Redundant Mechanisms to Form Silent Chromatin at Pericentromeric Regions Rely on BEND3 and DNA Methylation

Molecular Cell

Volumn 56, Issue 4, 2014, Pages 580-594

  Saksouk, Nehmé ^a   Barth, Teresa K ^b   Ziegler Birling, Celine ^c   Olova, Nelly ^d   Nowak, Agnieszka ^a   Rey, Elodie ^a   Mateos Langerak, Julio ^a   Urbach, Serge ^e   Reik, Wolf ^d,f,g   Torres Padilla, Maria Elena ^c   Imhof, Axel ^b   Déjardin, Jérome ^a  

^a INSTITUTE OF HUMAN GENETICS   (France)

^b UNIVERSITY OF MUNICH   (Germany)

^c INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

^d BABRAHAM INSTITUTE   (United Kingdom)

^e INSTITUT DE GÉNOMIQUE FONCTIONNELLE   (France)

^f WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^g UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DNA BINDING PROTEIN; DNA METHYLTRANSFERASE 1; DNA METHYLTRANSFERASE 3A; DNA METHYLTRANSFERASE 3B; H3 LYSINE 27 TRIMETHYLATION; HISTONE H3; PROTEIN BEND3; UNCLASSIFIED DRUG; BEND3 PROTEIN, MOUSE; DNA (CYTOSINE 5) METHYLTRANSFERASE; HETEROCHROMATIN; HISTONE; MICROSATELLITE DNA; NUCLEAR PROTEIN; PROTEOME; UHRF1 PROTEIN, MOUSE;

ANIMAL CELL; ARTICLE; CENTROMERE; CONSTITUTIVE HETEROCHROMATIN; DNA METHYLATION; EMBRYONIC STEM CELL; EPIGENETICS; NONHUMAN; PROTEIN ANALYSIS; PURIFICATION; QUANTITATIVE ANALYSIS; SIGNAL TRANSDUCTION; 129 MOUSE; ANIMAL; C57BL MOUSE; CELL CULTURE; CELL NUCLEUS; GENE LOCUS; GENE SILENCING; GENETICS; HETEROCHROMATIN; KNOCKOUT MOUSE; METABOLISM; PHYSIOLOGY;

ANIMALS; CELL NUCLEUS; CELLS, CULTURED; CENTROMERE; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; DNA METHYLATION; DNA-BINDING PROTEINS; EMBRYONIC STEM CELLS; GENE SILENCING; GENETIC LOCI; HETEROCHROMATIN; HISTONES; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROSATELLITE REPEATS; NUCLEAR PROTEINS; PROTEOME;

EID: 84912127424     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2014.10.001     Document Type: Article

References (63)

