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Restoring TRAIL Mediated Signaling in Ovarian Cancer Cells

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  • Published:
Archivum Immunologiae et Therapiae Experimentalis Aims and scope

Abstract

Ovarian cancer has emerged as a multifaceted and genomically complex disease. Genetic/epigenetic mutations, suppression of tumor suppressors, overexpression of oncogenes, rewiring of intracellular signaling cascades and loss of apoptosis are some of the deeply studied mechanisms. In vitro and in vivo studies have highlighted different molecular mechanisms that regulate tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) mediated apoptosis in ovarian cancer. In this review, we bring to limelight, expansion in understanding systematical characterization of ovarian cancer cells has led to the rapid development of new drugs and treatments to target negative regulators of TRAIL mediated signaling pathway. Wide ranging synthetic and natural agents have been shown to stimulate mRNA and protein expression of death receptors. This review is compartmentalized into programmed cell death protein 4, platelet-derived growth factor signaling and miRNA control of TRAIL mediated signaling to ovarian cancer. Mapatumumab and PRO95780 have been tested for efficacy against ovarian cancer. Use of high-throughput screening assays will aid in dissecting the heterogeneity of this disease and increasing a long-term survival which might be achieved by translating rapidly accumulating information obtained from molecular and cellular studies to clinic researches.

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References

  • Ausserlechner MJ, Salvador C, Deutschmann A et al (2013) Therapy-resistant acute lymphoblastic leukemia (ALL) cells inactivate FOXO3 to escape apoptosis induction by TRAIL and Noxa. Oncotarget 4:995–1007

    PubMed Central  PubMed  Google Scholar 

  • Aydin C, Sanlioglu AD, Bisgin A et al (2010) NF-kappaB targeting by way of IKK inhibition sensitizes lung cancer cells to adenovirus delivery of TRAIL. BMC Cancer 10:584

    CAS  PubMed Central  PubMed  Google Scholar 

  • Bevis KS, McNally LR, Sellers JC et al (2011) Anti-tumor activity of an anti-DR5 monoclonal antibody, TRA-8, in combination with taxane/platinum-based chemotherapy in an ovarian cancer model. Gynecol Oncol 121:193–199

    CAS  PubMed  Google Scholar 

  • Braga Lda C, Silva LM, Piedade JB et al (2014) Epigenetic and expression analysis of TRAIL-R2 and BCL2: on the TRAIL to knowledge of apoptosis in ovarian tumors. Arch Gynecol Obstet 289:1061–1069

    PubMed  Google Scholar 

  • Cai J, Yang C, Yang Q et al (2013) Deregulation of let-7e in epithelial ovarian cancer promotes the development of resistance to cisplatin. Oncogenesis 2:e75

    CAS  PubMed Central  PubMed  Google Scholar 

  • Camidge DR, Herbst RS, Gordon MS et al (2010) A phase I safety and pharmacokinetic study of the death receptor 5 agonistic antibody PRO95780 in patients with advanced malignancies. Clin Cancer Res 16:1256–1263

    CAS  PubMed  Google Scholar 

  • Chang HW, Ali SZ, Cho SK et al (2002a) Detection of allelic imbalance in ascitic supernatant by digital single nucleotide polymorphism analysis. Clin Cancer Res 8:2580–2585

    CAS  PubMed  Google Scholar 

  • Chang HW, Lee SM, Goodman SN et al (2002b) Assessment of plasma DNA levels, allelic imbalance, and CA 125 as diagnostic tests for cancer. J Natl Cancer Inst 94:1697–1703

    CAS  PubMed  Google Scholar 

  • Chang HW, Chuang LY, Ho CH et al (2008) Odds ratio-based genetic algorithms for generating SNP barcodes of genotypes to predict disease susceptibility. OMICS 12:71–81

    CAS  PubMed  Google Scholar 

  • Chang HW, Chuang LY, Tsai MT et al (2012) The importance of integrating SNP and cheminformatics resources to pharmacogenomics. Curr Drug Metab 13:991–999

    CAS  PubMed  Google Scholar 

  • Chen D, Zhang Y, Wang J et al (2013a) MicroRNA-200c overexpression inhibits tumorigenicity and metastasis of CD117+ CD44+ ovarian cancer stem cells by regulating epithelial-mesenchymal transition. J Ovarian Res 6:50

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chen JB, Chuang LY, Lin YD et al (2013b) Preventive SNP–SNP interactions in the mitochondrial displacement loop (D-loop) from chronic dialysis patients. Mitochondrion 13:698–704

    CAS  PubMed  Google Scholar 

  • Chen JB, Chuang LY, Lin YD et al (2014) Genetic algorithm-generated SNP barcodes of the mitochondrial D-loop for chronic dialysis susceptibility. Mitochondrial DNA 25:231–237

    CAS  PubMed  Google Scholar 

  • Chi HC, Chen SL, Liao CJ et al (2012) Thyroid hormone receptors promote metastasis of human hepatoma cells via regulation of TRAIL. Cell Death Differ 19:1802–1814

