Eph family co-expression patterns define unique clusters predictive of cancer phenotype

References

• Abraham S, Knapp DW, Cheng L, Snyder PW, Mittal SK, Bangari DS, Kinch M, et al. 2006. Expression of EphA2 and Ephrin A-1 in carcinoma of the urinary bladder. Clin Cancer Res 12:353–360
   PubMed Web of Science ®Google Scholar
• Arvanitis D, Davy A. 2008. Eph/ephrin signaling: Networks. Genes Dev 22:416–429
   PubMed Web of Science ®Google Scholar
• Astin JW, Batson J, Kadir S, Charlet J, Persad RA, Gillatt D, Oxley JD, Nobes CD. 2010. Competition amongst Eph receptors regulates contact inhibition of locomotion and invasiveness in prostate cancer cells. Nat Cell Biol 12:1194–1204
   PubMed Web of Science ®Google Scholar
• Batlle E, Henderson JT, Beghtel H, van den Born MM, Sancho E, Huls G, Meeldijk J, et al. 2002. Beta-catenin and TCF mediate cell positioning in the intestinal epithelium by controlling the expression of EphB/ephrinB. Cell 111:251–263
   PubMed Web of Science ®Google Scholar
• Batson J, Maccarthy-Morrogh L, Archer A, Tanton H, Nobes CD. 2014. EphA receptors regulate prostate cancer cell dissemination through Vav2-RhoA mediated cell-cell repulsion. Biol Open 3:453–462
   Google Scholar
• Becerikli M, Merwart B, Lam MC, Suppelna P, Rittig A, Mirmohammedsadegh A, Stricker I, et al. 2014. EPHB4 tyrosine-kinase receptor expression and biological significance in soft tissue sarcoma. Int J Cancer [Epub ahead of print]
   Google Scholar
• Berclaz G, Karamitopoulou E, Mazzucchelli L, Rohrbach V, Dreher E, Ziemiecki A, Andres AC. 2003. Activation of the receptor protein tyrosine kinase EphB4 in endometrial hyperplasia and endometrial carcinoma. Ann Oncol 14:220–226
   Google Scholar
• Binda E, Visioli A, Giani F, Lamorte G, Copetti M, Pitter KL, Huse JT, et al. 2012. The EphA2 receptor drives self-renewal and tumorigenicity in stem-like tumor-propagating cells from human glioblastomas. Cancer Cell 22:765–780
   PubMed Web of Science ®Google Scholar
• Boyd AW, Bartlett PF, Lackmann M. 2014. Therapeutic targeting of EPH receptors and their ligands. Nat Rev Drug Discov 13:39–62
   Google Scholar
• Brantley-Sieders DM. 2012. Clinical relevance of Ephs and ephrins in cancer: Lessons from breast, colorectal, and lung cancer profiling. Semin Cell Dev Biol 23:102–108
   PubMedGoogle Scholar
• Brantley-Sieders DM, Jiang A, Sarma K, Badu-Nkansah A, Walter DL, Shyr Y, Chen J. 2011. Eph/Ephrin profiling in human breast cancer reveals significant associations between expression level and clinical outcome. PLoS One 6:e24426
   PubMed Web of Science ®Google Scholar
• Brantley-Sieders DM, Zhuang G, Hicks D, Fang WB, Hwang Y, Cates JM, Coffman K, et al. 2008. The receptor tyrosine kinase EphA2 promotes mammary adenocarcinoma tumorigenesis and metastatic progression in mice by amplifying ErbB2 signaling. J Clin Invest 118:64–78
   PubMed Web of Science ®Google Scholar
• Cerami E, Gao J, Dogrusoz U, Gross BE, Sumer SO, Aksoy BA, Jacobsen A, et al. 2012. The cBio cancer genomics portal: An open platform for exploring multidimensional cancer genomics data. Cancer Discov 2:401–404
   PubMed Web of Science ®Google Scholar
• Chen J, Song W, Amato K. 2014. Eph receptor tyrosine kinases in cancer stem cells. Cytokine Growth Factor Rev [Epub ahead of print]
   Google Scholar
