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Acetylation regulates DNA repair mechanisms in human cells

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Pages 1506-1517 | Received 12 Feb 2016, Accepted 06 Apr 2016, Published online: 18 May 2016

References

  • Spange S, Wagner T, Heinzel T, Kramer OH. Acetylation of non-histone proteins modulates cellular signalling at multiple levels. Int J Biochem Cell Biol 2009; 41:185-98; PMID:18804549; http://dx.doi.org/10.1016/j.biocel.2008.08.027
  • Glozak MA, Sengupta N, Zhang X, Seto E. Acetylation and deacetylation of non-histone proteins. Gene 2005; 363:15-23; PMID:16289629; http://dx.doi.org/10.1016/j.gene.2005.09.010
  • Sadoul K, Wang J, Diagouraga B, Khochbin S. The tale of protein lysine acetylation in the cytoplasm. J Biomed Biotechnol 2011; 2011:970382; PMID:21151618; http://dx.doi.org/10.1155/2011/970382
  • Timmermann S, Lehrmann H, Polesskaya A, Harel-Bellan A. Histone acetylation and disease. Cell Mol Life Sci 2001; 58:728-36; PMID:11437234; http://dx.doi.org/10.1007/PL00000896
  • Xu W, Li Y, Liu C, Zhao S. Protein lysine acetylation guards metabolic homeostasis to fight against cancer. Oncogene 2014; 33:2279-85; PMID:23665675; http://dx.doi.org/10.1038/onc.2013.163
  • Iyer NG, Chin SF, Ozdag H, Daigo Y, Hu DE, Cariati M, Brindle K, Aparicio S, Caldas C. p300 regulates p53-dependent apoptosis after DNA damage in colorectal cancer cells by modulation of PUMA/p21 levels. Proc Natl Acad Sci U S A 2004; 101:7386-91; PMID:15123817; http://dx.doi.org/10.1073/pnas.0401002101
  • Yang MH, Nickerson S, Kim ET, Liot C, Laurent G, Spang R, Philips MR, Shan Y, Shaw DE, Bar-Sagi D, et al. Regulation of RAS oncogenicity by acetylation. Proc Natl Acad Sci U S A 2012; 109:10843-8; PMID:22711838; http://dx.doi.org/10.1073/pnas.1201487109
  • Dresler SL. Stimulation of deoxyribonucleic acid excision repair in human fibroblasts pretreated with sodium butyrate. Biochemistry 1985; 24:6861-9; PMID:4074730; http://dx.doi.org/10.1021/bi00345a019
  • Smith PJ. n-Butyrate alters chromatin accessibility to DNA repair enzymes. Carcinogenesis 1986; 7:423-9; PMID:3753905; http://dx.doi.org/10.1093/carcin/7.3.423
  • Smerdon MJ, Lan SY, Calza RE, Reeves R. Sodium butyrate stimulates DNA repair in UV-irradiated normal and xeroderma pigmentosum human fibroblasts. J Biol Chem 1982; 257:13441-7; PMID:7142158
  • Bird AW, Yu DY, Pray-Grant MG, Qiu Q, Harmon KE, Megee PC, Grant PA, Smith MM, Christman MF. Acetylation of histone H4 by Esa1 is required for DNA double-strand break repair. Nature 2002; 419:411-5; PMID:12353039; http://dx.doi.org/10.1038/nature01035
  • Megee PC, Morgan BA, Smith MM. Histone H4 and the maintenance of genome integrity. Genes Dev 1995; 9:1716-27; PMID:7622036; http://dx.doi.org/10.1101/gad.9.14.1716
  • Squatrito M, Gorrini C, Amati B. Tip60 in DNA damage response and growth control: many tricks in one HAT. Trends Cell Biol 2006; 16:433-42; PMID:16904321; http://dx.doi.org/10.1016/j.tcb.2006.07.007
  • Hasan S, El-Andaloussi N, Hardeland U, Hassa PO, Burki C, Imhof R, Schar P, Hottiger MO. Acetylation regulates the DNA end-trimming activity of DNA polymerase beta. Mol Cell 2002; 10:1213-22; PMID:12453427; http://dx.doi.org/10.1016/S1097-2765(02)00745-1
  • Muftuoglu M, Kusumoto R, Speina E, Beck G, Cheng WH, Bohr VA. Acetylation regulates WRN catalytic activities and affects base excision DNA repair. PLoS One 2008; 3:e1918; PMID:18398454; http://dx.doi.org/10.1371/journal.pone.0001918
  • Balakrishnan L, Stewart J, Polaczek P, Campbell JL, Bambara RA. Acetylation of Dna2 endonuclease/helicase and flap endonuclease 1 by p300 promotes DNA stability by creating long flap intermediates. J Biol Chem 2010; 285:4398-404; PMID:20019387; http://dx.doi.org/10.1074/jbc.M109.086397
