{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,29]],"date-time":"2026-09-29T05:35:20Z","timestamp":1790660120752,"version":"4.1.0"},"reference-count":94,"publisher":"Oxford University Press (OUP)","issue":"1","license":[{"start":{"date-parts":[[2024,10,14]],"date-time":"2024-10-14T00:00:00Z","timestamp":1728864000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100000925","name":"National Health and Medical Research Council","doi-asserted-by":"publisher","award":["1074258"],"award-info":[{"award-number":["1074258"]}],"id":[{"id":"10.13039\/501100000925","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000925","name":"NHMRC","doi-asserted-by":"publisher","award":["1054432"],"award-info":[{"award-number":["1054432"]}],"id":[{"id":"10.13039\/501100000925","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000925","name":"NHMRC","doi-asserted-by":"publisher","award":["1062854"],"award-info":[{"award-number":["1062854"]}],"id":[{"id":"10.13039\/501100000925","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Norman Beischer Scientific Fellowship"},{"name":"Melbourne International Research Scholarship"},{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","award":["R01GM099790"],"award-info":[{"award-number":["R01GM099790"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","award":["R35GM141710"],"award-info":[{"award-number":["R35GM141710"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2025,1,14]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:p>Premature ovarian insufficiency (POI) is characterized by the loss or complete absence of ovarian activity in women under the age of 40. Clinical presentation of POI varies with phenotypic severity ranging from premature loss of menses to complete gonadal dysgenesis. POI is genetically heterogeneous with &amp;gt;100 causative gene variants identified thus far. The etiology of POI varies from syndromic, idiopathic, monogenic to autoimmune causes the condition. Genetic diagnoses are beneficial to those impacted by POI as it allows for improved clinical management and fertility preservation. Identifying novel variants in candidate POI genes, however, is insufficient to make clinical diagnoses. The impact of missense variants can be predicted using bioinformatic algorithms but computational approaches have limitations and can generate false positive and false negative predictions. Functional characterization of missense variants, is therefore imperative, particularly for genes lacking a well-established genotype:phenotype correlation. Here we used whole-exome sequencing (WES) to identify the first case of a homozygous missense variant in DIS3 (c.2320C\u2009&amp;gt;\u2009T; p.His774Tyr) a critical component of the RNA exosome in a POI patient. This adds to the previously described compound heterozygous patient. We perform the first functional characterization of a human POI-associated DIS3 variant. A slight defect in mitotic growth was caused by the variant in a Saccharomyces cerevisiae model. Transgenic rescue of Dis3 knockdown in Drosophila melanogaster with human DIS3 carrying the patient variant led to aberrant ovarian development and egg chamber degeneration. This supports a potential deleterious impact of the human c.2320C\u2009&amp;gt;\u2009T; p.His774Tyr variant.<\/jats:p>","DOI":"10.1093\/biolre\/ioae148","type":"journal-article","created":{"date-parts":[[2024,10,14]],"date-time":"2024-10-14T11:51:53Z","timestamp":1728906713000},"page":"102-118","source":"Crossref","is-referenced-by-count":6,"title":["Functional characterization of human recessive <i>DIS3<\/i> variants in premature ovarian insufficiency"],"prefix":"10.1093","volume":"112","author":[{"given":"Brianna L","family":"Kline","sequence":"first","affiliation":[{"name":"Murdoch Children's Research Institute, Royal Children's Hospital , 50 Flemington Rd, Parkville VIC 3052, Melbourne ,","place":["Australia"]},{"name":"Department of Paediatrics, The University of Melbourne , Grattan Street, Parkville, VIC 3010, Melbourne ,","place":["Australia"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nicole A","family":"Siddall","sequence":"additional","affiliation":[{"name":"Department of Anatomy and Physiology, The University of Melbourne , Grattan Street, Parkville, VIC 3010, Melbourne ,","place":["Australia"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Fernando","family":"Wijaya","sequence":"additional","affiliation":[{"name":"Department