Focal adhesion kinase contributes to proliferative potential of ErbB2 mammary tumour cells but is dispensable for ErbB2 mammary tumour induction in vivo

Breast Cancer Research

Volumn 14, Issue 1, 2012, Pages

  Lahlou, Hicham ^a   Sanguin Gendreau, Virginie ^a   Frame, Margaret C ^c   Muller, William J ^a,b  

^a MCGILL UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CRE RECOMBINASE; EPIDERMAL GROWTH FACTOR RECEPTOR 2; FOCAL ADHESION KINASE; FOCAL ADHESION KINASE INHIBITOR; BCAR1 PROTEIN, MOUSE; CRK ASSOCIATED SUBSTRATE PROTEIN; ERBB2 PROTEIN, MOUSE; FOCAL ADHESION KINASE 1; FOCAL ADHESION KINASE 2; INTEGRASE; PAXILLIN; PTK2 PROTEIN, MOUSE; PTK2B PROTEIN, MOUSE; PXN PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CARCINOGENESIS; BREAST EPITHELIUM; BREAST HYPERPLASIA; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INACTIVATION; FEMALE; GENETIC RECOMBINATION; GENETIC TRANSCRIPTION; IN VIVO STUDY; MOUSE; MOUSE MAMMARY TUMOR ONCOVIRUS; NONHUMAN; PROTEIN EXPRESSION; TUMOR CELL; ANIMAL; APOPTOSIS; CANCER TRANSPLANTATION; CELL MOTION; CELL TRANSFORMATION; ENZYMOLOGY; EXPERIMENTAL NEOPLASM; GENE DELETION; GENETICS; LUNG TUMOR; METABOLISM; METASTASIS; PATHOLOGY; PHOSPHORYLATION; PHYSIOLOGY; TRANSGENIC MOUSE; TUMOR VOLUME;

ANIMALS; APOPTOSIS; CELL MOVEMENT; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; CRK-ASSOCIATED SUBSTRATE PROTEIN; FEMALE; FOCAL ADHESION KINASE 1; FOCAL ADHESION KINASE 2; GENE DELETION; INTEGRASES; LUNG NEOPLASMS; MAMMARY NEOPLASMS, EXPERIMENTAL; MICE; MICE, TRANSGENIC; NEOPLASM TRANSPLANTATION; PAXILLIN; PHOSPHORYLATION; RECEPTOR, ERBB-2; TUMOR BURDEN;

EID: 84857406562     PISSN: 14655411     EISSN: 1465542X     Source Type: Journal    
DOI: 10.1186/bcr3131     Document Type: Article

References (32)

