Viral small T oncoproteins transform cells by alleviating Hippo-pathway-mediated inhibition of the YAP proto-oncogene

Cell Reports

Volumn 8, Issue 3, 2014, Pages 707-713

  Nguyen, Hung Thanh ^a   Hong, Xin ^a,b,c   Tan, Sam ^a   Chen, Qingfeng ^b,c   Chan, Lifang ^a   Fivaz, Marc ^a,c   Cohen, Stephen M ^b,c   Mathijs Voorhoeve, P ^a  

^a DUKE NUS MEDICAL SCHOOL   (Singapore)

^b INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Singapore)

^c NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

ANKRD1 PROTEIN; CELL PROTEIN; CONNECTIVE TISSUE GROWTH FACTOR; LONG ACTING THYROID STIMULATOR; LONG ACTING THYROID STIMULATOR 1; LONG ACTING THYROID STIMULATOR 2; MITOGEN ACTIVATED PROTEIN KINASE; MYC PROTEIN; ONCOPROTEIN; P21 ACTIVATED KINASE 1; PROTEIN KINASE B; RAS PROTEIN; SURVIVIN; UNCLASSIFIED DRUG; VIRAL SMALL T ONCOPROTEIN;

ANCHORAGE INDEPENDENT GROWTH; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER INHIBITION; CELL MEMBRANE; CELL TRANSFORMATION; COLONY FORMATION; CONTROLLED STUDY; DISEASE ASSOCIATION; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; GENE INACTIVATION; HIPPO TUMOR SUPPRESSOR PATHWAY; HUMAN; HUMAN CELL; MOUSE; NF2 GENE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTO ONCOGENE; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR GENE; UPREGULATION; YAP PROTO ONCOGENE;

PYRONIA TITHONUS;

EID: 84924595157     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2014.06.062     Document Type: Article

References (38)

