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KEOPS in eukaryotes participates in its biogenesis, whose mutations are connected with Galloway-Mowat syndrome. However, the tRNA substrate selection mechanism by KEOPS and t6A modification function in mammalian cells remain unclear. Here, we confirmed that all ANN-decoding human cytoplasmic tRNAs harbor a t6A moiety. Using t6A modification systems from various eukaryotes, we proposed the possible coevolution of position 33 of initiator tRNAMet and modification enzymes. The role of the universal CCA end in t6A biogenesis varied among species. However, all KEOPSs critically depended on C32 and two base pairs in the D-stem. Knockdown of the catalytic subunit OSGEP in HEK293T cells had no effect on the steady-state abundance of cytoplasmic tRNAs but selectively inhibited tRNAIle aminoacylation. Combined with in vitro aminoacylation assays, we revealed that t6A functions as a tRNAIle isoacceptor-specific positive determinant for human cytoplasmic isoleucyl-tRNA synthetase (IARS1). t6A deficiency had divergent effects on decoding efficiency at ANN codons and promoted +1 frameshifting. Altogether, our results shed light on the tRNA recognition mechanism, revealing both commonality and diversity in substrate recognition by eukaryotic KEOPSs, and elucidated the critical role of t6A in tRNAIle aminoacylation and codon decoding in human cells.<\/jats:p>","DOI":"10.1093\/nar\/gkac056","type":"journal-article","created":{"date-parts":[[2022,1,25]],"date-time":"2022-01-25T12:22:30Z","timestamp":1643113350000},"page":"2223-2239","source":"Crossref","is-referenced-by-count":36,"title":["Commonality and diversity in tRNA substrate recognition in t6A biogenesis by eukaryotic KEOPSs"],"prefix":"10.1093","volume":"50","author":[{"given":"Jin-Tao","family":"Wang","sequence":"first","affiliation":[{"name":"State Key Laboratory of Molecular Biology, CAS Center for Excellence in Molecular Cell Science, Shanghai Institute of Biochemistry and Cell Biology, Chinese Academy of Sciences, University of Chinese Academy of Sciences, 320 Yue Yang Road, Shanghai 200031, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jing-Bo","family":"Zhou","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Molecular Biology, CAS Center for Excellence in Molecular Cell Science, Shanghai Institute of Biochemistry and Cell Biology, Chinese Academy of Sciences, University of Chinese Academy of Sciences, 320 Yue Yang Road, Shanghai 200031, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xue-Ling","family":"Mao","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Molecular Biology, CAS Center for Excellence in Molecular Cell Science, Shanghai Institute of Biochemistry and Cell Biology, Chinese Academy of Sciences, University of Chinese Academy of Sciences, 320 Yue Yang Road, Shanghai 200031, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Li","family":"Zhou","sequence":"additional","affiliation":[{"name":"School of Life Sciences, Lanzhou University, 222 South Tianshui Road, Lanzhou 730000, Gansu"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Meirong","family":"Chen","sequence":"additional","affiliation":[{"name":"School of Pharmacy, China Pharmaceutical University, 639 Longmian Avenue, Nanjing 211198, Jiangsu"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wenhua","family":"Zhang","sequence":"additional","affiliation":[{"name":"School of Life Sciences, Lanzhou University, 222 South Tianshui Road, Lanzhou 730000, Gansu"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3657-1166","authenticated-orcid":false,"given":"En-Duo","family":"Wang","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Molecular Biology, CAS Center for Excellence in Molecular Cell Science, Shanghai Institute of Biochemistry and Cell Biology, Chinese Academy of Sciences, University of Chinese Academy of Sciences, 320 Yue Yang Road, Shanghai 200031, China"},{"name":"School of Life Science and Technology, ShanghaiTech University, 393 Middle Hua Xia Road, Shanghai 