Bacterial Ribosome Rescue Systems
Abstract
:1. Introduction
2. Trans-Translation
3. RF-Dependent Ribosome Rescue Factors
4. RF Homologue That Acts as a Stop-Codon-Independent RF
5. Ribosome Rescue after the Stalled Ribosome Is Split into Subunits
6. EF-P
7. EF4 (LepA)
8. Arrest Sequences on mRNA
9. Recognition of Stalled Ribosome by Rescue Factors
10. mRNA Cleavage on the Ribosome
11. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Himeno, H.; Kurita, D.; Muto, A. tmRNA-mediated trans-translation as the major ribosome rescue system in a bacterial cell. Front. Genet. 2014, 5, 66. [Google Scholar] [CrossRef] [Green Version]
- Himeno, H.; Kurita, D.; Muto, A. Mechanism of trans-translation revealed by in vitro studies. Front. Microbiol. 2014, 5, 65. [Google Scholar] [CrossRef]
- Komine, Y.; Kitabatake, M.; Yokogawa, T.; Nishikawa, K.; Inokuchi, H. A tRNA-like structure is present in 10Sa RNA, a small stable RNA from Escherichia coli. Proc. Natl. Acad. Sci. USA 1994, 91, 9223–9227. [Google Scholar] [CrossRef] [Green Version]
- Ushida, C.; Himeno, H.; Watanabe, T.; Muto, A. tRNA-like structures in 10Sa RNAs of Mycoplasma capricolum and Bacillus subtilis. Nucleic Acids Res. 1994, 22, 3392–3396. [Google Scholar] [CrossRef] [Green Version]
- Keiler, K.C.; Waller, P.R.; Sauer, R.T. Role of a peptide tagging system in degradation of proteins synthesized from damaged messenger RNA. Science 1996, 271, 990–993. [Google Scholar] [CrossRef] [Green Version]
- Karzai, A.W.; Susskind, M.M.; Sauer, R.T. SmpB, a unique RNA-binding protein essential for the peptide-tagging activity of SsrA (tmRNA). EMBO J. 1999, 18, 3793–3799. [Google Scholar] [CrossRef] [Green Version]
- Gutmann, S.; Haebel, P.W.; Metzinger, L.; Sutter, M.; Felden, B.; Ban, N. Crystal structure of the transfer-RNA domain of transfer-messenger RNA in complex with SmpB. Nature 2003, 424, 699–703. [Google Scholar] [CrossRef]
- Bessho, Y.; Shibata, R.; Sekine, S.; Murayama, K.; Higashijima, K.; Hori-Takemoto, C.; Shirouzu, M.; Kuramitsu, S.; Yokoyama, S. Structural basis for functional mimicry of long-variable-arm tRNA by transfer-messenger RNA. Proc. Natl. Acad. Sci. USA 2007, 104, 8293–8298. [Google Scholar] [CrossRef] [Green Version]
- Kurita, D.; Sasaki, R.; Muto, A.; Himeno, H. Interaction of SmpB with ribosome from directed hydroxyl radical probing. Nucleic Acids Res. 2007, 35, 7248–7255. [Google Scholar] [CrossRef] [Green Version]
- Neubauer, C.; Gillet, R.; Kelley, A.C.; Ramakrishnan, V. Decoding in the absence of a codon by tmRNA and SmpB in the ribosome. Science 2012, 335, 1366–1369. [Google Scholar] [CrossRef] [Green Version]
- Gottesman, S.; Roche, E.; Zhou, Y.; Sauer, R.T. The ClpXP and ClpAP proteases degrade proteins with carboxy-terminal peptide tails added by the SsrA-tagging system. Genes Dev. 1998, 12, 1338–1347. [Google Scholar] [CrossRef]
- Campos-Silva, R.; D’Urso, G.; Delalande, O.; Giudice, E.; Macedo, A.J.; Gillet, R. Trans-translation is an appealing target for the development of new antimicrobial compounds. Microorganisms 2022, 10, 3. [Google Scholar] [CrossRef]
- Yamamoto, Y.; Sunohara, T.; Jojima, K.; Inada, T.; Aiba, H. SsrA-mediated trans-translation plays a role in mRNA quality control by facilitating degradation of truncated mRNAs. RNA 2003, 9, 408–418. [Google Scholar] [CrossRef] [Green Version]
