#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

A Barcode Screen for Epigenetic Regulators Reveals a Role for the NuB4/HAT-B Histone Acetyltransferase Complex in Histone Turnover


Dynamic modification of histone proteins plays a key role in regulating gene expression. However, histones themselves can also be dynamic, which potentially affects the stability of histone modifications. To determine the molecular mechanisms of histone turnover, we developed a parallel screening method for epigenetic regulators by analyzing chromatin states on DNA barcodes. Histone turnover was quantified by employing a genetic pulse-chase technique called RITE, which was combined with chromatin immunoprecipitation and high-throughput sequencing. In this screen, the NuB4/HAT-B complex, containing the conserved type B histone acetyltransferase Hat1, was found to promote histone turnover. Unexpectedly, the three members of this complex could be functionally separated from each other as well as from the known interacting factor and histone chaperone Asf1. Thus, systematic and direct interrogation of chromatin structure on DNA barcodes can lead to the discovery of genes and pathways involved in chromatin modification and dynamics.


Vyšlo v časopise: A Barcode Screen for Epigenetic Regulators Reveals a Role for the NuB4/HAT-B Histone Acetyltransferase Complex in Histone Turnover. PLoS Genet 7(10): e32767. doi:10.1371/journal.pgen.1002284
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002284

Souhrn

Dynamic modification of histone proteins plays a key role in regulating gene expression. However, histones themselves can also be dynamic, which potentially affects the stability of histone modifications. To determine the molecular mechanisms of histone turnover, we developed a parallel screening method for epigenetic regulators by analyzing chromatin states on DNA barcodes. Histone turnover was quantified by employing a genetic pulse-chase technique called RITE, which was combined with chromatin immunoprecipitation and high-throughput sequencing. In this screen, the NuB4/HAT-B complex, containing the conserved type B histone acetyltransferase Hat1, was found to promote histone turnover. Unexpectedly, the three members of this complex could be functionally separated from each other as well as from the known interacting factor and histone chaperone Asf1. Thus, systematic and direct interrogation of chromatin structure on DNA barcodes can lead to the discovery of genes and pathways involved in chromatin modification and dynamics.


Zdroje

1. RandoOJAhmadK 2007 Rules and regulation in the primary structure of chromatin. Curr Opin Cell Biol 19 250 256

2. BonasioRTuSReinbergD 2010 Molecular signals of epigenetic states. Science 330 612 616

3. HenikoffS 2008 Nucleosome destabilization in the epigenetic regulation of gene expression. Nat Rev Genet 9 15 26

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

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

6. 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

7. 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

8. KimHJSeolJHHanJWYounHDChoEJ 2007 Histone chaperones regulate histone exchange during transcription. EMBO J 26 4467 4474

9. DealRBHenikoffJGHenikoffS 2010 Genome-wide kinetics of nucleosome turnover determined by metabolic labeling of histones. Science 328 1161 1164

10. ParkYJLugerK 2008 Histone chaperones in nucleosome eviction and histone exchange. Curr Opin Struct Biol 18 282 289

11. DasCTylerJKChurchillME 2010 The histone shuffle: histone chaperones in an energetic dance. Trends Biochem Sci 35 476 489

12. De KoningLCorpetAHaberJEAlmouzniG 2007 Histone chaperones: an escort network regulating histone traffic. Nat Struct Mol Biol 14 997 1007

13. ParthunMRWidomJGottschlingDE 1996 The major cytoplasmic histone acetyltransferase in yeast: links to chromatin replication and histone metabolism. Cell 87 85 94

14. ParthunMR 2007 Hat1: the emerging cellular roles of a type B histone acetyltransferase. Oncogene 26 5319 5328

15. BensonLJPhillipsJAGuYParthunMRHoffmanCS 2007 Properties of the type B histone acetyltransferase Hat1: H4 tail interaction, site preference, and involvement in DNA repair. J Biol Chem 282 836 842

16. ChangLLorangerSSMizzenCErnstSGAllisCD 1997 Histones in transit: cytosolic histone complexes and diacetylation of H4 during nucleosome assembly in human cells. Biochemistry 36 469 480

17. PovedaASendraR 2008 Site specificity of yeast histone acetyltransferase B complex in vivo. FEBS J 275 2122 2136

18. GeZWangHParthunMR 2011 Nuclear Hat1p Complex (NuB4) Components Participate in DNA Repair-linked Chromatin Reassembly. J Biol Chem 286 16790 16799

