Protection of mouse photoreceptors by survival factors in retinal degenerations

Investigative Ophthalmology and Visual Science

Volumn 39, Issue 3, 1998, Pages 592-602

  LaVail, Matthew M ^a,b   Yasumura, Douglas ^a,b   Matthes, Michael T ^b   Lau Villacorta, Cathy ^a,b   Unoki, Kazuhiko ^b   Sung, Ching Hwa ^c   Steinberg, Roy H ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BASIC FIBROBLAST GROWTH FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR; CILIARY NEUROTROPHIC FACTOR; LEUKEMIA INHIBITORY FACTOR; MUTANT PROTEIN; NERVE GROWTH FACTOR; NEUROTROPHIN 3; NEUROTROPHIN 4; RHODOPSIN; SOMATOMEDIN B;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EYE PROTECTION; LIGHT DAMAGE; MOUSE; NONHUMAN; PHOTORECEPTOR; PRIORITY JOURNAL; RETINA DEGENERATION; SPECIES DIFFERENCE; SURVIVAL TIME; TRANSGENIC MOUSE;

ANIMALS; DRUG COMBINATIONS; GROWTH SUBSTANCES; INJECTIONS; LIGHT; MICE; MICE, INBRED BALB C; MICE, INBRED C3H; MICE, INBRED C57BL; MICE, MUTANT STRAINS; NEUROPROTECTIVE AGENTS; PHOTORECEPTORS; RADIATION INJURIES, EXPERIMENTAL; RATS; RATS, SPRAGUE-DAWLEY; RETINAL DEGENERATION; VITREOUS BODY;

EID: 0031937530     PISSN: 01460404     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (78)

1. Lindsay RM. Trophic protection of motor neurons: clinical potential in motor neuron diseases. J Neurol. 1994;241:S8-S11.
2. Hefti F. Neurotrophic factor therapy for nervous system degenerative diseases. J Neurobiol. 1994;25:1418-1435.
3. Lindholm D. Role of neurotrophins in preventing glutamate induced neuronal cell death. J Neurol. 1994;241:S16-S18.
4. McMahon SB, Priestley JV. Peripheral neuropathies and neurotrophic factors: animal models and clinical perspectives. Curr Opin Neurobiol. 1995;5:616-624.
5. Sendtner M, Holtmann B, Hughes RA. The response of motoneurons to neurotrophins. Neurochem Res. 1996;21:831-841.
6. 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.
7. 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.
8. 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.
9. 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.
10. Berson EL, Rosner B, Sandberg MA, et al. A randomized trial of vitamin A and vitamin E supplementation for retinitis pigmentosa. Arch Ophthalmol. 1993;111:761-772.
11. Bowes C, Li T, Danciger M, Baxter LC, Applebury ML, Farber DB. Retinal degeneration in the rd mouse is caused by a defect in the β subunit of rod cGMP-phosphdiesterase. Nature. 1990;347:677-680.
12. Pittler SJ, Baehr W. Identification of a nonsense mutation in the rod photoreceptor cGMP phosphodiesterase β-subunit gene of the rd mouse. Proc Natl Acad Sci USA. 1991;88:8322-8326.
13. Carter-Dawson LD, LaVail MM, Sidman RL. Differential effect of the rd mutation on rods and cones in the mouse retina. Invest Ophthalmol Vis Sci. 1978;17:489-498.
14. McLaughlin ME, Sandberg MA, Berson EL, Dryja TP. Recessive mutations in the gene encoding the β-subunit of rod phosphodiesterase in patients with retinitis pigmentosa. Nat Genet. 1993;4: 130-134.
15. McLaughlin ME, Ehrhart TL, Berson EL, Dryja TP. Mutation spectrum of the gene encoding the beta subunit of rod phosphodiesterase among patients with autosomal recessive retinitis pigmentosa. Proc Natl Acad Sci USA. 1995;92:3249-3253.
16. Gal A, Orth U, Baehr W, Schwinger E, Rosenberg T. Heterozygous missense mutation in the rod cGMP phosphodiesterase β-subunit gene in autosomal dominant stationary night blindness. Nat Genet. 1994;7:64-68.
17. Sanyal S, De Ruiter A, Hawkins RK. Development and degeneration of retina in rds mutant mice: light microscopy. J Comp Neurol. 1980;194:193-207.
