Access to the nucleus and functional association with c-Myc is required for the full oncogenic potential of ΔEGFR/EGFRvIII

Journal of Biological Chemistry

Volumn 288, Issue 5, 2013, Pages 3428-3438

  Gururaj, Anupama E ^a   Gibson, Laura ^a   Panchabhai, Sonali ^a   Bai, Ming Hui ^a   Manyam, Ganiraju ^a   Lu, Yue ^a   Latha, Khatri ^a   Rojas, Marta L ^a,b   Hwang, Yeohyeon ^a   Liang, Shoudan ^a   Bogler, Oliver ^a,b  

^a UNIVERSITY OF TEXAS   (United States)

^b UNIVERSITY OF TEXAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOINFORMATIC ANALYSIS; CHROMATIN IMMUNOPRECIPITATION; COLONY FORMATION; DATA SETS; FUNCTIONAL ASSOCIATIONS; GLIOBLASTOMAS; IN-VIVO; MASSIVELY PARALLEL SEQUENCING; NUCLEAR ACCUMULATION; ONCOGENIC POTENTIAL; TARGET GENES; THERAPEUTIC INTERVENTION; TRANSCRIPTIONAL REGULATION; TUMORIGENICITY;

BIOINFORMATICS; CELL MEMBRANES; GENE EXPRESSION; GENE THERAPY;

CHROMOSOMES;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BINDING SITE; BIOINFORMATICS; CARCINOGENESIS; CARCINOGENICITY; CELL NUCLEUS; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; COLONY FORMATION; CONTROLLED STUDY; E BOX ELEMENT; EGFRVIII GENE; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE MAPPING; GLIOMA CELL; MOUSE; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; ONCOGENE; ONCOGENE C MYC; PRIORITY JOURNAL; PROMOTER REGION; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; CELL NUCLEUS; CELL TRANSFORMATION, NEOPLASTIC; CHROMATIN IMMUNOPRECIPITATION; E-BOX ELEMENTS; GENOME, HUMAN; GLIOMA; HUMANS; MICE; MICE, NUDE; MUTANT PROTEINS; MUTATION; NUCLEAR EXPORT SIGNALS; NUCLEAR LOCALIZATION SIGNALS; PHENOTYPE; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN TRANSPORT; PROTO-ONCOGENE PROTEINS C-MYC; RECEPTOR, EPIDERMAL GROWTH FACTOR; TRANSCRIPTION FACTORS;

EID: 84873316091     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.399352     Document Type: Article

References (38)

