Synthesis and biological evaluation of dithiocarbamate esters of parthenolide as potential anti-acute myelogenous leukaemia agents

References

• Guzman ML, Rossi RM, Karnischky L, et al. The sesquiterpene lactone parthenolide induces apoptosis of human acute myelogenous leukemia stem and progenitor cells. Blood 2005;105:4163–9.
   PubMed Web of Science ®Google Scholar
• Siveen KS, Uddin S, Mohammad RM. Targeting acute myeloid leukemia stem cell signaling by natural products. Mol Cancer 2017;16:13.
   PubMed Web of Science ®Google Scholar
• Sarkozy C, Gardin C, Gachard N, et al. Outcome of older patients with acute myeloid leukemia in first relapse. Am J Hematol 2013;88:758–64.
   PubMed Web of Science ®Google Scholar
• Lapidot T, Sirard C, Vormoor J, et al. A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature 1994;367:645–8.
   PubMed Web of Science ®Google Scholar
• Sarry J-E, Murphy K, Perry R, et al. Human acute myelogenous leukemia stem cells are rare and heterogeneous when assayed in NOD/SCID/IL2R gamma c-deficient mice. J Clin Invest 2011;121:384–95.
   PubMed Web of Science ®Google Scholar
• Stiehl T, Baran N, Ho AD, Marciniak-Czochra A. Cell division patterns in acute myeloid leukemia stem-like cells determine clinical course: a model to predict patient survival. Cancer Res 2015;75:940–9.
   PubMed Web of Science ®Google Scholar
• Ho T-C, LaMere M, Stevens BM, et al. Evolution of acute myelogenous leukemia stem cell properties following treatment and progression. Blood 2016;128:1671–8.
   PubMed Web of Science ®Google Scholar
• Shlush LI, Mitchell A, Heisler L, et al. Tracing the origins of relapse in acute myeloid leukaemia to stem cells. Nature 2017;547:104–8.
   PubMed Web of Science ®Google Scholar
• Thomas D, Majeti R. Biology and relevance of human acute myeloid leukemia stem cells. Blood 2017;129:1577–85.
   PubMed Web of Science ®Google Scholar
• Eppert K, Takenaka K, Lechman ER, et al. Stem cell gene expression programs influence clinical outcome in human leukemia. Nat Med 2011;17:1086–91.
   PubMed Web of Science ®Google Scholar
• Chan WI, Huntly BJ. Leukemia stem cells in acute myeloid leukemia. Semin Oncol 2008;35:326–35.
   PubMed Web of Science ®Google Scholar
• Jin L, Hope KJ, Zhai Q, et al. Targeting of CD44 eradicates human acute myeloid leukemia stem cells. Nat Med 2006;12:1167–74.
   PubMed Web of Science ®Google Scholar
• Guzman ML, Rossi RM, Neelakantan S, et al. An orally bioavailable parthenolide analog selectively eradicates acute myelogenous leukemia stem and progenitor cells. Blood 2007;110:4427–35.
   PubMed Web of Science ®Google Scholar
• Zhou J, Zhang H, Gu P, et al. NF-kappa B pathway inhibitors preferentially inhibit breast cancer stem-like cells. Breast Cancer Res Treat 2008;111:419–27.
   PubMed Web of Science ®Google Scholar
• Huynh DT, Iannotti MJ, Gunn EJ, et al. Parthenolide and structurally related natural products as anti-cancer stem cell agents: a new era in treatment of multiple myeloma. Cancer Res 2010;70:4292.
   PubMed Web of Science ®Google Scholar
• Kawasaki BT, Hurt EM, Kalathur M, et al. Effects of the sesquiterpene lactone parthenolide on prostate tumor-initiating cells: an integrated molecular profiling approach. Prostate 2009;69:827–37.
   PubMed Web of Science ®Google Scholar
• Ghantous A, Sinjab A, Herceg Z, Darwiche N. Parthenolide: from plant shoots to cancer roots. Drug Discov Today 2013;18:894–905.
   PubMed Web of Science ®Google Scholar
• Dell'Agli M, Galli GV, Bosisio E, D'Ambrosio M. Inhibition of NF-kB and metalloproteinase-9 expression and secretion by parthenolide derivatives. Bioorg Med Chem Lett 2009;19:1858–60.
