Cell and Organ Transplantology. 2015; 3(2):177-183.
DOI: 10.22494/COT.V3I2.10
Brain tumor stem cells: phenotypic characterization and directed therapeutic approaches
Belska L. M., Lisyany M. I.
A. Romodanov State Institute of Neurosurgery NAMS of Ukraine, Kyiv, Ukraine
Abstract
The review presents the current conceptions of the origin, methods of isolation and phenotypic characterization of the brain tumor stem cells. Phenotypic similarity in molecular markers between cancer and neural stem cells is shown. Therapeutic approaches of impact on the brain tumor stem cells and on the intracellular signaling pathways of cancer stem cells are described.
Key words: brain tumor stem cells, neural stem cells, malignant gliomas, CD133, nestin
Full Text PDF (eng) Full Text PDF (ua)1. Bonnet D, Dick JF. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med. 1997; 3:730–737. https://doi.org/10.1038/nm0797-730 PMid:9212098 |
||||
2. Reya T, Morrison SJ, Clarke IL. Stem cells, cancer, and cancer stem cells. Nature. 2001; 414:105–111. https://doi.org/10.1038/35102167 PMid:11689955 |
||||
3. Clevers H. The cancer stem ceil: Premises, promises and challenges. Nat. Med. 2011; 17:313–319. https://doi.org/10.1038/nm.2304 PMid:21386835 |
||||
4. Suetsugu A, Nagaki M, Aokil H. Characterization of CD133+ hepatocellular carcinoma cells as cancer stem/progenitor cells. Biochem Biophys Res Commun. 2006; 29(4):820–824. https://doi.org/10.1016/j.bbrc.2006.10.128 PMid:17097610 |
||||
5. Yuan X, Curtin J, Xiong Y, et al. Isolation of cancer stem cells from adult glioblastoma multiforme. Oncogene. 2004; 16(23):9392–9400. https://doi.org/10.1038/sj.onc.1208311 PMid:15558011 |
||||
6. Vescovi AL, Gall R, Reynolds BA. Brain tumour stem cells. Nat. Rev.Canser. 2006; 6:425–436. https://doi.org/10.1038/nrc1889 PMid:16723989 |
||||
7. Dalerba P, Cho RW, Clarke MF. Cancer stem cells: Models and concepts. Ann. Rev. Med. 2007; 58:267–284. https://doi.org/10.1146/annurev.med.58.062105.204854 PMid:17002552 |
||||
8. Wicha MS. Cancer stem cells and metastasis: Lethal seeds. Clin. Cancer. Res. 2006; 12:5606–5607. https://doi.org/10.1158/1078-0432.CCR-06-1537 PMid:17020960 |
||||
9. Shiras A, Chettiar ST, Shepal V. Spontaneous transformation of human adult nontumorogenic stem sells to cancer stem cells is driven by gemonic instability in a human model of glioblastoma. Stem Cells. 2007; 25(6):1478–1489. https://doi.org/10.1634/stemcells.2006-0585 PMid:17332509 |
||||
10. Masui K, Suzuki SO, Torisu R. Glial progenitors in the brainstem give rise to malignant gliomas by platelet–derived growth factor stimulation. Glia. 2010; 58(9):1050–1065. https://doi.org/10.1002/glia.20986 PMid:20468047 |
||||
11. Junier MP, Sharif A. Instability of cell phenotype and tumor initiating cells in gliomas. Biol. Aujordhui (French). 2011; 205(1):63–74. https://doi.org/10.1051/jbio/2011002 PMid:21501577 |
||||
12. Galli R, Binda E, Orfanelli U. Isolation and characterization of tumorigenic, stem–like neural precursors from human glioblastoma. Cancer Res. 2004; 1(19):7011–7021. https://doi.org/10.1158/0008-5472.CAN-04-1364 PMid:15466194 |
||||
13. Singh SK, Clarke ID, Terasaki M, et al. Identification of a cancer stem cell in human brain tumors. Cancer Res. 2003; 63:5821–5828. PMid:14522905 |
||||
14. Zhang M, Song T, Yang L, et al. Nestin and CD–133: valuable stem cell–specific markers for determing clinical outcome of glioma patients. J. Exp Clin Cancer Res. 2008; 24(27):85–92. https://doi.org/10.1186/1756-9966-27-85 PMid:19108713 PMCid:PMC2633002 |
||||