    CAS  PubMed Central  PubMed  Google Scholar 

  • Cho SH, Park MH, Lee HP et al (2014) (E)-2,4-Bis(p-hydroxyphenyl)-2-butenal enhanced TRAIL-induced apoptosis in ovarian cancer cells through downregulation of NF-kappaB/STAT3 pathway. Arch Pharm Res 37:652–661

    CAS  PubMed  Google Scholar 

  • Chou J, Lin JH, Brenot A et al (2013) GATA3 suppresses metastasis and modulates the tumour microenvironment by regulating microRNA-29b expression. Nat Cell Biol 15:201–213

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chuang LY, Yang CH, Tsui KH et al (2008) Restriction enzyme mining for SNPs in genomes. Anticancer Res 28:2001–2007

    CAS  PubMed  Google Scholar 

  • Chuang LY, Lin YD, Chang HW et al (2012) An improved PSO algorithm for generating protective SNP barcodes in breast cancer. PLoS One 7:e37018

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chuang LY, Chang HW, Lin MC et al (2013) Improved branch and bound algorithm for detecting SNP–SNP interactions in breast cancer. J Clin Bioinforma 3:4

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chuang LY, Lane HY, Lin YD et al (2014) Identification of SNP barcode biomarkers for genes associated with facial emotion perception using particle swarm optimization algorithm. Ann Gen Psychiatry 13:15

    PubMed Central  PubMed  Google Scholar 

  • Costa PM, Cardoso AL, Pereira de Almeida LF et al (2012) PDGF-B-mediated downregulation of miR-21: new insights into PDGF signaling in glioblastoma. Hum Mol Genet 21:5118–5130

    CAS  PubMed Central  PubMed  Google Scholar 

  • Dokouhaki P, Schuh NW, Joe B et al (2013) NKG2D regulates production of soluble TRAIL by ex vivo expanded human gammadelta T cells. Eur J Immunol 43:3175–3182

    CAS  PubMed  Google Scholar 

  • Dong HP, Kleinberg L, Silins I et al (2008) Death receptor expression is associated with poor response to chemotherapy and shorter survival in metastatic ovarian carcinoma. Cancer 112:84–93

    PubMed  Google Scholar 

  • Dong Z, Yang L, Lai D (2013) KLF5 strengthens drug resistance of ovarian cancer stem-like cells by regulating survivin expression. Cell Prolif 46:425–435

    CAS  PubMed  Google Scholar 

  • Ehrenschwender M, Siegmund D, Wicovsky A et al (2010) Mutant PIK3CA licenses TRAIL and CD95L to induce non-apoptotic caspase-8-mediated ROCK activation. Cell Death Differ 17:1435–1447

    CAS  PubMed  Google Scholar 

  • El-Gazzar A, Wittinger M, Perco P et al (2010) The role of c-FLIP(L) in ovarian cancer: chaperoning tumor cells from immunosurveillance and increasing their invasive potential. Gynecol Oncol 117:451–459

    CAS  PubMed  Google Scholar 

  • Erichsen HC, Chanock SJ (2004) SNPs in cancer research and treatment. Br J Cancer 90:747–751

    CAS  PubMed Central  PubMed  Google Scholar 

  • Farrand L, Byun S, Kim JY et al (2013) Piceatannol enhances cisplatin sensitivity in ovarian cancer via modulation of p53, X-linked inhibitor of apoptosis protein (XIAP), and mitochondrial fission. J Biol Chem 288:23740–23750

    CAS  PubMed Central  PubMed  Google Scholar 

  • Festa M, Petrella A, Alfano S et al (2009) R-roscovitine sensitizes anaplastic thyroid carcinoma cells to TRAIL-induced apoptosis via regulation of IKK/NF-kappaB pathway. Int J Cancer 124:2728–2736

    CAS  PubMed  Google Scholar 

  • Fingas CD, Blechacz BR, Smoot RL et al (2010) A smac mimetic reduces TNF related apoptosis inducing ligand (TRAIL)-induced invasion and metastasis of cholangiocarcinoma cells. Hepatology 52:550–561

    CAS  PubMed Central  PubMed  Google Scholar 

  • Frederick PJ, Kendrick JE, Straughn JM Jr et al (2009) Effect of TRA-8 anti-death receptor 5 antibody in combination with chemotherapy in an ex vivo human ovarian cancer model. Int J Gynecol Cancer 19:814–819

    PubMed  Google Scholar 

  • Gao X, Wang B, Wei X et al (2012) Anticancer effect and mechanism of polymer micelle-encapsulated quercetin on ovarian cancer. Nanoscale 4:7021–7030

    CAS  PubMed  Google Scholar 

  • Garofalo M, Jeon YJ, Nuovo GJ et al (2013) MiR-34a/c-dependent PDGFR-alpha/beta downregulation inhibits tumorigenesis and enhances TRAIL-induced apoptosis in lung cancer. PLoS One 8:e67581

    CAS  PubMed Central  PubMed  Google Scholar 

  • Giacomini KM, Brett CM, Altman RB et al (2007) The pharmacogenetics research network: from SNP discovery to clinical drug response. Clin Pharmacol Ther 81:328–345

