ATP-dependent chromatin remodeling shapes the long noncoding RNA landscape

Genes and Development

Volumn 28, Issue 21, 2014, Pages 2348-2360

  Alcid, Eric A ^a   Tsukiyama, Toshio ^a  

^a Fred Hutchinson Cancer Research Center   (United States)

Author keywords

Antisense RNAs; Chromatin; Chromatin remodeling; LncRNAs

Indexed keywords

COMPLEMENTARY RNA; LONG UNTRANSLATED RNA; TRANSCRIPTOME; ADENOSINE TRIPHOSPHATE;

ARTICLE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN STRUCTURE; CONTROLLED STUDY; GENE INTERACTION; GENE MUTATION; NONHUMAN; REPRESSOR GENE; RNA INTERFERENCE; RNA TRANSCRIPTION; SACCHAROMYCES CEREVISIAE; CHEMISTRY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MUTATION; PHYSIOLOGY;

ADENOSINE TRIPHOSPHATE; CHROMATIN ASSEMBLY AND DISASSEMBLY; GENE EXPRESSION REGULATION, FUNGAL; MUTATION; RNA INTERFERENCE; RNA, LONG NONCODING; SACCHAROMYCES CEREVISIAE; TRANSCRIPTOME;

EID: 84908395055     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.250902.114     Document Type: Article

References (56)

