'Men are but worms:' Neuronal cell death in C. elegans and vertebrates

Cell Death and Differentiation

Volumn 11, Issue 1, 2004, Pages 38-48

  Putcha, G V ^a,b   Johnson Jr , Eugene M ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Bcl 2; Caspase; Kinase; Mitochondria; Neurotrophin; Transcription factor

Indexed keywords

ADAPTOR PROTEIN; APOPTOTIC PROTEASE ACTIVATING FACTOR 1; BH3 PROTEIN; BIM PROTEIN; CASPASE; CEP 1347; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN BAX; PROTEIN BCL 2; PROTEIN BCL W; PROTEIN BCL XL; PROTEIN MCL 1; SECOND MITOCHONDRIAL ACTIVATOR OF CASPASE; STRESS ACTIVATED PROTEIN KINASE;

ALZHEIMER DISEASE; APOPTOSIS; CAENORHABDITIS ELEGANS; CELL LINEAGE; DEGENERATIVE DISEASE; ENZYME ACTIVATION; GENE CONTROL; GENETIC REGULATION; GENETIC TRANSCRIPTION; HUMAN; NEMATODE; NERVE CELL DEGENERATION; NERVE CELL DIFFERENTIATION; NERVE CELL NECROSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN INTERACTION; REVIEW; SIGNAL TRANSDUCTION; SYMPATHETIC NERVE CELL; VERTEBRATE; WORM;

ANIMALS; APOPTOSIS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; NEURODEGENERATIVE DISEASES; NEURONS; SIGNAL TRANSDUCTION; VERTEBRATES;

CAENORHABDITIS ELEGANS; VERTEBRATA;

EID: 1642514774     PISSN: 13509047     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.cdd.4401352     Document Type: Review

References (133)

1. Kerr JF, Wyllie AH and Currie AR (1972) Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br. J. Cancer 26: 239-257
2. Zimmermann KC, Ricci JE, Droin NM and Green DR (2002) The role of ARK in stress-induced apoptosis in Drosophila cells. J. Cell Biol. 156: 1077-1087
3. Deshmukh M and Johnson Jr EM (1998) Evidence of a novel event during neuronal death: development of competence-to-die in response to cytoplasmic cytochrome c. Neuron 21: 695-705
4. Wiese S, Digby MR, Gunnersen JM, Gotz R, Pei G, Holtmann B, Lowenthal J and Sendtner M (1999) The anti-apoptotic protein ITA is essential for NGF-mediated survival of embryonic chick neurons. Nat. Neurosci. 2: 978-983
5. Stefanis L, Park DS, Friedman WJ and Greene LA (1999) Caspase-dependent and -independent death of camptothecin-treated embryonic cortical neurons. J. Neurosci. 19: 6235-6247
6. Deshmukh M and Johnson Jr EM (2000) Caspase inhibition extends the commitment to neuronal death beyond cytochrome c release to the point of mitochondrial depolarization. J. Cell Biol. 150: 131-143
7. Deshmukh M, Du C, Wang X and Johnson Jr EM (2002) Exogenous Smac induces competence and permits caspase activation in sympathetic neurons. J. Neurosci. 22: 8018-8027
8. Chang LK, Putcha GV, Deshmukh M and Johnson EM (2002) Mitochondrial involvement in the point of no return in neuronal apoptosis. Biochimie 84: 223-231
9. Chang LK, Schmidt RE and Johnson Jr EM (2003) Alternating metabolic pathways in NGF-deprived sympathetic neurons affect caspase-independent death. J. Cell Biol. 162: 245-256
10. Adams JM and Cory S (2001) Life-or-death decisions by the Bcl-2 protein family. Trends Biochem. Sci. 26: 61-66
11. Borner C, Martinou I, Mattmann C, Irmler M, Schaerer E, Martinou JC and Tschopp J (1994) The protein Bcl-2 alpha does not require membrane attachment, but two conserved domains to suppress apoptosis. J. Cell Biol. 126: 1059-1068
12. Borner C, Olivier R, Martinou I, Mattmann C, Tschopp J and Martinou JC (1994) Dissection of functional domains in Bcl-2 alpha by site-directed mutagenesis. Biochem. Cell Biol. 72: 463-469
