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Genomic Study of RNA Polymerase II and III SNAP-Bound Promoters Reveals a Gene Transcribed by Both Enzymes and a Broad Use of Common Activators


SNAPc is one of a few basal transcription factors used by both RNA polymerase (pol) II and pol III. To define the set of active SNAPc-dependent promoters in human cells, we have localized genome-wide four SNAPc subunits, GTF2B (TFIIB), BRF2, pol II, and pol III. Among some seventy loci occupied by SNAPc and other factors, including pol II snRNA genes, pol III genes with type 3 promoters, and a few un-annotated loci, most are primarily occupied by either pol II and GTF2B, or pol III and BRF2. A notable exception is the RPPH1 gene, which is occupied by significant amounts of both polymerases. We show that the large majority of SNAPc-dependent promoters recruit POU2F1 and/or ZNF143 on their enhancer region, and a subset also recruits GABP, a factor newly implicated in SNAPc-dependent transcription. These activators associate with pol II and III promoters in G1 slightly before the polymerase, and ZNF143 is required for efficient transcription initiation complex assembly. The results characterize a set of genes with unique properties and establish that polymerase specificity is not absolute in vivo.


Vyšlo v časopise: Genomic Study of RNA Polymerase II and III SNAP-Bound Promoters Reveals a Gene Transcribed by Both Enzymes and a Broad Use of Common Activators. PLoS Genet 8(11): e32767. doi:10.1371/journal.pgen.1003028
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003028

Souhrn

SNAPc is one of a few basal transcription factors used by both RNA polymerase (pol) II and pol III. To define the set of active SNAPc-dependent promoters in human cells, we have localized genome-wide four SNAPc subunits, GTF2B (TFIIB), BRF2, pol II, and pol III. Among some seventy loci occupied by SNAPc and other factors, including pol II snRNA genes, pol III genes with type 3 promoters, and a few un-annotated loci, most are primarily occupied by either pol II and GTF2B, or pol III and BRF2. A notable exception is the RPPH1 gene, which is occupied by significant amounts of both polymerases. We show that the large majority of SNAPc-dependent promoters recruit POU2F1 and/or ZNF143 on their enhancer region, and a subset also recruits GABP, a factor newly implicated in SNAPc-dependent transcription. These activators associate with pol II and III promoters in G1 slightly before the polymerase, and ZNF143 is required for efficient transcription initiation complex assembly. The results characterize a set of genes with unique properties and establish that polymerase specificity is not absolute in vivo.


Zdroje

1. HernandezN (2001) Small nuclear RNA genes: a model system to study fundamental mechanisms of transcription. J Biol Chem 276: 26733–26736.

2. JawdekarGW, HenryRW (2008) Transcriptional regulation of human small nuclear RNA genes. Biochim Biophys Acta 1779: 295–305.

3. KuhlmanTC, ChoH, ReinbergD, HernandezN (1999) The general transcription factors IIA, IIB, IIF, and IIE are required for RNA polymerase II transcription from the human U1 small nuclear RNA promoter. Mol Cell Biol 19: 2130–2141.

4. SchrammL, PendergrastPS, SunY, HernandezN (2000) Different human TFIIIB activities direct RNA polymerase III transcription from TATA-containing and TATA-less promoters. Genes Dev 14: 2650–2663.

5. TeichmannM, WangZ, RoederRG (2000) A stable complex of a novel transcription factor IIB- related factor, human TFIIIB50, and associated proteins mediate selective transcription by RNA polymerase III of genes with upstream promoter elements. Proc Natl Acad Sci U S A 97: 14200–14205.

6. FordE, StrubinM, HernandezN (1998) The Oct-1 POU domain activates snRNA gene transcription by contacting a region in the SNAPc largest subunit that bears sequence similarities to the Oct-1 coactivator OBF-1. Genes Dev 12: 3528–3540.

7. OrioliA, PascaliC, QuartararoJ, DiebelKW, PrazV, et al. (2011) Widespread occurrence of non-canonical transcription termination by human RNA polymerase III. Nucleic Acids Res 39: 5499–5512.

8. KunkelGR, PedersonT (1985) Transcription boundaries of U1 small nuclear RNA. Mol Cell Biol 5: 2332–2340.

9. CuelloP, BoydDC, DyeMJ, ProudfootNJ, MurphyS (1999) Transcription of the human U2 snRNA genes continues beyond the 3′ box in vivo. EMBO J 18: 2867–2877.

10. RosmarinAG, ResendesKK, YangZ, McMillanJN, FlemingSL (2004) GA-binding protein transcription factor: a review of GABP as an integrator of intracellular signaling and protein-protein interactions. Blood Cells Mol Dis 32: 143–154.

