Modulation of disk margin structure during renewal of cone outer segments in the vertebrate retina

Abstract

In the process of disk renewal in retinal cone outer segments (COSs), apical displacement of disks must be coupled to systematic reductions in disk area and perimeter in order to retain overall conical geometry. We have quantified these changes in disk area and perimeter segment lengths by morphometric analyses of cross sections of fully formed disks taken from basal to apical ends of COSs. Specifically excluded from these analyses are data arising from partial or incomplete disks within the COS, which do not conform to the conical geometry and which constitute a minor fraction of the COS disk population. Thus, our results address the long‐range pattern of structural changes affecting the major population of disks along the length of the COS. Our data indicate that decreases in total disk margin length associated with apical displacement of fully formed disks are due to decreases in the length of the margin opposite the cilium, i.e., the open margin segment. In contrast, the average length of the closed margin segment remains constant or increases slightly in the apical direction. The open margins of frog COS disks have recently been shown to possess a distinctive lattice of membrane‐associated components (Fetter and Corless: Invest. Ophthalmol. Vis. Sci. 28:646–657, '87). We have also examined COSs by the freeze‐fracture, deep‐etch technique for evidence of a mechanism whereby measured changes in open margin length may be accommodated while maintaining the overall organization of the open margin segments. In regions of membrane continuity between open margins and the COS plasma membrane, we have observed elevated ridges on the plasma membrane that (1) tend to lie parallel to the open margin segments, (2) have a similar axial spacing, (3) occasionally demonstrate interconnecting filaments similar to those of the open margin lattice, and (4) appear to have a particulate substructure. The mechanism proposed for reducing open margin length involves tangential displacement of the lateral edges of the open margin lattice to the adjacent plasma membrane. These shifted lattice domains initially give rise to the plasmalemmal ridges, which subsequently disassemble, and whose components become redistributed in the COS plasma membrane. These structural features of COS open margins suggest several revisions of our earlier model of disk morphogenesis (Corless and Fetter: J. Comp. Neurol. 257:24–38, '87), which was based on the margin structure of ROS disks alone. Eckmiller (J. Cell Biol. 105:2267–2277, '87) has recently proposed that partial disks observed within the COS represent sites of new disk formation. We evaluate the consequences of partial disk geometries for local remodelling of the open margin lattice and briefly outline an alternative interpretation of the partial COS disks that is fully consistent with available morphological data.