TRIM28 regulates RNA polymerase II promoter-proximal pausing and pause release

Nature Structural and Molecular Biology

Volumn 21, Issue 10, 2014, Pages 876-883

  Bunch, Heeyoun ^a   Zheng, Xiaofeng ^b   Burkholder, Adam ^b   Dillon, Simon T ^a   Motola, Shmulik ^c   Birrane, Gabriel ^a   Ebmeier, Christopher C ^d   Levine, Stuart ^c   Fargo, David ^b   Hu, Guang ^b   Taatjes, Dylan J ^d   Calderwood, Stuart K ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^c MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^d UNIVERSITY OF COLORADO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HEAT SHOCK TRANSCRIPTION FACTOR 1; PROTEIN; RNA POLYMERASE II; TRIPARTITE MOTIF CONTAINING 28; UNCLASSIFIED DRUG; ATM PROTEIN; ATM PROTEIN, HUMAN; DNA BINDING PROTEIN; DNA DEPENDENT PROTEIN KINASE; HEAT SHOCK PROTEIN 70; HEAT SHOCK TRANSCRIPTION FACTOR; HSPA1B PROTEIN, HUMAN; REPRESSOR PROTEIN; TRANSCRIPTION FACTOR; TRIM28 PROTEIN, HUMAN;

ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; GENE CONTROL; GENE EXPRESSION; GENE IDENTIFICATION; GENE SEQUENCE; GENE SILENCING; GENETIC ASSOCIATION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER PROXIMAL PAUSING; PROMOTER REGION; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; RNA TRANSCRIPTION; TRANSCRIPTION ELONGATION; TRANSCRIPTION INITIATION; WILD TYPE; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; GENETIC TRANSCRIPTION; GENETICS; HEK293 CELL LINE; HELA CELL LINE; METABOLISM; PHOSPHORYLATION; TUMOR CELL LINE;

MAMMALIA;

ATAXIA TELANGIECTASIA MUTATED PROTEINS; CELL LINE, TUMOR; DNA-ACTIVATED PROTEIN KINASE; DNA-BINDING PROTEINS; HEK293 CELLS; HELA CELLS; HSP70 HEAT-SHOCK PROTEINS; HUMANS; PHOSPHORYLATION; PROMOTER REGIONS, GENETIC; REPRESSOR PROTEINS; RNA POLYMERASE II; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 84922281026     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.2878     Document Type: Article

References (39)