11. CanellaD, PrazV, ReinaJH, CousinP, HernandezN (2010) Defining the RNA polymerase III transcriptome: Genome-wide localization of the RNA polymerase III transcription machinery in human cells. Genome Res 20: 710–721.

12. BarskiA, ChepelevI, LikoD, CuddapahS, FlemingAB, et al. (2010) Pol II and its associated epigenetic marks are present at Pol III-transcribed noncoding RNA genes. Nat Struct Mol Biol 17: 629–634.

13. 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.

14. 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.

15. HannonGJ, ChubbA, MaroneyPA, HannonG, AltmanS, et al. (1991) Multiple cis-acting elements are required for RNA polymerase III transcription of the gene encoding H1 RNA, the RNA component of human RNase P. J Biol Chem 266: 22796–22799.

16. LoboSM, HernandezN (1989) A 7 bp mutation converts a human RNA polymerase II snRNA promoter into an RNA polymerase III promoter. Cell 58: 55–67.

17. HenryRW, MittalV, MaB, KobayashiR, HernandezN (1998) SNAP19 mediates the assembly of a functional core promoter complex (SNAPc) shared by RNA polymerases II and III. Genes Dev 12: 2664–2672.

18. HernandezN (1985) Formation of the 3′ end of U1 snRNA is directed by a conserved sequence located downstream of the coding region. EMBO J 4: 1827–1837.

19. YuoCY, AresMJr, WeinerAM (1985) Sequences required for 3′ end formation of human U2 small nuclear RNA. Cell 42: 193–202.

20. BaileyTL, BodenM, BuskeFA, FrithM, GrantCE, et al. (2009) MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 37: W202–208.

21. HerrW, ClearyMA (1995) The POU domain: versatility in transcriptional regulation by a flexible two-in-one DNA-binding domain. Genes Dev 9: 1679–1693.

22. MyslinskiE, GerardMA, KrolA, CarbonP (2006) A genome scale location analysis of human Staf/ZNF143-binding sites suggests a widespread role for human Staf/ZNF143 in mammalian promoters. J Biol Chem 281: 39953–39962.

23. AnnoYN, MyslinskiE, Ngondo-MbongoRP, KrolA, PochO, et al. (2011) Genome-wide evidence for an essential role of the human Staf/ZNF143 transcription factor in bidirectional transcription. Nucleic Acids Res 39: 3116–3127.

24. BoevaV, SurdezD, GuillonN, TirodeF, FejesAP, et al. (2010) De novo motif identification improves the accuracy of predicting transcription factor binding sites in ChIP-Seq data analysis. Nucleic Acids Res 38: e126.

25. Michaud J, Praz V, James Faresse N, JnBaptiste C, Tyagi S, et al.. (Submitted) HCF-1 is a common component of active human HeLa-cell CpG-island promoters and coincides with ZNF143, THAP11, YY-1 and GABP transcription factor occupancy..

26. ValouevA, JohnsonDS, SundquistA, MedinaC, AntonE, et al. (2008) Genome-wide analysis of transcription factor binding sites based on ChIP-Seq data. Nat Methods 5: 829–834.

27. YuA, BaileyAD, WeinerAM (1998) Metaphase fragility of the human RNU1 and RNU2 loci is induced by actinomycin D through a p53-dependent pathway. Hum Mol Genet 7: 609–617.

28. YuA, FanHY, LiaoD, BaileyAD, WeinerAM (2000) Activation of p53 or loss of the Cockayne syndrome group B repair protein causes metaphase fragility of human U1, U2, and 5S genes. Mol Cell 5: 801–810.

29. WhiteRJ, GottliebTM, DownesCS, JacksonSP (1995) Cell cycle regulation of RNA polymerase III transcription. Mol Cell Biol 15: 6653–6662.

30. FairleyJA, ScottPH, WhiteRJ (2003) TFIIIB is phosphorylated, disrupted and selectively released from tRNA promoters during mitosis in vivo. EMBO J 22: 5841–5850.

31. HuP, SamudreK, WuS, SunY, HernandezN (2004) CK2 phosphorylation of Bdp1 executes cell cycle-specific RNA polymerase III transcription repression. Mol Cell 16: 81–92.

32. ChenD, HinkleyCS, HenryRW, HuangS (2002) TBP dynamics in living human cells: constitutive association of TBP with mitotic chromosomes. Mol Biol Cell 13: 276–284.

33. XingH, VanderfordNL, SargeKD (2008) The TBP-PP2A mitotic complex bookmarks genes by preventing condensin action. Nat Cell Biol 10: 1318–1323.

34. DenissovS, van DrielM, VoitR, HekkelmanM, HulsenT, et al. (2007) Identification of novel functional TBP-binding sites and general factor repertoires. EMBO J 26: 944–954.

