#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

The Relevance of MicroRNAs in Glioblastoma Stem Cells


Authors: R. Kleinová 1;  O. Slabý 1,2;  J. Šána 1,2
Authors‘ workplace: CEITEC –  Středoevropský technologický institut, MU, Brno 1;  Klinika komplexní onkologické péče, Masarykův onkologický ústav, Brno 2
Published in: Klin Onkol 2015; 28(5): 338-344
Category: Reviews
doi: https://doi.org/10.14735/amko2015338

Overview

Glioblastoma multiforme is the most common intracranial malignity of astrocyte origin in adults. Despite complex therapy consisting of maximal surgical resection, adjuvant concomitant chemoradiotherapy with temozolomide followed by temozolomide in monotherapy, the median of survival ranges between 12 and 15 months from dia­gnosis. This infaust prognosis is very often caused by both impossibility of achieving of sufficient radical surgical resection and tumor resistance to adjuvant therapy, which relates to the presence of glioblastoma stem cells. Similarly to normal stem cells, glioblastoma stem cells are capable of self‑ renewal, differentiation, and unlimited slow proliferation. Their resistance to conventional therapy is also due to higher expressions of DNA repair enzymes, antiapoptotic factors and multidrug transporters. Therefore, targeting these unique properties could be a novel promising therapeutic approach leading to more effective therapy and better prognosis of glioblastoma multiforme patients. One of the approaches how to successfully regulate above‑ mentioned properties is targeted regulation of microRNAs (miRNAs). These small non‑coding RNA molecules post‑transcriptionally regulate expression of more than 2/ 3 of all human genes that are also involved in stem cell associated signaling pathways. Moreover, deregulated expression of some miRNAs has been observed in many cancers, including glioblastoma multiforme.

Key words:
cancer stem cells –  glioblastoma multiforme –  microRNA

This study was supported by grant of Internal Grant Agency of the Czech Ministry of HealthNo. NT13514-4/2012 and project „CEITEC – Central European Institute of Technology“ (CZ.1.05/1.1.00/02.0068).

The authors declare they have no potential conflicts of interest concerning drugs, products, or services used in the study.

The Editorial Board declares that the manuscript met the ICMJE recommendation for biomedical papers.

Submitted:
12. 5. 2015

Accepted:
10. 9. 2015


Sources

1. Ohgaki H, Kleihues P. Population‑based studies on incidence, survival rates, and genetic alterations in astrocytic and oligodendroglial gliomas. J Neuropathol Exp Neurol 2005; 64(6): 479– 489.

2. Fadrus P, Lakomý R, Hübnerová P et al. Intrakraniální nádory –  dia­gnostika a terapie. Interni medicina pro praxi 2010; 12(7– 8): 376– 381.

3. Lakomý R, Fadrus, P, Slampa P et al. Multimodal treatment of glioblastoma multiforme: results of 86 consecutive patients dia­gnosed in period 2003– 2009. Klin Onkol 2011; 24(2): 112– 120.

4. Stopschinski BE, Beier CP, Beier D. Glioblastoma cancer stem cells –  from concept to clinical application. Cancer Lett 2013; 338(1): 32– 40. doi: 10.1016/ j.canlet.2012.05.033.

5. Lima FR, Kahn SA, Soletti RC et al. Glioblastoma: ther­apeutic challenges, what lies ahead. Biochim Biophys Acta 2012; 1826(2): 338– 349. doi: 10.1016/ j.bbcan.2012.05.004.

6. Jansson MD, Lund AH. MicroRNA and cancer. Mol Oncol 2012; 6(6): 590– 610. doi: 10.1016/ j.molonc.2012.09.006.

7. Liu C, Tang DG. MicroRNA regulation of cancer stem cells. Cancer Res 2011; 71(18): 5950– 5954. doi: 10.1158/ 0008‑ 5472.CAN‑ 11‑ 1035.

8. Furth J. Transmission of myeloid leukemia of mice: its relation to myeloma. J Exp Med 1935; 61(3): 423– 446.

9. Kleinsmith LJ, Pierce GB Jr. Multipotentiality of Single Embryonal Carcinoma Cells. Cancer Res 1964; 24: 1544– 1551.

10. Lapidot T, Sirard C, Vormoor J et al. A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature 1994; 367(6464): 645– 648.

11. Al‑ Hajj M, Wicha MS, Benito‑ Hernandez A et al. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA 2003; 100(7): 3983– 3988.

12. Singh SK, Clarke ID, Terasaki M et al. Identification of a cancer stem cell in human brain tumors. Cancer Res 2003; 63(18): 5821– 5828.

13. Bongiorno MR, Doukaki S, Malleo F et al. Identification of progenitor cancer stem cell in lentigo maligna melanoma. Dermatol Ther 2008; 21 (Suppl 1): 1– 5. doi: 10.1111/ j.1529‑ 8019.2008.00193.x.

14. O‘Brien CA, Pollett A, Gallinger S et al. A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature 2007; 445(7123): 106– 110.

15. Singh SK, Hawkins C, Clarke ID et al. Identification of human brain tumour initiating cells. Nature 2004; 432(7015): 396– 401.

