Disulfiram when combined with copper enhances the therapeutic effects of temozolomide for the treatment of glioblastoma

Clinical Cancer Research

Volumn 22, Issue 15, 2016, Pages 3860-3875

  Lun, Xueqing ^a   Wells, J Connor ^a   Grinshtein, Natalie ^b   King, Jennifer C ^a   Hao, Xiaoguang ^a   Dang, Ngoc Ha ^a   Wang, Xiuling ^a   Aman, Ahmed ^c   Uehling, David ^c   Datti, Alessandro ^d,e   Wrana, Jeffrey L ^d,f   Easaw, Jacob C ^a   Luchman, Artee ^a   Weiss, Samuel ^a,g   Cairncross, J Gregory ^a   Kaplan, David R ^b,f   Robbins, Stephen M ^a   Senger, Donna L ^a  

^a UNIVERSITY OF CALGARY   (Canada)

^b HOSPITAL FOR SICK CHILDREN   (Canada)

^c ONTARIO INSTITUTE FOR CANCER RESEARCH   (Canada)

^d MOUNT SINAI HOSPITAL   (Canada)

^e UNIVERSITY OF PERUGIA   (Italy)

^f UNIVERSITY OF TORONTO   (Canada)

^g UNIVERSITY OF CALGARY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

COPPER; DISULFIRAM; TEMOZOLOMIDE; ANTINEOPLASTIC AGENT; DACARBAZINE; PROTEASOME;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN TUMOR INITIATING CELL; CANCER CELL; CANCER CELL LINE; CANCER INHIBITION; CANCER SURVIVAL; CANCER TISSUE; CELL RENEWAL; CONTROLLED STUDY; DNA DAMAGE; DRUG CYTOTOXICITY; DRUG EFFICACY; DRUG POTENTIATION; FEMALE; GAMMA IRRADIATION; GLIOBLASTOMA; HIGH THROUGHPUT SCREENING; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOFLUORESCENCE; IN VITRO STUDY; IN VIVO STUDY; MICROARRAY ANALYSIS; MOUSE; MULTIPLE CYCLE TREATMENT; NONHUMAN; PRIORITY JOURNAL; WESTERN BLOTTING; ANALOGS AND DERIVATIVES; ANIMAL; CANCER STEM CELL; CELL PROLIFERATION; CELL SURVIVAL; DISEASE MODEL; DNA REPAIR; DRUG EFFECTS; DRUG RESISTANCE; DRUG SCREENING; GENE EXPRESSION PROFILING; GENETICS; METABOLISM; PATHOLOGY; TUMOR VOLUME;

ANIMALS; ANTINEOPLASTIC AGENTS; CELL PROLIFERATION; CELL SURVIVAL; COPPER; DACARBAZINE; DISEASE MODELS, ANIMAL; DISULFIRAM; DNA REPAIR; DRUG RESISTANCE, NEOPLASM; DRUG SCREENING ASSAYS, ANTITUMOR; DRUG SYNERGISM; FEMALE; GENE EXPRESSION PROFILING; GLIOBLASTOMA; HIGH-THROUGHPUT SCREENING ASSAYS; HUMANS; MICE; NEOPLASTIC STEM CELLS; PROTEASOME ENDOPEPTIDASE COMPLEX; TUMOR BURDEN; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84979980421     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-15-1798     Document Type: Article

References (52)

1. Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJ, et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 2005;352:987-96.
2. Cusulin C, Chesnelong C, Bose P, Bilenky M, Kopciuk K, Chan JA, et al. Precursor states of brain tumor initiating cell lines are predictive of survival in xenografts and associated with glioblastoma subtypes. Stem Cell Reports 2015;5:1-9.
3. Kelly JJ, Stechishin O, Chojnacki A, Lun X, Sun B, Senger DL, et al. Proliferation of human glioblastoma stem cells occurs independently of exogenous mitogens. Stem Cells 2009;27:1722-33.
4. Bao S, Wu Q, McLendon RE, Hao Y, Shi Q, Hjelmeland AB, et al. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 2006;444:756-60.
5. Singh SK, Hawkins C, Clarke ID, Squire JA, Bayani J, Hide T, et al. Identification of human brain tumour initiating cells. Nature 2004; 432:396-401.
6. Beier D, Schulz JB, Beier CP. Chemoresistance of glioblastoma cancer stem cells-much more complex than expected. Mol Cancer 2011;10:128.
7. Galli R, Binda E, Orfanelli U, Cipelletti B, Gritti A, De Vitis S, et al. Isolation and characterization of tumorigenic, stem-like neural precursors from human glioblastoma. Cancer Res 2004;64:7011-21.
8. Salmaggi A, Boiardi A, Gelati M, Russo A, Calatozzolo C, Ciusani E, et al. Glioblastoma-derived tumorospheres identify a population of tumor stem-like cells with angiogenic potential and enhanced multidrug resistance phenotype. Glia 2006;54:850-60.
9. Hegi ME, Diserens AC, Gorlia T, Hamou MF, de Tribolet N, Weller M, et al. MGMT gene silencing and benefit from temozolomide in glioblastoma. N Engl J Med 2005;352:997-1003.
10. Messaoudi K, Clavreul A, Lagarce F. Toward an effective strategy in glioblastoma treatment. Part I: resistance mechanisms and strategies to overcome resistance of glioblastoma to temozolomide. Drug Discov Today 2015;20:899-905.
11. Blough MD, Westgate MR, Beauchamp D, Kelly JJ, Stechishin O, Ramirez AL, et al. Sensitivity to temozolomide in brain tumor initiating cells. Neuro Oncol 2010;12:756-60.
12. Kelly JJ, Blough MD, Stechishin OD, Chan JA, Beauchamp D, Perizzolo M, et al. Oligodendroglioma cell lines containing t(1;19)(q10;p10). Neuro Oncol 2010;12:745-55.
13. Nguyen SA, Stechishin OD, Luchman HA, Lun XQ, Senger DL, Robbins SM, et al. Novel MSH6 mutations in treatment naive glioblastoma and anaplastic oligodendroglioma influence temozolomide resistance independently of MGMT methylation. Clin Cancer Res 2014;20:4894-903.
14. Cen D, Brayton D, Shahandeh B, Meyskens FL Jr, Farmer PJ. Disulfiram facilitates intracellular Cu uptake and induces apoptosis in human melanoma cells. J Med Chem 2004;47:6914-20.
15. Chen D, Cui QC, Yang H, Dou QP. Disulfiram, a clinically used antialcoholism drug and copper-binding agent, induces apoptotic cell death in breast cancer cultures and xenografts via inhibition of the proteasome activity. Cancer Res 2006;66:10425-33.
16. Conticello C, Martinetti D, Adamo L, Buccheri S, Giuffrida R, Parrinello N, et al. Disulfiram, an old drug with new potential therapeutic uses for human hematological malignancies. Int J Cancer 2012;131:2197-203.
17. Hothi P, Martins TJ, Chen L, Deleyrolle L, Yoon JG, Reynolds B, et al. Highthroughput chemical screens identify disulfiram as an inhibitor of human glioblastoma stem cells. Oncotarget 2012;3:1124-36.
18. Liu P, Brown S, Goktug T, Channathodiyil P, Kannappan V, Hugnot JP, et al. Cytotoxic effect of disulfiram/copper on human glioblastoma cell lines and ALDH-positive cancer-stem-like cells. Br J Cancer 2012; 107:1488-97.
