Cell cycle-dependent changes in H3K56ac in human cells

. 2015 ; 14 (24) : 3851-63.

Jazyk angličtina Země Spojené státy americké Médium print

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid26645646

The incorporation of histone H3 with an acetylated lysine 56 (H3K56ac) into the nucleosome is important for chromatin remodeling and serves as a marker of new nucleosomes during DNA replication and repair in yeast. However, in human cells, the level of H3K56ac is greatly reduced, and its role during the cell cycle is controversial. Our aim was to determine the potential of H3K56ac to regulate cell cycle progression in different human cell lines. A significant increase in the number of H3K56ac foci, but not in H3K56ac protein levels, was observed during the S and G2 phases in cancer cell lines, but was not observed in embryonic stem cell lines. Despite this increase, the H3K56ac signal was not present in late replication chromatin, and H3K56ac protein levels did not decrease after the inhibition of DNA replication. H3K56ac was not tightly associated with the chromatin and was primarily localized to active chromatin regions. Our results support the role of H3K56ac in transcriptionally active chromatin areas but do not confirm H3K56ac as a marker of newly synthetized nucleosomes in DNA replication.

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Hyland EM, Cosgrove MS, Molina H, Wang D, Pandey A, Cottee RJ, Boeke JD. Insights into the role of histone H3 and histone H4 core modifiable residues in Saccharomyces cerevisiae. Mol Cell Biol 2005; 25:10060-70; PMID:16260619; http://dx.doi.org/10.1128/MCB.25.22.10060-10070.2005 PubMed DOI PMC

Ozdemir A, Spicuglia S, Lasonder E, Vermeulen M, Campsteijn C, Stunnenberg HG, Logie C. Characterization of lysine 56 of histone H3 as an acetylation site in Saccharomyces cerevisiae. J Biol Chem 2005; 280:25949-52; PMID:15888442; http://dx.doi.org/10.1074/jbc.C500181200 PubMed DOI

Xu F, Zhang K, Grunstein M. Acetylation in histone H3 globular domain regulates gene expression in yeast. Cell 2005; 121:375-85; PMID:15882620; http://dx.doi.org/10.1016/j.cell.2005.03.011 PubMed DOI

Fillingham J, Recht J, Silva AC, Suter B, Emili A, Stagljar I, Krogan NJ, Allis CD, Keogh MC, Greenblatt JF. Chaperone control of the activity and specificity of the histone H3 acetyltransferase Rtt109. Mol Cell Biol 2008; 28:4342-53; PMID:18458063; http://dx.doi.org/10.1128/MCB.00182-08 PubMed DOI PMC

Kolonko EM, Albaugh BN, Lindner SE, Chen Y, Satyshur KA, Arnold KM, Kaufman PD, Keck JL, Denu JM. Catalytic activation of histone acetyltransferase Rtt109 by a histone chaperone. Proc Natl Acad Sci U S A 2010; 107:20275-80; PMID:21057107; http://dx.doi.org/10.1073/pnas.1009860107 PubMed DOI PMC

Erkmann JA, Kaufman PD. A negatively charged residue in place of histone H3K56 supports chromatin assembly factor association but not genotoxic stress resistance. DNA Repair (Amst) 2009; 8:1371-9; PMID:19796999; http://dx.doi.org/10.1016/j.dnarep.2009.09.004 PubMed DOI PMC

Smith S, Stillman B. Purification and characterization of CAF-I, a human cell factor required for chromatin assembly during DNA replication in vitro. Cell 1989; 58:15-25; PMID:2546672; http://dx.doi.org/10.1016/0092-8674(89)90398-X PubMed DOI

Recht J, Tsubota T, Tanny JC, Diaz RL, Berger JM, Zhang X, Garcia BA, Shabanowitz J, Burlingame AL, Hunt DF, et al.. 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 2006; 103:6988-93; PMID:16627621; http://dx.doi.org/10.1073/pnas.0601676103 PubMed DOI PMC

