Functional Antagonism between Sas3 and Gcn5 Acetyltransferases and ISWI Chromatin Remodelers

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Chromatin-modifying enzymes and ATP-dependent remodeling complexes have been intensely studied individually, yet how these activities are coordinated to ensure essential cell functions such as transcription, replication, and repair of damage is not well understood. In this study, we show that the critical loss of Sas3 and Gcn5 acetyltransferases in yeast can be functionally rescued by inactivation of ISWI remodelers. This genetic interaction depends on the ATPase activities of Isw1 and Isw2, suggesting that it involves chromatin remodeling activities driven by the enzymes. Genetic dissection of the Isw1 complexes reveals that the antagonistic effects are mediated specifically by the Isw1a complex. Loss of Sas3 and Gcn5 correlates with defective RNA polymerase II (RNAPII) occupancy at actively transcribed genes, as well as a significant loss of H3K14 acetylation. Inactivation of the Isw1a complex in the acetyltransferase mutants restores RNAPII recruitment at active genes, indicating that transcriptional regulation may be the mechanism underlying suppression. Dosage studies and further genetic dissection reveal that the Isw1b complex may act in suppression through down-regulation of Isw1a. These studies highlight the importance of balanced chromatin modifying and remodeling activities for optimal transcription and cell growth.

Vyšlo v časopise: Functional Antagonism between Sas3 and Gcn5 Acetyltransferases and ISWI Chromatin Remodelers. PLoS Genet 8(10): e32767. doi:10.1371/journal.pgen.1002994
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002994

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Zdroje

1. ClapierCR, CairnsBR (2009) The biology of chromatin remodeling complexes. Annu Rev Biochem 78: 273–304.

2. KorberP, BeckerPB (2010) Nucleosome dynamics and epigenetic stability. Essays Biochem 48: 63–74.

3. KouzaridesT (2007) Chromatin modifications and their function. Cell 128: 693–705.

4. TavernaSD, LiH, RuthenburgAJ, AllisCD, PatelDJ (2007) How chromatin-binding modules interpret histone modifications: lessons from professional pocket pickers. Nat Struct Mol Biol 14: 1025–1040.

5. SuganumaT, WorkmanJL (2008) Crosstalk among Histone Modifications. Cell 135: 604–607.

6. NarlikarGJ, FanHY, KingstonRE (2002) Cooperation between complexes that regulate chromatin structure and transcription. Cell 108: 475–487.

7. BergerSL (2007) The complex language of chromatin regulation during transcription. Nature 447: 407–412.

8. LiB, CareyM, WorkmanJL (2007) The role of chromatin during transcription. Cell 128: 707–719.

9. van AttikumH, GasserSM (2009) Crosstalk between histone modifications during the DNA damage response. Trends Cell Biol 19: 207–217.

10. PollardKJ, PetersonCL (1997) Role for ADA/GCN5 products in antagonizing chromatin-mediated transcriptional repression. Mol Cell Biol 17: 6212–6222.

11. RobertsSM, WinstonF (1997) Essential functional interactions of SAGA, a Saccharomyces cerevisiae complex of Spt, Ada, and Gcn5 proteins, with the Snf/Swi and Srb/mediator complexes. Genetics 147: 451–465.

12. SudarsanamP, CaoY, WuL, LaurentBC, WinstonF (1999) The nucleosome remodeling complex, Snf/Swi, is required for the maintenance of transcription in vivo and is partially redundant with the histone acetyltransferase, Gcn5. EMBO J 18: 3101–3106.

13. SyntichakiP, TopalidouI, ThireosG (2000) The Gcn5 bromodomain co-ordinates nucleosome remodelling. Nature 404: 414–417.

14. HassanAH, NeelyKE, WorkmanJL (2001) Histone acetyltransferase complexes stabilize swi/snf binding to promoter nucleosomes. Cell 104: 817–827.

15. WoodageT, BasraiMA, BaxevanisAD, HieterP, CollinsFS (1997) Characterization of the CHD family of proteins. Proc Natl Acad Sci U S A 94: 11472–11477.

16. TranHG, StegerDJ, IyerVR, JohnsonAD (2000) The chromo domain protein chd1p from budding yeast is an ATP-dependent chromatin-modifying factor. EMBO J 19: 2323–2331.

