The exosome contains domains with specific endoribonuclease, exoribonuclease and cytoplasmic mRNA decay activities (original) (raw)

References

  1. Moser, M.J., Holley, W.R., Chatterjee, A. & Mian, I.S. The proofreading domain of Escherichia coli DNA polymerase I and other DNA and/or RNA exonuclease domains. Nucleic Acids Res. 25, 5110–5118 (1997).
    Article CAS PubMed PubMed Central Google Scholar
  2. Mian, I.S. Comparative sequence analysis of ribonucleases HII, III, II PH and D. Nucleic Acids Res. 25, 3187–3195 (1997).
    Article CAS PubMed PubMed Central Google Scholar
  3. Deutscher, M.P. & Li, Z. Exoribonucleases and their multiple roles in RNA metabolism. Prog. Nucleic Acid Res. Mol. Biol. 66, 67–105 (2001).
    Article CAS PubMed Google Scholar
  4. Zuo, Y. & Deutscher, M.P. Exoribonuclease superfamilies: structural analysis and phylogenetic distribution. Nucleic Acids Res. 29, 1017–1026 (2001).
    Article CAS PubMed PubMed Central Google Scholar
  5. van Hoof, A., Lennertz, P. & Parker, R. Three conserved members of the RNase D family have unique and overlapping functions in the processing of 5S, 5.8S, U4, U5, RNase MRP and RNase P RNAs in yeast. EMBO J. 19, 1357–1365 (2000).
    Article CAS PubMed PubMed Central Google Scholar
  6. Muhlrad, D., Decker, C.J. & Parker, R. Turnover mechanisms of the stable yeast PGK1 mRNA. Mol. Cell. Biol. 15, 2145–2156 (1995).
    Article CAS PubMed PubMed Central Google Scholar
  7. Jacobs Anderson, J.S. & Parker, R. 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 (1998).
    Article Google Scholar
  8. van Hoof, A., Frischmeyer, P.A., Dietz, H.C. & Parker, R. Exosome-mediated recognition and degradation of mRNAs lacking a termination codon. Science 295, 2262–2264 (2002).
    Article CAS PubMed Google Scholar
  9. Meaux, S. & Van Hoof, A. Yeast transcripts cleaved by an internal ribozyme provide new insight into the role of the cap and poly(A) tail in translation and mRNA decay. RNA 12, 1323–1337 (2006).
    Article CAS PubMed PubMed Central Google Scholar
  10. Mitchell, P., Petfalski, E., Shevchenko, A., Mann, M. & Tollervey, D. The exosome: a conserved eukaryotic RNA processing complex containing multiple 3′ → 5′ exoribonucleases. Cell 91, 457–466 (1997).
    Article CAS PubMed Google Scholar
  11. Allmang, C. et al. The yeast exosome and human PM-Scl are related complexes of 3′ → 5′ exonucleases. Genes Dev. 13, 2148–2158 (1999).
    Article CAS PubMed PubMed Central Google Scholar
  12. Allmang, C. et al. Functions of the exosome in rRNA, snoRNA and snRNA synthesis. EMBO J. 18, 5399–5410 (1999).
    Article CAS PubMed PubMed Central Google Scholar
  13. 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. 20, 441–452 (2000).
    Article CAS PubMed PubMed Central Google Scholar
  14. de la Cruz, J., Kressler, D., Tollervey, D. & Linder, P. 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 (1998).
    Article CAS PubMed PubMed Central Google Scholar
  15. Liu, Q., Greimann, J.C. & Lima, C.D. Reconstitution, activities, and structure of the eukaryotic RNA exosome. Cell 127, 1223–1237 (2006).
    Article CAS PubMed Google Scholar
  16. Lorentzen, E. et al. The archaeal exosome core is a hexameric ring structure with three catalytic subunits. Nat. Struct. Mol. Biol. 12, 575–581 (2005).
    Article CAS PubMed Google Scholar
  17. 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 8, 1215–1226 (2000).
    Article CAS PubMed Google Scholar
  18. Navarro, M.V., Oliveira, C.C., Zanchin, N.I. & Guimaraes, B.G. Insights into the mechanism of progressive RNA degradation by the archaeal exosome. J. Biol. Chem. 283, 14120–14131 (2008).
    Article CAS PubMed Google Scholar
  19. Lorentzen, E. & Conti, E. Structural basis of 3′ end RNA recognition and exoribonucleolytic cleavage by an exosome RNase PH core. Mol. Cell 20, 473–481 (2005).
    Article CAS PubMed Google Scholar
  20. Buttner, K., Wenig, K. & Hopfner, K.P. Structural framework for the mechanism of archaeal exosomes in RNA processing. Mol. Cell 20, 461–471 (2005).
    Article PubMed Google Scholar
  21. Dziembowski, A., Lorentzen, E., Conti, E. & Seraphin, B. A single subunit, Dis3, is essentially responsible for yeast exosome core activity. Nat. Struct. Mol. Biol. 14, 15–22 (2007).
