Application of proteasomal inhibitors to mouse sympathetic neurons activates the intrinsic apoptotic pathway

Journal of Neurochemistry

Volumn 90, Issue 6, 2004, Pages 1511-1520

  Lang Rollin, Isabelle ^a   Vekrellis, Konstantinos ^b   Wang, Qiaohong ^a   Rideout, Hardy J ^c   Stefanis, Leonidas ^a,b  

^a Och Spine at New York Presbyterian Hospitals   (United States)

^b BIOMEDICAL RESEARCH FOUNDATION   (Greece)

^c IIBEAA ^*

Author keywords

Bax; Caspase; Cell death; Parkinson's disease; Proteasome; Ubiquitin

Indexed keywords

BH3 PROTEIN; BIM PROTEIN; CASPASE 3; CYTOCHROME C; PROTEASOME INHIBITOR; PROTEIN BAX; PROTEIN BCL 2;

ANIMAL CELL; APOPTOSIS; ARTICLE; CATECHOLAMINE NERVE CELL; CELL DEATH; CELL SURVIVAL; CONTROLLED STUDY; DEGENERATIVE DISEASE; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME RELEASE; GENE CONTROL; GENE DELETION; GENE OVEREXPRESSION; LEWY BODY; MOUSE; NERVE CELL CULTURE; NEUROPATHOLOGY; NEUROPROTECTION; NEWBORN; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN FAMILY; SYMPATHETIC NERVE CELL;

ACETYLCYSTEINE; ANIMALS; ANIMALS, NEWBORN; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; BCL-2-ASSOCIATED X PROTEIN; BLOTTING, WESTERN; CARRIER PROTEINS; CASPASE 3; CASPASES; CELL SURVIVAL; CELLS, CULTURED; CYSTEINE ENDOPEPTIDASES; CYSTEINE PROTEINASE INHIBITORS; CYTOCHROMES C; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG INTERACTIONS; ENZYME INHIBITORS; GANGLIA, SYMPATHETIC; GENES, BCL-2; GREEN FLUORESCENT PROTEINS; IMMUNOHISTOCHEMISTRY; LUMINESCENT PROTEINS; MEMBRANE PROTEINS; MICE; MICE, KNOCKOUT; MULTIENZYME COMPLEXES; NEURONS; OLIGOPEPTIDES; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-BCL-2; RHODAMINES; SIGNAL TRANSDUCTION; TIME FACTORS; UBIQUITIN;

ANIMALIA;

EID: 4544287486     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2004.02684.x     Document Type: Article

References (55)

