Hostname: page-component-586b7cd67f-gb8f7 Total loading time: 0 Render date: 2024-11-24T04:22:33.521Z Has data issue: false hasContentIssue false
  • English
  • Français

Photoreceptor calcium channels: Insight from night blindness

Published online by Cambridge University Press:  06 December 2005

CATHERINE W. MORGANS ,
PHILIPPA R. BAYLEY ,
NICHOLAS W. OESCH ,
GAOYING REN ,
LAKSHMI AKILESWARAN  and
W. ROWLAND TAYLOR
CATHERINE W. MORGANS
Affiliation:
Neurological Sciences Institute, Oregon Health and Science University, Beaverton
PHILIPPA R. BAYLEY
Affiliation:
Neurological Sciences Institute, Oregon Health and Science University, Beaverton
NICHOLAS W. OESCH
Affiliation:
Neurological Sciences Institute, Oregon Health and Science University, Beaverton
GAOYING REN
Affiliation:
Neurological Sciences Institute, Oregon Health and Science University, Beaverton
LAKSHMI AKILESWARAN
Affiliation:
Neurological Sciences Institute, Oregon Health and Science University, Beaverton
W. ROWLAND TAYLOR
Affiliation:
Neurological Sciences Institute, Oregon Health and Science University, Beaverton
Get access Rights & Permissions [Opens in a new window]

Abstract

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.

