Skip to main content
×
Home

Evidence for calcium/calmodulin dependence of spinule retraction in retinal horizontal cells

  • Yvonne Schmitz (a1), Konrad Kohler (a1) and Eberhart Zrenner (a1)
Abstract
Abstract

Horizontal cells of the carp retina alter their synaptic connections with cones during dark and light adaptation. At light onset, dendrites of horizontal cells, which are positioned laterally at the ribbon synapse, form “spinules,” little processes with membrane densities. Spinules are retracted again during dark adaptation. Spinule retraction is also elicited upon glutamate application to the retina. In the present study, we address the question whether calcium/calmodulin-dependent pathways are involved in dark- and glutamate-evoked spinule retraction. Light-adapted retinas were isolated and subsequently dark adapted during incubation in media of different calcium concentrations. Spinule retraction was clearly blocked in low-calcium solutions (5 μM and 50 nM CaCl2). Incubation in medium containing cobalt chloride (2 mM) had the same effect. Both treatments blocked the glutamate-induced spinule retraction as well. These results indicate that spinule retraction is induced by a calcium influx into horizontal cells. To investigate whether calmodulin, the primary calcium receptor in eukaryotic cells, is present at the site of spinule formation, light- and dark-adapted retinas, embedded in LR White resin, were labelled with an antibody against calmodulin and gold-conjugated secondary antibodies. Horizontal cell dendrites at the ribbon synapse revealed strong calmodulin immunoreactivity, which was more than twice as high in light- as in dark-adapted retinas. The incubation of isolated retinas with the calmodulin antagonists W5 and W13 inhibited spinule retraction. In summary, these results suggest that spinule retraction may be regulated by calcium influx into horizontal cells and subsequent calcium/calmodulin-dependent pathways.

