c-Jun N-terminal kinases/c-Jun and p38 pathways cooperate in ceramide-induced neuronal apoptosis

Neuroscience

Volumn 119, Issue 2, 2003, Pages 387-397

  Willaime Morawek, S ^a,b   Brami Cherrier, K ^a,b   Mariani, J ^b   Caboche, J ^a   Brugg, B ^a,b  

^a Laboratoire Signalisation Neuronale et Regulation Genique (UMR 7102)   (France)

^b Lab Developpement/Vieillissement S   (France)

Author keywords

Neuronal death; Primary cultures; SAPK; Serum withdrawal

Indexed keywords

4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; CERAMIDE; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN C JUN; SYNAPTOPHYSIN;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANIMAL CELL CULTURE; APOPTOSIS; ARTICLE; BRAIN CELL; CELL ACTIVATION; CELL DEATH; CONTROLLED STUDY; FEMALE; GENETIC TRANSFECTION; IMMUNOCYTOCHEMISTRY; MITOSIS; MOUSE; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; SURVIVAL RATE; WESTERN BLOTTING;

EID: 0038400952     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(02)00996-X     Document Type: Article

References (55)

1. Altman F.P. Tetrazolium salts and formazans. Prog Histochem Cytochem. 9:1976;1-56.
2. Angel P., Hattori K., Smeal T., Karin M. The jun proto-oncogene is positively autoregulated by its product, Jun/AP-1. Cell. 55:1988;875-885.
3. Behrens A., Sibilia M., Wagner E.F. Amino-terminal phosphorylation of c-Jun regulates stress-induced apoptosis and cellular proliferation. Nat Genet. 21:1999;326-329.
4. Bielawska A., Crane H.M., Liotta D., Obeid L.M., Hannun Y.A. Selectivity of ceramide-mediated biology lack of activity of erythro-dihydroceramide . J Biol Chem. 268:1993;26226-26232.
5. Bose R., Verheij M., Haimovitz-Friedman A., Scotto K., Fuks Z., Kolesnick R. Ceramide synthase mediates daunorubicin-induced apoptosis an alternative mechanism for generating death signals . Cell. 82:1995;405-414.
6. Brenner B., Koppenhoefer U., Weinstock C., Linderkamp O., Lang F., Gulbins E. Fas- or ceramide-induced apoptosis is mediated by a Rac1-regulated activation of Jun N-terminal kinase/p38 kinases and GADD153. J Biol Chem. 272:1997;22173-22181.
7. Brugg B., Michel P.P., Agid Y., Ruberg M. Ceramide induces apoptosis in cultured mesencephalic neurons. J Neurochem. 66:1996;733-739.
8. Chen Z., Seimiya H., Naito M., Mashima T., Kizaki A., Dan S., Imaizumi M., Ichijo H., Miyazono K., Tsuruo T. ASK1 mediates apoptotic cell death induced by genotoxic stress. Oncogene. 18:1999;173-180.
9. Coffey E.T., Hongisto V., Dickens M., Davis R.J., Courtney M.J. Dual roles for c-Jun N-terminal kinase in developmental and stress responses in cerebellar granule neurons. J Neurosci. 20:2000;7602-7613.
10. Coffey E.T., Smiciene G., Hongisto V., Cao J., Brecht S., Herdegen T., Courtney M.J. 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. 22:2002;4335-4345.
11. Crocker S.J., Lamba W.R., Smith P.D., Callaghan S.M., Slack R.S., Anisman H., Park D.S. c-Jun mediates axotomy-induced dopamine neuron death in vivo. Proc Natl Acad Sci USA. 98:2001;13385-13390.
12. Davis R.J. Signal transduction by the JNK group of MAP kinases. Cell. 103:2000;239-252.
13. Estus S., Zaks W.J., Freeman R.S., Gruda M., Bravo R., Johnson E.M. Jr. Altered gene expression in neurons during programmed cell death identification of c-jun as necessary for neuronal apoptosis . J Cell Biol. 127:1994;1717-1727.
14. France-Lanord V., Brugg B., Michel P.P., Agid Y., Ruberg M. Mitochondrial free radical signal in ceramide-dependent apoptosis a putative mechanism for neuronal death in Parkinson's disease . J Neurochem. 69:1997;1612-1621.
15. Ghatan S., Larner S., Kinoshita Y., Hetman M., Patel L., Xia Z., Youle R.J., Morrison R.S. p38 MAP kinase mediates bax translocation in nitric oxide-induced apoptosis in neurons. J Cell Biol. 150:2000;335-347.
16. Gupta S., Barrett T., Whitmarsh A.J., Cavanagh J., Sluss H.K., Derijard B., Davis R.J. Selective interaction of JNK protein kinase isoforms with transcription factors. EMBO J. 15:1996;2760-2770.
