{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,11]],"date-time":"2026-09-11T19:13:11Z","timestamp":1789153991353,"version":"build-2803163510"},"reference-count":115,"publisher":"MDPI AG","issue":"9","license":[{"start":{"date-parts":[[2023,5,6]],"date-time":"2023-05-06T00:00:00Z","timestamp":1683331200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100006769","name":"Russian Science Foundation","doi-asserted-by":"publisher","award":["18-14-00291"],"award-info":[{"award-number":["18-14-00291"]}],"id":[{"id":"10.13039\/501100006769","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100006769","name":"Russian Science Foundation","doi-asserted-by":"publisher","award":["075152021601"],"award-info":[{"award-number":["075152021601"]}],"id":[{"id":"10.13039\/501100006769","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100012190","name":"Ministry of Science and Higher Education of the Russian Federation","doi-asserted-by":"publisher","award":["18-14-00291"],"award-info":[{"award-number":["18-14-00291"]}],"id":[{"id":"10.13039\/501100012190","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100012190","name":"Ministry of Science and Higher Education of the Russian Federation","doi-asserted-by":"publisher","award":["075152021601"],"award-info":[{"award-number":["075152021601"]}],"id":[{"id":"10.13039\/501100012190","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>While protein synthesis is vital for the majority of cell types of the human body, diversely differentiated cells require specific translation regulation. This suggests the specialization of translation machinery across tissues and organs. Using transcriptomic data from GTEx, FANTOM, and Gene Atlas, we systematically explored the abundance of transcripts encoding translation factors and aminoacyl-tRNA synthetases (ARSases) in human tissues. We revised a few known and identified several novel translation-related genes exhibiting strict tissue-specific expression. The proteins they encode include eEF1A1, eEF1A2, PABPC1L, PABPC3, eIF1B, eIF4E1B, eIF4ENIF1, and eIF5AL1. Furthermore, our analysis revealed a pervasive tissue-specific relative abundance of translation machinery components (e.g., PABP and eRF3 paralogs, eIF2B and eIF3 subunits, eIF5MPs, and some ARSases), suggesting presumptive variance in the composition of translation initiation, elongation, and termination complexes. These conclusions were largely confirmed by the analysis of proteomic data. Finally, we paid attention to sexual dimorphism in the repertoire of translation factors encoded in sex chromosomes (eIF1A, eIF2\u03b3, and DDX3), and identified the testis and brain as organs with the most diverged expression of translation-associated genes.<\/jats:p>","DOI":"10.3390\/ijms24098361","type":"journal-article","created":{"date-parts":[[2023,5,8]],"date-time":"2023-05-08T03:34:53Z","timestamp":1683516893000},"page":"8361","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":16,"title":["Human Tissues Exhibit Diverse Composition of Translation Machinery"],"prefix":"10.3390","volume":"24","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-6560-8725","authenticated-orcid":false,"given":"Aleksandra S.","family":"Anisimova","sequence":"first","affiliation":[{"name":"Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State University, 119234 Moscow, Russia"},{"name":"Faculty of Bioengineering and Bioinformatics, Lomonosov Moscow State University, 119234 Moscow, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Natalia M.","family":"Kolyupanova","sequence":"additional","affiliation":[{"name":"Faculty of Bioengineering and Bioinformatics, Lomonosov Moscow State University, 119234 Moscow, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nadezhda E.","family":"Makarova","sequence":"additional","affiliation":[{"name":"Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State University, 119234 Moscow, Russia"},{"name":"Faculty of Bioengineering and Bioinformatics, Lomonosov Moscow State University, 119234 Moscow, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Artyom A.","family":"Egorov","sequence":"additional","affiliation":[{"name":"Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State University, 119234 Moscow, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6554-8128","authenticated-orcid":false,"given":"Ivan V.","family":"Kulakovskiy","sequence":"additional","affiliation":[{"name":"Vavilov Institute of General Genetics, Russian Academy of Sciences, 117971 Moscow, Russia"},{"name":"Institute of Protein Research, Russian Academy of Sciences, 142290 Pushchino, Russia"},{"name":"Laboratory of Regulatory Genomics, Institute of Fundamental Medicine and Biology, Kazan Federal University, 420008 