Human enhancer of filamentation 1-induced colorectal cancer cell migration: Role of serine phosphorylation and interaction with the breast cancer anti-estrogen resistance 3 protein

International Journal of Biochemistry and Cell Biology

Volumn 64, Issue , 2015, Pages 45-57

  Ibrahim, Rama ^a,b   Lemoine, Antoinette ^c   Bertoglio, Jacques ^a   Raingeaud, Joël ^a  

^a INSTITUT GUSTAVE ROUSSY   (France)

^b Department of Biochemistry and Microbiology Faculty of Pharmacy Tichrine University   (Syrian Arab Republic)

^c UNIVERSITÉ PARIS SACLAY   (France)

Author keywords

BCAR3; Colorectal cancer; Focal adhesion kinase; Nedd9; Phosphorylation

Indexed keywords

ADAPTOR PROTEIN; BIOLOGICAL MARKER; BREAST CANCER ANTIESTROGEN RESISTANCE 3; CRK ASSOCIATED SUBSTRATE PROTEIN; DOCKING PROTEIN; FOCAL ADHESION KINASE; HUMAN ENHANCER OF FILAMENTATION 1; MESSENGER RNA; PROTEIN TYROSINE KINASE; UNCLASSIFIED DRUG; BCAR3 PROTEIN, HUMAN; NEDD9 PROTEIN, HUMAN; PHOSPHOPROTEIN; SIGNAL TRANSDUCING ADAPTOR PROTEIN;

AMINO ACID SUBSTITUTION; ARTICLE; CACO 2 CELL LINE; CELL MIGRATION; CELL MOTILITY; CELL PROLIFERATION; COLORECTAL CANCER CELL LINE; COLORECTAL CARCINOMA; GENE MUTATION; GENE OVEREXPRESSION; HCT116 CELL LINE; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; TUMOR GROWTH; UPREGULATION; CELL MOTION; HUMAN; PHOSPHORYLATION; PHYSIOLOGY;

CITRUS MACROPHYLLA;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; CELL MOVEMENT; HCT116 CELLS; HUMANS; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL;

EID: 84926475235     PISSN: 13572725     EISSN: 18785875     Source Type: Journal    
DOI: 10.1016/j.biocel.2015.03.014     Document Type: Article

References (55)

