Opposing activities of the Ras and Hippo pathways converge on regulation of YAP protein turnover

EMBO Journal

Volumn 33, Issue 21, 2014, Pages 2447-2457

  Hong, Xin ^a,b   Nguyen, Hung Thanh ^c   Chen, Qingfeng ^a,d   Zhang, Rui ^e   Hagman, Zandra ^f   Voorhoeve, P Mathijs ^c   Cohen, Stephen M ^a,b  

^a INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^c DUKE NUS MEDICAL SCHOOL   (Singapore)

^d SINGAPORE MIT ALLIANCE FOR RESEARCH AND TECHNOLOGY   (Singapore)

^e STANFORD UNIVERSITY   (United States)

^f UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

anchorage independence; Hippo pathway; primary cell transformation; RasV12; tumor suppressor

Indexed keywords

AGAR; AMPHIREGULIN; EPIDERMAL GROWTH FACTOR RECEPTOR; HIPPO PROTEIN; MONOCLONAL ANTIBODY; PROTEIN; RAS PROTEIN; SHORT HAIRPIN RNA; SMALL INTERFERING RNA; SUPPRESSOR OF CYTOKINE SIGNALING; SUPPRESSOR OF CYTOKINE SIGNALING 5; SUPPRESSOR OF CYTOKINE SIGNALING 6; TRANSCRIPTION FACTOR YAP1; UNCLASSIFIED DRUG; BETA TRANSDUCIN REPEAT CONTAINING PROTEIN; BTRC PROTEIN, HUMAN; EGFR PROTEIN, HUMAN; HIPPO PROTEIN, HUMAN; PHOSPHOPROTEIN; PROTEIN SERINE THREONINE KINASE; SIGNAL TRANSDUCING ADAPTOR PROTEIN; SOCS5 PROTEIN, HUMAN; SOCS6 PROTEIN, HUMAN; UBIQUITIN PROTEIN LIGASE; YAP1 (YES-ASSOCIATED) PROTEIN, HUMAN;

ANCHORAGE INDEPENDENT GROWTH; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CARCINOGENESIS; CELL TRANSFORMATION; COLONY FORMATION; COLORECTAL CARCINOMA; CONTROLLED STUDY; CUTANEOUS MELANOMA; DOWN REGULATION; GENETIC TRANSFECTION; GLIOBLASTOMA; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOPRECIPITATION; IN VITRO STUDY; IN VIVO STUDY; LUCIFERASE ASSAY; MOUSE; NONHUMAN; POSITIVE FEEDBACK; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN METABOLISM; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; TUMOR XENOGRAFT; UBIQUITINATION; UPREGULATION; GENETICS; HEK293 CELL LINE; IMMUNOLOGY; METABOLISM; PATHOLOGY; SIGNAL TRANSDUCTION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; BETA-TRANSDUCIN REPEAT-CONTAINING PROTEINS; CELL TRANSFORMATION, NEOPLASTIC; HEK293 CELLS; HUMANS; PHOSPHOPROTEINS; PROTEIN STABILITY; PROTEIN-SERINE-THREONINE KINASES; RAS PROTEINS; RECEPTOR, EPIDERMAL GROWTH FACTOR; SIGNAL TRANSDUCTION; SKP CULLIN F-BOX PROTEIN LIGASES; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS; UP-REGULATION;

EID: 84922262192     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.15252/embj.201489385     Document Type: Article

References (49)

