EPOP Interacts with Elongin BC and USP7 to Modulate the Chromatin Landscape

Molecular Cell

Volumn 64, Issue 4, 2016, Pages 659-672

  Liefke, Robert ^a,b   Karwacki Neisius, Violetta ^a,b   Shi, Yang ^a,b  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

cancer; chromatin; Elongin BC; H2Bub; MYC; pluripotency; Polycomb; stem cells; transcription; USP7

Indexed keywords

DEUBIQUITINASE; ELONGIN B; ELONGIN BC; ELONGIN BC AND POLYCOMB REPRESSIVE COMPLEX 2 ASSOCIATED PROTEIN; ELONGIN C; GLUTAMATE DECARBOXYLASE 65; HISTONE H2B; MITOGEN ACTIVATED PROTEIN KINASE 1; MYC PROTEIN; OCTAMER TRANSCRIPTION FACTOR 4; PCG PROTEIN; POLYCOMB REPRESSIVE COMPLEX 2; PROTEIN; RNA POLYMERASE II; SHORT HAIRPIN RNA; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SOX2; UNCLASSIFIED DRUG; USP7 PROTEIN; VESICULAR GLUTAMATE TRANSPORTER 2; CHROMATIN; DNA DIRECTED DNA POLYMERASE ALPHA; E13 PROTEIN, MOUSE; ELONGIN; HISTONE; NERVE PROTEIN; PROTEIN BINDING; TRANSCRIPTION FACTOR; USP7 PROTEIN, MOUSE;

ANIMAL CELL; ARTICLE; CANCER CELL LINE; CELL PROLIFERATION; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; ENHANCER REGION; GENE INACTIVATION; GENE OVEREXPRESSION; HISTONE MODIFICATION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; MASS SPECTROMETRY; MOUSE; NERVE CELL DIFFERENTIATION; NONHUMAN; POLYMERASE CHAIN REACTION; PROMOTER REGION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; QUANTITATIVE ANALYSIS; RNA SEQUENCE; UPREGULATION; WESTERN BLOTTING; WILD TYPE; ANIMAL; CELL DIFFERENTIATION; CHEMISTRY; CYTOLOGY; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENETIC TRANSCRIPTION; GENETICS; MAMMALIAN EMBRYO; METABOLISM; MOUSE EMBRYONIC STEM CELL; PLURIPOTENT STEM CELL; TUMOR CELL LINE;

ANIMALS; CELL DIFFERENTIATION; CELL LINE, TUMOR; CHROMATIN; DNA POLYMERASE II; EMBRYO, MAMMALIAN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE REGULATORY NETWORKS; HISTONES; HUMANS; MICE; MOUSE EMBRYONIC STEM CELLS; NERVE TISSUE PROTEINS; PLURIPOTENT STEM CELLS; POLYCOMB REPRESSIVE COMPLEX 2; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; UBIQUITIN-SPECIFIC PROTEASES;

EID: 84995609052     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2016.10.019     Document Type: Article

References (45)

