EGFR inhibition in glioblastoma cells induces G2/M arrest and is independent of p53

Cancer Biology and Therapy

Volumn 6, Issue 4, 2007, Pages 571-579

  Kapoor, Gurpreet S ^a   Christie, Antoire ^a   O'Rourke, Donald M ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Cdc2; EGFR; erbB; G2 M; GBM; RTK; T691S; TP53

Indexed keywords

CYCLIN D1; CYCLIN DEPENDENT KINASE 1; CYCLIN DEPENDENT KINASE 6; CYCLIN DEPENDENT KINASE INHIBITOR 2B; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 2; GLYCOGEN SYNTHASE KINASE 3ALPHA; GLYCOGEN SYNTHASE KINASE 3BETA; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MUTANT PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; PROTEIN P53;

ANIMAL CELL; ARTICLE; CANCER CELL CULTURE; CELL CYCLE ARREST; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL TRANSFORMATION; CONTROLLED STUDY; GLIA CELL; GLIOBLASTOMA; MOUSE; NONHUMAN; NUDE MOUSE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION;

EID: 34548231710     PISSN: 15384047     EISSN: 15558576     Source Type: Journal    
DOI: 10.4161/cbt.6.4.3852     Document Type: Article

References (64)

1. O'Rourke DM, Nute EJ, Davis JG, Wu C, Lee A, Murali R, Zhang HT, Qian X, Kao CC, Greene MI. Inhibition of a naturally occurring EGFR oncoprotein by the p185neu ectodomain: Implications for subdomain contributions to receptor assembly. Oncogene 1998; 16:1197-207.
2. O'Rourke DM, Qian X, Zhang HT, Davis JG, Nute E, Meinkoth J, Greene MI. Trans receptor inhibition of human glioblastoma cells by erbB family ectodomains. Proc Natl Acad Sci USA 1997; 94:3250-5.
3. Kleihues P, Burger PC, Scheithauer BW. The new WHO classification of brain tumours. Brain Pathol 1993; 3:255-68.
4. Libermann TA, Nusbaum HR, Razon N, Kris R, Lax I, Soreq H, Whittle N, Waterfield MD, Ullrich A, Schlessinger J. Amplification and overexpression of the EGF receptor gene in primary human glioblastomas. J Cell Sci Suppl 1985; 3:161-72.
5. Wong AJ, Bigner SH, Bigner DD, Kinzler KW, Hamilton SR, Vogelstein B. Increased expression of the epidermal growth factor receptor gene in malignant gliomas is invariably associated with gene amplification. Proc Natl Acad Sci USA 1987; 84:6899-903.
6. 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.
7. Louis DN. A molecular genetic model of astrocytoma histopathology. Brain Pathol 1997; 7:755-64.
8. Reifenberger J, Ring GU, Gies U, Cobbers L, Oberstrass J, An HX, Niederacher D, Wechsler W, Reifenberger G. Analysis of p53 mutation and epidermal growth factor receptor amplification in recurrent gliomas with malignant progression. J Neuropathol Exp Neurol 1996; 55:822-31.
9. Watanabe K, Tachibana O, Sata K, Yonekawa Y, Kleihues P, Ohgaki H. Overexpression of the EGF receptor and p53 mutations are mutually exclusive in the evolution of primary and secondary glioblastomas. Brain Pathol 1996; 6:217-23, (discussion 23-4).
10. Vogelstein B, Lane D, Levine AJ. Surfing the p53 network. Nature 2000; 408:307-10.
11. 2/M transition by p53. Oncogene 2001; 20:1803-15.
12. Fridman JS, Lowe SW. Control of apoptosis by p53. Oncogene 2003; 22:9030-40.
13. Olivier M, Eeles R, Hollstein M, Khan MA, Harris CC, Hainaut P. The IARC TP53 database: New online mutation analysis and recommendations to users. Hum Mutat 2002; 19:607-14.
