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From vestigial to vestigial-like: the Drosophila gene that has taken wing

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Abstract

The members of the vestigial-like gene family have been identified as homologs of the Drosophila vestigial, which is essential to wing formation. All members of the family are characterized by the presence of the TONDU domain, a highly conserved sequence that mediates their interaction with the transcription factors of the TEAD family. Mammals possess four vestigial-like genes that can be subdivided into two classes, depending on the number of Tondu domains present. While vestigial proteins have been studied in great depth in Drosophila, we still have sketchy knowledge of the functions of vestigial-like proteins in vertebrates. Recent studies have unveiled unexpected functions for some of these members and reveal the role they play in the Hippo pathway. Here, we present the current knowledge about vestigial-like family gene members and their functions, together with their identification in different taxa.

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References

  • Adoutte A, Balavoine G, Lartillot N, Lespinet O, Prud’homme B, De Rosa R (2000) The new animal phylogeny: reliability and implications. Proc Natl Acad Sci U S A 97:4453–4456

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Andrianopoulos A, Timberlake WE (1991) ATTS, a new and conserved DNA binding domain. Plant Cell 3:747–748

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Antonescu CR, Zhang L, Nielsen GP, Rosenberg AE, Dal Cin P, Fletcher CD (2011) Consistent t(1;10) with rearrangements of TGFBR3 and MGEA5 in both myxoinflammatory fibroblastic sarcoma and hemosiderotic fibrolipomatous tumor. Genes Chromosomes Cancer 50:757–764

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ayllon F, Kjærner-Semb E, Furmanek T, Wennevik V, Solberg MF, Dahle G, Lasse Taranger G, Glover KA, Sällman Almén M, Rubin CJ, Edvardsen RB, Wargelius A (2015) The vgll3 locus controls age at maturity in wild and domesticated Atlantic salmon (Salmo salar) males. PLoS Genet 11, e1005628

    Article  PubMed  PubMed Central  Google Scholar 

  • Barrionuevo MG, Aybar MJ, Tribulo C (2014) Two different vestigial like 4 genes are differentially expressed during Xenopus laevis development. Int J Dev Biol 58:369–377

    Article  CAS  PubMed  Google Scholar 

  • Barson NJ, Aykanat T, Hindar K, Baranski M, Bolstad GH, Fiske P, Jacq C, Jensen AJ, Johnston SE, Karlsson S, Kent M, Moen T, Niemelä E, Nome T, Næsje TF, Orell P, Romakkaniemi A, Sægrov H, Urdal K, Erkinaro J, Lien S, Primmer C (2015) Sex-dependent dominance at a single locus maintains variation in age at maturity in salmon. Nature 528:405–408

    Article  CAS  PubMed  Google Scholar 

  • Baylies MK, Bate M, Ruiz Gomez M (1998) Myogenesis: a view from Drosophila. Cell 93:921–927

    Article  CAS  PubMed  Google Scholar 

  • Bernard F, Lalouette A, Gulaud M, Jeantet AY, Cossard R, Zider A, Ferveur JF, Silber J (2003) Control of apterous by vestigial drives indirect flight muscle development in Drosophila. Dev Biol 260:391–403

    Article  CAS  PubMed  Google Scholar 

  • Bernard F, Dutriaux A, Silber J, Lalouette A (2006) Notch pathway repression by vestigial is required to promote indirect flight muscle differentiation in Drosophila melanogaster. Dev Biol 295:164–177

    Article  CAS  PubMed  Google Scholar 

  • Bernard F, Kasherov P, Grenetier S, Dutriaux A, Zider A, Silber J, Lalouette A (2009) Integration of differentiation signals during indirect flight muscle formation by a novel enhancer of Drosophila vestigial gene. Dev Biol 332:258–272

