EphA2 expression is a key driver of migration and invasion and a poor prognostic marker in colorectal cancer

Clinical Cancer Research

Volumn 22, Issue 1, 2016, Pages 230-242

  Dunne, Philip D ^a   Dasgupta, Sonali ^a   Blayney, Jaine K ^a   McArt, Darragh G ^a   Redmond, Keara L ^a   Weir, Jessica Anne ^a   Bradley, Conor A ^a   Sasazuki, Takehiko ^b   Shirasawa, Senji ^c   Wang, Tingting ^d   Srivastava, Supriya ^d   Ong, Chee Wee ^a   Arthur, Ken ^a   Salto Tellez, Manuel ^a   Wilson, Richard H ^a   Johnston, Patrick G ^a   Van Schaeybroeck, Sandra ^a  

^a QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

^b KYUSHU UNIVERSITY   (Japan)

^c FUKUOKA UNIVERSITY   (Japan)

^d NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

EPHRIN RECEPTOR A2; HERMES ANTIGEN; K RAS PROTEIN; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN EFNA1; PROTEIN LGR5; PROTEIN RALA; PROTEIN RALGDS; REGULATOR PROTEIN; TUMOR MARKER; UNCLASSIFIED DRUG; GUANINE NUCLEOTIDE EXCHANGE FACTOR; KRAS PROTEIN, HUMAN; PROTEIN P21; RAL PROTEIN; RAS PROTEIN;

ARTICLE; CANCER PROGNOSIS; CANCER STAGING; CELL INVASION; CELL MIGRATION; COLORECTAL CANCER; COLORECTAL CANCER CELL LINE; COLORECTAL TUMOR; CONTROLLED STUDY; DAUGHTER CELL; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MAJOR CLINICAL STUDY; OVERALL SURVIVAL; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR DOWN REGULATION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; WILD TYPE; CELL MOTION; GENE EXPRESSION; GENETICS; KAPLAN MEIER METHOD; METABOLISM; MORTALITY; PATHOLOGY; PROGNOSIS; PROPORTIONAL HAZARDS MODEL; REPRODUCIBILITY; TUMOR CELL LINE; TUMOR INVASION;

BIOMARKERS, TUMOR; CELL LINE, TUMOR; CELL MOVEMENT; COLORECTAL NEOPLASMS; GENE EXPRESSION; HUMANS; KAPLAN-MEIER ESTIMATE; NEOPLASM INVASIVENESS; NEOPLASM STAGING; PROGNOSIS; PROPORTIONAL HAZARDS MODELS; PROTO-ONCOGENE PROTEINS P21(RAS); RAL GTP-BINDING PROTEINS; RAL GUANINE NUCLEOTIDE EXCHANGE FACTOR; RAS PROTEINS; RECEPTOR, EPHA2; REPRODUCIBILITY OF RESULTS; SIGNAL TRANSDUCTION;

EID: 84954526582     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-15-0603     Document Type: Article

References (50)

