Distinct mechanisms of neuronal apoptosis are triggered by antagonism of Bcl-2/Bcl-x(L) versus induction of the BH3-only protein Bim

Journal of Neurochemistry

Volumn 94, Issue 1, 2005, Pages 22-36

  Zimmermann, Angela K ^a   Loucks, F Alexandra ^b   Le, Shoshona S ^b   Butts, Brent D ^a   Florez McClure, Maria L ^a   Bouchard, Ron J ^b   Heidenreich, Kim A ^a,b   Linseman, Daniel A ^a,b  

^a UNIVERSITY OF COLORADO   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Apoptosis; Bcl 2; Bim; Cerebellar granule neuron; Glutathione; Oxidative stress

Indexed keywords

ACETYLCYSTEINE; ANTIOXIDANT; ANTISENSE OLIGONUCLEOTIDE; BH3 PROTEIN; BIM PROTEIN; CASPASE 3; CASPASE 9; GLUTATHIONE; HYBRID PROTEIN; PROTEIN BCL 2; PROTEIN BCL XL;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL DEATH; CELL SURVIVAL; CONFORMATIONAL TRANSITION; DRUG ANTAGONISM; GENE OVEREXPRESSION; GRANULE CELL; MEMBRANE DEPOLARIZATION; NERVE DEGENERATION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN INDUCTION; RAT;

ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; BCL-X PROTEIN; BENZOPYRANS; CARRIER PROTEINS; CELL COUNT; CELLS, CULTURED; DOSE-RESPONSE RELATIONSHIP, DRUG; MEMBRANE PROTEINS; NEURONS; NITRILES; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-BCL-2; RATS; RATS, SPRAGUE-DAWLEY;

EID: 21344460716     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2005.03156.x     Document Type: Article

References (59)