14. Watanabe K, Sato K, Biernat W, Tachibana O, von Ammon K, Ogata N, Yonekawa Y, Kleihues P, Ohgaki H. Incidence and timing of p53 mutations during astrocytoma progression in patients with multiple biopsies. Clin Cancer Res 1997; 3:523-30.
15. Peraud A, Kreth FW, Wiestler OD, Kleihues P, Reulen HJ. Prognostic impact of TP53 mutations and P53 protein overexpression in supratentorial WHO grade II astrocytomas and oligoastrocytomas. Clin Cancer Res 2002; 8:1117-24.
16. Fan S, Smith ML, Rivet IInd DJ, Duba D, Zhan Q, Kohn KW, Fornace Jr AJ, O'Connor PM. Disruption of p53 function sensitizes breast cancer MCF-7 cells to cisplatin and pentoxifylline. Cancer Res 1995; 55:1649-54.
17. Rusch V, Klimstra D, Venkatraman E, Oliver J, Martini N, Gralla R, Kris M, Dmitrovsky E. Aberrant p53 expression predicts clinical resistance to cisplatin-based chemotherapy in locally advanced non-small cell lung cancer. Cancer Res 1995; 55:5038-42.
18. Brachman DG, Beckett M, Graves D, Haraf D, Vokes E, Weichselbaum RR. p53 mutation does not correlate with radiosensitivity in 24 head and neck cancer cell lines. Cancer Res 1993; 53:3667-9.
19. Cunningham JM, Kimmel DW, Scheithauer BW, O'Fallon JR, Novotny PJ, Jenkins RB. Analysis of proliferation markers and p53 expression in gliomas of astrocytic origin: Relationships and prognostic value. J Neurosurg 1997; 86:121-30.
20. Danks RA, Chopra G, Gonzales MF, Orian JM, Kaye AH. Aberrant p53 expression does not correlate with the prognosis in anaplastic astrocytoma. Neurosurgery 1995; 37:246-54.
21. Pollack IF, Finkelstein SD, Woods J, Burnham J, Holmes EJ, Hamilton RL, Yates AJ, Boyett JM, Finlay JL, Sposto R. Expression of p53 and prognosis in children with malignant gliomas. N Engl J Med 2002; 346:420-7.
22. Olayioye MA, Neve RM, Lane HA, Hynes NE. The ErbB signaling network: Receptor heterodimerization in development and cancer. Embo J 2000; 19:3159-67.
23. Yarden Y, Sliwkowski MX. Untangling the ErbB signalling network. Nat Rev Mol Cell Biol 2001; 2:127-37.
24. Baselga J. A new anti-ErbB2 strategy in the treatment of cancer: Prevention of ligand-dependent ErbB2 receptor heterodimerization. Cancer Cell 2002; 2:93-5.
25. Klapper LN, Glathe S, Vaisman N, Hynes NE, Andrews GC, Sela M, Yarden Y. The ErbB-2/HER2 oncoprotein of human carcinomas may function solely as a shared coreceptor for multiple stroma-derived growth factors. Proc Natl Acad Sci USA 1999; 96:4995-5000.
26. Klapper LN, Kirschbaum MH, Sela M, Yarden Y. Biochemical and clinical implications of the ErbB/HER signaling network of growth factor receptors. Adv Cancer Res 2000; 77:25-79.
27. Mendelsohn J, Baselga J. The EGF receptor family as targets for cancer therapy. Oncogene 2000; 19:6550-65.
28. Potti A, Forseen SE, Koka VK, Pervez H, Koch M, Fraiman G, Mehdi SA, Levitt R. Determination of HER-2/neu overexpression and clinical predictors of survival in a cohort of 347 patients with primary malignant brain tumors. Cancer Invest 2004; 22:537-44.
29. 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 (Berl) 2004; 108:135-42.
30. Pegram M, Slamon D. Biological rationale for HER2/neu (c-erbB2) as a target for monoclonal antibody therapy. Semin Oncol 2000; 27:13-9.