    Article  CAS  PubMed  Google Scholar 

  • Beyer TA, Weiss A, Khomchuk Y, Huang K, Ogunjimi AA, Varelas X, Wrana JL (2013) Switch enhancers interpret TGF-β and Hippo signaling to control cell fate in human embryonic stem cells. Cell Rep 5:1611–1624

    Article  CAS  PubMed  Google Scholar 

  • Bonnet A, Dai F, Brand-Saberi B, Duprez D (2010) Vestigial-like 2 acts downstream of MyoD activation and is associated with skeletal muscle differentiation in chick myogenesis. Mech Dev 127:120–136

    Article  CAS  PubMed  Google Scholar 

  • Bridges CB, Morgan TH (1919) Contributions to the genetics of Drosophila melanogaster. Carnegie Inst Wash Publ 278:123–304

    Google Scholar 

  • Burglin TR (1991) The TEA domain: a novel, highly conserved DNA-binding motif. Cell 66:11–12

    Article  CAS  PubMed  Google Scholar 

  • Cagliero J, Forget A, Daldello E, Silber J, Zider A (2013) The Hippo kinase promotes Scalloped cytoplasmic localization independently of Warts in a CRM1/Exportin1-dependent manner in Drosophila. FASEB J 27:1330–1341

    Article  CAS  PubMed  Google Scholar 

  • Caine C, Kasherov P, Silber J, Lalouette A (2014) Mef2 interacts with the Notch pathway during adult muscle development in Drosophila melanogaster. PLoS One 9, e108149

    Article  PubMed  PubMed Central  Google Scholar 

  • Campbell SD, Duttaroy A, Katzen AL, Chovnick A (1991) Cloning and characterization of the scalloped region of Drosophila melanogaster. Genetics 127:367–380

    CAS  PubMed  PubMed Central  Google Scholar 

  • Campbell S, Inamdar M, Rodrigues V, Raghavan V, Palazzolo M, Chovnick A (1992) The scalloped gene encodes a novel, evolutionarily conserved transcription factor required for sensory organ differentiation in Drosophila. Genes Dev 6:367–379

    Article  CAS  PubMed  Google Scholar 

  • Carroll S, Grenier J, Weatherbe S (2001) From DNA to diversity. Blackwell, London

    Google Scholar 

  • Castilla MA, Lopez-Garcia MA, Atienza MR, Rosa-Rosa JM, Diaz-Martin J, Pecero ML, Vieites B, Romero-Perez L, Benitez J, Calcabrini A et al (2014) VGLL1 expression is associated with a triple-negative basal-like phenotype in breast cancer. Endocr Relat Cancer 21:587–599

    Article  CAS  PubMed  Google Scholar 

  • Chen HH, Maeda T, Mullett SJ, Stewart AF (2004a) Transcription cofactor Vgl-2 is required for skeletal muscle differentiation. Genesis 39:273–279

    Article  CAS  PubMed  Google Scholar 

  • Chen HH, Mullett SJ, Stewart AF (2004b) Vgl-4, a novel member of the vestigial-like family of transcription cofactors, regulates alpha1-adrenergic activation of gene expression in cardiac myocytes. J Biol Chem 279:30800–30806

    Article  CAS  PubMed  Google Scholar 

  • Chen L, Loh PG, Song H (2010) Structural and functional insights into the TEAD-YAP complex in the Hippo signaling pathway. Protein Cell 1:1073–1083

    Article  CAS  PubMed  Google Scholar 

  • Cody NA, Ouellet V, Manderson EN, Quinn MC, Filali-Mouhim A, Tellis P, Zietarska M, Provencher DM, Mes-Masson AM, Cevrette M et al (2007) Transfer of chromosome 3 fragments suppresses tumorigenicity of an ovarian cancer cell line monoallelic for chromosome 3p. Oncogene 26:618–632

