Molecules and Cells

  • 제37권12호
  • /
  • Pages.873-880
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  • 2014
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  • 1016-8478(pISSN)
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  • 0219-1032(eISSN)
한국분자세포생물학회 (Korean Society for Molecular and Cellular Biology)
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miRNA-183 Suppresses Apoptosis and Promotes Proliferation in Esophageal Cancer by Targeting PDCD4

  • Yang, Miao (Key Laboratory of Environmental Medicine Engineering, Ministry of Education, School of Public Health, Southeast University) ;
  • Liu, Ran (Key Laboratory of Environmental Medicine Engineering, Ministry of Education, School of Public Health, Southeast University) ;
  • Li, Xiajun (Key Laboratory of Environmental Medicine Engineering, Ministry of Education, School of Public Health, Southeast University) ;
  • Liao, Juan (Key Laboratory of Environmental Medicine Engineering, Ministry of Education, School of Public Health, Southeast University) ;
  • Pu, Yuepu (Key Laboratory of Environmental Medicine Engineering, Ministry of Education, School of Public Health, Southeast University) ;
  • Pan, Enchun (Key Laboratory of Environmental Medicine Engineering, Ministry of Education, School of Public Health, Southeast University) ;
  • Yin, Lihong (Key Laboratory of Environmental Medicine Engineering, Ministry of Education, School of Public Health, Southeast University) ;
  • Wang, Yi (Huaian Center for Disease Control and Prevention)
  • 투고 : 2014.06.05
  • 심사 : 2014.09.22
  • 발행 : 2014.12.31
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초록

In our previous study, miRNA-183, a miRNA in the miR-96-182-183 cluster, was significantly over-expressed in esophageal squamous cell carcinoma (ESCC). In the present study, we explored the oncogenic roles of miR-183 in ESCC by gain and loss of function analysis in an esophageal cancer cell line (EC9706). Genome-wide mRNA micro-array was applied to determine the genes that were regulated directly or indirectly by miR-183. 3'UTR luciferase reporter assay, RT-PCR, and Western blot were conducted to verify the target gene of miR-183. Cell culture results showed that miR-183 inhibited apoptosis (p < 0.05), enhanced cell proliferation (p < 0.05), and accelerated G1/S transition (p < 0.05). Moreover, the inhibitory effect of miR-183 on apoptosis was rescued when miR-183 was suppressed via miR-183 inhibitor (p < 0.05). Western blot analysis showed that the expression of programmed cell death 4 (PDCD4), which was predicted as the target gene of miR-183 by microarray profiling and bioinformatics predictions, decreased when miR-183 was over-expressed. The 3'UTR luciferase reporter assay confirmed that miR-183 directly regulated PDCD4 by binding to sequences in the 3'UTR of PDCD4. Pearson correlation analysis further confirmed the significant negative correlation between miR-183 and PDCD4 in both cell lines and in ESCC patients. Our data suggest that miR-183 might play an oncogenic role in ESCC by regulating PDCD4 expression.

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참고문헌

  1. Achille, A., Biasi, M.O., Zamboni, G., Bogina, G., Magalini, A.R., Pederzoli, P., Perucho, M., and Scarpa, A. (1996). Chromosome 7q allelic losses in pancreatic carcinoma. Cancer Res. 56, 3808-3813.
  2. Bieche, I., Champeme, M.H., Matifas, F., Hacene, K., Callahan, R., and Lidereau, R. (1992). Loss of heterozygosity on chromosome 7q and aggressive primary breast cancer. Lancet 339, 139-143. https://doi.org/10.1016/0140-6736(92)90208-K
  3. Borel, C., and Antonarakis, S.E. (2008). Functional genetic variation of human miRNAs and phenotypic consequences. Mamm. Genome 19, 503-509. https://doi.org/10.1007/s00335-008-9137-6
  4. Calin, G.A., and Croce, C.M. (2006). MicroRNA signatures in human cancers. Nat. Rev. Cancer 6, 857-866. https://doi.org/10.1038/nrc1997
  5. Corcoran, M.M., Mould, S.J., Orchard, J.A., Ibbotson, R.E., Chapman, R.M., Boright, A.P., Platt, C., Tsui, L.C., Scherer, S.W., and Oscier, D.G. (1999). Dysregulation of cyclin dependent kinase 6 expression in splenic marginal zone lymphoma through chromosome 7q translocations. Oncogene 18, 6271-6277. https://doi.org/10.1038/sj.onc.1203033
  6. Dubecz, A., Gall, I., Solymosi, N., Schweigert, M., Peters, J.H., Feith, M., and Stein, H.J. (2012). Temporal trends in long-term survival and cure rates in esophageal cancer: a seer database analysis. J. Thorac. Oncol. 7, 443-447. https://doi.org/10.1097/JTO.0b013e3182397751
  7. Eto, K., Goto, S., Nakashima, W., Ura, Y., and Abe, S.I. (2012). Loss of programmed cell death 4 induces apoptosis by promoting the translation of procaspase-3 mRNA. Cell Death Differ. 19, 573-581. https://doi.org/10.1038/cdd.2011.126
  8. Fang, L., Du, W.W., Yang, W.N., Rutnam, Z.J., Peng, C., Li, H.R., O'Malley, Y.Q., Askeland, R.W., Sugg, S., Liu, M.Y., et al. (2012). MiR-93 enhances angiogenesis and metastasis by targeting LATS2. Cell Cycle 11, 4352-4365. https://doi.org/10.4161/cc.22670
  9. Fassan, M., Cagol, M., Pennelli, G., Rizzetto, C., Giacomelli, L., Battaglia, G., Zaninotto, G., Ancona, E., Ruol, A., and Rugge, M. (2010). Programmed cell death 4 protein in esophageal cancer. Oncol. Rep. 24, 135-139.
