ATX1-Generated H3K4me3 Is Required for Efficient Elongation of Transcription, Not Initiation, at ATX1-Regulated Genes

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Tri-methylated H3 lysine 4 (H3K4me3) is associated with transcriptionally active genes, but its function in the transcription process is still unclear. Point mutations in the catalytic domain of ATX1 (ARABIDOPSIS TRITHORAX1), a H3K4 methyltransferase, and RNAi knockdowns of subunits of the AtCOMPASS–like (Arabidopsis Complex Proteins Associated with Set) were used to address this question. We demonstrate that both ATX1 and AtCOMPASS–like are required for high level accumulation of TBP (TATA-binding protein) and Pol II at promoters and that this requirement is independent of the catalytic histone modifying activity. However, the catalytic function is critically required for transcription as H3K4me3 levels determine the efficiency of transcription elongation. The roles of H3K4me3, ATX1, and AtCOMPASS–like may be of a general relevance for transcription of Trithorax-activated eukaryotic genes.

Vyšlo v časopise: ATX1-Generated H3K4me3 Is Required for Efficient Elongation of Transcription, Not Initiation, at ATX1-Regulated Genes. PLoS Genet 8(12): e32767. doi:10.1371/journal.pgen.1003111
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003111

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Zdroje

1. GardnerKE, AllisCD, StrahlBD (2011) Operating on chromatin, a colorful language where context matters. J Mol Biol 409 : 36–46.

2. ShuklaA, ChaurasiaP, BhaumikSR (2009) Histone methylation and ubiquitination with their cross-talk and roles in gene expression and stability. Cell Mol Life Sci 66 : 1419–1433.

3. RuthenburgAJ, LiH, PatelDJ, AllisCD (2007) Multivalent engagement of chromatin modifications by linked binding modules. Nat Rev Mol Cell Biol 8 : 983–994.

4. WangP, LinC, SmithER, GuoH, SandersonBW, et al. (2009) Global analysis of H3K4 methylation defines MLL family member targets and points to a role for MLL1-mediated H3K4 methylation in the regulation of transcriptional initiation by RNA polymerase II. Mol Cell Biol 29 : 6074–6085.

5. ZhangX, BernatavichuteYV, CokusS, PellegriniM, JacobsenSE (2009) Genome-wide analysis of mono-, di -⁠ and trimethylation of histone H3 lysine 4 in Arabidopsis thaliana. Genome Biol 10: R62.

6. LiX, WangX, HeK, MaY, SuN, et al. (2008) High-resolution mapping of epigenetic modifications of the rice genome uncovers interplay between dna methylation, histone methylation, and gene expression. Plant Cell 20 : 259–276.

7. van DijkK, DingY, MalkaramS, RiethovenJJ, LiuR, et al. (2010) Dynamic Changes in Genome-Wide Histone H3 Lysine 4 Methylation Patterns in Response to Dehydration Stress in Arabidopsis thaliana. BMC Plant Biol 10 : 238.

8. HenikoffS, ShilatifardA (2011) Histone modification: cause or cog? Trends Genet 27 : 389–396.

9. ShilatifardA (2012) The COMPASS Family of Histone H3K4 Methylases: Mechanisms of Regulation in Development and Disease Pathogenesis. Annu Rev Biochem 81 : 65–95.

10. AvramovaZ (2009) Evolution and pleiotropy of TRITHORAX function in Arabidopsis. Int J Dev Biol 53 : 371–381.

11. VeerappanCS, AvramovaZ, MoriyamaEN (2008) Evolution of SET-domain protein families in the unicellular and multicellular Ascomycota fungi. BMC Evol Biol 8 : 190.

12. Santos-RosaH, SchneiderR, BannisterAJ, SherriffJ, BernsteinBE, et al. (2002) Active genes are tri-methylated at K4 of histone H3. Nature 419 : 407–411.

13. BernsteinBE, HumphreyEL, ErlichRL, SchneiderR, BoumanP, et al. (2002) Methylation of histone H3 Lys 4 in coding regions of active genes. Proc Natl Acad Sci U S A 99 : 8695–8700.

14. Alvarez-VenegasR, AvramovaZ (2005) Methylation patterns of histone H3 Lys 4, Lys 9 and Lys 27 in transcriptionally active and inactive Arabidopsis genes and in atx1 mutants. Nucleic Acids Res 33 : 5199–5207.

15. DingY, AvramovaZ, FrommM (2011) Two distinct roles of ARABIDOPSIS HOMOLOG OF TRITHORAX1 (ATX1) at promoters and within transcribed regions of ATX1-regulated genes. Plant Cell 23 : 350–363.

