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PMID: 21378170 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

The histone modifications governing TFF1 transcription mediated by estrogen receptor.

The Journal of biological chemistry ·Vol. 286 ·No. 16 ·2011-04-22 ·Pages 13925-36

Li Y, Sun L, Zhang Y, Wang D, Wang F, Liang J, Gui B, Shang Y

Abstract

Transcription regulation by histone modifications is a major contributing factor to the structural and functional diversity in biology. These modifications are encrypted as histone codes or histone languages and function to establish and maintain heritable epigenetic codes that define the identity and the fate of the cell. Despite recent advances revealing numerous histone modifications associated with transcription regulation, how such modifications dictate the process of transcription is not fully understood. Here we describe spatial and temporal analyses of the histone modifications that are introduced during estrogen receptor α (ERα)-activated transcription. We demonstrated that aborting RNA polymerase II caused a disruption of the histone modifications that are associated with transcription elongation but had a minimal effect on modifications deposited during transcription initiation. We also found that the histone H3S10 phosphorylation mark is catalyzed by mitogen- and stress-activated protein kinase 1 (MSK1) and is recognized by a 14-3-3ζ/14-3-3ε heterodimer through its interaction with H3K4 trimethyltransferase SMYD3 and the p52 subunit of TFIIH. We showed that H3S10 phosphorylation is a prerequisite for H3K4 trimethylation. In addition, we demonstrated that SET8/PR-Set7/KMT5A is required for ERα-regulated transcription and its catalyzed H4K20 monomethylation is implicated in both transcription initiation and elongation. Our experiments provide a relatively comprehensive analysis of histone modifications associated with ERα-regulated transcription and define the biological meaning of several key components of the histone code that governs ERα-regulated transcription.

MeSH Terms
14-3-3 Proteins/metabolism Cell Line, Tumor Chromatin/chemistry DNA/chemistry Estrogen Receptor alpha/metabolism Gene Expression Regulation, Neoplastic Glutathione Transferase/metabolism Histones/chemistry Humans Phosphorylation Promoter Regions, Genetic Protein Structure, Tertiary Ribosomal Protein S6 Kinases, 90-kDa/metabolism Signal Transduction Trefoil Factor-1 Tumor Suppressor Proteins/metabolism
Chemicals
14-3-3 Proteins Chromatin Estrogen Receptor alpha Histones TFF1 protein, human Trefoil Factor-1 Tumor Suppressor Proteins DNA Glutathione Transferase Ribosomal Protein S6 Kinases, 90-kDa mitogen and stress-activated protein kinase 1
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Li Yanyan
Key Laboratory of Carcinogenesis and Translational Research (Ministry of Education), Department of Biochemistry and Molecular Biology, Peking University Health Science Center, Beijing 100191, China.
Sun Luyang
Zhang Yu
Wang Dandan
Wang Feng
Liang Jing
Gui Bin
Shang Yongfeng
References (80)
80 references, click to expand
  1. Two distinct nuclear receptor interaction domains in NSD1, a novel SET protein that exhibits characteristics of both corepressors and coactivators.
    EMBO J. 1998 Jun 15;17(12):3398-412 PMID: 9628876
  2. Estrogen signaling multiple pathways to impact gene transcription.
    Curr Genomics. 2006;7(8):497-508 PMID: 18369406
  3. The peroxisome proliferator-activated receptor gamma/retinoid X receptor alpha heterodimer targets the histone modification enzyme PR-Set7/Setd8 gene and regulates adipogenesis through a positive feedback loop.
    Mol Cell Biol. 2009 Jul;29(13):3544-55 PMID: 19414603
  4. Ordered recruitment of chromatin modifying and general transcription factors to the IFN-beta promoter.
    Cell. 2000 Nov 10;103(4):667-78 PMID: 11106736
  5. Influence of chromatin folding on transcription initiation and elongation by RNA polymerase III.
    Biochemistry. 1992 Sep 1;31(34):7977-88 PMID: 1510985
  6. Covalent modifications of histones during development and disease pathogenesis.
    Nat Struct Mol Biol. 2007 Nov;14(11):1008-16 PMID: 17984963
  7. PIM1-dependent phosphorylation of histone H3 at serine 10 is required for MYC-dependent transcriptional activation and oncogenic transformation.
