scholarly journals THE RENEWAL OF ROD AND CONE OUTER SEGMENTS IN THE RHESUS MONKEY

1971 ◽  
Vol 49 (2) ◽  
pp. 303-318 ◽  
Author(s):  
Richard W. Young

The renewal of retinal rod and cone outer segments has been studied by radioautography in rhesus monkeys examined 2 and 4 days after injection of leucine-3H. The cell outer segment consists of a stack of photosensitive, membranous discs. In both rods and cones some of the newly formed (radioactive) protein became distributed throughout the outer segment. Furthermore, in rods (but not in cones), there was a transverse band of concentrated radioactive protein slightly above the outer segment base 2 days after injection. This was due to the formation of new discs, into which labeled protein had been incorporated. At 4 days, these radioactive discs were located farther from the outer segment base. Repeated assembly of new discs had displaced them away from the basal assembly site and along the outer segment. Measurements of the displacement rate indicated that each retinal rod produces 80–90 discs per day, and that the entire complement of outer segment discs is replaced every 9–13 days. To compensate for the continual formation of new discs, groups of old discs are intermittently shed from the apical end of the cell and phagocytized by the pigment epithelium. Each pigment epithelial cell engulfs and destroys about 2000–4000 rod outer segment discs daily. The similarity between visual cells in the rhesus monkey and those in man suggests that the same renewal processes occur in the human retina.

1978 ◽  
Vol 76 (3) ◽  
pp. 593-604 ◽  
Author(s):  
W T O'Day ◽  
R W Young

Goldfish were placed on a daily light cycle of 12 h light and 12 h darkness for 18 days or longer. The visual cells and pigment epithelium of the retina were then examined by microscopy at many intervals throughout the cycle. Goldfish rods and cones follow a rhythmic pattern in eliminating packets of photosensitive membranes from their outer segments. Rods shed membranes early in the light period. The detached membranes are ingested by pigment epithelial cells or by ameboid phagocytes, which degrade them during the remainder of the light period. Cones discard membranes from the ends of their outer segments early in the dark period. During the next several hours, this debris is digested by the pigment epithelium or by ameboid phagocytes. Thus, the disposal phase of the outer-segment renewal process is similar in rods and cones, but is displaced in time by about 12 h. There is evidence that this daily rhythm of membrane disposal in rods and cones is a general property of vertebrate visual cells.


Physiology ◽  
2010 ◽  
Vol 25 (1) ◽  
pp. 8-15 ◽  
Author(s):  
Brian M. Kevany ◽  
Krzysztof Palczewski

Photoreceptor cells maintain a roughly constant length by continuously generating new outer segments from their base while simultaneously releasing mature outer segments engulfed by the retinal pigment epithelium (RPE). Thus postmitotic RPE cells phagocytose an immense amount of material over a lifetime, disposing of photoreceptor cell waste while retaining useful content. This review focuses on current knowledge of outer segment phagocytosis, discussing the steps involved along with their critical participants as well as how various perturbations in outer segment (OS) disposal can lead to retinopathies.


1974 ◽  
Vol 62 (2) ◽  
pp. 378-389 ◽  
Author(s):  
Carol Bibb ◽  
Richard W. Young

The renewal of glycerol in the visual cells and pigment epithelium of the frog retina was studied by autoradiographic analysis of animals injected with [2-3H]glycerol. Assay of chloroform:methanol extracts showed that the labeled precursor was used mainly in lipid synthesis, although there was also some utilization in the formation of protein. Radioactive glycerol was initially concentrated in the myoid portion of rods and cones, indicating that this is the site of phospholipid synthesis in visual cells. The glycogen bodies (paraboloids) of accessory cones were also heavily labeled, suggesting the diversion of some glycerol into glycogenic pathways. In the pigment epithelium, only the oil droplets became significantly radioactive. The outer plexiform layer (which contains the visual cell synaptic bodies) and the cone oil droplets gradually accumulated considerable amounts of labeled material. Within 1–4 h, labeled molecules began to appear in the visual cell outer segments, evidently having been transported there from the myoid portion of the inner segment. Most of these were phospholipid molecules which became distributed throughout the outer segments, presumably replacing comparable constituents in existing membranes. In rods only, there was also an aggregation of labeled material at the base of the outer segment due to membrane biogenesis. These highly radioactive membranes, containing labeled molecules of lipid and protein, were subsequently displaced along the rod outer segments due to repeated membrane assembly at the base. The distribution of radioactivity supported the conclusion that membrane renewal by molecular replacement is more rapid for lipid than it is for protein.


