Intracellular ATP levels determine cell death fate of cancer cells exposed to both standard and redox chemotherapeutic agents

Biochemical Pharmacology

Volumn 82, Issue 11, 2011, Pages 1540-1548

  Verrax, Julien ^a   Dejeans, Nicolas ^a   Sid, Brice ^a   Glorieux, Christophe ^a   Calderon, Pedro Buc ^a,b  

^a UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

^b UNIVERSIDAD ARTURO PRAT   (Chile)

Author keywords

Ascorbate; Cancer; Chemotherapy; Menadione; Oxidative stress

Indexed keywords

ADENOSINE TRIPHOSPHATE; ANTINEOPLASTIC AGENT; ASCORBIC ACID; CASPASE 3; MELPHALAN; MENADIONE; REACTIVE OXYGEN METABOLITE;

APOPTOSIS; ARTICLE; CANCER CELL; CELL DEATH; CELL FATE; CHRONIC MYELOID LEUKEMIA; CONTROLLED STUDY; CYTOTOXICITY; DRUG EFFICACY; ENZYME ACTIVATION; HUMAN; HUMAN CELL; NECROSIS; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PHENOTYPE; PRIORITY JOURNAL;

ADENOSINE TRIPHOSPHATE; ANTINEOPLASTIC AGENTS; ANTINEOPLASTIC AGENTS, ALKYLATING; APOPTOSIS; ASCORBIC ACID; CASPASE 3; DRUG INTERACTIONS; HUMANS; K562 CELLS; MELPHALAN; NECROSIS; OXIDATION-REDUCTION; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; VITAMIN K 3;

EID: 80255125980     PISSN: 00062952     EISSN: 18732968     Source Type: Journal    
DOI: 10.1016/j.bcp.2011.07.102     Document Type: Article

References (50)

