Publication Date

3-7-2024

Journal

American Journal of Human Genetics

DOI

10.1016/j.ajhg.2024.01.007

PMID

38325380

PMCID

PMC10940019

PubMedCentral® Posted Date

2-6-2024

PubMedCentral® Full Text Version

Post-print

Published Open-Access

yes

Keywords

Male, Female, Animals, Humans, Intellectual Disability, Zebrafish, Mutation, Missense, Transcription Factors, Hyperparathyroidism, Phenotype, Neurodevelopmental Disorders, behavioral problems, congenital anomalies, de novo mutation, developmental delay, hyperparathyroidism, hypotonia, intellectual disability, transcription factor, X-linked, ZFX, zinc finger

Abstract

Pathogenic variants in multiple genes on the X chromosome have been implicated in syndromic and non-syndromic intellectual disability disorders. ZFX on Xp22.11 encodes a transcription factor that has been linked to diverse processes including oncogenesis and development, but germline variants have not been characterized in association with disease. Here, we present clinical and molecular characterization of 18 individuals with germline ZFX variants. Exome or genome sequencing revealed 11 variants in 18 subjects (14 males and 4 females) from 16 unrelated families. Four missense variants were identified in 11 subjects, with seven truncation variants in the remaining individuals. Clinical findings included developmental delay/intellectual disability, behavioral abnormalities, hypotonia, and congenital anomalies. Overlapping and recurrent facial features were identified in all subjects, including thickening and medial broadening of eyebrows, variations in the shape of the face, external eye abnormalities, smooth and/or long philtrum, and ear abnormalities. Hyperparathyroidism was found in four families with missense variants, and enrichment of different tumor types was observed. In molecular studies, DNA-binding domain variants elicited differential expression of a small set of target genes relative to wild-type ZFX in cultured cells, suggesting a gain or loss of transcriptional activity. Additionally, a zebrafish model of ZFX loss displayed an altered behavioral phenotype, providing additional evidence for the functional significance of ZFX. Our clinical and experimental data support that variants in ZFX are associated with an X-linked intellectual disability syndrome characterized by a recurrent facial gestalt, neurocognitive and behavioral abnormalities, and an increased risk for congenital anomalies and hyperparathyroidism.

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