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The Daily Rhythm of Shedding and Degradation of Rod and Cone Outer Segment Membranes in the Chick Retina

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The Daily Rhythm of Shedding and Degradation of Rod and Cone Outer Segment Membranes in the Chick Retina The daily rhythm of shedding and degradation of rod and cone outer segment membranes in the chick retina Richard W. Young Newly hatched chickens were maintained on a daily light cycle of 12 hr of light and 12 hr of darkness for 12 days. The pigment epithelium was then examined by electron microscopy at different times of day. Shortly after the beginning of the light period, the rods discarded groups of outer segment membranes. During the remainder of the light period, the membranes were degraded by the pigment epithelium. Early in the dark period, the cones shed membranes, which were digested by the pigment epithelial cells during the subsequent hours of darkness. Available evidence suggests that at least some of the chemical activities of the visual cells and pigment epithelium oscillate with a daily rhythm, tohich is synchronized with the daily fluctua- tion of light in the environment. Key words: visual cells, daily rhythms, renewal, retina, membranes The continual renewal of the light-sensitive steps of membrane assembly. Groups of old membranes of rod outer segments has been membranes are shed intermittently from the amply documented in a wide selection of ver- tips of the rods. This tends to occur early in tebrate animals. In fact, the process has been the morning, in animals maintained on a observed wherever it has been sought—in cycle of 12 hr of light and 12 hr of darkness.3 amphibia, reptiles, birds, fish, and mammals. The adjacent pigment epithelial cells, which It seems to be a fundamental and universal envelop the ends of the outer segments, in- characteristic of rod visual cells.1 gest and degrade the detached membranes.4 The basic mechanism of the renewal pro- In contrast, progress in our understanding cess in rods is "membrane replacement," of the mechanism by which the other class of which has two components: formation of new visual cells, the cones, renew their outer membranes and disposal of old ones.2 The segments had been frustratingly slow. This new membrane constituents are produced in deficiency is even more disturbing when we the inner segment of the cell, then trans- acknowledge that cones play a more impor- ported to the outer segment for the final tant role in meeting human visual needs than do rods. At one time, it seemed as if cones did not From the Department of Anatomy and Jules Stein Eye produce new membranes, but the au- Institute, University of California at Los Angeles. toradiographic evidence on which this con- This research was supported by grants EY 00095 and EY clusion was based later was found to have 0444 from the United States Public Health Service. been misinterpreted.1' 5 Similarly, it ap- Submitted for publication June 1, 1977. peared at first that cones did not shed mem- Reprint requests: Dr. Richard W. Young, Department of Anatomy, School of Medicine, University of Califor- branes. This too proved to be incorrect, nia, Los Angeles, California, 90024. when evidence of disc shedding by cones 0146-0404/78/0217-0105$01.20/0 © 1978 Assoc. for Res. in Vis. and Ophthal., Inc. 105 Downloaded from iovs.arvojournals.org on 09/30/2021 Invest. Ophthalmol. Visual Sci. 106 Young February 1978 100 r 75 X < 50 25 A 10 12 14 16 18 20 22 24 TIME OF DAY Fig. 1. Changes in the number of phagosomes in pigment epithelial cells of the chick retina at different times of day, expressed as a percentage of the maximum observed concentration. Time of day is given in hours, counting from the onset of the light period. Phagosomes recorded during the light period were derived from rod outer segments; those observed during the dark period were from cones. The shaded curves (filled circles and solid line) represent freshly detached membranes (stage I, Table I). The other curves (triangles and dashed lines) represent older phagosomes, showing signs of degradation (stages II to IV, Table I). Thus the shaded curve indicates the approximate time and duration of membrane detachment and phagocytosis, and the dashed line indicates the period of membrane digestion. Note that although a few cones discard membranes throughout the dark period, the major phase of membrane shedding by cones occurs at the beginning of the dark period, 