Chelation of intracellular iron with the antifungal agent ciclopirox olamine induces cell death in leukemia and myeloma cells

Blood

Volumn 114, Issue 14, 2009, Pages 3064-3073

  Eberhard, Yanina ^a   McDermott, Sean P ^b,c   Wang, Xiaoming ^a   Gronda, Marcela ^a   Venugopal, Amudha ^a   Wood, Tabitha E ^a,d   Hurren, Rose ^a   Datti, Alessandro ^e   Batey, Robert A ^d   Wrana, Jeffrey ^e   Antholine, William E ^f   Dick, John ^b,c   Schimmer, Aaron D ^a  

^a PRINCESS MARGARET HOSPITAL   (Canada)

^b UNIVERSITY HEALTH NETWORK   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

^d UNIVERSITY OF TORONTO   (Canada)

^e MOUNT SINAI HOSPITAL   (Canada)

^f MEDICAL COLLEGE OF WISCONSIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CICLOPIROXOLAMINE; IRON; RIBONUCLEOTIDE REDUCTASE;

ACUTE GRANULOCYTIC LEUKEMIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER CELL CULTURE; CANCER SIZE; CANCER STEM CELL; CELL DEATH; CELL GROWTH; CELL VIABILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG CYTOTOXICITY; DRUG MECHANISM; ELECTRON SPIN RESONANCE; ENGRAFTMENT; FEMALE; HUMAN; HUMAN CELL; IRON CHELATION; LEUKEMIA CELL; MOUSE; MYELOMA; MYELOMA CELL; NONHUMAN; PRIORITY JOURNAL; SEVERE COMBINED IMMUNODEFICIENCY; SOLID TUMOR; TARGET CELL; WEIGHT REDUCTION;

ANIMALS; ANTIFUNGAL AGENTS; ANTIMETABOLITES, ANTINEOPLASTIC; APOPTOSIS; CELLS, CULTURED; CYTARABINE; DRUG SYNERGISM; ELECTRON SPIN RESONANCE SPECTROSCOPY; FIBROBLASTS; HUMANS; IMMUNOBLOTTING; IRON; IRON CHELATING AGENTS; LEUKEMIA, MYELOID, ACUTE; LUCIFERASES; LUNG; MICE; MICE, INBRED NOD; MICE, SCID; MICROTUBULE-ASSOCIATED PROTEINS; MULTIPLE MYELOMA; PROMOTER REGIONS, GENETIC; PYRIDONES; RIBONUCLEOTIDE REDUCTASES;

EID: 70449466605     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2009-03-209965     Document Type: Article

References (57)

