Molecules and Cells

Korean Society for Molecular and Cellular Biology (한국분자세포생물학회)
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MicroRNA-3200-5p Promotes Osteosarcoma Cell Invasion via Suppression of BRMS1

  • Li, Gen (Department of Orthopedics, Shanghai Tenth People's Hospital, Tongji University School of Medicine) ;
  • Li, Li (Department of Orthopedics, Changhai Hospital of Shanghai, The Second Military Medical University) ;
  • Sun, Qi (Department of Orthopedics, Shanghai Tenth People's Hospital, Tongji University School of Medicine) ;
  • Wu, Jiezhou (Department of Orthopedics, Shanghai Tenth People's Hospital, Tongji University School of Medicine) ;
  • Ge, Wei (Department of Orthopedics, Shanghai Tenth People's Hospital, Tongji University School of Medicine) ;
  • Lu, Guanghua (Department of Orthopedics, Shanghai Tenth People's Hospital, Tongji University School of Medicine) ;
  • Cai, Ming (Department of Orthopedics, Shanghai Tenth People's Hospital, Tongji University School of Medicine)
  • Received : 2017.09.04
  • Accepted : 2018.02.18
  • Published : 2018.06.30
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Abstract

Tumour metastasis is one of the most serious challenges of cancer as it is the major cause of mortality in patients with solid tumours, including osteosarcoma (OS). In this regard, anti-metastatic genes have potential for metastasis inhibition strategies. Recent evidence showed the importance of breast cancer metastasis suppressor 1 (BRMS1) in control of OS invasiveness, but the regulation of BRMS1 in OS remains largely unknown. Here, we used bioinformatics analyses to predict BRMS1-targeting microRNAs (miRNAs), and the functional binding of miRNAs to BRMS1 mRNA was evaluated using a dual luciferase reporter assay. Among all BRMS1-targeting miRNAs, only miR-151b, miR-7-5p and miR-3200-5p showed significant expression in OS specimens. Specifically, we found that only miR-3200-5p significantly inhibited protein translation of BRMS1 via pairing to the 3'-UTR of the BRMS1 mRNA. Moreover, we detected significantly lower BRMS1 and significantly higher miR-3200-5p in the OS specimens compared to the paired adjacent non-tumour bone tissues. Furthermore, BRMS1 and miR-3200-5p levels were inversely correlated to each other. Low BRMS1 was correlated with metastasis and poor patient survival. In vitro, overexpression of miR-3200-5p significantly decreased BRMS1 levels and promoted OS cell invasion and migration, while depletion of miR-3200-5p significantly increased BRMS1 levels and inhibited OS cell invasion and migration. Thus, our study revealed that miR-3200-5p may be a critical regulator of OS cell invasiveness.

