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Original Research

Disulfiram inhibits epithelial–mesenchymal transition through TGFβ–ERK–Snail pathway independently of Smad4 to decrease oral squamous cell carcinoma metastasis

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Pages 3887-3898 | Published online: 01 May 2019

References

  • Jemal A, Siegel R, Ward E, et al. Cancer statistics, 2008. CA Cancer J Clin. 2008;58(2):71–96.18287387
  • Warnakulasuriya S. Causes of oral cancer–an appraisal of controversies. Br Dent J. 2009;207(10):471–475. 19946320
  • Mascitti M, Rubini C, de Michele F, et al. American Joint Committee on Cancer staging system 7th edition versus 8th edition: any improvement for patients with squamous cell carcinoma of the tongue? Oral Surg Oral Med Oral Pathol Oral Radiol. 2018;126(5):415–423. 30217459
  • Rot S, Kaune T, Taubert H, et al. Prognostic impact of mRNA levels of LGR5 transcript variants in OSCC patients. BMC Cancer. 2019;19(1):155. 30770730
  • Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2018;68(6):394–424. 30207593
  • de Craene B, Berx G. Regulatory networks defining EMT during cancer initiation and progression. Nat Rev Cancer. 2013;13(2):97–110. 23344542
  • Chaw SY, Abdul Majeed A, Dalley AJ, Chan A, Stein S, Farah CS. Epithelial to mesenchymal transition (EMT) biomarkers–E-cadherin, beta-catenin, APC and Vimentin–in oral squamous cell carcinogenesis and transformation. Oral Oncol. 2012;48(10):997–1006. 22704062
  • Yang J, Weinberg RA. Epithelial-mesenchymal transition: at the crossroads of development and tumor metastasis. Dev Cell. 2008;14(6):818–829. 18539112
  • Kahata K, Dadras MS, Moustakas A. TGF-β family signaling in epithelial differentiation and epithelial-mesenchymal transition. Cold Spring Harb Perspect Biol. 2018;10(1):a022194. 28246184
  • Liu L-K, Jiang X-Y, Zhou -X-X, Wang D-M, Song X-L, Jiang H-B. Upregulation of vimentin and aberrant expression of E-cadherin/beta-catenin complex in oral squamous cell carcinomas: correlation with the clinicopathological features and patient outcome. Mod Pathol. 2010;23(2):213–224. 19915524
  • van Roy F. Beyond E-cadherin: roles of other cadherin superfamily members in cancer. Nat Rev Cancer. 2014;14(2):121–134. 24442140
  • You JS, Jones PA. Cancer genetics and epigenetics: two sides of the same coin? Cancer Cell. 2012;22(1):9–20.22789535
  • White RA, Malkoski SP, Wang X-J. TGFβ signaling in head and neck squamous cell carcinoma. Oncogene. 2010;29(40):5437–5446. 20676130
  • Kim SK, Fan Y, Papadimitrakopoulou V, et al. DPC4, a candidate tumor suppressor gene, is altered infrequently in head and neck squamous cell carcinoma. Cancer Res. 1996;56(11):2519–2521.8653689
  • Bornstein S, White R, Malkoski S, et al. Smad4 loss in mice causes spontaneous head and neck cancer with increased genomic instability and inflammation. J Clin Invest. 2009;119(11):3408–3419. 19841536
  • Deckers M, van Dinther M, Buijs J, et al. The tumor suppressor Smad4 is required for transforming growth factor beta-induced epithelial to mesenchymal transition and bone metastasis of breast cancer cells. Cancer Res. 2006;66(4):2202–2209. 16489022
  • Levy L, Hill CS. Smad4 dependency defines two classes of transforming growth factor {beta} (TGF-{beta}) target genes and distinguishes TGF-{beta}-induced epithelial-mesenchymal transition from its antiproliferative and migratory responses. Mol Cell Biol. 2005;25(18):8108–8125. 16135802
  • Kwentus J, Major LF. Disulfiram in the treatment of alcoholism; a review. J Stud Alcohol. 1979;40(5):428–446.381789
  • 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):127–134. 16880974
  • Skrott Z, Mistrik M, Andersen KK, et al. Alcohol-abuse drug disulfiram targets cancer via p97 segregase adaptor NPL4. Nature. 2017;552(7684):194–199. 29211715
  • 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):10425–10433. 17079463
  • Shian S-G, Kao Y-R, Wu FY-H, Wu C-W. Inhibition of invasion and angiogenesis by zinc-chelating agent disulfiram. Mol Pharmacol. 2003;64(5):1076–1084. 14573756
