Bacterial ribosome collision sensing by a MutS DNA repair ATPase paralogue.
Journal
Nature
ISSN: 1476-4687
Titre abrégé: Nature
Pays: England
ID NLM: 0410462
Informations de publication
Date de publication:
03 2022
03 2022
Historique:
received:
28
09
2021
accepted:
28
01
2022
pubmed:
11
3
2022
medline:
23
4
2022
entrez:
10
3
2022
Statut:
ppublish
Résumé
Ribosome stalling during translation is detrimental to cellular fitness, but how this is sensed and elicits recycling of ribosomal subunits and quality control of associated mRNA and incomplete nascent chains is poorly understood
Identifiants
pubmed: 35264791
doi: 10.1038/s41586-022-04487-6
pii: 10.1038/s41586-022-04487-6
pmc: PMC9041291
mid: NIHMS1783385
doi:
Substances chimiques
Proteins
0
Adenosine Triphosphatases
EC 3.6.1.-
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
509-514Subventions
Organisme : NINDS NIH HHS
ID : R01 NS102414
Pays : United States
Commentaires et corrections
Type : CommentIn
Informations de copyright
© 2022. The Author(s), under exclusive licence to Springer Nature Limited.
Références
Joazeiro, C. A. P. Ribosomal stalling during translation: providing substrates for ribosome-associated protein quality control. Annu. Rev. Cell Dev. Biol. 33, 343–368 (2017).
pubmed: 28715909
doi: 10.1146/annurev-cellbio-111315-125249
Meydan, S. & Guydosh, N. R. A cellular handbook for collided ribosomes: surveillance pathways and collision types. Curr. Genet. 67, 19–26 (2021).
pubmed: 33044589
doi: 10.1007/s00294-020-01111-w
Modrich, P. Mechanisms in E. coli and human mismatch repair (Nobel Lecture). Angew. Chem. Int. Ed. Engl. 55, 8490–8501 (2016).
pubmed: 27198632
pmcid: 5193110
doi: 10.1002/anie.201601412
Moore, S. D. & Sauer, R. T. The tmRNA system for translational surveillance and ribosome rescue. Annu. Rev. Biochem. 76, 101–124 (2007).
pubmed: 17291191
doi: 10.1146/annurev.biochem.75.103004.142733
Joazeiro, C. A. P. Mechanisms and functions of ribosome-associated protein quality control. Nat. Rev. Mol. Cell Biol. 20, 368–383 (2019).
pubmed: 30940912
pmcid: 7138134
doi: 10.1038/s41580-019-0118-2
Venkataraman, K., Guja, K. E., Garcia-Diaz, M. & Karzai, A. W. Non-stop mRNA decay: a special attribute of trans-translation mediated ribosome rescue. Front. Microbiol. 5, 93 (2014).
pubmed: 24653719
pmcid: 3949413
doi: 10.3389/fmicb.2014.00093
Howard, C. J. & Frost, A. Ribosome-associated quality control and CAT tailing. Crit. Rev. Biochem. Mol. Biol. 56, 603–620 (2021).
pubmed: 34233554
doi: 10.1080/10409238.2021.1938507
Lytvynenko, I. et al. Alanine tails signal proteolysis in bacterial ribosome-associated quality control. Cell 178, 76–90 (2019).
pubmed: 31155236
pmcid: 6642441
doi: 10.1016/j.cell.2019.05.002
D’Orazio, K. N. & Green, R. Ribosome states signal RNA quality control. Mol. Cell 81, 1372–1383 (2021).
pubmed: 33713598
pmcid: 8041214
doi: 10.1016/j.molcel.2021.02.022
Vind, A. C., Genzor, A. V. & Bekker-Jensen, S. Ribosomal stress-surveillance: three pathways is a magic number. Nucleic Acids Res. 48, 10648–10661 (2020).
pubmed: 32941609
pmcid: 7641731
doi: 10.1093/nar/gkaa757
Ikeuchi, K. et al. Collided ribosomes form a unique structural interface to induce Hel2‐driven quality control pathways. EMBO J. 38, 1–40 (2019).
doi: 10.15252/embj.2018100276
Simms, C. L., Yan, L. L. & Zaher, H. S. Ribosome collision is critical for quality control during no-go decay. Mol. Cell 68, 361–373 (2017).
pubmed: 28943311
pmcid: 5659757
doi: 10.1016/j.molcel.2017.08.019
Juszkiewicz, S. et al. ZNF598 is a quality control sensor of collided ribosomes. Mol. Cell 72, 469–481 (2018).