Li Q, Zhou H, Wurtele H, Davies B, Horazdovsky B, Verreault A, Zhang Z. Acetylation of histone H3 lysine 56 regulates replication-coupled nucleosome assembly. Cell 2008; 134:244-55; PMID:18662540; http://dx.doi.org/10.1016/j.cell.2008.06.018 PubMed DOI PMC

Chen CC, Carson JJ, Feser J, Tamburini B, Zabaronick S, Linger J, Tyler JK. Acetylated lysine 56 on histone H3 drives chromatin assembly after repair and signals for the completion of repair. Cell 2008; 134:231-43; PMID:18662539; http://dx.doi.org/10.1016/j.cell.2008.06.035 PubMed DOI PMC

Tsubota T, Berndsen CE, Erkmann JA, Smith CL, Yang L, Freitas MA, Denu JM, Kaufman PD. Histone H3-K56 acetylation is catalyzed by histone chaperone-dependent complexes. Mol Cell 2007; 25:703-12; PMID:17320445; http://dx.doi.org/10.1016/j.molcel.2007.02.006 PubMed DOI PMC

Han J, Zhou H, Horazdovsky B, Zhang K, Xu RM, Zhang Z. Rtt109 acetylates histone H3 lysine 56 and functions in DNA replication. Science 2007; 315:653-5; PMID:17272723; http://dx.doi.org/10.1126/science.1133234 PubMed DOI

Celic I, Masumoto H, Griffith WP, Meluh P, Cotter RJ, Boeke JD, Verreault A. The sirtuins hst3 and Hst4p preserve genome integrity by controlling histone h3 lysine 56 deacetylation. Curr Biol 2006; 16:1280-9; PMID:16815704; http://dx.doi.org/10.1016/j.cub.2006.06.023 PubMed DOI

Maas NL, Miller KM, DeFazio LG, Toczyski DP. Cell cycle and checkpoint regulation of histone H3 K56 acetylation by Hst3 and Hst4. Mol Cell 2006; 23:109-19; PMID:16818235; http://dx.doi.org/10.1016/j.molcel.2006.06.006 PubMed DOI

Keck KM, Pemberton LF. Interaction with the histone chaperone Vps75 promotes nuclear localization and HAT activity of Rtt109 in vivo. Traffic 2011; 12:826-39; PMID:21463458; http://dx.doi.org/10.1111/j.1600-0854.2011.01202.x PubMed DOI PMC

Das C, Lucia MS, Hansen KC, Tyler JK. CBP/p300-mediated acetylation of histone H3 on lysine 56. Nature 2009; 459:113-7; PMID:19270680; http://dx.doi.org/10.1038/nature07861 PubMed DOI PMC

Li Y, Jaramillo-Lambert AN, Yang Y, Williams R, Lee NH, Zhu W. And-1 is required for the stability of histone acetyltransferase Gcn5. Oncogene 2012; 31:643-52; PMID:21725360 PubMed PMC

Filippakopoulos P, Picaud S, Mangos M, Keates T, Lambert JP, Barsyte-Lovejoy D, Felletar I, Volkmer R, Müller S, Pawson T, et al.. Histone recognition and large-scale structural analysis of the human bromodomain family. Cell 2012; 149:214-31; PMID:22464331; http://dx.doi.org/10.1016/j.cell.2012.02.013 PubMed DOI PMC

Black JC, Mosley A, Kitada T, Washburn M, Carey M. The SIRT2 deacetylase regulates autoacetylation of p300. Mol Cell 2008; 32:449-55; PMID:18995842; http://dx.doi.org/10.1016/j.molcel.2008.09.018 PubMed DOI PMC

Groth A, Ray-Gallet D, Quivy JP, Lukas J, Bartek J, Almouzni G. Human Asf1 regulates the flow of S phase histones during replicational stress. Mol Cell 2005; 17:301-11; PMID:15664198; http://dx.doi.org/10.1016/j.molcel.2004.12.018 PubMed DOI

