Sequential treatment with AT-101 enhances cisplatin chemosensitivity in human non-small cell lung cancer cells through inhibition of apurinic/apyrimidinic endonuclease 1-activated IL-6/STAT3 signaling pathway

References

• Siegel R Ma J Zou Z Jemal A Cancer statistics, 2014 CA Cancer J Clin 2014 64 1 9 29 24399786
   PubMed Web of Science ®Google Scholar
• Chen W Zheng R Zhang S The incidences and mortalities of major cancers in China, 2009 Chin J Cancer 2013 32 3 106 112 23452393
   PubMedGoogle Scholar
• DeSantis CE Lin CC Mariotto AB Cancer treatment and survivorship statistics, 2014 CA Cancer J Clin 2014 64 4 252 271 24890451
   PubMed Web of Science ®Google Scholar
• Maccio A Madeddu C Cisplatin: an old drug with a newfound efficacy – from mechanisms of action to cytotoxicity Expert Opin Pharmacother 2013 14 13 1839 1857 23876094
   PubMed Web of Science ®Google Scholar
• O’Shea JJ Holland SM Staudt LM JAKs and STATs in immunity, immunodeficiency, and cancer N Engl J Med 2013 368 2 161 170 23301733
   PubMed Web of Science ®Google Scholar
• Yu H Jove R The STATs of cancer – new molecular targets come of age Nat Rev Cancer 2004 4 2 97 105 14964307
   PubMed Web of Science ®Google Scholar
• Huang S Chen M Shen Y Inhibition of activated Stat3 reverses drug resistance to chemotherapeutic agents in gastric cancer cells Cancer Lett 2012 315 2 198 205 22104727
   PubMed Web of Science ®Google Scholar
• Han Z Feng J Hong Z Silencing of the STAT3 signaling pathway reverses the inherent and induced chemoresistance of human ovarian cancer cells Biochem Biophys Res Commun 2013 435 2 188 194 23665025
   PubMed Web of Science ®Google Scholar
• Lo HW Cao X Zhu H Ali-Osman F Constitutively activated STAT3 frequently coexpresses with epidermal growth factor receptor in high-grade gliomas and targeting STAT3 sensitizes them to Iressa and alkylators Clin Cancer Res 2008 14 19 6042 6054 18829483
   PubMed Web of Science ®Google Scholar
• Yue P Zhang X Paladino D Hyperactive EGF receptor, Jaks and Stat3 signaling promote enhanced colony-forming ability, motility and migration of cisplatin-resistant ovarian cancer cells Oncogene 2012 31 18 2309 2322 21909139
   PubMed Web of Science ®Google Scholar
• Siveen KS Sikka S Surana R Targeting the STAT3 signaling pathway in cancer: role of synthetic and natural inhibitors Biochim Biophys Acta 2014 1845 2 136 154 24388873
   PubMed Web of Science ®Google Scholar
• Bhakat KK Mantha AK Mitra S Transcriptional regulatory functions of mammalian AP-endonuclease (APE1/Ref-1), an essential multifunctional protein Antioxid Redox Signal 2009 11 3 621 638 18715144
   PubMed Web of Science ®Google Scholar
• Abbotts R Madhusudan S Human AP endonuclease 1 (APE1): from mechanistic insights to druggable target in cancer Cancer Treat Rev 2010 36 5 425 435 20056333
   PubMed Web of Science ®Google Scholar
• Busso CS Lake MW Izumi T Posttranslational modification of mammalian AP endonuclease (APE1) Cell Mol Life Sci 2010 67 21 3609 3620 20711647
   PubMed Web of Science ®Google Scholar
• Kelley MR Georgiadis MM Fishel ML APE1/Ref-1 role in redox signaling: translational applications of targeting the redox function of the DNA repair/redox protein APE1/Ref-1 Curr Mol Pharmacol 2012 5 1 36 53 22122463
   PubMedGoogle Scholar
• Xanthoudakis S Smeyne RJ Wallace JD Curran T The redox/DNA repair protein, Ref-1, is essential for early embryonic development in mice Proc Natl Acad Sci U S A 1996 93 17 8919 8923 8799128
