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RNA Exosome pp 39-49 | Cite as

The Exosomes of Trypanosomes and Other Protists

  • Christine Clayton
  • Antonio Estevez
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 702)

Abstract

The archaeal exosome contains three heterodimeric RNase PH subunits, forming a hexamer with RNase activity; on top sits a trimer of two different SI domain proteins. In animals and yeast, six different, but related subunits form the RNase PH-like core, but these lack enzyme activity; there are three different Si-domain proteins and enzyme activity is provided by the endo/exonuc lease Rrp44 or—mainly in the nuclear exosome—the Rnase D enzyme Rrp6. Trypanosomes diverged from yeast and mammals very early in eukaryotic evolution. The trypanosome exosome is similar in subunit composition to the human exosome, but instead of being an optional component, trypanosome RRP6 is present in the nucleus and cytoplasm and is required for exosome stability. As in human cells and yeast, the trypanosome exosome has been shown to be required for processing and quality control of rRNA and to be involved in mRNA degradation. Electron microscopy results for a Leishmania exosome suggest that RRP6 is located on the side of the RnasePH ring, interacting with several exosome core proteins. Results of a search for exosome subunits in the genomes of widely diverged protists revealed varied exosome complexity; the Giardia exosome may be as simple as that of Archaea.

Keywords

mRNA Degradation Stress Granule Trypanosoma Brucei Thalassiosira Pseudonana Bloodstream Form 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. 1.
    Lorentzen E, Dziembowskiw A, Lindner D et al. RNA channelling by the archaeal exosome. EMBO Rep 2007; 8:470–476.PubMedCrossRefGoogle Scholar
  2. 2.
    Liu Q, Greimann JC, Lima CD. Reconstitution, activities and structure of the eukaryotic RNA exosome. Cell 2006; 127:1223–1237.PubMedCrossRefGoogle Scholar
  3. 3.
    Raijmakers R, Schilders G, Pruijn GJ. The exosome, a molecular machine for controlled RNA degradation in both nucleus and cytoplasm. Eur J Cell Biol 2004; 83:175–183.PubMedCrossRefGoogle Scholar
  4. 4.
    Mitchell P, Petfalski E, Houalla R et al. Rrp47p is an exosome-associated protein required forthe 3′ processing of stable RNAs. Mol Cell Biol 2003; 23:6982–6992.PubMedCrossRefGoogle Scholar
  5. 5.
    Chekanova JA, Shaw RJ, Wills MA et al. Poly(A) tail-dependent exonuclease AtRrp41p from Arabidopsis thaliana rescues 5.8 S rRNA processing and mRNA decay defects of the yeast ski6 mutant and is found in an exosome-sized complex in plant and yeast cells. J Biol Chem 2000; 275.Google Scholar
  6. 6.
    Zimmer S, Fei Z, Stern D. Genome-based analysis of Chlamydomonas reinhardtii exoribonucleases and poly(A) polymerases predicts unexpected organellar and exosomal features. Genetics 2008; 179:125–136.PubMedCrossRefGoogle Scholar
  7. 7.
    Lange H, Holec S, Cognat V et al. Degradation of a polyadenylated rRNA maturation by-product involves one of the three RRP6-like proteins in Arabidopsis thaliana. Mol Cell Biol 2008; 28:3038–3044.PubMedCrossRefGoogle Scholar
  8. 8.
    Liu Q, Greimann J, Lima C. Reconstitution, Activities and Structure of the Eukaryotic RNA Exosome. Cell 2007; 131:188–189.CrossRefGoogle Scholar
  9. 9.
    Chekanova J, Dutko J, Mian I et al. Arabidopsis thaliana exosome subunit AtRrp4p is a hydrolytic 3′→5′ exonuclease containing S1 and KH RNA-binding domains. Nucleic Acids Res 2002; 30:695–700.PubMedCrossRefGoogle Scholar
  10. 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; 14:15–22.PubMedCrossRefGoogle Scholar
  11. 11.
    Schaeffer D, Tsanova B, Barbas A et al. The exosome contains domains with specific endoribonuclease, exoribonuclease and cytoplasmic mRNA decay activities. Nat Struct Mol Biol 2008; 16:56–62.PubMedCrossRefGoogle Scholar
  12. 12.
