All Title Author
Keywords Abstract

PLOS ONE  2012 

Diversity and Complexity in Chromatin Recognition by TFII-I Transcription Factors in Pluripotent Embryonic Stem Cells and Embryonic Tissues

DOI: 10.1371/journal.pone.0044443

Full-Text   Cite this paper   Add to My Lib


GTF2I and GTF2IRD1 encode a family of closely related transcription factors TFII-I and BEN critical in embryonic development. Both genes are deleted in Williams-Beuren syndrome, a complex genetic disorder associated with neurocognitive, craniofacial, dental and skeletal abnormalities. Although genome-wide promoter analysis has revealed the existence of multiple TFII-I binding sites in embryonic stem cells (ESCs), there was no correlation between TFII-I occupancy and gene expression. Surprisingly, TFII-I recognizes the promoter sequences enriched for H3K4me3/K27me3 bivalent domain, an epigenetic signature of developmentally important genes. Moreover, we discovered significant differences in the association between TFII-I and BEN with the cis-regulatory elements in ESCs and embryonic craniofacial tissues. Our data indicate that in embryonic tissues BEN, but not the highly homologous TFII-I, is primarily recruited to target gene promoters. We propose a “feed-forward model” of gene regulation to explain the specificity of promoter recognition by TFII-I factors in eukaryotic cells.


