Indirect modulation of sensitivity to 5-fluorouracil by microRNA-96 in human colorectal cancer cells

Archives of Pharmacal Research

Volumn 38, Issue 2, 2015, Pages 239-248

  Kim, Sun Ah ^a   Kim, Injung ^a   Yoon, Sungjoo Kim ^a   Lee, Eun Kyung ^a   Kuh, Hyo Jeong ^a  

^a The Catholic University of Korea   (South Korea)

Author keywords

5 FU; Apoptosis; Drug resistance; MicroRNA 96; UBE2N; XIAP

Indexed keywords

FLUOROURACIL; MICRORNA; MICRORNA 96; PROTEIN MDM2; PROTEIN P53; TRANSCRIPTION FACTOR FKHRL1; UBIQUITIN CONJUGATING ENZYME E2; UNCLASSIFIED DRUG; X LINKED INHIBITOR OF APOPTOSIS; ANTINEOPLASTIC ANTIMETABOLITE; MIRN96 MICRORNA, HUMAN; UBE2N PROTEIN, HUMAN; UBIQUITIN CONJUGATING ENZYME; XIAP PROTEIN, HUMAN;

APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CANCER INHIBITION; CANCER RESISTANCE; CELL PROLIFERATION; CHEMOSENSITIVITY; COLORECTAL CANCER; COLORECTAL CANCER CELL LINE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DLD 1 CELL LINE; DOWN REGULATION; DRUG EXPOSURE; DRUG MECHANISM; DRUG SENSITIVITY; DRUG TARGETING; GENE INTERACTION; GENE OVEREXPRESSION; GENETIC TRANSFECTION; HCT116 CELL LINE; HT 29 CELL LINE; HUMAN; HUMAN CELL; LUCIFERASE ASSAY; MONOLAYER CULTURE; SIGNAL TRANSDUCTION; TUMOR SPHEROID; UPREGULATION; ANTAGONISTS AND INHIBITORS; CULTURE TECHNIQUE; DRUG EFFECTS; DRUG RESISTANCE; GENETICS; MULTICELLULAR SPHEROID; PATHOLOGY;

ANTIMETABOLITES, ANTINEOPLASTIC; APOPTOSIS; CELL CULTURE TECHNIQUES; DRUG RESISTANCE, NEOPLASM; FLUOROURACIL; HCT116 CELLS; HT29 CELLS; HUMANS; MICRORNAS; SPHEROIDS, CELLULAR; TRANSFECTION; UBIQUITIN-CONJUGATING ENZYMES; UP-REGULATION; X-LINKED INHIBITOR OF APOPTOSIS PROTEIN;

EID: 84925514234     PISSN: 02536269     EISSN: 19763786     Source Type: Journal    
DOI: 10.1007/s12272-014-0528-9     Document Type: Article

References (44)

