Meiotic gene silencing complex MTREC/NURS recruits the nuclear exosome to YTH-RNA-binding protein Mmi1
Autoři:
Yuichi Shichino aff001; Yoko Otsubo aff001; Masayuki Yamamoto aff001; Akira Yamashita aff001
Působiště autorů:
Laboratory of Cell Responses, National Institute for Basic Biology, Nishigonaka, Myodaiji, Okazaki, Aichi, Japan
aff001; Laboratory of Cell Responses, National Institute for Basic Biology, Myodaiji, Okazaki, Aichi, Japan
aff001; National Institute for Fusion Science,Oroshi, Toki, Gifu, Japan
aff002; National Institute for Fusion Science, Toki, Gifu, Japan
aff002; Center for Novel Science Initiatives, National Institutes of Natural Sciences, Nishigonaka, Myodaiji, Okazaki, Aichi, Japan
aff003; Center for Novel Science Initiatives, National Institutes of Natural Sciences, Myodaiji, Okazaki, Aichi, Japan
aff003; Department of Basic Biology, School of Life Science, SOKENDAI (The Graduate University for Advanced Studies), Nishigonaka, Myodaiji, Okazaki, Aichi, Japan
aff004; Department of Basic Biology, School of Life Science, SOKENDAI (The Graduate University for Advanced Studies), Myodaiji, Okazaki, Aichi, Japan
aff004
Vyšlo v časopise:
Meiotic gene silencing complex MTREC/NURS recruits the nuclear exosome to YTH-RNA-binding protein Mmi1. PLoS Genet 16(2): e32767. doi:10.1371/journal.pgen.1008598
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pgen.1008598
Souhrn
Accurate target recognition in transcript degradation is crucial for regulation of gene expression. In the fission yeast Schizosaccharomyces pombe, a number of meiotic transcripts are recognized by a YTH-family RNA-binding protein, Mmi1, and selectively degraded by the nuclear exosome during mitotic growth. Mmi1 forms nuclear foci in mitotically growing cells, and the nuclear exosome colocalizes to such foci. However, it remains elusive how Mmi1 and the nuclear exosome are connected. Here, we show that a complex called MTREC (Mtl1-Red1 core) or NURS (nuclear RNA silencing) that consists of a zinc-finger protein, Red1, and an RNA helicase, Mtl1, is required for the recruitment of the nuclear exosome to Mmi1 foci. Physical interaction between Mmi1 and the nuclear exosome depends on Red1. Furthermore, a chimeric protein involving Mmi1 and Rrp6, which is a nuclear-specific component of the exosome, suppresses the ectopic expression phenotype of meiotic transcripts in red1Δ cells and mtl1 mutant cells. These data indicate that the primary function of MTREC/NURS in meiotic transcript elimination is to link Mmi1 to the nuclear exosome physically.
Klíčová slova:
Co-immunoprecipitation – Exosomes – Gene expression – Immunoprecipitation – Messenger RNA – Plasmid construction – Schizosaccharomyces pombe – Yellow fluorescent protein
Zdroje
1. Bresson S, Tollervey D. Surveillance-ready transcription: nuclear RNA decay as a default fate. Open biology. 2018;8(3): 170270. doi: 10.1098/rsob.170270 29563193
2. Schmid M, Jensen TH. Controlling nuclear RNA levels. Nature reviews Genetics. 2018;19(8):518–29. doi: 10.1038/s41576-018-0013-2 29748575
3. Harigaya Y, Tanaka H, Yamanaka S, Tanaka K, Watanabe Y, Tsutsumi C, et al. Selective elimination of messenger RNA prevents an incidence of untimely meiosis. Nature. 2006;442(7098):45–50. doi: 10.1038/nature04881 16823445
4. Folco HD, Chalamcharla VR, Sugiyama T, Thillainadesan G, Zofall M, Balachandran V, et al. Untimely expression of gametogenic genes in vegetative cells causes uniparental disomy. Nature. 2017;543(7643):126–30. doi: 10.1038/nature21372 28199302