17. Ham J., Babij C., Whitfield J., Pfarr C.M., Lallemand D., Yaniv M., Rubin L.L. A c-Jun dominant negative mutant protects sympathetic neurons against programmed cell death. Neuron. 14:1995;927-939.
18. Ham J., Eilers A., Whitfield J., Neame S.J., Shah B. c-Jun and the transcriptional control of neuronal apoptosis. Biochem Pharmacol. 60:2000;1015-1021.
19. Hartfield P.J., Mayne G.C., Murray A.W. Ceramide induces apoptosis in PC12 cells. FEBS Lett. 401:1997;148-152.
20. Herdegen T., Claret F.X., Kallunki T., Martin-Villalba A., Winter C., Hunter T., Karin M. Lasting N-terminal phosphorylation of c-Jun and activation of c-Jun N- terminal kinases after neuronal injury. J Neurosci. 18:1998;5124-5135.
21. Herdegen T., Skene P., Bahr M. The c-Jun transcription factor bipotential mediator of neuronal death, survival and regeneration . Trends Neurosci. 20:1997;227-231.
22. Hunot S., Brugg B., Ricard D., Michel P.P., Muriel M.P., Ruberg M., Faucheux B.A., Agid Y., Hirsch E.C. Nuclear translocation of NF-kappaB is increased in dopaminergic neurons of patients with parkinson disease. Proc Natl Acad Sci USA. 94:1997;7531-7536.
23. Jaffrezou J.P., Maestre N., de Mas-Mansat V., Bezombes C., Levade T., Laurent G. Positive feedback control of neutral sphingomyelinase activity by ceramide. FASEB J. 12:1998;999-1006.
24. Kawamoto J.C., Barrett J.N. Cryopreservation of primary neurons for tissue culture. Brain Res. 384:1986;84-93.
25. Knusel B., Michel P.P., Schwaber J.S., Hefti F. Selective and nonselective stimulation of central cholinergic and dopaminergic development in vitro by nerve growth factor, basic fibroblast growth factor, epidermal growth factor, insulin and the insulin-like growth factors I and II. J Neurosci. 10:1990;558-570.
26. Kronke M. The mode of ceramide action the alkyl chain protrusion model . Cytokine Growth Factor Rev. 8:1997;103-107.
27. Lambeng N., Michel P.P., Brugg B., Agid Y., Ruberg M. Mechanisms of apoptosis in PC12 cells irreversibly differentiated with nerve growth factor and cyclic AMP. Brain Res. 821:1999;60-68.
28. Lambeng N., Willaime-Morawek S., Mariani J., Ruberg M., Brugg B. Activation of mitogen-activated protein kinase pathways during the death of PC12 cells is dependent on the state of differentiation. Mol Brain Res. 111:2003;52-60.
29. Le-Niculescu H., Bonfoco E., Kasuya Y., Claret F.X., Green D.R., Karin M. Withdrawal of survival factors results in activation of the JNK pathway in neuronal cells leading to Fas ligand induction and cell death. Mol Cell Biol. 19:1999;751-763.
30. Lozano J., Menendez S., Morales A., Ehleiter D., Liao W.C., Wagman R., Haimovitz-Friedman A., Fuks Z., Kolesnick R. Cell autonomous apoptosis defects in acid sphingomyelinase knockout fibroblasts. J Biol Chem. 276:2001;442-448.
31. Manthey C.L., Wang S.W., Kinney S.D., Yao Z. SB202190, a selective inhibitor of p38 mitogen-activated protein kinase, is a powerful regulator of LPS-induced mRNAs in monocytes. J Leukoc Biol. 64:1998;409-417.
32. Maroney A.C., Finn J.P., Connors T.J., Durkin J.T., Angeles T., Gessner G., Xu Z., Meyer S.L., Savage M.J., Greene L.A., Scott R.W., Vaught J.L. Cep-1347 (KT7515), a semisynthetic inhibitor of the mixed lineage kinase family. J Biol Chem. 276:2001;25302-25308.
33. Mathias S., Pena L.A., Kolesnick R.N. Signal transduction of stress via ceramide. Biochem J. 335:1998;465-480.
34. Mielke K., Herdegen T. JNK and p38 stress kinases degenerative effectors of signal- transduction-cascades in the nervous system . Prog Neurobiol. 61:2000;45-60.
35. Mitoma J., Ito M., Furuya S., Hirabayashi Y. Bipotential roles of ceramide in the growth of hippocampal neurons promotion of cell survival and dendritic outgrowth in dose- and developmental stage-dependent manners . J Neurosci Res. 51:1998;712-722.
36. Mizukami Y., Yoshioka K., Morimoto S., Yoshida K. A novel mechanism of JNK1 activation: nuclear translocation and activation of JNK1 during ischemia and reperfusion. J Biol Chem. 272:1997;16657-16662.