18. Travis GH, Sutcliffe JG, Bok D. The retinal degeneration slow (rds) gene product is a photoreceptor disc membrane-associated glycoprotein. Neuron. 1991;6:61-70.
19. Connell G, Bascom R, Molday L, Reid D, McInnes RR, Molday RS. Photoreceptor peripherin is the normal product of the gene responsible for retinal degeneration in the rds mouse. Proc Natl Acad Sci USA. 1991;88:723-726.
20. Sanyal S, Jansen HG. Absence of receptor segments in the retina of rds mutant mice. Neurosci Lett. 1981;21:23-26.
21. Sanyal S, Hawkins RK. Development and degeneration of retina in rds mutant mice: effects of light on the rate of degeneration in albino and pigmented homozygous and heterozygous mutant and normal mice. Vision Res. 1986;26:1177-1185.
22. Farrar GJ, Kenna P, Jordan SA, et al. A three-base-pair deletion in the peripherin-rds gene in one form of retinitis pigmentosa. Nature. 1991;354:478-480.
23. Kajiwara K, Hahn LB, Mukai S, Travis GH, Berson EL, Dryja TP. Mutations in the human retinal degeneration slow gene in autosomal dominant retinitis pigmentosa. Nature. 1991;354:480-483.
24. Kajiwara K, Sandberg MA, Berson EL, Dryja TP. A null mutation in the human peripherin/RDS gene in a family with autosomal dominant retinitis punctata albescens. Nat Genet. 1993;3:208-212.
25. Gorin MB, Jackson KE, Ferrell RE, et al. A peripherin/retinal degeneration slow mutation (Pro-210-Arg) associated with macular and peripheral retinal degeneration. Ophthalmology. 1995;102: 246-255.
26. Mullen RJ, LaVail MM. Two new types of retinal degeneration in cerebellar mutant mice. Nature. 1975;258:528-530.
27. LaVail MM. Analysis of neurological mutants with inherited retinal degeneration. Invest Ophthalmol Vis Res. 1981;21:638-657.
28. LaVail MM, Blanks JC, Mullen RJ. Retinal degeneration in the pcd cerebellar mutant mouse. I. Light microscopic and autoradio graphic analysis. J Comp Neurol. 1982;212:217-230.
29. LaVail MM, White MP, Gorrin GM, Porrello KV, Mullen RJ. Retinal degeneration in the nervous mutant mouse. I. Light microscopic cytopathology and changes in the interphotoreceptor matrix. J Comp Neurol. 1993;333:168-181.
30. Berson EL. Retinitis pigmentosa: unfolding its mystery. Proc Natl Acad Sci USA. 1996;93:4526-4528.
31. Dryja TP, Berson EL. Retinitis pigmentosa and allied diseases. Invest Ophthalmol Vis Sci. 1995;36:1197-1200.
32. Olsson JE, Gordon JW, Pawlyk BS, et al. Transgenic mice with a rhodopsin mutation (Pro23His): a mouse model of autosomal dominant retinitis pigmentosa. Neuron. 1992;9:815-830.
33. Naash MI, Hollyfield JG, Al-Ubaidi MR, Baehr W. Simulation of human autosomal dominant retinitis pigmentosa in transgenic mice expressing a mutated murine opsin gene. Proc Natl Acad Sci USA. 1993;90:5499-5503.
34. Sung C-H, Makino C, Baylor D, Nathans J. A rhodopsin gene mutation responsible for autosomal dominant retinitis pigmentosa results in a protein that is defective in localization to the photoreceptor outer segment. J Neurosci. 1994;14:5818-5833.
35. Dryja TP, McGee TL, Reichel E, et al. A point mutation of the rhodopsin gene in one form of retinitis pigmentosa. Nature. 1990; 343:364-366.
36. Sung C-H, Davenport CM, Hennessey JC, et al. Rhodopsin mutations in autosomal dominant retinitis pigmentosa. Proc Natl Acad Sci USA. 1991;88:6481-6485.
37. Silverman MS, Lett J, Valentino TL, Landgraf M, Wang X. Rescue of host cones by transplanted donor photoreceptors in the rd mouse. Invest Ophthalmol Vis Sci. 1993;34:1096.
