Microtubules in a rod-specific cytoskeleton associated with outer segment incisures

Abstract

In many vertebrate retinas the outer segments of rod photoreceptors have multiple incisures, that is, there are numerous indentations in the highly curved membrane forming the edge of their disks and in the plasma membrane enclosing the entire stack of disks. Immunofluorescent localization of tubulin in amphibian photoreceptors yielded a novel series of thin, parallel, fluorescent lines in rod outer segments that extended their full length and coincided with their multiple incisures. Electron-microscopic examination of amphibian retinas revealed the structures responsible for this fluorescence: longitudinally oriented microtubules were associated with incisures at heights throughout rod outer segments. These microtubules were located between the disk rims and the overlying plasma membrane, in the small cytoplasmic compartment at the mouth of incisures; the microtubules and membranes were separated from each other by distances that were uniform, as though interconnected by filaments described in other studies. Thus, in amphibian rod outer segments the incisures mark the site of a cytoskeletal system containing longitudinal microtubules distinct from those of the ciliary axoneme, linked by filaments to the adjacent membranes. This cytoskeleton is expected to be important for the normal structure, function, and renewal of rod outer segments. In amphibian cone outer segments, which do not have incisures, the only anti-tubulin immunofluorescence and the only microtubules were at the axoneme. These findings may help elucidate the diverse properties of rods and cones in many vertebrate retinas and could prove relevant for human retinal degenerations.

Collagen XVII and BPAG1 expression in the retina: Evidence for an anchoring complex in the central nervous system

“…It is possible that the differential expression of BPAG1 in these two cell types reflects a role of BPAG1 in outer segment structural stability or synthesis. This hypothesis is compatible with the specific cytoskeletal composition of rod outer segments (Eckmiller, 2000). The dysmorphisms in outer segment formation in the ␤2-deficient mice suggest a role for laminin 14 and 15 in their morphogenesis (Libby et al, 1999).…”

Mechanism of light‐induced translocation of arrestin and transducin in photoreceptors: Interaction‐restricted diffusion

“…Microtubules are particularly abundant in the inner segment (28). Biochemical fractionation of the retina showed that more arrestin is bound to tubulin in dark than in light.…”

Visual Arrestin Binding to Microtubules Involves a Distinct Conformational Change

“…The most conservative estimate of visual arrestin concentration in rod photoreceptors is ϳ150 M (29). Rod cells are neurons with a very high microtubule content (40). Calculations based on the law of mass action show that at 150 M arrestin in the presence of 150 M microtubules the proportion of MTbound arrestin in the dark would be 45-50% at a K d of 75-100 M (our lowest affinity estimate for full-length arrestin).…”

“…Recent measurements suggest that the arrestin concentration in rods may be much higher (41), which favors arrestin interaction with MTs even more. Moreover, MTs in rods are highly enriched in the inner segment (40) where arrestin is also concentrated in dark-adapted photoreceptors. Thus visual arrestin binding to MTs has particular physiological relevance in rods and demonstrates how microtubules serve as a default interaction partner in dark-adapted photoreceptors as we have shown recently (6).…”