The ciliary axoneme in photoreceptors from the retina of Xenopus laevis was examined by immunofluorescent staining of tubulin throughout the light/dark cycle. The immunofluorescent axoneme extended along only part of the length of rod outer segments but the entire length of cone outer segments. Both the cone axoneme and outer segment elongated during the day and shortened (presumably by shedding) during the night. Fragments of immunofluorescent axonemes were found within packets of outer segment material breaking off from cone tips. These findings show that the ciliary axoneme in the Xenopus retina is replaced during the renewal of outer segments in cones. No evidence has been found for renewal of the axoneme in rods, and thus the stability of the ciliary axoneme may differ in rod and cone photoreceptors.
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...
In many vertebrate retinas the outer segments of rod photoreceptors have multiple incisures, that is, there are numerous indentations in the highly curved membrane forming the edge of their disks and in the plasma membrane enclosing the entire stack of disks. Immunofluorescent localization of tubulin in amphibian photoreceptors yielded a novel series of thin, parallel, fluorescent lines in rod outer segments that extended their full length and coincided with their multiple incisures. Electron-microscopic examination of amphibian retinas revealed the structures responsible for this fluorescence: longitudinally oriented microtubules were associated with incisures at heights throughout rod outer segments. These microtubules were located between the disk rims and the overlying plasma membrane, in the small cytoplasmic compartment at the mouth of incisures; the microtubules and membranes were separated from each other by distances that were uniform, as though interconnected by filaments described in other studies. Thus, in amphibian rod outer segments the incisures mark the site of a cytoskeletal system containing longitudinal microtubules distinct from those of the ciliary axoneme, linked by filaments to the adjacent membranes. This cytoskeleton is expected to be important for the normal structure, function, and renewal of rod outer segments. In amphibian cone outer segments, which do not have incisures, the only anti-tubulin immunofluorescence and the only microtubules were at the axoneme. These findings may help elucidate the diverse properties of rods and cones in many vertebrate retinas and could prove relevant for human retinal degenerations.
scite is a Brooklyn-based organization that helps researchers better discover and understand research articles through Smart Citations–citations that display the context of the citation and describe whether the article provides supporting or contrasting evidence. scite is used by students and researchers from around the world and is funded in part by the National Science Foundation and the National Institute on Drug Abuse of the National Institutes of Health.
customersupport@researchsolutions.com
10624 S. Eastern Ave., Ste. A-614
Henderson, NV 89052, USA
Copyright © 2024 scite LLC. All rights reserved.
Made with 💙 for researchers
Part of the Research Solutions Family.