Role of compartmentalized redox-active iron in hydrogen peroxide-induced DNA damage and apoptosis

Biochemical Journal

Volumn 387, Issue 3, 2005, Pages 703-710

  Tenopoulou, Margarita ^a   Doulias, Paschalis Thomas ^a   Barbouti, Alexandra ^a   Brunk, Ulf ^b   Galaris, Dimitrios ^a  

^a UNIVERSITY OF IOANNINA   (Greece)

^b LINKÖPING UNIVERSITY   (Sweden)

Author keywords

Apoptosis; Desferrioxamine; DNA damage; Lysosome; Oxidative stress; Redox active iron

Indexed keywords

BIOLOGICAL MEMBRANES; CELLS; GLUCOSE; HYDROGEN PEROXIDE; IRON; OXIDATION; REDOX REACTIONS;

APOPTOSIS; JURKAT CELLS; OXIDATIVE STRESS; REDOX-ACTIVE IRON;

DNA;

ACRIDINE ORANGE; APOPTOSIS INDUCING FACTOR; CALCEIN; CYTOCHROME C; DEFEROXAMINE; ESTERASE; GLUCOSE OXIDASE; HYDROGEN PEROXIDE; IRON;

APOPTOSIS; ARTICLE; COMET ASSAY; CYTOSOL; DNA DAMAGE; DNA STRAND BREAKAGE; ENDOCYTOSIS; HUMAN; HUMAN CELL; IRON CHELATION; LEUKEMIA CELL LINE; LYSOSOME MEMBRANE; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PRIORITY JOURNAL;

APOPTOSIS; CELL MEMBRANE; DEFEROXAMINE; DNA DAMAGE; FLUORESCEINS; HUMANS; HYDROGEN PEROXIDE; IRON; IRON CHELATING AGENTS; JURKAT CELLS; LYSOSOMES; MEMBRANE POTENTIALS; MITOCHONDRIA; OXIDATION-REDUCTION; OXIDATIVE STRESS; TEMPERATURE; TIME;

EID: 18844425714     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20041650     Document Type: Article

References (43)

