Neuron-glial trafficking of NH4+ and K+: separate routes of uptake into glial cells of bee retina

Marcaggi, P., Jeanne, M. and Coles, J. A. (2004) Neuron-glial trafficking of NH4+ and K+: separate routes of uptake into glial cells of bee retina. European Journal of Neuroscience, 19(4), pp. 966-976. (doi: 10.1111/j.0953-816X.2004.03165.x)

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Publisher's URL: http://dx.doi.org/10.1111/j.0953-816X.2004.03165.x

Abstract

Ammonium (NH<sub>4</sub><sup>+</sup> and/or NH<sub>3</sub>) and K<sup>+</sup> are released from active neurons and taken up by glial cells, and can modify glial cell behaviour. Study of these fluxes is most advanced in the retina of the honeybee drone, which consists essentially of identical neurons (photoreceptors) and identical glial cells (outer pigment cells). In isolated bee retinal glial cells, ammonium crosses the membrane as NH<sub>4</sub><sup>+</sup> on a Cl<sup>−</sup> cotransporter. We have now investigated, in the more physiological conditions of a retinal slice, whether the NH<sub>4</sub><sup>+</sup> on a Cl<sup>−</sup> cotransporter can transport K<sup>+</sup> and whether the major K<sup>+</sup> conductance can transport NH<sub>4</sub><sup>+</sup>. We increased [NH<sub>4</sub><sup>+</sup>] or [K<sup>+</sup>] in the superfusate and monitored uptake by recording from the glial cell syncytium or from interstitial space with microelectrodes selective for H<sup>+</sup> or K<sup>+</sup> . In normal superfusate solution, ammonium acidified the glial cells but, after 6 min superfusion in low [Cl<sup>−</sup>] solution, ammonium alkalinized them. In the same low [Cl<sup>−</sup>] conditions, the rise in intraglial [K<sup>+</sup> ] induced by an increase in superfusate [K<sup>+</sup> ] was unchanged, i.e. no K<sup>+</sup> flux on the Cl<sup>−</sup> cotransporter was detected. Ba<sup>2+</sup> (5 mM) abolished the glial depolarization induced by K<sup>+</sup> released from photoreceptors but did not reduce NH<sub>4</sub><sup>+</sup>uptake. We estimate that when extracellular [NH<sub>4</sub><sup>+</sup>] is increased, 62–100% is taken up by the NH<sub>4</sub><sup>+</sup>- Cl<sup>−</sup> cotransporter and that when K<sup>+</sup> is increased, 77–100% is taken up by routes selective for K<sup>+</sup> . This separation makes it possible that the glial uptake of NH<sub>4</sub><sup>+</sup>and of K<sup>+</sup>, and hence their signalling roles, might be regulated separately.

Item Type:Articles
Status:Published
Refereed:Yes
Glasgow Author(s) Enlighten ID:Coles, Dr Jonathan
Authors: Marcaggi, P., Jeanne, M., and Coles, J. A.
College/School:College of Medical Veterinary and Life Sciences > Institute of Infection Immunity and Inflammation
Journal Name:European Journal of Neuroscience
Journal Abbr.:Europ. J. Neurosci.
Publisher:Wiley
ISSN:0953-816X
ISSN (Online):1460-9568

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