31. Tang CK, Gong XQ, Moscatello DK, Wong AJ, Lippman ME. Epidermal growth factor receptor vIII enhances tumorigenicity in human breast cancer. Cancer Res 2000; 60:3081-7.
32. Van Meir EG, Kikuchi T, Tada M, Li H, Diserens AC, Wojcik BE, Huang HJ, Friedmann T, de Tribolet N, Cavenee WK. Analysis of the p53 gene and its expression in human glioblastoma cells. Cancer Res 1994; 54:649-52.
33. Gomez-Manzano C, Fueyo J, Kyritsis AP, Steck PA, Roth JA, McDonnell TJ, Steck KD, Levin VA, Yung WK. Adenovirus-mediated transfer of the p53 gene produces rapid and generalized death of human glioma cells via apoptosis. Cancer Res 1996; 56:694-9.
34. Terasaki M, Kato S, Sugita Y, Shigemori M, Morimatsu M. Adenovirus-mediated over-expression of p21Waf-1 differentially affects the proliferation, telomerase activity, and expression of glial fibrillary acidic protein in human glioma cells. Int J Oncol 1999; 14:63-9.
35. Li H, Lochmuller H, Yong VW, Karpati G, Nalbantoglu J. Adenovirus-mediated wild-type p53 gene transfer and overexpression induces apoptosis of human glioma cells independent of endogenous p53 status. J Neuropathol Exp Neurol 1997; 56:872-8.
36. Asai A, Miyagi Y, Sugiyama A, Gamanuma M, Hong SH, Takamoto S, Nomura K, Matsutani M, Takakura K, Kuchino Y. Negative effects of wild-type p53 and s-Myc on cellular growth and tumorigenicity of glioma cells: Implication of the tumor suppressor genes for gene therapy. J Neurooncol 1994; 19:259-68.
37. Kapoor GS, Zhan Y, Johnson GR, O'Rourke DM. Distinct domains in the SHP-2 phosphatase differentially regulate epidermal growth factor receptor/NF-kappaB activation through Gab1 in glioblastoma cells. Mol Cell Biol 2004; 24:823-36.
38. Qian X, LeVea CM, Freeman JK, Dougall WC, Greene MI. Heterodimerization of epidermal growth factor receptor and wild-type or kinase-deficient Neu: A mechanism of interreceptor kinase activation and transphosphorylation. Proc Natl Acad Sci USA 1994; 91:1500-4.
39. Drebin JA, Link VC, Stern DF, Weinberg RA, Greene MI. Down-modulation of an oncogene protein product and reversion of the transformed phenotype by monoclonal antibodies. Cell 1985; 41:697-706.
40. Haas-Kogan D, Shalev N, Wong M, Mills G, Yount G, Stokoe D. Protein kinase B (PKB/Akt) activity is elevated in glioblastoma cells due to mutation of the tumor suppressor PTEN/MMAC. Curr Biol 1998; 8:1195-8.
41. Holland EC, Celestino J, Dai C, Schaefer L, Sawaya RE, Fuller GN. Combined activation of Ras and Akt in neural progenitors induces glioblastoma formation in mice. Nat Genet 2000; 25:55-7.
42. Sonoda Y, Ozawa T, Aldape KD, Deen DF, Berger MS, Pieper RO. Akt pathway activation converts anaplastic astrocytoma to glioblastoma multiforme in a human astrocyte model of glioma. Cancer Res 2001; 61:6674-8.
43. Kapoor GS, O'Rourke DM. Mitogenic signaling cascades in glial tumors. Neurosurgery 2003; 52:1425-34, (discussion 34-5).
44. 1-S transition control gene abnormalities. Cancer Res 2000; 60:417-24.
45. Hulleman E, Helin K. Molecular mechanisms in gliomagenesis. Adv Cancer Res 2005; 94:1-27.
46. Gomez-Manzano C, Fueyo J, Kyritsis AP, McDonnell TJ, Steck PA, Levin VA, Yung WK. Characterization of p53 and p21 functional interactions in glioma cells en route to apoptosis. J Natl Cancer Inst 1997; 89:1036-44.
