Abstract
Mature retinal rod photoreceptors sequester opsin in the disk and plasma membranes of the rod outer segment (ROS). Opsin is synthesized in the inner segment and is transferred to the outer segment along the connecting cilium that joins the two compartments. We have investigated early stages of retinal development during which the polarized distribution of opsin is established in the rod photoreceptor cell. Retinas were isolated from newborn rats, 3-21 d old, and incubated with affinity purified biotinyl-sheep anti-bovine opsin followed by avidin- ferritin. At early postnatal ages prior to the development of the ROS, opsin is labeled by antiopsin on the inner segment plasma membrane. At the fifth postnatal day, as ROS formation begins opsin was detected on the connecting cilium plasma membrane. However, the labeling density of the ciliary plasma membrane was not uniform: the proximal cilium was relatively unlabeled in comparison with the distal cilium and the ROS plasma membrane. In nearly mature rat retinas, opsin was no longer detected on the inner segment plasma membrane. A similar polarized distribution of opsin was also observed in adult human rod photoreceptor cells labeled with the same antibodies. These results suggest that some component(s) of the connecting cilium and its plasma membrane may participate in establishing and maintaining the polarized distribution of opsin.
Full Text
The Full Text of this article is available as a PDF (951.6 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Andrews L. D., Cohen A. I. Freeze-fracture studies of photoreceptor membranes: new observations bearing upon the distribution of cholesterol. J Cell Biol. 1983 Sep;97(3):749–755. doi: 10.1083/jcb.97.3.749. [DOI] [PMC free article] [PubMed] [Google Scholar]
- BONTING S. L., CARAVAGGIO L. L., GOURAS P. The rhodopsin cycle in the developing vertebrate retina. I. Relation of rhodopsin content, electroretinogram and rod structure in the rat. Exp Eye Res. 1961 Sep;1:14–24. doi: 10.1016/s0014-4835(61)80004-3. [DOI] [PubMed] [Google Scholar]
- Battelle B. A., LaVail M. M. Rhodopsin content and rod outer segment length in albino rat eyes: modification by dark adaptation. Exp Eye Res. 1978 Apr;26(4):487–497. doi: 10.1016/0014-4835(78)90134-3. [DOI] [PubMed] [Google Scholar]
- Besharse J. C., Pfenninger K. H. Membrane assembly in retinal photoreceptors I. Freeze-fracture analysis of cytoplasmic vesicles in relationship to disc assembly. J Cell Biol. 1980 Nov;87(2 Pt 1):451–463. doi: 10.1083/jcb.87.2.451. [DOI] [PMC free article] [PubMed] [Google Scholar]
- CARAVAGGIO L. L., BONTING S. L. The rhodopsin cycle in the developing vertebrate retina. II. Correlative study in normal mice and in mice with hereditary retinal degeneration. Exp Eye Res. 1963 Jan;2:12–19. doi: 10.1016/s0014-4835(63)80018-4. [DOI] [PubMed] [Google Scholar]
- DE ROBERTIS E. Some observations on the ultrastructure and morphogenesis of photoreceptors. J Gen Physiol. 1960 Jul;43(6):1–13. doi: 10.1085/jgp.43.6.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
- DOWLING J. E., SIDMAN R. L. Inherited retinal dystrophy in the rat. J Cell Biol. 1962 Jul;14:73–109. doi: 10.1083/jcb.14.1.73. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Galbavy E. S., Olson M. D. Morphogenesis of rod cells in the retina of the albino rat: a scanning electron microscopic study. Anat Rec. 1979 Dec;195(4):707–717. doi: 10.1002/ar.1091950410. [DOI] [PubMed] [Google Scholar]
- Gilula N. B., Satir P. The ciliary necklace. A ciliary membrane specialization. J Cell Biol. 1972 May;53(2):494–509. doi: 10.1083/jcb.53.2.494. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Heitzmann H., Richards F. M. Use of the avidin-biotin complex for specific staining of biological membranes in electron microscopy. Proc Natl Acad Sci U S A. 1974 Sep;71(9):3537–3541. doi: 10.1073/pnas.71.9.3537. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jan L. Y., Revel J. P. Ultrastructural localization of rhodopsin in the vertebrate retina. J Cell Biol. 1974 Aug;62(2):257–273. doi: 10.1083/jcb.62.2.257. [DOI] [PMC free article] [PubMed] [Google Scholar]
- LaVail M. M. Photoreceptor characteristics in congenic strains of RCS rats. Invest Ophthalmol Vis Sci. 1981 May;20(5):671–675. [PubMed] [Google Scholar]
- Nir I., Papermaster D. S. Differential distribution of opsin in the plasma membrane of frog photoreceptors: an immunocytochemical study. Invest Ophthalmol Vis Sci. 1983 Jul;24(7):868–878. [PubMed] [Google Scholar]
- Papermaster D. S. Preparation of antibodies to rhodopsin and the large protein of rod outer segments. Methods Enzymol. 1982;81:240–246. doi: 10.1016/s0076-6879(82)81037-9. [DOI] [PubMed] [Google Scholar]
- Papermaster D. S., Schneider B. G., Zorn M. A., Kraehenbuhl J. P. Immunocytochemical localization of opsin in outer segments and Golgi zones of frog photoreceptor cells. An electron microscope analysis of cross-linked albumin-embedded retinas. J Cell Biol. 1978 Apr;77(1):196–210. doi: 10.1083/jcb.77.1.196. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Peters K. R., Palade G. E., Schneider B. G., Papermaster D. S. Fine structure of a periciliary ridge complex of frog retinal rod cells revealed by ultrahigh resolution scanning electron microscopy. J Cell Biol. 1983 Jan;96(1):265–276. doi: 10.1083/jcb.96.1.265. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rothman J. E., Fries E., Dunphy W. G., Urbani L. J. The Golgi apparatus, coated vesicles, and the sorting problem. Cold Spring Harb Symp Quant Biol. 1982;46(Pt 2):797–805. doi: 10.1101/sqb.1982.046.01.075. [DOI] [PubMed] [Google Scholar]
- Röhlich P. The sensory cilium of retinal rods is analogous to the transitional zone of motile cilia. Cell Tissue Res. 1975 Aug 25;161(3):421–430. doi: 10.1007/BF00220009. [DOI] [PubMed] [Google Scholar]
- Satir B., Sale W. S., Satir P. Membrane renewal after dibucaine deciliation of Tetrahymena. Freeze-fracture technique, cilia, membrane structure. Exp Cell Res. 1976 Jan;97:83–91. doi: 10.1016/0014-4827(76)90657-1. [DOI] [PubMed] [Google Scholar]
- Steinberg R. H., Fisher S. K., Anderson D. H. Disc morphogenesis in vertebrate photoreceptors. J Comp Neurol. 1980 Apr 1;190(3):501–508. doi: 10.1002/cne.901900307. [DOI] [PubMed] [Google Scholar]
- Wald G. Molecular basis of visual excitation. Science. 1968 Oct 11;162(3850):230–239. doi: 10.1126/science.162.3850.230. [DOI] [PubMed] [Google Scholar]
- Young R. W. Passage of newly formed protein through the connecting cilium of retina rods in the frog. J Ultrastruct Res. 1968 Jun;23(5):462–473. doi: 10.1016/s0022-5320(68)80111-x. [DOI] [PubMed] [Google Scholar]