RETINOID CYCLING PROTEINS REDISTRIBUTE IN LIGHT-ADAPTED DARK-ADAPTED OCTOPUS RETINAS

In cephalopods, the complex rhodopsin-retinochrome system serves to re generate metarhodopsin and metaretinochrome after illumination. In the dark, a soluble protein, retinal-binding protein (RALBP), shuttles 11 -cis retinal released from metaretinechrome located in the photorecept or inner segments to metarhodopsin present in the rhabdoms. While in t he rhabdoms, RALBP delivers 11-cis retinal to regenerate rhodopsin and in turn binds the all-trans isomer released by metarhodopsin. RALBP t hen returns all-trans retinal to the inner segments to restore retinoc hrome. The conventional interpretation of retinoid cycling is contradi cted by immunocytochemical studies showing that, in addition to rhodop sin, retinochrome is present in the rhabdomal compartment, making poss ible the direct exchange of chromophores between the metapigments with the potential exclusion of RALBP. By using immunofluorescence and las er scanning confocal microscopy, we have precisely located opsin, apor etinochrome, and RALBP in light-/dark-adpated octopus retinas. We foun d differences in the distribution of all three proteins throughout the retina. Most significantly, comparison of cross sections though light - and dark-adpated 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 co re cytoplasm of the photoreceptor outer segments in the dark, and RALB P moved to the periphery in the light. Because of the colocalization o f opsin and retinochrome in the dark, we believe that the two metapigm ents participate directly in chromophore exchange. RALBP may serve to transport additional chromophore from the inner segments to the rhabdo ms and may not be immediately involved in the exchange process. (C) 19 95 Wiley-Liss, Inc.