• Chukkapalli S, Amessou M, Dilly AK, Dekhil H, Zhao J, Liu Q, Bejna A, et al. 2014. Role of the EphB2 receptor in autophagy, apoptosis and invasion in human breast cancer cells. Exp Cell Res 320:233–246
   PubMed Web of Science ®Google Scholar
• Clevers H, Batlle E. 2006. EphB/EphrinB receptors and Wnt signaling in colorectal cancer. Cancer Res 66:2–5
   PubMed Web of Science ®Google Scholar
• Cline MS, Craft B, Swatloski T, Goldman M, Ma S, Haussler D, Zhu J. 2013. Exploring TCGA Pan-Cancer data at the UCSC Cancer Genomics Browser. Sci Rep 3:2652
   PubMed Web of Science ®Google Scholar
• Cortina C, Palomo-Ponce S, Iglesias M, Fernández-Masip JL, Vivancos A, Whissell G, Humà M, et al. 2007. EphB-ephrin-B interactions suppress colorectal cancer progression by compartmentalizing tumor cells. Nat Genet 39:1376–1383
   PubMed Web of Science ®Google Scholar
• Davy A, Gale NW, Murray EW, Klinghoffer RA, Soriano P, Feuerstein C, Robbins SM. 1999. Compartmentalized signaling by GPI-anchored ephrin-A5 requires the Fyn tyrosine kinase to regulate cellular adhesion. Genes Dev 13:3125–3135
   PubMed Web of Science ®Google Scholar
• Day BW, Stringer BW, Al-Ejeh F, Ting MJ, Wilson J, Ensbey KS, Jamieson PR, et al. 2013a. EphA3 maintains tumorigenicity and is a therapeutic target in glioblastoma multiforme. Cancer Cell 23:238–248
   PubMed Web of Science ®Google Scholar
• Day BW, Stringer BW, Wilson J, Jeffree RL, Jamieson PR, Ensbey KS, Bruce ZC, et al. 2013b. Glioma surgical aspirate: A viable source of tumor tissue for experimental research. Cancers (Basel) 5:357–371
   Google Scholar
• Day BW, Stringer BW, Boyd AW. 2014. Eph receptors as therapeutic targets in glioblastoma. Br J Cancer 111:1255–1261
   PubMed Web of Science ®Google Scholar
• Davies H, Hunter C, Smith R, Stephens P, Greenman C, Bignell G, Teague J, et al. 2005. Somatic mutations of the protein kinase gene family in human lung cancer. Cancer Res 65:7591–7595
   PubMed Web of Science ®Google Scholar
• Depaepe V, Suarez-Gonzalez N, Dufour A, Passante L, Gorski JA, Jones KR, Ledent C, Vanderhaeghen P. 2005. Ephrin signalling controls brain size by regulating apoptosis of neural progenitors. Nature 435:1244–1250
   PubMed Web of Science ®Google Scholar
• Doble BW, Woodgett JR. 2003. GSK-3: Tricks of the trade for a multi-tasking kinase. J Cell Sci 116:1175–1186
   PubMed Web of Science ®Google Scholar
• Doble BW, Woodgett JR. 2007. Role of glycogen synthase kinase-3 in cell fate and epithelial-mesenchymal transitions. Cells Tissues Organs 185:73–84
   PubMed Web of Science ®Google Scholar
• Dohn M, Jiang J, Chen X. 2001. Receptor tyrosine kinase EphA2 is regulated by p53-family proteins and induces apoptosis. Oncogene 20:6503–6515
   PubMedGoogle Scholar
• Dopeso H, Mateo-Lozano S, Mazzolini R, Rodrigues P, Lagares-Tena L, Ceron J, Romero J, et al. 2009. The receptor tyrosine kinase EPHB4 has tumor suppressor activities in intestinal tumorigenesis. Cancer Res 69:7430–7438
   PubMed Web of Science ®Google Scholar
• Dottori M, Down M, Hüttmann A, Fitzpatrick DR, Boyd AW. 1999. Cloning and characterization of EphA3 (Hek) gene promoter: DNA methylation regulates expression in hematopoietic tumor cells. Blood 94:2477–2486
   PubMed Web of Science ®Google Scholar
• Duffy SL, Coulthard MG, Spanevello MD, Herath NI, Yeadon TM, McCarron JK, Carter JC, et al. 2008. Generation and characterization of EphA1 receptor tyrosine kinase reporter knockout mice. Genesis 46:553–561
