The 3’-5’ exoribonuclease Dis3 regulates the expression of specific microRNAs in Drosophila wing imaginal discs

RNA Biology

Volumn 12, Issue 7, 2015, Pages 728-741

  Towler, Benjamin P ^a   Jones, Christopher I ^a   Viegas, Sandra C ^b   Apura, Patricia ^b   Waldron, Joseph A ^a   Smalley, Sarah K ^a   Arraiano, Cecilia M ^b   Newbury, Sarah F ^a  

^a UNIVERSITY OF SUSSEX   (United Kingdom)

^b INSTITUTO DE TECNOLOGIA QUÍMICA E BIOLÓGICA   (Portugal)

Author keywords

Dis3 Taz; Drosophila development; Exoribonuclease; Imaginal discs; MiRNAs; RNA degradation; RNA stability

Indexed keywords

DROSOPHILA PROTEIN; EXORIBONUCLEASE; MICRORNA; PROTEIN DIS3; UNCLASSIFIED DRUG; DIS3 PROTEIN, DROSOPHILA; EXOSOME MULTIENZYME RIBONUCLEASE COMPLEX; TRANSCRIPTOME;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOPLASM; DROSOPHILA; FORELIMB; GENE EXPRESSION; GENE SILENCING; IMAGINAL DISC; INSECT DEVELOPMENT; LARVAL DEVELOPMENT; NONHUMAN; PHENOTYPE; RNA DEGRADATION; RNA SEQUENCE; ANIMAL; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; SEQUENCE ANALYSIS; TRIBOLIUM; WING;

ANIMALS; DROSOPHILA; DROSOPHILA PROTEINS; EXORIBONUCLEASES; EXOSOME MULTIENZYME RIBONUCLEASE COMPLEX; GENE KNOCKDOWN TECHNIQUES; IMAGINAL DISCS; MICRORNAS; SEQUENCE ANALYSIS, RNA; TRANSCRIPTOME; TRIBOLIUM; WINGS, ANIMAL;

EID: 84944449003     PISSN: 15476286     EISSN: 15558584     Source Type: Journal    
DOI: 10.1080/15476286.2015.1040978     Document Type: Article

References (53)

