96
Views
11
CrossRef citations to date
0
Altmetric
Review

YAP/TAZ: a promising target for squamous cell carcinoma treatment

, , , , , & show all
Pages 6245-6252 | Published online: 08 Jul 2019

References

  • Udan RS, Kango-Singh M, Nolo R, Tao C, Halder G. Hippo promotes proliferation arrest and apoptosis in the Salvador/Warts pathway. Nat Cell Biol. 2003;5(10):914–920. doi:10.1038/ncb105014502294
  • Huang J, Wu S, Barrera J, Matthews K, Pan D. The Hippo signaling pathway coordinately regulates cell proliferation and apoptosis by inactivating Yorkie, the Drosophila Homolog of YAP. Cell. 2005;122(3):421–434. doi:10.1016/j.cell.2005.06.00716096061
  • Kanai F, Marignani PA, Sarbassova D, et al. TAZ: a novel transcriptional co-activator regulated by interactions with 14-3-3 and PDZ domain proteins. Embo J. 2000;19(24):6778–6791. doi:10.1093/emboj/19.24.677811118213
  • Yu FX, Guan KL. The Hippo pathway: regulators and regulations. Genes Dev. 2013;27(4):355–371. doi:10.1101/gad.210773.11223431053
  • Justice RW, Zilian O, Woods DF, Noll M, Bryant PJ. The Drosophila tumor suppressor gene warts encodes a homolog of human myotonic dystrophy kinase and is required for the control of cell shape and proliferation. Genes Dev. 1995;9(5):534–546. doi:10.1101/gad.9.5.5347698644
  • Kango-Singh M. Shar-pei mediates cell proliferation arrest during imaginal disc growth in Drosophila. Development. 2002;129(24):5719–5730.12421711
  • Tapon N, Harvey KF, Bell DW, et al. salvador promotes both cell cycle exit and apoptosis in Drosophila and is mutated in human cancer cell lines. Cell. 2002;110(4):467–478.12202036
  • Harvey KF, Pfleger CM, Hariharan IK. The drosophila Mst ortholog, hippo, restricts growth and cell proliferation and promotes apoptosis. Cell. 2003;114(4):457–467.12941274
  • Pantalacci S, Tapon N, Leopold P. The Salvador partner Hippo promotes apoptosis and cell-cycle exit in drosophila. Nat Cell Biol. 2003;5(10):921–927. doi:10.1038/ncb105114502295
  • Wu S, Huang J, Dong J, Pan D. Hippo encodes a Ste-20 family protein kinase that restricts cell proliferation and promotes apoptosis in conjunction with Salvador and warts. Cell. 2003;114(4):445–456.12941273
  • Lai ZC, Wei X, Shimizu T, et al. Control of cell proliferation and apoptosis by mob as tumor suppressor, mats. Cell. 2005;120(5):675–685. doi:10.1016/j.cell.2004.12.03615766530
  • Zhang L, Ren F, Zhang Q, Chen Y, Wang B, Jiang J. The TEAD/TEF family of transcription factor scalloped mediates Hippo signaling in organ size control. Dev Cell. 2008;14(3):377–387. doi:10.1016/j.devcel.2008.01.00618258485
  • Guo T, Lu Y, Li P, et al. A novel partner of scalloped regulates Hippo signaling via antagonizing scalloped-yorkie activity. Cell Res. 2013;23(10):1201–1214. doi:10.1038/cr.2013.12023999857
  • Thompson BJ, Cohen SM. The Hippo pathway regulates the bantam microRNA to control cell proliferation and apoptosis in drosophila. Cell. 2006;126(4):767–774. doi:10.1016/j.cell.2006.07.01316923395
  • Sudol M. Yes-associated protein (YAP65) is a proline-rich phosphoprotein that binds to the SH3 domain of the Yes proto-oncogene product. Oncogene. 1994;9(8):2145–2152.8035999
  • Yu FX, Zhao B, Guan KL. Hippo pathway in organ size control, tissue homeostasis, and cancer. Cell. 2015;163(4):811–828. doi:10.1016/j.cell.2015.10.04426544935
  • Fu V, Plouffe SW, Guan KL. The Hippo pathway in organ development, homeostasis, and regeneration. Curr Opin Cell Biol. 2017;49:99–107. doi:10.1016/j.ceb.2017.12.01229316535
