The RNA Helicases AtMTR4 and HEN2 Target Specific Subsets of Nuclear Transcripts for Degradation by the Nuclear Exosome in
Cells rely on a number of RNA degradation pathways to ensure correct and timely processing and turnover of both coding and non-coding RNAs. Another important function of RNA degradation is the rapid elimination of misprocessed RNA species, maturation by-products, and nonfunctional RNAs that are frequently produced by pervasive transcription. The main 3′-5′ RNA degradation machine in eukaryotic cells is the exosome, which is activated by cofactors such as RNA helicases. In yeast and human, processing, turnover and surveillance of all nuclear exosome targets depend on a single RNA helicase, MTR4. We show here that the Arabidopsis exosome complex can associate with two related RNA helicases, MTR4 and HEN2. MTR4 and HEN2 reside in nucleolar and nucleoplasmic compartments, respectively, and target different subsets of nuclear RNA substrates for degradation by the exosome. The presence of both MTR4 and HEN2 homologues in green algae, mosses and land plants suggest that the functional duality of exosome-associated RNA helicases is evolutionarily conserved in the entire green lineage. The emerging picture is that, despite a high degree of sequence conservation, intracellular distribution, activities and functions of exosome cofactors vary considerably among different eukaryotes.
Vyšlo v časopise:
The RNA Helicases AtMTR4 and HEN2 Target Specific Subsets of Nuclear Transcripts for Degradation by the Nuclear Exosome in. PLoS Genet 10(8): e32767. doi:10.1371/journal.pgen.1004564
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1004564
Souhrn
Cells rely on a number of RNA degradation pathways to ensure correct and timely processing and turnover of both coding and non-coding RNAs. Another important function of RNA degradation is the rapid elimination of misprocessed RNA species, maturation by-products, and nonfunctional RNAs that are frequently produced by pervasive transcription. The main 3′-5′ RNA degradation machine in eukaryotic cells is the exosome, which is activated by cofactors such as RNA helicases. In yeast and human, processing, turnover and surveillance of all nuclear exosome targets depend on a single RNA helicase, MTR4. We show here that the Arabidopsis exosome complex can associate with two related RNA helicases, MTR4 and HEN2. MTR4 and HEN2 reside in nucleolar and nucleoplasmic compartments, respectively, and target different subsets of nuclear RNA substrates for degradation by the exosome. The presence of both MTR4 and HEN2 homologues in green algae, mosses and land plants suggest that the functional duality of exosome-associated RNA helicases is evolutionarily conserved in the entire green lineage. The emerging picture is that, despite a high degree of sequence conservation, intracellular distribution, activities and functions of exosome cofactors vary considerably among different eukaryotes.
Zdroje
1. Lykke-AndersenS, TomeckiR, JensenTH, DziembowskiA (2011) The eukaryotic RNA exosome: same scaffold but variable catalytic subunits. RNA Biol 8: 61–66.
2. JanuszykK, LimaCD (2014) The eukaryotic RNA exosome. Curr Opin Struct Biol 24C: 132–140.
3. SchneiderC, KudlaG, WlotzkaW, TuckA, TollerveyD (2012) Transcriptome-wide analysis of exosome targets. Mol Cell 48: 422–433.
4. GudipatiRK, XuZ, LebretonA, SéraphinB, SteinmetzLM, et al. (2012) Extensive degradation of RNA precursors by the exosome in wild-type cells. Mol Cell 48: 409–421.
5. ChekanovaJA, GregoryBD, ReverdattoSV, ChenH, KumarR, et al. (2007) Genome-wide high-resolution mapping of exosome substrates reveals hidden features in the Arabidopsis transcriptome. Cell 131: 1340–1353.
6. BrownJT, BaiX, JohnsonAW (2000) The yeast antiviral proteins Ski2p, Ski3p, and Ski8p exist as a complex in vivo. RNA 6: 449–457.
7. AndersonJS, ParkerRP (1998) The 3′ to 5′ degradation of yeast mRNAs is a general mechanism for mRNA turnover that requires the SKI2 DEVH box protein and 3′ to 5′ exonucleases of the exosome complex. EMBO J 17: 1497–1506.
