Journal of Neuroscience, Vol 5, 1035-1048, Copyright © 1985 by Society for Neuroscience
Membrane assembly in retinal photoreceptors. III. Distinct membrane domains of the connecting cilium of developing rods
JC Besharse, DM Forestner and DM Defoe
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.
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