Relation of retinomotor responses and contractile proteins in vertebrate retinas

Photoreceptors of many nonmammalian vertebrate species display pronounced light-dependent movements which are absent in mammalian species. In order to further analyze the molecular basis of receptor movements and of simultaneous migration of melanin granules in pigment epithelial processes, we investigated the distribution of actin, myosin and the actin-binding muscular proteins alpha-actinin and vinculin in the retina of various vertebrate species. The species investigated can be divided in two groups (i) those possessing retinomotor capacity (fish, frog, turtle, chick) and (ii) those in which retinomotor activities are negligible or absent (gecko, mouse, rat). Prominent bundles of actin filaments extending throughout the long axis of photoreceptor inner segments were only found in species possessing retinomotor capacity, while comparable actin filament bundles were absent or poorly developed in photoreceptors of species lacking significant retinomotor capacity. In all species examined, a well developed circumferential band of actin filaments was associated with the zonula adhaerens-like junctions between photoreceptors and Müller (glial) cells forming the external limiting membrane. This area was also identified as the exclusive site of myosin, alpha-actinin and vinculin (only in the chick, alpha-actinin-like immunoreactivity was also found along the photoreceptor actin filament bundles). Thus, the external limiting membrane may be important for both structural support and for providing a possible site of filament sliding for photoreceptor movements. In pigment epithelium actin, myosin, alpha-actinin and vinculin were concentrated circumferentially in the area of the terminal bar which has been previously shown to be contractile. In all species apical pigment-epithelial processes displayed actin-like fluorescence of varying intensities. Another site of actin-like staining were photoreceptor synaptic complexes which represent a well known site for synaptic plasticity. Immunoblotting studies on the avascular chick retina revealed polypeptide bands at Mr approximately 130 000, approximately 100 000, and 42 000 which were specific for vinculin, alpha-actinin and actin, respectively. A faint polypeptide band comigrating with thymus myosin heavy chain indicates myosin to be only a minor component of the retina (chick and fish).