    CAS  PubMed  Google Scholar 

  • Goncharenko-Khaider N, Matte I, Lane D et al (2012) Ovarian cancer ascites increase Mcl-1 expression in tumor cells through ERK1/2-Elk-1 signaling to attenuate TRAIL-induced apoptosis. Mol Cancer 11:84

    CAS  PubMed Central  PubMed  Google Scholar 

  • Gopalan A, Yu W, Sanders BG et al (2013) Simvastatin inhibition of mevalonate pathway induces apoptosis in human breast cancer cells via activation of JNK/CHOP/DR5 signaling pathway. Cancer Lett 329:9–16

    CAS  PubMed  Google Scholar 

  • Goplen D, Bougnaud S, Rajcevic U et al (2010) alphaB-crystallin is elevated in highly infiltrative apoptosis-resistant glioblastoma cells. Am J Pathol 177:1618–1628

    CAS  PubMed Central  PubMed  Google Scholar 

  • Gray HL, Sorensen EL, Hunt JS et al (2001) Three polymorphisms in the 3′ UTR of the TRAIL (TNF-related apoptosis-inducing ligand) gene. Genes Immun 2:469–470

    CAS  PubMed  Google Scholar 

  • Guo Y, Tian P, Yang C et al (2013) Silencing the double-stranded RNA binding protein DGCR8 inhibits ovarian cancer cell proliferation, migration, and invasion. Pharm Res. doi:10.1007/s11095-013-1219-9

    Google Scholar 

  • Horak P, Pils D, Haller G et al (2005a) Contribution of epigenetic silencing of tumor necrosis factor-related apoptosis inducing ligand receptor 1 (DR4) to TRAIL resistance and ovarian cancer. Mol Cancer Res 3:335–343

    CAS  PubMed  Google Scholar 

  • Horak P, Pils D, Kaider A et al (2005b) Perturbation of the tumor necrosis factor–related apoptosis-inducing ligand cascade in ovarian cancer: overexpression of FLIPL and deregulation of the functional receptors DR4 and DR5. Clin Cancer Res 11:8585–8591

    CAS  PubMed  Google Scholar 

  • Hotte SJ, Hirte HW, Chen EX et al (2008) A phase 1 study of mapatumumab (fully human monoclonal antibody to TRAIL-R1) in patients with advanced solid malignancies. Clin Cancer Res 14:3450–3455

    CAS  PubMed  Google Scholar 

  • Huang Y, Jin H, Liu Y et al (2011) FSH inhibits ovarian cancer cell apoptosis by up-regulating survivin and down-regulating PDCD6 and DR5. Endocr Relat Cancer 18:13–26

    CAS  PubMed  Google Scholar 

  • Huang JW, Wang Y, Dhillon KK et al (2013) Systematic screen identifies miRNAs that target RAD51 and RAD51D to enhance chemosensitivity. Mol Cancer Res 11:1564–1573

    CAS  PubMed  Google Scholar 

  • Huh JH, Kim TH, Kim K et al (2013) Dysregulation of miR-106a and miR-591 confers paclitaxel resistance to ovarian cancer. Br J Cancer 109:452–461

    CAS  PubMed Central  PubMed  Google Scholar 

  • Imam JS, Buddavarapu K, Lee-Chang JS et al (2010) MicroRNA-185 suppresses tumor growth and progression by targeting the Six1 oncogene in human cancers. Oncogene 29:4971–4979

    CAS  PubMed  Google Scholar 

  • Ishimura N, Isomoto H, Bronk SF et al (2006) Trail induces cell migration and invasion in apoptosis-resistant cholangiocarcinoma cells. Am J Physiol Gastrointest Liver Physiol 290:G129–G136

    CAS  PubMed  Google Scholar 

  • Jiang Q, Zhu H, Liang B et al (2012) Apoptosis-inducing effect of the DR5 monoclonal antibody, D-6, alone or in combination with cisplatin, on A2780 ovarian cancer cells. Mol Med Rep 6:316–320

    CAS  PubMed  Google Scholar 

  • Jiang L, Cao XC, Cao JG et al (2013) Casticin induces ovarian cancer cell apoptosis by repressing FoxM1 through the activation of FOXO3a. Oncol Lett 5:1605–1610

    CAS  PubMed Central  PubMed  Google Scholar 

  • Jung YH, Heo J, Lee YJ et al (2010) Quercetin enhances TRAIL-induced apoptosis in prostate cancer cells via increased protein stability of death receptor 5. Life Sci 86:351–357

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kamradt MC, Lu M, Werner ME et al (2005) The small heat shock protein alpha B-crystallin is a novel inhibitor of TRAIL-induced apoptosis that suppresses the activation of caspase-3. J Biol Chem 280:11059–11066

    CAS  PubMed  Google Scholar 

  • Keniry M, Pires MM, Mense S et al (2013) Survival factor NFIL3 restricts FOXO-induced gene expression in cancer. Genes Dev 27:916–927

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kikuchi S, Miyagishi R, Fukazawa T et al (2005) TNF-related apoptosis inducing ligand (TRAIL) gene polymorphism in Japanese patients with multiple sclerosis. J Neuroimmunol 167:170–174