1. Ideyama Y, Kudoh M, Tanimoto K, et al. Novel nonsteroidal inhibitor of cytochrome P450(17alpha) (17alpha-hydroxylase/C17-20 lyase), YM116, decreased prostatic weights by reducing serum concentrations of testosterone and adrenal androgens in rats. Prostate. 1998;37:10-18. (Pubitemid 28385180)
2. Sella A, Kilbourn R, Amato R, et al. Phase II study of ketoconazole combined with weekly doxorubicin in patients with androgen-independent prostate cancer. J Clin Oncol. 1994;12:683-688. (Pubitemid 24110905)
3. Small EJ, Halabi S, Dawson NA, et al. Antiandrogen withdrawal alone or in combination with ketoconazole in androgen-independent prostate cancer patients: a phase III trial (CALGB 9583). J Clin Oncol. 2004;22:1025-1033. (Pubitemid 41095034)
4. Millikan R, Thall PF, Lee SJ, et al. Randomized, multicenter, phase II trial of two multicomponent regimens in androgen-independent prostate cancer. J Clin Oncol. 2003;21:878-883. (Pubitemid 46606448)
5. Larkin M. Low-dose thalidomide seems to be effective in multiple myeloma. Lancet. 1999;354:925.
6. Barlogie B, Tricot G, Anaissie E, et al. Thalidomide and hematopoietic-cell transplantation for multiple myeloma. N Engl J Med. 2006;354:1021-1030. (Pubitemid 43357806)
7. Rajkumar SV, Blood E, Vesole D, Fonseca R, Greipp PR. Phase III clinical trial of thalidomide plus dexamethasone compared with dexamethasone alone in newly diagnosed multiple myeloma: a clinical trial coordinated by the Eastern Cooperative Oncology Group. J Clin Oncol. 2006;24:431-436. (Pubitemid 46630462)
8. Palumbo A, Bringhen S, Caravita T, et al. Oral melphalan and prednisone chemotherapy plus thalidomide compared with melphalan and prednisone alone in elderly patients with multiple myeloma: randomised controlled trial. Lancet. 2006;367:825-831. (Pubitemid 43363369)
9. Strupp C, Germing U, Aivado M, Misgeld E, Haas R, Gattermann N. Thalidomide for the treatment of patients with myelodysplastic syndromes. Leukemia. 2002;16:1-6. (Pubitemid 34105592)
10. Raza A, Meyer P, Dutt D, et al. Thalidomide produces transfusion independence in long-standing refractory anemias of patients with myelodysplastic syndromes. Blood. 2001;98:958-965.
11. Richardson PG, Blood E, Mitsiades CS, et al. A randomized phase 2 study of lenalidomide therapy for patients with relapsed or relapsed and refractory multiple myeloma. Blood. 2006;108:3458-3464. (Pubitemid 44776887)
12. List A, Dewald G, Bennett J, et al. Lenalidomide in the myelodysplastic syndrome with chromosome 5q deletion. N Engl J Med. 2006;355:1456-1465. (Pubitemid 44511560)
13. Sehgal VN. Ciclopirox: a new topical pyrodonium antimycotic agent. A double-blind study in superficial dermatomycoses. Br J Dermatol. 1976;95:83-88.
14. Alpermann HG, Schutz E. [Studies on the pharmacology and toxicology of ciclopiroxolamine (author's transl)]. Arzneimittelforschung. 1981;31:1328-1332.
15. Adam W, Peil HG, Savopoulos C, Vanderbeke O. [Clinical results with the antimycotic agent ciclopiroxolamine (author's transl)]. Arzneimittelforschung. 1981;31:1360-1365.
16. Ward AJ, Rosin MP. A protective effect of chromosome 11 against DNA damage by TPA-activated neutrophils but not TPA acting alone. Carcinogenesis. 1994;15:2851-2857.
17. Grimwade D, Walker H, Oliver F, et al. The importance of diagnostic cytogenetics on outcome in AML: analysis of 1,612 patients entered into the MRC AML 10 trial. The Medical Research Council Adult and Children's Leukaemia Working Parties. Blood. 1998;92:2322-2333.
18. Gunter B, Brideau C, Pikounis B, Liaw A. Statistical and graphical methods for quality control determination of high-throughput screening data. J Biomol Screen. 2003;8:624-633. (Pubitemid 40503571)
