Nucleosome-binding activities within JARID2 and EZH1 regulate the function of PRC2 on chromatin

Genes and Development

Volumn 27, Issue 24, 2013, Pages 2663-2677

  Son, Jinsook ^a   Shen, Steven S ^a   Margueron, Raphael ^a,b   Reinberg, Danny ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b INSTITUT CURIE   (France)

Author keywords

EZH1; EZH2; JARID2; Polycomb; PRC2

Indexed keywords

ENHANCER OF ZESTE HOMOLOG 1; JARID2 PROTEIN; NUCLEIC ACID BINDING PROTEIN; POLYCOMB REPRESSIVE COMPLEX 2; TRANSCRIPTION FACTOR EZH2; UNCLASSIFIED DRUG;

ARTICLE; CHROMATIN; CONTROLLED STUDY; MYOBLAST; NONHUMAN; NUCLEOSOME; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM;

EZH1; EZH2; JARID2; POLYCOMB; PRC2;

ANIMALS; CELL LINE; CHROMATIN; GENE KNOCKDOWN TECHNIQUES; HISTONE-LYSINE N-METHYLTRANSFERASE; HISTONES; MICE; MYOBLASTS; NIH 3T3 CELLS; NUCLEOSOMES; POLYCOMB REPRESSIVE COMPLEX 2; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY;

EID: 84890589760     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.225888.113     Document Type: Article

References (53)

