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When stable RNA becomes unstable: the degradation of ribosomes in bacteria and beyond

  • Ülo Maiväli

    Ülo Maiväli is a molecular biologist studying ribosomal metabolism in Escherichia coli. He obtained his PhD from the University of Tartu in 2004. Currently he is a researcher in the Institute of Technology, University of Tartu, Estonia.

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    , Anton Paier

    Anton Paier has a Master’s degree in Modern Literature from the University of Genua, Italy, a Bachelor’s in Military History from the University of Stockholm and a Master’s in Biomedical Laboratory Sciences from the Karolinska Institute (2008). Currently he is doing a PhD in Molecular Biology at the University of Tartu. His thesis is centered on the ribosomal degradation in E. coli.

    and Tanel Tenson

    Tanel Tenson is a biochemist and microbiologist studying the mechanisms of antibiotic action and antibiotic resistance. He obtained his PhD from the University of Tartu in 1997. Tanel Tenson is currently Professor of Technology of Antimicrobial Compounds at the Institute of Technology, University of Tartu.

Published/Copyright: March 24, 2013

Abstract

This review takes a comparative look at the various scenarios where ribosomes are degraded in bacteria and eukaryotes with emphasis on studies involving Escherichia coli and Saccharomyces cerevisiae. While the molecular mechanisms of degradation in bacteria and yeast appear somewhat different, we argue that the underlying causes of ribosome degradation are remarkably similar. In both model organisms during ribosomal assembly, partially formed pre-ribosomal particles can be degraded by at least two different sequentially-acting quality control pathways and fully assembled but functionally faulty ribosomes can be degraded in a separate quality control pathway. In addition, ribosomes that are both structurally- and functionally-sound can be degraded as an adaptive measure to stress.


Corresponding author: Ülo Maiväli, Institute of Technology, University of Tartu, Nooruse 1, Tartu 50411, Estonia

About the authors

Ülo Maiväli

Ülo Maiväli is a molecular biologist studying ribosomal metabolism in Escherichia coli. He obtained his PhD from the University of Tartu in 2004. Currently he is a researcher in the Institute of Technology, University of Tartu, Estonia.

Anton Paier

Anton Paier has a Master’s degree in Modern Literature from the University of Genua, Italy, a Bachelor’s in Military History from the University of Stockholm and a Master’s in Biomedical Laboratory Sciences from the Karolinska Institute (2008). Currently he is doing a PhD in Molecular Biology at the University of Tartu. His thesis is centered on the ribosomal degradation in E. coli.

Tanel Tenson

Tanel Tenson is a biochemist and microbiologist studying the mechanisms of antibiotic action and antibiotic resistance. He obtained his PhD from the University of Tartu in 1997. Tanel Tenson is currently Professor of Technology of Antimicrobial Compounds at the Institute of Technology, University of Tartu.

We thank Aivar Liiv and David Schryer for helpful comments on the manuscript and Sille Hausenberg for help with preparing the figures. This work was supported by the Estonian Science Agency grant no 9040 and by the European Regional Development Fund through the Center of Excellence in Chemical Biology.

References

Agafonov, D.E., Kolb, V.A., Nazimov, I.V., and Spirin, A.S. (1999). A protein residing at the subunit interface of the bacterial ribosome. Proc. Natl. Acad. Sci. USA 96, 12345–12349.10.1073/pnas.96.22.12345Search in Google Scholar

Allas, U., Liiv, A., and Remme, J. (2003). Functional interaction between RNase III and the Escherichia coli ribosome. BMC Mol. Biol. 4, 8.10.1186/1471-2199-4-8Search in Google Scholar

Allmang, C., Mitchell, P., Petfalski, E., and Tollervey, D. (2000). Degradation of ribosomal RNA precursors by the exosome. Nucleic Acids Res. 28, 1684–1691.10.1093/nar/28.8.1684Search in Google Scholar

Andersen, K.L., and Collins, K. (2011). Several RNase T2 enzymes function in induced tRNA and rRNA turnover in the ciliate Tetrahymena. Mol. Biol. Cell 23, 36–44.10.1091/mbc.e11-08-0689Search in Google Scholar