Keywords

Calcium channelCSNB2PhotoreceptorSynaptic transmissionRibbon synapse
Type
Research Article
Information
Visual Neuroscience , Volume 22 , Issue 5 , September 2005 , pp. 561 - 568
Copyright
© 2005 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Ball, S.L., Powers, P.A., Shin, H.-S., Morgans, C.W., Peachey, N.S., & Gregg, R.G. (2002). Role of the beta2 subunit of voltage-dependent calcium channels in the retinal outer plexiform layer. Investigative Ophthalmology and Visual Science 43, 1595–1603.Google Scholar
Barnes, S. & Hille, B. (1989). Ionic channels of the inner segment of tiger salamander cone photoreceptors. Journal of General Physiology 94, 719–743.CrossRefGoogle Scholar
Baumann, L., Gerstner, A., Zong, X., Biel, M., & Wahl-Schott, C. (2004). Functional characterization of the L-type Ca2+ channel Cav1.4 1 from mouse retina. Investigative Ophthalmology and Visual Science 45, 708–713.Google Scholar
Bech-Hansen, N.T., Naylor, M.J., Maybaum, T.A., Pearce, W.G., Koop, B., Fishman, G.A., Mets, M., Musarella, M.A., & Boycott, K.M. (1998). Loss-of-function mutations in a calcium-channel α1-subunit gene in Xp11.23 cause incomplete X-linked congenital stationary night blindness. Nature Genetics 19, 264–267.Google Scholar
Berntson, A., Smith, R., & Taylor, W. (2004). Transmission of single photon signals through a binary synapse in the mammalian retina. Visual Neuroscience 21, 693–702.CrossRefGoogle Scholar
Berntson, A., Taylor, W.R., & Morgans, C.W. (2003). Molecular identity, synaptic localization, and physiology of calcium channels in retinal bipolar cells. Journal of Neuroscience Research 71, 146–151.CrossRefGoogle Scholar
Blanks, J. & Johnson, L. (1983). Selective lectin binding of the developing mouse retina. Journal of Comparative Neurology 221, 31–41.CrossRefGoogle Scholar
Brandstätter, J.H., Fletcher, E.L., Garner, C.C., Gundelfinger, E.D., & Wässle, H. (1999). Differential expression of the presynaptic cytomatrix protein bassoon among ribbon synapses in the mammalian retina. European Journal of Neuroscience 11, 3683–3693.CrossRefGoogle Scholar
Brandt, A., Striessnig, J., & Moser, T. (2003). CaV1.3 Channels are essential for development and presynaptic activity of cochlear inner hair cells. Journal of Neuroscience 23, 10832–10840.Google Scholar
DeVries, S. & Baylor, D. (1995). An alternative pathway for signal flow from rod photoreceptors to ganglion cells in mammalian retina. Proceedings of the National Academy of Sciences of the U.S.A. 92, 10658–10662.CrossRefGoogle Scholar
DeVries, S.H. (2001). Exocytosed protons feedback to suppress the Ca2+ current in mammalian cone photoreceptors. Neuron 32, 1107–1117.CrossRefGoogle Scholar
Dick, O., Hack, I., Altrock, W.D., Garner, C.C., Gundelfinger, E.D., & BrandstÄtter, J.H. (2001). Localization of the presynaptic cytomatrix protein piccolo at ribbon and conventional synapses in the rat retina: Comparison with bassoon. Journal of Comparative Neurobiology 439, 224–234.CrossRefGoogle Scholar
Dick, O., Tom Dieck, S., Altrock, W., Ammermuller, J., Weiler, R., Garner, C., Gundelfinger, E., & Brandstatter, J. (2003). The presynaptic active zone protein bassoon is essential for photoreceptor ribbon synapse formation in the retina. Neuron 37, 775–786.CrossRefGoogle Scholar
Fei, Y. (2003). Development of the cone photoreceptor mosaic in the mouse retina revealed by fluorescent cones in transgenic mice. Molecular Vision 9, 31–42.Google Scholar
Field, G. & Rieke, F. (2002). Mechanisms regulating variability of the single photon responses of mammalian rod photoreceptors. Neuron 35, 733–747.CrossRefGoogle Scholar
Haeseleer, F., Imanishi, Y., Maeda, T., Possin, D., Maeda, A., Lee, A., Rieke, F., & Palczewski, K. (2004). Essential role of Ca2+-binding protein 4, a Cav1.4 channel regulator, in photoreceptor synaptic function. Nature Neuroscience 7, 1079–1087.Google Scholar
Hoda, J., Zaghetto, F., Koschak, A., & Striessnig, J. (2005). 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. Journal of Neuroscience 25, 252–259.Google Scholar
Hood, D.C. & Greenstein, V. (1990). Models of the normal and abnormal rod system. Vision Research 30, 51–68.CrossRefGoogle Scholar
Koschak, A., Reimer, D., Walter, D., Hoda, J., Heinzle, T., Grabner, M., & Striessnig, J. (2003). Cav1.4alpha1 subunits can form slowly inactivating dihydropyridine-sensitive L-type Ca2+ channels lacking Ca2+-dependent inactivation. Journal of Neuroscience 23, 6041–6049.Google Scholar
McRory, J., Hamid, J., Doering, C., Garcia, E., Parker, R., Hamming, K., Chen, L., Hildebrand, M., Beedle, A., Feldcamp, L., Zamponi, G., & Snutch, T. (2004). The CACNA1F gene encodes an L-type calcium channel with unique biophysical properties and tissue distribution. Journal of Neuroscience 24, 1707–1718.Google Scholar
