Histone Acetyl Transferase 1 Is Essential for Mammalian Development, Genome Stability, and the Processing of Newly Synthesized Histones H3 and H4

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Histone acetyltransferase 1 is an evolutionarily conserved type B histone acetyltransferase that is thought to be responsible for the diacetylation of newly synthesized histone H4 on lysines 5 and 12 during chromatin assembly. To understand the function of this enzyme in a complex organism, we have constructed a conditional mouse knockout model of Hat1. Murine Hat1 is essential for viability, as homozygous deletion of Hat1 results in neonatal lethality. The lungs of embryos and pups genetically deficient in Hat1 were much less mature upon histological evaluation. The neonatal lethality is due to severe defects in lung development that result in less aeration and respiratory distress. Many of the Hat1^−/− neonates also display significant craniofacial defects with abnormalities in the bones of the skull and jaw. Hat1^−/− mouse embryonic fibroblasts (MEFs) are defective in cell proliferation and are sensitive to DNA damaging agents. In addition, the Hat1^−/− MEFs display a marked increase in genome instability. Analysis of histone dynamics at sites of replication-coupled chromatin assembly demonstrates that Hat1 is not only responsible for the acetylation of newly synthesized histone H4 but is also required to maintain the acetylation of histone H3 on lysines 9, 18, and 27 during replication-coupled chromatin assembly.

Vyšlo v časopise: Histone Acetyl Transferase 1 Is Essential for Mammalian Development, Genome Stability, and the Processing of Newly Synthesized Histones H3 and H4. PLoS Genet 9(6): e32767. doi:10.1371/journal.pgen.1003518
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003518

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1. DasC, TylerJK, ChurchillME (2010) The histone shuffle: histone chaperones in an energetic dance. Trends Biochem Sci 35: 476–489.

2. AlabertC, GrothA (2012) Chromatin replication and epigenome maintenance. Nat Rev Mol Cell Biol 13: 153–167.

3. AvvakumovN, NouraniA, CoteJ (2011) Histone chaperones: modulators of chromatin marks. Mol Cell 41: 502–514.

4. MargueronR, ReinbergD (2010) Chromatin structure and the inheritance of epigenetic information. Nat Rev Genet 11: 285–296.

5. AnnunziatoAT (2012) Assembling chromatin: The long and winding road. Biochim Biophys Acta 1819: 196–210.

6. AnnunziatoAT, HansenJC (2000) Role of histone acetylation in the assembly and modulation of chromatin structures. Gene Expr 9: 37–61.

7. MasumotoH, HawkeD, KobayashiR, VerreaultA (2005) A role for cell-cycle-regulated histone H3 lysine 56 acetylation in the DNA damage response. Nature 436: 294–298.

8. OzdemirA, SpicugliaS, LasonderE, VermeulenM, CampsteijnC, et al. (2005) Characterization of lysine 56 of histone H3 as an acetylation site in Saccharomyces cerevisiae. J Biol Chem 280: 25949–25952.

9. XuF, ZhangK, GrunsteinM (2005) Acetylation in histone H3 globular domain regulates gene expression in yeast. Cell 121: 375–385.

10. YeJ, AiX, EugeniEE, ZhangL, CarpenterLR, et al. (2005) Histone H4 lysine 91 acetylation a core domain modification associated with chromatin assembly. Mol Cell 18: 123–130.

11. ChenCC, CarsonJJ, FeserJ, TamburiniB, ZabaronickS, et al. (2008) Acetylated lysine 56 on histone H3 drives chromatin assembly after repair and signals for the completion of repair. Cell 134: 231–243.

12. RechtJ, TsubotaT, TannyJC, DiazRL, BergerJM, et al. (2006) Histone chaperone Asf1 is required for histone H3 lysine 56 acetylation, a modification associated with S phase in mitosis and meiosis. Proc Natl Acad Sci U S A 103: 6988–6993.

