Anticancer activities of a benzimidazole compound through sirtuin inhibition in colorectal cancer

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References

• 1 Arnold M, Sierra MS, Laversanne M, Soerjomataram I, Jemal A, Bray F. Global patterns and trends in colorectal cancer incidence and mortality. Gut 66(4), 683–691 (2016).
  MedlineGoogle Scholar
• 2 Ferlay J, Shin HR, Bray F, Forman D, Mathers C, Parkin DM. Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int. J. Cancer 127(12), 2893–2917 (2010).
  Medline CASGoogle Scholar
• 3 Siegel RL, Miller KD, Fedewa SA et al. Colorectal cancer statistics, 2017. CA Cancer J. Clin. 67(3), 177–193 (2017).
  MedlineGoogle Scholar
• 4 Longley D, Johnston P. Molecular mechanisms of drug resistance. J. Pathol. 205(2), 275–292 (2005).
  Medline CASGoogle Scholar
• 5 Aidan JC, Priddee NR, McAleer JJ. Chemotherapy causes cancer! A case report of therapy related acute myeloid leukaemia in early stage breast cancer. Ulster Med. J. 82(2), 97–99 (2013).
  MedlineGoogle Scholar
• 6 Dizon DS, Krilov L, Cohen E et al. Clinical cancer advances 2016: annual report on progress against cancer from the American Society of Clinical Oncology. J. Clin. Oncol. 34(9), 987–1011 (2016).
  Medline CASGoogle Scholar
• 7 Gish RG, Finn RS, Marrero JA. Extending survival with the use of targeted therapy in the treatment of hepatocellular carcinoma. Gastroenterol. Hepatol. (NY) 9(4 Suppl. 2), 1–24 (2013).
  MedlineGoogle Scholar
• 8 Keng Yoon Y, Ein Oon C. Sirtuin inhibitors: an overview from medicinal chemistry perspective. Anticancer Agents Med. Chem. 16(8), 1003–1016 (2016).
  MedlineGoogle Scholar
• 9 Bradbury C, Khanim F, Hayden R et al. Histone deacetylases in acute myeloid leukaemia show a distinctive pattern of expression that changes selectively in response to deacetylase inhibitors. Leukemia 19(10), 1751–1759 (2005).
  Medline CASGoogle Scholar
• 10 Huffman DM, Grizzle WE, Bamman MM et al. SIRT1 is significantly elevated in mouse and human prostate cancer. Cancer Res. 67(14), 6612–6618 (2007).
  Medline CASGoogle Scholar
• 11 Stünkel W, Peh BK, Tan YC et al. Function of the SIRT1 protein deacetylase in cancer. Biotechnol. J. 2(11), 1360–1368 (2007).
  Medline CASGoogle Scholar
• 12 Schmidt MT, Smith BC, Jackson MD, Denu JM. Coenzyme specificity of Sir2 protein deacetylases implications for physiological regulation. J. Biol. Chem. 279(38), 40122–40129 (2004).
  Medline CASGoogle Scholar
• 13 Freitag M, Schemies J, Larsen T et al. Synthesis and biological activity of splitomicin analogs targeted at human NAD+-dependent histone deacetylases (sirtuins). Bioorg. Med. Chem. 19(12), 3669–3677 (2011).
  Medline CASGoogle Scholar
• 14 Oon CE, Strell C, Yeong KY, Östman A, Prakash J. SIRT1 inhibition in pancreatic cancer models: contrasting effects in vitro and in vivo. Eur. J. Pharmacol. 757, 59–67 (2015). • Reports the discovery of sirtuin inhibitor used in this study.
  Medline CASGoogle Scholar
• 15 Yoon Y, Ali M, Wei A et al. Correction: discovery of a potent and highly fluorescent sirtuin inhibitor. Medchemcomm 6(12), 2235–2235 (2015).
  CASGoogle Scholar
• 16 Tonelli M, Tasso B, Mina L, Paglietti G, Boido V, Sparatore F. Primary anti-proliferative activity evaluation of 1-(quinolizidin-1’-yl)methyl- and 1-(ω-tert-amino)alkyl-substituted 2-phenyl-, 2-benzyl- and 2-[(benzotriazol-1/2-yl)methyl]benzimidazoles on human cancer cell lines. Mol. Divers. 17(3), 409–419 (2013).