1. Aragona, M., Panciera, T., Manfrin, A., Giulitti, S., Michielin, F., Elvassore, N., Dupont, S., and Piccolo, S. (2013). A mechanical checkpoint controls multicellular growth through YAP/TAZ regulation by actin-processing factors. Cell 154, 1047-1059.
2. Barry, E.R., and Camargo, F.D. (2013). The Hippo superhighway: signaling crossroads converging on the Hippo/Yap pathway in stem cells and development. Curr. Opin. Cell Biol. 25, 247-253.
3. Brummelkamp, T.R., Bernards, R., and Agami, R. (2002). A system for stable expression of short interfering RNAs in mammalian cells. Science 296, 550-553.
4. Chen, Q., Khoury, M., and Chen, J. (2009). Expression of human cytokines dramatically improves reconstitution of specific human-blood lineage cells in humanized mice. Proc. Natl. Acad. Sci. USA 106, 21783-21788.
5. Cho, U.S., Morrone, S., Sablina, A.A., Arroyo, J.D., Hahn, W.C., and Xu, W. (2007). Structural basis of PP2A inhibition by small t antigen. PLoS Biol. 5, e202.
6. Couzens, A.L., Knight, J.D., Kean, M.J., Teo, G., Weiss, A., Dunham, W.H., Lin, Z.Y., Bagshaw, R.D., Sicheri, F., Pawson, T., et al. (2013). Protein interaction network of the mammalian Hippo pathway reveals mechanisms of kinasephosphatase interactions. Sci. Signal. 6, rs15.
7. Deacon, S.W., Beeser, A., Fukui, J.A., Rennefahrt, U.E., Myers, C., Chernoff, J., and Peterson, J.R. (2008). An isoform-selective, small-molecule inhibitor targets the autoregulatory mechanism of p21-activated kinase. Chem. Biol. 15, 322-331.
8. Dong, J., Feldmann, G., Huang, J., Wu, S., Zhang, N., Comerford, S.A., Gayyed, M.F., Anders, R.A., Maitra, A., and Pan, D. (2007). Elucidation of a universal size-control mechanism in Drosophila and mammals. Cell 130, 1120-1133.
9. Dumont, N., Crawford, Y.G., Sigaroudinia, M., Nagrani, S.S., Wilson, M.B., Buehring, G.C., Turashvili, G., Aparicio, S., Gauthier, M.L., Fordyce, C.A., et al. (2009). Human mammary cancer progression model recapitulates methylation events associated with breast premalignancy. Breast Cancer Res. 11, R87.
10. Dupont, S., Morsut, L., Aragona, M., Enzo, E., Giulitti, S., Cordenonsi, M., Zanconato, F., Le Digabel, J., Forcato, M., Bicciato, S., et al. (2011). Role of YAP/TAZ in mechanotransduction. Nature 474, 179-183.
11. Feng, H., Shuda, M., Chang, Y., and Moore, P.S. (2008). Clonal integration of a polyomavirus in human Merkel cell carcinoma. Science 319, 1096-1100.
12. Hahn, W.C., Counter, C.M., Lundberg, A.S., Beijersbergen, R.L., Brooks, M.W., and Weinberg, R.A. (1999). Creation of human tumour cells with defined genetic elements. Nature 400, 464-468.
13. Hahn, W.C., Dessain, S.K., Brooks, M.W., King, J.E., Elenbaas, B., Sabatini, D.M., DeCaprio, J.A., and Weinberg, R.A. (2002). Enumeration of the simian virus 40 early region elements necessary for human cell transformation. Mol. Cell. Biol. 22, 2111-2123.
14. Halder, G., Dupont, S., and Piccolo, S. (2012). Transduction of mechanical and cytoskeletal cues by YAP and TAZ. Nat. Rev. Mol. Cell Biol. 13, 591-600.
15. Hao, Y., Chun, A., Cheung, K., Rashidi, B., and Yang, X. (2008). Tumor suppressor LATS1 is a negative regulator of oncogene YAP. J. Biol. Chem. 283, 5496-5509.
16. He, H., Shulkes, A., and Baldwin, G.S. (2008). PAK1 interacts with beta-catenin and is required for the regulation of the beta-catenin signalling pathway by gastrins. Biochim. Biophys. Acta 1783, 1943-1954.
17. Lei, Q.Y., Zhang, H., Zhao, B., Zha, Z.Y., Bai, F., Pei, X.H., Zhao, S., Xiong, Y., and Guan, K.L. (2008). TAZ promotes cell proliferation and epithelial-mesenchymal transition and is inhibited by the hippo pathway. Mol. Cell. Biol. 28, 2426-2436.
18. Liu-Chittenden, Y., Huang, B., Shim, J.S., Chen, Q., Lee, S.J., Anders, R.A., Liu, J.O., and Pan, D. (2012). Genetic and pharmacological disruption of the TEAD-YAP complex suppresses the oncogenic activity of YAP. Genes Dev. 26, 1300-1305.
19. Locke, W.J., and Clark, S.J. (2012). Epigenome remodelling in breast cancer: insights from an early in vitro model of carcinogenesis. Breast Cancer Res. 14, 215.
