Glycogen synthase kinase-3β phosphorylates bax and promotes its mitochondrial localization during neuronal apoptosis

Journal of Neuroscience

Volumn 24, Issue 44, 2004, Pages 9993-10002

  Linseman, Daniel A ^a   Butts, Brent D ^a   Precht, Thomas A ^a   Phelps, Reid A ^a   Le, Shoshona S ^a   Laessig, Tracey A ^a   Bouchard, Ron J ^a   Florez McClure, Maria L ^a   Heidenreich, Kim A ^a,b  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b UNIVERSITY OF COLORADO   (United States)

Author keywords

Apoptosis; Bax; Cerebellar granule neuron; Glycogen synthase kinase; Mitochondria; Phosphorylation

Indexed keywords

AMINO ACID; CYTOCHROME C; GLYCOGEN SYNTHASE KINASE 3BETA; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; PROTEIN BAX; PROTEIN BCL 2;

ANIMAL CELL; APOPTOSIS; ARTICLE; BRAIN MITOCHONDRION; CELLULAR DISTRIBUTION; CEREBELLUM; CONFORMATIONAL TRANSITION; DELETION MUTANT; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; GENE TRANSLOCATION; GENETIC CONSERVATION; GENETIC VARIABILITY; GRANULE CELL; HUMAN; HUMAN CELL; KIDNEY CELL; NERVE CELL; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; RAT;

AMINO ACID SEQUENCE; ANIMALS; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; CELLS, CULTURED; CEREBELLUM; CONSERVED SEQUENCE; GLYCOGEN SYNTHASE KINASE 3; GREEN FLUORESCENT PROTEINS; HUMANS; MITOCHONDRIA; MOLECULAR SEQUENCE DATA; NERVE TISSUE PROTEINS; NEURONS; PHOSPHORYLATION; PROTEIN CONFORMATION; PROTEIN TRANSPORT; PROTO-ONCOGENE PROTEINS C-BCL-2; RATS; RATS, SPRAGUE-DAWLEY; RECOMBINANT FUSION PROTEINS; SERINE;

EID: 7744227096     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2057-04.2004     Document Type: Article

References (39)