  Medline CASGoogle Scholar
• 17 Blaszczak-Swiatkiewicz K, Olszewska P, Mikiciuk-Olasik E. Biological approach of anticancer activity of new benzimidazole derivatives. Pharmacol. Rep. 66(1), 100–106 (2014).
  Medline CASGoogle Scholar
• 18 Mantu D, Antoci V, Moldoveanu C, Zbancioc G, Mangalagiu II. Hybrid imidazole (benzimidazole)/pyridine (quinoline) derivatives and evaluation of their anticancer and antimycobacterial activity. J. Enzyme Inhib. Med. Chem. 31(Suppl. 2), 96–103 (2016).
  Medline CASGoogle Scholar
• 19 Özdemir A, Uzunoğlu S, Çalışkan B, Banoğlu E, Ark M. Anticancer activity of novel benzimidazole derivatives against MCF-7 cancer cells. FASEB J. 31(Suppl. 1), 934.910 (2017).
  Google Scholar
• 20 Chu B, Liu F, Li L et al. A benzimidazole derivative exhibiting antitumor activity blocks EGFR and HER2 activity and upregulates DR5 in breast cancer cells. Cell Death Dis. 6, e1686 (2015).
  Medline CASGoogle Scholar
• 21 Dai X, Wang L, Deivasigamni A et al. A novel benzimidazole derivative, MBIC inhibits tumor growth and promotes apoptosis via activation of ROS-dependent JNK signaling pathway in hepatocellular carcinoma. Oncotarget 8(8), 12831–12842 (2017).
  MedlineGoogle Scholar
• 22 Liu JF, Huang YL, Yang WH, Chang CS, Tang CH. 1-benzyl-2-phenylbenzimidazole (BPB), a benzimidazole derivative, induces cell apoptosis in human chondrosarcoma through intrinsic and extrinsic pathways. Int. J. Mol. Sci. 13(12), 16472–16488 (2012).
  Medline CASGoogle Scholar
• 23 Yoon YK, Ali MA, Wei AC et al. Correction: discovery of a potent and highly fluorescent sirtuin inhibitor. Medchemcomm 6(12), 2235–2235 (2015).
  CASGoogle Scholar
• 24 Chaitanya GV, Alexander JS, Babu PP. PARP-1 cleavage fragments: signatures of cell-death proteases in neurodegeneration. Cell Commun. Signal. 8(1), 31 (2010).
  Medline CASGoogle Scholar
• 25 Nosho K, Shima K, Irahara N et al. SIRT1 histone deacetylase expression is associated with microsatellite instability and CpG island methylator phenotype in colorectal cancer. Mod. Pathol. 22(7), 922–932 (2009).
  Medline CASGoogle Scholar
• 26 Chen X, Sun K, Jiao S et al. High levels of SIRT1 expression enhance tumorigenesis and associate with a poor prognosis of colorectal carcinoma patients. Sci. Rep. 4, 7481 (2014).
  Medline CASGoogle Scholar
• 27 Wang Q, Zhou Y, Weiss HL, Evers BM. Abstract 4619: Sirt2 protein is required for activation of mTOR signaling in colorectal cancer cells. Cancer Res. 76(Suppl. 14), 4619 (2016).
  MedlineGoogle Scholar
• 28 Fong Y, Lin Y-C, Wu C-Y et al. The antiproliferative and apoptotic effects of sirtinol, a sirtuin inhibitor on human lung cancer cells by modulating Akt/β-catenin-Foxo3a axis. ScientificWorldJournal 2014, 1–8 (2014).
  Google Scholar
• 29 Lara E, Mai A, Calvanese V et al. Salermide, a sirtuin inhibitor with a strong cancer-specific proapoptotic effect. Oncogene 28(6), 781–791 (2009).
  Medline CASGoogle Scholar
• 30 Hirai S, Endo S, Saito R et al. Antitumor effects of a sirtuin inhibitor, tenovin-6, against gastric cancer cells via death receptor 5 up-regulation. PLoS ONE 9(7), e102831 (2014).
  MedlineGoogle Scholar
• 31 Marques IJ, Weiss FU, Vlecken DH et al. Metastatic behaviour of primary human tumours in a zebrafish xenotransplantation model. BMC Cancer 9(1), 128 (2009).