1. Adams J. M. and Cory S. (2001) Life-or-death decisions by the Bcl-2 protein family. Trends Biochem. Sci. 26, 61-66.
2. Akiyama T., Bouillet P., Miyazaki T., Kadono Y., Chikuda H., Chung U. I., Fukuda A., Hikita A., Seto H., Okada T. et al. (2003) Regulation of osteoclast apoptosis by ubiquitylation of proapoptotic BH3-only Bcl-2 family member Bim. EMBO J. 22, 6653-6664.
3. Biswas S. C. and Greene L. A. (2002) Nerve growth factor (NGF) down-regulates the Bcl-2 homology 3 (BH3) domain-only protein Bim and suppresses its proapoptotic activity by phosphorylation. J. Biol. Chem. 277, 49511-49516.
4. Bossy-Wetzel E. and Green D. R. (1999) Caspases induce cytochrome c release from mitochondria by activating cytosolic factors. J. Biol. Chem. 274, 17484-17490.
5. Bredesen D. E. (2000) Apoptosis: overview and signal transduction pathways. J. Neurotrauma 17, 801-810.
6. Breitschopf K., Zeiher A. M. and Dimmeler S. (2000) Ubiquitin-mediated degradation of the proapoptotic active form of bid. A functional consequence on apoptosis induction. J. Biol. Chem. 275, 21648-21652.
7. Bush K. T., Goldberg A. L. and Nigam S. K. (1997) Proteasome inhibition leads to a heat-shock response, induction of endoplasmic reticulum cheperones, and thermotolerance. J. Biol. Chem. 272, 9086-9092.
8. Canu N., Barbato C., Ciotti M. T., Serafino A., Dus L. and Calissano P. (2000) Proteasome involvement and accumulation of ubiquitinated proteins in cerebellar granule neurons undergoing apoptosis. J. Neurosci. 20, 589-599.
9. Chung K. K., Dawson V. L. and Dawson T. M. (2001) The role of the ubiquitin-proteasomal pathway in Parkinson's disease and other neurodegenerative disorders. Trends Neurosci. 24, S7-S14.
10. Ciechanover A. (1998) The ubiquitin-proteasome pathway: on protein death and cell life. EMBO J. 17, 7151-7160.
11. Deckwerth T. L., Elliott J. L., Knudson C. M., Johnson E. M. Jr, Snider W. D. and Korsmeyer S. J. (1996) BAX is required for neuronal death after trophic factor deprivation and during development. Neuron 17, 401-411.
12. Dewson G., Snowden R. T., Almond J. B., Dyer M. J. and Cohen G. M. (2003) Conformational change and mitochondrial translocation of Bax accompany proteasome inhibitor-induced apoptosis of chronic lymphocytic leukemic cells. Oncogens 22, 2643-2654.
13. Dietrich P., Rideout H. J., Wang Q. and Stefanis L. (2003) Lack of p53 delays apoptosis, but increases ubiquitinated inclusions, in proteasomal inhibitor-treated cultured cortical neurons. Mol. Cell Neurosci. 24, 430-441.
14. Dimmeler S., Breitschopf K., Haendeler J. and Zeiher A. M. (1999) Dephosphorylation targets Bcl-2 for ubiquitin-dependent degradation: a link between the apoptosome and the proteasome pathway. J. Exp. Med. 189, 1815-1822.
15. Fenteany G., Standaert R. F., Reichard G. A., Corey E. J. and Schreiber S. L. (1994) A β-lactone related to lactacystin induces neurite outgrowth in a neuroblastoma cell line and inhibits cell cycle progression in an osteosarcoma cell line. Proc. Natl Acad. Sci. USA 91, 3358-3362.
16. Figueiredo-Pereira M., Berg K. 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.
17. Giasson B. I., Bruening W., Durham H. D. and Mushynski W. E. (1999) Activation of stress-activated protein kinases correlates with neurite outgrowth induced by proteasomal inhibition in PC12 cells. J. Neurochem. 72, 1081-1087.
18. Iwanaga K., Wakabayashi K., Yoshimoto M., Tomita I., Satoh H., Takashima H., Satoh A., Seto M., Tsujihata M. and Takahashi H. (1999) Lewy body-type degeneration in cardiac plexus in Parkinson's and incidental Lewy body diseases. Neurology. 52, 1269-1271.
19. Kikuchi S., Shinpo K., Tsuji S., Takeuchi M., Yamagishi S., Makita Z., Niino M., Yabe I. and Tashiro K. (2003) Effect of proteasome inhibitor on cultured mesencephalic dopaminergic neurons. Brain Res. 964, 228-236.
20. Kisselev A. F. and Goldberg A. L. (2001) Proteasome inhibitors: from research tools to drug candidates. Chem. Biol. 8, 739-758.