Kazan, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1774-8475","authenticated-orcid":false,"given":"Sergey E.","family":"Dmitriev","sequence":"additional","affiliation":[{"name":"Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State University, 119234 Moscow, Russia"},{"name":"Faculty of Bioengineering and Bioinformatics, Lomonosov Moscow State University, 119234 Moscow, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2023,5,6]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"e8503","DOI":"10.15252\/msb.20188503","article-title":"A deep proteome and transcriptome abundance atlas of 29 healthy human tissues","volume":"15","author":"Wang","year":"2019","journal-title":"Mol. Syst. Biol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"642","DOI":"10.1038\/s41586-020-2899-z","article-title":"Transcriptome and translatome co-evolution in mammals","volume":"588","author":"Wang","year":"2020","journal-title":"Nature"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"431","DOI":"10.1038\/s41576-018-0008-z","article-title":"Heterogeneity and specialized functions of translation machinery: From genes to organisms","volume":"19","author":"Genuth","year":"2018","journal-title":"Nat. Rev. Genet."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"31","DOI":"10.1146\/annurev-cellbio-100814-125346","article-title":"Translating the genome in time and space: Specialized ribosomes, RNA regulons, and RNA-binding proteins","volume":"31","author":"Shi","year":"2015","journal-title":"Annu. Rev. Cell Dev. Biol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"612","DOI":"10.1016\/j.tibs.2017.05.004","article-title":"The Growing Toolbox for Protein Synthesis Studies","volume":"42","author":"Iwasaki","year":"2017","journal-title":"Trends Biochem. Sci."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"749","DOI":"10.1016\/j.cell.2008.10.029","article-title":"Application of a translational profiling approach for the comparative analysis of CNS cell types","volume":"135","author":"Doyle","year":"2008","journal-title":"Cell"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"738","DOI":"10.1016\/j.cell.2008.10.028","article-title":"A translational profiling approach for the molecular characterization of CNS cell types","volume":"135","author":"Heiman","year":"2008","journal-title":"Cell"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"13939","DOI":"10.1073\/pnas.0907143106","article-title":"Cell-type-specific isolation of ribosome-associated mRNA from complex tissues","volume":"106","author":"Sanz","year":"2009","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"a032698","DOI":"10.1101\/cshperspect.a032698","article-title":"Ribosome Profiling: Global Views of Translation","volume":"11","author":"Ingolia","year":"2019","journal-title":"Cold Spring Harb. Perspect. Biol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"10924","DOI":"10.1523\/JNEUROSCI.0084-14.2014","article-title":"Ribosome profiling reveals a cell-type-specific translational landscape in brain tumors","volume":"34","author":"Gonzalez","year":"2014","journal-title":"J. Neurosci. Off. J. Soc. Neurosci."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"147","DOI":"10.1038\/nmeth.3208","article-title":"Quantitative profiling of initiating ribosomes in vivo","volume":"12","author":"Gao","year":"2015","journal-title":"Nat. Methods"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"15581","DOI":"10.1073\/pnas.2001788117","article-title":"Multifaceted deregulation of gene expression and protein synthesis with age","volume":"117","author":"Anisimova","year":"2020","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"e9","DOI":"10.1093\/nar\/gkaa1103","article-title":"Translation elongation rate varies among organs and decreases with age","volume":"49","author":"Gerashchenko","year":"2021","journal-title":"Nucleic Acids Res."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"224","DOI":"10.1016\/j.cels.2015.08.012","article-title":"Integrated Transcriptome and Proteome Analyses Reveal Organ-Specific Proteome Deterioration in Old Rats","volume":"1","author":"Ori","year":"2015","journal-title":"Cell Syst."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"116","DOI":"10.1186\/s13059-017-1222-2","article-title":"Translational contributions to tissue specificity in rhythmic and constitutive gene expression","volume":"18","author":"Arpat","year":"2017","journal-title":"Genome Biol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"e9275","DOI":"10.15252\/msb.20199275","article-title":"Translational efficiency across healthy and tumor tissues is proliferation-related","volume":"16","author":"Benisty","year":"2020","journal-title":"Mol. Syst. Biol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"3369","DOI":"10.1016\/j.jmb.2020.01.011","article-title":"TissueCoCoPUTs: Novel Human Tissue-Specific Codon and Codon-Pair Usage Tables Based on Differential Tissue Gene Expression","volume":"432","author":"Kames","year":"2020","journal-title":"J. Mol. Biol."