Regulation of cytoplasmic RNA stability: Lessons from Drosophila

Advanced Review

Sarah F. Newbury, Benjamin P. Towler

Published Online: Aug 15 2018

DOI: 10.1002/wrna.1499

Full article on Wiley Online Library: HTML PDF

Can't access this content? Tell your librarian.

The process of RNA degradation is a critical level of regulation contributing to the control of gene expression. In the last two decades a number of studies have shown the specific and targeted nature of RNA decay and its importance in maintaining homeostasis. The key players within the pathways of RNA decay are well conserved with their mutation or disruption resulting in distinct phenotypes as well as human disease. Model organisms including Drosophila melanogaster have played a substantial role in elucidating the mechanisms conferring control over RNA stability. A particular advantage of this model organism is that the functions of ribonucleases can be assessed in the context of natural cells within tissues in addition to individual immortalized cells in culture. Drosophila RNA stability research has demonstrated how the cytoplasmic decay machines, such as the exosome, Dis3L2 and Xrn1, are responsible for regulating specific processes including apoptosis, proliferation, wound healing and fertility. The work discussed here has begun to identify specific mRNA transcripts that appear sensitive to specific decay pathways representing mechanisms through which the ribonucleases control mRNA stability. Drosophila research has also contributed to our knowledge of how specific RNAs are targeted to the ribonucleases including AU rich elements, miRNA targeting and 3′ tailing. Increased understanding of these mechanisms is critical to elucidating the control elicited by the cytoplasmic ribonucleases which is relevant to human disease. This article is categorized under: RNA in Disease and Development > RNA in Development RNA Turnover and Surveillance > Regulation of RNA Stability RNA Turnover and Surveillance > Turnover/Surveillance Mechanisms

Methods of targeting decay. (a) AU rich elements (AREs) usually within the 3′UTR recruit specific RNA binding proteins (Drosophila TTP homology Tis11 shown). ARE binding proteins subsequently promote 3′→5′ decay by the exosome where in Drosophila Dis3/Tazman (named Rrp44 in S. cerevisiae) provides catalytic activity or 5′→3′ decay by XRN1/Pacman (Pcm). The direction of decay can be transcript and protein specific. (b) miRNAs direct the RNA induced silencing complex (RISC) containing either Ago1 or Ago2 to specific target sites, usually in the 3′UTR, and can promote translational repression at the stages of initiation or elongation depending on the nature of the ago protein. When extensive complementarity is present between a miRNA and its target Ago2‐RISC directs cleavage of the target RNA. Extended repression can also result in mRNA degradation through classical decay pathways. (c) an mRNA can be targeted for decay following nucleotide additions to the 3′ end. Uridylation by a Drosophila terminal Uridylyl transferase (TUTase) named tailor is depicted. This primes the RNA for Dis3L2 mediated decay

[ Normal View | Magnified View ]