15. Pallini RL, Ricci–Vitiani L, Montano N. Expression of the stem cell marker CD133 in recurrent glioblastoma and its value for prognosis. Cancer. 2011; 117(1):162–174. https://doi.org/10.1002/cncr.25581 PMid:20806346 |
||||
16. Zeppernick F, Ahmadi R, Campos B, et al. Stem cell marker CD133 affects clinical outcome in glioma patients. Clin Cancer Res. 2008; 14:123–129. https://doi.org/10.1158/1078-0432.CCR-07-0932 PMid:18172261 |
||||
17. Ma YH, Mentlein R, Knerlich F, et al. Expression of stem cell markers in human astrocytomas of different WHO grades. J. Neurooncol. 2008; 86:31–45. https://doi.org/10.1007/s11060-007-9439-7 PMid:17611714 |
||||
18. Kim KJ, Lee KH, Kim HS, et al. The presence of stem cell marker–expressing cells is not prognostically significant in glioblastomas. Neuropathology. 2011; 31:494–502. https://doi.org/10.1111/j.1440-1789.2010.01194.x PMid:21269333 |
||||
19. Lee J, Kotliarova S, Kotliarov Y, et al. Tumor stem cells derived from glioblastomas cultured in bFGF and EGF more closely mirror the phenotype and genotype of primary tumors than do serum–cultured cell lines. Cancer Cell. 2006; 9:391–403. https://doi.org/10.1016/j.ccr.2006.03.030 PMid:16697959 |
||||
20. Bo Qio, Zhang D, Tao J. A simplified and modified procedure to culture brain glioma stem cells from clinical specimens. Oncol Lett. 2012; 1:50–54. | ||||
21. Beier D, Hau P, Proescholdt M. CD133+ and CD133– glioblastoma–derived cancer stem cells show differential growth characteristics and molecular profiles. Cancer Res. 2007; 17(9):4010–4015. https://doi.org/10.1158/0008-5472.CAN-06-4180 PMid:17483311 |
||||
22. Choung YK, Toh TB, Zaiden N. Cryopreservation of neurosphtres derived from human glioblastoma multiforme. Stem Cells. 2009; 27(1):29–39. https://doi.org/10.1634/stemcells.2008-0009 PMid:18845764 PMCid:PMC2729678 |
||||
23. Read TA, Fogarty MP, Markant SL, et al. Identification of CD15 as a marker for tumor–propagating cells in a mouse model of medulloblastoma. Cancer Cell. 2009; 15:135–147. https://doi.org/10.1016/j.ccr.2008.12.016 PMid:19185848 PMCid:PMC2664097 |
||||
24. Son MJ, Woolard K, Nam DH, et al. SSEA–1 is an enrichment marker for tumorinitiating cells in human glioblastoma. Cell Stem Cell. 2009; 4:440–452. https://doi.org/10.1016/j.stem.2009.03.003 PMid:19427293 |
||||
25. He J, Liu Y, Zhuet T, et al. CD90 is identified as a marker for cancer stem cells in primary high–grade gliomas using tissue microarrays. Mol. Cell Proteomics. 2010; 11(6):M111.010744. | ||||
26. Tchoghandjian A, Baeza N, Colin C, et al. A2B5 cells from human glioblastoma have cancer stem cell properties. Brain Pathol. 2010; 20:211–221. https://doi.org/10.1111/j.1750-3639.2009.00269.x PMid:19243384 |
||||
27. Piepmeier JM, Fried I, Makuch R. Low–grade astrocytomas may arise from different astrocyte lineages. Neurosurgery. 1993; 33:627–632. https://doi.org/10.1227/00006123-199310000-00010 PMid:8232801 |
||||
28. Chinnaiyan P, Wang M, Rojiani AM, et al. The prognostic value of nestin expression in newly diagnosed glioblastoma: report from the Radiation Therapy Oncology Group. Radiat Oncol. 2008; 3:32. https://doi.org/10.1186/1748-717X-3-32 PMid:18817556 PMCid:PMC2563009 |
||||
29. Wan F, Herold–Mende C, Campos B, et al. Association of stem cell–related markers and survival in astrocytic gliomas. Biomarker. 2011; 16:136–143. https://doi.org/10.3109/1354750X.2010.536256 PMid:21323603 |
||||
30. Arai H, Ikota H, Sugawara K, et al. Nestin expression in brain tumors: its utility for pathological diagnosis and correlation with the prognosis of high–grade gliomas. Brain Tumor Pathol. 2012; 29:160–167. https://doi.org/10.1007/s10014-012-0081-5 PMid:22350668 |