},{"key":"ref_18","doi-asserted-by":"crossref","unstructured":"Karki, P., Carney, T.D., Maracci, C., Yatsenko, A.S., Shcherbata, H.R., and Rodnina, M.V. (2020). Tissue-Specific Regulation of Translational Readthrough Tunes Functions of the Traffic Jam Transcription Factor. bioRxiv.","DOI":"10.1101\/2020.12.04.411694"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"1004","DOI":"10.1261\/rna.043653.113","article-title":"Ribosome-omics of the human ribosome","volume":"20","author":"Gupta","year":"2014","journal-title":"Rna"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"236","DOI":"10.1186\/s13059-016-1104-z","article-title":"Patterns of ribosomal protein expression specify normal and malignant human cells","volume":"17","author":"Guimaraes","year":"2016","journal-title":"Genome Biol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"383","DOI":"10.1016\/j.cell.2011.03.028","article-title":"Ribosome-mediated specificity in Hox mRNA translation and vertebrate tissue patterning","volume":"145","author":"Kondrashov","year":"2011","journal-title":"Cell"},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Dittmar, K.A., Goodenbour, J.M., and Pan, T. (2006). Tissue-specific differences in human transfer RNA expression. PLoS Genet., 2.","DOI":"10.1371\/journal.pgen.0020221"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"2964","DOI":"10.1093\/nar\/gkq009","article-title":"Translation efficiency in humans: Tissue specificity, global optimization and differences between developmental stages","volume":"38","author":"Waldman","year":"2010","journal-title":"Nucleic Acids Res."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"24064","DOI":"10.1016\/S0021-9258(18)35946-5","article-title":"Tissue-specific expression in mammalian brain, heart, and muscle of S1, a member of the elongation factor-1 alpha gene family","volume":"267","author":"Lee","year":"1992","journal-title":"J. Biol. Chem."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"22915","DOI":"10.1074\/jbc.M101011200","article-title":"Characterization of elongation factor-1A (eEF1A-1) and eEF1A-2\/S1 protein expression in normal and wasted mice","volume":"276","author":"Khalyfa","year":"2001","journal-title":"J. Biol. Chem."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"1872","DOI":"10.1093\/nar\/29.9.1872","article-title":"Human testis expresses a specific poly(A)-binding protein","volume":"29","author":"Feral","year":"2001","journal-title":"Nucleic Acids Res."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"367","DOI":"10.1073\/pnas.0408378102","article-title":"An embryonic poly(A)-binding protein (ePAB) is expressed in mouse oocytes and early preimplantation embryos","volume":"102","author":"Seli","year":"2005","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1093\/molehr\/gat061","article-title":"Human embryonic poly(A)-binding protein (EPAB) alternative splicing is differentially regulated in human oocytes and embryos","volume":"20","author":"Lalioti","year":"2014","journal-title":"Mol. Hum. Reprod."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"101","DOI":"10.1006\/geno.2000.6418","article-title":"Human eIF5A2 on chromosome 3q25-q27 is a phylogenetically conserved vertebrate variant of eukaryotic translation initiation factor 5A with tissue-specific expression","volume":"71","author":"Jenkins","year":"2001","journal-title":"Genomics"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"111","DOI":"10.1007\/s00427-008-0268-2","article-title":"Evolutionary origin and phylogenetic analysis of the novel oocyte-specific eukaryotic translation initiation factor 4E in Tetrapoda","volume":"219","author":"Evsikov","year":"2009","journal-title":"Dev. Genes Evol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"146","DOI":"10.1016\/j.modgep.2005.06.011","article-title":"Sexually dimorphic expression of the X-linked gene Eif2s3x mRNA but not protein in mouse brain","volume":"6","author":"Xu","year":"2006","journal-title":"Gene Expr. Patterns"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"91","DOI":"10.1016\/S0378-1119(03)00742-X","article-title":"Promoter analysis of the human translation termination factor 1 gene","volume":"316","author":"Dubourg","year":"2003","journal-title":"Gene"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"27","DOI":"10.1016\/S0300-9084(97)87622-5","article-title":"Expression of the release factor eRF1 (Sup45p) gene of higher eukaryotes in yeast and mammalian tissues","volume":"79","author":"Urbero","year":"1997","journal-title":"Biochimie"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"16934","DOI":"10.1074\/jbc.271.28.16934","article-title":"Characterization of multiple mRNAs that encode mammalian translation initiation factor 5 (eIF-5)","volume":"271","author":"Si","year":"1996","journal-title":"J. Biol. Chem."