RNA Polyadenylation in Archaea: Not Observed in Haloferax While the Exosome Polynucleotidylates RNA in Sulfolobus

Overview

Journal EMBO Rep

Specialty Molecular Biology

Date 2005 Nov 12

PMID 16282984

Citations 34

Authors

Victoria Portnoy

Elena Evguenieva-Hackenberg

Franziska Klein

Pamela Walter

Esben Lorentzen

Gabriele Klug

Gadi Schuster

Affiliations

Soon will be listed here.

Abstract

The addition of poly(A) tails to RNA is a phenomenon common to all organisms examined so far. No homologues of the known polyadenylating enzymes are found in Archaea and little is known concerning the mechanisms of messenger RNA degradation in these organisms. Hyperthermophiles of the genus Sulfolobus contain a protein complex with high similarity to the exosome, which is known to degrade RNA in eukaryotes. Halophilic Archaea, however, do not encode homologues of these eukaryotic exosome components. In this work, we analysed RNA polyadenylation and degradation in the archaea Sulfolobus solfataricus and Haloferax volcanii. No RNA polyadenylation was detected in the halophilic archaeon H. volcanii. However, RNA polynucleotidylation occurred in hyperthermophiles of the genus Sulfolobus and was mediated by the archaea exosome complex. Together, our results identify the first organism without RNA polyadenylation and show a polyadenylation activity of the archaea exosome.

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References

Van Hoof A, Parker R . The exosome: a proteasome for RNA?. Cell. 1999; 99(4):347-50. DOI: 10.1016/s0092-8674(00)81520-2. View

Raijmakers R, Schilders G, Pruijn G . The exosome, a molecular machine for controlled RNA degradation in both nucleus and cytoplasm. Eur J Cell Biol. 2004; 83(5):175-83. DOI: 10.1078/0171-9335-00385. View

Koonin E, Wolf Y, 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):240-52. PMC: 311015. DOI: 10.1101/gr.162001. View

Zuo Y, Deutscher M . Exoribonuclease superfamilies: structural analysis and phylogenetic distribution. Nucleic Acids Res. 2001; 29(5):1017-26. PMC: 56904. DOI: 10.1093/nar/29.5.1017. View

Symmons M, Williams M, Luisi B, Jones G, Carpousis A . Running rings around RNA: a superfamily of phosphate-dependent RNases. Trends Biochem Sci. 2002; 27(1):11-8. DOI: 10.1016/s0968-0004(01)01999-5. View

Anantharaman V, Koonin E, Aravind L . Comparative genomics and evolution of proteins involved in RNA metabolism. Nucleic Acids Res. 2002; 30(7):1427-64. PMC: 101826. DOI: 10.1093/nar/30.7.1427. View

Edmonds M . A history of poly A sequences: from formation to factors to function. Prog Nucleic Acid Res Mol Biol. 2002; 71:285-389. DOI: 10.1016/s0079-6603(02)71046-5. View

Kushner S . mRNA decay in Escherichia coli comes of age. J Bacteriol. 2002; 184(17):4658-65; discussion 4657. PMC: 135271. DOI: 10.1128/JB.184.17.4658-4665.2002. View

Dreyfus M, Regnier P . The poly(A) tail of mRNAs: bodyguard in eukaryotes, scavenger in bacteria. Cell. 2002; 111(5):611-3. DOI: 10.1016/s0092-8674(02)01137-6. View

10.

Rott R, Zipor G, Portnoy V, Liveanu V, Schuster G . RNA polyadenylation and degradation in cyanobacteria are similar to the chloroplast but different from Escherichia coli. J Biol Chem. 2003; 278(18):15771-7. DOI: 10.1074/jbc.M211571200. View

11.

Yehudai-Resheff S, Portnoy V, Yogev S, Adir N, Schuster G . Domain analysis of the chloroplast polynucleotide phosphorylase reveals discrete functions in RNA degradation, polyadenylation, and sequence homology with exosome proteins. Plant Cell. 2003; 15(9):2003-19. PMC: 181327. DOI: 10.1105/tpc.013326. View

12.

Evguenieva-Hackenberg E, Walter P, Hochleitner E, Lottspeich F, Klug G . An exosome-like complex in Sulfolobus solfataricus. EMBO Rep. 2003; 4(9):889-93. PMC: 1326366. DOI: 10.1038/sj.embor.embor929. View

13.

Gagliardi D, Stepien P, Temperley R, Lightowlers R, Chrzanowska-Lightowlers Z . Messenger RNA stability in mitochondria: different means to an end. Trends Genet. 2004; 20(6):260-7. DOI: 10.1016/j.tig.2004.04.006. View

14.

Bollenbach T, Schuster G, Stern D . Cooperation of endo- and exoribonucleases in chloroplast mRNA turnover. Prog Nucleic Acid Res Mol Biol. 2004; 78:305-37. DOI: 10.1016/S0079-6603(04)78008-3. View

15.

Xiong Y, Steitz T . Mechanism of transfer RNA maturation by CCA-adding enzyme without using an oligonucleotide template. Nature. 2004; 430(7000):640-5. DOI: 10.1038/nature02711. View

16.

Perrin R, Lange H, Grienenberger J, Gagliardi D . AtmtPNPase is required for multiple aspects of the 18S rRNA metabolism in Arabidopsis thaliana mitochondria. Nucleic Acids Res. 2004; 32(17):5174-82. PMC: 521665. DOI: 10.1093/nar/gkh852. View

17.

Yue D, Maizels N, Weiner A . CCA-adding enzymes and poly(A) polymerases are all members of the same nucleotidyltransferase superfamily: characterization of the CCA-adding enzyme from the archaeal hyperthermophile Sulfolobus shibatae. RNA. 1996; 2(9):895-908. PMC: 1369424. View

18.

Lisitsky I, Klaff P, Schuster G . Addition of destabilizing poly (A)-rich sequences to endonuclease cleavage sites during the degradation of chloroplast mRNA. Proc Natl Acad Sci U S A. 1996; 93(23):13398-403. PMC: 24105. DOI: 10.1073/pnas.93.23.13398. View

19.

Coburn G, Mackie G . Degradation of mRNA in Escherichia coli: an old problem with some new twists. Prog Nucleic Acid Res Mol Biol. 1999; 62:55-108. DOI: 10.1016/s0079-6603(08)60505-x. View

20.

Allmang C, Kufel J, Chanfreau G, Mitchell P, Petfalski E, Tollervey D . Functions of the exosome in rRNA, snoRNA and snRNA synthesis. EMBO J. 1999; 18(19):5399-410. PMC: 1171609. DOI: 10.1093/emboj/18.19.5399. View