Browse > Article
http://dx.doi.org/10.5483/BMBRep.2018.51.3.015

DNA binding partners of YAP/TAZ  

Kim, Min-Kyu (Department of Biochemistry, College of Medicine, and Institute for Tumor Research, Chungbuk National University)
Jang, Ju-Won (Department of Biochemistry, College of Medicine, and Institute for Tumor Research, Chungbuk National University)
Bae, Suk-Chul (Department of Biochemistry, College of Medicine, and Institute for Tumor Research, Chungbuk National University)
Publication Information
BMB Reports / v.51, no.3, 2018 , pp. 126-133 More about this Journal
Abstract
Hippo signaling plays critical roles in regulation of tissue homeostasis, organ size, and tumorigenesis by inhibiting YES-associated protein (YAP) and PDZ-binding protein TAZ through MST1/2 and LATS1/2 pathway. It is also engaged in cross-talk with various other signaling pathways, including WNT, BMPs, Notch, GPCRs, and Hedgehog to further modulate activities of YAP/TAZ. Because YAP and TAZ are transcriptional coactivators that lack DNA-binding activity, both proteins must interact with DNA-binding transcription factors to regulate target gene's expression. To activate target genes involved in cell proliferation, TEAD family members are major DNA-binding partners of YAP/TAZ. Accordingly, YAP/TAZ were originally classified as oncogenes. However, YAP might also play tumor-suppressing role. For example, YAP can bind to DNA-binding tumor suppressors including RUNXs and p73. Thus, YAP might act either as an oncogene or tumor suppressor depending on its binding partners. Here, we summarize roles of YAP depending on its DNA-binding partners and discuss context-dependent functions of YAP/TAZ.
Keywords
LATS1/2; MST1/2; RUNX; TAZ; TEAD; YAP;
Citations & Related Records
연도 인용수 순위
  • Reference
1 Strano S, Munarriz E, Rossi M et al (2001) Physical interaction with Yes-associated protein enhances p73 transcriptional activity. J Biol Chem 276, 15164-15173   DOI
2 Del Mare S and Aqeilan RI (2015) Tumor Suppressor WWOX inhibits osteosarcoma metastasis by modulating RUNX2 function. Sci Rep 5, 12959   DOI
3 Das A, Chendil D, Dey S et al (2001) Ionizing radiation down-regulates p53 protein in primary Egr-1-/- mouse embryonic fibroblast cells causing enhanced resistance to apoptosis. J Biol Chem 276, 3279-3286   DOI
4 Murakami M, Nakagawa M, Olson EN and Nakagawa O (2005) A WW domain protein TAZ is a critical coactivator for TBX5, a transcription factor implicated in Holt-Oram syndrome. Proc Natl Acad Sci U S A 102, 18034-18039   DOI
5 Derynck R and Zhang YE (2003) Smad-dependent and Smad-independent pathways in TGF-beta family signalling. Nature 425, 577-584   DOI
6 Varelas X, Sakuma R, Samavarchi-Tehrani P et al (2008) TAZ controls Smad nucleocytoplasmic shuttling and regulates human embryonic stem-cell self-renewal. Nat Cell Biol 10, 837-848   DOI
7 Varelas X, Samavarchi-Tehrani P, Narimatsu M et al (2010) The Crumbs complex couples cell density sensing to Hippo-dependent control of the TGF-beta-SMAD pathway. Dev Cell 19, 831-844   DOI
8 Jacquemin P, Sapin V, Alsat E, Evain-Brion D, Dolle P and Davidson I (1998) Differential expression of the TEF family of transcription factors in the murine placenta and during differentiation of primary human trophoblasts in vitro. Dev Dyn 212, 423-436   DOI
9 Li Z, Zhao B, Wang P et al (2010) Structural insights into the YAP and TEAD complex. Genes Dev 24, 235-240   DOI
10 Chen L, Loh PG and Song H (2010) Structural and functional insights into the TEAD-YAP complex in the Hippo signaling pathway. Protein Cell 1, 1073-1083   DOI
11 Zhao B, Ye X, Yu J et al (2008) TEAD mediates YAP-dependent gene induction and growth control. Genes Dev 22, 1962-1971   DOI
