Clinical light exposure, photoreceptor degeneration, and AP-1 activation: A cell death or cell survival signal in the rhodopsin mutant retina?

Investigative Ophthalmology and Visual Science

Volumn 48, Issue 11, 2007, Pages 4907-4918

  Gu, Danian ^a   Beltran, William A ^a   Li, Zexiao ^a   Acland, Gregory M ^b   Aguirre, Gustavo D ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PROTEIN C FOS; PROTEIN C JUN; RHODOPSIN; TRANSCRIPTION FACTOR AP 1; TRANSCRIPTION FACTOR FRA 1; TRANSCRIPTION FACTOR JUNB; DNA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DEATH; CELL SURVIVAL; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DARK ADAPTATION; DNA BINDING; DOG; GEL MOBILITY SHIFT ASSAY; IMMUNOCYTOCHEMISTRY; LIGHT EXPOSURE; MUELLER CELL; NONHUMAN; PHOTOGRAPHY; PHOTORECEPTOR CELL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RETINA; RETINA DEGENERATION; SIGNAL TRANSDUCTION; WESTERN BLOTTING; ANIMAL; ANIMAL DISEASE; DOG DISEASE; GENE EXPRESSION REGULATION; GENETICS; IMMUNOHISTOCHEMISTRY; LIGHT; METABOLISM; PATHOLOGY; PHOSPHORYLATION; PHOTORECEPTOR; RADIATION EXPOSURE; RADIATION INJURY;

ANIMALS; BLOTTING, WESTERN; CELL DEATH; CELL SURVIVAL; DNA; DOG DISEASES; DOGS; ELECTROPHORETIC MOBILITY SHIFT ASSAY; GENE EXPRESSION REGULATION; IMMUNOHISTOCHEMISTRY; LIGHT; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; PHOSPHORYLATION; PHOTORECEPTORS, VERTEBRATE; PROTO-ONCOGENE PROTEINS C-FOS; RADIATION INJURIES, EXPERIMENTAL; RETINAL DEGENERATION; RHODOPSIN; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTOR AP-1;

EID: 38449108213     PISSN: 01460404     EISSN: None     Source Type: Journal    
DOI: 10.1167/iovs.07-0428     Document Type: Article

References (52)

