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Membrane assembly in retinal photoreceptors. III. Distinct membrane domains of the connecting cilium of developing rods. J Neurosci 1985 Apr;5(4):1035-48

Date

04/01/1985

Pubmed ID

3156973

Pubmed Central ID

PMC6565013

DOI

10.1523/JNEUROSCI.05-04-01035.1985

Scopus ID

2-s2.0-0021964082 (requires institutional sign-in at Scopus site)   83 Citations

Abstract

To investigate the putative role of the photoreceptor connecting cilium in the delivery of opsin to forming discs and in the maintenance of membrane domains (Besharse, J. C., and K. H. Pfenninger (1980) J. Cell Biol. 87: 451-463), we have studied developing photoreceptors of neonatal rats during the period of initial disc formation using conventional freeze-fracture, immunocytochemistry, and lectin cytochemistry. Specific anti-opsin-binding sites were localized in the distal cilium, the developing outer segment plasma membrane, and at focal sites on the inner segment plasma membrane at all developmental stages examined, including the period prior to the onset of disc morphogenesis. The proximal ciliary shaft generally lacked anti-opsin-binding sites or exhibited them in extremely low density. The distribution of anti-opsin-binding sites corresponded in a general way to the distribution of large intramembranous particles (IMPs) in freeze-fracture replicas like those seen in the rod outer segment (ROS). The proximal zone corresponded in freeze-fracture images to a zone of consecutive horizontal rows of intramembrane particles (ciliary necklaces) and axoneme-membrane cross-linkers. Although protoplasmic face leaflet IMPs similar to those of the distal cilium and outer segment were less abundant in the inner segment and proximal cilium than in the distal cilium and ROS, they were detected in these zones at low frequency. Cytochemistry with concanavalin A and wheatgerm agglutinin revealed the presence of a well developed glycocalyx in the proximal zone. Although opsin binds both lectins, the results suggest heterogeneity among the glycoconjugates of the three membrane domains. Our data define distinct membrane domains of the developing photoreceptor cilium that have important implications for the mechanisms for delivering and sequestering opsin in the outer segment. They also establish that the mechanism of opsin delivery to the distal zone occurs well in advance of the period of disc morphogenesis.

Author List

Besharse JC, Forestner DM, Defoe DM



MESH terms used to index this publication - Major topics in bold

Animals
Animals, Newborn
Antibodies
Binding Sites
Cilia
Concanavalin A
Eye Proteins
Histocytochemistry
Immunochemistry
Lectins
Membranes
Photoreceptor Cells
Rats
Rats, Inbred F344
Rats, Inbred Strains
Retina
Rod Opsins
Tissue Distribution
Wheat Germ Agglutinins