Wnt/β-catenin signaling regulates yes-associated protein (YAP) gene expression in colorectal carcinoma cells

Journal of Biological Chemistry

Volumn 287, Issue 15, 2012, Pages 11730-11739

  Konsavage, Wesley M ^a   Kyler, Sydney L ^a   Rennoll, Sherri A ^a   Jin, Ge ^a   Yochum, Gregory S ^a  

^a PENN STATE COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CULTURE; CELL SIGNALING; DISEASES; GENE EXPRESSION REGULATION; NUCLEIC ACIDS; TRANSCRIPTION FACTORS; TUMORS;

CARCINOMA CELLS; CATENIN SIGNALING; COLORECTAL CANCER CELL; COLORECTAL CARCINOMA; GENES EXPRESSION; NUCLEAR ACCUMULATION; PROTEIN EXPRESSIONS; PROTEIN GENES; TRANSCRIPTIONAL CO-ACTIVATORS; Β-CATENIN;

TRANSCRIPTION;

BETA CATENIN; ONCOPROTEIN; SHORT HAIRPIN RNA; T CELL FACTOR 4; T CELL FACTOR PROTEIN; UNCLASSIFIED DRUG; WNT PROTEIN; YES ASSOCIATED PROTEIN;

ANCHORAGE INDEPENDENT GROWTH; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER CELL; CARCINOGENESIS; CELL METABOLISM; CELL NUCLEUS; CELLULAR DISTRIBUTION; COLON MUCOSA; COLORECTAL CARCINOMA; COMPLEX FORMATION; CONTROLLED STUDY; CYTOPLASM; ENHANCER REGION; GENE EXPRESSION; GENE LOCUS; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; ONCOGENE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; TUMOR XENOGRAFT; YES ASSOCIATED PROTEIN GENE;

EID: 84859516537     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.327767     Document Type: Article

References (43)

