Caspase inhibitors protect against NMDA-mediated retinal ganglion cell death

Clinical and Experimental Ophthalmology

Volumn 39, Issue 6, 2011, Pages 545-554

  Schuettauf, Frank ^a,b   Stein, Thomas ^b   Choragiewicz, Tomasz J ^a,d   Rejdak, Robert ^a,d   Bolz, Sylvia ^a   Zurakowski, David ^c   Varde, Meghana A ^a   Laties, Alan M ^b   Thaler, Sebastian ^a  

^a UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c BOSTON CHILDREN S HOSPITAL   (United States)

^d MEDICAL UNIVERSITY OF LUBLIN   (Poland)

Author keywords

Apoptosis; Caspase; Caspase inhibitor; Excitotoxicity; Retinal ganglion cell

Indexed keywords

CASPASE 3; CASPASE 4; CASPASE 6; CASPASE 8; CASPASE 9; CASPASE INHIBITOR; DEVD FMK; DQMD FMK; IETD FMK; INTERLEUKIN 1BETA CONVERTING ENZYME; N METHYL DEXTRO ASPARTIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR STIMULATING AGENT; NEUROPROTECTIVE AGENT; UNCLASSIFIED DRUG; VEID FMK; YVAD FMK;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CELL COUNT; CELL DEATH; CELL SURVIVAL; COMPETITIVE INHIBITION; CONTROLLED STUDY; DRUG MECHANISM; ENZYME ACTIVATION; EXCITOTOXICITY; FEMALE; NEUROPROTECTION; NICK END LABELING; NONHUMAN; PROTEIN ANALYSIS; RAT; RETINA GANGLION CELL;

ANIMALS; APOPTOSIS; CASPASES; CELL COUNT; CELL SURVIVAL; CYTOPROTECTION; ENZYME INHIBITORS; EXCITATORY AMINO ACID AGONISTS; FEMALE; IN SITU NICK-END LABELING; INTRAVITREAL INJECTIONS; N-METHYLASPARTATE; RATS; RATS, INBRED BN; RATS, LONG-EVANS; RETINAL GANGLION CELLS;

EID: 79961207557     PISSN: 14426404     EISSN: 14429071     Source Type: Journal    
DOI: 10.1111/j.1442-9071.2010.02486.x     Document Type: Article

References (65)

