Chd1 co-localizes with early transcription elongation factors independently of H3K36 methylation and releases stalled RNA polymerase II at introns

Epigenetics and Chromatin

Volumn 7, Issue 1, 2014, Pages

  Park, Daechan ^a   Shivram, Haridha ^a   Iyer, Vishwanath R ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

Chromatin remodeling; Chromodomain helicase DNA binding protein 1 (Chd1); H3K36 methylation; Intron; Transcription elongation

Indexed keywords

CHROMODOMAIN HELICASE DNA BINDING PROTEIN 1; DNA BINDING PROTEIN; ELONGATION FACTOR; RNA POLYMERASE II; UNCLASSIFIED DRUG;

ARTICLE; BIOINFORMATICS; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; FUNGAL STRAIN; HISTONE METHYLATION; IMMUNOBLOTTING; INTRON; MUTANT; NONHUMAN; NUCLEOSOME; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SACCHAROMYCES CEREVISIAE; TRANSCRIPTION ELONGATION;

EID: 84988935720     PISSN: None     EISSN: 17568935     Source Type: Journal    
DOI: 10.1186/1756-8935-7-32     Document Type: Article

References (45)

1. Iyer VR: Nucleosome positioning: bringing order to the eukaryotic genome. Trends Cell Biol 2012, 22:250-256.
2. Yuan GC, Liu YJ, Dion MF, Slack MD, Wu LF, Altschuler SJ, Rando OJ: Genome-scale identification of nucleosome positions in S. cerevisiae. Science 2005, 309:626-630.
3. Lee W, Tillo D, Bray N, Morse RH, Davis RW, Hughes TR, Nislow C: A highresolution atlas of nucleosome occupancy in yeast. Nat Genet 2007, 39:1235-1244.
4. Shivaswamy S, Bhinge A, Zhao Y, Jones S, Hirst M, Iyer VR: Dynamic remodeling of individual nucleosomes across a eukaryotic genome in response to transcriptional perturbation. PLoS Biol 2008, 6:e65.
5. Kaplan N, Moore IK, Fondufe-Mittendorf Y, Gossett AJ, Tillo D, Field Y, LeProust EM, Hughes TR, Lieb JD, Widom J, Segal E: The DNA-encoded nucleosome organization of a eukaryotic genome. Nature 2009, 458:362-366.
6. Segal E, Fondufe-Mittendorf Y, Chen L, Thastrom A, Field Y, Moore IK, Wang JP, Widom J: A genomic code for nucleosome positioning. Nature 2006, 442:772-778.
7. Zhang Z, Wippo CJ, Wal M, Ward E, Korber P, Pugh BF: A packing mechanism for nucleosome organization reconstituted across a eukaryotic genome. Science 2011, 332:977-980.
8. Yen K, Vinayachandran V, Batta K, Koerber RT, Pugh BF: Genome-wide nucleosome specificity and directionality of chromatin remodelers. Cell 2012, 149:1461-1473.
9. Tirosh I, Sigal N, Barkai N: Widespread remodeling of mid-coding sequence nucleosomes by Isw1. Genome Biol 2010, 11:R49.
10. Gkikopoulos T, Schofield P, Singh V, Pinskaya M, Mellor J, Smolle M, Workman JL, Barton GJ, Owen-Hughes T: A role for Snf2-related nucleosome-spacing enzymes in genome-wide nucleosome organization. Science 2011, 333:1758-1760.
11. van Bakel H, Tsui K, Gebbia M, Mnaimneh S, Hughes TR, Nislow C: A compendium of nucleosome and transcript profiles reveals determinants of chromatin architecture and transcription. PLoS Genet 2013, 9:e1003479.
12. Hennig BP, Bendrin K, Zhou Y, Fischer T: Chd1 chromatin remodelers maintain nucleosome organization and repress cryptic transcription. EMBO Rep 2012, 13:997-1003.
13. Shim YS, Choi Y, Kang K, Cho K, Oh S, Lee J, Grewal SI, Lee D: Hrp3 controls nucleosome positioning to suppress non-coding transcription in eu-and heterochromatin. EMBO J 2012, 31:4375-4387.
