Stress-Induced PARP Activation Mediates Recruitment of Mi-2 to Promote Heat Shock Gene Expression

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Eukaryotic cells respond to genomic and environmental stresses, such as DNA damage and heat shock (HS), with the synthesis of poly-[ADP-ribose] (PAR) at specific chromatin regions, such as DNA breaks or HS genes, by PAR polymerases (PARP). Little is known about the role of this modification during cellular stress responses. We show here that the nucleosome remodeler dMi-2 is recruited to active HS genes in a PARP–dependent manner. dMi-2 binds PAR suggesting that this physical interaction is important for recruitment. Indeed, a dMi-2 mutant unable to bind PAR does not localise to active HS loci in vivo. We have identified several dMi-2 regions which bind PAR independently in vitro, including the chromodomains and regions near the N-terminus containing motifs rich in K and R residues. Moreover, upon HS gene activation, dMi-2 associates with nascent HS gene transcripts, and its catalytic activity is required for efficient transcription and co-transcriptional RNA processing. RNA and PAR compete for dMi-2 binding in vitro, suggesting a two step process for dMi-2 association with active HS genes: initial recruitment to the locus via PAR interaction, followed by binding to nascent RNA transcripts. We suggest that stress-induced chromatin PARylation serves to rapidly attract factors that are required for an efficient and timely transcriptional response.

Vyšlo v časopise: Stress-Induced PARP Activation Mediates Recruitment of Mi-2 to Promote Heat Shock Gene Expression. PLoS Genet 7(7): e32767. doi:10.1371/journal.pgen.1002206
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002206

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Zdroje

1. PeteschSJLisJT 2008 Rapid, transcription-independent loss of nucleosomes over a large chromatin domain at Hsp70 loci. Cell 134 74 84

2. WinegardenNAWongKSSoptaMWestwoodJT 1996 Sodium salicylate decreases intracellular ATP, induces both heat shock factor binding and chromosomal puffing, but does not induce hsp 70 gene transcription in Drosophila. J Biol Chem 271 26971 26980

3. TulinASpradlingA 2003 Chromatin loosening by poly(ADP)-ribose polymerase (PARP) at Drosophila puff loci. Science 299 560 562

4. ZobeckKLBuckleyMSZipfelWRLisJT 2010 Recruitment Timing and Dynamics of Transcription Factors at the Hsp70 Loci in Living Cells. Molecular Cell 40 965 975

5. KrishnakumarRKrausWL 2010 The PARP side of the nucleus: molecular actions, physiological outcomes, and clinical targets. Mol Cell 39 8 24

6. TillSLadurnerAG 2009 Sensing NAD metabolites through macro domains. Front Biosci 14 3246 3258

7. TiminszkyGTillSHassaPOHothornMKustatscherG 2009 A macrodomain-containing histone rearranges chromatin upon sensing PARP1 activation. Nat Struct Mol Biol 16 923 929

8. AhelDHorejsiZWiechensNPoloSEGarcia-WilsonE 2009 Poly(ADP-ribose)-dependent regulation of DNA repair by the chromatin remodeling enzyme ALC1. Science 325 1240 1243

9. GottschalkAJTiminszkyGKongSEJinJCaiY 2009 Poly(ADP-ribosyl)ation directs recruitment and activation of an ATP-dependent chromatin remodeler. Proc Natl Acad Sci U S A 106 13770 13774

10. PoloSEKaidiABaskcombLGalantyYJacksonSP 2010 Regulation of DNA-damage responses and cell-cycle progression by the chromatin remodelling factor CHD4. Embo J 29 3130 3139

11. FujitaNJayeDLGeigermanCAkyildizAMooneyMR 2004 MTA3 and the Mi-2/NuRD complex regulate cell fate during B lymphocyte differentiation. Cell 119 75 86

12. MurawskyCMBrehmABadenhorstPLoweNBeckerPB 2001 Tramtrack69 interacts with the dMi-2 subunit of the Drosophila NuRD chromatin remodelling complex. EMBO Rep 2 1089 1094

13. MarfellaCGImbalzanoAN 2007 The Chd family of chromatin remodelers. Mutat Res 618 30 40

14. KunertNWagnerEMurawskaMKlinkerHKremmerE 2009 dMec: a novel Mi-2 chromatin remodelling complex involved in transcriptional repression. Embo J 28 533 544

15. FengQZhangY 2001 The MeCP1 complex represses transcription through preferential binding, remodeling, and deacetylating methylated nucleosomes. Genes Dev 15 827 832

16. Le GuezennecXVermeulenMBrinkmanABHoeijmakersWACohenA 2006 MBD2/NuRD and MBD3/NuRD, two distinct complexes with different biochemical and functional properties. Mol Cell Biol 26 843 851

17. LykoFBeiselCMarholdJParoR 2006 Epigenetic regulation in Drosophila. Curr Top Microbiol Immunol 310 23 44

18. KehleJBeuchleDTreuheitSChristenBKennisonJA 1998 dMi-2, a hunchback-interacting protein that functions in polycomb repression. Science 282 1897 1900

19. KimJSifSJonesBJacksonAKoipallyJ 1999 Ikaros DNA-binding proteins direct formation of chromatin remodeling complexes in lymphocytes. Immunity 10 345 355

20. KoipallyJRenoldAKimJGeorgopoulosK 1999 Repression by Ikaros and Aiolos is mediated through histone deacetylase complexes. Embo J 18 3090 3100

