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Pathogenic mutations in TRMT10A cause intellectual disability, microcephaly, diabetes, and short stature in humans, and generate cytotoxic tRNA fragments in cultured cells; however, it is not clear how TRMT10A supports codon translation or brain functions. Here, we generated Trmt10a null mice and showed that tRNAGln(CUG) and initiator methionine tRNA levels were universally decreased in various tissues; the same was true in a human cell line lacking TRMT10A. Ribosome profiling of mouse brain revealed that dysfunction of TRMT10A causes ribosome slowdown at the Gln(CAG) codon and increases translation of Atf4 due to higher frequency of leaky scanning of its upstream open reading frames. Broadly speaking, translation of a subset of mRNAs, especially those for neuronal structures, is perturbed in the mutant brain. Despite not showing discernable defects in the pancreas, liver, or kidney, Trmt10a null mice showed lower body weight and smaller hippocampal postsynaptic densities, which is associated with defective synaptic plasticity and memory. Taken together, our study provides mechanistic insight into the roles of TRMT10A in the brain, and exemplifies the importance of universal tRNA modification during translation of specific codons.<\/jats:p>","DOI":"10.1093\/nar\/gkae520","type":"journal-article","created":{"date-parts":[[2024,7,2]],"date-time":"2024-07-02T00:02:37Z","timestamp":1719878557000},"page":"9230-9246","source":"Crossref","is-referenced-by-count":21,"title":["TRMT10A dysfunction perturbs codon translation of initiator methionine and glutamine and impairs brain functions in mice"],"prefix":"10.1093","volume":"52","author":[{"given":"Roland","family":"Tresky","sequence":"first","affiliation":[{"name":"Department of Molecular Physiology, Faculty of Life Sciences, Kumamoto University , Kumamoto\u00a0 860-8556 , Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yuta","family":"Miyamoto","sequence":"additional","affiliation":[{"name":"Department of Anatomy and Neurobiology, Faculty of Life 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Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yukie","family":"Takahashi","sequence":"additional","affiliation":[{"name":"Department of Anatomy and Neurobiology, Faculty of Life Sciences, Kumamoto University , Kumamoto\u00a0 860-8556 , Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yoshihiro","family":"Komohara","sequence":"additional","affiliation":[{"name":"Department of Cell Pathology, Faculty of Life Sciences, Kumamoto University , Kumamoto\u00a0 860-8556 , Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Huicong","family":"Ge","sequence":"additional","affiliation":[{"name":"Department of Molecular Physiology, Faculty of Life Sciences, Kumamoto University , Kumamoto\u00a0 860-8556 , Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kayo","family":"Nishiguchi","sequence":"additional","affiliation":[{"name":"Department of Molecular Physiology, Faculty of Life Sciences, Kumamoto University , Kumamoto\u00a0 860-8556 , Japan"},{"name":"Department of Nephrology, Faculty of Life Sciences, Kumamoto University , Kumamoto\u00a0 860-8556 , Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Takaichi","family":"Fukuda","sequence":"additional","affiliation":[{"name":"Department of Anatomy and Neurobiology, Faculty of Life Sciences, Kumamoto University , Kumamoto\u00a0 860-8556 , Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hitomi","family":"Kaneko","sequence":"additional","affiliation":[{"name":"Department of Molecular Physiology, Faculty of Life Sciences, Kumamoto University , Kumamoto\u00a0 860-8556 , Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nobuko","family":"Maeda","sequence":"additional","affiliation":[{"name":"Department of Gastroenterology and Hepatology, Faculty of Life Sciences, Kumamoto University , Kumamoto\u00a0 860-8556 , Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jin","family":"Matsuura","sequence":"additional","affiliation":[{"name":"Department of Molecular Physiology, Faculty of Life Sciences, Kumamoto University , Kumamoto\u00a0 860-8556 , Japan"},{"name":"Department of Neurosurgery, Faculty of Life Sciences, Kumamoto University , Kumamoto\u00a0 860-8556 , Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7724-3754","authenticated-orcid":false,"given":"Shintaro","family":"Iwasaki","sequence":"additional","affiliation":[{"name":"RNA Systems Biochemistry Laboratory, RIKEN Cluster for Pioneering Research , Saitama\u00a0 351-0198 , Japan"},{"name":"Department of Computational Biology and Medical Sciences, Graduate School of Frontier Sciences, The University of Tokyo , Chiba\u00a0 277-8561 , Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kourin","family":"Sakakida","sequence":"additional","affiliation":[{"name":"Department of Molecular Physiology, Faculty of Life Sciences, Kumamoto University , Kumamoto\u00a0 860-8556 , Japan"},{"name":"Department of Metabolic Medicine, Faculty of Life Sciences, Kumamoto University , Kumamoto\u00a0 860-8556 , Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9012-8328","authenticated-orcid":false,"given":"Norifumi","family":"Shioda","sequence":"additional","affiliation":[{"name":"Department of Genomic Neurology, Institute of Molecular Embryology and Genetics, Kumamoto University , Kumamoto\u00a0 860-0811 , Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4843-724X","authenticated-orcid":false,"given":"Fan-Yan","family":"Wei","sequence":"additional","affiliation":[{"name":"Department of Modomics Biology and Medicine, Institute of Development, Aging and Cancer, Tohoku University , Sendai\u00a0 980-8575 , Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5663-2627","authenticated-orcid":false,"given":"Kazuhito","family":"Tomizawa","sequence":"additional","affiliation":[{"name":"Department of Molecular Physiology, Faculty of Life Sciences, Kumamoto University , Kumamoto\u00a0 860-8556 , Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2393-5776","authenticated-orcid":false,"given":"Takeshi","family":"Chujo","sequence":"additional","affiliation":[{"name":"Department of Molecular Physiology, Faculty of Life Sciences, Kumamoto University , Kumamoto\u00a0 860-8556 , Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2024,7,2]]},"reference":[{"key":"2024082703503041600_B1","first-page":"138","article-title":"On protein 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Genet."},{"key":"2024082703503041600_B18","doi-asserted-by":"crossref","first-page":"e1003888","DOI":"10.1371\/journal.pgen.1003888","article-title":"tRNA methyltransferase homolog gene TRMT10A mutation in young onset diabetes and primary microcephaly in humans","volume":"9","author":"Igoillo-Esteve","year":"2013","journal-title":"PLos Genet."},{"key":"2024082703503041600_B19","doi-asserted-by":"crossref","first-page":"e001601","DOI":"10.1136\/bmjdrc-2020-001601","article-title":"tRNA methyltransferase 10 homologue A (TRMT10A) mutation in a Chinese patient with diabetes, insulin resistance, intellectual deficiency and microcephaly","volume":"8","author":"Lin","year":"2020","journal-title":"BMJ Open Diabetes Res Care"},{"key":"2024082703503041600_B20","doi-asserted-by":"crossref","first-page":"912","DOI":"10.12688\/f1000research.7106.1","article-title":"Case Report: compound heterozygous nonsense mutations in TRMT10A are associated with microcephaly, delayed development, and periventricular white matter hyperintensities","volume":"4","author":"Narayanan","year":"2015","journal-title":"F1000Res"},{"key":"2024082703503041600_B21","doi-asserted-by":"crossref","first-page":"90","DOI":"10.4274\/jcrpe.galenos.2021.2021.0110","article-title":"Expanding the Phenotype of TRMT10A Mutations: case Report and a Review of the Existing Cases","volume":"15","author":"Siklar","year":"2023","journal-title":"J. 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