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A Key Role for Chd1 in Histone H3 Dynamics at the 3′ Ends of Long Genes in Yeast


Chd proteins are ATP–dependent chromatin remodeling enzymes implicated in biological functions from transcriptional elongation to control of pluripotency. Previous studies of the Chd1 subclass of these proteins have implicated them in diverse roles in gene expression including functions during initiation, elongation, and termination. Furthermore, some evidence has suggested a role for Chd1 in replication-independent histone exchange or assembly. Here, we examine roles of Chd1 in replication-independent dynamics of histone H3 in both Drosophila and yeast. We find evidence of a role for Chd1 in H3 dynamics in both organisms. Using genome-wide ChIP-on-chip analysis, we find that Chd1 influences histone turnover at the 5′ and 3′ ends of genes, accelerating H3 replacement at the 5′ ends of genes while protecting the 3′ ends of genes from excessive H3 turnover. Although consistent with a direct role for Chd1 in exchange, these results may indicate that Chd1 stabilizes nucleosomes perturbed by transcription. Curiously, we observe a strong effect of gene length on Chd1's effects on H3 turnover. Finally, we show that Chd1 also affects histone modification patterns over genes, likely as a consequence of its effects on histone replacement. Taken together, our results emphasize a role for Chd1 in histone replacement in both budding yeast and Drosophila melanogaster, and surprisingly they show that the major effects of Chd1 on turnover occur at the 3′ ends of genes.


Vyšlo v časopise: A Key Role for Chd1 in Histone H3 Dynamics at the 3′ Ends of Long Genes in Yeast. PLoS Genet 8(7): e32767. doi:10.1371/journal.pgen.1002811
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002811

Souhrn

Chd proteins are ATP–dependent chromatin remodeling enzymes implicated in biological functions from transcriptional elongation to control of pluripotency. Previous studies of the Chd1 subclass of these proteins have implicated them in diverse roles in gene expression including functions during initiation, elongation, and termination. Furthermore, some evidence has suggested a role for Chd1 in replication-independent histone exchange or assembly. Here, we examine roles of Chd1 in replication-independent dynamics of histone H3 in both Drosophila and yeast. We find evidence of a role for Chd1 in H3 dynamics in both organisms. Using genome-wide ChIP-on-chip analysis, we find that Chd1 influences histone turnover at the 5′ and 3′ ends of genes, accelerating H3 replacement at the 5′ ends of genes while protecting the 3′ ends of genes from excessive H3 turnover. Although consistent with a direct role for Chd1 in exchange, these results may indicate that Chd1 stabilizes nucleosomes perturbed by transcription. Curiously, we observe a strong effect of gene length on Chd1's effects on H3 turnover. Finally, we show that Chd1 also affects histone modification patterns over genes, likely as a consequence of its effects on histone replacement. Taken together, our results emphasize a role for Chd1 in histone replacement in both budding yeast and Drosophila melanogaster, and surprisingly they show that the major effects of Chd1 on turnover occur at the 3′ ends of genes.


Zdroje

1. KornbergRDLorchY 1999 Twenty-five years of the nucleosome, fundamental particle of the eukaryote chromosome. Cell 98 285 294

2. Radman-LivajaMRandoOJ 2010 Nucleosome positioning: how is it established, and why does it matter? Dev Biol 339 258 266

3. KimuraHCookPR 2001 Kinetics of core histones in living human cells: little exchange of H3 and H4 and some rapid exchange of H2B. J Cell Biol 153 1341 1353

4. JacksonVChalkleyR 1985 Histone synthesis and deposition in the G1 and S phases of hepatoma tissue culture cells. Biochemistry 24 6921 6930

5. RufiangeAJacquesPEBhatWRobertFNouraniA 2007 Genome-wide replication-independent histone H3 exchange occurs predominantly at promoters and implicates H3 K56 acetylation and Asf1. Mol Cell 27 393 405

6. DionMFKaplanTKimMBuratowskiSFriedmanN 2007 Dynamics of replication-independent histone turnover in budding yeast. Science 315 1405 1408