1. Adams R.R., Maiato H., Earnshaw W.C., Carmena M. Essential roles of Drosophila inner centromere protein (INCENP) and aurora B in histone H3 phosphorylation, metaphase chromosome alignment, kinetochore disjunction, and chromosome segregation. J.Cell Biol. 2001, 153:865-880.
2. Arand J., Spieler D., Karius T., Branco M.R., Meilinger D., Meissner A., Jenuwein T., Xu G., Leonhardt H., Wolf V., Walter J. Invivo control of CpG and non-CpG DNA methylation by DNA methyltransferases. PLoS Genet. 2012, 8:e1002750.
3. Bachman K.E., Rountree M.R., Baylin S.B. Dnmt3a and Dnmt3b are transcriptional repressors that exhibit unique localization properties to heterochromatin. J.Biol. Chem. 2001, 276:32282-32287.
4. Blackledge N.P., Farcas A.M., Kondo T., King H.W., McGouran J.F., Hanssen L.L., Ito S., Cooper S., Kondo K., Koseki Y., et al. Variant PRC1 complex-dependent H2A ubiquitylation drives PRC2 recruitment and polycomb domain formation. Cell 2014, 157:1445-1459.
5. Blasco M.A. The epigenetic regulation of mammalian telomeres. Nat. Rev. Genet. 2007, 8:299-309.
6. Blewitt M.E., Gendrel A.V., Pang Z., Sparrow D.B., Whitelaw N., Craig J.M., Apedaile A., Hilton D.J., Dunwoodie S.L., Brockdorff N., et al. SmcHD1, containing a structural-maintenance-of-chromosomes hinge domain, has a critical role in X inactivation. Nat. Genet. 2008, 40:663-669.
7. Bonaldi T., Regula J.T., Imhof A. The use of mass spectrometry for the analysis of histone modifications. Methods Enzymol. 2004, 377:111-130.
8. Bostick M., Kim J.K., Estève P.O., Clark A., Pradhan S., Jacobsen S.E. UHRF1 plays a role in maintaining DNA methylation in mammalian cells. Science 2007, 317:1760-1764.
9. Boyer L.A., Plath K., Zeitlinger J., Brambrink T., Medeiros L.A., Lee T.I., Levine S.S., Wernig M., Tajonar A., Ray M.K., et al. Polycomb complexes repress developmental regulators in murine embryonic stem cells. Nature 2006, 441:349-353.
10. Brown K.E., Guest S.S., Smale S.T., Hahm K., Merkenschlager M., Fisher A.G. Association of transcriptionally silent genes with Ikaros complexes at centromeric heterochromatin. Cell 1997, 91:845-854.
11. Bullwinkel J., Baron-Lühr B., Lüdemann A., Wohlenberg C., Gerdes J., Scholzen T. Ki-67 protein is associated with ribosomal RNA transcription in quiescent and proliferating cells. J.Cell. Physiol. 2006, 206:624-635.
12. Bulut-Karslioglu A., Perrera V., Scaranaro M., de la Rosa-Velazquez I.A., van de Nobelen S., Shukeir N., Popow J., Gerle B., Opravil S., Pagani M., et al. A transcription factor-based mechanism for mouse heterochromatin formation. Nat. Struct. Mol. Biol. 2012, 19:1023-1030.
13. Carmena M., Wheelock M., Funabiki H., Earnshaw W.C. The chromosomal passenger complex (CPC): from easy rider to the godfather of mitosis. Nat. Rev. Mol. Cell Biol. 2012, 13:789-803.
14. Cooper S., Dienstbier M., Hassan R., Schermelleh L., Sharif J., Blackledge N.P., De Marco V., Elderkin S., Koseki H., Klose R., et al. Targeting polycomb to pericentric heterochromatin in embryonic stem cells reveals a role for H2AK119u1 in PRC2 recruitment. Cell Rep. 2014, 7:1456-1470.
15. Dai Q., Ren A., Westholm J.O., Serganov A.A., Patel D.J., Lai E.C. The BEN domain is a novel sequence-specific DNA-binding domain conserved in neural transcriptional repressors. Genes Dev. 2013, 27:602-614.
16. Déjardin J., Kingston R.E. Purification of proteins associated with specific genomic Loci. Cell 2009, 136:175-186.
17. Ehrlich M. DNA methylation in cancer: too much, but also too little. Oncogene 2002, 21:5400-5413.
18. Filion G.J., van Steensel B. Reassessing the abundance of H3K9me2 chromatin domains in embryonic stem cells. Nat. Genet. 2010, 42:4. author reply 5-6.
19. Fodor B.D., Shukeir N., Reuter G., Jenuwein T. Mammalian Su(var) genes in chromatin control. Annu. Rev. Cell Dev. Biol. 2010, 26:471-501.
20. Grewal S.I., Jia S. Heterochromatin revisited. Nat. Rev. Genet. 2007, 8:35-46.
21. He J., Shen L., Wan M., Taranova O., Wu H., Zhang Y. Kdm2b maintains murine embryonic stem cell status by recruiting PRC1 complex to CpG islands of developmental genes. Nat. Cell Biol. 2013, 15:373-384.
22. Heitz E. The heterochromatin of moss. Jahrb wiss Bot 1928, 762-818.