5. Hiriart E, Vavasseur A, Touat-Todeschini L, Yamashita A, Gilquin B, Lambert E, et al. Mmi1 RNA surveillance machinery directs RNAi complex RITS to specific meiotic genes in fission yeast. EMBO J. 2012;31(10):2296–308. doi: 10.1038/emboj.2012.105 22522705
6. Yamashita A, Shichino Y, Tanaka H, Hiriart E, Touat-Todeschini L, Vavasseur A, et al. Hexanucleotide motifs mediate recruitment of the RNA elimination machinery to silent meiotic genes. Open biology. 2012;2(3):120014. doi: 10.1098/rsob.120014 22645662
7. Kilchert C, Wittmann S, Passoni M, Shah S, Granneman S, Vasiljeva L. Regulation of mRNA Levels by Decay-Promoting Introns that Recruit the Exosome Specificity Factor Mmi1. Cell reports. 2015;13(11):2504–15. doi: 10.1016/j.celrep.2015.11.026 26670050
8. Chatterjee D, Sanchez AM, Goldgur Y, Shuman S, Schwer B. Transcription of lncRNA prt, clustered prt RNA sites for Mmi1 binding, and RNA polymerase II CTD phospho-sites govern the repression of pho1 gene expression under phosphate-replete conditions in fission yeast. RNA. 2016;22(7):1011–25. doi: 10.1261/rna.056515.116 27165520
9. Wang C, Zhu Y, Bao H, Jiang Y, Xu C, Wu J, et al. A novel RNA-binding mode of the YTH domain reveals the mechanism for recognition of determinant of selective removal by Mmi1. Nucleic Acids Res. 2016;44(2):969–82. doi: 10.1093/nar/gkv1382 26673708
10. Wu B, Xu J, Su S, Liu H, Gan J, Ma J. Structural insights into the specific recognition of DSR by the YTH domain containing protein Mmi1. Biochemical and biophysical research communications. 2017;491(2):310–6. doi: 10.1016/j.bbrc.2017.07.104 28735863
11. Hazra D, Chapat C, Graille M. m(6)A mRNA Destiny: Chained to the rhYTHm by the YTH-Containing Proteins. Genes. 2019;10(1):E49. doi: 10.3390/genes10010049 30650668
12. Yamanaka S, Yamashita A, Harigaya Y, Iwata R, Yamamoto M. Importance of polyadenylation in the selective elimination of meiotic mRNAs in growing S. pombe cells. EMBO J. 2010;29(13):2173–81. doi: 10.1038/emboj.2010.108 20512112
13. Ogami K, Chen Y, Manley JL. RNA surveillance by the nuclear RNA exosome: mechanisms and significance. Non-coding RNA. 2018;4(1). doi: 10.3390/ncrna4010008 29629374
14. Zinder JC, Lima CD. Targeting RNA for processing or destruction by the eukaryotic RNA exosome and its cofactors. Genes & development. 2017;31(2):88–100. doi: 10.1101/gad.294769.116 28202538
15. Kilchert C, Wittmann S, Vasiljeva L. The regulation and functions of the nuclear RNA exosome complex. Nat Rev Mol Cell Biol. 2016;17(4):227–39. doi: 10.1038/nrm.2015.15 26726035
16. Chekanova JA, Gregory BD, Reverdatto SV, Chen H, Kumar R, Hooker T, et al. Genome-wide high-resolution mapping of exosome substrates reveals hidden features in the Arabidopsis transcriptome. Cell. 2007;131(7):1340–53. doi: 10.1016/j.cell.2007.10.056 18160042
17. Gudipati RK, Xu Z, Lebreton A, Seraphin B, Steinmetz LM, Jacquier A, et al. Extensive degradation of RNA precursors by the exosome in wild-type cells. Mol Cell. 2012;48(3):409–21. doi: 10.1016/j.molcel.2012.08.018 23000176
18. Schneider C, Kudla G, Wlotzka W, Tuck A, Tollervey D. Transcriptome-wide analysis of exosome targets. Mol Cell. 2012;48(3):422–33. doi: 10.1016/j.molcel.2012.08.013 23000172