pubmed: 30293783
pmcid: 6224477
doi: 10.1016/j.molcel.2018.08.037
Garzia, A. et al. The E3 ubiquitin ligase and RNA-binding protein ZNF598 orchestrates ribosome quality control of premature polyadenylated mRNAs. Nat. Commun. 8, 16056 (2017).
pubmed: 28685749
pmcid: 5504347
doi: 10.1038/ncomms16056
Sundaramoorthy, E. et al. ZNF598 and RACK1 regulate mammalian ribosome-associated quality control function by mediating regulatory 40S ribosomal ubiquitylation. Mol. Cell 65, 751–760 (2017).
pubmed: 28132843
pmcid: 5321136
doi: 10.1016/j.molcel.2016.12.026
Juszkiewicz, S., Speldewinde, S. H., Wan, L., Svejstrup, J. Q. & Hegde, R. S. The ASC-1 complex disassembles collided ribosomes. Mol. Cell 79, 603–614 (2020).
pubmed: 32579943
pmcid: 7447978
doi: 10.1016/j.molcel.2020.06.006
Matsuo, Y. et al. RQT complex dissociates ribosomes collided on endogenous RQC substrate SDD1. Nat. Struct. Mol. Biol. 27, 323–332 (2020).
pubmed: 32203490
doi: 10.1038/s41594-020-0393-9
Matsuo, Y. et al. Ubiquitination of stalled ribosome triggers ribosome-associated quality control. Nat. Commun. 8, 159 (2017).
pubmed: 28757607
pmcid: 5534433
doi: 10.1038/s41467-017-00188-1
Glover, M. L. et al. NONU-1 encodes a conserved endonuclease required for mRNA translation surveillance. Cell Rep. 30, 4321–4331 (2020).
pubmed: 32234470
pmcid: 7184879
doi: 10.1016/j.celrep.2020.03.023
D’Orazio, K. N. et al. The endonuclease Cue2 cleaves mRNAs at stalled ribosomes during no go decay. eLife 8, e49117 (2019).
pubmed: 31219035
pmcid: 6598757
doi: 10.7554/eLife.49117
Nürenberg-Goloub, E. & Tampé, R. Ribosome recycling in mRNA translation, quality control, and homeostasis. Biol. Chem. 401, 47–61 (2019).
pubmed: 31665102
doi: 10.1515/hsz-2019-0279
Donaldson, K. M., Yin, H., Gekakis, N., Supek, F. & Joazeiro, C. A. P. Ubiquitin signals protein trafficking via interaction with a novel ubiquitin binding domain in the membrane fusion regulator, Vps9p. Curr. Biol. 13, 258–262 (2003).
pubmed: 12573224
doi: 10.1016/S0960-9822(03)00043-5
Burby, P. E. & Simmons, L. A. MutS2 promotes homologous recombination in Bacillus subtilis. J. Bacteriol. 199, e00682-16 (2017).
pubmed: 27799325
doi: 10.1128/JB.00682-16
Pinto, A. V. et al. Suppression of homologous and homeologous recombination by the bacterial MutS2 protein. Mol. Cell 17, 113–120 (2005).
pubmed: 15629722
doi: 10.1016/j.molcel.2004.11.035
Hingorani, M. M. Mismatch binding, ADP–ATP exchange and intramolecular signaling during mismatch repair. DNA Repair 38, 24–31 (2016).
pubmed: 26704427
doi: 10.1016/j.dnarep.2015.11.017
Groothuizen, F. S. & Sixma, T. K. The conserved molecular machinery in DNA mismatch repair enzyme structures. DNA Repair 38, 14–23 (2016).
pubmed: 26796427
doi: 10.1016/j.dnarep.2015.11.012
Kyrpides, N. C., Woese, C. R. & Ouzounis, C. A. KOW: a novel motif linking a bacterial transcription factor with ribosomal proteins. Trends Biochem. Sci. 21, 425–426 (1996).
pubmed: 8987397
doi: 10.1016/S0968-0004(96)30036-4
Fukui, K. & Kuramitsu, S. Structure and function of the small MutS-related domain. Mol. Biol. Int. 2011, 691735 (2011).
pubmed: 22091410
pmcid: 3200294
doi: 10.4061/2011/691735
Sachadyn, P. Conservation and diversity of MutS proteins. Mutat. Res. 694, 20–30 (2010).
pubmed: 20833188
doi: 10.1016/j.mrfmmm.2010.08.009
Pochopien, A. A. et al. Structure of Gcn1 bound to stalled and colliding 80S ribosomes. Proc. Natl Acad. Sci. USA 118, e2022756118 (2021).
pubmed: 33790014
pmcid: 8040806
doi: 10.1073/pnas.2022756118
Sohmen, D. et al. Structure of the Bacillus subtilis 70S ribosome reveals the basis for species-specific stalling. Nat. Commun. 6, 6941 (2015).
