Combined EGFR- and notch inhibition display additive inhibitory effect on glioblastoma cell viability and glioblastoma-induced endothelial cell sprouting in vitro

Cancer Cell International

Volumn 16, Issue 1, 2016, Pages

  Staberg, Mikkel ^a   Michaelsen, Signe Regner ^a   Olsen, Louise Stobbe ^a   Nedergaard, Mette Kjølhede ^b   Villingshøj, Mette ^a   Stockhausen, Marie Thérése ^a   Hamerlik, Petra ^a,c   Poulsen, Hans Skovgaard ^a  

^a FINSEN LABORATORY   (Denmark)

^b Mental Health Center Glostrup   (Denmark)

^c DANISH CANCER SOCIETY RESEARCH CENTER   (Denmark)

Author keywords

Angiogenesis; DAPT; EGFR; Endothelial spheroid sprouting; Gamma secretase inhibitor; Glioblastoma; Iressa; Notch; Tyrosine kinase inhibitor

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; GAMMA SECRETASE INHIBITOR; GEFITINIB; NOTCH RECEPTOR; TRANSCRIPTION FACTOR HES 1; VASCULOTROPIN;

ANTIANGIOGENIC ACTIVITY; ARTICLE; CELL VIABILITY; CONTROLLED STUDY; ENDOTHELIUM CELL; GLIOBLASTOMA CELL LINE; HUMAN; HUMAN CELL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

EID: 84964407601     PISSN: None     EISSN: 14752867     Source Type: Journal    
DOI: 10.1186/s12935-016-0309-2     Document Type: Article

References (46)