    Schneider C, Anderson J, Tollervey D. The exosome subunit rrp44 plays a direct role in RNA substrate recognition. Mol Cell 2007; 27:324–331.PubMedCrossRefGoogle Scholar
  13. 13.
    Lehner B, Sanderson CM. A protein interaction framework for human mRNA degradation. Genome Res 2004; 14:1315–1323.PubMedCrossRefGoogle Scholar
  14. 14.
    Palenchar JB, Bellofatto V. Gene transcription in trypanosomes. Mol Biochem Parasitol 2006; 146:135–141.PubMedCrossRefGoogle Scholar
  15. 15.
    Liang X, Haritan A, Uliel S et al. Trans and cis splicing in trypanosomatids: mechanism, factors and regulation. Eukaryot Cell 2003; 2:830–840.PubMedCrossRefGoogle Scholar
  16. 16.
    Ivens ACea. The genome of the kinetoplastid parasite, Leishmania major. Science 2005; 309–442.Google Scholar
  17. 17.
    Berriman Mea The genome of the African trypanosome, Trypanosoma brucei. Science 2005; 309:416–422.PubMedCrossRefGoogle Scholar
  18. 18.
    Clayton C, Shapira M. Post-transcriptional regulation of gene expression in trypanosomes and leishmanias. Mol Biochem Parasitol 2007; 156:93–101.PubMedCrossRefGoogle Scholar
  19. 19.
    Haile S, Papadopoulou B. Developmental regulation of gene expression in trypanosomatid parasitic protozoa. Curr Opin Microbiol 2007; 10:569–577.PubMedCrossRefGoogle Scholar
  20. 20.
    Estévez AM, Lehner B, Sanderson CM et al. The roles of inter-subunit interactions in exosome stability. J Biol Chem 2003; 278:34943–34951.PubMedCrossRefGoogle Scholar
  21. 21.
    Estévez A, Kempf T, Clayton CE. The exosome of Trypanosoma brucei. EMBO J 2001; 20:3831–3839.PubMedCrossRefGoogle Scholar
  22. 22.
    van Dijk E, Schilders G, Pruijn G. Human cell growth requires a functional cytoplasmic exosome, which is involved in various mRNA decay pathways. RNA 2007; 13:1027–1035.PubMedCrossRefGoogle Scholar
  23. 23.
    Haile S, Cristodero M, Clayton C et al. The subcellular localisation of trypanosome RRP6 and its association with the exosome. Mol Biochem Parasitol 2007; 151:52–58.PubMedCrossRefGoogle Scholar
  24. 24.
    Cristodero M, Böttcher B, Diepholz M et al. The exosome of Leishmania tarentolae: purification and structural analysis by electron microscopy. Mol Biochem Parasitol 2008; 159:24–29.PubMedCrossRefGoogle Scholar
  25. 25.
    LaCava J, Houseley J, Saveanu C et al. RNA degradation by the exosome Is promoted by a nuclear polyadenylation complex. Cell 2005; 121:713–724.PubMedCrossRefGoogle Scholar
  26. 26.
    Houseley J, Tollervey D. Yeast Trf5p is a nuclear poly(A) polymerase. EMBO Rep 2006; 7:205–211.PubMedCrossRefGoogle Scholar
  27. 27.
    Cristodero M, Clayton C. Trypanosome MTR4 in involved in ribosomal RNA processing. Nucleic Acids Res 2007; 35:7023–7030.PubMedCrossRefGoogle Scholar
  28. 28.
    Decuypere S, Vandesompele J, Yardley V et al. Differential polyadenylation of ribosomal RNA during posttranscriptional processing in Leishmania. Parasitology 2005; 131:321–329.PubMedCrossRefGoogle Scholar
  29. 29.
    Kabani S, Fenn K, Ross A et al. Genome-wide expression profiling of in vivo-derived bloodstream parasite stages and dynamic analysis of mRNA alterations during synchronous differentiation in Trypanosoma brucei. BMC Genomics 2009; 10:427.PubMedCrossRefGoogle Scholar
  30. 30.
    Queiroz R, Benz C, Fellenberg K et al. Transcriptome analysis of differentiating trypanosomes reveals the existence of multiple posttranscriptional regulons. BMC Genomics 2009; 10:495.PubMedCrossRefGoogle Scholar
  31. 31.
    Jensen B, Sivam D, Kifer C et al. Widespread variation in transcript abundance within and across developmental stages of Trypanosoma brucei. BMC Genomics 2009; 10:482.PubMedCrossRefGoogle Scholar
  32. 32.
    Haanstra J, Stewart M, Luu V-D et al. Control and regulation of gene expression: quantitative analysis of the expression of phosphoglycerate kinase in bloodstream form Trypanosoma brucei. J Biol Chem 2008; 283:2495–2507.PubMedCrossRefGoogle Scholar