References

Abdelmohsen,, K., & Gorospe,, M. (2010). Posttranscriptional regulation of cancer traits by HuR. WIREs RNA, 1(2), 214–229. https://doi.org/10.1002/wrna.4
Allmang,, C., Kufel,, J., Chanfreau,, G., Mitchell,, P., Petfalski,, E., & Tollervey,, D. (1999). Functions of the exosome in rRNA, snoRNA and snRNA synthesis. EMBO Journal, 18(19), 5399–5410. https://doi.org/10.1093/emboj/18.19.5399
Ameres,, S. L., Horwich,, M. D., Hung,, J. H., Xu,, J., Ghildiyal,, M., Weng,, Z., & Zamore,, P. D. (2010). Target RNA‐directed trimming and tailing of small silencing RNAs. Science, 328(5985), 1534–1539. https://doi.org/10.1126/science.1187058
An,, H., Lee,, K., & Kim,, J. (2004). Identification of an exoribonuclease homolog, CaKEM1/CaXRN1, in Candida albicans and its characterization in filamentous growth. FEMS Microbiology Letters, 235(2), 297–303. https://doi.org/10.1111/j.1574-6968.2004.tb09602.x
Antic,, S., Wolfinger,, M., Skucha,, A., Hosiner,, S., & Dorner,, S. (2015). General and microRNA‐mediated mRNA degradation occurs on ribosome complexes in Drosophila cells. Molecular and Cellular Biology, 35(13), 2309–2320. https://doi.org/10.1128/mcb.01346-14
Astuti,, D., Morris,, M. R., Cooper,, W. N., Staals,, R. H., Wake,, N. C., Fews,, G. A., … Maher,, E. R. (2012). Germline mutations in DIS3L2 cause the Perlman syndrome of overgrowth and Wilms tumor susceptibility. Nature Genetics, 44(3), 277–284. https://doi.org/10.1038/ng.1071
Baccarini,, A., Chauhan,, H., Gardner,, T. J., Jayaprakash,, A. D., Sachidanandam,, R., & Brown,, B. D. (2011). Kinetic analysis reveals the fate of a microRNA following target regulation in mammalian cells. Current Biology, 21(5), 369–376.
Bakheet,, T., Frevel,, M., Williams,, B. R. G., Greer,, W., & Khabar,, K. S. A. (2001). ARED: Human AU‐rich element‐containing mRNA database reveals an unexpectedly diverse functional repertoire of encoded proteins. Nucleic Acids Research, 29(1), 246–254.
Bakheet,, T., Hitti,, E., & Khabar,, K. S. A. (2018). ARED‐plus: An updated and expanded database of AU‐rich element‐containing mRNAs and pre‐mRNAs. Nucleic Acids Research, 46(D1), D218–D220. https://doi.org/10.1093/nar/gkx975
Bakheet,, T., Williams,, B. R., & Khabar,, K. S. (2006). ARED 3.0: The large and diverse AU‐rich transcriptome. Nucleic Acids Research, 34(Database issue), D111–D114. https://doi.org/10.1093/nar/gkj052
Bassett,, A. R., Tibbit,, C., Ponting,, C. P., & Liu,, J. (2013). Highly efficient targeted mutagenesis of Drosophila with the CRISPR/Cas9 system. Cell Reports, 4(1), 220–228. https://doi.org/10.1016/j.celrep.2013.06.020
Bazzini,, A. A., del Viso,, F., Moreno‐Mateos,, M. A., Johnstone,, T. G., Vejnar,, C. E., Qin,, Y., … Giraldez,, A. J. (2016). Codon identity regulates mRNA stability and translation efficiency during the maternal‐to‐zygotic transition. The EMBO Journal, 35(19), 2087–2103. https://doi.org/10.15252/embj.201694699
Berezikov,, E. (2011). Evolution of microRNA diversity and regulation in animals. Nature Reviews. Genetics, 12(12), 846–860. https://doi.org/10.1038/nrg3079
Bitetti,, A., Mallory,, A. C., Golini,, E., Carrieri,, C., Carreño Gutiérrez,, H., Perlas,, E., … Shkumatava,, A. (2018). MicroRNA degradation by a conserved target RNA regulates animal behavior. Nature Structural %26 Molecular Biology, 25(3), 244–251. https://doi.org/10.1038/s41594-018-0032-x
Boczonadi,, V., Müller,, J. S., Pyle,, A., Munkley,, J., Dor,, T., Quartararo,, J., … Horvath,, R. (2014). EXOSC8 mutations alter mRNA metabolism and cause hypomyelination with spinal muscular atrophy and cerebellar hypoplasia. [article]. Nature Communications, 5, 4287. https://doi.org/10.1038/ncomms5287
Bonneau,, F., Basquin,, J., Ebert,, J., Lorentzen,, E., & Conti,, E. (2009). The yeast exosome functions as a macromolecular cage to channel RNA substrates for degradation. Cell, 139(3), 547–559. https://doi.org/10.1016/j.cell.2009.08.042
Bortolamiol‐Becet,, D., Hu,, F., Jee,, D., Wen,, J., Okamura,, K., Lin,, C., … Lai,, E. C. (2015). Selective suppression of the splicing‐mediated MicroRNA pathway by the terminal Uridyltransferase tailor. Molecular Cell, 59(2), 217–228. https://doi.org/10.1016/j.molcel.2015.05.034
Braun,, J. E., Truffault,, V., Boland,, A., Huntzinger,, E., Chang,, C. T., Haas,, G., … Izaurralde,, E. (2012). A direct interaction between DCP1 and XRN1 couples mRNA decapping to 5′ exonucleolytic degradation. Nature Structural %26 Molecular Biology, 19(12), 1324–1331. https://doi.org/10.1038/nsmb.2413
Brown,, C. E., & Sachs,, A. B. (1998). Poly(a) tail length control in Saccharomyces cerevisiae occurs by message‐specific Deadenylation. Molecular and Cellular Biology, 18(11), 6548–6559.
Burroughs,, A. M., Ando,, Y., de Hoon,, M. J., Tomaru,, Y., Nishibu,, T., Ukekawa,, R., … Daub,, C. O. (2010). A comprehensive survey of 3′ animal miRNA modification events and a possible role for 3′ adenylation in modulating miRNA targeting effectiveness. Genome Research, 20(10), 1398–1410. https://doi.org/10.1101/gr.106054.110
Cairrao,, F., Arraiano,, C., & Newbury,, S. (2005). Drosophila gene tazman, an orthologue of the yeast exosome component Rrp44p/Dis3, is differentially expressed during development. Developmental Dynamics, 232(3), 733–737. https://doi.org/10.1002/dvdy.20269
Cairrao,, F., Halees,, A. S., Khabar,, K. S. A., Morello,, D., & Vanzo,, N. (2009). AU‐rich elements regulate Drosophila gene expression. Molecular and Cellular Biology, 29(10), 2636–2643. https://doi.org/10.1128/mcb.01506-08
Callahan,, K. P., & Butler,, J. S. (2008). Evidence for core exosome independent function of the nuclear exoribonuclease Rrp6p. Nucleic Acids Research, 36(21), 6645–6655. https://doi.org/10.1093/nar/gkn743
Carballo,, E., & Blackshear,, P. J. (2001). Roles of tumor necrosis factor‐alpha receptor subtypes in the pathogenesis of the tristetraprolin‐deficiency syndrome. Blood, 98(8), 2389–2395.
