Acquired MET expression confers resistance to EGFR inhibition in a mouse model of glioblastoma multiforme

Oncogene

Volumn 31, Issue 25, 2012, Pages 3039-3050

  Jun, H J ^a   Acquaviva, J ^a   Chi, D ^a   Lessard, J ^a   Zhu, H ^a   Woolfenden, S ^a   Bronson, R T ^b   Pfannl, R ^c   White, F ^d,e   Housman, D E ^d   Iyer, L ^c   Whittaker, C A ^d   Boskovitz, A ^c   Raval, A ^c   Charest, A ^a,c,d  

^a TUFTS MEDICAL CENTER   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^e Massachusetts Institute of Technology Cambridge   (United States)

Author keywords

c MET; EGFR; genetically engineered mouse model; glioblastoma; PTEN

Indexed keywords

CASPASE 3; CRE RECOMBINASE; CYCLIN DEPENDENT KINASE INHIBITOR 2A; EPIDERMAL GROWTH FACTOR RECEPTOR KINASE; KI 67 ANTIGEN; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; POLY(ADENOSINE DIPHOSPHATE RIBOSE); PROTEIN KINASE B; SCATTER FACTOR RECEPTOR; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CARCINOGENESIS; CELL CYCLE ARREST; CONTROLLED STUDY; CYTOSTASIS; ENZYME ACTIVITY; ENZYME INHIBITION; GENE DELETION; GENE EXPRESSION; GENE OVEREXPRESSION; GENETIC ENGINEERING; GLIOBLASTOMA; HISTOPATHOLOGY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; TRANSCRIPTION INITIATION; TUMOR CELL;

ANIMALS; DISEASE MODELS, ANIMAL; GENES, TUMOR SUPPRESSOR; GLIOBLASTOMA; HUMANS; MICE; MICE, TRANSGENIC; PROTO-ONCOGENE PROTEINS C-MET; RECEPTOR, EPIDERMAL GROWTH FACTOR;

MUS;

EID: 84862657056     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2011.474     Document Type: Article

References (55)

