Core pathway mutations induce de-differentiation of murine astrocytes into glioblastoma stem cells that are sensitive to radiation but resistant to temozolomide

Neuro-Oncology

Volumn 18, Issue 7, 2016, Pages 962-973

  Schmid, Ralf S ^a   Simon, Jeremy M ^a   Vitucci, Mark ^a   McNeill, Robert S ^a   Bash, Ryan E ^a   Werneke, Andrea M ^a   Huey, Lauren ^a   White, Kristen K ^a   Ewend, Matthew G ^a   Wu, Jing ^a   Miller, C Ryan ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

Astrocytes; glioblastoma; glioma stem cells; radiation; temozolomide

Indexed keywords

CD133 ANTIGEN; FORMALDEHYDE; K RAS PROTEIN; METHYLATED DNA PROTEIN CYSTEINE METHYLTRANSFERASE; NESTIN; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; RETINOBLASTOMA PROTEIN; TEMOZOLOMIDE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR HOXA; TRANSCRIPTION FACTOR SOX2; TRANSCRIPTOME; UNCLASSIFIED DRUG; DACARBAZINE;

ALLOGRAFT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTROCYTE; ASTROCYTE CULTURE; CANCER RADIOTHERAPY; CANCER SURVIVAL; CELL DEDIFFERENTIATION; CELL DIFFERENTIATION; CELL LINEAGE; CELL RENEWAL; CHROMATIN; CONTROLLED STUDY; DISEASE MODEL; DOWN REGULATION; DRUG EFFICACY; GENE; GENE ACTIVATION; GENE DELETION; GENE EXPRESSION PROFILING; GENE LOCUS; GENE MUTATION; GENE SILENCING; GENETIC ENGINEERING; GLIOBLASTOMA; IN VITRO STUDY; IN VIVO STUDY; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; ONCOGENE K RAS; ORTHOTOPIC TRANSPLANTATION; PROTEIN EXPRESSION; PTEN GENE; RADIOSENSITIVITY; RB GENE; REGULATORY SEQUENCE; RNA SEQUENCE; SIGNAL TRANSDUCTION; UPREGULATION; ANALOGS AND DERIVATIVES; ANIMAL; BRAIN NEOPLASMS; CANCER STEM CELL; CYTOLOGY; DRUG EFFECTS; DRUG RESISTANCE; GENETICS; METABOLISM; MUTATION; PATHOLOGY; RADIATION RESPONSE; TRANSGENIC MOUSE; TUMOR CELL LINE;

ANIMALS; ASTROCYTES; BRAIN NEOPLASMS; CELL DIFFERENTIATION; CELL LINE, TUMOR; DACARBAZINE; DRUG RESISTANCE, NEOPLASM; GLIOBLASTOMA; MICE, TRANSGENIC; MUTATION; NEOPLASTIC STEM CELLS; SIGNAL TRANSDUCTION;

EID: 84977478852     PISSN: 15228517     EISSN: 15235866     Source Type: Journal    
DOI: 10.1093/neuonc/nov321     Document Type: Article

References (61)

