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Published in: Tumor Biology 7/2014

01-07-2014 | Research Article

Up-regulation of microRNA-138 induce radiosensitization in lung cancer cells

Authors: Hui Yang, Yue Tang, Wei Guo, Yuwen Du, Yuanyuan Wang, Ping Li, Wenqiao Zang, Xiaojun Yin, Huaqi Wang, Heying Chu, Guojun Zhang, Guoqiang Zhao

Published in: Tumor Biology | Issue 7/2014

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Abstract

Deregulation of microRNAs (miRNAs) is implicated in tumor progression. We attempt to identify the association between miR-138 and Sentrin/SUMO-specific protease 1 (SENP1) as a radiosensitization-related gene and characterize the biological function by which SENP1 was regulated by miR-138 to influence radiosensitization in lung cancer cells. In this study, we showed that miRNA-138 is reduced in both lung cancer clinical specimens and cell lines and is effective to inhibit SENP1 expression. Moreover, high levels of miR-138 are associated with lower levels of lung cancer cell proliferation and colony formation. Then, we investigated the underlying mechanisms responsible for the increase in the radiosensitivity of lung cancer cells when SENP1 is inhibited by miR-138. We further show that the increased radiosensitivity may be the result of an increased γ-H2AX expression, an increased rate of apoptosis, and changes in the cell cycle. In conclusion, our data demonstrate that the miR-138/SENP1 cascade is relative to radiosensitization in lung cancer cells and is a potential radiotherapy target.
Literature
1.
go back to reference Webb S. Advances in three-dimensional conformal radiation therapy physics with intensity modulation. Lancet Oncol. 2000;1(1):30–6.CrossRefPubMed Webb S. Advances in three-dimensional conformal radiation therapy physics with intensity modulation. Lancet Oncol. 2000;1(1):30–6.CrossRefPubMed
2.
go back to reference Saadeddin A. Radiotherapy for NSCLC: review of conventional and new treatment techniques. J Infect Public Health. 2012;1:S45–9.CrossRef Saadeddin A. Radiotherapy for NSCLC: review of conventional and new treatment techniques. J Infect Public Health. 2012;1:S45–9.CrossRef
4.
go back to reference Ding J, Miao ZH, Meng LH, Geng MY. Emerging cancer therapeutic opportunities target DNA-repair systems. Trends Pharmacol Sci. 2006;27(6):338–44.CrossRefPubMed Ding J, Miao ZH, Meng LH, Geng MY. Emerging cancer therapeutic opportunities target DNA-repair systems. Trends Pharmacol Sci. 2006;27(6):338–44.CrossRefPubMed
5.
go back to reference Hinz JM, Yamada NA, Salazar EP, Tebbs RS, Thompson LH. Influence of double-strand-break repair pathways on radiosensitivity throughout the cell cycle in CHO cells. DNA Repair (Amst). 2005;4(7):782–92.CrossRef Hinz JM, Yamada NA, Salazar EP, Tebbs RS, Thompson LH. Influence of double-strand-break repair pathways on radiosensitivity throughout the cell cycle in CHO cells. DNA Repair (Amst). 2005;4(7):782–92.CrossRef
6.
go back to reference Halperin EC, Perez CA, Brady LW. Principles and practice of radiation oncology (5th edition). USA: Klouwer Business; 2008. p. 109–25. Halperin EC, Perez CA, Brady LW. Principles and practice of radiation oncology (5th edition). USA: Klouwer Business; 2008. p. 109–25.
7.
go back to reference Pawlik TM, Keyomarsi K. Role of cell cycle in mediating sensitivity to radiotherapy. Int J Radiat Oncol Biol Phys. 2004;59(4):928–42.CrossRefPubMed Pawlik TM, Keyomarsi K. Role of cell cycle in mediating sensitivity to radiotherapy. Int J Radiat Oncol Biol Phys. 2004;59(4):928–42.CrossRefPubMed
8.
go back to reference Joubert A, Foray N. Intrinsic radiosensitivity and DNA double-strand breaks in human cells. Cancer Radiother. 2007;11(3):129–42.CrossRefPubMed Joubert A, Foray N. Intrinsic radiosensitivity and DNA double-strand breaks in human cells. Cancer Radiother. 2007;11(3):129–42.CrossRefPubMed