    Nat Cell Biol. 2007 Aug;9(8):932-44 PMID: 17643117
  8. A site to remember: H3K36 methylation a mark for histone deacetylation.
    Mutat Res. 2007 May 1;618(1-2):130-4 PMID: 17346757
  9. LSD1 is a subunit of the NuRD complex and targets the metastasis programs in breast cancer.
    Cell. 2009 Aug 21;138(4):660-72 PMID: 19703393
  10. The RNA polymerase II trigger loop functions in substrate selection and is directly targeted by alpha-amanitin.
    Mol Cell. 2008 Jun 6;30(5):547-56 PMID: 18538653
  11. Transcriptional activation of the NF-kappaB p65 subunit by mitogen- and stress-activated protein kinase-1 (MSK1).
    EMBO J. 2003 Mar 17;22(6):1313-24 PMID: 12628924
  12. Histones and histone modifications.
    Curr Biol. 2004 Jul 27;14(14):R546-51 PMID: 15268870
  13. The role of chromatin during transcription.
    Cell. 2007 Feb 23;128(4):707-19 PMID: 17320508
  14. Phosphorylation of the RNA polymerase II C-terminal domain by TFIIH kinase is not essential for transcription of Saccharomyces cerevisiae genome.
    Proc Natl Acad Sci U S A. 2009 Aug 25;106(34):14276-80 PMID: 19666497
  15. Requirement of histone methyltransferase SMYD3 for estrogen receptor-mediated transcription.
    J Biol Chem. 2009 Jul 24;284(30):19867-77 PMID: 19509295
  16. The coregulator exchange in transcriptional functions of nuclear receptors.
    Genes Dev. 2000 Jan 15;14(2):121-41 PMID: 10652267
  17. Differential gene regulation by the SRC family of coactivators.
    Genes Dev. 2004 Jul 15;18(14):1753-65 PMID: 15256502
  18. Coordinated regulation of AIB1 transcriptional activity by sumoylation and phosphorylation.
    J Biol Chem. 2006 Aug 4;281(31):21848-21856 PMID: 16760465
  19. Positive histone marks are associated with active transcription from a methylated ICSBP/IRF8 gene.
    Gene. 2008 Mar 15;410(2):259-67 PMID: 18242011
  20. Regulation of transcription by a protein methyltransferase.
    Science. 1999 Jun 25;284(5423):2174-7 PMID: 10381882
  21. CBP/p300-mediated acetylation of histone H3 on lysine 56.
    Nature. 2009 May 7;459(7243):113-7 PMID: 19270680
  22. Crosstalk among Histone Modifications.
    Cell. 2008 Nov 14;135(4):604-7 PMID: 19013272
  23. p38 mitogen-activated protein kinase stimulates estrogen-mediated transcription and proliferation through the phosphorylation and potentiation of the p160 coactivator glucocorticoid receptor-interacting protein 1.
    Mol Endocrinol. 2006 May;20(5):971-83 PMID: 16410316
  24. Hypomethylation-linked activation of PAX2 mediates tamoxifen-stimulated endometrial carcinogenesis.
    Nature. 2005 Dec 15;438(7070):981-7 PMID: 16355216
  25. Phosphorylation of H3S10 blocks the access of H3K9 by specific antibodies and histone methyltransferase. Implication in regulating chromatin dynamics and epigenetic inheritance during mitosis.
    J Biol Chem. 2008 Nov 28;283(48):33585-90 PMID: 18835819
  26. SIP, a novel ankyrin repeat containing protein, sequesters steroid receptor coactivators in the cytoplasm.
    EMBO J. 2007 Jun 6;26(11):2645-57 PMID: 17476305
  27. Signaling to chromatin through histone modifications.
    Cell. 2000 Oct 13;103(2):263-71 PMID: 11057899
  28. Moving AHEAD with an international human epigenome project.
    Nature. 2008 Aug 7;454(7205):711-5 PMID: 18685699
  29. Histone modification levels are predictive for gene expression.
    Proc Natl Acad Sci U S A. 2010 Feb 16;107(7):2926-31 PMID: 20133639
  30. Estrogen-mediated regulation of p38 mitogen-activated protein kinase in human endometrium.
    J Clin Endocrinol Metab. 2006 Jun;91(6):2349-57 PMID: 16522698
  31. Dynamic histone H3 methylation during gene induction: HYPB/Setd2 mediates all H3K36 trimethylation.
    EMBO J. 2008 Jan 23;27(2):406-20 PMID: 18157086
  32. Phosphorylation of histone H3: a balancing act between chromosome condensation and transcriptional activation.
    Trends Genet. 2004 Apr;20(4):214-20 PMID: 15041176
  33. Histone H3 lysine 9 methyltransferase G9a is a transcriptional coactivator for nuclear receptors.
    J Biol Chem. 2006 Mar 31;281(13):8476-85 PMID: 16461774
  34. Phosphorylation of histone H3 at Ser10 facilitates RNA polymerase II release from promoter-proximal pausing in Drosophila.