Groth A, Rocha W, Verreault A, Almouzni G. Chromatin challenges during DNA replication and repair. Cell 2007; 128:721-33; PMID:17320509; http://dx.doi.org/10.1016/j.cell.2007.01.030 PubMed DOI

Michishita E, McCord RA, Boxer LD, Barber MF, Hong T, Gozani O, Chua KF. Cell cycle-dependent deacetylation of telomeric histone H3 lysine K56 by human SIRT6. Cell Cycle 2009; 8:2664-6; PMID:19625767; http://dx.doi.org/10.4161/cc.8.16.9367 PubMed DOI PMC

Hu C, Liu M, Zhang W, Xu Q, Ma K, Chen L, Wang Z, He S, Zhu H, Xu N. Upregulation of KLF4 by methylseleninic acid in human esophageal squamous cell carcinoma cells: Modification of histone H3 acetylation through HAT/HDAC interplay. Mol Carcinog 2014; 54(10):1051-9. PubMed

Im JS, Keaton M, Lee KY, Kumar P, Park J, Dutta A. ATR checkpoint kinase and CRL1βTRCP collaborate to degrade ASF1a and thus repress genes overlapping with clusters of stalled replication forks. Genes Dev 2014; 28:875-87; PMID:24700029; http://dx.doi.org/10.1101/gad.239194.114 PubMed DOI PMC

Armas-Pineda C, Arenas-Huertero F, Pérezpeñia-Diazconti M, Chico-Ponce de León F, Sosa-Sáinz G, Lezama P, Recillas-Targa F. Expression of PCAF, p300 and Gcn5 and more highly acetylated histone H4 in pediatric tumors. J Exp Clin Cancer Res 2007; 26:269-76; PMID:17725108 PubMed

Liu Y, Wang DL, Chen S, Zhao L, Sun FL. Oncogene Ras/phosphatidylinositol 3-kinase signaling targets histone H3 acetylation at lysine 56. J Biol Chem 2012; 287:41469-80; PMID:22982396; http://dx.doi.org/10.1074/jbc.M112.367847 PubMed DOI PMC

Xie W, Song C, Young NL, Sperling AS, Xu F, Sridharan R, Conway AE, Garcia BA, Plath K, Clark AT, et al.. Histone h3 lysine 56 acetylation is linked to the core transcriptional network in human embryonic stem cells. Mol Cell 2009; 33:417-27; PMID:19250903; http://dx.doi.org/10.1016/j.molcel.2009.02.004 PubMed DOI PMC

Stejskal S, Tesařová L, Koutná I. Mysterious Role of H3K56ac in Embryonic Stem Cells. Folia Biol (Praha) 2014; 60 Suppl 1:71-5; PMID:25369345 PubMed

Tjeertes JV, Miller KM, Jackson SP. Screen for DNA-damage-responsive histone modifications identifies H3K9Ac and H3K56Ac in human cells. EMBO J 2009; 28:1878-89; PMID:19407812; http://dx.doi.org/10.1038/emboj.2009.119 PubMed DOI PMC

Vempati RK, Jayani RS, Notani D, Sengupta A, Galande S, Haldar D. p300-mediated acetylation of histone H3 lysine 56 functions in DNA damage response in mammals. J Biol Chem 2010; 285:28553-64; PMID:20587414; http://dx.doi.org/10.1074/jbc.M110.149393 PubMed DOI PMC

Yuan J, Pu M, Zhang Z, Lou Z. Histone H3-K56 acetylation is important for genomic stability in mammals. Cell Cycle 2009; 8:1747-53; PMID:19411844; http://dx.doi.org/10.4161/cc.8.11.8620 PubMed DOI PMC

Drogaris P, Villeneuve V, Pomiès C, Lee EH, Bourdeau V, Bonneil E, Ferbeyre G, Verreault A, Thibault P. Histone deacetylase inhibitors globally enhance h3/h4 tail acetylation without affecting h3 lysine 56 acetylation. Sci Rep 2012; 2:220; PMID:22355734; http://dx.doi.org/10.1038/srep00220 PubMed DOI PMC

