lncRNA recruits RNAi and the exosome to dynamically regulate pho1 expression in response to phosphate levels in fission yeast

Genes and Development

Volumn 28, Issue 3, 2014, Pages 231-244

  Shah, Sneha ^a   Wittmann, Sina ^a   Kilchert, Cornelia ^a   Vasiljeva, Lidia ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Exosome; H3K9me; Noncoding RNA; RNAi; Transcription termination; Transient heterochromatin

Indexed keywords

MESSENGER RNA; PHOSPHATASE; PHOSPHATE; RNA BINDING PROTEIN; UNTRANSLATED RNA;

ARTICLE; CHROMATIN; EXOSOME; GENE; GENE LOCUS; HETEROCHROMATIN; HUMAN; HUMAN CELL; METHYLATION; MITOSIS; PHO1 REPRESSING TRANSCRIPT GENE; PRIORITY JOURNAL; RNA INTERFERENCE; SCHIZOSACCHAROMYCES; TRANSCRIPTION TERMINATION;

EXOSOME; H3K9ME; NONCODING RNA; RNAI; TRANSCRIPTION TERMINATION; TRANSIENT HETEROCHROMATIN;

ACID PHOSPHATASE; EXOSOMES; GENE EXPRESSION REGULATION, FUNGAL; HISTONES; METHYLATION; PHOSPHATES; RNA INTERFERENCE; RNA, LONG NONCODING; SCHIZOSACCHAROMYCES;

EID: 84893432469     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.230177.113     Document Type: Article

References (65)