13. Sedlak TW, Oltvai ZN, Yang E, Wang K, Boise LH, Thompson CB and Korsmeyer SJ (1995) Multiple Bcl-2 family members demonstrate selective dimerizations with Bax. Proc. Natl. Acad. Sci. USA 92: 7834-7838
14. Yin XM, Oltvai ZN and Korsmeyer SJ (1994) BH1 and BH2 domains of Bcl-2 are required for inhibition of apoptosis and heterodimerization with Bax. Nature 369: 321-323
15. Boyd JM, Gallo GJ, Elangovan B, Houghton AB, Malstrom S, Avery BJ, Ebb RG, Subramanian T, Chittenden T and Lutz RJ (1995) Bik, a novel death-inducing protein shares a distinct sequence motif with Bcl-2 family proteins and interacts with viral and cellular survival-promoting proteins. Oncogene 11: 1921-1928
16. Wang K, Yin XM, Chao DT, Milliman CL and Korsmeyer SJ (1996) Bid: a novel BH3 domain-only death agonist. Genes Dev. 10: 2859-2869
17. Inohara N, Ding LY, Chen S and Nunez G (1997) Harakiri, a novel regulator of cell death, encodes a protein that activates apoptosis and interacts selectively with survival-promoting proteins Bcl-2 and Bcl-X-L. EMBO J. 16: 1686-1694
18. Kelekar A, Chang BS, Harlan JE, Fesik SW and Thompson CB (1997) Bad is a BH3 domain-containing protein that forms an inactivating dimer with Bcl-X-L. Mol. Cell. Biol. 17: 7040-7046
19. Sattler M, Liang H, Nettesheim D, Meadows RP, Harlan JE, Eberstadt M, Yoon HS, Shuker SIB, Chang BS, Minn AJ, Thompson CB and Fesik SW (1997) Structure of Bcl-X-L-Bak peptide complex: recognition between regulators of apoptosis. Science 275: 983-986
20. Petros AM, Nettesheim DG, Wang Y, Olejniczak ET, Meadows RP, Mack J, Swift K, Matayoshi ED, Zhang H, Thompson CB and Fesik SW (2000) Rationale for Bcl-X-L/Bad peptide complex formation from structure, mutagenesis, and biophysical studies. Protein Sci. 9: 2528-2534
21. Liu X, Dai S, Zhu Y, Marrack P and Kappler JW (2003) The structure of a Bcl-X-L/Bim fragment complex: implications for Bim function. Immunity 19: 341-352
22. Oltvai ZN and Korsmeyer SJ (1994) Checkpoints of dueling dimers foil death wishes. Cell 79: 189-192
23. Knudson CM and Korsmeyer SJ (1997) Bcl-2 and Bax function independently to regulate cell death. Nat. Genet. 16: 358-363
24. Otter I, Conus S, Ravn U, Rager M, Olivier R, Monney L, Fabbro D and Borner C (1998) The binding properties and biological activities of Bcl-2 and Bax in cells exposed to apoptotic stimuli. J. Biol. Chem. 273: 6110-6120
25. Middleton G, Cox SW, Korsmeyer S and Davies AM (2000) Differences in Bcl-2- and Bax-independent function in regulating apoptosis in sensory neuron populations. Eur. J. Neurosci. 12: 819-827
26. Muchmore SW, Sattler M, Liang H, Meadows RP, Harlan JE, Yoon HS, Nettesheim D, Chang BS, Thompson CB, Wong SL, Ng SL and Fesik SW (1996) X-ray and NMR structure of human Bcl-X-L, an inhibitor of programmed cell death. Nature 381: 335-341
27. Antonsson B, Conti F, Ciavatta A, Montessuit S, Lewis S, Martinou I, Bernasconi L, Bernard A, Mermod JJ, Mazzei G, Maundrell K, Gambale F, Sadoul R and Martinou JC (1997) Inhibition of Bax channel-forming activity by Bcl-2. Science 277: 370-372
28. Minn AJ, Velez P, Schendel SL, Liang H, Muchmore SW, Fesik SW, Fill M and Thompson CB (1997) Bcl-X-L forms an ion channel in synthetic lipid membranes. Nature 385: 353-357
29. Schendel SL, Xie Z, Montal MO, Matsuyama S, Montal M and Reed JC (1997) Channel formation by antiapoptotic protein Bcl-2. Proc. Natl. Acad. Sci. USA 94: 5113-5118