37. Morishima Y., Gotoh Y., Zieg J., Barrett T., Takano H., Flavell R., Davis R.J., Shirasaki Y., Greenberg M.E. Beta-amyloid induces neuronal apoptosis via a mechanism that involves the c-Jun N-terminal kinase pathway and the induction of Fas ligand. J Neurosci. 21:2001;7551-7560.
38. Nakane M., Kubota M., Nakagomi T., Tamura A., Hisaki H., Shimasaki H., Ueta N. Lethal forebrain ischemia stimulates sphingomyelin hydrolysis and ceramide generation in the gerbil hippocampus. Neurosci Lett. 296:2000;89-92.
39. Namgung U., Xia Z. Arsenite-induced apoptosis in cortical neurons is mediated by c-Jun N- terminal protein kinase 3 and p38 mitogen-activated protein kinase. J Neurosci. 20:2000;6442-6451.
40. Obeid L.M., Linardic C.M., Karolak L.A., Hannun Y.A. Programmed cell death induced by ceramide. Science. 259:1993;1769-1771.
41. 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.
42. Santana P., Pena L.A., Haimovitz-Friedman A., Martin S., Green D., McLoughlin M., Cordon-Cardo C., Schuchman E.H., Fuks Z., Kolesnick R. Acid sphingomyelinase-deficient human lymphoblasts and mice are defective in radiation-induced apoptosis. Cell. 86:1996;189-199.
43. Schirakabe K., Yamaguchi K., Shibuya H., Irie K., Matsuda S., Moriguchi T., Gotoh Y., Matsumoto K., Nishida E. TAK1 mediates the ceramide signaling to stress activated potein kinase/c-Jun N-terminal kinase. J Biol Chem. 272:1997;8141-8144.
44. Slater T.F., Sawyer B., Sträuli U. Studies on succinate-tetrazolium reductase systems. Biochim Biophys Acta. 77:1963;383-393.
45. Spence M.W., Burgess J.K. Acid and neutral sphingomyelinases of rat brain activity in developing brain and regional distribution in adult brain . J Neurochem. 30:1978;917-919.
46. Takekawa M., Posas F., Saito H. A human homolog of the yeast Ssk2/Ssk22 MAP kinase kinase kinases, MTK1, mediates stress-induced activation of the p38 and JNK pathways. EMBO J. 16:1997;4973-4982.
47. Van Veldhoven P.P., Matthews T.J., Bolognesi D.P., Bell R.M. Changes in bioactive lipids, alkylacylglycerol and ceramide, occur in HIV-infected cells. Biochem Biophys Res Commun. 187:1992;209-216.
48. Watson A., Eilers A., Lallemand D., Kyriakis J., Rubin L.L., Ham J. Phosphorylation of c-Jun is necessary for apoptosis induced by survival signal withdrawal in cerebellar granule neurons. J Neurosci. 18:1998;751-762.
49. 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.
50. Willaime S., Vanhoutte P., Caboche J., Lemaigre-Dubreuil Y., Mariani J., Brugg B. Ceramide-induced apoptosis in cortical neurons is mediated by an increase in p38 phosphorylation and not by the decrease in ERK phosphorylation. Eur J Neurosci. 13:2001;2037-2046.
51. Xia Z., Dickens M., Raingeaud J., Davis R.J., Greenberg M.E. Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis. Science. 270:1995;1326-1331.
52. Zhang J., Gao J.X., Salojin K., Shao Q., Grattan M., Meagher C., Laird D.W., Delovitch T.L. Regulation of fas ligand expression during activation-induced cell death in T cells by p38 mitogen-activated protein kinase and c-Jun NH2-terminal kinase. J Exp Med. 191:2000;1017-1030.
53. Zhang Y., Zhou L., Miller C.A. A splicing variant of a death domain protein that is regulated by a mitogen-activated kinase is a substrate for c-Jun N-terminal kinase in the human central nervous system. Proc Natl Acad Sci USA. 95:1998;2586-2591.
54. Zhu X., Raina A.K., Rottkamp C.A., Aliev G., Perry G., Boux H., Smith M.A. Activation and redistribution of c-Jun N-terminal kinase/stress activated protein kinase in degenerating neurons in Alzheimer's disease. J Neurochem. 76:2001;435-441.
55. Zhuang S., Demirs J.T., Kochevar I.E. p38 Mitogen-activated protein kinase mediates Bid cleavage, mitochondrial dysfunction, and caspase-3 activation during apoptosis induced by singlet oxygen, but not by hydrogen peroxide. J Biol Chem. 275:2000;25939-25948.