||||
31. Kim KJ, Lee KH, Kim HS, et al. The presence of stem cell marker–expressing cells is not prognostically significant in glioblastomas. Neuropathology. 2011; 31:494–502. https://doi.org/10.1111/j.1440-1789.2010.01194.x PMid:21269333 |
||||
32. Gangemi RM, Griffero F, Marubbi D, et al. SOX2 silencing in glioblastoma tumor–initiating cells causes stop of proliferation and loss of tumorigenicity. Stem Cells. 2009; 27:40–48. https://doi.org/10.1634/stemcells.2008-0493 PMid:18948646 |
||||
33. Phi JH, Park SH, Kim SK, et al. Sox2 expression in brain tumors: a reflection of the neuroglial differentiation pathway. Am J Surg Pathol. 2008; 32:103–112. https://doi.org/10.1097/PAS.0b013e31812f6ba6 PMid:18162777 |
||||
34. Wan F, Herold–Mende C, Campos B, et al. Association of stem cell–related markers and survival in astrocytic gliomas. Biomarkers. 2011; 16:136–143. https://doi.org/10.3109/1354750X.2010.536256 PMid:21323603 |
||||
35. Mishima K, Kato Y, Kaneko MK, et al. Increased expression of podoplanin in malignant astrocytic tumors as a novel molecular marker of malignant progression. Acta Neuropathol. 2006; 111:483–488. https://doi.org/10.1007/s00401-006-0063-y PMid:16596424 |
||||
36. Venugopal C, Li N, Wang X, et al. Bmi1 marks intermediate precursors during differentiation of human brain tumor initiating cells. Stem Cell Res. 2012; 8:141–153. https://doi.org/10.1016/j.scr.2011.09.008 PMid:22265735 |
||||
37. Hayry V, Tynninen O, Haapasalo HK, et al. Stem cell protein BMI–1 is an independent marker for poor prognosis in oligodendroglial tumour. J. Neuropathol Appl Neurobiol. 2008; 34: 555–563. https://doi.org/10.1111/j.1365-2990.2008.00949.x PMid:18346113 |
||||
38. Hemmati HD, Nakano I, Lazareff JA, et al. Cancerous stem cells can arise from pediatric brain tumors. Proc Natl Acad Sci U S A. 2003; 100:15178–15183. https://doi.org/10.1073/pnas.2036535100 PMid:14645703 PMCid:PMC299944 |
||||
39. Ma YH, Mentlein R, Knerlich F, et al. Expression of stem cell markers in human astrocytomas of different WHO grades. J Neurooncol. 2008; 86:31–45. https://doi.org/10.1007/s11060-007-9439-7 PMid:17611714 |
||||
40. Kanemura Y, Mori K, Sakakibara S, Fujikawa H, et al. Musashi1, an evolutionarily conserved neural RNA–binding protein, is a versatile marker of human glioma cells in determining their cellular origin, malignancy, and proliferative activity. Differentiation. 2001; 68:141–152. https://doi.org/10.1046/j.1432-0436.2001.680208.x PMid:11686236 |
||||
41. Iavarone A, Lasorella A. ID proteins as targets in cancer and tools in neurobiology. Trends Mol Med. 2006; 12:88–594. https://doi.org/10.1016/j.molmed.2006.10.007 PMid:17071138 |
||||
42. Phi JH, Kim JH, Eun KM, et al. Upregulation of SOX2, NOTCH1, and ID1 in supratentorial primitive neuroectodermal tumors: a distinct differentiation pattern from that of medulloblastomas. J Neurosurg Pediatr. 2010; 5:608–614. https://doi.org/10.3171/2010.2.PEDS1065 PMid:20515335 |
||||
43. Du Z, Jia D, Liu S, et al. Oct4 is expressed in human gliomas and promotes colony formation in glioma cells. Glia. 2009; 57:724–733. https://doi.org/10.1002/glia.20800 PMid:18985733 |
||||
44. Guo YL, Liu S, Wang P, et al. Expression profile of embryonic stem cell–associated genes Oct4, Sox2 and Nanog in human gliomas. Histopathology. 2011; 59(4):763–775. https://doi.org/10.1111/j.1365-2559.2011.03993.x PMid:22014056 |
||||
45. Lottaz C, Beier D, Mayer K, et al. Transcriptional profiles of CD133+ and CD133–glioblastoma–derived cancer stem cell lines suggest different ctll of origin. Canser stem cell lines suggest different cell of origin Cancer Res. 2010; 70(5):2030–2040. https://doi.org/10.1158/0008-5472.CAN-09-1707 PMid:20145155 |
