Permeability and interaction of Ca2+ with cGMP-gated ion channels differ in retinal rod and cone photoreceptors

Jul 1, 1995Biophysical journal

How Calcium Moves Through and Affects Light-Sensing Channels Differ in Rod and Cone Cells of the Eye

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Abstract

The permeability ratio of calcium to sodium ions in cGMP-gated channels is 7.6 in cones compared to 3.1 in rods.

Cyclic GMP-dependent channels in cones have a higher calcium permeability ratio than those in rods.
Calcium ions block both cone and rod channels in a way that depends on voltage.
The extent of calcium block is similar for both types of channels near the reversal potential.
Voltage changes can relieve calcium block, but this relief is more effective in cones than in rods.
Differences in calcium binding sites may explain the distinct calcium permeability and phototransduction signals between cones and rods.

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We studied the ionic permeability of cGMP-dependent currents in membrane patches detached from the outer segment of retinal cone and rod photoreceptors. Reversal potentials measured in membranes exposed to symmetric Na+ but with varying cytoplasmic Ca2+ concentrations reveal that the permeability ratio, PCa/PNa, is higher in the cGMP-gated channels of cones (7.6 +/- 0.8) than in those of rods (3.1 +/- 1.0). Ca2+ blocks both channels in a voltage-dependent manner. At any Ca2+ concentration, the channel block is maximal near the ionic reversal potential. The maximal block is essentially identical in channels of cones and rods with respect to its extent and voltage and Ca2+ dependence. The Ca2+ block is relieved by voltage, but the features of this relief differ markedly between rods and cones. Whereas the Boltzmann distribution function describes the relief of block by hyperpolarizing voltages, any given voltage is more effective in relieving the Ca2+ block in cones than in rods. Similarly, depolarizing voltages more effectively relieve Ca2+ block in cones than in rods. Our results suggest that channels contain two binding sites for Ca2+, one of which is similar in the two receptor types. The second site either interacts more strongly with Ca2+ than the first one or it is located differently in the membrane, so as to be less sensitive to membrane voltage. The channels in rods and cones differ in the features of this second site. The difference in Ca2+ permeability between the channels is likely to result in light-dependent changes in cytoplasmic Ca2+ concentration that are larger and faster in cones than in rods. The functional differences between channels, therefore, may be critically important in explaining the differences in the phototransduction signal of the two photoreceptor types.

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Permeability and interaction of Ca2+ with cGMP-gated ion channels differ in retinal rod and cone photoreceptors

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