Continuous Histone Replacement by Hira Is Essential for Normal Transcriptional Regulation and De Novo DNA Methylation during Mouse Oogenesis

Molecular Cell

Volumn 60, Issue 4, 2015, Pages 611-625

  Nashun, Buhe ^a   Hill, Peter W S ^a   Smallwood, Sebastien A ^b   Dharmalingam, Gopuraja ^a   Amouroux, Rachel ^a   Clark, Stephen J ^b   Sharma, Vineet ^a   Ndjetehe, Elodie ^a   Pelczar, Pawel ^c,e   Festenstein, Richard J ^a   Kelsey, Gavin ^b,d   Hajkova, Petra ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b BABRAHAM INSTITUTE   (United Kingdom)

^c UNIVERSITY OF ZURICH   (Switzerland)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^e UNIVERSITY OF BASEL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; CRE RECOMBINASE; DEOXYRIBONUCLEASE I; DNA; DNA METHYLTRANSFERASE 3A; HISTONE H2A; HISTONE H2B; HISTONE H3; HISTONE H3.3 CHAPERONE HIRA; HISTONE H4; MESSENGER RNA; PROTAMINE; UNCLASSIFIED DRUG; CELL CYCLE PROTEIN; CHROMATIN; HIRA PROTEIN, MOUSE; HISTONE; TRANSCRIPTION FACTOR;

ANIMAL CELL; ARTICLE; CELL ACTIVATION; CELL COUNT; CELL CYCLE ARREST; CELL DEATH; CELL PROLIFERATION; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN STRUCTURE; CONTROLLED STUDY; CPG ISLAND; DNA DAMAGE; DNA METHYLATION; DOWN REGULATION; EMBRYO; EMBRYO DEVELOPMENT; ENZYME ACTIVITY; FEMALE; FERTILIZATION IN VITRO; GENE ACTIVATION; GENE EXPRESSION; GENE INACTIVATION; GENE SILENCING; GENETIC RECOMBINATION; GENETIC TRANSCRIPTION; GENOME; GERMINAL VESICLE; HISTONE MODIFICATION; HOMEOSTASIS; IN VITRO STUDY; IN VIVO STUDY; MEIOSIS; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; NUCLEAR REPROGRAMMING; OOCYTE; OOCYTE DEVELOPMENT; OOCYTE MATURATION; OVARY FOLLICLE DEVELOPMENT; PERINATAL PERIOD; PHENOTYPE; PROPHASE; PROTEIN ANALYSIS; PROTEIN DEPLETION; PROTEIN EXPRESSION; RNA SEQUENCE; STEADY STATE; TRANSCRIPTION ELONGATION; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; TURNOVER TIME; UPREGULATION; ANIMAL; CHROMATIN; FERTILIZATION; GENE EXPRESSION REGULATION; GENETICS; METABOLISM;

ANIMALS; CELL CYCLE PROTEINS; CHROMATIN; DNA METHYLATION; FEMALE; FERTILIZATION; GENE EXPRESSION REGULATION; HISTONE CHAPERONES; HISTONES; MICE; OOCYTES; OOGENESIS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 84947742475     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2015.10.010     Document Type: Article

References (53)

