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Structural Components and Architectures of RNA Exosomes

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Book cover RNA Exosome

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 702))

Abstract

A large body of structural work conducted over the past ten years has elucidated mechanistic details related to 3′ to 5′ processing and decay of RNA substrates by the RNA exosome. This chapter will focus on the structural organization of eukaryotic exosomes and their evolutionary cousins in bacteria and archaea with an emphasis on mechanistic details related to substrate recognition and to 3′ to 5′ phosphorolytic exoribonucleolytic activities of bacterial and archaeal exosomes as well as the hydrolytic exoribonucleolytic and endoribonucleolytic activities of eukaryotic exosomes. These points will be addressed in large part through presentation of crystal structures of phosphorolytic enzymes such as bacterial RNase PH, PNPase and archaeal exosomes and crystal structures of the eukaryotic exosome and exosome sub-complexes in addition to standalone structures of proteins that catalyze activities associated with the eukaryotic RNA exosome, namely Rrp44, Rrp6 and their bacterial counterparts.

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References

  1. Carpousis AJ. The Escherichia coli RNA degradosome: structure, function and relationship in other ribonucleolytic multienzyme complexes. Biochem Soc Trans 2002; 30(2):150–155.

    Article  PubMed  CAS  Google Scholar 

  2. Symmons MF, Jones GH, Luisi BF. A duplicated fold is the structural basis for polynucleotide phosphorylase catalytic activity, processivity and regulation. Structure 2000; 8(11): 1215–1226.

    Article  PubMed  CAS  Google Scholar 

  3. Evguenieva-Hackenberg E, Walter P, Hochleitner E et al. An exosome-like complex in Sulfolobus solfataricus. EMBO Rep 2003; 4(9):889–893.

    Article  PubMed  CAS  Google Scholar 

  4. Koonin EV, Wolf YI, 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 2001; 11(2):240–252.

    Article  PubMed  CAS  Google Scholar 

  5. Lorentzen E, Walter P, Fribourg S et al. The archaeal exosome core is a hexameric ring structure with three catalytic subunits. Nat Struct Mol Biol 2005; 12(7):575–581.

    Article  PubMed  CAS  Google Scholar 

  6. Buttner K, Wenig K, Hopfner KP. Structural framework for the mechanism of archaeal exosomes in RNA processing. Mol Cell 2005; 20(3):461–471.

    Article  PubMed  Google Scholar 

  7. Lorentzen E, Dziembowski A, Lindner D et al. RNA channelling by the archaeal exosome. EMBO Rep 2007; 8(5):470–476.

    Article  PubMed  CAS  Google Scholar 

  8. Nurmohamed S, Vaidialingam B, Callaghan AJ et al. Crystal structure of Escherichia coli polynucleotide phosphorylase core bound to RNase E, RNA and manganese: implications for catalytic mechanism and RNA degradosome assembly. J Mol Biol 2009; 389(1): 17–33.

    Article  PubMed  CAS  Google Scholar 

  9. Liu Q, Greimann JC, Lima CD. Reconstitution, activities and structure of the eukaryotic RNA exosome. Cell 2006; 127(6):1223–1237.

    Article  PubMed  CAS  Google Scholar 

  10. Dziembowski A, Lorentzen E, Conti E et al. A single subunit, Dis3, is essentially responsible for yeast exosome core activity. Nat Struct Mol Biol 2007; 14(1):15–22.

    Article  PubMed  CAS  Google Scholar 

  11. Liu QS, Greimann JC, Lima CD. Reconstitution, activities and structure of the eukaryotic RNA exosome (vol 127, pg 1223, 2006). Cell 2007; 131(1):188–189.

    Article  CAS  Google Scholar 

  12. Shi Z, Yang WZ, Lin-Chao S et al. Crystal structure of Escherichia coli PNPase: central channel residues are involved in processive RNA degradation. RNA 2008; 14(11):2361–2371.

    Article  PubMed  CAS  Google Scholar 

  13. Harlow LS, Kadziola A, Jensen KF et al. Crystal structure of the phosphorolytic exoribonuclease RNase PH from Bacillus subtilis and implications for its quaternary structure and tRNA binding. Protein Sci 2004; 13(3):668–677.

    Article  PubMed  CAS  Google Scholar 

  14. Ishii R, Nureki O, Yokoyama S. Crystal structure of the tRNA processing enzyme RNase PH from Aquifex aeolicus. J Biol Chem 2003; 278(34):32397–32404.

    Article  PubMed  CAS  Google Scholar 

  15. Navarro MV, Oliveira CC, Zanchin NI et al. Insights into the mechanism of progressive RNA degradation by the archaeal exosome. J Biol Chem 2008; 283(20):14120–14131.

    Article  PubMed  CAS  Google Scholar 

  16. Stehmeier P, Muller S. Phospho-regulated SUMO interaction modules connect the SUMO system to CK2 signaling. Mol Cell 2009; 33(3):400–409.