1. R. Abu-Ghazaleh, J. Kabir, H. Jia, M. Lobo, and I. Zachary Src mediates stimulation by vascular endothelial growth factor of the phosphorylation of focal adhesion kinase at tyrosine 861, and migration and anti-apoptosis in endothelial cells Biochem J 360 2001 255 264
2. J. Bain, L. Plater, M. Elliott, N. Shpiro, C.J. Hastie, and H. McLauchlan The selectivity of protein kinase inhibitors: a further update Biochem J 408 2007 297 315
3. P. Bradbury, M. Mahmassani, J. Zhong, K. Turner, A. Paul, and N.M. Verrills PP2A phosphatase suppresses function of the mesenchymal invasion regulator NEDD9 Biochim Biophys Acta 1823 2012 290 297
4. C.D. Browne, M.M. Hoefer, S.K. Chintalapati, M.H. Cato, Y. Wallez, and D.V. Ostertag SHEP1 partners with CasL to promote marginal zone B-cell maturation Proc Natl Acad Sci U S A 107 2010 18944 18949
5. V.G. Brunton, E. Avizienyte, V.J. Fincham, B. Serrels, C.A. Metcalf 3rd., and T.K. Sawyer Identification of Src-specific phosphorylation site on focal adhesion kinase: dissection of the role of Src SH2 and catalytic functions and their consequences for tumor cell behavior Cancer Res 65 2005 1335 1342
6. T.B. Deramaudt, D. Dujardin, A. Hamadi, F. Noulet, K. Kolli, and J. De Mey FAK phosphorylation at Tyr-925 regulates cross-talk between focal adhesion turnover and cell protrusion Mol Biol Cell 22 2011 964 975
7. S.J. Fashena, M.B. Einarson, G.M. O'Neill, C. Patriotis, and E.A. Golemis Dissection of HEF1-dependent functions in motility and transcriptional regulation J Cell Sci 115 2002 99 111
8. L. Feng, S. Guedes, and T. Wang Atrophin-1-interacting protein 4/human Itch is a ubiquitin E3 ligase for human enhancer of filamentation 1 in transforming growth factor-beta signaling pathways J Biol Chem 279 2004 29681 29690
9. M.L. Garron, D. Arsenieva, J. Zhong, A.B. Bloom, A. Lerner, and G.M. O'Neill Structural insights into the association between BCAR3 and Cas family members, an atypical complex implicated in anti-oestrogen resistance J Mol Biol 386 2009 190 203
10. M.S. Guerrero, J.T. Parsons, and A.H. Bouton Cas and NEDD9 contribute to tumor progression through dynamic regulation of the cytoskeleton Genes Cancer 3 2012 371 381
11. V. Hivert, J. Pierre, and J. Raingeaud Phosphorylation of human enhancer of filamentation (HEF1) on serine 369 induces its proteasomal degradation Biochem Pharmacol 78 2009 1017 1025
12. E. Izumchenko, M.K. Singh, O.V. Plotnikova, N. Tikhmyanova, J.L. Little, and I.G. Serebriiskii NEDD9 promotes oncogenic signaling in mammary tumor development Cancer Res 69 2009 7198 7206
13. H. Ji, M.R. Ramsey, D.N. Hayes, C. Fan, K. McNamara, and P. Kozlowski LKB1 modulates lung cancer differentiation and metastasis Nature 448 2007 807 810
14. Y. Jin, F. Li, C. Zheng, Y. Wang, Z. Fang, and C. Guo NEDD9 promotes lung cancer metastasis through epithelial-mesenchymal transition Int J Cancer 134 2014 2294 2304
15. M. Kim, J.D. Gans, C. Nogueira, A. Wang, J.H. Paik, and B. Feng Comparative oncogenomics identifies NEDD9 as a melanoma metastasis gene Cell 125 2006 1269 1281
16. S.H. Kim, D. Xia, S.W. Kim, V. Holla, D.G. Menter, and R.N. Dubois Human enhancer of filamentation 1 Is a mediator of hypoxia-inducible factor-1alpha-mediated migration in colorectal carcinoma cells Cancer Res 70 2010 4054 4063
17. S. Kondo, S. Iwata, T. Yamada, Y. Inoue, H. Ichihara, and Y. Kichikawa Impact of the integrin signaling adaptor protein NEDD9 on prognosis and metastatic behavior of human lung cancer Clin Cancer Res 18 2012 6326 6338
18. C. Kong, C. Wang, L. Wang, M. Ma, C. Niu, and X. Sun NEDD9 is a positive regulator of epithelial-mesenchymal transition and promotes invasion in aggressive breast cancer PLoS ONE 6 2011 e22666
