Combined inhibition of AXL, Lyn and p130Cas kinases block migration of triple negative breast cancer cells

References

• Suyama E, Kawasaki H, Wadhwa R, Taira K. Cell migration and metastasis as targets of small RNA-based molecular genetic analyses. J Muscle Res Cell Motil 2004; 25:303-8; PMID:15548858; http://dx.doi.org/10.1007/s10974-004-4343-7
   PubMed Web of Science ®Google Scholar
• Weigelt B, Peterse JL, van ‘t Veer LJ. Breast cancer metastasis: markers and models. Nat Rev Cancer 2005; 5:591-602; PMID:16056258; http://dx.doi.org/10.1038/nrc1670
   PubMed Web of Science ®Google Scholar
• Mehlen P, Puisieux A. Metastasis: a question of life or death. Nat Rev Cancer 2006; 6:449-58; PMID:16723991; http://dx.doi.org/10.1038/nrc1886
   PubMed Web of Science ®Google Scholar
• Stafford LJ, Vaidya KS, Welch DR. Metastasis suppressors genes in cancer. Int J Biochem Cell Biol 2008; 40:874-91; PMID:18280770; http://dx.doi.org/10.1016/j.biocel.2007.12.016
   PubMed Web of Science ®Google Scholar
• Holland SJ, Powell MJ, Franci C, Chan EW, Friera AM, Atchison RE, McLaughlin J, Swift SE, Pali ES, Yam G, et al. Multiple roles for the receptor tyrosine kinase axl in tumor formation. Cancer Res 2005; 65:9294-303; PMID:16230391; http://dx.doi.org/10.1158/0008-5472.CAN-05-0993
   PubMed Web of Science ®Google Scholar
• Linger RM, Keating AK, Earp HS, Graham DK. TAM receptor tyrosine kinases: biologic functions, signaling, and potential therapeutic targeting in human cancer. Adv Cancer Res 2008; 100:35-83; PMID:18620092; http://dx.doi.org/10.1016/S0065-230X(08)00002-X
   PubMed Web of Science ®Google Scholar
• Lai C, Lemke G. An extended family of protein-tyrosine kinase genes differentially expressed in the vertebrate nervous system. Neuron 1991; 6:691-704; PMID:2025425; http://dx.doi.org/10.1016/0896-6273(91)90167-X
   PubMed Web of Science ®Google Scholar
• Hafizi S, Dahlback B. Signalling and functional diversity within the Axl subfamily of receptor tyrosine kinases. Cytokine Growth Factor Rev 2006:295-304; http://dx.doi.org/10.1016/j.cytogfr.2006.04.004
   PubMed Web of Science ®Google Scholar
• Goruppi S, Ruaro E, Varnum B, Schneider C. Requirement of phosphatidylinositol 3-kinase-dependent pathway and Src for Gas6-Axl mitogenic and survival activities in NIH 3T3 fibroblasts. Mol Cell Biol 1997; 17:4442-53; PMID:9234702
   PubMed Web of Science ®Google Scholar
• Shankar SL, O’Guin K, Kim M, Varnum B, Lemke G, Brosnan CF, Shafit-Zagardo B. Gas6Axl signaling activates the phosphatidylinositol 3-kinaseAkt1 survival pathway to protect oligodendrocytes from tumor necrosis factor alpha-induced apoptosis. J Neurosci 2006; 26:5638-48; PMID:16723520; http://dx.doi.org/10.1523/JNEUROSCI.5063-05.2006
   PubMed Web of Science ®Google Scholar
• Ghosh AK, Secreto C, Boysen J, Sassoon T, Shanafelt TD, Mukhopadhyay D, Kay NE. The novel receptor tyrosine kinase Axl is constitutively active in B-cell chronic lymphocytic leukemia and acts as a docking site of nonreceptor kinases: implications for therapy. Blood 2011; 117:1928-37; PMID:21135257; http://dx.doi.org/10.1182/blood-2010-09-305649
