Structural basis of tRNA recognition by the widespread OB fold.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
29 Jul 2024
29 Jul 2024
Historique:
received:
28
03
2024
accepted:
18
07
2024
medline:
30
7
2024
pubmed:
30
7
2024
entrez:
29
7
2024
Statut:
epublish
Résumé
The widespread oligonucleotide/oligosaccharide-binding (OB)-fold recognizes diverse substrates from sugars to nucleic acids and proteins, and plays key roles in genome maintenance, transcription, translation, and tRNA metabolism. OB-containing bacterial Trbp and yeast Arc1p proteins are thought to recognize the tRNA elbow or anticodon regions. Here we report a 2.6 Å co-crystal structure of Aquifex aeolicus Trbp111 bound to tRNA
Identifiants
pubmed: 39075051
doi: 10.1038/s41467-024-50730-1
pii: 10.1038/s41467-024-50730-1
doi:
Substances chimiques
RNA, Transfer
9014-25-9
Bacterial Proteins
0
RNA-Binding Proteins
0
Saccharomyces cerevisiae Proteins
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
6385Subventions
Organisme : U.S. Department of Health & Human Services | NIH | National Institute of Diabetes and Digestive and Kidney Diseases (National Institute of Diabetes & Digestive & Kidney Diseases)
ID : ZIADK075136
Informations de copyright
© 2024. This is a U.S. Government work and not under copyright protection in the US; foreign copyright protection may apply.
Références
Raina, M. & Ibba, M. tRNAs as regulators of biological processes. Front. Genet. 5, 171 (2014).
pubmed: 24966867
pmcid: 4052509
doi: 10.3389/fgene.2014.00171
Zhang, J. Interplay between Host tRNAs and HIV-1: A structural perspective. Viruses 13, 1819 (2021).
Bou-Nader, C. et al. HIV-1 matrix-tRNA complex structure reveals basis for host control of Gag localization. Cell Host Microbe 29, 1421–1436.e7 (2021).
pubmed: 34384537
pmcid: 8650744
doi: 10.1016/j.chom.2021.07.006
Sumner, C. et al. Molecular determinants in tRNA D-arm required for inhibition of HIV-1 gag membrane binding. J. Mol. Biol. 434, 167390 (2022).
pubmed: 34883117
doi: 10.1016/j.jmb.2021.167390
Jiang, M. et al. Identification of tRNAs incorporated into wild-type and mutant human immunodeficiency virus type 1. J. Virol. 67, 3246–3253 (1993).
pubmed: 8497049
pmcid: 237665
doi: 10.1128/jvi.67.6.3246-3253.1993
Zhang, J. Recognition of the tRNA structure: Everything everywhere but not all at once. Cell Chem. Biol. 31, 36–52 (2024).
pubmed: 38159570
doi: 10.1016/j.chembiol.2023.12.008
Biela, A. et al. The diverse structural modes of tRNA binding and recognition. J. Biol. Chem. 299, 104966 (2023).
pubmed: 37380076
pmcid: 10424219
doi: 10.1016/j.jbc.2023.104966
Suzuki, T. The expanding world of tRNA modifications and their disease relevance. Nat. Rev. Mol. Cell Biol. 22, 375–392 (2021).
pubmed: 33658722
doi: 10.1038/s41580-021-00342-0
Orellana, E. A., Siegal, E. & Gregory, R. I. tRNA dysregulation and disease. Nat. Rev. Genet. 23, 651–664 (2022).
pubmed: 35681060
pmcid: 11170316
doi: 10.1038/s41576-022-00501-9
Bou-Nader, C. et al. Molecular basis for transfer RNA recognition by the double-stranded RNA-binding domain of human dihydrouridine synthase 2. Nucleic Acids Res. 47, 3117–3126 (2019).
pubmed: 30605527
pmcid: 6451096
doi: 10.1093/nar/gky1302
Kaminska, M., Shalak, V. & Mirande, M. The appended C-domain of human methionyl-tRNA synthetase has a tRNA-sequestering function. Biochemistry 40, 14309–14316 (2001).