1. Arlt, A., S.S. Muerkoster, and H. Schafer. 2013. Targeting apoptosis pathways in pancreatic cancer. Cancer Letters 332: 346-358.
2. Broker, L.E., F.A. Kruyt, and G. Giaccone. 2005. Cell death independent of caspase: A review. Clinical Cancer Research 11: 3155-3162.
3. Chen, R.X., Y.H. Xia, T.C. Xue, and S.L. Ye. 2012. Suppression of microRNA-96 expression inhibits the invasion of hepatocellular carcinoma cells. Molecular Medicine Reports 5: 800-804.
4. Cheng, J., Y.H. Fan, X. Xu, H. Zhang, J. Dou, Y. Tang, X. Zhong, Y. Rojas, Y. Yu, Y. Zhao, S.A. Vasudevan, H. Zhang, J.G. Nuchtern, E.S. Kim, X. Chen, F. Lu, and J. Yang. 2014. A small-molecule inhibitor of UBE2N induces neuroblastoma cell death via activation of p53 and JNK pathways. Cell Death and Disease 5: e1079.
5. Croce, C.M. 2009. Causes and consequences of microRNA dysregulation in cancer. Nature Reviews Genetics 10: 704-714.
6. Eckelman, B.P., G.S. Salvesen, and F.L. Scott. 2006. Human inhibitor of apoptosis proteins: Why XIAP is the black sheep of the family. EMBO Reports 7: 988-994.
7. Feng, J., J. Yu, X. Pan, Z. Li, Z. Chen, W. Zhang, B. Wang, L. Yang, H. Xu, G. Zhang, and Z. Xu. 2014. HERG1 functions as an oncogene in pancreatic cancer and is downregulated by miR-96. Oncotarget 5: 5832-5844.
8. Friedrich, J., W. Eder, J. Castaneda, M. Doss, E. Huber, R. Ebner, and L.A. Kunz-Schughart. 2007. A reliable tool to determine cell viability in complex 3-d culture: The acid phosphatase assay. Journal of Biomolecular Screening 12: 925-937.
9. Guo, Y., H. Liu, H. Zhang, C. Shang, and Y. Song. 2012. miR-96 regulates FOXO1-mediated cell apoptosis in bladder cancer. Oncology Letters 4: 561-565.
10. Guttilla, I.K., and B.A. White. 2009. Coordinate regulation of FOXO1 by miR-27a, miR-96, and miR-182 in breast cancer cells. Journal of Biological Chemistry 284: 23204-23216.
11. Haflidadottir, B.S., O. Larne, M. Martin, M. Persson, A. Edsjo, A. Bjartell, and Y. Ceder. 2013. Upregulation of miR-96 enhances cellular proliferation of prostate cancer cells through FOXO1. PLoS One 8: e72400.
12. Hamfjord, J., A.M. Stangeland, T. Hughes, M.L. Skrede, K.M. Tveit, T. Ikdahl, and E.H. Kure. 2012. Differential expression of miRNAs in colorectal cancer: Comparison of paired tumor tissue and adjacent normal mucosa using high-throughput sequencing. PLoS One 7: e34150.
13. Hicks, K.O., F.B. Pruijn, T.W. Secomb, M.P. Hay, R. Hsu, J.M. Brown, W.A. Denny, M.W. Dewhirst, and W.R. Wilson. 2006. Use of three-dimensional tissue cultures to model extravascular transport and predict in vivo activity of hypoxia-targeted anticancer drugs. Journal of the National Cancer Institute 98: 1118-1128.
14. Karasawa, H., K. Miura, W. Fujibuchi, K. Ishida, N. Kaneko, M. Kinouchi, M. Okabe, T. Ando, Y. Murata, H. Sasaki, K. Takami, A. Yamamura, C. Shibata, and I. Sasaki. 2009. Down-regulation of cIAP2 enhances 5-FU sensitivity through the apoptotic pathway in human colon cancer cells. Cancer Science 100: 903-913.
15. Kashkar, H. 2010. X-linked inhibitor of apoptosis: A chemoresistance factor or a hollow promise. Clinical Cancer Research 16: 4496-4502.
16. Kim, S.H., S.J. Choi, Y.C. Kim, and H.J. Kuh. 2009. Anti-tumor activity of noble indirubin derivatives in human solid tumor models in vitro. Arch Pharm Res 32: 915-922.
