ATRX Plays a Key Role in Maintaining Silencing at Interstitial Heterochromatic Loci and Imprinted Genes

Cell Reports

Volumn 11, Issue 3, 2015, Pages 405-418

  Voon, Hsiao P J ^a   Hughes, Jim R ^a   Rode, Christina ^a   DeLaRosa Velázquez, Inti A ^b   Jenuwein, Thomas ^b   Feil, Robert ^c   Higgs, Douglas R ^a   Gibbons, Richard J ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b MAX PLANCK INSTITUTE OF IMMUNOBIOLOGY AND EPIGENETICS   (Germany)

^c CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

DAXX PROTEIN; DNA; HISTONE H3; NUCLEAR PROTEIN; PROTEIN ATRX; UNCLASSIFIED DRUG; ATRX PROTEIN, MOUSE; DNA HELICASE; HETEROCHROMATIN; HISTONE;

ALLELE; ANIMAL CELL; ARTICLE; ATRX GENE; BINDING SITE; CONTROLLED STUDY; DNA METHYLATION; EMBRYONIC STEM CELL; FEMALE; GENE; GENE EXPRESSION; GENE MUTATION; GENE REPRESSION; GENE SILENCING; GENOME IMPRINTING; HETEROCHROMATIN; HISTONE MODIFICATION; IMPRINTED GENE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN LOCALIZATION; PROTEIN MODIFICATION; REGULATORY MECHANISM; TELOMERE; ANIMAL; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN IMMUNOPRECIPITATION; GENE INACTIVATION; GENE LOCUS; GENETICS; METABOLISM; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION;

ANIMALS; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN IMMUNOPRECIPITATION; DNA HELICASES; GENE KNOCKOUT TECHNIQUES; GENE SILENCING; GENETIC LOCI; HETEROCHROMATIN; HISTONES; MICE; NUCLEAR PROTEINS; REAL-TIME POLYMERASE CHAIN REACTION;

EID: 84928215174     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2015.03.036     Document Type: Article

References (49)

