Glioblastoma-derived epidermal growth factor receptor carboxyl-terminal deletion mutants are transforming and are sensitive to EGFR-directed therapies

Cancer Research

Volumn 71, Issue 24, 2011, Pages 7587-7596

  Cho, Jeonghee ^a,b   Pastorino, Sandra ^c   Zeng, Qing ^a   Xu, Xiaoyin ^a   Johnson, William ^a   Vandenberg, Scott ^d   Verhaak, Roel ^a,e   Cherniack, Andrew D ^e   Watanabe, Hideo ^a,e   Dutt, Amit ^a,e,f   Kwon, Jihyun ^b   Chao, Ying S ^c   Onofrio, Robert C ^e   Chiang, Derek ^a,e,g   Yuza, Yuki ^a,e   Kesari, Santosh ^c,h   Meyerson, Matthew ^a,e  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b Samsung Medical Center   (South Korea)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^f TATA MEMORIAL HOSPITAL   (India)

^g UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^h DANA FARBER CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CETUXIMAB; EPIDERMAL GROWTH FACTOR RECEPTOR; ERLOTINIB; LIGAND; MUTANT PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOPHOSPHORYLATION; CANCER SURVIVAL; CARBOXY TERMINAL SEQUENCE; CARCINOGENICITY; CELL TRANSFORMATION; CONTROLLED STUDY; DRUG MECHANISM; DRUG TARGETING; EPIDERMAL GROWTH FACTOR RECEPTOR GENE; GENE; GENE DELETION; GLIOBLASTOMA; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SURVIVAL TIME;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTINEOPLASTIC AGENTS; BRAIN NEOPLASMS; CELL LINE; CELL LINE, TUMOR; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; EXONS; GENE DELETION; GLIOBLASTOMA; HUMANS; KAPLAN-MEIER ESTIMATE; MICE; MICE, SCID; MUTATION; NIH 3T3 CELLS; PHOSPHORYLATION; PROTEIN KINASE INHIBITORS; QUINAZOLINES; RECEPTOR, EPIDERMAL GROWTH FACTOR; TUMOR BURDEN; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84255170397     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-11-0821     Document Type: Article

References (50)

1. Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJ, et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 2005;352:987-96. (Pubitemid 40349501)
2. DeAngelis LM. Brain tumors. N Engl J Med 2001;344:114-23. (Pubitemid 32052502)
3. Gurney JG, Kadan-Lottick N. Brain and other central nervous system tumors: rates, trends, and epidemiology. Curr Opin Oncol 2001;13:160-6. (Pubitemid 32433971)
4. Dietrich J, Diamond EL, Kesari S. Glioma stem cell signaling: therapeutic opportunities and challenges. Expert Rev Anticancer Ther 2010;10:709-22.
5. Verhaak RG, Hoadley KA, Purdom E, Wang V, Qi Y, Wilkerson MD, et al. Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell 2010;17:98-110.
6. Rao SK, Edwards J, Joshi AD, Siu IM, Riggins GJ. A survey of glioblastoma genomic amplifications and deletions. J Neurooncol 2010;96:169-79.
7. Toth J, Egervari K, Klekner A, Bognar L, Szanto J, Nemes Z, et al. Analysis of EGFR gene amplification, protein over-expression and tyrosine kinase domain mutation in recurrent glioblastoma. Pathol Oncol Res 2009;15:225-9.
8. The Cancer Genome Atlas Research Network. Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature 2008;455:1061-8.
9. Parsons DW, Jones S, Zhang X, Lin JC, Leary RJ, Angenendt P, et al. An integrated genomic analysis of human glioblastoma multiforme. Science 2008;321:1807-12.
10. Libermann TA, Nusbaum HR, Razon N, Kris R, Lax I, Soreq H, et al. Amplification, enhanced expression and possible rearrangement of EGF receptor gene in primary human brain tumours of glial origin. Nature 1985;313:144-7. (Pubitemid 15192341)
11. Schwechheimer K, Huang S, Cavenee WK. EGFR gene amplification- rearrangement in human glioblastomas. Int J Cancer 1995;62:145-8.
12. Malden LT, Novak U, Kaye AH, Burgess AW. Selective amplification of the cytoplasmic domain of the epidermal growth factor receptor gene in glioblastoma multiforme. Cancer Res 1988;48:2711-4.
13. Yamazaki H, Fukui Y, Ueyama Y, Tamaoki N, Kawamoto T, Taniguchi S, et al. Amplification of the structurally and functionally altered epidermal growth factor receptor gene (c-erbB) in human brain tumors. Mol Cell Biol 1988;8:1816-20.
14. Lee JC, Vivanco I, Beroukhim R, Huang JH, Feng WL, DeBiasi RM, et al. Epidermal growth factor receptor activation in glioblastoma through novel missense mutations in the extracellular domain. PLoS Med 2006;3:e485.
15. Nishikawa R, Ji XD, Harmon RC, Lazar CS, Gill GN, Cavenee WK, et al. A mutant epidermal growth factor receptor common in human glioma confers enhanced tumorigenicity. Proc Natl Acad Sci U S A 1994;91:7727-31. (Pubitemid 24238258)
16. Nagane M, Coufal F, Lin H, Bogler O, Cavenee WK, Huang HJ. 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. (Pubitemid 26374452)
17. 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 U S A 1992;89:4309-13.
18. Frederick L, Wang XY, Eley G, James CD. Diversity and frequency of epidermal growth factor receptor mutations in human glioblastomas. Cancer Res 2000;60:1383-7. (Pubitemid 30152011)
19. Shinojima N, Tada K, Shiraishi S, Kamiryo T, Kochi M, Nakamura H, et al. Prognostic value of epidermal growth factor receptor in patients with glioblastoma multiforme. Cancer Res 2003;63:6962-70. (Pubitemid 37322983)
20. Lassman AB, Rossi MR, Raizer JJ, Abrey LE, Lieberman FS, Grefe CN, 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. (Pubitemid 41611629)
21. Narita Y, Nagane M, Mishima K, Huang HJ, Furnari FB, Cavenee WK. Mutant epidermal growth factor receptor signaling down-regulates p27 through activation of the phosphatidylinositol 3-kinase/Akt pathway in glioblastomas. Cancer Res 2002;62:6764-9. (Pubitemid 35364149)
22. Huang PH, Xu AM, White FM. Oncogenic EGFR signaling networks in glioma. Sci Signal 2009;2:re6.
23. Wen PY, Kesari S. Malignant gliomas in adults.NEngl JMed 2008;359:492-507.
24. van den Bent MJ, Brandes AA, Rampling R, Kouwenhoven MC, Kros JM, Carpentier AF, et al. Randomized phase II trial of erlotinib versus temozolomide or carmustine in recurrent glioblastoma: EORTC brain tumor group study 26034. J Clin Oncol 2009;27:1268-74.
25. Reardon DA, Desjardins A, Vredenburgh JJ, Gururangan S, Friedman AH, Herndon JE 2nd, et al. Phase 2 trial of erlotinib plus sirolimus in adults with recurrent glioblastoma. J Neurooncol 2010;96:219-30.
26. Mellinghoff IK, Wang MY, Vivanco I, Haas-Kogan DA, Zhu S, Dia EQ, et al. Molecular determinants of the response of glioblastomas to EGFR kinase inhibitors. N Engl J Med 2005;353:2012-24. (Pubitemid 41609094)
27. Yang SH, Hong YK, Jeun SS, Kim IS, Hong JT, Sung JH, et al. Assessment of cetuximab efficacy by bioluminescence monitoring of intracranial glioblastoma xenograft in mouse. J Neurooncol 2009;95:23-8.
28. Diaz Miqueli A, Rolff J, Lemm M, Fichtner I, Perez R, Montero E. Radiosensitisation of U87MG brain tumours by anti-epidermal growth factor receptor monoclonal antibodies. Br J Cancer 2009;100:950-8.