1. Plate KH, Risau W. Angiogenesis in malignant gliomas. Glia. 1995;15(3):339-47.
2. Ghiaseddin A, Peters KB. Use of bevacizumab in recurrent glioblastoma. CNS Oncol. 2015;4(3):157-69.
3. Thomas AA, Omuro A. Current role of anti-angiogenic strategies for glioblastoma. Curr Treat Options Oncol. 2014;15(4):551-66.
4. Ekstrand AJ, James CD, Cavenee WK, Seliger B, Pettersson RF, Collins VP. Genes for epidermal growth-factor receptor, transforming growth factor-alpha, and epidermal growth-factor and their expression in human gliomas in vivo. Cancer Res. 1991;51(8):2164-72.
5. Wikstrand CJ, Reist CJ, Archer GE, Zalutsky MR, Bigner DD. The class III variant of the epidermal growth factor receptor (EGFRvIII): characterization and utilization as an immunotherapeutic target. J Neurovirol. 1998;4(2):148-58.
6. Sugawa N, Ekstrand AJ, James CD, Collins VP. Identical splicing of aberrant epidermal growth factor receptor transcripts from amplified rearranged genes in human glioblastomas. Proc Natl Acad Sci USA. 1990;87(21):8602-6.
7. Ekstrand AJ, Sugawa N, James CD, Collins VP. Amplified and rearranged epidermal growth factor receptor genes in human glioblastomas reveal deletions of sequences encoding portions of the N- and/or C-terminal tails. Proc Natl Acad Sci USA. 1992;89(10):4309-13.
8. Normanno N, De LA, Bianco C, Strizzi L, Mancino M, Maiello MR, Carotenuto A, De FG, Caponigro F, Salomon DS. Epidermal growth factor receptor (EGFR) signaling in cancer. Gene. 2006;366(1):2-16.
9. Bos JL. Ras oncogenes in human cancer: a review. Cancer Res. 1989;49(17):4682-9.
10. De LA, Carotenuto A, Rachiglio A, Gallo M, Maiello MR, Aldinucci D, Pinto A, Normanno N. The role of the EGFR signaling in tumor microenvironment. J Cell Physiol. 2008;214(3):559-67.
11. Petit AM, Rak J, Hung MC, Rockwell P, Goldstein N, Fendly B, Kerbel RS. Neutralizing antibodies against epidermal growth factor and ErbB-2/neu receptor tyrosine kinases down-regulate vascular endothelial growth factor production by tumor cells in vitro and in vivo: angiogenic implications for signal transduction therapy of solid tumors. Am J Pathol. 1997;151(6):1523-30.
12. Hirata A, Uehara H, Izumi K, Naito S, Kuwano M, Ono M. Direct inhibition of EGF receptor activation in vascular endothelial cells by gefitinib ('Iressa', ZD1839). Cancer Sci. 2004;95(7):614-8.
13. Teodorczyk M, Schmidt MH. Notching on cancer's door: notch signaling in brain tumors. Front Oncol. 2014;4:341.
14. Li JL, Harris AL. Crosstalk of VEGF and notch pathways in tumour angiogenesis: therapeutic implications. Front Biosci (Landmark Ed). 2009;14:3094-110.
15. Rehman AO, Wang CY. Notch signaling in the regulation of tumor angiogenesis. Trends Cell Biol. 2006;16(6):293-300.
16. Sahlgren C, Gustafsson MV, Jin S, Poellinger L, Lendahl U. Notch signaling mediates hypoxia-induced tumor cell migration and invasion. Proc Natl Acad Sci USA. 2008;105(17):6392-7.
17. Aguirre A, Rubio ME, Gallo V. Notch and EGFR pathway interaction regulates neural stem cell number and self-renewal. Nature. 2010;467(7313):323-7.
18. Fassl A, Tagscherer KE, Richter J, Berriel DM, Alcantara Llaguno SR, Campos B, Kopitz J, Herold-Mende C, Herzig S, Schmidt MH, et al. Notch1 signaling promotes survival of glioblastoma cells via EGFR-mediated induction of anti-apoptotic Mcl-1. Oncogene. 2012;31(44):4698-708.
19. Brennan C, Momota H, Hambardzumyan D, Ozawa T, Tandon A, Pedraza A, Holland E. Glioblastoma subclasses can be defined by activity among signal transduction pathways and associated genomic alterations. PLoS One. 2009;4(11):e7752.
20. Purow BW, Sundaresan TK, Burdick MJ, Kefas BA, Comeau LD, Hawkinson MP, Su Q, Kotliarov Y, Lee J, Zhang W, et al. Notch-1 regulates transcription of the epidermal growth factor receptor through p53. Carcinogenesis. 2008;29(5):918-25.
21. Fitzgerald K, Harrington A, Leder P. Ras pathway signals are required for notch-mediated oncogenesis. Oncogene. 2000;19(37):4191-8.
22. Stockhausen MT, Broholm H, Villingshoj 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(11):1513-26.
23. Stockhausen MT, Kristoffersen K, Stobbe L, Poulsen HS. Differentiation of glioblastoma multiforme stem-like cells leads to downregulation of EGFR and EGFRvIII and decreased tumorigenic and stem-like cell potential. Cancer Biol Ther. 2014;15(2):216-24.
24. Korff T, Augustin HG. Tensional forces in fibrillar extracellular matrices control directional capillary sprouting. J Cell Sci. 1999;112(Pt 19):3249-58.