14. Simic R, Lindstrom DL, Tran HG, Roinick KL, Costa PJ, Johnson AD, Hartzog GA, Arndt KM: Chromatin remodeling protein Chd1 interacts with transcription elongation factors and localizes to transcribed genes. EMBO J 2003, 22:1846-1856.
15. Warner MH, Roinick KL, Arndt KM: Rtf1 is a multifunctional component of the Paf1 complex that regulates gene expression by directing cotranscriptional histone modification. Mol Cell Biol 2007, 27:6103-6115.
16. Zentner GE, Tsukiyama T, Henikoff S: ISWI and CHD chromatin remodelers bind promoters but act in gene bodies. PLoS Genet 2013, 9:e1003317.
17. Pray-Grant MG, Daniel JA, Schieltz D, Yates JR 3rd, Grant PA: Chd1 chromodomain links histone H3 methylation with SAGA-and SLIK-dependent acetylation. Nature 2005, 433:434-438.
18. Sims RJ 3rd, Chen CF, Santos-Rosa H, Kouzarides T, Patel SS, Reinberg D: Human but not yeast CHD1 binds directly and selectively to histone H3 methylated at lysine 4 via its tandem chromodomains. J Biol Chem 2005, 280:41789-41792.
19. Flanagan JF, Blus BJ, Kim D, Clines KL, Rastinejad F, Khorasanizadeh S: Molecular implications of evolutionary differences in CHD double chromodomains. J Mol Biol 2007, 369:334-342.
20. Li B, Gogol M, Carey M, Lee D, Seidel C, Workman JL: Combined action of PHD and chromo domains directs the Rpd3S HDAC to transcribed chromatin. Science 2007, 316:1050-1054.
21. Li B, Jackson J, Simon MD, Fleharty B, Gogol M, Seidel C, Workman JL, Shilatifard A: Histone H3 lysine 36 dimethylation (H3K36me2) is sufficient to recruit the Rpd3s histone deacetylase complex and to repress spurious transcription. J Biol Chem 2009, 284:7970-7976.
22. Hon GC, Hawkins RD, Ren B: Predictive chromatin signatures in the mammalian genome. Hum Mol Genet 2009, 18:R195-R201.
23. Smolle M, Venkatesh S, Gogol MM, Li H, Zhang Y, Florens L, Washburn MP, Workman JL: Chromatin remodelers Isw1 and Chd1 maintain chromatin structure during transcription by preventing histone exchange. Nat Struct Mol Biol 2012, 19:884-892.
24. Radman-Livaja M, Quan TK, Valenzuela L, Armstrong JA, van Welsem T, Kim T, Lee LJ, Buratowski S, van Leeuwen F, Rando OJ, Hartzog GA: A key role for Chd1 in histone H3 dynamics at the 3' ends of long genes in yeast. PLoS Genet 2012, 8:e1002811.
25. Park D, Morris AR, Battenhouse A, Iyer VR: Simultaneous mapping of transcript ends at single-nucleotide resolution and identification of widespread promoter-associated non-coding RNA governed by TATA elements. Nucleic Acids Res 2014, 42:3736-3749.
26. Shivaswamy S, Iyer VR: Stress-dependent dynamics of global chromatin remodeling in yeast: dual role for SWI/SNF in the heat shock stress response. Mol Cell Biol 2008, 28:2221-2234.
27. Tran HG, Steger DJ, Iyer VR, Johnson AD: The chromo domain protein chd1p from budding yeast is an ATP-dependent chromatin-modifying factor. EMBO J 2000, 19:2323-2331.
28. Lee JS, Garrett AS, Yen K, Takahashi YH, Hu D, Jackson J, Seidel C, Pugh BF, Shilatifard A: Codependency of H2B monoubiquitination and nucleosome reassembly on Chd1. Genes Dev 2012, 26:914-919.
29. Cheung V, Chua G, Batada NN, Landry CR, Michnick SW, Hughes TR, Winston F: Chromatin-and transcription-related factors repress transcription from within coding regions throughout the Saccharomyces cerevisiae genome. PLoS Biol 2008, 6:e277.
