Login Register Cart 0
Generic placeholder image

Current Pharmaceutical Design

Editor-in-Chief

ISSN (Print): 1381-6128
ISSN (Online): 1873-4286

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
General Review Article

An Updated Review of Disulfiram: Molecular Targets and Strategies for Cancer Treatment

Author(s): Qingzhu Yang, Yao Yao, Kai Li, Lin Jiao, Jiazhen Zhu, Cheng Ni, Mengmeng Li, Q. Ping Dou* and Huanjie Yang*

Volume 25, Issue 30, 2019

Page: [3248 - 3256] Pages: 9

DOI: 10.2174/1381612825666190816233755

Price: $65

Abstract

Repurposing already approved drugs as new anticancer agents is a promising strategy considering the advantages such as low costs, low risks and less time-consumption. Disulfiram (DSF), as the first drug for antialcoholism, was approved by the U.S. Food and Drug Administration (FDA) over 60 years ago. Increasing evidence indicates that DSF has great potential for the treatment of various human cancers. Several mechanisms and targets of DSF related to cancer therapy have been proposed, including the inhibition of ubiquitin-proteasome system (UPS), cancer cell stemness and cancer metastasis, and alteration of the intracellular reactive oxygen species (ROS). This article provides a brief review about the history of the use of DSF in humans and its molecular mechanisms and targets of anticancer therapy, describes DSF delivery strategies for cancer treatment, summarizes completed and ongoing cancer clinical trials involving DSF, and offers strategies to better use DSF in cancer therapies.

Keywords: Disulfiram, cancer, molecular targets, drug delivery, clinical trials, anticancer agents.

