Regulation of TAZ in cancer

Xin Zhou, Qun-Ying Lei

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Protein Cell ›› 2016, Vol. 7 ›› Issue (8) : 548-561. DOI: 10.1007/s13238-016-0288-z
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Regulation of TAZ in cancer

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Abstract

TAZ, a transcriptional coactivator with PDZ-binding motif, is encoded by WWTR1 gene (WW domain containing transcription regulator 1). TAZ is tightly regulated in the hippo pathway-dependent and-independent manner in response to a wide range of extracellular and intrinsic signals, including cell density, cell polarity, F-actin related mechanical stress, ligands of G protein-coupled receptors (GPCRs), cellular energy status, hypoxia and osmotic stress. Besides its role in normal tissue development, TAZplays critical roles in cell proliferation, differentiation, apoptosis, migration, invasion, epithelial-mesenchymal transition (EMT), and stemness in multiple human cancers. We discuss here the regulators and regulation of TAZ. We also highlight the tumorigenic roles of TAZ and its potential therapeutic impact in human cancers.

Keywords

TAZ / the Hippo pathway / cancer

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Xin Zhou, Qun-Ying Lei. Regulation of TAZ in cancer. Protein Cell, 2016, 7(8): 548‒561 https://doi.org/10.1007/s13238-016-0288-z

References

[1]
Bao S, Wu Q, McLendon RE, Hao Y, Shi Q, Hjelmeland AB, Dewhirst MW, Bigner DD, Rich JN (2006) Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 444:756–760
CrossRef Google scholar
[2]
Bao Y, Nakagawa K, Yang Z, Ikeda M, Withanage K, Ishigami-Yuasa M, Okuno Y, Hata S, Nishina H, Hata Y (2011) A cell-based assay to screen stimulators of the Hippo pathway reveals the inhibitory effect of dobutamine on the YAP-dependent gene transcription. J Biochem 150:199–208
CrossRef Google scholar
[3]
Bartucci M, Dattilo R, Moriconi C, Pagliuca A, Mottolese M, Federici G, Benedetto AD, Todaro M, Stassi G, Sperati F, Amabile MI, Pilozzi E, Patrizii M, Biffoni M, Maugeri-Sacca M, Piccolo S, De Maria R (2015) TAZ is required for metastatic activity and chemoresistance of breast cancer stem cells. Oncogene 34:681–690
CrossRef Google scholar
[4]
Bendinelli P, Maroni P, Matteucci E, Luzzati A, Perrucchini G, Desiderio MA (2013) Hypoxia inducible factor-1 is activated by transcriptional co-activator with PDZ-binding motif (TAZ) versus WWdomain-containing oxidoreductase (WWOX) in hypoxic microenvironment of bone metastasis from breast cancer. Eur J Cancer 49:2608–2618
CrossRef Google scholar
[5]
Bhat KP, Salazar KL, Balasubramaniyan V, Wani K, Heathcock L, Hollingsworth F, James JD, Gumin J, Diefes KL, Kim SH, Turski A, Azodi Y, Yang Y, Doucette T, Colman H, Sulman EP, Lang FF, Rao G, Copray S, Vaillant BD, Aldape KD (2011) The transcriptional coactivator TAZ regulates mesenchymal differentiation in malignant glioma. Genes Dev 25:2594–2609
CrossRef Google scholar
[6]
Bothos J, Tuttle RL, Ottey M, Luca FC, Halazonetis TD (2005) Human LATS1 is a mitotic exit network kinase. Cancer Res 65:6568–6575
CrossRef Google scholar
[7]
Bui DA, Lee W, White AE, Harper JW, Schackmann RC, Overholtzer M, Selfors LM, Brugge JS (2016) Cytokinesis involves a nontranscriptional function of the Hippo pathway effector YAP. Sci Signal 9:ra23
[8]
Chan EH, Nousiainen M, Chalamalasetty RB, Schafer A, Nigg EA, Sillje HH (2005) The Ste20-like kinase Mst2 activates the human large tumor suppressor kinase Lats1. Oncogene 24:2076–2086
CrossRef Google scholar
[9]
