Superior antimitogenic and chemosensitization activities of the combination treatment of the histone deacetylase inhibitor apicidin and proteasome inhibitors on human colorectal cancer cells

Heider U, Rademacher J, Lamottke B, et al: Synergistic interaction of the histone deacetylase inhibitor SAHA with the proteasome inhibitor bortezomib in cutaneous T cell lymphoma. Eur J Haematol. 82:440–449. 2009. View Article : Google Scholar : PubMed/NCBI

Marks PA and Breslow R: Dimethyl sulfoxide to vorinostat: development of this histone deacetylase inhibitor as an anticancer drug. Nat Biotechnol. 25:84–90. 2007. View Article : Google Scholar : PubMed/NCBI

Frew AJ, Johnstone RW and Bolden JE: Enhancing the apoptotic and therapeutic effects of HDAC inhibitors. Cancer Lett. 280:125–133. 2009. View Article : Google Scholar : PubMed/NCBI

Andrews KT, Walduck A, Kelso MJ, Fairlie DP, Saul A and Parsons PG: Anti-malarial effect of histone deacetylation inhibitors and mammalian tumor cytodifferentiating agents. Int J Parasitol. 30:761–768. 2000. View Article : Google Scholar : PubMed/NCBI

Im JY, Park H, Kang KW, Choi WS and Kim HS: Modulation of cell cycles and apoptosis by apicidin in estrogen receptor (ER)-positive and -negative human breast cancer cells. Chem Biol Interact. 172:235–244. 2008. View Article : Google Scholar : PubMed/NCBI

Kim MS, Son MW, Kim WB, Park YI and Moon A: Apicidin, an inhibitor of histone deacetylase, prevents H-ras-induced invasive phenotype. Cancer Lett. 157:23–30. 2000. View Article : Google Scholar : PubMed/NCBI

Kwon SH, Ahn SH, Kim YK, et al: Apicidin, a histone deacetylase inhibitor, induces apoptosis and Fas/Fas ligand expression in human acute promyelocytic leukemia cells. J Biol Chem. 277:2073–2080. 2002. View Article : Google Scholar : PubMed/NCBI

Choi JH, Lee JY, Choi AY, et al: Apicidin induces endoplasmic reticulum stress- and mitochondrial dysfunction-associated apoptosis via phospholipase Cγ1- and Ca²⁺-dependent pathway in mouse Neuro-2a. Apoptosis. 17:1340–58. 2012.PubMed/NCBI

Kobayashi H, Tan EM and Fleming SE: Acetylation of histones associated with the p21WAF1/Cip1 gene transcription in human colorectal adenocarcinoma cells. Int J Cancer. 109:207–213. 2004. View Article : Google Scholar : PubMed/NCBI

Xu Y: Regulation of p53 responses by post-translational modifications. Cell Death Differ. 10:400–403. 2003. View Article : Google Scholar : PubMed/NCBI

Tang G, Minemoto Y, Dibling B, Purcell NH, Li Z, Karin M and Lin A: Inhibition of JNK activation through NF-κB target gene. Nature. 414:313–317. 2001.

Verma IM, Stevenson JK, Schwartz EM, Van Antwerp D and Miyamoto S: Rel/NF-κB family: intimate tales of association and dissociation. Genes Dev. 9:2723–2735. 1995.

Huang TT, Kudo N, Yoshida M and Miyanoto S: A nuclear export signal in the N-terminal regulatory domain of IκBα controls cytoplasmic localization of inactive NF-κB/IκBα complexes. Proc Natl Acad Sci USA. 97:1014–1019. 2000.

Zandi E, Rothwarf DM, Delhase M, Hayakawa M and Karin M: The IκB kinase complex (IKK) contains two kinase subunits, IKKα and IKKβ, necessary for IκB phosphorylation and NF-κB activation. Cell. 91:243–252. 1997.

Ghosh S, May MJ and Kopp EB: NF-κB and Rel proteins: evolutionarily conserved mediators of immune responses. Ann Rev Immunol. 16:225–260. 1998.

