Display options
Cite
Mohanty BK, Kushner SR. Inactivation of RNase P in Escherichia coli significantly changes post-transcriptional RNA metabolism. Mol Microbiol. 2021;117(1):121-142doi: 10.1111/mmi.14808.
Mohanty, B. K., & Kushner, S. R. (2022). Inactivation of RNase P in Escherichia coli significantly changes post-transcriptional RNA metabolism. Molecular microbiology, 117(1), 121-142. https://doi.org/10.1111/mmi.14808
Mohanty, Bijoy K, and Kushner, Sidney R. "Inactivation of RNase P in Escherichia coli significantly changes post-transcriptional RNA metabolism." Molecular microbiology vol. 117,1 (2022): 121-142. doi: https://doi.org/10.1111/mmi.14808
Mohanty BK, Kushner SR. Inactivation of RNase P in Escherichia coli significantly changes post-transcriptional RNA metabolism. Mol Microbiol. 2022 Jan;117(1):121-142. doi: 10.1111/mmi.14808. Epub 2021 Sep 25. PMID: 34486768.
Copy Download .nbib Format: NLM
Share it on

Mol Microbiol. 2022 Jan;117(1):121-142. doi: 10.1111/mmi.14808. Epub 2021 Sep 25.

Inactivation of RNase P in Escherichia coli significantly changes post-transcriptional RNA metabolism.

Molecular microbiology

Bijoy K Mohanty, Sidney R Kushner

Affiliations

  1. Department of Genetics, University of Georgia, Athens, Georgia, USA.
  2. Department of Microbiology, University of Georgia, Athens, Georgia, USA.

PMID: 34486768 DOI: 10.1111/mmi.14808

Abstract

Ribonuclease P (RNase P), which is required for the 5'-end maturation of tRNAs in every organism, has been shown to play a limited role in other aspects of RNA metabolism in Escherichia coli. Using RNA-sequencing (RNA-seq), we demonstrate that RNase P inactivation affects the abundances of ~46% of the expressed transcripts in E. coli and provide evidence that its essential function is its ability to generate pre-tRNAs from polycistronic tRNA transcripts. The RNA-seq results agreed with the published data and northern blot analyses of 75/83 transcripts (mRNAs, sRNAs, and tRNAs). Changes in transcript abundances in the RNase P mutant also correlated with changes in their half-lives. Inactivating the stringent response did not alter the rnpA49 phenotype. Most notably, increases in the transcript abundances were observed for all genes in the cysteine regulons, multiple toxin-antitoxin modules, and sigma S-controlled genes. Surprisingly, poly(A) polymerase (PAP I) modulated the abundances of ~10% of the transcripts affected by RNase P. A comparison of the transcriptomes of RNase P, RNase E, and RNase III mutants suggests that they affect distinct substrates. Together, our work strongly indicates that RNase P is a major player in all aspects of post-transcriptional RNA metabolism in E. coli.

© 2021 John Wiley & Sons Ltd.