of Anatomy and Physiology, The University of Melbourne , Grattan Street, Parkville, VIC 3010, Melbourne ,","place":["Australia"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Catherine J","family":"Stuart","sequence":"additional","affiliation":[{"name":"Department of Microbiology and Molecular Genetics, University of Texas Health Science Center at Houston , 7000 Fannin, Suite 1706, Houston, TX 77030 ,","place":["USA"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Luisa","family":"Orlando","sequence":"additional","affiliation":[{"name":"Department of Microbiology and Molecular Genetics, University of Texas Health Science Center at Houston , 7000 Fannin, Suite 1706, Houston, TX 77030 ,","place":["USA"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shabnam","family":"Bakhshalizadeh","sequence":"additional","affiliation":[{"name":"Murdoch Children's Research Institute, Royal Children's Hospital , 50 Flemington Rd, Parkville VIC 3052, Melbourne ,","place":["Australia"]},{"name":"Department of Paediatrics, The University of Melbourne , Grattan Street, Parkville, VIC 3010, Melbourne ,","place":["Australia"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Fateme","family":"Afkhami","sequence":"additional","affiliation":[{"name":"Department of Medical Genetics , Faculty of Medical Sciences, , Tehran Province, Tehran, Jalal Al Ahmad St, P9CJ+HC9 ,","place":["Iran"]},{"name":"Tarbiat Modares University , Faculty of Medical Sciences, , Tehran Province, Tehran, Jalal Al Ahmad St, P9CJ+HC9 ,","place":["Iran"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Katrina M","family":"Bell","sequence":"additional","affiliation":[{"name":"Murdoch Children's Research Institute, Royal Children's Hospital , 50 Flemington Rd, Parkville VIC 3052, Melbourne ,","place":["Australia"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sylvie","family":"Jaillard","sequence":"additional","affiliation":[{"name":"Murdoch Children's Research Institute, Royal Children's Hospital , 50 Flemington Rd, Parkville VIC 3052, Melbourne ,","place":["Australia"]},{"name":"INSERM , Institut de Recherche en Sant\u00e9, Environement et Travail, , 9 Av. du Professeur L\u00e9on Bernard, 35000, Rennes ,","place":["France"]},{"name":"University of Rennes , Institut de Recherche en Sant\u00e9, Environement et Travail, , 9 Av. du Professeur L\u00e9on Bernard, 35000, Rennes ,","place":["France"]},{"name":"CHU Rennes, Service de Cytog\u00e9n\u00e9tique et Biologie Cellulaire , 2 rue Henri Le Guilloux, 35033 Rennes CEDEX 9F-35033 ,","place":["France"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Gorjana","family":"Robevska","sequence":"additional","affiliation":[{"name":"Murdoch Children's Research Institute, Royal Children's Hospital , 50 Flemington Rd, Parkville VIC 3052, Melbourne ,","place":["Australia"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jocelyn A","family":"van den Bergen","sequence":"additional","affiliation":[{"name":"Murdoch Children's Research Institute, Royal Children's Hospital , 50 Flemington Rd, Parkville VIC 3052, Melbourne ,","place":["Australia"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shirin","family":"Shahbazi","sequence":"additional","affiliation":[{"name":"Department of Medical Genetics , Faculty of Medical Sciences, , Tehran Province, Tehran, Jalal Al Ahmad St, P9CJ+HC9 ,","place":["Iran"]},{"name":"Tarbiat Modares University , Faculty of Medical Sciences, , Tehran Province, Tehran, Jalal Al Ahmad St, P9CJ+HC9 ,","place":["Iran"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ambro","family":"van Hoof","sequence":"additional","affiliation":[{"name":"Department of Microbiology and Molecular Genetics, University of Texas Health Science Center at Houston , 7000 Fannin, Suite 1706, Houston, TX 77030 ,","place":["USA"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Katie L","family":"Ayers","sequence":"additional","affiliation":[{"name":"Murdoch Children's Research Institute, Royal Children's Hospital , 50 Flemington Rd, Parkville VIC 3052, Melbourne ,","place":["Australia"]},{"name":"Department of Paediatrics, The University of Melbourne , Grattan Street, Parkville, VIC 3010, Melbourne ,","place":["Australia"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Gary R","family":"Hime","sequence":"additional","affiliation":[{"name":"Department