Chan SW, Lim CJ, Guo K, Ng CP, Lee I, Hunziker W, Zeng Q, Hong W (2008) A role for TAZ in migration, invasion, and tumorigenesis of breast cancer cells. Cancer Res 68:2592–2598
CrossRef Google scholar
[10]
Chan SW, Lim CJ, Loo LS, Chong YF, Huang C, Hong W (2009) TEADs mediate nuclear retention of TAZ to promote oncogenic transformation. J Biol Chem 284:14347–14358
CrossRef Google scholar
[11]
Chan SW, Lim CJ, Huang C, Chong YF, Gunaratne HJ, Hogue KA, Blackstock WP, Harvey KF, Hong W (2011) WW domainmediated interaction with Wbp2 is important for the oncogenic property of TAZ. Oncogene 30:600–610
CrossRef Google scholar
[12]
Conley SJ, Gheordunescu E, Kakarala P, Newman B, Korkaya H, Heath AN, Clouthier SG, Wicha MS (2012) Antiangiogenic agents increase breast cancer stem cells via the generation of tumor hypoxia. Proc Natl Acad Sci USA 109:2784–2789
CrossRef Google scholar
[13]
Cordenonsi M, Zanconato F, Azzolin L, Forcato M, Rosato A, Frasson C, Inui M, Montagner M, Parenti AR, Poletti A, Daidone MG, Dupont S, Basso G, Bicciato S, Piccolo S (2011) The Hippo transducer TAZ confers cancer stem cell-related traits on breast cancer cells. Cell 147:759–772
CrossRef Google scholar
[14]
Cui CB, Cooper LF, Yang X, Karsenty G, Aukhil I (2003) Transcriptional coactivation of bone-specific transcription factor Cbfa1 by TAZ. Mol Cell Biol 23:1004–1013
CrossRef Google scholar
[15]
DeRan M, Yang J, Shen CH, Peters EC, Fitamant J, Chan P, Hsieh M, Zhu S, Asara JM, Zheng B, Bardeesy N, Liu J, Wu X (2014) Energy stress regulates hippo-YAP signaling involving AMPK-mediated regulation of angiomotin-like 1 protein. Cell Rep 9:495–503
CrossRef Google scholar
[16]
Di Palma T, D’Andrea B, Liguori GL, Liguoro A, de Cristofaro T, Del Prete D, Pappalardo A, Mascia A, Zannini M (2009) TAZ is a coactivator for Pax8 and TTF-1, two transcription factors involved in thyroid differentiation. Exp Cell Res 315:162–175
CrossRef Google scholar
[17]
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
CrossRef Google scholar
[18]
Enzo E, Santinon G, Pocaterra A, Aragona M, Bresolin S, Forcato M, Grifoni D, Pession A, Zanconato F, Guzzo G, Bicciato S, Dupont S (2015) Aerobic glycolysis tunes YAP/TAZ transcriptional activity. EMBO J 34:1349–1370
CrossRef Google scholar
[19]
Errani C, Zhang L, Sung YS, Hajdu M, Singer S, Maki RG, Healey JH, Antonescu CR (2011) A novel WWTR1-CAMTA1 gene fusion is a consistent abnormality in epithelioid hemangioendothelioma of different anatomic sites. Genes Chromosomes Cancer 50:644–653
CrossRef Google scholar
[20]
Feng X, Degese MS, Iglesias-Bartolome R, Vaque JP, Molinolo AA, Rodrigues M, Zaidi MR, Ksander BR, Merlino G, Sodhi A, Chen Q, Gutkind JS (2014) Hippo-independent activation of YAP by the GNAQ uveal melanoma oncogene through a trio-regulated rho GTPase signaling circuitry. Cancer Cell 25:831–845
CrossRef Google scholar
[21]
Feng J, Sun Q, Liu L, Xing D (2015) Photoactivation of TAZ via Akt/GSK3beta signaling pathway promotes osteogenic differentiation. Int J Biochem Cell Biol 66:59–68
CrossRef Google scholar
[22]
Finch-Edmondson ML, Strauss RP, Passman AM, Sudol M, Yeoh GC, Callus BA (2015) TAZ protein accumulation is negatively regulated by YAP abundance in mammalian cells. J Biol Chem 290:27928–27938
[23]
Gao J, Aksoy BA, Dogrusoz U, Dresdner G, Gross B, Sumer SO, Sun Y, Jacobsen A, Sinha R, Larsson E, Cerami E, Sander C, Schultz N (2013) Integrative analysis of complex cancer genomics and clinical profiles using the cBioPortal. Sci Signal 6:pl1
[24]
Gaspar P, Tapon N (2014) Sensing the local environment: actin architecture and Hippo signalling. Curr Opin Cell Biol 31:74–83
