Double duty: ZMYND8 in the DNA damage response and cancer

References

• Jackson SP, Bartek J. The DNA-damage response in human biology and disease. Nature. 2009;461:1071–8. doi:10.1038/nature08467. PMID:19847258
   PubMed Web of Science ®Google Scholar
• Ciccia A, Elledge SJ. The DNA damage response: making it safe to play with knives. Mol Cell. 2010;40:179–204. doi:10.1016/j.molcel.2010.09.019. PMID:20965415
   PubMed Web of Science ®Google Scholar
• Lukas J, Lukas C, Bartek J. More than just a focus: The chromatin response to DNA damage and its role in genome integrity maintenance. Nat Cell Biol. 2011;13:1161–9. doi:10.1038/ncb2344. PMID:21968989
   PubMed Web of Science ®Google Scholar
• Miller KM, Jackson SP. Histone marks: repairing DNA breaks within the context of chromatin. Biochem Soc Trans. 2012;40:370–6. doi:10.1042/BST20110747. PMID:22435814
   PubMed Web of Science ®Google Scholar
• Jackson SP, Durocher D. Regulation of DNA damage responses by ubiquitin and SUMO. Mol Cell. 2013;49:795–807. doi:10.1016/j.molcel.2013.01.017. PMID:23416108
   PubMed Web of Science ®Google Scholar
• Gong F, Miller KM. Mammalian DNA repair: HATs and HDACs make their mark through histone acetylation. Mutat Res. 2013;750:23–30. doi:10.1016/j.mrfmmm.2013.07.002. PMID:23927873
   PubMed Web of Science ®Google Scholar
• Gong F, Chiu LY, Miller KM. Acetylation reader proteins: linking acetylation signaling to genome maintenance and cancer. PLoS Genet. 2016;12:e1006272. doi:10.1371/journal.pgen.1006272. PMID:27631103
   PubMed Web of Science ®Google Scholar
• Agarwal P, Miller KM. The nucleosome: orchestrating DNA damage signaling and repair within chromatin. Biochem Cell Biol. 2016;94:381–95. doi:10.1139/bcb-2016-0017. PMID:27240007
   PubMedGoogle Scholar
• Polo SE, Jackson SP. Dynamics of DNA damage response proteins at DNA breaks: a focus on protein modifications. Genes Dev. 2011;25:409–33. doi:10.1101/gad.2021311. PMID:21363960
   PubMed Web of Science ®Google Scholar
• Negrini S, Gorgoulis VG, Halazonetis TD. Genomic instability–an evolving hallmark of cancer. Nat Rev Mol Cell Biol. 2010;11:220–8. doi:10.1038/nrm2858. PMID:20177397
   PubMed Web of Science ®Google Scholar
• Suganuma T, Workman JL. Signals and combinatorial functions of histone modifications. Annu Rev Biochem. 2011;80:473–99. doi:10.1146/annurev-biochem-061809-175347. PMID:21529160
   PubMed Web of Science ®Google Scholar
• Kouzarides T. Chromatin modifications and their function. Cell. 2007;128:693–705. doi:10.1016/j.cell.2007.02.005. PMID:17320507
   PubMed Web of Science ®Google Scholar
• Weake VM, Workman JL. Histone ubiquitination: triggering gene activity. Mol Cell. 2008;29:653–63. doi:10.1016/j.molcel.2008.02.014. PMID:18374642
   PubMed Web of Science ®Google Scholar
• Campos EI, Reinberg D. Histones: annotating chromatin. Annu Rev Genet. 2009;43:559–99. doi:10.1146/annurev.genet.032608.103928. PMID:19886812
   PubMed Web of Science ®Google Scholar
• Polo SE, Almouzni G. DNA damage leaves its mark on chromatin. Cell Cycle. 2007;6:2355–9. doi:10.4161/cc.6.19.4756. PMID:17703111
   PubMed Web of Science ®Google Scholar
• Shahbazian MD, Grunstein M. Functions of site-specific histone acetylation and deacetylation. Annu Rev Biochem. 2007;76:75–100. doi:10.1146/annurev.biochem.76.052705.162114. PMID:17362198
   PubMed Web of Science ®Google Scholar
• Ruthenburg AJ, Li H, Patel DJ, et al. Multivalent engagement of chromatin modifications by linked binding modules. Nat Rev Mol Cell Biol. 2007;8:983–94. doi:10.1038/nrm2298. PMID:18037899
   PubMed Web of Science ®Google Scholar