  MedlineGoogle Scholar
• 32 Carafa V, Rotili D, Forgione M et al. Sirtuin functions and modulation: from chemistry to the clinic. Clin. Epigenetics 8(1), 61 (2016). • Highlights the importance of sirtuin modulation in sirtuin inhibitor development.
  MedlineGoogle Scholar
• 33 Kozako T, Suzuki T, Yoshimitsu M, Arima N, Honda S-I, Soeda S. Anticancer agents targeted to sirtuins. Molecules 19(12), 20295–20313 (2014). • Accounts the role of SIRT1 and SIRT2 as anticancer therapy targets.
  MedlineGoogle Scholar
• 34 Kim H-W, Kim S-A, Ahn S-G. Sirtuin inhibitors, EX527 and AGK2, suppress cell migration by inhibiting HSF1 protein stability. Oncol. Rep. 35(1), 235–242 (2016).
  Medline CASGoogle Scholar
• 35 Bosch-Presegué L, Vaquero A. The dual role of sirtuins in cancer. Genes Cancer 2(6), 648–662 (2011). • Accounts the detailed information of sirtuin in cancer.
  Medline CASGoogle Scholar
• 36 Crowley LC, Christensen ME, Waterhouse NJ. Measuring survival of adherent cells with the colony-forming assay. Cold Spring Harb. Protoc. 2016(8), doi:10.1101/pdb.prot087171 (2016).
  Google Scholar
• 37 Munshi A, Hobbs M, Meyn RE. Clonogenic cell survival assay. Methods Mol. Med. 110, 21–28 (2005).
  MedlineGoogle Scholar
• 38 Chen J, Zhang B, Wong N et al. Sirtuin 1 is upregulated in a subset of hepatocellular carcinomas where it is essential for telomere maintenance and tumor cell growth. Cancer Res. 71(12), 4138–4149 (2011).
  Medline CASGoogle Scholar
• 39 Hao C, Zhu P-X, Yang X et al. Overexpression of SIRT1 promotes metastasis through epithelial–mesenchymal transition in hepatocellular carcinoma. BMC Cancer 14(1), 978 (2014).
  MedlineGoogle Scholar
• 40 Palmirotta R, Cives M, Della-Morte D et al. Sirtuins and cancer: role in the epithelial–mesenchymal transition. Oxid. Med. Cell. Longev. 2016, 1–9 (2016).
  Google Scholar
• 41 Zhang L, Wang X, Chen P. MiR-204 down regulates SIRT1 and reverts SIRT1-induced epithelial–mesenchymal transition, anoikis resistance and invasion in gastric cancer cells. BMC Cancer 13(1), 290 (2013).
  Medline CASGoogle Scholar
• 42 Wang J, Kim TH, Ahn MY et al. Sirtinol, a class III HDAC inhibitor, induces apoptotic and autophagic cell death in MCF-7 human breast cancer cells. Int. J. Oncol. 41(3), 1101–1109 (2012).
  Medline CASGoogle Scholar
• 43 Stenzinger A, Endris V, Klauschen F et al. High SIRT1 expression is a negative prognosticator in pancreatic ductal adenocarcinoma. BMC Cancer 13(1), 450 (2013).
  MedlineGoogle Scholar
• 44 Heltweg B, Gatbonton T, Schuler AD et al. Antitumor activity of a small-molecule inhibitor of human silent information regulator 2 enzymes. Cancer Res. 66(8), 4368–4377 (2006).
  Medline CASGoogle Scholar
• 45 Bosch-Presegue L, Vaquero A. Sirtuins in stress response: guardians of the genome. Oncogene 33(29), 3764–3775 (2014). • Accounts the detailed information of sirtuin in human genome.
  Medline CASGoogle Scholar
• 46 Head PE, Zhang H, Bastien AJ et al. Sirtuin 2 mutations in human cancers impair its function in genome maintenance. J. Biol. Chem. 292(24), 9919–9931 (2017).
  Medline CASGoogle Scholar
• 47 Wlodkowic D, Telford W, Skommer J, Darzynkiewicz Z. Apoptosis and beyond: cytometry in studies of programmed cell death. Methods Cell Biol. 103, 55–98 (2011).