19. Wickstrom M, Danielsson K, Rickardson L, Gullbo J, Nygren P, Isaksson A, et al. Pharmacological profiling of disulfiram using human tumor cell lines and human tumor cells from patients. Biochem Pharmacol 2007;73:25-33.
20. Johansson B. A review of the pharmacokinetics and pharmacodynamics of disulfiram and its metabolites. Acta Psychiatr Scand Suppl 1992;369: 15-26.
21. Borup C, Kaiser A, Jensen E. Long-term Antabuse treatment: tolerance and reasons for withdrawal. Acta Psychiatr Scand Suppl 1992;369:47-9.
22. Cvek B. Targeting malignancies with disulfiram (Antabuse): multidrug resistance, angiogenesis, and proteasome. Curr Cancer Drug Targets 2011;11:332-7.
23. Safi R, Nelson ER, Chitneni SK, Franz KJ, George DJ, Zalutsky MR, et al. Copper signaling axis as a target for prostate cancer therapeutics. Cancer Res 2014;74:5819-31.
24. Westhoff MA, Zhou S, Nonnenmacher L, Karpel-Massler G, Jennewein C, Schneider M, et al. Inhibition of NF-kappaB signaling ablates the invasive phenotype of glioblastoma. Mol Cancer Res 2013;11:1611-23.
25. Yip NC, Fombon IS, Liu P, Brown S, Kannappan V, Armesilla AL, et al. Disulfiram modulated ROS-MAPK and NFkappaB pathways and targeted breast cancer cells with cancer stem cell-like properties. Br J Cancer 2011;104:1564-74.
26. Kona FR, Buac D, A MB. Disulfiram, and disulfiram derivatives as novel potential anticancer drugs targeting the ubiquitin-proteasome system in both preclinical and clinical studies. Curr Cancer Drug Targets 2011; 11:338-46.
27. Brar SS, Grigg C, Wilson KS, Holder WD Jr, Dreau D, Austin C, et al. Disulfiram inhibits activating transcription factor/cyclic AMP-responsive element binding protein and human melanoma growth in a metal-dependent manner in vitro, in mice and in a patient with metastatic disease. Mol Cancer Ther 2004;3:1049-60.
28. Zemp FJ, Lun X, McKenzie BA, Zhou H, Maxwell L, Sun B, et al. Treating brain tumor-initiating cells using a combination of myxoma virus and rapamycin. Neuro Oncol 2013;15:904-20.
29. Rabinovich BA, Ye Y, Etto T, Chen JQ, Levitsky HI, Overwijk WW, et al. Visualizing fewer than 10 mouse T cells with an enhanced firefly luciferase in immunocompetent mouse models of cancer. Proc Natl Acad Sci U S A 2008;105:14342-6.
30. Grinshtein N, Datti A, Fujitani M, Uehling D, Prakesch M, Isaac M, et al. Small molecule kinase inhibitor screen identifies polo-like kinase 1 as a target for neuroblastoma tumor-initiating cells. Cancer Res 2011;71: 1385-95.
31. Smith KM, Datti A, Fujitani M, Grinshtein N, Zhang L, Morozova O, et al. Selective targeting of neuroblastoma tumour-initiating cells by compounds identified in stem cell-based small molecule screens. EMBO Mol Med 2010;2:371-84.
32. Wang L, Rahn JJ, Lun X, Sun B, Kelly JJ, Weiss S, et al. Gamma-secretase represents a therapeutic target for the treatment of invasive glioma mediated by the p75 neurotrophin receptor. PLoS Biol 2008;6:e289.
33. Ahn BY, Saldanha-Gama RF, Rahn JJ, Hao X, Zhang J, Dang NH, et al. Glioma invasion mediated by the p75 neurotrophin receptor (p75/ CD271) requires regulated interaction with PDLIM1. Oncogene 2016;35:1411-22.
34. Johnston AL, Lun X, Rahn JJ, Liacini A, Wang L, Hamilton MG, et al. The p75 neurotrophin receptor is a central regulator of glioma invasion. PLoS Biol 2007;5:e212.
35. Reynolds BA, Tetzlaff W, Weiss S. A multipotent EGF-responsive striatal embryonic progenitor cell produces neurons and astrocytes. J Neurosci 1992;12:4565-74.