   PubMed Web of Science ®Google Scholar
• Zhang YX, Knyazev PG, Cheburkin YV, Sharma K, Knyazev YP, Orfi L, Szabadkai I, Daub H, Keri G, Ullrich A. AXL is a potential target for therapeutic intervention in breast cancer progression. Cancer Res 2008; 68:1905-15; PMID:18339872; http://dx.doi.org/10.1158/0008-5472.CAN-07-2661
   PubMed Web of Science ®Google Scholar
• Gjerdrum C, Tiron C, Hoiby T, Stefansson I, Haugen H, Sandal T, Collett K, Li S, McCormack E, Gjertsen BT, et al. Axl is an essential epithelial-to-mesenchymal transition-induced regulator of breast cancer metastasis and patient survival. Proc Natl Acad Sci U S A 2010; 107:1124-9; PMID:20080645; http://dx.doi.org/10.1073/pnas.0909333107
   PubMed Web of Science ®Google Scholar
• Craven RJ, Xu LH, Weiner TM, Fridell YW, Dent GA, Srivastava S, Varnum B, Liu ET, Cance WG. Receptor tyrosine kinases expressed in metastatic colon cancer. Int J Cancer 1995; 60:791-7; PMID:7896447; http://dx.doi.org/10.1002/ijc.2910600611
   PubMed Web of Science ®Google Scholar
• Tworkoski K, Singhal G, Szpakowski S, Zito CI, Bacchiocchi A, Muthusamy V, Bosenberg M, Krauthammer M, Halaban R, Stern DF. Phosphoproteomic screen identifies potential therapeutic targets in melanoma. Mol Cancer Res 2011; 9:801-12; PMID:21521745; http://dx.doi.org/10.1158/1541-7786.MCR-10-0512
   PubMed Web of Science ®Google Scholar
• Avilla E, Guarino V, Visciano C, Liotti F, Svelto M, Krishnamoorthy G, Franco R, Melillo RM. Activation of TYRO3AXL tyrosine kinase receptors in thyroid cancer. Cancer Res 2011; 71:1792-804; PMID:21343401; http://dx.doi.org/10.1158/0008-5472.CAN-10-2186
   PubMed Web of Science ®Google Scholar
• Paccez JD, Vasques GJ, Correa RG, Vasconcellos JF, Duncan K, Gu X, Bhasin M, Libermann TA, Zerbini LF. The receptor tyrosine kinase Axl is an essential regulator of prostate cancer proliferation and tumor growth and represents a new therapeutic target. Oncogene 2012; PMID:22410775
   PubMed Web of Science ®Google Scholar
• Li Y, Ye X, Tan C, Hongo JA, Zha J, Liu J, Kallop D, Ludlam MJ, Pei L. Axl as a potential therapeutic target in cancer: role of Axl in tumor growth, metastasis and angiogenesis. Oncogene 2009; 28:3442-55; PMID:19633687; http://dx.doi.org/10.1038/onc.2009.212
   PubMed Web of Science ®Google Scholar
• Rankin EB, Fuh KC, Taylor TE, Krieg AJ, Musser M, Yuan J, Wei K, Kuo CJ, Longacre TA, Giaccia AJ. AXL is an essential factor and therapeutic target for metastatic ovarian cancer. Cancer Res 2010; 70:7570-9; PMID:20858715; http://dx.doi.org/10.1158/0008-5472.CAN-10-1267
   PubMed Web of Science ®Google Scholar
• Lee HJ, Jeng YM, Chen YL, Chung L, Yuan RH. Gas6Axl pathway promotes tumor invasion through the transcriptional activation of Slug in hepatocellular carcinoma. Carcinogenesis 2013; 19:19
   Google Scholar
• Ou WB, Corson JM, Flynn DL, Lu WP, Wise SC, Bueno R, Sugarbaker DJ, Fletcher JA. AXL regulates mesothelioma proliferation and invasiveness. Oncogene 2011; 30:1643-52; PMID:21132014; http://dx.doi.org/10.1038/onc.2010.555