pubmed: 11714285
doi: 10.1021/bi015670b
Swairjo, M. A., Morales, A. J., Wang, C. C., Ortiz, A. R. & Schimmel, P. Crystal structure of trbp111: a structure-specific tRNA-binding protein. EMBO J. 19, 6287–6298 (2000).
pubmed: 11101501
pmcid: 305853
doi: 10.1093/emboj/19.23.6287
Morales, A. J., Swairjo, M. A. & Schimmel, P. Structure-specific tRNA-binding protein from the extreme thermophile Aquifex aeolicus. EMBO J. 18, 3475–3483 (1999).
pubmed: 10369686
pmcid: 1171426
doi: 10.1093/emboj/18.12.3475
Teramoto, T. et al. Pentatricopeptide repeats of protein-only RNase P use a distinct mode to recognize conserved bases and structural elements of pre-tRNA. Nucleic Acids Res. 48, 11815–11826 (2020).
pubmed: 32719843
pmcid: 7708040
doi: 10.1093/nar/gkaa627
Aravind, L. & Koonin, E. V. Novel predicted RNA-binding domains associated with the translation machinery. J. Mol. Evol. 48, 291–302 (1999).
pubmed: 10093218
doi: 10.1007/PL00006472
Ishitani, R. et al. Alternative tertiary structure of tRNA for recognition by a posttranscriptional modification enzyme. Cell 113, 383–394 (2003).
pubmed: 12732145
doi: 10.1016/S0092-8674(03)00280-0
Pastore, C. et al. Crystal structure and RNA binding properties of the RNA recognition motif (RRM) and AlkB domains in human AlkB homolog 8 (ABH8), an enzyme catalyzing tRNA hypermodification. J. Biol. Chem. 287, 2130–2143 (2012).
pubmed: 22065580
doi: 10.1074/jbc.M111.286187
Cusack, S. Aminoacyl-tRNA synthetases. Curr. Opin. Struct. Biol. 7, 881–889 (1997).
pubmed: 9434910
doi: 10.1016/S0959-440X(97)80161-3
Kamalampeta, R., Keffer-Wilkes, L. C. & Kothe, U. tRNA binding, positioning, and modification by the pseudouridine synthase Pus10. J. Mol. Biol. 425, 3863–3874 (2013).
pubmed: 23743107
doi: 10.1016/j.jmb.2013.05.022
Yang, W. Q. et al. THUMPD3-TRMT112 is a m2G methyltransferase working on a broad range of tRNA substrates. Nucleic Acids Res. 49, 11900–11919 (2021).
pubmed: 34669960
pmcid: 8599901
doi: 10.1093/nar/gkab927
Jia, J., Arif, A., Ray, P. S. & Fox, P. L. WHEP domains direct noncanonical function of glutamyl-Prolyl tRNA synthetase in translational control of gene expression. Mol. Cell 29, 679–690 (2008).
pubmed: 18374644
pmcid: 2819395
doi: 10.1016/j.molcel.2008.01.010
Abeywansha, T. et al. The structural basis of tRNA recognition by arginyl-tRNA-protein transferase. Nat. Commun. 14, 2232 (2023).
pubmed: 37076488
pmcid: 10115844
doi: 10.1038/s41467-023-38004-8
Murzin, A. G. OB(oligonucleotide/oligosaccharide binding)-fold: common structural and functional solution for non-homologous sequences. EMBO J. 12, 861–867 (1993).
pubmed: 8458342
pmcid: 413284
doi: 10.1002/j.1460-2075.1993.tb05726.x
Agrawal, V. & Kishan, V. R. K. OB-fold: Growing bigger with functional consistency. Curr. Protein Pept. Sci. 4, 195–206 (2003).