1. Lightfoot HM, Lark A, Livasy CA, Moore DT, Cowan D, Dressler L, Craven RJ, Cance WG. Upregulation of focal adhesion kinase (FAK) expression in ductal carcinoma in situ (DCIS) is an early event in breast tumorigenesis. Breast Cancer Res Treat 2004, 88:109-116. 10.1007/s10549-004-1022-8, 15564794.
2. Oktay MH, Oktay K, Hamele-Bena D, Buyuk A, Koss LG. Focal adhesion kinase as a marker of malignant phenotype in breast and cervical carcinomas. Hum Pathol 2003, 34:240-245. 10.1053/hupa.2003.40, 12673558.
3. Lark AL, Livasy CA, Dressler L, Moore DT, Millikan RC, Geradts J, Iacocca M, Cowan D, Little D, Craven RJ, Cance W. High focal adhesion kinase expression in invasive breast carcinomas is associated with an aggressive phenotype. Mod Pathol 2005, 18:1289-1294. 10.1038/modpathol.3800424, 15861214.
4. Xu LH, Yang X, Bradham CA, Brenner DA, Baldwin AS, Craven RJ, Cance WG. The focal adhesion kinase suppresses transformation-associated, anchorage-independent apoptosis in human breast cancer cells. Involvement of death receptor-related signaling pathways. J Biol Chem 2000, 275:30597-30604.
5. Nurcombe V, Smart CE, Chipperfield H, Cool SM, Boilly B, Hondermarck H. The proliferative and migratory activities of breast cancer cells can be differentially regulated by heparan sulfates. J Biol Chem 2000, 275:30009-30018.
6. Schmitz KJ, Grabellus F, Callies R, Otterbach F, Wohlschlaeger J, Levkau B, Kimmig R, Schmid KW, Baba HA. High expression of focal adhesion kinase (p125FAK) in node-negative breast cancer is related to overexpression of HER-2/neu and activated Akt kinase but does not predict outcome. Breast Cancer Res 2005, 7:R194-203. 10.1186/bcr977, 1064131, 15743500.
7. Ignatoski KM, Maehama T, Markwart SM, Dixon JE, Livant DL, Ethier SP. ERBB-2 overexpression confers PI 3' kinase-dependent invasion capacity on human mammary epithelial cells. Br J Cancer 2000, 82:666-674. 10.1054/bjoc.1999.0979, 2363331, 10682681.
8. Behmoaram E, Bijian K, Jie S, Xu Y, Darnel A, Bismar TA, Alaoui-Jamali MA. Focal adhesion kinase-related proline-rich tyrosine kinase 2 and focal adhesion kinase are co-overexpressed in early-stage and invasive ErbB-2-positive breast cancer and cooperate for breast cancer cell tumorigenesis and invasiveness. Am J Pathol 2008, 173:1540-1550. 10.2353/ajpath.2008.080292, 2570143, 18832579.
9. Benlimame N, He Q, Jie S, Xiao D, Xu YJ, Loignon M, Schlaepfer DD, Alaoui-Jamali MA. FAK signaling is critical for ErbB-2/ErbB-3 receptor cooperation for oncogenic transformation and invasion. J Cell Biol 2005, 171:505-516. 10.1083/jcb.200504124, 2171271, 16275754.
10. McLean GW, Brown K, Arbuckle MI, Wyke AW, Pikkarainen T, Ruoslahti E, Frame MC. Decreased focal adhesion kinase suppresses papilloma formation during experimental mouse skin carcinogenesis. Cancer Res 2001, 61:8385-8389.
11. Hsia DA, Mitra SK, Hauck CR, Streblow DN, Nelson JA, Ilic D, Huang S, Li E, Nemerow GR, Leng J, Spencer KS, Cheresh DA, Schlaepfer DD. Differential regulation of cell motility and invasion by FAK. J Cell Biol 2003, 160:753-767. 10.1083/jcb.200212114, 2173366, 12615911.
12. McLean GW, Komiyama NH, Serrels B, Asano H, Reynolds L, Conti F, Hodivala-Dilke K, Metzger D, Chambon P, Grant SG, Frame MC. Specific deletion of focal adhesion kinase suppresses tumor formation and blocks malignant progression. Genes Dev 2004, 18:2998-3003. 10.1101/gad.316304, 535910, 15601818.
13. Slack-Davis JK, Hershey ED, Theodorescu D, Frierson HF, Parsons JT. Differential requirement for focal adhesion kinase signaling in cancer progression in the transgenic adenocarcinoma of mouse prostate model. Mol Cancer Ther 2009, 8:2470-2477. 10.1158/1535-7163.MCT-09-0262, 2728172, 19671741.
14. Lahlou H, Sanguin-Gendreau V, Zuo D, Cardiff RD, McLean GW, Frame MC, Muller WJ. Mammary epithelial-specific disruption of the focal adhesion kinase blocks mammary tumor progression. Proc Natl Acad Sci USA 2007, 104:20302-20307. 10.1073/pnas.0710091104, 2154426, 18056629.
15. Luo M, Fan H, Nagy T, Wei H, Wang C, Liu S, Wicha MS, Guan JL. Mammary epithelial-specific ablation of the focal adhesion kinase suppresses mammary tumorigenesis by affecting mammary cancer stem/progenitor cells. Cancer Res 2009, 69:466-474. 10.1158/0008-5472.CAN-08-3078, 3039129, 19147559.
16. Provenzano PP, Inman DR, Eliceiri KW, Beggs HE, Keely PJ. Mammary epithelial-specific disruption of focal adhesion kinase retards tumor formation and metastasis in a transgenic mouse model of human breast cancer. Am J Pathol 2008, 173:1551-1565. 10.2353/ajpath.2008.080308, 2570144, 18845837.