pubmed: 25903689
doi: 10.1038/ncomms7941
Smith, A. M., Costello, M. S., Kettring, A. H., Wingo, R. J. & Moore, S. D. Ribosome collisions alter frameshifting at translational reprogramming motifs in bacterial mRNAs. Proc. Natl Acad. Sci. USA 116, 21769–21779 (2019).
pubmed: 31591196
pmcid: 6815119
doi: 10.1073/pnas.1910613116
Borovinskaya, M. A., Shoji, S., Holton, J. M., Fredrick, K. & Cate, J. H. D. A steric block in translation caused by the antibiotic spectinomycin. ACS Chem. Biol. 2, 545–552 (2007).
pubmed: 17696316
pmcid: 4624401
doi: 10.1021/cb700100n
Brodersen, D. E. et al. The structural basis for the action of the antibiotics tetracycline, pactamycin, and hygromycin B on the 30S ribosomal subunit. Cell 103, 1143–1154 (2000).
pubmed: 11163189
doi: 10.1016/S0092-8674(00)00216-6
Svetlov, M. S. et al. High-resolution crystal structures of ribosome-bound chloramphenicol and erythromycin provide the ultimate basis for their competition. RNA 25, 600–606 (2019).
pubmed: 30733327
pmcid: 6467010
doi: 10.1261/rna.069260.118
Filbeck, S. et al. Mimicry of canonical translation elongation underlies alanine tail synthesis in RQC. Mol. Cell 81, 104–114 (2021).
pubmed: 33259811
doi: 10.1016/j.molcel.2020.11.001
Crowe-McAuliffe, C. et al. Structural basis for bacterial ribosome-associated quality control by RqcH and RqcP. Mol. Cell 81, 115–126 (2021).
pubmed: 33259810
doi: 10.1016/j.molcel.2020.11.002
Takada, H. et al. RqcH and RqcP catalyze processive poly-alanine synthesis in a reconstituted ribosome-associated quality control system. Nucleic Acids Res. 49, 8355–8369 (2021).
pubmed: 34255840
pmcid: 8373112
doi: 10.1093/nar/gkab589
Thrun, A. et al. Convergence of mammalian RQC and C-end rule proteolytic pathways via alanine tailing. Mol. Cell 81, 2112–2122 (2021).
pubmed: 33909987
doi: 10.1016/j.molcel.2021.03.004
Korostelev, A., Trakhanov, S., Laurberg, M. & Noller, H. F. Crystal structure of a 70S ribosome–tRNA complex reveals functional interactions and rearrangements. Cell 126, 1065–1077 (2006).
pubmed: 16962654
doi: 10.1016/j.cell.2006.08.032
Tejada-Arranz, A., de Crécy-Lagard, V. & de Reuse, H. Bacterial RNA degradosomes: molecular machines under tight control. Trends Biochem. Sci. 45, 42–57 (2020).
pubmed: 31679841
doi: 10.1016/j.tibs.2019.10.002
Arnaud, M., Chastanet, A. & Débarbouillé, M. New vector for efficient allelic replacement in naturally nontransformable, low-GC-content, gram-positive bacteria. Appl. Environ. Microbiol. 70, 6887–6891 (2004).
pubmed: 15528558
pmcid: 525206
doi: 10.1128/AEM.70.11.6887-6891.2004
Koo, B.-M. et al. Construction and analysis of two genome-scale deletion libraries for Bacillus subtilis. Cell Syst. 4, 291–305 (2017).
pubmed: 28189581
pmcid: 5400513
doi: 10.1016/j.cels.2016.12.013
Mende, D. R. et al. proGenomes2: an improved database for accurate and consistent habitat, taxonomic and functional annotations of prokaryotic genomes. Nucleic Acids Res. 48, D621–D625 (2020).
pubmed: 31647096
Bucher, P., Karplus, K., Moeri, N. & Hofmann, K. A flexible motif search technique based on generalized profiles. Comput. Chem. 20, 3–23 (1996).
pubmed: 8867839
doi: 10.1016/S0097-8485(96)80003-9
Levy, J. A., LaFlamme, C. W., Tsaprailis, G., Crynen, G. & Page, D. T. Dyrk1a mutations cause undergrowth of cortical pyramidal neurons via dysregulated growth factor signaling. Biol. Psychiatry 90, 295–306 (2021).
pubmed: 33840455
doi: 10.1016/j.biopsych.2021.01.012
Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676–682 (2012).
pubmed: 22743772
doi: 10.1038/nmeth.2019
Zivanov, J., Nakane, T. & Scheres, S. H. W. Estimation of high-order aberrations and anisotropic magnification from cryo-EM data sets in RELION-3.1. IUCrJ 7, 253–267 (2020).
