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Blockade of amiloride-sensitive sodium channels alters multiple components of the mammalian electroretinogram

Published online by Cambridge University Press:  02 June 2005

LAURA M. BROCKWAY ,
DALE J. BENOS ,
KENT T. KEYSER  and
TIMOTHY W. KRAFT
LAURA M. BROCKWAY
Affiliation:
Vision Science Research Center, University of Alabama at Birmingham, Birmingham
DALE J. BENOS
Affiliation:
Department of Physiology and Biophysics, University of Alabama at Birmingham, Birmingham
KENT T. KEYSER
Affiliation:
Vision Science Research Center, University of Alabama at Birmingham, Birmingham
TIMOTHY W. KRAFT
Affiliation:
Vision Science Research Center, University of Alabama at Birmingham, Birmingham Department of Physiological Optics, University of Alabama at Birmingham, Birmingham
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Abstract

Retinal neurons and Müller cells express amiloride-sensitive Na+ channels (ASSCs). Although all major subunits of these channels are expressed, their physiological role is relatively unknown in this system. In the present study, we used the electroretinogram (ERG) recorded from anesthetized rabbits and isolated rat and rabbit retina preparations to investigate the physiological significance of ASSCs in the retina. Based upon our previous study showing expression of α-ENaC and functional amiloride-sensitive currents in rabbit Müller cells, we expected changes in Müller cell components of the ERG. However, we observed changes in other components of the ERG as well. The presence of amiloride elicited changes in all major components of the ERG; the a-wave, b-wave, and d-wave (off response) were enhanced, while there was a reduction in the amplitude of the Müller cell response (slow PIII). These results suggest that ASSCs play an important role in retinal function including neuronal and Müller cell physiology.

Keywords

RetinaMüller cellSlow PIIIEpithelial sodium channelAcid-sensing ion channel
Type
Research Article
Information
Visual Neuroscience , Volume 22 , Issue 2 , March 2005 , pp. 143 - 151
Copyright
© 2005 Cambridge University Press

