Photoreceptor calcium channels: Insight from night blindness

The genetic locus for incomplete congenital stationary night blindness (CSNB2) has been identified as the CACNA1f gene, encoding the α1F calcium channel subunit, a member of the L-type family of calcium channels. The electroretinogram associated with CSNB2 implicates α1F in synaptic transmission between retinal photoreceptors and bipolar cells. Using a recently developed monoclonal antibody to α1F, we localize the channel to ribbon active zones in rod photoreceptor terminals of the mouse retina, supporting a role for α1F in mediating glutamate release from rods. Detergent extraction experiments indicate that α1F is part of a detergent-resistant active zone complex, which also includes the synaptic ribbons. Comparison of native mouse rod calcium currents with recombinant α1F currents reveals that the current–voltage relationship for the native current is shifted approximately 30 mV to more hyperpolarized potentials than for the recombinant α1F current, suggesting modulation of the native channel by intracellular factors. Lastly, we present evidence for L-type α1D calcium channel subunits in cone terminals of the mouse retina. The presence of α1D channels in cones may explain the residual visual abilities of individuals with CSNB2.

[1]  A. Koschak,et al.  Congenital Stationary Night Blindness Type 2 Mutations S229P, G369D, L1068P, and W1440X Alter Channel Gating or Functional Expression of Cav1.4 L-type Ca2+ Channels , 2005, The Journal of Neuroscience.

[2]  F. Rieke,et al.  Essential role of Ca2+-binding protein 4, a Cav1.4 channel regulator, in photoreceptor synaptic function , 2004, Nature Neuroscience.

[3]  W. R. Taylor,et al.  Transmission of single photon signals through a binary synapse in the mammalian retina , 2004, Visual Neuroscience.

[4]  W. Stell,et al.  Mutation of the Calcium Channel Gene Cacna1f Disrupts Calcium Signaling and Synaptic Transmission in Mouse Retina , 2004 .

[5]  Aaron M. Beedle,et al.  The CACNA1F Gene Encodes an L-Type Calcium Channel with Unique Biophysical Properties and Tissue Distribution , 2004, The Journal of Neuroscience.

[6]  C. Wahl-Schott,et al.  Functional characterization of the L-type Ca2+ channel Cav1.4alpha1 from mouse retina. , 2004, Investigative ophthalmology & visual science.

[7]  G. Richardson.  Faculty Opinions recommendation of CaV1.3 channels are essential for development and presynaptic activity of cochlear inner hair cells. , 2003 .

[8]  J. Engel,et al.  Cav1.3 (α1D) Ca2+ Currents in Neonatal Outer Hair Cells of Mice , 2003 .

[9]  J. Striessnig,et al.  CaV1.3 Channels Are Essential for Development and Presynaptic Activity of Cochlear Inner Hair Cells , 2003, The Journal of Neuroscience.

[10]  A. Dolphin.  Faculty Opinions recommendation of Cav1.4alpha1 subunits can form slowly inactivating dihydropyridine-sensitive L-type Ca2+ channels lacking Ca2+-dependent inactivation. , 2003 .

[11]  A. Koschak,et al.  Cav1.4α1 Subunits Can Form Slowly Inactivating Dihydropyridine-Sensitive L-Type Ca2+ Channels Lacking Ca2+-Dependent Inactivation , 2003, The Journal of Neuroscience.

[12]  Josef Ammermüller,et al.  The Presynaptic Active Zone Protein Bassoon Is Essential for Photoreceptor Ribbon Synapse Formation in the Retina , 2003, Neuron.

[13]  Y. Fei,et al.  Development of the cone photoreceptor mosaic in the mouse retina revealed by fluorescent cones in transgenic mice. , 2003, Molecular vision.

[14]  A. Berntson,et al.  Molecular identity, synaptic localization, and physiology of calcium channels in retinal bipolar cells , 2003, Journal of neuroscience research.

[15]  H. Wässle,et al.  The Cone Pedicle, the First Synapse in the Retina , 2003 .

[16]  J. Engel,et al.  Cav1.3 (alpha1D) Ca2+ currents in neonatal outer hair cells of mice. , 2003, The Journal of physiology.

[17]  A. Koschak,et al.  Cav 1 . 4 1 Subunits Can Form Slowly Inactivating Dihydropyridine-Sensitive L-Type Ca 2 Channels Lacking Ca 2-Dependent Inactivation , 2003 .

[18]  F. Rieke,et al.  Mechanisms Regulating Variability of the Single Photon Responses of Mammalian Rod Photoreceptors , 2002, Neuron.

