Differential distribution of voltage‐gated potassium channels Kv 1.1–Kv1.6 in the rat retina during development

The discharge behavior of neurons depends on a variable expression and sorting pattern of voltage‐dependent potassium (Kv) channels that changes during development. The rodent retina represents a neuronal network whose main functions develop after birth. To obtain information about neuronal maturation we analyzed the expression of subunits of the Kv1 subfamily in the rat retina during postnatal development using immunocytochemistry and immunoelectron microscopy. At postnatal day 5 (P5) all the α‐subunits of Kv1.1–Kv1.6 channels were found to be expressed in the ganglion cell layer (GCL), most of them already at P1 or P3. Their expression upregulates postnatally and the pattern and distribution change in an isoform‐specific manner. Additionally Kv1 channels are found in the outer and inner plexiform layer (OPL, IPL) and in the inner nuclear layer (INL) at different postnatal stages. In adult retina the Kv 1.3 channel localizes to the inner and outer segments of cones. In contrast, Kv1.4 is highly expressed in the outer retina at P8. In adult retina Kv1.4 occurs in rod inner segments (RIS) near the connecting cilium where it colocalizes with synapse associated protein SAP 97. By using confocal laser scanning microscopy we showed a differential localization of Kv1.1‐1.6 to cholinergic amacrine and rod bipolar cells of the INL of the adult retina. © 2006 Wiley‐Liss, Inc.

[1]  Marla B. Feller,et al.  Spontaneous patterned retinal activity and the refinement of retinal projections , 2005, Progress in Neurobiology.

[2]  Marla B Feller,et al.  Retinal waves: mechanisms and function in visual system development. , 2005, Cell calcium.

[3]  F. Ohl,et al.  Fallacies in behavioural interpretation of auditory cortex plasticity , 2004, Nature Reviews Neuroscience.

[4]  Heinz Wässle,et al.  Parallel processing in the mammalian retina , 2004, Nature Reviews Neuroscience.

[5]  H. Wässle,et al.  Types of bipolar cells in the mouse retina , 2004, The Journal of comparative neurology.

[6]  W. Wong,et al.  Differential Recruitment of Kv1.4 and Kv4.2 to Lipid Rafts by PSD-95* , 2004, Journal of Biological Chemistry.

[7]  O. Ottersen,et al.  Axonal sorting of Kir3.3 defines a GABA-containing neuron in the CA3 region of rodent hippocampus , 2003, Molecular and Cellular Neuroscience.

[8]  Xiong-Li Yang,et al.  Voltage-gated K+channel subunits on cholinergic and dopaminergic amacrine cells , 2003, Neuroreport.

[9]  Andrew D Huberman,et al.  Decoupling Eye-Specific Segregation from Lamination in the Lateral Geniculate Nucleus , 2002, The Journal of Neuroscience.

[10]  P. Witkovsky,et al.  Diurnal and circadian variation of protein kinase C immunoreactivity in the rat retina , 2001, The Journal of comparative neurology.

[11]  R. Luján,et al.  Subcellular compartmentalization of a potassium channel (Kv1.4): preferential distribution in dendrites and dendritic spines of neurons in the dorsal cochlear nucleus , 2000, The European journal of neuroscience.

[12]  Y. Kurachi,et al.  SAP family proteins. , 2000, Biochemical and biophysical research communications.

[13]  A. Draguhn,et al.  Expression of Kv1 Potassium Channels in Mouse Hippocampal Primary Cultures: Development and Activity-Dependent Regulation , 2000, The Journal of Neuroscience.

[14]  J. Trimmer,et al.  Psd-95 and Sap97 Exhibit Distinct Mechanisms for Regulating K+ Channel Surface Expression and Clustering , 2000, The Journal of cell biology.

[15]  P. Koulen Localization of synapse‐associated proteins during postnatal development of the rat retina , 1999, The European journal of neuroscience.

[16]  Simon C Watkins,et al.  Distinct Structural Requirements for Clustering and Immobilization of K+ Channels by PSD-95 , 1999, The Journal of general physiology.

[17]  E. Morii,et al.  Differential localization and expression of α and β isoenzymes of protein kinase c in the rat retina , 1998 .

[18]  L. Pinto,et al.  Localization of potassium channels in the retina. , 1998, Progress in retinal and eye research.