pubmed: 12769718
doi: 10.2174/1389203033487207
Theobald, D. L., Mitton-Fry, R. M. & Wuttke, D. S. Nucleic acid recognition by OB-Fold proteins. Annu. Rev. Biophys. Biomol. Struct. 32, 115–133 (2003).
pubmed: 12598368
pmcid: 1564333
doi: 10.1146/annurev.biophys.32.110601.142506
Nomanbhoy, T. et al. Simultaneous binding of two proteins to opposite sides of a single transfer RNA. Nat. Struct. Biol. 8, 344–348 (2001).
pubmed: 11276256
doi: 10.1038/86228
Kawaguchi, S. et al. The crystal structure of the ttCsaA protein: an export-related chaperone from Thermus thermophilus. EMBO J. 20, 562–569 (2001).
pubmed: 11157762
pmcid: 133483
doi: 10.1093/emboj/20.3.562
Simader, H. et al. Structural basis of yeast aminoacyl-tRNA synthetase complex formation revealed by crystal structures of two binary sub-complexes. Nucleic Acids Res. 34, 3968–3979 (2006).
pubmed: 16914447
pmcid: 1557820
doi: 10.1093/nar/gkl560
Deinert, K., Fasiolo, F., Hurt, E. C. & Simos, G. Arc1p Organizes the yeast aminoacyl-tRNA synthetase complex and stabilizes its interaction with the cognate tRNAs. J. Biol. Chem. 276, 6000–6008 (2001).
pubmed: 11069915
doi: 10.1074/jbc.M008682200
Graindorge, J. S., Senger, B., Tritch, D., Simos, G. & Fasiolo, F. Role of Arc1p in the modulation of yeast glutamyl-tRNA synthetase activity. Biochemistry 44, 1344–1352 (2005).
pubmed: 15667228
doi: 10.1021/bi049024z
Simos, G. et al. The yeast protein Arc1p binds to tRNA and functions as a cofactor for the methionyl- and glutamyl-tRNA synthetases. EMBO J. 15, 5437–5448 (1996).
pubmed: 8895587
pmcid: 452286
doi: 10.1002/j.1460-2075.1996.tb00927.x
Bour, T. et al. Apicomplexa-specific tRip facilitates import of exogenous tRNAs into malaria parasites. Proc. Natl. Acad. Sci. USA 113, 4717–4722 (2016).
pubmed: 27071116
pmcid: 4855611
doi: 10.1073/pnas.1600476113
Schwarz, M. A., Lee, D. D. & Bartlett, S. Aminoacyl tRNA synthetase complex interacting multifunctional protein 1 simultaneously binds Glutamyl-Prolyl-tRNA synthetase and scaffold protein aminoacyl tRNA synthetase complex interacting multifunctional protein 3 of the multi-tRNA synthetase complex. Int J. Biochem. Cell Biol. 99, 197–202 (2018).
pubmed: 29679766
pmcid: 5959800
doi: 10.1016/j.biocel.2018.04.015
Quevillon, S., Agou, F., Robinson, J. C. & Mirande, M. The p43 component of the mammalian multi-synthetase complex is likely to be the precursor of the endothelial monocyte-activating polypeptide II cytokine. J. Biol. Chem. 272, 32573–32579 (1997).
pubmed: 9405472
doi: 10.1074/jbc.272.51.32573
Renault, L. et al. Structure of the EMAPII domain of human aminoacyl-tRNA synthetase complex reveals evolutionary dimer mimicry. EMBO J. 20, 570–578 (2001).
pubmed: 11157763
pmcid: 133484
doi: 10.1093/emboj/20.3.570
Shalak, V. et al. The EMAPII cytokine is released from the mammalian multisynthetase complex after cleavage of its p43/proEMAPII component. J. Biol. Chem. 276, 23769–23776 (2001).
pubmed: 11306575
doi: 10.1074/jbc.M100489200
Kapps, D., Cela, M., Théobald-Dietrich, A., Hendrickson, T. & Frugier, M. OB or Not OB: Idiosyncratic utilization of the tRNA-binding OB-fold domain in unicellular, pathogenic eukaryotes. FEBS Lett. 590, 4180–4191 (2016).
