E-cadherin directly contributes to PI3K/AKT activation by engaging the PI3K-p85 regulatory subunit to adherens junctions of ovarian carcinoma cells

Oncogene

Volumn 28, Issue 9, 2009, Pages 1206-1217

  De Santis, G ^a   Miotti, S ^a   Mazzi, M ^a   Canevari, S ^a   Tomassetti, A ^a  

^a NATIONAL CANCER INSTITUTE   (Italy)

Author keywords

Cell cell adhesion; E cadherin; Ovarian carcinoma; PI3K

Indexed keywords

BETA CATENIN; CALCIUM; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; PROTEIN P85; PROTEIN SUBUNIT; UVOMORULIN;

ARTICLE; CALCIUM ABSORPTION; CARCINOMA CELL; CELL ADHESION; CELL CYCLE PROGRESSION; CELL FUNCTION; CELL INTERACTION; CELL JUNCTION; CELL PROLIFERATION; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN CELL; OVARY CARCINOMA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ADHERENS JUNCTIONS; CADHERINS; CALCIUM; CELL ADHESION; CELL LINE, TUMOR; ENZYME ACTIVATION; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; GENE KNOCKDOWN TECHNIQUES; HUMANS; IMMUNOHISTOCHEMISTRY; OVARIAN NEOPLASMS; PROTO-ONCOGENE PROTEINS C-AKT; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION;

EID: 62049085785     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2008.470     Document Type: Article

References (43)

