The role of CED-3-related cysteine proteases in apoptosis of cerebellar granule cells

Journal of Neuroscience

Volumn 17, Issue 16, 1997, Pages 6105-6113

  Eldadah, Basil A ^a   Yakovlev, Alexander G ^a,b   Faden, Alan I ^a,b  

^a GEORGETOWN UNIVERSITY   (United States)

^b GEORGETOWN UNIVERSITY   (United States)

Author keywords

Calcein AM; CED 3; Cerebellar granule cells; CPP32; ICE; Protease activity; RT PCR

Indexed keywords

CYSTEINE PROTEINASE;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL VIABILITY; CEREBELLUM; ENZYME ACTIVITY; GRANULE CELL; NERVE CELL DEGENERATION; NONHUMAN; POTASSIUM BLOOD LEVEL; PRIORITY JOURNAL; RAT;

EID: 0030804678     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.17-16-06105.1997     Document Type: Article

References (55)

1. Alnemri ES, Livingston DJ, Nicholson DW, Salvesen G, Thornberry NA, Wong WW, Yuan J (1996) Human ICE/CED-3 protease nomenclature. Cell 87:171.
2. Ankarcrona M, Dypbukt JM, Bonfoco E, Zhivotovsky B, Orrenius S, Lipton SA, Nicotera P (1995) Glutamate-induced neuronal death: a succession of necrosis or apoptosis depending on mitochondrial function. Neuron 15:961-973.
3. Armstrong RC, Aja TJ, Hoang KD, Gaur S, Bai X, Alnemri ES, Litwack G, Karanewsky DS, Fritz LC, Tomaselli KJ (1997) Activation of the CED3/ICE-related protease CPP32 in cerebellar granule neurons undergoing apoptosis but not necrosis. J Neurosci 17:553-562.
4. Atabay C, Cagnoli CM, Kharlamov E, Ikonomovic M D, Manev H (1996) Removal of serum from primary cultures of cerebellar granule neurons induces oxidative stress and DNA fragmentation: protection with antioxidants and glutamate receptor antagonists. J Neurosci Res 43: 465-475.
5. Balázs R, Jørgensen OS, Hack N (1988) N-methyl-D-aspartate promotes the survival of cerebellar granule cells in culture. Neuroscience 27:437-451.
6. Batistatou A, Greene LA (1993) Internucleosomal DNA cleavage and neuronal cell survival/death. J Cell Biol 122:523-532.
7. Boldin MP, Goncharov TM, Goltsev YV, Wallach D (1996) Involvement of MACH, a novel MORT1/FADD-interacting protease, in Fas/APO-1- and TNF receptor-induced cell death. Cell 85:803-815.
8. Bozyczko-Coyne D, Dobrzanski P, Meyer S, O'Kane T, Carswell S, Scott RW, Siman R (1996) ICE-related proteases involved in growth factor deprivation-induced neuronal apoptosis. Soc Neurosci Abstr 22:566.
9. Bredesen DE (1995) Neural apoptosis. Ann Neurol 38:839-851.
10. Casciola-Rosen L, Nicholson DW, Chong T, Rowan KR, Thornberry NA, Miller DK, Rosen A (1996) Apopain/CPP32 cleaves proteins that are essential for cellular repair: a fundamental principle of apoptotic death. J Exp Med 183:1957-1964.
11. Chomczynski P, Sacchi N (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162:156-159.
12. Darmon AJ, Nicholson DW, Bleackley RC (1995) Activation of the apoptotic protease CPP32 by cytotoxic T-cell-derived granzyme B. Nature 377:446-448.
13. D'Mello SR, Galli C, Ciotti T, Calissano P (1993) Induction of apoptosis in cerebellar granule neurons by low potassium: inhibition of death by insulin-like growth factor I and cAMP. Proc Natl Acad Sci USA 90:10989-10993.
14. Duan H, Orth K, Chinnaiyan AM, Poirier GG, Froelich CJ, He W-W, Dixit VM (1996) ICE-LAP6, a novel member of the ICE/Ced-3 gene family, is activated by the cytotoxic T cell protease granzyme B. J Biol Chem 271:16720-16724.
15. Eldadah BA, Yakovlev AG, Faden AI (1996) A new approach for the electrophoretic detection of apoptosis. Nucleic Acids Res 24:4092-4093.
16. Ellis HM, Horvitz HR (1986) Genetic control of programmed cell death in the nematode C. elegans. Cell 44:817-829.
17. Enari M, Talanian RV, Wong WW, Nagata S (1996) Sequential activation of ICE-like and CPP32-like proteases during Fas-mediated apoptosis. Nature 380:723-726.
18. Faucheu C, Diu A, Chan AWE, Blanchet A-M, Miossec C, Hervé F, Collard-Dutilleul V, Gu Y, Aldape RA, Lippke JA, Rocher C, Su MS-S, Livingston DJ, Hercend T, Lalanne J-L (1995) A novel human protease similar to the interleukin 1β-converting enzyme induces apoptosis in transfected cells. EMBO J 14:1914-1922.