9.
go back to reference Morrison C, Sonoda E, Takao N, Shinohara A, Yamamoto K, Takeda S. The controlling role of ATM in homologous recombinational repair of DNA damage. EMBO J. 2000;19(3):463–71.PubMedCentralCrossRefPubMed Morrison C, Sonoda E, Takao N, Shinohara A, Yamamoto K, Takeda S. The controlling role of ATM in homologous recombinational repair of DNA damage. EMBO J. 2000;19(3):463–71.PubMedCentralCrossRefPubMed
10.
11.
go back to reference Liang K, Jin W, Knuefermann C. Targeting the phosphatidylinositol 3-kinase/Akt pathway for enhancing breast cancer cells to radiotherapy. Mol Cancer Ther. 2003;2(4):353–60.PubMed Liang K, Jin W, Knuefermann C. Targeting the phosphatidylinositol 3-kinase/Akt pathway for enhancing breast cancer cells to radiotherapy. Mol Cancer Ther. 2003;2(4):353–60.PubMed
12.
go back to reference Bawa-Khalfe T, Cheng J, Lin SH, Ittmann MM, Yeh ET. SENP1 induces prostatic intraepithelial neoplasia through multiple mechanisms. J Biol Chem. 2010;285(33):25859–66.PubMedCentralCrossRefPubMed Bawa-Khalfe T, Cheng J, Lin SH, Ittmann MM, Yeh ET. SENP1 induces prostatic intraepithelial neoplasia through multiple mechanisms. J Biol Chem. 2010;285(33):25859–66.PubMedCentralCrossRefPubMed
13.
go back to reference Bettermann K, Benesch M, Weis S, Haybaeck J. SUMOylation in carcinogenesis. Cancer Lett. 2012;316(2):113–25.CrossRefPubMed Bettermann K, Benesch M, Weis S, Haybaeck J. SUMOylation in carcinogenesis. Cancer Lett. 2012;316(2):113–25.CrossRefPubMed
14.
go back to reference Wang RT, Zhi XY, Zhang Y, Zhang J. Inhibition of SENP1 induces radiosensitization in lung cancer cells. Exp Ther Med. 2013;6(4):1054–8.PubMedCentralPubMed Wang RT, Zhi XY, Zhang Y, Zhang J. Inhibition of SENP1 induces radiosensitization in lung cancer cells. Exp Ther Med. 2013;6(4):1054–8.PubMedCentralPubMed
15.
go back to reference Zhang H, Zhang H, Zhao M, Lv Z, Zhang X, Qin X, et al. MiR-138 inhibits tumor growth through repression of EZH2 in non-small cell lung cancer. Cell Physiol Biochem. 2013;31(1):56–65.CrossRefPubMed Zhang H, Zhang H, Zhao M, Lv Z, Zhang X, Qin X, et al. MiR-138 inhibits tumor growth through repression of EZH2 in non-small cell lung cancer. Cell Physiol Biochem. 2013;31(1):56–65.CrossRefPubMed
16.
go back to reference Limin L, Guoqing H, Hongyi Z, Yonghong G, Youshuo L, Jirong H. Down-regulation of miR-138 promotes colorectal cancer metastasis via directly targeting TWIST2. J Transl Med. 2013;11:275–85.CrossRef Limin L, Guoqing H, Hongyi Z, Yonghong G, Youshuo L, Jirong H. Down-regulation of miR-138 promotes colorectal cancer metastasis via directly targeting TWIST2. J Transl Med. 2013;11:275–85.CrossRef
17.
go back to reference Wang W, Zhao LJ, Tan YX, Ren H, Qi ZT. MiR-138 induces cell cycle arrest by targeting cyclin D3 in hepatocellular carcinoma. Carcinogenesis. 2012;33(5):1113–20.PubMedCentralCrossRefPubMed Wang W, Zhao LJ, Tan YX, Ren H, Qi ZT. MiR-138 induces cell cycle arrest by targeting cyclin D3 in hepatocellular carcinoma. Carcinogenesis. 2012;33(5):1113–20.PubMedCentralCrossRefPubMed
18.
go back to reference Taneja N, Davis M, Choy JS, Beckett MA, Singh R, Kron SJ, et al. Histone H2AX phosphorylation as a predictor of radiosensitivity and target for radiotherapy. J Biol Chem. 2004;279(3):2273–80.CrossRefPubMed Taneja N, Davis M, Choy JS, Beckett MA, Singh R, Kron SJ, et al. Histone H2AX phosphorylation as a predictor of radiosensitivity and target for radiotherapy. J Biol Chem. 2004;279(3):2273–80.CrossRefPubMed
19.
go back to reference Crawford M, Brawner E, Batte K, Yu L, Hunter MG, Otterson GA, et al. MicroRNA-126 inhibits invasion in non-small cell lung carcinoma cell lines. Biochem Biophys Res Commun. 2008;373(4):607–12.CrossRefPubMed Crawford M, Brawner E, Batte K, Yu L, Hunter MG, Otterson GA, et al. MicroRNA-126 inhibits invasion in non-small cell lung carcinoma cell lines. Biochem Biophys Res Commun. 2008;373(4):607–12.CrossRefPubMed
