Binding of TFIIIC to SINE Elements Controls the Relocation of Activity-Dependent Neuronal Genes to Transcription Factories

English version České info

In neurons, the timely and accurate expression of genes in response to synaptic activity relies on the interplay between epigenetic modifications of histones, recruitment of regulatory proteins to chromatin and changes to nuclear structure. To identify genes and regulatory elements responsive to synaptic activation in vivo, we performed a genome-wide ChIPseq analysis of acetylated histone H3 using somatosensory cortex of mice exposed to novel enriched environmental (NEE) conditions. We discovered that Short Interspersed Elements (SINEs) located distal to promoters of activity-dependent genes became acetylated following exposure to NEE and were bound by the general transcription factor TFIIIC. Importantly, under depolarizing conditions, inducible genes relocated to transcription factories (TFs), and this event was controlled by TFIIIC. Silencing of the TFIIIC subunit Gtf3c5 in non-stimulated neurons induced uncontrolled relocation to TFs and transcription of activity-dependent genes. Remarkably, in cortical neurons, silencing of Gtf3c5 mimicked the effects of chronic depolarization, inducing a dramatic increase of both dendritic length and branching. These findings reveal a novel and essential regulatory function of both SINEs and TFIIIC in mediating gene relocation and transcription. They also suggest that TFIIIC may regulate the rearrangement of nuclear architecture, allowing the coordinated expression of activity-dependent neuronal genes.

Vyšlo v časopise: Binding of TFIIIC to SINE Elements Controls the Relocation of Activity-Dependent Neuronal Genes to Transcription Factories. PLoS Genet 9(8): e32767. doi:10.1371/journal.pgen.1003699
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003699

Souhrn

Zdroje

1. van PraagH, KempermannG, GageFH (2000) Neural consequences of environmental enrichment. Nat Rev Neurosci 1: 191–198.

2. PhamTM, IckesB, AlbeckD, SoderstromS, GranholmAC, et al. (1999) Changes in brain nerve growth factor levels and nerve growth factor receptors in rats exposed to environmental enrichment for one year. Neuroscience 94: 279–286.

3. FalkenbergT, MohammedAK, HenrikssonB, PerssonH, WinbladB, et al. (1992) Increased expression of brain-derived neurotrophic factor mRNA in rat hippocampus is associated with improved spatial memory and enriched environment. Neurosci Lett 138: 153–156.

4. HeS, MaJ, LiuN, YuX (2010) Early enriched environment promotes neonatal GABAergic neurotransmission and accelerates synapse maturation. J Neurosci 30: 7910–7916.

5. YangXJ, SetoE (2008) The Rpd3/Hda1 family of lysine deacetylases: from bacteria and yeast to mice and men. Nat Rev Mol Cell Biol 9: 206–218.

6. LiB, CareyM, WorkmanJL (2007) The role of chromatin during transcription. Cell 128: 707–719.

7. WangZ, ZangC, CuiK, SchonesDE, BarskiA, et al. (2009) Genome-wide mapping of HATs and HDACs reveals distinct functions in active and inactive genes. Cell 138: 1019–1031.

8. BorrelliE, NestlerEJ, AllisCD, Sassone-CorsiP (2008) Decoding the epigenetic language of neuronal plasticity. Neuron 60: 961–974.

9. RiccioA (2010) Dynamic epigenetic regulation in neurons: enzymes, stimuli and signaling pathways. Nat Neurosci 13: 1330–1337.

10. MuseGW, GilchristDA, NechaevS, ShahR, ParkerJS, et al. (2007) RNA polymerase is poised for activation across the genome. Nat Genet 39: 1507–1511.

11. KimTH, BarreraLO, ZhengM, QuC, SingerMA, et al. (2005) A high-resolution map of active promoters in the human genome. Nature 436: 876–880.

12. SaundersA, CoreLJ, LisJT (2006) Breaking barriers to transcription elongation. Nat Rev Mol Cell Biol 7: 557–567.

13. BarskiA, JothiR, CuddapahS, CuiK, RohTY, et al. (2009) Chromatin poises miRNA- and protein-coding genes for expression. Genome Res 19 (10) 1742–51.

