776
Views
184
CrossRef citations to date
0
Altmetric
Review

The role of glioma stem cells in chemotherapy resistance and glioblastoma multiforme recurrence

, , , &

References

  • Louis DN, Ohgaki H, Wiestler OD, et al. The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol 2007;114(2):97-109
  • Legler JM, Ries LA, Smith MA, et al. Cancer surveillance series [corrected]: brain and other central nervous system cancers: recent trends in incidence and mortality. J Natl Cancer Inst 1999;91(16):1382-90
  • Stupp R, Dietrich PY, Ostermann Kraljevic S, et al. Promising survival for patients with newly diagnosed glioblastoma multiforme treated with concomitant radiation plus temozolomide followed by adjuvant temozolomide. J Clin Oncol 2002;20(5):1375-82
  • Stupp R, Mason WP, van den Bent MJ, et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 2005;352(10):987-96
  • Greaves M, Maley CC. Clonal evolution in cancer. Nature 2012;481(7381):306-13
  • Campbell PJ, Pleasance ED, Stephens PJ, et al. Subclonal phylogenetic structures in cancer revealed by ultra-deep sequencing. Proc Natl Acad Sci USA 2008;105(35):13081-6
  • Ding L, Ellis MJ, Li S, et al. Genome remodelling in a basal-like breast cancer metastasis and xenograft. Nature 2010;464(7291):999-1005
  • Navin N, Kendall J, Troge J, et al. Tumour evolution inferred by single-cell sequencing. Nature 2011;472(7341):90-4
  • Nowell PC. The clonal evolution of tumor cell populations. Science 1976;194(4260):23-8
  • Aparicio S, Caldas C. The implications of clonal genome evolution for cancer medicine. N Engl J Med 2013;368(9):842-51
  • Shapiro JR, Yung WK, Shapiro WR. Isolation, karyotype, and clonal growth of heterogeneous subpopulations of human malignant gliomas. Cancer Res 1981;41(6):2349-59
  • Little SE, Popov S, Jury A, et al. Receptor tyrosine kinase genes amplified in glioblastoma exhibit a mutual exclusivity in variable proportions reflective of individual tumor heterogeneity. Cancer Res 2012;72(7):1614-20
  • Snuderl M, Fazlollahi L, Le LP, et al. Mosaic amplification of multiple receptor tyrosine kinase genes in glioblastoma. Cancer Cell 2011;20(6):810-17
  • Singh SK, Clarke ID, Terasaki M, et al. Identification of a cancer stem cell in human brain tumors. Cancer Res 2003;63(18):5821-8
  • Singh SK, Hawkins C, Clarke ID, et al. Identification of human brain tumour initiating cells. Nature 2004;432(7015):396-401
  • Yuan X, Curtin J, Xiong Y, et al. Isolation of cancer stem cells from adult glioblastoma multiforme. Oncogene 2004;23(58):9392-400
  • Galli R, Binda E, Orfanelli U, et al. Isolation and characterization of tumorigenic, stem-like neural precursors from human glioblastoma. Cancer Res 2004;64(19):7011-21
  • Huang Z, Cheng L, Guryanova OA, et al. Cancer stem cells in glioblastoma – molecular signaling and therapeutic targeting. Protein Cell 2010;1(7):638-55
  • Auffinger B, Tobias AL, Han Y, et al. Conversion of differentiated cancer cells into cancer stem-like cells in a glioblastoma model after primary chemotherapy. Cell Death Differ 2014;21(7):1119-31
  • Ahmed AU, Auffinger B, Lesniak MS. Understanding glioma stem cells: rationale, clinical relevance and therapeutic strategies. Expert Rev Neurother 2013;13(5):545-55
  • Baronchelli S, Bentivegna A, Redaelli S, et al. Delineating the cytogenomic and epigenomic landscapes of glioma stem cell lines. PLoS ONE 2013;8(2):e57462
  • Alcantara Llaguno S, Chen J, Kwon CH, et al. Malignant astrocytomas originate from neural stem/progenitor cells in a somatic tumor suppressor mouse model. Cancer Cell 2009;15(1):45-56