19. Chen HM, Futcher B, Leatherwood J. The fission yeast RNA binding protein Mmi1 regulates meiotic genes by controlling intron specific splicing and polyadenylation coupled RNA turnover. PloS one. 2011;6(10):e26804. doi: 10.1371/journal.pone.0026804 22046364
20. St-Andre O, Lemieux C, Perreault A, Lackner DH, Bahler J, Bachand F. Negative regulation of meiotic gene expression by the nuclear poly(a)-binding protein in fission yeast. J Biol Chem. 2010;285(36):27859–68. doi: 10.1074/jbc.M110.150748 20622014
21. Sugiyama T, Sugioka-Sugiyama R. Red1 promotes the elimination of meiosis-specific mRNAs in vegetatively growing fission yeast. EMBO J. 2011;30(6):1027–39. doi: 10.1038/emboj.2011.32 21317872
22. Yamashita A, Takayama T, Iwata R, Yamamoto M. A novel factor Iss10 regulates Mmi1-mediated selective elimination of meiotic transcripts. Nucleic Acids Res. 2013;41(21):9680–7. doi: 10.1093/nar/gkt763 23980030
23. Lee NN, Chalamcharla VR, Reyes-Turcu F, Mehta S, Zofall M, Balachandran V, et al. Mtr4-like protein coordinates nuclear RNA processing for heterochromatin assembly and for telomere maintenance. Cell. 2013;155(5):1061–74. doi: 10.1016/j.cell.2013.10.027 24210919
24. Egan ED, Braun CR, Gygi SP, Moazed D. Post-transcriptional regulation of meiotic genes by a nuclear RNA silencing complex. RNA. 2014;20(6):867–81. doi: 10.1261/rna.044479.114 24713849
25. Zhou Y, Zhu J, Schermann G, Ohle C, Bendrin K, Sugioka-Sugiyama R, et al. The fission yeast MTREC complex targets CUTs and unspliced pre-mRNAs to the nuclear exosome. Nature communications. 2015;6:7050. doi: 10.1038/ncomms8050 25989903
26. Tashiro S, Asano T, Kanoh J, Ishikawa F. Transcription-induced chromatin association of RNA surveillance factors mediates facultative heterochromatin formation in fission yeast. Genes Cells. 2013;18(4):327–39. doi: 10.1111/gtc.12038 23388053
27. Zofall M, Yamanaka S, Reyes-Turcu FE, Zhang K, Rubin C, Grewal SI. RNA elimination machinery targeting meiotic mRNAs promotes facultative heterochromatin formation. Science. 2012;335(6064):96–100. doi: 10.1126/science.1211651 22144463
28. Chalamcharla VR, Folco HD, Dhakshnamoorthy J, Grewal SI. Conserved factor Dhp1/Rat1/Xrn2 triggers premature transcription termination and nucleates heterochromatin to promote gene silencing. Proc Natl Acad Sci U S A. 2015;112(51):15548–55. doi: 10.1073/pnas.1522127112 26631744
29. Shah S, Wittmann S, Kilchert C, Vasiljeva L. lncRNA recruits RNAi and the exosome to dynamically regulate pho1 expression in response to phosphate levels in fission yeast. Genes & development. 2014;28(3):231–44. doi: 10.1101/gad.230177.113 24493644
30. Touat-Todeschini L, Shichino Y, Dangin M, Thierry-Mieg N, Gilquin B, Hiriart E, et al. Selective termination of lncRNA transcription promotes heterochromatin silencing and cell differentiation. EMBO J. 2017;36(17):2626–41. doi: 10.15252/embj.201796571 28765164
31. Sugiyama T, Wanatabe N, Kitahata E, Tani T, Sugioka-Sugiyama R. Red5 and three nuclear pore components are essential for efficient suppression of specific mRNAs during vegetative growth of fission yeast. Nucleic Acids Res. 2013;41(13):6674–86. doi: 10.1093/nar/gkt363 23658229
32. Sugiyama T, Thillainadesan G, Chalamcharla VR, Meng Z, Balachandran V, Dhakshnamoorthy J, et al. Enhancer of Rudimentary Cooperates with Conserved RNA-Processing Factors to Promote Meiotic mRNA Decay and Facultative Heterochromatin Assembly. Mol Cell. 2016;61(5):747–59. doi: 10.1016/j.molcel.2016.01.029 26942678