pubmed: 27714804
doi: 10.1002/1873-3468.12441
Suzuki, H. et al. Binding properties of split tRNA to the C-terminal domain of methionyl-tRNA synthetase of nanoarchaeum equitans. J. Mol. Evol. 84, 267–278 (2017).
pubmed: 28589220
doi: 10.1007/s00239-017-9796-6
Goldgur, Y. et al. The crystal structure of phenylalanyl-tRNA synthetase from thermus thermophilus complexed with cognate tRNAPhe. Structure 5, 59–68 (1997).
pubmed: 9016717
doi: 10.1016/S0969-2126(97)00166-4
Kalogerakos, T., Dessen, P., Fayat, G. & Blanquet, S. Proteolytic cleavage of methionyl transfer ribonucleic acid synthetase from Bacillus stearothermophilus: effects on activity and structure. Biochemistry 19, 3712–3723 (1980).
pubmed: 6250575
doi: 10.1021/bi00557a012
Kohda, D., Yokoyama, S. & Miyazawa, T. Functions of isolated domains of methionyl-tRNA synthetase from an extreme thermophile, Thermus thermophilus HB8. J. Biol. Chem. 262, 558–563 (1987).
pubmed: 3542990
doi: 10.1016/S0021-9258(19)75819-0
Crepin, T., Schmitt, E., Blanquet, S. & Mechulam, Y. Structure and function of the C-terminal domain of methionyl-tRNA synthetase. Biochemistry 41, 13003–13011 (2002).
pubmed: 12390027
doi: 10.1021/bi026343m
Castro de Moura, M. et al. Entamoeba lysyl-tRNA synthetase contains a cytokine-like domain with chemokine activity towards human endothelial cells. PLoS Negl. Trop. Dis. 5, e1398 (2011).
pubmed: 22140588
pmcid: 3226552
doi: 10.1371/journal.pntd.0001398
Giessen, T. W. et al. A synthetic adenylation-domain-based tRNA-aminoacylation catalyst. Angew. Chem. Int. Ed. Engl. 54, 2492–2496 (2015).
pubmed: 25583137
doi: 10.1002/anie.201410047
Karanasios, E., Boleti, H. & Simos, G. Incorporation of the Arc1p tRNA-binding domain to the catalytic core of MetRS can functionally replace the yeast Arc1p–MetRS complex. J. Mol. Biol. 381, 763–771 (2008).
pubmed: 18598703
doi: 10.1016/j.jmb.2008.06.044
Kaminska, M., Deniziak, M., Kerjan, P., Barciszewski, J. & Mirande, M. A recurrent general RNA binding domain appended to plant methionyl-tRNA synthetase acts as a cis-acting cofactor for aminoacylation. EMBO J. 19, 6908–6917 (2000).
pubmed: 11118226
pmcid: 305886
doi: 10.1093/emboj/19.24.6908
Mellot, P., Mechulam, Y., Le Corre, D., Blanquet, S. & Fayat, G. Identification of an amino acid region supporting specific methionyl-tRNA synthetase: tRNA recognition. J. Mol. Biol. 208, 429–443 (1989).
pubmed: 2477552
doi: 10.1016/0022-2836(89)90507-X
Heffler, M. A., Walters, R. D. & Kugel, J. F. Using electrophoretic mobility shift assays to measure equilibrium dissociation constants: GAL4-p53 binding DNA as a model system. Biochem. Mol. Biol. Educ. 40, 383–387 (2012).
pubmed: 23166026
doi: 10.1002/bmb.20649
Li, S. et al. Structural basis of amino acid surveillance by higher-order tRNA-mRNA interactions. Nat. Struct. Mol. Biol. 26, 1094–1105 (2019).
pubmed: 31740854
pmcid: 6899168
doi: 10.1038/s41594-019-0326-7
Ohmori, S. et al. RNA Aptamers for a tRNA-binding protein from aeropyrum pernix with homologous counterparts distributed throughout evolution. Life 10, 11 (2020).