    CAS  PubMed  Google Scholar 

  • Kim EH, Kim HS, Kim SU et al (2005) Sodium butyrate sensitizes human glioma cells to TRAIL-mediated apoptosis through inhibition of Cdc2 and the subsequent downregulation of survivin and XIAP. Oncogene 24:6877–6889

    CAS  PubMed  Google Scholar 

  • Kim JY, Kim EH, Park SS et al (2008) Quercetin sensitizes human hepatoma cells to TRAIL-induced apoptosis via Sp1-mediated DR5 up-regulation and proteasome-mediated c-FLIPS down-regulation. J Cell Biochem 105:1386–1398

    CAS  PubMed  Google Scholar 

  • Kim JY, Kim EH, Kim SU et al (2010) Capsaicin sensitizes malignant glioma cells to TRAIL-mediated apoptosis via DR5 upregulation and survivin downregulation. Carcinogenesis 31:367–375

    CAS  PubMed  Google Scholar 

  • Kim YJ, Lee SA, Myung SC et al (2012) Radicicol, an inhibitor of Hsp90, enhances TRAIL-induced apoptosis in human epithelial ovarian carcinoma cells by promoting activation of apoptosis-related proteins. Mol Cell Biochem 359:33–43

    CAS  PubMed  Google Scholar 

  • Koksal IT, Sanlioglu AD, Karacay B et al (2008) Tumor necrosis factor-related apoptosis inducing ligand-R4 decoy receptor expression is correlated with high Gleason scores, prostate-specific antigen recurrence, and decreased survival in patients with prostate carcinoma. Urol Oncol 26:158–165

    CAS  PubMed  Google Scholar 

  • Kong D, Li Y, Wang Z et al (2009) miR-200 regulates PDGF-D-mediated epithelial-mesenchymal transition, adhesion, and invasion of prostate cancer cells. Stem Cells 27:1712–1721

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kuang Y, Cai J, Li D et al (2013) Repression of Dicer is associated with invasive phenotype and chemoresistance in ovarian cancer. Oncol Lett 5:1149–1154

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kuhnert F, Tam BY, Sennino B et al (2008) Soluble receptor-mediated selective inhibition of VEGFR and PDGFRbeta signaling during physiologic and tumor angiogenesis. Proc Natl Acad Sci USA 105:10185–10190

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kurita S, Higuchi H, Saito Y et al (2010) DNMT1 and DNMT3b silencing sensitizes human hepatoma cells to TRAIL-mediated apoptosis via up-regulation of TRAIL-R2/DR5 and caspase-8. Cancer Sci 101:1431–1439

    CAS  PubMed  Google Scholar 

  • Kurman RJ, Shih Ie M (2011) Molecular pathogenesis and extraovarian origin of epithelial ovarian cancer-shifting the paradigm. Hum Pathol 42:918–931

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lancaster JM, Sayer R, Blanchette C et al (2003) High expression of tumor necrosis factor-related apoptosis-inducing ligand is associated with favorable ovarian cancer survival. Clin Cancer Res 9:762–766

    CAS  PubMed  Google Scholar 

  • Lane D, Cote M, Grondin R et al (2006) Acquired resistance to TRAIL-induced apoptosis in human ovarian cancer cells is conferred by increased turnover of mature caspase-3. Mol Cancer Ther 5:509–521

    CAS  PubMed  Google Scholar 

  • Lee CS, Kim YJ, Kim W et al (2011a) Guanylate cyclase activator YC-1 enhances TRAIL-induced apoptosis in human epithelial ovarian carcinoma cells via activation of apoptosis-related proteins. Basic Clin Pharmacol Toxicol 109:283–291

    CAS  PubMed  Google Scholar 

  • Lee JC, Chou LC, Huang CH et al (2011b) CHM-1 induces apoptosis via p38-mediated upregulation of DR5 expression in human ovarian cancer SKOV3 cells. Eur J Pharmacol 670:96–104

    CAS  PubMed  Google Scholar 

  • Lee CS, Jang ER, Kim YJ et al (2012) Diarylheptanoid hirsutenone enhances apoptotic effect of TRAIL on epithelial ovarian carcinoma cell lines via activation of death receptor and mitochondrial pathway. Invest New Drugs 30:548–557

    CAS  PubMed  Google Scholar 

  • Lee JP, Hahn HS, Hwang SJ et al (2013) Selective cyclooxygenase inhibitors increase paclitaxel sensitivity in taxane-resistant ovarian cancer by suppressing P-glycoprotein expression. J Gynecol Oncol 24:273–279

    CAS  PubMed Central  PubMed  Google Scholar 

  • Li H, Cai Q, Godwin AK et al (2010) Enhancer of zeste homolog 2 promotes the proliferation and invasion of epithelial ovarian cancer cells. Mol Cancer Res 8:1610–1618

    CAS  PubMed Central  PubMed  Google Scholar 

  • Li S, Zhang L, Yao Q et al (2013a) Pathogen blocks host death receptor signalling by arginine GlcNAcylation of death domains. Nature 501:242–246

