FER kinase promotes breast cancer metastasis by regulating α 6 - And β 1 -integrin-dependent cell adhesion and anoikis resistance

Oncogene

Volumn 32, Issue 50, 2013, Pages 5582-5592

  Ivanova, I A ^a   Vermeulen, J F ^a   Ercan, C ^a   Houthuijzen, J M ^a,b   Saig, F A ^a   Vlug, E J ^a   Van Der Wall, E ^a,b   Van Diest, P J ^a   Vooijs, M ^a   Derksen, P W B ^a  

^a MAASTRICHT UNIVERSITY MEDICAL CENTER   (Netherlands)

^b UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

breast cancer; cell adhesion; cell migration; FER kinase; metastasis

Indexed keywords

ALPHA6 INTEGRIN; BETA1 INTEGRIN; PROTEIN KINASE FER;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANOIKIS; ARTICLE; BREAST CANCER; CANCER CELL CULTURE; CANCER GROWTH; CANCER PROGNOSIS; CANCER SURVIVAL; CELL MIGRATION; CONTROLLED STUDY; FEMALE; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; LYMPH NODE METASTASIS; METASTASIS; MOUSE; NONHUMAN; OVERALL SURVIVAL; PRIORITY JOURNAL; TUMOR INVASION;

EID: 84890559183     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2013.277     Document Type: Article

References (54)

