Early remodeling in an inducible animal model of retinal degeneration

Neuroscience

Volumn 160, Issue 2, 2009, Pages 517-529

  Nagar, S ^a   Krishnamoorthy, V ^a   Cherukuri, P ^a   Jain, V ^a   Dhingra, N K ^a  

^a NATIONAL BRAIN RESEARCH CENTRE   (India)

Author keywords

MNU; mouse; N methyl N nitrosourea; photoreceptor degeneration; retinal remodeling

Indexed keywords

CALBINDIN; GLIAL FIBRILLARY ACIDIC PROTEIN; METHYLNITROSOUREA; POSTSYNAPTIC DENSITY PROTEIN 95; PROTEIN KINASE C ALPHA; SYNAPTOPHYSIN; TUBULIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; IMMUNOBLOTTING; IMMUNOCYTOCHEMISTRY; IMMUNOLOCALIZATION; IMMUNOREACTIVITY; MOUSE; MUELLER CELL; NEUROFILAMENT; NONHUMAN; PHOTORECEPTOR; PRIORITY JOURNAL; RETINA CONE; RETINA DEGENERATION; RETINA GANGLION CELL; RETINA NERVE CELL; RETINA ROD; VISION;

ALKYLATING AGENTS; ANIMALS; DISEASE MODELS, ANIMAL; IMMUNOHISTOCHEMISTRY; MALE; METHYLNITROSOUREA; MICE; MICE, INBRED C57BL; NERVE DEGENERATION; NERVE REGENERATION; NEURONAL PLASTICITY; PHOTORECEPTOR CELLS, VERTEBRATE; RETINA; RETINAL DEGENERATION; SPATIAL BEHAVIOR; VISUAL ACUITY;

EID: 64049097877     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2009.02.056     Document Type: Article

References (72)

