Fas ligand-fas signaling participates in light-induced apoptotic death in photoreceptor cells

Investigative Ophthalmology and Visual Science

Volumn 53, Issue 7, 2012, Pages 3703-3716

  Chang, Qing ^a   Peter, Marcus E ^b   Grassi, Michael A ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; CASPASE 8; FAS ANTIGEN; FAS ASSOCIATED DEATH DOMAIN PROTEIN; FAS LIGAND; CYSTEINE PROTEINASE INHIBITOR; FAS PROTEIN, HUMAN; FAS PROTEIN, MOUSE; IMIDAZOLE DERIVATIVE; INDOLE DERIVATIVE; NECROSTATIN 1; NECROSTATIN-1;

ANIMAL CELL; APOPTOSIS; ARTICLE; CONTROLLED STUDY; FLUORESCENCE ACTIVATED CELL SORTING; FLUORESCENCE IN SITU HYBRIDIZATION; HUMAN; HUMAN TISSUE; IMMUNOFLUORESCENCE TEST; IMMUNOPRECIPITATION; LIGHT EXPOSURE; NECROPTOSIS; NICK END LABELING; NONHUMAN; PHOTORECEPTOR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; WESTERN BLOTTING; ANIMAL; DRUG ANTAGONISM; DRUG EFFECT; LIGHT; METABOLISM; MOUSE; PHYSIOLOGY;

ANIMALS; ANTIGENS, CD95; APOPTOSIS; BLOTTING, WESTERN; CASPASE 8; CYSTEINE PROTEINASE INHIBITORS; FAS LIGAND PROTEIN; HUMANS; IMIDAZOLES; IMMUNOPRECIPITATION; IN SITU NICK-END LABELING; INDOLES; LIGHT; MICE; PHOTORECEPTOR CELLS;

EID: 84865842787     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.11-8928     Document Type: Article

References (60)

