scholarly journals Rhythmic daily shedding of outer-segment membranes by visual cells in the goldfish.

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.

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.


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 187 (1089) ◽  
pp. 461-478 ◽  

The association between cone outer segments and pigment epithelial cells in the tapetal region of the cat’s retina was studied by both transmission and scanning electron microscopy. Although the cone outer segments do not reach the perikaryal surface of the pigment epithelium they are still closely associated with the apical processes of the pigment epithelium. These processes are leaf-like in shape and ensheath the cone outer segments in a unique way. Each sheath is formed usually by four processes. The base of each process is a broad cytoplasmic sheet which wraps in a spiral of one and a half to two turns in the space above the outer segment’s tip. The processes of each sheath wrap concentrically in this space and form a tunnel whose wall is at least six laminae thick. Where the outer segment is inserted into the sheath, the thickness of the sheath diminishes to three or four laminae. This is because each process gradually narrows in width and, therefore, makes fewer turns. Since the processes continue to narrow as they extend along the outer segment the completeness of ensheathment gradually diminishes from the tip to the base of the outer segment. The processes finally narrow to pointed tips and some processes of each sheath reach the base of the outer segment.


1972 ◽  
Vol 53 (1) ◽  
pp. 185-209 ◽  
Author(s):  
Matthew M. LaVail ◽  
Richard L. Sidman ◽  
Deborah O'Neil

Protein synthesis and displacement in photoreceptor and pigment epithelial cells of inbred normal (Fisher) and mutant (RCS) rats with inherited retinal degeneration has been studied by light and electron microscope radioautography. Groups of animals 14, 15, 17, 19, 27, 35, and 50 days of age were injected with amino acids-H3 and killed at subsequent time intervals. In normal rats, radioactive protein synthesized in the rod inner segments was incorporated into outer segment saccules and displaced outward; the total renewal time of outer segments at all ages was approximately 9 days. In RCS photoreceptors, outer segment displacement was slowed from the normal rate before day 17 and at all subsequent stages. Most of the newly synthesized protein appeared to migrate only into the basal third of the outer segments. Labeling of pigment epithelial cells in RCS rats was always heavier than in controls. Labeled protein was displaced as early as 1 hr postinjection from pigment epithelial cell somas into the apical processes, and by 2 hr postinjection was located in the adjacent lamellar whorls characteristic of the mutant rat retina. After 1 day, radioactivity was present in the 14, 15, 17, and 19 day series of RCS rats in the apical third of the outer segment layer (occupied mainly by extra lamellar material) while there were few silver grains in the middle third of the layer (occupied mainly by distal parts of outer segments). The RCS pigment epithelial cells thus have an unusual synthetic role and appear to be a source of the extra lamellar material. Electron microscope examination revealed that many intact pigment epithelial cell processes were incorporated into the large whorls of extra lamellae. In addition, many disorganized outer segment saccules were observed in continuity with longer membranous lamellae and large lamellar whorls. The extra lamellar material therefore appears to be derived from both rod outer segments and pigment epithelial cells.


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.


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.


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.


Marine catfishes (Ariidae) and freshwater catfishes (Ictaluridae) have ocular tapeta lucida. Species examined were Bagre marinus (Mitchill), Arius felis (L.), Ictalurus punctatus (Rafinesque), I. natalis (Lesueur), I. nebulosus (Lesueur) and Pylodictis olivaris (Rafinesque). The tapeta are white reflectors located in the pigment epithelium; they occupy most of the fundus except for a narrow black ventral field. A more extensive study was made of the tapetum of the hardhead catfish A. felis . In histologic sections the tapetum is yellow brown and is easily confused with retinal pigment. It can be distinguished because it stains with ferric-ferricyanide and dissolves in methanol-hydrochloric acid after Carnoy fixation. The tapetum is occluded by melanosomes which move inwards in light, and it is exposed by movement outwards of melanosomes in dim light or darkness. Electron microscopy shows that processes of the pigment epithelial cells contain many membrane-bound tapetal spheres which enclose the tapetal pigment and are responsible for reflexion of light. Spheres are 370 nm in diameter (average); there are about 5.5 spheres in 1 μm 3 , and the tapetum is about 90 μm thick. Rods and cones are equal in number; rods form a single layer, cones are single and possess an accessory outer segment. Transmission of the tapetum is minimal at short wavelengths and rises steadily above 500 nm. Reflectance is diffuse; it rises to a maximum at 500 nm, and is high at long wavelengths. The tapetum has a high refractive index, ca . 1.56, favouring light scattering. Some characteristics of the extracted tapetal pigment are pre­sented: it is light yellow, and absorbance maxima occur at 260 and 330 nm in acidic meth­anol. The pigment epithelium contains lysosome-like bodies but no myeloid bodies. The hardhead retina contains a visual pigment 527 2 . Measurements of natural light (irradiance) in coastal waters inhabited by sea catfishes are presented: the waters are turbid and transmit maximally at 575 to 580 nm. The findings, in relation to earlier work on the catfish eye, performance of the eye and habits of the fish are discussed.


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.


2005 ◽  
Vol 22 (2) ◽  
pp. 203-209 ◽  
Author(s):  
GUS J. MENGER ◽  
JOSEPH R. KOKE ◽  
GREGORY M. CAHILL

Key indicators of circadian regulation include the persistence of physiological rhythmicity in the absence of environmental time cues and entrainment of this rhythmicity by the ambient light cycle. In some teleosts, the inner segments of rod and cone photoreceptors contract and elongate according to changes in ambient lighting and the circadian cycle. Pigment granules in the retinal pigment epithelium (RPE) disperse and aggregate in a similar manner. Collectively, these movements are known as retinomotor movements. We report the histological characterization of diurnal and circadian retinomotor movements in zebrafish, Danio rerio. Adult fish subjected to a 14:10 light:dark (LD) cycle, constant darkness (DD), or constant light (LL) were sacrificed at 1–13 h intervals and processed for semithin sectioning of the retina. Using bright-field microscopy, 15 measurements of pigment granule position and the inner segment lengths of 30 rods and 30–45 cones were collected from the central third of the dorso-optic retina per time point. In LD, rods and cones followed a clear diurnal rhythm in their inner segment movements. Short-single, UV-sensitive cones were found to contract significantly 1 h before light onset in LD conditions. In DD conditions, the inner segments movements of short-single and double cones displayed statistically significant rhythms. RPE pigment granule movements are rhythmically regulated in both LD and DD although fluctuations are damped in the absence of photic cues. No significant retinomotor movements were observed in LL. These findings indicate retinomotor movements in zebrafish are differentially regulated by an endogenous oscillator and by light-dependent mechanisms.


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