  • Piccolo S, Dupont S, Cordenonsi M. The biology of YAP/TAZ: hippo signaling and beyond. Physiol Rev. 2014;94(4):1287–1312. doi:10.1152/physrev.00005.201425287865
  • Zhao B, Tumaneng K, Guan KL. The Hippo pathway in organ size control, tissue regeneration and stem cell self-renewal. Nat Cell Biol. 2011;13(8):877–883. doi:10.1038/ncb230321808241
  • Hong AW, Meng Z, Guan KL. The Hippo pathway in intestinal regeneration and disease. Nat Rev Gastroenterol Hepatol. 2016;13(6):324–337. doi:10.1038/nrgastro.2016.5927147489
  • Chan EH, Nousiainen M, Chalamalasetty RB, Schafer A, Nigg EA, Sillje HH. The Ste20-like kinase Mst2 activates the human large tumor suppressor kinase Lats1. Oncogene. 2005;24(12):2076–2086. doi:10.1038/sj.onc.120844515688006
  • Hwang E, Ryu KS, Paakkonen K, et al. Structural insight into dimeric interaction of the SARAH domains from Mst1 and RASSF family proteins in the apoptosis pathway. Proc Natl Acad Sci U S A. 2007;104(22):9236–9241. doi:10.1073/pnas.061071610417517604
  • Ni L, Zheng Y, Hara M, Pan D, Luo X. Structural basis for Mob1-dependent activation of the core Mst-Lats kinase cascade in Hippo signaling. Genes Dev. 2015;29(13):1416–1431. doi:10.1101/gad.264929.11526108669
  • Hao Y, Chun A, Cheung K, Rashidi B, Yang X. Tumor suppressor LATS1 is a negative regulator of oncogene YAP. J Biol Chem. 2008;283(9):5496–5509. doi:10.1074/jbc.M70903720018158288
  • Schumacher B, Skwarczynska M, Rose R, Ottmann C. Structure of a 14-3-3sigma-YAP phosphopeptide complex at 1.15 A resolution. Acta Crystallogr Sect F Struct Biol Cryst Commun. 2010;66(Pt 9):978–984. doi:10.1107/S1744309110025479
  • Zhao B, Li L, Tumaneng K, Wang CY, Guan KL. A coordinated phosphorylation by Lats and CK1 regulates YAP stability through SCF(beta-TRCP). Genes Dev. 2010;24(1):72–85. doi:10.1101/gad.184381020048001
  • Guo L, Teng L. YAP/TAZ for cancer therapy: opportunities and challenges (review). Int J Oncol. 2015;46(4):1444–1452. doi:10.3892/ijo.2015.287725652178
  • Zhao B, Ye X, Yu J, et al. TEAD mediates YAP-dependent gene induction and growth control. Genes Dev. 2008;22(14):1962–1971. doi:10.1101/gad.166440818579750
  • Lei QY, Zhang H, Zhao B, et al. TAZ promotes cell proliferation and epithelial-mesenchymal transition and is inhibited by the hippo pathway. Mol Cell Biol. 2008;28(7):2426–2436. doi:10.1128/MCB.01874-0718227151
  • Lamar JM, Stern P, Liu H, Schindler JW, Jiang ZG, Hynes RO. The Hippo pathway target, YAP, promotes metastasis through its TEAD-interaction domain. Proc Natl Acad Sci U S A. 2012;109(37):E2441–50. doi:10.1073/pnas.121202110922891335
  • Komuro A, Nagai M, Navin NE, Sudol M. 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. 2003;278(35):33334–33341. doi:10.1074/jbc.M30559720012807903
  • Murakami M, Nakagawa M, Olson EN, Nakagawa O. 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. 2005;102(50):18034–18039. doi:10.1073/pnas.050910910216332960
  • Manderfield LJ, Engleka KA, Aghajanian H, et al. Pax3 and hippo signaling coordinate melanocyte gene expression in neural crest. Cell Rep. 2014;9(5):1885–1895. doi:10.1016/j.celrep.2014.10.06125466249
  • Halder G, Johnson RL. Hippo signaling: growth control and beyond. Development. 2011;138(1):9–22. doi:10.1242/dev.04550021138973
  • Zhao B, Li L, Lei Q, Guan KL. The Hippo-YAP pathway in organ size control and tumorigenesis: an updated version. Genes Dev. 2010;24(9):862–874. doi:10.1101/gad.190921020439427
  • Kim M, Kim T, Johnson RL, Lim DS. Transcriptional co-repressor function of the hippo pathway transducers YAP and TAZ. Cell Rep. 2015;11(2):270–282. doi:10.1016/j.celrep.2015.03.01525843714