1. Berson EL. Retinitis pigmentosa. The Friedenwald Lecture. Invest Ophthalmol Vis Sci. 1993;34:1659-1676.
2. Dryja TP, Berson EL. Retinitis pigmentosa and allied diseases: implications of genetic heterogeneity. Invest Ophthalmol Vis Sci. 1995;36:1197-1200.
3. Berson EL, Rosner B, Weigel-DiFranco C, Dryja TP, Sandberg MA. Disease progression in patients with dominant retinitis pigmentosa and rhodopsin mutations. Invest Ophthalmol Vis Sci. 2002;43:3027-3036.
4. van den Born LI, van Schooneveld MJ, de Jong LAMS, et al. Thr4Lys rhodopsin mutation is associated with autosomal dominant retinitis pigmentosa of the cone-rod type in a small Dutch family. Ophthalmic Genet. 1994;15:51-60.
5. To K, Adamian M, Dryja TP, Berson EL. Histopathologic study of variation in severity of retinitis pigmentosa due to the dominant rhodopsin mutation Pro23His. Am J Ophthalmol. 2002;134:290-293.
6. 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.
7. Cideciyan AV, Hood DC, Huang Y, et al. Disease sequence from mutant rhodopsin allele to rod and cone photoreceptor degeneration in man. Proc Natl Acad Sci USA. 1998;95:7103-7108.
8. Kijas JW, Cideciyan AV, Aleman TS, et al. Naturally occurring rhodopsin mutation in the dog causes retinal dysfunction and degeneration mimicking human dominant retinitis pigmentosa. Proc Natl Acad Sci USA. 2002;99:6328-6333.
9. Cideciyan AV, Jacobson SG, Aleman TS, et al. In vivo dynamics of retinal injury and repair in the rhodopsin mutant dog model of human retinitis pigmentosa. Proc Natl Acad Sci USA. 2005;102:5233-5238.
10. Zhu L, Jang GF, Jastrzebska B, et al. A naturally occurring mutation of the opsin gene (T4R) in dogs affects glycosylation and stability of the G protein-coupled receptor. J Biol Chem. 2004;279:53828-53839.
11. Hao W, Wenzel A, Obin MS, et al. Evidence for two apoptotic pathways in light-induced retinal degeneration. Nat Genet. 2002;32:254-260.
12. Wenzel A, Grimm C, Seeliger MW, et al. Prevention of photoreceptor apoptosis by activation of the glucocorticoid receptor. Invest Ophthalmol Vis Sci. 2001;42:1653-1659.
13. Angel P, Karin M. The role of Jun, Fos and the AP-1 complex in cell-proliferation and transformation. Biochim Biophys Acta. 1991;1072:129-157.
14. Reddy SP, Mossman BT. Role and regulation of activator protein-1 in toxicant-induced responses of the lung. Am J Physiol. 2002;283:L1161-L1178.
15. Karin M, Liu Z, Zandi E. AP-1 function and regulation. Curr Opin Cell Biol. 1997;9:240-246.
16. Pearson G, Robinson F, Beers Gibson T, et al. Mitogen-activated protein (MAP) kinase pathways: regulation and physiological functions. Endocr Rev. 2001;22:153-183.
17. Rubinfeld H, Seger R. The ERK cascade: a prototype of MAPK signaling. Mol Biotechnol. 2005;31:151-174.
18. Aguirre GD, Acland GM. Models, mutants and man: searching for unique phenotypes and genes in the dog model of inherited retinal degeneration. In: Ostrander EA, Giger U, Lindblad-Toh K, eds. The Dog and Its Genome. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press; 2006:291-325.
19. Aguirre GD, Baldwin V, Pearce-Kelling S, Narfstrom K, Ray K, Acland GM. Congenital stationary night blindness in the dog: common mutation in the RPE65 gene indicates founder effect. Mol Vis. 1998;4:23-29.
20. Zangerl B, Goldstein O, Philp AR, et al. Identical mutation in a novel retinal gene causes progressive rod-cone degeneration in dogs and retinitis pigmentosa in humans. Genomics. 2006;88:551-563.
21. Acland GM, Aguirre GD, Bennett J, et al. Long-term restoration of rod and cone vision by single dose rAAV-mediated gene transfer to the retina in a canine model of childhood blindness. Mol Ther. 2005;12:1072-1082.
22. Acland GM, Aguirre GD, Ray J, et al. Gene therapy restores vision in a canine model of childhood blindness. Nat Genet. 2001;28:92-95.
23. Wenzel A, Remé CE, Williams TP, Hafezi F, Grimm C. The RPE65 Leu450Met variation increases retinal resistance against light-induced degeneration by slowing rhodopsin regeneration. J Neurosci. 2001;21:53-58.
24. Kremers JJ, van Norren D. Retinal damage in macaque after white exposures to light lasting ten minutes to twelve hours. Invest Ophthalmol Vis Sci. 1989;30:1032-1040.
25. Nygaard RW, Frumkes TE. Calibration of the retinal illuminance provided by Maxwellian views. Vision Res. 1982;22:433-434.
26. Beltran WA, Rohrer H, Aguirre GD. Immunolocalization of ciliary neurotrophic factor receptor alpha (CNTFRalpha) in mammalian photoreceptor cells. Mol Vis. 2005;11:232-244.
27. Gorski K, Carneiro M, Schibler U. Tissue-specific in vitro transcription from the mouse albumin promoter. Cell. 1986;47:767-776.