17. Kobayashi, H., S. Man, C.H. Graham, S.J. Kapitain, B.A. Teicher, and R.S. Kerbel. 1993. Acquired multicellular-mediated resistance to alkylating agents in cancer. Proceedings of the National Academy of Sciences of the United States of America 90: 3294-8.
18. Laine, A., I. Topisirovic, D. Zhai, J.C. Reed, K.L. Borden, and Z. Ronai. 2006. Regulation of p53 localization and activity by Ubc13. Molecular and Cellular Biology 26: 8901-8913.
19. Lee, S.H., J.K. Nam, J.K. Park, J.H. Lee, S. Min Do, and H.J. Kuh. 2014. Differential protein expression and novel biomarkers related to 5-FU resistance in a 3D colorectal adenocarcinoma model. Oncology Reports 32: 1427-1434.
20. Li, Y., T.G. Vandenboom 2nd, D. Kong, Z. Wang, S. Ali, P.A. Philip, and F.H. Sarkar. 2009. Up-regulation of miR-200 and let-7 by natural agents leads to the reversal of epithelial-to-mesenchymal transition in gemcitabine-resistant pancreatic cancer cells. Cancer Research 69: 6704-6712.
21. Lin, H., T. Dai, H. Xiong, X. Zhao, X. Chen, C. Yu, J. Li, X. Wang, and L. Song. 2010. Unregulated miR-96 induces cell proliferation in human breast cancer by downregulating transcriptional factor FOXO3a. PLoS One 5: e15797.
22. Manoochehri, M., A. Karbasi, M. Bandehpour, and B. Kazemi. 2014. Down-regulation of BAX gene during carcinogenesis and acquisition of resistance to 5-FU in colorectal cancer. Pathology & Oncology Research 20: 301-307.
23. Mattie, M.D., C.C. Benz, J. Bowers, K. Sensinger, L. Wong, G.K. Scott, V. Fedele, D. Ginzinger, R. Getts, and C. Haqq. 2006. Optimized high-throughput microRNA expression profiling provides novel biomarker assessment of clinical prostate and breast cancer biopsies. Molecular Cancer 5: 24.
24. Mikhail, A.S., S. Eetezadi, and C. Allen. 2013. Multicellular tumor spheroids for evaluation of cytotoxicity and tumor growth inhibitory effects of nanomedicines in vitro: A comparison of docetaxel-loaded block copolymer micelles and Taxotere(R). PLoS One 8: e62630.
25. Minchinton, A.I., and I.F. Tannock. 2006. Drug penetration in solid tumours. Nature Reviews Cancer 6: 583-592.
26. Park, J.K., S.H. Lee, J.H. Kang, K. Nishio, N. Saijo, and H.J. Kuh. 2004. Synergistic interaction between gefitinib (Iressa, ZD1839) and paclitaxel against human gastric carcinoma cells. Anti-Cancer Drugs 15: 809-818.
27. Ress, A.L., V. Stiegebauer, E. Winter, D. Schwarzenbacher, T. Kiesslich, S. Lax, S. Jahn, A. Deutsch, T. Bauernhofer, H. Ling, H. Samonigg, A. Gerger, G. Hoefler, and M. Pichler. 2014. MiR-96-5p influences cellular growth and is associated with poor survival in colorectal cancer patients. Molecular Carcinogenesis. doi: 10.1002/mc.22218.
28. Schimmer, A.D., S. Dalili, R.A. Batey, and S.J. Riedl. 2006. Targeting XIAP for the treatment of malignancy. Cell Death and Differentiation 13: 179-188.
29. Schimmer, A.D., E.H. Estey, G. Borthakur, B.Z. Carter, G.J. Schiller, M.S. Tallman, J.K. Altman, J.E. Karp, J. Kassis, D.W. Hedley, J. Brandwein, W. Xu, D.H. Mak, E. Lacasse, C. Jacob, S.J. Morris, J. Jolivet, and M. Andreeff. 2009. Phase I/II trial of AEG35156 X-linked inhibitor of apoptosis protein antisense oligonucleotide combined with idarubicin and cytarabine in patients with relapsed or primary refractory acute myeloid leukemia. Journal of Clinical Oncology 27: 4741-4746.