38. Yasumura D, Matthes MT, Lau C, Unoki K, Steinberg RH, LaVail MM. Attempts to rescue photoreceptors with survival factors in mice with inherited retinal degenerations or constant light damage. [ARVO Abstract]. Invest Ophthalmol Vis Sci. 1995;36:S252.
39. LaVail MM, Yasumura D, Matthes MT, Lau-Villacorta C, Sung C-H, Steinberg RH. CNTF delays photoreceptor degeneration in rd and Q344ter mutant rhodopsin transgenic mice. [ARVO Abstract]. Invest Ophthalmol Vis Sci. 1996;37:S437.
40. LaVail MM, Battelle BA. Influence of eye pigmentation and light deprivation on inherited retinal dystrophy in the rat. Exp Eye Res. 1975;21:167-192.
41. Panayotatos N, Radziejewska E, Acheson A, Pearsall D, Thadani A, Wong V. Exchange of a single amino acid interconverts the specific activity and gel mobility of human and rat ciliary neurotrophic factors. J Biol Chem. 1993;268:19000-19003.
42. LaVail MM, Gorrin GM, Repaci MA, Yasumura D. Light-induced retinal degeneration in albino mice and rats: strain and species differences. In: Hollyfield JG, Anderson RE, LaVail MM, eds. Degenerative Retinal Disorders: Clinical and Laboratory Investigations. New York: Alan R. Liss; 1987:439-454.
43. Carter-Dawson LD, LaVail MM. Rods and cones in the mouse retina. I. Structural analysis using light and electron microscopy. J Comp Neurol. 1979;188:245-262.
44. 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.
45. Tansley K. The formation of rosettes in the rat retina. Br J Ophthalmol. 1933;17:321-336.
46. Cayouette M, Gravel C. Adenovirus-mediated gene transfer of ciliary neurotrophic factor can prevent photoreceptor degeneration in the retinal degeneration (rd) mouse. Hum Gene Ther. 1997;8: 423-430.
47. Caffé AR, Söderpalm A, van Veen T. Photoreceptor-specific protein expression of mouse retina in organ culture and retardation of rd degeneration in vitro by a combination of basic fibroblast growth factor and nerve growth factors. Curr Eye Res. 1993;12:719-726.
48. Matthes MT, Yasumura D, Yancopoulos GD, et al. Activation of CNTF and BDNF receptors in the retina: role in photoreceptor rescue. [ARVO Abstract]. Invest Ophthalmol Vis Sci. 1995;36: S252.
49. Kirsch M, Kasper EM, Hofmann H-D. CNTF in the rat retina: expression and biological effects. Soc Neurosci Abstr. 1995;21: 547.
50. Jelsma TN, Friedman HH, Berkelaar M, Bray GM, Aguayo AJ. Different forms of the neurotrophin receptor trkB mRNA predominate in rat retina and optic nerve. J Neurobiol. 1993;24:1207-1214.
51. Rickman DW, Brecha NC. Expression of the proto-oncogene, trk, receptors in the developing rat retina. Vis Neurosci. 1995;12:215-222.
52. Ugolini G, Cremisi F, Maffei L. TrkA, TrkB, and p75 mRNA expression is developmentally regulated in the rat retina. Brain Res. 1995;704:121-124.
53. Cohen-Cory S, Escandon E, Fraser SE. The cellular patterns of BDNF and trkB expression suggest multiple roles for BDNF during Xenopus visual system development. Dev Biol. 1996;179:102-115.
54. Hallböök F, Bäkström A, Kullander K, Ebendal T, Carri NG. Expression of neurotrophins and trk receptors in the avian retina. J Comp Neurol. 1996;364:664-676.
55. Tso MOM, Zhang C, Abler AS, et al. Apoptosis leads to photoreceptor degeneration in inherited retinal dystrophy of RCS rats. Invest Ophthalmol Vis Sci. 1994;35:2693-2699.
56. Shahinfar S, Edward DP, Tso MOM. A pathologic study of photoreceptor cell death in retinal photic injury. Curr Eye Res. 1991; 10:47-59.
57. Remé CE, Weller M, Szczesny P, et al. Light-induced apoptosis in the rat retina in vivo. Morphological features, threshold and time course. In: Anderson RE, LaVail MM, Hollyfield JG, eds. Degenerative Diseases of the Retina. New York: Plenum Press; 1995:19-25.
