Receptor interacting protein kinases mediate retinal detachment-induced photoreceptor necrosis and compensate for inhibition of apoptosis

Proceedings of the National Academy of Sciences of the United States of America

Volumn 107, Issue 50, 2010, Pages 21695-21700

  Trichonas, George ^a,b   Murakami, Yusuke ^a,b   Thanos, Aristomenis ^a   Morizane, Yuki ^a,b   Kayama, Maki ^a,b   Debouck, Christine M ^c   Hisatomi, Toshio ^a,b,d   Miller, Joan W ^a,b   Vavvas, Demetrios G ^a,b  

^a MASSACHUSETTS EYE AND EAR INFIRMARY   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c TetraLogic Pharmaceuticals   (United States)

^d KYUSHU UNIVERSITY   (Japan)

Author keywords

Degenerations; Necroptosis

Indexed keywords

BENZYLOXYCARBONYLVALYLALANYLASPARTYL FLUOROMETHYL KETONE; CASPASE; ENZYME INHIBITOR; NECROSTATIN 1; PROTEIN KINASE; RECEPTOR INTERACTING PROTEIN SERINE THREONINE KINASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL DEATH; CELL LOSS; DEATH; ENZYME INHIBITION; EXPERIMENTAL MODEL; MITOCHONDRION; MORPHOLOGY; MOUSE; NECROSIS; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PHOTORECEPTOR; PHOTORECEPTOR CELL; PRIORITY JOURNAL; PROTEIN INTERACTION; RETINA DETACHMENT;

ANIMALS; APOPTOSIS; APOPTOSIS INDUCING FACTOR; CASPASES; ENZYME INHIBITORS; GTPASE-ACTIVATING PROTEINS; MICE; MICE, KNOCKOUT; NECROSIS; PHOTORECEPTOR CELLS, VERTEBRATE; RATS; REACTIVE OXYGEN SPECIES; RECEPTOR-INTERACTING PROTEIN SERINE-THREONINE KINASES; RETINAL DETACHMENT;

EID: 78650718758     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1009179107     Document Type: Article

References (48)

