Patterns of interdisk connections within the lamellar domains of retinal rod outer segment disks: Observations relevant to the axial propagation of incisures

Abstract

In rod outer segments (ROSs) of the Congo eel salamander (Amphiuma), we have observed a system of cytoplasmic filaments that interconnect the lamellar domains of adjacent disks. In longitudinal sections, these filaments occur in pairs, spaced 18-20 nm apart. Each filament is 9-11 nm in length, and perpendicular to the disk membrane. Such filament pairs display extended axial alignment through the lamellar domains of successive disks, indicating the involvement of trans-membranous elements. In cross-sectional views, these filaments appear as a row of paired, punctate densities with a periodic spacing of 14-16 nm. Such views indicate that these filaments are organized on a two-dimensional crystalline lattice, oriented perpendicular to the disk lamellae. The linear interdisk densities of the terminal loop complex appear to be identical to these cytoplasmic filaments: both are equal in length, and both are organized as two-dimensional assemblies with equivalent orientations and lattice parameters. These shared features suggest a common subset of molecular components and lattice determinants. Where the paired filament assemblies intersect the disks, one observes a characteristic dilatation of the intradisk space. In these regions, the disk is 3-6 nm wider than adjacent lamellar regions, and tends to approximate the width of the terminal loop expansion along the disk perimeter. Within such dilatations, we have not been able to demonstrate crescentic densities corresponding to those found within the terminal loop region. Paired filament arrays are not randomly located within the lamellar domains, but lie parallel to the local disk perimeter. Both single and multiple arrays are commonly observed. Single arrays are recessed about 80 nm from the disk edge. When more than one array is present, the additional arrays lie parallel to the first and are spaced at intervals of about 70 nm. Thus, in three dimensions, the multiple arrays appear as regularly spaced sheets of filaments, parallel to the local disk perimeter and perpendicular to the lamellar domains. The characteristic interval between such filament arrays suggests the presence of 'spacer' molecules that organize the two-dimensional filament lattices in the third dimension. Such a spacing mechanism may also account for the minimum width observed for disk lobule segments defined by extended parallel incisures. The potential role of paired filament arrays in the axial propagation of incisures is discussed.