Chen L, Fischle W, Verdin E and Greene WC: Duration of nuclear NF-κB action regulated by reversible acetylation. Science. 293:1653–2657. 2001.

Zhong H, May MJ, Jimi E and Ghosh S: The phosphorylation status of nuclear NF-κB determines its association with CBP/ p300 or HDAC-1. Mol Cell. 9:625–636. 2002.

Sterz J, von Metzler I, Hahne JC, et al: The potential of proteasome inhibitors in cancer therapy. Expert Opin Investig Drugs. 17:879–895. 2008. View Article : Google Scholar : PubMed/NCBI

Abaza MS, Al-Safar A, Al-Sawan S and Al-Attiyah R: c-myc anti-sense oligonucleotides sensitize human colorectal cancer cells to chemotherapeutic drugs. Tumor Biol. 29:287–303. 2008. View Article : Google Scholar : PubMed/NCBI

Abaza MSI: Augmentation of the anticancer effects of proteasome inhibitors by combination with sodium butyrate in human colorectal cancer cells. Exp Ther Med. 1:675–693. 2010.

Lam PK, To EW, Chan ES, Liew CT, Lung IW and King WK: In vitro modulation of head and neck cell growth by human recombinant interferon α and 13-cis-retinoic acid. Br J Biomed Sci. 58:226–229. 2001.

Abaza MSI, Bahman AM, Al-Attiyah RJ and Kollamparambil AM: Synergistic induction of apoptosis and chemosensitization of human colorectal cancer cells by histone deacetylase inhibitor, scriptaid and proteasome inhibitors: potential mechanisms of action. Tumor Biol. 33:1951–1972. 2012. View Article : Google Scholar

Rosato RR and Grant S: Histone deacetylase inhibitors in clinical development. Expert Opin Investig Drugs. 13:21–38. 2004. View Article : Google Scholar : PubMed/NCBI

Mayo MW, Denlinger CE, Broad RM, et al: Ineffectiveness of histone deacetylase inhibitors to induce apoptosis involves the transcriptional activation of NF-κB through the Akt pathway. J Biol Chem. 278:18980–18989. 2003.PubMed/NCBI

Dasmahapatra G, Lembersky D, Son MP, et al: Carfilzomib interacts synergistically with histone deacetylase inhibitors in mantle cell lymphoma cells in vitro and in vivo. Mol Cancer Ther. 10:1686–1697. 2011. View Article : Google Scholar : PubMed/NCBI

Savita B, Sriram B, Kevin D, et al: The histone deacetylase inhibitor PCI-24781 induces caspase and reactive oxygen species-dependent apoptosis through NFκB mechanisms and is synergistic with bortezomib in lymphoma cells. Clin Cancer Res. 15:3354–3365. 2009.PubMed/NCBI

Luu T, Chung C and Somlo G: Combining emerging agents in advanced breast cancer. Oncologist. 16:760–771. 2011. View Article : Google Scholar : PubMed/NCBI

Masdehors P, Omura S, Merle-Béral H, et al: Increased sensitivity of CCL-derived lymphocytes to apoptotic death activation by the proteasome-specific inhibitor lactacystin. Br J Haematol. 105:752–757. 1999. View Article : Google Scholar : PubMed/NCBI

Frankland-Searby S and Bhaumik SR: The 26S proteasome complex: An attractive target for cancer therapy. Biochim Biophys Acta. 1825:64–76. 2012.PubMed/NCBI

Adams J: The proteasome: a suitable anti-neoplastic target. Nat Rev Cancer. 4:349–360. 2004. View Article : Google Scholar : PubMed/NCBI

Nawrocki ST, Bruns CJ, Harbison MT, et al: Effects of the proteasome inhibitor PS-341 on apoptosis and angiogenesis in orthotopic human pancreatic tumor xenografts. Mol Cancer Ther. 1:1243–1253. 2002.PubMed/NCBI

