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Brief Report

Application of Recombination -Induced Tag Exchange (RITE) to study histone dynamics in human cells

ORCID Icon, ORCID Icon, & ORCID Icon
Pages 901-913 | Received 31 Oct 2019, Accepted 05 Mar 2020, Published online: 31 Mar 2020

References

  • Bondarenko VA, Steele LM, Újvári A, et al. Nucleosomes can form a polar barrier to transcript elongation by RNA polymerase II. Mol Cell. 2006;24:469–479.
  • de Jong BE, van Noort J. Overcoming chromatin barriers. Elife. 2019;8. DOI:10.7554/eLife.50761
  • Li B, Carey M, Workman JL. The role of chromatin during transcription. Cell. 2007;128:707–719.
  • Weber CM, Ramachandran S, Henikoff S. Nucleosomes are context-specific, H2A.Z-modulated barriers to RNA polymerase. Mol Cell. 2014;53:819–830.
  • Clapier CR, Cairns BR. The biology of chromatin remodeling complexes. Annu Rev Biochem. 2009;78:273–304.
  • Cramer P. Organization and regulation of gene transcription. Nature. 2019;573:45–54.
  • Smolle M, Workman JL, Venkatesh S. reSETting chromatin during transcription elongation. Epigenetics. 2013;8:10–15.
  • 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.
  • 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.
  • Terweij M, van Leeuwen F. Histone exchange: sculpting the epigenome. Front Life Sci. 2013;7:63–79.
  • Mei Q, Huang J, Chen W, et al. Regulation of DNA replication-coupled histone gene expression. Oncotarget. 2017;8. DOI:10.18632/oncotarget.21887
  • Hamiche A, Shuaib M. Chaperoning the histone H3 family. Biochim Biophys Acta Gene Regul Mech. 2012;1819(3–4):230–237.
  • Sauer PV, Gu Y, Liu WH, et al. Mechanistic insights into histone deposition and nucleosome assembly by the chromatin assembly factor-1. Nucleic Acids Res. 2018;46:9907–9917.
  • Shibahara K-I, Stillman B. Replication-dependent marking of DNA by PCNA facilitates CAF-1-coupled inheritance of chromatin. Cell. 1999;96:575–585.
  • Kimura H, Cook PR. Kinetics of core histones in living human cells. J Cell Biol. 2001;153:1341–1354.
  • Thiriet C, Hayes JJ. Histone dynamics during transcription: exchange of H2a/H2b dimers and H3/H4 tetramers during pol II elongation. Results Probl Cell Differ. 2006;41:77–90.
  • Ahmad K, Henikoff S. The histone variant H3.3 marks active chromatin by replication-independent nucleosome assembly. Mol Cell. 2002;9:1191–1200.
  • Ray-Gallet D, Woolfe A, Vassias I, et al. Dynamics of histone H3 deposition in vivo reveal a nucleosome gap-filling mechanism for H3.3 to maintain chromatin integrity. Mol Cell. 2011;44:928–941.
  • Schneiderman JI, Orsi GA, Hughes KT, et al. Nucleosome-depleted chromatin gaps recruit assembly factors for the H3.3 histone variant. Proc Nat Acad Sci. 2012;109:19721–19726.
  • Schwartz BE. Transcriptional activation triggers deposition and removal of the histone variant H3.3. Genes Dev. 2005;19:804–814.
  • Tagami H, Ray-Gallet D, Almouzni G, et al. Histone H3.1 and H3.3 complexes mediate nucleosome assembly pathways dependent or independent of DNA synthesis. Cell. 2004;116:51–61.
  • Goldberg AD, Banaszynski LA, Noh K-M, et al. Distinct factors control histone variant H3.3 localization at specific genomic regions. Cell. 2010;140:678–691.
  • Lewis PW, Elsaesser SJ, Noh K-M, et al. Daxx is an H3.3-specific histone chaperone and cooperates with ATRX in replication-independent chromatin assembly at telomeres. Proc Nat Acad Sci. 2010;107:14075–14080.
  • Ray-Gallet D, Quivy J-P, Scamps C, et al. HIRA is critical for a nucleosome assembly pathway independent of DNA synthesis. Mol Cell. 2002;9:1091–1100.
  • Drane P, Ouararhni K, Depaux A, et al. The death-associated protein DAXX is a novel histone chaperone involved in the replication-independent deposition of H3.3. Genes Dev. 2010;24:1253–1265.
  • Maze I, Wenderski W, Noh K-M, et al. Critical role of histone turnover in neuronal transcription and plasticity. Neuron. 2015;87:77–94.
  • Tvardovskiy A, Schwämmle V, Kempf SJ, et al. Accumulation of histone variant H3.3 with age is associated with profound changes in the histone methylation landscape. Nucleic Acids Res. 2017;45:9272–9289.
  • Dion MF, Kaplan T, Kim M, et al. Dynamics of replication-independent histone turnover in budding yeast. Science. 2007;315:1405–1408.