8. De la CruzJ, KresslerD, TollerveyD, LinderP (1998) Dob1p (Mtr4p) is a putative ATP-dependent RNA helicase required for the 3′ end formation of 5.8S rRNA in Saccharomyces cerevisiae. EMBO J 17: 1128–1140.
9. LubasM, ChristensenMS, KristiansenMS, DomanskiM, FalkenbyLG, et al. (2011) Interaction profiling identifies the human nuclear exosome targeting complex. Mol Cell 43: 624–637.
10. BernsteinJ, PattersonDN, WilsonGM, TothEA (2008) Characterization of the Essential Activities of Saccharomyces cerevisiae Mtr4p, a 3′-5′ Helicase Partner of the Nuclear Exosome. J Biol Chem 283: 4930–4942.
11. KobayashiK, OteguiMS, KrishnakumarS, MindrinosM, ZambryskiP (2007) INCREASED SIZE EXCLUSION LIMIT 2 encodes a putative DEVH box RNA helicase involved in plasmodesmata function during Arabidopsis embryogenesis. Plant Cell 19: 1885–1897.
12. WesternTL, ChengY, LiuJ, ChenX (2002) HUA ENHANCER2, a putative DExH-box RNA helicase, maintains homeotic B and C gene expression in Arabidopsis. Development 129: 1569–1581.
13. LangeH, SementFM, GagliardiD (2011) MTR4, a putative RNA helicase and exosome co-factor, is required for proper rRNA biogenesis and development in Arabidopsis thaliana. Plant J 68: 51–63.
14. AbbasiN, KimHB, ParkN-I, KimH-S, KimY-K, et al. (2010) APUM23, a nucleolar Puf domain protein, is involved in pre-ribosomal RNA processing and normal growth patterning in Arabidopsis. Plant J 64: 960–976.
15. PetrickaJJ, NelsonTM (2007) Arabidopsis nucleolin affects plant development and patterning. Plant Physiol 144: 173–186.
16. KojimaH, SuzukiT, KatoT, EnomotoK, SatoS, et al. (2007) Sugar-inducible expression of the nucleolin-1 gene of Arabidopsis thaliana and its role in ribosome synthesis, growth and development. Plant J 49: 1053–1063.
17. PontvianneF, MatiaI, DouetJ, TourmenteS, MedinaFJ, et al. (2007) Characterization of AtNUC-L1 Reveals a Central Role of Nucleolin in Nucleolus Organization and Silencing of AtNUC-L2 Gene in Arabidopsis. Mol Biol Cell 18: 369–379.
18. ByrneME (2009) A role for the ribosome in development. Trends Plant Sci 14: 512–519.
19. RosadoA, SohnEJ, DrakakakiG, PanS, SwidergalA, et al. (2010) Auxin-mediated ribosomal biogenesis regulates vacuolar trafficking in Arabidopsis. Plant Cell 22: 143–158.
20. ChengY, KatoN, WangW, LiJ, ChenX (2003) Two RNA binding proteins, HEN4 and HUA1, act in the processing of AGAMOUS pre-mRNA in Arabidopsis thaliana. Dev Cell 4: 53–66.
21. AndersenPR, DomanskiM, KristiansenMS, StorvallH, NtiniE, et al. (2013) The human cap-binding complex is functionally connected to the nuclear RNA exosome. Nat Struct Mol Biol 20: 1367–1376.
22. LangeH, SementFM, CanadayJ, GagliardiD (2009) Polyadenylation-assisted RNA degradation processes in plants. Trends Plant Sci 14: 497–504.
23. ZhangW, MurphyC, SieburthLE (2010) Conserved RNaseII domain protein functions in cytoplasmic mRNA decay and suppresses Arabidopsis decapping mutant phenotypes. Proc Natl Acad Sci USA 107: 15981–15985.
