Early changes in synaptic connectivity following progressive photoreceptor degeneration in RCS rats

European Journal of Neuroscience

Volumn 22, Issue 5, 2005, Pages 1057-1072

  Cuenca, Nicolás ^a,b   Pinilla, Isabel ^a,c   Sauvé, Yves ^a   Lund, Raymond ^a  

^a UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF ALICANTE   (Spain)

^c HOSPITAL UNIVERSITARIO MIGUEL SERVET   (Spain)

Author keywords

Bipolar; Horizontal; Outer plexiform layer; Photoreceptor; Retinal degeneration

Indexed keywords

ANTIBODY; ANTIGEN; BASSOON ANTIGEN; CALBIDIN ANTIGEN; METABOTROPIC RECEPTOR 6; PARVALBUMIN; PROTEIN GAMMA TRANSDUCIN; PROTEIN KINASE C ALPHA; RECOVERIN; SYNAPTOPHYSIN; TRANSDUCIN; UNCLASSIFIED DRUG;

A WAVE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; B WAVE; CONTROLLED STUDY; DISEASE COURSE; ELECTRORETINOGRAM; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; NERVE CELL DEGENERATION; NONHUMAN; PHOTORECEPTOR; PHOTORECEPTOR CELL; POSTSYNAPTIC MEMBRANE; PRESYNAPTIC NERVE; PRIORITY JOURNAL; RAT; RETINA; RETINA BIPOLAR GANGLION CELL; RETINA CONE; RETINA DEGENERATION; RETINA ROD; SYNAPTIC TRANSMISSION;

AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; CONES (RETINA); DISEASE MODELS, ANIMAL; ELECTRORETINOGRAPHY; IMMUNOHISTOCHEMISTRY; NERVE TISSUE PROTEINS; PHOTORECEPTORS; RATS; RATS, MUTANT STRAINS; RECEPTORS, METABOTROPIC GLUTAMATE; RETINAL DEGENERATION; SYNAPSES; SYNAPTOPHYSIN; TRANSDUCIN;

EID: 25844524933     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2005.04300.x     Document Type: Article

References (40)