16. NgHH, RobertF, YoungRA, StruhlK (2003) Targeted recruitment of Set1 histone methylase by elongating Pol II provides a localized mark and memory of recent transcriptional activity. Mol Cell 11 : 709–719.

17. SmithE, LinC, ShilatifardA (2011) The super elongation complex (SEC) and MLL in development and disease. Genes Dev 25 : 661–672.

18. EissenbergJC, ShilatifardA (2010) Histone H3 lysine 4 (H3K4) methylation in development and differentiation. Dev Biol 339 : 240–249.

19. TrievelRC, ShilatifardA (2009) WDR5, a complexed protein. Nat Struct Mol Biol 16 : 678–680.

20. JiangD, KongNC, GuX, LiZ, HeY (2011) Arabidopsis COMPASS-like complexes mediate histone H3 lysine-4 trimethylation to control floral transition and plant development. PLoS Genet 7: e1001330 doi:10.1371/journal.pgen.1001330.

21. PatelA, DharmarajanV, CosgroveMS (2008) Structure of WDR5 bound to mixed lineage leukemia protein-1 peptide. J Biol Chem 283 : 32158–32161.

22. SongJJ, KingstonRE (2008) WDR5 interacts with mixed lineage leukemia (MLL) protein via the histone H3-binding pocket. J Biol Chem 283 : 35258–35264.

23. TakahashiYH, WestfieldGH, OleskieAN, TrievelRC, ShilatifardA, et al. (2011) Structural analysis of the core COMPASS family of histone H3K4 methylases from yeast to human. Proc Natl Acad Sci U S A 108 : 20526–20531.

24. ArdehaliMB, MeiA, ZobeckKL, CaronM, LisJT, et al. (2011) Drosophila Set1 is the major histone H3 lysine 4 trimethyltransferase with role in transcription. Embo J 30 : 2817–2828.

25. Garcia-OlmedoF, MolinaA, AlamilloJM, Rodriguez-PalenzuelaP (1998) Plant defense peptides. Biopolymers 47 : 479–491.

26. JiangD, GuX, HeY (2009) Establishment of the winter-annual growth habit via FRIGIDA-mediated histone methylation at FLOWERING LOCUS C in Arabidopsis. Plant Cell 21 : 1733–1746.

27. VermeulenM, MulderKW, DenissovS, PijnappelWW, van SchaikFM, et al. (2007) Selective anchoring of TFIID to nucleosomes by trimethylation of histone H3 lysine 4. Cell 131 : 58–69.

28. OdhoZ, SouthallSM, WilsonJR (2010) Characterization of a novel WDR5-binding site that recruits RbBP5 through a conserved motif to enhance methylation of histone H3 lysine 4 by mixed lineage leukemia protein-1. J Biol Chem 285 : 32967–32976.

29. AvdicV, ZhangP, LanouetteS, GroulxA, TremblayV, et al. (2011) Structural and biochemical insights into MLL1 core complex assembly. Structure 19 : 101–108.

30. DouY, MilneTA, RuthenburgAJ, LeeS, LeeJW, et al. (2006) Regulation of MLL1 H3K4 methyltransferase activity by its core components. Nat Struct Mol Biol 13 : 713–719.

31. PhatnaniHP, GreenleafAL (2006) Phosphorylation and functions of the RNA polymerase II CTD. Genes Dev 20 : 2922–2936.

32. BuratowskiS (2009) Progression through the RNA polymerase II CTD cycle. Mol Cell 36 : 541–546.

33. NechaevS, AdelmanK (2011) Pol II waiting in the starting gates: Regulating the transition from transcription initiation into productive elongation. Biochim Biophys Acta 1809 : 34–45.

34. KomarnitskyP, ChoEJ, BuratowskiS (2000) Different phosphorylated forms of RNA polymerase II and associated mRNA processing factors during transcription. Genes Dev 14 : 2452–2460.

35. EgloffS, MurphyS (2008) Cracking the RNA polymerase II CTD code. Trends Genet 24 : 280–288.

36. WilsonJR, JingC, WalkerPA, MartinSR, HowellSA, et al. (2002) Crystal structure and functional analysis of the histone methyltransferase SET7/9. Cell 111 : 105–115.

37. BriggsSD, BrykM, StrahlBD, CheungWL, DavieJK, et al. (2001) Histone H3 lysine 4 methylation is mediated by Set1 and required for cell growth and rDNA silencing in Saccharomyces cerevisiae. Genes Dev 15 : 3286–3295.

