Biallelic variants in COPB1 cause a novel, severe intellectual disability syndrome with cataracts and variable microcephaly.


Journal

Genome medicine
ISSN: 1756-994X
Titre abrégé: Genome Med
Pays: England
ID NLM: 101475844

Informations de publication

Date de publication:
25 02 2021
Historique:
received: 08 07 2020
accepted: 11 02 2021
entrez: 26 2 2021
pubmed: 27 2 2021
medline: 21 1 2022
Statut: epublish

Résumé

Coat protein complex 1 (COPI) is integral in the sorting and retrograde trafficking of proteins and lipids from the Golgi apparatus to the endoplasmic reticulum (ER). In recent years, coat proteins have been implicated in human diseases known collectively as "coatopathies". Whole exome or genome sequencing of two families with a neuro-developmental syndrome, variable microcephaly and cataracts revealed biallelic variants in COPB1, which encodes the beta-subunit of COPI (β-COP). To investigate Family 1's splice donor site variant, we undertook patient blood RNA studies and CRISPR/Cas9 modelling of this variant in a homologous region of the Xenopus tropicalis genome. To investigate Family 2's missense variant, we studied cellular phenotypes of human retinal epithelium and embryonic kidney cell lines transfected with a COPB1 expression vector into which we had introduced Family 2's mutation. We present a new recessive coatopathy typified by severe developmental delay and cataracts and variable microcephaly. A homozygous splice donor site variant in Family 1 results in two aberrant transcripts, one of which causes skipping of exon 8 in COPB1 pre-mRNA, and a 36 amino acid in-frame deletion, resulting in the loss of a motif at a small interaction interface between β-COP and β'-COP. Xenopus tropicalis animals with a homologous mutation, introduced by CRISPR/Cas9 genome editing, recapitulate features of the human syndrome including microcephaly and cataracts. In vitro modelling of the COPB1 c.1651T>G p.Phe551Val variant in Family 2 identifies defective Golgi to ER recycling of this mutant β-COP, with the mutant protein being retarded in the Golgi. This adds to the growing body of evidence that COPI subunits are essential in brain development and human health and underlines the utility of exome and genome sequencing coupled with Xenopus tropicalis CRISPR/Cas modelling for the identification and characterisation of novel rare disease genes.

Sections du résumé

BACKGROUND
Coat protein complex 1 (COPI) is integral in the sorting and retrograde trafficking of proteins and lipids from the Golgi apparatus to the endoplasmic reticulum (ER). In recent years, coat proteins have been implicated in human diseases known collectively as "coatopathies".
METHODS
Whole exome or genome sequencing of two families with a neuro-developmental syndrome, variable microcephaly and cataracts revealed biallelic variants in COPB1, which encodes the beta-subunit of COPI (β-COP). To investigate Family 1's splice donor site variant, we undertook patient blood RNA studies and CRISPR/Cas9 modelling of this variant in a homologous region of the Xenopus tropicalis genome. To investigate Family 2's missense variant, we studied cellular phenotypes of human retinal epithelium and embryonic kidney cell lines transfected with a COPB1 expression vector into which we had introduced Family 2's mutation.
RESULTS
We present a new recessive coatopathy typified by severe developmental delay and cataracts and variable microcephaly. A homozygous splice donor site variant in Family 1 results in two aberrant transcripts, one of which causes skipping of exon 8 in COPB1 pre-mRNA, and a 36 amino acid in-frame deletion, resulting in the loss of a motif at a small interaction interface between β-COP and β'-COP. Xenopus tropicalis animals with a homologous mutation, introduced by CRISPR/Cas9 genome editing, recapitulate features of the human syndrome including microcephaly and cataracts. In vitro modelling of the COPB1 c.1651T>G p.Phe551Val variant in Family 2 identifies defective Golgi to ER recycling of this mutant β-COP, with the mutant protein being retarded in the Golgi.
CONCLUSIONS
This adds to the growing body of evidence that COPI subunits are essential in brain development and human health and underlines the utility of exome and genome sequencing coupled with Xenopus tropicalis CRISPR/Cas modelling for the identification and characterisation of novel rare disease genes.

Identifiants

pubmed: 33632302
doi: 10.1186/s13073-021-00850-w
pii: 10.1186/s13073-021-00850-w
pmc: PMC7908744
doi:

Substances chimiques

COPB1 protein, human 0
Coatomer Protein 0

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

34

Subventions

Organisme : Wellcome Trust
ID : 101480Z
Pays : United Kingdom
Organisme : Biotechnology and Biological Sciences Research Council
ID : BB/K019988/1
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 204378/Z/16/Z
Pays : United Kingdom
Organisme : Department of Health
ID : RP-2016-07-011
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/V012177/1
Pays : United Kingdom

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Auteurs

William L Macken (WL)

Wessex Clinical Genetics Service, Princess Anne Hospital, University Hospital Southampton NHS Foundation Trust, Coxford Rd, Southampton, SO165YA, UK.