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"22254","DOI":"10.1074\/jbc.273.35.22254","article-title":"Molecular cloning of a novel member of the eukaryotic polypeptide chain-releasing factors (eRF). Its identification as eRF3 interacting with eRF1","volume":"273","author":"Hoshino","year":"1998","journal-title":"J. Biol. Chem."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"5801","DOI":"10.1128\/MCB.25.14.5801-5811.2005","article-title":"Involvement of human release factors eRF3a and eRF3b in translation termination and regulation of the termination complex formation","volume":"25","author":"Chauvin","year":"2005","journal-title":"Mol. Cell. Biol."},{"key":"ref_37","doi-asserted-by":"crossref","unstructured":"Cao, Y., Portela, M., Janikiewicz, J., Doig, J., and Abbott, C.M. (2014). Characterisation of translation elongation factor eEF1B subunit expression in mammalian cells and tissues and co-localisation with eEF1A2. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0114117"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"673","DOI":"10.1038\/embor.2011.82","article-title":"Transformation of eEF1Bdelta into heat-shock response transcription factor by alternative splicing","volume":"12","author":"Kaitsuka","year":"2011","journal-title":"EMBO Rep."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"119","DOI":"10.1016\/0014-5793(94)01403-N","article-title":"A mitochondrial elongation factor-like protein is over-expressed in tumours and differentially expressed in normal tissues","volume":"358","author":"Wells","year":"1995","journal-title":"FEBS Lett."},{"key":"ref_40","first-page":"37","article-title":"Differential and Tissue-specific Expression of Mitochondrial Elongation Factor Tu and Ts during Development","volume":"31","author":"Chen","year":"1999","journal-title":"Sheng Wu Hua Xue Yu Sheng Wu Wu Li Xue Bao"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"594","DOI":"10.1016\/j.cmet.2019.06.002","article-title":"Metabolite Exchange between Mammalian Organs Quantified in Pigs","volume":"30","author":"Jang","year":"2019","journal-title":"Cell Metab."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"417","DOI":"10.1016\/j.cmet.2018.10.013","article-title":"Quantitative Analysis of the Whole-Body Metabolic Fate of Branched-Chain Amino Acids","volume":"29","author":"Neinast","year":"2019","journal-title":"Cell Metab."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"141","DOI":"10.1038\/s42255-021-00517-1","article-title":"Circulating metabolite homeostasis achieved through mass action","volume":"4","author":"Li","year":"2022","journal-title":"Nat. Metab."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"1709","DOI":"10.1074\/mcp.M112.024919","article-title":"Initial quantitative proteomic map of 28 mouse tissues using the SILAC mouse","volume":"12","author":"Geiger","year":"2013","journal-title":"Mol. Cell. Proteom."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"779","DOI":"10.1146\/annurev-biochem-060713-035802","article-title":"The scanning mechanism of eukaryotic translation initiation","volume":"83","author":"Hinnebusch","year":"2014","journal-title":"Annu. Rev. Biochem."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"75","DOI":"10.3389\/fonc.2015.00075","article-title":"The eEF1A Proteins: At the Crossroads of Oncogenesis, Apoptosis, and Viral Infections","volume":"5","author":"Abbas","year":"2015","journal-title":"Front. Oncol."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"100067","DOI":"10.1016\/j.bbadva.2022.100067","article-title":"The eEF1 family of mammalian translation elongation factors","volume":"3","author":"Negrutskii","year":"2023","journal-title":"BBA Adv."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"24453","DOI":"10.1016\/S0021-9258(20)80547-X","article-title":"Differential expression of S1 and elongation factor-1 alpha during rat development","volume":"268","author":"Lee","year":"1993","journal-title":"J. Biol. Chem."},{"key":"ref_49","unstructured":"(2023, March 05). \u201cChromosome Y: Chromosome Summary\u2014Homo Sapiens\u201d. Ensembl Release 88. 2017-03-29. Available online: https:\/\/grch37.ensembl.org\/Homo_sapiens\/Location\/Chromosome?r=Y."