1. Lipton SA, Rosenberg PA. Excitatory amino acids as a final common pathway for neurologic disorders. N Eng J Med 1994; 330: 613-22.
2. Hynd MR, Scott HL, Dodd PR. Glutamate-mediated excitotoxicity and neurodegeneration in Alzheimer's disease. Neurochem Int 2004; 45: 583-95.
3. Seo SY, Yun BS, Ryoo IJ etal. Complestatin is a noncompetitive peptide antagonist of N-methyl-D-aspartate and alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid/kainate receptors: secure blockade of ischemic neuronal death. J Pharmacol Exp Ther 2001; 299: 377-84.
4. Casson RJ. Possible role of excitotoxicity in the pathogenesis of glaucoma. Clin Experiment Ophthalmol 2006; 34: 54-63.
5. Ju WK, Lindsey JD, Angert M, Patel A, Weinreb RN. Glutamate receptor activation triggers OPA1 release and induces apoptotic cell death in ischemic rat retina. Mol Vis 2008; 14: 2629-38.
6. Choi DW. Glutamate neurotoxicity and diseases of the nervous system. Neuron 1988; 1: 623-34.
7. Dong CJ, Guo Y, Agey P, Wheeler L, Hare WA. Alpha2 adrenergic modulation of NMDA receptor function as a major mechanism of RGC protection in experimental glaucoma and retinal excitotoxicity. Invest Ophthalmol Vis Sci 2008; 49: 4515-22.
8. Schuettauf F, Naskar R, Vorwerk CK, Zurakowski D, Dreyer EB. Ganglion cell loss after optic nerve crush mediated through AMPA-kainate and NMDA receptors. Invest Ophthalmol Vis Sci 2000; 41: 4313-16.
9. Friedlander RM. Apoptosis and caspases in neurodegenerative diseases. N Engl J Med 2003; 348: 1365-75.
10. Lam TT, Abler AS, Kwong JM, Tso MO. N-methyl-D-aspartate (NMDA) - induced apoptosis in rat retina. Invest Ophthalmol Vis Sci 1999; 40: 2391-7.
11. Chen TA, Yang F, Cole GM, Chan SO. Inhibition of caspase-3-like activity reduces glutamate induced cell death in adult rat retina. Brain Res 2001; 904: 177-88.
12. Ientile R, Macaione V, Teletta M, Pedale S, Torre V, Macaione S. Apoptosis and necrosis occurring in excitotoxic cell death in isolated chick embryo retina. J Neurochem 2001; 79: 71-8.
13. Ankarcona M, Dypbukt JM, Bonfoco E etal. Glutamate-induced neuronal death: a succession of necrosis or apoptosis depending on mitochondrial integrity. Neuron 1995; 15: 961-73.
14. Wilson SE. Stimulus-specific and cell type-specific cascades: emerging principles relating to control of apoptosis in the eye. Exp Eye Res 1999; 69: 255-66.
15. Srinivasula SM, Ahmad M, Fernandes-Alnemri T, Litwack G, Alnemri ES. Molecular ordering of the Fas-apoptotic pathway: the Fas/APO-1 protease Mch5 is a CrmA-inhibitable protease that activates multiple Ced-3/ICE- like cysteine proteases. Proc Natl Acad Sci USA 1996; 93: 14486-91.
16. Srinivasula SM, Ahmad M, Fernandes-Alnemri T, Alnemri ES. Autoactivation of procaspase-9 by Apaf-1-mediated oligomerization. Mol Cell 1998; 1: 949-57.
17. Dugan L, Sensi S, Canzoniero L etal. Mitochondrial production of reactive oxygen species in cortical neurons following exposure to N-methyl-D-Aspartate. J Neurosci 1995; 15: 6377-88.
18. Greenlund LJ, Deckwerth TL, Johnson EM Jr. Superoxide dismutase delays neuronal apoptosis: a role for reactive oxygen species in programmed neuronal death. Neuron 1995; 14: 303-15.
19. Hirst DG, Robson T. Nitrosative stress as a mediator of apoptosis: implications for cancer therapy. Curr Pharm Des 2010; 16: 45-55.
20. Tezel G, Wax MB. Inhibition of caspase activity in retinal cell apoptosis induced by various stimuli in vitro. Invest Ophthalmol Vis Sci 1999; 40: 2660-7.
21. Laabich A, Cooper NG. Neuroprotective effect of AIP on N-methyl-D-aspartate-induced cell death in retinal neurons. Brain Res Mol Brain Res 2000; 85: 32-40.
22. Schuettauf F, Vorwerk C, Naskar R etal. Adeno-associated viruses containing bFGF or BDNF are neuroprotective against excitotoxicity. Curr Eye Res 2004; 29: 379-86.
