Skip to main content
SpringerLink
Log in

The Bacterial Counterparts of the Eukaryotic Exosome: An Evolutionary Perspective

  • Protocol
  • First Online:
The Eukaryotic RNA Exosome

Part of the book series: Methods in Molecular Biology ((MIMB,volume 2062))

Abstract

There are striking similarities between the processes of RNA degradation in bacteria and eukaryotes, which rely on the same basic set of enzymatic activities. In particular, enzymes that catalyze 3′→5′ RNA decay share evolutionary relationships across the three domains of life. Over the years, a large body of biochemical and structural data has been generated that elucidated the mechanism of action of these enzymes. In this overview, to trace the evolutionary origins of the multisubunit RNA exosome complex, we compare the structural and functional characteristics of the eukaryotic and prokaryotic exoribonucleolytic activities.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Protocol
USD 49.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 109.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 139.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 199.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Similar content being viewed by others

References

  1. Sikorska N, Zuber H, Gobert A, Lange H, Gagliardi D (2017) RNA degradation by the plant RNA exosome involves both phosphorolytic and hydrolytic activities. Nat Commun 8:2162

    Article  PubMed  PubMed Central  Google Scholar 

  2. Labno A, Tomecki R, Dziembowski A (2016) Cytoplasmic RNA decay pathways - enzymes and mechanisms. Biochim Biophys Acta 1863:3125–3147

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  4. Makino DL, Schuch B, Stegmann E, Baumgartner M, Basquin C, Conti E (2015) RNA degradation paths in a 12-subunit nuclear exosome complex. Nature 524:54–58

    Article  CAS  PubMed  Google Scholar 

  5. Deutscher MP, Reuven NB (1991) Enzymatic basis for hydrolytic versus phosphorolytic mRNA degradation in Escherichia coli and Bacillus subtilis. Proc Natl Acad Sci U S A 88:3277–3280

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Arraiano CM, Matos RG, Barbas A (2010) RNase II: the finer details of the modus operandi of a molecular killer. RNA Biol 7:276–281

    Article  CAS  PubMed  Google Scholar 

  7. Cannistraro VJ, Kennell D (1994) The processive reaction mechanism of ribonuclease II. J Mol Biol 243:930–943

    Article  CAS  PubMed  Google Scholar 

  8. Barbas A, Matos RG, Amblar M, Lopez-Vinas E, Gomez-Puertas P, Arraiano CM (2009) Determination of key residues for catalysis and RNA cleavage specificity: one mutation turns RNase II into a “SUPER-ENZYME”. J Biol Chem 284:20486–20498

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Frazao C, McVey CE, Amblar M, Barbas A, Vonrhein C, Arraiano CM, Carrondo MA (2006) Unravelling the dynamics of RNA degradation by ribonuclease II and its RNA-bound complex. Nature 443:110–114

    Article  CAS  PubMed  Google Scholar 

  10. Amblar M, Barbas A, Fialho AM, Arraiano CM (2006) Characterization of the functional domains of Escherichia coli RNase II. J Mol Biol 360:921–933

    Article  CAS  PubMed  Google Scholar 

  11. Barbas A, Matos RG, Amblar M, Lopez-Vinas E, Gomez-Puertas P, Arraiano CM (2008) 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

    Article  CAS  PubMed  Google Scholar 

  12. Matos RG, Barbas A, Gomez-Puertas P, Arraiano CM (2011) Swapping the domains of exoribonucleases RNase II and RNase R: conferring upon RNase II the ability to degrade ds RNA. Proteins 79:1853–1867

    Article  CAS  PubMed  Google Scholar 

  13. Matos RG, Barria C, Moreira RN, Barahona S, Domingues S, Arraiano CM (2014) The importance of proteins of the RNase II/RNB-family in pathogenic bacteria. Front Cell Infect Microbiol 4:68

    Article  PubMed  PubMed Central  Google Scholar 

  14. Spickler C, Mackie GA (2000) Action of RNase II and polynucleotide phosphorylase against RNAs containing stem-loops of defined structure. J Bacteriol 182:2422–2427