23. Iurlaro M., Ficz G., Oxley D., Raiber E.A., Bachman M., Booth M.J., Andrews S., Balasubramanian S., Reik W. A screen for hydroxymethylcytosine and formylcytosine binding proteins suggests functions in transcription and chromatin regulation. Genome Biol. 2013, 14:R119.
24. 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.
25. Kadauke S., Blobel G.A. Mitotic bookmarking by transcription factors. Epigenetics Chromatin 2013, 6:6.
26. Kalb R., Latwiel S., Baymaz H.I., Jansen P.W., Müller C.W., Vermeulen M., Müller J. Histone H2A monoubiquitination promotes histone H3 methylation in Polycomb repression. Nat. Struct. Mol. Biol. 2014, 21:569-571.
27. Kind J., Pagie L., Ortabozkoyun H., Boyle S., de Vries S.S., Janssen H., Amendola M., Nolen L.D., Bickmore W.A., van Steensel B. Single-cell dynamics of genome-nuclear lamina interactions. Cell 2013, 153:178-192.
28. Ku M., Koche R.P., Rheinbay E., Mendenhall E.M., Endoh M., Mikkelsen T.S., Presser A., Nusbaum C., Xie X., Chi A.S., et al. Genomewide analysis of PRC1 and PRC2 occupancy identifies two classes of bivalent domains. PLoS Genet. 2008, 4:e1000242.
29. Lehnertz B., Ueda Y., Derijck A.A.H.A., Braunschweig U., Perez-Burgos L., Kubicek S., Chen T., Li E., Jenuwein T., Peters A.H.F.M. Suv39h-mediated histone H3 lysine 9 methylation directs DNA methylation to major satellite repeats at pericentric heterochromatin. Curr. Biol. 2003, 13:1192-1200.
30. Mikkelsen T.S., Ku M., Jaffe D.B., Issac B., Lieberman E., Giannoukos G., Alvarez P., Brockman W., Kim T.K., Koche R.P., et al. Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 2007, 448:553-560.
31. Murakami H., Goto D.B., Toda T., Chen E.S., Grewal S.I., Martienssen R.A., Yanagida M. Ribonuclease activity of Dis3 is required for mitotic progression and provides a possible link between heterochromatin and kinetochore function. PLoS ONE 2007, 2:e317.
32. Nozawa R.S., Nagao K., Masuda H.T., Iwasaki O., Hirota T., Nozaki N., Kimura H., Obuse C. Human POGZ modulates dissociation of HP1alpha from mitotic chromosome arms through Aurora B activation. Nat. Cell Biol. 2010, 12:719-727.
33. Okano M., Bell D.W., Haber D.A., Li E. DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 1999, 99:247-257.
34. Ong S.E., Foster L.J., Mann M. Mass spectrometric-based approaches in quantitative proteomics. Methods 2003, 29:124-130.
35. Pasini D., Bracken A.P., Hansen J.B., Capillo M., Helin K. The polycomb group protein Suz12 is required for embryonic stem cell differentiation. Mol. Cell. Biol. 2007, 27:3769-3779.
36. Peng J.C., Karpen G.H. Epigenetic regulation of heterochromatic DNA stability. Curr. Opin. Genet. Dev. 2008, 18:204-211.
37. Peters A.H., O'Carroll D., Scherthan H., Mechtler K., Sauer S., Schöfer C., Weipoltshammer K., Pagani M., Lachner M., Kohlmaier A., et al. Loss of the Suv39h histone methyltransferases impairs mammalian heterochromatin and genome stability. Cell 2001, 107:323-337.
38. Peters A.H., Kubicek S., Mechtler K., O'Sullivan R.J., Derijck A.A., Perez-Burgos L., Kohlmaier A., Opravil S., Tachibana M., Shinkai Y., et al. Partitioning and plasticity of repressive histone methylation states in mammalian chromatin. Mol. Cell 2003, 12:1577-1589.
39. Puschendorf M., Terranova R., Boutsma E., Mao X., Isono K., Brykczynska U., Kolb C., Otte A.P., Koseki H., Orkin S.H., et al. PRC1 and Suv39h specify parental asymmetry at constitutive heterochromatin in early mouse embryos. Nat. Genet. 2008, 40:411-420.
40. Qin J., Whyte W.A., Anderssen E., Apostolou E., Chen H.H., Akbarian S., Bronson R.T., Hochedlinger K., Ramaswamy S., Young R.A., Hock H. The polycomb group protein L3mbtl2 assembles an atypical PRC1-family complex that is essential in pluripotent stem cells and early development. Cell Stem Cell 2012, 11:319-332.
41. Reynolds N., Salmon-Divon M., Dvinge H., Hynes-Allen A., Balasooriya G., Leaford D., Behrens A., Bertone P., Hendrich B. NuRD-mediated deacetylation of H3K27 facilitates recruitment of Polycomb Repressive Complex 2 to direct gene repression. EMBO J. 2012, 31:593-605.
42. Rosnoblet C., Vandamme J., Völkel P., Angrand P.O. Analysis of the human HP1 interactome reveals novel binding partners. Biochem. Biophys. Res. Commun. 2011, 413:206-211.