23. Thaler S, Choragiewicz TJ, Rejdak R etal. Neuroprotection by acetoacetate and beta-hydroxybutyrate against NMDA-induced RGC damage in rat-possible involvement of kynurenic acid. Graefes Arch Clin Exp Ophthalmol 2010; 248: 1729-35.
24. Perche O, Doly M, Ranchon-Cole I. Caspase-dependent apoptosis in light-induced retinal degeneration. Invest Ophthalmol Vis Sci 2007; 48: 2753-9.
25. Schuettauf F, Eibl KH, Thaler S etal. Toxicity study of erucylphosphocholine in a rat model. Curr Eye Res 2005; 30: 813-20.
26. Schuettauf F, Zurakowski D, Quinto K etal. Neuroprotective effects of cardiotrophin-like cytokine on retinal ganglion cells. Graefes Arch Clin Exp Ophthalmol 2005; 243: 1036-42.
27. Manabe S, Lipton SA. Divergent NMDA signals leading to proapoptotic and antiapoptotic pathways in the rat retina. Invest Ophthalmol Vis Sci 2003; 44: 385-92.
28. Sokal RR, Rohlf FJ. Biometry, 3rd edn. New York: W. H. Freeman & Company, 1995; 708-13.
29. Miller RG. Simultaneous Statistical Inference, 2nd edn. New York: Springer-Verlag New York, Inc, 1981; 67-8.
30. Sakhi S, Bruce A, Sun N, Tocco G, Baudry M, Schreiber SS. p53 induction is associated with neuronal damage in the central nervous system. Proc Natl Acad Sci USA 1994; 91: 7525-9.
31. Villapol S, Acarin L, Faiz M, Castellano B, Gonzalez B. Distinct spatial and temporal activation of caspase pathways in neurons and glial cells after excitotoxic damage to the immature rat brain. J Neurosci Res 2007; 85: 3545-56.
32. Wang Y, Dong XX, Cao Y etal. p53 induction contributes to excitotoxic neuronal death in rat striatum through apoptotic and autophagic mechanisms. Eur J Neurosci 2009; 30: 2258-70.
33. Gorman AM, Orrenius S, Ceccatelli S. Apoptosis in neuronal cells: role of caspases. Neuroreport 1998; 9: 49-55.
34. Du Y, Bales KR, Dodel RC etal. Activation of a caspase 3-related cysteine protease is required for glutamate-mediated apoptosis of cultured cerebellar granule neurons. Proc Natl Acad Sci USA 1997; 94: 11657-62.
35. Villapol S, Acarin L, Faiz M, Castellano B, Gonzalez B. Survivin and heat shock protein 25/27 colocalize with cleaved caspase-3 in surviving reactive astrocytes following excitotoxicity to the immature brain. Neuroscience 2008; 153: 108-19.
36. McKinnon SJ, Lehman DM, Kerrigan-Baumrind LA etal. Caspase activation and amyloid precursor protein cleavage in rat ocular hypertension. Invest Ophthalmol Vis Sci 2002; 43: 1077-87.
37. Singh M, Savitz SI, Hoque R etal. Cell-specific caspase expression by different neuronal phenotypes in transient retinal ischemia. J Neurochem 2001; 77: 466-75.
38. Chaudhary P, Ahmed F, Quebada P, Sharma SC. Caspase inhibitors block the retinal ganglion cell death following optic nerve transection. Brain Res Mol Brain Res 1999; 67: 36-45.
39. Vidal-Sanz M, Lafuente M, Sobrado-Calvo P etal. Death and neuroprotection of retinal ganglion cells after different types of injury. Neurotox Res 2000; 2: 215-27.
40. Beer R, Franz G, Krajewski S etal. Temporal and spatial profile of caspase 8 expression and proteolysis after experimental traumatic brain injury. J Neurochem 2001; 78: 862-73.
41. Gerhardt E, Kugler S, Leist M etal. Cascade of caspase activation in potassium-deprived cerebellar granule neurons: targets for treatment with peptide and protein inhibitors of apoptosis. Mol Cell Neurosci 2001; 17: 717-31.
42. Kermer P, Ankerhold R, Klocker N, Krajewski S, Reed JC, Bahr M. Caspase-9: involvement in secondary death of axotomized rat retinal ganglion cells in vivo. Brain Res Mol Brain Res 2000; 85: 144-50.
43. Tezel G, Yang X. Caspase-independent component of retinal ganglion cell death, in vitro. Invest Ophthalmol Vis Sci 2004; 45: 4049-59.
