UVB Induces a Genome-Wide Acting Negative Regulatory Mechanism That Operates at the Level of Transcription Initiation in Human Cells

English version České info

Our genome is continuously exposed to genotoxic attacks that generate aberrant DNA structures. These can block the transcribing DNA-dependent RNA polymerase II (Pol II) enzyme and can lead to deleterious cellular processes. Cells have developed several mechanisms to stop Pol II, repair the roadblocks and to restore normal polymerase traffic. Numerous efforts investigated the fate of blocked Pol II during DNA repair mechanisms and suggested that stopped Pol II complexes can either backtrack, be removed or bypass the lesions to allow repair. We carried out a genome-wide analysis of Pol II behavior upon a DNA damaging stress, UVB, which is relevant from the public health standpoint. Thus, we could follow UVB-induced Pol II behavior changes on every human gene over time. We uncovered a novel UV induced negative regulatory mechanism, which inhibits the recruitment of Pol II to the promoters of about 93% of all transcribed genes, and a small subset of gene (including regulators of repair, cell growth and survival) that escapes this negative regulation, probably because their gene products are required during/after UVB irradiation. Thus, we uncover how a cell induces a global negative regulation at the level of transcription initiation in response to a genotoxic stress.

Vyšlo v časopise: UVB Induces a Genome-Wide Acting Negative Regulatory Mechanism That Operates at the Level of Transcription Initiation in Human Cells. PLoS Genet 10(7): e32767. doi:10.1371/journal.pgen.1004483
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004483

Souhrn

Zdroje

1. GuentherMG, LevineSS, BoyerLA, JaenischR, YoungRA (2007) A chromatin landmark and transcription initiation at most promoters in human cells. Cell 130: 77–88.

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

3. ZeitlingerJ, StarkA, KellisM, HongJW, NechaevS, et al. (2007) RNA polymerase stalling at developmental control genes in the Drosophila melanogaster embryo. Nat Genet 39: 1512–1516.

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

5. LeeC, LiX, HechmerA, EisenM, BigginMD, et al. (2008) NELF and GAGA factor are linked to promoter-proximal pausing at many genes in Drosophila. Mol Cell Biol 28: 3290–3300.

6. GilchristDA, Dos SantosG, FargoDC, XieB, GaoY, et al. (2010) Pausing of RNA polymerase II disrupts DNA-specified nucleosome organization to enable precise gene regulation. Cell 143: 540–551.

7. RahlPB, LinCY, SeilaAC, FlynnRA, McCuineS, et al. (2010) c-Myc regulates transcriptional pause release. Cell 141: 432–445.

8. NechaevS, FargoDC, dos SantosG, LiuL, GaoY, et al. (2010) Global analysis of short RNAs reveals widespread promoter-proximal stalling and arrest of Pol II in Drosophila. Science 327: 335–338.

9. MinIM, WaterfallJJ, CoreLJ, MunroeRJ, SchimentiJ, et al. (2011) Regulating RNA polymerase pausing and transcription elongation in embryonic stem cells. Genes Dev 25: 742–754.

10. AnamikaK, GyenisA, ToraL (2013) How to stop: the mysterious links among RNA polymerase II occupancy 3′ of genes, mRNA 3′ processing and termination. Transcription 4: 7–12.

11. AnamikaK, GyenisA, PoidevinL, PochO, ToraL (2012) RNA polymerase II pausing downstream of core histone genes is different from genes producing polyadenylated transcripts. PLoS One 7: e38769.

12. GrossoAR, de AlmeidaSF, BragaJ, Carmo-FonsecaM (2012) Dynamic transitions in RNA polymerase II density profiles during transcription termination. Genome Res 22: 1447–1456.

13. WelborenWJ, van DrielMA, Janssen-MegensEM, van HeeringenSJ, SweepFC, et al. (2009) ChIP-Seq of ERalpha and RNA polymerase II defines genes differentially responding to ligands. EMBO J 28: 1418–1428.

14. SvejstrupJQ (2007) Contending with transcriptional arrest during RNAPII transcript elongation. Trends Biochem Sci 32: 165–171.

15. RastogiRP, Richa, KumarA, TyagiMB, SinhaRP (2010) Molecular mechanisms of ultraviolet radiation-induced DNA damage and repair. J Nucleic Acids 2010: 592980.

16. SancarA, Lindsey-BoltzLA, Unsal-KacmazK, LinnS (2004) Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu Rev Biochem 73: 39–85.

17. Giglia-MariG, ZotterA, VermeulenW (2011) DNA damage response. Cold Spring Harb Perspect Biol 3: a000745.

18. HanawaltPC, SpivakG (2008) Transcription-coupled DNA repair: two decades of progress and surprises. Nat Rev Mol Cell Biol 9: 958–970.