Aronson, A.I. and McCarthy, B.J. (1961). Studies of E. coli ribosomal RNA and its degradation products. Biophys. J. 1, 215–226.10.1016/S0006-3495(61)86885-9Search in Google Scholar

Ashford, A.J. and Pain, V.M. (1986). Effect of diabetes on the rates of synthesis and degradation of ribosomes in rat muscle and liver in vivo. J. Biol. Chem. 261, 4059–4065.10.1016/S0021-9258(17)35621-1Search in Google Scholar

Ault-Riché, D., Fraley, C.D., Tzeng, C.M., and Kornberg, A. (1998). Novel assay reveals multiple pathways regulating stress-induced accumulations of inorganic polyphosphate in Escherichia coli. J. Bacteriol. 180, 1841–1847.10.1128/JB.180.7.1841-1847.1998Search in Google Scholar PubMed PubMed Central

Basturea, G.N., Zundel, M.A., and Deutscher, M.P. (2011). Degradation of ribosomal RNA during starvation: comparison to quality control during steady-state growth and a role for RNase PH. RNA 17, 338–345.10.1261/rna.2448911Search in Google Scholar PubMed PubMed Central

Basturea, G.N., Harris, T.K., and Deutscher, M.P. (2012). Growth of a bacterium that apparently uses arsenic instead of phosphorus is a consequence of massive ribosome breakdown. J. Biol. Chem. 287, 28816–28819.10.1074/jbc.C112.394403Search in Google Scholar PubMed PubMed Central

Bessarab, D.A., Kaberdin, V.R., Wei, C.L., Liou, G.G., and Lin-Chao, S. (1998). RNA components of Escherichia coli degradosome: evidence for rRNA decay. Proc. Natl. Acad. Sci. USA 95, 3157–3161.10.1073/pnas.95.6.3157Search in Google Scholar PubMed PubMed Central

Bremer, H. and Dennis, P.P. (1987). Modulation of chemical composition and other parameters of the cell by growth rate. In: Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology. (American Society for Microbiology, Washington, DC), pp. 1527–1542.Search in Google Scholar

Cebollero, E., Reggiori, F., and Kraft, C. (2012). Reticulophagy and ribophagy: regulated degradation of protein production factories. Int. J. Cell Biol. 2012, 182834.10.1155/2012/182834Search in Google Scholar PubMed PubMed Central

Chen, C. and Deutscher, M.P. (2005). Elevation of RNase R in response to multiple stress conditions. J. Biol. Chem. 280, 34393–34396.10.1074/jbc.C500333200Search in Google Scholar PubMed

Chen, C. and Deutscher, M.P. (2010). RNase R is a highly unstable protein regulated by growth phase and stress. RNA 16, 667–672.10.1261/rna.1981010Search in Google Scholar PubMed PubMed Central

Cole, S.E., LaRiviere, F.J., Merrikh, C.N., and Moore, M.J. (2009). A convergence of rRNA and mRNA quality control pathways revealed by mechanistic analysis of nonfunctional rRNA decay. Mol. Cell 34, 440–450.10.1016/j.molcel.2009.04.017Search in Google Scholar PubMed PubMed Central

Dalebroux, Z.D. and Swanson, M.S. (2012). ppGpp: magic beyond RNA polymerase. Nat. Rev. Microbiol. 10, 203–212.10.1038/nrmicro2720Search in Google Scholar PubMed

Davey, H.M., Cross, E.J.M., Davey, C.L., Gkargkas, K., Delneri, D., Hoyle, D.C., Oliver, S.G., Kell, D.B., and Griffith, G.W. (2012). Genome-wide analysis of longevity in nutrient-deprived Saccharomyces cerevisiae reveals importance of recycling in maintaining cell viability. Environ. Microbiol. 14, 1249–1260.10.1111/j.1462-2920.2012.02705.xSearch in Google Scholar PubMed

Davies, B.W., Köhrer, C., Jacob, A.I., Simmons, L.A., Zhu, J., Aleman, L.M., RajBhandary, U.L., and Walker, G.C. (2010). Role of Escherichia coli YbeY, a highly conserved protein, in rRNA processing. Mol. Microbiol. 78, 506–518.10.1111/j.1365-2958.2010.07351.xSearch in Google Scholar PubMed PubMed Central