19. Fernandes-Alnemri T, Litwack G, Alnemri ES (1994) CPP32, a novel human apoptotic protein with homology to Caenorhabditis elegans cell death protein ced-3 and mammalian interleukin-1β-converting enzyme J Biol Chem 269:30761-30764.
20. Fernandes-Alnemri T, Litwack G, Alnemri ES (1995a) Mch2, a new member of the apoptotic Ced-3/Ice cysteine protease gene family Cancer Res 55:2737-2742.
21. Fernandes-Alnemri T, Litwack G, Alnemri ES (1995b) Mch3, a novel human apoptotic cysteine protease highly related to CPP32. Cancer Res 53:6045-6052.
22. Fernandes-Alnemri T, Armstrong RC, Krebs J, Srinivasula SM, Wang L, Bullrich F, Fritz LC, Trapani JA, Tomaselli KJ, Litwack G, Alnemri ES (1996) In vitro activation of CPP32 and Mch3 by Mch4, a novel human apoptotic cysteine protease containing two FADD-like domains. Proc Natl Acad Sci USA 93:7464-7469.
23. Gavrieli Y, Sherman Y, Ben-Sasson SA (1992) Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J Cell Biol 119:493-501.
24. Hartley A, Stone JM, Heron C, Cooper JM, Schapira AHV (1994) Complex I inhibitors induce dose-dependent apoptosis in PC12 cells: relevance to Parkinson's disease. J Neurochem 63:1987-1990.
25. Jacobson MD, Weil M, Raff MC (1996) Role of ced-3/ICE-family proteases in staurosporine-induced programmed cell death. J Cell Biol 133:1041-1051.
26. Kamens J, Paskind M, Hugunin M, Talanian RV, Allen H, Banach D, Bump N, Hackett M, Johnston CG, Li P, Mankovich JA, Terranova M, Ghayur T (1995) Identification and characterization of ICH-2, a novel member of the interleukin-1β converting enzyme family of cysteine proteases. J Biol Chem 270:15250-15256.
27. Kaufmann SH, Desnoyers S, Ottaviano Y, Davidson ND, Poirier GG (1993) Specific proteolytic cleavage of poly(ADP-ribose) polymerase: an early marker of chemotherapy-induced apoptosis. Cancer Res 53:3976-3985.
28. Kayalar C, Örd T, Testa MP, Zhong LT, Bredesen DE (1996) Cleavage of actin by interleukin 1β-converting enzyme to reverse DNase I inhibition. Proc Natl Acad Sci USA 93:2234-2238.
29. Kerr JFR, Wyllie AH, Currie AR (1972) Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer 26:239-257.
30. Kuida K, Lippke JA, Ku G, Harding MW, Livingston DJ, Su MS-S, Flavell RA (1995) Altered cytokine export and apoptosis in mice deficient in interleukin-1β converting enzyme. Science 267:2000-2003.
31. Kuida K, Zheng TS, Na S, Kuan C-Y, Yang D, Karasuyama H, Rakic P, Flavell RA (1996) Decreased apoptosis in the brain and premature lethality in CPP32-deficient mice. Nature 384:368-372.
32. Kumar S, Kinoshita M, Noda M, Copeland NG, Jenkins NA (1994) Induction of apoptosis by the mouse Nedd2 gene, which encodes a protein similar to the product of the Caenorhabditis elegans cell death gene ced-3 and the mammalian IL-1β-converting enzyme. Genes Dev 8:1613-1626.
33. Li Y, Sharov VG, Jiang N, Zaloga C, Sabbah HN, Chopp N (1995) Ultrastructural and light microscopic evidence of apoptosis after middle cerebral artery occlusion in the rat. Am J Pathol 146:1045-1051.
34. Linnik MD, Zobrist RH, Hatfield MD (1993) Evidence supporting a role for programmed cell death in focal cerebral ischemia in rats. Stroke 24:2002-2009.
35. Liu X, Kim CN, Pohl J, Wang X (1996) Purification and characterization of an interleukin-1β-converting enzyme family protease that activates cysteine protease P32 (CPP32). J Biol Chem 271:13371-13376.
36. Martin SJ, Green DR (1995) Protease activation during apoptosis: death by a thousand cuts? Cell 82:349-352.
37. Miller TM, Johnson EM (1996) Metabolic and genetic analyses of apoptosis in potassium/serum-deprived rat cerebellar granule cells. J Neurosci 16:7487-7495.
38. relIII, members of the ICE/CED-3 family of cysteine proteases. J Biol Chem 270:15870-15876.