19. SvejstrupJQ (2002) Mechanisms of transcription-coupled DNA repair. Nat Rev Mol Cell Biol 3: 21–29.

20. CompeE, EglyJM (2012) TFIIH: when transcription met DNA repair. Nat Rev Mol Cell Biol 13: 343–354.

21. LagerwerfS, VrouweMG, OvermeerRM, FousteriMI, MullendersLH (2011) DNA damage response and transcription. DNA Repair (Amst) 10: 743–750.

22. CostaRM, ChigancasV, Galhardo RdaS, CarvalhoH, MenckCF (2003) The eukaryotic nucleotide excision repair pathway. Biochimie 85: 1083–1099.

23. SelbyCP, DrapkinR, ReinbergD, SancarA (1997) RNA polymerase II stalled at a thymine dimer: footprint and effect on excision repair. Nucleic Acids Res 25: 787–793.

24. TornalettiS, HanawaltPC (1999) Effect of DNA lesions on transcription elongation. Biochimie 81: 139–146.

25. Livingstone-ZatchejM, MeierA, SuterB, ThomaF (1997) RNA polymerase II transcription inhibits DNA repair by photolyase in the transcribed strand of active yeast genes. Nucleic Acids Res 25: 3795–3800.

26. WilsonMD, HarremanM, SvejstrupJQ (2013) Ubiquitylation and degradation of elongating RNA polymerase II: The last resort. Biochim Biophys Acta 1829: 151–157.

27. LjungmanM, ZhangF (1996) Blockage of RNA polymerase as a possible trigger for UV light-induced apoptosis. Oncogene 13: 823–831.

28. DonahueBA, YinS, TaylorJS, ReinesD, HanawaltPC (1994) Transcript cleavage by RNA polymerase II arrested by a cyclobutane pyrimidine dimer in the DNA template. Proc Natl Acad Sci U S A 91: 8502–8506.

29. WalmacqC, CheungAC, KireevaML, LubkowskaL, YeC, et al. (2012) Mechanism of translesion transcription by RNA polymerase II and its role in cellular resistance to DNA damage. Mol Cell 46: 18–29.

30. TornalettiS, ReinesD, HanawaltPC (1999) Structural characterization of RNA polymerase II complexes arrested by a cyclobutane pyrimidine dimer in the transcribed strand of template DNA. J Biol Chem 274: 24124–24130.

31. KalogerakiVS, TornalettiS, CooperPK, HanawaltPC (2005) Comparative TFIIS-mediated transcript cleavage by mammalian RNA polymerase II arrested at a lesion in different transcription systems. DNA Repair (Amst) 4: 1075–1087.

32. Velez-CruzR, ZadorinAS, CoinF, EglyJM (2013) Sirt1 suppresses RNA synthesis after UV irradiation in combined xeroderma pigmentosum group D/Cockayne syndrome (XP-D/CS) cells. Proc Natl Acad Sci U S A 110: E212–220.

33. JensenA, MullendersLH (2010) Transcription factor IIS impacts UV-inhibited transcription. DNA Repair (Amst) 9: 1142–1150.

34. HahN, DankoCG, CoreL, WaterfallJJ, SiepelA, et al. (2011) A rapid, extensive, and transient transcriptional response to estrogen signaling in breast cancer cells. Cell 145: 622–634.

35. ZeiselA, KostlerWJ, MolotskiN, TsaiJM, KrauthgamerR, et al. (2011) Coupled pre-mRNA and mRNA dynamics unveil operational strategies underlying transcriptional responses to stimuli. Mol Syst Biol 7: 529.

36. SeilaAC, CoreLJ, LisJT, SharpPA (2009) Divergent transcription: a new feature of active promoters. Cell cycle 8: 2557–2564.

37. YeT, KrebsAR, ChoukrallahMA, KeimeC, PlewniakF, et al. (2011) seqMINER: an integrated ChIP-seq data interpretation platform. Nucleic Acids Res 39: e35.

38. KamieniarzK, IzzoA, DundrM, TropbergerP, OzreticL, et al. (2012) A dual role of linker histone H1.4 Lys 34 acetylation in transcriptional activation. Genes Dev 26: 797–802.

39. HuangD (2009) Systematic and integrative analysis of large gene lists using DAVID Bioinformatics Resources. Nat Protoc 4: 44–57.

40. TassyO, PourquieO (2013) Manteia, a predictive data mining system for vertebrate genes and its applications to human genetic diseases. Nucleic Acids Res 42 (D1) D882–D891.

41. HoogstratenD, BerginkS, NgJM, VerbiestVH, LuijsterburgMS, et al. (2008) Versatile DNA damage detection by the global genome nucleotide excision repair protein XPC. Journal of cell science 121: 2850–2859.

42. KanehisaM, GotoS, SatoY, FurumichiM, TanabeM (2012) KEGG for integration and interpretation of large-scale molecular data sets. Nucleic Acids Res 40: D109–114.

43. BaskaranR, DahmusME, WangJY (1993) Tyrosine phosphorylation of mammalian RNA polymerase II carboxyl-terminal domain. Proc Natl Acad Sci U S A 90: 11167–11171.