pubmed: 32148853
pmcid: 7055373
doi: 10.1107/S2052252520000081
Pettersen, E. F. et al. UCSF Chimera—a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605–1612 (2004).
pubmed: 15264254
doi: 10.1002/jcc.20084
Crowe-McAuliffe, C. et al. Structural basis for antibiotic resistance mediated by the Bacillus subtilis ABCF ATPase VmlR. Proc. Natl Acad. Sci. USA 115, 8978–8983 (2018).
pubmed: 30126986
pmcid: 6130385
doi: 10.1073/pnas.1808535115
Matzov, D. et al. The cryo-EM structure of hibernating 100S ribosome dimer from pathogenic Staphylococcus aureus. Nat. Commun. 8, 723 (2017).
pubmed: 28959035
pmcid: 5620080
doi: 10.1038/s41467-017-00753-8
Hoffman, D. W. et al. Crystal structure of prokaryotic ribosomal protein L9: a bi-lobed RNA-binding protein. EMBO J. 13, 205–212 (1994).
pubmed: 8306963
pmcid: 394794
doi: 10.1002/j.1460-2075.1994.tb06250.x
Zimmermann, L. et al. A completely reimplemented MPI Bioinformatics Toolkit with a new HHpred server at its core. J. Mol. Biol. 430, 2237–2243 (2018).
pubmed: 29258817
doi: 10.1016/j.jmb.2017.12.007
Liebschner, D. et al. Macromolecular structure determination using X-rays, neutrons and electrons: recent developments in Phenix. Acta Crystallogr. D 75, 861–877 (2019).
doi: 10.1107/S2059798319011471
Emsley, P., Lohkamp, B., Scott, W. G. & Cowtan, K. Features and development of Coot. Acta Crystallogr. D 66, 486–501 (2010).
pubmed: 20383002
pmcid: 2852313
doi: 10.1107/S0907444910007493
Croll, T. I. ISOLDE: a physically realistic environment for model building into low-resolution electron-density maps. Acta Crystallogr. D 74, 519–530 (2018).
doi: 10.1107/S2059798318002425
Jumper, J. et al. Highly accurate protein structure prediction with AlphaFold. Nature 596, 583–589 (2021).
pubmed: 34265844
pmcid: 8371605
doi: 10.1038/s41586-021-03819-2
Kelley, L. A., Mezulis, S., Yates, C. M., Wass, M. N. & Sternberg, M. J. E. The Phyre2 web portal for protein modeling, prediction and analysis. Nat. Protoc. 10, 845–858 (2015).
pubmed: 25950237
pmcid: 5298202
doi: 10.1038/nprot.2015.053
Humphrey, W., Dalke, A. & Schulten, K. VMD: visual molecular dynamics. J. Mol. Graph. 14, 33–38 (1996).
pubmed: 8744570
doi: 10.1016/0263-7855(96)00018-5
Ribeiro, J. V. et al. QwikMD—integrative molecular dynamics toolkit for novices and experts. Sci. Rep. 6, 26536 (2016).
pubmed: 27216779
pmcid: 4877583
doi: 10.1038/srep26536
Trabuco, L. G., Villa, E., Mitra, K., Frank, J. & Schulten, K. Flexible fitting of atomic structures into electron microscopy maps using molecular dynamics. Structure 16, 673–683 (2008).
pubmed: 18462672
pmcid: 2430731
doi: 10.1016/j.str.2008.03.005
Phillips, J. C. et al. Scalable molecular dynamics on CPU and GPU architectures with NAMD. J. Chem. Phys. 153, 044130 (2020).
pubmed: 32752662
pmcid: 7395834
doi: 10.1063/5.0014475
Rundlet, E. J. et al. Structural basis of early translocation events on the ribosome. Nature 595, 741–745 (2021).
pubmed: 34234344
pmcid: 8318882
doi: 10.1038/s41586-021-03713-x
Loveland, A. B., Demo, G. & Korostelev, A. A. Cryo-EM of elongating ribosome with EF-Tu•GTP elucidates tRNA proofreading. Nature 584, 640–645 (2020).
pubmed: 32612237
pmcid: 7483604
doi: 10.1038/s41586-020-2447-x
Goddard, T. D. et al. UCSF ChimeraX: meeting modern challenges in visualization and analysis. Protein Sci. 27, 14–25 (2018).
pubmed: 28710774
doi: 10.1002/pro.3235
Amiri, H. & Noller, H. F. Structural evidence for product stabilization by the ribosomal mRNA helicase. RNA 25, 364–375 (2019).
pubmed: 30552154
pmcid: 6380275
doi: 10.1261/rna.068965.118