Null and missense mutations of ERI1 cause a recessive phenotypic dichotomy in humans.

Humans Exoribonucleases / genetics Histones / genetics Mutation, Missense / genetics RNA, Ribosomal, 5.8S RNA RNA, Messenger / genetics
ERI1 exoribonuclease ribosomopathy short stature skeletal dysplasia spondyloepimetaphyseal dysplasia

Journal

American journal of human genetics
ISSN: 1537-6605
Titre abrégé: Am J Hum Genet
Pays: United States
ID NLM: 0370475

Informations de publication

Date de publication:
06 07 2023
Historique:
received: 13 01 2023
revised: 31 05 2023
accepted: 01 06 2023
pmc-release: 06 01 2024
medline: 10 7 2023
pubmed: 24 6 2023
entrez: 23 6 2023
Statut: ppublish

Résumé

ERI1 is a 3'-to-5' exoribonuclease involved in RNA metabolic pathways including 5.8S rRNA processing and turnover of histone mRNAs. Its biological and medical significance remain unclear. Here, we uncover a phenotypic dichotomy associated with bi-allelic ERI1 variants by reporting eight affected individuals from seven unrelated families. A severe spondyloepimetaphyseal dysplasia (SEMD) was identified in five affected individuals with missense variants but not in those with bi-allelic null variants, who showed mild intellectual disability and digital anomalies. The ERI1 missense variants cause a loss of the exoribonuclease activity, leading to defective trimming of the 5.8S rRNA 3' end and a decreased degradation of replication-dependent histone mRNAs. Affected-individual-derived induced pluripotent stem cells (iPSCs) showed impaired in vitro chondrogenesis with downregulation of genes regulating skeletal patterning. Our study establishes an entity previously unreported in OMIM and provides a model showing a more severe effect of missense alleles than null alleles within recessive genotypes, suggesting a key role of ERI1-mediated RNA metabolism in human skeletal patterning and chondrogenesis.

Identifiants

DOI: 10.1016/j.ajhg.2023.06.001 PMID: 37352860 PMC: PMC10357479
pubmed: 37352860
pii: S0002-9297(23)00202-1
doi: 10.1016/j.ajhg.2023.06.001
pmc: PMC10357479
pii:
doi:

Substances chimiques

Exoribonucleases EC 3.1.-
Histones 0
RNA, Ribosomal, 5.8S 0
RNA 63231-63-0
RNA, Messenger 0
ERI1 protein, human EC 3.1.-

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

1068-1085

Informations de copyright

Copyright © 2023 American Society of Human Genetics. Published by Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests The Department of Molecular and Human Genetics at Baylor College of Medicine receives revenue from clinical genetic testing completed at Baylor Genetics Laboratories.

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Auteurs

Long Guo (L)

Department of Laboratory Animal Science, School of Basic Medical Sciences, Xi'an Jiaotong University, Xi'an 710061, China; National Local Joint Engineering Research Center for Precision Surgery & Regenerative Medicine, the First Affiliated Hospital of Xi'an Jiaotong University, Xi'an 710061, China; Center of Medical Genetics, Northwest Women's and Children's Hospital, the Affiliated Northwest Women's and Children's Hospital of Xi'an Jiaotong University Health Science Center, Xi'an 710003, China. Electronic address: longguo601@gmail.com.

Smrithi Salian (S)

Department of Pediatrics, CHU Sainte Justine Research Center, University of Montreal, 3175 Cote-Sainte-Catherine, Montreal, QC H3T 1C5, Canada.

Jing-Yi Xue (JY)

Department of Laboratory Animal Science, School of Basic Medical Sciences, Xi'an Jiaotong University, Xi'an 710061, China; Laboratory for Bone and Joint Diseases, RIKEN Center for Integrative Medical Sciences, Tokyo 108-8639, Japan.

Nicola Rath (N)

Research Unit Molecular Immune Regulation, Helmholtz Zentrum München, German Research Center for Environmental Health, D-81377 Munich, Germany.

Justine Rousseau (J)

Department of Pediatrics, CHU Sainte Justine Research Center, University of Montreal, 3175 Cote-Sainte-Catherine, Montreal, QC H3T 1C5, Canada.

