EGFR signaling is differentially activated in patient-derived glioblastoma stem cells

Journal of Experimental Therapeutics and Oncology

Volumn 8, Issue 3, 2010, Pages 247-260

  Howard, Brian M ^a   Gursel, Demirkan B ^a   Bleau, Anne Marie ^b   Beyene, Robel T ^a   Holland, Eric C ^b   Boockvar, John A ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

AKT; Brain tumor stem cells; EGFR; Glioblastoma; GSK3

Indexed keywords

4 (3 CHLOROANILINO) 6,7 DIMETHOXYQUINAZOLINE; EPIDERMAL GROWTH FACTOR RECEPTOR; ERLOTINIB; GLYCOGEN SYNTHASE KINASE 3BETA; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN KINASE B;

AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CANCER STEM CELL; CELL CYCLE; CONTROLLED STUDY; DNA SEQUENCE; ENZYME ACTIVATION; ENZYME INHIBITION; GLIOBLASTOMA; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; MISSENSE MUTATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SENESCENCE; SIGNAL TRANSDUCTION; SINGLE NUCLEOTIDE POLYMORPHISM;

1-PHOSPHATIDYLINOSITOL 3-KINASE; CELL LINE, TUMOR; GLIOBLASTOMA; GLYCOGEN SYNTHASE KINASE 3; HUMANS; NEOPLASTIC STEM CELLS; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS C-AKT; PTEN PHOSPHOHYDROLASE; QUINAZOLINES; RECEPTOR, EPIDERMAL GROWTH FACTOR; SIGNAL TRANSDUCTION; TYRPHOSTINS;

EID: 77954367523     PISSN: 13594117     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (51)

