Home LiteratureArticle Details
PMID: 12628927 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Transcription factor YY1 functions as a PcG protein in vivo.

The EMBO journal ·Vol. 22 ·No. 6 ·2003-03-17 ·Pages 1347-58

Atchison L, Ghias A, Wilkinson F, Bonini N, Atchison ML

Abstract

Polycomb group (PcG) proteins function as high molecular weight complexes that maintain transcriptional repression patterns during embryogenesis. The vertebrate DNA binding protein and transcriptional repressor, YY1, shows sequence homology with the Drosophila PcG protein, pleiohomeotic (PHO). YY1 might therefore be a vertebrate PcG protein. We used Drosophila embryo and larval/imaginal disc transcriptional repression systems to determine whether YY1 repressed transcription in a manner consistent with PcG function in vivo. YY1 repressed transcription in Drosophila, and this repression was stable on a PcG-responsive promoter, but not on a PcG-non-responsive promoter. PcG mutants ablated YY1 repression, and YY1 could substitute for PHO in repressing transcription in wing imaginal discs. YY1 functionally compensated for loss of PHO in pho mutant flies and partially corrected mutant phenotypes. Taken together, these results indicate that YY1 functions as a PcG protein. Finally, we found that YY1, as well as Polycomb, required the co-repressor protein CtBP for repression in vivo. These results provide a mechanism for recruitment of vertebrate PcG complexes to DNA and demonstrate new functions for YY1.

MeSH Terms
Alcohol Oxidoreductases Animals DNA-Binding Proteins/chemistry,genetics,metabolism Drosophila/embryology Drosophila Proteins/chemistry,genetics,metabolism Embryo, Nonmammalian Erythroid-Specific DNA-Binding Factors Gene Expression Regulation, Developmental Genes, Insect Genes, Reporter Homeodomain Proteins/chemistry,metabolism Larva Models, Biological Mutation Phenotype Phosphoproteins/genetics,metabolism Polycomb Repressive Complex 1 Polycomb-Group Proteins Promoter Regions, Genetic Repressor Proteins/chemistry,metabolism Transcription Factors/metabolism Transgenes YY1 Transcription Factor
Chemicals
DNA-Binding Proteins Drosophila Proteins Erythroid-Specific DNA-Binding Factors Homeodomain Proteins Pc protein, Drosophila Phosphoproteins Polycomb-Group Proteins Repressor Proteins Transcription Factors YY1 Transcription Factor pho protein, Drosophila phol protein, Drosophila Alcohol Oxidoreductases C-terminal binding protein Polycomb Repressive Complex 1
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Atchison Lakshmi
Department of Biology, Chestnut Hill College, 9601 Germantown Avenue, Philadelphia, PA 19118, USA. [email protected]
Ghias Ayesha
Wilkinson Frank
Bonini Nancy
Atchison Michael L
References (67)
67 references, click to expand
  1. Polycomb silencing and the maintenance of stable chromatin states.
    Results Probl Cell Differ. 1999;25:205-28 PMID: 10339748
  2. RYBP, a new repressor protein that interacts with components of the mammalian Polycomb complex, and with the transcription factor YY1.
    EMBO J. 1999 Jun 15;18(12):3404-18 PMID: 10369680
  3. Stabilization of chromatin structure by PRC1, a Polycomb complex.
    Cell. 1999 Jul 9;98(1):37-46 PMID: 10412979
  4. The DNA-binding polycomb group protein pleiohomeotic mediates silencing of a Drosophila homeotic gene.
    Development. 1999 Sep;126(17):3905-13 PMID: 10433918
  5. Unlocking the mechanisms of transcription factor YY1: are chromatin modifying enzymes the key?
    Gene. 1999 Aug 20;236(2):197-208 PMID: 10452940
  6. Targeted disruption of mouse Yin Yang 1 transcription factor results in peri-implantation lethality.
    Mol Cell Biol. 1999 Oct;19(10):7237-44 PMID: 10490658
  7. Polycomb group protein complexes: do different complexes regulate distinct target genes?
    Biochim Biophys Acta. 1999 Oct 6;1447(1):1-16 PMID: 10500238
  8. Functional antagonism of the Polycomb-Group genes eed and Bmi1 in hemopoietic cell proliferation.
    Genes Dev. 1999 Oct 15;13(20):2691-703 PMID: 10541555
  9. A Drosophila ESC-E(Z) protein complex is distinct from other polycomb group complexes and contains covalently modified ESC.
