The evolving landscape of glioblastoma stem cells

Current Opinion in Neurology

Volumn 26, Issue 6, 2013, Pages 701-707

  Yan, Kenneth ^a,b,c   Yang, Kailin ^a,c   Rich, Jeremy N ^a  

^a LERNER RESEARCH INSTITUTE   (United States)

^b CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c CASE WESTERN RESERVE UNIVERSITY   (United States)

Author keywords

Cancer stem cells; Glioblastoma; Glioma stem cells

Indexed keywords

MICRORNA 124; MICRORNA 125B; MICRORNA 1275; MICRORNA 137; MICRORNA 143; MICRORNA 145; MICRORNA 18A; MICRORNA 204; MICRORNA 21; MICRORNA 211; MICRORNA 23B; MICRORNA 452; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

CANCER GENETICS; CANCER RESISTANCE; CANCER STEM CELL; CELL ACTIVATION; CELL FUNCTION; CELL INVASION; CELL METABOLISM; CELL RENEWAL; CELL SPECIFICITY; CELL SURVIVAL; CONTROLLED CLINICAL TRIAL (TOPIC); EPIGENETICS; GLIOBLASTOMA; HUMAN; INTRACELLULAR SIGNALING; NEOVASCULARIZATION (PATHOLOGY); NONHUMAN; PHENOTYPE; REVIEW; TARGET CELL; TRANSCRIPTION REGULATION; TUMOR GROWTH; TUMOR INVASION; TUMOR MICROENVIRONMENT; TUMOR VASCULARIZATION; ANIMAL; BRAIN TUMOR; CELL DIFFERENTIATION; PATHOLOGY; PHYSIOLOGY; TUMOR RECURRENCE;

ANIMALS; BRAIN NEOPLASMS; CELL DIFFERENTIATION; GLIOBLASTOMA; HUMANS; NEOPLASM RECURRENCE, LOCAL; NEOPLASTIC STEM CELLS;

EID: 84892441562     PISSN: 13507540     EISSN: 14736551     Source Type: Journal    
DOI: 10.1097/WCO.0000000000000032     Document Type: Review

References (68)