    Article CAS PubMed Google Scholar
  22. Chekanova, J.A., Dutko, J.A., Mian, I.S. & Belostotsky, D.A. Arabidopsis thaliana exosome subunit AtRrp4p is a hydrolytic 3′ → 5′ exonuclease containing S1 and KH RNA-binding domains. Nucleic Acids Res. 30, 695–700 (2002).
    Article CAS PubMed PubMed Central Google Scholar
  23. 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 29, 717–728 (2008).
    Article CAS PubMed Google Scholar
  24. Schneider, C., Anderson, J.T. & Tollervey, D. The exosome subunit Rrp44 plays a direct role in RNA substrate recognition. Mol. Cell 27, 324–331 (2007).
    Article CAS PubMed PubMed Central Google Scholar
  25. Wang, H.W. et al. Architecture of the yeast Rrp44 exosome complex suggests routes of RNA recruitment for 3′ end processing. Proc. Natl. Acad. Sci. USA 104, 16844–16849 (2007).
    Article CAS PubMed PubMed Central Google Scholar
  26. Frazão, C. et al. Unravelling the dynamics of RNA degradation by ribonuclease II and its RNA-bound complex. Nature 443, 110–114 (2006).
    Article PubMed Google Scholar
  27. Barbas, A. et al. New insights into the mechanism of RNA degradation by ribonuclease II: identification of the residue responsible for setting the RNase II end product. J. Biol. Chem. 283, 13070–13076 (2008).
    Article CAS PubMed Google Scholar
  28. Arcus, V.L., Backbro, K., Roos, A., Daniel, E.L. & Baker, E.N. Distant structural homology leads to the functional characterization of an archaeal PIN domain as an exonuclease. J. Biol. Chem. 279, 16471–16478 (2004).
    Article CAS PubMed Google Scholar
  29. Levin, I. et al. Crystal structure of a PIN (PilT N-terminus) domain (AF0591) from Archaeoglobus fulgidus at 1.90 resolution. Proteins 56, 404–408 (2004).
    Article CAS PubMed Google Scholar
  30. Glavan, F., Behm-Ansmant, I., Izaurralde, E. & Conti, E. Structures of the PIN domains of SMG6 and SMG5 reveal a nuclease within the mRNA surveillance complex. EMBO J. 25, 5117–5125 (2006).
    Article CAS PubMed PubMed Central Google Scholar
  31. Daines, D.A., Wu, M.H. & Yuan, S.Y. VapC-1 of nontypeable Haemophilus influenzae is a ribonuclease. J. Bacteriol. 189, 5041–5048 (2007).
    Article CAS PubMed PubMed Central Google Scholar
  32. Bunker, R.D., McKenzie, J.L., Baker, E.N. & Arcus, V.L. Crystal structure of PAE0151 from Pyrobaculum aerophilum, a PIN-domain (VapC) protein from a toxin-antitoxin operon. Proteins 72, 510–518 (2008).
    Article CAS PubMed Google Scholar
  33. Eberle, A.B., Lykke-Andersen, S., Muhlemann, O. & Jensen, T.H. SMG6 promoted endonucleoytic cleavage of nonsense mRNA in human cells. Nat. Struct. Mol. Biol. advance online publication, doi:10.1038/nsmb.1530 (07 December 2008).
  34. Fatica, A., Tollervey, D. & Dlakic, M. PIN domain of Nob1p is required for D-site cleavage in 20S pre-rRNA. RNA 10, 1698–1701 (2004).
    Article CAS PubMed PubMed Central Google Scholar
  35. Bleichert, F., Granneman, S., Osheim, Y.N., Beyer, A.L. & Baserga, S.J. The PINc domain protein Utp24, a putative nuclease, is required for the early cleavage steps in 18S rRNA maturation. Proc. Natl. Acad. Sci. USA 103, 9464–9469 (2006).
    Article CAS PubMed PubMed Central Google Scholar
  36. Amblar, M. & Arraiano, C.M. A single mutation in Escherichia coli ribonuclease II inactivates the enzyme without affecting RNA binding. FEBS J. 272, 363–374 (2005).
    Article CAS PubMed Google Scholar
  37. Amblar, M., Barbas, A., Fialho, A.M. & Arraiano, C.M. Characterization of the functional domains of Escherichia coli RNase II. J. Mol. Biol. 360, 921–933 (2006).
    Article CAS PubMed Google Scholar
  38. Barbas, A. et al. New insights into the mechanism of RNA degradation by ribonuclease II: identification of the residue responsible for setting the RNase II end product. J. Biol. Chem. 283, 13070–13076 (2008).
    Article CAS PubMed Google Scholar
  39. 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. 232, 733–737 (2005).
    Article CAS PubMed Google Scholar
  40. Johnson, A.W. & Kolodner, R.D. Synthetic lethality of sep1 (xrn1) ski2 and sep1 (xrn1) ski3 mutants of Saccharomyces cerevisiae is independent of killer virus and suggests a general role for these genes in translation control. Mol. Cell. Biol. 15, 2719–2727 (1995).