    Mol Cell Biol. 2000 May;20(9):3069-78 PMID: 10757791
  10. Recruitment of components of Polycomb Group chromatin complexes in Drosophila.
    Development. 2001 Jan;128(1):75-85 PMID: 11092813
  11. The Drosophila Polycomb Group proteins ESC and E(Z) are present in a complex containing the histone-binding protein p55 and the histone deacetylase RPD3.
    Development. 2001 Jan;128(2):275-86 PMID: 11124122
  12. The iab-7 polycomb response element maps to a nucleosome-free region of chromatin and requires both GAGA and pleiohomeotic for silencing activity.
    Mol Cell Biol. 2001 Feb;21(4):1311-8 PMID: 11158316
  13. The polycomb group protein EED interacts with YY1, and both proteins induce neural tissue in Xenopus embryos.
    Mol Cell Biol. 2001 Feb;21(4):1360-9 PMID: 11158321
  14. The Polycomb group--no longer an exclusive club?
    Curr Opin Genet Dev. 2001 Apr;11(2):175-81 PMID: 11250141
  15. Mice doubly deficient for the Polycomb Group genes Mel18 and Bmi1 reveal synergy and requirement for maintenance but not initiation of Hox gene expression.
    Development. 2001 May;128(9):1587-97 PMID: 11290297
  16. Mechanisms of transcriptional memory.
    Nat Rev Mol Cell Biol. 2001 Jun;2(6):409-21 PMID: 11389465
  17. The polycomb-group gene Ezh2 is required for early mouse development.
    Mol Cell Biol. 2001 Jul;21(13):4330-6 PMID: 11390661
  18. Regulation of transcription factor YY1 by acetylation and deacetylation.
    Mol Cell Biol. 2001 Sep;21(17):5979-91 PMID: 11486036
  19. The MCP silencer of the Drosophila Abd-B gene requires both Pleiohomeotic and GAGA factor for the maintenance of repression.
    Development. 2001 Jun;128(11):2163-73 PMID: 11493537
  20. Establishment of Polycomb silencing requires a transient interaction between PC and ESC.
    Genes Dev. 2001 Oct 1;15(19):2509-14 PMID: 11581156
  21. CtBP, an unconventional transcriptional corepressor in development and oncogenesis.
    Mol Cell. 2002 Feb;9(2):213-24 PMID: 11864595
  22. Overlapping and unique roles for C-terminal binding protein 1 (CtBP1) and CtBP2 during mouse development.
    Mol Cell Biol. 2002 Aug;22(15):5296-307 PMID: 12101226
  23. The core of the polycomb repressive complex is compositionally and functionally conserved in flies and humans.
    Mol Cell Biol. 2002 Sep;22(17):6070-8 PMID: 12167701
  24. Pleiohomeotic can link polycomb to DNA and mediate transcriptional repression.
    Mol Cell Biol. 2002 Nov;22(21):7473-83 PMID: 12370294
  25. Ten different Polycomb group genes are required for spatial control of the abdA and AbdB homeotic products.
    Development. 1992 Feb;114(2):493-505 PMID: 1350533
  26. Functional antagonism between YY1 and the serum response factor.
    Mol Cell Biol. 1992 Sep;12(9):4209-14 PMID: 1508214
  27. Transcriptional repression by YY1, a human GLI-Krüppel-related protein, and relief of repression by adenovirus E1A protein.
    Cell. 1991 Oct 18;67(2):377-88 PMID: 1655281
  28. Isolation of a candidate repressor/activator, NF-E1 (YY-1, delta), that binds to the immunoglobulin kappa 3' enhancer and the immunoglobulin heavy-chain mu E1 site.
