Differentiation of glioblastoma multiforme stem-like cells leads to downregulation of EGFR and EGFRvIII and decreased tumorigenic and stem-like cell potential

References

• Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJ, Belanger K, Brandes AA, Marosi C, Bogdahn U, et al, European Organisation for Research and Treatment of Cancer Brain Tumor and Radiotherapy Groups, National Cancer Institute of Canada Clinical Trials Group. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 2005; 352:987 - 96; http://dx.doi.org/10.1056/NEJMoa043330; PMID: 15758009
   PubMed Web of Science ®Google Scholar
• Ekstrand AJ, Longo N, Hamid ML, Olson JJ, Liu L, Collins VP, James CD. Functional characterization of an EGF receptor with a truncated extracellular domain expressed in glioblastomas with EGFR gene amplification. Oncogene 1994; 9:2313 - 20; PMID: 8036013
   PubMed Web of Science ®Google Scholar
• Huang HS, Nagane M, Klingbeil CK, Lin H, Nishikawa R, Ji XD, Huang CM, Gill GN, Wiley HS, Cavenee WK. The enhanced tumorigenic activity of a mutant epidermal growth factor receptor common in human cancers is mediated by threshold levels of constitutive tyrosine phosphorylation and unattenuated signaling. J Biol Chem 1997; 272:2927 - 35; http://dx.doi.org/10.1074/jbc.272.5.2927; PMID: 9006938
   PubMed Web of Science ®Google Scholar
• Nishikawa R, Ji XD, Harmon RC, Lazar CS, Gill GN, Cavenee WK, Huang HJ. A mutant epidermal growth factor receptor common in human glioma confers enhanced tumorigenicity. Proc Natl Acad Sci U S A 1994; 91:7727 - 31; http://dx.doi.org/10.1073/pnas.91.16.7727; PMID: 8052651
   PubMed Web of Science ®Google Scholar
• Shinojima N, Tada K, Shiraishi S, Kamiryo T, Kochi M, Nakamura H, Makino K, Saya H, Hirano H, Kuratsu J, et al. Prognostic value of epidermal growth factor receptor in patients with glioblastoma multiforme. Cancer Res 2003; 63:6962 - 70; PMID: 14583498
   PubMed Web of Science ®Google Scholar
• Torp SH, Helseth E, Dalen A, Unsgaard G. Relationships between Ki-67 labelling index, amplification of the epidermal growth factor receptor gene, and prognosis in human glioblastomas. Acta Neurochir (Wien) 1992; 117:182 - 6; http://dx.doi.org/10.1007/BF01400618; PMID: 1414519
   PubMed Web of Science ®Google Scholar
• Lassman AB, Rossi MR, Raizer JJ, Abrey LE, Lieberman FS, Grefe CN, Lamborn K, Pao W, Shih AH, Kuhn JG, et al. Molecular study of malignant gliomas treated with epidermal growth factor receptor inhibitors: tissue analysis from North American Brain Tumor Consortium Trials 01-03 and 00-01. Clin Cancer Res 2005; 11:7841 - 50; http://dx.doi.org/10.1158/1078-0432.CCR-05-0421; PMID: 16278407
   PubMed Web of Science ®Google Scholar
• Mellinghoff IK, Wang MY, Vivanco I, Haas-Kogan DA, Zhu S, Dia EQ, Lu KV, Yoshimoto K, Huang JH, Chute DJ, et al. Molecular determinants of the response of glioblastomas to EGFR kinase inhibitors. N Engl J Med 2005; 353:2012 - 24; http://dx.doi.org/10.1056/NEJMoa051918; PMID: 16282176
   PubMed Web of Science ®Google Scholar
• Rich JN, Reardon DA, Peery T, Dowell JM, Quinn JA, Penne KL, Wikstrand CJ, Van Duyn LB, Dancey JE, McLendon RE, et al. Phase II trial of gefitinib in recurrent glioblastoma. J Clin Oncol 2004; 22:133 - 42; http://dx.doi.org/10.1200/JCO.2004.08.110; PMID: 14638850
   PubMed Web of Science ®Google Scholar
• Bigner SH, Humphrey PA, Wong AJ, Vogelstein B, Mark J, Friedman HS, Bigner DD. Characterization of the epidermal growth factor receptor in human glioma cell lines and xenografts. Cancer Res 1990; 50:8017 - 22; PMID: 2253244
   PubMed Web of Science ®Google Scholar
• Pandita A, Aldape KD, Zadeh G, Guha A, James CD. Contrasting in vivo and in vitro fates of glioblastoma cell subpopulations with amplified EGFR. Genes Chromosomes Cancer 2004; 39:29 - 36; http://dx.doi.org/10.1002/gcc.10300; PMID: 14603439
