RUNX3 contributes to carboplatin resistance in epithelial ovarian cancer cells

Gynecologic Oncology

Volumn 138, Issue 3, 2015, Pages 647-655

  Barghout, Samir H ^a   Zepeda, Nubia ^a   Vincent, Krista ^a   Azad, Abul K ^a   Xu, Zhihua ^a   Yang, Christine ^a   Steed, Helen ^a   Postovit, Lynne Marie ^a   Fu, Yangxin ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Carboplatin; Chemoresistance; cIAP2; Epithelial ovarian cancer; RUNX3

Indexed keywords

CARBOPLATIN; CISPLATIN; INHIBITOR OF APOPTOSIS PROTEIN 2; TRANSCRIPTION FACTOR RUNX3; ANTINEOPLASTIC AGENT; BIRC3 PROTEIN, HUMAN; INHIBITOR OF APOPTOSIS PROTEIN; RUNX3 PROTEIN, HUMAN; UBIQUITIN PROTEIN LIGASE;

APOPTOSIS; ARTICLE; BASAL CELL CARCINOMA; CANCER CELL; CANCER RESISTANCE; CONTROLLED STUDY; DRUG MECHANISM; ENDOTHELIUM CELL; GENE OVEREXPRESSION; HEK293 CELL LINE; HUMAN; HUMAN CELL; HUMAN TISSUE; IC50; OVARY CARCINOMA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; REVERSE TRANSCRIPTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; BIOSYNTHESIS; DRUG RESISTANCE; GENE SILENCING; GENETICS; METABOLISM; NEOPLASMS, GLANDULAR AND EPITHELIAL; OVARIAN NEOPLASMS; TUMOR CELL LINE;

ANTINEOPLASTIC AGENTS; CARBOPLATIN; CELL LINE, TUMOR; CORE BINDING FACTOR ALPHA 3 SUBUNIT; DRUG RESISTANCE, NEOPLASM; GENE KNOCKDOWN TECHNIQUES; HUMANS; INHIBITOR OF APOPTOSIS PROTEINS; NEOPLASMS, GLANDULAR AND EPITHELIAL; OVARIAN NEOPLASMS; UBIQUITIN-PROTEIN LIGASES;

EID: 84941365721     PISSN: 00908258     EISSN: 10956859     Source Type: Journal    
DOI: 10.1016/j.ygyno.2015.07.009     Document Type: Article

References (40)