« Previous Next »
[1]
Grodzki M. Ueber äthylirte Sulfoharnstoffe. Eur J Inorg Chem 1881; 14(2): 2754-8.
[2]
Kwentus J, Major LF. Disulfiram in the treatment of alcoholism; a review. J Stud Alcohol 1979; 40(5): 428-46.
[http://dx.doi.org/10.15288/jsa.1979.40.428] [PMID: 381789]
[3]
Sauna ZE, Shukla S, Ambudkar SV. Disulfiram, an old drug with new potential therapeutic uses for human cancers and fungal infections. Mol Biosyst 2005; 1(2): 127-34.
[http://dx.doi.org/10.1039/b504392a] [PMID: 16880974]
[4]
Williams EE. Effects of alcohol on workers with carbon disulfide. J Am Med Assoc 1937; 109(109): 1472-3.
[5]
Hald J, Jacobsen E. A drug sensitizing the organism to ethyl alcohol. Lancet 1948; 2(6539): 1001-4.
[http://dx.doi.org/10.1016/S0140-6736(48)91514-1] [PMID: 18103475]
[6]
Jacobsen E. The metabolism of ethyl alcohol. Pharmacol Rev 1952; 4(2): 107-35.
[PMID: 1484941672]
[7]
Marshall EK Jr, Fritz WF. The metabolism of ethyl alcohol. J Pharmacol Exp Ther 1953; 109(4): 431-43.
[PMID: 13109709]
[8]
Kjeldgaard NO. Inhibition of aldehyde oxidase from liver by tetraethylthiuram-disulphide (Antabuse). Pharmacol Toxicol 2009; 5(4): 397-403.
[9]
Harada S, Agarwal DP, Goedde HW. Mechanism of alcohol sensitivity and disulfiram-ethanol reaction. Subst Alcohol Actions Misuse 1982; 3(1-2): 107-15.
[PMID: 7135154]
[10]
Barth KS, Malcolm RJ. Disulfiram: an old therapeutic with new applications. CNS Neurol Disord Drug Targets 2010; 9(1): 5-12.
[http://dx.doi.org/10.2174/187152710790966678] [PMID: 20201810]
[11]
Skrott Z, Mistrik M, Andersen KK, et al. Alcohol-abuse drug disulfiram targets cancer via p97 segregase adaptor NPL4. Nature 2017; 552(7684): 194-9.
[http://dx.doi.org/10.1038/nature25016] [PMID: 29211715]
[12]
Wattenberg LW. Inhibition of dimethylhydrazine-induced neoplasia of the large intestine by disulfiram. J Natl Cancer Inst 1975; 54(4): 1005-6.
[http://dx.doi.org/10.1093/jnci/54.4.1005] [PMID: 1127713]
[13]
Chen D, Cui QC, Yang H, Dou QP. Disulfiram, a clinically used anti-alcoholism 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(21): 10425-33.
[http://dx.doi.org/10.1158/0008-5472.CAN-06-2126] [PMID: 17079463]
[14]
Liu X, Wang L, Cui W, et al. Targeting ALDH1A1 by disulfiram/copper complex inhibits non-small cell lung cancer recurrence driven by ALDH-positive cancer stem cells. Oncotarget 2016; 7(36): 58516-30.
[http://dx.doi.org/10.18632/oncotarget.11305] [PMID: 27542268]
[15]
Papaioannou M, Mylonas I, Kast RE, Brüning A. Disulfiram/copper causes redox-related proteotoxicity and concomitant heat shock response in ovarian cancer cells that is augmented by auranofin-mediated thioredoxin inhibition. Oncoscience 2013; 1(1): 21-9.
[http://dx.doi.org/10.18632/oncoscience.5] [PMID: 25593981]
[16]
Hothi P, Martins TJ, Chen L, et al. High-throughput chemical screens identify disulfiram as an inhibitor of human glioblastoma stem cells. Oncotarget 2012; 3(10): 1124-36.
[http://dx.doi.org/10.18632/oncotarget.707] [PMID: 23165409]
[17]
Liu P, Brown S, Goktug T, et al. Cytotoxic effect of disulfiram/copper on human glioblastoma cell lines and ALDH-positive cancer-stem-like cells. Br J Cancer 2012; 107(9): 1488-97.
[http://dx.doi.org/10.1038/bjc.2012.442] [PMID: 23033007]
[18]
Jin N, Zhu X, Cheng F, Zhang L. Disulfiram/copper targets stem cell-like ALDH+ population of multiple myeloma by inhibition of ALDH1A1 and Hedgehog pathway. J Cell Biochem 2018; 119(8): 6882-93.