Davis, B.D., Luger, S.M., and Tai, P.C. (1986). Role of ribosome degradation in the death of starved Escherichia coli cells. J. Bacteriol. 166, 439–445.10.1128/jb.166.2.439-445.1986Search in Google Scholar PubMed PubMed Central

Deutscher, M.P. (2003). Degradation of stable RNA in bacteria. J. Biol. Chem. 278, 45041–45044.10.1074/jbc.R300031200Search in Google Scholar PubMed

Deutscher, M.P. (2006). Degradation of RNA in bacteria: comparison of mRNA and stable RNA. Nucleic Acids Res. 34, 659–666.10.1093/nar/gkj472Search in Google Scholar PubMed PubMed Central

Deutscher, M.P. (2009). Maturation and degradation of ribosomal RNA in bacteria. Prog. Mol. Biol. Transl. Sci. 85, 369–391.10.1016/S0079-6603(08)00809-XSearch in Google Scholar

Dewe, J.M., Whipple, J.M., Chernyakov, I., Jaramillo, L.N., and Phizicky, E.M. (2012). The yeast rapid tRNA decay pathway competes with elongation factor 1A for substrate tRNAs and acts on tRNAs lacking one or more of several modifications. RNA 18, 1886–1896.10.1261/rna.033654.112Search in Google Scholar PubMed PubMed Central

Dez, C., Houseley, J., and Tollervey, D. (2006). Surveillance of nuclear-restricted pre-ribosomes within a subnucleolar region of Saccharomyces cerevisiae. EMBO J. 25, 1534–1546.10.1038/sj.emboj.7601035Search in Google Scholar PubMed PubMed Central

Ding, Q., Markesbery, W.R., Chen, Q., Li, F., and Keller, J.N. (2005). Ribosome dysfunction is an early event in Alzheimer’s disease. J. Neurosci. 25, 9171–9175.10.1523/JNEUROSCI.3040-05.2005Search in Google Scholar PubMed PubMed Central

Dong, H., Nilsson, L., and Kurland, C.G. (1995). Gratuitous overexpression of genes in Escherichia coli leads to growth inhibition and ribosome destruction. J. Bacteriol. 177, 1497–1504.10.1128/jb.177.6.1497-1504.1995Search in Google Scholar PubMed PubMed Central

Ehrenberg, M., Bremer, H., and Dennis, P.P. (2013). Medium-dependent control of the bacterial growth rate. Biochimie 95, 643–658.10.1016/j.biochi.2012.11.012Search in Google Scholar PubMed

El-Sharoud, W.M. (2004). Ribosome inactivation for preservation: concepts and reservations. Sci. Prog. 87, 137–152.10.3184/003685004783238517Search in Google Scholar PubMed

Frazier, A.D. and Champney, W.S. (2012). Impairment of ribosomal subunit synthesis in aminoglycoside-treated ribonuclease mutants of Escherichia coli. Arch. Microbiol. 194, 1033–1041.10.1007/s00203-012-0839-5Search in Google Scholar PubMed PubMed Central

Freed, E.F., Bleichert, F., Dutca, L.M., and Baserga, S.J. (2010). When ribosomes go bad: diseases of ribosome biogenesis. Mol. Biosyst. 6, 481–493.10.1039/b919670fSearch in Google Scholar PubMed PubMed Central

Fujii, K., Kitabatake, M., Sakata, T., Miyata, A., and Ohno, M. (2009). A role for ubiquitin in the clearance of nonfunctional rRNAs. Genes Dev. 23, 963–974.10.1101/gad.1775609Search in Google Scholar PubMed PubMed Central

Fujii, K., Sakata, T., Kitabatake, M., and Ohno, M. (2012). 40S subunit dissociation and proteasome-dependent RNA degradation in nonfunctional 25S rRNA decay. EMBO J. 31, 2579–2589.10.1038/emboj.2012.85Search in Google Scholar

Gausing, K. (1977). Regulation of ribosome production in Escherichia coli: synthesis and stability of ribosomal RNA and of ribosomal protein messenger RNA at different growth rates. J. Mol. Biol. 115, 335–354.10.1016/0022-2836(77)90158-9Search in Google Scholar

Gutgsell, N.S. and Jain, C. (2012). Role of precursor sequences in the ordered maturation of E. coli 23S ribosomal RNA. RNA 18, 345–353.Search in Google Scholar

