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Review

Recent insights into Histone Acetyltransferase-1: biological function and involvement in pathogenesis

, ORCID Icon, , , ORCID Icon & ORCID Icon
Pages 838-850 | Received 24 Jul 2020, Accepted 17 Sep 2020, Published online: 04 Oct 2020

References

  • Brownell JE, Allis CD. Special HATs for special occasions: linking histone acetylation to chromatin assembly and gene activation. Curr Opin Genet Dev. 1996;6:176–184.
  • Biswas S, Rao CM. Epigenetic tools (The writers, the readers and the erasers) and their implications in cancer therapy. Eur J Pharmacol. 2018;837:8–24.
  • Xu H, Wang Y, Lin S, et al. PTMD: A database of human disease-associated post-translational modifications. Genom Proteom Bioinform. 2018;16:244–251.
  • Yang X-J. The diverse superfamily of lysine acetyltransferases and their roles in leukemia and other diseases. Nucleic Acids Res. 2004;32:959–976.
  • Sharma S, Kelly TK, Jones PA. Epigenetics in cancer. Carcinogenesis. 2010;31:27–36.
  • Allfrey VG, Faulkner R, Mirsky AE. Acetylation and methylation of histones and their possible role in the regulation of RNA synthesis. Proc Natl Acad Sci. 1964;51:786–794.
  • Ehrenhofer-Murray AE. Chromatin dynamics at DNA replication, transcription and repair. Eur J Biochem. 2004;271:2335–2349.
  • Thiagalingam S, Cheng KH, Lee HJ, et al. Histone deacetylases: unique players in shaping the epigenetic histone code. Ann N Y Acad Sci. 2003;983:84–100.
  • Seto E, Yoshida M. Erasers of histone acetylation: the histone deacetylase enzymes. Cold Spring Harb Perspect Biol. 2014;6:a018713–a018713.
  • Josling GA, Selvarajah SA, Petter M, et al. The role of bromodomain proteins in regulating gene expression. Genes (Basel). 2012;3:320–343.
  • Tessarz P, Kouzarides T. Histone core modifications regulating nucleosome structure and dynamics. Nat Rev Mol Cell Biol. 2014;15:703–708.
  • Murr R, Loizou JI, Yang Y-G, et al. Histone acetylation by Trrap–Tip60 modulates loading of repair proteins and repair of DNA double-strand breaks. Nat Cell Biol. 2006;8:91–99.
  • Gong F, Miller KM. Mammalian DNA repair: HATs and HDACs make their mark through histone acetylation. Mutat Res Mol Mech Mutagen. 2013;750:23–30.
  • Ruiz-Carrillo A, Wangh L, Allfrey V. Processing of newly synthesized histone molecules. Science. 1975;190:117–128.
  • Jackson V, Shires A, Tanphaichitr N, et al. Modifications to histones immediately after synthesis. J Mol Biol. 1976;104:471–483.
  • Annunziato AT, Hansen JC. Role of histone acetylation in the assembly and modulation of chromatin structures. Gene Expr. 2001;9:37–61.
  • Krude T. Chromatin: nucleosome assembly during DNA replication. Curr Biol. 1995;5:1232–1234.
  • Verreault A. De novo nucleosome assembly: new pieces in an old puzzle. Genes Dev. 2000;14:1430–1438.
  • Campos EI, Reinberg D. Histones: annotating chromatin. Annu Rev Genet. 2009;43:559–599.
  • Sobel RE, Cook RG, Perry CA, et al. Conservation of deposition-related acetylation sites in newly synthesized histones H3 and H4. Proc Natl Acad Sci. 1995;92:1237–1241.
  • Kuo MH, Brownell JE., Sobel RE, et al. Transcription-linked acetylation by Gcn5p of histones H3 and H4 at specific lysines. Nature. 1996;383:269–272.
  • Parthun MR. Histone acetyltransferase 1: more than just an enzyme? Biochim Biophys Acta - Genet Regul Mech. 2012;1819:256–263.
  • Chicoine LG, Schulman IG, Richman R, et al. Nonrandom utilization of acetylation sites in histones isolated from Tetrahymena evidence for functionally distinct H4 acetylation sites. J Biol Chem. 1986;261.
  • Benson LJ, Gu Y, Yakovleva T, et al. Modifications of H3 and H4 during chromatin replication, nucleosome assembly, and histone exchange. J Biol Chem. 2006;281:9287–9296.
  • Cousens LS, Alberts BM. Accessibility of newly synthesized chromatin to histone acetylase. J Biol Chem. 1982;257.
