NAR Breakthrough Article: A dimeric state for PRC2

Nucleic Acids Research

Volumn 42, Issue 14, 2014, Pages 9236-9248

  Davidovich, Chen ^a   Goodrich, Karen J ^a   Gooding, Anne R ^a   Cech, Thomas R ^a  

^a UNIVERSITY OF COLORADO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EMBRYONIC ECTODERM DEVELOPMENT PROTEIN; POLYCOMB REPRESSIVE COMPLEX 2; RETINOBLASTOMA BINDING PROTEIN 4; RNA; TRANSCRIPTION FACTOR EZH2; HYBRID PROTEIN; MALTOSE BINDING PROTEIN;

ANIMAL CELL; ARTICLE; BACULOVIRUS EXPRESSION SYSTEM; CHROMATIN; CONTROLLED STUDY; DIMERIZATION; GEL PERMEATION CHROMATOGRAPHY; IMMUNOPRECIPITATION; LIGHT SCATTERING; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PURIFICATION; PROTEIN SUBUNIT; PROTEIN TRANSPORT; RNA BINDING; SF9 CELL LINE; ANIMAL; CHEMISTRY; GENETICS; HUMAN; ISOLATION AND PURIFICATION; METABOLISM; PROTEIN MULTIMERIZATION; SPODOPTERA;

ANIMALS; HUMANS; MALTOSE-BINDING PROTEINS; POLYCOMB REPRESSIVE COMPLEX 2; PROTEIN MULTIMERIZATION; RECOMBINANT FUSION PROTEINS; RNA; SF9 CELLS; SPODOPTERA;

EID: 84906220100     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku540     Document Type: Article

References (53)

