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Article

Zfp703 Is a Wnt/β-Catenin Feedback Suppressor Targeting the β-Catenin/Tcf1 Complex

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Pages 1793-1802 | Received 09 Nov 2015, Accepted 05 Apr 2016, Published online: 17 Mar 2023

REFERENCES

  • Clevers H, Nusse R. 2012. Wnt/beta-catenin signaling and disease. Cell 149:1192–1205. http://dx.doi.org/10.1016/j.cell.2012.05.012.
  • Fodde R, Brabletz T. 2007. Wnt/beta-catenin signaling in cancer stemness and malignant behavior. Curr Opin Cell Biol 19:150–158. http://dx.doi.org/10.1016/j.ceb.2007.02.007.
  • Cancer Genome Atlas Network. 2012. Comprehensive molecular characterization of human colon and rectal cancer. Nature 487:330–337. http://dx.doi.org/10.1038/nature11252.
  • Liu F, van den Broek O, Destree O, Hoppler S. 2005. Distinct roles for Xenopus Tcf/Lef genes in mediating specific responses to Wnt/beta-catenin signalling in mesoderm development. Development 132:5375–5385. http://dx.doi.org/10.1242/dev.02152.
  • Jho EH, Zhang T, Domon C, Joo CK, Freund JN, Costantini F. 2002. Wnt/beta-catenin/Tcf signaling induces the transcription of Axin2, a negative regulator of the signaling pathway. Mol Cell Biol 22:1172–1183. http://dx.doi.org/10.1128/MCB.22.4.1172-1183.2002.
  • Niida A, Hiroko T, Kasai M, Furukawa Y, Nakamura Y, Suzuki Y, Sugano S, Akiyama T. 2004. DKK1, a negative regulator of Wnt signaling, is a target of the beta-catenin/TCF pathway. Oncogene 23:8520–8526. http://dx.doi.org/10.1038/sj.onc.1207892.
  • Yan D, Wallingford JB, Sun TQ, Nelson AM, Sakanaka C, Reinhard C, Harland RM, Fantl WJ, Williams LT. 2001. Cell autonomous regulation of multiple Dishevelled-dependent pathways by mammalian Nkd. Proc Natl Acad Sci U S A 98:3802–3807. http://dx.doi.org/10.1073/pnas.071041898.
  • Cadigan KM, Waterman ML. 2012. TCF/LEFs and Wnt signaling in the nucleus. Cold Spring Harb Perspect Biol 4(11):a007906. http://dx.doi.org/10.1101/cshperspect.a007906.
  • Zeng W, Wharton KA, Jr, Mack JA, Wang K, Gadbaw M, Suyama K, Klein PS, Scott MP. 2000. naked cuticle encodes an inducible antagonist of Wnt signalling. Nature 403:789–795. http://dx.doi.org/10.1038/35001615.
  • Hovanes K, Li TW, Munguia JE, Truong T, Milovanovic T, Lawrence Marsh J, Holcombe RF, Waterman ML. 2001. Beta-catenin-sensitive isoforms of lymphoid enhancer factor-1 are selectively expressed in colon cancer. Nat Genet 28:53–57. http://dx.doi.org/10.1038/ng0501-53.
  • Filali M, Cheng N, Abbott D, Leontiev V, Engelhardt JF. 2002. Wnt-3A/beta-catenin signaling induces transcription from the LEF-1 promoter. J Biol Chem 277:33398–33410. http://dx.doi.org/10.1074/jbc.M107977200.
  • Aguilera O, Fraga MF, Ballestar E, Paz MF, Herranz M, Espada J, Garcia JM, Munoz A, Esteller M, Gonzalez-Sancho JM. 2006. Epigenetic inactivation of the Wnt antagonist DICKKOPF-1 (DKK-1) gene in human colorectal cancer. Oncogene 25:4116–4121. http://dx.doi.org/10.1038/sj.onc.1209439.