  • 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):1564–1574. 21487404
  • Loo TW, Clarke DM. Blockage of drug resistance in vitro by disulfiram, a drug used to treat alcoholism. J Natl Cancer Inst. 2000;92(11):898–902.10841824
  • Terashima Y, Toda E, Itakura M, et al. Targeting FROUNT with disulfiram regulates macrophage responses in cancer. SSRN J. 2018.
  • Cho H-J, Lee T-S, Park J-B, 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):1069–1076.18047805
  • Han D, Wu G, Chang C, et al. Disulfiram inhibits TGF-β-induced epithelial-mesenchymal transition and stem-like features in breast cancer via ERK/NF-κB/Snail pathway. Oncotarget. 2015;6(38):40907–40919. 26517513
  • Qiu W, Schönleben F, Li X, Su GH. Disruption of transforming growth factor beta-Smad signaling pathway in head and neck squamous cell carcinoma as evidenced by mutations of SMAD2 and SMAD4. Cancer Lett. 2007;245(1–2):163–170. 16478646
  • Hahn SA, Schutte M, Hoque AT, et al. DPC4, a candidate tumor suppressor gene at human chromosome 18q21.1. Science. 1996;271(5247):350–353.8553070
  • Iamaroon A, Pattamapun K, Piboonniyom S-O. Aberrant expression of Smad4, a TGF-beta signaling molecule, in oral squamous cell carcinoma. J Oral Sci. 2006;48(3):105–109.17023741
  • Wang X, Sun W, Bai J, et al. Growth inhibition induced by transforming growth factor-beta1 in human oral squamous cell carcinoma. Mol Biol Rep. 2009;36(5):861–869. 18418730
  • Amit A, Edwards CL, Athey P, Kaplan AL. Extensive subcutaneous metastases from squamous cell carcinoma of the cervix in patient with HIV. Int J Gynecol Cancer. 2001;11(1):78–80.11285038
  • Kouvaris JR, Plataniotis GA, Floros DG, Sykiotis CA, Trakadas SJ, Vlahos LJ. A benign-looking subcutaneous metastasis from squamous cell cervical carcinoma: A case report and review of the literature. Int J Gynecol Cancer. 2000;10(6):503–506.11240721
  • Hoffman GR, Hayter JP. Widespread subcutaneous distant metastases from a head and neck squamous cell carcinoma. J Oral Maxillofac Surg. 2002;60(8):954–958.12149748
  • Li Y, Wang L-H, Zhang H-T, 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):439–451. 29148232
  • Feng X-H DR. Specificity and versatility in tgf-beta signaling through Smads. Annu Rev Cell Dev Biol. 2005;21:659–693.16212511
  • Chow JYC, Quach KT, Cabrera BL, Cabral JA, Beck SE, Carethers JM. RAS/ERK modulates TGFbeta-regulated PTEN expression in human pancreatic adenocarcinoma cells. Carcinogenesis. 2007;28(11):2321–2327. 17638924
  • Iglesias M, Frontelo P, Gamallo C, Quintanilla M. Blockade of Smad4 in transformed keratinocytes containing a Ras oncogene leads to hyperactivation of the Ras-dependent Erk signalling pathway associated with progression to undifferentiated carcinomas. Oncogene. 2000;19(36):4134–4145. 10962574
  • Xie L, Law BK, Chytil AM, Brown KA, Aakre ME, Moses HL. Activation of the Erk pathway is required for TGF-beta1-induced EMT in vitro. Neoplasia. 2004;6(5):603–610. 15548370
  • Derynck R, Zhang YE. Smad-dependent and Smad-independent pathways in TGF-beta family signalling. Nature. 2003;425(6958):577–584. 14534577
  • Zhang YE. Non-Smad pathways in TGF-beta signaling. Cell Res. 2009;19(1):128–139. 19114990
  • Vincent T, Neve EPA, Johnson JR, et al. A SNAIL1-SMAD3/4 transcriptional repressor complex promotes TGF-beta mediated epithelial-mesenchymal transition. Nat Cell Biol. 2009;11(8):943–950. 19597490
  • Wang Y, Shi J, Chai K, Ying X, Zhou BP. The role of snail in EMT and tumorigenesis. Curr Cancer Drug Targets. 2013;13(9):963–972.24168186
  • Chen H, Zhu G, Li Y, et al. Extracellular signal-regulated kinase signaling pathway regulates breast cancer cell migration by maintaining slug expression. Cancer Res. 2009;69(24):9228–9235. 19920183
  • Hsu Y-L, Hou M-F, Kuo P-L, Huang Y-F, Tsai E-M. Breast tumor-associated osteoblast-derived CXCL5 increases cancer progression by ERK/MSK1/Elk-1/snail signaling pathway. Oncogene. 2013;32(37):4436–4447. 23045282
  • Roberts PJ, Der CJ. Targeting the Raf-MEK-ERK mitogen-activated protein kinase cascade for the treatment of cancer. Oncogene. 2007;26(22):3291–331017496923