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Proteoglycans in the mouse interphotoreceptor matrix. III. Changes during photoreceptor development and degeneration
1Cullen Eye Institute, Baylor College of Medicine, Houston, TX 77030.
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 micron long and 5-10 nm in diameter), and type C filaments (up to 1 micron 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.
Insights
Sulfated proteoglycans in the interphotoreceptor matrix (IPM) of rds mice develop similarly to normal mice. Photoreceptor degeneration leads to the loss of these IPM proteoglycans, suggesting photoreceptors maintain them.
Area of Science:
- Ophthalmology
- Developmental Biology
- Biochemistry
Background:
- The interphotoreceptor matrix (IPM) is a complex extracellular matrix crucial for photoreceptor function.
- Sulfated proteoglycans are key components of the IPM, but their developmental roles and regulation are not fully understood.
- The rds mouse model exhibits photoreceptor degeneration, providing a unique system to study IPM changes.
Purpose of the Study:
- To investigate the distribution and development of sulfated proteoglycans in the IPM of rds mice during photoreceptor degeneration.
- To compare the IPM proteoglycan profiles in rds mice with those of normal mice.
- To determine the role of photoreceptors in the maintenance of IPM proteoglycans.
Main Methods:
- Electron microscopy was used to examine the IPM.
- Cupromeronic Blue (CmB) staining identified sulfated proteoglycans.
- Chondroitinase AC pretreatment was employed to analyze proteoglycan composition.
- RDS mice at various ages were compared with normal mice.
Main Results:
- Three types of CmB-positive filaments (A, B, C) were identified in the IPM, with distinct morphologies and distributions.
- IPM proteoglycan development in early postnatal rds mice mirrored that of normal mice.
- During photoreceptor degeneration, type B and C filaments persisted, while type A filaments were mainly in pigment epithelial cells.
- In aged rds mice with minimal photoreceptors, IPM staining was significantly reduced.
- Chondroitinase AC treatment largely eliminated CmB staining, indicating the presence of chondroitin sulfate proteoglycans.
Conclusions:
- Chondroitin sulfate proteoglycans in the IPM of rds mice exhibit normal structural types and early development.
- Differences in proteoglycan distribution in rds mice are attributed to photoreceptor loss.
- Photoreceptor cells appear critical for the maintenance of IPM proteoglycans.