13. ZhouH, MaddenBJ, MuddimanDC, ZhangZ (2006) Chromatin assembly factor 1 interacts with histone h3 methylated at lysine 79 in the processes of epigenetic silencing and DNA repair. Biochemistry 45: 2852–2861.

14. MaasNL, MillerKM, DeFazioLG, ToczyskiDP (2006) Cell cycle and checkpoint regulation of histone H3 K56 acetylation by Hst3 and Hst4. Mol Cell 23: 109–119.

15. YuanJ, PuM, ZhangZ, LouZ (2009) Histone H3-K56 acetylation is important for genomic stability in mammals. Cell Cycle 8: 1747–1753.

16. KaplanT, LiuCL, ErkmannJA, HolikJ, GrunsteinM, et al. (2008) Cell cycle- and chaperone-mediated regulation of H3K56ac incorporation in yeast. PLoS Genet 4: e1000270.

17. LiQ, ZhouH, WurteleH, DaviesB, HorazdovskyB, et al. (2008) Acetylation of histone H3 lysine 56 regulates replication-coupled nucleosome assembly. Cell 134: 244–255.

18. MersfelderEL, ParthunMR (2006) The tale beyond the tail: histone core domain modifications and the regulation of chromatin structure. Nucleic Acids Res 34: 2653–2662.

19. BrownellJE, AllisCD (1996) Special HATs for special occasions: linking histone acetylation to chromatin assembly and gene activation. Current Opinion in Genetics & Development 6: 176–184.

20. KleffS, AndrulisED, AndersonCW, SternglanzR (1995) Identification of a gene encoding a yeast histone H4 acetyltransferase. J Biol Chem 270: 24674–24677.

21. ParthunMR, WidomJ, GottschlingDE (1996) The major cytoplasmic histone acetyltransferase in yeast: links to chromatin replication and histone metabolism. Cell 87: 85–94.

22. DriscollR, HudsonA, JacksonSP (2007) Yeast Rtt109 promotes genome stability by acetylating histone H3 on lysine 56. Science 315: 649–652.

23. HanJ, ZhouH, HorazdovskyB, ZhangK, XuRM, et al. (2007) Rtt109 acetylates histone H3 lysine 56 and functions in DNA replication. Science 315: 653–655.

24. SchneiderJ, BajwaP, JohnsonFC, BhaumikSR, ShilatifardA (2006) Rtt109 is required for proper H3K56 acetylation: a chromatin mark associated with the elongating RNA polymerase II. J Biol Chem 281: 37270–37274.

25. SklenarAR, ParthunMR (2004) Characterization of yeast histone H3-specific type B histone acetyltransferases identifies an ADA2-independent Gcn5p activity. BMC Biochem 5: 11.

26. BurgessRJ, ZhouH, HanJ, ZhangZ (2010) A role for Gcn5 in replication-coupled nucleosome assembly. Mol Cell 37: 469–480.

27. YangX, YuW, ShiL, SunL, LiangJ, et al. (2011) HAT4, a Golgi apparatus-anchored B-type histone acetyltransferase, acetylates free histone H4 and facilitates chromatin assembly. Mol Cell 44: 39–50.

28. QianYW, WangYC, HollingsworthREJr, JonesD, LingN, et al. (1993) A retinoblastoma-binding protein related to a negative regulator of Ras in yeast. Nature 364: 648–652.

29. AiX, ParthunMR (2004) The nuclear Hat1p/Hat2p complex: a molecular link between type B histone acetyltransferases and chromatin assembly. Mol Cell 14: 195–205.

30. LusserA, EberharterA, LoidlA, Goralik-SchramelM, HorngacherM, et al. (1999) Analysis of the histone acetyltransferase B complex of maize embryos. Nucleic Acids Res 27: 4427–4435.

31. ImhofA, WolffeAP (1999) Purification and properties of the xenopus hat1 acetyltransferase: association with the 14-3-3 proteins in the oocyte nucleus. Biochemistry 38: 13085–13093.