1974 ◽  
Vol 61 (2) ◽  
pp. 327-343 ◽  
Author(s):  
Carol Bibb ◽  
Richard W. Young

The renewal of fatty acids in the visual cells and pigment epithelium of the frog retina was studied by autoradiographic analysis of animals injected with tritiated palmitic, stearic, or arachidonic acids. Most of the radioactive material could be extracted from the retina with chloroform-methanol, indicating that the fatty acids had been esterified in lipids. Analysis of the extracts, after injection of [3H]palmitic acid, revealed that the radioactivity was predominantly in phospholipid. Palmitic acid was initially concentrated in the pigment epithelium, particularly in oil droplets which are storage sites for vitamin A esterified with fatty acid. The cytoplasm, but not the nucleus of these cells, was also heavily labeled. Radioactive fatty acid was bound immediately to the visual cell outer segment membranes, including detached rod membranes which had been phagocytized by the pigment epithelium. This is believed to be due to fatty acid exchange in phospholipid molecules already situated in the membranes. Gradually, the concentration of radioactive material in the visual cell outer segment membranes increased, apparently as a result of the addition of new phospholipid molecules, possibly augmented by the transfer from the pigment epithelium of esterified vitamin A. Injected fatty acid became particularly concentrated in new membranes which are continually assembled at the base of rod outer segments. This localized concentration was short-lived, apparently due to the rapid renewal of fatty acid. The results support the conclusion that rods renew the lipids of their outer segments by membrane replacement, whereas both rods and cones renew the membrane lipids by molecular replacement, including fatty acid exchange and replacement of phospholipid molecules in existing membranes.


1972 ◽  
Vol 5 (3) ◽  
pp. 349-393 ◽  
Author(s):  
Stanley D. Carlson

Visual pigments are embedded in the disc membranes of the outer segments of vertebrate rods and cones and in the microvilli of invertebrate visual cells. The pigment molecule in both is a most fascinating aggregate of known (the ubiquitous II-cis isomer of vitamin A1 or A2-aldehyde = retinal1 or 2; Hubbard & Wald, 1952) covalently bonded to the unknown (a protein termed opsin) (Anderson, Hoffman & Hall, 1971). This conjugated molecule is called rhodopsin or dehydrorhodopsin (porphryopsin) when the prosthetic portion is retinall or 2 respectively. So sensitive is this sterically hindered, bent and twisted molecule to light that absorption of one photon can initiate its isomerization to the all trans form. This conformational change is but one (but the best known) of the factors leading to receptor membrane changes ushering in the visual impulse.


1978 ◽  
Vol 77 (1) ◽  
pp. 196-210 ◽  
Author(s):  
DS Papermaster ◽  
BG Schneider ◽  
MA Zorn ◽  
JP Kraehenbuhl

Adult vertebrate retinal cells (rod and cones) continuously synthesize membrane proteins and transport them to the organelle specialized for photon capture, the outer segment. The cell structures involved in the synthesis of opsin have been identified by means of immunocytochemistry at the electron microscope level. Two indirect detection systems were used: (a) rabbit antibodies to frog opsin were localized with ferritin conjugated F(ab')2 of sheep antibodies to rabbit F(ab')2 and (b) sheep antibodies to cattle opsin were coupled to biotin and visualized by means of avidin-ferritin conjugates (AvF). The reagents were applied directly to the surface of thin sections of frog retinal tissues embedded in glutaraldehyde cross-linked bovine serum albumin (BSA). Specific binding of anti-opsin antibodies indicates that opsin is localized in the disks of rod outer segments (ROS), as expected, and in the Golgi zone of the rod cell inner segments. In addition, we observed quantitatively different labeling patterns of outer segments of rods and cones with each of the sera employed. These reactions may indicate immunological homology of rod and cone photopigments. Because these quantitiative variations of labeling density extend along the entire length of the outer segment, they also serve to identify the cell which has shed its disks into adjacent pigment ipithelial cell phagosomes.


Photoreceptors of anchovies Anchoa mitchilli and A. hepsetus consist of normal rods and two unusual kinds of cones. The latter lie in single vertical rows, and the rods lie between them. Both participate in photomechanical movements, and movement of the cones is closely coordinated with that of pigment cell processes. There are long cones having a cuneate outer segment and short cones having a bilobed outer segment. Long and short (bifid) cones alternate within a row and are staggered between adjacent rows. Both kinds possess calycal processes; long cones have a lateral sac or accessory outer segment. The long and short cones are associated to form a structure called a cone unit, which consists of the outer segment and ellipsoid of a long cone joined to two outer segment lobes of two adjacent short cones. The lobes of the latter are partly enclosed by the ellipsoid of the long cone. A cone row consists of a row of cone units isolated from each other by processes of the pigment epithelium containing stacks of guanine crystals which form a tapetum. Dorsal and ventral faces of inner segments have contact zones characterized by subsurface cisternae. Lamellae in the cone outer segments are arranged longitudinally with respect to the cell axis and short and long cone lamellae are perpendicular to each other; lamellae of the rods are transverse. Long cone lamellae are perpendicular to the cone row, and in the central retina are almost horizontal to the long axis of the body. Some vesicular/tubular structures also occur in the cone outer segments. Outer and inner segments of cones are joined by a broad connecting structure containing a stalk and root portion corresponding to a modified and reduced cilium shaft and centriole, respectively. The rod has a typical connecting stalk. Mitochondria of cone ellipsoids have expanded perimitochondrial spaces between outer and inner membranes. The organization of the anchovy cones is compared with that of other vertebrates. It is suggested that the cone unit may be a two channel analyser for the detection of plane polarized light and function in conjunction with the overlying reflector of regularly arranged platelets.