Chang,, C. T., Bercovich,, N., Loh,, B., Jonas,, S., & Izaurralde,, E. (2014). The activation of the decapping enzyme DCP2 by DCP1 occurs on the EDC4 scaffold and involves a conserved loop in DCP1. Nucleic Acids Research, 42(8), 5217–5233.
Chang,, H. M., Triboulet,, R., Thornton,, J. E., & Gregory,, R. I. (2013). A role for the Perlman syndrome exonuclease Dis3l2 in the Lin28‐let‐7 pathway. Nature, 497(7448), 244–248. https://doi.org/10.1038/nature12119
Chapman,, E. G., Moon,, S. L., Wilusz,, J., & Kieft,, J. S. (2014). RNA structures that resist degradation by Xrn1 produce a pathogenic dengue virus RNA. eLife, 3, e01892. https://doi.org/10.7554/eLife.01892
Chapman,, M. A., Lawrence,, M. S., Keats,, J. J., Cibulskis,, K., Sougnez,, C., Schinzel,, A. C., … Golub,, T. R. (2011). Initial genome sequencing and analysis of multiple myeloma. Nature, 471(7339), 467–472. https://doi.org/10.1038/nature09837
Cheadle,, C., Fan,, J., Cho‐Chung,, Y. S., Werner,, T., Ray,, J., Do,, L., … Becker,, K. G. (2005). Stability regulation of mRNA and the control of gene expression. Annals of the New York Academy of Sciences, 1058, 196–204. https://doi.org/10.1196/annals.1359.026
Chen,, C. Y., & Shyu,, A. B. (1995). AU‐rich elements: Characterization and importance in mRNA degradation. Trends in Biochemical Sciences, 20(11), 465–470.
De Almeida,, C., Scheer,, H., Zuber,, H., & Gagliardi,, D. (2018). RNA uridylation: A key posttranscriptional modification shaping the coding and noncoding transcriptome. WIREs RNA, 9(1). https://doi.org/10.1002/wrna.1440
de Groen,, F. L., Krijgsman,, O., Tijssen,, M., Vriend,, L. E., Ylstra,, B., Hooijberg,, E., … Carvalho,, B. (2014). Gene‐dosage dependent overexpression at the 13q amplicon identifies DIS3 as candidate oncogene in colorectal cancer progression. Genes, Chromosomes %26 Cancer, 53(4), 339–348. https://doi.org/10.1002/gcc.22144
de la Mata,, M., Gaidatzis,, D., Vitanescu,, M., Stadler,, M. B., Wentzel,, C., Scheiffele,, P., … Grosshans,, H. (2015). Potent degradation of neuronal miRNAs induced by highly complementary targets. EMBO Reports, 16(4), 500–511. https://doi.org/10.15252/embr.201540078
De Lella Ezcurra,, A. L., Bertolin,, A. P., Kim,, K., Katz,, M. J., Gándara,, L., Misra,, T., … Wappner,, P. (2016). miR‐190 enhances HIF‐dependent responses to hypoxia in Drosophila by inhibiting the Prolyl‐4‐hydroxylase Fatiga. PLoS Genetics, 12(5), e1006073. https://doi.org/10.1371/journal.pgen.1006073
Decker,, C. J., & Parker,, R. (1993). A turnover pathway for both stable and unstable mRNAs in yeast: Evidence for a requirement for deadenylation. Genes %26 Development, 7(8), 1632–1643.
Di Donato,, N., Neuhann,, T., Kahlert,, A., Klink,, B., Hackmann,, K., Neuhann,, I., … Rump,, A. (2016). Mutations in EXOSC2 are associated with a novel syndrome characterised by retinitis pigmentosa, progressive hearing loss, premature ageing, short stature, mild intellectual disability and distinctive gestalt. Journal of Medical Genetics, 53(6), 419–425. https://doi.org/10.1136/jmedgenet-2015-103511
Ding,, L., Ley,, T. J., Larson,, D. E., Miller,, C. A., Koboldt,, D. C., Welch,, J. S., … DiPersio,, J. F. (2012). Clonal evolution in relapsed acute myeloid leukaemia revealed by whole‐genome sequencing. Nature, 481(7382), 506–510. https://doi.org/10.1038/nature10738
Duffy,, J. B. (2002). GAL4 system in Drosophila: A fly geneticist`s Swiss army knife. Genesis, 34(1–2), 1–15. https://doi.org/10.1002/gene.10150
Eberle,, A. B., Lykke‐Andersen,, S., Mühlemann,, O., & Jensen,, T. H. (2008). SMG6 promotes endonucleolytic cleavage of nonsense mRNA in human cells. [article]. Nature Structural %26 Molecular Biology, 16, 49. https://doi.org/10.1038/nsmb.1530
Eckmann,, C. R., Rammelt,, C., & Wahle,, E. (2011). Control of poly(A) tail length. WIREs RNA, 2(3), 348–361. https://doi.org/10.1002/wrna.56
Eggens,, V. R. C., Barth,, P. G., Niermeijer,, J. F., Berg,, J. N., Darin,, N., Dixit,, A., … Baas,, F. (2014). EXOSC3 mutations in pontocerebellar hypoplasia type 1: Novel mutations and genotype‐phenotype correlations. Orphanet Journal of Rare Diseases, 9(1), 23. https://doi.org/10.1186/1750-1172-9-23
Eulalio,, A., Rehwinkel,, J., Stricker,, M., Huntzinger,, E., Yang,, S. F., Doerks,, T., … Izaurralde,, E. (2007). Target‐specific requirements for enhancers of decapping in miRNA‐mediated gene silencing. Genes %26 Development, 21(20), 2558–2570. https://doi.org/10.1101/gad.443107
Faehnle,, C. R., Walleshauser,, J., & Joshua‐Tor,, L. (2014). Mechanism of Dis3l2 substrate recognition in the Lin28‐let‐7 pathway. Nature, 514(7521), 252–256. https://doi.org/10.1038/nature13553
Fenger‐Gron,, M., Fillman,, C., Norrild,, B., & Lykke‐Andersen,, J. (2005). Multiple processing body factors and the ARE binding protein TTP activate mRNA decapping. Molecular Cell, 20(6), 905–915. https://doi.org/10.1016/j.molcel.2005.10.031
Forstemann,, K., Horwich,, M. D., Wee,, L., Tomari,, Y., & Zamore,, P. D. (2007). Drosophila microRNAs are sorted into functionally distinct argonaute complexes after production by dicer‐1. Cell, 130(2), 287–297. https://doi.org/10.1016/j.cell.2007.05.056
Frazao,, C., McVey,, C. E., Amblar,, M., Barbas,, A., Vonrhein,, C., Arraiano,, C. M., & Carrondo,, M. A. (2006). Unravelling the dynamics of RNA degradation by ribonuclease II and its RNA‐bound complex. Nature, 443(7107), 110–114. https://doi.org/10.1038/nature05080
Garneau,, N. L., Wilusz,, J., & Wilusz,, C. J. (2007). The highways and byways of mRNA decay. Nature Reviews. Molecular Cell Biology, 8(2), 113–126. https://doi.org/10.1038/nrm2104
Gatfield,, D., & Izaurralde,, E. (2004). Nonsense‐mediated messenger RNA decay is initiated by endonucleolytic cleavage in Drosophila. Nature, 429(6991), 575–578. https://doi.org/10.1038/nature02559
Graham,, A. C., Kiss,, D. L., & Andrulis,, E. D. (2006). Differential distribution of exosome subunits at the nuclear lamina and in cytoplasmic foci. Molecular Biology of the Cell, 17(3), 1399–1409. https://doi.org/10.1091/mbc.E05-08-0805
