Copine-III interacts with ErbB2 and promotes tumor cell migration

Oncogene

Volumn 29, Issue 11, 2010, Pages 1598-1610

  Heinrich, C ^a   Keller, C ^a   Boulay, A ^a   Vecchi, M ^b   Bianchi, M ^b   Sack, R ^a   Lienhard, S ^a   Duss, S ^a   Hofsteenge, J ^a   Hynes, N E ^a  

^a FRIEDRICH MIESCHER INSTITUTE FOR BIOMEDICAL RESEARCH   (Switzerland)

^b FIRC INSTITUTE OF MOLECULAR ONCOLOGY   (Italy)

Author keywords

Cell migration; Copine III; ErbB2; FRET acceptor photobleaching; HRG; Quantitative mass spectrometry

Indexed keywords

COPINE III; EPIDERMAL GROWTH FACTOR RECEPTOR 2; FOCAL ADHESION KINASE; PHOSPHOLIPID BINDING PROTEIN; RECEPTOR FOR ACTIVATED C KINASE 1; UNCLASSIFIED DRUG;

ARTICLE; BREAST CANCER; BREAST TUMOR; CANCER CELL CULTURE; CARCINOGENESIS; CELL MIGRATION; CELL MOTILITY; CONTROLLED STUDY; CPNE3 GENE; GENE; HUMAN; HUMAN CELL; HUMAN TISSUE; OVARY ADENOCARCINOMA; OVARY TUMOR; PRIORITY JOURNAL; PROGNOSIS; PROSTATE CANCER; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTO ONCOGENE; TUMOR CELL;

BINDING SITES; BLOTTING, WESTERN; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL MOVEMENT; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MALE; MODELS, BIOLOGICAL; OVARIAN NEOPLASMS; PHOSPHOPROTEINS; PROSTATIC NEOPLASMS; PROTEIN BINDING; RECEPTOR, ERBB-2; RNA INTERFERENCE; TYROSINE;

EID: 77949657155     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2009.456     Document Type: Article

References (49)