  10. Fassan, M., Realdon, S., Pizzi, M., Balistreri, M., Battaglia, G., Zaninotto, G., Ancona, E., and Rugge, M. (2012). Programmed cell death 4 nuclear loss and miR-21 or activated Akt overexpression in esophageal squamous cell carcinogenesis. Dis. Esophagus 25, 263-268. https://doi.org/10.1111/j.1442-2050.2011.01236.x
  11. Frankel, L.B., Christoffersen, N.R., Jacobsen, A., Lindow, M., Krogh, A., and Lund, A.H. (2008). Programmed cell death 4 (PDCD4) is an important functional target of the microRNA miR-21 in breast cancer cells. J. Biol. Chem. 283, 1026-1033. https://doi.org/10.1074/jbc.M707224200
  12. Gaur, A.B., Holbeck, S.L., Colburn, N.H., and Israel, M.A. (2011). Downregulation of Pdcd4 by mir-21 facilitates glioblastoma proliferation in vivo. Neuro Oncol. 13, 580-590. https://doi.org/10.1093/neuonc/nor033
  13. Guo, X., Li, W., Wang, Q., and Yang, H.S. (2011). AKT activation by Pdcd4 knockdown up-regulates cyclin D1 expression and promotes cell proliferation. Genes Cancer 2, 818-828. https://doi.org/10.1177/1947601911431082
  14. Guo, P., Huang, Z.L., Yu, P., and Li, K. (2012). Trends in cancer mortality in China: an update. Ann. Oncol. 23, 2755-2762. https://doi.org/10.1093/annonc/mds069
  15. Han, Y., Chen, J., Zhao, X., Liang, C., Wang, Y., Sun, L., Jiang, Z., Zhang, Z., Yang, R., Li, Z., et al. (2011). MicroRNA expression signatures of bladder cancer revealed by deep sequencing. PLoS One 6, e18286. https://doi.org/10.1371/journal.pone.0018286
  16. He, J., and Chen, W. (2012). Chinese Cancer Registry Annual Report (Beijing, China: Military Medical Sciences Press).
