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The Journal of Neuroscience, November 15, 1998, 18(22):9153-9162

A Ca²⁺/Calmodulin-Dependent Protein Kinase Modulates Drosophila Photoreceptor K⁺ Currents: A Role in Shaping the Photoreceptor Potential

Asher Peretz^{1, 2}, Ilane Abitbol¹, Alexander Sobko¹, Chun-Fang Wu², and Bernard Attali¹

¹ Neurobiology Department, Weizmann Institute of Science, Rehovot 76100, Israel, and ² Department of Biological Sciences, University of Iowa, Iowa City, Iowa 52442

Light activation of Drosophila photoreceptors leads to the generation of a depolarizing receptor potential via opening of transient receptor potential and transient receptor potential-like cationic channels. Counteracting the light-activated depolarizing current are two voltage-gated K⁺ conductances, I_A and I_K, that are expressed in these sensory neurons. Here we show that Drosophila photoreceptors I_A and I_K are regulated by calcium-calmodulin (Ca²⁺/calmodulin) via a Ca²⁺/calmodulin-dependent protein kinase (CaM kinase), with I_K being far more sensitive than I_A. Inhibition of Ca²⁺/calmodulin by N-(6 aminohexyl)-5-chloro-1-naphthalenesulfonamide or trifluoperazine markedly reduced the K⁺ current amplitudes. Likewise, inhibition of CaM kinases by KN-93 potently depressed I_K and accelerated its C-type inactivation kinetics. The effect of KN-93 was specific because its structurally related but functionally inactive analog KN-92 was totally ineffective. In Drosophila photoreceptor mutant Sh^KS133, which allows isolation of I_K, we demonstrate by current-clamp recording that inhibition of I_K by quinidine or tetraethylammonium increased the amplitude of the photoreceptor potential, depressed light adaptation, and slowed down the termination of the light response. Similar results were obtained when CaM kinases were blocked by KN-93. These findings place photoreceptor K⁺ channels as an additional target for Ca²⁺/calmodulin and suggest that I_K is well suited to act in concert with other components of the signaling machinery to sharpen light response termination and fine tune photoreceptor sensitivity during light adaptation.

Key words: potassium channels; phototransduction; calmodulin; light adaptation; photoreceptor; CaM kinase; Drosophila

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Copyright © 1998 Society for Neuroscience  0270-6474/98/18229153-10$05.00/0

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