Challenges to targeting epidermal growth factor receptor in glioblastoma: Escape mechanisms and combinatorial treatment strategies

Neuro-Oncology

Volumn 16, Issue , 2014, Pages viii14-viii19

  Roth, Patrick ^a   Weller, Michael ^a  

^a UNIVERSITY HOSPITAL ZURICH   (Switzerland)

Author keywords

EGFR; EGFRvIII; escape mechanism; therapeutic targeting; therapy resistance

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR ANTIBODY; EPIDERMAL GROWTH FACTOR RECEPTOR KINASE INHIBITOR; ANTINEOPLASTIC AGENT;

CANCER IMMUNOTHERAPY; CANCER PATIENT; CANCER RESISTANCE; DRUG MECHANISM; DRUG TARGETING; GLIOBLASTOMA; HUMAN; IN VITRO STUDY; IN VIVO STUDY; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); REVIEW; ANTAGONISTS AND INHIBITORS; BRAIN NEOPLASMS; DRUG RESISTANCE; IMMUNOLOGY; METABOLISM; SIGNAL TRANSDUCTION; TREATMENT OUTCOME;

ANTINEOPLASTIC AGENTS; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; BRAIN NEOPLASMS; DRUG RESISTANCE, NEOPLASM; GLIOBLASTOMA; HUMANS; RECEPTOR, EPIDERMAL GROWTH FACTOR; SIGNAL TRANSDUCTION; TREATMENT OUTCOME;

EID: 84911112588     PISSN: 15228517     EISSN: 15235866     Source Type: Journal    
DOI: 10.1093/neuonc/nou222     Document Type: Review

References (58)