2018 ◽  
Author(s):  
Tylor R. Lewis ◽  
Sean R. Kundinger ◽  
Brian A. Link ◽  
Christine Insinna ◽  
Joseph C. Besharse

AbstractBackgroundKIF17, a kinesin-2 motor that functions in intraflagellar transport, can regulate the onset of photoreceptor outer segment development. However, the function of KIF17 in a mature photoreceptor remains unclear. Additionally, the ciliary localization of KIF17 is regulated by a C-terminal consensus sequence (KRKK) that is immediately adjacent to a conserved residue (mouse S1029/zebrafish S815) previously shown to be phosphorylated by CaMKII. Yet, whether this phosphorylation can regulate the localization, and thus function, of KIF17 in ciliary photoreceptors remains unknown.ResultsUsing transgenic expression in both mammalian cells and zebrafish photoreceptors, we show that phospho-mimetic KIF17 has enhanced localization to cilia. Importantly, expression of phospho-mimetic KIF17 is associated with greatly enhanced turnover of the photoreceptor outer segment through disc shedding in a cell-autonomous manner, while genetic mutants of kif17 in zebrafish and mice have diminished disc shedding. Lastly, cone expression of constitutively active tCaMKII leads to a kif17-dependent increase in disc shedding.ConclusionsTaken together, our data support a model in which phosphorylation of KIF17 promotes its ciliary localization. In cone photoreceptor outer segments, this promotes disc shedding, a process essential for photoreceptor maintenance and homeostasis. While disc shedding has been predominantly studied in the context of the mechanisms underlying phagocytosis of outer segments by the retinal pigment epithelium, this work implicates photoreceptor-derived signaling in the underlying mechanisms of disc shedding.


1978 ◽  
Vol 201 (1143) ◽  
pp. 169-177 ◽  

Histological examination of the retinae of Xenopus tadpoles undergoing the extensive transformations of metamorphic climax revealed a progressive and dramatic decrease in the length of rod outer segments (r. o. s.) (by 1.22 µm/day), which was reversed after the completion of metamorphosis, when r. o. s. grew longer (by 1.11 µm/day). The rate of r. o. s. disk addition during these two periods was determined by examining the incorporation of [ 3 H]-leucine by light microscopic autoradiography. The band of labelled protein in r. o. s. was displaced sclerally at a rate of 1.70 µm/day during the first half of metamorphic climax, and of 1.56 µm/day in young juveniles during the second month after metamorphosis. The similarity of the rate of band displacement at these times indicates that the changes in r. o. s. length associated with metamorphosis result from major changes in the rate of disk shedding and/or phagocytosis, which was about 2.92 µm/day pre-metamorphically and 0.45 µm/day post-metamorphically. E. m. observation at these stages and during the final stages of metamorphic climax revealed no significant alterations in the cellular organization or ultrastructure of rods or pigment epithelium, even though some r. o. s. were only 3 µm long. This large change in r. o. s. length undoubtedly influences the animal’s scotopic sensitivity and the relative mesopic activity of its rods and cones, and may have important effects on the animal’s visual physiology.


1975 ◽  
Vol 64 (1) ◽  
pp. 235-241 ◽  
Author(s):  
W T Mason ◽  
K J Bighouse

The developing chick retina from stages 39-45 has been examined by biochemical and electron microscope techniques. The levels of rhodopsin contained in the maturing chick retina were evaluated by detergent extraction and correlated with rod outer segment formation. It was found that the appearance of rhodopsin in significant levels preceded outer segment formation by at least 2 days, thus implying that rhodopsin is synthesized in the receptor cell inner segment and translocated to the outer limb when disk membrane biogenesis occurs. The level of rhodopsin continues to rise as the rod outer segment develops. Development of both rods and cones originates and proceeds most rapidly in the fundus or central region and proceeds toward the periphery. In general, rod outer segments were noted to develop far more rapidly than cone outer segments.


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