Caspase-independent photoreceptor apoptosis in vivo and diffrential expression of apoptotic protease activating factor-1 and caspase-3 during retinal development

Cell Death and Differentiation

Volumn 9, Issue 11, 2002, Pages 1220-1231

  Donovan, M ^a   Cotter, T G ^a  

^a UNIVERSITY COLLEGE CORK   (Ireland)

Author keywords

Apoptosis; Caspase independent; Light; Photoreceptor; Retinitis pigmentosa

Indexed keywords

APOPTOTIC PROTEASE ACTIVATING FACTOR 1; BENZYLOXYCARBONYLVALYLALANYLASPARTYL FLUOROMETHYL KETONE; CALCIUM; CALCIUM CHANNEL BLOCKING AGENT; CALPAIN; CASPASE 3; CASPASE 7; CASPASE 8; CASPASE 9; CASPASE INHIBITOR; CYTOCHROME C; DILTIAZEM; INTERLEUKIN 1BETA CONVERTING ENZYME; APAF1 PROTEIN, MOUSE; BENZYLOXYCARBONYLVALYL ALANYL ASPARTYL FLUOROMETHYL KETONE; BENZYLOXYCARBONYLVALYL-ALANYL-ASPARTYL FLUOROMETHYL KETONE; CASP3 PROTEIN, MOUSE; CASPASE; CYSTEINE PROTEINASE INHIBITOR; PEPTIDE CHLOROMETHYL KETONE; PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL DEATH; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOSOL; ENZYME ACTIVATION; HUMAN; HUMAN CELL; IN VIVO STUDY; INHIBITION KINETICS; LIGHT EXPOSURE; MALE; MOUSE; MOUSE STRAIN; NONHUMAN; PHOTORECEPTOR; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RETINA DEGENERATION; RETINA DEVELOPMENT; RETINA DYSTROPHY; ANIMAL; BIOSYNTHESIS; DRUG ANTAGONISM; DRUG EFFECT; ENZYMOLOGY; GENETICS; LIGHT; METABOLISM; PHYSIOLOGY; PRENATAL DEVELOPMENT; PROTEIN SYNTHESIS; RETINA;

AMINO ACID CHLOROMETHYL KETONES; ANIMALS; APOPTOSIS; APOPTOTIC PROTEASE-ACTIVATING FACTOR 1; CALCIUM; CALCIUM CHANNEL BLOCKERS; CALPAIN; CASPASE 3; CASPASES; CYSTEINE PROTEINASE INHIBITORS; CYTOCHROME C GROUP; DILTIAZEM; LIGHT; MICE; PHOTORECEPTORS; PROTEIN BIOSYNTHESIS; PROTEINS; RETINA;

EID: 0036850537     PISSN: 13509047     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.cdd.4401105     Document Type: Article

References (60)