1. R.L. Siegel, K.D. Miller, and A. Jemal Cancer statistics, 2015 CA Cancer J. Clin. 65 2015 5 29
2. N. Auersperg, A.S. Wong, K.C. Choi, S.K. Kang, and P.C. Leung Ovarian surface epithelium: biology, endocrinology, and pathology Endocr. Rev. 22 2001 255 288
3. K. Levanon, C. Crum, and R. Drapkin New insights into the pathogenesis of serous ovarian cancer and its clinical impact J. Clin. Oncol. 26 2008 5284 5293
4. T.A. Yap, C.P. Carden, and S.B. Kaye Beyond chemotherapy: targeted therapies in ovarian cancer Nat. Rev. Cancer 9 2009 167 181
5. S. Vaughan, J.I. Coward, R.C. Bast Jr., A. Berchuck, J.S. Berek, J.D. Brenton, G. Coukos, C.C. Crum, R. Drapkin, D. Etemadmoghadam, M. Friedlander, H. Gabra, S.B. Kaye, C.J. Lord, E. Lengyel, D.A. Levine, I.A. McNeish, U. Menon, G.B. Mills, K.P. Nephew, A.M. Oza, A.K. Sood, E.A. Stronach, H. Walczak, D.D. Bowtell, and F.R. Balkwill Rethinking ovarian cancer: recommendations for improving outcomes Nat. Rev. Cancer 11 2011 719 725
6. L. Kelland The resurgence of platinum-based cancer chemotherapy Nat. Rev. Cancer 7 2007 573 584
7. Z.H. Siddik Cisplatin: mode of cytotoxic action and molecular basis of resistance Oncogene 22 2003 7265 7279
8. L. Galluzzi, L. Senovilla, I. Vitale, J. Michels, I. Martins, O. Kepp, M. Castedo, and G. Kroemer Molecular mechanisms of cisplatin resistance Oncogene 31 2012 1869 1883
9. Y. Ito, S.C. Bae, and L.S. Chuang The RUNX family: developmental regulators in cancer Nat. Rev. Cancer 15 2015 81 95
10. G. Huang, K. Shigesada, K. Ito, H.J. Wee, T. Yokomizo, and Y. Ito Dimerization with PEBP2beta protects RUNX1/AML1 from ubiquitin-proteasome-mediated degradation EMBO J. 20 2001 723 733
11. Q.L. Li, K. Ito, C. Sakakura, H. Fukamachi, K. Inoue, X.Z. Chi, K.Y. Lee, S. Nomura, C.W. Lee, S.B. Han, H.M. Kim, W.J. Kim, H. Yamamoto, N. Yamashita, T. Yano, T. Ikeda, S. Itohara, J. Inazawa, T. Abe, A. Hagiwara, H. Yamagishi, A. Ooe, A. Kaneda, T. Sugimura, T. Ushijima, S.C. Bae, and Y. Ito Causal relationship between the loss of RUNX3 expression and gastric cancer Cell 109 2002 113 124
12. M.M. Subramaniam, J.Y. Chan, K.G. Yeoh, T. Quek, K. Ito, and M. Salto-Tellez Molecular pathology of RUNX3 in human carcinogenesis Biochim. Biophys. Acta 1796 2009 315 331
13. M. Salto-Tellez, B.K. Peh, K. Ito, S.H. Tan, P.Y. Chong, H.C. Han, K. Tada, W.Y. Ong, R. Soong, D.C. Voon, and Y. Ito RUNX3 protein is overexpressed in human basal cell carcinomas Oncogene 25 2006 7646 7649
14. T. Tsunematsu, Y. Kudo, S. Iizuka, I. Ogawa, T. Fujita, H. Kurihara, Y. Abiko, and T. Takata RUNX3 has an oncogenic role in head and neck cancer PLoS One 4 2009 e5892
15. N.S. Nevadunsky, J.S. Barbieri, J. Kwong, M.A. Merritt, W.R. Welch, R.S. Berkowitz, and S.C. Mok RUNX3 protein is overexpressed in human epithelial ovarian cancer Gynecol. Oncol. 112 2009 325 330
16. C.W. Lee, L.S. Chuang, S. Kimura, S.K. Lai, C.W. Ong, B. Yan, M. Salto-Tellez, M. Choolani, and Y. Ito RUNX3 functions as an oncogene in ovarian cancer Gynecol. Oncol. 122 2011 410 417
17. M. Keita, M. Bachvarova, C. Morin, M. Plante, J. Gregoire, M.C. Renaud, A. Sebastianelli, X.B. Trinh, and D. Bachvarov The RUNX1 transcription factor is expressed in serous epithelial ovarian carcinoma and contributes to cell proliferation, migration and invasion Cell Cycle 12 2013 972 986
18. Z.Q. Wang, M. Keita, M. Bachvarova, S. Gobeil, C. Morin, M. Plante, J. Gregoire, M.C. Renaud, A. Sebastianelli, X.B. Trinh, and D. Bachvarov Inhibition of RUNX2 transcriptional activity blocks the proliferation, migration and invasion of epithelial ovarian carcinoma cells PLoS One 8 2013 e74384
19. A.H. Greer, T. Yong, K. Fennell, Y.W. Moustafa, M. Fowler, F. Galiano, S.W. Ng, R.S. Berkowitz, J. Cardelli, S. Meyers, and J.N. Davis Knockdown of core binding factorbeta alters sphingolipid metabolism J. Cell. Physiol. 228 2013 2350 2364
20. N. Xu, C. Shen, Y. Luo, L. Xia, F. Xue, Q. Xia, and J. Zhang Upregulated miR-130a increases drug resistance by regulating RUNX3 and Wnt signaling in cisplatin-treated HCC cell Biochem. Biophys. Res. Commun. 425 2012 468 472
21. Y. Zhang, Q. Lu, and X. Cai MicroRNA-106a induces multidrug resistance in gastric cancer by targeting RUNX3 FEBS Lett. 587 2013 3069 3075
