Summary
Although it is now clear that the outer segments of mature vertebrate cones are regularly renewed, it is not known how a cone outer segment can maintain a tapered shape if its narrower tip is periodically lost by shedding. This problem was addressed by morphological examination of photoreceptors in retinas of anurans (Xenopus laevis) and monkeys (Macaca fascicularis). Light microscopy revealed a marked daily change in the shape of cone outer segments in X. laevis: at light offset they were long and conical, at light onset they had shed their narrow tips, were sharply truncated, and 40% shorter. Electron microscopy revealed previously undescribed fine-structural features in these mature cone outer segments, most notably the presence of many partial membrane infoldings within their distal lamellae. The growth of each of these “distal invaginations” apparently split 1 pre-existing distal lamella into 2 daughter lamellae of reduced width. The formation of distal invaginations at various heights within a cone outer segment would thus make it longer and narrower. Similar ultrastructural features were also found in cone outer segments of monkey retinas. These findings suggest that during outer segment renewal the tapered shape of mature cone outer segments is maintained via a remodelling process that accompanies the formation of distal invaginations.
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References
Anderson DH, Fisher SK, Steinberg RH (1978) Mammalian cones: Disc shedding, phagocytosis, and renewal. Invest Ophthalmol Vis Sci 17:117–133
Anderson DH, Fisher SK, Breding DJ (1986) A concentration of fucosylated glycoconjugates at the base of cone outer segments: Quantitative electron microscope autoradiography. Exp Eye Res 42:267–283
Bernstein SA, Breding DJ, Fisher SK (1984) The influence of light on cone disk shedding in the lizard Sceloporus occidentalis. J Cell Biol 99:379–389
Bok D (1985) Retinal photoreceptor-pigment epithelium interactions. Invest Ophthalmol Vis Sci 26:1659–1694
Borwein B (1981) The retinal receptor: a description. In: Enoch JM, Tobey FL (eds) Vertebrate photoreceptor optics, Springer, Berlin Heidelberg New York, pp 11–81
Carter-Dawson LD, La Vail MM (1979) Rods and cones in the mouse retina: I. Structural analysis using light and electron microscopy. J Comp Neurol 188:245–262
Eckmiller MS (1987a) Photoreceptor outer segment renewal: Special features in cones. In: Zrenner E, Krastel H, Goebel HH (eds) Advances in the biosciences, Research in retinitis pigmentosa, Vol. 62, Pergamon Press, Oxford, pp 397–403
Eckmiller MS (1987b) Cone outer segment morphogenesis: Taper change and distal invaginations. J Cell Biol 105:2267–2277
Eckmiller MS (1988) Distal invaginations and cone outer segment shape. Proc Int Soc Eye Res V:162. Abstracts, Eighth International Congress of Eye Research, San Francisco, California, USA, 1988, International Society for Eye Research, Ridgefield, NJ
Eckmiller MS (1989a) Outer segment growth and periciliary vesicle turnover in developing photoreceptors of Xenopus laevis. Cell Tissue Res 255:283–292
Eckmiller MS (1989b) Diurnal changes in cone outer segment (COS) shape during renewal. Invest Ophthalmol Vis Sci [Suppl] 30:156
Eckmiller MS (1989c) Morphogenesis and renewal of outer segments in cone photoreceptors. Habilitation Thesis. Heinrich-Heine-Universität Düsseldorf
Fetter DF, Corless JM (1987) Morphological components associated with frog cone outer segment disc margins. Invest Ophthalmol Vis Sci 28:646–657
Immel JH, Fisher SK (1985) Cone photoreceptor shedding in the tree shrew (Tupaia belangerii). Cell Tissue Res 239:667–675
Nieuwkoop FW, Faber J (1956) Normal table of Xenopus laevis Daudin. North Holland Publishing Co, Amsterdam
Rodieck RW (1973) The vertebrate retina. WH Freeman, San Francisco
Steinberg RH, Fisher SK, Anderson DH (1980) Disc morphogenesis in vertebrate photoreceptors. J Comp Neurol 190:501–518
Young RW (1978) Visual cells, daily rhythms, and vision research. Vision Res 18:573–578
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Portions of this work have been published in abbreviated or preliminary form (Eckmiller 1988, 1989b, c)
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Eckmiller, M.S. Distal invaginations and the renewal of cone outer segments in anuran and monkey retinas. Cell Tissue Res 260, 19–28 (1990). https://doi.org/10.1007/BF00297486
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DOI: https://doi.org/10.1007/BF00297486