Genome-wide analysis reveals distinct substrate specificities of Rrp6, Dis3, and core exosome subunits

RNA

Volumn 16, Issue 4, 2010, Pages 781-791

  Kiss, Daniel L ^a   Andrulis, Erik D ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Core exosome; Dis3; mRNA turnover; NMD; RNase; Rrp6; UTR

Indexed keywords

DIS3 EXONUCLEASE; EXONUCLEASE; MESSENGER RNA; PROTEIN SUBUNIT; RRP6 EXONUCLEASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL NUCLEUS; CELL PROLIFERATION; CONTROLLED STUDY; CYTOPLASM; DEPLETION; DNA MICROARRAY; DROSOPHILA MELANOGASTER; ENZYME SPECIFICITY; EXOSOME; GENE; GENE EXPRESSION; GENETIC TRANSCRIPTION; GENOME ANALYSIS; METABOLISM; NONHUMAN; NUCLEUS ACCUMBENS; PRIORITY JOURNAL; RNA INTERFERENCE; TISSUE CULTURE CELL;

ANIMALS; CELLS, CULTURED; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GENOME, INSECT; GENOME-WIDE ASSOCIATION STUDY; RIBONUCLEASES; RNA INTERFERENCE; RNA, MESSENGER; RNA, SMALL INTERFERING; SUBSTRATE SPECIFICITY;

DROSOPHILA MELANOGASTER;

EID: 77950244851     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.1906710     Document Type: Article

References (45)