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References

REFERENCES

Baylor, D.A., Nunn, B.J., & Schnapf, J.L. (1984). The photocurrent, noise, and spectral sensitivity of rods of the monkey Macaca fascicularis. Journal of Physiology (London) 357, 575–607.CrossRefGoogle Scholar
Bowmaker, J.K., Dartnall, H.J., & Mollon, J.D. (1980). Microspectrophotometric demonstration of four classes of photoreceptor in an old world primate, Macaca fascicularis. Journal of Physiology (London) 298, 131–143.CrossRefGoogle Scholar
Brockway, L.M., Zhou, Z.H., Bubien, J.K., Jovov, B., Benos, D.J., & Keyser, K.T. (2002). Rabbit retinal neurons and glia express a variety of ENaC/DEG subunits. American Journal of Physiology—Cell Physiology 283, C126–C134Google Scholar
Chang, S.S., Grunder, S., Hanukoglu, A., Rosler, A., Mathew, P.M., Hanukoglu, I., Schild, L., Lu, Y., Shimkets, R.A., Nelson-Williams, C., Rossier, B.C., & Lifton, R.P. (1996). Mutations in subunits of the epithelial sodium channel cause salt wasting with hyperkalaemic acidosis, pseudohypoaldosteronism type 1. Nature Genetics 12, 248–253.CrossRefGoogle Scholar
Chen, C.C., Zimmer, A., Sun, W.H., Hall, J., & Brownstein, M.J. (2002). A role for ASIC3 in the modulation of high-intensity pain stimuli. Proceedings of the National Academy of Sciences of the U.S.A. 99, 8992–8997.CrossRefGoogle Scholar
Dartnall, H.J.A. (1972). Photosensitivity. In Handbook of Sensory Physiology: Photochemistry of Vision, ed. Dartnall, H.J.A., pp. 122–145. New York: Springer-Verlag.CrossRef
de Weille, J. & Bassilana, F. (2001). Dependence of the acid-sensitive ion channel, ASIC1a, on extracellular Ca2+ ions. Brain Research 900, 277–281.CrossRefGoogle Scholar
Dick, E. & Miller, R.F. (1985). Extracellular K+ activity changes related to electroretinogram components. I. Amphibian (I-type) retinas. Journal of General Physiology 85, 885–909.Google Scholar
Dong, C.-J. & Hare, W.A. (2002). GABAc feedback pathway modulates the amplitude and kinetics of ERG b-wave in a mammalian retina in vivo. Vision Research 42, 1081–1087.CrossRefGoogle Scholar
Ettaiche, M., Guy, N., Hofman, P., Lazdunski, M., & Waldmann, R. (2004). Acid-sensing ion channel 2 is important for retinal function and protects against light-induced retinal degeneration. Journal of Neuroscience 24, 1005–1012.Google Scholar
Frishman, L.J. & Steinberg, R.H. (1989). Intraretinal analysis of the threshold dark-adapted ERG of cat retina. Journal of Neurophysiology 61, 1221–1232.Google Scholar
Golestaneh, N., de Kozak, Y., Klein, C., & Mirshahi, M. (2001). Epithelial sodium channel and the mineralcorticoid receptor in cultured rat Müller glial cells. Glia 33, 160–168.3.0.CO;2-4>CrossRefGoogle Scholar
Green, D.G. & Kapousta-Bruneau, N.V. (1999). A dissection of the electroretinogram from the isolated rat retina with microelectrodes and drugs. Visual Neuroscience 16, 727–741.Google Scholar
Gurevich, L. & Slaughter, M.M. (1993). Comparison of the waveforms of the ON bipolar neuron and the b-wave of the electroretinogram. Visual Neuroscience 33, 2431–2435.Google Scholar
Karwoski, C.J., Lu, H.K., & Newman, E.A. (1989). Spatial buffering of light-evoked potassium increases by retinal Muller (glial) cells. Science 244, 578–580.CrossRefGoogle Scholar
Kellenberger, S. & Schild, L. (2002). Epithelial sodium channel/degenerin family of ion channels: A variety of functions for a shared structure. Physiological Reviews 82, 735–767.CrossRefGoogle Scholar
Lilley, S., LeTissier, P., & Robbins, J. (2004). The discovery and characterization of a proton-gated sodium current in rat retinal ganglion cells. Journal of Neuroscience 24, 1013–1022.Google Scholar
Lyubarsky, A.L. & Pugh, E.N., Jr. (1996). Recovery phase of the murine rod photoresponse reconstructed from electroretinographic recordings. Journal of Neuroscience 16, 563–571.Google Scholar
Matsuo, T. (1998). Expression of amiloride-sensitive sodium channel in rat eye. Acta Medica Okayama 52, 279–283.Google Scholar
Mirshahi, M., Nicolas, C., Mirshahi, S., Golestaneh, N., d'Hermies, F., & Agarwal, M.K. (1999). Immunohistochemical analysis of the sodium channel in rodent and human eye. Experimental Eye Research 69, 21–32.CrossRefGoogle Scholar
Newman, E.A. (1985). Membrane physiology of retinal glial (Muller) cells. Journal of Neuroscience 5, 2225–2239.Google Scholar
Newman, E.A., Frambach, D.A., & Odette, L.L. (1984). Control of extracellular potassium levels by retinal glial cell K+ siphoning. Science 225, 1174–1175.CrossRefGoogle Scholar
Oakley, B. & Green, D.G. (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
Penn, R.D. & Hagins, W.A. (1969). Signal transmission along retinal rods and the origin of the electroretinographic a-wave. Nature 223, 201–204.CrossRefGoogle Scholar
Stockton, R.A. & Slaughter, M.M. (1989). B-wave of the electroretinogram. A reflection of ON bipolar cell activity. Journal of General Physiology 93, 101–122.Google Scholar
Tucker, G.S., Hamasaki, D.I., Labbie, A., & Bradford, N. (1982). Physiologic and anatomic development of the photoreceptors of normally-reared and dark-reared rabbits. Experimental Brain Research 48, 263–271.Google Scholar
Waldmann, R., Bassilana, F., de Weille, J., Champigny, G., Heurteaux, C., & Lazdunski, M. (1997). Molecular cloning of a non-inactivating proton-gated Na+ channel specific for sensory neurons. Journal of Biological Chemistry 272, 20975–20978.CrossRefGoogle Scholar
Warnock, D.G. (2001). Genetic forms of human hypertension. Current Opinion in Nephrology and Hypertension 10, 493–499.CrossRefGoogle Scholar
Yan, K. & Matthews, G. (1992). Blockers of potassium channels reduce the outward dark current in rod photoreceptor inner segments. Visual Neuroscience 8, 479–481.CrossRefGoogle Scholar
Yang, Z. & Jiang, C. (1999). Opposite effects of pH on open-state probability and single channel conductance of Kir4.1 channels. Journal of Physiology 520, 921–927.Google Scholar
Zhang, X., Wensel, T.G., & Kraft, T.W. (2003). GTPase regulators and photoresponses in cones of the eastern chipmunk. Journal of Neuroscience 23, 1287–1297.Google Scholar