Tyrosine phosphorylation of transcriptional coactivator WW-domain binding protein 2 regulates estrogen receptor α function in breast cancer via the Wnt pathway

FASEB Journal

Volumn 25, Issue 9, 2011, Pages 3004-3018

  Lim, Shen Kiat ^a,b   Orhant Prioux, Magali ^b   Toy, Weiyi ^a,b   Tan, Kah Yap ^a,b   Lim, Yoon Pin ^a,b,c,d  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^c NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^d BIOINFORMATICS INSTITUTE   (Singapore)

Author keywords

catenin; Crosstalk; EGFR; Er ; WBP2

Indexed keywords

ANTINEOPLASTIC AGENT; BETA CATENIN; BINDING PROTEIN; EPIDERMAL GROWTH FACTOR RECEPTOR; ESTROGEN; ESTROGEN RECEPTOR ALPHA; FH 535; FULVESTRANT; PROGESTERONE; PROTEIN KINASE P60; PROTEIN KINASE YES; TAMOXIFEN; TYROSINE; UNCLASSIFIED DRUG; VIMENTIN; WNT PROTEIN; WW BINDING PROTEIN 2;

ANCHORAGE INDEPENDENT GROWTH; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREAST CANCER; CANCER CELL; CANCER GROWTH; CANCER INHIBITION; CELL ADHESION; CELL INVASION; CELL MIGRATION; CELL MOTILITY; CELL PROLIFERATION; DRUG DOSE INCREASE; DRUG MEGADOSE; DRUG POTENTIATION; ENZYME ACTIVITY; FEMALE; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; MOUSE; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; TUMOR GROWTH; TUMOR VOLUME;

ANIMALS; ANTINEOPLASTIC AGENTS; CARRIER PROTEINS; CELL LINE; ESTROGEN RECEPTOR ALPHA; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, SRC; HUMANS; MAMMARY NEOPLASMS, ANIMAL; MICE; MICE, NUDE; MUTATION; NEOPLASMS, EXPERIMENTAL; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-YES; TYROSINE; WNT PROTEINS;

MUS;

EID: 80052684667     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.10-169136     Document Type: Article

References (50)

