Divalent Cation Selectivity Is a Function of Gating in Native and Recombinant Cyclic Nucleotide–gated Ion Channels from Retinal Photoreceptors

Jun 3, 1999The Journal of general physiology

How ion channel opening controls preference for certain ions in light-sensing eye cells

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Abstract

The selectivity of Ca2+ over Na+ is approximately 7.4-fold greater in cone photoreceptors than in rod photoreceptors under dark-adapted conditions.

Cyclic nucleotide concentration affects the ion selectivity of cGMP-gated channels in both rod and cone photoreceptors.
The probability of channel opening ranges from 1-5% in darkness to nearly zero in bright light, influencing ion selectivity.
As the probability of channel opening increases, the selectivity for Ca2+ over Na+ also increases.
Ion selectivity for divalent cations is specifically linked to the gating of the channels.
Cyclic nucleotide-gated channels in rod photoreceptors consist of heteromeric assemblies of alpha and beta subunits, influencing their selectivity.

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The selectivity of Ca2+ over Na+ is approximately 3.3-fold larger in cGMP-gated channels of cone photoreceptors than in those of rods when measured under saturating cGMP concentrations, where the probability of channel opening is 85-90%. Under physiological conditions, however, the probability of opening of the cGMP-gated channels ranges from its largest value in darkness of 1-5% to essentially zero under continuous, bright illumination. We investigated the ion selectivity of cGMP-gated channels as a function of cyclic nucleotide concentration in membrane patches detached from the outer segments of rod and cone photoreceptors and have found that ion selectivity is linked to gating. We determined ion selectivity relative to Na+ (PX/PNa) from the value of reversal potentials measured under ion concentration gradients. The selectivity for Ca2+ over Na+ increases continuously as the probability of channel opening rises. The dependence of PCa/PNa on cGMP concentration, in both rods and cones, is well described by the same Hill function that describes the cGMP dependence of current amplitude. At the cytoplasmic cGMP concentrations expected in dark-adapted intact photoreceptors, PCa/PNa in cone channels is approximately 7.4-fold greater than that in rods. The linkage between selectivity and gating is specific for divalent cations. The selectivity of Ca2+ and Sr2+ changes with cGMP concentration, but the selectivity of inorganic monovalent cations, Cs+ and NH4+, and organic cations, methylammonium+ and dimethylammonium+, is invariant with cGMP. Cyclic nucleotide-gated channels in rod photoreceptors are heteromeric assemblies of alpha and beta subunits. The maximal PCa/PNa of channels formed from alpha subunits of bovine rod channels is less than that of heteromeric channels formed from alpha and beta subunits. In addition, Ca2+ is a more effective blocker of channels formed by alpha subunits than of channels formed by alpha and beta subunits. The cGMP-dependent shift in divalent cation selectivity is a property of alphabeta channels and not of channels formed from alpha subunits alone.

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Divalent Cation Selectivity Is a Function of Gating in Native and Recombinant Cyclic Nucleotide–gated Ion Channels from Retinal Photoreceptors

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