B-cell immune deficiency in twin sisters expands the phenotype of MOPDI.

MOPDI RNU4ATAC U4atac snRNA immunodeficiency microcephalic osteodysplastic primordial dwarfism type I

Journal

Clinical genetics
ISSN: 1399-0004
Titre abrégé: Clin Genet
Pays: Denmark
ID NLM: 0253664

Informations de publication

Date de publication:
04 Jun 2024
Historique:
revised: 03 05 2024
received: 26 02 2024
accepted: 26 05 2024
medline: 5 6 2024
pubmed: 5 6 2024
entrez: 5 6 2024
Statut: aheadofprint

Résumé

Microcephalic osteodysplastic primordial dwarfism type I (MOPDI) is a very rare and severe autosomal recessive disorder characterized by marked intrauterine growth retardation, skeletal dysplasia, microcephaly and brain malformations. MOPDI is caused by biallelic mutations in RNU4ATAC, a non-coding gene involved in U12-type splicing of 1% of the introns in the genome, which are recognized by their specific splicing consensus sequences. Here, we describe a unique observation of immunodeficiency in twin sisters with mild MOPDI, who harbor a novel n.108_126del mutation, encompassing part of the U4atac snRNA 3' stem-loop and Sm protein binding site, and the previously reported n.111G>A mutation. Interestingly, both twin sisters show mild B-cell anomalies, including low naive B-cell counts and increased memory B-cell and plasmablasts counts, suggesting partial and transitory blockage of B-cell maturation and/or excessive activation of naive B-cells. Hence, the localization of a mutation in stem II of U4atac snRNA, as observed in another RNU4ATAC-opathy with immunodeficiency, that is, Roifman syndrome (RFMN), is not required for the occurrence of an immune deficiency. Finally, we emphasize the importance of considering immunodeficiency in MOPDI management to reduce the risk of serious infectious episodes.

Identifiants

pubmed: 38837402
doi: 10.1111/cge.14571
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© 2024 The Author(s). Clinical Genetics published by John Wiley & Sons Ltd.

Références

Majewski F, Spranger J. A new type of primordial dwarfism. Monatsschr Kinderheilkd (1902). 1976;124:499‐503.
Meinecke P, Passarge E. Microcephalic osteodysplastic primordial dwarfism type I/III in sibs. J Med Genet. 1991;28:795‐800. doi:10.1136/jmg.28.11.795
Putoux A, Alqahtani A, Pinson L, et al. Refining the phenotypical and mutational spectrum of Taybi‐Linder syndrome. Clin Genet. 2016;90:550‐555. doi:10.1111/cge.12781
Edery P, Marcaillou C, Sahbatou M, et al. Association of TALS developmental disorder with defect in minor splicing component U4atac snRNA. Science. 2011;332:240‐243. doi:10.1126/science.1202205
He H, Liyanarachchi S, Akagi K, et al. Mutations in U4atac snRNA, a component of the minor spliceosome, in the developmental disorder MOPD I. Science. 2011;332:238‐240. doi:10.1126/science.1200587
Padgett RA. New connections between splicing and human disease. Trends Genet. 2012;28:147‐154. doi:10.1016/j.tig.2012.01.001
Cologne A, Benoit‐Pilven C, Besson A, et al. New insights into minor splicing—a transcriptomic analysis of cells derived from TALS patients. RNA. 2019;25:1130‐1149. doi:10.1261/rna.071423.119
Benoit‐Pilven C, Besson A, Putoux A, et al. Clinical interpretation of variants identified in RNU4ATAC, a non‐coding spliceosomal gene. PLoS One. 2020;15:e0235655. doi:10.1371/journal.pone.0235655
Farach LS, Little ME, Duker AL, et al. The expanding phenotype of RNU4ATAC pathogenic variants to Lowry Wood syndrome. Am J Med Genet A. 2018;176:465‐469. doi:10.1002/ajmg.a.38581
Heremans J, Garcia‐Perez JE, Turro E, et al. Abnormal differentiation of B cells and megakaryocytes in patients with Roifman syndrome. J Allergy Clin Immunol. 2018;142:630‐646. doi:10.1016/j.jaci.2017.11.061
Merico D, Roifman M, Braunschweig U, et al. Compound heterozygous mutations in the noncoding RNU4ATAC cause Roifman syndrome by disrupting minor intron splicing. Nat Commun. 2015;6:8718. doi:10.1038/ncomms9718
Roifman CM. Antibody deficiency, growth retardation, spondyloepiphyseal dysplasia and retinal dystrophy: a novel syndrome. Clin Genet. 1999;55:103‐109. doi:10.1034/j.1399‐0004.1999.550206.x
Khatri D, Putoux A, Cologne A, et al. Deficiency of the minor spliceosome component U4atac snRNA secondarily results in ciliary defects in human and zebrafish. Proc Natl Acad Sci U S A. 2023;120:e2102569120. doi:10.1073/pnas.2102569120
Hagiwara H, Matsumoto H, Uematsu K, et al. Immunodeficiency in a patient with microcephalic osteodysplastic primordial dwarfism type I as compared to Roifman syndrome. Brain Dev. 2021;43:337‐342. doi:10.1016/j.braindev.2020.09.007
Sirohi N, Duker AL, Bober MB, DeFelice ML. Immune deficiency in microcephalic osteodysplastic primordial dwarfism type I/III. J Clin Immunol. 2023;43:895‐897. doi:10.1007/s10875‐023‐01447‐1
Almentina Ramos Shidi F, Cologne A, Delous M, et al. Mutations in the non‐coding RNU4ATAC gene affect the homeostasis and function of the integrator complex. Nucleic Acids Res. 2023;51:712‐727. doi:10.1093/nar/gkac1182
Sigaudy S, Toutain A, Moncla A, et al. Microcephalic osteodysplastic primordial dwarfism Taybi‐Linder type: report of four cases and review of the literature. Am J Med Genet. 1998;80:16‐24.
Shukla GC, Cole AJ, Dietrich RC, Padgett RA. Domains of human U4atac snRNA required for U12‐dependent splicing in vivo. Nucleic Acids Res. 2002;30:4650‐4657. doi:10.1093/nar/gkf609