35. MittalV, MaB, HernandezN (1999) SNAP(c): a core promoter factor with a built-in DNA-binding damper that is deactivated by the Oct-1 POU domain. Genes Dev 13: 1807–1821.

36. MaB, HernandezN (2001) A map of protein-protein contacts within the small nuclear RNA-activating protein complex SNAPc. J Biol Chem 276: 5027–5035.

37. LaiHT, KangYS, StumphWE (2008) Subunit stoichiometry of the Drosophila melanogaster small nuclear RNA activating protein complex (SNAPc). FEBS Lett 582: 3734–3738.

38. KimMK, KangYS, LaiHT, BarakatNH, MaganteD, et al. (2010) Identification of SNAPc subunit domains that interact with specific nucleotide positions in the U1 and U6 gene promoters. Mol Cell Biol 30: 2411–2423.

39. HungKH, StumphWE (2011) Regulation of snRNA gene expression by the Drosophila melanogaster small nuclear RNA activating protein complex (DmSNAPc). Crit Rev Biochem Mol Biol 46: 11–26.

40. Hernandez N (1992) Transcription of vertebrate snRNA genes and related genes. In: McKnight SL, Yamamoto KR, editors. Transcriptional regulation. Cold Spring Harbor: Cold Spring Harbor Laboratory Press. pp. 281–313.

41. EgloffS, O'ReillyD, MurphyS (2008) Expression of human snRNA genes from beginning to end. Biochem Soc Trans 36: 590–594.

42. EgloffS, SzczepaniakSA, DienstbierM, TaylorA, KnightS, et al. (2010) The integrator complex recognizes a new double mark on the RNA polymerase II carboxyl-terminal domain. J Biol Chem 285: 20564–20569.

43. EgloffS, ZaborowskaJ, LaitemC, KissT, MurphyS (2012) Ser7 Phosphorylation of the CTD Recruits the RPAP2 Ser5 Phosphatase to snRNA Genes. Mol Cell 45: 111–122.

44. SmithER, LinC, GarrettAS, ThorntonJ, MohagheghN, et al. (2011) The little elongation complex regulates small nuclear RNA transcription. Mol Cell 44: 954–965.

45. ProudfootNJ (2011) Ending the message: poly(A) signals then and now. Genes Dev 25: 1770–1782.

46. ChenX, FangF, LiouYC, NgHH (2008) Zfp143 regulates Nanog through modulation of Oct4 binding. Stem Cells 26: 2759–2767.

47. SchaubM, MyslinskiE, KrolA, CarbonP (1999) Maximization of selenocysteine tRNA and U6 small nuclear RNA transcriptional activation achieved by flexible utilization of a Staf zinc finger. J Biol Chem 274: 25042–25050.

48. YuanCC, ZhaoX, FlorensL, SwansonSK, WashburnMP, et al. (2007) CHD8 associates with human Staf and contributes to efficient U6 RNA polymerase III transcription. Mol Cell Biol 27: 8729–8738.

49. CanellaD, BernasconiD, GilardiF, LemartelotG, MigliavaccaE, et al. (2012) A multiplicity of factors contributes to selective RNA polymerase III occupancy of a subset of RNA polymerase III genes in mouse liver. Genome Res

50. SepehriS, HernandezN (1997) The largest subunit of human RNA polymerase III is closely related to the largest subunit of yeast and trypanosome RNA polymerase III. Genome Res 7: 1006–1019.

51. LaiJS, HerrW (1992) Ethidium bromide provides a simple tool for identifying genuine DNA-independent protein associations. Proc Natl Acad Sci U S A 89: 6958–6962.

52. MittalV, ClearyMA, HerrW, HernandezN (1996) The Oct-1 POU-specific domain can stimulate small nuclear RNA gene transcription by stabilizing the basal transcription complex SNAPc. Mol Cell Biol 16: 1955–1965.

53. JothiR, CuddapahS, BarskiA, CuiK, ZhaoK (2008) Genome-wide identification of in vivo protein-DNA binding sites from ChIP-Seq data. Nucleic Acids Res 36: 5221–5231.

54. WhitfieldML, ZhengLX, BaldwinA, OhtaT, HurtMM, et al. (2000) Stem-loop binding protein, the protein that binds the 3′ end of histone mRNA, is cell cycle regulated by both translational and posttranslational mechanisms. Mol Cell Biol 20: 4188–4198.

55. ElbashirSM, HarborthJ, LendeckelW, YalcinA, WeberK, et al. (2001) Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 411: 494–498.

56. DomitrovichAM, KunkelGR (2003) Multiple, dispersed human U6 small nuclear RNA genes with varied transcriptional efficiencies. Nucleic Acids Res 31: 2344–2352.

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Genetika Reprodukčná medicína

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