Dissecting the role of H3K64me3 in mouse pericentromeric heterochromatin

Nature Communications

Volumn 4, Issue , 2013, Pages

  Lange, Ulrike C ^a   Siebert, Stéphanie ^b   Wossidlo, Mark ^c   Weiss, Thomas ^a   Ziegler Birling, Céline ^b   Walter, Jörn ^d   Torres Padilla, Maria Elena ^b   Daujat, Sylvain ^b   Schneider, Robert ^b  

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

^b INSERM   (France)

^c SAARLAND UNIVERSITY   (Germany)

^d STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA METHYLTRANSFERASE 1; DNA METHYLTRANSFERASE 3A; DNA METHYLTRANSFERASE 3B; H3K64ME3 PROTEIN; HETEROCHROMATIN PROTEIN 1; HISTONE METHYLTRANSFERASE; UNCLASSIFIED DRUG;

BIOCHEMISTRY; CHROMOSOME; ENZYME ACTIVITY; GENOME; METHYLATION; PROTEIN; RODENT;

ANIMAL CELL; ANIMAL CELL CULTURE; ARTICLE; CELL CYCLE PHASE; CELL SYNCHRONIZATION; CENTROMERE; CONSTITUTIVE HETEROCHROMATIN; CONTROLLED STUDY; DNA HISTONE INTERACTION; DNA METHYLATION; DNA MODIFICATION; EMBRYO; EMBRYONIC STEM CELL; ENZYME ACTIVITY; HETEROCHROMATIN; IMMUNOFLUORESCENCE; IN VITRO STUDY; INTERSPERSED REPEAT; MOUSE; NONHUMAN; NUCLEOSOME; WESTERN BLOTTING;

EID: 84881355049     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms3233     Document Type: Article

References (52)