Auteurs

Lucas W Gauthier (LW)

Department of Genetics, Clinical Genetics Unit, Centre de Référence Maladies Rares des Anomalies du Développement Sud-Est, Hospices Civils de Lyon, Université Claude Bernard Lyon 1, Bron, France.

Morgane Gossez (M)

CIRI, Centre International de Recherche en Infectiologie, Univ Lyon, Inserm U1111, Université Claude Bernard-Lyon 1, CNRS, UMR5308, ENS Lyon, Lyon, France.
Immunology Laboratory, Hospices Civils de Lyon, Edouard Herriot Hospital, Lyon, France.

Christophe Malcus (C)

Immunology Laboratory, Hospices Civils de Lyon, Edouard Herriot Hospital, Lyon, France.

Sébastien Viel (S)

Plateforme de Biothérapies et de production de MTI, Hôpital Edouard Herriot, Hospices Civils de Lyon, Lyon, France.

Guillaume Monneret (G)

Immunology Laboratory, Hospices Civils de Lyon, Edouard Herriot Hospital, Lyon, France.
Equipe d'Accueil 7426, Pathophysiology of Injury-Induced Immunosuppression, Université Claude Bernard Lyon 1, Hospices Civils de Lyon - bioMérieux, Hôpital Edouard Herriot, Lyon, France.

Remy Bordonné (R)

Institut de Génétique Moléculaire de Montpellier, University of Montpellier, CNRS UMR5535, Montpellier, France.

Linda Pons (L)

Unité Fonctionnelle de Cytogénétique, Laboratoire de Biologie Médicale, Centre hospitalier de Valence, Valence, France.

Sara Cabet (S)

Pediatric and Fetal Imaging Department, Femme-Mère-Enfant Hospital, Hospices Civils de Lyon, Claude Bernard Lyon 1 University, Lyon, France.
Institut NeuroMyoGène, CNRS UMR5292, INSERM U1028, Claude Bernard Lyon 1 University, Lyon, France.

Marion Delous (M)

Université Claude Bernard Lyon 1, INSERM, CNRS, Centre de Recherche en Neurosciences de Lyon CRNL U1028 UMR5292, Genetics of Neurodevelopment Team (GENDEV), Bron, France.

Sylvie Mazoyer (S)

Université Claude Bernard Lyon 1, INSERM, CNRS, Centre de Recherche en Neurosciences de Lyon CRNL U1028 UMR5292, Genetics of Neurodevelopment Team (GENDEV), Bron, France.

Audrey Putoux (A)

Department of Genetics, Clinical Genetics Unit, Centre de Référence Maladies Rares des Anomalies du Développement Sud-Est, Hospices Civils de Lyon, Université Claude Bernard Lyon 1, Bron, France.
Université Claude Bernard Lyon 1, INSERM, CNRS, Centre de Recherche en Neurosciences de Lyon CRNL U1028 UMR5292, Genetics of Neurodevelopment Team (GENDEV), Bron, France.

Patrick Edery (P)

Department of Genetics, Clinical Genetics Unit, Centre de Référence Maladies Rares des Anomalies du Développement Sud-Est, Hospices Civils de Lyon, Université Claude Bernard Lyon 1, Bron, France.
Université Claude Bernard Lyon 1, INSERM, CNRS, Centre de Recherche en Neurosciences de Lyon CRNL U1028 UMR5292, Genetics of Neurodevelopment Team (GENDEV), Bron, France.

Classifications MeSH