[1]  Bayarsaihan D, Bitchevaia NK, Enkhmandakh B, Tussie-Luna MI, Leckman JF, et al. (2003) Expression of BEN, a member of TFII-I family of transcription factors, during mouse pre- and postimplantation development. Gene Expres Patterns 3: 577–587.
[2]  Enkhmandakh B, Bitchevaia N, Ruddle F, Bayarsaihan D (2004) The early embryonic expression of TFII-I during mouse preimplantation development. Gene Expr Patterns 4: 25–28.
[3]  Yoshikawa T, Piao Y, Zhong J, Matoba R, Carter MG, et al. (2006) High-throughput screen for genes predominantly expressed in the ICM of mouse blastocysts by whole mount in situ hybridization. Gene Expr Patterns 6: 213–224.
[4]  Makeyev AV, Bayarsaihan D (2009) New TFII-I family target genes involved in embryonic development. Biochem Biophys Res Commun 386: 554–558.
[5]  Chimge N, Makeyev AV, Waigel SJ, Enkhmandakh B, Bayarsaihan D (2012) PI3K/Akt-dependent functions of TFII-I transcription factors in mouse embryonic stem cells. J Cell Biochem 113: 1122–1131.
[6]  Enkhmandakh B, Makeyev AV, Erdenechimeg L, Ruddle FH, Chimge NO, et al. (2009) Essential functions of the Williams-Beuren syndrome-associated TFII-I genes in embryonic development. Proc Natl Acad Sci U S A 106: 181–186.
[7]  Vullhorst D, Buonanno A (2005) Multiple GTF2I-like repeats of general transcription factor 3 exhibit DNA binding properties. Evidence for a common origin as a sequence-specific DNA interaction module. J Biol Chem 280: 31722–31731.
[8]  Bayarsaihan D, Ruddle FH (2000) Isolation and characterization of BEN, a member of the TFII-I family of DNA-binding proteins containing distinct helix-loop-helix domains. Proc Natl Acad Sci USA 97: 7342–7347.
[9]  O’Mahoney JV, Guven KL, Lin J, Joya JE, Robinson CS, et al. (1998) Identification of a novel slow-muscle-fiber enhancer binding protein, MusTRD1. Mol Cell Biol 18: 6641–6652.
[10]  Ring C, Ogata S, Meek L, Song J, Ohta T, et al. (2002) The role of a Williams-Beuren syndrome-associated helix-loop-helix domain-containing transcription factor in activin/nodal signaling. Genes Dev 16: 820–835.
[11]  Ku M, Sokol SY, Wu J, Tussie-Luna MI, Roy AL, et al. (2005) Positive and negative regulation of the transforming growth factor beta/activin target gene goosecoid by the TFII-I family of transcription factors. Mol Cell Biol 25: 7144–7157.
[12]  Chimge NO, Makeyev AV, Ruddle FH, Bayarsaihan D (2008) Identification of the TFII-I family target genes in the vertebrate genome. Proc Natl Acad Sci U S A 105: 9006–9010.
[13]  Tantin D, Tussie-Luna MI, Roy AL, Sharp PA (2004) Regulation of immunoglobulin promoter activity by TFII-I class transcription factors. J Biol Chem 279: 5460–5469.
[14]  Lazebnik MB, Tussie-Luna MI, Roy AL (2008) Determination and functional analysis of the consensus binding site for TFII-I family member BEN, implicated in Williams-Beuren syndrome. J Biol Chem 283: 11078–11082.
[15]  Chen J, Malcolm T, Estable MC, Roeder RG, Sadowski I (2005) TFII-I regulates induction of chromosomally integrated human immunodeficiency virus type 1 long terminal repeat in cooperation with USF. J Virol 79: 4396–4406.
[16]  Roy AL, Du H, Gregor PD, Novina CD, Martinez E, et al. (1997) Cloning of an inr- and E-box-binding protein, TFII-I, that interacts physically and functionally with USF1. EMBO J 16: 7091–7104.
[17]  Ogura Y, Azuma M, Tsuboi Y, Kabe Y, Yamaguchi Y, et al. (2006) TFII-I down-regulates a subset of estrogen-responsive genes through its interaction with an initiator element and estrogen receptor alpha. Genes Cells 11: 373–381.
[18]  Grueneberg DA, Henry RW, Brauer A, Novina CD, Cheriyath V, et al. (1997) A multifunctional DNA-binding protein that promotes the formation of serum response factor/homeodomain complexes: identity to TFII-I. Genes Dev 11: 2482–2493.
[19]  Jackson TA, Taylor HE, Sharma D, Desiderio S, Danoff SK (2005) Vascular endothelial growth factor receptor-2: counter-regulation by the transcription factors, TFII-I and TFII-IRD1. J Biol Chem 280: 29856–29863.
[20]  Crusselle-Davis VJ, Vieira KF, Zhou Z, Anantharaman A, Bungert J (2006) Antagonistic regulation of beta-globin gene expression by helix-loop-helix proteins USF and TFII-I. Mol Cell Biol 26: 6832–6843.
[21]  Makeyev AV, Bayarsaihan D (2011) Molecular basis of Williams-Beuren syndrome: role of TFII-I in craniofacial development. Cleft Plate Craniof J 48: 109–116.
[22]  Shin H, Liu T, Manrai AK, Liu XS (2009) CEAS: cis-regulatory element annotation system. Bioinformatics 25: 2605–2606.
[23]  Bailey TL, Elkan C (1994) “Fitting a mixture model by expectation maximization to discover motifs in biopolymers”. Proceedings of the Second International Conference on Intelligent Systems for Molecular Biology, 28–36, AAAI Press, Menlo Park, California.
[24]  Dennis GJ, Sherman BT, Hosack DA, Yang J, Gao W, et al. (2003) DAVID: Database for Annotation, Visualization, and Integrated Discovery. Genome Biology 4: P3.
[25]  Mikkelsen TS, Ku M, Jaffe DB, Issac B, Lieberman E, et al. (2007) Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 448: 553–560.
[26]  Salbaum JM, Kappen C (2010) Neural tube defect genes and maternal diabetes during pregnancy. Birth Defects Res A Clin Mol Teratol 88: 601–611.
[27]  Maurer J, Fuchs S, Jager R, Kurz B, Sommer L, et al. (2007) Establishment and controlled differentiation of neural crest stem cell lines using conditional transgenesis. Differentiation 75: 580–591.
[28]  Dahl JA, Reiner AH, Klungland A, Wakayama T, Collas P (2010) Histone H3 lysine 27 methylation asymmetry on developmentally-regulated promoters distinguish the first two lineages in mouse preimplantation embryos. PLoS One 5: e9150.
[29]  Li QR, Xing XB, Chen TT, Li RX, Dai J, et al. (2011) Large-scale phosphoproteome profiles comprehensive features of mouse embryonic stem cells. Mol Cell Proteomics 10: M110.
[30]  Kambere MB, Lane RP (2007) Co-regulation of a large and rapidly evolving repertoire of odorant receptor genes. BMC Neurosci Suppl 3: S2.
[31]  Shykind BM, Rohani SC, O’Donnell S, Nemes A, Mendelsohn M, et al. (2004) Gene switching and the stability of odorant receptor gene choice. Cell 117: 801–815.
[32]  Vassalli A, Feinstein P, Mombaerts P (2011) Homeodomain binding motifs modulate the probability of odorant receptor gene choice in transgenic mice. Mol Cell Neurosci 46: 381–396.
[33]  Hoppe R, Frank H, Breer H, Strotmann J (2003) The clustered olfactory receptor gene family 262: Genomic organization, promoter elements, and interacting transcription factors. Genome Res 13: 2674–2685.
[34]  Macquarrie KL, Fong AP, Morse RH, Tapscott SJ (2011) Genome-wide transcription factor binding: beyond direct target regulation. Trends Genet 27: 141–148.
[35]  Bayarsaihan D, Makeyev AV, Enkhmandakh B (2012) Epigenetic modulation by TFII-I during embryonic stem cell differentiation. J Cell Biochem 113: 3056–3060.
[36]  Kyba M, Perlingeiro RC, Daley GQ (2002) HoxB4 confers definitive lymphoid-myeloid engraftment potential on embryonic stem cell and yolk sac hematopoietic progenitors. Cell 109: 29–37.
[37]  Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402–408.
[38]  Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: e45.


comments powered by Disqus

Contact Us


微信:OALib Journal