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 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.


CONCLUSIONS
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.
Departments of Pathology, Biochemistry and Physiology, Universidad Central Del Caribe, Bayamón, Puerto Rico, United States of America.
Astrid
A
Zayas-Santiago
Paul Flechsig Institute of Brain Research, Faculty of Medicine, University of Leipzig, Leipzig, Germany; Division of Soft Matter Physics, Department of Physics, University of Leipzig, Leipzig, Germany.
Silke
S
Agte
Departments of Pathology, Biochemistry and Physiology, Universidad Central Del Caribe, Bayamón, Puerto Rico, United States of America.
Yomarie
Y
Rivera
Departments of Pathology, Biochemistry and Physiology, Universidad Central Del Caribe, Bayamón, Puerto Rico, United States of America.
Jan
J
Benedikt
Paul Flechsig Institute of Brain Research, Faculty of Medicine, University of Leipzig, Leipzig, Germany; Department of Physiology, Development and Neuroscience, University of Cambridge, Cambridge, United Kingdom.
Elke
E
Ulbricht
Paul Flechsig Institute of Brain Research, Faculty of Medicine, University of Leipzig, Leipzig, Germany.
Anett
A
Karl
Departments of Pathology, Biochemistry and Physiology, Universidad Central Del Caribe, Bayamón, Puerto Rico, United States of America.
José
J
Dávila
Department of Physical Sciences, Universidad de Puerto Rico, Recinto de Río Piedras, Río Piedras, Puerto Rico, United States of America.
Alexey
A
Savvinov
Departments of Pathology, Biochemistry and Physiology, Universidad Central Del Caribe, Bayamón, Puerto Rico, United States of America.
Yuriy
Y
Kucheryavykh
Departments of Pathology, Biochemistry and Physiology, Universidad Central Del Caribe, Bayamón, Puerto Rico, United States of America.
Mikhail
M
Inyushin
Departments of Pathology, Biochemistry and Physiology, Universidad Central Del Caribe, Bayamón, Puerto Rico, United States of America.
Luis A
LA
Cubano
Paul Flechsig Institute of Brain Research, Faculty of Medicine, University of Leipzig, Leipzig, Germany.
Thomas
T
Pannicke
Charité, Berlin, Germany.
Rüdiger W
RW
Veh
Paul Flechsig Institute of Brain Research, Faculty of Medicine, University of Leipzig, Leipzig, Germany; Translational Centre for Regenerative Medicine (TRM) University of Leipzig, Leipzig, Germany.
Mike
M
Francke
Faculty of Life Sciences, University of Manchester, Manchester, United Kingdom.
Alexei
A
Verkhratsky
Departments of Pathology, Biochemistry and Physiology, Universidad Central Del Caribe, Bayamón, Puerto Rico, United States of America.
Misty J
MJ
Eaton
Paul Flechsig Institute of Brain Research, Faculty of Medicine, University of Leipzig, Leipzig, Germany.
Andreas
A
Reichenbach
Departments of Pathology, Biochemistry and Physiology, Universidad Central Del Caribe, Bayamón, Puerto Rico, United States of America.
Serguei N
SN
Skatchkov
D000489:Alligators and Crocodiles / Q000378:metabolism; D000818:Animals; D063928:Ependymoglial Cells / Q000166:cytology*; D005456:Fluorescent Dyes / Q000737:chemistry; D005971:Glutamates / Q000378:metabolism; D015640:Ion Channel Gating; D008564:Membrane Potentials; D009419:Nerve Tissue Proteins / Q000378:metabolism; D009474:Neurons / Q000378:metabolism; D020419:Photoreceptor Cells, Vertebrate / Q000166:cytology*; D011188:Potassium / Q000737:chemistry; D024661:Potassium Channels, Inwardly Rectifying / Q000378:metabolism*; D024683:Potassium Channels, Tandem Pore Domain / Q000378:metabolism; D017434:Protein Structure, Tertiary; D012160:Retina / Q000378:metabolism / Q000502:physiology*; D015398:Signal Transduction; D000098854:Kcnj10 Channel
D005456:Fluorescent Dyes; D005971:Glutamates; D000098854:Kcnj10 Channel; D009419:Nerve Tissue Proteins; D024661:Potassium Channels, Inwardly Rectifying; D024683:Potassium Channels, Tandem Pore Domain; C420132:potassium channel subfamily K member 3; D011188:Potassium