Graham,, A. C., Kiss,, D. L., & Andrulis,, E. D. (2009). Core exosome‐independent roles for Rrp6 in cell cycle progression. Molecular Biology of the Cell, 20(8), 2242–2253. https://doi.org/10.1091/mbc.E08-08-0825
Grima,, D. P., Sullivan,, M., Zabolotskaya,, M. V., Browne,, C., Seago,, J., Wan,, K. C., … Newbury,, S. F. (2008). The 5′→3′ exoribonuclease pacman is required for epithelial sheet sealing in Drosophila and genetically interacts with the phosphatase puckered. Biology of the Cell, 100(12), 687–701. https://doi.org/10.1042/bc20080049
Gudipati,, R. K., Xu,, Z., Lebreton,, A., Seraphin,, B., Steinmetz,, L. M., Jacquier,, A., & Libri,, D. (2012). Extensive degradation of RNA precursors by the exosome in wild‐type cells. Molecular Cell, 48(3), 409–421. https://doi.org/10.1016/j.molcel.2012.08.018
Haas,, G., Cetin,, S., Messmer,, M., Chane‐Woon‐Ming,, B., Terenzi,, O., Chicher,, J., … Pfeffer,, S. (2016). Identification of factors involved in target RNA‐directed microRNA degradation. Nucleic Acids Research, 44(6), 2873–2887.
Hales,, K. G., Korey,, C. A., Larracuente,, A. M., & Roberts,, D. M. (2015). Genetics on the fly: A primer on the Drosophila model system. Genetics, 201(3), 815–842. https://doi.org/10.1534/genetics.115.183392
Han,, B. W., Hung,, J. H., Weng,, Z., Zamore,, P. D., & Ameres,, S. L. (2011). The 3′‐to‐5′ exoribonuclease nibbler shapes the 3′ ends of microRNAs bound to Drosophila Argonaute1. Current Biology, 21(22), 1878–1887. https://doi.org/10.1016/j.cub.2011.09.034
Han,, J., & van Hoof,, A. (2016). The RNA exosome channeling and direct access conformations have distinct in vivo functions. Cell Reports, 16(12), 3348–3358. https://doi.org/10.1016/j.celrep.2016.08.059
Heo,, I., Joo,, C., Kim,, Y. K., Ha,, M., Yoon,, M. J., Cho,, J., … Kim,, V. N. (2009). TUT4 in concert with Lin28 suppresses microRNA biogenesis through pre‐microRNA uridylation. Cell, 138(4), 696–708. https://doi.org/10.1016/j.cell.2009.08.002
Herzog,, V. A., Reichholf,, B., & Ameres,, S. L. (2017). Thiol‐linked alkylation for the metabolic sequencing of RNA (SLAMseq).
Hopkins,, K. C., McLane,, L. M., Maqbool,, T., Panda,, D., Gordesky‐Gold,, B., & Cherry,, S. (2013). A genome‐wide RNAi screen reveals that mRNA decapping restricts bunyaviral replication by limiting the pools of Dcp2‐accessible targets for cap‐snatching. Genes %26 Development, 27(13), 1511–1525. https://doi.org/10.1101/gad.215384.113
Hou,, D., Ruiz,, M., & Andrulis,, E. D. (2012). The ribonuclease Dis3 is an essential regulator of the developmental transcriptome. [journal article]. BMC Genomics, 13(1), 359. https://doi.org/10.1186/1471-2164-13-359
Iwasaki,, S., Kawamata,, T., & Tomari,, Y. (2009). Drosophila argonaute1 and argonaute2 employ distinct mechanisms for translational repression. Molecular Cell, 34(1), 58–67. https://doi.org/10.1016/j.molcel.2009.02.010
Jonas,, S., Christie,, M., Peter,, D., Bhandari,, D., Loh,, B., Huntzinger,, E., … Izaurralde,, E. (2014). An asymmetric PAN3 dimer recruits a single PAN2 exonuclease to mediate mRNA deadenylation and decay. Nature Structural %26 Molecular Biology, 21(7), 599–608. https://doi.org/10.1038/nsmb.2837
Jones,, C. I., Grima,, D. P., Waldron,, J. A., Jones,, S., Parker,, H. N., & Newbury,, S. F. (2013). The 5′‐3′ exoribonuclease Pacman (Xrn1) regulates expression of the heat shock protein Hsp67Bc and the microRNA miR‐277‐3p in Drosophila wing imaginal discs. RNA Biology, 10(8), 1345–1355. https://doi.org/10.4161/rna.25354
Jones,, C. I., Pashler,, A. L., Towler,, B. P., Robinson,, S. R., & Newbury,, S. F. (2016). RNA‐seq reveals post‐transcriptional regulation of Drosophila insulin‐like peptide dilp8 and the neuropeptide‐like precursor Nplp2 by the exoribonuclease Pacman/XRN1. Nucleic Acids Research, 44(1), 267–280.
Jones,, C. I., Zabolotskaya,, M. V., & Newbury,, S. F. (2012). The 5′ → 3′ exoribonuclease XRN1/Pacman and its functions in cellular processes and development. WIREs RNA, 3(4), 455–468. https://doi.org/10.1002/wrna.1109
Juvvuna,, P. K., Khandelia,, P., Lee,, L. M., & Makeyev,, E. V. (2012). Argonaute identity defines the length of mature mammalian microRNAs. Nucleic Acids Research, 40(14), 6808–6820. https://doi.org/10.1093/nar/gks293
Kaberdin,, V. R., Singh,, D., & Lin‐Chao,, S. (2011). Composition and conservation of the mRNA‐degrading machinery in bacteria. Journal of Biomedical Science, 18, 23. https://doi.org/10.1186/1423-0127-18-23
Kadaba,, S., Krueger,, A., Trice,, T., Krecic,, A. M., Hinnebusch,, A. G., & Anderson,, J. (2004). Nuclear surveillance and degradation of hypomodified initiator tRNAMet in S. cerevisiae. Genes %26 Development, 18(11), 1227–1240. https://doi.org/10.1101/gad.1183804
Kahvejian,, A., Svitkin,, Y. V., Sukarieh,, R., M`Boutchou,, M. N., & Sonenberg,, N. (2005). Mammalian poly(A)‐binding protein is a eukaryotic translation initiation factor, which acts via multiple mechanisms. Genes %26 Development, 19(1), 104–113. https://doi.org/10.1101/gad.1262905
Katoh,, T., Sakaguchi,, Y., Miyauchi,, K., Suzuki,, T., Kashiwabara,, S., & Baba,, T. (2009). Selective stabilization of mammalian microRNAs by 3′ adenylation mediated by the cytoplasmic poly(A) polymerase GLD‐2. Genes %26 Development, 23(4), 433–438. https://doi.org/10.1101/gad.1761509
Kim,, J., & Kim,, J. (2002). KEM1 is involved in filamentous growth of Saccharomyces cerevisiae. FEMS Microbiology Letters, 216(1), 33–38. https://doi.org/10.1111/j.1574-6968.2002.tb11410.x
Kim,, K., Vinayagam,, A., & Perrimon,, N. (2014). A rapid genome‐wide microRNA screen identifies miR‐14 as a modulator of hedgehog signaling. Cell Reports, 7(6), 2066–2077. https://doi.org/10.1016/j.celrep.2014.05.025
Kinoshita,, N., Goebl,, M., & Yanagida,, M. (1991). The fission yeast dis3+ gene encodes a 110‐kDa essential protein implicated in mitotic control. Molecular and Cellular Biology, 11(12), 5839–5847.