    Article CAS PubMed PubMed Central Google Scholar
  41. Andrade, J.M., Pobre, V., Silva, I.J., Domingues, S. & Arraiano, C.M. The role of 3′ to 5′ exonucleases in RNA degradation. Prog. Nucleic Acid Res. Mol. Biol. (in the press).
  42. Mackie, G.A. Ribonuclease E is a 5′-end-dependent endonuclease. Nature 395, 720–723 (1998).
    Article CAS PubMed Google Scholar
  43. Yang, W. An equivalent metal ion in one- and two-metal-ion catalysis. Nat. Struct. Mol. Biol. 15, 1228–1231 (2008).
    Article PubMed PubMed Central Google Scholar
  44. Ross-Macdonald, P. et al. Large-scale analysis of the yeast genome by transposon tagging and gene disruption. Nature 402, 413–418 (1999).
    Article CAS PubMed Google Scholar
  45. Chekanova, J.A. et al. Genome-wide high-resolution mapping of exosome substrates reveals hidden features in the Arabidopsis transcriptome. Cell 131, 1340–1353 (2007).
    Article CAS PubMed Google Scholar
  46. Koonin, E.V., Wolf, Y.I. & Aravind, L. Prediction of the archaeal exosome and its connections with the proteasome and the translation and transcription machineries by a comparative-genomic approach. Genome Res. 11, 240–252 (2001).
    Article CAS PubMed PubMed Central Google Scholar
  47. Carpousis, A.J., Van Houwe, G., Ehretsmann, C. & Krisch, H.M. Copurification of E. coli RNAase E and PNPase: evidence for a specific association between two enzymes important in RNA processing and degradation. Cell 76, 889–900 (1994).
    Article CAS PubMed Google Scholar
  48. Py, B., Causton, H., Mudd, E.A. & Higgins, C.F. A protein complex mediating mRNA degradation in Escherichia coli. Mol. Microbiol. 14, 717–729 (1994).
    Article CAS PubMed Google Scholar
  49. Liu, J., Valencia-Sanchez, M.A., Hannon, G.J. & Parker, R. MicroRNA-dependent localization of targeted mRNAs to mammalian P-bodies. Nat. Cell Biol. 7, 719–723 (2005).
    Article CAS PubMed PubMed Central Google Scholar
  50. Ingelfinger, D., Arndt-Jovin, D.J., Luhrmann, R. & Achsel, T. The human LSm1–7 proteins colocalize with the mRNA-degrading enzymes Dcp1/2 and Xrnl in distinct cytoplasmic foci. RNA 8, 1489–1501 (2002).
    CAS PubMed PubMed Central Google Scholar
  51. Bashkirov, V.I., Scherthan, H., Solinger, J.A., Buerstedde, J.M. & Heyer, W.D. A mouse cytoplasmic exoribonuclease (mXRN1p) with preference for G4 tetraplex substrates. J. Cell Biol. 136, 761–773 (1997).
    Article CAS PubMed PubMed Central Google Scholar
  52. Cougot, N., Babajko, S. & Seraphin, B. Cytoplasmic foci are sites of mRNA decay in human cells. J. Cell Biol. 165, 31–40 (2004).
    Article CAS PubMed PubMed Central Google Scholar
  53. Zheng, D. et al. Deadenylation is prerequisite for P-body formation and mRNA decay in mammalian cells. J. Cell Biol. 182, 89–101 (2008).
    Article CAS PubMed PubMed Central Google Scholar
  54. Andrei, M.A. et al. A role for eIF4E and eIF4E-transporter in targeting mRNPs to mammalian processing bodies. RNA 11, 717–727 (2005).
    Article CAS PubMed PubMed Central Google Scholar
  55. Giaever, G. et al. Functional profiling of the Saccharomyces cerevisiae genome. Nature 418, 387–391 (2002).
    Article CAS PubMed Google Scholar
  56. Rockmill, B., Lambie, E.J. & Roeder, G.S. Spore enrichment. Methods Enzymol. 194, 146–149 (1991).
    Article CAS PubMed Google Scholar
  57. Sikorski, R.S. & Hieter, P. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122, 19–27 (1989).
    CAS PubMed PubMed Central Google Scholar
  58. Wilson, M.A., Meaux, S. & van Hoof, A. A genomic screen in yeast reveals novel aspects of nonstop mRNA metabolism. Genetics 177, 773–784 (2007).
    Article CAS PubMed PubMed Central Google Scholar
  59. van Hoof, A., Staples, R.R., Baker, R.E. & Parker, R. Function of the ski4p (Csl4p) and Ski7p proteins in 3′-to-5′ degradation of mRNA. Mol. Cell. Biol. 20, 8230–8243 (2000).
    Article CAS PubMed PubMed Central Google Scholar
  60. Lebreton, A., Tomecki, R., Dziembowski, A. & Séraphin, B. Endonucleolytic RNA cleavage by a eukaryotic exosome. Nature advance online publication, doi:10.1038/nature07480 (7 December 2008).

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