- Oussenko, I.A.; Abe, T.; Ujiie, H.; Muto, A.; Bechhofer, D.H. Participation of 3′-to-5′ exoribonucleases in the turnover of Bacillus subtilis mRNA. J. Bacteriol. 2005, 187, 2758–2767. [Google Scholar] [CrossRef] [Green Version]
- Richards, J.; Mehta, P.; Karzai, A.W. RNase R degrades non-stop mRNAs selectively in an SmpB-tmRNA-dependent manner. Mol. Microbiol. 2006, 62, 1700–1712. [Google Scholar] [CrossRef]
- Mehta, P.; Richards, J.; Karzai, A.W. tmRNA determinants required for facilitating nonstop mRNA decay. RNA 2006, 12, 2187–2198. [Google Scholar] [CrossRef] [Green Version]
- Liang, W.; Deutscher, M.P. A novel mechanism for ribonuclease regulation: Transfer-messenger RNA (tmRNA) and its associated protein SmpB regulate the stability of RNase R. J. Biol. Chem. 2010, 285, 29054–29058. [Google Scholar] [CrossRef] [Green Version]
- Ge, Z.; Mehta, P.; Richards, J.; Karzai, A.W. Non-stop mRNA decay initiates at the ribosome. Mol. Microbiol. 2010, 78, 1159–1170. [Google Scholar] [CrossRef] [Green Version]
- Liang, W.; Malhotra, A.; Deutscher, M.P. Acetylation regulates the stability of a bacterial protein: Growth stage-dependent modification of RNase R. Mol. Cell. 2011, 44, 160–166. [Google Scholar] [CrossRef] [Green Version]
- Rae, C.D.; Gordiyenko, Y.; Ramakrishnan, V. How a circularized tmRNA moves through the ribosome. Science 2019, 363, 740–744. [Google Scholar] [CrossRef]
- Guyomar, C.; D’Urso, G.; Chat, S.; Giudice, E.; Gillet, R. Structures of tmRNA and SmpB as they transit through the ribosome. Nat. Commun. 2021, 12, 4909. [Google Scholar] [CrossRef]
- Wimberly, B.T.; Brodersen, D.E.; Clemons, W.M., Jr.; Morgan-Warren, R.J.; Carter, A.P.; Vonrhein, C.; Hartsch, T.; Ramakrishnan, V. Structure of the 30S ribosomal subunit. Nature 2000, 407, 327–339. [Google Scholar] [CrossRef]
- Carter, A.P.; Clemons, W.M., Jr.; Brodersen, D.E.; Morgan-Warren, R.J.; Hartsch, T.; Wimberly, B.T.; Ramakrishnan, V. Crystal structure of an initiation factor bound to the 30S ribosomal subunit. Science 2001, 291, 498–501. [Google Scholar] [CrossRef] [Green Version]
- Noeske, J.; Wasserman, M.R.; Terry, D.S.; Altman, R.B.; Blanchard, S.C.; Cate, J.H.D. High-resolution structure of the Escherichia coli ribosome. Nat. Struct. Mol. Biol. 2015, 22, 336–341. [Google Scholar] [CrossRef]
- Watson, Z.L.; Ward, F.R.; Méheust, R.; Ad, O.; Schepartz, A.; Banfield, J.F.; Cate, J.H.D. Structure of the bacterial ribosome at 2 Å resolution. Elife 2020, 9, e60482. [Google Scholar] [CrossRef]
- Lee, S.; Ishii, M.; Tadaki, T.; Muto, A.; Himeno, H. Determinants on tmRNA for initiating efficient and precise trans-translation: Some mutations upstream of the tag-encoding sequence of Escherichia coli tmRNA shift the initiation point of trans-translation in vitro. RNA 2001, 7, 999–1012. [Google Scholar] [CrossRef] [Green Version]
- Withey, J.; Friedman, D. Analysis of the role of trans-translation in the requirement of tmRNA for lambdaimmP22 growth in Escherichia coli. J. Bacteriol. 1999, 181, 2148–2157. [Google Scholar] [CrossRef] [Green Version]
- Muto, A.; Fujihara, A.; Ito, K.; Matsuno, J.; Ushida, C.; Himeno, H. Requirement of transfer-messenger RNA for the growth of Bacillus subtilis under stresses. Genes Cells 2000, 5, 627–635. [Google Scholar] [CrossRef]