1. Allis, C. D. & J., T. Danny Reinberg. Epigenetics (Cold Spring Harbor Laboratory Press, 2009).
2. Grewal, S. I. & Jia, S. Heterochromatin revisited. Nat. Rev. Genet. 8, 35-46 (2007). (Pubitemid 46006048)
3. Martens, J. H. et al. The profile of repeat-associated histone lysine methylation states in the mouse epigenome. EMBO J. 24, 800-812 (2005). (Pubitemid 40396109)
4. Kazazian, Jr. H. H. Mobile elements: drivers of genome evolution. Science 303, 1626-1632 (2004). (Pubitemid 38338313)
5. Maison, C. & Almouzni, G. HP1 and the dynamics of heterochromatin maintenance. Nat. Rev. Mol. Cell. Biol. 5, 296-304 (2004). (Pubitemid 38480610)
6. Peng, J. C. & Karpen, G. H. Epigenetic regulation of heterochromatic DNA stability. Curr. Opin. Genet. Dev. 18, 204-211 (2008). (Pubitemid 351749828)
7. Joseph, A., Mitchell, A. R. & Miller, O. J. The organization of the mouse satellite DNA at centromeres. Exp. Cell. Res. 183, 494-500 (1989). (Pubitemid 19218506)
8. Kuznetsova, I., Podgornaya, O. & Ferguson-Smith, M. A. High-resolution organization of mouse centromeric and pericentromeric DNA. Cytogenet. Genome. Res. 112, 248-255 (2006). (Pubitemid 43260753)
9. Guenatri, M., Bailly, D., Maison, C. & Almouzni, G. Mouse centric and pericentric satellite repeats form distinct functional heterochromatin. J. Cell Biol. 166, 493-505 (2004). (Pubitemid 39097169)
10. Daujat, S. et al. H3K64 trimethylation marks heterochromatin and is dynamically remodeled during developmental reprogramming. Nat. Struct. Mol. Biol. 16, 777-781 (2009).
11. Probst, A. V. & Almouzni, G. Heterochromatin establishment in the context of genome-wide epigenetic reprogramming. Trends Genet. 27, 177-185 (2011).
12. Bannister, A. J. et al. Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature 410, 120-124 (2001). (Pubitemid 32225848)
13. Lachner, M., O'Carroll, D., Rea, S., Mechtler, K. & Jenuwein, T. Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature 410, 116-120 (2001). (Pubitemid 32225847)
14. Lehnertz, B. et al. Suv39h-mediated histone H3 lysine 9 methylation directs DNA methylation to major satellite repeats at pericentric heterochromatin. Curr. Biol. 13, 1192-1200 (2003). (Pubitemid 36872941)
15. Schotta, G. et al. A silencing pathway to induce H3-K9 and H4-K20 trimethylation at constitutive heterochromatin. Genes Dev. 18, 1251-1262 (2004). (Pubitemid 38720593)
16. O'Carroll, D. et al. Isolation and characterization of Suv39h2, a second histone H3 methyltransferase gene that displays testis-specific expression. Mol. Cell. Biol. 20, 9423-9433 (2000). (Pubitemid 32246126)
17. Peters, A. H. et al. Loss of the Suv39h histone methyltransferases impairs mammalian heterochromatin and genome stability. Cell 107, 323-337 (2001). (Pubitemid 33049976)
18. Rea, S. et al. Regulation of chromatin structure by site-specific histone H3 methyltransferases. Nature 406, 593-599 (2000). (Pubitemid 30641039)
19. Eymery, A., Callanan, M. & Vourc'h, C. The secret message of heterochromatin: new insights into the mechanisms and function of centromeric and pericentric repeat sequence transcription. Int. J. Dev. Biol. 53, 259-268 (2009).
20. Grewal, S. I. & Elgin, S. C. Transcription and RNA interference in the formation of heterochromatin. Nature 447, 399-406 (2007). (Pubitemid 46816745)
21. Hahn, M. et al. Suv4-20h2 mediates chromatin compaction and is important for cohesin recruitment to heterochromatin. Genes Dev. 27, 859-872 (2013).
22. Aagaard, L. et al. Functional mammalian homologues of the Drosophila PEVmodifier Su(var)3-9 encode centromere-associated proteins which complex with the heterochromatin component M31. EMBO J. 18, 1923-1938 (1999). (Pubitemid 29158536)
23. Fuks, F. et al. The methyl-CpG-binding protein MeCP2 links DNA methylation to histone methylation. J. Biol. Chem. 278, 4035-4040 (2003). (Pubitemid 36801137)
24. Jones, P. L. et al. Methylated DNA and MeCP2 recruit histone deacetylase to repress transcription. Nat. Genet. 19, 187-191 (1998). (Pubitemid 28248804)
25. Nan, X. et al. Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature 393, 386-389 (1998). (Pubitemid 28269714)
26. Reik, W., Dean, W. & Walter, J. Epigenetic reprogramming in mammalian development. Science 293, 1089-1093 (2001). (Pubitemid 32758081)
