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Trans-acting regulators of ribonuclease activity

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Abstract

RNA metabolism needs to be tightly regulated in response to changes in cellular physiology. Ribonucleases (RNases) play an essential role in almost all aspects of RNA metabolism, including processing, degradation, and recycling of RNA molecules. Thus, living systems have evolved to regulate RNase activity at multiple levels, including transcription, post-transcription, post-translation, and cellular localization. In addition, various trans-acting regulators of RNase activity have been discovered in recent years. This review focuses on the physiological roles and underlying mechanisms of trans-acting regulators of RNase activity.

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References

  • Abrell, J.W. 1971. Ribonuclease I released from Escherichia coli by osmotic shock. Arch. Biochem. Biophys. 142, 693–700.

    Article  CAS  PubMed  Google Scholar 

  • Aiba, H. 2007. Mechanism of RNA silencing by Hfq-binding small RNAs. Curr. Opin. Microbiol. 10, 134–139.

    Article  CAS  PubMed  Google Scholar 

  • Andrade, J.M., Cairrão, F., and Arraiano, C.M. 2006. RNase R affects gene expression in stationary phase: regulation of ompA. Mol. Microbiol. 60, 219–228.

    Article  CAS  PubMed  Google Scholar 

  • Arraiano, C.M., Mauxion, F., Viegas, S.C., Matos, R.G., and Séraphin, B. 2013. Intracellular ribonucleases involved in transcript processing and decay: precision tools for RNA. Biochim. Biophys. Acta Gene Regul. Mech. 1829, 491–513.

    Article  CAS  Google Scholar 

  • Aseev, L.V. and Boni, I.V. 2011. Extraribosomal functions of bacterial ribosomal proteins. Mol. Biol. 45, 739–750.

    Article  CAS  Google Scholar 

  • Baek, Y.M., Jang, K.J., Lee, H., Yoon, S., Baek, A., Lee, K., and Kim, D.E. 2019. The bacterial endoribonuclease RNase E can cleave RNA in the absence of the RNA chaperone Hfq. J. Biol. Chem. 294, 16465–16478.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bandyra, K.J. and Luisi, B.F. 2018. RNase E and the high-fidelity orchestration of RNA metabolism. Microbiol. Spectr. 6, RWR–0008–2017.

    Article  Google Scholar 

  • Bartel, D.P. 2009. MicroRNAs: target recognition and regulatory functions. Cell 136, 215–233.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bechhofer, D.H. and Deutscher, M.P. 2019. Bacterial ribonucleases and their roles in RNA metabolism. Crit. Rev. Biochem. Mol. 54, 242–300.

    Article  CAS  Google Scholar 

  • Beintema, J.J. and van der Laan, J.M. 1986. Comparison of the structure of turtle pancreatic ribonuclease with those of mammalian ribonucleases. FEBS Lett. 194, 338–342.

    Article  CAS  PubMed  Google Scholar 

  • Bernstein, E., Caudy, A.A., Hammond, S.M., and Hannon, G.J. 2001. Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 409, 363–366.

    Article  CAS  PubMed  Google Scholar 

  • Blaszczyk, J., Gan, J., Tropea, J.E., Court, D.L., Waugh, D.S., and Ji, X. 2004. Noncatalytic assembly of ribonuclease III with double-stranded RNA. Structure 12, 457–466.

    Article  CAS  PubMed  Google Scholar 

  • Blázquez, M., Fominaya, J.M., and Hofsteenge, J. 1996. Oxidation of sulfhydryl groups of ribonuclease inhibitor in epithelial cells is sufficient for its intracellular degradation. J. Biol. Chem. 271, 18638–18642.

    Article  PubMed  Google Scholar 

  • Bruce, H.A., Du, D., Matak-Vinkovic, D., Bandyra, K.J., Broadhurst, R.W., Martin, E., Sobott, F., Shkumatov, A.V., and Luisi, B.F. 2018. Analysis of the natively unstructured RNA/protein-recognition core in the Escherichia coli RNA degradosome and its interactions with regulatory RNA/Hfq complexes. Nucleic Acids Res. 46, 387–402.

    Article  CAS  PubMed  Google Scholar 

  • Buckle, A.M., Schreiber, G., and Fersht, A.R. 1994. Protein-Protein recognition-crystal structural-analysis of a barnase barstar complex at 2.0-Å resolution. Biochemistry 33, 8878–8889.

    Article  CAS  PubMed  Google Scholar 

  • Bycroft, M., Hubbard, T.J., Proctor, M., Freund, S.M., and Murzin, A.G. 1997. The solution structure of the S1 RNA binding domain: a member of an ancient nucleic acid-binding fold. Cell 88, 235–242.

    Article  CAS  PubMed  Google Scholar 

  • Cahová, H., Winz, M.L., Höfer, K., Nübel, G., and Jäschke, A. 2015. NAD captureSeq indicates NAD as a bacterial cap for a subset of regulatory RNAs. Nature 519, 374–377.

    Article  PubMed  CAS  Google Scholar 

  • Cairrão, F., Chora, A., Zilhão, R., Carpousis, A.J., and Arraiano, C.M. 2001. RNase II levels change according to the growth conditions: characterization of gmr, a new Escherichia coli gene involved in the modulation of RNase II. Mol. Microbiol. 39, 1550–1561.

    Article  PubMed  Google Scholar 

  • Cairrão, F., Cruz, A., Mori, H., and Arraiano, C.M. 2003. Cold shock induction of RNase R and its role in the maturation of the quality control mediator SsrA/tmRNA. Mol. Microbiol. 50, 1349–1360.

    Article  PubMed  CAS  Google Scholar 

  • Callaghan, A.J., Marcaida, M.J., Stead, J.A., McDowall, K.J., Scott, W.G., and Luisi, B.F. 2005a. Structure of Escherichia coli RNase E catalytic domain and implications for RNA turnover. Nature 437, 1187–1191.

    Article  CAS  PubMed  Google Scholar 

  • Callaghan, A.J., Redko, Y., Murphy, L.M., Grossmann, J.G., Yates, D., Garman, E., Ilag, L.L., Robinson, C.V., Symmons, M.F., McDowall, K.J., et al. 2005b. “Zn-link”: a metal-sharing interface that organizes the quaternary structure and catalytic site of the endoribonuclease, RNase E. Biochemistry 44, 4667–4675.

    Article  CAS  PubMed  Google Scholar 

  • Cannistraro, V.J. and Kennell, D. 1989. Purification and characterization of ribonuclease M and mRNA degradation in Escherichia coli. Eur. J. Biochem. 181, 363–370.

    Article  CAS  PubMed  Google Scholar 

  • Cannistraro, V.J. and Kennell, D. 1991. RNase I*, a form of RNase I, and mRNA degradation in Escherichia coli. J. Bacteriol. 173, 4653–4659.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Caruthers, J.M., Feng, Y., McKay, D.B., and Cohen, S.N. 2006. Retention of core catalytic functions by a conserved minimal ribonuclease E peptide that lacks the domain required for tetramer formation. J. Biol. Chem. 281, 27046–27051.

    Article  CAS  PubMed  Google Scholar 

  • Carzaniga, T., Briani, F., Zangrossi, S., Merlino, G., Marchi, P., and Dehò, G. 2009. Autogenous regulation of Escherichia coli polynucleotide phosphorylase expression revisited. J. Bacteriol. 191, 1738–1748.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Celesnik, H., Deana, A., and Belasco, J.G. 2007. Initiation of RNA decay in Escherichia coli by 5′ pyrophosphate removal. Mol. Cell 27, 79–90.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ceyssens, P.J., Minakhin, L., Van den Bossche, A., Yakunina, M., Klimuk, E., Blasdel, B., De Smet, J., Noben, J.P., Bläsi, U., Severinov, K., et al. 2014. Development of giant bacteriophage ΦKZ is independent of the host transcription apparatus. J. Virol. 88, 10501–10510.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chen, C. and Deutscher, M.P. 2005. Elevation of RNase R in response to multiple stress conditions. J. Biol. Chem. 280, 34393–34396.