    Article  CAS  PubMed  Google Scholar 

  • Cody NA, Shen Z, Ripeau JS, Provencher DM, Mes-Masson AM, Cevrette M, Tonin PN (2009) Characterization of the 3p12.3-pcen region associated with tumor suppression in a novel ovarian cancer cell line model genetically modified by chromosome 3 fragment transfer. Mol Carcinog 48:1077–1092

    Article  CAS  PubMed  Google Scholar 

  • Cousminer DL, Berry DJ, Timpson NJ et al (2013) Genome-wide association and longitudinal analyses reveal genetic loci linking pubertal height growth, pubertal timing and childhood adiposity. Hum Mol Genet 22:2735–2747

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dehal P, Boore JL (2005) Two rounds of whole genome duplication in the ancestral vertebrate. PLoS Biol 3, e314

    Article  PubMed  PubMed Central  Google Scholar 

  • Delanoue R, Legent K, Godefroy N, Flagiello D, Dutriaux A, Vaudin P, Becker J, Silber J (2004) The Drosophila wing differentiation factor vestigial-scalloped is required for cell proliferation and cell survival at the dorso-ventral boundary of the wing imaginal disc. Cell Death Differ 11:110–122

    Article  CAS  PubMed  Google Scholar 

  • Delsuc F, Brinkmann H, Chourrout D, Philippe H (2006) Tunicates and not cephalochordates are the closest living relatives of vertebrates. Nature 439:965–968

    Article  CAS  PubMed  Google Scholar 

  • Deng H, Hughes SC, Bell JB, Simmonds AJ (2009) Alternative requirements for Vestigial, Scalloped, and Dmef2 during muscle differentiation in Drosophila melanogaster. Mol Biol Cell 20:256–269

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Deng H, Bell JB, Simonds AJ (2010) Vestigial is required during late-stage muscle differentiation in Drosophila melanogaster embryos. Mol Biol Cell 21:3304–3316

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Deshpande N, Chopr A, Rangarajan A, Sashidhara LS, Rodrigues V, Krishna S (1997) The human transcription enhancer factor-1, TEF-1, can substitute for Drosophila scalloped during wingblade development. J Biol Chem 272:10664–10668

    Article  CAS  PubMed  Google Scholar 

  • Djiane A, Zaessinger S, Babaoglan AB, Bray SJ (2014) Notch inhibits Yorkie activity in Drosophila wing discs. PLoS One 9, e106211

    Article  PubMed  PubMed Central  Google Scholar 

  • Faucheux C, Naye F, Tréguer K, Fédou S, Thiébaud P, Thézé N (2010) Vestigial like gene family expression in Xenopus: common and divergent features with other vertebrates. Int J Dev Biol 54:1375–1382

    Article  CAS  PubMed  Google Scholar 

  • Frigerio G, Burri M, Bopp D, Baumgartner S, Noll M (1986) Structure of the segmentation gene paired and the Drosophila PRD gene set as part of a gene network. Cell 47:735–746

    Article  CAS  PubMed  Google Scholar 

  • Fristrom D (1969) Cellular degeneration in the production of some mutant phenotypes in Drosophila melanogaster. Mol Gen Genet 103:363–379

    Article  CAS  PubMed  Google Scholar 

  • Gambaro K, Quinn MC, Wojnarowicz PM, Arcand SL, De Ladurantaye M, Barres V, RIPEAU JS, Killary AM, Davis EC, Lavoie J et al (2013) VGLL3 expression is associated with a tumor suppressor phenotype in epithelial ovarian cancer. Mol Oncol 7:513–530

    Article  CAS  PubMed  Google Scholar 

  • Garcia-Bellido A (1975) Genetic control of wing disc development in Drosophila. Ciba Found Symp 161–182

  • Gat-Yablonski G, Frumkin-Ben David R, Bar M, Potievsky O, Phillip M, Lazaz L (2011) Homozygous microdeletion of the POU1F1, CHMP2B, and VGLL3 genes in chromosome 3—a novel syndrome. Am J Med Genet A 155A:2242–2246

