Characteristic bimodal profiles of RNA polymerase II at thousands of active mammalian promoters

Genome Biology

Volumn 15, Issue 6, 2014, Pages

  Quinodoz, Mathieu ^a   Gobet, Cédric ^a   Naef, Felix ^a   Gustafson, Kyle B ^a,b  

^a EPFL   (Switzerland)

^b UNIVERSITY OF LAUSANNE   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL FACTOR; DRB SENSITIVITY INDUCING FACTOR; ELONGATION FACTOR; HISTONE; MESSENGER RNA; NEGATIVE ELONGATION FACTOR; RNA POLYMERASE II; UNCLASSIFIED DRUG; PROTEIN BINDING;

ANIMAL TISSUE; ARTICLE; BASE PAIRING; CHROMATIN IMMUNOPRECIPITATION; CPG ISLAND; ENZYME BINDING; ENZYME STRUCTURE; GENE SEQUENCE; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; MAMMAL; MOUSE; NONHUMAN; NUCLEOSOME; NUCLEOTIDE SEQUENCE; PROMOTER REGION; RNA SEQUENCE; TATA BOX; TRANSCRIPTION INITIATION SITE; ANIMAL; GENETICS; HELA CELL LINE; METABOLISM; PHYSIOLOGY;

MAMMALIA;

ANIMALS; CHROMATIN IMMUNOPRECIPITATION; HELA CELLS; HISTONES; HUMANS; MICE; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; RNA POLYMERASE II; RNA, MESSENGER; TRANSCRIPTION INITIATION SITE; TRANSCRIPTION, GENETIC;

EID: 84912085999     PISSN: 14747596     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/gb-2014-15-6-r85     Document Type: Article

References (55)