27. Surani, M. A., Hayashi, K. & Hajkova, P. Genetic and epigenetic regulators of pluripotency. Cell 128, 747-762 (2007). (Pubitemid 46273582)
28. Mayer, W., Niveleau, A.,Walter, J., Fundele, R. & Haaf, T. Demethylation of the zygotic paternal genome. Nature 403, 501-502 (2000). (Pubitemid 30082186)
29. Oswald, J. et al. Active demethylation of the paternal genome in the mouse zygote. Curr. Biol. 10, 475-478 (2000). (Pubitemid 30247337)
30. Smith, Z. D. et al. A unique regulatory phase of DNA methylation in the early mammalian embryo. Nature 484, 339-344 (2012).
31. Santos, F., Hendrich, B., Reik, W. & Dean, W. Dynamic reprogramming of DNA methylation in the early mouse embryo. Dev. Biol. 241, 172-182 (2002). (Pubitemid 34066770)
32. Muto, M. et al. Targeted disruption of Np95 gene renders murine embryonic stem cells hypersensitive to DNA damaging agents and DNA replication blocks. J. Biol. Chem. 277, 34549-34555 (2002).
33. Tsumura, A. et al. Maintenance of self-renewal ability of mouse embryonic stem cells in the absence of DNA methyltransferases Dnmt1, Dnmt3a and Dnmt3b. Genes. Cells 11, 805-814 (2006). (Pubitemid 43923351)
34. Bostick, M. et al. UHRF1 plays a role in maintaining DNA methylation in mammalian cells. Science 317, 1760-1764 (2007). (Pubitemid 47461842)
35. Sharif, J. et al. The SRA protein Np95 mediates epigenetic inheritance by recruiting Dnmt1 to methylated DNA. Nature 450, 908-912 (2007). (Pubitemid 350231331)
36. Arand, J. et al. In vivo control of CpG and Non-CpG DNA methylation by DNA methyltransferases. PLoS Genet. 8, e1002750 (2012).
37. Wossidlo, M. et al. 5-Hydroxymethylcytosine in the mammalian zygote is linked with epigenetic reprogramming. Nat. Commun. 2, 241 (2011).
38. Kourmouli, N. et al. Heterochromatin and tri-methylated lysine 20 of histone H4 in animals. J. Cell Sci. 117, 2491-2501 (2004). (Pubitemid 38877845)
39. Singh, P. B. HP1 proteins-what is the essential interaction? Genetika 46, 1424-1429 (2010).
40. Dialynas, G. K. et al. Plasticity of HP1 proteins in mammalian cells. J. Cell. Sci. 120, 3415-3424 (2007). (Pubitemid 350028349)
41. Mosch, K., Franz, H., Soeroes, S., Singh, P. B. & Fischle, W. HP1 recruits activity-dependent neuroprotective protein to H3K9me3 marked pericentromeric heterochromatin for silencing of major satellite repeats. PLoS One 6, e15894 (2011).
42. Kourmouli, N., Sun, Y. M., van der Sar, S., Singh, P. B. & Brown, J. P. Epigenetic regulation of mammalian pericentric heterochromatin in vivo by HP1. Biochem. Biophys. Res. Commun. 337, 901-907 (2005). (Pubitemid 41446999)
43. Cloos, P. A. et al. The putative oncogene GASC1 demethylates tri-and dimethylated lysine 9 on histone H3. Nature 442, 307-311 (2006). (Pubitemid 44114906)
44. Iwamori, N., Zhao, M., Meistrich, M. L. & Matzuk, M. M. The testis-enriched histone demethylase, KDM4D, regulates methylation of histone H3 lysine 9 during spermatogenesis in the mouse but is dispensable for fertility. Biol. Reprod. 84, 1225-1234 (2011).
45. Whetstine, J. R. et al. Reversal of histone lysine trimethylation by the JMJD2 family of histone demethylases. Cell 125, 467-481 (2006).
46. Cosgrove, M. S., Boeke, J. D. & Wolberger, C. Regulated nucleosome mobility and the histone code. Nat. Struct. Mol. Biol. 11, 1037-1043 (2004). (Pubitemid 39453330)
47. Mersfelder, E. L. & Parthun, M. R. The tale beyond the tail: histone core domain modifications and the regulation of chromatin structure. Nucleic Acids Res. 34, 2653-2662 (2006). (Pubitemid 43985628)
48. Tropberger, P. & Schneider, R. Going global: novel histone modifications in the globular domain of H3. Epigenetics 5, 112-117 (2010).
49. Huang, C. et al. Dual-specificity histone demethylase KIAA1718 (KDM7A) regulates neural differentiation through FGF4. Cell Res. 20, 154-165 (2010).
50. Klose, R. J., Kallin, E. M. & Zhang, Y. JmjC-domain-containing proteins and histone demethylation. Nat. Rev. Genet. 7, 715-727 (2006). (Pubitemid 44260007)
51. Darzynkiewicz, Z., Juan, G. & Bedner, E. Determining cell cycle stages by flow cytometry. Curr. Protoc. Cell. Biol. Chapter 8, Unit 8.4 (2001).
52. Dyer, P. N. et al. Reconstitution of nucleosome core particles from recombinant histones and DNA. Methods. Enzymol. 375, 23-44 (2004). (Pubitemid 38124858)