1. An J., Chen Y. and Huang Z. (2004) Critical upstream signals of cytochrome c release induced by a novel Bcl-2 inhibitor. J. Biol. Chem. 279, 19 133-19 140.
2. Bouillet P., Cory S., Zhang L. C., Strasser A. and Adams J. M. (2001) Degenerative disorders caused by Bcl-2 deficiency prevented by loss of its BH3-only antagonist Bim. Dev. Cell 1, 645-653.
3. Bouillet P. and Strasser A. (2002) BH3-only proteins - evolutionarily conserved pro-apoptotic Bcl-2 family members essential for initiating programmed cell death. J. Cell Sci. 115, 1567-1574.
4. Chen J., Freeman A., Liu J., Dai Q. and Lee R. M. (2002) The apoptotic effect of HA14-1, a Bcl-2-interacting small molecular compound, requires Bax translocation and is enhanced by PK11195. Mol. Cancer Ther. 1, 961-967.
5. Cheng E. H., Sheiko T. V., Fisher J. K., Craigen W. J. and Korsmeyer S. J. (2003) VDAC2 inhibits BAK activation and mitochondrial apoptosis. Science 301, 513-517.
6. Coffey E. T., Smiciene G., Hongisto V., Cao J., Brecht S., Herdegen T. and Courtney M. J. (2002) c-Jun N-terminal protein kinase (JNK) 2/3 is specifically activated by stress, mediating c-Jun activation, in the presence of constitutive JNK1 activity in cerebellar neurons. J. Neurosci. 22, 4335-4345.
7. D'Mello S. R., Galli C., Ciotti T. and 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, 10 989-10 993.
8. Degenhardt K., Sundararajan R., Lindsten T., Thompson C. and White E. (2002) Bax and Bak independently promote cytochrome c release from mitochondria. J. Biol. Chem. 277, 14 127-14 134.
9. Dijkers P. F., Medema R. H., Lammers J. W., Koenderman L. and Coffer P. J. (2000) Expression of the pro-apoptotic Bcl-2 family member Bim is regulated by the forkhead transcription factor FKHR-L1. Curr. Biol. 10, 1201-1204.
10. Dispersyn G., Nuydens R., Connors R., Borgers M. and Geerts H. (1999) Bcl-2 protects against FCCP-induced apoptosis and mitochondrial membrane potential depolarization in PC12 cells. Biochim. Biophys. Acta. 1428, 357-371.
11. Ekshyyan O. and Aw T. Y. (2004) Apoptosis in acute and chronic neurological disorders. Front. Biosci. 9, 1567-1576.
12. Enyedy I. J., Ling Y., Nacro K. et al. (2001) Discovery of small-molecule inhibitors of Bcl-2 through structure-based computer screening. J. Med. Chem. 44, 4313-4324.
13. Fiskum G., Starkov A., Polster B. M. and Chinopoulos C. (2003) Mitochondrial mechanisms of neural cell death and neuroprotective interventions in Parkinson's disease. Ann. NY Acad. Sci. 991, 111-119.
14. Gilley J., Coffer P. J. and Ham J. (2003) FOXO transcription factors directly activate Bim gene expression and promote apoptosis in sympathetic neurons. J. Cell Biol. 162, 613-622.
15. Guegan C., Vila M., Rosoklija G., Hays A. P. and Przedborski S. (2001) Recruitment of the mitochondrial-dependent apoptotic pathway in amyotrophic lateral sclerosis. J. Neurosci. 21, 6569-6576.
16. Harris C. A. and Johnson E. M. Jr. (2001) BH3-only Bcl-2 family members are coordinately regulated by the JNK pathway and require Bax to induce apoptosis in neurons. J. Biol. Chem. 276, 37754-37760.
17. Hildeman D. A., Mitchell T., Aronow B., Wojciechowski S., Kappler J. and Marrack P. (2003) Control of Bcl-2 expression by reactive oxygen species. Proc. Natl Acad. Sci. USA 100, 15 035-15 040.
18. Hinds M. G., Lackmann M., Skea G. L., Harrison P. J., Huang D. C. and Day C. L. (2003) The structure of Bcl-w reveals a role for the C-terminal residues in modulating biological activity. EMBO J. 22, 1497-1507.
19. Hochman A., Stemin H., Gorodin S., Korsmeyer S., Ziv I., Melamed E. and Offen D. (1998) Enhanced oxidative stress and altered anti-oxidants in brains of Bcl-2-deficient mice. J. Neurochem. 71, 741-748.
20. Hsu S. Y., Lin P. and Hsueh A. J. (1998) Bod (Bcl-2-related ovarian death gene) is an ovarian BH3-domain-containing pro-apoptotic Bcl-2 protein capable of dimerization with diverse anti-apoptotic Bcl-2 members. Mol. Endocrinol. 12, 1432-1440.
21. Inoue H., Tsukita K., Iwasato T. et al. (2003) The crucial role of caspase-9 in the disease progression of a transgenic ALS mouse model. EMBO J. 22, 6665-6674.