1. Arigo JT, Eyler DE, Carroll KL, Corden JL. 2006. Termination of cryptic unstable transcripts is directed by yeast RNA-binding proteins Nrd1 and Nab3. Mol Cell 23: 841-851.
2. Birse CE, Lee BA, Hansen K, Proudfoot NJ. 1997. Transcriptional termination signals for RNA polymerase II in fission yeast. EMBO J 16: 3633-3643.
3. Birse CE, Minvielle-Sebastia L, Lee BA, Keller W, Proudfoot NJ. 1998. Coupling termination of transcription to messenger RNA maturation in yeast. Science 280: 298-301.
4. Buhler M, Moazed D. 2007. Transcription and RNAi in heterochromatic gene silencing. Nat Struct Mol Biol 14: 1041-1048.
5. Buhler M, Verdel A, Moazed D. 2006. Tethering RITS to a nascent transcript initiates RNAi-and heterochromatindependent gene silencing. Cell 125: 873-886.
6. Cam HP, Chen ES, Grewal SIS. 2009. Transcriptional scaffolds for heterochromatin assembly. Cell 136: 610-614.
7. 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.
8. Carter-O'Connell I, Peel MT, Wykoff DD, O'Shea EK. 2012. Genome-wide characterization of the phosphate starvation response in Schizosaccharomyces pombe. BMC Genomics 13: 697.
9. 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.
10. Ciais D, Bohnsack MT, Tollervey D. 2008. The mRNA encoding the yeast ARE-binding protein Cth2 is generated by a novel 39processing pathway. Nucleic Acids Res 36: 3075-3084.
11. Colmenares SU, Buker SM, Buhler M, Dlakic M, Moazed D. 2007. Coupling of double-stranded RNA synthesis and siRNA generation in fission yeast RNAi. Mol Cell 27: 449-461.
12. Coy S, Vasiljeva L. 2010. The exosome and heterochromatin: Multilevel regulation of gene silencing. Adv Exp Med Biol 702: 105-121.
13. Creamer TJ, Darby MM, Jamonnak N, Schaughency P, Hao H, Wheelan SJ, Corden JL. 2011. Transcriptome-wide binding sites for components of the Saccharomyces cerevisiae nonpoly(A) termination pathway: Nrd1, Nab3, and Sen1. PLoS Genet 7: e1002329.
14. Djupedal I, Portoso M, Spahr H, Bonilla C, Gustafsson CM, Allshire RC, Ekwall K. 2005. RNA Pol II subunit Rpb7 promotes centromeric transcription and RNAi-directed chromatin silencing. Genes Dev 19: 2301-2306.
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. Gerace EL, Halic M, Moazed D. 2010. The methyltransferase activity of Clr4Suv39h triggers RNAi independently of histone H3K9 methylation. Mol Cell 39: 360-372.
18. Greger IH, Aranda A, Proudfoot N. 2000. Balancing transcriptional interference and initiation on the GAL7 promoter of Saccharomyces cerevisiae. Proc Natl Acad Sci 97: 8415-8420.
19. Gudipati RK, Villa T, Boulay J, Libri D. 2008. Phosphorylation of the RNA polymerase II C-terminal domain dictates transcription termination choice. Nat Struct Mol Biol 15: 786-794.
20. Gudipati RK, Xu Z, Lebreton A, Seraphin B, Steinmetz LM, Jacquier A, Libri D. 2012. Extensive degradation of RNA precursors by the exosome in wild-type cells. Mol Cell 48: 409-421.
21. Gullerova M, Proudfoot NJ. 2008. Cohesin complex promotes transcriptional termination between convergent genes in S. pombe. Cell 132: 983-995.
22. Gullerova M, Proudfoot NJ. 2010. Transcriptional interference and gene orientation in yeast: Noncoding RNA connections. Cold Spring Harb Symp Quant Biol 75: 299-311.
23. Hainer SJ, Pruneski JA, Mitchell RD, Monteverde RM, Martens JA. 2011. Intergenic transcription causes repression by directing nucleosome assembly. Genes Dev 25: 29-40.
24. Harigaya Y, Tanaka H, Yamanaka S, Tanaka K, Watanabe Y, Tsutsumi C, Chikashige Y, Hiraoka Y, Yamashita A, Yamamoto M. 2006. Selective elimination of messenger RNA prevents an incidence of untimely meiosis. Nature 442: 45-50.
25. Henry TC, Power JE, Kerwin CL, Mohammed A, Weissman JS, Cameron DM, Wykoff DD. 2011. Systematic screen of Schizosaccharomyces pombe deletion collection uncovers parallel evolution of the phosphate signal transduction pathway in yeasts. Eukaryot Cell 10: 198-206.