1. Al-Maghtheh, M., Gregory, C., Inglehearn, C., Hardcastle, A. & Bhattacharya, S. (1993) Rhodopsin mutations in autosomal dominant retinitis pigmentosa. Hum. Mutat., 2, 249-255.
2. Bourne, M.C., Campbell, D.A. & Tansley, K. (1938) Hereditary degeneration of the rat retina. Br. J. Ophthalmol., 122, 613-623.
3. Chu, Y., Humphrey, M.F. & Constable, I.J. (1993) Horizontal cells of the normal and dystrophic rat retina: a wholemount study using immunolabelling for the 28-kDa calcium-binding protein. Exp. Eye Res., 57, 141-148.
4. Claes, E., Seeliger, M., Michalakis, S., Biel, M., Humphries, P. & Haverkamp, S. (2004) Morphological characterization of the retina of the CNGA3 (-/-) Rho (-/-) mutant mouse lacking functional cones and rods. Invest. Ophthalmol. Vis. Sci., 45, 2039-2048.
5. Cuenca, N., Pinilla, I., Sauve, Y., Lu, B., Wang, S. & Lund, R.D. (2004) Regressive and reactive changes in the connectivity patterns of rod and cone pathways of P23H transgenic rat retina. Neuroscience, 127, 301-317.
6. D'Cruz, P.M., Yasumura, D., Weir, J., Matthes, M.T., Abderrahim, H., LaVail, M.M. & Vollrath, D. (2000) Mutation of the receptor tyrosine kinase gene (Mertk) in the retinal dystrophic RCS rat. Hum. Mol. Genet., 9, 645-651.
7. Davidorf, F.H., Mendlovic, D.B., Bowyer, D.W., Gresak, P.M., Foreman, B.C., Werling, K.T. & Chambers, R.B. (1991) Pathogenesis of retinal dystrophy in the Royal College of Surgeons rat. Ann. Ophthalmol., 23, 87-94.
8. Dick, O., tom Dieck, S., Altrock, W.D., Ammermuller, J., Weiler, R., Garner, C.C., Gundelfinger, E.D. & Brandstatter, J.H. (2003) The presynaptic active zone protein bassoon is essential for photoreceptor ribbon synapse formation in the retina. Neuron, 37, 775-786.
9. Dowling, J.E. & Sidman, R.L. (1962) Inherited retinal dystrophy in the rat. J. Cell Biol., 14, 73-109.
10. Eisenfeld, A.J., LaVail, M.M. & LaVail, J.H. (1984) Assessment of possible transneuronal changes in the retina of rats with inherited retinal dystrophy: cell size, number, synapses, and axonal transport by retinal ganglion cells. J. Comp. Neurol., 223, 22-34.
11. Fariss, R.N., Li, Z.Y. & Milam, A.H. (2000) Abnormalities in rod photoreceptors, amacrine cells, and horizontal cells in human retinas with retinitis pigmentosa. Am. J. Ophthalmol., 129, 215-223.
12. Gal, A., Li, Y., Thompson, D.A., Weir, J., Orth, U., Jacobson, S.G., Apfelstedt-Sylla, E. & Vollrath, D. (2000) Mutations in MERTK, the human orthologue of the RCS rat retinal dystrophy gene, cause retinitis pigmentosa. Nature Genet., 26, 270-271.
13. Jansen, H.G. & Sanyal, S. (1987) Synaptic changes in the terminals of rod photoreceptors of albino mice after partial visual cell loss induced by brief exposure to constant light. Cell Tissue Res., 250, 43-52.
14. Jansen, H.G. & Sanyal, S. (1984) Development and degeneration of retina in rds mutant mice: electron microscopy. J. Comp. Neurol., 224, 71-84.
15. Kajiwara, K., Berson, E.L. & Dryja, T.P. (1994) Digenic retinitis pigmentosa due to mutations at the unlinked peripherin/RDS and ROM1 loci. Science, 264, 1604-1608.
16. Kwan, A.S.L., Wang, S. & Lund, R.D. (1999) Photoreceptor layer reconstruction in rodent model of retinal degeneration. Exp. Neurol., 159, 21-33.
17. LaVail, M.M. (2001) Legacy of the RCS rat: impact of a seminal study on retinal cell biology and retinal degenerative diseases. Prog. Brain Res., 131, 617-627.
18. LaVail, M.M. & Battelle, B.A. (1975) Influence of eye pigmentation and light deprivation on inherited retinal dystrophy in the rat. Exp. Eye Res., 21, 167-192.
19. Lewis, G.P., Linberg, K.A. & Fisher, S.K. (1998) Neurite outgrowth from bipolar and horizontal cells after experimental retinal detachment. Invest. Ophthalmol. Vis. Sci., 39, 424-434.
20. Li, L. & Turner, J.E. (1991) Optimal conditions for long-term photoreceptor cell rescue in RCS rats: the necessity for healthy RPE transplants. Exp. Eye Res., 52, 669-679.
21. Lin, N., Fan, W., Sheedlo, H.J., Aschenbrenner, J.E. & Turner, J.E. (1996) Photoreceptor repair in response to RPE transplants in RCS rats: outer segment regeneration. Curr. Eye Res., 15, 1069-1077.
