Abstract
BackgroundMüller 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.MethodsWe 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.ResultsImmunohistochemistry 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.ConclusionOur 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.
Highlights
Muller glial cells [1] serve numerous fundamental functions in the retina of vertebrates; many of these functions depend on potassium channels, responsible for a high potassium conductance of the cell membrane [2,3,4]
Glial markers in caiman Muller cells First, we analyzed the presence of the established glial marker proteins, S100b, glutamine synthetase (GS), vimentin, and GFAP in caiman retinal Muller cells
We examined the localization of the alpha subunit of G-protein transducin (Gat1), a G-protein involved in phototransduction, in caiman photoreceptor cells
Summary
Muller glial cells [1] serve numerous fundamental functions in the retina of vertebrates; many of these functions depend on potassium channels, responsible for a high potassium conductance of the cell membrane [2,3,4]. We report a study of Muller cells from retinae of caiman (Caiman crocodilus fuscus), which has perfect night vision as well as vision in the bright daylight, with a large scale of adaptation to different light intensities. This ability is reflected by several morphological and functional idiosyncrasies in the caiman vision system [17]. In most vertebrates, including humans, Muller 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, observed. Localization and function of potassium channels in Muller cells from the retina of crocodiles remain, hitherto, unknown
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