Retinomotor pigment migration in the teleost retinal pigment epithelium. I. Roles for actin and microtubules in pigment granule transport and cone movement.

In lower vertebrates, retinal pigment epithelial (RPE) cells and photoreceptors undergo dramatic "retinomotor movements" in response to changes in light conditions. In the dark, RPE pigment granules aggregate to the (choroidal) base of the RPE cells, cones elongate, and rods contract. In the light, movements are reversed: pigment granules migrate out into the long apical projections of the RPE cells, cones contract, and rods elongate. In this report the time courses of dark-induced pigment aggregation and light-induced dispersion have been characterized (and compared to cone movements) in the blue stripe grunt, Haemulon sciurus. It was found that aggregation and dispersion occur at linear rates of 3.4-3.5 microns/min and that RPE movements are kinetically independent from cone movements induced by the same changes in light conditions. The roles of actin and microtubules in RPE and cone movements were also investigated by using the actin-inhibitors, cytochalasins-B and -D, and the microtubule inhibitor, colchicine. Light-induced pigment dispersion, as well as maintenance of the fully dispersed (light-adapted) position appear to require actin-dependent processes. Intraocularly injected cytochalasins-B and -D fully prevented pigment dispersion when administered to dark-adapted animals immediately prior to their exposure to light, and caused pigment aggregation to the RPE cell base when administered to fully light-adapted animals. Ultrastructural studies showed that actin filaments, which in untreated retinas were found closely associated with pigment granules and the plasma membrane, were disrupted after cytochalasin-B treatment. Both dispersive and aggregative pigment movements within the cell body appeared to require microtubule-dependent processes. Intraocularly injected colchicine disrupted microtubules and blocked pigment granule translocation in both directions in the cell body. A hypothetical model to explain pigment movements in response to changes in light conditions is proposed based on these observations as well as on data from the literature.