Translocation of G_qα Mediates Long-Term Adaptation inDrosophilaPhotoreceptors

Abstract

Light adaptation is a process that enables photoreceptor cells to operate over a wide range of light intensities without saturation. In invertebrate photoreceptors, fast adaptation is mediated by a Ca 2ϩ -dependent negative-feedback mechanism, which mainly affects the terminal steps of the cascade. Therefore, the response to each photon is smaller as light intensity increases, accommodating both high sensitivity and a vast dynamic range. Here, we describe a novel type of adaptation, which is mediated by one of the first steps in the phototransduction cascade affecting the sensitivity to absorbed photons. Long exposure to light resulted in dramatic reduction in the probability of each absorbed photon to elicit a response, whereas the size and shape of each single photon response did not change. To dissect the molecular mechanism underlying this form of adaptation we used a series of Drosophila mutants. Genetic dissection showed a pivotal role for light-induced translocation of G q ␣ between the signaling membrane and the cytosol. Biochemical studies revealed that the sensitivity to light depends on membrane G q ␣ concentration, which was modulated either by light or by mutations that impaired its targeting to the membrane. We conclude that long-term adaptation is mediated by the movement of G q ␣ from the signaling membrane to the cytosol, thereby reducing the probability of each photon to elicit a response. The slow time scale of this adaptation fits well with day/night light intensity changes, because there is no need to maintain single photon sensitivity during daytime.

Opsin1-2, Gqα and arrestin levels at Limulus rhabdoms are controlled by diurnal light and a circadian clock

“…This finding is consistent with results from other invertebrates showing that RhG q α levels are higher in the dark than in the light (Narita et al, 1999;Terakita et al, 1996;Kosloff et al, 2003;Frechter et al, 2007). A surprising finding is that dark-adaptive increases in RhG q α levels in Limulus require clock input.…”

“…Our study provides the first evidence that the dark-adaptive translocation of G q α to rhabdoms can be regulated by a circadian clock (Table1, Fig.8) and is mediated by cAMP-dependent processes (Fig.9). The clock-and cAMP-regulated increase in rhabdomeral G q α we describe in Limulus is clearly different from what has been described in Drosophila photoreceptors, where light-and dark-adapted changes in G q α at the rhabdoms are regulated entirely by light and darkness (Kosloff et al, 2003;Frechter et al, 2007). In Drosophila, the unconventional class III myosin NINAC (neither inactivation nor afterpotential C) is thought to play a role in G q α translocation from the cytoplasm to the rhabdom (Cronin et al, 2004;Lee and Montell, 2004).…”

“…Gain may be increased by increasing the number of G q α molecules activated by the photoisomerization of rhodopsin. A study from Drosophila provides direct evidence that rhabdomeral levels of G q α can contribute to the sensitivity of rhabdomeral photoreceptors (Frechter et al, 2007). As was described in the Introduction, the clock directly influences photoreceptor physiology by decreasing noise, increasing gain and increasing the duration of quantum bumps.…”

“…Because effects of the clock on RhG q α levels were only observed in eyes exposed to diurnal light (Table2), we conclude that the clock targets processes that increase RhG q α levels during dark adaptation. In both ciliated and rhabdomeral photoreceptors, the increase in RhG q α levels within the photosensitive compartment during dark adaptation is attributed to G q α translocation from the cytoplasm to photosensitive membranes (Kosloff et al, 2003;Frechter et al, 2007;Arshavsky and Burns, 2012). We were unable to directly assay G q α translocation in LE retinular cells (see Materials and methods); however, because the mechanism is broadly conserved in evolution,…”

Role of Ca2+/Calmodulin-dependent Protein Kinase II in Drosophila Photoreceptors

“…Light adaptation can be arbitrarily subdivided into long term and short term adaptation and may involve multiple regulations to reduce the efficiency of rhodopsin, G protein, or cation channels. For example, translocation of both G q (12,13) and TRPlike channels (14,15) out of the visual organelle may contribute to long term adaptation in Drosophila. In contrast, short term adaptation may be orchestrated by modulating the activity of signaling proteins by protein kinases.…”