1. Akiyama T, Matsuda S, Namba Y, Saito T, Toyoshima K, Yamamoto T. (1991). The transforming potential of the c-erbB-2 protein is regulated by its autophosphorylation at the carboxyl-terminal domain. Mol Cell Biol 11: 833-842.
2. Benes CH, Wu N, Elia AE, Dharia T, Cantley LC, Soltoff SP. (2005). The C2 domain of PKCdelta is a phosphotyrosine binding domain. Cell 121: 271-280.
3. Blagoev B, Kratchmarova I, Ong SE, Nielsen M, Foster LJ, Mann M. (2003). A proteomics strategy to elucidate functional protein-protein interactions applied to EGF signaling. Nat Biotechnol 21: 315-318.
4. Brunton VG, Avizienyte E, Fincham VJ, Serrels B, Metcalf 3rd CA, Sawyer TK, et al. (2005). Identification of Src-specific phosphoryla-tion 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: 1335-1342.
5. Church DL, Lambie EJ. (2003). The promotion of gonadal cell divisions by the Caenorhabditis elegans TRPM cation channel GON-2 is antagonized by GEM-4 copine. Genetics 165: 563-574.
6. Citri A, Yarden Y. (2006). EGF-ERBB signalling: towards the systems level. Nat Rev Mol Cell Biol 7: 505-516.
7. Cox EA, Bennin D, Doan AT, O'Toole T, Huttenlocher A. (2003). RACK1 regulates integrin-mediated adhesion, protrusion, and chemotactic cell migration via its Src-binding site. Mol Biol Cell 14: 658-669.
8. Creutz CE, Tomsig JL, Snyder SL, Gautier MC, Skouri F, Beisson J, et al. (1998). The copines, a novel class of C2 domain-containing, calcium-dependent, phospholipid-binding proteins conserved from Paramecium to humans. J Biol Chem 273: 1393-1402.
9. Dankort D, Maslikowski B, Warner N, Kanno N, Kim H, Wang Z, et al. (2001). Grb2 and Shc adapter proteins play distinct roles in Neu (ErbB-2)-induced mammary tumorigenesis: implications for human breast cancer. Mol Cell Biol 21: 1540-1551.
10. Dankort DL, Wang Z, Blackmore V, Moran MF, Muller WJ. (1997). Distinct tyrosine autophosphorylation sites negatively and positively modulate neu-mediated transformation. Mol Cell Biol 17: 5410-5425.
11. Farmer P, Bonnefoi H, Becette V, Tubiana-Hulin M, Fumoleau P, Larsimont D, et al. (2005). Identification of molecular apocrine breast tumours by microarray analysis. Oncogene 24: 4660-4671.
12. Gharbi S, Gaffney P, Yang A, Zvelebil MJ, Cramer R, Waterfield MD, et al. (2002). Evaluation of two-dimensional differential gel electrophoresis for proteomic expression analysis of a model breast cancer cell system. Mol Cell Proteomics 1: 91-98.
13. Gottschalk A, Almedom RB, Schedletzky T, Anderson SD, Yates 3rd JR, Schafer WR. (2005). Identification and characterization of novel nicotinic receptor-associated proteins in Caenorhabditis elegans. EMBO J 24: 2566-2578.
14. Graus-Porta D, Beerli RR, Daly JM, Hynes NE. (1997). ErbB-2, the preferred heterodimerization partner of all ErbB receptors, is a mediator of lateral signaling. EMBO J 16: 1647-1655.
15. Guerrero-Valero M, Marin-Vicente C, Gomez-Fernandez JC, Corba-lan-Garcia S. (2007). The C2 domains of classical PKCs are specific PtdIns(4,5)P2-sensing domains with different affinities for membrane binding. J Mol Biol 371: 608-621.
16. Hazan R, Margolis B, Dombalagian M, Ullrich A, Zilberstein A, Schlessinger J. (1990). Identification of autophosphorylation sites of HER2/neu. Cell Growth Differ 1: 3-7.
17. Hendrix ND, Wu R, Kuick R, Schwartz DR, Fearon ER, Cho KR. (2006). Fibroblast growth factor 9 has oncogenic activity and is a downstream target of Wnt signaling in ovarian endometrioid adenocarcinomas. Cancer Res 66: 1354-1362.
18. Holbro T, Beerli RR, Maurer F, Koziczak M, Barbas 3rd CF, Hynes NE. (2003). The ErbB2/ErbB3 heterodimer functions as an oncogenic unit: ErbB2 requires ErbB3 to drive breast tumor cell proliferation. Proc Natl Acad Sci USA 100: 8933-8938.
19. Holbro T, Hynes NE. (2004). ErbB receptors: directing key signaling networks throughout life. Annu Rev Pharmacol Toxicol 44: 195-217.
20. Hua J, Grisafi P, Cheng SH, Fink GR. (2001). Plant growth homeostasis is controlled by the Arabidopsis BON1 and BAP1 genes. Genes Dev 15: 2263-2272.
21. Hynes NE, Lane HA. (2005). ERBB receptors and cancer: the complexity of targeted inhibitors. Nat Rev Cancer 5: 341-354.
22. Keely PJ, Westwick JK, Whitehead IP, Der CJ, Parise LV. (1997). Cdc42 and Rac1 induce integrin-mediated cell motility and invasiveness through PI(3)K. Nature 390: 632-636.
23. Kenworthy AK. (2001). Imaging protein-protein interactions using fluorescence resonance energy transfer microscopy. Methods 24: 289-296.
24. Kheifets V, Mochly-Rosen D. (2007). Insight into intra-and inter-molecular interactions of PKC: design of specific modulators of kinase function. Pharmacol Res 55: 467-476.