    Article  CAS  PubMed  Google Scholar 

  • Chen, C. and Deutscher, M.P. 2010. RNase R is a highly unstable protein regulated by growth phase and stress. RNA 16, 667–672.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen, W.X., Zhang, Z.Z., Chen, J., Zhang, J., Zhang, J., Wu, Y., Huang, Y., Cai, X.F., and Huang, A.L. 2008. HCV core protein interacts with Dicer to antagonize RNA silencing. Virus Res. 133, 250–258.

    Article  CAS  PubMed  Google Scholar 

  • Chendrimada, T.P., Gregory, R.I., Kumaraswamy, E., Norman, J., Cooch, N., Nishikura, K., and Shiekhattar, R. 2005. TRBP recruits the Dicer complex to Ago2 for microRNA processing and gene silencing. Nature 436, 740–744.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng, Z.F. and Deutscher, M.P. 2005. An important role for RNase R in mRNA decay. Mol. Cell 17, 313–318.

    Article  CAS  PubMed  Google Scholar 

  • Cho, K.H. 2017. The structure and function of the Gram-positive bacterial RNA degradosome. Front. Microbiol. 8, 154.

    Article  PubMed  PubMed Central  Google Scholar 

  • Cho, S., Beintema, J.J., and Zhang, J. 2005. The ribonuclease A superfamily of mammals and birds: identifying new members and tracing evolutionary histories. Genomics 85, 208–220.

    Article  CAS  PubMed  Google Scholar 

  • Christensen, D.G., Meyer, J.G., Baumgartner, J.T., D’Souza, A.K., Nelson, W.C., Payne, S.H., Kuhn, M.L., Schilling, B., and Wolfe, A.J. 2018. Identification of novel protein lysine acetyltransferases in Escherichia coli. mBio 9, e01905–18.

    Article  PubMed  PubMed Central  Google Scholar 

  • Colak, G., Xie, Z., Zhu, A.Y., Dai, L., Lu, Z., Zhang, Y., Wan, X., Chen, Y., Cha, Y.H., Lin, H., et al. 2013. Identification of lysine succinylation substrates and the succinylation regulatory enzyme CobB in Escherichia coli. Mol. Cell. Proteomics 12, 3509–3520.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Condon, C. and Putzer, H. 2002. The phylogenetic distribution of bacterial ribonucleases. Nucleic Acids Res. 30, 5339–5346.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Court, D.L., Gan, J., Liang, Y.H., Shaw, G.X., Tropea, J.E., Costantino, N., Waugh, D.S., and Ji, X. 2013. RNase III: Genetics and function; structure and mechanism. Annu. Rev. Genet. 47, 405–431.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Crouch, R.J. 1974. Ribonuclease 3 does not degrade deoxyribonucleic acid-ribonucleic acid hybrids. J. Biol. Chem. 249, 1314–1316.

    Article  CAS  PubMed  Google Scholar 

  • Daniels, S.M., Melendez-Peña, C.E., Scarborough, R.J., Daher, A., Christensen, H.S., El Far, M., Purcell, D.F.J., Lainé, S., and Gatignol, A. 2009. Characterization of the TRBP domain required for Dicer interaction and function in RNA interference. BMC Mol. Biol. 10, 38.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Datta, A.K. and Burma, D.P. 1972. Association of ribonuclease I with ribosomes and their subunits. J. Biol. Chem. 247, 6795–6801.

    Article  CAS  PubMed  Google Scholar 

  • Denli, A.M., Tops, B.B.J., Plasterk, R.H.A., Ketting, R.F., and Hannon, G.J. 2004. Processing of primary microRNAs by the Microprocessor complex. Nature 432, 231–235.

    Article  CAS  PubMed  Google Scholar 

  • Deutscher, M.P. 2015. How bacterial cells keep ribonucleases under control. FEMS Microbiol. Rev. 39, 350–361.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dickson, K.A., Haigis, M.C., and Raines, R.T. 2005. Ribonuclease inhibitor: structure and function. Prog. Nucleic Acid Res. Mol. Biol. 80, 349–374.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dincbas-Renqvist, V., Pépin, G., Rakonjac, M., Plante, I., Ouellet, D.L., Hermansson, A., Goulet, I., Doucet, J., Samuelsson, B., Rådmark, O., et al. 2009. Human Dicer C-terminus functions as a 5-lipoxygenase binding domain. Biochim. Biophys. Acta 1789, 99–108.

    Article  CAS  PubMed  Google Scholar 

  • Domingues, S., Moreira, R.N., Andrade, J.M., dos Santos, R.F., Bárria, C., Viegas, S.C., and Arraiano, C.M. 2015. The role of RNase R in trans-translation and ribosomal quality control. Biochimie 114, 113–118.

    Article  CAS  PubMed  Google Scholar 

  • Donovan, W.P. and Kushner, S.R. 1986. Polynucleotide phosphorylase and ribonuclease II are required for cell viability and mRNA turnover in Escherichia coli K-12. Proc. Natl. Acad. Sci. USA 83, 120–124.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Drake, M., Furuta, T., Suen, K.M., Gonzalez, G., Liu, B., Kalia, A., Ladbury, J.E., Fire, A.Z., Skeath, J.B., and Arur, S. 2014. A Requirement for ERK-dependent Dicer phosphorylation in coordinating oocyte-to-embryo transition in Caenorhabditis elegans. Dev. Cell 31, 614–628.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dürwald, H. and Hoffmann-Berling, H. 1968. Endonuclease-I-deficient and ribonuclease I-deficient Escherichia coli mutants. J. Mol. Biol. 34, 331–346.

    Article  PubMed  Google Scholar 

  • Dyer, K.D. and Rosenberg, H.F. 2006. The RNase a superfamily: generation of diversity and innate host defense. Mol. Divers. 10, 585–597.

    Article  CAS  PubMed  Google Scholar 

  • Elson, D. 1958. Latent ribonuclease activity in a ribonucleoprotein. Biochim. Biophys. Acta 27, 216–217.

    Article  CAS  PubMed  Google Scholar 

  • Filippov, V., Solovyev, V., Filippova, M., and Gill, S.S. 2000. A novel type of RNase III family proteins in eukaryotes. Gene 245, 213–221.

    Article  CAS  PubMed  Google Scholar 

  • Fominaya, J.M. and Hofsteenge, J. 1992. Inactivation of ribonuclease inhibitor by thiol-disulfide exchange. J. Biol. Chem. 267, 24655–24660.

    Article  CAS  PubMed  Google Scholar 

  • Fontaine, B.M., Martin, K.S., Garcia-Rodriguez, J.M., Jung, C., Briggs, L., Southwell, J.E., Jia, X., and Weinert, E.E. 2018. RNase I regulates Escherichia coli 2′,3′-cyclic nucleotide monophosphate levels and biofilm formation. Biochem. J. 475, 1491–1506.

    Article  CAS  PubMed  Google Scholar 

  • Fukunaga, R., Han, B.W., Hung, J.H., Xu, J., Weng, Z.P., and Zamore, P.D. 2012. Dicer partner proteins tune the length of mature miRNAs in flies and mammals. Cell 151, 533–546.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gao, J., Lee, K., Zhao, M., Qiu, J., Zhan, X., Saxena, A., Moore, C.J., Cohen, S.N., and Georgiou, G. 2006. Differential modulation of E. coli mRNA abundance by inhibitory proteins that alter the composition of the degradosome. Mol. Microbiol. 61, 394–406.

    Article  CAS  PubMed  Google Scholar 

  • Gbenle, G.O. 1990. Trypanosoma brucei: calcium-dependent endoribonuclease is associated with inhibitor protein. Exp. Parasitol. 71, 432–438.

    Article  CAS  PubMed  Google Scholar 

  • Gegenheimer, P., Watson, N., and Apirion, D. 1977. Multiple pathways for primary processing of ribosomal RNA in Escherichia coli. J. Biol. Chem. 252, 3064–3073.

