Exo- and Endoribonucleolytic Activities of Yeast Cytoplasmic and Nuclear RNA Exosomes Are Dependent on the Noncatalytic Core and Central Channel

Molecular Cell

Volumn 48, Issue 1, 2012, Pages 133-144

  Wasmuth, Elizabeth V ^a,b   Lima, Christopher D ^a  

^a NEW YORK STRUCTURAL BIOLOGY CENTER   (United States)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENDORIBONUCLEASE RRP44; EXORIBONUCLEASE; EXORIBONUCLEASE RRP6; NUCLEAR RNA; RIBONUCLEASE; RNA EXOSOME CORE EXO9; UNCLASSIFIED DRUG;

ARTICLE; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME REGULATION; EXOSOME; NONHUMAN; PROTEIN FUNCTION; YEAST;

CATALYTIC DOMAIN; CELL NUCLEUS; CYTOPLASM; ENDORIBONUCLEASES; EXORIBONUCLEASES; EXOSOME MULTIENZYME RIBONUCLEASE COMPLEX; MODELS, MOLECULAR; MUTATION; PROTEIN SUBUNITS; RECOMBINANT PROTEINS; RNA, FUNGAL; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84867395423     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2012.07.012     Document Type: Article

References (42)

1. Allmang C., Kufel J., Chanfreau G., Mitchell P., Petfalski E., Tollervey D. Functions of the exosome in rRNA, snoRNA and snRNA synthesis. EMBO J. 1999, 18:5399-5410.
2. Allmang C., Mitchell P., Petfalski E., Tollervey D. Degradation of ribosomal RNA precursors by the exosome. Nucleic Acids Res. 2000, 28:1684-1691.
3. Anderson J.S., Parker R.P. 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. 1998, 17:1497-1506.
4. Assenholt J., Mouaikel J., Andersen K.R., Brodersen D.E., Libri D., Jensen T.H. Exonucleolysis is required for nuclear mRNA quality control in yeast THO mutants. RNA 2008, 14:2305-2313.
5. Basu U., Meng F.L., Keim C., Grinstein V., Pefanis E., Eccleston J., Zhang T., Myers D., Wasserman C.R., Wesemann D.R., et al. The RNA exosome targets the AID cytidine deaminase to both strands of transcribed duplex DNA substrates. Cell 2011, 144:353-363.
6. Bonneau F., Basquin J., Ebert J., Lorentzen E., Conti E. The yeast exosome functions as a macromolecular cage to channel RNA substrates for degradation. Cell 2009, 139:547-559.
7. Bühler M., Haas W., Gygi S.P., Moazed D. RNAi-dependent and -independent RNA turnover mechanisms contribute to heterochromatic gene silencing. Cell 2007, 129:707-721.
8. Butler, J.S., and Mitchell, P. (2010). Rrp6, Rrp47 and cofactors of the nuclear exosome. In RNA Exosome, T.H. Jensen, ed. (New York: Landes Bioscience and Springer Science). Adv. Exp. Med. Biol. 702, 91-104.
9. Büttner K., Wenig K., Hopfner K.P. The exosome: a macromolecular cage for controlled RNA degradation. Mol. Microbiol. 2006, 61:1372-1379.
10. Callahan K.P., Butler J.S. Evidence for core exosome independent function of the nuclear exoribonuclease Rrp6p. Nucleic Acids Res. 2008, 36:6645-6655.
11. Callahan K.P., Butler J.S. TRAMP complex enhances RNA degradation by the nuclear exosome component Rrp6. J. Biol. Chem. 2010, 285:3540-3547.
12. Davis C.A., Ares M. Accumulation of unstable promoter-associated transcripts upon loss of the nuclear exosome subunit Rrp6p in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 2006, 103:3262-3267.
13. Doma M.K., Parker R. Endonucleolytic cleavage of eukaryotic mRNAs with stalls in translation elongation. Nature 2006, 440:561-564.
14. Dziembowski A., Lorentzen E., Conti E., Séraphin B. A single subunit, Dis3, is essentially responsible for yeast exosome core activity. Nat. Struct. Mol. Biol. 2007, 14:15-22.
15. Flynt A.S., Greimann J.C., Chung W.J., Lima C.D., Lai E.C. MicroRNA biogenesis via splicing and exosome-mediated trimming in Drosophila. Mol. Cell 2010, 38:900-907.
16. Greimann J.C., Lima C.D. Reconstitution of RNA exosomes from human and Saccharomyces cerevisiae cloning, expression, purification, and activity assays. Methods Enzymol. 2008, 448:185-210.
17. Houseley J., LaCava J., Tollervey D. RNA-quality control by the exosome. Nat. Rev. Mol. Cell Biol. 2006, 7:529-539.
18. Januszyk, K., and Lima, C.D. (2010). Structural components and architectures of RNA exosomes. In RNA Exosome, T.H. Jensen, ed. (New York: Landes Bioscience and Springer Science). Adv. Exp. Med. Biol. 702, 9-28.
19. Januszyk K., Liu Q., Lima C.D. Activities of human RRP6 and structure of the human RRP6 catalytic domain. RNA 2011, 17:1566-1577.
20. Larimer F.W., Stevens A. Disruption of the gene XRN1, coding for a 5'→3' exoribonuclease, restricts yeast cell growth. Gene 1990, 95:85-90.