Häuser, R., Pech, M., Kijek, J., Yamamoto, H., Titz, B., Naeve, F., Tovchigrechko, A., Yamamoto, K., Szaflarski, W., Takeuchi, N., et al. (2012). RsfA (YbeB) Proteins are conserved ribosomal silencing factors. PLOS Genet. 8, e1002815.10.1371/journal.pgen.1002815Search in Google Scholar PubMed PubMed Central

Henras, A.K., Soudet, J., Gérus, M., Lebaron, S., Caizergues-Ferrer, M., Mougin, A., and Henry, Y. (2008). The post-transcriptional steps of eukaryotic ribosome biogenesis. Cell. Mol. Life Sci. 65, 2334–2359.10.1007/s00018-008-8027-0Search in Google Scholar PubMed

Hillwig, M.S., Contento, A.L., Meyer, A., Ebany, D., Bassham, D.C., and Macintosh, G.C. (2011). RNS2, a conserved member of the RNase T2 family, is necessary for ribosomal RNA decay in plants. Proc. Natl. Acad. Sci. USA 108, 1093–1098.10.1073/pnas.1009809108Search in Google Scholar PubMed PubMed Central

Hoat, T.X., Nakayashiki, H., Tosa, Y., and Mayama, S. (2006). Specific cleavage of ribosomal RNA and mRNA during victorin-induced apoptotic cell death in oat. Plant J. 46, 922–933.10.1111/j.1365-313X.2006.02752.xSearch in Google Scholar PubMed

Hsu, D., Shih, L.M., and Zee, Y.C. (1994). Degradation of rRNA in Salmonella strains: a novel mechanism to regulate the concentrations of rRNA and ribosomes. J. Bacteriol. 176, 4761–4765.10.1128/jb.176.15.4761-4765.1994Search in Google Scholar PubMed PubMed Central

Jacob, A.I., Köhrer, C., Davies, B.W., RajBhandary, U.L., and Walker, G.C. (2013). Conserved bacterial RNase YbeY plays key roles in 70S ribosome quality control and 16S rRNA maturation. Mol. Cell 49, 427–438.10.1016/j.molcel.2012.11.025Search in Google Scholar PubMed PubMed Central

Jia, J., Arif, A., Willard, B., Smith, J.D., Stuehr, D.J., Hazen, S.L., and Fox, P.L. (2012). Protection of extraribosomal RPL13a by GAPDH and dysregulation by S-nitrosylation. Mol. Cell 47, 656–663.10.1016/j.molcel.2012.06.006Search in Google Scholar PubMed PubMed Central

Johnson, R.M., Evans, J.D., Robinson, G.E., and Berenbaum, M.R. (2009). Changes in transcript abundance relating to colony collapse disorder in honey bees (Apis mellifera). Proc. Natl. Acad. Sci. USA 106, 14790–14795.10.1073/pnas.0906970106Search in Google Scholar PubMed PubMed Central

Johnston, G.C., Singer, R.A., and McFarlane, S. (1977). Growth and cell division during nitrogen starvation of the yeast Saccharomyces cerevisiae. J. Bacteriol. 132, 723–730.10.1128/jb.132.2.723-730.1977Search in Google Scholar

Ju, Q. and Warner, J.R. (1994). Ribosome synthesis during the growth cycle of Saccharomyces cerevisiae. Yeast 10, 151–157.10.1002/yea.320100203Search in Google Scholar

Kaczanowska, M. and Ryden-Aulin, M. (2007). Ribosome biogenesis and the translation process in Escherichia coli. Microbiol. Mol. Biol. Rev. 71, 477–494.10.1128/MMBR.00013-07Search in Google Scholar

Kalpaxis, D.L., Karahalios, P., and Papapetropoulou, M. (1998). Changes in ribosomal activity of Escherichia coli cells during prolonged culture in sea salts medium. J. Bacteriol. 180, 3114–3119.10.1128/JB.180.12.3114-3119.1998Search in Google Scholar

Kaplan, R. and Apirion, D. (1975). The fate of ribosomes in Escherichia coli cells starved for a carbon source. J. Biol. Chem. 250, 1854–1863.10.1016/S0021-9258(19)41773-0Search in Google Scholar

