Neuroprotection in the juvenile rat model of light-induced retinopathy: Evidence suggesting a role for FGF-2 and CNTF

Investigative Ophthalmology and Visual Science

Volumn 48, Issue 5, 2007, Pages 2311-2320

  Joly, Sandrine ^a   Pernet, Vincent ^a   Chemtob, Sylvain ^b   Di Polo, Adriana ^a   Lachapelle, Pierre ^a,c  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c RESEARCH INSTITUTE OF THE MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CILIARY NEUROTROPHIC FACTOR; FIBROBLAST GROWTH FACTOR 2; NEUROPROTECTIVE AGENT;

ANALYTIC METHOD; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DEATH; CONTROLLED STUDY; FEMALE; HISTOLOGY; IMMUNOHISTOCHEMISTRY; LIGHT EXPOSURE; MOLECULAR DYNAMICS; MUELLER CELL; NEUROPROTECTION; NICK END LABELING; NONHUMAN; PHOTORECEPTOR; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; RETINA; RETINOPATHY; UPREGULATION; WESTERN BLOTTING; ANIMAL; CELL PROTECTION; DISEASE MODEL; FLUORESCENCE MICROSCOPY; FLUORESCENT ANTIBODY TECHNIQUE; METABOLISM; NEWBORN; PATHOLOGY; PREGNANCY; RADIATION EXPOSURE; RADIATION INJURY; RETINA DEGENERATION; SPRAGUE DAWLEY RAT;

ANIMALS; ANIMALS, NEWBORN; BLOTTING, WESTERN; BRAIN-DERIVED NEUROTROPHIC FACTOR; CELL DEATH; CILIARY NEUROTROPHIC FACTOR; CYTOPROTECTION; DISEASE MODELS, ANIMAL; FEMALE; FIBROBLAST GROWTH FACTOR 2; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; IN SITU NICK-END LABELING; MICROSCOPY, FLUORESCENCE; NEUROPROTECTIVE AGENTS; PREGNANCY; RADIATION INJURIES, EXPERIMENTAL; RATS; RATS, SPRAGUE-DAWLEY; RETINA; RETINAL DEGENERATION; UP-REGULATION;

EID: 34250189859     PISSN: 01460404     EISSN: None     Source Type: Journal    
DOI: 10.1167/iovs.06-1205     Document Type: Article

References (68)