19. Mao X, Stewart AK, Hurren R, et al. A chemical biology screen identifies glucocorticoids that regulate c-maf expression by increasing its proteasomal degradation through up-regulation of ubiquitin. Blood. 2007;110:4047-4054. (Pubitemid 350248461)
20. Schimmer AD, Welsh K, Pinilla C, et al. Small-molecule antagonists of apoptosis suppressor XIAP exhibit broad antitumor activity. Cancer Cell. 2004;5:25-35. (Pubitemid 38121594)
21. Hamid R, Rotshteyn Y, Rabadi L, Parikh R, Bullock P. Comparison of alamar blue and MTT assays for high through-put screening. Toxicol In Vitro. 2004;18:703-710. (Pubitemid 38900879)
22. Buick RN, Till JE, McCulloch EA. Colony assay for proliferative blast cells circulating in myeloblastic leukaemia. Lancet. 1977;1:862-863.
23. Schimmer AD, Thomas MP, Hurren R, et al. Identification of small molecules that sensitize resistant tumor cells to tumor necrosis factor-family death receptors. Cancer Res. 2006;66:2367-2375. (Pubitemid 43294952)
24. Krajewski S, Zapata JM, Reed JC. Detection of multiple antigens on western blots. Anal Biochem. 1996;236:221-228. (Pubitemid 26136099)
25. Pham NA, Jacobberger JW, Schimmer AD, Cao P, Gronda M, Hedley DW. The dietary isothiocyanate sulforaphane targets pathways of apoptosis, cell cycle arrest, and oxidative stress in human pancreatic cancer cells and inhibits tumor growth in severe combined immunodeficient mice. Mol Cancer Ther. 2004;3:1239-1248. (Pubitemid 39440169)
26. Breuer W, Epsztejn S, Millgram P, Cabantchik IZ. Transport of iron and other transition metals into cells as revealed by a fluorescent probe. Am J Physiol. 1995;268:C1354-C1361.
27. Breuer W, Epsztejn S, Cabantchik ZI. Iron acquired from transferrin by K562 cells is delivered into a cytoplasmic pool of chelatable iron(II). J Biol Chem. 1995;270:24209-24215.
28. Warner JK, Wang JC, Takenaka K, et al. Direct evidence for cooperating genetic events in the leukemic transformation of normal human hematopoietic cells. Leukemia. 2005;19:1794-1805. (Pubitemid 41486158)
29. Barabé F, Kennedy JA, Hope KJ, Dick JE. Modeling the initiation and progression of human acute leukemia in mice. Science. 2007;316:600-604. (Pubitemid 46683146)
30. Bonnet D, Dick JE. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med. 1997;3:730-737. (Pubitemid 27298715)
31. Mazurier F, Doedens M, Gan OI, Dick JE. Rapid myeloerythroid repopulation after intrafemoral transplantation of NOD-SCID mice reveals a new class of human stem cells. Nat Med. 2003;9:959-963. (Pubitemid 36889941)
32. Wanner RM, Spielmann P, Stroka DM, et al. Epolones induce erythropoietin expression via hypoxia-inducible factor-1 alpha activation. Blood. 2000;96:1558-1565. (Pubitemid 30658491)
33. Stubbe J. Ribonucleotide reductases: amazing and confusing. J Biol Chem. 1990;265:5329-5332.
34. Reichard P. Interactions between deoxyribonucleotide and DNA synthesis. Annu Rev Biochem. 1988;57:349-374.
35. Gräslund A, Sahlin M, Sjoberg BM. The tyrosyl free radical in ribonucleotide reductase. Environ Health Perspect. 1985;64:139-149. (Pubitemid 16135785)
36. Furukawa T, Naitoh Y, Kohno H, Tokunaga R, Taketani S. Iron deprivation decreases ribonucleotide reductase activity and DNA synthesis. Life Sci. 1992;50:2059-2065.
37. Bergeron RJ, Ingeno MJ. Microbial iron chelator-induced cell cycle synchronization in L1210 cells: potential in combination chemotherapy. Cancer Res. 1987;47:6010-6016.
38. Estrov Z, Cohen A, Gelfand EW, Freedman MH. Synergistic antiproliferative effects on HL-60 cells: deferoxamine enhances cytosine arabinoside, methotrexate, and daunorubicin cytotoxicity. Am J Pediatr Hematol Oncol. 1988;10:288-291. (Pubitemid 18273420)