   PubMed Web of Science ®Google Scholar
• Gopal YV, Arora TS, Van Dyke MW. Parthenolide specifically depletes histone deacetylase 1 protein and induces cell death through ataxia telangiectasia mutated. Chem Biol 2007;14:813–23.
   PubMed Web of Science ®Google Scholar
• Kim YJ, Choi M-H, Hong S-T, Bae YM. Resistance of cholangiocarcinoma cells to parthenolide-induced apoptosis by the excretory-secretory products of Clonorchis sinensis. Parasitol Res 2009;104:1011–6.
   PubMed Web of Science ®Google Scholar
• Riganti C, Doublier S, Viarisio D, et al. Artemisinin induces doxorubicin resistance in human colon cancer cells via calcium-dependent activation of HIF-1 alpha and P-glycoprotein overexpression. Br J Pharmacol 2009;156:1054–66.
   PubMed Web of Science ®Google Scholar
• Hassane DC, Guzman ML, Corbett C, et al. Discovery of agents that eradicate leukemia stem cells using an in silico screen of public gene expression data. Blood 2008;111:5654–62.
   PubMed Web of Science ®Google Scholar
• Kim YR, Eom JI, Kim SJ, et al. Myeloperoxidase expression as a potential determinant of parthenolide-induced apoptosis in leukemia bulk and leukemia stem cells. J Pharmacol Exp Ther 2010;335:389–400.
   PubMed Web of Science ®Google Scholar
• Nasim S, Crooks PA. Antileukemic activity of aminoparthenolide analogs. Bioorg Med Chem Lett 2008;18:3870–3.
   PubMed Web of Science ®Google Scholar
• Nakshatri H, Appaiah HN, Anjanappa M, et al. NF-kappa B-dependent and -independent epigenetic modulation using the novel anti-cancer agent DMAPT. Cell Death Dis 2015;6:e1608.
   PubMed Web of Science ®Google Scholar
• Neelakantan S, Nasim S, Guzman ML, et al. Aminoparthenolides as novel anti-leukemic agents: discovery of the NF-kappaB inhibitor, DMAPT (LC-1). Bioorg Med Chem Lett 2009;19:4346–9.
   PubMed Web of Science ®Google Scholar
• Peese K. New agents for the treatment of leukemia: discovery of DMAPT (LC-1). Drug Discov Today 2010;15:322.
   Web of Science ®Google Scholar
• Lickliter J. A phase 1 dose-escalation study to evaluate the safety, tolerability and pharmacokinetics of ACT001 in patients with advanced solid tumors. Availabel from: https://www.anzctr.org.au/Trial/Registration/TrialReview.aspx?ACTRN=12616000228482p.
   Google Scholar
• Carta F, Aggarwal M, Maresca A, et al. Dithiocarbamates strongly inhibit carbonic anhydrases and show antiglaucoma action in vivo. J Med Chem 2012;55:1721–30.
   PubMed Web of Science ®Google Scholar
• Carta F, Aggarwal M, Maresca A, et al. Dithiocarbamates: a new class of carbonic anhydrase inhibitors. Crystallographic and kinetic investigations. Chem Commun 2012;48:1868–70.
   PubMed Web of Science ®Google Scholar
• Imamura H, Ohtake N, Jona H, et al. Dicationic dithiocarbamate carbapenems with anti-MRSA activity. Bioorg Med Chem 2001;9:1571–8.
   PubMed Web of Science ®Google Scholar
• Len C, Boulogne-Merlot A-S, Postel D, et al. Synthesis and antifungal activity of novel bis(dithiocarbamate) derivatives of glycerol. J Agric Food Chem 1996;44:2856–8.
   Web of Science ®Google Scholar
• Dehmel F, Weinbrenner S, Julius H, et al. Trithiocarbonates as a novel class of HDAC inhibitors: SAR studies, isoenzyme selectivity, and pharmacological profiles. J Med Chem 2008;51:3985–4001.
   PubMed Web of Science ®Google Scholar
• Ding PP, Gao M, Mao BB, et al. Synthesis and biological evaluation of quinazolin-4(3H)-one derivatives bearing dithiocarbamate side chain at C2-position as potential antitumor agents. Eur J Med Chem 2016;108:364–73.