   PubMed Web of Science ®Google Scholar
• Meira LB Devaraj S Kisby GE Heterozygosity for the mouse Apex gene results in phenotypes associated with oxidative stress Cancer Res 2001 61 14 5552 5557 11454706
   PubMed Web of Science ®Google Scholar
• Al-Safi RI Odde S Shabaik Y Neamati N Small-molecule inhibitors of APE1 DNA repair function: an overview Curr Mol Pharmacol 2012 5 1 14 35 22122462
   PubMedGoogle Scholar
• Wang D Xiang DB Yang XQ APE1 overexpression is associated with cisplatin resistance in non-small cell lung cancer and targeted inhibition of APE1 enhances the activity of cisplatin in A549 cells Lung Cancer 2009 66 3 298 304 19324449
   PubMed Web of Science ®Google Scholar
• Imai A Zeitlin BD Visioli F Metronomic dosing of BH3 mimetic small molecule yields robust antiangiogenic and antitumor effects Cancer Res 2012 72 3 716 725 22158856
   PubMed Web of Science ®Google Scholar
• Loberg RD McGregor N Ying C Sargent E Pienta KJ In vivo evaluation of AT-101 (R-(-)-gossypol acetic acid) in androgen-independent growth of VCaP prostate cancer cells in combination with surgical castration Neoplasia 2007 9 12 1030 1037 18084610
   PubMed Web of Science ®Google Scholar
• Ko CH Shen SC Yang LY Lin CW Chen YC Gossypol reduction of tumor growth through ROS-dependent mitochondria pathway in human colorectal carcinoma cells Int J Cancer 2007 121 8 1670 1679 17597109
   PubMed Web of Science ®Google Scholar
• Pang X Wu Y Wu Y (-)-Gossypol suppresses the growth of human prostate cancer xenografts via modulating VEGF signaling-mediated angiogenesis Mol Cancer Ther 2011 10 5 795 805 21372225
   PubMed Web of Science ®Google Scholar
• Karaca B Atmaca H Bozkurt E Combination of AT-101/cisplatin overcomes chemoresistance by inducing apoptosis and modulating epigenetics in human ovarian cancer cells Mol Biol Rep 2013 40 6 3925 3933 23269627
   PubMed Web of Science ®Google Scholar
• Schelman WR Mohammed TA Traynor AM A phase I study of AT-101 with cisplatin and etoposide in patients with advanced solid tumors with an expanded cohort in extensive-stage small cell lung cancer Invest New Drugs 2014 32 2 295 302 23860642
   PubMed Web of Science ®Google Scholar
• Qian C Li M Sui J Identification of a novel potential antitumor activity of gossypol as an APE1/Ref-1 inhibitor Drug Des Devel Ther 2014 8 485 496
   PubMed Web of Science ®Google Scholar
• Baggstrom MQ Qi Y Koczywas M A phase II study of AT-101 (Gossypol) in chemotherapy-sensitive recurrent extensive-stage small cell lung cancer J Thorac Oncol 2011 6 10 1757 1760 21918390
   PubMed Web of Science ®Google Scholar
• Sonpavde G Matveev V Burke JM Randomized phase II trial of docetaxel plus prednisone in combination with placebo or AT-101, an oral small molecule Bcl-2 family antagonist, as first-line therapy for metastatic castration-resistant prostate cancer Ann Oncol 2012 23 7 1803 1808 22112969
   PubMed Web of Science ®Google Scholar
• Lee MJ Ye AS Gardino AK Sequential application of anticancer drugs enhances cell death by rewiring apoptotic signaling networks Cell 2012 149 4 780 794 22579283
   PubMed Web of Science ®Google Scholar
• Ren T Qing Y Dai N Apurinic/apyrimidinic endonuclease 1 induced upregulation of fibroblast growth factor 2 and its receptor 3 induces angiogenesis in human osteosarcoma cells Cancer Sci 2014 105 2 186 194 24329908