12 Mo JS, Meng Z, Kim YC et al (2015) Cellular energy stress induces AMPK-mediated regulation of YAP and the Hippo pathway. Nat Cell Biol 17, 500-510   DOI
13 Zhao B, Lei QY and Guan K L (2008) The Hippo-YAP pathway: new connections between regulation of organ size and cancer. Curr Opin Cell Biol 20, 638-646   DOI
14 Zhou Y, Huang T Cheng AS, Yu J, Kang W and To KF (2016) The TEAD Family and Its Oncogenic Role in Promoting Tumorigenesis. Int J Mol Sci 17, 1-15
15 Hiemer SE, Szymaniak AD and Varelas X (2014) The transcriptional regulators TAZ and YAP direct transforming growth factor beta-induced tumorigenic phenotypes in breast cancer cells. J Biol Chem 289, 13461-13474   DOI
16 Rashidian J, Le Scolan E, Ji X et al (2015) Ski regulates Hippo and TAZ signaling to suppress breast cancer progression. Sci Signal 8, ra14   DOI
17 Kaneko KJ and DePamphilis ML (1998) Regulation of gene expression at the beginning of mammalian development and the TEAD family of transcription factors. Dev Genet 22, 43-55   DOI
18 You B, Yang YL, Xu Z et al (2015) Inhibition of ERK1/2 down-regulates the Hippo/YAP signaling pathway in human NSCLC cells. Oncotarget 6, 4357-4368
19 Nguyen LT, Tretiakova MS, Silvis MR et al (2015) ERG Activates the YAP1 Transcriptional Program and Induces the Development of Age-Related Prostate Tumors. Cancer Cell 27, 797-808   DOI
20 Chan LH, Wang W, Yeung W, Deng Y, Yuan P and Mak KK (2014) Hedgehog signaling induces osteosarcoma development through Yap1 and H19 overexpression. Oncogene 33, 4857-4866   DOI
21 Zhang W, Nandakumar N, Shi Y et al (2014) Downstream of mutant KRAS, the transcription regulator YAP is essential for neoplastic progression to pancreatic ductal adenocarcinoma. Sci Signal 7, ra42   DOI
22 Cai H and Xu Y (2013) The role of LPA and YAP signaling in long-term migration of human ovarian cancer cells. Cell Commun Signal 11, 31   DOI
23 Artinian N, Cloninger C, Holmes B, Benavides-Serrato A, Bashir T and Gera J (2015) Phosphorylation of the Hippo Pathway Component AMOTL2 by the mTORC2 Kinase Promotes YAP Signaling, Resulting in Enhanced Glioblastoma Growth and Invasiveness. J Biol Chem 290, 19387-19401   DOI
24 Yu FX, Luo J, Mo JS et al (2014) Mutant Gq/11 promote uveal melanoma tumorigenesis by activating YAP. Cancer Cell 25, 822-830   DOI
25 Serrano I, McDonald PC, Lock F, Muller WJ and Dedhar S (2013) Inactivation of the Hippo tumour suppressor pathway by integrin-linked kinase. Nat Commun 4, 2976
26 Wang J, Park JS, Wei Y et al (2013) TRIB2 acts downstream of Wnt/TCF in liver cancer cells to regulate YAP and C/EBPalpha function. Mol Cell 51, 211-225   DOI
27 Liu AM, Xu Z and Luk JM (2012) An update on targeting Hippo-YAP signaling in liver cancer. Expert Opin Ther Targets 16, 243-247   DOI
28 Li C, Srivastava RK, Elmets CA, Afaq F and Athar M (2013) Arsenic-induced cutaneous hyperplastic lesions are associated with the dysregulation of Yap, a Hippo signaling-related protein. Biochem Biophys Res Commun 438, 607-612   DOI
29 Thongon N, Castiglioni I, Zucal C et al (2016) The GSK3beta inhibitor BIS I reverts YAP-dependent EMT signature in PDAC cell lines by decreasing SMADs expression level. Oncotarget 7, 26551-26566
30 Pobbati AV and Hong W (2013) Emerging roles of TEAD transcription factors and its coactivators in cancers. Cancer Biol Ther 14, 390-398   DOI
31 Zawacka-Pankau J, Kostecka A, Sznarkowska A, Hedstrom E and Kawiak A (2010) p73 tumor suppressor protein: a close relative of p53 not only in structure but also in anti-cancer approach? Cell Cycle 9, 720-728   DOI
32 Basu S, Totty NF, Irwin MS, Sudol M and Downward J (2003) Akt phosphorylates the Yes-associated protein, YAP, to induce interaction with 14-3-3 and attenuation of p73-mediated apoptosis. Mol Cell 11, 11-23   DOI