1. Stupp R, Hegi ME, Mason WP, et al. Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase III study: 5-year analysis of the EORTC-NCIC trial. Lancet Oncol 2009; 10:459-466.
2. Cancer Genome Atlas Research Network. Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature 2008; 455:1061-1068.
3. Parsons DW, Jones S, Zhang X, et al. An integrated genomic analysis of human glioblastoma multiforme. Science 2008; 321:1807-1812.
4. 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; 17:98-110.
5. Singh SK, Hawkins C, Clarke I D, et al. Identification of human brain tumour initiating cells. Nature 2004; 432:396-401.
6. Hemmati HD, Nakano I, Lazareff JA, et al. Cancerous stem cells can arise from pediatric brain tumors. Proc Natl Acad Sci USA 2003; 100:15178- 15183.
7. Bao S, Wu Q, McLendon RE, et al. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 2006; 444:756-760.
8. 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.
9. Bao S, Wu Q, Sathornsumetee S, et al. Stem cell-like glioma cells promote tumor angiogenesis through vascular endothelial growth factor. Cancer Res 2006; 66:7843-7848.
10. hen J, Li Y, Yu TS, et al. A restricted cell population propagates glioblastoma growth after chemotherapy. Nature 2012; 488:522-526.
11. Gao X, McDonald JT, Hlatky L, Enderling H. Acute and fractionated irradiation differentially modulate glioma stem cell division kinetics. Cancer Res 2013; 73:1481-1490.
12. Wang J, Wakeman TP, Lathia JD, et al. Notch promotes radioresistance of glioma stem cells. Stem Cells 2010; 28:17-28.
13. Jin X, Jeon HY, Joo KM, et al. Frizzled 4 regulates stemness and invasiveness of migrating glioma cells established by serial intracranial transplantation. Cancer Res 2011; 71:3066-3075.
14. Piccirillo SG, Reynolds BA, Zanetti N, et al. Bone morphogenetic proteins inhibit the tumorigenic potential of human brain tumour-initiating cells. Nature 2006; 444:761-765.
15. Ikushima H, Todo T, Ino Y, et al. Autocrine TGF-beta signaling maintains tumorigenicity of glioma-initiating cells through Sry-related HMG-box factors. Cell Stem Cell 2009; 5:504-514.
16. Penuelas S, Anido J, Prieto-Sanchez RM, et al. TGF-beta increases gliomainitiating cell self-renewal through the induction of LIF in human glioblastoma. Cancer Cell 2009; 15:315-327.
17. Soeda A, Inagaki A, Oka N, et al. Epidermal growth factor plays a crucial role in mitogenic regulation of human brain tumor stem cells. J Biol Chem 2008; 283:10958-10966.
18. Eyler CE, Foo WC, LaFiura KM, et al. Brain cancer stem cells display preferential sensitivity to Akt inhibition. Stem Cells 2008; 26:3027-3036.
19. 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.
20. Godlewski J, Nowicki MO, Bronisz A, et al. Targeting of the Bmi-1 oncogene/ stem cell renewal factor by microRNA-128 inhibits glioma proliferation and self-renewal. Cancer Res 2008; 68:9125-9130.
21. Calabrese C, Poppleton H, Kocak M, et al. A perivascular niche for brain tumor stem cells. Cancer Cell 2007; 11:69-82.
22. Li Z, Bao S, Wu Q, et al. Hypoxia-inducible factors regulate tumorigenic capacity of glioma stem cells. Cancer Cell 2009; 15:501-513.
23. Hjelmeland AB, Wu Q, Heddleston JM, et al. Acidic stress promotes a glioma stem cell phenotype. Cell Death Differ 2011; 18:829-840.
24. .Wei Y, Jiang Y, Zou F, et al. Activation of PI3K/Akt pathway by CD133-p85 interaction promotes tumorigenic capacity of glioma stem cells. Proc Natl Acad Sci USA 2013; 110:6829-6834.
25. Pasquale EB. Eph-ephrin bidirectional signaling in physiology and disease. Cell 2008; 133:38-52.
26. Binda E, Visioli A, Giani F, et al. The EphA2 receptor drives self-renewal and tumorigenicity in stem-like tumor-propagating cells from human glioblastomas Cancer Cell 2012; 22:765-780.
27. Day BW, Stringer BW, Al-Ejeh F, et al. EphA3 maintains tumorigenicity and is a therapeutic target in glioblastoma multiforme. Cancer Cell 2013; 23:238- 248.
28. Kim Y, Kim E, Wu Q, et al. Platelet-derived growth factor receptors differentially inform intertumoral and intratumoral heterogeneity. Genes Dev 2012; 26:1247-1262.
29. Joo KM, Jin J, Kim E, et al. MET signaling regulates glioblastoma stem cells. Cancer Res 2012; 72:3828-3838.
30. Li Y, Li A, Glas M, et al. c-Met signaling induces a reprogramming network and supports the glioblastoma stem-like phenotype. Proc Natl Acad Sci USA 2011; 108:9951-9956.
31. Kim KH, Seol HJ, Kim EH, et al. Wnt/beta-catenin signaling is a key downstream mediator of MET signaling in glioblastoma stem cells. Neuro Oncol 2013; 15:161-171.
32. De Bacco F, Casanova E, Medico E, et al. The MET oncogene is a functional marker of a glioblastoma stem cell subtype. Cancer Res 2012; 72:4537- 4550.
33. Jahangiri A, De Lay M, Miller LM, et al. Gene expression profile identifies tyrosine kinase c-Met as a targetable mediator of antiangiogenic therapy resistance. Clin Cancer Res 2013; 19:1773-1783.
34. .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; 3:1567-1579.
35. Soroceanu L, Murase R, Limbad C, et al. Id-1 is a key transcriptional regulator of glioblastoma aggressiveness and a novel therapeutic target. Cancer Res 2013; 73:1559-1569.