1. Lee, J. W., Lee, Y. C., Na, S. Y., Jung, D. J., and Lee, S. K. (2001) Transcriptional coregulators of the nuclear receptor superfamily: coactivators and corepressors. Cell. Mol. Life Sci. 58, 289-297 (Pubitemid 32217360)
2. McKenna, N. J., and O'Malley, B. W. (2002) Combinatorial control of gene expression by nuclear receptors and coregulators. Cell 108, 465-474 (Pubitemid 34260872)
3. Chan, S. W., Lim, C. J., Guo, K., Ng, C. P., Lee, I., Hunziker, W., Zeng, Q., and Hong, W. (2008) A role for TAZ in migration, invasion, and tumorigenesis of breast cancer cells. Cancer Res. 68, 2592-2598 (Pubitemid 351556257)
4. Oh, A. S., Lahusen, J. T., Chien, C. D., Fereshteh, M. P., Zhang, X., Dakshanamurthy, S., Xu, J., Kagan, B. L., Wellstein, A., and Riegel, A. T. (2008) Tyrosine phosphorylation of the nuclear receptor coactivator AIB1/SRC-3 is enhanced by Abl kinase and is required for its activity in cancer cells. Mol. Cell. Biol. 28, 6580-6593
5. Talukder, A. H., Li, D. Q., Manavathi, B., and Kumar, R. (2008) Serine 28 phosphorylation of NRIF3 confers its co-activator function for estrogen receptor-alpha transactivation. Oncogene 27, 5233-5242
6. Wu, R. C., Qin, J., Hashimoto, Y., Wong, J., Xu, J., Tsai, S. Y., Tsai, M. J., and O'Malley, B. W. (2002) Regulation of SRC-3 (pCIP/ACTR/AIB-1/RAC-3/ TRAM-1) Coactivator activity by IB kinase. Mol. Cell. Biol. 22, 3549-3561 (Pubitemid 34453993)
7. Lazaro, J. B., Bailey, P. J., and Lassar, A. B. (2002) Cyclin D-cdk4 activity modulates the subnuclear localization and interaction of MEF2 with SRC-family coactivators during skeletal muscle differentiation. Genes Dev. 16, 1792-1805 (Pubitemid 34803895)
8. Rowan, B. G., Garrison, N., Weigel, N. L., and O'Malley, B. W. (2000) 8-Bromo-cyclic AMP induces phosphorylation of two sites in SRC-1 that facilitate ligand-independent activation of the chicken progesterone receptor and are critical for functional cooperation between SRC-1 and CREB binding protein. Mol. Cell. Biol. 20, 8720-8730 (Pubitemid 32245905)
9. Pierce, K. L., Luttrell, L. M., and Lefkowitz, R. J. (2001) New mechanisms in heptahelical receptor signaling to mitogen activated protein kinase cascades. Oncogene 20, 1532-1539
10. Lahusen, T., Henke, R. T., Kagan, B. L., Wellstein, A., and Riegel, A. T. (2009) The role and regulation of the nuclear receptor co-activator AIB1 in breast cancer. Breast Cancer Res. Treat. 116, 225-237
11. Dhananjayan, S. C., Ramamoorthy, S., Khan, O. Y., Ismail, A., Sun, J., Slingerland, J., O'Malley, B. W., and Nawaz, Z. (2006) WW domain binding protein-2, an E6-associated protein interacting protein, acts as a coactivator of estrogen and progesterone receptors. Mol. Endocrinol. 20, 2343-2354 (Pubitemid 44496405)
12. Overholtzer, M., Zhang, J., Smolen, G. A., Muir, B., Li, W., Sgroi, D. C., Deng, C. X., Brugge, J. S., and Haber, D. A. (2006) Transforming properties of YAP, a candidate oncogene on the chromosome 11q22 amplicon. Proc. Natl. Acad. Sci. U. S. A. 103, 12405-12410 (Pubitemid 44267272)
13. Strano, S., Munarriz, E., Rossi, M., Castagnoli, L., Shaul, Y., Sacchi, A., Oren, M., Sudol, M., Cesareni, G., and Blandino, G. (2001) Physical interaction with Yes-associated protein enhances p73 transcriptional activity. J. Biol. Chem. 276, 15164 -15173
14. Zaidi, S. K., Sullivan, A. J., Medina, R., Ito, Y., Van Wijnen, A. J., Stein, J. L., Lian, J. B., and Stein, G. S. (2004) Tyrosine phosphorylation controls Runx2-mediated subnuclear targeting of YAP to repress transcription. EMBO J. 23, 790-799 (Pubitemid 38418746)
15. Vassilev, A., Kaneko, K. J., Shu, H., Zhao, Y., and DePamphilis, M. L. (2001) TEAD/TEF transcription factors utilize the activation domain of YAP65, a Src/Yes-associated protein localized in the cytoplasm. Genes Dev. 15, 1229-1241 (Pubitemid 32472752)