21. Lebreton A., Tomecki R., Dziembowski A., Séraphin B. Endonucleolytic RNA cleavage by a eukaryotic exosome. Nature 2008, 456:993-996.
22. Liu Q., Greimann J.C., Lima C.D. Reconstitution, activities, and structure of the eukaryotic RNA exosome. Cell 2006, 127:1223-1237.
23. Lorentzen E., Conti E. The exosome and the proteasome: nano-compartments for degradation. Cell 2006, 125:651-654.
24. Lorentzen E., Basquin J., Tomecki R., Dziembowski A., Conti E. Structure of the active subunit of the yeast exosome core, Rrp44: diverse modes of substrate recruitment in the RNase II nuclease family. Mol. Cell 2008, 29:717-728.
25. Malet H., Topf M., Clare D.K., Ebert J., Bonneau F., Basquin J., Drazkowska K., Tomecki R., Dziembowski A., Conti E., et al. RNA channelling by the eukaryotic exosome. EMBO Rep. 2010, 11:936-942.
26. Midtgaard S.F., Assenholt J., Jonstrup A.T., Van L.B., Jensen T.H., Brodersen D.E. Structure of the nuclear exosome component Rrp6p reveals an interplay between the active site and the HRDC domain. Proc. Natl. Acad. Sci. USA 2006, 103:11898-11903.
27. Neil H., Malabat C., d'Aubenton-Carafa Y., Xu Z., Steinmetz L.M., Jacquier A. Widespread bidirectional promoters are the major source of cryptic transcripts in yeast. Nature 2009, 457:1038-1042.
28. Orban T.I., Izaurralde E. Decay of mRNAs targeted by RISC requires XRN1, the Ski complex, and the exosome. RNA 2005, 11:459-469.
29. Schaeffer D., van Hoof A. Different nuclease requirements for exosome-mediated degradation of normal and nonstop mRNAs. Proc. Natl. Acad. Sci. USA 2011, 108:2366-2371.
30. Schaeffer D., Tsanova B., Barbas A., Reis F.P., Dastidar E.G., Sanchez-Rotunno M., Arraiano C.M., van Hoof A. The exosome contains domains with specific endoribonuclease, exoribonuclease and cytoplasmic mRNA decay activities. Nat. Struct. Mol. Biol. 2009, 16:56-62.
31. 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, 37:1127-1140.
32. Seol Y., Skinner G.M., Visscher K. Elastic properties of a single-stranded charged homopolymeric ribonucleotide. Phys. Rev. Lett. 2004, 93:118102.
33. Seol Y., Skinner G.M., Visscher K., Buhot A., Halperin A. Stretching of homopolymeric RNA reveals single-stranded helices and base-stacking. Phys. Rev. Lett. 2007, 98:158103.
34. Smart O.S., Neduvelil J.G., Wang X., Wallace B.A., Sansom M.S. HOLE: a program for the analysis of the pore dimensions of ion channel structural models. J. Mol. Graph. 1996, 14:354-360. 376.
35. Stead J.A., Costello J.L., Livingstone M.J., Mitchell P. The PMC2NT domain of the catalytic exosome subunit Rrp6p provides the interface for binding with its cofactor Rrp47p, a nucleic acid-binding protein. Nucleic Acids Res. 2007, 35:5556-5567.
36. Symmons M.F., Jones G.H., Luisi B.F. A duplicated fold is the structural basis for polynucleotide phosphorylase catalytic activity, processivity, and regulation. Structure 2000, 8:1215-1226.
37. Tomecki R., Kristiansen M.S., Lykke-Andersen S., Chlebowski A., Larsen K.M., Szczesny R.J., Drazkowska K., Pastula A., Andersen J.S., Stepien P.P., et al. The human core exosome interacts with differentially localized processive RNases: hDIS3 and hDIS3L. EMBO J. 2010, 29:2342-2357.
38. van Hoof A., Lennertz P., Parker R. Yeast exosome mutants accumulate 3'-extended polyadenylated forms of U4 small nuclear RNA and small nucleolar RNAs. Mol. Cell. Biol. 2000, 20:441-452.
39. van Hoof A., Frischmeyer P.A., Dietz H.C., Parker R. Exosome-mediated recognition and degradation of mRNAs lacking a termination codon. Science 2002, 295:2262-2264.
40. Wang H.W., Wang J., Ding F., Callahan K., Bratkowski M.A., Butler J.S., Nogales E., Ke A. Architecture of the yeast Rrp44 exosome complex suggests routes of RNA recruitment for 3' end processing. Proc. Natl. Acad. Sci. USA 2007, 104:16844-16849.
41. Wyers F., Rougemaille M., Badis G., Rousselle J.C., Dufour M.E., Boulay J., Régnault B., Devaux F., Namane A., Séraphin B., et al. Cryptic pol II transcripts are degraded by a nuclear quality control pathway involving a new poly(A) polymerase. Cell 2005, 121:725-737.
42. Xu Z., Wei W., Gagneur J., Perocchi F., Clauder-Münster S., Camblong J., Guffanti E., Stutz F., Huber W., Steinmetz L.M. Bidirectional promoters generate pervasive transcription in yeast. Nature 2009, 457:1033-1037.