1. Albert I, Mavrich TN, Tomsho LP, Qi J, Zanton SJ, Schuster SC, Pugh BF. 2007. Translational and rotational settings of H2A.Z nucleosomes across the Saccharomyces cerevisiae genome. Nature 446: 572–576.
2. Anders S, Huber W. 2010. Differential expression analysis for sequence count data. Genome Biol 11: R106.
3. Anders S, Pyl PT, Huber W. 2014. HTSeq-A Python framework to work with high-throughput sequencing data. bioRxiv.
4. Batista PJ, Chang HY. 2013. Long noncoding RNAs: cellular address codes in development and disease. Cell 152: 1298–1307.
5. Camblong J, Iglesias N, Fickentscher C, Dieppois G, Stutz F. 2007. Antisense RNA stabilization induces transcriptional gene silencing via histone deacetylation in S. cerevisiae. Cell 131: 706–717.
6. Camblong J, Beyrouthy N, Guffanti E, Schlaepfer G, Steinmetz LM, Stutz F. 2009. Trans-acting antisense RNAs mediate transcriptional gene cosuppression in S. cerevisiae. Genes Dev 23: 1534–1545.
7. Carrozza MJ, Li B, Florens L, Suganuma T, Swanson SK, Lee KK, Shia WJ, Anderson S, Yates J, Washburn MP, et al. 2005. Histone H3 methylation by Set2 directs deacetylation of coding regions by Rpd3S to suppress spurious intragenic transcription. Cell 123: 581–592.
8. Castelnuovo M, Rahman S, Guffanti E, Infantino V, Stutz F, Zenklusen D. 2013. Bimodal expression of PHO84 is modulated by early termination of antisense transcription. Nat Struct Mol Biol 20: 851–858.
9. Cheung V, Chua G, Batada NN, Landry CR, Michnick SW, Hughes TR, Winston F. 2008. Chromatin- and transcriptionrelated factors repress transcription fromwithin coding regions throughout the Saccharomyces cerevisiae genome. PLoS Biol 6: e277.
10. Churchman LS, Weissman JS. 2011. Nascent transcript sequencing visualizes transcription at nucleotide resolution. Nature 469: 368–373.
11. Core LJ, Waterfall J, Lis J. 2008. Nascent RNA sequencing reveals widespread pausing and divergent initiation at human promoters. Science 322: 1845–1848.
12. Davis CA, Ares M Jr. 2006. Accumulation of unstable promoterassociated transcripts upon loss of the nuclear exosome subunit Rrp6p in Saccharomyces cerevisiae. Proc Natl Acad Sci 103: 3262–3267.
13. Djebali S, Davis CA, Merkel A, Dobin A, Lassmann T, Mortazavi A, Tanzer A, Lagarde J, Lin W, Schlesinger F, et al. 2012. Landscape of transcription in human cells. Nature 489: 101–108.
14. Doolittle WF. 2013. Is junk DNA bunk? A critique of ENCODE. Proc Natl Acad Sci 110: 5294–5300.
15. Drinnenberg IA, Weinberg DE, Xie KT, Mower JP, Wolfe KH, Fink GR, Bartel DP. 2009. RNAi in budding yeast. Science 326: 544–550.
16. Drinnenberg IA, Fink GR, Bartel DP. 2011. Compatibility with killer explains the rise of RNAi-deficient fungi. Science 333: 1592.
17. Eden E, Navon R, Steinfeld I, Lipson D, Yakhini Z. 2009. GOrilla: a tool for discovery and visualization of enriched GO terms in ranked gene lists. BMC Bioinformatics 10: 48.
18. Flicek P, Amode MR, Barrell D, Beal K, Billis K, Brent S, Carvalho-Silva D, Clapham P, Coates G, Fitzgerald S, et al. 2014. Ensembl 2014. Nucleic Acids Res 42: D749–D755.
19. Floer M, Wang X, Prabhu V, Berrozpe G, Narayan S, Spagna D, Alvarez D, Kendall J, Krasnitz A, Stepansky A, et al. 2010. A RSC/nucleosome complex determines chromatin architecture and facilitates activator binding. Cell 141: 407–418.
20. Flynn RA, Chang HY. 2014. Long noncoding RNAs in cell-fate programming and reprogramming. Cell Stem Cell 14: 752–761.
21. Goldstein G, McCusker J. 1999. Three new dominant drug resistance cassettes for gene disruption in Saccharomyces cerevisiae. Yeast 15: 1541–1553.
22. Gupta RA, Shah N, Wang KC, Kim J, Horlings HM, Wong DJ, Tsai MC, Hung T, Argani P, Rinn JL, et al. 2010. Long noncoding RNA HOTAIR reprograms chromatin state to promote cancer metastasis. Nature 464: 1071–1076.
23. Hartley PD, Madhani HD. 2009. Mechanisms that specify promoter nucleosome location and identity. Cell 137: 445–458.
24. Hongay CF, Grisafi PL, Galitski T, Fink GR. 2006. Antisense transcription controls cell fate in Saccharomyces cerevisiae. Cell 127: 735–745.
25. Houseley J, Rubbi L, Grunstein M, Tollervey D, Vogelauer M. 2008. A ncRNA modulates histone modification and mRNA induction in the yeast GAL gene cluster. Mol Cell 32: 685–695.
26. Kellis M, Wold B, Snyder M., Bernstein BE, Kundaje A, Marinov GK, Ward LD, Birney E, Crawford GE, Dekker J, et al 2014. Defining functional DNA elements in the human genome. Proc Natl Acad Sci 111: 6131–6138.
27. Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL. 2013. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol 14: R36.
28. Kobor MS, Venkatasubrahmanyam S, Meneghini MD, Gin JW, Jennings JL, Link AJ, Madhani HD, Rine J. 2004. A protein complex containing the conserved Swi2/Snf2-related ATPase Swr1p deposits histone variant H2A.Z into euchromatin. PLoS Biol 2: E131.
29. Lee JT, Bartolomei MS. 2013. X-inactivation, imprinting, and long noncoding RNAs in health and disease. Cell 152: 1308–1323.
30. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R. 2009. The sequence alignment/map format and SAMtools. Bioinformatics 25: 2078–2079.
31. Lickwar CR, Rao B, Shabalin AA, Nobel AB, Strahl BD, Lieb JD. 2009. The Set2/Rpd3S pathway suppresses cryptic transcription without regard to gene length or transcription frequency. PLoS ONE 4: e4886.
32. Louro R, Smirnova AS, Verjovski-Almeida S. 2009. Long intronic noncoding RNA transcription: expression noise or expression choice? Genomics 93: 291–298.
33. Marquardt S, Escalante-Chong R, Pho N, Wang J, Churchman LS, Springer M, Buratowski S. 2014. A chromatin-based mechanism for limiting divergent noncoding transcription. Cell 157: 1712–1723.
34. Nagalakshmi U, Wang Z, Waern K, Shou C, Raha D, Gerstein M, Snyder M. 2008. The transcriptional landscape of the yeast genome defined by RNA sequencing. Science 320: 1344–1349.
35. Neil H, Malabat C, d’Aubenton-Carafa Y, Xu Z, Steinmetz LM, Jacquier A. 2009. Widespread bidirectional promoters are the major source of cryptic transcripts in yeast. Nature 457: 1038–1042.
36. Papamichos-Chronakis M, Watanabe S, Rando OJ, Peterson CL. 2011. Global regulation of H2A.Z localization by the INO80 chromatin-remodeling enzyme is essential for genome integrity. Cell 144: 200–213.
37. Parkhomchuk D, Borodina T, Amstislavskiy V, Banaru M, Hallen L, Krobitsch S, Lehrach H, Soldatov A. 2009. Transcriptome analysis by strand-specific sequencing of complementary DNA. Nucleic Acids Res 37: e123.
38. Quinlan AR, Hall IM. 2010. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26: 841–842.
39. Rhee HS, Pugh BF. 2012. Genome-wide structure and organization of eukaryotic pre-initiation complexes. Nature 483: 295–301.
40. Rinn JL, Kertesz M, Wang JK, Squazzo SL, Xu X, Brugmann SA, Goodnough LH, Helms JA, Farnham PJ, Segal E, et al. 2007. Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs. Cell 129: 1311–1323.
41. Schulz D, Schwalb B, Kiesel A, Baejen C, Torkler P, Gagneur J, Soeding J, Cramer P. 2013. Transcriptome surveillance by selective termination of noncoding RNA synthesis. Cell 155: 1075–1087.
42. Sultan M, Dokel S, Amstislavskiy V, Wuttig D, Sultmann H, Lehrach H, Yaspo ML. 2012. A simple strand-specific RNAseq library preparation protocol combining the Illumina TruSeq RNA and the dUTP methods. Biochem Biophys Res Commun 422: 643–646.
43. Teif VB, Vainshtein Y, Caudron-Herger M, Mallm JP, Marth C, Hofer T, Rippe K. 2012. Genome-wide nucleosome positioning during embryonic stem cell development. Nat Struct Mol Biol 19: 1185–1192.
44. Tong AH, Evangelista M, Parsons AB, Xu H, Bader GD, Page N, Robinson M, Raghibizadeh S, Hogue CW, Bussey H, et al. 2001. Systematic genetic analysis with ordered arrays of yeast deletion mutants. Science 294: 2364–2368.
45. Tsai MC, Manor O, Wan Y, Mosammaparast N, Wang JK, Lan F, Shi Y, Segal E, Chang HY. 2010. Long noncoding RNA as modular scaffold of histone modification complexes. Science 329: 689–693.
46. Van de Vosse DW, Wan Y, Lapetina DL, Chen WM, Chiang JH, Aitchison JD, Wozniak RW. 2013. A role for the nucleoporin Nup170p in chromatin structure and gene silencing. Cell 152: 969–983.
47. van Dijk EL, Chen CL, d’Aubenton-Carafa Y, Gourvennec S, Kwapisz M, Roche V, Bertrand C, Silvain M, Legoix-Ne P, Loeillet S, et al. 2011. XUTs are a class of Xrn1-sensitive antisense regulatory non-coding RNA in yeast. Nature 475: 114–117.
48. Venter JC, Adams MD, Myers EW, Li PW, Mural RJ, Sutton GG, Smith HO, Yandell M, Evans CA, Holt RA, et al. 2001. The sequence of the human genome. Science 291: 1304–1351.
49. Venters BJ, Pugh BF. 2013. Genomic organization of human transcription initiation complexes. Nature 502: 53–58.
50. Whitehouse I, Rando OJ, Delrow J, Tsukiyama T. 2007. Chromatin remodelling at promoters suppresses antisense transcription. Nature 450: 1031–1035.
51. Wyers F, Rougemaille M, Badis G, Rousselle J-C, Dufour M-E, Boulay J, Régnault B, Devaux F, Namane A, Séraphin B. 2005. Cryptic Pol II transcripts are degraded by a nuclear quality control pathway involving a new poly(A) polymerase. Cell 121: 725–737.
52. Xu Z, Wei W, Gagneur J, Perocchi F, Clauder-Munster S, Camblong J, Guffanti E, Stutz F, Huber W, Steinmetz LM. 2009. Bidirectional promoters generate pervasive transcription in yeast. Nature 457: 1033–1037.
53. Yadon AN, Van de Mark D, Basom R, Delrow J, Whitehouse I, Tsukiyama T. 2010. Chromatin remodeling around nucleosome- free regions leads to repression of noncoding RNA transcription. Mol Cell Biol 30: 5110–5122.
54. Yen K, Vinayachandran V, Batta K, Koerber RT, Pugh BF. 2012. Genome-wide nucleosome specificity and directionality of chromatin remodelers. Cell 149: 1461–1473.
55. Yen K, Vinayachandran V, Pugh BF. 2013. SWR-C and INO80 chromatin remodelers recognize nucleosome-free regions near +1 nucleosomes. Cell 154: 1246–1256.
56. Zofall M, Fischer T, Zhang K, Zhou M, Cui B, Veenstra TD, Grewal SI. 2009. Histone H2A.Z cooperates with RNAi and heterochromatin factors to suppress antisense RNAs. Nature 461: 419–422.