  • Naryzhny SN, Lee H. The post-translational modifications of proliferating cell nuclear antigen: acetylation, not phosphorylation, plays an important role in the regulation of its function. J Biol Chem 2004; 279:20194-9; PMID:14988403; http://dx.doi.org/10.1074/jbc.M312850200
  • Hasan S, Stucki M, Hassa PO, Imhof R, Gehrig P, Hunziker P, Hubscher U, Hottiger MO. Regulation of human flap endonuclease-1 activity by acetylation through the transcriptional coactivator p300. Mol Cell 2001; 7:1221-31; PMID:11430825; http://dx.doi.org/10.1016/S1097-2765(01)00272-6
  • Zhang M, Xiang S, Joo HY, Wang L, Williams KA, Liu W, Hu C, Tong D, Haakenson J, Wang C, et al. HDAC6 deacetylates and ubiquitinates MSH2 to maintain proper levels of MutSalpha. Mol Cell 2014; 55:31-46; PMID:24882211; http://dx.doi.org/10.1016/j.molcel.2014.04.028
  • Radhakrishnan R, Li Y, Xiang S, Yuan F, Yuan Z, Telles E, Fang J, Coppola D, Shibata D, Lane WS, et al. Histone deacetylase 10 regulates DNA mismatch repair and may involve the deacetylation of MutS homolog 2. J Biol Chem 2015; 290:22795-804; PMID:26221039; http://dx.doi.org/10.1074/jbc.M114.612945
  • Goellner EM, Smith CE, Campbell CS, Hombauer H, Desai A, Putnam CD, Kolodner RD. PCNA and Msh2-Msh6 activate an Mlh1-Pms1 endonuclease pathway required for Exo1-independent mismatch repair. Mol Cell 2014; 55:291-304; PMID:24981171; http://dx.doi.org/10.1016/j.molcel.2014.04.034
  • Smith CE, Bowen N, Graham WJt, Goellner EM, Srivatsan A, Kolodner RD. Activation of saccharomyces cerevisiae Mlh1-Pms1 endonuclease in a reconstituted mismatch repair system. J Biol Chem 2015; 290:21580-90; PMID:26170454; http://dx.doi.org/10.1074/jbc.M115.662189
  • Desai A, Gerson S. Exo1 independent DNA mismatch repair involves multiple compensatory nucleases. DNA Repair (Amst) 2014; 21:55-64; PMID:25037770; http://dx.doi.org/10.1016/j.dnarep.2014.06.005
  • Goellner EM, Putnam CD, Kolodner RD. Exonuclease 1-dependent and independent mismatch repair. DNA Repair (Amst) 2015; 32:24-32; PMID:25956862; http://dx.doi.org/10.1016/j.dnarep.2015.04.010
  • Lei X, Zhu Y, Tomkinson A, Sun L. Measurement of DNA mismatch repair activity in live cells. Nucleic Acids Res 2004; 32:e100; PMID:15249596; http://dx.doi.org/10.1093/nar/gnh098
  • Kadyrov FA, Genschel J, Fang Y, Penland E, Edelmann W, Modrich P. A possible mechanism for exonuclease 1-independent eukaryotic mismatch repair. Proc Natl Acad Sci U S A 2009; 106:8495-500; PMID:19420220; http://dx.doi.org/10.1073/pnas.0903654106
  • Sattler U, Frit P, Salles B, Calsou P. Long-patch DNA repair synthesis during base excision repair in mammalian cells. EMBO Rep 2003; 4:363-7; PMID:12671676; http://dx.doi.org/10.1038/sj.embor.embor796
  • Tornaletti S, Maeda LS, Kolodner RD, Hanawalt PC. Effect of 8-oxoguanine on transcription elongation by T7 RNA polymerase and mammalian RNA polymerase II. DNA Repair (Amst) 2004; 3:483-94; PMID:15084310; http://dx.doi.org/10.1016/j.dnarep.2004.01.003
  • Kathe SD, Shen GP, Wallace SS. Single-stranded breaks in DNA but not oxidative DNA base damages block transcriptional elongation by RNA polymerase II in HeLa cell nuclear extracts. J Biol Chem 2004; 279:18511-20; PMID:14978042; http://dx.doi.org/10.1074/jbc.M313598200
  • Kitsera N, Stathis D, Luhnsdorf B, Muller H, Carell T, Epe B, Khobta A. 8-Oxo-7,8-dihydroguanine in DNA does not constitute a barrier to transcription, but is converted into transcription-blocking damage by OGG1. Nucleic Acids Res 2011; 39:5926-34; PMID:21441539; http://dx.doi.org/10.1093/nar/gkr163
  • Brand M, Moggs JG, Oulad-Abdelghani M, Lejeune F, Dilworth FJ, Stevenin J, Almouzni G, Tora L. UV-damaged DNA-binding protein in the TFTC complex links DNA damage recognition to nucleosome acetylation. EMBO J 2001; 20:3187-96; PMID:11406595; http://dx.doi.org/10.1093/emboj/20.12.3187