25. 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(16):7843-8.
26. Andersson U, Guo D, Malmer B, Bergenheim AT, Brannstrom T, Hedman H, Henriksson R. Epidermal growth factor receptor family (EGFR, ErbB2-4) in gliomas and meningiomas. Acta Neuropathol. 2004;108(2):135-42.
27. Kanamori M, Kawaguchi T, Nigro JM, Feuerstein BG, Berger MS, Miele L, Pieper RO. Contribution of notch signaling activation to human glioblastoma multiforme. J Neurosurg. 2007;106(3):417-27.
28. Cenciarelli C, Marei HE, Zonfrillo M, Pierimarchi P, Paldino E, Casalbore P, Felsani A, Vescovi AL, Maira G, Mangiola A. PDGF receptor alpha inhibition induces apoptosis in glioblastoma cancer stem cells refractory to anti-notch and anti-EGFR treatment. Mol Cancer. 2014;13:247.
29. Wang WM, Zhao ZL, Ma SR, Yu GT, Liu B, Zhang L, Zhang WF, Kulkarni AB, Sun ZJ, Zhao YF. Epidermal growth factor receptor inhibition reduces angiogenesis via hypoxia-inducible factor-1alpha and notch1 in head neck squamous cell carcinoma. PLoS One. 2015;10(2):e0119723.
30. Takano S, Yoshii Y, Kondo S, Suzuki H, Maruno T, Shirai S, Nose T. Concentration of vascular endothelial growth factor in the serum and tumor tissue of brain tumor patients. Cancer Res. 1996;56(9):2185-90.
31. Nam DH, Park K, Suh YL, Kim JH. Expression of VEGF and brain specific angiogenesis inhibitor-1 in glioblastoma: prognostic significance. Oncol Rep. 2004;11(4):863-9.
32. Zhou L, Wang DS, Li QJ, Sun W, Zhang Y, Dou KF. Downregulation of the notch signaling pathway inhibits hepatocellular carcinoma cell invasion by inactivation of matrix metalloproteinase-2 and -9 and vascular endothelial growth factor. Oncol Rep. 2012;28(3):874-82.
33. Wang Z, Banerjee S, Li Y, Rahman KM, Zhang Y, Sarkar FH. Down-regulation of notch-1 inhibits invasion by inactivation of nuclear factor-kappaB, vascular endothelial growth factor, and matrix metalloproteinase-9 in pancreatic cancer cells. Cancer Res. 2006;66(5):2778-84.
34. Pore N, Jiang Z, Gupta A, Cerniglia G, Kao GD, Maity A. EGFR tyrosine kinase inhibitors decrease VEGF expression by both hypoxia-inducible factor (HIF)-1-independent and HIF-1-dependent mechanisms. Cancer Res. 2006;66(6):3197-204.
35. Thurston G, Kitajewski J. VEGF and delta-notch: interacting signalling pathways in tumour angiogenesis. Br J Cancer. 2008;99(8):1204-9.
36. Paris D, Quadros A, Patel N, DelleDonne A, Humphrey J, Mullan M. Inhibition of angiogenesis and tumor growth by beta and gamma-secretase inhibitors. Eur J Pharmacol. 2005;514(1):1-15.
37. Li JL, Sainson RC, Oon CE, Turley H, Leek R, Sheldon H, Bridges E, Shi W, Snell C, Bowden ET, et al. DLL4-notch signaling mediates tumor resistance to anti-VEGF therapy in vivo. Cancer Res. 2011;71(18):6073-83.
38. Raghu H, Lakka SS, Gondi CS, Mohanam S, Dinh DH, Gujrati M, Rao JS. Suppression of uPA and uPAR attenuates angiogenin mediated angiogenesis in endothelial and glioblastoma cell lines. PLoS One. 2010;5(8):e12458.
39. Nicosia RF, Nicosia SV, Smith M. Vascular endothelial growth factor, platelet-derived growth factor, and insulin-like growth factor-1 promote rat aortic angiogenesis in vitro. Am J Pathol. 1994;145(5):1023-9.
40. Granata R, Trovato L, Lupia E, Sala G, Settanni F, Camussi G, Ghidoni R, Ghigo E. Insulin-like growth factor binding protein-3 induces angiogenesis through IGF-I- and SphK1-dependent mechanisms. J Thromb Haemost. 2007;5(4):835-45.
41. Zadeh G, Bhat KP, Aldape K. EGFR and EGFRvIII in glioblastoma: partners in crime. Cancer Cell. 2013;24(4):403-4.
42. Azuaje F, Tiemann K, Niclou SP. Therapeutic control and resistance of the EGFR-driven signaling network in glioblastoma. Cell Commun Signal. 2015;13:23.
43. Stockhausen MT, Kristoffersen K, Poulsen HS. Notch signaling and brain tumors. Adv Exp Med Biol. 2012;727:289-304.
44. Ma J, Meng Y, Kwiatkowski DJ, Chen X, Peng H, Sun Q, Zha X, Wang F, Wang Y, Jing Y, et al. Mammalian target of rapamycin regulates murine and human cell differentiation through STAT3/p63/jagged/notch cascade. J Clin Invest. 2010;120(1):103-14.
45. Reardon DA, Wen PY, Mellinghoff IK. Targeted molecular therapies against epidermal growth factor receptor: past experiences and challenges. Neuro Oncol. 2014;16(Suppl 8):viii7-13.
46. Krop I, Demuth T, Guthrie T, Wen PY, Mason WP, Chinnaiyan P, Butowski N, Groves MD, Kesari S, Freedman SJ, et al. Phase I pharmacologic and pharmacodynamic study of the gamma secretase (notch) inhibitor MK-0752 in adult patients with advanced solid tumors. J Clin Oncol. 2012;30(19):2307-13.