1. Ahmed N, Thompson EW, Quinn MA. (2007). Epithelial-mesenchymal interconversions in normal ovarian surface epithelium and ovarian carcinomas: an exception to the norm. J Cell Physiol 213: 581-588.
2. Amzel LM, Huang CH, Mandelker D, Lengauer C, Gabelli SB, Vogelstein B. (2008). Structural comparisons of class I phosphoinositide 3-kinases. Nat Rev Cancer 8: 665-669.
3. Anderson CB, Neufeld KL, White RL. (2002). Subcellular distribution of Wnt pathway proteins in normal and neoplastic colon. Proc Natl Acad Sci USA 99: 8683-8688.
4. Andl CD, Rustgi AK. (2005). No one-way street: cross-talk between e-cadherin and receptor tyrosine kinase (RTK) signaling: a mechanism to regulate RTK activity. Cancer Biol Ther 4: 28-31.
5. Aunoble B, Sanches R, Didier E, Bignon YJ. (2000). Major oncogenes and tumor suppressor genes involved in epithelial ovarian cancer (review). Int J Oncol 16: 567-576.
6. Brugge J, Hung MC, Mills GB. (2007). A new mutational AKTivation in the PI3K pathway. Cancer Cell 12: 104-107.
7. Calautti E, Li J, Saoncella S, Brissette J, Goetinck P. (2005). Phosphoinositide 3-kinase signaling to Akt promotes keratinocyte differentiation versus death. J Biol Chem 280: 32856-32865.
8. Campbell IG, Russell SE, Choong DY, Montgomery KG, Ciavarella ML, Hooi CS et al. (2004). Mutation of the PIK3CA gene in ovarian and breast cancer. Cancer Res 64: 7678-7681.
9. Carneiro F, Oliveira C, Suriano G, Seruca R. (2008). Molecular pathology of familial gastric cancer, with an emphasis on hereditary diffuse gastric cancer. J Clin Pathol 61: 25-30.
10. Castellano G, Reid JF, Alberti P, Carcangiu ML, Tomassetti A, Canevari S. (2006). New potential ligand-receptor signaling loops in ovarian cancer identified in multiple gene expression studies. Cancer Res 66: 10709-10719.
11. Conacci-Sorrell M, Simcha I, Ben Yedidia T, Blechman J, Savagner P, Ben Ze'ev A. (2003). Autoregulation of E-cadherin expression by cadherin-cadherin interactions: the roles of β-catenin. J Cell Biol 163: 847-857.
12. Davies BR, Worsley SD, Ponder BA. (1998). Expression of E-cadherin, alpha-catenin and beta-catenin in normal ovarian surface epithelium and epithelial ovarian cancers. Histopathology 32: 69-80.
13. Herzig M, Savarese F, Novatchkova M, Semb H, Christofori G. (2006). Tumor progression induced by the loss of E-cadherin independent of beta-catenin/Tcf-mediated Wnt signaling. Oncogene 26: 2290-2298.
14. Himanen JP, Saha N, Nikolov DB. (2007). Cell-cell signaling via Eph receptors and ephrins. Curr Opin Cell Biol 19: 534-542.
15. Kovacs EM, Ali RG, McCormack AJ, Yap AS. (2002). E-cadherin homophilic ligation directly signals through Rac and phosphatidylinositol 3-kinase to regulate adhesive contacts. J Biol Chem 277: 6708-6718.
16. Levine DA, Bogomolniy F, Yee CJ, Lash A, Barakat RR, Borgen PI et al. (2005). Frequent mutation of the PIK3CA gene in ovarian and breast cancers. Clin Cancer Res 11: 2875-2878.
17. Marques FR, Fonsechi-Carvasan GA, Angelo Andrade LA, Bottcher-Luiz F. (2004). Immunohistochemical patterns for alpha- and beta-catenin, E- and N-cadherin expression in ovarian epithelial tumors. Gynecol Oncol 94: 16-24.
18. McLachlan RW, Kraemer A, Helwani FM, Kovacs EM, Yap AS. (2007). E-cadherin adhesion activates c-Src signaling at cell-cell contacts. Mol Biol Cell 18: 3214-3223.
19. McLachlan RW, Yap AS. (2007). Not so simple: the complexity of phosphotyrosine signaling at cadherin adhesive contacts. J Mol Med 85: 545-554.
20. Miotti S, Tomassetti A, Facetti I, Sanna E, Berno V, Canevari S. (2005). Simultaneous expression of caveolin-1 and E-cadherin in ovarian carcinoma cells stabilizes adherens junctions through inhibition of src-related kinases. Am J Pathol 167: 1411-1427.
21. Niessen CM, Gottardi CJ. (2008). Molecular components of the adherens junction. Biochim Biophys Acta 1778: 562-571.
22. Pang JH, Kraemer A, Stehbens SJ, Frame MC, Yap AS. (2005). Recruitment of phosphoinositide 3-kinase defines a positive contribution of tyrosine kinase signaling to E-cadherin function. J Biol Chem 280: 3043-3050.
23. Pece S, Chiariello M, Murga C, Gutkind JS. (1999). Activation of the protein kinase Akt/PKB by the formation of E-cadherin-mediated cell-cell junctions. Evidence for the association of phosphatidylinositol 3-kinase with the E-cadherin adhesion complex. J Biol Chem 274: 19347-19351.
24. Qian X, Karpova T, Sheppard AM, McNally J, Lowy DR. (2004). E-cadherin-mediated adhesion inhibits ligand-dependent activation of diverse receptor tyrosine kinases. EMBO J 23: 1739-1748.
25. Reddy P, Liu L, Ren C, Lindgren P, Boman K, Shen Y et al. (2005). Formation of E-cadherin-mediated cell-cell adhesion activates AKT and mitogen activated protein kinase via phosphatidylinositol 3 kinase and ligand-independent activation of epidermal growth factor receptor in ovarian cancer cells. Mol Endocrinol 19: 2564-2578.
26. Samuels Y, Diaz Jr LA, Schmidt-Kittler O, Cummins JM, Delong L, Cheong I et al. (2005). Mutant PIK3CA promotes cell growth and invasion of human cancer cells. Cancer Cell 7: 561-573.
27. Samuels Y, Wang Z, Bardelli A, Silliman N, Ptak J, Szabo S et al. (2004). High frequency of mutations of the PIK3CA gene in human cancers. Science 304: 554.
28. Sanna E, Miotti S, Mazzi M, De Santis G, Canevari S, Tomassetti A. (2007). Binding of nuclear caveolin-1 to promoter elements of growth-associated genes in ovarian carcinoma cells. Exp Cell Res 313: 1307-1317.
29. Seidel B, Braeg S, Adler G, Wedlich D, Menke A. (2004). E- and N-cadherin differ with respect to their associated p120ctn isoforms and their ability to suppress invasive growth in pancreatic cancer cells. Oncogene 23: 5532-5542.
30. Sundfeldt K. (2003). Cell-cell adhesion in the normal ovary and ovarian tumors of epithelial origin; an exception to the rule. Mol Cell Endocrinol 202: 89-96.
31. Tomassetti A, De Santis G, Castellano G, Miotti S, Mazzi M, Tomasoni D et al. (2008). Variant HNF1 modulates epithelial plasticity of normal and transformed ovary cells. Neoplasia 10: 1481-1492.
32. van Hengel J, Van Roy F. (2007). Diverse functions of p120ctn in tumors. Biochim Biophys Acta 1773: 78-88.
33. Van Roy F, Berx G. (2008). The cell-cell adhesion molecule E-cadherin. Cell Mol Life Sci 65: 3756-3788.
34. Virnekas B, Ge L, Pluckthun A, Schneider KC, Wellnhofer G, Moroney SE. (1994). Trinucleotide phosphoramidites: ideal reagents for the synthesis of mixed oligonucleotides for random mutagenesis. Nucleic Acids Res 22: 5600-5607.
35. Vivanco I, Sawyers CL. (2002). The phosphatidylinositol 3-Kinase AKT pathway in human cancer. Nat Rev Cancer 2: 489-501.
36. Vogt PK, Kang S, Elsliger MA, Gymnopoulos M. (2007). Cancer-specific mutations in phosphatidylinositol 3-kinase. Trends Biochem Sci 32: 342-349.
37. Wang Y, Helland A, Holm R, Kristensen GB, Borresen-Dale AL. (2005). PIK3CA mutations in advanced ovarian carcinomas. Hum Mutat 25: 322.
38. Woenckhaus J, Steger K, Sturm K, Munstedt K, Franke FE, Fenic I. (2007). Prognostic value of PIK3CA and phosphorylated AKT expression in ovarian cancer. Virchows Arch 450: 387-395.
39. Wong AS, Gumbiner BM. (2003). Adhesion-independent mechanism for suppression of tumor cell invasion by E-cadherin. J Cell Biol 161: 1191-1203.
40. Woodfield RJ, Hodgkin MN, Akhtar N, Morse MA, Fuller KJ, Saqib K et al. (2001). The p85 subunit of phosphoinositide 3-kinase is associated with beta-catenin in the cadherin-based adhesion complex. Biochem J 360: 335-344.
41. Xie Z, Bikle DD. (2007). The recruitment of phosphatidylinositol 3-kinase to the E-cadherin-catenin complex at the plasma membrane is required for calcium-induced phospholipase C-gamma1 activation and human keratinocyte differentiation. J Biol Chem 282: 8695-8703.
42. Yap AS, Crampton MS, Hardin J. (2007). Making and breaking contacts: the cellular biology of cadherin regulation. Curr Opin Cell Biol 19: 508-514.
43. Zhang L, Huang J, Yang N, Greshock J, Liang S, Hasegawa K et al. (2007). Integrative genomic analysis of phosphatidylinositol 3′-kinase family identifies PIK3R3 as a potential therapeutic target in epithelial ovarian cancer. Clin Cancer Res 13: 5314-5321.