Role of labile iron in the toxicity of pharmacological ascorbate

Free Radical Biology and Medicine

Volumn 84, Issue , 2015, Pages 289-295

  Du, Juan ^a   Wagner, Brett A ^a   Buettner, Garry R ^a,b   Cullen, Joseph J ^a,b,c  

^a UNIVERSITY OF IOWA   (United States)

^b UNIVERSITY OF IOWA HOSPITALS AND CLINICS   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

8 QUINOLINOL; ASCORBIC ACID; BIPYRIDINE; DEFEROXAMINE; HYDROGEN PEROXIDE; HYDROXYL RADICAL; IRON; SMALL INTERFERING RNA; UROPORPHYRINOGEN DECARBOXYLASE; ANTINEOPLASTIC AGENT; IRON CHELATING AGENT;

ARTICLE; CANCER GROWTH; CANCER INHIBITION; CATALYSIS; CELL CULTURE; CELL PROTECTION; CELL SURVIVAL; CLONOGENESIS; CLONOGENIC ASSAY; CONTROLLED STUDY; CYTOTOXICITY; DOWN REGULATION; ENZYME REPRESSION; FENTON REACTION; FLOW CYTOMETRY; GENE SILENCING; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IN VIVO STUDY; IRON STORAGE; MOLECULAR SIZE; PANCREATIC CANCER CELL LINE; PRIORITY JOURNAL; PROTEIN EXPRESSION; UPREGULATION; DRUG INTERACTION; METABOLISM; OXIDATION REDUCTION REACTION; TUMOR CELL LINE;

ANIMALIA;

ANTINEOPLASTIC AGENTS; ASCORBIC ACID; CELL LINE, TUMOR; DRUG INTERACTIONS; HUMANS; HYDROGEN PEROXIDE; IRON; IRON CHELATING AGENTS; OXIDATION-REDUCTION;

EID: 84929162789     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2015.03.033     Document Type: Article

References (48)