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

45. MunozMJ, Perez SantangeloMS, ParonettoMP, de la MataM, PelischF, et al. (2009) DNA damage regulates alternative splicing through inhibition of RNA polymerase II elongation. Cell 137: 708–720.

46. LuoZ, ZhengJ, LuY, BregmanDB (2001) Ultraviolet radiation alters the phosphorylation of RNA polymerase II large subunit and accelerates its proteasome-dependent degradation. Mutat Res 486: 259–274.

47. HeidemannM, HintermairC, VossK, EickD (2012) Dynamic phosphorylation patterns of RNA polymerase II CTD during transcription. Biochim Biophys Acta 1829 (1) 55–62.

48. LuH, ZawelL, FisherL, EglyJM, ReinbergD (1992) Human general transcription factor IIH phosphorylates the C-terminal domain of RNA polymerase II. Nature 358: 641–645.

49. Koch-PaizCA, AmundsonSA, BittnerML, MeltzerPS, FornaceAJJr (2004) Functional genomics of UV radiation responses in human cells. Mutat Res 549: 65–78.

50. KristensenU, EpanchintsevA, RauschendorfMA, LaugelV, StevnsnerT, et al. (2013) Regulatory interplay of Cockayne syndrome B ATPase and stress-response gene ATF3 following genotoxic stress. Proceedings of the National Academy of Sciences of the United States of America 110: E2261–2270.

51. MoneMJ, VolkerM, NikaidoO, MullendersLH, van ZeelandAA, et al. (2001) Local UV-induced DNA damage in cell nuclei results in local transcription inhibition. EMBO reports 2: 1013–1017.

52. SerozT, HwangJR, MoncollinV, EglyJM (1995) TFIIH: a link between transcription, DNA repair and cell cycle regulation. Curr Opin Genet Dev 5: 217–221.

53. HoogstratenD, NiggAL, HeathH, MullendersLH, van DrielR, et al. (2002) Rapid switching of TFIIH between RNA polymerase I and II transcription and DNA repair in vivo. Mol Cell 10: 1163–1174.

54. Giglia-MariG, TheilAF, MariPO, MourguesS, NonnekensJ, et al. (2009) Differentiation driven changes in the dynamic organization of Basal transcription initiation. PLoS Biol 7: e1000220.

55. CoinF, OksenychV, MocquetV, GrohS, BlattnerC, et al. (2008) Nucleotide excision repair driven by the dissociation of CAK from TFIIH. Molecular cell 31: 9–20.

56. LeeD, LisJT (1998) Transcriptional activation independent of TFIIH kinase and the RNA polymerase II mediator in vivo. Nature 393: 389–392.

57. ParvinJD, SharpPA (1993) DNA topology and a minimal set of basal factors for transcription by RNA polymerase II. Cell 73: 533–540.

58. ParvinJD, ShykindBM, MeyersRE, KimJ, SharpPA (1994) Multiple sets of basal factors initiate transcription by RNA polymerase II. J Biol Chem 269: 18414–18421.

59. UshevaA, ShenkT (1994) TATA-binding protein-independent initiation: YY1, TFIIB, and RNA polymerase II direct basal transcription on supercoiled template DNA. Cell 76: 1115–1121.

60. 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.

61. Proietti-De-SantisL, DraneP, EglyJM (2006) Cockayne syndrome B protein regulates the transcriptional program after UV irradiation. The EMBO journal 25: 1915–1923.

62. RockxDA, MasonR, van HoffenA, BartonMC, CitterioE, et al. (2000) UV-induced inhibition of transcription involves repression of transcription initiation and phosphorylation of RNA polymerase II. Proc Natl Acad Sci U S A 97: 10503–10508.

63. FousteriM, VermeulenW, van ZeelandAA, MullendersLH (2006) Cockayne syndrome A and B proteins differentially regulate recruitment of chromatin remodeling and repair factors to stalled RNA polymerase II in vivo. Mol Cell 23: 471–482.

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

65. LescureA, LutzY, EberhardD, JacqX, KrolA, et al. (1994) The N-terminal domain of the human TATA-binding protein plays a role in transcription from TATA-containing RNA polymerase II and III promoters. EMBO J 13: 1166–1175.

66. MarinoniJC, RoyR, VermeulenW, MiniouP, LutzY, et al. (1997) Cloning and characterization of p52, the fifth subunit of the core of the transcription/DNA repair factor TFIIH. EMBO J 16: 1093–1102.

67. MoncollinV, SchaefferL, ChalutC, EglyJM (1992) Expression in Escherichia coli: purification and properties of the recombinant human general transcription factor rTFIIB. Protein Expr Purif 3: 374–379.

68. BradsherJ, AuriolJ, Proietti de SantisL, IbenS, VoneschJL, et al. (2002) CSB is a component of RNA pol I transcription. Molecular cell 10: 819–829.

69. PruittKD, TatusovaT, KlimkeW, MaglottDR (2009) NCBI Reference Sequences: current status, policy and new initiatives. Nucleic Acids Res 37: D32–36.