  • Harvey KF, Zhang X, Thomas DM. The Hippo pathway and human cancer. Nat Rev Cancer. 2013;13(4):246–257. doi:10.1038/nrc345823467301
  • Yu FX, Zhao B, Panupinthu N, et al. Regulation of the Hippo-YAP pathway by G-protein-coupled receptor signaling. Cell. 2012;150(4):780–791. doi:10.1016/j.cell.2012.06.03722863277
  • Webb C, Upadhyay A, Giuntini F, et al. Structural features and ligand binding properties of tandem WW domains from YAP and TAZ, nuclear effectors of the Hippo pathway. Biochemistry. 2011;50(16):3300–3309. doi:10.1021/bi200188821417403
  • Ernst A, Appleton BA, Ivarsson Y, et al. A structural portrait of the PDZ domain family. J Mol Biol. 2014;426(21):3509–3519. doi:10.1016/j.jmb.2014.08.01225158098
  • Schlegelmilch K, Mohseni M, Kirak O, et al. Yap1 acts downstream of alpha-catenin to control epidermal proliferation. Cell. 2011;144(5):782–795. doi:10.1016/j.cell.2011.02.03121376238
  • Xu CM, Liu WW, Liu CJ, Wen C, Lu HF, Wan FS. Mst1 overexpression inhibited the growth of human non-small cell lung cancer in vitro and in vivo. Cancer Gene Ther. 2013;20(8):453–460. doi:10.1038/cgt.2013.4023928732
  • Bai H, Zhang N, Xu Y, et al. Yes-associated protein regulates the hepatic response after bile duct ligation. Hepatology. 2012;56(3):1097–1107. doi:10.1002/hep.2576922886419
  • Anakk S, Bhosale M, Schmidt VA, Johnson RL, Finegold MJ, Moore DD. Bile acids activate YAP to promote liver carcinogenesis. Cell Rep. 2013;5(4):1060–1069. doi:10.1016/j.celrep.2013.10.03024268772
  • Zhang W, Cohen SM. The Hippo pathway acts via p53 and microRNAs to control proliferation and proapoptotic gene expression during tissue growth. Biol Open. 2013;2(8):822–828. doi:10.1242/bio.2013431723951408
  • Bai H, Gayyed MF, Lam-Himlin DM, et al. Expression of Yes-associated protein modulates Survivin expression in primary liver malignancies. Hum Pathol. 2012;43(9):1376–1385. doi:10.1016/j.humpath.2011.12.00122436626
  • Barry ER, Morikawa T, Butler BL, et al. Restriction of intestinal stem cell expansion and the regenerative response by YAP. Nature. 2013;493(7430):106–110. doi:10.1038/nature1169323178811
  • Fujii M, Toyoda T, Nakanishi H, et al. TGF-beta synergizes with defects in the Hippo pathway to stimulate human malignant mesothelioma growth. J Exp Med. 2012;209(3):479–494. doi:10.1084/jem.2011165322329991
  • Zhou D, Zhang Y, Wu H, et al. 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. 2011;108(49):E1312–E1320. doi:10.1073/pnas.111042810822042863
  • Camargo FD, Gokhale S, Johnnidis JB, et al. YAP1 increases organ size and expands undifferentiated progenitor cells. Curr Biol. 2007;17(23):2054–2060. doi:10.1016/j.cub.2007.10.03917980593
  • Heinemann A, Cullinane C, De Paoli-Iseppi R, et al. HDAC inhibitors synergistically induces apoptosis of melanoma and suppresses AKT and YAP signaling. Oncotarget. 2015;6(25):21507–21521. doi:10.18632/oncotarget.424226087189
  • Lin Z, Zhou P, von Gise A, et al. Pi3kcb links Hippo-YAP and PI3K-AKT signaling pathways to promote cardiomyocyte proliferation and survival. Circ Res. 2015;116(1):35–45. doi:10.1161/CIRCRESAHA.115.30445725249570
  • Lau AN, Curtis SJ, Fillmore CM, et al. Tumor-propagating cells and Yap/Taz activity contribute to lung tumor progression and metastasis. Embo J. 2014;33(5):468–481. doi:10.1002/embj.20138608224497554
  • Perra A, Kowalik MA, Ghiso E, et al. YAP activation is an early event and a potential therapeutic target in liver cancer development. J Hepatol. 2014;61(5):1088–1096. doi:10.1016/j.jhep.2014.06.03325010260