CrossRef Google scholar
[25]
Hanahan D, Weinberg RA (2011) Hallmarks of cancer: the next generation. Cell 144:646–674
CrossRef Google scholar
[26]
Hansen CG, Moroishi T, Guan KL (2015) YAP and TAZ: a nexus for Hippo signaling and beyond. Trends Cell Biol 25:499–513
CrossRef Google scholar
[27]
Harvey K, Tapon N (2007) The Salvador–Warts–Hippo pathway: an emerging tumour-suppressor network. Nat Rev Cancer 7:182–191
CrossRef Google scholar
[28]
Harvey KF, Zhang X, Thomas DM (2013) The Hippo pathway and human cancer. Nat Rev Cancer 13:246–257
CrossRef Google scholar
[29]
Hegi ME, Diserens AC, Gorlia T, Hamou MF, de Tribolet N, Weller M, Kros JM, Hainfellner JA, Mason W, Mariani L, Bromberg JE, Hau P, Mirimanoff RO, Cairncross JG, Janzer RC, Stupp R (2005) MGMT gene silencing and benefit from temozolomide in glioblastoma. N Engl J Med 352:997–1003
CrossRef Google scholar
[30]
Hergovich A (2011) MOB control: reviewing a conserved family of kinase regulators. Cell Signal 23:1433–1440
CrossRef Google scholar
[31]
Hergovich A, Schmitz D, Hemmings BA (2006) The human tumour suppressor LATS1 is activated by human MOB1 at the membrane. Biochem Biophys Res Commun 345:50–58
CrossRef Google scholar
[32]
Hiemer SE, Zhang L, Kartha VK, Packer TS, Almershed M, Noonan V, Kukuruzinska M, Bais MV, Monti S, Varelas X (2015) A YAP/TAZ-regulated molecular signature is associated with oral squamous cell carcinoma. Mol Cancer Res 13:957–968
CrossRef Google scholar
[33]
Higashi T, Hayashi H, Ishimoto T, Takeyama H, Kaida T, Arima K, Taki K, Sakamoto K, Kuroki H, Okabe H, Nitta H, Hashimoto D, Chikamoto A, Beppu T, Baba H (2015) miR-9-3p plays a tumoursuppressor role by targeting TAZ (WWTR1) in hepatocellular carcinoma cells. Br J Cancer 113:252–258
CrossRef Google scholar
[34]
Hoa L, Kulaberoglu Y, Gundogdu R, Cook D, Mavis M, Gomez M, Gomez V, Hergovich A (2016) The characterisation of LATS2 kinase regulation in Hippo-YAP signalling. Cell Signal 28:488–497
CrossRef Google scholar
[35]
Hong JH, Yaffe MB (2006) TAZ: a beta-catenin-like molecule that regulates mesenchymal stem cell differentiation. Cell Cycle 5:176–179
CrossRef Google scholar
[36]
Hong JH, Hwang ES, McManus MT, Amsterdam A, Tian Y, Kalmukova R, Mueller E, Benjamin T, Spiegelman BM, Sharp PA, Hopkins N, Yaffe MB (2005) TAZ, a transcriptional modulator of mesenchymal stem cell differentiation. Science 309:1074–1078
CrossRef Google scholar
[37]
Hossain Z, Ali SM, Ko HL, Xu J, Ng CP, Guo K, Qi Z, Ponniah S, Hong W, Hunziker W (2007) Glomerulocystic kidney disease in mice with a targeted inactivation of Wwtr1. Proc Natl Acad Sci USA 104:1631–1636
CrossRef Google scholar
[38]
Huang W, Lv X, Liu C, Zha Z, Zhang H, Jiang Y, Xiong Y, Lei QY, Guan KL (2012) The N-terminal phosphodegron targets TAZ/WWTR1 protein for SCFbeta-TrCP-dependent degradation in response to phosphatidylinositol 3-kinase inhibition. J Biol Chem 287:26245–26253
CrossRef Google scholar
[39]
Jaffe AB, Hall A (2005) Rho GTPases: biochemistry and biology. Annu Rev Cell Dev Biol 21:247–269
CrossRef Google scholar
[40]
Jang EJ, Jeong H, Han KH, Kwon HM, Hong JH, Hwang ES (2012) TAZ suppresses NFAT5 activity through tyrosine phosphorylation. Mol Cell Biol 32:4925–4932
CrossRef Google scholar
[41]
Jeong H, Bae S, An SY, Byun MR, Hwang JH, Yaffe MB, Hong JH, Hwang ES (2010) TAZ as a novel enhancer of MyoD-mediated myogenic differentiation. FASEB J 24:3310–3320
CrossRef Google scholar
[42]
Jiao S, Wang H, Shi Z, Dong A, Zhang W, Song X, He F, Wang Y, Zhang Z, Wang W, Wang X, Guo T, Li P, Zhao Y, Ji H, Zhang L, Zhou Z (2014) A peptide mimicking VGLL4 function acts as a YAP antagonist therapy against gastric cancer. Cancer Cell 25:166–180