1. Adam S., Polo S.E., Almouzni G. Transcription recovery after DNA damage requires chromatin priming by the H3.3 histone chaperone HIRA. Cell 2013, 155:94-106.
2. Akiyama T., Suzuki O., Matsuda J., Aoki F. Dynamic replacement of histone H3 variants reprograms epigenetic marks in early mouse embryos. PLoS Genet. 2011, 7:e1002279.
3. Anderson H.E., Wardle J., Korkut S.V., Murton H.E., López-Maury L., Bähler J., Whitehall S.K. The fission yeast HIRA histone chaperone is required for promoter silencing and the suppression of cryptic antisense transcripts. Mol. Cell. Biol. 2009, 29:5158-5167.
4. 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.
5. Baubec T., Colombo D.F., Wirbelauer C., Schmidt J., Burger L., Krebs A.R., Akalin A., Schübeler D. Genomic profiling of DNA methyltransferases reveals a role for DNMT3B in genic methylation. Nature 2015, 520:243-247.
6. Blackwell C., Martin K.A., Greenall A., Pidoux A., Allshire R.C., Whitehall S.K. The Schizosaccharomyces pombe HIRA-like protein Hip1 is required for the periodic expression of histone genes and contributes to the function of complex centromeres. Mol. Cell. Biol. 2004, 24:4309-4320.
7. Burgess R.J., Zhang Z. Histone chaperones in nucleosome assembly and human disease. Nat. Struct. Mol. Biol. 2013, 20:14-22.
8. 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.
9. Chotalia M., Smallwood S.A., Ruf N., Dawson C., Lucifero D., Frontera M., James K., Dean W., Kelsey G. Transcription is required for establishment of germline methylation marks at imprinted genes. Genes Dev. 2009, 23:105-117.
10. De La Fuente R. Chromatin modifications in the germinal vesicle (GV) of mammalian oocytes. Dev. Biol. 2006, 292:1-12.
11. Deal R.B., Henikoff J.G., Henikoff S. Genome-wide kinetics of nucleosome turnover determined by metabolic labeling of histones. Science 2010, 328:1161-1164.
12. Dhayalan A., Rajavelu A., Rathert P., Tamas R., Jurkowska R.Z., Ragozin S., Jeltsch A. The Dnmt3a PWWP domain reads histone 3 lysine 36 trimethylation and guides DNA methylation. J. Biol. Chem. 2010, 285:26114-26120.
13. 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.
14. Greenall A., Williams E.S., Martin K.A., Palmer J.M., Gray J., Liu C., Whitehall S.K. Hip3 interacts with the HIRA proteins Hip1 and Slm9 and is required for transcriptional silencing and accurate chromosome segregation. J. Biol. Chem. 2006, 281:8732-8739.
15. Guo X., Wang L., Li J., Ding Z., Xiao J., Yin X., He S., Shi P., Dong L., Li G., et al. Structural insight into autoinhibition and histone H3-induced activation of DNMT3A. Nature 2015, 517:640-644.
16. Gurard-Levin Z.A., Quivy J.P., Almouzni G. Histone chaperones: assisting histone traffic and nucleosome dynamics. Annu. Rev. Biochem. 2014, 83:487-517.
17. Hajkova P., Jeffries S.J., Lee C., Miller N., Jackson S.P., Surani M.A. Genome-wide reprogramming in the mouse germ line entails the base excision repair pathway. Science 2010, 329:78-82.
18. Hödl M., Basler K. Transcription in the absence of histone H3.3. Curr. Biol. 2009, 19:1221-1226.
19. Hoek M., Stillman B. Chromatin assembly factor 1 is essential and couples chromatin assembly to DNA replication in vivo. Proc. Natl. Acad. Sci. USA 2003, 100:12183-12188.
20. Inoue A., Zhang Y. Nucleosome assembly is required for nuclear pore complex assembly in mouse zygotes. Nat. Struct. Mol. Biol. 2014, 21:609-616.
21. Kaneda M., Okano M., Hata K., Sado T., Tsujimoto N., Li E., Sasaki H. Essential role for de novo DNA methyltransferase Dnmt3a in paternal and maternal imprinting. Nature 2004, 429:900-903.
22. Kobayashi H., Sakurai T., Imai M., Takahashi N., Fukuda A., Yayoi O., Sato S., Nakabayashi K., Hata K., Sotomaru Y., et al. Contribution of intragenic DNA methylation in mouse gametic DNA methylomes to establish oocyte-specific heritable marks. PLoS Genet. 2012, 8:e1002440.
23. 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.
24. Lan Z.J., Xu X., Cooney A.J. Differential oocyte-specific expression of Cre recombinase activity in GDF-9-iCre, Zp3cre, and Msx2Cre transgenic mice. Biol. Reprod. 2004, 71:1469-1474.
25. Li R., Albertini D.F. The road to maturation: somatic cell interaction and self-organization of the mammalian oocyte. Nat. Rev. Mol. Cell Biol. 2013, 14:141-152.
26. Lin C.J., Conti M., Ramalho-Santos M. Histone variant H3.3 maintains a decondensed chromatin state essential for mouse preimplantation development. Development 2013, 140:3624-3634.
27. Lin C.J., Koh F.M., Wong P., Conti M., Ramalho-Santos M. Hira-mediated H3.3 incorporation is required for DNA replication and ribosomal RNA transcription in the mouse zygote. Dev. Cell 2014, 30:268-279.
