Hostname: page-component-7c8c6479df-hgkh8 Total loading time: 0 Render date: 2024-03-28T17:27:28.127Z Has data issue: false hasContentIssue false

Retinal bipolar cell types differ in their inventory of ion channels

Published online by Cambridge University Press:  24 April 2006

ELENA IVANOVA
Affiliation:
Institut für Biologische Informationsverarbeitung 1, Forschungszentrum Jülich, Jülich, Germany
FRANK MÜLLER
Affiliation:
Institut für Biologische Informationsverarbeitung 1, Forschungszentrum Jülich, Jülich, Germany

Abstract

Bipolar cells were recorded in rat retinal slices to study the distribution of hyperpolarization-activated and cyclic nucleotide-gated (HCN) channels. Patch-clamp whole cell measurements were combined with intracellular filling and recorded cells were morphologically identified. HCN channel isoforms HCN1-4 are differentially expressed in bipolar cells. Each bipolar cell type has a characteristic inventory of HCN channels. The combination of HCN channel currents and other voltage-gated currents can be used as a kind of “finger print” to electrophysiologically identify and classify bipolar cell types. Using this approach of combined electrophysiological and morphological classification we could identify a new ON-cone bipolar cell type.

Type
Research Article
Copyright
2006 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

Akopian, A. & Witkovsky, P. (1996). D2 dopamine receptor-mediated inhibition of a hyperpolarization activated current in rod photoreceptors. Journal of Neurophysiology 76, 18281835.Google Scholar
Awatramani, G.B. & Slaughter, M.M. (2000). Origin of transient and sustained responses in ganglion cells of the retina. Journal of Neuroscience 20, 70877095.Google Scholar
Boos, R., Schneider, H., & Wässle, H. (1993). Voltage- and transmitter-gated currents of AII-amacrine cells in a slice preparation of the rat retina. Journal of Neuroscience 13, 28742888.Google Scholar
Clark, S., Jordt, S.E., Jentsch, T.J., & Mathie, A. (1998). Characterization of the hyperpolarization-activated chloride current in dissociated rat sympathetic neurons. Journal of Physiology 506, 665678.CrossRefGoogle Scholar
Connaughton, V.P. & Maguire, G. (1998). Differential expression of voltage-gated K+ and Ca2+ currents in bipolar cells in the zebrafish retinal slice. European Journal of Neuroscience 10, 13501362.CrossRefGoogle Scholar
Demontis, G.C., Longoni, B., Barcaro, U., & Cervetto, L. (1999). Properties and functional roles of hyperpolarization-gated currents in guinea-pig retinal rods. Journal of Physiology 515, 813828.CrossRefGoogle Scholar
Euler, T. & Masland, R.H. (2000). Light-evoked responses of bipolar cells in a mammalian retina. Journal of Neurophysiology 83, 18171829.Google Scholar
Euler, T., Schneider, H., & Wässle, H. (1996). Glutamate response of bipolar cells in a slice preparation of the rat retina. Journal of Neuroscience 16, 29342944.Google Scholar
Euler, T. & Wässle, H. (1995). Immunocytochemical identification of cone bipolar cells in the rat retina. Journal of Comparative Neurology 361, 461478.CrossRefGoogle Scholar
Enz, R., Ross, B.J., & Cutting, G.R. (1999). Expression of the voltage-gated chloride channel ClC-2 in rod bipolar cells of the rat retina. Journal of Neuroscience 19, 98419847.Google Scholar
Feigenspan, A. & Bormann, J. (1994). Facilitation of GABAergic signaling in the retina by receptors stimulating adenylate cyclase. Proceedings of the National Academy of Sciences of the United States of America 91, 1089310897.CrossRefGoogle Scholar
Gotzes, S., de Vente, J., & Müller, F. (1998). Nitric oxide modulates cGMP levels in neurons of the inner and outer retina in opposite ways. Visual Neuroscience 15, 945955.Google Scholar
Haeseleer, F., Sokal, I., Verlinde, C.L., Erdjument-Bromage, H., Tempst, P., Pronin, A.N., Benovic, J.L., Fariss R.N., &Palczewski K. (2000). Five members of a novel Ca2+-binding protein (CABP) subfamily with similarity to calmodulin. Journal of Biological Chemistry 275, 12471260.CrossRefGoogle Scholar
Hartveit, E. (1997). Functional organization of cone bipolar cells in the rat retina. Journal of Neurophysiology 77, 17161730.Google Scholar
Haverkamp, S., Ghosh, K.K., Hirano, A., & Wässle, H. (2003). Immunocytochemical description of five bipolar cell types of the mouse retina. Journal of Comparative Neurology 455, 463476.CrossRefGoogle Scholar
Haverkamp, S. & Wässle, H. (2000). Immunocytochemical analysis of the mouse retina. Journal of Comparative Neurology 424, 123.Google Scholar
Hu, H.J. & Pan, Z.H. (2002). Differential expression of K(+) currents in mammalian retinal bipolar cells. Visual Neuroscience 19, 163173.CrossRefGoogle Scholar
Kaneko, A., Pinto, L.H., & Tachibana, M. (1989). Transient calcium current of retinal bipolar cells of the mouse. Journal of Physiology 410, 613629.CrossRefGoogle Scholar
Kaneko, A. & Tachibana, M. (1985). A voltage-clamp analysis of membrane currents in solitary bipolar cells dissociated from Carassius auratus. Journal of Physiology (Lond.) 358, 131152.CrossRefGoogle Scholar