7. IzbanMGLuseDS 1991 Transcription on nucleosomal templates by RNA polymerase II in vitro: inhibition of elongation with enhancement of sequence-specific pausing. Genes Dev 5 683 696

8. LiBCareyMWorkmanJL 2007 The role of chromatin during transcription. Cell 128 707 719

9. CheungVChuaGBatadaNNLandryCRMichnickSW 2008 Chromatin- and transcription-related factors repress transcription from within coding regions throughout the Saccharomyces cerevisiae genome. PLoS Biol 6 e277 10.1371/journal.pbio.0060277

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

11. HoLCrabtreeGR 2010 Chromatin remodelling during development. Nature 463 474 484

12. FlanaganJFMiLZChruszczMCymborowskiMClinesKL 2005 Double chromodomains cooperate to recognize the methylated histone H3 tail. Nature 438 1181 1185

13. SimsRJ3rdChenCFSantos-RosaHKouzaridesTPatelSS 2005 Human but not yeast CHD1 binds directly and selectively to histone H3 methylated at lysine 4 via its tandem chromodomains. J Biol Chem 280 41789 41792

14. MorettiniSTribusMZeilnerASebaldJCampo-FernandezB 2011 The chromodomains of CHD1 are critical for enzymatic activity but less important for chromatin localization. Nucleic Acids Res 39 3103 3115

15. HaukGMcKnightJNNodelmanIMBowmanGD 2010 The chromodomains of the Chd1 chromatin remodeler regulate DNA access to the ATPase motor. Mol Cell 39 711 723

16. StockdaleCFlausAFerreiraHOwen-HughesT 2006 Analysis of nucleosome repositioning by yeast ISWI and Chd1 chromatin remodeling complexes. J Biol Chem 281 16279 16288

17. LusserAUrwinDLKadonagaJT 2005 Distinct activities of CHD1 and ACF in ATP-dependent chromatin assembly. Nat Struct Mol Biol 12 160 166

18. TranHGStegerDJIyerVRJohnsonAD 2000 The chromo domain protein chd1p from budding yeast is an ATP-dependent chromatin-modifying factor. Embo J 19 2323 2331

19. WalfridssonJKhorosjutinaOMatikainenPGustafssonCMEkwallK 2007 A genome-wide role for CHD remodelling factors and Nap1 in nucleosome disassembly. Embo J 26 2868 2879

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

21. McDanielIELeeJMBergerMSHanagamiCKArmstrongJA 2008 Investigations of CHD1 function in transcription and development of Drosophila melanogaster. Genetics 178 583 587

22. SimicRLindstromDLTranHGRoinickKLCostaPJ 2003 Chromatin remodeling protein Chd1 interacts with transcription elongation factors and localizes to transcribed genes. Embo J 22 1846 1856

23. StokesDGTartofKDPerryRP 1996 CHD1 is concentrated in interbands and puffed regions of Drosophila polytene chromosomes. Proc Natl Acad Sci U S A 93 7137 7142

24. AlenCKentNAJonesHSO'SullivanJArandaA 2002 A role for chromatin remodeling in transcriptional termination by RNA polymerase II. Mol Cell 10 1441 1452

25. BiswasDDutta-BiswasRStillmanDJ 2007 Chd1 and yFACT act in opposition in regulating transcription. Mol Cell Biol 27 6279 6287

26. ChuYSuttonASternglanzRPrelichG 2006 The BUR1 cyclin-dependent protein kinase is required for the normal pattern of histone methylation by SET2. Mol Cell Biol 26 3029 3038

27. KeoghMCKurdistaniSKMorrisSAAhnSHPodolnyV 2005 Cotranscriptional set2 methylation of histone H3 lysine 36 recruits a repressive Rpd3 complex. Cell 123 593 605

28. QuanTKHartzogGA 2010 Histone H3K4 and K36 methylation, Chd1 and Rpd3S oppose the functions of Saccharomyces cerevisiae Spt4–Spt5 in transcription. Genetics 184 321 334

29. Pray-GrantMGDanielJASchieltzDYatesJR3rdGrantPA 2005 Chd1 chromodomain links histone H3 methylation with SAGA- and SLIK-dependent acetylation. Nature 433 434 438

