Cytoskeleton participation in subcellular trafficking of signal transduction proteins in rod photoreceptor cells.
Light sensitivity and adaptation, general characteristics of rod photoreceptor cell vision, allow rods to modulate their response depending on the lighting environment to which they are exposed. In dim light, rods are maximally sensitive, whereas, in bright light, rods are essentially inactive. In the retinas of dark-adapted mice, arrestin (an inhibitory protein) is located in the rod inner segment (RIS), and transducin (an activating protein) is located in the rod outer segment (ROS). In light-adapted retinas, the proteins have reciprocal localizations. In this study, our data demonstrate that the temporal and spatial changes in the subcellular localization of arrestin and beta-transducin are correlated with the amount of light to which the animals are exposed. By using the frog Xenopus laevis and immunofluorescence confocal microscopy, our results also show that in the dark-adapted retina some arrestin remains in the ROS. The data most dramatically demonstrate that this residual arrestin is highly concentrated in the connecting cilium, the axoneme, and the microtubules associated with the disc incisures. These data suggest a structure-function relationship between the light-dependent positional status of arrestin and the elements of the rod photoreceptor cytoskeleton. The massive, rapid, light-induced reciprocal changes in the subcellular concentrations of these proteins must directly affect phototransduction and appear to be a general phenomenon by which photoreceptor cells rapidly and transiently regulate the trafficking and subcellular concentration of a variety of signal transduction proteins within the RIS and ROS. Hereditary mutations in the components of the movement mechanism should lead to defects in vision and possibly blindness.
McGinnis
James F
JF
Department of Ophthalmology, Dean McGee Eye Institute, University of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma, USA. james-mcginnis@ouhsc.edu
Matsumoto
Brian
B
Whelan
James P
JP
Cao
Wei
W
D000818:Animals; D019393:Arrestin / Q000378:metabolism; D003599:Cytoskeleton / Q000378:metabolism* / Q000648:ultrastructure*; D003623:Dark Adaptation / Q000502:physiology; D007150:Immunohistochemistry; D051379:Mice; D008807:Mice, Inbred BALB C; D021381:Protein Transport / Q000502:physiology*; D017948:Retinal Rod Photoreceptor Cells / Q000378:metabolism* / Q000648:ultrastructure*; D012374:Rod Cell Outer Segment / Q000378:metabolism / Q000648:ultrastructure; D015398:Signal Transduction / Q000502:physiology*; D013997:Time Factors; D015293:Transducin / Q000378:metabolism; D014785:Vision, Ocular / Q000502:physiology; D014982:Xenopus laevis
D019393:Arrestin; D015293:Transducin