16. Lobo NA, Shimono Y, Qian D et al. The bio­logy of cancer stem cells. Annu Rev Cell Dev Biol 2007; 23: 675– 699.

17. Pardal R, Clarke MF, Morrison SJ. Applying the principles of stem‑ cell bio­logy to cancer. Nat Rev Cancer 2003; 3(12): 895– 902.

18. Foreman KE, Rizzo OC, Miele L. The cancer stem cell hypothesis. In: Bagley RG (ed.). Stem cells and cancer. 1. vyd. New York: Springer 2009.

19. Arteaga CL. Inhibition of TGFbeta signaling in cancer therapy. Curr Opin Genet Dev 2006; 16(1): 30– 37.

20. Coni S, Infante P, Gulino A. Control of stem cells and cancer stem cells by Hedgehog signaling: pharmacologic clues from pathway dissection. Biochem Pharmacol 2013; 85(5): 623– 628. doi: 10.1016/ j.bcp.2012.11.001.

21. Abel EV, Kim EJ, Wu J et al. The notch pathway is important in maintaining the cancer stem cell population in pancreatic cancer. PLoS One 2014; 9(3). doi: 10.1371/ journal.pone.0091983.

22. Christensen J, Bentz S, Sengstag T et al. FOXQ1, a novel target of the Wnt pathway and a new marker for activation of Wnt signaling in solid tumors. PLoS One 2013; 8(3): e60051. doi: 10.1371/ journal.pone.0060051.

23. Lou H, Dean M. Targeted therapy for cancer stem cells: the patched pathway and ABC transporters. Oncogene 2007; 26(9): 1357– 1360.

24. Reynolds BA, Weiss S. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 1992; 255(5052): 1707– 1710.

25. Miraglia S, Godfrey W, Yin AH et al. A novel five‑ transmembrane hematopoietic stem cell antigen: isolation, characterization, and molecular cloning. Blood 1997; 90(12): 5013– 5021.

26. Wright MH, Calcagno AM, Salcido CD et al. Brca1 breast tumors contain distinct CD44+/ CD24–  and CD133+ cells with cancer stem cell characteristics. Breast Cancer Res 2008; 10(1): R10. doi: 10.1186/ bcr1855.

27. Son MJ, Woolard K, Nam DH et al. SSEA‑ 1 is an enrichment marker for tumor‑ initiating cells in human glioblastoma. Cell Stem Cell 2009; 4(5): 440– 452. doi: 10.1016/ j.stem.2009.03.003.

28. Richichi C, Brescia P, Alberizzi V et al. Marker‑ independent method for isolating slow‑ dividing cancer stem cells in human glioblastoma. Neoplasia 2013; 15(7): 840– 847.

29. Fukaya R, Ohta S, Yamaguchi M et al. Isolation of cancer stem‑like cells from a side population of a human glioblastoma cell line, SK‑ MG‑ 1. Cancer Lett 2010; 291(2): 150– 157. doi: 10.1016/ j.canlet.2009.10.010.

30. Heddleston JM, Li Z, Lathia JD et al. Hypoxia induc­ible factors in cancer stem cells. Br J Cancer 2010; 102(5): 789– 795. doi: 10.1038/ sj.bjc.6605551.

31. Heddleston JM, Li Z, McLendon RE et al. The hypoxic microenvironment maintains glioblastoma stem cells and promotes reprogramming towards a cancer stem cell phenotype. Cell Cycle 2009; 8(20): 3274– 3284.

32. Friedman RC, Farh KK, Burge CB et al. Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 2009; 19(1): 92– 105. doi: 10.1101/ gr.082701.108.

33. Lim LP, Lau NC, Garrett‑ Engele P et al. Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature 2005; 433(7027): 769– 773.

34. Lang MF, Yang S, Zhao C et al. Genome‑ wide profiling identified a set of miRNAs that are differentially expressed in glioblastoma stem cells and normal neural stem cells. PLoS One 2012; 7(4): e36248. doi: 10.1371/ journal.pone.0036248.

35. Kamal M, Shaaban AM, Zhang L et al. Loss of CSMD1 expression is associated with high tumour grade and poor survival in invasive ductal breast carcinoma. Breast Cancer Res Treat 2010; 121(3): 555– 563. doi: 10.1007/ s10549‑ 009‑ 0500‑ 4.

36. Sakaki‑ Yumoto M, Katsuno Y, Derynck R. TGF‑β family signaling in stem cells. Biochim Biophys Acta 2013; 1830(2): 2280– 2296. doi: 10.1016/ j.bbagen.2012.08.008.

37. Tang MR, Wang YX, Guo S et al. CSMD1 exhibits antitumor activity in A375 melanoma cells through activation of the Smad pathway. Apoptosis 2012; 17(9): 927– 937. doi: 10.1007/ s10495‑ 012‑ 0727‑ 0.

38. Guessous F, Alvarado‑ Velez M, Marcinkiewicz L et al. Oncogenic effects of miR‑ 10b in glioblastoma stem cells. J Neurooncol 2013; 112(2): 153– 163. doi: 10.1007/ s11060‑ 013‑ 1047‑ 0.