26. Hiriart E, Vavasseur A, Touat-Todeschini L, Yamashita A, Gilquin B, Lambert E, Perot J, Shichino Y, Nazaret N, Boyault C, et al. 2012. Mmi1 RNA surveillance machinery directs RNAi complex RITS to specific meiotic genes in fission yeast. EMBO J 31: 2296-2308.
27. Hong EJ, Villen J, Gerace EL, Gygi SP, Moazed D. 2005. A cullin E3 ubiquitin ligase complex associates with Rik1 and the Clr4 histone H3-K9 methyltransferase and is required for RNAi-mediated heterochromatin formation. RNA Biol 2: 106-111.
28. 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.
29. Iida T, Nakayama J, Moazed D. 2008. siRNA-mediated heterochromatin establishment requires HP1 and is associated with antisense transcription. Mol Cell 31: 178-189.
30. Kato H, Goto DB, Martienssen RA, Urano T, Furukawa K, Murakami Y. 2005. RNA polymerase II is required for RNAi-dependent heterochromatin assembly. Science 309: 467-469.
31. Keogh MC, Buratowski S. 2004. Using chromatin immunoprecipitation to map cotranscriptional mRNA processing in Saccharomyces cerevisiae. Methods Mol Biol 257: 1-16.
32. Kim M, Ahn SH, Krogan NJ, Greenblatt JF, Buratowski S. 2004a. Transitions in RNA polymerase II elongation complexes at the 39 ends of genes. EMBO J 23: 354-364.
33. Kim M, Krogan NJ, Vasiljeva L, Rando OJ, Nedea E, Greenblatt JF, Buratowski S. 2004b. The yeast Rat1 exonuclease promotes transcription termination by RNA polymerase II. Nature 432: 517-522.
34. Kim M, Vasiljeva L, Rando OJ, Zhelkovsky A, Moore C, Buratowski S. 2006. Distinct pathways for snoRNA and mRNA termination. Mol Cell 24: 723-734.
35. Kim T, Xu Z, Clauder-Munster S, Steinmetz LM, Buratowski S. 2012. Set3 HDAC mediates effects of overlapping noncoding transcription on gene induction kinetics. Cell 150: 1158-1169.
36. Lee NN, Chalamcharla VR, Reyes-Turcu F, Mehta S, Zofall M, Balachandran V, Dhakshnamoorthy J, Taneja N, Yamanaka S, Zhou M, et al. 2013. Mtr4-like protein coordinates nuclear RNA processing for heterochromatin assembly and for telomere maintenance. Cell 155: 1061-1074.
37. Luo W, Johnson AW, Bentley DL. 2006. The role of Rat1 in coupling mRNA 39-end processing to transcription termination: Implications for a unified allosteric-torpedo model. Genes Dev 20: 954-965.
38. Marina DB, Shankar S, Natarajan P, Finn KJ, Madhani HD. 2013. A conserved ncRNA-binding protein recruits silencing factors to heterochromatin through an RNAi-independent mechanism. Genes Dev 27: 1851-1856.
39. Martens JA, Laprade L, Winston F. 2004. Intergenic transcription is required to repress the Saccharomyces cerevisiae SER3 gene. Nature 429: 571-574.
40. Noma K, Sugiyama T, Cam H, Verdel A, Zofall M, Jia S, Moazed D, Grewal SI. 2004. RITS acts in cis to promote RNA interference-mediated transcriptional and post-transcriptional silencing. Nat Genet 36: 1174-1180.
41. Pinskaya M, Gourvennec S, Morillon A. 2009. H3 lysine 4 diand tri-methylation deposited by cryptic transcription attenuates promoter activation. EMBO J 28: 1697-1707.
42. Reinheckel T, Peters C, Kruger A, Turk B, Vasiljeva O. 2012. Differential impact of cysteine cathepsins on genetic mouse models of de novo carcinogenesis: Cathepsin B as emerging therapeutic target. Front Pharmacol 3: 133.
43. Roguev A, Shevchenko A, Schaft D, Thomas H, Stewart AF. 2004. A comparative analysis of an orthologous proteomic environment in the yeasts Saccharomyces cerevisiae and Schizosaccharomyces pombe. Mol Cell Proteomics 3: 125-132.
44. Rondón AG, Mischo HE, Kawauchi J, Proudfoot NJ. 2009. Failsafe transcriptional termination for protein-coding genes in S. cerevisiae. Mol Cell 36: 88-98.
45. Rougemaille M, Libri D. 2010. Control of cryptic transcription in eukaryotes. Adv Exp Med Biol 702: 122-131.