  • Loyola A, Bonaldi T, Roche D, et al. PTMs on H3 variants before chromatin assembly potentiate their final epigenetic state. Mol Cell. 2006;24:309–316.
  • Sakamoto A, Terui Y, Uemura T, et al. Polyamines regulate gene expression by stimulating translation of histone acetyltransferase mRNAs. J Biol Chem. 2020;295:8736–8745.
  • Di Martile M, Del Bufalo D, Trisciuoglio D. The multifaceted role of lysine acetylation in cancer: prognostic biomarker and therapeutic target. Oncotarget. 2016;7:55789–55810.
  • Trisciuoglio D, Di Martile M, Del Bufalo D. Emerging role of histone acetyltransferase in stem cells and cancer. Stem Cells Int. 2018;2018:1–11.
  • Avvakumov N, Côté J. The MYST family of histone acetyltransferases and their intimate links to cancer. Oncogene. 2007;26:5395–5407.
  • Iyer NG, Özdag H, Caldas C. p300/CBP and cancer. Oncogene. 2004;23:4225–4231.
  • McCullough CE, Marmorstein R. Molecular basis for histone acetyltransferase regulation by binding partners, associated domains, and autoacetylation. ACS Chem Biol. 2016;11:632–642.
  • Kleff S, Andrulis ED, Anderson CW, et al. Identification of a gene encoding a yeast histone H4 acetyltransferase. J Biol Chem. 1995;270:24674–24677.
  • Parthun MR, Widom J, Gottschling DE. The major cytoplasmic histone acetyltransferase in yeast: links to chromatin replication and histone metabolism. Cell. 1996;87:85–94.
  • Verreault A, Kaufman PD, Kobayashi R, et al. Nucleosomal DNA regulates the core-histone-binding subunit of the human Hat1 acetyltransferase. Curr Biol. 1998;8:96–108.
  • Wu H, Moshkina N, Min J, et al. Structural basis for substrate specificity and catalysis of human histone acetyltransferase 1. Proc Natl Acad Sci U S A. 2012;109:8925–8930.
  • Murzina NV, Pei XY, Zhang W, et al. Structural basis for the recognition of histone H4 by the histone-chaperone RbAp46. Structure. 2008;16:1077–1085.
  • Lusser A, Eberharter A, Loidl A, et al. Analysis of the histone acetyltransferase B complex of maize embryos. Nucleic Acids Res. 1999;27:4427–4435.
  • Imhof A, Wolffe AP. Purification and properties of the xenopus Hat1 acetyltransferase: association with the 14-3-3 proteins in the oocyte nucleus. Biochemistry. 1999;38:13085–13093.
  • Lebel EA, Boukamp P, Tafrov ST. Irradiation with heavy-ion particles changes the cellular distribution of human histone acetyltransferase HAT1. Mol Cell Biochem. 2010;339:271–284.
  • Ruiz-García AB, Sendra R, Galiana M, et al. Hat1 and Hat2 proteins are components of a yeast nuclear histone acetyltransferase enzyme specific for free histone H4. J Biol Chem. 1998;273:12599–12605.
  • Ai X, Parthun MR. The nuclear Hat1p/Hat2p complex. Mol Cell. 2004;14:195–205.
  • Poveda A, Pamblanco M, Tafrov S, et al. Hif1 is a component of yeast histone acetyltransferase B, a complex mainly localized in the nucleus. J Biol Chem. 2004;279:16033–16043.
  • Mosammaparast N, Guo Y, Shabanowitz J, et al. Pathways mediating the nuclear import of histones H3 and H4 in yeast. J Biol Chem. 2002;277:862–868.
  • Barman HK, Takami Y, Nishijima H, et al. Histone acetyltransferase-1 regulates integrity of cytosolic histone H3-H4 containing complex. Biochem Biophys Res Commun. 2008;373:624–630.
  • Campos EI, Fillingham J, Li G, et al. The program for processing newly-synthesized histones H3.1 and H4 HHS public access author manuscript. Nat Struct Mol Biol. 2010;17:1343–1351.
  • Ejlassi-Lassallette A, Mocquard E, Arnaud M-C, et al. H4 replication-dependent diacetylation and Hat1 promote S-phase chromatin assembly in vivo. Mol Biol Cell. 2011;22:245–255.
  • Saade E, Mechold U, Kulyyassov A, et al. Analysis of interaction partners of H4 histone by a new proteomics approach. Proteomics. 2009;9:4934–4943.
  • Saavedra F, Gurard-Levin ZA, Rojas-Villalobos C, et al. JMJD1B, a novel player in histone H3 and H4 processing to ensure genome stability. Epigene Chromat. 2020;13. DOI:10.1186/s13072-020-00331-1.