24. ShinJ-H, WangH-LV, LeeJ, DinwiddieBL, BelostotskyDA, et al. (2013) The role of the Arabidopsis Exosome in siRNA-independent silencing of heterochromatic loci. PLoS Genet 9: e1003411 doi:10.1371/journal.pgen.1003411
25. KumakuraN, OtsukiH, TsuzukiM, TakedaA, WatanabeY (2013) Arabidopsis AtRRP44A is the functional homolog of Rrp44/Dis3, an exosome component, is essential for viability and is required for RNA processing and degradation. PLoS ONE 8: e79219 doi:10.1371/journal.pone.0079219
26. HookerTS, LamP, ZhengH, KunstL (2007) A core subunit of the RNA-processing/degrading exosome specifically influences cuticular wax biosynthesis in Arabidopsis. Plant Cell 19: 904–913.
27. ChenX, GoodwinSM, LiuX, ChenX, BressanRA, et al. (2005) Mutation of the RESURRECTION1 locus of Arabidopsis reveals an association of cuticular wax with embryo development. Plant Physiol 139: 909–919.
28. AllmangC, PetfalskiE, PodtelejnikovA, MannM, TollerveyD, et al. (1999) The yeast exosome and human PM-Scl are related complexes of 3′ – 5′ exonucleases. Genes Dev 13: 2148–2158.
29. GrahamAC, KissDL, AndrulisED (2006) Differential distribution of exosome subunits at the nuclear lamina and in cytoplasmic foci. Mol Biol Cell 17: 1399–1409.
30. TomeckiR, KristiansenMS, Lykke-AndersenS, ChlebowskiA, LarsenKM, et al. (2010) The human core exosome interacts with differentially localized processive RNases: hDIS3 and hDIS3L. EMBO J 29: 2342–2357.
31. StaalsRHJ, BronkhorstAW, SchildersG, SlomovicS, SchusterG, et al. (2010) Dis3-like 1: a novel exoribonuclease associated with the human exosome. EMBO J 29: 2358–2367.
32. DorceyE, Rodriguez-VillalonA, SalinasP, SantuariL, PradervandS, et al. (2012) Context-Dependent Dual Role of SKI8 Homologs in mRNA Synthesis and Turnover. PLoS Genet 8: e1002652 doi:10.1371/journal.pgen.1002652
33. FabreA, CharrouxB, Martinez-VinsonC, RoquelaureB, OdulE, et al. (2012) SKIV2L Mutations Cause Syndromic Diarrhea, or Trichohepatoenteric Syndrome. The American Journal of Human Genetics 90: 689–692.
34. WeirJR, BonneauF, HentschelJ, ContiE (2010) Structural analysis reveals the characteristic features of Mtr4, a DExH helicase involved in nuclear RNA processing and surveillance. Proc Natl Acad Sci USA 107: 12139–12144.
35. JacksonRN, KlauerAA, HintzeBJ, RobinsonH, van HoofA, et al. (2010) The crystal structure of Mtr4 reveals a novel arch domain required for rRNA processing. EMBO J 29: 2205–2216.
36. JohnsonSJ, JacksonRN (2013) Ski2-like RNA helicase structures: Common themes and complex assemblies. RNA Biol 10: 33–43.
37. HalbachF, RodeM, ContiE (2012) The crystal structure of S. cerevisiae Ski2, a DExH helicase associated with the cytoplasmic functions of the exosome. RNA 18: 124–134.
38. PihKT, YiMJ, LiangYS, ShinBJ, ChoMJ, et al. (2000) Molecular cloning and targeting of a fibrillarin homolog from Arabidopsis. Plant Physiol 123: 51–58.
39. BarnecheF, SteinmetzF, EcheverríaM (2000) Fibrillarin genes encode both a conserved nucleolar protein and a novel small nucleolar RNA involved in ribosomal RNA methylation in Arabidopsis thaliana. J Biol Chem 275: 27212–27220.
40. KastenmayerJP, GreenPJ (2000) Novel features of the XRN-family in Arabidopsis: evidence that AtXRN4, one of several orthologs of nuclear Xrn2p/Rat1p, functions in the cytoplasm. Proc Natl Acad Sci USA 97: 13985–13990.
