Monoallelic pathogenic ALG5 variants cause atypical polycystic kidney disease and interstitial fibrosis.

ALG5 N-linked glycosylation autosomal dominant tubulo-interstitial kidney disease autosomal-dominant polycystic kidney disease renal insufficiency

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:
04 08 2022
Historique:
received: 11 03 2022
accepted: 23 06 2022
pubmed: 28 7 2022
medline: 10 8 2022
entrez: 27 7 2022
Statut: ppublish

Résumé

Disorders of the autosomal dominant polycystic kidney disease (ADPKD) spectrum are characterized by the development of kidney cysts and progressive kidney function decline. PKD1 and PKD2, encoding polycystin (PC)1 and 2, are the two major genes associated with ADPKD; other genes include IFT140, GANAB, DNAJB11, and ALG9. Genetic testing remains inconclusive in ∼7% of the families. We performed whole-exome sequencing in a large multiplex genetically unresolved (GUR) family affected by ADPKD-like symptoms and identified a monoallelic frameshift variant (c.703_704delCA) in ALG5. ALG5 encodes an endoplasmic-reticulum-resident enzyme required for addition of glucose molecules to the assembling N-glycan precursors. To identify additional families, we screened a cohort of 1,213 families with ADPKD-like and/or autosomal-dominant tubulointerstitial kidney diseases (ADTKD), GUR (n = 137) or naive to genetic testing (n = 1,076), by targeted massively parallel sequencing, and we accessed Genomics England 100,000 Genomes Project data. Four additional families with pathogenic variants in ALG5 were identified. Clinical presentation was consistent in the 23 affected members, with non-enlarged cystic kidneys and few or no liver cysts; 8 subjects reached end-stage kidney disease from 62 to 91 years of age. We demonstrate that ALG5 haploinsufficiency is sufficient to alter the synthesis of the N-glycan chain in renal epithelial cells. We also show that ALG5 is required for PC1 maturation and membrane and ciliary localization and that heterozygous loss of ALG5 affects PC1 maturation. Overall, our results indicate that monoallelic variants of ALG5 lead to a disorder of the ADPKD-spectrum characterized by multiple small kidney cysts, progressive interstitial fibrosis, and kidney function decline.

Identifiants

pubmed: 35896117
pii: S0002-9297(22)00266-X
doi: 10.1016/j.ajhg.2022.06.013
pmc: PMC9388391
pii:
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1484-1499

Subventions

Organisme : NIDDK NIH HHS
ID : R01 DK058816
Pays : United States

Informations de copyright

Copyright © 2022 American Society of Human Genetics. Published by Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests The authors declare no competing interests.

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Auteurs

Hugo Lemoine (H)

Univ. Brest, Inserm, UMR 1078, GGB, 29200 Brest, France.

Loann Raud (L)

Univ. Brest, Inserm, UMR 1078, GGB, 29200 Brest, France.

François Foulquier (F)

Univ. Lille, CNRS, UMR 8576 - UGSF - Unité de Glycobiologie Structurale et Fonctionnelle, 59000 Lille, France.

John A Sayer (JA)

Translational and Clinical Research Institute, Faculty of Medical Sciences, Newcastle University, Newcastle Upon Tyne NE1 3BZ, UK; The Newcastle upon Tyne Hospitals NHS Foundation Trust, Renal Services, Freeman Road, Newcastle Upon Tyne NE7 7DN, UK; NIHR Newcastle Biomedical Research Centre, Newcastle University, Newcastle Upon Tyne NE4 5PL, UK.

Baptiste Lambert (B)

Univ. Lille, CNRS, UMR 8576 - UGSF - Unité de Glycobiologie Structurale et Fonctionnelle, 59000 Lille, France.

Eric Olinger (E)

Translational and Clinical Research Institute, Faculty of Medical Sciences, Newcastle University, Newcastle Upon Tyne NE1 3BZ, UK.

Siriane Lefèvre (S)

Univ. Brest, Inserm, UMR 1078, GGB, 29200 Brest, France; Service de Néphrologie, Hôpital de Lorient, 56322 Lorient, France.

Bertrand Knebelmann (B)

Service de Néphrologie et Transplantation rénale, Hôpital Necker, APHP, Université de Paris, Paris, France.

Peter C Harris (PC)

Division of Nephrology and Hypertension, Mayo Clinic, Rochester, MN 55902, USA.

Pascal Trouvé (P)

Univ. Brest, Inserm, UMR 1078, GGB, 29200 Brest, France.

Aurore Desprès (A)

Service de Génétique moléculaire, CHRU Brest, 29609 Brest, France.

Gabrielle Duneau (G)

Association des Urémiques de Bretagne, Lorient, France.

Marie Matignon (M)

University Paris Est Créteil, Institut National de la Santé et de la Recherche Médicale (INSERM), Assistance Publique des Hôpitaux de Paris (AP-HP), Hôpitaux Universitaires Henri Mondor, Service de Néphrologie et Transplantation, Fédération Hospitalo-Universitaire "Innovative Therapy for Immune Disorders", Créteil, France.

Anais Poyet (A)

Association Régionale d'Aide aux Urémiques du Centre Ouest (ARAUCO), Bourges, France.

Noémie Jourde-Chiche (N)

Centre de Néphrologie et Transplantation Rénale, Hôpital de la Conception (APHM), Marseille, France.

Dominique Guerrot (D)

Service de Néphrologie, Dialyse et Transplantation, CHU de Rouen, Rouen, France.

Sandrine Lemoine (S)

Néphrologie, Dialyse, Hypertension artérielle et Exploration Fonctionnelle rénale, Groupement Hospitalier Edouard Herriot, Hospices Civils de Lyon, Lyon, France.

Guillaume Seret (G)

Néphrologie-Dialyse, Association ECHO, Le Mans, France.

Miguel Barroso-Gil (M)

Translational and Clinical Research Institute, Faculty of Medical Sciences, Newcastle University, Newcastle Upon Tyne NE1 3BZ, UK.

Coralie Bingham (C)

Royal Devon and Exeter NHS Foundation Trust, Exeter EX2 5DW, UK.

Rodney Gilbert (R)

Southampton Children's Hospital, University of Southampton, Southampton SO16 6YD, UK.

Yannick Le Meur (Y)

Univ Brest, UMR 1227, LBAI, Labex IGO, 29200 Brest, France; Service de Néphrologie, Hémodialyse et Transplantation rénale, CHRU Brest, 29609 Brest, France.

Marie-Pierre Audrézet (MP)

Univ. Brest, Inserm, UMR 1078, GGB, 29200 Brest, France; Service de Génétique moléculaire, CHRU Brest, 29609 Brest, France.

Emilie Cornec-Le Gall (E)

Univ. Brest, Inserm, UMR 1078, GGB, 29200 Brest, France; Service de Néphrologie, Hémodialyse et Transplantation rénale, CHRU Brest, 29609 Brest, France. Electronic address: emilie.cornec-legall@chu-brest.fr.

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