58. Organisciak DT, Kutty RK, Leffak M, et al. Oxidative damage and responses in retinal nuclei arising from intense light exposure. In: Anderson RE, LaVail MM, Hollyfield JG, eds. Degenerative Diseases of the Retina. New York: Plenum Press; 1995:9-17.
59. Li S, Chang C-J, Abler AS, Tso MOM. Inhibitory effects of cycloheximide and flunarizine on light-induced apoptosis of photoreceptor cells. In: Anderson RE, LaVail MM, Hollyfield JG, eds. Degenerative Diseases of the Retina. New York: Plenum Press; 1995:27-38.
60. Chang G-Q, Hao Y, Wong F. Apoptosis: final common pathway of photoreceptor death in rd, rds, and rhodopsin mutant mice. Neuron. 1993;11:595-605.
61. Lolley RN, Rong H, Craft CM. Linkage of photoreceptor degeneration by apoptosis with inherited defect in phototransduction. Invest Ophthalmol Vis Sci. 1994;35:358-362.
62. Lolley RN. The rd gene defect triggers programmed rod cell death. Invest Ophthalmol Vis Sci. 1994;35:4182-4191.
63. Portera-Cailliau C, Sung C-H, Nathans J, Adler R. Apoptotic photoreceptor cell death in mouse models of retinitis pigmentosa. Proc Natl Acad Sci USA. 1994;91:974-978.
64. Al-Ubaidi MR, Mangini NJ, Quiambao AB, et al. Unscheduled DNA replication precedes apoptosis of photoreceptors expressing SV40 T antigen. Exp Eye Res. 1997;64:573-585.
65. Li Z-Y, Milam AH. Apoptosis in retinitis pigmentosa. In: Anderson RE, LaVail MM, Hollyfield JG, eds. Degenerative Diseases of the Retina. New York: Plenum Press; 1995:1-8.
66. Grotta JC. Current medical and surgical therapy for cerebrovascular disease. N Engl J Med. 1987;317:1505-1516.
67. Takahashi K, Lam TT, Edward DP, Büchi ER, Tso MOM. Protective effects of flunarizine on ischemic injury in the rat retina. Arch Ophthalmol. 1992;110:862-870.
68. Cheng B, Mattson MP. NGF and bFGF protect rat hippocampal and human cortical neurons against hypoglycemic damage for stabilizing calcium homeostasis. Neuron. 1991;7:1031-1041.
69. LaVail MM, Sidman RL. C57BL/6J mice with inherited retinal degeneration. Arch Ophthalmol. 1974;91:394-400.
70. LaVail MM, Matthes MT, Yasumura D, Lau C, Unoki K, Steinberg RH. Photoreceptor rescue by survival promoting factors in constant light damage and in RCS rats with inherited retinal dystrophy. [ARVO Abstract]. Invest Ophthalmol Vis Sci. 1995;36(Suppl): S211.
71. LaVail MM, Matthes MT, Yasumura D, Steinberg RH. Histological method to assess photoreceptor light damage and protection by survival factors. In: LaVail MM, Hollyfield JG, Anderson RE, eds. Degenerative Retinal Diseases. New York: Plenum Publishing; 1997:369-384.
72. 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.
73. 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.
74. Steinberg RH, Song Y, Cheng T, et al. Exposure to constant light up-regulates the expression of bFGF, CNTF, FGFR-1, and GFAP mRNA in the rat retina. [ARVO Abstract]. Invest Ophthalmol Vis Sci. 1995;36:S637.
75. 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.
76. Steinberg RH, Flannery JG, Naash M, et al. Transgenic rat models of inherited retinal degeneration caused by mutant opsin genes. [ARVO Abstract]. Invest Ophthalmol Vis Sci. 1996;37: S698.
77. Bennett J, Wilson J, Sun D, Forbes B, Maguire A. Photoreceptor cell rescue in retinal degeneration (rd) mice by in vivo gene therapy. Nat Med. 1996;2:649-654.
78. LaVail MM, Steinberg RH, Matthes MT, et al. Protection from constant light damage by NT-3 overexpressed by the lens in transgenic mice. [ARVO Abstract]. Invest Ophthalmol Vis Sci. 1997;38: S479.