17. Pray-GrantMG, DanielJA, SchieltzD, YatesJR3rd, GrantPA (2005) Chd1 chromodomain links histone H3 methylation with SAGA- and SLIK-dependent acetylation. Nature 433: 434–438.

18. KastenM, SzerlongH, Erdjument-BromageH, TempstP, WernerM, et al. (2004) Tandem bromodomains in the chromatin remodeler RSC recognize acetylated histone H3 Lys14. EMBO J 23: 1348–1359.

19. VanDemarkAP, KastenMM, FerrisE, HerouxA, HillCP, et al. (2007) Autoregulation of the rsc4 tandem bromodomain by gcn5 acetylation. Mol Cell 27: 817–828.

20. PokholokDK, HarbisonCT, LevineS, ColeM, HannettNM, et al. (2005) Genome-wide map of nucleosome acetylation and methylation in yeast. Cell 122: 517–527.

21. DurantM, PughBF (2006) Genome-wide relationships between TAF1 and histone acetyltransferases in Saccharomyces cerevisiae. Mol Cell Biol 26: 2791–2802.

22. HoweL, AustonD, GrantP, JohnS, CookRG, et al. (2001) Histone H3 specific acetyltransferases are essential for cell cycle progression. Genes Dev 15: 3144–3154.

23. KristjuhanA, WalkerJ, SukaN, GrunsteinM, RobertsD, et al. (2002) Transcriptional inhibition of genes with severe histone h3 hypoacetylation in the coding region. Mol Cell 10: 925–933.

24. RobertF, PokholokDK, HannettNM, RinaldiNJ, ChandyM, et al. (2004) Global position and recruitment of HATs and HDACs in the yeast genome. Mol Cell 16: 199–209.

25. LafonA, ChangCS, ScottEM, JacobsonSJ, PillusL (2007) MYST opportunities for growth control: yeast genes illuminate human cancer gene functions. Oncogene 26: 5373–5384.

26. RosalenyLE, Ruiz-GarciaAB, Garcia-MartinezJ, Perez-OrtinJE, TorderaV (2007) The Sas3p and Gcn5p histone acetyltransferases are recruited to similar genes. Genome Biol 8: R119.

27. ZhangW, BoneJR, EdmondsonDG, TurnerBM, RothSY (1998) Essential and redundant functions of histone acetylation revealed by mutation of target lysines and loss of the Gcn5p acetyltransferase. EMBO J 17: 3155–3167.

28. ChoiJK, GrimesDE, RoweKM, HoweLJ (2008) Acetylation of Rsc4p by Gcn5p is essential in the absence of histone H3 acetylation. Mol Cell Biol 28: 6967–6972.

29. LaurentBC, YangX, CarlsonM (1992) An essential Saccharomyces cerevisiae gene homologous to SNF2 encodes a helicase-related protein in a new family. Mol Cell Biol 12: 1893–1902.

30. ShenX, MizuguchiG, HamicheA, WuC (2000) A chromatin remodelling complex involved in transcription and DNA processing. Nature 406: 541–544.

31. NeigebornL, CarlsonM (1984) Genes affecting the regulation of SUC2 gene expression by glucose repression in Saccharomyces cerevisiae. Genetics 108: 845–858.

32. TsukiyamaT, PalmerJ, LandelCC, ShiloachJ, WuC (1999) Characterization of the imitation switch subfamily of ATP-dependent chromatin-remodeling factors in Saccharomyces cerevisiae. Genes Dev 13: 686–697.

33. GelbartME, RechsteinerT, RichmondTJ, TsukiyamaT (2001) Interactions of Isw2 chromatin remodeling complex with nucleosomal arrays: analyses using recombinant yeast histones and immobilized templates. Mol Cell Biol 21: 2098–2106.

34. FazzioTG, TsukiyamaT (2003) Chromatin remodeling in vivo: evidence for a nucleosome sliding mechanism. Mol Cell 12: 1333–1340.

35. VaryJCJr, GangarajuVK, QinJ, LandelCC, KooperbergC, et al. (2003) Yeast Isw1p forms two separable complexes in vivo. Mol Cell Biol 23: 80–91.