33 Strano S, Monti O, Pediconi N et al (2005) The transcriptional coactivator Yes-associated protein drives p73 gene-target specificity in response to DNA Damage. Mol Cell 18, 447-459   DOI
34 Oka T, Mazack V and Sudol M (2008) Mst2 and Lats kinases regulate apoptotic function of Yes kinaseassociated protein (YAP). J Biol Chem 283, 27534-27546   DOI
35 Rossi M, De Laurenzi V, Munarriz E et al (2005) The ubiquitin-protein ligase Itch regulates p73 stability. EMBO J 24, 836-848   DOI
36 Bernassola F, Salomoni P, Oberst A et al (2004) Ubiquitin-dependent degradation of p73 is inhibited by PML. J Exp Med 199, 1545-1557   DOI
37 Okazaki T, Kageji T, Kuwayama K et al (2012) Upregulation of endogenous PML induced by a combination of interferon-beta and temozolomide enhances p73/YAPmediated apoptosis in glioblastoma. Cancer Lett 323, 199-207   DOI
38 Cottini F, Hideshima T, Xu C et al (2014) Rescue of Hippo coactivator YAP1 triggers DNA damage-induced apoptosis in hematological cancers. Nat Med 20, 599-606   DOI
39 Levy D, Adamovich Y, Reuven N and Shaul Y (2008) Yap1 phosphorylation by c-Abl is a critical step in selective activation of proapoptotic genes in response to DNA damage. Mol Cell 29, 350-361   DOI
40 Levy D, AdamovichY, Reuven N and Shaul Y (2007) The Yes-associated protein 1 stabilizes p73 by preventing Itch-mediated ubiquitination of p73. Cell Death Differ 14, 743-751   DOI
41 Lapi E, Di Agostino S, Donzelli S et al (2008) PML, YAP, and p73 are components of a proapoptotic autoregulatory feedback loop. Mol Cell 32, 803-814   DOI
42 Keshet R, Adler J, Ricardo Lax I et al (2015) c-Abl antagonizes the YAP oncogenic function. Cell Death Differ 22, 935-945   DOI
43 Rosenbluh J, Nijhawan D, Cox AG et al (2012) beta-Catenin-driven cancers require a YAP1 transcriptional complex for survival and tumorigenesis. Cell 151, 1457-1473   DOI
44 Zaidi SK, Sullivan AJ, Medina R et al (2004) Tyrosine phosphorylation controls Runx2-mediated subnuclear targeting of YAP to repress transcription. EMBO J 23, 790-799   DOI
45 Omerovic J, Puggioni EM, Napoletano S et al (2004) Ligand-regulated association of ErbB-4 to the transcriptional co-activator YAP65 controls transcription at the nuclear level. Exp Cell Res 294, 469-479   DOI
46 Haskins JW, Nguyen DX and Stern DF (2014) Neuregulin 1-activated ERBB4 interacts with YAP to induce Hippo pathway target genes and promote cell migration. Sci Signal 7, ra116   DOI
47 Schuchardt BJ, Bhat V, Mikles DC, McDonald CB, Sudol M and Farooq A (2014) Molecular basis of the binding of YAP transcriptional regulator to the ErbB4 receptor tyrosine kinase. Biochimie 101, 192-202   DOI
48 Harvey K and Tapon N (2007) The Salvador-Warts-Hippo pathway - an emerging tumour-suppressor network. Nat Rev Cancer 7, 182-191   DOI
49 Zhao B, Wei X, Li W 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   DOI
50 Camargo FD, Gokhale S, Johnnidis JB et al (2007) YAP1 increases organ size and expands undifferentiated progenitor cells. Curr Biol 17, 2054-2060   DOI
51 Dong J, Feldmann G, Huang J et al (2007) Elucidation of a universal size-control mechanism in Drosophila and mammals. Cell 130, 1120-1133   DOI
52 Huang J, Wu S, Barrera J, Matthews K and Pan D (2005) The Hippo signaling pathway coordinately regulates cell proliferation and apoptosis by inactivating Yorkie, the Drosophila Homolog of YAP. Cell 122, 421-434   DOI
53 Fang KS, Barker K, Sudol M and Hanafusa H (1994) A transmembrane protein-tyrosine phosphatase contains spectrin-like repeats in its extracellular domain. J Biol Chem 269, 14056-14063
54 Zhu C, Li L and Zhao B (2015) The regulation and function of YAP transcription co-activator. Acta Biochim Biophys Sin (Shanghai) 47, 16-28   DOI
55 Komori T, Yagi H, Nomura S et al (1997) Targeted disruption of Cbfa1 results in a complete lack of bone formation owing to maturational arrest of osteoblasts. Cell 89, 755-764   DOI