• Musselman CA, Lalonde ME, Cote J, et al. Perceiving the epigenetic landscape through histone readers. Nat Struct Mol Biol. 2012;19:1218–27. doi:10.1038/nsmb.2436. PMID:23211769
   PubMed Web of Science ®Google Scholar
• Xu Y, Price BD. Chromatin dynamics and the repair of DNA double strand breaks. Cell Cycle. 2011;10:261–7. doi:10.4161/cc.10.2.14543. PMID:21212734
   PubMed Web of Science ®Google Scholar
• Seeber A, Dion V, Gasser SM. Remodelers move chromatin in response to DNA damage. Cell Cycle. 2014;13:877–8. doi:10.4161/cc.28200. PMID:24552812
   PubMed Web of Science ®Google Scholar
• Rogakou EP, Pilch DR, Orr AH, et al. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J Biol Chem. 1998;273:5858–68. doi:10.1074/jbc.273.10.5858. PMID:9488723
   PubMed Web of Science ®Google Scholar
• Stucki M, Clapperton JA, Mohammad D, et al. MDC1 directly binds phosphorylated histone H2AX to regulate cellular responses to DNA double-strand breaks. Cell. 2005;123:1213–26. doi:10.1016/j.cell.2005.09.038. PMID:16377563
   PubMed Web of Science ®Google Scholar
• Botuyan MV, Lee J, Ward IM, et al. Structural basis for the methylation state-specific recognition of histone H4-K20 by 53BP1 and Crb2 in DNA repair. Cell. 2006;127:1361–73. doi:10.1016/j.cell.2006.10.043. PMID:17190600
   PubMed Web of Science ®Google Scholar
• Fradet-Turcotte A, Canny MD, Escribano-Diaz C, et al. 53BP1 is a reader of the DNA-damage-induced H2A Lys 15 ubiquitin mark. Nature. 2013;499:50–4. doi:10.1038/nature12318. PMID:23760478
   PubMed Web of Science ®Google Scholar
• Dawson MA, Kouzarides T, Huntly BJ. Targeting epigenetic readers in cancer. N Engl J Med. 2012;367:647–57. doi:10.1056/NEJMra1112635. PMID:22894577
   PubMed Web of Science ®Google Scholar
• Fujisawa T, Filippakopoulos P. Functions of bromodomain-containing proteins and their roles in homeostasis and cancer. Nat Rev Mol Cell Biol. 2017;18:246–62. doi:10.1038/nrm.2016.143. PMID:28053347
   PubMed Web of Science ®Google Scholar
• Filippakopoulos P, Picaud S, Mangos M, et al. Histone recognition and large-scale structural analysis of the human bromodomain family. Cell. 2012;149:214–31. doi:10.1016/j.cell.2012.02.013. PMID:22464331
   PubMed Web of Science ®Google Scholar
• Filippakopoulos P, Knapp S. The bromodomain interaction module. FEBS Lett. 2012;586:2692–704. doi:10.1016/j.febslet.2012.04.045. PMID:22710155
   PubMed Web of Science ®Google Scholar
• Gong F, Chiu LY, Cox B, et al. Screen identifies bromodomain protein ZMYND8 in chromatin recognition of transcription-associated DNA damage that promotes homologous recombination. Genes Dev. 2015;29:197–211. doi:10.1101/gad.252189.114. PMID:25593309
   PubMed Web of Science ®Google Scholar
• Muller S, Filippakopoulos P, Knapp S. Bromodomains as therapeutic targets. Expert Rev Mol Med. 2011;13:e29. doi:10.1017/S1462399411001992. PMID:21933453
   PubMed Web of Science ®Google Scholar
• Barbieri I, Cannizzaro E, Dawson MA. Bromodomains as therapeutic targets in cancer. Brief Funct Genomics. 2013;12:219–30. doi:10.1093/bfgp/elt007. PMID:23543289
   PubMed Web of Science ®Google Scholar
• Zhang G, Smith SG, Zhou MM. Discovery of Chemical Inhibitors of Human Bromodomains. Chem Rev. 2015;115:11625–68. doi:10.1021/acs.chemrev.5b00205. PMID:26492937
   PubMed Web of Science ®Google Scholar
• Filippakopoulos P, Qi J, Picaud S, et al. Selective inhibition of BET bromodomains. Nature. 2010;468:1067–73. doi:10.1038/nature09504. PMID:20871596
   PubMed Web of Science ®Google Scholar
