Publication Date

4-6-2023

Journal

American Journal of Human Genetics

DOI

10.1016/j.ajhg.2023.03.001

PMID

36965478

PMCID

PMC10119142

PubMedCentral® Posted Date

3-24-2023

PubMedCentral® Full Text Version

Post-print

Published Open-Access

yes

Keywords

Paraparesis, Spastic, Humans, Alternative Splicing, DNA-Binding Proteins, Transcription Factors, HeLa Cells, Protein Isoforms, RNA-Seq, Male, Female, Pedigree, Alleles, Infant, Child, Preschool, Child, Adolescent, Protein Structure, Secondary, RNA, Small Nuclear, gene discovery, Mendelian disorder, progressive spasticity, alternative splicing, spliceosome, rare diseases, monogenic diseases

Abstract

The vast majority of human genes encode multiple isoforms through alternative splicing, and the temporal and spatial regulation of those isoforms is critical for organismal development and function. The spliceosome, which regulates and executes splicing reactions, is primarily composed of small nuclear ribonucleoproteins (snRNPs) that consist of small nuclear RNAs (snRNAs) and protein subunits. snRNA gene transcription is initiated by the snRNA-activating protein complex (SNAPc). Here, we report ten individuals, from eight families, with bi-allelic, deleterious SNAPC4 variants. SNAPC4 encoded one of the five SNAPc subunits that is critical for DNA binding. Most affected individuals presented with delayed motor development and developmental regression after the first year of life, followed by progressive spasticity that led to gait alterations, paraparesis, and oromotor dysfunction. Most individuals had cerebral, cerebellar, or basal ganglia volume loss by brain MRI. In the available cells from affected individuals, SNAPC4 abundance was decreased compared to unaffected controls, suggesting that the bi-allelic variants affect SNAPC4 accumulation. The depletion of SNAPC4 levels in HeLa cell lines via genomic editing led to decreased snRNA expression and global dysregulation of alternative splicing. Analysis of available fibroblasts from affected individuals showed decreased snRNA expression and global dysregulation of alternative splicing compared to unaffected cells. Altogether, these data suggest that these bi-allelic SNAPC4 variants result in loss of function and underlie the neuroregression and progressive spasticity in these affected individuals.

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Graphical Abstract

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