  • Bao S, Wu Q, McLendon RE, et al. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 2006;444(7120):756-60
  • Bobola MS, Blank A, Berger MS, et al. Apurinic/apyrimidinic endonuclease activity is elevated in human adult gliomas. Clin Cancer Res 2001;7(11):3510-18
  • Bartkova J, Hamerlik P, Stockhausen MT, et al. Replication stress and oxidative damage contribute to aberrant constitutive activation of DNA damage signalling in human gliomas. Oncogene 2010;29(36):5095-102
  • 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):HY27-30
  • Wei J, Barr J, Kong LY, et al. Glioma-associated cancer-initiating cells induce immunosuppression. Clin Cancer Res 2010;16(2):461-73
  • Fei S, Qi X, Kedong S, et al. The antitumor effect of mesenchymal stem cells transduced with a lentiviral vector expressing cytosine deaminase in a rat glioma model. J Cancer Res Clin Oncol 2012;138(2):347-57
  • Ropolo M, Daga A, Griffero F, et al. Comparative analysis of DNA repair in stem and nonstem glioma cell cultures. Mol Cancer Res 2009;7(3):383-92
  • Glas M, Rath BH, Simon M, et al. Residual tumor cells are unique cellular targets in glioblastoma. Ann Neurol 2010;68(2):264-9
  • Mao XG, Zhang X, Xue XY, et al. Brain Tumor Stem-Like Cells Identified by Neural Stem Cell Marker CD15. Translat Oncol 2009;2(4):247-57
  • Wang J, Wakeman TP, Lathia JD, et al. Notch promotes radioresistance of glioma stem cells. Stem Cells 2010;28(1):17-28
  • Zhu TS, Costello MA, Talsma CE, et al. Endothelial cells create a stem cell niche in glioblastoma by providing NOTCH ligands that nurture self-renewal of cancer stem-like cells. Cancer Res 2011;71(18):6061-72
  • Wei J, Wu A, Kong LY, et al. Hypoxia potentiates glioma-mediated immunosuppression. PLoS One 2011;6(1):e16195
  • Rosso L, Brock CS, Gallo JM, et al. A new model for prediction of drug distribution in tumor and normal tissues: pharmacokinetics of temozolomide in glioma patients. Cancer Res 2009;69(1):120-7
  • Filatova A, Acker T, Garvalov BK. The cancer stem cell niche(s): the crosstalk between glioma stem cells and their microenvironment. Biochim Biophys Acta 2013;1830(2):2496-508
  • Seidel S, Garvalov BK, Wirta V, et al. A hypoxic niche regulates glioblastoma stem cells through hypoxia inducible factor 2 alpha. Brain 2010;133(Pt 4):983-95
  • Pistollato F, Abbadi S, Rampazzo E, et al. Intratumoral hypoxic gradient drives stem cells distribution and MGMT expression in glioblastoma. Stem Cells 2010;28(5):851-62
  • Wu A, Wei J, Kong LY, et al. Glioma cancer stem cells induce immunosuppressive macrophages/microglia. Neuro Oncol 2010;12(11):1113-25
  • Gautschi OP, Cadosch D, Collen TD, et al. [Glioblastoma multiforme–new hope due to modern therapeutical approaches]. Praxis 2010;99(5):295-308
  • Pardridge WM. Drug transport across the blood-brain barrier. J Cerebral Blood Flow Metab 2012;32(11):1959-72
  • Brada M, Judson I, Beale P, et al. Phase I dose-escalation and pharmacokinetic study of temozolomide (SCH 52365) for refractory or relapsing malignancies. Br J Cancer 1999;81(6):1022-30
  • Ostermann S, Csajka C, Buclin T, et al. Plasma and cerebrospinal fluid population pharmacokinetics of temozolomide in malignant glioma patients. Clin Cancer Res 2004;10(11):3728-36
  • Portnow J, Badie B, Chen M, et al. The neuropharmacokinetics of temozolomide in patients with resectable brain tumors: potential implications for the current approach to chemoradiation. Clin Cancer Res 2009;15(22):7092-8
  • Beier D, Rohrl S, Pillai DR, et al. Temozolomide preferentially depletes cancer stem cells in glioblastoma. Cancer Res 2008;68(14):5706-15