1. Remé CE, Weller M, Szczesny P, Munz K, Hafezi F, Reinboth J and Clausen, M (1995) Degenrative Diseases of the Retina: New York: Plenum.
2. Milam AH, Li ZY and Fariss RN (1998) Histopathology of the human retina in retinitis pigmentosa. Frog. Retin Eye Res. 17: 175-205
3. Chang GQ, Hao Y and Wong F (1993) Apoptosis: final common pathway of photoreceptor death in rd, rds, and rhodopsin mutant mice. Neuron. 11: 595-605
4. Remé CE, Grimm C, Hafezi F, Marti A and Wenzel A (1998) Apoptotic cell death in retinal degenerations. Prog. Retin. Eye Res. 17: 443-464
5. Travis GH (1998) Mechanisms of cell death in the inherited retinal degenerations. Am. J. Hum. Genet. 62: 503-508
6. Wolf BB and Green DR (1999) Suicidal tendencies: apoptotic cell death by caspase family proteinases. J. Biol. Chem. 274: 20049-20052
7. Samali A, Zhivotovsky B, Jones D, Nagata S and Orrenius S (1999) Apoptosis: cell death defined by caspase activation. Cell Death Differ. 6: 495-496
8. Slee EA, Harte MT Kluck RM, Wolf BB, Casiano CA, Newmeyer DD, Wang HG, Reed JC, Nicholson DW, Alnemri E S, Green DR and Martin SJ (1999) Ordering the cytochrome c-initiated caspase cascade: hierarchical activation of caspases-2, -3, -6, -7, -8, and -10 in a caspase-9-dependent manner. J. Cell Biol. 144: 281-292
9. Okuno S, Shimizu S, Ito T, Nomura M, Hamada E, Tsujimoto Y and Matsuda H (1998) Bcl-2 prevents caspase-independent cell death. J. Biol. Chem. 273: 34272-34277
10. Lavoie JN, Nguyen M, Marcellus RC, Branton PE and Shore GC (1998) E4orf4, a novel adenovirus death factor that induces p53-independent apoptosis by a pathway that is not inhibited by zVAD-fmk. J. Cell Biol. 140: 637-645
11. Borner C and Monney L (1999) Apoptosis without caspases: an inefficient molecular guillotine? Cell Death Differ. 6: 497-507
12. Leist M and Jaattela M (2001) Four deaths and a funeral: from caspases to alternative mechanisms. Nat. Rev. Mol. Cell Biol. 2: 589-598
13. Carmody RJ and Cotter TG (2000) Oxidative stress induces caspase-independent retinal apoptosis in vitro. Cell Death Differ. 7: 282-291
14. Ray SK, Fidan M, Nowak MW, Wilford GG, Hogan EL and Banik NIL (2000) Oxidative stress and Ca2+ influx upregulate calpain and induce apoptosis in PC12 cells. Brain Res. 852: 326-334
15. Wolf BB, Goldstein JC, Stennicke HR, Beere H, Amarante-Mendes GP, Salvesen GS and Green DR (1999) Calpain functions in a caspase-independent manner to promote apoptosis-like events during platelet activation. Blood 94: 1683-1692
16. Wang KK (2000) Calpain and caspase: can you tell the difference? Trends Neurosci. 23: 20-26
17. Vanags DM, Porn-Ares MI, Coppola S, Burgess DH and Orrenius S (1996) Protease involvement in fodrin cleavage and phosphatidylserine exposure in apoptosis. J. Biol. Chem. 271: 31075-31085
18. Wood DE, Thomas A, Devi LA, Berman Y, Beavis RC, Reed JC and Newcomb EW (1998) Bax cleavage is mediated by calpain during drug-induced apoptosis. Oncogene 17: 1069-1078
19. Lee MS, Kwon YT, Li M, Peng J, Friedlander RM and Tsai LH (2000) Neurotoxicity induces cleavage of p35 to p25 by calpain. Nature 405: 360-364
20. Piechaczyk M (2000) Proteolysis of p53 protein by ubiquitous calpains. Methods Mol. Biol. 144: 297-307
21. McGinnis KM, Gnegy ME, Park YH, Mukerjee N and Wang KK (1999) Procaspase-3 and poly(ADP)ribose polymerase (PARP) are calpain substrates. Biochem. Biophys. Res. Commun. 263: 94-99
22. Squier MK and Cohen JJ (1997) Calpain, an upstream regulator of thymocyte apoptosis. J. Immunol. 158: 3690-3697
23. Lankiewicz S, Marc Luetjens C, Truc Bui N, Krohn AJ, Poppe M, Cole GM, Saido TC and Prehn JH (2000) Activation of calpain I converts excitotoxic neuron death into a caspase-independent cell death. J. Biol. Chem. 275: 17064-17071