36. FlanaganJF, MiLZ, ChruszczM, CymborowskiM, ClinesKL, et al. (2005) Double chromodomains cooperate to recognize the methylated histone H3 tail. Nature 438: 1181–1185.

37. CareyM, LiB, WorkmanJL (2006) RSC exploits histone acetylation to abrogate the nucleosomal block to RNA polymerase II elongation. Mol Cell 24: 481–487.

38. FerreiraH, FlausA, Owen-HughesT (2007) Histone modifications influence the action of Snf2 family remodelling enzymes by different mechanisms. J Mol Biol 374: 563–579.

39. YadonAN, TsukiyamaT (2011) SnapShot: Chromatin remodeling: ISWI. Cell 144: 453–453 e451.

40. BoyerLA, LatekRR, PetersonCL (2004) The SANT domain: a unique histone-tail-binding module? Nat Rev Mol Cell Biol 5: 158–163.

41. PinskayaM, NairA, ClynesD, MorillonA, MellorJ (2009) Nucleosome remodeling and transcriptional repression are distinct functions of Isw1 in Saccharomyces cerevisiae. Mol Cell Biol 29: 2419–2430.

42. BoyerLA, LangerMR, CrowleyKA, TanS, DenuJM, et al. (2002) Essential role for the SANT domain in the functioning of multiple chromatin remodeling enzymes. Mol Cell 10: 935–942.

43. YuJ, LiY, IshizukaT, GuentherMG, LazarMA (2003) A SANT motif in the SMRT corepressor interprets the histone code and promotes histone deacetylation. EMBO J 22: 3403–3410.

44. MorillonA, KarabetsouN, O'SullivanJ, KentN, ProudfootN, et al. (2003) Isw1 chromatin remodeling ATPase coordinates transcription elongation and termination by RNA polymerase II. Cell 115: 425–435.

45. GrantPA, EberharterA, JohnS, CookRG, TurnerBM, et al. (1999) Expanded lysine acetylation specificity of Gcn5 in native complexes. J Biol Chem 274: 5895–5900.

46. WhitehouseI, RandoOJ, DelrowJ, TsukiyamaT (2007) Chromatin remodelling at promoters suppresses antisense transcription. Nature 450: 1031–1035.

47. TiroshI, SigalN, BarkaiN (2010) Widespread remodeling of mid-coding sequence nucleosomes by Isw1. Genome Biol 11: R49.

48. SekingerEA, MoqtaderiZ, StruhlK (2005) Intrinsic histone-DNA interactions and low nucleosome density are important for preferential accessibility of promoter regions in yeast. Mol Cell 18: 735–748.

49. CairnsBR (2009) The logic of chromatin architecture and remodelling at promoters. Nature 461: 193–198.

50. RineJ (1991) Gene overexpression in studies of Saccharomyces cerevisiae. Methods Enzymol 194: 239–251.

51. SopkoR, HuangD, PrestonN, ChuaG, PappB, et al. (2006) Mapping pathways and phenotypes by systematic gene overexpression. Mol Cell 21: 319–330.

52. PrelichG (2012) Gene overexpression: uses, mechanisms, and interpretation. Genetics 190: 841–854.

53. YangXJ, SetoE (2008) Lysine acetylation: codified crosstalk with other posttranslational modifications. Mol Cell 31: 449–461.

54. SpangeS, WagnerT, HeinzelT, KramerOH (2009) Acetylation of non-histone proteins modulates cellular signalling at multiple levels. Int J Biochem Cell Biol 41: 185–198.

55. SukaN, SukaY, CarmenAA, WuJ, GrunsteinM (2001) Highly specific antibodies determine histone acetylation site usage in yeast heterochromatin and euchromatin. Mol Cell 8: 473–479.

56. GoldmarkJP, FazzioTG, EstepPW, ChurchGM, TsukiyamaT (2000) The Isw2 chromatin remodeling complex represses early meiotic genes upon recruitment by Ume6p. Cell 103: 423–433.

57. KentNA, KarabetsouN, PolitisPK, MellorJ (2001) In vivo chromatin remodeling by yeast ISWI homologs Isw1p and Isw2p. Genes Dev 15: 619–626.