1. Rahl, P.B. et al. c-Myc regulates transcriptional pause release. Cell 141, 432-445 (2010).
2. Rasmussen, E.B., Lis, J.T In vivo transcriptional pausing and cap formation on three Drosophila heat shock genes. Proc. Natl. Acad. Sci. USA 90, 7923-7927 (1993).
3. Nechaev, S. et al. Global analysis of short RNAs reveals widespread promoter-proximal stalling and arrest of Pol II in Drosophila. Science 327, 335-338 (2010).
4. Muse, G.W. et al. RNA polymerase is poised for activation across the genome. Nat. Genet. 39, 1507-1511 (2007).
5. Core, L.J., Waterfall, J.J., Lis, J.T. Nascent RNA sequencing reveals widespread pausing and divergent initiation at human promoters. Science 322, 1845-1848 (2008).
6. Zeitlinger, J. et al. Whole-genome ChIP-chip analysis of Dorsal, Twist, and Snail suggests integration of diverse patterning processes in the Drosophila embryo. Genes Dev. 21, 385-390 (2007).
7. Seila, A.C. et al. Divergent transcription from active promoters. Science 322, 1849-1851 (2008).
8. Adelman, K., Lis, J.T. Promoter-proximal pausing of RNA polymerase II: emerging roles in metazoans. Nat. Rev. Genet. 13, 720-731 (2012).
9. Gaertner, B. et al. Poised RNA polymerase II changes over developmental time and prepares genes for future expression. Cell Reports 2, 1670-1683 (2012).
10. Wu, C.H. et al. NELF and DSIF cause promoter proximal pausing on the hsp70 promoter in Drosophila. Genes Dev. 17, 1402-1414 (2003).
11. Peterlin, B.M., Price, D.H. Controlling the elongation phase of transcription with P-TEFb. Mol. Cell 23, 297-305 (2006).
12. Gilchrist, D.A. et al. NELF-mediated stalling of Pol II can enhance gene expression by blocking promoter-proximal nucleosome assembly. Genes Dev. 22, 1921-1933 (2008).
13. Rabindran, S.K., Giorgi, G., Clos, J., Wu, C. Molecular cloning and expression of a human heat shock factor, HSF1. Proc. Natl. Acad. Sci. USA 88, 6906-6910 (1991).
14. Sun, J., Li, R. Human negative elongation factor activates transcription and regulates alternative transcription initiation. J. Biol. Chem. 285, 6443-6452 (2010).
15. Cheng, B. et al. Functional association of Gdown1 with RNA polymerase II poised on human genes. Mol. Cell 45, 38-50 (2012).
16. Byun, J.S. et al. ELL facilitates RNA polymerase II pause site entry and release. Nat. Commun. 3, 633 (2012).
17. Ulrich, H. DNA and RNA aptamers as modulators of protein function. Med. Chem. 1, 199-208 (2005).
18. Hendrix, D.A., Hong, J.W., Zeitlinger, J., Rokhsar, D.S., Levine, M.S. Promoter elements associated with RNA Pol II stalling in the Drosophila embryo. Proc. Natl. Acad. Sci. USA 105, 7762-7767 (2008).
19. Lee, C. et al. NELF and GAGA factor are linked to promoter-proximal pausing at many genes in Drosophila. Mol. Cell. Biol. 28, 3290-3300 (2008).
20. Iyengar, S., Ivanov, A.V., Jin, V.X., Rauscher, F.J. III, Farnham, P.J. Functional analysis of KAP1 genomic recruitment. Mol. Cell. Biol. 31, 1833-1847 (2011).
21. Chen, L. et al. Tripartite motif containing 28 (Trim28) can regulate cell proliferation by bridging HDAC1/E2F interactions. J. Biol. Chem. 287, 40106-40118 (2012).
22. Messerschmidt, D.M. et al. Trim28 is required for epigenetic stability during mouse oocyte to embryo transition. Science 335, 1499-1502 (2012).
23. Hu, G. et al. A genome-wide RNAi screen identifies a new transcriptional module required for self-renewal. Genes Dev. 23, 837-848 (2009).
24. Chikuma, S., Suita, N., Okazaki, I.M., Shibayama, S., Honjo, T. TRIM28 prevents autoinflammatory T cell development in vivo. Nat. Immunol. 13, 596-603 (2012).
25. Vassylyev, D.G. et al. Structural basis for substrate loading in bacterial RNA polymerase. Nature 448, 163-168 (2007).
26. Kininis, M., Isaacs, G.D., Core, L.J., Hah, N., Kraus, W.L. Postrecruitment regulation of RNA polymerase II directs rapid signaling responses at the promoters of estrogen target genes. Mol. Cell. Biol. 29, 1123-1133 (2009).
27. Zobeck, K.L., Buckley, M.S., Zipfel, W.R., Lis, J.T. Recruitment timing and dynamics of transcription factors at the Hsp70 loci in living cells. Mol. Cell 40, 965-975 (2010).
28. Gilchrist, D.A. et al. Regulating the regulators: the pervasive effects of Pol II pausing on stimulus-responsive gene networks. Genes Dev. 26, 933-944 (2012).
29. Makalowski, W., Boguski, M.S. Evolutionary parameters of the transcribed mammalian genome: an analysis of 2, 820 orthologous rodent and human sequences. Proc. Natl. Acad. Sci. USA 95, 9407-9412 (1998).
30. Ziv, Y. et al. Chromatin relaxation in response to DNA double-strand breaks is modulated by a novel ATM-and KAP-1 dependent pathway. Nat. Cell Biol. 8, 870-876 (2006).
31. White, D. et al. The ATM substrate KAP1 controls DNA repair in heterochromatin: regulation by HP1 proteins and serine 473/824 phosphorylation. Mol. Cancer Res. 10, 401-414 (2012).
32. Lee, D.H. et al. Phosphoproteomic analysis reveals that PP4 dephosphorylates KAP-1 impacting the DNA damage response. EMBO J. 31, 2403-2415 (2012).
33. Li, X. et al. Role for KAP1 serine 824 phosphorylation and sumoylation/desumoylation switch in regulating KAP1-mediated transcriptional repression. J. Biol. Chem. 282, 36177-36189 (2007).
34. Chen, B.P. et al. Ataxia telangiectasia mutated (ATM) is essential for DNA-PKcs phosphorylations at the Thr-2609 cluster upon DNA double strand break. J. Biol. Chem. 282, 6582-6587 (2007).
35. Yoon, Y.J. et al. KRIBB11 inhibits HSP70 synthesis through inhibition of heat shock factor 1 function by impairing the recruitment of positive transcription elongation factor b to the hsp70 promoter. J. Biol. Chem. 286, 1737-1747 (2011).
36. Wolf, D., Goff, S.P. TRIM28 mediates primer binding site-targeted silencing of murine leukemia virus in embryonic cells. Cell 131, 46-57 (2007).
37. Ivanov, A.V. et al. PHD domain-mediated E3 ligase activity directs intramolecular sumoylation of an adjacent bromodomain required for gene silencing. Mol. Cell 28, 823-837 (2007).
38. Lee, W. et al. A high-resolution atlas of nucleosome occupancy in yeast. Nat. Genet. 39, 1235-1244 (2007).
39. Herquel, B. et al. Transcription cofactors TRIM24, TRIM28, and TRIM33 associate to form regulatory complexes that suppress murine hepatocellular carcinoma. Proc. Natl. Acad. Sci. USA 108, 8212-8217 (2011).