Krutá M, Bálek L, Hejnová R, Dobšáková Z, Eiselleová L, Matulka K, Bárta T, Fojtík P, Fajkus J, Hampl A, et al.. Decrease in abundance of apurinic/apyrimidinic endonuclease causes failure of base excision repair in culture-adapted human embryonic stem cells. Stem Cells 2013; 31:693-702; http://dx.doi.org/10.1002/stem.1312 PubMed DOI

Kunova M, Matulka K, Eiselleova L, Salykin A, Kubikova I, Kyrylenko S, Hampl A, Dvorak P. Adaptation to robust monolayer expansion produces human pluripotent stem cells with improved viability. Stem Cells Transl Med 2013; 2:246-54; PMID:23486835; http://dx.doi.org/10.5966/sctm.2012-0081 PubMed DOI PMC

Outeiro TF, Kontopoulos E, Altmann SM, Kufareva I, Strathearn KE, Amore AM, Volk CB, Maxwell MM, Rochet JC, McLean PJ, et al.. Sirtuin 2 inhibitors rescue α-synuclein-mediated toxicity in models of Parkinson disease. Science 2007; 317:516-9; PMID:17588900; http://dx.doi.org/10.1126/science.1143780 PubMed DOI

Bitterman KJ, Anderson RM, Cohen HY, Latorre-Esteves M, Sinclair DA. Inhibition of silencing and accelerated aging by nicotinamide, a putative negative regulator of yeast sir2 and human SIRT1. J Biol Chem 2002; 277:45099-107; PMID:12297502; http://dx.doi.org/10.1074/jbc.M205670200 PubMed DOI

North BJ, Marshall BL, Borra MT, Denu JM, Verdin E. The human Sir2 ortholog, SIRT2, is an NAD+-dependent tubulin deacetylase. Mol Cell 2003; 11:437-44; PMID:12620231; http://dx.doi.org/10.1016/S1097-2765(03)00038-8 PubMed DOI

Yang B, Zwaans BM, Eckersdorff M, Lombard DB. The sirtuin SIRT6 deacetylates H3 K56Ac in vivo to promote genomic stability. Cell Cycle 2009; 8:2662-3; PMID:19597350; http://dx.doi.org/10.4161/cc.8.16.9329 PubMed DOI PMC

Borra MT, Smith BC, Denu JM. Mechanism of human SIRT1 activation by resveratrol. J Biol Chem 2005; 280:17187-95; PMID:15749705; http://dx.doi.org/10.1074/jbc.M501250200 PubMed DOI

Bowers EM, Yan G, Mukherjee C, Orry A, Wang L, Holbert MA, Crump NT, Hazzalin CA, Liszczak G, Yuan H, et al.. Virtual ligand screening of the p300/CBP histone acetyltransferase: identification of a selective small molecule inhibitor. Chem Biol 2010; 17:471-82; PMID:20534345; http://dx.doi.org/10.1016/j.chembiol.2010.03.006 PubMed DOI PMC

Nguyen VT, Giannoni F, Dubois MF, Seo SJ, Vigneron M, Kédinger C, Bensaude O. In vivo degradation of RNA polymerase II largest subunit triggered by α-amanitin. Nucleic Acids Res 1996; 24:2924-9; PMID:8760875; http://dx.doi.org/10.1093/nar/24.15.2924 PubMed DOI PMC

Gu B, Watanabe K, Dai X. Pygo2 regulates histone gene expression and H3 K56 acetylation in human mammary epithelial cells. Cell Cycle 2012; 11:79-87; PMID:22186018; http://dx.doi.org/10.4161/cc.11.1.18402 PubMed DOI PMC

Bártová E, Galiová G, Krejcí J, Harnicarová A, Strasák L, Kozubek S. Epigenome and chromatin structure in human embryonic stem cells undergoing differentiation. Dev Dyn 2008; 237:3690-702; http://dx.doi.org/10.1002/dvdy.21773 PubMed DOI