Kiss,, D. L., & Andrulis,, E. D. (2010). Genome‐wide analysis reveals distinct substrate specificities of Rrp6, Dis3, and core exosome subunits. RNA, 16(4), 781–791. https://doi.org/10.1261/rna.1906710
Kowalinski,, E., Kogel,, A., Ebert,, J., Reichelt,, P., Stegmann,, E., Habermann,, B., & Conti,, E. (2016). Structure of a cytoplasmic 11‐subunit RNA exosome complex. Molecular Cell, 63(1), 125–134. https://doi.org/10.1016/j.molcel.2016.05.028
Larimer,, F. W., & Stevens,, A. (1990). Disruption of the gene XRN1, coding for a 5′→3′ exoribonuclease, restricts yeast cell growth. Gene, 95(1), 85–90.
Lebreton,, A., Tomecki,, R., Dziembowski,, A., & Seraphin,, B. (2008). Endonucleolytic RNA cleavage by a eukaryotic exosome. Nature, 456(7224), 993–996. https://doi.org/10.1038/nature07480
Lee,, M., Choi,, Y., Kim,, K., Jin,, H., Lim,, J., Nguyen,, T. A., … Kim,, V. N. (2014). Adenylation of maternally inherited microRNAs by Wispy. Molecular Cell, 56(5), 696–707. https://doi.org/10.1016/j.molcel.2014.10.011
Li,, C.‐H., Irmer,, H., Gudjonsdottir‐Planck,, D., Freese,, S., Salm,, H., Haile,, S., … Clayton,, C. (2006). Roles of a Trypanosoma brucei 5′→3′ exoribonuclease homolog in mRNA degradation. RNA, 12(12), 2171–2186. https://doi.org/10.1261/rna.291506
Lim,, J., Ha,, M., Chang,, H., Kwon,, S. C., Simanshu,, D. K., Patel,, D. J., & Kim,, V. N. (2014). Uridylation by TUT4 and TUT7 marks mRNA for degradation. Cell, 159(6), 1365–1376. https://doi.org/10.1016/j.cell.2014.10.055
Lin,, C. J., Wen,, J., Bejarano,, F., Hu,, F., Bortolamiol‐Becet,, D., Kan,, L., … Lai,, E. C. (2017). Characterization of a TUTase/RNase complex required for Drosophila gametogenesis. RNA, 23(3), 284–296. https://doi.org/10.1261/rna.059527.116
Liu,, N., Abe,, M., Sabin,, L. R., Hendriks,, G. J., Naqvi,, A. S., Yu,, Z., … Bonini,, N. M. (2011). The exoribonuclease Nibbler controls 3′ end processing of microRNAs in Drosophila. Current Biology, 21(22), 1888–1893. https://doi.org/10.1016/j.cub.2011.10.006
Londin,, E., Loher,, P., Telonis,, A. G., Quann,, K., Clark,, P., Jing,, Y., … Rigoutsos,, I. (2015). Analysis of 13 cell types reveals evidence for the expression of numerous novel primate‐ and tissue‐specific microRNAs. Proceedings of the National Academy of Sciences of the United States of America, 112(10), E1106–E1115. https://doi.org/10.1073/pnas.1420955112
Lowell,, J. E., Rudner,, D. Z., & Sachs,, A. B. (1992). 3`‐UTR‐dependent deadenylation by the yeast poly(a) nuclease. Genes %26 Development, 6(11), 2088–2099.
Lubas,, M., Damgaard,, C. K., Tomecki,, R., Cysewski,, D., Jensen,, T. H., & Dziembowski,, A. (2013). Exonuclease hDIS3L2 specifies an exosome‐independent 3′‐5′ degradation pathway of human cytoplasmic mRNA. EMBO Journal, 32(13), 1855–1868. https://doi.org/10.1038/emboj.2013.135
Makino,, D. L., Baumgartner,, M., & Conti,, E. (2013). Crystal structure of an RNA‐bound 11‐subunit eukaryotic exosome complex. Nature, 495(7439), 70–75. https://doi.org/10.1038/nature11870
Malecki,, M., Viegas,, S. C., Carneiro,, T., Golik,, P., Dressaire,, C., Ferreira,, M. G., & Arraiano,, C. M. (2013). The exoribonuclease Dis3L2 defines a novel eukaryotic RNA degradation pathway. EMBO Journal, 32(13), 1842–1854. https://doi.org/10.1038/emboj.2013.63
Malet,, H., Topf,, M., Clare,, D. K., Ebert,, J., Bonneau,, F., Basquin,, J., … Lorentzen,, E. (2010). RNA channelling by the eukaryotic exosome. EMBO Reports, 11(12), 936–942. https://doi.org/10.1038/embor.2010.164
Mamolen,, M., Smith,, A., & Andrulis,, E. D. (2010). Drosophila melanogaster Dis3 N‐terminal domains are required for ribonuclease activities, nuclear localization and exosome interactions. Nucleic Acids Research, 38(16), 5507–5517. https://doi.org/10.1093/nar/gkq295
Marin‐Vicente,, C., Domingo‐Prim,, J., Eberle,, A. B., & Visa,, N. (2015). RRP6/EXOSC10 is required for the repair of DNA double‐strand breaks by homologous recombination. Journal of Cell Science, 128(6), 1097–1107. https://doi.org/10.1242/jcs.158733
Maryati,, M., Airhihen,, B., & Winkler,, G. S. (2015). The enzyme activities of Caf1 and Ccr4 are both required for deadenylation by the human Ccr4–Not nuclease module. Biochemical Journal, 469(Pt 1), 169–176. https://doi.org/10.1042/bj20150304
Mitchell,, P., Petfalski,, E., Shevchenko,, A., Mann,, M., & Tollervey,, D. (1997). The exosome: A conserved eukaryotic RNA processing complex containing multiple 3′→5′ exoribonucleases. Cell, 91(4), 457–466.
Modepalli,, V., & Moran,, Y. (2017). Evolution of miRNA tailing by 3′ terminal uridylyl transferases in Metazoa. Genome Biology and Evolution, 9(6), 1547–1560. https://doi.org/10.1093/gbe/evx106
Molleston,, J. M., Sabin,, L. R., Moy,, R. H., Menghani,, S. V., Rausch,, K., Gordesky‐Gold,, B., … Cherry,, S. (2016). A conserved virus‐induced cytoplasmic TRAMP‐like complex recruits the exosome to target viral RNA for degradation. Genes %26 Development, 30(14), 1658–1670. https://doi.org/10.1101/gad.284604.116
Moon,, S. L., Dodd,, B. J., Brackney,, D. E., Wilusz,, C. J., Ebel,, G. D., & Wilusz,, J. (2015). Flavivirus sfRNA suppresses antiviral RNA interference in cultured cells and mosquitoes and directly interacts with the RNAi machinery. Virology, 485, 322–329. https://doi.org/10.1016/j.virol.2015.08.009
Morris,, M. R., Astuti,, D., & Maher,, E. R. (2013). Perlman syndrome: Overgrowth Wilms tumor predisposition and DIS3L2. American Journal of Medical Genetics. Part C, Seminars in Medical Genetics, 163C(2), 106–113. https://doi.org/10.1002/ajmg.c.31358
Mullen,, T. E., & Marzluff,, W. F. (2008). Degradation of histone mRNA requires oligouridylation followed by decapping and simultaneous degradation of the mRNA both 5′ to 3′ and 3′ to 5′. Genes %26 Development, 22(1), 50–65. https://doi.org/10.1101/gad.1622708