[http://dx.doi.org/10.1002/jcb.26885] [PMID: 29665144]
[19]
Kim SK, Kim H, Lee DH, et al. Reversing the intractable nature of pancreatic cancer by selectively targeting ALDH-high, therapy-resistant cancer cells. PLoS One 2013; 8(10) e78130
[http://dx.doi.org/10.1371/journal.pone.0078130] [PMID: 24194908]
[20]
Wu L, Meng F, Dong L, et al. Disulfiram and BKM120 in combination with chemotherapy impede tumor progression and delay tumor recurrence in tumor initiating cell-rich TNBC. Sci Rep 2019; 9(1): 236.
[http://dx.doi.org/10.1038/s41598-018-35619-6] [PMID: 30659204]
[21]
Cho HJ, Lee TS, Park JB, et al. Disulfiram suppresses invasive ability of osteosarcoma cells via the inhibition of MMP-2 and MMP-9 expression. J Biochem Mol Biol 2007; 40(6): 1069-76.
[PMID: 18047805]
[22]
Wang NN, Wang LH, Li Y, et al. Targeting ALDH2 with disulfiram/copper reverses the resistance of cancer cells to microtubule inhibitors. Exp Cell Res 2018; 362(1): 72-82.
[http://dx.doi.org/10.1016/j.yexcr.2017.11.004] [PMID: 29155365]
[23]
Li Y, Fu SY, Wang LH, et al. Copper improves the anti-angiogenic activity of disulfiram through the EGFR/Src/VEGF pathway in gliomas. Cancer Lett 2015; 369(1): 86-96.
[http://dx.doi.org/10.1016/j.canlet.2015.07.029] [PMID: 26254539]
[24]
Kim JY, Cho Y, Oh E, et al. Disulfiram targets cancer stem-like properties and the HER2/Akt signaling pathway in HER2-positive breast cancer. Cancer Lett 2016; 379(1): 39-48.
[http://dx.doi.org/10.1016/j.canlet.2016.05.026] [PMID: 27238567]
[25]
Xu B, Wang S, Li R, et al. Disulfiram/copper selectively eradicates AML leukemia stem cells in vitro and in vivo by simultaneous induction of ROS-JNK and inhibition of NF-κB and Nrf2. Cell Death Dis 2017; 8(5) e2797
[http://dx.doi.org/10.1038/cddis.2017.176] [PMID: 28518151]
[26]
Wang H, Yang Q, Dou QP, Yang H. Discovery of natural product proteasome inhibitors as novel anticancer therapeutics: current status and perspectives. Curr Protein Pept Sci 2018; 19(4): 358-67.
[http://dx.doi.org/10.2174/1389203718666170111121856] [PMID: 28079010]
[27]
Kleiger G, Mayor T. Perilous journey: a tour of the ubiquitin-proteasome system. Trends Cell Biol 2014; 24(6): 352-9.
[http://dx.doi.org/10.1016/j.tcb.2013.12.003] [PMID: 24457024]
[28]
Lövborg H. Ouml, Berg F, Rickardson L, Gullbo J, Nygren P, Larsson R. Inhibition of proteasome activity, nuclear factor-κB translocation and cell survival by the antialcoholism drug disulfiram. Int J Cancer 2006; 118(6): 1577-80.
[http://dx.doi.org/10.1002/ijc.21534] [PMID: 16206267]
[29]
Rickardson L, Wickström M, Larsson R, Lövborg H. Image-based screening for the identification of novel proteasome inhibitors. J Biomol Screen 2007; 12(2): 203-10.
[http://dx.doi.org/10.1177/1087057106297115] [PMID: 17208922]
[30]
Cvek B, Milacic V, Taraba J, Dou QP. Ni(II), Cu(II), and Zn(II) diethyldithiocarbamate complexes show various activities against the proteasome in breast cancer cells. J Med Chem 2008; 51(20): 6256-8.
[http://dx.doi.org/10.1021/jm8007807] [PMID: 18816109]
[31]
Hasinoff BB, Patel D. Disulfiram is a slow-binding partial noncompetitive inhibitor of 20S proteasome activity. Arch Biochem Biophys 2017; 633: 23-8.
[http://dx.doi.org/10.1016/j.abb.2017.09.003] [PMID: 28887129]
[32]
Lun X, Wells JC, Grinshtein N, et al. Disulfiram when combined with copper enhances the therapeutic effects of temozolomide for the treatment of glioblastoma. Clin Cancer Res 2016; 22(15): 3860-75.