1. Margueron, R. and Reinberg, D. (2011) The Polycomb complex PRC2 and its mark in life. Nature, 469, 343-349.
2. Simon, J.A. and Kingston, R.E. (2013) Occupying chromatin: Polycomb mechanisms for getting to genomic targets, stopping transcriptional traffic, and staying put. Mol. Cell, 49, 808-824.
3. Di Croce, L. and Helin, K. (2013) Transcriptional regulation by Polycomb group proteins. Nat. Struct. Mol. Biol., 20, 1147-1155.
4. Cao, R. and 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. Margueron, R., Justin, N., Ohno, K., Sharpe, M.L., Son, J., Drury, W.J. 3rd, Voigt, P., Martin, S.R., Taylor, W.R., De Marco, V. et al. (2009) Role of the polycomb protein EED in the propagation of repressive histone marks. Nature, 461, 762-767.
6. Xu, C., Bian, C., Yang, W., Galka, M., Ouyang, H., Chen, C., Qiu, W., Liu, H., Jones, A.E., MacKenzie, F. et al. (2010) Binding of different histone marks differentially regulates the activity and specificity of polycomb repressive complex 2 (PRC2). Proc. Natl. Acad. Sci. U.S.A., 107, 19266-19271.
7. Schmitges, F.W., Prusty, A.B., Faty, M., Stutzer, A., Lingaraju, G.M., 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.
8. Yuan, W., Xu, M., Huang, C., Liu, N., Chen, S. and Zhu, B. (2011) H3K36 methylation antagonizes PRC2-mediated H3K27 methylation. J. Biol. Chem., 286, 7983-7989.
9. Cao, R., Wang, L., Wang, H., Xia, L., Erdjument-Bromage, H., Tempst, P., Jones, R.S. and Zhang, Y. (2002) Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science, 298, 1039-1043.
10. Kim, H., Kang, K. and Kim, J. (2009) AEBP2 as a potential targeting protein for Polycomb Repression Complex PRC2. Nucleic Acids Res., 37, 2940-2950.
11. Schwartz, Y.B. and Pirrotta, V. (2007) Polycomb silencing mechanisms and the management of genomic programmes. Nat. Rev. Genet., 8, 9-22.
12. Cuddapah, S., Roh, T.Y., Cui, K., Jose, C.C., Fuller, M.T., Zhao, K. and Chen, X. (2012) A novel human polycomb binding site acts as a functional polycomb response element in Drosophila. PloS ONE, 7, e36365.
13. Sing, A., Pannell, D., Karaiskakis, A., Sturgeon, K., Djabali, M., Ellis, J., Lipshitz, H.D. and Cordes, S.P. (2009) A vertebrate Polycomb response element governs segmentation of the posterior hindbrain. Cell, 138, 885-897.
14. Woo, C.J., Kharchenko, P.V., Daheron, L., Park, P.J. and Kingston, R.E. (2010) A region of the human HOXD cluster that confers polycomb-group responsiveness. Cell, 140, 99-110.
15. Tsai, M.C., Manor, O., Wan, Y., Mosammaparast, N., Wang, J.K., Lan, F., Shi, Y., Segal, E. and Chang, H.Y. (2010) Long noncoding RNA as modular scaffold of histone modification complexes. Science, 329, 689-693.
16. Rinn, J.L., Kertesz, M., Wang, J.K., Squazzo, S.L., Xu, X., Brugmann, S.A., Goodnough, L.H., Helms, J.A., Farnham, P.J., Segal, E. et al. (2007) Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs. Cell, 129, 1311-1323.
17. Chu, C., Qu, K., Zhong, F.L., Artandi, S.E. and Chang, H.Y. (2011) Genomic maps of long noncoding RNA occupancy reveal principles of RNA-chromatin interactions. Mol. Cell, 44, 667-678.
18. Zhao, J., Sun, B.K., Erwin, J.A., Song, J.J. and Lee, J.T. (2008) Polycomb proteins targeted by a short repeat RNA to the mouse X chromosome. Science, 322, 750-756.
19. Kanhere, A., Viiri, K., Araujo, C.C., Rasaiyaah, J., Bouwman, R.D., Whyte, W.A., Pereira, C.F., Brookes, E., Walker, K., Bell, G.W. et al. (2010) Short RNAs are transcribed from repressed polycomb target genes and interact with polycomb repressive complex-2. Mol. Cell, 38, 675-688.
20. Zhao, J., Ohsumi, T.K., Kung, J.T., Ogawa, Y., Grau, D.J., Sarma, K., Song, J.J., Kingston, R.E., Borowsky, M. and Lee, J.T. (2010) Genome-wide identification of polycomb-associated RNAs by RIP-seq. Mol. Cell, 40, 939-953.
21. Khalil, A.M., Guttman, M., Huarte, M., Garber, M., Raj, A., Rivea Morales, D., Thomas, K., Presser, A., Bernstein, B.E., van Oudenaarden, A. et al. (2009) Many human large intergenic noncoding RNAs associate with chromatin-modifying complexes and affect gene expression. Proc. Natl. Acad. Sci. U.S.A., 106, 11667-11672.
22. Guttman, M., Donaghey, J., Carey, B.W., Garber, M., Grenier, J.K., Munson, G., Young, G., Lucas, A.B., Ach, R., Bruhn, L. et al. (2011) lincRNAs act in the circuitry controlling pluripotency and differentiation. Nature, 477, 295-300.
23. Davidovich, C., Zheng, L., Goodrich, K.J. and Cech, T.R. (2013) Promiscuous RNA binding by Polycomb repressive complex 2. Nat. Struct. Mol. Biol., 20, 1250-1257.
24. Kaneko, S., Li, G., Son, J., Xu, C.F., Margueron, R., Neubert, T.A. and 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.
25. Margueron, R., Li, G., Sarma, K., Blais, A., Zavadil, J., Woodcock, C.L., Dynlacht, B.D. and Reinberg, D. (2008) Ezh1 and Ezh2 maintain repressive chromatin through different mechanisms. Mol. Cell, 32, 503-518.
26. Casanova, M., Preissner, T., Cerase, A., Poot, R., Yamada, D., Li, X., Appanah, R., Bezstarosti, K., Demmers, J., Koseki, H. et al. (2011) Polycomblike 2 facilitates the recruitment of PRC2 Polycomb group complexes to the inactive X chromosome and to target loci in embryonic stem cells. Development, 138, 1471-1482.
27. Tie, F., Prasad-Sinha, J., Birve, A., Rasmuson-Lestander, A. and Harte, P.J. (2003) A 1-megadalton ESC/E(Z) complex from Drosophila that contains polycomblike and RPD3. Mol. Cell. Biol., 23, 3352-3362.