Hyunyun Kim (H)

Department of Pediatrics, CHU Sainte Justine Research Center, University of Montreal, 3175 Cote-Sainte-Catherine, Montreal, QC H3T 1C5, Canada.

Sophie Ehresmann (S)

Molecular Biology Program, Université de Montréal, Montréal, QC H3T 1J4, Canada.

Shahida Moosa (S)

Division of Molecular Biology and Human Genetics, Stellenbosch University and Medical Genetics, Tygerberg Hospital, Tygerberg 7505, South Africa.

Norio Nakagawa (N)

Department of Pediatrics, Graduate School of Medical Science, Kyoto Prefectural University of Medicine, Kyoto 602-8566, Japan; Department of Pediatrics, North Medical Center, Kyoto Prefectural University of Medicine, Kyoto 602-8566, Japan.

Hiroshi Kuroda (H)

Department of Pediatrics, Kyoto City Hospital, Kyoto 604-8845, Japan.

Jill Clayton-Smith (J)

Manchester Centre for Genomic Medicine, St Mary's Hospital, Manchester University Foundation NHS Trust, Health Innovation Manchester, M13 9WL Manchester, UK; Division of Evolution and Genomic Sciences, School of Biological Sciences, Faculty of Biology, Medicine and Health, The University of Manchester, M13 9PL Manchester, UK.

Juan Wang (J)

Department of Ultrasound, the Second Affiliated Hospital of Xi'an Jiaotong University, Xi'an 710004, China.

Zheng Wang (Z)

Laboratory for Bone and Joint Diseases, RIKEN Center for Integrative Medical Sciences, Tokyo 108-8639, Japan.

Siddharth Banka (S)

Manchester Centre for Genomic Medicine, St Mary's Hospital, Manchester University Foundation NHS Trust, Health Innovation Manchester, M13 9WL Manchester, UK; Division of Evolution and Genomic Sciences, School of Biological Sciences, Faculty of Biology, Medicine and Health, The University of Manchester, M13 9PL Manchester, UK.

Adam Jackson (A)

Manchester Centre for Genomic Medicine, St Mary's Hospital, Manchester University Foundation NHS Trust, Health Innovation Manchester, M13 9WL Manchester, UK; Division of Evolution and Genomic Sciences, School of Biological Sciences, Faculty of Biology, Medicine and Health, The University of Manchester, M13 9PL Manchester, UK.

Yan-Min Zhang (YM)

Shaanxi Institute for Pediatric Diseases, Xi'an Children's Hospital, Affiliated Children's Hospital of Xi'an Jiaotong University, Xi'an 710082, China.

Zhen-Jie Wei (ZJ)

Laboratory for Bone and Joint Diseases, RIKEN Center for Integrative Medical Sciences, Tokyo 108-8639, Japan.

Irina Hüning (I)

Institute of Human Genetics, University of Lübeck, 23538 Lübeck, Germany.

Theresa Brunet (T)

Institute of Human Genetics, School of Medicine, Technical University Munich, 80333 Munich, Germany; Department of Paediatric Neurology and Developmental Medicine, Hauner Children's Hospital, Ludwig Maximilian University of Munich, 80539 Munich, Germany.

Hirofumi Ohashi (H)

Division of Medical Genetics, Saitama Children's Hospital, Saitama 330-8777, Japan.

Molly F Thomas (MF)

Division of Gastroenterology, Department of Medicine, Massachusetts General Hospital, Boston, MA 02114, USA.

Caleb Bupp (C)

Spectrum Health, Grand Rapids, MI 49503, USA.

Noriko Miyake (N)

Department of Human Genetics, Research Institute, National Center for Global Health and Medicine, Tokyo 162-8655, Japan.

Naomichi Matsumoto (N)

Department of Human Genetics, Yokohama City University Graduate School of Medicine, Yokohama 236-0004, Japan.

Roberto Mendoza-Londono (R)

Division of Clinical and Metabolic Genetics, The Hospital for Sick Children, Program in Genetics and Genome Biology, SickKids Research Institute, and Department of Paediatrics, University of Toronto, Toronto, ON M5G 1X8, Canada.

Gregory Costain (G)

Department of Molecular Genetics, University of Toronto, Toronto, ON M5S 1A4, Canada.