[http://dx.doi.org/10.1158/1078-0432.CCR-15-1798] [PMID: 27006494]
[33]
Song X, Kim SY, Zhou Z, Lagasse E, Kwon YT, Lee YJ. Hyperthermia enhances mapatumumab-induced apoptotic death through ubiquitin-mediated degradation of cellular FLIP(long) in human colon cancer cells. Cell Death Dis 2013; 4(4)e577
[http://dx.doi.org/10.1038/cddis.2013.104] [PMID: 23559011]
[34]
Isakov E, Stanhill A. Stalled proteasomes are directly relieved by P97 recruitment. J Biol Chem 2011; 286(35): 30274-83.
[http://dx.doi.org/10.1074/jbc.M111.240309] [PMID: 21733848]
[35]
Siddique HR, Saleem M. Role of BMI1, a stem cell factor, in cancer recurrence and chemoresistance: preclinical and clinical evidences. Stem Cells 2012; 30(3): 372-8.
[http://dx.doi.org/10.1002/stem.1035] [PMID: 22252887]
[36]
Carnero A, Garcia-Mayea Y, Mir C, Lorente J, Rubio IT. LLeonart ME. The cancer stem-cell signaling network and resistance to therapy. Cancer Treat Rev 2016; 49: 25-36.
[http://dx.doi.org/10.1016/j.ctrv.2016.07.001] [PMID: 27434881]
[37]
Toledo-Guzmán M, Ibañez MH, Gomez-Gallegos A, Ortiz-Sánchez E. ALDH as a stem cell marker in solid tumors. Curr Stem Cell Res Ther 2019; 14(5): 375-88.
[PMID: 30095061]
[38]
Koppaka V, Thompson DC, Chen Y, et al. Aldehyde dehydrogenase inhibitors: a comprehensive review of the pharmacology, mechanism of action, substrate specificity, and clinical application. Pharmacol Rev 2012; 64(3): 520-39.
[http://dx.doi.org/10.1124/pr.111.005538] [PMID: 22544865]
[39]
Iwatsuki M, Mimori K, Yokobori T, et al. Epithelial-mesenchymal transition in cancer development and its clinical significance. Cancer Sci 2010; 101(2): 293-9.
[http://dx.doi.org/10.1111/j.1349-7006.2009.01419.x] [PMID: 19961486]
[40]
Li Y, Wang LH, Zhang HT, et al. Disulfiram combined with copper inhibits metastasis and epithelial-mesenchymal transition in hepatocellular carcinoma through the NF-κB and TGF-β pathways. J Cell Mol Med 2018; 22(1): 439-51.
[http://dx.doi.org/10.1111/jcmm.13334] [PMID: 29148232]
[41]
Korkaya H, Paulson A, Iovino F, Wicha M. HER2 regulates the normal and malignant mammary stem/progenitor cell population that drives tumorigenesis and invasion. Oncogene 2008; 27(47): 6120-30.
[http://dx.doi.org/10.1038/onc.2008.207] [PMID: 18591932]
[42]
Duru N, Candas D, Jiang G, Li JJ. Breast cancer adaptive resistance: HER2 and cancer stem cell repopulation in a heterogeneous tumor society. J Cancer Res Clin Oncol 2014; 140(1): 1-14.
[http://dx.doi.org/10.1007/s00432-013-1494-1] [PMID: 23990015]
[43]
Galadari S, Rahman A, Pallichankandy S, Thayyullathil F. Reactive oxygen species and cancer paradox: To promote or to suppress? Free Radic Biol Med 2017; 104: 144-64.
[http://dx.doi.org/10.1016/j.freeradbiomed.2017.01.004] [PMID: 28088622]
[44]
Lin S, Li Y, Jr AAZ, Werner J, Bazhin AV. Reactive oxygen species and colorectal cancer. J Cell Physiol 2017; 9(4): 350-7.
[PMID: 29215746]
[45]
Qian X, Nie X, Yao W, et al. Reactive oxygen species in cancer stem cells of head and neck squamous cancer. Semin Cancer Biol 2018; 53: 248-57.
[http://dx.doi.org/10.1016/j.semcancer.2018.06.001] [PMID: 29935313]
[46]
Yip NC, Fombon IS, Liu P, et al. Disulfiram modulated ROS-MAPK and NFκB pathways and targeted breast cancer cells with cancer stem cell-like properties. Br J Cancer 2011; 104(10): 1564-74.
[http://dx.doi.org/10.1038/bjc.2011.126] [PMID: 21487404]
[47]