33. Shichino Y, Otsubo Y, Kimori Y, Yamamoto M, Yamashita A. YTH-RNA-binding protein prevents deleterious expression of meiotic proteins by tethering their mRNAs to nuclear foci. eLife. 2018;7:e32155. doi: 10.7554/eLife.32155 29424342
34. Xie G, Vo TV, Thillainadesan G, Holla S, Zhang B, Jiang Y, et al. A conserved dimer interface connects ERH and YTH family proteins to promote gene silencing. Nature communications. 2019;10(1):251. doi: 10.1038/s41467-018-08273-9 30651569
35. Cole C, Barber JD, Barton GJ. The Jpred 3 secondary structure prediction server. Nucleic Acids Res. 2008;36(Web Server issue):W197–201. doi: 10.1093/nar/gkn238 18463136
36. Fox MJ, Mosley AL. Rrp6: Integrated roles in nuclear RNA metabolism and transcription termination. Wiley interdisciplinary reviews RNA. 2016;7(1):91–104. doi: 10.1002/wrna.1317 26612606
37. Shichino Y, Yamashita A, Yamamoto M. Meiotic long non-coding meiRNA accumulates as a dot at its genetic locus facilitated by Mmi1 and plays as a decoy to lure Mmi1. Open biology. 2014;4(6):140022. doi: 10.1098/rsob.140022 24920274
38. Meola N, Domanski M, Karadoulama E, Chen Y, Gentil C, Pultz D, et al. Identification of a Nuclear Exosome Decay Pathway for Processed Transcripts. Mol Cell. 2016;64(3):520–33. doi: 10.1016/j.molcel.2016.09.025 27871484
39. Ogami K, Richard P, Chen Y, Hoque M, Li W, Moresco JJ, et al. An Mtr4/ZFC3H1 complex facilitates turnover of unstable nuclear RNAs to prevent their cytoplasmic transport and global translational repression. Genes & development. 2017;31(12):1257–71. doi: 10.1101/gad.302604.117 28733371
40. Silla T, Karadoulama E, Makosa D, Lubas M, Jensen TH. The RNA Exosome Adaptor ZFC3H1 Functionally Competes with Nuclear Export Activity to Retain Target Transcripts. Cell reports. 2018;23(7):2199–210. doi: 10.1016/j.celrep.2018.04.061 29768216
41. Gutz H, Heslot H, Leupold U, Loprieno N. Schizosaccharomyces pombe. In Handbook of Genetics. King RD, editor. New York: Plenum Publishing Corporation; 1974. 395–446.
42. Moreno S, Klar A, Nurse P. Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol. 1991;194:795–823. doi: 10.1016/0076-6879(91)94059-l 2005825
43. Bahler J, Wu JQ, Longtine MS, Shah NG, McKenzie A 3rd, Steever AB, et al. Heterologous modules for efficient and versatile PCR-based gene targeting in Schizosaccharomyces pombe. Yeast. 1998;14(10):943–51. doi: 10.1002/(SICI)1097-0061(199807)14:10<943::AID-YEA292>3.0.CO;2-Y 9717240
44. Sato M, Dhut S, Toda T. New drug-resistant cassettes for gene disruption and epitope tagging in Schizosaccharomyces pombe. Yeast. 2005;22(7):583–91. doi: 10.1002/yea.1233 15942936
45. Basi G, Schmid E, Maundrell K. TATA box mutations in the Schizosaccharomyces pombe nmt1 promoter affect transcription efficiency but not the transcription start point or thiamine repressibility. Gene. 1993;123:131–6. doi: 10.1016/0378-1119(93)90552-e 8422997
46. Matsuo T, Otsubo Y, Urano J, Tamanoi F, Yamamoto M. Loss of the TOR kinase Tor2 mimics nitrogen starvation and activates the sexual development pathway in fission yeast. Mol Cell Biol. 2007;27(8):3154–64. doi: 10.1128/MCB.01039-06 17261596
47. Kato H, Okazaki K, Iida T, Nakayama J, Murakami Y, Urano T. Spt6 prevents transcription-coupled loss of posttranslationally modified histone H3. Scientific reports. 2013;3:2186. doi: 10.1038/srep02186 23851719
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