1. Jones CI, Zabolotskaya MV, Newbury SF. The 5′ ->3′ exoribonuclease XRN1/Pacman and its functions in cellular processes and development. Wiley Interdiscip Rev RNA 2012; 3:455-68; PMID:22383165; http://dx.doi.org/10.1002/wrna.1109.
2. Arraiano CM, Mauxion F, Viegas SC, Matos RG, Seraphin B. Intracellular ribonucleases involved in transcript processing and decay: precision tools for RNA. Biochim Biophys Acta 2013; 1829:491-513; PMID:23545199; http://dx.doi.org/10.1016/j.bbagrm.2013.03.009.
3. Reis FP, Pobre V, Silva IJ, Malecki M, Arraiano CM. The RNase II/RNB family of exoribonucleases: putting the 'Dis' in disease. Wiley Interdiscip Rev RNA 2013; 4:607-15; PMID:23776156; http://dx.doi.org/10.1002/wrna.1180.
4. Jones CI, Newbury SF. Functions of microRNAs in Drosophila development. Biochem Soc Trans 2010;38:1137-43; PMID:20659018; http://dx.doi.org/10.1042/BST0381137.
5. Jones CI, Grima DP, Waldron JA, Jones S, Parker HN, Newbury SF. 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 Biol 2013; 10:1345-55; PMID:23792537; http://dx.doi.org/10.4161/rna.25354.
6. Waldron JA, Jones CI, Towler BP, Pashler AL, Grima DP, Hebbes DP, Crossman SH, Zabolotskaya MV, Newbury SF. Xrn/Pacman affects apoptosis and regulates expression of hid and reaper. Biol Open. 2015 Apr 2. pii: BIO201410199. doi:10.1242/bio.201410199. [Epub ahead of print]
7. Cairrao F, Arraiano C, Newbury S. Drosophila gene tazman, an orthologue of the yeast exosome component Rrp44p/Dis3, is differentially expressed during development. Dev Dyn 2005; 232:733-7; PMID:15704111; http://dx.doi.org/10.1002/dvdy.20269.
8. Malecki M, Viegas SC, Carneiro T, Golik P, Dressaire C, Ferreira MG, Arraiano CM. The exoribonuclease Dis3L2 defines a novel eukaryotic RNA degradation pathway. EMBO J 2013; 32:1842-54; PMID:23503588; http://dx.doi.org/10.1038/emboj.2013.63.
9. Mitchell P, Petfalski E, Shevchenko A, Mann M, Tollervey D. The exosome: a conserved eukaryotic RNA processing complex containing multiple 3′-5′ exoribonucleases. Cell 1997; 91:457-66; PMID:9390555; http://dx.doi.org/10.1016/S0092-8674(00)80432-8.
10. Halbach F, Reichelt P, Rode M, Conti E. The yeast ski complex: crystal structure and RNA channeling to the exosome complex. Cell 2013; 154:814-26; PMID:23953113; http://dx.doi.org/10.1016/j.cell.2013.07.017.
11. Tomecki R, Kristiansen MS, Lykke-Andersen S, Chlebowski A, Larsen KM, Szczesny RJ, Drazkowska K, Pastula A, Andersen JS, Stepien PP, et al. The human core exosome interacts with differentially localized processive RNases: hDIS3 and hDIS3L. EMBO J 2010; 29:2342-57; PMID:20531386; http://dx.doi.org/10.1038/emboj.2010.121.
12. Staals RH, Bronkhorst AW, Schilders G, Slomovic S, Schuster G, Heck AJ, Raijmakers R, Pruijn GJ. Dis3-like 1: a novel exoribonuclease associated with the human exosome. EMBO J 2010; 29:2358-67; PMID:20531389; http://dx.doi.org/10.1038/emboj.2010.122.
13. Schneider C, Leung E, Brown J, Tollervey D. The N-terminal PIN domain of the exosome subunit Rrp44 harbors endonuclease activity and tethers Rrp44 to the yeast core exosome. Nucleic Acids Res 2009; 37:1127-40; PMID:19129231; http://dx.doi.org/10.1093/nar/gkn1020.
14. Schaeffer D, Reis FP, Johnson SJ, Arraiano CM, van Hoof A. The CR3 motif of Rrp44p is important for interaction with the core exosome and exosome function. Nucleic Acids Res 2012; 40:9298-307; PMID:22833611; http://dx.doi.org/10.1093/nar/gks693.
15. Schaeffer D, Tsanova B, Barbas A, Reis FP, Dastidar EG, Sanchez-Rotunno M, Arraiano CM, van Hoof A. The exosome contains domains with specific endoribonuclease, exoribonuclease and cytoplasmic mRNA decay activities. Nat Struct Mol Biol 2009; 16:56-62; PMID:19060898; http://dx.doi.org/10.1038/nsmb.1528.
16. Chang HM, Triboulet R, Thornton JE, Gregory RI. A role for the Perlman syndrome exonuclease Dis3l2 in the Lin28-let-7 pathway. Nature 2013; 497:244-8; PMID:23594738; http://dx.doi.org/10.1038/nature12119.
17. Lubas M, Damgaard CK, Tomecki R, Cysewski D, Jensen TH, Dziembowski A. Exonuclease hDIS3L2 specifies an exosome-independent 3′-5′ degradation pathway of human cytoplasmic mRNA. EMBO J 2013; 32:1855-68; PMID:23756462; http://dx.doi.org/10.1038/emboj.2013.135.