CrossRef Google scholar
[43]
Kan Z, Jaiswal BS, Stinson J, Janakiraman V, Bhatt D, Stern HM, Yue P, Haverty PM, Bourgon R, Zheng J, Moorhead M, Chaudhuri S, Tomsho LP, Peters BA, Pujara K, Cordes S, Davis DP, Carlton VE, Yuan W, Li L, Wang W, Eigenbrot C, Kaminker JS, Eberhard DA, Waring P, Schuster SC, Modrusan Z, Zhang Z, Stokoe D, de Sauvage FJ, Faham M, Seshagiri S (2010) Diverse somatic mutation patterns and pathway alterations in human cancers. Nature 466:869–873
CrossRef Google scholar
[44]
Kanai F, Marignani PA, Sarbassova D, Yagi R, Hall RA, Donowitz M, Hisaminato A, Fujiwara T, Ito Y, Cantley LC, Yaffe MB (2000) TAZ: a novel transcriptional co-activator regulated by interactions with 14-3-3 and PDZ domain proteins. EMBO J 19:6778–6791
CrossRef Google scholar
[45]
Kim M, Kim T, Johnson RL, Lim DS (2015) Transcriptional corepressor function of the hippo pathway transducers YAP and TAZ. Cell Rep 11:270–282
CrossRef Google scholar
[46]
Lau AN, Curtis SJ, Fillmore CM, Rowbotham SP, Mohseni M, Wagner DE, Beede AM, Montoro DT, Sinkevicius KW, Walton ZE, Barrios J, Weiss DJ, Camargo FD, Wong KK, Kim CF (2014) Tumor-propagating cells and Yap/Taz activity contribute to lung tumor progression and metastasis. EMBO J 33:468–481
CrossRef Google scholar
[47]
Lei QY, Zhang H, Zhao B, Zha ZY, Bai F, Pei XH, Zhao S, Xiong Y, Guan KL (2008) TAZ promotes cell proliferation and epithelialmesenchymal transition and is inhibited by the hippo pathway. Mol Cell Biol 28:2426–2436
CrossRef Google scholar
[48]
Li Q, Li S, Mana-Capelli S, Roth Flach RJ, Danai LV, Amcheslavsky A, Nie Y, Kaneko S, Yao X, Chen X, Cotton JL, Mao J, McCollum D, Jiang J, Czech MP, Xu L, Ip YT (2014) The conserved misshapen-warts-Yorkie pathway acts in enteroblasts to regulate intestinal stem cells in Drosophila. Dev Cell 31:291–304
CrossRef Google scholar
[49]
Li J, Fang L, Yu W, Wang Y (2015a) MicroRNA-125b suppresses the migration and invasion of hepatocellular carcinoma cells by targeting transcriptional coactivator with PDZ-binding motif. Oncol Lett 9:1971–1975
[50]
Li Z, Wang Y, Zhu Y, Yuan C, Wang D, Zhang W, Qi B, Qiu J, Song X, Ye J, Wu H, Jiang H, Liu L, Zhang Y, Song LN, Yang J, Cheng J (2015b) The Hippo transducer TAZ promotes epithelial to mesenchymal transition and cancer stem cell maintenance in oral cancer. Mol Oncol 9:1091–1105
[51]
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
CrossRef Google scholar
[52]
Liu CY, Lv X, Li T, Xu Y, Zhou X, Zhao S, Xiong Y, Lei QY, Guan KL (2011) PP1 cooperates with ASPP2 to dephosphorylate and activate TAZ. J Biol Chem 286:5558–5566
CrossRef Google scholar
[53]
Liu G, Yu FX, Kim YC, Meng Z, Naipauer J, Looney DJ, Liu X, Gutkind JS, Mesri EA, Guan KL (2015) Kaposi sarcoma-associated herpesvirus promotes tumorigenesis by modulating the Hippo pathway. Oncogene 34:3536–3546
CrossRef Google scholar
[54]
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
CrossRef Google scholar
[55]
Luo J, Manning BD, Cantley LC (2003) Targeting the PI3K-Akt pathway in human cancer: rationale and promise. Cancer Cell 4:257–262
CrossRef Google scholar
[56]
Mahoney WM, Jr, Hong JH , YaffeMB, Farrance IK (2005) The transcriptional co-activator TAZ interacts differentially with transcriptional enhancer factor-1 (TEF-1) family members. Biochem J 388:217–225
CrossRef Google scholar
[57]
Makita R, Uchijima Y, Nishiyama K, Amano T, Chen Q, Takeuchi T, Mitani A, Nagase T, Yatomi Y, Aburatani H, Nakagawa O, Small EV, Cobo-Stark P, Igarashi P, Murakami M, Tominaga J, Sato T, Asano T, Kurihara Y, Kurihara H (2008) Multiple renal cysts, urinary concentration defects, and pulmonary emphysematous changes in mice lacking TAZ. Am J Physiol Renal Physiol 294: F542–F553