    Article  PubMed  Google Scholar 

  • Goulev Y, Fauny JD, Gonzales-Marti B, Flagiello D, Silber J, Zider A (2008) SCALLOPED interacts with YORKIE, the nuclear effector of the hippo tumor-suppressor pathway in Drosophila. Curr Biol 18:435–441

    Article  CAS  PubMed  Google Scholar 

  • Gunther S, Mielcarek M, Kruger M, Braun T (2004) VITO-1 is an essential cofactor of TEF1-dependent muscle-specific gene regulation. Nucleic Acids Res 32:791–802

    Article  PubMed  PubMed Central  Google Scholar 

  • Guo T, Lu Y, Li P, Yin MX, Lv D, Zhang W, Wang H, Zhou Z, Ji H, Zhao Y et al (2013) A novel partner of Scalloped regulates Hippo signaling via antagonizing Scalloped-Yorkie activity. Cell Res 23:1201–1214

    Article  PubMed  PubMed Central  Google Scholar 

  • Guss KA, Mistry H, Skeath JB (2008) Vestigial expression in the Drosophila embryonic central nervous system. Dev Dyn 237:2483–2489

    Article  PubMed  PubMed Central  Google Scholar 

  • Halder G, Carroll SB (2001) Binding of the Vestigial co-factor switches the DNA-target selectivity of the Scalloped selector protein. Development 128:3295–3305

    CAS  PubMed  Google Scholar 

  • Halder G, Polaczyk P, Kraus ME, Hudson A, Kim J, Laughon A, Carroll S (1998) The Vestigial and Scalloped proteins act together to directly regulate wing-specific gene expression in Drosophila. Genes Dev 12:3900–3909

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hallor KH, Sciot R, Staaf J, Heidenblad M, Rydholm A, Bauer HC, Astrom K, Domanski HA, Meis JM, Kindblom LG et al (2009) Two genetic pathways, t(1;10) and amplification of 3p11-12, in myxoinflammatory fibroblastic sarcoma, haemosiderotic fibrolipomatous tumour, and morphologically similar lesions. J Pathol 217:716–727

    Article  CAS  PubMed  Google Scholar 

  • Halperin DS, Pan C, Lusis AJ, Tontonoz P (2013) Vestigial-like 3 is an inhibitor of adipocyte differentiation. J Lipid Res 54:473–481

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hamade A, Rizk F, Genet C, Cousin X (2013) Comparative expression pattern of two vestigial-like 2 genes in zebrafish. Bioeng Biosci 1:11–16

    CAS  Google Scholar 

  • Harvey KF, Zhang X, Thomas DM (2013) The Hippo pathway and human cancer. Nat Rev Cancer 13:246–257

    Article  CAS  PubMed  Google Scholar 

  • Helias-Rodzewicz Z, Perot G, Chibon F, Ferreira C, Lagarde P, Terrier P, Coindre JM, Aurias A (2010) YAP1 and VGLL3, encoding two cofactors of TEAD transcription factors, are amplified and overexpressed in a subset of soft tissue sarcomas. Genes Chromosomes Cancer 49:1161–1171

    Article  CAS  PubMed  Google Scholar 

  • Hiemer SE, Szymaniak AD, Varelas X (2014) The transcriptional regulators TAZ and YAP direct transforming growth factor β-induced tumorigenic phenotypes in breast cancer cells. J Biol Chem 289:13461–13474

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hoegg S, Brinkmann H, Taylor JS, Meyer A (2004) Phylogenetic timing of the fish-specific genome duplication correlates with the diversification of teleost fish. J Mol Evol 59:190–203

    Article  CAS  PubMed  Google Scholar 

  • Jacquemin P, Davidson I (1997) The role of the TEF transcription factors in cardiogenesis and other developmental processes. Trends Cardiovasc Med 7:192–197

