An H3K36 Methylation-Engaging Tudor Motif of Polycomb-like Proteins Mediates PRC2 Complex Targeting

Molecular Cell

Volumn 49, Issue 3, 2013, Pages 571-582

  Cai, Ling ^a   Rothbart, Scott B ^a   Lu, Rui ^a   Xu, Bowen ^a   Chen, Wei Yi ^b   Tripathy, Ashutosh ^a   Rockowitz, Shira ^c   Zheng, Deyou ^c   Patel, Dinshaw J ^d   Allis, C David ^b   Strahl, Brian D ^a   Song, Jikui ^e   Wang, Gang Greg ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b ROCKEFELLER UNIVERSITY   (United States)

^c ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^d MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE H3; LYSINE; LYSINE 36; POLYCOMB GROUP PROTEIN; POLYCOMB LIKE PROTEIN; POLYCOMB REPRESSIVE COMPLEX 2; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CHROMATIN; CONTROLLED STUDY; GENE SILENCING; GENE TARGETING; METHYLATION; MOUSE; NONHUMAN; PLURIPOTENT STEM CELL; PROTEIN BINDING; PROTEIN STABILITY;

AMINO ACID MOTIFS; ANIMALS; CALORIMETRY; CARRIER PROTEINS; CELL DIFFERENTIATION; CELL NUCLEUS; CONSERVED SEQUENCE; DNA-BINDING PROTEINS; GENETIC COMPLEMENTATION TEST; GENETIC LOCI; HISTONES; HUMANS; LYSINE; METHYLATION; MICE; MODELS, MOLECULAR; NUCLEAR PROTEINS; PEPTIDES; PLURIPOTENT STEM CELLS; POLYCOMB REPRESSIVE COMPLEX 2; PROTEIN BINDING; PROTEIN TRANSPORT; STRUCTURE-ACTIVITY RELATIONSHIP; THERMODYNAMICS; TRANSCRIPTION FACTORS;

MURINAE;

EID: 84873417354     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2012.11.026     Document Type: Article

References (39)