    Article  CAS  PubMed  Google Scholar 

  • Gone, S., Alfonso-Prieto, M., Paudyal, S., and Nicholson, A.W. 2016. Mechanism of ribonuclease III catalytic regulation by serine phosphorylation. Sci. Rep. 6, 25448.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Górna, M.W., Carpousis, A.J., and Luisi, B.F. 2012. From conformational chaos to robust regulation: the structure and function of the multi-enzyme RNA degradosome. Q. Rev. Biophys. 45, 105–145.

    Article  PubMed  CAS  Google Scholar 

  • Górna, M.W., Pietras, Z., Tsai, Y.C., Callaghan, A.J., Hernández, H., Robinson, C.V., and Luisi, B.F. 2010. The regulatory protein RraA modulates RNA-binding and helicase activities of the E. coli RNA degradosome. RNA 16, 553–562.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Green, P.J. 1994. The Ribonucleases of higher-plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 45, 421–445.

    Article  CAS  Google Scholar 

  • Gregory, R.I., Yan, K.P., Amuthan, G., Chendrimada, T., Doratotaj, B., Cooch, N., and Shiekhattar, R. 2004. The microprocessor complex mediates the genesis of microRNAs. Nature 432, 235–240.

    Article  CAS  PubMed  Google Scholar 

  • Gross, T.J., Powers, L.S., Boudreau, R.L., Brink, B., Reisetter, A., Goel, K., Gerke, A.K., Hassan, I.H., and Monick, M.M. 2014. A microRNA processing defect in smokers’ macrophages is linked to SUMOylation of the endonuclease DICER. J. Biol. Chem. 289, 12823–12834.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guillet, V., Lapthorn, A., Hartley, R.W., and Mauguen, Y. 1993. Recognition between a bacterial ribonuclease, barnase, and its natural inhibitor, barstar. Structure 1, 165–176.

    Article  CAS  PubMed  Google Scholar 

  • Gurevitz, M. and Apirion, D. 1983. Interplay among processing and degradative enzymes and a precursor ribonucleic acid in the selective maturation and maintenance of ribonucleic acid molecules. Biochemistry 22, 4000–4005.

    Article  CAS  PubMed  Google Scholar 

  • Gurevitz, M., Watson, N., and Apirion, D. 1982. A cleavage site of ribonuclease F. A putative processing endoribonuclease from Escherichia coli. Eur. J. Biochem. 124, 553–559.

    Article  CAS  PubMed  Google Scholar 

  • Haase, A.D., Jaskiewicz, L., Zhang, H.D., Lainé, S., Sack, R., Gatignol, A., and Filipowicz, W. 2005. TRBP, a regulator of cellular PKR and HIV-1 virus expression, interacts with Dicer and functions in RNA silencing. EMBO Rep. 6, 961–967.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Han, J., Lee, Y., Yeom, K.H., Kim, Y.K., Jin, H., and Kim, V.N. 2004. The Drosha-DGCR8 complex in primary microRNA processing. Genes Dev. 18, 3016–3027.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hardwick, S.W., Chan, V.S.Y., Broadhurst, R.W., and Luisi, B.F. 2011. An RNA degradosome assembly in Caulobacter crescentus. Nucleic Acids Res. 39, 1449–1459.

    Article  CAS  PubMed  Google Scholar 

  • Hartley, R.W. 1988. Barnase and barstar: expression of its cloned inhibitor permits expression of a cloned ribonuclease. J. Mol. Biol. 202, 913–915.

    Article  CAS  PubMed  Google Scholar 

  • Hartley, R.W. 1989. Barnase and barstar: two small proteins to fold and fit together. Trends Biochem. Sci. 14, 450–454.

    Article  CAS  PubMed  Google Scholar 

  • Hartley, R.W. 1993. Directed mutagenesis and barnase-barstar recognition. Biochemistry 32, 5978–5984.

    Article  CAS  PubMed  Google Scholar 

  • Hofsteenge, J., Kieffer, B., Matthies, R., Hemmings, B.A., and Stone, S.R. 1988. Amino acid sequence of the ribonuclease inhibitor from porcine liver reveals the presence of leucine-rich repeats. Biochemistry 27, 8537–8544.

    Article  CAS  PubMed  Google Scholar 

  • Hua, Z. and Kao, T.H. 2006. Identification and characterization of components of a putative Petunia S-locus F-box-containing E3 ligase complex involved in S-RNase-based self-incompatibility. Plant Cell 18, 2531–2553.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hua, Z. and Kao, T.H. 2008. Identification of major lysine residues of S3-RNase of Petunia inflata involved in ubiquitin-26S proteasome-mediated degradation in vitro. Plant J. 54, 1094–1104.

    Article  CAS  PubMed  Google Scholar 

  • Hunt, A., Rawlins, J.P., Thomaides, H.B., and Errington, J. 2006. Functional analysis of 11 putative essential genes in Bacillus subtilis. Microbiology 152, 2895–2907.

    Article  CAS  PubMed  Google Scholar 

  • Irie, M. 1997. Structures and functions of ribonucleases. Yakugaku Zasshi 117, 561–582.

    Article  CAS  PubMed  Google Scholar 

  • Jain, C. and Belasco, J.G. 1995. RNase E autoregulates its synthesis by controlling the degradation rate of its own mRNA in Escherichia coli: unusual sensitivity of the rne transcript to RNase E activity. Genes Dev. 9, 84–96.

    Article  CAS  PubMed  Google Scholar 

  • Jain, C., Deana, A., and Belasco, J.G. 2002. Consequences of RNase E scarcity in Escherichia coli. Mol. Microbiol. 43, 1053–1064.

    Article  CAS  PubMed  Google Scholar 

  • Jarrige, A.C., Mathy, N., and Portier, C. 2001. PNPase autocontrols its expression by degrading a double-stranded structure in the pnp mRNA leader. EMBO J. 20, 6845–6855.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jensen, P.E. and Leister, D. 2014. Chloroplast evolution, structure and functions. F1000Prime Rep. 6, 40.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ji, X. 2008. The mechanism of RNase III action: how dicer dices. Curr. Top. Microbiol. Immunol. 320, 99–116.

    CAS  PubMed  Google Scholar 

  • Johnson, R.J., McCoy, J.G., Bingman, C.A., Phillips, G.N.Jr., and Raines, R.T. 2007. Inhibition of human pancreatic ribonuclease by the human ribonuclease inhibitor protein. J. Mol. Biol. 368, 434–449.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaberdin, V.R., Miczak, A., Jakobsen, J.S., Lin-Chao, S., McDowall, K.J., and von Gabain, A. 1998. The endoribonucleolytic N-terminal half of Escherichia coli RNase E is evolutionarily conserved in Synechocystis sp. and other bacteria but not the C-terminal half, which is sufficient for degradosome assembly. Proc. Natl. Acad. Sci. USA 95, 11637–11642.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaberdin, V.R., Singh, D., and Lin-Chao, S. 2011. Composition and conservation of the mRNA-degrading machinery in bacteria. J. Biomed. Sci. 18, 23.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kajava, A.V. 1998. Structural diversity of leucine-rich repeat proteins. J. Mol. Biol. 277, 519–527.

    Article  CAS  PubMed  Google Scholar 

  • Kaplan, R. and Apirion, D. 1975. Decay of ribosomal ribonucleic acid in Escherichia coli cells starved for various nutrients. J. Biol. Chem. 250, 3174–3178.

    Article  CAS  PubMed  Google Scholar 

  • Kerscher, O., Felberbaum, R., and Hochstrasser, M. 2006. Modification of proteins by ubiquitin and ubiquitin-like proteins. Annu. Rev. Cell. Dev. Biol. 22, 159–180.