201210, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3701-5965","authenticated-orcid":false,"given":"Xiao-Long","family":"Zhou","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Molecular Biology, CAS Center for Excellence in Molecular Cell Science, Shanghai Institute of Biochemistry and Cell Biology, Chinese Academy of Sciences, University of Chinese Academy of Sciences, 320 Yue Yang Road, Shanghai 200031, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2022,2,1]]},"reference":[{"key":"2022022611393264900_B1","doi-asserted-by":"crossref","first-page":"1957","DOI":"10.1261\/rna.077537.120","article-title":"Comparative patterns of modified nucleotides in individual tRNA species from a mesophilic and two thermophilic archaea","volume":"26","author":"Wolff","year":"2020","journal-title":"RNA"},{"key":"2022022611393264900_B2","doi-asserted-by":"crossref","first-page":"375","DOI":"10.1038\/s41580-021-00342-0","article-title":"The expanding world of tRNA modifications and their disease relevance","volume":"22","author":"Suzuki","year":"2021","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"2022022611393264900_B3","doi-asserted-by":"crossref","first-page":"7087","DOI":"10.1007\/s00018-021-03948-x","article-title":"Modifications of the human tRNA anticodon loop and their associations with genetic diseases","volume":"78","author":"Zhou","year":"2021","journal-title":"Cell. Mol. Life Sci."},{"key":"2022022611393264900_B4","doi-asserted-by":"crossref","first-page":"2143","DOI":"10.1093\/nar\/gkz011","article-title":"Matching tRNA modifications in humans to their known and predicted enzymes","volume":"47","author":"de\u00a0Crecy-Lagard","year":"2019","journal-title":"Nucleic Acids Res."},{"key":"2022022611393264900_B5","doi-asserted-by":"crossref","first-page":"10818","DOI":"10.1093\/nar\/gkab865","article-title":"The structural and functional workings of KEOPS","volume":"49","author":"Beenstock","year":"2021","journal-title":"Nucleic Acids Res."},{"key":"2022022611393264900_B6","doi-asserted-by":"crossref","first-page":"1529","DOI":"10.4161\/15476286.2014.992277","article-title":"Diversity of the biosynthesis pathway for threonylcarbamoyladenosine (t(6)A), a universal modification of tRNA","volume":"11","author":"Thiaville","year":"2014","journal-title":"RNA Biol."},{"key":"2022022611393264900_B7","doi-asserted-by":"crossref","first-page":"2894","DOI":"10.1093\/nar\/gkp152","article-title":"The universal YrdC\/Sua5 family is required for the formation of threonylcarbamoyladenosine in tRNA","volume":"37","author":"El\u00a0Yacoubi","year":"2009","journal-title":"Nucleic Acids Res."},{"key":"2022022611393264900_B8","doi-asserted-by":"crossref","first-page":"5850","DOI":"10.1093\/nar\/gky323","article-title":"The structure of the TsaB\/TsaD\/TsaE complex reveals an unexpected mechanism for the bacterial t6A tRNA-modification","volume":"46","author":"Missoury","year":"2018","journal-title":"Nucleic Acids Res."},{"key":"2022022611393264900_B9","doi-asserted-by":"crossref","first-page":"1395","DOI":"10.1093\/nar\/gkx1300","article-title":"Structure and mechanism of a bacterial t6A biosynthesis system","volume":"46","author":"Luthra","year":"2018","journal-title":"Nucleic Acids Res."},{"key":"2022022611393264900_B10","doi-asserted-by":"crossref","first-page":"13666","DOI":"10.1074\/jbc.M112.344028","article-title":"Biosynthesis of threonylcarbamoyl adenosine (t6A), a universal tRNA nucleoside","volume":"287","author":"Deutsch","year":"2012","journal-title":"J. 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Struct. Mol. Biol."},{"key":"2022022611393264900_B24","doi-asserted-by":"crossref","first-page":"1199","DOI":"10.1111\/mmi.13209","article-title":"Essentiality of threonylcarbamoyladenosine (t(6)A), a universal tRNA modification, in bacteria","volume":"98","author":"Thiaville","year":"2015","journal-title":"Mol. Microbiol."},{"key":"2022022611393264900_B25","doi-asserted-by":"crossref","first-page":"1529","DOI":"10.1038\/ng.3933","article-title":"Mutations in KEOPS-complex genes cause nephrotic syndrome with primary microcephaly","volume":"49","author":"Braun","year":"2017","journal-title":"Nat. Genet."