   PubMed Web of Science ®Google Scholar
• Li B, Zhou S, Wang S, et al. Efficient synthesis of organic sulfonic acid derivatives containing dithiocarbamate side chains. Tetrahedron 2016;72:3885–9.
   Web of Science ®Google Scholar
• Li R-D, Wang H-L, Li Y-B, et al. Discovery and optimization of novel dual dithiocarbamates as potent anticancer agents. Eur J Med Chem 2015;93:381–91.
   PubMed Web of Science ®Google Scholar
• Qian Y, Ma G-Y, Yang Y, et al. Synthesis, molecular modeling and biological evaluation of dithiocarbamates as novel antitubulin agents. Bioorg Med Chem 2010;18:4310–6.
   PubMed Web of Science ®Google Scholar
• Zahran MAH, Salem TAR, Samaka RM, et al. Design, synthesis and antitumor evaluation of novel thalidomide dithiocarbamate and dithioate analogs against Ehrlich ascites carcinoma-induced solid tumor in Swiss albino mice. Bioorg Med Chem 2008;16:9708–18.
   PubMed Web of Science ®Google Scholar
• Zhang Y, Liu B, Wu X, et al. New pyridin-3-ylmethyl carbamodithioic esters activate pyruvate kinase M2 and potential anticancer lead compounds. Bioorg Med Chem 2015;23:4815–23.
   PubMed Web of Science ®Google Scholar
• Johansson B. A review of the pharmacokinetics and pharmacodynamics of disulfiram and its metabolites. Acta Psychiatr Scand Suppl 1992;369:15–26.
   PubMedGoogle Scholar
• Guo X, Xu B, Pandey S, et al. Disulfiram/copper complex inhibiting NF kappa B activity and potentiating cytotoxic effect of gemcitabine on colon and breast cancer cell lines. Cancer Lett 2010;290:104–13.
   PubMed Web of Science ®Google Scholar
• Jivan R, Damelin LH, Birkhead M, et al. Disulfiram/copper-disulfiram damages multiple protein degradation and turnover pathways and cytotoxicity is enhanced by metformin in oesophageal squamous cell carcinoma cell lines. J Cell Biochem 2015;116:2334–43.
   PubMed Web of Science ®Google Scholar
• 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;66:10425–33.
   PubMed Web of Science ®Google Scholar
• Dastjerdi MN, Babazadeh Z, Salehi M, et al. Comparison of the anti-cancer effect of disulfiram and 5-Aza-CdR on pancreatic cancer cell line PANC-1. Adv Biomed Res 2014;3:156.
   PubMedGoogle Scholar
• Lin J, Haffner MC, Zhang Y, et al. Disulfiram is a DNA demethylating agent and inhibits prostate cancer cell growth. Prostate 2011;71:333–43.
   PubMed Web of Science ®Google Scholar
• Liu P, Kumar IS, Brown S, et al. Disulfiram targets cancer stem-like cells and reverses resistance and cross-resistance in acquired paclitaxel-resistant triple-negative breast cancer cells. Br J Cancer 2013;109:1876–85.
   PubMed Web of Science ®Google Scholar
• 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;107:1488–97.
   PubMed Web of Science ®Google Scholar
• 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;104:1564–74.
   PubMed Web of Science ®Google Scholar
• Clinical trials. Gov identifier NCT 01777919.
   Google Scholar
• Shehzad A, Lee J, Lee YS. Autocrine prostaglandin E2 signaling promotes promonocytic leukemia cell survival via COX-2 expression and MAPK pathway. BMB Rep 2015;48:109–14.
   PubMed Web of Science ®Google Scholar
• Konig H, Copland M, Chu S, et al. Effects of dasatinib on Src kinase activity and downstream intracellular signaling in primitive chronic myelogenous leukemia hematopoietic cells. Cancer Res 2008;68:9624–33.
   PubMed Web of Science ®Google Scholar
• Balko JM, Schwarz LJ, Bhola NE, et al. Activation of MAPK pathways due to DUSP4 loss promotes cancer stem cell-like phenotypes in basal-like breast cancer. Cancer Res 2013;73:6346–58.