39. Visvanathan J, Lee S, Lee B et al. The microRNA miR‑ 124 antagonizes the anti‑neural REST/ SCP1 pathway during embryonic CNS development. Genes Dev 2007; 21(7): 744– 749.

40. Conti L, Crisafulli L, Caldera V et al. REST controls self‑ renewal and tumorigenic competence of human glioblastoma cells. PLoS One 2012; 7(6). doi: 10.1371/ journal.pone.0038486.

41. Silber J, Lim DA, Petritsch C et al. miR‑ 124 and miR‑ 137 inhibit proliferation of glioblastoma multiforme cells and induce differentiation of brain tumor stem cells. BMC Med 2008; 6: 14. doi: 10.1186/ 1741‑ 7015‑ 6‑ 14.

42. Bier A, Giladi N, Kronfeld N et al. MicroRNA‑ 137 is downregulated in glioblastoma and inhibits the stemness of glioma stem cells by targeting RTVP‑ 1. Oncotarget 2013; 4(5): 665– 676.

43. Fareh M, Turchi L, Virolle V et al. The miR 302- 367 cluster drastically affects self‑ renewal and infiltration pro­perties of glioma‑ initiating cells through CXCR4 repres­sion and consequent disruption of the SHH‑ GLI‑ NANOG network. Cell Death Differ 2012; 19(2): 232– 244. doi: 10.1038/ cdd.2011.89.

44. Jackson EL, Garcia‑ Verdugo JM, Gil‑ Perotin S et al. PDGFR alpha‑ positive B cells are neural stem cells in the adult SVZ that form glioma‑like growths in response to increased PDGF signaling. Neuron 2006; 51(2): 187– 199.

45. Boockvar JA, Kapitonov D, Kapoor G et al. Constitutive EGFR signaling confers a motile phenotype to neural stem cells. Mol Cell Neurosci 2003; 24(4): 1116– 1130.

46. Papagiannakopoulos T, Friedmann‑Morvinski D, Neveu P et al. Pro‑neural miR‑ 128 is a glioma tumor sup­pressor that targets mitogenic kinases. Oncogene 2012; 31(15): 1884– 1895. doi: 10.1038/ onc.2011.380.

47. Aldaz B, Sagardoy A, Nogueira L et al. Involvement of miRNAs in the differentiation of human glioblastoma multiforme stem‑like cells. PLoS One 2013; 8(10): e77098. doi: 10.1371/ journal.pone.0077098.

48. Li W, Guo F, Wang P et al. miR‑ 221/ 222 confers radioresistance in glioblastoma cells through activating Akt independent of PTEN status. Curr Mol Med 2014; 14(1): 185– 195.

49. Schramedei K, Morbt N, Pfeifer G et al. MicroRNA‑ 21 targets tumor suppressor genes ANP32A and SMARCA4. Oncogene 2011; 30(26): 2975– 2985. doi: 10.1038/ onc.2011.15.

50. Schraivogel D, Weinmann L, Beier D et al. CAMTA1 is a novel tumour suppressor regulated by miR‑ 9/ 9* in glioblastoma stem cells. Embo J 2011; 30(20): 4309– 4322. doi: 10.1038/ emboj.2011.301.

51. Wu N, Xiao L, Zhao X et al. miR‑ 125b regulates the proliferation of glioblastoma stem cells by targeting E2F2. FEBS Lett 2012; 586(21): 3831– 3839. doi: 10.1016/ j.febslet.2012.08.023.

52. Ernst A, Campos B, Meier J et al. De‑ repression of CTGF via the miR‑ 17- 92 cluster upon differentiation of human glioblastoma spheroid cultures. Oncogene 2010; 29(23): 3411– 3422. doi: 10.1038/ onc.2010.83.

53. Asuthkar S, Velpula KK, Chetty C et al. Epigenetic regulation of miRNA‑ 211 by MMP‑ 9 governs glioma cell apoptosis, chemosensitivity and radiosensitivity. Oncotarget 2012; 3(11): 1439– 1454.

54. Li WQ, Li YM, Tao BB et al. Downregulation of ABCG2 expression in glioblastoma cancer stem cells with miRNA‑ 328 may decrease their chemoresistance. Med Sci Monit 2010; 16(10): HY27–HY 30.

55. Pan YZ, Morris ME, Yu AM. MicroRNA‑ 328 negatively regulates the expression of breast cancer resistance protein (BCRP/ ABCG2) in human cancer cells. Mol Pharmacol 2009; 75(6): 1374– 1379. doi: 10.1124/ mol.108.054163.

56. Zhang S, Wan Y, Pan T et al. MicroRNA‑ 21 inhibitor sensitizes human glioblastoma U251 stem cells to chemotherapeutic drug temozolomide. J Mol Neurosci 2012; 47(2): 346– 356. doi: 10.1007/s12031‑ 012‑ 9759‑ 8.

Labels
Paediatric clinical oncology Surgery Clinical oncology
Login
Forgotten password

Enter the email address that you registered with. We will send you instructions on how to set a new password.

Login

Don‘t have an account?  Create new account

#ADS_BOTTOM_SCRIPTS#