YIPF5 mutations cause neonatal diabetes and microcephaly through endoplasmic reticulum stress.


Journal

The Journal of clinical investigation
ISSN: 1558-8238
Titre abrégé: J Clin Invest
Pays: United States
ID NLM: 7802877

Informations de publication

Date de publication:
01 12 2020
Historique:
received: 23 06 2020
accepted: 27 08 2020
pubmed: 10 11 2020
medline: 17 2 2021
entrez: 9 11 2020
Statut: ppublish

Résumé

Neonatal diabetes is caused by single gene mutations reducing pancreatic β cell number or impairing β cell function. Understanding the genetic basis of rare diabetes subtypes highlights fundamental biological processes in β cells. We identified 6 patients from 5 families with homozygous mutations in the YIPF5 gene, which is involved in trafficking between the endoplasmic reticulum (ER) and the Golgi. All patients had neonatal/early-onset diabetes, severe microcephaly, and epilepsy. YIPF5 is expressed during human brain development, in adult brain and pancreatic islets. We used 3 human β cell models (YIPF5 silencing in EndoC-βH1 cells, YIPF5 knockout and mutation knockin in embryonic stem cells, and patient-derived induced pluripotent stem cells) to investigate the mechanism through which YIPF5 loss of function affects β cells. Loss of YIPF5 function in stem cell-derived islet cells resulted in proinsulin retention in the ER, marked ER stress, and β cell failure. Partial YIPF5 silencing in EndoC-βH1 cells and a patient mutation in stem cells increased the β cell sensitivity to ER stress-induced apoptosis. We report recessive YIPF5 mutations as the genetic cause of a congenital syndrome of microcephaly, epilepsy, and neonatal/early-onset diabetes, highlighting a critical role of YIPF5 in β cells and neurons. We believe this is the first report of mutations disrupting the ER-to-Golgi trafficking, resulting in diabetes.

Identifiants

pubmed: 33164986
pii: 141455
doi: 10.1172/JCI141455
pmc: PMC7685733
doi:
pii:

Substances chimiques

Vesicular Transport Proteins 0
YIPF5 protein, human 0

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

6338-6353

Subventions

Organisme : Wellcome Trust
Pays : United Kingdom
Organisme : Wellcome Trust
ID : WT098395/Z/12/Z
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 105636/Z/14/Z
Pays : United Kingdom
Organisme : Department of Health
Pays : United Kingdom

Commentaires et corrections

Type : CommentIn

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Auteurs

Elisa De Franco (E)

Institute of Biomedical and Clinical Science, University of Exeter Medical School, Exeter, United Kingdom.

Maria Lytrivi (M)

ULB Center for Diabetes Research and.
Division of Endocrinology, Erasmus Hospital, Université Libre de Bruxelles, Brussels, Belgium.

Hazem Ibrahim (H)

Stem Cells and Metabolism Research Program, Faculty of Medicine, University of Helsinki, Helsinki, Finland.

Hossam Montaser (H)

Stem Cells and Metabolism Research Program, Faculty of Medicine, University of Helsinki, Helsinki, Finland.

Matthew N Wakeling (MN)

Institute of Biomedical and Clinical Science, University of Exeter Medical School, Exeter, United Kingdom.

Federica Fantuzzi (F)

ULB Center for Diabetes Research and.
Endocrinology and Metabolism, Department of Medicine and Surgery, University of Parma, Parma, Italy.

Kashyap Patel (K)

Institute of Biomedical and Clinical Science, University of Exeter Medical School, Exeter, United Kingdom.

Céline Demarez (C)

ULB Center for Diabetes Research and.

Ying Cai (Y)

ULB Center for Diabetes Research and.

Mariana Igoillo-Esteve (M)

ULB Center for Diabetes Research and.

Cristina Cosentino (C)

ULB Center for Diabetes Research and.

Väinö Lithovius (V)

Stem Cells and Metabolism Research Program, Faculty of Medicine, University of Helsinki, Helsinki, Finland.

Helena Vihinen (H)

Electron Microscopy Unit, Institute of Biotechnology, University of Helsinki, Helsinki, Finland.