    Article  CAS  PubMed  Google Scholar 

  • Khemici, V., Poljak, L., Luisi, B.F., and Carpousis, A.J. 2008. The RNase E of Escherichia coli is a membrane-binding protein. Mol. Microbiol. 70, 799–813.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kim, M. and Kim, K. 2017. Stress-responsively modulated ymdAB-clsC operon plays a role in biofilm formation and apramycin susceptibility in Escherichia coli. FEMS Microbiol. Lett. 364, fnx114.

    Article  Google Scholar 

  • Kim, T., Lee, J., and Kim, K. 2013. Escherichia coli YmdB regulates biofilm formation independently of its role as an RNase III modulator. BMC Microbiol. 13, 266.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kim, K., Manasherob, R., and Cohen, S.N. 2008. YmdB: a stress-responsive ribonuclease-binding regulator of E. coli RNase III activity. Genes Dev. 22, 3497–3508.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim, B.M., Schultz, L.W., and Raines, R.T. 1999. Variants of ribonuclease inhibitor that resist oxidation. Protein Sci. 8, 430–434.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kitahara, K. and Miyazaki, K. 2011. Specific inhibition of bacterial RNase T2 by helix 41 of 16S ribosomal RNA. Nat. Commun. 2, 549.

    Article  PubMed  CAS  Google Scholar 

  • Klockow, L.C., Sharifi, H.J., Wen, X., Flagg, M., Furuya, A.K.M., Nekorchuk, M., and de Noronha, C.M.C. 2013. The HIV-1 protein Vpr targets the endoribonuclease Dicer for proteasomal degradation to boost macrophage infection. Virology 444, 191–202.

    Article  CAS  Google Scholar 

  • Kobe, B. and Deisenhofer, J. 1995. A structural basis of the interactions between leucine-rich repeats and protein ligands. Nature 374, 183–186.

    Article  CAS  PubMed  Google Scholar 

  • Koo, H., Park, S., Kwak, M.K., and Lee, J.S. 2020. Regulation of gene expression by protein lysine acetylation in Salmonella. J. Microbiol. 58, 979–987.

    Article  PubMed  CAS  Google Scholar 

  • Koslover, D.J., Callaghan, A.J., Marcaida, M.J., Garman, E.F., Martick, M., Scott, W.G., and Luisi, B.F. 2008. The crystal structure of the Escherichia coli RNase E apoprotein and a mechanism for RNA degradation. Structure 16, 1238–1244.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kosuge, T., Isemura, M., Takahashi, Y., Odani, S., and Odani, S. 2003. Ribonuclease inhibitors in Malus x domestica (common apple): isolation and partial characterization. Biosci. Biotechnol. Biochem. 67, 698–703.

    Article  CAS  PubMed  Google Scholar 

  • Krajcikova, D. and Hartley, R.W. 2004. A new member of the bacterial ribonuclease inhibitor family from Saccharopolyspora erythraea. FEBS Lett. 557, 164–168.

    Article  CAS  PubMed  Google Scholar 

  • Krajcikova, D., Hartley, R.W., and Sevcik, J. 1998. Isolation and purification of two novel streptomycete RNase inhibitors, SaI14 and SaI20, and cloning, sequencing, and expression in Escherichia coli of the gene coding for SaI14. J. Bacteriol. 180, 1582–1585.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lai, Z., Ma, W., Han, B., Liang, L., Zhang, Y., Hong, G., and Xue, Y. 2002. An F-box gene linked to the self-incompatibility (S) locus of Antirrhinum is expressed specifically in pollen and tapetum. Plant Mol. Biol. 50, 29–42.

    Article  CAS  PubMed  Google Scholar 

  • Lambert, P.A. and Smith, A.R. 1976. Antimicrobial action of dodecyldiethanolamine: activation of ribonuclease I in Escherichia coli. Microbios 17, 35–49.

    CAS  PubMed  Google Scholar 

  • Lee, Y., Ahn, C., Han, J., Choi, H., Kim, J., Yim, J., Lee, J., Provost, P., Rådmark, O., Kim, S., et al. 2003a. The nuclear RNase III Drosha initiates microRNA processing. Nature 425, 415–419.

    Article  CAS  PubMed  Google Scholar 

  • Lee, K., Bernstein, J.A., and Cohen, S.N. 2002. RNase G complementation of rne null mutation identifies functional interrelationships with RNase E in Escherichia coli. Mol. Microbiol. 43, 1445–1456.

    Article  CAS  PubMed  Google Scholar 

  • Lee, F.S., Fox, E.A., Zhou, H.M., Strydom, D.J., and Vallee, B.L. 1988. Primary structure of human placental ribonuclease inhibitor. Biochemistry 27, 8545–8553.

    Article  CAS  PubMed  Google Scholar 

  • Lee, Y., Hur, I., Park, S.Y., Kim, Y.K., Suh, M.R., and Kim, V.N. 2006. The role of PACT in the RNA silencing pathway. EMBO J. 25, 522–532.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee, M., Joo, M., Sim, M., Sim, S.H., Kim, H.L., Lee, J., Ryu, M., Yeom, J.H., Hahn, Y., Ha, N.C., et al. 2019a. The coordinated action of RNase III and RNase G controls enolase expression in response to oxygen availability in Escherichia coli. Sci. Rep. 9, 17257.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lee, J., Lee, D.H., Jeon, C.O., and Lee, K. 2019b. RNase G controls tpiA mRNA abundance in response to oxygen availability in Escherichia coli. J. Microbiol. 57, 910–917.

    Article  CAS  PubMed  Google Scholar 

  • Lee, M., Ryu, M., Joo, M., Seo, Y.J., Lee, J., Kim, H.M., Shin, E., Yeom, J.H., Kim, Y.H., Bae, J., et al. 2021. Endoribonuclease-mediated control of hns mRNA stability constitutes a key regulatory pathway for Salmonella Typhimurium pathogenicity island 1 expression. PLoS Pathog. 17, e1009263.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee, F.S., Shapiro, R., and Vallee, B.L. 1989. Tight-binding inhibition of angiogenin and ribonuclease A by placental ribonuclease inhibitor. Biochemistry 28, 225–230.

    Article  CAS  PubMed  Google Scholar 

  • Lee, F.S. and Vallee, B.L. 1993. Structure and action of mammalian ribonuclease (angiogenin) inhibitor. Prog. Nucleic Acid Res. Mol. Biol. 44, 1–30.

    Article  CAS  PubMed  Google Scholar 

  • Lee, M., Yeom, J.H., Sim, S.H., Ahn, S., and Lee, K. 2009. Effects of Escherichia coli RraA orthologs of Vibrio vulnificus on the ribonucleolytic activity of RNase E in vivo. Curr. Microbiol. 58, 349–353.

    Article  CAS  PubMed  Google Scholar 

  • Lee, K., Zhan, X., Gao, J., Qiu, J., Feng, Y., Meganathan, R., Cohen, S.N., and Georgiou, G. 2003b. RraA. a protein inhibitor of RNase E activity that globally modulates RNA abundance in E. coli. Cell 114, 623–634.

    CAS  PubMed  Google Scholar 

  • Lee, H.Y., Zhou, K.H., Smith, A.M., Noland, C.L., and Doudna, J.A. 2013. Differential roles of human Dicer-binding proteins TRBP and PACT in small RNA processing. Nucleic Acids Res. 41, 6568–6576.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lehnik-Habrink, M., Newman, J., Rothe, F.M., Solovyova, A.S., Rodrigues, C., Herzberg, C., Commichau, F.M., Lewis, R.J., and Stülke, J. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li, Z. and Deutscher, M.P. 1996. Maturation pathways for E. coli tRNA precursors: a random multienzyme process in vivo. Cell 86, 503–512.

    Article  CAS  PubMed  Google Scholar 

  • Li, Z. and Deutscher, M.P. 2002. RNase E plays an essential role in the maturation of Escherichia coli tRNA precursors. RNA 8, 97–109.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li, Z., Pandit, S., and Deutscher, M.P. 1999. RNase G (CafA protein) and RNase E are both required for the 5′-maturation of 16S ribosomal RNA. EMBO J. 18, 2878–2885.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li, S., Sun, P., Williams, J.S., and Kao, T.H. 2014. Identification of the self-incompatibility locus F-box protein-containing complex in Petunia inflata. Plant Reprod. 27, 31–45.

