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Review

Recognition of cancer mutations in histone H3K36 by epigenetic writers and readers

, ORCID Icon, , ORCID Icon, &
Pages 683-692 | Received 30 May 2018, Accepted 12 Jul 2018, Published online: 23 Aug 2018

References

  • Rothbart SB, Strahl BD. Interpreting the language of histone and DNA modifications. Biochim Biophys Acta. 2014;1839:627–643.
  • Bannister AJ, Kouzarides T. Regulation of chromatin by histone modifications. Cell Res. 2011;21:381–395.
  • Andrews FH, Strahl BD, Kutateladze TG. Insights into newly discovered marks and readers of epigenetic information. Nat Chem Biol. 2016;12:662–668.
  • Taverna SD, Li H, Ruthenburg AJ, et al. How chromatin-binding modules interpret histone modifications: lessons from professional pocket pickers. Nat Struct Mol Biol. 2007;14:1025–1040.
  • Musselman CA, Lalonde ME, Cote J, et al. Perceiving the epigenetic landscape through histone readers. Nat Struct Mol Biol. 2012;19:1218–1227.
  • Patel DJ, Wang Z. Readout of epigenetic modifications. Annu Rev Biochem. 2013;82:81–118.
  • Feinberg AP. The key role of epigenetics in human disease prevention and mitigation. N Engl J Med. 2018;378:1323–1334.
  • McDaniel SL, Strahl BD. Shaping the cellular landscape with Set2/SETD2 methylation. Cell Mol Life Sci. 2017;74:3317–3334.
  • Khuong-Quang DA, Buczkowicz P, Rakopoulos P, et al. K27M mutation in histone H3.3 defines clinically and biologically distinct subgroups of pediatric diffuse intrinsic pontine gliomas. Acta Neuropathol. 2012;124:439–447.
  • Schwartzentruber J, Korshunov A, Liu XY, et al. Driver mutations in histone H3.3 and chromatin remodelling genes in paediatric glioblastoma. Nature. 2012;482:226–231.
  • Wu G, Broniscer A, McEachron TA, et al. Somatic histone H3 alterations in pediatric diffuse intrinsic pontine gliomas and non-brainstem glioblastomas. Nat Genet. 2012;44:251–253.
  • Behjati S, Tarpey PS, Presneau N, et al. Distinct H3F3A and H3F3B driver mutations define chondroblastoma and giant cell tumor of bone. Nat Genet. 2013;45:1479–1482.
  • Papillon-Cavanagh S, Lu C, Gayden T, et al. Impaired H3K36 methylation defines a subset of head and neck squamous cell carcinomas. Nat Genet. 2017;49:180–185.
  • Strahl BD, Grant PA, Briggs SD, et al. Set2 is a nucleosomal histone H3-selective methyltransferase that mediates transcriptional repression. Mol Cell Biol. 2002;22:1298–1306.
  • Rayasam GV, Wendling O, Angrand PO, et al. NSD1 is essential for early post-implantation development and has a catalytically active SET domain. EMBO J. 2003;22:3153–3163.
  • Angrand PO, Apiou F, Stewart AF, et al. NSD3, a new SET domain-containing gene, maps to 8p12 and is amplified in human breast cancer cell lines. Genomics. 2001;74:79–88.
  • Eram MS, Kuznetsova E, Li F, et al. Kinetic characterization of human histone H3 lysine 36 methyltransferases, ASH1L and SETD2. Biochim Biophys Acta. 2015;1850:1842–1848.
  • Yi X, Jiang XJ, Li XY, et al. Histone methyltransferases: novel targets for tumor and developmental defects. Am J Transl Res. 2015;7:2159–2175.
  • Edmunds JW, Mahadevan LC, Clayton AL. Dynamic histone H3 methylation during gene induction: HYPB/Setd2 mediates all H3K36 trimethylation. EMBO J. 2008;27:406–420.
  • Sun XJ, Wei J, Wu XY, et al. Identification and characterization of a novel human histone H3 lysine 36-specific methyltransferase. J Biol Chem. 2005;280:35261–35271.