- Julio, S.M.; Heithoff, D.M.; Mahan, M.J. ssrA (tmRNA) plays a role in Salmonella enterica serovar Typhimurium pathogenesis. J. Bacteriol. 2000, 182, 1558–1563. [Google Scholar] [CrossRef] [Green Version]
- Keiler, K.C.; Shapiro, L. TmRNA is required for correct timing of DNA replication in Caulobacter crescentus. J. Bacteriol. 2003, 185, 573–580. [Google Scholar]
- Chadani, Y.; Ono, K.; Ozawa, S.; Takahashi, Y.; Takai, K.; Nanamiya, H.; Tozawa, Y.; Kutsukake, K.; Abo, T. Ribosome rescue by Escherichia coli ArfA (YhdL) in the absence of trans-translation system. Mol. Microbiol. 2010, 78, 796–808. [Google Scholar] [CrossRef] [PubMed]
- Chadani, Y.; Ito, K.; Kutsukake, K.; Abo, T. ArfA recruits release factor 2 to rescue stalled ribosomes by peptidyl-tRNA hydrolysis in Escherichia coli. Mol. Microbiol. 2012, 86, 37–50. [Google Scholar] [CrossRef] [PubMed]
- Shimizu, Y. ArfA recruits RF2 into stalled ribosomes. J. Mol. Biol. 2012, 423, 624–631. [Google Scholar] [CrossRef]
- Kurita, D.; Chadani, Y.; Muto, A.; Abo, T.; Himeno, H. ArfA recognizes the lack of mRNA in the mRNA channel after RF2 binding for ribosome rescue. Nucleic Acids Res. 2014, 42, 13339–13352. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chadani, Y.; Matsumoto, E.; Aso, H.; Wada, T.; Kutsukake, K.; Sutou, S.; Abo, T. trans-translation-mediated tight regulation of the expression of the alternative ribosome-rescue factor ArfA in Escherichia coli. Genes Genet. Syst. 2011, 86, 151–163. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Schaub, R.E.; Poole, S.J.; Garza-Sánchez, F.; Benbow, S.; Hayes, C.S. Proteobacterial ArfA peptides are synthesized from non-stop messenger RNAs. J. Biol. Chem. 2012, 287, 29765–29775. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Goralski, T.D.P.; Kirimanjeswara, G.S.; Keiler, K.C. A New Mechanism for Ribosome Rescue Can Recruit RF1 or RF2 to Nonstop Ribosomes. mBio 2018, 9, e02436-18. [Google Scholar] [CrossRef] [Green Version]
- Shimokawa-Chiba, N.; Müller, C.; Fujiwara, K.; Beckert, B.; Ito, K.; Wilson, D.N.; Chiba, S. Release factor-dependent ribosome rescue by BrfA in the Gram-positive bacterium Bacillus subtilis. Nat. Commun. 2019, 10, 5397. [Google Scholar] [CrossRef]
- Laurberg, M.; Asahara, H.; Korostelev, A.; Zhu, J.; Trakhanov, S.; Noller, H.F. Structural basis for translation termination on the 70S ribosome. Nature 2008, 454, 852–857. [Google Scholar] [CrossRef]
- Korostelev, A.; Asahara, H.; Lancaster, L.; Laurberg, M.; Hirschi, A.; Zhu, J.; Trakhanov, S.; Scott, W.G.; Noller, H.F. Crystal structure of a translation termination complex formed with release factor RF2. Proc. Natl. Acad. Sci. USA 2008, 105, 19684–19689. [Google Scholar] [CrossRef] [Green Version]
- Weixlbaumer, A.; Jin, H.; Neubauer, C.; Voorhees, R.M.; Petry, S.; Kelley, A.C.; Ramakrishnan, V. Insights into translational termination from the structure of RF2 bound to the ribosome. Science 2008, 322, 953–956. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Korostelev, A.; Zhu, J.; Asahara, H.; Noller, H.F. Recognition of the amber UAG stop codon by release factor RF1. EMBO J. 2010, 29, 2577–2585. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- James, N.R.; Brown, A.; Gordiyenko, Y.; Ramakrishnan, V. Translational termination without a stop codon. Science 2016, 354, 1437–1440. [Google Scholar] [CrossRef] [Green Version]