Zhang, J. & Ferré-D’Amaré, A. R. Direct evaluation of tRNA aminoacylation status by the T-box riboswitch using tRNA-mRNA stacking and steric readout. Mol. Cell 55, 148–155 (2014).
pubmed: 24954903
pmcid: 4104367
doi: 10.1016/j.molcel.2014.05.017
Jean, J. M. & Hall, K. B. 2-Aminopurine fluorescence quenching and lifetimes: role of base stacking. Proc. Natl. Acad. Sci. USA 98, 37–41 (2001).
pubmed: 11120885
doi: 10.1073/pnas.98.1.37
Ruff, M. et al. Class II aminoacyl transfer RNA synthetases: crystal structure of yeast aspartyl-tRNA synthetase complexed with tRNA(Asp). Science 252, 1682–1689 (1991).
pubmed: 2047877
doi: 10.1126/science.2047877
Nissen, P., Thirup, S., Kjeldgaard, M. & Nyborg, J. The crystal structure of Cys-tRNACys-EF-Tu-GDPNP reveals general and specific features in the ternary complex and in tRNA. Structure 7, 143–156 (1999).
pubmed: 10368282
doi: 10.1016/S0969-2126(99)80021-5
Cook, A. G., Fukuhara, N., Jinek, M. & Conti, E. Structures of the tRNA export factor in the nuclear and cytosolic states. Nature 461, 60–65 (2009).
pubmed: 19680239
doi: 10.1038/nature08394
Beenstock, J. et al. A substrate binding model for the KEOPS tRNA modifying complex. Nat. Commun. 11, 6233 (2020).
pubmed: 33277478
pmcid: 7718258
doi: 10.1038/s41467-020-19990-5
Simos, G., Sauer, A., Fasiolo, F. & Hurt, E. C. A conserved domain within Arc1p delivers tRNA to aminoacyl-tRNA synthetases. Mol. Cell 1, 235–242 (1998).
pubmed: 9659920
doi: 10.1016/S1097-2765(00)80024-6
Skeparnias, I. et al. Structural basis of MALAT-1 RNA maturation and mascRNA biogenesis. Nat. Struct. Mol. Biol. https://doi.org/10.1038/s41594-024-01340-4 (2024).
Andreeva, A., Kulesha, E., Gough, J. & Murzin, A. G. The SCOP database in 2020: expanded classification of representative family and superfamily domains of known protein structures. Nucleic Acids Res. 48, D376–d382 (2020).
pubmed: 31724711
doi: 10.1093/nar/gkz1064
Bianco, P. R. OB-fold Families of genome guardians: A universal theme constructed from the small β-barrel building block. Front. Mol. Biosci. 9, 784451 (2022).
Chakshusmathi, G., Kim, S. D., Rubinson, D. A. & Wolin, S. L. A La protein requirement for efficient pre-tRNA folding. EMBO J. 22, 6562–6572 (2003).
pubmed: 14657028
pmcid: 291820
doi: 10.1093/emboj/cdg625
Wilusz, J. E. et al. A triple helix stabilizes the 3’ ends of long noncoding RNAs that lack poly(A) tails. Genes Dev. 26, 2392–2407 (2012).
pubmed: 23073843
pmcid: 3489998
doi: 10.1101/gad.204438.112
Brown, J. A. et al. Structural insights into the stabilization of MALAT1 noncoding RNA by a bipartite triple helix. Nat. Struct. Mol. Biol. 21, 633–640 (2014).
pubmed: 24952594
pmcid: 4096706
doi: 10.1038/nsmb.2844
Golinelli-Cohen, M. P. & Mirande, M. Arc1p is required for cytoplasmic confinement of synthetases and tRNA. Mol. Cell Biochem. 300, 47–59 (2007).
