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Decay-Initiating Endoribonucleolytic Cleavage by RNase Y Is Kept under Tight Control via Sequence Preference and Sub-cellular Localisation


Ribonucleic acids (RNA) are key intermediates between the heritable genome and the expression of proteins. Thus the level of a specific RNA determines the capability of the cell to produce the corresponding protein. Bacteria maintain a very high turnover (high production but also high decay-rate) of RNA molecules, to ensure that they can, at any time, change the protein production program in response to outside stimuli. However, all types of RNA molecules do not have the same half-life, some last for tens of minutes whereas most only last for seconds. Here we examine how endoribonuclease Y (RNase Y), one of the enzymes that cleave RNA into smaller fragments, chooses its targets from the pool of cellular RNA. We show that RNase Y prefers to cleave RNA at a specific ribonucleotide sequence, thus keeping the RNA degradation to the correct level, not too fast and not too slow. RNase Y is anchored to the inside of the cell envelope, and we furthermore show that releasing RNase Y into the interior of the cell results in poor growth, but is at the same time able to compensate for the loss of CshA, another factor in the RNA decay machinery.


Vyšlo v časopise: Decay-Initiating Endoribonucleolytic Cleavage by RNase Y Is Kept under Tight Control via Sequence Preference and Sub-cellular Localisation. PLoS Genet 11(10): e32767. doi:10.1371/journal.pgen.1005577
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005577

Souhrn

Ribonucleic acids (RNA) are key intermediates between the heritable genome and the expression of proteins. Thus the level of a specific RNA determines the capability of the cell to produce the corresponding protein. Bacteria maintain a very high turnover (high production but also high decay-rate) of RNA molecules, to ensure that they can, at any time, change the protein production program in response to outside stimuli. However, all types of RNA molecules do not have the same half-life, some last for tens of minutes whereas most only last for seconds. Here we examine how endoribonuclease Y (RNase Y), one of the enzymes that cleave RNA into smaller fragments, chooses its targets from the pool of cellular RNA. We show that RNase Y prefers to cleave RNA at a specific ribonucleotide sequence, thus keeping the RNA degradation to the correct level, not too fast and not too slow. RNase Y is anchored to the inside of the cell envelope, and we furthermore show that releasing RNase Y into the interior of the cell results in poor growth, but is at the same time able to compensate for the loss of CshA, another factor in the RNA decay machinery.


Zdroje

1. Anderson KL, Dunman PM (2009) Messenger RNA Turnover Processes in Escherichia coli, Bacillus subtilis, and Emerging Studies in Staphylococcus aureus. Int J Microbiol 2009: 525491. doi: 10.1155/2009/525491 19936110

2. Bandyra KJ, Bouvier M, Carpousis AJ, Luisi BF (2013) The social fabric of the RNA degradosome. Biochim Biophys Acta 1829: 514–522. doi: 10.1016/j.bbagrm.2013.02.011 23459248

3. Laalami S, Zig L, Putzer H (2014) Initiation of mRNA decay in bacteria. Cell Mol Life Sci 71: 1799–1828. doi: 10.1007/s00018-013-1472-4 24064983

4. Shahbabian K, Jamalli A, Zig L, Putzer H (2009) RNase Y, a novel endoribonuclease, initiates riboswitch turnover in Bacillus subtilis. EMBO J 28: 3523–3533. doi: 10.1038/emboj.2009.283 19779461

5. Lehnik-Habrink M, Schaffer M, Mader U, Diethmaier C, Herzberg C, et al. (2011) RNA processing in Bacillus subtilis: identification of targets of the essential RNase Y. Mol Microbiol 81: 1459–1473. doi: 10.1111/j.1365-2958.2011.07777.x 21815947

6. Newman JA, Hewitt L, Rodrigues C, Solovyova A, Harwood CR, et al. (2011) Unusual, dual endo- and exonuclease activity in the degradosome explained by crystal structure analysis of RNase J1. Structure 19: 1241–1251. doi: 10.1016/j.str.2011.06.017 21893285