1. Banin E., Cideciyan A.V., Aleman T.S., Petters R.M., Wong F., Milam A.H., and Jacobson S.G. Retinal rod photoreceptor-specific gene mutation perturbs cone pathway development. Neuron 23 (1999) 549-557
2. Barhoum R., Martínez-Navarrete G., Corrochano S., Germain F., Fernandez-Sanchez L., de La Rosa E.J., de La Villa P., and Cuenca N. Functional and structural modifications during retinal degeneration in the rd10 mouse. Neuroscience 155 (2008) 698-713
3. Blanks J.C., Johnson L.V., and Hageman G.S. Stage-specific binding of peanut agglutinin to aggregates of degenerating photoreceptor cells in the rd mouse retina. Exp Eye Res 57 (1993) 265-273
4. Brandstätter J.H., Fletcher E.L., Garner C.C., Gundelfinger E.D., and Wässle H. Differential expression of the presynaptic cytomatrix protein bassoon among ribbon synapses in the mammalian retina. Eur J Neurosci 11 (1999) 3683-3693
5. Chen J., and Nathans J. Genetic ablation of cone photoreceptors eliminates retinal folds in the retinal degeneration 7 (rd7) mouse. Invest Ophthalmol Vis Sci 48 (2007) 2799-2805
6. Coffey P.J., Girman S., Wang S.M., Hetherington L., Keegan D.J., Adamson P., Greenwood J., and Lund R.D. Long-term preservation of cortically dependent visual function in RCS rats by transplantation. Nat Neurosci 5 (2002) 53-56
7. Coombs J., van der List D., Wang G.Y., and Chalupa L.M. Morphological properties of mouse retinal ganglion cells. Neuroscience 140 (2006) 123-136
8. Crawley J.N. Behavioral phenotyping of transgenic and knockout mice: experimental design and evaluation of general health, sensory functions, motor abilities, and specific behavioral tests. Brain Res 835 (1999) 18-26
9. Cuenca N., Pinilla I., Sauvé Y., and Lund R. Early changes in synaptic connectivity following progressive photoreceptor degeneration in RCS rats. Eur J Neurosci 22 (2005) 1057-1072
10. Dhingra N.K., Ramamohan Y., and Raju T.R. Developmental expression of synaptophysin, synapsin-I and syntaxin in the rat retina. Dev Brain Res 102 (1997) 267-273
11. Dhingra N.K., and Smith R.G. Spike generator limits efficiency of information transfer in a retinal ganglion cell. J Neurosci 24 (2004) 2914-2922
12. Dhingra N.K., Cherukuri P., Krishnamoorthy V., Baloni S., and Jose S.K. Morphological and behavioral characterization of N-methyl N-nitrosourea-induced mouse model of retinal degeneration. Soc Neurosci Abstr 699 (2007) 19/S19
13. Fariss R.N., Li Z.Y., and Milam A.H. Abnormalities in rod photoreceptors, amacrine cells, and horizontal cells in human retinas with retinitis pigmentosa. Am J Ophthalmol 129 (2000) 215-223
14. Fisher S.K., and Lewis G.P. Müller cell neuronal remodeling in retinal detachment and reattachment and their potential consequences for visual recovery: a review and reconsideration of recent data. Vis Res 43 (2003) 887-897
15. Fox M.W. The visual cliff test for the study of visual depth perception in the mouse. Anim Behav 13 (1965) 232-233
16. Gargini C., Terzibasi E., Mazzoni F., and Strettoi E. Retinal organization in the retinal degeneration 10 (rd10) mutant mouse: A morphological and ERG study. J Comp Neurol 500 (2007) 222-238
17. Hafezi F., Grimm C., Simmen B.C., Wenzel A., and Remé C.E. Molecular ophthalmology: an update on animal models for retinal degenerations and dystrophies. Br J Ophthalmol 84 (2000) 922-927
18. Hara A., Niwa M., Aoki H., Kumada M., Kunisada T., Oyama T., Yamamoto T., Kozawa O., and Mori H. A new model of retinal photoreceptor cell degeneration induced by a chemical hypoxia-mimicking agent, cobalt chloride. Brain Res 1109 (2006) 192-200
19. Hartong D.T., Berson E.L., and Dryja T.P. Retinitis pigmentosa. Lancet 368 (2006) 1795-1809
20. Haverkamp S., and Wässle H. Immunocytochemical analysis of the mouse retina. J Comp Neurol 424 (2000) 1-23
21. Haverkamp S., Ghosh S.K., Hirano A.A., and Wässle H. Immunocytochemical description of five bipolar cell types of the mouse retina. J Comp Neurol 455 (2003) 463-476
22. Herrold K.M. Pigmentary degeneration of the retina induced by N-methyl-N-nitrosourea. An experimental study in Syrian hamsters. Arch Ophthalmol 78 (1967) 650-653
23. Humayun M.S., de Juan Jr. E., Dagnelie G., Greenberg R.J., Propst R.H., and Phillips D.H. Visual perception elicited by electrical stimulation of retina in blind humans. Arch Ophthalmol 114 (1996) 40-46
24. Huxlin K.R., Dreher Z., Schulz M., and Dreher B. Glial reactivity in the retina of adult rats. Glia 15 (1995) 105-118
25. Johnson L.V., Hageman G.S., and Blanks J.C. Interphotoreceptor matrix domains ensheath vertebrate cone photoreceptor cells. Invest Ophthalmol Vis Sci 27 (1986) 129-135
