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Unidirectional Photoreceptor-to-Müller Glia Coupling and Unique K(+) Channel Expression in Caiman Retina

BACKGROUND: Müller cells, the principal glial cells of the vertebrate retina, are fundamental for the maintenance and function of neuronal cells. In most vertebrates, including humans, Müller cells abundantly express Kir4.1 inwardly rectifying potassium channels responsible for hyperpolarized membra...

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Autores principales: Zayas-Santiago, Astrid, Agte, Silke, Rivera, Yomarie, Benedikt, Jan, Ulbricht, Elke, Karl, Anett, Dávila, José, Savvinov, Alexey, Kucheryavykh, Yuriy, Inyushin, Mikhail, Cubano, Luis A., Pannicke, Thomas, Veh, Rüdiger W., Francke, Mike, Verkhratsky, Alexei, Eaton, Misty J., Reichenbach, Andreas, Skatchkov, Serguei N.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4022631/
https://www.ncbi.nlm.nih.gov/pubmed/24831221
http://dx.doi.org/10.1371/journal.pone.0097155
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author Zayas-Santiago, Astrid
Agte, Silke
Rivera, Yomarie
Benedikt, Jan
Ulbricht, Elke
Karl, Anett
Dávila, José
Savvinov, Alexey
Kucheryavykh, Yuriy
Inyushin, Mikhail
Cubano, Luis A.
Pannicke, Thomas
Veh, Rüdiger W.
Francke, Mike
Verkhratsky, Alexei
Eaton, Misty J.
Reichenbach, Andreas
Skatchkov, Serguei N.
author_facet Zayas-Santiago, Astrid
Agte, Silke
Rivera, Yomarie
Benedikt, Jan
Ulbricht, Elke
Karl, Anett
Dávila, José
Savvinov, Alexey
Kucheryavykh, Yuriy
Inyushin, Mikhail
Cubano, Luis A.
Pannicke, Thomas
Veh, Rüdiger W.
Francke, Mike
Verkhratsky, Alexei
Eaton, Misty J.
Reichenbach, Andreas
Skatchkov, Serguei N.
author_sort Zayas-Santiago, Astrid
collection PubMed
description BACKGROUND: Müller cells, the principal glial cells of the vertebrate retina, are fundamental for the maintenance and function of neuronal cells. In most vertebrates, including humans, Müller cells abundantly express Kir4.1 inwardly rectifying potassium channels responsible for hyperpolarized membrane potential and for various vital functions such as potassium buffering and glutamate clearance; inter-species differences in Kir4.1 expression were, however, observed. Localization and function of potassium channels in Müller cells from the retina of crocodiles remain, hitherto, unknown. METHODS: We studied retinae of the Spectacled caiman (Caiman crocodilus fuscus), endowed with both diurnal and nocturnal vision, by (i) immunohistochemistry, (ii) whole-cell voltage-clamp, and (iii) fluorescent dye tracing to investigate K(+) channel distribution and glia-to-neuron communications. RESULTS: Immunohistochemistry revealed that caiman Müller cells, similarly to other vertebrates, express vimentin, GFAP, S100β, and glutamine synthetase. In contrast, Kir4.1 channel protein was not found in Müller cells but was localized in photoreceptor cells. Instead, 2P-domain TASK-1 channels were expressed in Müller cells. Electrophysiological properties of enzymatically dissociated Müller cells without photoreceptors and isolated Müller cells with adhering photoreceptors were significantly different. This suggests ion coupling between Müller cells and photoreceptors in the caiman retina. Sulforhodamine-B injected into cones permeated to adhering Müller cells thus revealing a uni-directional dye coupling. CONCLUSION: Our data indicate that caiman Müller glial cells are unique among vertebrates studied so far by predominantly expressing TASK-1 rather than Kir4.1 K(+) channels and by bi-directional ion and uni-directional dye coupling to photoreceptor cells. This coupling may play an important role in specific glia-neuron signaling pathways and in a new type of K(+) buffering.