  • Kizer KO, Phatnani HP, Shibata Y, et al. A novel domain in Set2 mediates RNA polymerase II interaction and couples histone H3 K36 methylation with transcript elongation. Mol Cell Biol. 2005;25:3305–3316.
  • Lu C, Jain SU, Hoelper D, et al. Histone H3K36 mutations promote sarcomagenesis through altered histone methylation landscape. Science. 2016;352:844–849.
  • Carrozza MJ, Li B, Florens L, et al. Histone H3 methylation by Set2 directs deacetylation of coding regions by Rpd3S to suppress spurious intragenic transcription. Cell. 2005;123:581–592.
  • Keogh MC, Kurdistani SK, Morris SA, et al. Cotranscriptional set2 methylation of histone H3 lysine 36 recruits a repressive Rpd3 complex. Cell. 2005;123:593–605.
  • Smolle M, Venkatesh S, Gogol MM, et al. Chromatin remodelers Isw1 and Chd1 maintain chromatin structure during transcription by preventing histone exchange. Nat Struct Mol Biol. 2012;19:884–892.
  • Maltby VE, Martin BJ, Schulze JM, et al. Histone H3 lysine 36 methylation targets the Isw1b remodeling complex to chromatin. Mol Cell Biol. 2012;32:3479–3485.
  • Gilbert TM, McDaniel SL, Byrum SD, et al. A PWWP domain-containing protein targets the NuA3 acetyltransferase complex via histone H3 lysine 36 trimethylation to coordinate transcriptional elongation at coding regions. Mol Cell Proteomics. 2014;13:2883–2895.
  • Lee CH, Wu J, Li B. Chromatin remodelers fine-tune H3K36me-directed deacetylation of neighbor nucleosomes by Rpd3S. Mol Cell. 2013;52:255–263.
  • Venkatesh S, Smolle M, Li H, et al. Set2 methylation of histone H3 lysine 36 suppresses histone exchange on transcribed genes. Nature. 2012;489:452–455.
  • Venkatesh S, Li H, Gogol MM, et al. Selective suppression of antisense transcription by Set2-mediated H3K36 methylation. Nat Commun. 2016;7:13610.
  • Li B, Gogol M, Carey M, et al. Infrequently transcribed long genes depend on the Set2/Rpd3S pathway for accurate transcription. Genes Dev. 2007;21:1422–1430.
  • Li B, Gogol M, Carey M, et al. Combined action of PHD and chromo domains directs the Rpd3S HDAC to transcribed chromatin. Science. 2007;316:1050–1054.
  • Dronamraju R, Jha DK, Eser U, et al. Set2 methyltransferase facilitates cell cycle progression by maintaining transcriptional fidelity. Nucleic Acids Res. 2018;46:1331–1344.
  • Jha DK, Strahl BD. An RNA polymerase II-coupled function for histone H3K36 methylation in checkpoint activation and DSB repair. Nat Commun. 2014;5:3965.
  • McDaniel SL, Hepperla AJ, Huang J, et al. H3K36 methylation regulates nutrient stress response in saccharomyces cerevisiae by enforcing transcriptional fidelity. Cell Rep. 2017;19:2371–2382.
  • Sen P, Dang W, Donahue G, et al. H3K36 methylation promotes longevity by enhancing transcriptional fidelity. Genes Dev. 2015;29:1362–1376.
  • Sorenson MR, Jha DK, Ucles SA, et al. Histone H3K36 methylation regulates pre-mRNA splicing in Saccharomyces cerevisiae. RNA Biol. 2016;13:412–426.
  • Pai CC, Deegan RS, Subramanian L, et al. A histone H3K36 chromatin switch coordinates DNA double-strand break repair pathway choice. Nat Commun. 2014;5:4091.
  • Carvalho S, Vitor AC, Sridhara SC, et al. SETD2 is required for DNA double-strand break repair and activation of the p53-mediated checkpoint. Elife. 2014;3:e02482.