28. Ljungman M., Hanawalt P.C. Efficient protection against oxidative DNA damage in chromatin. Mol. Carcinog. 1992, 5:264-269.
29. Loppin B., Bonnefoy E., Anselme C., Laurençon A., Karr T.L., Couble P. The histone H3.3 chaperone HIRA is essential for chromatin assembly in the male pronucleus. Nature 2005, 437:1386-1390.
30. Maze I., Noh K.M., Soshnev A.A., Allis C.D. Every amino acid matters: essential contributions of histone variants to mammalian development and disease. Nat. Rev. Genet. 2014, 15:259-271.
31. Maze I., Wenderski W., Noh K.M., Bagot R.C., Tzavaras N., Purushothaman I., Elsässer S.J., Guo Y., Ionete C., Hurd Y.L., et al. Critical Role of Histone Turnover in Neuronal Transcription and Plasticity. Neuron 2015, 87:77-94.
32. Mito Y., Henikoff J.G., Henikoff S. Genome-scale profiling of histone H3.3 replacement patterns. Nat. Genet. 2005, 37:1090-1097.
33. Nashun B., Yukawa M., Liu H., Akiyama T., Aoki F. Changes in the nuclear deposition of histone H2A variants during pre-implantation development in mice. Development 2010, 137:3785-3794.
34. Pan H., O'brien M.J., Wigglesworth K., Eppig J.J., Schultz R.M. Transcript profiling during mouse oocyte development and the effect of gonadotropin priming and development in vitro. Dev. Biol. 2005, 286:493-506.
35. 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.
36. Polo S.E., Roche D., Almouzni G. New histone incorporation marks sites of UV repair in human cells. Cell 2006, 127:481-493.
37. Ransom M., Dennehey B.K., Tyler J.K. Chaperoning histones during DNA replication and repair. Cell 2010, 140:183-195.
38. Ray-Gallet D., Quivy J.P., Scamps C., Martini E.M.D., Lipinski M., Almouzni G. HIRA is critical for a nucleosome assembly pathway independent of DNA synthesis. Mol. Cell 2002, 9:1091-1100.
39. Sakai A., Schwartz B.E., Goldstein S., Ahmad K. Transcriptional and developmental functions of the H3.3 histone variant in Drosophila. Curr. Biol. 2009, 19:1816-1820.
40. Santenard A., Ziegler-Birling C., Koch M., Tora L., Bannister A.J., Torres-Padilla M.E. Heterochromatin formation in the mouse embryo requires critical residues of the histone variant H3.3. Nat. Cell Biol. 2010, 12:853-862.
41. Shirane K., Toh H., Kobayashi H., Miura F., Chiba H., Ito T., Kono T., Sasaki H. Mouse oocyte methylomes at base resolution reveal genome-wide accumulation of non-CpG methylation and role of DNA methyltransferases. PLoS Genet. 2013, 9:e1003439.
42. Smallwood S.A., Kelsey G. De novo DNA methylation: a germ cell perspective. Trends Genet. 2012, 28:33-42.
43. Smallwood S.A., Tomizawa S., Krueger F., Ruf N., Carli N., Segonds-Pichon A., Sato S., Hata K., Andrews S.R., Kelsey G. Dynamic CpG island methylation landscape in oocytes and preimplantation embryos. Nat. Genet. 2011, 43:811-814.
44. Smallwood S.A., Lee H.J., Angermueller C., Krueger F., Saadeh H., Peat J., Andrews S.R., Stegle O., Reik W., Kelsey G. Single-cell genome-wide bisulfite sequencing for assessing epigenetic heterogeneity. Nat. Methods 2014, 11:817-820.
45. Tagami H., Ray-Gallet D., Almouzni G., Nakatani Y. Histone H3.1 and H3.3 complexes mediate nucleosome assembly pathways dependent or independent of DNA synthesis. Cell 2004, 116:51-61.
46. Tang M.C., Jacobs S.A., Mattiske D.M., Soh Y.M., Graham A.N., Tran A., Lim S.L., Hudson D.F., Kalitsis P., O'Bryan M.K., et al. Contribution of the two genes encoding histone variant h3.3 to viability and fertility in mice. PLoS Genet. 2015, 11:e1004964.
47. Teves S.S., Weber C.M., Henikoff S. Transcribing through the nucleosome. Trends Biochem. Sci. 2014, 39:577-586.
48. Tomizawa S., Nowacka-Woszuk J., Kelsey G. DNA methylation establishment during oocyte growth: mechanisms and significance. Int. J. Dev. Biol. 2012, 56:867-875.
49. Trapnell C., Williams B.A., Pertea G., Mortazavi A., Kwan G., van Baren M.J., Salzberg S.L., Wold B.J., Pachter L. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat. Biotechnol. 2010, 28:511-515.
50. Veselovska L., Smallwood S.A., Saadeh H., Stewart K.R., Krueger F., Maupetit-Méhouas S., Arnaud P., Tomizawa S., Andrews S., Kelsey G. Deep sequencing and de novo assembly of the mouse oocyte transcriptome define the contribution of transcription to the DNA methylation landscape. Genome Biol. 2015, 16:209.
51. 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.
52. Wyrick J.J., Holstege F.C., Jennings E.G., Causton H.C., Shore D., Grunstein M., Lander E.S., Young R.A. Chromosomal landscape of nucleosome-dependent gene expression and silencing in yeast. Nature 1999, 402:418-421.
53. Yang X., Han H., De Carvalho D.D., Lay F.D., Jones P.A., Liang G. Gene body methylation can alter gene expression and is a therapeutic target in cancer. Cancer Cell 2014, 26:577-590.