38. RoguevA, SchaftD, ShevchenkoA, PijnappelWW, WilmM, et al. (2001) The Saccharomyces cerevisiae Set1 complex includes an Ash2 homologue and methylates histone 3 lysine 4. Embo J 20 : 7137–7148.

39. MilneTA, DouY, MartinME, BrockHW, RoederRG, et al. (2005) MLL associates specifically with a subset of transcriptionally active target genes. Proc Natl Acad Sci U S A 102 : 14765–14770.

40. LawitSJ, O'GradyK, GurleyWB, Czarnecka-VernerE (2007) Yeast two-hybrid map of Arabidopsis TFIID. Plant Mol Biol 64 : 73–87.

41. BhaumikSR, GreenMR (2001) SAGA is an essential in vivo target of the yeast acidic activator Gal4p. Genes Dev 15 : 1935–1945.

42. LarschanE, WinstonF (2001) The S. cerevisiae SAGA complex functions in vivo as a coactivator for transcriptional activation by Gal4. Genes Dev 15 : 1946–1956.

43. QiuH, HuC, YoonS, NatarajanK, SwansonMJ, et al. (2004) An array of coactivators is required for optimal recruitment of TATA binding protein and RNA polymerase II by promoter-bound Gcn4p. Mol Cell Biol 24 : 4104–4117.

44. KimM, SuhH, ChoEJ, BuratowskiS (2009) Phosphorylation of the yeast Rpb1 C-terminal domain at serines 2, 5, and 7. J Biol Chem 284 : 26421–26426.

45. ChapmanRD, HeidemannM, AlbertTK, MailhammerR, FlatleyA, et al. (2007) Transcribing RNA polymerase II is phosphorylated at CTD residue serine-7. Science 318 : 1780–1782.

46. GomesNP, BjerkeG, LlorenteB, SzostekSA, EmersonBM, et al. (2006) Gene-specific requirement for P-TEFb activity and RNA polymerase II phosphorylation within the p53 transcriptional program. Genes Dev 20 : 601–612.

47. LevineM (2011) Paused RNA polymerase II as a developmental checkpoint. Cell 145 : 502–511.

48. SimsRJ3rd, BelotserkovskayaR, ReinbergD (2004) Elongation by RNA polymerase II: the short and long of it. Genes Dev 18 : 2437–2468.

49. CoreLJ, LisJT (2008) Transcription regulation through promoter-proximal pausing of RNA polymerase II. Science 319 : 1791–1792.

50. CoreLJ, WaterfallJJ, LisJT (2008) Nascent RNA sequencing reveals widespread pausing and divergent initiation at human promoters. Science 322 : 1845–1848.

51. YapKL, ZhouMM (2010) Keeping it in the family: diverse histone recognition by conserved structural folds. Crit Rev Biochem Mol Biol 45 : 488–505.

52. SimsRJ3rd, MillhouseS, ChenCF, LewisBA, Erdjument-BromageH, et al. (2007) Recognition of trimethylated histone H3 lysine 4 facilitates the recruitment of transcription postinitiation factors and pre-mRNA splicing. Mol Cell 28 : 665–676.

53. Rodriguez-GilA, Garcia-MartinezJ, PelechanoV, Munoz-Centeno MdeL, GeliV, et al. (2010) The distribution of active RNA polymerase II along the transcribed region is gene-specific and controlled by elongation factors. Nucleic Acids Res 38 : 4651–4664.

54. KaratasH, TownsendEC, BernardD, DouY, WangS (2010) Analysis of the binding of mixed lineage leukemia 1 (MLL1) and histone 3 peptides to WD repeat domain 5 (WDR5) for the design of inhibitors of the MLL1-WDR5 interaction. J Med Chem 53 : 5179–5185.

55. DingY, FrommM, AvramovaZ (2012) Multiple exposures to drought ‘train’ transcriptional responses in Arabidopsis. Nat Commun 3 : 740.

56. DingY, WangX, SuL, ZhaiJ, CaoS, et al. (2007) SDG714, a histone H3K9 methyltransferase, is involved in Tos17 DNA methylation and transposition in rice. Plant Cell 19 : 9–22.

57. KayserJP, ValletJL, CernyRL (2004) Defining parameters for homology-tolerant database searching. J Biomol Tech 15 : 285–295.

58. DingY, AvramovaZ, FrommM (2011) The Arabidopsis trithorax-like factor ATX1 functions in dehydration stress responses via ABA-dependent and ABA-independent pathways. Plant J 66 : 735–744.