1. Alekseyenko, A.A., Gorchakov, A.A., Kharchenko, P.V., Kuroda, M.I., Reciprocal interactions of human C10orf12 and C17orf96 with PRC2 revealed by BioTAP-XL cross-linking and affinity purification. Proc. Natl. Acad. Sci. USA 111 (2014), 2488–2493.
2. Aso, T., Lane, W.S., Conaway, J.W., Conaway, R.C., Elongin (SIII): a multisubunit regulator of elongation by RNA polymerase II. Science 269 (1995), 1439–1443.
3. Aso, T., Haque, D., Barstead, R.J., Conaway, R.C., Conaway, J.W., The inducible elongin A elongation activation domain: structure, function and interaction with the elongin BC complex. EMBO J. 15 (1996), 5557–5566.
4. Batta, K., Zhang, Z., Yen, K., Goffman, D.B., Pugh, B.F., Genome-wide function of H2B ubiquitylation in promoter and genic regions. Genes Dev. 25 (2011), 2254–2265.
5. Ben-Porath, I., Thomson, M.W., Carey, V.J., Ge, R., Bell, G.W., Regev, A., Weinberg, R.A., An embryonic stem cell-like gene expression signature in poorly differentiated aggressive human tumors. Nat. Genet. 40 (2008), 499–507.
6. Benayoun, B.A., Pollina, E.A., Ucar, D., Mahmoudi, S., Karra, K., Wong, E.D., Devarajan, K., Daugherty, A.C., Kundaje, A.B., Mancini, E., et al. H3K4me3 breadth is linked to cell identity and transcriptional consistency. Cell 158 (2014), 673–688.
7. Brower, C.S., Sato, S., Tomomori-Sato, C., Kamura, T., Pause, A., Stearman, R., Klausner, R.D., Malik, S., Lane, W.S., Sorokina, I., et al. Mammalian mediator subunit mMED8 is an Elongin BC-interacting protein that can assemble with Cul2 and Rbx1 to reconstitute a ubiquitin ligase. Proc. Natl. Acad. Sci. USA 99 (2002), 10353–10358.
8. Chen, K., Chen, Z., Wu, D., Zhang, L., Lin, X., Su, J., Rodriguez, B., Xi, Y., Xia, Z., Chen, X., et al. Broad H3K4me3 is associated with increased transcription elongation and enhancer activity at tumor-suppressor genes. Nat. Genet. 47 (2015), 1149–1157.
9. Clouaire, T., Webb, S., Skene, P., Illingworth, R., Kerr, A., Andrews, R., Lee, J.H., Skalnik, D., Bird, A., Cfp1 integrates both CpG content and gene activity for accurate H3K4me3 deposition in embryonic stem cells. Genes Dev. 26 (2012), 1714–1728.
10. De Cegli, R., Iacobacci, S., Flore, G., Gambardella, G., Mao, L., Cutillo, L., Lauria, M., Klose, J., Illingworth, E., Banfi, S., di Bernardo, D., Reverse engineering a mouse embryonic stem cell-specific transcriptional network reveals a new modulator of neuronal differentiation. Nucleic Acids Res. 41 (2013), 711–726.
11. Eilers, M., Eisenman, R.N., Myc's broad reach. Genes Dev. 22 (2008), 2755–2766.
12. Fuchs, G., Shema, E., Vesterman, R., Kotler, E., Wolchinsky, Z., Wilder, S., Golomb, L., Pribluda, A., Zhang, F., Haj-Yahya, M., et al. RNF20 and USP44 regulate stem cell differentiation by modulating H2B monoubiquitylation. Mol. Cell 46 (2012), 662–673.
13. Györffy, B., Lanczky, A., Eklund, A.C., Denkert, C., Budczies, J., Li, Q., Szallasi, Z., An online survival analysis tool to rapidly assess the effect of 22,277 genes on breast cancer prognosis using microarray data of 1,809 patients. Breast Cancer Res. Treat. 123 (2010), 725–731.
14. Hanahan, D., Weinberg, R.A., Hallmarks of cancer: the next generation. Cell 144 (2011), 646–674.