   PubMed Web of Science ®Google Scholar
• Cardoso AA Jiang Y Luo M APE1/Ref-1 regulates STAT3 transcriptional activity and APE1/Ref-1-STAT3 dual-targeting effectively inhibits pancreatic cancer cell survival PLoS One 2012 7 10 e47462 23094050
   PubMed Web of Science ®Google Scholar
• Huang YW Wang LS Dowd MK Wan PJ Lin YC (–)-Gossypol reduces invasiveness in metastatic prostate cancer cells Anticancer Res 2009 29 6 2179 2188 19528479
   PubMed Web of Science ®Google Scholar
• Huang YW Wang LS Chang HL Molecular mechanisms of (–)-gossypol-induced apoptosis in human prostate cancer cells Anticancer Res 2006 26 3A 1925 1933 16827126
   PubMed Web of Science ®Google Scholar
• Jiang J Slivova V Jedinak A Sliva D Gossypol inhibits growth, invasiveness, and angiogenesis in human prostate cancer cells by modulating NF-κB/AP-1 dependent- and independent-signaling Clin Exp Metastasis 2012 29 2 165 178 22167622
   PubMed Web of Science ®Google Scholar
• Hsiao WT Tsai MD Jow GM Tien LT Lee YJ Involvement of Smac, p53, and caspase pathways in induction of apoptosis by gossypol in human retinoblastoma cells Mol Vis 2012 18 2033 2042 22876131
   PubMed Web of Science ®Google Scholar
• Volate SR Kawasaki BT Hurt EM Gossypol induces apoptosis by activating p53 in prostate cancer cells and prostate tumor-initiating cells Mol Cancer Ther 2010 9 2 461 470 20124455
   PubMed Web of Science ®Google Scholar
• Xu L Yang D Wang S (–)-Gossypol enhances response to radiation therapy and results in tumor regression of human prostate cancer Mol Cancer Ther 2005 4 2 197 205 15713891
   PubMed Web of Science ®Google Scholar
• Balakrishnan K Burger JA Wierda WG Gandhi V AT-101 induces apoptosis in CLL B cells and overcomes stromal cell-mediated Mcl-1 induction and drug resistance Blood 2009 113 1 149 153 18836097
   PubMed Web of Science ®Google Scholar
• Zerp SF Stoter R Kuipers G AT-101, a small molecule inhibitor of anti-apoptotic Bcl-2 family members, activates the SAPK/JNK pathway and enhances radiation-induced apoptosis Radiat Oncol 2009 4 47 19852810
   PubMed Web of Science ®Google Scholar
• Moretti L Li B Kim KW Chen H Lu B AT-101, a pan-Bcl-2 inhibitor, leads to radiosensitization of non-small cell lung cancer J Thorac Oncol 2010 5 5 680 687 20354451
   PubMed Web of Science ®Google Scholar
• McGregor N Patel L Craig M Weidner S Wang S Pienta KJ AT-101 (R-(–)-gossypol acetic acid) enhances the effectiveness of androgen deprivation therapy in the VCaP prostate cancer model J Cell Biochem 2010 110 5 1187 1194 20589722
   PubMed Web of Science ®Google Scholar
• Hu W Wang F Tang J Proapoptotic protein Smac mediates apoptosis in cisplatin-resistant ovarian cancer cells when treated with the anti-tumor agent AT101 J Biol Chem 2012 287 1 68 80 22052903
   PubMed Web of Science ®Google Scholar
• Kisim A Atmaca H Cakar B Pretreatment with AT-101 enhances tumor necrosis factor-related apoptosis-inducing ligand (TRAIL)-induced apoptosis of breast cancer cells by inducing death receptors 4 and 5 protein levels J Cancer Res Clin Oncol 2012 138 7 1155 1163 22411600
   PubMed Web of Science ®Google Scholar
• Billard C Development of Noxa-like BH3 mimetics for apoptosis-based therapeutic strategy in chronic lymphocytic leukemia Mol Cancer Res 2012 10 6 673 676 22466256
   PubMed Web of Science ®Google Scholar
