Repression of intestinal stem cell function and tumorigenesis through direct phosphorylation of β-catenin and yap by PKCζ

Cell Reports

Volumn 10, Issue 5, 2015, Pages 740-754

  Llado, Victoria ^a   Nakanishi, Yuki ^a   Duran, Angeles ^a   Reina Campos, Miguel ^a   Shelton, Phillip M ^a   Linares, Juan F ^a   Yajima, Tomoko ^a   Campos, Alex ^a   Aza Blanc, Pedro ^a   Leitges, Michael ^b   Diaz Meco, Maria T ^a   Moscat, Jorge ^a  

^a BURNHAM INSTITUTE   (United States)

^b UNIVERSITY OF OSLO   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; ONCOPROTEIN; PROTEIN KINASE C ZETA; UNCLASSIFIED DRUG; YAP PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CARCINOGENESIS; CELL ACTIVITY; CELL FUNCTION; COLON ADENOCARCINOMA; CONTROLLED STUDY; DOWN REGULATION; ENZYME SUBSTRATE; HUMAN; IN VIVO STUDY; INHIBITION KINETICS; INTESTINAL CARCINOGENESIS; INTESTINAL STEM CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; SIGNAL TRANSDUCTION; TISSUE REGENERATION;

MUS;

EID: 84923333865     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2015.01.007     Document Type: Article

References (32)