• Dawson MA, Prinjha RK, Dittmann A, et al. Inhibition of BET recruitment to chromatin as an effective treatment for MLL-fusion leukaemia. Nature. 2011;478:529–33. doi:10.1038/nature10509. PMID:21964340
   PubMed Web of Science ®Google Scholar
• Andrieu G, Belkina AC, Denis GV. Clinical trials for BET inhibitors run ahead of the science. Drug Discov Today Technol. 2016;19:45–50. doi:10.1016/j.ddtec.2016.06.004. PMID:27769357
   PubMedGoogle Scholar
• Boi M, Gaudio E, Bonetti P, et al. The BET Bromodomain Inhibitor OTX015 Affects Pathogenetic Pathways in Preclinical B-cell Tumor Models and Synergizes with Targeted Drugs. Clin Cancer Res. 2015;21:1628–38. doi:10.1158/1078-0432.CCR-14-1561. PMID:25623213
   PubMed Web of Science ®Google Scholar
• Adhikary S, Sanyal S, Basu M, et al. Selective Recognition of H3.1K36 Dimethylation/H4K16 Acetylation Facilitates the Regulation of All-trans-retinoic Acid (ATRA)-responsive Genes by Putative Chromatin Reader ZMYND8. J Biol Chem. 2016;291:2664–81. doi:10.1074/jbc.M115.679985. PMID:26655721
   PubMed Web of Science ®Google Scholar
• Shen H, Xu W, Guo R, et al. Suppression of Enhancer Overactivation by a RACK7-Histone Demethylase Complex. Cell. 2016;165:331–42. doi:10.1016/j.cell.2016.02.064. PMID:27058665
   PubMed Web of Science ®Google Scholar
• Li N, Li Y, Lv J, et al. ZMYND8 Reads the Dual Histone Mark H3K4me1-H3K14ac to Antagonize the Expression of Metastasis-Linked Genes. Mol Cell. 2016;63:470–84. doi:10.1016/j.molcel.2016.06.035. PMID:27477906
   PubMed Web of Science ®Google Scholar
• Savitsky P, Krojer T, Fujisawa T, et al. Multivalent Histone and DNA Engagement by a PHD/BRD/PWWP Triple Reader Cassette Recruits ZMYND8 to K14ac-Rich Chromatin. Cell Rep. 2016;17:2724–37. doi:10.1016/j.celrep.2016.11.014. PMID:27926874
   PubMed Web of Science ®Google Scholar
• Spruijt CG, Luijsterburg MS, Menafra R, et al. ZMYND8 Co-localizes with NuRD on Target Genes and Regulates Poly(ADP-Ribose)-Dependent Recruitment of GATAD2A/NuRD to Sites of DNA Damage. Cell Rep. 2016;17:783–98. doi:10.1016/j.celrep.2016.09.037. PMID:27732854
   PubMed Web of Science ®Google Scholar
• Gong F, Clouaire T, Aguirrebengoa M, et al. Histone demethylase KDM5A regulates the ZMYND8-NuRD chromatin remodeler to promote DNA repair. J Cell Biol. 2017;216:1959–74. doi:10.1083/jcb.201611135. PMID:28572115
   PubMed Web of Science ®Google Scholar
• Fossey SC, Kuroda S, Price JA, et al. Identification and characterization of PRKCBP1, a candidate RACK-like protein. Mamm Genome. 2000;11:919–25. doi:10.1007/s003350010174. PMID:11003709
   PubMed Web of Science ®Google Scholar
• Malovannaya A, Lanz RB, Jung SY, et al. Analysis of the human endogenous coregulator complexome. Cell. 2011;145:787–99. doi:10.1016/j.cell.2011.05.006. PMID:21620140
   PubMed Web of Science ®Google Scholar
• Eberl HC, Spruijt CG, Kelstrup CD, et al. A map of general and specialized chromatin readers in mouse tissues generated by label-free interaction proteomics. Mol Cell. 2013;49:368–78. doi:10.1016/j.molcel.2012.10.026. PMID:23201125
   PubMed Web of Science ®Google Scholar
• Nishibuchi G, Shibata Y, Hayakawa T, et al. Physical and functional interactions between the histone H3K4 demethylase KDM5A and the nucleosome remodeling and deacetylase (NuRD) complex. J Biol Chem. 2014;289:28956–70. doi:10.1074/jbc.M114.573725. PMID:25190814
   PubMed Web of Science ®Google Scholar
• Xia L, Huang W, Bellani M, et al. CHD4 Has Oncogenic Functions in Initiating and Maintaining Epigenetic Suppression of Multiple Tumor Suppressor Genes. Cancer Cell. 2017;31:653–68 e7. doi:10.1016/j.ccell.2017.04.005.