  • Blough MD, Westgate MR, Beauchamp D, et al. Sensitivity to temozolomide in brain tumor initiating cells. Neuro-oncol 2010;12(7):756-60
  • Hermisson M, Klumpp A, Wick W, et al. O6-methylguanine DNA methyltransferase and p53 status predict temozolomide sensitivity in human malignant glioma cells. J Neurochem 2006;96(3):766-76
  • Liu G, Yuan X, Zeng Z, et al. Analysis of gene expression and chemoresistance of CD133+ cancer stem cells in glioblastoma. Mol Cancer 2006;5:67
  • Hegi ME, Diserens AC, Gorlia T, et al. MGMT gene silencing and benefit from temozolomide in glioblastoma. N Engl J Med 2005;352(10):997-1003
  • Beier D, Schulz JB, Beier CP. Chemoresistance of glioblastoma cancer stem cells–much more complex than expected. Mol Cancer 2011;10:128
  • Sorensen MD, Fosmark S, Hellwege S, et al. Chemoresistance and chemotherapy targeting stem-like cells in malignant glioma. Adv Exp Med Biol 2015;853:111-38
  • Bleau AM, Hambardzumyan D, Ozawa T, et al. PTEN/PI3K/Akt pathway regulates the side population phenotype and ABCG2 activity in glioma tumor stem-like cells. Cell Stem Cell 2009;4(3):226-35
  • Clement V, Sanchez P, de Tribolet N, et al. HEDGEHOG-GLI1 signaling regulates human glioma growth, cancer stem cell self-renewal, and tumorigenicity. Curr Biol 2007;17(2):165-72
  • Schatton T, Murphy GF, Frank NY, et al. Identification of cells initiating human melanomas. Nature 2008;451(7176):345-9
  • Hirschmann-Jax C, Foster AE, Wulf GG, et al. A distinct "side population" of cells with high drug efflux capacity in human tumor cells. Proc Natl Acad Sci USA 2004;101(39):14228-33
  • Hjelmeland AB, Wu Q, Heddleston JM, et al. Acidic stress promotes a glioma stem cell phenotype. Cell Death Differ 2011;18(5):829-40
  • Wang J, Sakariassen PO, Tsinkalovsky O, et al. CD133 negative glioma cells form tumors in nude rats and give rise to CD133 positive cells. Int J Canc 2008;122(4):761-8
  • Chen R, Nishimura MC, Bumbaca SM, et al. A hierarchy of self-renewing tumor-initiating cell types in glioblastoma. Cancer Cell 2010;17(4):362-75
  • Dahan P, Martinez Gala J, Delmas C, et al. Ionizing radiations sustain glioblastoma cell dedifferentiation to a stem-like phenotype through survivin: possible involvement in radioresistance. Cell Death Dis 2014;5:e1543
  • Phillips HS, Kharbanda S, Chen R, et al. Molecular subclasses of high-grade glioma predict prognosis, delineate a pattern of disease progression, and resemble stages in neurogenesis. Cancer Cell 2006;9(3):157-73
  • Sturm D, Witt H, Hovestadt V, et al. Hotspot mutations in H3F3A and IDH1 define distinct epigenetic and biological subgroups of glioblastoma. Cancer Cell 2012;22(4):425-37
  • Verhaak RG, Hoadley KA, Purdom E, et al. Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell 2010;17(1):98-110
  • Brennan CW, Verhaak RG, McKenna A, et al. The somatic genomic landscape of glioblastoma. Cell 2013;155(2):462-77
  • Lu C, Ward PS, Kapoor GS, et al. IDH mutation impairs histone demethylation and results in a block to cell differentiation. Nature 2012;483(7390):474-8
  • Mao P, Joshi K, Li J, et al. Mesenchymal glioma stem cells are maintained by activated glycolytic metabolism involving aldehyde dehydrogenase 1A3. Proc Natl Acad Sci USA 2013;110(21):8644-9
  • Yip S, Miao J, Cahill DP, et al. MSH6 mutations arise in glioblastomas during temozolomide therapy and mediate temozolomide resistance. Clin Cancer Res 2009;15(14):4622-9
  • Johannessen TC, Bjerkvig R, Tysnes BB. DNA repair and cancer stem-like cells–potential partners in glioma drug resistance? Cancer Treat Rev 2008;34(6):558-67