39. Leardi A, Caraglia M, Selleri C, et al. Desferioxamine increases iron depletion and apoptosis induced by ara-C of human myeloid leukaemic cells. Br J Haematol. 1998;102:746-752. (Pubitemid 28387058)
40. Colly LP, Richel DJ, Arentsen-Honders MW, Kester MG, ter Riet PM, Willemze R. Increase in Ara-C sensitivity in Ara-C sensitive and -resistant leukemia by stimulation of the salvage and inhibition of the de novo pathway. Ann Hematol. 1992;65:26-32.
41. Iwasaki H, Huang P, Keating MJ, Plunkett W. Differential incorporation of ara-C, gemcitabine, and fludarabine into replicating and repairing DNA in proliferating human leukemia cells. Blood. 1997;90:270-278. (Pubitemid 27276571)
42. Altieri DC. Survivin, cancer networks and pathway-directed drug discovery. Nat Rev Cancer. 2008;8:61-70.
43. Fukuda S, Pelus LM. Survivin, a cancer target with an emerging role in normal adult tissues. Mol Cancer Ther. 2006;5:1087-1098. (Pubitemid 43881300)
44. Altieri DC. The molecular basis and potential role of survivin in cancer diagnosis and therapy. Trends Mol Med. 2001;7:542-547. (Pubitemid 33127139)
45. Altieri DC. Validating survivin as a cancer therapeutic target. Nat Rev Cancer. 2003;3:46-54. (Pubitemid 37328886)
46. Singer CR, Linch DC. Comparison of the sensitivity of normal and leukaemic myeloid progenitors to in-vitro incubation with cytotoxic drugs: a study of pharmacological purging. Leuk Res. 1987;11:953-959.
47. Spiro TE, Socquet M, Delforge A, Stryckmans P. Chemotherapeutic sensitivity of normal and leukemic hematopoietic progenitor cells to N-[4-(9-acridinylamino)-3-methoxyphenyl]-methanesulfonamide, a new anticancer agent. J Natl Cancer Inst. 1981;66:615-618. (Pubitemid 11101028)
48. Leem SH, Park JE, Kim IS, Chae JY, Sugino A, Sunwoo Y. The possible mechanism of action of ciclopirox olamine in the yeast Saccharomyces cerevisiae. Mol Cells. 2003;15:55-61. (Pubitemid 41582942)
49. Hoffbrand AV, Ganeshaguru K, Hooton JW, Tattersall MH. Effect of iron deficiency and desferrioxamine on DNA synthesis in human cells. Br J Haematol. 1976;33:517-526. (Pubitemid 10150297)
50. Epstein MA, Achong BG, Barr YM. Desferrioxamine and iron. Lancet. 1964;1:708-709.
51. Hodges YK, Antholine WE, Horwitz LD. Effect on ribonucleotide reductase of novel lipophilic iron chelators: the desferri-exochelins. Biochem Biophys Res Commun. 2004;315:595-598.
52. Thelander L, Eriksson S, Akerman M. Ribonucleotide reductase from calf thymus: separation of the enzyme into two nonidentical subunits, proteins M1 and M2. J Biol Chem. 1980;255:7426-7432.
53. Li J, Zheng LM, King I, Doyle TW, Chen SH. Syntheses and antitumor activities of potent inhibitors of ribonucleotide reductase: 3-amino-4-methylpyridine-2-carboxaldehydethiosemicarba- zone (3-AMP), 3-amino-pyridine-2-carboxaldehyde-thiosemicarbazone (3-AP) and its water-soluble prodrugs. Curr Med Chem. 2001;8:121-133. (Pubitemid 32409769)
54. McClarty GA, Chan AK, Wright JA. Hydroxyurea-induced conversion of mammalian ribonucleotide reductase to a form hypersensitive to bleomycin. Cancer Res. 1986;46:4516-4521.
55. Park MH, Wolff EC, Folk JE. Is hypusine essential for eukaryotic cell proliferation? Trends Biochem Sci. 1993;18:475-479. (Pubitemid 23362305)
56. Schnier J, Schwelberger HG, Smit-McBride Z, Kang HA, Hershey JW. Translation initiation factor 5A and its hypusine modification are essential for cell viability in the yeast Saccharomyces cerevisiae. Mol Cell Biol. 1991;11:3105-3114. (Pubitemid 21895697)
57. Clement PM, Hanauske-Abel HM, Wolff EC, Kleinman HK, Park MH. The antifungal drug ciclopirox inhibits deoxyhypusine and proline hydroxylation, endothelial cell growth and angiogenesis in vitro. Int J Cancer. 2002;100:491-498.