3-DIMENSIONAL MEMBRANE CRYSTALS IN AMPHIBIAN CONE OUTER SEGMENTS .1. LIGHT-DEPENDENT CRYSTAL-FORMATION IN FROG RETINAS

When frog retinas are exposed to light, a series of three-dimensional crystals develop within the outer segment disk system of cones but not rods. The crystals involve components that span cytoplasmic, disk mem brane, and intradisk domains of the outer segment. The crystalline mem brane domains are directly continuous with adjacent, noncrystalline la mellar regions. In axial extent, the crystals may involve as few as 1 or 2 disks or as many as 30 disks. However, within each disk, only one crystalline domain typically is observed. Within a crystal, the membr anes are more planar in shape and more uniform in axial spacing then a djacent, noncrystalline lamellar regions. Furthermore, as crystalline domains expand laterally, one observes increased axial spacing disorde r in noncrystalline lamellar regions, along with an increase in the wi dth of the intradisk compartment. Thus, crystals appear to grow latera lly by depleting adjacent lamellar regions of components that influenc e the normal membrane pair separation and axial spacing of cone outer segment disks. In isolated retinas, the crystalline domains appear to be randomly distributed along the length of the outer segment and show no preference for association with either the closed or open margins of the disk. After 45 min in the light, the crystals occupy similar to 10% of the cone outer segment volume. On the basis of comparative str uctural, biochemical, and physiological data, cone outer segment cryst als may represent a cocrystal between bleached, phosphorylated opsin ( providing transmembrane and intradisk elements) and the cytoplasmic pr otein, arrestin (providing trans-cytoplasmic elements). Thus, crystal formation may provide one mechanism of light adaptation within the con e outer segment. The spontaneous, bleaching-induced formation of these crystals in situ offers the possibility that cocrystals of cone outer segment components can be prepared in vitro for higher resolution cry stallographic analyses. (C) 1994 Academic Press, Inc.