1. Nishikawa, R., Ji, X. D., Harmon, R. C., Lazar, C. S., Gill, G. N., Cavenee, W. K., and Huang, H. J. (1994) Amutant epidermal growth factor receptor common in human glioma confers enhanced tumorigenicity. Proc. Natl. Acad. Sci. U. S. A. 91, 7727-7731
2. Furnari, F. B., Fenton, T., Bachoo, R. M., Mukasa, A., Stommel, J. M., Stegh, A., Hahn, W. C., Ligon, K. L., Louis, D. N., Brennan, C., Chin, L., De Pinho, R. A., and Cavenee, W. K. (2007) Malignant astrocytic glioma. Genetics, biology, and paths to treatment. Genes Dev. 21, 2683-2710
3. Hanada, N., Lo, H. W., Day, C. P., Pan, Y., Nakajima, Y., and Hung, M. C. (2006) Co-regulation of B-Myb expression by E2F1 and EGF receptor. Mol. Carcinog. 45, 10-17
4. Hung, L. Y., Tseng, J. T., Lee, Y. C., Xia, W., Wang, Y. N., Wu, M. L., Chuang, Y. H., Lai, C. H., and Chang, W. C. (2008) Nuclear epidermal growth factor receptor (EGFR) interacts with signal transducer and activator of transcription 5 (STAT5) in activating Aurora-A gene expression. Nucleic Acids Res. 36, 4337-4351
5. Huo, L., Wang, Y. N., Xia, W., Hsu, S. C., Lai, C. C., Li, L. Y., Chang, W. C., Wang, Y., Hsu, M. C., Yu, Y. L., Huang, T. H., Ding, Q., Chen, C. H., Tsai, C. H., and Hung, M. C. (2010) RNA helicase A is a DNA-binding partner for EGFR-mediated transcriptional activation in the nucleus. Proc. Natl. Acad. Sci. U. S. A. 107, 16125-16130
6. Lin, S. Y., Makino, K., Xia, W., Matin, A., Wen, Y., Kwong, K. Y., Bourguignon, L., and Hung, M. C. (2001) Nuclear localization of EGF receptor and its potential new role as a transcription factor. Nat. Cell Biol. 3, 802-808
7. Lo, H. W., Hsu, S. C., Ali-Seyed, M., Gunduz, M., Xia, W., Wei, Y., Bartholomeusz, G., Shih, J. Y., and Hung, M. C. (2005) Nuclear interaction of EGFR and STAT3 in the activation of the iNOS/NO pathway. Cancer Cell 7, 575-589
8. De La Iglesia, N., Konopka, G., Puram, S. V., Chan, J. A., Bachoo, R. M., You, M. J., Levy, D. E., Depinho, R. A., and Bonni, A. (2008) Identification of a PTEN-regulated STAT3 brain tumor suppressor pathway. Genes Dev. 22, 449-462
9. Lo, H. W., Cao, X., Zhu, H., and Ali-Osman, F. (2010) Cyclooxygenase-2 is a novel transcriptional target of the nuclear EGFR-STAT3 and EGFRvIII-STAT3 signaling axes. Mol. Cancer Res. 8, 232-245
10. Latha, K., Li, M., Chumbalkar, V., Gururaj, A., Hwang, Y., Dakeng, S., Sawaya, R., Aldape, K., Cavenee, W. K., Bogler, O., and Furnari, F. B. (2013) Nuclear EGFRvIII-STAT5b complex contributes to glioblastoma cell survival by direct activation of the Bcl-XL promoter. Int. J. Cancer 132, 509-520
11. Wang, S. C., and Hung, M. C. (2009) Nuclear translocation of the epidermal growth factor receptor family membrane tyrosine kinase receptors. Clin. Cancer Res. 15, 6484-6489
12. Lo, H. W., Xia, W., Wei, Y., Ali-Seyed, M., Huang, S. F., and Hung, M. C. (2005) Novel prognostic value of nuclear epidermal growth factor receptor in breast cancer. Cancer Res. 65, 338-348
13. Psyrri, A., Egleston, B., Weinberger, P., Yu, Z., Kowalski, D., Sasaki, C., Haffty, B., Rimm, D., and Burtness, B. (2008) Correlates and determinants of nuclear epidermal growth factor receptor content in an oropharyngeal cancer tissue microarray. Cancer Epidemiol. Biomarkers Prev. 17, 1486-1492
14. Psyrri, A., Yu, Z., Weinberger, P. M., Sasaki, C., Haffty, B., Camp, R., Rimm, D., and Burtness, B. A. (2005) Quantitative determination of nuclear and cytoplasmic epidermal growth factor receptor expression in oropharyngeal squamous cell cancer by using automated quantitative analysis. Clin. Cancer Res. 11, 5856-5862
15. Kim, J., Jahng, W. J., Di Vizio, D., Lee, J. S., Jhaveri, R., Rubin, M. A., Shisheva, A., and Freeman, M. R. (2007) The phosphoinositide kinase PIKfyve mediates epidermal growth factor receptor trafficking to the nucleus. Cancer Res. 67, 9229-9237
16. Xia, W., Wei, Y., Du, Y., Liu, J., Chang, B., Yu, Y. L., Huo, L. F., Miller, S., and Hung, M. C. (2009) Nuclear expression of epidermal growth factor receptor is a novel prognostic value in patients with ovarian cancer. Mol. Carcinog. 48, 610-617
17. Pelengaris, S., Khan, M., and Evan, G. (2002) c-MYC. More than just a matter of life and death. Nat. Rev. Cancer 2, 764-776
18. Soucek, L., and Evan, G. I. (2010) The ups and downs of Myc biology. Curr. Opin. Genet. Dev. 20, 91-95
19. Albihn, A., Johnsen, J. I., and Henriksson, M. A. (2010) MYC in oncogenesis and as a target for cancer therapies. Adv. Cancer Res. 107, 163-224