  • Wharton SB, McNelis U, Bell HS, Whittle IR. Expression of poly(ADP-ribose) polymerase and distribution of poly(ADP-ribosyl)ation in glioblastoma and in a glioma multicellular tumour spheroid model. Neuropathol Appl Neurobiol 2000;26(6):528-35
  • Bartek J, Lukas J. Chk1 and Chk2 kinases in checkpoint control and cancer. Cancer Cell 2003;3(5):421-9
  • Xu ZY, Wang K, Li XQ, et al. The ABCG2 transporter is a key molecular determinant of the efficacy of sonodynamic therapy with Photofrin in glioma stem-like cells. Ultrasonics 2013;53(1):232-8
  • Golebiewska A, Bougnaud S, Stieber D, et al. Side population in human glioblastoma is non-tumorigenic and characterizes brain endothelial cells. Brain 2013;136(Pt 5):1462-1475
  • Cui D, Xu Q, Wang K, Che X. Gli1 is a potential target for alleviating multidrug resistance of gliomas. J Neurol Sci 2010;288(1-2):156-66
  • Haar CP, Hebbar P, Wallace GC, et al. Drug resistance in glioblastoma: a mini review. Neurochem Res 2012;37(6):1192-200
  • Martin V, Xu J, Pabbisetty SK, et al. Tie2-mediated multidrug resistance in malignant gliomas is associated with upregulation of ABC transporters. Oncogene 2009;28(24):2358-63
  • Gong W, Wang Z, Wan Y, et al. Downregulation of ABCG2 protein inhibits migration and invasion in U251 glioma stem cells. Neuroreport 2014;25(8):625-32
  • Kanno H, Sato H, Yokoyama TA, et al. The VHL tumor suppressor protein regulates tumorigenicity of U87-derived glioma stem-like cells by inhibiting the JAK/STAT signaling pathway. Int J Oncol 2013;42(3):881-6
  • Korkaya H, Paulson A, Charafe-Jauffret E, et al. Regulation of mammary stem/progenitor cells by PTEN/Akt/beta-catenin signaling. PLoS Biol 2009;7(6):e1000121
  • Nduom EK, Hadjipanayis CG, Van Meir EG. Glioblastoma cancer stem-like cells: implications for pathogenesis and treatment. Cancer J 2012;18(1):100-6
  • Rheinbay E, Suva ML, Gillespie SM, et al. An aberrant transcription factor network essential for Wnt signaling and stem cell maintenance in glioblastoma. Cell Rep 2013;3(5):1567-79
  • Vescovi AL, Galli R, Reynolds BA. Brain tumour stem cells. Nat Rev Cancer 2006;6(6):425-36
  • Zhou BB, Zhang H, Damelin M, et al. Tumour-initiating cells: challenges and opportunities for anticancer drug discovery. Nat Rev Drug Discov 2009;8(10):806-23
  • Park DM, Rich JN. Biology of glioma cancer stem cells. Mol Cells 2009;28(1):7-12
  • Piccirillo SG, Reynolds BA, Zanetti N, et al. Bone morphogenetic proteins inhibit the tumorigenic potential of human brain tumour-initiating cells. Nature 2006;444(7120):761-5
  • Gal H, Pandi G, Kanner AA, et al. MIR-451 and Imatinib mesylate inhibit tumor growth of Glioblastoma stem cells. Biochem Biophys Res Commun 2008;376(1):86-90
  • 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):3411-22
  • 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
  • Liong C, Ortiz D, Ao-ieong E, et al. Localized increase of tissue oxygen tension by magnetic targeted drug delivery. Nanotechnology 2014;25(26):265102
  • 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):3274-84
  • Gillespie DL, Aguirre MT, Ravichandran S, et al. RNA interference targeting hypoxia-inducible factor 1alpha via a novel multifunctional surfactant attenuates glioma growth in an intracranial mouse model. J Neurosurg 2015;122(2):331-41
  • Teodorczyk M, Schmidt MH. Notching on Cancer’s Door: Notch Signaling in Brain Tumors. Front Oncol 2014;4:341
  • Galan-Moya EM, Le Guelte A, Lima Fernandes E, et al. Secreted factors from brain endothelial cells maintain glioblastoma stem-like cell expansion through the mTOR pathway. EMBO Rep 2011;12(5):470-6
