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Androl."},{"issue":"21","key":"10.1016\/j.semcdb.2021.12.003_bib87","doi-asserted-by":"crossref","first-page":"15167","DOI":"10.1074\/jbc.M113.453936","article-title":"Disruption of Ttll5\/Stamp gene (Tubulin tyrosine ligase-like protein 5\/SRC-1 and TIF2 associated modulatory protein gene) in male mice causes sperm malformation and infertility","volume":"288","author":"Lee","year":"2013","journal-title":"J. Biol. Chem."},{"issue":"20","key":"10.1016\/j.semcdb.2021.12.003_bib88","first-page":"4546","article-title":"Mutations in the polyglutamylase gene TTLL5, expressed in photoreceptor cells and spermatozoa, are associated with cone-rod degeneration and reduced male fertility","volume":"25","author":"Bedoni","year":"2016","journal-title":"Hum. Mol. Genet."},{"issue":"14","key":"10.1016\/j.semcdb.2021.12.003_bib89","doi-asserted-by":"crossref","first-page":"2757","DOI":"10.1242\/jcs.185983","article-title":"Ttll9-\/- mice sperm flagella show shortening of doublet 7, reduction of doublet 5 polyglutamylation and a stall in beating","volume":"129","author":"Konno","year":"2016","journal-title":"J. Cell Sci."},{"issue":"19","key":"10.1016\/j.semcdb.2021.12.003_bib90","doi-asserted-by":"crossref","first-page":"3017","DOI":"10.1091\/mbc.e14-06-1072","article-title":"The cytosolic carboxypeptidases CCP2 and CCP3 catalyze posttranslational removal of acidic amino acids","volume":"25","author":"Tort","year":"2014","journal-title":"Mol. Biol. 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Cell Sci."},{"key":"10.1016\/j.semcdb.2021.12.003_bib96","doi-asserted-by":"crossref","first-page":"1962","DOI":"10.1038\/ncomms2962","article-title":"alphaTAT1 is the major alpha-tubulin acetyltransferase in mice","volume":"4","author":"Kalebic","year":"2013","journal-title":"Nat. Commun."},{"issue":"22","key":"10.1016\/j.semcdb.2021.12.003_bib97","doi-asserted-by":"crossref","first-page":"7853","DOI":"10.1073\/pnas.0409626102","article-title":"A vital role of tubulin-tyrosine-ligase for neuronal organization","volume":"102","author":"Erck","year":"2005","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"issue":"20","key":"10.1016\/j.semcdb.2021.12.003_bib98","doi-asserted-by":"crossref","first-page":"3391","DOI":"10.1093\/hmg\/ddz186","article-title":"Defective tubulin detyrosination causes structural brain abnormalities with cognitive deficiency in humans and mice","volume":"28","author":"Pagnamenta","year":"2019","journal-title":"Hum. Mol. 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