Keywords: genome-wide RNA-seq; polyadenylation; sRNA; transcriptome

References

  1. Agrawal, A., Mohanty, B.K. & Kushner, S.R. (2014) Processing of the seven valine tRNAs in Escherichia coli involves novel features of RNase P. Nucleic Acids Research, 42, 11166-11179. https://doi.org/10.1093/nar/gku758 - PubMed
  2. Alifano, P., Rivellini, F., Piscitelli, C., Arraiano, C.M., Bruni, C.B. & Carlomagno, M.S. (1994) Ribonuclease E provides substrates for ribonuclease P-dependent processing of a polycistronic mRNA. Genes and Development, 8, 3021-3031. https://doi.org/10.1101/gad.8.24.3021 - PubMed
  3. Altuvia, S., Weinstein-Fischer, D., Zhang, A., Postow, L. & Storz, G. (1997) A small, stable RNA induced by oxidative stress: role as a pleiotropic regulator and antimutator. Cell, 90, 43-53. https://doi.org/10.1016/S0092-8674(00)80312-8 - PubMed
  4. August, J., Ortiz, P.J. & Hurwitz, J. (1962) Ribonucleic acid-dependent ribonucleotide incorporation. I. Purification and properties of the enzyme. Journal of Biological Chemistry, 237, 3786-3793. https://doi.org/10.1016/S0021-9258(19)84523-4 - PubMed
  5. Babitzke, P. & Kushner, S.R. (1991) The Ams (altered mRNA stability) protein and ribonuclease E are encoded by the same structural gene of Escherichia coli. Proceedings of the National Academy of Sciences of the United States of America, 88, 1-5. https://doi.org/10.1073/pnas.88.1.1 - PubMed
  6. Baer, M.F., Wesolowski, D. & Altman, S. (1989) Characterization in vitro of the defect in a temperature-sensitive mutant of the protein subunit of RNase P from Escherichia coli. Journal of Bacteriology, 171, 6862-6866. https://doi.org/10.1128/jb.171.12.6862-6866.1989 - PubMed
  7. Battesti, A. & Bouveret, E. (2006) Acyl carrier protein/SpoT interaction, the switch linking SpoT-dependent stress response to fatty acid metabolism. Molecular Microbiology, 62, 1048-1063. https://doi.org/10.1111/j.1365-2958.2006.05442.x - PubMed
  8. Bech, F.W., Jorgensen, S.T., Diderichsen, B. & Karlstrom, O.H. (1985) Sequence of the relB transcription unit from Escherichia coli and identification of the relB gene. The EMBO Journal, 4, 1059-1066. https://doi.org/10.1002/j.1460-2075.1985.tb03739.x - PubMed
  9. Bechhofer, D.H. & Deutscher, M.P. (2019) Bacterial ribonucleases and their roles in RNA metabolism. Critical Reviews in Biochemistry and Molecular Biology, 54, 242-300. https://doi.org/10.1080/10409238.2019.1651816 - PubMed
  10. Benjamini, Y. & Hochberg, Y. (1995) Controlling the false discovery rate - a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society Series B-Statistical Methodology, 57, 289-300. https://doi.org/10.1111/j.2517-6161.1995.tb02031.x - PubMed
  11. Blum, E., Carpousis, A.J. & Higgins, C.F. (1999) Polyadenylation promotes degradation of 3'-structured RNA by the Escherichia coli mRNA degradosome in vitro. Journal of Biological Chemistry, 274, 4009-4016. https://doi.org/10.1074/jbc.274.7.4009 - PubMed
  12. Bothwell, A.L., Stark, B.C. & Altman, S. (1976) Ribonuclease P substrate specificity: cleavage of a bacteriophage phi80-induced RNA. Proceedings of the National Academy of Sciences of the United States of America, 73, 1912-1916. https://doi.org/10.1073/pnas.73.6.1912 - PubMed
  13. Chonoles Imlay, K.R., Korshunov, S. & Imlay, J.A. (2015) Physiological roles and adverse effects of the two cystine importers of Escherichia coli. Journal of Bacteriology, 197, 3629-3644. https://doi.org/10.1128/JB.00277-15 - PubMed