30. Schlesinger PH, Gross A, Yin XM, Yamamoto K, Saito M, Waksman G and Korsmeyer SJ (1997) Comparison of the ion channel characteristics of proapoptotic Bax and antiapoptotic Bcl-2. Proc. Natl. Acad. Sci. USA 94: 11357-11362
31. Cheng EH, Sheiko TV, Fisher JK, Craigen WJ and Korsmeyer SJ (2003) VDAC2 inhibits Bak activation and mitochondrial apoptosis. Science 301: 513-517
32. 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
33. Basanez G, Sharpe JC, Galanis J, Brandt TB, Hardwick JM and Zimmerberg J (2002) Bax-type apoptotic proteins porate pure lipid bilayers through a mechanism sensitive to intrinsic monolayer curvature. J. Biol. Chem. 277: 49360-49365
34. Coughlin MD and Collins MB (1985) Nerve growth factor-independent development of embryonic mouse sympathetic neurons in dissociated cell culture. Dev. Biol. 110: 392-401
35. Levi-Montalcini R and Booker B (1960) Destruction of the sympathetic ganglia in mammals by an antiserum to the nerve growth-promoting factor. Proc. Natl. Acad. Sci. USA 46: 384-391
36. Deckwerth TL and Johnson Jr EM (1993) Temporal analysis of events associated with programmed cell death (apoptosis) of sympathetic neurons deprived of nerve growth factor. J. Cell Biol. 123: 1207-1222
37. Edwards SN, Buckmaster AE and Tolkovsky AM (1991) The death programme in cultured sympathetic neurones can be suppressed at the posttranslational level by nerve growth factor, cyclic AMP, and depolarization. J. Neurochem. 57: 2140-2143
38. Martin DP, Schmidt RE, DiStefano PS, Lowry OH, Carter JG and Johnson Jr EM (1988) Inhibitors of protein synthesis and RNA synthesis prevent neuronal death caused by nerve growth factor deprivation, J. Cell Biol. 106: 829-844
39. Deckwerth TL, Elliott JL, Knudson CM, Johnson EM, Snider WD and Korsmeyer SJ (1996) Bax is required for neuronal death after trophic factor deprivation and during development. Neuron 17: 401-411
40. Deshmukh M, Vasilakos J, Deckwerth TL, Lampe PA, Shivers BD and Johnson Jr EM (1996) Genetic and metabolic status of NGF-deprived sympathetic neurons saved by an inhibitor of ICE family proteases. J. Cell Biol. 135: 1341-1354
41. McCarthy MJ, Rubin LL and Philpott KL (1997) Involvement of caspases in sympathetic neuron apoptosis. J. Cell Sci. 110: 2165-2173
42. Troy CM, Stefanis L, Prochiantz A, Greene LA and Shelanski ML (1996) The contrasting roles of ICE family proteases and interleukin-1-β in apoptosis induced by trophic factor withdrawal and by copper/zinc superoxide dismutase down-regulation. Proc. Natl. Acad. Sci. USA 93: 5635-5640
43. 2+ determine nerve growth factor dependence of sympathetic ganglion cells. Proc. Natl. Acad. Sci. USA 86: 6421-6425
44. Rydel RE and Greene LA (1988) cAMP analogs promote survival and neurite outgrowth in cultures of rat sympathetic and sensory neurons independently of nerve growth factor. Proc. Natl. Acad. Sci. USA 85: 1257-1261
45. Johnson Jr EM, Chang JY, Koike T and Martin DP (1989) Why do neurons die when deprived of trophic factor? Neurobiol. Aging 10: 549-552
46. Conradt B and Horvitz HR (1998) The C. elegans protein EGL-1 is required for programmed cell death and interacts with the Bcl-2-like protein Ced-9. Cell 93: 519-529
47. Putcha GV, Moulder KL, Golden JP, Bouillet P, Adams JA, Strasser A and Johnson EM (2001) Induction of Bim, a proapoptotic BH3-only Bcl-2 family member, is critical for neuronal apoptosis. Neuron 29: 615-628