44. Scaffidi C, Fulda S, Srinivasan A etal. Two CD95 (APO-1/Fas) signaling pathways. EMBO J 1998; 17: 1675-87.
45. Li H, Zhu H, Xu CJ, Yuan J. Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell 1998; 94: 491-501.
46. Yu SP, Yeh C, Strasser U, Tian M, Choi DW. NMDA receptor-mediated K+ efflux and neuronal apoptosis. Science 1999; 284: 336-9.
47. Bortner CD, Hughes FM Jr, Cidlowski JA. A primary role for K+ and Na+ efflux in the activation of apoptosis. J Biol Chem 1997; 272: 32436-42.
48. Hughes FM Jr, Bortner CD, Purdy GD, Cidlowski JA. Intracellular K+ suppresses the activation of apoptosis in lymphocytes. J Biol Chem 1997; 272: 30567-76.
49. Bhat RV, DiRocco R, Marcy VR etal. Increased expression of IL-1beta converting enzyme in hippocampus after ischemia: selective localization in microglia. J Neurosci 1996; 16: 4146-54.
50. Miyamae T, Inaba Y, Nishimura G etal. Effect of anakinra on arthropathy in CINCA/NOMID syndrome. Pediatr Rheumatol Online J 2010; 8: 9.
51. Ali SM, Wong VY, Kikly K etal. Apoptosis in polycystic kidney disease: involvement of caspases. Am J Physiol Regul Integr Comp Physiol 2000; 278: R763-9.
52. Kinoshita M, Tomimoto H, Kinoshita A, Kumar S, Noda M. Up-regulation of the Nedd2 gene encoding an ICE/Ced-3-like cysteine protease in the gerbil brain after transient global ischemia. J Cereb Blood Flow Metab 1997; 17: 507-14.
53. Kurokawa T, Katai N, Shibuki H etal. BDNF diminishes caspase-2 but not c-Jun immunoreactivity of neurons in retinal ganglion cell layer after transient ischemia. Invest Ophthalmol Vis Sci 1999; 40: 3006-11.
54. Cascio C, Guarneri R, Russo D etal. A caspase-3-dependent pathway is predominantly activated by the excitotoxin pregnenolone sulfate and requires early and late cytochrome c release and cell-specific caspase-2 activation in the retinal cell death. J Neurochem 2002; 83: 1358-71.
55. Siliprandi R, Canella R, Carmignoto G etal. N-methyl-D-aspartate induced neurotoxicity in the adult rat retina. Vis Neurosci 1992; 8: 567-73.
56. Vorwerk CK, Lipton SA, Zurakowski D, Hyman BT, Sabel BA, Dreyer EB. Chronic low dose glutamate is toxic to retinal ganglion cells; toxicity blocked by memantine. Invest Ophthalmol Vis Sci 1996; 37: 1618-24.
57. Perry VH. Evidence for an amacrine cell system in the ganglion cell layer of the rat retina. Neuroscience 1981; 6: 931-44.
58. Sabel BA, Sauttner J, Stoehr T, Siliprandi R. A behavioral model of excitotoxicity: retinal degeneration, loss of vision, and subsequent recovery after intraocular NMDA administration in adult rats. Exp Brain Res 1995; 106: 93-105.
59. Nakazawa T, Shimura M, Endo S, Takahashi H, Mori N, Tamai M. N-Methyl-D-Aspartic acid suppresses Akt activity through protein phosphatase in retinal ganglion cells. Mol Vis 2005; 11: 1173-82.
60. Berger AB, Sexton KB, Bogyo M. Commonly used caspase inhibitors designed based on substrate specificity profiles lack selectivity. Cell Res 2006; 16: 961-3.
61. Bessero AC, Chiodini F, Rungger-Brandle E, Bonny C, Clarke PG. Role of the c-Jun N-terminal kinase pathway in retinal excitotoxicity, and neuroprotection by its inhibition. J Neurochem 2010; 113: 1307-18.
62. Chiu K, Lam TT, Ying Li WW, Caprioli J, Kwong Kwong JM. Calpain and N-methyl-d-aspartate (NMDA)-induced excitotoxicity in rat retinas. Brain Res 2005; 1046: 207-15.
63. Lemaire C, Andreau K, Souvannavong V, Adam A. Inhibition of caspase activity induces a switch from apoptosis to necrosis. FEBS Lett 1998; 425: 266-70.
64. Vandenabeele P, Vanden BT, Festjens N. Caspase inhibitors promote alternative cell death pathways. Sci STKE 2006; 2006: pe44.
65. Vercammen D, Beyaert R, Denecker G etal. Inhibition of caspases increases the sensitivity of L929 cells to necrosis mediated by tumor necrosis factor. J Exp Med 1998; 187: 1477-85.