  14. Chung, D.-H., Min, Z., Wang, B.-C. & Kushner, S.R. (2010) Single amino acid changes in the predicted RNase H domain of E. coli RNase G lead to the complementation of RNase E mutants. RNA, 16, 1371-1385. - PubMed
  15. Clarke, J.E., Kime, L., Romero, A.D. & McDowall, K.J. (2014) Direct entry by RNase E is a major pathway for the degradation and processing of RNA in Escherichia coli. Nucleic Acids Research, 42, 11733-11751. - PubMed
  16. Coburn, G.A. & Mackie, G.A. (1996) Differential sensitivities of portions of the mRNA for ribosomal protein S20 to 3'-exonucleases is dependent on oligoadenylation and RNA secondary structure. Journal of Biological Chemistry, 271, 15776-15781. - PubMed
  17. Dunn, J.J. & Studier, F.W. (1973) T7 early RNAs and Escherichia coli ribosomal RNAs are cut from large precursor RNAs in vivo by ribonuclease III. Proceedings of the National Academy of Sciences of the United States of America, 70, 3296-3300. https://doi.org/10.1073/pnas.70.12.3296 - PubMed
  18. Ellis, J.C. & Brown, J.W. (2009) The RNase P family. RNA Biology, 6, 362-369. https://doi.org/10.4161/rna.6.4.9241 - PubMed
  19. Esquerre, T., Laguerre, S., Turlan, C., Carpousis, A.J., Girbal, L. & Cocaign-Bousquet, M. (2014) Dual role of transcription and transcript stability in the regulation of gene expression in Escherichia coli cells cultured on glucose at different growth rates. Nucleic Acids Research, 42, 2460-2472. - PubMed
  20. Fajardo, D.A., Cheung, J., Ito, C., Sugawara, E., Nikaido, H. & Misra, R. (1998) Biochemistry and regulation of a novel Escherichia coli K-12 porin protein, OmpG, which produces unusually large channels. Journal of Bacteriology, 180, 4452-4459. - PubMed
  21. Garrey, S.M. & Mackie, G.A. (2011) Roles of the 5'-phosphate sensor domain in RNase E. Molecular Microbiology, 80, 1613-1624. https://doi.org/10.1111/j.1365-2958.2011.07670.x - PubMed
  22. Gossringer, M., Lechner, M., Brillante, N., Weber, C., Rossmanith, W. & Hartmann, R.K. (2017) Protein-only RNase P function in Escherichia coli: viability, processing defects and differences between PRORP isoenzymes. Nucleic Acids Research, 45, 7441-7454. https://doi.org/10.1093/nar/gkx405 - PubMed
  23. Guerrier-Takada, C., Gardiner, K., Marsh, T., Pace, N. & Altman, S. (1983) The RNA moiety of ribonuclease P is the catalytic subunit of the enzyme. Cell, 35, 849-857. https://doi.org/10.1016/0092-8674(83)90117-4 - PubMed
  24. Gupta, R.S. & Schlessinger, D. (1976) Coupling of rates of transcription, translation, and messenger ribonucleic acid degradation in streptomycin-dependent mutants of Escherichia coli. Journal of Bacteriology, 125, 84-93. https://doi.org/10.1128/jb.125.1.84-93.1976 - PubMed
  25. Hansen, A., Pfeiffer, T., Zuleeg, T., Limmer, S., Ciesiolka, J., Feltens, R. et al. (2001) Exploring the minimal substrate requirements for trans-cleavage by RNase P holoenzymes from Escherichia coli and Bacillus subtilis. Molecular Microbiology, 41, 131-143. https://doi.org/10.1046/j.1365-2958.2001.02467.x - PubMed
  26. Harms, A., Brodersen, D.E., Mitarai, N. & Gerdes, K. (2018) Toxins, targets, and triggers: an overview of toxin-antitoxin biology. Molecular Cell, 70, 768-784. https://doi.org/10.1016/j.molcel.2018.01.003 - PubMed