    Article  PubMed  CAS  Google Scholar 

  • Liang, W. and Deutscher, M.P. 2010. A novel mechanism for ribonuclease regulation: transfer-messenger RNA (tmRNA) and its associated protein SmpB regulate the stability of RNase R. J. Biol. Chem. 285, 29054–29058.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liang, W. and Deutscher, M.P. 2013. Ribosomes regulate the stability and action of the exoribonuclease RNase R. J. Biol. Chem. 288, 34791–34798.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liang, W., Malhotra, A., and Deutscher, M.P. 2011. Acetylation regulates the stability of a bacterial protein: growth stage-dependent modification of RNase R. Mol. Cell 44, 160–166.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lim, B. and Lee, K. 2015. Stability of the osmoregulated promoter-derived proP mRNA is posttranscriptionally regulated by RNase III in Escherichia coli. J. Bacteriol. 197, 1297–1305.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lim, B., Sim, M., Lee, H., Hyun, S., Lee, Y., Hahn, Y., Shin, E., and Lee, K. 2015. Regulation of Escherichia coli RNase III activity. J. Microbiol. 53, 487–494.

    Article  CAS  PubMed  Google Scholar 

  • Lin-Chao, S. and Cohen, S.N. 1991. The rate of processing and degradation of antisense RNAI regulates the replication of ColE1-type plasmids in vivo. Cell 65, 1233–1242.

    Article  CAS  PubMed  Google Scholar 

  • Lindahl, L. and Zengel, J.M. 1979. Operon-specific regulation of ribosomal protein synthesis in Escherichia coli. Proc. Natl. Acad. Sci. USA 76, 6542–6546.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liou, G.G., Jane, W.N., Cohen, S.N., Lin, N.S., and Lin-Chao, S. 2001. RNA degradosomes exist in vivo in Escherichia coli as multicomponent complexes associated with the cytoplasmic membrane via the N-terminal region of ribonuclease E. Proc. Natl. Acad. Sci. USA 98, 63–68.

    Article  CAS  PubMed  Google Scholar 

  • Lomax, J.E., Bianchetti, C.M., Chang, A., Phillips, G.N.Jr., Fox, B.G., and Raines, R.T. 2014. Functional evolution of ribonuclease inhibitor: insights from birds and reptiles. J. Mol. Biol. 426, 3041–3056.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lu, L., Li, J., Moussaoui, M., and Boix, E. 2018. Immune modulation by human secreted RNases at the extracellular space. Front. Immunol. 9, 1012.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lu, F. and Taghbalout, A. 2013. Membrane association via an aminoterminal amphipathic helix is required for the cellular organization and function of RNase II. J. Biol. Chem. 288, 7241–7251.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lu, F. and Taghbalout, A. 2014. The Escherichia coli major exoribonuclease RNase II is a component of the RNA degradosome. Biosci. Rep. 34, e00166.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Luciano, D.J., Levenson-Palmer, R., and Belasco, J.G. 2019. Stresses that raise Np4A levels induce protective nucleoside tetraphosphate capping of bacterial RNA. Mol. Cell 75, 957–966.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Luciano, D.J., Vasilyev, N., Richards, J., Serganov, A., and Belasco, J.G. 2017. A novel RNA phosphorylation state enables 5′ end-dependent degradation in Escherichia coli. Mol. Cell 67, 44–54.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Macrae, I.J., Li, F., Zhou, K., Cande, W.Z., and Doudna, J.A. 2006. Structure of Dicer and mechanistic implications for RNAi. Cold Spring Harb. Symp. Quant. Biol. 71, 73–80.

    Article  CAS  PubMed  Google Scholar 

  • Macrae, I.J., Ma, E., Zhou, M., Robinson, C.V., and Doudna, J.A. 2008. In vitro reconstitution of the human RISC-loading complex. Proc. Natl. Acad. Sci. USA 105, 512–517.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Makarov, E.M. and Apirion, D. 1992. 10Sa RNA: processing by and inhibition of RNase III. Biochem. Int. 26, 1115–1124.

    CAS  PubMed  Google Scholar 

  • Marchand, I., Nicholson, A.W., and Dreyfus, M. 2001. Bacteriophage T7 protein kinase phosphorylates RNase E and stabilizes mRNAs synthesized by T7 RNA polymerase. Mol. Microbiol. 42, 767–776.

    Article  CAS  PubMed  Google Scholar 

  • Martin, W., Rujan, T., Richly, E., Hansen, A., Cornelsen, S., Lins, T., Leister, D., Stoebe, B., Hasegawa, M., and Penny, D. 2002. Evolutionary analysis of Arabidopsis, cyanobacterial, and chloroplast genomes reveals plastid phylogeny and thousands of cyanobacterial genes in the nucleus. Proc. Natl. Acad. Sci. USA 99, 12246–12251.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Masse, E., Escorcia, F.E., and Gottesman, S. 2003. Coupled degradation of a small regulatory RNA and its mRNA targets in Escherichia coli. Genes Dev. 17, 2374–2383.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Matsunaga, J., Dyer, M., Simons, E.L., and Simons, R.W. 1996a. Expression and regulation of the rnc and pdxJ operons of Escherichia coli. Mol. Microbiol. 22, 977–989.

    Article  CAS  PubMed  Google Scholar 

  • Matsunaga, J., Simons, E.L., and Simons, R.W. 1996b. RNase III autoregulation: structure and function of rncO, the posttranscriptional “operator”. RNA 2, 1228–1240.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mayer, J.E. and Schweiger, M. 1983. RNase III is positively regulated by T7 protein kinase. J. Biol. Chem. 258, 5340–5343.

    Article  CAS  PubMed  Google Scholar 

  • McClure, B.A., Haring, V., Ebert, P.R., Anderson, M.A., Simpson, R.J., Sakiyama, F., and Clarke, A.E. 1989. Style self-incompatibility gene products of Nicotiana alata are ribonucleases. Nature 342, 955–957.

    Article  CAS  PubMed  Google Scholar 

  • McDowall, K.J. and Cohen, S.N. 1996. The N-terminal domain of the rne gene product has RNase E activity and is non-overlapping with the arginine-rich RNA-binding site. J. Mol. Biol. 255, 349–355.

    Article  CAS  PubMed  Google Scholar 

  • Miczak, A., Kaberdin, V.R., Wei, C.L., and Lin-Chao, S. 1996. Proteins associated with RNase E in a multicomponent ribonucleolytic complex. Proc. Natl. Acad. Sci. USA 93, 3865–3869.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mohanty, B.K. and Kushner, S.R. 2003. Genomic analysis in Escherichia coli demonstrates differential roles for polynucleotide phosphorylase and RNase II in mRNA abundance and decay. Mol. Microbiol. 50, 645–658.

    Article  CAS  PubMed  Google Scholar 

  • Monzingo, A.F., Gao, J., Qiu, J., Georgiou, G., and Robertus, J.D. 2003. The X-ray structure of Escherichia coli RraA (MenG), A protein inhibitor of RNA processing. J. Mol. Biol. 332, 1015–1024.

    Article  CAS  PubMed  Google Scholar 

  • Moore, C.J., Go, H., Shin, E., Ha, H.J., Song, S., Ha, N.C., Kim, Y.H., Cohen, S.N., and Lee, K. 2021. Substrate-dependent effects of quaternary structure on RNase E activity. Genes Dev. doi:https://doi.org/10.1101/gad.335828.119.