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spelling pubmed-40226312014-05-21 Unidirectional Photoreceptor-to-Müller Glia Coupling and Unique K(+) Channel Expression in Caiman Retina Zayas-Santiago, Astrid Agte, Silke Rivera, Yomarie Benedikt, Jan Ulbricht, Elke Karl, Anett Dávila, José Savvinov, Alexey Kucheryavykh, Yuriy Inyushin, Mikhail Cubano, Luis A. Pannicke, Thomas Veh, Rüdiger W. Francke, Mike Verkhratsky, Alexei Eaton, Misty J. Reichenbach, Andreas Skatchkov, Serguei N. PLoS One Research Article BACKGROUND: Müller cells, the principal glial cells of the vertebrate retina, are fundamental for the maintenance and function of neuronal cells. In most vertebrates, including humans, Müller cells abundantly express Kir4.1 inwardly rectifying potassium channels responsible for hyperpolarized membrane potential and for various vital functions such as potassium buffering and glutamate clearance; inter-species differences in Kir4.1 expression were, however, observed. Localization and function of potassium channels in Müller cells from the retina of crocodiles remain, hitherto, unknown. METHODS: We studied retinae of the Spectacled caiman (Caiman crocodilus fuscus), endowed with both diurnal and nocturnal vision, by (i) immunohistochemistry, (ii) whole-cell voltage-clamp, and (iii) fluorescent dye tracing to investigate K(+) channel distribution and glia-to-neuron communications. RESULTS: Immunohistochemistry revealed that caiman Müller cells, similarly to other vertebrates, express vimentin, GFAP, S100β, and glutamine synthetase. In contrast, Kir4.1 channel protein was not found in Müller cells but was localized in photoreceptor cells. Instead, 2P-domain TASK-1 channels were expressed in Müller cells. Electrophysiological properties of enzymatically dissociated Müller cells without photoreceptors and isolated Müller cells with adhering photoreceptors were significantly different. This suggests ion coupling between Müller cells and photoreceptors in the caiman retina. Sulforhodamine-B injected into cones permeated to adhering Müller cells thus revealing a uni-directional dye coupling. CONCLUSION: Our data indicate that caiman Müller glial cells are unique among vertebrates studied so far by predominantly expressing TASK-1 rather than Kir4.1 K(+) channels and by bi-directional ion and uni-directional dye coupling to photoreceptor cells. This coupling may play an important role in specific glia-neuron signaling pathways and in a new type of K(+) buffering. Public Library of Science 2014-05-15 /pmc/articles/PMC4022631/ /pubmed/24831221 http://dx.doi.org/10.1371/journal.pone.0097155 Text en © 2014 Zayas-Santiago et al http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Zayas-Santiago, Astrid
Agte, Silke
Rivera, Yomarie
Benedikt, Jan
Ulbricht, Elke
Karl, Anett
Dávila, José
Savvinov, Alexey
Kucheryavykh, Yuriy
Inyushin, Mikhail
Cubano, Luis A.
Pannicke, Thomas
Veh, Rüdiger W.
Francke, Mike
Verkhratsky, Alexei
Eaton, Misty J.
Reichenbach, Andreas
Skatchkov, Serguei N.
Unidirectional Photoreceptor-to-Müller Glia Coupling and Unique K(+) Channel Expression in Caiman Retina
title Unidirectional Photoreceptor-to-Müller Glia Coupling and Unique K(+) Channel Expression in Caiman Retina
title_full Unidirectional Photoreceptor-to-Müller Glia Coupling and Unique K(+) Channel Expression in Caiman Retina
title_fullStr Unidirectional Photoreceptor-to-Müller Glia Coupling and Unique K(+) Channel Expression in Caiman Retina
title_full_unstemmed Unidirectional Photoreceptor-to-Müller Glia Coupling and Unique K(+) Channel Expression in Caiman Retina
title_short Unidirectional Photoreceptor-to-Müller Glia Coupling and Unique K(+) Channel Expression in Caiman Retina
title_sort unidirectional photoreceptor-to-müller glia coupling and unique k(+) channel expression in caiman retina
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4022631/
https://www.ncbi.nlm.nih.gov/pubmed/24831221
http://dx.doi.org/10.1371/journal.pone.0097155
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