20.
go back to reference Zhang JG, Wang JJ, Zhao F, Liu Q, Jiang K, Yang GH. MicroRNA-21 (miR-21) represses tumor suppressor PTEN and promotes growth and invasion in non-small cell lung cancer (NSCLC). Clin Chim Acta. 2010;411(11–12):846–52.CrossRefPubMed Zhang JG, Wang JJ, Zhao F, Liu Q, Jiang K, Yang GH. MicroRNA-21 (miR-21) represses tumor suppressor PTEN and promotes growth and invasion in non-small cell lung cancer (NSCLC). Clin Chim Acta. 2010;411(11–12):846–52.CrossRefPubMed
21.
go back to reference Ceppi P, Mudduluru G, Kumarswamy R, Rapa I, Scagliotti GV, Papotti M, et al. Loss of miR-200c expression induces an aggressive, invasive, and chemoresistant phenotype in non-small cell lung cancer. Mol Cancer Res. 2010;8(9):1207–16.CrossRefPubMed Ceppi P, Mudduluru G, Kumarswamy R, Rapa I, Scagliotti GV, Papotti M, et al. Loss of miR-200c expression induces an aggressive, invasive, and chemoresistant phenotype in non-small cell lung cancer. Mol Cancer Res. 2010;8(9):1207–16.CrossRefPubMed
22.
go back to reference Chen Z, Zeng H, Guo Y, Liu P, Pan H, Deng A, et al. miRNA-145 inhibits non-small cell lung cancer cell proliferation by targeting c-Myc. J Exp Clin Cancer Res. 2010;29:151.PubMedCentralCrossRefPubMed Chen Z, Zeng H, Guo Y, Liu P, Pan H, Deng A, et al. miRNA-145 inhibits non-small cell lung cancer cell proliferation by targeting c-Myc. J Exp Clin Cancer Res. 2010;29:151.PubMedCentralCrossRefPubMed
23.
go back to reference Takahashi Y, Forrest AR, Maeno E, Hashimoto T, Daub CO, Yasuda J. MiR-107 and miR-185 can induce cell cycle arrest in human non small cell lung cancer cell lines. PLoS One. 2009;4(8):e6677.PubMedCentralCrossRefPubMed Takahashi Y, Forrest AR, Maeno E, Hashimoto T, Daub CO, Yasuda J. MiR-107 and miR-185 can induce cell cycle arrest in human non small cell lung cancer cell lines. PLoS One. 2009;4(8):e6677.PubMedCentralCrossRefPubMed
24.
go back to reference Zhang JG, Guo JF, Liu DL, Liu Q, Wang JJ. MicroRNA-101 exerts tumor-suppressive functions in non-small cell lung cancer through directly targeting enhancer of zeste homolog 2. J Thorac Oncol. 2011;6(4):671–8.CrossRefPubMed Zhang JG, Guo JF, Liu DL, Liu Q, Wang JJ. MicroRNA-101 exerts tumor-suppressive functions in non-small cell lung cancer through directly targeting enhancer of zeste homolog 2. J Thorac Oncol. 2011;6(4):671–8.CrossRefPubMed
25.
go back to reference Qiu S, Huang D, Yin D, Li F, Li X, Kung HF, et al. Suppression of tumorigenicity by microRNA-138 through inhibition of EZH2-CDK4/6- pRb-E2F1 signal loop in glioblastoma multiforme. Biochim Biophys Acta. 2013;1832(10):1697–707.CrossRefPubMed Qiu S, Huang D, Yin D, Li F, Li X, Kung HF, et al. Suppression of tumorigenicity by microRNA-138 through inhibition of EZH2-CDK4/6- pRb-E2F1 signal loop in glioblastoma multiforme. Biochim Biophys Acta. 2013;1832(10):1697–707.CrossRefPubMed
26.
go back to reference Wang Q, Zhong M, Liu W, Li J, Huang J, Zheng L. Alterations of microRNAs in cisplatin-resistant human non-small cell lung cancer cells (A549/DDP). Exp Lung Res. 2011;37(7):427–34.CrossRefPubMed Wang Q, Zhong M, Liu W, Li J, Huang J, Zheng L. Alterations of microRNAs in cisplatin-resistant human non-small cell lung cancer cells (A549/DDP). Exp Lung Res. 2011;37(7):427–34.CrossRefPubMed
Metadata
Title
Up-regulation of microRNA-138 induce radiosensitization in lung cancer cells
Authors
Hui Yang
Yue Tang
Wei Guo
Yuwen Du
Yuanyuan Wang
Ping Li
Wenqiao Zang
Xiaojun Yin
Huaqi Wang
Heying Chu
Guojun Zhang
Guoqiang Zhao
Publication date
01-07-2014
Publisher
Springer Netherlands
Published in
Tumor Biology / Issue 7/2014
Print ISSN: 1010-4283
Electronic ISSN: 1423-0380
DOI
https://doi.org/10.1007/s13277-014-1879-z

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