36. De Lepeleire I, Reiss TF, Rochette F, Botto A, Zhang J, Kundu S, et al. Montelukast causes prolonged, potent leukotriene D4-receptor antagonism in the airways of patients with asthma. Clin Pharmacol Ther 1997;61:83-92.
37. Reiss TF, Sorkness CA, Stricker W, Botto A, Busse WW, Kundu S, et al. Effects of montelukast (MK-0476); a potent cysteinyl leukotriene receptor antagonist, on bronchodilation in asthmatic subjects treated with and without inhaled corticosteroids. Thorax 1997;52:45-8.
38. Richards DA. Prophylactic value of clioquinol against travellers' diarrhoea. Lancet 1971;1:44-5.
39. Cvek B. Nonprofit drugs as the salvation of the world's healthcare systems: the case of Antabuse (disulfiram). Drug Discov Today 2012;17:409-12.
40. Choi SA, Choi JW, Wang KC, Phi JH, Lee JY, Park KD, et al. Disulfiram modulates stemness and metabolism of brain tumor initiating cells in atypical teratoid/rhabdoid tumors. Neuro Oncol 2015;17:810-21.
41. Kast RE, Halatsch ME. Matrix metalloproteinase-2 and -9 in glioblastoma: a trio of old drugs-captopril, disulfiram and nelfinavir-are inhibitors with potential as adjunctive treatments in glioblastoma. Arch Med Res 2012;43:243-7.
42. Triscott J, Lee C, Hu K, Fotovati A, Berns R, Pambid M, et al. Disulfiram, a drug widely used to control alcoholism, suppresses the self-renewal of glioblastoma and over-rides resistance to temozolomide. Oncotarget 2012;3:1112-23.
43. Paranjpe A, Zhang R, Ali-Osman F, Bobustuc GC, Srivenugopal KS. Disulfiram is a direct and potent inhibitor of human O6-methylguanine-DNA methyltransferase (MGMT) in brain tumor cells and mouse brain and markedly increases the alkylating DNA damage. Carcinogenesis 2014; 35:692-702.
44. Kreklau EL, Kurpad C, Williams DA, Erickson LC. Prolonged inhibition of O(6)-methylguanine DNA methyltransferase in human tumor cells by O (6)-benzylguanine in vitro and in vivo. J Pharmacol Exp Ther 1999;291: 1269-75.
45. Veverka KA, Johnson KL, Mays DC, Lipsky JJ, Naylor S. Inhibition of aldehyde dehydrogenase by disulfiram and its metabolite methyl diethylthiocarbamoyl-sulfoxide. Biochem Pharmacol 1997;53:511-8.
46. Hemmati HD, Nakano I, Lazareff JA, Masterman-Smith M, Geschwind DH, Bronner-Fraser M, et al. Cancerous stem cells can arise from pediatric brain tumors. Proc Natl Acad Sci U S A 2003;100:15178-83.
47. Vescovi AL, Galli R, Reynolds BA. Brain tumour stem cells. Nat Rev Cancer 2006;6:425-36.
48. Chen J, Li Y, Yu TS, McKay RM, Burns DK, Kernie SG, et al. A restricted cell population propagates glioblastoma growth after chemotherapy. Nature 2012;488:522-6.
49. Moreb JS, Ucar D, Han S, Amory JK, Goldstein AS, Ostmark B, et al. The enzymatic activity of human aldehyde dehydrogenases 1A2 and 2 (ALDH1A2 and ALDH2) is detected by Aldefluor, inhibited by diethylaminobenzaldehyde and has significant effects on cell proliferation and drug resistance. Chem Biol Interact 2012;195:52-60.
50. Landen CN Jr, Goodman B, Katre AA, Steg AD, Nick AM, Stone RL, et al. Targeting aldehyde dehydrogenase cancer stem cells in ovarian cancer. Mol Cancer Ther 2010;9:3186-99.
51. Hegi ME, Stupp R. Withholding temozolomide in glioblastoma patients with unmethylated MGMT promoter-still a dilemma? Neuro Oncol 2015;17:1425-7.
52. Gourzones-Dmitriev C, Kassambara A, Sahota S, Reme T, Moreaux J, Bourquard P, et al. DNA repair pathways in human multiple myeloma: role in oncogenesis and potential targets for treatment. Cell Cycle 2013;12:2760-73.