#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

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


Článek vyšel v časopise

PLOS Genetics


2020 Číslo 2
Nejčtenější tento týden
Nejčtenější v tomto čísle
Kurzy

Zvyšte si kvalifikaci online z pohodlí domova

Důležitost adherence při depresivním onemocnění
nový kurz
Autoři: MUDr. Eliška Bartečková, Ph.D.

Koncepce osteologické péče pro gynekology a praktické lékaře
Autoři: MUDr. František Šenk

Sekvenční léčba schizofrenie
Autoři: MUDr. Jana Hořínková, Ph.D.

Hypertenze a hypercholesterolémie – synergický efekt léčby
Autoři: prof. MUDr. Hana Rosolová, DrSc.

Multidisciplinární zkušenosti u pacientů s diabetem
Autoři: Prof. MUDr. Martin Haluzík, DrSc., prof. MUDr. Vojtěch Melenovský, CSc., prof. MUDr. Vladimír Tesař, DrSc.

Všechny kurzy
Přihlášení
Zapomenuté heslo

Zadejte e-mailovou adresu, se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.

Přihlášení

Nemáte účet?  Registrujte se

#ADS_BOTTOM_SCRIPTS#