19. MersfelderELParthunMR 2008 Involvement of Hat1p (Kat1p) catalytic activity and subcellular localization in telomeric silencing. J Biol Chem 283 29060 29068

20. SuterBPogoutseOGuoXKroganNLewisP 2007 Association with the origin recognition complex suggests a novel role for histone acetyltransferase Hat1p/Hat2p. BMC Biol 5 38

21. QinSParthunMR 2006 Recruitment of the type B histone acetyltransferase Hat1p to chromatin is linked to DNA double-strand breaks. Mol Cell Biol 26 3649 3658

22. RosalenyLEAntunezORuiz-GarciaABPerez-OrtinJETorderaV 2005 Yeast HAT1 and HAT2 deletions have different life-span and transcriptome phenotypes. FEBS Lett 579 4063 4068

23. QinSParthunMR 2002 Histone H3 and the histone acetyltransferase Hat1p contribute to DNA double-strand break repair. Mol Cell Biol 22 8353 8365

24. KellyTJQinSGottschlingDEParthunMR 2000 Type B histone acetyltransferase Hat1p participates in telomeric silencing. Mol Cell Biol 20 7051 7058

25. FillinghamJRechtJSilvaACSuterBEmiliA 2008 Chaperone control of the activity and specificity of the histone H3 acetyltransferase Rtt109. Mol Cell Biol 28 4342 4353

26. CamposEIFillinghamJLiGZhengHVoigtP 2010 The program for processing newly synthesized histones H3.1 and H4. Nat Struct Mol Biol 17 1343 1351

27. FillinghamJKainthPLambertJPvan BakelHTsuiK 2009 Two-color cell array screen reveals interdependent roles for histone chaperones and a chromatin boundary regulator in histone gene repression. Mol Cell 35 340 351

28. SuttonABucariaJOsleyMASternglanzR 2001 Yeast ASF1 protein is required for cell cycle regulation of histone gene transcription 9. Genetics 158 587 596

29. LambertJPFillinghamJSiahbaziMGreenblattJBaetzK 2010 Defining the budding yeast chromatin-associated interactome. Mol Syst Biol 6 448

30. LiQZhouHWurteleHDaviesBHorazdovskyB 2008 Acetylation of histone H3 lysine 56 regulates replication-coupled nucleosome assembly. Cell 134 244 255

31. SharpJAFoutsETKrawitzDCKaufmanPD 2001 Yeast histone deposition protein Asf1p requires Hir proteins and PCNA for heterochromatic silencing 5. Curr Biol 11 463 473

32. GreenEMAntczakAJBaileyAOFrancoAAWuKJ 2005 Replication-Independent Histone Deposition by the HIR Complex and Asf1. Curr Biol 15 2044 2049

33. AndrewsAJChenXZevinAStargellLALugerK 2010 The histone chaperone Nap1 promotes nucleosome assembly by eliminating nonnucleosomal histone DNA interactions. Mol Cell 37 834 842

34. BurgessRJZhouHHanJZhangZ 2010 A role for Gcn5 in replication-coupled nucleosome assembly. Mol Cell 37 469 480

35. LukERanjanAFitzgeraldPCMizuguchiGHuangY 2010 Stepwise histone replacement by SWR1 requires dual activation with histone H2A.Z and canonical nucleosome. Cell 143 725 736

36. Papamichos-ChronakisMWatanabeSRandoOJPetersonCL 2011 Global regulation of H2A.Z localization by the INO80 chromatin-remodeling enzyme is essential for genome integrity 1. Cell 144 200 213

37. LingerJTylerJK 2006 Global replication-independent histone H4 exchange in budding yeast. Eukaryot Cell 5 1780 1787

38. KroganNJDoverJWoodASchneiderJHeidtJ 2003 The Paf1 complex is required for histone H3 methylation by COMPASS and Dot1p: linking transcriptional elongation to histone methylation. Mol Cell 11 721 729

39. SmithAMHeislerLESt OngeRPFarias-HessonEWallaceIM 2010 Highly-multiplexed barcode sequencing: an efficient method for parallel analysis of pooled samples. Nucleic Acids Res 38 e142

40. SmithAMHeislerLEMellorJKaperFThompsonMJ 2009 Quantitative phenotyping via deep barcode sequencing. Genome Res 19 1836 1842