32. VerreaultA, KaufmanPD, KobayashiR, StillmanB (1998) Nucleosomal DNA regulates the core-histone-binding subunit of the human Hat1 acetyltransferase. Curr Biol 8: 96–108.

33. ChangL, LorangerSS, MizzenC, ErnstSG, AllisCD, et al. (1997) Histones in transit: cytosolic histone complexes and diacetylation of H4 during nucleosome assembly in human cells. Biochemistry 36: 469–480.

34. Ruiz-GarciaAB, SendraR, GalianaM, PamblancoM, Perez-OrtinJE, et al. (1998) HAT1 and HAT2 proteins are components of a yeast nuclear histone acetyltransferase enzyme specific for free histone H4. J Biol Chem 273: 12599–12605.

35. KellyTJ, QinS, GottschlingDE, ParthunMR (2000) Type B histone acetyltransferase Hat1p participates in telomeric silencing. Mol Cell Biol 20: 7051–7058.

36. QinS, ParthunMR (2002) Histone H3 and the histone acetyltransferase Hat1p contribute to DNA double-strand break repair. Mol Cell Biol 22: 8353–8365.

37. BarmanHK, TakamiY, OnoT, NishijimaH, SanematsuF, et al. (2006) Histone acetyltransferase 1 is dispensable for replication-coupled chromatin assembly but contributes to recover DNA damages created following replication blockage in vertebrate cells. Biochem Biophys Res Commun 345: 1547–1557.

38. BensonLJ, PhillipsJA, GuY, ParthunMR, HoffmanCS, et al. (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.

39. GeZ, WangH, ParthunMR (2011) Nuclear Hat1p Complex (NuB4) Components Participate in DNA Repair-linked Chromatin Reassembly. J Biol Chem 286: 16790–16799.

40. VerzijlbergenKF, van WelsemT, SieD, LenstraTL, TurnerDJ, et al. (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.

41. ParthunMR (2012) Histone acetyltransferase 1: More than just an enzyme? Biochim Biophys Acta 1819: 256–263.

42. Ejlassi-LassalletteA, MocquardE, ArnaudMC, ThirietC (2011) H4 replication-dependent diacetylation and Hat1 promote S-phase chromatin assembly in vivo. Mol Biol Cell 22: 245–255.

43. CamposEI, FillinghamJ, LiG, ZhengH, VoigtP, et al. (2010) The program for processing newly synthesized histones H3.1 and H4. Nat Struct Mol Biol 17: 1343–1351.

44. TagamiH, Ray-GalletD, AlmouzniG, NakataniY (2004) Histone H3.1 and H3.3 complexes mediate nucleosome assembly pathways dependent or independent of DNA synthesis. Cell 116: 51–61.

45. BarmanHK, TakamiY, NishijimaH, ShibaharaK, SanematsuF, et al. (2008) Histone acetyltransferase-1 regulates integrity of cytosolic histone H3-H4 containing complex. Biochem Biophys Res Commun 373: 624–630.

46. DraneP, OuararhniK, DepauxA, ShuaibM, HamicheA (2010) The death-associated protein DAXX is a novel histone chaperone involved in the replication-independent deposition of H3.3. Genes Dev 24: 1253–1265.

47. SaadeE, MecholdU, KulyyassovA, VertutD, LipinskiM, et al. (2009) Analysis of interaction partners of H4 histone by a new proteomics approach. Proteomics 9: 4934–4943.

48. SirbuBM, CouchFB, FeigerleJT, BhaskaraS, HiebertSW, et al. (2011) Analysis of protein dynamics at active, stalled, and collapsed replication forks. Genes Dev 25: 1320–1327.