15. Henry, K.W., Wyce, A., Lo, W.S., Duggan, L.J., Emre, N.C., Kao, C.F., Pillus, L., Shilatifard, A., Osley, M.A., Berger, S.L., Transcriptional activation via sequential histone H2B ubiquitylation and deubiquitylation, mediated by SAGA-associated Ubp8. Genes Dev. 17 (2003), 2648–2663.
16. Hwang, J., Saffert, R.T., Kalejta, R.F., Elongin B-mediated epigenetic alteration of viral chromatin correlates with efficient human cytomegalovirus gene expression and replication. MBio, 2, 2011 e00023–e11.
17. Jiang, H., Shukla, A., Wang, X., Chen, W.Y., Bernstein, B.E., Roeder, R.G., Role for Dpy-30 in ES cell-fate specification by regulation of H3K4 methylation within bivalent domains. Cell 144 (2011), 513–525.
18. Kareta, M.S., Gorges, L.L., Hafeez, S., Benayoun, B.A., Marro, S., Zmoos, A.F., Cecchini, M.J., Spacek, D., Batista, L.F., O'Brien, M., et al. Inhibition of pluripotency networks by the Rb tumor suppressor restricts reprogramming and tumorigenesis. Cell Stem Cell 16 (2015), 39–50.
19. Karlebach, G., Shamir, R., Modelling and analysis of gene regulatory networks. Nat. Rev. Mol. Cell Biol. 9 (2008), 770–780.
20. Kim, J., Woo, A.J., Chu, J., Snow, J.W., Fujiwara, Y., Kim, C.G., Cantor, A.B., Orkin, S.H., A Myc network accounts for similarities between embryonic stem and cancer cell transcription programs. Cell 143 (2010), 313–324.
21. Kim, J., Kim, J.A., McGinty, R.K., Nguyen, U.T., Muir, T.W., Allis, C.D., Roeder, R.G., The n-SET domain of Set1 regulates H2B ubiquitylation-dependent H3K4 methylation. Mol. Cell 49 (2013), 1121–1133.
22. Klein, A.M., Mazutis, L., Akartuna, I., Tallapragada, N., Veres, A., Li, V., Peshkin, L., Weitz, D.A., Kirschner, M.W., Droplet barcoding for single-cell transcriptomics applied to embryonic stem cells. Cell 161 (2015), 1187–1201.
23. Li, X.S., Trojer, P., Matsumura, T., Treisman, J.E., Tanese, N., Mammalian SWI/SNF—a subunit BAF250/ARID1 is an E3 ubiquitin ligase that targets histone H2B. Mol. Cell. Biol. 30 (2010), 1673–1688.
24. Liefke, R., Borggrefe, T., Probing the epigenetic status at Notch target genes. Methods Mol. Biol. 1187 (2014), 255–276.
25. Liefke, R., Shi, Y., The PRC2-associated factor C17orf96 is a novel CpG island regulator in mouse ES cells. Cell Discov., 1, 2015, 15008.
26. Lin, C., Garrett, A.S., De Kumar, B., Smith, E.R., Gogol, M., Seidel, C., Krumlauf, R., Shilatifard, A., Dynamic transcriptional events in embryonic stem cells mediated by the super elongation complex (SEC). Genes Dev. 25 (2011), 1486–1498.
27. Lin, C.Y., Lovén, J., Rahl, P.B., Paranal, R.M., Burge, C.B., Bradner, J.E., Lee, T.I., Young, R.A., Transcriptional amplification in tumor cells with elevated c-Myc. Cell 151 (2012), 56–67.
28. Lowell, S., Benchoua, A., Heavey, B., Smith, A.G., Notch promotes neural lineage entry by pluripotent embryonic stem cells. PLoS Biol., 4, 2006, e121.
29. Maertens, G.N., El Messaoudi-Aubert, S., Elderkin, S., Hiom, K., Peters, G., Ubiquitin-specific proteases 7 and 11 modulate Polycomb regulation of the INK4a tumour suppressor. EMBO J. 29 (2010), 2553–2565.
30. Mahrour, N., Redwine, W.B., Florens, L., Swanson, S.K., Martin-Brown, S., Bradford, W.D., Staehling-Hampton, K., Washburn, M.P., Conaway, R.C., Conaway, J.W., Characterization of Cullin-box sequences that direct recruitment of Cul2-Rbx1 and Cul5-Rbx2 modules to Elongin BC-based ubiquitin ligases. J. Biol. Chem. 283 (2008), 8005–8013.