   PubMed Web of Science ®Google Scholar
• Piao LS, Hur W, Kim T-K, et al. CD133+ liver cancer stem cells modulate radioresistance in human hepatocellular carcinoma. Cancer Lett 2012;315:129–37.
   PubMed Web of Science ®Google Scholar
• Mulholland DJ, Kobayashi N, Ruscetti M, et al. Pten Loss and RAS/MAPK activation cooperate to promote EMT and metastasis initiated from prostate cancer stem/progenitor cells. Cancer Res 2012;72:1878–89.
   PubMed Web of Science ®Google Scholar
• Wang YK, Zhu YL, Qiu FM, et al. Activation of Akt and MAPK pathways enhances the tumorigenicity of CD133+primary colon cancer cells. Carcinogenesis 2010;31:1376–80.
   PubMed Web of Science ®Google Scholar
• Karsy M, Albert L, Tobias ME, et al. All-trans retinoic acid modulates cancer stem cells of glioblastoma multiforme in an MAPK-dependent manner. Anticancer Res 2010;30:4915–20.
   PubMed Web of Science ®Google Scholar
• Kumar D, Kumar S, Gorain M, et al. Notch1-MAPK signaling axis regulates CD133+ cancer stem cell-mediated melanoma growth and angiogenesis. J Invest Dermatol 2016;136:2462–74.
   PubMed Web of Science ®Google Scholar
• Ishimoto T, Nagano O, Yae T, et al. CD44 variant regulates redox status in cancer cells by stabilizing the xCT subunit of system xc(-) and thereby promotes tumor growth. Cancer Cell 2011;19:387–400.
   PubMed Web of Science ®Google Scholar
• Bharti R, Dey G, Mandal M. Cancer development, chemoresistance, epithelial to mesenchymal transition and stem cells: a snapshot of IL-6 mediated involvement. Cancer Lett 2016;375:51–61.
   PubMed Web of Science ®Google Scholar
• Dreesen O, Brivanlou AH. Signaling pathways in cancer and embryonic stem cells. Stem Cell Rev 2007;3:7–17.
   PubMed Web of Science ®Google Scholar
• Long J, Ding Y-H, Wang P-P, et al. Protection-group-free semisyntheses of parthenolide and its cyclopropyl analogue. J Org Chem 2013;78:10512–8.
   PubMed Web of Science ®Google Scholar
• Long J, Zhang S-F, Wang P-P, et al. Total syntheses of parthenolide and its analogues with macrocyclic stereocontrol. J Med Chem 2014;57:7098–112.
   PubMed Web of Science ®Google Scholar
• Yang Z, Kuang B, Kang N, et al. Synthesis and anti-acute myeloid leukemia activity of C-14 modified parthenolide derivatives. Eur J Med Chem 2017;127:296–304.
   PubMed Web of Science ®Google Scholar
• Yang Z-J, Ge W-Z, Li Q-Y, et al. Syntheses and biological evaluation of costunolide, parthenolide, and their fluorinated analogues. J Med Chem 2015;58:7007–20.
   PubMed Web of Science ®Google Scholar
• Zhang Q, Lu Y, Ding Y, et al. Guaianolide sesquiterpene lactones, a source to discover agents that selectively inhibit acute myelogenous leukemia stem and progenitor cells. J Med Chem 2012;55:8757–69.
   PubMed Web of Science ®Google Scholar
• Fuchs D, Daniel V, Sadeghi M, et al. Salinomycin overcomes ABC transporter-mediated multidrug and apoptosis resistance in human leukemia stem cell-like KG-1a cells. Biochem Biophys Res Commun 2010;394:1098–104.
   PubMed Web of Science ®Google Scholar
• Liu Y, Chen F, Wang S, et al. Low-dose triptolide in combination with idarubicin induces apoptosis in AML leukemic stem-like KG1a cell line by modulation of the intrinsic and extrinsic factors. Cell Death Dis 2013;4:e948
   PubMed Web of Science ®Google Scholar
• Weng G, Zeng Y, Huang J, et al. Curcumin enhanced busulfan-induced apoptosis through downregulating the expression of survivin in leukemia stem-like KG1a cells. Biomed Res Int 2015;2015:1.
   Web of Science ®Google Scholar