26. Jones B.W., Watt C.B., Frederick J.M., Baehr W., Chen C.K., Levine E.M., Milam A.H., LaVail M.M., and Marc R.E. Retinal remodeling triggered by photoreceptor degenerations. J Comp Neurol 464 (2003) 1-16
27. Jones B.W., and Marc R.E. Retinal remodeling during degeneration. Exp Eye Res 81 (2005) 123-137
28. Kiuchi K., Yoshizawa K., Shikata N., Moriguchi K., and Tsubura A. Morphologic characteristics of retinal degeneration induced by sodium iodate in mice. Curr Eye Res 25 (2002) 373-379
29. Kiuchi K., Kondo M., Ueno S., Moriguchi K., Yoshizawa K., Miyake Y., Matsumura M., and Tsubura A. Functional rescue of N-methyl-N-nitrosourea-induced retinopathy by nicotinamide in Sprague-Dawley rats. Curr Eye Res 26 (2003) 355-362
30. Krishnamoorthy V., Jain V., Cherukuri P., Baloni S., and Dhingra N.K. Intravitreal injection of fluorochrome-conjugated peanut agglutinin results in specific and reversible labeling of mammalian cones in vivo. Invest Ophthalmol Vis Sci 49 (2008) 2643-2650
31. Li Z.Y., Kljavin I.J., and Milam A.H. Rod photoreceptor neurite sprouting in retinitis pigmentosa. J Neurosci 15 (1995) 5429-5438
32. Liang L., Katagiri Y., Franco L.M., Yamauchi Y., Enzmann V., Kaplan H.J., and Sandell J.H. Long-term cellular and regional specificity of the photoreceptor toxin, iodoacetic acid (IAA), in the rabbit retina. Vis Neurosci 25 (2008) 167-177
33. Linberg K.A., Lewis G.P., Matsumoto B., and Fisher S.K. Immunocytochemical evidence that rod connected horizontal cell axon terminals remodel in response to experimental retinal detachment in the cat. Mol Vis 12 (2006) 1674-1686
34. MacLaren R.E., Pearson R.A., MacNeil A., Douglas R.H., Salt T.E., Akimoto M., Swaroop A., Sowden J.C., and Ali R.R. Retinal repair by transplantation of photoreceptor precursors. Nature 444 (2006) 203-207
35. Maeda H., Ogata N., Yi X., Takeuchi M., Ohkuma H., and Uyama M. Apoptosis of photoreceptor cells in ornithine-induced retinopathy. Graefes Arch Clin Exp Ophthalmol 236 (1998) 207-212
36. Marc R.E., Jones B.W., Watt C.B., and Strettoi E. Neural remodeling in retinal degeneration. Prog Retin Eye Res 22 (2003) 607-655
37. Marc R.E., Jones B.W., Watt C.B., Vazquez-Chona F., Vaughan D.K., and Organisciak D.T. Extreme retinal remodeling triggered by light damage: implications for age related macular degeneration. Mol Vis 14 (2008) 782-806
38. Marcus R.C., and Easter Jr. S.S. Expression of glial fibrillary acidic protein and its relation to tract formation in embryonic zebrafish (Danio rerio). J Comp Neurol 359 (1995) 365-381
39. Margalit E., and Sadda S.R. Retinal and optic nerve diseases. Artif Organs 27 (2003) 963-974
40. Margolis D.J., Newkirk G., Euler T., and Detwiler P.B. Functional stability of retinal ganglion cells after degeneration-induced changes in synaptic input. J Neurosci 28 (2008) 6526-6536
41. Meyer J.S., Katz M.L., Maruniak J.A., and Kirk M.D. Embryonic stem cell-derived neural progenitors incorporate into degenerating retina and enhance survival of host photoreceptors. Stem Cells 24 (2006) 274-283
42. Miki K., Uehara N., Shikata N., Matsumura M., and Tsubura A. Poly (ADP-ribose) polymerase inhibitor 3-aminobenzamide rescues N-methyl-N-nitrosourea-induced photoreceptor cell apoptosis in Sprague-Dawley rats through preservation of nuclear factor-κB activity. Exp Eye Res 84 (2007) 285-292
43. Milam A.H., Dacey D.M., and Dizhoor A.M. Recoverin immunoreactivity in mammalian cone bipolar cells. Vis Neurosci 10 (1993) 1-12
44. Milam A.H., Li Z.Y., and Fariss R.N. Histopathology of the human retina in retinitis pigmentosa. Prog Ret Eye Res 17 (1998) 175-205
45. Molday R.S., and MacKenzie D. Monoclonal antibodies to rhodopsin: characterization, cross-reactivity, and application as structural probes. Biochemistry 22 (1983) 653-660
46. Moriguchi K., Yuri T., Yoshizawa K., Kiuchi K., Takada H., Inoue Y., Hada T., Matsumura M., and Tsubura A. Dietary docosahexaenoic acid protects against N-methyl-N-nitrosourea-induced retinal degeneration in rats. Exp Eye Res 77 (2003) 167-173
47. Nakajima M., Nambu H., Shikata N., Senzaki H., Miki H., and Tsubura A. Pigmentary degeneration induced by N-methyl-N-nitrosourea and the fate of pigment epithelial cells in the rat retina. Pathol Int 46 (1996) 874-882
48. 57BL mice. Pathol Int 47 (1997) 377-383
49. Nambu H., Taomoto M., Ogura E., and Tsubura A. Time-specific action N-methyl-N-nitrosourea in the occurrence of retinal dysplasia and retinal degeneration in neonatal mice. Pathol Int 48 (1998) 199-205