    Article  CAS  PubMed  Google Scholar 

  • Jaillon O, Aury JM, Brunet F, Petit JL, Stange-Thomann N, Mauceli E, Bouneau L, Fischer C, Ozouf-Costaz C, Bernot A et al (2004) Genome duplication in the teleost fish Tetraodon nigroviridis reveals the early vertebrate proto-karyotype. Nature 431:946–957

    Article  PubMed  Google Scholar 

  • Jiang W, Yao F, He J, Lv B, Fang W, Zhu W, He G, Chen J (2014) Downregulation of VGLL4 in the progression of esophageal squamous cell carcinoma. Tumour Biol 36:1289–1297

    Article  PubMed  Google Scholar 

  • Jiao S, Wang H, Shi Z, Dong A, Zhang W, Song X, He F, Wang Y, Zhang Z, Wang W et al (2014) A peptide mimicking VGLL4 function acts as a YAP antagonist therapy against gastric cancer. Cancer Cell 25:166–180

    Article  CAS  PubMed  Google Scholar 

  • Jin HS, Park HS, Shin JH, Kim DH, Jun SH, Lee CJ, Lee TH (2011) A novel inhibitor of apoptosis protein (IAP)-interacting protein, Vestigial-like (Vgl)-4, counteracts apoptosis-inhibitory function of IAPs by nuclear sequestration. Biochem Biophys Res Commun 412:454–459

    Article  CAS  PubMed  Google Scholar 

  • Johnson CW, Heernandez-Lagunas L, Feng W, Melvin VS, Williams T, Artinger KB (2011) Vgll2a is required for neural crest cell survival during zebrafish craniofacial development. Dev Biol 357:269–281

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim J, Sebring A, Esch JJ, Kraus ME, Vorwerk K, Magee J, Carroll SB (1996) Integration of positional signals and regulation of wing formation and identity by Drosophila vestigial gene. Nature 382:133–138

    Article  CAS  PubMed  Google Scholar 

  • Kitagawa M (2007) A Sveinsson’s chorioretinal atrophy-associated missense mutation in mouse Tead1 affects its interaction with the co-factors YAP and TAZ. Biochem Biophys Res Commun 361:1022–1026

    Article  CAS  PubMed  Google Scholar 

  • Klein T, Martinez Arias A (1999) The vestigial gene product provides a molecular context for the interpretation of signals during the development of the wing in Drosophila. Development 126:913–925

    CAS  PubMed  Google Scholar 

  • Koontz LM, Liu-Cittenden Y, Yin F, Zheng Y, Yu J, Huang B, Chen Q, Wu S, Pan D (2013) The Hippo effector Yorkie controls normal tissue growth by antagonizing scalloped-mediated default repression. Dev Cell 25:388–401

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kurrasch DM, Cheung CC, Lee FY, Tran PV, Hata K, Ingraham HA (2007) The neonatal ventromedial hypothalamus transcriptome reveals novel markers with spatially distinct patterning. J Neurosci 27:13624–13634

    Article  CAS  PubMed  Google Scholar 

  • Lagha M, Sato T, Regnault B, Cumano A, Zuniga A, Licht J, Relaix F, Buckingham M (2010) Transcriptome analyses based on genetic screens for Pax3 myogenic targets in the mouse embryo. BMC Genomics 11:696

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Legent K, Dutriaux A, Delanoue R, Silber J (2006) Cell cycle genes regulate vestigial and scalloped to ensure normal proliferation in the wing disc of Drosophila melanogaster. Gene Cells 11:907–918

    Article  CAS  Google Scholar 

  • Li H, Wang Z, Zhang W, Quian K, Liao G, Xu W, Zhang S (2015a) VGLL4 inhibits EMT in part through suppressing Wnt/beta-catenin signaling pathway in gastric cancer. Med Oncol 32:83