1. Organisciak DT, Darrow RM, Barsalou LS. Light-induced retinal degeneration. In: Levin LA, Di Polo A, eds. Ocular Neuroprotection. New York: Marcel Dekker, Inc; 2003:85-107.
2. Li F, Cao W, Anderson RE. Protection of photoreceptor cells in adult rats from light-induced degeneration by adaptation to bright cyclic light. Exp Eye Res. 2001;73:569-577.
3. Penn JS, Thum LA, Naash MI. Photoreceptor physiology in the rat is governed by the light environment. Exp Eye Res. 1989;49:205-215.
4. Marc RE, Jones BW, Watt CB, Strettoi E. Neural remodeling in retinal degeneration. Prog Retin Eye Res. 2003;22:607-655.
5. Penn JS, Thum LA. A comparison of the retinal effects of light damage and high illuminance light history. Prog Clin Biol Res. 1987;247:425-438.
6. Organisciak DT, Winkler BS. Retinal light damage: practical and theoretical considerations. Prog Retin Eye Res. 1994;13:1-29.
7. Organisciak DT, Jiang YL, Wang HM, Pickford M, Blanks JC. Retinal light damage in rats exposed to intermittent light: comparison with continuous light exposure. Invest Ophthalmol Vis Sci. 1989; 30:795-805.
8. O'Steen WK, Anderson KV, Shear CR. Photoreceptor degeneration in albino rats: dependency on age. Invest Ophthalmol. 1974;13: 334-339.
9. Noell WK, Walker VS, Kang BS, Berman S. Retinal damage by light in rats. Invest Ophthalmol. 1966;5:450-473.
10. Wenzel A, Grimm C, Samardzija M, Reme CE. Molecular mechanisms of light-induced photoreceptor apoptosis and neuroprotection for retinal degeneration. Prog Retin Eye Res. 2005;24:275-306.
11. Li F, Cao W, Anderson RE. Alleviation of constant-light-induced photoreceptor degeneration by adaptation of adult albino rat to bright cyclic light. Invest Ophthalmol Vis Sci. 2003;44:4968-4975.
12. Penn JS, Naash MI, Anderson RE. Effect of light history on retinal antioxidants and light damage susceptibility in the rat. Exp Eye Res. 1987;44:779-788.
13. O'Steen WK, Shear CR, Anderson KV. Retinal damage after prolonged exposure to visible light: a light and electron microscopic study. Am J Anat. 1972;134:5-21.
14. Grignolo A, Orzalesi N, Castellazzo R, Vittone P. Retinal damage by visible light in albino rats: an electron microscope study. Ophthalmologica. 1969;157:43-59.
15. Kuwabara T, Gorn RA. Retinal damage by visible light: an electron microscopic study. Arch Ophthalmol. 1968;79:69-78.
16. Zhang C, Lei B, Lam TT, Yang F, Sinha D, Tso MO. Neuroprotection of photoreceptors by minocycline in light-induced retinal degeneration. Invest Ophthalmol Vis Sci. 2004;45:2753-2759.
17. Joly S, Pernet V, Dorfman AL, Chemtob S, Lachapelle P. Light-induced retinopathy: comparing adult and juvenile rats. Invest Ophthalmol Vis Sci. 2006;47:3202-3212.
18. Chaum E. Retinal neuroprotection by growth factors: a mechanistic perspective. J Cell Biochem. 2003;88:57-75.
19. Okoye G, Zimmer J, Sung J, et al. Increased expression of brain-derived neurotrophic factor preserves retinal function and slows cell death from rhodopsin mutation or oxidative damage. J Neu rosci. 2003;23:4164-4172.
20. LaVail MM, Yasumura D, Matthes MT, et al. Protection of mouse photoreceptors by survival factors in retinal degenerations. Invest Ophthalmol Vis Sci. 1998;39:592-602.
21. Cayouette M, Behn D, Sendtner M, Lachapelle P, Gravel C. Intraocular gene transfer of ciliary neurotrophic factor prevents death and increases responsiveness of rod photoreceptors in the retinal degeneration slow mouse. J Neurosci. 1998;18:9282-9293.
22. Gao H, Hollyfield JG. Basic fibroblast growth factor: increased gene expression in inherited and light-induced photoreceptor degeneration. Exp Eye Res. 1996;62:181-189.
23. Faktorovich EG, Steinberg RH, Yasumura D, Matthes MT, LaVail MM. Photoreceptor degeneration in inherited retinal dystrophy delayed by basic fibroblast growth factor. Nature. 1990;347:83-86.
24. McGee Sanftner LH, Abel H, Hauswirth WW, Flannery JG. Glial cell line derived neurotrophic factor delays photoreceptor degeneration in a transgenic rat model of retinitis pigmentosa. Mol Ther. 2001;4:622-629.
