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Multiple functions of cation-chloride cotransporters in the fish retina

Published online by Cambridge University Press:  28 September 2007

ANDREY V. DMITRIEV ,
NINA A. DMITRIEVA ,
KENT T. KEYSER  and
STUART C. MANGEL
ANDREY V. DMITRIEV
Affiliation:
Department of Neuroscience, The Ohio State University College of Medicine, Columbus, Ohio
NINA A. DMITRIEVA
Affiliation:
Department of Neurological Surgery, The Ohio State University College of Medicine, Columbus, Ohio Department of Vision Sciences and the Vision Science Research Center, University of Alabama at Birmingham, Birmingham, Alabama
KENT T. KEYSER
Affiliation:
Department of Vision Sciences and the Vision Science Research Center, University of Alabama at Birmingham, Birmingham, Alabama
STUART C. MANGEL
Affiliation:
Department of Neuroscience, The Ohio State University College of Medicine, Columbus, Ohio
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Abstract

A GABA- or glycine-induced increase in Cl− permeability can produce either a depolarization or hyperpolarization, depending on the Cl− equilibrium potential. It has been shown that retinal neurons express the chloride cotransporters, Na-K-2Cl (NKCC) and K-Cl (KCC), the primary molecular mechanisms that control the intracellular Cl− concentration. We thus studied (1) the localization of these cotransporters in the fish retina, and (2) how suppression of cotransporter activity in the fish retina affects function. Specific antibodies against NKCC and KCC2 revealed that both cotransporters were expressed in the outer and inner plexiform layers, and colocalized in many putative amacrine cells and in cells of the ganglion cell layer. However, the somata of putative horizontal cells displayed only NKCC immunoreactivity and many bipolar cells were only immunopositive for KCC2. In the outer retina, application of bumetanide, a specific inhibitor of NKCC activity, (1) increased the steady-state extracellular concentration of K+ ([K+]o) and enhanced the light-induced decrease in the [K+]o, (2) increased the sPIII photoreceptor-dependent component of the ERG, and (3) reduced the extracellular space volume. In contrast, in the outer retina, application of furosemide, a specific inhibitor of KCC activity, decreased sPIII and the light-induced reduction in [K+]o, but had little effect on steady-state [K+]o. In the inner retina, bumetanide increased the sustained component of the light-induced increase in [K+]o. These findings thus indicate that NKCC and KCC2 control the [K+]o and extracellular space volume in the retina in addition to regulating GABA- and glycine-mediated synaptic transmission. In addition, the anatomical and electrophysiological results together suggest that all of the major neuronal types in the fish retina are influenced by chloride cotransporter activity.

Keywords

Na-K-Cl cotransporterK-Cl cotransporterbumetanidefurosemideextracellular K+extracellular volume
Type
Research Article
Information
Visual Neuroscience , Volume 24 , Issue 4 , July 2007 , pp. 635 - 645
Copyright
© 2007 Cambridge University Press

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