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Deficiency of the minor spliceosome component U4atac snRNA secondarily results in ciliary defects in human and zebrafish

Title: Deficiency of the minor spliceosome component U4atac snRNA secondarily results in ciliary defects in human and zebrafish
Authors: Khatri, Deepak; Putoux, Audrey; Cologne, Audric; Kaltenbach, Sophie; Besson, Alicia; Bertiaux, Eloïse; Guguin, Justine; Fendler, Adèle; Dupont, Marie; Benoit-Pilven, Clara; Qebibo, Leila; Ahmed-Elie, Samira; Audebert-Bellanger, Séverine; Blanc, Pierre; Rambaud, Thomas; Castelle, Martin; Cornen, Gaëlle; Grotto, Sarah; Guët, Agnès; Guibaud, Laurent; Michot, Caroline; Odent, Sylvie; Ruaud, Lyse; Sacaze, Elise; Hamel, Virginie; Bordonné, Rémy; Leutenegger, Anne-Louise; Edery, Patrick; Burglen, Lydie; Attié-Bitach, Tania; Mazoyer, Sylvie; Delous, Marion
Contributors: Centre de recherche en neurosciences de Lyon - Lyon Neuroscience Research Center (CRNL); Université Claude Bernard Lyon 1 (UCBL); Université de Lyon-Université de Lyon-Université Jean Monnet - Saint-Étienne (UJM)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS); Hospices Civils de Lyon (HCL); Laboratoire de Biométrie et Biologie Evolutive - UMR 5558 (LBBE); Université de Lyon-Université de Lyon-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS); Hôpital Necker - Enfants Malades AP-HP; Assistance publique - Hôpitaux de Paris (AP-HP) (AP-HP); Université de Genève = University of Geneva (UNIGE); Imagine - Institut des maladies génétiques (IHU) (Imagine - U1163); Institut National de la Santé et de la Recherche Médicale (INSERM)-Université Paris Cité (UPCité); CHU Trousseau APHP; Assistance publique - Hôpitaux de Paris (AP-HP) (AP-HP)-Sorbonne Université (SU); Sorbonne Université (SU); Hôpital Morvan Brest; CH Morlaix; Maternité Port-Royal CHU Cochin; Assistance publique - Hôpitaux de Paris (AP-HP) (AP-HP)-Hôpital Cochin AP-HP; Hôpital Louis Mourier - AP-HP Colombes; Université de Lyon; Institut de Génétique et Développement de Rennes (IGDR); Université de Rennes (UR)-Centre National de la Recherche Scientifique (CNRS)-Structure Fédérative de Recherche en Biologie et Santé de Rennes (Biosit : Biologie - Santé - Innovation Technologique); Centre Hospitalier Universitaire de Rennes CHU Rennes = Rennes University Hospital Pontchaillou; Maladies neurodéveloppementales et neurovasculaires (NeuroDiderot (UMR_S_1141 / U1141)); Hôpital Robert Debré; Centre Hospitalier Régional Universitaire de Brest (CHRU Brest); Institut de Génétique Moléculaire de Montpellier (IGMM); Centre National de la Recherche Scientifique (CNRS)-Université de Montpellier (UM); This work was supported by CNRS, Inserm, Université de Montpellier, Université Paris 7 and Université Lyon 1 through recurrent funding; the Fondation Maladies Rares (“Small Animal Models and Rare Diseases” program, no. 20161207); the Agence Nationale de la Recherche (no. ANR-18CE12-0007-01); and the Fondation pour la recherche sur le Cerveau « Espoir en tête » (confocal microscope). E.B. was supported by an European Molecular Biology Organization long-term fellowship (ALTF-284-2019) and the Novartis Foundation for medical-biological Research (18B112).; ANR-18-CE12-0007,U4ATAC-BRAIN,Rôle de l'épissage mineur dans le développement cérébral(2018)
Source: ISSN: 0027-8424.
Publisher Information: CCSD; National Academy of Sciences
Publication Year: 2023
Collection: Université Jean Monnet – Saint-Etienne: HAL
Subject Terms: U4atac; genetic disease; minor introns; primary cilium; splicing; MESH: Female; MESH: Animals; MESH: Humans; MESH: Spliceosomes; MESH: RNA; Small Nuclear; MESH: Zebrafish; MESH: Fetal Growth Retardation; MESH: Mutation; MESH: Ciliopathies; [SDV.GEN]Life Sciences [q-bio]/Genetics
Description: International audience ; In the human genome, about 750 genes contain one intron excised by the minor spliceosome. This spliceosome comprises its own set of snRNAs, among which U4atac. Its noncoding gene, , has been found mutated in Taybi-Linder (TALS/microcephalic osteodysplastic primordial dwarfism type 1), Roifman (RFMN), and Lowry-Wood (LWS) syndromes. These rare developmental disorders, whose physiopathological mechanisms remain unsolved, associate ante- and post-natal growth retardation, microcephaly, skeletal dysplasia, intellectual disability, retinal dystrophy, and immunodeficiency. Here, we report bi-allelic mutations in five patients presenting with traits suggestive of the Joubert syndrome (JBTS), a well-characterized ciliopathy. These patients also present with traits typical of TALS/RFMN/LWS, thus widening the clinical spectrum of -associated disorders and indicating ciliary dysfunction as a mechanism downstream of minor splicing defects. Intriguingly, all five patients carry the n.16G>A mutation, in the Stem II domain, either at the homozygous or compound heterozygous state. A gene ontology term enrichment analysis on minor intron-containing genes reveals that the cilium assembly process is over-represented, with no less than 86 cilium-related genes containing at least one minor intron, among which there are 23 ciliopathy-related genes. The link between mutations and ciliopathy traits is supported by alterations of primary cilium function in TALS and JBTS-like patient fibroblasts, as well as by zebrafish model, which exhibits ciliopathy-related phenotypes and ciliary defects. These phenotypes could be rescued by WT but not by pathogenic variants-carrying human U4atac. Altogether, our data indicate that alteration of cilium biogenesis is part of the physiopathological mechanisms of TALS/RFMN/LWS, secondarily to defects of minor intron splicing.
Document Type: article in journal/newspaper
Language: English
Relation: info:eu-repo/semantics/altIdentifier/pmid/36802443; PUBMED: 36802443
DOI: 10.1073/pnas.2102569120
Availability: https://univ-rennes.hal.science/hal-04021151; https://univ-rennes.hal.science/hal-04021151v1/document; https://univ-rennes.hal.science/hal-04021151v1/file/Khatri-2023-pnas.2102569120.pdf; https://doi.org/10.1073/pnas.2102569120
Rights: info:eu-repo/semantics/OpenAccess
Accession Number: edsbas.32DAD44E
Database: BASE