  27. Hartmann, R.K., Heinrich, J., Schlegl, J. & Schuster, H. (1995) Precursor of C4 antisense RNA of bacteriophages P1 and P7 is a substrate for RNase P of Escherichia coli. Proceedings of the National Academy of Sciences of the United States of America, 92, 5822-5826. https://doi.org/10.1073/pnas.92.13.5822 - PubMed
  28. Hashimoto, M., Ichimura, T., Mizoguchi, H., Tanaka, K., Fujimitsu, K., Keyamura, K. et al. (2005) Cell size and nucleoid organization of engineered Escherichia coli cells with a reduced genome. Molecular Microbiology, 55, 137-149. https://doi.org/10.1111/j.1365-2958.2004.04386.x - PubMed
  29. Hryniewicz, M.M. & Kredich, N.M. (1994) Stoichiometry of binding of CysB to the cysJIH, cysK, and cysP promoter regions of Salmonella typhimurium. Journal of Bacteriology, 176, 3673-3682. https://doi.org/10.1128/jb.176.12.3673-3682.1994 - PubMed
  30. Iost, I. & Dreyfus, M. (1995) The stability of Escherichia coli lacZ mRNA depends upon the simultaneity of its synthesis and translation. The EMBO Journal, 14, 3252-3261. https://doi.org/10.1002/j.1460-2075.1995.tb07328.x - PubMed
  31. Irving, S.E., Choudhury, N.R. & Corrigan, R.M. (2021) The stringent response and physiological roles of (pp)pGpp in bacteria. Nature Reviews Microbiology, 19, 256-271. https://doi.org/10.1038/s41579-020-00470-y - PubMed
  32. Jarrous, N. & Gopalan, V. (2010) Archaeal/eukaryal RNase P: subunits, functions and RNA diversification. Nucleic Acids Research, 38, 7885-7894. https://doi.org/10.1093/nar/gkq701 - PubMed
  33. Jishage, M. & Ishihama, A. (1995) Regulation of RNA polymerase sigma subunit synthesis in Escherichia coli: intracellular levels of sigma 70 and sigma 38. Journal of Bacteriology, 177, 6832-6835. https://doi.org/10.1128/jb.177.23.6832-6835.1995 - PubMed
  34. Kanda, T., Abiko, G., Kanesaki, Y., Yoshikawa, H., Iwai, N. & Wachi, M. (2020) RNase E-dependent degradation of tnaA mRNA encoding tryptophanase is prerequisite for the induction of acid resistance in Escherichia coli. Scientific Reports, 10, 7128. https://doi.org/10.1038/s41598-020-63981-x - PubMed
  35. Kavita, K., de Mets, F. & Gottesman, S. (2018) New aspects of RNA-based regulation by Hfq and its partner sRNAs. Current Opinion in Microbiology, 42, 53-61. https://doi.org/10.1016/j.mib.2017.10.014 - PubMed
  36. Keseler, I.M., Mackie, A., Santos-Zavaleta, A., Billington, R., Bonavides-Martinez, C., Caspi, R. et al. (2017) The EcoCyc database: reflecting new knowledge about Escherichia coli K-12. Nucleic Acids Research, 45, D543-D550. - PubMed
  37. Khodursky, A.B., Peter, B.J., Cozzarelli, N.R., Botstein, D., Brown, P.O. & Yanofsky, C. (2000) DNA microarray analysis of gene expression in response to physiological and genetic changes that affect tryptophan metabolism in Escherichia coli. Proceedings of the National Academy of Sciences of the United States of America, 97, 12170-12175. https://doi.org/10.1073/pnas.220414297 - PubMed
  38. Kim, Y. & Lee, Y. (2009) Novel function of C5 protein as a metabolic stabilizer of M1 RNA. FEBS Letters, 583, 419-429. https://doi.org/10.1016/j.febslet.2008.12.040 - PubMed
  39. Kime, L., Clarke, J.E., Romero, A.D., Grasby, J.A. & McDowall, K.J. (2014) Adjacent single-stranded regions mediate processing of tRNA precursors by RNase E direct entry. Nucleic Acids Research, 42, 4577-4589. https://doi.org/10.1093/nar/gkt1403 - PubMed