||||
47. Jamal M, Rath BN, Tsang P, et al. The brain microenvironment preferentially enhances the radioresistance of CD 133(+) glioblastoma stem–like. Neoplasia. 2012; 14:150–158. https://doi.org/10.1593/neo.111794 PMid:22431923 PMCid:PMC3306260 |
||||
48. He J, Liu Y, Lubman D. Targeting glioblastoma stem cells: cell surface markers. Curr Med Chem. 2012; 19(35):6050–6055. https://doi.org/10.2174/0929867311209066050 PMid:22963566 |
||||
49. Lisyany NI. Immunologija i immunoterapija zlokachestvennyh gliom golovnogo mozga. [Immunology and Immunotherapy of malignant gliomas of the brain]. Serija «Nejroimmunologija». Kiev: Interservis – Series “Neuroimmunology”. Kiev: Interservice. 2011; 5: 240 p. | ||||
50. Purow MW, Haque BW, Noel RM, et al. Expression of Notch–1 and its ligands, Delta–like–1 and Jagged–1, is critical for glioma cell survival and proliferation. Cancer Res. 2005; 65(6):2353–2563. https://doi.org/10.1158/0008-5472.CAN-04-1890 PMid:15781650 |
||||
51. Fan X, Mikolaenko I, Elhassan I, et al. Notch1 and notch2 have opposite effects on embryonal brain tumor growth. Cancer Res. 2004; 64(21):7787–7793. https://doi.org/10.1158/0008-5472.CAN-04-1446 PMid:15520184 |
||||
52. Zhang XP, Zheng G, Zou L, et al. Notch activation promotes cell proliferation and the formation of neural stem cell–like colonies in human glioma cells. Mol Cell Biochem. 2008; 307:101–108. https://doi.org/10.1007/s11010-007-9589-0 PMid:17849174 |
||||
53. Park Y, Rangel C, Reynolds MM, et al. Drosophila perlecan modulates FGF and hedgehog signals to activate neural stem cell division. Dev Bio. 2003; 253(2):247–257. https://doi.org/10.1016/S0012-1606(02)00019-2 |
||||
54. Becher OJ, Hambardzumyan D, Fomchenko EI, et al. Gli activity correlates with tumor grade in platelet–derived growth factor–induced gliomas. Cancer Res. 2008; 68(7):2241–2249. https://doi.org/10.1158/0008-5472.CAN-07-6350 PMid:18381430 |
||||
55. Dahmane N, Sanchez P, Gitton Y, et al. The Sonic Hedgehog–Gli pathway regulates dorsal brain growth and tumorigenesis. Development. 2001; 128:5201–5212. PMid:11748155 |
||||
56. Clement V, Sanchez P, Tribolet N, et al. HEDGEHOG–GLI1 signaling regulates human glioma growth, cancer stem cell self–renewal, and tumorigenicity. Curr Biol: CB. 2007; 17:165–172. https://doi.org/10.1016/j.cub.2006.11.033 PMid:17196391 PMCid:PMC1855204 |
||||
57. Bar EE, Chaudhry A, Lin A, et al. Cyclopamine–mediated hedgehog pathway inhibition depletes stem–like cancer cells in glioblastoma. Stem Cells. 2007; 25:2524–2533. https://doi.org/10.1634/stemcells.2007-0166 PMid:17628016 PMCid:PMC2610257 |
||||
58. Lie DC, Colamarino SA, Song HJ, et al. Wnt signalling regulates adult hippocampal neurogenesis. Nature. 2005; 437(7063):1370–1375. https://doi.org/10.1038/nature04108 PMid:16251967 |
||||
59. Pu P, Zhang Z, Kang C, et al. Downregulation of Wnt2 and betacatenin by siRNA suppresses malignant glioma cell growth. Cancer Gene Ther. 2009; 16(4):351–361. https://doi.org/10.1038/cgt.2008.78 PMid:18949017 |
||||
60. Yu JM, Jun ES, Jung JS, et al. Role of Wnt5a in the proliferation of human glioblastoma cells. Cancer Lett. 2007; 257:172–181. https://doi.org/10.1016/j.canlet.2007.07.011 PMid:17709179 |
Belska LM, Lisyany MI. Brain tumor stem cells: phenotypic characterization and directed therapeutic approaches. Cell and Organ Transplantology. 2015; 3(2):177-183. doi: 10.22494/COT.V3I2.10
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