Involvement of the proteasome in the programmed cell death of NGF-deprived sympathetic neurons

EMBO Journal

Volumn 15, Issue 15, 1996, Pages 3845-3852

  Sadoul, Rémy ^a   Fernandez, Pierre Alain ^a   Quiquerez, Anne Lise ^a   Martinou, Isabelle ^a   Maki, Masatoshi ^b   Schröter, Michael ^c   Becherer, J David ^a   Irmler, Martin ^c   Tschopp, Jurg ^c   Martinou, Jean Claude ^a  

^a GLAXOSMITHKLINE   (United States)

^b KYOTO UNIVERSITY   (Japan)

^c UNIVERSITY OF LAUSANNE   (Switzerland)

Author keywords

Interleukin 1 converting enzyme; Nerve growth factor; Programmed cell death; Proteasome; Sympathetic neurons

Indexed keywords

INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; NERVE GROWTH FACTOR; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PROTEASOME;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL DEATH; CELL SURVIVAL; CONTROLLED STUDY; MACROPHAGE; MOUSE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PROCESSING; RAT; SYMPATHETIC NERVE CELL;

ANIMALIA;

EID: 9544239345     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1002/j.1460-2075.1996.tb00758.x     Document Type: Article

References (58)

1. Alkalay, I., Yaron, A., Hatzubai, A., Orian, A. and Ciechanover, A. (1995) Stimulation-dependent IκBa phosphorylation marks the NF-κB inhibitor for degradation via the ubiquitin-proteasome pathway. Proc. Natl Acad. Sci. USA, 92, 10599-10603.
2. Barr, P.J. (1991) Mammalian subtilisins: the long sought dibasic processing endoproteases. Cell, 66, 1-3.
3. Barrett, A.J. (1981) Cystatin, the egg white inhibitor of cysteine proteinases. Methods Enzymol., 80, 771-778.
4. Bump, N.J. et al. (1995) Inhibition of ICE family proteases by baculovirus antiapoptotic protein P35. Science, 269, 1885-1888.
5. Clarke, P.G. (1985) Neuronal death during development in the isthmooptic nucleus of the chick: sustaining role of afferents from the tectum. J. Comp. Neurol., 234, 365-379.
6. de Murcia, G. and Menissier de Murcia, J. (1994) Poly(ADP-ribose) polymerase: a molecular nick-sensor. Trends Biochem. Sci., 19, 172-176.
7. Ellis, R.E., Yuan, J. and Horvitz, H.R. (1991) Mechanisms and functions of cell death. Annu. Rev. Cell Biol., 7, 663-698.
8. Fenteany, G., Standaert, R.F., Lane, W.S., Choi, S., Corey, E.J. and Schreiber, S.L. (1995) Inhibition of proteasome activities and subunit-specific amino-terminal threonine modification by lactacystin. Science, 268, 726-731.
9. Figueiredo-Pereira, M.E., Berg, K.A. and Wilk, S. (1994) A new inhibitor of the chymotrypsin-like activity of the multicatalytic proteinase complex (20S proteasome) induces accumulation of ubiquitin-protein conjugates in a neuronal cell. J. Neurochem., 63, 1578-1581.
10. Gagliardini, V., Fernandez, P.-A., Lee, R.K.K., Drexler, H.C.A., Rotello, R.J., Fishman, M.C. and Yuan, J. (1994) Prevention of vertebrate neuronal death by the crmA gene. Science, 263, 826-828.
11. Garcia, I., Martinou, I., Tsujimoto, Y. and Martinou, J.C. (1992) Prevention of programmed cell death of sympathetic neurons by the bcl-2 proto-oncogene. Science, 258, 302-304.
12. Glotzer, M., Murray, A.W. and Kirschner, M.W. (1991) Cyclin is degraded by the ubiquitin pathway. Nature, 349, 132-138.
13. Glucksman, A. (1951) Cell deaths in normal vertebrate ontogeny. Cambridge Philos. Soc. Biol. Rev., 26, 59-86.
14. Goldberg, A.L. and Rock, K.L. (1992) Proteolysis, proteasomes and antigen presentation. Nature, 357, 375-379.
15. Grimm, L.M., Goldberg, A.L., Poirier, G.G., Schwartz, L.M. and Osborne, B.A. (1996) Proteasomes play an essential role in thymocyte apoptosis. EMBO J., 15, 3835-3844.
16. Grune, T., Reinheckel, T., Joshi, M. and Davies, K.J. (1995) Proteolysis in cultured liver epithelial cells during oxidative stress. Role of the multicatalytic proteinase complex, proteasome. J. Biol. Chem., 270, 2344-2351.
17. Gu, Y., Sarnecki, C., Aldape, R.A., Livingston, D.J. and Su, M.S. (1995) Cleavage of poly(ADP-ribose) polymerase by interleukin-1 beta converting enzyme and its homologs TX and Nedd-2. J. Biol. Chem., 270, 18715-18718.
