Effects of dasatinib on EphA2 receptor tyrosine kinase activity and downstream signalling in pancreatic cancer

Bantscheff M, Eberhard D, Abraham Y, Bastuck S, Boesche M, Hobson S, Mathieson T, Perrin J, Raida M, Rau C, Reader V, Sweetman G, Bauer A, Bouwmeester T, Hopf C, Kruse U, Neubauer G, Ramsden N, Rick J, Kuster B, Drewes G (2007) Quantitative chemical proteomics reveals mechanisms of action of clinical ABL kinase inhibitors. Nat Biotechnol 25: 1035–1044

Batlle E, Bacani J, Begthel H, Jonkeer S, Gregorieff A, Born Mvd, Malats Nr, Sancho E, Boon E, Pawson T, Gallinger S, Pals S, Clevers H (2005) EphB receptor activity suppresses colorectal cancer progression. Nature 435: 1126–1130

Brantley DM, Cheng N, Thompson EJ, Lin Q, Brekken RA, Thorpe PE, Muraoka RS, Cerretti DP, Pozzi A, Jackson D, Lin C, Chen J (2002) Soluble Eph A receptors inhibit tumor angiogenesis and progression in vivo. Oncogene 21: 7011–7026

Carles-Kinch K, Kilpatrick KE, Stewart JC, Kinch MS (2002) Antibody targeting of the EphA2 tyrosine kinase inhibits malignant cell behavior. Cancer Res 62: 2840–2847

Dobrzanski P, Hunter K, Jones-Bolin S, Chang H, Robinson C, Pritchard S, Zhao H, Ruggeri B (2004) Antiangiogenic and antitumor efficacy of EphA2 receptor antagonist. Cancer Res 64: 910–919

Dodelet VC, Pasquale EB (2000) Eph receptors and ephrin ligands: embryogenesis to tumorigenesis. Oncogene 19: 5614–5619

Duxbury MS, Ito H, Zinner MJ, Ashley SW, Whang EE (2004) Ligation of EphA2 by Ephrin A1-Fc inhibits pancreatic adenocarcinoma cellular invasiveness. Biochem Biophys Res Commun 320: 1096–1102

Easty DJ, Herlyn M, Bennett DC (1995) Abnormal protein tyrosine kinase gene expression during melanoma progression and metastasis. Int J Cancer 60: 129–136

Fang WB, Brantley-Sieders DM, Parker MA, Reith AD, Chen J (2005) A kinase-dependent role for EphA2 receptor in promoting tumor growth and metastasis. Oncogene 24: 7859–7868

Guo H, Miao H, Gerber L, Singh J, Denning MF, Gilliam AC, Wang B (2006) Disruption of EphA2 receptor tyrosine kinase leads to increased susceptibility to carcinogenesis in mouse skin. Cancer Res 66: 7050–7058

Holland SJ, Gale NW, Gish GD, Roth RA, Zhou S, Cantley LC, Henkemeyer M, Yancopoulos GD, Pawson T (1997) Juxtamembrane tyrosine residues couple the Eph family receptor EphB2/Nuk to specific SH2 domain proteins in neuronal cells. EMBO J 16: 3877–3888

Huang F, Reeves K, Han X, Fairchild C, Platero S, Wong TW, Lee F, Shaw P, Clark E (2007) Identification of candidate molecular markers predicting sensitivity in solid tumors to dasatinib: rationale for patient selection. Cancer Res 67: 2226–2238

Huusko P, Ponciano-Jackson D, Wolf M, Kiefer JA, Azorsa DO, Tuzmen S, Weaver D, Robbins C, Moses T, Allinen M, Hautaniemi S, Chen Y, Elkahloun A, Basik M, Bova GS, Bubendorf L, Lugli A, Sauter G, Schleutker J, Ozcelik H, Elowe S, Pawson T, Trent JM, Carpten JD, Kallioniemi OP, Mousses S (2004) Nonsense-mediated decay microarray analysis identifies mutations of EPHB2 in human prostate cancer. Nat Genet 36: 979–983

Ihle JN (1995) Cytokine receptor signalling. Nature 377: 591–594

Ireton RC, Chen J (2005) EphA2 receptor tyrosine kinase as a promising target for cancer therapeutics. Curr Cancer Drug Targets 5: 149–157

Jiang T, Qiu Y (2003) Interaction between Src and a C-terminal proline-rich motif of Akt is required for Akt activation. J Biol Chem 278: 15789–15793

Johnson F, Saigal B, Tran H, Donato N (2007) Abrogation of signal transducer and activator of transcription 3 reactivation after Src kinase inhibition results in synergistic antitumor effects. Clin Cancer Res 13: 4233–4244

