Expression and light-dependent translocation of β-arrestin in the visual system of the terrestrial slug Limax valentianus

Abstract

Vertebrates, cephalopods, and arthropods are equipped with eyes having the highest spatiotemporal resolution among the animal phyla. In parallel, it is only the animals in these three phyla that have visual arrestin specialized for the termination of visual signaling triggered by opsin, in addition to ubiquitously expressed β-arrestin that serves in terminating general G protein-coupled receptor signaling. Indeed, visual arrestin in Drosophila and rodents translocates to the opsin-rich subcellular region in response to light to reduce the overall sensitivity of photoreceptors in an illuminated environment (i.e. light adaptation). We thus hypothesized that visual arrestin has taken over the role of β-arrestin in those animals having an eye with high spatiotemporal resolution during evolution. If this is true, it is expected that β-arrestin plays a role similar to visual arrestin in those animals having low resolution eyes. In the present study, we focused on the terrestrial mollusk Limax, a species related to cephalopods but has only β-arrestin, and generated antibody against β-arrestin. We found that β-arrestin is highly expressed in photosensory neurons, and translocates into the microvilli of the rhabdomere within 30 min in response to short wavelength light (400 nm), to which the eye of Limax exhibits a robust response. These observations suggest that β-arrestin functions in the visual system of those animals that do not have visual arrestin. We also exploited anti-β-arrestin antibody to visualize the optic nerve projecting to the brain, and demonstrated its usefulness for tracing a visual ascending pathway.