25. Kiely PA, Baillie GS, Barrett R, Buckley DA, Adams DR, Houslay MD, et al. (2009). Phosphorylation of RACK1 on tyrosine 52 by c-Abl is required for IGF-I-mediated regulation of focal adhesion kinase (FAK). J Biol Chem 284: 20263-20274.
26. Klemke RL, Cai S, Giannini AL, Gallagher PJ, de Lanerolle P, Cheresh DA. (1997). Regulation of cell motility by mitogen-activated protein kinase. J Cell Biol 137: 481-492.
27. Lane HA, Beuvink I, Motoyama AB, Daly JM, Neve RM, Hynes NE. (2000). ErbB2 potentiates breast tumor proliferation through modulation of p27(Kip1)-Cdk2 complex formation: receptor over-expression does not determine growth dependency. Mol Cell Biol 20: 3210-3223.
28. Marone R, Hess D, Dankort D, Muller WJ, Hynes NE, Badache A. (2004). Memo mediates ErbB2-driven cell motility. Nat Cell Biol 6: 515-522.
29. McCahill A, Warwicker J, Bolger GB, Houslay MD, Yarwood SJ. (2002). The RACK1 scaffold protein: a dynamic cog in cell response mechanisms. Mol Pharmacol 62: 1261-1273.
30. Meira M, Masson R, Stagljar I, Lienhard S, Maurer F, Boulay A, et al. (2009). Memo is a cofilin-interacting protein that influences PLCgamma1 and cofilin activities, and is essential for maintaining directionality during ErbB2-induced tumor-cell migration. J Cell Sci 122: 787-797.
31. Miller LD, Lee KC, Mochly-Rosen D, Cartwright CA. (2004). RACK1 regulates Src-mediated Sam68 and p190RhoGAP signaling. Oncogene 23: 5682-5686.
32. Nagy P, Bene L, Balazs M, Hyun WC, Lockett SJ, Chiang NY, et al. (1998). EGF-induced redistribution of erbB2 on breast tumor cells: flow and image cytometric energy transfer measurements. Cytometry 32: 120-131.
33. Nalefski EA, Falke JJ. (1996). The C2 domain calcium-binding motif: structural and functional diversity. Protein Sci 5: 2375-2390.
34. Patterson RL, van Rossum DB, Nikolaidis N, Gill DL, Snyder SH. (2005). Phospholipase C-gamma: diverse roles in receptor-mediated calcium signaling. Trends Biochem Sci 30: 688-697.
35. Perkins DN, Pappin DJ, Creasy DM, Cottrell JS. (1999). Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 20: 3551-3567.
36. Rhodes DR, Yu J, Shanker K, Deshpande N, Varambally R, Ghosh D, et al. (2004). ONCOMINE: a cancer microarray database and integrated data-mining platform. Neoplasia 6: 1-6.
37. Ron D, Chen CH, Caldwell J, Jamieson L, Orr E, Mochly-Rosen D. (1994). Cloning of an intracellular receptor for protein kinase C: a homolog of the beta subunit of G proteins. Proc Natl Acad Sci USA 91: 839-843.
38. Ross JS, Fletcher JA. (1998). The HER-2/neu oncogene in breast cancer: prognostic factor, predictive factor, and target for therapy. Stem Cells 16: 413-428.
39. Schlessinger J. (2000). Cell signaling by receptor tyrosine kinases. Cell 103: 211-225.
40. Schulze WX, Deng L, Mann M. (2005). Phosphotyrosine interactome of the ErbB-receptor kinase family. Mol Syst Biol E-pub 25 May 2005.
41. Schulze WX, Mann M. (2004). A novel proteomic screen for peptide-protein interactions. J Biol Chem 279: 10756-10764.
42. Slamon DJ, Clark GM, Wong SG, Levin WJ, Ullrich A, McGuire WL. (1987). Human breast cancer: correlation of relapse and survival with amplification of the HER-2/neu oncogene. Science 235: 177-182.
43. Tomsig JL, Creutz CE. (2002). Copines: a ubiquitous family of Ca(2+)-dependent phospholipid-binding proteins. Cell Mol Life Sci 59: 1467-1477.
44. Tomsig JL, Snyder SL, Creutz CE. (2003). Identification of targets for calcium signaling through the copine family of proteins. Characterization of a coiled-coil copine-binding motif. J Biol Chem 278: 10048-10054.
45. Tomsig JL, Sohma H, Creutz CE. (2004). Calcium-dependent regulation of tumour necrosis factor-alpha receptor signalling by copine. Biochem J 378: 1089-1094.
46. Traxler P, Allegrini PR, Brandt R, Brueggen J, Cozens R, Fabbro D, et al. (2004). AEE788: a dual family epidermal growth factor receptor/ErbB2 and vascular endothelial growth factor receptor tyrosine kinase inhibitor with antitumor and antiangiogenic activity. Cancer Res 64: 4931-4941.
47. White SL, Gharbi S, Bertani MF, Chan HL, Waterfield MD, Timms JF. (2004). Cellular responses to ErbB-2 overexpression in human mammary luminal epithelial cells: comparison of mRNA and protein expression. Br J Cancer 90: 173-181.
48. Yarden Y, Sliwkowski MX. (2001). Untangling the ErbB signalling network. Nat Rev Mol Cell Biol 2: 127-137.
49. Yu YP, Landsittel D, Jing L, Nelson J, Ren B, Liu L, et al. (2004). Gene expression alterations in prostate cancer predicting tumor aggression and preceding development of malignancy. J Clin Oncol 22: 2790-2799.