Copyright
References
Hide All
Ascher P. & Nowak L. (1988). Quisqualate and kainate-activated channels in mouse central neurons in culture. Journal of Physiology 399, 227245.
Baylor D.A., Fuortes M.G.F. & O'Bryan P.M. (1971). Receptive fields of single cones in the retina of the turtle. Journal of Physiology 24, 265294.
Behrens U.D., Wagner H.-J. & Kirsch M. (1992). cAMP-mediated second messenger mechanisms are involved in spinule formation in teleost cone horizontal cells. Neuroscience Letters 147, 9396.
Bronstein J.M., Wasterlain C.G., Bok D., Lasher R. & Farber D.B. (1988). Localization of retinal calmodulin kinase. Experimental Eye Research 47, 391402.
Bronstein J.M., Wasterlain C.G., Lasher R. & Farber D.B. (1991). Dark-induced changes in activity and compartmentalization of retinal calmodulin kinase in the rat. Brain Research 495, 8388.
Burkhardt D.A. (1977). Responses and receptive-field organization of cones in perch retinas. Journal of Neurophysiology 40, 5362.
Copenhagen D.R. & Jahr C.E. (1989). Release of endogenous excitatory amino acids from turtle photoreceptors. Nature 341, 536539.
Djamgoz M.B.A., Downing J.E.G., Kirsch M., Prince D.J. & Wagner H.-J. (1988). Plasticity of cone horizontal cell functioning in cyprinid fish retina: Effects of background illumination of moderate intensity. Journal of Neurocytology 17, 701710.
Djamgoz M.B.A., Kirsch M. & Wagner H.-J. (1989). Haloperidol suppresses light-induced spinule formation and biphasic responses of horizontal cells in fish (roach) retina. Neuroscience Letters 107, 200204.
Gilbertson T.A., Scobey R. & Wilson M. (1991). Permeation of calcium ions through non-NMDA glutamate channels in retinal bipolar cells. Science 251, 16131615.
Gnegy M.E. (1993). Calmodulin in neurotransmitter and hormone action. Annual Reviews of Pharmacology and Toxicology 33, 4570.
Hamano K., Kiyama H., Emson P.C., Manabe R., Nakauchi M. & Tohyama M. (1990). Localization of two calcium binding proteins, calbindin (28 kd) and parvalbumin (12 kd), in the vertebrate retina. Journal of Comparative Neurology 302, 417424.
Hankins M.W. & Ruddock K.H. (1984). Hyperpolarization of fish retinal horizontal cells by kainate and quisqualate. Nature 308, 360362.
Hidaka H. & Tanaka T. (1983). Naphthalenesulfonamides as calmodulin antagonists. Methods of Enzymology 102, 185194.
Janssen-Bienhold U., Nagel H. & Weiler R. (1993). In vitro phosphorylation in isolated horizontal cells of the fish retina: Effects of the state of light adaptation. European Journal of Neuroscience 5, 584593.
Kamermans M., Van Dijk H. & Spekreijse H. (1991). Color opponency in cone driven horizontal cells in carp retina. Journal of General Physiology 819, 843.
Kaneko A. & Shimazaki H. (1975). Effects of external ions on the synaptic transmission from photoreceptors to horizontal cells in the carp retina. Journal of Physiology 252, 509522.
Kasai H. (1993). Cytosolic Ca2+ gradients, Ca2+ binding proteins and synaptic plasticity. Neuroscience Research 16, 17.
Kirsch M., Djamgoz M.B.A. & Wagner H.-J. (1990). Correlation of spinule dynamics and plasticity of the horizontal cell spectral response in cyprinid fish retina: Quantitative analysis. Cell and Tissue Research 260, 123130.
Kirsch M., Wagner H.-J. & Djamgoz M.B.A. (1991). Dopamine and plasticity of horizontal cell function in the teleost retina: Regulation of a spectral mechanism through D1-receptors. Vision Research 31, 401412.
Koch C. & Zador A. (1993). The function of dendritic spines: Devices subserving biochemical rather than electrical compartmentalization. Journal of Neuroscience 13, 413422.
Kohler K., Kolbinger W., Kurz-Isler G. & Weiler R. (1990). Endogenous dopamine and cyclic events in the retina, II: Correlation of retinomotor movement, spinule formation, and connexon density of gap junctions with dopamine activity during light/dark cycles. Visual Neuroscience 5, 417428.
Kohler K. & Weiler R. (1990). Dopaminergic modulation of transient neurite outgrowth from horizontal cells of the fish retina is not mediated by cAMP. European Journal of Neuroscience 2, 788794.
Lasater E.M. (1991). Characteristics of single channels activated by quisqualate and kainate in teleost retinal horizontal cells. Vision Research 31, 413424.
Linn C.P. & Christensen B.N. (1992). Excitatory amino acid regulation of intracellular Ca2+ in isolated catfish cone horizontal cells measured under voltage- and concentration-clamp conditions. Journal of Neuroscience 12, 21562164.
Negishi K., Kato S. & Teranishi T. (1988). Dopamine cells and rod bipolar cells contain protein kinase C-like immunoreactivity in some vertebrate retinas. Neuroscience Letters 94, 247252.