17. Pylayeva Y, Gillen KM, Gerald W, Beggs HE, Reichardt LF, Giancotti FG. Ras- and PI3K-dependent breast tumorigenesis in mice and humans requires focal adhesion kinase signaling. J Clin Invest 2009, 119:252-266. 2631302, 19147981.
18. Andrechek ER, Hardy WR, Siegel PM, Rudnicki MA, Cardiff RD, Muller WJ. Amplification of the neu/erbB-2 oncogene in a mouse model of mammary tumorigenesis. Proc Natl Acad Sci USA 2000, 97:3444-3449. 16259, 10716706.
19. Siegel PM, Ryan ED, Cardiff RD, Muller WJ. Elevated expression of activated forms of Neu/ErbB-2 and ErbB-3 are involved in the induction of mammary tumors in transgenic mice: implications for human breast cancer. Embo J 1999, 18:2149-2164. 10.1093/emboj/18.8.2149, 1171299, 10205169.
20. White DE, Kurpios NA, Zuo D, Hassell JA, Blaess S, Mueller U, Muller WJ. Targeted disruption of beta1-integrin in a transgenic mouse model of human breast cancer reveals an essential role in mammary tumor induction. Cancer Cell 2004, 6:159-170. 10.1016/j.ccr.2004.06.025, 15324699.
21. Soriano P. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat Genet 1999, 21:70-71. 10.1038/5007, 9916792.
22. Ursini-Siegel J, Hardy WR, Zuo D, Lam SH, Sanguin-Gendreau V, Cardiff RD, Pawson T, Muller WJ. ShcA signalling is essential for tumour progression in mouse models of human breast cancer. Embo J 2008, 27:910-920. 10.1038/emboj.2008.22, 2274931, 18273058.
23. Weis SM, Lim ST, Lutu-Fuga KM, Barnes LA, Chen XL, Gothert JR, Shen TL, Guan JL, Schlaepfer DD, Cheresh DA. Compensatory role for Pyk2 during angiogenesis in adult mice lacking endothelial cell FAK. J Cell Biol 2008, 181:43-50. 10.1083/jcb.200710038, 2287283, 18391070.
24. Fan H, Guan JL. Compensatory function of Pyk2 protein in the promotion of focal adhesion kinase (FAK)-null mammary cancer stem cell tumorigenicity and metastatic activity. J Biol Chem 2011, 286:18573-18582. 10.1074/jbc.M110.200717, 3099673, 21471206.
25. Marcotte R, Smith HW, Sanguin-Gendreau V, McDonough RV, Muller WJ. Mammary epithelial-specific disruption of c-Src impairs cell cycle progression and tumorigenesis. Proc Natl Acad Sci USA 2012, 109:2808-2813. 10.1073/pnas.1018861108, 21628573.
26. Huck L, Pontier SM, Zuo DM, Muller WJ. beta1-integrin is dispensable for the induction of ErbB2 mammary tumors but plays a critical role in the metastatic phase of tumor progression. Proc Natl Acad Sci USA 2010, 107:15559-15564. 10.1073/pnas.1003034107, 2932605, 20713705.
27. Pontier SM, Huck L, White DE, Rayment J, Sanguin-Gendreau V, Hennessy B, Zuo D, St-Arnaud R, Mills GB, Dedhar S, Marshall CJ, Muller WJ. Integrin-linked kinase has a critical role in ErbB2 mammary tumor progression: implications for human breast cancer. Oncogene 2010, 29:3374-3385. 10.1038/onc.2010.86, 20305688.
28. Cabodi S, Tinnirello A, Bisaro B, Tornillo G, del Pilar Camacho-Leal M, Forni G, Cojoca R, Iezzi M, Amici A, Montani M, Eva A, Di Stefano P, Muthuswamy SK, Tarone G, Turco E, Defilippi P. p130Cas is an essential transducer element in ErbB2 transformation. Faseb J 2010, 24:3796-3808. 10.1096/fj.10-157347, 20505116.
29. Rothenberg SM, Engelman JA, Le S, Riese DJ 2, Haber DA, Settleman J. Modeling oncogene addiction using RNA interference. Proc Natl Acad Sci USA 2008, 105:12480-12484. 10.1073/pnas.0803217105, 2517605, 18711136.
30. Tanjoni I, Walsh C, Uryu S, Tomar A, Nam JO, Mielgo A, Lim ST, Liang C, Koenig M, Sun C, Patel N, Kwok C, McMahon G, Stupack DG, Schlaepfer DD. PND-1186 FAK inhibitor selectively promotes tumor cell apoptosis in three-dimensional environments. Cancer Biol Ther 2010, 9:764-777. 10.4161/cbt.9.10.11434, 2933317, 20234191.
31. Walsh C, Tanjoni I, Uryu S, Tomar A, Nam JO, Luo H, Phillips A, Patel N, Kwok C, McMahon G, Stupack DG, Schlaepfer DD. Oral delivery of PND-1186 FAK inhibitor decreases tumor growth and spontaneous breast to lung metastasis in pre-clinical models. Cancer Biol Ther 2010, 9:778-790. 10.4161/cbt.9.10.11433, 2933309, 20234193.
32. Roberts WG, Ung E, Whalen P, Cooper B, Hulford C, Autry C, Richter D, Emerson E, Lin J, Kath J, Coleman K, Yao L, Martinez-Alsina L, Lorenzen M, Berliner M, Luzzio M, Patel N, Schmitt E, LaGreca S, Jani J, Wessel M, Marr E, Griffor M, Vajdos F. Antitumor activity and pharmacology of a selective focal adhesion kinase inhibitor, PF-562,271. Cancer Res 2008, 68:1935-1944. 10.1158/0008-5472.CAN-07-5155, 18339875.