Morrison BW, Doudican NA, Patel KR, Orlow SJ. Disulfiram induces copper-dependent stimulation of reactive oxygen species and activation of the extrinsic apoptotic pathway in melanoma. Melanoma Res 2010; 20(1): 11-20.
[http://dx.doi.org/10.1097/CMR.0b013e328334131d] [PMID: 19966593]
[48]
Chiba T, Suzuki E, Yuki K, et al. Disulfiram eradicates tumor-initiating hepatocellular carcinoma cells in ROS-p38 MAPK pathway-dependent and -independent manners. PLoS One 2014; 9(1) e84807
[http://dx.doi.org/10.1371/journal.pone.0084807] [PMID: 24454751]
[49]
Park YM, Go YY, Shin SH, Cho JG, Woo JS, Song JJ. Anti-cancer effects of disulfiram in head and neck squamous cell carcinoma via autophagic cell death. PLoS One 2018; 13(9) e0203069
[http://dx.doi.org/10.1371/journal.pone.0203069] [PMID: 30212479]
[50]
Yang Z, Guo F, Albers AE, Sehouli J, Kaufmann AM. Disulfiram modulates ROS accumulation and overcomes synergistically cisplatin resistance in breast cancer cell lines. Biomed Pharmacother 2019; 113108727
[http://dx.doi.org/10.1016/j.biopha.2019.108727] [PMID: 30870721]
[51]
D’Autréaux B, Toledano MB. ROS as signalling molecules: mechanisms that generate specificity in ROS homeostasis. Nat Rev Mol Cell Biol 2007; 8(10): 813-24.
[http://dx.doi.org/10.1038/nrm2256] [PMID: 17848967]
[52]
Chithiramohan A, George S. Pharmacological interventions for alcohol relapse prevention. Int J Med Update 2015; 10(2): 41-5.
[http://dx.doi.org/10.4314/ijmu.v10i2.7]
[53]
Fuller RK, Gordis E. Does disulfiram have a role in alcoholism treatment today? Addiction 2004; 99(1): 21-4.
[http://dx.doi.org/10.1111/j.1360-0443.2004.00597.x] [PMID: 14678055]
[54]
Strømme JH, Eldjarn L. Distribution and chemical forms of diethyldithiocarbamate and tetraethylthiuram disulphide (disculfiram) in mice in relation to radioprotection. Biochem Pharmacol 1966; 15(3): 287-97.
[http://dx.doi.org/10.1016/0006-2952(66)90300-5] [PMID: 5911543]
[55]
Glauser TA, Nelson AN, Zembower DE, Lipsky JJ, Weinshilboum RM. Diethyldithiocarbamate S-methylation: evidence for catalysis by human liver thiol methyltransferase and thiopurine methyltransferase. J Pharmacol Exp Ther 1993; 266(1): 23-32.
[PMID: 8392551]
[56]
Butcher K, Kannappan V, Kilari RS, et al. Investigation of the key chemical structures involved in the anticancer activity of disulfiram in A549 non-small cell lung cancer cell line. BMC Cancer 2018; 18(1): 753.
[http://dx.doi.org/10.1186/s12885-018-4617-x] [PMID: 30031402]
[57]
Madan A, Parkinson A, Faiman MD. Identification of the human P-450 enzymes responsible for the sulfoxidation and thiono-oxidation of diethyldithiocarbamate methyl ester: role of P-450 enzymes in disulfiram bioactivation. Alcohol Clin Exp Res 1998; 22(6): 1212-9.
[http://dx.doi.org/10.1111/j.1530-0277.1998.tb03901.x] [PMID: 9756035]
[58]
Johansson B, Petersen EN, Arnold E. Diethylthiocarbamic acid methyl ester. A potent inhibitor of aldehyde dehydrogenase found in rats treated with disulfiram or diethyldithiocarbamic acid methyl ester. Biochem Pharmacol 1989; 38(7): 1053-9.
[http://dx.doi.org/10.1016/0006-2952(89)90248-7] [PMID: 2539814]
[59]
Hart BW, Faiman MD. In vitro and in vivo inhibition of rat liver aldehyde dehydrogenase by S-methyl N,N-diethylthiolcarbamate sulfoxide, a new metabolite of disulfiram. Biochem Pharmacol 1992; 43(3): 403-6.
[http://dx.doi.org/10.1016/0006-2952(92)90555-W] [PMID: 1311578]
[60]