  • Xia Y, Chang T, Wang Y, et al. YAP promotes ovarian cancer cell tumorigenesis and is indicative of a poor prognosis for ovarian cancer patients. PLoS One. 2014;9(3):e91770. doi:10.1371/journal.pone.009177024622501
  • Wu Q, Li J, Sun S, et al. YAP/TAZ-mediated activation of serine metabolism and methylation regulation is critical for LKB1-deficient breast cancer progression. Biosci Rep. 2017;37(5):BSR20171072. doi:10.1042/BSR2017107228931725
  • Zhou GX, Li XY, Zhang Q, et al. Effects of the hippo signaling pathway in human gastric cancer. Asian Pac J Cancer Prev. 2013;14(9):5199–5205.24175801
  • Wang Y, Xie C, Li Q, Xu K, Wang E. Clinical and prognostic significance of Yes-associated protein in colorectal cancer. Tumour Biol. 2013;34(4):2169–2174. doi:10.1007/s13277-013-0751-x23558963
  • Debaugnies M, Sanchez-Danes A, Rorive S, et al. YAP and TAZ are essential for basal and squamous cell carcinoma initiation. EMBO Rep. 2018;19:7. doi:10.15252/embr.201845809
  • Maglic D, Schlegelmilch K, Dost AF, et al. YAP-TEAD signaling promotes basal cell carcinoma development via a c-JUN/AP1 axis. Embo J. 2018;37:17. doi:10.15252/embj.201798642
  • Akladios B, Mendoza Reinoso V, Cain JE, et al. Positive regulatory interactions between YAP and Hedgehog signalling in skin homeostasis and BCC development in mouse skin in vivo. PLoS One. 2017;12(8):e0183178. doi:10.1371/journal.pone.018317828820907
  • Quan T, Xu Y, Qin Z, et al. Elevated YAP and its downstream targets CCN1 and CCN2 in basal cell carcinoma: impact on keratinocyte proliferation and stromal cell activation. Am J Pathol. 2014;184(4):937–943. doi:10.1016/j.ajpath.2013.12.01724485923
  • Guo P, Kang S, Zhao F. High expression of TAZ/YAP promotes the progression of malignant melanoma and affects the postoperative survival of patients. Pharmazie. 2018;73(11):662–665. doi:10.1691/ph.2018.849930396386
  • Xiong H, Yu Q, Gong Y, et al. Yes-Associated Protein (YAP) promotes tumorigenesis in melanoma cells through stimulation of low-density Lipoprotein Receptor-Related Protein 1 (LRP1). Sci Rep. 2017;7(1):15528. doi:10.1038/s41598-017-14764-429138479
  • Kim MH, Kim CG, Kim SK, et al. YAP-induced PD-L1 expression drives immune evasion in BRAFi-resistant melanoma. Cancer Immunol Res. 2018. doi:10.1158/2326-6066.CIR-17-0320
  • Sambandam SAT, Kasetti RB, Xue L, Dean DC, Lu Q, Li Q. 14-3-3sigma regulates keratinocyte proliferation and differentiation by modulating Yap1 cellular localization. J Invest Dermatol. 2015;135(6):1621–1628. doi:10.1038/jid.2015.4225668240
  • Elbediwy A, Vincent-Mistiaen ZI, Spencer-Dene B, et al. Integrin signalling regulates YAP and TAZ to control skin homeostasis. Development. 2016;143(10):1674–1687. doi:10.1242/dev.13372826989177
  • Jia J, Li C, Luo S, et al. Yes-associated protein contributes to the development of human cutaneous squamous cell carcinoma via activation of RAS. J Invest Dermatol. 2016;136(6):1267–1277. doi:10.1016/j.jid.2016.02.00526902922
  • Li Y, Kong F, Wang J, et al. S100A7 induction is repressed by YAP via the Hippo pathway in A431 cells. Oncotarget. 2016;7(25):38133–38142. doi:10.18632/oncotarget.947727203549
  • Li Y, Kong F, Shao Q, et al. Activity are suppressed by S100A7 via p65/NFkappaB-mediated repression of DeltaNp63. Mol Cancer Res. 2017;15(12):1752–1763. doi:10.1158/1541-7786.MCR-17-034928923839
  • Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J, Jemal A. Global cancer statistics, 2012. CA Cancer J Clin. 2015;65(2):87–108. doi:10.3322/caac.2126225651787
  • Yamana H. [Molecular biology for esophageal squamous cell carcinoma]. Nihon Rinsho. 2011;69(Suppl 6):51–56.
