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Article

Mechanism of Action of Phenethylisothiocyanate and Other Reactive Oxygen Species-Inducing Anticancer Agents

, , , , , , & show all
Pages 2382-2395 | Received 04 Dec 2013, Accepted 08 Apr 2014, Published online: 20 Mar 2023

REFERENCES

  • Lydon N. 2009. Attacking cancer at its foundation. Nat. Med. 15:1153–1157. http://dx.doi.org/10.1038/nm1009-1153.
  • Fruehauf JP, Meyskens FLJr. 2007. Reactive oxygen species: a breath of life or death? Clin. Cancer Res. 13:789–794. http://dx.doi.org/10.1158/1078-0432.CCR-06-2082.
  • Trachootham D, Alexandre J, Huang P. 2009. Targeting cancer cells by ROS-mediated mechanisms: a radical therapeutic approach? Nat. Rev. Drug Discov. 8:579–591. http://dx.doi.org/10.1038/nrd2803.
  • Engel RH, Evens AM. 2006. Oxidative stress and apoptosis: a new treatment paradigm in cancer. Front. Biosci. 11:300–312. http://dx.doi.org/10.2741/1798.
  • Schumacker PT. 2006. Reactive oxygen species in cancer cells: live by the sword, die by the sword. Cancer Cell 10:175–176. http://dx.doi.org/10.1016/j.ccr.2006.08.015.
  • Chintharlapalli S, Papineni S, Lei P, Pathi S, Safe S. 2011. Betulinic acid inhibits colon cancer cell and tumor growth and induces proteasome-dependent and -independent downregulation of specificity proteins (Sp) transcription factors. BMC Cancer 11:371. http://dx.doi.org/10.1186/1471-2407-11-371.
  • Pathi SS, Jutooru I, Chadalapaka G, Sreevalsan S, Anand S, Thatcher GR, Safe S. 2011. GT-094, a NO-NSAID, inhibits colon cancer cell growth by activation of a reactive oxygen species-microRNA-27a: ZBTB10-specificity protein pathway. Mol. Cancer Res. 9:195–202. http://dx.doi.org/10.1158/1541-7786.MCR-10-0363.
  • Jutooru I, Chadalapaka G, Abdelrahim M, Basha MR, Samudio I, Konopleva M, Andreeff M, Safe S. 2010. Methyl 2-cyano-3,12-dioxooleana-1,9-dien-28-oate decreases specificity protein transcription factors and inhibits pancreatic tumor growth: role of microRNA-27a. Mol. Pharmacol. 78:226–236. http://dx.doi.org/10.1124/mol.110.064451.
  • Chadalapaka G, Jutooru I, Safe S. 2012. Celastrol decreases specificity proteins (Sp) and fibroblast growth factor receptor-3 (FGFR3) in bladder cancer cells. Carcinogenesis 33:886–894. http://dx.doi.org/10.1093/carcin/bgs102.
  • Jutooru I, Chadalapaka G, Sreevalsan S, Lei P, Barhoumi R, Burghardt R, Safe S. 2010. Arsenic trioxide downregulates specificity protein (Sp) transcription factors and inhibits bladder cancer cell and tumor growth. Exp. Cell Res. 316:2174–2188. http://dx.doi.org/10.1016/j.yexcr.2010.04.027.
  • Jutooru I, Chadalapaka G, Lei P, Safe S. 2010. Inhibition of NFkappaB and pancreatic cancer cell and tumor growth by curcumin is dependent on specificity protein down-regulation. J. Biol. Chem. 285:25332–25344. http://dx.doi.org/10.1074/jbc.M109.095240.
  • Pathi SS, Lei P, Sreevalsan S, Chadalapaka G, Jutooru I, Safe S. 2011. Pharmacologic doses of ascorbic acid repress specificity protein (Sp) transcription factors and Sp-regulated genes in colon cancer cells. Nutr. Cancer 63:1133–1142. http://dx.doi.org/10.1080/01635581.2011.605984.