Karbstein, K. (2013). Quality control mechanisms during ribosome maturation. Trends Cell Biol., in press. DOI 10.1016/j.tcb.2013.01.004.10.1016/j.tcb.2013.01.004Search in Google Scholar PubMed PubMed Central

King, K.L., Jewell, C.M., Bortner, C.D., and Cidlowski, J.A. (2000). 28S ribosome degradation in lymphoid cell apoptosis: evidence for caspase and Bcl-2-dependent and -independent pathways. Cell Death Differ. 7, 994–1001.10.1038/sj.cdd.4400731Search in Google Scholar PubMed

Kitahara, K. and Miyazaki, K. (2011). Specific inhibition of bacterial RNase T2 by helix 41 of 16S ribosomal RNA. Nat. Commun. 2, 549–547.10.1038/ncomms1553Search in Google Scholar PubMed

Kraft, C., Deplazes, A., Sohrmann, M., and Peter, M. (2008). Mature ribosomes are selectively degraded upon starvation by an autophagy pathway requiring the Ubp3p/Bre5p ubiquitin protease. Nat. Cell Biol. 10, 602–610.10.1038/ncb1723Search in Google Scholar PubMed

Krokowski, D., Gaccioli, F., Majumder, M., Mullins, M.R., Yuan, C.L., Papadopoulou, B., Merrick, W.C., Komar, A.A., Taylor, D.J., and Hatzoglou, M. (2011). Characterization of hibernating ribosomes in mammalian cells. Cell Cycle 10, 2691–2702.10.4161/cc.10.16.16844Search in Google Scholar PubMed PubMed Central

Kuroda, A., Murphy, H., Cashel, M., and Kornberg, A. (1997). Guanosine tetra- and pentaphosphate promote accumulation of inorganic polyphosphate in Escherichia coli. J. Biol. Chem. 272, 21240–21243.10.1074/jbc.272.34.21240Search in Google Scholar PubMed

Kuroda, A., Tanaka, S., Ikeda, T., Kato, J., Takiguchi, N., and Ohtake, H. (1999). Inorganic polyphosphate kinase is required to stimulate protein degradation and for adaptation to amino acid starvation in Escherichia coli. Proc. Natl. Acad. Sci. USA 96, 14264–14269.10.1073/pnas.96.25.14264Search in Google Scholar PubMed PubMed Central

Kuroda, A., Nomura, K., Ohtomo, R., Kato, J., Ikeda, T., Takiguchi, N., Ohtake, H., and Kornberg, A. (2001). Role of inorganic polyphosphate in promoting ribosomal protein degradation by the Lon protease in E. coli. Science 293, 705–708.10.1126/science.1061315Search in Google Scholar PubMed

Lafontaine, D.L.J. (2010). A ‘garbage can’ for ribosomes: how eukaryotes degrade their ribosomes. Trends Biochem. Sci. 35, 267–277.10.1016/j.tibs.2009.12.006Search in Google Scholar PubMed

LaRiviere, F.J., Cole, S.E., Ferullo, D.J., and Moore, M.J. (2006). A late-acting quality control process for mature eukaryotic rRNAs. Mol. Cell 24, 619–626.10.1016/j.molcel.2006.10.008Search in Google Scholar PubMed

Lebaron, S., Schneider, C., van Nues, R.W., Swiatkowska, A., Walsh, D., Böttcher, B., Granneman, S., Watkins, N.J., and Tollervey, D. (2012). Proofreading of pre-40S ribosome maturation by a translation initiation factor and 60S subunits. Nat. Struct. Mol. Biol. 19, 744–753.10.1038/nsmb.2308Search in Google Scholar PubMed PubMed Central

Li, Z., Reimers, S., Pandit, S., and Deutscher, M.P. (2002). RNA quality control: degradation of defective transfer RNA. EMBO J. 21, 1132–1138.10.1093/emboj/21.5.1132Search in Google Scholar PubMed PubMed Central

Liang, W. and Deutscher, M.P. (2011). Post-translational modification of RNase R is regulated by stress-dependent reduction in the acetylating enzyme Pka (YfiQ). RNA 18, 37–41.10.1261/rna.030213.111Search in Google Scholar PubMed PubMed Central

