Mutational analysis of N-Bak reveals different structural requirements for antiapoptotic activity in neurons and proapoptotic activity in nonneuronal cells

Molecular and Cellular Neuroscience

Volumn 23, Issue 1, 2003, Pages 134-143

  Sun, Yun Fu ^a   Yu, Li Ying ^a   Saarma, Mart ^a   Arumäe, Urmas ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

ISOPROTEIN; PROTEIN; PROTEIN N BAK; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; BRAIN NERVE CELL; CARBOXY TERMINAL SEQUENCE; CELL STRAIN COS1; CYTOTOXICITY; GENE DELETION; MUTATIONAL ANALYSIS; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN STRUCTURE;

EID: 0037835612     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1044-7431(03)00023-X     Document Type: Article

References (52)

1. Antonsson B. Bax and other pro-apoptotic Bcl-2 family "killer-proteins" and their victim the mitochondrion. Cell Tissue Res. 306:2001;347-361.
2. Antonsson B., Martinou J.C. The Bcl-2 protein family. Exp. Cell Res. 256:2000;50-57.
3. Bergeron L., Perez G.I., Macdonald G., Shi L., Sun Y., Jurisicova A., Varmuza S., Latham K.E., Flaws J.A., Salter J.C., Hara H., Moskowitz M.A., Li E., Greenberg A., Tilly J.L., Yuan J. Defects in regulation of apoptosis in caspase-2-deficient mice. Genes Dev. 12:1998;1304-1314.
4. Cheng E.H., Wei M.C., Weiler S., Flavell R.A., Mak T.W., Lindsten T., Korsmeyer S.J. BCL-2, BCL-X(L) sequester BH3 domain-only molecules preventing BAX- and BAK-mediated mitochondrial apoptosis. Mol. Cell. 8:2001;705-711.
5. Chittenden T., Flemington C., Houghton A.B., Ebb R.G., Gallo G.J., Elangovan B., Chinnadurai G., Lutz R.J. A conserved domain in Bak, distinct from BH1 and BH2, mediates cell death and protein binding functions. EMBO J. 14:1995;5589-5596.
6. Condorelli F., Salomoni P., Cotteret S., Cesi V., Srinivasula S.M., Alnemri E.S., Calabretta B. Caspase cleavage enhances the apoptosis-inducing effects of BAD. Mol. Cell. Biol. 21:2001;3025-3036.
7. Deckwerth T.L., Elliott J.L., Knudson C.M., Johnson E.M.J., Snider W.D., Korsmeyer S.J. BAX is required for neuronal death after trophic factor deprivation and during development. Neuron. 17:1996;401-411.
8. Deckwerth T.L., Johnson E.M.J. Temporal analysis of events associated with programmed cell death (apoptosis) of sympathetic neurons deprived of nerve growth factor. J. Cell Biol. 123:1993;1207-1222.
9. Desagher S., Osen-Sand A., Montessuit S., Magnenat E., Vilbois F., Hochmann A., Journot L., Antonsson B., Martinou J.C. Phosphorylation of bid by casein kinases I and II regulates its cleavage by caspase 8. Mol. Cell. 8:2001;601-611.
10. Desagher S., Osen-Sand A., Nichols A., Eskes R., Montessuit S., Lauper S., Maundrell K., Antonsson B., Martinou J.C. Bid-induced conformational change of Bax is responsible for mitochondrial cytochrome c release during apoptosis. J. Cell Biol. 144:1999;891-901.
11. Deshmukh M., Du C., Wang X., Johnson E.M. Jr. Exogenous smac induces competence and permits caspase activation in sympathetic neurons. J. Neurosci. 22:2002;8018-8027.
12. Deshmukh M., Johnson E.M.J. Evidence of a novel event during neuronal death development of competence-to-die in response to cytoplasmic cytochrome . c. Neuron. 21:1998;695-705.
13. Edwards S.N., Tolkovsky A.M. Characterization of apoptosis in cultured rat sympathetic neurons after nerve growth factor withdrawal. J. Cell Biol. 124:1994;537-546.
14. Eskes R., Desagher S., Antonsson B., Martinou J.C. Bid induces the oligomerization and insertion of Bax into the outer mitochondrial membrane. Mol. Cell. Biol. 20:2000;929-935.
15. Fesik S.W. Insights into programmed cell death through structural biology. Cell. 103:2000;273-282.