7. Kaito C, Kurokawa K, Matsumoto Y, Terao Y, Kawabata S, et al. (2005) Silkworm pathogenic bacteria infection model for identification of novel virulence genes. Mol Microbiol 56: 934–944. 15853881

8. Marincola G, Schafer T, Behler J, Bernhardt J, Ohlsen K, et al. (2012) RNase Y of Staphylococcus aureus and its role in the activation of virulence genes. Mol Microbiol 85: 817–832. doi: 10.1111/j.1365-2958.2012.08144.x 22780584

9. Gilet L, DiChiara JM, Figaro S, Bechhofer DH, Condon C (2015) Small stable RNA maturation and turnover in Bacillus subtilis. Mol Microbiol 95: 270–282. doi: 10.1111/mmi.12863 25402410

10. Hunt A, Rawlins JP, Thomaides HB, Errington J (2006) Functional analysis of 11 putative essential genes in Bacillus subtilis. Microbiology 152: 2895–2907. 17005971

11. Lehnik-Habrink M, Newman J, Rothe FM, Solovyova AS, Rodrigues C, et al. (2011) RNase Y in Bacillus subtilis: a Natively disordered protein that is the functional equivalent of RNase E from Escherichia coli. J Bacteriol 193: 5431–5441. doi: 10.1128/JB.05500-11 21803996

12. Redder P, Linder P (2012) New Range of Vectors with a Stringent 5-Fluoroorotic Acid-Based Counterselection System for Generating Mutants by Allelic Replacement in Staphylococcus aureus. Appl Environ Microbiol 78: 3846–3854. doi: 10.1128/AEM.00202-12 22447609

13. Figaro S, Durand S, Gilet L, Cayet N, Sachse M, et al. (2013) Bacillus subtilis mutants with knockouts of the genes encoding ribonucleases RNase Y and RNase J1 are viable, with major defects in cell morphology, sporulation, and competence. J Bacteriol 195: 2340–2348. doi: 10.1128/JB.00164-13 23504012

14. Kang SO, Caparon MG, Cho KH (2010) Virulence gene regulation by CvfA, a putative RNase: the CvfA-enolase complex in Streptococcus pyogenes links nutritional stress, growth-phase control, and virulence gene expression. Infect Immun 78: 2754–2767. doi: 10.1128/IAI.01370-09 20385762

15. Nagata M, Kaito C, Sekimizu K (2008) Phosphodiesterase activity of CvfA is required for virulence in Staphylococcus aureus. J Biol Chem 283: 2176–2184. 17951247

16. Numata S, Nagata M, Mao H, Sekimizu K, Kaito C (2014) CvfA protein and polynucleotide phosphorylase act in an opposing manner to regulate Staphylococcus aureus virulence. J Biol Chem 289: 8420–8431. doi: 10.1074/jbc.M114.554329 24492613

17. Roux CM, Demuth JP, Dunman PM (2011) Characterization of components of the Staphylococcus aureus messenger RNA degradosome holoenzyme-like complex. J Bacteriol.

18. Oun S, Redder P, Didier JP, Francois P, Corvaglia AR, et al. (2013) The CshA DEAD-box RNA helicase is important for quorum sensing control in Staphylococcus aureus. RNA Biol 10: 157–165. doi: 10.4161/rna.22899 23229022

19. Giraud C, Hausmann S, Lemeille S, Prados J, Redder P, et al. (2015) The C-terminal region of the RNA helicase CshA is required for the interaction with the degradosome and turnover of bulk RNA in the opportunistic pathogen Staphylococcus aureus. RNA Biology 12: 658–674. doi: 10.1080/15476286.2015.1035505 25997461

20. Lehnik-Habrink M, Pfortner H, Rempeters L, Pietack N, Herzberg C, et al. (2010) The RNA degradosome in Bacillus subtilis: identification of CshA as the major RNA helicase in the multiprotein complex. Mol Microbiol 77: 958–971. doi: 10.1111/j.1365-2958.2010.07264.x 20572937

21. Carpousis AJ (2007) The RNA degradosome of Escherichia coli: an mRNA-degrading machine assembled on RNase E. Annu Rev Microbiol 61: 71–87. 17447862

22. Bonnin R, Bouloc P (2015) RNA Degradation in Staphylococcus aureus: Diversity of Ribonucleases and Their Impact. International Journal of Genomics 2015: 12.