30. KroganNJKimMAhnSHZhongGKoborMS 2002 RNA polymerase II elongation factors of Saccharomyces cerevisiae: a targeted proteomics approach. Mol Cell Biol 22 6979 6992

31. 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

32. 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

33. KhorosjutinaOWanrooijPHWalfridssonJSzilagyiZZhuX 2010 A chromatin-remodeling protein is a component of fission yeast mediator. J Biol Chem 285 29729 29737

34. KonevAYTribusMParkSYPodhraskiVLimCY 2007 CHD1 motor protein is required for deposition of histone variant H3.3 into chromatin in vivo. Science 317 1087 1090

35. LinJJLehmannLWBonoraGSridharanRVashishtAA 2011 Mediator coordinates PIC assembly with recruitment of CHD1. Genes Dev 25 2198 2209

36. EhrensbergerAHKornbergRD 2011 Isolation of an activator-dependent, promoter-specific chromatin remodeling factor. Proc Natl Acad Sci U S A 108 10115 10120

37. LoppinBBonnefoyEAnselmeCLaurenconAKarrTL 2005 The histone H3.3 chaperone HIRA is essential for chromatin assembly in the male pronucleus. Nature 437 1386 1390

38. OrsiGACoublePLoppinB 2009 Epigenetic and replacement roles of histone variant H3.3 in reproduction and development. Int J Dev Biol 53 231 243

39. YuanGCLiuYJDionMFSlackMDWuLF 2005 Genome-scale identification of nucleosome positions in S. cerevisiae. Science 309 626 630

40. GkikopoulosTSchofieldPSinghVPinskayaMMellorJ 2011 A role for Snf2-related nucleosome-spacing enzymes in genome-wide nucleosome organization. Science 333 1758 1760

41. XellaBGodingCAgricolaEDi MauroECasertaM 2006 The ISWI and CHD1 chromatin remodelling activities influence ADH2 expression and chromatin organization. Mol Microbiol 59 1531 1541

42. WoodageTBasraiMABaxevanisADHieterPCollinsFS 1997 Characterization of the CHD family of proteins. Proc Natl Acad Sci U S A 94 11472 11477

43. TsukiyamaTPalmerJLandelCCShiloachJWuC 1999 Characterization of the imitation switch subfamily of ATP-dependent chromatin-remodeling factors in Saccharomyces cerevisiae. Genes Dev 13 686 697

44. AhmadKHenikoffS 2002 The histone variant H3.3 marks active chromatin by replication-independent nucleosome assembly. Mol Cell 9 1191 1200

45. LingXHarknessTASchultzMCFisher-AdamsGGrunsteinM 1996 Yeast histone H3 and H4 amino termini are important for nucleosome assembly in vivo and in vitro: redundant and position-independent functions in assembly but not in gene regulation. Genes Dev 10 686 699

46. Ejlassi-LassalletteAMocquardEArnaudMCThirietC 2011 H4 replication-dependent diacetylation and Hat1 promote S-phase chromatin assembly in vivo. Mol Biol Cell 22 245 255

47. ElsaesserSJGoldbergADAllisCD 2010 New functions for an old variant: no substitute for histone H3.3. Curr Opin Genet Dev 20 110 117

48. JamaiAImoberdorfRMStrubinM 2007 Continuous histone H2B and transcription-dependent histone H3 exchange in yeast cells outside of replication. Mol Cell 25 345 355

49. Lopes da RosaJHolikJGreenEMRandoOJKaufmanPD 2011 Overlapping regulation of CenH3 localization and histone H3 turnover by CAF-1 and HIR proteins in Saccharomyces cerevisiae. Genetics 187 9 19

50. KaplanTLiuCLErkmannJAHolikJGrunsteinM 2008 Cell cycle- and chaperone-mediated regulation of H3K56ac incorporation in yeast. PLoS Genet 4 e1000270 doi:10.1371/journal.pgen.1000270

51. Radman-LivajaMVerzijlbergenKFWeinerAvan WelsemTFriedmanN 2011 Patterns and mechanisms of ancestral histone protein inheritance in budding yeast. PLoS Biol 9 e1001075 doi:10.1371/journal.pbio.1001075