    Google Scholar 

  • Morita, T., Maki, K., and Aiba, H. 2005. RNase E-based ribonucleoprotein complexes: mechanical basis of mRNA destabilization mediated by bacterial noncoding RNAs. Genes Dev. 19, 2176–2186.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Murashko, O.N., Kaberdin, V.R., and Lin-Chao, S. 2012. Membrane binding of Escherichia coli RNase E catalytic domain stabilizes protein structure and increases RNA substrate affinity. Proc. Natl. Acad. Sci. USA 109, 7019–7024.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Na, D. 2020. User guides for biologists to learn computational methods. J. Microbiol. 58, 173–175.

    Article  PubMed  Google Scholar 

  • Neu, H.C. and Heppel, L.A. 1964a. Some observations on the “Latent” ribonuclease of Escherichia coli. Proc. Natl. Acad. Sci. USA 51, 1267–1274.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Neu, H.C. and Heppel, L.A. 1964b. The release of ribonuclease into the medium when Escherichia coli cells are converted to speroplasts. J. Biol. Chem. 239, 3893–3900.

    Article  CAS  PubMed  Google Scholar 

  • Neu, H.C. and Heppel, L.A. 1965. The release of enzymes from Escherichia coli by osmotic shock and during the formation of spheroplasts. J. Biol. Chem. 240, 3685–3692.

    Article  CAS  PubMed  Google Scholar 

  • Nicholson, A.W. 2014. Ribonuclease III mechanisms of double-stranded RNA cleavage. Wiley Interdiscip. Rev. RNA 5, 31–48.

    Article  CAS  PubMed  Google Scholar 

  • Nimmo, R.A. and Slack, F.J. 2009. An elegant miRror: microRNAs in stem cells, developmental timing and cancer. Chromosoma 118, 405–418.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nossal, N.G. and Singer, M.F. 1968. The processive degradation of individual polyribonucleotide chains. I. Escherichia coli ribonuclease II. J. Biol. Chem. 243, 913–922.

    Article  CAS  PubMed  Google Scholar 

  • Ota, H., Sakurai, M., Gupta, R., Valente, L., Wulff, B.E., Ariyoshi, K., Iizasa, H., Davuluri, R.V., and Nishikura, K. 2013. ADAR1 forms a complex with Dicer to promote microRNA processing and RNA-induced gene silencing. Cell 153, 575–589.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Papageorgiou, A.C., Shapiro, R., and Acharya, K.R. 1997. Molecular recognition of human angiogenin by placental ribonuclease inhibitor-an X-ray crystallographic study at 2.0 angstrom resolution. EMBO J. 16, 5162–5177.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Paudyal, S., Alfonso-Prieto, M., Carnevale, V., Redhu, S.K., Klein, M.L., and Nicholson, A.W. 2015. Combined computational and experimental analysis of a complex of ribonuclease III and the regulatory macrodomain protein, YmdB. Proteins 83, 459–472.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pepin, G., Perron, M.P., and Provost, P. 2012. Regulation of human Dicer by the resident ER membrane protein CLIMP-63. Nucleic Acids Res. 40, 11603–11617.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pfeiffer, V., Papenfort, K., Lucchini, S., Hinton, J.C., and Vogel, J. 2009. Coding sequence targeting by MicC RNA reveals bacterial mRNA silencing downstream of translational initiation. Nat. Struct. Mol. Biol. 16, 840–846.

    Article  CAS  PubMed  Google Scholar 

  • Pietras, Z., Hardwick, S.W., Swiezewski, S., and Luisi, B.F. 2013. Potential regulatory interactions of Escherichia coli RraA protein with DEAD-box helicases. J. Biol. Chem. 288, 31919–31929.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Portier, C., Dondon, L., Grunberg-Manago, M., and Régnier, P. 1987. The first step in the functional inactivation of the Escherichia coli polynucleotide phosphorylase messenger is a ribonuclease III processing at the 5′ end. EMBO J. 6, 2165–2170.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Prévost, K., Desnoyers, G., Jacques, J.F., Lavoie, F., and Massé, E. 2011. Small RNA-induced mRNA degradation achieved through both translation block and activated cleavage. Genes Dev. 25, 385–396.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Purusharth, R.I., Klein, F., Sulthana, S., Jäger, S., Jagannadham, M.V., Evguenieva-Hackenberg, E., Ray, M.K., and Klug, G. 2005. Exoribonuclease R interacts with endoribonuclease E and an RNA helicase in the psychrotrophic bacterium Pseudomonas syringae Lz4W. J. Biol. Chem. 280, 14572–14578.

    Article  CAS  PubMed  Google Scholar 

  • Py, B., Higgins, C.F., Krisch, H.M., and Carpousis, A.J. 1996. A DEAD-box RNA helicase in the Escherichia coli RNA degradosome. Nature 381, 169–172.

    Article  CAS  PubMed  Google Scholar 

  • Qi, D., Alawneh, A.M., Yonesaki, T., and Otsuka, Y. 2015. Rapid degradation of host mRNAs by stimulation of RNase E activity by Srd of bacteriophage T4. Genetics 201, 977–987.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qiao, H., Wang, H., Zhao, L., Zhou, J., Huang, J., Zhang, Y., and Xue Y. 2004. The F-box protein AhSLF-S2 physically interacts with S-RNases that may be inhibited by the ubiquitin/26S proteasome pathway of protein degradation during compatible pollination in Antirrhinum. Plant Cell 16, 582–595.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rådmark, O., Werz, O., Steinhilber, D., and Samuelsson, B. 2007. 5-Lipoxygenase: regulation of expression and enzyme activity. Trends Biochem. Sci. 32, 332–341.

    Article  PubMed  CAS  Google Scholar 

  • Regnier, P. and Portier, C. 1986. Initiation, attenuation and RNase III processing of transcripts from the Escherichia coli operon encoding ribosomal protein S15 and polynucleotide phosphorylase. J. Mol. Biol. 187, 23–32.

    Article  CAS  PubMed  Google Scholar 

  • Ren, J., Lee, J., and Na, D. 2020. Recent advances in genetic engineering tools based on synthetic biology. J. Microbiol. 58, 1–10.

    Article  CAS  PubMed  Google Scholar 

  • Richards, J., Luciano, D.J., and Belasco, J.G. 2012. Influence of translation on RppH-dependent mRNA degradation in Escherichia coli. Mol. Microbiol. 86, 1063–1072.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Richards, J., Mehta, P., and Karzai, A.W. 2006. RNase R degrades non-stop mRNAs selectively in an SmpB-tmRNA-dependent manner. Mol. Microbiol. 62, 1700–1712.

    Article  CAS  PubMed  Google Scholar 

  • Robert-Le Meur, M. and Portier, C. 1992. E. coli polynucleotide phosphorylase expression is autoregulated through an RNase III-dependent mechanism. EMBO J. 11, 2633–2641.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Robertson, E.S., Aggison, L.A., and Nicholson, A.W. 1994. Phosphorylation of elongation factor G and ribosomal protein S6 in bacteriophage T7-infected Escherichia coli. Mol. Microbiol. 11, 1045–1057.

    Article  CAS  PubMed  Google Scholar 

  • Rutkoski, T.J. and Raines, R.T. 2008. Evasion of ribonuclease inhibitor as a determinant of ribonuclease cytotoxicity. Curr. Pharm. Biotechnol. 9, 185.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schilling, B., Christensen, D., Davis, R., Sahu, A.K., Hu, L.I., Walker-Peddakotla, A., Sorensen, D.J., Zemaitaitis, B., Gibson, B.W., and Wolfe, A.J. 2015. Protein acetylation dynamics in response to carbon overflow in Escherichia coli. Mol. Microbiol. 98, 847–863.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sevcik, J., Urbanikova, L., Dauter, Z., and Wilson, K.S. 1998. Recognition of RNase Sa by the inhibitor barstar: structure of the complex at 1.7 A resolution. Acta Crystallogr. D Biol. Crystallogr. 54, 954–963.

    Article  CAS  PubMed  Google Scholar 

  • Shapiro, R. 2001. Cytoplasmic ribonuclease inhibitor. Methods Enzymol. 341, 611–628.

