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.

Serca isoform expression in the mammalian retina

“…At higher confocal gains, SERCA2 immunofluorescence was observed in mouse photoreceptor inner segments (ISs; arrowheads in Fig. 1B), consistent with SERCA2 expression in the IS region that contains large amounts of ER cisternae (Mercurio and Holtzman, 1982). The most pronounced SERCA2 signal in mouse was detected in cell bodies of presumed amacrine cells lining the proximal end of the INL and in cells localized to the ganglion cell layer (arrows in Fig.…”

“…In neurons, the ER consists of a network of cisternae extending throughout the cell, from the synaptic terminal to dendritic branches (Mercurio and Holtzman, 1982;Verkhratsky, 2005). Ca 2+ release from and sequestration into neuronal ER can exert both local and global control over Ca 2+ -dependent cytoplasmic events, allowing it to regulate many cellular functions, including gene expression, protein synthesis, synaptic transmission and apoptosis (reviewed in Meldolesi and Pozzan, 2002;Berridge et al, 2003;Breckenridge et al, 2003;Verkhratsky, 2005).…”

Calcium regulation in photoreceptors

“…ER and its specializations are found in all parts of the inner segment, including the soma and the synaptic terminal (149)(150). Ca 2+ is sequestered into both rough and smooth ER (151)(152)(153).…”

“…The density of the ER structures is highest in the subellipsoid space (the myoid), from which other organelles are effectively excluded. The myoid ER is involved in synthesis of OS and IS proteins (149). It is thought to be continuous with the smooth ER which has access into synaptic terminals (149,151).…”

Kinetics of Synaptic Transmission at Ribbon Synapses of Rods and Cones

“…Intracellular calcium is stored and released from the endoplasmic reticulum. Ultrastructural studies revealed smooth endoplasmic reticulum in the inner segments and synaptic terminals of photoreceptors [154] capable of accumulating calcium ions [155]. There are two principal mechanisms of calcium release from internal stores: CICR mediated by ryanodine receptors and release mediated by receptors for the second messenger, IP3 [156].…”