Dedifferentiation of patient-derived glioblastoma multiforme cell lines results in a cancer stem cell-like state with mitogen-independent growth

Journal of Cellular and Molecular Medicine

Volumn 19, Issue 6, 2015, Pages 1262-1272

  Olmez, Inan ^a   Shen, Wangzhen ^a   Mcdonald, Hayes ^b   Ozpolat, Bulent ^c  

^a VANDERBILT UNIVERSITY   (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

Cancer stem cells; EphB4; Epidermal growth factor receptor; Glioblastoma multiforme; Nanog; Oct4; Salinomycin; Sox2

Indexed keywords

BETA CATENIN; DACARBAZINE; EGFR PROTEIN, HUMAN; EPIDERMAL GROWTH FACTOR RECEPTOR; MITOGENIC AGENT; NOTCH1 RECEPTOR; TEMOZOLOMIDE;

ANALOGS AND DERIVATIVES; CANCER STEM CELL; CELL DEDIFFERENTIATION; CELL PROLIFERATION; CELL REPROGRAMMING TECHNIQUE; CELL SURVIVAL; DRUG EFFECTS; DRUG RESISTANCE; GENE EXPRESSION REGULATION; GENETICS; GLIOBLASTOMA; HUMAN; INDUCED PLURIPOTENT STEM CELL; METABOLISM; MULTICELLULAR SPHEROID; NEURAL STEM CELL; NUCLEAR REPROGRAMMING; PATHOLOGY; PROCEDURES; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TUMOR CELL LINE; WESTERN BLOTTING;

BETA CATENIN; BLOTTING, WESTERN; CELL DEDIFFERENTIATION; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; CELLULAR REPROGRAMMING; CELLULAR REPROGRAMMING TECHNIQUES; DACARBAZINE; DRUG RESISTANCE, NEOPLASM; GENE EXPRESSION REGULATION, NEOPLASTIC; GLIOBLASTOMA; HUMANS; INDUCED PLURIPOTENT STEM CELLS; MITOGENS; NEOPLASTIC STEM CELLS; NEURAL STEM CELLS; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTOR, NOTCH1; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SPHEROIDS, CELLULAR;

EID: 84929945695     PISSN: 15821838     EISSN: None     Source Type: Journal    
DOI: 10.1111/jcmm.12479     Document Type: Article

References (47)