Liang, W. and Deutscher, M.P. (2012a). Post-translational modification of RNase R is regulated by stress-dependent reduction in the acetylating enzyme Pka (YfiQ). RNA 18, 37–41.10.1261/rna.030213.111Search in Google Scholar

Liang, W. and Deutscher, M.P. (2012b). Transfer-messenger RNA-SmpB protein regulates ribonuclease R turnover by promoting binding of HslUV and lon proteases. J. Biol. Chem. 287, 33472–33479.10.1074/jbc.M112.375287Search in Google Scholar PubMed PubMed Central

Liu, M., Gong, X., Alluri, R.K., Wu, J., Sablo, T., and Li, Z. (2012). Characterization of RNA damage under oxidative stress in Escherichia coli. Biol. Chem. 393, 123–132.10.1515/hsz-2011-0247Search in Google Scholar PubMed PubMed Central

MacIntosh, G.C. (2011). RNase T2 family: enzymatic properties, functional diversity, and evolution of ancient ribonucleases. In: Ribonucleases, Nucleic Acids and Molecular Biology 26, A.W. Nicholson, ed. (Springer-Verlag), pp. 89–114.10.1007/978-3-642-21078-5_4Search in Google Scholar

Maes, A., Gracia, C., Hajnsdorf, E., and Régnier, P. (2011). Search for poly(A) polymerase targets in E. coli reveals its implication in surveillance of Glu tRNA processing and degradation of stable RNAs. Mol. Microbiol. 83, 436–451.10.1111/j.1365-2958.2011.07943.xSearch in Google Scholar PubMed

Metodiev, M.D., Lesko, N., Park, C.B., Amara, Y., Shi, Y., Wibom, R., Hultenby, K., Gustafsson, C.M., and Larsson, N.-G. (2009). Methylation of 12S rRNA is necessary for in vivo stability of the small subunit of the mammalian mitochondrial ribosome. Cell Metab. 9, 386–397.10.1016/j.cmet.2009.03.001Search in Google Scholar PubMed

Molin, S., Von Meyenburg, K., Maaloe, O., Hansen, M.T., and Pato, M.L. (1977). Control of ribosome synthesis in Escherichia coli: analysis of an energy source shift-down. J. Bacteriol. 131, 7–17.10.1128/jb.131.1.7-17.1977Search in Google Scholar PubMed PubMed Central

Moll, I. and Engelberg-Kulka, H. (2012). Selective translation during stress in Escherichia coli. Trends Biochem. Sci. 37, 493–498.10.1016/j.tibs.2012.07.007Search in Google Scholar PubMed PubMed Central

Mroczek, S. and Kufel, J. (2008). Apoptotic signals induce specific degradation of ribosomal RNA in yeast. Nucleic Acids Res. 36, 2874–2888.10.1093/nar/gkm1100Search in Google Scholar PubMed PubMed Central

Nanamiya, H., Akanuma, G., Natori, Y., Murayama, R., Kosono, S., Kudo, T., Kobayashi, K., Ogasawara, N., Park, S.-M., Ochi, K., et al. (2004). Zinc is a key factor in controlling alternation of two types of L31 protein in the Bacillus subtilis ribosome. Mol. Microbiol. 52, 273–283.10.1111/j.1365-2958.2003.03972.xSearch in Google Scholar PubMed

Narla, A. and Ebert, B.L. (2010). Ribosomopathies: human disorders of ribosome dysfunction. Blood 115, 3196–3205.10.1182/blood-2009-10-178129Search in Google Scholar PubMed PubMed Central

Nierhaus, K.H. and Dohme, F. (1974). Total reconstitution of functionally active 50S ribosomal subunits from Escherichia coli. Proc. Natl. Acad. Sci. USA 71, 4713–4717.10.1073/pnas.71.12.4713Search in Google Scholar PubMed PubMed Central

Nunomura, A., Moreira, P.I., Castellani, R.J., Lee, H.-G., Zhu, X., Smith, M.A., and Perry, G. (2012). Oxidative damage to RNA in aging and neurodegenerative disorders. Neurotox. Res. 22, 231–248.10.1007/s12640-012-9331-xSearch in Google Scholar PubMed