1. den Hollander AI, Black A, Bennett J, Cremers FP. Lighting a candle in the dark: advances in genetics and gene therapy of recessive retinal dystrophies. J Clin Invest. 2010;120:3042-3053.
2. Wright AF, Chakarova CF, Abd El-Aziz MM, Bhattacharya SS. Photoreceptor degeneration: genetic and mechanistic dissection of a complex trait. Nat Rev Genet. 2010;11:273-284.
3. Stone J, Maslim J, Valter-Kocsi K, et al. Mechanisms of photoreceptor death and survival in mammalian retina. Prog Retin Eye Res. 1999;18:689-735.
4. Portera-Cailliau C, Sung CH, Nathans J, Adler R. Apoptotic photoreceptor cell death in mouse models of retinitis pigmentosa. Proc Natl Acad Sci U S A. 1994;91:374-378.
5. Dunaief JL, Dentchev T, Ying GS, Milam AH. The role of apoptosis in age-related macular degeneration. Arch Ophthalmol. 2002;120:1435-1442.
6. Quintyn JC, Ranty ML, Mathis A. Photoreceptor apoptosis in human retinal detachment. Am J Ophthalmol. 2006;141:227-228.
7. Bird A. How to keep photoreceptors alive. Proc Natl Acad Sci U S A. 2007;104:2033-2034.
8. Ripps H. Cell death in retinitis pigmentosa: gap junctions and the 'by-stander' effect. Exp Eye Res. 2002;74:327-336.
9. Krebs MP, White DA, Kaushal S. Biphasic photoreceptor degeneration induced by light in a T17M rhodopsin mouse model of cone bystander damage. Invest Ophthalmol Vis Sci. 2009;50:2956-2965.
10. Chrysostomou V, Valter K, Stone J. Cone-rod dependence in the rat retina: variation with the rate of rod damage. Invest Ophthalmol Vis Sci. 2009;50:3017-3023.
11. Wenzel A, Grimm C, Samardzija M, Remé CE. Molecular mechanisms of light-induced photoreceptor apoptosis and neuroprotection for retinal degeneration. Prog Retin Eye Res. 2005;24:275-306.
12. Xu H, Chen M, Forrester JV. Para-inflammation in the aging retina. Prog Retin Eye Res. 2009;28:348-368.
13. Ding X, Patel M, Chan CC. Molecular pathology of age-related macular degeneration. Prog Retin Eye Res. 2009;28:1-18.
14. Yu DY, Cringle SJ, Su EN, Yu PK. Intraretinal oxygen levels before and after photoreceptor loss in the RGC rat. Invest Ophthalmol Vis Sci. 2000;41:3999-4006.
15. Yu DY, Cringle S, Valter K, Walsh N, Lee D, Stone J. Photoreceptor death, trophic factor expression, retinal oxygen status, and photoreceptor function in the P23H rat. Invest Ophthalmol Vis Sci. 2004;45:2013-2019.
16. Stone J, Maslim J, Valter K, et al. Mechanisms of photoreceptor death and survival in mammalian retina. Prog Retin Eye Res. 1999;18:689-735.
17. Organisciak DT, Winkler BS. Retinal light damage: practical and theoretical considerations. Prog Retin Eye Res. 1994;13: 1-29.
18. Huang HL, Fang LW, Lu SP, Chou CK, Luh TY, Lai MZ. DNAdamaging reagents induce apoptosis through reactive oxygen species-dependent Fas aggregation. Oncogene. 2003;22:8168-8177.
19. Wang L, Azad N, Kongkaneramit L, et al. The Fas death signaling pathway connecting reactive oxygen species generation and FLICE inhibitory protein down-regulation. J Immunol. 2008;180:3072-3080.
20. Peter ME, Budd RC, Desbarats J, et al. The CD95 receptor: apoptosis revisited. Cell. 2007;129:447-450.
21. Lambert C, Landau AM, Desbarats J. Fas-beyond death: a regenerative role for Fas in the nervous system. Apoptosis. 2003;8:551-562.
22. Wajant H, Pfizenmaier K, Scheurich P. Non-apoptotic Fas signaling. Cytokine Growth Factor Rev. 2003;14:53-66.
23. Corsini NS, Sancho-Martinez I, Laudenklos S, et al. The death receptor CD95 activates adult neural stem cells for working memory formation and brain repair. Cell Stem Cells. 2009;5: 178-190.
24. Landau AM, Luk KC, Jones ML, et al. Defective Fas expression exacerbates neurotoxicity in a model of Parkinson's disease. J Exp Med. 2005;202:575-581.
25. Raoul C, Buhler E, Sadeghi C, et al. Chronic activation in presymptomatic amyotrophic lateral sclerosis (ALS) mice of a feedback loop involving Fas, Daxx, and FasL. Proc Natl Acad Sci U S A. 2006;103:6007-6012.
26. Raoul C, Estevez AG, Nishimune H, et al. Motoneuron death triggered by a specific pathway downstream of Fas. potentiation by ALS-linked SOD1 mutations. Neuron. 2002;35:1067-1083.
27. Choi C, Benveniste EN. Fas ligand/Fas system in the brain: regulator of immune and apoptotic response. Brian Res Rev. 2004;44:65-81.
28. Zacks DN, Zheng QD, Han Y, Bakhru R, Miller JW. FASmediated apoptosis and its relation to intrinsic pathway activation in an experimental model of retinal detachment. Invest Ophthalmol Vis Sci. 2004;45:4563-4569.
29. Zacks DN, Boehlke C, Richards AL, Zheng QD. Role of the Fassignaling pathway in photoreceptor neuroprotection. Arch Ophthalmol. 2007;125:1389-1395.
30. Besirli CG, Chinskey ND, Zheng QD, Zacks DN. Inhibition of retinal detachment-induced apoptosis in photoreceptors by a small peptide inhibitor of the fas receptor. Invest Ophthalmol Vis Sci. 2010;51:2177-2184.
31. Blackshaw S, Fraioli RE, Furukawa T, Cepko CL. Comprehensive analysis of photoreceptor gene expression and the identification of candidate retinal disease genes. Cell. 2001; 107:579-589.
32. Kanan Y, Moiseyev G, Agarwal N, Ma JX, Al-Ubaidi MR. Light induces programmed cell death by activating multiple independent proteases in a cone photoreceptor cell line. Invest Ophthalmol Vis Sci. 2007;48:40-51.