1. Strobl LJ, Eick D: Hold back of RNA polymerase II at the transcription start site mediates down-regulation of c-myc in vivo. EMBO J 1992, 11:3307-3314.
2. Ptashne M, Gann A: Transcriptional activation by recruitment. Nature 1997, 386:569-577.
3. Guenther MG, Levine SS, Boyer LA, Jaenisch R, Young RA: A chromatin landmark and transcription initiation atmost promoters in human cells. Cell 2007, 130:77-88.
4. Gilmour DS, Lis JT: RNA polymerase II interacts with the promoter region of the noninduced hsp70 gene in Drosophila melanogaster cells.Mol Cell Biol 1986, 6:3984.
5. Adelman K, Lis JT: Promoter-proximal pausing of RNA polymerase II: emerging roles inmetazoans. Nat Genet 2012, 13:720-731.
6. Nechaev S, Adelman K: Pol II waiting in the starting gates: regulating the transition from transcription initiation into productive elongation. Biochim Biophys Acta 2011, 1809:34-45.
7. Mavrich TN, Jiang C, Ioshikhes IP, Li X, Venters BJ, Zanton SJ, Tomsho LP, Qi J, Glaser RL, Schuster SC, Gilmour DS, Albert I, Pugh BF: Nucleosome organization in the Drosophila genome. Nature 2008, 453:358-362.
8. Rasmussen EB, Lis JT: In vivo transcriptional pausing and cap formation on three Drosophila heat shock genes. Proc Natl Acad Sci USA 1993, 90:7923-7927.
9. Kwak H, Fuda NJ, Core LJ, Lis JT: Precisemaps of RNA polymerase reveal how promoters direct initiation and pausing. Science 2013, 339:950-953.
10. Core LJ, Waterfall JJ, Lis JT: Nascent RNA sequencing reveals widespread pausing and divergent initiation at human promoters. Science 2008, 322:1845-1848.
11. Min IM, Waterfall JJ, Core LJ, Munroe RJ, Schimenti J, Lis JT: Regulating RNA polymerase pausing and transcription elongation in embryonic stem cells. Genes Dev 2011, 25:742-754.
12. Zeitlinger J, Stark A, Kellis M, Hong J-W, Nechaev S, Adelman K, Levine M, Young RA: RNA polymerase stalling at developmental control genes in the Drosophila melanogaster embryo. Nat Genet 2007, 39:1512-1516.
13. Muse GW, Gilchrist DA, Nechaev S, Shah R, Parker JS, Grissom SF, Zeitlinger J, Adelman K: RNA polymerase is poised for activation across the genome. Nat Genet 2007, 39:1507-1511.
14. Seila AC, Calabrese JM, Levine SS, Yeo GW, Rahl PB, Flynn RA, Young RA, Sharp PA: Divergent transcription from active promoters. Science 2008, 322:1849-1851.
15. Sultan M, Schulz MH, Richard H, Magen A, Klingenhoff A, Scherf M, Seifert M, Borodina T, Soldatov A, Parkhomchuk D, Schmidt D, O'Keeffe S, Haas S, Vingron M, Lehrach H, Yaspo ML: A global view of gene activity and alternative splicing by deep sequencing of the human transcriptome. Sci (New York, NY) 2008, 321:956-960.
16. Rahl PB, Lin CY, Seila AC, Flynn RA, McCuine S, Burge CB, Sharp PA, Young RA: c-Myc regulates transcriptional pause release. Cell 2010, 141:432-445.
17. Gilchrist DA, Dos Santos G, Fargo DC, Xie B, Gao Y, Li L, Adelman K: Pausing of RNA polymerase II disrupts DNA-specified nucleosome organization to enable precise gene regulation. Cell 2010, 143:540-551.
18. Yin H, Sweeney S, Raha D, Snyder M, Lin H: A high-resolution whole-genome map of key chromatinmodifications in the adult Drosophila melanogaster. PLoS Genet 2011, 7:1002380.
19. Rhee HS, Pugh BF: Genome-wide structure and organization of eukaryotic pre-initiation complexes. Nature 2012, 483:295-301.
20. Li J, Liu Y, Rhee HS, Ghosh SKB, Bai L, Pugh BF, Gilmour DS: Kinetic competition between elongation rate and binding of NELF controls promoter-proximal pausing. Mol Cell 2013, 50:711-722.
21. Fenouil R, Cauchy P, Koch F, Descostes N, Cabeza JZ, Innocenti C, Ferrier P, Spicuglia S, Gut M, Gut I, Andrau JC: CpG islands and GC content dictate nucleosome depletion in a transcription-independent manner atmammalian promoters. Genome Res 2012, 22:2399-2408.
22. Le Martelot G, Canella D, Symul L, Migliavacca E, Gilardi F, Liechti R, Martin O, Harshman K, Delorenzi M, Desvergne B, Herr W, Deplancke B, Schibler U, Rougemont J, Guex N, Hernandez N, Naef F, The CycliX consortium: Genome-wide RNA polymerase II profiles and RNA accumulation reveal kinetics of transcription and associated epigenetic changes during diurnal cycles. PLoS Biol 2012, 10:1001442.
23. Liu P, Xiang Y, Fujinaga K, Bartholomeeusen K, Nilson K, Price DH, Peterlin BM: Release of P-TEFb from 7SK snRNP activates HEXIM1 transcription. J Biol Chem 2014, 289:9918-9925.
24. Kwak H, Lis JT: Control of transcriptional elongation. Ann Rev Genet 2013, 47:483-508.
25. Yang MQ, Koehly LM, Elnitski LL: Comprehensive annotation of bidirectional promoters identifies co-regulation among breast and ovarian cancer genes. PLoS Comp Bio 2007, 3:72.
26. Barski A, Cuddapah S, Cui K, Roh T-Y, Schones DE, Wang Z, Wei G, Chepelev I, Zhao K: High-resolution profiling of histone methylations in the human genome. Cell 2007, 129:823-837.
27. Lauberth SM, Nakayama T, Wu X, Ferris AL, Tang Z, Hughes SH, Roeder RG: H3K4me3 interactions with TAF3 regulate preinitiation complex assembly and selective gene activation. Cell 2013, 152:1021-1036.