14. SahaRN, WissinkEM, BaileyER, ZhaoM, FargoDC, et al. (2011) Rapid activity-induced transcription of Arc and other IEGs relies on poised RNA polymerase II. Nat Neurosci 14: 848–856.

15. RohTY, CuddapahS, ZhaoK (2005) Active chromatin domains are defined by acetylation islands revealed by genome-wide mapping. Genes Dev 19: 542–552.

16. KimTK, HembergM, GrayJM, CostaAM, BearDM, et al. (2010) Widespread transcription at neuronal activity-regulated enhancers. Nature 465: 182–187.

17. SutherlandH, BickmoreWA (2009) Transcription factories: gene expression in unions? Nat Rev Genet 10: 457–466.

18. LanctotC, CheutinT, CremerM, CavalliG, CremerT (2007) Dynamic genome architecture in the nuclear space: regulation of gene expression in three dimensions. Nat Rev Genet 8: 104–115.

19. EdelmanLB, FraserP (2012) Transcription factories: genetic programming in three dimensions. Curr Opin Genet Dev 22: 110–114.

20. IborraFJ, PomboA, JacksonDA, CookPR (1996) Active RNA polymerases are localized within discrete transcription “factories” in human nuclei. J Cell Sci 109 (Pt 6) 1427–1436.

21. CookPR (2010) A model for all genomes: the role of transcription factories. J Mol Biol 395: 1–10.

22. SchoenfelderS, SextonT, ChakalovaL, CopeNF, HortonA, et al. (2010) Preferential associations between co-regulated genes reveal a transcriptional interactome in erythroid cells. Nat Genet 42: 53–61.

23. Roy-EngelAM (2012) LINEs, SINEs and other retroelements: do birds of a feather flock together? Front Biosci 17: 1345–1361.

24. PauleMR, WhiteRJ (2000) Survey and summary: transcription by RNA polymerases I and III. Nucleic Acids Res 28: 1283–1298.

25. MoqtaderiZ, WangJ, RahaD, WhiteRJ, SnyderM, et al. (2010) Genomic binding profiles of functionally distinct RNA polymerase III transcription complexes in human cells. Nat Struct Mol Biol 17: 635–640.

26. OlerAJ, AllaRK, RobertsDN, WongA, HollenhorstPC, et al. (2010) Human RNA polymerase III transcriptomes and relationships to Pol II promoter chromatin and enhancer-binding factors. Nat Struct Mol Biol 17: 620–628.

27. CarriereL, GrazianiS, AlibertO, Ghavi-HelmY, BoussouarF, et al. (2011) Genomic binding of Pol III transcription machinery and relationship with TFIIS transcription factor distribution in mouse embryonic stem cells. Nucleic Acids Res 40 (1) 270–83.

28. RosenzweigMR, BennettEL, HebertM, MorimotoH (1978) Social grouping cannot account for cerebral effects of enriched environments. Brain Res 153: 563–576.

29. NithianantharajahJ, HannanAJ (2006) Enriched environments, experience-dependent plasticity and disorders of the nervous system. Nat Rev Neurosci 7: 697–709.

30. RiccioA, AlvaniaRS, LonzeBE, RamananN, KimT, et al. (2006) A nitric oxide signaling pathway controls CREB-mediated gene expression in neurons. Mol Cell 21: 283–294.

31. GreenbergME, ZiffEB, GreeneLA (1986) Stimulation of neuronal acetylcholine receptors induces rapid gene transcription. Science 234: 80–83.

32. LyfordGL, YamagataK, KaufmannWE, BarnesCA, SandersLK, et al. (1995) Arc, a growth factor and activity-regulated gene, encodes a novel cytoskeleton-associated protein that is enriched in neuronal dendrites. Neuron 14: 433–445.

33. GuzowskiJF, McNaughtonBL, BarnesCA, WorleyPF (1999) Environment-specific expression of the immediate-early gene Arc in hippocampal neuronal ensembles. Nat Neurosci 2: 1120–1124.

