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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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References

REFERENCES

Dmitriev, A.V., Govardovskii, V.I., Schwahn, H.N. & Steinberg R.H. (1999). Light-induced changes of extracellular ions and volume in the isolated chick retina-pigment epithelium preparation. Visual Neuroscience 16, 1157–1167.Google Scholar
Gamba, G. (2005). Molecular physiology and pathophysiology of electroneutral cation-chloride cotransporters. Physiological Reviews 85, 423–493.Google Scholar
Gavrikov, K.E., Dmitriev, A.V., Keyser, K.T. & Mangel, S.C. (2003). Cation-chloride cotransporters mediate neural computation in the retina. Proceedings of the National Academy of Sciences of the USA 100, 16047–16052.Google Scholar
Gavrikov, K.E., Nilson, J.E., Dmitriev, A.V., Zucker, C.L. & Mangel S.C. (2006). Dendritic compartmentalization of chloride cotransporters underlies directional responses of starburst amacrine cells in retina. Proceedings of the National Academy of Sciences of the USA 103, 18793–18798.Google Scholar
Gosmanov, A.R., Lindinger, M.I. & Thomason, D.B. (2003). Riding the tides: K+ concentration and volume regulation by muscle Na+-K+-2Cl− cotransport activity. News in Physiological Sciences 18, 196–200.Google Scholar
Govardovskii, V.I., Li, J.-D., Dmitriev, A.V & Steinberg, R.H. (1994). Mathematical model of TMA+ diffusion and prediction of light-dependent subretinal hydration in chick retina. Investigative Ophthalmology & Visual Science 35, 2712–2724.Google Scholar
Hanitzsch, R. (1973). Intraretinal isolation of P3 subcomponents in the isolated rabbit retina after treatment with sodium aspartate. Vision Research 13, 2093–2102.Google Scholar
Karwoski, C.J., Frambach, D.A. & Proenza, L.M. (1985). Laminar profile of resistivity in frog retina. Journal of Neurophysiology 54, 1607–1619.Google Scholar
Kuffler, S.W. (1967). Neuroglial cells: Physiological properties and a potassium mediated effect on the glial membrane potential. Proceedings of the Royal Society. B, Biological Sciences 168, 1–21.Google Scholar
Kuntz, C.A., Crook, R.B., Dmitriev, A.V. & Steinberg, R.H. (1994). Modification by cyclic adenosine monophosphate of basolateral membrane chloride conductance in chick retinal pigment epithelium. Investigative Ophthalmology & Visual Science 35, 422–433.Google Scholar
Li, J.-D., Gallemore, R.P., Dmitriev, A.V. & Steinberg R.H. (1994). Light-dependent hydration of the space surrounding photoreceptors in chick retina. Investigative Ophthalmology & Visual Science 35, 2700–2711.Google Scholar
Lytle, C., Xu, J.C., Biemesderfer, D. & Forbush, B. (1995). Distribution and diversity of Na-K-Cl cotransport proteins: A study with monoclonal antibodies. American Journal of Physiology 269, C1496–C1505.Google Scholar
Maksay, G., Korpi, E.R. & Uusi-Oukari, M. (1998). Bimodal action of furosemide on convulsant [3H] EBOB binding to cerebellar and cortical GABAA receptors. Neurochemistry International 33, 353–358.Google Scholar
Miller, R.F. & Dacheux, R.F. (1976). Synaptic organization and ionic basis of On and Off channels in mudpuppy retina. I. Intracellular analysis of chloride-sensitive electrogenic properties of receptors, horizontal cells, bipolar cells, and amacrine cell. Journal of General Physiology 67, 639–659.Google Scholar
Miller, R.F. & Dacheux, R.F. (1983). Intracellular chloride in retinal neurons: Measurement and meaning. Vision Research 23, 399–411.Google Scholar
Nicholson, C. & Sykova, E. (1998). Extracellular space structure revealed by diffusion analysis. Trends in Neurosciences 21, 207–215.Google Scholar
Oakley, B. & Green, D.C. (1976). Correlation of light-induced changes in retinal extracellular potassium concentration with c-wave of the electroretinogram. Journal of Neurophysiology 39, 1117–1133.Google Scholar
Payne, J.A., Rivera, C., Voipio, J. & Kaila, K. (2003). Cation-chloride co-transporters in neuronal communication, development and trauma. Trends in Neurosciences 26, 199–206.Google Scholar
Russell, J.M. (2000). Sodium-potassium-chloride cotransport. Physiological Reviews 80, 211–276.Google Scholar
Vardi, N., Zhang, L.L., Payne, J.A. & Sterling, P. (2000). Evidence that different cation chloride cotransporters in retinal neurons allow opposite responses to GABA. Journal of Neuroscience 20, 7657–7663.Google Scholar
Vu, T.Q., Payne, J.A. & Copenhagen, D.R. (2000). Localization and developmental expression patterns of the neuronal K-Cl cotransporter (KCC2) in the rat retina. Journal of Neuroscience 20, 1414–1423.Google Scholar
Williams, J.R., Sharp, J.W., Kumari, V.G., Wilson, M. & Payne, J.A. (1999). The neuron-specific K-Cl cotransporter, KCC2. Journal of Biological Chemistry 274, 12656–12664.Google Scholar
Witkovsky, P., Dudek, F.E. & Ripps, H. (1975). Slow PIII component of the carp electroretinogram. Journal of General Physiology 65, 119–134.Google Scholar