Yu C, Rahmani M, Conrad D, Subler M, Dent P and Grant S: The proteasome inhibitor bortezomib interacts synergistically with histone deacetylase inhibitors to induce apoptosis in Bcr/Abl⁺ cells sensitive and resistant to ST1571. Blood. 102:3765–3774. 2003. View Article : Google Scholar : PubMed/NCBI

Vigushin DM and Coomes RC: Histone deacetylase inhibitors in cancer treatment. Anticancer Drugs. 13:1–13. 2002. View Article : Google Scholar

Duan J, Friedman J, Nottingham L, Chen Z, Ara G and Van Waes C: Nuclear factor-κ p65 small interfering RNA or proteasome inhibitor bortezomib sensitizes head and neck squamous cell carcinomas to classic histone deacetylae inhibitors and novel histone deacetylase inhibitor PZD101. Mol Cancer Ther. 6:37–50. 2007.

Denlinger C, Keller M, Mayo M, Broad RM and Jones DR: Combined proteasome and histone deacetylase inhibition in non-small cell lung cancer. J Thorac Cardiovasc Surg. 127:1078–1086. 2004. View Article : Google Scholar : PubMed/NCBI

Tai DI, Tsai SL, Chang YH, et al: Constitutive activation of nuclear factor kappaB in hepatocellular carcinoma. Cancer. 89:2274–2228. 2000. View Article : Google Scholar : PubMed/NCBI

Johnstone RW: Histone-deacetylase inhibitors: novel drugs for the treatment of cancer. Nat Rev Drug Discov. 1:287–299. 2002. View Article : Google Scholar : PubMed/NCBI

Yin L, Laevsky G and Giardina C: Butyrate suppression of colonocyte NF-kappa B activation and cellular proteasome activity. J Biol Chem. 276:44641–44646. 2001. View Article : Google Scholar : PubMed/NCBI

Jiang Y, Wang Y, Su Z, et al: Synergistic induction of apoptosis in HeLa cells by the proteasome inhibitor bortezomib and histone deacetylase inhibitor SAHA. Mol Med Rep. 3:613–619. 2010.PubMed/NCBI

Perez-Galan P, Roue G, Villamor N, Montserrat E, Campo E and Colomer D: The proteasome inhibitor bortezomib induces apoptosis in mantle-cell lymphoma through generation of ROS and Noxa activation independent of p53 status. Blood. 107:257–264. 2006. View Article : Google Scholar : PubMed/NCBI

Heider U, von Metzler I, Kaiser M, et al: Synergistic interaction of the histone deacetylase inhibitor SAHA with the proteasome bortezomib in mantle cell lymphoma. Eur J Haematol. 80:133–142. 2008. View Article : Google Scholar : PubMed/NCBI

Ling YH, Liebes L, Zou Y and Perez-Soler R: Reactive oxygen species generation and mitochondrial dysfunction in the apoptotic response to bortezomib, a novel proteasome inhibitor, in human H460 non-small cell lung cancer cells. J Biol Chem. 278:33714–33723. 2003. View Article : Google Scholar : PubMed/NCBI

Pei XY, Dai Y and Grant S: Synergistic induction of oxidative injury and apoptosis in human multiple myeloma cells by the proteasome inhibitors bortezomib and histone deacetylase inhibitors. Clin Cancer Res. 10:3839–3852. 2004. View Article : Google Scholar

Pitts TM, Morrow M, Kaufman SA, Tentler JJ and Eckhardt SG: Vorinostat and bortezomib exert synergistic antiproliferative and proapoptotic effects in colon cancer cells models. Mol Cancer Ther. 8:342–349. 2009. View Article : Google Scholar : PubMed/NCBI

Perez-Galan P, Roue G, Villamor N, Montserrat E, Campo E and Colomer D: The BH3-mimetic GX15-070 synergizes with bortezomib in mantle cell lymphoma by enhancing Noxa-mediated activation of Bak. Blood. 109:4441–4449. 2007. View Article : Google Scholar : PubMed/NCBI

