SETDB1 modulates PRC2 activity at developmental genes independently of H3K9 trimethylation in mouse ES cells

Genome Research

Volumn 25, Issue 9, 2015, Pages 1325-1335

  Fei, Qi ^a   Yang, Xiaoqin ^b   Jiang, Hua ^a   Wang, Qian ^b   Yu, Yanyan ^a   Yu, Yiling ^a   Yi, Wei ^a   Zhou, Shaolian ^a   Chen, Taiping ^d   Lu, Chris ^a   Atadja, Peter ^a   Liu, Xiaole Shirley ^c   Li, En ^a   Zhang, Yong ^b   Shou, Jianyong ^e  

^a Novartis Institutes for Biomedical Research   (China)

^b TONGJI UNIVERSITY   (China)

^c HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^d UNIVERSITY OF TEXAS   (United States)

^e Lilly China Research and Development Center   (China)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE H3; METHYLTRANSFERASE; OCTAMER TRANSCRIPTION FACTOR 4; POLYCOMB REPRESSIVE COMPLEX 2; PROTEIN; S ADENOSYLMETHIONINE; SETDB1 PROTEIN; SUZ12 PROTEIN; TET1 PROTEIN; TRANSCRIPTION FACTOR EZH2; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SOX2; UNCLASSIFIED DRUG; HISTONE; HISTONE LYSINE METHYLTRANSFERASE; PROTEIN BINDING; SETDB1 PROTEIN, MOUSE;

ANIMAL CELL; ARTICLE; BINDING SITE; CELL DIFFERENTIATION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DEVELOPMENTAL GENE; DNA METHYLATION; EMBRYO; EMBRYONIC STEM CELL; ENZYME ACTIVITY; GENE DELETION; GENE EXPRESSION; IN VITRO STUDY; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; MOUSE; NERVE CELL DIFFERENTIATION; NONHUMAN; NUCLEOSOME; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN DEPLETION; SUSPENSION CELL CULTURE; WESTERN BLOTTING; ANIMAL; GENE EXPRESSION REGULATION; METABOLISM; METHYLATION; REGULATORY SEQUENCE;

ANIMALS; BINDING SITES; EMBRYONIC STEM CELLS; GENE EXPRESSION REGULATION; HISTONE-LYSINE N-METHYLTRANSFERASE; HISTONES; METHYLATION; MICE; POLYCOMB REPRESSIVE COMPLEX 2; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; REGULATORY SEQUENCES, NUCLEIC ACID;

EID: 84940988212     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.177576.114     Document Type: Article

References (44)

