ORCID

0000-0002-6611-9616

Date of Award

5-7-2024

Author's School

Graduate School of Arts and Sciences

Author's Department

Biology & Biomedical Sciences (Molecular Cell Biology)

Degree Name

Doctor of Philosophy (PhD)

Degree Type

Dissertation

Abstract

UBE3A is a HECT (homologous to E6AP-Terminus) domain E3 ubiquitin ligase that targets substrate proteins for polyubiquitination and subsequent degradation through the ubiquitin-proteasome pathway. The UBE3A gene is of unique interest for its gene dosage-dependent effect in the developing brain: deletion of the maternal copy of UBE3A causes a severe intellectual disability known as Angelman syndrome; meanwhile, duplication or triplication of the genomic region containing UBE3A is linked to a prevalent syndromic form of autism known as Dup15q syndrome. However, little is known about the effects of missense variants which cause a single amino acid change in the resulting UBE3A enzyme, and predicting the disease outcome for a given variant remains a challenge. In this thesis work, I posed the hypothesis that investigating variants’ effects on UBE3A functional activity levels is critical for predicting disease. Here, I describe the use of a high throughput assay to screen functional consequences of UBE3A missense variants. Through this screen, we identified a novel subclass of UBE3A gain of function variants with hyperactive enzyme activity. Through collaboration with clinical centers, we confirmed that individuals possessing hyperactivating UBE3A variants exhibited phenotypes that were distinguishable from Angelman syndrome. For this thesis work, I focused on a specific strong gain of function variant – the Q588E variant – whose activity levels are 388% of wild-type (WT) UBE3A. First, structure-function analysis revealed that Q588 forms a regulatory site in UBE3A that is conserved among HECT domain ubiquitin ligases and perturbed in various neurodevelopmental disorders. Next, I established a mouse model of the hyperactive Q588E variant (Q606E in mouse) and showed that the presence of this variant is sufficient to cause early developmental disease phenotypes. Finally, I focused on deep characterization of disease in this mouse model. Extensive behavioral testing in adult mice revealed motor deficits, hypoactivity, and deficits in stereotypic behaviors, but no changes in readouts of social, anxiety, or cognitive deficits. Mice harboring the hyperactive variant displayed global microcephaly that was acquired during postnatal development. Finally, proteomic analysis revealed changes in key proteins and protein pathways related to neurodevelopmental disease. Importantly, these phenotypic outcomes differed from previous findings in both Angelman syndrome mouse models and a model of a weak gain of function variant in UBE3A, supporting that the strength of UBE3A gain-of-function changes the type and severity of aberrant phenotypes. Finally, these findings have broad implications for the heterogeneous phenotypes observed in individuals with UBE3A gain-of-function variants.

Language

English (en)

Chair and Committee

Jason Yi

Available for download on Saturday, April 26, 2025

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