21. Kitagawa H., Tani E., Ikemoto H., Ozaki I., Nakano A. and Omura S. (1999) Proteasome inhibitors induce mitochondria-independent apoptosis in human glioma cells. FEBS Lett. 443, 181-186.
22. Lang-Rollin I., Rideout H. and Stefanis L. (2003) Ubiquitinated inclusions and neuronal cell death. Histol. Histopathol. 18, 509-517.
23. Li B. and Dou Q. P. (2000) Bax degradation by the ubiquitin/proteasome- dependent pathway: involvement in tumor survival and progression. Proc. Natl Acad. Sci. USA 97, 3850-3855.
24. Lin K. I., Baraban J. M. and Ratan R. R. (1998) Inhibition versus induction of apoptosis by proteasome inhibitors depends on concentration. Cell Death Differ. 5, 577-583.
25. Lopes U., Ernhardt P., Yao R. and Cooper G. (1997) p53-dependent induction of apoptosis by proteasome inhibitors. J. Biol. Chem. 272, 12893-12896.
26. Luciano F., Jacquel A., Colosetti P., Herrant M., Cagnol S., Pages G. and Auberger P. (2003) Phosphorylation of Bim-EL by Erk1/2 on serine 69 promotes its degradation via the proteasome pathway and regulates its proapoptotic function. Oncogene 22, 6785-6793.
27. MacFarlane M., Merrison W., Bratton S. B. and Cohen G. M. (2002) Proteasome-mediated degradation of Smac during apoptosis: XIAP promotes Smac ubiquitination in vitro. J. Biol. Chem. 277, 36611-36616.
28. McNaught K. S., Olanow C. W., Halliwell B., Isacson O. and Jenner P. (2001) Failure of the ubiquitin-proteasome system in Parkinson's disease. Nature Rev. Neurosci. 2, 589-594.
29. McNaught K. S., Mytilineou C., Jnobaptiste R., Yabut J., Shashidharan P., Jenner P. and Olanow C. W. (2002) Impairment of the ubiquitin-proteasome system causes dopaminergic cell death and inclusion body formation in ventral mesencephalic cultures. J. Neurochem. 81, 301-306.
30. Morris E. J., Keramaris E., Rideout H. J., Slack R. S., Dyson N. J., Stefanis L. and Park D. S. (2001) Cyclin-dependent kinases and P53 pathways are activated independently and mediate Bax activation in neurons after DNA damage. J. Neurosci. 21, 5017-5026.
31. O'Connor L., Strasser A., O'Reilly L. A., Hausmann G., Adams J. M., Cory S. and Huang D. C. (1998) Bim: a novel member of the Bcl-2 family that promotes apoptosis. EMBO J. 17, 384-395.
32. Ostrowska H., Wojcik C., Wilk S., Omura S., Kozlowski L., Stoklosa T., Worowski K. and Radziwon P. (2000) Separation of cathepsin A-like enzyme and the proteasome: evidence that lactacystin/beta-lactone is not a specific inhibitor of the proteasome. Int. J. Biochem. Cell Biol. 32, 747-757.
33. Pasquini L. A., Moreno M. B., Adamo A. M., Pasquini J. M. and Soto E. (2000) Lactacystin, a specific inhibitor of the proteasome, induces apoptosis and activates caspase-3 in cultured cerebellar granule cells. J. Neurosci. Res. 59, 601-611.
34. Petrucelli L., O'Farrell C., Lockhart P. J., Baptista M., Kehoe K., Vink L., Choi P., Wolozin B., Farrer M., Hardy J. and Cookson M. R. (2002) Parkin protects against the toxicity associated with mutant alpha-synuclein: proteasome dysfunction selectively affects catecholaminergic neurons. Neuron 36, 1007-1019.
35. Putcha G. V., Deshmukh M. and Johnson E. M. Jr (1999) BAX translocation is a critical event in neuronal apoptosis: regulation by neuroprotectants, BCL-2, and caspases. J. Neurosci. 19, 7476-7485.
36. Putcha G. V., Moulder K. L., Golden J. P., Bouillet P., Adams J. A., Strasser A. and Johnson E. M. (2001) Induction of BIM, a proapoptotic BH3-only BCL-2 family member, is critical for neuronal apoptosis. Neuron 29, 615-628.
37. Qiu J. H., Asai A., Chi S., Saito N., Hamada H. and Kirino T. (2000) Proteasome inhibitors induce cytochrome c-caspase-3-like protease- mediated apoptosis in cultured cortical neurons. J. Neurosci. 20, 259-265.
38. Rideout H. J. and Stefanis L. (2001) Caspase inhibition: a potential therapeutic strategy in neurological diseases. Histol. Histopathol. 16, 895-908.