41. Zakrzewska-PlaczekM, SouretFF, SobczykGJ, GreenPJ, KufelJ (2010) Arabidopsis thaliana XRN2 is required for primary cleavage in the pre-ribosomal RNA. Nucleic Acids Res 38: 4487–4502.
42. TillemansV, DispaL, RemacleC, CollingeM, MotteP (2005) Functional distribution and dynamics of Arabidopsis SR splicing factors in living plant cells. Plant J 41: 567–582.
43. LorkovicZJ, LopatoS, PexaM, LehnerR, BartaA (2004) Interactions of Arabidopsis RS domain containing cyclophilins with SR proteins and U1 and U11 small nuclear ribonucleoprotein-specific proteins suggest their involvement in pre-mRNA Splicing. J Biol Chem 279: 33890–33898.
44. Marchler-BauerA, ZhengC, ChitsazF, DerbyshireMK, GeerLY, et al. (2013) CDD: conserved domains and protein three-dimensional structure. Nucleic Acids Res 41: D348–352.
45. DèrozierS, SamsonF, TambyJ-P, GuichardC, BrunaudV, et al. (2011) Exploration of plant genomes in the FLAGdb++ environment. Plant Methods 7: 8.
46. SherstnevA, DucC, ColeC, ZacharakiV, HornyikC, et al. (2012) Direct sequencing of Arabidopsis thaliana RNA reveals patterns of cleavage and polyadenylation. Nat Struct Mol Biol 19: 845–852.
47. LiuJ, JungC, XuJ, WangH, DengS, et al. (2012) Genome-wide analysis uncovers regulation of long intergenic noncoding RNAs in Arabidopsis. Plant Cell 24: 4333–4345.
48. GoliszA, SikorskiPJ, KruszkaK, KufelJ (2013) Arabidopsis thaliana LSM proteins function in mRNA splicing and degradation. Nucleic Acids Res 41 (12) 6232–49.
49. GyI, GasciolliV, LauresserguesD, MorelJ-B, GombertJ, et al. (2007) Arabidopsis FIERY1, XRN2, and XRN3 are endogenous RNA silencing suppressors. Plant Cell 19: 3451–3461.
50. MorenoAB, Martínez de AlbaAE, BardouF, CrespiMD, VaucheretH, et al. (2013) Cytoplasmic and nuclear quality control and turnover of single-stranded RNA modulate post-transcriptional gene silencing in plants. Nucleic Acids Res 41: 4699–4708.
51. ElmayanT, BalzergueS, BéonF, BourdonV, DaubremetJ, et al. (1998) Arabidopsis mutants impaired in cosuppression. Plant Cell 10: 1747–1758.
52. Martínez de AlbaAE, JauvionV, MalloryAC, BouteillerN, VaucheretH (2011) The miRNA pathway limits AGO1 availability during siRNA-mediated PTGS defense against exogenous RNA. Nucleic Acids Res 39: 9339–9344.
53. DaxingerL, HunterB, SheikhM, JauvionV, GasciolliV, et al. (2008) Unexpected silencing effects from T-DNA tags in Arabidopsis. Trends Plant Sci 13: 4–6.
54. Le MassonI, JauvionV, BouteillerN, RivardM, ElmayanT, et al. (2012) Mutations in the Arabidopsis H3K4me2/3 demethylase JMJ14 suppress posttranscriptional gene silencing by decreasing transgene transcription. Plant Cell 24: 3603–3612.
55. LangeH, HolecS, CognatV, PieuchotL, Le RetM, et al. (2008) Degradation of a polyadenylated rRNA maturation by-product involves one of the three RRP6-like proteins in Arabidopsis thaliana. Mol Cell Biol 28: 3038–3044.
56. ZhangH, TangK, QianW, DuanC-G, WangB, et al. (2014) An Rrp6-like Protein Positively Regulates Noncoding RNA Levels and DNA Methylation in Arabidopsis. Mol Cell 54: 418–30 doi:10.1016/j.molcel.2014.03.019
57. SchildersG, DijkEvan, PruijnGJM (2007) C1D and hMtr4p associate with the human exosome subunit PM/Scl-100 and are involved in pre-rRNA processing. Nucleic Acids Res 35: 2564–2572.