},{"key":"2022022611393264900_B26","doi-asserted-by":"crossref","first-page":"354","DOI":"10.1128\/MCB.00754-09","article-title":"The Sua5 protein is essential for normal translational regulation in yeast","volume":"30","author":"Lin","year":"2010","journal-title":"Mol. Cell Biol."},{"key":"2022022611393264900_B27","doi-asserted-by":"crossref","first-page":"29","DOI":"10.15698\/mic2016.01.473","article-title":"Global translational impacts of the loss of the tRNA modification t(6)A in yeast","volume":"3","author":"Thiaville","year":"2016","journal-title":"Microb. Cell"},{"key":"2022022611393264900_B28","doi-asserted-by":"crossref","first-page":"3967","DOI":"10.1038\/s41467-019-11951-x","article-title":"Defects in t(6)A tRNA modification due to GON7 and YRDC mutations lead to Galloway-Mowat syndrome","volume":"10","author":"Arrondel","year":"2019","journal-title":"Nat. Commun."},{"key":"2022022611393264900_B29","doi-asserted-by":"crossref","first-page":"545","DOI":"10.1038\/ejhg.2017.30","article-title":"tRNA N6-adenosine threonylcarbamoyltransferase defect due to KAE1\/TCS3 (OSGEP) mutation manifest by neurodegeneration and renal tubulopathy","volume":"25","author":"Edvardson","year":"2017","journal-title":"Eur. J. Hum. Genet."},{"key":"2022022611393264900_B30","doi-asserted-by":"crossref","first-page":"147","DOI":"10.1016\/j.jsb.2011.03.018","article-title":"Strategies for the structural analysis of multi-protein complexes: lessons from the 3D-Repertoire project","volume":"175","author":"Collinet","year":"2011","journal-title":"J. Struct. Biol."},{"key":"2022022611393264900_B31","doi-asserted-by":"crossref","first-page":"1804","DOI":"10.1093\/nar\/gku1397","article-title":"The ATP-mediated formation of the YgjD-YeaZ-YjeE complex is required for the biosynthesis of tRNA t6A in Escherichia coli","volume":"43","author":"Zhang","year":"2015","journal-title":"Nucleic Acids Res."},{"key":"2022022611393264900_B32","doi-asserted-by":"crossref","first-page":"36608","DOI":"10.1074\/jbc.M806745200","article-title":"The CP2 domain of leucyl-tRNA synthetase is crucial for amino acid activation and post-transfer editing","volume":"283","author":"Zhou","year":"2008","journal-title":"J. Biol. 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Clin. Invest."},{"key":"2022022611393264900_B43","doi-asserted-by":"crossref","first-page":"299","DOI":"10.1146\/annurev-genet-110410-132531","article-title":"Human mitochondrial tRNAs: biogenesis, function, structural aspects, and diseases","volume":"45","author":"Suzuki","year":"2011","journal-title":"Annu. Rev. Genet."},{"key":"2022022611393264900_B44","doi-asserted-by":"crossref","first-page":"3266","DOI":"10.1091\/mbc.e02-11-0757","article-title":"Possibility of cytoplasmic pre-tRNA splicing: the yeast tRNA splicing endonuclease mainly localizes on the mitochondria","volume":"14","author":"Yoshihisa","year":"2003","journal-title":"Mol. Biol. Cell"},{"key":"2022022611393264900_B45","doi-asserted-by":"crossref","first-page":"7435","DOI":"10.1073\/pnas.91.16.7435","article-title":"Human cytoplasmic isoleucyl-tRNA synthetase: selective divergence of the anticodon-binding domain and acquisition of a new structural unit","volume":"91","author":"Shiba","year":"1994","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"2022022611393264900_B46","doi-asserted-by":"crossref","first-page":"4488","DOI":"10.1073\/pnas.96.8.4488","article-title":"Genetic dissection of protein-protein interactions in multi-tRNA synthetase complex","volume":"96","author":"Rho","year":"1999","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"2022022611393264900_B47","doi-asserted-by":"crossref","first-page":"e00690-18","DOI":"10.1128\/JB.00690-18","article-title":"tRNA modification profiles and codon-decoding strategies in Methanocaldococcus jannaschii","volume":"201","author":"Yu","year":"2019","journal-title":"J. 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