22. Jana N. R., Zemskov E. A., Wang G. and Nukina N. (2001) Altered proteasomal function due to the expression of polyglutamine-expanded truncated N-terminal huntingtin induces apoptosis by caspase activation through mitochondrial cytochrome c release. Hum. Mol. Genet. 10, 1049-1059.
23. Kuida K., Haydar T. F., Kuan C. Y., Gu Y., Taya C., Karasuyama H., Su M. S., Rakic P. and Flavell R. A. (1998) Reduced apoptosis and cytochrome c-mediated caspase activation in mice lacking caspase-9. Cell 94, 325-337.
24. Kushnareva Y. E. and Sokolove P. M. (2000) Pro-oxidants open both the mitochondrial permeability transition pore and a low-conductance channel in the inner mitochondrial membrane. Arch. Biochem. Biophys. 376, 377-388.
25. Li D., Ueta E., Kimura T., Yamamoto T. and Osaki T. (2004) Reactive oxygen species (ROS) control the expression of Bcl-2 family proteins by regulating their phosphorylation and ubiquitination. Cancer Sci. 95, 644-650.
26. Li H., Zhu H., Xu C. J. and Yuan J. ( 1998) Cleavage of Bid by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell 94, 491-501.
27. Linseman D. A., Phelps R. A., Bouchard R. J., Le S. S., Laessig T. A., McClure M. L. and Heidenreich K. A. (2002) Insulin-like growth factor-I blocks Bcl-2 interacting mediator of cell death (Bim) induction and intrinsic death signaling in cerebellar granule neurons. J. Neurosci. 22, 9287-9297.
28. Linseman D. A., Comejo B. J., Le S. S., Meintzer M. K., Laessig T. A., Bouchard R. J. and Heidenreich K. A. (2003) A myocyte enhancer factor 2D (MEF2D) kinase activated during neuronal apoptosis is a novel target inhibited by lithium. J. Neurochem. 85, 1488-1499.
29. Linseman D. A., Butts B. D., Precht T. A., Phelps R. A., Le S. S., Laessig T. A., Bouchard R. J., Florez-McClure M. L. and Heidenreich K. A. (2004) Glycogen synthase kinase-3β phosphorylates Bax and promotes its mitochondrial localization during neuronal apoptosis. J. Neurosci. 24, 9993-10 002.
30. Lossi L. and Merighi A. (2003) In vivo cellular and molecular mechanisms of neuronal apoptosis in the mammalian CNS. Prog. Neurobiol. 69, 287-312.
31. Marani M., Tenev T., Hancock D., Downward J. and Lemoine N. R. (2002) Identification of novel isoforms of the BH3-domain protein Bim which directly activate Bax to trigger apoptosis. Mol. Cell. Biol. 22, 3577-3589.
32. Martinou J. C. and Green D. R. (2001) Breaking the mitochondrial barrier. Nat. Rev. Mol. Cell. Biol. 2, 63-67.
33. Mukherjee S. B., Das M., Sudhandiran G. and Shaha C. (2002) Increase in cytosolic Ca2+ levels through the activation of non-selective cation channels induced by oxidative stress causes mitochondrial depolarization leading to apoptosis-like death in Leishmania donovani promastigotes. J. Biol. Chem. 277, 24 717-24 727.
34. Murphy K. M., Streips U. N. and Lock R. B. (2000) Bcl-2 inhibits a Fas-induced conformational change in the Bax N-terminus and Bax mitochondrial translocation. J. Biol. Chem. 275, 17 225-17 228.
35. Nutt L. K., Pataer A., Pahler J., Fang B., Roth J., McConkey D. J. and Swisher S. G. (2002) Bax and Bak promote apoptosis by modulating endoplasmic reticular and mitochondrial Ca2+ stores. J. Biol. Chem. 277, 9219-9225.
36. Ohga Y., Zirrgiebel U., Hamner S., Michaelidis T. M., Cooper J., Thoenen H. and Lindholm D. (1996) Cell density increases Bcl-2 and Bcl-x expression in addition to survival of cultured cerebellar granule neurons. Neuroscience 73, 913-917.
37. Perez D. and White E. (2000) TNF-α signals apoptosis through a Bid-dependent conformational change in Bax that is inhibited by E1B 19K. Mol. Cell 6, 53-63.
38. Precht T. A., Phelps R. A., Linseman D. A., Butts B. D., Le S. S., Laessig T. A., Bouchard R. J. and Heidenreich K. A. (2005) The permeability transition pore triggers Bax translocation to mitochondria during neuronal apoptosis. Cell Death Diff. 12, 255-265.
39. Putcha G. V., Moulder K. L., Golden J. P., Bouillet P., Adams J. A., Strasser A. and Johnson E. M. Jr (2001) Induction of Bim, a proapoptotic BH3-only Bcl-2 family member, is critical for neuronal apoptosis. Neuron 29, 615-628.
