Summary
Aberrations of photoreceptor ultrastructure resulting from carotenoid/retinoid (vitamin A) deprivation were studied in the retina of Manduca sexta. The syndrome of chromophore deficiency included hypertrophy of smooth endoplasmic reticulum, variable dilation of rhabdomeric microvilli, the insertion of endomembrane fingers into such enlarged microvilli, and the formation of ‘rhabdomeric vacuoles’, intracellular compartments containing microvilli similar to those of the rhabdomere. Retinas were processed either with conventional procedures employing preliminary aldehyde fixation followed by heavy metal postfixation, or by fixation and incubation in unbuffered OsO4. The latter method deposits osmium throughout the endomembrane system, within the rhabdomeric vacuoles, and in the extracellular space of the rhabdom. However, the intravillous fingers were rarely impregnated with osmium, despite their continuity with densely stained cisternae of the smooth endoplasmic reticulum. We suggest that the insertion of endomembrane fingers into dilated microvilli results from a cytoskeleton-mediated link between cisternae of the smooth endoplasmic reticulum and the rhabdomeric membrane, an association that may be important in the turnover of photoreceptor membrane. We interpret endomembrane hypertrophy and development of rhabdomeric vacuoles as symptoms of disturbance in the pathway leading to the assembly of the rhabdomere resulting from reduced synthesis of visual pigment.
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References
Arikawa K, Hicks JL, Williams DS (1990) Identification of actin filaments in the rhabdomeral microvilli of Drosophila photoreceptors. J Cell Biol 110:1993–1998
Bennett RR, White RH (1989) Influence of carotenoid deficiency on visual sensitivity, visual pigment, and P-face particles of photoreceptor membrane in the moth Manduca sexta. J Comp Physiol [A] 164:321–331
Bennett RR, White RH (1991) 11-Cis retinal restores visual function in vitamin A-deficient Manduca. Visual Neurosci 6:473–479
Blest AD, Stowe S (1990) Dynamic microvillar cytoskeletons in arthropod and squid photoreceptors. Cell Motil Cytoskeleton 17:1–5
Blest AD, Stowe S, Eddey W (1982) A labile, Ca2+ dependent cytoskeleton in rhabdomeral microvilli of blowflies. Cell Tissue Res 223:553–573
Boschek CB, Hamdorf K (1976) Rhodopsin particles in the photoreceptor membrane of an insect. Z Naturforsch 31C:763
Cutz E, Rhoads JM, Drumm B, Sherman PM, Durie PR, Forstner GG (1989) Microvillus inclusion disease: an inherited defect of brush-border assembly and differentiation. N Engl J Med 320:646–651
De Couet HG, Stowe S, Blest AD (1984) Membrane-associated actin in the rhabdomeral microvilli of crayfish photoreceptors. J Cell Biol 98:834–846
Eguchi E, Maeda S, Shimizu I (1991) The formation of myeloid bodies in retinular cells of the pupal compound eyes of silk-worm moths (Bombyx mori) exposed to constant bright light. Cell Tissue Res 265:381
El-Gammal S, Hamdorf K, Henning U (1987) The paracrystalline structure of an insect rhabdomere (Calliphora erythrocephala). Cell Tissue Res 248:511–518
Hafner GS, Tokarski TR, Kipp J (1991) Changes in the microvillus cytoskeleton during rhabdom formation in the retina of the crayfish Procambarus clarkii. J Neurocytol 20:585–596
Harris WA, Ready DF, Lipson ED, Hudspeth AJ, Stark WS (1977) Vitamin A deprivation and Drosophila photopigments. Nature 266:648–650
Johnson JK, Chamberlain SC (1989) Membrane associated axial filaments in rhabdomeral microvilli of Limulus lateral eye photoreceptors. Invest Ophthalmol Vis Sci 30:292
Locke M (1985) A structural analysis of post-embryonic development. In: Kerkut GA, Gilbert LI (eds) Comprehensive insect physiology, biochemistry and pharmacology, vol 2. Pergamon Press, Oxford, NY, pp 87–149
Matsumoto H, Isono K, Pye Q, Pak WL (1987) Gene encoding cytoskeletal proteins in Drosophila rhabdomeres. Proc Natl Acad Sci USA 84:958–989
Matsumoto-Suzuki E, Hirosawa K, Hotta Y (1989) Structure of the subrhabdomeric cisternae in the photoreceptor cells of Drosophila melanogaster. J Neurocytol 18:87–93