    Article  CAS  PubMed  Google Scholar 

  • Li N, Yu N, Wang J, Xi H, Lu W, Xu H, Deng M, Zheng G, Liu H (2015b) miR-222/VGLL4/YAP-TEAD1 regulatory loop promotes proliferation and invasion of gastric cancer cells. Am J Cancer Res 5:1158–1168

    PubMed  PubMed Central  Google Scholar 

  • Maeda T, Chapman DL, Stewart AF (2002) Mammalian vestigial-like 2, a cofactor of TEF-1 and MEF2 transcription factors that promotes skeletal muscle differentiation. J Biol Chem 277:48889–48898

    Article  CAS  PubMed  Google Scholar 

  • Magico AC, Bell JB (2011) Identification of a classical bipartite nuclear localization signal in Drosophila TEA/ATTS protein scalloped. PLoS One 6, e21431

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mann RS, Carroll SB (2002) Molecular mechanisms of selector gene function and evolution. Curr Opin Genet Dev 12:592–600

    Article  CAS  PubMed  Google Scholar 

  • Mann CJ, Osborn DP, Hughes SM (2007) Vestigial-like-2b (VITO-1b) and Tead-3a (Tef-5a) expression in zebrafish skeletal muscle, brain and notochord. Gene Expr Patterns 7:827–836

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mann KM, Ward JM, Yew CC, Kovochich A, Dawson DW, Black MA, Brett BT, Sheetz TE, Dupuy AJ, Australian Pancreatic Cancer Genome I et al (2012) Sleeping Beauty mutagenesis reveals cooperating mutations and pathways in pancreatic adenocarcinoma. Proc Natl Acad Sci U S A 109:5934–5941

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maqbool T, Soler C, Jagla T, Daczewska M, Lodha N, Palliyil S, VijayRaghavan K, Jagla K (2006) Shaping leg muscles in Drosophila: role of ladybird a conserved regulator of appendicular myogenesis. PLoS ONE 1, e122

    Article  PubMed  PubMed Central  Google Scholar 

  • Melvin VS, Feng W, Hernandez-Lagunas L, Artinger KB, Williams T (2013) A morpholino-based screen to identify novel genes involved in craniofacial morphogenesis. Dev Dyn 242:817–831

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mielcarek M, Gunther S, Kruger M, Braun T (2002) VITO-1, a novel vestigial related protein is predominantly expressed in the skeletal muscle lineage. Mech Dev 119(Suppl 1):S269–S274

    Article  PubMed  Google Scholar 

  • Mielcarek M, Piotrowska I, Schneider A, Gunther S, Braun T (2009) VITO-2, a new SID domain protein, is expressed in the myogenic lineage during early mouse embryonic development. Gene Expr Patterns 9:129–137

    Article  CAS  PubMed  Google Scholar 

  • Ng M, Diaz-Benjumea FJ, Vincent J-P, Wu J, Cohen SM (1996) Specification of the wing by localized expression of wingless protein. Nature 381:316–318

    Article  CAS  PubMed  Google Scholar 

  • Niro C, Demignon J, Vincent S, Liu Y, Giordani J, Sgarioto N, Favier M, Guillet-Deniau I, Blais A, Maire P (2010) Six1 and Six4 gene expression is necessary to activate the fast-type muscle gene program in the mouse primary myotome. Dev Biol 338:168–182

    Article  CAS  PubMed  Google Scholar 

  • Panopoulou G, Hennig S, Groth D, Krause A, Poustka AJ, Herwig R, Vingron M, Lehrach H (2003) New evidence for genome-wide duplications at the origin of vertebrates using an amphioxus gene set and completed animal genomes. Genome Res 13:1056–1066

    Article  PubMed  PubMed Central  Google Scholar 

  • Paumard-Rigal S, Zider A, Vaudin P, Silber J (1998) Specific interactions between vestigial and scalloped are required to promote wing tissue proliferation in Drosophila melanogaster. Dev Genes Evol 208:440–446