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References

  1. Al-Khanbashi, M., Caramuta, S., Alajmi, A.M., Al-Haddabi, I., Al-Riyami, M., Lui, W.O., and Al-Moundhri, M.S. (2016). Tissue and serum miRNA profile in locally advanced breast cancer (LABC). in response to neo-adjuvant chemotherapy (NAC). Treatment. PLoS One 11, e0152032. https://doi.org/10.1371/journal.pone.0152032
  2. Catalano, V., Turdo, A., Di Franco, S., Dieli, F., Todaro, M., and Stassi, G. (2013). Tumor and its microenvironment: a synergistic interplay. Semi. Cancer Biol. 23, 522-532. https://doi.org/10.1016/j.semcancer.2013.08.007
  3. Coronnello, C., and Benos, P.V. (2013). ComiR: Combinatorial microRNA target prediction tool. Nucleic Acids Res. 41, W159-164. https://doi.org/10.1093/nar/gkt379
  4. Ding, L., Congwei, L., Bei, Q., Tao, Y., Ruiguo, W., Heze, Y., Bo, D., and Zhihong, L. (2016). mTOR: An attractive therapeutic target for osteosarcoma? Oncotarget 7, 50805-50813.
  5. Fogh, J., Wright, W.C., and Loveless, J.D. (1977). Absence of HeLa cell contamination in 169 cell lines derived from human tumors. J. Natl. Cancer Inst. 58, 209-214. https://doi.org/10.1093/jnci/58.2.209
  6. Garcia, D.M., Baek, D., Shin, C., Bell, G.W., Grimson, A., and Bartel, D.P. (2011). Weak seed-pairing stability and high target-site abundance decrease the proficiency of lsy-6 and other microRNAs. Nat. Struct. Mol. Biol. 18, 1139-1146. https://doi.org/10.1038/nsmb.2115
  7. Han, K., Chen, X., Bian, N., Ma, B., Yang, T., Cai, C., Fan, Q., Zhou, Y., and Zhao, T.B. (2015). MicroRNA profiling identifies MiR-195 suppresses osteosarcoma cell metastasis by targeting CCND1. Oncotarget 6, 8875-8889.
  8. Huo, X., Li, S., Shi, T., Suo, A., Ruan, Z., Guo, H. and Yao, Y. (2015). Cullin3 promotes breast cancer cells metastasis and epithelial-mesenchymal transition by targeting BRMS1 for degradation. Oncotarget 6, 41959-41975.
  9. Hurst, D.R., Xie, Y., Vaidya, K.S., Mehta, A., Moore, B.P., Accavitti-Loper, M.A., Samant, R.S., Saxena, R., Silveira, A.C., and Welch, D.R. (2008). Alterations of BRMS1-ARID4A interaction modify gene expression but still suppress metastasis in human breast cancer cells. J. Biol. Chem. 283, 7438-7444. https://doi.org/10.1074/jbc.M709446200
  10. Meehan, W.J., Samant, R.S., Hopper, J.E., Carrozza, M.J., Shevde, L.A., Workman, J.L., Eckert, K.A., Verderame, M.F., and Welch, D.R. (2004). Breast cancer metastasis suppressor 1 (BRMS1). forms complexes with retinoblastoma-binding protein 1 (RBP1). and the mSin3 histone deacetylase complex and represses transcription. J. Biol. Chem. 279, 1562-1569. https://doi.org/10.1074/jbc.M307969200
  11. Nagji, A.S., Liu, Y., Stelow, E.B., Stukenborg, G.J., and Jones, D.R. (2010). BRMS1 transcriptional repression correlates with CpG island methylation and advanced pathological stage in non-small cell lung cancer. J. Pathol. 221, 229-237. https://doi.org/10.1002/path.2707
  12. Ponten, J., and Saksela, E. (1967). Two established in vitro cell lines from human mesenchymal tumours. Int. J. Cancer 2, 434-447. https://doi.org/10.1002/ijc.2910020505
  13. Ren, L., Mendoza, A., Zhu, J., Briggs, J.W., Halsey, C., Hong, E.S., Burkett, S.S., Morrow, J., Lizardo, M.M., Osborne, T., et al. (2015). Characterization of the metastatic phenotype of a panel of established osteosarcoma cells. Oncotarget 6, 29469-29481.
  14. Roesley, S.N., Suryadinata, R., Morrish, E., Tan, A.R., Issa, S.M., Oakhill, J.S., Bernard, O., Welch, D.R., and Sarcevic, B. (2016). Cyclindependent kinase-mediated phosphorylation of breast cancer metastasis suppressor 1 (BRMS1). affects cell migration. Cell Cycle 15, 137-151. https://doi.org/10.1080/15384101.2015.1121328
  15. Samant, R.S., Clark, D.W., Fillmore, R.A., Cicek, M., Metge, B.J., Chandramouli, K.H., Chambers, A.F., Casey, G., Welch, D.R., and Shevde, L.A. (2007). Breast cancer metastasis suppressor 1 (BRMS1). inhibits osteopontin transcription by abrogating NF-kappaB activation. Mol. Cancer 6, 6.
  16. Seraj, M.J., Harding, M.A., Gildea, J.J., Welch, D.R., and Theodorescu, D. (2000a). The relationship of BRMS1 and RhoGDI2 gene expression to metastatic potential in lineage related human bladder cancer cell lines. Clin. Exp. Metastasis 18, 519-525. https://doi.org/10.1023/A:1011819621859
  17. Seraj, M.J., Samant, R.S., Verderame, M.F., and Welch, D.R. (2000b). Functional evidence for a novel human breast carcinoma metastasis suppressor, BRMS1, encoded at chromosome 11q13. Cancer Res. 60, 2764-2769.
  18. Smith, P.W., Liu, Y., Siefert, S.A., Moskaluk, C.A., Petroni, G.R., and Jones, D.R. (2009). Breast cancer metastasis suppressor 1 (BRMS1). suppresses metastasis and correlates with improved patient survival in non-small cell lung cancer. Cancer Lett. 276, 196-203. https://doi.org/10.1016/j.canlet.2008.11.024
  19. Wang, W., Zhou, X., and Wei, M. (2015). MicroRNA-144 suppresses osteosarcoma growth and metastasis by targeting ROCK1 and ROCK2. Oncotarget 6, 10297-10308.
  20. Wang, Z., Wang, C., Zhou, Z., Sun, M., Zhou, C., Chen, J., Yin, F., Wang, H., Lin, B., Zuo, D., et al. (2016). CD151-mediated adhesion is crucial to osteosarcoma pulmonary metastasis. Oncotarget 7, 60623-60638.
  21. Yan, H.L., Li, L., Li, S.J., Zhang, H.S., and Xu, W. (2016). miR-346 promotes migration and invasion of nasopharyngeal carcinoma cells via targeting BRMS1. J. Biochem. Mol. Toxicol. 30, 602-607. https://doi.org/10.1002/jbt.21827

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