25. Gauthier R, Joly S, Pernet V, Lachapelle P, Di Polo A. Brain-derived neurotrophic factor gene delivery to Müller glia preserves structure and function of light-damaged photoreceptors. Invest Ophthalmol Vis Sci. 2005;46:3383-3392.
26. Ikeda K, Tanihara H, Tatsuno T, Noguchi H, Nakayama C. Brain-derived neurotrophic factor shows a protective effect and improves recovery of the ERG b-wave response in light-damage. J Neurochem. 2003;87:290-296.
27. LaVail MM, Unoki K, Yasumura D, Matthes MT, Yancopoulos GD, Steinberg RH. Multiple growth factors, cytokines, and neurotrophins rescue photoreceptors from the damaging effects of constant light. Proc Natl Acad Sci USA. 1992;89:11249-11253.
28. Imai D, Yoneya S, Gehlbach PL, Wei LL, Mori K. Intraocular gene transfer of pigment epithelium-derived factor rescues photoreceptors from light-induced cell death. J Cell Physiol. 2005;202:570-578.
29. Cao W, Tombran-Tink J, Elias R, Sezate S, Mrazek D, McGinnis JF. In vivo protection of photoreceptors from light damage by pigment epithelium-derived factor. Invest Ophthalmol Vis Sci. 2001; 42:1646-1652.
30. Masuda K, Watanabe I, Unoki K, Ohba N, Muramatsu T. Functional Rescue of photoreceptors from the damaging effects of constant light by survival-promoting factors in the rat. Invest Ophthalmol Vis Sci. 1995;36:2142-2146.
31. Faktorovich EG, Steinberg RH, Yasumura D, Matthes MT, LaVail MM. Basic fibroblast growth factor and local injury protect photoreceptors from light damage in the rat. J Neurosci. 1992;12:3554-3567.
32. Machida S, Chaudhry P, Shinohara T, et al. Lens epithelium-derived growth factor promotes photoreceptor survival in light-damaged and RCS rats. Invest Ophthalmol Vis Sci. 2001;42:1087-1095.
33. Cao W, Li F, Steinberg RH, LaVail MM. Development of normal and injury-induced gene expression of aFGF, bFGF, CNTF, BDNF, GFAP and IGF-I in the rat retina. Exp Eye Res. 2001;72:591-604.
34. Cao W, Wen R, Li F, Lavail MM, Steinberg RH. Mechanical injury increases bFGF and CNTF mRNA expression in the mouse retina. Exp Eye Res. 1997;65:241-248.
35. Wen R, Song Y, Cheng T, et al. Injury-induced upregulation of bFGF and CNTF mRNAS in the rat retina. J Neurosci. 1995;15: 7377-7385.
36. Walsh N, Valter K, Stone J. Cellular and subcellular patterns of expression of bFGF and CNTF in the normal and light stressed adult rat retina. Exp Eye Res. 2001;72:495-501.
37. Wen R, Cheng T, Song Y, et al. Continuous exposure to bright light upregulates bFGF and CNTF expression in the rat retina. Curr Eye Res. 1998;17:494-500.
38. Gargini C, Bisti S, Demontis GC, Valter K, Stone J, Cervetto L. Electroretinogram changes associated with retinal upregulation of trophic factors: observations following optic nerve section. Neuroscience. 2004;126:775-783.
39. Valter K, Bisti S, Gargini C, et al. Time course of neurotrophic factor upregulation and retinal protection against light-induced damage after optic nerve section. Invest Ophthalmol Vis Sci. 2005;46:1748-1754.
40. Seki M, Nawa H, Fukuchi T, Abe H, Takei N. BDNF is upregulated by postnatal development and visual experience: quantitative and immunohistochemical analyses of BDNF in the rat retina. Invest Ophthalmol Vis Sci. 2003;44:3211-3218.
41. Rapp LM, Naash MI, Wiegand RD, Joel CD, Nielson JC, Anderson RE. Morphological and biochemical comparisons between retinal regions having differing Susceptibility to photoreceptor degeneration. In: Liss AR, ed. Retinal Degeneration: Experimental and Clinical Studies. New York: Springer; 1985:421-437.
42. Micheva KD, Vallee A, Beaulieu C, Herman IM, Leclerc N. beta-Actin is confined to structures having high capacity of remodelling in developing and adult rat cerebellum. Eur J Neurosci. 1998;10: 3785-3798.
43. Weinberger R, Schevzov G, Jeffrey P, Gordon K, Hill M, Gunning P. The molecular composition of neuronal microfilaments is spatially and temporally regulated. J Neurosci. 1996;16:238-252.
44. Grosche J, Grimm D, Clemens N, Reichenbach A. Retinal light damage vs. normal aging of rats: altered morphology, intermediate filament expression, and nuclear organization of Muller (glial) cells. J Hirnforsch. 1997;38:459-470.