    Article  CAS  PubMed  Google Scholar 

  • Shen, H., Liu, H., Wang, H., Teng, M., and Li, X. 2013. Preliminary crystallographic analysis of RraB from Escherichia coli. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 69, 1268–1271.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sim, S., Kim, K., and Lee, Y. 2002. 3′-end processing of precursor M1 RNA by the N-terminal half of RNase E. FEBS Lett. 529, 225–231.

    Article  CAS  PubMed  Google Scholar 

  • Sim, M., Lim, B., Sim, S.H., Kim, D., Jung, E., Lee, Y., and Lee, K. 2014. Two tandem RNase III cleavage sites determine betT mRNA stability in response to osmotic stress in Escherichia coli. PLoS ONE 9, e100520.

    Article  PubMed  PubMed Central  Google Scholar 

  • Sim, S.H., Yeom, J.H., Shin, C., Song, W.S., Shin, E., Kim, H.M., Cha, C.J., Han, S.H., Ha, N.C., Kim, S.W., et al. 2010. Escherichia coli ribonuclease III activity is downregulated by osmotic stress: consequences for the degradation of bdm mRNA in biofilm formation. Mol. Microbiol. 75, 413–425.

    Article  CAS  PubMed  Google Scholar 

  • Sims, T.L. and Ordanic, M. 2001. Identification of a S-ribonuclease-binding protein in Petunia hybrida. Plant Mol. Biol. 47, 771–783.

    Article  CAS  PubMed  Google Scholar 

  • Singh, D., Chang, S.J., Lin, P.H., Averina, O.V., Kaberdin, V.R., and Lin-Chao, S. 2009. Regulation of ribonuclease E activity by the L4 ribosomal protein of Escherichia coli. Proc. Natl. Acad. Sci. USA 106, 864–869.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Song, L., Gao, S., Jiang, W., Chen, S., Liu, Y., Zhou, L., and Huang, W. 2011. Silencing suppressors: viral weapons for countering host cell defenses. Protein Cell 2, 273–281.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Song, W., Kim, Y.H., Sim, S.H., Hwang, S., Lee, J.H., Lee, Y., Bae, J., Hwang, J., and Lee, K. 2014. Antibiotic stress-induced modulation of the endoribonucleolytic activity of RNase III and RNase G confers resistance to aminoglycoside antibiotics in Escherichia coli. Nucleic Acids Res. 42, 4669–4681.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Song, L., Wang, G., Malhotra, A., Deutscher, M.P., and Liang, W. 2016. Reversible acetylation on Lys501 regulates the activity of RNase II. Nucleic Acids Res. 44, 1979–1988.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sousa, S., Marchand, I., and Dreyfus, M. 2001. Autoregulation allows Escherichia coli RNase E to adjust continuously its synthesis to that of its substrates. Mol. Microbiol. 42, 867–878.

    Article  CAS  PubMed  Google Scholar 

  • Spahr, P.F. and Gesteland, R.F. 1968. Specific cleavage of bacteriophage R17 RNA by an endonuclease isolated from E. coli MRE-600. Proc. Natl. Acad. Sci. USA 59, 876–883.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Srivastava, S.K., Cannistraro, V.J., and Kennell, D. 1992. Broad-specificity endoribonucleases and mRNA degradation in Escherichia coli. J. Bacteriol. 174, 56–62.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sulthana, S., Basturea, G.N., and Deutscher, M.P. 2016. Elucidation of pathways of ribosomal RNA degradation: an essential role for RNase E. RNA 22, 1163–1171.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takayama, S. and Isogai, A. 2005. Self-incompatibility in plants. Annu. Rev. Plant Biol. 56, 467–489.

    Article  CAS  PubMed  Google Scholar 

  • Tang, X., Li, M., Tucker, L., and Ramratnam, B. 2011. Glycogen synthase kinase 3 beta (GSK3β) phosphorylates the RNAase III enzyme Drosha at S300 and S302. PLoS ONE 6, e20391.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tang, X., Wen, S., Zheng, D., Tucker, L., Cao, L.L., Pantazatos, D., Moss, S.F., and Ramratnam, B. 2013. Acetylation of Drosha on the N-terminus inhibits its degradation by ubiquitination. PLoS ONE 8, e72503.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tang, X., Zhang, Y., Tucker, L., and Ramratnam, B. 2010. Phosphorylation of the RNase III enzyme Drosha at Serine300 or Serine302 is required for its nuclear localization. Nucleic Acids Res. 38, 6610–6619.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tock, M.R., Walsh, A.P., Carroll, G., and McDowall, K.J. 2000. The CafA protein required for the 5′-maturation of 16S rRNA is a 5′-end-dependent ribonuclease that has context-dependent broad sequence specificity. J. Biol. Chem. 275, 8726–8732.

    Article  CAS  PubMed  Google Scholar 

  • Ueno, H. and Yonesaki, T. 2004. Phage-induced change in the stability of mRNAs. Virology 329, 134–141.

    Article  CAS  PubMed  Google Scholar 

  • Ulferts, R. and Ziebuhr, J. 2011. Nidovirus ribonucleases: structures and functions in viral replication. RNA Biol. 8, 295–304.

    Article  CAS  PubMed  Google Scholar 

  • Van den Bossche, A., Hardwick, S.W., Ceyssens, P.J., Hendrix, H., Voet, M., Dendooven, T., Bandyra, K.J., De Maeyer, M., Aertsen, A., Noben, J.P., et al. 2016. Structural elucidation of a novel mechanism for the bacteriophage-based inhibition of the RNA degradosome. Elife 5, e16413.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • van Rij, R.P. and Berezikov, E. 2009. Small RNAs and the control of transposons and viruses in Drosophila. Trends Microbiol. 17, 163–171.

    Article  CAS  PubMed  Google Scholar 

  • Venkataraman, K., Guja, K.E., Garcia-Diaz, M., and Karzai, A.W. 2014. Non-stop mRNA decay: a special attribute of trans-translation mediated ribosome rescue. Front. Microbiol. 5, 93.

    Article  PubMed  PubMed Central  Google Scholar 

  • Vermeulen, A., Behlen, L., Reynolds, A., Wolfson, A., Marshall, W.S., Karpilow, J., and Khvorova, A. 2005. The contributions of dsRNA structure to Dicer specificity and efficiency. RNA 11, 674–682.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vincent, H.A. and Deutscher, M.P. 2006. Substrate recognition and catalysis by the exoribonuclease RNase R. J. Biol. Chem. 281, 29769–29775.

    Article  CAS  PubMed  Google Scholar 

  • Vincent, H.A. and Deutscher, M.P. 2009a. Insights into how RNase R degrades structured RNA: analysis of the nuclease domain. J. Mol. Biol. 387, 570–583.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vincent, H.A. and Deutscher, M.P. 2009b. 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 

  • Voss, J.E., Luisi, B.F., and Hardwick, S.W. 2014. Molecular recognition of RhlB and RNase D in the Caulobacter crescentus RNA degradosome. Nucleic Acids Res. 42, 13294–13305.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wachi, M., Umitsuki, G., Shimizu, M., Takada, A., and Nagai, K. 1999. Escherichia coli cafA gene encodes a novel RNase, designated as RNase G, involved in processing of the 5′ end of 16S rRNA. Biochem. Biophys. Res. Commun. 259, 483–488.

    Article  CAS  PubMed  Google Scholar 

  • Wahid, F., Shehzad, A., Khan, T., and Kim, Y.Y. 2010. MicroRNAs: synthesis, mechanism, function, and recent clinical trials. Biochim. Biophys. Acta 1803, 1231–1243.

    Article  CAS  PubMed  Google Scholar 

  • Wang, Y., Kato, N., Jazag, A., Dharel, N., Otsuka, M., Taniguchi, H., Kawabe, T., and Omata, M. 2006. Hepatitis C virus core protein is a potent inhibitor of RNA silencing-based antiviral response. Gastroenterology 130, 883–892.

