Home LiteratureArticle Details
PMID: 17923685 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

T-bet's ability to regulate individual target genes requires the conserved T-box domain to recruit histone methyltransferase activity and a separate family member-specific transactivation domain.

Molecular and cellular biology ·Vol. 27 ·No. 24 ·2007-12-00 ·Pages 8510-21

Lewis MD, Miller SA, Miazgowicz MM, Beima KM, Weinmann AS

Abstract

Appropriate cellular differentiation and specification rely upon the ability of key developmental transcription factors to precisely establish gene expression patterns. These transcription factors often regulate epigenetic events. However, it has been unclear whether this is the only role that they play in functionally regulating developmental gene expression pathways or whether they also participate in downstream transactivation events at the same promoter. The T-box transcription factor family is important in cellular specification events in many developmental systems, and determining the molecular mechanisms by which this family regulates gene expression networks warrants attention. Here, we examine the mechanism by which T-bet, a critical T-box protein in the immune system, influences transcription. T-bet is both necessary and sufficient to induce permissive histone H3-K4 dimethyl modifications at the CXCR3 and IFN-gamma promoters. A T-bet structure-function analysis revealed that the conserved T-box domain, with a small C-terminal portion, is required for recruiting histone methyltransferase activity to promoters. Interestingly, this function is conserved in the T-box family and is necessary, but not sufficient, to induce transcription, with an independent transactivation activity also required. The requirement for two separable functional activities may ultimately contribute to the stringent role for T-box proteins in establishing specific developmental gene expression pathways.