58. DeuringR, FantiL, ArmstrongJA, SarteM, PapoulasO, et al. (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.

59. FyodorovDV, BlowerMD, KarpenGH, KadonagaJT (2004) Acf1 confers unique activities to ACF/CHRAC and promotes the formation rather than disruption of chromatin in vivo. Genes Dev 18: 170–183.

60. CoronaDF, SiriacoG, ArmstrongJA, SnarskayaN, McClymontSA, et al. (2007) ISWI regulates higher-order chromatin structure and histone H1 assembly in vivo. PLoS Biol 5: e232 doi:10.1371/journal.pbio.0050232.

61. MorillonA, KarabetsouN, NairA, MellorJ (2005) Dynamic lysine methylation on histone H3 defines the regulatory phase of gene transcription. Mol Cell 18: 723–734.

62. LindstromKC, VaryJCJr, ParthunMR, DelrowJ, TsukiyamaT (2006) Isw1 functions in parallel with the NuA4 and Swr1 complexes in stress-induced gene repression. Mol Cell Biol 26: 6117–6129.

63. MitchellL, LambertJP, GerdesM, Al-MadhounAS, SkerjancIS, et al. (2008) Functional dissection of the NuA4 histone acetyltransferase reveals its role as a genetic hub and that Eaf1 is essential for complex integrity. Mol Cell Biol 28: 2244–2256.

64. CoronaDF, ClapierCR, BeckerPB, TamkunJW (2002) Modulation of ISWI function by site-specific histone acetylation. EMBO Rep 3: 242–247.

65. Shogren-KnaakM, IshiiH, SunJM, PazinMJ, DavieJR, et al. (2006) Histone H4-K16 acetylation controls chromatin structure and protein interactions. Science 311: 844–847.

66. FerreiraR, EberharterA, BonaldiT, ChiodaM, ImhofA, et al. (2007) Site-specific acetylation of ISWI by GCN5. BMC Mol Biol 8: 73.

67. LugerK, DechassaML, TremethickDJ (2012) New insights into nucleosome and chromatin structure: an ordered state or a disordered affair? Nat Rev Mol Cell Biol 13: 436–447.

68. LusserA, UrwinDL, KadonagaJT (2005) Distinct activities of CHD1 and ACF in ATP-dependent chromatin assembly. Nat Struct Mol Biol 12: 160–166.

69. MaierVK, ChiodaM, RhodesD, BeckerPB (2008) ACF catalyses chromatosome movements in chromatin fibres. EMBO J 27: 817–826.

70. StockdaleC, FlausA, FerreiraH, Owen-HughesT (2006) Analysis of nucleosome repositioning by yeast ISWI and Chd1 chromatin remodeling complexes. J Biol Chem 281: 16279–16288.

71. GangarajuVK, BartholomewB (2007) Dependency of ISW1a chromatin remodeling on extranucleosomal DNA. Mol Cell Biol 27: 3217–3225.

72. Amberg D, Burke D, Strathern J (2005) Methods in yeast genetics: a Cold Spring Harbor Laboratory course manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.

73. LongtineMS, McKenzieA3rd, DemariniDJ, ShahNG, WachA, et al. (1998) Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14: 953–961.

74. EngebrechtJ, HirschJ, RoederGS (1990) Meiotic gene conversion and crossing over: their relationship to each other and to chromosome synapsis and segregation. Cell 62: 927–937.

75. DarstRP, GarciaSN, KochMR, PillusL (2008) Slx5 promotes transcriptional silencing and is required for robust growth in the absence of Sir2. Mol Cell Biol 28: 1361–1372.

76. KentNA, MellorJ (1995) Chromatin structure snap-shots: rapid nuclease digestion of chromatin in yeast. Nucleic Acids Res 23: 3786–3787.

77. WuL, WinstonF (1997) Evidence that Snf-Swi controls chromatin structure over both the TATA and UAS regions of the SUC2 promoter in Saccharomyces cerevisiae. Nucleic Acids Res 25: 4230–4234.

78. WangSS, ZhouBO, ZhouJQ (2011) Histone H3 lysine 4 hypermethylation prevents aberrant nucleosome remodeling at the PHO5 promoter. Mol Cell Biol 31: 3171–3181.