24. DeBiasi RL, Edelstein CL, Sherry B and Tyler KL (2001) Calpain inhibition protects against virus-induced apoptotic myocardial injury. J. Virol. 75: 351-361
25. Sindram D, Kohli V, Madden JF and Clavien PA (1999) Calpain inhibition prevents sinusoidal endothelial cell apoptosis in the cold ischemic rat liver. Transplantation 68: 136-140
26. Ray SK, Wilford GG, Matzelle DC, Hogan EL and Banik NL (1999) Calpeptin and methylprednisolone inhibit apoptosis in rat spinal cord injury. Ann, NY Acad. Sci. 890: 261-269
27. Donovan M, Carmody RJ and Cotter TG (2001) Light-induced photoreceptor apoptosis in vivo requires neuronal nitric-oxide synthase and guanylate cyclase activity and is caspase-3-independent. J. Biol. Chem. 276: 23000-23008
28. Germain M, Affar EB, D'Amours D, Dixit VM, Salvesen GS and Poirier GG (1999) Cleavage of automodified poly(ADP-ribose) polymerase during apoptosis. Evidence for involvement of caspase-7. J. Biol. Chem. 274: 28379-28384
29. Krajewski S, Gascoyne RD, Zapata JM, Krajewska M, Kitada S, Chhanabhai M, Horsman D and Berean K (1997) Immunolocalization of the ICE/Ced-3-family protease, CPP32 (Caspase-3), in non-Hodgkin's lymphomas, chronic lymphocytic leukemias, and reactive lymph nodes. Blood 89: 3817-3825
30. Katai N, Kikuchi T, Shibuki H, Kuroiwa S, Arai J, Kurokawa T and Yoshimura N (1999) Caspaselike proteases activated in apoptotic photoreceptors of Royal College of Surgeons rats. Invest. Ophthalmol. Vis. Sci. 40: 1802-1807.
31. Grimm C, Wenzel A, Hafezi F and Reme CE (2000) Gene expression in the mouse retina: the effect of damaging light. Mol. Vis. 6: 252-260
32. Xiang J, Chao DT and Korsmeyer SJ (1996) BAX-induced cell death may not require interleukin 1 beta-converting enzyme-like proteases. Proc. Natl. Acad. Sci. USA 93: 14559-14563
33. McCarthy NJ, Whyte MK, Gilbert CS and Evan GI (1997) Inhibition of Ced-3/ICE-related proteases does not prevent cell death induced by oncogenes, DNA damage, or the Bcl-2 homologue Bak. J. Cell Biol. 136: 215-227
34. Liu C, Li Y, Peng M, Laties AM and Wen R (1999) Activation of caspase-3 in the retina of transgenic rats with the rhodopsin mutation s334ter during photoreceptor degeneration. J. Neurosci. 19: 4778-4785
35. Yoshizawa K, Yang J, Senzaki H, Uemura Y, Kiyozuka Y, Shikata N, Oishi Y, Miki Hand Tsubura, A (2000) Caspase-3 inhibitor rescues N-methyl-N-nitrosourea-induced retinal degeneration in Sprague-Dawley rats. Exp. Eye Res. 71: 629-635
36. Li P, Nijhawan D, Budilhardjo I, Srinivasula SM, Ahmad M, Alnemri ES and Wang X (1997) Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 91: 479-489
37. Deveraux QL, Roy N, Stennicke HR, Van Arsdale T, Zhou Q, Srinivasula SM, Alnemri ES, Salvesen GS and Reed JC (1998) IAPs block apoptotic events induced by caspase-8 and cytochrome c by direct inhibition of distinct caspases. EMBO J. 17: 2215-2223
38. Vier J, Furmann C and Hacker G Baculovirus (2000) P35 protein does not inhibit caspase-9 in a cell-free system of apoptosis. Biochem. Biophys. Res. Commun. 276: 855-861
39. Yakovlev AG, Ota K, Wang G, Movsesyan V, Bao WL, Yoshihara K and Faden A (2001) Differential expression of apoptotic protease-activating factor-1 and caspase-3 genes and susceptibility to apoptosis during brain development and after traumatic brain injury. J. Neurosci. 21: 7439-7446
40. Angelastro JM, Moon NY, Liu DX, Yang AS, Greene LA and Franke TF (2001) Characterization of a novel isoform of caspase-9 that inhibits apoptosis. J. Biol. Chem. 276: 12190-12200
41. Seol DW and Billiar TR (1999) A caspase-9 variant missing the catalytic site is an endogenous inhibitor of apoptosis. J. Biol. Chem. 274: 2072-2076