1. Lapidot T, Sirard C, Vormoor J, Murdoch B, Hoang T, Caceres-Cortes J, Minden M, Paterson B, Caligiuri MA, Dick JE. A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature 367:645-648, 1994. (Pubitemid 24067706)
2. Hemmati HD, Nakano I, Lazareff JA, Masterman-Smith M, Geschwind DH, Bronner-Fraser M, Kornblum HI. Cancerous stem cells can arise from pediatric brain tumors. Proc Natl Acad Sci U S A 100:15178-15183, 2003. (Pubitemid 37518036)
3. 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 63:5821-5828, 2003. (Pubitemid 37187480)
4. 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 432:396-401, 2004. (Pubitemid 39551674)
5. Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJ, Belanger K, Brandes AA, Marosi C, Bogdahn U, Curschmann J, Janzer RC, Ludwin SK, Gorlia T, Allgeier A, Lacombe D, Cairncross JG, Eisenhauer E, Mirimanoff RO. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 352:987-996, 2005.
6. Rich JN, Bao S. Chemotherapy and cancer stem cells. Cell Stem Cell 1:353-355, 2007.
7. Wang J. Evaluating Therapeutic Efficacy against Cancer Stem Cells: New Challenges Posed by a New Paradigm. Cell Stem Cell 1:497-501, 2007. (Pubitemid 350056411)
8. Lee J, Kotliarova S, Kotliarov Y, Li A, Su Q, Donin NM, Pastorino S, Purow BW, Christopher N, Zhang W, Park JK, Fine HA. 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 9:391-403, 2006. (Pubitemid 43668737)
9. Vescovi AL, Galli R, Reynolds BA. Brain tumour stem cells. Nat Rev Cancer 6:425-436, 2006.
10. Ono M, Kuwano M. Molecular mechanisms of epidermal growth factor receptor (EGFR) activation and response to gefitinib and other EGFR-targeting drugs. Clin Cancer Res 12:7242-7251, 2006. (Pubitemid 46095395)
11. Nicholas MK, Lukas RV, Jafri NF, Faoro L, Salgia R. Epidermal growth factor receptor - mediated signal transduction in the development and therapy of gliomas. Clin Cancer Res 12: 7261-7270, 2006. (Pubitemid 46095397)
12. Ohgaki H, Kleihues P. Genetic pathways to primary and secondary glioblastoma. Am J Pathol 170:1445-1453, 2007. (Pubitemid 47339290)
13. Bleau AM, Howard BM, Taylor LA, Gursel D, Greenfield JP, Lim Tung HY, Holland EC, Boockvar JA. New strategy for the analysis of phenotypic marker antigens in brain tumor-derived neurospheres in mice and humans. Neurosurg Focus 24:E28, 2008.
14. Hamburger AW, Salmon SE. Primary Bioassay of Human Tumor Stem Cells. Science 197:461-463, 1977.
15. Tropepe V, Sibilia M, Ciruna BG, Rossant J, Wagner EF, van der Kooy D. Distinct neural stem cells proliferate in response to EGF and FGF in the developing mouse telencephalon. Dev Biol 208:166-188, 1999. (Pubitemid 29149456)
16. Howard B, Chen Y, Zecevic N. Cortical progenitor cells in the developing human telencephalon. Glia 53:57-66, 2006. (Pubitemid 43076212)
17. Kamei Y, Inagaki N, Nishizawa M, Tsutsumi O, Taketani Y, Inagaki M. Visualization of mitotic radial glial lineage cells in the developing rat brain by Cdc2 kinase-phosphorylated vimentin. Glia 23:191-199, 1998. (Pubitemid 28259717)
18. Tsujimura K, Ogawara M, Takeuchi Y, Imajoh-Ohmi S, Ha MH, Inagaki M. Visualization and function of vimentin phosphorylation by cdc2 kinase during mitosis. J Biol Chem 269:31097-31106, 1994. (Pubitemid 24377604)
19. 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 23:9392-9400, 2004. (Pubitemid 40069671)
20. Calabrese C, Poppleton H, Kocak M, Hogg TL, Fuller C, Hamner B, Oh EY, Gaber MW, Finklestein D, Allen M, Frank A, Bayazitov IT, Zakharenko SS, Gajjar A, Davidoff A, Gilbertson RJ. A perivascular niche for brain tumor stem cells. Cancer Cell 11:69-82, 2007.
21. Zhang QB, Ji XY, Huang Q, Dong J, Zhu YD, Lan Q. Differentiation profile of brain tumor stem cells: a comparative study with neural stem cells. Cell Res 16:909-915, 2006. (Pubitemid 44973578)
22. 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 283:10958-10966, 2008.
23. Beier D, Hau P, Proescholdt M, Lohmeier A, Wischhusen J, Oefner PJ, Aigner L, Brawanski A, Bogdahn U, Beier CP. CD133(+) and CD133(-) glioblastoma-derived cancer stem cells show differential growth characteristics and molecular profiles. Cancer Res 67:4010-4015, 2007. (Pubitemid 46815044)
24. Schmidt MH, Furnari FB, Cavenee WK, Bogler O. Epidermal growth factor receptor signaling intensity determines intracellular protein interactions, ubiquitination, and internalization. Proc Natl Acad Sci U S A 100:6505-6510, 2003. (Pubitemid 36666611)
25. Mellinghoff IK, Cloughesy TF, Mischel PS. PTEN-mediated resistance to epidermal growth factor receptor kinase inhibitors. Clin Cancer Res 13:378-381, 2007. (Pubitemid 46225339)
26. Mellinghoff IK, Wang MY, Vivanco I, Haas-Kogan DA, Zhu S, Dia EQ, Lu KV, Yoshimoto K, Huang JH, Chute DJ, Riggs BL, Horvath S, Liau LM, Cavenee WK, Rao PN, Beroukhim R, Peck TC, Lee JC, Sellers WR, Stokoe D, Prados M, Cloughesy TF, Sawyers CL, Mischel PS. Molecular determinants of the response of glioblastomas to EGFR kinase inhibitors. N Engl J Med 353:2012-2024, 2005.
27. Ditlevsen DK, Owczarek S, Berezin V, Bock E. Relative role of upstream regulators of Akt, ERK and CREB in NCAM- and FGF2-mediated signalling. Neurochem Int, 53:137-147, 2008.
28. Rao RD, Mladek AC, Lamont JD, Goble JM, Erlichman C, James CD, Sarkaria JN. Disruption of parallel and converging signaling pathways contributes to the synergistic antitumor effects of simultaneous mTOR and EGFR inhibition in GBM cells. Neoplasia 7:921-929, 2005.