[58]
Matsui Y, Lai ZC (2013) Mutual regulation between Hippo signaling and actin cytoskeleton. Protein Cell 4:904–910
CrossRef Google scholar
[59]
Meng Z, Moroishi T, Mottier-Pavie V, Plouffe SW, Hansen CG, Hong AW, Park HW, Mo JS, Lu W, Lu S, Flores F, Yu FX, Halder G, Guan KL (2015) MAP4K family kinases act in parallel to MST1/2 to activate LATS1/2 in the Hippo pathway. Nat Commun 6:8357
CrossRef Google scholar
[60]
Miller E, Yang J, DeRan M, Wu C, Su AI, Bonamy GM, Liu J, Peters EC, Wu X (2012) Identification of serum-derived sphingosine-1-phosphate as a small molecule regulator of YAP. Chem Biol 19:955–962
CrossRef Google scholar
[61]
Mo JS, Yu FX, Gong R, Brown JH, Guan KL (2012) Regulation of the Hippo-YAP pathway by protease-activated receptors (PARs). Genes Dev 26:2138–2143
CrossRef Google scholar
[62]
Mo JS, Meng Z, Kim YC, Park HW, Hansen CG, Kim S, Lim DS, Guan KL (2015) Cellular energy stress induces AMPK-mediated regulation of YAP and the Hippo pathway. Nat Cell Biol 17:500–510
CrossRef Google scholar
[63]
Mori M, Triboulet R, Mohseni M, Schlegelmilch K, Shrestha K, Camargo FD, Gregory RI (2014) Hippo signaling regulates microprocessor and links cell-density-dependent miRNA biogenesis to cancer. Cell 156:893–906
CrossRef Google scholar
[64]
Moroishi T, Park HW, Qin B, Chen Q, Meng Z, Plouffe SW, Taniguchi K, Yu FX, Karin M, Pan D, Guan KL (2015) A YAP/TAZ-induced feedback mechanism regulates Hippo pathway homeostasis. Genes Dev 29:1271–1284
CrossRef Google scholar
[65]
Murakami M, Tominaga J, Makita R, Uchijima Y, Kurihara Y, Nakagawa O, Asano T, Kurihara H (2006) Transcriptional activity of Pax3 is co-activated by TAZ. Biochem Biophys Res Commun 339:533–539
CrossRef Google scholar
[66]
Noguchi S, Saito A, Horie M, Mikami Y, Suzuki HI, Morishita Y, Ohshima M, Abiko Y, Mattsson JS, Konig H, Lohr M, Edlund K, Botling J, Micke P, Nagase T (2014) An integrative analysis of the tumorigenic role of TAZ in human non-small cell lung cancer. Clin Cancer Res 20:4660–4672
CrossRef Google scholar
[67]
O’Hayre M, Vazquez-Prado J, Kufareva I, Stawiski EW, Handel TM, Seshagiri S, Gutkind JS (2013) The emerging mutational landscape of G proteins and G-protein-coupled receptors in cancer. Nat Rev Cancer 13:412–424
CrossRef Google scholar
[68]
Park KS, Whitsett JA, Di Palma T, Hong JH, Yaffe MB, Zannini M (2004) TAZ interacts with TTF-1 and regulates expression of surfactant protein-C. J Biol Chem 279:17384–17390
CrossRef Google scholar
[69]
Remue E, Meerschaert K, Oka T, Boucherie C, Vandekerckhove J, Sudol M, Gettemans J (2010) TAZ interacts with zonula occludens-1 and-2 proteins in a PDZ-1 dependent manner. FEBS Lett 584:4175–4180
CrossRef Google scholar
[70]
Schwab LP, Peacock DL, Majumdar D, Ingels JF, Jensen LC, Smith KD, Cushing RC, Seagroves TN (2012) Hypoxia-inducible factor 1alpha promotes primary tumor growth and tumor-initiating cell activity in breast cancer. Breast Cancer Res 14:R6
[71]
Shen S, Guo X, Yan H, Lu Y, Ji X, Li L, Liang T, Zhou D, Feng XH, Zhao JC, Yu J, Gong XG, Zhang L, Zhao B (2015) A miR-130a-YAP positive feedback loop promotes organ size and tumorigenesis. Cell Res 25:997–1012
CrossRef Google scholar
[72]
Sorrentino G, Ruggeri N, Specchia V, Cordenonsi M, Mano M, Dupont S, Manfrin A, Ingallina E, Sommaggio R, Piazza S, Rosato A, Piccolo S, Del Sal G (2014) Metabolic control of YAP and TAZ by the mevalonate pathway. Nat Cell Biol 16:357–366
