DOI QR코드

DOI QR Code

MicroRNA-203 As a Stemness Inhibitor of Glioblastoma Stem Cells

  • Deng, Yifan (Department of Neurosurgery, Huizhou Municipal Central Hospital) ;
  • Zhu, Gang (Department of Neurosurgery, Huizhou Municipal Central Hospital) ;
  • Luo, Honghai (Department of Neurosurgery, Huizhou Municipal Central Hospital) ;
  • Zhao, Shiguang (Department of Neurosurgery, The First Affiliated Hospital of Harbin Medical University)
  • Received : 2016.05.03
  • Accepted : 2016.07.13
  • Published : 2016.08.31

Abstract

Glioblastoma stem cells (GBM-SCs) are believed to be a subpopulation within all glioblastoma (GBM) cells that are in large part responsible for tumor growth and the high grade of therapeutic resistance that is so characteristic of GBM. MicroRNAs (miR) have been implicated in regulating the expression of oncogenes and tumor suppressor genes in cancer stem cells, including GBM-SCs, and they are a potential target for cancer therapy. In the current study, miR-203 expression was reduced in $CD133^+$ GBM-SCs derived from six human GBM biopsies. MicroRNA-203 transfected GBM-SCs had reduced capacity for self-renewal in the cell sphere assay and increased expression of glial and neuronal differentiation markers. In addition, a reduced proliferation rate and an increased rate of apoptosis were observed. Therefore, miR-203 has the potential to reduce features of stemness, specifically in GBM-SCs, and is a logical target for GBM gene therapy.

Keywords

References

  1. Bao, S., Wu, Q., McLendon, R.E., Hao, Y., Shi, Q., Hjelmeland, A.B., Dewhirst, M.W., Bigner, D.D., and Rich, J.N. (2006). Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 444, 756-760. https://doi.org/10.1038/nature05236
  2. Beier, D., Hau, P., Proescholdt, M., Lohmeier, A., Wischhusen, J., Oefner, P.J., Aigner, L., Brawanski, A., Bogdahn, U., and Beier, C.P. (2007). CD133(+) and CD133(-) glioblastoma-derived cancer stem cells show differential growth characteristics and molecular profiles. Cancer Res. 67, 4010-4015. https://doi.org/10.1158/0008-5472.CAN-06-4180
  3. Beier, D., Wischhusen, J., Dietmaier, W., Hau, P., Proescholdt, M., Brawanski, A., Bogdahn, U., and Beier, C.P. (2008). CD133 expression and cancer stem cells predict prognosis in high-grade oligodendroglial tumors. Brain Pathol. 18, 370-377. https://doi.org/10.1111/j.1750-3639.2008.00130.x
  4. Chen, Z., Li, D., Cheng, Q., Ma, Z., Jiang, B., Peng, R., Chen, R., Cao, Y., and Wan, X. (2014). MicroRNA-203 inhibits the proliferation and invasion of U251 glioblastoma cells by directly targeting PLD2. Mol. Med. Rep. 9, 503-508. https://doi.org/10.3892/mmr.2013.1814
  5. Chomczynski, P., and Sacchi, N. (2006). The single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction: twenty-something years on. Nat. Protoc. 1, 581-585. https://doi.org/10.1038/nprot.2006.83
  6. Clevers, H. (2011). The cancer stem cell: premises, promises and challenges. Nat. Med. 17, 313-319. https://doi.org/10.1038/nm.2304
  7. Dean, M., Fojo, T., and Bates, S. (2005). Tumour stem cells and drug resistance. Nat. Rev. Cancer 5, 275-284. https://doi.org/10.1038/nrc1590
  8. Dontula, R., Dinasarapu, A., Chetty, C., Pannuru, P., Herbert, E., Ozer, H., and Lakka, S.S. (2013). MicroRNA 203 modulates Glioma cell migration via Robo1/ERK/MMP-9 signaling. Genes Cancer 4, 285-296. https://doi.org/10.1177/1947601913500141
  9. Hayes, J., Peruzzi, P.P., and Lawler, S. (2014). MicroRNAs in cancer: biomarkers, functions and therapy. Trends Mol. Med. 20, 460-469. https://doi.org/10.1016/j.molmed.2014.06.005
  10. Heywood, R.M., Marcus, H.J., Ryan, D.J., Piccirillo, S.G., Al-Mayhani, T.M., and Watts, C. (2012). A review of the role of stem cells in the development and treatment of glioma. Acta Neurochir (Wien) 154, 951-969; discussion 969. https://doi.org/10.1007/s00701-012-1338-9
  11. Lena, A.M., Shalom-Feuerstein, R., Rivetti di Val Cervo, P., Aberdam, D., Knight, R.A., Melino, G., and Candi, E. (2008). miR-203 represses 'stemness' by repressing DeltaNp63. Cell Death Differ. 15, 1187-1195. https://doi.org/10.1038/cdd.2008.69
  12. Omuro, A., and DeAngelis, L.M. (2013). Glioblastoma and other malignant gliomas: a clinical review. JAMA 310, 1842-1850. https://doi.org/10.1001/jama.2013.280319
  13. Schraivogel, D., Weinmann, L., Beier, D., Tabatabai, G., Eichner, A., Zhu, J.Y., Anton, M., Sixt, M., Weller, M., Beier, C.P., et al. (2011). CAMTA1 is a novel tumour suppressor regulated by miR-9/9* in glioblastoma stem cells. EMBO J. 30, 4309-4322. https://doi.org/10.1038/emboj.2011.301
  14. Singh, S.K., Clarke, I.D., Terasaki, M., Bonn, V.E., Hawkins, C., Squire, J., and Dirks, P.B. (2003). Identification of a cancer stem cell in human brain tumors. Cancer Res. 63, 5821-5828.
  15. Visvader, J.E., and Lindeman, G.J. (2008). Cancer stem cells in solid tumours: accumulating evidence and unresolved questions. Nat. Rev. Cancer 8, 755-768. https://doi.org/10.1038/nrc2499
  16. Yi, R., Poy, M.N., Stoffel, M., and Fuchs, E. (2008). A skin microRNA promotes differentiation by repressing 'stemness'. Nature 452, 225-229. https://doi.org/10.1038/nature06642
  17. Zhao, S., Deng, Y., Liu, Y., Chen, X., Yang, G., Mu, Y., Zhang, D., Kang, J., and Wu, Z. (2013). MicroRNA-153 is tumor suppressive in glioblastoma stem cells. Mol. Biol. Rep. 40, 2789-2798. https://doi.org/10.1007/s11033-012-2278-4
  18. Zhao, B., Bian, E.B., and Li, J. (2014). New advances of microRNAs in glioma stem cells, with special emphasis on aberrant methylation of microRNAs. J. Cell Physiol. 229, 1141-1147. https://doi.org/10.1002/jcp.24540