  40. Kirsebom, L.A., Baer, M.F. & Altman, S. (1988) Differential effects of mutations in the protein and RNA moieties of RNase P on the efficiency of suppression by various tRNA suppressors. Journal of Molecular Biology, 204, 879-888. https://doi.org/10.1016/0022-2836(88)90048-4 - PubMed
  41. Klein, G., Stupak, A., Biernacka, D., Wojtkiewicz, P., Lindner, B. & Raina, S. (2016) Multiple transcriptional factors regulate transcription of the rpoE gene in Escherichia coli under different growth conditions and when the lipopolysaccharide biosynthesis is defective. Journal of Biological Chemistry, 291, 22999-23019. https://doi.org/10.1074/jbc.M116.748954 - PubMed
  42. Kredich, N.M. (1992) The molecular basis for positive regulation of cys promoters in Salmonella typhimurium and Escherichia coli. Molecular Microbiology, 6, 2747-2753. https://doi.org/10.1111/j.1365-2958.1992.tb01453.x - PubMed
  43. Lee, H., Pine, P.S., McDaniel, J., Salit, M. & Oliver, B. (2016) External RNA controls consortium beta version update. Journal of Genomics, 4, 19-22. https://doi.org/10.7150/jgen.16082 - PubMed
  44. Li, L., Huang, D., Cheung, M.K., Huang, Q. & Kwan, H.S. (2013) BSRD: a repository of bacterial small regulatory RNA. Nucleic Acids Research, 41, D233-D238. - PubMed
  45. Li, Y. & Altman, S. (2003) A specific endoribonuclease, RNase P, affects gene expression of polycistronic operon mRNAs. Proceedings of the National Academy of Sciences of the United States of America, 100, 13213-13218. https://doi.org/10.1073/pnas.2235589100 - PubMed
  46. Li, Y., Cole, K. & Altman, S. (2003) The effect of a single, temperature-sensitive mutation on global gene expression in Escherichia coli. RNA, 9, 518-532. https://doi.org/10.1261/rna.2198203 - PubMed
  47. Li, Z. & Deutscher, M.P. (2002) RNase E plays an essential role in the maturation of Escherichia coli tRNA precursors. RNA, 8, 97-109. https://doi.org/10.1017/S1355838202014929 - PubMed
  48. Lin, H.C., Zhao, J., Niland, C.N., Tran, B., Jankowsky, E. & Harris, M.E. (2016) Analysis of the RNA binding specificity landscape of C5 protein reveals structure and sequence preferences that direct RNase P specificity. Cell Chemical Biology, 23, 1271-1281. https://doi.org/10.1016/j.chembiol.2016.09.002 - PubMed
  49. Lochowska, A., Iwanicka-Nowicka, R., Zaim, J., Witkowska-Zimny, M., Bolewska, K. & Hryniewicz, M.M. (2004) Identification of activating region (AR) of Escherichia coli LysR-type transcription factor CysB and CysB contact site on RNA polymerase alpha subunit at the cysP promoter. Molecular Microbiology, 53, 791-806. https://doi.org/10.1111/j.1365-2958.2004.04161.x - PubMed
  50. Loria, A. & Pan, T. (2000) The 3' substrate determininants for the catalytic efficiency of the Bacillus subtilis RNase P holoenzyme suggest autolytic proccessing of the RNase P RNA in vivo. RNA, 6, 1413-1422. - PubMed
  51. Maes, A., Gracia, C., Innocenti, N., Zhang, K., Aurell, E. & Hajnsdorf, E. (2017) Landscape of RNA polyadenylation in E. coli. Nucleic Acids Research, 45, 2746-2756. - PubMed
  52. Majdalani, N., Hernandez, D. & Gottesman, S. (2002) Regulation and mode of action of the second small RNA activator of RpoS translation, RprA. Molecular Microbiology, 46, 813-826. https://doi.org/10.1046/j.1365-2958.2002.03203.x - PubMed
  53. McClain, W.H., Lai, L.B. & Gopalan, V. (2010) Trials, travails and triumphs: an account of RNA catalysis in RNase P. Journal of Molecular Biology, 397, 627-646. https://doi.org/10.1016/j.jmb.2010.01.038 - PubMed