43. Rothbart S.B., Krajewski K., Nady N., Tempel W., Xue S., Badeaux A.I., Barsyte-Lovejoy D., Martinez J.Y., Bedford M.T., Fuchs S.M., et al. Association of UHRF1 with methylated H3K9 directs the maintenance of DNA methylation. Nat. Struct. Mol. Biol. 2012, 19:1155-1160.
44. Rountree M.R., Bachman K.E., Baylin S.B. DNMT1 binds HDAC2 and a new co-repressor, DMAP1, to form a complex at replication foci. Nat. Genet. 2000, 25:269-277.
45. Santos F., Peters A.H., Otte A.P., Reik W., Dean W. Dynamic chromatin modifications characterise the first cell cycle in mouse embryos. Dev. Biol. 2005, 280:225-236.
46. Sathyan K.M., Shen Z., Tripathi V., Prasanth K.V., Prasanth S.G. A BEN-domain-containing protein associates with heterochromatin and represses transcription. J.Cell Sci. 2011, 124:3149-3163.
47. Saurin A.J., Shiels C., Williamson J., Satijn D.P., Otte A.P., Sheer D., Freemont P.S. The human polycomb group complex associates with pericentromeric heterochromatin to form a novel nuclear domain. J.Cell Biol. 1998, 142:887-898.
48. Schotta G., Lachner M., Sarma K., Ebert A., Sengupta R., Reuter G., Reinberg D., Jenuwein T. A silencing pathway to induce H3-K9 and H4-K20 trimethylation at constitutive heterochromatin. Genes Dev. 2004, 18:1251-1262.
49. Sharif J., Muto M., Takebayashi S., Suetake I., Iwamatsu A., Endo T.A., Shinga J., Mizutani-Koseki Y., Toyoda T., Okamura K., et al. The SRA protein Np95 mediates epigenetic inheritance by recruiting Dnmt1 to methylated DNA. Nature 2007, 450:908-912.
50. Simon J.A., Kingston R.E. Occupying chromatin: Polycomb mechanisms for getting to genomic targets, stopping transcriptional traffic, and staying put. Mol. Cell 2013, 49:808-824.
51. Smith Z.D., Meissner A. DNA methylation: roles in mammalian development. Nat. Rev. Genet. 2013, 14:204-220.
52. Solovei I., Wang A.S., Thanisch K., Schmidt C.S., Krebs S., Zwerger M., Cohen T.V., Devys D., Foisner R., Peichl L., et al. LBR and lamin A/C sequentially tether peripheral heterochromatin and inversely regulate differentiation. Cell 2013, 152:584-598.
53. Strahl B.D., Allis C.D. The language of covalent histone modifications. Nature 2000, 403:41-45.
54. Tavares L., Dimitrova E., Oxley D., Webster J., Poot R., Demmers J., Bezstarosti K., Taylor S., Ura H., Koide H., et al. RYBP-PRC1 complexes mediate H2A ubiquitylation at polycomb target sites independently of PRC2 and H3K27me3. Cell 2012, 148:664-678.
55. Towbin B.D., González-Aguilera C., Sack R., Gaidatzis D., Kalck V., Meister P., Askjaer P., Gasser S.M. Step-wise methylation of histone H3K9 positions heterochromatin at the nuclear periphery. Cell 2012, 150:934-947.
56. Trojer P., Reinberg D. Facultative heterochromatin: is there a distinctive molecular signature?. Mol. Cell 2007, 28:1-13.
57. Trojer P., Cao A.R., Gao Z., Li Y., Zhang J., Xu X., Li G., Losson R., Erdjument-Bromage H., Tempst P., et al. L3MBTL2 protein acts in concert with PcG protein-mediated monoubiquitination of H2A to establish a repressive chromatin structure. Mol. Cell 2011, 42:438-450.
58. Tsumura A., Hayakawa T., Kumaki Y., Takebayashi S., Sakaue M., Matsuoka C., Shimotohno K., Ishikawa F., Li E., Ueda H.R., et al. Maintenance of self-renewal ability of mouse embryonic stem cells in the absence of DNA methyltransferases Dnmt1, Dnmt3a and Dnmt3b. Genes Cells 2006, 11:805-814.
59. Vissel B., Choo K.H. Mouse major (gamma) satellite DNA is highly conserved and organized into extremely long tandem arrays: implications for recombination between nonhomologous chromosomes. Genomics 1989, 5:407-414.
60. Voncken J.W., Schweizer D., Aagaard L., Sattler L., Jantsch M.F., van Lohuizen M. Chromatin-association of the Polycomb group protein BMI1 is cell cycle-regulated and correlates with its phosphorylation status. J.Cell Sci. 1999, 112:4627-4639.
61. Xie S., Jakoncic J., Qian C. UHRF1 double tudor domain and the adjacent PHD finger act together to recognize K9me3-containing histone H3 tail. J.Mol. Biol. 2012, 415:318-328.
62. Ye Q., Worman H.J. Interaction between an integral protein of the nuclear envelope inner membrane and human chromodomain proteins homologous to Drosophila HP1. J.Biol. Chem. 1996, 271:14653-14656.
63. Zhu Q., Pao G.M., Huynh A.M., Suh H., Tonnu N., Nederlof P.M., Gage F.H., Verma I.M. BRCA1 tumour suppression occurs via heterochromatin-mediated silencing. Nature 2011, 477:179-184.