58. HouseleyJ, TollerveyD (2006) Yeast Trf5p is a nuclear poly(A) polymerase. EMBO Rep 7: 205–211.
59. LaCavaJ, HouseleyJ, SaveanuC, PetfalskiE, ThompsonE, et al. (2005) RNA degradation by the exosome is promoted by a nuclear polyadenylation complex. Cell 121: 713–724.
60. WyersF, RougemailleM, BadisG, RousselleJ-C, DufourM-E, et al. (2005) Cryptic pol II transcripts are degraded by a nuclear quality control pathway involving a new poly(A) polymerase. Cell 121: 725–737.
61. VanacovaS, WolfJ, MartinG, BlankD, DettwilerS, et al. (2005) A new yeast poly(A) polymerase complex involved in RNA quality control. PLoS Biol 3: e189 doi:10.1371/journal.pbio.0030189
62. HolubP, VanacovaS (2012) TRAMP Stimulation of Exosome. Eukaryotic RNases and their Partners in RNA Degradation and Biogenesis, Part A, in: The Enzymes 31: 77–90.
63. EgeciogluDE, HenrasAK, ChanfreauGF (2006) Contributions of Trf4p- and Trf5p-dependent polyadenylation to the processing and degradative functions of the yeast nuclear exosome. RNA 12: 26–32.
64. San PaoloS, VanacovaS, SchenkL, ScherrerT, BlankD, et al. (2009) Distinct roles of non-canonical poly(A) polymerases in RNA metabolism. PLoS Genet 5: e1000555 doi:10.1371/journal.pgen.1000555
65. KarimiM, InzéD, DepickerA (2002) GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci 7: 193–195.
66. NakamuraS, ManoS, TanakaY, OhnishiM, NakamoriC, et al. (2010) Gateway binary vectors with the bialaphos resistance gene, bar, as a selection marker for plant transformation. Biosci Biotechnol Biochem 74: 1315–1319.
67. KimSH, MacfarlaneS, KalininaNO, RakitinaDV, RyabovEV, et al. (2007) Interaction of a plant virus-encoded protein with the major nucleolar protein fibrillarin is required for systemic virus infection. Proc Natl Acad Sci USA 104: 11115–11120.
68. Nisa-MartínezR, LaporteP, Jiménez-ZurdoJI, FrugierF, CrespiM, et al. (2013) Localization of a bacterial group II intron-encoded protein in eukaryotic nuclear splicing-related cell compartments. PLoS ONE 8: e84056 doi:10.1371/journal.pone.0084056
69. CloughSJ, BentAF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16: 735–743.
70. PoirierI, HammannP, KuhnL, BertrandM (2013) Strategies developed by the marine bacterium Pseudomonas fluorescens BA3SM1 to resist metals: A proteome analysis. Aquat Toxicol 128–129: 215–232.
71. HuangDW, ShermanBT, LempickiRA (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4: 44–57.
72. HuangDW, ShermanBT, LempickiRA (2009) Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res 37: 1–13.
73. LurinC, AndrésC, AubourgS, BellaouiM, BittonF, et al. (2004) Genome-wide analysis of Arabidopsis pentatricopeptide repeat proteins reveals their essential role in organelle biogenesis. Plant Cell 16: 2089–2103.
74. Yang YH, Dudoit S, Luu P, Lin DM, Peng V, et al.. (2002) Normalization for cDNA microarray data: a robust composite method addressing single and multiple slide systematic variation. Nucleic Acids Res 30 : e15. PMCID:PMC100354
75. LameschP, BerardiniTZ, LiD, SwarbreckD, WilksC, et al. (2012) The Arabidopsis Information Resource (TAIR): improved gene annotation and new tools. Nucleic Acids Res 40: D1202–1210.
76. AltschulSF, GishW, MillerW, MyersEW, LipmanDJ (1990) Basic local alignment search tool. J Mol Biol 215: 403–410.
77. FloreaL, HartzellG, ZhangZ, RubinGM, MillerW (1998) A computer program for aligning a cDNA sequence with a genomic DNA sequence. Genome Res 8: 967–974.
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Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
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