Protein kinase C is required for light adaptation in Drosophila photoreceptors

Abstract

Protein kinase C (PKC) is a key enzyme for many cellular processes but its physiological roles are poorly understood. An excellent opportunity to investigate the function of PKC has been provided by the identification of an eye-specific PKC in Drosophila and a null PKC mutant, inaCP209 (refs 5,6). Bright conditioning lights delivered to inaC photoreceptors lead to an abnormal loss of sensitivity in whole cell recordings from dissociated ommatidia; this has been interpreted as 'hyper-adaptation' and PKC's role has been suggested to be distinct from light adaptation. A presumably related finding is that during intense light, the response of inaC declines to baseline. Invertebrate photoreceptors use the phosphoinositide signalling cascade, responding to single photons with so-called quantum bumps which sum to form the macroscopic response to light. Light adaptation allows photoreceptors to adjust their sensitivity over the enormous range of ambient intensities. Although the molecular mechanism of light adaptation remains obscure, it is a negative-feedback process mediated by a rise in cytosolic calcium and a decrease in bump size. We now show that under physiological conditions light adaptation is severely reduced in inaC, suggesting that eye-specific PKC, itself activated by a rise in cytosolic calcium and diacylglycerol, is required for adaptation. Furthermore, we show that in the absence of PKC individual bumps fail to terminate normally, an effect that can account for the pleiotropic manifestations of the inaC phenotype.

Protein Kinase C Activators Inhibit the Visual Cascade inLimulusVentral Photoreceptors at an Early Stage

“…Light adaptation is usually accompanied by a reduced response latency and duration (Fuortes and Hodgkin, 1964). In Drosophila photoreceptors, the presence of an eye-specific PKC appears to be necessary for light adaptation (Hardie et al, 1993). Our pharmacological results do not support the concept that PKC mediates light adaptation in Limulus ventral photoreceptors.…”

“…In the Drosophila inaC mutant the latter phase is missing; instead the response to sustained bright light decays slowly to baseline (Hardie et al, 1993). Ventral photoreceptors that were incubated overnight in 25 M Gö 6976 displayed receptor potentials in response to prolonged bright light (log 10 Ϫ1) that still showed a rapid transition from a transient phase to a sustained steady-state phase (Fig.…”

“…Application of PKC activators to photoreceptors of the clam Lima evokes an inward current that shares some of the characteristics of the light-induced current (Gomez and Nasi, 1998). Studies of the Drosophila mutant inactivationno-afterpotential C (inaC), which lacks an eye-specific PKC (Smith et al, 1991), have indicated a role for PKC in adaptation and response deactivation (Smith et al, 1991;Hardie et al, 1993). In the horseshoe crab Limulus polyphemus, PKC activators induce rhabdom shedding when injected into the compound lateral eye before dawn (Jinks et al, 1996).…”

Systems analysis of the single photon response in invertebrate photoreceptors

“…The molecular details of the positive feedback are still unknown. The negative feedback is mediated by several Ca 2ϩ -dependent processes, including phosphorylation of several proteins by Ca 2ϩ -calmodulin-dependent protein kinase (CamK) (2,14,15) and by eye-specific protein kinase C (ePKC) (16,17). …”

Calcium Transients in the Rhabdomeres of Dark- and Light-Adapted Fly Photoreceptor Cells

“…Ca 2ϩ has been proposed to act directly on the light-activated channels (Hardie and Minke, 1994;Hardie, 1995;Obukhov et al, 1998), or via binding to calmodulin that interacts with the light-activated channels (Phillips et al, 1992: Warr andKelly, 1996;Scott et al, 1997). Additionally, a Ca 2ϩ -regulated PKC (Huber et al, 1998) is crucial for Ca 2ϩ -dependent deactivation of the light response (Ranganathan et al, 1991) and light adaptation (Hardie et al, 1993). Other important molecules in the phototransduction cascade that have been suggested to be modulated by Ca 2ϩ or by Ca 2ϩ /calmodulin include neitherinactivation-nor-afterpotential C (Porter et al, 1993), inactivationnor-afterpotential D (Chevesich et al, 1997), and PLC (Running Deer et al, 1995).…”