1. Bernstein E., Duncan E.M., Masui O., Gil J., Heard E., Allis C.D. Mouse polycomb proteins bind differentially to methylated histone H3 and RNA and are enriched in facultative heterochromatin. Mol. Cell. Biol. 2006, 26:2560-2569.
2. Boulay G., Rosnoblet C., Guérardel C., Angrand P.O., Leprince D. Functional characterization of human Polycomb-like 3 isoforms identifies them as components of distinct EZH2 protein complexes. Biochem. J. 2011, 434:333-342.
3. Bracken A.P., Helin K. Polycomb group proteins: navigators of lineage pathways led astray in cancer. Nat. Rev. Cancer 2009, 9:773-784.
4. Cao R., Zhang Y. SUZ12 is required for both the histone methyltransferase activity and the silencing function of the EED-EZH2 complex. Mol. Cell 2004, 15:57-67.
5. Cao R., Wang H., He J., Erdjument-Bromage H., Tempst P., Zhang Y. Role of hPHF1 in H3K27 methylation and Hox gene silencing. Mol. Cell. Biol. 2008, 28:1862-1872.
6. Chi P., Allis C.D., Wang G.G. Covalent histone modifications-miswritten, misinterpreted and mis-erased in human cancers. Nat. Rev. Cancer 2010, 10:457-469.
7. Friberg A., Oddone A., Klymenko T., Müller J., Sattler M. Structure of an atypical Tudor domain in the Drosophila Polycomblike protein. Protein Sci. 2010, 19:1906-1916.
8. Fuchs S.M., Krajewski K., Baker R.W., Miller V.L., Strahl B.D. Influence of combinatorial histone modifications on antibody and effector protein recognition. Curr. Biol. 2011, 21:53-58.
9. Hunkapiller J., Shen Y., Diaz A., Cagney G., McCleary D., Ramalho-Santos M., Krogan N., Ren B., Song J.S., Reiter J.F. Polycomb-like 3 promotes polycomb repressive complex 2 binding to CpG islands and embryonic stem cell self-renewal. PLoS Genet. 2012, 8:e1002576.
10. Kaustov L., Ouyang H., Amaya M., Lemak A., Nady N., Duan S., Wasney G.A., Li Z., Vedadi M., Schapira M., et al. Recognition and specificity determinants of the human cbx chromodomains. J. Biol. Chem. 2011, 286:521-529.
11. Kawakami S., Mitsunaga K., Kikuti Y.Y., Ando A., Inoko H., Yamamura K., Abe K. Tctex3, related to Drosophila polycomblike, is expressed in male germ cells and mapped to the mouse t-complex. Mamm. Genome 1998, 9:874-880.
12. Klose R.J., Zhang Y. Regulation of histone methylation by demethylimination and demethylation. Nat. Rev. Mol. Cell Biol. 2007, 8:307-318.
13. Kouzarides T. Chromatin modifications and their function. Cell 2007, 128:693-705.
14. Li H., Ilin S., Wang W., Duncan E.M., Wysocka J., Allis C.D., Patel D.J. Molecular basis for site-specific read-out of histone H3K4me3 by the BPTF PHD finger of NURF. Nature 2006, 442:91-95.
15. Li G., Margueron R., Ku M., Chambon P., Bernstein B.E., Reinberg D. Jarid2 and PRC2, partners in regulating gene expression. Genes Dev. 2010, 24:368-380.
16. Margueron R., Reinberg D. The Polycomb complex PRC2 and its mark in life. Nature 2011, 469:343-349.
17. Margueron R., Justin N., Ohno K., Sharpe M.L., Son J., Drury W.J., Voigt P., Martin S.R., Taylor W.R., De Marco V., et al. Role of the polycomb protein EED in the propagation of repressive histone marks. Nature 2009, 461:762-767.
18. Micci F., Panagopoulos I., Bjerkehagen B., Heim S. Consistent rearrangement of chromosomal band 6p21 with generation of fusion genes JAZF1/PHF1 and EPC1/PHF1 in endometrial stromal sarcoma. Cancer Res. 2006, 66:107-112.
19. 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.
20. Pasini D., Cloos P.A., Walfridsson J., Olsson L., Bukowski J.P., Johansen J.V., Bak M., Tommerup N., Rappsilber J., Helin K. JARID2 regulates binding of the Polycomb repressive complex 2 to target genes in ES cells. Nature 2010, 464:306-310.
21. Peng J.C., Valouev A., Swigut T., Zhang J., Zhao Y., Sidow A., Wysocka J. Jarid2/Jumonji coordinates control of PRC2 enzymatic activity and target gene occupancy in pluripotent cells. Cell 2009, 139:1290-1302.
22. 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.
23. Rothbart S.B., Krajewski K., Strahl B.D., Fuchs S.M. Peptide microarrays to interrogate the " histone code" Methods Enzymol. 2012, 512:107-135.
24. Ruthenburg A.J., Li H., Milne T.A., Dewell S., McGinty R.K., Yuen M., Ueberheide B., Dou Y., Muir T.W., Patel D.J., Allis C.D. Recognition of a mononucleosomal histone modification pattern by BPTF via multivalent interactions. Cell 2011, 145:692-706.
25. Sarma K., Margueron R., Ivanov A., Pirrotta V., Reinberg D. Ezh2 requires PHF1 to efficiently catalyze H3 lysine 27 trimethylation in vivo. Mol. Cell. Biol. 2008, 28:2718-2731.
26. Schmitges F.W., Prusty A.B., Faty M., Stützer A., Lingaraju G.M., Aiwazian J., Sack R., Hess D., Li L., Zhou S., et al. Histone methylation by PRC2 is inhibited by active chromatin marks. Mol. Cell 2011, 42:330-341.
27. Selenko P., Sprangers R., Stier G., Bühler D., Fischer U., Sattler M. SMN tudor domain structure and its interaction with the Sm proteins. Nat. Struct. Biol. 2001, 8:27-31.
28. Shen X., Kim W., Fujiwara Y., Simon M.D., Liu Y., Mysliwiec M.R., Yuan G.C., Lee Y., Orkin S.H. Jumonji modulates polycomb activity and self-renewal versus differentiation of stem cells. Cell 2009, 139:1303-1314.
29. Sun B., Hong J., Zhang P., Dong X., Shen X., Lin D., Ding J. Molecular basis of the interaction of Saccharomyces cerevisiae Eaf3 chromo domain with methylated H3K36. J. Biol. Chem. 2008, 283:36504-36512.
30. Vermeulen M., Eberl H.C., Matarese F., Marks H., Denissov S., Butter F., Lee K.K., Olsen J.V., Hyman A.A., Stunnenberg H.G., Mann M. Quantitative interaction proteomics and genome-wide profiling of epigenetic histone marks and their readers. Cell 2010, 142:967-980.
31. Vezzoli A., Bonadies N., Allen M.D., Freund S.M., Santiveri C.M., Kvinlaug B.T., Huntly B.J., Göttgens B., Bycroft M. Molecular basis of histone H3K36me3 recognition by the PWWP domain of Brpf1. Nat. Struct. Mol. Biol. 2010, 17:617-619.
32. Voigt P., LeRoy G., Drury W.J., Zee B.M., Son J., Beck D.B., Young N.L., Garcia B.A., Reinberg D. Asymmetrically modified nucleosomes. Cell 2012, 151:181-193.
33. Walker E., Chang W.Y., Hunkapiller J., Cagney G., Garcha K., Torchia J., Krogan N.J., Reiter J.F., Stanford W.L. Polycomb-like 2 associates with PRC2 and regulates transcriptional networks during mouse embryonic stem cell self-renewal and differentiation. Cell Stem Cell 2010, 6:153-166.
34. Wang S., Robertson G.P., Zhu J. A novel human homologue of Drosophila polycomblike gene is up-regulated in multiple cancers. Gene 2004, 343:69-78.
35. Wang G.G., Song J., Wang Z., Dormann H.L., Casadio F., Li H., Luo J.L., Patel D.J., Allis C.D. Haematopoietic malignancies caused by dysregulation of a chromatin-binding PHD finger. Nature 2009, 459:847-851.
36. Wu S.F., Zhang H., Cairns B.R. Genes for embryo development are packaged in blocks of multivalent chromatin in zebrafish sperm. Genome Res. 2011, 21:578-589.
37. Xiao S., Xie D., Cao X., Yu P., Xing X., Chen C.C., Musselman M., Xie M., West F.D., Lewin H.A., et al. Comparative epigenomic annotation of regulatory DNA. Cell 2012, 149:1381-1392.
38. Xu C., Cui G., Botuyan M.V., Mer G. Structural basis for the recognition of methylated histone H3K36 by the Eaf3 subunit of histone deacetylase complex Rpd3S. Structure 2008, 16:1740-1750.
39. Yuan W., Xu M., Huang C., Liu N., Chen S., Zhu B. H3K36 methylation antagonizes PRC2-mediated H3K27 methylation. J. Biol. Chem. 2011, 286:7983-7989.