    Article  PubMed  CAS  Google Scholar 

  17. Lorentzen E, Conti E. Structural basis of 3′ end RNA recognition and exoribonucleolytic cleavage by an exosome RNase PH core. Mol Cell 2005; 20(3):473–481.

    Article  PubMed  CAS  Google Scholar 

  18. Ramos CR, Oliveira CL, Torriani IL et al. The Pyrococcus exosome complex: structural and functional characterization. J Biol Chem 2006; 281(10):6751–6759.

    Article  PubMed  CAS  Google Scholar 

  19. Bonneau F, Basquin J, Ebert J et al. The yeast exosome functions as a macromolecular cage to channel RNA substrates for degradation. Cell 2009; 139(3):547–559.

    Article  PubMed  CAS  Google Scholar 

  20. Valverde R, Edwards L, Regan L. Structure and function of KH domains. FEBS J 2008; 275(11):2712–2726.

    Article  PubMed  CAS  Google Scholar 

  21. Bycroft M, Hubbard TJ, Proctor M et al. The solution structure of the S1 RNA binding domain: a member of an ancient nucleic acid-binding fold. Cell 1997; 88(2):235–242.

    Article  PubMed  CAS  Google Scholar 

  22. Subramanian AR. Structure and functions of ribosomal protein S1. Prog Nucleic Acid Res Mol Biol 1983; 28:101–142.

    Article  PubMed  CAS  Google Scholar 

  23. Schubert M, Edge RE, Lario P et al. Structural characterization of the RNase ES1 domain and identification of its oligonucleotide-binding and dimerization interfaces. J Mol Biol 2004; 341(1):37–54.

    Article  PubMed  CAS  Google Scholar 

  24. Briani F, Curti S, Rossi F et al. Polynucleotide phosphorylase hinders mRNA degradation upon ribosomal protein S1 overexpression in Escherichia coli. RNA 2008; 14(11):2417–2429.

    Article  PubMed  CAS  Google Scholar 

  25. Stickney LM, Hankins JS, Miao X et al. Function of the conserved S1 and KH domains in polynucleotide phosphorylase. J Bacteriol 2005; 187(21):7214–7221.

    Article  PubMed  CAS  Google Scholar 

  26. Blake PR, Park JB, Zhou ZH et al. Solution-state structure by NMR of zinc-substituted rubredoxin from the marine hyperthermophilic archaebacterium Pyrococcus furiosus. Protein Sci 1992; 1(11):1508–1521.

    Article  PubMed  CAS  Google Scholar 

  27. Day MW, Hsu BT, Joshua-Tor L et al. X-ray crystal structures of the oxidized and reduced forms of the rubredoxin from the marine hyperthermophilic archaebacterium Pyrococcus furiosus. Protein Sci 1992; 1(11):1494–1507.

    Article  PubMed  CAS  Google Scholar 

  28. Oddone A, Lorentzen E, Basquin J et al. Structural and biochemical characterization of the yeast exosome component Rrp40. EMBO Rep 2007; 8(1):63–69.

    Article  PubMed  CAS  Google Scholar 

  29. Jarrige A, Brechemier-Baey D, Mathy N et al. Mutational analysis of polynucleotide phosphorylase from Escherichia coli. J Mol Biol 2002; 321(3):397–409.

    Article  PubMed  CAS  Google Scholar 

  30. Lorentzen E, Basquin J, Tomecki R et al. 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(6):717–728.

    Article  PubMed  CAS  Google Scholar 

  31. Schneider C, Anderson JT, Tollervey D. The exosome subunit Rrp44 plays a direct role in RNA substrate recognition. Mol Cell 2007; 27(2):324–331.

    Article  PubMed  CAS  Google Scholar 

  32. Chen CY, Gherzi R, Ong SE et al. AU binding proteins recruit the exosome to degrade ARE-containing mRNAs. Cell 2001; 107(4):451–464.

    Article  PubMed  CAS  Google Scholar 

  33. Frazao C, McVey CE, Amblar M et al. Unravelling the dynamics of RNA degradation by ribonuclease II and its RNA-bound complex. Nature 2006; 443(7107):110–114.

    Article  PubMed  CAS  Google Scholar 

  34. Wall D, Kolenbrander PE, Kaiser D. The Myxococcus xanthus pilQ (sglA) gene encodes a secretin homolog required for Type IV pilus biogenesis, social motility and development. J Bacteriol 1999; 181(1):24–33.

    PubMed  CAS  Google Scholar 

  35. Arcus VL, Backbro K, Roos A et al. Distant structural homology leads to the functional characterization of an archaeal PIN domain as an exonuclease. J Biol Chem 2004; 279(16):16471–16478.

    Article  PubMed  CAS  Google Scholar 

  36. Jeyakanthan J, Inagaki E, Kuroishi C et al. Structure of PIN-domain protein PH0500 from Pyrococcus horikoshii. Acta Crystallogr Sect F Struct Biol Cryst Commun 2005; 61(Pt 5):463–468.