45. Kostyk SK, D'Amore PA, Herman IM, Wagner JA. Optic nerve injury alters basic fibroblast growth factor localization in the retina and optic tract. J Neurosci. 1994;14:1441-1449.
46. Cao W, Wen R, Li F, Cheng T, Steinberg RH. Induction of basic fibroblast growth factor mRNA by basic fibroblast growth factor in Müller cells. Invest Ophthalmol Vis Sci. 1997;38:1358-1366.
47. Harada T, Harada C, Kohsaka S, et al. Microglia-Muller glia cell interactions control neurotrophic factor production during light-induced retinal degeneration. J Neurosci. 2002;22:9228-9236.
48. Zhang C, Shen JK, Lam TT, et al. Activation of microglia and chemokines in light-induced retinal degeneration. Mol Vis. 2005; 11:887-895.
49. Sapieha PS, Peltier M, Rendahl KG, Manning WC, Di Polo A. Fibroblast growth factor-2 gene delivery stimulates axon growth by adult retinal ganglion cells after acute optic nerve injury. Mol Cell Neurosci. 2003;24:656-672.
50. Valter K, van Driel D, Bisti S, Stone J. FGFR1 expression and FGFR1-FGF-2 colocalisation in rat retina: sites of FGF-2 action on rat photoreceptors. Growth Factors. 2002;20:177-188.
51. Valter K, Bisti S, Stone J. Location of CNTFRalpha on outer segments: evidence of the site of action of CNTF in rat retina. Brain Res. 2003;985:169-175.
52. Beltran WA, Rohrer H, Aguirre GD. Immunolocalization of ciliary neurotrophic factor receptor alpha (CNTFRalpha) in mammalian photoreceptor cells. Mol Vis. 2005;11:232-244.
53. Rohrer B, Korenbrot JI, LaVail MM, Reichardt LF, Xu B. Role of neurotrophin receptor TrkB in the maturation of rod photoreceptors and establishment of synaptic transmission to the inner retina. J Neurosci. 1999;19:8919-8930.
54. Orr HT, Cohen AI, Lowry OH. The distribution of taurine in the vertebrate retina. J Neurochem. 1976;26:609-611.
55. Pasantes-Morales H, Cruz C. Taurine and hypotaurine inhibit light-induced lipid peroxidation and protect rod outer segment structure. Brain Res. 1985;330:154-157.
56. Young TL, Cepko CL. A role for ligand-gated ion channels in rod photoreceptor development. Neuron. 2004;41:867-879.
57. Delyfer MN, Forster V, Neveux N, Picaud S, Leveillard T, Sahel JA. Evidence for glutamate-mediated excitotoxic mechanisms during photoreceptor degeneration in the rd1 mouse retina. Mol Vis. 2005;11:688-696.
58. Lima L, Obregon F, Rousso T, Quintal M, Benzo Z, Auladell C. Content and concentration of taurine, hypotaurine, and zinc in the retina, the hippocampus, and the dentate gyrus of the rat at various postnatal days. Neurochem Res. 2004;29:247-255.
59. Lima L. Taurine and its trophic effects in the retina. Neurochem Res. 1999;24:1333-1338.
60. Militante JD, Lombardini JB. Taurine: evidence of physiological function in the retina. Nutr Neurosci. 2002;5:75-90.
61. Saransaari P, Oja SS. Taurine and neural cell damage. Amino Acids. 2000;19:509-526.
62. Gordon WC, Casey DM, Lukiw WJ, Bazan NG. DNA damage and repair in light-induced photoreceptor degeneration. Invest Ophthalmol Vis Sci. 2002;43:3511-3521.
63. Rapp LM, Williams TP. A parametric study of retinal light damage in albino and pigmented rats. In: Williams TP, Baker BN, eds. The Effects of Constant Light on Visual Processes. New York: Plenum Press; 1980;135-159.
64. LaVail MM, Matthes MT, Yasumura D, Steinberg RH. Variability in rate of cone degeneration in the retinal degeneration (rd/rd) mouse. Exp Eye Res. 1997;65:45-50.
65. Szel A, Rohlich P, Caffe AR, Juliusson B, Aguirre G, Van Veen T. Unique topographic separation of two spectral classes of cones in the mouse retina. J Comp Neurol. 1992;325:327-342.
66. Birch DG, Jacobs GH. Light-induced damage to photopic and scotopic mechanisms in the rat depends on rearing conditions. Exp Neurol. 1980;68:269-283.
67. Cicerone CM. Cones survive rods in the light-damaged eye of the albino rat. Science. 1976;194:1183-1185.
68. LaVail MM. Survival of some photoreceptor cells in albino rats following long-term exposure to continuous light. Invest Ophthalmol. 1976;15:64-70.