16. Griffiths G.J., Dubrez L., Morgan C.P., Jones N.A., Whitehouse J., Corfe B.M., Dive C., Hickman J.A. Cell damage-induced conformational changes of the pro-apoptotic protein Bak in vivo precede the onset of apoptosis. J. Cell Biol. 144:1999;903-914.
17. Gross A., Yin X.M., Wang K., Wei M.C., Jockel J., Milliman C., Erdjument-Bromage H., Tempst P., Korsmeyer S.J. Caspase cleaved BID targets mitochondria and is required for cytochrome c release, while Bcl-XL prevents this release but not tumor necrosis factor-R1/fas death. J. Biol. Chem. 274:1999;1156-1163.
18. Hamnér S., Arumäe U., Li-Ying Y., Sun Y.F., Saarma M., Lindholm D. Functional characterization of two splice variants of rat bad and their interaction with Bcl-w in sympathetic neurons. Mol. Cell. Neurosci. 17:2001;97-106.
19. Han J., Flemington C., Houghton A.B., Gu Z., Zambetti G.P., Lutz R.J., Zhu L., Chittenden T. Expression of bbc3, a pro-apoptotic BH3-only gene, is regulated by diverse cell death and survival signals. Proc. Natl. Acad. Sci. USA. 98:2001;11318-11323.
20. Harris C.A., Johnson E.M.J. BH3-only Bcl-2 family members are coordinately regulated by the JNK pathway and require Bax to induce apoptosis in neurons. J. Biol. Chem. 276:2001;37754-37760.
21. Hegde R., Srinivasula S.M., Ahmad M., Fernandes-Alnemri T., Alnemri E.S. Blk, a BH3-containing mouse protein that interacts with Bcl-2 and Bcl-xL, is a potent death agonist. J. Biol. Chem. 273:1998;7783-7786.
22. Holinger E.P., Chittenden T., Lutz R.J. Bak BH3 peptides antagonize Bcl-xL function and induce apoptosis through cytochrome c-independent activation of caspases. J. Biol. Chem. 274:1999;13298-13304.
23. Huang D.C., Adams J.M., Cory S. The conserved N-terminal BH4 domain of Bcl-2 homologues is essential for inhibition of apoptosis and interaction with CED-4. EMBO J. 17:1998;1029-1039.
24. Imaizumi K., Tsuda M., Imai Y., Wanaka A., Takagi T., Tohyama M. Molecular cloning of a novel polypeptide, DP5, induced during programmed neuronal death. J. Biol. Chem. 272:1997;18842-18848.
25. Kaufmann S.H., Hengartner M.O. Programmed cell death alive and well in the new millennium . Trends Cell Biol. 11:2001;526-534.
26. Kim B.C., Mamura M., Choi K.S., Calabretta B., Kim S.J. Transforming growth factor beta 1 induces apoptosis through cleavage of BAD in a Smad3-dependent mechanism in FaO hepatoma cells. Mol. Cell. Biol. 22:2002;1369-1378.
27. Martin D.P., Ito A., Horigome K., Lampe P.A., Johnson E.M.J. Biochemical characterization of programmed cell death in NGF-deprived sympathetic neurons. J. Neurobiol. 23:1992;1205-1220.
28. Martin D.P., Schmidt R.E., DiStefano P.S., Lowry O.H., Carter J.G., Johnson E.M.J. Inhibitors of protein synthesis and RNA synthesis prevent neuronal death caused by nerve growth factor deprivation. J. Cell Biol. 106:1988;829-844.
29. Nakano K., Vousden K.H. PUMA, a novel proapoptotic gene, is induced by p53. Mol. Cell. 7:2001;683-694.
30. Neame S.J., Rubin L.L., Philpott K.L. Blocking cytochrome c activity within intact neurons inhibits apoptosis. J. Cell Biol. 142:1998;1583-1593.
31. Nouraini S., Six E., Matsuyama S., Krajewski S., Reed J.C. Theputative pore-forming domain of Bax regulates mitochondrial localization and interaction with Bcl-X(L). Mol. Cell. Biol. 20:2000;1604-1615.
32. Oda E., Ohki R., Murasawa H., Nemoto J., Shibue T., Yamashita T., Tokino T., Taniguchi T., Tanaka N. Noxa, a BH3-only member of the Bcl-2 family and candidate mediator of p53-induced apoptosis. Science. 288:2000;1053-1058.
33. Oltvai Z.N., Milliman C.L., Korsmeyer S.J. Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death. Cell. 74:1993;609-619.