   Google Scholar
• Easty DJ, Bennett DC. 2000. Protein tyrosine kinases in malignant melanoma. Melanoma Res 10:401–411
   PubMedGoogle Scholar
• Franceschini A, Szklarczyk D, Frankild S, Kuhn M, Simonovic M, Roth A, Lin J, et al. 2013. STRING v9.1: Protein-protein interaction networks, with increased coverage and integration. Nucleic Acids Res 41:D808–D815
   PubMed Web of Science ®Google Scholar
• Fukai J, Yokote H, Yamanaka R, Arao T, Nishio K, Itakura T. 2008. EphA4 promotes cell proliferation and migration through a novel EphA4-FGFR1 signaling pathway in the human glioma U251 cell line. Mol Cancer Ther 7:2768–2778
   PubMed Web of Science ®Google Scholar
• Gao J, Aksoy BA, Dogrusoz U, Dresdner G, Gross B, Sumer SO, Sun Y, et al. 2013. Integrative analysis of complex cancer genomics and clinical profiles using the cBioPortal. Sci Signal 6:pl1
   PubMed Web of Science ®Google Scholar
• Giaginis C, Tsoukalas N, Bournakis E, Alexandrou P, Kavantzas N, Patsouris E, Theocharis S. 2014. Ephrin (Eph) receptor A1, A4, A5 and A7 expression in human non-small cell lung carcinoma: Associations with clinicopathological parameters, tumor proliferative capacity and patients' survival. BMC Clin Pathol 14:1–12
   Google Scholar
• Goldman M, Craft B, Swatloski T, Ellrott K, Cline M, Diekhans M, Ma S, et al. 2013. The UCSC Cancer Genomics Browser: Update 2013. Nucleic Acids Res 41:D949– D954
   Google Scholar
• Harada K, Hiramoto-Yamaki N, Negishi M, Katoh H. 2011. Ephexin4 and EphA2 mediate resistance to anoikis through RhoG and phosphatidylinositol 3-kinase. Exp Cell Res 317:1701–1713
   PubMed Web of Science ®Google Scholar
• Herath NI, Boyd AW. 2010. The role of Eph receptors and ephrin ligands in colorectal cancer. Int J Cancer 126:2003–2011
   Google Scholar
• Herath NI, Doecke J, Spanevello MD, Leggett BA, Boyd AW. 2009. Epigenetic silencing of EphA1 expression in colorectal cancer is correlated with poor survival. Br J Cancer 100:1095–1102
   PubMed Web of Science ®Google Scholar
• Herath NI, Spanevello MD, Doecke JD, Smith FM, Pouponnot C, Boyd AW. 2012. Complex expression patterns of Eph receptor tyrosine kinases and their ephrin ligands in colorectal carcinogenesis. Eur J Cancer 48:753–762
   Google Scholar
• Herath NI, Spanevello MD, Sabesan S, Newton T, Cummings M, Duffy S, Lincoln D, et al. 2006. Over-expression of Eph and ephrin genes in advanced ovarian cancer: Ephrin gene expression correlates with shortened survival. BMC Cancer 6:144
   Google Scholar
• Heroult M, Schaffner F, Augustin HG. 2006. Eph receptor and ephrin ligand-mediated interactions during angiogenesis and tumor progression. Exp Cell Res 312:642–650
   PubMedGoogle Scholar
• Hu M, Carles-Kinch KL, Zelinski DP, Kinch MS. 2004. EphA2 induction of fibronectin creates a permissive microenvironment for malignant cells. Mol Cancer Res 2:533–540
   PubMed Web of Science ®Google Scholar
• Huang J, Xiao D, Li G, Ma J, Chen P, Yuan W, Hou F, et al. 2014. EphA2 promotes epithelial-mesenchymal transition through the Wnt/beta-catenin pathway in gastric cancer cells. Oncogene 33:2737–2747
   Google Scholar
• Ji XD, Li G, Feng YX, Zhao JS, Li JJ, Sun ZJ, Shi S, et al. 2011. EphB3 is overexpressed in non-small-cell lung cancer and promotes tumor metastasis by enhancing cell survival and migration. Cancer Res 71:1156–1166