CrossRef Google scholar
[73]
Sudol M, Bork P, Einbond A, Kastury K, Druck T, Negrini M, Huebner K, Lehman D (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
CrossRef Google scholar
[74]
Sudol M, Shields DC, Farooq A (2012) Structures of YAP protein domains reveal promising targets for development of new cancer drugs. Semin Cell Dev Biol 23:827–833
CrossRef Google scholar
[75]
Tan G, Cao X, Dai Q, Zhang B, Huang J, Xiong S, Zhang Y, Chen W, Yang J, Li H (2015) A novel role for microRNA-129-5p in inhibiting ovarian cancer cell proliferation and survival via direct suppression of transcriptional co-activators YAP and TAZ. Oncotarget 6:8676–8686
CrossRef Google scholar
[76]
Tanas MR, Sboner A, Oliveira AM, Erickson-Johnson MR, Hespelt J, Hanwright PJ, Flanagan J, Luo Y, Fenwick K, Natrajan R, Mitsopoulos C, Zvelebil M, Hoch BL, Weiss SW, Debiec-Rychter M, Sciot R, West RB, Lazar AJ, Ashworth A, Reis-Filho JS, Lord CJ, Gerstein MB, Rubin MA, Rubin BP (2011) Identification of a disease-defining gene fusion in epithelioid hemangioendothelioma. Sci Transl Med 3:98ra82
[77]
Tanas MR, Ma S, Jadaan FO, Ng CK, Weigelt B, Reis-Filho JS, Rubin BP (2016) Mechanism of action of a WWTR1(TAZ)-CAMTA1 fusion oncoprotein. Oncogene 35:929–938
CrossRef Google scholar
[78]
Tian Y, Kolb R, Hong JH, Carroll J, Li D, You J, Bronson R, Yaffe MB, Zhou J, Benjamin T (2007) TAZ promotes PC2 degradation through a SCFbeta-Trcp E3 ligase complex. Mol Cell Biol 27:6383–6395
CrossRef Google scholar
[79]
Tian T, Li A, Lu H, Luo R, Zhang M, Li Z (2015) TAZ promotes temozolomide resistance by upregulating MCL-1 in human glioma cells. Biochem Biophys Res Commun 463:638–643
CrossRef Google scholar
[80]
Valencia-Sama I, Zhao Y, Lai D, Janse van Rensburg HJ, Hao Y, Yang X (2015) Hippo component TAZ functions as a co-repressor and negatively regulates DeltaNp63 transcription through TEA domain (TEAD) transcription factor. J Biol Chem 290:16906–16917
CrossRef Google scholar
[81]
Varelas X, Sakuma R, Samavarchi-Tehrani P, Peerani R, Rao BM, Dembowy J, Yaffe MB, Zandstra PW, Wrana JL (2008) TAZ controls Smad nucleocytoplasmic shuttling and regulates human embryonic stem-cell self-renewal. Nat Cell Biol 10:837–848
CrossRef Google scholar
[82]
Varelas X, Samavarchi-Tehrani P, Narimatsu M, Weiss A, Cockburn K, Larsen BG, Rossant J, Wrana JL (2010) The Crumbs complex couples cell density sensing to Hippo-dependent control of the TGF-beta-SMAD pathway. Dev Cell 19:831–844
CrossRef Google scholar
[83]
Vaupel P, Mayer A (2007) Hypoxia in cancer: significance and impact on clinical outcome. Cancer Metastasis Rev 26:225–239
CrossRef Google scholar
[84]
Vici P, Mottolese M, Pizzuti L, Barba M, Sperati F, Terrenato I, Di Benedetto A, Natoli C, Gamucci T, Angelucci D, Ramieri MT, Di Lauro L, Sergi D, Bartucci M, Dattilo R, Pagliuca A, De Maria R, Maugeri-Sacca M (2014) The Hippo transducer TAZ as a biomarker of pathological complete response in HER2-positive breast cancer patients treated with trastuzumab-based neoadjuvant therapy. Oncotarget 5:9619–9625
CrossRef Google scholar
[85]
Wang Y, Dong Q, Zhang Q, Li Z, Wang E, 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
CrossRef Google scholar
[86]
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
[87]
Wang Z, Wu Y, Wang H, Zhang Y, Mei L, Fang X, Zhang X, Zhang F, Chen H, Liu Y, Jiang Y, Sun S, Zheng Y, Li N, Huang L (2014) Interplay of mevalonate and Hippo pathways regulates RHAMM transcription via YAP to modulate breast cancer cell motility. Proc Natl Acad Sci USA 111:E89–E98
[88]
Wang W, Li X, Chen J (2015a) Energy crisis and the Hippo pathway. Cell Cycle 14:1995–1996