• Thakur A Lum LG Schalk D Pan-Bcl-2 inhibitor AT-101 enhances tumor cell killing by EGFR targeted T cells PLoS One 2012 7 11 e47520 23185240
   PubMed Web of Science ®Google Scholar
• Ikuta K Takemura K Kihara M Overexpression of constitutive signal transducer and activator of transcription 3 mRNA in cisplatin-resistant human non-small cell lung cancer cells Oncol Rep 2005 13 2 217 222 15643501
   PubMed Web of Science ®Google Scholar
• Kulesza DW Carré T Chouaib S Kaminska B Silencing of the transcription factor STAT3 sensitizes lung cancer cells to DNA damaging drugs, but not to TNFα- and NK cytotoxicity Exp Cell Res 2013 319 4 506 516 23149124
   PubMed Web of Science ®Google Scholar
• Tezcanli Kaymaz B Bozok Cetintas V Eroglu Z Kosova B Suppression of STAT3 by chemically modified siRNAs increases the chemotherapeutic sensitivity of parental and cisplatin-resistant non-small cell lung cancer cells J BUON 2014 19 1 145 152 24659656
   PubMed Web of Science ®Google Scholar
• Akagunduz O Karaca B Atmaca H Radiosensitization of hormone-refractory prostate cancer cells by gossypol treatment J BUON 2010 15 4 763 767 21229643
   PubMed Web of Science ®Google Scholar
• Galluzzi L Senovilla L Vitale I Molecular mechanisms of cisplatin resistance Oncogene 2012 31 15 1869 1883 21892204
   PubMed Web of Science ®Google Scholar
• Koberle B Tomicic MT Usanova S Kaina B Cisplatin resistance: preclinical findings and clinical implications Biochim Biophys Acta 2010 1806 2 172 182 20647037
   PubMed Web of Science ®Google Scholar
• Galluzzi L Vitale I Michels J Systems biology of cisplatin resistance: past, present and future Cell Death Dis 2014 5 e1257 24874729
   PubMed Web of Science ®Google Scholar
• Rabik CA Dolan ME Molecular mechanisms of resistance and toxicity associated with platinating agents Cancer Treat Rev 2007 33 1 9 23 17084534
   PubMed Web of Science ®Google Scholar
• Martin LP Hamilton TC Schilder RJ Platinum resistance: the role of DNA repair pathways Clin Cancer Res 2008 14 5 1291 1295 18316546
   PubMed Web of Science ®Google Scholar
• Sugimura K Miyata H Tanaka K Let-7 expression is a significant determinant of response to chemotherapy through the regulation of IL-6/STAT3 pathway in esophageal squamous cell carcinoma Clin Cancer Res 2012 18 18 5144 5153 22847808
   PubMed Web of Science ®Google Scholar
• Deng S Yuan H Yi J Gossypol acetic acid induces apoptosis in RAW264.7 cells via a caspase-dependent mitochondrial signaling pathway J Vet Sci 2013 14 3 281 289 23820203
   PubMed Web of Science ®Google Scholar
• Li G Liu L Shan C RhoA/ROCK/PTEN signaling is involved in AT-101-mediated apoptosis in human leukemia cells in vitro and in vivo Cell Death Dis 2014 5 e998 24434521
   PubMed Web of Science ®Google Scholar
• Sahin O Wang Q Brady SW Biomarker-guided sequential targeted therapies to overcome therapy resistance in rapidly evolving highly aggressive mammary tumors Cell Res 2014 24 5 542 559 24675532
   PubMed Web of Science ®Google Scholar
• Saiyin W Wang D Li L Sequential release of autophagy inhibitor and chemotherapeutic drug with polymeric delivery system for oral squamous cell carcinoma therapy Mol Pharm 2014 11 5 1662 1675 24666011
   PubMed Web of Science ®Google Scholar
• Janes KA Reinhardt HC Yaffe MB Cytokine-induced signaling networks prioritize dynamic range over signal strength Cell 2008 135 2 343 354 18957207
   PubMed Web of Science ®Google Scholar