    Genes Dev. 2007 Nov 1;21(21):2818-31 PMID: 17942706
  35. The 14-3-3 proteins: integrators of diverse signaling cues that impact cell fate and cancer development.
    Trends Cell Biol. 2009 Jan;19(1):16-23 PMID: 19027299
  36. Cyclic, proteasome-mediated turnover of unliganded and liganded ERalpha on responsive promoters is an integral feature of estrogen signaling.
    Mol Cell. 2003 Mar;11(3):695-707 PMID: 12667452
  37. The multiple roles of transcription/repair factor TFIIH.
    Trends Biochem Sci. 1996 Sep;21(9):346-50 PMID: 8870499
  38. Specificity and mechanism of the histone methyltransferase Pr-Set7.
    Genes Dev. 2005 Jun 15;19(12):1444-54 PMID: 15933069
  39. Histone-modifying enzymes: encrypting an enigmatic epigenetic code.
    Curr Opin Struct Biol. 2006 Dec;16(6):753-60 PMID: 17070031
  40. Phosphorylation and functions of the RNA polymerase II CTD.
    Genes Dev. 2006 Nov 1;20(21):2922-36 PMID: 17079683
  41. Nucleosome and chromatin fiber dynamics.
    Curr Opin Struct Biol. 2005 Apr;15(2):188-96 PMID: 15837178
  42. CARM1 mediates the ligand-independent and tamoxifen-resistant activation of the estrogen receptor alpha by cAMP.
    Genes Dev. 2010 Apr 1;24(7):708-19 PMID: 20360387
  43. SMYD3 encodes a histone methyltransferase involved in the proliferation of cancer cells.
    Nat Cell Biol. 2004 Aug;6(8):731-40 PMID: 15235609
  44. [Role of TFIIH in transcriptional regulation].
    Tanpakushitsu Kakusan Koso. 2000 Jun;45(9 Suppl):1505-12 PMID: 10879127
  45. Inhibition of the ERK/MAP kinase pathway attenuates heme oxygenase-1 expression and heme-mediated neuronal injury.
    Neurosci Lett. 2006 May 8;398(3):230-4 PMID: 16443326
  46. Nickel compounds induce phosphorylation of histone H3 at serine 10 by activating JNK-MAPK pathway.
    Carcinogenesis. 2008 Jun;29(6):1276-81 PMID: 18375956
  47. Identification of the MLL2 complex as a coactivator for estrogen receptor alpha.
    J Biol Chem. 2006 Jun 9;281(23):15714-20 PMID: 16603732
  48. The catalytic subunit of the proteasome is engaged in the entire process of estrogen receptor-regulated transcription.
    EMBO J. 2006 Sep 20;25(18):4223-33 PMID: 16957778
  49. The general transcription factors of RNA polymerase II.
    Genes Dev. 1996 Nov 1;10(21):2657-83 PMID: 8946909
  50. Estrogen receptor-alpha directs ordered, cyclical, and combinatorial recruitment of cofactors on a natural target promoter.
