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Diurnal rodents as animal models of human central vision: characterisation of the retina of the sand rat Psammomys obsesus

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Abstract

Background

Cone photoreceptor-based central vision is of paramount importance in human eyesight, and the increasing numbers of persons affected by macular degeneration emphasizes the need for relevant and amenable animal models. Although laboratory mice and rats have provided valuable information on retinal diseases, they have inherent limitations for studies on macular pathology. In the present study, we extend our recent analyses of diurnal murid rodents to demonstrate that the sand rat Psammomys obesus has a remarkably cone-rich retina, and represents a useful adjunct to available animal models of central vision.

Methods

Adult P. obesus were captured and transferred to animal facilities where they were maintained under standard light/dark cycles. Animals were euthanised and their eyes enucleated. Tissue was either fixed in paraformaldehyde and prepared for immunohistochemistry, or solubilized in lysis buffer and separated by SDS-PAGE and subjected to western blot analysis. Samples were labelled with a battery of antibodies against rod and cone photoreceptors, inner retinal neurones, and glia.

Results

P. obesus showed a high percentage of cones, 41% of total photoreceptor numbers in both central and peripheral retina. They expressed multiple cone-specific proteins, including short and medium-wavelength opsin and cone transducin. A second remarkable feature of the retina concerned the horizontal cells, which expressed high levels of glial fibrillar acidic protein and occludin, two proteins which are not seen in other species.

Conclusion

The retina of P. obesus displays high numbers of morphologically and immunologically identifiable cones which will facilitate analysis of cone pathophysiology in this species. The unusual horizontal cell phenotype may be related to the cone distribution or to an alternative facet of the animals lifestyle.

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References

  1. Jackson GR, Owsley C, Curcio CA (2002) Photoreceptor degeneration and dysfunction in aging and age-related maculopathy. Ageing Res Rev 1:381–396

    Article  PubMed  Google Scholar 

  2. Rattner A, Nathans J (2006) Macular degeneration: recent advances and therapeutic opportunities. Nat Rev Neurosci 7:860–872

    Article  PubMed  CAS  Google Scholar 

  3. Jeon CJ, Strettoi E, Masland RH (1998) The major cell populations of the mouse retina. J Neurosci 18:8936–8946

    PubMed  CAS  Google Scholar 

  4. Szel A, Rohlich P (1992) Two cone types of rat retina detected by anti-visual pigment antibodies. Exp Eye Res 55:47–52

    Article  PubMed  CAS  Google Scholar 

  5. Weng J, Mata NL, Azarian SM, Tzekov RT, Birch DG, Travis GH (1999) Insights into the function of Rim protein in photoreceptors and etiology of Stargardt's disease from the phenotype in abcr knockout mice. Cell 98:13–23

    Article  PubMed  CAS  Google Scholar 

  6. Kryger Z, Galli-Resta L, Jacobs GH, Reese BE (1998) The topography of rod and cone photoreceptors in the retina of the ground squirrel. Vis Neurosci 15:685–691

    Article  PubMed  CAS  Google Scholar 

  7. Blanks JC, Johnson LV (1984) Specific binding of peanut lectin to a class of retinal photoreceptor cells. A species comparison. Invest Ophthalmol Vis Sci 25:546–557

    PubMed  CAS  Google Scholar 

  8. Hendrickson A, Hicks D (2002) Distribution and density of medium- and short-wavelength selective cones in the domestic pig retina. Exp Eye Res 74:435–444

    Article  PubMed  CAS  Google Scholar 

  9. Bobu C, Craft CM, Masson-Pevet M, Hicks D (2006) Photoreceptor organization and rhythmic phagocytosis in the nile rat Arvicanthis ansorgei: a novel diurnal rodent model for the study of cone pathophysiology. Invest Ophthalmol Vis Sci 47:3109–3118

    Article  PubMed  Google Scholar 

  10. Boudard DL, Tanimoto N, Huber G, Beck SC, Seeliger MW, Hicks D (2010) Cone loss is delayed relative to rod loss during induced retinal degeneration in the diurnal cone-rich rodent Arvicanthis ansorgei. Neuroscience 169:1815–1830

    Article  PubMed  CAS  Google Scholar 

  11. Mehdi MK, Hicks D (2010) Structural and physiological responses to prolonged constant lighting in the cone-rich retina of Arvicanthis ansorgei. Exp Eye Res 91:793–799

    Article  Google Scholar 

  12. Vaughan DK, Fisher SK (1987) The distribution of F-actin in cells isolated from vertebrate retinas. Exp Eye Res 44:393–406

    Article  PubMed  CAS  Google Scholar 

  13. Hughes WF (1991) Quantitation of ischemic damage in the rat retina. Exp Eye Res 53:573–582

    Article  PubMed  CAS  Google Scholar 

  14. Bobu C, Lahmam M, Vuillez P, Ouarour A, Hicks D (2008) Photoreceptor organisation and phenotypic characterization in retinas of two diurnal rodent species: potential use as experimental animal models for human vision research. Vision Res 48:424–432

    Article  PubMed  CAS  Google Scholar 

  15. Heesy CP, Hall MI (2010) The nocturnal bottleneck and the evolution of mammalian vision. Brain Behav Evol 75:195–203

    Article  PubMed  Google Scholar 

  16. Schmidt-Nielsen K, Haines HB, Hackel DB (1963) Diabetes mellitus in the sand rat induced by standard laboratory diets. Science 143:689–690

