Upregulation of Eps8 in oral squamous cell carcinoma promotes cell migration and invasion through integrin-dependent Rac1 activation

Oncogene

Volumn 28, Issue 27, 2009, Pages 2524-2534

  Yap, L F ^a,b   Jenei, V ^c,d   Robinson, C M ^e   Moutasim, K ^c,d   Benn, T M ^a   Threadgold, S P ^a   Lopes, V ^f   Wei, W ^g   Thomas, G J ^c,d   Paterson, I C ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

^b CANCER RESEARCH INITIATIVES FOUNDATION   (Malaysia)

^c QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^d UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^e NEWCASTLE UNIVERSITY   (United Kingdom)

^f UNIVERSITY OF EDINBURGH   (United Kingdom)

^g UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

Eps8; Integrin; Invasion; Migration; Oral cancer; Rac1

Indexed keywords

ALPHAVBETA1 INTEGRIN; ALPHAVBETA6 INTEGRIN; GUANOSINE TRIPHOSPHATASE; INTEGRIN; RAC1 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELL INVASION; CELL MIGRATION; CELL MOTILITY; CELL PROLIFERATION; CELL SPREADING; CELLULAR DISTRIBUTION; CONTROLLED STUDY; EPS8 GENE; GENE EXPRESSION; GENE FUNCTION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; KERATINOCYTE; LYMPH NODE METASTASIS; MOUTH CARCINOMA; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SQUAMOUS CELL CARCINOMA; TUMOR GENE; UPREGULATION; WESTERN BLOTTING;

ANTIGENS, NEOPLASM; BLOTTING, WESTERN; CARCINOMA, SQUAMOUS CELL; CELL LINE, TUMOR; CELL MEMBRANE; CELL MOVEMENT; CELLS, CULTURED; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IMMUNOHISTOCHEMISTRY; INTEGRINS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; KERATINOCYTES; MOUTH MUCOSA; MOUTH NEOPLASMS; NEOPLASM INVASIVENESS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RAC1 GTP-BINDING PROTEIN; RECEPTORS, VITRONECTIN; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; UP-REGULATION;

EID: 67650423992     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2009.105     Document Type: Article

References (38)