  • Dunleavy EM, Pidoux AL, Monet M, et al. A NASP (N1/N2)-related protein, Sim3, binds CENP-A and is required for its deposition at fission yeast centromeres. Mol Cell. 2007;28:1029–1044.
  • Fillingham J, Recht J, Silva AC, et al. Chaperone control of the activity and specificity of the histone H3 acetyltransferase Rtt109. Mol Cell Biol. 2008;28:4342–4353.
  • Blackwell JS, Wilkinson ST, Mosammaparast N, et al. Mutational analysis of H3 and H4 N termini reveals distinct roles in nuclear import. J Biol Chem. 2007;282:20142–20150.
  • Alvarez F, Muñoz F, Schilcher P, et al. Sequential establishment of marks on soluble histones H3 and H4. J Biol Chem. 2011;286:17714–17721.
  • Agudelo Garcia PA, Lovejoy CM, Nagarajan P, et al. Histone acetyltransferase 1 is required for DNA replication fork function and stability. J Biol Chem. 2020;295:8363–8373.
  • An S, Yoon J, Kim H, et al. Structure-based nuclear import mechanism of histones H3 and H4 mediated by Kap123. Elife. 2017;6. DOI:10.7554/eLife.30244
  • Garcia PAA, Hoover ME, Zhang P, et al. Identification of multiple roles for histone acetyltransferase 1 in replication-coupled chromatin assembly. Nucleic Acids Res. 2017;45:9319–9335.
  • Varga J, Korbai S, Neller A, et al. Hat1 acetylates histone H4 and modulates the transcriptional program in drosophila embryogenesis. Sci Rep. 2019;9:17973.
  • Nagarajan P, Ge Z, Sirbu B, et al. Histone acetyl transferase 1 is essential for mammalian development, genome stability, and the processing of newly synthesized histones H3 and H4. PLoS Genet. 2013;9. DOI:10.1371/journal.pgen.1003518.
  • Agudelo Garcia PA, Nagarajan P, Parthun MR. Hat1-dependent lysine acetylation targets diverse cellular functions. J Proteome Res. 2020;19:1663–1673.
  • Suter B, Pogoutse O, Guo X, et al. Association with the origin recognition complex suggests a novel role for histone acetyltransferase Hat1p/Hat2p. BMC Biol. 2007;5:38.
  • Yang X, Li L, Liang J, et al. Histone acetyltransferase 1 promotes homologous recombination in DNA repair by facilitating histone turnover. J Biol Chem. 2013;288:18271–18282.
  • Braunstein M, Sobel RE, Allis CD, et al. Efficient transcriptional silencing in saccharomyces cerevisiae requires a heterochromatin histone acetylation pattern. Mol Cell Biol. 1996;16:4349–4356.
  • Qin S, Parthun MR. Histone H3 and the histone acetyltransferase Hat1p contribute to DNA double-strand break repair. Mol Cell Biol. 2002;22:8353–8365.
  • Benson LJ, Phillips JA, Gu Y, et al. Properties of the type B histone acetyltransferase Hat1. J Biol Chem. 2007;282:836–842.
  • Tong K, Keller T, Hoffman CS, et al. Schizosaccharomyces pombe Hat1 (Kat1) is associated with Mis16 and is required for telomeric silencing. Eukaryot Cell. 2012;11:1095–1103.
  • Barman HK, Takami Y, Ono T, et al. 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. 2006;345:1547–1557.
  • Kelly TJ, Qin S, Gottschling DE, et al. Type B histone acetyltransferase Hat1p participates in telomeric silencing. Mol Cell Biol. 2000;20:7051–7058.
  • Mersfelder EL, Parthun MR. Involvement of Hat1p (Kat1p) catalytic activity and subcellular localization in telomeric silencing. J Biol Chem. 2008;283:29060–29068.
  • Mukherjee SP, Behar M, Birnbaum HA, et al. Analysis of the RelA: CBP/p300 interaction reveals its involvement in NF-κB-driven transcription. PLoS Biol. 2013;11:e1001647.
  • Sadler AJ, Suliman BA, Yu L, et al. The acetyltransferase HAT1 moderates the NF-κB response by regulating the transcription factor PLZF. Nat Commun. 2015;6:6795.
  • Olsen JV, Blagoev B, Gnad F, et al. Global, in vivo, and site-specific phosphorylation dynamics in signaling networks. Cell. 2006;127:635–648.
  • Lin RJ, Nagy L, Inoue S, et al. Role of the histone deacetylase complex in acute promyelocytic leukaemia. Nature. 1998;391:811–814.