- Ma, C.; Kurita, D.; Li, N.; Chen, Y.; Himeno, H.; Gao, N. Mechanistic insights into the alternative translation termination by ArfA and RF2. Nature 2017, 541, 550–553. [Google Scholar] [CrossRef] [PubMed]
- Huter, P.; Müller, C.; Beckert, B.; Arenz, S.; Berninghausen, O.; Beckmann, R.; Wilson, D.N. Structural basis for ArfA-RF2-mediated translation termination on mRNAs lacking stop codons. Nature 2017, 541, 546–549. [Google Scholar] [CrossRef] [PubMed]
- Zeng, F.; Chen, Y.; Remis, J.; Shekhar, M.; Phillips, J.C.; Tajkhorshid, E.; Jin, H. Structural basis of co-translational quality control by ArfA and RF2 bound to ribosome. Nature 2017, 541, 554–557. [Google Scholar] [CrossRef] [PubMed]
- Demo, G.; Svidritskiy, E.; Madireddy, R.; Diaz-Avalos, R.; Grant, T.; Grigorieff, N.; Sousa, D.; Korostelev, A.A. Mechanism of ribosome rescue by ArfA and RF2. Elife 2017, 6, e23687. [Google Scholar] [CrossRef] [Green Version]
- Van der Stel, A.X.; Gordon, E.R.; Sengupta, A.; Martínez, A.K.; Klepacki, D.; Perry, T.N.; Herrero Del Valle, A.; Vázquez-Laslop, N.; Sachs, M.S.; Cruz-Vera, L.R.; et al. Structural basis for the tryptophan sensitivity of TnaC-mediated ribosome stalling. Nat. Commun. 2021, 12, 5340. [Google Scholar] [CrossRef]
- Pape, T.; Wintermeyer, W.; Rodnina, M. Induced fit in initial selection and proofreading of aminoacyl-tRNA on the ribosome. EMBO J. 1999, 18, 3800–3807. [Google Scholar] [CrossRef] [Green Version]
- Gromadski, K.B.; Rodnina, M.V. Kinetic determinants of high-fidelity tRNA discrimination on the ribosome. Mol. Cell 2004, 13, 191–200. [Google Scholar] [CrossRef] [Green Version]
- Zaher, H.S.; Green, R. Quality control by the ribosome following peptide bond formation. Nature 2009, 457, 161–166. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Handa, Y.; Inaho, N.; Nameki, N. YaeJ is a novel ribosome-associated protein in Escherichia coli that can hydrolyze peptidyl-tRNA on stalled ribosomes. Nucleic Acids Res. 2011, 39, 1739–1748. [Google Scholar] [CrossRef] [PubMed]
- Chadani, Y.; Ono, K.; Kutsukake, K.; Abo, T. Escherichia coli YaeJ protein mediates a novel ribosome-rescue pathway distinct from SsrA- and ArfA-mediated pathways. Mol. Microbiol. 2011, 80, 772–785. [Google Scholar] [CrossRef] [PubMed]
- Richter, R.; Rorbach, J.; Pajak, A.; Smith, P.M.; Wessels, H.J.; Huynen, M.A.; Smeitink, J.A.; Lightowlers, R.N.; Chrzanowska-Lightowlers, Z.M. A functional peptidyl-tRNA hydrolase, ICT1, has been recruited into the human mitochondrial ribosome. EMBO J. 2010, 29, 1116–1125. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Antonicka, H.; Ostergaard, E.; Sasarman, F.; Weraarpachai, W.; Wibrand, F.; Pedersen, A.M.; Rodenburg, R.J.; van der Knaap, M.S.; Smeitink, J.A.; Chrzanowska-Lightowlers, Z.M.; et al. Mutations in C12orf65 in patients with encephalomyopathy and a mitochondrial translation defect. Am. J. Hum. Genet. 2010, 87, 115–122. [Google Scholar] [CrossRef] [Green Version]
