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Structure and function of yeast Lso2 and human CCDC124 bound to hibernating ribosomes.

Wells JN, Buschauer R, Mackens-Kiani T, Best K, Kratzat H, Berninghausen O, Becker T, Gilbert W, Cheng J, Beckmann R
PLoS Biol 18 e3000780 (2020)
Related entries: 6z6j, 6z6k, 6z6m, 6z6n

Cited: 28 times
EuropePMC logo PMID: 32687489

Abstract

Cells adjust to nutrient deprivation by reversible translational shutdown. This is accompanied by maintaining inactive ribosomes in a hibernation state, in which they are bound by proteins with inhibitory and protective functions. In eukaryotes, such a function was attributed to suppressor of target of Myb protein 1 (Stm1; SERPINE1 mRNA-binding protein 1 [SERBP1] in mammals), and recently, late-annotated short open reading frame 2 (Lso2; coiled-coil domain containing short open reading frame 124 [CCDC124] in mammals) was found to be involved in translational recovery after starvation from stationary phase. Here, we present cryo-electron microscopy (cryo-EM) structures of translationally inactive yeast and human ribosomes. We found Lso2/CCDC124 accumulating on idle ribosomes in the nonrotated state, in contrast to Stm1/SERBP1-bound ribosomes, which display a rotated state. Lso2/CCDC124 bridges the decoding sites of the small with the GTPase activating center (GAC) of the large subunit. This position allows accommodation of the duplication of multilocus region 34 protein (Dom34)-dependent ribosome recycling system, which splits Lso2-containing, but not Stm1-containing, ribosomes. We propose a model in which Lso2 facilitates rapid translation reactivation by stabilizing the recycling-competent state of inactive ribosomes.

Reviews - 6z6l mentioned but not cited (1)

  1. The space between notes: emerging roles for translationally silent ribosomes. Smith PR, Pandit SC, Loerch S, Campbell ZT. Trends Biochem Sci 47 477-491 (2022)

Articles - 6z6l mentioned but not cited (2)

  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. Visualization of translation and protein biogenesis at the ER membrane. Gemmer M, Chaillet ML, van Loenhout J, Cuevas Arenas R, Vismpas D, Gröllers-Mulderij M, Koh FA, Albanese P, Scheltema RA, Howes SC, Kotecha A, Fedry J, Förster F. Nature 614 160-167 (2023)


Reviews citing this publication (2)

  1. Domesticated LTR-Retrotransposon gag-Related Gene (Gagr) as a Member of the Stress Response Network in Drosophila. Nefedova L, Gigin A, Kim A. Life (Basel) 12 364 (2022)
  2. The coordinated management of ribosome and translation during injury and regeneration. Nguyen T, Mills JC, Cho CJ. Front Cell Dev Biol 11 1186638 (2023)

Articles citing this publication (23)