  • Jamai A, Imoberdorf RM, Strubin M. Continuous histone H2B and transcription-dependent histone H3 exchange in yeast cells outside of replication. Mol Cell. 2007;25:345–355.
  • Rufiange A, Jacques P-É, Bhat W, et al. Genome-wide replication-independent histone H3 exchange occurs predominantly at promoters and implicates H3K56 acetylation and Asf1. Mol Cell. 2007;27:393–405.
  • Radman-Livaja M, Verzijlbergen KF, Weiner A, et al. Patterns and mechanisms of ancestral histone protein inheritance in budding yeast. PLoS Biol. 2011;9:e1001075.
  • Huang C, Zhang Z, Xu M, et al. H3.3-H4 Tetramer splitting events feature cell-type specific enhancers. PLoS Genet. 2013;9(6):e1003558.
  • Kraushaar DC, Jin W, Maunakea A, et al. Genome-wide incorporation dynamics reveal distinct categories of turnover for the histone variant H3.3. Genome Biol. 2013;14:R121.
  • Yildirim O, Hung J-H, Cedeno RJ, et al. A system for genome-wide histone variant dynamics in ES cells reveals dynamic MacroH2A2 replacement at promoters. PLoS Genet. 2014;10:e1004515.
  • Hödl M, Basler K. Transcription in the absence of histone H3.3. Curr Biol. 2009;19:1221–1226.
  • Jang C-W, Shibata Y, Starmer J, et al. Histone H3.3 maintains genome integrity during mammalian development. Genes Dev. 2015;29:1377–1392.
  • Nashun B, Hill PW, Smallwood SA, et al. Continuous histone replacement by Hira is essential for normal transcriptional regulation and de novo DNA methylation during mouse oogenesis. Mol Cell. 2015;60:611–625.
  • Fang H-T, Farran CAE, Xing QR, et al. Global H3.3 dynamic deposition defines its bimodal role in cell fate transition. Nat Commun. 2018;9. DOI:10.1038/s41467-018-03904-7
  • Kong Q, Banaszynski LA, Geng F, et al. Histone variant H3.3–mediated chromatin remodeling is essential for paternal genome activation in mouse preimplantation embryos. J Biol Chem. 2018;293:3829–3838.
  • Delaney K, Mailler J, Wenda JM, et al. Differential expression of histone H3.3 genes and their role in modulating temperature stress response in Caenorhabditis elegans. Genetics. 2018;209:551–565.
  • Banaszynski LA, Wen D, Dewell S, et al. Hira-dependent histone H3.3 deposition facilitates PRC2 recruitment at developmental loci in ES cells. Cell. 2013;155:107–120.
  • Harada A, Okada S, Konno D, et al. Chd2 interacts with H3.3 to determine myogenic cell fate. Embo J. 2012;31:2994–3007.
  • Harada A, Maehara K, Sato Y, et al. Incorporation of histone H3.1 suppresses the lineage potential of skeletal muscle. Nucleic Acids Res. 2014;43:775–786.
  • Yuen BTK, Bush KM, Barrilleaux BL, et al. Histone H3.3 regulates dynamic chromatin states during spermatogenesis. Development. 2014;141:3483–3494.
  • Jullien J, Astrand C, Szenker E, et al. HIRA dependent H3.3 deposition is required for transcriptional reprogramming following nuclear transfer to Xenopus oocytes. Epigenetics Chromatin. 2012;5. DOI:10.1186/1756-8935-5-17
  • Tamura T, Smith M, Kanno T, et al. Inducible deposition of the Histone variant H3.3 in interferon-stimulated genes. J Biol Chem. 2009;284:12217–12225.
  • Buschbeck M, Hake SB. Variants of core histones and their roles in cell fate decisions, development and cancer. Nat Rev Mol Cell Biol. 2017;18:299–314.
  • Deal RB, Henikoff S. Capturing the dynamic epigenome. Genome Biol. 2010;11:218.
  • Ha M, Kraushaar DC, Zhao K. Genome-wide analysis of H3.3 dissociation reveals high nucleosome turnover at distal regulatory regions of embryonic stem cells. Epigenetics Chromatin. 2014;7(1). DOI:10.1186/1756-8935-7-38
  • Deal RB, Henikoff JG, Henikoff S. Genome-wide kinetics of nucleosome turnover determined by metabolic labeling of histones. Science. 2010;328:1161–1164.
  • Deaton AM, Mariluz G-R, Mieczkowski J, et al. Enhancer regions show high histone H3.3 turnover that changes during differentiation. eLife. 2016;5. DOI:10.7554/eLife.15316
  • Terweij M, van Welsem T, van Deventer S, et al. Recombination-Induced Tag Exchange (RITE) cassette series to monitor protein dynamics in saccharomyces cerevisiae. G3. 2013;3:1261–1272.
  • Verzijlbergen KF, Menendez-Benito V, van Welsem T, et al. Recombination-induced tag exchange to track old and new proteins. Proc Nat Acad Sci. 2010;107:64–68.