  • Li F, Mao G, Tong D, et al. The histone mark H3K36me3 regulates human DNA mismatch repair through its interaction with MutSalpha. Cell. 2013;153:590–600.
  • Pai CC, Kishkevich A, Deegan RS, et al. Set2 methyltransferase facilitates DNA replication and promotes genotoxic stress responses through MBF-dependent transcription. Cell Rep. 2017;20:2693–2705.
  • Pfister SX, Ahrabi S, Zalmas LP, et al. SETD2-dependent histone H3K36 trimethylation is required for homologous recombination repair and genome stability. Cell Rep. 2014;7:2006–2018.
  • Kumar GS, Chang W, Xie T, et al. Sequence requirements for combinatorial recognition of histone H3 by the MRG15 and Pf1 subunits of the Rpd3S/Sin3S corepressor complex. J Mol Biol. 2012;422:519–531.
  • Jelinic P, Pellegrino J, David G. A novel mammalian complex containing Sin3B mitigates histone acetylation and RNA polymerase II progression within transcribed loci. Mol Cell Biol. 2011;31:54–62.
  • Guo R, Zheng L, Park JW, et al. BS69/ZMYND11 reads and connects histone H3.3 lysine 36 trimethylation-decorated chromatin to regulated pre-mRNA processing. Mol Cell. 2014;56:298–310.
  • Wen H, Li Y, Xi Y, et al. ZMYND11 links histone H3.3K36me3 to transcription elongation and tumour suppression. Nature. 2014;508:263–268.
  • Baubec T, Colombo DF, Wirbelauer C, et al. Genomic profiling of DNA methyltransferases reveals a role for DNMT3B in genic methylation. Nature. 2015;520:243–247.
  • Morselli M, Pastor WA, Montanini B, et al. In vivo targeting of de novo DNA methylation by histone modifications in yeast and mouse. Elife. 2015;4:e06205.
  • Neri F, Rapelli S, Krepelova A, et al. Intragenic DNA methylation prevents spurious transcription initiation. Nature. 2017;543:72–77.
  • Pradeepa MM, Sutherland HG, Ule J, et al. Psip1/Ledgf p52 binds methylated histone H3K36 and splicing factors and contributes to the regulation of alternative splicing. PLoS Genet. 2012;8:e1002717.
  • Zhu L, Li Q, Wong SH, et al. ASH1L links histone H3 lysine 36 dimethylation to MLL leukemia. Cancer Discov. 2016;6:770–783.
  • Musselman CA, Avvakumov N, Watanabe R, et al. Molecular basis for H3K36me3 recognition by the Tudor domain of PHF1. Nat Struct Mol Biol. 2012;19:1266–1272.
  • Brien GL, Gambero G, O’Connell DJ, et al. Polycomb PHF19 binds H3K36me3 and recruits PRC2 and demethylase NO66 to embryonic stem cell genes during differentiation. Nat Struct Mol Biol. 2012;19:1273–1281.
  • Cai L, Rothbart SB, Lu R, et al. An H3K36 methylation-engaging Tudor motif of polycomb-like proteins mediates PRC2 complex targeting. Mol Cell. 2013;49:571–582.
  • Ballare C, Lange M, Lapinaite A, et al. Phf19 links methylated Lys36 of histone H3 to regulation of Polycomb activity. Nat Struct Mol Biol. 2012;19:1257–1265.
  • Qin S, Guo Y, Xu C, et al. Tudor domains of the PRC2 components PHF1 and PHF19 selectively bind to histone H3K36me3. Biochem Biophys Res Commun. 2013;430:547–553.
  • Gibson MD, Gatchalian J, Slater A, et al. PHF1 Tudor and N-terminal domains synergistically target partially unwrapped nucleosomes to increase DNA accessibility. Nucleic Acids Res. 2017;45:3767–3776.
  • Gatchalian J, Kingsley MC, Moslet SD, et al. An aromatic cage is required but not sufficient for binding of Tudor domains of the Polycomblike protein family to H3K36me3. Epigenetics. 2015;10:467–473.