30. Schmidt, W.M., M. Kalipciyan, E. Dornstauder, B. Rizovski, G.G. Steger, R. Sedivy, M.W. Mueller, and R.M. Mader. 2004. Dissecting progressive stages of 5-fluorouracil resistance in vitro using RNA expression profiling. International Journal of Cancer 112: 200-212.
31. Suzuki, Y., Y. Imai, H. Nakayama, K. Takahashi, K. Takio, and R. Takahashi. 2001. A serine protease, HtrA2, is released from the mitochondria and interacts with XIAP, inducing cell death. Molecular Cell 8: 613-621.
32. Tanaka, M., H.I. Suzuki, J. Shibahara, A. Kunita, T. Isagawa, A. Yoshimi, M. Kurokawa, K. Miyazono, H. Aburatani, S. Ishikawa, and M. Fukayama. 2014. EVI1 oncogene promotes KRAS pathway through suppression of microRNA-96 in pancreatic carcinogenesis. Oncogene 33: 2454-2463.
33. Tang, X., D. Zheng, P. Hu, Z. Zeng, M. Li, L. Tucker, R. Monahan, M.B. Resnick, M. Liu, and B. Ramratnam. 2014. Glycogen synthase kinase 3 beta inhibits microRNA-183-96-182 cluster via the beta-Catenin/TCF/LEF-1 pathway in gastric cancer cells. Nucleic Acids Research 42: 2988-2998.
34. Tredan, O., C.M. Galmarini, K. Patel, and I.F. Tannock. 2007. Drug resistance and the solid tumor microenvironment. Journal of the National Cancer Institute 99: 1441-1454.
35. Vichai, V., and K. Kirtikara. 2006. Sulforhodamine B colorimetric assay for cytotoxicity screening. Nature Protocols 1: 1112-1116.
36. Wang, Y., J.W. Huang, P. Calses, C.J. Kemp, and T. Taniguchi. 2012. MiR-96 downregulates REV1 and RAD51 to promote cellular sensitivity to cisplatin and PARP inhibition. Cancer Research 72: 4037-4046.
37. Xia, Y., and K. Lee. 2010. Targeting multidrug resistance with small molecules for cancer therapy. Biomolecules & Therapeutics 18: 375-385.
38. Xu, D., X. He, Y. Chang, C. Xu, X. Jiang, S. Sun, and J. Lin. 2013. Inhibition of miR-96 expression reduces cell proliferation and clonogenicity of HepG2 hepatoma cells. Oncology Reports 29: 653-661.
39. Xu, X.M., J.C. Qian, Z.L. Deng, Z. Cai, T. Tang, P. Wang, K.H. Zhang, and J.P. Cai. 2012. Expression of miR-21, miR-31, miR-96 and miR-135b is correlated with the clinical parameters of colorectal cancer. Oncology Letters 4: 339-345.
40. Yeon, S.E., Y. Da No, S.H. Lee, S.W. Nam, I.H. Oh, J. Lee, and H.J. Kuh. 2013. Application of concave microwells to pancreatic tumor spheroids enabling anticancer drug evaluation in a clinically relevant drug resistance model. PLoS One 8: e73345.
41. Yu, S., Z. Lu, C. Liu, Y. Meng, Y. Ma, W. Zhao, J. Liu, J. Yu, and J. Chen. 2010. miRNA-96 suppresses KRAS and functions as a tumor suppressor gene in pancreatic cancer. Cancer Research 70: 6015-6025.
42. Zhang, L., K. Pickard, V. Jenei, M.D. Bullock, A. Bruce, R. Mitter, G. Kelly, C. Paraskeva, J. Strefford, J. Primrose, G.J. Thomas, G. Packham, and A.H. Mirnezami. 2013. miR-153 supports colorectal cancer progression via pleiotropic effects that enhance invasion and chemotherapeutic resistance. Cancer Research 73: 6435-6447.
43. Zhang, N., Y. Yin, S.J. Xu, and W.S. Chen. 2008. 5-Fluorouracil: Mechanisms of resistance and reversal strategies. Molecules 13: 1551-1569.
44. Zhou, Y., G. Wan, R. Spizzo, C. Ivan, R. Mathur, X. Hu, X. Ye, J. Lu, F. Fan, L. Xia, G.A. Calin, L.M. Ellis, and X. Lu. 2014. miR-203 induces oxaliplatin resistance in colorectal cancer cells by negatively regulating ATM kinase. Molecular Oncology 8: 83-92.