Human promoters are intrinsically directional

Molecular Cell

Volumn 57, Issue 4, 2015, Pages 674-684

  Duttke, Sascha H C ^a   Lacadie, Scott A ^e   Ibrahim, Mahmoud M ^e,f   Glass, Christopher K ^b,c   Corcoran, David L ^g   Benner, Christopher ^d   Heinz, Sven ^b,d   Kadonaga, James T ^a   Ohler, Uwe ^e,f  

^a SECTION OF MOLECULAR BIOLOGY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^d SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^e MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^f HUMBOLDT UNIVERSITY   (Germany)

^g DUKE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DEOXYRIBONUCLEASE I; RNA POLYMERASE II;

ARTICLE; CHROMATIN; CONTROLLED STUDY; GENE SEQUENCE; HELA CELL LINE; HUMAN; HUMAN CELL; PROMOTER REGION; RNA TRANSCRIPTION; TRANSCRIPTION INITIATION; BIOLOGICAL MODEL; DNA SEQUENCE; GENETIC TRANSCRIPTION; PHYSIOLOGY; TRANSCRIPTION INITIATION SITE;

EUKARYOTA;

HELA CELLS; HUMANS; MODELS, GENETIC; PROMOTER REGIONS, GENETIC; RNA POLYMERASE II; SEQUENCE ANALYSIS, DNA; TRANSCRIPTION INITIATION SITE; TRANSCRIPTION, GENETIC;

EID: 84923997553     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2014.12.029     Document Type: Article

References (57)