18. Hershko, A. and Ciechanover, A. (1992) The ubiquitin system for protein degradation. Annu. Rev. Biochem., 61, 761-807.
19. Hogquist, K.A., Nett, M.A., Unanue, E.R. and Chaplin, D.D. (1991) Interleukin 1 is processed and released during apoptosis. Proc. Natl Acad. Sci. USA, 88, 8485-8489.
20. Inoue, S., Bar-Nun, S., Roitelman, J. and Simoni, R.D. (1991) Inhibition of degradation of 3-hydroxy-3-methylglutaryl-coenzyme A reductase in vivo by cysteine protease inhibitors. J. Biol. Chem., 266, 13311-13317.
21. Jones, M.E., Haire, M.F., Kloetzel, P.M., Mykles, D.L. and Schwartz, L.M. (1995) Changes in the structure and function of the multicatalytic proteinase (proteasome) during programmed cell death in the intersegmental muscles of the hawkmoth, Manduca sexta. Dev. Biol., 169, 436-447.
22. Kumar, S. and Harvey, N.L. (1995) Role of multiple cellular proteases in the execution of programmed cell death. FEBS Lett., 375, 169.
23. Lazebnik, Y.A., Kaufmann, S.H., Desnoyers, S., Poirier, G.G. and Earnshaw, W.C. (1994) Cleavage of poly(ADP-ribose) polymerase by a proteinase with properties like ICE. Nature, 371, 346-347.
24. Li, P. et al. (1995) Mice deficient in IL-1 beta-converting enzyme are defective in production of mature IL-1 beta and resistant to endotoxic shock. Cell, 80, 401-411.
25. Maki, M., Takano, E., Osawa, T., Ooi, T., Murachi, T. and Hatanaka, M. (1988) Analysis of stucture-function relationship of pig Calpastatin by expression of mutated cDNAs in Escherichia coli. J. Biol. Chem., 263, 10254-10261.
26. Maki, M., Ma, H., Takano, E., Adachi, Y., Lee, W.J., Hatanaka, M. and Murachi, T. (1991) Calpastatins: biochemical and molecular biological studies. Biomed. Biochim. Acta, 50, 509-516.
27. Martin, D.P., Ito, A., Horigome, K., Lampe, P.A. and Johnson, J.E.M. (1992) Biochemical characterization of programmed cell death in NGF-deprived sympathetic neurons. J. Neurobiol., 23, 1205-1220.
28. Martinou, I., Fernandez, P.A., Missotten, M., White, E., Allet, B., Sadoul, R. and Martinou, J.C. (1995) Viral proteins E1B19K and p35 protect sympathetic neurons from cell death induced by NGF deprivation. J. Cell Biol., 128, 201-208.
29. Mazzei, G., Winger, L., Osen-Sand, A., Bernasconi, L.M., Benotto, W. and Shaw, A.R. (1990) Interleukin-1 alpha, a major component of fetal calf serum: artifacts in IL-1 bioassays. In The Physiological and Pathologicals Effects of Cytokines. Wiley-Liss, UK, pp.13-17.
30. Molineaux, S.M. et al. (1993) Interleukin 1 beta (IL-1 beta) processing in murine macrophages requires a structurally conserved homologue of human IL-1 beta converting enzyme. Proc. Natl Acad. Sci. USA, 90, 1809-1813.
31. Mosmann, T. (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods, 65, 55-63.
32. Nicholson, D.N. et al. (1995) Identification and inhibition of the ICE/ CED-3 protease necessary for mammalian apoptosis. Nature, 376, 37-43.
33. Omura, S., Fujimoto, T., Otoguro, K., Matsuzaki, K., Moriguchi, R., Tanaka, H. and Sasaki, Y. (1991) Lactacystin, a novel microbial metabolite, induces neuritogenesis of neuroblastoma cells. J. Antibiot., 44, 113-117.
34. Oppenheim, R.W. (1991) Cell death during development of the nervous system. Annu. Rev. Neurosci., 14, 453-501.
35. Pacifici, R.E., Kono, Y. and Davies, K.J. (1993) Hydrophobicity as the signal for selective degradation of hydroxyl radical-modified hemoglobin by the multicatalytic proteinase complex, proteasome. J. Biol. Chem., 268, 15405-15411.
36. Pagano, M., Tam, S.W., Theodoras, A.M., Beer-Romero, P., Del Sal, G., Chau, V., Yew, P.R., Draetta, G.F. and Rolfe, M. (1995) Role of the ubiquitin-proteasome pathway in regulating abundance of the cyclin-dependent kinase inhibitor p27. Science, 269, 682-685.
37. Palombella, V.J., Rando, O.J., Goldberg, A.L. and Maniatis, T. (1994) The ubiquitin-proteasome pathway is required for processing the NF-kappa B1 precursor protein and the activation of NF-kappa B. Cell, 78, 773-785.