  • Verzijlbergen KF, van Welsem T, Sie D, et al. A barcode screen for epigenetic regulators reveals a role for the NuB4/HAT-B histone acetyltransferase complex in histone turnover. PLoS Genet. 2011;7:e1002284.
  • Audergon PNCB, Catania S, Kagansky A, et al. Restricted epigenetic inheritance of H3K9 methylation. Science. 2015;348:132–135.
  • De Vos D, Frederiks F, Terweij M, et al. Progressive methylation of ageing histones by Dot1 functions as a timer. EMBO Rep. 2011;12:956–962.
  • Gan H, Serra-Cardona A, Hua X, et al. The Mcm2-Ctf4-Polα axis facilitates parental histone H3-H4 transfer to lagging strands. Mol Cell. 2018;72. DOI:10.1016/j.molcel.2018.09.001
  • Hughes AL, Hughes CE, Henderson KA, et al. Selective sorting and destruction of mitochondrial membrane proteins in aged yeast. eLife. 2016;5. DOI:10.7554/eLife.13943
  • Sadeghi L, Prasad P, Ekwall K, et al. The Paf1 complex factors Leo1 and Paf1 promote local histone turnover to modulate chromatin states in fission yeast. EMBO Rep. 2015;16:1673–1687.
  • Svensson JP, Shukla M, Menendez-Benito V, et al. A nucleosome turnover map reveals that the stability of histone H4 Lys20 methylation depends on histone recycling in transcribed chromatin. Genome Res. 2015;25:872–883.
  • Yu C, Gan H, Serra-Cardona A, et al. A mechanism for preventing asymmetric histone segregation onto replicating DNA strands. Science. 2018;361:1386–1389.
  • Ramakrishnan S, Pokhrel S, Palani S, et al. Counteracting h3k4 methylation modulators set1 and jhd2 co-regulate chromatin dynamics and gene transcription. Nat Commun. 2016;7.
  • Radman-Livaja M, Quan TK, Valenzuela L, et al. A key role for Chd1 in histone H3 dynamics at the 3′ ends of long genes in yeast. PLoS Genet. 2012;8:e1002811.
  • Cong L, Ran FA, Cox D, et al. Multiplex genome engineering using crispr/cas systems. Science. 2013;15:819-823.
  • Mali P, Yang L, Esvelt KM, et al. RNA-guided human genome engineering via Cas9. Science. 2013;339:823–826.
  • Hockemeyer D, Soldner F, Beard C, et al. Efficient targeting of expressed and silent genes in human escs and ipscs using zinc-finger nucleases. Nat Biotechnol. 2009;27:851-857.
  • Pchelintsev NA, Mcbryan T, Rai TS, et al. Placing the HIRA histone chaperone complex in the chromatin landscape. Cell Rep. 2013;3:1012–1019.
  • Carvalho S, Raposo AC, Martins FB, et al. Histone methyltransferase SETD2 coordinates FACT recruitment with nucleosome dynamics during transcription. Nucleic Acids Res. 2013;41(5):2881–2893.
  • Langmead B, Trapnell C, Pop M, et al. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 2009;10:R25.
  • Kim D, Langmead B, Salzberg SL. HISAT: a fast spliced aligner with low memory requirements. Nat Methods. 2015;12:357–360.
  • Galic H, Vasseur P, Radman-Livaja M. The budding yeast heterochromatic SIR complex resets upon exit from stationary phase. bioRxiv. 2019.
  • Thayer NH, Leverich CK, Fitzgibbon MP, et al. Identification of long-lived proteins retained in cells undergoing repeated asymmetric divisions. Proc Nat Acad Sci. 2014;111:14019–14026.
  • van Deventer S, Menendez-Benito V, van Leeuwen F, et al. N-terminal acetylation and replicative age affect proteasome localization and cell fitness during aging. J Cell Sci. 2014;128:109–117.
  • Menendez-Benito V, van Deventer S, Jimenez-Garcia V, et al. Spatiotemporal analysis of organelle and macromolecular complex inheritance. Proc Nat Acad Sci. 2012;110:175–180.
  • Lengefeld J, Yen E, Chen X, et al. Spatial cues and not spindle pole maturation drive the asymmetry of astral microtubules between new and preexisting spindle poles. Mol Biol Cell. 2018;29:10–28.
  • Toyama BH, Drigo RAE, Lev-Ram V, et al. Visualization of long-lived proteins reveals age mosaicism within nuclei of postmitotic cells. J Cell Biol. 2018;218:433–444.
  • Tran V, Lim C, Xie J, et al. Asymmetric division of Drosophila male germline stem cell shows asymmetric histone distribution. Science. 2012;338:679–682.
  • Chung HK, Jacobs CL, Huo Y, et al. Tunable and reversible drug control of protein production via a self-excising degron. Nat Chem Biol. 2015;11:713–720.
  • Jacobs CL, Badiee RK, Lin MZ. StaPLs: versatile genetically encoded modules for engineering drug-inducible proteins. Nat Methods. 2018;15:523–526.