39. Muzio M, Chinnaiyan AM, Kischkel FC, O'Rourke K, Shevchenko A, Ni J, Scaffidi C, Bretz JD, Zhang M, Gentz R, Mann M, Krammer PH, Peter ME, Dixit VM (1996) FLICE, a novel FADD-homologous ICE/CED-3-like protease, is recruited to the CD95 (Fas/APO-1) death-inducing signaling complex. Cell 85:817-827.
40. Ni B, Wu X, Du Y, Hamilton-Byrd E, Rockey PK, Rosteck Jr P, Poirier GG, Su Y, Paul SM (1996) Cloning and expression of a rat brain ICE-related protease (IRP) and role in KCI deficiency-mediated apoptosis of cultured cerebellar granule cells. Soc Neurosci Abstr 22:567.
41. Nicholson DW, Ali A, Thornberry NA, Vaillancourt JP, Ding CK, Gallant M, Gareau Y, Griffin PR, Labelle M, Lazebnik YA, Munday NA, Raju SM, Smulson ME, Yamin T-T, Yu VL, Miller DK (1995) Identification and inhibition of the ICE/CED-3 protease necessary for mammalian apoptosis. Nature 376:37-43.
42. Oppenheim RW (1991) Cell death during development of the nervous system. Annu Rev Neurosci 14:453-501.
43. Portera-Cailliau C, Hedreen JC, Price DL, Koliatsos VE (1995) Evidence for apoptotic cell death in Huntington disease and excitotoxic animal models. J Neurosci 15:3775-3787.
44. Quan LT, Tewari M, O'Rourke K, Dixit V, Snipas SJ, Poirier GG, Ray C, Pickup DJ, Salvesen GS (1996) Proteolytic activation of the cell death protease Yama/CPP32 by granzyme B. Proc Natl Acad Sci USA 93:1972-1976.
45. Rabizadeh S, Gralla EB, Borchelt DR, Gwinn R, Valentine JS, Sisodia S, Wong P, Lee M, Hahn H, Bredesen DE (1995) Mutations associated with amyotrophic lateral sclerosis convert superoxide dismutase from an antiapoptotic gene to a proapoptotic gene: studies in yeast and neural cells. Proc Natl Acad Sci USA 92:3024-3028.
46. Rink A, Fung K-M, Trojanowski JQ, Lee, V M-Y, Neugebauer E, McIntosh TK (1995) Evidence of apoptotic cell death after experimental traumatic brain injury in the rat. Am J Pathol 147:1575-1583.
47. Schramm M, Eimerl S, Costa E (1990) Serum and depolarizing agents cause acute neurotoxicity in cultured cerebellar granule cells: role of the glutamate receptor responsive to N-methyl-D-aspartate. Proc Natl Acad Sci USA 87:1193-1197.
48. Schulz JB, Weller M, Klockgether T (1996) Potassium deprivation-induced apoptosis of cerebellar granule neurons: a sequential requirement for new mRNA and protein synthesis, ICE-like protease activity, and reactive oxygen species. J Neurosci 16:4696-4706.
49. Tewari M, Quan LT, O'Rourke K, Desnoyers S, Zeng Z, Beidler DR, Dixit VM (1995) Yama/CPP32β, a mammalian homolog of CED-3 is a crmA-inhibitable protease that cleaves the death substrate poly(ADP-ribose) polymerase. Cell 81:801-809.
50. Thangnipon W, Kingsbury A, Webb M, Balazs R (1983) Observations on rat cerebellar cells in vitro: influence of substratum, potassium concentration and relationship between neurones and astrocytes. Dev Brain Res 11:177-189.
51. Thornberry NA, Bull HG, Calaycay JR, Chapman KT, Howard AD, Kostura MJ, Miller DK, Molineaux SM, Weidner JR, Aunins J, Elliston KO, Ayala JM, Casano FJ, Chin J, Ding GJ-F, Egger LA, Gaffney EP, Limjuco G, Palyha OC, Raju SM, Rolando AM, Salley JP, Yamin T-T, Lee TD, Shively JE, MacCross M, Mumford RA, Schmidt JA, Tocci MJ (1992) A novel heterodimeric cysteine protease is required for interleukin-1β processing in monocytes. Nature 356:768-774.
52. Wang L, Miura M, Bergeron L, Zhu H, Yuan J (1994) Ich-1, an Ice/Ced-3-related gene, encodes both positive and negative regulators of programmed cell death. Cell 78:739-750.
53. Wyllie AH (1980) Glucocorticoid-induced thymocyte apoptosis is associated with endogenous endonuclease activation. Nature 284:555-556.
54. Yan G-M, Ni B, Weller M, Wood K, Paul SM (1994) Depolarization or glutamate receptor activation blocks apoptotic cell death of cultured cerebellar granule neurons. Brain Res 656:43-51.
55. Zhu H, Fearnhead HO, Cohen GM (1995) An ICE-like protease is a common mediator of apoptosis induced by diverse stimuli in human monocytic THP.1 cells. FEBS Lett 374:303-308.