1. D. Trachootham, J. Alexandre, and P. Huang Targeting cancer cells by ROS-mediated mechanisms: a radical therapeutic approach? Nat Rev Drug Discov 8 2009 579 591
2. B. Kumar, S. Koul, L. Khandrika, R.B. Meacham, and H.K. Koul Oxidative stress is inherent in prostate cancer cells and is required for aggressive phenotype Cancer Res 68 2008 1777 1785 (Pubitemid 351416563)
3. J. Verrax, R. Pedrosa, R. Beck, N. Dejeans, H. Taper, and P. Calderon In situ modulation of oxidative stress: a novel and efficient strategy to kill cancer cells Curr Med Chem 16 2009 1821 1830
4. N. Hempel, H. Ye, B. Abessi, B. Mian, and J.A. Melendez Altered redox status accompanies progression to metastatic human bladder cancer Free Radic Biol Med 46 2009 42 50
5. H.R. Rezvani, A.L. Kim, R. Rossignol, N. Ali, M. Daly, and W. Mahfouf XPC silencing in normal human keratinocytes triggers metabolic alterations that drive the formation of squamous cell carcinomas J Clin Invest 121 2011 195 211
6. M. Koptyra, R. Falinski, M.O. Nowicki, T. Stoklosa, I. Majsterek, and M. Nieborowska-Skorska BCR/ABL kinase induces self-mutagenesis via reactive oxygen species to encode imatinib resistance Blood 108 2006 319 327 (Pubitemid 43990645)
7. F. Weinberg, R. Hamanaka, W.W. Wheaton, S. Weinberg, J. Joseph, and M. Lopez Mitochondrial metabolism and ROS generation are essential for Kras-mediated tumorigenicity Proc Natl Acad Sci USA 107 2010 8788 8793
8. D. Komatsu, M. Kato, J. Nakayama, S. Miyagawa, and T. Kamata NADPH oxidase 1 plays a critical mediating role in oncogenic Ras-induced vascular endothelial growth factor expression Oncogene 27 2008 4724 4732
9. C. Xia, Q. Meng, L.Z. Liu, Y. Rojanasakul, X.R. Wang, and B.H. Jiang Reactive oxygen species regulate angiogenesis and tumor growth through vascular endothelial growth factor Cancer Res 67 2007 10823 10830 (Pubitemid 350145911)
10. K.H. Vousden, and K.M. Ryan p53 and metabolism Nat Rev Cancer 9 2009 691 700
11. R.G. Jones, and C.B. Thompson Tumor suppressors and cell metabolism: a recipe for cancer growth Genes Dev 23 2009 537 548
12. K. Irani, Y. Xia, J.L. Zweier, S.J. Sollott, C.J. Der, and E.R. Fearon Mitogenic signaling mediated by oxidants in ras-transformed fibroblasts Science 275 1997 1649 1652 (Pubitemid 27120541)
13. O. Vafa, M. Wade, S. Kern, M. Beeche, T. Pandita, and G. Hampton c-Myc can induce DNA damage, increase reactive oxygen species, and mitigate p53 function: a mechanism for oncogene-induced genetic instability Mol Cell 9 2002 1031 1044 (Pubitemid 34626672)
14. G.T. Wondrak Redox-directed cancer therapeutics: molecular mechanisms and opportunities Antioxid Redox Sign 11 2009 3013 3069
15. M.C. Jaramillo, M.M. Briehl, and M.E. Tome Manganese porphyrin glutathionylates the p65 subunit of NF-κB to potentiate glucocorticoid-induced apoptosis in lymphoma Free Radic Biol Med 49 2010 S63
16. M.C. Jaramillo, J.B. Frye, J.D. Crapo, M.M. Briehl, and M.E. Tome Increased manganese superoxide dismutase expression or treatment with manganese porphyrin potentiates dexamethasone-induced apoptosis in lymphoma cells Cancer Res 69 2009 5450 5457
17. N. Dejeans, N. Tajeddine, R. Beck, J. Verrax, H. Taper, and P. Gailly Endoplasmic reticulum calcium release potentiates the ER stress and cell death caused by an oxidative stress in MCF-7 cells Biochem Pharmacol 79 2010 1221 1230
18. Beck R, Pedrosa RC, Dejeans N, Glorieux C, Leveque P, Gallez B, et al., Ascorbate/menadione-induced oxidative stress kills cancer cells that express normal or mutated forms of the oncogenic protein Bcr-Abl. An in vitro and in vivo mechanistic study. Invest New Drugs 2010, in press.
19. J. Verrax, S. Vanbever, J. Stockis, H. Taper, and P.B. Calderon Role of glycolysis inhibition and poly(ADP-ribose) polymerase activation in necrotic-like cell death caused by ascorbate/menadione-induced oxidative stress in K562 human chronic myelogenous leukemic cells Int J Cancer 120 2007 1192 1197
20. G.F. Merrill, E.J. Kurth, D.G. Hardie, and W.W. Winder AICA riboside increases AMP-activated protein kinase, fatty acid oxidation, and glucose uptake in rat muscle Am J Physiol 273 1997 E1107 E1112
21. F. Wroblewski, and J. Ladue Lactic dehydrogenase activity in blood Proc Soc Exp Biol Med 90 1955 210 213
22. D.W. Nicholson, A. Ali, N.A. Thornberry, J.P. Vaillancourt, C.K. Ding, and M. Gallant Identification and inhibition of the ICE/CED-3 protease necessary for mammalian apoptosis Nature 376 1995 37 43
23. O.H. Lowry, N.J. Rosebrough, A.L. Farr, and R.J. Randall Protein measurement with the Folin phenol reagent J Biol Chem 193 1951 265 275
24. J. Verrax, and P. Calderon Pharmacologic concentrations of ascorbate are achieved by parenteral administration and exhibit antitumoral effects Free Radic Biol Med 47 2009 32 40
25. M.M. Bradford A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Anal Biochem 72 1976 248 254
26. J. Verrax, J. Stockis, A. Tison, H.S. Taper, and P.B. Calderon Oxidative stress by ascorbate/menadione association kills K562 human chronic myelogenous leukaemia cells and inhibits its tumour growth in nude mice Biochem Pharmacol 72 2006 671 680 (Pubitemid 44233542)