  • Jeong S, Stein A. Micrococcal nuclease digestion of nuclei reveals extended nucleosome ladders having anomalous DNA lengths for chromatin assembled on non-replicating plasmids in transfected cells. Nucleic Acids Res 1994; 22:370-5; PMID:7510391; http://dx.doi.org/10.1093/nar/22.3.370
  • Pluciennik A, Dzantiev L, Iyer RR, Constantin N, Kadyrov FA, Modrich P. PCNA function in the activation and strand direction of MutLalpha endonuclease in mismatch repair. Proc Natl Acad Sci U S A 2010; 107:16066-71; PMID:20713735; http://dx.doi.org/10.1073/pnas.1010662107
  • Dherin C, Gueneau E, Francin M, Nunez M, Miron S, Liberti SE, Rasmussen LJ, Zinn-Justin S, Gilquin B, Charbonnier JB, et al. Characterization of a highly conserved binding site of Mlh1 required for exonuclease I-dependent mismatch repair. Mol Cell Biol 2009; 29:907-18; PMID:19015241; http://dx.doi.org/10.1128/MCB.00945-08
  • Balasubramanyam K, Altaf M, Varier RA, Swaminathan V, Ravindran A, Sadhale PP, Kundu TK. Polyisoprenylated benzophenone, garcinol, a natural histone acetyltransferase inhibitor, represses chromatin transcription and alters global gene expression. J Biol Chem 2004; 279:33716-26; PMID:15155757; http://dx.doi.org/10.1074/jbc.M402839200
  • Oike T, Ogiwara H, Torikai K, Nakano T, Yokota J, Kohno T. Garcinol, a histone acetyltransferase inhibitor, radiosensitizes cancer cells by inhibiting non-homologous end joining. Int J Radiat Oncol Biol Phys 2012; 84:815-21; PMID:22417805; http://dx.doi.org/10.1016/j.ijrobp.2012.01.017
  • Bhakat KK, Hazra TK, Mitra S. Acetylation of the human DNA glycosylase NEIL2 and inhibition of its activity. Nucleic Acids Res 2004; 32:3033-9; PMID:15175427; http://dx.doi.org/10.1093/nar/gkh632
  • Bhakat KK, Mokkapati SK, Boldogh I, Hazra TK, Mitra S. Acetylation of human 8-oxoguanine-DNA glycosylase by p300 and its role in 8-oxoguanine repair in vivo. Mol Cell Biol 2006; 26:1654-65; PMID:16478987; http://dx.doi.org/10.1128/MCB.26.5.1654-1665.2006
  • Hasan S, Hassa PO, Imhof R, Hottiger MO. Transcription coactivator p300 binds PCNA and may have a role in DNA repair synthesis. Nature 2001; 410:387-91; PMID:11268218; http://dx.doi.org/10.1038/35066610
  • Cazzalini O, Sommatis S, Tillhon M, Dutto I, Bachi A, Rapp A, Nardo T, Scovassi AI, Necchi D, Cardoso MC, et al. CBP and p300 acetylate PCNA to link its degradation with nucleotide excision repair synthesis. Nucleic Acids Res 2014; 42:8433-48; PMID:24939902; http://dx.doi.org/10.1093/nar/gku533
  • Tillhon M, Cazzalini O, Nardo T, Necchi D, Sommatis S, Stivala LA, Scovassi AI, Prosperi E. p300/CBP acetyl transferases interact with and acetylate the nucleotide excision repair factor XPG. DNA Repair (Amst) 2012; 11:844-52; PMID:22954786; http://dx.doi.org/10.1016/j.dnarep.2012.08.001
  • Tini M, Benecke A, Um SJ, Torchia J, Evans RM, Chambon P. Association of CBP/p300 acetylase and thymine DNA glycosylase links DNA repair and transcription. Mol Cell 2002; 9:265-77; PMID:11864601; http://dx.doi.org/10.1016/S1097-2765(02)00453-7
  • Wu Y, Chen H, Lu J, Zhang M, Zhang R, Duan T, Wang X, Huang J, Kang T. Acetylation-dependent function of human single-stranded DNA binding protein 1. Nucleic Acids Res 2015; 43:7878-87; PMID:26170237; http://dx.doi.org/10.1093/nar/gkv707
  • Kadyrov FA, Dzantiev L, Constantin N, Modrich P. Endonucleolytic function of MutLalpha in human mismatch repair. Cell 2006; 126:297-308; PMID:16873062; http://dx.doi.org/10.1016/j.cell.2006.05.039
  • Genschel J, Modrich P. Mechanism of 5'-directed excision in human mismatch repair. Mol Cell 2003; 12:1077-86; PMID:14636568; http://dx.doi.org/10.1016/S1097-2765(03)00428-3
  • Zhang Y, Yuan F, Presnell SR, Tian K, Gao Y, Tomkinson AE, Gu L, Li GM. Reconstitution of 5'-directed human mismatch repair in a purified system. Cell 2005; 122:693-705; PMID:16143102; http://dx.doi.org/10.1016/j.cell.2005.06.027
  • Ramanathan B, Smerdon MJ. Enhanced DNA repair synthesis in hyperacetylated nucleosomes. J Biol Chem 1989; 264:11026-34; PMID:2738057.