56 Otto F, Thornell AP, Crompton T et al (1997) Cbfa1, a candidate gene for cleidocranial dysplasia syndrome, is essential for osteoblast differentiation and bone development. Cell 89, 765-771   DOI
57 Marzia M, Sims NA, Voit S et al (2000) Decreased c-Src expression enhances osteoblast differentiation and bone formation. J Cell Biol 151, 311-320   DOI
58 Sudol M, Bork P, Einbond A et al (1995) Characterization of the mammalian YAP (Yes-associated protein) gene and its role in defining a novel protein module, the WW domain. J Biol Chem 270, 14733-14741   DOI
59 Kanai F, Marignani PA, Sarbassova D et al (2000) TAZ: a novel transcriptional co-activator regulated by interactions with 14-3-3 and PDZ domain proteins. EMBO J 19, 6778-6791   DOI
60 Saucedo LJ and Edgar BA (2007) Filling out the Hippo pathway. Nat Rev Mol Cell Biol 8, 613-621   DOI
61 Soriano P, Montgomery C, Geske R and Bradley A (1991) Targeted disruption of the c-src proto-oncogene leads to osteopetrosis in mice. Cell 64, 693-702   DOI
62 Hong JH, Hwang ES, McManus MT et al (2005) TAZ, a transcriptional modulator of mesenchymal stem cell differentiation. Science 309, 1074-1078   DOI
63 Li QL, Ito K, Sakakura C et al (2002) Causal relationship between the loss of RUNX3 expression and gastric cancer. Cell 109, 113-124   DOI
64 Jang JW, Kim MK, Lee YS et al (2017) RAC-LATS1/2 signaling regulates YAP activity by switching between the YAP-binding partners TEAD4 and RUNX3. Oncogene 36, 999-1011   DOI
65 Zender L, Spector MS, Xue W et al (2006) Identification and validation of oncogenes in liver cancer using an integrative oncogenomic approach. Cell 125, 1253-1267   DOI
66 Grannas K, Arngarden L, Lonn P et al (2015) Crosstalk between Hippo and TGFbeta: Subcellular Localization of YAP/TAZ/Smad Complexes. J Mol Biol 427, 3407-3415   DOI
67 Barry ER, Morikawa T, Butler BL et al (2013) Restriction of intestinal stem cell expansion and the regenerative response by YAP. Nature 493, 106-110
68 Morin-Kensicki EM, Boone BN, Howell M et al (2006) Defects in yolk sac vasculogenesis, chorioallantoic fusion, and embryonic axis elongation in mice with targeted disruption of Yap65. Mol Cell Biol 26, 77-87   DOI
69 Hall CA, Wang R, Miao J et al (2010) Hippo pathway effector Yap is an ovarian cancer oncogene. Cancer Res 70, 8517-8525   DOI
70 Wang Y, Dong Q, Zhang Q, Li Z, Wang E and Qiu X (2010) Overexpression of yes-associated protein contributes to progression and poor prognosis of non-small-cell lung cancer. Cancer Sci 101, 1279-1285   DOI
71 Zhou Z, Zhu JS and Xu ZP (2011) RNA interference mediated YAP gene silencing inhibits invasion and metastasis of human gastric cancer cell line SGC-7901. Hepatogastroenterology 58, 2156-2161
72 Chan SW, Lim CJ, Loo LS, Chong YF, Huang C and Hong W (2009) TEADs mediate nuclear retention of TAZ to promote oncogenic transformation. J Biol Chem 284, 14347-14358   DOI
73 Yu FX, Zhao B, Panupinthu N et al (2012) Regulation of the Hippo-YAP pathway by G-protein-coupled receptor signaling. Cell 150, 780-791   DOI
74 Mo JS, Yu FX, Gong R, Brown JH and Guan KL (2012) Regulation of the Hippo-YAP pathway by proteaseactivated receptors (PARs). Genes Dev 26, 2138-2143   DOI
75 Liu-Chittenden Y, Huang B, Shim JS et al (2012) Genetic and pharmacological disruption of the TEAD-YAP complex suppresses the oncogenic activity of YAP. Genes Dev 26, 1300-1305   DOI
76 Zhao B, Kim J, Ye X, Lai ZC and Guan KL (2009) Both TEAD-binding and WW domains are required for the growth stimulation and oncogenic transformation activity of yes-associated protein. Cancer Res 69, 1089-1098
77 Zhang H, Pasolli HA and Fuchs E (2011) Yes-associated protein (YAP) transcriptional coactivator functions in balancing growth and differentiation in skin. Proc Natl Acad Sci U S A 108, 2270-2275   DOI
