Association of Kinesin with Microtubules in Diverse Cytoskeletal Systems in the Outer Segments of Rods and Cones

Abstract

The membranous outer segments of vertebrate photoreceptors are supported by cytoskeletons consisting of microtubules and associated proteins, which occur as the ciliary axoneme in rods and cones, and as a separate cytoskeletal system at the incisures of rod outer segments. We performed an immunocytochemical study of the cytoskeleton in photoreceptors isolated from amphibian retinas and found that immunoreactivity to the heavy chain of the motor protein kinesin was closely associated with the microtubules in each of these outer segment cytoskeletal systems. In the outer segments of cones, kinesin heavy chain immunoreactivity was confined to a streak at the axoneme that extended to the outer segment tip. In the outer segments of rods, kinesin heavy chain immunoreactivity was found as both a short streak at the axoneme and a series of long parallel lines that coincided with the microtubules at rod outer segment incisures. Our findings constitute the first report of kinesin in the axoneme of cones and at the incisures of rods. Closely associated with microtubules, kinesin in photoreceptor outer segment axonemes and at rod outer segment incisures can transport materials longitudinally along the microtubules and/or connect these with each other and/or with other components. Because these cytoskeletal systems differ in fundamental ways, kinesin can play different roles in each case, e.g., kinesin at rod outer segment incisures can have structural and functional roles that are unique to rods. These findings may have clinical relevance because similar cytoskeletal systems are expected to occur in the outer segments of human photoreceptors; thus, a disturbance involving kinesin in the cytoskeletal systems at photoreceptor axonemes and/or at rod outer segment incisures could interfere with the normal structure and function of photoreceptors and contribute to human photoreceptor degenerations.

Heterotrimeric Kinesin-2 (KIF3) Mediates Transition Zone and Axoneme Formation of Mouse Photoreceptors

“…9, D-F, I, and J). An axoneme extends from the basal body, through the PTZ into the OS to about half-length in the rod and to the cone tip in Xenopus (61). The precise axoneme extension in much smaller mouse rods and cones is unknown.…”

Light-Dependent Translocation of Arrestin in the Absence of Rhodopsin Phosphorylation and Transducin Signaling

“…One mechanism by which arrestin redistribution in vertebrate rods could occur is by active transport along the microtubules present in the ciliary axoneme and along the rod outer segment incisures. These structures show immunoreactivity to the kinesin heavy chain (Eckmiller and Toman, 1998), a plus-end directed molecular motor. Interestingly, arrestin immunoreactivity accumulates at these structures in Xenopus retinas during dark adaptation, suggesting that arrestin is a cargo for microtubule-based transport after changes in lighting conditions (McGinnis et al, 2002).…”

Interaction of glutamic-acid-rich proteins with the cGMP signalling pathway in rod photoreceptors

“…Mammalian rods usually have a single incisure per disc 17 and incisures of adjacent discs are aligned for several micrometres along the outer segment. Several of these longitudinal clefts are laterally displaced 18 . Therefore, decoration of incisures similar to the pattern shown in Fig.…”