    Article  CAS  PubMed  Google Scholar 

  • Wang, H.W., Noland, C., Siridechadilok, B., Taylor, D.W., Ma, E.B., Felderer, K., Doudna, J.A., and Nogales, E. 2009. Structural insights into RNA processing by the human RISC-loading complex. Nat. Struct. Mol. Biol. 16, 1148–1153.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weinert, B.T., Iesmantavicius, V., Wagner, S.A., Schölz, C., Gummesson, B., Beli, P., Nyström, T., and Choudhary, C. 2013. Acetylphosphate is a critical determinant of lysine acetylation in E. coli. Mol. Cell 51, 265–272.

    Article  CAS  PubMed  Google Scholar 

  • Williams, J.S., Wu, L., Li, S., Sun, P., and Kao, T.H. 2015. Insight into S-RNase-based self-incompatibility in Petunia: recent findings and future directions. Front. Plant Sci. 6, 41.

    Article  PubMed  PubMed Central  Google Scholar 

  • Wilson, R.C., Tambe, A., Kidwell, M.A., Noland, C.L., Schneider, C.P., and Doudna, J.A. 2015. Dicer-TRBP complex formation ensures accurate mammalian microRNA biogenesis. Mol. Cell 57, 397–407.

    Article  CAS  PubMed  Google Scholar 

  • Wool, I.G. 1996. Extraribosomal functions of ribosomal proteins. Trends Biochem. Sci. 21, 164–165.

    Article  CAS  PubMed  Google Scholar 

  • Worrall, J.A., Górna, M., Crump, N.T., Phillips, L.G., Tuck, A.C., Price, A.J., Bavro, V.N., and Luisi, B.F. 2008. Reconstitution and analysis of the multienzyme Escherichia coli RNA degradosome. J. Mol. Biol. 382, 870–883.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yakovlev, G.I., Moiseyev, G.P., Protasevich, II, Ranjbar, B., Bocharov, A.L., Kirpichnikov, M.P., Gilli, R.M., Briand, C.M., Hartley, R.W., and Makarov, A.A. 1995. Dissociation constants and thermal stability of complexes of Bacillus intermedius RNase and the protein inhibitor of Bacillus amyloliquefaciens RNase. FEBS Lett. 366, 156–158.

    Article  CAS  PubMed  Google Scholar 

  • Yang, W., Chendrimada, T.P., Wang, Q., Higuchi, M., Seeburg, P.H., Shiekhattar, R., and Nishikura, K. 2006. Modulation of microRNA processing and expression through RNA editing by ADAR deaminases. Nat. Struct. Mol. Biol. 13, 13–21.

    Article  CAS  PubMed  Google Scholar 

  • Yang, Q., Li, W., She, H., Dou, J., Duong, D.M., Du, Y., Yang, S.H., Seyfried, N.T., Fu, H.A., Gao, G.D., et al. 2015. Stress induces p38 MAPK-mediated phosphorylation and inhibition of Drosha-dependent cell survival. Mol. Cell 57, 721–734.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yates, J.L. and Nomura, M. 1980. E. coli ribosomal protein L4 is a feedback regulatory protein. Cell 21, 517–522.

    Article  CAS  PubMed  Google Scholar 

  • Ye, P.Y., Liu, Y., Chen, C., Tang, F., Wu, Q., Wang, X., Liu, C.G., Liu, X., Liu, R., Liu, Y., et al. 2015. An mTORC1-Mdm2-Drosha Axis for miRNA biogenesis in response to glucose- and amino acid-deprivation. Mol. Cell 57, 708–720.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yeom, J.H., Go, H., Shin, E., Kim, H.L., Han, S.H., Moore, C.J., Bae, J., and Lee, K. 2008a. Inhibitory effects of RraA and RraB on RNAse E-related enzymes imply conserved functions in the regulated enzymatic cleavage of RNA. FEMS Microbiol. Lett. 285, 10–15.

    Article  CAS  PubMed  Google Scholar 

  • Yeom, J.H., Shin, E., Go, H., Sim, S.H., Seong, M.J., and Lee, K. 2008b. Functional implications of the conserved action of regulators of ribonuclease activity. J. Microbiol. Biotechnol. 18, 1353–1356.

    CAS  PubMed  Google Scholar 

  • Young, R.A. and Steitz, J.A. 1978. Complementary sequences 1700 nucleotides apart form a ribonuclease III cleavage site in Escherichia coli ribosomal precursor RNA. Proc. Natl. Acad. Sci. USA 75, 3593–3597.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zeng, Y., Yi, R., and Cullen, B.R. 2003. MicroRNAs and small interfering RNAs can inhibit mRNA expression by similar mechanisms. Proc. Natl. Acad. Sci. USA 100, 9779–9784.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang, J.Y., Deng, X.M., Li, F.P., Wang, L., Huang, Q.Y., Zhang, C.C., and Chen, W.L. 2014. RNase E forms a complex with polynucleotide phosphorylase in cyanobacteria via a cyanobacterial-specific nonapeptide in the noncatalytic region. RNA 20, 568–579.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang, D., de Souza, R.F., Anantharaman, V., Iyer, L.M., and Aravind, L. 2012. Polymorphic toxin systems: comprehensive characterization of trafficking modes, processing, mechanisms of action, immunity and ecology using comparative genomics. Biol. Direct 7, 18.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang, K., Zheng, S., Yang, J.S., Chen, Y., and Cheng, Z. 2013. Comprehensive profiling of protein lysine acetylation in Escherichia coli. J. Proteome Res. 12, 844–851.

    Article  CAS  PubMed  Google Scholar 

  • Zhao, L., Huang, J., Zhao, Z., Li, Q., Sims, T.L., and Xue, Y. 2010. The Skp1-like protein SSK1 is required for cross-pollen compatibility in S-RNase-based self-incompatibility. Plant J. 62, 52–63.

    Article  CAS  PubMed  Google Scholar 

  • Zhao, Y. and Srivastava, D. 2007. A developmental view of microRNA function. Trends Biochem. Sci. 32, 189–197.

    Article  CAS  PubMed  Google Scholar 

  • Zhou, C., Zhang, J., Hu, X., Li, C., Wang, L., Huang, Q., and Chen, W. 2020. RNase II binds to RNase E and modulates its endoribonucleolytic activity in the cyanobacterium Anabaena PCC 7120. Nucleic Acids Res. 48, 3922–3934.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu, L.Q., Gangopadhyay, T., Padmanabha, K.P., and Deutscher, M.P. 1990. Escherichia coli rna gene encoding RNase I: cloning, overexpression, subcellular distribution of the enzyme, and use of an rna deletion to identify additional RNases. J. Bacteriol. 172, 3146–3151.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zilhão, R., Cairrão, F., Régnier, P., and Arraiano, C.M. 1996. PNPase modulates RNase II expression in Escherichia coli: implications for mRNA decay and cell metabolism. Mol. Microbiol. 20, 1033–1042.

    Article  PubMed  Google Scholar 

  • Zilhão, R., Régnier, P., and Arraiano, C.M. 1995. The role of endonucleases in the expression of ribonuclease II in Escherichia coli. FEMS Microbiol. Lett. 130, 237–244.

    Article  PubMed  Google Scholar 

  • Zundel, M.A., Basturea, G.N., and Deutscher, M.P. 2009. Initiation of ribosome degradation during starvation in Escherichia coli. RNA 15, 977–983.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zuo, Y., Vincent, H.A., Zhang, J., Wang, Y., Deutscher, M.P., and Malhotra, A. 2006. Structural basis for processivity and single-strand specificity of RNase II. Mol. Cell 24, 149–156.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This research was supported by the Chung-Ang University Graduate Research Scholarship in 2017 and the National Research Foundation of Korea (NRF) (grant no. 2019R1I1-A1A01063517 to M. L).

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Lee, J., Lee, M. & Lee, K. Trans-acting regulators of ribonuclease activity. J Microbiol. 59, 341–359 (2021). https://doi.org/10.1007/s12275-021-0650-6

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