   PubMed Web of Science ®Google Scholar
• Paccez JD, Vasques GJ, Correa RG, Vasconcellos JF, Duncan K, Gu X, Bhasin M, Libermann TA, Zerbini LF. The receptor tyrosine kinase Axl is an essential regulator of prostate cancer proliferation and tumor growth and represents a new therapeutic target. Oncogene 2013; 32:689-98; PMID:22410775; http://dx.doi.org/10.1038/onc.2012.89
   PubMed Web of Science ®Google Scholar
• Leconet W, Larbouret C, Chardes T, Thomas G, Neiveyans M, Busson M, Jarlier M, Radosevic-Robin N, Pugniere M, Bernex F, et al. Preclinical validation of AXL receptor as a target for antibody-based pancreatic cancer immunotherapy. Oncogene 2013; 18:487
   Google Scholar
• Keating AK, Kim GK, Jones AE, Donson AM, Ware K, Mulcahy JM, Salzberg DB, Foreman NK, Liang X, Thorburn A, et al. Inhibition of Mer and Axl receptor tyrosine kinases in astrocytoma cells leads to increased apoptosis and improved chemosensitivity. Mol Cancer Ther 2010; 9:1298-307; PMID:20423999; http://dx.doi.org/10.1158/1535-7163.MCT-09-0707
   PubMed Web of Science ®Google Scholar
• Verma A, Warner SL, Vankayalapati H, Bearss DJ, Sharma S. Targeting Axl and Mer kinases in cancer. Mol Cancer Ther 2011; 10:1763-73; PMID:21933973; http://dx.doi.org/10.1158/1535-7163.MCT-11-0116
   PubMed Web of Science ®Google Scholar
• Boschelli F, Arndt K, Gambacorti-Passerini C. Bosutinib: a review of preclinical studies in chronic myelogenous leukaemia. Eur J Cancer 2010; 46:1781-9; PMID:20399641; http://dx.doi.org/10.1016/j.ejca.2010.02.032
   PubMed Web of Science ®Google Scholar
• Gherardi E, Birchmeier W, Birchmeier C, Vande Woude G. Targeting MET in cancer: rationale and progress. Nat Rev Cancer 2012; 12:89-103; PMID:22270953; http://dx.doi.org/10.1038/nrc3205
   PubMed Web of Science ®Google Scholar
• Schroeder GM, An Y, Cai ZW, Chen XT, Clark C, Cornelius LA, Dai J, Gullo-Brown J, Gupta A, Henley B, et al. Discovery of N-(4-(2-amino-3-chloropyridin-4-yloxy)-3-fluorophenyl)-4-ethoxy-1-(4-fluorophenyl)-2-oxo-1,2-dihydropyridine-3-carboxamide (BMS-777607), a selective and orally efficacious inhibitor of the Met kinase superfamily. J Med Chem 2009; 52:1251-4; PMID:19260711; http://dx.doi.org/10.1021/jm801586s
   PubMed Web of Science ®Google Scholar
• Hochgrafe F, Zhang L, O’Toole SA, Browne BC, Pinese M, Porta Cubas A, Lehrbach GM, Croucher DR, Rickwood D, Boulghourjian A, et al. Tyrosine phosphorylation profiling reveals the signaling network characteristics of Basal breast cancer cells. Cancer Res 2010; 70:9391-401; PMID:20861192; http://dx.doi.org/10.1158/0008-5472.CAN-10-0911
   PubMed Web of Science ®Google Scholar
• Meric F, Lee WP, Sahin A, Zhang H, Kung HJ, Hung MC. Expression profile of tyrosine kinases in breast cancer. Clin Cancer Res 2002; 8:361-7; PMID:11839650
   PubMed Web of Science ®Google Scholar
• Kohn KW, Zeeberg BR, Reinhold WC, Sunshine M, Luna A, Pommier Y. Gene expression profiles of the NCI-60 human tumor cell lines define molecular interaction networks governing cell migration processes. PLoS One 2012; 7:3 PMID:22570691; http://dx.doi.org/10.1371/journal.pone.0035716
