Development of resistance to EGFR-targeted therapy in malignant glioma can occur through EGFR-dependent and -independent mechanisms

Cancer Research

Volumn 75, Issue 10, 2015, Pages 2109-2119

  Klingler, Stefan ^a   Guo, Baofeng ^a   Yao, Jun ^b   Yan, Haiyan ^c   Zhang, Ling ^a   Vaseva, Angelina V ^a   Chen, Sida ^a   Canoll, Peter ^d   Horner, James W ^b   Wang, Y Alan ^b   Paik, Ji Hye ^e   Ying, Haoqiang ^b   Zheng, Hongwu ^a  

^a Simons Center for Quantitative Biology   (United States)

^b UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^c DANA FARBER CANCER INSTITUTE   (United States)

^d Department of Medicine   (United States)

^e WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CRIZOTINIB; CYCLIN DEPENDENT KINASE INHIBITOR 2A; DACTOLISIB; DOXYCYCLINE; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR KINASE INHIBITOR; ERLOTINIB; GEFITINIB; MAMMALIAN TARGET OF RAPAMYCIN; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; SCATTER FACTOR; EGFR PROTEIN, MOUSE; IMIDAZOLE DERIVATIVE; PTEN PROTEIN, MOUSE; PYRAZOLE DERIVATIVE; PYRIDINE DERIVATIVE; QUINAZOLINE DERIVATIVE; QUINOLINE DERIVATIVE;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; AUTOPHOSPHORYLATION; CANCER RESISTANCE; CARCINOGENESIS; CONTROLLED STUDY; GLIOMA; IN VITRO STUDY; IN VIVO STUDY; MOLECULARLY TARGETED THERAPY; MOUSE; MOUSE MODEL; NONHUMAN; PRIORITY JOURNAL; SURVIVAL RATE; TUMOR RECURRENCE; TUMOR REGRESSION; ANIMAL; ANTAGONISTS AND INHIBITORS; BRAIN NEOPLASMS; C57BL MOUSE; DRUG RESISTANCE; GENETICS; HUMAN; METABOLISM; PHOSPHORYLATION; PROTEIN PROCESSING; TRANSGENIC MOUSE; TUMOR CELL CULTURE;

ANIMALS; BRAIN NEOPLASMS; CYCLIN-DEPENDENT KINASE INHIBITOR P16; DOXYCYCLINE; DRUG RESISTANCE, NEOPLASM; ERLOTINIB HYDROCHLORIDE; GLIOMA; HUMANS; IMIDAZOLES; MICE, INBRED C57BL; MICE, TRANSGENIC; MOLECULAR TARGETED THERAPY; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PTEN PHOSPHOHYDROLASE; PYRAZOLES; PYRIDINES; QUINAZOLINES; QUINOLINES; RECEPTOR, EPIDERMAL GROWTH FACTOR; TUMOR CELLS, CULTURED;

EID: 84943194890     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-14-3122     Document Type: Article

References (44)