33. Schneider BG, Kraig E. Na{thorn}, K{thorn}-ATPase of the photoreceptor: selective expression of a3 and b2 isoforms. Exp Eye Res. 1990; 51:553-564.
34. Vandenabeele P, Galluzzi L, Vanden Berghe T, Kroemer G. Molecular mechanisms of necroptosis: an ordered cellular explosion. Nat Rev Mol Cell Biol. 2010;11:700-714.
35. Hitomi J, Christofferson DE, Ng A, et al. Identification of a molecular signaling network that regulates a cellular necrotic cell death pathway. Cell. 2008;135:1311-1323.
36. Degterev A, Hitomi J, Germscheid M, et al. Identification of RIP1 kinase as a specific cellular target of necrostatins. Nat Chem Biol. 2008;4:313-321.
37. Kayagaki N, Kawasaki A, Ebata T, et al. Metalloproteinasemediated release of human Fas ligand. J Exp Med. 1995;182: 1777-1783.
38. Wenzel A, Reme 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.
39. Donovan M, Carmody RJ, Cotter TG. Light-induced photoreceptor apoptosis in vivo requires neuronal nitric-oxide synthase and guanylate cyclase activity and is caspase-3- independent. J Biol Chem. 2001;276:23000-23008.
40. Hao W, Wenzel A, Obin MS, et al. Evidence for two apoptotic pathways in light-induced retinal degeneration. Nat Genet. 2002;32:254-260.
41. Poon HK, Tso MO, Lam TT. c-Fos protein in photoreceptor cell death after photic injury in rats. Invest Ophthalmol Vis Sci. 2000;41:2755-2758.
42. Lohr HR, Kuntchithapautham K, Sharma AK, Rohrer B. Multiple, parallel cellular suicide mechanisms participate in photoreceptor cell death. Exp Eye Res. 2006;83:380-389.
43. Lautrette C, Giraud S, Vermot-Desroches C, Preud'homme JL, Jauberteau MO. Expression of a functional Fas death receptor by human foetal motoneurons. Neuroscience. 2003;119:377-385.
44. Tan E, Ding XQ, Saadi A, Agarwal N, Naash MI, Al-Ubaidi MR. Expression of cone-photoreceptor-specific antigens in a cell line derived from retinal tumors in transgenic mice. Invest Ophthalmol Vis Sci. 2004;45:764-768.
45. Krishnamoorthy RR, Crawford MJ, Chaturvedi MM, et al. Photo-oxidative stress down-modulates the activity of nuclear factor-kappaB via involvement of caspase-1, leading to apoptosis of photoreceptor cells. J Biol Chem. 1999;274: 3734-3743.
46. Tanito M, Kwon YW, Kondo N, et al. Cytoprotective effects of geranylgeranylacetone against retinal photooxidative damage. J Neurosci. 2005;25:2396-2404.
47. Shimazaki H, Hironaka K, Fujisawa T, et al. Edaravone-loaded liposome eyedrops protect against light-induced retinal damage in mice. Invest Ophthalmol Vis Sci. 2011;52:7289-7297.
48. Sharma AK, Rohrer B. Sustained elevation of intracellular cGMP causes oxidative stress triggering calpain-mediated apoptosis in photoreceptor degeneration. Curr Eye Res. 2007;32:259-269.
49. Cullen SP, Martin SJ. Caspase activation pathways: some recent progress. Cell Death Differ. 2009;16:935-938.
50. Holler N, Zaru R, Micheau O, et al. Fas triggers an alternative, caspase-8-independent cell death pathway using the kinase RIP as effector molecule. Nat Immunol. 2000;1:489-495.
51. Cho YS, Challa S, Moquin D, et al. Phosphorylation-driven assembly of the RIP1-RIP3 complex regulates programmed necrosis and virus-induced inflammation. Cell. 2009;137: 1112-1123.
52. Trichonas G, Murakami Y, Thanos A, et al. Receptor interacting protein kinases mediate retinal detachment-induced photoreceptor necrosis and compensate for inhibition of apoptosis. Proc Natl Acad Sci U S A. 2010;107:21695-21700.
53. Wallach D, Varfolomeev EE, Malinin NL, Goltsev YV, Kovalenko AV, Boldin MP. Tumor necrosis factor receptor and Fas signaling mechanisms. Annu Rev Immunol. 1999;17:331-367.
54. Yang JH, Basinger SF, Gross RL, Wu SM. Blue light-induced generation of reactive oxygen species in photoreceptor ellipsoids requires mitochondrial electron transport (2003). Invest Ophthalmol Vis Sci. 2003;44:1312-1319.
55. Yamashita H, Horie, K, Yamamoto T, Nagano T, Hirano T. Lightinduced retinal damage in mice. Hydrogen peroxide production and superoxide dismutase activity in retina. Retina. 1992; 12:59-66.
56. Yuan J, Murrell GA, Trickett A, Wang MX. Involvement of cytochrome c release and caspase-3 activation in the oxidative stress-induced apoptosis in human tendon fibroblasts. Biochim Biophys Acta. 2003;1641:35-41.
57. Shiah SG, Chuang SE, Chau YP, Shen SC, Kuo ML. Activation of c-Jun NH2-terminal kinase and subsequent CPP32/Yama during topoisomerase inhibitor beta-lapachone-induced apoptosis through an oxidation-dependent pathway. Cancer Res. 1999;59:391-398.
58. Shrivastava P, Pantano C, Watkin R, et al. Reactive nitrogen species-induced cell death requires Fas-dependent activation of c-Jun N-terminal kinase. Mol Cell Biol. 2004;24:6763-6772.
59. Anathy V, Aesif SW, Guala AS, et al. Redox amplification of apoptosis by caspase-dependent cleavage of glutaredoxin 1 and S-glutathionylation of Fas. J Cell Biol. 2009;184:241-252.
60. Sato T, Machida T, Takahashi S, et al. Fas-mediated apoptosome formation is dependent on reactive oxygen species derived from mitochondrial permeability transition in Jurkat cells. J Immunol. 2004;173:285-296.