1. Weller M, van den Bent M, Hopkins K, et al. EANO guideline on the diagnosis and treatment of malignant glioma. Lancet Oncol. 2014; 15(9):e395-e403.
2. Hatanpaa KJ, Burma S, Zhao D, et al. Epidermal growth factor receptor in glioma: signal transduction, neuropathology, imaging, and radioresistance. Neoplasia. 2010;12(9):675-684.
3. Schneider MR, Wolf E. The epidermal growth factor receptor ligands at a glance. J Cell Physiol. 2009;218(3):460-466.
4. Weller M, Kaulich K, Hentschel B, et al. Assessment and prognostic significance of the epidermal growth factor receptor vIII mutation in glioblastoma patients treated with concurrent and adjuvant temozolomide radiochemotherapy. Int J Cancer. 2014;134(10): 2437-2447.
5. Heimberger AB, Hlatky R, Suki D, et al. Prognostic effect of epidermal growth factor receptor and EGFRvIII in glioblastoma multiforme patients. Clin Cancer Res. 2005;11(4):1462-1466.
6. Steinbach JP, Supra P, Huang HJ, et al. CD95-mediated apoptosis of human glioma cells: modulation by epidermal growth factor receptor activity. Brain Pathol. 2002;12(1):12-20.
7. Steinbach JP, Supra P, Huang HJ, et al. CD95-mediated apoptosis of human glioma cells: modulation by epidermal growth factor receptor activity. Brain Pathol. 2002;12(1):12-20.
8. Munoz JL, Rodriguez-Cruz V, Greco SJ, et al. Temozolomide resistance in glioblastoma cells occurs partly through epidermal growth factor receptor-mediated induction of connexin 43. Cell Death Dis. 2014;5: e1145.
9. Marie Y, Carpentier AF, Omuro AM, et al. EGFR tyrosine kinase domain mutations in human gliomas. Neurology. 2005;64(8):1444-1445.
10. Mellinghoff IK, Wang MY, Vivanco I, et al. Molecular determinants of the response of glioblastomas to EGFR kinase inhibitors. N Engl J Med. 2005;353(19):2012-2024.
11. Vivanco I, Robins HI, Rohle D, et al. Differential sensitivity of glioma versus lung cancer-specific EGFR mutations to EGFR kinase inhibitors. Cancer Discov. 2012;2(5):458-471.
12. Brennan CW, Verhaak RG, McKenna A, et al. The somatic genomic landscape of glioblastoma. Cell. 2013;155(2):462-477.
13. Weiner LM, Surana R, Wang S. Monoclonal antibodies: versatile platforms for cancer immunotherapy. Nat Rev Immunol. 2010; 10(5):317-327.
14. Lassman AB, Rossi MR, Raizer JJ, 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(21):7841-7850.
15. Stommel JM, Kimmelman AC, Ying H, et al. Coactivation of receptor tyrosine kinases affects the response of tumor cells to targeted therapies. Science. 2007;318(5848):287-290.
16. Snuderl M, Fazlollahi L, Le LP, et al. Mosaic amplification of multiple receptor tyrosine kinase genes in glioblastoma. Cancer Cell. 2011; 20(6):810-817.
17. Bianco R, Shin I, Ritter CA, et al. Loss of PTEN/MMAC1/TEP in EGF receptor-expressing tumor cells counteracts the antitumor action of EGFR tyrosine kinase inhibitors. Oncogene. 2003;22(18): 2812-2822.
18. Wang MY, Lu KV, Zhu S, et al. Mammalian target of rapamycin inhibition promotes response to epidermal growth factor receptor kinase inhibitors in PTEN-deficient and PTEN-intact glioblastoma cells. Cancer Res. 2006;66(16):7864-7869.
19. Fan QW, Cheng CK, Nicolaides TP, et al. A dual phosphoinositide-3-kinase alpha/mTOR inhibitor cooperates with blockade of epidermal growth factor receptor in PTEN-mutant glioma. Cancer Res. 2007;67(17):7960-7965.
20. Fenton TR, Nathanson D, Ponte de Albuquerque C, et al. Resistance to EGF receptor inhibitors in glioblastoma mediated by phosphorylation of the PTEN tumor suppressor at tyrosine 240. Proc Natl Acad Sci USA. 2012;109(35):14164-14169.
21. Li J, Zhu S, Kozono D, et al. Genome-wide shRNA screen revealed integrated mitogenic signaling between dopamine receptor D2 (DRD2) and epidermal growth factor receptor (EGFR) in glioblastoma. Oncotarget. 2014;5(4):882-893.
22. Akhavan D, Pourzia AL, Nourian AA, et al. De-repression of PDGFRb transcription promotes acquired resistance to EGFR tyrosine kinase inhibitors in glioblastoma patients. Cancer Discov. 2013;3(5): 534-547.
23. Iwanami A, Gini B, Zanca C, et al. PML mediates glioblastoma resistance to mammalian target of rapamycin (mTOR)-targeted therapies. Proc Natl Acad Sci USA. 2013;110(11):4339-4344.
24. Srikanth M, Das S, Berns EJ, et al. Nanofiber-mediated inhibition of focal adhesion kinase sensitizes glioma stemlike cells to epidermal growth factor receptor inhibition. Neuro Oncol. 2013;15(3):319-329.
25. Eimer S, Dugay F, Airiau K, et al. Cyclopamine cooperates with EGFR inhibition to deplete stem-like cancer cells in glioblastoma-derived spheroid cultures. Neuro Oncol. 2012;14(12):1441-1451.
26. Geoerger B, Gaspar N, Opolon P, et al. EGFR tyrosine kinase inhibition radiosensitizes and induces apoptosis in malignant glioma and childhood ependymoma xenografts. Int J Cancer. 2008;123(1): 209-216.
27. Krishnan S, Brown PD, Ballman KV, et al. Phase I trial of erlotinib with radiation therapy in patients with glioblastoma multiforme: results of North Central Cancer Treatment Group protocol N0177. Int J Radiat Oncol Biol Phys. 2006;65(4):1192-1199.
28. Chakravarti A, Wang M, Robins HI, et al. RTOG 0211: a phase 1/2 study of radiation therapy with concurrent gefitinib for newly diagnosed glioblastoma patients. Int J Radiat Oncol Biol Phys. 2013;85(5):1206-1211.
29. Prados MD, Chang SM, Butowski N, et al. Phase II study of erlotinib plus temozolomide during and after radiation therapy in patients with newly diagnosed glioblastoma multiforme or gliosarcoma. J Clin Oncol. 2009;27(4):579-584.
30. Reardon DA, Groves MD, Wen PY, et al. A phase I/II trial of pazopanib in combination with lapatinib in adult patients with relapsed malignant glioma. Clin Cancer Res. 2013;19(4):900-908.