[89]
Wang W, Xiao ZD, Li X, Aziz KE, Gan B, Johnson RL, Chen J(2015b) AMPK modulates Hippo pathway activity to regulate energy homeostasis. Nat Cell Biol 17:490–499
[90]
Warburg O (1956a) On respiratory impairment in cancer cells. Science 124:269–270
[91]
Warburg O (1956b) On the origin of cancer cells. Science 123:309–314
[92]
Wei Z, Wang Y, Li Z, Yuan C, Zhang W, Wang D, Ye J, Jiang H, Wu Y, Cheng J (2013) Overexpression of Hippo pathway effector TAZ in tongue squamous cell carcinoma: correlation with clinicopathological features and patients’ prognosis. J Oral Pathol Med 42:747–754
CrossRef Google scholar
[93]
Wilson WR, Hay MP (2011) Targeting hypoxia in cancer therapy. Nat Rev Cancer 11:393–410
CrossRef Google scholar
[94]
Xiang L, Gilkes DM, Hu H, Takano N, Luo W, Lu H, Bullen JW, Samanta D, Liang H, Semenza GL (2014) Hypoxia-inducible factor 1 mediates TAZ expression and nuclear localization to induce the breast cancer stem cell phenotype. Oncotarget 5:12509–12527
[95]
Xiang L, Gilkes DM, Hu H, Luo W, Bullen JW, Liang H, Semenza GL (2015) HIF-1alpha and TAZ serve as reciprocal co-activators in human breast cancer cells. Oncotarget 6:11768–11778
CrossRef Google scholar
[96]
Xie M, Zhang L, He CS, Hou JH, Lin SX, Hu ZH, Xu F, Zhao HY (2012) Prognostic significance of TAZ expression in resected non-small cell lung cancer. J Thorac Oncol 7:799–807
CrossRef Google scholar
[97]
Xu W, Wei Y, Wu S, Wang Y, Wang Z, Sun Y, Cheng SY, Wu J (2015) Up-regulation of the Hippo pathway effector TAZ renders lung adenocarcinoma cells harboring EGFR-T790M mutation resistant to gefitinib. Cell Biosci 5:7
CrossRef Google scholar
[98]
Yan L, Cai Q, Xu Y (2014) Hypoxic conditions differentially regulate TAZ and YAP in cancer cells. Arch Biochem Biophys 562:31–36
CrossRef Google scholar
[99]
Yang N, Morrison CD, Liu P, Miecznikowski J, Bshara W, Han S, Zhu Q, Omilian AR, Li X, Zhang J (2012) TAZ induces growth factorindependent proliferation through activation of EGFR ligand amphiregulin. Cell Cycle 11:2922–2930
CrossRef Google scholar
[100]
Yang S, Zhang L, Liu M, Chong R, Ding SJ, Chen Y, Dong J (2013) CDK1 phosphorylation of YAP promotes mitotic defects and cell motility and is essential for neoplastic transformation. Cancer Res 73:6722–6733
CrossRef Google scholar
[101]
Yu FX, Guan KL (2013) The Hippo pathway: regulators and regulations. Genes Dev 27:355–371
CrossRef Google scholar
[102]
Yu FX, Zhao B, Panupinthu N, Jewell JL, Lian I, Wang LH, Zhao J, Yuan H, Tumaneng K, Li H, Fu XD, Mills GB, Guan KL (2012) Regulation of the Hippo-YAP pathway by G-protein-coupled receptor signaling. Cell 150:780–791
CrossRef Google scholar
[103]
Yu FX, Zhang Y, Park HW, Jewell JL, Chen Q, Deng Y, Pan D, Taylor SS, Lai ZC, Guan KL (2013) Protein kinase A activates the Hippo pathway to modulate cell proliferation and differentiation. Genes Dev 27:1223–1232
CrossRef Google scholar
[104]
Yu FX, Luo J, Mo JS, Liu G, Kim YC, Meng Z, Zhao L, Peyman G, Ouyang H, Jiang W, Zhao J, Chen X, Zhang L, Wang CY, Bastian BC, Zhang K, Guan KL (2014) Mutant Gq/11 promote uveal melanoma tumorigenesis by activating YAP. Cancer Cell 25:822–830
CrossRef Google scholar
[105]
Yu FX, Zhao B, Guan KL (2015) Hippo pathway in organ size control, tissue homeostasis, and cancer. Cell 163:811–828
CrossRef Google scholar
[106]
Yuan TL, Cantley LC (2008) PI3K pathway alterations in cancer: variations on a theme. Oncogene 27:5497–5510
CrossRef Google scholar
[107]
Yuan J, Xiao G, Peng G, Liu D, Wang Z, Liao Y, Liu Q, Wu M, Yuan X (2015) MiRNA-125a-5p inhibits glioblastoma cell proliferation and promotes cell differentiation by targeting TAZ. Biochem Biophys Res Commun 457:171–176