  • Yan Q, Carmody RJ, Qu Z, et al. Nuclear factor-κB binding motifs specify Toll-like receptor-induced gene repression through an inducible repressosome. Proc Natl Acad Sci U S A. 2012;109:14140–14145.
  • Yang G, Feng J, Liu Y, et al. HAT1 signaling confers to assembly and epigenetic regulation of HBV cccDNA minichromosome. Theranostics. 2019;9:7345–7358.
  • Yang L, Lin C, Jin C, et al. LncRNA-dependent mechanisms of androgen-receptor-regulated gene activation programs. Nature. 2013;500:598–602.
  • Espíndola MS, Soares LS, Galvão-Lima LJ, et al. Epigenetic alterations are associated with monocyte immune dysfunctions in HIV-1 infection. Sci Rep. 2018;8:1–14.
  • Jin X, Tian S, Li P. Histone acetyltransferase 1 promotes cell proliferation and induces cisplatin resistance in hepatocellular carcinoma. Oncol Res. 2017;25:939–946.
  • Han N, Shi L, Guo Q, et al. HAT1 induces lung cancer cell apoptosis via up regulating Fas. Oncotarget. 2017;8:89970–89977.
  • Miao BP, Zhang RS, Yang G, et al. Histone acetyltransferase 1 up regulates Bcl2L12 expression in nasopharyngeal cancer cells. Arch Biochem Biophys. 2018;646:72–79.
  • Fan P, Zhao J, Meng Z, et al. Overexpressed histone acetyltransferase 1 regulates cancer immunity by increasing programmed death-ligand 1 expression in pancreatic cancer. J Exp Clin Cancer Res. 2019;38:1–12.
  • Xue L, Hou J, Wang Q, et al. RNAi screening identifies HAT1 as a potential drug target in esophageal squamous cell carcinoma. Int J Clin Exp Pathol. 2014;7:3898–3907.
  • Seiden-Long IM, Brown KR, Shih W, et al. Transcriptional targets of hepatocyte growth factor signaling and Ki-ras oncogene activation in colorectal cancer. Oncogene. 2006;25:91–102.
  • Gruber JJ, Geller B, Lipchik AM, et al. HAT1 coordinates histone production and acetylation via H4 promoter binding. Mol Cell. 2019;75:711–724.e5.
  • Luan Y, Ngo L, Han Z, et al. Histone Acetyltransferases. In: Epigenetic technological applications Elsevier; 2015. p 291–317. DOI: 10.1016/B978-0-12-801080-8.00014-4
  • Zheng Y, Balasubramanyam K, Cebrat M, et al. Synthesis and evaluation of a potent and selective cell-permeable p300 histone acetyltransferase inhibitor. J Am Chem Soc. 2005;127:17182–17183.
  • Huang M, Huang J, Zheng Y, et al. Histone acetyltransferase inhibitors: an overview in synthesis, structure-activity relationship and molecular mechanism. Eur J Med Chem. 2019;178:259–286.
  • Eliseeva ED, Valkov V, Jung M, et al. Characterization of novel inhibitors of histone acetyltransferases. Mol Cancer Ther. 2007;6:2391–2398.
  • Manzo F, Tambaro FP, Mai A, et al. Histone acetyltransferase inhibitors and preclinical studies. Expert Opin Ther Pat. 2009;19:761–774.
  • Dekker FJ, Haisma HJ. Histone acetyl transferases as emerging drug targets. Drug Discov Today. 2009;14:942–948.
  • Brown JAL. Patent spotlight: small-molecule lysine acetyltransferase inhibitors (KATi). Pharm Pat Anal. 2020;9:17–28.
  • Lau OD, Kundu TK, Soccio RE, et al. HATs off: selective synthetic inhibitors of the histone acetyltransferases p300 and PCAF. Mol Cell. 2000;5:589–595.
  • Lau OD, Courtney AD, Vassilev A, et al. p300/CBP-associated factor histone acetyltransferase processing of a peptide substrate. J Biol Chem. 2000;275:21953–21959.
  • Sagar V, Zheng W, Thompson PR, et al. Bisubstrate analogue structure–activity relationships for p300 histone acetyltransferase inhibitors. Bioorg Med Chem. 2004;12:3383–3390.
  • Cebrat M, Kim CM, Thompson PR, et al. Synthesis and analysis of potential prodrugs of coenzyme A analogues for the inhibition of the histone acetyltransferase p300. Bioorg Med Chem. 2003;11:3307–3313.
  • Ngo L, Brown T, Zheng YG. Bisubstrate inhibitors to target histone acetyltransferase 1. Chem Biol Drug Des. 2019;93:865–873.

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