34. Putcha G.V., Deshmukh M., Johnson E.M.J. BAX translocation is a critical event in neuronal apoptosis regulation by neuroprotectants, BCL-2, and caspases . J. Neurosci. 19:1999;7476-7485.
35. Putcha G.V., Deshmukh M., Johnson E.M.J. Inhibition of apoptotic signaling cascades causes loss of trophic factor dependence during neuronal maturation. J. Cell Biol. 149:2000;1011-1018.
36. Putcha G.V., Harris C.A., Moulder K.L., Easton R.M., Thompson C.B., Johnson E.M.J. Intrinsic and extrinsic pathway signaling during neuronal apoptosis lessons from the analysis of mutant mice . J. Cell Biol. 157:2002;441-453.
37. Putcha G.V., Moulder K.L., Golden J.P., Bouillet P., Adams J.A., Strasser A., Johnson E.M. Induction of BIM, a proapoptotic BH3-only BCL-2 family member, is critical for neuronal apoptosis. Neuron. 29:2001;615-628.
38. Puthalakath H., Huang D.C., O'Reilly L.A., King S.M., Strasser A. The proapoptotic activity of the Bcl-2 family member Bim is regulated by interaction with the dynein motor complex. Mol. Cell. 3:1999;287-296.
39. Roucou X., Martinou J.C. Conformational change of Bax a question of life or death . Cell Death Differ. 8:2001;875-877.
40. Sattler M., Liang H., Nettesheim D., Meadows R.P., Harlan J.E., Eberstadt M., Yoon H.S., Shuker S.B., Chang B.S., Minn A.J., Thompson C.B., Fesik S.W. Structure of Bcl-xL-Bak peptide complex recognition between regulators of apoptosis . Science. 275:1997;983-986.
41. Simonen M., Keller H., Heim J. The BH3 domain of Bax is sufficient for interaction of Bax with itself and with other family members and it is required for induction of apoptosis. Eur. J. Biochem. 249:1997;85-91.
42. Sun Y.F., Yu L.Y., Saarma M., Timmusk T., Arumäe U. Neuron-specific Bcl-2 homology 3 domain-only splice variant of Bak is anti-apoptotic in neurons, but pro-apoptotic in non-neuronal cells. J. Biol. Chem. 276:2001;16240-16247.
43. Suzuki M., Youle R.J., Tjandra N. Structure of Bax coregulation of dimer formation and intracellular localization . Cell. 103:2000;645-654.
44. Verma S., Zhao L.J., Chinnadurai G. Phosphorylation of the Proapoptotic Protein BIK. Mapping of phosphorylation sites and effect on apoptosis. J. Biol. Chem. 276:2001;4671-4676.
45. Wang K., Gross A., Waksman G., Korsmeyer S.J. Mutagenesis of the BH3 domain of BAX identifies residues critical for dimerization and killing. Mol. Cell. Biol. 18:1998;6083-6089.
46. Wang X. The expanding role of mitochondria in apoptosis. Genes Dev. 15:2001;2922-2933.
47. Wei M.C., Lindsten T., Mootha V.K., Weiler S., Gross A., Ashiya M., Thompson C.B., Korsmeyer S.J. tBID, a membrane-targeted death ligand, oligomerizes BAK to release cytochrome c. Genes Dev. 14:2000;2060-2071.
48. Whitfield J., Neame S.J., Paquet L., Bernard O., Ham J. Dominant-negative c-Jun promotes neuronal survival by reducing BIM expression and inhibiting mitochondrial cytochrome c release. Neuron. 29:2001;629-643.
49. Yu J., Zhang L., Hwang P.M., Kinzler K.W., Vogelstein B. PUMA induces the rapid apoptosis of colorectal cancer cells. Mol. Cell. 7:2001;673-682.
50. Zha J., Harada H., Osipov K., Jockel J., Waksman G., Korsmeyer S.J. BH3 domain of BAD is required for heterodimerization with BCL-XL and pro-apoptotic activity. J. Biol. Chem. 272:1997;24101-24104.
51. Zha J., Weiler S., Oh K.J., Wei M.C., Korsmeyer S.J. Posttranslational N-myristoylation of BID as a molecular switch for targeting mitochondria and apoptosis. Science. 290:2000;1761-1765.
52. Zimmermann K.C., Bonzon C., Green D.R. The machinery of programmed cell death. Pharmacol. Ther. 92:2001;57-70.