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Matos RG, Barbas A, Arraiano CM (2010) Comparison of EMSA and SPR for the characterization of RNA-RNase II complexes. Protein J 29:394–397

    Article  CAS  PubMed  Google Scholar 

  16. Matos RG, Barbas A, Arraiano CM (2009) RNase R mutants elucidate the catalysis of structured RNA: RNA-binding domains select the RNAs targeted for degradation. Biochem J 423:291–301

    Article  CAS  PubMed  Google Scholar 

  17. Reis FP et al (2013) Modulating the RNA processing and decay by the exosome: altering Rrp44/Dis3 activity and end-product. PLoS One 8:e76504

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Amblar M, Arraiano CM (2005) A single mutation in Escherichia coli ribonuclease II inactivates the enzyme without affecting RNA binding. FEBS J 272:363–374

    Article  CAS  PubMed  Google Scholar 

  19. Charpentier X, Faucher SP, Kalachikov S, Shuman HA (2008) Loss of RNase R induces competence development in Legionella pneumophila. J Bacteriol 190:8126–8136

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. 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

    Article  CAS  PubMed  Google Scholar 

  21. Lorentzen E, Basquin J, Tomecki R, Dziembowski A, Conti E (2008) 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

    Article  CAS  PubMed  Google Scholar 

  22. Makino DL, Baumgartner M, Conti E (2013) Crystal structure of an RNA-bound 11-subunit eukaryotic exosome complex. Nature 495:70–75

    Article  CAS  PubMed  Google Scholar 

  23. Vincent HA, Deutscher MP (2009) The roles of individual domains of RNase R in substrate binding and exoribonuclease activity. The nuclease domain is sufficient for digestion of structured RNA. J Biol Chem 284:486–494

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Chu LY, Hsieh TJ, Golzarroshan B, Chen YP, Agrawal S, Yuan HS (2017) Structural insights into RNA unwinding and degradation by RNase R. Nucleic Acids Res 45:12015–12024

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Bonneau F, Basquin J, Ebert J, Lorentzen E, Conti E (2009) The yeast exosome functions as a macromolecular cage to channel RNA substrates for degradation. Cell 139:547–559

    Article  CAS  PubMed  Google Scholar 

  26. Han J, van Hoof A (2016) The RNA exosome channeling and direct access conformations have distinct in vivo functions. Cell Rep 16:3348–3358

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Schneider C, Tollervey D (2013) Threading the barrel of the RNA exosome. Trends Biochem Sci 38:485–493

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Tomecki R, Drazkowska K, Dziembowski A (2010) Mechanisms of RNA degradation by the eukaryotic exosome. Chembiochem 11:938–945

    Article  CAS  PubMed  Google Scholar 

  29. Wang HW et al (2007) Architecture of the yeast Rrp44 exosome complex suggests routes of RNA recruitment for 3′ end processing. Proc Natl Acad Sci U S A 104:16844–16849

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Januszyk K, Lima CD (2014) The eukaryotic RNA exosome. Curr Opin Struct Biol 24:132–140

    Article  CAS  PubMed  Google Scholar 

  31. Lebreton A, Tomecki R, Dziembowski A, Seraphin B (2008) Endonucleolytic RNA cleavage by a eukaryotic exosome. Nature 456:993–996

    Article  CAS  PubMed  Google Scholar 

  32. Schaeffer D et al (2009) The exosome contains domains with specific endoribonuclease, exoribonuclease and cytoplasmic mRNA decay activities. Nat Struct Mol Biol 16:56–62

    Article  CAS  PubMed  Google Scholar 

  33. Schneider C, Leung E, Brown J, Tollervey D (2009) The N-terminal PIN domain of the exosome subunit Rrp44 harbors endonuclease activity and tethers Rrp44 to the yeast core exosome. Nucleic Acids Res 37:1127–1140

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Schaeffer D, Reis FP, Johnson SJ, Arraiano CM, van Hoof A (2012) The CR3 motif of Rrp44p is important for interaction with the core exosome and exosome function. Nucleic Acids Res 40:9298–9307