Madan A, Parkinson A, Faiman MD. Identification of the human and rat P450 enzymes responsible for the sulfoxidation of S-methyl N,N-diethylthiolcarbamate (DETC-ME). The terminal step in the bioactivation of disulfiram. Drug Metab Dispos 1995; 23(10): 1153-62.
[PMID: 8654205]
[61]
Mays DC, Nelson AN, Fauq AH, et al. S-methyl N,N-diethylthiocarbamate sulfone, a potential metabolite of disulfiram and potent inhibitor of low Km mitochondrial aldehyde dehydrogenase. Biochem Pharmacol 1995; 49(5): 693-700.
[http://dx.doi.org/10.1016/0006-2952(94)00504-F] [PMID: 7887984]
[62]
Center for Substance Abuse Treatment.. Incorporating alcohol pharmacotherapies into medical practice.Treatment Improvement Protocol (TIP) Series No 49. Rockville, MD: Substance Abuse and Mental Health Services Administration (US): 2009. Report No.: (SMA) 09-4380.
[63]
Wang Y, Li W, Patel SS, et al. Blocking the formation of radiation-induced breast cancer stem cells. Oncotarget 2014; 5(11): 3743-55.
[http://dx.doi.org/10.18632/oncotarget.1992] [PMID: 25003837]
[64]
Arnal N, de Alaniz MJ, Marra CA. Cytotoxic effects of copper overload on human-derived lung and liver cells in culture. Biochim Biophys Acta 2012; 1820(7): 931-9.
[http://dx.doi.org/10.1016/j.bbagen.2012.03.007] [PMID: 22450155]
[65]
Ishida S, Andreux P, Poitry-Yamate C, Auwerx J, Hanahan D. Bioavailable copper modulates oxidative phosphorylation and growth of tumors. Proc Natl Acad Sci USA 2013; 110(48): 19507-12.
[http://dx.doi.org/10.1073/pnas.1318431110] [PMID: 24218578]
[66]
Denoyer D, Masaldan S, La Fontaine S, Cater MA. Targeting copper in cancer therapy: ‘Copper That Cancer’. Metallomics 2015; 7(11): 1459-76.
[http://dx.doi.org/10.1039/C5MT00149H] [PMID: 26313539]
[67]
Choi SA, Choi JW, Wang KC, et al. Disulfiram modulates stemness and metabolism of brain tumor initiating cells in atypical teratoid/rhabdoid tumors. Neuro-oncol 2015; 17(6): 810-21.
[http://dx.doi.org/10.1093/neuonc/nou305] [PMID: 25378634]
[68]
Cong J, Wang Y, Zhang X, et al. A novel chemoradiation targeting stem and nonstem pancreatic cancer cells by repurposing disulfiram. Cancer Lett 2017; 409: 9-19.
[http://dx.doi.org/10.1016/j.canlet.2017.08.028] [PMID: 28864067]
[69]
Huang J, Campian JL, Gujar AD, et al. Final results of a phase I dose-escalation, dose-expansion study of adding disulfiram with or without copper to adjuvant temozolomide for newly diagnosed glioblastoma. J Neurooncol 2018; 138(1): 105-11.
[http://dx.doi.org/10.1007/s11060-018-2775-y] [PMID: 29374809]
[70]
Johansson B. A review of the pharmacokinetics and pharmacodynamics of disulfiram and its metabolites. Acta Psychiatr Scand Suppl 1992; 369(S369): 15-26.
[http://dx.doi.org/10.1111/j.1600-0447.1992.tb03310.x] [PMID: 1471547]
[71]
Shergill M, Patel M, Khan S, Bashir A, McConville C. Development and characterisation of sustained release solid dispersion oral tablets containing the poorly water soluble drug disulfiram. Int J Pharm 2016; 497(1-2): 3-11.
[http://dx.doi.org/10.1016/j.ijpharm.2015.11.029] [PMID: 26608620]
[72]
Makadia HK, Siegel SJ. Poly lactic-co-glycolic acid (PLGA) as biodegradable controlled drug delivery carrier. Polymers (Basel) 2011; 3(3): 1377-97.
[http://dx.doi.org/10.3390/polym3031377] [PMID: 22577513]
[73]
Wang Z, Tan J, McConville C, et al. Poly lactic-co-glycolic acid controlled delivery of disulfiram to target liver cancer stem-like cells. Nanomedicine 2017; 13(2): 641-57.