42. Srinivasula SM, Ahmad M, Guo Y, Zhan Y,Lazebnik Y, Fernandes-Alnemri T and Alnemri ES (1999) Identification of an endogenous dominant-negative short isoform of caspase-9 that can regulate apoptosis. Cancer Res. 59: 999-1002
43. Fujita E, Jinbo A, Matuzaki H, Konishi H, Kikkawa U and Momoi T (1999) Akt phosphorylation site found in human caspase-9 is absent in mouse caspase-9. Biochem. Biophys. Res. Commun. 264: 550-555
44. Mathiasen IS, Lademann U and Jaattela M (1999) Apoptosis induced by vitamin D compounds in breast cancer cells is inhibited by Bcl-2 but does not involve known caspases or p53. Cancer Res. 59: 4848-4856
45. Nylandsted J, Rohde M, Brand K, Bastholm L, Elling F and Jaattela M (2000) Selective depletion of heat shock protein 70 (Hsp70) activates a tumor-specific death program that is independent of caspases and bypasses Bcl-2. Proc. Natl. Acad. Sci. USA. 97: 7871-7876
46. Lindenboim L, Yuan J and Stein R (2000) Bcl-xS and Bax induce different apoptotic pathways in PC12 cells. Oncogene 19: 1783-1793
47. Elliott K, Ge K, Du W and Prendergast GC (2000) The c-Myc-interacting adaptor protein Bin 1 activates a caspase-independent cell death program. Oncogene 19: 4669-4684
48. de Bilbao F, Guarin E, Nef P, Vallet P, Giannakopoulos P and Dubois-Dauphin M (1999) Postnatal distribution of cpp32/caspase 3 mRNA in the mouse central nervous system: an in situ hybridization study. J. Comp. Neurol. 409: 339-357
49. Mooney SM and Miller MW (2000) Expression of bcl-2, bax, and caspase-3 in the brain of the developing rat. Brain Res. Dev. Brain Res. 123: 103-117
50. Wolf BB, Schuler M, Li W, Eggers-Sedlet B, Lee W, Tailor P, Fitzgerald P, Mills GB and Green R (2001) Defective cytochrome c-dependent caspase activation in ovarian cancer cell lines due to diminished or absent apoptotic protease activating factor-1 activity. J. Biol. Chem. 276: 34244-34251.
51. Jia L, Srinivasula SM, Liu FT, Newland AC, Fernandes-Alnemri T, Alnemri ES and Kelsey SM (2001) Apaf-1 protein deficiency confers resistance to cytochrome c-dependent apoptosis in human leukemic cells. Blood 98: 414-421
52. Fortin A, Cregan SP, MacLaurin JG, Kushwaha N, Hickman ES, Thompson CS, Hakim A, Albert PR, Cecconi F, Helin K, Park DS and Slack RS (2001) APAF1 is a key transcriptional target for p53 in the regulation of neuronal cell death. J. Cell Biol. 155: 207-216
53. Foghsgaard L, Wissing D, Mauch D, Lademann U, Bastholm L, Boes M, Elling F, Leist M and Jaattela M (2001) Cathepsin Bacts as a dominant execution protease in tumor cell apoptosis induced by tumor necrosis factor. J. Cell Biol. 153: 999-1010
54. Volbracht C, Leist M, Kolb SA and Nicotera P (2001) Apoptosis in caspase-inhibited neurons. Mol. Med. 7: 36-48
55. Saito K, Elce JS, Hamos JE and Nixon RA (1993) Widespread activation of calcium-activated neutral proteinase (calpain) in the brain in Alzheimer disease: a potential molecular basis for neuronal degeneration. Proc. Natl. Acad. Sci. USA 90: 2628-2632
56. Lee KS, Frank S, Vanderklish P, Arai A and Lynch G (1991) Inhibition of proteolysis protects hippocampal neurons from ischemia. Proc. Natl. Acad. Sci. USA 88: 7233-7237
57. David LL, Shearer TR and Shih M (1993) Sequence analysis of lens beta-crystallins suggests involvement of calpain in cataract formation. J. Biol. Chem. 268: 1937-1940
58. Azarian SM and Williams DS (1995) Calpain activity in the retinas of normal and RCS rats. Curr. Eye Res. 14: 731-735
59. Suzuki K (1991) Nomenclature of calcium dependent proteinase. Biomed. Biochim. Acta 50: 483-484
60. Frasson M, Sahel JA, Fabre M, Simonutti M, Dreyfus H and Picaud S (1999) Retinitis pigmentosa: rod photoreceptor rescue by a calcium-channel blocker in the rd mouse. Nat. Med. 5: 1183-1187