MeSH Terms
Animals Chromatin/metabolism Conserved Sequence Gene Expression Regulation Histone Methyltransferases Histone-Lysine N-Methyltransferase/metabolism Histones/metabolism Interferon-gamma/genetics Lysine/metabolism Mice Mice, Inbred BALB C Promoter Regions, Genetic/genetics Protein Binding Protein Methyltransferases Protein Structure, Tertiary Receptors, CXCR3/genetics Sequence Deletion Structure-Activity Relationship T-Box Domain Proteins/chemistry,metabolism Transcriptional Activation
Chemicals
Chromatin Histones Receptors, CXCR3 T-Box Domain Proteins T-box transcription factor TBX21 Interferon-gamma Histone Methyltransferases Protein Methyltransferases Histone-Lysine N-Methyltransferase Lysine
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Lewis Megan D
Department of Immunology, University of Washington, Seattle, WA 98195, USA.
Miller Sara A
Miazgowicz Michael M
Beima Kristin M
Weinmann Amy S
References (40)
40 references, click to expand
  1. T-bet antagonizes mSin3a recruitment and transactivates a fully methylated IFN-gamma promoter via a conserved T-box half-site.
    Proc Natl Acad Sci U S A. 2005 Feb 8;102(6):2034-9 PMID: 15684083
  2. Eomesodermin is required for mouse trophoblast development and mesoderm formation.
    Nature. 2000 Mar 2;404(6773):95-9 PMID: 10716450
  3. Three neural tubes in mouse embryos with mutations in the T-box gene Tbx6.
    Nature. 1998 Feb 12;391(6668):695-7 PMID: 9490412
  4. Hlx is induced by and genetically interacts with T-bet to promote heritable T(H)1 gene induction.
    Nat Immunol. 2002 Jul;3(7):652-8 PMID: 12055627
  5. Interaction of GATA-3/T-bet transcription factors regulates expression of sialyl Lewis X homing receptors on Th1/Th2 lymphocytes.
    Proc Natl Acad Sci U S A. 2006 Nov 7;103(45):16894-9 PMID: 17075044
  6. Identification of cooperative monomeric Brachyury sites conferring T-bet responsiveness to the proximal IFN-gamma promoter.
    Int Immunol. 2003 Oct;15(10):1149-60 PMID: 13679385
  7. Distinct effects of T-bet in TH1 lineage commitment and IFN-gamma production in CD4 and CD8 T cells.
    Science. 2002 Jan 11;295(5553):338-42 PMID: 11786644
  8. T-bet is a STAT1-induced regulator of IL-12R expression in naïve CD4+ T cells.
    Nat Immunol. 2002 Jun;3(6):549-57 PMID: 12006974
  9. The T-box family.
    Genome Biol. 2002;3(6):REVIEWS3008 PMID: 12093383
  10. Modulation of chromatin structure regulates cytokine gene expression during T cell differentiation.
    Immunity. 1998 Dec;9(6):765-75 PMID: 9881967
  11. Evolutionarily conserved sequence elements that positively regulate IFN-gamma expression in T cells.
    Proc Natl Acad Sci U S A. 2004 Aug 24;101(34):12622-7 PMID: 15304658
  12. Control of effector CD8+ T cell function by the transcription factor Eomesodermin.
    Science. 2003 Nov 7;302(5647):1041-3 PMID: 14605368
  13. Methylation of lysine 4 on histone H3: intricacy of writing and reading a single epigenetic mark.
    Mol Cell. 2007 Jan 12;25(1):15-30 PMID: 17218268
  14. Identification of a conserved GATA3 response element upstream proximal from the interleukin-13 gene locus.
    J Biol Chem. 2002 Nov 1;277(44):42399-408 PMID: 12205084
  15. A distal conserved sequence element controls Ifng gene expression by T cells and NK cells.
    Immunity. 2006 Nov;25(5):717-29 PMID: 17070076
  16. Homozygous silencing of T-box transcription factor EOMES leads to microcephaly with polymicrogyria and corpus callosum agenesis.
    Nat Genet. 2007 Apr;39(4):454-6 PMID: 17353897
  17. T-box genes in human disorders.
    Hum Mol Genet. 2003 Apr 1;12 Spec No 1:R37-44 PMID: 12668595
  18. Effector and memory CD8+ T cell fate coupled by T-bet and eomesodermin.
    Nat Immunol. 2005 Dec;6(12):1236-44 PMID: 16273099
  19. Regulation of Th2 differentiation and Il4 locus accessibility.
    Annu Rev Immunol. 2006;24:607-56 PMID: 16551261
  20. Role of T-bet in commitment of TH1 cells before IL-12-dependent selection.
    Science. 2001 Jun 8;292(5523):1907-10 PMID: 11397944
  21. IL-2 production in developing Th1 cells is regulated by heterodimerization of RelA and T-bet and requires T-bet serine residue 508.
    J Exp Med. 2005 Nov 7;202(9):1289-300 PMID: 16275766
  22. A distal enhancer in the interferon-gamma (IFN-gamma) locus revealed by genome sequence comparison.
    J Biol Chem. 2004 Feb 6;279(6):4802-10 PMID: 14607827
  23. NFATc2 and T-bet contribute to T-helper-cell-subset-specific regulation of IL-21 expression.
    Proc Natl Acad Sci U S A. 2005 Feb 8;102(6):2016-21 PMID: 15684054
  24. WDR5 associates with histone H3 methylated at K4 and is essential for H3 K4 methylation and vertebrate development.
    Cell. 2005 Jun 17;121(6):859-72 PMID: 15960974
  25. T-box genes in early embryogenesis.
    Dev Dyn. 2004 Jan;229(1):201-18 PMID: 14699590
  26. T-bet regulates Th1 responses through essential effects on GATA-3 function rather than on IFNG gene acetylation and transcription.
    J Exp Med. 2006 Mar 20;203(3):755-66 PMID: 16520391
  27. An interacting network of T-box genes directs gene expression and fate in the zebrafish mesoderm.
    Proc Natl Acad Sci U S A. 2003 Aug 5;100(16):9410-5 PMID: 12883008
  28. A cell autonomous function of Brachyury in T/T embryonic stem cell chimaeras.
    Nature. 1991 Sep 26;353(6342):348-51 PMID: 1922339
  29. Isolating human transcription factor targets by coupling chromatin immunoprecipitation and CpG island microarray analysis.
    Genes Dev. 2002 Jan 15;16(2):235-44 PMID: 11799066
  30. T(H) cell differentiation is accompanied by dynamic changes in histone acetylation of cytokine genes.
    Nat Immunol. 2002 Jul;3(7):643-51 PMID: 12055628
  31. T-box genes in vertebrate development.
    Annu Rev Genet. 2005;39:219-39 PMID: 16285859
  32. Transcription factors T-bet and Runx3 cooperate to activate Ifng and silence Il4 in T helper type 1 cells.
    Nat Immunol. 2007 Feb;8(2):145-53 PMID: 17195845
  33. T-bet binding to newly identified target gene promoters is cell type-independent but results in variable context-dependent functional effects.
    J Biol Chem. 2006 Apr 28;281(17):11992-2000 PMID: 16473879
  34. TBX5 mutations and congenital heart disease: Holt-Oram syndrome revealed.
    Curr Opin Cardiol. 2004 May;19(3):211-5 PMID: 15096952
  35. T-bet is required for optimal proinflammatory CD4+ T-cell trafficking.
    Blood. 2005 Nov 15;106(10):3432-9 PMID: 16014561
  36. Temporal dissection of T-bet functions.
    J Immunol. 2007 Mar 15;178(6):3457-65 PMID: 17339440
  37. A novel transcription factor, T-bet, directs Th1 lineage commitment.
    Cell. 2000 Mar 17;100(6):655-69 PMID: 10761931
  38. T helper cell fate specified by kinase-mediated interaction of T-bet with GATA-3.
    Science. 2005 Jan 21;307(5708):430-3 PMID: 15662016
  39. Cutting edge: changes in histone acetylation at the IL-4 and IFN-gamma loci accompany Th1/Th2 differentiation.
    J Immunol. 2002 Jul 15;169(2):647-50 PMID: 12097365
  40. Th2-specific chromatin remodeling and enhancer activity in the Th2 cytokine locus control region.
    Immunity. 2004 Dec;21(6):865-76 PMID: 15589174
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
1098-5549
Published
2007-12-00
Epub
2007-00-08
Pages
8510-21
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC2169399
Subset
IM
Grants
NIGMS NIH HHS · T32 GM07270 · United States
NIGMS NIH HHS · T32 GM007270 · United States
NCI NIH HHS · CA09537 · United States
NCI NIH HHS · T32 CA009537 · United States
NIAID NIH HHS · R01 AI061061 · United States
NIAID NIH HHS · R56 AI061061 · United States
NIAID NIH HHS · AI061061 · 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: product@genelibs.com