- Chan, K.H.; Petrychenko, V.; Mueller, C.; Maracci, C.; Holtkamp, W.; Wilson, D.N.; Fischer, N.; Rodnina, M.V. Mechanism of ribosome rescue by alternative ribosome-rescue factor B. Nat. Commun. 2020, 11, 4106. [Google Scholar] [CrossRef]
- Gagnon, M.G.; Seetharaman, S.V.; Bulkley, D.; Steitz, T.A. Structural basis for the rescue of stalled ribosomes: Structure of YaeJ bound to the ribosome. Science 2012, 335, 1370–1372. [Google Scholar] [CrossRef] [Green Version]
- Carbone, C.E.; Demo, G.; Madireddy, R.; Svidritskiy, E.; Korostelev, A.A. ArfB can displace mRNA to rescue stalled ribosomes. Nat. Commun. 2020, 11, 5552. [Google Scholar] [CrossRef]
- Yonashiro, R.; Tahara, E.B.; Bengtson, M.H.; Khokhrina, M.; Lorenz, H.; Chen, K.C.; Kigoshi-Tansho, Y.; Savas, J.N.; Yates, J.R.; Kay, S.A.; et al. The Rqc2/Tae2 subunit of the ribosome-associated quality control (RQC) complex marks ribosome-stalled nascent polypeptide chains for aggregation. Elife 2016, 5, e11794. [Google Scholar] [CrossRef]
- Lytvynenko, I.; Paternoga, H.; Thrun, A.; Balke, A.; Müller, T.A.; Chiang, C.H.; Nagler, K.; Tsaprailis, G.; Anders, S.; Bischofs, I.; et al. Alanine Tails Signal Proteolysis in Bacterial Ribosome-Associated Quality Control. Cell 2019, 178, 76–90.e22. [Google Scholar] [CrossRef]
- Crowe-McAuliffe, C.; Takada, H.; Murina, V.; Polte, C.; Kasvandik, S.; Tenson, T.; Ignatova, Z.; Atkinson, G.C.; Wilson, D.N.; Hauryliuk, V. Structural Basis for Bacterial Ribosome-Associated Quality Control by RqcH and RqcP. Mol. Cell 2021, 81, 115–126.e7. [Google Scholar] [CrossRef] [PubMed]
- Filbeck, S.; Cerullo, F.; Paternoga, H.; Tsaprailis, G.; Joazeiro, C.A.P.; Pfeffer, S. Mimicry of Canonical Translation Elongation Underlies Alanine Tail Synthesis in RQC. Mol. Cell 2021, 81, 104–114.e6. [Google Scholar] [CrossRef] [PubMed]
- Zhang, Y.; Mandava, C.S.; Cao, W.; Li, X.; Zhang, D.; Li, N.; Zhang, Y.; Zhang, X.; Qin, Y.; Mi, K.; et al. HflX is a ribosome-splitting factor rescuing stalled ribosomes under stress conditions. Nat. Struct. Mol. Biol. 2015, 22, 906–913. [Google Scholar] [CrossRef] [PubMed]
- Richmond, C.S.; Glasner, J.D.; Mau, R.; Jin, H.; Blattner, F.R. Genome-wide expression profiling in Escherichia coli K-12. Nucleic Acids Res. 1999, 27, 3821–3835. [Google Scholar] [CrossRef]
- Desai, N.; Yang, H.; Chandrasekaran, V.; Kazi, R.; Minczuk, M.; Ramakrishnan, V. Elongational stalling activates mitoribosome-associated quality control. Science 2020, 370, 1105–1110. [Google Scholar] [CrossRef]
- Glick, B.R.; Ganoza, M.C. Identification of a soluble protein that stimulates peptide bond synthesis. Proc. Natl. Acad. Sci. USA 1975, 72, 4257–4260. [Google Scholar] [CrossRef] [Green Version]
- Zou, S.B.; Roy, H.; Ibba, M.; Navarre, W.W. Elongation factor P mediates a novel post-transcriptional regulatory pathway critical for bacterial virulence. Virulence 2011, 2, 147–151. [Google Scholar] [CrossRef] [Green Version]
- Zou, S.B.; Hersch, S.J.; Roy, H.; Wiggers, J.B.; Leung, A.S.; Buranyi, S.; Xie, J.L.; Dare, K.; Ibba, M.; Navarre, W.W. Loss of elongation factor P disrupts bacterial outer membrane integrity. J. Bacteriol. 2012, 194, 413–425. [Google Scholar] [CrossRef] [Green Version]
- Doerfel, L.K.; Wohlgemuth, I.; Kothe, C.; Peske, F.; Urlaub, H.; Rodnina, M.V. EF-P is essential for rapid synthesis of proteins containing consecutive proline residues. Science 2013, 339, 85–88. [Google Scholar] [CrossRef] [Green Version]