   Web of Science ®Google Scholar
• Sun Y, Jiang X, Price BD. Tip60: connecting chromatin to DNA damage signaling. Cell Cycle. 2010;9:930–6. doi:10.4161/cc.9.5.10931. PMID:20160506
   PubMed Web of Science ®Google Scholar
• Tang J, Cho NW, Cui G, et al. Acetylation limits 53BP1 association with damaged chromatin to promote homologous recombination. Nat Struct Mol Biol. 2013;20:317–25. doi:10.1038/nsmb.2499. PMID:23377543
   PubMed Web of Science ®Google Scholar
• Larsen DH, Poinsignon C, Gudjonsson T, et al. The chromatin-remodeling factor CHD4 coordinates signaling and repair after DNA damage. J Cell Biol. 2010;190:731–40. doi:10.1083/jcb.200912135. PMID:20805324
   PubMed Web of Science ®Google Scholar
• Smeenk G, Wiegant WW, Vrolijk H, et al. The NuRD chromatin-remodeling complex regulates signaling and repair of DNA damage. J Cell Biol. 2010;190:741–9. doi:10.1083/jcb.201001048. PMID:20805320
   PubMed Web of Science ®Google Scholar
• Chou DM, Adamson B, Dephoure NE, et al. A chromatin localization screen reveals poly (ADP ribose)-regulated recruitment of the repressive polycomb and NuRD complexes to sites of DNA damage. Proc Natl Acad Sci U S A. 2010;107:18475–80. doi:10.1073/pnas.1012946107. PMID:20937877
   PubMed Web of Science ®Google Scholar
• Polo SE, Kaidi A, Baskcomb L, et al. Regulation of DNA-damage responses and cell-cycle progression by the chromatin remodelling factor CHD4. EMBO J. 2010;29:3130–9. doi:10.1038/emboj.2010.188. PMID:20693977
   PubMed Web of Science ®Google Scholar
• Pan MR, Hsieh HJ, Dai H, et al. Chromodomain helicase DNA-binding protein 4 (CHD4) regulates homologous recombination DNA repair, and its deficiency sensitizes cells to poly(ADP-ribose) polymerase (PARP) inhibitor treatment. J Biol Chem. 2012;287:6764–72. doi:10.1074/jbc.M111.287037. PMID:22219182
   PubMed Web of Science ®Google Scholar
• Li DQ, Kumar R. Mi-2/NuRD complex making inroads into DNA-damage response pathway. Cell Cycle. 2010;9:2071–9. doi:10.4161/cc.9.11.11735. PMID:20505336
   PubMed Web of Science ®Google Scholar
• Shanbhag NM, Rafalska-Metcalf IU, Balane-Bolivar C, et al. ATM-dependent chromatin changes silence transcription in cis to DNA double-strand breaks. Cell. 2010;141:970–81. doi:10.1016/j.cell.2010.04.038. PMID:20550933
   PubMed Web of Science ®Google Scholar
• Ohle C, Tesorero R, Schermann G, et al. Transient RNA-DNA Hybrids Are Required for Efficient Double-Strand Break Repair. Cell. 2016;167:1001–13 e7. doi:10.1016/j.cell.2016.10.001.
   Web of Science ®Google Scholar
• Gaillard H, Aguilera A. Transcription as a Threat to Genome Integrity. Annu Rev Biochem. 2016;85:291–317. doi:10.1146/annurev-biochem-060815-014908. PMID:27023844
   PubMed Web of Science ®Google Scholar
• Aronica L, Kasparek T, Ruchman D, et al. The spliceosome-associated protein Nrl1 suppresses homologous recombination-dependent R-loop formation in fission yeast. Nucleic Acids Res. 2016;44:1703–17. doi:10.1093/nar/gkv1473. PMID:26682798
   PubMed Web of Science ®Google Scholar
• Barski A, Cuddapah S, Cui K, et al. High-resolution profiling of histone methylations in the human genome. Cell. 2007;129:823–37. doi:10.1016/j.cell.2007.05.009. PMID:17512414
   PubMed Web of Science ®Google Scholar
• Nishioka K, Chuikov S, Sarma K, et al. Set9, a novel histone H3 methyltransferase that facilitates transcription by precluding histone tail modifications required for heterochromatin formation. Genes Dev. 2002;16:479–89. doi:10.1101/gad.967202. PMID:11850410
   PubMed Web of Science ®Google Scholar
• Zegerman P, Canas B, Pappin D, et al. Histone H3 lysine 4 methylation disrupts binding of nucleosome remodeling and deacetylase (NuRD) repressor complex. J Biol Chem. 2002;277:11621–4. doi:10.1074/jbc.C200045200. PMID:11850414