19. S.F. Law, J. Estojak, B. Wang, T. Mysliwiec, G. Kruh, and E.A. Golemis Human enhancer of filamentation 1, a novel p130cas-like docking protein, associates with focal adhesion kinase and induces pseudohyphal growth in Saccharomyces cerevisiae Mol Cell Biol 16 1996 3327 3337
20. T.H. Leu, and M.C. Maa Tyr-863 phosphorylation enhances focal adhesion kinase autophosphorylation at Tyr-397 Oncogene 21 2002 6992 7000
21. Y. Li, J.H. Bavarva, Z. Wang, J. Guo, C. Qian, and S.N. Thibodeau HEF1, a novel target of Wnt signaling, promotes colonic cell migration and cancer progression Oncogene 30 2011 2633 2643
22. Y. Lim, I. Han, J. Jeon, H. Park, Y.Y. Bahk, and E.S. Oh Phosphorylation of focal adhesion kinase at tyrosine 861 is crucial for Ras transformation of fibroblasts J Biol Chem 279 2004 29060 29065
23. J.L. Little, V. Serzhanova, E. Izumchenko, B.L. Egleston, E. Parise, and A.J. Klein-Szanto A requirement for Nedd9 in luminal progenitor cells prior to mammary tumorigenesis in MMTV-HER2/ErbB2 mice Oncogene 2013
24. X. Liu, A.E. Elia, S.F. Law, E.A. Golemis, J. Farley, and T. Wang A novel ability of Smad3 to regulate proteasomal degradation of a Cas family member HEF1 EMBO J 19 2000 6759 6769
25. J.T. Lucas Jr., B.P. Salimath, M.G. Slomiany, and S.A. Rosenzweig Regulation of invasive behavior by vascular endothelial growth factor is HEF1-dependent Oncogene 29 2010 4449 4459
26. A. Makkinje, R.I. Near, G. Infusini, P. Vanden Borre, A. Bloom, and D. Cai AND-34/BCAR3 regulates adhesion-dependent p130Cas serine phosphorylation and breast cancer cell growth pattern Cell Signal 21 2009 1423 1435
27. A. Makkinje, P. Vanden Borre, R.I. Near, P.S. Patel, and A. Lerner Breast cancer anti-estrogen resistance 3 (BCAR3) protein augments binding of the c-Src SH3 domain to Crk-associated substrate (p130cas) J Biol Chem 287 2012 27703 27714
28. S.N. Manie, A.R. Beck, A. Astier, S.F. Law, T. Canty, and H. Hirai Involvement of p130(Cas) and p105(HEF1), a novel Cas-like docking protein, in a cytoskeleton-dependent signaling pathway initiated by ligation of integrin or antigen receptor on human B cells J Biol Chem 272 1997 4230 4236
29. A.J. Minn, G.P. Gupta, P.M. Siegel, P.D. Bos, W. Shu, and D.D. Giri Genes that mediate breast cancer metastasis to lung Nature 436 2005 518 524
30. S.K. Mitra, and D.D. Schlaepfer Integrin-regulated FAK-Src signaling in normal and cancer cells Curr Opin Cell Biol 18 2006 516 523
31. K. Nakamura, H. Yano, E. Schaefer, and H. Sabe Different modes and qualities of tyrosine phosphorylation of Fak and Pyk2 during epithelial-mesenchymal transdifferentiation and cell migration: analysis of specific phosphorylation events using site-directed antibodies Oncogene 20 2001 2626 2635
32. L. Naldini, U. Blomer, P. Gallay, D. Ory, R. Mulligan, and F.H. Gage In vivo gene delivery and stable transduction of nondividing cells by a lentiviral vector Science 272 1996 263 267
33. M. Natarajan, J.E. Stewart, E.A. Golemis, E.N. Pugacheva, K. Alexandropoulos, and B.D. Cox HEF1 is a necessary and specific downstream effector of FAK that promotes the migration of glioblastoma cells Oncogene 25 2006 1721 1732
34. C. Nourry, L. Maksumova, M. Pang, X. Liu, and T. Wang Direct interaction between Smad3, APC10, CDH1 and HEF1 in proteasomal degradation of HEF1 BMC Cell Biol 5 2004 20
35. G.M. O'Neill, S.J. Fashena, and E.A. Golemis Integrin signalling: a new Cas(t) of characters enters the stage Trends Cell Biol 10 2000 111 119
36. E.N. Pugacheva, and E.A. Golemis The focal adhesion scaffolding protein HEF1 regulates activation of the Aurora-A and Nek2 kinases at the centrosome Nat Cell Biol 7 2005 937 946