1. Ostrom QT, Gittleman H, Liao P, et al. CBTRUS statistical report: primary brain and central nervous system tumors diagnosed in the United States in 2007-2011. Neuro Oncol. 2014;16: (suppl 4):iv1-i63.
2. 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):987-996.
3. Galli R, Binda E, Orfanelli U, et al. Isolation and characterization of tumorigenic, stem-like neural precursors fromhuman glioblastoma. Cancer Res. 2004;64(19):7011-7021.
4. Singh SK, Hawkins C, Clarke ID, et al. Identification of human brain tumour initiating cells. Nature. 2004;432(7015):396-401.
5. Vescovi AL, Galli R, Reynolds BA. Brain tumour stem cells. Nat Rev Cancer. 2006;6(6):425-436.
6. 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):756-760.
7. Beier D, Schulz JB, Beier CP. Chemoresistance of glioblastoma cancer stem cells-much more complex than expected. Mol Cancer. 2011;10:128.
8. Weller M, Stupp R, Reifenberger G, et al. MGMT promoter methylation in malignant gliomas: ready for personalized medicine? Nat Rev Neurol. 2010;6(1):39-51.
9. 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.
10. Vitucci M, Hayes DN, Miller CR. Gene expression profiling of gliomas: merging genomic and histopathological classification for personalised therapy. Br J Cancer. 2011;104(4):545-553.
11. The Cancer Genome Atlas Research Network. Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature. 2008;455(7216):1061-1068.
12. 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):157-173.
13. 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.
14. Brennan CW, Verhaak RG, McKenna A, et al. The somatic genomic landscape of glioblastoma. Cell. 2013;155(2):462-477.
15. Schmid RS, Vitucci M, Miller CR. Genetically engineered mouse models of diffuse gliomas. Brain Res Bull. 2012;88(1):72-79.
16. McNeill RS, Vitucci M, Wu J, Miller CR. Contemporary murine models in preclinical astrocytoma drug development. Neuro Oncol. 2015;17(1):12-28.
17. Vitucci M, Karpinich NO, Bash RE, et al. Cooperativity between MAPK and PI3 K signaling activation is required for glioblastoma pathogenesis. Neuro Oncol. 2013;15(10):1317-1329.
18. McNeill RS, Schmid RS, Bash RE, et al. Modeling astrocytoma pathogenesis in vitro and in vivo using cortical astrocytes or neural stem cells from conditional, genetically engineered mice. J Vis Exp. 2014;(90):e51763.
19. Prabhu A, Sarcar B, Miller CR, et al. Ras-mediated modulation of pyruvate dehydrogenase activity regulates mitochondrial reserve capacity and contributes to glioblastoma tumorigenesis. Neuro Oncol. 2015;17(9):1220-1230.
20. Song Y, Zhang Q, Kutlu B, et al. Evolutionary etiology of high-grade astrocytomas. Proc Natl Acad Sci USA. 2013;110(44):17933-17938.
21. Xiao A, Wu H, Pandolfi PP, Louis DN, Van Dyke T. Astrocyte inactivation of the pRb pathway predisposes mice to malignant astrocytoma development that is accelerated by PTEN mutation. Cancer Cell. 2002;1(2):157-168.
22. Dinca EB, Sarkaria JN, Schroeder MA, et al. Bioluminescence monitoring of intracranial glioblastoma xenograft: response to primary and salvage temozolomide therapy. J Neurosurg. 2007; 107(3):610-616.
23. Buszczak M, Spradling AC. Searching chromatin for stem cell identity. Cell. 2006;125(2):233-236.
24. Song L, Zhang Z, Grasfeder LL, et al. Open chromatin defined by DNaseI and FAIRE identifies regulatory elements that shape cell-type identity. Genome Res. 2011;21(10):1757-1767.
25. Salhia B, Tran NL, Chan A, et al. The guanine nucleotide exchange factors trio, Ect2, and Vav3 mediate the invasive behavior of glioblastoma. Am J Pathol. 2008;173(6):1828-1838.
26. Yang R, Wu Y, Wang M, et al. HDAC9 promotes glioblastoma growth via TAZ-mediated EGFR pathway activation. Oncotarget. 2015;6(10):7644-7656.
27. Savary K, Caglayan D, Caja L, et al. Snail depletes the tumorigenic potential of glioblastoma. Oncogene. 2013;32(47):5409-5420.
28. Cahoy JD, Emery B, Kaushal A, et al. A transcriptome database for astrocytes, neurons, and oligodendrocytes: a new resource for understanding brain development and function. J Neurosci. 2008;28(1):264-278.
29. Lein ES, Hawrylycz MJ, Ao N, et al. Genome-wide atlas of gene expression in the adult mouse brain. Nature. 2007;445(7124): 168-176.
30. Zeisel A, Munoz-Manchado AB, Codeluppi S, et al. Brain structure. Cell types in the mouse cortex and hippocampus revealed by single-cell RNA-seq. Science. 2015;347(6226):1138-1142.
31. Zhang Y, Chen K, Sloan SA, et al. An RNA-sequencing transcriptome and splicing database of glia, neurons, and vascular cells of the cerebral cortex. J Neurosci. 2014;34(36):11929-11947.
32. Abdel-Fattah R, Xiao A, Bomgardner D, et al. Differential expression of HOX genes in neoplastic and non-neoplastic human astrocytes. J Pathol. 2006;209(1):15-24.
33. Shah N, Sukumar S. The Hox genes and their roles in oncogenesis. Nat Rev Cancer. 2010;10(5):361-371.