48. Whitfield J, Neame SJ, 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
49. Imaizumi K, Tsuda M, Imai Y, Wanaka A, Takagi T and Tohyama M (1997) Molecular cloning of a novel polypeptide, Dp5, induced during programmed neuronal death. J. Biol. Chem. 272: 18842-18848
50. Harris CA and Johnson Jr EM (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
51. Putcha GV, Harris CA, Moulder KL, Easton RM, Thompson CB and Johnson Jr EM (2002) Intrinsic and extrinsic pathway signaling during neuronal apoptosis: Lessons from the analysis of mutant mice. J. Cell Biol. 157: 441-453
52. Putcha GV, Le S, Frank S, Besirli CG, Clark K, Chu B, Alix S, Youle RJ, LaMarche A, Maroney AC and Johnson Jr EM (2003) Jnk-mediated Bim phosphorylation potentiates Bax-dependent apoptosis. Neuron 38: 899-914
53. Conradt B and Horvitz HR (1999) The TRA-1A sex determination protein of C. elegans regulates sexually dimorphic cell deaths by repressing the Egl-1 cell death activator gene. Cell 98: 317-327
54. Metzstein MM and Horvitz HR (1999) The C. elegans cell death specification gene ces-1 encodes a snail family zinc finger protein. Mol. Cell 4: 309-319
55. Thellmann M, Hatzold J and Conradt B (2003) The Snail-like Ces-1 protein of C. elegans can block the expression of the BH3-only cell-death activator gene Egl-1 by antagonizing the function of bHLH proteins. Development 130: 4057-4071
56. Horvitz HR (2003) Worms, life, and death (Nobel Lecture). Chembiochem 4: 697-711
57. Lonze BE and Ginty DD (2002) Function and regulation of CREB family transcription factors in the nervous system. Neuron 35: 605-623
58. Maggirwar SB, Sarmiere PD, Dewhurst S and Freeman RS (1998) Nerve growth factor-dependent activation of NF-kappaB contributes to survival of sympathetic neurons. J. Neurosci. 18: 10356-10365
59. Sarmiere PD and Freeman RS (2001) Analysis of the NF-kappa B and Pl 3-kinase/Akt survival pathways in nerve growth factor-dependent neurons. Mol. Cell. Neurosci. 18: 320-331
60. Creedon DJ, Johnson EM and Lawrence JC (1996) Mitogen-activated protein kinase-independent pathways mediate the effects of nerve growth factor and cAMP on neuronal survival. J. Biol. Chem. 271: 20713-20718
61. Virdee K and Tolkovsky AM (1996) Inhibition of p42 and p44 mitogen-activated protein kinase activity by PD98059 does not suppress nerve growth factor-induced survival of sympathetic neurones. J. Neurochem. 67: 1801-1805
62. Crowder RJ and Freeman RS (1998) Phosphatidylinositol 3-kinase and Akt protein kinase are necessary and sufficient for the survival of nerve growth factor-dependent sympathetic neurons. J. Neurosci. 18: 2933-2943
63. Philpott KL, McCarthy MJ, Klippel A and Rubin LL (1997) Activated phosphatidylinositol 3-kinase and Akt kinase promote survival of superior cervical neurons. J. Cell Biol. 139: 809-815
64. Tsui-Pierchala BA, Putcha GV and Johnson Jr EM (2000) Phosphatidylinositol 3-kinase is required for the trophic, but not the survival-promoting, actions of NGF on sympathetic neurons. J. Neurosci. 20: 7228-7237
65. Estus S, Zaks WJ, Freeman RS, Gruda M, Bravo R and Johnson Jr EM (1994) Altered gene expression in neurons during programmed cell death: identification of c-jun as necessary for neuronal apoptosis. J. Cell Biol. 127: 1717-1727
66. Ham J, Babij C, Whitfield J, Pfarr CM, Lallemand D, Yaniv M and Rubin LL (1995) A c-Jun dominant negative mutant protects sympathetic neurons against programmed cell death. Neuron 14: 927-939