  • Lathia JD, Li M, Hall PE, et al. Laminin alpha 2 enables glioblastoma stem cell growth. Ann Neurol 2012;72(5):766-78
  • Ulasov IV, Nandi S, Dey M, et al. Inhibition of Sonic hedgehog and Notch pathways enhances sensitivity of CD133(+) glioma stem cells to temozolomide therapy. Mol Med 2011;17(1-2):103-12
  • Ricci-Vitiani L, Pallini R, Biffoni M, et al. Tumour vascularization via endothelial differentiation of glioblastoma stem-like cells. Nature 2010;468(7325):824-8
  • Wang CH, Chiou SH, Chou CP, et al. Photothermolysis of glioblastoma stem-like cells targeted by carbon nanotubes conjugated with CD133 monoclonal antibody. Nanomedicine 2011;7(1):69-79
  • Smith LM, Nesterova A, Ryan MC, et al. CD133/prominin-1 is a potential therapeutic target for antibody-drug conjugates in hepatocellular and gastric cancers. Br J Cancer 2008;99(1):100-9
  • Wu ZB, Qiu C, Zhang AL, et al. Glioma-associated antigen HEATR1 induces functional cytotoxic T lymphocytes in patients with glioma. J Immunol Res 2014;2014:131494
  • Bielamowicz K, Khawja S, Ahmed N. Adoptive cell therapies for glioblastoma. Front Oncol 2013;3:275
  • Wu J, Lai G, Wan F, et al. Knockdown of checkpoint kinase 1 is associated with the increased radiosensitivity of glioblastoma stem-like cells. Tohoku J Exp Med 2012;226(4):267-74
  • Nadkarni A, Shrivastav M, Mladek AC, et al. ATM inhibitor KU-55933 increases the TMZ responsiveness of only inherently TMZ sensitive GBM cells. J Neurooncol 2012;110(3):349-57
  • Signore M, Pelacchi F, di Martino S, et al. Combined PDK1 and CHK1 inhibition is required to kill glioblastoma stem-like cells in vitro and in vivo. Cell Death Dis 2014;5:e1223
  • Vecchio D, Daga A, Carra E, et al. Predictability, efficacy and safety of radiosensitization of glioblastoma-initiating cells by the ATM inhibitor KU-60019. Int J Cancer 2014;135(2):479-91
  • Facchino S, Abdouh M, Chatoo W, Bernier G. BMI1 confers radioresistance to normal and cancerous neural stem cells through recruitment of the DNA damage response machinery. J Neurosci 2010;30(30):10096-111
  • Imai Y, Yoshimori M, Fukuda K, et al. The PI3K/Akt inhibitor LY294002 reverses BCRP-mediated drug resistance without affecting BCRP translocation. Oncol Rep 2012;27(6):1703-9
  • Martín V, Sanchez-Sanchez AM, Herrera F, et al. Melatonin-induced methylation of the ABCG2/BCRP promoter as a novel mechanism to overcome multidrug resistance in brain tumour stem cells. Br J Cancer 2013;108(10):2005-12
  • Carra E, Barbieri F, Marubbi D, et al. Sorafenib selectively depletes human glioblastoma tumor-initiating cells from primary cultures. Cell Cycle 2013;12(3):491-500
  • Aldea MD, Petrushev B, Soritau O, et al. Metformin plus sorafenib highly impacts temozolomide resistant glioblastoma stem-like cells. J BUON 2014;19(2):502-11
  • Chang CJ, Hsu CC, Yung MC, et al. Enhanced radiosensitivity and radiation-induced apoptosis in glioma CD133-positive cells by knockdown of SirT1 expression. Biochem Biophys Res Commun 2009;380(2):236-42
  • Cheng L, Wu Q, Guryanova OA, et al. Elevated invasive potential of glioblastoma stem cells. Biochem Biophys Res Commun 2011;406(4):643-8
  • Scatena R, Bottoni P, Pontoglio A, Giardina B. Cancer stem cells: the development of new cancer therapeutics. Expert Opin Biol Ther 2011;11(7):875-92
  • Inda MM, Bonavia R, Mukasa A, et al. Tumor heterogeneity is an active process maintained by a mutant EGFR-induced cytokine circuit in glioblastoma. Genes Dev 2010;24(16):1731-45

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.