1. Louis DN, Ohgaki H, Wiestler O.D., Cavenee WK, Burger PC, Jouvet A, et al The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol 2007; 114: 97-109.
2. Wen PY, Kesari S. Malignant gliomas in adults. N Engl J Med 2008; 359: 492-507.
3. 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.
4. Brennan CW, Verhaak RG, McKenna A, Campos B., Noushmehr H, Salama SR, et al The somatic genomic landscape of glioblastoma. Cell 2013; 155: 462-77.
5. 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.
6. Phillips HS, Kharbanda S, Chen R., Forrest WF, Soriano RH, Wu TD, et al Molecular subclasses of high-grade glioma predict prognosis, delineate a pattern of disease progression, and resemble stages in neurogenesis. Cancer Cell 2006; 9: 157-73.
7. TCGA. Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature 2008; 455: 1061-8.
8. Verhaak RG, Hoadley KA, Purdom E, Wang V., Qi Y, Wilkerson MD, et al Integrated genomic analysis identifies clinically relevant subtypes of glio-blastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell 2010; 17: 98-110.
9. 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.
10. Fan QW, Cheng CK, Gustafson W.C., Charron E., Zipper P, Wong RA, et al EGFR phosphorylates tumor-derived EGFRvIII driving STAT3/5 and progression in glioblastoma. Cancer Cell 2013; 24: 438-49.
11. Sugawa N, Ekstrand AJ, James C.D., Collins VP. Identical splicing of aberrant epidermal growth factor receptor transcripts from amplified rearranged genes in human glioblastomas. Proc Natl Acad Sci U S A 1990; 87: 8602-6.
12. Zadeh G, Bhat KP, Aldape K. EGFR and EGFRvIII in glioblastoma: partners in crime. Cancer Cell 2013; 24: 403-4.
13. Nathanson DA, Gini B, Mottahedeh J., Visnyei K, Koga T, Gomez G., et al. Targeted therapy resistance mediated by dynamic regulation of extrachromosomal mutant EGFR DNA. Science 2014; 343: 72-6.
14. Okada Y, Hurwitz EE, Esposito J.M., Brower MA, Nutt CL, Louis DN. Selection pressures of TP53 mutation and microenvironmental location influence epidermal growth factor receptor gene amplification in human glioblastomas. Cancer Res 2003; 63: 413-6.
15. Snuderl M, Fazlollahi L, Le L.P., Nitta M., Zhelyazkova BH, Davidson CJ, et al. Mosaic amplification of multiple receptor tyrosine kinase genes in glio-blastoma. Cancer Cell 2011; 20: 810-7.
16. Szerlip NJ, Pedraza A, Chakravarty D., Azim M, McGuire J, Fang Y., et al. Intratumoral heterogeneity of receptor tyrosine kinases EGFR and PDGFRA amplification in glioblastoma defines subpopulations with distinct growth factor response. Proc Natl Acad Sci U S A 2012; 109: 3041-6.
17. 1 cell-cycle arrest pathways to induce glioma-like lesions in mice. Genes Dev 1998; 12: 3675-85.
18. Inda MM, Bonavia R, Mukasa A., Narita Y, Sah DW, Vandenberg S, et al Tumor heterogeneity is an active process maintained by a mutant EGFR-induced cytokine circuit in glioblastoma. Genes Dev 2010; 24: 1731-45.
19. Mukasa A, Wykosky J, Ligon K.L., Chin L., Cavenee WK, Furnari F. Mutant EGFR is required for maintenance of glioma growth in vivo, and its ablation leads to escape from receptor dependence. Proc Natl Acad Sci U S A 2010; 107: 2616-21.
20. Zhu H, Acquaviva J, Ramachandran P., Boskovitz A, Woolfenden S, Pfannl R., et al. Oncogenic EGFR signaling cooperates with loss of tumor suppressor gene functions in gliomagenesis. Proc Natl Acad Sci U S A 2009; 106:2712-6.
21. Lynch TJ, Bell DW, Sordella R, Gurubhagavatula S., Okimoto RA, Brannigan BW, et al. Activating mutations in the epidermal growth factor receptor underlying responsiveness of non-small-cell lung cancer to gefitinib. N Engl J Med 2004; 350: 2129-39.
22. Paez JG, Janne PA, Lee J.C., Tracy S., Greulich H, Gabriel S, et al EGFR mutations in lung cancer: correlation with clinical response to gefitinib therapy. Science 2004; 304: 1497-500.