- Ude, S.; Lassak, J.; Starosta, A.L.; Kraxenberger, T.; Wilson, D.N.; Jung, K. Translation elongation factor EF-P alleviates ribosome stalling at polyproline stretches. Science 2013, 339, 82–85. [Google Scholar] [CrossRef]
- Wohlgemuth, I.; Brenner, S.; Beringer, M.; Rodnina, M.V. Modulation of the rate of peptidyl transfer on the ribosome by the nature of substrates. J. Biol. Chem. 2008, 283, 32229–32235. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dibb, N.J.; Wolfe, P.B. lep operon proximal gene is not required for growth or secretion by Escherichia coli. J. Bacteriol. 1986, 166, 83–87. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pech, M.; Karim, Z.; Yamamoto, H.; Kitakawa, M.; Qin, Y.; Nierhaus, K.H. Elongation factor 4 (EF4/LepA) accelerates protein synthesis at increased Mg2+ concentrations. Proc. Natl. Acad. Sci. USA 2011, 108, 3199–3203. [Google Scholar] [CrossRef] [Green Version]
- Qin, Y.; Polacek, N.; Vesper, O.; Staub, E.; Einfeldt, E.; Wilson, D.N.; Nierhaus, K.H. The highly conserved LepA is a ribosomal elongation factor that back-translocates the ribosome. Cell 2006, 127, 721–733. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gagnon, M.G.; Lin, J.; Steitz, T.A. Elongation factor 4 remodels the A-site tRNA on the ribosome. Proc. Natl. Acad. Sci. USA 2016, 113, 4994–4999. [Google Scholar] [CrossRef] [Green Version]
- Liu, H.; Chen, C.; Zhang, H.; Kaur, J.; Goldman, Y.E.; Cooperman, B.S. The conserved protein EF4 (LepA) modulates the elongation cycle of protein synthesis. Proc. Natl. Acad. Sci. USA 2011, 108, 16223–16228. [Google Scholar] [CrossRef] [Green Version]
- Gagnon, M.G.; Lin, J.; Bulkley, D.; Steitz, T.A. Crystal structure of elongation factor 4 bound to a clockwise ratcheted ribosome. Science 2014, 345, 684–687. [Google Scholar] [CrossRef]
- Nakatogawa, H.; Ito, K. The ribosomal exit tunnel functions as a discriminating gate. Cell 2002, 108, 629–636. [Google Scholar] [CrossRef] [Green Version]
- Gong, F.; Yanofsky, C. Instruction of translating ribosome by nascent peptide. Science 2002, 297, 1864–1867. [Google Scholar] [CrossRef]
- Chiba, S.; Lamsa, A.; Pogliano, K. A ribosome-nascent chain sensor of membrane protein biogenesis in Bacillus subtilis. EMBO J. 2009, 28, 3461–3475. [Google Scholar] [CrossRef] [Green Version]
- Ingolia, N.T.; Ghaemmaghami, S.; Newman, J.R.; Weissman, J.S. Genome-wide analysis in vivo of translation with nucleotide resolution using ribosome profiling. Science 2009, 324, 218–223. [Google Scholar] [CrossRef] [Green Version]
- Ingolia, N.T.; Lareau, L.F.; Weissman, J.S. Ribosome profiling of mouse embryonic stem cells reveals the complexity and dynamics of mammalian proteomes. Cell 2011, 147, 789–802. [Google Scholar] [CrossRef] [Green Version]
- Li, G.W.; Oh, E.; Weissman, J.S. The anti-Shine-Dalgarno sequence drives translational pausing and codon choice in bacteria. Nature 2012, 484, 538–541. [Google Scholar] [CrossRef]
- Borg, A.; Ehrenberg, M. Determinants of the rate of mRNA translocation in bacterial protein synthesis. J. Mol. Biol. 2015, 427, 1835–1847. [Google Scholar] [CrossRef]