  54. McCullen, C.A., Benhammou, J.N., Majdalani, N. & Gottesman, S. (2010) Mechanism of positive regulation by DsrA and RprA small noncoding RNAs: pairing increases translation and protects mRNA from degradation. Journal of Bacteriology, 192, 5559-5571. - PubMed
  55. McDowall, K.J., Kaberdin, V.R., Wu, S.-W., Cohen, S.N. & Lin-Chao, S. (1995) Site-specific RNase E cleavage of oligonucleotides and inhibition by stem-loops. Nature, 374, 287-290. https://doi.org/10.1038/374287a0 - PubMed
  56. McDowall, K.J., Lin-Chao, S. & Cohen, S.N. (1994) A + U content rather than a particular nucleotide order determines the specificity of RNase E cleavage. Journal of Biological Chemistry, 269, 10790-10796. https://doi.org/10.1016/S0021-9258(17)34129-7 - PubMed
  57. Mildenhall, K.B., Wiese, N., Chung, D., Maples, V.F., Mohanty, B.K. & Kushner, S.R. (2016) RNase E-based degradosome modulates polyadenylation of mRNAs after Rho-independent transcription terminators in Escherichia coli. Molecular Microbiology, 101, 645-655. - PubMed
  58. Missiakas, D., Mayer, M.P., Lemaire, M., Georgopoulos, C. & Raina, S. (1997) Modulation of the Escherichia coli sigmaE (RpoE) heat-shock transcription-factor activity by the RseA, RseB and RseC proteins. Molecular Microbiology, 24, 355-371. - PubMed
  59. Mohanty, B.K., Agrawal, A. & Kushner, S.R. (2020) Generation of pre-tRNAs from polycistronic operons is the essential function of RNase P in Escherichia coli. Nucleic Acids Research, 48, 2564-2578. https://doi.org/10.1093/nar/gkz1188 - PubMed
  60. Mohanty, B.K., Giladi, H., Maples, V.F. & Kushner, S.R. (2008) Analysis of RNA decay, processing, and polyadenylation in Escherichia coli and other prokaryotes. Methods in Enzymology, 447, 3-29. - PubMed
  61. Mohanty, B.K. & Kushner, S.R. (1999) Analysis of the function of Escherichia coli poly(A) polymerase I in RNA metabolism. Molecular Microbiology, 34, 1094-1108. https://doi.org/10.1046/j.1365-2958.1999.01673.x - PubMed
  62. Mohanty, B.K. & Kushner, S.R. (2003) Genomic analysis in Escherichia coli demonstrates differential roles for polynucleotide phosphorylase and RNase II in mRNA abundance and decay. Molecular Microbiology, 50, 645-658. https://doi.org/10.1046/j.1365-2958.2003.03724.x - PubMed
  63. Mohanty, B.K. & Kushner, S.R. (2006) The majority of Escherichia coli mRNAs undergo post-transcriptional modification in exponentially growing cells. Nucleic Acids Research, 34, 5695-5704. https://doi.org/10.1093/nar/gkl684 - PubMed
  64. Mohanty, B.K. & Kushner, S.R. (2007) Ribonuclease P processes polycistronic tRNA transcripts in Escherichia coli independent of ribonuclease E. Nucleic Acids Research, 35, 7614-7625. https://doi.org/10.1093/nar/gkm917 - PubMed
  65. Mohanty, B.K. & Kushner, S.R. (2008) Rho-independent transcription terminators inhibit RNase P processing of the secG leuU and metT tRNA polycistronic transcripts in Escherichia coli. Nucleic Acids Research, 36, 364-375. https://doi.org/10.1093/nar/gkm991 - PubMed
  66. Mohanty, B.K. & Kushner, S.R. (2010) Processing of the Escherichia coli leuX tRNA transcript, encoding tRNAleu5, requires either the 3'-5' exoribonuclease polynucleotide phosphorylase or RNase P to remove the Rho-independent transcription terminator. Nucleic Acids Research, 38, 597-607. - PubMed
