Table of Contents Author Guidelines Submit a Manuscript
Archaea
Volume 2012, Article ID 721869, 7 pages
http://dx.doi.org/10.1155/2012/721869
Research Article

Crystal Structure of a 9-Subunit Archaeal Exosome in Pre-Catalytic States of the Phosphorolytic Reaction

Department of Structural Cell Biology, Max Planck Institute of Biochemistry, Am Klopferspitz 18, 82152 Martinsried, Germany

Received 11 September 2012; Accepted 4 December 2012

Academic Editor: Anita Marchfelder

Copyright © 2012 Esben Lorentzen and Elena Conti. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. J. Houseley, J. LaCava, and D. Tollervey, “RNA-quality control by the exosome,” Nature Reviews Molecular Cell Biology, vol. 7, no. 7, pp. 529–539, 2006. View at Publisher · View at Google Scholar · View at Scopus
  2. E. Lorentzen and E. Conti, “The exosome and the proteasome: nano-compartments for degradation,” Cell, vol. 125, no. 4, pp. 651–654, 2006. View at Publisher · View at Google Scholar · View at Scopus
  3. K. Büttner, K. Wenig, and K. P. Hopfner, “Structural framework for the mechanism of archaeal exosomes in RNA processing,” Molecular Cell, vol. 20, no. 3, pp. 461–471, 2005. View at Publisher · View at Google Scholar · View at Scopus
  4. E. Lorentzen, A. Dziembowski, D. Lindner, B. Seraphin, and E. Conti, “RNA channelling by the archaeal exosome,” EMBO Reports, vol. 8, no. 5, pp. 470–476, 2007. View at Publisher · View at Google Scholar · View at Scopus
  5. F. Bonneau, J. Basquin, J. Ebert, E. Lorentzen, and E. Conti, “The yeast exosome functions as a macromolecular cage to channel RNA substrates for degradation,” Cell, vol. 139, no. 3, pp. 547–559, 2009. View at Publisher · View at Google Scholar · View at Scopus
  6. H. Malet, M. Topf, D. K. Clare et al., “RNA channelling by the eukaryotic exosome,” EMBO Reports, vol. 11, no. 12, pp. 936–942, 2010. View at Publisher · View at Google Scholar · View at Scopus
  7. E. V. Wasmuth and C. D. Lima, “Exo- and endoribonucleolytic activities of yeast cytoplasmic and nuclear RNA exosomes are dependent on the noncatalytic core and central channel,” Molecular Cell, vol. 48, no. 1, pp. 133–144, 2012. View at Google Scholar
  8. Q. Liu, J. C. Greimann, and C. D. Lima, “Reconstitution, activities, and structure of the eukaryotic RNA exosome,” Cell, vol. 127, no. 6, pp. 1223–1237, 2006. View at Publisher · View at Google Scholar · View at Scopus
  9. A. Dziembowski, E. Lorentzen, E. Conti, and B. Séraphin, “A single subunit, Dis3, is essentially responsible for yeast exosome core activity,” Nature Structural and Molecular Biology, vol. 14, no. 1, pp. 15–22, 2007. View at Publisher · View at Google Scholar · View at Scopus
  10. E. Lorentzen, P. Walter, S. Fribourg, E. Evguenieva-Hackenberg, G. Klug, and E. Conti, “The archaeal exosome core is a hexameric ring structure with three catalytic subunits,” Nature Structural and Molecular Biology, vol. 12, no. 7, pp. 575–581, 2005. View at Publisher · View at Google Scholar · View at Scopus
  11. P. Walter, F. Klein, E. Lorentzen, A. Ilchmann, G. Klug, and E. Evguenieva-Hackenberg, “Characterization of native and reconstituted exosome complexes from the hyperthermophilic archaeon Sulfolobus solfataricus,” Molecular Microbiology, vol. 62, no. 4, pp. 1076–1089, 2006. View at Publisher · View at Google Scholar · View at Scopus
  12. C. Allmang, E. Petfalski, A. Podtelejnikov, M. Mann, D. Tollervey, and P. Mitchell, “The yeast exosome and human PM-Scl are related complexes of 3′ → 5′ exonucleases,” Genes and Development, vol. 13, no. 16, pp. 2148–2158, 1999. View at Google Scholar · View at Scopus
  13. P. Mitchell, E. Petfalski, A. Shevchenko, M. Mann, and D. Tollervey, “The exosome: a conserved eukaryotic RNA processing complex containing multiple 3′ → 5′ exoribonucleases,” Cell, vol. 91, no. 4, pp. 457–466, 1997. View at Google Scholar · View at Scopus
  14. E. Lorentzen, J. Basquin, R. Tomecki, A. Dziembowski, and E. Conti, “Structure of the active subunit of the yeast exosome core, Rrp44: diverse modes of substrate recruitment in the RNase II nuclease family,” Molecular Cell, vol. 29, no. 6, pp. 717–728, 2008. View at Publisher · View at Google Scholar · View at Scopus
  15. C. Allmang, J. Kufel, G. Chanfreau, P. Mitchell, E. Petfalski, and D. Tollervey, “Functions of the exosome in rRNA, snoRNA and snRNA synthesis,” The EMBO Journal, vol. 18, no. 19, pp. 5399–5410, 1999. View at Publisher · View at Google Scholar · View at Scopus
  16. S. F. Midtgaard, J. Assenholt, A. T. Jonstrup, L. B. Van, T. H. Jensen, and D. E. Brodersen, “Structure of the nuclear exosome component Rrp6p reveals an interplay between the active site and the HRDC domain,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 32, pp. 11898–11903, 2006. View at Publisher · View at Google Scholar · View at Scopus