1. Piccirillo SG, Binda E, Fiocco R, et al. Brain cancer stem cells. J Mol Med. 2009; 87: 1087-95.
2. Kelly JJ, Stechishin O, Chojnacki A, et al. Proliferation of human glioblastoma stem cells occurs independently of exogenous mitogens. Stem Cells. 2009; 27: 1722-33.
3. Singh SK, Clarke ID, Terasaki M, et al. Identification of a cancer stem cell in human brain tumors. Cancer Res. 2003; 63: 5821-8.
4. Lathia JD, Hitomi M, Gallagher J, et al. Distribution of CD133 reveals glioma stem cells self-renew through symmetric and asymmetric cell divisions. Cell Death Dis. 2011; 2: e200.
5. He J, Liu Y, Xie X, et al. Identification of cell surface glycoprotein markers for glioblastoma-derived stem-like cells using a lectin microarray and LC-MS/MS approach. J Proteome Res. 2010; 9: 2565-72.
6. 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: 440-52.
7. Kang MJ, Kim HP, Lee KS, et al. Proteomic analysis reveals that CD147/EMMPRIN confers chemoresistance in cancer stem cell-like cells. Proteomics. 2013; 13: 1714-25.
8. Galli R, Binda E, Orfanelli U, et al. Isolation and characterization of tumorigenic, stem-like neural precursors from human glioblastoma. Cancer Res. 2004; 64: 7011-21.
9. Reya T, Clevers H. Wnt signalling in stem cells and cancer. Nature. 2005; 434: 843-50.
10. Purow BW, Haque RM, Noel MW, 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: 2353-63.
11. 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: 3066-75.
12. Wang J, Wakeman TP, Lathia JD, et al. Notch promotes radioresistance of glioma stem cells. Stem Cells. 2010; 28: 17-28.
13. Kim Y, Kim KH, Lee J, et al. Wnt activation is implicated in glioblastoma radioresistance. Lab Invest. 2012; 92: 466-73.
14. Takahashi K, Tanabe K, Ohnuki M, et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell. 2007; 131: 861-72.
15. Ben-Porath I, Thomson MW, Carey VJ, et al. An embryonic stem cell-like gene expression signature in poorly differentiated aggressive human tumors. Nat Genet. 2008; 40: 499-507.
16. Schoenhals M, Kassambara A, De Vos J, et al. Embryonic stem cell markers expression in cancers. Biochem Biophys Res Commun. 2009; 383: 157-62.
17. Slanina H, Mundlein S, Hebling S, et al. Role of epidermal growth factor receptor signaling in the interaction of Neisseria meningitidis with endothelial cells. Infect Immun. 2014; 82: 1243-55.
18. Neely MD, Litt MJ, Tidball AM, et al. DMH1, a highly selective small molecule BMP inhibitor promotes neurogenesis of hiPSCs: comparison of PAX6 and SOX1 expression during neural induction. ACS Chem Neurosci. 2012; 3: 482-91.
19. Sangodkar J, Dhawan NS, Melville H, et al. Targeting the FOXO1/KLF6 axis regulates EGFR signaling and treatment response. J Clin Invest. 2012; 122: 2637-51.
20. van Meerloo J, Kaspers GJ, Cloos J. Cell sensitivity assays: the MTT assay. Methods Mol Biol. 2011; 731: 237-45.
21. Laks DR, Masterman-Smith M, Visnyei K, et al. Neurosphere formation is an independent predictor of clinical outcome in malignant glioma. Stem Cells. 2009; 27: 980-7.
22. Furnari FB, Fenton T, Bachoo RM, et al. Malignant astrocytic glioma: genetics, biology, and paths to treatment. Genes Dev. 2007; 21: 2683-710.
23. Nagane M, Coufal F, Lin H, et al. A common mutant epidermal growth factor receptor confers enhanced tumorigenicity on human glioblastoma cells by increasing proliferation and reducing apoptosis. Cancer Res. 1996; 56: 5079-86.
24. Lal A, Glazer CA, Martinson HM, et al. Mutant epidermal growth factor receptor up-regulates molecular effectors of tumor invasion. Cancer Res. 2002; 62: 3335-9.
25. Gupta PB, Onder TT, Jiang G, et al. Identification of selective inhibitors of cancer stem cells by high-throughput screening. Cell. 2009; 138: 645-59.
26. Guha A, Feldkamp MM, Lau N, et al. Proliferation of human malignant astrocytomas is dependent on Ras activation. Oncogene. 1997; 15: 2755-65.
27. Holland EC, Celestino J, Dai C, et al. Combined activation of Ras and Akt in neural progenitors induces glioblastoma formation in mice. Nat Genet. 2000; 25: 55-7.
28. Jun HJ, Bronson RT, Charest A. Inhibition of EGFR induces a c-MET-driven stem cell population in glioblastoma. Stem Cells. 2013; 32: 338-48.
29. Zbinden M, Duquet A, Lorente-Trigos A, et al. NANOG regulates glioma stem cells and is essential in vivo acting in a cross-functional network with GLI1 and p53. EMBO J. 2010; 29: 2659-74.
30. Chen S, Xu Y, Chen Y, et al. SOX2 gene regulates the transcriptional network of oncogenes and affects tumorigenesis of human lung cancer cells. PLoS ONE. 2012; 7: e36326.
31. Oates AC, Lackmann M, Power MA, et al. An early developmental role for eph-ephrin interaction during vertebrate gastrulation. Mech Dev. 1999; 83: 77-94.
32. O'Leary DD, Wilkinson DG. Eph receptors and ephrins in neural development. Curr Opin Neurobiol. 1999; 9: 65-73.
33. Chen T, Liu X, Yi S, et al. EphB4 is overexpressed in gliomas and promotes the growth of glioma cells. Tumour Biol. 2013; 34: 379-85.
34. Noren NK, Lu M, Freeman AL, et al. Interplay between EphB4 on tumor cells and vascular ephrin-B2 regulates tumor growth. Proc Natl Acad Sci USA. 2004; 101: 5583-8.
35. Kumar SR, Singh J, Xia G, et al. Receptor tyrosine kinase EphB4 is a survival factor in breast cancer. Am J Pathol. 2006; 169: 279-93.
36. Xia G, Kumar SR, Stein JP, et al. EphB4 receptor tyrosine kinase is expressed in bladder cancer and provides signals for cell survival. Oncogene. 2006; 25: 769-80.
37. Limbourg A, Ploom M, Elligsen D, et al. Notch ligand Delta-like 1 is essential for postnatal arteriogenesis. Circ Res. 2007; 100: 363-71.
38. Hitoshi S, Alexson T, Tropepe V, et al. Notch pathway molecules are essential for the maintenance, but not the generation, of mammalian neural stem cells. Genes Dev. 2002; 16: 846-58.
39. Hitoshi S, Seaberg RM, Koscik C, et al. Primitive neural stem cells from the mammalian epiblast differentiate to definitive neural stem cells under the control of Notch signaling. Genes Dev. 2004; 18: 1806-11.
40. Fan X, Khaki L, Zhu TS, et al. NOTCH pathway blockade depletes CD133-positive glioblastoma cells and inhibits growth of tumor neurospheres and xenografts. Stem Cells. 2010; 28: 5-16.
41. 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: 101-8.
42. - glioblastoma-derived cancer stem cells show differential growth characteristics and molecular profiles. Cancer Res. 2007; 67: 4010-5.
43. Rossi M, Magnoni L, Miracco C, et al. β-Catenin and Gli1 are prognostic markers in glioblastoma. Cancer Biol Ther. 2011; 11: 753-61.
44. Zhang N, Wei P, Gong A, et al. FoxM1 promotes β-catenin nuclear localization and controls Wnt target-gene expression and glioma tumorigenesis. Cancer Cell. 2011; 20: 427-42.
45. Yan D, Wiesmann M, Rohan M, et al. Elevated expression of axin2 and hnkd mRNA provides evidence that Wnt/β-catenin signaling is activated in human colon tumors. Proc Natl Acad Sci USA. 2001; 98: 14973-8.
46. Wu ZQ, Brabletz T, Fearon E, et al. Canonical Wnt suppressor, Axin2, promotes colon carcinoma oncogenic activity. Proc Natl Acad Sci USA. 2012; 109: 11312-7.
47. Major MB, Roberts BS, Berndt JD, et al. New regulators of Wnt/β-catenin signaling revealed by integrative molecular screening. Sci Signal. 2008; 1: ra12.