1. Dunaief JL, Dentchev T, Ying GS, Milam AH (2002) The role of apoptosis in age-related macular degeneration. Arch Ophthalmol 120:1435-1442.
2. Barber AJ, et al. (1998) Neural apoptosis in the retina during experimental and human diabetes. Early onset and effect of insulin. J Clin Invest 102:783-791.
3. Cook B, Lewis GP, Fisher SK, Adler R (1995) Apoptotic photoreceptor degeneration in experimental retinal detachment. Invest Ophthalmol Vis Sci 36:990-996.
4. Arroyo JG, Yang L, Bula D, Chen DF (2005) Photoreceptor apoptosis in human retinal detachment. Am J Ophthalmol 139:605-610.
5. Campo RV, et al. (1999) Pars plana vitrectomy without scleral buckle for pseudophakic retinal detachments. Ophthalmology 106:1811-1815.
6. Kroemer G, et al.; Nomenclature Committee on Cell Death 2009 (2009) Classification of cell death: Recommendations of the Nomenclature Committee on Cell Death 2009. Cell Death Differ 16:3-11.
7. Golstein P, Kroemer G (2007) Cell death by necrosis: Towards a molecular definition. Trends Biochem Sci 32:37-43.
8. Festjens N, Vanden Berghe T, Vandenabeele P (2006) Necrosis, a well-orchestrated form of cell demise: Signalling cascades, important mediators and concomitant immune response. Biochim Biophys Acta 1757:1371-1387.
9. Holler N, et al. (2000) Fas triggers an alternative, caspase-8- independent cell death pathway using the kinase RIP as effector molecule. Nat Immunol 1:489-495.
10. Degterev A, et al. (2008) Identification of RIP1 kinase as a specific cellular target of necrostatins. Nat Chem Biol 4:313-321.
11. Degterev A, et al. (2005) Chemical inhibitor of nonapoptotic cell death with therapeutic potential for ischemic brain injury. Nat Chem Biol 1:112-119.
12. Festjens N, Vanden Berghe T, Cornelis S, Vandenabeele P (2007) RIP1, a kinase on the crossroads of a cell's decision to live or die. Cell Death Differ 14:400-410.
13. Lin Y, Devin A, Rodriguez Y, Liu ZG (1999) Cleavage of the death domain kinase RIP by caspase-8 prompts TNF-induced apoptosis. Genes Dev 13:2514-2526.
14. He S, et al. (2009) Receptor interacting protein kinase-3 determines cellular necrotic response to TNF-alpha. Cell 137:1100-1111.
15. Cho YS, et al. (2009) Phosphorylation-driven assembly of the RIP1-RIP3 complex regulates programmed necrosis and virus-induced inflammation. Cell 137:1112-1123.
16. Zhang DW, et al. (2009) RIP3, an energy metabolism regulator that switches TNFinduced cell death from apoptosis to necrosis. Science 325:332-336.
17. Nakazawa T, et al. (2006) Characterization of cytokine responses to retinal detachment in rats. Mol Vis 12:867-878.
18. Zacks DN, et al. (2003) Caspase activation in an experimental model of retinal detachment. Invest Ophthalmol Vis Sci 44:1262-1267.
19. Zacks DN, Zheng QD, Han Y, Bakhru R, Miller JW (2004) FAS-mediated apoptosis and its relation to intrinsic pathway activation in an experimental model of retinal detachment. Invest Ophthalmol Vis Sci 45:4563-4569.
20. Hisatomi T, et al. (2001) Relocalization of apoptosis-inducing factor in photoreceptor apoptosis induced by retinal detachment in vivo. Am J Pathol 158:1271-1278.
21. Galluzzi L, Kepp O, Kroemer G (2009) RIP kinases initiate programmed necrosis. J Mol Cell Biol 1:8-10.
22. Grasl-Kraupp B, et al. (1995) In situ detection of fragmented DNA (TUNEL assay) fails to discriminate among apoptosis, necrosis, and autolytic cell death: A cautionary note. Hepatology 21:1465-1468.
23. Teng X, et al. (2007) Structure-activity relationship study of [1,2,3]thiadiazole necroptosis inhibitors. Bioorg Med Chem Lett 17:6836-6840.
24. Hoglen NC, et al. (2004) Characterization of IDN-6556 (3-[2-(2-tert-butylphenylaminooxalyl)-amino]-propionylamino]-4-oxo-5-(2,3,5, 6-tetrafluoro-phenoxy)-pentanoic acid): A liver-targeted caspase inhibitor. J Pharmacol Exp Ther 309:634-640.
25. Hisatomi T, et al. (2003) Clearance of apoptotic photoreceptors: Elimination of apoptotic debris into the subretinal space and macrophage-mediated phagocytosis via phosphatidylserine receptor and integrin alphavbeta3. Am J Pathol 162:1869-1879.
26. Erickson PA, Fisher SK, Anderson DH, Stern WH, Borgula GA (1983) Retinal detachment in the cat: The outer nuclear and outer plexiform layers. Invest Ophthalmol Vis Sci 24:927-942.
27. You Z, et al. (2008) Necrostatin-1 reduces histopathology and improves functional outcome after controlled cortical impact in mice. J Cereb Blood Flow Metab 28: 1564-1573.
28. Nakazawa T, et al. (2007) Monocyte chemoattractant protein 1 mediates retinal detachment-induced photoreceptor apoptosis. Proc Natl Acad Sci USA 104: 2425-2430.
29. Kim YS, Morgan MJ, Choksi S, Liu ZG (2007) TNF-induced activation of the Nox1 NADPH oxidase and its role in the induction of necrotic cell death. Mol Cell 26: 675-687.
30. Susin SA, et al. (1999) Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 397:441-446.
31. Hisatomi T, et al. (2008) HIV protease inhibitors provide neuroprotection through inhibition of mitochondrial apoptosis in mice. J Clin Invest 118:2025-2038.
32. Krantic S, Mechawar N, Reix S, Quirion R (2007) Apoptosis-inducing factor: A matter of neuron life and death. Prog Neurobiol 81:179-196.
33. Arimura N, et al. (2009) Intraocular expression and release of high-mobility group box 1 protein in retinal detachment. Lab Invest 89:278-289.
34. Scaffidi P, Misteli T, Bianchi ME (2002) Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature 418:191-195.
35. Donovan M, Cotter TG (2002) Caspase-independent photoreceptor apoptosis in vivo and differential expression of apoptotic protease activating factor-1 and caspase-3 during retinal development. Cell Death Differ 9:1220-1231.
36. Sanges D, Comitato A, Tammaro R, Marigo V (2006) Apoptosis in retinal degeneration involves cross-talk between apoptosis-inducing factor (AIF) and caspase-12 and is blocked by calpain inhibitors. Proc Natl Acad Sci USA 103:17366-17371.
37. Murakami Y, et al. (2008) Inhibition of nuclear translocation of apoptosis-inducing factor is an essential mechanism of the neuroprotective activity of pigment epithelium-derived factor in a rat model of retinal degeneration. Am J Pathol 173: 1326-1338.
38. Vandenabeele P, Declercq W, Van Herreweghe F, Vanden Berghe T (2010) The role of the kinases RIP1 and RIP3 in TNF-induced necrosis. Sci Signal 3:re4.
39. Lee TH, Shank J, Cusson N, Kelliher MA (2004) The kinase activity of Rip1 is not required for tumor necrosis factor-alpha-induced IkappaB kinase or p38 MAP kinase activation or for the ubiquitination of Rip1 by Traf2. J Biol Chem 279:33185-33191.
40. Mahoney DJ, et al. (2008) Both cIAP1 and cIAP2 regulate TNFalpha-mediated NFkappaB activation. Proc Natl Acad Sci USA 105:11778-11783.
41. Wang L, Du F, Wang X (2008) TNF-alpha induces two distinct caspase-8 activation pathways. Cell 133:693-703.
42. Zacks DN, Boehlke C, Richards AL, Zheng QD (2007) Role of the Fas-signaling pathway in photoreceptor neuroprotection. Arch Ophthalmol 125:1389-1395.
43. Vercammen D, et al. (1998) Dual signaling of the Fas receptor: Initiation of both apoptotic and necrotic cell death pathways. J Exp Med 188:919-930.
44. Lin Y, et al. (2004) Tumor necrosis factor-induced nonapoptotic cell death requires receptor-interacting protein-mediated cellular reactive oxygen species accumulation. J Biol Chem 279:10822-10828.
45. Moubarak RS, et al. (2007) Sequential activation of poly(ADP-ribose) polymerase 1, calpains, and Bax is essential in apoptosis-inducing factor-mediated programmed necrosis. Mol Cell Biol 27:4844-4862.
46. Zitvogel L, Kepp O, Kroemer G (2010) Decoding cell death signals in inflammation and immunity. Cell 140:798-804.
47. Cavassani KA, et al. (2008) TLR3 is an endogenous sensor of tissue necrosis during acute inflammatory events. J Exp Med 205:2609-2621.
48. Newton K, Sun X, Dixit VM (2004) Kinase RIP3 is dispensable for normal NF-kappa Bs, signaling by the B-cell and T-cell receptors, tumor necrosis factor receptor 1, and Tolllike receptors 2 and 4. Mol Cell Biol 24:1464-1469.