  67. Mohanty, B.K. & Kushner, S.R. (2016) Regulation of mRNA decay in bacteria. Annual Review of Microbiology, 70, 25-44. https://doi.org/10.1146/annurev-micro-091014-104515 - PubMed
  68. Mohanty, B.K. & Kushner, S.R. (2018) Enzymes involved in post-transcriptional RNA metabolism in Gram-negative bacteria. Microbiology Spectrum, 6, RWR-0011-2017. - PubMed
  69. Mohanty, B.K. & Kushner, S.R. (2019a) Analysis of post-transcriptional RNA metabolism in prokaryotes. Methods, 155, 124-130. https://doi.org/10.1016/j.ymeth.2018.11.006 - PubMed
  70. Mohanty, B.K. & Kushner, S.R. (2019b) New insights into the relationship between tRNA processing and polyadenylation in Escherichia coli. Trends in Genetics, 35, 434-445. https://doi.org/10.1016/j.tig.2019.03.003 - PubMed
  71. Mohanty, B.K., Maples, V.F. & Kushner, S.R. (2012) Polyadenylation helps regulate functional tRNA levels in Escherichia coli. Nucleic Acids Research, 40, 4589-4603. https://doi.org/10.1093/nar/gks006 - PubMed
  72. Monroe, R.S., Ostrowski, J., Hryniewicz, M.M. & Kredich, N.M. (1990) In vitro interactions of CysB protein with the cysK and cysJIH promoter regions of Salmonella typhimurium. Journal of Bacteriology, 172, 6919-6929. https://doi.org/10.1128/jb.172.12.6919-6929.1990 - PubMed
  73. Muthuramalingam, M., White, J.C. & Bourne, C.R. (2016) Toxin-antitoxin modules are pliable switches activated by multiple protease pathways. Toxins, 8, 214. https://doi.org/10.3390/toxins8070214 - PubMed
  74. O'Hara, E.B., Chekanova, J.A., Ingle, C.A., Kushner, Z.R., Peters, E. & Kushner, S.R. (1995) Polyadenylylation helps regulate mRNA decay in Escherichia coli. Proceedings of the National Academy of Sciences of the United States of America, 92, 1807-1811. https://doi.org/10.1073/pnas.92.6.1807 - PubMed
  75. Ono, M. & Kuwano, M. (1979) A conditional lethal mutation in an Escherichia coli strain with a longer chemical lifetime of mRNA. Journal of Molecular Biology, 129, 343-357. - PubMed
  76. Ow, M.C. & Kushner, S.R. (2002) Initiation of tRNA maturation by RNase E is essential for cell viability in E. coli. Genes and Development, 16, 1102-1115. https://doi.org/10.1101/gad.983502 - PubMed
  77. Park, O.H., Ha, H., Lee, Y., Boo, S.H., Kwon, D.H., Song, H.K. et al. (2019) Endoribonucleolytic cleavage of m(6)A-containing RNAs by RNase P/MRP complex. Molecular Cell, 74, 494-507.e8. https://doi.org/10.1016/j.molcel.2019.02.034 - PubMed
  78. Peck-Miller, K.A. & Altman, S. (1991) Kinetics of the processing of the precursor to 4.5 S RNA, a naturally occurring substrate for RNase P from Escherichia coli. Journal of Molecular Biology, 221, 1-5. https://doi.org/10.1016/0022-2836(91)80194-Y - PubMed
  79. Peltz, S.W., Donahue, J.L. & Jacobson, A. (1992) A mutation in the tRNA nucleotidyltransferase gene promotes stabilization of mRNAs in Saccharomyces cerevisiae. Molecular and Cellular Biology, 12, 5778-5784. https://doi.org/10.1128/MCB.12.12.5778 - PubMed
  80. Pobre, V. & Arraiano, C.M. (2015) Next generation sequencing analysis reveals that the ribonucleases RNase II, RNase R and PNPase affect bacterial motility and biofilm formation in E. coli. BMC Genomics, 16, 72. https://doi.org/10.1186/s12864-015-1237-6 - PubMed
  81. Reichenbach, B., Maes, A., Kalamorz, F., Hajnsdorf, E. & Gorke, B. (2008) The small RNA GlmY acts upstream of the sRNA GlmZ in the activation of glmS expression and is subject to regulation by polyadenylation in Escherichia coli. Nucleic Acids Research, 36, 2570-2580. https://doi.org/10.1093/nar/gkn091 - PubMed