   PubMed Web of Science ®Google Scholar
• Kang JU, Koo SH, Kwon KC, Park JW, Kim JM. 2009. Identification of novel candidate target genes, including EPHB3, MASP1 and SST at 3q26.2-q29 in squamous cell carcinoma of the lung. BMC Cancer 9:237
   Google Scholar
• Kawai H, Kobayashi M, Hiramoto-Yamaki N, Harada K, Negishi M, Katoh H. 2013. Ephexin4-mediated promotion of cell migration and anoikis resistance is regulated by serine 897 phosphorylation of EphA2. FEBS Open Bio 3:78–82
   PubMed Web of Science ®Google Scholar
• Kim Y, Park E, Noh H, Park S. 2013. Expression of EphA8-Fc in transgenic mouse embryos induces apoptosis of neural epithelial cells during brain development. Dev Neurobiol 73:702–712
   Google Scholar
• Kopantzev EP, Monastyrskaya GS, Vinogradova TV, Zinovyeva MV, Kostina MB, Filyukova OB, Tonevitsky AG, et al. 2008. Differences in gene expression levels between early and later stages of human lung development are opposite to those between normal lung tissue and non-small lung cell carcinoma. Lung Cancer 62:23–34
   Google Scholar
• Kumar SR, Scehnet JS, Ley EJ, Singh J, Krasnoperov V, Liu R, Manchanda PK, et al. 2009. Preferential induction of EphB4 over EphB2 and its implication in colorectal cancer progression. Cancer Res 69:3736–3745
   PubMed Web of Science ®Google Scholar
• Kwon MJ. 2013. Emerging roles of claudins in human cancer. Int J Mol Sci 14:18148–18180
   Google Scholar
• Lackmann M, Boyd A.W. 2008. Eph, a protein family coming of age: More confusion, insight, or complexity? Sci Signal 1:re2
   PubMed Web of Science ®Google Scholar
• Larsen AB, Pedersen MW, Stockhausen MT, Grandal MV, van Deurs B, Poulsen HS. 2007. Activation of the EGFR gene target EphA2 inhibits epidermal growth factor-induced cancer cell motility. Mol Cancer Res 5:283–293
   PubMedGoogle Scholar
• Lawrence MS, Stojanov P, Polak P, Kryukov GV, Cibulskis K, Sivachenko A, Carter SL, et al. 2013. Mutational heterogeneity in cancer and the search for new cancer-associated genes. Nature 499:214–218
   PubMed Web of Science ®Google Scholar
• Li G, Ji XD, Gao H, Zhao JS, Xu JF, Sun ZJ, Deng YZ, et al. 2012. EphB3 suppresses non-small-cell lung cancer metastasis via a PP2A/RACK1/Akt signalling complex. Nat Commun 3:667
   Google Scholar
• Li JJ, Liu DP, Liu GT, Xie D. 2009. EphrinA5 acts as a tumor suppressor in glioma by negative regulation of epidermal growth factor receptor. Oncogene 28:1759–1768
   PubMed Web of Science ®Google Scholar
• Lisabeth EM, Falivelli G, Pasquale EB. 2013. Eph receptor signaling and ephrins. Cold Spring Harb Perspect Biol 5:a009159
   Google Scholar
• Lisabeth EM, Fernandez C, Pasquale EB. 2012. Cancer somatic mutations disrupt functions of the EphA3 receptor tyrosine kinase through multiple mechanisms. Biochemistry 51:1464–1475
   PubMedGoogle Scholar
• Liu C, Huang H, Wang C, Kong Y, Zhang H. 2014. Involvement of ephrin receptor A4 in pancreatic cancer cell motility and invasion. Oncol Lett 7:2165–2169
   PubMed Web of Science ®Google Scholar
• Liu DP, Wang Y, Koeffler HP, Xie D. 2007. Ephrin-A1 is a negative regulator in glioma through down-regulation of EphA2 and FAK. Int J Oncol 30:865–871
   Google Scholar
• Lu M, Miller KD, Gokmen-Polar Y, Jeng MH, Kinch MS. 2003. EphA2 overexpression decreases estrogen dependence and tamoxifen sensitivity. Cancer Res 63:3425–3429
   PubMed Web of Science ®Google Scholar