Nusspaumer, G., Remacha, M., and Ballesta, J.P. (2000). Phosphorylation and N-terminal region of yeast ribosomal protein P1 mediate its degradation, which is prevented by protein P2. EMBO J. 19, 6075–6084.10.1093/emboj/19.22.6075Search in Google Scholar PubMed PubMed Central

Ougland, R., Zhang, C.-M., Liiv, A., Johansen, R.F., Seeberg, E., Hou, Y.-M., Remme, J., and Falnes, P.Ø. (2004). AlkB restores the biological function of mRNA and tRNA inactivated by chemical methylation. Mol. Cell 16, 107–116.10.1016/j.molcel.2004.09.002Search in Google Scholar PubMed

Panse, V.G. and Johnson, A.W. (2010). Maturation of eukaryotic ribosomes: acquisition of functionality. Trends Biochem. Sci. 35, 260–266.10.1016/j.tibs.2010.01.001Search in Google Scholar PubMed PubMed Central

Pestov, D.G. and Shcherbik, N. (2012). Rapid cytoplasmic turnover of yeast ribosomes in response to rapamycin inhibition of TOR. Mol. Cell. Biol. 32, 2135–2144.10.1128/MCB.06763-11Search in Google Scholar PubMed PubMed Central

Piir, K., Paier, A., Liiv, A., Tenson, T., and Maivali, U. (2011). Ribosome degradation in growing bacteria. EMBO Rep. 12, 458–462.10.1038/embor.2011.47Search in Google Scholar PubMed PubMed Central

Polikanov, Y.S., Blaha, G.M., and Steitz, T.A. (2012). How hibernation factors RMF, HPF, and YfiA turn off protein synthesis. Science 336, 915–918.10.1126/science.1218538Search in Google Scholar PubMed PubMed Central

Pulk, A., Liiv, A., Peil, L., Maivali, U., Nierhaus, K., and Remme, J. (2010). Ribosome reactivation by replacement of damaged proteins. Mol. Microbiol. 75, 801–814.10.1111/j.1365-2958.2009.07002.xSearch in Google Scholar PubMed

Ramagopal, S. and Subramanian, A.R. (1974). Alteration in the acetylation level of ribosomal protein L12 during growth cycle of Escherichia coli. Proc. Natl. Acad. Sci. USA 71, 2136–2140.10.1073/pnas.71.5.2136Search in Google Scholar PubMed PubMed Central

Scott, M., Gunderson, C.W., Mateescu, E.M., Zhang, Z., and Hwa, T. (2010). Interdependence of cell growth and gene expression: origins and consequences. Science 330, 1099–1102.10.1126/science.1192588Search in Google Scholar PubMed

Shajani, Z., Sykes, M.T., and Williamson, J.R. (2011). Assembly of bacterial ribosomes. Annu. Rev. Biochem. 80, 501–526.10.1146/annurev-biochem-062608-160432Search in Google Scholar PubMed

Shcherbik, N. and Pestov, D.G. (2011). The ubiquitin ligase Rsp5 is required for ribosome stability in Saccharomyces cerevisiae. RNA 17, 1422–1428.10.1261/rna.2615311Search in Google Scholar PubMed PubMed Central

Silvers, J.A. and Champney, W.S. (2005). Accumulation and turnover of 23S ribosomal RNA in azithromycin-inhibited ribonuclease mutant strains of Escherichia coli. Arch. Microbiol. 184, 66–77.10.1007/s00203-005-0017-0Search in Google Scholar PubMed

Slomovic, S., Fremder, E., Staals, R.H.G., Pruijn, G.J.M., and Schuster, G. (2010). Addition of poly(A) and poly(A)-rich tails during RNA degradation in the cytoplasm of human cells. Proc. Natl. Acad. Sci. USA 107, 7407–7412.10.1073/pnas.0910621107Search in Google Scholar PubMed PubMed Central

Strunk, B.S., Novak, M.N., Young, C.L., and Karbstein, K. (2012). A translation-like cycle is a quality control checkpoint for maturing 40S ribosome subunits. Cell 150, 111–121.10.1016/j.cell.2012.04.044Search in Google Scholar PubMed PubMed Central

Thompson, D.M. and Parker, R. (2009). Stressing out over tRNA cleavage. Cell 138, 215–219.10.1016/j.cell.2009.07.001Search in Google Scholar PubMed

