Kinetic properties of single-ion channels activated by light in Limulus ventral nerve photoreceptors

Abstract

Previous results on Limulus ventral photoreceptors have suggested that besides inositol trisphosphate, another unknown transmitter may also work in the transduction cascade. This assumption has been supported by the finding of two light-activated channel types. The present report furnishes further evidence of the dual transmitter mechanism in phototransduction by analyzing the kinetic properties and voltage dependency of these cation channels with conductances of ~12pS and ~30pS. Single-channel currents were recorded in Limulus ventral nerve photoreceptors in cell-attached configuration at 14 °C. At Vm~ + 80 mV, the open-time histograms of both channels were fit best by the sum of two exponentials; time constants (and weights) were: 0.81 ms (0.62) and 6.20 ms (0.38) for the 12 pS channels and 2.38 ms (0.43) and 19.4 ms (0.57) for the 30 pS channels. At this potential the mean open times were 2.7 ms for the 12pS and 13.3 ms for the 30 pS channels, about two-times larger than at hyperpolarizing potentials. The deactivation kinetics were also different for the two channels. The time constants of the decay of the channel activity, after switching off the light, were 2.5 s for the 12 pS and 12.9 s for the 30 pS channels. The 12 pS channel exhibits bursting and subconductance states at positive potentials. The subconductances are about 20%, 46% and 72% of the fully open state. Results show that the two types of light-activated channels have different kinetic parameters, voltage dependence and gating mechanisms. The two channels are suggested to be gated by different transmitters or processes. It is proposed that for the 30 pS channel the transmitter could be calcium ion or a calcium-dependent transmitter.

Three components in the light‐induced current of the Limulus ventral photoreceptor.

“…One of the components may be activated by intracellular calcium ions while the other two are activated by different transmitters. This hypothesis is also discussed by Bolsover & Brown (1985), Payne et al (1986b) and Nagy (1990Nagy ( , 1991.…”

“…This conclusion is supported by previous results as well. Three types of single light-induced ion channels have been found in Limulus ventral photoreceptors (Nagy & Stieve, 1990;Nagy, 1990). Although it is not yet clear, due to the different experimental conditions, whether these different channel types cause the current components, we nevertheless assume this to be the most probable explanation.…”

“…This accounts for component 1, which is the smallest. The channels having the second largest reversal potential and largest single-channel conductance (30 pS; Nagy, 1990) have the longest latency and slowest decay after illumination. These channels could be responsible for the third component.…”

“…However, indications are accumulating suggesting that the light-induced current is composed of multiple components (Maaz, Nagy, Stieve & KlomfaB, 1981; Stieve, Schnakenberg, Kuhn & Reuss, 1986;Helrich, Stieve & Deckert, 1988) and that the transduction mechanism may have different pathways (Payne & Fein, 1986;Payne, Corsou & Fein, 1986 a;Payne, Corsou, Fein & Berridge, 1986b;Nagy, 1990Nagy, , 1991. This is further supported by recent patch clamp investigations on Limulus ventral photoreceptors which have shown that there are three types of light-activated ionic channels which differ in their activation and deactivation kinetics and reversal potentials (Nagy & Stieve, 1990;Nagy, 1990). Robinson, Wood, Szuts, Fein, Hamm & Lisman (1990) recently reported that three different light-activated G-proteins exist in squid photoreceptors.…”

“…Most of the experiments were carried out on-line with an IBM-compatible personal computer (DATAG, FRG) and an A/D converter (Keithley, DAS 16; for details see Nagy, 1990). Some signals were replayed from magnetic tapes to the computer.…”