22. Little, C.W., Castillo, B., DiLoreto, D.A., Cox, C., Wyatt, J., del Cerro, C. & del Cerro, M. (1996) Transplantation of human fetal retinal pigment epithelium rescues photoreceptor cells from degeneration in the Royal College of Surgeons rat retina. Invest. Ophthalmol. Vis. Sci., 37, 204-211.
23. Lu, B., Lund, R.D. & Coffey, P.J. (2001) Basal increase in c-fos-like expression in superior colliculus of RCS dystrophic rats can be abolished by intraocular injection of tetrodotoxin. Neuroscience, 107, 109-115.
24. Lund, R.D., Adamson, P., Sauve, Y., Keegan, D.J., Girman, S.V., Wang, S., Winton, H., Kanuga, N., Kwan, A.S., Beauchene, L., Zerbib, A., Hetherington, L., Couraud, P.O., Coffey, P. & Greenwood, J. (2001) Subretinal transplantation of genetically modified human cell lines attenuates loss of visual function in dystrophic rats. Proc. Natl Acad. Sci., USA, 98, 9942-9947.
25. Lund, R.D., Ono, S.J., Keegan, D.J. & Lawrence, J.M. (2003) Retinal transplantation: progress and problems in clinical application. J. Leukoc. Biol., 74, 151-160.
26. Marc, R.E., Murry, R.F., Fisher, S.K., Linberg, K.A. & Lewis, G.P. (1998) Amino acid signatures in the detached cat retina. Invest. Ophthalmol. Vis. Sci., 39, 1694-1702.
27. McGinnis, J.F., Stepanik, P.L., Chen, W., Elias, R., Cao, W. & Lerious, V. (1999) Unique retina cell phenotypes revealed by immunological analysis of recoverin expression in rat retina cells. J. Neurosci. Res., 55, 252-260.
28. McLaughlin, M.E., Ehrhart, T.L., Berson, E.L. & Dryja, T.P. (1995) Mutation spectrum of the gene encoding the b subunit of rod phosphodiesterase among patients with autosomal recessive retinitis pigmentosa. Proc. Natl Acad. Sci., USA, 92, 3249-3253.
29. Nandrot, E., Dufour, E.M., Provost, A.C., Pequignot, M.O., Bonnel, S., Gogat, K., Marchant, D., Rouillac, C., Sepulchre de Conde, B., Bihoreau, M.T., Shaver, C., Dufier, J.L., Marsac, C., Lathrop, M., Menasche, M. & Abitbol, M.M. (2000) Homozygous deletion in the coding sequence of the c-mer gene in RCS rats unravels general mechanisms of physiological cell adhesion and apoptosis. Neurobiol. Dis., 7, 586-599.
30. Nusinowitz, S., Nguyen, L., Radu, R., Kashani, Z., Farber, D. & Danciger, M. (2003) Electroretinographic evidence for altered phototransduction gain and slowed recovery from photobleaches in albino mice with a MET450 variant in RPE65. Exp. Eye Res., 77, 627-638.
31. Park, S.J., Kim, I.B., Choi, K.R., Moon, J.I., Oh, S.J., Chung, J.W. & Chun, M.H. (2001) Reorganization of horizontal cell processes in the developing FVB/N mouse retina. Cell Tissue Res., 306, 341-346.
32. Pignatelli, V., Cepko, C.L. & Strettoi, E. (2004) Inner retinal abnormalities in a mouse model of Leber's congenital amaurosis. J. Comp. Neurol., 469, 351-359.
33. Pinilla, I., Lund, R.D. & Sauvé, Y. (2005) Cone function studied with flicker electroretinogram during progressive retinal degeneration in RCS rats. Exp. Eye Res., 80, 51-59.
34. Pinilla, I., Sauvé, Y. & Lund, R.D. (2004) Contribution of rod and cone pathways to dark-adapted electroretinogram (ERG) b-wave following retinal degeneration in RCS rats. Vis. Res., 44, 2467-2474.
35. Sauvé, Y., Girman, S.V., Wang, S., Lawrence, J.M. & Lund, R.D. (2001) Progressive visual sensitivity loss in the RCS rat: perimetric study in the superior colliculus and retinal anatomy. Neuroscience, 103, 51-63.
36. Sheedlo, H.J., Li, L.X. & Turner, J.E. (1989) Functional and structural characteristics of photoreceptor cells rescued in RPE-cell grafted retinas of RCS dystrophic rats. Exp. Eye Res., 48, 841-854.
37. Stockton, R.A. & Slaughter, M.M. (1989) B-wave of the electroretinogram. A reflection of ON bipolar cell activity. J. Gen. Physiol., 93, 101-122.
38. Strettoi, E. & Pignatelli, V. (2000) Modifications of retinal neurons in a mouse model of retinitis pigmentosa. Proc. Natl Acad. Sci., USA, 97, 11020-11025.
39. Tso, M.O., Zhan, G.C., Abler, A.S., Chang, C.J., Wong, F., Chang, G.Q. & Lam, T.T. (1994) Apoptosis leads to photoreceptor degeneration in inherited retinal dystrophy of RCS rats. Invest. Ophthalmol. Vis. Sci., 35, 2693-2699.
40. Vollrath, D., Feng, W., Duncan, J.L., Yasumura, D., D'Cruz, P.M., Chappelow, A., Matthes, M.T., Kay, M.A. & LaVail, M.M. (2001) Correction of the retinal dystrophy phenotype of the RCS rat by viral gene transfer of Mertk. Proc. Natl Acad. Sci., USA, 98, 12584-12589.