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tmRNA-SmpB: a journey to the centre of the bacterial ribosome.

Weis F, Bron P, Giudice E, Rolland JP, Thomas D, Felden B, Gillet R
EMBO J 29 3810-8 (2010)
Cited: 38 times
EuropePMC logo PMID: 20953161

Abstract

Ribosomes mediate protein synthesis by decoding the information carried by messenger RNAs (mRNAs) and catalysing peptide bond formation between amino acids. When bacterial ribosomes stall on incomplete messages, the trans-translation quality control mechanism is activated by the transfer-messenger RNA bound to small protein B (tmRNA-SmpB ribonucleoprotein complex). Trans-translation liberates the stalled ribosomes and triggers degradation of the incomplete proteins. Here, we present the cryo-electron microscopy structures of tmRNA-SmpB accommodated or translocated into stalled ribosomes. Two atomic models for each state are proposed. This study reveals how tmRNA-SmpB crosses the ribosome and how, as the problematic mRNA is ejected, the tmRNA resume codon is placed onto the ribosomal decoding site by new contacts between SmpB and the nucleotides upstream of the tag-encoding sequence. This provides a structural basis for the transit of the large tmRNA-SmpB complex through the ribosome and for the means by which the tmRNA internal frame is set for translation to resume.

Reviews - 3iyq mentioned but not cited (2)

  1. Trans-translation exposed: understanding the structures and functions of tmRNA-SmpB. Giudice E, Macé K, Gillet R. Front Microbiol 5 113 (2014)
  2. The World of Stable Ribonucleoproteins and Its Mapping With Grad-Seq and Related Approaches. Gerovac M, Vogel J, Smirnov A. Front Mol Biosci 8 661448 (2021)

Articles - 3iyq mentioned but not cited (2)

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Reviews citing this publication (15)

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  6. tmRNA-mediated trans-translation as the major ribosome rescue system in a bacterial cell. Himeno H, Kurita D, Muto A. Front Genet 5 66 (2014)
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  13. The SmpB C-terminal tail helps tmRNA to recognize and enter stalled ribosomes. Miller MR, Buskirk AR. Front Microbiol 5 462 (2014)
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  15. Mechanism of trans-translation revealed by in vitro studies. Himeno H, Kurita D, Muto A. Front Microbiol 5 65 (2014)

Articles citing this publication (19)

  1. Decoding in the absence of a codon by tmRNA and SmpB in the ribosome. Neubauer C, Gillet R, Kelley AC, Ramakrishnan V. Science 335 1366-1369 (2012)
  2. The complex of tmRNA-SmpB and EF-G on translocating ribosomes. Ramrath DJ, Yamamoto H, Rother K, Wittek D, Pech M, Mielke T, Loerke J, Scheerer P, Ivanov P, Teraoka Y, Shpanchenko O, Nierhaus KH, Spahn CM. Nature 485 526-529 (2012)
  3. Nascentome analysis uncovers futile protein synthesis in Escherichia coli. Ito K, Chadani Y, Nakamori K, Chiba S, Akiyama Y, Abo T. PLoS ONE 6 e28413 (2011)
  4. Cryo-electron microscopy modeling by the molecular dynamics flexible fitting method. Chan KY, Trabuco LG, Schreiner E, Schulten K. Biopolymers 97 678-686 (2012)
  5. The role of SmpB and the ribosomal decoding center in licensing tmRNA entry into stalled ribosomes. Miller MR, Liu Z, Cazier DJ, Gebhard GM, Herron SR, Zaher HS, Green R, Buskirk AR. RNA 17 1727-1736 (2011)
  6. Structural basis for ArfA-RF2-mediated translation termination on mRNAs lacking stop codons. Huter P, Müller C, Beckert B, Arenz S, Berninghausen O, Beckmann R, Wilson DN. Nature 541 546-549 (2017)
  7. Escherichia coli NusG Links the Lead Ribosome with the Transcription Elongation Complex. Washburn RS, Zuber PK, Sun M, Hashem Y, Shen B, Li W, Harvey S, Acosta Reyes FJ, Gottesman ME, Knauer SH, Frank J. iScience 23 101352 (2020)
  8. Visualizing compaction of polysomes in bacteria. Cougot N, Molza AE, Delesques J, Giudice E, Cavalier A, Rolland JP, Ermel G, Blanco C, Thomas D, Gillet R. J. Mol. Biol. 426 377-388 (2014)
  9. RNA structure prediction using positive and negative evolutionary information. Rivas E. PLoS Comput Biol 16 e1008387 (2020)
  10. Structures of Mycobacterium smegmatis 70S ribosomes in complex with HPF, tmRNA, and P-tRNA. Mishra S, Ahmed T, Tyagi A, Shi J, Bhushan S. Sci Rep 8 13587 (2018)
  11. Structures of tmRNA and SmpB as they transit through the ribosome. Guyomar C, D'Urso G, Chat S, Giudice E, Gillet R. Nat Commun 12 4909 (2021)
  12. The structure of an elongation factor G-ribosome complex captured in the absence of inhibitors. Macé K, Giudice E, Chat S, Gillet R. Nucleic Acids Res. 46 3211-3217 (2018)
  13. tRNA/mRNA Mimicry by tmRNA and SmpB in Trans-Translation. Kurita D, Muto A, Himeno H. J Nucleic Acids 2011 130581 (2011)
  14. tmRNA on its way through the ribosome: two steps of resume, and what next? Fu J, Hashem Y, Wower J, Frank J. RNA Biol 8 586-590 (2011)
  15. An expanded class of histidine-accepting viral tRNA-like structures. Langeberg CJ, Sherlock ME, MacFadden A, Kieft JS. RNA 27 653-664 (2021)
  16. Let's see how tmRNA rescues a stuck ribosome. Klaholz BP. EMBO J. 29 3747-3749 (2010)
  17. Requirements for resuming translation in chimeric transfer-messenger RNAs of Escherichia coli and Mycobacterium tuberculosis. Wower IK, Zwieb C, Wower J. BMC Mol. Biol. 15 19 (2014)
  18. How a circularized tmRNA moves through the ribosome. Rae CD, Gordiyenko Y, Ramakrishnan V. Science 363 740-744 (2019)
  19. In vivo tmRNA protection by SmpB and pre-ribosome binding conformation in solution. Ranaei-Siadat E, Mérigoux C, Seijo B, Ponchon L, Saliou JM, Bernauer J, Sanglier-Cianférani S, Dardel F, Vachette P, Nonin-Lecomte S. RNA 20 1607-1620 (2014)


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