1. Bilodeau S, Kagey MH, Frampton GM, Rahl PB, Young RA. 2009. SetDB1 contributes to repression of genes encoding developmental regulators and maintenance of ES cell state. Genes Dev 23: 2484-2489.
2. Binda O, LeRoy G, Bua DJ, Garcia BA, Gozani O, Richard S. 2010. Trimethylation of histone H3 lysine 4 impairs methylation of histone H3 lysine 9: Regulation of lysine methyltransferases by physical interaction with their substrates. Epigenetics 5: 767-775.
3. Boyer LA, Lee TI, Cole MF, Johnstone SE, Levine SS, Zucker JP, Guenther MG, Kumar RM, Murray HL, Jenner RG, et al. 2005. Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 122: 947-956.
4. Boyer LA, Plath K, Zeitlinger J, Brambrink T, Medeiros LA, Lee TI, Levine SS, Wernig M, Tajonar A, Ray MK, et al. 2006. Polycomb complexes repress developmental regulators in murine embryonic stem cells. Nature 441: 349-353.
5. Chamberlain SJ, Yee D, Magnuson T. 2008. Polycomb repressive complex 2 is dispensable for maintenance of embryonic stem cell pluripotency. Stem Cells 26: 1496-1505.
6. Chen L, Daley GQ. 2008. Molecular basis of pluripotency. Hum Mol Genet 17: R23-R27.
7. Chen X, Xu H, Yuan P, Fang F, Huss M, Vega VB, Wong E, Orlov YL, Zhang W, Jiang J, et al. 2008. Integration of external signaling pathways with the core transcriptional network in embryonic stem cells. Cell 133: 1106-1117.
8. Dodge JE, Kang YK, Beppu H, Lei H, Li E. 2004. Histone H3-K9 methyltransferase ESET is essential for early development. Mol Cell Biol 24: 2478-2486.
9. Herz HM, Shilatifard A. 2010. The JARID2-PRC2 duality. Genes Dev 24: 857-861.
10. Hong SH, Rampalli S, Lee JB, McNicol J, Collins T, Draper JS, Bhatia M. 2011. Cell fate potential of human pluripotent stem cells is encoded by histone modifications. Cell Stem Cell 9: 24-36.
11. Karimi MM, Goyal P, Maksakova IA, Bilenky M, Leung D, Tang JX, Shinkai Y, Mager DL, Jones S, Hirst M, et al. 2011. DNA methylation and SETDB1/H3K9me3 regulate predominantly distinct sets of genes, retroelements, and chimeric transcripts in mESCs. Cell Stem Cell 8: 676-687.
12. Kim J, Chu J, Shen X, Wang J, Orkin SH. 2008. An extended transcriptional network for pluripotency of embryonic stem cells. Cell 132: 1049-1061.
13. Landt SG, Marinov GK, Kundaje A, Kheradpour P, Pauli F, Batzoglou S, Bernstein BE, Bickel P, Brown JB, Cayting P, et al. 2012. ChIP-seq guidelines and practices of the ENCODE and modENCODE consortia. Genome Res 22: 1813-1831.
14. Langmead B, Trapnell C, Pop M, Salzberg S. 2009. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10: R25.
15. Lee TI, Jenner RG, Boyer LA, Guenther MG, Levine SS, Kumar RM, Chevalier B, Johnstone SE, ColeMF, Isono K, et al. 2006. Control of developmental regulators by Polycomb in human embryonic stem cells. Cell 125: 301-313.
16. Lee JS, Smith E, Shilatifard A. 2010. The language of histone crosstalk. Cell 142: 682-685.
17. Liu S, Brind'Amour J, Karimi MM, Shirane K, Bogutz A, Lefebvre L, Sasaki H, Shinkai Y, Lorincz MC. 2014. Setdb1 is required for germline development and silencing of H3K9me3-marked endogenous retroviruses in primordial germ cells. Genes Dev 28: 2041-2055.
18. Lohmann F, Loureiro J, Su H, Fang Q, Lei H, Lewis T, Yang Y, Labow M, Li E, Chen T, et al. 2010. KMT1E mediated H3K9 methylation is required for the maintenance of embryonic stem cells by repressing trophectoderm differentiation. Stem Cells 28: 201-212.
19. Lohse B, Helgstrand C, Kristensen JBL, Leurs U, Cloos PAC, Kristensen JL, Clausen RP. 2013. Posttranslational modifications of the histone 3 tail and their impact on the activity of histone lysine demethylases in vitro. PLoS One 8: E67653.
20. Luger K, Rechsteiner TJ, Richmond TJ. 1999. Expression and purification of recombinant histones and nucleosome reconstitution. Methods Mol Biol 119: 1-16.
21. Margueron R, Reinberg D. 2011. The Polycomb complex PRC2 and its mark in life. Nature 469: 343-349.