50. Newcombe J., Woodroofe M.N., and Cuzner M.L. Distribution of glial fibrillary acidic protein in gliosed human white matter. J Neurochem 47 (1986) 1713-1719
51. Nixon R.A., Paskevich P.A., Sihag R.K., and Thayer C.Y. Phosphorylation on carboxyl terminus domains of neurofilament proteins in retinal ganglion cell neurons in vivo: influences on regional neurofilament accumulation, interneurofilament spacing, and axon caliber. J Cell Biol 126 (1994) 1031-1046
52. Noëll W.K., Walker V.S., Kang B.S., and Berman S. Retinal damage by light in rats. Invest Ophthalmol Vis Sci 5 (1966) 450-473
53. Ogino H., Ito M., Matsumoto K., Yagyu S., Tsuda H., Hirono I., Wild C.P., and Montesano R. Retinal degeneration induced by N-methyl-N-nitrosourea and detection of 7-methyldeoxyguanosine in the rat retina. Toxicol Pathol 21 (1993) 21-25
54. Park S.J., Kim I.B., Choi K.R., Moon J.I., Oh S.J., Chung J.W., and Chun M.H. Reorganization of horizontal cell processes in the developing FVB/N mouse retina. Cell Tissue Res 306 (2001) 341-346
55. Peichl L., and Bolz J. Kainic acid induces sprouting of retinal neurons. Science 223 (1984) 503-504
56. Peichl L., and Gonzalez-Soriano J. Morphological types of horizontal cell in rodent retinae: a comparison of rat, mouse, gerbil, and guinea pig. Vis Neurosci 11 (1994) 501-517
57. Pignatelli V., Cepko C.L., and Strettoi E. Inner retinal abnormalities in a mouse model of Leber's congenital amaurosis. J Comp Neurol 469 (2004) 351-359
58. Robinson G.A., and Madison R.D. Axotomized mouse retinal ganglion cells containing melanopsin show enhanced survival, but not enhanced axon regrowth into a peripheral nerve graft. Vis Res 44 (2004) 2667-2674
59. Santos A., Humayun M.S., de Juan Jr. E., Greenberg R.J., Marsh M.J., Klock I.B., and Milam A.H. Preservation of the inner retina in retinitis pigmentosa. A morphometric analysis. Arch Ophthalmol 115 (1997) 511-515
60. Sternberger L.A., and Sternberger N.H. Monoclonal antibodies distinguish phosphorylated and nonphosphorylated forms of neurofilaments in situ. Proc Natl Acad Sci U S A 80 (1983) 6126-6130
61. Strettoi E., and Pignatelli V. Modifications of retinal neurons in a mouse model of retinitis pigmentosa. Proc Natl Acad Sci U S A 97 (2000) 11020-11025
62. Strettoi E., Porciatti V., Falsini B., Pignatelli V., and Rossi C. Morphological and functional abnormalities in the inner retina of the rd/rd mouse. J Neurosci 22 (2002) 5492-5504
63. Strettoi E., Pignatelli V., Rossi C., Porciatti V., and Falsini B. Remodeling of second-order neurons in the retina of rd/rd mutant mice. Vis Res 43 (2003) 867-877
64. Sullivan R.K.P., Wolde Mussie E., and Pow D.V. Dendritic and synaptic plasticity of neurons in the human age-related macular degeneration retina. Invest Ophthalmol Vis Sci 48 (2007) 2782-2791
65. Taomoto M., Nambu H., Senzaki H., Shikata N., Oishi Y., Fujii T., Miki H., Uyama M., and Tsubura A. Retinal degeneration induced by N-methyl-N-nitrosourea in Syrian golden hamsters. Graefes Arch Clin Exp Ophthalmol 236 (1998) 688-695
66. Tsubura A., Yoshizawa K., Kiuchi K., and Moriguchi K. N-methyl-N-nitrosourea-induced retinal degeneration in animals. Acta Histochem Cytochem 36 (2003) 263-270
67. Uehara N., Miki K., Tsukamoto R., Matsuoka Y., and Tsubura A. Nicotinamide blocks N-methyl-N-nitrosourea-induced photoreceptor cell apoptosis in rats through poly (ADP-ribose) polymerase activity and Jun N-terminal kinase/activator protein-1 pathway inhibition. Exp Eye Res 82 (2006) 488-495
68. Wan J., Zheng H., Chen Z.L., Xiao H.L., Shen Z.J., and Zhou G.M. Preferential regeneration of photoreceptor from Müller glia after retinal degeneration in adult rat. Vis Res 48 (2008) 223-234
69. Wang Z.J., Lam K.W., Lam T.T., and Tso M.O. Iron-induced apoptosis in the photoreceptor cells of rats. Invest Ophthalmol Vis Sci 39 (1998) 631-633
70. Wasowicz M., Morice C., Ferrari P., Callebert J., and Versaux-Botteri C. Long-term effects of light damage on the retina of albino and pigmented rats. Invest Ophthalmol Vis Sci 43 (2002) 813-820
71. Yoshizawa K., Nambu H., Yang J., Oishi Y., Senzaki H., Shikata N., Miki H., and Tsubura A. Mechanisms of photoreceptor cell apoptosis induced by N-methyl-N-nitrosourea in Sprague-Dawley rats. Lab Invest 79 (1999) 1359-1367
72. Yoshizawa K., Yang J., Senzaki H., Uemura Y., Kiyozuka Y., Shikata N., Oishi Y., Miki H., and Tsubura A. Caspase-3 inhibitor rescues N-methyl-N-nitrosourea-induced retinal degeneration in Sprague-Dawley rats. Exp Eye Res 71 (2000) 629-635