Gabriele Hahn (G)

Institute for Radiological Diagnostics, Universitätsklinikum Carl Gustav Carus Dresden, Technische Universität, 01307 Dresden, Germany.

Nataliya Di Donato (N)

Institute for Clinical Genetics, University Hospital, TU Dresden, 01069 Dresden, Germany.

Gökhan Yigit (G)

Institute of Human Genetics, University Medical Center Göttingen, 37075 Göttingen, Germany; DZHK (German Center for Cardiovascular Research), partner site Göttingen, 37075 Göttingen, Germany.

Takahiro Yamada (T)

Department of Medical Ethics and Medical Genetics, Kyoto University School of Public Health, Kyoto 606-8501, Japan.

Gen Nishimura (G)

Laboratory for Bone and Joint Diseases, RIKEN Center for Integrative Medical Sciences, Tokyo 108-8639, Japan.

K Mark Ansel (KM)

Department of Microbiology and Immunology, University of California San Francisco, San Francisco, CA 94143, USA.

Bernd Wollnik (B)

Institute of Human Genetics, University Medical Center Göttingen, 37075 Göttingen, Germany; DZHK (German Center for Cardiovascular Research), partner site Göttingen, 37075 Göttingen, Germany; Cluster of Excellence "Multiscale Bioimaging: from Molecular Machines to Networks of Excitable Cells" (MBExC), University of Göttingen, 37075 Göttingen, Germany.

Martin Hrabě de Angelis (M)

Institute of Experimental Genetics, German Mouse Clinic, Helmholtz Zentrum München, German Research Center for Environmental Health (GmbH), 85764 Neuherberg, Germany; Chair of Experimental Genetics, TUM School of Life Sciences, Technische Universität München, 85354 Freising, Germany; German Center for Diabetes Research (DZD), 85764 Neuherberg, Germany.

André Mégarbané (A)

Department of Human Genetics, Gilbert and Rose-Marie Chagoury School of Medicine, Lebanese American University, 1102-2801, Lebanon and Institut Jerome Lejeune, 75015 Paris, France.

Jill A Rosenfeld (JA)

Department of Molecular & Human Genetics, Baylor College of Medicine, Houston, TX 77030, USA; Baylor Genetics Laboratories, Houston, TX 77021, USA.

Vigo Heissmeyer (V)

Research Unit Molecular Immune Regulation, Helmholtz Zentrum München, German Research Center for Environmental Health, D-81377 Munich, Germany; Institute for Immunology, Biomedical Center, Faculty of Medicine, Ludwig-Maximilians-Universität in Munich, 82152 Planegg-Martinsried, Germany.

Shiro Ikegawa (S)

Laboratory for Bone and Joint Diseases, RIKEN Center for Integrative Medical Sciences, Tokyo 108-8639, Japan.

Philippe M Campeau (PM)

Department of Pediatrics, CHU Sainte Justine Research Center, University of Montreal, 3175 Cote-Sainte-Catherine, Montreal, QC H3T 1C5, Canada. Electronic address: p.campeau@umontreal.ca.

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Classifications MeSH

questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Primates › Haplorhini › Catarrhini › Hominidae › Humains › Null and missense mutations of ERI1 cause a...
questionsmedicales.fr › Enzymes et coenzymes › Enzymes › Hydrolases › Esterases › Ribonucléases › Exoribonucleases › Null and missense mutations of ERI1 cause a...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Nucléoprotéines › Histone › Null and missense mutations of ERI1 cause a...
questionsmedicales.fr › Phénomènes génétiques › Variation génétique › Mutation › Mutation faux-sens › Null and missense mutations of ERI1 cause a...
questionsmedicales.fr › Acides nucléiques, nucléotides et nucléosides › Acides nucléiques › ARN › ARN ribosomique › ARN ribosomique 5.8S › Null and missense mutations of ERI1 cause a...
questionsmedicales.fr › Acides nucléiques, nucléotides et nucléosides › Acides nucléiques › ARN › Null and missense mutations of ERI1 cause a...
questionsmedicales.fr › Acides nucléiques, nucléotides et nucléosides › Acides nucléiques › ARN › ARN messager › Null and missense mutations of ERI1 cause a...