1. Anastas J.N., Moon R.T. WNT signalling pathways as therapeutic targets in cancer. Nat. Rev. Cancer 2013, 13:11-26.
2. Azzolin L., Panciera T., Soligo S., Enzo E., Bicciato S., Dupont S., Bresolin S., Frasson C., Basso G., Guzzardo V., et al. YAP/TAZ incorporation in the β-catenin destruction complex orchestrates the Wnt response. Cell 2014, 158:157-170.
3. Barker N., van Es J.H., Kuipers J., Kujala P., van den Born M., Cozijnsen M., Haegebarth A., Korving J., Begthel H., Peters P.J., Clevers H. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 2007, 449:1003-1007.
4. Barker N., Ridgway R.A., van Es J.H., van de Wetering M., Begthel H., van den Born M., Danenberg E., Clarke A.R., Sansom O.J., Clevers H. Crypt stem cells as the cells-of-origin of intestinal cancer. Nature 2009, 457:608-611.
5. Barry E.R., Camargo F.D. The Hippo superhighway: signaling crossroads converging on the Hippo/Yap pathway in stem cells and development. Curr. Opin. Cell Biol. 2013, 25:247-253.
6. Barry E.R., Morikawa T., Butler B.L., Shrestha K., de la Rosa R., Yan K.S., Fuchs C.S., Magness S.T., Smits R., Ogino S., et al. Restriction of intestinal stem cell expansion and the regenerative response by YAP. Nature 2013, 493:106-110.
7. Cai J., Zhang N., Zheng Y., de Wilde R.F., Maitra A., Pan D. The Hippo signaling pathway restricts the oncogenic potential of an intestinal regeneration program. Genes Dev. 2010, 24:2383-2388.
8. Clevers H. The intestinal crypt, a prototype stem cell compartment. Cell 2013, 154:274-284.
9. Clevers H., Loh K.M., Nusse R. Stem cell signaling. An integral program for tissue renewal and regeneration: Wnt signaling and stem cell control. Science 2014, 346:1248012.
10. DeRan M., Yang J., Shen C.H., Peters E.C., Fitamant J., Chan P., Hsieh M., Zhu S., Asara J.M., Zheng B., et al. Energy stress regulates hippo-YAP signaling involving AMPK-mediated regulation of angiomotin-like 1 protein. Cell Rep. 2014, 9:495-503.
11. Egan L.J., Eckmann L., Greten F.R., Chae S., Li Z.W., Myhre G.M., Robine S., Karin M., Kagnoff M.F. IkappaB-kinasebeta-dependent NF-kappaB activation provides radioprotection to the intestinal epithelium. Proc. Natl. Acad. Sci. USA 2004, 101:2452-2457.
12. Galvez A.S., Duran A., Linares J.F., Pathrose P., Castilla E.A., Abu-Baker S., Leitges M., Diaz-Meco M.T., Moscat J. Protein kinase Czeta represses the interleukin-6 promoter and impairs tumorigenesis invivo. Mol. Cell. Biol. 2009, 29:104-115.
13. Harvey K.F., Zhang X., Thomas D.M. The Hippo pathway and human cancer. Nat. Rev. Cancer 2013, 13:246-257.
14. Korinek V., Barker N., Moerer P., van Donselaar E., Huls G., Peters P.J., Clevers H. Depletion of epithelial stem-cell compartments in the small intestine of mice lacking Tcf-4. Nat. Genet. 1998, 19:379-383.
15. Li L., Clevers H. Coexistence of quiescent and active adult stem cells in mammals. Science 2010, 327:542-545.
16. Li V.S., Ng S.S., Boersema P.J., Low T.Y., Karthaus W.R., Gerlach J.P., Mohammed S., Heck A.J., Maurice M.M., Mahmoudi T., Clevers H. Wnt signaling through inhibition of β-catenin degradation in an intact Axin1 complex. Cell 2012, 149:1245-1256.
17. Ma L., Tao Y., Duran A., Llado V., Galvez A., Barger J.F., Castilla E.A., Chen J., Yajima T., Porollo A., et al. Control of nutrient stress-induced metabolic reprogramming by PKCζ in tumorigenesis. Cell 2013, 152:599-611.
18. Mao J., Wang J., Liu B., Pan W., Farr G.H., Flynn C., Yuan H., Takada S., Kimelman D., Li L., Wu D. Low-density lipoprotein receptor-related protein-5 binds to Axin and regulates the canonical Wnt signaling pathway. Mol. Cell 2001, 7:801-809.
19. Merlos-Suárez A., Barriga F.M., Jung P., Iglesias M., Céspedes M.V., Rossell D., Sevillano M., Hernando-Momblona X., da Silva-Diz V., Muñoz P., et al. The intestinal stem cell signature identifies colorectal cancer stem cells and predicts disease relapse. Cell Stem Cell 2011, 8:511-524.
20. Mo J.S., Park H.W., Guan K.L. The Hippo signaling pathway in stem cell biology and cancer. EMBO Rep. 2014, 15:642-656.
21. Moscat J., Diaz-Meco M.T., Wooten M.W. Of the atypical PKCs, Par-4 and p62: recent understandings of the biology and pathology of a PB1-dominated complex. Cell Death Differ. 2009, 16:1426-1437.
22. Niehrs C. The complex world of WNT receptor signalling. Nat. Rev. Mol. Cell Biol. 2012, 13:767-779.
23. Rosenbluh J., Nijhawan D., Cox A.G., Li X., Neal J.T., Schafer E.J., Zack T.I., Wang X., Tsherniak A., Schinzel A.C., et al. β-Catenin-driven cancers require a YAP1 transcriptional complex for survival and tumorigenesis. Cell 2012, 151:1457-1473.
24. Schepers A.G., Snippert H.J., Stange D.E., van den Born M., van Es J.H., van de Wetering M., Clevers H. Lineage tracing reveals Lgr5+ stem cell activity in mouse intestinal adenomas. Science 2012, 337:730-735.
25. Schwitalla S., Fingerle A.A., Cammareri P., Nebelsiek T., Göktuna S.I., Ziegler P.K., Canli O., Heijmans J., Huels D.J., Moreaux G., et al. Intestinal tumorigenesis initiated by dedifferentiation and acquisition of stem-cell-like properties. Cell 2013, 152:25-38.
26. Steinhardt A.A., Gayyed M.F., Klein A.P., Dong J., Maitra A., Pan D., Montgomery E.A., Anders R.A. Expression of Yes-associated protein in common solid tumors. Hum. Pathol. 2008, 39:1582-1589.
27. Tolwinski N.S., Wehrli M., Rives A., Erdeniz N., DiNardo S., Wieschaus E. Wg/Wnt signal can be transmitted through arrow/LRP5,6 and Axin independently of Zw3/Gsk3beta activity. Dev. Cell 2003, 4:407-418.
28. Touil Y., Igoudjil W., Corvaisier M., Dessein A.F., Vandomme J., Monté D., Stechly L., Skrypek N., Langlois C., Grard G., et al. Colon cancer cells escape 5FU chemotherapy-induced cell death by entering stemness and quiescence associated with the c-Yes/YAP axis. Clin. Cancer Res. 2014, 20:837-846.
29. Vermeulen L., Snippert H.J. Stem cell dynamics in homeostasis and cancer of the intestine. Nat. Rev. Cancer 2014, 14:468-480.
30. Wang L., Shi S., Guo Z., Zhang X., Han S., Yang A., Wen W., Zhu Q. Overexpression of YAP and TAZ is an independent predictor of prognosis in colorectal cancer and related to the proliferation and metastasis of colon cancer cells. PLoS ONE 2013, 8:e65539.
31. Wood L.D., Parsons D.W., Jones S., Lin J., Sjöblom T., Leary R.J., Shen D., Boca S.M., Barber T., Ptak J., et al. The genomic landscapes of human breast and colorectal cancers. Science 2007, 318:1108-1113.
32. Zhou D., Zhang Y., Wu H., Barry E., Yin Y., Lawrence E., Dawson D., Willis J.E., Markowitz S.D., Camargo F.D., Avruch J. 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. USA 2011, 108:E1312-E1320.