  • Murillo G, Mehta RG. 2001. Cruciferous vegetables and cancer prevention. Nutr. Cancer 41:17–28. http://dx.doi.org/10.1080/01635581.2001.9680607.
  • Cohen JH, Kristal AR, Stanford JL. 2000. Fruit and vegetable intakes and prostate cancer risk. J. Natl. Cancer Inst. 92:61–68. http://dx.doi.org/10.1093/jnci/92.1.61.
  • Sahu RP, Srivastava SK. 2009. The role of STAT-3 in the induction of apoptosis in pancreatic cancer cells by benzyl isothiocyanate. J. Natl. Cancer Inst. 101:176–193. http://dx.doi.org/10.1093/jnci/djn470.
  • Xu C, Shen G, Chen C, Gelinas C, Kong AN. 2005. Suppression of NF-kappaB and NF-kappaB-regulated gene expression by sulforaphane and PEITC through IkappaBalpha, IKK pathway in human prostate cancer PC-3 cells. Oncogene 24:4486–4495. http://dx.doi.org/10.1038/sj.onc.1208656.
  • Kallifatidis G, Rausch V, Baumann B, Apel A, Beckermann BM, Groth A, Mattern J, Li Z, Kolb A, Moldenhauer G, Altevogt P, Wirth T, Werner J, Schemmer P, Buchler MW, Salnikov AV, Herr I. 2009. Sulforaphane targets pancreatic tumour-initiating cells by NF-kappaB-induced antiapoptotic signalling. Gut 58:949–963. http://dx.doi.org/10.1136/gut.2008.149039.
  • Kim JH, Xu C, Keum YS, Reddy B, Conney A, Kong AN. 2006. Inhibition of EGFR signaling in human prostate cancer PC-3 cells by combination treatment with beta-phenylethyl isothiocyanate and curcumin. Carcinogenesis 27:475–482. http://dx.doi.org/10.1093/carcin/bgi272.
  • Yang MD, Lai KC, Lai TY, Hsu SC, Kuo CL, Yu CS, Lin ML, Yang JS, Kuo HM, Wu SH, Chung JG. 2010. Phenethyl isothiocyanate inhibits migration and invasion of human gastric cancer AGS cells through suppressing MAPK and NF-kappaB signal pathways. Anticancer Res. 30:2135–2143.
  • Lai KC, Huang AC, Hsu SC, Kuo CL, Yang JS, Wu SH, Chung JG. 2010. Benzyl isothiocyanate (BITC) inhibits migration and invasion of human colon cancer HT29 cells by inhibiting matrix metalloproteinase-2/-9 and urokinase plasminogen (uPA) through PKC and MAPK signaling pathway. J. Agric. Food Chem. 58:2935–2942. http://dx.doi.org/10.1021/jf9036694.
  • Srivastava SK, Xiao D, Lew KL, Hershberger P, Kokkinakis DM, Johnson CS, Trump DL, Singh SV. 2003. Allyl isothiocyanate, a constituent of cruciferous vegetables, inhibits growth of PC-3 human prostate cancer xenografts in vivo. Carcinogenesis 24:1665–1670. http://dx.doi.org/10.1093/carcin/bgg123.
  • Xiao D, Vogel V, Singh SV. 2006. Benzyl isothiocyanate-induced apoptosis in human breast cancer cells is initiated by reactive oxygen species and regulated by Bax and Bak. Mol. Cancer Ther. 5:2931–2945. http://dx.doi.org/10.1158/1535-7163.MCT-06-0396.
  • Kim SH, Nagalingam A, Saxena NK, Singh SV, Sharma D. 2011. Benzyl isothiocyanate inhibits oncogenic actions of leptin in human breast cancer cells by suppressing activation of signal transducer and activator of transcription 3. Carcinogenesis 32:359–367. http://dx.doi.org/10.1093/carcin/bgq267.