    Cell. 2003 Dec 12;115(6):751-63 PMID: 14675539
  51. Structural and functional analysis of SET8, a histone H4 Lys-20 methyltransferase.
    Genes Dev. 2005 Jun 15;19(12):1455-65 PMID: 15933070
  52. Regulation of estrogen rapid signaling through arginine methylation by PRMT1.
    Mol Cell. 2008 Jul 25;31(2):212-21 PMID: 18657504
  53. High-resolution profiling of histone methylations in the human genome.
    Cell. 2007 May 18;129(4):823-37 PMID: 17512414
  54. Mitogen- and stress-activated kinase 1-mediated histone H3 phosphorylation is crucial for cell transformation.
    Cancer Res. 2008 Apr 1;68(7):2538-47 PMID: 18381464
  55. Histone H3 phosphorylation by IKK-alpha is critical for cytokine-induced gene expression.
    Nature. 2003 Jun 5;423(6940):655-9 PMID: 12789342
  56. Chromatin remodelling during development.
    Nature. 2010 Jan 28;463(7280):474-84 PMID: 20110991
  57. Alpha-amanitin: a specific inhibitor of one of two DNA-pendent RNA polymerase activities from calf thymus.
    Biochem Biophys Res Commun. 1970 Jan 6;38(1):165-71 PMID: 4907405
  58. An acetylation switch modulates the transcriptional activity of estrogen-related receptor alpha.
    Mol Endocrinol. 2010 Jul;24(7):1349-58 PMID: 20484414
  59. A nucleosomal function for IkappaB kinase-alpha in NF-kappaB-dependent gene expression.
    Nature. 2003 Jun 5;423(6940):659-63 PMID: 12789343
  60. DOT1L/KMT4 recruitment and H3K79 methylation are ubiquitously coupled with gene transcription in mammalian cells.
    Mol Cell Biol. 2008 Apr;28(8):2825-39 PMID: 18285465
  61. Identification of protein arginine methyltransferase 2 as a coactivator for estrogen receptor alpha.
    J Biol Chem. 2002 Aug 9;277(32):28624-30 PMID: 12039952
  62. Requirement of Rsk-2 for epidermal growth factor-activated phosphorylation of histone H3.
    Science. 1999 Aug 6;285(5429):886-91 PMID: 10436156
  63. Molecular basis for the recognition of phosphorylated and phosphoacetylated histone h3 by 14-3-3.
    Mol Cell. 2005 Oct 28;20(2):199-211 PMID: 16246723
  64. The language of covalent histone modifications.
    Nature. 2000 Jan 6;403(6765):41-5 PMID: 10638745
  65. The SRC family of nuclear receptor coactivators.
    Gene. 2000 Mar 7;245(1):1-11 PMID: 10713439
  66. Real-time observation of the transition from transcription initiation to elongation of the RNA polymerase.
    Proc Natl Acad Sci U S A. 2009 Dec 29;106(52):22175-80 PMID: 20018723
  67. Histone crosstalk between H3S10ph and H4K16ac generates a histone code that mediates transcription elongation.
    Cell. 2009 Sep 18;138(6):1122-36 PMID: 19766566
  68. TFIIH kinase places bivalent marks on the carboxy-terminal domain of RNA polymerase II.
    Mol Cell. 2009 May 15;34(3):387-93 PMID: 19450536
  69. MSK2 and MSK1 mediate the mitogen- and stress-induced phosphorylation of histone H3 and HMG-14.
    EMBO J. 2003 Jun 2;22(11):2788-97 PMID: 12773393
  70. THE OCCURRENCE OF EPSILON-N-METHYL LYSINE IN HISTONES.
    Biochemistry. 1964 Jan;3:10-5 PMID: 14114491
  71. Specific inhibition of nuclear RNA polymerase II by alpha-amanitin.
    Science. 1970 Oct 23;170(3956):447-9 PMID: 4918258
  72. Molecular functions of the histone acetyltransferase chaperone complex Rtt109-Vps75.
    Nat Struct Mol Biol. 2008 Sep;15(9):948-56 PMID: 19172748
  73. The complex language of chromatin regulation during transcription.
    Nature. 2007 May 24;447(7143):407-12 PMID: 17522673
  74. Faithful in vitro transcription by fission yeast RNA polymerase III reveals unique alpha-amanitin sensitivity.
    Gene Expr. 1999;8(3):165-74 PMID: 10634318
  75. Cofactor dynamics and sufficiency in estrogen receptor-regulated transcription.
    Cell. 2000 Dec 8;103(6):843-52 PMID: 11136970
  76. The nucleosomal response associated with immediate-early gene induction is mediated via alternative MAP kinase cascades: MSK1 as a potential histone H3/HMG-14 kinase.
    EMBO J. 1999 Sep 1;18(17):4779-93 PMID: 10469656
  77. Molecular determinants for the tissue specificity of SERMs.
    Science. 2002 Mar 29;295(5564):2465-8 PMID: 11923541
  78. The diverse functions of histone lysine methylation.
    Nat Rev Mol Cell Biol. 2005 Nov;6(11):838-49 PMID: 16261189
  79. DLP, a novel Dim1 family protein implicated in pre-mRNA splicing and cell cycle progression.
    J Biol Chem. 2004 Jul 30;279(31):32839-47 PMID: 15161931
  80. Cracking the RNA polymerase II CTD code.
    Trends Genet. 2008 Jun;24(6):280-8 PMID: 18457900
Article Info
Journal
The Journal of biological chemistry
Abbr.
J Biol Chem
ISSN
1083-351X
Published
2011-04-22
Epub
2011-00-04
Pages
13925-36
Language
English
Region
United States
NLM ID
2985121R
PMCID
PMC3077593
Subset
IM
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