1. Ferlay J, Shin HR, Bray F, Forman D, Mathers C, Parkin DM. Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int J Cancer 2008; 127: 2893-2917.
2. Jemal A, Siegel R, Xu J, Ward E. Cancer statistics 2010. CA Cancer J Clin 2010; 60: 277-300.
3. Hudis CA. Trastuzumab: mechanism of action and use in clinical practice. N Engl J Med 2007; 357: 39-51.
4. Heath RJ, Insall RH. F-BAR domains: multifunctional regulators of membrane curvature. J Cell Sci 2008; 121: 1951-1954.
5. Pawson T, Letwin K, Lee T, Hao QL, Heisterkamp N, Groffen J. The FER gene is evolutionarily conserved and encodes a widely expressed member of the FPS/FES protein-tyrosine kinase family. Mol Cell Biol 1989; 9: 5722-5725.
6. Zirngibl R, Schulze D, Mirski SE, Cole SP, Greer PA. Subcellular localization analysis of the closely related Fps/Fes and Fer protein-tyrosine kinases suggests a distinct role for Fps/Fes in vesicular trafficking. Exp Cell Res 2001; 266: 87-94.
7. Kim L, Wong TW. The cytoplasmic tyrosine kinase FER is associated with the catenin-like substrate pp120 and is activated by growth factors. Mol Cell Biol 1995; 15: 4553-4561.
8. Kim L, Wong TW. Growth factor-dependent phosphorylation of the actin-binding protein cortactin is mediated by the cytoplasmic tyrosine kinase FER. J Biol Chem 1998; 273: 23542-23548.
9. Xu G, Craig AW, Greer P, Miller M, Anastasiadis PZ, Lilien J et al. Continuous association of cadherin with beta-catenin requires the non-receptor tyrosinekinase Fer. J Cell Sci 2004; 117: 3207-3219.
10. El Sayegh TY, Arora PD, Fan L, Laschinger CA, Greer PA, McCulloch CA et al. Phosphorylation of N-cadherin-associated cortactin by Fer kinase regulates N-cadherin mobility and intercellular adhesion strength. Mol Biol Cell 2005; 16: 5514-5527.
11. Rosato R, Veltmaat JM, Groffen J, Heisterkamp N. Involvement of the tyrosine kinase fer in cell adhesion. Mol Cell Biol 1998; 18: 5762-5770.
12. Arregui C, Pathre P, Lilien J, Balsamo J. The nonreceptor tyrosine kinase fer mediates cross-talk between N-cadherin and beta1-integrins. J Cell Biol 2000; 149: 1263-1274.
13. Sangrar W, Gao Y, Scott M, Truesdell P, Greer PA. Fer-mediated cortactin phosphorylation is associated with efficient fibroblast migration and is dependent on reactive oxygen species generation during integrin-mediated cell adhesion. Mol Cell Biol 2007; 27: 6140-6152.
14. Craig AW, Greer PA. Fer kinase is required for sustained p38 kinase activation and maximal chemotaxis of activated mast cells. Mol Cell Biol 2002; 22: 6363-6374.
15. Itoh T, Hasegawa J, Tsujita K, Kanaho Y, Takenawa T. The tyrosine kinase Fer is a downstream target of the PLD-PA pathway that regulates cell migration. Sci Signal 2009; 2: ra52.
16. Yoneyama T, Angata K, Bao X, Courtneidge S, Chanda SK, Fukuda M. Fer kinase regulates cell migration through alpha-dystroglycan glycosylation. Mol Biol Cell 2012; 23: 771-780.
17. Pasder O, Shpungin S, Salem Y, Makovsky A, Vilchick S, Michaeli S et al. Downregulation of Fer induces PP1 activation and cell-cycle arrest in malignant cells. Oncogene 2006; 25: 4194-4206.
18. Voisset E, Lopez S, Chaix A, Georges C, Hanssens K, Prebet T et al. FES kinases are required for oncogenic FLT3 signaling. Leukemia 2010; 24: 721-728.
19. Allard P, Zoubeidi A, Nguyen LT, Tessier S, Tanguay S, Chevrette M et al. Links between Fer tyrosine kinase expression levels and prostate cell proliferation. Mol Cell Endocrinol 2000; 159: 63-77.
20. Zoubeidi A, Rocha J, Zouanat FZ, Hamel L, Scarlata E, Aprikian AG et al. The Fer tyrosine kinase cooperates with interleukin-6 to activate signal transducer and activator of transcription 3 and promote human prostate cancer cell growth. Mol Cancer Res 2009; 7: 142-155.
21. Li H, Ren Z, Kang X, Zhang L, Li X, Wang Y et al. Identification of tyrosinephosphorylated proteins associated with metastasis and functional analysis of FER in human hepatocellular carcinoma cells. BMC Cancer 2009; 9: 366.
22. Wei C, Wu S, Li X, Wang Y, Ren R, Lai Y et al. High expression of FER tyrosine kinase predicts poor prognosis in clear cell renal cell carcinoma. Oncol Lett 2013; 5: 473-478.
23. Miyata Y, Kanda S, Sakai H, Greer PA. Fer expression correlates with malignant aggressiveness and poor prognosis in renal cell carcinoma. Cancer Sci 104: 681-686.
24. Guo C, Stark GR. FER tyrosine kinase (FER) overexpression mediates resistance to quinacrine through EGF-dependent activation of NF-kappaB. Proc Natl Acad Sci USA 2011; 108: 7968-7973.
25. Rae JM, Creighton CJ, Meck JM, Haddad BR, Johnson MD. MDA-MB-435 cells are derived from M14 melanoma cells: a loss for breast cancer, but a boon for melanoma research. Breast Cancer Res Treat 2007; 104: 13-19.
26. Kenny PA, Lee GY, Myers CA, Neve RM, Semeiks JR, Spellman PT et al. The morphologies of breast cancer cell lines in three-dimensional assays correlate with their profiles of gene expression. Mol Oncol 2007; 1: 84-96.
27. Frisch SM, Francis H. Disruption of epithelial cell-matrix interactions induces apoptosis. J Cell Biol 1994; 124: 619-626.
28. Derksen PW, Liu X, Saridin F, van der Gulden H, Zevenhoven J, Evers B et al. Somatic inactivation of E-cadherin and p53 in mice leads to metastatic lobular mammary carcinoma through induction of anoikis resistance and angiogenesis. Cancer Cell 2006; 10: 437-449.