22. Matsui T, Leung D, Miyashita H, Maksakova IA, Miyachi H, Kimura H, Tachibana M, Lorincz MC, Shinkai Y. 2010. Proviral silencing in embryonic stem cells requires the histone methyltransferase ESET. Nature 464: 927-931.
23. Mendenhall EM, 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.
24. Mysliwiec MR, Carlson CD, Tietjen J, Hung H, Ansari AZ, Lee Y. 2012. Jarid2 (Jumonji, AT rich interactive domain 2) regulates NOTCH1 expression via histone modification in the developing heart. J Biol Chem 287: 1235-1241.
25. Nishiyama A, Xin L, Sharov AA, Thomas M, Mowrer G, Meyers E, Piao Y, Mehta S, Yee S, Nakatake Y, et al. 2009. Uncovering early response of gene regulatory networks in ESCs by systematic induction of transcription factors. Cell Stem Cell 5: 420-433.
26. 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.
27. Peng JC, 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.
28. Peters AH, Kubicek S, Mechtler K, O'Sullivan RJ, Derijck AA, Perez-Burgos L, Kohlmaier A, Opravil S, Tachibana M, Shinkai Y, et al. 2003. Partitioning and plasticity of repressive histone methylation states in mammalian chromatin. Mol Cell 12: 1577-1589.
29. Plath K, Fang J, Mlynarczyk-Evans SK, Cao R, Worringer KA, Wang H, de la Cruz CC, Otte AP, Panning B, Zhang Y. 2003. Role of histone H3 lysine 27 methylation in X inactivation. Science 300: 131-135.
30. Quinlan AR, Hall IM. 2010. BEDTools: A flexible suite of utilities for comparing genomic features. Bioinformatics 26: 841-842.
31. Rapicavoli NA, Poth EM, Zhu H, Blackshaw S. 2011. The long noncoding RNA Six3OS acts in trans to regulate retinal development by modulating Six3 activity. Neural Dev 6: 32.
32. Rinn JL, Kertesz M, Wang JK, Squazzo SL, Xu X, Brugmann SA, Goodnough LH, 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.
33. Schmitges FW, 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.
34. Schultz DC, Ayyanathan K, Negorev D, Maul GG, Rauscher FJ III. 2002. SETDB1: A novel KAP-1-associated histone H3, lysine 9-specific methyltransferase that contributes to HP1-mediated silencing of euchromatic genes by KRAB zinc-finger proteins. Genes Dev 16: 919-932.
35. Simon MD, 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.
36. Surani MA, Hayashi K, Hajkova P. 2007. Genetic and epigenetic regulators of pluripotency. Cell 128: 747-762.
37. Tan SL, Nishi M, Ohtsuka T, Matsui T, Takemoto K, Kamio-Miura A, Aburatani H, Shinkai Y, Kageyama R. 2012. Essential roles of the histonemethyltransferase ESET in the epigenetic control of neural progenitor cells during development. Development 139: 3806-3816.
38. Wang H, Cao R, Xia L, Erdjument-Bromage H, Borchers C, Tempst P, Zhang Y. 2001. Purification and functional characterization of a histone H3-lysine 4-specific methyltransferase. Mol Cell 8: 1207-1217.
39. Wang X, Pan L, Wang S, Zhou J, McDowell W, Park J, Haug J, Staehling K, Tang H, Xie T. 2011. Histone H3K9 trimethylase Eggless controls germline stem cell maintenance and differentiation. PLoS Genet 7: E1002426.
40. Xu K, Wu ZJ, Groner AC, He HH, Cai C, Lis RT, Wu X, Stack EC, Loda M, Liu T, et al. 2012. EZH2 oncogenic activity in castration-resistant prostate cancer cells is Polycomb-independent. Science 338: 1465-1469.
41. Yap DB, Chu J, Berg T, Schapira M, Cheng SW, Moradian A, Morin RD, Mungall AJ, Meissner B, Boyle M, et al. 2011. Somatic mutations at EZH2 Y641 act dominantly through a mechanism of selectively altered PRC2 catalytic activity, to increase H3K27 trimethylation. Blood 117: 2451-2459.
42. Yuan P, Han J, Guo G, Orlov YL, Huss M, Loh YH, Yaw LP, Robson P, Lim B, Ng HH. 2009. Eset partners with Oct4 to restrict extraembryonic trophoblast lineage potential in embryonic stem cells. Genes Dev 23: 2507-2520.
43. Yuan W, Xu M, Huang C, Liu N, Chen S, Zhu B. 2011. H3K36 methylation antagonizes PRC2-mediated H3K27 methylation. J Biol Chem 286: 7983-7989.
44. Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, Bernstein BE, Nusbaum C, Myers RM, Brown M, Li W, et al. 2008. Model-based analysis of ChIPSeq (MACS). Genome Biol 9: R137.