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Lubas M, Damgaard CK, Tomecki R, Cysewski D, Jensen TH, Dziembowski A (2013) Exonuclease hDIS3L2 specifies an exosome-independent 3′-5′ degradation pathway of human cytoplasmic mRNA. EMBO J 32:1855–1868

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Malecki M, Viegas SC, Carneiro T, Golik P, Dressaire C, Ferreira MG, Arraiano CM (2013) The exoribonuclease Dis3L2 defines a novel eukaryotic RNA degradation pathway. EMBO J 32:1842–1854

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Staals RH et al (2010) Dis3-like 1: a novel exoribonuclease associated with the human exosome. EMBO J 29:2358–2367

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Tomecki R et al (2010) The human core exosome interacts with differentially localized processive RNases: hDIS3 and hDIS3L. EMBO J 29:2342–2357

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Grunberg-Manago M (1963) Enzymatic synthesis of nucleic acids. Prog Biophys Mol Biol 13:175–239

    Article  CAS  PubMed  Google Scholar 

  40. Wang G, Shimada E, Zhang J, Hong JS, Smith GM, Teitell MA, Koehler CM (2012) Correcting human mitochondrial mutations with targeted RNA import. Proc Natl Acad Sci U S A 109:4840–4845

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Arraiano CM et al (2010) The critical role of RNA processing and degradation in the control of gene expression. FEMS Microbiol Rev 34:883–923

    Article  CAS  PubMed  Google Scholar 

  42. Arraiano CM, Mauxion F, Viegas SC, Matos RG, Seraphin B (2013) Intracellular ribonucleases involved in transcript processing and decay: precision tools for RNA. Biochim Biophys Acta 1829:491–513

    Article  CAS  PubMed  Google Scholar 

  43. Carpousis AJ, Van Houwe G, Ehretsmann C, Krisch HM (1994) 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

    Article  CAS  PubMed  Google Scholar 

  44. Iost I, Dreyfus M (2006) DEAD-box RNA helicases in Escherichia coli. Nucleic Acids Res 34:4189–4197

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Miczak A, Kaberdin VR, Wei CL, Lin-Chao S (1996) Proteins associated with RNase E in a multicomponent ribonucleolytic complex. Proc Natl Acad Sci U S A 93:3865–3869

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Py B, Higgins CF, Krisch HM, Carpousis AJ (1996) A DEAD-box RNA helicase in the Escherichia coli RNA degradosome. Nature 381:169–172

    Article  CAS  PubMed  Google Scholar 

  47. Vanzo NF et al (1998) Ribonuclease E organizes the protein interactions in the Escherichia coli RNA degradosome. Genes Dev 12:2770–2781

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Lin PH, Lin-Chao S (2005) RhlB helicase rather than enolase is the beta-subunit of the Escherichia coli polynucleotide phosphorylase (PNPase)-exoribonucleolytic complex. Proc Natl Acad Sci U S A 102:16590–16595

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Coburn GA, Miao X, Briant DJ, Mackie GA (1999) Reconstitution of a minimal RNA degradosome demonstrates functional coordination between a 3′ exonuclease and a DEAD-box RNA helicase. Genes Dev 13:2594–2603

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Mohanty BK, Maples VF, Kushner SR (2004) The Sm-like protein Hfq regulates polyadenylation dependent mRNA decay in Escherichia coli. Mol Microbiol 54:905–920

    Article  CAS  PubMed  Google Scholar 

  51. Nurmohamed S, Vaidialingam B, Callaghan AJ, Luisi BF (2009) 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 389:17–33

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Shi Z, Yang WZ, Lin-Chao S, Chak KF, Yuan HS (2008) Crystal structure of Escherichia coli PNPase: central channel residues are involved in processive RNA degradation. RNA 14:2361–2371

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  54. Hardwick SW, Gubbey T, Hug I, Jenal U, Luisi BF (2012) Crystal structure of Caulobacter crescentus polynucleotide phosphorylase reveals a mechanism of RNA substrate channelling and RNA degradosome assembly. Open Biol 2:120028