67. Eilers A, Whitfield J, Babij C, Rubin LL and Ham J (1998) Role of the Jun kinase pathway in the regulation of c-Jun expression and apoptosis in sympathetic neurons. J. Neurosci. 18: 1713-1724
68. Dijkers PF, Medema RH, Lammers JW, Koenderman L and Coffer PJ (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
69. Dijkers PF, Birkenkamp KU, Lam EW, Thomas NS, Lammers JW, Koenderman L and Coffer PJ (2002) FKHR-L1 can act as a critical effector of cell death induced by cytokine withdrawal: protein kinase B-enhanced cell survival through maintenance of mitochondrial integrity. J. Cell Biol. 156: 531-542
70. Bouillet P, Zhang LC, Huang DC, Webb GC, Bottema CD, Shore P, Eyre HJ, Sutherland GR and Adams JM (2001) Gene structure alternative splicing, and chromosomal localization of pro-apoptotic Bcl-2 relative Bim. Mamm. Genome 12: 163-168
71. Sanz C, Mellstrom B, Link WA, Naranjo JR and Fernandez-Luna JL (2001) Interleukin 3-dependent activation of DREAM is involved in transcriptional silencing of the apoptotic Hrk gene in hematopoietic progenitor cells. EMBO J. 20: 2286-2292
72. Gilley J, Coffer PJ and Ham J (2003) FOXO transcription factors directly activate Bim gene expression and promote apoptosis in sympathetic neurons. J. Cell Biol. 162: 613-622
73. Ley R, Balmanno K, Hadfield K, Weston C and Cook SJ (2003) Activation of the ERK1/2 signaling pathway promotes phosphorylation and proteasome-dependent degradation of the BH3-only protein, Bim. J. Biol. Chem. 278: 18811-18816
74. Reginato MJ, Mills KR, Paulus JK, Lynch DK, Sgroi DC, Debnath J, Muthuswamy SK and Brugge JS (2003) Integrins and EGFR coordinately regulate the pro-apoptotic protein Bim to prevent anoikis. Nat. Cell Biol. 5: 733-740
75. Weston CR, Balmanno K, Chalmers C, Hadfield K, Molton SA, Ley R, Wagner EF and Cook SJ (2003) Activation of ERK1/2 by deltaRaf-1:ER* represses Bim expression independently of the JNK or PI3K pathways. Oncogene 22: 1281-1293
76. Shinjyo T, Kuribara R, Inukai T, Hosoi H, Kinoshita T, Miyajima A, Houghton PJ, Look AT, Ozawa K and Inaba T (2001) Downregulation of Bim, a proapoptotic relative of Bcl-2, is a pivotal step in cytokine-initiated survival signaling in murine hematopoietic progenitors. Mol. Cell. Biol. 21: 854-864
77. Lei K and Davis RJ (2003) Jnk phosphorylation of Bim-related members of the Bcl-2 family induces Bax-dependent apoptosis. Proc. Natl. Acad. Sci. USA 100: 2432-2437
78. Biswas SC and Greene LA (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
79. Liu DX and Greene LA (2001) Regulation of neuronal survival and death by E2F-dependent gene repression and derepression. Neuron 32: 425-438
80. Crowder RJ and Freeman RS (1999) The survival of sympathetic neurons promoted by potassium depolarization, but not by cyclic AMP, requires phosphatidylinositol 3- kinase and Akt. J. Neurochem. 73: 466-475
81. Vaillant AR, Mazzoni I, Tudan C, Boudreau M, Kaplan DR and Miller FD (1999) Depolarization and neurotrophins converge on the phosphatidylinositol 3- kinase-Akt pathway to synergistically regulate neuronal survival. J. Cell Biol. 146: 955-966
82. Miller TM, Tansey MG, Johnson Jr EM and Creedon DJ (1997) Inhibition of phosphatidylinositol 3-kinase activity blocks depolarization- and insulin-like growth factor I-mediated survival of cerebellar granule cells. J. Biol. Chem. 272: 9847-9853