  17. Hu, Y., Correa, A.M., Hoque, A., Guan, B., Ye, F., Huang, J., Swisher, S.G., Wu, T.T., Ajani, J.A., and Xu, X.C. (2011). Prognostic significance of differentially expressed miRNAs in esophageal cancer. Int. J. Cancer 128, 132-143. https://doi.org/10.1002/ijc.25330
  18. Hvid-Jensen, F., Pedersen, L., Drewes, A.M., Sorensen, H.T., and Funch-Jensen, P. (2011). Incidence of adenocarcinoma among patients with Barrett's esophagus. N. Engl. J. Med. 365, 1375-1383. https://doi.org/10.1056/NEJMoa1103042
  19. Jiang, Y., Zhang, S.H., Han, G.Q., and Qin, C.Y. (2010). Interaction of Pdcd4 with eIF4E inhibits the metastatic potential of hepatocellular carcinoma. Biomed. Pharmacother. 64, 424-429. https://doi.org/10.1016/j.biopha.2010.01.015
  20. Koo, S.H., Ihm, C.H., Kwon, K.C., Park, J.W., Kim, J.M., and Kong, G. (2001). Genetic alterations in hepatocellular carcinoma and intrahepatic cholangiocarcinoma. Cancer Genet. Cytogenet. 130, 22-28. https://doi.org/10.1016/S0165-4608(01)00460-5
  21. Kwong, D., Lam, A., Guan, X., Law, S., Tai, A., Wong, J., and Sham, J. (2004). Chromosomal aberrations in esophageal squamous cell carcinoma among Chinese: Gain of 12p predicts poor prognosis after surgery. Hum. Pathol. 35, 309-316. https://doi.org/10.1016/j.humpath.2003.10.020
  22. Lankat-Buttgereit, B., and Goke, R. (2009). The tumour suppressor Pdcd4: recent advances in the elucidation of function and regulation. Biol. Cell 101, 309-317. https://doi.org/10.1042/BC20080191
  23. Li, G.R., Luna, C., Qiu, J.M., Epstein, D.L., and Gonzalez, P. (2010a). Targeting of integrin ${\beta}1$ and kinesin $2{\alpha}$ by microRNA 183. J. Biol. Chem. 285, 5461-5471. https://doi.org/10.1074/jbc.M109.037127
  24. Li, J., Fu, H., Xu, C., Tie, Y., Xing, R., Zhu, J., Qin, Y., Sun, Z., and Zheng, X. (2010b). miR-183 inhibits TGF-beta1-induced apoptosis by downregulation of PDCD4 expression in human hepatocellular carcinoma cells. BMC Cancer 10, 354. https://doi.org/10.1186/1471-2407-10-354
  25. Lin, Y., Totsuka, Y., He, Y., Kikuchi, S., Qiao, Y., Ueda, J., Wei, W., Inoue, M., and Tanaka, H. (2013). Epidemiology of esophageal cancer in Japan and China. J. Epidemiol. 23, 233-242. https://doi.org/10.2188/jea.JE20120162
  26. Livak, K.J., and Schmittgen, T.D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2-$^{-{\Delta}{\Delta}Ct}$ method. Methods 25, 402-408. https://doi.org/10.1006/meth.2001.1262
  27. Ma, G., Zhang, H., Dong, M., Zheng, X.Y., Ozaki, I., Matsuhashi, S., and Guo, K.J. (2013). Downregulation of programmed cell death 4 (PDCD4) in tumorigenesis and progression of human digestive tract cancers. Tumor Biol. 34, 3879-3885. https://doi.org/10.1007/s13277-013-0975-9
  28. Matsuhashi, S., Hamajima, H., Xia, J.H., Zhang, H., Mizuta, T., Anzai, K., and Ozaki, I. (2014). Control of a tumor suppressor PDCD4: Degradation mechanisms of the protein in hepatocellular carcinoma cells. Cell. Signal. 26, 603-610. https://doi.org/10.1016/j.cellsig.2013.11.038
  29. Patil, V.S., Zhou, R., and Rana, T.M. (2014). Gene regulation by non-coding RNAs. Crit. Rev. Biochem. Mol. Biol. 49, 16-32. https://doi.org/10.3109/10409238.2013.844092
  30. Reis, P.P., Tomenson, M., Cervigne, N.K., Machado, J., Jurisica, I., Pintilie, M., Sukhai, M.A., Perez-Ordonez, B., Grenman, R., Gilbert, R.W., et al. (2010). Programmed cell death 4 loss increases tumor cell invasion and is regulated by miR-21 in oral squamous cell carcinoma. Mol. Cancer 9, 238. https://doi.org/10.1186/1476-4598-9-238
  31. Salic, A., and Mitchison, T.J. (2008). A chemical method for fast and sensitive detection of DNA synthesis in vivo. Proc. Natl. Acad. Sci. USA 105, 2415-2420. https://doi.org/10.1073/pnas.0712168105
  32. Santhanam, A.N., Baker, A.R., Hegamyer, G., Kirschmann, D.A., and Colburn, N.H. (2010). Pdcd4 repression of lysyl oxidase inhibits hypoxia-induced breast cancer cell invasion. Oncogene 29, 3921-3932. https://doi.org/10.1038/onc.2010.158
  33. Sarver, A.L., Li, L.H., and Subramanian, S. (2010). MicroRNA miR-183 functions as an oncogene by targeting the transcription factor EGR1 and promoting tumor cell migration. Cancer Res. 70, 9570-9580. https://doi.org/10.1158/0008-5472.CAN-10-2074