[19]  P. Powers,et al.  Role of the beta(2) subunit of voltage-dependent calcium channels in the retinal outer plexiform layer. , 2002, Investigative ophthalmology & visual science.

[20]  S. DeVries,et al.  Exocytosed Protons Feedback to Suppress the Ca2+ Current in Mammalian Cone Photoreceptors , 2001, Neuron.

[21]  P. Sterling,et al.  Microcircuits for Night Vision in Mouse Retina , 2001, The Journal of Neuroscience.

[22]  C. Garner,et al.  Localization of the presynaptic cytomatrix protein Piccolo at ribbon and conventional synapses in the rat retina: Comparison with Bassoon , 2001, The Journal of comparative neurology.

[23]  C. Morgans.  Localization of the α1F Calcium Channel Subunit in the Rat Retina , 2001 .

[24]  R. Maleszka,et al.  Expression of the alpha1F calcium channel subunit by photoreceptors in the rat retina. , 2001, Molecular vision.

[25]  C. Morgans.  Localization of the alpha(1F) calcium channel subunit in the rat retina. , 2001, Investigative ophthalmology & visual science.

[26]  T. Südhof,et al.  RIBEYE, a Component of Synaptic Ribbons A Protein's Journey through Evolution Provides Insight into Synaptic Ribbon Function , 2000, Neuron.

[27]  H. Wässle,et al.  Differential expression of the presynaptic cytomatrix protein bassoon among ribbon synapses in the mammalian retina , 1999, The European journal of neuroscience.

[28]  C. Morgans.  Calcium channel heterogeneity among cone photoreceptors in the tree shrew retina , 1999, The European journal of neuroscience.

[29]  J. L. Schnapf,et al.  The Photovoltage of Macaque Cone Photoreceptors: Adaptation, Noise, and Kinetics , 1999, The Journal of Neuroscience.

[30]  T. Meitinger,et al.  An L-type calcium-channel gene mutated in incomplete X-linked congenital stationary night blindness , 1998, Nature Genetics.

[31]  W. R. Taylor,et al.  Calcium Extrusion from Mammalian Photoreceptor Terminals , 1998, The Journal of Neuroscience.

[32]  C. Morgans,et al.  Localization and properties of voltage-gated calcium channels in cone photoreceptors of Tupaia belangeri , 1998, Visual Neuroscience.

[33]  Kym M. Boycott,et al.  Loss-of-function mutations in a calcium-channel α1-subunit gene in Xp11.23 cause incomplete X-linked congenital stationary night blindness , 1998, Nature Genetics.

[34]  Thomas C. Südhof,et al.  Rim is a putative Rab3 effector in regulating synaptic-vesicle fusion , 1997, Nature.

[35]  H. Wässle,et al.  A SNARE Complex Containing Syntaxin 3 Is Present in Ribbon Synapses of the Retina , 1996, The Journal of Neuroscience.

[36]  F. Tremblay,et al.  Visual evoked potentials with crossed asymmetry in incomplete congenital stationary night blindness. , 1996, Investigative ophthalmology & visual science.

[37]  H. Reuter.  Diversity and function of presynaptic calcium channels in the brain , 1996, Current Opinion in Neurobiology.

[38]  M. Wilkinson,et al.  The dihydropyridine-sensitive calcium channel subtype in cone photoreceptors , 1996, The Journal of general physiology.

[39]  D. Baylor,et al.  An alternative pathway for signal flow from rod photoreceptors to ganglion cells in mammalian retina. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[40]  J. L. Schnapf,et al.  Photovoltage of rods and cones in the macaque retina. , 1995, Science.

[41]  R. Tsien,et al.  Roles of N-type and Q-type Ca2+ channels in supporting hippocampal synaptic transmission. , 1994, Science.

[42]  T. Yagi,et al.  Ionic conductances of monkey solitary cone inner segments. , 1994, Journal of neurophysiology.

[43]  G. Isenberg,et al.  L-type Ca 2+ Channels , 1994 .

[44]  E. Zrenner,et al.  Clinical findings in patients with congenital stationary night blindness of the Schubert-Bornschein type. , 1993, German journal of ophthalmology.

[45]  V. Greenstein,et al.  Models of the normal and abnormal rod system , 1990, Vision Research.

[46]  B. Hille,et al.  Ionic channels of the inner segment of tiger salamander cone photoreceptors , 1989, The Journal of general physiology.

[47]  K. Yagasaki,et al.  Congenital stationary night blindness with negative electroretinogram. A new classification. , 1986 .

[48]  J. Blanks,et al.  Selective lectin binding of the developing mouse retina , 1983, The Journal of comparative neurology.