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Caveolin-1 Sensitivity of Excitatory Amino Acid Transporters EAAT1, EAAT2, EAAT3, and EAAT4

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Abstract

Excitatory amino acid transporters EAAT1 (SLC1A3), EAAT2 (SLC1A2), EAAT3 (SLC1A1), and EAAT4 (SLC1A6) serve to clear l-glutamate from the synaptic cleft and are thus important for the limitation of neuronal excitation. EAAT3 has previously been shown to form complexes with caveolin-1, a major component of caveolae, which participate in the regulation of transport proteins. The present study explored the impact of caveolin-1 on electrogenic transport by excitatory amino acid transporter isoforms EAAT1-4. To this end cRNA encoding EAAT1, EAAT2, EAAT3, or EAAT4 was injected into Xenopus oocytes without or with additional injection of cRNA encoding caveolin-1. The l-glutamate (2 mM)-induced inward current (I Glu) was taken as a measure of glutamate transport. As a result, I Glu was observed in EAAT1-, EAAT2-, EAAT3-, or EAAT4-expressing oocytes but not in water-injected oocytes, and was significantly decreased by coexpression of caveolin-1. Caveolin-1 decreased significantly the maximal transport rate. Treatment of EAATs-expressing oocytes with brefeldin A (5 µM) was followed by a decrease in conductance, which was similar in oocytes expressing EAAT together with caveolin-1 as in oocytes expressing EAAT1-4 alone. Thus, caveolin-1 apparently does not accelerate transporter protein retrieval from the cell membrane. In conclusion, caveolin-1 is a powerful negative regulator of the excitatory glutamate transporters EAAT1, EAAT2, EAAT3, and EAAT4.

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Acknowledgments

The authors acknowledge the meticulous preparation of the manuscript by Tanja Loch and Lejla Subasic as well as technical support by Elfriede Faber. This study was supported by the Deutsche Forschungsgemeinschaft, Grant-Number: GRK 1302, SFB 773 B4/A1, and La 315/13-3.

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  1. Department of Physiology I, University of Tübingen, Gmelinstr. 5, 72076, Tübingen, Germany

    Abeer Abousaab, Jamshed Warsi, Bernat Elvira & Florian Lang

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  1. Abeer Abousaab
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Correspondence to Florian Lang.

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This article does not contain any studies with human participants performed by any of the authors. All animal experiments conform with the ‘European Convention for the Protection of Vertebrate Animals used for Experimental and other Scientific Purposes’ (Council of Europe No 123, Strasbourg 1985) and were conducted according to the German law for the welfare of animals. The surgical procedures on the adult Xenopus laevis frogs were reviewed and approved by the respective government authority of the state Baden-Württemberg (Regierungspräsidium) prior to the start of the study (Anzeige für Organentnahme nach §36).

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Abousaab, A., Warsi, J., Elvira, B. et al. Caveolin-1 Sensitivity of Excitatory Amino Acid Transporters EAAT1, EAAT2, EAAT3, and EAAT4. J Membrane Biol 249, 239–249 (2016). https://doi.org/10.1007/s00232-015-9863-0

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