34. WangZ, ZangC, RosenfeldJA, SchonesDE, BarskiA, et al. (2008) Combinatorial patterns of histone acetylations and methylations in the human genome. Nat Genet 40: 897–903.

35. DownTA, HubbardTJ (2005) NestedMICA: sensitive inference of over-represented motifs in nucleic acid sequence. Nucleic Acids Res 33: 1445–1453.

36. MuotriAR, ChuVT, MarchettoMC, DengW, MoranJV, et al. (2005) Somatic mosaicism in neuronal precursor cells mediated by L1 retrotransposition. Nature 435: 903–910.

37. MuotriAR, MarchettoMC, CoufalNG, OefnerR, YeoG, et al. (2010) L1 retrotransposition in neurons is modulated by MeCP2. Nature 468: 443–446.

38. BeauregardA, CurcioMJ, BelfortM (2008) The take and give between retrotransposable elements and their hosts. Annu Rev Genet 42: 587–617.

39. SasakiT, NishiharaH, HirakawaM, FujimuraK, TanakaM, et al. (2008) Possible involvement of SINEs in mammalian-specific brain formation. Proc Natl Acad Sci U S A 105: 4220–4225.

40. TashiroK, TeissierA, KobayashiN, NakanishiA, SasakiT, et al. (2011) A mammalian conserved element derived from SINE displays enhancer properties recapitulating Satb2 expression in early-born callosal projection neurons. PLoS One 6: e28497.

41. WeinerAM, DeiningerPL, EfstratiadisA (1986) Nonviral retroposons: genes, pseudogenes, and transposable elements generated by the reverse flow of genetic information. Annu Rev Biochem 55: 631–661.

42. BoyleAL, BallardSG, WardDC (1990) Differential distribution of long and short interspersed element sequences in the mouse genome: chromosome karyotyping by fluorescence in situ hybridization. Proc Natl Acad Sci U S A 87: 7757–7761.

43. MaDK, JangMH, GuoJU, KitabatakeY, ChangML, et al. (2009) Neuronal activity-induced Gadd45b promotes epigenetic DNA demethylation and adult neurogenesis. Science 323: 1074–1077.

44. RedmondL, KashaniAH, GhoshA (2002) Calcium regulation of dendritic growth via CaM kinase IV and CREB-mediated transcription. Neuron 34: 999–1010.

45. NottA, WatsonPM, RobinsonJD, CrepaldiL, RiccioA (2008) S-Nitrosylation of histone deacetylase 2 induces chromatin remodelling in neurons. Nature 455: 411–415.

46. LinY, BloodgoodBL, HauserJL, LapanAD, KoonAC, et al. (2008) Activity-dependent regulation of inhibitory synapse development by Npas4. Nature 455: 1198–1204.

47. HsiehYJ, KunduTK, WangZ, KovelmanR, RoederRG (1999) The TFIIIC90 subunit of TFIIIC interacts with multiple components of the RNA polymerase III machinery and contains a histone-specific acetyltransferase activity. Mol Cell Biol 19: 7697–7704.

48. MertensC, RoederRG (2008) Different functional modes of p300 in activation of RNA polymerase III transcription from chromatin templates. Mol Cell Biol 28: 5764–5776.

49. NomaK, CamHP, MaraiaRJ, GrewalSI (2006) A role for TFIIIC transcription factor complex in genome organization. Cell 125: 859–872.

50. MoqtaderiZ, StruhlK (2004) Genome-wide occupancy profile of the RNA polymerase III machinery in Saccharomyces cerevisiae reveals loci with incomplete transcription complexes. Mol Cell Biol 24: 4118–4127.

51. HiragaS, BotsiosS, DonzeD, DonaldsonAD (2012) TFIIIC localizes budding yeast ETC sites to the nuclear periphery. Mol Biol Cell 23: 2741–2754.

52. JourdainS, AckerJ, DucrotC, SentenacA, LefebvreO (2003) The tau95 subunit of yeast TFIIIC influences upstream and downstream functions of TFIIIC.DNA complexes. J Biol Chem 278: 10450–10457.