    Article  PubMed  Google Scholar 

  37. Glavan F, Behm-Ansmant I, Izaurralde E et al. Structures of the PIN domains of SMG6 and SMG5 reveal a nuclease within the mRNA surveillance complex. EMBO J 2006; 25(21):5117–5125.

    Article  PubMed  CAS  Google Scholar 

  38. De Vivo M, Dal Peraro M, Klein ML. Phosphodiester cleavage in ribonuclease H occurs via an associative two-metal-aided catalytic mechanism. J Am Chem Soc 2008; 130(33): 10955–10962.

    Article  PubMed  Google Scholar 

  39. Steitz TA, Steitz JA. A general two-metal-ion mechanism for catalytic RNA. Proc Natl Acad Sci USA 1993; 90(14):6498–6502.

    Article  PubMed  CAS  Google Scholar 

  40. Cheng ZF, Deutscher MP. Purification and characterization of the Escherichia coli exoribonuclease RNase R. Comparison with RNase II. J Biol Chem 2002; 277(24):21624–21629.

    Article  PubMed  CAS  Google Scholar 

  41. Cheng ZF, Deutscher MP. An important role for RNase R in mRNA decay. Mol Cell 2005; 17(2):313–318.

    Article  PubMed  CAS  Google Scholar 

  42. Wang HW, Wang J, Ding F et al. Architecture of the yeast Rrp44 exosome complex suggests routes of RNA recruitment for 3′ end processing. Proc Natl Acad Sci USA 2007; 104(43): 16844–16849.

    Article  PubMed  CAS  Google Scholar 

  43. Hernandez H, Dziembowski A, Taverner T et al. Subunit architecture of multimeric complexes isolated directly from cells. EMBO Rep 2006; 7(6):605–610.

    PubMed  CAS  Google Scholar 

  44. Midtgaard SF, Assenholt J, Jonstrup AT et al. 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(32):11898–11903.

    Article  PubMed  CAS  Google Scholar 

  45. Zuo Y, Wang Y, Malhotra A. Crystal structure of Escherichia coli RNase D, an exoribonuclease involved in structured RNA processing. Structure 2005; 13(7):973–984.

    Article  PubMed  CAS  Google Scholar 

  46. Phillips S, Butler JS. Contribution of domain structure to the RNA 3′ end processing and degradation functions ofthe nuclear exosome subunit Rrp6p. RNA 2003; 9(9):1098–1107.

    Article  PubMed  CAS  Google Scholar 

  47. Ollis DL, Brick P, Hamlin R et al. Structure of large fragment of Escherichia coli DNA polymerase I complexed with dTMP. Nature 1985; 313(6005):762–766.

    Article  PubMed  CAS  Google Scholar 

  48. Beese LS, Steitz TA. Structural basis for the 3′-5′exonuclease activity of Escherichia coli DNA polymerase I: a two metal ion mechanism. EMBO J 1991; 10(1):25–33.

    PubMed  CAS  Google Scholar 

  49. Cristodero M, Bottcher B, Diepholz M et al. The Leishmania tarentolae exosome: purification and structural analysis by electron microscopy. Mol Biochem Parasitol 2008; 159(1):24–29.

    Article  PubMed  CAS  Google Scholar 

  50. Lehner B, Sanderson CM. A protein interaction framework for human mRNA degradation. Genome Res 2004; 14(7):1315–1323.

    Article  PubMed  CAS  Google Scholar 

  51. Callahan KP, Butler JS. Evidence for core exosome independent function of the nuclear exoribonuclease Rrp6p. Nucleic Acids Res 2008; 36(21):6645–6655.

    Article  PubMed  CAS  Google Scholar 

  52. Callahan KP, Butler JS. TRAMP complex enhances RNA degradation by the nuclear exosome component Rrp6. J Biol Chem 2010; 285(6):3540–3547.

    Article  PubMed  CAS  Google Scholar 

  53. Bayne EH, White SA, Allshire RC. DegrAAAded into silence. Cell 2007; 129(4):651–653.

    Article  PubMed  CAS  Google Scholar 

  54. Houseley J, Tollervey D. The nuclear RNA surveillance machinery: the link between ncRNAs and genome structure in budding yeast? Biochim Biophys Acta 2008; 1779(4):239–246.

    PubMed  CAS  Google Scholar 

  55. Lebreton A, Seraphin B. Exosome-mediated quality control: substrate recruitment and molecular activity. Biochim Biophys Acta 2008; 1779(9):558–565.

    PubMed  CAS  Google Scholar 

  56. Mitchell P, Petfalski E, Shevchenko A et al. The exosome: a conserved eukaryotic RNA processing complex containing multiple 3′→5′ exoribonucleases. Cell 1997; 91(4):457–466.

    Article  PubMed  CAS  Google Scholar 

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Januszyk, K., Lima, C.D. (2010). Structural Components and Architectures of RNA Exosomes. In: Jensen, T.H. (eds) RNA Exosome. Advances in Experimental Medicine and Biology, vol 702. Springer, New York, NY. https://doi.org/10.1007/978-1-4419-7841-7_2

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