[http://dx.doi.org/10.1016/j.nano.2016.08.001] [PMID: 27521693]
[74]
Wang C, Yang J, Han H, et al. Disulfiram-loaded porous PLGA microparticle for inhibiting the proliferation and migration of non-small-cell lung cancer. Int J Nanomedicine 2017; 12: 827-37.
[http://dx.doi.org/10.2147/IJN.S121948] [PMID: 28182125]
[75]
Song W, Tang Z, Lei T, et al. Stable loading and delivery of disulfiram with mPEG-PLGA/PCL mixed nanoparticles for tumor therapy. Nanomedicine 2016; 12(2): 377-86.
[http://dx.doi.org/10.1016/j.nano.2015.10.022] [PMID: 26711966]
[76]
Chen W, Yang W, Chen P, Huang Y, Li F. Disulfiram copper nanoparticles prepared with a stabilized metal ion ligand complex method for treating drug-resistant prostate cancers. ACS Appl Mater Interfaces 2018; 10(48): 41118-28.
[http://dx.doi.org/10.1021/acsami.8b14940] [PMID: 30444340]
[77]
Zhou L, Yang L, Yang C, et al. Membrane loaded copper oleate PEGylated liposome combined with disulfiram for improving synergistic antitumor effect in vivo. Pharm Res 2018; 35(7): 147.
[http://dx.doi.org/10.1007/s11095-018-2414-5] [PMID: 29796711]
[78]
Liu P, Wang Z, Brown S, et al. Liposome encapsulated Disulfiram inhibits NFκB pathway and targets breast cancer stem cells in vitro and in vivo. Oncotarget 2014; 5(17): 7471-85.
[http://dx.doi.org/10.18632/oncotarget.2166] [PMID: 25277186]
[79]
Najlah M, Ahmed Z, Iqbal M, et al. Development and characterisation of disulfiram-loaded PLGA nanoparticles for the treatment of non-small cell lung cancer. Eur J Pharm Biopharm 2017; 112: 224-33.
[http://dx.doi.org/10.1016/j.ejpb.2016.11.032] [PMID: 27915005]
[80]
Madala HR, Punganuru SR, Ali-Osman F, Zhang R, Srivenugopal KS. Brain- and brain tumor-penetrating disulfiram nanoparticles: Sequence of cytotoxic events and efficacy in human glioma cell lines and intracranial xenografts. Oncotarget 2017; 9(3): 3459-82.
[PMID: 29423059]
[81]
Agarwal R, Iezhitsa I, Agarwal P, et al. Liposomes in topical ophthalmic drug delivery: an update. Drug Deliv 2016; 23(4): 1075-91.
[PMID: 25116511]
[82]
Lee JH, Lee JE, Kahng JY, et al. Human glioblastoma arises from subventricular zone cells with low-level driver mutations. Nature 2018; 560(7717): 243-7.
[http://dx.doi.org/10.1038/s41586-018-0389-3] [PMID: 30069053]
[83]
Newton HB. Overview of the molecular genetics and molecular chemotherapy of GBM. Glioblastoma 2010; pp. 1-42.
[http://dx.doi.org/10.1007/978-1-4419-0410-2_1]
[84]
Rasper M, Schäfer A, Piontek G, et al. Aldehyde dehydrogenase 1 positive glioblastoma cells show brain tumor stem cell capacity. Neuro-oncol 2010; 12(10): 1024-33.
[http://dx.doi.org/10.1093/neuonc/noq070] [PMID: 20627895]
[85]
Gaba SJ, Préfaut C. Comparison of pulmonary and systemic effects of adenosine triphosphate in chronic obstructive pulmonary disease--ATP: a pulmonary controlled vasoregulator? Eur Respir J 1990; 3(4): 450-5.
[PMID: 2365039]
[86]
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(3): 692-702.
[http://dx.doi.org/10.1093/carcin/bgt366] [PMID: 24193513]
[87]
Triscott J, Rose Pambid M, Dunn SE. Concise review: bullseye: targeting cancer stem cells to improve the treatment of gliomas by repurposing disulfiram. Stem Cells 2015; 33(4): 1042-6.
[http://dx.doi.org/10.1002/stem.1956] [PMID: 25588723]
[88]
Sharifzad F, Ghavami S, Verdi J, et al. Glioblastoma cancer stem cell biology: potential theranostic targets. Drug Resist Updat 2019; 42: 35-45.