McDonald K (1984) Osmium ferricyanide fixation improves microfilament preservation and membrane visualization in a variety of animal cell types. J Ultrastruct Res 86:107–118
Oliveira L, Burns A, Bisalputra T, Yang KC (1983) The use of an ultralow viscosity medium (VCD HSXA) in the rapid embedding of plant-cells for electron-microscopy. J Microsc 132:195–202
Paulsen R, Schwemer J (1979) Vitamin A deficiency reduces the concentration of visual pigment protein within blowfly photoreceptor membranes. Biochim Biophys Acta 557:385–390
Paulsen R, Schwemer J (1983) Biogenesis of blowfly photoreceptor membranes in regulated by 11-cis retinal. Eur J Biochem 137:609–614
Rodriguez-Boulan E, Nelson WJ (1989) Morphogenesis of the polarized epithelial cell phenotype. Science 245:718–725
Saibil H (1982) An ordered membrane-cytoskeleton network in squid photoreceptor microvilli. J Mol Biol 158:435–456
Sapp RJ, Christianson JS, Maier L, Studer K, Stark WS (1991a) Carotenoid replacement therapy in Drosophila: recovery of membrane, opsin and visual pigment. Exp Eye Res 53:73–79
Sapp RJ, Christianson JS, Stark WS (1991b) Turnover of membrane and opsin in visual receptors of normal and mutant Drosophila. J Neurocytol 20:597–608
Schinz RH, Lo M-VC, Larrivee DC, Pak WL (1982) Freeze-fracture study of the Drosophila photoreceptor membrane: mutations affecting membrane particle density. J Cell Biol 93:961–969
Schwemer J (1984) Renewal of visual pigment in photoreceptors of the blowfly. J Comp Physiol [A] 154:535–547
Schwemer J, Henning U (1984) Morphological correlates of visual pigment turnover in photoreceptors of the fly Calliphora erythrocephala. Cell Tissue Res 236:293–303
Stark WS, Sapp RJ, Schilly D (1988) Rhabdomere turnover and rhodopsin cycle: maintenance of retinula cells in Drosophila melanogaster. J Neurocytol 17:499–509
Stowe S, Davis DT (1990) Anti-actin immunoreactivity in retained in rhabdoms of Drosophila ninaC photoreceptors. Cell Tissue Res 260:431–434
Tsukita S, Tsukita S, Matsumoto G (1988) Light-induced structural changes of cytoskeleton in squid photoreceptor microvilli detected by rapid-freeze method. J Cell Biol 106:1151–1160
Walz B, Baumann O (1989) Calcium-sequestering cell organelles: in situ localization, morphological and functional characterization. Prog Histochem Cytochem 201:1–45
White RH (1967) The effect of light and light deprivation upon the ultrastructure of the larval mosquito eye. II. The rhabdom. J Exp Zool 166:405–426
White RH, Bennett RR (1988) Myeloid bodies and intracellular microvilli in chromophore-deprived Manduca photoreceptors. In: Hara T (ed) Molecular physiology of retinal proteins. Proceedings of Yamada Conference XXI. Yamada Science Foundation. Osaka, pp 425–426
White RH, Bennett RR (1989) Ultrastructure of carotenoid-deprivation in photoreceptors of Manduca sexta: myeloid bodies and intracellular microvilli. Cell Tissue Res 257:519–528
White RH, Bennett RR (1991) Osmium deposition specific to smooth endoplasmic reticulum of insect photoreceptors and sarcoplasmic reticulum of muscle. Invest Ophthalmol Vis Sci 32:1151
White RH, Bennett RR (1992) Assembly of rhabdomeric membrane from smooth endoplasmic reticulum can be activated by light in chromophore-deprived photoreceptors of Manduca sexta. Cell Tissue Res 270:65–72
White RH, Brown PK, Hurley AK, Bennett RR (1983) Rhodopsins, retinula cell ultrastructure, and receptor potentials in the compound eye of Manduca sexta. J Comp Physiol [A] 153:59–66
Whittle AC (1976) Reticular specialization in photoreceptors: a review. Zool Scripta 5:191–206
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White, R.H., Bennett, R.R. Rhabdomeric membrane and smooth endoplasmic reticulum in photoreceptors of Manduca sexta: modulations associated with the diurnal light/dark cycle and effects of chromophore deprivation. Cell Tissue Res. 270, 57–64 (1992). https://doi.org/10.1007/BF00381879
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DOI: https://doi.org/10.1007/BF00381879