  • Guo J, Cagatay T, Zhou G, Chan CC, Blythe S, Suyama K, Zheng L, Pan K, Qian C, Hamelin R, Thibodeau SN, Klein PS, Wharton KA, Liu W. 2009. Mutations in the human naked cuticle homolog NKD1 found in colorectal cancer alter Wnt/Dvl/beta-catenin signaling. PLoS One 4:e7982. http://dx.doi.org/10.1371/journal.pone.0007982.
  • Salahshor S, Woodgett JR. 2005. The links between axin and carcinogenesis. J Clin Pathol 58:225–236. http://dx.doi.org/10.1136/jcp.2003.009506.
  • Garriock RJ, Warkman AS, Meadows SM, D'Agostino S, Krieg PA. 2007. Census of vertebrate Wnt genes: isolation and developmental expression of Xenopus Wnt2, Wnt3, Wnt9a, Wnt9b, Wnt10a, and Wnt16. Dev Dyn 236:1249–1258. http://dx.doi.org/10.1002/dvdy.21156.
  • Yi F, Pereira L, Hoffman JA, Shy BR, Yuen CM, Liu DR, Merrill BJ. 2011. Opposing effects of Tcf3 and Tcf1 control Wnt stimulation of embryonic stem cell self-renewal. Nat Cell Biol 13:762–770. http://dx.doi.org/10.1038/ncb2283.
  • Hikasa H, Ezan J, Itoh K, Li X, Klymkowsky MW, Sokol SY. 2010. Regulation of TCF3 by Wnt-dependent phosphorylation during vertebrate axis specification. Dev Cell 19:521–532. http://dx.doi.org/10.1016/j.devcel.2010.09.005.
  • Cavallo RA, Cox RT, Moline MM, Roose J, Polevoy GA, Clevers H, Peifer M, Bejsovec A. 1998. Drosophila Tcf and Groucho interact to repress Wingless signalling activity. Nature 395:604–608. http://dx.doi.org/10.1038/26982.
  • Roose J, Molenaar M, Peterson J, Hurenkamp J, Brantjes H, Moerer P, van de Wetering M, Destree O, Clevers H. 1998. The Xenopus Wnt effector XTcf-3 interacts with Groucho-related transcriptional repressors. Nature 395:608–612. http://dx.doi.org/10.1038/26989.
  • Polakis P. 2012. Wnt signaling in cancer. Cold Spring Harb Perspect Biol 4(5):a008052. http://dx.doi.org/10.1101/cshperspect.a008052.
  • Hanson AJ, Wallace HA, Freeman TJ, Beauchamp RD, Lee LA, Lee E. 2012. XIAP monoubiquitylates Groucho/TLE to promote canonical Wnt signaling. Mol Cell 45:619–628. http://dx.doi.org/10.1016/j.molcel.2011.12.032.
  • Behrens J, von Kries JP, Kuhl M, Bruhn L, Wedlich D, Grosschedl R, Birchmeier W. 1996. Functional interaction of beta-catenin with the transcription factor LEF-1. Nature 382:638–642. http://dx.doi.org/10.1038/382638a0.
  • Molenaar M, van de Wetering M, Oosterwegel M, Peterson-Maduro J, Godsave S, Korinek V, Roose J, Destree O, Clevers H. 1996. XTcf-3 transcription factor mediates beta-catenin-induced axis formation in Xenopus embryos. Cell 86:391–399. http://dx.doi.org/10.1016/S0092-8674(00)80112-9.
  • Chodaparambil JV, Pate KT, Hepler MR, Tsai BP, Muthurajan UM, Luger K, Waterman ML, Weis WI. 2014. Molecular functions of the TLE tetramerization domain in Wnt target gene repression. EMBO J 33:719–731. http://dx.doi.org/10.1002/embj.201387188.
  • Dunty WC, Jr, Biris KK, Chalamalasetty RB, Taketo MM, Lewandoski M, Yamaguchi TP. 2008. Wnt3a/beta-catenin signaling controls posterior body development by coordinating mesoderm formation and segmentation. Development 135:85–94.