  17. J. A. Stead, J. L. Costello, M. J. Livingstone, and P. Mitchell, “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 Research, vol. 35, no. 16, pp. 5556–5567, 2007. View at Publisher · View at Google Scholar · View at Scopus
  18. V. Portnoy, E. Evguenieva-Hackenberg, F. Klein et al., “RNA polyadenylation in archaea: not observed in Haloferax while the exosome polynucleotidylates RNA in Sulfolobus,” EMBO Reports, vol. 6, no. 12, pp. 1188–1193, 2005. View at Publisher · View at Google Scholar · View at Scopus
  19. V. Portnoy and G. Schuster, “RNA polyadenylation and degradation in different Archaea; roles of the exosome and RNase R,” Nucleic Acids Research, vol. 34, no. 20, pp. 5923–5931, 2006. View at Publisher · View at Google Scholar · View at Scopus
  20. M. F. Symmons, G. H. Jones, and B. F. Luisi, “A duplicated fold is the structural basis for polynucleotide phosphorylase catalytic activity, processivity, and regulation,” Structure, vol. 8, no. 11, pp. 1215–1226, 2000. View at Publisher · View at Google Scholar · View at Scopus
  21. M. F. Symmons, M. G. Williams, B. F. Luisi, G. H. Jones, and A. J. Carpousis, “Running rings around RNA: a superfamily of phosphate-dependent RNases,” Trends in Biochemical Sciences, vol. 27, no. 1, pp. 11–18, 2002. View at Publisher · View at Google Scholar · View at Scopus
  22. E. Lorentzen and E. Conti, “Structural basis of 3′ end RNA recognition and exoribonucleolytic cleavage by an exosome RNase PH core,” Molecular Cell, vol. 20, no. 3, pp. 473–481, 2005. View at Publisher · View at Google Scholar · View at Scopus
  23. C. Lu, F. Ding, and A. Ke, “Crystal structure of the S. solfataricus archaeal exosome reveals conformational flexibility in the RNA-binding ring,” PLoS One, vol. 5, no. 1, Article ID e8739, 2010. View at Publisher · View at Google Scholar · View at Scopus
  24. M. V. A. S. Navarro, C. C. Oliveira, N. I. T. Zanchin, and B. G. Guimarães, “Insights into the mechanism of progressive RNA degradation by the archaeal exosome,” Journal of Biological Chemistry, vol. 283, no. 20, pp. 14120–14131, 2008. View at Publisher · View at Google Scholar · View at Scopus
  25. C. L. Ng, D. G. Waterman, A. A. Antson, and M. Ortiz-Lombardía, “Structure of the Methanothermobacter thermautotrophicus exosome RNase PH ring,” Acta Crystallographica Section D, vol. 66, part 5, pp. 522–528, 2010. View at Publisher · View at Google Scholar · View at Scopus
  26. E. Evguenieva-Hackenberg, V. Roppelt, P. Finsterseifer, and G. Klug, “Rrp4 and Csl4 are needed for efficient degradation but not for polyadenylation of synthetic and natural RNA by the archaeal exosome,” Biochemistry, vol. 47, no. 50, pp. 13158–13168, 2008. View at Publisher · View at Google Scholar · View at Scopus
  27. E. Lorentzen and E. Conti, “Expression, reconstitution, and structure of an archaeal RNA degrading exosome,” Methods in Enzymology, vol. 447, pp. 417–435, 2008. View at Publisher · View at Google Scholar · View at Scopus
  28. W. Kabsch, “XDS,” Acta Crystallogr D, vol. 66, part 2, pp. 125–132, 2010. View at Google Scholar
  29. G. N. Murshudov, A. A. Vagin, and E. J. Dodson, “Refinement of macromolecular structures by the maximum-likelihood method,” Acta Crystallographica D, vol. 53, no. 3, pp. 240–255, 1997. View at Publisher · View at Google Scholar · View at Scopus
  30. P. D. Adams, P. V. Afonine, G. Bunkóczi et al., “PHENIX: a comprehensive Python-based system for macromolecular structure solution,” Acta Crystallogr D, vol. 66, part 2, pp. 213–221, 2010. View at Google Scholar
  31. P. Emsley, B. Lohkamp, W. G. Scott, and K. Cowtan, “Features and development of Coot,” Acta Crystallographica Section D, vol. 66, part 4, pp. 486–501, 2010. View at Publisher · View at Google Scholar · View at Scopus
  32. L. S. Harlow, A. Kadziola, K. F. Jensen, and S. Larsen, “Crystal structure of the phosphorolytic exoribonuclease RNase PH from Bacillus subtilis and implications for its quaternary structure and tRNA binding,” Protein Science, vol. 13, no. 3, pp. 668–677, 2004. View at Publisher · View at Google Scholar · View at Scopus
  33. S. Nurmohamed, B. Vaidialingam, A. J. Callaghan, and B. F. Luisi, “Crystal structure of escherichia coli polynucleotide phosphorylase core bound to RNase E, RNA and manganese: implications for catalytic mechanism and RNA degradosome assembly,” Journal of Molecular Biology, vol. 389, no. 1, pp. 17–33, 2009. View at Publisher · View at Google Scholar · View at Scopus