28. Brannan K, Kim H, Erickson B, Glover-Cutter K, Kim S, Fong N, Kiemele L, Hansen K, Davis R, Lykke-Andersen J, Bentley DL: mRNA decapping factors and the exonuclease Xrn2 function in widespread premature termination of RNA polymerase II transcription. Mol Cell 2012, 46:311-324.
29. Carninci P, Sandelin A, Lenhard B, Katayama S, Shimokawa K, Ponjavic J, Semple CAM, Taylor MS, Engström PG, Frith MC, Forrest ARR, Alkema WB, Tan SL, Plessy C, Kodzius R, Ravasi T, Kasukawa T, Fukuda S, Kanamori-Katayama M, Kitazume Y, Kawaji H, Kai C, Nakamura M, Konno H, Nakano K, Mottagui-Tabar S, Arner P, Chesi A, Gustincich S, Persichetti F, et al: Genome-wide analysis of mammalian promoter architecture and evolution. Nat Genet 2006, 38:626-635.
30. Balwierz PJ, Carninci P, Daub CO, Kawai J, Hayashizaki Y, Van Belle W, Beisel C, van Nimwegen E: Methods for analyzing deep sequencing expression data: constructing the human and mouse promoterome with deepCAGE data. Genome Biol 2009, 10:79.
31. Rach EA, Winter DR, Benjamin AM, Corcoran DL, Ni T, Zhu J, Ohler U: Transcription initiation patterns indicate divergent strategies for gene regulation at the chromatin level. PLoS Genet 2011, 7:1001274.
32. Hansen KD, Brenner SE, Dudoit S: Biases in Illumina transcriptome sequencing caused by random hexamer priming. Nucleic Acids Res 2010, 38:131.
33. Roberts A, Trapnell C, Donaghey J, Rinn JL, Pachter L: Improving RNA-seq expression estimates by correcting for fragment bias. Genome Biol 2011, 12:22.
34. Kawaji H, Severin J, Lizio M, Forrest ARR, van Nimwegen E, Rehli M, Schroder K, Irvine K, Suzuki H, Carninci P, Hayashizaki Y, Daub CO: Update of the FANTOM web resource: frommammalian transcriptional landscape to its dynamic regulation. Nucleic Acids Res 2010, 39:856-860.
35. Haberle V: CAGEr: analysis of CAGE (cap analysis of gene expression) sequencing data for precisemapping of transcription start sites and promoteromemining. [http://bioconductor.org/packages/release/bioc/html/CAGEr.html]
36. Vogel C, de Sousa Abreu R, Ko D, Le S-Y, Shapiro BA, Burns SC, Sandhu D, Boutz DR, Marcotte EM, Penalva LO: Sequence signatures and mRNA concentration can explain two-thirds of protein abundance variation in a human cell line. Mol Syst Biol 2010, 6:400.
37. Valen E, Sandelin A: Genomic and chromatin signals underlying transcription start-site selection. Cell 2011, 27:475-485.
38. Bucher P: Weight matrix descriptions of four eukaryotic RNA polymerase II promoter elements derived from 502 unrelated promoter sequences. JMol Biol 1990, 212:563-578.
39. Vavouri T, Lehner B: Human genes with CpG island promoters have a distinct transcription-associated chromatin organization. Genome Biol 2012, 13:110.
40. Karlić R, Chung H-R, Lasserre J, Vlahoviček K, Vingron M: Histone modification levels are predictive for gene expression. PNAS 2010, 107:2926-2931.
41. Guo J, Price DH: RNA polymerase II transcription elongation control. Chem Rev 2013, 113:8583-8603.
42. Li J, Gilmour DS: Distinctmechanisms of transcriptional pausing orchestrated by GAGA factor and M1BP, a novel transcription factor. EMBO J 2013, 32:1829-1841.
43. Skene PJ, Hernandez AE, Groudine M, Henikoff S, Espinosa JM: The nucleosomal barrier to promoter escape by RNA polymerase II is overcome by the chromatin remodeler Chd1. eLife 2014, 3:e02042.
44. Reppas NB, Wade JT, Church GM, Struhl K: The transition between transcriptional initiation and elongation in E. coli is highly variable and often rate limiting. Mol Cell 2006, 24:747-757.
45. Danko CG, Hah N, Luo X, Martins AL, Core L, Lis JT, Siepel A, Kraus WL: Signaling pathways differentially affect RNA polymerase II initiation, pausing, and elongation rate in cells. Mol Cell 2013, 50:212-222.
46. Brookes E, Pombo A: Modifications of RNA polymerase II are pivotal in regulating gene expression states. EMBO Rep 2009, 10:1213-1219.
47. Koike N, Yoo SH, Huang HC, Kumar V, Lee C, Kim TK, Takahashi JS: Transcriptional architecture and chromatin landscape of the core circadian clock in mammals. Science 2012, 338:349-354.
48. Langmead B, Trapnell C, Pop M, Salzberg SL: Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 2009, 10:25.
49. Pepke S, Wold B, Mortazavi A: Computation for ChIP-seq and RNA-seq studies. Nat Methods 2009, 6:22-32.
50. Andrews S: FastQC a quality control tool for high throughput sequence data. [http://www.bioinformatics.babraham.ac.uk/projects/fastqc]
51. Lebedeva S, Jens M, Theil K, Schwanhäusser B, Selbach M, Landthaler M, Rajewsky N: Transcriptome-wide analysis of regulatory interactions of the RNA-binding protein HuR. Mol Cell 2011, 43:340-352.
52. Jouffe C, Cretenet G, Symul L, Martin E, Atger F, Naef F, Gachon F: The circadian clock coordinates ribosome biogenesis. PLoS Biol 2013, 11:1001455.
53. Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, Batut P, Chaisson M, Gingeras TR: STAR: ultrafast universal RNA-seq aligner. Bioinformatics 2013, 29:15-21.
54. Pearson WR, Lipman DJ: Improved tools for biological sequence comparison. PNAS 1988, 85:2444-2448.
55. CycliX database. [cyclix.vital-it.ch]