  • Garriock RJ, Chalamalasetty RB, Kennedy MW, Canizales LC, Lewandoski M, Yamaguchi TP. 2015. Lineage tracing of neuromesodermal progenitors reveals novel Wnt-dependent roles in trunk progenitor cell maintenance and differentiation. Development 142:1628–1638. http://dx.doi.org/10.1242/dev.111922.
  • Nakaya MA, Biris K, Tsukiyama T, Jaime S, Rawls JA, Yamaguchi TP. 2005. Wnt3a links left-right determination with segmentation and anteroposterior axis elongation. Development 132:5425–5436. http://dx.doi.org/10.1242/dev.02149.
  • Maretto S, Cordenonsi M, Dupont S, Braghetta P, Broccoli V, Hassan AB, Volpin D, Bressan GM, Piccolo S. 2003. Mapping Wnt/beta-catenin signaling during mouse development and in colorectal tumors. Proc Natl Acad Sci U S A 100:3299–3304. http://dx.doi.org/10.1073/pnas.0434590100.
  • Dunty WC, Jr, Kennedy MW, Chalamalasetty RB, Campbell K, Yamaguchi TP. 2014. Transcriptional profiling of Wnt3a mutants identifies Sp transcription factors as essential effectors of the Wnt/beta-catenin pathway in neuromesodermal stem cells. PLoS One 9:e87018. http://dx.doi.org/10.1371/journal.pone.0087018.
  • Chalamalasetty RB, Garriock RJ, Dunty WC, Jr, Kennedy MW, Jailwala P, Si H, Yamaguchi TP. 2014. Mesogenin 1 is a master regulator of paraxial presomitic mesoderm differentiation. Development 141:4285–4297. http://dx.doi.org/10.1242/dev.110908.
  • Yamaguchi TP, Takada S, Yoshikawa Y, Wu N, McMahon AP. 1999. T (Brachyury) is a direct target of Wnt3a during paraxial mesoderm specification. Genes Dev 13:3185–3190. http://dx.doi.org/10.1101/gad.13.24.3185.
  • Galceran J, Sustmann C, Hsu SC, Folberth S, Grosschedl R. 2004. LEF1-mediated regulation of Delta-like1 links Wnt and Notch signaling in somitogenesis. Genes Dev 18:2718–2723. http://dx.doi.org/10.1101/gad.1249504.
  • Hofmann M, Schuster-Gossler K, Watabe-Rudolph M, Aulehla A, Herrmann BG, Gossler A. 2004. WNT signaling, in synergy with T/TBX6, controls Notch signaling by regulating Dll1 expression in the presomitic mesoderm of mouse embryos. Genes Dev 18:2712–2717. http://dx.doi.org/10.1101/gad.1248604.
  • ten Berge D, Koole W, Fuerer C, Fish M, Eroglu E, Nusse R. 2008. Wnt signaling mediates self-organization and axis formation in embryoid bodies. Cell Stem Cell 3:508–518. http://dx.doi.org/10.1016/j.stem.2008.09.013.
  • Pilon N, Oh K, Sylvestre JR, Savory JG, Lohnes D. 2007. Wnt signaling is a key mediator of Cdx1 expression in vivo. Development 134:2315–2323. http://dx.doi.org/10.1242/dev.001206.
  • Galceran J, Farinas I, Depew MJ, Clevers H, Grosschedl R. 1999. Wnt3a−/−-like phenotype and limb deficiency in Lef1−/− Tcf1−/− mice. Genes Dev 13:709–717. http://dx.doi.org/10.1101/gad.13.6.709.
  • Takada S, Stark KL, Shea MJ, Vassileva G, McMahon JA, McMahon AP. 1994. Wnt-3a regulates somite and tailbud formation in the mouse embryo. Genes Dev 8:174–189. http://dx.doi.org/10.1101/gad.8.2.174.