83. Dudek H, Datta SR, Franke TF, Birnbaum MJ, Yao R, Cooper GM, Segal RA, Kaplan DR and Greenberg ME (1997) Regulation of neuronal survival by the serine-threonine protein kinase Akt. Science 275: 661-665
84. Miller TM, Moulder KL, Knudson CM, Creedon DJ, Deshmukh M, Korsmeyer SJ and Johnson Jr EM (1997) Bax deletion further orders the cell death pathway in cerebellar granule cells and suggests a caspase-independent pathway to cell death. J. Cell Biol. 139: 205-217
85. Lonze BE, Riccio A, Cohen S and Ginty DD (2002) Apoptosis, axonal growth defects, and degeneration of peripheral neurons in mice lacking CREB. Neuron 34: 371-385
86. Riccio A, Ahn S, Davenport CM, Blendy JA and Ginty DD (1999) Mediation by a CREB family transcription factor of NGF-dependent survival of sympathetic neurons. Science 286: 2358-2361
87. Greenlund LJ, Korsmeyer SJ and Johnson Jr EM (1995) Role of Bcl-2 in the survival and function of developing and mature sympathetic neurons. Neuron 15: 649-661
88. Michaelidis TM, Sendtner M, Cooper JD, Airaksinen MS, Holtmann B, Meyer M and Thoenen H (1996) Inactivation of Bcl-2 results in progressive degeneration of motoneurons, sympathetic and sensory neurons during early postnatal development. Neuron 17: 75-89
89. Motoyama N, Wang F, Roth KA, Sawa H, Nakayama K, Negishi I, Senju S, Zhang Q and Fujii S (1995) Massive cell death of immature hematopoietic cells and neurons in Bcl-X-deficient mice. Science 267: 1506-1510
90. Shindler KS, Latham CB and Roth KA (1997) Bax deficiency prevents the increased cell death of immature neurons in Bcl-X-deficient mice. J. Neurosci. 17: 3112-3119
91. Buettner R, Mora LB and Jove R (2002) Activated STAT signaling in human tumors provides novel molecular targets for therapeutic intervention. Clin. Cancer Res. 8: 945-954
92. Mayr B and Montminy M (2001) Transcriptional regulation by the phosphorylation-dependent factor CREB. Nat. Rev. Mol. Cell Biol. 2: 599-609
93. Chen C, Edelstein LC and Gelinas C (2000) The Rel/NF-kappaB family directly activates expression of the apoptosis inhibitor Bcl-X-L. Mol. Cell. Biol. 20: 2687-2695
94. Zong WX, Edelstein LC, Chen C, Bash J and Gelinas C (1999) The prosurvival Bcl-2 homolog Bfl-1/A1 is a direct transcriptional target of NF-kappaB that blocks TNFalpha-induced apoptosis. Genes Dev. 13: 382-387
95. Chu ZL, McKinsey TA, Liu L, Gentry JJ, Malim MH and Ballard DW (1997) Suppression of tumor necrosis factor-induced cell death by inhibitor of apoptosis c-IAP2 is under NF-kappaB control. Proc. Natl. Acad. Sci. USA 94: 10057-10062
96. Wang CY, Mayo MW, Korneluk RG, Goeddel DV and Baldwin Jr AS (1998) NF-kappaB antiapoptosis: induction of TRAF1 and TRAF2 and c-IAP1 and c-IAP2 to suppress caspase-8 activation. Science 281: 1680-1683
97. Sun W, Gould TW, Vinsant S, Prevette D and Oppenheim RW (2003) Neuromuscular development after the prevention of naturally occurring neuronal death by Bax deletion. J. Neurosci. 23: 7298-7310
98. Putcha GV, Deshmukh M and Johnson Jr EM (2000) Inhibition of apoptotic signaling cascades causes loss of trophic factor dependence during neuronal maturation. J. Cell Biol. 149: 1011-1018
99. Knudson CM, Tung KS, Tourtellotte WG, Brown GA and Korsmeyer SJ (1995) Bax-deficient mice with lymphoid hyperplasia and male germ cell death. Science 270: 96-99