38. Peters, J.M. (1994) Proteasomes: protein degradation machines of the cell. Trends Biochem. Sci., 19, 377-382.
39. Raff, M.C., Barres, B.A., Burne, J.F., Coles, H.S., Ishizaki, Y. and Jacobson, M.D. (1993) Programmed cell death and the control of cell survival: lessons from the nervous system. Science, 262, 695-700.
40. Ray, C.A., Black, R.A., Kronheim, S.R., Greenstreet, T.A., Sleath, P.R., Salvesen, G.S. and Pickup, D. (1992) Viral inhibition of inflammation: cowpox virus encodes an inhibitor of the interleukin-1β converting enzyme. Cell, 69, 597-604.
41. Roberts-Lewis, J.M., Savage, M.J., Marcy, V.R., Pinsker, L.R. and Siman, R. (1994) Immunolocalization of calpain I-mediated spectrin degradation to vulnerable neurons in the ischemic gerbil brain. J. Neurosci., 14, 3934-3944.
42. Rock, K.L., Gramm, C., Rothstein, L., Clark, K., Stein, R., Dick, L., Hwang, D. and Goldberg, A.L. (1994) Inhibitors of the proteasome block the degradation of most cell proteins and the generation of peptides presented on MHC class I molecules. Cell, 78, 761-771.
43. Siman, R. and Noszek, J.C. (1988) Excitatory amino acids activate calpain I and induce structural protein breakdown in vivo. Neuron, 1, 279-287.
44. Squier, M.K., Miller, A.C., Malkinson, A.M. and Cohen, J.J. (1994) Calpain activation in apoptosis. J. Cell Physiol., 159, 229-237.
45. Tewari, M., Quan, L.T., O'Rourke, K., Desnoyers, S., Zeng, Z., Beidler, D.R., Poirier, G.G., Salvesen, G.S. and Dixit, V.M. (1995) Yama/CPP32 beta, a mammalian homolog of CED-3, is a CrmA-inhibitable protease that cleaves the death substrate poly(ADP-ribose) polymerase. Cell, 81, 801-809.
46. Thornberry, N.A. et al. (1992) A novel heterodimeric cysteine protease is required for interleukin-1 beta processing in monocytes. Nature, 356, 768-774.
47. Thornberry, N.A., Peterson, E.P., Zhao, J.J., Howard, A.D., Griffin, P.R. and Chapman, K.T. (1994) Inactivation of interleukin-1 beta converting enzyme by peptide (acyloxy)methyl ketones. Biochemistry, 33, 3934-3940.
48. Treier, M., Staszewski, L.M. and Bohmann, D. (1994) Ubiquitin-dependent c-Jun degradation in vivo is mediated by the delta domain. Cell, 78, 787-798.
49. Tsubuki, S., Kawasaki, H., Saito, Y., Miyashita, N., Inomata, M. and Kawashima, S. (1993) Purification and characterization of a Z-Leu-Leu-Leu-MCA degrading protease expected to regulate neurite formation: a novel catalytic activity in proteasome. Biochem. Biophys. Res. Commun., 196, 1195-1201.
50. Tsujinaka, T., Kajiwara, Y., Kambayashi, J., Sakon, M., Higuchi, N., Tanaka, T. and Mori, T. (1988) Synthesis of a new cell penetrating calpain inhibitor (Calpeptin). Biochem. Biophys. Res. Commun., 153, 1201-1208.
51. Vinitsky, A., Michaud, C., Powers, J.C. and Orlowski, M. (1992) Inhibition of the chymotrypsin-like activity of the pituitary multicatalytic proteinase complex. Biochemistry, 31, 9421-9428.
52. Walker, N.P. et al. (1994) Crystal structure of the cysteine protease interleukin-1 beta-converting enzyme: a (p20/p10)2 homodimer. Cell, 78, 343-352.
53. Ward, C.L., Omura, S. and Kopito, R.R. (1995) Degradation of CFTR by the ubiquitin-proteasome pathway. Cell, 83, 121-127.
54. Wilcox, D. and Mason, R.W. (1992) Inhibition of cysteine proteinases in lysosomes and whole cells. Biochem. J., 285, 495-502.
55. Wil, .S. and Figueiredo-Pereira, M.E. (1993) Synthetic inhibitors of the multicatalytic proteinase complex (proteasome). Enzyme Protein, 47, 306-313.
56. Xue, D. and Horvitz, H.R. (1995) Inhibition of the Caenorhabditis elegans cell-death protease CED-3 by a CED-3 cleavage site in baculovirus p35 protein. Nature, 377, 248-251.
57. Yuan, J. (1995) Molecular control of life and death. Curr. Opin. Cell Biol., 7, 211-214.
58. Yuan, J., Shaham, S., Ledoux, S., Ellis, H.M. and Horvitz, H.R. (1993) The C.elegans cell death gene ced-3 encodes a protein similar to mammalian interleukin-1β-converting enzyme. Cell, 75, 641-652.