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"400","DOI":"10.1038\/nature03479","article-title":"X-inactivation profile reveals extensive variability in X-linked gene expression in females","volume":"434","author":"Carrel","year":"2005","journal-title":"Nature"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"494","DOI":"10.1038\/nature13206","article-title":"Mammalian Y chromosomes retain widely expressed dosage-sensitive regulators","volume":"508","author":"Bellott","year":"2014","journal-title":"Nature"},{"key":"ref_52","doi-asserted-by":"crossref","unstructured":"Berletch, J.B., Ma, W., Yang, F., Shendure, J., Noble, W.S., Disteche, C.M., and Deng, X. (2015). Escape from X inactivation varies in mouse tissues. PLoS Genet., 11.","DOI":"10.1371\/journal.pgen.1005079"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"343","DOI":"10.3109\/10409238.2014.931339","article-title":"The Ded1\/DDX3 subfamily of DEAD-box RNA helicases","volume":"49","author":"Sharma","year":"2014","journal-title":"Crit. Rev. Biochem. Mol. Biol."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"2517","DOI":"10.2174\/092986707782023677","article-title":"The DDX3 subfamily of the DEAD box helicases: Divergent roles as unveiled by studying different organisms and in vitro assays","volume":"14","author":"Rosner","year":"2007","journal-title":"Curr. Med. Chem."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"213","DOI":"10.1016\/j.yexcr.2004.07.005","article-title":"Human DDX3Y, the Y-encoded isoform of RNA helicase DDX3, rescues a hamster temperature-sensitive ET24 mutant cell line with a DDX3X mutation","volume":"300","author":"Sekiguchi","year":"2004","journal-title":"Exp. Cell Res."},{"key":"ref_56","doi-asserted-by":"crossref","unstructured":"Venkataramanan, S., Calviello, L., Wilkins, K., and Floor, S.N. (2020). DDX3X and DDX3Y are redundant in protein synthesis. bioRxiv.","DOI":"10.1101\/2020.09.30.319376"},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"46","DOI":"10.5582\/bst.2016.01216","article-title":"Progress in understanding the molecular functions of DDX3Y (DBY) in male germ cell development and maintenance","volume":"11","author":"Kotov","year":"2017","journal-title":"Biosci. Trends"},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"15041","DOI":"10.1038\/srep15041","article-title":"DDX3Y gene rescue of a Y chromosome AZFa deletion restores germ cell formation and transcriptional programs","volume":"5","author":"Ramathal","year":"2015","journal-title":"Sci. Rep."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"121","DOI":"10.1262\/jrd.2018-145","article-title":"An azoospermic factor gene, Ddx3y and its paralog, Ddx3x are dispensable in germ cells for male fertility","volume":"65","author":"Matsumura","year":"2019","journal-title":"J. Reprod. Dev."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"404","DOI":"10.1016\/j.neuron.2020.01.042","article-title":"Pathogenic DDX3X Mutations Impair RNA Metabolism and Neurogenesis during Fetal Cortical Development","volume":"106","author":"Lennox","year":"2020","journal-title":"Neuron"},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"1725","DOI":"10.1093\/hmg\/7.11.1725","article-title":"Characterization of genes encoding translation initiation factor eIF-2gamma in mouse and human: Sex chromosome localization, escape from X-inactivation and evolution","volume":"7","author":"Ehrmann","year":"1998","journal-title":"Hum. Mol. Genet."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"69","DOI":"10.1126\/science.1242544","article-title":"Two Y genes can replace the entire Y chromosome for assisted reproduction in the mouse","volume":"343","author":"Yamauchi","year":"2014","journal-title":"Science"},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"409","DOI":"10.1002\/humu.23170","article-title":"EIF2S3 Mutations Associated with Severe X-Linked Intellectual Disability Syndrome MEHMO","volume":"38","author":"Skopkova","year":"2017","journal-title":"Hum. Mutat."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"605","DOI":"10.1007\/s00439-020-02143-5","article-title":"A genomics approach to females with infertility and recurrent pregnancy loss","volume":"139","author":"Maddirevula","year":"2020","journal-title":"Hum. Genet."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"47","DOI":"10.1042\/BJ20120467","article-title":"Embryonic poly(A)-binding protein (EPAB) is required for oocyte maturation and female fertility in mice","volume":"446","author":"Lalioti","year":"2012","journal-title":"Biochem. J."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"335","DOI":"10.1007\/s10815-016-0654-z","article-title":"The poly(A)-binding protein genes, EPAB, PABPC1, and PABPC3 are differentially expressed in infertile men with non-obstructive azoospermia","volume":"33","author":"Ozturk","year":"2016","journal-title":"J. Assist. Reprod. Genet."