46. Schweingruber ME, Fluri R, Maundrell K, Schweingruber AM, Dumermuth E. 1986. Identification and characterization of thiamin repressible acid phosphatase in yeast. J Biol Chem 261: 15877-15882.
47. + gene, encoding a putative nuclear 59 / 39 exoribonuclease, is required for proper chromosome segregation in fission yeast. Nucleic Acids Res 29: 1326-1333.
48. Sugiyama T, Sugioka-Sugiyama R. 2011. Red1 promotes the elimination of meiosis-specific mRNAs in vegetatively growing fission yeast. EMBO J 30: 1027-1039.
49. Tashiro S, Asano T, Kanoh J, Ishikawa F. 2013. Transcriptioninduced chromatin association of RNA surveillance factors mediates facultative heterochromatin formation in fission yeast. Genes Cells 18: 327-339.
50. Thiebaut M, Kisseleva-Romanova E, Rougemaille M, Boulay J, Libri D. 2006. Transcription termination and nuclear degradation of cryptic unstable transcripts: A role for the nrd1-nab3 pathway in genome surveillance. Mol Cell 23: 853-864.
51. Tittel-Elmer M, Bucher E, Broger L, Mathieu O, Paszkowski J, Vaillant I. 2010. Stress-induced activation of heterochromatic transcription. PLoS Genet 6: e1001175.
52. Tuck AC, Tollervey D. 2013. A transcriptome-wide atlas of RNP composition reveals diverse classes of mRNAs and lncRNAs. Cell 154: 996-1009.
53. Vasiljeva L, Buratowski S. 2006. Nrd1 interacts with the nuclear exosome for 39 processing of RNA polymerase II transcripts. Mol Cell 21: 239-248.
54. Vasiljeva L, Kim M, Mutschler H, Buratowski S, Meinhart A. 2008a. The Nrd1-Nab3-Sen1 termination complex interacts with the Ser5-phosphorylated RNA polymerase II C-terminal domain. Nat Struct Mol Biol 15: 795-804.
55. Vasiljeva L, Kim M, Terzi N, Soares LM, Buratowski S. 2008b. Transcription termination and RNA degradation contribute to silencing of RNA polymerase II transcription within heterochromatin. Mol Cell 29: 313-323.
56. Verdel A, Jia S, Gerber S, Sugiyama T, Gygi S, Grewal SI, Moazed D. 2004. RNAi-mediated targeting of heterochromatin by the RITS complex. Science 303: 672-676.
57. Wang SW, Asakawa K, Win TZ, Toda T, Norbury CJ. 2005. Inactivation of the pre-mRNA cleavage and polyadenylation factor Pfs2 in fission yeast causes lethal cell cycle defects. Mol Cell Biol 25: 2288-2296.
58. Weiner A, Chen HV, Liu CL, Rahat A, Klien A, Soares L, Gudipati M, Pfeffner J, Regev A, Buratowski S, et al. 2012. Systematic dissection of roles for chromatin regulators in a yeast stress response. PLoS Biol 10: e1001369.
59. West S, Gromak N, Proudfoot NJ. 2004. Human 59 / 39 exonuclease Xrn2 promotes transcription termination at co-transcriptional cleavage sites. Nature 432: 522-525.
60. Wilhelm BT, Marguerat S, Watt S, Schubert F, Wood V, Goodhead I, Penkett CJ, Rogers J, Bahler J. 2008. Dynamic repertoire of a eukaryotic transcriptome surveyed at singlenucleotide resolution. Nature 453: 1239-1243.
61. Woolcock KJ, Stunnenberg R, Gaidatzis D, Hotz HR, Emmerth S, Barraud P, Buhler M. 2012. RNAi keeps Atf1-bound stress response genes in check at nuclear pores. Genes Dev 26: 683-692.
62. Xiang S, Cooper-Morgan A, Jiao X, Kiledjian M, Manley JL, Tong L. 2009. Structure and function of the 59 / 39 exoribonuclease Rat1 and its activating partner Rai1. Nature 458: 784-788.
63. Yamamoto M. 2010. The selective elimination of messenger RNA underlies the mitosis-meiosis switch in fission yeast. Proc Jpn Acad, Ser B, Phys Biol Sci 86: 788-797.
64. Yamanaka S, Mehta S, Reyes-Turcu FE, Zhuang F, Fuchs RT, Rong Y, Robb GB, Grewal SIS. 2013. RNAi triggered by specialized machinery silences developmental genes and retrotransposons. Nature 493: 557-560.
65. Zofall M, Yamanaka S, Reyes-Turcu FE, Zhang K, Rubin C, Grewal SIS. 2012. RNA elimination machinery targeting meiotic mRNAs promotes facultative heterochromatin formation. Science 335: 96-100.