1. Andl CD, Mizushima T, Nakagawa H, Oyama K, Harada H, Chruma K et al. (2003). Epidermal growth factor receptor mediates increased cell proliferation, migration, and aggregation in esophageal keratinocytes in vitro and in vivo. J Biol Chem 278: 1824-1830.
2. Brennan C, Momota H, Hambardzumyan D, Ozawa T, Tandon A, Pedraza A et al. (2009). Glioblastoma subclasses can be defined by activity among signal transduction pathways and associated genomic alterations. PLoS One 4: e7752.
3. Busse D, Doughty RS, Ramsey TT, Russell WE, Price JO, Flanagan WM et al. (2000). Reversible G(1) arrest induced by inhibition of the epidermal growth factor receptor tyrosine kinase requires up-regulation of p27(KIP1) independent of MAPK activity. J Biol Chem 275: 6987-6995.
4. Cheng J, Huang H, Zhang ZT, Shapiro E, Pellicer A, Sun TT et al. (2002). Overexpression of epidermal growth factor receptor in urothelium elicits urothelial hyperplasia and promotes bladder tumor growth. Cancer Res 62: 4157-4163.
5. Ciardiello F, McGeady ML, Kim N, Basolo F, Hynes N, Langton BC et al. (1990). Transforming growth factor-alpha expression is enhanced in human mammary epithelial cells transformed by an activated c-Ha-ras protooncogene but not by the c-neu protooncogene, and overexpression of the transforming growth factor-alpha complementary DNA leads to transformation. Cell Growth Differ 1: 407-420.
6. Coleman JE, Huentelman MJ, Kasparov S, Metcalfe BL, Paton JF, Katovich MJ et al. (2003). Efficient large-scale production and concentration of HIV-1-based lentiviral vectors for use in vivo. Physiol Genomics 12: 221-228.
7. Di Fiore PP, Pierce JH, Fleming TP, Hazan R, Ullrich A, King CR et al. (1987). Overexpression of the human EGF receptor confers an EGF-dependent transformed phenotype to NIH 3T3 cells. Cell 51: 1063-1070.
8. Di Marco E, Pierce JH, Aaronson SA, Di Fiore PP. (1990). Mechanisms by which EGF receptor and TGF alpha contribute to malignant transformation. Nat Immun Cell Growth Regul 9: 209-221.
9. Di Marco E, Pierce JH, Fleming TP, Kraus MH, Molloy CJ, Aaronson SA et al. (1989). Autocrine interaction between TGF alpha and the EGF-receptor: quantitative requirements for induction of the malignant phenotype. Oncogene 4: 831-838.
10. Ding H, Shannon P, Lau N, Wu X, Roncari L, Baldwin RL et al. (2003). Oligodendrogliomas result from the expression of an activated mutant epidermal growth factor receptor in a RAS transgenic mouse astrocytoma model. Cancer Res 63: 1106-1113.
11. Ekstrand AJ, James CD, Cavenee WK, Seliger B, Pettersson RF, Collins VP. (1991). Genes for epidermal growth factor receptor, transforming growth factor alpha, and epidermal growth factor and their expression in human gliomas in vivo. Cancer Res 51: 2164-2172.
12. Engelman JA, Settleman J. (2008). Acquired resistance to tyrosine kinase inhibitors during cancer therapy. Curr Opin Genet Dev 18: 73-79.
13. Engelman JA, Zejnullahu K, Mitsudomi T, Song Y, Hyland C, Park JO et al. (2007). MET amplification leads to gefitinib resistance in lung cancer by activating ERBB3 signaling. Science 316: 1039-1043.
14. Fan QW, Cheng CK, Nicolaides TP, Hackett CS, Knight ZA, Shokat KM et al. (2007). A dual phosphoinositide-3-kinase alpha/mTOR inhibitor cooperates with blockade of epidermal growth factor receptor in PTEN-mutant glioma. Cancer Res 67: 7960-7965.
15. Follenzi A, Ailles LE, Bakovic S, Geuna M, Naldini L. (2000). Gene transfer by lentiviral vectors is limited by nuclear translocation and rescued by HIV-1 pol sequences. Nat Genet 25: 217-222.
16. Friedman HS, Bigner DD. (2005). Glioblastoma multiforme and the epidermal growth factor receptor. N Engl J Med 353: 1997-1999.
17. Guillamo JS, de Bouard S, Valable S, Marteau L, Leuraud P, Marie Y et al. (2009). Molecular mechanisms underlying effects of epidermal growth factor receptor inhibition on invasion, proliferation, and angiogenesis in experimental glioma. Clin Cancer Res 15: 3697-3704.