53. StevenseM, MuramotoT, MullerI, ChubbJR (2010) Digital nature of the immediate-early transcriptional response. Development 137: 579–584.

54. OsborneCS, ChakalovaL, BrownKE, CarterD, HortonA, et al. (2004) Active genes dynamically colocalize to shared sites of ongoing transcription. Nat Genet 36: 1065–1071.

55. OsborneCS, ChakalovaL, MitchellJA, HortonA, WoodAL, et al. (2007) Myc dynamically and preferentially relocates to a transcription factory occupied by Igh. PLoS Biol 5: e192.

56. MitchellJA, FraserP (2008) Transcription factories are nuclear subcompartments that remain in the absence of transcription. Genes Dev 22: 20–25.

57. GhamariA, van de CorputMP, ThongjueaS, van CappellenWA, van IjckenW, et al. (2013) In vivo live imaging of RNA polymerase II transcription factories in primary cells. Genes Dev 27: 767–777.

58. WalczakA, SzczepankiewiczAA, RuszczyckiB, MagalskaA, ZamlynskaK, et al. (2013) Novel higher-order epigenetic regulation of the Bdnf gene upon seizures. J Neurosci 33: 2507–2511.

59. TolhuisB, PalstraRJ, SplinterE, GrosveldF, de LaatW (2002) Looping and interaction between hypersensitive sites in the active beta-globin locus. Mol Cell 10: 1453–1465.

60. SpilianakisCG, FlavellRA (2004) Long-range intrachromosomal interactions in the T helper type 2 cytokine locus. Nat Immunol 5: 1017–1027.

61. CarterD, ChakalovaL, OsborneCS, DaiYF, FraserP (2002) Long-range chromatin regulatory interactions in vivo. Nat Genet 32: 623–626.

62. FlavellSW, GreenbergME (2008) Signaling mechanisms linking neuronal activity to gene expression and plasticity of the nervous system. Annu Rev Neurosci 31: 563–590.

63. BadingH, GintyDD, GreenbergME (1993) Regulation of gene expression in hippocampal neurons by distinct calcium signaling pathways. Science 260: 181–186.

64. KolovosP, KnochTA, GrosveldFG, CookPR, PapantonisA (2012) Enhancers and silencers: an integrated and simple model for their function. Epigenetics Chromatin 5: 1.

65. LunyakVV, PrefontaineGG, NunezE, CramerT, JuBG, et al. (2007) Developmentally regulated activation of a SINE B2 repeat as a domain boundary in organogenesis. Science 317: 248–251.

66. RomanAC, Gonzalez-RicoFJ, MoltoE, HernandoH, NetoA, et al. (2011) Dioxin receptor and SLUG transcription factors regulate the insulator activity of B1 SINE retrotransposons via an RNA polymerase switch. Genome Res 21: 422–432.

67. D'AmbrosioC, SchmidtCK, KatouY, KellyG, ItohT, et al. (2008) Identification of cis-acting sites for condensin loading onto budding yeast chromosomes. Genes Dev 22: 2215–2227.

68. HiranoT (2006) At the heart of the chromosome: SMC proteins in action. Nat Rev Mol Cell Biol 7: 311–322.

69. HiranoT, MitchisonTJ (1994) A heterodimeric coiled-coil protein required for mitotic chromosome condensation in vitro. Cell 79: 449–458.

70. ManuelidisL (1984) Different central nervous system cell types display distinct and nonrandom arrangements of satellite DNA sequences. Proc Natl Acad Sci U S A 81: 3123–3127.

71. WittmannM, QueisserG, EderA, WiegertJS, BengtsonCP, et al. (2009) Synaptic activity induces dramatic changes in the geometry of the cell nucleus: interplay between nuclear structure, histone H3 phosphorylation, and nuclear calcium signaling. J Neurosci 29: 14687–14700.

72. BordenJ, ManuelidisL (1988) Movement of the X chromosome in epilepsy. Science 242: 1687–1691.

73. BrownK (2002) Visualizing nuclear proteins together with transcribed and inactive genes in structurally preserved cells. Methods 26: 10–18.