   PubMed Web of Science ®Google Scholar
• Stockhausen MT, Broholm H, Villingshøj M, Kirchhoff M, Gerdes T, Kristoffersen K, Kosteljanetz M, Spang-Thomsen M, Poulsen HS. Maintenance of EGFR and EGFRvIII expressions in an in vivo and in vitro model of human glioblastoma multiforme. Exp Cell Res 2011; 317:1513 - 26; http://dx.doi.org/10.1016/j.yexcr.2011.04.001; PMID: 21514294
   PubMed Web of Science ®Google Scholar
• Lee J, Kotliarova S, Kotliarov Y, Li A, Su Q, Donin NM, Pastorino S, Purow BW, Christopher N, Zhang W, 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; http://dx.doi.org/10.1016/j.ccr.2006.03.030; PMID: 16697959
   PubMed Web of Science ®Google Scholar
• Galli R, Binda E, Orfanelli U, Cipelletti B, Gritti A, De Vitis S, Fiocco R, Foroni C, Dimeco F, Vescovi A. Isolation and characterization of tumorigenic, stem-like neural precursors from human glioblastoma. Cancer Res 2004; 64:7011 - 21; http://dx.doi.org/10.1158/0008-5472.CAN-04-1364; PMID: 15466194
   PubMed Web of Science ®Google Scholar
• Ignatova TN, Kukekov VG, Laywell ED, Suslov ON, Vrionis FD, Steindler DA. Human cortical glial tumors contain neural stem-like cells expressing astroglial and neuronal markers in vitro. Glia 2002; 39:193 - 206; http://dx.doi.org/10.1002/glia.10094; PMID: 12203386
   PubMed Web of Science ®Google Scholar
• Singh SK, Clarke ID, Terasaki M, Bonn VE, Hawkins C, Squire J, Dirks PB. Identification of a cancer stem cell in human brain tumors. Cancer Res 2003; 63:5821 - 8; PMID: 14522905
   PubMed Web of Science ®Google Scholar
• Singh SK, Hawkins C, Clarke ID, Squire JA, Bayani J, Hide T, Henkelman RM, Cusimano MD, Dirks PB. Identification of human brain tumour initiating cells. Nature 2004; 432:396 - 401; http://dx.doi.org/10.1038/nature03128; PMID: 15549107
   PubMed Web of Science ®Google Scholar
• Yuan X, Curtin J, Xiong Y, Liu G, Waschsmann-Hogiu S, Farkas DL, Black KL, Yu JS. Isolation of cancer stem cells from adult glioblastoma multiforme. Oncogene 2004; 23:9392 - 400; http://dx.doi.org/10.1038/sj.onc.1208311; PMID: 15558011
   PubMed Web of Science ®Google Scholar
• Bao S, Wu Q, McLendon RE, Hao Y, Shi Q, Hjelmeland AB, Dewhirst MW, Bigner DD, Rich JN. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 2006; 444:756 - 60; http://dx.doi.org/10.1038/nature05236; PMID: 17051156
   PubMed Web of Science ®Google Scholar
• Bao S, Wu Q, Sathornsumetee S, Hao Y, Li Z, Hjelmeland AB, Shi Q, McLendon RE, Bigner DD, Rich JN. Stem cell-like glioma cells promote tumor angiogenesis through vascular endothelial growth factor. Cancer Res 2006; 66:7843 - 8; http://dx.doi.org/10.1158/0008-5472.CAN-06-1010; PMID: 16912155
   PubMed Web of Science ®Google Scholar
• Lathia JD, Gallagher J, Myers JT, Li M, Vasanji A, McLendon RE, Hjelmeland AB, Huang AY, Rich JN. Direct in vivo evidence for tumor propagation by glioblastoma cancer stem cells. PLoS One 2011; 6:e24807; http://dx.doi.org/10.1371/journal.pone.0024807; PMID: 21961046
   PubMedGoogle Scholar
• Liu G, Yuan X, Zeng Z, Tunici P, Ng H, Abdulkadir IR, Lu L, Irvin D, Black KL, Yu JS. Analysis of gene expression and chemoresistance of CD133+ cancer stem cells in glioblastoma. Mol Cancer 2006; 5:67; http://dx.doi.org/10.1186/1476-4598-5-67; PMID: 17140455
   PubMed Web of Science ®Google Scholar
• Massard C, Deutsch E, Soria JC. Tumour stem cell-targeted treatment: elimination or differentiation. Ann Oncol 2006; 17:1620 - 4; http://dx.doi.org/10.1093/annonc/mdl074; PMID: 16600978
   PubMed Web of Science ®Google Scholar
• Sell S. Stem cell origin of cancer and differentiation therapy. Crit Rev Oncol Hematol 2004; 51:1 - 28; http://dx.doi.org/10.1016/j.critrevonc.2004.04.007; PMID: 15207251