12 hr after the phase of synchronized shedding of rod membranes. was detected in humans and squirrels.6' 7 wise, their outer segments would soon disap- Nevertheless, no synthesis emerged to tie pear. the sparse bits of information into a coherent This suggested a simple hypothesis: Rods hypothesis of cone outer segment renewal. and cones both renew their outer segments Recently, in considering the implications by membrane replacement. The process fol- of LaVail's report3 that rat rods shed mem- lows a daily rhythm, and the rhythms of rods branes early in the daily light period, it oc- and cones are separated in time by approxi- curred to me that cones might also dispose of mately 12 hr. outer segment membranes at a certain time To learn if renewal by membrane replace- of day. Accordingly, O'Day and I8 looked for ment was unique to goldfish cones or was a evidence of this process in goldfish which more fundamental process which also occurs were on a daily cycle of 12 hr of light and 12 in other vertebrate animals, I repeated the hr of darkness. experiment in a diurnal lizard which con- Shortly after the beginning of the light tained only cones in its retina." The results period, the rods shed packets of membranes were unequivocal. Throughout the entire 12 from the ends of their outer segments, hr light period, there was not the slightest thereby confirming in a fish a rhythmic pro- evidence of any membrane detachment from cess previously documented in rats3 and the ends of the cones. However, less than an frogs.9' l0 Later in the day, soon after the hour after the beginning of the dark period, onset of the dark period, a comparable burst there was a brief phase of membrane shed- of membrane detachment from the ends of ding from the tips of the cone outer seg- the cones took place. If the cones dispose of ments. Before the dark period was over, the membranes on a regular basis, they must also membranes had been fully degraded by the repeatedly form new membranes. Other- pigment epithelium. Downloaded from iovs.arvojournals.org on 09/30/2021 Volume 17 Number 2 Rhythmic shedding of rod and cone membranes 107 The highly reproducible demonstration of Table 1. Number of phagosomes/100 a rhythmic daily disposal of membranes by visual cells in the central region of the cones in a fish and a reptile strongly sup- retina at different times of day ported the proposal that this was a common Phagosome stage characteristic of vertebrate cones. However, Time of day there are some unusual features in these (hr:min) I II HI IV animals. Both are "cold-blooded" (ectother- Light period (0:00): mic). The lizards are unusual among verte- 0.15 0 0 0 0.5 brates in that they lack rods entirely. Fur- 0:30 5.9 8.1 0.8 0.6 0:45 2.3 8.8 2.3 1.9 thermore, the pigment epithelium in the 1:00 0.4 6.7 11.3 0.8 goldfish is atypical, being filled with tapetal 2:00 0 3.4 5.1 19.2 granules, which seem to limit its phagocytic 4:35 0 0 0 8.1 6:35 0 0 0.4 5.2 and degradative capacities, so that these are 8:35 0 0 0 0 supplemented by the acitivities of ameboid 10:10 0 0 0 0 cells. 11:10 0 0 0 0 11:40 0 0.5 0 2.0 Therefore I repeated the experiment in Dark period (12:00): another class of vertebrate animals—a class 12:10 4.8 0 0 0.4 which is homeothermic, with a duplex retina 12:20 7.2 0 0 0.7 and a more conventional pigment epithe- 12:30 4.4 4.1 2.2 0 12:40 12.8 8.4 2.7 0 lium. The animal selected was a bird, the 12:50 9.3 0.7 1.4 0.7 chicken. A report of the results of this exper- 13:00 0.6 6.6 5.9 5.0 iment is given below. 13:30 0.9 7.3 20.0 7.4 14:00 0 4.6 15.1 4.4 Methods 15:00 0.5 11.6 4.8 10.5 16:00 1.2 7.3 4.1 19.8 Twenty-six male chicks (Gallus doinesticus, 18:00 1.1 5.3 2.8 11.9 white Leghorn, XL-link variety) were obtained 20:00 0 4.3 10.0 12.5 22:00 0 1.6 2.0 4.0 from Pace/Setter Products, Inc., Cucamonga, 23:00 2.2 5.1 1.8 2.9 Calif., the clay after hatching. They were main- 23:55 0 0 0 0.8 tained in a photographic darkroom in three metal cages, each measuring 30 by 45 by 60 cm, with a gently removed from the cage without disturbing wire mesh floor. An electric heating pad, set at the remaining chicks. The heads were decapitated "medium,' was lodged against the back wall of into ice-cold fixative in the dark, then brought into each cage to raise the temperature slightly above the light for further dissection. The eyes were that of the darkroom, which was regulated at 24° to enucleated, and the front half of the globe 25° C.
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