1. MacDonald, B. T., Tamai, K., and He, X. (2009) Wnt/β-catenin signaling: components, mechanisms, and diseases. Dev. Cell 17, 9-26
2. Rizvi, A. Z., and Wong, M. H. (2005) Epithelial stem cells and their niche: there's no place like home. Stem Cells 23, 150-165 (Pubitemid 40239512)
3. Sancho, E., Batlle, E., and Clevers, H. (2004) Signaling pathways in intestinal development and cancer. Annu. Rev. Cell Dev. Biol. 20, 695-723 (Pubitemid 39488655)
4. Nusse, R. (2005) Wnt signaling in disease and in development. Cell Res 15, 28-32
5. Mosimann, C., Hausmann, G., and Basler, K. (2009) β-Catenin hits chromatin: regulation of Wnt target gene activation. Nat. Rev. Mol. Cell Biol. 10, 276-286
6. Korinek, V., Barker, N., Morin, P. J., van Wichen, D., de Weger, R., Kinzler, K. W., Vogelstein, B., and Clevers, H. (1997) Constitutive transcriptional activation by a β-catenin-Tcf complex in APC-/- colon carcinoma. Science 275, 1784-1787 (Pubitemid 27136714)
7. Bottomly, D., Kyler, S. L., McWeeney, S. K., and Yochum, G. S. (2010) Identification of {β}-catenin binding regions in colon cancer cells using ChIP-Seq. Nucleic Acids Res. 38, 5735-5745
8. Zhao, B., Li, L., Lei, Q., and Guan, K. L. (2010) The Hippo-YAP pathway in organ size control and tumorigenesis: an updated version. Genes Dev. 24, 862-874
9. Harvey, K. F., Pfleger, C. M., and Hariharan, I. K. (2003) The Drosophila Mst ortholog, hippo, restricts growth and cell proliferation and promotes apoptosis. Cell 114, 457-467 (Pubitemid 37100994)
10. Pantalacci, S., Tapon, N., and Léopold, P. (2003) The Salvador partner Hippo promotes apoptosis and cell-cycle exit in Drosophila. Nat. Cell Biol. 5, 921-927 (Pubitemid 37220699)
11. Wu, S., Huang, J., Dong, J., and Pan, D. (2003) Hippo encodes a Ste-20 family protein kinase that restricts cell proliferation and promotes apoptosis in conjunction with salvador and warts. Cell 114, 445-456 (Pubitemid 37100993)
12. Zhao, B., Ye, X., Yu, J., Li, L., Li, W., Li, S., Lin, J. D., Wang, C. Y., Chinnaiyan, A. M., Lai, Z. C., and Guan, K. L. (2008) TEAD mediates YAP-dependent gene induction and growth control. Genes Dev. 22, 1962-1971 (Pubitemid 352008643)
13. 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
14. Camargo, F. D., Gokhale, S., Johnnidis, J. B., Fu, D., Bell, G. W., Jaenisch, R., and Brummelkamp, T. R. (2007) YAP1 increases organ size and expands undifferentiated progenitor cells. Curr. Biol. 17, 2054-2060 (Pubitemid 350180465)
15. Lu, L., Li, Y., Kim, S. M., Bossuyt, W., Liu, P., Qiu, Q., Wang, Y., Halder, G., Finegold, M. J., Lee, J. S., and Johnson, R. L. (2010) Hippo signaling is a potent in vivo growth and tumor suppressor pathway in the mammalian liver. Proc. Natl. Acad. Sci. U.S.A. 107, 1437-1442
16. Song, H., Mak, K. K., Topol, L., Yun, K., Hu, J., Garrett, L., Chen, Y., Park, O., Chang, J., Simpson, R. M., Wang, C. Y., Gao, B., Jiang, J., and Yang, Y. (2010) Mammalian Mst1 and Mst2 kinases play essential roles in organ size control and tumor suppression. Proc. Natl. Acad. Sci. U.S.A. 107, 1431-1436
17. Zhou, D., Zhang, Y., Wu, H., Barry, E., Yin, Y., Lawrence, E., Dawson, D., Willis, J. E., Markowitz, S. D., Camargo, F. D., and Avruch, J. (2011) Mst1 and Mst2 protein kinases restrain intestinal stem cell proliferation and colonic tumorigenesis by inhibition of Yes-associated protein (Yap) overabundance. Proc. Natl. Acad. Sci. U.S.A. 108, E1312-E1320
18. Cai, J., Zhang, N., Zheng, Y., de Wilde, R. F., Maitra, A., and Pan, D. (2010) The Hippo signaling pathway restricts the oncogenic potential of an intestinal regeneration program. Genes Dev. 24, 2383-2388
19. Steinhardt, A. A., Gayyed, M. F., Klein, A. P., Dong, J., Maitra, A., Pan, D., Montgomery, E. A., and Anders, R. A. (2008) Expression of Yes-associated protein in common solid tumors. Hum. Pathol. 39, 1582-1589
20. Dignam, J. D., Lebovitz, R. M., and Roeder, R. G. (1983) Accurate transcription initiation byRNApolymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 11, 1475-1489
21. Yochum, G. S., Sherrick, C. M., Macpartlin, M., and Goodman, R. H. (2010) A beta-catenin/TCF-coordinated chromatin loop at MYC integrates 5′ and 3′ Wnt responsive enhancers. Proc. Natl. Acad. Sci. U.S.A. 107, 145-150
22. Yochum. (2011) Multiple Wnt/ß-catenin responsive enhancers align with the MYC promoter through long-range chromatin loops. PLoS ONE 6, e18966
23. Sansom, O. J., Meniel, V. S., Muncan, V., Phesse, T. J., Wilkins, J. A., Reed, K. R., Vass, J. K., Athineos, D., Clevers, H., and Clarke, A. R. (2007) Myc deletion rescues Apc deficiency in the small intestine. Nature 446, 676-679 (Pubitemid 46606884)
