Structural features of the terminal loop region of frog retinal rod outer segment disk membranes: III. Implications of the terminal loop complex for disk morphogenesis, membrane fusion, and cell surface interactions.

The perimeter of rod outer segment (ROS) disks displays a two-dimensional lattice of components referred to as the terminal loop complex (Corless, Fetter, Zampighi, Costello, and Wall-Buford: J. Comp. Neurol. 257:9-23, '87b). We take the view that this pattern of structural organization reflects the mechanism(s) whereby the disk perimeter is defined and constructed. Herein we develop and partially evaluate a generalized template mechanism of disk perimeter development, to account for the structure and the axial alignment of both marginal and incisural domains. Components of the terminal loop complex are conceived as the morphogens that determine the location and guide the differentiation of the disk perimeter. Briefly, we postulate that transmembranous components of the terminal loop complex are present within the reflection of plasmalemma that forms the base of the rod outer segment. These components interact with the cytoplasmic template provided by the perimeter lattice present along the lower surface of the most basal disk, thereby propagating the lattice and creating an extracellular template. The latter is then available to interact with corresponding elements distributed within the apical surface of the adjacent disk precursor evagination. The progressive interaction and alignment of these extracellular domains form the scaffolding that guides the restructuring of the plasmalemma, to form the mature disk margin topology. Successive repetitions of this process are seen to produce an axial stacking of disks whose perimeters are aligned and ensheathed by a two-dimensional net.