Cited by

  1. Reduced circulating microRNA-203 predicts poor prognosis for glioblastoma 2017, https://doi.org/10.3233/CBM-170335
  2. Comparative studies of vertebrate iduronate 2-sulfatase (IDS) genes and proteins: evolution of A mammalian X-linked gene vol.7, pp.1, 2017, https://doi.org/10.1007/s13205-016-0595-3
  3. miR-484/MAP2/c-Myc-positive regulatory loop in glioma promotes tumor-initiating properties through ERK1/2 signaling vol.49, pp.2, 2018, https://doi.org/10.1007/s10735-018-9760-9
  4. The MicroRNA-551a/MEF2C Axis Regulates the Survival and Sphere Formation of Cancer Cells in Response to 5-Fluorouracil vol.42, pp.2, 2019, https://doi.org/10.14348/molcells.2018.0288
  5. Pathological and Molecular Features of Glioblastoma and Its Peritumoral Tissue vol.11, pp.4, 2016, https://doi.org/10.3390/cancers11040469
  6. MicroRNA Signature in Human Normal and Tumoral Neural Stem Cells vol.20, pp.17, 2016, https://doi.org/10.3390/ijms20174123
  7. MicroRNA‐203 reinforces stemness properties in melanoma and augments tumorigenesis in vivo vol.234, pp.11, 2019, https://doi.org/10.1002/jcp.28619
  8. New emerging roles of CD133 in cancer stem cell: Signaling pathway and miRNA regulation vol.234, pp.12, 2019, https://doi.org/10.1002/jcp.28824
  9. MicroRNA‐203 diminishes the stemness of human colon cancer cells by suppressing GATA6 expression vol.235, pp.3, 2016, https://doi.org/10.1002/jcp.29192
  10. Understanding Glioblastoma Biomarkers: Knocking a Mountain with a Hammer vol.9, pp.5, 2020, https://doi.org/10.3390/cells9051236
  11. miRNA signature in glioblastoma: Potential biomarkers and therapeutic targets vol.117, pp.None, 2020, https://doi.org/10.1016/j.yexmp.2020.104550
  12. HOTAIR Contributes to Stemness Acquisition of Cervical Cancer through Regulating miR-203 Interaction with ZEB1 on Epithelial-Mesenchymal Transition vol.2021, pp.None, 2016, https://doi.org/10.1155/2021/4190764
  13. Glioblastoma and MiRNAs vol.13, pp.7, 2016, https://doi.org/10.3390/cancers13071581
  14. A longitudinal study of alterations of circulating DJ-1 and miR203a-3p in association to olanzapine medication in a sample of first episode patients with schizophrenia vol.146, pp.None, 2016, https://doi.org/10.1016/j.jpsychires.2021.12.049