  82. Reiter, N.J., Osterman, A., Torres-Larios, A., Swinger, K.K., Pan, T. & Mondragon, A. (2010) Structure of a bacterial ribonuclease P holoenzyme in complex with tRNA. Nature, 468, 784-789. https://doi.org/10.1038/nature09516 - PubMed
  83. Richards, J. & Belasco, J.G. (2019) Obstacles to scanning by RNase E govern bacterial mRNA lifetimes by hindering access to distal cleavage sites. Molecular Cell, 74, 284-295.e5. https://doi.org/10.1016/j.molcel.2019.01.044 - PubMed
  84. Salgado, H., Santos-Zavaleta, A., Gama-Castro, S., Millan-Zarate, D., Diaz-Peredo, E., Sanchez-Solano, F. et al. (2001) RegulonDB (version 3.2): transcriptional regulation and operon organization in Escherichia coli K-12. Nucleic Acids Research, 29, 72-74. https://doi.org/10.1093/nar/29.1.72 - PubMed
  85. Schedl, P. & Primakoff, P. (1973) Mutants of Escherichia coli thermosensitive for the synthesis of transfer RNA. Proceedings of the National Academy of Sciences of the United States of America, 70, 2091-2095. https://doi.org/10.1073/pnas.70.7.2091 - PubMed
  86. Stead, M.B., Agarwal, A., Bowden, K.D., Nasir, R., Meagher, R.B., Mohanty, B.K. et al. (2012) RNA snap™: a rapid, quantitative, and inexpensive, method for isolating total RNA from bacteria. Nucleic Acids Research, 40, e156. https://doi.org/10.1093/nar/gks680 - PubMed
  87. Stead, M.B., Marshburn, S., Mohanty, B.K., Mitra, J., Pena Castillo, L., Ray, D. et al. (2011) Analysis of Escherichia coli RNase E and RNase III activity in vivo using tiling microarrays. Nucleic Acids Research, 39, 3188-3203. https://doi.org/10.1093/nar/gkq1242 - PubMed
  88. Suwa, S., Nagai, Y., Fujimoto, A., Kikuchi, Y. & Tanaka, T. (2009) Analysis on substrate specificity of Escherichia coli ribonuclease P using shape variants of pre-tRNA: proposal of subsites model for substrate shape recognition. Journal of Biochemistry, 145, 151-160. https://doi.org/10.1093/jb/mvn150 - PubMed
  89. Vinella, D., Albrecht, C., Cashel, M. & D'Ari, R. (2005) Iron limitation induces SpoT-dependent accumulation of ppGpp in Escherichia coli. Molecular Microbiology, 56, 958-970. https://doi.org/10.1111/j.1365-2958.2005.04601.x - PubMed
  90. Wendrich, T.M., Blaha, G., Wilson, D.N., Marahiel, M.A. & Nierhaus, K.H. (2002) Dissection of the mechanism for the stringent factor RelA. Molecular Cell, 10, 779-788. https://doi.org/10.1016/S1097-2765(02)00656-1 - PubMed
  91. Wu, S., Chen, Y., Lindell, M., Mao, G. & Kirsebom, L.A. (2011) Functional coupling between a distal interaction and the cleavage site in bacterial RNase-P-RNA-mediated cleavage. Journal of Molecular Biology, 411, 384-396. https://doi.org/10.1016/j.jmb.2011.05.049 - PubMed
  92. Xiao, H., Kalman, M., Ikehara, K., Zemel, S., Glaser, G. & Cashel, M. (1991) Residual guanosine 3',5'-bispyrophosphate synthetic activity of relA null mutants can be eliminated by spoT null mutations. Journal of Biological Chemistry, 266, 5980-5990. https://doi.org/10.1016/S0021-9258(19)67694-5 - PubMed
  93. Zhao, J. & Harris, M.E. (2019) Distributive enzyme binding controlled by local RNA context results in 3' to 5' directional processing of dicistronic tRNA precursors by Escherichia coli ribonuclease P. Nucleic Acids Research, 47, 1451-1467. - PubMed

Publication Types

Grant support