    Article  PubMed  PubMed Central  Google Scholar 

  55. Bermudez-Cruz RM, Fernandez-Ramirez F, Kameyama-Kawabe L, Montanez C (2005) Conserved domains in polynucleotide phosphorylase among eubacteria. Biochimie 87:737–745

    Article  CAS  PubMed  Google Scholar 

  56. Leszczyniecka M, DeSalle R, Kang DC, Fisher PB (2004) The origin of polynucleotide phosphorylase domains. Mol Phylogenet Evol 31:123–130

    Article  CAS  PubMed  Google Scholar 

  57. Garcia-Mena J, Das A, Sanchez-Trujillo A, Portier C, Montanez C (1999) A novel mutation in the KH domain of polynucleotide phosphorylase affects autoregulation and mRNA decay in Escherichia coli. Mol Microbiol 33:235–248

    Article  CAS  PubMed  Google Scholar 

  58. Jarrige A, Brechemier-Baey D, Mathy N, Duche O, Portier C (2002) Mutational analysis of polynucleotide phosphorylase from Escherichia coli. J Mol Biol 321:397–409

    Article  CAS  PubMed  Google Scholar 

  59. Casinhas J, Matos RG, Haddad N, Arraiano CM (2018) Biochemical characterization of Campylobacter jejuni PNPase, an exoribonuclease important for bacterial pathogenicity. Biochimie 147:70–79

    Article  CAS  PubMed  Google Scholar 

  60. Stickney LM, Hankins JS, Miao X, Mackie GA (2005) Function of the conserved S1 and KH domains in polynucleotide phosphorylase. J Bacteriol 187:7214–7221

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Gas ME, Seraphin B (2010) Twins take the job. EMBO J 29:2260–2261

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

This work was supported by project Lisboa-01-0145-FEDER-007660 (Microbiologia Molecular, Estrutural e Celular) funded by FEDER through COMPETE 2020—Programa Operacional Competitividade e Internacionalização (POCI) and by project PTDC/BIM-MEC/3749/2014 to SCV, project PTDC/BIA-BQM/28479/2017 to RGM and project PTDC/BIAMIC/1399/2014 to CMA, funded by Fundação para a Ciência e Tecnologia, Portugal (FCT). SCV was financed by FCT program IF (ref. IF/00217/2015); RGM was financed by an FCT contract (ref. CEECIND/02065/2017).

Author information

Authors and Affiliations

  1. Instituto de Tecnologia Química e Biológica António Xavier, Oeiras, Portugal

    Sandra C. Viegas, Rute G. Matos & Cecília M. Arraiano

Authors
  1. Sandra C. Viegas
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Rute G. Matos
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Cecília M. Arraiano
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Sandra C. Viegas or Cecília M. Arraiano .

Editor information

Editors and Affiliations

  1. Laboratory of Cellular and Structural Biology, The Rockefeller University, New York, NY, USA

    John LaCava

  2. Central European Institute of Technology (CEITEC), Masaryk University, Brno, Czech Republic

    Štěpánka Vaňáčová

Rights and permissions

Reprints and permissions

Copyright information

© 2020 Springer Science+Business Media, LLC, part of Springer Nature

About this protocol

Check for updates. Verify currency and authenticity via CrossMark

Cite this protocol

Viegas, S.C., Matos, R.G., Arraiano, C.M. (2020). The Bacterial Counterparts of the Eukaryotic Exosome: An Evolutionary Perspective. In: LaCava, J., Vaňáčová, Š. (eds) The Eukaryotic RNA Exosome. Methods in Molecular Biology, vol 2062. Humana, New York, NY. https://doi.org/10.1007/978-1-4939-9822-7_2

Download citation

  • DOI: https://doi.org/10.1007/978-1-4939-9822-7_2

  • Published:

  • Publisher Name: Humana, New York, NY

  • Print ISBN: 978-1-4939-9821-0

  • Online ISBN: 978-1-4939-9822-7

  • eBook Packages: Springer Protocols

Publish with us

Policies and ethics

Search

Navigation