Modulation of an electrical synapse between solitary pairs of catfish horizontal cells by dopamine and second messengers.
- 1 July 1989
- journal article
- research article
- Published by Wiley in The Journal of Physiology
- Vol. 414 (1) , 351-375
- https://doi.org/10.1113/jphysiol.1989.sp017692
Abstract
1. Retinas from channel catfish were dissociated and the cells maintained in culture. Horizontal cells that normally receive input from cone photoreceptors were identified. The conductance of the electrical junction formed between a pair of ‘cone’ horizontal cells was measured by controlling the membrane voltage of each cell with a voltage clamp maintained through either a micropipette or a patch pipette. The two techniques yielded similar results. 2. Transjunctional current was measured while transjunctional voltage was stepped to values between +/‐ 60 mV. The current (measured 5 ms after a step) was proportional to voltage over the range tested. For steps to voltages greater than +/‐ 45 mV, the current exhibited a slight time‐dependent decline. 3. Dopamine decreased junctional conductance in a dose‐dependent fashion. A 50% reduction was obtained with 10 nM‐dopamine. The D1 agonist fenoldopam (100 nM) also decreased junctional conductance. The uncoupling produced by either agent was rapid and reversible. 4. The introduction of 100 microM‐cyclic AMP into one cell of a pair decreased junctional conductance by, on average, 40%. Forskolin (1‐10 microM), an activator of adenylate cyclase, decreased junctional conductance 50‐90%. 5. The introduction of 80 microM‐cyclic GMP into one cell of a pair decreased junctional conductance by, on average, 40%. Nitroprusside (1‐10 microM), an activator of guanylate cyclase, reduced junctional conductance 40‐65%. 6. The introduction of a peptide inhibitor specific for the cyclic AMP‐dependent protein kinase reversed a decrease in junctional conductance produced by superfusion with either dopamine (1 microM), fenoldopam (100 nM) or forskolin (5‐10 microM). 7. Intracellular Ca2+ concentration was measured with the fluorescent indicator Fura‐2. The intracellular Ca2+ concentration was increased by activation of a Ca2+ current. Junctional conductance remained constant as the internal Ca2+ concentration changed from 100 to 700 nM. 8. Intracellular pH was measured with the fluorescent indicator bis‐carboxyethylcarboxyfluorescein. The application of acetate (2.5 mM) reduced intracellular pH by 0.2‐0.3 units and decreased junctional conductance by approximately 50%. A subsequent application of fenoldopam did not alter intracellular pH, but decreased junctional conductance by more than 50%. 9. The sensitivity of the junctional conductance between isolated horizontal cells to dopamine is consistent with dopamine having a direct effect on coupling in intact retina. Dopamine regulates the activity of a cyclic AMP‐dependent protein kinase which in turn modulates junctional conductance. Changes in intracellular pH and Ca2+ concentration are not involved in mediating the effect of dopamine on coupling. Cyclic GMP and intracellular pH may participate in regulatory pathways independent of that used by cyclic AMP.This publication has 37 references indexed in Scilit:
- Inositol trisphosphate, a novel second messenger in cellular signal transductionNature, 1984
- Determination of synaptic phenotype: insulin and cAMP independently initiate development of electrotonic coupling between cultured sympathetic neurons.Proceedings of the National Academy of Sciences, 1984
- Ionic currents of solitary horizontal cells isolated from goldfish retina.The Journal of Physiology, 1983
- Dopamine modulates S-potential amplitude and dye-coupling between external horizontal cells in carp retinaNature, 1983
- Aluminum: a requirement for activation of the regulatory component of adenylate cyclase by fluoride.Proceedings of the National Academy of Sciences, 1982
- Carp horizontal cells in culture respond selectively to L-glutamate and its agonists.Proceedings of the National Academy of Sciences, 1982
- CHARACTERIZATION OF THE PERIPHERAL AND CENTRAL EFFECTS OF SK-AND-F 82526, A NOVEL DOPAMINE RECEPTOR AGONIST1982
- Isolated horizontal cells from carp retina demonstrate dopamine-dependent accumulation of cyclic AMP.Proceedings of the National Academy of Sciences, 1981
- Junctional intercellular communication: the cell-to-cell membrane channel.Physiological Reviews, 1981
- Surface Movements during the Growth of Single Explanted NeuronsProceedings of the National Academy of Sciences, 1970