Poster Presentation 50th Lorne Proteins Conference 2025

Functional characterization of ataxia-linked mutations in a human glutamate transporter (#342)

Emily Zhou 1 , Kelly Kong 2 , Chelsea Briot 1 , Donald J. van Meyel 2 , Renae M. Ryan 1
  1. School of Medical Sciences, Faculty of Medicine and Health, University of Sydney, Sydney, NSW, Australia
  2. Research Institute of the McGill University Health Centre, Montreal, Quebec, Canada

Episodic ataxia type 6 (EA6) is a rare neurological disease where patients exhibit episodes of symptoms including ataxia, hemiplegia, and migraine. The disease has been linked to mutations in the SLC1A3 gene, which encodes for the human Excitatory Amino Acid Transporter 1 (hEAAT1). These transporters are expressed on glial cells and play a vital role in the reuptake of glutamate from the synapse, preventing glutamate spillover and excitotoxicity1. However, they also exhibit a dual function, where they have the capacity to facilitate chloride flux2. Whilst the pathogenesis of EA6 was previously thought to have been due to dysfunction in the glutamate transport function of the transporter, recent work suggests the disease is likely to be caused by dysfunction in the chloride channel function of the transporter3.

In this study, we have functionally characterized and investigated four hEAAT1 patient-derived variants linked to EA6 both in vitro and in vivo. Wild type and mutant hEAAT1 transporters were expressed in Xenopus laevis oocytes and two-electrode voltage clamp electrophysiology was used to assess transport and chloride channel properties. These mutations exhibited dysfunctions in the chloride channel, with no effect on glutamate transport. Two mutant transporters demonstrated an increase in chloride flux, whilst the other two demonstrated a decrease in chloride flux. These variants were also investigated in vivo in a Drosophila melanogaster behavioural model, where it was observed that these mutations appeared to cause an ataxia phenotype in the larvae. Overall, the results, combined with the results of previously characterized ataxia-linked mutations, suggests the pathogenesis of EA6 is due to dysfunction of the hEAAT1 chloride channel function leading to disruption of chloride homeostasis in glial cells.

References:

  1. Vandenberg, R.J. & Ryan, R.M. Mechanisms of glutamate transport. Physiological reviews 93, 1621-1657 (2013).
  2. Chen, I., Wu, Q., Font, J. & Ryan, R.M. The twisting elevator mechanism of glutamate transporters reveals the structural basis for the dual transport-channel functions. Current Opinion in Structural Biology 75, 102405 (2022).
  3. Wu, Q., et al. Ataxia-linked SLC1A3 mutations alter EAAT1 chloride channel activity and glial regulation of CNS function. The Journal of Clinical Investigation 132 (2022).