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Ribosome collisions induce mRNA cleavage and ribosome rescue in bacteria.

Saito K, Kratzat H, Campbell A, Buschauer R, Burroughs AM, Berninghausen O, Aravind L, Green R, Beckmann R, Buskirk AR
Nature 603 503-508 (2022)
Related entries: 7qg8, 7qgh, 7qgn, 7qgr, 7qgu

Cited: 26 times
EuropePMC logo PMID: 35264790

Abstract

Ribosome rescue pathways recycle stalled ribosomes and target problematic mRNAs and aborted proteins for degradation1,2. In bacteria, it remains unclear how rescue pathways distinguish ribosomes stalled in the middle of a transcript from actively translating ribosomes3-6. Here, using a genetic screen in Escherichia coli, we discovered a new rescue factor that has endonuclease activity. SmrB cleaves mRNAs upstream of stalled ribosomes, allowing the ribosome rescue factor tmRNA (which acts on truncated mRNAs3) to rescue upstream ribosomes. SmrB is recruited to ribosomes and is activated by collisions. Cryo-electron microscopy structures of collided disomes from E. coli and Bacillus subtilis show distinct and conserved arrangements of individual ribosomes and the composite SmrB-binding site. These findings reveal the underlying mechanisms by which ribosome collisions trigger ribosome rescue in bacteria.

Articles - 7qh4 mentioned but not cited (1)

  1. Ribosome collisions induce mRNA cleavage and ribosome rescue in bacteria. Saito K, Kratzat H, Campbell A, Buschauer R, Burroughs AM, Berninghausen O, Aravind L, Green R, Beckmann R, Buskirk AR. Nature 603 503-508 (2022)


Reviews citing this publication (4)

  1. Ribosome-associated quality-control mechanisms from bacteria to humans. Filbeck S, Cerullo F, Pfeffer S, Joazeiro CAP. Mol Cell 82 1451-1466 (2022)
  2. Understanding the Stringent Response: Experimental Context Matters. Dworkin J. mBio 14 e0340422 (2023)
  3. Tailor made: the art of therapeutic mRNA design. Metkar M, Pepin CS, Moore MJ. Nat Rev Drug Discov 23 67-83 (2024)
  4. Co-transcriptional gene regulation in eukaryotes and prokaryotes. Shine M, Gordon J, Schärfen L, Zigackova D, Herzel L, Neugebauer KM. Nat Rev Mol Cell Biol 25 534-554 (2024)

Articles citing this publication (21)