52. VerzijlbergenKFMenendez-BenitoVvan WelsemTvan DeventerSJLindstromDL 2010 Recombination-induced tag exchange to track old and new proteins. Proc Natl Acad Sci U S A 107 64 68

53. VerzijlbergenKFvan WelsemTSieDLenstraTLTurnerDJ 2011 A barcode screen for epigenetic regulators reveals a role for the NuB4/HAT-B histone acetyltransferase complex in histone turnover. PLoS Genet 7 e1002284 doi:10.1371/journal.pgen.1002284

54. LiuCLKaplanTKimMBuratowskiSSchreiberSL 2005 Single-nucleosome mapping of histone modifications in S. cerevisiae. PLoS Biol 3 e328 doi:10.1371/journal.pbio.0030328

55. PokholokDKHarbisonCTLevineSColeMHannettNM 2005 Genome-wide map of nucleosome acetylation and methylation in yeast. Cell 122 517 527

56. ZhangLSchroederSFongNBentleyDL 2005 Altered nucleosome occupancy and histone H3K4 methylation in response to ‘transcriptional stress’. Embo J 24 2379 2390

57. BiswasDTakahataSXinHDutta-BiswasRYuY 2008 A role for Chd1 and Set2 in negatively regulating DNA replication in Saccharomyces cerevisiae. Genetics 178 649 659

58. DrouinSLarameeLJacquesPEForestABergeronM 2010 DSIF and RNA polymerase II CTD phosphorylation coordinate the recruitment of Rpd3S to actively transcribed genes. PLoS Genet 6 e1001173 doi:10.1371/journal.pgen.1001173

59. CarrozzaMJLiBFlorensLSuganumaTSwansonSK 2005 Histone H3 methylation by Set2 directs deacetylation of coding regions by Rpd3S to suppress spurious intragenic transcription. Cell 123 581 592

60. EngeholmMde JagerMFlausABrenkRvan NoortJ 2009 Nucleosomes can invade DNA territories occupied by their neighbors. Nat Struct Mol Biol 16 151 158

61. SchwartzBEAhmadK 2005 Transcriptional activation triggers deposition and removal of the histone variant H3.3. Genes Dev 19 804 814

62. SiriacoGDeuringRChiodaMBeckerPBTamkunJW 2009 Drosophila ISWI regulates the association of histone H1 with interphase chromosomes in vivo. Genetics 182 661 669

63. SchwartzBEWernerJKLisJT 2004 Indirect immunofluorescent labeling of Drosophila polytene chromosomes: visualizing protein interactions with chromatin in vivo. Methods Enzymol 376 393 404

64. WinstonFDollardCRicupero-HovasseSL 1995 Construction of a set of convenient Saccharomyces cerevisiae strains that are isogenic to S288C. Yeast 11 53 55

65. RoseMDWinstonFHieterP 1990 Methods in Yeast Genetics: a laboratory course manual Cold Spring Harbor, New York Cold Spring Harbor Laboratory Press

66. ValenzuelaLDhillonNKamakakaRT 2009 Transcription independent insulation at TFIIIC-dependent insulators. Genetics 183 131 148

67. LittMDSimpsonMRecillas-TargaFPrioleauMNFelsenfeldG 2001 Transitions in histone acetylation reveal boundaries of three separately regulated neighboring loci. Embo J 20 2224 2235

68. LiebJDLiuXBotsteinDBrownPO 2001 Promoter-specific binding of Rap1 revealed by genome-wide maps of protein-DNA association. Nat Genet 28 327 334

69. LiuCLSchreiberSLBernsteinBE 2003 Development and validation of a T7 based linear amplification for genomic DNA. BMC Genomics 4 19

70. DietzlGChenDSchnorrerFSuKCBarinovaY 2007 A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 448 151 156

71. KimTSLiuCLYassourMHolikJFriedmanN 2010 RNA polymerase mapping during stress responses reveals widespread nonproductive transcription in yeast. Genome Biol 11 R75

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