29. Ellis AG, Doherty MM, Walker F, Weinstock J, Nerrie M, Vitali A, Murphy R, Johns TG, Scott AM, Levitzki A, McLachlan G, Webster LK, Burgess AW, Nice EC. Preclinical analysis of the analinoquinazoline AG1478, a specific small molecule inhibitor of EGF receptor tyrosine kinase. Biochem Pharmacol 71:1422-1434, 2006.
30. Shmelkov SV, Butler JM, Hooper AT, Hormigo A, Kushner J, Milde T, St Clair R, Baljevic M, White I, Jin DK, Chadburn A, Murphy AJ, Valenzuela DM, Gale NW, Thurston G, Yancopoulos GD, D'Angelica M, Kemeny N, Lyden D, Rafii S. CD133 expression is not restricted to stem cells, and both CD133+ and CD133- metastatic colon cancer cells initiate tumors. J Clin Invest 118:2111-2120, 2008.
31. Failor KL, Desyatnikov Y, Finger LA, Firestone GL. Glucocorticoid-induced degradation of glycogen synthase kinase-3 protein is triggered by serum- and glucocorticoid-induced protein kinase and Akt signaling and controls betacatenin dynamics and tight junction formation in mammary epithelial tumor cells. Mol Endocrinol 21:2403-2415, 2007. (Pubitemid 47529354)
32. Diehl JA, Cheng M, Roussel MF, Sherr CJ. Glycogen synthase kinase-3beta regulates cyclin D1 proteolysis and subcellular localization. Genes Dev 12:3499-3511, 1998. (Pubitemid 28553242)
33. Nair VD, Olanow CW. Differential modulation of Akt/glycogen synthase kinase-3beta pathway regulates apoptotic and cytoprotective signaling responses. J Biol Chem 283: 15469-15478, 2008.
34. Cui H, Meng Y, Bulleit RF. Inhibition of glycogen synthase kinase 3beta activity regulates proliferation of cultured cerebellar granule cells. Brain Res Dev Brain Res 111:177-188, 1998.
35. Linseman DA, Butts BD, Precht TA, Phelps RA, Le SS, Laessig TA, Bouchard RJ, Florez-McClure ML, Heidenreich KA. Glycogen synthase kinase-3beta phosphorylates Bax and promotes its mitochondrial localization during neuronal apoptosis. J Neurosci 24:9993-10002, 2004.
36. Beurel E, Kornprobst M, Blivet-Van Eggelpoel MJ, Ruiz-Ruiz C, Cadoret A, Capeau J, Desbois-Mouthon C. GSK-3beta inhibition by lithium confers resistance to chemotherapy-induced apoptosis through the repression of CD95 (Fas/APO-1) expression. Exp Cell Res 300:354-364, 2004. (Pubitemid 39314425)
37. Waite KA, Eng C. Protean PTEN: form and function. Am J Hum Genet 70:829-844, 2002.
38. Gilbertson RJ, Rich JN. Making a tumour's bed: glioblastoma stem cells and the vascular niche. Nat Rev Cancer 7:733-736, 2007.
39. Pollard SM, Yoshikawa K, Clarke ID, Danovi D, Stricker S, Russell R, Bayani J, Head R, Lee M, Bernstein M, Squire JA, Smith A, Dirks P. Glioma stem cell lines expanded in adherent culture have tumor-specific phenotypes and are suitable for chemical and genetic screens. Cell Stem Cell 4:568-580, 2009.
40. Salmaggi A, Boiardi A, Gelati M, Russo A, Calatozzolo C, Ciusani E, Sciacca FL, Ottolina A, Parati EA, La Porta C, Alessandri G, Marras C, Croci D, De Rossi M. Glioblastoma-derived tumorospheres identify a population of tumor stemlike cells with angiogenic potential and enhanced multidrug resistance phenotype. Glia 54:850-860, 2006.
41. Donnenberg VS, Donnenberg AD. Multiple drug resistance in cancer revisited: the cancer stem cell hypothesis. J Clin Pharmacol 45:872-877, 2005. (Pubitemid 41060226)
42. Bar EE, Chaudhry A, Lin A, Fan X, Schreck K, Matsui W, Piccirillo S, Vescovi AL, DiMeco F, Olivi A, Eberhart CG. Cyclopamine-mediated hedgehog pathway inhibition depletes stem-like cancer cells in glioblastoma. Stem Cells 25:2524-2533, 2007. (Pubitemid 47582744)
43. 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 444:756-760, 2006. (Pubitemid 44949604)
44. McKillop D, Hutchison M, Partridge EA, Bushby N, Cooper CM, Clarkson-Jones JA, Herron W, Swaisland HC. Metabolic disposition of gefitinib, an epidermal growth factor receptor tyrosine kinase inhibitor, in rat, dog and man. Xenobiotica 34:917-934, 2004. (Pubitemid 39648170)
45. Stommel JM, Kimmelman AC, Ying H, Nabioullin R, Ponugoti AH, Wiedemeyer R, Stegh AH, Bradner JE, Ligon KL, Brennan C, Chin L, DePinho RA: Coactivation of receptor tyrosine kinases affects the response of tumor cells to targeted therapies. Science 318:287-290, 2007. (Pubitemid 47574858)
46. Engelman JA, Luo J, Cantley LC. The evolution of phosphatidylinositol 3-kinases as regulators of growth and metabolism. Nat Rev Genet 7:606-619, 2006. (Pubitemid 44100518)
47. Zhao JJ, Roberts TM: PI3 kinases in cancer: from oncogene artifact to leading cancer target. Sci STKE 2006:pe52, 2006.
48. Fan QW, Cheng CK, Nicolaides TP, Hackett CS, Knight ZA, Shokat KM, Weiss WA. A dual phosphoinositide-3-kinase alpha/mTOR inhibitor cooperates with blockade of epidermal growth factor receptor in PTEN-mutant glioma. Cancer Res 67:7960-7965, 2007.
49. Brewer GJ, Torricelli JR, Evege EK, Price PJ. Optimized survival of hippocampal neurons in B27-supplemented Neurobasal, a new serum-free medium combination. J Neurosci Res 35:567-576, 1993.
50. Urbanska K, Trojanek J, Del Valle L, Eldeen MB, Hofmann F, Garcia-Echeverria C, Khalili K, Reiss K. Inhibition of IGF-I receptor in anchorage-independence attenuates GSK-3beta constitutive phosphorylation and compromises growth and survival of medulloblastoma cell lines. Oncogene 26: 2308-2317, 2007. (Pubitemid 46572811)
51. Blackburn RV, Galoforo SS, Berns CM, Motwani NM, Corry PM, Lee YJ. Differential induction of cell death in human glioma cell lines by sodium nitroprusside. Cancer 82: 1137-1145, 1998. (Pubitemid 28136529)