22. Y. Zheng, R. Wang, H.Z. Song, B.Z. Pan, Y.W. Zhang, and L.B. Chen Epigenetic downregulation of RUNX3 by DNA methylation induces docetaxel chemoresistance in human lung adenocarcinoma cells by activation of the AKT pathway Int. J. Biochem. Cell Biol. 45 2013 2369 2378
23. B.C. Behrens, T.C. Hamilton, H. Masuda, K.R. Grotzinger, J. Whang-Peng, K.G. Louie, T. Knutsen, W.M. McKoy, R.C. Young, and R.F. Ozols Characterization of a cis-diamminedichloroplatinum(II)-resistant human ovarian cancer cell line and its use in evaluation of platinum analogues Cancer Res. 47 1987 414 418
24. T.G. Shepherd, B.L. Theriault, E.J. Campbell, and M.W. Nachtigal Primary culture of ovarian surface epithelial cells and ascites-derived ovarian cancer cells from patients Nat. Protoc. 1 2006 2643 2649
25. Y. Fu, A.C. Chang, M. Fournier, L. Chang, K. Niessen, and A. Karsan RUNX3 maintains the mesenchymal phenotype after termination of the Notch signal J. Biol. Chem. 286 2011 11803 11813
26. K. Ito, Q. Liu, M. Salto-Tellez, T. Yano, K. Tada, H. Ida, C. Huang, N. Shah, M. Inoue, A. Rajnakova, K.C. Hiong, B.K. Peh, H.C. Han, T. Ito, M. Teh, K.G. Yeoh, and Y. Ito RUNX3, a novel tumor suppressor, is frequently inactivated in gastric cancer by protein mislocalization Cancer Res. 65 2005 7743 7750
27. T. Yano, K. Ito, H. Fukamachi, X.Z. Chi, H.J. Wee, K. Inoue, H. Ida, P. Bouillet, A. Strasser, S.C. Bae, and Y. Ito The RUNX3 tumor suppressor upregulates Bim in gastric epithelial cells undergoing transforming growth factor beta-induced apoptosis Mol. Cell. Biol. 26 2006 4474 4488
28. N. Gupta, Z. Xu, A. El-Sehemy, H. Steed, and Y. Fu Notch3 induces epithelial-mesenchymal transition and attenuates carboplatin-induced apoptosis in ovarian cancer cells Gynecol. Oncol. 130 2013 200 206
29. N.A. Franken, H.M. Rodermond, J. Stap, J. Haveman, and C. van Bree Clonogenic assay of cells in vitro Nat. Protoc. 1 2006 2315 2319
30. A. Munshi, M. Hobbs, and R.E. Meyn Clonogenic cell survival assay Methods Mol. Med. 110 2005 21 28
31. Y. Fu, A. Chang, L. Chang, K. Niessen, S. Eapen, A. Setiadi, and A. Karsan Differential regulation of transforming growth factor beta signaling pathways by Notch in human endothelial cells J. Biol. Chem. 284 2009 19452 19462
32. Y. Fu, H. Sies, and X.G. Lei Opposite roles of selenium-dependent glutathione peroxidase-1 in superoxide generator diquat- and peroxynitrite-induced apoptosis and signaling J. Biol. Chem. 276 2001 43004 43009
33. R.F. Ozols, B.N. Bundy, B.E. Greer, J.M. Fowler, D. Clarke-Pearson, R.A. Burger, R.S. Mannel, K. DeGeest, E.M. Hartenbach, and R. Baergen Phase III trial of carboplatin and paclitaxel compared with cisplatin and paclitaxel in patients with optimally resected stage III ovarian cancer: a Gynecologic Oncology Group study J. Clin. Oncol. 21 2003 3194 3200
34. A.D. Schimmer Inhibitor of apoptosis proteins: translating basic knowledge into clinical practice Cancer Res. 64 2004 7183 7190
35. L. Farrand, S. Byun, J.Y. Kim, A. Im-Aram, J. Lee, S. Lim, K.W. Lee, J.Y. Suh, H.J. Lee, and B.K. Tsang 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 2013 23740 23750
36. L. Farrand, J.Y. Kim, S. Byun, A. Im-Aram, J. Lee, J.Y. Suh, K.W. Lee, H.J. Lee, and B.K. Tsang The diarylheptanoid hirsutenone sensitizes chemoresistant ovarian cancer cells to cisplatin via modulation of apoptosis-inducing factor and X-linked inhibitor of apoptosis J. Biol. Chem. 289 2014 1723 1731
37. T. Nomura, M. Yamasaki, Y. Nomura, and H. Mimata Expression of the inhibitors of apoptosis proteins in cisplatin-resistant prostate cancer cells Oncol. Rep. 14 2005 993 997
38. H.H. Wu, J.Y. Wu, Y.W. Cheng, C.Y. Chen, M.C. Lee, Y.G. Goan, and H. Lee cIAP2 upregulated by E6 oncoprotein via epidermal growth factor receptor/phosphatidylinositol 3-kinase/AKT pathway confers resistance to cisplatin in human papillomavirus 16/18-infected lung cancer Clin. Cancer Res. 16 2010 5200 5210
39. C. Zeng, S. Vangveravong, J.E. McDunn, W.G. Hawkins, and R.H. Mach Sigma-2 receptor ligand as a novel method for delivering a SMAC mimetic drug for treating ovarian cancer Br. J. Cancer 109 2013 2368 2377
40. F.S. Collins, and H. Varmus A new initiative on precision medicine N. Engl. J. Med. 372 2015 793 795