  • Muramatsu T, Imoto I, Matsui T, et al. YAP is a candidate oncogene for esophageal squamous cell carcinoma. Carcinogenesis. 2011;32(3):389–398. doi:10.1093/carcin/bgq25421112960
  • Yeo MK, Kim SH, Kim JM, et al. Correlation of expression of phosphorylated and non-phosphorylated Yes-associated protein with clinicopathological parameters in esophageal squamous cell carcinoma in a Korean population. Anticancer Res. 2012;32(9):3835–3840.22993326
  • Ge L, Smail M, Meng W, et al. Yes-associated protein expression in head and neck squamous cell carcinoma nodal metastasis. PLoS One. 2011;6(11):e27529. doi:10.1371/journal.pone.002752922096589
  • Saladi SV, Ross K, Karaayvaz M, et al. ACTL6A is co-amplified with p63 in squamous cell carcinoma to drive YAP activation, regenerative proliferation, and poor prognosis. Cancer Cell. 2017;31(1):35–49. doi:10.1016/j.ccell.2016.12.00128041841
  • Wang Y, Gersten A, Moleirinho S, Gunn-Moore FJ, Reynolds PA, Prystowsky MB. Fibroblasts in head and neck squamous cell carcinoma associated with perineural invasion have high-level nuclear Yes-Associated Protein (YAP) Expression. Acad Pathol. 2015;2(4):2374289515616972. doi:10.1177/237428951561697228725753
  • Verduci L, Ferraiuolo M, Sacconi A, et al. The oncogenic role of circPVT1 in head and neck squamous cell carcinoma is mediated through the mutant p53/YAP/TEAD transcription-competent complex. Genome Biol. 2017;18(1):237. doi:10.1186/s13059-017-1368-y29262850
  • Snijders AM, Schmidt BL, Fridlyand J, et al. Rare amplicons implicate frequent deregulation of cell fate specification pathways in oral squamous cell carcinoma. Oncogene. 2005;24(26):4232–4242. doi:10.1038/sj.onc.120860115824737
  • Hiemer SE, Zhang L, Kartha VK, et al. A YAP/TAZ-regulated molecular signature is associated with oral squamous cell carcinoma. Mol Cancer Res. 2015;13(6):957–968. doi:10.1158/1541-7786.MCR-14-058025794680
  • Chen X, Gu W, Wang Q, et al. C-MYC and BCL-2 mediate YAP-regulated tumorigenesis in OSCC. Oncotarget. 2018;9(1):668–679. doi:10.18632/oncotarget.2308929416644
  • Wei Z, Wang Y, Li Z, et al. Overexpression of Hippo pathway effector TAZ in tongue squamous cell carcinoma: correlation with clinicopathological features and patients’ prognosis. Int J Stomatol Occlusion Med. 2013;42(10):747–754. doi:10.1111/jop.12062
  • Silverberg SG, Ioffe OB. Pathology of cervical cancer. Cancer J. 2003;9(5):335–347.14690308
  • Liu T, Liu Y, Gao H, Meng F, Yang S, Lou G. Clinical significance of yes-associated protein overexpression in cervical carcinoma: the differential effects based on histotypes. Int J Gynecol Cancer. 2013;23(4):735–742. doi:10.1097/IGC.0b013e31828c861923502453
  • Liu-Chittenden Y, Huang B, Shim JS, et al. Genetic and pharmacological disruption of the TEAD-YAP complex suppresses the oncogenic activity of YAP. Genes Dev. 2012;26(12):1300–1305. doi:10.1101/gad.192856.11222677547
  • Brodowska K, Al-Moujahed A, Marmalidou A, et al. The clinically used photosensitizer Verteporfin (VP) inhibits YAP-TEAD and human retinoblastoma cell growth in vitro without light activation. Exp Eye Res. 2014;124:67–73. doi:10.1016/j.exer.2014.04.01124837142
  • Wang C, Zhu X, Feng W, et al. Verteporfin inhibits YAP function through up-regulating 14-3-3sigma sequestering YAP in the cytoplasm. Am J Cancer Res. 2016;6(1):27–37.27073720
  • Zhou X, Wang Z, Huang W, Lei QY. G protein-coupled receptors: bridging the gap from the extracellular signals to the Hippo pathway. Acta Biochim Biophys Sin (Shanghai). 2015;47(1):10–15. doi:10.1093/abbs/gmu10825491506
  • Liu G, Yu FX, Kim YC, et al. Kaposi sarcoma-associated herpesvirus promotes tumorigenesis by modulating the Hippo pathway. Oncogene. 2015;34(27):3536–3546. doi:10.1038/onc.2014.28125195862
  • Hsu YL, Hung JY, Chou SH, et al. Angiomotin decreases lung cancer progression by sequestering oncogenic YAP/TAZ and decreasing Cyr61 expression. Oncogene. 2015;34(31):4056–4068. doi:10.1038/onc.2014.33325381822
  • Kang W, Huang T, Zhou Y, et al. miR-375 is involved in Hippo pathway by targeting YAP1/TEAD4-CTGF axis in gastric carcinogenesis. Cell Death Dis. 2018;9(2):92. doi:10.1038/s41419-017-0134-029367737