16. Komuro, A., Nagai, M., Navin, N. E., and Sudol, M. (2003) WW domain-containing protein YAP associates with ErbB-4 and acts as a co-transcriptional activator for the carboxyl-terminal fragment of ErbB-4 that translocates to the nucleus. J. Biol. Chem. 278, 33334-33341 (Pubitemid 37055785)
17. Chen, Y., Choong, L. Y., Lin, Q., Philp, R., Wong, C. H., Ang, B. K., Tan, Y. L., Loh, M. C., Hew, C. L., Shah, N., Druker, B. J., Chong, P. K., and Lim, Y. P. (2007) Differential expression of novel tyrosine kinase substrates during breast cancer development. Mol. Cell. Proteomics 6, 2072-2087
18. Lim, Y. P., Diong, L. S., Qi, R., Druker, B. J., and Epstein, R. J. (2003) Phosphoproteomic fingerprinting of epidermal growth factor signaling and anticancer drug action in human tumor cells. Mol. Cancer Ther. 2, 1369-1377
19. Toy, W., Lim, S. K., Loh, M. C., and Lim, Y. P. (2010) EGF-induced tyrosine phosphorylation of Endofin is dependent on PI3K activity and proper localization to endosomes. Cell. Signal. 22, 437-446
20. Liang, K. Y., and Scott, L. Z. (1986) Longitudinal data analysis using generalized linear models. Biometrika 73, 13-22
21. Fox, E. M., Andrade, J., and Shupnik, M. A. (2009) Novel actions of estrogen to promote proliferation: integration of cytoplasmic and nuclear pathways. Steroids 74, 622-627
22. Migliaccio, A., Castoria, G., Di Domenico, M., Ciociola, A., Lombardi, M., De Falco, A., Nanayakkara, M., Bottero, D., De Stasio, R., Varricchio, L., and Auricchio, F. (2006) Crosstalk between EGFR and extranuclear steroid receptors. Ann. N. Y. Acad. Sci. 1089, 194-200 (Pubitemid 47092061)
23. Lange, C. A. (2004) Making sense of cross-talk between steroid hormone receptors and intracellular signaling pathways: who will have the last word? Mol. Endocrinol. 18, 269-278
24. Kariagina, A., Xie, J., Leipprandt, J. R., and Haslam, S. Z. Amphiregulin mediates estrogen, progesterone, and EGFR signaling in the normal rat mammary gland and in hormonedependent rat mammary cancers. Horm. Cancer 1, 229 -244
25. Biscardi, J. S., Ishizawar, R. C., Silva, C. M., and Parsons, S. J. (2000) Tyrosine kinase signalling in breast cancer: epidermal growth factor receptor and c-Src interactions in breast cancer. Breast Cancer Res. 2, 203-210 (Pubitemid 32223586)
26. Brown, M. T., and Cooper, J. A. (1996) Regulation, substrates and functions of src. Biochim. Biophys. Acta 1287, 121-149 (Pubitemid 26189191)
27. Sudol, M. (1994) Yes-associated protein (YAP65) is a prolinerich phosphoprotein that binds to the SH3 domain of the Yes proto-oncogene product. Oncogene 9, 2145-2152
28. Chen, H. I., Einbond, A., Kwak, S. J., Linn, H., Koepf, E., Peterson, S., Kelly, J. W., and Sudol, M. (1997) Characterization of the WW domain of human yes-associated protein and its polyproline-containing ligands. J. Biol. Chem. 272, 17070-17077 (Pubitemid 27289814)
29. Chen, H. I., and Sudol, M. (1995) The WW domain of Yesassociated protein binds a proline-rich ligand that differs from the consensus established for Src homology 3-binding modules. Proc. Natl. Acad. Sci. U. S. A. 92, 7819-7823
30. Biscardi, J. S., Maa, M. C., Tice, D. A., Cox, M. E., Leu, T. H., and Parsons, S. J. (1999) c-Src-mediated phosphorylation of the epidermal growth factor receptor on Tyr845 and Tyr1101 is associated with modulation of receptor function. J. Biol. Chem. 274, 8335-8343
31. Callige, M., and Richard-Foy, H. (2006) Ligand-induced estrogen receptor alpha degradation by the proteasome: new actors? Nucl. Recept. Signal. 4, e004
32. Toy, W., Lim, S. K., Loh, M. C., and Lim, Y. P. EGF-induced tyrosine phosphorylation of Endofin is dependent on PI3K activity and proper localization to endosomes. Cell. Signal. 22, 437-446
33. Chan, S. W., Lim, C. J., Huang, C., Chong, Y. F., Gunaratne, H. J., Hogue, K. A., Blackstock, W. P., Harvey, K. F., and Hong, W. (2011) WW domain-mediated interaction with Wbp2 is important for the oncogenic property of TAZ. Oncogene 30, 600-610