28. Kuzmichev, A., Margueron, R., Vaquero, A., Preissner, T.S., Scher, M., Kirmizis, A., Ouyang, X., Brockdorff, N., Abate-Shen, C., Farnham, P. et al. (2005) Composition and histone substrates of polycomb repressive group complexes change during cellular differentiation. Proc. Natl. Acad. Sci. U.S.A., 102, 1859-1864.
29. Ciferri, C., Lander, G.C., Maiolica, A., Herzog, F., Aebersold, R. and Nogales, E. (2012) Molecular architecture of human polycomb repressive complex 2. eLife, 1, e00005.
30. Nekrasov, M., Wild, B. and Muller, J. (2005) Nucleosome binding and histone methyltransferase activity of Drosophila PRC2. EMBO Reports, 6, 348-353.
31. Muller, J., Hart, C.M., Francis, N.J., Vargas, M.L., Sengupta, A., Wild, B., Miller, E.L., O'Connor, M.B., Kingston, R.E. and Simon, J.A. (2002) Histone methyltransferase activity of a Drosophila Polycomb group repressor complex. Cell, 111, 197-208.
32. Yuan, W., Wu, T., Fu, H., Dai, C., Wu, H., Liu, N., Li, X., Xu, M., Zhang, Z., Niu, T. et al. (2012) Dense chromatin activates Polycomb repressive complex 2 to regulate H3 lysine 27 methylation. Science, 337, 971-975.
33. Lu, Q. (2005) Seamless cloning and gene fusion. Trends Biotechnol., 23, 199-207.
34. Yin, J., Straight, P.D., McLoughlin, S.M., Zhou, Z., Lin, A.J., Golan, D.E., Kelleher, N.L., Kolter, R. and Walsh, C.T. (2005) Genetically encoded short peptide tag for versatile protein labeling by Sfp phosphopantetheinyl transferase. Proc. Natl. Acad. Sci. U.S.A., 102, 15815-15820.
35. Gupta, R.A., Shah, N., Wang, K.C., Kim, J., Horlings, H.M., Wong, D.J., Tsai, M.C., Hung, T., Argani, P., Rinn, J.L. et al. (2010) Long non-coding RNA HOTAIR reprograms chromatin state to promote cancer metastasis. Nature, 464, 1071-1076.
36. Ryder, S.P., Recht, M.I. and Williamson, J.R. (2008) Quantitative analysis of protein-RNA interactions by gel mobility shift. Methods Mol. Biol., 488, 99-115.
37. Kapust, R.B. and Waugh, D.S. (1999) Escherichia coli maltose-binding protein is uncommonly effective at promoting the solubility of polypeptides to which it is fused. Protein Sci., 8, 1668-1674.
38. Wen, J., Arakawa, T. and Philo, J.S. (1996) Size-exclusion chromatography with on-line light-scattering, absorbance, and refractive index detectors for studying proteins and their interactions. Analyt. Biochem., 240, 155-166.
39. Kaneko, S., Son, J., Shen, S.S., Reinberg, D. and Bonasio, R. (2013) PRC2 binds active promoters and contacts nascent RNAs in embryonic stem cells. Nat. Struct. Mol. Biol., 20, 1258-1264.
40. Ballare, C., Lange, M., Lapinaite, A., Martin, G.M., Morey, L., Pascual, G., Liefke, R., Simon, B., Shi, Y., Gozani, O. et al. (2012) Phf19 links methylated Lys36 of histone H3 to regulation of Polycomb activity. Nat. Struct. Mol. Biol. 19, 1257-1265.
41. Wu, L., Murat, P., Matak-Vinkovic, D., Murrell, A. and Balasubramanian, S. (2013) The binding interaction between long non-coding RNA HOTAIR and PRC2 proteins. Biochemistry.52, 9519-9527.
42. Ptashne, M. (1986) A Genetic Switch : Gene Control and Phage [Lambda]. Cell Press; Blackwell Scientific Publications, Cambridge, MA and Palo Alto, CA.
43. Senear, D.F. and Brenowitz, M. (1991) Determination of binding constants for cooperative site-specific protein-DNA interactions using the gel mobility-shift assay. J. Biol. Chem., 266, 13661-13671.
44. Hansen, K.H., Bracken, A.P., Pasini, D., Dietrich, N., Gehani, S.S., Monrad, A., Rappsilber, J., Lerdrup, M. and Helin, K. (2008) A model for transmission of the H3K27me3 epigenetic mark. Nat. Cell Biol., 10, 1291-1300.
45. Isono, K., Endo, T.A., Ku, M., Yamada, D., Suzuki, R., Sharif, J., Ishikura, T., Toyoda, T., Bernstein, B.E. and Koseki, H. (2013) SAM domain polymerization links subnuclear clustering of PRC1 to gene silencing. Dev. Cell, 26, 565-577.
46. Canzio, D., Chang, E.Y., Shankar, S., Kuchenbecker, K.M., Simon, M.D., Madhani, H.D., Narlikar, G.J. and Al-Sady, B. (2011) Chromodomain-mediated oligomerization of HP1 suggests a nucleosome-bridging mechanism for heterochromatin assembly. Mol. Cell, 41, 67-81.
47. Henikoff, S. and Shilatifard, A. (2011) Histone modification: cause or cog? Trends Genet., 27, 389-396.
48. Abel, K.J., Brody, L.C., Valdes, J.M., Erdos, M.R., McKinley, D.R., Castilla, L.H., Merajver, S.D., Couch, F.J., Friedman, L.S., Ostermeyer, E.A. et al. (1996) Characterization of EZH1, a human homolog of Drosophila Enhancer of zeste near BRCA1. Genomics, 37, 161-171.
49. Mousavi, K., Zare, H., Wang, A.H. and Sartorelli, V. (2012) Polycomb protein Ezh1 promotes RNA polymerase II elongation. Mol. Cell, 45, 255-262.
50. Shen, X., Liu, Y., Hsu, Y.J., Fujiwara, Y., Kim, J., Mao, X., Yuan, G.C. and 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.
51. Hidalgo, I., Herrera-Merchan, A., Ligos, J.M., Carramolino, L., Nunez, J., Martinez, F., Dominguez, O., Torres, M. and Gonzalez, S. (2012) Ezh1 is required for hematopoietic stem cell maintenance and prevents senescence-like cell cycle arrest. Cell Stem Cell, 11, 649-662.
52. Son, J., Shen, S.S., Margueron, R. and Reinberg, D. (2013) Nucleosome-binding activities within JARID2 and EZH1 regulate the function of PRC2 on chromatin. Genes Dev., 27, 2663-2677.
53. Lee, J.T. (2011) Gracefully ageing at 50, X-chromosome inactivation becomes a paradigm for RNA and chromatin control. Nat. Rev. Mol. Cell Biol., 12, 815-826.