  1. A distinct mammalian disome collision interface harbors K63-linked polyubiquitination of uS10 to trigger hRQT-mediated subunit dissociation. Narita M, Denk T, Matsuo Y, Sugiyama T, Kikuguchi C, Ito S, Sato N, Suzuki T, Hashimoto S, Machová I, Tesina P, Beckmann R, Inada T. Nat Commun 13 6411 (2022)
  2. A trailing ribosome speeds up RNA polymerase at the expense of transcript fidelity via force and allostery. Wee LM, Tong AB, Florez Ariza AJ, Cañari-Chumpitaz C, Grob P, Nogales E, Bustamante CJ. Cell 186 1244-1262.e34 (2023)
  3. The translating bacterial ribosome at 1.55 Å resolution generated by cryo-EM imaging services. Fromm SA, O'Connor KM, Purdy M, Bhatt PR, Loughran G, Atkins JF, Jomaa A, Mattei S. Nat Commun 14 1095 (2023)
  4. Gut colonization by Bacteroides requires translation by an EF-G paralog lacking GTPase activity. Han W, Peng BZ, Wang C, Townsend GE, Barry NA, Peske F, Goodman AL, Liu J, Rodnina MV, Groisman EA. EMBO J 42 e112372 (2023)
  5. Posttranscriptional Regulation by Copper with a New Upstream Open Reading Frame. Roy G, Antoine R, Schwartz A, Slupek S, Rivera-Millot A, Boudvillain M, Jacob-Dubuisson F. mBio 13 e0091222 (2022)
  6. Human mitochondria require mtRF1 for translation termination at non-canonical stop codons. Krüger A, Remes C, Shiriaev DI, Liu Y, Spåhr H, Wibom R, Atanassov I, Nguyen MD, Cooperman BS, Rorbach J. Nat Commun 14 30 (2023)
  7. Atlas of mRNA translation and decay for bacteria. Huch S, Nersisyan L, Ropat M, Barrett D, Wu M, Wang J, Valeriano VD, Vardazaryan N, Huerta-Cepas J, Wei W, Du J, Steinmetz LM, Engstrand L, Pelechano V. Nat Microbiol 8 1123-1136 (2023)
  8. Druggable differences: Targeting mechanistic differences between trans-translation and translation for selective antibiotic action. Srinivas P, Keiler KC, Dunham CM. Bioessays 44 e2200046 (2022)
  9. Learning structural heterogeneity from cryo-electron sub-tomograms with tomoDRGN. Powell BM, Davis JH. Nat Methods (2024)
  10. Visualization of translation reorganization upon persistent ribosome collision stress in mammalian cells. Fedry J, Silva J, Vanevic M, Fronik S, Mechulam Y, Schmitt E, des Georges A, Faller WJ, Förster F. Mol Cell 84 1078-1089.e4 (2024)
  11. arfA antisense RNA regulates MscL excretory activity. Morra R, Pratama F, Butterfield T, Tomazetto G, Young K, Lopez R, Dixon N. Life Sci Alliance 6 e202301954 (2023)
  12. Recognition of an Ala-rich C-degron by the E3 ligase Pirh2. Wang X, Li Y, Yan X, Yang Q, Zhang B, Zhang Y, Yuan X, Jiang C, Chen D, Liu Q, Liu T, Mi W, Yu Y, Dong C. Nat Commun 14 2474 (2023)
  13. Shutdown of multidrug transporter bmrCD mRNA expression mediated by the ribosome-associated endoribonuclease (Rae1) cleavage in a new cryptic ORF. Deves V, Trinquier A, Gilet L, Alharake J, Condon C, Braun F. RNA 29 1108-1116 (2023)
  14. Streptomyces rare codon UUA: from features associated with 2 adpA related locations to candidate phage regulatory translational bypassing. Antonov IV, O'Loughlin S, Gorohovski AN, O'Connor PBF, Baranov PV, Atkins JF. RNA Biol 20 926-942 (2023)
  15. A method to enrich polypeptidyl-tRNAs to capture snapshots of translation in the cell. Yamakawa A, Niwa T, Chadani Y, Kobo A, Taguchi H. Nucleic Acids Res 51 e30 (2023)
  16. B. subtilis MutS2 splits stalled ribosomes into subunits without mRNA cleavage. Park EN, Mackens-Kiani T, Berhane R, Esser H, Erdenebat C, Burroughs AM, Berninghausen O, Aravind L, Beckmann R, Green R, Buskirk AR. EMBO J 43 484-506 (2024)
  17. Riboformer: a deep learning framework for predicting context-dependent translation dynamics. Shao B, Yan J, Zhang J, Liu L, Chen Y, Buskirk AR. Nat Commun 15 2011 (2024)
  18. Ribosome collisions: New ways to initiate ribosome rescue. Leedom SL, Keiler KC. Curr Biol 32 R469-R472 (2022)
  19. Ribosome profiling reveals downregulation of UMP biosynthesis as the major early response to phage infection. O'Connor PBF, Mahony J, Casey E, Baranov PV, van Sinderen D, Yordanova MM. Microbiol Spectr 12 e0398923 (2024)
  20. The Giardia lamblia ribosome structure reveals divergence in several biological pathways and the mode of emetine function. Eiler DR, Wimberly BT, Bilodeau DY, Taliaferro JM, Reigan P, Rissland OS, Kieft JS. Structure 32 400-410.e4 (2024)
  21. Transient disome complex formation in native polysomes during ongoing protein synthesis captured by cryo-EM. Flügel T, Schacherl M, Unbehaun A, Schroeer B, Dabrowski M, Bürger J, Mielke T, Sprink T, Diebolder CA, Guillén Schlippe YV, Spahn CMT. Nat Commun 15 1756 (2024)


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