Tsai, Y.C., Du, D., Dominguez-Malfavon, L., Dimastrogiovanni, D., Cross, J., Callaghan, A.J., Garcia-Mena, J., and Luisi, B.F. (2012). Recognition of the 70S ribosome and polysome by the RNA degradosome in Escherichia coli. Nucleic Acids Res. 40, 10417–10431.10.1093/nar/gks739Search in Google Scholar PubMed PubMed Central

Tsuboi, T., Kuroha, K., Kudo, K., Makino, S., Inoue, E., Kashima, I., and Inada, T. (2012). Dom34:hbs1 plays a general role in quality-control systems by dissociation of a stalled ribosome at the 3′ end of aberrant mRNA. Mol. Cell 46, 518–529.10.1016/j.molcel.2012.03.013Search in Google Scholar PubMed

Van Dyke, N., Chanchorn, E., and Van Dyke, M.W. (2013). The Saccharomyces cerevisiae protein Stm1p facilitates ribosome preservation during quiescence. Biochem. Biophys. Res. Com. 430, 745–750.10.1016/j.bbrc.2012.11.078Search in Google Scholar PubMed

Vesper, O., Amitai, S., Belitsky, M., Byrgazov, K., Kaberdina, A.C., Engelberg-Kulka, H., and Moll, I. (2011). Selective translation of leaderless mRNAs by specialized ribosomes generated by MazF in Escherichia coli. Cell 147, 147–157.10.1016/j.cell.2011.07.047Search in Google Scholar PubMed PubMed Central

Wada, A. (1998). Growth phase coupled modulation of Escherichia coli ribosomes. Genes Cells 3, 203–208.10.1046/j.1365-2443.1998.00187.xSearch in Google Scholar

Wada, A., Mikkola, R., Kurland, C.G., and Ishihama, A. (2000). Growth phase-coupled changes of the ribosome profile in natural isolates and laboratory strains of Escherichia coli. J. Bacteriol. 182, 2893–2899.10.1128/JB.182.10.2893-2899.2000Search in Google Scholar

Warner, J.R. (1999). The economics of ribosome biosynthesis in yeast. Trends Biochem. Sci. 24, 437–440.10.1016/S0968-0004(99)01460-7Search in Google Scholar

Wilusz, J.E., Whipple, J.M., Phizicky, E.M., and Sharp, P.A. (2011). tRNAs marked with CCACCA are targeted for degradation. Science 334, 817–821.10.1126/science.1213671Search in Google Scholar PubMed PubMed Central

Wu, J. and Li, Z. (2008). Human polynucleotide phosphorylase reduces oxidative RNA damage and protects HeLa cell against oxidative stress. Biochem. Biophys. Res. Commun. 372, 288–292.10.1016/j.bbrc.2008.05.058Search in Google Scholar PubMed PubMed Central

Wu, J., Jiang, Z., Liu, M., Gong, X., Wu, S., Burns, C.M., and Li, Z. (2009). Polynucleotide phosphorylase protects Escherichia coli against oxidative stress. Biochemistry 48, 2012–2020.10.1021/bi801752pSearch in Google Scholar PubMed PubMed Central

Yoshida, H., Maki, Y., Furuike, S., Sakai, A., Ueta, M., and Wada, A. (2012). YqjD is an inner membrane protein associated with stationary-phase ribosomes in Escherichia coli. J. Bacteriol. 194, 4178–4183.10.1128/JB.00396-12Search in Google Scholar PubMed PubMed Central

Zhou, Z. and Deutscher, M.P. (1997). An essential function for the phosphate-dependent exoribonucleases RNase PH and polynucleotide phosphorylase. J. Bacteriol. 179, 4391–4395.10.1128/jb.179.13.4391-4395.1997Search in Google Scholar PubMed PubMed Central

Zundel, M.A., Basturea, G.N., and Deutscher, M.P. (2009). Initiation of ribosome degradation during starvation in Escherichia coli. RNA 15, 977–983.10.1261/rna.1381309Search in Google Scholar PubMed PubMed Central

Received: 2013-2-7
Accepted: 2013-3-20
Published Online: 2013-3-24
Published in Print: 2013-7-1

©2013 by Walter de Gruyter Berlin Boston

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