   PubMed Web of Science ®Google Scholar
• Li X, Liu L, Yang S, et al. Histone demethylase KDM5B is a key regulator of genome stability. Proc Natl Acad Sci U S A. 2014;111:7096–101. doi:10.1073/pnas.1324036111. PMID:24778210
   PubMed Web of Science ®Google Scholar
• Conomos D, Reddel RR, Pickett HA. NuRD-ZNF827 recruitment to telomeres creates a molecular scaffold for homologous recombination. Nat Struct Mol Biol. 2014; doi:10.1038/nsmb.2877. PMID: 25150861
   PubMed Web of Science ®Google Scholar
• Panagopoulos I, Micci F, Thorsen J, et al. Fusion of ZMYND8 and RELA genes in acute erythroid leukemia. PLoS One. 2013;8:e63663. doi:10.1371/journal.pone.0063663. PMID: 23667654
   PubMed Web of Science ®Google Scholar
• Cancer Genome Atlas Research N. Integrated genomic analyses of ovarian carcinoma. Nature. 2011;474:609–15. doi:10.1038/nature10166. PMID: 21720365
   PubMed Web of Science ®Google Scholar
• Basu M, Khan MW, Chakrabarti P, et al. Chromatin reader ZMYND8 is a key target of all trans retinoic acid-mediated inhibition of cancer cell proliferation. Biochim Biophys Acta. 2017;1860:450–9. doi:10.1016/j.bbagrm.2017.02.004. PMID: 28232094
   PubMed Web of Science ®Google Scholar
• Basu M, Sengupta I, Khan MW, et al. Dual histone reader ZMYND8 inhibits cancer cell invasion by positively regulating epithelial genes. Biochem J. 2017;474:1919–34. doi:10.1042/BCJ20170223. PMID: 28432260
   PubMed Web of Science ®Google Scholar
• Lai AY, Wade PA. Cancer biology and NuRD: a multifaceted chromatin remodelling complex. Nat Rev Cancer. 2011;11:588–96. doi:10.1038/nrc3091. PMID: 21734722
   PubMed Web of Science ®Google Scholar
• Le Gallo M, O'Hara AJ, Rudd ML, et al. Exome sequencing of serous endometrial tumors identifies recurrent somatic mutations in chromatin-remodeling and ubiquitin ligase complex genes. Nat Genet. 2012;44:1310–5. doi:10.1038/ng.2455. PMID: 23104009
   PubMed Web of Science ®Google Scholar
• Teng YC, Lee CF, Li YS, et al. Histone demethylase RBP2 promotes lung tumorigenesis and cancer metastasis. Cancer Res. 2013;73:4711–21. doi:10.1158/0008-5472.CAN-12-3165. PMID: 23722541
   PubMed Web of Science ®Google Scholar
• Hou J, Wu J, Dombkowski A, et al. Genomic amplification and a role in drug-resistance for the KDM5A histone demethylase in breast cancer. Am J Transl Res. 2012;4:247–56. PMID: 22937203
   PubMed Web of Science ®Google Scholar
• Sharma SV, Lee DY, Li B, et al. A chromatin-mediated reversible drug-tolerant state in cancer cell subpopulations. Cell. 2010;141:69–80. doi:10.1016/j.cell.2010.02.027. PMID: 20371346
   PubMed Web of Science ®Google Scholar
• Rodriguez R, Miller KM. Unravelling the genomic targets of small molecules using high-throughput sequencing. Nat Rev Genet. 2014;15:783–96. doi:10.1038/nrg3796. PMID: 25311424
   PubMed Web of Science ®Google Scholar
• Dawson MA. The cancer epigenome: Concepts, challenges, and therapeutic opportunities. Science. 2017;355:1147–52. doi:10.1126/science.aam7304. PMID: 28302822
   PubMed Web of Science ®Google Scholar
• Brown JS, O'Carrigan B, Jackson SP, et al. Targeting DNA Repair in Cancer: Beyond PARP Inhibitors. Cancer Discov. 2017;7:20–37. doi:10.1158/2159-8290.CD-16-0860. PMID: 28003236
   PubMed Web of Science ®Google Scholar
• Jackson SP, Helleday T. DNA REPAIR. Drugging DNA repair Science. 2016;352:1178–9.
   Google Scholar
• Zacharioudakis E, Agarwal P, Bartoli A, et al. Chromatin Regulates Genome Targeting with Cisplatin. Angew Chem Int Ed Engl. 2017;56:6483–7. doi:10.1002/anie.201701144. PMID: 28474855
   PubMed Web of Science ®Google Scholar