1. Agarwal-Mawal A, Qureshi HY, Cafferty PW, Yuan Z, Han D, Lin R, Paudel HK (2003) 14-3-3 connects glycogen synthase kinase-3 beta to tau within a brain microtubule-associated tau phosphorylation complex. J Biol Chem 278:12722-12728.
2. Biondi RM, Nebreda AR (2003) Signalling specificity of Ser/Thr protein kinases through docking-site-mediated interactions. Biochem J 372:1-13.
3. Brunei A, Datta SR, Greenberg ME (2001) Transcription-dependent and -independent control of neuronal survival by the PI3K-Akt signaling pathway. Curr Opin Neurobiol 11:297-305.
4. Cregan SP, MacLaurin JG, Craig CG, Robertson GS, Nicholson DW, Park DS, Slack RS (1999) Bax-dependent caspase-3 activation is a key determinant in p53-induced apoptosis in neurons. J Neurosci 19:7860-7869.
5. D'Mello SR, Galli C, Ciotti T, 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 90:10989-10993.
6. Doble BW, Woodgett JR (2003) GSK-3: tricks of the trade for a multi-tasking kinase. J Cell Sci 116:1175-1186.
7. Fiol CJ, Mahrenholz AM, Wang Y, Roeske RW, Roach PJ (1987) Formation of protein kinase recognition sites by covalent modification of the substrate. Molecular mechanism for the synergistic action of casein kinase II and glycogen synthase kinase 3. J Biol Chem 262:14042-14048.
8. Fukunaga K, Miyamoto E (1998) Role of MAP kinase in neurons. Mol Neurobiol 16:79-95.
9. Gardai SJ, Hildeman DA, Frankel SK, Whitlock BB, Frasch SC, Borregaard N, Marrack P, Bratton DL, Henson PM (2004) Phosphorylation of Bax Ser184 by Akt regulates its activity and apoptosis in neutrophils. J Biol Chem 279:21085-21095.
10. Hart MJ, de los Santos R, Albert IN, Rubinfeld B, Polakis P (1998) Down-regulation of beta-catenin by human axin and its association with the APC tumor suppressor, beta-catenin and GSK3 beta. Curr Biol 8:573-581.
11. Hetman M, Cavanaugh JE, Kimelman D, Xia Z (2000) Role of glycogen synthase kinase-3β in neuronal apoptosis induced by trophic withdrawal. J Neurosci 20:2567-2574.
12. Hsu YT, Youle RJ (1997) Nonionic detergents induce dimerization among members of the Bcl-2 family. J Biol Chem 272:13829-13834.
13. Kaytor MD, Orr HT (2002) The GSK3 beta signaling cascade and neurodegenerative disease. Curr Opin Neurobiol 12:275-278.
14. Lawlor MA, Alessi DR (2001) PKB/Akt: a key mediator of cell proliferation, survival and insulin responses? J Cell Sci 114:2903-2910.
15. Li M, Wang X, Meintzer MK, Laessig T, Birnbaum MJ, Heidenreich KA (2000) Cyclic AMP promotes neuronal survival by phosphorylation of glycogen synthase kinase 3beta. Mol Cell Biol 20:9356-9363.
16. Linseman DA, Phelps RA, Bouchard RJ, Le SS, Laessig TA, McClure ML, Heidenreich KA (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.
17. Linseman DA, Cornejo BJ, Le SS, Meintzer MK, Laessig TA, Bouchard RJ, Heidenreich KA (2003) A myocyte enhancer factor 2D (MEF2D) kinase activated during neuronal apoptosis is a novel target inhibited by lithium. J Neurochem 85:1488-1499.
18. Mielke K, Herdegen T (2000) JNK and p38 stress kinases-degenerative effectors of signal-transduction-cascades in the nervous system. Prog Neurobiol 61:45-60.
19. Naerum L, Norskov-Lauritsen L, Olesen PH (2002) Scaffold hopping and optimization towards libraries of glycogen synthase kinase-3 inhibitors. Bioorg Med Chem Lett 12:1525-1528.
20. Nomura M, Shimizu S, Sugiyama T, Narita M, Ito T, Matsuda H, Tsujimoto Y (2003) 14-3-3 interacts directly with and negatively regulates proapoptotic Bax. J Biol Chem 278:2058-2065.
21. Oltvai ZN, Milliman CL, Korsmeyer SJ (1993) Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death. Cell 74:609-619.
22. Perez M, Rojo AI, Wandosell F, Diaz-Nido J, Avila J (2003) Prion peptide induces neuronal cell death through a pathway involving glycogen synthase kinase 3. Biochem J 372:129-136.
23. Phiel CJ, Wilson CA, Lee VM, Klein PS (2003) GSK-3alpha regulates production of Alzheimer's disease amyloid-beta peptides. Nature 423:435-439.
24. Plotkin B, Kaidanovich O, Talior I, Eldar-Finkelman H (2003) Insulin mimetic action of synthetic phosphorylated peptide inhibitors of glycogen synthase kinase-3. J Pharmacol Exp Ther 305:974-980.
25. Putcha GV, Deshmukh M, 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.
26. Putcha GV, Harris CA, Moulder KL, Easton RM, Thompson CB, 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.
27. Schinzel A, Kaufmann T, Schuler M, Martinalbo J, Grubb D, Borner C (2004) Conformational control of Bax localization and apoptotic activity by Pro168. J Cell Biol 164:1021-1032.
28. Schmitt E, Paquet C, Beauchemin M, Dever-Bertrand J, Bertrand R (2000) Characterization of Bax-sigma, a cell death-inducing isoform of Bax. Biochem Biophys Res Commun 270:868-879.
29. Selimi F, Vogel MW, Mariani J (2000) Bax inactivation in lurcher mutants rescues cerebellar granule cells but not purkinje cells or inferior olivary neurons. J Neurosci 20:5339-5345.
30. Somervaille TC, Linch DC, Khwaja A (2001) Growth factor withdrawal from primary human erythroid progenitors induces apoptosis through a pathway involving glycogen synthase kinase-3 and Bax. Blood 98:1374-1381.
31. Tsuruta F, Masuyama N, Gotoh Y (2002) The phosphatidylinositol 3-kinase (PI3K)-Akt pathway suppresses Bax translocation to mitochondria. J Biol Chem 277:14040-14047.
32. Vila M, Przedborski S (2003) Targeting programmed cell death in neurodegenerative diseases. Nat Rev Neurosci 4:365-375.
33. Vila M, Jackson-Lewis V, Vukosavic S, Djaldetti R, Liberatore G, Offen D, Korsmeyer SJ, 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.
34. Watcharasit P, Bijur GN, Song L, Zhu J, Chen X, Jope RS (2003) Glycogen synthase kinase-3beta (GSK3beta) binds to and promotes the actions of p53. J Biol Chem 278:48872-48879.
35. Wellmann H, Kaltschmidt B, Kaltschmidt C (1999) Optimized protocol for biolistic transfection of brain slices and dissociated cultured neurons with a hand-held gene gun. J Neurosci Methods 92:55-64.
36. Wolter KG, Hsu YT, Smith CL, Nechushtan A, Xi XG, Youle RJ (1997) Movement of Bax from the cytosol to mitochondria during apoptosis. J Cell Biol 139:1281-1292.
37. Yamaguchi H, Wang HG (2001) The protein kinase PKB/Akt regulates cell survival and apoptosis by inhibiting Bax conformational change. Oncogene 20:7779-7786.
38. Zong WX, Lindsten T, Ross AJ, MacGregor GR, Thompson CB (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.
39. Zou H, Li Y, Liu X, Wang X (1999) An APAF-1.cytochrome c multimeric complex is a functional apoptosome that activates procaspase-9. J Biol Chem 274:11549-11556.