28. Beltran WA, Hammond P, Acland GM, Aguirre GD. A frameshift mutation in RPGR exon ORF15 causes photoreceptor degeneration and inner retina remodeling in a model of X-linked retinitis pigmentosa. Invest Ophthalmol Vis Sci. 2006;47:1669-1681.
29. Remé CE. The dark side of light: rhodopsin and the silent death of vision. The Proctor Lecture. Invest Ophthalmol Vis Sci. 2005;46:2671-2682.
30. Grimm C, Wenzel A, Hafezi F, Yu S, Redmond TM, Reme CE. Protection of Rpe65-deficient mice identifies rhodopsin as a mediator of light-induced retinal degeneration. Nat Genet. 2000;25:63-66.
31. Wenzel A, Grimm C, Marti A, et al. c-Fos controls the "private pathway" of light-induced apoptosis of retinal photoreceptors. J Neurosci. 2000;20:81-88.
32. White DA, Hauswirth WW, Kaushal S, Lewin AS. Increased sensitivity to light-induced damage in a mouse model of autosomal dominant retinal disease. Invest Ophthalmol Vis Sci. 2007;48:1942-1951.
33. Oku H, Ikeda T, Honma Y, et al. Gene expression of neurotrophins and their high-affinity Trk receptors in cultured human Muller cells. Ophthalmic Res. 2002;34:38-42.
34. Honjo M, Tanihara H, Kido N, Inatani M, Okazaki K, Honda Y. Expression of ciliary neurotrophic factor activated by retinal Müller cells in eyes with NMDA- and kainic acid-induced neuronal death. Invest Ophthalmol Vis Sci. 2000;41:552-560.
35. Schutte M, Werner P. Redistribution of glutathione in the ischemic rat retina. Neurosci Lett. 1998;246:53-56.
36. Bringmann A, Pannicke T, Grosche J, et al. Müller cells in the healthy and diseased retina. Prog Retin Eye Res. 2006;25:397-424.
37. Wahlin KJ, Adler R, Zack DJ, Campochiaro PA. Neurotrophic signaling in normal and degenerating rodent retinas. Exp Eye Res. 2001;73:693-701.
38. Wahlin KJ, Campochiaro PA, Zack DJ, Adler R. Neurotrophic factors cause activation of intracellular signaling pathways in Muller cells and other cells of the inner retina, but not photoreceptors. Invest Ophthalmol Vis Sci. 2000;41:927-936.
39. Joly S, Pernet V, Chemtob S, Di Polo A, Lachapelle P. Neuroprotection in the juvenile rat model of light-induced retinopathy: evidence suggesting a role for FGF-2 and CNTF. Invest Ophthalmol Vis Sci. 2007;48:2311-2320.
40. Frigg R, Wenzel A, Samardzija M, et al. The prion protein is neuroprotective against retinal degeneration in vivo. Exp Eye Res. 2006;83:1350-1358.
41. Hafezi F, Steinbach JP, Marti A, et al. The absence of c-fos prevents light-induced apoptotic cell death of photoreceptors in retinal degeneration in vivo. Nat Med. 1997;3:346-349.
42. Li G, Anderson RE, Tomita H, et al. Nonredundant role of Akt2 for neuroprotection of rod photoreceptor cells from light-induced cell death. J Neurosci. 2007;27:203-211.
43. Huang H, Frank MB, Dozmorov I, et al. Identification of mouse retinal genes differentially regulated by dim and bright cyclic light rearing. Exp Eye Res. 2005;80:727-739.
44. Wenzel A, Grimm C, Samardzija M, Remé CE. The genetic modifier Rpe65Leu(450): effect on light damage susceptibility in c-Fos-deficient mice. Invest Ophthalmol Vis Sci. 2003;44:2798-2802.
45. Samardzija M, Wenzel A, Aufenberg S, Thiersch M, Reme C, Grimm C. Differential role of Jak-STAT signaling in retinal degenerations. FASEB J. 2006;20:2411-2413.
46. Sung CH, Davenport CM, Nathans J. Rhodopsin mutations responsible for autosomal dominant retinitis pigmentosa: clustering of functional classes along the polypeptide chain. J Biol Chem. 1993;268:26645-26649.
47. Sung CH, Schneider BG, Agarwal N, Papermaster DS, Nathans J. Functional heterogeneity of mutant rhodopsins responsible for autosomal dominant retinitis pigmentosa. Proc Natl Acad Sci USA. 1991;88:8840-8844.
48. Noorwez SM, Malhotra R, McDowell JH, Smith KA, Krebs MP, Kaushal S. Retinoids assist the cellular folding of the autosomal dominant retinitis pigmentosa opsin mutant P23H. J Biol Chem. 2004;279:16278-16284.
49. Mendes HF, van der Spuy J, Chapple JP, Cheetham ME. Mechanisms of cell death in rhodopsin retinitis pigmentosa: implications for therapy. Trends Mol Med. 2005;11:177-185.
50. John SK, Smith JE, Aguirre GD, Milam AH. Loss of cone molecular markers in rhodopsin-mutant human retinas with retinitis pigmentosa. Mol Vis. 2000;6:204-215.
51. Li Z-Y, Jacobson SG, Milam AH. Autosomal dominant retinitis pigmentosa caused by the threonine-17-methionine rhodopsin mutation: retinal histopathology and immunocytochemistry. Exp Eye Res. 1994;58:397-408.
52. Milam AH, Li Z-Y, Fariss RN. Histopathology of the human retina in retinitis pigmentosa. Prog Retin Eye Res. 1998;17:175-205.