1. Abmayr S.M., Workman J.L. Holding on through DNA replication: histone modification or modifier?. Cell 2012, 150:875-877.
2. Ahmad K., Henikoff S. The histone variant H3.3 marks active chromatin by replication-independent nucleosome assembly. Mol. Cell 2002, 9:1191-1200.
3. Banaszynski L.A., Wen D., Dewell S., Whitcomb S.J., Lin M., Diaz N., Elsässer S.J., Chapgier A., Goldberg A.D., Canaani E., et al. Hira-dependent histone H3.3 deposition facilitates PRC2 recruitment at developmental loci in ES cells. Cell 2013, 155:107-120.
4. Barlow D.P. Genomic imprinting: a mammalian epigenetic discovery model. Annu. Rev. Genet. 2011, 45:379-403.
5. Brinkman A.B., Gu H., Bartels S.J., Zhang Y., Matarese F., Simmer F., Marks H., Bock C., Gnirke A., Meissner A., Stunnenberg H.G. Sequential ChIP-bisulfite sequencing enables direct genome-scale investigation of chromatin and DNA methylation cross-talk. Genome Res. 2012, 22:1128-1138.
6. Bulut-Karslioglu A., De La Rosa-Velázquez I.A., Ramirez F., Barenboim M., Onishi-Seebacher M., Arand J., Galán C., Winter G.E., Engist B., Gerle B., et al. Suv39h-dependent H3K9me3 marks intact retrotransposons and silences LINE elements in mouse embryonic stem cells. Mol. Cell 2014, 55:277-290.
7. Bush K.M., Yuen B.T., Barrilleaux B.L., Riggs J.W., O'Geen H., Cotterman R.F., Knoepfler P.S. Endogenous mammalian histone H3.3 exhibits chromatin-related functions during development. Epigenetics Chromatin 2013, 6:7.
8. Day D.S., Luquette L.J., Park P.J., Kharchenko P.V. Estimating enrichment of repetitive elements from high-throughput sequence data. Genome Biol. 2010, 11:R69.
9. Dhayalan A., Tamas R., Bock I., Tattermusch A., Dimitrova E., Kudithipudi S., Ragozin S., Jeltsch A. The ATRX-ADD domain binds to H3 tail peptides and reads the combined methylation state of K4 and K9. Hum. Mol. Genet. 2011, 20:2195-2203.
10. Drané P., Ouararhni K., Depaux A., Shuaib M., Hamiche A. 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.
11. Elsaesser S.J., Goldberg A.D., Allis C.D. New functions for an old variant: no substitute for histone H3.3. Curr. Opin. Genet. Dev. 2010, 20:110-117.
12. Eustermann S., Yang J.C., Law M.J., Amos R., Chapman L.M., Jelinska C., Garrick D., Clynes D., Gibbons R.J., Rhodes D., et al. Combinatorial readout of histone H3 modifications specifies localization of ATRX to heterochromatin. Nat. Struct. Mol. Biol. 2011, 18:777-782.
13. Fournier C., Goto Y., Ballestar E., Delaval K., Hever A.M., Esteller M., Feil R. Allele-specific histone lysine methylation marks regulatory regions at imprinted mouse genes. EMBO J. 2002, 21:6560-6570.
14. Garrick D., Sharpe J.A., Arkell R., Dobbie L., Smith A.J., Wood W.G., Higgs D.R., Gibbons R.J. Loss of Atrx affects trophoblast development and the pattern of X-inactivation in extraembryonic tissues. PLoS Genet. 2006, 2:e58.
15. Girardot M., Hirasawa R., Kacem S., Fritsch L., Pontis J., Kota S.K., Filipponi D., Fabbrizio E., Sardet C., Lohmann F., et al. PRMT5-mediated histone H4 arginine-3 symmetrical dimethylation marks chromatin at G+ C-rich regions of the mouse genome. Nucleic Acids Res. 2014, 42:235-248.
16. Goldberg A.D., Banaszynski L.A., Noh K.M., Lewis P.W., Elsaesser S.J., Stadler S., Dewell S., Law M., Guo X., Li X., et al. Distinct factors control histone variant H3.3 localization at specific genomic regions. Cell 2010, 140:678-691.
17. Groth A., Rocha W., Verreault A., Almouzni G. Chromatin challenges during DNA replication and repair. Cell 2007, 128:721-733.
18. Hake S.B., Garcia B.A., Duncan E.M., Kauer M., Dellaire G., Shabanowitz J., Bazett-Jones D.P., Allis C.D., Hunt D.F. Expression patterns and post-translational modifications associated with mammalian histone H3 variants. J.Biol. Chem. 2006, 281:559-568.
19. Heaphy C.M., de Wilde R.F., Jiao Y., Klein A.P., Edil B.H., Shi C., Bettegowda C., Rodriguez F.J., Eberhart C.G., Hebbar S., et al. Altered telomeres in tumors with ATRX and DAXX mutations. Science 2011, 333:425.
20. Iwase S., Xiang B., Ghosh S., Ren T., Lewis P.W., Cochrane J.C., Allis C.D., Picketts D.J., Patel D.J., Li H., Shi Y. ATRX ADD domain links an atypical histone methylation recognition mechanism to human mental-retardation syndrome. Nat. Struct. Mol. Biol. 2011, 18:769-776.
21. Jackson V. Deposition of newly synthesized histones: hybrid nucleosomes are not tandemly arranged on daughter DNA strands. Biochemistry 1988, 27:2109-2120.
22. Jasencakova Z., Scharf A.N., Ask K., Corpet A., Imhof A., Almouzni G., Groth A. Replication stress interferes with histone recycling and predeposition marking of new histones. Mol. Cell 2010, 37:736-743.
23. Jiao Y., Shi C., Edil B.H., de Wilde R.F., Klimstra D.S., Maitra A., Schulick R.D., Tang L.H., Wolfgang C.L., Choti M.A., et al. DAXX/ATRX, MEN1, and mTOR pathway genes are frequently altered in pancreatic neuroendocrine tumors. Science 2011, 331:1199-1203.
24. Kelsey G., Feil R. New insights into establishment and maintenance of DNA methylation imprints in mammals. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2013, 368:20110336.