    Proc Natl Acad Sci U S A. 1991 Nov 1;88(21):9804-8 PMID: 1946405
  29. Detection in situ of genomic regulatory elements in Drosophila.
    Proc Natl Acad Sci U S A. 1987 Dec;84(24):9123-7 PMID: 2827169
  30. Interactions of thePolycomb group of genes with homeotic loci ofDrosophila.
    Roux Arch Dev Biol. 1991 Jul;199(7):387-396 PMID: 28305613
  31. Genetic transformation of Drosophila with transposable element vectors.
    Science. 1982 Oct 22;218(4570):348-53 PMID: 6289436
  32. DNA binding sites for the transcriptional activator/repressor YY1.
    Nucleic Acids Res. 1995 Nov 11;23(21):4457-65 PMID: 7501470
  33. Function of the Polycomb protein is conserved in mice and flies.
    Development. 1995 Sep;121(9):2847-52 PMID: 7555711
  34. Transformation of axial skeleton due to overexpression of bmi-1 in transgenic mice.
    Nature. 1995 Apr 20;374(6524):724-7 PMID: 7715727
  35. Transcriptional silencing by the Polycomb protein in Drosophila embryos.
    EMBO J. 1995 Mar 15;14(6):1209-20 PMID: 7720711
  36. Relief of YY1 transcriptional repression by adenovirus E1A is mediated by E1A-associated protein p300.
    Genes Dev. 1995 May 15;9(10):1188-98 PMID: 7758944
  37. Transcriptional repression of the c-fos gene by YY1 is mediated by a direct interaction with ATF/CREB.
    J Virol. 1995 Jul;69(7):4323-30 PMID: 7769693
  38. An analysis of genes regulated by the multi-functional transcriptional regulator Yin Yang-1.
    Nucleic Acids Res. 1994 Dec 11;22(24):5151-5 PMID: 7816599
  39. Mechanisms of heritable gene repression during development of Drosophila.
    Curr Opin Cell Biol. 1993 Dec;5(6):999-1005 PMID: 7907493
  40. Posterior transformation, neurological abnormalities, and severe hematopoietic defects in mice with a targeted deletion of the bmi-1 proto-oncogene.
    Genes Dev. 1994 Apr 1;8(7):757-69 PMID: 7926765
  41. YY1 represses rat serum amyloid A1 gene transcription and is antagonized by NF-kappa B during acute-phase response.
    Mol Cell Biol. 1994 Sep;14(9):6253-63 PMID: 8065357
  42. Transcriptional activation of Drosophila homeotic genes from distant regulatory elements.
    Trends Genet. 1993 Mar;9(3):75-9 PMID: 8098166
  43. Bifunctional transcriptional properties of YY1 in regulating muscle actin and c-myc gene expression during myogenesis.
    Oncogene. 1994 Apr;9(4):1047-52 PMID: 8134108
  44. DNA bending and orientation-dependent function of YY1 in the c-fos promoter.
    Genes Dev. 1993 Dec;7(12B):2497-509 PMID: 8276234
  45. Novel embryonic and adult homeotic phenotypes are produced by pleiohomeotic mutations in Drosophila.
    Dev Biol. 1994 Feb;161(2):393-407 PMID: 8313991
  46. Characterization of the human granulocyte-macrophage colony-stimulating factor gene promoter: an AP1 complex and an Sp1-related complex transactivate the promoter activity that is suppressed by a YY1 complex.
    Mol Cell Biol. 1996 Jan;16(1):157-67 PMID: 8524292
  47. Characterization of functional domains within the multifunctional transcription factor, YY1.
    J Biol Chem. 1995 Dec 15;270(50):30213-20 PMID: 8530432
  48. A role for mel-18, a Polycomb group-related vertebrate gene, during theanteroposterior specification of the axial skeleton.
