Expanding the genotype-phenotype landscape of PDE10A-associated movement disorders.


Journal

Parkinsonism & related disorders
ISSN: 1873-5126
Titre abrégé: Parkinsonism Relat Disord
Pays: England
ID NLM: 9513583

Informations de publication

Date de publication:
03 2023
Historique:
received: 25 11 2022
revised: 08 02 2023
accepted: 10 02 2023
pubmed: 23 2 2023
medline: 8 3 2023
entrez: 22 2 2023
Statut: ppublish

Résumé

Phosphodiesterase 10A (PDE10A) controls body movements by regulating cyclic adenosine monophosphate signaling in the basal ganglia. Two classes of PDE10A variants are reported with distinctive genotype-phenotype correlation. The autosomal recessive mutations in the GAF-A and catalytic domains are associated with compromised membrane localization, and manifest with infantile onset chorea, developmental, and cognition delay with normal brain MRI. Conversely, autosomal dominant mutations in the GAF-B domain cause protein aggregates which results in childhood onset chorea in the context of normal cognition and development, with striatal lesions. Phenotypic characteristics of affected individuals with PDE10A mutations belonging to a single family were recorded. In addition, Sanger sequencing and in silico analysis were used to identify the mutations. Homozygosity mapping was applied together with whole exome sequencing. Four individuals from a consanguineous family affected with PDE10A mutations were observed for up to 40 years. Although these individuals displayed a clinical phenotype attributed to the recessive GAF-A mutations, they revealed a bi-allelic GAF-B mutation (c.883G > A:p. D295 N; p.Asp295Asn) that was segregated with all affected individuals. In addition to chorea, we observed peculiar foot deformities and pronounced social phobia, with normal brain MRI. In silico structural analysis suggested that the GAF-B mutation blocked allosteric PDE10A activation. The resulting lack of PDE10A activity likely phenocopies GAF-A mutations, and this is achieved through a distinct mechanism. Collectively, our findings demonstrate the association of recessive and dominant phenotypes of known variants, and further expands the genotype-phenotype landscape of PDE10A-associated movement disorders.

Sections du résumé

BACKGROUND
Phosphodiesterase 10A (PDE10A) controls body movements by regulating cyclic adenosine monophosphate signaling in the basal ganglia. Two classes of PDE10A variants are reported with distinctive genotype-phenotype correlation. The autosomal recessive mutations in the GAF-A and catalytic domains are associated with compromised membrane localization, and manifest with infantile onset chorea, developmental, and cognition delay with normal brain MRI. Conversely, autosomal dominant mutations in the GAF-B domain cause protein aggregates which results in childhood onset chorea in the context of normal cognition and development, with striatal lesions.
METHODS
Phenotypic characteristics of affected individuals with PDE10A mutations belonging to a single family were recorded. In addition, Sanger sequencing and in silico analysis were used to identify the mutations. Homozygosity mapping was applied together with whole exome sequencing.
RESULTS
Four individuals from a consanguineous family affected with PDE10A mutations were observed for up to 40 years. Although these individuals displayed a clinical phenotype attributed to the recessive GAF-A mutations, they revealed a bi-allelic GAF-B mutation (c.883G > A:p. D295 N; p.Asp295Asn) that was segregated with all affected individuals. In addition to chorea, we observed peculiar foot deformities and pronounced social phobia, with normal brain MRI. In silico structural analysis suggested that the GAF-B mutation blocked allosteric PDE10A activation. The resulting lack of PDE10A activity likely phenocopies GAF-A mutations, and this is achieved through a distinct mechanism.
CONCLUSIONS
Collectively, our findings demonstrate the association of recessive and dominant phenotypes of known variants, and further expands the genotype-phenotype landscape of PDE10A-associated movement disorders.

Identifiants

pubmed: 36805523
pii: S1353-8020(23)00046-9
doi: 10.1016/j.parkreldis.2023.105323
pii:
doi:

Substances chimiques

Phosphoric Diester Hydrolases EC 3.1.4.-
PDE10A protein, human EC 3.1.4.-

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

105323

Informations de copyright

Copyright © 2023 Elsevier Ltd. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of competing interest The authors report no competing or conflict of interests.

Auteurs

Saeed Bohlega (S)

Movement Disorders Program, Neuroscience Centre, King Faisal Specialist Hospital and Research Centre (KFSH&RC), Riyadh, Kingdom of Saudi Arabia. Electronic address: boholega@kfshrc.edu.sa.

Ali H Abusrair (AH)

Movement Disorders Program, Neuroscience Centre, King Faisal Specialist Hospital and Research Centre (KFSH&RC), Riyadh, Kingdom of Saudi Arabia.

Zainah Al-Qahtani (Z)

Movement Disorders Program, Neuroscience Centre, King Faisal Specialist Hospital and Research Centre (KFSH&RC), Riyadh, Kingdom of Saudi Arabia.

Francisco J Guzmán-Vega (FJ)

Bioscience Program, Biological and Environmental Science and Engineering Division, King Abdullah University of Science and Technology (KAUST), Thuwal, Kingdom of Saudi Arabia; Computational Biology Research Center, King Abdullah University of Science and Technology, (KAUST), Thuwal, Kingdom of Saudi Arabia.

Reshmi Ramakrishnan (R)

Bioscience Program, Biological and Environmental Science and Engineering Division, King Abdullah University of Science and Technology (KAUST), Thuwal, Kingdom of Saudi Arabia; Computational Biology Research Center, King Abdullah University of Science and Technology, (KAUST), Thuwal, Kingdom of Saudi Arabia.

Haya Aldosari (H)

Department of Genetics, Research Centre, King Faisal Specialist Hospital and Research Centre (KFSH&RC), Riyadh, Kingdom of Saudi Arabia.

Amaal Aldakheel (A)

Movement Disorders Program, Neuroscience Centre, King Faisal Specialist Hospital and Research Centre (KFSH&RC), Riyadh, Kingdom of Saudi Arabia.

Salma Al-Qahtani (S)

Movement Disorders Program, Neuroscience Centre, King Faisal Specialist Hospital and Research Centre (KFSH&RC), Riyadh, Kingdom of Saudi Arabia.

Dorota Monies (D)

Department of Genetics, Research Centre, King Faisal Specialist Hospital and Research Centre (KFSH&RC), Riyadh, Kingdom of Saudi Arabia.

Stefan T Arold (ST)

Bioscience Program, Biological and Environmental Science and Engineering Division, King Abdullah University of Science and Technology (KAUST), Thuwal, Kingdom of Saudi Arabia; Computational Biology Research Center, King Abdullah University of Science and Technology, (KAUST), Thuwal, Kingdom of Saudi Arabia; Centre de Biologie Structurale (CBS), INSERM, CNRS, Université de Montpellier, F-34090, Montpellier, France.

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