   PubMed Web of Science ®Google Scholar
• Davis MI, Hunt JP, Herrgard S, Ciceri P, Wodicka LM, Pallares G, Hocker M, Treiber DK, Zarrinkar PP. Comprehensive analysis of kinase inhibitor selectivity. Nat Biotechnol 2011; 29:1046-51; PMID:22037378; http://dx.doi.org/10.1038/nbt.1990
   PubMed Web of Science ®Google Scholar
• Choi YL, Bocanegra M, Kwon MJ, Shin YK, Nam SJ, Yang JH, Kao J, Godwin AK, Pollack JR. LYN is a mediator of epithelial-mesenchymal transition and a target of dasatinib in breast cancer. Cancer Res 2010; 70:2296-306; PMID:20215510; http://dx.doi.org/10.1158/0008-5472.CAN-09-3141
   PubMed Web of Science ®Google Scholar
• Geiger B. A role for p130Cas in mechanotransduction. Cell 2006; 127:879-81; PMID:17129774; http://dx.doi.org/10.1016/j.cell.2006.11.020
   PubMed Web of Science ®Google Scholar
• Wozniak MA, Modzelewska K, Kwong L, Keely PJ. Focal adhesion regulation of cell behavior. Biochim Biophys Acta 2004; 5:2-3; PMID:15246682
   PubMed Web of Science ®Google Scholar
• Nielsen TO, Hsu FD, Jensen K, Cheang M, Karaca G, Hu Z, Hernandez-Boussard T, Livasy C, Cowan D, Dressler L, et al. Immunohistochemical and clinical characterization of the basal-like subtype of invasive breast carcinoma. Clin Cancer Res 2004; 10:5367-74; PMID:15328174; http://dx.doi.org/10.1158/1078-0432.CCR-04-0220
   PubMed Web of Science ®Google Scholar
• Rakha EA, Reis-Filho JS, Ellis IO. Basal-like breast cancer: a critical review. J Clin Oncol 2008; 26:2568-81; PMID:18487574; http://dx.doi.org/10.1200/JCO.2007.13.1748
   PubMed Web of Science ®Google Scholar
• Zhang Z, Lee JC, Lin L, Olivas V, Au V, LaFramboise T, Abdel-Rahman M, Wang X, Levine AD, Rho JK, et al. Activation of the AXL kinase causes resistance to EGFR-targeted therapy in lung cancer. Nat Genet 2012; 44:852-60; PMID:22751098; http://dx.doi.org/10.1038/ng.2330
   PubMed Web of Science ®Google Scholar
• Vuoriluoto K, Haugen H, Kiviluoto S, Mpindi JP, Nevo J, Gjerdrum C, Tiron C, Lorens JB, Ivaska J. Vimentin regulates EMT induction by Slug and oncogenic H-Ras and migration by governing Axl expression in breast cancer. Oncogene 2011; 30:1436-48; PMID:21057535; http://dx.doi.org/10.1038/onc.2010.509
   PubMed Web of Science ®Google Scholar
• Tan DS, Haaland B, Gan JM, Tham SC, Sinha I, Tan EH, Lim KH, Takano A, Krisna SS, Thu MM, et al. Bosutinib inhibits migration and invasion via ack1 in kras mutant non-small cell lung cancer. Mol Cancer 2014; 13:1476-4598; PMID:24461128; http://dx.doi.org/10.1186/1476-4598-13-13
   PubMed Web of Science ®Google Scholar
• Holland SJ, Pan A, Franci C, Hu Y, Chang B, Li W, Duan M, Torneros A, Yu J, Heckrodt TJ, et al. R428, a selective small molecule inhibitor of Axl kinase, blocks tumor spread and prolongs survival in models of metastatic breast cancer. Cancer Res 2010; 70:1544-54; PMID:20145120; http://dx.doi.org/10.1158/0008-5472.CAN-09-2997
   PubMed Web of Science ®Google Scholar