1. Bernstein B. E, Mikkelsen TS, Xie X, Kamal M, Huebert DJ, Cuff J, Fry B, Meissner A, Wernig M, Plath K, et al. 2006. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125: 315-326.
2. Blais A., van Oevelen CJ, Margueron R, Acosta-Alvear D, Dynlacht B.D. 2007. Retinoblastoma tumor suppressor protein-dependent methylation of histone H3 lysine 27 is associated with irreversible cell cycle exit. J Cell Biol 179: 1399-1412.
3. Brown J. L, Mucci D, Whiteley M, Dirksen ML, Kassis JA. 1998. The Drosophila Polycomb group gene pleiohomeotic encodes a DNA binding protein with homology to the transcription factor YY1. Mol Cell 1: 1057-1064.
4. Cao R., Zhang Y. 2004. SUZ12 is required for both the histone methyltransferase activity and the silencing function of the EED-EZH2 complex. Mol Cell 15: 57-67.
5. Cao R., Wang L, Wang H, Xia L, Erdjument-Bromage H, Tempst P, Jones RS, Zhang Y. 2002. Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science 298: 1039-1043.
6. Christensen J., Agger K, Cloos PA, Pasini D, Rose S, Sennels L, Rappsilber J., Hansen KH, Salcini AE, Helin K. 2007. RBP2 belongs to a family of demethylases, specific for tri-and dimethylated lysine 4 on histone 3. Cell 128: 1063-1076.
7. Ezhkova E., Pasolli HA, Parker JS, Stokes N, Su IH, Hannon G, Tarakhovsky A., Fuchs E. 2009. Ezh2 orchestrates gene expression for the stepwise differentiation of tissue-specific stem cells. Cell 136: 1122-1135.
8. Ezhkova E., Lien WH, Stokes N, Pasolli HA, Silva JM, Fuchs E. 2011. EZH1 and EZH2 cogovern histone H3K27 trimethylation and are essential for hair follicle homeostasis and wound repair. Genes Dev 25: 485-498.
9. Gao Z., Zhang J, Bonasio R, Strino F, Sawai A, Parisi F, Kluger Y, Reinberg D. 2012. PCGF homologs, CBX proteins, and RYBP define functionally distinct PRC1 family complexes. Mol Cell 45: 344-356.
10. Herz H. M, Mohan M, Garrett AS, Miller C, Casto D, Zhang Y, Seidel C., Haug JS, Florens L, Washburn MP, et al. 2012. Polycomb repressive complex 2-dependent and-independent functions of Jarid2 in transcriptional regulation in Drosophila. Mol Cell Biol 32: 1683-1693.
11. Hidalgo I., Herrera-Merchan A, Ligos JM, Carramolino L, Nunez J, Martinez F, Dominguez O, Torres M, Gonzalez S. 2012. Ezh1 is required for hematopoietic stem cell maintenance and prevents senescence-like cell cycle arrest. Cell Stem Cell 11: 649-662.
12. Jacobs J. J, van Lohuizen M. 1999. Cellular memory of transcriptional states by Polycomb-group proteins. Semin Cell Dev Biol 10: 227-235.
13. Jung J., Mysliwiec MR, Lee Y. 2005. Roles of JUMONJI in mouse embryonic development. Dev Dyn 232: 21-32.
14. Kaneko S., Li G, Son J, Xu CF, Margueron R, Neubert TA, Reinberg D. 2010. Phosphorylation of the PRC2 component Ezh2 is cell cycle-regulated and up-regulates its binding to ncRNA. Genes Dev 24: 2615-2620.
15. Kaneko S., Bonasio R, Saldana-Meyer R, Yoshida T, Son J, Nishino K., Umezawa A, Reinberg D. Interactions between JARID2 and noncoding RNAs regulate PRC2 recruitment to chromatin. Mol Cell (in press).
16. Kim T. G, Kraus JC, Chen J, Lee Y. 2003. JUMONJI, a critical factor for cardiac development, functions as a transcriptional repressor. J Biol Chem 278: 42247-42255.
17. Kim H., Kang K, Kim J. 2009. AEBP2 as a potential targeting protein for Polycomb repression complex PRC2. Nucleic Acids Res 37: 2940-2950.
18. Klose R. J, Yamane K, Bae Y, Zhang D, Erdjument-Bromage H, Tempst P., Wong J, Zhang Y. 2006. The transcriptional repressor JHDM3A demethylates trimethyl histone H3 lysine 9 and lysine 36. Nature 442: 312-316.
19. Kuzmichev A., Nishioka K, Erdjument-Bromage H, Tempst P, Reinberg D. 2002. Histone methyltransferase activity associated with a human multiprotein complex containing the Enhancer of Zeste protein. Genes Dev 16: 2893-2905.
20. Laible G., Wolf A, Dorn R, Reuter G, Nislow C, Lebersorger A, Popkin D., Pillus L, Jenuwein T. 1997. Mammalian homologues of the Polycomb-group gene Enhancer of zeste mediate gene silencing in Drosophila heterochromatin and at S. cerevisiae telomeres. EMBO J 16: 3219-3232.
21. Landeira D., Sauer S, Poot R, Dvorkina M, Mazzarella L, Jorgensen H. F, Pereira CF, Leleu M, Piccolo FM, Spivakov M, et al. 2010. Jarid2 is a PRC2 component in embryonic stem cells required for multi-lineage differentiation and recruitment of PRC1 and RNA Polymerase II to developmental regulators. Nat Cell Biol 12: 618-624.
22. Lee Y., Song AJ, Baker R, Micales B, Conway SJ, Lyons GE. 2000. Jumonji, a nuclear protein that is necessary for normal heart development. Circ Res 86: 932-938.
23. Lewis E.B. 1978. A gene complex controlling segmentation in Drosophila. Nature 276: 565-570.
24. Li G., Margueron R, Ku M, Chambon P, Bernstein BE, Reinberg D. 2010. Jarid2 and PRC2, partners in regulating gene expression. Genes Dev 24: 368-380.
25. Luger K., Rechsteiner TJ, Richmond TJ. 1999. Expression and purification of recombinant histones and nucleosome reconstitution. Methods Mol Biol 119: 1-16.
26. Margueron R., Reinberg D. 2011. The Polycomb complex PRC2 and its mark in life. Nature 469: 343-349.
27. Margueron R., Li G, Sarma K, Blais A, Zavadil J, Woodcock CL, Dynlacht B. D, Reinberg D. 2008. Ezh1 and Ezh2 maintain repressive chromatin through different mechanisms. Mol Cell 32: 503-518.