Murakami,, H., Goto,, D. B., Toda,, T., Chen,, E. S., Grewal,, S. I., Martienssen,, R. A., & Yanagida,, M. (2007). Ribonuclease activity of Dis3 is required for mitotic progression and provides a possible link between heterochromatin and kinetochore function. PLoS One, 2(3), e317. https://doi.org/10.1371/journal.pone.0000317
Murray,, E. L., & Schoenberg,, D. R. (2007). A+U‐rich instability elements differentially activate 5′‐3′ and 3′‐5` mRNA decay. Molecular and Cellular Biology, 27(8), 2791–2799. https://doi.org/10.1128/mcb.01445-06
Nagarajan,, V. K., Jones,, C. I., Newbury,, S. F., & Green,, P. J. (2013). XRN 5′‐‐%3E3′ exoribonucleases: Structure, mechanisms and functions. Biochimica et Biophysica Acta, 1829(6–7), 590–603. https://doi.org/10.1016/j.bbagrm.2013.03.005
Newbury,, S. F. (2006). Control of mRNA stability in eukaryotes. Biochemical Society Transactions, 34(Pt 1), 30–34. https://doi.org/10.1042/bst20060030
Ng,, D., Toure,, O., Wei,, M. H., Arthur,, D. C., Abbasi,, F., Fontaine,, L., … Toro,, J. R. (2007). Identification of a novel chromosome region, 13q21.33‐q22.2, for susceptibility genes in familial chronic lymphocytic leukemia. Blood, 109(3), 916–925. https://doi.org/10.1182/blood-2006-03-011825
Nishioka,, K., Wang,, X. F., Miyazaki,, H., Soejima,, H., & Hirose,, S. (2018). Mbf1 ensures polycomb silencing by protecting E(z) mRNA from degradation by Pacman. Development, 145(5), dev162461. https://doi.org/10.1242/dev.162461
Ohkura,, H., Adachi,, Y., Kinoshita,, N., Niwa,, O., Toda,, T., & Yanagida,, M. (1988). Cold‐sensitive and caffeine‐supersensitive mutants of the Schizosaccharomyces pombe dis genes implicated in sister chromatid separation during mitosis. EMBO Journal, 7(5), 1465–1473.
Okada,, H., Schittenhelm,, R. B., Straessle,, A., & Hafen,, E. (2015). Multi‐functional regulation of 4E‐BP gene expression by the Ccr4‐not complex. PLoS One, 10(3), e0113902. https://doi.org/10.1371/journal.pone.0113902
Orban,, T. I., & Izaurralde,, E. (2005). Decay of mRNAs targeted by RISC requires XRN1, the Ski complex, and the exosome. RNA, 11(4), 459–469. https://doi.org/10.1261/rna.7231505
Pandey,, U. B., & Nichols,, C. D. (2011). Human disease models in Drosophila melanogaster and the role of the fly in therapeutic drug discovery. Pharmacological Reviews, 63(2), 411–436. https://doi.org/10.1124/pr.110.003293
Park,, J.‐E., Yi,, H., Kim,, Y. J., Chang,, H., & Kim,, V. N. (2016). Regulation of poly(a) tail and translation during the somatic cell cycle. Molecular Cell, 62(3), 462–471. https://doi.org/10.1016/j.molcel.2016.04.007
Pashler,, A. L., Towler,, B. P., Jones,, C. I., & Newbury,, S. F. (2016). The roles of the exoribonucleases DIS3L2 and XRN1 in human disease. Biochemical Society Transactions, 44(5), 1377–1384. https://doi.org/10.1042/bst20160107
Peng,, S. S., Chen,, C. Y., Xu,, N., & Shyu,, A. B. (1998). RNA stabilization by the AU‐rich element binding protein, HuR, an ELAV protein. EMBO Journal, 17(12), 3461–3470. https://doi.org/10.1093/emboj/17.12.3461
Perez‐Ortin,, J. E., Alepuz,, P., Chavez,, S., & Choder,, M. (2013). Eukaryotic mRNA decay: Methodologies, pathways, and links to other stages of gene expression. Journal of Molecular Biology, 425(20), 3750–3775. https://doi.org/10.1016/j.jmb.2013.02.029
Pfeiffer,, B. D., Ngo,, T.‐T. B., Hibbard,, K. L., Murphy,, C., Jenett,, A., Truman,, J. W., & Rubin,, G. M. (2010). Refinement of tools for targeted gene expression in Drosophila. Genetics, 186(2), 735–755. https://doi.org/10.1534/genetics.110.119917
Pirouz,, M., Du,, P., Munafo,, M., & Gregory,, R. I. (2016). Dis3l2‐mediated decay is a quality control pathway for noncoding RNAs. Cell Reports, 16(7), 1861–1873. https://doi.org/10.1016/j.celrep.2016.07.025
Preker,, P., Nielsen,, J., Kammler,, S., Lykke‐Andersen,, S., Christensen,, M. S., Mapendano,, C. K., … Jensen,, T. H. (2008). RNA exosome depletion reveals transcription upstream of active human promoters. Science, 322(5909), 1851–1854. https://doi.org/10.1126/science.1164096
Presnyak,, V., Alhusaini,, N., Chen,, Y.‐H., Martin,, S., Morris,, N., Kline,, N., … Coller,, J. (2015). Codon optimality is a major determinant of mRNA stability. Cell, 160(6), 1111–1124. https://doi.org/10.1016/j.cell.2015.02.029
Rehwinkel,, J. A. N., Behm‐Ansmant,, I., Gatfield,, D., & Izaurralde,, E. (2005). A crucial role for GW182 and the DCP1:DCP2 decapping complex in miRNA‐mediated gene silencing. RNA, 11(11), 1640–1647. https://doi.org/10.1261/rna.2191905
Reimao‐Pinto,, M. M., Ignatova,, V., Burkard,, T. R., Hung,, J. H., Manzenreither,, R. A., Sowemimo,, I., … Ameres,, S. L. (2015). Uridylation of RNA hairpins by tailor confines the emergence of MicroRNAs in Drosophila. Molecular Cell, 59(2), 203–216. https://doi.org/10.1016/j.molcel.2015.05.033
Reimao‐Pinto,, M. M., Manzenreither,, R. A., Burkard,, T. R., Sledz,, P., Jinek,, M., Mechtler,, K., & Ameres,, S. L. (2016). Molecular basis for cytoplasmic RNA surveillance by uridylation‐triggered decay in Drosophila. EMBO Journal, 35(22), 2417–2434. https://doi.org/10.15252/embj.201695164
Reis,, F. P., Barbas,, A., Klauer‐King,, A. A., Tsanova,, B., Schaeffer,, D., López‐Viñas,, E., … Arraiano,, C. M. (2013). Modulating the RNA processing and decay by the exosome: Altering Rrp44/Dis3 activity and end‐product. PLoS One, 8(11), e76504. https://doi.org/10.1371/journal.pone.0076504
Reiter,, L. T., Potocki,, L., Chien,, S., Gribskov,, M., & Bier,, E. (2001). A systematic analysis of human disease‐associated gene sequences in Drosophila melanogaster. Genome Research, 11(6), 1114–1125. https://doi.org/10.1101/gr.169101
Rissland,, O. S., Mikulasova,, A., & Norbury,, C. J. (2007). Efficient RNA polyuridylation by noncanonical poly(a) polymerases. Molecular and Cellular Biology, 27(10), 3612–3624. https://doi.org/10.1128/mcb.02209-06
Rose,, A. E., Poliseno,, L., Wang,, J., Clark,, M., Pearlman,, A., Wang,, G., … Osman,, I. (2011). Integrative genomics identifies molecular alterations that challenge the linear model of melanoma progression. Cancer Research, 71(7), 2561–2571. https://doi.org/10.1158/0008-5472.can-10-2958