23. Pao W, Miller V, Zakowski M., Doherty J, Politi K, Sarkaria I., et al. EGF receptor genemutations arecommoninlungcancersfrom "never smokers" and are associated with sensitivity of tumors to gefitinib and erlotinib. Proc Natl Acad Sci U S A 2004; 101: 13306-11.
24. Brandes AA, Franceschi E, Tosoni A., Hegi ME, Stupp R. Epidermal growth factor receptor inhibitors in neuro-oncology: hopes and disappointments. Clin Cancer Res 2008; 14: 957-60.
25. Wen PY, Chang SM, Lamborn K.R., Kuhn JG, Norden AD, Cloughesy TF, 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: 567-78.
26. Yung WK, Vredenburgh JJ, Cloughesy T.F., Nghiemphu P., Klencke B, Gilbert MR, et al Safety and efficacy of erlotinib in first-relapse glioblastoma: a phase II open-label study. Neuro Oncol 2010; 12: 1061-70.
27. Aguirre AJ, Bardeesy N, Sinha M., Lopez L, Tuveson DA, Horner J, et al Activated Kras and Ink4a/Arf deficiency cooperate to produce metastatic pancreatic ductal adenocarcinoma. Genes Dev 2003; 17: 3112-26.
28. Zheng H, Ying H, Yan H., Kimmelman AC, Hiller DJ, Chen AJ, et al p53 and Pten control neural and glioma stem/progenitor cell renewal and differentiation. Nature 2008; 455: 1129-33.
29. 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.
30. Imayoshi I, Sakamoto M, Ohtsuka T., Takao K, Miyakawa T, Yamaguchi M., et al. Roles of continuous neurogenesis in the structural and functional integrity of the adult forebrain. Nat Neurosci 2008; 11: 1153-61.
31. Lin W, Kemper A, McCarthy K.D., Pytel P., Wang JP, Campbell IL, et al. Interferon-gamma induced medulloblastoma in the developing cerebellum. J Neurosci 2004; 24: 10074-83.
32. Zheng H, Ying H, Wiedemeyer R., Yan H, Quayle SN, Ivanova E.V., et al. PLAGL2 regulates Wnt signaling to impede differentiation in neural stem cells and gliomas. Cancer Cell 2010; 17: 497-509.
33. Zheng H, Ying H, Yan H., Kimmelman AC, Hiller DJ, Chen AJ, et al Pten and p53 converge on c-Myc to control differentiation, self-renewal, and transformation of normal and neoplastic stem cells in glioblastoma. Cold Spring Harb Symp Quant Biol 2008; 73: 427-37.
34. Furnari FB, Fenton T, Bachoo R.M., Mukasa A., Stommel JM, Stegh A, et al. Malignant astrocytic glioma: genetics, biology, and paths to treatment. Genes Dev 2007; 21: 2683-710.
35. Sharma SV, Bell DW, Settleman J, Haber DA Epidermal growth factor receptor mutations in lung cancer. Nat Rev Cancer 2007; 7: 169-81.
36. Weinstein IB. Cancer. Addiction to oncogenes-the Achilles heal of cancer. Science 2002; 297: 63-4.
37. Engelman JA, Zejnullahu K, Mitsudomi T., Song Y, Hyland C, Park J.O., et al. MET amplification leads to gefitinib resistance in lung cancer by activating ERBB3 signaling. Science 2007; 316: 1039-43.
38. Turke AB, Zejnullahu K, Wu Y.L., Song Y., Dias-Santagata D, Lifshits E, et al Preexistence and clonal selection of MET amplification in EGFR mutant NSCLC. Cancer Cell 2010; 17: 77-88.
39. Dunn GP, Rinne ML, Wykosky J, Genovese G., Quayle SN, Dunn IF, et al. Emerging insights into the molecular and cellular basis of glioblastoma. Genes Dev 2012; 26: 756-84.
40. Barkovich KJ, Hariono S, Garske A.L., Zhang J., Blair JA, Fan QW, et al. Kinetics of inhibitor cycling underlie therapeutic disparities between EGFR-driven lung and brain cancers. Cancer Discov 2012; 2: 450-7.
41. Hegi ME, Diserens AC, Bady P, Kamoshima Y., Kouwenhoven MC, Delorenzi M, et al. Pathway analysis of glioblastoma tissue after preoperative treatment with the EGFR tyrosine kinase inhibitor gefitinib-a phase II trial. Mol Cancer Ther 2011; 10: 1102-12.
42. Vivanco I, Robins HI, Rohle D, Campos C., Grommes C, Nghiemphu PL, et al Differential sensitivity of glioma-versus lung cancer-specific EGFR mutations to EGFR kinase inhibitors. Cancer Discov 2012; 2: 458-71.
43. 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.
44. Weihua Z, Tsan R, Huang W.C., Wu Q., Chiu CH, Fidler IJ, et al. Survival of cancer cells is maintained by EGFR independent of its kinase activity. Cancer Cell 2008; 13: 385-93.