31. Ng, H.H., Surani, M.A., The transcriptional and signalling networks of pluripotency. Nat. Cell Biol. 13 (2011), 490–496.
32. Nie, Z., Hu, G., Wei, G., Cui, K., Yamane, A., Resch, W., Wang, R., Green, D.R., Tessarollo, L., Casellas, R., et al. c-Myc is a universal amplifier of expressed genes in lymphocytes and embryonic stem cells. Cell 151 (2012), 68–79.
33. Nishiyama, A., Sharov, A.A., Piao, Y., Amano, M., Amano, T., Hoang, H.G., Binder, B.Y., Tapnio, R., Bassey, U., Malinou, J.N., et al. Systematic repression of transcription factors reveals limited patterns of gene expression changes in ES cells. Sci. Rep., 3, 2013, 1390.
34. Pavri, R., Zhu, B., Li, G., Trojer, P., Mandal, S., Shilatifard, A., Reinberg, D., Histone H2B monoubiquitination functions cooperatively with FACT to regulate elongation by RNA polymerase II. Cell 125 (2006), 703–717.
35. Rahl, P.B., Lin, C.Y., Seila, A.C., Flynn, R.A., McCuine, S., Burge, C.B., Sharp, P.A., Young, R.A., c-Myc regulates transcriptional pause release. Cell 141 (2010), 432–445.
36. Sabò, A., Kress, T.R., Pelizzola, M., de Pretis, S., Gorski, M.M., Tesi, A., Morelli, M.J., Bora, P., Doni, M., Verrecchia, A., et al. Selective transcriptional regulation by Myc in cellular growth control and lymphomagenesis. Nature 511 (2014), 488–492.
37. Sarkari, F., Sanchez-Alcaraz, T., Wang, S., Holowaty, M.N., Sheng, Y., Frappier, L., EBNA1-mediated recruitment of a histone H2B deubiquitylating complex to the Epstein-Barr virus latent origin of DNA replication. PLoS Pathog., 5, 2009, e1000624.
38. Smits, A.H., Jansen, P.W., Poser, I., Hyman, A.A., Vermeulen, M., Stoichiometry of chromatin-associated protein complexes revealed by label-free quantitative mass spectrometry-based proteomics. Nucleic Acids Res., 41, 2013, e28.
39. Torres-Padilla, M.E., Chambers, I., Transcription factor heterogeneity in pluripotent stem cells: a stochastic advantage. Development 141 (2014), 2173–2181.
40. van der Knaap, J.A., Kumar, B.R., Moshkin, Y.M., Langenberg, K., Krijgsveld, J., Heck, A.J., Karch, F., Verrijzer, C.P., GMP synthetase stimulates histone H2B deubiquitylation by the epigenetic silencer USP7. Mol. Cell 17 (2005), 695–707.
41. Voigt, P., Tee, W.W., Reinberg, D., A double take on bivalent promoters. Genes Dev. 27 (2013), 1318–1338.
42. Weake, V.M., Workman, J.L., Histone ubiquitination: triggering gene activity. Mol. Cell 29 (2008), 653–663.
43. Whyte, W.A., Orlando, D.A., Hnisz, D., Abraham, B.J., Lin, C.Y., Kagey, M.H., Rahl, P.B., Lee, T.I., Young, R.A., Master transcription factors and mediator establish super-enhancers at key cell identity genes. Cell 153 (2013), 307–319.
44. Wu, L., Lee, S.Y., Zhou, B., Nguyen, U.T., Muir, T.W., Tan, S., Dou, Y., ASH2L regulates ubiquitylation signaling to MLL: trans-regulation of H3 K4 methylation in higher eukaryotes. Mol. Cell 49 (2013), 1108–1120.
45. Zhang, Z., Jones, A., Sun, C.W., Li, C., Chang, C.W., Joo, H.Y., Dai, Q., Mysliwiec, M.R., Wu, L.C., Guo, Y., et al. PRC2 complexes with JARID2, MTF2, and esPRC2p48 in ES cells to modulate ES cell pluripotency and somatic cell reprogramming. Stem Cells 29 (2011), 229–240.