Evidence for the transport of opsin in the connecting cilium and basal rod outer segment in rat retina: rapid-freeze, deep-etch and horseradish peroxidase labelling studies
In order to clarify the pathway of opsin transport in the connecting cilium and basal rod outer segment, we examined rat rod cells by a rapid-freeze and deep-etch technique and also examined the uptake of horseradish peroxidase into isolated retina. The distribution of intramembrane particles on the P-face of the cilium indicated that the ciliary plasma membrane has similar opsin content to the basal rod outer segment plasma membrane. Dilated cisternae were detected below the stack of disk membranes at the basal rod outer segment in fresh retina. The fine structure of the P-face and true surface of these cisternae was identical to that of the disk membrane. Uptake of horseradish peroxidase was detected in the cisternae or in both cisternae and most basal disk, indicating that the cisternae are formed prior to the disk membrane. In the distal part of connecting cilium, we found axially oriented infoldings on the P-face of the plasma membrane, and subplasmalemmal tubules or cisternae adjacent and parallel to them. Such subplasmalemmal membranes were labeled by exogeneous horseradish peroxidase, suggesting that the infoldings are invaginating plasma membrane. These results may indicate that opsin molecules are conveyed on the ciliary plasma membrane, and that this opsin-rich plasma membrane is internalized in the distal connecting cilium to form dilated cisternae, which subsequently change to the disk membranes.
KeywordsRetina Horseradish Peroxidase True Surface Disk Membrane Basal Disk
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Besharse, J. C., Hollyfield, J. G.
&Rayborn, M. E.
(1977) Turnover of rod photoreceptor outer segments. I. Membrane addition and loss in relationship to temperature.Journal of Cell Biology
, 490–506.Google Scholar
Besharse, J. C., Forestner, D. M.
&Defoe, D. M.
(1985) Membrane assembly in retinal photoreceptors III. Distinct membrane domains of the connecting cilium of developing rods.Journal of Neuroscience
, 1035–48.PubMedGoogle Scholar
Chabre, M., Cavaggioni, A., Osborne, H. B., Gulik-Krzywicki, T.
, &Olive, J.
(1972) A rhodopsin-lipid- water lamellar system: its characterization by X-ray diffraction and electron microscopy.FEBS Letters
, 197–202.PubMedGoogle Scholar
Chaitin, M. H., Schneider, B. G., Hall, M. O.
&Paper- Master, D. S.
(1984) Actin in the photoreceptor connecting cilium: immunocytochemical localization to the site of outer segment disk formation.Journal of Cell Biology
, 239–47.PubMedGoogle Scholar
Fliesler, S. J., Rayborn, M. E.
&Hollyfield, J. G.
(1985) Membrane morphogenesis in retinal rod outer segments: inhibition by tunicamycin.Journal of Cell Biology
, 574–87.PubMedGoogle Scholar
Flower, N. E.
(1971) Particles within membranes: a freeze- etch view.Journal of Cell Science
, 435–41.PubMedGoogle Scholar
Fung, B. K.-K.
&Hubbell, W. L.
(1972) Preparation and properties of phospholipid bilayers containing rhodopsin.Proceeding of the National Academy of Sciences (USA)
, 2617–21.Google Scholar
Gilula, N. B.
(1972) The ciliary necklace. A ciliary membrane specialization.Journal of Cell Biology
, 494–509.PubMedGoogle Scholar
Gotow, T., Miyaguchi, K.
&Hashimoto, P. H.
(1991) Cytoplasmic architecture of the axon terminal: filamentous strands specially associated with synaptic vesicles.Neuroscience
, 587–98.PubMedGoogle Scholar
Hall, M. O., Bok, D.
&Bacharach, A. D. E.
(1969) Biosynthesis and assembly of the rod outer segment membrane system: function and fate of visual pigment in the frog retina.Journal of Molecular Biology
, 397–406.PubMedGoogle Scholar
Heuser, J. E.
&Reese, T. S.
(1973) Evidence for recycling of synaptic vesicle membrane during transmitter release at the frog neuromuscular junction.Journal of Cell Biology
, 315–44.PubMedGoogle Scholar
(1974) Membrane particles of the connecting cilium.Journal of Ultrastructure Research
, 305–12.Google Scholar
Nilsson, S. E. G.
(1964) Receptor cell outer segment development and ultrastructure of the disk membranes in the retina of the tadpole (Rana pipiens).Journal of Ultrastructure Research
, 581–620.PubMedGoogle Scholar
&Papermaster, D. S.
(1983) Differential distribution of opsin in the plasma membrane of frog photoreceptors: an immunocytochemical study.Investigative Ophthalmology & Visual Science
, 868–78.Google Scholar
Nir, I., Cohen, D. A.
&Papermaster, D. S.
(1984) Immunocytochemical localization of opsin in the cell membrane of developing rat retinal photoreceptors.Journal of Cell Biology
, 1788–95.PubMedGoogle Scholar
Papermaster, D. S., Converse, C. A.
(1975) Membrane biosynthesis in the frog retina: opsin transport in the photoreceptor cell.Biochemistry
, 2438–42.Google Scholar
Papermaster, D. S., Schneider, B. G., Zorn, M. A.
&Kraehenbuhl, J. P.
(1978) Immunocytochemical localization of opsin in the outer segments and Golgi zones of frog photoreceptor cells.Journal of Cell Biology
, 196–210.PubMedGoogle Scholar
Peters, K. R., Palade, G. E., Schneider, B. G.
&Paper-Master, D. S.
(1983) Fine structure of a periciliary ridge complex of frog retinal rod cells revealed by ultrahigh resolution scanning electron microscopy.Journal of Cell Biology
, 265–76.PubMedGoogle Scholar
Richardson, T. M.
(1969) Cytoplasmic and ciliary connections between the inner and outer segments of mammalian visual receptors.Vision Research
, 727–31.PubMedGoogle Scholar
(1975) The sensory cilium of retinal rods is analogous to the transitional zone of motile cilia.Cell and Tissue Research
, 421–30.PubMedGoogle Scholar
Steinberg, R. H., Fisher, S. K.
&Anderson, D. H.
(1980) Disc morphogenesis in vertebrate photoreceptors.Journal of Comparative Neurology
, 501–18.PubMedGoogle Scholar
Young, R. W.
(1967) The renewal of photoreceptor cell outer segments.Journal of Cell Biology
, 61–72.PubMedGoogle Scholar
Young, R. W.
(1968) Passage of newly formed protein through the connecting cilium of retinal rods in the frog.Journal of Ultrastructure Research
, 462–73.PubMedGoogle Scholar
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