20. Shingu, T., Chumbalkar, V. C, Gwak, H. S., Fujiwara, K., Kondo, S., Farrell, N. P., and Bogler, O. (2010) The polynuclear platinum BBR3610 induces G2/M arrest and autophagy early and apoptosis late in glioma cells. Neuro. Oncol. 12, 1269-1277
21. Chen, B., Borinstein, S. C., Gillis, J., Sykes, V. W., and Bogler, O. (2000) The glioma-associated protein SETA interacts with AIP1/Alix and ALG-2 and modulates apoptosis in astrocytes. J. Biol. Chem. 275, 19275-19281
22. Hsu, S. C, and Hung, M. C (2007) Characterization of a novel tripartite nuclear localization sequence in the EGFR family. J. Biol. Chem. 282, 10432-10440
23. Hwang, Y., Chumbalkar, V., Latha, K., and Bogler, O. (2011) Forced dimerization increases the activity of AEGFR/EGFRvIII and enhances its oncogenicity. Mol. Cancer Res. 9, 1199-1208
24. Kajiwara, Y., Panchabhai, S., and Levin, V. A. (2008) A new preclinical 3-dimensional agarose colony formation assay. Technol. Cancer Res. Treat. 7, 329-334
25. Gururaj, A. E., Singh, R. R., Rayala, S. K., Holm, C, Den Hollander, P., Zhang, H, Balasenthil, S., Talukder, A. H., Landberg, G., and Kumar, R. (2006) MTA1, a transcriptional activator of breast cancer amplified sequence 3. Proc. Natl. Acad. Sci. U. S. A. 103, 6670-6675
26. Zhang, Y., Liu, T., Meyer, C. A., Eeckhoute, J., Johnson, D. S., Bernstein, B. E., Nusbaum, C, Myers, R. M., Brown, M., Li, W., and Liu, X. S. (2008) Model-based analysis of ChIP-Seq (MACS). Genome Biol. 9, R137
27. McLean, C. Y., Bristor, D., Hiller, M., Clarke, S. L., Schaar, B. T., Lowe, C. B., Wenger, A. M., and Bejerano, G. (2010) GREAT improves functional interpretation of cis-regulatory regions. Nat. Biotechnol. 28, 495-501
28. Lo, H. W., Ali-Seyed, M., Wu, Y., Bartholomeusz, G., Hsu, S. C, and Hung, M. C. (2006) Nuclear-cytoplasmic transport of EGFR involves receptor endocytosis, importin β1 and CRM1. J. Cell Biochem. 98, 1570-1583
29. La Cour, T., Kiemer, L., Mølgaard, A., Gupta, R., Skriver, K., and Brunak, S. (2004) Analysis and prediction of leucine-rich nuclear export signals. Protein Eng. Des. Sel. 17, 527-536
30. Huang, H. S., Nagane, M., Klingbeil, C. K., Lin, H., Nishikawa, R., Ji, X. D., Huang, C. M., Gill, G. N., Wiley, H. S., and Cavenee, W. K. (1997) The enhanced tumorigenic activity of a mutant epidermal growth factor receptor common in human cancers is mediated by threshold levels of constitutive tyrosine phosphorylation and unattenuated signaling. J. Biol. Chem. 272, 2927-2935
31. Red Brewer, M., Choi, S. H., Alvarado, D., Moravcevic, K., Pozzi, A., Lemmon, M. A., and Carpenter, G. (2009) The juxtamembrane region of the EGF receptor functions as an activation domain. Mol. Cell 34, 641-651
32. Jaganathan, S., Yue, P., Paladino, D. C., Bogdanovic, J., Huo, Q., and Turkson, J. (2011) A functional nuclear epidermal growth factor receptor, SRC and Stat3 heteromeric complex in pancreatic cancer cells. PloS ONE 6, e19605
33. Bailey, T. L., and Gribskov, M. (1998) Combining evidence using p-values. Application to sequence homology searches. Bioinformatics 14, 48-54
34. Tijssen, M. R., Cvejic, A., Joshi, A., Hannah, R. L., Ferreira, R., Forrai, A., Bellissimo, D. C., Oram, S. H., Smethurst, P. A., Wilson, N. K., Wang, X., Ottersbach, K., Stemple, D. L., Green, A. R., Ouwehand, W. H., and Göttgens, B. (2011) Genome-wide analysis of simultaneous GATA1/2, RUNX1, FLI1, and SCL binding in megakaryocytes identifies hematopoietic regulators. Dev. Cell 20, 597-609
35. Ma, Z., Swigut, T., Valouev, A., Rada-Iglesias, A., and Wysocka, J. (2011) Sequence-specific regulator Prdm14 safeguards mouse ESCs from entering extraembryonic endoderm fates. Nat. Struct. Mol. Biol. 18, 120-127
36. Kim, S. W., Yoon, S. J., Chuong, E., Oyolu, C., Wills, A. E., Gupta, R., and Baker, J. (2011) Chromatin and transcriptional signatures for Nodal signaling during endoderm formation in hESCs. Dev. Biol. 357, 492-504
37. Tang, Q., Chen, Y., Meyer, C., Geistlinger, T., Lupien, M., Wang, Q., Liu, T., Zhang, Y., Brown, M., and Liu, X. S. (2011) A comprehensive view of nuclear receptor cancer cistromes. Cancer Res. 71, 6940-6947
38. Jensen, N. A., Pedersen, K. M., Lihme, F., Rask, L., Nielsen, J. V., Rasmussen, T. E., and Mitchelmore, C. (2003) Astroglial c-Myc overexpression predisposes mice to primary malignant gliomas. J. Biol. Chem. 278, 8300-8308