49. ParthunMR (2007) Hat1: the emerging cellular roles of a type B histone acetyltransferase. Oncogene 26: 5319–5328.

50. BensonLJ, GuY, YakovlevaT, TongK, BarrowsC, et al. (2006) Modifications of H3 and H4 during chromatin replication, nucleosome assembly, and histone exchange. J Biol Chem 281: 9287–9296.

51. AlvarezF, MunozF, SchilcherP, ImhofA, AlmozuniG, et al. (2011) Sequential establishment of marks on soluble histones H3 and H4. J Biol Chem 286: 17714–17721.

52. MegeePC, MorganBA, MittmanBA, SmithMM (1990) Genetic analysis of histone H4: essential role of lysines subject to reversible acetylation. Science 247: 841–845.

53. MaXJ, WuJ, AltheimBA, SchultzMC, GrunsteinM (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. ShibaharaK, VerreaultA, StillmanB (2000) The N-terminal domains of histones H3 and H4 are not necessary for chromatin assembly factor-1- mediated nucleosome assembly onto replicated DNA in vitro. Proc Natl Acad Sci U S A 97: 7766–7771.

55. NakanoS, StillmanB, HorvitzHR (2011) Replication-coupled chromatin assembly generates a neuronal bilateral asymmetry in C. elegans. Cell 147: 1525–1536.

56. TongK, KellerT, HoffmanCS, AnnunziatoAT (2012) Schizosaccharomyces pombe Hat1 (Kat1) is associated with Mis16, and is required for telomeric silencing. Eukaryot Cell 11: 1095–1103.

57. KellyTJ, QinS, GottschlingDE, ParthunMR (2000) Type B histone acetyltransferase Hat1p participates in telomeric silencing. Mol Cell Biol 20: 7051–7058.

58. JasencakovaZ, ScharfAN, AskK, CorpetA, ImhofA, et al. (2010) Replication stress interferes with histone recycling and predeposition marking of new histones. Mol Cell 37: 736–743.

59. LoyolaA, AlmouzniG (2007) Marking histone H3 variants: how, when and why? Trends Biochem Sci 32: 425–433.

60. LoyolaA, BonaldiT, RocheD, ImhofA, AlmouzniG (2006) PTMs on H3 variants before chromatin assembly potentiate their final epigenetic state. Mol Cell 24: 309–316.

61. SobelRE, CookRG, PerryCA, AnnunziatoAT, AllisCD (1995) Conservation of deposition-related acetylation sites in newly synthesized histones H3 and H4. Proc Natl Acad Sci U S A 92: 1237–1241.

62. LewisPW, ElsaesserSJ, NohKM, StadlerSC, AllisCD (2010) Daxx is an H3.3-specific histone chaperone and cooperates with ATRX in replication-independent chromatin assembly at telomeres. Proc Natl Acad Sci U S A 107: 14075–14080.

63. CorpetA, AlmouzniG (2009) Making copies of chromatin: the challenge of nucleosomal organization and epigenetic information. Trends Cell Biol 19: 29–41.

64. Hogan B, Costantini F, Lacy E (1986) Manipulating the mouse embryo : a laboratory manual. Cold Spring Harbor, N.Y.: Cold Spring Harbor Laboratory. ix, 332 p. p.

65. ChangL, RyanCA, SchneiderCA, AnnunziatoAT (1999) Preparation/analysis of chromatin replicated in vivo and in isolated nuclei. Methods Enzymol 304: 76–99.

66. PerryCA, AllisCD, AnnunziatoAT (1993) Parental nucleosomes segregated to newly replicated chromatin are underacetylated relative to those assembled de novo. Biochemistry 32: 13615–13623.

67. AnnunziatoAT, EasonMB, PerryCA (1995) Relationship between methylation and acetylation of arginine-rich histones in cycling and arrested HeLa cells. Biochemistry 34: 2916–2924.

68. PanyimS, ChalkleyR (1969) High resolution acrylamide gel electrophoresis of histones. Arch Biochem Biophys 130: 337–346.