- Mohammad, F.; Woolstenhulme, C.J.; Green, R.; Buskirk, A.R. Clarifying the Translational Pausing Landscape in Bacteria by Ribosome Profiling. Cell Rep. 2016, 14, 686–694. [Google Scholar] [CrossRef] [Green Version]
- Mohammad, F.; Green, R.; Buskirk, A.R. A systematically-revised ribosome profiling method for bacteria reveals pauses at single-codon resolution. Elife 2019, 8, e42591. [Google Scholar] [CrossRef]
- Chadani, Y.; Niwa, T.; Chiba, S.; Taguchi, H.; Ito, K. Integrated in vivo and in vitro nascent chain profiling reveals widespread translational pausing. Proc. Natl. Acad. Sci. USA 2016, 113, E829–E838. [Google Scholar] [CrossRef] [Green Version]
- Ivanova, N.; Pavlov, M.Y.; Felden, B.; Ehrenberg, M. Ribosome rescue by tmRNA requires truncated mRNAs. J. Mol. Biol. 2004, 338, 33–41. [Google Scholar] [CrossRef]
- Asano, K.; Kurita, D.; Takada, K.; Konno, T.; Muto, A.; Himeno, H. Competition between trans-translation and termination or elongation of translation. Nucleic Acids Res. 2005, 33, 5544–5552. [Google Scholar] [CrossRef] [Green Version]
- Kurita, D.; Miller, M.R.; Muto, A.; Buskirk, A.R.; Himeno, H. Rejection of tmRNA·SmpB after GTP hydrolysis by EF-Tu on ribosomes stalled on intact mRNA. RNA 2014, 20, 1706–1714. [Google Scholar] [CrossRef] [Green Version]
- Ramrath, D.J.F.; Yamamoto, H.; Rother, K.; Wittek, D.; Pech, M.; Mielke, T.; Loerke, J.; Scheerer, P.; Ivanov, P.; Teraoka, Y.; et al. The complex of tmRNA-SmpB and EF-G on translocating ribosomes. Nature 2012, 485, 526–529. [Google Scholar] [CrossRef]
- Hussain, T.; Llácer, J.L.; Wimberly, B.T.; Kieft, J.S.; Ramakrishnan, V. Large-Scale Movements of IF3 and tRNA during Bacterial Translation Initiation. Cell 2016, 167, 133–144.e13. [Google Scholar] [CrossRef] [Green Version]
- Hilal, T.; Yamamoto, H.; Loerke, J.; Bürger, J.; Mielke, T.; Spahn, C.M.T. Structural insights into ribosomal rescue by Dom34 and Hbs1 at near-atomic resolution. Nat. Commun. 2016, 7, 13521. [Google Scholar] [CrossRef] [Green Version]
- Ben-Shem, A.; Garreau de Loubresse, N.; Melnikov, S.; Jenner, L.; Yusupova, G.; Yusupov, M. The structure of the eukaryotic ribosome at 3.0 A resolution. Science 2011, 334, 1524–1529. [Google Scholar] [CrossRef] [Green Version]
- Schubert, K.; Karousis, E.D.; Jomaa, A.; Scaiola, A.; Echeverria, B.; Gurzeler, L.A.; Leibundgut, M.; Thiel, V.; Mühlemann, O.; Ban, N. SARS-CoV-2 Nsp1 binds the ribosomal mRNA channel to inhibit translation. Nat. Struct. Mol. Biol. 2020, 27, 959–966. [Google Scholar] [CrossRef]
- Thoms, M.; Buschauer, R.; Ameismeier, M.; Koepke, L.; Denk, T.; Hirschenberger, M.; Kratzat, H.; Hayn, M.; Mackens-Kiani, T.; Cheng, J.; et al. Structural basis for translational shutdown and immune evasion by the Nsp1 protein of SARS-CoV-2. Science 2020, 369, 1249–1255. [Google Scholar] [CrossRef]
- Yuan, S.; Peng, L.; Park, J.J.; Hu, Y.; Devarkar, S.C.; Dong, M.B.; Shen, Q.; Wu, S.; Chen, S.; Lomakin, I.B.; et al. Nonstructural Protein 1 of SARS-CoV-2 Is a Potent Pathogenicity Factor Redirecting Host Protein Synthesis Machinery toward Viral RNA. Mol. Cell. 2020, 80, 1055–1066.e6. [Google Scholar] [CrossRef]
- Kamada, K.; Hanaoka, F. Conformational change in the catalytic site of the ribonuclease YoeB toxin by YefM antitoxin. Mol. Cell. 2005, 19, 497–509. [Google Scholar] [CrossRef]