Russo,, J., Lee,, J. E., López,, C. M., Anderson,, J., Nguyen,, T. P., Heck,, A. M., … Wilusz,, C. J. (2017). The CELF1 RNA‐binding protein regulates decay of signal recognition particle mRNAs and limits secretion in mouse myoblasts. PLoS One, 12(1), e0170680. https://doi.org/10.1371/journal.pone.0170680
Schaeffer,, D., Reis,, F. P., Johnson,, S. J., Arraiano,, C. M., & van Hoof,, A. (2012). The CR3 motif of Rrp44p is important for interaction with the core exosome and exosome function. Nucleic Acids Research, 40(18), 9298–9307. https://doi.org/10.1093/nar/gks693
Schaeffer,, D., Tsanova,, B., Barbas,, A., Reis,, F. P., Dastidar,, E. G., Sanchez‐Rotunno,, M., … van Hoof,, A. (2009). The exosome contains domains with specific endoribonuclease, exoribonuclease and cytoplasmic mRNA decay activities. Nature Structural %26 Molecular Biology, 16(1), 56–62. https://doi.org/10.1038/nsmb.1528
Schaeffer,, D., & van Hoof,, A. (2011). Different nuclease requirements for exosome‐mediated degradation of normal and nonstop mRNAs. Proceedings of the National Academy of Sciences of the United States of America, 108(6), 2366–2371. https://doi.org/10.1073/pnas.1013180108
Schertel,, C., Rutishauser,, T., Förstemann,, K., & Basler,, K. (2012). Functional characterization of Drosophila microRNAs by a novel in vivo library. Genetics, 192(4), 1543–1552.
Schneider,, C., Anderson,, J. T., & Tollervey,, D. (2007). The exosome subunit Rrp44 plays a direct role in RNA substrate recognition. Molecular Cell, 27(2), 324–331. https://doi.org/10.1016/j.molcel.2007.06.006
Schneider,, C., Kudla,, G., Wlotzka,, W., Tuck,, A., & Tollervey,, D. (2012). Transcriptome‐wide analysis of exosome targets. Molecular Cell, 48(3–3), 422–433. https://doi.org/10.1016/j.molcel.2012.08.013
Schneider,, C., Leung,, E., Brown,, J., & Tollervey,, D. (2009). The N‐terminal PIN domain of the exosome subunit Rrp44 harbors endonuclease activity and tethers Rrp44 to the yeast core exosome. Nucleic Acids Research, 37(4), 1127–1140. https://doi.org/10.1093/nar/gkn1020
Schoenberg,, D. R., & Maquat,, L. E. (2012). Regulation of cytoplasmic mRNA decay. Nature Reviews. Genetics, 13(4), 246–259. https://doi.org/10.1038/nrg3160
Sharif,, H., & Conti,, E. (2013). Architecture of the Lsm1‐7‐Pat1 complex: A conserved assembly in eukaryotic mRNA turnover. Cell Reports, 5(2), 283–291. https://doi.org/10.1016/j.celrep.2013.10.004
Sinturel,, F., Brechemier‐Baey,, D., Kiledjian,, M., Condon,, C., & Benard,, L. (2012). Activation of 5′‐3′ exoribonuclease Xrn1 by cofactor Dcs1 is essential for mitochondrial function in yeast. Proceedings of the National Academy of Sciences of the United States of America, 109(21), 8264–8269. https://doi.org/10.1073/pnas.1120090109
Smith,, S. B., Kiss,, D. L., Turk,, E., Tartakoff,, A. M., & Andrulis,, E. D. (2011). Pronounced and extensive microtubule defects in a Saccharomyces cerevisiae DIS3 mutant. Yeast, 28(11), 755–769. https://doi.org/10.1002/yea.1899
Snee,, M. J., Wilson,, W. C., Zhu,, Y., Chen,, S. Y., Wilson,, B. A., Kseib,, C., … Skeath,, J. B. (2016). Collaborative control of cell cycle progression by the RNA exonuclease Dis3 and Ras is conserved across species. Genetics, 203(2), 749–762. https://doi.org/10.1534/genetics.116.187930
Spasic,, M., Friedel,, C. C., Schott,, J., Kreth,, J., Leppek,, K., Hofmann,, S., … Stoecklin,, G. (2012). Genome‐wide assessment of AU‐rich elements by the AREScore algorithm. PLoS Genetics, 8(1), e1002433. https://doi.org/10.1371/journal.pgen.1002433
Staals,, R. H. J., Bronkhorst,, A. W., Schilders,, G., Slomovic,, S., Schuster,, G., Heck,, A. J. R., … Pruijn,, G. J. M. (2010). Dis3‐like 1: A novel exoribonuclease associated with the human exosome. The EMBO Journal, 29(14), 2358–2367. https://doi.org/10.1038/emboj.2010.122
Steinbrunn,, T., Stuhmer,, T., Gattenlohner,, S., Rosenwald,, A., Mottok,, A., Unzicker,, C., … Bargou,, R. C. (2011). Mutated RAS and constitutively activated Akt delineate distinct oncogenic pathways, which independently contribute to multiple myeloma cell survival. Blood, 117(6), 1998–2004. https://doi.org/10.1182/blood-2010-05-284422
Suh,, Y. S., Bhat,, S., Hong,, S. H., Shin,, M., Bahk,, S., Cho,, K. S., … Yu,, K. (2015). Genome‐wide microRNA screening reveals that the evolutionary conserved miR‐9a regulates body growth by targeting sNPFR1/NPYR. Nature Communications, 6, 7693. https://doi.org/10.1038/ncomms8693
Synowsky,, S. A., van Wijk,, M., Raijmakers,, R., & Heck,, A. J. (2009). Comparative multiplexed mass spectrometric analyses of endogenously expressed yeast nuclear and cytoplasmic exosomes. Journal of Molecular Biology, 385(4), 1300–1313. https://doi.org/10.1016/j.jmb.2008.11.011
Temme,, C., Simonelig,, M., & Wahle,, E. (2014). Deadenylation of mRNA by the CCR4‐NOT complex in Drosophila: Molecular and developmental aspects. Frontiers in Genetics, 5, 143. https://doi.org/10.3389/fgene.2014.00143
Temme,, C., Zhang,, L., Kremmer,, E., Ihling,, C., Chartier,, A., Sinz,, A., … Wahle,, E. (2010). Subunits of the Drosophila CCR4‐NOT complex and their roles in mRNA deadenylation. RNA, 16(7), 1356–1370. https://doi.org/10.1261/rna.2145110
Tharun,, S. (2009). Lsm1‐7‐Pat1 complex: A link between 3′ and 5′‐ends in mRNA decay? RNA Biology, 6(3), 228–232.
Thomas,, M. P., Liu,, X., Whangbo,, J., McCrossan,, G., Sanborn,, K. B., Basar,, E., … Lieberman,, J. (2015). Apoptosis triggers specific, rapid, and global mRNA decay with 3′ Uridylated intermediates degraded by DIS3L2, Apoptosis triggers specific, rapid, and global mRNA decay with 3′ Uridylated intermediates degraded by DIS3L2. Cell Reports, 11(7), 1079–1089. https://doi.org/10.1016/j.celrep.2015.04.026