Johnson FM, Saigal B, Talpaz M, Donato NJ (2005) Dasatinib (BMS-354825) tyrosine kinase inhibitor suppresses invasion and induces cell cycle arrest and apoptosis of head and neck squamous cell carcinoma and non-small cell lung cancer cells. Clin Cancer Res 11: 6924–6932

Kanai M, Konda Y, Nakajima T, Izumi Y, Kanda N, Nanakin A, Kubohara Y, Chiba T (2003) Differentiation-inducing factor-1 (DIF-1) inhibits STAT3 activity involved in gastric cancer cell proliferation via MEK-ERK-dependent pathway. Oncogene 22: 548–554

Kiewlich D, Zhang J, Grossy C, Xiay W, Larseny B, Cobby RR, Birocy S, Guy J-M, Satoy T, Lighty DR, Heitnery T, Willudaz J, Vogely D, Monteclaroy F, Citkowiczy A, Roffler SR, Zajchowski DA (2006) Anti-EphA2 antibodies decrease EphA2 protein levels in murine CT26 colorectal and human MDA-231 breast tumors but do not inhibit tumor growth. Neoplasia 8: 18–30

Kinch MS, Burridge K (1995) Altered adhesions in ras-transformed breast epithelial cells. Biochem Soc Trans 23: 446–450

Kinch MS, Carles-Kinch K (2003) Overexpression and functional alterations of the EphA2 tyrosine kinase in cancer. Clin Exp Metastasis 20: 59–68

Kinch MS, Moore M-B, Harpole Jr DH (2003) Predictive value of the EphA2 receptor tyrosine kinase in lung cancer recurrence and survival. Clin Cancer Res 9: 613–618

Knöll B, Drescher U (2004) Src family kinases are involved in EphA receptor-mediated retinal axon guidance. J Neurosci 24: 6248–6257

Kullander K, Klein R (2002) Mechanisms and functions of Eph and ephrin signalling. Nat Rev Mol Cell Biol 3: 475–486

Landen Jr CN, Chavez-Reyes A, Bucana C, Schmandt R, Deavers MT, Lopez-Berestein G, Sood AK (2005) Therapeutic EphA2 gene targeting in vivo using neutral liposomal small interfering RNA delivery. Cancer Res 65: 6910–6918

Landen Jr CN, Lu C, Han LY, Coffman KT, Bruckheimer E, Halder J, Mangala LS, Merritt WM, Lin YG, Gao C, Schmandt R, Kamat AA, Li Y, Thaker P, Gershenson DM, Parikh NU, Gallick GE, Kinch MS, Sood AK (2006) Efficacy and antivascular effects of EphA2 reduction with an agonistic antibody in ovarian cancer. J Natl Cancer Inst 98: 1558–1570

Lombardo LJ, Lee FY, Chen P, Norris D, Barrish JC, Behnia K, Castaneda S, Cornelius LA, Das J, Doweyko AM, Fairchild C, Hunt JT, Inigo I, Johnston K, Kamath A, Kan D, Klei H, Marathe P, Pang S, Peterson R, Pitt S, Schieven GL, Schmidt RJ, Tokarski J, Wen M-L, Wityak J, Borzilleri RM (2004) Discovery of N-(2-chloro-6-methyl- phenyl)-2-(6-(4-(2-hydroxyethyl)- piperazin-1-yl)-2-methylpyrimidin-4- ylamino)thiazole-5-carboxamide (BMS-354825), a dual Src/Abl kinase inhibitor with potent antitumor activity in preclinical assays. J Med Chem 47: 6658–6661

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

Miao H, Burnett E, Kinch M, Simon E, Wang B (2000) Activation of EphA2 kinase suppresses integrin function and causes focal-adhesion kinase dephosphorylation. Nat Cell Biol 2: 62–69

Miao H, Wei B-R, Peehl DM, Li Q, Alexandrou T, Schelling JR, Rhim JS, Sedor JR, Burnett E, Wang B (2001) Activation of EphA receptor tyrosine kinase inhibits the Ras/MAPK pathway. Nat Cell Biol 3: 527–530

Miyazaki T, Kato H, Fukuchi M, Nakajima M, Kuwano H (2003) EphA2 overexpression correlates with poor prognosis in esophageal squamous cell carcinoma. Int J Cancer 103: 657–663

Mudali SV, Fu B, Lakkur SS, Luo M, Embuscado EE, Iacobuzio-Donahue CA (2006) Patterns of EphA2 protein expression in primary and metastatic pancreatic carcinoma and correlation with genetic status. Clin Exp Metastasis 23: 357–365

Nakamoto M, Bergemann AD (2002) Diverse roles for the Eph family of receptor tyrosine kinases in carcinogenesis. Microsc Res Tech 59: 58–67

Ogawa K, Pasqualini R, Lindberg RA, Kain R, Freeman AL, Pasquale EB (2000) The ephrin-A1 ligand and its receptor, EphA2, are expressed during tumor neovascularization. Oncogene 19: 6043–6052