  • Krishnan V, Liu B, Zhou Z. 'Relax and Repair' to restrain aging. Aging (Albany NY) 2011; 3:943-54; PMID:22067432; http://dx.doi.org/10.18632/aging.100399
  • Zhang W, Wu H, Yang M, Ye S, Li L, Zhang H, Hu J, Wang X, Xu J, Liang A. SIRT1 inhibition impairs non-homologous end joining DNA damage repair by increasing Ku70 acetylation in chronic myeloid leukemia cells. Oncotarget 2015 Dec 3; [Epub ahead of print]; PMID:26646449; http://dx.doi.org/10.18632/oncotarget.6455
  • Johnson DP, Spitz GS, Tharkar S, Quayle SN, Shearstone JR, Jones S, McDowell ME, Wellman H, Tyler JK, Cairns BR, et al. HDAC1,2 inhibition impairs EZH2- and BBAP-mediated DNA repair to overcome chemoresistance in EZH2 gain-of-function mutant diffuse large B-cell lymphoma. Oncotarget 2015; 6:4863-87; PMID:25605023; http://dx.doi.org/10.18632/oncotarget.3120
  • Balakrishnan L, Bambara RA. Okazaki fragment metabolism. Cold Spring Harb Perspect Biol 2013; 5:a010173; PMID:23378587; http://dx.doi.org/10.1101/cshperspect.a010173
  • Choudhary C, Kumar C, Gnad F, Nielsen ML, Rehman M, Walther TC, Olsen JV, Mann M. Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science 2009; 325:834-40; PMID:19608861; http://dx.doi.org/10.1126/science.1175371
  • Balakrishnan L, Bambara RA. Eukaryotic lagging strand DNA replication employs a multi-pathway mechanism that protects genome integrity. J Biol Chem 2011; 286:6865-70; PMID:21177245; http://dx.doi.org/10.1074/jbc.R110.209502
  • Balakrishnan L, Bambara RA. Flap endonuclease 1. Annu Rev Biochem 2013; 82:119-38; PMID:23451868; http://dx.doi.org/10.1146/annurev-biochem-072511-122603
  • Reijns MA, Kemp H, Ding J, de Proce SM, Jackson AP, Taylor MS. Lagging-strand replication shapes the mutational landscape of the genome. Nature 2015; 518:502-6; PMID:25624100; http://dx.doi.org/10.1038/nature14183
  • Hombauer H, Campbell CS, Smith CE, Desai A, Kolodner RD. Visualization of eukaryotic DNA mismatch repair reveals distinct recognition and repair intermediates. Cell 2011; 147:1040-53; PMID:22118461; http://dx.doi.org/10.1016/j.cell.2011.10.025
  • Masih PJ, Kunnev D, Melendy T. Mismatch Repair proteins are recruited to replicating DNA through interaction with Proliferating Cell Nuclear Antigen (PCNA). Nucleic Acids Res 2008; 36:67-75; PMID:17984070; http://dx.doi.org/10.1093/nar/gkm943
  • Constantin N, Dzantiev L, Kadyrov FA, Modrich P. Human mismatch repair: reconstitution of a nick-directed bidirectional reaction. J Biol Chem 2005; 280:39752-61; PMID:16188885; http://dx.doi.org/10.1074/jbc.M509701200
  • Mokkapati SK, Wiederhold L, Hazra TK, Mitra S. Stimulation of DNA glycosylase activity of OGG1 by NEIL1: functional collaboration between two human DNA glycosylases. Biochemistry 2004; 43:11596-604; PMID:15350146; http://dx.doi.org/10.1021/bi049097i
  • Hegde ML, Hazra TK, Mitra S. Early steps in the DNA base excision/single-strand interruption repair pathway in mammalian cells. Cell Res 2008; 18:27-47; PMID:18166975; http://dx.doi.org/10.1038/cr.2008.8

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