Hostname: page-component-78c5997874-t5tsf Total loading time: 0 Render date: 2024-11-03T01:02:35.520Z Has data issue: false hasContentIssue false
  • English
  • Français

HCN4-like immunoreactivity in rat retinal ganglion cells

Published online by Cambridge University Press:  18 February 2008

HANAKO OI ,
GLORIA J. PARTIDA ,
SHERWIN C. LEE  and
ANDREW T. ISHIDA
HANAKO OI
Affiliation:
Section of Neurobiology, Physiology and Behavior, University of California, Davis, California
GLORIA J. PARTIDA
Affiliation:
Section of Neurobiology, Physiology and Behavior, University of California, Davis, California
SHERWIN C. LEE
Affiliation:
Section of Neurobiology, Physiology and Behavior, University of California, Davis, California
ANDREW T. ISHIDA
Affiliation:
Section of Neurobiology, Physiology and Behavior, University of California, Davis, California Department of Ophthalmology and Vision Science, University of California, Davis, California
Get access Rights & Permissions [Opens in a new window]

Abstract

Antisera directed against hyperpolarization-activated, cyclic nucleotide–sensitive (HCN) channels bind to somata in the ganglion cell layer of rat and rabbit retinas, and mRNA for different HCN channel isoforms has been detected in the ganglion cell layer of mouse retina. However, previous studies neither provided evidence that any of the somata are ganglion cells (as opposed to displaced amacrine cells) nor quantified these cells. We therefore tested whether isoform-specific anti-HCN channel antisera bind to ganglion cells labeled by retrograde transport of fluorophore-coupled dextran. In flat-mounted adult rat retinas, the number of dextran-backfilled ganglion cells agreed with cell densities reported in previous studies, and anti-HCN4 antisera bound to the somata of approximately 40% of these cells. The diameter of these somata ranged from 7 to 30 μm. Consistent with localization to cell membranes, the immunoreactivity formed a thin line that circumscribed individual somata. Optic fiber layer axon fascicles, and the proximal dendrites of some ganglion cells, also displayed binding of anti-HCN4 antisera. These results suggest that the response of some mammalian retinal ganglion cells to hyperpolarization may be modulated by changes in intracellular cAMP levels, and could thus be more complex than expected from previous voltage and current recordings.

Keywords

ImmunocytochemistryRetinal ganglion cellsHCN channels
Type
BRIEF COMMUNICATION
Information
Visual Neuroscience , Volume 25 , Issue 1 , January 2008 , pp. 95 - 102
Copyright
© 2008 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

