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The Journal of Neuroscience, July 12, 2006, 26(28):7513-7522; doi:10.1523/JNEUROSCI.4545-05.2006

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Cellular/Molecular
Intersubunit Interactions in EAAT4 Glutamate Transporters

Delany Torres-Salazar1,2 and Christoph Fahlke1,2,3,4

1Abteilung Neurophysiologie, Medizinische Hochschule, 30625 Hannover, Germany, 2Abteilung Physiologie, Rheinisch-Westfälische Technische Hochschule Aachen, 52074 Aachen, Germany, 3Centro de Estudios Cientificos, Valdivia 509000, Chile, and 4Zentrum für Systemische Neurowissenschaften, 30559 Hannover, Germany

Correspondence should be addressed to Christoph Fahlke, Abteilung Neurophysiologie, Medizinische Hochschule Hannover, Carl-Neuberg-Strasse 1, D-30625 Hannover, Germany. Email: fahlke.christoph{at}mh-hannover.de

Excitatory amino acid transporters (EAATs) play a central role in the termination of synaptic transmission and in extracellular glutamate homeostasis in the mammalian CNS. A functional transporter is assembled as oligomer consisting of three subunits, each of which appears to transport glutamate independently from the neighboring subunits. EAATs do not only sustain a secondary-active glutamate transport but also function as anion channel. We here address the question whether intersubunit interactions play a role in pore-mediated anion conduction. We expressed a neuronal isoform, EAAT4, heterologously in Xenopus oocytes and mammalian cells and measured glutamate flux and anion currents under various concentrations of Na+ and glutamate. EAAT4 anion channels are active in the absence of both substrates, and increasing concentrations activate EAAT4 anion currents with a sigmoidal concentration dependence. Because only one glutamate molecule is cotransported per uptake cycle, the cooperativity between glutamate binding sites most likely arises from an interaction between different carrier domains. This interaction is modified by two point mutations close to the putative glutamate binding site, G464S and Q467S. Both mutations alter the dissociation constants and Hill coefficient of the substrate dependence of anion currents, leaving the concentration dependence of glutamate uptake unaffected. Our results demonstrate that glutamate carriers cooperatively interact during anion channel activation.

Key words: glutamate transporter; chloride channel; synaptic transmission; patch clamp; neurotransmitter; cell excitability

Received Oct. 24, 2005; revised May 9, 2006; accepted June 8, 2006.

Correspondence should be addressed to Christoph Fahlke, Abteilung Neurophysiologie, Medizinische Hochschule Hannover, Carl-Neuberg-Strasse 1, D-30625 Hannover, Germany. Email: fahlke.christoph{at}mh-hannover.de


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