Unidirectional Photoreceptor-to-Muller Glia Coupling and Unique K+ Channel Expression in Caiman Retina

Background: Muller cells, the principal glial cells of the vertebrate retina, are fundamental for the maintenance and function of neuronal cells. 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, however, observed. Localization and function of potassium channels in Muller 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 Muller cells, similarly to other vertebrates, express vimentin, GFAP, S100 beta, and glutamine synthetase. In contrast, Kir4.1 channel protein was not found in Muller cells but was localized in photoreceptor cells. Instead, 2P-domain TASK-1 channels were expressed in Muller cells. Electrophysiological properties of enzymatically dissociated Muller cells without photoreceptors and isolated Muller cells with adhering photoreceptors were significantly different. This suggests ion coupling between Muller cells and photoreceptors in the caiman retina. Sulforhodamine-B injected into cones permeated to adhering Muller cells thus revealing a uni-directional dye coupling. Conclusion: Our data indicate that caiman Muller 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.