The Journal of General Physiology
Cell MicroControls
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Published online 11 April 2005 doi:10.1085/jgp.200509269
The Rockefeller University Press, 0022-1295 $8.00
JGP, Volume 125, Number 5, 455-464
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On the Gating Mechanisms of the Light-dependent Conductance in Pecten Hyperpolarizing Photoreceptors

Does Light Remove Inactivation in Voltage-dependent K Channels?



Maria del Pilar Gomeza,b and Enrico Nasia,b

a Department of Physiology and Biophysics, Boston University School of Medicine, Boston, MA 02118
b Marine Biological Laboratory, Woods Hole, MA 02543

Correspondence to Maria del Pilar Gomez: mpgomez{at}bu.edu

The hyperpolarizing receptor potential of ciliary photoreceptors of scallop and other mollusks is mediated by a cGMP-activated K conductance; these cells also express a transient potassium current triggered by depolarization. During steady illumination, the outward currents elicited by voltage steps lose their decay kinetics. One interesting conjecture that has been proposed is that the currents triggered by light and by depolarization are mediated by the same population of channels, and that illumination evokes the receptor potential by removing their steady-state inactivation. Exploiting the information that has become available on the phototransduction cascade of ciliary photoreceptors, we demonstrated that the same downstream signaling elements are implicated in the modulation of voltage-elicited currents: direct chemical stimulation both at the level of the G protein and of the final messenger that controls the light-dependent channels (cGMP) also attenuate the falling phase of the voltage-activated current. Application of a protein kinase G antagonist was ineffective, suggesting that a cGMP-initiated phosphorylation step is not implicated. To ascertain the commonality of ionic pathways we used pharmacological blockers. Although millimolar 4-aminopyridine (4-AP) suppressed both currents, at micromolar concentrations only the photocurrent was blocked. Conversely, barium completely and reversibly antagonized the transient voltage-activated current with no detectable effect on the light-evoked current. These results rule out that the same ionic pores mediate both currents; the mechanism of light modulation of the depolarization-evoked K current was elucidated as a time-dependent increase in the light-sensitive conductance that is superimposed on the inactivating K current.

Key Words: photoreceptors • CNG channel • potassium ion channels • gating, ion channels • blockers, potassium channel


Abbreviations used in this paper: 4-AP, 4-aminopyridine; ASW, artificial sea water; 8-Br-cGMP, 8-bromo cyclic guanosine monophosphate; CNGC, cyclic nucleotide–gated channel; GTP-{gamma}-S, guanosine 5'-O-[3-thiotriphosphate].


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