39. Rideout H. J. and Stefanis L. (2002) Proteasomal inhibition-induced inclusion formation and death in cortical neurons require transcription and ubiquitination. Mol Cell Neurosci. 21, 223-238.
40. Rideout H. J., Wang Q., Park D. S. and Stefanis L. (2003) Cyclin-dependent kinase activity is required for apoptotic death but not inclusion formation in cortical neurons after proteasomal inhibition. J. Neurosci. 23, 1237-1245.
41. Rideout H. J., Larsen K. L., Sulzer D. and Stefanis L. (2001a) Proteasomal inhibition leads to formation of ubiquitin/α-Synuclein- immunoreactive inclusions in PC12 Cells. J. Neurochem. 78, 899-908.
42. Rideout H. J., Zang E., Yeasmin M., Gordon R., Jabado O., Park D. S. and Stefanis L. (2001b) Inhibitors of trypsin-like serine proteases prevent DNA damage-induced neuronal death by acting upstream of the mitochondrial checkpoint and of p53 induction. Neuroscience 107, 339-352.
43. Sadoul R., Fernandez P. A., Quiquerez A. L., Martinou I., Maki M., Schroter M., Becherer J. D., Irmler M., Tschopp J. and Martinou J. C. (1996) Involvement of the proteasome in the programmed cell death of NGF-deprived sympathetic neurons. EMBO J. 15, 3845-3852.
44. Stefanis L., Troy C. M., Qi H. and Greene L. A. (1997) Inhibitors of trypsin-like serine proteases inhibit processing of the caspase Nedd-2 and protect PC12 cells and sympathetic neurons from death evoked by withdrawal of trophic support. J. Neurochem. 69, 1425-1437.
45. Stefanis L., Park D. S., Friedman W. J. and Greene L. A. (1999) Caspase-dependent and - independent death of camptothecin-treated embryonic cortical neurons. J. Neurosci. 19, 6235-6247.
46. Stefanis L., Larsen K. L., Rideout H. J., Sulzer D. S. and Greene L. A. (2001) Expression of A53T mutant, but not wild type, α-synuclein in PC12 cells induces alterations of the ubiquitin-dependent degradation system, loss of dopamine release, and autophagic cell death. J. Neurosci. 21, 9549-9560.
47. Tanaka Y, Engelender S., Igarashi S., Rao R. K., Wanner T., Tanzi R. E., Sawa A. L., Dawson V., Dawson T. M. and Ross C. A. (2001) Inducible expression of mutant alpha-synuclein decreases proteasome activity and increases sensitivity to mitochondria-dependent apoptosis. Hum. Mol. Genet. 10, 919-926.
48. Tofaris G. K., Layfield R. and Spillantini M. G. (2001) alpha-synuclein metabolism and aggregation is linked to ubiquitin-independent degradation by the proteasome. FEBS Lett. 509, 22-26.
49. Troy C. M., Stefanis L., Prochiantz A., Greene L. A. and Shelanski M. L. (1996) The contrasting roles of ICE family proteases and interleukin-1beta in apoptosis induced by trophic factor withdrawal and by copper/zinc superoxide dismutase down-regulation. Proc. Natl Acad. Sci. USA 93, 5635-5640.
50. Troy C. M., Rabacchi S. A., Friedman W. J., Frappier T. F., Brown K. and Shelanski M. L. (2000) Caspase-2 mediates neuronal cell death induced by beta-amyloid. J. Neurosci. 20, 1386-1392.
51. Urushitani M., Kurisu J., Tsukita K. and Takahashi R. (2002) Proteasomal inhibition by misfolded mutant superoxide dismutase 1 induces selective motor neuron death in familial amyotrophic lateral sclerosis. J. Neurochem. 83, 1030-1042.
52. Valentijn A. J., Metcalfe A. D., Kott J., Streuli C. H. and Gilmore A. P. (2003) Spatial and temporal changes in Bax subcellular localization during anoikis. J. Cell Biol. 162, 599-612.
53. Wakabayashi K. and Takahashi H. (1997) Neuropathology of autonomic nervous system in Parkinson's disease. Eur. Neurol. 38, 2-7.
54. Whitfield J., Neame S. J., Paquet L., Bernard O. and Ham J. (2001) Dominant-negative c-Jun promotes neuronal survival by reducing BIM expression and inhibiting mitochondrial cytochrome c release. Neuron 29, 629-643.
55. Zhai Q., Wang J., Kim A., Liu Q., Watts R., Hoopfer E., Mitchison T., Luo L. and He Z. (2003) Involvement of the ubiquitin-proteasome system in the early stages of wallerian degeneration. Neuron. 39, 217-225.