Olayioye MA, Badache A, Daly JM, Hynes NE (2001) An essential role for Src kinase in ErbB receptor signaling through the MAPK pathway. Exp Cell Res 267: 81–87

Pandey A, Lazar DF, Saltiel AR, Dixit VM (1994) Activation of the Eck receptor protein tyrosine kinase stimulates phosphatidylinositol 3-kinase activity. J Biol Chem 269: 30154–30157

Pasquale EB (2004) Eph-ephrin promiscuity is now crystal clear. Nat Neurosci 7: 417–418

Pratt RL, Kinch MS (2002) Activation of the EphA2 tyrosine kinase stimulates the MAP/ERK kinase signaling cascade. Oncogene 21: 7690–7699

Rix U, Hantschel O, Durnberger G, Remsing Rix LL, Planyavsky M, Fernbach NV, Kaupe I, Bennett KL, Valent P, Colinge J, Kocher T, Superti-Furga G (2007) Chemical proteomic profiles of the BCR-ABL inhibitors imatinib, nilotinib, and dasatinib reveal novel kinase and nonkinase targets. Blood 110: 4055–4063

Serrels A, Macpherson IR, Evans TR, Lee FY, Clark EA, Sansom OJ, Ashton GH, Frame MC, Brunton VG (2006) Identification of potential biomarkers for measuring inhibition of Src kinase activity in colon cancer cells following treatment with dasatinib. Mol Cancer Ther 5: 3014–3022

Shor AC, Keschman EA, Lee FY, Muro-Cacho C, Letson GD, Trent JC, Pledger WJ, Jove R (2007) Dasatinib inhibits migration and invasion in diverse human sarcoma cell lines and induces apoptosis in bone sarcoma cells dependent on SRC kinase for survival. Cancer Res 67: 2800–2808

Talpaz M, Shah NP, Kantarjian H, Donato N, Nicoll J, Paquette R, Cortes J, O'Brien S, Nicaise C, Bleickardt E, Blackwood-Chirchir MA, Iyer V, Chen T-T, Huang F, Decillis AP, Sawyers CL (2006) Dasatinib in imatinib-resistant Philadelphia chromosome-positive leukemias. N Engl J Med 354: 2531–2541

Trevino JG, Summy JM, Lesslie DP, Parikh NU, Hong DS, Lee FY, Donato NJ, Abbruzzese JL, Baker CH, Gallick GE (2006) Inhibition of SRC expression and activity inhibits tumor progression and metastasis of human pancreatic adenocarcinoma cells in an orthotopic nude mouse model. Am J Pathol 168: 962–972

Walker-Daniels J, Hess AR, Hendrix MJ, Kinch MS (2003) Differential regulation of EphA2 in normal and malignant cells. Am J Pathol 162: 1037–1042

Walker-Daniels J, Riese II DJ, Kinch MS (2002) c-Cbl-dependent EphA2 protein degradation is induced by ligand binding. Mol Cancer Res 1: 79–87

Wang XD, Reeves K, Luo FR, Xu LA, Lee F, Clark E, Huang F (2007) Identification of candidate predictive and surrogate molecular markers for dasatinib in prostate cancer: rationale for patient selection and efficacy monitoring. Genome Biol 8: R255

Wang Y, Ota S, Kataoka H, Kanamori M, Li Z, Band H, Tanaka M, Sugimura H (2002) Negative regulation of EphA2 receptor by Cbl. Biochem Biophys Res Commun 296: 214–220

Yeatman TJ (2004) A renaissance for SRC. Nat Rev Cancer 4: 470–480

Yokogami K, Wakisaka S, Avruch J, Reeves SA (2000) Serine phosphorylation and maximal activation of STAT3 during CNTF signaling is mediated by the rapamycin target mTOR. Curr Biol 10: 47–50

Zantek ND, Azimi M, Fedor-Chaiken M, Wang B, Brackenbury R, Kinch MS (1999) E-cadherin regulates the function of the EphA2 receptor tyrosine kinase. Cell Growth Differ 10: 629–638

Zantek ND, Walker-Daniels J, Stewart J, Hansen RK, Robinson D, Miao H, Wang B, Kung H-J, Bissell MJ, Kinch MS (2001) MCF-10A-NeoST: a new cell system for studying cell-ECM and cell-cell interactions in breast cancer. Clin Cancer Res 7: 3640–3648

Zelinski DP, Zantek ND, Stewart JC, Irizarry AR, Kinch MS (2001) EphA2 overexpression causes tumorigenesis of mammary epithelial cells. Cancer Res 61: 2301–2306

Zimmer M, Palmer A, Kohler J, Klein R (2003) EphB-ephrinB bi-directional endocytosis terminates adhesion allowing contact mediated repulsion. Nat Cell Biol 5: 869–878