A concentration of fucosylated glycoconjugates at the base of cone outer segments: Quantitative electron microscope autoradiography

Anderson, Don H.; Fisher, Steven K.; Breding, David J.

doi:10.1016/0014-4835(86)90061-8

Cited by 11 publications

(6 citation statements)

References 38 publications

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“…In contrast, the COS region is formed entirely from repeated evaginations of the cone outer segment plasma membrane, resulting in a largely contiguous stack of parallel membrane sheets (Cohen, 1968;Laties et al, 1976). In COS these "disks"-or, more properly, "lamellae"-are in continuity with the plasma membrane and exposed to the extracellular environment of the outer retina (Young, 1967;Liebman and Entine, 1974;Anderson et al, 1986).…”

Section: A Structural Organizationmentioning

confidence: 99%

Photoreceptor renewal: A role for peripherin/rds

Boesze‐Battaglia¹,

Goldberg²

2002

International Review of Cytology

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Visual transduction begins with the detection of light within the photoreceptor cell layer of the retina. Within this layer, specialized cells, termed rods and cones, contain the proteins responsible for light capture and its transduction to nerve impulses. The phototransductive proteins reside within an outer segment region that is connected to an inner segment by a thin stalk rich in cytoskeletal elements. A unique property of the outer segments is the presence of an elaborate intracellular membrane system that holds the phototransduction proteins and provides the requisite lipid environment. The maintenance of normal physiological function requires that these postmitotic cells retain the unique structure of the outer segment regions-stacks of membrane saccules in the case of rods and a continuous infolding of membrane in the case of cones. Both photoreceptor rod and cone cells achieve this through a series of coordinated steps. As new membranous material is synthesized, transported, and incorporated into newly forming outer segment membranes, a compensatory shedding of older membranous material occurs, thereby maintaining the segment at a constant length. These processes are collectively referred to as ROS (rod outer segment) or COS (cone outer segment) renewal. We review the cellular and molecular events responsible for these renewal processes and present the recent but compelling evidence, drawn from molecular genetic, biochemical, and biophysical approaches, pointing to an essential role for a unique tetraspanning membrane protein, called peripherin/rds, in the processes of disk morphogenesis.

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Section: A Structural Organizationmentioning

confidence: 99%

Photoreceptor renewal: A role for peripherin/rds

Boesze‐Battaglia¹,

Goldberg²

2002

International Review of Cytology

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“…Homogeneous distribution of all the new molecules throughout the COS could not occur instantaneously. If all membrane entering COS flowed directly into BE, autoradiograms prepared after very short survival times should produce a linear gradient of labeling over COS (high over the BE, decreasing gradually to a low at the tip), which has not been reported (heavier labeling over the basal half of COS has recently been observed: Anderson et al, 1986).…”

Section: E M B R a N E Flow Routes Within C O Smentioning

confidence: 99%

“…Unfortunately, the morphologic findings of the present study do not specify the immediately preceding step, namely where the membrane that enters preexisting lamellae during DI formation comes from, which depends on how membrane flows within the rest of the COS. Now that mature COS are known to incorporate new membrane, it is somewhat puzzling that a diffuse autoradiographic labeling is observed over COS. It is widely assumed (O'Day and Young, 1979;Papermaster and Schneider, I982;Bok, 1985;Anderson et al, 1986;Roof, 1986) that new membrane is added to COS as BE, but that COS fail to display an autoradiographic band of label because protein molecules quickly diffuse throughout the fluid and topologically continuous COS membrane system. However, contradictory resuits have been reported regarding the rate of longitudinal diffusion within COS membranes (cf.…”

Section: E M B R a N E Flow Routes Within C O Smentioning

confidence: 99%

“…It is generally assumed (Young, 1976;Bok, 1985;Anderson et al, 1986;Roof, 1986) that COS exhibit no localLzation of autoradiographic labeling because molecules quickly diffuse throughout their fluid and topologically continuous membrane system, but the rate of longitudinal diffusion within COS membranes is not certain (of. Liebman andEntine, 1974, with Liebman, 1975).…”

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confidence: 99%

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Cone outer segment morphogenesis: taper change and distal invaginations.

Eckmiller

1987

The Journal of Cell Biology

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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...

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“…The radioactive “reaction bands” formed at the base of the OS are displaced progressively toward the retinal pigment epithelium (RPE) juxtaposed to the apex of the OS. In ~10 days, the distalmost OS discs appeared to be sloughed off in stacks and engulfed by RPE cells through phagocytosis (Young 1967, 1971; LaVail 1983; Anderson et al 1986). Thus, Young concluded that the mouse rod OS renews every ~10 days.…”

Section: Non-cell-autonomous Regulation Of Photoreceptor Cilium Removalmentioning

confidence: 99%

The Biology of Ciliary Dynamics

Hsu

Chuang

Sung

2017

Cold Spring Harb Perspect Biol

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The cilium is an evolutionally conserved apical membrane protrusion that senses and transduces diverse signals to regulate a wide range of cellular activities. The cilium is dynamic in length, structure, and protein composition. Dysregulation of ciliary dynamics has been linked with ciliopathies and other human diseases. The cilium undergoes cell-cycle-dependent assembly and disassembly, with ciliary resorption linked with G1-S transition and cell-fate choice. In the resting cell, the cilium remains sensitive to environmental cues for remodeling during tissue homeostasis and repair. Recent findings further reveal an interplay between the cilium and extracellular vesicles and identify bioactive cilium-derived vesicles, posing a previously unrecognized role of cilia for sending signals. The photoreceptor outer segment is a notable dynamic cilium. A recently discovered protein transport mechanism in photoreceptors maintains light-regulated homeostasis of ciliary length.

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A concentration of fucosylated glycoconjugates at the base of cone outer segments: Quantitative electron microscope autoradiography

Cited by 11 publications

References 38 publications

Photoreceptor renewal: A role for peripherin/rds

Photoreceptor renewal: A role for peripherin/rds

Cone outer segment morphogenesis: taper change and distal invaginations.

The Biology of Ciliary Dynamics

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