41. PierceSEDavisRWNislowCGiaeverG 2007 Genome-wide analysis of barcoded Saccharomyces cerevisiae gene-deletion mutants in pooled cultures. Nat Protoc 2 2958 2974

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

43. DealRBHenikoffS 2010 Capturing the dynamic epigenome. Genome Biol 11 218

44. TongAHBooneC 2006 Synthetic genetic array analysis in Saccharomyces cerevisiae. Methods Mol Biol 313 171 192

45. VerreaultAKaufmanPDKobayashiRStillmanB 1996 Nucleosome assembly by a complex of CAF-1 and acetylated histones H3/H4. Cell 87 95 104

46. BensonLJGuYYakovlevaTTongKBarrowsC 2006 Modifications of H3 and H4 during Chromatin Replication, Nucleosome Assembly, and Histone Exchange. J Biol Chem 281 9287 9296

47. SobelRECookRGPerryCAAnnunziatoATAllisCD 1995 Conservation of deposition-related acetylation sites in newly synthesized histones H3 and H4. Proc Natl Acad Sci U S A 92 1237 1241

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

49. AiXParthunMR 2004 The nuclear Hat1p/Hat2p complex: a molecular link between type B histone acetyltransferases and chromatin assembly. Mol Cell 14 195 205

50. BlackwellJSJrWilkinsonSTMosammaparastNPembertonLF 2007 Mutational analysis of H3 and H4 N termini reveals distinct roles in nuclear import. J Biol Chem 282 20142 20150

51. GlowczewskiLWaterborgJHBermanJG 2004 Yeast chromatin assembly complex 1 protein excludes nonacetylatable forms of histone H4 from chromatin and the nucleus. Mol Cell Biol 24 10180 10192

52. DionMFAltschulerSJWuLFRandoOJ 2005 Genomic characterization reveals a simple histone H4 acetylation code. Proc Natl Acad Sci U S A 102 5501 5506

53. MaXJWuJAltheimBASchultzMCGrunsteinM 1998 Deposition-related sites K5/K12 in histone H4 are not required for nucleosome deposition in yeast. Proc Natl Acad Sci U S A 95 6693 6698

54. 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

55. PovedaAPamblancoMTafrovSTorderaVSternglanzR 2004 Hif1 is a component of yeast histone acetyltransferase B, a complex mainly localized in the nucleus. J Biol Chem 279 16033 16043

56. DunleavyEMPidouxALMonetMBonillaCRichardsonW 2007 A NASP (N1/N2)-related protein, Sim3, binds CENP-A and is required for its deposition at fission yeast centromeres. Mol Cell 28 1029 1044

57. LenstraTLBenschopJJKimTSchulzeJMBrabersNA 2011 The specificity and topology of chromatin interaction pathways in yeast. Mol Cell 42 536 549

58. van WageningenSKemmerenPLijnzaadPMargaritisTBenschopJJ 2010 Functional overlap and regulatory links shape genetic interactions between signaling pathways. Cell 143 991 1004

59. FeserJTruongDDasCCarsonJJKieftJ 2010 Elevated histone expression promotes life span extension. Mol Cell 39 724 735

60. MosammaparastNGuoYShabanowitzJHuntDFPembertonLF 2002 Pathways mediating the nuclear import of histones H3 and H4 in yeast. J Biol Chem 277 862 868

61. SharpJARizkiGKaufmanPD 2005 Regulation of histone deposition proteins Asf1/Hir1 by multiple DNA damage checkpoint kinases in Saccharomyces cerevisiae. Genetics 171 885 899

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

63. Katan-KhaykovichYStruhlK 2011 Splitting of H3-H4 tetramers at transcriptionally active genes undergoing dynamic histone exchange. Proc Natl Acad Sci U S A 108 1296 1301

64. GradolattoARogersRSLavenderHTavernaSDAllisCD 2008 Saccharomyces cerevisiae Yta7 regulates histone gene expression. Genetics 179 291 304

65. GauthierNPJensenLJWernerssonRBrunakSJensenTS 2010 Cyclebase.org: version 2.0, an updated comprehensive, multi-species repository of cell cycle experiments and derived analysis results. Nucleic Acids Res 38 D699 D702

66. KleffSAndrulisEDAndersonCWSternglanzR 1995 Identification of a gene encoding a yeast histone H4 acetyltransferase. J Biol Chem 270 24674 24677

