Cone outer segment morphogenesis: taper change and distal invaginations.

Abstract

Abstract. Because cone outer segments (COS) are now known to be continually renewed, I reexamined COS morphogenesis in retinas of Xenopus tadpoles (prepared by standard histologic techniques and viewed by light and electron microscopy) to clarify how COS incorporate new membrane. I observed that developing COS underwent an unexpected shape change: they were always conical, but their taper (width divided by length) continually decreased. Ultrastructural examination revealed that many of the membrane foldings within distal COS were partial or incomplete, not extending across the full COS width but ending at variable distances from the ciliary side. Because these partial folds represented infoldings of the plasma membrane of an existing lamella, and they occurred at all COS levels except the base, I have termed them distal invaginations (DI). The completion of each DI increased COS length by one lamella but caused no noticeable change in local COS width; thus the formation of many DI throughout the distal COS presumably resulted in the observed decrease in overall COS taper. Based on these findings, I suggest that DI indicate growing membrane fronts and may represent sites where newly synthesized membrane is incorporated into COS. Because DI occur in developing and adult COS of various vertebrate species, I propose that DI formation plays an important role in the generation of COS taper during development and the remodeling of COS taper in mature cones after tip shedding.THOtJGI-I it is now accepted that the light-sensitive outer segments (OS) ~ of both vertebrate rods and cones are regularly renewed (Anderson et al., 1978;Young, 1978;Bok, 1985;Roof, 1986), numerous aspects of cone outer segment (COS) renewal remain problematical. I have reexamined the morphogenesis of COS to clarify how new membrane is incorporated into COS.Rod outer segment (ROS) membranes are renewed in a very orderly manner, as first revealed by autoradiography (Young, 1967): radioactive protein molecules become trapped in new membranous disks generated at the OS base, producing an autoradiographic band of label; the unchanged band is displaced sclerally as additional disks form below, and finally discarded from the OS tip and phagocytized by the pigment epithelium (Young and Bok, 1969). This pattern of membrane renewal is consistent with the ultrastructural morphology and cylindrical shape of mature ROS (Young, 1976;Steinberg et al., 1980;Bok, 1985). It is thus clear how new membrane is incorporated into ROS: each membrane entering via the connecting cilium becomes distributed into successive new membrane folds that evaginate from the cilium at the OS base, these evaginations expand to the full OS width and are displaced away from the base, then lose their 1. Abbreviations used in thispaper: BE, basal evagination; COS, cone outer segment; DI, distal invagination; LM, light microscopy; OS, outer segment; ROS, rod outer segment.connections and become isolated into separate disks surrounded by the plasma membrane.COS differ from ROS in structural...

Early development of the nervous system of the eutherian <i>Tupaia belangeri</i>

“…In this model, continuity between the interior of the disks and the extracellular space, as seen in mature cones, results from the secondary fusion between the disks and the cell membrane of the outer segment. In contrast, disks in the developing cone outer segments of Tupaia belangeri develop between the apposed membranes of two neighboring "basal evaginations" (Steinberg et al, 1980;Eckmiller 1987Eckmiller , 1990 rich in cytoplasm, which protrude from the position of the eccentrically localized ciliary axoneme to the opposite side ( Fig. 3b, c).…”

Rod disc renewal occurs by evagination of the ciliary plasma membrane that makes cadherin-based contacts with the inner segment

“…The cylindrical outer segment (OS) contains ∼1,000 stacked discontinuous membranous discs packed with the light-sensitive pigment rhodopsin. This contrasts with the cone OS, which consists of a series of evaginations of the plasma membrane that remain exposed to the extracellular space (1). OS constituents are synthesized in the inner segment (IS) and then transported to the OS via a nonmotile cilium (connecting cilium) that resembles the transition zone of the primary cilium.…”

Electromagnetic Modeling of Retinal Photoreceptors

“…This uniform helical antenna has the geometrical parameters of the turn number of 10, the pitch angle of 12. The diameters of the rod outer segment (ROS) and cone outer segment (COS) vary between 1-3 microns [1,13,15,27,28]. The spacing between each fold is between 24-30 nm [36,37].…”

“…Although there are experimental evidences of genetic differences between each visual pigment, the effects of size, shape [13,14] and physical structure of the cones shouldn't be neglected for the spectral discrimination mechanism. Sheppard [1] suggests that the spectral selectivity of an individual cone might be substantially affected by its physical characteristics (size, index of refraction, etc.)…”