  • Chadalapaka G, Jutooru I, Burghardt R, Safe S. 2010. Drugs that target specificity proteins downregulate epidermal growth factor receptor in bladder cancer cells. Mol. Cancer Res. 8:739–750. http://dx.doi.org/10.1158/1541-7786.MCR-09-0493.
  • Trachootham D, Zhou Y, Zhang H, Demizu Y, Chen Z, Pelicano H, Chiao PJ, Achanta G, Arlinghaus RB, Liu J, Huang P. 2006. Selective killing of oncogenically transformed cells through a ROS-mediated mechanism by beta-phenylethyl isothiocyanate. Cancer Cell 10:241–252. http://dx.doi.org/10.1016/j.ccr.2006.08.009.
  • Xiao D, Powolny AA, Moura MB, Kelley EE, Bommareddy A, Kim SH, Hahm ER, Normolle D, Van Houten B, Singh SV. 2010. Phenethyl isothiocyanate inhibits oxidative phosphorylation to trigger reactive oxygen species-mediated death of human prostate cancer cells. J. Biol. Chem. 285:26558–26569. http://dx.doi.org/10.1074/jbc.M109.063255.
  • Powolny AA, Singh SV. 2010. Differential response of normal (PrEC) and cancerous human prostate cells (PC-3) to phenethyl isothiocyanate-mediated changes in expression of antioxidant defense genes. Pharm. Res. 27:2766–2775. http://dx.doi.org/10.1007/s11095-010-0278-4.
  • Sahu RP, Zhang R, Batra S, Shi Y, Srivastava SK. 2009. Benzyl isothiocyanate-mediated generation of reactive oxygen species causes cell cycle arrest and induces apoptosis via activation of MAPK in human pancreatic cancer cells. Carcinogenesis 30:1744–1753. http://dx.doi.org/10.1093/carcin/bgp157.
  • Tang L, Zhang Y. 2005. Mitochondria are the primary target in isothiocyanate-induced apoptosis in human bladder cancer cells. Mol. Cancer Ther. 4:1250–1259. http://dx.doi.org/10.1158/1535-7163.MCT-05-0041.
  • Mertens-Talcott SU, Chintharlapalli S, Li X, Safe S. 2007. The oncogenic microRNA-27a targets genes that regulate specificity protein transcription factors and the G2-M checkpoint in MDA-MB-231 breast cancer cells. Cancer Res. 67:11001–11011. http://dx.doi.org/10.1158/0008-5472.CAN-07-2416.
  • Kim K, Chadalapaka G, Lee SO, Yamada D, Sastre-Garau X, Defossez PA, Park YY, Lee JS, Safe S. 2012. Identification of oncogenic microRNA-17–92/ZBTB4/specificity protein axis in breast cancer. Oncogene 31:1034–1044. http://dx.doi.org/10.1038/onc.2011.296.
  • Kim K, Jutooru I, Chadalapaka G, Johnson G, Frank J, Burghardt R, Kim S, Safe S. 2013. HOTAIR is a negative prognostic factor and exhibits pro-oncogenic activity in pancreatic cancer. Oncogene 32:1616–1625. http://dx.doi.org/10.1038/onc.2012.193.
  • Raj L, Ide T, Gurkar AU, Foley M, Schenone M, Li X, Tolliday NJ, Golub TR, Carr SA, Shamji AF, Stern AM, Mandinova A, Schreiber SL, Lee SW. 2011. Selective killing of cancer cells by a small molecule targeting the stress response to ROS. Nature 475:231–234. http://dx.doi.org/10.1038/nature10167.
  • O'Hagan HM, Wang W, Sen S, Destefano Shields C, Lee SS, Zhang YW, Clements EG, Cai Y, Van Neste L, Easwaran H, Casero RA, Sears CL, Baylin SB. 2011. Oxidative damage targets complexes containing DNA methyltransferases, SIRT1, and polycomb members to promoter CpG Islands. Cancer Cell 20:606–619. http://dx.doi.org/10.1016/j.ccr.2011.09.012.