67. YeJAiXEugeniEEZhangLCarpenterLR 2005 Histone H4 lysine 91 acetylation a core domain modification associated with chromatin assembly. Mol Cell 18 123 130

68. JasencakovaZScharfANAskKCorpetAImhofA 2010 Replication stress interferes with histone recycling and predeposition marking of new histones. Mol Cell 37 736 743

69. van LeeuwenFGafkenPRGottschlingDE 2002 Dot1p modulates silencing in yeast by methylation of the nucleosome core. Cell 109 745 756

70. SawadaKYangZHortonJRCollinsREZhangX 2004 Structure of the conserved core of the yeast Dot1p, a nucleosomal histone H3 lysine 79 methyltransferase 2. J Biol Chem 279 43296 43306

71. AdkinsMWCarsonJJEnglishCMRameyCJTylerJK 2007 The histone chaperone anti-silencing function 1 stimulates the acetylation of newly synthesized histone H3 in S-phase. J Biol Chem 282 1334 1340

72. De VosDFrederiksFTewijMvan WelsemTVerzijlbergenKF 2011 Progressive methylation of aging histones by Dot1 acts as a timer. EMBO Rep in press

73. ClaytonALHazzalinCAMahadevanLC 2006 Enhanced histone acetylation and transcription: a dynamic perspective. Mol Cell 23 289 296

74. PedruzziIBurckertNEggerPDe VirgilioC 2000 Saccharomyces cerevisiae Ras/cAMP pathway controls post-diauxic shift element-dependent transcription through the zinc finger protein Gis1. EMBO J 19 2569 2579

75. TuSBullochEMYangLRenCHuangWC 2007 Identification of histone demethylases in Saccharomyces cerevisiae. J Biol Chem 282 14262 14271

76. TronnersjoSHanefalkCBalciunasDHuGZNordbergN 2007 The jmjN and jmjC domains of the yeast zinc finger protein Gis1 interact with 19 proteins involved in transcription, sumoylation and DNA repair. Mol Genet Genomics 277 57 70

77. KlopfEPaskovaLSoleCMasGPetryshynA 2009 Cooperation between the INO80 complex and histone chaperones determines adaptation of stress gene transcription in the yeast Saccharomyces cerevisiae. Mol Cell Biol 29 4994 5007

78. HannumGSrivasRGuenoleAvan AttikumHKroganNJ 2009 Genome-wide association data reveal a global map of genetic interactions among protein complexes. PLoS Genet 5 e1000782 doi:10.1371/journal.pgen.1000782

79. Ben AroyaSCoombesCKwokTO'DonnellKABoekeJD 2008 Toward a comprehensive temperature-sensitive mutant repository of the essential genes of Saccharomyces cerevisiae. Mol Cell 30 248 258

80. DaiJHylandEMYuanDSHuangHBaderJS 2008 Probing nucleosome function: a highly versatile library of synthetic histone H3 and H4 mutants. Cell 134 1066 1078

81. HoCHMagtanongLBarkerSLGreshamDNishimuraS 2009 A molecular barcoded yeast ORF library enables mode-of-action analysis of bioactive compounds. Nat Biotechnol 27 369 377

82. YanZCostanzoMHeislerLEPawJKaperF 2008 Yeast Barcoders: a chemogenomic application of a universal donor-strain collection carrying bar-code identifiers 36. Nat Methods 5 719 725

83. EasonRGPourmandNTongprasitWHermanZSAnthonyK 2004 Characterization of synthetic DNA bar codes in Saccharomyces cerevisiae gene-deletion strains. Proc Natl Acad Sci U S A 101 11046 11051

84. van BakelHHolstegeFC 2004 In control: systematic assessment of microarray performance. EMBO Rep 5 964 969

85. MargaritisTLijnzaadPvan LeenenDBouwmeesterDKemmerenP 2009 Adaptable gene-specific dye bias correction for two-channel DNA microarrays. Mol Syst Biol 5 266

86. RadonjicMAndrauJCLijnzaadPKemmerenPKockelkornTT 2005 Genome-wide analyses reveal RNA polymerase II located upstream of genes poised for rapid response upon S. cerevisiae stationary phase exit. Mol Cell 18 171 183

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2011 Číslo 10
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Aktuální možnosti diagnostiky a léčby litiáz
nový kurz
Autori: MUDr. Tomáš Ürge, PhD.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#