24. Archbold, H. C., Yang, Y. X., Chen, L., and Cadigan, K. M. (2012) How do they do Wnt they do?: Regulation of transcription by the Wnt/β-catenin pathway. Acta Physiol. 204, 74-109
25. Hatzis, P., van der Flier, L. G., van Driel, M. A., Guryev, V., Nielsen, F., Denissov, S., Nijman, I. J., Koster, J., Santo, E. E., Welboren, W., Versteeg, R., Cuppen, E., van de Wetering, M., Clevers, H., and Stunnenberg, H. G. (2008) Genome-wide pattern of TCF7L2/TCF4 chromatin occupancy in colorectal cancer cells. Mol. Cell. Biol. 28, 2732-2744 (Pubitemid 351542371)
26. Yochum, G. S., McWeeney, S., Rajaraman, V., Cleland, R., Peters, S., and Goodman, R. H. (2007) Serial analysis of chromatin occupancy identifies β-catenin target genes in colorectal carcinoma cells. Proc. Natl. Acad. Sci. U.S.A. 104, 3324-3329 (Pubitemid 46364158)
27. van de Wetering, M., Sancho, E., Verweij, C., de Lau, W., Oving, I., Hurlstone, A., van der Horn, K., Batlle, E., Coudreuse, D., Haramis, A. P., Tjon-Pon-Fong, M., Moerer, P., van den Born, M., Soete, G., Pals, S., Eilers, M., Medema, R., and Clevers, H. (2002) The β-catenin/TCF-4 complex imposes a crypt progenitor phenotype on colorectal cancer cells. Cell 111, 241-250 (Pubitemid 35292444)
28. Zhao, B., Wei, X., Li, W., Udan, R. S., Yang, Q., Kim, J., Xie, J., Ikenoue, T., Yu, J., Li, L., Zheng, P., Ye, K., Chinnaiyan, A., Halder, G., Lai, Z. C., and Guan, K. L. (2007) Inactivation of YAP oncoprotein by the Hippo pathway is involved in cell contact inhibition and tissue growth control. Genes Dev. 21, 2747-2761 (Pubitemid 350070721)
29. Zhang, X., George, J., Deb, S., Degoutin, J. L., Takano, E. A., Fox, S. B., Bowtell, D. D., and Harvey, K. F. (2011) The Hippo pathway transcriptional co-activator, YAP, is an ovarian cancer oncogene. Oncogene 30, 2810-2822
30. Hall, C. A., Wang, R., Miao, J., Oliva, E., Shen, X., Wheeler, T., Hilsenbeck, S. G., Orsulic, S., and Goode, S. (2010) Hippo pathway effector Yap is an ovarian cancer oncogene. Cancer Res. 70, 8517-8525
31. da Costa, L. T., He, T. C., Yu, J., Sparks, A. B., Morin, P. J., Polyak, K., Laken, S., Vogelstein, B., and Kinzler, K. W. (1999) CDX2 is mutated in a colorectal cancer with normal APC/β-catenin signaling. Oncogene 18, 5010-5014 (Pubitemid 29425309)
32. Kim, N. G., Koh, E., Chen, X., and Gumbiner, B. M. (2011) E-cadherin mediates contact inhibition of proliferation through Hippo signalingpathway components. Proc. Natl. Acad. Sci. U.S.A. 108, 11930-11935
33. Anderson, C. B., Neufeld, K. L., and White, R. L. (2002) Subcellular distribution of Wnt pathway proteins in normal and neoplastic colon. Proc. Natl. Acad. Sci. U.S.A. 99, 8683-8688 (Pubitemid 34693620)
34. Clevers, H. (2006) Wnt/β-catenin signaling in development and disease. Cell 127, 469-480
35. Liu, A. M., Poon, R. T., and Luk, J. M. (2010) MicroRNA-375 targets Hippo-signaling effector YAP in liver cancer and inhibits tumor properties. Biochem. Biophys. Res. Commun. 394, 623-627
36. Silvis, M. R., Kreger, B. T., Lien, W. H., Klezovitch, O., Rudakova, G. M., Camargo, F. D., Lantz, D. M., Seykora, J. T., and Vasioukhin, V. (2011) α-Catenin is a tumor suppressor that controls cell accumulation by regulating the localization and activity of the transcriptional coactivator Yap1. Sci. Signal 4, ra33
37. Schlegelmilch, K., Mohseni, M., Kirak, O., Pruszak, J., Rodriguez, J. R., Zhou, D., Kreger, B. T., Vasioukhin, V., Avruch, J., Brummelkamp, T. R., and Camargo, F. D. (2011) Yap1 acts downstream of α-catenin to control epidermal proliferation. Cell 144, 782-795
38. Deleted in proof
39. Hanahan, D., and Weinberg, R. A. (2011) Hallmarks of cancer: the next generation. Cell 144, 646-674
40. Varelas, X., Miller, B. W., Sopko, R., Song, S., Gregorieff, A., Fellouse, F. A., Sakuma, R., Pawson, T., Hunziker, W., McNeill, H., Wrana, J. L., and Attisano, L. (2010) The Hippo pathway regulates Wnt/β-catenin signaling. Dev. Cell 18, 579-591
41. Hergovich, A., and Hemmings, B. A. (2010) TAZ-mediated crosstalk between Wnt and Hippo signaling. Dev. Cell 18, 508-509
42. Heallen, T., Zhang, M., Wang, J., Bonilla-Claudio, M., Klysik, E., Johnson, R. L., and Martin, J. F. (2011) Hippo pathway inhibits Wnt signaling to restrain cardiomyocyte proliferation and heart size. Science 332, 458-461
43. Barker, N., and Clevers, H. (2006) Mining the Wnt pathway for cancer therapeutics. Nat. Rev. Drug. Discov. 5, 997-1014 (Pubitemid 44835127)