18. Huang PH, Cavenee WK, Furnari FB, White FM. (2007). Uncovering therapeutic targets for glioblastoma: a systems biology approach. Cell Cycle 6: 2750-2754.
19. Huang TT, Sarkaria SM, Cloughesy TF, Mischel PS. (2009). Targeted therapy for malignant glioma patients: lessons learned and the road ahead. Neurotherapeutics 6: 500-512.
20. Lesche R, Groszer M, Gao J, Wang Y, Messing A, Sun H et al. (2002). Cre/loxP-mediated inactivation of the murine Pten tumor suppressor gene. Genesis 32: 148-149.
21. Liang H, O'Reilly S, Liu Y, Abounader R, Laterra J, Maher VM et al. (2004). Sp1 regulates expression of MET, and ribozyme-induced down-regulation of MET in fibrosarcoma-derived human cells reduces or eliminates their tumorigenicity. Int J Oncol 24: 1057-1067.
22. Ling YH, Li T, Yuan Z, Haigentz Jr M, Weber TK, Perez-Soler R. (2007). Erlotinib, an effective epidermal growth factor receptor tyrosine kinase inhibitor, induces p27KIP1 up-regulation and nuclear translocation in association with cell growth inhibition and G1/S phase arrest in human non-small-cell lung cancer cell lines. Mol Pharmacol 72: 248-258.
23. Maruno M, Kovach JS, Kelly PJ, Yanagihara T. (1991). Transforming growth factor-alpha, epidermal growth factor receptor, and proliferating potential in benign and malignant gliomas. J Neurosurg 75: 97-102.
24. McLendon R, Friedman A, Bigner D, Van Meir EG, Brat DJ, Mastrogianakis M et al. (2008). Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature 455: 1061-1068.
25. Mellinghoff IK, Cloughesy TF, Mischel PS. (2007). PTEN-mediated resistance to epidermal growth factor receptor kinase inhibitors. Clin Cancer Res 13: 378-381.
26. Mellinghoff IK, Wang MY, Vivanco I, Haas-Kogan DA, Zhu S, Dia EQ et al. (2005). Molecular determinants of the response of glioblastomas to EGFR kinase inhibitors. N Engl J Med 353: 2012-2024.
27. Mishima K, Higashiyama S, Asai A, Yamaoka K, Nagashima Y, Taniguchi N et al. (1998). Heparin-binding epidermal growth factor-like growth factor stimulates mitogenic signaling and is highly expressed in human malignant gliomas. Acta Neuropathol 96: 322-328.
28. Mueller KL, Hunter LA, Ethier SP, Boerner JL. (2008). Met and c-Src cooperate to compensate for loss of epidermal growth factor receptor kinase activity in breast cancer cells. Cancer Res 68: 3314-3322.
29. Mueller KL, Yang ZQ, Haddad R, Ethier SP, Boerner JL. (2010). EGFR/Met association regulates EGFR TKI resistance in breast cancer. J Mol Signal 5: 8.
30. Peng D, Fan Z, Lu Y, DeBlasio T, Scher H, Mendelsohn J. (1996). Anti-epidermal growth factor receptor monoclonal antibody 225 up-regulates p27KIP1 and induces G1 arrest in prostatic cancer cell line DU145. Cancer Res 56: 3666-3669.
31. Phillips HS, Kharbanda S, Chen R, Forrest WF, Soriano RH, Wu TD et al. (2006). Molecular subclasses of high-grade glioma predict prognosis, delineate a pattern of disease progression, and resemble stages in neurogenesis. Cancer Cell 9: 157-173.
32. Ramnarain DB, Park S, Lee DY, Hatanpaa KJ, Scoggin SO, Otu H et al. (2006). Differential gene expression analysis reveals generation of an autocrine loop by a mutant epidermal growth factor receptor in glioma cells. Cancer Res 66: 867-874.
33. Rosenthal A, Lindquist PB, Bringman TS, Goeddel DV, Derynck R. (1986). Expression in rat fibroblasts of a human transforming growth factor-alpha cDNA results in transformation. Cell 46: 301-309.
34. Samuels V, Barrett JM, Bockman S, Pantazis CG, Allen Jr MB. (1989). Immunocytochemical study of transforming growth factor expression in benign and malignant gliomas. Am J Pathol 134: 894-902.
35. Sarkaria JN, Yang L, Grogan PT, Kitange GJ, Carlson BL, Schroeder MA et al. (2007). Identification of molecular characteristics correlated with glioblastoma sensitivity to EGFR kinase inhibition through use of an intracranial xenograft test panel. Mol Cancer Ther 6: 1167-1174.