Michna, M., Knirsch, M., Hoda, J.-C., Muenkner, S., Langer, P., Platzer, J., Striessnig, J., & Engel, J. (2003). Cav1.3 (alpha1D) Ca2+ currents in neonatal outer hair cells of mice. Journal of Physiology (London) 553, 747–758.Google Scholar
Miyake, Y., Yagasaki, K., Horiguchi, M., Kawase, Y., & Kanda, T. (1986). Congenital stationary night blindness with negative electroretinogram. A new classification. Archives in Ophthalmology 104, 1013–1020.Google Scholar
Morgans, C.W. (1999). Calcium channel heterogeneity among cone photoreceptors in the tree shrew retina. European Journal of Neuroscience 11, 2989–2993.CrossRefGoogle Scholar
Morgans, C.W. (2001). Localization of the {alpha}1F calcium channel subunit in the rat retina. Investigative Ophthalmology and Visual Science 42, 2414–2418.Google Scholar
Morgans, C.W., BrandstÄtter, J.H., Kellerman, J., Betz, H., & Wässle, H. (1996). A SNARE complex containing syntaxin 3 is present in ribbon synapses of the retina. Journal of Neuroscience 16, 6713–6721.Google Scholar
Morgans, C.W., El Far, O., Berntson, A., Wassle, H., & Taylor, W.R. (1998). Calcium extrusion from mammalian photoreceptor terminals. Journal of Neuroscience 18, 2467–2474.Google Scholar
Morgans, C.W., Gaughwin, P., & Maleszka, R. (2001). Expression of the alpha1F calcium channel subunit by photoreceptors in the rat retina. Molecular Vision 7, 202–209.Google Scholar
Orton, N., Mansergh, F., Vessey, J., Lalonde, M., Tremblay, F., Barnes, S., Rancourt, D., Stell, W., & Bech-Hansen, N. (2004). Mutation of the calcium channel gene cacna1f disrupts calcium signaling and synaptic transmission in the mouse retina. IOVS 2004; 45:ARVO Abstract 2507.Google Scholar
Reuter, H. (1996). Diversity and function of presynaptic calcium channels in the brain. Current Opinions in Neurobiology 6, 331–337.CrossRefGoogle Scholar
Ruether, K., Apfelstedt-Sylla, E., & Zrenner, E. (1993). Clinical findings in patients with congenital stationary night blindness of the Schubert-Bornschein type. German Journal of Ophthalmology 2, 429–435.Google Scholar
Schmitz, F., Konigstorfer, A., & Sudhof, T. (2000). RIBEYE, a component of synaptic ribbons: A protein's journey through evolution provides insight into synaptic ribbon function. Neuron 28, 857–872.CrossRefGoogle Scholar
Schneeweis, D.M. & Schnapf, J.L. (1995). Photovoltage of rods and cones in the macaque retina. Science 268, 1053–1056.CrossRefGoogle Scholar
Schneeweis, D.M. & Schnapf, J.L. (1999). The photovoltage of macaque cone photoreceptors: adaptation, noise, and kinetics. Journal of Neuroscience 19, 1203–1216.Google Scholar
Strom, T.M., Nyakatura, G., Apfelstedt-Sylla, E., Hellebrand, H., Lorenz, B., Weber, B.H.F., Wutz, K., Gutwillinger, N., Ruther, K., Drescher, B., Sauer, C., Zrenner, E., Meitinger, T., Rosenthal, A., & Meindl, A. (1998). An L-type calcium-channel gene mutated in incomplete X-linked congenital stationary night blindness. Nature Genetics 19, 260–263.Google Scholar
Taylor, W.R. & Morgans, C.W. (1998). Localization and properties of voltage-gated calcium channels in cone photoreceptors of Tupaia belangeri. Visual Neuroscience 15, 541–552.Google Scholar
Tremblay, F., De Becker, I., Cheung, C., & Laroche, G. (1996). Visual evoked potentials with crossed asymmetry in incomplete congenital stationary night blindness. Investigative Ophthalmology and Visual Science 37, 1783–1792.Google Scholar
Tsukamoto, Y., Morigiwa, K., Ueda, M., & Sterling, P. (2001). Microcircuits for night vision in mouse retina. Journal of Neuroscience 21, 8616–8623.Google Scholar
Wang, Y., Okamoto, M., Schmitz, F., Hofmann, K., & Südhof, T.C. (1997). Rim is a putative Rab3 effector in regulating synaptic-vesicle fusion. Nature 388, 593–598.CrossRefGoogle Scholar
Wässle, H., Haverkamp, S., Grünert, U., & Morgnas, C. (2003). The cone pedicle, the first synapse in the retina. In The Neural Basis of Early Vision, ed. Kaneko, A., pp. 19–38. Tokyo: Springer-Verlag.CrossRef
Wheeler, D.B., Randall, A., Tsien, R.W., Ullrich, B., & Südhof, T.C. (1994). Roles of N-type and Q-type Ca2+ channels in supporting hippocampal synaptic transmission. Science 264, 107–111.CrossRefGoogle Scholar
Wilkinson, M.F. & Barnes, S. (1996). The dihydropyridine-sensitive calcium channel subtype in cone photoreceptors. Journal of General Physiology 107, 621–630.CrossRefGoogle Scholar
Yagi, T. & Macleish, P.R. (1994). Ionic conductances of monkey solitary cone inner segments. Journal of Neurophysiology 71, 656–665.Google Scholar