47. Lang FF, Bruner JM, Fuller GN, Aldape K, Prados MD, Chang S, Berger MS, McDermott MW, Kunwar SM, Junck LR, Chandler W, Zwiebel JA, Kaplan RS, Yung WK. Phase I trial of adenovirus-mediated p53 gene therapy for recurrent glioma: Biological and clinical results. J Clin Oncol 2003; 21:2508-18.
48. Tzahar E, Waterman H, Chen X, Levkowitz G, Karunagaran D, Lavi S, Ratzkin BJ, Yarden Y. A hierarchical network of interreceptor interactions determines signal transduction by Neu differentiation factor/neuregulin and epidermal growth factor. Mol Cell Biol 1996; 16:5276-87.
49. Lenferink AE, Pinkas-Kramarski R, van de Poll ML, van Vugt MJ, Klapper LN, Tzahar E, Waterman H, Sela M, van Zoelen EJ, Yarden Y. Differential endocytic routing of homo- and hetero-dimeric ErbB tyrosine kinases confers signaling superiority to receptor heterodimers. Embo J 1998; 17:3385-97.
50. Kapoor GS, O'Rourke DM. Receptor tyrosine kinase signaling in gliomagenesis: Pathobiology and therapeutic approaches. Cancer Biol Ther 2003; 2:330-42.
51. Cross DA, Alessi DR, Cohen P, Andjelkovich M, Hemmings BA. Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature 1995; 378:785-9.
52. Sulis ML, Parsons R. PTEN: From pathology to biology. Trends Cell Biol 2003; 13:478-83.
53. Diehl JA, Cheng M, Roussel MF, Sherr CJ. Glycogen synthase kinase-3beta regulates cyclin D1 proteolysis and subcellular localization. Genes Dev 1998; 12:3499-511.
54. Ramljak D, Calvert RJ, Wiesenfeld PW, Diwan BA, Catipovic B, Marasas WF, Victor TC, Anderson LM, Gelderblom WC. A potential mechanism for fumonisin B(1)-mediated hepatocarcinogenesis: Cyclin D1 stabilization associated with activation of Akt and inhibition of GSK-3beta activity. Carcinogenesis 2000; 21:1537-46.
55. Hannon GJ, Beach D. p15INK4B is a potential effector of TGF-beta-induced cell cycle arrest. Nature 1994; 371:257-61.
56. Pavletich NP. Mechanisms of cyclin-dependent kinase regulation: Structures of Cdks, their cyclin activators, and Cip and INK4 inhibitors. J Mol Biol 1999; 287:821-8.
57. Guan KL, Jenkins CW, Li Y, Nichols MA, Wu X, O'Keefe CL, Matera AG, Xiong Y. Growth suppression by p18, a p16INK4/MTS1- and p14INK4B/MTS2-related CDK6 inhibitor, correlates with wild-type pRb function. Genes Dev 1994; 8:2939-52.
58. Hirai H, Roussel MF, Kato JY, Ashmun RA, Sherr CJ. Novel INK4 proteins, p19 and p18, are specific inhibitors of the cyclin D-dependent kinases CDK4 and CDK6. Mol Cell Biol 1995; 15:2672-81.
59. Kastan MB, Bartek J. Cell-cycle checkpoints and cancer. Nature 2004; 432:316-23.
60. Nyberg KA, Michelson RJ, Putnam CW, Weinert TA. Toward maintaining the genome: DNA damage and replication checkpoints. Annu Rev Genet 2002; 36:617-56.
61. Sancar A, Lindsey-Boltz LA, Unsal-Kacmaz K, Linn S. Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu Rev Biochem 2004; 73:39-85.
62. Okumura E, Fukuhara T, Yoshida H, Hanada Si S, Kozutsumi R, Mori M, Tachibana K, Kishimoto T. Akt inhibits Myt1 in the signalling pathway that leads to meiotic G2/M-phase transition. Nat Cell Biol 2002; 4:111-6.
63. 2/M transition. Mol Cell Biol 2005; 25:5725-37.
64. 2/M checkpoint activation by etoposide through the Akt/GSK3 pathway to inhibit apoptosis. Oncogene 2005; 24:1973-81.