30. Quan TK, Hartzog GA: Histone H3K4 and K36 methylation, Chd1 and Rpd3S oppose the functions of Saccharomyces cerevisiae Spt4-Spt5 in transcription. Genetics 2010, 184:321-334.
31. Alexander RD, Innocente SA, Barrass JD, Beggs JD: Splicing-dependent RNA polymerase pausing in yeast. Mol Cell 2010, 40:582-593.
32. Carrillo Oesterreich F, Preibisch S, Neugebauer KM: Global analysis of nascent RNA reveals transcriptional pausing in terminal exons. Mol Cell 2010, 40:571-581.
33. Wilhelm BT, Marguerat S, Aligianni S, Codlin S, Watt S, Bahler J: Differential patterns of intronic and exonic DNA regions with respect to RNA polymerase II occupancy, nucleosome density and H3K36me3 marking in fission yeast. Genome Biol 2011, 12:R82.
34. Skene PJ, Hernandez AE, Groudine M, Henikoff S: The nucleosomal barrier to promoter escape by RNA polymerase II is overcome by the chromatin remodeler Chd1. Elife 2014, 3:e02042.
35. Park D, Lee Y, Bhupindersingh G, Iyer VR: Widespread misinterpretable ChIP-seq bias in yeast. PLoS ONE 2013, 8:e83506.
36. Carrozza MJ, Li B, Florens L, Suganuma T, Swanson SK, Lee KK, Shia WJ, Anderson S, Yates J, Washburn MP, Workman JL: Histone H3 methylation by Set2 directs deacetylation of coding regions by Rpd3S to suppress spurious intragenic transcription. Cell 2005, 123:581-592.
37. Joshi AA, Struhl K: Eaf3 chromodomain interaction with methylated H3-K36 links histone deacetylation to Pol II elongation. Mol Cell 2005, 20:971-978.
38. Keogh MC, Kurdistani SK, Morris SA, Ahn SH, Podolny V, Collins SR, Schuldiner M, Chin K, Punna T, Thompson NJ, Boone C, Emili A, Weissman JS, Hughes TR, Strahl BD, Grunstein M, Greenblatt JF, Buratowski S, Krogan NJ: Cotranscriptional set2 methylation of histone H3 lysine 36 recruits a repressive Rpd3 complex. Cell 2005, 123:593-605.
39. Schaft D, Roguev A, Kotovic KM, Shevchenko A, Sarov M, Shevchenko A, Neugebauer KM, Stewart AF: The histone 3 lysine 36 methyltransferase, SET2, is involved in transcriptional elongation. Nucleic Acids Res 2003, 31:2475-2482.
40. Winzeler EA, Shoemaker DD, Astromoff A, Liang H, Anderson K, Andre B, Bangham R, Benito R, Boeke JD, Bussey H, Chu AM, Connelly C, Davis K, Dietrich F, Dow SW, El Bakkoury M, Foury F, Friend SH, Gentalen E, Giaever G, Hegemann JH, Jones T, Laub M, Liao H, Liebundguth N, Lockhart DJ, Lucau-Danila A, Lussier M, M'Rabet N, Menard P, et al: Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science 1999, 285:901-906.
41. Longtine MS, McKenzie A 3rd, Demarini DJ, Shah NG, Wach A, Brachat A, Philippsen P, Pringle JR: Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 1998, 14:953-961.
42. Li H, Durbin R: Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 2009, 25:1754-1760.
43. Jiang C, Pugh BF: A compiled and systematic reference map of nucleosome positions across the Saccharomyces cerevisiae genome. Genome Biol 2009, 10:R109.
44. Rizzo JM, Bard JE, Buck MJ: Standardized collection of MNase-seq experiments enables unbiased dataset comparisons. BMC Mol Biol 2012, 13:15.
45. Rizzo JM, Mieczkowski PA, Buck MJ: Tup1 stabilizes promoter nucleosome positioning and occupancy at transcriptionally plastic genes. Nucleic Acids Res 2011, 39:8803-8819.