34. Clevers, H. (2006) Wnt/beta-catenin signaling in development and disease. Cell 127, 469-480
35. Mohinta, S., Wu, H., Chaurasia, P., and Watabe, K. (2007) Wnt pathway and breast cancer. Front. Biosci. 12, 4020-4033
36. Mulholland, D. J., Dedhar, S., Coetzee, G. A., and Nelson, C. C. (2005) Interaction of nuclear receptors with the Wnt/betacatenin/ Tcf signaling axis: Wnt you like to know? Endocr. Rev. 26, 898-915 (Pubitemid 41770157)
37. El-Tanani, M., Fernig, D. G., Barraclough, R., Green, C., and Rudland, P. (2001) Differential modulation of transcriptional activity of estrogen receptors by direct protein-protein interactions with the T cell factor family of transcription factors. J. Biol. Chem. 276, 41675-41682
38. Handeli, S., and Simon, J. A. (2008) A small-molecule inhibitor of Tcf/beta-catenin signaling down-regulates PPARgamma and PPARdelta activities. Mol. Cancer Ther. 7, 521-529 (Pubitemid 351482135)
39. Baichwal, V. R., and Tjian, R. (1990) Control of c-Jun activity by interaction of a cell-specific inhibitor with regulatory domain delta: differences between v- and c-Jun. Cell 63, 815-825 (Pubitemid 120035054)
40. Williams, T., and Tjian, R. (1991) Analysis of the DNA-binding and activation properties of the human transcription factor AP-2. Genes Dev. 5, 670-682 (Pubitemid 21905986)
41. Nerlov, C., and Ziff, E. B. (1994) Three levels of functional interaction determine the activity of CCAAT/enhancer binding protein-alpha on the serum albumin promoter. Genes Dev. 8, 350-362 (Pubitemid 24065976)
42. Yagi, R., Chen, L. F., Shigesada, K., Murakami, Y., and Ito, Y. (1999) AWWdomain-containing yes-associated protein (YAP) is a novel transcriptional co-activator. EMBO J. 18, 2551-2562 (Pubitemid 29213286)
43. Jolliffe, C. N., Harvey, K. F., Haines, B. P., Parasivam, G., and Kumar, S. (2000) Identification of multiple proteins expressed in murine embryos as binding partners for the WW domains of the ubiquitin-protein ligase Nedd4. Biochem. J. 351, 557-565
44. Pirozzi, G., McConnell, S. J., Uveges, A. J., Carter, J. M., Sparks, A. B., Kay, B. K., and Fowlkes, D. M. (1997) Identification of novel human WW domain-containing proteins by cloning of ligand targets. J. Biol. Chem. 272, 14611-14616 (Pubitemid 27251722)
45. Louie, M. C., Zou, J. X., Rabinovich, A., and Chen, H. W. (2004) ACTR/AIB1 functions as an E2F1 coactivator to promote breast cancer cell proliferation and antiestrogen resistance. Mol. Cell. Biol. 24, 5157-5171 (Pubitemid 38738153)
46. Arimura, A., vn Peer, M., Schroder, A. J., and Rothman, P. B. (2004) The transcriptional co-activator p/CIP (NCoA-3) is up-regulated by STAT6 and serves as a positive regulator of transcriptional activation by STAT6. J. Biol. Chem. 279, 31105-31112
47. Kouzmenko, A. P., Takeyama, K., Ito, S., Furutani, T., Sawatsubashi, S., Maki, A., Suzuki, E., Kawasaki, Y., Akiyama, T., Tabata, T., and Kato, S. (2004) Wnt/beta-catenin and estrogen signaling converge in vivo. J. Biol. Chem. 279, 40255-40258 (Pubitemid 39287607)
48. Hecht, A., Vleminckx, K., Stemmler, M. P., Van Roy, F., and Kemler, R. (2000) The p300/CBP acetyltransferases function as transcriptional coactivators of beta-catenin in vertebrates. EMBO J. 19, 1839-1850 (Pubitemid 30204395)
49. Barker, N., Hurlstone, A., Musisi, H., Miles, A., Bienz, M., and Clevers, H. (2001) The chromatin remodelling factor Brg-1 interacts with beta-catenin to promote target gene activation. EMBO J. 20, 4935-4943 (Pubitemid 32848645)
50. Yang, X., Chen, M. W., Terry, S., Vacherot, F., Bemis, D. L., Capodice, J., Kitajewski, J., De la Taille, A., Benson, M. C., Guo, Y., and Buttyan, R. (2006) Complex regulation of human androgen receptor expression by Wnt signaling in prostate cancer cells. Oncogene 25, 3436-3444 (Pubitemid 43877046)