Meshorer E, Yellajoshula D, George E, Scambler PJ, Brown DT, Misteli T. Hyperdynamic plasticity of chromatin proteins in pluripotent embryonic stem cells. Dev Cell 2006; 10:105-16; PMID:16399082; http://dx.doi.org/10.1016/j.devcel.2005.10.017 PubMed DOI PMC

Barta T, Dolezalova D, Holubcova Z, Hampl A. Cell cycle regulation in human embryonic stem cells: links to adaptation to cell culture. Exp Biol Med (Maywood) 2013; 238:271-5; PMID:23598972; http://dx.doi.org/10.1177/1535370213480711 PubMed DOI

Zhang L, Eugeni EE, Parthun MR, Freitas MA. Identification of novel histone post-translational modifications by peptide mass fingerprinting. Chromosoma 2003; 112:77-86; PMID:12937907; http://dx.doi.org/10.1007/s00412-003-0244-6 PubMed DOI

Horwitz GA, Zhang K, McBrian MA, Grunstein M, Kurdistani SK, Berk AJ. Adenovirus small e1a alters global patterns of histone modification. Science 2008; 321:1084-5; PMID:18719283; http://dx.doi.org/10.1126/science.1155544 PubMed DOI PMC

O'Sullivan RJ, Kubicek S, Schreiber SL, Karlseder J. Reduced histone biosynthesis and chromatin changes arising from a damage signal at telomeres. Nat Struct Mol Biol 2010; 17:1218-25; PMID:20890289; http://dx.doi.org/10.1038/nsmb.1897 PubMed DOI PMC

Yu Y, Song C, Zhang Q, DiMaggio PA, Garcia BA, York A, Carey MF, Grunstein M. Histone H3 lysine 56 methylation regulates DNA replication through its interaction with PCNA. Mol Cell 2012; 46:7-17; PMID:22387026; http://dx.doi.org/10.1016/j.molcel.2012.01.019 PubMed DOI PMC

Li B, Su T, Ferrari R, Li JY, Kurdistani SK. A unique epigenetic signature is associated with active DNA replication loci in human embryonic stem cells. Epigenetics 2014; 9:257-67; PMID:24172870; http://dx.doi.org/10.4161/epi.26870 PubMed DOI PMC

Prieur A, Besnard E, Babled A, Lemaitre JM. p53 and p16(INK4A) independent induction of senescence by chromatin-dependent alteration of S-phase progression. Nat Commun 2011; 2:473; PMID:21915115; http://dx.doi.org/10.1038/ncomms1473 PubMed DOI

Sajish M, Schimmel P. A human tRNA synthetase is a potent PARP1-activating effector target for resveratrol. Nature 2015; 519:370-3; PMID:25533949; http://dx.doi.org/10.1038/nature14028 PubMed DOI PMC

Wang X, Pan L, Feng Y, Wang Y, Han Q, Han L, Han S, Guo J, Huang B, Lu J. P300 plays a role in p16(INK4a) expression and cell cycle arrest. Oncogene 2008; 27:1894-904; PMID:17906698; http://dx.doi.org/10.1038/sj.onc.1210821 PubMed DOI

Peck B, Chen CY, Ho KK, Di Fruscia P, Myatt SS, Coombes RC, Fuchter MJ, Hsiao CD, Lam EW. SIRT inhibitors induce cell death and p53 acetylation through targeting both SIRT1 and SIRT2. Mol Cancer Ther 2010; 9:844-55; PMID:20371709; http://dx.doi.org/10.1158/1535-7163.MCT-09-0971 PubMed DOI

Fu M, Wang C, Rao M, Wu X, Bouras T, Zhang X, Li Z, Jiao X, Yang J, Li A, et al.. Cyclin D1 represses p300 transactivation through a cyclin-dependent kinase-independent mechanism. J Biol Chem 2005; 280:29728-42; PMID:15951563; http://dx.doi.org/10.1074/jbc.M503188200 PubMed DOI

