Smooth endoplasmic reticulum and other agranular reticulum in frog retinal photoreceptors

Abstract

Frog retinal photoreceptors are favourable material for studying a number of unresolved issues concerning the interconnections, three-dimensional organization and functions of intracellular membrane systems in neurons. At least two distinct regions of smooth endoplasmic reticulum (SER) are present in these cells. One region, the subellipsoid SER, is located in rod cells at the base of the mitochondria-rich ellipsoid region, and is comprised of arrays of stacked tubules which exhibit frequent continuities with the rough endoplasmic reticulum (RER). The subellipsoid SER is also present throughout the ellipsoid region and at the apex of the inner segment. The second region of SER, the axonal SER, is comprised of agranular sacs and tubules present in the axons of rod cells, the perinuclear and Golgi regions of rod and cone cells and the synaptic terminals of rod and cone cells. There sacs and tubules exhibit continuities with cisternae of RER and with the nuclear envelope. Serial section analyses indicate that this SER can extend as a continuous networking along the entire length of the rod axons and throughout synaptic terminals. The axonal SER is distinct from the subellipsoid SER not only in location and morphology but also in its ability to bind divalent lead ions, a property it shares with synaptic vesicles, with agranular sacs at one face to the Golgi apparatus and with sacs extending from the Golgi apparatus toward the axons hillock. These latter sacs may serve in transport from the Golgi region to the axon. The axons SER in the axon, terminals, and the perinuculear and Golgi regions appear to be a source of synaptic vesicles as evidenced by this lead binding capacity and by the observation of vesicles, with the size (50-75 nm) and appearance of synaptic vesicles, budding from SER in direct continuity, with RER. The endoplasmic reticulum (ER) in synaptic terminals of frog photoreceptors is not continuous with endocytic structures found in the same region, such as blunt-ended tubules or anastomosing networks of tubules. Nor does the ER acquire exogenous horseradish peroxidase. These observations suggest that the ER does not play a direct role in membrane recycling in photoreceptors.