   PubMed Web of Science ®Google Scholar
• Kristoffersen K, Villingshøj M, Poulsen HS, Stockhausen MT. Level of Notch activation determines the effect on growth and stem cell-like features in glioblastoma multiforme neurosphere cultures. Cancer Biol Ther 2013; 14:625 - 37; http://dx.doi.org/10.4161/cbt.24595; PMID: 23792644
   PubMed Web of Science ®Google Scholar
• Campos B, Wan F, Farhadi M, Ernst A, Zeppernick F, Tagscherer KE, Ahmadi R, Lohr J, Dictus C, Gdynia G, et al. Differentiation therapy exerts antitumor effects on stem-like glioma cells. Clin Cancer Res 2010; 16:2715 - 28; http://dx.doi.org/10.1158/1078-0432.CCR-09-1800; PMID: 20442299
   PubMed Web of Science ®Google Scholar
• Ying M, Wang S, Sang Y, Sun P, Lal B, Goodwin CR, Guerrero-Cazares H, Quinones-Hinojosa A, Laterra J, Xia S. Regulation of glioblastoma stem cells by retinoic acid: role for Notch pathway inhibition. Oncogene 2011; 30:3454 - 67; http://dx.doi.org/10.1038/onc.2011.58; PMID: 21383690
   PubMed Web of Science ®Google Scholar
• Engstrom CM, Demers D, Dooner M, McAuliffe C, Benoit BO, Stencel K, Joly M, Hulspas R, Reilly JL, Savarese T, et al. A method for clonal analysis of epidermal growth factor-responsive neural progenitors. J Neurosci Methods 2002; 117:111 - 21; http://dx.doi.org/10.1016/S0165-0270(02)00074-2; PMID: 12100976
   PubMed Web of Science ®Google Scholar
• Mori H, Ninomiya K, Kino-oka M, Shofuda T, Islam MO, Yamasaki M, Okano H, Taya M, Kanemura Y. Effect of neurosphere size on the growth rate of human neural stem/progenitor cells. J Neurosci Res 2006; 84:1682 - 91; http://dx.doi.org/10.1002/jnr.21082; PMID: 17044035
   PubMed Web of Science ®Google Scholar
• Joo KM, Kim SY, Jin X, Song SY, Kong DS, Lee JI, Jeon JW, Kim MH, Kang BG, Jung Y, et al. Clinical and biological implications of CD133-positive and CD133-negative cells in glioblastomas. Lab Invest 2008; 88:808 - 15; http://dx.doi.org/10.1038/labinvest.2008.57; PMID: 18560366
   PubMed Web of Science ®Google Scholar
• Piccirillo SG, Combi R, Cajola L, Patrizi A, Redaelli S, Bentivegna A, Baronchelli S, Maira G, Pollo B, Mangiola A, et al. Distinct pools of cancer stem-like cells coexist within human glioblastomas and display different tumorigenicity and independent genomic evolution. Oncogene 2009; 28:1807 - 11; http://dx.doi.org/10.1038/onc.2009.27; PMID: 19287454
   PubMed Web of Science ®Google Scholar
• Kukekov VG, Laywell ED, Suslov O, Davies K, Scheffler B, Thomas LB, O’Brien TF, Kusakabe M, Steindler DA. Multipotent stem/progenitor cells with similar properties arise from two neurogenic regions of adult human brain. Exp Neurol 1999; 156:333 - 44; http://dx.doi.org/10.1006/exnr.1999.7028; PMID: 10328940
   PubMed Web of Science ®Google Scholar
• Lee A, Kessler JD, Read TA, Kaiser C, Corbeil D, Huttner WB, Johnson JE, Wechsler-Reya RJ. Isolation of neural stem cells from the postnatal cerebellum. Nat Neurosci 2005; 8:723 - 9; http://dx.doi.org/10.1038/nn1473; PMID: 15908947
   PubMed Web of Science ®Google Scholar
• Lim DA, Cha S, Mayo MC, Chen MH, Keles E, VandenBerg S, Berger MS. Relationship of glioblastoma multiforme to neural stem cell regions predicts invasive and multifocal tumor phenotype. Neuro Oncol 2007; 9:424 - 9; http://dx.doi.org/10.1215/15228517-2007-023; PMID: 17622647
   PubMed Web of Science ®Google Scholar
• Weickert CS, Webster MJ, Colvin SM, Herman MM, Hyde TM, Weinberger DR, Kleinman JE. Localization of epidermal growth factor receptors and putative neuroblasts in human subependymal zone. J Comp Neurol 2000; 423:359 - 72; http://dx.doi.org/10.1002/1096-9861(20000731)423:3<359::AID-CNE1>3.0.CO;2-0; PMID: 10870078