36. Schlegel U, Moots PL, Rosenblum MK, Thaler HT, Furneaux HM. (1990). Expression of transforming growth factor alpha in human gliomas. Oncogene 5: 1839-1842.
37. Seol DW, Zarnegar R. (1998). Structural and functional characterization of the mouse c-met proto-oncogene (hepatocyte growth factor receptor) promoter. Biochim Biophys Acta 1395: 252-258.
38. Serrano M, Lee H, Chin L, Cordon-Cardo C, Beach D, DePinho RA. (1996). Role of the INK4a locus in tumor suppression and cell mortality. Cell 85: 27-37.
39. Shankar V, Ciardiello F, Kim N, Derynck R, Liscia DS, Merlo G et al. (1989). Transformation of an established mouse mammary epithelial cell line following transfection with a human transforming growth factor alpha cDNA. Mol Carcinogen 2: 1-11.
40. Shimshek DR, Kim J, Hubner MR, Spergel DJ, Buchholz F, Casanova E et al. (2002). Codon-improved Cre recombinase (iCre) expression in the mouse. Genesis 32: 19-26.
41. Shin KJ, Wall EA, Zavzavadjian JR, Santat LA, Liu J, Hwang JI et al. (2006). A single lentiviral vector platform for microRNA-based conditional RNA interference and coordinated transgene expression. Proc Natl Acad Sci USA 103: 13759-13764.
42. Stommel JM, Kimmelman AC, Ying H, Nabioullin R, Ponugoti AH, Wiedemeyer R et al. (2007). Coactivation of receptor tyrosine kinases affects the response of tumor cells to targeted therapies. Science 318: 287-290.
43. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA et al. (2005). Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci USA 102: 15545-15550.
44. Suzuki R, Shimodaira H. (2006). Pvclust: an R package for assessing the uncertainty in hierarchical clustering. Bioinformatics 22: 1540-1542.
45. Tang P, Steck PA, Yung WK. (1997). The autocrine loop of TGF-alpha/EGFR and brain tumors. J Neurooncol 35: 303-314.
46. Turke AB, Zejnullahu K, Wu YL, Song Y, Dias-Santagata D, Lifshits E et al. (2010). Preexistence and clonal selection of MET amplification in EGFR mutant NSCLC. Cancer Cell 17: 77-88.
47. van den Bent MJ, Brandes AA, Rampling R, Kouwenhoven MC, Kros JM, Carpentier AF et al. (2009). Randomized phase II trial of erlotinib versus temozolomide or carmustine in recurrent glioblastoma: EORTC brain tumor group study 26034. J Clin Oncol 27: 1268-1274.
48. van der Valk P, Lindeman J, Kamphorst W. (1997). Growth factor profiles of human gliomas. Do non-tumour cells contribute to tumour growth in glioma? Ann Oncol 8: 1023-1029.
49. Verhaak RG, Hoadley KA, Purdom E, Wang V, Qi Y, Wilkerson MD et al. (2010). Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell 17: 98-110.
50. Watanabe S, Lazar E, Sporn MB. (1987). Transformation of normal rat kidney (NRK) cells by an infectious retrovirus carrying a synthetic rat type alpha transforming growth factor gene. Proc Natl Acad Sci USA 84: 1258-1262.
51. Woolfenden S, Zhu H, Charest A. (2009). A Cre/LoxP conditional luciferase reporter transgenic mouse for bioluminescence monitoring of tumorigenesis. Genesis 47: 659-666.
52. Yung WK, Zhang X, Steck PA, Hung MC. (1990). Differential amplification of the TGF-alpha gene in human gliomas. Cancer Commun 2: 201-205.
53. Zennou V, Serguera C, Sarkis C, Colin P, Perret E, Mallet J et al. (2001). The HIV-1 DNA flap stimulates HIV vector-mediated cell transduction in the brain. Nat Biotechnol 19: 446-450.
54. Zhu H, Acquaviva J, Ramachandran P, Boskovitz A, Woolfenden S, Pfannl R et al. (2009). Oncogenic EGFR signaling cooperates with loss of tumor suppressor gene functions in gliomagenesis. Proc Natl Acad Sci USA 106: 2712-2716.
55. Zhu X, Santat LA, Chang MS, Liu J, Zavzavadjian JR, Wall EA et al. (2007). A versatile approach to multiple gene RNA interference using microRNA-based short hairpin RNAs. BMC Mol Biol 8: 98.