37. A.G. Regelmann, N.M. Danzl, C. Wanjalla, and K. Alexandropoulos The hematopoietic isoform of Cas-Hef1-associated signal transducer regulates chemokine-induced inside-out signaling and T cell trafficking Immunity 25 2006 907 918
38. R.B. Riggins, L.A. Quilliam, and A.H. Bouton Synergistic promotion of c-Src activation and cell migration by Cas and AND-34/BCAR3 J Biol Chem 278 2003 28264 28273
39. E. Saade, U. Mechold, A. Kulyyassov, D. Vertut, M. Lipinski, and V. Ogryzko Analysis of interaction partners of H4 histone by a new proteomics approach Proteomics 9 2009 4934 4943
40. V. Sanz-Moreno, G. Gadea, J. Ahn, H. Paterson, P. Marra, and S. Pinner Rac activation and inactivation control plasticity of tumor cell movement Cell 135 2008 510 523
41. D.D. Schlaepfer, and T. Hunter Evidence for in vivo phosphorylation of the Grb2 SH2-domain binding site on focal adhesion kinase by Src-family protein-tyrosine kinases Mol Cell Biol 16 1996 5623 5633
42. R.S. Schrecengost, R.B. Riggins, K.S. Thomas, M.S. Guerrero, and A.H. Bouton Breast cancer antiestrogen resistance-3 expression regulates breast cancer cell migration through promotion of p130Cas membrane localization and membrane ruffling Cancer Res 67 2007 6174 6182
43. N.R. Schuh, M.S. Guerrero, R.S. Schrecengost, and A.H. Bouton BCAR3 regulates Src/p130 Cas association, Src kinase activity, and breast cancer adhesion signaling J Biol Chem 285 2010 2309 2317
44. N. Sima, X. Cheng, F. Ye, D. Ma, X. Xie, and W. Lu The overexpression of scaffolding protein NEDD9 promotes migration and invasion in cervical cancer via tyrosine phosphorylated FAK and SRC PLoS ONE 8 2013 e74594
45. K.J. Simpson, L.M. Selfors, J. Bui, A. Reynolds, D. Leake, and A. Khvorova Identification of genes that regulate epithelial cell migration using an siRNA screening approach Nat Cell Biol 10 2008 1027 1038
46. M. Singh, L. Cowell, S. Seo, G. O'Neill, and E. Golemis Molecular basis for HEF1/NEDD9/Cas-L action as a multifunctional co-ordinator of invasion, apoptosis and cell cycle Cell Biochem Biophys 48 2007 54 72
47. M.K. Singh, E. Izumchenko, A.J. Klein-Szanto, B.L. Egleston, M. Wolfson, and E.A. Golemis Enhanced genetic instability and dasatinib sensitivity in mammary tumor cells lacking NEDD9 Cancer Res 70 2010 8907 8916
48. N. Tikhmyanova, and E.A. Golemis NEDD9 and BCAR1 negatively regulate E-cadherin membrane localization, and promote E-cadherin degradation PLoS ONE 6 2011 e22102
49. C. Tomkiewicz, L. Herry, L.C. Bui, C. Metayer, M. Bourdeloux, and R. Barouki The aryl hydrocarbon receptor regulates focal adhesion sites through a non-genomic FAK/Src pathway Oncogene 32 2013 1811 1820
50. P. Vanden Borre, R.I. Near, A. Makkinje, G. Mostoslavsky, and A. Lerner BCAR3/AND-34 can signal independent of complex formation with CAS family members or the presence of p130Cas Cell Signal 23 2011 1030 1040
51. Y. Wallez, P.D. Mace, E.B. Pasquale, and S.J. Riedl NSP-CAS protein complexes: emerging signaling modules in cancer Genes Cancer 3 2012 382 393
52. Y. Wallez, S.J. Riedl, and E.B. Pasquale Association of the breast cancer antiestrogen resistance protein 1 (BCAR1) and BCAR3 scaffolding proteins in cell signaling and antiestrogen resistance J Biol Chem 289 2014 10431 10444
53. D. Xia, V.R. Holla, D. Wang, D.G. Menter, and R.N. DuBois HEF1 is a crucial mediator of the proliferative effects of prostaglandin E(2) on colon cancer cells Cancer Res 70 2010 824 831
54. M. Zheng, and P.J. McKeown-Longo Regulation of HEF1 expression and phosphorylation by TGF-beta 1 and cell adhesion J Biol Chem 277 2002 39599 39608
55. M. Zheng, and P.J. McKeown-Longo Cell adhesion regulates Ser/Thr phosphorylation and proteasomal degradation of HEF1 J Cell Sci 119 2006 96 103