[http://dx.doi.org/10.1016/j.drup.2018.03.003] [PMID: 30877905]
[89]
Triscott J, Lee C, Hu K, 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(10): 1112-23.
[http://dx.doi.org/10.18632/oncotarget.604] [PMID: 23047041]
[90]
Huang J, Campian JL, Gujar AD, et al. A phase I study to repurpose disulfiram in combination with temozolomide to treat newly diagnosed glioblastoma after chemoradiotherapy. J Neurooncol 2016; 128(2): 259-66.
[http://dx.doi.org/10.1007/s11060-016-2104-2] [PMID: 26966095]
[91]
Raso MG, Wistuba II. Molecular pathogenesis of early-stage non-small cell lung cancer and a proposal for tissue banking to facilitate identification of new biomarkers. J Thorac Oncol 2007; 2(7)(Suppl. 3): S128-35.
[http://dx.doi.org/10.1097/JTO.0b013e318074fe42] [PMID: 17603309]
[92]
Sakashita S, Sakashita M, Sound Tsao M. Genes and pathology of non-small cell lung carcinoma. Semin Oncol 2014; 41(1): 28-39.
[http://dx.doi.org/10.1053/j.seminoncol.2013.12.008] [PMID: 24565579]
[93]
Okudela K, Woo T, Mitsui H, Tajiri M, Masuda M, Ohashi K. Expression of the potential cancer stem cell markers, CD133, CD44, ALDH1, and β-catenin, in primary lung adenocarcinoma--their prognostic significance. Pathol Int 2012; 62(12): 792-801.
[http://dx.doi.org/10.1111/pin.12019] [PMID: 23252868]
[94]
Huang CP, Tsai MF, Chang TH, et al. ALDH-positive lung cancer stem cells confer resistance to epidermal growth factor receptor tyrosine kinase inhibitors. Cancer Lett 2013; 328(1): 144-51.
[http://dx.doi.org/10.1016/j.canlet.2012.08.021] [PMID: 22935675]
[95]
Nechushtan H, Hamamreh Y, Nidal S, et al. A phase IIb trial assessing the addition of disulfiram to chemotherapy for the treatment of metastatic non-small cell lung cancer. Oncologist 2015; 20(4): 366-7.
[http://dx.doi.org/10.1634/theoncologist.2014-0424] [PMID: 25777347]
[96]
Schrecengost R, Knudsen KE. Molecular pathogenesis and progression of prostate cancer. Semin Oncol 2013; 40(3): 244-58.
[http://dx.doi.org/10.1053/j.seminoncol.2013.04.001] [PMID: 23806491]
[97]
van den Hoogen C, van der Horst G, Cheung H, et al. High aldehyde dehydrogenase activity identifies tumor-initiating and metastasis-initiating cells in human prostate cancer. Cancer Res 2010; 70(12): 5163-73.
[http://dx.doi.org/10.1158/0008-5472.CAN-09-3806] [PMID: 20516116]
[98]
Januchowski R, Wojtowicz K, Zabel M. The role of aldehyde dehydrogenase (ALDH) in cancer drug resistance. Biomed Pharmacother 2013; 67(7): 669-80.
[http://dx.doi.org/10.1016/j.biopha.2013.04.005] [PMID: 23721823]
[99]
Zhou W, Yang Y, Gu Z, et al. ALDH1 activity identifies tumor-initiating cells and links to chromosomal instability signatures in multiple myeloma. Leukemia 2014; 28(5): 1155-8.
[http://dx.doi.org/10.1038/leu.2013.383] [PMID: 24365790]
[100]
Croker AK, Goodale D, Chu J, et al. High aldehyde dehydrogenase and expression of cancer stem cell markers selects for breast cancer cells with enhanced malignant and metastatic ability. J Cell Mol Med 2009; 13(8B): 2236-52.
[http://dx.doi.org/10.1111/j.1582-4934.2008.00455.x] [PMID: 18681906]
[101]
Askgaard G, Friis S, Hallas J, Thygesen LC, Pottegård A. Use of disulfiram and risk of cancer: a population-based case-control study. Eur J Cancer Prev 2014; 23(3): 225-32.
[http://dx.doi.org/10.1097/CEJ.0b013e3283647466] [PMID: 23863824]

Rights & Permissions Print Cite
Article Metrics
66
8
1
1
© 2024 Bentham Science Publishers | Privacy Policy