of Anatomy and Physiology, The University of Melbourne , Grattan Street, Parkville, VIC 3010, Melbourne ,","place":["Australia"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Andrew H","family":"Sinclair","sequence":"additional","affiliation":[{"name":"Murdoch Children's Research Institute, Royal Children's Hospital , 50 Flemington Rd, Parkville VIC 3052, Melbourne ,","place":["Australia"]},{"name":"Department of Paediatrics, The University of Melbourne , Grattan Street, Parkville, VIC 3010, Melbourne ,","place":["Australia"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Elena J","family":"Tucker","sequence":"additional","affiliation":[{"name":"Murdoch Children's Research Institute, Royal Children's Hospital , 50 Flemington Rd, Parkville VIC 3052, Melbourne ,","place":["Australia"]},{"name":"Department of Paediatrics, The University of Melbourne , Grattan Street, Parkville, VIC 3010, Melbourne ,","place":["Australia"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2024,10,14]]},"reference":[{"key":"2025011610391968800_ref1","doi-asserted-by":"crossref","first-page":"609","DOI":"10.1210\/er.2016-1047","article-title":"Premature ovarian insufficiency: new perspectives on genetic cause and phenotypic Spectrum","volume":"37","author":"Tucker","year":"2016","journal-title":"Endocr Rev"},{"key":"2025011610391968800_ref2","doi-asserted-by":"crossref","first-page":"104246","DOI":"10.1016\/j.ebiom.2022.104246","article-title":"Genetic landscape of a large cohort of primary ovarian insufficiency: new genes and pathways and implications for personalized medicine","volume":"84","author":"Heddar","year":"2022","journal-title":"EBioMedicine"},{"key":"2025011610391968800_ref3","doi-asserted-by":"crossref","first-page":"403","DOI":"10.1080\/13697137.2019.1574738","article-title":"The global prevalence of primary ovarian insufficiency and early menopause: a meta-analysis","volume":"22","author":"Golezar","year":"2019","journal-title":"Climacteric"},{"key":"2025011610391968800_ref4","doi-asserted-by":"crossref","first-page":"911","DOI":"10.1016\/S0140-6736(10)60355-8","article-title":"Primary ovarian insufficiency","volume":"376","author":"De Vos","year":"2010","journal-title":"Lancet"},{"key":"2025011610391968800_ref5","doi-asserted-by":"crossref","first-page":"1588","DOI":"10.1016\/j.fertnstert.2016.09.046","article-title":"Hormone replacement therapy in young women with primary ovarian insufficiency and early menopause","volume":"106","author":"Sullivan","year":"2016","journal-title":"Fertil Steril"},{"key":"2025011610391968800_ref6","doi-asserted-by":"crossref","first-page":"926","DOI":"10.1093\/humrep\/dew027","article-title":"ESHRE guideline: management of women with premature ovarian insufficiency","volume":"31","author":"European Society for Human, R","year":"2016","journal-title":"Hum Reprod"},{"key":"2025011610391968800_ref7","volume-title":"Human reproductive and prenatal genetics","author":"Leung","year":"2023","edition":"Second"},{"key":"2025011610391968800_ref8","first-page":"439","volume-title":"Chapter 17\u2014Update on the genetics and genomics of premature ovarian insufficiency, in Human Reproductive and Prenatal Genetics","author":"Tucker","year":"2023"},{"key":"2025011610391968800_ref9","doi-asserted-by":"crossref","first-page":"9","DOI":"10.1016\/j.maturitas.2020.06.004","article-title":"New insights into the genetic basis of premature ovarian insufficiency: novel causative variants and candidate genes revealed by genomic sequencing","volume":"141","author":"Jaillard","year":"2020","journal-title":"Maturitas"},{"key":"2025011610391968800_ref10","doi-asserted-by":"crossref","first-page":"1573","DOI":"10.1007\/s10815-014-0342-9","article-title":"Genetics of primary ovarian insufficiency: a review","volume":"31","author":"Fortuno","year":"2014","journal-title":"J Assist Reprod Genet"},{"key":"2025011610391968800_ref11","doi-asserted-by":"crossref","DOI":"10.3390\/genes13112113","article-title":"Integral role of the mitochondrial ribosome in supporting ovarian function: MRPS7 variants in syndromic premature ovarian insufficiency","volume":"13","author":"Kline","year":"2022","journal-title":"Genes (Basel)"},{"key":"2025011610391968800_ref12","doi-asserted-by":"crossref","first-page":"529","DOI":"10.1038\/nrm1964","article-title":"RNA-quality control by the