  34. Shibahara, K., Asano, M., Ishida, Y., Aoki, T., Koike, T., and Honjo, T. (1995). Isolation of a novel mouse gene MA-3 that is induced upon programmed cell death. Gene 166, 297-301. https://doi.org/10.1016/0378-1119(95)00607-9
  35. Tanaka, H., Sasayama, T., Tanaka, K., Nakamizo, S., Nishihara, M., Mizukawa, K., Kohta, M., Koyama, J., Miyake, S., Taniguchi, M., et al. (2013). MicroRNA-183 upregulates HIF-1alpha by targeting isocitrate dehydrogenase 2 (IDH2) in glioma cells. J. Neuro-Oncol. 111, 273-283. https://doi.org/10.1007/s11060-012-1027-9
  36. Thomson, D.W., Bracken, C.P., and Goodall, G.J. (2011). Experimental strategies for microRNA target identification. Nucleic Acids Res. 39, 6845-6853. https://doi.org/10.1093/nar/gkr330
  37. Ueno, K., Hirata, H., Shahryari, V., Deng, G., Tanaka, Y., Tabatabai, Z.L., Hinoda, Y., and Dahiya, R. (2013). microRNA-183 is an oncogene targeting Dkk-3 and SMAD4 in prostate cancer. Br. J. Cancer 108, 1659-1667. https://doi.org/10.1038/bjc.2013.125
  38. Wang, W., Zhao, J., Wang, H., Sun, Y., Peng, Z., Zhou, G., Fan, L., Wang, X., Yang, S., Wang, R., et al. (2010). 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. https://doi.org/10.1016/j.yexcr.2010.05.027
  39. Wei, N., Liu, S.S., Chan, K.K.L., and Ngan, H.Y.S. (2012). Tumour suppressive function and modulation of programmed Cell Death 4 (PDCD4) in ovarian cancer. PLoS One 7, e30311 . https://doi.org/10.1371/journal.pone.0030311
  40. Yang, M., Liu, R., Sheng, J.Y., Liao, J., Wang, Y., Pan, E.C., Guo, W., Pu, Y.P., and Yin, L.H. (2013). Differential expression profiles of microRNAs as potential biomarkers for the early diagnosis of esophageal squamous cell carcinoma. Oncol. Rep. 29, 169-176. https://doi.org/10.3892/or.2012.2105
  41. Zhang, H., OzakiZ, I., Mizuta, T., Hamajima, H., Yasutake, T., Eguchi, Y., Ideguchi, H., Yamamoto, K., and Matsuhashi, S. (2006). Involvement of programmed cell death 4 in transforming growth factor-beta 1-induced apoptosis in human hepatocellular carcinoma. Oncogene 25, 6101-6112. https://doi.org/10.1038/sj.onc.1209634
  42. Zhang, S.H., Li, J.F., Jiang, Y., Xu, Y.J., and Qin, C.Y. (2009). Programmed cell death 4 (PDCD4) suppresses metastastic potential of human hepatocellular carcinoma cells. J. Exp. Clin. Cancer Res. 28, 71. https://doi.org/10.1186/1756-9966-28-71
  43. Zhang, X., Wang, X.Y., Song, X.G., Liu, C.M., Shi, Y.Y., Wang, Y.K., Afonja, O., Ma, C.H., Chen, Y.H.H., and Zhang, L.N. (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. https://doi.org/10.1111/j.1349-7006.2010.01664.x
  44. Zhao, H.E., Guo, M.J., Zhao, G.Y., Ma, Q., Ma, B.A., Qiu, X.C., and Fan, Q.Y. (2012). miR-183 inhibits the metastasis of osteosarcoma via downregulation of the expression of Ezrin in F5M2 cells. Int. J. Mol. Med. 30, 1013-1020. https://doi.org/10.3892/ijmm.2012.1111
  45. Zhu, J.F., Feng, Y.P., Ke, Z.F., Yang, Z., Zhou, J.Y., Huang, X.R., and Wang, L.T. (2012). Down-regulation of miR-183 promotes migration and invasion of osteosarcoma by targeting Ezrin. Am. J. Pathol. 180, 2440-2451. https://doi.org/10.1016/j.ajpath.2012.02.023

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  17. Mutations in GAS5 affect the transformation from benign prostate proliferation to aggressive prostate cancer by affecting the transcription efficiency of GAS5 pp.00219541, 2019, https://doi.org/10.1002/jcp.27561
  18. HDAC-Linked “Proliferative” miRNA Expression Pattern in Pancreatic Neuroendocrine Tumors vol.19, pp.9, 2018, https://doi.org/10.3390/ijms19092781
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  29. Phosphatase and Tensin Homolog (PTEN) of Japanese Flounder—Its Regulation by miRNA and Role in Autophagy, Apoptosis and Pathogen Infection vol.21, pp.20, 2014, https://doi.org/10.3390/ijms21207725
  30. Network analysis of miRNA targeting m6A-related genes in patients with esophageal cancer vol.9, pp.None, 2014, https://doi.org/10.7717/peerj.11893
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