1. Öllinger, K. and Brunk, U. (1995) Cellular injury induced by oxidative stress is mediated through lysosomal damage. Free Radical Biol. Med. 19, 565-574
2. Zhengquan, Y., Persson, H., Eaton, J. and Brunk, U. (2003) Intralysosomal iron: A major determinant of oxidant-induced cell death. Free Radical Biol. Med. 34, 1243-1252
3. Galaris, D. and Evangelou, A. (2002) The role of oxidative stress in mechanism of metal-induced carcinogenesis. Crit. Rev. Oncol. Heamatol. 42, 93-103
4. Epsztejn, S., Kakhlon, O., Glickstein, H., Breuer, W. and Cabantchik, Z. (1997) Fluorescence analysis of the labile iron pool of mammalian cells. Anal. Biochem. 248, 31-40
5. Kakhlon, O. and Cabantchik, Z. (2002) The labile iron pool: Characterization, measurement, and participation in cellular processes. Free Radical Biol. Med. 33, 1037-1046
6. Esposito, B., Epsztejn, S., Breuer, W. and Cabantchik, Z. (2002) A review of fluorescence methods for assessing labile iron in cells and biological fluids. Anal. Biochem. 304, 1-18
7. Schafer, F. and Buettner, G. (2000) Acidic pH amplifies iron-mediated lipid peroxidation in cells. Free Radical Biol. Med. 28, 1175-1181
8. Pisoni, R., Acker, T., Lisowski, K., Lemons, R. and Thoene, J. (1990) A cystein-specific lysosomal transport system provides a major route for the delivery of thiol to human fibroblast lysosomes: possible role in supporting lysosomal proteolysis. J. Cell Biol. 110, 327-335
9. Brunk, U., Neuzil, J. and Eaton, J. (2001) Lysosomal involvement in apoptosis. Redox Rep. 6, 91-97
10. 2 is a consequence of lysosomal rupture. Biochem. J. 356, 549-555
11. Guicciardi, M., Leist, M. and Gores, G. (2004) Lysosomes in cell death. Oncogene 23, 2881-2890
12. Halliwell, B. and Aruoma, O. (1991) DNA damage by oxygen-derived species: Its mechanism and measurement in mammalian systems. FEBS Lett. 281, 9-19
13. Barbouti, A., Doulias, P., Zhu, B., Frei, B. and Galaris, D. (2001) Intracellular iron but not copper plays a critical role in hydrogen peroxide-induced DNA damage. Free Radical Biol. Med. 31, 490-498
14. Doulias, P., Christoforidis, S., Brunk, U. and Galaris, D. (2003) Endosomal and lysosomal effects of desferrioxamine: protection of HeLa cells from hydrogen peroxide-induced DNA damage and induction of cell-cycle arrest. Free Radical Biol. Med. 35, 719-728
15. Kurz, T., Leake, A., Zglinicki, T. and Brunk, U. (2004) Relocated redox-active iron is an important mediator of oxidative-stress-induced DNA damage. Biochem. J. 378, 1039-1045
16. Meneghini, R. (1997) Iron homeostasis, oxidative stress, and DMA damage. Free Radical Biol. Med. 23, 783-792
17. Chevion, M. (1988) A site-specific mechanism for free radical induced biological damage: the essential role of redox-active transition metals. Free Radical Biol. Med. 5, 27-37
18. 2. Blood 95, 2960-2966
19. Lloyd, J., Cable, H. and Rice-Evans, C. (1991) Evidence that desferrioxamine cannot enter cells by passive diffusion. Biochem. Pharmacol. 41, 1361-1363
20. Cable, H. and Lloyd, J. B. (1999) Cellular uptake and release of two contrasting iron chelators. J. Pharmacol. 51, 131-134
21. Singh, N., McCoy, M., Tice, R. and Schneider, E. (1988) A simple technique tor quantitation of low levels of DNA damage in individual cells. Exp. Cell Res. 184, 461-470
22. Collins, A., Dobson, V., Dusinska, M., Kennedy, G. and Stetina, R. (1997) The comet assay; what can it really tell us? Mutat. Res. 375, 183-193
23. 2+-dependent DNA damage in human peripheral blood lymphocytes. Free Radical Biol. Med. 26, 548-556
24. Collins, A., Ma, A. and Duthie, S. (1995) The kinetics of repair of oxidative DNA damage (strand breaks and oxidized pyrimidines) in human cells. Mutat. Res. 336, 69-77
25. Duthie, S. and Hawdon, A. (1998) DNA instability (strand breakage, uracil misincorporation and defective repair) is increased by folic acid depletion in human lymphocytes in vitro. FASEB J. 14, 1491-1497
26. Cossarizza, A., Baccarani-Contri, M., Kalashnikova, G. and Franceschi, C. (1993) A new method for the cytofluorimetric analysis of mitochondrial membrane potential using the J-aggregate forming lipophilic cation 5,5′,6, 6′-tetrachloro-1,1′,3.3′-tetraethylbenzimidazolcarbocyanine iodide (JC-1). Biochem. Biophys. Res. Commun. 197, 40-45
27. Yang, J., Liu, X., Bhalla, K., Kim, C., Ibrado, A., Cai, J., Peng, T., Jones, D. and Wang, X. (1997) Prevention of apoptosis by Bcl-2: release of cytochrome c from mitochondria blocked. Science 275, 1129-1132
28. Wolgemuth, D. and Hsu, M. (1981) Visualization of nascent RNA transcripts and simultaneous transcription and replication in viral nucleoprotein complexes from adenovirus 2-infected HeLa cells. J. Mol. Biol. 147, 247-268
29. Doulias, P., Barbouti, A., Galaris, D. and Ischiropoulos, C. (2001) SIN-1-induced DNA damage in isolated human peripheral blood lymphocytes as assessed by single cell gel electrophoresis (comet assay). Free Radical Biol. Med. 30, 679-685
30. 2. Free Radical Biol. Med. 33, 691-702
31. Konijn, A., Glickstein, H., Vaisman, B., Meyron-Holtz, E., Slotki, I. and Cabantchik, Z. (1999) The cellular labile iron pool and intracellular ferritin in K562 cells. Blood 94, 2128-2134
32. Persson, H., Zhengquan, Y., Tirosh, O., Eaton, J. and Brunk, U. (2003) Prevention of oxidant-induced cell death by lysosomotropic iron chelators. Free Radical Biol. Med. 34, 1295-1305
33. Kågedal, K., Zhao, M., Svensson, I. and Brunk, U. (2001) Sphingosine-induced apoptosis is dependent on lysosomal proteases. Biochem. J. 369, 335-343
34. Li, W., Yuan, X., Nordgren, G., Dalen, H., Dobowchik, G., Firestone, R. and Brunk, U. (2000) Induction of cell death by the lysosomotropic detergent MSDH. FEBS Lett. 470, 35-39
35. 2 gradients across biomembranes. FEBS Lett. 475, 121-126
36. Richardson, D. and Ponka, P. (1997) The molecular mechanisms of the metabolism and transport of iron in normal and neoplastic cells. Biochim. Biophys. Acta 1331, 1-40
37. Dice, J. (2000) Lysosomal Pathways of Protein Degradation. Eurekah.com/Landes Bioscience, Georgetown, TX
38. Yu, Z., Li, W., Hillman, J. and Brunk, U. (2004) Human neuroblastoma (SH-SY5Y) cells are highly sensitive to the lysosomotropic aldehyde 3-aminopropanal. Brain Res. 1016, 163-169
39. Boya, P., Andreau, K., Poncet, D., Zamzami, N., Perfettini, J., Metivier, D., Ojcius, D., Jaattela, M. and Kroemer, G. (2003) Lysosomal membrane permeabilization induces cell death in a mitochondrion-dependent fashion. J. Exp. Med. 197, 1323-1334
40. Zhao, M., Antunes, F., Neuzil, J., Eaton, J. and Brunk, U. (2003) Relocation of lysosomal enzymes induces mitochondria-mediated oxidative stress, release of cytochrome c and apoptosis. Eur. J. Biochem. 270, 3778-3786
41. Cirman, T., Oresic, K., Mazovec, G., Turk, V., Reed, J., Myers, R., Salvesen, G. and Turk, B. (2004) Selective disruption of lysosomes in HeLa cells triggers apoptosis mediated by cleavage of Bid by multiple papain-like lysosomal cathepsins. J. Biol. Chem. 279, 3578-3587
42. Yuan, X., Li, W., Dalen, H., Lotem, J., Sachs, L. and Brunk, U. (2002) Lysosomal destabilization in p53-induced apoptosis. Proc. Natl. Acad. Sci. U.S.A. 99, 6286-6291
43. Zhao, M., Eaton, J. and Brunk, U. (2000) Protection against oxidant-mediated lysosomal rupture: a new anti-apoptotic activity of Bcl-2? FEBS Lett. 485, 104-108