Karschin, A. & Wässle, H. (1990). Voltage- and transmitter-gated currents in isolated rod bipolar cells of rat retina. Journal of Neurophysiology 63, 860876.Google Scholar
Kaupp, U.B. & Seifert, R. (2001). Molecular diversity of pacemaker ion channels. Annual Review of Physiology 63, 235257.CrossRefGoogle Scholar
Lasater, E.M. (1988). Membrane currents of retinal bipolar cells in culture. Journal of Neurophysiology 60, 14601480.Google Scholar
Ludwig, A., Zong, X., Jeglitsch, M., Hofmann, F., & Biel, M. (1998). A family of hyperpolarization-activated mammalian cation channels. Nature 393, 587591.CrossRefGoogle Scholar
Ludwig, A., Zong, X., Stieber, J., Hullin, R., Hofmann, F., & Biel, M. (1999). Two pacemaker channels from human heart with profoundly different activation kinetics. European Molecular Biology Organization Journal 18, 23232329.CrossRefGoogle Scholar
Ma, Y.P., Cu, J., Hu, H.J., & Pan, Z.H. (2003). Mammalian retinal bipolar cells express inwardly rectifying K+ currents (IKir) with a different distribution than that of Ih. Journal of Neurophysiology 90, 34793489.CrossRefGoogle Scholar
Masland, R.H. (2001). The fundamental plan of the retina. Nature Reviews Neuroscience 4, 877886.CrossRefGoogle 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, 20842096.CrossRefGoogle Scholar
Okada, T., Horiguchi, H., & Tachibana, M. (1995). Ca (2+)-dependent Cl- current at the presynaptic terminals of goldfish retinal bipolar cells. Neuroscience Research 23, 297303.CrossRefGoogle Scholar
Pan, Z.H. (2000). Differential expression of high- and two types of low-voltage-activated calcium currents in rod and cone bipolar cells of the rat retina. Journal of Neurophysiology 83, 513527.Google Scholar
Pan, Z.H. & Hu, H.J. (2000). Voltage-dependent Na(+) currents in mammalian retinal cone bipolar cells. Journal of Neurophysiology 84, 25642571.Google Scholar
Pan, Z.H., Hu, H.J., Perring, P., & Andrade, R. (2001). T-type Ca(2+) channels mediate neuro-transmitter release in retinal bipolar cells. Neuron 32, 8998.CrossRefGoogle Scholar
Petrucci, C., Resta, V., Fien, F., Bigiani, A., & Bagnoli, P. (2001). Modulation of potassium current and calcium influx by somatostatin in rod bipolar cells isolated from the rabbit retina via sst2 receptors. Naunyn-Schmiedeberg's Archives of Pharmacology 363, 680694.CrossRefGoogle Scholar
Protti, D.A., Flores-Herr, N., & von Gersdorff, H. (2000). Light evokes Ca(2+) spikes in the axon terminal of a retinal bipolar cell. Neuron 25, 215227.CrossRefGoogle Scholar
Protti, D.A. & Llano, I. (1998). Calcium currents and calcium signaling in rod bipolar cells of rat retinal slices. Journal of Neuroscience 18, 37153724.Google Scholar
Qu, J., Kryukova, Y., Potapova, I.A., Doronin, S.V., Larsen, M., Krishnamurthy, G., Cohen, I.S., & Robinson, R.B. (2004). MiRP1 modulates HCN2 channel expression and gating in cardiac myocytes. Journal of Biological Chemistry 279, 4349743502.CrossRefGoogle Scholar
Santoro, B., Liu, D.T., Yao, H., Bartsch, D., Kandel, E.R., Siegelbaum, S.A., & Tibbs, G.R. (1998). Identification of a gene encoding a hyperpolarization-activated pacemaker channel of brain. Cell 93, 717729.CrossRefGoogle Scholar
Seifert, R., Scholten, A., Gauss, R., Mincheva, A., Lichter, P., & Kaupp, U.B. (1999). Molecular characterization of a slowly gating human hyperpolarization-activated channel predominantly expressed in thalamus, heart, and testis. Proceedings of the National Academy of Sciences of the United States of America 96, 93919396.CrossRefGoogle Scholar
Tabata, T. & Ishida, A.T. (1996). Transient and sustained depolarization of retinal ganglion cells by Ih. Journal of Neurophysiology 75, 19321943.Google Scholar
Vaney, D.I., Nelson, J.C., & Pow, D.V. (1998). Neurotransmitter coupling through gap junctions in the retina. Journal of Neuroscience 18, 1059410602.Google Scholar
Veruki, M.L. & Yeh, H.H. (1994). Vasoactive intestinal polypeptide modulates GABAA receptor function through activation of cyclic AMP. Visual Neuroscience 11, 899908.CrossRefGoogle Scholar
Wässle, H. (2004). Parallel processing in the mammalian retina. Nature Reviews Neuroscience 5, 747757.CrossRefGoogle Scholar
Wässle, H. & Boycott, B.B. (1991). Functional architecture of the mammalian retina. Physiological Reviews 71, 447480.Google Scholar
Yazulla, S., Studholme, K.M., Fan, S.F., & Mora-Ferrer, C. (2001). Neuromodulation of voltage-dependent K+ channels in bipolar cells: immunocytochemical and electrophysiological studies. Progress in Brain Research 131, 201213.CrossRefGoogle Scholar
Yu, H., Wu, J., Potapova, I., Wymore, R.T., Holmes, B., Zuckerman, J., Pan, Z., Wang, H., Shi, W., Robinson, R.B., El-Maghrabi, M.R., Benjamin, W., Dixon, J., McKinnon, D., Cohen, I.S., & Wymore, R. (2001). MinK-related peptide 1. A β subunit for the HCN ion channel subunit family enhances expression and speeds activation. Circulation Research 88, 8487.Google Scholar