    CAS  PubMed  Google Scholar 

  • Li X, Chen T, Lin S et al (2013b) Valeriana jatamansi constituent IVHD-valtrate as a novel therapeutic agent to human ovarian cancer: in vitro and in vivo activities and mechanisms. Curr Cancer Drug Targets 13:472–483

    CAS  PubMed  Google Scholar 

  • Lin Y, Devin A, Cook A et al (2000) The death domain kinase RIP is essential for TRAIL (Apo2L)-induced activation of IkappaB kinase and c-Jun N-terminal kinase. Mol Cell Biol 20:6638–6645

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lin GT, Tseng HF, Chang CK et al (2008) SNP combinations in chromosome-wide genes are associated with bone mineral density in Taiwanese women. Chin J Physiol 51:32–41

    CAS  PubMed  Google Scholar 

  • Lin GT, Tseng HF, Yang CH et al (2009) Combinational polymorphisms of seven CXCL12-related genes are protective against breast cancer in Taiwan. OMICS 13:165–172

    CAS  PubMed  Google Scholar 

  • Lin T, Chen Y, Ding Z et al (2013) Novel insights into the synergistic interaction of a thioredoxin reductase inhibitor and TRAIL: the activation of the ASK1-ERK-Sp1 pathway. PLoS One 8:e63966

    CAS  PubMed Central  PubMed  Google Scholar 

  • Liu S, Fang Y, Shen H et al (2013) Berberine sensitizes ovarian cancer cells to cisplatin through miR-21/PDCD4 axis. Acta Biochim Biophys Sin 45:756–762

    CAS  PubMed  Google Scholar 

  • Long Q, Xiel Y, Huang Y et al (2013) Induction of apoptosis and inhibition of angiogenesis by PEGylated liposomal quercetin in both cisplatin-sensitive and cisplatin-resistant ovarian cancers. J Biomed Nanotechnol 9:965–975

    CAS  PubMed  Google Scholar 

  • Madsen CV, Dahl Steffensen K, Waldstrom M et al (2012a) Immunohistochemical expression of platelet-derived growth factor receptors in ovarian cancer patients with long-term follow-up. Pathol Res Int 2012:851432

    Google Scholar 

  • Madsen CV, Steffensen KD, Olsen DA et al (2012b) Serial measurements of serum PDGF-AA, PDGF-BB, FGF2, and VEGF in multiresistant ovarian cancer patients treated with bevacizumab. J Ovarian Res 5:23

    CAS  PubMed Central  PubMed  Google Scholar 

  • Madsen CV, Steffensen KD, Olsen DA et al (2012c) Serum platelet-derived growth factor and fibroblast growth factor in patients with benign and malignant ovarian tumors. Anticancer Res 32:3817–3825

    PubMed  Google Scholar 

  • Mandal R, Raab M, Matthess Y et al (2014) pERK 1/2 inhibit Caspase-8 induced apoptosis in cancer cells by phosphorylating it in a cell cycle specific manner. Mol Oncol 8:232–249

    CAS  PubMed  Google Scholar 

  • Matei D, Kelich S, Cao L et al (2007a) PDGF BB induces VEGF secretion in ovarian cancer. Cancer Biol Ther 6:1951–1959

    CAS  PubMed  Google Scholar 

  • Matei D, Satpathy M, Cao L et al (2007b) The platelet-derived growth factor receptor alpha is destabilized by geldanamycins in cancer cells. J Biol Chem 282:445–453

    CAS  PubMed  Google Scholar 

  • Mathey S, Graeser MK, Zu Eulenburg C et al (2013) Platelet-derived growth factor receptor beta serum concentrations during first-line therapy in ovarian cancer. Oncology 85:69–77

    CAS  PubMed  Google Scholar 

  • Matsuo K, Nishimura M, Komurov K et al (2014) Platelet-derived growth factor receptor alpha (PDGFRalpha) targeting and relevant biomarkers in ovarian carcinoma. Gynecol Oncol 132:166–175

    CAS  PubMed  Google Scholar 

  • Mi YY, Li JM, Shao N et al (2011) TRAIL gene polymorphism and genetic susceptibility to prostate cancer in the Chinese Han population of Nanjing. Zhonghua Nan Ke Xue 17:242–246

    CAS  PubMed  Google Scholar 

  • Min KJ, Jang JH, Lee JT et al (2012) Glucocorticoid receptor antagonist sensitizes TRAIL-induced apoptosis in renal carcinoma cells through up-regulation of DR5 and down-regulation of c-FLIP(L) and Bcl-2. J Mol Med 90:309–319

    CAS  PubMed  Google Scholar 

  • Nakano H, Yamada Y, Miyazawa T et al (2013) Gain-of-function microRNA screens identify miR-193a regulating proliferation and apoptosis in epithelial ovarian cancer cells. Int J Oncol 42:1875–1882

    CAS  PubMed Central  PubMed  Google Scholar 

  • Nessa MU, Beale P, Chan C et al (2011) Synergism from combinations of cisplatin and oxaliplatin with quercetin and thymoquinone in human ovarian tumour models. Anticancer Res 31:3789–3797