31. Kreisl TN, Lassman AB, Mischel PS, et al. A pilot study of everolimus and gefitinib in the treatment of recurrent glioblastoma (GBM). J Neurooncol. 2009;92(1):99-105.
32. Wen PY, Chang SM, Lamborn KR, et al. Phase I/II study of erlotinib and temsirolimus for patients with recurrent malignant gliomas: North American Brain Tumor Consortium trial 04-02. Neuro Oncol. 2014;16(4):567-578.
33. Eisenstat DD, Nabors L, Mason W, et al. A phase II study of daily afatinib (BIBW 2992) with or without temozolomide (21/28 days) in the treatment of patients with recurrent glioblastoma. J Clin Oncol. 2011;29(suppl; abstr 2010).
34. Solomon MT, Selva JC, Figueredo J, et al. Radiotherapy plus nimotuzumab or placebo in the treatment of high grade glioma patients: results from a randomized, double blind trial. BMC Cancer. 2013;13:299.
35. Bartels U,Wolff J, Gore L, et al. Phase 2 study of safety and efficacy of nimotuzumab in pediatric patients with progressive diffuse intrinsic pontine glioma. Neuro Oncol. 2014.
36. Weinandy A, Piroth MD, Goswami A, et al. Cetuximab induces eme1-mediated DNA repair: a novel mechanism for cetuximab resistance. Neoplasia. 2014;16(3):207-220.
37. Johns TG, Perera RM, Vernes SC, et al. The efficacy of epidermal growth factor receptor-specific antibodies against glioma xenografts is influenced by receptor levels, activation status, and heterodimerization. Clin Cancer Res. 2007;13(6):1911-1925.
38. Mishima K, Johns TG, Luwor RB, et al. Growth suppression of intracranial xenografted glioblastomas overexpressing mutant epidermal growth factor receptors by systemic administration of monoclonal antibody (mAb) 806, a novel monoclonal antibody directed to the receptor. Cancer Res. 2001;61(14):5349-5354.
39. Gan HK, Fichtel L, Lassman AB, et al. A phase 1 study evaluating ABT-414 in combination with temozolomide (TMZ) for subjects with recurrent or unresectable glioblastoma (GBM). J Clin Oncol. 2014;32:5s(suppl; abstr 2021).
40. Wygoda Z, Kula D, Bierzynska-Macyszyn G, et al. Use of monoclonal anti-EGFR antibody in the radioimmunotherapy of malignant gliomas in the context of EGFR expression in grade III and IV tumors. Hybridoma. 2006;25(3):125-132.
41. Liu TF, Hall PD, Cohen KA, et al. Interstitial diphtheria toxin-epidermal growth factor fusion protein therapy produces regressions of subcutaneous human glioblastoma multiforme tumors in athymic nude mice. Clin Cancer Res. 2005;11(1):329-334.
42. Yamazaki H, Kijima H, Ohnishi Y, et al. Inhibition of tumor growth by ribozyme-mediated suppression of aberrant epidermal growth factor receptor gene expression. J Natl Cancer Inst. 1998;90(8):581-587.
43. Kang CS, Pu PY, Li YH, et al. An in vitro study on the suppressive effect of glioma cell growth induced by plasmid-based small interference RNA (siRNA) targeting human epidermal growth factor receptor. J Neurooncol. 2005;74(3):267-273.
44. Nagane M, Levitzki A, Gazit A, et al. Drug resistance of human glioblastoma cells conferred by a tumor-specific mutant epidermal growth factor receptor through modulation of Bcl-XL and caspase-3-like proteases. Proc Natl Acad Sci USA. 1998;95(10): 5724-5729.
45. Montano N, Cenci T, Martini M, et al. Expression of EGFRvIII in glioblastoma: prognostic significance revisited. Neoplasia. 2011; 13(12):1113-1121.
46. Shinojima N, Tada K, Shiraishi S, et al. Prognostic value of epidermal growth factor receptor in patients with glioblastoma multiforme. Cancer Res. 2003;63(20):6962-6970.
47. Emlet DR, Gupta P, Holgado-Madruga M, et al. Targeting a glioblastoma cancer stem-cell population defined by EGF receptor variant III. Cancer Res. 2014;74(4):1238-1249.
48. Fan QW, Cheng CK, Gustafson WC, et al. EGFR phosphorylates tumor-derived EGFRvIII driving STAT3/5 and progression in glioblastoma. Cancer Cell. 2013;24(4):438-449.
49. Inda MM, Bonavia R, Mukasa A, et al. Tumor heterogeneity is an active process maintained by a mutant EGFR-induced cytokine circuit in glioblastoma. Genes Dev. 2010;24(16): 1731-1745.
50. Johnson H, Del Rosario AM, Bryson BD, et al. Molecular characterization of EGFR and EGFRvIII signaling networks in human glioblastoma tumor xenografts. Mol Cell Proteomics. 2012; 11(12):1724-1740.
51. Lal B, Goodwin CR, Sang Y, et al. EGFRvIII and c-Met pathway inhibitors synergize against PTEN-null/EGFRvIII+ glioblastoma xenografts. Mol Cancer Ther. 2009;8(7):1751-1760.
52. Hu J, Jo M, Cavenee WK, et al. Crosstalk between the urokinase-type plasminogen activator receptor and EGF receptor variant III supports survival and growth of glioblastoma cells. Proc Natl Acad Sci USA. 2011;108(38):15984-15989.
53. Chakravarti A, Loeffler JS, Dyson NJ. Insulin-like growth factor receptor I mediates resistance to anti-epidermal growth factor receptor therapy in primary human glioblastoma cells through continued activation of phosphoinositide 3-kinase signaling. Cancer Res. 2002;62(1):200-207.
54. Lotsch D, Steiner E, Holzmann K, et al. Major vault protein supports glioblastoma survival and migration by upregulating the EGFR/PI3K signalling axis. Oncotarget. 2013;4(11):1904-1918.
55. Schulte A, Liffers K, Kathagen A, et al. Erlotinib resistance in EGFR-amplified glioblastoma cells is associated with upregulation of EGFRvIII and PI3Kp110delta. Neuro Oncol. 2013;15(10): 1289-1301.
56. Roth P, Eisele G, Weller M. Immunology of brain tumors. Handb Clin Neurol. 2012;104:45-51.
57. Sampson JH, Heimberger AB, Archer GE, et al. Immunologic escape after prolonged progression-free survival with epidermal growth factor receptor variant III peptide vaccination in patients with newly diagnosed glioblastoma. J Clin Oncol. 2010;28(31): 4722-4729.
58. Pellegatta S, Cuppini L, Finocchiaro G. Brain cancer immunoediting: novel examples provided by immunotherapy of malignant gliomas. Expert Rev Anticancer Ther. 2011;11(11):1759-1774.