Altomare, C., Bucchi, A., Camatini, E., Baruscotti, M., Viscomi, C., Moroni, A. & DiFrancesco, D. (2001). Integrated allosteric model of voltage gating of HCN channels. Journal of General Physiology 117, 519–532.Google Scholar
Bunt, A.H., Lund, R.D. & Lund, J.S. (1974). Retrograde axonal transport of horseradish peroxidase by ganglion cells of the albino rat retina. Brain Research 73, 215–228.Google Scholar
Chen, L., Yu, Y.C., Zhao, J.W. & Yang, X.L. (2004). Inwardly rectifying potassium channels in rat retinal ganglion cells. European Journal of Neuroscience 20, 956–964.Google Scholar
Chen, S., Wang, J. & Siegelbaum, S.A. (2001). Properties of hyperpolarization-activated pacemaker current defined by coassembly of HCN1 and HCN2 subunits and basal modulation by cyclic nucleotide. Journal of General Physiology 117, 491–504.Google Scholar
Danias, J., Shen, F., Goldblum, D., Chen, B., Ramos-Esteban, J., Podos, S.M. & MITTAG, T. (2002). Cytoarchitecture of the retinal ganglion cells in the rat. Investigative Ophthalmology and Visual Science 43, 587–594.Google Scholar
Dreher, B., Sefton, A.J., Ni, S.Y. & Nisbett, G. (1985). The morphology, number, distribution and central projections of Class I retinal ganglion cells in albino and hooded rats. Brain, Behavior and Evolution 26, 10–48.Google Scholar
Dunn, T.A., Wang, C.T., Colicos, M.A., Zaccolo, M., DiPilato, L.M., Zhang, J., Tsien, R.Y. & Feller, M.B. (2006). Imaging of cAMP levels and protein kinase A activity reveals that retinal waves drive oscillations in second-messenger cascades. Journal of Neuroscience 26, 12807–12815.Google Scholar
Eng, D.L., Gordon, T.R., Kocsis, J.D. & Waxman, S.G. (1990). Current-clamp analysis of a time-dependent rectification in rat optic nerve. Journal of Physiology 421, 185–202.Google Scholar
Franz, O., Liss, B., Neu, A. & Roeper, J. (2000). Single-cell mRNA expression of HCN1 correlate with a fast gating phenotype of hyperpolarization-activated cyclic nucleotide-activated ion channels (Ih) in central neurons. European Journal of Neuroscience 12, 2685–2693.Google Scholar
Fyk-Kolodziej, B. & Pourcho, R.G. (2007). Differential distribution of hyperpolarization-activated and cyclic nucleotide-gated channels in cone bipolar cells of the rat retina. Journal of Comparative Neurology 501, 891–903.Google Scholar
Hayashida, Y. & Ishida, A.T. (2004). Dopamine receptor activation can reduce voltage-gated Na+ current by modulating both entry into and recovery from inactivation. Journal of Neurophysiology 92, 3134–3141.Google Scholar
Huang, X.R., Knighton, R.W. & Shestopalov, V. (2006). Quantifying retinal nerve fiber layer thickness in whole-mounted retina. Experimental Eye Research 83, 1096–1101.Google Scholar
Huxlin, K.R. & Goodchild, A.K. (1997). Retinal ganglion cells in the albino rat: revised morphological classification. Journal of Comparative Neurology 385, 309–323.Google Scholar
Kim, I.B., Lee, E.J., Kang, T.H., Chung, J.W. & Chun, M.H. (2003). Morphological analysis of the hyperpolarization-activated cyclic nucleotide-gated cation channel 1 (HCN1) immunoreactive bipolar cells in the rabbit retina. Journal of Comparative Neurology 467, 389–402.Google Scholar
Kim, K.J. & Rieke, F. (2001). Temporal contrast adaptation in the input and output signals of salamander retinal ganglion cells. Journal of Neuroscience 21, 287–299.Google Scholar
Koizumi, A., Jakobs, T.C. & Masland, R.H. (2004). Inward rectifying currents stabilize the membrane potential in dendrites of mouse amacrine cells: Patch-clamp recordings and single-cell RT-PCR. Molecular Vision 10, 328–340.Google Scholar
Larsen, J.N., Bersani, M., Olcese, J., Holst, J.J. & Møller M. (1990). Somatostatin and prosomatostatin in the retina of the rat: An immunohistochemical, in-situ hybridization, and chromatographic study. Visual Neuroscience 5, 441–452.Google Scholar
Lee, S.C., Hayashida, Y. & Ishida, A.T. (2003). Availability of low-threshold Ca2+ current in retinal ganglion cells. Journal of Neurophysiology 90, 3888–3901.Google Scholar