  Medline CASGoogle Scholar
• 48 Kan WLT, Yin C, Xu HX et al. Antitumor effects of novel compound, guttiferone K, on colon cancer by p21Waf1/Cip1-mediated G0/G1 cell cycle arrest and apoptosis. Int. J. Cancer 132(3), 707–716 (2013).
  Medline CASGoogle Scholar
• 49 Peck B, Chen C-Y, Ho K-K et al. SIRT inhibitors induce cell death and p53 acetylation through targeting both SIRT1 and SIRT2. Mol. Cancer Ther. 9(4), 844–855 (2010). • Reveals the effect on SIRT1 and SIRT2 inhibition by different sirtuin inhibitors.
  Medline CASGoogle Scholar
• 50 Karimian A, Ahmadi Y, Yousefi B. Multiple functions of p21 in cell cycle, apoptosis and transcriptional regulation after DNA damage. DNA Repair (Amst.) 42, 63–71 (2016).
  Medline CASGoogle Scholar
• 51 Ford J, Jiang M, Milner J. Cancer-specific functions of SIRT1 enable human epithelial cancer cell growth and survival. Cancer Res. 65(22), 10457–10463 (2005).
  Medline CASGoogle Scholar
• 52 Nakano K, Vousden KH. PUMA, a novel proapoptotic gene, is induced by p53. Mol. Cell 7(3), 683–694 (2001).
  Medline CASGoogle Scholar
• 53 Xia M, Knezevic D, Vassilev LT. p21 does not protect cancer cells from apoptosis induced by nongenotoxic p53 activation. Oncogene 30(3), 346–355 (2011).
  MedlineGoogle Scholar
• 54 Chen T, Turner J, McCarthy S, Scaltriti M, Bettuzzi S, Yeatman TJ. Clusterin-mediated apoptosis is regulated by adenomatous polyposis coli and is p21 dependent but p53 independent. Cancer Res. 64(20), 7412–7419 (2004).
  Medline CASGoogle Scholar
• 55 Dvory-Sobol H, Sagiv E, Kazanov D, Ben-Ze'ev A, Arber N. Targeting the active beta-catenin pathway to treat cancer cells. Mol. Cancer Ther. 5(11), 2861–2871 (2006).
  Medline CASGoogle Scholar
• 56 Sharma NK, Kumar A, Kumari A et al. Nitric oxide down-regulates topoisomerase i and induces camptothecin resistance in human breast MCF-7 tumor cells. PLoS ONE 10(11), e0141897 (2015).
  MedlineGoogle Scholar
• 57 Paul-Samojedny M, Kokocińska D, Samojedny A et al. Expression of cell survival/death genes: Bcl-2 and Bax at the rate of colon cancer prognosis. Biochim. Biophys. Acta 1741(1), 25–29 (2005).
  Medline CASGoogle Scholar
• 58 Yip K, Reed J. Bcl-2 family proteins and cancer. Oncogene 27(50), 6398–6406 (2008).
  Medline CASGoogle Scholar
• 59 Wajant H, Scheurich P. Tumor necrosis factor receptor-associated factor (TRAF) 2 and its role in TNF signaling. Int. J. Biochem. Cell Biol. 33(1), 19–32 (2001).
  Medline CASGoogle Scholar
• 60 Shu HB, Takeuchi M, Goeddel DV. The tumor necrosis factor receptor 2 signal transducers TRAF2 and c-IAP1 are components of the tumor necrosis factor receptor 1 signaling complex. Proc. Natl Acad. Sci. USA 93(24), 13973–13978 (1996).
  Medline CASGoogle Scholar
• 61 Petersen SL, Chen TT, Lawrence DA, Marsters SA, Gonzalvez F, Ashkenazi A. TRAF2 is a biologically important necroptosis suppressor. Cell Death Differ. 22(11), 1846–1857 (2015).
  Medline CASGoogle Scholar
• 62 Moskalev AA, Proshkina EN, Shaposhnikov MV. Gadd45 proteins in aging and longevity of mammals and drosophila. In: Life Extension: Lessons from Drosophila. Springer, Cham, Switzerland, 39–65 (2015).
  Google Scholar
• 63 Tamura ER, De Vasconcellos FJ, Sarkar D, Libermann AT, Fisher BP, Zerbini FL. GADD45 proteins: central players in tumorigenesis. Curr. Mol. Med. 12(5), 634–651 (2012).
  Medline CASGoogle Scholar