25. Kernohan K.D., Jiang Y., Tremblay D.C., Bonvissuto A.C., Eubanks J.H., Mann M.R., Bérubé N.G. ATRX partners with cohesin and MeCP2 and contributes to developmental silencing of imprinted genes in the brain. Dev. Cell 2010, 18:191-202.
26. Kernohan K.D., Vernimmen D., Gloor G.B., Bérubé N.G. Analysis of neonatal brain lacking ATRX or MeCP2 reveals changes in nucleosome density, CTCF binding and chromatin looping. Nucleic Acids Res. 2014, 42:8356-8368.
27. Kraushaar D.C., Jin W., Maunakea A., Abraham B., Ha M., Zhao K. Genome-wide incorporation dynamics reveal distinct categories of turnover for the histone variant H3.3. Genome Biol. 2013, 14:R121.
28. Lamble S., Batty E., Attar M., Buck D., Bowden R., Lunter G., Crook D., El-Fahmawi B., Piazza P. Improved workflows for high throughput library preparation using the transposome-based Nextera system. BMC Biotechnol. 2013, 13:104.
29. Langmead B. Aligning short sequencing reads with Bowtie. Curr. Protoc. Bioinformatics 2010, Chapter 11:7.
30. Law M.J., Lower K.M., Voon H.P., Hughes J.R., Garrick D., Viprakasit V., Mitson M., De Gobbi M., Marra M., Morris A., et al. ATR-X syndrome protein targets tandem repeats and influences allele-specific expression in a size-dependent manner. Cell 2010, 143:367-378.
31. Lovejoy C.A., Li W., Reisenweber S., Thongthip S., Bruno J., de Lange T., De S., Petrini J.H., Sung P.A., Jasin M., et al. Loss of ATRX, genome instability, and an altered DNA damage response are hallmarks of the alternative lengthening of telomeres pathway. PLoS Genet. 2012, 8:e1002772. ALT Starr Cancer Consortium.
32. McKittrick E., Gafken P.R., Ahmad K., Henikoff S. Histone H3.3 is enriched in covalent modifications associated with active chromatin. Proc. Natl. Acad. Sci. USA 2004, 101:1525-1530.
33. Pannetier M., Julien E., Schotta G., Tardat M., Sardet C., Jenuwein T., Feil R. PR-SET7 and SUV4-20H regulate H4 lysine-20 methylation at imprinting control regions in the mouse. EMBO Rep. 2008, 9:998-1005.
34. Pchelintsev N.A., McBryan T., Rai T.S., van Tuyn J., Ray-Gallet D., Almouzni G., Adams P.D. Placing the HIRA histone chaperone complex in the chromatin landscape. Cell Rep. 2013, 3:1012-1019.
35. Rando O.J., Ahmad K. Rules and regulation in the primary structure of chromatin. Curr. Opin. Cell Biol. 2007, 19:250-256.
36. Ray-Gallet D., Quivy J.P., Scamps C., Martini E.M., Lipinski M., Almouzni G. HIRA is critical for a nucleosome assembly pathway independent of DNA synthesis. Mol. Cell 2002, 9:1091-1100.
37. Regha K., Sloane M.A., Huang R., Pauler F.M., Warczok K.E., Melikant B., Radolf M., Martens J.H., Schotta G., Jenuwein T., Barlow D.P. Active and repressive chromatin are interspersed without spreading in an imprinted gene cluster in the mammalian genome. Mol. Cell 2007, 27:353-366.
38. Schwartz B.E., Ahmad K. Transcriptional activation triggers deposition and removal of the histone variant H3.3. Genes Dev. 2005, 19:804-814.
39. Schwartzentruber J., Korshunov A., Liu X.Y., Jones D.T., Pfaff E., Jacob K., Sturm D., Fontebasso A.M., Quang D.A., Tönjes M., et al. Driver mutations in histone H3.3 and chromatin remodelling genes in paediatric glioblastoma. Nature 2012, 482:226-231.
40. Singh P., Wu X., Lee D.H., Li A.X., Rauch T.A., Pfeifer G.P., Mann J.R., Szabó P.E. Chromosome-wide analysis of parental allele-specific chromatin and DNA methylation. Mol. Cell. Biol. 2011, 31:1757-1770.
41. Soria G., Polo S.E., Almouzni G. Prime, repair, restore: the active role of chromatin in the DNA damage response. Mol. Cell 2012, 46:722-734.
42. Su Z., Boersma M.D., Lee J.H., Oliver S.S., Liu S., Garcia B.A., Denu J.M. ChIP-less analysis of chromatin states. Epigenetics & chromatin 2014, 7:7.
43. Trapnell C., Pachter L., Salzberg S.L. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 2009, 25:1105-1111.
44. Weaver J.R., Bartolomei M.S. Chromatin regulators of genomic imprinting. Biochim. Biophys. Acta 2014, 1839:169-177.
45. Williamson C.M., Blake A., Thomas S., Beechey C.V., Hancock J., Cattanach B.M., Peters J. Mouse Imprinting Data and References 2014, MRC Harwell, Oxfordshire. http://www.har.mrc.ac.uk/research/genomic_imprinting/.
46. Wirbelauer C., Bell O., Schübeler D. Variant histone H3.3 is deposited at sites of nucleosomal displacement throughout transcribed genes while active histone modifications show a promoter-proximal bias. Genes Dev. 2005, 19:1761-1766.
47. Wong L.H., Ren H., Williams E., McGhie J., Ahn S., Sim M., Tam A., Earle E., Anderson M.A., Mann J., Choo K.H. Histone H3.3 incorporation provides a unique and functionally essential telomeric chromatin in embryonic stem cells. Genome Res. 2009, 19:404-414.
48. Wong L.H., McGhie J.D., Sim M., Anderson M.A., Ahn S., Hannan R.D., George A.J., Morgan K.A., Mann J.R., Choo K.H. ATRX interacts with H3.3 in maintaining telomere structural integrity in pluripotent embryonic stem cells. Genome Res. 2010, 20:351-360.
49. Yuan P., Han J., Guo G., Orlov Y.L., Huss M., Loh Y.H., Yaw L.P., Robson P., Lim B., Ng H.H. Eset partners with Oct4 to restrict extraembryonic trophoblast lineage potential in embryonic stem cells. Genes Dev. 2009, 23:2507-2520.