Proteoglycans in the mouse interphotoreceptor matrix. III. Changes during photoreceptor development and degeneration in the rds mutant

Abstract

The distribution of sulfated proteoglycans in the interphotoreceptor matrix (IPM) was examined during development and degeneration of photoreceptors in the rds mouse with electron microscopy after staining with the cationic dye Cupromeronic Blue (CmB). Three distinct CmB-positive filaments types were observed: type A (45–55 nm long and around 5 nm in diameter), type B (up to 0·5 μm long and 5–10 nm in diameter), and type C filaments (up to 1 μm long and 15–25 nm in diameter. During early postnatal development, before degenerative changes occur in photoreceptors, CmB-positive filaments were virtually identical in morphology and pattern of development as those recently reported for the normal mouse IPM ( Tawara, Varner and Hollyfield, 1989 Exp. Eye Res. 48, 815-39). From 10 days to 1 year of age, during the period of progressive degeneration and loss of photoreceptor cells, numerous type B and type C filaments were present in the IPM. Type B filaments were distributed throughout the IPM, whereas type C were predominantly located around the apical termination of photoreceptor inner segments and between the pigment epithelial microvilli. Type A filaments were located principally in the apical cytoplasm of the pigment epithelial cells and in the proximal IPM. In the 20-month-old rds mouse, a time when virtually no photoreceptor cells remain, only minimal CmB staining was evident at the interface between the pigment epithelium and retina. Pretreatment with chondroitinase AC eliminated most CmB-positive filaments from the 18-day-old and 20-month-old mouse IPM. These findings suggest that there are no major differences in structural type or early postnatal development of chondroitin sulfate-type proteoglycans in the IPM between rds and normal mice. Any differences in distribution of chondroitin sulfate-type proteoglycans between rds and normal mice can be accounted for by the absence of photoreceptor outer segments and progressive loss of photoreceptor cells in this mutant. The disappearance of these IPM proteoglycans following photoreceptor degeneration suggests that photoreceptors may be critically involved in the maintenance of these matrix components.