of rat aortas. Cancer Res. 53 (1993) 2548-2552
44. Henderson B.W., Sitnik-Busch T.M., and Vaughan L.A. Potentiation of photodynamic therapy antitumor activity in mice by nitric oxide synthase inhibition is fluence rate-dependent. Photochem. Photobiol. 70 (1999) 64-71
45. Korbelik M., Parkins C.S., Shibuya H., Cecic I., Stratford M.R.C., and Chaplin D.J. Nitric oxide production by tumor tissue: impact on the response to photodynamic therapy. Br. J. Cancer 82 (2000) 1835-1843
46. Yee E.L., Pitt B.R., Billiar T.R., and Kim Y.-M. Effect of nitric oxide on heme metabolism in pulmonary artery endothelial cells. Am. J. Physiol. 271 (1996) L512-L518
47. Nunoshiba T., DeRojas-Walker T., Wishnok J.S., Tannenbaum S.R., and Demple B. Activation by nitric oxide of an oxidative stress response that defends E.coli against activated macrophages. Proc. Natl. Acad. Sci. USA 90 (1993) 9993-9997
48. Hentze M.W., and Kuhn L.C. Molecular control of vertegrate iron metabolism: mRNA-based regulatory circuits operated by iron, nitric oxide, and oxidative stress. Proc. Natl. Acad. Sci. USA 76 (2002) 423-430
49. Keberle H. The biochemistry of desferrioxamine and its relationship to iron metabolism. Ann. N. Y. Acad. Sci. 119 (1964) 758-768
50. Gomes E.R., Almeida R.D., Carvalho A.P., and Duarte C.B. Nitric oxide modulates tumor cell death induced by photodynamic therapy through a cGMP-dependent mechanism. Photochem. Photobiol. 76 (2002) 423-430
51. Peng Q., Berg K., Moan J., Kongshaug M., and Nesland J.M. 5-Aminolevulinic acid-based photodynamic therapy; principles, and experimental research. Photochem. Photobiol. 65 (1997) 235-251