100. Lindsten T, Ross AJ, King A, Zong W, Rathmell JC, Shiels HA, Ulrich E, Waymire KG, Mahar P, Frauwirth K, Chen Y, Wei M, Eng VM, Adelman DM, Simon MC, Me A, Golden JA, Evan G, Korsmeyer SJ, MacGregor GR and Thompson CB (2000) The combined functions of proapoptotic BCL-2 family members Bak and Bax are essential for normal development of multiple tissues. Mol. Cell 6: 1389-1399
101. Wei MC, Zong WX, Cheng EH, Lindsten T, Panoutsakopoulou V, Ross AJ, Roth KA, MacGregor GR, Thompson CB and Korsmeyer SJ (2001) Proapoptotic Bax and Bak: a requisite gateway to mitochondrial dysfunction and death. Science 292: 727-730
102. White FA, Kellerpeck CR, Knudson CM, Korsmeyer SJ and Snider WD (1998) Widespread elimination of naturally occurring neuronal death in Bax-deficient mice. J. Neurosci. 18: 1428-1439
103. Aloyz RS, Bamji SX, Pozniak CD, Tome JG, Atwal J, Kaplan DR and Miller FD (1998) p53 is essential for developmental neuron death as regulated by the TrkA and p75 neurotrophin receptors. J. Cell Biol. 143: 1691-1703
104. Desagher S, Osen-Sand A, Nichols A, Eskes R, Montessuit S, Lauper S, Maundrell K, Antonsson B and Martinou J-C (1999) Bid-induced conformational change in Bax is responsible for mitochondrial cytochrome c release during apoptosis. J. Cell Biol. 144: 891-901
105. Putcha GV, Deshmukh M and Johnson Jr EM (1999) Bax translocation is a critical event in neuronal apoptosis: regulation by neuroprotectants, Bcl-2, and caspases. J. Neurosci. 19: 7476-7485
106. McGinnis KM, Gnegy ME and Wang KK (1999) Endogenous Bax translocation in SH-SY5Y human neuroblastoma cells and cerebellar granule neurons undergoing apoptosis. J. Neurochem. 72: 1899-1906
107. Li L, Oppenheim RW and Milligan CE (2001) Characterization of the execution pathway of developing motoneurons deprived of trophic support. J. Neurobiol. 46: 249-264
108. Besirli CG, Deckwerth TL, Crowder RJ, Freeman RS and Johnson Jr EM (2003) Cytosine arabinoside rapidly activates Bax-dependent apoptosis and a delayed Bax-independent death pathway in sympathetic neurons. Cell Death Differ. 10: 1045-1058
109. Davies AM and Rosenthal A (1994) Neurons from mouse embryos with a null mutation in the tumour suppressor gene p53 undergo normal cell death in the absence of neurotrophins. Neurosci. Lett. 182: 112-114
110. Sadoul R, Quiquerez AL, Martinou I, Fernandez PA and Martinou JC (1996) p53 protein in sympathetic neurons: cytoplasmic localization and no apparent function in apoptosis. J. Neurosci. Res. 43: 594-601
111. Martinou I, Fernandez PA, Missotten M, White E, Allet B, Sadoul R and Martinou JC (1995) Viral proteins E1B19K and p35 protect sympathetic neurons from cell death induced by NGF deprivation. J. Cell Biol. 128: 201-208
112. Chen RW, Saunders PA, Wei H, Li Z, Seth P and Chuang DM (1999) Involvement of glyceraldehyde-3-phosphate dehydrogenase (GAPDH) and p53 in neuronal apoptosis: evidence that GAPDH is upregulated by p53. J. Neurosci. 19: 9654-9662
113. Enokido Y, Araki T, Tanaka K, Aizawa S and Hatanaka H (1996) Involvement of p53 in DNA strand break-induced apoptosis in postmitotic CNS neurons. Eur. J. Neurosci. 8: 1812-1821
114. Enokido Y, Araki T, Aizawa S and Hatanaka H (1996) p53 involves cytosine arabinoside-induced apoptosis in cultured cerebellar granule neurons. Neurosci. Lett. 203: 1-4
115. Morris EJ, Keramaris E, Rideout HJ, Slack RS, Dyson NJ, Stefanis L and Park DS (2001) Cyclin-dependent kinases and p53 pathways are activated independently and mediate Bax activation in neurons after DNA damage. J. Neurosci. 21: 5017-5026