  1. Structural basis for translational shutdown and immune evasion by the Nsp1 protein of SARS-CoV-2. Thoms M, Buschauer R, Ameismeier M, Koepke L, Denk T, Hirschenberger M, Kratzat H, Hayn M, Mackens-Kiani T, Cheng J, Straub JH, Stürzel CM, Fröhlich T, Berninghausen O, Becker T, Kirchhoff F, Sparrer KMJ, Beckmann R. Science 369 1249-1255 (2020)
  2. Differences in structure and hibernation mechanism highlight diversification of the microsporidian ribosome. Ehrenbolger K, Jespersen N, Sharma H, Sokolova YY, Tokarev YS, Vossbrinck CR, Barandun J. PLoS Biol 18 e3000958 (2020)
  3. The Halastavi árva Virus Intergenic Region IRES Promotes Translation by the Simplest Possible Initiation Mechanism. Abaeva IS, Vicens Q, Bochler A, Soufari H, Simonetti A, Pestova TV, Hashem Y, Hellen CUT. Cell Rep 33 108476 (2020)
  4. Structures of the eukaryotic ribosome and its translational states in situ. Hoffmann PC, Kreysing JP, Khusainov I, Tuijtel MW, Welsch S, Beck M. Nat Commun 13 7435 (2022)
  5. Structural basis for clearing of ribosome collisions by the RQT complex. Best K, Ikeuchi K, Kater L, Best D, Musial J, Matsuo Y, Berninghausen O, Becker T, Inada T, Beckmann R. Nat Commun 14 921 (2023)
  6. Structural remodeling of ribosome associated Hsp40-Hsp70 chaperones during co-translational folding. Chen Y, Tsai B, Li N, Gao N. Nat Commun 13 3410 (2022)
  7. Impact of Genome Reduction in Microsporidia. Jespersen N, Monrroy L, Barandun J. Exp Suppl 114 1-42 (2022)
  8. TORC1 phosphorylates and inhibits the ribosome preservation factor Stm1 to activate dormant ribosomes. Shetty S, Hofstetter J, Battaglioni S, Ritz D, Hall MN. EMBO J 42 e112344 (2023)
  9. CryoEM reveals that ribosomes in microsporidian spores are locked in a dimeric hibernating state. McLaren M, Conners R, Isupov MN, Gil-Díez P, Gambelli L, Gold VAM, Walter A, Connell SR, Williams B, Daum B. Nat Microbiol 8 1834-1845 (2023)
  10. Dynamic association of human Ebp1 with the ribosome. Bhaskar V, Desogus J, Graff-Meyer A, Schenk AD, Cavadini S, Chao JA. RNA 27 411-419 (2021)
  11. Hibernation-Promoting Factor Sequesters Staphylococcus aureus Ribosomes to Antagonize RNase R-Mediated Nucleolytic Degradation. Lipońska A, Yap MF. mBio 12 e0033421 (2021)
  12. High-resolution structures of a thermophilic eukaryotic 80S ribosome reveal atomistic details of translocation. Kišonaitė M, Wild K, Lapouge K, Ruppert T, Sinning I. Nat Commun 13 476 (2022)
  13. Mechanism of 5S RNP recruitment and helicase-surveilled rRNA maturation during pre-60S biogenesis. Lau B, Huang Z, Kellner N, Niu S, Berninghausen O, Beckmann R, Hurt E, Cheng J. EMBO Rep 24 e56910 (2023)
  14. Negative charge in the RACK1 loop broadens the translational capacity of the human ribosome. Rollins MG, Shasmal M, Meade N, Astar H, Shen PS, Walsh D. Cell Rep 36 109663 (2021)
  15. Overlapping regions of Caf20 mediate its interactions with the mRNA-5'cap-binding protein eIF4E and with ribosomes. Nwokoye EC, AlNaseem E, Crawford RA, Castelli LM, Jennings MD, Kershaw CJ, Pavitt GD. Sci Rep 11 13467 (2021)
  16. 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)
  17. A molecular network of conserved factors keeps ribosomes dormant in the egg. Leesch F, Lorenzo-Orts L, Pribitzer C, Grishkovskaya I, Roehsner J, Chugunova A, Matzinger M, Roitinger E, Belačić K, Kandolf S, Lin TY, Mechtler K, Meinhart A, Haselbach D, Pauli A. Nature 613 712-720 (2023)
  18. A multiplex platform for small RNA sequencing elucidates multifaceted tRNA stress response and translational regulation. Watkins CP, Zhang W, Wylder AC, Katanski CD, Pan T. Nat Commun 13 2491 (2022)
  19. Functionally distinct roles for eEF2K in the control of ribosome availability and p-body abundance. Smith PR, Loerch S, Kunder N, Stanowick AD, Lou TF, Campbell ZT. Nat Commun 12 6789 (2021)
  20. Molecular basis for recognition and deubiquitination of 40S ribosomes by Otu2. Ikeuchi K, Ivic N, Buschauer R, Cheng J, Fröhlich T, Matsuo Y, Berninghausen O, Inada T, Becker T, Beckmann R. Nat Commun 14 2730 (2023)
  21. Rebirth of the translational machinery: The importance of recycling ribosomes. Young DJ, Guydosh NR. Bioessays 44 e2100269 (2022)
  22. Structure of the reduced microsporidian proteasome bound by PI31-like peptides in dormant spores. Jespersen N, Ehrenbolger K, Winiger RR, Svedberg D, Vossbrinck CR, Barandun J. Nat Commun 13 6962 (2022)
  23. The dynamic architecture of Map1- and NatB-ribosome complexes coordinates the sequential modifications of nascent polypeptide chains. Knorr AG, Mackens-Kiani T, Musial J, Berninghausen O, Becker T, Beatrix B, Beckmann R. PLoS Biol 21 e3001995 (2023)


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