Dataset Information

Photoreceptor coupling is controlled by connexin 35 phosphorylation in zebrafish retina.

ABSTRACT: Electrical coupling of neurons is widespread throughout the CNS and is observed among retinal photoreceptors from essentially all vertebrates. Coupling dampens voltage noise in photoreceptors and rod-cone coupling provides a means for rod signals to enter the cone pathway, extending the dynamic range of rod-mediated vision. This coupling is dynamically regulated by a circadian rhythm and light adaptation. We examined the molecular mechanism that controls photoreceptor coupling in zebrafish retina. Connexin 35 (homologous to Cx36 of mammals) was found at both cone-cone and rod-cone gap junctions. Photoreceptors showed strong Neurobiotin tracer coupling at night, extensively labeling the network of cones. Tracer coupling was significantly reduced in the daytime, showing a 20-fold lower diffusion coefficient for Neurobiotin transfer. The phosphorylation state of Cx35 at two regulatory phosphorylation sites, Ser110 and Ser276, was directly related to tracer coupling. Phosphorylation was high at night and low during the day. Protein kinase A (PKA) activity directly controlled both phosphorylation state and tracer coupling. Both were significantly increased in the day by pharmacological activation of PKA and significantly reduced at night by inhibition of PKA. The data are consistent with direct phosphorylation of Cx35 by PKA. We conclude that the magnitude of photoreceptor coupling is controlled by the dynamic phosphorylation and dephosphorylation of Cx35. Furthermore, the nighttime state is characterized by extensive coupling that results in a well connected cone network.

SUBMITTER: Li H

PROVIDER: S-EPMC2909833 | biostudies-literature | 2009 Dec

REPOSITORIES: biostudies-literature

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Photoreceptor coupling is controlled by connexin 35 phosphorylation in zebrafish retina.

Li Hongyan H Chuang Alice Z AZ O'Brien John J

The Journal of neuroscience : the official journal of the Society for Neuroscience 20091201 48

Electrical coupling of neurons is widespread throughout the CNS and is observed among retinal photoreceptors from essentially all vertebrates. Coupling dampens voltage noise in photoreceptors and rod-cone coupling provides a means for rod signals to enter the cone pathway, extending the dynamic range of rod-mediated vision. This coupling is dynamically regulated by a circadian rhythm and light adaptation. We examined the molecular mechanism that controls photoreceptor coupling in zebrafish retin ...[more]

PMID: 19955370

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Project description: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, S100?, 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.

Dataset Information

Photoreceptor coupling is controlled by connexin 35 phosphorylation in zebrafish retina.

Publications

Photoreceptor coupling is controlled by connexin 35 phosphorylation in zebrafish retina.

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