1. Allmang C, Kufel J, Chanfreau G, Mitchell P, Petfalski E, Tollervey D. 1999a. Functions of the exosome in rRNA, snoRNA and snRNA synthesis. EMBO J 18: 5399-5410.
2. Allmang C, Petfalski E, Podtelejnikov A, Mann M, Tollervey D, Mitchell P. 1999b. The yeast exosome and human PM-Scl are related complexes of 3′→5′ exonucleases. Genes & Dev 13: 2148-2158.
3. Allmang C, Mitchell P, Petfalski E, Tollervey D. 2000. Degradation of ribosomal RNA precursors by the exosome. Nucleic Acids Res 28: 1684-1691.
4. Anderson JR, Mukherjee D, Muthukumaraswamy K, Moraes KC, Wilusz CJ, Wilusz J. 2006. Sequence-specific RNA binding mediated by the RNase PH domain of components of the exosome. RNA 12: 1810-1816.
5. Andrulis ED, Werner J, Nazarian A, Erdjument-Bromage H, Tempst P, Lis JT. 2002. The RNA processing exosome is linked to elongating RNA polymerase II in Drosophila. Nature 420: 837-841.
6. Blattner J, Clayton CE. 1995. The 3′-untranslated regions from the Trypanosoma brucei phosphoglycerate kinase-encoding genes mediate developmental regulation. Gene 162: 153-156.
7. Bousquet-Antonelli C, Presutti C, Tollervey D. 2000. Identification of a regulated pathway for nuclear pre-mRNA turnover. Cell 102: 765-775.
8. Buttner K, Wenig K, Hopfner KP. 2005. Structural framework for the mechanism of archaeal exosomes in RNA processing. Mol Cell 20: 461-471.
9. Callahan KP, Butler JS. 2008. Evidence for core exosome independent function of the nuclear exoribonuclease Rrp6p. Nucleic Acids Res 36: 6645-6655.
10. Chekanova JA, Gregory BD, Reverdatto SV, Chen H, Kumar R, Hooker T, Yazaki J, Li P, Skiba N, Peng Q, et al. 2007. Genome-wide high-resolution mapping of exosome substrates reveals hidden features in the Arabidopsis transcriptome. Cell 131: 1340-1353.
11. Chen CY, Gherzi R, Ong SE, Chan EL, Raijmakers R, Pruijn GJ, Stoecklin G, Moroni C, Mann M, Karin M. 2001. AU binding proteins recruit the exosome to degrade ARE-containing mRNAs. Cell 107: 451-464.
12. Colasante C, Robles A, Li CH, Schwede A, Benz C, Voncken F, Guilbride DL, Clayton C. 2007. Regulated expression of glycosomal phosphoglycerate kinase in Trypanosoma brucei. Mol Biochem Parasitol 151: 193-204.
13. Das B, Butler JS, Sherman F. 2003. Degradation of normal mRNA in the nucleus of Saccharomyces cerevisiae. Mol Cell Biol 23: 5502-5515.
14. Dziembowski A, Lorentzen E, Conti E, Seraphin B. 2007. A single subunit, Dis3, is essentially responsible for yeast exosome core activity. Nat Struct Mol Biol 14: 15-22.
15. Edgar R, Domrachev M, Lash AE. 2002. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 30: 207-210.
16. Estevez AM, Lehner B, Sanderson CM, Ruppert T, Clayton C. 2003. The roles of intersubunit interactions in exosome stability. J Biol Chem 278: 34943-34951.
17. Forler D, Kocher T, Rode M, Gentzel M, Izaurralde E, Wilm M. 2003. An efficient protein complex purification method for functional proteomics in higher eukaryotes. Nat Biotechnol 21: 89-92.
18. Fox MG. 1997. Identification of a new ribosomal RNA in Drosophila melanogaster. Gene 194: 291-295.
19. Gatfield D, Izaurralde E. 2004. Nonsense-mediated messenger RNA decay is initiated by endonucleolytic cleavage in Drosophila. Nature 429: 575-578.
20. Graham AC, Kiss DL, Andrulis ED. 2006. Differential distribution of exosome subunits at the nuclear lamina and in cytoplasmic foci. Mol Biol Cell 17: 1399-1409.
21. Graham AC, Davis SM, Andrulis ED. 2009a. Interdependent nucleocytoplasmic trafficking and interactions of Dis3 with Rrp6, the core exosome, and importin-α3. Traffic 10: 499-513.
22. Graham AC, Davis SM, Andrulis ED. 2009b. Core exosome-independent roles for Rrp6 in cell cycle progression. Mol Biol Cell 20: 2242-2253.
23. Hilleren P, McCarthy T, Rosbash M, Parker R, Jensen TH. 2001. Quality control of mRNA 3′-end processing is linked to the nuclear exosome. Nature 413: 538-542.
24. Houalla R, Devaux F, Fatica A, Kufel J, Barrass D, Torchet C, Tollervey D. 2006. Microarray detection of novel nuclear RNA substrates for the exosome. Yeast 23: 439-454.
25. Houseley J, LaCava J, Tollervey D. 2006. RNA-quality control by the exosome. Nat Rev Mol Cell Biol 7: 529-539.
26. Hu W, Sweet TJ, Chamnongpol S, Baker KE, Coller J. 2009. Co-translational mRNA decay in Saccharomyces cerevisiae. Nature 461: 225-229.
27. Jackson AL, Linsley PS. 2004. Noise amidst the silence: Off-target effects of siRNAs? Trends Genet 20: 521-524.
28. Jackson AL, Bartz SR, Schelter J, Kobayashi SV, Burchard J, Mao M, Li B, Cavet G, Linsley PS. 2003. Expression profiling reveals off-target gene regulation by RNAi. Nat Biotechnol 21: 635-637.
29. Jackson AL, Burchard J, Schelter J, Chau BN, Cleary M, Lim L, Linsley PS. 2006. Widespread siRNA 'off-target' transcript silencing mediated by seed region sequence complementarity. RNA 12: 1179-1187.
30. Met in S. cerevisiae. Genes & Dev 18: 1227-1240.
31. Lejeune F, Li X, Maquat LE. 2003. Nonsense-mediated mRNA decay in mammalian cells involves decapping, deadenylating, and exonucleolytic activities. Mol Cell 12: 675-687.
32. Lin WJ, Duffy A, Chen CY. 2007. Localization of AU-rich element-containing mRNA in cytoplasmic granules containing exosome subunits. J Biol Chem 282: 19958-19968.
33. Liu Q, Greimann JC, Lima CD. 2006. Reconstitution, activities, and structure of the eukaryotic RNA exosome. Cell 127: 1223-1237.
34. Lorentzen E, Walter P, Fribourg S, Evguenieva-Hackenberg E, Klug G, Conti E. 2005. The archaeal exosome core is a hexameric ring structure with three catalytic subunits. Nat Struct Mol Biol 12: 575-581.
35. 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: 457-466.
36. Neil H, Malabat C, d'Aubenton-Carafa Y, Xu Z, Steinmetz LM, Jacquier A. 2009. Widespread bidirectional promoters are the major source of cryptic transcripts in yeast. Nature 451: 1038-1042.
37. Pavlakis GN, Jordan BR, Wurst RM, Vournakis JN. 1979. Sequence and secondary structure of Drosophila melanogaster 5.8S and 2S rRNAs and of the processing site between them. Nucleic Acids Res 7: 2213-2238.
38. Preker P, Nielsen J, Kammler S, Lykke-Andersen S, Christensen MS, Mapendano CK, Schierup MH, Jensen TH. 2008. RNA exosome depletion reveals transcription upstream of active human promoters. Science 322: 1851-1854.
39. Rehwinkel J, Letunic I, Raes J, Bork P, Izaurralde E. 2005. Nonsense-mediated mRNA decay factors act in concert to regulate common mRNA targets. RNA 11: 1530-1544.
40. Schmid M, Jensen TH. 2008. The exosome: A multipurpose RNA-decay machine. Trends Biochem Sci 33: 501-510.
41. Schneider C, Anderson JT, Tollervey D. 2007. The exosome subunit Rrp44 plays a direct role in RNA substrate recognition. Mol Cell 27: 324-331.
42. Shimada T. 1992. Distribution of split 5.8S ribosomal RNA in Diptera. Insect Mol Biol 1: 45-49.
43. van Dijk EL, Schilders G, Pruijn GJ. 2007. Human cell growth requires a functional cytoplasmic exosome, which is involved in various mRNA decay pathways. RNA 13: 1027-1035.
44. van Hoof A, Parker R. 1999. The exosome: A proteasome for RNA? Cell 99: 347-350.
45. Wyers F, Rougemaille M, Badis G, Rousselle JC, Dufour ME, Boulay J, Regnault B, Devaux F, Namane A, Seraphin B, 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.