Year of Award

2024

Document Type

Thesis

Degree Type

Master of Science (MS)

Degree Name

Neuroscience

Department or School/College

Division of Biological Sciences

Committee Chair

Michael P. Kavanagh

Commitee Members

Richard Bridges, Kasper Hansen, Beverly Piggott, Katie Holick

Keywords

GABA transport, epilepsy, autism, butyrate

Subject Categories

Molecular and Cellular Neuroscience

Abstract

An increasing number of spontaneous mutations in the GABA transporter gene SLC6A1 (GAT-1) have been associated with pediatric epilepsy and neurodevelopmental disorders. The molecular mechanisms and impact of mutations on GABA homeostasis and neuronal circuit function are poorly understood. Furthermore, there are currently no validated therapeutic approaches to treat patients. A de novo mutation (S295L) in the GABA transporter gene SLC6A1 that was identified in a pediatric patient was introduced into a human cDNA construct, and mutant and wild-type transporters were expressed and studied in Xenopus oocytes by voltage clamp and radiolabeled GABA flux measurement. In addition, the effect of the mutation on behavior and on GABA homeostasis and neuronal signaling was studied in acute cortical slices from transgenic SLC6A1 S295L knock-in mice using patch clamp recording of neurons and by measuring radiolabeled GABA flux in brain tissue from wild-type, heterozygous, and homozygous mutant mice. The S295L mutation caused a profound loss of function in the mutant GABA transporter. Heterologous co-expression of mutant and wild-type transporter showed no dominant negative effect of the mutation. Consistent with this finding, there was a 50% loss of SLC6A1 activity in heterozygous S295L mutant mice. This loss was partially compensated by an increase in SLC6A11 (GAT-3) activity. The dysregulation of GABA homeostasis in the mutant mice resulted in neurophysiological deficits including abnormal burst spiking and impaired hippocampal synaptic plasticity.

We tested the ability of 4-phenylbutyrate, an FDA-approved drug reported to act as a chemical chaperone, to rescue impaired GABA uptake and homeostasis by increasing surface trafficking. We found that the drug instead acted as a direct allosteric activator of SLC6A1 and SLC6A11. Notably, addition of low millimolar concentrations of sodium butyrate to acute brain slices from heterozygous mutant animals restored GABA uptake to normal wild-type levels. We demonstrate that a series of fatty acids and analogs unexpectedly act as positive allosteric modulators (PAMs) of human SLC6A1 and SLC6A11 in vitro. This mouse preclinical model is likely representative of many de novo SLC6A1 loss-of-function mutations, suggesting that fatty acid-based PAMs should be further evaluated as a potential therapeutic approach for SLC6A1 disease.

Available for download on Friday, June 20, 2025

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© Copyright 2024 Alessandra G. Jester