Eija Jokitalo (E)

Electron Microscopy Unit, Institute of Biotechnology, University of Helsinki, Helsinki, Finland.

Thomas W Laver (TW)

Institute of Biomedical and Clinical Science, University of Exeter Medical School, Exeter, United Kingdom.

Matthew B Johnson (MB)

Institute of Biomedical and Clinical Science, University of Exeter Medical School, Exeter, United Kingdom.

Toshiaki Sawatani (T)

ULB Center for Diabetes Research and.

Hadis Shakeri (H)

ULB Center for Diabetes Research and.

Nathalie Pachera (N)

ULB Center for Diabetes Research and.

Belma Haliloglu (B)

Yeditepe University Hospital, Istanbul, Turkey.

Mehmet Nuri Ozbek (MN)

Gazi Yaşargil Education and Research Hospital, Diyarbakır, Turkey.

Edip Unal (E)

Dicle University, Faculty of Medicine, Department of Pediatric Endocrinology, Diyarbakır, Turkey.

Ruken Yıldırım (R)

Dicle University, Faculty of Medicine, Department of Pediatric Endocrinology, Diyarbakır, Turkey.

Tushar Godbole (T)

Harmony Health Hub, Nashik, India.

Melek Yildiz (M)

Istanbul University, Istanbul Faculty of Medicine, Department of Pediatric Endocrinology, Istanbul, Turkey.

Banu Aydin (B)

Kanuni Sultan Suleyman Training and Research Hospital, Department of Pediatric Endocrinology, Istanbul, Turkey.

Angeline Bilheu (A)

Institute of Interdisciplinary Research (IRIBHM), ULB Neuroscience Institute, Université Libre de Bruxelles, Brussels, Belgium.

Ikuo Suzuki (I)

Institute of Interdisciplinary Research (IRIBHM), ULB Neuroscience Institute, Université Libre de Bruxelles, Brussels, Belgium.
VIB-KU Leuven Center for Brain & Disease Research, Leuven, Belgium.
Department of Neurosciences, Leuven Brain Institute, KU Leuven, Leuven, Belgium.

Sarah E Flanagan (SE)

Institute of Biomedical and Clinical Science, University of Exeter Medical School, Exeter, United Kingdom.

Pierre Vanderhaeghen (P)

Institute of Interdisciplinary Research (IRIBHM), ULB Neuroscience Institute, Université Libre de Bruxelles, Brussels, Belgium.
VIB-KU Leuven Center for Brain & Disease Research, Leuven, Belgium.
Department of Neurosciences, Leuven Brain Institute, KU Leuven, Leuven, Belgium.
Welbio, Université Libre de Bruxelles, Brussels, Belgium.

Valérie Senée (V)

Université de Paris, Faculté de Médecine Paris-Diderot, U958, Paris, France.

Cécile Julier (C)

Université de Paris, Faculté de Médecine Paris-Diderot, U958, Paris, France.

Piero Marchetti (P)

Department of Clinical and Experimental Medicine, University of Pisa, Pisa, Italy.

Decio L Eizirik (DL)

ULB Center for Diabetes Research and.
Welbio, Université Libre de Bruxelles, Brussels, Belgium.
Indiana Biosciences Research Institute, Indianapolis, Indiana, USA.

Sian Ellard (S)

Institute of Biomedical and Clinical Science, University of Exeter Medical School, Exeter, United Kingdom.

Jonna Saarimäki-Vire (J)

Stem Cells and Metabolism Research Program, Faculty of Medicine, University of Helsinki, Helsinki, Finland.

Timo Otonkoski (T)

Stem Cells and Metabolism Research Program, Faculty of Medicine, University of Helsinki, Helsinki, Finland.
Children's Hospital, University of Helsinki and Helsinki University Hospital, Helsinki, Finland.

Miriam Cnop (M)

ULB Center for Diabetes Research and.
Division of Endocrinology, Erasmus Hospital, Université Libre de Bruxelles, Brussels, Belgium.

Andrew T Hattersley (AT)

Institute of Biomedical and Clinical Science, University of Exeter Medical School, Exeter, United Kingdom.

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