    CAS  PubMed  Google Scholar 

  • Ning Y, Li Q, Xiang H et al (2012) Apoptosis induced by 7-difluoromethoxyl-5,4′-di-n-octyl genistein via the inactivation of FoxM1 in ovarian cancer cells. Oncol Rep 27:1857–1864

    CAS  PubMed  Google Scholar 

  • Pal R, Gochhait S, Chattopadhyay S et al (2011) Functional implication of TRAIL -716 C/T promoter polymorphism on its in vitro and in vivo expression and the susceptibility to sporadic breast tumor. Breast Cancer Res Treat 126:333–343

    PubMed  Google Scholar 

  • Parajuli B, Shin SJ, Kwon SH et al (2013) Salinomycin induces apoptosis via death receptor-5 up-regulation in cisplatin-resistant ovarian cancer cells. Anticancer Res 33:1457–1462

    CAS  PubMed  Google Scholar 

  • Park SJ, Kim MJ, Kim HB et al (2009) Trichostatin A sensitizes human ovarian cancer cells to TRAIL-induced apoptosis by down-regulation of c-FLIPL via inhibition of EGFR pathway. Biochem Pharmacol 77:1328–1336

    CAS  PubMed  Google Scholar 

  • Pearson JS, Giogha C, Ong SY et al (2013) A type III effector antagonizes death receptor signalling during bacterial gut infection. Nature 501:247–251

    CAS  PubMed  Google Scholar 

  • Petrucci E, Pasquini L, Bernabei M et al (2012) A small molecule SMAC mimic LBW242 potentiates TRAIL- and anticancer drug-mediated cell death of ovarian cancer cells. PLoS One 7:e35073

    CAS  PubMed Central  PubMed  Google Scholar 

  • Prat J (2012) Ovarian carcinomas: five distinct diseases with different origins, genetic alterations, and clinicopathological features. Virchows Arch 460:237–249

    PubMed  Google Scholar 

  • Rocconi RP, Matthews KS, Kimball KJ et al (2008) Expression of c-kit and platelet-derived growth factor receptors in ovarian granulosa cell tumors. Reprod Sci 15:673–677

    PubMed  Google Scholar 

  • Salani R, Neuberger I, Kurman RJ et al (2007) Expression of extracellular matrix proteins in ovarian serous tumors. Int J Gynecol Pathol 26:141–146

    PubMed  Google Scholar 

  • Sarkar S, Faller DV (2013) Telomere-homologous G-rich oligonucleotides sensitize human ovarian cancer cells to TRAIL-induced growth inhibition and apoptosis. Nucleic Acid Ther 23:167–174

    CAS  PubMed Central  PubMed  Google Scholar 

  • Shao M, Rossi S, Chelladurai B et al (2011) PDGF induced microRNA alterations in cancer cells. Nucleic Acids Res 39:4035–4047

    CAS  PubMed Central  PubMed  Google Scholar 

  • Shi J, Zheng D, Liu Y et al (2005) Overexpression of soluble TRAIL induces apoptosis in human lung adenocarcinoma and inhibits growth of tumor xenografts in nude mice. Cancer Res 65:1687–1692

    CAS  PubMed  Google Scholar 

  • Srivastava RK, Kurzrock R, Shankar S (2010) MS-275 sensitizes TRAIL-resistant breast cancer cells, inhibits angiogenesis and metastasis, and reverses epithelial-mesenchymal transition in vivo. Mol Cancer Ther 9:3254–3266

    CAS  PubMed  Google Scholar 

  • Sun C, Li N, Zhou B et al (2013a) miR-222 is upregulated in epithelial ovarian cancer and promotes cell proliferation by downregulating P27. Oncol Lett 6:507–512

    PubMed Central  PubMed  Google Scholar 

  • Sun Y, Mu F, Li C et al (2013b) Aspidin BB, a phloroglucinol derivative, induces cell cycle arrest and apoptosis in human ovarian HO-8910 cells. Chem Biol Interact 204:88–97

    CAS  PubMed  Google Scholar 

  • Sung B, Prasad S, Ravindran J et al (2012) Capsazepine, a TRPV1 antagonist, sensitizes colorectal cancer cells to apoptosis by TRAIL through ROS-JNK-CHOP-mediated upregulation of death receptors. Free Radic Biol Med 53:1977–1987

    CAS  PubMed Central  PubMed  Google Scholar 

  • Syed V, Mukherjee K, Godoy-Tundidor S et al (2007) Progesterone induces apoptosis in TRAIL-resistant ovarian cancer cells by circumventing c-FLIPL overexpression. J Cell Biochem 102:442–452

    CAS  PubMed  Google Scholar 

  • Trauzold A, Siegmund D, Schniewind B et al (2006) TRAIL promotes metastasis of human pancreatic ductal adenocarcinoma. Oncogene 25:7434–7439

    CAS  PubMed  Google Scholar 

  • Volkmann J, Reuning U, Rudelius M et al (2013) High expression of crystallin alphaB represents an independent molecular marker for unfavourable ovarian cancer patient outcome and impairs TRAIL- and cisplatin-induced apoptosis in human ovarian cancer cells. Int J Cancer 132:2820–2832