pubmed: 17131041
doi: 10.1007/s11010-006-9367-4
Khan, K. et al. Multimodal cotranslational interactions direct assembly of the human multi-tRNA synthetase complex. Proc. Natl. Acad. Sci. USA 119, e2205669119 (2022).
pubmed: 36037331
pmcid: 9457175
doi: 10.1073/pnas.2205669119
Hood, I. V. et al. Crystal structure of an adenovirus virus-associated RNA. Nat. Commun. 10, 2871 (2019).
pubmed: 31253805
pmcid: 6599070
doi: 10.1038/s41467-019-10752-6
Sapkota, K. P., Li, S. & Zhang, J. Cotranscriptional assembly and native purification of large RNA-RNA complexes for structural analyses. Methods Mol. Biol. 2568, 1–12 (2023).
pubmed: 36227558
pmcid: 11275850
doi: 10.1007/978-1-0716-2687-0_1
Bou-Nader, C. & Zhang, J. Rational engineering enables co-crystallization and structural determination of the HIV-1 matrix-tRNA complex. STAR Protoc. 3, 101056 (2022).
pubmed: 35005638
doi: 10.1016/j.xpro.2021.101056
McCoy, A. J. et al. Phaser crystallographic software. J. Appl. Crystallogr. 40, 658–674 (2007).
pubmed: 19461840
pmcid: 2483472
doi: 10.1107/S0021889807021206
Suddala, K. C. & Zhang, J. High-affinity recognition of specific tRNAs by an mRNA anticodon-binding groove. Nat. Struct. Mol. Biol. 26, 1114–1122 (2019).
pubmed: 31792448
pmcid: 6903423
doi: 10.1038/s41594-019-0335-6
Emsley, P., Lohkamp, B., Scott, W. G. & Cowtan, K. Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486–501 (2010).
pubmed: 20383002
pmcid: 2852313
doi: 10.1107/S0907444910007493
Liebschner, D. et al. Macromolecular structure determination using X-rays, neutrons and electrons: recent developments in Phenix. Acta Crystallogr D Struct. Biol. 75, 861–877 (2019).
pubmed: 31588918
pmcid: 6778852
doi: 10.1107/S2059798319011471
Zhao, H., Brautigam, C. A., Ghirlando, R. & Schuck, P. Overview of current methods in sedimentation velocity and sedimentation equilibrium analytical ultracentrifugation. Curr. Protoc. Protein Sci. 71, 20.12.1–20.12.49 (2013).
Schuck, P. Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and lamm equation modeling. Biophys. J. 78, 1606–1619 (2000).
pubmed: 10692345
pmcid: 1300758
doi: 10.1016/S0006-3495(00)76713-0
Laue, T. M., Shah, B. D., Ridgeway, T. M. & Pelletier, S. L. Analytical ultracentrifugation in biochemistry and polymer science, (Royal Society of Chemistry, 1992).
Zhao, H., Piszczek, G. & Schuck, P. SEDPHAT–a platform for global ITC analysis and global multi-method analysis of molecular interactions. Methods 76, 137–148 (2015).
pubmed: 25477226
doi: 10.1016/j.ymeth.2014.11.012
Yariv, B. et al. Using evolutionary data to make sense of macromolecules with a “face-lifted” ConSurf. Protein Sci. 32, e4582 (2023).
pubmed: 36718848
pmcid: 9942591
doi: 10.1002/pro.4582
Eiler, S., Dock-Bregeon, A., Moulinier, L., Thierry, J. C. & Moras, D. Synthesis of aspartyl-tRNA(Asp) in Escherichia coli–a snapshot of the second step. EMBO J. 18, 6532–6541 (1999).
pubmed: 10562565
pmcid: 1171716
doi: 10.1093/emboj/18.22.6532
Bochkarev, A., Pfuetzner, R. A., Edwards, A. M. & Frappier, L. Structure of the single-stranded-DNA-binding domain of replication protein A bound to DNA. Nature 385, 176–181 (1997).
pubmed: 8990123
doi: 10.1038/385176a0