Mouse Models of Inherited Retinal Degeneration with Photoreceptor Cell Loss
Abstract
:1. Introduction
2. Background
2.1. Photoreceptor (PR) Cell Structure
- The outer segment (OS), which is cylindrical in rod PR cells and tapered in cones, contains phototransduction proteins that sense light and amplify the ensuing signal, culminating in PR cell hyperpolarization (Figure 1c). Much of the phototransduction apparatus is localized to double-bilayer discs formed by evagination of the plasma membrane at the base of the OS. These discs are largely internalized in rods except at the base of the OS, but remain contiguous with the plasma membrane in cones to yield a highly convoluted OS surface [23].
- The OS is stabilized by a ciliary axoneme, which runs through much of its length (Figure 1d; Ax). At the proximal end of the axoneme, the connecting cilium, analogous to the transition zone in other cilia (Figure 1d; CC-TZ), serves as a conduit through which all membrane and protein components destined for the OS are thought to pass. At the base of the connecting cilium lies the basal body (Figure 1d; BB), a cylindrical organelle derived from the mother centriole. Altogether these structures represent a modified primary cilium that encompasses an extensive network of protein complexes that transport proteins and lipids and shares characteristics with primary cilia in many other cell types. The ciliary networks also function to prevent the flow of OS components to other parts of the cell and may associate with the intracellular trafficking apparatus to ensure the directed movement of needed components to the OS.
- The inner segment (IS) contains the biosynthetic machinery and energy sources needed to produce and assemble newly synthesized phototransduction proteins and their associated membranes (Figure 1d). The capacity of this cellular factory is impressive, as up to 10% of the OS is shed daily and removed via phagocytosis by the retinal pigment epithelium (see below) and must be renewed. Most protein and lipid components are synthesized de novo, but the IS also has an extensive recycling machinery that can reassemble components provided from outside the cell.
- The cell body or soma includes the nucleus, which is highly condensed in rod PR cells, but is larger in cones and includes patches of heterochromatin (Figure 1e). To increase the density of rod and cone OSs in the retina, the somas are stacked in columns within the outer nuclear layer (ONL). This arrangement necessitates thin cell extensions reaching from the soma to the IS or to the synapse. PR cell loss is measured by counting ONL nuclei, which are prominently stained in retinal sections (Figure 1a), or in the case of rods, which are more abundant than cones, by measuring ONL thickness from micrographs or by OCT.
- The PR cell terminus contains ribbon synapses close to the presynaptic membrane loaded with vesicles containing the excitatory neurotransmitter glutamate (Figure 1f). In the dark, a steady-state level of glutamate is released at the synapse, which is reduced when the cells are hyperpolarized in the light. Changes in glutamate levels at the synapse signal postsynaptic secondary neurons in the inner nuclear layer, which communicate with ganglion cells on the vitreal surface of the retina that connect through long axons to the visual cortex of the brain.
2.2. Neighboring Cells
2.3. Inherited Diseases that Cause PR Cell Loss
3. Methods
3.1. Public Database and Literature Searches
3.2. Search Strategy
3.3. Comparative Analysis and Updating the MGI Database
3.4. Inclusion/Exclusion Criteria
3.5. Heterogeneity of Data
3.6. Comparison of Progressive PR Cell Loss
3.7. Generation of Primary Data Using Fundus Imaging and OCT Scans
4. Results
4.1. Summary of Studies that Report PR Cell Loss
4.1.1. PR Cell Loss Models
4.1.2. Mouse Models from Phenotyping Programs
5. Analysis
5.1. Progression of PR Cell Loss
5.2. Biological Processes Affected by Mutations
5.2.1. Category 01: Ciliary Function and Trafficking
5.2.2. Category 02: Visual Transduction
5.2.3. Category 03: Metabolism
5.2.4. Category 04: Visual Cycle and Retinoids
5.2.5. Category 05: Synapse
5.2.6. Category 06: Channels and Transporters
5.2.7. Category 07: Adhesion and Cytoskeletal
5.2.8. Category 08: Signaling
5.2.9. Category 09: Transcription Factors
5.2.10. Category 10: DNA Repair, RNA Biogenesis, and Protein Modification
5.2.11. Category 11: Immune Response
5.3. Omitted Models with PR Abnormalities that May be of Interest
5.4. Factors Leading to Phenotypic Variability
5.4.1. Effects of Allelic Heterogeneity
5.4.2. Effects of Genetic Interactions
5.4.3. Effects of Environment on PR Degeneration
5.5. Relationship to Human Disease Genes
6. Discussion
6.1. Variability in Measuring PR Cell Loss
6.2. Correlation of PR Cell Loss with Gene Function
7. Conclusions
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
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Collin, G.B.; Gogna, N.; Chang, B.; Damkham, N.; Pinkney, J.; Hyde, L.F.; Stone, L.; Naggert, J.K.; Nishina, P.M.; Krebs, M.P. Mouse Models of Inherited Retinal Degeneration with Photoreceptor Cell Loss. Cells 2020, 9, 931. https://doi.org/10.3390/cells9040931
Collin GB, Gogna N, Chang B, Damkham N, Pinkney J, Hyde LF, Stone L, Naggert JK, Nishina PM, Krebs MP. Mouse Models of Inherited Retinal Degeneration with Photoreceptor Cell Loss. Cells. 2020; 9(4):931. https://doi.org/10.3390/cells9040931
Chicago/Turabian StyleCollin, Gayle B., Navdeep Gogna, Bo Chang, Nattaya Damkham, Jai Pinkney, Lillian F. Hyde, Lisa Stone, Jürgen K. Naggert, Patsy M. Nishina, and Mark P. Krebs. 2020. "Mouse Models of Inherited Retinal Degeneration with Photoreceptor Cell Loss" Cells 9, no. 4: 931. https://doi.org/10.3390/cells9040931