• Braunger J, Schleithoff L, Schulz AS, Kessler H, Lammers R, Ullrich A, Bartram CR, Janssen JW. Intracellular signaling of the UfoAxl receptor tyrosine kinase is mediated mainly by a multi-substrate docking-site. Oncogene 1997; 14:2619-31; PMID:9178760; http://dx.doi.org/10.1038/sj.onc.1201123
   PubMed Web of Science ®Google Scholar
• Ye X, Li Y, Stawicki S, Couto S, Eastham-Anderson J, Kallop D, Weimer R, Wu Y, Pei L. An anti-Axl monoclonal antibody attenuates xenograft tumor growth and enhances the effect of multiple anticancer therapies. Oncogene 2010; 29:5254-64; PMID:20603615; http://dx.doi.org/10.1038/onc.2010.268
   PubMed Web of Science ®Google Scholar
• Yeh CY, Shin SM, Yeh HH, Wu TJ, Shin JW, Chang TY, Raghavaraju G, Lee CT, Chiang JH, Tseng VS, et al. Transcriptional activation of the Axl and PDGFR-alpha by c-Met through a ras- and Src-independent mechanism in human bladder cancer. BMC Cancer 2011; 11:139; PMID:21496277; http://dx.doi.org/10.1186/1471-2407-11-139
   PubMed Web of Science ®Google Scholar
• Meyer AS, Miller MA, Gertler FB, Lauffenburger DA. The receptor AXL diversifies EGFR signaling and limits the response to EGFR-targeted inhibitors in triple-negative breast cancer cells. Science Signaling 2013; 6:ra66; PMID:23921085; http://dx.doi.org/10.1126/scisignal.2004155
   PubMed Web of Science ®Google Scholar
• Cunningham-Edmondson AC, Hanks SK. p130Cas substrate domain signaling promotes migration, invasion, and survival of estrogen receptor-negative breast cancer cells. Breast Cancer (London) 2009; 2009:39-52; PMID:21253442
   PubMedGoogle Scholar
• Defilippi P, Di Stefano P, Cabodi S. p130Cas: a versatile scaffold in signaling networks. Trends Cell Biol 2006; 16:257-63; PMID:16581250; http://dx.doi.org/10.1016/j.tcb.2006.03.003
   PubMed Web of Science ®Google Scholar
• Sanchez-Bailon MP, Calcabrini A, Gomez-Dominguez D, Morte B, Martin-Forero E, Gomez-Lopez G, Molinari A, Wagner KU, Martin-Perez J. Src kinases catalytic activity regulates proliferation, migration and invasiveness of MDA-MB-231 breast cancer cells. Cell Signal 2012; 24:1276-86; PMID:22570868; http://dx.doi.org/10.1016/j.cellsig.2012.02.011
   PubMed Web of Science ®Google Scholar
• Vultur A, Buettner R, Kowolik C, Liang W, Smith D, Boschelli F, Jove R. SKI-606 (bosutinib), a novel Src kinase inhibitor, suppresses migration and invasion of human breast cancer cells. Mol Cancer Ther 2008; 7:1185-94; PMID:18483306; http://dx.doi.org/10.1158/1535-7163.MCT-08-0126
   PubMed Web of Science ®Google Scholar
• Paolino M, Choidas A, Wallner S, Pranjic B, Uribesalgo I, Loeser S, Jamieson AM, Langdon WY, Ikeda F, Fededa JP, et al. The E3 ligase Cbl-b and TAM receptors regulate cancer metastasis via natural killer cells. Nature 2014; 19; PMID:24553136; http://dx.doi.org/10.1038/nature12998
   PubMed Web of Science ®Google Scholar
• Conradt L, Godl K, Schaab C, Tebbe A, Eser S, Diersch S, Michalski CW, Kleeff J, Schnieke A, Schmid RM, et al. Disclosure of erlotinib as a multikinase inhibitor in pancreatic ductal adenocarcinoma. Neoplasia 2011; 13:1026-34; PMID:22131878
   PubMed Web of Science ®Google Scholar