• McCarron JK, Stringer BW, Day BW, Boyd AW. 2010. Ephrin expression and function in cancer. Future Oncol 6:165–176
   Google Scholar
• Macrae M, Neve RM, Rodriguez-Viciana P, Haqq C, Yeh J, Chen C, Gray JW, McCormick F. 2005. A conditional feedback loop regulates Ras activity through EphA2. Cancer Cell 8:111–118
   PubMed Web of Science ®Google Scholar
• Marshall CJ. 1995. Specificity of receptor tyrosine kinase signaling: Transient versus sustained extracellular signal-regulated kinase activation. Cell 80:179–185
   PubMed Web of Science ®Google Scholar
• Maki-Nevala S, Kaur Sarhadi V, Tuononen K, Lagström S, Ellonen P, Rönty M, Wirtanen A, et al. 2013. Mutated ephrin receptor genes in non-small cell lung carcinoma and their occurrence with driver mutations-targeted resequencing study on formalin-fixed, paraffin-embedded tumor material of 81 patients. Genes Chromosomes Cancer 52:1141–1149
   Google Scholar
• Miao H, Li DQ, Mukherjee A, Guo H, Petty A, Cutter J, Basilion JP, et al. 2009. EphA2 mediates ligand-dependent inhibition and ligand-independent promotion of cell migration and invasion via a reciprocal regulatory loop with Akt. Cancer Cell 16:9–20
   PubMed Web of Science ®Google Scholar
• Miao H, Wei BR, Peehl DM, Li Q, Alexandrou T, Schelling JR, Rhim JS, et al. 2001. Activation of EphA receptor tyrosine kinase inhibits the Ras/MAPK pathway. Nat Cell Biol 3:527–530
   PubMed Web of Science ®Google Scholar
• Miyazaki K, Inokuchi M, Takagi Y, Kato K, Kojima K, Sugihara K. 2013. EphA4 is a prognostic factor in gastric cancer. BMC Clin Pathol 13:1–9
   Google Scholar
• Nakamura R, Kataoka H, Sato N, Kanamori M, Ihara M, Igarashi H, Ravshanov S, et al. 2005. EPHA2/EFNA1 expression in human gastric cancer. Cancer Sci 96:42–47
   PubMed Web of Science ®Google Scholar
• Noren NK, Foos G, Hauser CA, Pasquale EB. 2006. The EphB4 receptor suppresses breast cancer cell tumorigenicity through an Abl-Crk pathway. Nat Cell Biol 8:815–825
   PubMed Web of Science ®Google Scholar
• Onder TT, Gupta PB, Mani SA, Yang J, Lander ES, Weinberg RA. 2008. Loss of E-cadherin promotes metastasis via multiple downstream transcriptional pathways. Cancer Res 68:3645–3654
   PubMed Web of Science ®Google Scholar
• Pasquale EB. 2005. Eph receptor signalling casts a wide net on cell behaviour. Nat Rev Mol Cell Biol 6:462–475
   PubMed Web of Science ®Google Scholar
• Pasquale EB. 2008. Eph-ephrin bidirectional signaling in physiology and disease. Cell 133:38–52
   PubMed Web of Science ®Google Scholar
• Pasquale EB. 2010. Eph receptors and ephrins in cancer: Bidirectional signalling and beyond. Nat Rev Cancer 10:165–180
   PubMed Web of Science ®Google Scholar
• Perl AK, Wilgenbus P, Dahl U, Semb H, Christofori G. 1998. A causal role for E-cadherin in the transition from adenoma to carcinoma. Nature 392:190–193
   PubMed Web of Science ®Google Scholar
• Ståhl S, Kaminskyy VO, Efazat G, Hyrslova Vaculova A, Rodriguez-Nieto S, Moshfegh A, Lewensohn R, et al. 2013. Inhibition of Ephrin B3-mediated survival signaling contributes to increased cell death response of non-small cell lung carcinoma cells after combined treatment with ionizing radiation and PKC 412. Cell Death Dis 4:e454
   Google Scholar
• Stephen LJ, Fawkes AL, Verhoeve A, Lemke G, Brown A. 2007. A critical role for the EphA3 receptor tyrosine kinase in heart development. Dev Biol 302:66–79