   PubMed Web of Science ®Google Scholar
• Aguirre A, Rubio ME, Gallo V. Notch and EGFR pathway interaction regulates neural stem cell number and self-renewal. Nature 2010; 467:323 - 7; http://dx.doi.org/10.1038/nature09347; PMID: 20844536
   PubMed Web of Science ®Google Scholar
• Ayuso-Sacido A, Moliterno JA, Kratovac S, Kapoor GS, O’Rourke DM, Holland EC, García-Verdugo JM, Roy NS, Boockvar JA. Activated EGFR signaling increases proliferation, survival, and migration and blocks neuronal differentiation in post-natal neural stem cells. J Neurooncol 2010; 97:323 - 37; http://dx.doi.org/10.1007/s11060-009-0035-x; PMID: 19855928
   PubMed Web of Science ®Google Scholar
• Boockvar JA, Kapitonov D, Kapoor G, Schouten J, Counelis GJ, Bogler O, Snyder EY, McIntosh TK, O’Rourke DM. Constitutive EGFR signaling confers a motile phenotype to neural stem cells. Mol Cell Neurosci 2003; 24:1116 - 30; http://dx.doi.org/10.1016/j.mcn.2003.09.011; PMID: 14697673
   PubMed Web of Science ®Google Scholar
• Mazzoleni S, Politi LS, Pala M, Cominelli M, Franzin A, Sergi Sergi L, Falini A, De Palma M, Bulfone A, Poliani PL, et al. Epidermal growth factor receptor expression identifies functionally and molecularly distinct tumor-initiating cells in human glioblastoma multiforme and is required for gliomagenesis. Cancer Res 2010; 70:7500 - 13; http://dx.doi.org/10.1158/0008-5472.CAN-10-2353; PMID: 20858720
   PubMed Web of Science ®Google Scholar
• Howard BM, Gursel DB, Bleau AM, Beyene RT, Holland EC, Boockvar JA. EGFR signaling is differentially activated in patient-derived glioblastoma stem cells. J Exp Ther Oncol 2010; 8:247 - 60; PMID: 20734923
   PubMedGoogle Scholar
• Del Vecchio CA, Jensen KC, Nitta RT, Shain AH, Giacomini CP, Wong AJ. Epidermal growth factor receptor variant III contributes to cancer stem cell phenotypes in invasive breast carcinoma. Cancer Res 2012; 72:2657 - 71; http://dx.doi.org/10.1158/0008-5472.CAN-11-2656; PMID: 22419663
   PubMed Web of Science ®Google Scholar
• Wong A, Mitra S, Del Vecchio CA, Shirboll S. Expression of EGFRvIII in brain tumor stem cells. J Clin Oncol 2012; 26:15s
   Google Scholar
• Liu XJ, Wu WT, Wu WH, Yin F, Ma SH, Qin JZ, Liu XX, Liu YN, Zhang XY, Li P, et al. A minority subpopulation of CD133(+) /EGFRvIII(+) /EGFR(-) cells acquires stemness and contributes to gefitinib resistance. CNS Neurosci Ther 2013; 19:494 - 502; http://dx.doi.org/10.1111/cns.12092; PMID: 23575351
   PubMed Web of Science ®Google Scholar
• Dirks PB. Brain tumor stem cells: bringing order to the chaos of brain cancer. J Clin Oncol 2008; 26:2916 - 24; http://dx.doi.org/10.1200/JCO.2008.17.6792; PMID: 18539973
   PubMed Web of Science ®Google Scholar
• Soeda A, Inagaki A, Oka N, Ikegame Y, Aoki H, Yoshimura S, Nakashima S, Kunisada T, Iwama T. Epidermal growth factor plays a crucial role in mitogenic regulation of human brain tumor stem cells. J Biol Chem 2008; 283:10958 - 66; http://dx.doi.org/10.1074/jbc.M704205200; PMID: 18292095
   PubMed Web of Science ®Google Scholar
• Phillips HS, Kharbanda S, Chen R, Forrest WF, Soriano RH, Wu TD, Misra A, Nigro JM, Colman H, Soroceanu L, et al. Molecular subclasses of high-grade glioma predict prognosis, delineate a pattern of disease progression, and resemble stages in neurogenesis. Cancer Cell 2006; 9:157 - 73; http://dx.doi.org/10.1016/j.ccr.2006.02.019; PMID: 16530701
   PubMed Web of Science ®Google Scholar
• Verhaak RG, Hoadley KA, Purdom E, Wang V, Qi Y, Wilkerson MD, Miller CR, Ding L, Golub T, Mesirov JP, et al, Cancer Genome Atlas Research Network. Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell 2010; 17:98 - 110; http://dx.doi.org/10.1016/j.ccr.2009.12.020; PMID: 20129251
   PubMed Web of Science ®Google Scholar