1. Allegra CJ, Yothers G, O'Connell MJ, Sharif S, Petrelli NJ, Colangelo LH, et al. Phase III trial assessing bevacizumab in stages II and III carcinoma of the colon: results of NSABP protocol C-08. J Clin Oncol 2011;29:11-6.
2. Alberts SR, Sargent DJ, Nair S, Mahoney MR, Mooney M, Thibodeau SN, et al. Effect of oxaliplatin, fluorouracil, and leucovorin with or without cetuximab on survivalamong patientswith resected stage III colon cancer: a randomized trial. Jama 2012;307:1383-93.
3. Pasquale EB. Eph receptors and ephrins in cancer: bidirectional signalling and beyond. Nat Rev Cancer 2010;10:165-80.
4. Pasquale EB. Eph receptor signalling casts a wide net on cell behaviour. Nat Rev Mol Cell Biol 2005;6:462-75.
5. Himanen JP. Ectodomain structures of Eph receptors. Semin Cell Dev Biol 2012;23:35-42.
6. Janes PW, Nievergall E, Lackmann M. Concepts and consequences of Eph receptor clustering. Semin Cell Dev Biol 2012;23:43-50.
7. Boyd AW, Bartlett PF, Lackmann M. Therapeutic targeting of EPH receptors and their ligands. Nat Rev Drug Discov 2014;13:39-62.
8. Udayakumar D, Zhang G, Ji Z, Njauw CN, Mroz P, Tsao H. EphA2 is a critical oncogene in melanoma. Oncogene 2011;30:4921-9.
9. Brantley-Sieders DM, Zhuang G, Hicks D, Fang WB, Hwang Y, Cates JM, et al. The receptor tyrosine kinase EphA2 promotes mammary adenocarcinoma tumorigenesis and metastatic progression in mice by amplifying ErbB2 signaling. J Clin Invest 2008;118:64-78.
10. Binda E, Visioli A, Giani F, Lamorte G, Copetti M, Pitter KL, et al. The EphA2 receptor drives self-renewal and tumorigenicity in stem-like tumor-propagating cells from human glioblastomas. Cancer Cell 2012;22:765-80.
11. Brannan JM, Dong W, Prudkin L, Behrens C, Lotan R, Bekele BN, et al. Expression of the receptor tyrosine kinase EphA2 is increased in smokers and predicts poor survival in non-small cell lung cancer. Clin Cancer Res 2009;15:4423-30.
12. Miura K, Wakayama Y, Tanino M, Orba Y, Sawa H, Hatakeyama M, et al. Involvement of EphA2-mediated tyrosine phosphorylation of Shp2 in Shp2-regulated activation of extracellular signal-regulated kinase. Oncogene 2013;32:5292-301.
13. Kyula JN, Van Schaeybroeck S, Doherty J, Fenning CS, Longley DB, Johnston PG. Chemotherapy-induced activation of ADAM-17: a novel mechanism of drug resistance in colorectal cancer. Clin Cancer Res 2010; 16:3378-89.
14. Van Schaeybroeck S, Kyula JN, Fenton A, Fenning CS, Sasazuki T, Shirasawa S, et al. Oncogenic Kras promotes chemotherapy-induced growth factor shedding via ADAM17. Cancer Res 2011;71:1071-80.
15. Van Schaeybroeck S, Kalimutho M, Dunne PD, Carson R, Allen W, Jithesh PV, et al. ADAM17-dependent c-MET-STAT3 signaling mediates resistance to MEK inhibitors in KRAS mutant colorectal cancer. Cell reports 2014;7: 1940-55.
16. Van Schaeybroeck S, Kelly DM, Kyula J, Stokesberry S, Fennell DA, Johnston PG, et al. Src and ADAM-17-mediated shedding of transforming growth factor-alpha is a mechanism of acute resistance to TRAIL. Cancer Res 2008;68:8312-21.
17. Dunne PD, McArt DG, Blayney JK, Kalimutho M, Greer S, Wang T, et al. AXL is a key regulator of inherent and chemotherapy-induced invasion and predicts a poor clinical outcome in early-stage colon cancer. Clin Cancer Res 2014;20:164-75.
18. Ong CW, Kim LG, Kong HH, Low LY, Iacopetta B, Soong R, et al. CD133 expression predicts for non-response to chemotherapy in colorectal cancer. Mod Pathol 2010;23:450-7.
19. Wang T, Ong CW, Shi J, Srivastava S, Yan B, Cheng CL, et al. Sequential expression of putative stem cell markers in gastric carcinogenesis. Br J Cancer 2011;105:658-65.
20. Wang T, Yeoh KG, Salto-Tellez M. Lgr5 expression is absent in human premalignant lesions of the stomach. Gut 2012;61:1777-8.
21. Oladipo O, Conlon S, O'Grady A, Purcell C, Wilson C, Maxwell PJ, et al. The expression and prognostic impact of CXC-chemokines in stage II and III colorectal cancer epithelial and stromal tissue. Br J Cancer 2011;104: 480-7.
22. Barrett T, Troup DB, Wilhite SE, Ledoux P, Evangelista C, Kim IF, et al. NCBI GEO: archive for functional genomics data sets-10 years on. Nucleic Acids Res 2011;39:D1005-10.
23. Edgar R, Domrachev M, Lash AE. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 2002;30:207-10.
24. Shirasawa S, Furuse M, Yokoyama N, Sasazuki T. Altered growth of human colon cancer cell lines disrupted at activated Ki-ras. Science 1993;260:85-8.
25. Miao H, Li DQ, Mukherjee A, Guo H, Petty A, Cutter J, et al. EphA2mediates ligand-dependent inhibition and ligand-independent promotion of cell migration and invasion via a reciprocal regulatory loop with Akt. Cancer Cell 2009;16:9-20.