1. Barry ER, Camargo FD, (2013) The Hippo superhighway: signaling crossroads converging on the Hippo/Yap pathway in stem cells and development. Curr Opin Cell Biol 25: 247-253
2. Cai J, Zhang N, Zheng Y, de Wilde RF, Maitra A, Pan D, (2010) The Hippo signaling pathway restricts the oncogenic potential of an intestinal regeneration program. Genes Dev 24: 2383-2388
3. Chen Q, Khoury M, 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
4. Di Fiore F, Sesboue R, Michel P, Sabourin JC, Frebourg T, (2010) Molecular determinants of anti-EGFR sensitivity and resistance in metastatic colorectal cancer. Br J Cancer 103: 1765-1772
5. Dong J, Feldmann G, Huang J, Wu S, Zhang N, Comerford SA, Gayyed MF, Anders RA, Maitra A, Pan D, (2007) Elucidation of a universal size-control mechanism in Drosophila and mammals. Cell 130: 1120-1133
6. Dupont S, Morsut L, Aragona M, Enzo E, Giulitti S, Cordenonsi M, Zanconato F, Le Digabel J, Forcato M, Bicciato S, Elvassore N, Piccolo S, (2011) Role of YAP/TAZ in mechanotransduction. Nature 474: 179-183
7. Elenbaas B, Spirio L, Koerner F, Fleming MD, Zimonjic DB, Donaher JL, Popescu NC, Hahn WC, Weinberg RA, (2001) Human breast cancer cells generated by oncogenic transformation of primary mammary epithelial cells. Genes Dev 15: 50-65
8. Eser S, Reiff N, Messer M, Seidler B, Gottschalk K, Dobler M, Hieber M, Arbeiter A, Klein S, Kong B, Michalski CW, Schlitter AM, Esposito I, Kind AJ, Rad L, Schnieke AE, Baccarini M, Alessi DR, Rad R, Schmid RM, et al, (2013) Selective Requirement of PI3K/PDK1 Signaling for Kras Oncogene-Driven Pancreatic Cell Plasticity and Cancer. Cancer Cell 23: 406-420
9. Fearon ER, Cho KR, Nigro JM, Kern SE, Simons JW, Ruppert JM, Hamilton SR, Preisinger AC, Thomas G, Kinzler KW, Vogelstein B, (1990) Identification of a chromosome 18q gene that is altered in colorectal cancers. Science 247: 49-56
10. Fulda S, Rajalingam K, Dikic I, (2012) Ubiquitylation in immune disorders and cancer: from molecular mechanisms to therapeutic implications. EMBO Mol Med 4: 545-556
11. Gaedcke J, Grade M, Jung K, Camps J, Jo P, Emons G, Gehoff A, Sax U, Schirmer M, Becker H, Beissbarth T, Ried T, Ghadimi BM, (2010) Mutated KRAS results in overexpression of DUSP4, a MAP-kinase phosphatase, and SMYD3, a histone methyltransferase, in rectal carcinomas. Genes Chromosomes Cancer 49: 1024-1034
12. Hahn WC, Counter CM, Lundberg AS, Beijersbergen RL, Brooks MW, Weinberg RA, (1999) Creation of human tumour cells with defined genetic elements. Nature 400: 464-468
13. Hahn WC, Dessain SK, Brooks MW, King JE, Elenbaas B, Sabatini DM, DeCaprio JA, Weinberg RA, (2002) Enumeration of the simian virus 40 early region elements necessary for human cell transformation. Mol Cell Biol 22: 2111-2123
14. Hao Y, Chun A, Cheung K, Rashidi B, Yang X, (2008) Tumor suppressor LATS1 is a negative regulator of oncogene YAP. J Biol Chem 283: 5496-5509
15. Harvey KF, Zhang X, Thomas DM, (2013) The Hippo pathway and human cancer. Nat Rev Cancer 13: 246-257
16. Heallen T, Zhang M, Wang J, Bonilla-Claudio M, Klysik E, Johnson RL, Martin JF, (2011) Hippo pathway inhibits Wnt signaling to restrain cardiomyocyte proliferation and heart size. Science 332: 458-461