Till,, D. D., Linz,, B., Seago,, J. E., Elgar,, S. J., Marujo,, P. E., de Lourdes Elias,, M., … Newbury,, S. F. (1998). Identification and developmental expression of a 5′–3′ exoribonuclease from Drosophila melanogaster. Mechanisms of Development, 79(1), 51–55. https://doi.org/10.1016/S0925-4773(98)00173-7
Tomari,, Y., Du,, T., & Zamore,, P. D. (2007). Sorting of Drosophila small silencing RNAs. Cell, 130(2), 299–308. https://doi.org/10.1016/j.cell.2007.05.057
Tomecki,, R., Drazkowska,, K., Kucinski,, I., Stodus,, K., Szczesny,, R. J., Gruchota,, J., … Dziembowski,, A. (2014). Multiple myeloma‐associated hDIS3 mutations cause perturbations in cellular RNA metabolism and suggest hDIS3 PIN domain as a potential drug target. Nucleic Acids Research, 42(2), 1270–1290. https://doi.org/10.1093/nar/gkt930
Tomecki,, R., Kristiansen,, M. S., Lykke‐Andersen,, S., Chlebowski,, A., Larsen,, K. M., Szczesny,, R. J., … Jensen,, T. H. (2010). The human core exosome interacts with differentially localized processive RNases: hDIS3 and hDIS3L. EMBO Journal, 29(14), 2342–2357. https://doi.org/10.1038/emboj.2010.121
Towler,, B. P., Jones,, C. I., Harper,, K. L., Waldron,, J. A., & Newbury,, S. F. (2016). A novel role for the 3′‐5′ exoribonuclease Dis3L2 in controlling cell proliferation and tissue growth. RNA Biology, 13(12), 1286–1299.
Towler,, B. P., Jones,, C. I., & Newbury,, S. F. (2015). Mechanisms of regulation of mature miRNAs. Biochemical Society Transactions, 43(6), 1208–1214. https://doi.org/10.1042/bst20150157
Towler,, B. P., Jones,, C. I., Viegas,, S. C., Apura,, P., Waldron,, J. A., Smalley,, S. K., … Newbury,, S. F. (2015). The 3′‐5′ exoribonuclease Dis3 regulates the expression of specific microRNAs in Drosophila wing imaginal discs. RNA Biology, 12(7), 728–741. https://doi.org/10.1080/15476286.2015.1040978
Ustianenko,, D., Hrossova,, D., Potesil,, D., Chalupnikova,, K., Hrazdilova,, K., Pachernik,, J., … Vanacova,, S. (2013). Mammalian DIS3L2 exoribonuclease targets the uridylated precursors of let‐7 miRNAs. RNA, 19(12), 1632–1638. https://doi.org/10.1261/rna.040055.113
Vallejo,, D. M., Caparros,, E., & Dominguez,, M. (2011). Targeting Notch signalling by the conserved miR‐8/200 microRNA family in development and cancer cells. The EMBO Journal, 30(4), 756–769. https://doi.org/10.1038/emboj.2010.358
Vindry,, C., Lauwers,, A., Hutin,, D., Soin,, R., Wauquier,, C., Kruys,, V., & Gueydan,, C. (2012). dTIS11 protein‐dependent polysomal deadenylation is the key step in AU‐rich element‐mediated mRNA decay in Drosophila cells. The Journal of Biological Chemistry, 287(42), 35527–35538. https://doi.org/10.1074/jbc.M112.356188
Wahle,, E., & Winkler,, G. S. (2013). RNA decay machines: Deadenylation by the Ccr4‐not and Pan2‐Pan3 complexes. Biochimica et Biophysica Acta, 1829(6–7), 561–570. https://doi.org/10.1016/j.bbagrm.2013.01.003
Waldron,, J. A., Jones,, C. I., Towler,, B. P., Pashler,, A. L., Grima,, D. P., Hebbes,, S., … Newbury,, S. F. (2015). Xrn1/Pacman affects apoptosis and regulates expression of hid and reaper. Biology Open, 4(5), 649–660. https://doi.org/10.1242/bio.201410199
Wan,, J., Yourshaw,, M., Mamsa,, H., Rudnik‐Schoneborn,, S., Menezes,, M. P., Hong,, J. E., … Jen,, J. C. (2012). Mutations in the RNA exosome component gene EXOSC3 cause pontocerebellar hypoplasia and spinal motor neuron degeneration. Nature Genetics, 44(6), 704–708. https://doi.org/10.1038/ng.2254
Wasmuth,, E. V., & Lima,, C. D. (2012). Exo‐ and endoribonucleolytic activities of yeast cytoplasmic and nuclear RNA exosomes are dependent on the noncatalytic core and central channel. Molecular Cell, 48(1), 133–144. https://doi.org/10.1016/j.molcel.2012.07.012
Wei,, Y., Xiao,, Q., Zhang,, T., Mou,, Z., You,, J., & Ma,, W.‐J. (2009). Differential regulation of mRNA stability controls the transient expression of genes encoding Drosophila antimicrobial peptide with distinct immune response characteristics. Nucleic Acids Research, 37(19), 6550–6561. https://doi.org/10.1093/nar/gkp693
Wells,, S. E., Hillner,, P. E., Vale,, R. D., & Sachs,, A. B. (1998). Circularization of mRNA by eukaryotic translation initiation factors. Molecular Cell, 2(1), 135–140.
Wolf,, J., & Passmore,, L. A. (2014). mRNA Deadenylation by Pan2/Pan3. Biochemical Society Transactions, 42(1), 184–187.
Wyers,, F., Rougemaille,, M., Badis,, G., Rousselle,, J. C., Dufour,, M. E., Boulay,, J., … Jacquier,, A. (2005). Cryptic pol II transcripts are degraded by a nuclear quality control pathway involving a new poly(A) polymerase. Cell, 121(5), 725–737. https://doi.org/10.1016/j.cell.2005.04.030
Wyman,, S. K., Knouf,, E. C., Parkin,, R. K., Fritz,, B. R., Lin,, D. W., Dennis,, L. M., … Tewari,, M. (2011). Post‐transcriptional generation of miRNA variants by multiple nucleotidyl transferases contributes to miRNA transcriptome complexity. Genome Research, 21(9), 1450–1461. https://doi.org/10.1101/gr.118059.110
Yamashita,, A., Chang,, T. C., Yamashita,, Y., Zhu,, W., Zhong,, Z., Chen,, C. Y., & Shyu,, A. B. (2005). Concerted action of poly(A) nucleases and decapping enzyme in mammalian mRNA turnover. Nature Structural %26 Molecular Biology, 12(12), 1054–1063. https://doi.org/10.1038/nsmb1016
Zabolotskaya,, M. V., Grima,, D. P., Lin,, M. D., Chou,, T. B., & Newbury,, S. F. (2008). The 5′‐3′ exoribonuclease Pacman is required for normal male fertility and is dynamically localized in cytoplasmic particles in Drosophila testis cells. The Biochemical Journal, 416(3), 327–335. https://doi.org/10.1042/bj20071720
Zhang,, K., Dion,, N., Fuchs,, B., Damron,, T., Gitelis,, S., Irwin,, R., … Sarkar,, G. (2002). The human homolog of yeast SEP1 is a novel candidate tumor suppressor gene in osteogenic sarcoma. Gene, 298(2), 121–127.

Access to this WIREs title is by subscription only.

Recommend to Your
Librarian Now!

Regulation of cytoplasmic RNA stability: Lessons from Drosophila

Browse by Topic

Access to this WIREs title is by subscription only.

The latest WIREs articles in your inbox