Pochet R., Pasteels B., Seto-Oshima A., Bastianelli E., Kitajima S. & Van Eldik L.J. (1991). Calmodulin and calbindin localization in retina from six vertebrate species. Journal of Comparative Neurology 314, 750762.
Polak K.A., Edelman A.M., Wasley J.W.F. & Cohan C.S. (1991). A novel calmodulin antagonist, CGS 9343B, modulates calciumdependent changes in neurite outgrowth cone movements. Journal of Neuroscience 11, 534542.
Raynauld J.-P., Laviolette J.R. & Wagner H.-J. (1979). Goldfish retina: A correlate between cone activity and morphology of the horizontal cell in cone pedicles. Science 204, 14361438.
Rosenmund C. & Westbrook G.L. (1993). Calcium-induced actin depolymerization reduces NMDA channel activity. Neuron 10, 805814.
Schmitz F., Kirsch M. & Wagner H.-J. (1989). Calcium-modulated synaptic ribbon dynamics in cone photoreceptors: A pharmacological and electron-spectroscopic study. European Journal of Cell Biology 49, 207212.
Schmitz F. & Drenckhahn D. (1991). Influence of Ca2+ on synaptic morphology of fish cone photoreceptors. Brain Research 546, 341344.
Schmitz Y. & Kohler K. (1993). Spinule formation in the fish retina: Is there an involvement of tubulin and actin? An electron-microscopic immunogold study. Journal of Neurocytology 22, 205214.
Schmitz Y., Kohler K. & Zrenner E. (1993). Synaptic plasticity in the fish retina: Calmodulin and spinule retraction. Society of Neuroscience Abstracts 19, 117.
Schulman H. & Hanson P.I. (1993). Multifunctional Ca2+/calmodulin-dependent protein kinase. Neurochemistry Research 18, 6577.
Schwartz E.A. (1986). Synaptic transmission in amphibian retinae during conditions unfavourable for calcium entry into presynaptic terminals. Journal of Physiology 376, 411428.
Siekevitz P. (1991). Possible role for calmodulin and the Ca2+/ calmodulin-dependent protein kinase II in postsynaptic neurotransmission. Proceedings of the National Academy of Sciences of the U.S.A. 88, 53745378.
Siman R., Baudry M. & Lynch G.S. (1986). Calcium-activated proteases as possible mediators of synaptic plasticity. In Synaptic Function, ed. Edelman G.M., Gall W.E. & Cowan W.M., pp. 519548. New York: John Wiley & Sons.
Tachibana M. (1983). Ionic currents of solitary horizontal cells isolated from goldfish retina. Journal of Physiology 345, 329351.
Takahashi K.-I., Dixon D.B. & Copenhagen D.R. (1993). Modulation of a sustained calcium current by intracellular pH in horizontal cells of fish retina. Journal of General Physiology 101, 695714.
Van Buskirk R. & Dowling J.E. (1981). Isolated horizontal cells from carp retina demonstrate dopamine-dependent accumulation of cyclic AMP. Proceedings of the National Academy of Sciences of the U.S.A. 78, 78257829.
Wagner H.-J. (1980). Light-dependent plasticity of the morphology of horizontal cell terminals in cone pedicles of fish retinas. Journal of Neurocytology 9, 573590.
Wagner H.-J. & Djamgoz M.B.A. (1993). Spinules: A case for retinal synaptic plasticity. Trends in Neuroscience 16, 201206.
Weiler R. & Janssen-Bienhold U. (1993). Spinule-type neurite outgrowth from horizontal cells during light adaptation in the carp retina: An actin-dependent process. Journal of Neurocytology 22, 129139.
Weiler R., Kohler K., Kirsch M. & Wagner H.-J. (1988). Glutamate and dopamine modulate synaptic plasticity in horizontal cell dendrites of fish retina. Neuroscience Letters 87, 205209.
Weiler R., Kohler K. & Janssen U. (1991). Protein kinase C mediates transient neurite outgrowth in the retina during light adaptation. Proceedings of the National Academy of Sciences of the U.S.A. 88, 36033607.
Weiler R. & Schultz K. (1993). Ionotropic non-N-methyl-D-aspartate agonists induce retraction of dendritic spinules from retinal horizontal cells. Proceedings of the National Academy of Sciences of the U.S.A. 90, 65336537.
Weiler R. & Wagner H.-J. (1984). Light-dependent change of conehorizontal cell interactions in carp retina. Brain Research 298, 19.
Winslow R.L., Miller R.F. & Ogden T.E. (1989). Functional role of spines in the retinal horizontal cell network. Proceedings of the National Academy of Sciences of the U.S.A. 86, 387391.
Wu S.M. (1992). Feedback connections and operation of the outer plexiform layer of the retina. Current Opinion in Neurobiology 2, 462468.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Visual Neuroscience
  • ISSN: 0952-5238
  • EISSN: 1469-8714
  • URL: /core/journals/visual-neuroscience
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Keywords:

Metrics

Full text views

Total number of HTML views: 0
Total number of PDF views: 1 *
Loading metrics...

Abstract views

Total abstract views: 136 *
Loading metrics...

* Views captured on Cambridge Core between September 2016 - 23rd November 2017. This data will be updated every 24 hours.