CrossRef Google scholar
[108]
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
[109]
Zanconato F, Forcato M, Battilana G, Azzolin L, Quaranta E, Bodega B, Rosato A, Bicciato S, Cordenonsi M, Piccolo S (2015) Genome-wide association between YAP/TAZ/TEAD and AP-1 at enhancers drives oncogenic growth. Nat Cell Biol 17:1218–1227
CrossRef Google scholar
[110]
Zhang H, Liu CY, Zha ZY, Zhao B, Yao J, Zhao S, Xiong Y, Lei QY, Guan KL (2009) TEAD transcription factors mediate the function of TAZ in cell growth and epithelial-mesenchymal transition. J Biol Chem 284:13355–13362
CrossRef Google scholar
[111]
Zhang W, Gao Y, Li P, Shi Z, Guo T, Li F, Han X, Feng Y, Zheng C, Wang Z, Chen H, Zhou Z, Zhang L, Ji H (2014) VGLL4 functions as a new tumor suppressor in lung cancer by negatively regulating the YAP-TEAD transcriptional complex. Cell Res 24:331–343
CrossRef Google scholar
[112]
Zhang H, Ramakrishnan SK, Triner D, Centofanti B, Maitra D, Gyorffy B, Sebolt-Leopold JS, Dame MK, Varani J, Brenner DE, Fearon ER, Omary MB, Shah YM (2015a) Tumor-selective proteotoxicity of verteporfin inhibits colon cancer progression independently of YAP1. Sci Signal 8:ra98
[113]
Zhang L, Chen X, Stauffer S, Yang S, Chen Y, Dong J (2015b) CDK1 phosphorylation of TAZ in mitosis inhibits its oncogenic activity. Oncotarget 6:31399–31412
[114]
Zhao Y, Yang X (2015) Regulation of sensitivity of tumor cells to antitubulin drugs by Cdk1-TAZ signalling. Oncotarget 6:21906–21917
CrossRef Google scholar
[115]
Zhao B, Lei QY, Guan KL (2008) The Hippo-YAP pathway: new connections between regulation of organ size and cancer. Curr Opin Cell Biol 20:638–646
CrossRef Google scholar
[116]
Zhao B, Li L, Lei Q, Guan KL (2010a) The Hippo-YAP pathway in organ size control and tumorigenesis: an updated version. Genes Dev 24:862–874
[117]
Zhao B, Li L, Tumaneng K, Wang CY, Guan KL (2010b) A coordinated phosphorylation by Lats and CK1 regulates YAP stability through SCF(beta-TRCP). Genes Dev 24:72–85
[118]
Zhao B, Li L, Wang L, Wang CY, Yu J, Guan KL (2012) Cell detachment activates the Hippo pathway via cytoskeleton reorganization to induce anoikis. Genes Dev 26:54–68
CrossRef Google scholar
[119]
Zheng Y, Wang W, Liu B, Deng H, Uster E, Pan D (2015) Identification of Happyhour/MAP4K as Alternative Hpo/Mst-like Kinases in the Hippo Kinase Cascade. Dev Cell 34:642–655
CrossRef Google scholar
[120]
Zhou Z, Hao Y, Liu N, Raptis L, Tsao MS, Yang X (2011) TAZ is a novel oncogene in non-small cell lung cancer. Oncogene 30:2181–2186
CrossRef Google scholar
[121]
Zhou X, Wang S, Wang Z, Feng X, Liu P, Lv XB, Li F, Yu FX, Sun Y, Yuan H, Zhu H, Xiong Y, Lei QY, Guan KL (2015a) Estrogen regulates Hippo signaling via GPER in breast cancer. J Clin Invest 125:2123–2135
[122]
Zhou X, Wang Z, Huang W, Lei QY (2015b) G protein-coupled receptors: bridging the gap from the extracellular signals to the Hippo pathway. Acta Biochim Biophys Sin (Shanghai) 47:10–15
[123]
Zhu G, Wang Y, Mijiti M, Wang Z, Wu PF, Jiafu D (2015) Upregulation of miR-130b enhances stem cell-like phenotype in glioblastoma by inactivating the Hippo signaling pathway. Biochem Biophys Res Commun 465:194–199
CrossRef Google scholar
[124]
Zuo QF, Zhang R, Li BS, Zhao YL, Zhuang Y, Yu T, Gong L, Li S, Xiao B, Zou QM (2015) MicroRNA-141 inhibits tumor growth and metastasis in gastric cancer by directly targeting transcriptional co-activator with PDZ-binding motif, TAZ. Cell Death Dis 6:e1623

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