},{"key":"ref_67","doi-asserted-by":"crossref","unstructured":"Xie, J., Wei, X., and Chen, Y. (2021). Loss of PABPC1 is compensated by elevated PABPC4 and correlates with transcriptome changes. bioRxiv.","DOI":"10.1101\/2021.02.07.430165"},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1006\/geno.2001.6530","article-title":"A novel poly(A)-binding protein gene (PABPC5) maps to an X-specific subinterval in the Xq21.3\/Yp11.2 homology block of the human sex chromosomes","volume":"74","author":"Blanco","year":"2001","journal-title":"Genomics"},{"key":"ref_69","unstructured":"Kinney, J.M., and Tucker, H.N. (1992). Energy Metabolism: Tissue Determinants and Cellular Corollaries, Raven Press."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"1226","DOI":"10.1101\/gad.314724.118","article-title":"Functions of unconventional mammalian translational GTPases GTPBP1 and GTPBP2","volume":"32","author":"Zinoviev","year":"2018","journal-title":"Genes Dev."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"455","DOI":"10.1126\/science.1249749","article-title":"RNA function. Ribosome stalling induced by mutation of a CNS-specific tRNA causes neurodegeneration","volume":"345","author":"Ishimura","year":"2014","journal-title":"Science"},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"360","DOI":"10.1006\/bbrc.1997.6103","article-title":"Identification of human and mouse GP-1, a putative member of a novel G-protein family","volume":"231","author":"Senju","year":"1997","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1016\/S0378-1119(00)00346-2","article-title":"Cloning, expression analysis, and chromosomal mapping of GTPBP2, a novel member of the G protein family","volume":"256","author":"Watanabe","year":"2000","journal-title":"Gene"},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1042\/BJ20111765","article-title":"Multiple isoforms of the translation initiation factor eIF4GII are generated via use of alternative promoters, splice sites and a non-canonical initiation codon","volume":"448","author":"Coldwell","year":"2012","journal-title":"Biochem. J."},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"334","DOI":"10.1128\/MCB.18.1.334","article-title":"A novel functional human eukaryotic translation initiation factor 4G","volume":"18","author":"Gradi","year":"1998","journal-title":"Mol. Cell. Biol."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"865","DOI":"10.1016\/j.mod.2005.04.002","article-title":"Functional diversity of the eukaryotic translation initiation factors belonging to eIF4 families","volume":"122","author":"Hernandez","year":"2005","journal-title":"Mech. Dev."},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"1699","DOI":"10.1242\/dev.043125","article-title":"Mutation of Eif4g3, encoding a eukaryotic translation initiation factor, causes male infertility and meiotic arrest of mouse spermatocytes","volume":"137","author":"Sun","year":"2010","journal-title":"Development"},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"164","DOI":"10.3109\/10409238.2014.887051","article-title":"Transcriptome-wide studies uncover the diversity of modes of mRNA recruitment to eukaryotic ribosomes","volume":"49","author":"Shatsky","year":"2014","journal-title":"Crit. Rev. Biochem. Mol. Biol."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"1234","DOI":"10.1042\/BST20150164","article-title":"eIF2B: Recent structural and functional insights into a key regulator of translation","volume":"43","author":"Wortham","year":"2015","journal-title":"Biochem. Soc. Trans."},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"571","DOI":"10.1042\/BJ20150828","article-title":"Stoichiometry of the eIF2B complex is maintained by mutual stabilization of subunits","volume":"473","author":"Wortham","year":"2016","journal-title":"Biochem. J."},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"403","DOI":"10.1093\/jmcb\/mjaa018","article-title":"eIF-Three to Tango: Emerging functions of translation initiation factor eIF3 in protein synthesis and disease","volume":"12","author":"Wolf","year":"2020","journal-title":"J. Mol. Cell Biol."},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"20160176","DOI":"10.1098\/rstb.2016.0176","article-title":"Human eIF3: From \u2018blobology\u2019 to biological insight","volume":"372","author":"Cate","year":"2017","journal-title":"Philos. Trans. R. Soc. B"},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"10948","DOI":"10.1093\/nar\/gkx805","article-title":"Embraced by eIF3: Structural and functional insights into the roles of eIF3 across the translation cycle","volume":"45","author":"Valasek","year":"2017","journal-title":"Nucleic Acids Res."},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"387","DOI":"10.1016\/j.jmb.2014.11.009","article-title":"Distinct features of cap binding by eIF4E1b proteins","volume":"427","author":"Kubacka","year":"2015","journal-title":"J. Mol. Biol."