40. Putcha G. V., Harris C. A., Moulder K. L., Easton R. M., Thompson C. B. and Johnson E. M. Jr (2002) Intrinsic and extrinsic pathway signaling during neuronal apoptosis: lessons from the analysis of mutant mice. J. Cell Biol. 157, 441-453.
41. Reimertz C., Kogel D., Rami A., Chittenden T. and Prehn J. H. (2003) Gene expression during ER stress-induced apoptosis in neurons: induction of the BH3-only protein Bbc3/PUMA and activation of the mitochondrial apoptosis pathway. J. Cell Biol. 162, 587-597.
42. Scanlon J. M. and Reynolds I. J. (1998) Effects of oxidants and glutamate receptor activation on mitochondrial membrane potential in rat forebrain neurons. J. Neurochem. 71, 2392-2400.
43. Scorrano L., Oakes S. A., Opferman J. T., Cheng E. H., Sorcinelli M. D., Pozzan T. and Korsmeyer S. J. (2003) Bax and Bak regulation of endoplasmic reticulum Ca2+: a control point for apoptosis. Science 300, 135-139.
44. Slee E. A., Adrain C. and Martin S. J. (1999) Serial killers: ordering caspase activation events in apoptosis. Cell Death Differ. 6, 1067-1074.
45. Strasser A., Puthalakath H., Bouillet P., Huang D. C., O'Connor L., O'Reilly L. A., Cullen L., Cory S. and Adams J. M. (2000) The role of Bim, a pro-apoptotic BH3-only member of the Bcl-2 family in cell-death control. Ann. NY Acad. Sci. 917, 541-548.
46. Sugiyama T., Shimizu S., Matsuoka Y., Yoneda Y. and Tsujimoto Y. (2002) Activation of mitochondrial voltage-dependent anion channel by a pro-apoptotic BH3-only protein Bim. Oncogene 21, 4944-4956.
47. Tatton W. G., Chalmers-Redman R., Brown D. and Tatton N. (2003) Apoptosis in Parkinson's disease: signals for neuronal degradation. Ann. Neurol. 53, S61-S72.
48. Vaudry D., Falluel-Morel A., Leuillet S., Vaudry H. and Gonzalez B. J. (2003) Regulators of cerebellar granule cell development act through specific signaling pathways. Science 300, 1532-1534.
49. Vila M., Jackson-Lewis V., Vukosavic S., Djaldetti R., Liberalere G., Offen D., Korsmeyer S. J. and Przedborski S. (2001) Bax ablation prevents dopaminergic neurodegeneration in the 1-methyl-4-phenyl-1,2,3,6- tetrahydropyridine mouse model of Parkinson's disease. Proc. Natl Acad. Sci. USA 98, 2837-2842.
50. Viswanath V., Wu Y., Boonplueang R., Chen S., Stevenson F. F., Yantiri F., Yang L., Beal M. F. and Andersen J. K. (2001) Caspase-9 activation results in downstream caspase-8 activation and Bid cleavage in 1-methyl-4-phenyl-1,2,3, 6-tetrahydropyridine-induced Parkinson's disease. J. Neurosci. 21, 9519-9528.
51. Voehringer D. W. and Meyn R. E. (2000) Redox aspects of Bcl-2 function. Antioxidants Redox Signaling 2, 537-550.
52. Waldmeier P. C., Zimmermann K., Qian T., Tintelnot-Bolmley M. and Lemasters J. J. (2003) Cyclophilin D as a drug target. Curr. Med. Chem. 10, 1485-1506.
53. Wang J. L., Liu D., Zhang Z. J., Shan S., Han X., Srinivasula S. M., Croce C. M., Alnemri E. S. and Huang Z. (2000) Structure-based discovery of an organic compound that binds Bcl-2 protein and induces apoptosis of tumor cells. Proc. Natl Acad. Sci. USA 97, 7124-7129.
54. Wei M. C., Zong W. X., Cheng E. H., Lindsten T., Panoutsakopoulou V., Ross A. J., Roth K. A., MacGregor G. R., Thompson C. B. and Korsmeyer S. J. (2001) Pro-apoptotic Bax and Bak: a requisite gateway to mitochondrial dysfunction and death. Science 292, 727-730.
55. 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.
56. Wilson-Annan J., O'Reilly L. A., Crawford S. A. et al. (2003) Proapoptotic BH3-only proteins trigger membrane integration of prosurvival Bcl-w and neutralize its activity. J. Cell Biol. 162, 877-887.
57. Yang J., Liu X., Bhalla K., Kim C. N., Ibrado A. M., Cai J., Peng T. I., Jones D. P. and Wang X. (1997) Prevention of apoptosis by Bcl-2: release of cytochrome c from mitochondria blocked. Science 275, 1129-1132.
58. Zong W. X., Lindsten T., Ross A. J., MacGregor G. R. and Thompson C. B. (2001) BH3-only proteins that bind pro-survival Bcl-2 family members fail to induce apoptosis in the absence of Bax and Bak. Genes Dev. 15, 1481-1486.
59. Zou H., Li Y., Liu X. and Wang X. (1999) An APAF-1 cytochrome c multimeric complex is a functional apoptosome that activates procaspase-9. J. Biol. Chem. 274, 11 549-11 556.