  33. 33.
    Mayho M, Fenn K, Craddy P et al. Post-transcriptional control of nuclear-encoded cytochrome oxidase subunits in Trypanosoma brucei: evidence for genome-wide conservation of life-cycle stage-specific regulatory elements. Nucleic Acids Res 2006; 34:5312–5324.PubMedCrossRefGoogle Scholar
  34. 34.
    Gunzl A, Bruderer T, Laufer G et al. RNA polymerase I transcribes procyclin genes and variant surface glycoprotein gene expression sites in Trypanosoma brucei. Eukaryot Cell 2003; 2:542–551.PubMedCrossRefGoogle Scholar
  35. 35.
    Hotz H-R, Biebinger S, Flaspohler J et al. PARP gene expression: regulation at many levels. Mol Biochem Parasitol 1998; 91:131–143.PubMedCrossRefGoogle Scholar
  36. 36.
    Stoecklin G, Mayo T, Anderson P. ARE-mRNA degradation requires the 5′—3′ decay pathway. EMBO Rep 2006; 7:72–77.PubMedCrossRefGoogle Scholar
  37. 37.
    Orban TI, Izaurralde E. Decay of mRNAs targeted by RISC requires XRN1, the Ski complex and the exosome. RNA 2005; 11:459–469.PubMedCrossRefGoogle Scholar
  38. 38.
    Haile S, Dupe A, Papadopoulou B. Deadenylation-independent stage-specific mRNA degradation in Leishmania. Nucleic Acids Res 2008; 36:1634–1644.PubMedCrossRefGoogle Scholar
  39. 39.
    Schwede A, Manful T, Jha B et al. The role of deadenylation in the degradation of unstable mRNAs in trypanosomes. Nucleic Acids Res 2009; 37:5511–5528.PubMedCrossRefGoogle Scholar
  40. 40.
    Haile S, Estévez AM, Clayton C. A role for the exosome in the initiation of degradation of unstable mRNAs. RNA 2003; 9:1491–1501.PubMedCrossRefGoogle Scholar
  41. 41.
    Schwede A, Ellis L, Luther J et al. A role for Caf1 in mRNA deadenylation and decay in trypanosomes and human cells. Nucleic Acids Res 2008; 36:3374–3388.PubMedCrossRefGoogle Scholar
  42. 42.
    Li C-H, Irmer H, Gudjonsdottir-Planck D et al. Roles of a Trypanosoma brucei 5′→3′ exoribonuclease homologue in mRNA degradation. RNA 2006; 12:2171–2186.PubMedCrossRefGoogle Scholar
  43. 43.
    Irmer H, Clayton CE. Degradation of the EP1 mRNA in Trypanosoma brucei is initiated by destruction of the 3′-untranslated region. Nucleic Acids Res 2001; 29:4707–4715.PubMedCrossRefGoogle Scholar
  44. 44.
    Anderson P, Kedersha N. RNA granules: posttranscriptional and epigenetic modulators of gene expression. Nat Rev Mol Cell Biol 2009; 10:430–436.PubMedCrossRefGoogle Scholar
  45. 45.
    Buchan J, Parker R. Eukaryotic stress granules: the ins and outs of translation. Mol Cell 2009; 36:932–941.PubMedCrossRefGoogle Scholar
  46. 46.
    Kramer S, Queiroz R, Ellis L et al. Stress granules and the heat shock response in Trypanosoma brucei. J Cell Sci 2008; 121:3002–3014.PubMedCrossRefGoogle Scholar
  47. 47.
    Holetz F, Correa A, Avila A et al. Evidence of P-body-like structures in Trypanosoma cruzi. Biochem Biophys Res Commun 2007; 356:1062–1067.PubMedCrossRefGoogle Scholar
  48. 48.
    Chowdhury A, Mukhopadhyay J, Tharun S. The decapping activator Lsm1p-7p-Pat1p complex has the intrinsic ability to distinguish between oligoadenylated and polyadenylated RNAs. RNA 2007.Google Scholar
  49. 49.
    Liu Q, Liang X, Uliel S et al. Identification and Functional Characterization of Lsm Proteins in Trypanosoma brucei. J Biol Chem 2004; 279:18210–18219.PubMedCrossRefGoogle Scholar
  50. 50.
    Rodnguez-Ezpeleta N, Brinkmann H, Burger G et al. Toward resolving the eukaryotic tree: the phylogenetic positions of Jakobids and Cercozoans. Curr Biol 2007; 17:1420–1425.CrossRefGoogle Scholar

Copyright information

© Landes Bioscience and Springer Science+Business Media 2010

Authors and Affiliations

  • Christine Clayton
    • 1
  • Antonio Estevez
    • 2
  1. 1.Zentrum für Molekulare Biologie der Universität HeidelbergHeidelbergGermany
  2. 2.Instituto de parasitologia y Biomedicina “Lopez-Neyra”, CSICGranadaSpain

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