},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"37389","DOI":"10.1074\/jbc.M704629200","article-title":"CPEB interacts with an ovary-specific eIF4E and 4E-T in early Xenopus oocytes","volume":"282","author":"Minshall","year":"2007","journal-title":"J. Biol. Chem."},{"key":"ref_86","doi-asserted-by":"crossref","unstructured":"Yang, G., Xin, Q., Feng, I., and Dean, J. (2022). Germ-cell specific eIF4E1B regulates maternal RNA translation to ensure zygotic genome activation. bioRxiv.","DOI":"10.1101\/2022.07.27.501690"},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"64","DOI":"10.1186\/s13578-021-00577-6","article-title":"The role of CPEB family proteins in the nervous system function in the norm and pathology","volume":"11","author":"Kozlov","year":"2021","journal-title":"Cell Biosci."},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"3298","DOI":"10.1093\/nar\/gkt1265","article-title":"Human 4E-T represses translation of bound mRNAs and enhances microRNA-mediated silencing","volume":"42","author":"Kamenska","year":"2014","journal-title":"Nucleic Acids Res."},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"3142","DOI":"10.1093\/emboj\/19.12.3142","article-title":"A novel shuttling protein, 4E-T, mediates the nuclear import of the mRNA 5\u2032 cap-binding protein, eIF4E","volume":"19","author":"Dostie","year":"2000","journal-title":"EMBO J."},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"1102","DOI":"10.1111\/j.1742-4658.2006.05135.x","article-title":"Differential expression of eIF5A-1 and eIF5A-2 in human cancer cells","volume":"273","author":"Clement","year":"2006","journal-title":"FEBS J."},{"key":"ref_91","doi-asserted-by":"crossref","unstructured":"Loughran, G., Firth, A.E., Atkins, J.F., and Ivanov, I.P. (2018). Translational autoregulation of BZW1 and BZW2 expression by modulating the stringency of start codon selection. PLoS ONE, 13.","DOI":"10.1371\/journal.pone.0192648"},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"7997","DOI":"10.1093\/nar\/gkx469","article-title":"eIF1 modulates the recognition of suboptimal translation initiation sites and steers gene expression via uORFs","volume":"45","author":"Fijalkowska","year":"2017","journal-title":"Nucleic Acids Res."},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"174","DOI":"10.1016\/j.gene.2018.02.013","article-title":"Translation control of mRNAs encoding mammalian translation initiation factors","volume":"651","author":"Andreev","year":"2018","journal-title":"Gene"},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"18056","DOI":"10.1073\/pnas.1009269107","article-title":"Initiation context modulates autoregulation of eukaryotic translation initiation factor 1 (eIF1)","volume":"107","author":"Ivanov","year":"2010","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_95","doi-asserted-by":"crossref","first-page":"526","DOI":"10.1038\/s41580-018-0011-4","article-title":"Roadblocks and resolutions in eukaryotic translation","volume":"19","author":"Schuller","year":"2018","journal-title":"Nat. Reviews. Mol. Cell Biol."},{"key":"ref_96","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.celrep.2016.08.088","article-title":"Dynamic Regulation of a Ribosome Rescue Pathway in Erythroid Cells and Platelets","volume":"17","author":"Mills","year":"2016","journal-title":"Cell Rep."},{"key":"ref_97","doi-asserted-by":"crossref","unstructured":"O\u2019Connell, A.E., Gerashchenko, M.V., O\u2019Donohue, M.F., Rosen, S.M., Huntzinger, E., Gleeson, D., Galli, A., Ryder, E., Cao, S., and Murphy, Q. (2019). Mammalian Hbs1L deficiency causes congenital anomalies and developmental delay associated with Pelota depletion and 80S monosome accumulation. PLoS Genet., 15.","DOI":"10.1371\/journal.pgen.1007917"},{"key":"ref_98","doi-asserted-by":"crossref","first-page":"6053","DOI":"10.1074\/jbc.M809636200","article-title":"Dissection of the structural organization of the aminoacyl-tRNA synthetase complex","volume":"284","author":"Kaminska","year":"2009","journal-title":"J. Biol. Chem."},{"key":"ref_99","doi-asserted-by":"crossref","first-page":"556","DOI":"10.1006\/bbrc.1995.1696","article-title":"A novel gene oriented in a head-to-head configuration with the human histidyl-tRNA synthetase (HRS) gene encodes an mRNA that predicts a polypeptide homologous to HRS","volume":"210","author":"Raben","year":"1995","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"ref_100","doi-asserted-by":"crossref","first-page":"3643","DOI":"10.1093\/nar\/gky211","article-title":"A threonyl-tRNA synthetase-like protein has tRNA aminoacylation and editing activities","volume":"46","author":"Chen","year":"2018","journal-title":"Nucleic Acids Res."