  • Musselman CA, Gibson MD, Hartwick EW, et al. Binding of PHF1 Tudor to H3K36me3 enhances nucleosome accessibility. Nat Commun. 2013;4:2969.
  • Bender S, Tang Y, Lindroth AM, et al. Reduced H3K27me3 and DNA hypomethylation are major drivers of gene expression in K27M mutant pediatric high-grade gliomas. Cancer Cell. 2013;24:660–672.
  • Chan KM, Fang D, Gan H, et al. The histone H3.3K27M mutation in pediatric glioma reprograms H3K27 methylation and gene expression. Genes Dev. 2013;27:985–990.
  • Lewis PW, Muller MM, Koletsky MS, et al. Inhibition of PRC2 activity by a gain-of-function H3 mutation found in pediatric glioblastoma. Science. 2013;340:857–861.
  • Lewis PW, Allis CD. Poisoning the “histone code” in pediatric gliomagenesis. Cell Cycle. 2013;12:3241–3242.
  • Brown ZZ, Muller MM, Jain SU, et al. Strategy for “detoxification” of a cancer-derived histone mutant based on mapping its interaction with the methyltransferase PRC2. J Am Chem Soc. 2014;136:13498–13501.
  • Brown ZZ, Muller MM, Kong HE, et al. Targeted histone peptides: insights into the spatial regulation of the methyltransferase PRC2 by using a Surrogate of heterotypic chromatin. Angew Chem Int Ed Engl. 2015;54:6457–6461.
  • Jayaram H, Hoelper D, Jain SU, et al. S-adenosyl methionine is necessary for inhibition of the methyltransferase G9a by the lysine 9 to methionine mutation on histone H3. Proc Natl Acad Sci USA. 2016;113:6182–6187.
  • Justin N, Zhang Y, Tarricone C, et al. Structural basis of oncogenic histone H3K27M inhibition of human polycomb repressive complex 2. Nat Commun. 2016;7:11316.
  • Jiao L, Liu X. Structural basis of histone H3K27 trimethylation by an active polycomb repressive complex 2. Science. 2015;350:aac4383.
  • Fang D, Gan H, Lee JH, et al. The histone H3.3K36M mutation reprograms the epigenome of chondroblastomas. Science. 2016;352:1344–1348.
  • Yang S, Zheng X, Lu C, et al. Molecular basis for oncohistone H3 recognition by SETD2 methyltransferase. Genes Dev. 2016;30:1611–1616.
  • Schmitges FW, Prusty AB, Faty M, et al. Histone methylation by PRC2 is inhibited by active chromatin marks. Mol Cell. 2011;42:330–341.
  • Yuan W, Xu M, Huang C, et al. H3K36 methylation antagonizes PRC2-mediated H3K27 methylation. J Biol Chem. 2011;286:7983–7989.
  • Zhang Y, Shan CM, Wang J, et al. Molecular basis for the role of oncogenic histone mutations in modulating H3K36 methylation. Sci Rep. 2017;7:43906.
  • Banaszynski LA, Allis CD, Lewis PW. Histone variants in metazoan development. Dev Cell. 2010;19:662–674.
  • Vezzoli A, Bonadies N, Allen MD, et al. Molecular basis of histone H3K36me3 recognition by the PWWP domain of Brpf1. Nat Struct Mol Biol. 2010;17:617–619.
  • Klein BJ, Muthurajan UM, Lalonde ME, et al. Bivalent interaction of the PZP domain of BRPF1 with the nucleosome impacts chromatin dynamics and acetylation. Nucleic Acids Res. 2016;44:472–484.
  • Drouin S, Laramee L, Jacques PE, et al. DSIF and RNA polymerase II CTD phosphorylation coordinate the recruitment of Rpd3S to actively transcribed genes. PLoS Genet. 2010;6:e1001173.
  • Andrews FH, Gatchalian J, Krajewski K, et al. Regulation of methyllysine readers through phosphorylation. ACS Chem Biol. 2016;11:547–553.

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