17. Herranz H, Hong X, Hung NT, Voorhoeve PM, Cohen SM, (2012) Oncogenic cooperation between SOCS family proteins and EGFR identified using a Drosophila epithelial transformation model. Genes Dev 26: 1602-1611
18. Hong X, Hammell M, Ambros V, Cohen SM, (2009) Immunopurification of Ago1 miRNPs selects for a distinct class of microRNA targets. Proc Natl Acad Sci USA 106: 15085-15090
19. Iwatsuki M, Mimori K, Ishii H, Yokobori T, Takatsuno Y, Sato T, Toh H, Onoyama I, Nakayama KI, Baba H, Mori M, (2010) Loss of FBXW7, a cell cycle regulating gene, in colorectal cancer: clinical significance. Int J Cancer 126: 1828-1837
20. Johnson R, Halder G, (2014) The two faces of Hippo: targeting the Hippo pathway for regenerative medicine and cancer treatment. Nat Rev Drug Discov 13: 63-79
21. Kapoor A, Yao W, Ying H, Hua S, Liewen A, Wang Q, Zhong Y, Wu CJ, Sadanandam A, Hu B, Chang Q, Chu GC, Al-Khalil R, Jiang S, Xia H, Fletcher-Sananikone E, Lim C, Horwitz GI, Viale A, Pettazzoni P, et al, (2014) Yap1 activation enables bypass of oncogenic kras addiction in pancreatic cancer. Cell 158: 185-197
22. Lei QY, Zhang H, Zhao B, Zha ZY, Bai F, Pei XH, Zhao S, Xiong Y, Guan KL, (2008) TAZ promotes cell proliferation and epithelial-mesenchymal transition and is inhibited by the hippo pathway. Mol Cell Biol 28: 2426-2436
23. Linossi EM, Nicholson SE, (2012) The SOCS box-adapting proteins for ubiquitination and proteasomal degradation. IUBMB Life 64: 316-323
24. Liu CY, Zha ZY, Zhou X, Zhang H, Huang W, Zhao D, Li T, Chan SW, Lim CJ, Hong W, Zhao S, Xiong Y, Lei QY, Guan KL, (2010) The hippo tumor pathway promotes TAZ degradation by phosphorylating a phosphodegron and recruiting the SCF{beta}-TrCP E3 ligase. J Biol Chem 285: 37159-37169
25. Liu AM, Xu Z, Luk JM, (2012) An update on targeting Hippo-YAP signaling in liver cancer. Expert Opin Ther Targets 16: 243-247
26. Liu-Chittenden Y, Huang B, Shim JS, Chen Q, Lee SJ, Anders RA, Liu JO, Pan D, (2012) Genetic and pharmacological disruption of the TEAD-YAP complex suppresses the oncogenic activity of YAP. Genes Dev 26: 1300-1305
27. Mao JH, Perez-Losada J, Wu D, Delrosario R, Tsunematsu R, Nakayama KI, Brown K, Bryson S, Balmain A, (2004) Fbxw7/Cdc4 is a p53-dependent, haploinsufficient tumour suppressor gene. Nature 432: 775-779
28. Marmor MD, Yarden Y, (2004) Role of protein ubiquitylation in regulating endocytosis of receptor tyrosine kinases. Oncogene 23: 2057-2070
29. Matallanas D, Romano D, Al-Mulla F, O'Neill E, Al-Ali W, Crespo P, Doyle B, Nixon C, Sansom O, Drosten M, Barbacid M, Kolch W, (2011) Mutant K-Ras activation of the proapoptotic MST2 pathway is antagonized by wild-type K-Ras. Mol Cell 44: 893-906
30. Moberg KH, Bell DW, Wahrer DC, Haber DA, Hariharan IK, (2001) Archipelago regulates Cyclin E levels in Drosophila and is mutated in human cancer cell lines. Nature 413: 311-316
31. Pan D, (2010) The hippo signaling pathway in development and cancer. Dev Cell 19: 491-505
32. Prahallad A, Sun C, Huang S, Di Nicolantonio F, Salazar R, Zecchin D, Beijersbergen RL, Bardelli A, Bernards R, (2012) Unresponsiveness of colon cancer to BRAF(V600E) inhibition through feedback activation of EGFR. Nature 483: 100-103