},{"key":"ref_101","doi-asserted-by":"crossref","first-page":"6062","DOI":"10.1073\/pnas.0400782101","article-title":"A gene atlas of the mouse and human protein-encoding transcriptomes","volume":"101","author":"Su","year":"2004","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_102","doi-asserted-by":"crossref","first-page":"1152","DOI":"10.1093\/bioinformatics\/17.12.1152","article-title":"Differential expression of genes coding for ribosomal proteins in different human tissues","volume":"17","author":"Bortoluzzi","year":"2001","journal-title":"Bioinformatics"},{"key":"ref_103","doi-asserted-by":"crossref","first-page":"eaao0665","DOI":"10.1126\/sciadv.aao0665","article-title":"Variant ribosomal RNA alleles are conserved and exhibit tissue-specific expression","volume":"4","author":"Parks","year":"2018","journal-title":"Sci. Adv."},{"key":"ref_104","doi-asserted-by":"crossref","first-page":"95","DOI":"10.1016\/j.tibs.2018.10.009","article-title":"Ribosome Stoichiometry: From Form to Function","volume":"44","author":"Emmott","year":"2019","journal-title":"Trends Biochem. Sci."},{"key":"ref_105","doi-asserted-by":"crossref","first-page":"865","DOI":"10.1016\/j.celrep.2015.09.056","article-title":"Differential Stoichiometry among Core Ribosomal Proteins","volume":"13","author":"Slavov","year":"2015","journal-title":"Cell Rep."},{"key":"ref_106","doi-asserted-by":"crossref","first-page":"355","DOI":"10.1038\/nrm3359","article-title":"Specialized ribosomes: A new frontier in gene regulation and organismal biology","volume":"13","author":"Xue","year":"2012","journal-title":"Nat. Reviews. Mol. Cell Biol."},{"key":"ref_107","doi-asserted-by":"crossref","first-page":"234","DOI":"10.1038\/s42003-018-0239-8","article-title":"Global analysis of tRNA and translation factor expression reveals a dynamic landscape of translational regulation in human cancers","volume":"1","author":"Zhang","year":"2018","journal-title":"Commun. Biol."},{"key":"ref_108","doi-asserted-by":"crossref","first-page":"20","DOI":"10.1186\/2049-3002-1-20","article-title":"The metabolic demands of cancer cells are coupled to their size and protein synthesis rates","volume":"1","author":"Dolfi","year":"2013","journal-title":"Cancer Metab."},{"key":"ref_109","doi-asserted-by":"crossref","first-page":"762","DOI":"10.1016\/j.tcb.2022.03.006","article-title":"Moonlighting translation factors: Multifunctionality drives diverse gene regulation","volume":"32","author":"Farache","year":"2022","journal-title":"Trends Cell Biol."},{"key":"ref_110","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1146\/annurev-neuro-071013-014100","article-title":"Translational control in synaptic plasticity and cognitive dysfunction","volume":"37","author":"Buffington","year":"2014","journal-title":"Annu. Rev. Neurosci."},{"key":"ref_111","doi-asserted-by":"crossref","first-page":"507","DOI":"10.1134\/S0026893321030080","article-title":"mRNA Targeting, Transport and Local Translation in Eukaryotic Cells: From the Classical View to a Diversity of New Concepts","volume":"55","author":"Lashkevich","year":"2021","journal-title":"Mol. Biol."},{"key":"ref_112","doi-asserted-by":"crossref","unstructured":"Allen, S.R., Stewart, R.K., Rogers, M., Ruiz, I.J., Cohen, E., Laederach, A., Counter, C.M., Sawyer, J.K., and Fox, D.T. (2022). Distinct responses to rare codons in select Drosophila tissues. bioRxiv.","DOI":"10.7554\/eLife.76893.sa2"},{"key":"ref_113","doi-asserted-by":"crossref","unstructured":"Hernandez-Alias, X., Benisty, H., Serrano, L., and Schaefer, M.H. (2022). Using protein-per-mRNA differences among human tissues in codon optimization. bioRxiv.","DOI":"10.1101\/2022.03.22.485268"},{"key":"ref_114","doi-asserted-by":"crossref","first-page":"535","DOI":"10.1016\/j.cell.2016.03.014","article-title":"On the Dependency of Cellular Protein Levels on mRNA Abundance","volume":"165","author":"Liu","year":"2016","journal-title":"Cell"},{"key":"ref_115","unstructured":"Sergushichev, A.A. (2016). An algorithm for fast preranked gene set enrichment analysis using cumulative statistic calculation. bioRxiv."}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/24\/9\/8361\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T19:30:25Z","timestamp":1760124625000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/24\/9\/8361"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,5,6]]},"references-count":115,"journal-issue":{"issue":"9","published-online":{"date-parts":[[2023,5]]}},"alternative-id":["ijms24098361"],"URL":"https:\/\/doi.org\/10.3390\/ijms24098361","relation":{"has-preprint":[{"id-type":"doi","id":"10.1101\/2023.01.16.524297","asserted-by":"object"}]},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,5,6]]}}}