exosome","volume":"7","author":"Houseley","year":"2006","journal-title":"Nat Rev Mol Cell Biol"},{"key":"2025011610391968800_ref13","doi-asserted-by":"crossref","first-page":"227","DOI":"10.1038\/nrm.2015.15","article-title":"The regulation and functions of the nuclear RNA exosome complex","volume":"17","author":"Kilchert","year":"2016","journal-title":"Nat Rev Mol Cell 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DIS3, EXOSC10, or XRN2 reveals the immediate impact of Exoribonucleolysis on nuclear RNA metabolism and transcriptional control","volume":"26","author":"Davidson","year":"2019","journal-title":"Cell Rep"},{"key":"2025011610391968800_ref18","doi-asserted-by":"crossref","first-page":"70","DOI":"10.1038\/nature11870","article-title":"Crystal structure of an RNA-bound 11-subunit eukaryotic exosome complex","volume":"495","author":"Makino","year":"2013","journal-title":"Nature"},{"key":"2025011610391968800_ref19","doi-asserted-by":"crossref","first-page":"2091","DOI":"10.1042\/BCJ20170962","article-title":"DIS3 isoforms vary in their endoribonuclease activity and are differentially expressed within haematological cancers","volume":"475","author":"Robinson","year":"2018","journal-title":"Biochem J"},{"key":"2025011610391968800_ref20","doi-asserted-by":"crossref","first-page":"1622","DOI":"10.1101\/gr.189597.115","article-title":"DIS3 shapes the RNA polymerase II transcriptome in humans by degrading a variety of unwanted transcripts","volume":"25","author":"Szczepinska","year":"2015","journal-title":"Genome Res"},{"key":"2025011610391968800_ref21","doi-asserted-by":"crossref","first-page":"993","DOI":"10.1038\/nature07480","article-title":"Endonucleolytic RNA cleavage by a eukaryotic exosome","volume":"456","author":"Lebreton","year":"2008","journal-title":"Nature"},{"key":"2025011610391968800_ref22","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1007\/978-1-4939-9822-7_1","article-title":"The RNA exosome and human disease","volume":"2062","author":"Fasken","year":"2020","journal-title":"Methods Mol Biol"},{"key":"2025011610391968800_ref23","doi-asserted-by":"crossref","first-page":"594","DOI":"10.1111\/cge.13928","article-title":"Bi-allelic missense variant, p.Ser35Leu in EXOSC1 is associated with pontocerebellar hypoplasia","volume":"99","author":"Somashekar","year":"2021","journal-title":"Clin Genet"},{"key":"2025011610391968800_ref24","doi-asserted-by":"crossref","first-page":"419","DOI":"10.1136\/jmedgenet-2015-103511","article-title":"Mutations in EXOSC2 are associated with a novel syndrome characterised by retinitis pigmentosa, progressive hearing loss, premature ageing, short stature, mild intellectual disability and distinctive gestalt","volume":"53","author":"Di Donato","year":"2016","journal-title":"J Med Genet"},{"key":"2025011610391968800_ref25","doi-asserted-by":"crossref","first-page":"103649","DOI":"10.1016\/j.ejmg.2019.04.006","article-title":"Novel EXOSC3 pathogenic variant results in a mild course of neurologic disease with cerebellum involvement","volume":"63","author":"Le Duc","year":"2020","journal-title":"Eur J Med Genet"},{"key":"2025011610391968800_ref26","doi-asserted-by":"crossref","first-page":"2218","DOI":"10.1093\/hmg\/ddaa108","article-title":"Biallelic variants in the RNA exosome gene EXOSC5 are associated with developmental delays, short 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factors","volume":"2","author":"Xie","year":"2013","journal-title":"Wiley Interdiscip Rev Dev Biol"},{"key":"2025011610391968800_ref45","doi-asserted-by":"crossref","first-page":"103","DOI":"10.1002\/aja.1001990204","article-title":"Genetics of nanos localization in drosophila","volume":"199","author":"Wang","year":"1994","journal-title":"Dev Dyn"},{"key":"2025011610391968800_ref46","doi-asserted-by":"crossref","first-page":"5951","DOI":"10.1038\/s41467-021-26191-1","article-title":"Author correction: a single-cell atlas and lineage analysis of the adult drosophila ovary","volume":"12","author":"Rust","year":"2021","journal-title":"Nat Commun"},{"key":"2025011610391968800_ref47","doi-asserted-by":"crossref","first-page":"REVIEWS1017","DOI":"10.1186\/gb-2000-1-3-reviews1017","article-title":"The function and regulation of vasa-like genes in germ-cell development","volume":"1","author":"Raz","year":"2000","journal-title":"Genome 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