    Article  Google Scholar 

  17. Nesher R, Gross DJ, Donath MY, Cerasi E, Kaiser N (1999) Interaction between genetic and dietary factors determines beta-cell function in Psammomys obesus, an animal model of type 2 diabetes. Diabetes 48:731–737

    Article  PubMed  CAS  Google Scholar 

  18. Kanety H, Moshe S, Shafrir E, Lunenfeld B, Karasik A (1994) Hyperinsulinemia induces a reversible impairment in insulin receptor function leading to diabetes in the sand rat model of non-insulin-dependent diabetes mellitus. Proc Natl Acad Sci USA 91:1853–1857

    Article  PubMed  CAS  Google Scholar 

  19. Larabi Y, Dahmani Y, Gernigon T, Nguyen-Legros J (1991) Tyrosine hydroxylase immunoreactivity in the retina of the diabetic sand rat Psammomys obesus. J Hirnforsch 32:525–531

    PubMed  CAS  Google Scholar 

  20. Wulf E, Deboben A, Bautz FA, Faulstich H, Wieland T (1979) Fluorescent phallotoxin, a tool for the visualization of cellular actin. Proc Natl Acad Sci USA 76:4498–4502

    Article  PubMed  CAS  Google Scholar 

  21. Russ PK, Davidson MK, Hoffman LH, Haselton FR (1998) Partial characterization of the human retinal endothelial cell tight and adherens junction complexes. Invest Ophthalmol Vis Sci 39:2479–2485

    PubMed  CAS  Google Scholar 

  22. Williams CD, Rizzolo LJ (1997) Remodeling of junctional complexes during the development of the outer blood-retinal barrier. Anat Rec 249:380–388

    Article  PubMed  CAS  Google Scholar 

  23. Omri S, Omri B, Savoldelli M, Jonet L, Thillaye-Goldenberg B, Thuret G, Gain P, Jeanny JC, Crisanti P, Behar-Cohen F (2010) The outer limiting membrane (OLM) revisited: clinical implications. Clin Ophthalmol 4:183–195

    PubMed  CAS  Google Scholar 

  24. Saitou M, Furuse M, Sasaki H, Schulzke JD, Fromm M, Takano H, Noda T, Tsukita S (2000) Complex phenotype of mice lacking occludin, a component of tight junction strands. Mol Biol Cell 11:4131–4142

    PubMed  CAS  Google Scholar 

  25. Chiba H, Osanai M, Murata M, Kojima T, Sawada N (2008) Transmembrane proteins of tight junctions. Biochim Biophys Acta 1778:588–600

    Article  PubMed  CAS  Google Scholar 

  26. Schnitzer J (1985) Distribution and immunoreactivity of glia in the retina of the rabbit. J Comp Neurol 240:128–142

    Article  PubMed  CAS  Google Scholar 

  27. Dräger UC (1983) Coexistence of neurofilaments and vimentin in a neurone of adult mouse retina. Nature 303:169–172

    Article  PubMed  Google Scholar 

  28. Linser PJ, Smith K, Angelides K (1985) A comparative analysis of glial and neuronal markers in the retina of fish: variable character of horizontal cells. J Comp Neurol 237:264–272

    Article  PubMed  CAS  Google Scholar 

  29. Knabe W (2000) Kuhn HJ (2000) Capillary-contacting horizontal cells in the retina of the tree shrew Tupaia belangeri belong to the mammalian type A. Cell Tissue Res 299:307–311

    PubMed  CAS  Google Scholar 

  30. Hicks D, Molday RS (1986) Differential immunogold-dextran labeling of bovine and frog rod and cone cells using monoclonal antibodies against bovine rhodopsin. Exp Eye Res 42:55–71

    Article  PubMed  CAS  Google Scholar 

  31. Zhu X, Brown B, Li A, Mears AJ, Swaroop A, Craft CM (2003) GRK1-dependent phosphorylation of S and M opsins and their binding to cone arrestin during cone phototransduction in the mouse retina. J Neurosci 23:6152–6160

    PubMed  CAS  Google Scholar 

  32. Molday RS, Hicks D, Molday L (1987) Peripherin. A rim-specific membrane protein of rod outer segment discs. Invest Ophthalmol Vis Sci 28:50–61

    PubMed  CAS  Google Scholar 

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Acknowledgements

The authors are very grateful to grant support from the Fritz Tobler Foundation, Switzerland. We wish to thank Drs. F. Béhar-Cohen and S. Omri for helpful discussions.

Conflict of interest

The authors declare that they have no financial relationships of any kind connected with the data presented in this study. The authors have full control of all primary data, and they agree to allow Graefe's Archive for Clinical and Experimental Ophthalmology to review their data upon request.

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Correspondence to David Hicks.

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Saïdi, T., Mbarek, S., Chaouacha-Chekir, R.B. et al. Diurnal rodents as animal models of human central vision: characterisation of the retina of the sand rat Psammomys obsesus . Graefes Arch Clin Exp Ophthalmol 249, 1029–1037 (2011). https://doi.org/10.1007/s00417-011-1641-9

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