1. Q. Chen, M.G. Espey, M.C. Krishna, J.B. Mitchell, C.P. Corpe, G.R. Buettner, E. Shacter, and M. Levine Ascorbic acid at pharmacologic concentrations selectively kills cancer cells: ascorbic acid as a pro-drug for hydrogen peroxide delivery to tissues Proc. Natl. Acad. Sci. USA 102 2005 13604 13609
2. Q. Chen, M.G. Espey, A.Y. Sun, J.H. Lee, M.C. Krishna, E. Shacter, P.L. Choyke, C. Pooput, K.L. Kirk, G.R. Buettner, and M. Levine Ascorbic acid in pharmacologic concentrations: a pro-drug for selective delivery of ascorbate radical and hydrogen peroxide to extracellular fluid in vivo Proc. Natl. Acad. Sci. USA 104 2007 8749 8754
3. J. Du, S.M. Martin, M. Levine, B.A. Wagner, G.R. Buettner, S.H. Wang, A.F. Taghiyev, C. Du, C.M. Knudson, and J.J. Cullen Mechanisms of ascorbate-induced cytotoxicity in pancreatic cancer Clin. Cancer Res. 16 2 2010 509 520
4. 2 generation Cancer Res. 73 2013 5232 5241
5. G.R. Buettner In the absence of catalytic metals, ascorbate does not autoxidize at pH 7: ascorbate as a test for catalytic metals J. Biochem. Biophys. Methods 16 1988 27 40
6. G.R. Buettner, and B.A. Jurkiewicz Catalytic metals, ascorbate, and free radicals: combinations to avoid Radiat. Res. 145 1996 532 541
7. M.V.1 Clément, J. Ramalingam, L.H. Long, and B. Halliwell The in vitro cytotoxicity of ascorbate depends on the culture medium used to perform the assay and involves hydrogen peroxide Antioxid. Redox Signal. 3 1 2001 157 163
8. B.A. Wagner, J.R. Witmer, T.J. van 't Erve, and G.R. Buettner An assay for the rate of removal of extracellular hydrogen peroxide by cells Redox Biol 1 2013 210 217
9. S.J. Dixon, and B.R. Stockwell The role of iron and reactive oxygen species in cell death Nat. Chem. Biol. 10 2014 9 17
10. W.F. Blakely, A.F. Fuciarelli, B.J. Wegher, and M. Dizdaroglu Hydrogen peroxide-induced base damage in deoxyribonucleic acid Radiat. Res. 121 3 1990 338 343
11. S.L. Hempel, G.R. Buettner, Y.Q. O'Malley, D.A. Wessels, and D.A. Flaherty Fluorescein diacetate is superior for detecting intracellular oxidants: comparison to 2'7'dichlorodihydrofluorescein diacetate, 5(and 6)-carboxy-2'7'-dichlorodihydrofluorescein diacetate and dihydrorhodamine 123 Free Radic. Biol. Med. 27 1999 146 159
12. A. Samuni, J. Aronovitch, D. Godinger, M. Chevion, and G. Czapski On the cytotoxicity of vitamin C and metal ions. A site-specific Fenton mechanism Eur. J. Biochem. 137 1-2 1983 119 124
13. E.S. Henle, and S. Linn Formation, prevention, and repair of DNA damage by iron/hydrogen peroxide J. Biol. Chem. 272 31 1997 19095 19098
14. G.R. Buettner In the absence of catalytic metals, ascorbate does not autoxidize at pH 7: ascorbate as a test for catalytic metals J. Biochem. Biophys. Methods 16 1988 27 40
15. A. Barbouti, P.T. Doulias, B.Z. Zhu, B. Frei, and D. Galaris Intracellular iron, but not copper, plays a critical role in hydrogen peroxide-induced DNA damage Free Radic. Biol. Med. 31 4 2001 490 498
16. Y.Y. Chen, K.P. Ho, Q. Xia, and Z.M. Qian Hydrogen peroxide enhances iron-induced injury in isolated heart and ventricular cardiomyocyte in rats Mol. Cell. Biochem. 231 2002 61 68
17. S.K. Jonas, and P.A. Riley Modification of the in vitro cytotoxicity of hydrogen peroxide by iron complexes Free Radic. Res. Commun. 17 1992 407 418
18. P. Wardman, and L.P. Candeias Fenton chemistry: an introduction Radiat. Res. 145 5 1996 523 531
19. R. Roots, and S. Okada Estimation of life times and diffusion distances of radicals involved in X-ray induced strand breaks of killing of mammalian cells Radiat. Res. 64 1975 306 320
20. S.L. Hempel, G.R. Buettner, D.A. Wessels, G.M. Galvan, and Y. O'Malley Extracellular iron(II) can protect cells from hydrogen peroxide Arch. Biochem. Biophys. 330 1996 401 408
21. S.Y. Qian, and G.R. Buettner Iron and dioxygen chemistry is an important route to initiation of biological free radical oxidations: An electron paramagnetic resonance spin trapping study Free Radic. Biol. Med. 26 1999 1447 1456
22. J. Qian, J. Niu, M. Li, P.J. Chiao, and M.-S. Tsao In vitro modeling of human pancreatic duct epithelial cell transformation defines gene expression changes induced by K-ras oncogenic activation in pancreatic carcinogenesis Cancer Res. 65 2005 5045 5053
23. E. Prus, and E. Fibach Flow cytometry measurement of the labile iron pool in human hematopoietic cells Cytometry Part A 73A 2008 22 27
24. J.M. Vislisel, F.Q. Schafer, and G.R. Buettner A simple and sensitive assay for ascorbate using a plate reader Anal. Biochem. 365 2007 31 39
25. Y. Song, and G.R. Buettner Thermodynamic and kinetic considerations for the reaction of semiquinone radicals to form superoxide and hydrogen peroxide Free Radic. Biol. Med. 49 2010 919 962