18. Ustianenko D, Hrossova D, Potesil D, Chalupnikova K, Hrazdilova K, Pachernik J, Cetkovska K, Uldrijan S, Zdrahal Z, Vanacova S. Mammalian DIS3L2 exoribonuclease targets the uridylated precursors of let-7 miRNAs. RNA 2013; 19:1632-8; PMID:24141620; http://dx.doi.org/10.1261/rna.040055.113.
19. Graham AC, Davis SM, Andrulis ED. Interdependent nucleocytoplasmic trafficking and interactions of Dis3 with Rrp6, the core exosome and importin-alpha3. Traffic 2009; 10:499-513; PMID:19220816; http://dx.doi.org/10.1111/j.1600-0854.2009.00888.x.
20. Mamolen M, Smith A, Andrulis ED. Drosophila melanogaster Dis3 N-terminal domains are required for ribonuclease activities, nuclear localization and exosome interactions. Nucleic Acids Res 2010; 38:5507-17; PMID:20421210; http://dx.doi.org/10.1093/nar/gkq295.
21. Chlebowski A, Lubas M, Jensen TH, Dziembowski A. RNA decay machines: the exosome. Biochim Biophys Acta 2013; 1829:552-60; PMID:23352926; http://dx.doi.org/10.1016/j.bbagrm.2013.01.006.
22. Gudipati RK, Xu Z, Lebreton A, Seraphin B, Steinmetz LM, Jacquier A, Libri D. Extensive degradation of RNA precursors by the exosome in wild-type cells. Mol Cell 2012; 48:409-21; PMID:23000176; http://dx.doi.org/10.1016/j.molcel.2012.08.018.
23. Sloan KE, Schneider C, Watkins NJ. Comparison of the yeast and human nuclear exosome complexes. Biochem Soc Trans 2012; 40:850-5; PMID:22817747; http://dx.doi.org/10.1042/BST20120061.
24. Tomecki R, Drazkowska K, Kucinski I, Stodus K, Szczesny RJ, Gruchota J, Owczarek EP, Kalisiak K, Dziembowski A. Multiple myeloma-associated hDIS3 mutations cause perturbations in cellular RNA metabolism and suggest hDIS3 PIN domain as a potential drug target. Nucleic Acids Res 2014; 42:1270-90; PMID:24150935; http://dx.doi.org/10.1093/nar/gkt930.
25. Chapman MA, Lawrence MS, Keats JJ, Cibulskis K, Sougnez C, Schinzel AC, Harview CL, Brunet JP, Ahmann GJ, Adli M, et al. Initial genome sequencing and analysis of multiple myeloma. Nature 2011; 471:467-72; PMID:21430775; http://dx.doi.org/10.1038/nature09837.
26. Ding L, Ley TJ, Larson DE, Miller CA, Koboldt DC, Welch JS, Ritchey JK, Young MA, Lamprecht T, McLellan MD, et al. Clonal evolution in relapsed acute myeloid leukaemia revealed by whole-genome sequencing. Nature 2012; 481:506-10; PMID:22237025; http://dx.doi.org/10.1038/nature10738.
27. Parsons DW, Li M, Zhang X, Jones S, Leary RJ, Lin JC, Boca SM, Carter H, Samayoa J, Bettegowda C, et al. The genetic landscape of the childhood cancer medulloblastoma. Science 2011; 331:435-9; PMID:21163964; http://dx.doi.org/10.1126/science.1198056.
28. Rose AE, Poliseno L, Wang J, Clark M, Pearlman A, Wang G, Vega Y Saenz de Miera EC, Medicherla R, Christos PJ, Shapiro R, et al. Integrative genomics identifies molecular alterations that challenge the linear model of melanoma progression. Cancer Res 2011; 71:2561-71; PMID:21343389; http://dx.doi.org/10.1158/0008-5472.CAN-10-2958.
29. Liu X, Zheng Q, Vrettos N, Maragkakis M, Alexiou P, Gregory BD, Mourelatos Z. A MicroRNA precursor surveillance system in quality control of MicroRNA synthesis. Mol Cell 2014; 55:868-79; PMID:25175028; http://dx.doi.org/10.1016/j.molcel.2014.07.017.
30. Flynt AS, Greimann JC, Chung WJ, Lima CD, Lai EC. MicroRNA biogenesis via splicing and exosome-mediated trimming in Drosophila. Mol cell 2010; 38:900-7; PMID:20620959; http://dx.doi.org/10.1016/j.molcel.2010.06.014.
31. Hou D, Ruiz M, Andrulis ED. The ribonuclease Dis3 is an essential regulator of the developmental transcriptome. BMC Genomics 2012; 13:359; PMID:22853036; http://dx.doi.org/10.1186/1471-2164-13-359.
32. Kiss DL, Andrulis ED. Genome-wide analysis reveals distinct substrate specificities of Rrp6, Dis3, and core exosome subunits. RNA 2010; 16:781-91; PMID:20185544; http://dx.doi.org/10.1261/rna.1906710.
33. Dos Santos G, Schroeder AJ, Goodman JL, Strelets VB, Crosby MA, Thurmond J, Emmert DB, Gelbart WM; the FlyBase Consortium. (2015) FlyBase: introduction of the Drosophila melanogaster Release 6 reference genome assembly and large-scale migration of genome annotations. Nucleic Acids Res. http://dx.doi.org/10.1093/nar/gku1099
34. Friedlander MR, Chen W, Adamidi C, Maaskola J, Einspanier R, Knespel S, Rajewsky N. Discovering microRNAs from deep sequencing data using miRDeep. Nat Biotechnol 2008; 26:407-15; PMID:18392026; http://dx.doi.org/10.1038/nbt1394.