29. Gimeno R, Weijer K, Voordouw A, Uittenbogaart CH, Legrand N, Alves NL et al. Monitoring the effect of gene silencing by RNA interference in human CD34 cells injected into newborn RAG2/ gammac/ mice: functional inactivation of p53 in developing T cells. Blood 2004; 104: 3886-3893.
30. Leone BA, Romero A, Rabinovich MG, Vallejo CT, Bianco A, Perez JE et al. Stage IV breast cancer: clinical course and survival of patients with osseous versus extraosseous metastases at initial diagnosis. The GOCS (Grupo Oncologico Cooperativo del Sur) experience. Am J Clin Oncol 1988; 11: 618-622.
31. Rosen PR, Groshen S, Saigo PE, Kinne DW, Hellman S. A long-term follow-up study of survival in stage I (T1N0M0) and stage II (T1N1M0) breast carcinoma. J Clin Oncol 1989; 7: 355-366.
32. Braun S, Cevatli BS, Assemi C, Janni W, Kentenich CR, Schindlbeck C et al. Comparative analysis of micrometastasis to the bone marrow and lymph nodes of node-negative breast cancer patients receiving no adjuvant therapy. J Clin Oncol 2001; 19: 1468-1475.
33. Giampieri S, Manning C, Hooper S, Jones L, Hill CS, Sahai E. Localized and reversible TGFbeta signalling switches breast cancer cells from cohesive to single cell motility. Nat Cell Biol 2009; 11: 1287-1296.
34. Neve RM, Chin K, Fridlyand J, Yeh J, Baehner FL, Fevr T et al. A collection of breast cancer cell lines for the study of functionally distinct cancer subtypes. Cancer Cell 2006; 10: 515-527.
35. Kao J, Salari K, Bocanegra M, Choi YL, Girard L, Gandhi J et al. Molecular profiling of breast cancer cell lines defines relevant tumor models and provides a resource for cancer gene discovery. PLoS One 2009; 4: e6146.
36. Brew CT, Aronchik I, Kosco K, McCammon J, Bjeldanes LF, Firestone GL. Indole-3- carbinol inhibits MDA-MB-231 breast cancer cell motility and induces stress fibers and focal adhesion formation by activation of Rho kinase activity. Int J Cancer 2009; 124: 2294-2302.
37. Bharadwaj S, Thanawala R, Bon G, Falcioni R, Prasad GL. Resensitization of breast cancer cells to anoikis by tropomyosin-1: role of Rho kinase-dependent cytoskeleton and adhesion. Oncogene 2005; 24: 8291-8303.
38. Greer P. Closing in on the biological functions of Fps/Fes and Fer. Nat Rev Mol Cell Biol 2002; 3: 278-289.
39. MacGrath SM, Koleske AJ. Cortactin in cell migration and cancer at a glance. J Cell Sci 2012; 125: 1621-1626.
40. Sung BH, Zhu X, Kaverina I, Weaver AM. Cortactin controls cell motility and lamellipodial dynamics by regulating ECM secretion. Curr Biol 2011; 21: 1460-1469.
41. Caswell PT, Chan M, Lindsay AJ, McCaffrey MW, Boettiger D, Norman JC. Rab-coupling protein coordinates recycling of alpha5beta1 integrin and EGFR1 to promote cell migration in 3D microenvironments. J Cell Biol 2008; 183: 143-155.
42. Mills GB, Jurisica I, Yarden Y, Norman JC. Genomic amplicons target vesicle recycling in breast cancer. J Clin Invest 2009; 119: 2123-2127.
43. Fei F, Kweon SM, Haataja L, De Sepulveda P, Groffen J, Heisterkamp N. The Fer tyrosine kinase regulates interactions of Rho GDP-dissociation inhibitor alpha with the small GTPase Rac. BMC Biochem 2010; 11: 48.
44. Sander EE, ten Klooster JP, van Delft S, van der Kammen RA, Collard JG. Rac downregulates Rho activity: reciprocal balance between both GTPases determines cellular morphology and migratory behavior. J Cell Biol 1999; 147: 1009-1022.
45. Santner SJ, Dawson PJ, Tait L, Soule HD, Eliason J, Mohamed AN et al. Malignant MCF10CA1 cell lines derived from premalignant human breast epithelial MCF10AT cells. Breast Cancer Res Treat 2001; 65: 101-110.
46. Wetterwald A, van der Pluijm G, Que I, Sijmons B, Buijs J, Karperien M et al. Optical imaging of cancer metastasis to bone marrow: a mouse model of minimal residual disease. Am J Pathol 2002; 160: 1143-1153.
47. Craig AW, Zirngibl R, Williams K, Cole LA, Greer PA. Mice devoid of fer proteintyrosine kinase activity are viable and fertile but display reduced cortactin phosphorylation. Mol Cell Biol 2001; 21: 603-613.
48. Schackmann RC, van Amersfoort M, Haarhuis JH, Vlug EJ, Halim VA, Roodhart JM et al. Cytosolic p120-catenin regulates growth of metastatic lobular carcinoma through Rock1-mediated anoikis resistance. J Clin Invest 2011; 121: 3176-3188.
49. Ivanova IA, D0Souza SJ, Dagnino L. E2F1 stability is regulated by a novel-PKC/ p38beta MAP kinase signaling pathway during keratinocyte differentiation. Oncogene 2006; 25: 430-437.
50. Vespa A, D'Souza SJ, Dagnino L. A novel role for integrin-linked kinase in epithelial sheet morphogenesis. Mol Biol Cell 2005; 16: 4084-4095.
51. Danen EH, Sonneveld P, Brakebusch C, Fassler R, Sonnenberg A. The fibronectinbinding integrins alpha5beta1 and alphavbeta3 differentially modulate RhoA-GTP loading, organization of cell matrix adhesions, and fibronectin fibrillogenesis. J Cell Biol 2002; 159: 1071-1086.
52. Vermeulen JF, van de Ven RA, Ercan C, van der Groep P, van der Wall E, Bult P et al. Nuclear kaiso expression is associated with high grade and triple-negative invasive breast cancer. PLoS One 2012; 7: e37864.
53. Hoefnagel LD, van de Vijver MJ, van Slooten HJ, Wesseling P, Wesseling J, Westenend PJ et al. Receptor conversion in distant breast cancer metastases. Breast Cancer Res 2010; 12: R75.
54. van Diest PJ. No consent should be needed for using leftover body material for scientific purposes. BMJ 2002; 325: 648-651.