78 Fernandez LA, Squatrito M, Northcott P et al (2012) Oncogenic YAP promotes radioresistance and genomic instability in medulloblastoma through IGF2-mediated Akt activation. Oncogene 31, 1923-1937   DOI
79 Fujii M, Nakanishi H, Toyoda T et al (2012) Convergent signaling in the regulation of connective tissue growth factor in malignant mesothelioma: TGFbeta signaling and defects in the Hippo signaling cascade. Cell Cycle 11, 3373-3379   DOI
80 Xia Y, Zhang YL, Yu C, Chang T and Fan HY (2014) YAP/TEAD co-activator regulated pluripotency and chemoresistance in ovarian cancer initiated cells. PLoS One 9, e109575   DOI
81 Chen L, Chan SW, Zhang X et al (2010) Structural basis of YAP recognition by TEAD4 in the hippo pathway. Genes Dev 24, 290-300   DOI
82 Fossdal R, Jonasson F, Kristjansdottir GT et al (2004) A novel TEAD1 mutation is the causative allele in Sveinsson's chorioretinal atrophy (helicoid peripapillary chorioretinal degeneration). Hum Mol Genet 13, 975-981   DOI
83 Kitagawa M (2007) A Sveinsson's chorioretinal atrophyassociated missense mutation in mouse Tead1 affects its interaction with the co-factors YAP and TAZ. Biochem Biophys Res Commun 361, 1022-1026   DOI
84 Zhang J, Ji JY, Yu M et al (2009) YAP-dependent induction of amphiregulin identifies a non-cell-autonomous component of the Hippo pathway. Nat Cell Biol 11, 1444-1450   DOI
85 Yang N, Morrison CD, Liu P et al (2012) TAZ induces growth factor-independent proliferation through activation of EGFR ligand amphiregulin. Cell Cycle 11, 2922-2930   DOI
86 Neto-Silva RM, de Beco S and Johnston LA (2010) Evidence for a growth-stabilizing regulatory feedback mechanism between Myc and Yorkie, the Drosophila homolog of Yap. Dev Cell 19, 507-520   DOI
87 Komuro A, Nagai M, Navin NE 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   DOI
88 Zagurovskaya M, Shareef MM, Das A et al (2009) EGR-1 forms a complex with YAP-1 and upregulates Bax expression in irradiated prostate carcinoma cells. Oncogene 28, 1121-1131   DOI
89 Qiao Y, Lin SJ, Chen Y et al (2016) RUNX3 is a novel negative regulator of oncogenic TEAD-YAP complex in gastric cancer. Oncogene 35, 2664-2674   DOI
90 Yagi R, Chen LF, Shigesada K, Murakami Y and Ito Y (1999) A WW domain-containing yes-associated protein (YAP) is a novel transcriptional co-activator. EMBO J 18, 2551-2562   DOI
91 Ferrigno O, Lallemand F, Verrecchia F et al (2002) Yes-associated protein (YAP65) interacts with Smad7 and potentiates its inhibitory activity against TGF-beta/Smad signaling. Oncogene 21, 4879-4884   DOI
92 Kurisaki A, Kose S, Yoneda Y, Heldin CH and Moustakas A (2001) Transforming growth factor-beta induces nuclear import of Smad3 in an importin-beta1 and Ran-dependent manner. Mol Biol Cell 12, 1079-1091   DOI
93 Vassilev A, Kaneko KJ, Shu H, Zhao Y and DePamphilis ML (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   DOI
94 Xiao JH, Davidson I, Matthes H, Garnier JM and Chambon P (1991) Cloning, expression, and transcriptional properties of the human enhancer factor TEF-1. Cell 65, 551-568   DOI
95 Aqeilan RI, Kuroki T, Pekarsky Y et al (2004) Loss of WWOX expression in gastric carcinoma. Clin Cancer Res 10, 3053-3058   DOI
96 Aqeilan RI, Donati V, Gaudio E et al (2007) Association of Wwox with ErbB4 in breast cancer. Cancer Res 67, 9330-9336   DOI
97 Aqeilan RI, Hassan MQ, de Bruin A et al (2008) The WWOX tumor suppressor is essential for postnatal survival and normal bone metabolism. J Biol Chem 283, 21629-21639   DOI
98 Aqeilan RI, Donati V, Palamarchuk A et al (2005) WW domain-containing proteins, WWOX and YAP, compete for interaction with ErbB-4 and modulate its transcriptional function. Cancer Res 65, 6764-6772   DOI