27. J. Verrax, M. Delvaux, N. Beghein, H. Taper, B. Gallez, and P. Buc Calderon Free Radic Res 39 2005 649 657
28. L. Galluzzi, S.A. Aaronson, J. Abrams, E.S. Alnemri, D.W. Andrews, and E.H. Baehrecke Guidelines for the use and interpretation of assays for monitoring cell death in higher eukaryotes Cell Death Differ 16 2009 1093 1107
29. M. Leist, B. Single, A. Castoldi, S. Kühnle, and P. Nicotera Intracellular adenosine triphosphate (ATP) concentration: a switch in the decision between apoptosis and necrosis J Exp Med 185 1997 1481 1486 (Pubitemid 27187604)
30. Y. Eguchi, S. Shimizu, and Y. Tsujimoto Intracellular ATP levels determine cell death fate by apoptosis or necrosis Cancer Res 57 1997 1835 1840 (Pubitemid 27209706)
31. H. Zou, Y. Li, X. Liu, and X. Wang An APAF-1.cytochrome c multimeric complex is a functional apoptosome that activates procaspase-9 J Biol Chem 274 1999 11549 11556
32. A. Samali, H. Nordgren, B. Zhivotovsky, E. Peterson, and S. Orrenius A comparative study of apoptosis and necrosis in HepG2 cells: oxidant-induced caspase inactivation leads to necrosis Biochem Biophys Res Commun 255 1999 6 11 (Pubitemid 29292055)
33. M.B. Hampton, and S. Orrenius Dual regulation of caspase activity by hydrogen peroxide: implications for apoptosis FEBS Lett 414 1997 552 556 (Pubitemid 27390666)
34. R. Beck, J. Verrax, N. Dejeans, H. Taper, and P. Buc Calderon Menadione reduction by pharmacological doses of ascorbate induces an oxidative stress that kills breast cancer cells Int J Toxicol 28 2009 33 42
35. D. Hanahan, and R.A. Weinberg Hallmarks of cancer: the next generation Cell 144 2011 646 674
36. H. Jijakli, A.B. Nadi, L. Cook, L. Best, A. Sener, and W.J. Malaisse Insulinotropic action of methyl pyruvate: enzymatic and metabolic aspects Arch Biochem Biophys 335 1996 245 257 (Pubitemid 26384790)
37. D.G. Hardie, and D. Carling The AMP-activated protein kinase - fuel gauge of the mammalian cell? Eur J Biochem 246 1997 259 273 (Pubitemid 27232500)
38. Z. Dagher, N. Ruderman, K. Tornheim, and Y. Ido The effect of AMP-activated protein kinase and its activator AICAR on the metabolism of human umbilical vein endothelial cells Biochem Biophys Res Commun 265 1999 112 115
39. D. Trachootham, Y. Zhou, H. Zhang, Y. Demizu, Z. Chen, and H. Pelicano Selective killing of oncogenically transformed cells through a ROS-mediated mechanism by beta-phenylethyl isothiocyanate Cancer Cell 10 2006 241 252 (Pubitemid 44311067)
40. H. Pelicano, L. Feng, Y. Zhou, J.S. Carew, E.O. Hileman, and W. Plunkett Inhibition of mitochondrial respiration: a novel strategy to enhance drug-induced apoptosis in human leukemia cells by a reactive oxygen species-mediated mechanism J Biol Chem 278 2003 37832 37839 (Pubitemid 37175311)
41. J. Lu, E.H. Chew, and A. Holmgren Targeting thioredoxin reductase is a basis for cancer therapy by arsenic trioxide Proc Natl Acad Sci U S A 104 2007 12288 12293 (Pubitemid 47206130)
42. B. Tareen, J. Summers, J. Jamison, D. Neal, K. McGuire, and L. Gerson A 12 week, open label, phase I/IIa study using apatone for the treatment of prostate cancer patients who have failed standard therapy Int J Med Sci 5 2008 62 67 (Pubitemid 351871013)
43. I. Batinic-Haberle, Z. Rajic, and L. Benov A combination of two antioxidants (an SOD mimic and ascorbate) produces a pro-oxidative effect forcing Escherichia coli to adapt via induction of oxyR regulon Anticancer Agents Med Chem 11 2011 329 340
44. X. Ye, D. Fels, C. Dedeugd, M.W. Dewhirst, K. Leong, and I. Batinic-Haberle The in vitro cytotoxic effects of Mn(III) alkylpyridylporphyrin/ ascorbate system on four tumor cell lines Free Radic Biol Med 47 2009 S137
45. Q. Chen, M. Espey, A. Sun, C. Pooput, K. Kirk, and M. Krishna Pharmacologic doses of ascorbate act as a prooxidant and decrease growth of aggressive tumor xenografts in mice Proc Natl Acad Sci U S A 105 2008 11105 11109
46. Q. Chen, M. Espey, A. Sun, J. Lee, M. Krishna, and E. Shacter Ascorbate in pharmacologic concentrations selectively generates ascorbate radical and hydrogen peroxide in extracellular fluid in vivo Proc Natl Acad Sci U S A 104 2007 8749 8754 (Pubitemid 47175383)
47. Q. Chen, M. Espey, M. Krishna, J. Mitchell, C. Corpe, and G. Buettner Pharmacologic ascorbic acid concentrations selectively kill cancer cells: action as a pro-drug to deliver hydrogen peroxide to tissues Proc Natl Acad Sci U S A 102 2005 13604 13609 (Pubitemid 41420895)
48. A. Biroccio, B. Benassi, F. Fiorentino, and G. Zupi Glutathione depletion induced by c-Myc downregulation triggers apoptosis on treatment with alkylating agents Neoplasia 6 2004 195 206 (Pubitemid 38657075)
49. P. Gomez-Bougie, L. Oliver, S. Le Gouill, R. Bataille, and M. Amiot Melphalan-induced apoptosis in multiple myeloma cells is associated with a cleavage of Mcl-1 and Bim and a decrease in the Mcl-1/Bim complex Oncogene 24 2005 8076 8079 (Pubitemid 41746750)
50. D. Acehan, X. Jiang, D.G. Morgan, J.E. Heuser, X. Wang, and C.W. Akey Three-dimensional structure of the apoptosome: implications for assembly, procaspase-9 binding, and activation Mol Cell 9 2002 423 432 (Pubitemid 34195566)