Byun JS, Wong MM, Cui W, Idelman G, Li Q, De Siervi A, Bilke S, Haggerty CM, Player A, Wang YH, et al.. Dynamic bookmarking of primary response genes by p300 and RNA polymerase II complexes. Proc Natl Acad Sci U S A 2009; 106:19286-91; PMID:19880750; http://dx.doi.org/10.1073/pnas.0905469106 PubMed DOI PMC

Mandal P, Verma N, Chauhan S, Tomar RS. Unexpected histone H3 tail-clipping activity of glutamate dehydrogenase. J Biol Chem 2013; 288:18743-57; PMID:23673664; http://dx.doi.org/10.1074/jbc.M113.462531 PubMed DOI PMC

Jack AP, Bussemer S, Hahn M, Pünzeler S, Snyder M, Wells M, Csankovszki G, Solovei I, Schotta G, Hake SB. H3K56me3 is a novel, conserved heterochromatic mark that largely but not completely overlaps with H3K9me3 in both regulation and localization. PLoS One 2013; 8:e51765; PMID:23451023; http://dx.doi.org/10.1371/journal.pone.0051765 PubMed DOI PMC

Chao SH, Greenleaf AL, Price DH. Juglone, an inhibitor of the peptidyl-prolyl isomerase Pin1, also directly blocks transcription. Nucleic Acids Res 2001; 29:767-73; PMID:11160900; http://dx.doi.org/10.1093/nar/29.3.767 PubMed DOI PMC

Tan Y, Xue Y, Song C, Grunstein M. Acetylated histone H3K56 interacts with Oct4 to promote mouse embryonic stem cell pluripotency. Proc Natl Acad Sci U S A 2013; 110:11493-8; PMID:23798425; http://dx.doi.org/10.1073/pnas.1309914110 PubMed DOI PMC

Shechter D, Dormann HL, Allis CD, Hake SB. Extraction, purification and analysis of histones. Nat Protoc 2007; 2:1445-57; PMID:17545981; http://dx.doi.org/10.1038/nprot.2007.202 PubMed DOI

Rodriguez-Collazo P, Leuba SH, Zlatanova J. Robust methods for purification of histones from cultured mammalian cells with the preservation of their native modifications. Nucleic Acids Res 2009; 37:e81; PMID:19443446; http://dx.doi.org/10.1093/nar/gkp273 PubMed DOI PMC

Wiśniewski JR, Zougman A, Mann M. Combination of FASP and StageTip-based fractionation allows in-depth analysis of the hippocampal membrane proteome. J Proteome Res 2009; 8:5674-8; PMID:19848406; http://dx.doi.org/10.1021/pr900748n PubMed DOI

Činčárová L, Lochmanová G, Nováková K, Šultesová P, Konečná H, Fajkusová L, Fajkus J, Zdráhal Z. A combined approach for the study of histone deacetylase inhibitors. Mol Biosyst 2012; 8:2937-45; http://dx.doi.org/10.1039/c2mb25136a PubMed DOI

MacLean B, Tomazela DM, Shulman N, Chambers M, Finney GL, Frewen B, Kern R, Tabb DL, Liebler DC, MacCoss MJ. Skyline: an open source document editor for creating and analyzing targeted proteomics experiments. Bioinformatics 2010; 26:966-8; PMID:20147306; http://dx.doi.org/10.1093/bioinformatics/btq054 PubMed DOI PMC

Raimondo F, Gavrielides M, Karayannopoulou G, Lyroudia K, Pitas I, Kostopoulos I. utomated evaluation of HER-2/neu status in breast tissue from fluorescent in situ hybridization images. IEEE Trans Image Process 2005; 14:1288-99; PMID:16190465; http://dx.doi.org/10.1109/TIP.2005.852806 PubMed DOI

Matula P, Verissimo F, Wörz S, Eils R, Pepperkok R, Rohr K. Quantification of fluorescent spots in time series of 3-D confocal microscopy images of endoplasmic reticulum exit sites based on the HMAX transform. San Diego: SPIE, 2010.

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