23. Chaudhuri RR, Allen AG, Owen PJ, Shalom G, Stone K, et al. (2009) Comprehensive identification of essential Staphylococcus aureus genes using Transposon-Mediated Differential Hybridisation (TMDH). BMC Genomics 10: 291. doi: 10.1186/1471-2164-10-291 19570206

24. Cheng ZF, Deutscher MP (2003) Quality control of ribosomal RNA mediated by polynucleotide phosphorylase and RNase R. Proc Natl Acad Sci U S A 100: 6388–6393. 12743360

25. Linder P, Lemeille S, Redder P (2014) Transcriptome-wide analyses of 5'-ends in RNase J mutants of a gram-positive pathogen reveal a role in RNA maturation, regulation and degradation. PLoS Genet 10: e1004207. doi: 10.1371/journal.pgen.1004207 24586213

26. Fechter P, Caldelari I, Lioliou E, Romby P (2014) Novel aspects of RNA regulation in Staphylococcus aureus. FEBS Lett 588: 2523–2529. doi: 10.1016/j.febslet.2014.05.037 24873876

27. Sassi M, Augagneur Y, Mauro T, Ivain L, Chabelskaya S, et al. (2015) SRD: a Staphylococcus regulatory RNA database. RNA 21: 1005–1017. doi: 10.1261/rna.049346.114 25805861

28. Huntzinger E, Boisset S, Saveanu C, Benito Y, Geissmann T, et al. (2005) Staphylococcus aureus RNAIII and the endoribonuclease III coordinately regulate spa gene expression. Embo J 24: 824–835. 15678100

29. Redder P (2015) Using EMOTE to map the exact 5'-ends of processed RNA on a transcriptome-wide scale. Methods Mol Biol 1259: 69–85. doi: 10.1007/978-1-4939-2214-7_5 25579580

30. Zuker M (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31: 3406–3415. 12824337

31. Gutierrez-Preciado A, Henkin TM, Grundy FJ, Yanofsky C, Merino E (2009) Biochemical features and functional implications of the RNA-based T-box regulatory mechanism. Microbiol Mol Biol Rev 73: 36–61. doi: 10.1128/MMBR.00026-08 19258532

32. Ruiz de los Mozos I, Vergara-Irigaray M, Segura V, Villanueva M, Bitarte N, et al. (2013) Base pairing interaction between 5'- and 3'-UTRs controls icaR mRNA translation in Staphylococcus aureus. PLoS Genet 9: e1004001. doi: 10.1371/journal.pgen.1004001 24367275

33. ten Broeke-Smits NJ, Pronk TE, Jongerius I, Bruning O, Wittink FR, et al. (2010) Operon structure of Staphylococcus aureus. Nucleic Acids Res 38: 3263–3274. doi: 10.1093/nar/gkq058 20150412

34. Khemici V, Poljak L, Luisi BF, Carpousis AJ (2008) The RNase E of Escherichia coli is a membrane-binding protein. Mol Microbiol 70: 799–813. doi: 10.1111/j.1365-2958.2008.06454.x 18976283

35. Clarke JE, Kime L, Romero AD, McDowall KJ (2014) Direct entry by RNase E is a major pathway for the degradation and processing of RNA in Escherichia coli. Nucleic Acids Res 42: 11733–11751. doi: 10.1093/nar/gku808 25237058

36. Lioliou E, Sharma CM, Caldelari I, Helfer AC, Fechter P, et al. (2012) Global regulatory functions of the Staphylococcus aureus endoribonuclease III in gene expression. PLoS Genet 8: e1002782. doi: 10.1371/journal.pgen.1002782 22761586

37. Redder P, Hausmann S, Khemici V, Yasrebi H, Linder P (2015) Bacterial versatility requires DEAD-box RNA helicases. FEMS Microbiol Rev.

38. Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25: 1754–1760. doi: 10.1093/bioinformatics/btp324 19451168

Štítky
Genetika Reprodukčná medicína

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PLOS Genetics


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