Methylation of RNA polymerase II non-consensus Lysine residues marks early transcription in mammalian cells

eLife

Volumn 4, Issue DECEMBER2015, 2015, Pages

  Dias, João D ^a,b,c   Rito, Tiago ^a   Triglia, Elena Torlai ^a   Kukalev, Alexander ^a   Ferrai, Carmelo ^a,b   Chotalia, Mita ^b   Brookes, Emily ^b,e   Kimura, Hiroshi ^d   Pombo, Ana ^a,b  

^a MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY OF PORTO   (Portugal)

^d TOKYO INSTITUTE OF TECHNOLOGY   (Japan)

^e UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

RNA POLYMERASE II; LYSINE; SERINE;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; CELL VIABILITY; CHROMATIN IMMUNOPRECIPITATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE MUTATION; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN METHYLATION; PROTEIN PHOSPHORYLATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA TRANSCRIPTION; WESTERN BLOTTING; ANIMAL; CONSENSUS; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; METABOLISM; METHYLATION; NIH 3T3 CELL LINE; PHOSPHORYLATION; PROTEIN PROCESSING;

ANIMALS; CONSENSUS; GENE EXPRESSION REGULATION; LYSINE; METHYLATION; MICE; NIH 3T3 CELLS; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; RNA POLYMERASE II; SERINE; TRANSCRIPTION, GENETIC;

EID: 84964357500     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.11215     Document Type: Article

References (51)