20. Manser, E., Huang, H.Y., Loo, T.H., Chen, X.Q., Dong, J.M., Leung, T., and Lim, L. (1997). Expression of constitutively active alpha-PAK reveals effects of the kinase on actin and focal complexes. Mol. Cell. Biol. 17, 1129-1143.
21. 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. USA 103, 12405-12410.
22. Ribeiro, P.S., Josué, F., Wepf, A., Wehr, M.C., Rinner, O., Kelly, G., Tapon, N., and Gstaiger, M. (2010). Combined functional genomic and proteomic approaches identify a PP2A complex as a negative regulator of Hippo signaling. Mol. Cell 39, 521-534.
23. Sablina, A.A., and Hahn, W.C. (2008). SV40 small T antigen and PP2A phosphatase in cell transformation. Cancer Metastasis Rev. 27, 137-146.
24. Sablina, A.A., Hector, M., Colpaert, N., and Hahn, W.C. (2010). Identification of PP2A complexes and pathways involved in cell transformation. Cancer Res. 70, 10474-10484.
25. Shaw, R.J., Paez, J.G., Curto, M., Yaktine, A., Pruitt, W.M., Saotome, I., O'Bryan, J.P., Gupta, V., Ratner, N., Der, C.J., et al. (2001). The Nf2 tumor suppressor, merlin, functions in Rac-dependent signaling. Dev. Cell 1, 63-72.
26. Shuda, M., Kwun, H.J., Feng, H., Chang, Y., and Moore, P.S. (2011). Human Merkel cell polyomavirus small T antigen is an oncoprotein targeting the 4E-BP1 translation regulator. J. Clin. Invest. 121, 3623-3634.
27. Taglieri, D.M., Monasky, M.M., Knezevic, I., Sheehan, K.A., Lei, M., Wang, X., Chernoff, J., Wolska, B.M., Ke, Y., and Solaro, R.J. (2011). Ablation of p21-activated kinase-1 in mice promotes isoproterenol-induced cardiac hypertrophy in association with activation of Erk1/2 and inhibition of protein phosphatase 2A. J. Mol. Cell. Cardiol. 51, 988-996.
28. Voorhoeve, P.M., and Agami, R. (2003). The tumor-suppressive functions of the human INK4A locus. Cancer Cell 4, 311-319.
29. Wada, K., Itoga, K., Okano, T., Yonemura, S., and Sasaki, H. (2011). Hippo pathway regulation by cell morphology and stress fibers. Development 138, 3907-3914.
30. Wang, Z., Fu, M., Wang, L., Liu, J., Li, Y., Brakebusch, C., and Mei, Q. (2013). p21-activated kinase 1 (PAK1) can promote ERK activation in a kinase-independent manner. J. Biol. Chem. 288, 20093-20099.
31. Westphal, R.S., Coffee, R.L., Jr., Marotta, A., Pelech, S.L., and Wadzinski, B.E. (1999). Identification of kinase-phosphatase signaling modules composed of p70 S6 kinase-protein phosphatase 2A (PP2A) and p21-activated kinase-PP2A. J. Biol. Chem. 274, 687-692.
32. Xiao, G.H., Beeser, A., Chernoff, J., and Testa, J.R. (2002). p21-activated kinase links Rac/Cdc42 signaling to merlin. J. Biol. Chem. 277, 883-886.
33. Yin, F., Yu, J., Zheng, Y., Chen, Q., Zhang, N., and Pan, D. (2013). Spatial organization of Hippo signaling at the plasma membrane mediated by the tumor suppressor Merlin/NF2. Cell 154, 1342-1355.
34. Zhang, J., Ji, J.Y., Yu, M., Overholtzer, M., Smolen, G.A., Wang, R., Brugge, J.S., Dyson, N.J., and Haber, D.A. (2009). YAP-dependent induction of amphiregulin identifies a non-cell-autonomous component of the Hippo pathway. Nat. Cell Biol. 11, 1444-1450.
35. Zhang, N., Bai, H., David, K.K., Dong, J., Zheng, Y., Cai, J., Giovannini, M., Liu, P., Anders, R.A., and Pan, D. (2010). The Merlin/NF2 tumor suppressor functions through the YAP oncoprotein to regulate tissue homeostasis in mammals. Dev. Cell 19, 27-38.
36. Zhao, B., Wei, X., Li, W., Udan, R.S., Yang, Q., Kim, J., Xie, J., Ikenoue, T., Yu, J., Li, L., et al. (2007). Inactivation of YAP oncoprotein by the Hippo pathway is involved in cell contact inhibition and tissue growth control. Genes Dev. 21, 2747-2761.
37. Zhao, B., Li, L., Lei, Q., and Guan, K.L. (2010a). The Hippo-YAP pathway in organ size control and tumorigenesis: an updated version. Genes Dev. 24, 862-874.
38. Zhao, B., Li, L., Tumaneng, K., Wang, C.Y., and Guan, K.L. (2010b). A coordinated phosphorylation by Lats and CK1 regulates YAP stability through SCF(beta-TRCP). Genes Dev. 24, 72-85.