- Neubauer, C.; Gao, Y.G.; Andersen, K.R.; Dunham, C.M.; Kelley, A.C.; Hentschel, J.; Gerdes, K.; Ramakrishnan, V.; Brodersen, D.E. The structural basis for mRNA recognition and cleavage by the ribosome-dependent endonuclease RelE. Cell 2009, 139, 1084–1095. [Google Scholar] [CrossRef] [Green Version]
- Ruangprasert, A.; Maehigashi, T.; Miles, S.J.; Giridharan, N.; Liu, J.X.; Dunham, C.M. Mechanisms of toxin inhibition and transcriptional repression by Escherichia coli DinJ-YafQ. J. Biol. Chem. 2014, 289, 20559–20569. [Google Scholar] [CrossRef] [Green Version]
- Schureck, M.A.; Maehigashi, T.; Miles, S.J.; Marquez, J.; Cho, S.E.; Erdman, R.; Dunham, C.M. Structure of the Proteus vulgaris HigB-(HigA)2-HigB toxin-antitoxin complex. J. Biol. Chem. 2014, 289, 1060–1070. [Google Scholar] [CrossRef] [Green Version]
- Zeng, F.; Jin, H. Peptide release promoted by methylated RF2 and ArfA in nonstop translation is achieved by an induced-fit mechanism. RNA 2016, 22, 49–60. [Google Scholar] [CrossRef] [Green Version]
- D’Orazio, K.N.; Wu, C.C.; Sinha, N.; Loll-Krippleber, R.; Brown, G.W.; Green, R. The endonuclease Cue2 cleaves mRNAs at stalled ribosomes during No Go Decay. Elife 2019, 8, e49117. [Google Scholar] [CrossRef]
- Saito, K.; Kratzat, H.; Campbell, A.; Buschauer, R.; Burroughs, A.M.; Berninghausen, O.; Aravind, L.; Beckmann, R.; Green, R.; Buskirk, A.R. Ribosome collisions in bacteria promote ribosome rescue by triggering mRNA cleavage by SmrB. bioRxiv 2021, 456513. [Google Scholar]
- Burroughs, A.M.; Aravind, L. The origin and evolution of release factors: Implications for translation termination, ribosome rescue, and quality control pathways. Int. J. Mol. Sci. 2019, 20, 1981. [Google Scholar] [CrossRef] [Green Version]
Protein | Domain | pI |
---|---|---|
Escherichia coli MG1655 SmpB | N-terminal domain (1–130) | 9.58 |
C-terminal tail (131–160) | 10.37 | |
Escherichia coli MG1655 ArfA | N-terminal region (1–25) | 6.70 |
C-terminal region (26–55) | 11.13 | |
Escherichia coli MG1655 ArfB | N-terminal domain (1–100) | 8.16 |
C-terminal tail (101–160) | 12.11 | |
Escherichia coli MG1655 RF2 | Domain I (1–106) | 4.02 |
Domain II (107–208) | 4.79 | |
Domain III (209–300) | 6.38 | |
Domain IV (301–360) | 5.24 | |
Escherichia coli MG1655 EF-G | Domain I (7–279) | 5.08 |
Domain II (280–405) | 4.58 | |
Domain III (408–484) | 4.77 | |
Domain IV (485–609) | 8.75 | |
Domain V (610–699) | 4.94 | |
Saccharomyces cerevisiae Stm1 | Domain I (1–153) | 9.07 |
Domain II (154–218) | 6.48 | |
Domain III (219–273) | 12.23 | |
SARS-CoV-2 Nsp1 | N-terminal domain (1–127) | 5.94 |
C-terminal domain (128–180) | 4.63 |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Kurita, D.; Himeno, H. Bacterial Ribosome Rescue Systems. Microorganisms 2022, 10, 372. https://doi.org/10.3390/microorganisms10020372
Kurita D, Himeno H. Bacterial Ribosome Rescue Systems. Microorganisms. 2022; 10(2):372. https://doi.org/10.3390/microorganisms10020372
Chicago/Turabian StyleKurita, Daisuke, and Hyouta Himeno. 2022. "Bacterial Ribosome Rescue Systems" Microorganisms 10, no. 2: 372. https://doi.org/10.3390/microorganisms10020372
APA StyleKurita, D., & Himeno, H. (2022). Bacterial Ribosome Rescue Systems. Microorganisms, 10(2), 372. https://doi.org/10.3390/microorganisms10020372