   PubMedGoogle Scholar
• Sukka-Ganesh B, Mohammed KA, Kaye F, Goldberg EP, Nasreen N. 2012. Ephrin-A1 inhibits NSCLC tumor growth via induction of Cdx-2 a tumor suppressor gene. BMC Cancer 12:309
   Google Scholar
• Taddei ML, Parri M, Angelucci A, Bianchini F, Marconi C, Giannoni E, Raugei G, et al. 2011. EphA2 induces metastatic growth regulating amoeboid motility and clonogenic potential in prostate carcinoma cells. Mol Cancer Res 9:149–160
   Google Scholar
• Tanaka M, Kamata R, Sakai R. 2005. EphA2 phosphorylates the cytoplasmic tail of Claudin-4 and mediates paracellular permeability. J Biol Chem 280:42375–42382
   PubMed Web of Science ®Google Scholar
• Toma MI, Erdmann K, Diezel M, Meinhardt M, Zastrow S, Fuessel S, Wirth MP, Baretton GB. 2014. Lack of Ephrin receptor A1 is a favorable independent prognostic factor in clear cell renal cell carcinoma. PLoS One 9:e102262
   Google Scholar
• Thiery JP, Acloque H, Huang RY, Nieto MA. 2009. Epithelial-mesenchymal transitions in development and disease. Cell 139:871–890
   PubMed Web of Science ®Google Scholar
• Vail ME, Murone C, Tan A, Hii L, Abebe D, Janes PW, Lee FT, et al. 2014. Targeting EphA3 inhibits cancer growth by disrupting the tumor stromal microenvironment. Cancer Res 74:4470–4481
   PubMed Web of Science ®Google Scholar
• Vendrell JA, Magnino F, Danis E, Duchesne MJ, Pinloche S, Pons M, Birnbaum D, et al. 2004. Estrogen regulation in human breast cancer cells of new downstream gene targets involved in estrogen metabolism, cell proliferation and cell transformation. J Mol Endocrinol 32:397–414
   Google Scholar
• Walker-Daniels J, Coffman K, Azimi M, Rhim JS, Bostwick DG, Snyder P, Kerns BJ, et al. 1999. Overexpression of the EphA2 tyrosine kinase in prostate cancer. Prostate 41:275–280
   PubMed Web of Science ®Google Scholar
• Wood LD, Calhoun ES, Silliman N, Ptak J, Szabo S, Powell SM, Riggins GJ, et al. 2006. Somatic mutations of GUCY2F, EPHA3, and NTRK3 in human cancers. Hum Mutat 27:1060–1061
   PubMedGoogle Scholar
• Yang NY, Fernandez C, Richter M, Xiao Z, Valencia F, Tice DA, Pasquale EB. 2011. Crosstalk of the EphA2 receptor with a serine/threonine phosphatase suppresses the Akt-mTORC1 pathway in cancer cells. Cell Signal 23:201–212
   PubMed Web of Science ®Google Scholar
• Yokote H, Fujita K, Jing X, Sawada T, Liang S, Yao L, Yan X, et al. 2005. Trans-activation of EphA4 and FGF receptors mediated by direct interactions between their cytoplasmic domains. Proc Natl Acad Sci U S A 102:18866–18871
   PubMed Web of Science ®Google Scholar
• Zelinski DP, Zantek ND, Stewart JC, Irizarry AR, Kinch MS. 2001. EphA2 overexpression causes tumorigenesis of mammary epithelial cells. Cancer Res 61:2301–2306
   PubMed Web of Science ®Google Scholar
• Zhang G, Njauw CN, Park JM, Naruse C, Asano M, Tsao H. 2008. EphA2 is an essential mediator of UV radiation-induced apoptosis. Cancer Res 68:1691–1696
   PubMed Web of Science ®Google Scholar
• Zhuang G, Brantley-Sieders DM, Vaught D, Yu J, Xie L, Wells S, Jackson D, et al. 2010. Elevation of receptor tyrosine kinase EphA2 mediates resistance to trastuzumab therapy. Cancer Res 70:299–308
   PubMed Web of Science ®Google Scholar
• Zhuang G, Song W, Amato K, Hwang Y, Lee K, Boothby M, Ye F, et al. 2012. Effects of cancer-associated EPHA3 mutations on lung cancer. J Natl Cancer Inst 104:1182–1197
   PubMedGoogle Scholar