    CAS  PubMed  Google Scholar 

  • von Pawel J, Harvey JH, Spigel DR et al (2014) Phase II trial of mapatumumab, a fully human agonist monoclonal antibody to tumor necrosis factor-related apoptosis-inducing ligand receptor 1 (TRAIL-R1), in combination with paclitaxel and carboplatin in patients with advanced non-small-cell lung cancer. Clin Lung Cancer 15(188–196):e182

    Google Scholar 

  • Wahl H, Tan L, Griffith K et al (2007) Curcumin enhances Apo2L/TRAIL-induced apoptosis in chemoresistant ovarian cancer cells. Gynecol Oncol 105:104–112

    CAS  PubMed  Google Scholar 

  • Wang Q, Ji Y, Wang X et al (2000) Isolation and molecular characterization of the 5′-upstream region of the human TRAIL gene. Biochem Biophys Res Commun 276:466–471

    CAS  PubMed  Google Scholar 

  • Wang W, Zhao J, Wang H et al (2010a) Programmed cell death 4 (PDCD4) mediates the sensitivity of gastric cancer cells to TRAIL-induced apoptosis by down-regulation of FLIP expression. Exp Cell Res 316:2456–2464

    CAS  PubMed  Google Scholar 

  • Wang WQ, Zhang H, Wang HB et al (2010b) Programmed cell death 4 (PDCD4) enhances the sensitivity of gastric cancer cells to TRAIL-induced apoptosis by inhibiting the PI3K/Akt signaling pathway. Mol Diagn Ther 14:155–161

    CAS  PubMed  Google Scholar 

  • Wang D, Liu D, Gao J et al (2013a) TRAIL-induced miR-146a expression suppresses CXCR4-mediated human breast cancer migration. FEBS J 280:3340–3353

    CAS  PubMed  Google Scholar 

  • Wang P, Chen J, Mu LH et al (2013b) Propofol inhibits invasion and enhances paclitaxel- induced apoptosis in ovarian cancer cells through the suppression of the transcription factor slug. Eur Rev Med Pharmacol Sci 17:1722–1729

    CAS  PubMed  Google Scholar 

  • Wang YQ, Guo RD, Guo RM et al (2013c) MicroRNA-182 promotes cell growth, invasion, and chemoresistance by targeting programmed cell death 4 (PDCD4) in human ovarian carcinomas. J Cell Biochem 114:1464–1473

    CAS  PubMed  Google Scholar 

  • Wang Z, Ting Z, Li Y et al (2013d) microRNA-199a is able to reverse cisplatin resistance in human ovarian cancer cells through the inhibition of mammalian target of rapamycin. Oncol Lett 6:789–794

    CAS  PubMed Central  PubMed  Google Scholar 

  • Weber A, Wandinger KP, Mueller W et al (2004) Identification and functional characterization of a highly polymorphic region in the human TRAIL promoter in multiple sclerosis. J Neuroimmunol 149:195–201

    CAS  PubMed  Google Scholar 

  • Wu SJ, Chuang LY, Lin YD et al (2013) Particle swarm optimization algorithm for analyzing SNP–SNP interaction of renin-angiotensin system genes against hypertension. Mol Biol Rep 40:4227–4233

    CAS  PubMed  Google Scholar 

  • Xiang Y, Ma N, Wang D et al (2014) MiR-152 and miR-185 co-contribute to ovarian cancer cells cisplatin sensitivity by targeting DNMT1 directly: a novel epigenetic therapy independent of decitabine. Oncogene 33:378–386

    CAS  PubMed  Google Scholar 

  • Yamamoto S, Tsuda H, Takano M et al (2008) Expression of platelet-derived growth factors and their receptors in ovarian clear-cell carcinoma and its putative precursors. Mod Pathol 21:115–124

    CAS  PubMed  Google Scholar 

  • Yan X, Xu L, Qi J et al (2009) sTRAIL levels and TRAIL gene polymorphisms in Chinese patients with fatty liver disease. Immunogenetics 61:551–556

    CAS  PubMed  Google Scholar 

  • Yan X, Lyu T, Jia N et al (2013) Huaier aqueous extract inhibits ovarian cancer cell motility via the AKT/GSK3beta/beta-catenin pathway. PLoS ONE 8:e63731

    CAS  PubMed Central  PubMed  Google Scholar 

  • Yang CH, Chuang LY, Chen YJ et al (2011) Computational analysis of simulated SNP interactions between 26 growth factor-related genes in a breast cancer association study. OMICS 15:399–407

    CAS  PubMed  Google Scholar 

  • Yang CH, Chuang LY, Cheng YH et al (2012) Single nucleotide polymorphism barcoding to evaluate oral cancer risk using odds ratio-based genetic algorithms. Kaohsiung J Med Sci 28:362–368

    CAS  PubMed  Google Scholar 

  • Yang CH, Cheng YH, Chuang LY et al (2013a) Drug-SNPing: an integrated drug-based, protein interaction-based tagSNP-based pharmacogenomics platform for SNP genotyping. Bioinformatics 29:758–764