    Article  CAS  PubMed  Google Scholar 

  • Peng Z, Skoog L, Hellborg H, Jonstam G, Wingmo IL, Hjalm-Eriksson M, Harmenberg U, Cedermark GC, Andersson K, Ahrlund-Richter L et al (2014) An expression signature at diagnosis to estimate prostate cancer patients’ overall survival. Prostate Cancer Prostatic Dis 17:81–90

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pobbati AV, Hong W (2013) Emerging roles of TEAD transcription factors and its coactivators in cancers. Cancer Biol Ther 14:390–398

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pobbati AV, Chan SW, Lee I, Song H, Hong W (2012) Structural and functional similarity between the Vgll1-TEAD and the YAP-TEAD complexes. Structure 20:1135–1140

    Article  CAS  PubMed  Google Scholar 

  • Rosenfeld JA, Amron D, Andermann E, Andermann F, Veilleux M, Curry C, Fisher J, Deputy S, Aylsworth AS, Powell CM et al (2012) Genotype-phenotype correlation in interstitial 6q deletions: a report of 12 new cases. Neurogenetics 13:31–47

    Article  PubMed  Google Scholar 

  • Salichs E, Ledda A, Mularoni L, Alba MM, De La Luna S (2009) Genome-wide analysis of histidine repeats reveals their role in the localization of human proteins to the nuclear speckles compartment. PLoS Genet 5, e1000397

    Article  PubMed  PubMed Central  Google Scholar 

  • Sebe-Pedros A, Zheng Y, Ruiz-Trillo I, Pan D (2012) Premetazoan origin of the hippo signaling pathway. Cell Rep 1:13–20

    Article  CAS  PubMed  Google Scholar 

  • Simmonds AJ, Liu X, Soanes KH, Krause HM, Irvine KD, Bell JB (1998) Molecular interactions between Vestigial and Scalloped promote wing formation in Drosophila. Genes Dev 12:3815–3820

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sudarsan V, Anant S, Guptan P, Vijayraghavan K, Skaer H (2001) Myoblast diversification and ectodermal signaling in Drosophila. Dev Cell 1:829–839

    Article  CAS  PubMed  Google Scholar 

  • Tajonar A, Maehr R, Hu G, Sneddon JB, Rivera-Feliciano J, Cohen DE, Elledge SJ, Melton DA (2013) VGLL4 is a novel regulator of survival in human embryonic stem cells. Stem Cells

  • Taylor JS, Braasch I, Frickey T, Meyer A, Van De Peer Y (2003) Genome duplication, a trait shared by 22000 species of ray-finned fish. Genome Res 13:382–390

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Teng AC, Kuraitis D, Deeke SA, Ahmadi A, Dugan SG, Cheng BL, Crowson MG, Burgon PG, Suuronen EJ, Chen HH et al (2010) IRF2BP2 is a skeletal and cardiac muscle-enriched ischemia-inducible activator of VEGFA expression. FASEB J 24:4825–4834

    Article  CAS  PubMed  Google Scholar 

  • Thisse B, Pflumio S, Fürthauer M, Loppin B, Heyer V, Degrave A, Woehl R, Lux A, Steffan T, Charbonnier XQ, Thisse C (2001) Expression of the zebrafish genome during embryogenesis (NIH R01 RR15402). ZFIN direct data submission. http://zfin.org/

  • Vaudin P, Delanoue R, Davidson I, Silber J, Zider A (1999) TONDU (TDU), a novel human protein related to the product of vestigial (vg) gene of Drosophila melanogaster interacts with vertebrate TEF factors and substitutes for Vg function in wing formation. Development 126:4807–4816

    CAS  PubMed  Google Scholar 

  • Wang WZ, Guo X, Duan C, Ma WJ, Zhang YG, Xu P, Gao ZQ, Wang ZF, Yan H, Zhang YF et al (2009) Comparative analysis of gene expression profiles between the normal human cartilage and the one with endemic osteoarthritis. Osteoarthr Cartil 17:83–90

