Retinoid cycling proteins redistribute in light‐/dark‐adapted octopus retinas

Abstract

In cephalopods, the complex rhodopsin-retinochrome system serves to regenerate metarhodopsin and metaretinochrome after illumination. In the dark, a soluble protein, retinal-binding protein (RALBP), shuttles 11-cis retinal released from metaretinochrome located in the photoreceptor inner segments to metarhodopsin present in the rhabdoms. While in the rhabdoms, RALBP delivers 11-cis retinal to regenerate rhodopsin and in turn binds the all-trans isomer released by metarhodopsin. RALBP then returns all-trans retinal to the inner segments to restore retinochrome. The conventional interpretation of retinoid cycling is contradicted by immunocytochemical studies showing that, in addition to rhodopsin, retinochrome is present in the rhabdomal compartment, making possible the direct exchange of chromophores between the metapigments with the potential exclusion of RALBP. By using immunofluorescence and laser scanning confocal microscopy, we have precisely located opsin, aporetinochrome, and RALBP in light-/dark-adapted octopus retinas. We found differences in the distribution of all three proteins throughout the retina. Most significantly, comparison of cross sections though light- and dark-adapted rhabdoms showed a dramatic shift in position of the proteins. In the dark, opsin and retinochrome colocalized at the base of the rhabdomal microvilli. In the light, opsin redistributed along the length of the microvillar membranes, and retinochrome retreated to a location that is perhaps extracellular. RALBP was present in the core cytoplasm of the photoreceptor outer segments in the dark, and RALBP moved to the periphery in the light. Because of the colocalization of opsin and retinochrome in the dark, we believe that the two metapigments participate directly in chromophore exchange. RALBP may serve to transport additional chromophore from the inner segments to the rhabdoms and may not be immediately involved in the exchange process.

Evolution of the visual cycle: the role of retinoid-binding proteins

“…This may be an oversimplification of a more complicated process involving interesting light-dependent changes in the distribution of the key proteins. In a detailed scanning confocal microscopy study, Robles et al (1995) showed that in addition to rhodopsin, retinochrome is present in the rhabdomal compartment. In the dark, opsin and retinochrome co-localize at the base of the rhabdomal microvilli.…”

Control ofDrosophilaRetinoid and Fatty Acid Binding Glycoprotein Expression by Retinoids and Retinoic Acid: Northern, Western and Immunocytochemical Analyses

“…An extracellular function would be consistent with the recent evidence suggesting that RFABG is related to insect lipophorins, secreted fatty acid carriers (Kutty et al, 1996). It is noteworthy that retinochrome in the octopus is also seen extracellularly in light adapted eyes (Robles et al, 1995).…”

“…Based on previous research in the blowfly (Schwemer, 1993) and honeybee (Smith and Goldsmith, 1991) which showed that vitamin A and photoisomerase are localized distally, the Semper cells, also distal, are prime candidates for involvement in retinoid metabolism. It was suggested that retinochrome and retinal binding protein may be expressed in supportive cells in the octopus (Robles et al, 1995).…”

Toward Developing Models to Study the Disease, Ecology, and Evolution of the Eye in Mollusca*

“…This is surprising, as molluscan systems have shown potential for study of basic visual processes, physiology of vision, development of the visual system, and evolution. For example, past work (Robles et al 1995, Torres et al 1997 has shown that cytoskeletal organization of photoreceptor cells is regulated by the state of light-and dark-adaptation in cephalopod eyes. It is known that some disease states in the human retina, such as macular degeneration, affect cytoskeletal development and organization (Eckmiller 2004).…”

“…Other work on the cephalopod retina has focused on light/dark adaptation-how the eye acclimates to changes in light levels in the environment (Young 1963a). Work on cephalopods has identified important sub-cellular alternations to the shape of photoreceptor cells and movements of cytoskeleton and photopigments within these cells in response to changes in light intensity (Robles et al 1995, Marinez et al 2000, Gray et al 2008. These studies have important application to understanding human eye disease.…”