1. Akhtar MS, Heidemann M, Tietjen JR, Zhang DW, Chapman RD, Eick D, Ansari AZ. 2009. TFIIH kinase places bivalent marks on the carboxy-terminal domain of RNA polymerase II. Molecular Cell 34:387-393. doi: 10.1016/j.molcel.2009.04.016
2. Anders S, Pyl PT, Huber W. 2015. HTSeq-a python framework to work with high-throughput sequencing data. Bioinformatics 31:166-169. doi: 10.1093/bioinformatics/btu638
3. Bannister AJ, Kouzarides T. 2011. Regulation of chromatin by histone modifications. Cell Research 21:381-395. doi: 10.1038/cr.2011.22
4. Bentley DL. 2014. Coupling mRNA processing with transcription in time and space. Nature Reviews. Genetics 15:163-175. doi: 10.1038/nrg3662
5. Biggar KK, Li SS. 2015. Non-histone protein methylation as a regulator of cellular signalling and function. Nature Reviews. Molecular Cell Biology 16:5-17. doi: 10.1038/nrm3915
6. Billon N, Jolicoeur C, Ying QL, Smith A, Raff M. 2002. Normal timing of oligodendrocyte development from genetically engineered, lineage-selectable mouse ES cells. Journal of Cell Science 115:3657-3665. doi: 10.1242/jcs.00049
7. Bonn S, Zinzen RP, Perez-Gonzalez A, Riddell A, Gavin AC, Furlong EE. 2012. Cell type-specific chromatin immunoprecipitation from multicellular complex samples using BiTS-ChIP. Nature Protocols 7:978-994. doi: 10.1038/nprot.2012.049
8. Brookes E, Pombo A. 2009. Modifications of RNA polymerase II are pivotal in regulating gene expression states. EMBO Reports 10:1213-1219. doi: 10.1038/embor.2009.221
9. Brookes E, de Santiago I, Hebenstreit D, Morris KJ, Carroll T, Xie SQ, Stock JK, Heidemann M, Eick D, Nozaki N, Kimura H, Ragoussis J, Teichmann SA, Pombo A. 2012. Polycomb associates genome-wide with a specific RNA polymerase II variant, and regulates metabolic genes in ESCs. Cell Stem Cell 10:157-170. doi: 10.1016/j.stem.2011.12.017
10. Buratowski S. 2003. The CTD code. Nature Structural Biology 10:679-680. doi: 10.1038/nsb0903-679
11. Buratowski S. 2009. Progression through the RNA polymerase II CTD cycle. Molecular Cell 36:541-546. doi: 10.1016/j.molcel.2009.10.019
12. Chao SH, Price DH. 2001. Flavopiridol inactivates p-TEFb and blocks most RNA polymerase II transcription in vivo. The Journal of Biological Chemistry 276:31793-31799. doi: 10.1074/jbc.M102306200
13. Chapman RD, Conrad M, Eick D. 2005. Role of the mammalian RNA polymerase II C-terminal domain (CTD) nonconsensus repeats in CTD stability and cell proliferation. Molecular and Cellular Biology 25:7665-7674. doi: 10.1128/MCB.25.17.7665-7674.2005
14. Chapman RD, Heidemann M, Albert TK, Mailhammer R, Flatley A, Meisterernst M, Kremmer E, Eick D. 2007. Transcribing RNA polymerase II is phosphorylated at CTD residue serine-7. Science 318:1780-1782. doi: 10.1126/science.1145977
15. Chapman RD, Heidemann M, Hintermair C, Eick D. 2008. Molecular evolution of the RNA polymerase II CTD. Trends in Genetics: TIG 24:289-296. doi: 10.1016/j.tig.2008.03.010
16. Corden JL. 2013. RNA polymerase II C-terminal domain: tethering transcription to transcript and template. Chemical Reviews 113:8423-8455. doi: 10.1021/cr400158h
17. Darzacq X, Shav-Tal Y, de Turris V, Brody Y, Shenoy SM, Phair RD, Singer RH. 2007. In vivo dynamics of RNA polymerase II transcription. Nature Structural Molecular Biology 14:796-806. doi: 10.1038/nsmb1280
18. Efron B. 2013. Lars: least angle regression, lasso and forward stagewise, pp. R Package Version 1:2.
19. Egloff S, Dienstbier M, Murphy S. 2012. Updating the RNA polymerase CTD code: adding gene-specific layers. Trends in Genetics 28:333-341. doi: 10.1016/j.tig.2012.03.007
20. Eick D, Geyer M. 2013. The RNA polymerase II carboxy-terminal domain (CTD) code. Chemical Reviews 113: 8456-8490. doi: 10.1021/cr400071f
21. Ghosh A, Shuman S, Lima CD. 2011. Structural insights to how mammalian capping enzyme reads the CTD code. Molecular Cell 43:299-310. doi: 10.1016/j.molcel.2011.06.001
22. Gu B, Eick D, Bensaude O. 2013. CTD serine-2 plays a critical role in splicing and termination factor recruitment to RNA polymerase II in vivo. Nucleic Acids Research 41:1591-1603. doi: 10.1093/nar/gks1327
23. Hamamoto R, Saloura V, Nakamura Y. 2015. Critical roles of non-histone protein lysine methylation in human tumorigenesis. Nature Reviews Cancer 15:110-124. doi: 10.1038/nrc3884
24. Hintermair C, Heidemann M, Koch F, Descostes N, Gut M, Gut I, Fenouil R, Ferrier P, Flatley A, Kremmer E, Chapman RD, Andrau J-C, Eick D. 2012. Threonine-4 of mammalian RNA polymerase II CTD is targeted by polo-like kinase 3 and required for transcriptional elongation. The EMBO Journal 31:2784-2797. doi: 10.1038/emboj.2012.123
25. Hsin J-P, Manley JL. 2012. The RNA polymerase II CTD coordinates transcription and RNA processing. Genes & Development 26:2119-2137. doi: 10.1101/gad.200303.112
26. Jonkers I, Kwak H, Lis JT. 2014. Genome-wide dynamics of pol II elongation and its interplay with promoter proximal pausing, chromatin, and exons. eLife 3:e02407. doi: 10.7554/eLife.02407
27. Karantzal E, Schulz H, Hummel O, Hubner N, Hatzopoulos AK, Kretsovali A. 2008. Histone deacetylase inhibition accelerates the early events of stem cell differentiation: transcriptomic and epigenetic analysis. Genome Biology 9:R65. doi: 10.1186/gb-2008-9-4-r65
28. Kimura H, Hayashi-Takanaka Y, Goto Y, Takizawa N, Nozaki N. 2008. The organization of histone H3 modifications as revealed by a panel of specific monoclonal antibodies. Cell Structure and Function 33:61-73. doi: 10.1247/csf.07035