1. Adachi N., Lieber M.R. Bidirectional gene organization: a common architectural feature of the human genome. Cell 2002, 109:807-809.
2. Almada A.E., Wu X., Kriz A.J., Burge C.B., Sharp P.A. Promoter directionality is controlled by U1 snRNP and polyadenylation signals. Nature 2013, 499:360-363.
3. Andersson R., Gebhard C., Miguel-Escalada I., Hoof I., Bornholdt J., Boyd M., Chen Y., Zhao X., Schmidl C., Suzuki T., et al. An atlas of active enhancers across human cell types and tissues. Nature 2014, 507:455-461. FANTOM Consortium.
4. Arigo J.T., Eyler D.E., Carroll K.L., Corden J.L. Termination of cryptic unstable transcripts is directed by yeast RNA-binding proteins Nrd1 and Nab3. Mol. Cell 2006, 23:841-851.
5. Bernstein B.E., Birney E., Dunham I., Green E.D., Gunter C., Snyder M. An integrated encyclopedia of DNA elements in the human genome. Nature 2012, 489:57-74. ENCODE Project Consortium.
6. Bilmes J. A gentle tutorial on the EM algorithm and its application to parameter estimation for Gaussian mixture and Hidden Markov Models. International Computer Science Insitute 1997, ICSI-TR 97.
7. Birney E., Stamatoyannopoulos J.A., Dutta A., Guigó R., Gingeras T.R., Margulies E.H., Weng Z., Snyder M., Dermitzakis E.T., Thurman R.E., et al. Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 2007, 447:799-816. ENCODE Project Consortium, NISC Comparative Sequencing ProgramNISC Comparative Sequencing Program, Baylor College of Medicine Human Genome Sequencing CenterBaylor College of Medicine Human Genome Sequencing Center, Washington University Genome Sequencing CenterWashington University Genome Sequencing Center, Broad InstituteBroad Institute, Children's Hospital Oakland Research InstituteChildren's Hospital Oakland Research Institute.
8. Bonn S., Zinzen R.P., Girardot C., Gustafson E.H., Perez-Gonzalez A., Delhomme N., Ghavi-Helm Y., Wilczyński B., Riddell A., Furlong E.E.M. Tissue-specific analysis of chromatin state identifies temporal signatures of enhancer activity during embryonic development. Nat. Genet. 2012, 44:148-156.
9. Boyle A.P., Davis S., Shulha H.P., Meltzer P., Margulies E.H., Weng Z., Furey T.S., Crawford G.E. High-resolution mapping and characterization of open chromatin across the genome. Cell 2008, 132:311-322.
10. Brannan K., Kim H., Erickson B., Glover-Cutter K., Kim S., Fong N., Kiemele L., Hansen K., Davis R., Lykke-Andersen J., Bentley D.L. mRNA decapping factors and the exonuclease Xrn2 function in widespread premature termination of RNA polymerase II transcription. Mol. Cell 2012, 46:311-324.
11. Butler J.E.F., Kadonaga J.T. The RNA polymerase II core promoter: a key component in the regulation of gene expression. Genes Dev. 2002, 16:2583-2592.
12. Carninci P., Kasukawa T., Katayama S., Gough J., Frith M.C., Maeda N., Oyama R., Ravasi T., Lenhard B., Wells C., et al. The transcriptional landscape of the mammalian genome. Science 2005, 309:1559-1563.
13. Core L.J., Waterfall J.J., Lis J.T. Nascent RNA sequencing reveals widespread pausing and divergent initiation at human promoters. Science 2008, 322:1845-1848.
14. Core L.J., Waterfall J.J., Gilchrist D.A., Fargo D.C., Kwak H., Adelman K., Lis J.T. Defining the status of RNA polymerase at promoters. Cell Rep. 2012, 2:1025-1035.
15. Duttke S.H.C. RNA polymerase III accurately initiates transcription from RNA polymerase II promoters invitro. J.Biol. Chem. 2014, 289:20396-20404.
16. Edgar R., Domrachev M., Lash A.E. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 2002, 30:207-210.
17. Ernst J., Kellis M. ChromHMM: automating chromatin-state discovery and characterization. Nat. Methods 2012, 9:215-216.
18. Fenouil R., Cauchy P., Koch F., Descostes N., Cabeza J.Z., Innocenti C., Ferrier P., Spicuglia S., Gut M., Gut I., Andrau J.C. CpG islands and GC content dictate nucleosome depletion in a transcription-independent manner at mammalian promoters. Genome Res. 2012, 22:2399-2408.
19. Frith M.C., Valen E., Krogh A., Hayashizaki Y., Carninci P., Sandelin A. A code for transcription initiation in mammalian genomes. Genome Res. 2008, 18:1-12.
20. Gardiner-Garden M., Frommer M. CpG islands in vertebrate genomes. J.Mol. Biol. 1987, 196:261-282.
21. Greer E.L., Shi Y. Histone methylation: a dynamic mark in health, disease and inheritance. Nat. Rev. Genet. 2012, 13:343-357.
22. Grzechnik P., Tan-Wong S.M., Proudfoot N.J. Terminate and make a loop: regulation of transcriptional directionality. Trends Biochem. Sci. 2014, 39:319-327.
23. Hoffman M.M., Buske O.J., Wang J., Weng Z., Bilmes J.A., Noble W.S. Unsupervised pattern discovery in human chromatin structure through genomic segmentation. Nat. Methods 2012, 9:473-476.
24. Hsin J.-P., Manley J.L. The RNA polymerase II CTD coordinates transcription and RNA processing. Genes Dev. 2012, 26:2119-2137.
25. Ibrahim M.M., Lacadie S.A., Ohler U. JAMM: A Peak Finder for Joint Analysis of NGS Replicates. Bioinformatics 2015, 31:48-55.
26. Kapranov P., Cheng J., Dike S., Nix D.A., Duttagupta R., Willingham A.T., Stadler P.F., Hertel J., Hackermüller J., Hofacker I.L., et al. RNA maps reveal new RNA classes and a possible function for pervasive transcription. Science 2007, 316:1484-1488.
27. Katayama S., Tomaru Y., Kasukawa T., Waki K., Nakanishi M., Nakamura M., Nishida H., Yap C.C., Suzuki M., Kawai J., et al. Antisense transcription in the mammalian transcriptome. Science 2005, 309:1564-1566. RIKEN Genome Exploration Research Group, Genome Science Group (Genome Network Project Core Group)Genome Science Group (Genome Network Project Core Group), FANTOM ConsortiumFANTOM Consortium.