116. Miyashita T, Krajewski S, Krajewska M, Wang HG, Lin HK, Liebermann DA, Hoffman B and Reed JC (1994) Tumor suppressor p53 is a regulator of Bcl-2 and Bax gene expression in vitro and in vivo. Oncogene 9: 1799-1805
117. Neame SJ, Rubin LL and Philpott KL (1998) Blocking cytochrome c activity within intact neurons inhibits apoptosis. J. Cell Biol. 142: 1583-1593
118. Suzuki M, Youle RJ and Tjandra N (2000) Structure of Bax: coregulation of dimer formation and intracellular localization. Cell 103: 645-654
119. Sundararajan R and White E (2001) E1B 19K blocks Bax oligomerization and tumor necrosis factor alpha-mediated apoptosis. J. Virol. 75: 7506-7516
120. O'Connor L, Strasser A, O'Reilly LA, Hausmann G, Adams JM, Cory S and Huang DC (1998) BIM: a novel member of the Bcl-2 family that promotes apoptosis. EMBO J. 17: 384-395
121. Hsu YT and Youle RJ (1997) Nonionic detergents induce dimerization among members of the Bcl-2 family. J. Biol. Chem. 272: 13829-13834
122. Antonsson B, Montessuit S, Sanchez B and Martinou JC (2001) Bax is present as a high molecular weight oligomer/complex in the mitochondrial membrane of apoptotic cells. J. Biol. Chem. 276: 11615-11623
123. Tanabe H, Eguchi Y, Shimizu S, Martinou JC and Tsujimoto Y (1998) Death-signalling cascade in mouse cerebellar granule neurons. Eur. J. Neurosci. 10: 1403-1411
124. Yamaguchi H, Bhalla K and Wang HG (2003) Bax plays a pivotal role in thapsigargin-induced apoptosis of human colon cancer HCT116 cells by controlling Smac/Diablo and Omi/HtrA2 release from mitochondria. Cancer Res. 63: 1483-1489
125. Kostic V, Jackson-Lewis V, de Bilbao F, Dubois-Dauphin M and Przedborski S (1997) Bcl-2: prolonging life in a transgenic mouse model of familial amyotrophic lateral sclerosis. Science 277: 559-562
126. Li MW, One VO, Guegan C, Chen MH, Jackson-Lewis V, Andrews LJ, Olszewski AJ, Stieg PE, Lee JP, Przedborski S and Friedlander RM (2000) Functional role of caspase-1 and caspase-3 in an ALS transgenic mouse model. Science 288: 335-339
127. Chang LK and Johnson Jr EM (2002) Cyclosporin A inhibits caspase-independent death of NGF-deprived sympathetic neurons: a potential role for mitochondrial permeability transition. J. Cell Biol. 157: 771-781
128. Werth JL, Deshmukh M, Cocabo J, Johnson EM and Rothman SM (2000) Reversible physiological alterations in sympathetic neurons deprived of NGF but protected from apoptosis by caspase inhibition or Bax deletion. Exp. Neurol. 161: 203-211
129. Harris CA, Deshmukh M, Tsui-Pierchala B, Maroney AC and Johnson Jr EM (2002) Inhibition of the c-Jun N-terminal kinase signaling pathway by the mixed lineage kinase inhibitor CEP-1347 (KT7515) preserves metabolism and growth of trophic factor-deprived neurons. J. Neurosci. 22: 103-113
130. Chen F, Hersh BM, Conradt B, Zhou Z, Riemer D, Gruenbaum Y and Horvitz HR (2000) Translocation of C. elegans Ced-4 to nuclear membranes during programmed cell death. Science 287: 1485-1489
131. Aravind L, Dixit VM and Koonin EV (2001) Apoptotic molecular machinery: vastly increased complexity in vertebrates revealed by genome comparisons. Science 291: 1279-1284
132. Tran H, Brunet A, Griffith EC and Greenberg ME (2003) The many forks in FOXO's road. Science STKE 2003: RE5
133. Letai A, Bassik MC, Walensky LD, Sorcinelli MD, Weiler S and Korsmeyer SJ (2002) Distinct BH3 domains either sensitize or activate mitochondrial apoptosis, serving as prototype cancer therapeutics. Cancer Cell 2: 183-192