    CAS  PubMed  Google Scholar 

  • Yang CH, Lin YD, Chaung LY et al (2013b) Evaluation of breast cancer susceptibility using improved genetic algorithms in generating genotype SNP barcodes. IEEE/ACM Trans Comput Biol Bioinform 10:361–371

    PubMed  Google Scholar 

  • Yasukagawa T, Niwa Y, Simizu S et al (2012) Suppression of cellular invasion by glybenclamide through inhibited secretion of platelet-derived growth factor in ovarian clear cell carcinoma ES-2 cells. FEBS Lett 586:1504–1509

    CAS  PubMed  Google Scholar 

  • Yaylım İ, Ozkan N, Turan S et al (2012) sTRAIL serum levels and TRAIL 1595 genotypes: associations with progress and prognosis of colorectal carcinoma. J Cancer Ther 3:941–947

    Google Scholar 

  • Ye B, Aponte M, Dai Y et al (2007) Ginkgo biloba and ovarian cancer prevention: epidemiological and biological evidence. Cancer Lett 251:43–52

    CAS  PubMed  Google Scholar 

  • Yen CY, Liu SY, Chen CH et al (2008) Combinational polymorphisms of four DNA repair genes XRCC1, XRCC2, XRCC3, and XRCC4 and their association with oral cancer in Taiwan. J Oral Pathol Med 37:271–277

    CAS  PubMed  Google Scholar 

  • Yildiz Y, Yaylim-Eraltan I, Arikan S et al (2010) Is there any correlation between TNF-related apoptosis-inducing ligand (TRAIL) genetic variants and breast cancer? Arch Med Sci AMS 6:932–936

    CAS  Google Scholar 

  • Yoo NJ, Kim MS, Lee SH (2012) Expression and mutation analyses of Fas, FLIP and Bcl-2 in granulosa cell tumor of ovary. Tumori 98:118e–121e

    PubMed  Google Scholar 

  • Yoo KH, Park JH, Lee DK et al (2013) Pomolic acid induces apoptosis in SK-OV-3 human ovarian adenocarcinoma cells through the mitochondrial-mediated intrinsic and death receptor-induced extrinsic pathways. Oncol Lett 5:386–390

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang X, Wang X, Song X et al (2010) Programmed cell death 4 enhances chemosensitivity of ovarian cancer cells by activating death receptor pathway in vitro and in vivo. Cancer Sci 101:2163–2170

    CAS  PubMed  Google Scholar 

  • Zhang X, Liu P, Zhang B et al (2013) Inhibitory effects of STAT3 decoy oligodeoxynucleotides on human epithelial ovarian cancer cell growth in vivo. Int J Mol Med 32:623–628

    CAS  PubMed  Google Scholar 

  • Zhu H, Liu XW, Ding WJ et al (2010) Up-regulation of death receptor 4 and 5 by celastrol enhances the anti-cancer activity of TRAIL/Apo-2L. Cancer Lett 297:155–164

    CAS  PubMed  Google Scholar 

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Acknowledgments

This work was supported by the funds of the NSC103-2320-B-037-008, the 103CM-KMU-09 the National Sun Yat-sen University-KMU Joint Research Project (#NSYSU-KMU 103-p014), and Health and welfare surcharge of tobacco products, the Ministry of Health and Welfare, Taiwan, Republic of China (MOHW103-TD-B-111-05).

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Authors and Affiliations

  1. Laboratory for Translational Oncology and Personalized Medicine, RLMC, 35 km Ferozepur Road, Lahore, Pakistan

    Ammad Ahmad Farooqi

  2. Department of Molecular Medicine, Institute of Experimental Medicine, Istanbul University, Istanbul, Turkey

    Ilhan Yaylim & Nazlı Ezgi Ozkan

  3. Department of Obstetrics and Gynecology, RLMC, 35 km Ferozepur Road, Lahore, Pakistan

    Farrukh Zaman & Talha Abdul Halim

  4. Institute of Medical Science and Technology, National Sun Yat-Sen University, Kaohsiung, Taiwan

    Hsueh-Wei Chang

  5. Cancer Center, Translational Research Center, Kaohsiung Medical University Hospital, Kaohsiung Medical University, Kaohsiung, Taiwan

    Hsueh-Wei Chang

  6. Department of Biomedical Science and Environmental Biology, Kaohsiung Medical University, Kaohsiung, Taiwan

    Hsueh-Wei Chang

Authors
  1. Ammad Ahmad Farooqi
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  2. Ilhan Yaylim
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  3. Nazlı Ezgi Ozkan
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  4. Farrukh Zaman
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  5. Talha Abdul Halim
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  6. Hsueh-Wei Chang
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Corresponding authors

Correspondence to Ammad Ahmad Farooqi or Hsueh-Wei Chang.

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Farooqi, A.A., Yaylim, I., Ozkan, N.E. et al. Restoring TRAIL Mediated Signaling in Ovarian Cancer Cells. Arch. Immunol. Ther. Exp. 62, 459–474 (2014). https://doi.org/10.1007/s00005-014-0307-9

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  • DOI: https://doi.org/10.1007/s00005-014-0307-9

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