Lee, S.C. & Ishida, A.T. (2007). Ih without Kir in adult rat retinal ganglion cells. Journal of Neurophysiology 97, 3790–3799.Google Scholar
Lipton, S.A. & Tauck, D.L. (1987). Voltage-dependent conductances of solitary ganglion cells dissociated from the rat retina. Journal of Physiology 385, 361–391.Google Scholar
Ludwig, A., Zong, X., Jeglitsch, M., Hofmann, F. & Biel, M. (1998). A family of hyperpolarization-activated mammalian cation channels. Nature 393, 587–591.Google Scholar
Lukasiewicz, P.D. & Werblin, F.S. (1988). A slowly inactivating potassium current truncates spike activity in ganglion cells of the tiger salamander retina. Journal of Neuroscience 8, 4470–4481.Google Scholar
Martin-Martinelli, E., Savy, C. & Nguyen-Legros, J. (1994). Morphometry and distribution of displaced dopaminergic cells in rat retina. Brain Research Bulletin 34, 467–482.Google Scholar
Mills, S.L., Xia, X.B., Hoshi, H., Firth, S.I., Rice, M.E., Frishman, L.J. & Marshak, D.W. (2007). Dopaminergic modulation of tracer coupling in a ganglion-amacrine cell network. Visual Neuroscience 24, 1–16.Google Scholar
Moosmang, S., Stieber, J., Zong, X., Biel, M., Hofmann, F. & Ludwig, A. (2001). Cellular expression and functional characterization of four hyperpolarization-activated pacemaker channels in cardiac and neuronal tissues. European Journal of Biochemistry 268, 1646–1652.Google Scholar
Müller, F., Scholten, A., Ivanova, E., Haverkamp, S., Kremmer, E. & Kaupp, U.B. (2003). HCN channels are expressed differentially in retinal bipolar cells and concentrated at synaptic terminals. European Journal of Neuroscience 17, 2084–2096.Google Scholar
Nir, I., Harrison, J.M., Haque, R., Low, M.J., Grandy, D.K., Rubinstein, M. & Iuvone, P.M. (2002). Dysfunctional light-evoked regulation of cAMP in photoreceptors and abnormal retinal adaptation in mice lacking dopamine D4 receptors. Journal of Neuroscience 22, 2063–2073.Google Scholar
O'Brien, B.J., Isayama, T., Richardson, R. & Berson, D.M. (2002). Intrinsic physiological properties of cat retinal ganglion cells. Journal of Physiology 538, 787–802.Google Scholar
Partida, G.J., Lee, S.C., Haft-Candell, L., Nichols, G.S. & Ishida, A.T. (2004). DARPP-32-like immunoreactivity in AII amacrine cells of rat retina. Journal of Comparative Neurology 480, 251–263.Google Scholar
Peichl, L. (1989). Alpha and delta ganglion cells in the rat retina. Journal of Comparative Neurology 286, 120–139.Google Scholar
Perry, V.H. (1981). Evidence for an amacrine cell system in the ganglion cell layer of the rat retina. Neuroscience 6, 931–944.Google Scholar
Reiff, D.F. & Guenther, E. (1999). Developmental changes in voltage-activated potassium currents of rat retinal ganglion cells. Neuroscience 92, 1103–1117.Google Scholar
Santoro, B., Chen, S., Luthi, A., Pavlidis, P., Shumyatsky, G.P., Tibbs, G.R. & Siegelbaum, S.A. (2000). Molecular and functional heterogeneity of hyperpolarization-activated pacemaker channels in the mouse CNS. Journal of Neuroscience 20, 5264–5275.Google Scholar
Santoro, B. & Tibbs, G.R. (1999). The HCN gene family: Molecular basis of the hyperpolarization-activated pacemaker channels. Annals of the New York Academy of Sciences 868, 741–764.Google Scholar
Sun, W., Li, N. & He, S. (2002). Large-scale morphological survey of rat retinal ganglion cells. Visual Neuroscience 19, 483–493.Google Scholar
Tabata, T. & Ishida, A.T. (1996). Transient and sustained depolarization of retinal ganglion cells by Ih. Journal of Neurophysiology 75, 1932–1943.Google Scholar
Vaquero, C.F., Pignatelli, A., Partida, G.J. & Ishida, A.T. (2001). A dopamine- and protein kinase A-dependent mechanism for network adaptation in retinal ganglion cells. Journal of Neuroscience 21, 8624–8635.Google Scholar
Vidal-Sanz, M., Villegas-Perez, M.P., Bray, G.M. & Aguayo, A.J. (1988). Persistent retrograde labeling of adult rat retinal with the carbocyanine dye diI. Experimental Neurology 102, 92–101.Google Scholar
Yeh, H.H. & Olschowka, J.A. (1989). A system of corticotropin releasing factor-containing amacrine cells in the rat retina. Neuroscience 33, 229–240.Google Scholar