Annie Godwin (A)

European Xenopus Resource Centre, University of Portsmouth School of Biological Sciences, King Henry Building, King Henry I Street, Portsmouth, PO1 2DY, UK.

Gabrielle Wheway (G)

Faculty of Medicine, University of Southampton, Duthie Building, Southampton General Hospital, Tremona Road, Southampton, SO16 6YD, UK.

Karen Stals (K)

Exeter Genomics Laboratory, Level 3 RILD building, Royal Devon & Exeter NHS Foundation Trust, Barrack Road, Exeter, EX2 5DW, UK.

Liliya Nazlamova (L)

Faculty of Medicine, University of Southampton, Duthie Building, Southampton General Hospital, Tremona Road, Southampton, SO16 6YD, UK.

Sian Ellard (S)

Exeter Genomics Laboratory, Level 3 RILD building, Royal Devon & Exeter NHS Foundation Trust, Barrack Road, Exeter, EX2 5DW, UK.
University of Exeter Medical School, RILD building, Royal Devon & Exeter NHS Foundation Trust, Barrack Road, Exeter, EX2 5DW, UK.

Ahmed Alfares (A)

Department of Pediatrics, College of Medicine, Qassim University, Qassim, Saudi Arabia.
Department of Pathology and Laboratory Medicine, King Abdulaziz Medical City, Riyadh, Saudi Arabia.

Taghrid Aloraini (T)

Department of Pathology and Laboratory Medicine, King Abdulaziz Medical City, Riyadh, Saudi Arabia.

Lamia AlSubaie (L)

Division of Genetics, Department of Pediatrics, King Abdullah Specialized Children Hospital, King Abdulaziz Medical City, Ministry of National Guard Health Affairs (MNGHA), Riyadh, Saudi Arabia.
King Abdullah International Medical Research Centre, Ministry of National Guard Health Affairs (MNGHA), Riyadh, Saudi Arabia.

Majid Alfadhel (M)

Division of Genetics, Department of Pediatrics, King Abdullah Specialized Children Hospital, King Abdulaziz Medical City, Ministry of National Guard Health Affairs (MNGHA), Riyadh, Saudi Arabia.
King Abdullah International Medical Research Centre, Ministry of National Guard Health Affairs (MNGHA), Riyadh, Saudi Arabia.
King Saud bin Abdulaziz University for Health Sciences, Ministry of National Guard Health Affairs (MNGHA), Riyadh, Saudi Arabia.

Sulaiman Alajaji (S)

King Saud bin Abdulaziz University for Health Sciences, Ministry of National Guard Health Affairs (MNGHA), Riyadh, Saudi Arabia.
Division of Allergy and Clinical Immunology, Department of Pediatrics, King Abdullah Specialized Children Hospital, King Abdulaziz Medical City, Ministry of National Guard Health Affairs (MNGHA), Riyadh, Saudi Arabia.

Htoo A Wai (HA)

Faculty of Medicine, University of Southampton, Duthie Building, Southampton General Hospital, Tremona Road, Southampton, SO16 6YD, UK.

Jay Self (J)

Faculty of Medicine, University of Southampton, Duthie Building, Southampton General Hospital, Tremona Road, Southampton, SO16 6YD, UK.

Andrew G L Douglas (AGL)

Wessex Clinical Genetics Service, Princess Anne Hospital, University Hospital Southampton NHS Foundation Trust, Coxford Rd, Southampton, SO165YA, UK.
Faculty of Medicine, University of Southampton, Duthie Building, Southampton General Hospital, Tremona Road, Southampton, SO16 6YD, UK.

Alexander P Kao (AP)

Zeiss Global Centre, School of Mechanical and Design Engineering, University of Portsmouth, Portsmouth, PO1 3DJ, UK.

Matthew Guille (M)

European Xenopus Resource Centre, University of Portsmouth School of Biological Sciences, King Henry Building, King Henry I Street, Portsmouth, PO1 2DY, UK. matthew.guille@port.ac.uk.

Diana Baralle (D)

Wessex Clinical Genetics Service, Princess Anne Hospital, University Hospital Southampton NHS Foundation Trust, Coxford Rd, Southampton, SO165YA, UK. d.baralle@soton.ac.uk.
Faculty of Medicine, University of Southampton, Duthie Building, Southampton General Hospital, Tremona Road, Southampton, SO16 6YD, UK. d.baralle@soton.ac.uk.

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