[19]  Y. Jan,et al.  Presynaptic Localization of Kv1.4-Containing A-Type Potassium Channels Near Excitatory Synapses in the Hippocampus , 1998, The Journal of Neuroscience.

[20]  D. Bredt,et al.  N-Terminal Palmitoylation of PSD-95 Regulates Association with Cell Membranes and Interaction with K+ Channel Kv1.4 , 1998, Neuron.

[21]  N. K. Dhingra,et al.  Developmental expression of synaptophysin, synapsin I and syntaxin in the rat retina. , 1997, Brain research. Developmental brain research.

[22]  Y. Hata,et al.  Clustering and Enhanced Activity of an Inwardly Rectifying Potassium Channel, Kir4.1, by an Anchoring Protein, PSD-95/SAP90* , 1997, The Journal of Biological Chemistry.

[23]  M. Sheng,et al.  Differential K+ Channel Clustering Activity of PSD-95 and SAP97, Two Related Membrane-associated Putative Guanylate Kinases , 1996, Neuropharmacology.

[24]  O. Pongs,et al.  Presynaptic potassium channels , 1996, Current Opinion in Neurobiology.

[25]  F. Werblin,et al.  Requirement for Cholinergic Synaptic Transmission in the Propagation of Spontaneous Retinal Waves , 1996, Science.

[26]  L. Pinto,et al.  Identification and localization of K+ channels in the mouse retina , 1995, Visual Neuroscience.

[27]  O. Pongs,et al.  Immunohistochemical Localization of Five Members of the KV1 Channel Subunits: Contrasting Subcellular Locations and Neuron‐specific Co‐localizations in Rat Brain , 1995, The European journal of neuroscience.

[28]  S. Ito,et al.  The Shaker-like potassium channels of the mouse rod bipolar cell and their contributions to the membrane current , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[29]  J. Trimmer,et al.  Association and colocalization of K+ channel alpha- and beta-subunit polypeptides in rat brain , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[30]  E. Gundelfinger,et al.  Molecular characterization and spatial distribution of SAP97, a novel presynaptic protein homologous to SAP90 and the Drosophila discs-large tumor suppressor protein , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[31]  M. Linial,et al.  Nucleotide bindind by the synapse associated protein SAP90 , 1995, FEBS letters.

[32]  C. Shatz,et al.  Transient period of correlated bursting activity during development of the mammalian retina , 1993, Neuron.

[33]  J. Dolly,et al.  Oligomeric properties of alpha-dendrotoxin-sensitive potassium ion channels purified from bovine brain. , 1992, Biochemistry.

[34]  J. Ruppersberg,et al.  Characterization of a Shaw‐related potassium channel family in rat brain. , 1992, The EMBO journal.

[35]  Lawrence Salkoff,et al.  Shaker, Shal, Shab, and Shaw express independent K+ current systems , 1991, Neuron.

[36]  G. W. Balkema A synaptic antigen (B16) is localized in retinal synaptic ribbons , 1991, The Journal of comparative neurology.

[37]  B. Boycott,et al.  Functional architecture of the mammalian retina. , 1991, Physiological reviews.

[38]  Yuh Nung Jan,et al.  Evidence for the formation of heteromultimeric potassium channels in Xenopus oocytes , 1990, Nature.

[39]  B. Sakmann,et al.  Heteromultimeric channels formed by rat brain potassium-channel proteins , 1990, Nature.

[40]  R. North,et al.  Heteropolymeric potassium channels expressed in xenopus oocytes from cloned subunits , 1990, Neuron.

[41]  L. Maffei,et al.  Spontaneous impulse activity of rat retinal ganglion cells in prenatal life. , 1988, Science.

[42]  T. Voigt,et al.  Cholinergic amacrine cells in the rat retina , 1986, The Journal of comparative neurology.

[43]  J. Mills,et al.  Acetylcholine synthesis by displaced amacrine cells. , 1980, Science.

[44]  M. Lavail,et al.  Rods and cones in the mouse retina. I. Structural analysis using light and electron microscopy , 1979, The Journal of comparative neurology.

[45]  H. Jindrová Vertebrate phototransduction: activation, recovery, and adaptation. , 1998, Physiological research.

[46]  Y. Jan,et al.  Structural elements involved in specific K+ channel functions. , 1992, Annual review of physiology.