  • Wu CI, Hoffman JA, Shy BR, Ford EM, Fuchs E, Nguyen H, Merrill BJ. 2012. Function of Wnt/beta-catenin in counteracting Tcf3 repression through the Tcf3-beta-catenin interaction. Development 139:2118–2129. http://dx.doi.org/10.1242/dev.076067.
  • Brault V, Moore R, Kutsch S, Ishibashi M, Rowitch DH, McMahon AP, Sommer L, Boussadia O, Kemler R. 2001. Inactivation of the beta-catenin gene by Wnt1-Cre-mediated deletion results in dramatic brain malformation and failure of craniofacial development. Development 128:1253–1264.
  • Perantoni AO, Timofeeva O, Naillat F, Richman C, Pajni-Underwood S, Wilson C, Vainio S, Dove LF, Lewandoski M. 2005. Inactivation of FGF8 in early mesoderm reveals an essential role in kidney development. Development 132:3859–3871. http://dx.doi.org/10.1242/dev.01945.
  • Biris KK, Dunty WC, Jr, Yamaguchi TP. 2007. Mouse Ripply2 is downstream of Wnt3a and is dynamically expressed during somitogenesis. Dev Dyn 236:3167–3172. http://dx.doi.org/10.1002/dvdy.21342.
  • Iacovino M, Bosnakovski D, Fey H, Rux D, Bajwa G, Mahen E, Mitanoska A, Xu Z, Kyba M. 2011. Inducible cassette exchange: a rapid and efficient system enabling conditional gene expression in embryonic stem and primary cells. Stem Cells 29:1580–1588. http://dx.doi.org/10.1002/stem.715.
  • Chalamalasetty RB, Dunty WC, Jr, Biris KK, Ajima R, Iacovino M, Beisaw A, Feigenbaum L, Chapman DL, Yoon JK, Kyba M, Yamaguchi TP. 2011. The Wnt3a/beta-catenin target gene Mesogenin1 controls the segmentation clock by activating a Notch signalling program. Nat Commun 2:390. http://dx.doi.org/10.1038/ncomms1381.
  • Veeman MT, Slusarski DC, Kaykas A, Louie SH, Moon RT. 2003. Zebrafish prickle, a modulator of noncanonical Wnt/Fz signaling, regulates gastrulation movements. Curr Biol 13:680–685. http://dx.doi.org/10.1016/S0960-9822(03)00240-9.
  • Slorach EM, Chou J, Werb Z. 2011. Zeppo1 is a novel metastasis promoter that represses E-cadherin expression and regulates p120-catenin isoform expression and localization. Genes Dev 25:471–484. http://dx.doi.org/10.1101/gad.1998111.
  • Liu X, Zhang X, Zhan Q, Brock MV, Herman JG, Guo M. 2012. CDX2 serves as a Wnt signaling inhibitor and is frequently methylated in lung cancer. Cancer Biol Ther 13:1152–1157. http://dx.doi.org/10.4161/cbt.21344.
  • Hryniuk A, Grainger S, Savory JG, Lohnes D. 2014. Cdx1 and Cdx2 function as tumor suppressors. J Biol Chem 289:33343–33354. http://dx.doi.org/10.1074/jbc.M114.583823.
  • Weidinger G, Thorpe CJ, Wuennenberg-Stapleton K, Ngai J, Moon RT. 2005. The Sp1-related transcription factors sp5 and sp5-like act downstream of Wnt/beta-catenin signaling in mesoderm and neuroectoderm patterning. Curr Biol 15:489–500. http://dx.doi.org/10.1016/j.cub.2005.01.041.
  • Ginestier C, Sircoulomb F, Charafe-Jauffret E, Chaffanet M, Birnbaum D. 2011. ZNF703: a novel oncogene involved in breast cancer. Med Sci (Paris) 27:357–359. (In French.) http://dx.doi.org/10.1051/medsci/2011274008.