    Article  CAS  PubMed  Google Scholar 

  • Williams JA, Bell JB (1988) Molecular organization of the vestigial region in Drosophila melanogaster. Embo J 7:1355–1363

    CAS  PubMed  PubMed Central  Google Scholar 

  • Williams JA, Atkin AL, Bell JB (1990) The functional organization of the vestigial locus in Drosophila melanogaster. Mol Gen Genet 221:8–16

    Article  CAS  PubMed  Google Scholar 

  • Williams JA, Bell JB, Carroll SB (1991) Control of Drosophila wing and haltere development by the nuclear vestigial gene product. Genes Dev 5:2481–2495

    Article  CAS  PubMed  Google Scholar 

  • Williams JA, Paddock SW, Carroll SB (1993) Pattern formation in a secondary field: a hierarchy of regulatory genes subdivides the developing Drosophila wing disc into discrete subregions. Development 117:571–584

    CAS  PubMed  Google Scholar 

  • Williams JA, Paddock SW, Vorwerk K, Carroll SB (1994) Organization of wing formation and induction of a wing-patterning gene at the dorsal/ventral compartment boundary. Nature 368:299–305

    Article  CAS  PubMed  Google Scholar 

  • Wu S, Liu Y, Zheng Y, Dong J, Pan D (2008) The TEAD/TEF family protein scalloped mediates transcriptional output of the Hippo growth-regulatory pathway. Dev Cell 14:388–398

    Article  CAS  PubMed  Google Scholar 

  • Xiao JH, Davidson I, Matthes H, Garnier JM, Chambon P (1991) Cloning, expression, and transcriptional properties of the human enhancer factor TEF-1. Cell 65:551–568

    Article  CAS  PubMed  Google Scholar 

  • Zhang L, Ren F, Zhang Q, Chen Y, Wang B, Jiang J (2008) The TEAD/TEF family of transcription factor scalloped mediates Hippo signaling in organ size control. Dev Cell 14:377–387

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang W, Gao Y, Li P, Shi Z, Guo T, Li F, Han X, Feng Y, Zheng C, Wang Z et al (2014) VGLL4 functions as a new tumor suppressor in lung cancer by negatively regulating the YAP-TEAD transcriptional complex. Cell Res 24:331–343

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

This work was supported by the University of Bordeaux and the Centre National de la Recherche Scientifique (CNRS). We thank Joanna Munro for the careful reading of the manuscript and helpful suggestions. We thank reviewers for their constructive comments on an earlier version of the manuscript.

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Authors and Affiliations

  1. Univ. Bordeaux, BMGIC, U1035, F-33000, Bordeaux, France

    Emilie Simon, Corinne Faucheux, Nadine Thézé & Pierre Thiébaud

  2. INSERM, BMGIC, U1035, F-33000, Bordeaux, France

    Emilie Simon, Corinne Faucheux, Nadine Thézé & Pierre Thiébaud

  3. Univ Paris Diderot, Sorbonne Paris Cité, IJM, UMR 7592 CNRS, F-75205, Paris, France

    Alain Zider

  4. Univ. Bordeaux, INSERM U1035, 146 rue Léo Saignat, 33076, Bordeaux CEDEX, France

    Pierre Thiébaud

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  2. Corinne Faucheux
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  3. Alain Zider
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  4. Nadine Thézé
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  5. Pierre Thiébaud
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Corresponding author

Correspondence to Pierre Thiébaud.

Additional information

Communicated by Claude Desplan

Nadine Thézé and Pierre Thiébaud are co-senior authors.

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Simon, E., Faucheux, C., Zider, A. et al. From vestigial to vestigial-like: the Drosophila gene that has taken wing. Dev Genes Evol 226, 297–315 (2016). https://doi.org/10.1007/s00427-016-0546-3

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  • DOI: https://doi.org/10.1007/s00427-016-0546-3

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