36. Lee C, Fotovati A, Triscott J, et al. Polo-like kinase 1 inhibition kills glioblastoma multiforme brain tumor cells in part through loss of SOX2 and delays tumor progression in mice. Stem Cells 2012; 30:1064-1075.
37. Bazzoli E, Pulvirenti T, Oberstadt MC, et al. MEF promotes stemness in the pathogenesis of gliomas. Cell Stem Cell 2012; 11:836-844.
38. Joshi K, Banasavadi-Siddegowda Y, Mo X, et al. MELK-dependent FOXM1 phosphorylation is essential for proliferation of glioma stem cells. Stem Cells 2013; 31:1051-1063.
39. Gu C, Banasavadi-Siddegowda YK, Joshi K, et al. Tumor-specific activation of the C-JUN/MELK pathway regulates glioma stem cell growth in a p53-dependent manner. Stem Cells 2013; 31:870-881.
40. * in glioma initiating cells requires NOTCH-1 signaling. Stem Cells 2013; 31:1252-1265.
41. Polajeva J, Swartling FJ, Jiang Y, et al. miRNA-21 is developmentally regulated in mouse brain and is co-expressed with SOX2 in glioma. BMC Cancer 2012; 12:378.
42. Geng J, Luo H, Pu Y, et al. Methylation mediated silencing of miR-23b expression and its role in glioma stemcells.Neurosci Lett2012;528:185-189.
43. Wei J, Wang F, Kong LY, et al. miR-124 inhibits STAT3 signaling to enhance T cell-mediated immune clearance of glioma. Cancer Res 2013; 73:3913- 3926.
44. Wu N, Xiao L, Zhao X, et al. miR-125b regulates the proliferation of glioblastoma stem cells by targeting E2F2. FEBS Lett 2012; 586:3831-3839.
45. Shi L, Wan Y, Sun G, et al. Functional differences of miR-125b on the invasion of primary glioblastoma CD133-negative cells and CD133-positive cells. Neuromol Med 2012; 14:303-316.
46. 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; 4:665-676.
47. Zhao S, Liu H, Liu Y, et al. miR-143 inhibits glycolysis and depletes stemness of glioblastoma stem-like cells. Cancer Lett 2013; 333:253-260.
48. Lee HK, Bier A, Cazacu S, et al. MicroRNA-145 is downregulated in glial tumors and regulates glioma cell migration by targeting connective tissue growth factor. PLoS One 2013; 8:e54652.
49. Ying Z, Li Y, Wu J, et al. Loss of miR-204 expression enhances glioma migration and stem cell-like phenotype. Cancer Res 2013; 73:990-999.
50. 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; 3:1439-1454.
51. Liu L, Chen K, Wu J, et al. Downregulation of miR-452 promotes stem-like traits and tumorigenicity of gliomas. Clin Cancer Res 2013; 19:3429-3438.
52. Katsushima K, Shinjo K, Natsume A, et al. Contribution of microRNA-1275 to Claudin11 protein suppression via a polycomb-mediated silencing mechanism in human glioma stem-like cells. J Biol Chem 2012; 287:27396-27406.
53. Gargiulo G, Cesaroni M, Serresi M, et al. In vivo RNAi screen for BMI1 targets identifies TGF-beta/BMP-ER stress pathways as key regulators of neural- And malignant glioma-stem cell homeostasis. Cancer Cell 2013; 23:660-676.
54. Kim E, Kim M, Woo DH, et al. Phosphorylation of EZH2 activates STAT3 signaling via STAT3 methylation and promotes tumorigenicity of glioblastoma stem-like cells. Cancer Cell 2013; 23:839-852.
55. Lewis PW, Muller MM, Koletsky MS, et al. Inhibition of PRC2 activity by a gain-of-function H3 mutation found in pediatric glioblastoma. Science 2013; 340:857-861.
56. Natsume A, Ito M, Katsushima K, et al. Chromatin regulator PRC2 is a key regulator of epigenetic plasticity in glioblastoma. Cancer Res 2013; 73:4559-4570.
57. Gallo M, Ho J, Coutinho FJ, et al. A tumorigenic MLL-homeobox network in human glioblastoma stem cells. Cancer Res 2013; 73:417-427.
58. Gopisetty G, Xu J, Sampath D, et al. Epigenetic regulation of CD133/PROM1 expression in glioma stem cells by Sp1/myc and promoter methylation. Oncogene 2013; 32:3119-3129.
59. Vander Heiden MG, Cantley LC, Thompson CB. Understanding the Warburg effect: The metabolic requirements of cell proliferation. Science 2009; 324:1029-1033.
60. Vlashi E, Lagadec C, Vergnes L, et al.Metabolic state of glioma stem cells and nontumorigenic cells. Proc Natl Acad Sci USA 2011; 108:16062-16067.
61. 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; 110:8644-8649.
62. Janiszewska M, Suva ML, Riggi N, et al. Imp2 controls oxidative phosphorylation and is crucial for preserving glioblastoma cancer stem cells. Genes Dev 2012; 26:1926-1944.
63. 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; 8:3274- 3284.
64. Wang R, Chadalavada K, Wilshire J, et al. Glioblastoma stem-like cells give rise to tumour endothelium. Nature 2010; 468:829-833.
65. Ricci-Vitiani L, Pallini R, Biffoni M, et al. Tumour vascularization via endothelial differentiation of glioblastoma stem-like cells. Nature 2010; 468:824- 828.
66. .Cheng L, Huang Z, Zhou W, et al. Glioblastoma stem cells generate vascular pericytes to support vessel function and tumor growth. Cell 2013; 153:139- 152.
67. Ye XZ, Xu SL, Xin YH, et al. Tumor-associated microglia/macrophages enhance the invasion of glioma stem-like cells via TGF-beta1 signaling pathway. J Immunol 2012; 189:444-453.
68. Hardee ME, Marciscano AE, Medina-Ramirez CM, et al. Resistance of glioblastoma-initiating cells to radiation mediated by the tumor microenvironment can be abolished by inhibiting transforming growth factor-beta. Cancer Res 2012; 72:4119-4129.