  • Sircoulomb F, Nicolas N, Ferrari A, Finetti P, Bekhouche I, Rousselet E, Lonigro A, Adelaide J, Baudelet E, Esteyries S, Wicinski J, Audebert S, Charafe-Jauffret E, Jacquemier J, Lopez M, Borg JP, Sotiriou C, Popovici C, Bertucci F, Birnbaum D, Chaffanet M, Ginestier C. 2011. ZNF703 gene amplification at 8p12 specifies luminal B breast cancer. EMBO Mol Med 3:153–166. http://dx.doi.org/10.1002/emmm.201100121.
  • Ring DB, Johnson KW, Henriksen EJ, Nuss JM, Goff D, Kinnick TR, Ma ST, Reeder JW, Samuels I, Slabiak T, Wagman AS, Hammond ME, Harrison SD. 2003. Selective glycogen synthase kinase 3 inhibitors potentiate insulin activation of glucose transport and utilization in vitro and in vivo. Diabetes 52:588–595. http://dx.doi.org/10.2337/diabetes.52.3.588.
  • Bennett CN, Ross SE, Longo KA, Bajnok L, Hemati N, Johnson KW, Harrison SD, MacDougald OA. 2002. Regulation of Wnt signaling during adipogenesis. J Biol Chem 277:30998–31004. http://dx.doi.org/10.1074/jbc.M204527200.
  • Dutta S, Sriskanda S, Boobalan E, Alur RP, Elkahloun A, Brooks BP. 2015. nlz1 is required for cilia formation in zebrafish embryogenesis. Dev Biol 406:203–211. http://dx.doi.org/10.1016/j.ydbio.2015.08.019.
  • Zhang X, Peterson KA, Liu XS, McMahon AP, Ohba S. 2013. Gene regulatory networks mediating canonical Wnt signal-directed control of pluripotency and differentiation in embryo stem cells. Stem Cells 31:2667–2679. http://dx.doi.org/10.1002/stem.1371.
  • Gadue P, Huber TL, Paddison PJ, Keller GM. 2006. Wnt and TGF-beta signaling are required for the induction of an in vitro model of primitive streak formation using embryonic stem cells. Proc Natl Acad Sci U S A 103:16806–16811. http://dx.doi.org/10.1073/pnas.0603916103.
  • Lindsley RC, Gill JG, Murphy TL, Langer EM, Cai M, Mashayekhi M, Wang W, Niwa N, Nerbonne JM, Kyba M, Murphy KM. 2008. Mesp1 coordinately regulates cardiovascular fate restriction and epithelial-mesenchymal transition in differentiating ESCs. Cell Stem Cell 3:55–68. http://dx.doi.org/10.1016/j.stem.2008.04.004.
  • Szeto DP, Kimelman D. 2004. Combinatorial gene regulation by Bmp and Wnt in zebrafish posterior mesoderm formation. Development 131:3751–3760. http://dx.doi.org/10.1242/dev.01236.
  • Yoshikawa Y, Fujimori T, McMahon AP, Takada S. 1997. Evidence that absence of Wnt-3a signaling promotes neuralization instead of paraxial mesoderm development in the mouse. Dev Biol 183:234–242. http://dx.doi.org/10.1006/dbio.1997.8502.
  • Gujral TS, MacBeath G. 2010. A system-wide investigation of the dynamics of Wnt signaling reveals novel phases of transcriptional regulation. PLoS One 5:e10024. http://dx.doi.org/10.1371/journal.pone.0010024.
  • Mallo M, Wellik DM, Deschamps J. 2010. Hox genes and regional patterning of the vertebrate body plan. Dev Biol 344:7–15. http://dx.doi.org/10.1016/j.ydbio.2010.04.024.
  • American Veterinary Medical Association. 2013. AVMA guidelines for the euthanasia of animals. American Veterinary Medical Association, Schaumburg, IL.https://www.avma.org/KB/Policies/Pages/Euthanasia-Guidelines.aspx.

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