29. Eller JL, Longo SL, Hicklin DJ, Canute GW. Activity of anti-epidermal growth factor receptor monoclonal antibody C225 against glioblastoma multiforme. Neurosurgery 2002;51:1005-13; discussion 13-4.
30. Belda-Iniesta C, Carpeno Jde C, Saenz EC, Gutierrez M, Perona R, Baron MG. Long term responses with cetuximab therapy in glioblastoma multiforme. Cancer Biol Ther 2006;5:912-4.
31. Greulich H, Chen TH, Feng W, Janne PA, Alvarez JV, Zappaterra M, et al. Oncogenic transformation by inhibitor-sensitive and -resistant EGFR mutants. PLoS Med 2005;2:e313.
32. Ji H, Zhao X, Yuza Y, Shimamura T, Li D, Protopopov A, et al. Epidermal growth factor receptor variant III mutations in lung tumorigenesis and sensitivity to tyrosine kinase inhibitors. Proc Natl Acad Sci U S A 2006;103:7817-22.
33. Jiang J, Greulich H, Janne PA, Sellers WR, Meyerson M, Griffin JD. Epidermal growth factor-independent transformation of Ba/F3 cells with cancer-derived epidermal growth factor receptor mutants induces gefitinib-sensitive cell cycle progression. Cancer Res 2005; 65:8968-74. (Pubitemid 41377388)
34. Stegh AH, Kesari S,Mahoney JE, Jenq HT, Forloney KL, Protopopov A, et al. Bcl2L12-mediated inhibition of effector caspase-3 and caspase-7 via distinct mechanisms in glioblastoma. Proc Natl Acad Sci U S A 2008;105:10703-8.
35. Ligon KL, Huillard E, Mehta S, Kesari S, Liu H, Alberta JA, et al. Olig2-regulated lineage-restricted pathway controls replication competence in neural stem cells and malignant glioma. Neuron 2007;53:503-17. (Pubitemid 46216748)
36. Sequist LV, Besse B, Lynch TJ, Miller VA, Wong KK, Gitlitz B, et al. Neratinib, an irreversible pan-ErbB receptor tyrosine kinase inhibitor: results of a phase II trial in patients with advanced non-small-cell lung cancer. J Clin Oncol 2010;28:3076-83.
37. Walker F, Hibbs ML, Zhang HH, Gonez LJ, Burgess AW. Biochemical characterization of mutant EGF receptors expressed in the hemopoietic cell line BaF/3. Growth Factors 1998;16:53-67. (Pubitemid 28499711)
38. Jonker DJ, O'Callaghan CJ, Karapetis CS, Zalcberg JR, Tu D, Au HJ, et al. Cetuximab for the treatment of colorectal cancer. N Engl J Med 2007;357:2040-8. (Pubitemid 350106711)
39. Mitsudomi T, Morita S, Yatabe Y, Negoro S, Okamoto I, Tsurutani J, et al. Gefitinib versus cisplatin plus docetaxel in patients with non-small-cell lung cancer harbouring mutations of the epidermal growth factor receptor (WJTOG3405): an open label, randomised phase 3 trial. Lancet Oncol 2010;11:121-8.
40. Chen WS, Lazar CS, Lund KA, Welsh JB, Chang CP, Walton GM, et al. Functional independence of the epidermal growth factor receptor from a domain required for ligand-induced internalization and calcium regulation. Cell 1989;59:33-43. (Pubitemid 19248556)
41. Grandal MV, Zandi R, Pedersen MW, Willumsen BM, van Deurs B, Poulsen HS. EGFRvIII escapes down-regulation due to impaired internalization and sorting to lysosomes. Carcinogenesis 2007;28:1408-17. (Pubitemid 47241789)
42. Masui H, Wells A, Lazar CS, Rosenfeld MG, Gill GN. Enhanced tumorigenesis of NR6 cells which express non-down-regulating epidermal growth factor receptors. Cancer Res 1991;51:6170-5.
43. Wells A, Welsh JB, Lazar CS, Wiley HS, Gill GN, Rosenfeld MG. Ligand-induced transformation by a noninternalizing epidermal growth factor receptor. Science 1990;247:962-4.
44. Zhang X, Pickin KA, Bose R, Jura N, Cole PA, Kuriyan J. Inhibition of the EGF receptor by binding of MIG6 to an activating kinase domain interface. Nature 2007;450:741-4. (Pubitemid 350207680)
45. Ying H, Zheng H, Scott K, Wiedemeyer R, Yan H, Lim C, et al. Mig-6 controls EGFR trafficking and suppresses gliomagenesis. Proc Natl Acad Sci U S A 2010;107:6912-7.
46. Beebe JA, Wiepz GJ, Guadarrama AG, Bertics PJ, Burke TJ. A carboxyl-terminal mutation of the epidermal growth factor receptor alters tyrosine kinase activity and substrate specificity as measured by a fluorescence polarization assay. J Biol Chem 2003; 278:26810-6. (Pubitemid 36876830)
47. Jura N, Endres NF, Engel K, Deindl S, Das R, Lamers MH, et al. Mechanism for activation of the EGF receptor catalytic domain by the juxtamembrane segment. Cell 2009;137:1293-307.
48. Pines G, Huang PH, Zwang Y, White FM, Yarden Y. EGFRvIV: a previously uncharacterized oncogenic mutant reveals a kinase auto-inhibitory mechanism. Oncogene 2010;29:5850-60.
49. Harding J, Burtness B. Cetuximab: an epidermal growth factor receptor chemeric human-murine monoclonal antibody. Drugs Today (Barc) 2005;41:107-27. (Pubitemid 40461533)
50. Li S, Schmitz KR, Jeffrey PD, Wiltzius JJW, Kussie P, Ferguson KM. Structural basis for inhibition of the epidermal growth factor receptor by cetuximab. Cancer Cell 2005;7:301-11. (Pubitemid 40544648)