33. Qiu X, Zheng J, Guo X, Gao X, Liu H, Tu Y, Zhang Y, (2013) Reduced expression of SOCS2 and SOCS6 in hepatocellular carcinoma correlates with aggressive tumor progression and poor prognosis. Mol Cell Biochem 378: 99-106
34. Reddy BV, Irvine KD, (2013) Regulation of Hippo signaling by EGFR-MAPK signaling through Ajuba family proteins. Dev Cell 24: 459-471
35. Shao DD, Xue W, Krall EB, Bhutkar A, Piccioni F, Wang X, Schinzel AC, Sood S, Rosenbluh J, Kim JW, Zwang Y, Roberts TM, Root DE, Jacks T, Hahn WC, (2014) KRAS and YAP1 Converge to Regulate EMT and Tumor Survival. Cell 158: 171-184
36. Strohmaier H, Spruck CH, Kaiser P, Won KA, Sangfelt O, Reed SI, (2001) Human F-box protein hCdc4 targets cyclin E for proteolysis and is mutated in a breast cancer cell line. Nature 413: 316-322
37. TCGA Network (2012) Comprehensive molecular characterization of human colon and rectal cancer. Nature 487: 330-337
38. Voorhoeve PM, Agami R, (2003) The tumor-suppressive functions of the human INK4A locus. Cancer Cell 4: 311-319
39. Voorhoeve PM, le Sage C, Schrier M, Gillis AJ, Stoop H, Nagel R, Liu YP, van Duijse J, Drost J, Griekspoor A, Zlotorynski E, Yabuta N, De Vita G, Nojima H, Looijenga LH, Agami R, (2006) A genetic screen implicates miRNA-372 and miRNA-373 as oncogenes in testicular germ cell tumors. Cell 124: 1169-1181
40. Wang L, Shi S, Guo Z, Zhang X, Han S, Yang A, Wen W, Zhu Q, (2013) 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 8: e65539
41. Wang Z, Liu P, Inuzuka H, Wei W, (2014) Roles of F-box proteins in cancer. Nat Rev Cancer 14: 233-247
42. Yin F, Yu J, Zheng Y, Chen Q, Zhang N, Pan D, (2013) Spatial organization of Hippo signaling at the plasma membrane mediated by the tumor suppressor Merlin/NF2. Cell 154: 1342-1355
43. Young A, Lou D, McCormick F, (2013) Oncogenic and wild-type Ras play divergent roles in the regulation of mitogen-activated protein kinase signaling. Cancer Discov 3: 112-123
44. Yuen HF, McCrudden CM, Huang YH, Tham JM, Zhang X, Zeng Q, Zhang SD, Hong W, (2013) TAZ expression as a prognostic indicator in colorectal cancer. PLoS ONE 8: e54211
45. Zhang J, Ji JY, Yu M, Overholtzer M, Smolen GA, Wang R, Brugge JS, Dyson NJ, Haber DA, (2009) YAP-dependent induction of amphiregulin identifies a non-cell-autonomous component of the Hippo pathway. Nat Cell Biol 11: 1444-1450
46. Zhao B, Wei X, Li W, Udan RS, Yang Q, Kim J, Xie J, Ikenoue T, Yu J, Li L, Zheng P, Ye K, Chinnaiyan A, Halder G, Lai ZC, Guan KL, (2007) Inactivation of YAP oncoprotein by the Hippo pathway is involved in cell contact inhibition and tissue growth control. Genes Dev 21: 2747-2761
47. Zhao B, Ye X, Yu J, Li L, Li W, Li S, Lin JD, Wang CY, Chinnaiyan AM, Lai ZC, Guan KL, (2008) TEAD mediates YAP-dependent gene induction and growth control. Genes Dev 22: 1962-1971
48. Zhao B, Li L, Tumaneng K, Wang CY, Guan KL, (2010) A coordinated phosphorylation by Lats and CK1 regulates YAP stability through SCF(beta-TRCP). Genes Dev 24: 72-85
49. Zhu JG, Dai QS, Han ZD, He HC, Mo RJ, Chen G, Chen YF, Wu YD, Yang SB, Jiang FN, Chen WH, Sun ZL, Zhong WD, (2013) Expression of SOCSs in human prostate cancer and their association in prognosis. Mol Cell Biochem 381: 51-59