  • Lee Y, Kim M, Han J, Yeom KH, Lee S, Baek SH, Kim VN. 2004. MicroRNA genes are transcribed by RNA polymerase II. EMBO J. 23:4051–4060. http://dx.doi.org/10.1038/sj.emboj.7600385.
  • Woods K, Thomson JM, Hammond SM. 2007. Direct regulation of an oncogenic micro-RNA cluster by E2F transcription factors. J. Biol. Chem. 282:2130–2134. http://dx.doi.org/10.1074/jbc.C600252200.
  • van Haaften G, Agami R. 2010. Tumorigenicity of the miR-17-92 cluster distilled. Genes Dev. 24:1–4. http://dx.doi.org/10.1101/gad.1887110.
  • Nicolas M, Noe V, Jensen KB, Ciudad CJ. 2001. Cloning and characterization of the 5′-flanking region of the human transcription factor Sp1 gene. J. Biol. Chem. 276:22126–22132. http://dx.doi.org/10.1074/jbc.M010740200.
  • Wang L, Wei D, Huang S, Peng Z, Le X, Wu TT, Yao J, Ajani J, Xie K. 2003. Transcription factor Sp1 expression is a significant predictor of survival in human gastric cancer. Clin. Cancer Res. 9:6371–6380.
  • Yao JC, Wang L, Wei D, Gong W, Hassan M, Wu TT, Mansfield P, Ajani J, Xie K. 2004. Association between expression of transcription factor Sp1 and increased vascular endothelial growth factor expression, advanced stage, and poor survival in patients with resected gastric cancer. Clin. Cancer Res. 10:4109–4117. http://dx.doi.org/10.1158/1078-0432.CCR-03-0628.
  • Jiang NY, Woda BA, Banner BF, Whalen GF, Dresser KA, Lu D. 2008. Sp1, a new biomarker that identifies a subset of aggressive pancreatic ductal adenocarcinoma. Cancer Epidemiol. Biomarkers Prev. 17:1648–1652. http://dx.doi.org/10.1158/1055-9965.EPI-07-2791.
  • Lou Z, O'Reilly S, Liang H, Maher VM, Sleight SD, McCormick JJ. 2005. Down-regulation of overexpressed sp1 protein in human fibrosarcoma cell lines inhibits tumor formation. Cancer Res. 65:1007–1017.
  • Zannetti A, Del Vecchio S, Carriero MV, Fonti R, Franco P, Botti G, D'Aiuto G, Stoppelli MP, Salvatore M. 2000. Coordinate up-regulation of Sp1 DNA-binding activity and urokinase receptor expression in breast carcinoma. Cancer Res. 60:1546–1551.
  • Chiefari E, Brunetti A, Arturi F, Bidart JM, Russo D, Schlumberger M, Filetti S. 2002. Increased expression of AP2 and Sp1 transcription factors in human thyroid tumors: a role in NIS expression regulation? BMC Cancer 2:35. http://dx.doi.org/10.1186/1471-2407-2-35.
  • Hosoi Y, Watanabe T, Nakagawa K, Matsumoto Y, Enomoto A, Morita A, Nagawa H, Suzuki N. 2004. Up-regulation of DNA-dependent protein kinase activity and Sp1 in colorectal cancer. Int. J. Oncol. 25:461–468. http://dx.doi.org/10.3892/ijo.25.2.461.
  • Chadalapaka G, Jutooru I, Chintharlapalli S, Papineni S, Smith RIII, Li X, Safe S. 2008. Curcumin decreases specificity protein expression in bladder cancer cells. Cancer Res. 68:5345–5354. http://dx.doi.org/10.1158/0008-5472.CAN-07-6805.
  • Noratto GD, Jutooru I, Safe S, Angel-Morales G, Mertens-Talcott SU. 2013. The drug resistance suppression induced by curcuminoids in colon cancer SW-480 cells is mediated by reactive oxygen species-induced disruption of the microRNA-27a-ZBTB10-Sp axis. Mol. Nutr. Food Res. 57:1638–1648. http://dx.doi.org/10.1002/mnfr.201200609.

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