e-book An Ancient History of Dogs: Spaniels through the Ages

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An Ancient History of Dogs: Spaniels Through the Ages

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Curated by editor P. A variation in retinal thickness is observed and some areas with a single row of photoreceptor nuclei that are still present. Ultrastructure of nontapetal a and tapetal retina b from the same dog shown in Figure 4.

A brief history of dogs - David Ian Howe

Note the severely disorganized outer and inner retinal cell layers and structures. The RPE cell layer appears preserved, however. In b there is relative sparing of the retina with some minor remnants of photoreceptor nuclei with inner segments arrow and an abundance of RPE apical microvilli. RPE: retinal pigment epithelial cells, T: tapetal cells. Bar depicts magnification which is the same for a and b. The retinas of the second dog, 6-years-old, showed signs of bilateral generalized retinal degeneration, with complete atrophy of the inferior retina, and a lack of photoreceptor cells in this area, while in the superior retina layers of photoreceptor nuclei could be observed.

The 3-year-old dog, however, demonstrated mainly normal retinal morphology except for changes in the photoreceptor cell layer at all retinal locations examined: cone cell nuclei appeared slightly abnormal, with dense chromatin and with photoreceptor inner segments condensed and shrunken Figure 6.

English Springer Spaniel

Photoreceptor outer segments could not be clearly visualized in the thin sections obtained, and thus their ultrastructure was not possible to fully evaluate. Ultrastructure of the outer retina of a normal 2-year-old dog a and that of the affected 3-year-old dog b. Note the condensed configuration of the cone nuclei in the retina of the affected animal arrow in comparison to that of the normal one in a , arrow and the dark appearance of the inner segments in the retina of the affected animal.

The present study indicates that a majority of the American ESS dogs with hereditary retinal degeneration can be associated with homozygosity for the disease causing allele of the RPGRIP1 gene. However, four of the 6 dogs homozygous for the RPGRIP1 mutation had clinical signs of disease while 2 were completely normal appearing both by ophthalmoscopic examination and by ERG.

Thus, a clear genotype-phenotype discordance was observed in regards to this group of ESS dogs.


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The reason for the latter finding is unclear. It appears likely that additional factors are warranted for initiation of photoreceptor cell death such as additional loci involved as modifiers of the disease, as have been described for various forms of PRA, for example, prcd and X-linked PRA [ 9 , 31 ]. It could possibly also be that there is not full penetrance for the mutation [ 32 ].

Similar findings have been observed in comparable human clinical studies in cone rod dystrophies and degenerations. A phenotypic variation between clinical signs in affected individuals and in the onset of hereditary retinal dystrophies has been observed, also by functional testing in human cone rod dystrophies [ 33 ]. The variation in clinical signs and time for initial symptoms is especially true for retinopathies caused by the RPGRIP1 mutation, on a variable genetic background, such as is the case in the human population.

In purebred dogs, however, a more uniform phenotype is usually expressed, due to a more homogenous background. This fact is true for most forms of PRA; however, for the cone-rod dystrophies observed in the longhaired and shorthaired Dachshund breeds, with the RPGRIP1 and NPHP4 mutations, respectively, severe heterogeneity has been described for both [ 22 , 27 , 34 ]. In retinal degeneration of the ESS dog clinical signs most often appear comparably late in life and are often difficult to evaluate by the owner.

For most of the affected dogs observed in the present study the owners had not noted any visual impairment. The owner of an year-old dog from the present study described that the dog could still play with a transparent frisbee and could easily walk down an indoor stairway in low-lighting conditions. This dog had moderately advanced retinal degeneration with ophthalmoscopically visible changes and was homozygous for the RPGRIP1 mutation.

Another dog showing clinical signs of retinal degeneration had been diagnosed as ophthalmoscopically normal by a veterinary ophthalmologist one year previously, at the age of 7 years. ERGs showed, however, severely reduced retinal function in accordance with a cone rod dystrophy. It is likely that the cone affection in the disease is early onset, and a defect the dog learns to live with as long as its rod function is normal.