28. Kruesi W.S., Core L.J., Waters C.T., Lis J.T., Meyer B.J. Condensin controls recruitment of RNA polymerase II to achieve nematode X-chromosome dosage compensation. eLife 2013, 2:e00808.
29. Kuhn R.M., Haussler D., Kent W.J. The UCSC genome browser and associated tools. Brief. Bioinform. 2013, 14:144-161.
30. Lam M.T.Y., Cho H., Lesch H.P., Gosselin D., Heinz S., Tanaka-Oishi Y., Benner C., Kaikkonen M.U., Kim A.S., Kosaka M., et al. Rev-Erbs repress macrophage gene expression by inhibiting enhancer-directed transcription. Nature 2013, 498:511-515.
31. Langmead B., Salzberg S.L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 2012, 9:357-359.
32. Lauberth S.M., Nakayama T., Wu X., Ferris A.L., Tang Z., Hughes S.H., Roeder R.G. H3K4me3 interactions with TAF3 regulate preinitiation complex assembly and selective gene activation. Cell 2013, 152:1021-1036.
33. Lawrence M., Huber W., Pagès H., Aboyoun P., Carlson M., Gentleman R., Morgan M.T., Carey V.J. Software for computing and annotating genomic ranges. PLoS Comput. Biol. 2013, 9:e1003118.
34. Lenhard B., Sandelin A., Carninci P. Metazoan promoters: emerging characteristics and insights into transcriptional regulation. Nat. Rev. Genet. 2012, 13:233-245.
35. Lepoivre C., Belhocine M., Bergon A., Griffon A., Yammine M., Vanhille L., Zacarias-Cabeza J., Garibal M.-A., Koch F., Maqbool M.A., et al. Divergent transcription is associated with promoters of transcriptional regulators. BMC Genomics 2013, 14:914.
36. Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet. Journal. 2011, 10.14806/ej.17.1.200.
37. Megraw M., Pereira F., Jensen S.T., Ohler U., Hatzigeorgiou A.G. A transcription factor affinity-based code for mammalian transcription initiation. Genome Res. 2009, 19:644-656.
38. Narlikar L., Jothi R. ChIP-Seq data analysis: identification of protein-DNA binding sites with SISSRs peak-finder. Methods Mol. Biol. 2012, 802:305-322.
39. Natarajan A., Yardimci G.G., Sheffield N.C., Crawford G.E., Ohler U. Predicting cell-type-specific gene expression from regions of open chromatin. Genome Res. 2012, 22:1711-1722.
40. Neil H., Malabat C., d'Aubenton-Carafa Y., Xu Z., Steinmetz L.M., Jacquier A. Widespread bidirectional promoters are the major source of cryptic transcripts in yeast. Nature 2009, 457:1038-1042.
41. Ni T., Corcoran D.L., Rach E.A., Song S., Spana E.P., Gao Y., Ohler U., Zhu J. A paired-end sequencing strategy to map the complex landscape of transcription initiation. Nat. Methods 2010, 7:521-527.
42. Ntini E., Järvelin A.I., Bornholdt J., Chen Y., Boyd M., Jørgensen M., Andersson R., Hoof I., Schein A., Andersen P.R., et al. Polyadenylation site-induced decay of upstream transcripts enforces promoter directionality. Nat. Struct. Mol. Biol. 2013, 20:923-928.
43. Preker P., Nielsen J., Kammler S., Lykke-Andersen S., Christensen M.S., Mapendano C.K., Schierup M.H., Jensen T.H. RNA exosome depletion reveals transcription upstream of active human promoters. Science 2008, 322:1851-1854.
44. Quinlan A.R., Hall I.M. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 2010, 26:841-842.
45. Rach E.A., Winter D.R., Benjamin A.M., Corcoran D.L., Ni T., Zhu J., Ohler U. Transcription initiation patterns indicate divergent strategies for gene regulation at the chromatin level. PLoS Genet. 2011, 7:e1001274.
46. Rhee H.S., Pugh B.F. Genome-wide structure and organization of eukaryotic pre-initiation complexes. Nature 2012, 483:295-301.
47. Schulz D., Schwalb B., Kiesel A., Baejen C., Torkler P., Gagneur J., Soeding J., Cramer P. Transcriptome surveillance by selective termination of noncoding RNA synthesis. Cell 2013, 155:1075-1087.
48. Seila A.C., Calabrese J.M., Levine S.S., Yeo G.W., Rahl P.B., Flynn R.A., Young R.A., Sharp P.A. Divergent transcription from active promoters. Science 2008, 322:1849-1851.
49. Seila A.C., Core L.J., Lis J.T., Sharp P.A. Divergent transcription: a new feature of active promoters. Cell Cycle 2009, 8:2557-2564.
50. Sigova A.A., Mullen A.C., Molinie B., Gupta S., Orlando D.A., Guenther M.G., Almada A.E., Lin C., Sharp P.A., Giallourakis C.C., Young R.A. Divergent transcription of long noncoding RNA/mRNA gene pairs in embryonic stem cells. Proc. Natl. Acad. Sci. USA 2013, 110:2876-2881.
51. Sing T., Sander O., Beerenwinkel N., Lengauer T. ROCR: visualizing classifier performance in R. Bioinformatics 2005, 21:3940-3941.
52. Taramasco, O., and Bauer, S. (2013). RHmm: Hidden Markov Models simulations and estimations. https://r-forge.r-project.org/R/?group_id=85.
53. Thorvaldsdóttir H., Robinson J.T., Mesirov J.P. Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration. Brief. Bioinform. 2013, 14:178-192.
54. Thurman R.E., Rynes E., Humbert R., Vierstra J., Maurano M.T., Haugen E., Sheffield N.C., Stergachis A.B., Wang H., Vernot B., et al. The accessible chromatin landscape of the human genome. Nature 2012, 489:75-82.
55. Viterbi A. Error bounds for convolutional codes and an asymptotically optimum decoding algorithm. IEEE Trans. Inf. Theory 1967, 13:260-269.
56. Wakano C., Byun J.S., Di L.-J., Gardner K. The dual lives of bidirectional promoters. Biochim. Biophys. Acta 2012, 1819:688-693.
57. Wickham H. ggplot2: Elegant Graphics for Data Analysis 2009, Springer, New York.