1. Alevizos I, Mahadevappa M, Zhang X, Ohyama H, Kohno Y, Posner M et al. (2001). Oral cancer in vivo gene expression profiling assisted by laser capture microdissection and microarray analysis. Oncogene 20: 6196-6204.
2. Al Moustafa AE, Alaoui-Jamali MA, Batist G, Hernandez-Perez M, Serruya C, Alpert L et al. (2002). Identification of genes associated withhead and neck carcinogenesis by cDNA microarray comparison between matched primary normal epithelial and squamous carcinoma cells. Oncogene 21: 2634-2640.
3. Bates RC, Bellovin DI, Brown C, Maynard E, Wu B, Kawakatsu H et al. (2005). Transcriptional activation of integrin b6 during the epithelial-mesenchymal transition defines a novel prognostic indicator of aggressive colon carcinoma. J Clin Invest 115: 339-347.
4. Croce A, Cassata G, Disanza A, Gagliani MC, Tacchetti C, Malabarba MG et al. (2004). A novel actin barbed-end-capping activity in EPS-8 regulates apical morphogenesis in intestinal cells of Caenorhabditis elegans. Nat Cell Biol 6: 1173-1179.
5. Cromer A, Carles A, Millon R, Ganguli G, Chalmel F, Lemaire F et al. (2004). Identification of genes associated withtumorigenesis and metastatic potential of hypopharyngeal cancer by microarray analysis. Oncogene 23: 2484-2498.
6. del Pozo MA, Price LS, Alderson NB, Ren XD, Schwartz MA. (2000). Adhesion to the extracellular matrix regulates the coupling of the small GTPase Rac to its effector PAK. EMBO J 19: 2008-2014.
7. del Pozo MA, Alderson NB, Kiosses WB, Chiang HH, Anderson RG, Schwartz MA. (2004). Integrins regulate Rac targeting by internalization of membrane domains. Science 303: 839-842.
8. Disanza A, Carlier MF, Stradal TE, Didry D, Frittoli E, Confalonieri S et al. (2004). Eps8 controls actin-based motility by capping the barbed ends of actin filaments. Nat Cell Biol 6: 1180-1188.
9. Dormond O, Foletti A, Paroz C, Ruegg C. (2001). NSAIDS inhibit αvβ3 integrin-mediated and Cdc/Rac-dependent endothelial-cell spreading, migration and angiogenesis. Nat Med 7: 1041-1047.
10. Elayadi AN, Samli KN, Prudkin L, Liu YH, Bian A, Xie XJ et al. (2007). A peptide selected by biopanning identifies the integrin αvβ6 as a prognostic biomarker for non-small cell lung cancer. Cancer Res 67: 5889-5895.
11. Fazioli F, Minichiello L, Matoska V, Castagnino P, Miki T, Wong WT et al. (1993). Eps8, a substrate for the epidermal growth factor receptor kinase, enhances EGF-dependent mitogenic signals. EMBO J 12: 3799-3808.
12. Funato Y, Terabayashi T, Suenaga N, Seiki M, Takenawa T, Miki H. (2004). IRSp53/Eps8 complex is important for positive regulation of Rac and cancer cell motility/invasiveness. Cancer Res 64: 5237-5244.
13. Innocenti M, Frittoli E, Ponzanelli I, Falck JR, Brachmann SM, Di Fiore PP et al. (2003). Phosphoinositide 3-kinase activates Rac by entering in a complex with Eps8, Abi1, and Sos-1. J Cell Biol 160: 17-23.
14. Inobe M, Katsube K, Miyagoe Y, Nabeshima Y, Takeda S. (1999). Identification of EPS8 as a Dvl1-associated molecule. Biochem Biophys Res Commun 266: 216-221.
15. Irizarry RA, Bolstad BM, Collin F, Cope LM, Hobbs B, Speed TP. (2003). Summaries of Affymetrix Gene Chip probe level data. Nucleic Acids Res 31: e15.
16. Jeon GA, Lee JS, Patel V, Gutkind JS, Thorgeirsson SS, Kim EC et al. (2004). Global gene expression profiles of human head and neck squamous carcinoma cell lines. Int J Cancer 112: 249-258.
17. Kim M, Califano J. (2004). Molecular Pathology of Head and Neck Cancer. Int J Cancer 112: 545-553.
18. Maa MC, Hsieh CY, Leu TH. (2001). Overexpression of p97Eps8 leads to cellular transformation: implication of pleckstrin homology domain in p97Eps8-mediated ERK activation. Oncogene 20: 106-112.
19. Maa MC, Lee JC, Chen YJ, Chen YJ, Lee YC, Wang ST et al. (2007). EPS8 facilitates cellular growthand motility of colon cancer cells by increasing the expression and activity of focal adhesion kinase. J Biol Chem 282: 19399-19409.
20. Marsh D, Dickinson S, Neill GW, Marshall JF, Hart IR, Thomas GJ. (2008). alphavbeta6 integrin promotes invasion of morphoeic basal cell carcinoma through stromal modulation. Cancer Res 68: 3295-3303.
21. Matoskova B, Wong WT, Salcini AE, Pelicci PG, Di Fiore PP. (1995). Constitutive phosphorylation of Eps8 in tumor cell lines: relevance to malignant transformation. Mol Cell Biol 15: 3805-3812.
22. Miki H, Yamaguchi H, Suetsugu S, Takenawa T. (2000). IRSp53 is an essential intermediate between Rac and WAVE in the regulation of membrane ruffling. Nature 408: 732-735.
23. Myers JN, Greenberg JS, Mo V, Roberts D. (2001). Extracapsular spread. A significant predictor of treatment failure in patients with squamous cell carcinoma of the tongue. Cancer 92: 3030-3036.
24. Nystrom ML, Thomas GJ, Hart IR, Stone M, McKenzie IC, Marshall JF. (2005). Development of a quantitative method to analyse tumor cell invasion in organotypic culture. J Pathol 205: 468-475.
25. Nystrom ML, McCulloch D, Weinreb PH, Violette SM, Speight PM, Marshall JF et al. (2006). Cyclooxygenase-2 inhibition suppresses alphavbeta6 integrin-dependent oral squamous carcinoma invasion. Cancer Res 66: 10833-41082.
26. Parkin DM, Bray F, Ferlay J, Pisani P. (2005). Global cancer statistics 2002. CA Cancer J Clin 55: 74-108.
27. Prime SS, Nixon SV, Crane IJ, Stone A, Matthews JB, Maitland NJ et al. (1990). The behaviour of human oral squamous cell carcinoma in cell culture. J Pathol 160: 259-269.
28. Scita G, Nordstrom J, Carbone R, Tenca P, Giardina G, Gutkind S et al. (1999). EPS8 and E3B1 transduce signals from Ras to Rac. Nature 401: 290-293.
29. Scita G, Tenca P, Areces LB, Tocchetti A, Frittoli E, Giardina G et al. (2001). An effector region in Eps8 is responsible for the activation of the Rac-specific GEF activity of Sos-1 and for the proper localization of the Rac-based actin-polymerizing machine. J Cell Biol 154: 1031-1044.
30. Ramsay AG, Keppler MD, Jazayeri M, Thomas GJ, Parsons M, Violette S et al. (2007). HS1-associated protein X-1 regulates carcinoma cell migration and invasion via clathrin-mediated endocytosis of integrin alphavbeta6. Cancer Res 67: 5275-5284.
31. Thirthagiri E, Robinson CM, Huntley S, Davies M, Yap LF, Prime SS et al. (2007). Spindle assembly checkpoint and centrosome abnormalities in oral cancer. Cancer Lett 258: 276-285.
32. Thomas GJ, Hart IR, Speight PM, Marshall JF. (2002). Binding of TGF-beta1 latency-associated peptide (LAP) to alpha(v)beta6 integrin modulates behaviour of squamous carcinoma cells. Br J Cancer 87: 859-867.
33. Thomas GJ, Lewis MP, Hart IR, Marshall JF, Speight PM. (2001). AlphaVbeta6 integrin promotes invasion of squamous carcinoma cells through up-regulation of matrix metalloproteinase-9. Int J Cancer 92: 641-650.
34. Tusher VG, Tibshirani R, Chu G. (2001). Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA 98: 5116-5121.
35. Welsch T, Endlich K, Giese T, Buchler MW, Schmidt J. (2007). Eps8 is increased in pancreatic cancer and required for dynamic actin-based cell protrusions and intercellular cytoskeletal organization. Cancer Lett 255: 205-218.
36. Woolgar JA, Rogers SN, Lowe D, Brown JS, Vaughan ED. (2003). Cervical lymphnode metastasis in oral cancer: the importance of even microscopic extracapsular spread. Oral Oncol 39: 130-137.
37. Yao J, Weremowicz S, Feng B, Gentleman RC, Marks JR, Gelman R et al. (2006). Combined cDNA array comparative genomic hybridization and serial analysis of gene expression analysis of breast tumor progression. Cancer Res 66: 4065-4078.
38. Yeudall WA, Miyazaki H, Ensley JF, Cardinali M, Gutkind JS, Patel V. (2005). Uncoupling of epidermal growthfactor-dependent proliferation and invasion in a model of squamous carcinoma progression. Oral Oncol 41: 698-708.