Morphology of one 3-year-old ESS dog, homozygous for the RPGRIP1 mutation, showed ultrastructural changes specifically in cones, while rod photoreceptors were still normal appearing. It is possible that the visual problems become apparent clinically later in life when also the rods start to degenerate. Further, this second phase appears to occur at a variable time point, but most often not until late in life, then leading to a rather fast generalized severe retinal degeneration retinal atrophy.

ERG recordings proved to be useful in the masked study of the present investigation for objectively detecting reduced photoreceptor function in accordance with cone rod dystrophy due to the RPGRIP1 mutation. In two cases, however, function in genetically affected individuals was found to be within normal limits. These discordant clinical results could be consistent with incomplete penetrance for the mutation, but other factors previously outlined may also be involved. This could also be a candidate gene since it is known to affect the English and American Cocker Spaniel dog breeds, distant relatives to the ESS dog Liz Hansen, personal communication Four were found to be heterozygous and four were homozygous for the normal wild-type allele Table 1.

Although the number of cases is small there appears to be a tendency for a later onset of PRA among the other eight cases. None of the normal dogs were found to be homozygous for the RPGRIP1 insertion in the Swedish samples, but to make any inferences about the penetrance, a much larger data set would be needed. Taken together, the study of the Swedish samples suggests that at least one more gene is responsible for PRA in the Swedish population. There are strong indications that the RPGRIP1 gene is involved in the cone rod dystrophy described herein, but the genotype-phenotype discordance observed shows that the genetic background most probably is more complex than previously suspected.

In conclusion, there are strong indications that other mutations or modulating genes may be involved in cone rod dystrophy of ESS dogs and could also be causative to other types of hereditary retinal degenerations in the breed.

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Further investigations in regards to additional loci or genes required for development of cord1 are therefore warranted. An important goal for vision research is to provide effective treatments for the millions of people affected with retinal blinding disorders. Therapeutic intervention using large animal models such as dogs and cats are effective and necessary methods to utilize before proceeding with human treatment trials.

Proof of principle was obtained through therapeutic studies using gene therapy in a dog model of LCA [ 45 ], resulting in successful restoration of vision. Similar procedures were performed in human patients with successful outcome [ 46 , 47 ]. Another promising therapeutic method for retinal blinding disease is stem cell therapy, with or without combination of gene therapy [ 48 ].

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In preparation for such studies it is, however, of utmost importance that the animal model with its specific retinal disease is precisely characterized clinically beforehand, and with molecular methods, for maximal outcome in the translational process. The authors would like to thank the breeders and owners of English Springer Spaniel dogs for participation in eye examinations with their dogs, which made this study possible. Gary S. National Center for Biotechnology Information , U. Journal List Stem Cells Int v.

Stem Cells Int. Published online Feb Madsen , 5 and Tomas F. Richard W. Tomas F. Author information Article notes Copyright and License information Disclaimer. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract Intensive breeding and selection on desired traits have produced high rates of inherited diseases in dogs. Introduction The domestic dog has a unique population history with bottlenecks that has shaped the diversity and structure of the canine genome.

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Materials and Methods 2. Open in a separate window. Table 2 Details in regards to dogs in the masked ERG study.


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  • Figure 1. Morphology Upon the owner's request due to unrelated medical problems, three American ESS dogs were euthanized and the eye tissue made available for the present study. Results 3. Figure 2. Figure 3. Morphology Light and electron microscopies were performed using retinal sections from 3 dogs. Figure 4. Figure 5. Figure 6. Discussion The present study indicates that a majority of the American ESS dogs with hereditary retinal degeneration can be associated with homozygosity for the disease causing allele of the RPGRIP1 gene.

    Acknowledgments The authors would like to thank the breeders and owners of English Springer Spaniel dogs for participation in eye examinations with their dogs, which made this study possible. References 1.


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    Genome sequence, comparative analysis and haplotype structure of the domestic dog. Genetic evidence for an East Asian origin of domestic dogs. Genome-wide SNP and haplotype analyses reveal a rich history underlying dog domestication. Efficient mapping of mendelian traits in dogs through genome-wide association. Nature Genetics.