26. Balasubramaniam D, Paul LN, Homan KT, Hall MC, Stauffacher CV. Specificity of HCPTP variants toward EphA2 tyrosines by quantitative selected reaction monitoring. Protein Sci 2011;20:1172-81.
27. Fang WB, Brantley-Sieders DM, Hwang Y, Ham AJ, Chen J. Identification and functional analysis of phosphorylated tyrosine residues within EphA2 receptor tyrosine kinase. J Biol Chem 2008;283:16017-26.
28. Macrae M, Neve RM, Rodriguez-Viciana P, Haqq C, Yeh J, Chen C, et al. A conditional feedback loop regulates Ras activity through EphA2. Cancer Cell 2005;8:111-8.
29. Miao H, Gale NW, Guo H, Qian J, Petty A, Kaspar J, et al. EphA2 promotes infiltrative invasion of glioma stem cells in vivo through cross-talk with Akt and regulates stem cell properties. Oncogene 2015;34:558-67.
30. Song W, Ma Y, Wang J, Brantley-Sieders D, Chen J. JNK signaling mediates EPHA2-dependent tumor cell proliferation, motility, and cancer stem cell-like properties in non-small cell lung cancer. Cancer Res 2014;74:2444-54.
31. Todaro M, Francipane MG, Medema JP, Stassi G. Colon cancer stem cells: promise of targeted therapy. Gastroenterology 2010;138:2151-62.
32. Heidorn SJ, Milagre C, Whittaker S, Nourry A, Niculescu-Duvas I, Dhomen N, et al. Kinase-dead BRAF and oncogenic RAS cooperate to drive tumor progression through CRAF. Cell 2010;140:209-21.
33. Ferro E, Trabalzini L. Ral GDS family members couple Ras to Ral signalling and that's not all. Cell Signal 2010;22:1804-10.
34. Smith JJ, Deane NG, Wu F, Merchant NB, Zhang B, Jiang A, et al. Experimentally derived metastasis gene expression profile predicts recurrence and death in patients with colon cancer. Gastroenterology 2010;138: 958-68.
35. Zelinski DP, Zantek ND, Stewart JC, Irizarry AR, Kinch MS. EphA2 overexpression causes tumorigenesis of mammary epithelial cells. Cancer Res 2001;61:2301-6.
36. Easty DJ, Guthrie BA, Maung K, Farr CJ, Lindberg RA, Toso RJ, et al. Protein B61 as a new growth factor: expression of B61 and up-regulation of its receptor epithelial cell kinase during melanoma progression. Cancer Res 1995;55:2528-32.
37. Wykosky J, Gibo DM, Stanton C, Debinski W. EphA2 as a novel molecular marker and target in glioblastoma multiforme. Mol Cancer Res 2005;3: 541-51.
38. Bogan C, Chen J, O'Sullivan MG, Cormier RT. Loss of EphA2 receptor tyrosine kinase reduces ApcMin/+tumorigenesis. Int J Cancer 2009; 124:1366-71.
39. Kataoka H, Igarashi H, Kanamori M, Ihara M, Wang JD, Wang YJ, et al. Correlation of EPHA2 overexpression with high microvessel count in human primary colorectal cancer. Cancer Sci 2004;95:136-41.
40. Du L, Rao G, Wang H, Li B, Tian W, Cui J, et al. CD44-positive cancer stem cells expressing cellular prion protein contribute to metastatic capacity in colorectal cancer. Cancer Res 2013;73:2682-94.
41. Tsuji S, Kawasaki Y, Furukawa S, Taniue K, Hayashi T, Okuno M, et al. The miR-363-GATA6-Lgr5 pathway is critical for colorectal tumourigenesis. Nat Commun 2014;5:3150.
42. Walker-Daniels J, Riese DJ 2nd, Kinch MS. c-Cbl-dependent EphA2 protein degradation is induced by ligand binding. Mol Cancer Res 2002;1:79-87.
43. Klijn C, Durinck S, Stawiski EW, Haverty PM, Jiang Z, Liu H, et al. A comprehensive transcriptional portrait of human cancer cell lines. Nat Biotechnol 2015;33:306-12.
44. Dohn M, Jiang J, Chen X. Receptor tyrosine kinase EphA2 is regulated by p53-family proteins and induces apoptosis. Oncogene 2001;20:6503-15.
45. Du X, Baldwin C, Hooker E, Glorion P, Lemay S. Basal and Src kinasemediated activation of the EphA2 promoter requires a cAMP-responsive element but is CREB-independent. J Cell Biochem 2011;112:1268-76.
46. Davies H, Bignell GR, Cox C, Stephens P, Edkins S, Clegg S, et al. Mutations of the BRAF gene in human cancer. Nature 2002;417:949-54.
47. Neel NF, Martin TD, Stratford JK, Zand TP, Reiner DJ, Der CJ. The Ral GEF ral effector signaling network: the road less traveled for anti-ras drug discovery. Genes Cancer 2011;2:275-87.
48. Martin TD, Samuel JC, Routh ED, Der CJ, Yeh JJ. Activation and involvement of Ral GTPases in colorectal cancer. Cancer Res 2011;71:206-15.
49. Yan C, Liu D, Li L, Wempe MF, Guin S, Khanna M, et al. Discovery and characterization of small molecules that target the GTPase Ral. Nature 2014;515:443-7.
50. Sadanandam A, Lyssiotis CA, Homicsko K, Collisson EA, Gibb WJ, Wullschleger S, et al. A colorectal cancer classification system that associates cellular phenotype and responses to therapy. Nat Med 2013; 19:619-25.