Miller C, Ban K, Dujka ME, et al: NPI-0052, a novel proteasome inhibitor, induces caspase-8 and ROS-dependent apoptosis alone and in combination with HDAC inhibitors in leukemia cells. Blood. 110:267–277. 2007. View Article : Google Scholar : PubMed/NCBI

Yu C, Friday BB, Yang L, et al: Mitochondrial Bax translocation partially mediates synergistic cytotoxicity between histone deacetylase inhibitors and proteasome inhibitors in glioma cells. Neuro Oncol. 10:309–319. 2007. View Article : Google Scholar

Orlowski RZ: The role of ubiquitin-proteasome pathway in apoptosis. Cell Death Diff. 6:303–331. 1999. View Article : Google Scholar

Buoncervello M, Borghi P, Romagnoli G, et al: Apicidin and docetaxel combination treatment drives CTCFL expression and HMGB1 release acting as potential antitumor immune response inducers in metastatic breast cancer cells. Neoplasia. 14:855–867. 2012.

Lawen A: Apoptosis - an introduction. Bioessays. 25:888–896. 2003. View Article : Google Scholar

Lei K, Nimmual A, Zong WX, et al: The Bax subfamily of Bcl2 related proteins is essential for apoptotic signal transduction by c-Jun NH2-terminal kinase. Mol Cell Biol. 22:4929–4942. 2002. View Article : Google Scholar : PubMed/NCBI

Tacchini L, Dansi P, Matteucci E, Bemelli-Zazzera A and Desiderio MA: Influence of proteasome and redox state on heat shock-induced activation of stress kinases, AP-1 and HSF. Biochim Biophy Acta. 1538:76–89. 2001. View Article : Google Scholar : PubMed/NCBI

Gardai SJ, Hildeman DH, Frankel SK, et al: phosphorylation of Bax Ser 184by Akt regulates its activity and apoptosis in neutrophils. J Biol Chem. 279:21085–21095. 2004. View Article : Google Scholar : PubMed/NCBI

Catley L, Weisberg E, Kiziltepe T, et al: Aggresome induction by proteasome inhibitor bortezomib and α-tubulin hyperacetylation by tubulin deacetylase (TDAC) inhibitor LBH589 are synergistic in myeloma cells. Blood. 108:3441–3449. 2006.

Baldini E, Gardin G, Giannessi P, et al: A randomized trial of chemotherapy with or without estrogenic recruitment in locally advanced breast cancer. North-West Oncology Group (GONO) study, Italy. Tumori. 83:829–833. 1997.PubMed/NCBI

Hwang JJ, Kim YS, Kim T, et al: A novel histone deacetylase inhibitor, CG2007745, potentiates anticancer effect of docetaxel in prostate cancer via decreasing Mcl-1 and Bcl-(XL). Invest New Drugs. 30:1434–1442. 2011. View Article : Google Scholar : PubMed/NCBI

Linares A, Dalenc F, Balaguer P, Boulle N and Gavailles V: Manipulating protein acetylation in breast cancer: a promising approaching in combination with hormonal therapies? J Biomed Biotechnol. 2011:1–15. 2011. View Article : Google Scholar : PubMed/NCBI

Munster PN, Thurn KT, Thomas S, et al: A phase II study of the histone deacetylase inhibitor vorinostat combined with tamoxifen for the treatment of patients with hormone therapy-resistant breast cancer. Br J Cancer. 104:1828–1835. 2011. View Article : Google Scholar : PubMed/NCBI

O’Connor OA, Heaney ML, Schwartz L, et al: Clinical experience with intravenous and oral formulations of the novel histone deacetylase inhibitor suberoylanilide hydroxamic acid in patients with advanced hematologic malignancies. J Clin Oncol. 24:166–173. 2005.

Vansteenkiste J, Van Cutsem E, Dumez H, et al: Early phase II trial of oral vorinostat in telapsed or refractory breast, colorectal, or non-small cell lung cancer. Invest New Drugs. 26:483–488. 2008. View Article : Google Scholar : PubMed/NCBI