35. Graham AC, Kiss DL, Andrulis ED. Differential distribution of exosome subunits at the nuclear lamina and in cytoplasmic foci. Mol Biol Cell 2006; 17:1399-409; PMID:16407406; http://dx.doi.org/10.1091/mbc.E05-08-0805.
36. Bejarano F, Bortolamiol-Becet D, Dai Q, Sun K, Saj A, Chou YT, Raleigh DR, Kim K, Ni JQ, Duan H, et al. A genome-wide transgenic resource for conditional expression of Drosophila microRNAs. Development 2012; 139:2821-31; PMID:22745315; http://dx.doi.org/10.1242/dev.079939.
37. Schertel C, Rutishauser T, Forstemann K, Basler K. Functional characterization of Drosophila microRNAs by a novel in vivo library. Genetics 2012; 192:1543-52; PMID:23051640; http://dx.doi.org/10.1534/genetics.112.145383.
38. Lee M, Choi Y, Kim K, Jin H, Lim J, Nguyen TA, Yang J, Jeong M, Giraldez AJ, Yang H, et al. Adenylation of maternally inherited microRNAs by Wispy. Mol cell 2014; 56:696-707; PMID:25454948; http://dx.doi.org/10.1016/j.molcel.2014.10.011.
39. Han BW, Hung JH, Weng Z, Zamore PD, Ameres SL. The 3′-to-5′ exoribonuclease Nibbler shapes the 3′ ends of microRNAs bound to Drosophila Argonaute1. Curr Biol 2011; 21:1878-87; PMID:22055293; http://dx.doi.org/10.1016/j.cub.2011.09.034.
40. Chatterjee S, Grosshans H. Active turnover modulates mature microRNA activity in Caenorhabditis elegans. Nature 2009; 461:546-9; PMID:19734881; http://dx.doi.org/10.1038/nature08349.
41. Fatica A, Bozzoni I. Long non-coding RNAs: new players in cell differentiation and development. Nat Rev Genet 2014; 15:7-21; PMID:24296535; http://dx.doi.org/10.1038/nrg3606.
42. Forstemann K, Tomari Y, Du T, Vagin VV, Denli AM, Bratu DP, Klattenhoff C, Theurkauf WE, Zamore PD. Normal microRNA maturation and germ-line stem cell maintenance requires Loquacious, a doublestranded RNA-binding domain protein. PLoS Biol 2005; 3:e236; PMID:15918770; http://dx.doi.org/10.1371/journal.pbio.0030236.
43. Michlewski G, Guil S, Caceres JF. Stimulation of primiR-18a processing by hnRNP A1. Adv Exp Med Biol 2010; 700:28-35; PMID:21627027; http://dx.doi.org/10.1007/978-1-4419-7823-3_3.
44. Liu N, Abe M, Sabin LR, Hendriks GJ, Naqvi AS, Yu Z, Cherry S, Bonini NM. The exoribonuclease Nibbler controls 3′ end processing of microRNAs in Drosophila. Curr Biol 2011; 21:1888-93; PMID:22055292; http://dx.doi.org/10.1016/j.cub.2011.10.006.
45. Sullivan W, Ashburner A, Hawley RS. Drosophila Protocols. New York, USA: Cold Spring Harbor Laboratory Press, 2000.
46. Chen C, Khaleel SS, Huang H, Wu CH. Software for pre-processing Illumina next-generation sequencing short read sequences. Source code for biology and medicine 2014; 9:8; PMID:24955109; http://dx.doi.org/10.1186/1751-0473-9-8.
47. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods 2012; 9:357-9; PMID:22388286; http://dx.doi.org/10.1038/nmeth.1923.
48. Stark A, Brennecke J, Russell RB, Cohen SM. Identification of Drosophila MicroRNA targets. PLoS Biol 2003; 1:E60; PMID:14691535; http://dx.doi.org/10.1371/journal.pbio.0000060.
49. Esslinger SM, Schwalb B, Helfer S, Michalik KM, Witte H, Maier KC, Martin D, Michalke B, Tresch A, Cramer P, et al. Drosophila miR-277 controls branched-chain amino acid catabolism and affects lifespan. RNA Biol 2013; 10:1042-56; PMID:23669073; http://dx.doi.org/10.4161/rna.24810.
50. Marrone AK, Edeleva EV, Kucherenko MM, Hsiao NH, Shcherbata HR. Dg-Dys-Syn1 signaling in Drosophila regulates the microRNA profile. BMC Cell Biol 2012; 13:26; PMID:23107381; http://dx.doi.org/10.1186/1471-2121-13-26.
51. Vlachos IS, Paraskevopoulou MD, Karagkouni D, Georgakilas G, Vergoulis T, Kanellos I, Anastasopoulos IL, Maniou S, Karathanou K, Kalfakakou D, et al. DIANA-TarBase v7.0: indexing more than half a million experimentally supported miRNA:mRNA interactions. Nucleic Acids Res 2015; 43:D153-9; PMID:25416803; http://dx.doi.org/10.1093/nar/gku1215.
52. Liu N, Landreh M, Cao K, Abe M, Hendriks GJ, Kennerdell JR, Zhu Y, Wang LS, Bonini NM. The micro-RNA miR-34 modulates ageing and neurodegeneration in Drosophila. Nature 2012; 482:519-23; PMID:22343898; http://dx.doi.org/10.1038/nature10810.
53. Yamamoto A, Zwarts L, Callaerts P, Norga K, Mackay TF, Anholt RR. Neurogenetic networks for startleinduced locomotion in Drosophila melanogaster. Proc Natl Acad Sci U S A 2008; 105:12393-8; PMID:18713854; http://dx.doi.org/10.1093/nar/gku109910.1073/pnas.0804889105.