34. Clark MJ, Homer N, O'Connor BD, et al. U87MG decoded: the genomic sequence of a cytogenetically aberrant human cancer cell line. PLoS Genet. 2010;6(1):e1000832.
35. Chalmers AJ, Ruff EM, Martindale C, Lovegrove N, Short SC. Cytotoxic effects of temozolomide and radiation are additiveand schedule-dependent. Int J Radiat Oncol Biol Phys. 2009; 75(5):1511-1519.
36. Combs SE, Schulz-Ertner D, Roth W, Herold-Mende C, Debus J, Weber KJ. In vitro responsiveness of glioma cell lines to multimodality treatment with radiotherapy, temozolomide, and epidermal growth factor receptor inhibition with cetuximab. Int J Radiat Oncol Biol Phys. 2007;68(3):873-882.
37. Yang X, Darling JL, McMillan TJ, Peacock JH, Steel GG. Radiosensitivity, recovery and dose-rate effect in three human glioma cell lines. Radiother Oncol. 1990;19(1):49-56.
38. Agarwala SS, Kirkwood JM. Temozolomide, a novel alkylating agent with activity in the central nervous system, may improve the treatment of advanced metastatic melanoma. Oncologist. 2000;5(2):144-151.
39. Happold C, Roth P, Wick W, et al. Distinct molecular mechanisms of acquired resistance to temozolomide in glioblastoma cells. J Neurochem. 2012;122(2):444-455.
40. Chabot GG. Clinical pharmacokinetics of irinotecan. Clin Pharmacokinet. 1997;33(4):245-259.
41. Bachoo RM, Maher EA, Ligon KL, et al. Epidermal growth factor receptor and Ink4a/Arf: convergent mechanisms governing terminal differentiation and transformation along the neural stem cell to astrocyte axis. Cancer Cell. 2002;1(3):269-277.
42. Friedmann-Morvinski D, Bushong EA, Ke E, et al. Dedifferentiation of neurons and astrocytes by oncogenes can induce gliomas in mice. Science. 2012;338(6110):1080-1084.
43. Wegner M, Stolt CC. From stem cells to neurons and glia: a Soxist's view of neural development. Trends Neurosci. 2005;28(11): 583-588.
44. Iv Santaliz-Ruiz LE, Xie X, Old M, Teknos TN, Pan Q. Emerging role of nanog in tumorigenesis and cancer stem cells. Int J Cancer. 2014; 135(12):2741-2748.
45. Sarkar A, Hochedlinger K. The sox family of transcription factors: versatile regulators of stem and progenitor cell fate. Cell Stem Cell. 2013;12(1):15-30.
46. Glasgow SM, Zhu W, Stolt CC, et al. Mutual antagonism between Sox10 and NFIA regulates diversification of glial lineages and glioma subtypes. Nat Neurosci. 2014;17(10):1322-1329.
47. Cerami E, Gao J, Dogrusoz U, et al. The cBio cancer genomics portal: an open platform for exploring multidimensional cancer genomics data. Cancer Discov. 2012;2(5):401-404.
48. Chow LM, Endersby R, Zhu X, et al. Cooperativity within and among Pten, p53, and Rb pathways induces high-grade astrocytoma in adult brain. Cancer Cell. 2011;19(3):305-316.
49. MacPherson D, Dyer MA. Retinoblastoma: from the two-hit hypothesis to targeted chemotherapy. Cancer Res. 2007;67(16): 7547-7550.
50. Dannenberg JH, van Rossum A, Schuijff L, te Riele H. Ablation of the retinoblastoma gene family deregulates G(1) control causing immortalization and increased cell turnover under growthrestricting conditions. Genes Dev. 2000;14(23):3051-3064.
51. 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.
52. Galvao RP, Kasina A, McNeill RS, et al. Transformation of quiescent adult oligodendrocyte precursor cells into malignant glioma through a multistep reactivation process. Proc Natl Acad Sci USA. 2014;111(40):E4214-E4223.
53. Zheng H, Ying H, Yan H, et al. p53 and Pten control neural and glioma stem/progenitor cell renewal and differentiation. Nature. 2008;455(7216):1129-1133.
54. Sage J. The retinoblastoma tumor suppressor and stem cell biology. Genes Dev. 2012;26(13):1409-1420.
55. Bender RH, Haigis KM, Gutmann DH. Activated K-Ras, but not H-Ras or N-Ras, regulates brain neural stem cell proliferation in a Raf/Rb-dependent manner. Stem Cells. 2015;33(6): 1998-2010.
56. Meacham CE, Morrison SJ. Tumour heterogeneity and cancer cell plasticity. Nature. 2013;501(7467):328-337.
57. Liu C, Sage JC, Miller MR, et al. Mosaic analysis with double markers reveals tumor cell of origin in glioma. Cell. 2011; 146(2):209-221.
58. Irvin DM, McNeill RS, Bash RE, Miller CR. Intrinsic astrocyte heterogeneity influences tumor growth in glioma mouse models. Brain Pathol. 2016. DOI: 10.1111/bpa.12348.
59. Gaspar N, Marshall L, Perryman L, et al. MGMT-independent temozolomide resistance in pediatric glioblastoma cells associated with a PI3-kinase-mediated HOX/stem cell gene signature. Cancer Res. 2010;70(22):9243-9252.
60. Costa BM, Smith JS, Chen Y, et al. Reversing HOXA9 oncogene activation by PI3 K inhibition: epigenetic mechanism and prognostic significance in human glioblastoma. Cancer Res. 2010;70(2):453-462.
61. Halliday J, Helmy K, Pattwell SS, et al. In vivo radiation response of proneural glioma characterized by protective p53 transcriptional program and proneural-mesenchymal shift. Proc Natl Acad Sci USA. 2014;111(14):5248-5253.