21. ReddyBABajpePKBassettAMoshkinYMKozhevnikovaE 2010 Drosophila transcription factor Tramtrack69 binds MEP1 to recruit the chromatin remodeler NuRD. Mol Cell Biol 30 5234 5244

22. StielowBSapetschnigAKrugerIKunertNBrehmA 2008 Identification of SUMO-dependent chromatin-associated transcriptional repression components by a genome-wide RNAi screen. Mol Cell 29 742 754

23. MurawskaMKunertNvan VugtJLangstGKremmerE 2008 dCHD3, a novel ATP-dependent chromatin remodeler associated with sites of active transcription. Mol Cell Biol 28 2745 2757

24. GagneJPHunterJMLabrecqueBChabotBPoirierGG 2003 A proteomic approach to the identification of heterogeneous nuclear ribonucleoproteins as a new family of poly(ADP-ribose)-binding proteins. Biochem J 371 331 340

25. PleschkeJMKleczkowskaHEStrohmMAlthausFR 2000 Poly(ADP-ribose) binds to specific domains in DNA damage checkpoint proteins. J Biol Chem 275 40974 40980

26. ZhangYLiuSMickaninCFengYCharlatO RNF146 is a poly(ADP-ribose)-directed E3 ligase that regulates axin degradation and Wnt signalling. Nat Cell Biol 13 623 629

27. ArmstrongJAPapoulasODaubresseGSperlingASLisJT 2002 The Drosophila BRM complex facilitates global transcription by RNA polymerase II. Embo J 21 5245 5254

28. BadenhorstPXiaoHCherbasLKwonSYVoasM 2005 The Drosophila nucleosome remodeling factor NURF is required for Ecdysteroid signaling and metamorphosis. Genes Dev 19 2540 2545

29. DeuringRFantiLArmstrongJASarteMPapoulasO 2000 The ISWI chromatin-remodeling protein is required for gene expression and the maintenance of higher order chromatin structure in vivo. Mol Cell 5 355 365

30. KelleyDEStokesDGPerryRP 1999 CHD1 interacts with SSRP1 and depends on both its chromodomain and its ATPase/helicase-like domain for proper association with chromatin. Chromosoma 108 10 25

31. ArdehaliMBYaoJAdelmanKFudaNJPeteschSJ 2009 Spt6 enhances the elongation rate of RNA polymerase II in vivo. Embo J 28 1067 1077

32. SaundersAWernerJAndrulisEDNakayamaTHiroseS 2003 Tracking FACT and the RNA polymerase II elongation complex through chromatin in vivo. Science 301 1094 1096

33. BatscheEYanivMMuchardtC 2006 The human SWI/SNF subunit Brm is a regulator of alternative splicing. Nat Struct Mol Biol 13 22 29

34. SimsRJ3rdMillhouseSChenCFLewisBAErdjument-BromageH 2007 Recognition of trimethylated histone H3 lysine 4 facilitates the recruitment of transcription postinitiation factors and pre-mRNA splicing. Mol Cell 28 665 676

35. SrinivasanSArmstrongJADeuringRDahlsveenIKMcNeillH 2005 The Drosophila trithorax group protein Kismet facilitates an early step in transcriptional elongation by RNA Polymerase II. Development 132 1623 1635

36. TyagiARymeJBrodinDOstlund FarrantsAKVisaN 2009 SWI/SNF associates with nascent pre-mRNPs and regulates alternative pre-mRNA processing. PLoS Genet 5 e1000470 doi:10.1371/journal.pgen.1000470

37. AhelIAhelDMatsusakaTClarkAJPinesJ 2008 Poly(ADP-ribose)-binding zinc finger motifs in DNA repair/checkpoint proteins. Nature 451 81 85

38. BouazouneKMitterwegerALangstGImhofAAkhtarA 2002 The dMi-2 chromodomains are DNA binding modules important for ATP-dependent nucleosome mobilization. Embo J 21 2430 2440

39. ChouDMAdamsonBDephoureNETanXNottkeAC 2010 A chromatin localization screen reveals poly (ADP ribose)-regulated recruitment of the repressive polycomb and NuRD complexes to sites of DNA damage. Proc Natl Acad Sci U S A 107 18475 18480

40. LarsenDHPoinsignonCGudjonssonTDinantCPayneMR 2010 The chromatin-remodeling factor CHD4 coordinates signaling and repair after DNA damage. J Cell Biol 190 731 740

41. SmeenkGWiegantWWVrolijkHSolariAPPastinkA 2010 The NuRD chromatin-remodeling complex regulates signaling and repair of DNA damage. J Cell Biol 190 741 749

42. BoehmAKSaundersAWernerJLisJT 2003 Transcription factor and polymerase recruitment, modification, and movement on dhsp70 in vivo in the minutes following heat shock. Mol Cell Biol 23 7628 7637

43. KustatscherGHothornMPugieuxCScheffzekKLadurnerAG 2005 Splicing regulates NAD metabolite binding to histone macroH2A. Nat Struct Mol Biol 12 624 625

44. GilbertCSvejstrupJQ 2006 RNA immunoprecipitation for determining RNA-protein associations in vivo. Curr Protoc Mol Biol Chapter 27 Unit 27 24

45. KarrasGIKustatscherGBuhechaHRAllenMDPugieuxC 2005 The macro domain is an ADP-ribose binding module. Embo J 24 1911 1920