29. Kishore SP, Perkins SL, Templeton TJ, Deitsch KW. 2009. An unusual recent expansion of the C-terminal domain of RNA polymerase II in primate malaria parasites features a motif otherwise found only in mammalian polymerases. Journal of Molecular Evolution 68:706-714. doi: 10.1007/s00239-009-9245-2
30. Kolde, R. (2015). Pheatmap: Pretty Heatmaps.
31. Langmead B, Salzberg SL. 2012. Fast gapped-read alignment with bowtie 2. Nature Methods 9:357-359. doi: 10.1038/nmeth.1923
32. Litingtung Y, Lawler AM, Sebald SM, Lee E, Gearhart JD, Westphal H, Corden JL. 1999. Growth retardation and neonatal lethality in mice with a homozygous deletion in the C-terminal domain of RNA polymerase II. MGG -Molecular and General Genetics 261:100-105. doi: 10.1007/s004380050946
33. Liu P, Kenney JM, Stiller JW, Greenleaf AL. 2010. Genetic organization, length conservation, and evolution of RNA polymerase II carboxyl-terminal domain. Molecular Biology and Evolution 27:2628-2641. doi: 10.1093/molbev/msq151
34. Lunde BM, Reichow SL, Kim M, Suh H, Leeper TC, Yang F, Mutschler H, Buratowski S, Meinhart A, Varani G. 2010. Cooperative interaction of transcription termination factors with the RNA polymerase II c-terminal domain. Nature Structural & Molecular Biology 17:1195-1201. doi: 10.1038/nsmb.1893
35. Mikkelsen TS, Ku M, Jaffe DB, Issac B, Lieberman E, Giannoukos G, Alvarez P, Brockman W, Kim T-K, Koche RP, Lee W, Mendenhall E, O’Donovan A, Presser A, Russ C, Xie X, Meissner A, Wernig M, Jaenisch R, Nusbaum C, Lander ES, Bernstein BE. 2007. Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 448:553-560. doi: 10.1038/nature06008
36. Muñoz MJ, Santangelo MSP, Paronetto MP, de la Mata M, Pelisch F, Boireau S, Glover-Cutter K, Ben-Dov C, Blaustein M, Lozano JJ, Bird G, Bentley D, Bertrand E, Kornblihtt AR. 2009. DNA damage regulates alternative splicing through inhibition of RNA polymerase II elongation. Cell 137:708-720. doi: 10.1016/j.cell.2009.03.010
37. Nguyen VT, Giannoni F, Dubois MF, Seo SJ, Vigneron M, Kédinger C, Bensaude O. 1996. In vivo degradation of RNA polymerase II largest subunit triggered by alpha-amanitin. Nucleic Acids Research 24:2924-2929. doi: 10.1093/nar/24.15.2924
38. Niwa H, Smith AG, Jun-ichi M. 2000. Quantitative expression of oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells. Nature Genetics 24:372-376. doi: 10.1038/74199
39. Quinodoz M, Gobet C, Naef F, Gustafson KB. 2014. Characteristic bimodal profiles of RNA polymerase II at thousands of active mammalian promoters. Genome Biology 15:R85. doi: 10.1186/gb-2014-15-6-r85
40. Rechtsteiner A, Ercan S, Takasaki T, Phippen TM, Egelhofer TA, Wang W, Kimura H, Lieb JD, Strome S, Reik W. 2010. The histone H3K36 methyltransferase MES-4 acts epigenetically to transmit the memory of germline gene expression to progeny. PLoS Genetics 6:e1001091. doi: 10.1371/journal.pgen.1001091
41. Schröder S, Herker E, Itzen F, He D, Thomas S, Gilchrist DA, Kaehlcke K, Cho S, Pollard KS, Capra JA, Schnölzer M, Cole PA, Geyer M, Bruneau BG, Adelman K, Ott M. 2013. Acetylation of RNA polymerase II regulates growth-factor-induced gene transcription in mammalian cells. Molecular Cell 52:314-324. doi: 10.1016/j.molcel.2013.10.009
42. Simonti CN, Pollard KS, Schröder S, He D, Bruneau BG, Ott M, Capra JA. 2015. Evolution of lysine acetylation in the RNA polymerase II C-terminal domain. BMC Evolutionary Biology 15:35. doi: 10.1186/s12862-015-0327-z
43. Sims RJ, Rojas LA, Beck D, Bonasio R, Schuller R, Drury WJ, Eick D, Reinberg D. 2011. The C-terminal domain of RNA polymerase II is modified by site-specific methylation. Science 332:99-103. doi: 10.1126/science.1202663
44. Stock JK, Giadrossi S, Casanova M, Brookes E, Vidal M, Koseki H, Brockdorff N, Fisher AG, Pombo A. 2007. Ring1-mediated ubiquitination of H2A restrains poised RNA polymerase II at bivalent genes in mouse ES cells. Nature Cell Biology 9:1428-1435. doi: 10.1038/ncb1663
45. Tee W-W, Shen SS, Oksuz O, Narendra V, Reinberg D. 2014. Erk1/2 activity promotes chromatin features and RNAPII phosphorylation at developmental promoters in mouse ESCs. Cell 156:678-690. doi: 10.1016/j.cell.2014.01.009
46. Tietjen JR, Zhang DW, Rodríguez-Molina JB, White BE, Akhtar MS, Heidemann M, Li X, Chapman RD, Shokat K, Keles S, Eick D, Ansari AZ. 2010. Chemical-genomic dissection of the CTD code. Nature Structural & Molecular Biology 17:1154-1161. doi: 10.1038/nsmb.1900
47. Winsor TS, Bartkowiak B, Bennett CB, Greenleaf AL, Lustig AJ. 2013. A DNA damage response system associated with the phosphoCTD of elongating RNA polymerase II. PLoS ONE 8:e60909. doi: 10.1371/journal.pone.0060909
48. Wozniak GG, Strahl BD. 2014. Hitting the ‘mark’: interpreting lysine methylation in the context of active transcription. Biochimica Et Biophysica Acta (BBA) - Gene Regulatory Mechanisms 1839:1353-1361. doi: 10.1016/j.bbagrm.2014.03.002
49. Xie SQ, Martin S, Guillot PV, Bentley DL, Pombo A. 2006. Splicing speckles are not reservoirs of RNA polymerase II, but contain an inactive form, phosphorylated on Serine2 residues of the C-terminal domain. Molecular Biology of the Cell 17:1723-1733. doi: 10.1091/mbc.E05-08-0726
50. Xing H, Mo Y, Liao W, Zhang MQ, Ioshikhes I. 2012. Genome-wide localization of protein-DNA binding and histone modification by a bayesian change-point method with ChIP-seq data. PLoS Computational Biology 8: e1002613. doi: 10.1371/journal.pcbi.1002613
51. Yang C, Stiller JW. 2014. Evolutionary diversity and taxon-specific modifications of the RNA polymerase II c-terminal domain. Proceedings of the National Academy of Sciences 111:5920-5925. doi: 10.1073/pnas.1323616111