28. Margueron R., Justin N, Ohno K, Sharpe ML, Son J, Drury WJ 3rd, Voigt P, Martin SR, Taylor WR, De Marco V, et al. 2009. Role of the polycomb protein EED in the propagation of repressive histone marks. Nature 461: 762-767.
29. Mendenhall E. M, Koche RP, Truong T, Zhou VW, Issac B, Chi AS, Ku M, Bernstein BE. 2010. GC-rich sequence elements recruit PRC2 in mammalian ES cells. PLoS Genet 6: e1001244.
30. Mochizuki-Kashio M., Mishima Y, Miyagi S, Negishi M, Saraya A, Konuma T, Shinga J, Koseki H, Iwama A. 2011. Dependency on the polycomb gene Ezh2 distinguishes fetal from adult hematopoietic stem cells. Blood 118: 6553-6561.
31. Montgomery N. D, Yee D, Chen A, Kalantry S, Chamberlain SJ, Otte A. P, Magnuson T. 2005. The murine polycomb group protein Eed is required for global histone H3 lysine-27 methylation. Curr Biol 15: 942-947.
32. Murzina N. V, Pei XY, Zhang W, Sparkes M, Vicente-Garcia J, Pratap J. V, McLaughlin SH, Ben-Shahar TR, Verreault A, Luisi BF, et al. 2008. Structural basis for the recognition of histone H4 by the histone-chaperone RbAp46. Structure 16: 1077-1085.
33. O'Carroll D, Erhardt S, Pagani M, Barton SC, Surani MA, Jenuwein T. 2001. The polycomb-group gene Ezh2 is required for early mouse development. Mol Cell Biol 21: 4330-4336.
34. Pasini D., Bracken AP, Jensen MR, Lazzerini Denchi E, Helin K. 2004. Suz12 is essential for mouse development and for EZH2 histone methyltransferase activity. EMBO J 23: 4061-4071.
35. Pasini D., Bracken AP, Hansen JB, Capillo M, Helin K. 2007. The polycomb group protein Suz12 is required for embryonic stem cell differentiation. Mol Cell Biol 27: 3769-3779.
36. Pasini D., Cloos PA, Walfridsson J, Olsson L, Bukowski JP, Johansen J. V, Bak M, Tommerup N, Rappsilber J, Helin K. 2010. JARID2 regulates binding of the Polycomb repressive complex 2 to target genes in ES cells. Nature 464: 306-310.
37. Peng J. C, Valouev A, Swigut T, Zhang J, Zhao Y, Sidow A, Wysocka J. 2009. Jarid2/Jumonji coordinates control of PRC2 enzymatic activity and target gene occupancy in pluripotent cells. Cell 139: 1290-1302.
38. Rinn J. L, Kertesz M, Wang JK, Squazzo SL, Xu X, Brugmann SA, Goodnough L. H, Helms JA, Farnham PJ, Segal E, et al. 2007. Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs. Cell 129: 1311-1323.
39. Schmitges F. W, Prusty AB, Faty M, Stutzer A, Lingaraju GM, Aiwazian J., Sack R, Hess D, Li L, Zhou S, et al. 2011. Histone methylation by PRC2 is inhibited by active chromatin marks. Mol Cell 42: 330-341.
40. Schuettengruber B., Chourrout D, Vervoort M, Leblanc B, Cavalli G. 2007. Genome regulation by polycomb and trithorax proteins. Cell 128: 735-745.
41. Shen X., Liu Y, Hsu YJ, Fujiwara Y, Kim J, Mao X, Yuan GC, Orkin S.H. 2008. EZH1 mediates methylation on histone H3 lysine 27 and complements EZH2 in maintaining stem cell identity and executing pluripotency. Mol Cell 32: 491-502.
42. Shen X., Kim W, Fujiwara Y, Simon MD, Liu Y, Mysliwiec MR, Yuan G. C, Lee Y, Orkin SH. 2009. Jumonji modulates polycomb activity and self-renewal versus differentiation of stem cells. Cell 139: 1303-1314.
43. Simon M. D, Chu F, Racki LR, de la Cruz CC, Burlingame AL, Panning B., Narlikar GJ, Shokat KM. 2007. The site-specific installation of methyl-lysine analogs into recombinant histones. Cell 128: 1003-1012.
44. Stojic L., Jasencakova Z, Prezioso C, Stutzer A, Bodega B, Pasini D, Klingberg R, Mozzetta C, Margueron R, Puri PL, Schwarzer D., Helin K, Fischle W, Orlando V. 2011. Chromatin regulated interchange between polycomb repressive complex 2 (PRC2)-Ezh2 and PRC2-Ezh1 complexes controls myogenin activation in skeletal muscle cells. Epigenetics Chromatin 4: 16.
45. Takeuchi T., Watanabe Y, Takano-Shimizu T, Kondo S. 2006. Roles of jumonji and jumonji family genes in chromatin regulation and development. Dev Dyn 235: 2449-2459.
46. Tie F., Stratton CA, Kurzhals RL, Harte PJ. 2007. The N terminus of Drosophila ESC binds directly to histone H3 and is required for E(Z)-dependent trimethylation of H3 lysine 27. Mol Cell Biol 27: 2014-2026.
47. Vermaak D., Wade PA, Jones PL, Shi YB, Wolffe AP. 1999. Functional analysis of the SIN3-histone deacetylase RPD3-RbAp48-histone H4 connection in the Xenopus oocyte. Mol Cell Biol 19: 5847-5860.
48. Visser H. P, Gunster MJ, Kluin-Nelemans HC, Manders EM, Raaphorst F. M, Meijer CJ, Willemze R, Otte AP. 2001. The Polycomb group protein EZH2 is upregulated in proliferating, cultured human mantle cell lymphoma. Br J Haematol 112: 950-958.
49. Voigt P., Tee WW, Reinberg D. 2013. A double take on bivalent promoters. Genes Dev 27: 1318-1338.
50. Wang L., Brown JL, Cao R, Zhang Y, Kassis JA, Jones RS. 2004. Hierarchical recruitment of polycomb group silencing complexes. Mol Cell 14: 637-646.
51. Zhang Z., Jones A, Sun CW, Li C, Chang CW, Joo HY, Dai Q, Mysliwiec M. R, Wu LC, Guo Y, et al. 2011. PRC2 complexes with JARID2, MTF2, and esPRC2p48 in ES cells to modulate ES cell pluripotency and somatic cell reprogramming. Stem Cells 29: 229-240.
52. Zhao J., Sun BK, Erwin JA, Song JJ, Lee JT. 2008. Polycomb proteins targeted by a short repeat RNA to the mouse X chromosome. Science 322: 750-756.
53. Zhao J., Ohsumi TK, Kung JT, Ogawa Y, Grau DJ, Sarma K, Song JJ, Kingston RE, Borowsky M, Lee JT. 2010. Genome-wide identification of polycomb-associated RNAs by RIP-seq. Mol Cell 40: 939-953.