26. Y. Hata, T. Kawabe, H. Hiraishi, S. Ota, A. Terano, and K.J. Ivey Hydrogen peroxide-mediated cytotoxicity to cultured colonic epithelial cells Life Sci. 60 24 1997 2221 2230
27. M. Mojić, J. Bogdanović Pristov, D. Maksimović-Ivanić, D.R. Jones, M. Stanić, S. Mijatović, and I. Spasojević Extracellular iron diminishes anticancer effects of vitamin C: an in vitro study Sci. Rep 4 2014 5955
28. 3+ transport across isolated intestinal brush-border membrane of the mouse Biochim. Biophys. Acta 772 2 1984 220 226
29. J. Kaplan, I. Jordan, and A. Sturrock Regulation of the transferrin-independent iron transport system in cultural cells J. Biol. Chem. 266 1991 2997 3004
30. T. Chepda, M. Cadau, P. Girin, J. Frey, and A. Chamson Monitoring of ascorbate at a constant rate in cell culture: effect on cell growth In Vitro Cell Dev. Biol. Anim. 37 1 2001 26 30
31. B.A. Wagner, S. Venkataraman, and G.R. Buettner The rate of oxygen utilization by cells Free Radic. Biol. Med. 51 2011 700 712
32. E. Ito, S. Yue, E.H. Moriyama, A.B. Hui, I. Kim, W. Shi, N.M. Alajez, N. Bhogal, G. Li, A. Datti, A.D. Schimmer, B.C. Wilson, P.P. Liu, D. Durocher, B.G. Neel, B. O'Sullivan, B. Cummings, R. Bristow, J. Wrana, and F.F. Liu Uroporphyrinogen decarboxylase is a radiosensitizing target for head and neck cancer Sci. Transl. Med. 3 2011 67ra7
33. 2 and transition metal ions in the genotoxic action of ascorbate in cell culture models Toxicol. Lett. 170 2007 57 65
34. H.1 Glickstein, R.B. El, M. Shvartsman, and Z.I. Cabantchik Intracellular labile iron pools as direct targets of iron chelators: a fluorescence study of chelator action in living cells Blood 106 2005 3242 3250
35. D.M. De Silva, C.C. Askwith, and J. Kaplan Molecular mechanisms of iron uptake in eukaryotes Physiol. Rev. 76 1996 31 47
36. D.J. Lane, and D.R. Richardson The active role of vitamin C in mammalian iron metabolism: much more than just enhanced iron absorption! Free Radic. Biol. Med. 75 2014 69 83
37. P. Brissot, M. Ropert, C. Le Lan, and O. Loréal Non-transferrin bound iron: a key role in iron overload and iron toxicity Biochim. Biophys. Acta 1820 2012 403 410
38. O. Kakhlon, and Z.I. Cabantchik The labile iron pool: characterization, measurement and participation in cellular process Free Radic. Biol. Med. 33 2002 1037 1046
39. F. Petrat, U. Rauen, and H. de Groot Determination of the chelatable iron pool of isolated rat hepatocytes by digital fluorescence microscopy using the fluorescent probe, Phen Green SK Hepatology 29 1999 1171 1179
40. F. Thomas, G. Serratrice, C. Béguin, E.S. Aman, J.L. Pierre, M. Fontecave, and J.P. Laulhère Calcein as a fluorescent probe for ferric iron. Application to iron nutrition in plant cells J. Biol. Chem. 274 1999 13375 13383
41. I. De Domenico, D. McVey Ward, and J. Kaplan Regulation of iron acquisition and storage: consequences for iron-linked disorders Nat. Rev. Mol. Cell. Biol. 9 2008 72 81
42. A.R. Giandomenico, G.E. Cerniglia, J.E. Biaglow, C.W. Stevens, and C.J. Koch The importance of sodium pyruvate in assessing damage produced by hydrogen peroxide Free Radic. Biol. Med 23 1997 426 434
43. Z.K. Pinnix, L.D. Miller, W. Wang, R. D'Agostino Jr, T. Kute, M.C. Willingham, H. Hatcher, L. Tesfay, G. Sui, X. Di, S.V. Torti, and F.M. Torti Ferroportin and iron regulation in breast cancer progression and prognosis Sci. Transl. Med. 2 2010 43ra56
44. M.K. Kiessling, C.D. Klemke, M.M. Kaminski, I.E. Galani, P.H. Krammer, and K. Gülow Inhibition of constitutively activated nuclear factor -κB induces reactive oxygen species- and iron-dependent cell death in cutanous T-cell lymphoma Cancer Res. 69 2009 2365 2374
45. W.S. Yang, and B.R. Stockwell Synthetic lethal screening identifies compounds activating iron-dependent, non-apoptotic cell death in oncogenic-RAS-harboring cancer cells Chem. Biol. 15 2008 234 245
46. J. Verrax, and P.B. Calderon Pharmacologic concentrations of ascorbate are achieved by parenteral administration and exhibit antitumoral effects Free Radic. Biol. Med. 47 2009 32 40
47. K.E. Olney, J. Du, T.J. van 't Erve, J.R. Witmer, Z.A. Sibenaller, B.A. Wagner, G.R. Buettner, and J.J. Cullen Inhibitors of hydroperoxide metabolism enhance ascorbate-induced cytotoxicity Free Radic. Res. 47 3 2013 154 163
48. A. Al-Qenaei, A. Yiakouvaki, O. Reelfs, P. Santambrogio, S. Levi, N.D. Hall, R.M. Tyrrell, and C. Pourzand Role of intracellular labile iron, ferritin, and antioxidant defence in resistance of chronically adapted Jurkat T cells to hydrogen peroxide Free Radic. Biol. Med. 68 2014 87 100