    Development. 1996 May;122(5):1513-22 PMID: 8625838
  49. Transcriptional silencing of homeotic genes in Drosophila.
    Bioessays. 1995 Sep;17(9):775-84 PMID: 8763830
  50. Positional cloning of a global regulator of anterior-posterior patterning in mice.
    Nature. 1996 Sep 19;383(6597):250-3 PMID: 8805699
  51. Transcriptional repression by YY1 is mediated by interaction with a mammalian homolog of the yeast global regulator RPD3.
    Proc Natl Acad Sci U S A. 1996 Nov 12;93(23):12845-50 PMID: 8917507
  52. Characterization of the transcriptional regulator YY1. The bipartite transactivation domain is independent of interaction with the TATA box-binding protein, transcription factor IIB, TAFII55, or cAMP-responsive element-binding protein (CPB)-binding protein.
    J Biol Chem. 1997 Jan 17;272(3):1709-17 PMID: 8999850
  53. PcG complexes and chromatin silencing.
    Curr Opin Genet Dev. 1997 Apr;7(2):249-58 PMID: 9115424
  54. Everything you have ever wanted to know about Yin Yang 1......
    Biochim Biophys Acta. 1997 Apr 18;1332(2):F49-66 PMID: 9141463
  55. Murine Polycomb- and trithorax-group genes regulate homeotic pathways and beyond.
    Trends Genet. 1997 May;13(5):167-70 PMID: 9153995
  56. Multiple mechanisms of transcriptional repression by YY1.
    Mol Cell Biol. 1997 Jul;17(7):3723-32 PMID: 9199306
  57. The role of mel-18, a mammalian Polycomb group gene, during IL-7-dependent proliferation of lymphocyte precursors.
    Immunity. 1997 Jul;7(1):135-46 PMID: 9252126
  58. Chromatin-silencing mechanisms in Drosophila maintain patterns of gene expression.
    Trends Genet. 1997 Aug;13(8):314-8 PMID: 9260517
  59. Identification of YY1 sequences necessary for association with the nuclear matrix and for transcriptional repression functions.
    J Cell Biochem. 1998 Mar 15;68(4):484-99 PMID: 9493911
  60. Drosophila CtBP: a Hairy-interacting protein required for embryonic segmentation and hairy-mediated transcriptional repression.
    EMBO J. 1998 Apr 1;17(7):2067-78 PMID: 9524128
  61. The Drosophila esc and E(z) proteins are direct partners in polycomb group-mediated repression.
    Mol Cell Biol. 1998 May;18(5):2825-34 PMID: 9566901
  62. The Drosophila Polycomb group gene pleiohomeotic encodes a DNA binding protein with homology to the transcription factor YY1.
    Mol Cell. 1998 Jun;1(7):1057-64 PMID: 9651589
  63. A conserved sequence motif in Polycomb-response elements.
    Mol Cell. 1998 Jun;1(7):1065-6 PMID: 9651590
  64. The Drosophila Polycomb Group proteins ESC and E(Z) bind directly to each other and co-localize at multiple chromosomal sites.
    Development. 1998 Sep;125(17):3483-96 PMID: 9693151
  65. Genetic interactions and dosage effects of Polycomb group genes in mice.
    Development. 1998 Sep;125(18):3543-51 PMID: 9716520
  66. C-Terminal binding protein is a transcriptional repressor that interacts with a specific class of vertebrate Polycomb proteins.
    Mol Cell Biol. 1999 Jan;19(1):777-87 PMID: 9858600
  67. The oncogene and Polycomb-group gene bmi-1 regulates cell proliferation and senescence through the ink4a locus.
    Nature. 1999 Jan 14;397(6715):164-8 PMID: 9923679
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
2003-03-17
Pages
1347-58
Language
English
Region
England
NLM ID
8208664
PMCID
PMC151054
Subset
IM
Grants
NIGMS NIH HHS · R01 GM042415 · United States
NIDDK NIH HHS · T32 DK007708 · United States
NEI NIH HHS · R29-EY11259 · United States
NIDDK NIH HHS · T32 DK07708 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]